Advances in Plant Pathology, Volume 11 (Advances in Plant Pathology)

Advances in

Plant Pathology Volume 11

EDITORIAL BOARD Michael J. Daniels

The Sainsbury Laboratory, Norwich, UK Richard I. Hamilton

Agriculture Canada Research Station, Vancouver, Canada David S. Ingram

Royal Botanic Garden, Edinburgh, UK Paul H. Williams

University of Wisconsin-Madison, USA

Advances in

Plant Pathology series edited by

j . H . Andrews

I.C. Tommerup

Department of Plant Pathology The University of Wisconsin Jvladison, Wisconsin USA

and

Volume 11

ACADEMIC PRESS Harcourt Brace & Company, Publishers London San Diego New York Sydney Tokyo Toronto

Boston

CSIRO Laboratoryfor Rural Research Wembley, Western Australia Australia

ACADEMIC PRESS LIMITED 24/28 Oval Road, London NW1 7DX

United States Edition published by ACADEMIC PRESS INC. San Diego, CA 92101 This book is printed on acid free paper Copyright 9 1995 by Academic Press Limited

All Rights Reserved No part of this book may be reproduced in any form by photostat, microfilm, or any other means, without written permission from the publishers

A catalogue record for this book is available from the British Library ISBN 0-12-033711-8

Typeset by Colset Private Ltd, Singapore Printed and Bound in Great Britain by T.J. Press (Padstow) Ltd, Padstow, Cornwall

Contents

Contributors Preface 1. The Concept of Agricultural Sustainability A. Hamblin

vii ix 1

2. Prehistoric Agricultural Methods as Models for Sustainability W. M. Denevan

21

3. Sustainable Agriculture: An Agroecological Perspective S. R. Gliessman

45

4. Developing Biofertilizer and Biocontrol Agents that Meet Farmers' Expectations M. E. Leggett and S. C. Gleddie

59

5. Pathogens' Responses to the Management of Disease Resistance Genes J. K. M. Brown

75

6. Three Sources for Non-chemical Management of Plant Disease: Towards an Ecological Framework A. P. Maloney

103

7. Classical Biological Control of Plant Pathogens J. K. Scott

131

8. Economic Thresholds and Nematode Management R. McSorley and L. W. Duncan

147

9. Evaluation of Micro-organisms for Biocontrol: Botrytis cinerea and Strawberry, a Case Study J . C . Sutton

173

I0. Biodiversity and Biocontrol: Lessons from Insect Pest Management M.A. Altieri

191

1 I. Plant Protection Using Natural Defence Systems of Plants B.J. Deverall

211

12. The Role of Soil Microbiology in Sustainable Intensive Agriculture C. E. Panldaurst and J. M. Lynch

229

vi

Contents

13. World Integrated Pathogen and Pest Management and Sustainable Agriculture in the Developing World J . W . Bentley, J. Castafio-Zapata and K. L. Andrews

249

14. The Diversity of Fungi Associated with Vascular Plants: the Known, the Unknown and the Need to Bridge the Knowledge Gap P. F. Cannon and D. L. Hawksworth

277

15. Adventures of a Rose Pathologist C. Harwood

303

Index

317

Contributors

M.A. ALTIERI, Division of Biological Control, University of California at Berkeley, Berkeley CA 94 720, USA K. L. ANDREWS, Escuela Agricola Panamericana, Apartado Postal 93, Tegucigalpa, Honduras j . w . BENTLEY, CasiUa 1663, Cochabamba, Bolivia. j. K. M. BROWN, John Innes Research Institute, Norwich Research, Colney, Norwich

NR4 7UH, UK P. F. CANNON, International Mycological Research Institute, Bakenham Lane, Egham, Surrey TW20 9TY, UK

J. CASTANO-ZAPATA, Escuela Agricola Panamericana, Apartado Postal 93, Tegucigalpa, Honduras W. M. DENEVAN, Department of Geography, 455 Science Hall, University of Wisconsin, Madison 53706, USA B.J. DEVERALL, Department of Crop Sciences, The University of Sydney, N S W 2006, Australia LARRY DUNCAN, Citrus Research and Education Center, 700 Experiment Station Road, Lake Alfred, Florida 33850, USA S. C. GLEDDIE, PhilomBios, #318-111 Research Drive, Innovation Place, Saskatoon SASK S7N 3R2, Canada S. R. GLIESSMAN, AgroecologicalProgram, University of California Santa Cruz, Santa

Cruz, CA 95064, USA

A. HAMBLIN, Bureau of Resource Sciences, PO Box Ell, Queen Victoria Terrace, Canberra, ACT 2600, Australia C. H A R W O O D , Bear Creek Gardens Inc., P.O. Box 9100, Medford, Oregon 97501,

USA

viii

Contributors

D.L. HAWKSWORTH, International Mycological Research Institute, Bakenham Lane, Egham, Surrey TW20 9TY, UK M. E. LEGGETT, PhilomBios, #318-111 ResearchDrive, Innovation Place, Saskatoon, SASK S7N 3R2, Canada j. M. LYNCH, Horticultural Research Institute, Worthing Road, Littlehampton, West Sussex BN17 6LP, UK

A.P. MALONEY, Department of Plant Pathology, CorneU University, Ithaca N Y 14853, USA R. McSORLEY, Department of Entomology aria Nematology, University of Florida, PO Box 110620, GainesviUe, Florida 32611 0620, USA C. E. PANKHURST, CSIRO Division of Soils, Private Bag No 2, Glen Osmond 5064, Australia j . K . SCOTT, CSIRO Division of Entomology, Private Bag, PO Wembley 6014, Australia j . c . SUTTON, Department of Environmental Biology, Ontario Agricultural College, University ojc Guelph, Guelph, Ontario N1G 2W1, Canada

Preface

The series Advances in Plant Pathology publishes articles on issues of current or future interest and importance in plant pathology. Since its initiation one decade ago, the hallmark of Advances in Plant Pathology has been that the articles are essentially essays rather than merely reviews. The emphasis on ideas, together with flexibility of format, length and content will continue. Our goal is both to draw insights and concepts from relevant disciplines into the realm of plant pathology and to reveal the general biological principles of plant pathology to the broad audience of biologists. Thus, thought-provoking articles ranging from a very basic to an applied focus on a wide variety of topics will continue to be written for diverse readers, including undergraduate and postgraduate students, researchers and teachers. While most volumes will have no particular theme, others, such as the recent volume on mycorrhiza, will treat a particular subject in depth. Controversial viewpoints will be encouraged. Articles that are fundamentally editorial in scope will be included periodically in the series. We want to serve the interests of all plant pathologists and welcome suggestions for specific articles or future volumes in the series. These comments or ideas should be sent to John Andrews, Department of Plant Pathology, 1630 Linden Drive, University of Wisconsin, Madison, WI 53706, USA (Fax 608-263-2626). Madison, Wisconsin, USA & Perth, WA, Australia, 1994

j . H. Andrews & I. C. Tommerup

This Page Intentionally Left Blank

THE CONCEPT OF AGRICULTURAL SUSTAINABILITY Ann Hamblin

Bureau of Resource Sciences, PO Box Ell, Queen Victoria Terrace, Canberra, A C T 2600, Australia (current addressfor correspondence: Cooperative Research Centrefor Soil & Land Management, Private Bag 2, Glen Osmond 5066, Australia).

I. Introduction II. Attributes of Sustainable Agriculture III. Agricultural Sustainability: a Realistic Concept for High Productivity Farming? IV. Integrating Ecological and Economic Aspects of Plant Disease Control in Sustainable Agriculture V. High Production Versus Low Production Environments and Farming Systems VI. Conclusions References

1 4 7 13 !5 16 17

I. I N T R O D U C T I O N The word sustainability does not appear in most English language dictionaries. It is a word of the late twentieth century; an abstract concept coined from a verb meaning to support, endure or maintain for a prolonged period. It has, however, come into common usage as a broad ethical concept, implying moral choices relating to the use and distribution of material goods within and between societies, both present and future (Pearce et al., 1988). Long-expressed concerns over the effects of indefinite material growth and the need for balanced development (Daly, 1988) were given a special focus by the World Commission on Environment and Development (WECD) report 'Our Common Future' (1987). This focused public attention on the nexus between poverty, population growth and environmental deterioration. The report proposed a solution based on 'sustainable development'. The Commission's thesis was that it is possible to meet the needs of present populations without compromising future generations' needs by limiting the exploitation of natural resources through effective management and social organization. Economic growth is essential for poor countries, but the present solution of providing this through natural resource exploitation is unsustainable. These propositions require hard decisions and changes in the distribution of wealth, and organization of goods and trade, between rich and poor countries, and within rich countries. ADVANCES IN P L A N T P A T H O L O G Y - - V O L . 11 ISBN 0-12-033711-8

Copyright 9 1995 Academic Press Limited All rights of reproduction in any form reserved

2

A. Hamblin

The thinking embodied in ' O u r Common Future' is not new, but it presents strong challenges to the neoclassical economic stance that natural resources are an infinite good, which do not require intrinsic valuation. It also challenges the assumption that optimization of wealth distribution occurs most readily through competition. If it were actually possible to have totally free trade and markets this might be the case, but in the current world situation the frequency of market failure (lack of monetary value for things that are greatly valued by the community) is so common that alternative methods of resource preservation have to be found. While many environmentalists would like to see more regulation to achieve this, the most effective long-term solution is for people to decide that they want to preserve, and give them the means to do that. Education, democratization through communication networks, and access to alternative economic opportunities may be some of the alternatives that bring progressive, permanent improvement. In recent years there has been a plethora of publications on what constitutes sustainable agriculture. Many western governments have espoused the term (e.g. Science Council of Canada, 1991; Australian Agricultural Council, 1991), but the notion of what sustainable agriculture means at national level varies from country to country, culture to culture. While northern hemisphere industrial countries place substantial emphasis on the preservation of rural landscapes and wildlife habitats in their definitions of sustainable agriculture (OECD, 1992) the principal goals of the developing world are to alleviate rural poverty and provide long-term production security (World Bank, 1992). Sustainable agriculture is discussed substantially in terms of land management, agricultural policy, pesticide reduction programmes, at the level of general goals, rather than at the specific level of mechanisms for widespread implementation. The implications for plant pathologists, agronomists and other agricultural scientists are that great expectations are placed on increased use of various biological control strategies for pest management. The concept of sustainable development also implies that reducing the dependence on pesticides should not be at the expense of desired levels of food production and farm viability. The conservation of biodiversity has also become a significant international goal, with the development of the International Convention on Biodiversity (1992) as part of the United Nations Conference on Environment and Development (1992). However, conservation of biodiversity in sustainable agriculture is still at best a hazily articulated concept (Sandlund et al., 1992), as what constitutes biodiversity varies with the type of life form, the scale of the organisms and environment, and the extent of knowledge about the biota in question. For example, with animal organisms, from plankton to whales, abundance of organisms appears related to body size (Damuth, 1987). In plant species, isozyme surveys of genetic material have shown about 80% of molecular diversity of the species occurs in any one population; however, Brown and Schoen (1992) argue that this does not imply redundancy in the majority of populations as abundance of plant genetic diversity also depends on the mating

The Concept of Agricultural Sustainability

3

system of the plant category, the pattern of species heterozygosity, and the spatial demography of the germplasm. Even greater complexity may surround the estimation of microbial biodiversity, because of shear lack of taxonomic knowledge, as well as such microbial attributes as lack of mobility, and functional coevolution with plants which additionally affect rates of genetic change (Holdgate, 1991). Wilson (1988) for example, estimated the total number of species of bacteria worldwide to be no more than 3600, compared with 46 983 species of fungi (a remarkably precise figure surely?), whereas Erwin (1982) has speculated that there may be up to 30 million species of insects unreported in tropical environments, compared with the 750 000 so far recorded, and May (1988) prudently cautioned against such simplistic number-counting by demonstrating how dependent estimates were upon base assumptions of host-specificity and habitat characterization. Conservation of biodiversity for sustainable agriculture is often translated to mean the conservation of the genetic resources of domesticated species and their progenitors, in which context it has long been actively promoted by FAO (Food and Agriculture Organization), the Consultative Group on International Agricultural Research (CGIAR) and the International Plant Genetic Resources Institute (IPGRI), particularly for plant species. Habitat conservation and in situ genetic resource conservation are less well catered for in most countries, or internationally. Yet the significance of such conservation cannot be over emphasized in relation to the future success of biological control programmes that are dependent on utilization of natural predators of exogenous pests, weeds and vectorborne diseases. Well-known examples of successful biocontrol are frequent in Australia, where the relatively recent introduction of alien pests has often been sufficiently well documented to enable location of predators from the region of origin to be identified, introduced and established. A formal system of identification, preconditioning, quarantine, testing and controlled release exists in Australia for biological control organisms, both for control of insect and other invertebrate pests (mainly in horticultural and animal production systems) and for weed control, particularly in aquatic parks and reserves, and remote or inaccessible environments where other forms of control are unsuitable or impossible (Corey et al., 1993). Biological control of weed species through the introduction of herbivorous predatory insects and fungal pathogens from the centres of origin has been successful in a number of cases, as in control of prickly pear, blackberry, and skeleton weed, and Cullen (1993) documented 35 other species which are currently being investigated for biological control measures. However, the success rate is relatively low in cases where the original ecosystems have deteriorated, or where the pest species is introduced into a different climatic environment and pest-pathogen life cycles become non-synchronous (see also Scott, Chapter 7, this volume). Today, many of the South African, Middle Eastern, and South American environments which have yielded the pathogens and predators of these Australian aliens are increasingly genetically eroded, making the chances of success for

4

A. Hamblin

control of current or future pathogens and pests either lower or more costly. Similarly in north America some 50-80 % of pathogens are estimated to be alien, the majority from Europe. In the United States the loss to food and fibre crops from insect pests has been estimated at 13 %, and total pathogen, pest and weed losses of the order of 37 % of production - all in a country which strives to maintain low pathogen and pest levels through widespread use of pesticides and cultural practices (Pimentel etal., 1991). Ironically, however, Pimentel (1993) considered that this dependence on pesticides for pathogen control has led to a doubling of the crop losses (from 7 to 13% attributable to insect pests for example) between 1945 and 1991, because of the abandonment of traditional forms of crop protection, such as wide rotations, integration of animal and plant production systems on farm, and narrowing of the genetic pool in monocultured crop varieties. Biological control has not been used as a main-line strategy, compared with the investment in resistance breeding (and more recently genetic manipulation of the host for herbicide resistance) and in increasingly selective pesticides. The implications of loss or threats to native habitats have been only cursorily considered at the political and scientific policy level in relation to such environmentally benign agricultural strategies as resistance breeding, biological control of soft-borne pathogens and plant-symbiont nutrition. An opportunity currently exists, however, with the International Convention on Biodiversity (1992) which the majority of developed countries have ratified, to advocate for the restricted use of pesticides in, and preservation of, agricultural regions in close proximity to biomes known to contain progenitors and land-races of agricultural plant species. Such advocacy will be dependent on the specialized knowledge of plant pathologists, breeders and agronomists being presented into the arena of international conventions and politics. Professional societies and Academies have an important role in advocating such policies to national governments.

II. ATTRIBUTES OF SUSTAINABLE AGRICULTURE Despite the differences in national interpretation of sustainable agriculture, there is substantial agreement among agricultural scientists, ecologists and economists on the properties of sustainable agricultural system - sometimes termed agroecosystems. Ecological concepts of resilience and diversity have been incorporated into the characterization of such systems (Holling, 1973). Conway (1985), Marten (1988) and others have distinguished the attributes of productivity, stability, sustainability and equitability in such traditional agroecosystems as the village-garden agriculture of Indonesia, in which sustainability is associated with the ability to maintain production over long time periods, relative to human life. These systems are resilient in that they recover from stresses (such as seasonal droughts or insect pests) and from major perturbations (such as climatic fluctuations or wars), as shown in Fig. 1. Systems based in environments of low intrinsic fertility (old,

The Concept of Agricultural Sustainability

5

Productivity

Yield

High

Time r

Stability

Yield Low

High

Time Sustainability With Stress

l Yield

Low

W-V High

y

Time Sustainability With Perturbation

Yield High Time Fig. 1. Definitions of high (day) and low (night) levels of productivity, stability, sustainability with stress (~) on sustainability with perturbation (+) adapted from Conway (1985).

6

A. Hamblin

weathered soils, arid zones), which have low potential productivity, may also often have low stability of production because of the erratic nature of the rainfall or erosivity of the soils, as in most of the semi-arid tropics and subtropics. Such systems are inherently less resilient to exogenous stresses than those in environments of high intrinsic fertility (postglacial and alluvial softs) and high climatic stability (e.g. cool and warm temperate climates with low rainfall variability). However, all ecosystems can be pressured beyond their limits if their traditional, sustainable farming practices are intensified, either by shortening the time between biological stresses (as has been the case in the decrease from 20 years to 5 or fewer years between clearing events in tropical forests traditionally used for shifting agriculture, as population pressure increases) or by increasing the loading of inputs into the system within a given period (as in the case of nitrate loading in European cereal production). In high input agricultural systems, typical of the developed world and irrigated regions, strategies for reducing the use of pesticides and inorganic fertilizers have become central to most discussions on sustainable agriculture, as evidence of the adverse environmental, human health and trading effects of the increasing use of these agricultural chemicals accumulates (OECD, 1992). In low-input systems, typical of non-irrigated agriculture in the developing world, lack of fertilizer, overgrazing, and vegetation clearance from population pressure, are the symptoms of unsustainability most frequently identified (FAO, 1989). In both these end-members of the full range of global farming systems, solutions to inadequate farming practices are sought in the greater use of rotations for weed control and crop health, continued reliance on both conventional plant breeding and genetic engineering for pest and disease control, residue retention and minimum tillage for organic matter build-up, and the interspersing of agroforestry with conventional cropping or pastures. All solutions appear to place heavy reliance on farmers and scientists having a good understanding of both biology and economics of the production system, and being capable of managing plant health and nutrition by the relatively sophisticated and complex regimes of integrated pest management, biological control and appropriate rotational agronomy. In a number of European countries national policies have recently been developed to gradually reduce the use of agricultural pesticides, improve their efficacy and regulate their application. Sweden, Denmark and the Netherlands have now embarked on such programmes of agricultural chemical reduction (Hurst, 1992). This is expected to provoke other agricultural exporting countries into similar action because of the advantage which low pesticide users can command in trade. Non-commercial barriers may be erected in the same way in which unilateral banning of older generations of pesticides has operated in favour of those countries which remove declared pesticides from use. However, reduction in overall levels of pesticide use requires wide consensus from all sectors, including producers, chemical compa~nies, government agencies, and research and development organizations. In the Netherlands, reducing the dependence on soil sterilants and

The Concept of Agricultural Sustainability

7

pesticides in the production of lucrative, export-quality bulb, tuber and root crops, to which nearly 9 million kilograms of pesticides are applied per year (Zadoks, 1993), requires major change to farming practice, legislation and monitoring, and to research directions. It may also result in lower production in a sector of the economy responsible for a large proportion of export earnings. While Rabbinge (1991) estimated that the European Community as a whole could reduce its cultivated area by 60 % and its pesticide used by 80 % and still feed itself comfortably, without producing vast surpluses of subsidized commodities that distort world trade, the political will to change is still to come, and with it the scientific support to help producers transform their systems without large production and economic loss. For nearly all systems of agricultural production which are now dependent to some degree or other on control of weeds, pests and diseases by chemical pesticides, such reduction programmes will require a high level of information, education and co-operation between producers and agricultural servicing institutions. In some farming environments, however, the increasing prevalence of pesticide resistance in weed species (Powles and Matthews, 1992), and in pests such as Helicoverpaarmiga (Forrester, 1990) may threaten long-term capacity to produce certain types of crops at an economic rate of return.

III. AGRICULTURAL SUSTAINABILITY: A REALISTIC CONCEPT FOR HIGH PRODUCTIVITY FARMING? In the 1960-1980s the successes of the cereal breeding programmes associated with the 'Green Revolution' led to the consensus among agronomists that potential yield set by radiation and temperature was the realistic target for field production, with the progressive removal of abiotic and biotic stresses, the former through inputs of irrigation, fertilizers and pest-controlling chemicals, the latter through continued refining of the plant canopy by breeding (MAFF, 1978; CIMMYT, 1989). In addition, in North America and western Europe producer subsidy protection over the period 1975-1990 was equivalent to 25-55 %, compared with an average of 10-15 % in Australia for example (OECD, 1980-1990). This has encouraged inefficient, high use of inputs above the effective rate of return. The result has been extraordinarily large and continued increases in biological productivity, that is, expressed as yields (kg ha-1 year-1), but not necessarily in economic productivity (ratio of all outputs to inputs expressed in $). The amount of nitrogen fertilizer required to produce a tonne of wheat in the UK is 6.5 times that used in Australia, for example, but the average profit margin per tonne is little different. Other striking differences between increases in productivity and inputs of fertilizer and pesticides which show the differences between developing and industrial countries are shown in Table I, where we can see an example of the marginal rate of return for increased application of pesticide, by comparing the Netherlands, France and the UK. 'Low input' countries such as Australia and

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Table I. Kilograms of N, P, and K fertilizer, and active pesticide used per hectare of crop land for selected countries compared with yields and yield increase in cereals. ,,

Country India Pakistan Argentina United Kingdom The Netherlands France USA Australia

hak~_~NPK applied (1987-1990)

kg active ingredient ha-1 ( 1 9 8 2 - 1 9 8 5 )

% Increase in cereals 1979-1989

Average cereal yield: kg ha-1 1988-1990

62 85 5 359 662 405 95 26

0.30 0.09 0.40 5.07 10.35 5.16 1.97 0.75

42 27 16 5 19 31 6 17

1865 1745 2262 5792 6681 6101 4341 1650

Source: Food and Agriculture Organization of the United Nations (several years) and World Resources Institute (1992).

Argentina still have sufficient difference in intrinsic fertility that this is reflected in their relative yields. Although these are gross averages across many different crops and production environments, the heavy reliance on pesticides and fertilizers in western Europe is particularly noticeable. The economic consequences of subsidized production in high-income countries is now recognized to be causing severe distortion to world prices of agricultural commodities, with increasingly adverse environmental consequences in the countries of production, while failing to halt the declining terms of trade experienced by commercial farmers in those countries. The revised Common Agricultural Policy (European Community, 1992), and the so-called Blair House agreement of the General Agreement on Tariffs and Trade (GATT), linalized in December 1993, both seek to reign back the extent and intensity of agricultural production in the northern industrial countries through progressive reduction in subsidies and removing some land from agricultural production. The impact of both on farming practice may be small unless they are accompanied by an objective rethinking of the production environment by nutritionists, agronomists and pathologists. Such innovation is necessary to utilize the principle of biological diversification more effectively so that the identified advantages of mixtures of varieties, wider rotations, mosaics of biotypes within fields, companion species, predator refuges and conservation strips, as for example described by Strange (1993), can be implemented on a much wider scale in commercial agriculture. The introduction of alternative, minor crops and pasture plants such as legumes, which are constituents of nutritionally sustainable systems, and provide alternative income sources, have notoriously high disease and pest susceptibility, particularly where hosts (often with accompanying pathogens) are introduced into new environments (Allen, 1983). Allen points out that traditional farming systems (in Latin America and Africa) which use companion cropping of legume-cereals (such as

The Concept of Agricultural Sustainability

9

maize/cowpea, or maize/15'ean) nearly always have lower incidence and severity of leaf fungal pathogens than where the same crops are grown as single, more densely planted stands, even within the same environment. Current attempts on the part of agronomists to reverse the 'monoculture-intensification' trend of the past two decades pose significant challenge to plant pathologists. As epidemiologists and geneticists have frequently pointed out, domesticated species are often most susceptible to their normally endemic (co-evolved) pathogens when introduced into new environments. Harlan (1976) cited such classic cases of rust epidemics in maize after its introduction from Mexico into Africa, coffee rust in the New World and Panama disease of banana, as examples of this type of disruption of the normal host-pathogen fitness and virulence levels. He pointed out that the 'virtual carpet' of wheat from northern Canada to Argentina, and of rice from Korea to Indonesia and India, had put an unprecedented pressure on conventional breeding strategies, given the narrowness of the genetic base and the lack of co-evolution of these cereals' major pathogens that is now occurring. Where grain, shrub and pasture legumes are introduced into such cropping systems to improve stability and diversification, the new introductions are frequently beset by almost epidemic attacks of their otherwise endemic fungal or viral pathogens (Allen, 1983). Another practical problem for pathologists charged with protecting the production of minor crops is that investment in their resistance breeding is small relative to that devoted to cereals, both internationally (Consultative Group on International Agricultural Research, 1992) and at national level in many instances (Clements etal., 1992). Support for biocontrol agents capable of suppressing major fungal pathogens in woody and perennial species, such as Phytophthora cinnamoni for example, which attacks some 200 tree crop species worldwide is a similar area of under-investment compared with such heavily researched pathogens as Pythium spp. and Puccinia spp.; many of the tree species concerned are of more significance to plantations and conservation management than to the annum income-generation of commercial agriculture, so conventional economic justification has been harder to demonstrate. The rate of development of resistance to pesticides in some instances has been documented as being as little as one year (Lolium rigidum to Chlorosufuron; Powles and Matthews, 1992), although more generally resistance may occur between 5 and 10 years' use. In this species the occurrence of multiple resistance, sometimes to herbicides which have never been applied to the population in question, has also been noted in Australia. While the very wide gene pool of L. rigidum, and its strongly competitive ability against most other species, have made its resistance a particularly difficult problem in minimum-tillage systems of pasture-croprotations, herbicide resistance is now a widespread phenomenon of many cropping environments in which systemic compounds have been in use for a number of years. Quantification of disease levels and resistance breeding is more advanced for fungal than bacterial pathogens as a whole; for example, the epidemiology

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A. Hamblin

Table II. World records of resistance to pesticides in Arthropoda 1970-1989. ,,.

Cases (number by species) by pesticide group

1970

1976

1980

1989

DDT Cyclodeine Organophosphate Carbamate Pyrethroid Fumigant Others Total

98 140 54 3 3 3 12 313

203 225 147 36 6 8 20 646

229 369 200 51 22 17 41 829

263 291 260 85 48 12 40 99

Source: Georghiou and Lagunes-Tejeda (1991).

and genetics of cereal rusts are particularly well documented. The International Centre for Improvement in Wheat and Maize has reported the breakdown in resistance of wheat cultivars to Puccinia recondita f.sp tritici (stem rust) within 3-5 years on average (Roelfs and Bushnell, 1985), and in an unusually welldocumented case, changes in the pathogenicity of stripe rust (Puccinia striiformis f.sp. tritic0 have been followed from the first detection in Australia in 1979 over a period of 10 years. Wellings and McIntosh (1990) observed 15 different pathotypes in Australia and New Zealand, with single gene mutations being the most likely cause of variation. Resistant varieties were effectively developed against the identified pathotypes, but breakdown against the first genes isolated (Yr2, Yr3, Yr4) occurring within one season. Subsequent spread of new pathotypes occurred at the rate of one to two a year, resulting from a single mutational event in each generation, in a step-wise progression. Using this example McIntosh (1992) has stressed the need to recognize and exploit longer-lasting (durable) resistance based on the concept of race-non-specific mechanisms such as multiple-gene resistance with adult-plant stage control, conferring non-hypersensitive response (Johnson and Law, 1975). Resistance in plant insect pests has become a very significant concern in a number of intensive annual and perennial cropping environments, and the current status of resistance to pesticides in arthropods is graphically illustrated in Table II, showing the continued increase in the resistance to the 'softer' pyrethroid group of insecticides in the 1980s, as these have been introduced to lessen the deleterious effects of the organophosphate and D D T groups which were so heavily used in the previous decade. The introduction of integrated pest management (IPM) systems has for long been heralded as the strategic, safe and sustainable alternative to the problem of resistance against such effective and devastating pests as Helicoverpa armigera (boll worm) in cotton. However, this system is not in fact sustainable, but represents a best-bet option for delaying the onset of resistance, as work in the Australian cotton industry demonstrates. The present, highly successful Australian cotton industry is some 25 years old. It has expanded rapidly to a position of being the

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fourth largest trader of cotton internationally earning more in exports than the total export value of fisheries and rivalling forest products, and is characterized by a sophisticated and well-informed producer population. Cotton is a notoriously heavy user of pesticide, fertilizer and defoliant chemicals, but the earlier near-obliteration of the Australian cotton industry in northern Australia in the 1960-1970s, by over-use of D D T and organochlorines, sharpened producer and scientist awareness for a programme of IPM from the inception of the present industry in northern New South Wales in the mid 1970s. The strategy has consisted of a number of components: breeding of hairy-leafed ('ockra') type varieties which offer physical barriers to insect attack; production of early-season varieties which avoid the optimum temperature development period of Helicoverpa sp. build up; use of an early-warning and risk-optimization model (Sirotac) to minimize the use of aerial spraying in conjunction with 'pestscouts' reporting the population build up; and a highly sophisticated chemical strategy which has used a sequence of pyrethroid-substitution compounds differing stepwise in their functional radical to minimize the selection challenge for pest resistance. Nevertheless, resistance to pyrethroids and endosulphan has occurred, and continues to increase with a progressive narrowing of the 'window' of use from 12 to 6 weeks in most districts. While current pyrethroid substitutions are delaying the rate of reduction of the window of effective control, they cannot stop it. Alternative strategies being investigated currently are the growing of buffer (alternative host) crops around each block of cotton, the use of Bacillus thuringiensis (Bt) mixed with, or instead of, pyrethroids, suppression of the resistance mechanism (via oxidative detoxification) with piperonyl butoxide, and the projected development of genetically engineered host-plant resistance (Forrester, 1990). At the same time increasing pressure is being placed on the industry from environmental and community groups for scaling down even further the number of pesticide applications, with particular concerns being expressed about the residue levels occasionally found in tailing waters and outflows from irrigation areas which form part of the Darling River Basin, relatively high up in this major catchment. I have gone into some detail over this one example because it presents all the challenges which pathologists of the high-input systems of the northern hemisphere face as countries in that region implement pesticide reduction programmes. Simply put, there are strong vested commercial and national interests in maintenance of high productivity systems, which for some crop environments are extremely difficult to achieve without reliance on practices which can be environmentally damaging. Even where strategies are devised to overcome the reliance on chemical control of a pathogen there may be substantial grower, processor or marketer resistance, or inability, to use the strategy. The theoretical attractiveness of the use of multiple-gene resistance by physically growing mixtures of varieties of similar architecture and phenology has long been advocated (Frey, 1976; Hamblin etal., 1976). However, successful commercialization has been the exception rather than the rule. The attempt to

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introduce Maris Tricorn, a mixture of three varieties of malting barley developed by the Plant Breeding Institute, Cambridge, illustrates this nicely. In the early 1980s this varietal mixture was promoted to reduce the reliance on a similar 'replacement strategy' use of fungicides against powdery mildew (Erysiphegraminis DC. f.sp. hordd Marchal), which had developed all the same problems of ineffective fungicide control due to the vast haploid population of that pathogen in which pathogenicity is frequently the result of sorting in individual gene frequencies (Wolfe, 1987). Despite the simplicity and cost effectiveness of the diverse mixture strategy, it was not attractive to the industry because of the reluctance of maltsters to accept the mixture, although the composition and malting qualities of all individual varieties were well known. The mixture strategy will not, as Wolfe pointed out, work well if the foliar disease is migratory, with new waves of inoculum entering the crop environment every few generations, and works best where genetic shift occurs as the result of within-crop spread. Varieties must also have sufficiently close phenologies, nutritional requirements and quality attributes to satisfy production demands. Nevertheless, it remains an under-utilized strategy in which market resistance is largely traditional rather than based on valid technical grounds. Such social, institutional and political aspects of high productivity agricultural systems are as significant to the successful introduction of alternative strategies of plant protection as the scientific problems posed by them. However, even in the scientific arena, there is a curious dearth of discussion within the scientific establishment on the anticipated longer-term biological outcomes of some of the proposed strategies. Such discussion has largely been within the ambit of non-government environmentalist organizations, and vary from the frankly emotive anti-science stand to the informed and thoughtful prospect of replacing one flawed system with another. Take the case of the significant amount of current interest and investment in the use of Bacillus thuringiatsis (Bt) strains as biocides, in IPM and resistance breeding. The natural toxins in different strains of Bt are selective amino acids which bind to receptor proteins in insect gut, causing the gut wall to disintegrate; over 50 compounds have been identified, often with very selective targets. They have been widely heralded as benign, not only because of their natural origin, but also because the strategy of using mixtures of the toxins was expected to reduce to almost zero the odds of resistance developing in any target pathogen. By altering the toxin spectrum over time, or by producing a suite of genetically altered host varieties with a range of toxins, it was inferred that crop pest and disease levels will be able to be kept at current very low levels without the environmental and resistance problems of current chemicals. However, recent reports of resistance in Colorado beetle and diamondback moths to Bt are indicative that even with these precautions there can never be a completely resistance-free insecticide (Holmes, 1993). Moreover, the insertion of Bt genes into crop plants may present a stronger selection pressure than the simpler use of the toxins as sprays, which break down rapidly in UV light. Strategies such as growing refuge areas of non-transgenic forms adjacent to transgenic

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crops of potatoes and cotton are being tested in limited-scale field situations, to diminish the possibility of any selection towards insect resistance, but the size of such refuge areas, ratios of transgenic to non-transformed plants, and producer willingness to forfeit a proportion of production as a hedge against future possible mutation are all unknown at the present time. It is against such complex issues that the claims by proponents of'organic farming' that this is more sustainable than conventional methods of plant protection should be weighed. However, the focus of much of the writing about, and research towards, more sustainable agricultural systems seldom considers plant protection in these terms.

IV. INTEGRATING ECOLOGICAL AND ECONOMIC ASPECTS OF PLANT DISEASE CONTROL IN SUSTAINABLE AGRICULTURE What then should be the position of responsible plant pathologists in seeking to provide more sustainable plant protection from the great host of diseases, insect vectors and predators, and alternate hosts associated with weed infestations? Should research continue to be directed to systems which will rely on pesticide applications, even if this is by means of inserting herbicide-resistance genes into target crops, as in the case of cotton and potato currently being developed como mercially? Can reliance on breeding as a strategy against leaf fungal diseases of annual crops continue indefinitely, in agroecosystems that are subjected to widespread fungicide applications several times every year, and where target efficiency may average little more than 50%, according to the significant improvements that have been demonstrated in calibration, operating conditions and reduced non-target loss experimentally (Hurst, 1992)? Would it not frequently be more effective to reduce the density of the crop canopy, and lower the dependence on the small range of crops currently grown in most environments that encourages large expanses of monocultures based on a narrow genetic base? Is the use of benefit-cost analysis as frequently invoked as Koch's postulates in plant pathology management? Let us look first at all the possible strategies, their current status and the plant types at which they are directed. For some 20 years the theoretical treatment of ecology has been stimulated by the insights of Robert MacArthur and his associates into relationships between the abundance and diversity of species and their environments. MacArthur's most pertinent contribution was to demonstrate the extremes in strategies employed by different species to maximize their numbers and persistence in island biogeographies (MacArthur and Wilson, 1967). Starting from the proposition that species cannot maximize both growth rate and competitive advantage (as metabolic energy and genetic transformation trade-offs occur between these), there are two basic strategies which can be employed to maximize one or the other. These are the 'r-strategy' and 'K-strategy'. r-~pe species are exploiters, opportunistic in behaviour, maximizing their growth rate whenever conditions are favourable, and profiting from uncrowded or

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Table IlL Principal control strategies for different pest problems (after Conway, 1981).

Strategy Pesticides Biocontrol

Cultural controls Resistance breeding

Mating control

r-pests Widely based on forecasting Not often practicable

K-pests

Intermediate Selective Introduction of natural predators and pathogens < ............

Time of planting, cultivation, sanitation ............. > General, polygenic .......... > < .......... Not effective?

Precisely targeted on monitoring

Change in rotation, destruction of alternate hosts Specific, monogenic Sterile mating, attractants ,,

unstable environments. K-type species are highly competitive, and favoured by crowded or stable environments. Their growth rates are lower than for r-strategists, but their competitive ability is greater; they have evolved in stable habitats where populations are maintained at relatively constant levels, often through low fecundity, high longevity and larger size. These concepts have been fruitfully pursued by May (1981) and Conway (1981) in relation to the most effective strategies for disease and pest control. The classical economic evaluation of the effectiveness of any strategy of pathogen control is, as mentioned, to apply a cost-benefit analysis, in which the total costs of control and the total revenues from control are assessed to identify the marginal rate of return for each additional cost increment. Conway (1981) considered a number of pathogen-control strategies for r and K classic pest types and for a range of intermediates, which include most introduced pathogens (frequently having been introduced in association with the cultivated host), separated from their natural predators or regulating climatic regime. Such intermediate types have often assumed the dimensions of a severe pathogen inadvertently through deliberate control of another, perceived threat; the weed science literature is rich in examples of little-known mosses, sedges or minor grasses suddenly becoming intractable weeds after selective herbicides have been used against another spectrum of weed types. Conway argued for a conceptual framework which would consider all pest and pathogen types within a farming system, and compare the pest 'strategies' with the possible control strategies, along the lines of the matrix shown in Table III. The effectiveness of any strategy should be assessed according to the frequency and scale of economic loss (yield or quality), the pathogen range, and the feasibility of implementation of the control measure. Table III does not go so far as to consider the interactions of different pathogens and strategies within the farming system, although this is the reason why plant resistance is so often a preferred strategy, as it allows more than one pathogen to be accounted for within a single 'package' of genetic composition. If agricultural scientists who service high-productivity farming systems are going to be effective in devising alternative pest and pathogen

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management strategies which are less reliant on selective pesticides and narrow gene resistance, it is essential that such systematic consideration of the total host and pest-pathogen spectrum be viewed together in this way.

V. HIGH PRODUCTION VERSUS LOW PRODUCTION ENVIRONMENTS AND FARMING SYSTEMS Misunderstanding abounds in popular literature as to what constitutes a high production system versus a low production system, the two often being confused with the level of inputs into the system. As noted earlier, some environments are intrinsically more productive than others, but increases in productivity are everywhere possible by the reduction of environmental constraints such as fluctuating water supply (as for example by supplementary irrigation to high biomass crops in sandy soils, even where grown in reliable rainfall regions of humid temperate zones). Intrinsically low-productivity regions can be made modestly secure by such strategies as planting dates which avoid climatic extremes (frost or high temperatures), or the use of compound fertilizers and soil amendments to overcome gross nutritional deficiencies (e.g. phosphate in most African and Asian alfisols, or the small quantities ofCu, Mo, Zn and B needed to rectify a wide range of minor and micronutrient deficiencies in Brazilian and Australian ultisols). There is a convincing body of evidence on the positive feedback between overcoming such gross nutritional deficiencies and the increased resistance of most crop species to root disease infection (Huber and McCay-Buis, 1993). These improvements in the stability (reduced variation) of the production system also provide increased sustainability, not only by reduction in food production shortfall, but also by maintaining a denser or more complete plant cover, capable of better protection against erosion and with a potential for increased residue and organic matter retention. Advocates of a universal reduction in the use of pesticides, fertilizers and other inputs based on the extremes of high input systems in the northern hemisphere are misguided; for the low input systems of the developing world, and the extensive production systems of Australia, south America and Canada, such a move would represent a significant deterioration, and in the tropics an absolute collapse, in the current fragile level of sustainability of production systems that are normally severely nutrient deficient (Pieri, 1992; Hamblin and Kyneur, 1993). For each economic and physical production environment there are a number of best-bet optimizations, but in all cases there will be a spectrum of plant pathogens to contend with. Breeders working across a range of production environments in the eastern Mediterranean have found that a general shift in the type of pathogen occurs where the crop biomass increases from an equivalent (in barley and wheat) yield of less than 1-2 t ha-1 to over some 3 t ha-1 (Ceccarelli et al., 1992; Hamblin, AI-Taweel, Yau and Walker, unpublished data). Lower yielding environments are, in rainfed conditions, typified by abiotic stresses in the soft;

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water deficiency or excess, nutritional imbalance and root pests and diseases. Higher yielding environments (with irrigation or higher, more reliable rainfall) are typified by biotic constraints deriving from the humid microclimate of the crop, and the specific attributes of the plant canopy in relation to radiation capture. They are the pre-eminent focus of leaf pests and diseases. Thus, where improvements in the production systems of low-yielding environments (through wide rotations, increased nutrition, retention of mulches and other soil structural improvement practices) increase the crop biomass to 8-10 t ha-1 of dry matter, leaf fungal pathogens increase in significance, whereas with the reduction of inputs in currently high-input systems in the Netherlands and Denmark as a result of their pesticide reduction programme, there may be a progressive scaling back in plant populations and lowering of fertilizer input to match, and a possible resumption of root pathogen problems.

VI. CONCLUSIONS Few natural, and almost no agricultural, ecosystems would today qualify for being in a 'steady-state' condition, physically, chemically or microbially. Over the past 40 years novel germplasm has been widely introduced into all but the most remote food production systems and many plantation and perennial grazing systems; there has been a significant narrowing of the genetic base in most commercially produced plant and animal varieties; a rapid increase in the use of inorganic fertilizers and pesticides; cultural changes that have included narrowing of rotational practices, the development of extensive monocultures, increasing mechanization and expansion of irrigation. In addition there has been a massive expansion into low-productivity environments in the tropical and subtropical regions as the result of population pressure and the continuing belief in agriculture as the engine to economic growth (World Bank, 1989). Add to these changes the more subtle environmental effects such as loss of remnant native vegetation habitats, hedgerows in Europe, wetlands in North America, and 'bush' reserves in the southern continents, which provided predator niches and influenced the microclimates of adjacent arable lands, and we can appreciate the extent and unprecedented rate at which agriculture's biophysical environment has been perturbed. Current scientific strategies to maintain and improve yields in support of high-input agricutture place great emphasis on 'fail-safe' techniques for each component of the production sequence with little consideration of the integration of these componeats in a holistic, systems approach. Research for sustainable agricultural practices requires a far greater emphasis on such an approach than is now fashionabl,.', despite all the rhetoric given politically to sustainability. It requires every scientist to step outside his or her field of specialization, develop common goals and methods of communication, and consider a much wider set of spatial and temporal scales and interactions than is usual. Perhaps before

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all this is possible, there must be an emotional and mental disengagement from the conventional mind-set which seeks to achieve supremacy over every pathogen for higher and yet higher yields, and replaces it with a goal of increased product diversity, increased profit per unit of input, and increased stability of production.

REFERENCES Allen, D.J. (1983). 'The Pathology of Tropical Food Legumes: Disease Resistance in Crop Improvement'. Wiley Interscience, Chichester. Australian Agricultural Council. ( 1991). ' Sustainable Agriculture'. Report of the Working Group on Sustainable Agriculture. Standing Committee on Agriculture Technical Report Series 36. CSIRO, Melbourne. Brown, H. D. and Schoen, D.J. (1992). Plant population genetic structure and biological conservation. In 'Conservation of Biodiversity for Sustainable Development' (O. T. Sandlund, K. Hindar and A. H .D. Brown, eds), pp. 88-104. Scandinavian University Press, Oslo. Ceccarelli, S., Grando, S. and Hamblin, J. (1992). Relationship between barley grain yield measured in low- and high-yielding environments. Euphytica 57, 49-58. CIMMYT (1989). see International Maize and Wheat Improvement Centre. Clements, R.J., Rosielle, A.A. and Hilton, R. D. (1992). 'National Review of Crop Improvement in the Australian Grains Industry'. A report to the Board of the Grains Research and Development Corporation, Canberra. Conway, G. (1981). Man and pests. In 'Theoretical Ecology: Principles and Applications' (R.M. May, ed.), pp. 161-178. Blackwell, Oxford. Conway, G. (1985). Agroecosystem analysis. Agricultural Administration 20, 31-55. Consultative Group on International Agricultural Research, (CGIAR) (1992). 'Review of CGIAR Priorities and Strategies - Part 1. CGIAR'. The World Bank, Washington (unpublished). Corey, S. A., Dall, J. D. and Milne, W. M. (1993). 'Pest Control and Sustainable Agriculture', CSIRO, Melbourne. Cullen, J. M. (1993). Opportunities and challenges in biological control. In 'Pest Control and Sustainable Agriculture' (S. A. Corey, J. D. Dall. and W. M. Milne, eds), pp. 44-50. CSIRO, Melbourne. Daly, H. E. (1988). On sustainable development and national accounts. In 'Economics, Growth and Sustainable Environments' (D. Collard, D. Pearce and D. Ulph, eds), pp. 38-56. MacMillan, London. Damuth, J. (1987). Interspecific allometry of population density in mammals and other animals; the independence of body mass and population energy use. Biology Journal of the Linnean Society 31, 193-246. Erwin, T. L. (1982). Tropical forests; their richness in Coleoptera and other arthropod species. Coleopterist's Bulletin 36, 74- 75. European Community (1992). 'Revised Common Agricultural Policy'. EC, Brussels. Food and Agriculture Organization (FAO) (1980-90). Annual Yearbooks for 'Fertilizer Use' and 'Food Production Statistics'. FAO, Rome. Food and Agriculture Organization (FAO) (1989). 'Environment and Agriculture; Environmental Problems Affecting Agriculture in the Asia and Pacific Region'. World Food Day Symposium, 11 October 1989. FAO Regional Office for Asia and the Pacific, Bangkok. Forrester, N. W. (1990). Resistance management in Australian cotton. In 'The Australian

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Cotton Industry Under the Microscope', pp. 361-368. Fifth Australian Cotton Conference, August 8-9th, 1990. Broadbeach, Queensland. Frey, K.J. (1976). Breeding concepts and techniques for self pollinated crops. In 'International Worshop on Grain Legumes' January 13-16, 1976, pp. 257-278. ICRISAT, Hyderabad. Georghiou, G.P. and Lagunes-Tejeda, A. (1991). 'The Occurrence of Resistance to Pesticides in Arthropods. An Index of Cases Reported Through 1989'. Food and Agriculture Organization of the United Nations, Rome. Hamblin, A. and Kyneur, G. (1993). 'Trends in Wheat Yields and Soil Fertility in Australia'. Bureau of Resource Sciences, Australian Government Publishing Services, Canberrra. Hamblin, J., Rowell, J . G . and Redden, R. (1976). Selection for mixed cropping. Euphytica 20, 97-106. Harlan, J. R. (1976). Diseases as a factor in plant evolution. Annual Review of Phytopathology 14, 31-51. Holdgate, M. W. (1991). Conservation in a world context. In 'The Scientific Management of Temperate Communities for Conservation' (I. F. Spellberg, F. B. Goldsmith and M. G. Morris, eds), pp. 1-26. Blackwell, Oxford. HoUing, C.S. (1973). Resilience and stability of ecological systems. Annual Review of Ecology and Systematics 4, 1-24. Holmes, R. (1993). The perils of planting pesticides. New Scientist 1888, 34-37. Huber, D. M. and McCay-Buis, T. S. (1993). A multiple component analysis of the takeall disease of cereals. Plant Disease 77, 437-447. Hurst, P. (1992). 'Pesticide Reduction Programmes in Denmark, the Netherlands and Sweden'. World Wide Fund International in collaboration with the Pesticides Trust, London, Gland, Switzerland. International Maize and Wheat Improvement Centre. (1989).' 1987-88 CIMMYT World Wheat Facts and Trends, the Wheat Revolution Revisited: Recent Trends and Future Challenges'. CIMMYT, Mexico, DF. Johnson, R. and Law, C. N. (1975). Genetic control of durable resistance to yellow rust (Puccinia striiformis) in the wheat cultivar Hybride de Bersee. Annals of Applied Biology. 81, 385-391. MacArthur, R . H . and Wilson, E.O. (1967). An equilibrium theory in insular zoogeography. Evolution 17, 373-387. McIntosh, R. A. (1992). Close genetic linkages of genes conferring adult-plant resistance to leaf rust and stripe rust in wheat. Plant Pathology 41,523-527. Marten, G. G. (1988). Productivity, stability, sustainability, equitability and autonomy as properties for agroecosystem assessment. Agricultural Systems 26, 291-316. May, R. M. (1988). How many species are there on earth? Science 241, 1441-1449. May, R. M. (ed). (1981). 'Theoretical Ecology: Principles and Applications', 2nd edn. Blackwell, Oxford. Ministry of Agriculture, Fisheries and Food, (MAFF). (1978). 'Maximising Yields of Crops'. Proceedings of a Symposium of the Agricultural Development and Advisory Service and the Agricultural Research Council, 17-19 January, 1978. HMSO, London. Organization of Economic Development and Co-operation. (1980-1990). 'Agricultural Policies, Markets and Trade Monitoring Outlook'. OECD, Paris. Organization of Economic Development and Co-operation, (OECD). (1992). 'Agents for Change'. OECD Workshop on Sustainable Agriculture, Technology and Practices, Paris, February 11-13, 1992. OCDE/GD (92)49, OECD, Paris. Pearce, D., Markandya, A. and Barbier, A. B. (1989). 'Blueprint for a Green Economy'. Earthscan, London.

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Pieri, C. V. M-G. (1992). 'Fertility of Soils and the Future of Farming in the West African Savannah'. Springer Verlag, Berlin, Heidelberg. Pimentel, D. (1993). Cultural controls for insect pest management. In 'Pest Control and Sustainable Agriculture' (S. A. Corey, J. D. Dall and W. M. Milne, eds), pp. 33-38. CSIRO, Melbourne. Pimentel, D., McLaughlin, L., Zepp, A., Lakitin, B., Kraus, T., Kleinman, P., van Ceni, F., Roach, W. J., Graap, E., Keeton, W. S. and Selig. G. (1991). Environmental and economic impacts of reducing U.S. agricultural pesticide use. In 'Handbook of Pest Management in Agriculture', Vol. 1, pp. 679-719. CRC Press, Boca Raton, FL. Powles, S. B. and Matthews, J. M. (1992). Multiple herbicide resistance in annual ryegrass (Lolium rigidum). A driving force for the adoption of integrated weed management. In 'Achievements and Developments in Combating Pest Resistance' (I. Denholm, A. Devonshire and D. Holloman, eds), pp. 1-13. Elsevier, London. Rabbinge, R. (1991). 'Perspectives for Rural Areas in the European Community'. Presentation to the Council of Ministers. October 1 1991. WRR, The Hague. Roelfs, A. P. and Bushnell, W. R. (1985). 'The Cereal Rusts. Vol 2. Diseases, Distribution, Epidemology and Control'. Academic Press, Orlando. Sandlund, O. T., Hindar, K. and Brown, A. H. D. (1992). 'Conservation of Biodiversity for Sustainable Development'. Scandinavian University Press, Oslo. Science Council of Canada. (1991). 'It's Everybody's Business'. Publications Office, Science Council of Canada, Ottawa. Strange, R.N. (1993). 'Plant Disease Control: Towards Environmentally Acceptable Methods'. Chapman & Hall, London. Wellings, C. R. and McIntosh, R. A. (1990). Puccinia striiformis f.sp. tritici in Australasia: pathogenic changes during the first 10 years. Plant Pathology, 39, 316-325. Wilson, E. O. (1988). 'Biodiversity'. National Academy Press, Washington, DC. Wolfe, M. S. (1987). Trying to understand and control powdery mildew. In 'Populations of Plant Pathogens: their Dynamics and Genetics' (M. S. Wolfe and C. E. Caten, eds), pp. 253-277. Blackwell, Oxford. World Bank (1989). 'Renewable Resource Management in Agriculture. A World Bank Operations Evaluation Study'. Operations Evaluation Department, The World Bank, Washington, DC. World Bank (1992). 'Development and the Environment'. World Development Report 1992. Oxford University Press, New York. World Commission on Environment and Development. (1987). 'Our Common Future'. Oxford University Press, Oxford. World Resources Institute. (1992). 'World Resources 1992-93'. Oxford University Press, New York. Zadoks, J. C. (1993). Antipodes on crop protection in sustainable agriculture. In 'Pest Control and Sustainable Agriculture', (S. A. Corey, D.J. Dall and W. M. Milne, eds) pp. 3-12. CSIRO, Melbourne.

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2 PREHISTORIC AGRICULTURAL METHODS AS MODELS FOR SUSTAINABILITY William M. Denevan Department of Geography, University of Wisconsin, Madison, Wisconsin 53706-1491, USA

I. Introduction II. Literature Review III. Forms of Prehistoric Agriculture A. Shifting Cultivation B. Rainfed Cultivation C. Agroforestry-Garden-Field Crop Integration D. Dryland Farming E. Terracing F. Drained Fields IV. Soil and Pest Management A. Soil Fertility B. Pests V. Sustainability vs. Collapse VI. Conclusions References

21 22 23 23 24 25 26 27 29 31 31 32 33 37 39

I. I N T R O D U C T I O N In recent years scholars have argued that agricultural methods employed in prehistoric times could serve as models for sustainable agriculture today (Denevan, 1980a; Smith, 1987; Treacy, 1989; Erickson, 1992). Many such methods continue in use (terracing, irrigation), by both modern (fossil-fuel based) and traditional farmers. What are particularly instructive are production systems that originated in prehistory and continued in place for long periods of time, thus demonstrating sustainability. Such methods and systems will be examined here. Many early crop systems, of course, ultimately did collapse owing to environmental change, excessive pressure on the agricultural environment, or social breakdowns. On the other hand, some ancient agricultural systems have continued in production to the present. 'Prehistory' here will refer to before 1492 for the New XJVorld and a more arbitrary BC for the Old World (Barker, 1985), without being bound strictly for ADVANCES IN PLANT PATHOLOGY--VOL. 11 ISBN 0-12-033711-8

Copyright9 1995 AcademicPressLimited All rights of reproductionin anyform reserved

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either. By'agriculture' I refer to all forms of planting and managing crops (which may or may not be fully domesticated). By 'methods' I mean the techniques used to construct crop fields, to plant them, and to manipulate the physical character of the crop environment (soil, water, slope, microclimate, plant and animal competition, and disease). By 'model' I mean viable methods which are instructive for making present agriculture more sustainable. By 'sustainable' I refer to methods and agroecosystems based on local inputs and on recycling, to potentially continuous duration, and to a deterioration of the resource base which is manageable or reversible. The topic is enormous and has received considerable attention, especially in the last 25 years as the result of the discovery of vast remains of ancient fields throughout the world, primarily by means of aerial photography. Here I only attempt to provide a general view of prehistoric agroecological systems and methods (forms, functions, extent, antiquity), plus some brief case studies of agricultural collapses. The focus is on field technology, not on crops themselves. In the Conclusion, I comment on the relevance of prehistoric agricultural methods to agricultural development today. A lengthy bibliography leads the reader to further information and analyses.

II. LITERATURE REVIEW

Surveys of prehistoric agricultural technology are relatively few and are mostly recent. Books and articles on the topic before 1952 are remarkably simplified, speculative, and inaccurate. Entire systems of cultivation are unmentioned. Treatments of prehistoric agriculture often gave much more attention to crop domestication (e.g. Struever, 1971; Bender, 1975). This reflected minimal interest in early agricultural technology by archaeologists and historians. However, this has now changed dramatically, especially in the New World where there have been major interdisciplinary projects on pre-Columbian cultivation practices. Classical descriptions of the methods of ancient agriculture include the works of Hesiod, Xenophon, Varro, Cato, and Columella (Fussell, 1972). Butzer (1994) diagrams the evolution of Classical Greek and Roman writing on agronomy, 700 BC to AD 600, in his excellent discussion of Islamic traditions of agroecology. Prior to 1952 modern descriptions of prehistoric agricultural practices were mainly brief sections of regional studies. Two noteworthy exceptions were 'Farmers of Forty Centuries' on East Asia by King in 1911 and Latcham's 1936 book on the Andes. Examples of specific topical and regional studies include Schilling (1938) on the chinampas of Mexico, Cook (1916) on Peruvian terraces, Bryan (1941) on the southwest USA, and Curwen (1938) and others on northwest Europe. Several important studies were published in the mid 1950s, and research has since accelerated. 'Plough and Pasture: The Early History of Farming' by

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Curwen and Hatt (1953), was the first book-length modern synthesis. A briefer review the same year was 'Conquest of the Land Through Seven Thousand Years', by Lowdermilk (1953). Volumes were published on soil and civilization by Hyams (1952) and by Carter and Dale (1955). These were followed rapidly by articles on qanats (Cressey, 1958), terraces (Spencer and Hale, 1961), and irrigation (Steward, 1955; Wittfogel, 1957). The first survey of prehistoric agriculture in the New World was by Armillas in 1961. A classic history of husbandry is 'The Care of the Earth' by Lord (1963). We now have a large number of regional studies and surveys and reports on particular techniques, reflecting an increased archaeological focus on remnants of ancient fields. Some of the most useful regional syntheses and collections include: Bradley (1978), Mercer (1981), Fowler (1983) and Barker (1985) on northwest Europe; Evenari et al. (1971) on the Negev; Hutterer (1983) on Southeast Asia; Raychaudhuri (1964) on India; Harrison and Turner (1978) on the Maya; Denevan etal. (1987) on the Andes; Doolittle (1992) on North America; Smith (1987) and Denevan (1980c) on Latin America; Denevan (1980b), Matheny and Gurr (1983), and Scarborough and Isaac (1993) on the Americas; Rojas (1988) on Mexico; Farmington (1985)on the tropics; Killion (1992) and Whitmore and Turner (1992) on Mesoamerica; and Woods (1992) on the midwest USA. Books on specific field systems include Kosok (1965) on irrigation in Peru; Darch (1983) on drained fields in Latin America; Siemens (1989) on raised fields in Mexico; Donkin (1979) on New World terraces; Doolittle (1990) on irrigation in Mexico; Rojas (1983) on chinampas in Mexico; Turner and Harrison (1983) on raised fields in Belize; and Turner (1983) on terraces in Yucaffm.

III. FORMS OF PREHISTORIC AGRICULTURE Agiculture can be classified into a few basic types based on environmental manipulation for the purpose of improving conditions for crop gowth. For prehistoric times these forms can be determined from field remnants which can be measured and studied archaeologically and in their environmental context. Additional information can be derived from artistic representations, early writing, and from inference from ethnohistoric or ethnographic analogy.

A. Shifting Cultivation One of the most widespread forms of agriculture, past and present, is the alternation of short periods of cultivation with longer periods of grass, scrub, or forest fallow which permits soil recovery and reduction of pest competition. This technique is sustainable under a modified forest cover as long as the fallows are sufficient. However, population densities (under 30 per kmZ) and productivity per area are relatively low. Shifting (swidden) cultivation occurs on good as well as

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poor soils, its advantage being labor efficiency, given plentiful land (Boserup, 1965). Relatively little labor is required to clear forest in contrast to the labor needed to practice permanent cultivation requiring soil fertility maintenance, water management and pest control. The problem with describing prehistoric shifting cultivation is that it is almost impossible to demonstrate its occurrence. Swidden fields leave no physical signature and hence their past presence can only be inferred. Pollen and other studies can demonstrate forest clearance, but cannot indicate whether cropping was permanent or shifting. The same is true of sediment transfer studies which indicate accelerated erosion from deforestation. An argument can be made that long-fallow shifting cultivation was not at all common when forest clearing was by stone axes, which are very inefficient compared to metal axes (Denevan, 1992), especially for large trees and hardwood trees such as are found in tropical forests. Clearing would have concentrated on light woody vegetation, softwoods, and young secondary formations. Once cleared of forest, near-permanent cultivation rather than shifting cultivation was likely, especially on good softs. Once a plot was opened it was probably more efficient to maintain it permanently or semi-permanently in crops by means of high labor inputs to combat pests and to maintain soil fertility than it was to practice shifting cultivation. Fire may have been a more important means of forest removal in Europe than clearing with either stone or early metal axes. However, it has been demonstrated experimentally that deciduous forest could have been cleared in Neolithic Europe with flint stone axes (Iverson, 1956). Whatever the means of clearing, patterns of village abandonment in Denmark suggest that early fields remained in production for 50 years or so (Iverson, 1956). Rowley-Conwy (1981) provides a convincing argument that Neolithic agriculture in Europe was primarily permanent not shifting, made possible by usually being located on good soil (also Vasey, 1992). Efficient bronze axes do not appear in Europe until after 2000 BC, and there were no metal tree-cutting axes in the Americas until after 1492. Doolittle (1992) believes that shifting cultivation was rare in prehistoric eastern North America.

B. Rainfed Cultivation

Rainfed cultivation is the most common form of agriculture, here referring to cropping dependcnt on adequate rainfall, good soil fertility, and relative permanence. It was the usual form of temperate agriculture in Europe and Asia, based on various types of soil turning tools. The oldest traction plows date to about 3000 BC in Mesopotamia (Curwen and Hatt, 1953:64). There were no traction plows in the Americas until after 1492, although foot plows were used in the Andes (Gade and Rios, 1972). The earliest agriculture in western Europe was based on digging sticks, hoes, and footplows. The light plow (ard, spade plow, coulterless plow) appears by 1000 BC in Britain. It could be used only on well-drained soils, usually upland, and is

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associated with the so-called 'Celtic' field system of square plots, which continued into the Roman period. This cultivation was based on the use of manure and humus transport, rotation of crops, and periodic fallow. The life span of some field systems was several hundred years (Curwen and Hatt, 1953; Bradley, 1978). Iron plowshares and heavy plows (coulter plows) capable of plowing ridges in heavy bottomland soils appear in Britain by 100 BC, creating narrow strip fields. By the Middle Ages a characteristic three-field system prevailed with rotation of wheat with barley-oats-beans and with pasture. Most early rainfed agicuhure is difficult to identify on the landscape because usually it was ephemeral and left no traces after lengthy abandonment or destruction of plow traces by later cultivation activity. An exception is the lynchet, many of which have survived to the present in northwest Europe. Lynchets were created by both non-plow and light-plow cultivation. By breaking the soil, soil moved to the lower edge of slope fields creating low ridges. Some of the lynchets produced by the light plow are very high (4 m) indicating lengthy cultivation by a settled population (Curwen and Hatt, 1953:66). Some surface and buried plow marks made by the light plow and by spades occur in uplands (Bradley, 1978; Halliday et al., 1981). Ridge and furrow patterns created by the coulter plow in Medieval times survive in many parts of western Europe (Beresford, 1948). These various plow marks are indicative of permanent fields.

C. Agroforestry-Garden-Field Crop Integration In tropical forests especially, field systems may be less clearly defined than elsewhere. Farmers rely on different strategies simultaneously, and over time a plot of land may rotate through a sequence of varied forms of management. These can include horticultural polyculture fields, swiddens, house gardens, managed fallows, and forest manipulation of both wild and cultivated plants. A single household may be involved in all of these as a means of food security. The diversity and rotation of systems and plants also permits environmental protection and recovery, whether intentional or a byproduct. Current examples of such integrated agroforestry systems in the Americas have been described for the Bora in eastern Peru (Denevan and Padoch, 1988) and for other tribes (Alcorn, 1989, 1990). The Huastec, for example, have a ' sequential agroforestry system' or 'working succession', in which 'there is a mosaic of maize fields, gardens, (managed) fallow thickets, and forested plots', involving deforestation and forest recovery over 15-20 years (Alcorn, 1990). Over time, the forest associated with such a system becomes an anthropic forest in which species composition, density, and distribution are to a large extent determined by human activity. Such 'economic' forests may have a reduced biodiversity and biomass, but they nevertheless are forests, forests that are sustainable and protective of soil, water and wildlife, in contrast to sites where forests are converted to grassland and scrub.

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It is difficult, however, to identify such integrated systems of land use in prehistoric times, since little physical evidence has survived. The argument is mostly inferential (Alcorn, 1981; Gordon, 1982; G6mez-Pompa and Kaus, 1990). Stone walls forming compounds around ruins of Mayan houses probably contained house gardens, as they do today. The current unnatural concentrations of economic plant species in forests have been attributed to a long history of human forest manipulation in Yucauln, Central America, and elsewhere. Large quantities of fruit pollen in the archaeological site of Araracuara on the R~o Caquet~ in the Colombian Amazon suggest fruit orchards or agroforestry (Fernanda Herrera etal., 1992). Also, a reliance on inefficient stone axes, as mentioned earlier, would seem to have encouraged small permanent fields and gardens and forest management rather than shifting cultivation (Denevan, 1992). Integration of field, garden, and forest could have been productive, protective, and sustainable and it was probably common prehistorically in the tropics as well as elsewhere. Surviving examples provide models for ecologically viable production systems under difficult soil and climatic conditions.

D. Dryland Farming Lawton and Wilkie (1979) indicate five forms of dryland farming, and others can be added (also see Scarborough, 1992). The first is 'dry farming' in which fields are often planted but are only harvested when there has been adequate rainfall. Dry farming can be inferred for prehistory, and was probably common, but no archaeological evidence survives. It may date to 5000 BC on the fertile loess softs of Shensi Province, China (Lawton and Wilkie, 1979:24). 'Runoff farming' occurs where fields are located to receive runoff from adjacent, unprepared slopes into natural catchment basins or into plots surrounded by stone or earthen walls, such as in the Anasazi southwest USA (AD 200-1500) (Vivian, 1974). Stonewall check dams across intermittent streams (wadis, arroyos) trap water (and soft) for small garden plots. Prehistoric check dam remnants are common in the Middle East (Evenari etal., 1971) and the southwest USA/northwest Mexico (Doolittle, 1985). 'Water harvesting' refers to the concentration of runoff from prepared watersheds, cleared and compacted, and directed by stone walls. This has been described by Evenari et al. (1971) for the Negev Desert where it dates to 1000 BC and irrigated 300 000 ha during Nabataean times (250 B C - A D 630). Evenari has attempted to re-establish this system at the ancient sites of Shivta and Avdat. 'Floodwater farming' refers to flood plains planted in crops after flood waters have receded or where fields are watered by flash floods on alluvial fans. A variation is 'recessional' or 'decrue' farming (Vasey, 1992:119-120) in which moist river banks are planted as river levels drop. Such 'natural irrigation' undoubtedly preceded canal irrigation but there is little archaeological evidence. In Egypt, there was 'artificial floodwater farming' along the Nile. The area cultivated was

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increased by controlling the length of time water remained in natural flood basins by means of dams, dredging, deepening overflow channels, and digging ditches to breach natural levees; the earliest evidence is c. 3100 BC or Late Predynastic (Butzer, 1976:19-21). 'Irrigation farming', or canal irrigation, involves the artificial transfer of water from source to field via canals fed by a regulated, reliable source of water. Enormous complex systems developed early involving dams, reservoirs, headgates, diversion embankments, terraces, and other features. Prehistoric irrigation was widespread throughout the arid lands of the Mediterranean and Middle East, extending to China, and including the padi systems of wetlands in East and Southeast Asia. In the New World, irrigation extended from Colorado to central Chile. Because remains of ancient canal structures are so widespread in arid lands and are associated with early civilizations, irrigation is probably the best studied form of prehistoric cultivation. Canals reflect sophisticated engineering skills and massive labor inputs. In Iran, small-scale ditch irrigation dates to 5500 BC, and by 700 BC large complex irrigation systems had been developed (Lawton and Wilkie, 1979). In the Middle East subsurface canals/chains of wells (qanats) date to at least 500 BC in I r a n - I r a q - T u r k e y (English, 1968). Irrigation canals and reservoirs were developed in central Mexico by 600-700 BC, in coastal Peru by 400 BC, and by the Hohokam culture of Arizona by 300 BC (Lawton and Wilkie, 1979; Doolittle, 1990). There are other ancient types of dryland farming. 'Sunken fields' in Peru include pukios, or depressions dug down to the water table in coastal valleys, and cultivated cochas, or artificial ponds that collect rainfall on the Lake Titicaca plain. Rock mulches, piles of or strips of rocks or layers of gravel, occur by the hundreds of thousands in the Negev (Evenari et al., 1971), in the southwest USA (Lightfoot, 1993), and elsewhere. 'Manual irrigation' involves the transfer of water directly from lakes or rivers (or wells) by hand (splash irrigation and container or pot irrigation) or by simple lift devices such as the shaduf (pole and bucket lever) in the Middle East and the water wheel. In Egypt, buckets were used by 3000 BC, the shadufby 2700 Be, and water wheels by 300 BC (Lawton and Wilkie, 1979).

E. Terracing Agricultural terraces serve to control erosion, increase soil depth, modify microclimate, and especially to help manage irrigation water on slopes. In fact, the distribution of terraces corresponds closely to the distribution of dry-land irrrigation, although there are rainfed terraces, especially in the Asian wet tropics. The distribution of prehistoric terraces fairly well matches the present distribution of cultivated terraces, given that most terraces originated in prehistory (Fig. 1). While there are considerable differences in terrace form, size, and organization, the two basic types are sloping-field terraces, usually rainfed, and bench

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Fig. 1. Prehistoric terraces still in cultivation, Pisac, Peru (photographed by R. Shippee and G. Johnson in 1931, reproduced by permission of the American Museum of Natural History).

terraces which are flat floored with vertical back walls and which are usually irrigated by an associated canal system. Bench terraces may have evolved as a response to uncertain or decreased rainfall (Donkin, 1979). Thus, in contrast to other forms of ancient agriculture whose non-sustainability was related to climatic change or human-induced environmental problems (deforestation, siltation, erosion, or soil decline caused by population pressure on the land), terracing actually evolved as a means of controlling these problems and changes. Because terrace walls frequently collapse and must be repaired, and because the terrace field itself is disturbed by cultivation, dating is difficult. Irrigated bench terraces (padi rice) were probably in use in China by 2500 ac (Hallsworth, 1987). Wadi check-dam terraces were in use in the Negev by 2000 BC (Evenari et al., 1971). In the New World in central Mexico and Peru, terraces date to 500-600 8c (Donkin, 1979). Some of the most impressive ancient terracing, in terms of size, stone work, and extent (over 1 million ha) is in the Andes, described by numerous sixteenth century writers. For example, Garcilaso de la Vega (1966:241-242) wrote: In order to make these terraces they would construct three walls of solid masonry', one in front and one at each end. They sloped back slightly.., so as to withstand the weight of earth with which they are filled to the level of the top of the walls.

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Above the first platform they built another smaller one, and above that another still smaller.., like stairs in a staircase, and all the cultivable and irrigable land being put to use. If there were rocky places, the rock~ were removed and replaced by earth brought from elsewhere to form the terraces. F. Drained Fields

Prehistoric drained fields have received less attention than other forms of ancient intensive agriculture. Recent discoveries indicate that drainage technology was widespread, but the technique is now entirely abandoned in many areas of former occurrence. Drainage of periodically flooded terrain or lake and river margins was accomplished by ditching, artificial raised fields or beds (mounds, ridges, platforms), or a combination of both. Some of the platform fields are enormous - up to 25 m wide, 400 m long, and 2 m high (Denevan, 1970). Early drainage for agriculture was undertaken in Roman England (Fens), by the Etruscans in Italy (Pontine Marshes), and in the ninth century AD in the Netherlands (polders) (Wagret, 1968). However, remains of older and more extensive systems of raised fields and canals have been found in the tropical lowlands of Asia and Latin America and in highland basins in Mexico and the Andes from Colombia to Bolivia. A system of dug drains, apparently for agriculture, has been uncovered beneath peat in Kuk Swamp in highland Papua New Guinea, which dates to about 7000 BC and continued with interruptions to the present (Golson, 1977). If correct, this would be one of the oldest dates for water-managed fields anywhere. Raised fields on the shores of Lake Titicaca (waru waru) date to c. 850-800 BC (Kolata, 1993:215), and those in the Basin of Mexico (chinampas) are at least 1500 years old. Large zones of tropical prehistoric raised fields occur in the Mayan lowlands of Mexico-Belize, upper Amazonia in Bolivia, the Venezuelan Llanos, the Guayas Basin of Ecuador, northern Colombia, and the Guiana coast (Fig. 2). Declining soil fertility was not likely a factor in sustainability. Organic muck rich in decomposed aquatic vegetation and wild life, algae and silt was transferred periodically from the ditches to field surfaces, making continuous cultivation possible, even where natural soils were of low fertility. This has been demonstrated by excavations of prehistoric raised fields at Lake Titicaca; in addition, remains of fish were spread over those fields and plant residues and dung were probably also used (Kolata, 1993; Carney et al., 1993). Experimental raised fields at Titicaca gave potato yields of 8-16 t ha compared to only 1-6 t on comparable flat-surface fields (Erickson, 1993; Kolata, 1993). Other functions of raised fields in addition to drainage and fertility management include frost induction (water in ditches acts as a heat sink, releasing energy at night) in highland regions, improved aeration and tilth, and reduction of weeds, insects, and pathogens (Kolata, 1993). A small form of raised field (1-2 m wide), not usually associated with poor drainage, is the garden bed or lazy bed, found in many parts of the world, past

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Fig. 2. Abandoned prehistoric raised fields, Llanos de Mojos, Bolivian Amazon (T. English, Bristow Helicopters Inc. 1961, provided by W. M. Denevan).

and present. Prehistoric remnants have been found in Ireland dating to 2000 BC (Fowler, 1983) and in Wisconsin and Michigan in the USA dating to 1100-1200 AD (Gallagher, 1992). Several hundred sites have been reported in the USA since the nineteenth century, but most have now been destroyed. Functions were likely similar to those of the larger raised fields. A variation is the Indian corn hill, a

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practice that continued after European settlement; remains of a few of these still survive (Gallagher, 1992). All the large New World raised fields have long been abandoned, except for a few sectors of chinampas at the edge of Mexico City. Most of the relic fields are in remote areas, now largely depopulated, which may explain abandonment either before or after European arrival. Changing climate and water regimes could also have been factors. Remnants of millions of raised fields survive in the Americas. They stand out clearly from the air, even when little relief remains, and they are easily mapped from air photos. They cover 122 000 ha of ditch and field surface at Lake Titicaca (Erickson, pers. comm.) and over 9 0 0 0 0 h a in the San Jorge savannas of northern Colombia (J.J. Parsons, pers. comm.), with lesser extents elsewhere. Large sectors of raised fields have been destroyed by human activity, burial under sediment, and by erosion. They are a lost system of agriculture in Yucat~in and in South America, but they once helped feed the Classic Maya civilization and the Tiwanaku empire in Bolivia. Several attempts at restoration have been made, the most successful being on both the Peruvian and Bolivian sides of Lake Titicaca - over 1000 ha of fields in over 50 communities - thanks in large part to the efforts of archaeologists Erickson and Kolata.

IV. SOIL AND PEST MANAGEMENT For an agricultural system to be sustained, several critical components of the agro-ecosystem must be controlled, including water, soil depth and fertility, and pests (weeds, insects, animals, pathogens). We have already discussed means of water control and erosion control. Fertility and pest control merit separate attention.

A. Soil Fertility The use of fertilizer to maintain or improve soil fertility may be nearly as old as agriculture itself, but it is difficult to demonstrate archaeologically unless there are chemical or biological indicators. Most important were organic additives: human and animal wastes, ash, garbage, crop residues, leaves, compost, cleared weeds, seaweed, mulch, urine, stable straw, ant-nest refuse, turf and muck. Manure, including human waste and compost, was used in India and China at least by 500 BC (Raychaudhuri, 1964; Thurston, 1992). The Chinese developed its use into a high skill 'which made agriculture permanent' (Curwen and Hatt, 1953; also see King, 1911). Manure was used by the early Greeks (Mather and Hart, 1956). In Europe, stable dung was the common manure, and manuring was also accomplished by grazing livestock on stubble or by folding (rotating pens

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on fields). Manuring was common during the Iron Age (Vasey, 1992). Roman farmers were competent in using various manures. Forms of early manuring in northern Europe are described by Fenton (1981). There are numerous sixteenth century descriptions of Inca use of fertilizers in Peru. Guano was applied on coastal fields and was transported by llama caravan for at least short distances into the interior (Julien, 1985). Fish were also used for fertilizer on the coast (Donkin, 1979). In the Andes, llama dung was used to fertilize potato crops, and there is one report of human manure (Garcilaso de la Vega, 1966). In highland Mexico, a soldier of CortSz reported stacks of human waste along the Aztec roads, probably for use as fertilizer (Armillas, 1961). Organic muck from the ditches between chinampas in Mexico was used as a fertilizer (Armillas, 1971; Wilken, 1987). The sunken fields of coastal Peru were fertilized with amendments of decomposing vegetation according to Latcham (1936). Inorganic additives were also transported short distances to fields, including silts, nitrates and ash in Bolivia (Soria Lens, 1954:92) and silt trap fields were cultivated in Peru and Mexico. In the Colombian Amazon at Araracuara (AD 800), alluvial sediments were transferred from flood plains to bluff top farms; organic wastes were also added (Fernanda Herrera etal., 1992). In the Brazilian Amazon prehistoric settlement sites with rich black anthropogenic softs (terra preta) were sought out by farmers (Smith, 1980). Green manuring (planting of nitrogen-fixing legumes) is difficult to identify archaeologically; however, the interplanting of beans served this function and was widespread in both the Old and New Worlds. An Inca fertilizer practice near Cuzco (now rare) is that of llakoshka, which increases yields by 20% or more (Anonymous, 1985). Seeds are dipped into a putrefying and fermenting mixture of dried llama dung, salt, and chicha (maize beer), and sometimes juice from the fruit of the molle tree (Schinus moUe). Resulting biochemical processes make inorganic elements in the soil more easily assimilated; parasites and aerobic organisms are destroyed; an anaerobic bloom is created; the dung provides nutrients for the seedlings and root system; yeast from the chicha turns seed starch to sugar which is advantageous to root development; plus there are other positive effects.

B. Pests

It is also virtually impossible to determine means of pest control through archaeology, and early written descriptions are rare. We can infer that crop losses were minimized by intercropping numerous species and varieties in each field. Also, a certain amount of crop loss was simply tolerated and compensated for by having larger fields, as long as land was plentiful. However, the biblical plagues of locusts were not myths and crop destruction was periodically devastating.

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An excellent study by Thurston (1992)examines traditional practices of plant disease management. Most examples are contemporary, but they are suggestive of prehistoric methods. There are some specific examples from the past of plant pathogen control. Homer (eighth century BC) mentioned 'pest averting sulfur'; Pliny (420 BC) reported that amurca (liquid waste) of olives was applied to plants to prevent blight; and other Greeks and Romans mentioned the use of amurca to control plant diseases and insects and as a fertilizer; Cato (200 BC) suggested burning sulfur to fumigate trees; ashes were used to control plant disease in ancient India (Thurston, 1992). Biological control of diseases particularly included multicropping. The use of manure and other organic additives was a common means of control. In China c. 300 BC, farmers used the yellow citrus ant to protect citrus fruit (Thurston, 1992). On the north coast of Peru, farmers today use lady bugs as a predator to control cotton insects, and a portrayal of a similar insect on a late prehispanic textile suggests that the practice was ancient (Vreeland, 1986). The current chinarnpa raised fields of Mexico have a reduced level of fungi and nematodes, probably because of high aquatic-related biological activity. This was also true of prehistoric raised fields in various parts of the world (Thurston, 1992). Other traditional methods mentioned by Thurston for controlling diseases include spacing, depth of planting, time of planting, disease-free soil, flooding, mulching, fallowing, and burning. Control of animal, especially bird, pests was commonly done by scare devices, crop guards and noise makers. On the other hand, large animal pests such as deer and monkeys may have been tolerated in fields so they could be more readily killed as game. The sixteenth century Peruvian chronicler and artist Guam~n Poma de Ayala (1980) depicted Inca farmers protecting crops from birds with slings, noise makers and guards. The control of weeds by traditional farmers is by shading, planting of companion plants, and removal by hand or with simple cutting tools (Altieri and Liebman, 1986). Gordon (1982) believes that in the tropics in prehistoric times, before the availability of metal machetes, weeding was more selective and less indiscriminate of the plants to be removed. Useful plants were thus allowed to survive in fields and fallows. Also, when weeds were pulled out by the roots the scattering of seeds was minimized and weed invasion thus reduced.

V. SUSTAINABILITY VS. COLLAPSE Sustainability of ancient field systems is demonstrated by continuance over long periods of time. Prehistoric agriculturalists, based on sophisticated environmental and agronomic knowledge, developed ecologically sound systems of land management that were productive, utilizing local resources and recycling. However, it is a mistake to believe that sustainable agriculture was a universal characteristic of our ancestors. There were massive crop failures and field abandonments due to

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environmental change and mismanagement, social disruptions. The following are a few examples of sustained and failed cultivation systems in prehistory under different circumstances. Lake Titicaca. The raised fields around Lake Titicaca in Peru and Bolivia were the major provider of food for the Tiwanaku civilization (AD 100-1000) and may have supported over 1 million people. They were still in use during the Inca period (AD 1450-1532), but terrace agriculture had become more important. There were earlier periods of regional abandonment. In particular, there was contraction of raised fields in the northern Titicaca basin during the expansion of raised fields during the Tiwanaku period in the south. Kolata (1993) believes that the collapse of the Tiwanaku state resulted from raised field abandonment caused by prolonged drought starting about AD 1000, as evidenced by ice cores. Erickson (1988), on the other hand, attributes field contraction to shifts in regional political power. In any event, few raised fields were still in cultivation in the sixteenth century, probably because of depopulation from European diseases. An entire agrotechnology vanished. In part, this was because the Spaniards converted the lake plain lands into cattle and sheep haciendas. One argument about the evolution and abandonment of raised fields is that this form of agriculture is extremely labor intensive and therefore is not economically practical under low population densities. Erickson (1993), however, has demonstrated that while construction labor costs are high, the maintenance costs are low, so that over a period of a decade or more, raised field cultivation is actually more labor efficient than flat-field cultivation, especially given the much higher crop yields of raised fields. Colca Valley. A large portion of terraced land in the Andes is abandoned. An interdisciplinary project in the Colca Valley (elevation c. 3500 m) in southern Peru examined the history and causes of abandonment (Denevan, 1987). Since most of the Colca terraces are irrigated, decreased precipitation has been considered the reason for large sectors going out of production (Donkin, 1979). Climatic change probably was the reason for abandonment of unirrigated sloping field terraces c. AD 500-600. However, this apparently stimulated the construction of irrigated bench terraces. If so, climatic change led to more sophisticated terracing, not a decline (Treacy and Denevan, 1994). On air photos we measured 62% terrace abandonment (Denevan, 1987). Most of this occurred in the early colonial period when the population declined by 75 % mainly from epidemics. The terraces most distant from the surviving villages on the valley floor were abandoned and remain out of use. Previously, rural settlement was more dispersed with people living on their fields or in small defensive villages on hilltops and ridges. Options for other food production or migration, given a dense regional population, were limited. People now tend to migrate and seek opportunities elsewhere rather than make large labor investments in restoring and maintaining terraces and canals in a rugged landscape. The Intravalley Canal of Peru. This is the longest (74 km) canal and one of the largest construction projects in prehistoric America (Posorski and Posorski 1982;

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Kus, 1984; Ortloff etal., 1985). It was built by the north coast Chimu state between A D 1000 and 1300 to move water from the Chicama Valley south to the Moche Valley to expand irrigated desert cultivation in the vicinity of the great Chimu city of Chan Chan. However, examination of sediments in the canal shows that the southern portion never functioned. Recent measurements of the canal indicate that some sections run uphill, as much as 31 m, making gravity flow impossible. Explanations, hotly disputed, include: (1) inept surveying, which seems improbable given known Chimu engineering skills; (2) tectonic uplift, which would have had to have been substantial over just a few hundred years or less; and (3) the canal was never intended to function, but rather was a periodic, massive public works project to keep discontented people occupied during droughts, with no concern for viability requiring the maintenance of a down-slope gradient. Regardless, if the canal had ever functioned, only a small portion of the water entering would have reached its destination given a high rate of loss due to evaporation and seepage. In addition, functioning portions of the system were periodically destroyed by floods associated with El Nifio climatic events; also river down cutting caused by both uplift and flooding resulted in cut offs of inlet canals. Today, only 35-40% of ancient irrigated lands in the Moche Valley are still under cultivation. Thus, we have explanations for ancient agricultural failure here which are technical, environmental and social, considerations which all come into play in agricultural collapses elsewhere. Ceylon. Some irrigation canal systems and associated fields were in near continuous use for very long periods. A monumental system of canals, dams (up to 30 rn high), and reservoirs (tanks) on the island of Ceylon (Sri Lanka) fed rice padi fields from AD 100-1300 (Murphey, 1957). One huge reservoir covered 2500 ha at Anuradhapura and fed fields by canal 90 km distant. This system took 1400 years to build, an incremental process characteristic of most intensive, landscaped cultivation. Production was halted by periodic invasion and resulting destruction and breakdown of management, but the final collapse resulted more from depopulation due to virulent malaria than from environmental factors such as climatic change, siltation, soil decline, or floods that breached the tanks. With control of malaria, part of the ancient system has been restored, but new deforestation causing soil erosion has been severe. North China. Over thousands of years China developed some of the most sophisticated and sustainable methods of agriculture in the world (King, 1911)" irrigation, terracing, padi, diking, soil conservation, manuring. Nevertheless, massive failures have occurred. In Shansi Province, deep, rich loess soils experienced tremendous erosion following deforestation for agriculture dating back 4000 years. This resulted in extensive abandonment of crop land and depopulation. In addition, enormous quantities of silt from this erosion flowed into the Hwang Ho (Yellow River) causing siltation of canals and flooding of entire regions of cropland, not to mention the destruction of villages and loss of millions of lives (Lowdermilk, 1953).

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Mesopotamia. The Mesopotamian story is well known but complex (Jacobsen and Adams, 1958). Irrigation agriculture dates to 4000 BC along the TigrisEuphrates and was well developed with canals, dams, and reservoirs during the Sumerian Empire (2500-2000 BC). By the Sasserian period (AD 226-640) massive state-managed canal systems had been developed, which (1) extended irrigation, and (2) maintained the system in the face of siltation of canals and flooding, in part related to deforestation in the headwater mountains to the north. Groundwater salinization had been managed by fallowing, but this was increasingly shortened with population growth, and salinization became serious, leading to land abandonment and new canals. During periods of state decline due to invasions, internal disorder, and depopulation, centralized irrigation management collapsed, but irrigation still continued at the local level with simpler canal methods such as had existed before the rise of states. State control actually contributed to irrigation failure by making the system dependent on state man power and capital for maintenance and by extending the length of canal networks making them vulnerable to greater and more rapid siltation (Adams, 1974; Gibson, 1974). Thus in Mesopotamia we see enduring sustainability at the local level, despite human-induced environmental problems, and expansion, overshoot, and collapse at the state level, with state management both exacerbating the environmental problems and not being able to cope with them when the state was weakened. The collapse of agricultural systems in prehistory resulted from natural and human-induced environmental change, both over population and depopulation, and political/social/managerial breakdowns. Often we do not know what the critical factors were, or at least the triggering factor. The Classic Maya (AD 300-900) is an example, for which there was political collapse, depopulation, and change from intensive to extensive agriculture (Harrison and Turner, 1978). Natural environmental change at times may have been crucial. In northern Mesopotamia at 2200 BC, drought seems to have contributed to agricultural abandonment leading to migrations and invasions into the irrigated lands to the south which caused the collapse of the Akkadian empire there (Weiss et al., 1993). Political and demographic collapse do not necessarily mean there was complete agicultural abandonment and loss of agroecological knowledge. The people surviving may have continued production, with technological and/or spatial adjustments. Butzer (1976:111) points out that in the Nile floodplain, during the rise and fall of kingdoms over thousands of years, there was 'an unexpected continuity in environmental exploitation strategies between prehistoric communities of the Pleistocene and the much more complex and sophisticated cultures of historical times'. In the Andes, although some detail has been lost, the terracing and irrigation technology at the community level today is basically the same as that for adjacent fields abandoned 500 years or more ago. Complete loss of technology, as with the raised fields of South America and Yucat~in, was unusual.

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VI. CONCLUSIONS We have briefly examined the forms, functions, antiquity, extent and success of prehistoric agricultural methods. The topic is large and fascinating, and the literature is considerable. Many ancient methods have continued to the present, providing clues to former techniques, viability, and productivity; however, such analogy is not necessarily valid. Change and innovation have been continuous. The distribution and extent of many of these methods is suggested by surviving field features, but most ancient fields have been destroyed by subsequent agriculture, other human and natural activity, or have been buried under sand and sediment. We know most about intensive forms of agricultural landscape modification and least about shifting cultivation, agroforestry, rainfed cultivation, flood water farming and dry farming. Thus, conclusions about the sustainability and longevity of ancient methods may be distorted. Landscaped fields require high labor inputs to construct and often also to maintain. To justify such inputs, such fields need to be utilized every year, or with only brief fallow periods, and for long periods of time without abandonment. For this to be possible, soil maintenance and pest control techniques must be employed. Prehistoric terraced, irrigated, drained, and padi fields appear to have been sustainable because of the endurance of their landscaped components, but they were sustainable because of effective soil and pest management. The presence of such fields alone implies such management and suggests continuous cultivation. Thus the agroecological lessons to be learned from the study of ancient fields and methods are derived from both (1) a soft technology (ephemeral) based on cultivation techniques and on the management of soils and pests, and (2) a hard technology (enduring) based on landscape modification to improve the cultivation medium by increasing water availability, by drainage, by erosion control and by microclimatic modification. Sustainability is dependent on the former, but cultivation may not even be possible without the latter. Knowledge of the former mainly comes from sketchy written evidence. Knowledge of the latter mainly comes from remnant fields and field features from which considerable detail about methods can be derived. The techniques for both are similar to techniques practiced by traditional farmers today, but some former methods have been lost entirely. Ancient fields have served as models for revivals, as witness the building or rebuilding of raised fields and terraces in Mexico and South America and runoff fields in the Negev. However, viable ancient agricultural methods are not necessarily successfully transferable to different times, environments, and cultures (Chapin, 1988); the same is true, of course, of modern methods. Both ephemeral and landscaped methods of cultivation involved long-term, sustainable crop production. For the ephemeral fields, this was made possible by usually being located on the best soils. However, in time, even fertile soils decrease in tilth, increase in pest levels, and decrease in productivity. As populations grew, good land decreased and opportunities for expanding the cultivated

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area were thus reduced, and soils were maintained by short-term fallowing, application of fertilizer, green manuring, and other techniques. Long-fallow shifting cultivation was unlikely until the availability of metal tools for clearing forest. Pathogens, animal and insect pests, and weeds were controlled by a variety of methods. Environmental disturbance is the inevitable result of any form of agriculture. Deforestation is required and soils are modified. Fertility declines, erosion occurs, pests increase, and water regimes are altered. It can be hypothesized that techniques of sustainability evolved in response to these habitat changes in order to continue an adequate level of productivity, given limited land. Of course such adaptation is not inevitable, and field abandonment and agricultural collapse may occur as result of excessive pressure on the land due to population growth, inappropriate or inadequate technology, or environmental change (natural or man made). Examples are commonplace in prehistory as we have seen, just as they are today. Furthermore, knowledge of sustainable technology does not suffice if sources of fertilizer are depleted, if infestations of pests are overwhelming, or if long-term climatic change occurs. On the other hand, landscaped cultivation systems are fully dependent on maintenance of the physical infrastructure (terraces, etc.). If this is neglected, the system will collapse in full or in part. The reasons may be environmental (floods, drought, tectonic, volcanic), demographic decline (the most labor intensive fields will be abandoned), or social (warfare, managerial, costs). Failure to restore abandoned fields may reflect other food getting options or migration, as we found with terrace abandonment in the Colca Valley of Peru (Denevan, 1987). Ecological and social factors, of course, may interact to bring about agrarian collapse, as for example drought or sedimentation/salinization of irrigation systems and warfare in Mesopotamia. William Clarke (1977) has delineated seven 'principles of permanence' in traditional agriculture in the Pacific that allowed continuing (or sustainable) cultivation for centuries or millennia: 1. 2. 3. 4. 5.

Cultivation is not dependent on external energy or nutrient sources. Agricultural systems are not self polluting. Net energy yields are positive. Only renewable resources are used. Agricultural resources are spread throughout a community rather than being concentrated. 6. Resources are considered as 'productive capital' to be preserved for future generations. 7. Agriculture is based on polyculture and integration of tree and non-tree crops and wild plants. These principles characterized much of prehistoric agriculture and made possible a resiliency in the face of environmental, demographic and social change. Much more research is needed, however, to understand more fully the bases for prehistoric agricultural permanence. Insights are provided by successful existing

Prehistoric Agricultural Methods as Models for Sustainability

39

methods of traditional agriculture, which provide models for sustainability (see Klee, 1980; Wilken, 1987; Browder, 1989; Thurston, 1992). However, prehistoric methods are particularly instructive as they provide a long-term perspective on successful, sustained crop production. Out of prehistoric agricultural methods emerged two pattems: (1) continuity (with continuing modification) maintained by traditional farmers, and (2) evolution into modern agriculture, with increasing emphasis on machinery, nonrenewable energy, and use of chemicals. Now, given the high cost of fossil fuels and environmental decline, arguments are being made that we must integrate the two approaches, seeking a compromise between the sustainability of the former and the high productivity of the latter.

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SUSTAINABLE AGRICULTURE: AN AGROECOLOGICAL PERSPECTIVE Stephen R. Gliessman Agroecology Program, Board of Environmental Studies, University of California, Santa Cruz, CA 95064, USA

I. Introduction II. An Agroecological Approach A. The Ecosystem Foundation B. The Agroecosystem C. Sustainable Agriculture III. Plant Pathology in the Agroecosystem A. The Pathosystem B. Traditional Agroecosystem Management C. Strawberries and Methyl Bromide IV. Plant~Pathogens in Sustainable Agroecosystems Acknowledgments References

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I. I N T R O D U C T I O N Agriculture worldwide has benefited from several decades of increasing yields and surplus production of many commodities. But the costs of maintaining these yields, from ecological, economic, and social perspectives, have led to the current debate about how to ensure the long-term sustainability of our food and agricultural systems, yet still meet the needs of a burgeoning human population (Edwards et al., 1990; Allen et al., 1991; Schaller, 1993). A sustainable agriculture must balance the needs of ecological soundness, economic viability and social equity. Current agricultural practices are pointed to as the principal area in which to begin the shift towards more sustainable food and agricultural systems (Francis and Madden, 1993). Some of us involved in the discussions about sustainability believe that the widespread use of synthetic chemical fertilizers and pesticides is contributing to the degradation of most agricultural systems. Others insist that without the use of these inputs, production levels would immediately collapse. But what is often lost in this debate is that sustainable agriculture is not a way to ADVANCES IN PLANT PATHOLOGY--VOL. 11 ISBN 0-12-033711-8

Copyright9 1995 AcademicPress Limited All rights of reproduaion in anyform reserved

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farm - rather it is an approach to understanding how our food and fiber systems might be designed and managed so as to lessen or avoid our dependency on these external inputs in the first place (Gliessman, 1990a; Edwards etal., 1993). It is a focus that brings together the all too often isolated fields of agronomy and ecology in order to go beyond crop yields. It is an agroecological approach that simultaneously strives to improve yields, as well as understand the processes that permit the maintenance of those yields. The primary goal is to establish a means of determining the long-term sustainability of agricultural systems (Gliessman, 1990a). Such an approach could have special application in the area of plant pathology.

II. AN AGROECOLOGICAI. APPROACH A. The Ecosystem Foundation There has been a recent emergence of research activity on the ecology of agricultural systems (Altieri, 1987; Carroll et al., 1990; Gliessman, 1990a). After a long history of separation and lack of interaction, ecologists and agronomists have begun to combine forces in order to study and help solve the problems confronting our food production systems. Out of this the field of agroecology has taken form. The primary foundation of agroecology is the concept of the ecosystem, defined as a functional system of complementary relations between living organisms and their environment, delimited by arbitrarily chosen boundaries, which in space and time appears to maintain a steady yet dynamic equilibrium (Gliessman, 1990a). Such an equilibrium can be considered to be sustainable in a definitive sense. A well-developed, mature natural ecosystem is relatively stable, selfsustaining, and able to maintain productivity using energy inputs of solar radiation alone (Fig. 1). In examining agricultural systems from an ecosystem perspective, we have a basis for looking beyond a primary focus on system outputs (yield or harvest), and instead look at the complex set of biological, physical, and chemical interactions that determine the processes that permit us to achieve and sustain those yields. Hence, agroecology becomes much more process oriented. An understanding of the chief characteristics of natural ecosystems, as well as the differences that are introduced once human manipulation of the system takes place for the purpose of agricultural production, can be an important step in an analysis of sustainability. These characteristics are as follows:

1. Energy Flow Energy flows through a natural ecosystem as a result of complex sets of trophic interactions, certain amounts being dissipated at different stages along the food chain, with the greatest amount of energy in the system ultimately moving along the detritus pathway (Odum, 1971). Annual production of the system can be

Sustainable Agriculture: An Agroecological Perspective ATMOSPHERE AND RAIN

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I I

' l

4
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5 Frequency of plant resistance allele

Fig. 2. Modifications of the theoretical 'boom-and-bust' cycle in agriculture. 5, the resistance allele's frequency rises if crop varieties carrying it are popular; 6, an effective resistance allele is not used if varieties carrying it are not popular, even if the frequency of the matching virulence allele is low; 8, the virulence allele is selected as the acreage of varieties which have the resistance allele rises (see phase 2 in Fig. 1); 9, the frequency of an ineffective resistance allele may remain high, because the varieties which have it also have other, desirable characters, or because the gene is combined with more effective resistances in new varieties; 10, the resistance aUele's frequency falls if varieties with more effective resistances replace those with the defeated resistance; 11, the virulence allele's frequency rises if this gene is associated with virulences which overcome newly introduced resistances, but falls if it is dissociated from them; 7, the resistance is durable, so that varieties with it do not select virulent pathogens. T h e s e two a s s u m p t i o n s do not hold in m o d e r n agricultural systems, however. Firstly, in most crops, few varieties are widely grown, so that, although there are m a n y individual plants, there are c o m p a r a t i v e l y very few genotypes. Secondly, the frequency of a resistance gene in the p o p u l a t i o n of a crop is d e t e r m i n e d indirectly, by h u m a n i n t e r v e n t i o n in choosing varieties (point 5 in Fig. 2).

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Resistance to a disease can be a significant factor in a farmer's choice of which variety to plant, but control of any single disease is only one of many factors which a farmer must consider. If effective fungicides are available, disease resistance may be a relatively minor consideration, compared to yield and quality. Since the number of varieties is limited, any single resistance gene is inevitably associated with other characters which may be more important in determining farmers' choices of varieties. The frequency of a resistance is therefore not determined directly by the frequency of the corresponding virulence, but by farmers' estimates of the profitability of varieties with that resistance. Some effective resistances have been introduced in new varieties, but, in contrast to the prediction of phase 1 of the theoretical cycle, have not reached high frequencies because the varieties carrying them were not very popular (point 6 in Fig. 2). Examples of such genes are the powdery mildew resistances Mlal and Mla9 in barley (Brown and J#rgensen, 1991). Furthermore, breeders may have difficulty in transferring a useful resistance into commercial cultivars. Despite the fact that the gene mlo, for resistance to barley mildew, has been used in popular spring barley varieties for 15 years (J#rgensen, 1992), no commercial winter barley variety has yet been bred with mlo perhaps because of the difficulty of breeding successful varieties from crosses of winter and spring cultivars.

2. The Fate of Ineffective Resistances The need to consider the overall value of varieties may cause a resistance to be widely used, even when the matching virulence is at a high frequency, in contrast to phase 3 of the model cycle (point 9 in Fig. 2). For instance, many wheat varieties carry a segment of chromosome 1R, translocated from rye. The translocated chromosome, designated 1B-1R, carries the gene Yr9 for resistance to yellow rust (Macer, 1975). Many popular British wheat varieties have the 1B-1R translocation, and therefore Yr9 too, even though the matching virulence has been at a high frequency for several years (Bayles and Stigwood, 1993). This is because the principal target of selection by breeders is increased yield, and the 1B-1R chromosome appears to increase the yield of wheat varieties which carry it (Rajaram etal., 1983). Furthermore, the simple model considers only a single resistance and its corresponding virulence. However, even when a resistance is no longer effective, it may still be presellt in breeding programmes, if the varieties which carried it are considered to be good parents because of their other properties. The old, defeated resistance may th,:refore be combined with effective resistances in new varieties. This has happened repeatedly in barley breeding, where the seven alleles at the Mla locus that ha,,e been used in breeding have been combined with alleles at at least seven other 13ci (Wolfe, 1984; Brown and J~rgensen, 1991). The genes Mlg and Mlra are particularly common in modern barley varieties, despite having little effect against most of the (E. graminis) E.g.f.sp. hordei population in Europe (Limpert, 1987a; Brown and Wolfe, 1990; Wolfe etal., 1992).

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Even when a resistance gene does fall into disuse, this does not happen because possession of that gene causes an inherent lack of fitness in plants which carry it. Firstly, the generalization that resistances to pathogens impose a fitness cost on plants which carry them is not actually valid (Parker, 1992). Secondly, its frequency falls because other, more effective resistance genes, are carried by varieties that are selected by breeders and chosen by farmers (Person, 1966) (point 10 in Fig. 2). As with the introduction of a new cuhivar in the cycle's first phase, many factors other than susceptibility to one single disease contribute to the withdrawal of a variety from cultivation.

B. The Dynamics of Virulence

1. Selectionfor Virulence The second part of the model cycle, the increase in the frequency of virulence, is caused by natural selection on the pathogen population, effected by plants which carry the matching resistance gene. There are three prerequisites for natural selection to occur: there must be variation in a character, the variation must affect fitness and these varying characters, which affect fitness, must be inherited. If these criteria are fulfilled, natural selection is inevitable in a large population (Crow and Kimura, 1970). In many pathogens, including those that cause rusts, smuts and powdery and downy mildews, many virulences conform to the gene-for-gene hypothesis of Flor (1956). Individual isolates of these fungi vary in carrying the virulence or avirulence allele of any one such gene. Which allele the pathogen carries has a major effect on its fitness, by affecting its ability to reproduce on a plant which carries the corresponding resistance. Numerous studies have shown that avirulence is inherited, and have revealed the nature of its genetic control (Thompson and Burdon, 1992). Virulence should therefore be subject to natural selection, and indeed, pathogens have adapted to many host resistance genes. The plant pathology literature contains many examples of selection for virulence. One of the clearest is that of the evolution of yellow rust of wheat (Puccinia striiformis f.sp. triticz) in Australia (Wellings and McIntosh, 1990). There, wheat was free of this serious disease until 1979, when the first outbreaks were caused by race 104E137A-. This race subsequently mutated stepwise to virulence on three resistance genes, YrA, Yr6 and Yr7, carried by Australian varieties which were unaffected by the original epidemic. Phase two of the theoretical cycle can therefore occur in agriculture (point 8 in Fig. 2). However, we can distinguish two different processes by which a virulence may be selected. One follows the introduction of a new resistance gene, when the matching virulence has not previously been selected, while the other follows the rise in frequency of a resistance gene in subsequent cycles.

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2. Adaptation to a New Plant Resistance When a new resistance gene loses its effectiveness, because the pathogen has adapted to it, the resistance is said to have broken down. The breakdowns of three barley powdery mildew resistances in the British Isles have been studied in detail. One clone of E.g.f.sp. hordei broke the resistance of cv. Triumph, conferred by Ml(Ab) + Mla7, in the early 1980s (Brown and Wolfe, 1990; Brown et al., 1990), while another clone broke the resistance of cv. Klaxon (Mla7 + Mlk + MlLa) in 1986 (Brown etal., 1993). The resistance of a group of varieties, conferred by Mlal3, broke down through the emergence of several clones, of which two were especially important (Brown et al., 1991). The isolates in each of these clones had many other factors in common, including other virulences, characteristic responses to fungicides and genetic fingerprints, produced by a D N A probe which can identify whether or not several isolates are members of the same clone (Brown and Simpson, 1994). The exact sequence of events which led to the emergence of these predominant clones is not known, but reasonable hypotheses can be proposed. In none of these three cases had the virulent clone been detected in Britain before the new resistance was introduced. The factors that can introduce a new virulence into a population are mutation, recombination or migration. The T r i u m p h gene, Ml(Ab), had not previously been used in commerce, so the virulent clone was probably a novel mutant from within the British population of E.g.f.sp. hordei. O f the three resistance genes in Klaxon, MILa had not previously been used together with M/a 7 or Mlk in a popular variety. The virulent clone may therefore have been either a mutant or a recombinant progeny of a cross between an isolate with virulence on MlLa and one virulent on Mla7 and Mlk. In the case of Mlal3, one of the two clones which initiated much of the epidemic was probably a migrant from further east in Europe, while the other may have been a novel, indigenous mutant (Wolfe et al., 1992). W h y the population of E.g.f.sp. hordei with virulence towards a new resistance should be so strongly clonal can be explained by thinking of the evolution of each clone as a kind of founder event. Clearly, each clone multiplied rapidly from a low frequency, since the resistance had previously been effective. Once such a clone had successfully infected a plant in a field sown as a monoculture, there would have been no further barrier to its spread, by means of airborne conidiospores, to other, genetically identical plants in the same field, and thence to other fields of the same variety or of other varieties with the same resistance. If dispersal were sufficiently rapid, there would have been little competition with other clones. Since mutation and recombination are both random processes, it is likely that the identities of the predominant, virulent clones were largely determined by chance. The effective population size of a subpopulation of E.g.f.sp. hordei that is virulent on varieties with a new resistance may therefore be extremely small. This simple model may be relevant to some other pathogens, but not to others. The genetic uniformity of E . g . f . s p . hordei populations on newly susceptible

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varieties, over large areas, indicates that the pathogen's rate of dispersal is high relative to the rate of mutation. If it were not, we would expect to have seen local, virulent populations, which were genetically different from one another. The model therefore assumes that mutants to virulence are quite rare, and that the pathogen reproduces and disperses sufficiently rapidly for its propagules to be quickly dispersed over a wide area. The adaptation of E.g.f.sp. hordei to new resistances through the emergence of a genetically uniform pathogen population may therefore be applicable to other pathogens which have high dispersal rates, but not to those with more restricted dispersal rates. The spectacular epidemics of stem rust on wheat in the northern prairies of the USA earlier in this century were often caused by one physiologic race of (P. graminis) P.g.f.sp. tritici. For instance, race 56 caused severe rust on the bread wheat variety Ceres in 1934 and 1937, while race 15B devastated durum wheat in 1953 and 1954 (Stakman, 1955). It is tempting to speculate that, had modern methods of molecular analysis been available, races such as these might have been identified as clones. In barley mildew, therefore, and perhaps in other crop diseases, the breakdown of a resistance occurs through the evolution of one clone, or very few clones, of the pathogen. This process differs from that in the theoretical cycle. The model assumes that each virulence is an independent factor, the dynamics of which depend only on its own fitness. As with resistant varieties, however, the entity that is selected is not a single gene, but an entire genotype.

3. Reselection of a Virulence by a Recycled Resistance Once a virulence gene has evolved in E.g.f.sp. hordei, however, the subpopulation of individuals that carry it rapidly becomes genetically diverse, either by selection of further mutants (Wolfe etal., 1983) or by recombination (Welz and Kranz, 1987; Brown and Wolfe, 1990). Therefore, when a resistance gene is used again, in a subsequent cycle, it is faced by a genetically diverse population of the pathogen, in which the selected virulence is less tightly associated with other characters. In this situation it might be expected that the dynamics of well-established virulences would fit theoretical predictions. This indeed appears to be the case, since the frequencies of virulence genes in the E.g.f.sp. hordei population in a barley-growing area in Denmark were found to be generally close to the values expected from a simple model (Hovm~ller etal., 1993). The contrast between these two kinds of selection for virulent isolates emphasizes that the population genetics of plant pathogens are inseparable from their population structure. Our understanding of the evolution of host-pathogen interactions in crops must be based on a broad view of the ecology of the disease, rather than on simple principles drawn from the theory of natural selection in large, outbreeding populations (Barrett, 1987; Frank, 1992; Thompson and Burdon, 1992).

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4. The Fate of Unnecessary Virulence In the fourth phase of the simple, model cycle, virulences that are no longer necessary for infection of the plant population cause a reduction in the fitness of pathogens that carry them, so that their frequency decreases. However, there is no evidence that selection against unnecessary virulence is a general phenomenon (Parlevliet, 1981 ; Antonovics and Alexander, 1989), although Leonard (1969) presented an important counter-example, in which the possession of virulence genes reduced the competitive ability of isolates of oat stem rust (P. graminis f.sp.

a0enag), The actual behaviour of virulence genes which become unnecessary for infection of the crop can be understood in relation to the pathogen' s population structure. When a resistance gene is withdrawn from commercial varieties, the frequency of the corresponding virulence may either rise or fall (point 11 in Fig. 2). The direction in which it changes depends on the sign of the covariance, or gametic disequilibrium, between it and virulences that are required to overcome the resistance of new varieties (Hovm~ller et al., 1992; Brown, 1994). If the newly selected virulences occur in clones which do not carry the old, unnecessary virulence, so that gametic disequilibrium is negative, the frequency of the old virulence will fall. However, if the old and new virulences are associated, so that gametic disequilibrium is positive, the frequency of the old virulence can rise. For instance, the clone of E.g.f.sp. hordeiwhich broke the resistance of Triumph barley had three unnecessary virulence genes, which matched resistances that were no longer used in commercial barley varieties (Brown and Wolfe, 1990). These virulences persisted in the population of E.g.f.sp. hordei, because of their association with the virulence V(Ab), which was required to infect Triumph (the letters following V in the symbol for a virulence gene correspond to the suffix of the matching Ml resistance gene). The frequency of one of these unnecessary virulences, Va6, later fell, because the clone that broke the resistance of Klaxon carried its avirulence allele (Brown etal., 1993). This effect, known as hitch-hiking selection, is particularly strong in pathogens that reproduce clonally, being greatly weakened if even a limited amount of sexual reproduction breaks up gametic disequilibrium (Brown, 1994). Even if there were a small cost associated with virulence, the fact that fitness is characteristic of the entire genome in a clonal pathogen means that a virulence need not be counterselected, if it is associated with genes that are positively selected (Osterg~trd, 1987; Brown, 1994). Consequently, after a resistance gene is no longer used, the frequency of the corresponding virulence gene may fall, rise or stay constant.

5. Durable Resistance A final, and most important, way in which agricultural systems deviate from the simple, theoretical models is that not all resistances select increased virulence (point 7 in Fig. 2). Many are durable, in that they have remained effective despite being exposed to large amounts of pathogen inoculum (Johnson, 1984). The failure of pathogens to adapt to durable resistances is discussed further below.

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6. Co-evolution of Plants and Pathogens in Agriculture To understand the co-evolution of crops and their pathogens, we must indeed consider the selection for resistance exerted by the pathogen population, and that for virulence imposed by the crop, which occurs in theoretical models of natural systems. However, although these model systems provide some insights into the evolution of pathogens on crops, there are many features of agricultural systems which differ from the simple, theoretical predictions. Among those that must be considered are, on the plant side, the need for breeders and farmers to balance many factors in producing and growing new varieties, the possibility of combining several resistances in a single variety and the existence of durable resistances. We must also take account of the processes by which pathogens adapt to new resistances, by mutation, recombination or migration, the unique population structure of each pathogen, caused by its ecology and epidemiology, and, consequently, the often unpredictable changes in virulence gene frequencies. Proposals for managing resistance genes, in order to control diseases reliably, can be evaluated against the background of the boom-and-bust cycle and the ways in which it is modified in agriculture.

IV. RESISTANCES IN MONOCULTURE A. Durable Resistance By no means all resistances that have been used in crops grown in monoculture have broken down. Indeed, the history of plant breeding includes many examples of successful control of diseases by durable resistances, which have remained effective despite prolonged, widespread use in environments that are favourable to the disease (Johnson and Law, 1975). Durable resistance has been discussed frequently in the plant pathological literature, both in general terms and in relation to many specific diseases, for instance by Johnson (1984, 1993). From a pathogen's point of view, a resistance gene may have a durable effect for two reasons. Firstly, the epidemiology of the disease may prevent rapid evolution, in that a resistant variety may not be exposed to large amounts of inoculum, so that there is relatively little opportunity for the pathogen to adapt to it. Secondly, a genetic factor may prevent the pathogen from adapting quickly to a resistance, despite its population size being large. Johnson (1984) has emphasized that durability is only a description about the past behaviour of a resistance. Even if a pathogen population has so far been unable to adapt to a resistance, it cannot be guaranteed that it will continue to fail to do so. The example discussed in the next paragraph illustrates this point.

1. Durability and Epidemiology The first case is illustrated by the resistance of barley to wheat vtem rust, P.g.f.sp. tritici, (Steffenson, 1992). This disease was previously serious in the Red River

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Valley, a major barley-producing region in the northern part of the American prairies. Since 1942, barley varieties in this area have been protected against stem rust by resistance based on the gene Rpgl. For over 40 years, losses due to rust were minimal. However, a race of P.g.f.sp. tritici, Q C C , virulent on Rpgl cultivars, was first detected in Canada in 1988 (Martens et al., 1989), and caused moderate epidemics during 1990 and 1991. The longevity of the Rpgl resistance was at least partly due to epidemiological factors, rather than purely to properties of Rpgl itself. One factor was that barley is sown and harvested early in the Red River Valley, so that crops probably escaped the worst damage from rust inoculum blown northwards, from Mexico and Texas towards the northern prairies, on the 'Puccinia pathway'. Another was that the population size of P.g. f.sp. tritici was reduced by the use of resistant varieties of another host, wheat, and by the barberry eradication programme. If these two factors did indeed reduce the population size of the pathogen, they would also have reduced the number of virulent mutants that might have started an epidemic of stem rust on barley.

2. Durability and Genetics The second reason for durability is shown by another barley disease resistance gene, mlo. This gene has provided almost complete control of powdery mildew since its introduction into commercial varieties in 1979 (JCrgensen, 1992). Like Rpgl, mlo fits Johnson's (1984)definition of durable resistance, since varieties carrying it have been grown on a total of several million hectares in northern Europe, an environment which is not only highly conducive to barley mildew, but in which mildew is extremely common. Unlike mlo, other single genes for mildew resistance, which fit the gene-for-gene model, have broken down within 2-4 years (Wolfe and Schwarzbach, 1978; Wolfe, 1984; Brown etal., 1991). The apparent inability of E.g.f.sp. hordei to adapt to mlo may be due to the mechanism of this resistance, which differs from those of race-specific resistances (JCrgensen, 1992). Isolates of E.g.f.sp. hordei with increased aggressiveness towards mlo have been selected in the laboratory, although they formed fewer colonies than wildtype, virulent isolates did on varieties without mlo (Schwarzbach, 1979). However, isolates with even this low level of increased aggressiveness have apparently not yet been selected in natural populations by the extensive cultivation of mlo varieties (Schwarzbach, 1987; Andersen, 1991). This lack of adaptation by E.g.f.sp. hordei indicates either that mutants to high aggressiveness on mlo barley occur at an extremely low frequency, and are thus very rarely available to be selected on these varieties, or that mlo-aggressive mutants have low fitness, which outweighs favourable selection by the resistant host.

3. The Absence of General Models for Durable Resistance The durable Rpgl and mlo resistances illustrate a common misconception about durable resistance. Following the experiences of Vanderplank (1968) in breeding potatoes for resistance to late blight (Phytophthora infestans), some pathologists have assumed that resistances that are based on single genes, and which provide

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complete protection against disease, will break down rapidly, while polygenic resistances that do not show a hypersensitive response to infection will be more durable. Some durable resistances are indeed polygenic, but some such resistances have been found to have some degree of race-specific effect on the pathogen (Parlevliet, 1993). However, many more durable resistances than the two discussed above are based on one gene or other simple genetic systems (Johnson, 1984, 1993). There is no single model for durable resistance, either for its genetic control or for the phenotype of its expression. A corollary of the absence of a single model is that there is no simple formula for breeding for durable resistance, to which a pathogen will not be able to adapt. A sensible strategy is to select resistant progeny from crosses of parents with durable resistances, but the success of even this method cannot be absolutely guaranteed (Johnson, 1984, 1993). Breeding for durable resistance to a particular disease must be firmly based on knowledge of the genetics of both the host and the pathogen, rather than on broad, general concepts. However, a long-term commitment to breeding for durable resistance may be repaid by success. In Australia, for example, stem rust of wheat has declined greatly in importance through such a programme (McIntosh, 1992).

B. Strategies for Introducing New Resistance Genes

1. Pyramiding Resistance Genes As an alternative to introducing each new resistance gene by itself in a separate cuhivar, several resistances could be combined in a single variety. This strategy, of deploying pyramids of resistance genes, might prolong the usefulness of the resistance genes if a pathogen could only reproduce on the resistant variety if it carried all the virulences matching the genes in the pyramid. In theory, the probability that a single, mutant individual would arise, with independent mutations to all the virulences, should be extremely low. The aim of pyramiding new resistance genes is therefore to reduce the pathogen's effective rate of mutation to virulence. However, pyramiding has not been uniformly effective in providing durable resistance. The enormous size of many pathogen populations allows multiple mutants to appear, and furthermore, in some cases, the frequency of mutation to multiple virulence may be higher than the product of the separate mutation rates (Mundt, 1990). While many resistance pyramids have broken down, those that have been most effective appear to have been particular combinations of resistance genes. In North America, combinations of resistance genes which have included Sr2 have provided durable resistance to stem rust, while gene combinations including Lrl3 or Lr34 have been durably effective in controlling leaf rust (Puccinia recondita f.sp. tritic0 (Kolmer etal., 1991). Mundt (1991) suggested that some such resistance pyramids may be durable because pathogen races with the corresponding combination of virulences lack

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fitness. This hypothesis is certainly worth further exploration, since at least one virulence, matching the Cf9 resistance of tomato to Cladosporiumfulvum, is caused by deletion of the region of chromosome which carries the avirulence gene, avr9 (van den Ackerveken et al., 1992). Fitness might be reduced if the deletion of avr9 also caused the loss of other functions in the pathogen. Isolates of C. fulvurn that lack avr9 have not been found in cultivated tomato crops (R. P. Oliver, pers. comm.), but as yet, the contributions to fitness of the virulence and avirulence alleles have not been compared. Resistance gene pyramids are also likely to have greater durability if the pathogen has a wholly asexual life cycle, and cannot bring together separate mutations by recombination (Marshall, 1977). Combinations of resistance genes have provided good resistance to wheat stem rust in Australia for many years (Mclntosh, 1992). One factor that might favour this is that the alternate host of P.g.f.sp. tritici does not occur in Australia. Breeders can therefore create combinations of resistance genes in new varieties which are effective against current races of P.g.f.sp. tritici, and even against races which might arise in future, by a small number of mutations, without having to fear the rapid emergence of virulent, recombinant pathogen clones. Pyramiding has provided some successful, durable resistances, but in future, the use of molecular genetic markers to tag genes might make it easier to introduce a group of several resistances into a new variety. For instance, there are two sources of durable resistance to eyespot of wheat, caused by Pseudocercosporella herpotrichoides. One is derived from the French variety Capelle Desprez, the other from V P M , derived from a cross of wheat with a wild grass, Aegilops ventricosa. Molecular markers linked to both these resistance genes have been discovered (Worland et al., 1988; Koebner and Martin, 1990). Plants with both genes have better eyespot resistance than those with either alone (Doussinault and Douaire, 1978). It is difficult to assess levels of eyespot infection accurately, so the use of molecular tags should make it easier for breeders to select plants that carry both resistances.

2. Introducing Resistance Genes Separately By contrast, breeders have sometimes introduced different resistances into cultivation in different varieties, intentionally or otherwise. Some resistances cannot be combined in a single variety, since, in several plants, genes for resistance to one disease are clustered, with many alleles mapping to a single locus (Pryor and Ellis, 1993). When resistance genes are introduced separately, virulences matching the different resistances usually evolve in different pathogen clones, so that gametic disequilibrium between the virulences is negative (Osterg~rd and Hovm#ller, 1991). Such a situation arose in the E.g.f.sp. hordei population in Britain in the 1970s, when different barley varieties with Mla7 + Mlk, Mlal2 or MILa were introduced. The gametic disequilibria between the matching virulences were strongly negative, especially those between Va7 and VLa and between Val2 and Va7 (Wolfe, 1984).

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The fact that different fractions of the pathogen population carried different virulences could be exploited in the design of variety mixtures (Wolfe, 1985) or diversification schemes (Priestley and Bayles, 1980). However, any such benefits are likely to be short-lived if the pathogen has a sexual phase in its life cycle, as does E.g.f.sp. hordei. Races with the combination of virulences required to overcome the combined resistances could be produced by sexual recombination between those with the separate virulences (Wolfe and Barrett, 1976). The composition of the E.g.f.sp. hordei population that broke the resistance of Klaxon is at least consistent with this hypothesis (Brown etal., 1993).

C. Managed Deployment of Resistance Genes Both the identification of durable resistances and the creation of resistance gene pyramids aim to create single varieties in such a way as to restrict the evolution of virulent pathogens. A different approach which aims to limit pathogen evolution is to manage the deployment of varieties in order to control the spread of virulent pathogen populations.

1. The Puccinia Pathway in North America Several pathogens are dispersed over long distances by the wind. A number of proposals have been made to exploit this aspect of their epidemiology in schemes for prolonging the effectiveness of resistance genes. One of these sought to exploit annual movements of populations of the oat crown rust pathogen, Puccinia coronata, through three geographical zones, during the late 1960s and the 1970s (Frey etal., 1977). This fungus overwinters on the small area of production of winter oats in northern Mexico and the southern USA. In spring, spores move through a second region, the central prairies in the USA, and finally, in summer, infect spring oats in the northern USA and southern Canada. Plant breeders in these three regions agreed to use different crown rust resistance genes in their oat breeding programmes. The aim of this plan was to impose selection for different virulences in populations of P. coronata in the three regions. The southern rust population would then be unable to infect the northern oat crop in spring, and vice versa in autumn. However, a sharp decline in the area sown to oats led to this scheme being abandoned because it was too administratively complex to be worthwhile (Mundt and Browning, 1985). A similar proposal was made by Knott (1972), to control stem rust of wheat, caused by Puccinia graminis f.sp. tritici. Dividing the North American continent into the same three areas as described in the previous paragraph, Knott proposed that breeders in the southern zone should use resistances that were not race specific, or else race-specific resistances that were not to be used further north. However, this proposal has not been implemented.

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2. Mildew Resistance Genes in Europe Another proposal for the spatial deployment of resistance genes was based on movements of the barley mildew pathogen across Europe over several years. Several changes in frequencies of virulence genes are consistent with populations of E.g.f. sp. hordeimoving from west to east, in the direction of the prevailing wind, by about 110 km each year (Limpert, 1987a, b). Using these results, Limpert and Fischbeck (1987) proposed that new genes for mildew resistance should be introduced first in countries in eastern Europe. Later, they could be used in countries successively further west. Limpert and Fischbeck (1987) predicted that these genes would still be effective in more westerly countries, because the local population of mildew clones would not include virulent immigrant spores from the east. This proposal has, in fact, been subjected inadvertently to a test, and its effectiveness disproved. The barley mildew resistance gene Mlal3 was introduced into cultivars first in Czechoslovakia in 1978 (Br/ickner, 1987; Dreiseitl, 1993), then in Germany and Scandinavia in the early 1980s (Brown and J~rgensen, 1991), then in the British Isles in 1986, where Val3 mildew first became common in 1988 (Brown et al., 1991). One of the two clones which broke down the Mlal3 resistance was indistinguishable from samples obtained earlier in Czechoslovakia (Wolfe et al., 1992). The ineffectiveness of Limpert and Fischbeck's (1987) plan can be understood by considering the epidemiology of barley mildew further. Two patterns of wind dispersal of mildew in Europe can be distinguished, one of which is the gross movement of populations of E.g.f.sp. hordei by the prevailing wind over some 110 krn each year (Limpert, 1987a, b). On the other hand, individual spores of E.g.f.sp. hordei have been found to be blown several hundred kilometres, across the North Sea, in a single day (Hermansen et al., 1978). This latter form of dispersal presumably occurs whatever the direction of the wind. Easterly winds are unusual in Europe, but do occur several times a year. The combined epidemiological and genetic evidence indicates that it is highly probable that the mildew epidemic on Mlal3 barley was initiated by spores from further east. Even a single dispersal event would have been sufficient, since, to a virulent spore, a field of a resistant variety would be an unoccupied niche, and therefore, once a single infection was established, a potential focal source of disease propagules. Although bulk spore movement is from west to east, the possible dispersal of spores by the wind in every direction in Europe apparently allows epidemics to be initiated in ways that are not necessarily consistent with the prevailing wind. 3. Lettuce Downy Mildew: Combining Resistance Genes with Fungicides The failure of schemes for deploying resistance genes in cereals contrasts with the success of a management plan for genes for resistance to downy mildew (Bremia lactucae) in lettuce grown under glass or other protection in England (Crute, 1989, 1992). There is a long history of breeding lettuce for downy mildew resistance but, between 1978 and 1983, mildew was effectively controlled by a fungicide, metalaxyl (Crute, 1987). Between 1983 and 1986, a strain of B. lactucaewhich was

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resistant to phenylamide fungicides, including metalaxyl, caused failures of mildew control (Crute etal., 1987). It was recognized that the most common phenylamide-resistant isolates carried avirulence towards a resistance gene, Dm11, which was present in several varieties at the time. Control of mildew was therefore re-established by advising lettuce growers to use varieties with Droll and to treat them with metalaxyl (Crute, 1989, 1992). This strategy provided good control for a time, until metalaxy-resistant isolates of B. lactucae, virulent on Dm11, became common. However, these isolates were avirulent on the resistances Dm6, Din16 and R18, so metalaxyl could still be used to control mildew on varieties which had one of these resistances (Crute, 1992). Two factors have contributed largely to the success of this scheme for controlling lettuce downy mildew. Firstly, the disease presents a severe economic threat to growers. Sales of lettuce depend to a large extent on heads being seen, by consumers, to be of high quality. Even modest blemishes, caused by disease, can render the crop unmarketable. The high cost of mildew infection therefore means that growers are receptive to workable schemes for controlling it (Crute, 1989). Secondly, several effective resistance genes are present in advanced breeding material. Selections from these lines, which have both a chosen combination of downy mildew resistances and good, marketable quality, can be multiplied and entered into trials in as short a time as one season after new resistance gene combinations are demanded. Lettuce breeders can therefore respond effectively to pathologists' recommendations (I. R. Crute, pers. comm.). In cereals, by contrast, low levels of diseases on cereals do not greatly affect the market value of the crop, while the long lead time required to produce a new variety means that breeders cannot respond immediately to advice from pathologists. These factors have, no doubt, been partly responsible for the lack of enthusiasm for resistance gene management schemes in cereals.

V. GENETICALLY DIVERSE CROPPING SYSTEMS A. Multilines and Variety Mixtures An alternative to monoculture is the use of heterogenous cropping systems, in which seeds of several varieties of a crop species are sown in the same field. Two forms of this kind of cropping have been studied. Multilines are mixtures of different lines of a single variety, differing mainly in their resistance to one disease (Browning and Frey, 1969). They can be developed by introducing different resistance genes into the genetic background of the chosen variety by backcrossing (e.g. Briggle, 1969; K#lster etal., 1986). In variety mixtures, by contrast, different varieties, each with different genes for resistance to the target disease, are sown together (Jensen, 1952; Wolfe and Barrett, 1980; Mundt and Browning, 1985; Wolfe, 1985). Both multilines and variety mixtures can produce considerable reductions in

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the severity of disease. This can lead to lower expenditure on fungicides, improved yield and quality and greater stability of performance across different environments and in different years (Wolfe, 1985). Mixed varieties have several advantages over multilines, in that they can control diseases other than the one that is the primary target for control and can also buffer the crop against nonbiological stresses, so that temporal and geographical variation in the crop's performance is reduced (Mundt and Browning, 1985; Wolfe, 1985). However, one of the major obstacles to the widespread use of spring barley mixtures in Britain has been the reluctance of maltsters to consider using a variety mixture, because of the possible differences in malting quality of the component varieties (Wolfe, 1984). If the market requires a highly uniform end product, multilines should be acceptable even when variety mixtures are not, because of their greater genetic uniformity in characters other than disease resistance (Wolfe, 1985).

1. Control of Disease in Mixtures Mixtures - whether multilines or mixed varieties - control disease in several ways. The principal mechanisms are epidemiological, in restricting the spread of spores from one compatible host to another. If a clone of a pathogen is virulent on some varieties in a mixture, but not on the others, its rate of increase is reduced, partly because the distance between susceptible host plants is greater than in a stand of a pure variety, and partly because resistant plants act as barriers to spore dispersal (Burdon, 1978; Chin and Wolfe, 1984a). A physiological mechanism may also restrict the growth of virulent pathogens in mixtures. This is induced resistance, a process in which prior infection by an avirulent pathogen limits the development of a later infection by a virulent one. This would enhance the effect of a mixture if each plant were infected by a population comprising both virulent and avirulent spores (Chin and Wolfe, 1984a). Induced resistance is a rather weak, localized effect in cereals, both in response to rusts (Johnson, 1978) and mildew (Woolacott and Archer, 1984; Martinelli, 1990). However, in many dicotyledonous crop species, which express induced resistance strongly (Kuc, 1982), it might be exploited in designing mixtures. Many theoretical studies of the behaviour of pathogen populations in mixtures can be interpreted in terms of the distance and barrier effects. It has been proposed that the reduction of disease in a mixture, compared to a pure variety, depends on the relative rates of autodeposition of spores, on the plant on which they were formed, and allodeposition, on other plants. If the varieties in a mixture are fully randomized, increasing allodeposition would increase the effectiveness of a mixture, since both the distance and barrier effects would make greater contributions to reducing the severity of disease, because the rate of transmission of spores between plants is restricted (Barrett, 1980; Ostergaard, 1983). More generally, increasing the probability of alloinfection, by increasing the chance that a spore would land on a plant of a different variety to that on which it was formed, has been predicted to increase the effectiveness of a mixture (Mundt and Leonard, 1986; Mundt et al., 1986). This probability can be manipulated experi-

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mentally by altering the layout of the mixture, such that the unit areas occupied by plants of the same variety are varied. Reducing the unit area would increase the barrier effect, and thus reduce the rate of successful alloinfection.

2. Pathogen Populations in Mixtures: Theory Interest in the genetic adaptation of pathogens to mixtures has focused on the prediction that races of the pathogen, capable of attacking all varieties in the mixture, may be selected. The evolution of such super-races, and their importance relative to simpler races, is favoured in theoretical models if there is little or no selection against unnecessary virulence (Groth, 1976; Barrett and Wolfe, 1978; Marshall and Pryor, 1978). A second factor which is predicted to favour complex pathogen races is a high rate of allodeposition, so that there is a relatively high probability of spores, formed on one variety, infecting another (Barrett, 1978, 1980; Ostergaard, 1983). Barrett (1980) showed that, if the rate of allodeposition is low, complex races of the pathogen may be favoured early in the epidemic, when a pathogen clone which is able to infect all components of the mixture would have an advantage. Later, simple races should replace the more complex ones, because, once the disease is well established, individuals with optimum fitness on one host variety would be favoured. With a high rate of allodeposition, however, complex races would predominate and ultimately become fixed. To summarize the conclusions of these theoretical models, the dynamics of pathogen race frequencies depend on the balance between the advantage to the pathogen of being able to reproduce on a greater proportion of the mixture and the cost of the ability to infect more varieties successfully.

3. Pathogen Populations in Mixtures: Data There have been comparatively few attempts at critical tests of hypotheses about the evolution of pathogen populations in mixtures. The influence of pathogen fitness on the evolution of complex races has been particularly neglected. However, the hypothesis that greater alloinfection would favour more complex races has been tested. Huang et al. (1994) investigated the selection of races of E.g.f. sp. hordei, capable of attacking all three varieties in a barley variety mixture, in relation to the relative proportions of auto- and alloinfections. They studied changes in race frequencies in pure stands and in four layouts of mixture. In one type of mixture, plants of the three varieties were sown randomly, so that the host genotypes were thoroughly mixed. The three other types of mixtures were sown as alternating rows, with blocks of one, three or six rows of the different varieties. The rate of alloinfection therefore decreased in the different types of plot, going from random mixtures, through one-, three- and six-row mixtures, to pure stands. There was no evidence that more complex pathogen races, with virulence on more varieties, had a selective advantage over simpler races in pure stands or in six-row mixtures. The rate of selection for complex races was successively greater, however, in three-row, one-row and random mixtures. The hypothesis

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that greater alloinfection would favour more complex races of mildew could therefore be accepted. Other reports of experimental work on pathogen evolution in mixtures have described changes in the composition of the population and commented on possible reasons for these observations. Munk (1983) found an increase of complex races of E.g.f.sp. hordei in a mixture of seven barley varieties with different mildew resistance genes, in which there was a particularly high rate of alloinfection. Chin and Wolfe (1984b) found selection for complex races in some mixtures, but not in others. In some experiments, simple races predominated on plants of one variety in a mixture, but complex races on another. Observations of race frequencies in field trials are consistent with Barrett's (1980) prediction that complex races may be favoured at the start of the season and later replaced by simpler ones (Barrett and Wolfe, 1980). The greatest use of variety mixtures in modern agriculture was in the former German Democratic Republic (GDR), where most spring barley was grown as mixtures between 1984 and 1991 (Wolfe et al., 1992). However, the genetic diversity in these mixtures was limited. Most mixtures included varieties with the mildew resistance genes Mlal2, Mlal3 and mlo. In a survey carried out in 1990, there was a significant increase in the frequency of pathogen races with combined virulence for the two race-specific genes, Mlal2 and Mlal3; as mentioned above, mlo is still effective against all known clones of E.g.f.sp. hordei. In 1991, however, the frequency of the complex race, with Val2 + Val3, fell relative to that of simple races, which carried either Val2 or Val3, but not both (Schaffner et al., 1992). Isolates with the combined virulence were generally more sensitive to ergosterol C14 demethylation inhibitor (DMI) fungicides than isolates with single virulences, so the increased use of D M I fungicides during 1991 m a y h a v e selected against the complex virulence (Wolfe et al., 1992).

4. Pathogen Fitness in Mixtures Theoretical analyses of the fitness of pathogens in mixtures have concentrated on the cost of unnecessary virulence genes, which allow a pathogen to overcome racespecific resistances. However, a more general aspect of pathogen fitness is adaptation to different host varieties. Many other genes in a plant, apart from recognized resistance genes, may affect quantitatively the ability of an individual pathogen isolate to grow and reproduce. If there were no such adaptation to the genetic 'background' of a plant variety, one would expect a mixture of different varieties, carrying the same resistance genes, to have a similar level of disease to that on the varieties grown as pure stands. However, three different barley mixtures, each of which consisted of three varieties with the same identified resistance genes, all reduced the amount of mildew substantially compared to that on pure stands of the same varieties, although the reduction was not as great as that in a mixture of three varieties with different resistances (Wolfe et al., 1981). Unidentified, 'background' genes may therefore have influenced the performance of these mixtures.

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There is some evidence for adaptation of pathogens to different varieties in several diseases. Adaptation of this kind, not governed by race-specific resistances, has been found in potato late blight, with isolates of P. infestans being better adapted, in general, to the potato variety from which they were isolated than to other varieties (Jeffrey et al., 1962; Caten, 1974). In work on other diseases Leonard (1969) observed adaptation of (P. graminis) P.g.f.sp. avenae to Craig or Clintand A oats, Clifford and Clothier (1974) detected adaptation of brown rust (Puccinia hordes) isolates to the barley varieties Julia, Sultan or Vada, and Chin and Wolfe (1984b) discovered isolates of E.g.f.sp. hordei which were differentially adapted to Hassan or Wing barley. Clearly, future results on changes in the composition of pathogen populations in variety mixtures need to be interpreted in relation to the fitness of isolates on varieties, not just in terms of the costs and benefits of particular race-specific virulences. If adaptation of isolates to varieties' genetic backgrounds is indeed a general phenomenon, a mixed variety should be expected to provide better control of disease than a muhiline, the components of which carried the same resistance genes as did the varieties in the mixture. I am not aware that this hypothesis has been tested.

5. Predicting the Peorormance of a Mixture A further, important question which has not received much attention is the extent to which the genetic composition of a pathogen population affects the performance of a mixture. MartineUi (1990) predicted that a mixture of varieties with different resistance genes, effective against different fractions of the pathogen population, would control disease more effectively than a mixture in which the resistances in the different varieties were effective against the same pathogen clones. In a field trial, the choice of varieties to include in mixtures was made on the basis of knowledge of the frequencies of virulence genes and genotypes in the previous year. The prediction was confirmed. A mixture of three varieties which were susceptible to mildew, but to different clones of E.g.f.sp. hordei that were then prevalent in the population, was more effective in reducing disease and increasing yield than a mixture of three other varieties, which also carried different resistances but which were susceptible to the same, common clones of E.g. f.sp. hordei. These results indicate that the value of a mixture might be optimized by choosing the component varieties carefully, taking into account the contemporary genetic composition of the target pathogen (Wolfe and Barrett, 1980). Much of the theory of the genetic composition of pathogen populations in mixtures has studied equilibrium frequencies of genotypes (Groth, 1976; Barrett and Wolfe, 1978; Marshall and Pryor, 1978; q)sterg~trd, 1983). Martinelli's (1990) results, however, indicate that the long-term equilibria of genotype frequencies, and the question of whether simple or complex races will predominate, is essentially irrelevant to the performance of a mixture in any given season. Much more significant is the composition of the population at the start of that season itself, since a pathogen goes through a small number of

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generations in each season, and the effect that the mixture is expected to have on that population.

B. Diversification Schemes A less extreme type of genetic heterogeneity than variety mixtures is diversification of varieties between fields (Priestley and Bayles, 1980). A farmer using a diversification scheme would plant neighbouring fields with varieties which, if not resistant, are susceptible to different races of the pathogen. This is a form of deployment of varieties in monoculture, but the principle is the same as that of variety mixtures, since the pathogen is being manipulated through its inability to grow on more than one variety. It might be expected that this kind of varietal diversification would not control disease very effectively if spores were mainly dispersed to other plants in the same field, as is the case for many foliar diseases. Studies of oat crown rust showed that this is indeed the case if the initial inoculum is dispersed evenly over the crop (Mundt and Leonard, 1985). However, inter-field diversification can inhibit the spread of a pathogen if an epidemic is initiated from a strongly focal source, by disrupting the progress of the epidemic front (Mundt and Leonard, 1985; Mundt and Brophy, 1988). Diversification schemes might therefore provide some control of diseases which are dispersed from a few point sources, but be relatively ineffective against diseases which are well dispersed at the start of each year's epidemic, as are powdery mildew and yellow rust of cereals in Britain.

Vl. UNIFORMITY OR DIVERSITY? Monoculture is a highly attractive system, both for farmers and for consumers. For the farmer, it offers the opportunity to choose the varieties that will return the greatest profit, and to maximize the efficiency of his operations. For consumers, especially those that are food-processing companies, it allows optimization of production runs and thus savings in costs (Marshall, 1977). However, monoculture clearly has risks, because of the rapid adaptation of pathogen populations to crop varieties. Monoculture need not be abandoned, but in order for it to be successful, the performance of crop varieties should be predictable. Clearly, this is not so if crops are vulnerable to the sudden, unpredictable emergence of virulent pathogens. Durable resistance is therefore an essential component of successful monoculture. Whether it is achieved by the chance discovery of genetic systems which provide effective resistance, or by the deliberate combination of proven genes, there is no single formula for durable resistance (Johnson, 1984, 1993), and no substitute for hard work and good luck. Mixed varieties have proved to be effective in controlling many diseases

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(Wolfe, 1985), and are a valid alternative to chemical control of disease. They offer the possibility of increasing yields, or at least stabilizing them, while reducing input costs. From a pathologist's point of view, some questions about the control of disease in mixtures need to be answered by further research. However, the greatest obstacle to the use of.mixtures is the demand for uniform produce. Much of the output of cereal production in the industrialized world is used for animal feed; here the progress of mixtures should not be limited by the fastidiousness of consumer demand. For many other uses of cereals and other crops, the require: ment that produce should have predictable characteristics may be more justified. Perhaps the greatest need for research on mixtures is therefore in assessing whether the produce of variety mixtures is indeed more variable in quality than that of pure lines and, if it is, in reducing this variation to such a level that mixtures can be used to provide the raw material for food and drink processing. At present, many farmers face a multitude of conflicting pressures, many of them political in nature. Much of the general public demands that farms should be run on environmentally benevolent lines and, at the same time, wishes to buy high quality produce, free of disease. The political insistence on reducing the production of crops which are in surplus conflicts with the need of farmers to increase output, because of falling prices. Whether they are presented within the framework of uniformity or diversity, plans for controlling disease by the use of genetic resistance must take account of the economic pressures on farmers and, in particular, must allow them to grow the most profitable varieties.

ACKNOWLEDGEMENTS

I thank John Barrett, Roy Johnson, Chris Mundt and Martin Wolfe for helpful comments on a draft of this review, and Ian Crate for discussion on lettuce downy mildew. Work on cereal pathology at the John Innes Centre is supported by the Ministry of Agriculture, Fisheries and Food.

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THREE SOURCES FOR NON-CHEMICAL MANAGEMENT OF PLANT DISEASE: TOWARDS AN ECOLOGICAL FRAMEWORK Alan Maloney Department of Plant Pathology, Cornell University, Ithaca, NY 14853, USA

I. II. III. IV.

Goals for Disease Management in the Coming Decades Context: Sustainability Sustainability and Non-chemical Approaches to Disease Management Non-chemical Disease Management-Three Lines of Research A. Traditonal Farming: Learning from Sustainable Peasant Agriculture B. Role of Biotechnology (Molecular Biology) in Developing Alternatives to Chemical Disease Management C. Biological Control V. Conclusions Acknowledgments References

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I. GOALS FOR DISEASE MANAGEMENT IN THE COMING DECADES The growing interest in non-chemical methods of disease control, pest management and weed control are in part a reaction to the environmental and health hazards resulting from modern agriculture's enormous dependence on chemical inputs. Some of the problems associated with the chemical paradigm of modern agriculture as currently practiced are pollution and negative health effects resulting from toxicity, overuse and overdependence on chemical pesticides, large inefficiencies of energy and resource use, interruption of natural ecological nutrient cycling, land and water degradation, and destruction of biological communities that otherwise support crop production. Practices that use or disperse fewer chemicals, whether in agriculture or in other industries, are perceived as more beneficial, because they offer the promise of less environmental pollution. Other problems associated with the chemical paradigm of modern agriculture are economic in nature. To be certain, improved agricultural productivity has been achieved in many cases, especially as measured by macroeconomic criteria in the short term. However, this apparent progress has often been undermined by other effects of modern agriculture: pollution and illness, concentration of ADVANCES IN P L A N T P A T H O L O G Y - - V O L . 11 ISBN 0-12-033711-8

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economic power, disempowerment and displacement of rural communities, rampant land degradation, and wholesale loss of traditional knowledge and social structures. Because of the narrower margin for absorbing failure in agrarian societies, these social costs may be more apparent in the developing countries. Social, political and economic critiques have been leveled at modern agriculture, and its promotion in developing countries (Altieri, 1987; Blaikie and Brookfield, 1987; George, 1990; Wright, 1990). According to these critics, agriculture that depends less on the chemical paradigm and industrial technology is perceived as more beneficial, because it allows for more stable economic and social/political structures in agriculture. My intention here is to present a conceptual framework that identifies three different lines of research that can contribute to non-chemical approaches to disease management. These are traditional farming practices, biotechnology and biological control. In addition, a revised definition of biological control will be presented. My hope is that comparing and contrasting these three categories will be useful both for analyzing existing practices and identifying fertile territory for future research directions in plant disease management. Before discussing the particular categories, I place this work in the context of agroecology and sustainable agriculture. II. CONTEXT: SUSTAINABILITY

This chapter seeks to establish ways to discover and understand how to make disease management in agriculture more environmentally sustainable. The principles of sustainability in agriculture are taken from the principles of applied ecology and agroecology. As applied ecology, agriculture must be based in basic ecological theory, including particularly r- and K-selection, island biogeography, community structure, stability and invasiveness, and succession (Thomas and Kevan, 1993). Agroecology recognizes the importance of ecological theory in agriculture, but explicitly acknowledges agriculture as a human activity, carried out within ecosystems in which human social systems are an integral part (Altieri, 1987). There are a number of criteria that can be used to evaluate whether agricultural practices and tools are ecologically sustainable: 1. Emphasizing land management for the long term (Blaikie and Brookfield, 1987) and employing practices that enhance the long-term productivity of the soil, diversifying the agricultural landscape, protecting the soil from erosion, recharging groundwater supplies and maintaining the soil organismal communities for efficient organic residue recycling and disease control. 'The wincipal basis of sustainable land use is the long-term maintenance of the productive capacity of soils' (Thomas and Kevan, 1993). 2. Putting a full array of natural processes to work directly and indirectly in

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commodity production, rather than paying to eclipse all but a few such processes. 3. Minimizing energy loss in agriculture by increasing the efficiency of energy (fossil fuel or biological) transfer between trophic levels or steps during commodity production. These are necessary, though not sufficient, criteria. Additional criteria will need to be added for local conditions or particular practices. In addition to environmental sustainability, this chapter recognizes the related issues of economic sustainability, which usually top the lists of features of sustainable agriculture. Sustainable agriculture and sustainable development have become expressed goals of most governments, the United Nations, businesses, environmental groups and trade organizations. Government policy for sustainable agriculture customarily responds to shrinking numbers of farms, diminishing farm profitability, and other aspects of an economically vulnerable agricultural sector. Its responses include setting priorities for diversifying or preserving the agricultural sector of a region (which is defacto social and environmental, not just economic, policy), and implementing a variety of policies to enhance farmers' ability to stay in business. These actions are clearly critical for maintaining farming and related agricultural practices as a part of a region's social and economic fabric: for agricultural operations to be sustainable, they must be economically viable. Therefore, in discussing disease management in the context of sustainable agriculture, we must attend to both economic and environmental sustainability and must recognize the interdependence of the two. We must recognize that humans are not separate from ecosystems, but major actors within ecosystems, and as such, humans must protect the environmental support systems that allow ecosystems to maintain themselves. A primary goal of sustainability is therefore the maintenance or rehabilitation of the environmental support systems, by bringing human activities into balance with the rest of the ecosystems in which they are carried out. Therefore, while agricultural sustainability requires that farming and other forms of agriculture must be by some definition economically viable activity, there are environmental and ecological constraints which must be attended to if human populations are to live without diminishing the capacity of their environment to sustain them. This will be an ongoing process, with dual challenges. The first is to discover and understand how to make human activities, such as agriculture, both environmentally and economically sustainable. The second is to effect those changes. Hawken (1993) has defined sustainability in a way that neatly ties together economic and environmental aspects of sustainability, in this case in a discussion of the relationship between business and the environment. He describes it primarily in relation to business in a broad sense, but it applies well to agriculture. He recognizes the tensions between economic activities and the environment, and offers some general ideals for designing those activities to replenish the environment. Sustainability is defined:

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9 in terms of the carrying capacity of the ecosystem, and described with inputoutput models of energy and resource consumption. Sustainability is an economic state where the demands placed upon the environment by people and commerce can be met without reducing the capacity of the environment to provide for future generations. It can also be expressed in the simple terms of an economic golden rule for the restorative economy: Leave the world better than you found it, take no more than you need, try not to harm life or the environment, make amends if you do. Sustainability means that your service or product does not compete in the marketplace in terms of its superior image, power, speed, packaging, etc. Instead, your business must deliver clothing, objects, food, or services to the customer in a way that reduces consumption, energy use, distribution costs, economic concentration, soil erosion, atmospheric pollution, and other forms of environmental damage (Hawken, 1993).

III. SUSTAINABILITY AND NON-CHEMICAL APPROACHES TO DISEASE M A N A G E M E N T Sustainability is a new paradigm for modern agriculture, and the design and assessment of specific practices to approach a goal of sustainability is necessarily an ongoing process. This sets a challenge to be met by researchers, farmers, and others. Answering this challenge will take the form of a dialectic between our understanding of available practices and our expanding knowledge of ecological relationships in agroecosystems. Discussions of sustainability commonly comprise discourses on 'macroecological' questions, such as fertilizer use, groundwater nitrification, soil erosion, and overall productivity 9 They rarely treat the topic of disease management, though as with all aspects of agriculture, disease management can be assessed within a conceptual framework of sustainability and a theoretical ecological framework. It must be noted that although this chapter exclusively addresses non-chemical means for disease management within a context of sustainability, it should not be inferred that any particular methodology or set of practices is a priori excluded. For instance, because organic agriculture explicitly rules out the use of external chemical inputs, some may assume that 'sustainable' agriculture is a synonym for 'organic' agriculture. I do not make such an assumption, for to believe that sustainability would be achieved only by the complete removal of chemical inputs would be far too simplistic. M u c h current design of chemical approaches to disease or pest management places a very high priority not only on efficacy and retarding the development of pathogen resistance to fungicides and insecticides, but also on the specificity and biodegradability of pesticides (De Waard et al., 1993). This trend is a direct result of environmental concerns about chemical pesticides. The place of chemical control in sustainable agriculture was addressed recently (Corey et al., 1993).

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IV. NON-CHEMICAL DISEASE MANAGEMENT: THREE LINES OF RESEARCH The remainder of this chapter consists of a discussion of the potential for research to contribute to the development of non-chemical disease management in the coming decades. Three sources of'non-chemical' disease management strategies are discussed: traditional farming systems, biotechnology and biological control. The three are rarely considered together, except as one is perceived to threaten to replace another in the development of modern agriculture. Too often it is assumed that one particular lens for agriculture is the only one that can be used. In contrast, I am proposing a different way to frame the relationship among these sources of non-chemical methods. Rather than regard traditional farming systems and biotechnology as opposing poles, I propose to view biological control as a bridge that draws from and connects these two approaches. In doing so, I hope to demonstrate the potential of all three lines of research to contribute to sustainable agricultural practices that will far exceed the results delivered to date. Furthermore, I suggest that by comparing and contrasting these approaches, we can derive fresh perspectives, tools, and practices for the development of nonchemical approaches to disease management. From judicious and balanced attention to all three, we can improve our chances to foster wisdom in our interactions with the land. This chapter recognizes the cultural basis of both science and agriculture. The term agriculture will usually be used with the modifiers 'traditional' or 'modern' to generally distinguish between peasant agriculture in developing countries and the more mechanized, high-input variety commonly associated with industrialized nations. 'Western science' will be used to denote research and development fostered mainly in and by universities and corporations in the industrialized nations. Much of this chapter refers to culturally specific practices and traditions in agriculture. To avoid confusion, the term 'cultural practices', commonly used in both agricultural and anthropological literature, will be replaced with 'agronomic practices'. In each major section devoted to different lines of research, examples will be cited only to illustrate the discussion; they will not be exhaustive.

A. Traditional Farming: Learning from Sustainable Peasant Agriculture Many traditional farming practices and systems are &facto sustainable, because they have supported sizable human populations on the same lands for hundreds and sometimes thousands of years. Sustainable traditional farming systems have evolved in many different cultures, in many different regions of the world, under a diverse variety of climatic conditions. Sustainable farming practices have developed because they have proven flexible and resilient. Traditional farming practices, as described by Thurston (1992) and many anthropologists and ecologists, are part and parcel of the practices of agrarian

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societies and traditional farming systems in particular ecological settings. Sustainability in traditional systems has not been achieved by the application of any Western definition of scientific research, but has been derived through long tenure on the same or similar land, trial and error with crops and practices, and sharing of knowledge within and among families in rural communities. Indigenous knowledge applicable to farming is site-specific and dynamic, not static. Traditional farmers in developing countries, like their counterparts in 'modern' and organic agriculture in the industrial nations are constantly experimenting (Chambers et al., 1989; Thurston, 1992), and in so doing, generating new knowledge. Some practices endure, others pass away. Indigenous knowledge of agriculture and ecosystems has been long ignored, and undermined, by Western agricultural sciences (Thurston, 1992). 'Most scientists and many of the world's farmers have abandoned traditional farming practices and systems in an effort to increase food production and income and to improve the efficiency of land and labor use' (Trutmann and Thurston, 1993). A large body of literature on traditional farming systems is already accessible, but most of it is not in the agricultural science literature. Reporting on indigenous knowledge systems has come from ' . . . anthropologists, ethnobotanists, archaeologists, and geographers- and to a lesser extent, ecologists, economists, and sociologists...' (Thurston, 1992). In any case, it has been done by scientists and social scientists who have attempted to understand not only the specific practices but also the cultural underpinnings of these practices. Crossing geographic and cultural divides between industrial agricultural and traditional systems is seriously needed in agricultural science. If our goal is to develop sustainable agricultural practices, it seems reasonable to try to understand how these practices work. The importance of understanding such practices in the context of agricultural sustainability is easily established, because many of the features of peasant agriculture satisfy goals of agricultural sustainability (Trutmann and Thurston, 1993). Traditional agricultural practices are less fossil-fuel intensive and chemical intensive than 'modern' agricultural practices. Most traditional farming systems utilize crops with a broad genetic base. Many include the return of considerable amounts of organic material to the land, ensuring high levels of microbial diversity in soils. And many are highly productive and resilient to the effects of local pests and pathogens, over the long term. Study of traditional farming systems presents a great challenge in itself. Western scientists often minimize of dismiss farmer practices, unless they persist and look carefully at what the farmers do. Western scientists must surmount cultural and/or linguistic boundaries that isolate them from traditional farmers, if they are to understand traditional farming systems. One example, from one of the few projects that has involved both anthropologists and a plant pathologist, illustrates this point. In a research project to understand constraints to bean production in Rwanda, anthropologists concluded from surveys that farmers regarded insect pests as the worst problems they faced, and that plant diseases were rarely considered a problem. Only after further studies did the team discern

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that the farmers did not identify particular diseases, but identified different periods and kinds of rain that led to plant putrefaction. From the Western science perspective, the rains predisposed crops to seed and seedling rots by various kinds of pathogens, and thus were a related rather than a central factor (P. Trutmann, pers. comm.) Furthermore, when resurveyed, farmers placed 'rain tolerance' (disease resistance) second in importance on a list of factors for which they selected varieties for their planting mixtures (Trutmann et al., 1993). At least two features are critical to good studies of traditional farming systems: (1) interdisciplinary collaboration among scientists and social scientists; and (2) collaboration with those most knowledgeable about these systems, the local farm families, understand and develop methods and technology (after Chambers, 1990). The initial emphasis should be on learning from the farmer about her or his crops, fields, practices and beliefs. Observational research must be emphasized, including: extended discussion with farmers about their own perceptions of their practices, the diseases present and how farmers deal with them; (Western) scientific assessment of disease, the suppressive potentials of the individual practices, and overall farming system; and finally, comparison of these with modern agriculture. It should go without saying that the visiting scientist must have respect for the culture and practices of the traditional farmers, and avoid judgmentalism. Assertions that particular practices are 'right' or 'wrong', 'good' or 'bad' too often have simplistic and culture-bound connotations.

1. Plant Disease Management in Traditional Farming Systems Thurston (1992), in 'Sustainable Practices for Plant Disease Management in Traditional Farming Systems', has made by far the most extensive study and compilation of traditional agricultural practices that are specifically relevant to plant disease management. The general lesson of this important book is that there is a wealth of diverse sustainable agricultural practices used in traditional farming systems throughout the world, and that workers in international agriculture need to understand these practices and the sociocultural context in which they are used. In the context of this chapter, the importance of his book lies in its usefulness as a starting point for research into traditional farming practices for sustainable disease management strategies. 2. Examples Although there are many distinct sets of practices that make up traditional agricultural systems, the plant disease management implications of very few have received any attention from agricultural scientists. Genetic heterogeneity of crops seems to be a linchpin of disease management in many systems. In a study of bean production in central Africa (Trutmann et al., 1993), farmers preferred mixtures to single varieties, and selected their varieties on the basis of yield and, apparently, disease resistance, although the farmers involved in the study were unable to express the methods they used to select varieties with physiological resistance to disease. One of their techniques, however, was to test germplasm

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themselves, either by planting it directly in with their own mixtures or in isolated portions of their fields. Direct evaluation of germplasm by the Western scientists demonstrated that many varieties were completely resistant to local strains of important pathogens. The proportion, in mixtures, of varieties resistant to anthracnose (Colletotrichum lindemuthianum) was higher in areas in which this disease was a severe problem, and lower in areas where it was less favorable to anthracnose development. Mixtures whose varieties had resistance to various pathogens offered protection for the entire crop in a field, preventing epidemics of any single disease, and guaranteeing the farmer at least some harvest. Varietal mixtures reduced disease severity and spread more than the mean of the disease resistance of the individual varieties in the mixtures (Wolfe, 1985; Trutmann and Graf, 1993). Farmers in this study also culled blemished seed (damaged or infested by pathogens) from their mixtures before planting, thus reducing the inoculum of various pathogens (Trutmann etal., 1993). Another feature of many traditional systems, with implications for disease management, is the addition of 'copious quantities of organic amendments' (Thurston, 1992). This practice undoubtedly builds a high degree of microbial diversity in soils, which has been shown by research in biological control to enhance the suppression of soilborne pathogens. However, reports on the microbiology of traditional agricultural systems are almost non-existent. Slash/mulch agricultural practices have evolved in many locations around the world. The central characteristic of this kind of farming system is the cutting of the vegetative growth of perennial plants and leaving the cuttings in place as mulch, into which a crop is planted. Slash/mulch practices are used in many different climatic zones. Some utilize native plants without cultivating them; others plant trees or herbaceous legumes for the purpose of providing mulch. The use of slashed mulches is a multipurpose practice which serves to insulate soils from temperature extremes, retain soil moisture, return nutrients to the roots of crop plants, suppress weed growth, and reduce or prevent erosion. Numerous slash/ mulch systems are used in drier settings around the world, also. For example fast-growing leguminous trees such as Erythrina and Leucaena are used as shade for perennials such as coffee, mulch, green manures, forage and live fences. Fixed nitrogen and rapid cycling of nutrients are obtained by mulching with the periodically pruned branches and leaves, in between tree rows (Ramfrez et al., 1993). Although there is little or no information available as to the effects of these practices on plant disease (H. D. Thurston, pers. comm.), one such system in Mexico has been documented by Garcia-Espinosa and colleagues (Garcia-Espinosa, 1980; Garcia-Espinosa etal., 1994). In Tabasco, large swampy areas are inundated for up to 7 months of the year. The dominant vegetation is popdl grass (Thalia geniculata) or other marsh grasses, which are cut down at the beginning of the dry season. Short-season maize varieties or other crops are planted in the high-organic-content soils. As the seedlings emerge, a superficial burn of the mulch is carried out, scorching but not killing the germinating maize nor damaging the regrowth of the grasses. The popdl system produces high yields of maize

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(higher than neighboring mechanized maize cropping), and requires minimal input besides labor. Experiments to investigate soilborne plant disease demonstrated that popdl soils suppressed the severity of several pathogens (GarciaEspinosa, 1980; Lumsden et al., 1981). Plastic mulches have become widely used in vegetable and fruit cropping in North America (an excellent example of an environmentally non-sustainable practice, considering the many square kilometres of plastic sheeting that are discarded every year). Organic mulches as used in traditional farming systems are used by some farmers. Researchers at the US Department of Agriculture have been experimenting with a slash/mulch system using vetch species (Abdul-Baki and Teasdale, 1993). Seeded in the fall, the vetch was cut down in spring and left in place, and~'omato seedlings were planted directly into the slashed legume. Fruit yields were higher than with plastic mulch, and far higher than for non-mulched tomatoes. Damage from potato beetle was minimal and there were indications of reduced disease incidence. The use of organic mulches resembles the use of crop residues in biological control (Cook and Baker, 1983). Crop residues can have positive or negative effects on pathogens (e.g. Rickerl etal., 1992). Some foliar pathogens can overwinter successfully in crop residues, providing next season's inoculum, but different pathogens may be affected by different cultural practices during distinct phases of crop growth or times of the year, or pathogens of some crop species may be inhibited by mulches consisting of the residues of other plant species. As for other traditional practices, there is abundant anecdotal evidence of the impact of slash/mulch systems on plant diseases. However, almost no specific attention has been given to disease-reduction in slash/mulch or other traditional practices, or to ways of improving the disease management in such systems or integrating the use of such practices to modern agriculture.

3. Research in Disease Management of the Role of Traditional Practices Study of disease management implications of traditional farming systems may lead to the emergence of several kinds of knowledge relevant to sustainable agriculture. One has to do with improvements in developing-country agriculture, one with integration of sustainable practices into modern agricultural systems, and the other with a possible overriding lesson for modern agriculture. What conclusions can be drawn from research on disease management in traditional agricultural systems so far? 1. Many improvements in traditional farming systems are undoubtedly possible and desirable, but practices and technologies developed for disease management in industrialized countries cannot be transferred wholesale to developing countries. The dominant model of Western agriculture emphasizes monocultures, heavy and repeated applications of fossil-fuel derived inorganic fertilizers to satisfy nutrient demands of high-yielding monocultures, pesticides to combat a wide array of weeds, insects, and pathogens; substitution of

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mechanization for human or animal labor at every opportunity; cultivar uniformity; and, finally, nearly exclusive reliance by growers on corporations for these inputs. These features are in direct contrast to traditional farming systems which have evolved in the absence of all these inputs. Traditional farming in developing countries typically involves peasant agriculture on small farms. Peasant agricultural practices result from a long-term process of adjusting to the environment (Teri and Mohammad, 1988). They are holistic, pragmatic, culturally embedded, site-specific and based on ethnobotanical knowledge. It is clear that direct transfer of technology from industrialized nations usually fails in traditional agricultural settings. Wholesale importation of Western technology and practices disrupts longstanding integrated crop production systems, destabilizes communities economically and lacks the environmental sensitivity to maintain ecological sustainability. In addition to all the specific detailed questions that Western studies may have investigated in traditional production systems, they should return to a few very basic questions. What factors and practices, from both farmers' and scientists' perspectives, keep the crops healthy? Are particular practices in traditional systems responsible for suppression of particular diseases? Or does only an integrated ensemble of practices provide sustainable disease protection? The answers could lead to insights about how to improve traditional systems, or to transfer certain lessons or practices to modern agriculture. 2. Traditional farming systems provide a potentially rich source for finding new approaches for disease management in industrialized countries. They represent applied ecological science in cultural contexts different from those that give rise to science as we describe it. How to understand this knowledge, and how to integrate it into modem agricultural science, is not obvious. It is no doubt as foolish to expect traditional practices to transfer wholesale to industrialized countries as vice versa. Knowledge in traditional farming systems takes the form of local specific knowledge of a particular place: its particular softs, weather, crops, animals and neighboring plants. But the ecological lessons from such systems should inform agricultural science in the industrialized countries. This requires one to learn to understand the traditional practices within the frame of reference of the farmers themselves, to expect that farmers' practices are based on internally consistent world views, and to persist in learning the descriptive language and customs, and then recast these in terms of Western scientific practice. 3. Neither of the previous two conclusions admits yet another possibility, namely that traditiomd farming systems may provide the nucleus for an agricultural paradigm that offers an alternative to modern agricultural systems. For instance, one of the central characteristics of traditional agricultural systems that seems to be the main component of disease management potential is the diversity in the genetic base, soil microbial communities, management options, and heterogeneity of the cropping systems and surrounding ecosystems. This

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is in marked contrast to modern agricultural trends towards homogenenizing and simplifying the genetic base of crops, losing diversity in microbial populations, and depending on a few uniform external inputs. The lessons known by and learned from peasant farmers need to be reconciled with the practices of industrial agriculture. The benefits of understanding traditional farming are not restricted to traditional systems themselves, but ' . . . may reveal important ecological clues for the development of alternative production and management systems. Industrial countries have much more to learn and probably will benefit more from the study of traditional agriculture than will developing countries . . . ' (Altieri, 1987).

B. Role of Biotechnology (Molecular Biology) in Developing Alternatives to Chemical Disease Management The second group of disease management practices discussed are those derived from agricultural biotechnology, and these are explored in relation to their economic and environmental sustainability. They present striking contrasts to the traditional systems in that they involve newly acquired techniques, are undertaken primarily in industrialized nations, and rely most heavily on Western practices of laboratory science. Just as important insights into non-chemical methods of disease management await us through the study of traditional farming systems, significant contributions may also be derived from molecular biological research. As with most other fields of agricultural research in the industrialized nations, plant pathology has undergone rapid expansion in molecular biology research during the past decade and a half. Agricultural biotechnology could be defined as including almost any use of selective breeding, biochemical experimentation to modify plant or animal varieties, and tissue culture methods to produce somatic mutants or disease-free plant material. A more specific definition is used here, namely, the use of recombinant DNA or molecular biological technologies to modify and study plants, animals or microbes. Whereas traditional farming systems represent applied ecology, agricultural biotechnology is applied molecular biology. To a great extent, agricultural biotechnology has so far been an extension of conventional genetic or breeding research. There are at least two important differences between the two kinds of research. First, whereas conventional breeding work is carried out at least with exposure to agroecosystems, agricultural biotechnology begins with experimentation and design that is completely removed in time and place from agroecosystems, and placed in isolation in laboratories. Second, in agricultural biotechnology, genetic combinations between non-related organisms can be made and are a primary focus of this kind of work. Among the first priorities for agricultural biotechnology research has been

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the generation of crop varieties with improved agronomic or nutritional characteristics, herbicide tolerance, and pest- or disease-resistance. Transgenic crop varieties are anticipated to serve a variety of specific purposes, from simplifying the management, protection, or storage of crops, modifying the nutrient composition of crops, and increasing the efficiency of microbial adjuncts to crop varieties. Although the major emphasis in agricultural biotechnology is on the generation of new plant and microbial varieties, this has not been its exclusive focus. Several classes of molecular biological techniques - particularly DNA hybridization and sequence amplification methods such as Southern hybridization and polymerase chain reaction (PCR) - provide the capability to detect genes and microbial organisms with great precision and sensitivity, and are increasingly important in plant disease diagnostic applications and the study of microbial ecology. Agricultural biotechnology is still in its infancy. The use of recombinant technology to develop a commercially useful disease-resistant cuhivar has not yet proven a shortcut to conventional breeding approaches. Isolating appropriate genes and establishing stable transgenically derived resistance that is durable in the field requires lengthy experimentation. No plants constructed for resistance in such a way have yet been commercialized. A number of biological hurdles confront researchers in understanding the mechanism of expression of transgenic resistance. However, as more resistance genes are isolated and methodologies for locating them are improved, recombinant approaches will probably accelerate the development of new varieties. For any particular type of genetic modification, the initial few examples will require the longest research time, and subsequent varieties will be quicker to develop. In addition, for ecological, social and political reasons, such organisms require much more scrutiny for environmental safety than conventionally derived organisms do. Finally, the environmental sustainability of genetically engineered organisms is uncertain. So far, the primary motivation for agricultural biotechnology has been the development of products for use in modern agricultural contexts. Molecular biological methodologies have given scientists the power to alter organisms' genomes rapidly by making changes in their genetic structures that probably would never have occurred in nature, and to select organisms that express specific traits. Many countries' legal systems allow these organisms to be patented. The perceived control that recombinant methodologies gives scientists over the genetics of organisms, and the results for product ownership and potential profit, make for an obvious linkage between corporations (or governments) and agricultural biotechnology. Many hundreds of millions of dollars have already been spent on such research in the industrial nations. Thus, the emphasis in agricultural biotechnology has been economic, which predisposes it more to considerations of economic sustainability. Environmental sustainability of particular genetically modified organisms, and the fit between them and ecosystems in which they might be placed, is not an ongoing concern of research in agricultural biotechnology. If considered, it is separate from and

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pursued much later than the economic usefulness of a genetically engineered organism. The genetic manipulation of plants and animals for agriculture is as old as agriculture itself, and biotechnological modification represents part of a continuum of technological approaches to that end. However, since its inception, genetic engineering has been a social issue as well as an environmental one. The question of what amounts to 'appropriate deployment' has become a critical question regarding the use of genetically engineered organisms (Altieri, 1987). Debates on the use of genetically engineering and genetically engineered organisms in the environment often spill over into political arenas (witness the ongoing debates in Europe and the United States over bovine somatotropin and licensing of and public acceptance of, tomatoes modified for extended shelf life). The importance of the social aspect of the deployment of genetically engineered organisms is regrettably trivialized by those who maintain that public resistance occurs only because the public is scientifically illiterate. The only aspects of these concerns that are routinely required by government policies are 'scientific risk assessment' aspects of environmental and human health safety issues pertaining to genetic engineering (Lesser and Maloney, 1993, Maloney, 1995). It must be noted, however, that scientific risk assessment addresses only one small component of environmental sustainability. It only asks whether a genetically engineered organism will do no environmental harm, over a short term. It does not ask the far more important question for environmental and economic sustainability, namely, 'Will it fit into an agroecosystem or into an economic system, over the long term'. Possibly more important for environmentally sustainable plant disease management in the future will be the impact of molecular biological tools on pathogen identification and microbial ecology. Hybridizational and PCR techniques already available are increasingly important for detection and diagnosis of particular pathogens or for monitoring their population levels before they attain critical disease thresholds. More important in the long run, these techniques are useful in investigating organismal ecology. In some cases they permit the re-examination of problems previously intractable for want of appropriate tools. Mutational labeling of microbial strains facilitates selection and tracking of microbial isolates. PCR technology, especially, provides a qualitative improvement in detecting microbial populations that are dispersed, uncommon, or unculturable. Pathogen taxonomic and epidemiological studies now routinely include DNA sequence or restriction fragment-length polymorphism (RFLP) analysis. These and other basic methods have been introduced into the majority of plant pathology research operations in industrialized countries, and are being used increasingly in developing countries and international agricultural centers. Such research does not necessarily lead to the development of disease-resistant plant varieties. Application of various recombinant DNA techniques may greatly broaden our understanding of plant disease interactions and microbial-plant ecology and provide a basis for new biological control strategies (Nelson and Maloney, 1992, 1994).

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1. Examples Transfer to plants of pathogen genes whose presence or expression confers pathogen resistance to a crop ('pathogen-derived resistance'; Sanford and Johnston, 1985) represents one recombinant approach to non-chemical disease management. Numerous transgenic lines resistant to different virus strains have now been established, with varying levels and breadths of protection to different viral strains (Fitchen and Beachy, 1993). The mechanisms of resistance are not yet well understood in most cases. Single-gene resistance to bacterial or fungal pathogens has been demonstrated to be accessible and transferable through cloning based on molecular mapping (Martin et al., 1993b). A tomato gene that confers resistance to races of Pseudomonas syringae has been isolated from a resistant cultivar and transferred to susceptible cultivars (Martin et al., 1993a). The molecular engineering of endophytic and epiphytic microbes has not yet been applied to plant disease management, but is a commercially appealing strategy for disease protection. The basic approach is to transfer traits to plant symbionts or other plant-associated microbes to confer some kind of protection to the plant through production of a pathogen-suppressive chemical (toxin) or nutrients that change the epiphytic microbial community (Andrews, 1992). Technical feasibility of this approach has already been demonstrated for insect pest management: Clavibacter strains were engineered to express 6-endotoxin from Bacillus thuringiensis in maize (Fahey et al., 1991). In other experiments, the potential for entirely artificial plant-microbe symbioses has been explored, using transgenic plants that synthesize opines (normally conferred on a plant only by Agrobacterium tumefaciens parasitism), and transgenic P. fluorescens strains that have been engineered to utilize the same opines (Farrand et al., 1994). Modification of Pseudomonas syringae strains for loss of ice nucleation properties is an example of genetic engineering of an epiphytic bacterium. Plant protection, in this case from cold temperatures rather than disease, was achieved by displacing a resident microbial strain with the non ice-nucleating strain (Lindow, 1987). By themselves, the developments listed here are significant breakthroughs in technology and disease management, and provide insight into the genetic and cellular basis of plant disease processes. Used appropriately, modified plants and microbes could be integrated into agricultural production systems for significant improvements in the management of refractory diseases. 2. Conclusions Several features of agricultural biotechnology have been discussed in this section. What roles may there be for applied molecular biology in sustainable disease management practices? 1. So far, agricultural biotechnology research is predisposed toward improvements to modern agriculture in industrialized regions of the world. Agricultural biotechnology is research intensive, and emphasizes the innovation of

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individual varieties of plants or microbes. A number of planned and anticipated genetically engineered plants are predicted to reduce the need for chemical pesticides. These would therefore contribute to non-chemical plant disease management, and should be evaluated for their sustainability. Agricultural biotechnology emphasizes the development of marketable products for use in agriculture. Its focus is more on innovations for economic usefulness than for ecological appropriateness, thus it is oriented more toward a context of economic than environmental sustainability. Risk assessment of genetically engineered organisms (GEOs) addresses only whether GEOs will do obvious harm in the short run. It does not address whether a genetically engineered organism will fit within a context of either economic or environmental sustainability. Therefore it should not be regarded as a major criterion for agricultural sustainability. The operational basis of agricultural biotechnology is the development, in laboratories, of genetically engineered organisms that meet particular economic needs of corporations or farmers. This practice inherently disconnects agricultural ecosystems from their component organisms, by isolating the organisms from their environments during the entire process of their genetic modification. Field testing is essential to eventual use of the modified plants, but as currently practiced is aimed mainly at establishing the efficacy of the modified organism; only incidentally does it address the fit of such organisms within an ecosystem. Reconciling the tendency of biotechnology research to undermine holistic perspectives with an agroecological framework for sustainable agriculture is a critical challenge. The greatest relevance to sustainable plant disease management of agricultural biotechnology may lie in the tools it provides for understanding microbial ecology, plant-microbe interactions, and the importance of biological diversity in agroecosystems.

C. Biological Control Although they are by no means identical, next to 'organic agriculture', 'biological control' probably most typifies for the public the notion of non-chemical pest or disease management. Introduced as a specific term in the early twentieth century, the definition of biological control has undergone several modifications. Biological control of insects is better known than that for plant disease, through widespread use of integrated pest management based heavily on principles of insect population ecology and parasitology. Insect predators and parasitoids are widely used on some cropping systems, as is the bacterial lepidopteran pathogen Bacillus thuringiensis and, increasingly, baculoviruses. In their important book 'The Nature and Practice of Biological Control of Plant Pathogens' (1983), Cook and Baker suggested that biological control offers the chance of improving crop production ' . . . within existing resources, avoiding pathogen resistance to chemicals, and relatively pollution- and risk-free

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c o n t r o l . . . ' , making biological control environmentally attractive. One of their descriptions identifies it as a non-chemical means of disease management" ' . . . Biological control may be accomplished: through cultural practices (habitat management) that create an environment favorable to antagonists, host plant resistance, or both; through plant breeding to improve resistance to the pathogen or suitability of the host plant to the activities of antagonists; through the mass introduction of antagonists, nonpathogenic strains, or other beneficial organisms or agents' (Cook and Baker, 1983). They gave a formal definition of biological control in plant disease applications" 'The reduction of the amount of inoculum or disease-producing activity of a pathogen accomplished by or through one or more organisms other than man . . . ' (Cook and Baker, 1983). However, this definition gives the impression that biological control is a result mainly of direct interactions between individual antagonists and pathogens, and that human activity is somehow peripheral to biological control. This impression is tacitly contradicted by their book's detailed discussions, but should be explicitly addressed. First, it has been shown repeatedly, especially for soils and composts, that biological control depends on the activity of microbial communities. Second, although many individual antagonists with biological control potential have been isolated, upon subsequent field experimentation their activity is commonly not maintained or is insufficient to explain directly the extent of disease suppression that may be seen in the field. Third, many traits have been hypothesized to be significant in microbial interactions, but there are few cases in which any single trait has been shown to play a definitive role in disease suppression. Finally, human intervention is integral to the enhancement of biological control, whether through individual species or through agronomic practices. We are left with the knowledge that plant disease can be suppressed by microbial activity, and that in agroecosystems, human manipulation is needed to enhance the conditions for that microbial activity. The effectiveness of this manipulation is often predictable, though we cannot often identify or control the individual traits or species which effect this suppression. Therefore, ensembles of properties and organisms, and indirect effects of agronomic practices, microbial species and microbial communities on pathogens, should be accommodated in a definition of biological control; pragmatically, they may be more important for pathogen suppression than are direct interactions between individual organisms. Therefore, a revised definition is offered here to fully legitimate agronomic practices, the indirect effects of practices on disease management, and the necessary role of human intervention within biological control: Biological control involves the stimulation or enhancement of biological activity in ord~,rto reduce the amount of inoculum or disease-producing activity of pathogens.

1. Two Subdisciplines a. Agronomic Practices Biological control has come to have two distinct subdisciplines. The first is based on 'exploitation or manipulation of natural com-

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munities' for pathogen control (Cook, 1993). It consists mainly of agronomic practices utilized for their tendency to enhance plant health or to directly reduce the incidence of disease. Examples include crop or cultivar rotation, various tilling strategies, addition of organic amendments such as compost, mulch or manures, sanitation practices, flooding before planting, soil aeration or solarization, and so forth. Overlap between agronomic practices for biological control and traditional practices that affect disease management provides a major link between biological controland traditional practices. 'Biological control' provides a Western scientific lens with which to interpret many of the traditional farming practices that should be evaluated for plant disease management potential. A number of cases of direct relationships are known between particular practices and the decline or occurrence of particular pathogens (Palti, 1981; Cook and Baker, 1983). Reports of research that could be relevant to biological control of plant disease is dispersed in the agricultural and ecological literature. Conversely, research that focuses on agronomic characteristics, such as yield, and their relationship to cropping practices (cultivar or crop rotation, for instance), tillage, fertility management, and so forth, commonly includes only anecdotal reports of disease pressure.

b. Microbial Antagonism The second subfield of biocontrol has come to be called microbial antagonism: the deliberate use of specific antagonist organisms for prevention or management of specific diseases. Research into microbial antagonism has expanded so much, relative to research into agronomic controls, that the term 'biological control' is often used nearly synonymously with microbial antagonism (cf. Andrews, 1992). Microbial antagonists have been sought and studied for several reasons, including the relative ease of working with individual microbial isolates compared to systems or communities. Microbes, especially bacteria and viruses, and to a somewhat lesser extent, fungi, lend themselves to genetic manipulation and the study of cause-effect relationships of their behavior. The advent of recombinant DNA technology has provided new methods for manipulating and studying the behavior of microbial antagonists (Nelson and Maloney, 1992; Cook, 1993; Kluepfel, 1993). As noted before, microbial antagonism has been attractive because of its anticipated similarity to pesticide-style control for a variety of diseases. The isolation and development of a microbial antagonist follows a somewhat routine path (Maloy, 1993). Typically, microbial field isolates are screened for their effectiveness in reducing the severity of a particular disease or their ability to interfere with pathogen growth or reproduction. This step can derive from field observations, but is most commonly performed in vitro. Isolates' physiological characteristics may be studied. Strains are then assessed for performance in the field. Further strain selection, genetic manipulation, and formulation may be carried out to improve their effectiveness against particular pathogens, efficacy in the field, simplify their dispersal, and increase their shelf life. There are numerous examples of this procedure in temperate agriculture (e.g. Handelsman etal.,

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1990), and a few from tropical agriculture (e.g. Mew and Rosales, 1986). Cook (1993) recently outlined the process, from screening of field isolates to commercial use, of biocontrol agents for the suppression of take-all (Gaeumannomycesgraminis var. triticz)on wheat. Recombinant DNA methodologies are now used extensively in microbial antagonism research. There has been a resurgence in research on antagonists during the past decade, partially stimulated by the availability of recombinant DNA methods to study their behavior, genetics and physiology (Nelson and Maloney, 1992; Sutton and Peng, 1993). Topics of such research range from tracking microbial distribution and fate in soils, understanding or enhancing antagonist suppressiveness, and the role of antibiosis in survival of bacteria in the rhizosphere, to research on the molecular basis of piant-microbe associations, directed at the possibility of creating artificial symbioses that would effect control of pathogens (Weller, 1988).

2. Biocontrol- Slow to Develop? Biological control, especially when limited to the definition as 'microbial antagonism', is often considered to have fallen far short of its promise. Direct field experimentation with promising individual strains has resulted in only a very few consistently effective and economical (or commercially viable) antagonist formulations (Adams, 1990; Cook, 1993). The central criticism of biological control acknowledged by Cook and Baker in 1983 ' . . . [T]here was nothing to sell the grower . . . ' is still true today (Andrews, 1992). Indeed, only eight products for biological control are currently registered for sale in the United States (Becker and Schwinn, 1993). This has led to considerable pessimism for the future of biological control as a significant contributor to plant disease management, if only saleable products are counted (el. Andrews, 1992). Development has been hampered by several factors, among them the success of the chemical paradigm - the creation of toxins and other inputs that enhanced productivity in the short term - and the failure of microbial antagonists to meet the same criteria as effective fungicides, such as rapid action, cost- or laborefficiency, ease of application, and broad effectiveness. Finally, there are many microbial isolates that have been demonstrated to have potential as antagonists for different pathogens. This has rarely been followed by intensive efforts on formulation of the antagonists to optimize their performance and to make their storage and packaging convenient (Cook, 1993). Research efforts and funding in biological control have not been as sustained or intensive as efforts in chemical control. Funding and research effort dedicated to an ecological approach to plant disease management has been small relative to that which has been devoted to plant physiochemistry and chemical pesticides. It is no surprise that biological control is in its infancy (Adams, 1990; Andrews, 1992). Authors are alternately optimistic and pessimistic about the prospects that biocontrol will ever provide much economic control of plant pathogens (Adams, 1990; Andrews, 1992; Sutton and Peng, 1993). However, they are in general

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agreement that sustained, prolonged research into the ecological mechanisms that underlie biocontrol is vital to the eventual availability of biological control strategies.

3. Ecological Basis of Biological Control Essentially, biological control is applied microbial ecology for plant disease management: it emphasizes the behavior and activity of microbes in suppressing plant diseases. It represents a very different approach to plant disease management than does chemical control. Broader usefulness of biological control will rely on greater understanding of the relationships among microbial populations, between microbial populations and soils, and between microbes and plants. A strong theoretical ecological basis for research in biological control exists. New techniques for the study of microbial ecology and physiology, including methods for assessing microbial activity and recombinant DNA-based manipulation and detection methods, are readily available along with the entire spectrum of more classical approaches. With appropriate support for such research, and incentives for interdisciplinary collaboration on biological control, this work should flourish. One of the most difficult but important research areas related to biological control is the composition and microevolution of rhizosphere and phylloplane microbial communities. This topic has widespread implications for biological control and agroecology, because it addresses the diversity and interactions within microbial communities, and thus the role of direct and indirect effects of both microbial antagonism and agronomic practices in pathogen suppression. Increasing breadth and detail in such research is possible by combining conventional microbiological techniques with the use of selectable markers, sophisticated statistical approaches, and computer simulations.

4. Evaluating for Agroecological Sustainability The effective application of ecological principles in the design of biological control strategies contributes in general to their environmental sustainability: strategies' fit in a particular agroecosystem is not a priori guaranteed, but resulting disease management strategies will already have taken many ecological relationships into account. Agronomic practices and microbial anatagonists can be considered from the standpoints of prevention of pathogen establishment or control of established pathogen populations (after Huber and Watson, 1970). Categories describing the practical applicability of biocontrol strategies can be a basis of criteria for economic and environmental sustainability of biological control practices. Microbial antagonists, for example, can be considered in terms of the temporal durability of the control they provide: self-sustaining control resulting from the single application of a biocontrol agent; partially self-sustaining, requiring occasional reapplication; and transient control requiring repeated application (the mode of use of typical fungicides) (Cook, 1993). Identification, study and development of agromic practices with biological control potential that meet criteria of agroecological sustainability should be promoted.

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5. Examples The use of organic amendments, ranging from crop residues to manure to dredged canal mud is a feature of many traditional and modern agricultural systems (Thurston, 1992; Cook and Baker, 1983). Specific effects of particular organic amendments on individual pathogens have not been well described. It may be that the use of diverse organic amendments serves to prevent establishment of pathogens as much as control existing pathogen populations. Research on, and use of, composted materials for pathogen suppression is increasingly important in biological control for container and field use (Hoitink and Fahy, 1986; Nelson and Craft, 1992). The relationship of suppressiveness of compost microbial communities to compost starting material and compost age is critical for reliable use of composts in disease management applications (Boehm et al., 1993). Many microbial antagonists - mycoparasitic, fungal and bacterial - display disease-suppressive qualities (Cook and Baker, 1983). More microbial antagonist research has been performed on soilborne pathogens than foliar ones (Andrews, 1992; Becker and Schwinn, 1993), in part because of the importance of soilborne diseases in many crops, and the prohibitive costs or health hazards of chemical control for many soilborne pathogens (Cook, 1993). Several reviews, which examine various aspects of microbial antagonism research, have been published in the past few years (Cook, 1993; Sutton and Peng, 1993; Adams, 1990; Baker, 1987), so examples will be presented only briefly here. The best known mechanism of biological control is mycoparasitism. Several mycoparasites, such as Sporidesmium sclerotivorum, Talaromycesflavus and Coniothyrium minitans, have been demonstrated to have great potential for the control of sclerotia-forming fungal parasites such as Sclerotinia and Sclerotium spp. Pythium nunn shows promise for use in control of pathogenic Pythium species. Trichoderma harzianum, although a poor competitor in non-sterile soils, is useful in many biocontrol applications if it is the initial colonizer of a substrate. S. sclerotivorum is the most thoroughly understood mycoparasite from an ecological perspective (Adams, 1990). A considerable body of research now exists on the production of antibiotics by several strains of Pseudomonasfluorescens, which provide significant suppression of several soilborne pathogens, including Pythium species and Gaeumannomyces graminis var. tritici (take-all of wheat) (Howie and Suslow, 1991; Mazzola and Cook, 1991; Mazzola etal., 1992; Keel etal., 1992). Progress has been made in understanding the role of antibiosis as a mechanism to enhance colonization and population growth; current emphasis includes the regulation of antibiosis biosynthesis in natural environments. Agrobacterium radiobacter strain K84, and its recombinant derivative K1026, are the premier examples of economical biological control with a bacterial antagonist (Ryder and Jones, 1990). This case illustrates how multiple dominant antagonist traits can be understood and combined with appropriate application methods to generate a disease-management strategy that is apparently ecologically sound (,Jones and Kerr, 1989). The effectiveness of A. radiobacter strains in controlling

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crown gall (A. tumefaciens) on fruit trees is commonly attributed to their production of agrocin and at least one other antibiotic. However, their effectiveness also depends on their ability to colonize tree roots efficiently. This is enhanced by dipping bare root stocks in antagonist suspensions, thus applying the antagonist directly to the pathogen's normal infection courts (Cook, 1993). Finally, strain K1026 was engineered to prevent transfer of agrocin resistance from A. radiobacter to A. tumefaciens, and, interestingly, is the only recombinant microbe licensed in any country for commercial use in agriculture. Mechanisms of antibiosis have received the bulk of attention in recent years. The roles of several other microbial traits are being studied as well, including siderophore production (Loper, 1988; Keel et al., 1989; Kraus and Loper, 1992), nutrient competition and pathogen stimulant inactivation (Maloney et al., 1994). Handelsman and colleagues found that a strain of Bacillus cereus (UW85) was effective in field trials against alfalfa damping off caused by Phytophthora megasperma f.sp. medicaginis (Handelsman et al., 1990). Using discriminant analysis, they found that application of UW85 resulted in significant alteration in the entire rhizosphere community, in terms of the distribution and abundance of other rhizosphere species. However biological control was effective, and microbial community alteration occurred without the persistence of high populations of UW85, which were found to be greatly reduced in the rhizosphere soon after application (Gilbert et al., 1993).

6. Conclusions 1. The redefinition of biological control given here, by emphasizing the stimulation of biological activity for the reduction of disease or pathogen activity, legitimizes direct and indirect effects of microbial behavior, and recognizes the central role of human actions in enhancing these effects. 2. Development of biological control methods should proceed with conscious attention to ecological principles. Greater understanding of community ecology of the rhizosphere should be possible with further application of increasingly well-developed and applicable ecological theory and molecular and statistical techniques. The linkage to microbial ecology, and the use of microbes resident in local agroecosystems, predispose biological control approaches to a high degree of environmental sustainability. 3. Under the definition given in this chapter, biological control as a scientific discipline works well as a bridge among different approaches for non-chemical disease management. It can accommodate a wide variety of agronomic practices. Furthermore, it can serve as a Western scientific lens to both learn from and interpret the disease management implications of traditional farming practices and acknowledge the indigenous knowledge underlying traditional farming systems. On the other hand, because it incorporates research and use of individual microbial varieties, and because it can use recombinant DNA methods in ecological studies, it also can draw on and overlap with perspectives from agricultural biotechnology.

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4. Greatly increased support for research is needed for the study of the relationship of agronomic practices to microbial community ecology and disease management, the basis of disease management through the use of individual antagonists, and the integration of agronomic practices that reinforce disease management in individual cropping systems. 5. Strengthening the economic sustainability of biological control approaches to plant disease management is critical. This can take the form of expansion of research on antagonist formulations for ease of use and efficacy, the relation and development of agronomic practices for plant disease management, and integrating, into modem agriculture, alternative criteria by which disease management strategies can be valued and which enhance the economic and cultural stability of farms and farming communities.

V. C O N C L U S I O N S

Although there are some critics of agriculture who value wilderness over all else, and believe that a hunter-gatherer lifestyle is the only way that human populations can achieve environmental sustainability, this chapter does not accept these views. It is the perspective of this chapter that agriculture is an activity basic to, and embedded in, human culture. Agroecology is taken as the best overall framework within which to develop disease management strategies for agriculture, and by which to assess sustainability in agriculture. It is a unique agricultural science because it is inclusive and sensitive toward human social and cultural systems, rather than treating agriculture as something separate from social systems. Agroecological research emphasizes agricultural sustainability through 'defining the principles upon which to base agroecosystem design, farmer evaluation and adoption of technologies, and validation of local practices that have emerged over centuries of agricultural activities' (Altieri and Hecht, 1990). In a broad sense, then, agroecology's strength is that it can accommodate both economic and ecological components of sustainability. Its customary focus is developing world agriculture, but it would be a wise approach to adopt for research in modern agricultural systems as well. 1. This chapter has presented three perspectives within which research on nonchemical disease management strategies exist and can be developed: traditional farming systems, biological control, and agricultural biotechnology. Valuable insight and methods for environmentally sustainable disease management strategies can be gained from all three. 2. A subtheme of this chapter has been to emphasize that no single research discipline can provide comprehensive disease management strategies. Forging an ecological framework for disease management will require a great expansion of interdisciplinary research in agriculture. Interdisciplinary collaborations are sorely needed to develop disease management strategies and

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to understand their ecological basis, so they can be applied effectively and for maximum economic and environmental sustainability. They should probably be the norm rather than the exception for research in both modern and traditional agricultural systems. This is one of the most difficult and exciting challenges in research today. To develop non-chemical disease management, it is critical that diverse research be supported. Commercial products are clearly important, but farmers and other agriculturists must have a wide range of practices and management options at their disposal. They must also have access to all the information and knowledge that might benefit them, to enhance their ability to adopt approaches that are economic and increasingly environmentally sustainable. A diverse base for research and outreach must be supported, in industrialized and agrarian nations, which emphasizes interdisciplinary collaboration, and farmer research, as well as university and corporate-based research. In addition to the research base in universities and corporations, extension and outreach networks of universities, government agencies and non-governmental development organizations will be more, not less, important to the long-term accomplishment of these on-going processes. Farmers should be encouraged to carry out their own research, as many farmers already do, and to communicate their knowledge to others, thereby adding to the 'indigenous' knowledge base. Biological control stands at the center of the spectrum of the three perspectives described in this chapter. Focusing biological control research through a lens of applied ecology predisposes biological control approaches to environmental sustainability. The philosophical roots and the ecological basis of biological control make it the best perspective in Western science from which to build ecological approaches to disease management for sustainable modern agriculture. If agriculture is to evolve towards both economic and environmental sustainability, many of the criteria by which it is evaluated will be changed or reordered. Incorporating long-term land and crop management perspectives into modern agriculture is crucial to the development of alternatives to the narrowly short-term economic criteria by which disease management methods are currently evaluated. Many, possibly most, biocontrol strategies may be more suitable for long-term rather than short-term land and crop management by farmers. Thus, biological control approaches, while not easily adapted to customary notions of fungicide control, for example, are pre-adapted to fit into long-term sustainable agricultural systems. The redefinition of biological control described in this chapter focuses on indirect effects on disease by antagonist and agronomic practices. In so doing, it further emphasizes biological control as a pragmatic and holistic approach to disease management, particularly for modern agricultural contexts. Environmental sustainability is an indispensable criterion for agricultural

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practices, but risk analysis is insufficient as an indicator of environmental sustainability. 8. Economic sustainability of agricultural practices is an indispensable criterion for agricultural practices, and must be examined critically in relationship to social structures. 9. Research on microbial biological control and on traditional agricultural systems needs a dramatic increase in funding support. Biotechnological research relevant to disease management already has a strong corporate base, and is not threatened. However, broad-based ecological analysis should be incorporated into biotechnological research and development projects long before the risk assessment or field-testing stage. 10. 'The challenge for sustainable agricultural research will be to learn how to share innovations and insights between industrial and developing countries and to end the one-way transfer of technology from the industrial world to the Third World' (Altieri, 1987). It is essential that researchers and practitioners respect the differences in agriculture as practiced in different parts of the world. Science is a culturally embedded practice, which operates under particular assumptions which may not be shared in different cultures. Agriculture is also a cultural practice, but with great differences in kinds of knowledge, integration with communities and ecosystems, and types of social and economic priorities in different cultures. Neither Western science nor modern agriculture should be regarded as the arbiters of validity of agricultural knowledge. Western definitions of science are not needed to legitimize the importance of traditional practices. However, traditional practices do not necessarily provide exact models by which to achieve transformations of modern agriculture to sustainability.

ACKNOWLEDGMENTS

I thank J. Confrey for invaluable comments and suggestions on the organization and content of this chapter, P. Trutmann, H. D. Thurston and C. StockweU for critical reading of the manuscript, and E.B. Nelson for the suggestion to pursue the topic.

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(1992). Contribution of phenzaine antibiotic biosynthesis to the ecological competence of fluorescent pseudomonads in soil habitats. Applied and Environmental Microbiology 58, 2616-2624. Mew, T. W. and Rosales, A. M. (1986). Bacterization of rice plants for control of sheath blight caused by Rhizoctonia solani. Phytopathology 76, 1260-1264. National Research Council (US), Board on Agriculture (1989). 'Alternative Agriculture'. National Academy Press, Washington. Nelson, E. B. and Craft, C. M. (1992). Suppression of dollar spot on creeping bentgrassa and annual bluegrass turf with compost-amended topdressings. Plant Disease 76~ 954-958. Nelson, E. B. and Maloney, A. P. (1992). Molecular approaches for understanding biological control mechanisms in bacteria: Studies of the interaction of Enterobacter cloacae with Pythium ultimum. CanadianJournal of Plant Pathology 14, 106-114. Nelson, E. B. and Maloney, A. P. (1994). Applications of recombinant DNA technology for the management of soil-borne diseases. In 'Management of Soil-borne Diseases' (V. K. Gupta and R.S. Utkhede, eds). M/S Narosa Publishers, New Delhi, in press. Palti, J. (1981). 'Cultural Practices and Infectious Crop Diseases'. Springer-Verlag, Berlin. Ramirez, C., S~nchez, G., Kass, D., Vfquez, E., Sgmchez,J., V~tsquez, N. and Ramfrez, G. (1993). Advances in Erythrina research at CATIE. In 'Fast-Growing Trees and Nitrogen-Fixing Trees. Proceedings of an International Conference' (D. Werner and P. Mueller, eds), pp. 96-105. Gustav Fischer Verlag, Stuttgart. Rickerl, D. H., Cuff, E. A., Touchton, J. T. and Gordon, W. B. (1992). Crop mulch effects on Rhizoctonia soil infestation and disease severity in conservation-tilled cotton. Soil Biology and Biochemistry 24, 553-557. Ryder, M. H. and Jones, D. A. (1990). Biological control of crown gall. In 'Biological Control of Soil-Borne Plant Pathogens' (D. Homby, ed.), pp. 45-63. CAB International, Wallingford. Sanford, J. C. and Johnston, S.A. (1985). The concept of parasite-derived resistancederiving resistance genes from the parasite's own gerome. Journal of Theoretical Biology 113, 395-405. Sutton, J. C. and Peng, G. (1993). Manipulation and vectoring of biocontrol organisms to manage foliage and fruit diseases in cropping systems. Annual Review of Phytopathology 31,473-493. Teri, J. M. and Mohamed, R. A. (1988). Prospects for integrated disease management in the small farm context in Southern Africa. NorAgric OccasionalPapers Series C. Development and Environment 3, pp. 97-105. Norwegian Center for International Agricultural Development, Agricultural University of Norway. Thomas, V. G. and Kevan, P. G. (1993). Basic principles of agroecology and sustainable agriculture. Journal of Agricultural and Environmental Ethics 6, 1-19. Thurston, H. D. (1992). 'Sustainable Practices for Plant Disease Management in Traditional Farming Systems'. Westview Press, Boulder, CO. Trutmann, P. and Graf, W. (1993). The impact of pathogens and arthropod pests on common bean production in Rwanda. International Journal of Pest Management 39, 328-333.' Trutmann, P. and Thurston, H. D. (1993). Disease management and the quest for sustainable systems. Proceedings of International Symposium on Agroclimatology and Sustainable Agriculture in Stressed Environments. Hyderabad, India. 1993. Trutmann, P., Voss, J. and Fairhead, J. (1993). Management of common bean diseases by farmers in the Central African Highlands. InternationalJournal of Pest Management 39, 334-342.

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WeUer, D. M. (1988). Biological control of soilborne pathogens in the rhizosphere with bacteria. Annual Review of Phytopathology 26, 379-407. Wolfe, M. (1985). The current status and prospects of multiline and variety mixtures. Annual Review of Phytopatholo~ 23, 251-273. Wright, A. (1990). 'The Death of Ram6n GonzS.lez: The Modem Agricultural Dilemma'. University of Texas Press, Austin.

7 CLASSICAL BIOLOGICAL CONTROL OF PLANT PATHOGENS John K. Scott CSIRO Division of Entomology, Private Bag PO, Wembley WA 6014, Australia

I. Introduction A. Theory of Classical Biological Control B. Examples of Classical Biological Control II. Biological Control and Plant Pathogens III. Classical Biological Control and Plant Pathogens IV. Classical Biological Control Using the Example of Phytophthora cinnamomi A. Taxonomy B. Region of Origin C. Survey for Mycoparasites D. Host Specificity E. Effectiveness of Exotic Biological Control Agents F. Suitability of Release Areas V. Conclusions Acknowledgements References

131 132 133 133 135 136 136 137 137 138 138 140 141 142 142

I. I N T R O D U C T I O N Biological control as broadly understood is the use of organisms for the control of pest species. Historically, one of the first methods used was classical biological control. This involves the importation of natural enemies of a pest from the native range to the country of introduction, and subsequent release of these agents (Wapshere etal., 1989). This type of biological control remains the principal means adopted against weeds and insect pests (Wapshere et al., 1989; Debach and Rosen, 1991; Julien, 1992). The term 'biological control' covers many methods including increasing or augmenting the density of local natural enemies, competitively displacing the pest species from the site of infestation, manipulating the environment or other organisms to favour natural enemies and conferring resistance on the host plant. Biological control of plant pathogens has mostly been concerned with using methods other than the classical approach favoured for weeds and insects (Cook, 1990). Research into controlling plant pathogens by biological means has been directed to manipulation of the environment to ADVANCES IN PLANT PATHOLOGY--VOL. 11 ISBN 0-12-033711-8

Copyright9 1995 AcademicPressLimited All rights of reproductionin anyform reserved

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encourage resident antagonists (--biological control agents) or the introduction of antagonists (Cook, 1990). In the latter case, the introduced antagonists already exist in the pest's environment. The purpose of this chapter is to bring a different perspective to the subject of biological control of plant pathogens. Using the example of a major pathogen, Phytophthora cinnamomi, I will approach the question of its control as if it were an introduced weed that was to be subjected to classical biological control. I will outline the theory of classical biological control, give examples of the wide range of types of organisms and habitats that have been involved in this method, and present a case for the classical biological control of

P. cinnamomi.

A. Theory of Classical Biological Control Biological control is a practical application of the science of population biology (Schroeder and Goeden, 1986). The dynamics of natural enemy populations are manipulated to reduce and stabilize those of the pest species. Classical biological control is based on three principles; the host specificity of natural enemies, the pre-adaptation of natural enemies to the new environments infested by the pest species, and the control of pest populations by natural enemies.

1. Host Specificity Some natural enemies have evolved host specificity where they will only feed on one host species or a group of closely related host species. Often there is evidence for co-evolution between the agent and the target in that related agents are found on related targets, suggesting an 'arms race' over a long co-evolutionary history. Demonstrating host specificity is an essential part of the risk assessment undertaken before introducing organisms into a new environment. Host specificity may give an agent selective advantage over polyphagous species. The hypotheses suggested to explain host specificity include reduced competition by having the ability to use a toxic host or enemy-free space (Jaenike, 1990). To maintain host specificity it is imperative that the agent has mechanisms for locating the host and often the life cycles of the target and host are closely intertwined. This close association is important in that it increases the likelihood of the agent being able to locate the host in the area of introduction and subsequently, to control the host' s density. The selection pressure to evolve traits enabling a response to a particular pest's density would be less for a polyphagous natural enemy that could seek out alternative hosts.

2. Pre-adaptation to the Region of Introduction Many physiological studies have shown that organisms have definable environmental limits for existence. There are also many other habitat constraints, for example soil type (Bruehl, 1987). It is possible to measure these constraints and to determine if a biological control agent is adapted to the proposed area of

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introduction. One of the commonest methods used in biological control is to select agents from areas that match closely the climate of the region infested by the pest. However, the suitability of the climate of the introduction area may not be immediately evident. In some cases an area of introduction without a climate matching the source region can prove to be more suited to a biological control agent than both the source region and areas that match it for climate (Scott, 1992).

3. Potentialfor Regulation of Pest Populations Classical biological control is not attempting to restore the 'natural balance' (Wapshere et al., 1989). This is impossible to achieve since the exotic pest has created a new situation in the region of introduction. At present it is not possible to predict the degree of reduction in a pest population caused by natural enemies introduced as biological control agents. In biological control of weeds all agents are host specific, just over two-thirds of agents that are released become established in their new environment, and about a third had an impact on the pest population (Julien etal., 1984; Waage and Greathead, 1988; Crawley, 1989). This impact becomes stabilized, hopefully at a point below the threshold importance of the pest. The effectiveness of a biological control agent in its region of origin does not necessarily transfer to the region of introduction. In the beststudied biological control system, that of the winter moth, Operothtera brumata, an insignificant parasitoid in the native range, the tachsinid fly Cyzenis albicans, proved to be an important control agent (Hassell, 1978). The reasons for this could not be predicted beforehand (soil conditions were important) and most biological control releases are based on an ad hoc assessment of the potential for population regulation. Despite the difficulties of prior identification of effective biological control agents, the practice of classical biological control has led to many successes.

B. Examples of Classical Biological Control A wide range of organisms has been subjected to classical biological control (Table II). The type of agents used ranges from insects to fungi and viruses. There appears to be no known limits to the habitats where classical biological control could operate. By definition, the region of origin of the pest is excluded.

II. BIOLOGICAL CONTROL AND PLANT PATHOGENS Baker and Cook (1982) defined the biological control of plant pathogens as 'the reduction of inoculum density or disease-producing activities of a pathogen or parasite in its active or dormant state, by one or more organisms, accomplished naturally or through manipulation of the environment, host or antagonist, or by mass introduction of one or more antagonists'. The biological control of plant

Table 1. Examples of classical biological control showing the diversity of taxa and habitat. Examples of target organisms

Examples of exotic control agents

Species Algae Pteridophyta Monocotyledonae Dicotyledonae

Species

Mollusca Myriapoda lnsecta

Various species Salvinia modesta Pistia stratiotes Opuntia stricta Hakea sericea Chondrila juncea Theba pisana Ommatoiulus moreleti Neodiprion sertifer

Pisces lnsecta lnsecta lnsecta lnsecta Fungus lnsecta lnsecta Virus

Arachnida Amphibia Mammalia

Oryctes rhinoceros Sirex noctilio Tetranychus urticae Bubus marinus Oryctolagus cuniculus

Baculovirus Nematoda Arachnida Various diseases Virus

Various fish species Cyrtobagous singularis Neohydronomus affinis Cactoblastis cactorum Carposina autologa Puccinia chondrillina Under investigation Under investigation European sawfly Polyhedrosis virus Rhabdionvirus oryctes Deladenus siridicola Ph ytoseiulus persimilis Under investigation Myxomatosis

Habitat

Reference

1992 1992 1992 1992 1992 1992

Aquatic habitats Water surface Water surface Range land Nature reserves Crops and pasture Crops and pasture Urban areas Canadian forests

Julien, Julien, Julien, Julien, Julien, Julien,

Pacific Islands Pine plantations Greenhouses Nature reserves Pasture and rangeland

Caltagirone, 1981 Taylor, 1981 Caltagirone, 1981

Bird, 1953

Fenner, 1983

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diseases has been reviewed extensively (Fravel, 1988; Nigam and Mukerji, 1988; Weller, 1988; Adams, 1990; Cook, 1990; Gabriel and Cook, 1990; Harman and Lumsden, 1990; Deacon, 1991; Sivan and Chet, 1992). Recently, three strategies have been identified: regulation of the pathogen population, exclusion of infection by use of beneficial micro-organisms and host plant resistance (Gabriel and Cook, 1990). Similar strategies exist against insects, although not usually called biological control, but not for weeds where host-plant resistance only applies against parasitic plants. Research on the biological control of soil borne pathogens has concentrated on crop rotations and stimulating resident antagonists (Cook, 1990). Adams (1990) remarks that mycoparasites have not been considered economical to use against plant pathogens because of the high dosages required. The use of introduced biological control organisms has been neglected because of the view that they would not establish or maintain populations any higher than that which occurred naturally (Cook, 1990). In the above context 'introduced' is equivalent to augmentative biological control as used against insects and weeds (Wapshere et al., 1989) where the introduced organisms already form part of the ecosystem and are not of exotic origin. In general, exotic agents have not been used in biological control against plant pathogens although there are some examples both as a result of deliberate or accidental introductions. III. CLASSICAL BIOLOGICAL CONTROL AND PLANT PATHOGENS The successful use of the mycoparasite Sporidesmium sclerotivorum against Sclerotinia and Sclerotium species (Adams and Ayers, 1982) is claimed to be an example of the classical biological control approach as used in entomology (Cook, 1990). This is not strictly true since the biological control agent was already known to be present in the region (Adams and Ayers, 1981) and was not a new introduction of an exotic species. There is, however, evidence from accidental introductions of mycoparasites of plant pathogens that classical biological control could be possible. The rust of poplars Melampsora larici-populina was accidentally introduced into Australia and caused premature defoliation in poplars. After 2-3 years the effect of the rust diminished. This was found to be due to a hyperparasite, Cladosporium tenuissimum, which presumably was also accidentally introduced (Sharma and Heather, 1978; Gibbs, 1986). The discovery of virus-mediated attenuation of fungal pathogenesis (Nuss, 1992) opens up a promising new area in biological control. This is best illustrated by the hypovirulence caused by double-stranded RNAs in the chestnut blight fungus Cryphonectria parasitica (Choi and Nuss, 1992) and Dutch elm disease, Ophiostoma ulmi (Rogers et al., 1987). The proposed introduction of viruses into the introduced Dutch elm disease population of New Zealand (C. M. Brasier, pers. comm.), if approved, will be the first example of classical biological control against a fungus.

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IV. CLASSICAL BIOLOGICAL CONTROL USING THE EXAMPLE OF PHYTOPHTHORA ClNNAMOMI The soilborne pathogenic fungus P. cinnamomi is probably the most destructive exotic organism present in the environment of south west Australia. It is the cause of the disease jarrah dieback, which has a major detrimental impact on the commercial use of jarrah forest (Eucalyptus marginata) and of pine plantations. The disease attacks plant species belonging to 40 different families. The fungus has spread to National Parks where it causes major changes to vegetation structure and is a threat to rare plant species (Malajczuk and Glenn, 1981; Dell and Malajczuk, 1989). It is also an important disease of container grown plants in nurseries (Hardy and Sivasithamparam, 1988) and is regarded as one of the most important plant pathogens of the world, especially for the avocado industry (Zentmyer, 1980). In south west Australia the disease was first reported in 1921 from the Darling Range near Perth. P. cinnamomi was first isolated from jarrah in 1964. Considerable research has been directed towards the control of P. cinnamomi with limited success (reviewed in Shearer and Tippett, 1989), although the spread of the disease has been lessened by a quarantine programme. Research in Western Australia and elsewhere is directed towards using phosphonic (phosphorous) acid as a fungicide (Pegg and De Boer, 1990), breeding resistance in the important timber species Eucalyptus marginata (Cahill et al., 1992) and examining the biotic causes of 'suppressive soils', soils where the fungus is present, but the disease absent (Malajczuk, 1983). Biological control by manipulation of the soil microflora has not been successful in south west Australia because of environmental conditions that cause a lack of suitable micro-organisms in soils that are nutrient poor and from which the litter is removed by regular fire management (Malajczuk, 1983). There has already been considerable research into using biological control agents against P. cinnamomi (Zentmyer, 1980; Malajczuk, 1983). However, this research has only taken place in areas where the pathogen is introduced. In classical biological control of insects and weeds it is usual to search for control agents in the region of origin of the pest species. It is assumed that at least some of the organisms attacking the pest species in its region of origin would have been associated with the pest sufficiently long to have evolved host specificity and effective mechanisms for locating the host. In the following sections, aspects usually used when assessing whether a weed could be a suitable target will be applied to P. cinnamomi with the objective of its control in south west Australia.

A. Taxonomy Correct taxonomic identifications are the foundation on which biological control studies are based. The target for biological control must be correctly identified to

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ensure that surveys for control agents in the region of origin are made of the same species (Rosen, 1986). The taxonomy of P. cinnamomi is well known (Zentmyer, 1980). Within P. cinnamomi the two mating types A1 and A2 are genetically isolated in Australia (Old etal., 1984). Isozyme work by Old et al. (1984) found low levels of variability within the A1 and A2 which suggests an extra-Australian origin for the fungus. The A2 form is widespread whereas the A1 is known from more restricted areas including Australia, Southeast Asia and the Cape Province of South Africa. Oudemans and Coffey (1991) report on a worldwide comparison of isozymes within P. cinnamomi, but their work does not indicate a source area for the fungus. Little variation was found within the A2 form which was distinct from the A1 form. The comparatively good understanding that exists for the taxonomy of P. cinnamomi ensures that surveys for biological control agents can examine the same fungus in both the regions where it is an introduced pest and in the regions of origin.

B. Region of Origin Zentmyer (1988) discusses the origin and distribution of the fungus. The Americas were excluded as were Western Australia and Victoria in southern Australia because of the historical incidence of large-scale vegetation changes due to the fungus. This leaves a large area of the world as the possible source, principally Southeast Asia and subSaharan Africa. The fungus was first described in 1922 as a new disease affecting cinnamon trees in Sumatra. This led to the assumption that the fungus is native to Southeast Asia. However, Von Broembsen and Kruger (1985) claim the fungus is indigenous to South Africa. Zentmyer (1988) concluded that the fungus has two possible origins, one in Southeast Asia, ranging from New Guinea through Indonesia, including Sumatra, Malaysia and Taiwan, the second in the southern Cape Province of South Africa.

C. Survey for Mycoparasites Many parasites of fungi are known (Darpoux, 1960; Bruehl, 1987; Sundheim and Tronsma, 1988) and 23 antagonists (mycoparasites, mycophages, antibiotic producers) are known to attack P. cinnamomi (Table II). A range of methods of attack, from antibiotics to oospore parasitism, are involved. There is only one report of organisms that feed on or destroy P. cinnamomi in its probable area of origin, Southeast Asia or south west South Africa. Maas and Kotze (1989) isolated bacteria (pseudomonads) and fungi (Penicillium spp., Trichoderma spp.) from different soils used to grow avocados in South Africa and found significantly more antagonistic organisms in pathogen-free soil. Methods are available for selecting amongst the antagonists that are undoubtedly present in the areas of origin (Merriman and Russell, 1990;

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Mulligan and Deacon, 1992). Surveys would also have to be made in Australia to establish whether or not the potential biological control agents are already present (and by implication proved to be ineffective).

D. Host Specificity A search of the literature indicates that none of the organisms listed in Table II is host specific to P. cinnamomi. This is to be expected since the source of the antagonists has always been in areas where the host is introduced, for example, Australia and USA. It is possible for a host-specific antagonist to migrate with the host fungus from a region of origin, but none has been detected so far. This would be exactly the pattern expected if a survey were made of the organisms attacking an introduced weed or insect, and it is only in the region of origin that host-specific organisms would be found. There have been few studies of host specificity among the mycoparasites, but the co-evolution of mycoviruses, bacteria, algae and fungi with fungi indicates that host specificity is widespread (Pirozynski and Hawksworth, 1988). Mycoparasites with limited host ranges are known (Pirozynski and Hawksworth, 1988). Some examples are Verticillium biguttatum which is used for the control of the soilborne pathogen, Rhizoctonia solani in potato (Van Den Boogert et al., 1990), and Olpidiopsis gracilis, which is a mycoparasite of a range of Phytophthora and Pythium species (Pemberton et al., 1990). The taxonomically isolated position of the Oomycetes with respect to other fungi (Brasier and Hansen, 1992) increases the likelihood of finding biological control agents that are host specific. Methods for determining host specificity of mycoparasites of P. cinnamorni would have to be developed, but could be based on the methods used in biological control of weeds. Testing starts with species closely related to the target, then tests are expanded to other related species before considering species of economic and environmental importance (Wapshere, 1974).

E. Effectiveness of Exotic Biological Control Agents Studies in South Africa give an indication that effective agents may exist. Phytophthora cinnamomi is a widely distributed pathogen in South Africa where it is a problem in nurseries, crops and plantations (Von Broembsen, 1984a,b). However, Von Broembsen and Kruger (1985) found that P. cinnamomi is widespread in native vegetation containing susceptible species in the south west Cape Province without the invasion and destruction that has accompanied the fungus in ecologically similar south west Australia. The non-invasive situation in south west Africa could be due to a number of explanations, soil type for example. Microbial activity is known to be an important cause of suppressive soils (Malajczuk, 1983) and this may be the case in the south west Cape Province.

Table 11. Organisms antagonistic t o P. cinnamomi. Mycorrhizal associations are excluded. Antagonistic organisms Bacteria and Actinomycetes Bacillus sp. Bacillus sp. Pseudomanas sp. Bacillus subtilis var. niger Streptomyces sp. Streptomyces sp. Streptomyces griseoloalbus Fungi Anguillospora pseudolongissima Catenaria anguillulae Epicoccum purpurascens Humicola fuscoatra Hyphochytrium catenoides Myrothecium roridum Oidiodendron maius Penicillium funiculosum Pythium nunn Trichoderma harzianum Trichoderma koningii Trichoderma viride Amoebas Arachnula impatiens Gephyramoeba sp. Unidentified leptomyxid

Reaction recorded

Specificity level

Antagonistic t o growth Antibiotic production Antagonistic t o growth Sporangium abortion Antagonistic t o growth Inhibited growth Antibiotic production Oospore parasite Oospore parasite Antibiotic production Oospore parasite Oospore parasite Antibiotic production Antagonism Antagonism Hyphal parasitism Hyphal lysis from antibiotic production Antibiotic production Hyphal lysis from antibiotic production Lysis of hyphae and chlamydospores Mycophagous Mycophagous

Oornycetes Non-specific Non-specific Oomy cetes Oomycetes Non-specific Nonspecific ? Non-specific Non-specific Non-specific

Where studied

Reference

Australia USA Australia Australia Australia Australia USA

Malajczuk et a/., 1977 Hutchins, 1980 Malajczuk etal., 1977 Broadbent and Baker, 1974 Malajczuk e t a/., 1977 Halsall, 1982 Rose etal., 1980

USA USA Europe USA USA USA Europe USA USA USA Australia Europe

Daft and Tsao, 1983 Daft and Tsao, 1984 Brown etal., 1987 Daft and Tsao, 1983 Daft and Tsao, 1983 Gees and Coffey, 1989 Schild etal., 1988 Fang and Tsao, 1989 Lifshitz et al., 1984 Kelley and Rodriguez-Kabana, 1976 Simon et a/., 1988 Reeves, 1975

Australia

Old and Oros, 1980

Australia Australia

Chakraborty etal., 1983 Chakraborty etal., 1983

J. K. Scott

140

Table III. Climate matches between sites in Western Australia and the rest of the world. MI is the match index calculated in the match climates option in CLIMEX. MI ranges from 0 to 1, the latter being an identical climate pattern of rainfall and temperature. The three highest matching sites with MI over 0.70 are shown. ,

Sites in High matching sites in Southwest Australia eastern Australia Dwellingup Eneabba

None None

Esperance

Victor Harbour

Jarrahwood

Robe None

Port Lincoln

MI

High matching sites elsewhere

Jonkershoek (South Africa) Iraklion (Greece) Larache (Morocco) 0.83 Cape Town (South Africa) 0.83 Elsenburg (South Africa) 0.80 Wingfield (South Africa) Groot Drakenstein (South Africa) Heldervue (South Africa) Jonkershoek (South Africa)

MI 0.74 0.74 0.74 0.88 0.84 0.79 0.80 0.79 0.77

F. Suitability of R e l e a s e A r e a s

As a first step, exotic biological control agents are searched for in those regions of origin of the pest that closely resemble the pest-infested area. On a broad scale, the P. cinnamomi infested areas of south west Australia are jarrah forest on ironstone gravels with a sandy matrix and heathlands on low nutrient sands. The climate is Mediterranean. The places that could be searched for exotic biological control agents include Southeast Asia and South Africa. 1. Climate Four widely separated sites with comprehensive climate records and representative of P. cinnamomi-infested areas in south west Australia were selected for the comparison of climates (Table III). Eneabba and Esperance represent the climate of heathlands while DweUingup and Jarrahwood represent the climates ofjarrah forest. The climate of these sites within the P. cinnamomi-infested areas of south west Australia was compared with the world set of climate stations given in C L I M E X (4.2 version) (Sutherst and Maywald, 1985). The four sites from south west Australia resemble those of south west Cape Province more than other areas of the world, including eastern Australia (Table III). No sites in Southeast Asia are included among the sites with a high degree of climate match. 2. Vegetation and Soils Heathlands on low nutrient soils are found in south west Australia and south west Africa (Specht, 1979; Groves, 1983), but not in Southeast Asia apart from very small areas of lowland infertile sands and subalpine habitats (Specht and Womersley, 1979). Floristically, the heathlands of Australia are regarded as more similar to South Africa than other regions (Specht, 1979). Many plant families are shared between the two regions and only a few have penetrated into Indo-

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Malaya or elsewhere (Specht, 1979; Specht and Womersley, 1979). The jarrah forests do not have an analogous vegetation type in similar climates outside Australia (Dell and Havel, 1989). Fire plays an important role in the environment of both south west Australia and south west Africa (Gill and Groves, 1981). There appears to be little documentation of the role of fire in heathlands of Southeast Asia. Some of the soil types present in south west Australia are found in Southeast Asia and in south west Africa (FAO-Unesco, 1977, 1978, 1979); however, detailed comparisons of soil types between these areas are not available. The environment of south west Australia corresponds closely to that of south west Africa. This suggests that the south west Cape Province would be the most suitable region to search for biological control agents that are preadapted to south west Australian conditions.

V. CONCLUSIONS Classical biological control, as shown by successful programmes against weeds and insects, offers considerable advantages over other control methods. It is reasonably permanent, has no harmful side effects, attack is limited to a very small group of related species, agents are self perpetuating, often density dependent and self disseminating. Costs are non-recurrent and risks are known and evaluated before introduction (Wapshere et al., 1989). With these advantages it is surprising that classical approach to the biological control of plant pathogens has not been considered more often. P. cinnamorni conforms to the profile of an organism that could be targeted by classical biological control. It is exotic to south west Australia. It is known to be attacked by many organisms. However, the source areas have not been searched. A search should be made of the south west Cape Province to determine whether mycoparasites associated with P. cinnamomi have potential to be used as biological control agents. Such a project is technologically feasible given that considerable work has already been done on the biological control of P. cinnamorni. If a search in South Africa proved unsuccessful then a search for biological control agents in Southeast Asia should not be excluded. There might be other reasons for the different behaviour ofP. cinnamorni in native vegetation in south west Cape Province. A study of this area could lead to a better understanding of the management of P. cinnamorni in Australia. A successful project would lead not only to the protection of natural resources in Australia, but potentially to the development of methods of control for a worldwide problem. There is strong evidence for the importance of hyperparasites of soil fungi (Bruehl, 1987). Other important plant diseases that are exotic species could be considered as targets for classical biological control. An example would be late blight of potato, Phytophthora infestans, which originates from Mexico and is now an exotic introduction in many parts of the world (Zentmyer, 1988; Fry et al., 1992).

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Classical biological control is unlikely to be the only solution to a pest problem and certainly will not eradicate the pest. Modern weed and insect control is an integration of biological, cultural and chemical control. This is also likely to be the case with plant pathogens (Sivan and Chet, 1992), especially for P. cinnamomi which occurs over a wide diversity of habitats.

ACKNOWLEDGEMENTS I thank Drs C. M. Brasier, G. E. St. J. Hardy, N. Malajczuk, K. M. Old, J. Ridsdill-Smith, and I. T o m m e r u p for debate over the different types of biological control.

REFERENCES Adams, P.B. (1990). The potential of mycoparasites for biological control of plant diseases. Annual Review of Phytopathology 28, 59-72. Adams, P. B. and Ayers, W. A. (1981). Sporidesmium sclerotivorum: distribution and function in natural biological control of sclerotial fungi. Phytopathology 71, 90-93. Adams, P. B. and Ayers, W. A. (1982). Biological control of Sclerotinia lettuce drop in the field by Sporidesmium sclerotivorum. Phytopathology 72, 485-488. Baker, K.F. and Cook, R.J. (1982). 'Biological Control of Plant Pathogens'. The American Phytopathological Society, St Paul, MN. Bird, F. T. (1953). The use of a virus disease in the biological control of the European sawfly, Neodiprion setifer (Geoffr.). Canadian Entomologist 85, 437-446. Brasier, C. M. and Hansen, E. M. (1992). Evolutionary biology of Phytophthora Part II. Phylogeny, speciation, and population structure. Annual Review of Phytopathology 30, 173-200. Broadbent, P. and Baker, K. F. (1974). Association of bacteria with sporangium formation and breakdown of sporangia in Phytophthora spp. Australian Journal of Agricultural Research 25, 139-145. Brown, A. E., Finlay, R. and Ward, J. S. (1987). Antifungal compounds produced by Epicoccum purpurascens against soil-borne plant pathogenic fungi. Soil Biology and Biochemistry 19, 657-664. Bruehl, G. W. (1987). 'Soilborne Plant Pathogens'. MacMillan, New York. Cahill, D. M., Bennett, I.J. and McComb, J. A. (1992). Resistance of micropropagated Eucalyptus marginata to Phytophthora cinnamomi. Plant Disease 76, 630-623. Caltagirone, L.E. (1981). Landmark examples in classical biological control. Annual Review of Entomology 26, 213-232. Chakraborty, S., Old, K. M. and Warcup, J. H. (1983). Amoebae from a take-all suppressive soil which feed on Gaeumannomycesgraminis tritici and other soil fungi. Soil Biology

and BiochemisOy 15, 17- 24. Choi, G. H. and Nuss, D. L. (1992). Hypovirulence of chestnut blight fungus conferred by an infectious viral eDNA. Science 257, 800-803. Cook, R. J. (1990). Twenty-five years of progress towards biological control. In 'Biological Control of Soil-borne Plant Pathogens' (D. Hornby, ed.), pp. 1-14. CAB International, Wallingford. Crawley, M.J. (1989). The successes and failures of weed biocontrol using insects. Biocontrol News and Information 10, 213-223.

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Daft, G . C . and Tsao, P . H . (1983). Susceptibility of Phytophthora cinnamomi and P. parasitica to fungi known to parasitize other oomycetes. Transactions of the British

Mycological Society 81, 71-76. Daft, G. C. and Tsao, P. H. (1984). Parasitism of Phytophthora cinnamomi and P. parasitica spores by Catenaria anguiUulae in a soil environment. Transactions of the British Mycological Society 82, 485-490. Darpoux, H. (1960). Biological interference with epidemics. In 'Plant Pathology an Advanced Treatise' Vol. III (J. G. Horsfall and A. E. Dimond, eds), pp. 521-565. Academic Press, New York. Deacon, J. W. (1991). Significance of ecology in the development of biocontrol agents against soil-borne plant pathogens. Biocontrol Science and Technology 1, 5-20. Debach, P. and Rosen, D. (1991). 'Biological Control by Natural Enemies', 2nd edn. Cambridge University Press, Cambridge. Dell, B. and Havel, J. J. (1989). The jarrah forest, an introduction. In 'The Jarrah Forest' (B. Dell, J . J . Havel and N. Malajczuk eds), pp. 1-10. Kluwer Academic, Dordrecht. Dell, B. and Malajczuk, N. (1989). Jarrah dieback- a disease caused by Phytophthora cinnamomi. In 'The Jarrah Forest' (B. Dell, J. J. Havel and N. Malajczuk, eds), pp. 67-87. Kluwer Academic, Dordrecht. Fang, J . G . and Tsao, P . H . (1989). Penicillium funiculosum as a biocontrol agent for Phytophthora root rot of azalea. Phytopathology 79, 1159. FAO-Unesco (1977). 'Soil map of the world 1:5 000 000. Volume VI Africa'. Unesco, Paris. FAO-Unesco (1978). 'Soil map of the world 1:5 000 000. Volume X Australasia'. Unesco, Paris. FAO-Unesco (1979). 'Soil map of the world 1:5 000 000. Volume XI Southeast Asia'. Unesco, Paris. Fenner, F. (1983). Biological control, as exemplified by smallpox eradication and myxomatosis. Proceedings of the Royal Society of London Series B 218, 259-285. Fravel, D. R. (1988). Role of antibiosis in the biocontrol of plant diseases. Annual Review of Phytopathology 26, 75-91. Fry, W. E., Goodwin, S. B., Matuszak, J. M., Spielman, L.J., Milgroom, M. G. and Drenth, A. (1992). Population genetics and intercontinental migrations of Phytophthora infestans. Annual Review of Phytopathology 30, 107-129. Gabriel, C. J. and Cook, R. J. (1990). Biological control of plant pathogens. FA 0 Plant Protection Bulletin 38, 95-99. Gees, R. and Coffey, M. D. (1989). Evaluation of a strain ofMyrothecium roridum as a potential biocontrol agent against Phytophthora cinnamomi. Phytopathology 79, 1079-1084. Gibbs, A. (1986). Microbial invasions. In 'Ecology of Biological Invasions: an Australian Perspective' (R. H. Groves and J . J . Burdon, eds), pp. 115-119. Australian Academy of Science, Canberra. Gill, A . M . and Groves, R . H . (1981). Fire regimes in heathlands and their plant ecological effects. In 'Ecosystems of the World Vol. 9, Heathlands and Related Shrublands of the World. B. Analytical Studies' (R. L. Specht, ed.), pp. 61-84. Elsevier, Amsterdam. Groves, R. H. (1983). Nutrient cycling in Australian heath and South African fynbos. In 'Mediterranean-type Ecosystems the Role of Nutrients' (F. J. Kruger, D. T. Mitchell and J. U. M. Jarvis, eds), pp. 179-191. Springer-Verlag, Berlin. Halsall, D. M. (1982). A forest soil suppressive to Phytophthora cinnamomi and conducive to Phytophthora c~yptogea. II. Suppression of sporulation. Australian Journal of Botany 30, 27-37. Hardy, G. E. St. J. and Sivasithamparam, K. (1988). Phytophthora spp. associated with container-grown plants in nurseries in Western Australia. Plant Disease 72, 435-437.

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Harman, G. E. and Lumsden, R. D. (1990). Biological disease control. In 'The Rhizosphere' (J. M. Lynch ed.), pp. 259-280. John Wiley, Chichester. Hassell, M. P. (1978). 'The dynamics of arthropod predator-prey systems'. Princeton University Press, Princeton. Hutchins, A. S. (1980). In vitro inhibition of root-rot pathogens PheUinus weirii, Armillariella mellea, Fomes annosus and Phytophthora cinnamomi by a newly isolated Bacillus sp. Microbial Ecology 6, 253-259. Jaenike, J. (1990). Host specialization in phytophagous insects. Annual Review of Ecology and Systematics 21, 243-273. Julien, M. H. (1992). 'Biological Control of Weeds a World Catalogue of Agents and their Target Weeds'. CAB International, Wallingford. Julien, M. H., Herr, J. D. and Chan, R. R. (1984). Biological control of weeds: an evaluation. Protection Ecology 7, 3-25. Kelley, W. D. and Rodrigues-Kabana, R. (1976). Competition between Phytophthora cinnamomi and Trichoderma spp. in autoclaved soil. Canadian Journal of Microbiology 22, 1120-1127. Lifshitz, R., Dupler, M., Elad, Y. and Baker, R. (1984). Hyphal interactions between a mycoparasite, Pythium nunn, and several soil fungi. Canadian Journal of Microbiology 30, 1482-1487. Maas, E. M. C. and Kotze, J. M. (1989). Evaluating micro-organisms from avocado soils for antagonism to Phytophthora cinnamomi. Yearbook - South African Avocado GrowersAssociation 12, 56-57. [not seen - Abstract no. 7960 Review of Plant Pathology 71 (12)]. Malajczuk, N. (1983). Microbial antagonism to Phytophthora. In 'Phytophthora its Biology, Taxonomy, Ecoiogy, and Pathology' (D. C. Erwin, S. Bartnicki-Garcia, and P. H. Tsao, eds), pp. 197-218. American Phytopathological Society, St Paul, MN. Malajczuk, N. and Glenn, A. R. (1981). Phytophthora cinnamomi - a threat to the heathlands. In 'Ecosystems of the World Vol. 9, Heathlands and Related Shrublands of the World. B. Analytical Studies' (R. L. Specht, ed.), pp. 241-247. Elsevier, Amsterdam. Malajczuk, N., Nesbitt, H . J . and Glenn, A. R. (1977). A light and electron microscope study of the interaction of soil bacteria with Phytophthora cinnamomi Rands. CanadianJournal of Microbiology 23, 1518-1525. Merriman, P. and Russell, K. (1990). Screening strategies for biological control. In 'Biological Control of Soil-borne Plant Pathogens' (D. Hornby, ed.), pp. 1-14. CAB International, Wallingford. Mulligan, D. F. C. and Deacon, J. W. (1992). Detection of presumptive mycoparasites in soil placed on host-colonized agar plates. Mycological Research 96, 605-608. Nigam, N. and Mukerji, K. G. (1988). Biological control - concepts and practices. In 'Biological Control of Plant Diseases' Vol. 1 (K. G. Mukerji and K. L. Garg, eds), pp. 1-13. CRC Press, Boca Raton, FL. Nuss, D. L. (1992). Biological control of chestnut blight: an example of virus-mediated attenuation of fungal pathogenesis. Microbiological Reviews 56, 561-576. Old, K. M. and Oros,J. M. (1980). Mycophagous amoebae in Australian forest soils. Soil Biology and Bioctumist~y 12, 169-175. Old, K. M., Mora:l, G. F. and Bell, J. C. (1984). Isozyme variability among isolates of Phytophthora cinna:nomi from Australia and Papua New Guinea. CanadianJournal of Botany 62, 2016-2022. Oudemans, P. and Coffey, M. D. (1991). Isozyme comparison within and among worldwide sources of t}ree morphologically distinct species of Phytophthora. Mycological Research 95, 19-30. Pegg, K. G. and De Boer, R. F. (1990). Proceedings of the phosphonic (phosphorous) acid workshop. Australasian Plant Pathology 19, 112. Pemberton, C. M., Davey, R. A., Webster, J., Dick, M. W. and Clark, G. (1990). Infec-

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tion of Pythium and Phytophthora species by Olpidiopsis gracilis (Oomycetes). Mycological Research 94, 1081-1085. Pirozynski, K. A. and Hawksworth, D. L. (1988). Coevolution of fungi with plants and animals: introduction and overview. In 'Coevolution of Fungi with Plants and Animals' (K. A. Pirozynski and D. L. Hawksworth, eds), pp. 1-29. Academic Press, London. Reeves, R . J . (1975). Behaviour of Phytophthora cinnamomi Rands in different soils and water regimes. Soil Biology and Biochemistry 7, 19-24. Rogers, H. J., Buck, K. W. and Brasier, C. M. (1987). A mitochondrial target for doublestranded RNA in diseased isolates of the fungus that causes Dutch elm disease. Nature 329, 558-560. Rose, S. L., Li, C. Y. and Hutchins, A. S. (1980). A streptomycete antagonist to Phellinus weirii, Fomes annosus and Phytophthora cinnamomi. Canadian Journal of Microbiology 26, 583-587. Rosen, D. (1986). The role of taxonomy in effective biological control programs. Agriculture, Ecosystems and Environment 15, 121-129. Scott, J. K. (1992). Biology and climatic requirements of Perapion antiquum (Coleoptera: Apionidae) in southern Africa: implications for the biological control of Emex spp. in Australia. Bulletin of Entomological Research 82, 399-406. Schild, D. E., Kennedy, A. and Stuart, M. R. (1988). Isolation ofsymbiont and associated fungi from ectomycorrhizas of Sitka spruce. EuropeanJournal of Forest Pathology 18, 51-61. Schroeder, D. and Goeden, R. D. (1986). The search for arthropod natural enemies of introduced weeds for biological control - in theory and practice. BiocontrolNews and Information 7, 147-155. Sharma, J. K. and Heather, W. A. (1978). Parasitism of uredospores ofMelampsora laricipopulina Kleb. by Cladosporium sp. EuropeanJournal of Forest Pathology 8, 48-54. Shearer, B. L. and Tippett, J. T. (1989). Jarrah disback: The dynamics and management of Phytophthora cinnamomi in the jarrah (Eucalyptus marginata) forest of south-western Australia. Department of Conservation and Land Management Research Bulletin 3, 1-76. Simon, A., Dunlop, R . W . , Ghisalberti, E.L. and Sivasithamparam, K. (1988). Trichoderma koningii produces a pyrone compound with antibiotic properties. Soil Biology and Biochemistry 20, 263-264. Sivan, A. and Chet, I. (1992). Microbial control of plant diseases. In 'Environmental Microbiology' (R. Mitchell, ed.), pp. 335-354. Wiley-Liss, New York. Specht, R. L. (1979). Heathlands and related shrublands of the world. In 'Ecosystems of the World Vol. 9A, Heathlands and Related Shrublands Descriptive Studies' (R. L. Specht, ed.), pp. 1-18. Elsevier, Amsterdam. Specht, R. L. and Womersley, J. S. (1979). Heathlands and related shrublands of Malesia (with particular reference to Borneo and New Guinea). In 'Ecosystems of the World Vol. 9A, Heathlands and Related Shrublands Descriptive Studies' (R. L. Specht, ed.), pp. 321-338. Elsevier, Amsterdam. Sundheim, L. and Tronsma, A. (1988). Hyperparasites in biological control. In 'Biological Control of Plant Diseases' Vol. 1 (K. G. Mukerji and K. L. Garg, eds), pp. 53-69. CRC Press, Boca Raton, FL. Sutherst, R . W . and Maywald, G . F . (1985). A computerised system for matching climates in ecology. Agriculture Ecosystems and Environment 13, 281-299. Taylor, K. L. (1981). The sirex woodwasp: ecology and control of an introduced forest insect. In 'The Ecology of Pests Some Australian Case Histories' (R. L. Kitching and R. E. Jones, eds), pp. 231-248. CSIRO, Melbourne. Van Den Boogert, P. H . J . F . , Jager, G. and Velvis, H. (1990). Verticillium biguttatum, an important mycoparasite for the control of Rhizoctonia solani in potato. In 'Biological Control of Soil-borne Plant Pathogens' (D. Hornby, ed.), pp. 77-91. CAB International, Wallingford.

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8 ECONOMIC THRESHOLDS AND NEMATODE MANAGEMENT R. McSorley* and L . W . Duncan t * University of Florida, IFAS, Department of Entomology and Nematology, Gainesville, FL 32611, USA t University of Florida, IFAS, Citrus Research and Education Center, Lake Alfred, FL 33850 USA

I. Introduction II. Modeling Nematode-Host Interactions A. Nematode-Crop Damage Functions B. Models of Nematode Population Change C. Management Functions and Optimum Control D. Model Limitations E. Derivation and Use of the Economic Threshold III. Nematode Population Management A. Host-plant Resistance B. Crop Rotation C. Other Cultural Practices D. Biological Control E. Integrated Management IV. Perspectives References

147 148 149 150 150 152 154 155 155 157 158 159 161 161 162

I. I N T R O D U C T I O N Models to estimate economic threshold population levels of plant-parasitic nematodes are increasingly used to help manage these pests. Originally derived to aid in preplant decisions regarding nematode management, equations relating crop yield to nematode population density are now being used as components of more complex models to help investigate long-term behavior of cropping systems. As such, economic models are required for the development and implementation of integrated pest management (IPM) systems for nematode management (Barker and Noe, 1987; Dale etal., 1988; Kerry, 1990; Luc etal., 1990; Duncan, 1991; McSorley and Phillips, 1993). Indeed, as strategies to manage nematodes become more complex to reduce the reliance on pesticides (Alphey et al., 1988; Ferris and Greco, 1990; Sasser and Uzzell, 1991), the need to understand the relative economics of various permutations of cropping systems and control methods intensifies. ADVANCES IN PLANT PATHOLOGY--VOL. 11 ISBN 0-12-033711-8

Copyright9 1995 AcademicPressLimited All rightsof reproductionin anyform reserved

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Increased research has also reinforced awareness that valid estimates of economic thresholds are difficult to attain. Methods to assess more accurately levels of nematodes in soil and plant material are needed (Ferris et al., 1990; Schomaker and Been, 1992). Similarly, the accuracy of economic predictions based on the measurement of plant-parasitic nematodes depends heavily on factors that influence the host-parasite interaction (McSorley, 1992). Variation in the characteristics of a given soil environment (e.g. soil texture, cultural practices, presence or absence of competing organisms) and those extraneous factors that will occur at an unknown frequency or intensity (e.g. rainfall, temperature, crop prices), compromise the value of current efforts to forecast nematode-induced crop loss. The ability to reflect the influence of these factors on economic thresholds is key to the development of nematology IPM systems. Our intent in this chapter is to review methods that have been developed to estimate nematode population thresholds and apply the information for nematode control. Interest in alternatives to nematicides for nematode control is high. Quantitative models of the effects on nematode populations of crop rotation, biological control, resistance and tolerance, cultural practices and other control measures have been developed to help foster research progress and to aid in their application in the field. Accordingly, some methods to manage nematodes are reviewed as are methods to predict their effects on nematode populations.

II. MODELING N E M A T O D E - H O S T INTERACTIONS Research to characterize effects of nematodes on farm profits has emphasized the development of mathematical functions describing (1) nematode-crop damage; (2) nematode population change; and (3) control efficacy. In the context of this chapter, we refer to these equations as nematode management functions. Information derived from management functions and knowledge of production and control costs and expected crop values are used to estimate the economic effects of nematodes and various management options on farm profits during one or more growing seasons. Most of the equations used to model nematode-crop relationships are of simple form. Many are referred to as critical-point models, because they relate one event (yield, or end-of-season population density) to another (often preplant population density) at a single point in time (Duncan and McSorley, 1987). Such equations have proven useful in nematology because few management methods can be used after a crop is planted, migration does not appreciably affect nematode population change during a growing season, and, within limits discussed below, population dynamics of many species tend to be somewhat stable in response to normal patterns of climatic variation. When management decisions pertain to a single cropping season, or to a predetermined sequence of management options, the economic threshold - that population density at which the cost of nematode management equals the value

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of the increased crop yield expected from management - may be of prime concern. An extension of the concept of economic threshold is the optimizing threshold (Ferris, 1978) - that population density (following management) at which the difference in the predicted value of a crop and the management cost to attain that density are maximized. For the case of a single cropping season, determination of an optimizing threshold usually requires more precision in the required control-cost vs. efficacy models and in the ability to characterize nematode density than is currently possible. Therefore, the examples presented here involve economic thresholds rather than optimizing thresholds. Nevertheless, long-term profits and agricultural sustainability are affected by the cumulative impact of nematodes and nematode management programs. The concept of optimization is fundamental to the use of discrete models to select the most profitable long-term management strategies from a variety of management options (Ferris, 1978; Noe etal., 1991).

A. Nematode-Crop Damage Functions Equations used to describe the effects of nematodes on crop yield frequently reflect intraspecific competition among nematodes. The damage attributable to individual nematodes often decreases with increasing density. Thus, while yield may be inversely related to preplant nematode density (Pi) in a linear manner (Rodriguez-Kabana and King, 1985; Todd, 1989), often logarithmic transformations are required to linearize the relationships (Oostenbrink, 1966; Kimpinski and McRae, 1988; McSorley and Dickson, 1989; Sasser and Uzzell, 1991). Linear models have also been used to describe effects of more than one nematode species on yield by adding together population densities weighted for pathogenicity (Hijink, 1964), or by considering them in a multiple regression model (Noling, 1987). Quadratic models have been well-fit to the yield-nematode relationship (Barker et al., 1981) as have inverse logistic (Noe et al., 1991), exponential decay (Timmer and Davis, 1982), and inverse linear functions (Elston etal., 1991). Seinhorst (1965) proposed the crop-loss model Y=m

+ (1 - m ) z t ' - v

for

P > T,

and

Y - 1.0

for

P< T

where P is the nematode density, Y is the yield at a density of P nematodes/yield in the absence of nematodes, m is the minimum yield observed at high nematode density, T is the highest value of P below which yield is unaffected (Fig. 1) and z - the proportion of undamaged root at P - 1.0 (a constant slightly less than 1.0). Both the model and its descriptive parameters have been used widely to characterize basic plant-nematode relationships (Duncan and Ferris, 1983b; Inserra et al., 1983; Ferris and Greco, 1990; Trudgill, 1991). The model was also extended to include effects of multiple species infections (Duncan and Ferris, 1983a; Jones and Kempton, 1978).

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Fig. 1. Comparison of shape of hypothetical damage functions for a tolerant cultivar (A) and an intolerant cultivar (B). With use of the more tolerant cultivar, the tolerance limit increases from Tb to Ta and relative yield is greater through most of the range of initial nematode densities (Pi). B. Models of Nematode Population Change

Quantitative models of nematode population change are most often expressed as critical point equations relating end of season population density (Pf) to preplant density (Seinhorst, 1966; Jones and Kempton, 1978; Ferris, 1985), although some multiple function simulation models have been developed (Ferris, 1976; McSorley and Ferris, 1979; Jaffee a al., 1992). As with most damage functions, density-dependent effects are an important component of all population growth models (Fig. 2). Population decline in the absence of hosts or due to nematode antagonists, or chemical nematicides, has also been modeled using density-dependent (Ferris, 1985; Jaffee et al., 1992) and density-independent (Kinloch, 1982; Schmitt aal., 1987; Noe aal., 1991) functions. Cost-control functions used to derive optimization thresholds have also been estimated from damage functions and equations relating crop yield and nematicide dose (Schmitt a al., 1987). C. Management Functions and Optimum Control

True profit maximization requires a long-range approach to all aspects of farming systems. By determining appropriate and varied criteria, management functions

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10000

[]

1000

......... IX.

I

Do []

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1 0.1

, ,

, , ,

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Fig. 2. Relationship between Pf and Pi (log scale) for Meloidogyne incognita on corn, calculated from Seinhorst's (1966) model Pf - aEPi[(a - 1)Pi + E] -1, with E - equilibrium density - 505 and a - maximum multiplication rate - 475. Model is compared to actual Pf data (McSorley and Gallaher, 1993a), and the bold line indicates the maintenance line where Pr - Pi (reproduced by the permission of the Society of Nematologists). can be used to investigate effects of nematode management on agricultural sustainability. Specific criteria can include effects of management on crop profitability (Duncan, 1983; Noe, 1988), movement and fate of nematicides in soil (Swartz et al., 1989), and the effects of various management practices on nontarget organisms, soil conservation, and fertility. Particularly as management options diversify, some form of system modeling is required to understand and compare the dynamics of nematode control for different management sequences. The potential use of nematode management functions to investigate long-term behavior of management systems was proposed early in the development of these models (Jones and Kempton, 1978). Computer algorithms employing various combinations of management functions in temporal sequence have been used to investigate long-term effects of nematodes and nematode management on yields of annual and perennial crops (Jones and Kempton, 1978; Duncan, 1983; Ferris etal., 1986; Kinloch, 1986; Noling and Ferris, 1987; Ferris and Greco, 1990; Noe etal., 1991). The associated crop prices and control costs have been used to estimate the relative values of large numbers of potential management sequence permutations, which have included crop rotation, use of resistant varieties, and use of chemical and biological control. The effects of variable control costs and fluctuating crop values on the relative value of different management options have been described.

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To date, no data have been published to validate the specific output of any of these models in the form of field comparisons of particular cropping and management sequences. Nevertheless, promising sequences of multiple pest control options have been published (Ferris and Greco, 1990; Noe et al., 1991) and should stimulate such research.

D. Model Limitations 1. Methods

Data for deriving damage functions for nematode management have been obtained in pot studies, in microplots, and in small field plots. All such methods have important advantages and serious limitations. Studies in pots are useful to determine basic host-nematode relationships, such as pathogenicity and host resistance (Seinhorst, 1966; Trudgill, 1991), but plant growth and nematode distribution in soil are necessarily artificial. Similar problems can occur in microplot studies in which nematode inoculum is introduced as part of the experiment. Such experiments permit good control of experimental variables, but for this reason may not produce results similar to those from field plots with more natural conditions (McSorley and Phillips, 1993). Techniques have been developed to establish small field plots with a wide range of naturally occurring nematode densities. Methods include the use of preliminary surveys to identify such plots (Duncan and Ferris, 1983a, b; Noe, 1988; McSorley and Dickson, 1989) as well as prior manipulation of nematode populations using nematicides (Sasser et al., 1975; Ferris, 1985), combinations of crop species with variable host efficacy (Oostenbrink, 1966; Ferris, 1985), and, to minimize environmental variability, combinations of variably resistant cultivars of the same crop species (Francl and Kenworthy, 1989). Although nematode distribution in soil and the nematode-host interaction in field plots are natural, other problems are well noted. Population densities in field plots are unknown and must be estimated. Ferris (1984a) has proposed methods to reduce effects of sample error on model derivation. Perhaps the most serious problem encountered in small field plots is the lack of experimental control. Variation of edaphic (Schmitt et al., 1987), chemical (Trudgill, 1987), and biotic factors (Duncan and Ferris, 1983b) between plots influences nematode densities and behavior as ,*'ell as plant growth and yield. Researchers must attempt to identify important covariate factors (Duncan and Ferris, 1983b; Noe and Imbriani, 1986) with the knowledge that measured relationships may still be confounded by unmeasured variables. Measurements of average nematode density in the field do not provide information about the spatial patterns of nematodes. Because the relationship between nematode density and yield is not linear, there is a tendency to overestimate crop loss using damage functions derived from small plots (Seinhorst, 1973; Perry, 1983; Noe and Barker, 1985). Better understanding of potential relationships

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between the population mean and population aggregation parameters for various systems may help resolve this problem (Ferris, 1984a; Noe and Barker, 1985).

2. Variability in Nematode Management Functions Environmental conditions affect the shape of all management functions, so that the accuracy of generalizations depends on the degree to which these conditions vary between years and sites. Tylenchulus semipenetrans population change is affected by changes in the mass density and probably the carbohydrate level in citrus roots, which can vary annually as well as seasonally (Duncan and Eissenstat, 1993; Duncan etal., 1993). Seasonal variation in reproduction and damage functions has also been reported (Barker etal., 1985; McSorley and Dickson, 1989). Soil texture is the most notable edaphic characteristic affecting the shape of the damage function (Schmitt and Barker, 1981; Trudgill, 1986). Other causes of variation in management functions include temperature (Nardacci and Barker, 1979), fertility level (Noe and Imbriani, 1986), plant cultivar (Fig. 1; Inserra etal., 1983), other pests (Duncan and Ferris, 1983a, b), and different isolates of the same nematode (Inserra et al., 1983; Noe, 1991).

3. Characterizing Population Density Estimates of nematode population density are required in most research to derive damage functions and are the basis for subsequent management decisions. However, population estimates for nematodes can be highly variable due to aggregated spatial patterns of nematodes in fields (Noe and Campbell, 1985; McSorley, 1987; $chomaker and Been, 1992). Sample confidence interval halflengths equal to 50-100% of the mean are routinely attained in research and advisory work (Davis, 1984; McSorley and Dickson, 1991). Progress is possible only because ranges of nematode densities between plots or fields are often very large. Thus, the use of population density classes in combination with damage functions has proven useful for advisory purposes (Barker and Noe, 1987). Although methods have been proposed to address the problem of variability in determination of damage functions (Ferris, 1984a), improved techniques for sampling and enumerating nematodes are required (Barker and Imbriani, 1984; Noe and Campbell, 1985; Francl, 1986; Belair and Boivin, 1988; Ferris etal., 1990; Duncan, 1991). An important aspect of estimating nematode density is that sample size is usually very small, due to the cost of processing samples of soil and root material. Subsamples are often processed from well-mixed composite samples of soil and/or roots obtained from numerous sites within a field or experimental plot. Thus, the number of processed samples is usually far fewer than the actual number of sampled sites within an area. Problems of estimating variance and estimating proper sample size for the case of small sample numbers have been noted (Schmitt etal., 1990; Duncan etal., 1994). Progress in sampling will likely result from a combination of improved understanding of sampling requirements (Shomaker and Been, 1992), mechanization of equipment to collect the requisite material

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(Ferris et al., 1990), and improvements in processing efficiency (McSorley, 1987) including new methods to quantify nematodes in samples (Schots et al., 1992).

E. Derivation and Use of the Economic Threshold Derivation of an economic threshold population density for a single cropping season is straightforward when the damage function is linear, but becomes more involved for non-linear damage functions when incomplete nematode control is expected (Ferris, 1978; Schmitt etal., 1987; McSorley and Phillips, 1993). When sufficient information is available, it will be possible to include stochastic elements in economic threshold estimates and other model-derived predictions (Ferris, 1984b; McSorley and Phillips, 1993). Variability in management functions is due to factors that are intrinsic (e.g. soil texture, crop variety) or extrinsic (e.g. precipitation, temperature) to the system. To a certain extent, it is possible to identify important intrinsic factors, develop models that are appropriate for different cases and thereby reduce model variability (Schmitt and Barker, 1981). Similarly, it may be useful to develop predictive models for broad classes of extrinsic factors (e.g. wet and dry years) and to use historic data to estimate probabilities associated with those conditions (McSorley, 1992). As system conditions are defined with increased precision, methods to reflect sample and experimental error in point estimates (e.g. predicted yield based on estimated Pi) have been proposed (Ferris, 1984b). Probabilities based on extrinsic factors can also be imposed on these estimates. A similar approach would be to combine the use of management functions with plant growth models (Trudgill, 1992). Algorithms to simulate multiple cropping seasons can incorporate stochastic elements by iteratively assigning probabilities to extrinsic events based on historical data (Ferris and Wilson, 1987). Thus, estimation of forecast reliability requires identification of key extrinsic and intrinsic factors and model derivation for those conditions. Knowledge of these key factors is critical to optimize forecasting accuracy with respect to research costs for model development. Some key factors are likely to be discernible from current management strategies. For example, temperature during and shortly after planting is likely to contribute to variability of management functions for systems in which early or late planting can be used for nematode management. In some cases, desired models may be robust enough to include variation in several factors (McSorley and Gallaher, 1993a). However, strong interactions between key factors will add to research requirements to derive appropriate management functions. Nevertheless, this approach is an excellent way to test continually our understanding of the nematode-host interaction, and providing confidence estimates for predictions from incomplete models will only enhance their value.

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III. NEMATODE POPULATION MANAGEMENT As nematicide usage as a management tool becomes more limited due to environmental concerns, regulation, or loss of efficacy because of biodegradation (Felsott, 1989), it will be essential to develop and rely on effective alternatives for managing economic nematode pests. The status and prospects of alternative methods for managing nematode infestations are reviewed. Nevertheless, the importance of exclusion or quarantine as a first line of defense against nematode infestation should not be overlooked. Exclusion has limited the spread or infestation level of nematodes in many situations (Maas, 1987). For instance, it has been known for many years that the spread of Radopholus similis to new banana plantations can be limited by paring, heat treatment, or chemotherapy of planting material (Blake, 1969). Tylenchulus semipenetrans, Pratylenchuscoffeae and Radopholus citrophilus are excluded from many citrus orchards in Florida by a mandatory nursery certification program, and, in the case of the latter species, by the use of physical barriers (Duncan etal., 1990). Maas (1987) has recently reviewed quarantine and certification practices, including physical methods for disinfestation of soil (particularly in greenhouse and propagation situations) and planting material. Once sites are infested with economic levels of plant-parasitic nematodes, then other management methods must be sought, such as nematicides or the alternatives of host-plant resistance, crop rotation, other cultural practices, and biological control.

A. Host-plant Resistance The use of resistant or tolerant cultivars provides a relatively inexpensive yet highly effective means of managing certain nematodes on a number of crops (Roberts, 1982; Cook and Evans, 1987). Resistant cultivars have been particularly useful against Globoderaspp. on potato (Cook and Evans, 1987), Heterodera avenae and other nematodes on cereal crops (Cook, 1974), Heteroderaglycines and Meloidogyne spp. on soybean (Fassuliotis, 1982, 1987; Cook and Evans, 1987; Dropkin, 1988), and Meloidogyne spp. on tomato (Roberts, 1982; Fassuliotis, 1987), cotton (Fassuliotis, 1982), and tobacco (Slana and Stavely, 1981). In addition to these examples, resistant cultivars are available and used for many other nematode-host combinations (Sasser and Kirby, 1979; Fassuliotis, 1982, 1987; Roberts, 1982; Cook and Evans, 1987). Most nematologists use the terms resistance and susceptibility to refer to the degree of nematode reproduction and the terms tolerance and intolerance to refer to the effect of the nematode population on the plant (Cook, 1974; Roberts, 1982; Cook and Evans, 1987; Trudgill, 1991). Often, resistance and tolerance are found in the same host, but many exceptions occur. For example, the potato cultivar Maris Piper, which is susceptible to Globodera paUida, is more tolerant of the nematode than is the resistant clone 12380 ac2 (Trudgill, 1991).

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The plant damage function (Fig. 1) is an expression of tolerance since it is expressed in terms of plant response. The shape of the damage function will shift as cultivar usage is changed (Fig. 1). The damage function, while an expression of tolerance, is often the result of resistance. A given initial nematode density (Pi) may be less effective on a resistant host than on a susceptible host since a much lower percentage of the initial population available may actually infect the host plant. Several different mechanisms of resistance may operate against plant-parasitic nematodes. Nematode infection may be reduced by root exudates from plants such as asparagus, marigold, or neem (Rohde, 1972; Alam etal., 1975; Veech, 1981; Huang, 1985), or enhanced by exudates which stimulate egg hatch (Shepherd and Clarke, 1971; Veech, 1981). Nematodes which have already entered plant tissue may be affected by hypersensitive reactions (Huang, 1985; TrudgiU, 1991), host nutrition (Huang, 1985; Melakeberhan and Ferris, 1988; Powers and McSorley, 1993), or production of chemical products which interfere with nematode-host recognition. (Veech, 1981, 1982; Huang, 1985; Kaplan and Davis, 1987). More resistance methods are effective and, therefore, resistance more often available against sedentary endoparasites than against migratory endoparasites or ectoparasites (Roberts, 1982). Many plant species are non-hosts which support no reproduction and, therefore, are immune to certain nematode species (Nusbaum and Barker, 1971; Rohde, 1972; Roberts, 1982). However, even plants that are highly resistant (but not immune) may support some reproduction (Cook and Evans, 1987), and with many ectoparasites, resistance may be limited to differences in population densities among cuhivars (Cook, 1974). Description of these intermediate levels of resistance can be difficult and imprecise, particularly since nematode reproduction depends on Pi (Seinhorst, 1966, 1970; McSorley and Gallaher, 1992). Population models that relate final nematode density (Pf) to Pi (Seinhorst, 1966) are useful in expressing the host-parasite relationship over a range of Pi (Fig. 2). Their use provides a quantitative description of host status (Seinhorst, 1970; Nusbaum and Barker, 1971), which may change from good at low densities to poor at very high Pi for the same nematode-host combination (McSorley and Gallaher, 1993b). Because resistant cuhivars may permit some nematode reproduction, their continual usage can select for populations or pathotypes that can overcome host resistance. Widespread planting of the potato cultivar Maris Piper, which is resistant to Globodera rostochiensis, resulted in increased incidence of G. paUida (Cook and Evans, 1987). Overuse of resistant cultivars has caused similar problems with Heterodera glycines on soybean (Dropkin, 1988), M. incognita on tobacco (Cook and Evans, 1987), and H. avenae on some cereal crops (Cook and Evans, 1987). Rotation of cultivars has helped limit the ability of H. glycines to overcome resistance in soybean (Young, 1984), and growth of partially resistant potato cultivars with polygenic resistance has been useful against mixed pathotypes of Globodera spp. (Forrest and Phillips, 1984). Environmental factors, particularly temperature,

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may also limit efficacy of host resistance (Cook and Evans, 1987; Dropkin, 1988). For example, the M i gene conferring resistance in tomato to M. incognita is inactivated by temperatures greater than 32~ (Dropkin, 1969; Araujo et al., 1982). Much additional research will be needed not only to understand further the complex genetics of nematode resistance (Sidhu and Webster, 1981; Fassuliotis, 1987; Triantaphyllou, 1987; Trudgill, 1991), but also simply to identify the many crop cultivars which have never even been screened for their response to plantparasitic nematodes.

B. Crop Rotation Because soil-dwelling plant-parasitic nematodes are relatively immobile compared to foliar plant pathogens or insects, crop rotation has long been an important method for managing them (Good, 1968; Nusbaum and Ferris, 1973; Johnson, 1982; Trivedi and Barker, 1986). A non-host, cotton, can be rotated with peanut for managing M. arenaria (Rodriguez-Kabana etal., 1987a), maize can be rotated with soybean for management of H. g~cines (Ross, 1962; Schmitt, 1991) or M. incognita (Kinloch, 1983), rotations with legumes or other non-hosts are used against H. avenae on cereal crops (Brown, 1987), alfalfa rotations are useful against H. schachtii on sugarbeet (Weischer and Steudel, 1972), and many other examples of successful rotations are available (Good, 1968; Johnson, 1982; Trivedi and Barker, 1986). In locations warm enough for winter crop production, low value cover or forage crops may affect the nematode population in subsequent cash crops (Brodie etal., 1970). Damage from M. incognita to soybean was more severe after a winter cover crop of clover than after rye (McSorley and GaUaher, 1991). A winter crop of snap bean was more heavily damaged by Meloidogyne spp. after a summer cover crop of sesbania (Sesbania macrocarpa) than after hairy indigo (Indigofera hirsuta) or sorghum (Rhoades, 1976). Unusual non-host or antagonistic crops have been introduced into rotations in some locations to reduce nematode densities (Reddy et al., 1986; Rodriguez-Kabana et al., 1989). In some cases, favorable effects from crop rotation can persist for several seasons (McSorley and Gallaher, 1993b), but in other instances rotation effects may diminish after a single season (Rodriguez-Kabana and Touchton, 1984). The planning of crop (including weeds or fallow) sequences that minimize nematode population densities has been termed the cropping systems approach to nematode management (Trivedi and Barker, 1986; Noe, 1988). The design of a successful cropping system depends on economics (Ferris and Noling, 1987). In the southeastern United States, rotation of peanut with maize or sorghum for management of M. arenaria is unattractive because of the low economic value of these crops (Rodriguez-Kabana et al., 1989), but some 3-year sequences of peanut and soybean were profitable (Rodriguez-Kabana et al., 1988). Noe et al. (1991) developed models to determine the profitability of 3-year sequences of cotton and soybean based on density of Hoplolaimus columbus, damage functions, and economic data.

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With the long rotations used against some cyst nematodes, it may be necessary to project nematode populations and yields over many years to assess profitability of proposed crop sequences (Jones and Kempton, 1978). In perennial crops, it is essential to evaluate economics of management practices over the life of the crop, since short-term calculations may show a loss during the first few years when the crop is being established (Ferris and Noling, 1987). Designs of many cropping systems are complicated by the occurrence of several species of plant-parasitic nematodes in the same field (Christie, 1959). These situations can often be simplified by focusing on the key nematode pest (McSorley and Gallaher, 1991).

C. Other Cultural Practices The efficacy of solar heating beneath clear plastic mulch for nematode management was first recognized in the 1930s (Hagan, 1933). Within the past 15 years, the technique of soil solarization for nematode management has received increased attention and improvement. Optimum results are achieved during seasons of intense solar radiation and high temperature, when soil is moistened to improve heat conduction, when thin clear plastic tarps are used, and when tarps are maintained in place for 4-8 weeks (Katan, 1981; Heald, 1987). Best results have been obtained in locations with hot, relatively cloudless conditions during solarization including Israel (Katan, 1981), California (Stapleton and DeVay, 1983), and Texas (Heald and Robinson, 1987). Results obtained under subtropical conditions involving frequent rainfall and cloud cover have also been encouraging (McSorley and Parrado, 1986), although solarization was not as effective as soil fumigation under such conditions (Overman and Jones, 1986). Some cultural practices are relatively neutral toward plant-parasitic nematodes, and so their inclusion in sustainable systems may be based on other factors. Minimum tillage systems are adopted for their beneficial effects in conserving soil moisture, organic matter, and nutrients (Stinner and Crossley, 1982; Altieri, 1987; House and Brust, 1989), but the effect of tillage practices on plant-parasitic nematodes has often been minimal or inconsistent (Minton, 1986; McSorley and Gallaher, 1993b). Intercropping or mixed cropping may be beneficial in maintaining habitat diversity and reducing damage from some insect herbivores (Vandermeer, 1990). Occasional benefits in nematode management have been observed in crops interplanted with marigold (Khan etal., 1971; Davide, 1979) or sesame (Tanda and Atwal, 1988), but in general nematodes reproduce well on roots of interplanted host crops (Hackney and Dickerson, 1975; Powers et al., 1994). Other methods of nematode management are applicable in certain situations. Planting dates can be optimized to take advantage of reduced nematode development during cool seasons, as with M. incognita on winter wheat in California (Roberts etal., 1981), H. avenae on wheat in southern Australia (Brown, 1987), or H. schachtii and Ditylenchus dipsaci on sugarbeet (Weischer and Steudel, 1972).

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Adjustment of planting dates can also be used to increase nematode mortality from high soil temperatures (Schmitt, 1991). Flooding can be effective where it is practical (Trivedi and Barker, 1986), such as for managing M. graminicola in rice (Bridge and Page, 1982; Bridge etal., 1990). Fallow is highly effective in reducing nematode densities (Christie, 1959; Johnson, 1982; Rhoades, 1983; Duncan, 1986; Sarah, 1989) but the adverse effects on beneficial plant symbionts, soil fertility, and potential for erosion may not be compatible with sustainable systems. Trap crops were used for management of H. schachtii on sugarbeet in the 1800s but were ineffective against M. incognita on pineapple in Hawaii in the 1940s (Godfrey and Hagan, 1934). Manipulation of soil moisture through irrigation practices affects damage ofD. dipsaci to alfalfa (Griffin, 1992). Toppling of banana plants damaged by Radopholus similis can be reduced by propping or guying (Sarah, 1989). Control of weeds and proper management of groundcover is important in fruit groves (Nyczepir, 1991), and management of weed hosts (Rhoades, 1983) and volunteer plants (den Ouden, 1967) is essential for annual crops, too, as is destruction of old crop residues (Christie, 1959; Trivedi and Barker, 1986). Burning of crop residues can be effective against above-ground parasites such as D. angustus on rice (Bridge et al., 1990).

D. Biological Control Antagonists of nematodes are widely distributed among soil fungi (Stifling, 1984, 1991; Gray, 1988), bacteria (Sayre and Starr, 1988), arthropods (Walter etal., 1988), other nematodes (Small, 1987), and a variety of other invertebrate organisms (Small, 1988). Much of the effort to develop biological control of nematodes can be considered in three categories: (1) elucidation of natural control; (2) augmentation of antagonists; and (3) manipulation of the soil environment to enhance antagonistic activity. Elucidating natural control includes the detection and identification of antagonists of nematodes as well as attempts to document naturally occurring levels of nematode control. A growing body of evidence has been produced in the past 15 years showing that stable agricultural systems - perennial crops (Stifling et al., 1979; Stifling, 1984), monocultures (Kerry et al., 1982), or long-term rotations of crops which are all hosts to a nematode species (Minton and Sayre, 1989) - can foster density-dependent regulation of nematodes by antagonistic organisms. In most cases cited above, the equilibrium attained between antagonists and nematodes results in nematode densities below or near plant tolerance thresholds. Indeed, the lack of damage by nematodes under nominally conducive conditions has been used as a potential indicator of biological control (Stifling et al., 1979). Since a vast assay of potential nematode antagonists typically occur in most soils (Gray, 1987; Rodriguez-Kabana and Morgan-Jones, 1988), it is likely that natural control may often result from a combination of organisms rather than from a single antagonist.

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Exploitation of natural control will remain largely fortuitous until the conditions which sustain such systems are better understood (Stifling, 1991). Features common to most of the organisms shown to be capable of effective natural control are a high degree of specialization as parasites of nematodes and the existence of a survival stage for periods when nematode density is reduced. Although the longterm economics of natural control compared to other forms of nematode control may be favorable in some systems, a sustained period of crop loss due to nematodes can be anticipated before an equilibrium is established between the antagonist and nematode populations. Methods to minimize economic loss without reducing nematode populations (e.g. use of less-profitable but nematode-tolerant crops) during the establishment phase of such systems may be an interesting area for research. Effective biological control of nematodes has been achieved in pots and microplots augmented with a large variety of organisms antagonistic to nematodes (Stifling, 1991). However, with few exceptions (Cayrol etal., 1978; Cayrol, 1983), augmentation of biocontrol organisms has had very limited success at the commercial level. It is difficult to elucidate environmental requirements for survival (Kerry aal., 1980; McInnes and Jaffee, 1989), or the induction of nematophagy in facultative parasites (Gray, 1988), or factors involved in fungistasis (Jaffee and Zehr, 1985). It is even less feasible to create or to overcome such conditions, given the complexity and variety of soil environments (Kerry, 1990). Many of the most successful antagonists are fastidious and difficult to culture in large quantities (Stifling and Wachtel, 1980; Reise etal., 1988). Nevertheless, with accumulating experience, promising approaches to overcome some of these difficulties have become more apparent (Morgan-Jones and Rodriguez-Kabana, 1987; Gray, 1987; Kerry, 1990; Stifling, 1991) and considerable resources are currently devoted to research in this area. Attempts to manipulate the soil environment to enhance biological control have emphasized the use of organic amendments (Muller and Gooch, 1982) which can reduce populations of plant parasitic nematodes by a variety of mechanisms including release or production of toxic products (Prot and Kornprobst, 1983; Rodriguez-Kabana, 1986), increased community diversity with concomitant increase in antibiotics and allelochemicals (Spiegel a al., 1987), and possibly stimulation of predation and parasitism (Stirling, 1991). Current emphasis is on amendments containing substrates which are components of nematodes (such as chitin and collagen) and vulnerable to attack by enzymes released during substrate decomposition (Rodriguez-Kabana a al., 1987b; Galper et al., 1991). At least one soil-amendment for nematode control is commercially available (Spiegel et al., 1989). Integration of biological control in programs to manage nematodes can benefit from epidemiological studies that define the effects of epizootics on nematode population dynamics and the requirements for maintenance and activity of antagonist populations (Jaffee et al., 1992). Model development is constrained by difficulty in measuring and interpreting the population density and the propagule

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activity potential for many antagonists of nematodes (Kerry, 1990), although progress is being made (Stirling etal., 1979; Kerry etal., 1982; Mclnnis and Jaffee, 1989). Similarly, estimating the role of antagonists in nematode mortality can require complex methods (Kerry, 1980; Jaffee etal., 1988). As techniques are developed to measure important parameters of the interactions between nematodes and biological control agents, models to help predict optimum conditions to achieve economic control can be developed (Perry, 1978; Jaffee et al., 1992). The derivation of nematode management functions will be particularly important to validate systems involving biological control where anticipated nematode mortality may be low-to-moderate.

E. Integrated Management Some of the principles of integrated pest management (Andow and Rosset, 1990), which have been widely applied in the reactive chemical management of aboveground insect pests, are not particularly applicable in below-ground systems in which management decisions must often be made before the crop is planted. Nevertheless, integrated practices are increasing in importance in nematology, since they combine the advantages of several of the methods described above. Management of cyst nematodes on potatoes in the UK involves rotation, nematicides and use ofcultivars with various degrees of resistance (Jones and Kempton, 1978; Trudgill, 1986). Tylenchulus semipenetrans on citrus is managed by exclusion, resistant rootstocks, fumigation of planting sites, post-planting nematicide application, and maintenance of plant health (Duncan and Cohn, 1990). Management ofH. avenae on wheat in Australia includes use of crop rotation, optimum planting date, resistant or tolerant cultivars, favorable tillage practices and nematicide application, if sampling indicates populations are above the threshold (Brown, 1987). The management of R. similis on bananas can involve a combination of exclusion and plant inspection, treatment of planting sites by nematicides or fallow, preparation of nematode-free planting material, nematicide application after planting, and propping or guying of damaged plants (Sarah, 1989). When plants are seriously infected with plant-parasitic nematodes, integrating improved soil fertility (Good, 1968), use of mulches (Watson, 1945), and increased irrigation may be of some benefit in prolonging productivity. As the characteristics of sustainable agricultural systems become better understood, it will be necessary to recognize which nematode management practices are compatible for integration into specific systems.

IV. PERSPECTIVES Most scientists and producers recognize that maximizing profits and returns may not be the same as maximizing yields (Ferris, 1978; Ferris and Noling, 1987).

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Although cost and benefits are often calculated in terms of monetary values of inputs and yields, the long-term conservation of fertility, water, soils, and the agroecosystem itself must also be considered. Soil fumigation practices used extensively in the past (Lembright, 1990) were highly effective in increasing yields, but were very expensive and disruptive of entire soil ecosystems. Although much research was needed to perfect the application technology of soil fumigation (Lembright, 1990), relatively little knowledge of the biology of the soil system was needed to perform broad-spectrum soil fumigation. In contrast, many of the alternative methods described in this chapter (e. g. resistant cultivars, biological control, crop rotation) are highly specific, and their successful use requires considerable knowledge of the biology and ecology of specific nematodes on specific host cultivars. Not only is there a need for thresholds and damage functions for key nematode pests of many crops, but also for basic research knowledge to improve methods of nematode detection, sampling, recovery, and to identify more easily species, pathotypes, and populations (McSorley, 1987; Dropkin, 1988; Duncan, 1991). The collection of this information will depend on an increased number of agricultural scientists trained in nematology, plant pathology, agronomy, ecology, and related disciplines. The evidence presented in this chapter suggests that, although constant vigilance and attention are required, effective nematode management practices can be integrated into most sustainable systems. A major concern is that a level and system of production considered sustainable at one point in time cannot remain so for very long if demand is escalating from a rapidly growing h u m a n population (Paddock, 1992).

REFERENCES Alam, M. M., Masood, A. and Husain, S. I. (1975). Effect ofmargosa and marigold rootexudates on mortality and larval hatch of certain nematodes. IndianJournal of Experimental Biology 13, 412-414. Alphey, T . J . w . , Phillips, M. S. and Trudgill, D. L. (1988). Integrated control of potato cyst nematodes using small amounts of nematicide and potatoes with partial resistance. Annals of Applied Biology 113, 545-552. Ahieri, M. A. (1987). 'Agroecology'. Westview Press, Boulder, CO. Andow, D. A. and Rosset, P. M. (1990). Integrated pest management. In 'Agroecology' (C. R. CarroU, J. H. Vandermeer and P. M. Rosset, eds), pp. 413-439. McGraw-Hill, New York. Araujo, M. T., Bassett, M.J., Augustine, J. j. and Dickson, D. W. (1982). Effects of the temperature and duration of the initial incubation period on resistance to Meloidogyne incognita in tomato. Journal of Nematology 14, 411-413. Barker, K. R. and Imbriani, J. L. (1984). Nematode advisory programs - status and prospects. Plant Disease 68, 735-741. Barker, K. R. and Noe, J. P. (1987). Establishing and using threshold population levels. In 'Vistas on Nematology' (J. A. Veech and D. W. Dickson, eds), pp. 75-81. Society of Nematologists, Hyattsville, MD.

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Barker, K. R., Todd, F. A., Shane, W. W. and Nelson, L. A. (1981). Interrelationships of Meloidogyne species with flue-cured tobacco. Journal of Nematology 13, 67-78. Barker, K. R., Schmitt, D. P. and Imbriani, J. L. (1985). Nematode population dynamics with emphasis on determining damage potential to crops. In 'An Advanced Treatise on Meloidogyne, Vol. II, Methodology' (K. R. Barker, C. C. Carter and J. N. Sasser, eds), pp. 135-148. North Carolina State University Graphics, Raleigh. Belair, G. and Boivin, G. (1988). Spatial pattern and sequential sampling plan for Meloidogyne hapla in muck-grown carrots. Phytopathology 78, 604-607. Blake, C. D. (1969). Nematode parasites of banana and their control. In 'Nematodes of Tropical Crops' (J. E. Peachey, ed.), pp. 109-132. Commonwealth Agricultural Bureaux, Farnham Royal. Bridge, J. and Page, S . J . L . (1982). The rice root-knot nematode, Meloidogynegraminicola on deep water rice (Oryza sativa subsp, indica). Revue de Ngmatologie 5, 225-232. Bridge, J., Luc, M., and Plowright, R. A. (1990). Nematode parasites of rice. In 'Plant Parasitic Nematodes in Subtropical and Tropical Agriculture' (M. Luc, R. A. Sikora and J. Bridge, eds), pp. 69-108. CAB International, Wallingford. Brodie, B. B., Good, J. M. and Jaworski, C. A. (1970). Population dynamics of plant nematodes in cultivated soil: effect of summer cover crops in old agricultural land. Jour-

nal of Nematology 2, 147-151. Brown, R. H. (1987). Control strategies in low-value crops. In 'Principles and Practice of Nematode Control in Crops' (R. H. Brown and B.R. Kerry, eds), pp. 351-387. Academic Press Australia, Sydney. Cayrol, J . C . (1983). Lutte biologique contre les Meloidogyne au moyen d'Arthrobotrys irregularis. Revue de Nematologie 6, 265-273. Cayrol, J. C., Frankowski, J.P., Laniece, A., D'Hardemare, G. and Talon, J. P. (1978). Contre les nematodes en champigonniere. Mise au point d'une methode de lutte biologique a l'aide d'un Hyphornycete predateur: Arthrobotrys robusta souche 'antipolis' (Royal 300). Pepinieristes, Horticulteurs, Maraichers, Revue Horticole 184, 23-30. Christie, J. R. (1959). 'Plant Nematodes. Their Bionomics and Control', Agricultural Experiment Station, University of Florida, Gainesville. Cook, R. (1974). Nature and inheritance of nematode resistance in cereals. Journal of Nematology 6, 165-174. Cook, R. and Evans, K. (1987). Resistance and tolerance. In 'Principles and Practice of Nematode Control in Crops' (R. H. Brown and B.R. Kerry, eds), pp. 179-231. Academic Press Australia, Sydney. Dale, M. F. B., Phillips, M. S., Ayers, R. M., Hancock, M., Holliday, M., Mackay, G.R. and Tones, S.J. (1988). The assessment of the tolerance of partially resistant potato clones to damage by the potato cyst nematode Globoderapallida at different sites and in different years. Annals of Applied Biology 113, 79-88. Davide, R. G. (1979). Effect of nematicides and Tageteserectaon the control of Meloidogyne incognita and on yield of tomato. Philippine Agriculturist 60, 285-292. Davis, R . M . (1984). Distribution of Tylenchulus semipenetrans in a Texas grapefruit orchard. Journal of Nematology 16, 313-317. Dropkin, V. H. (1969). The necrotic reaction of tomatoes and other hosts to Meloidogyne: Reversal by temperature. Phytopathology 59, 1632-1637. Dropkin, V . H . (1988). The concept of race in phytonernatology. Annual Review of Phytopathology 26, 145-161. Duncan, L.W. (1983). Predicting effects of plant-parasitic nematode communities on crop growth. PhD. Thesis, University of California, Riverside. Duncan, L. W. (1986). Effects of bare fallow on plant-parasitic nematodes in the Sahelian zone of Senegal. Revue de Nematologie 9, 75-81. Duncan, L.W. (1991). Current options for nematode management. Annual Review of Phytopathology 29, 469-490.

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Trudgill, D. L. (1992). Mechanisms of damage and of tolerance in nematode infested plants. In 'Nematology from Molecule to Ecosystem' (F. J. Gommers and P. W. Th. Mass, eds), pp. 133-145. European Society of Nematologists, Invergourie, Dundee. Vandermeer, J. H. (1990). Intercropping. In 'Agroecology' (C. R. Carroll, J. H. Vandermeer and P. M. Rosset, eds), pp. 481-516. McGraw-Hill, New York. Veech, J . A . (1981). Plant resistance to nematodes. In 'Plant Parasitic Nematodes. Vol. III' (B. M. Zuckerman and R. A. Rohde, eds), pp. 377-403. Academic Press, New York. Veech, J. A. (1982). Phytoalexins and their role in the resistance of plants to nematodes. Journal of Nematology 14, 2-9. Walter, D. E., Hunt, H. W. and Elliot, E. T. (1988). Guilds or functional groups? An analysis of predatory arthropods from a shortgrass steppe soil. Pedobiologia 31,247-260. Watson, J. R. (1945). Mulches to control root-knot. Proceedings of the Florida Academy of Science 7, 151-153. Weischer, B. and Steudel, W. (1972). Nematode diseases of sugar-beet. In 'Economic Nematology' (J. M. Webster, ed.), pp. 49-65. Academic Press, New York. Young, L. D. (1984). Changes in the reproduction of Heterodera glycines on different lines of Glycine max. Journal of Nematology 16, 304-309.

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9 EVALUATION OF MICRO-ORGANISMS FOR BIOCONTROL: BO TRYTIS ClNEREA AND STRAWBERRY, A CASE STUDY

j.c.

Sutton

Department of Environmental Biology, University of Guelph, Guelph, Ontario, Canada, N1G 2W1

I. II. III. IV.

Introduction Socioeconomic Goals and Obligations in Biocontrol Research Objectives Background Perspectives A. Strawberry Cropping Systems B. Pathogen Ecology and Gray Mold Epidemiology C. Disease Management Strategies D. Conventional Disease Management E. Selection of Biocontrol Organisms - the Challenge V. Biocontrol Research A. Selection of Organisms B. Biocontrol Tests C. Vectoring of Biocontrol Organisms by Bees D. Biocontrol Mechanisms of Gliocladium roseum VI. Conclusions and Future Directions Acknowledgments References

173 174 175 175 175 176 177 177 177 178 178 178 183 186 186 187 187

I. I N T R O D U C T I O N Communities of indigenous organisms in cropping systems are vast and relatively unexploited reservoirs of antagonistic organisms that can suppress plant pathogens in developing crops, in crop residues and in the crop environment (Cook and Baker, 1983; Cook, 1993; Sutton and Peng, 1993). The antagonists usually are fungi, prokaryotes and microfauna, but larger arthropods and other organisms can also be important. Crop rotation, tillage methods, application of organic amendments and other cultural practices frequently capitalize on indigenous organisms to suppress pathogens. Indigenous organisms also can be isolated, evaluated for antagonism of pathogens, and introduced into crops as biocontrol agents. Experimental introduction of antagonists to suppress pathogens of ADVANCES IN PLANT PATHOLOGY--VOL. 11 ISBN 0-12-033711-8

Copyright9 1995 Acadanic PressLimited All rights of reproductionin anyform reserved

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foliage, flowers and fruits has had an erratic and sometimes disappointing history in which microbes that were promising under controlled conditions often performed poorly in the crop. However, several recent successes in biocontrol in crops have kindled a fresh enthusiasm and optimism among investigators such that introduced antagonists are now often seen as powerful tools to manage diseases that presently go uncontrolled and as good alternatives to chemical pesticides (Cook, 1993; Sutton and Peng, 1993). Prominent among recent successes in biocontrol are systems developed against Botrytis cinerea in strawberry, raspberry, grape, orchard fruits, spruce seedlings and other crops (Sutton and Peng, 1993). The present article focuses on microbial biocontrol of B. cinerea in strawberry, in which the pathogen causes gray mold fruit rot, a destructive disease of worldwide importance. Consideration is given to background perspectives, concepts, methods, strategies, pitfalls, progress and future directions in this biocontrol system.

II. SOCIOECONOMIC GOALS AND OBLIGATIONS IN BIOCONTROL The most important goal in biocontrol research is to develop methods and strategies that are effective in the cropping system. The literature is crammed with reports of biocontrol conducted solely under artificial conditions and of questionable relevance to crop conditions. Controlled studies can be meaningful and useful, however, when they complement or otherwise relate to research done in the crop. Demonstrations of effective biocontrol of pathogens in crops almost always invokes enthusiastic acclaim by growers and the public at large, and generally bodes well for continued support and advancement of biocontrol. For commercial application, biocontrol must be efficient, dependable, cost effective, and safe for humans, the crop and the environment (Scher and Castagno, 1986). Like other disease-management methods, biocontrol ideally aims to suppress disease sufficiently so that avoidable yield losses are minimized and crop quality is maintained at an acceptable level (Zadoks and Schein, 1979). Performance testing of biocontrol agents under representative cropping conditions, perhaps using a standard fungicide treatment as a yardstick, will be critical to assure efficiency and dependability of new biocontrol agents, and to convince growers that the new-fangled methods are worth adopting. In many instances, biocontrol may have to be integrated with other measures to achieve satisfactory disease management. Cost effectiveness of biocontrol is a function of production and marketing costs of the agents, methods and strategies of application, and treatment effectiveness. Investigators would do well to ponder these points when developing biocontrol. For example, there would be little point in extensively evaluating a biocontrol agent that would be overly expensive to produce and maintain, or to apply to a crop on a commercial scale. Biocontrol researchers usually are in the difficult situation of not knowing what regulations (if any) will be in place when the time comes to apply for registration

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of an organism as a biocontrol agent. Unfortunately, regulations developed to date are guided chiefly by principles pertaining to chemical pesticides instead of appropriate biological information. Cook (1992, 1993) proposed an imaginative framework to improve and expedite registration and oversight of biocontrol agents without compromising health and safety issues. Clearly it makes sense for investigators to screen out organisms that could represent a significant risk to humans, the environment, or the crop itself. Fortunately, health risks associated with organisms that do not grow above 35 ~ are chiefly allergies or toxicoses from microbial metabolites, and should normally be preventable through simple precautionary measures. Indigenous organisms, by their nature, should not threaten the environment when used judiciously. Preoccupied with selecting and evaluating antagonistic organism, many investigators resist the effort involved in applying for registration, developing formulations and scaled-up production, and organizing the marketing ofbiocontrol agents. Yet, as Cook (1993) pointed out, companies should not necessarily be expected to undertake ventures with biocontrol agents, most of which represent 'small potatoes' economically. Collective effort of researchers with growers' organizations, university alumni associations, or other groups, could ensure that biocontrol agents are put to use for the benefit of all.

III. RESEARCH OBJECTIVES The foregoing considerations were guiding principles in our attempts to develop biocontrol ofB. cinerea in strawberry. The primary objective was to develop a flexible biocontrol system that was at least as effective as conventional fungicides in suppressing B. cinerea and fruit rot under a broad range of microclimatic and cropping conditions in the field. The system would incorporate methods and strategies for applying biocontrol agents to optimize efficiency and minimize any ecological disturbance of microbial populations that might be counterproductive to strawberry health management. Attempts to integrate biocontrol with other disease management methods, and to register and commercialize the biocontrol agent(s) would await the outcome of the initial work. Earlier reports had indicated that microbial suppression of B. cinerea in strawberry appeared feasible (Bhatt and Vaughan, 1962, 1963; Tronsmo and Dennis, 1977).

IV. BACKGROUND PERSPECTIVES A. Strawberry Cropping Systems The cropping system is fundamental to an understanding of disease epidemics and to development of rational methods and strategies for disease management. Strawberry production systems were summarized recently by Galletta and

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Bringhurst (1990). A majority of strawberries in Ontario are June-bearing cuhivars that are grown as perennials in matted rows for up to 5-7 years, and a few are everbearers. Plantings are protected with straw mulch from December until April, when regrowth begins. June bearers flower and fruit from early May to July, and everbearers from late June until October. Renovation of June-bearer plantings is done after harvest and can include mowing of the foliage, tilling between the rows, plant thinning, and application of fertilizer and herbicide.

B. Pathogen Ecology and Gray Mold Epidemiology Studies on the biology, ecology and population dynamics of B. cinerea and on the epidemiology of gray mold in strawberry plantings provided important information for rational development of biocontrol. An insidious pathogen, B. cinerea in most instances symptomlessly infects the leaves, crowns, flowers and fruits of strawberry, and progressively colonizes the tissues only when they senesce, ripen, or die (Powelson, 1960; Jarvis, 1962a, b; Jarvis and Borecka, 1968; Bristow et al., 1986; Braun and Sutton, 1988; Simpson, 1989, 1991; Sutton, 1990). The leaves are infected chiefly when they expand, but the pathogen remains quiescent in the epidermis until the tissues senesce and die, when the fungus can progressively colonize the tissues (Braun and Sutton, 1988; Sutton, 1990). Mycelium in dead strawberry leaves is the chief source of inoculum (conidia) in gray mold epidemics in Ontario (Braun and Sutton, 1987; Sutton, 1990, 1991). Apothecia of the teleomorph, Bot~yotiniafuckeliana, were not found in systematic searches of Ontario strawberry fields (Sutton, 1990). Dispersed conidia can infect various parts of the flowers. Senescent sepals, petals, stamens, pistils and peduncles are important sources of mycelium of B. cinerea capable of invading contiguous receptacles and initiating fruit rot. While flower parts, especially stamens, are important pathways of fruit infection, direct infection of fruit by germ tubes may occur in some instances. Affected fruit develop a characteristic light brown rot, chiefly from the calyx end, as they ripen in the field or after harvest, and may become covered with grayish hyphae and conidiophores of the pathogen. Infection cycles of B. cinerea on the leaves occur year-round and in concert with leaf flushes. In June-bearers, leaves produced in flushes that peak in July (after renovation), September, and April-May, die in September-April, May, and June, respectively (Braun and Sutton 1986, 1988). Because B. cinerea does not produce lesions or accelerate senescence of the leaves, leaf life span is a critical factor that determines the duration of infection cycles and limits the rate of inoculum increase. Thus latent periods (infection to sporulation) are 7-8 months in leaves infected in Septe]nber, but only 6-8 weeks in leaves infected in April. Infection cycles may be abJx~ptly completed when the leaves are kiUed by frost, pesticides, or other agents.

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C. Disease Management Strategies From the ecological and epidemiological information, suppression of conidial production by B. cinerea in the dead leaves and protection of the flowers against infection by conidia are rational strategies for fruit rot control. The first oPthese might be achieved by protecting the green leaves against infection, by eradicating B. cinerea when it is quiescent in the epidermis, by suppressing colonization of dying leaves by the pathogen, or by destroying or inhibiting the fungus after it has colonized the tissues. In the second strategy, suppression of pre- and postinfection events on various flower organs can be visualized.

D. Conventional Disease Management Development of resistance to gray mold combined with other desired characteristics in strawberry has met with only moderate success, and the disease continues to be a serious threat in a majority of cultivars (Maas, 1978, 1984; Barritt, 1980; Simpson, 1991). In Ontario, careful site selection, weed control, irrigation scheduling, fertilization, foliage removal at renovation, and fruit handling and storage are recommended to suppress gray mold (Sutton etal., 1988; Sutton, 1990). The mainstay control, however, is fungicide sprays applied at intervals during flowering and fruiting, but this is threatened by pathogen resistance and public opposition. Chlorothalonil targeted at the pathogen in the foliage before flowering effectively controlled fruit rot without leaving residues in the fruit but has not been registered for this purpose in Canada (Sutton, 1990). Vulnerability of strawberry crops to gray mold in Ontario and elsewhere is unfortunately increasing with the decline in availability of effective fungicides. Can microbial biocontrol reverse this trend plus alleviate concerns with chemical residues?

E. Selection of Biocontrol Organisms - the Challenge Selection of antagonists to suppress effectively a pathogen in a cropping system is a formidable challenge given the staggering numbers of microbial isolates that could be evaluated. Which microbial species justify or do not justify evaluation? To what extent should intraspecific variation in biocontrol effectiveness be explored? Should genetically altered organisms be considered? How can the field of potential contestants be narrowed to manageable numbers without compromising the detection of exceptional antagonists? By what methods should candidate organisms be evaluated in order to provide a realistic estimate of their performance against a pathogen in a crop? Investigators of chemicals as potential fungicides or of host gene pools for disease resistance have long faced problems that parallel those in biocontrol and much could be learned from their experiences (Cook, 1992). In sharp contrast to the sparingly few microbes normally lined up in biocontrol tests, chemicals and genotypes are typically evaluated by the

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thousand. Logistical problems may not allow such numbers in biocontrol, but there may be rational means to narrow the field of organisms tested.

V. BIOCONTROL RESEARCH A. Selection of Organisms We subscribed to the views that ecological adaptation of the microbe to the crop plant would be advantageous, even prerequisite, for effective and sustained biocontrol in the cropping system, and that micro-organisms from strawberry would include the best-adapted forms. Strawberry plants in effect function as selective substrates and substrata in competitive colonization by indigenous organisms (Cooke and Rayner, 1984), and we can take advantage of this in narrowing the field of organisms for tests against B. cinerea. Ecological observations of the strawberry microflora was a further basis for selecting test organisms. As an initial step, the mycoflora of living, senescing, and dead leaves, flowers, and fruits of strawberries in plantings that were not treated with fungicides was quantified year round (McLean, 1988; McLean and Sutton, 1992). Washed and unwashed tissues were incubated in high humidity and on agar media in preparation for fungal identification or recovery. Total genera and species identified in leaves, calyces, petals, and fruits were 24, 15, 12, and 10, respectively, and thus notably low. Alternaria alternata, B. cinerea, Gloeosporium spp., Gnomonia comari, Penicillium spp., Trichothecium roseum and Verticillium spp. were frequent in all tissues studied. Golletotrichum dematium, Coniellafragariae, Epicoccum purpurascens and Gliodadium roseum were frequent only in the leaves, Cladosporium spp. were frequent in leaves, calyces and petals, but not in the fruits, and Rhizopus stolonifer was common only in the fruits. Other mycelial fungi and pink yeasts were infrequent, but white yeasts were abundant in all tissues examined. From their frequent occurrence or high densities in the tissues, E. purpurascens, G. roseum, T. roseum, Cladosporium spp. and several yeasts appeared well adapted and competitive as non-pathogens in strawberry. Weak pathogens also were retained for biocontrol tests because of potential antagonism of virulent forms through induced resistance or other mechanisms (Ku6, 1987). About 400 isolates of micro-organisms from living and dead foliage, flowers and fruit of strawberry plants in the field and in the wild formed the basis of our biocontrol screening program. When feasible, several isolates of the same species or genus were included. Isolates of mycelial fungi, yeasts, and bacteria were used.

B. Biocontrol Tests 1. General Considerations Effectiveness of micro-organisms in controlling foliage, flower and fruit diseases can be evaluated with confidence only in the cropping system or under conditions

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Plant population

" Environment (microclimate, soil, organisms) Cultural practices other human \ interference . Biocontrol agent I" population _..

Pathogen population

Fig. 1. Schematic illustration of interactions among plants, pathogens, biocontrol agents, environmental variables, and human interferences in biocontrol systems in crops (adapted from Burpee, 1990).

closely representative of the cropping system (Sutton and Peng, 1993). The rationale of this precept is clear. Disease epidemics involve spatiotemporal interactions between host and pathogen populations under the influence of the environment and human interferences (Kranz, 1974; Zadoks and Schein, 1979). Micro-organisms introduced into a crop to control a disease must be able to interact appropriately with the pathogen, the host, and other organisms under the prevailing microclimatic conditions in order to be effective (Fig. 1). The biocontrol system is highly dynamic and can involve growth and development of the host, infection cycles and serial dispersals of the pathogen, quantitative shifts in populations of the biocontrol agent and indigenous organisms, and microclimatic fluctuations. In general, epidemics cannot be satisfactorily simulated in the laboratory, growth room, and greenhouse, and biocontrol tests done in these conditions should be interpreted accordingly. Biocontrol tests under controlled conditions can serve effectively for use in preliminary screening of organisms and for complementing work done in the crop. A key objective in the design of biocontrol tests done in plots or in controlled environments is to minimize representational errors (Vanderplank, 1963; James, 1974; Zadoks and Schein, 1979; Aust and Kranz, 1988; Sutton, 1988) relative to the well-managed crop. Procedures in field plots for biocontrol tests should follow good crop recommendations and are generally similar to those used for plots to test chemical pesticides and other disease-control measures. Possible interplot interference by dispersal of test organisms among plots is a special consideration

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in the spacing of plots for biocontrol tests. In this respect, sprinkler irrigation may best be avoided in favor of trickle or furrow methods. In many field studies it is necessary to introduce the pathogen to assure adequate density and distribution of inoculum in plots. However, the common practice of applying a high population of pathogen propagules at about the same time as when the biocontrol agent is introduced is, in most instances, unrepresentative of natural dispersal patterns and densities of pathogens in the field, and may overwhelm biocontrol effectiveness of many organisms. A more realistic alternative is to provide a source of initial inoculum in plots early in the cropping season and allow infection cycles of the pathogen and disease increase to occur naturally. Even in controlled tests, measures such as plant growth conditions (light, fertilizer, etc.) and pathogen treatments can be taken to simulate those of the cropping system and to minimize cryptic errors. For logistical reasons, only a few organisms normally can receive intensive evaluation under representative crop conditions in the field. These tests usually are intensive and demand numerous measurements of biocontrol agents, pathogen populations, disease, plant growth, and microclimatic variables. Each organism may require a series of evaluations to answer critical questions pertaining to concentration, timing and targeting of inoculum applications. Organisms can be effectively evaluated in large numbers, however, using whole plants, attached plant organs, or detached tissues in the field, greenhouse, growth room, or lal~oratory, and selected observations of these tests compared with those in field plots. In vitro methods are unrealistic for screening and results usually do not correlate well with those obtained in the field (Andrews, 1985). 2. Screening Organisms The microbial isolates from strawberry were evaluated against B. cinerea in a sequence of tests on strawberry plants in the laboratory, growth room, greenhouse, and field plots (Peng and Sutton, 1991). It can be argued that the respective environments increasingly mimicked those of commercial strawberry crops microclimatically and microbiologically. Consistent with disease-management strategies, tests were done against B. cinerea in leaves, and to protect flowers and fruits against the pathogen. Initial screening was done using a leaf disc assay. Discs from 10-day-old leaves of greenhouse-grown plants were washed to remove incidental organisms, placed in humidity chambers, and inoculated with propagule suspensions first of the test organisms (107 ml -~) and 24 h later with B. cinerea (106 conidia ml-l). After a further 24 h to allow infection by the pathogen, the discs were transferred to an agar medium containing paraquat to kill the tissues and allow rapid production of conidiophores of the pathogen which were quantified as an indication of biocontrol effectiveness of the test organism. Biocontrol ranged from 0 to 100 %, but none of the organisms promoted the pathogen. Cluster analysis separated the organisms into five categories of biocontrol effectiveness. Bacteria, yeasts, Verticillium spp., T. roseum and Aspergillus spp. were relatively ineffective. Isolates of

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E. purpurascens and A. alternata turned up in three and all five clusters, respectively, underscoring the importance of quantifying biocontrol on an isolate basis. The most powerful cluster ( > 96% suppression) included all tested isolates of G. roseum, Myrothecium verrucaria and Trichoderma viride, plus some isolates of Penicillium spp., Fusarium spp., Colletotrichum gloeosporioides and E. purpurascens besides A. alternata. Eleven organisms, representing members of each cluster, were then evaluated against B. cinerea on detached petals, and on attached leaves and flowers of strawberry in the growth room and greenhouse (Peng and Sutton, 1991). Tissues were inoculated as before with test organisms and 24 h later with the pathogen. After a 24-h postinoculation humid period, discs cut from attached leaves and petals and stamens detached from test flowers were placed on the paraquat medium and conidiophores of B. cinerea were later estimated. Biocontrol effectiveness of the organisms among the assays was similar in pattern and ranking. A Pearson's r value of 0.96 (P _< 0.01) was obtained when observations of leaf-disc and petal assays were compared. Biosuppression on attached organs ranged from 24-65% to 97-100% and r values of 0.78-0.94 and 0.82-0.96 (P < 0.01) were obtained, respectively in comparisons of these observations with those in leaf disc and petal assays. While relative effectiveness of a majority of the organisms was similar in the different tests, E. purpurascens and M. verrucaria were notably less effective on attached than on detached tissues. G. roseum was completely effective or nearly so in all tests. The 11 organisms were evaluated over 2 years in the field using 4 m x 1 m plots in 2-3 year-old matted row plantings of 'Redcoat' strawberries, the same as used in the controlled environments (Peng and Sutton, 1991). The plantings were maintained according to Ontario recommendations but without fungicides, and trickle irrigation was used in place of sprinklers. A spore suspension of B. cinerea (2 x 103 conidia m1-1) was applied in the plots when flowering began in order to reduce marked irregularity in pathogen distribution. A more realistic method of introducing the pathogen would have been to apply infested host leaves, but this was not practical in these instances. Key remaining questions were when and how to introduce the test organisms. Recognizing that density of biocontrol organisms introduced to above-ground portions of plants usually declines precipitously, and that our purpose was to estimate relative, not optimal, performance of the organisms, it was decided to apply treatments four times on a weekly schedule during the flowering and fruiting period. As with fungicide treatments, weekly applications of biocontrol agents targeted primarily at the flowers were not ideal because flowers that opened shortly after treatment probably went untreated. Suspensions of fungal conidia and yeast cells (106 and 107 propagules ml -l water plus surfactant, respectively), a suitable check, and captan to serve as a standard of commercial disease control, were applied with a compressed air sprayer shortly before nightfall and dew onset. The importance of timing biocontrol treatments in relation to daily changes in microclimate remains in question. An open-top chamber was positioned over each plot during treatment to prevent

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spray drift. Incidence of B. cinerea in stamens and fruits were estimated to measure biocontrol effectiveness. Relative effectiveness of the organisms correlated significantly among the field tests (Pearson's coefficient, r, - 0.53 - 0.89, P _ 0.01 - 0.01) and among field and controlled tests (Spearman's ranking coefficient 0.42 - 0.82, P _ 0.10 0.01). Consistent ranking was evident for a majority of isolates but M. verrucaria and A. alternata ranked poorly in the field compared with controlled conditions. The generally similar rankings of isolates among controlled and field tests indicated that each of the controlled assays was suitable for preliminary appraisal of test organisms. It did not seem to matter whether leaves or flowers were used or whether they were attached or detached. The leaf disc assay, however, was least demanding in terms of plant materials, growth facilities, and time. In the field tests, isolates of G. roseum, Penicillium sp., T. viride, G. gloeosporioides, E. purpurascens and T. roseum were the more effective organisms and suppressed B. cinerea by 79-93 % in stamens and 48-76 % in fruits. Several of these isolates were at least as effective as captan. All except T. viride were prominent members of the strawberry mycoflora (McLean and Sutton, 1992). Isolates of G. roseum, Penicillium sp. and T. viride were selected for further evaluation as biocontrol agents; each were highly effective in a majority of tests and none had produced symptoms on strawberry. 3. Further Evaluation of Leading Candidates Suppression of B. cinerea in Redcoat plantings at two or three locations in two growing seasons gave no assurance of general effectiveness of the biocontrol candidates in strawberry cropping systems. The possibility that host genotype and microclimatic conditions not experienced in the initial tests could affect biocontrol (Fig. 1) prompted investigations of biocontrol by G. roseum in eight June-bearing cultivars (Annapolis, Blomidon, Governor Simcoe, Honeoye, Kent Redcoat, Vantage and Veestar) of differing parentage and susceptibility to B. cinerea (G. Xue, J. C. Sutton and J. A. Sullivan, unpublished). The studies were done in field plots during 2 years using methods similar to those in the previous studies. It turned out that the cultivars and biocontrol agent did not interactively affect B. cinerea. Gliocladium roseum suppressed B. cinerea in leaves, petals, stamens and fruits as effectively or better than did captan. Ranking of fruit rot incidence among the cultivars correlated well with that of sporulation density of B. cinerea on leaves and sporulation incidence on stamens (Spearman's coefficient - 0.76 in both cases), but negatively with sporulation density on petals ( - 0.82). The tests increased confidence that G. roseum was effective in a wide range of weather conditions. Biocontrol of B. cinerea in everbearer strawberries presented special challenges related to prolonged flowering and fruiting and sparse epidemiologic information. In a 2-year study, G. roseum, T. viride and captan were applied weekly for 12 weeks, starting at first flowering, to cuhivars Tribute and Tristar (A. Dale and J . C . Sutton, unpublished). Fruits harvested twice weekly from late July until

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October were assessed for incidence of B. cinerea. The test organisms were of similar effectiveness in both years. The biocontrol agents (applied at 107 conidia ml-1) and the fungicide suppressed incidence of B. cinerea in fruits by 32-70%, with the poorer performance levels during cool and humid conditions late in the cropping season. G. roseum reduced flower abortion from 9 to 2 % during August. The agents were about 10-25 % less effective than captan in suppressing B. cinerea in fruit harvested in late July and early August, but of similar or greater effectiveness in fruit of subsequent harvests. Possibly a build-up of the agents in the crop during the initial weeks of treatment raised the level of biocontrol. As in Junebearers, strategies to optimize timing of biocontrol treatments in everbearers remain to be worked out. The isolates of G. roseum, T. viride and Penicillium sp. were remarkably effective in suppressing sporulation potential of B. cinerea in strawberry leaves. Redcoat leaves were inoculated with B. cinerea (105-106 conidia m1-1) and treated 2-5 weeks later with the test isolates (107 conidia ml-1) or with chlorothalonil. The respective organisms suppressed B. cinerea by 97-100 % in attached leaves in the greenhouse, by 58, 64 and 48 % respectively in semisenescent overwintered leaves in the field, and by 81-100%, 59-100% and 53-87% when applied to green leaves in strawberry field plots in spring, late summer and early autumn (Peng and Sutton, 1990; Sutton and Peng, 1993). G. roseum was consistently as effective as ehlorothalonil, which in previous studies suppressed B. cinerea in strawberry leaves better than other commercially available fungicides and controlled fruit rot when applied only to the leaves before flowering began (Braun and Sutton, 1986; Sutton, 1990). Penicillium sp. and T. viride were as effective as chlorothalonil in the greenhouse but in only three of six field studies. G. roseum was selected for continued development as a biocontrol agent based on consistent effectiveness of all tested isolates under a wide range of conditions in strawberry cropping systems. The antagonist also has the advantages of easy inoculum production, sticky conidia which may help avoid allergic responses in the user, and common occurrence as an indigenous fungus in strawberry fields which may favor registration for commercial use.

C. Vectoring of Biocontrol Organisms by Bees Efficiency of application method could be a decisive factor in acceptability of biocontrol by strawberry growers. Spray methods are acceptable for treating foliage but are highly inefficient for treating flowers (Sutton, 1990). In seeking an alternative it was surmised that bees, including the European honey bee (Apis mellifera L.), might serve as vehicles to deliver biocontrol agents to strawberry flowers. Bees, after all, are well known as vectors of pollen, fungi and bacteria among flowers of various plant species (Free, 1970; Harrison et al., 1980). Honey bees were therefore examined as vectors of G. roseum to strawberry flowers. Vectoring was investigated using a powder formulation of the biocontrol agent

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and an inoculum dispenser to contaminate the bees with the formulation each time they left the hive (Peng et al., 1992). Constructed of wood, hardware cloth, and Plexiglas | the dispenser fitted inside the lower portion and front of the hive. A formulation of G. roseum with pure talc and corn meal (10:1, w : w ) at 5 x 108cfu g - ' was spread about 5-8 mm deep on a removable tray in the dispenser. Outgoing bees were obliged to crawl about 12 cm through the inoculum before leaving the hive. Bees emerging from dispensers carried an average of 570 000 cfu G. roseum per bee and deposited a mean of 1600-27 000 cfu on each flower. Inoculum density of G. roseum on flowers treated by bees was at least as high, and more stable, than on flowers in plots that received weekly sprays of 107 conidia G. roseum m l - ' water plus surfactant. Effectiveness of the bee and spray methods in suppressing B. cinerea on petals, stamens and fruits was in each instance high and did not differ significantly. While bees were effective delivery vehicles of G. roseum to strawberry flowers, absolute efficacy of this method in terms of inoculum required per unit area of strawberry planting remains to be estimated. In other recent biocontrol studies, honey bees successfully vectored G. roseum to raspberry flowers (Yu and Sutton, unpublished), species of Gliocladium, Epicoccum and Alternaria to rapeseed flowers (Israel and Boland, 1992), and Pseudomonas fluorescens and Erwinia herbicola to apple and pear flowers (Thomson et al., 1992; Johnson etal., 1993). Fungal agents were formulated with various talcum powders, pulverized corn meal, wheat flour, soya flour and corn starch, each with particle sizes generally in the range of 5-15 #m (Yu and Sutton, unpublished; Israel and Boland, 1992), while bacteria were adsorbed on apple and cattail pollen (Thomson et al., 1992) or were used as freeze-dried preparations with cryoprotective skim milk and xanthan (Johnson etal., 1993). Interestingly, this surge of studies on vectoring of biocontrol agents came a century after Waite (1891) first discovered that honey bees vectored the pathogen Erwinia amylovora to pear blossoms. Principal stages in vectoring of biocontrol agents are acquisition and transport of inoculum by the vector, and transfer of the inoculum from the vector to target sites. Sufficient inoculum must be vectored to suppress the pathogen adequately. In the vectoring studies of G. roseum, the bees acquired inoculum on almost all external surfaces, including those of the head, thorax, wings, abdomen and legs (Peng et al., 1992). Conidia and carrier particles were especially abundant on the setae. Stickiness of the conidia possibly facilitated acquisition; however, bees are able also to vector dry-spored fungi (Israel and Boland, 1992). Many bees attempted to remove inoculum, especially from the head and antennae, for about 20-50 s immediately prior to take-off, but otherwise did not show abnormal behavior or signs of stress. Accumulations of inoculum in front of dispensers and inoculum clouds sometimes visible around bees indicated considerable inoculum loss at take-off. Inoculum recovered from plants in check plots probably resulted from inoculum loss by overflying bees. Transfer of inoculum from the bee to the flower may involve direct contact of the bee with flower parts and possibly local dispersal

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while the bee actively moves when on the flower. Honey bees often make good contact with strawberry stamens, which probably is important for biocontrol. Redistribution of inoculum among flowers is possible and some inoculum is deposited in the hive, so it is questionable whether the honey should be used for human consumption. Mobility of bees presents problems in studies of vectoring in field plots. Screening materials used to separate bee treatments from those without bees results in substantial shading (e.g. 30-60%) and thus microclimatic shifts in plots. Construction of screened enclosures over all plots equalizes the microclimatic changes, but is expensive and sometimes impractical. Honey bees behave differently when confined in enclosures than when allowed to forage freely. Many spend considerable time attempting to escape, and usually do so should a hole develop in the screening. Bees allowed to forage freely may provide the most representative information on vectoring relative to that which would take place in crops, but check treatments must still be protected from intrusions by bees. Honey bees readily establish foraging patterns in preferred nectar sources outside plot areas, as occurred in our studies when nearby rapeseed bloomed (Peng et al., 1992). Chemical bee attractants applied in plots help to avoid external foraging but represent an additional interference factor. The importance of'foreign' bees and other insects as interference factors in vectoring studies is not known. Honey bees generally do not forage readily in cool ( < 17~ or rainy weather, but brief periods of unfavorable conditions did not markedly reduce vectoring of G. roseum and biocontrol of B. cinerea in strawberry. Species of bumble bees (Bombus spp.) that regularly forage when air temperature falls as low as 6~ (Heinrich, 1979) are now under investigation as vectors of G. roseum (Yu and Sutton, unpublished). Quantitative and spatial information of bee colonies in relation to vectoring of biocontrol agents and biocontrol effectiveness require field-scale studies. These kinds of observations in small plots are confounded by variable foraging by bees outside the plot area, either out of necessity or because of preferences in nectar sources. Outside foraging can diminish markedly as the planting area increases provided that suitable precautions are taken. It is well known, for example, that bees of colonies placed in a crop before flowering begins will probably establish foraging patterns outside the crop area and maintain these even after the crop begins to flower. This can be avoided by introducing colonies after flowering has begun. Because of bee foraging habits, quantitative information of vectoring in small plots, unlike that of spray treatments, should not be extrapolated to the field scale. Studies on the number, size and distribution of colonies in relation to vectoring and biocontrol of B. cinerea under various weather conditions are needed to provide information to optimize vectoring operations in crops. This information would also allow realistic comparisons on the efficiency of inoculum application by bees and as sprays.

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D. Biocontrol Mechanisms of Gliocladium roseum The effectiveness of G. roseum in suppressing B. cinerea in strawberry under a wide range of conditions is a function of its ecological relationships with strawberry and its ability to outcompete B. cinerea in the tissues under cool as well as warm temperatures. The ecological relationships are best known for strawberry leaves. Like B. cinerea, G. roseum is able to penetrate into the leaves while they are green and to colonize the tissues progressively when they senesce and die. After application to green leaves infected with B. cinerea, isolates of the antagonist markedly suppressed growth and sporulation of the pathogen when the leaves senesced and died (Sutton and Peng, 1993). Evidently, G. roseum colonizes and exploits the leaf tissues much more rapidly than B. cinerea and largely precludes colonization by the pathogen. Effectiveness of the antagonist was markedly reduced when it was applied to senescent or dead leaves, probably because the pathogen had a head start in colonizing the tissues under these circumstances. Unlike isolates of T. viride and Penicillium sp., those of G. roseum markedly suppressed G. roseum at 10~ and 15~ as well as at 20~ and 25~ (Sutton and Peng, 1993). From our studies, substrate competition rather than antibiosis or hyperparasitism is the key biocontrol mechanism of G. roseum against B. cinerea in strawberry leaves (Peng, 1991; Sutton and Peng, 1993). The antagonist is able to produce antifungal metabolites that suppress growth and germination of B. cinerea in vitro, but ultraviolet-light induced mutants that produced high, moderate, or non-detectable levels of the principal metabolite did not differ in biocontrol effectiveness against the pathogen. Although G. roseum is a well-known mycoparasite, no evidence was found for mycoparasitism of B. cinerea in strawberry leaves.

VI. CONCLUSIONS AND FUTURE DIRECTIONS Screening of strawberry-associated microflora against B. cinerea by means of assays on strawberry plant materials and field plot tests successfully identified biocontrol agents that performed well in the strawberry cropping system. Gliocladium roseum, Penicillium sp. and T. viride emerged as the best group of antagonists within the limits of the tests; however, field tests of additional organisms that were effective in the leaf disc assays would probably identify other useful agents, as might tests of further microflora from cultivated or wild strawberries, or other sources. Gliocladium roseum has numerous advantages for practical biocontrol of B. cinerea in strawberry. Because it is effective in leaves, flowers and fruits, it can be targeted successfully against B. cinerea at the inoculum source in the leaves or to protect the flowers and fruits directly. The ability of G. roseum to penetrate and survive in the leaves results in extraordinary persistence of the antagonist in the foliage for weeks or months after application, which is in sharp contrast to many biocontrol agents that are active against pathogens chiefly on the phylloplane and

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quickly decline in numbers and activity after application (Andrews, 1985). As a consequence of its persistence in green leaves and biocontrol activity when the leaves senesce and die, G. roseum applied once at any time while the leaves are green potentially controls B. cinerea in each leaf flush. As found in field studies and in contrast to chlorothalonil, G. roseum is less effective or ineffective when applied to senescing or dead leaves (Sutton and Peng, 1993). Inoculum production of G. roseurn is easily scaled up on cheap substrates such as wheat grains which should favor cost effectiveness of biocontrol. Besides its versatility against B. cinerea in strawberry, G. roseum also suppresses effectively the pathogen in raspberry and in spruce seedlings (Sutton, unpublished; Zhang etal., 1994) thereby widening the market potential of the antagonist. Further studies are needed to facilitate and optimize use of G. roseum in strawberry crops, and probably to satisfy registration requirements in Canada. Information is required on methods to produce, formulate, store and package inoculum on a commercial scale while maintaining important quality characteristics including viability and effectiveness of the biocontrol agent. Treatment methodology also requires further investigation. The possibility that a single spray applied to the leaves before flowering would suppress initial inoculum sufficiently to obviate the need to treat the flowers, as was observed with fungicide treatments (Braun and Sutton, 1986), is worth exploring. Studies are needed to optimize the timing of sprays applied to flowers in respect to frequency, host phenology, and microclimatic variables such as rain, daily periods of light and darkness, and dryness and wetness of the foliage and flowers. Much remains to be learned of spray nozzles, application pressures and droplet sizes in relation to spray applications. The newly emerging methods of inoculum delivery by bees will undoubtedly be further explored, and could be easy to implement since many growers already use bees to pollinate strawberries. Integration of biocontrol methods with other practices to protect and produce strawberries should not prove difficult; few potential conflicts are foreseen except in some instances between insecticides and bee vectors. Use of G. roseum or other agents to control B. cinerea on the farm would be a major step towards non-chemical disease management in strawberries.

ACKNOWLEDGMENTS Support by the Natural Sciences and Engineering Research Council of Canada, Grant OGP0006119, and of the Pesticides Advisory Committee of the Ontario Ministry of the Environment, is gratefully acknowledged.

REFERENCES Andrews, J. H. (1985). Strategies for selecting antagonistic microorganisms from the phyUoplane. In 'Biological Control on the Phylloplane' (C. E. Windles and S. E. Lindow, eds), pp. 31-44. The American Phytopathological Society, St Paul, MN.

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Aust, H.J. and Kranz, J. (1988). Experiments and procedures in epidemiological field studies. In 'Experimental Techniques in Plant Disease Epidemiology' (J. Kranz and J. Rotem, eds), pp. 7-17. Springer-Verlag, Berlin. Barritt, B. H. (1980). Resistance of strawberry clones to Bottytis fruit rot. Journal of the American Societyfor Horticultural Science 105, 160-164. Bhatt, D. D. and Vaughan, E. K. (1962). Preliminary investigations on biological control of grey mould (Botrytis cinerea) of strawberries. Plant Disease Reporter 46, 342-345. Bhatt, D. D. and Vaughan, E. K. (1963). Interrelationships among fungi associated with strawberries in Oregon. Phytopathology 53, 217-220. Braun, P.G. and Sutton, J . C . (1986). Management of strawberry gray mould by fungicides targeted against inoculum in crop residues. In 'Proceedings of the British Crop Protection Conference, Pests and Diseases' Vol. 3, pp. 915-921. British Crop Protection Council, Croydon. Braun, P. G. and Sutton, J. C. (1987). Inoculum sources of Botrytis cinerea in fruit rot of strawberry in Ontario. CanadianJournal of Plant Pathologj, 9, 1-5. Braun, P. G. and Sutton,J. C. (1988). Infection cycles and population dynamics of Botrytis cinerea in strawberry leaves. CanadianJournal of Plant Pathology 10, 133-141. Bristow, P.R., McNichol, R.J. and Williamson, B. (1986). Infection of strawberry flowers by Bot~ytis cinerea and its relevance to grey mould development. Annals of Applied Biology 109, 545-554. Burpee, L. L. (1990). The influence of abiotic factors on biological control of soilborne plant pathogenic fungi. Canadian Journal of Plant Pathology 12, 308-317. Cook, R.J. (1992). Reflections of a regulated biocontrol researcher. In 'Regulations and Guidelines: Critical Issues in Biological Control. Proceedings of a USDA/CSRS National Workshop, June 10-12, 1991, Vienna, VA (R. Charudattan and H.W. Browning, eds), pp. 9-24. Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL. Cook, R.J. (1993). Making greater use of microorganisms for biological control of plant pathogens. Annual Review of Phytopatholog), 31, 53-80. Cook, R.J. and Baker, K. F. (1983). 'The Nature and Practice of Biological Control of Plant Pathogens'. The American Phytopathological Society, St Paul, MN. Cooke, R. C. and Rayner, A. D. M. (1984). 'Ecology of Saprotrophic Fungi'. Longman, London. Galletta, G.J. and Bringhurst, R. S. (1990). Strawberry Management. In 'Small Fruit Crop Management' (G. J. Galletta and D. G. Himelrick, eds), pp. 83-156. Prentice Hall, Englewood Cliffs, NJ. Free, J. B. (1970). 'Insect Pollination of Crop Plants'. Academic Press, London. Harrison, M. D., Brewer, J. W. and Merrill, L. D. (1980). Insect involvement in the transmission of bacterial pathogens. In 'Vectors of Plant Pathogens' (K. F. Harris and K. Maramorosch, eds), pp. 293-324. Academic Press, New York. Heinrich, B. (1979). 'Bumblebee Economics'. Harvard University Press, Cambridge, MA. Israel, M. S. and Boland, G.J. (1992). Influence of formulation on efficacy of honey bees to transmit biological controls for management of sclerotinia stem rot of canola. (Abstr.) Canadian Journal of Plant Pathology 14, 244. Jarvis, W. R. (1962a). The infection of strawberry and raspberry fruits by Botrytis cinerea Fr. Annals of Applied Biology 50, 569-575. Jarvis, W. R. (1962b). The epidemiology of Botrytis cinerea Pers. in strawberries. In 'Proceedings of the 16th International Horticultural Congress, August 31-September 8, 1982, Brussels, Belgium'. pp. 258-262. Duculot, Gembloux, Belgium. Jarvis, W. R. and Borecka, H. (1968). The susceptibility of strawberry flowers to infection by Botrytis cinerea. Horticultural Research 8, 147-154.

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James, w . c. (1974). Assessment of plant diseases and losses. Annual Review of Phytopathology 12, 27-48. Johnson, K. B., Stockwell, V. O., Burgett, D. M., Sugar, D. and Loper, J. E. (1993). Dispersal of Erwinia amylovora and Pseudomonasfluorescens by honey bees from hives to apple and pear blossoms. Phytopathology 83, 478-484. Ku6, J. (1987). Plant immunization and its applicability for plant disease control. In 'Innovative Approaches to Plant Disease Control' (I. Chet, ed.), pp. 255-274. Wiley, New York. Kranz, J. (1974). Comparison of epidemics. Annual Review of Phytopathology 12, 355374. Maas, J. L. (1978). Screening for resistance to fruit rot in strawberries and raspberries: a review. HortScience 13, 423-426. Maas, J. L. ed. (1984). 'Compendium of Strawberry Diseases'. The American Phytopathological Society, St Paul, MN. McLean, M. A. (1988). The microflora of strawberry in relation to biological control of grey mould fruit rot caused by Botrytis cinerea Pers. ex. Fr. MSc Thesis, University of Guelph, Guelph, Ontario. McLean, M. A. and Sutton, J. C. (1992). Mycoflora of strawberry in Ontario. Canadian Journal of Botany 70, 846-852. Peng, G. (1991). Biological control of grey mould (Botrytis cinerea) on strawberries. PhD thesis, University of Guelph, Guelph, Ontario. Peng, G. and Sutton, J. C. (1990). Biological methods to control grey mould of strawberry. 'Proceedings of the Brighton Crop Protection Conference, Pests and Diseases', Vol. 1, pp. 233-240. British Crop Protection Council, Farnham, UK. Peng, G. and Sutton, J. C. (1991). Evaluation of microorganisms for biocontrol of Botrytis cinerea in strawberry. CanadianJournal of Plant Pathology 13,247-257. Peng, G., Sutton, J. C. and Kevan, P. G. (1992). Effectiveness of honey bees for applying the biocontrol agent Gliocladium roseum to strawberry flowers to suppress Botrytis cinerea. Canadian Journal of Plant Pathology 14, 117-129. Powelson, R. L. (1960). The initiation of strawberry fruit rot caused by Botrytis cinerea. Phytopathology 50, 491-494. Scher, F. M. and Castagno, J. R. (1986). Biocontrol: A view from industry. CanadianJourhal of Plant Pathology 8, 222-224. Simpson, D. W. (1989). Botrytis cinerea infection in pistillate and hermaphrodite strawberry flowers. Acta Horticulturae 265, 555-560. 9 Simpson, D. W. (1991). Resistance of Botrytis cinerea in pistillate genotypes of the cultivated strawberry Fragaria ananassa. Journal of Horticultural Science 66, 719-723. Sutton, J . C . (1988). Predictive value of weather variables in the epidemiology and management of foliar diseases. Fitopatologia brasileira 13, 305-312. Sutton, J. C. (1990). Epidemiology and management of botrytis leaf blight of onion and gray mould of strawberry: a comparative analysis. CanadianJournal of Plant Pathology 12, 100-110. Sutton, J. C. (1991). Alternative methods for managing gray mold of strawberry. In 'The Strawberry into the 21st Century' (A. Dale and J. J. Luby, eds), pp. 183-191. Timber Press, Portland, OR. Sutton, J. C. and Peng, G. (1993). Biocontrol of Botrytis cinerea in strawberry leaves. Phytopathology 83, 615-621. Sutton, J. C. and Peng, G. (1993). Manipulation and vectoring of biocontrol organisms to manage foliage and fruit diseases in cropping systems. Annual Review of Phytopathology 31,473-493. Sutton, J. C., James, T. D. W. and Dale, A. (1988). Harvesting and bedding practices in relation to grey mould of strawberries. Annals of Applied Biology 113, 167-175.

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Thomson, S. V., Hansen, D. R., Flint, K. M. and Vandenberg, J. D. (1992). Dissemination of bacteria antagonistic to Erwinia amylovora by honey bees. Plant Disease 76, 1052-1056. Tronsmo, A. and Dennis, C. (1977). The use of Trichoderma species to control strawberry fruit rots. NetherlandsJournal of Plant Pathology 83, 449-455. Suppl. I. Vanderplank, J. E. (1963). 'Plant diseases: Epidemics and Control'. Academic Press, New York. Waite, M. B. (1891). Results from recent investigations in pear blight. (Abstr.) Botanical Gazette 16, 259. Zadoks, J. C. and Schein, R. D. (1979). 'Epidemiology and Plant Disease Management'. Oxford University Press, New York. Zhang, P. G., Sutton, J. C. and Hopkin, A. A. (1994). Evaluation of microorganisms for biocontrol of Bot~ytis cinerea in container-grown black spruce seedlings. CanadianJournal of Forest Research 24, 1312-1316.

10 BIODIVERSITY AND BIOCONTROL: LESSONS FROM INSECT PEST MANAGEMENT M i g u e l A. Altieri Division of Biological Control, University of California - Berkeley, 1050 San Pablo Avenue, Albany, CA 94706, USA

I. II. III. IV.

Introduction Ecological Theory Concerning Biodiversity and Biocontrol Agroecosystem Biodiversification and Biological Control Enhancing Natural Enemy Biodiversity in Agroecosystems: the Case of Parasitic Hymenoptera A. Multiple Introductions of Parasitoids B. Reducing Direct Mortality by Eliminating Pesticides C. Provision of Supplementary Resources D. Increasing Adjacent Vegetational Diversity E. Increasing Within-field Plant Diversity F. Manipulating Host-plant Attributes G. Manipulations with Semiochemicals V. Conclusions References

191 192 194 202 203 203 204 204 204 205 205 206 206

I. I N T R O D U C T I O N Agriculture is a process of artificially manipulating nature and implies the simplification of the structure of the environment over vast areas, replacing nature' s diversity with a small number of cultivated plant species and domesticated animals. This process of biodiversity simplification reaches an extreme form in agricultural monocultures, which constitute artificial ecosystems, lacking selfregulatory mechanisms and thus requiring constant human intervention in the form of agrochemical inputs to maintain productivity (Ahieri, 1987). Nowhere are the consequences of biodiversity reduction more evident than in the realm of agricultural pest management. The instability of agroecosystems becomes manifest as the worsening of most insect pest problems is increasingly linked to the expansion of crop monocultures at the expense of the natural vegetation and local habitat complexity (Altieri and Letourneau, 1982). Plant communities that are modified to meet the special needs of humans become subject to heavy pest damage and generally the more intensely such communities are ADVANCES IN PLANT PATHOLOGY~VOL. 11 ISBN 0-12-033711-8

Copyright9 1995 Academic Press Limited All rights of reproduaion in anyform reserved

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modified, the more abundant and serious the pests. The inherent self-regulation characteristics of natural communities are lost when humans modify such communities through the shattering of the fragile thread of community interactions (Turnbull, 1969). Ecological theory suggests that this breakdown can be repaired by restoring the elements of community homeostasis through the addition or enhancement of biodiversity (Perrin, 1980). In modern agroecosystems, the experimental evidence suggests that biodiversity can be used for improved pest management (Flint and Roberts, 1988; Andow, 1991). Several studies have shown that it is possible to stabilize insect communities of agroecosystems by designing and constructing vegetational architectures which support populations of natural enemies and/or that have direct regulatory effects on pest herbivores. Biodiversity in agroecosystems can be as varied as the various crops, weeds, arthropods or micro-organisms involved, according to geographical location, climatic, edaphic, human and socioeconomic factors. Complementary interactions between the various biotic components can also be of a multiple nature. Some of these interactions can be used to induce positive and direct effects on the biological control of specific crop pests, as well as on soil fertility regeneration and/or enhancement and soil conservation. The exploitation of these interactions in real situations involves agroecosystem design and management and requires an understanding of the numerous relationships between soils, micro-organisms, plants, insect herbivores and natural enemies (Price et al., 1980). The idea is to enhance and/or regenerate the right kind of biodiversity that can subsidize the sustainability of agroecosystems by providing ecological services such as biological pest control but also nutrient cycling, water and soil conservation, etc.

II. ECOLOGICAL THEORY CONCERNING BIODIVERSlTY AND BIOCONTROL Mixing certain plant species with the primary host of a specialized herbivore gives a fairly consistent result: specialized species usually exhibit higher abundance in monoculture than in polycultures. In a recent review, Andow (1991) identified 209 published studies that deal with the effects of vegetation diversity in agroecosystems on herbivorous arthropod populations. Fifty-two per cent of the 287 total herbivore species examined in these studies were found to be less abundant in diversified systems than in monocultures, while only 15.3% (44 species) exhibited higher densities in polycultures. Among the various ecological hypotheses that have been offered to explain lower pest-population loads in multispecies plant association, only one pertains to the role of natural enemies. This 'natural enemy hypothesis' predicts that there will be a greater abundance and diversity of natural enemies of pest insects in polycultures than in monocultures (Root, 1973). Predators tend to be polyphagous and have broad habitat requirements, so they would be expected to

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encounter a greater array of alternative prey and microhabitats in a heterogeneous environment. Annual crop monocultures do not provide adequate alternative sources of food (pollen, nectar, prey), shelter, breeding and nesting sites for the effective performance of natural enemies (Rabbet al., 1976). The natural enemy hypothesis has been stated in the following way: 1. A greater diversity of prey and microhabitats is available within complex environments. As a result, relatively stable populations of generalized pre: dators can persist in these habitats because they can exploit the wide variety of herbivores that become available at different times or in different microhabitats (Root, 1973). 2. Specialized predators are less likely to fluctuate widely because the refuge provided by a complex environment enables their prey to escape widespread annihilation (Risch, 1981). 3. Diverse habitats offer many important requisites for adult predators and parasites, such as nectar and pollen sources, which are not available in monocultures, reducing the probability that they will leave or become locally extinct (Risch, 1981). According to Root' s enemies hypothesis, generalist and specialist natural enemies are expected to be more abundant in polycultures and, therefore, more effectively suppress herbivore population densities in polycultures than in monocultures. Generalist predators and parasitoids should be more abundant in polycultures than monocultures because (1) they switch and feed on the greater variety of herbivores that become available in polycultures at different times during the growing season; (2) they maintain reproducing populations in polycultures while in monocultures only males of some parasitoids are produced; (3) they can utilize hosts in polycultures that they would normally not encounter and use in monocultures; (4) they can exploit the greater variety of herbivores available in different microhabitats in the polycultures; and (5) prey or hosts are more abundant or more available in polycultures (Andow, 1991). Specialist predator and parasitoid populations are expected to be more abundant and effective in polycultures than monocultures because prey or host refuges in polycultures enable the prey or host populations to persist, which stabilizes predator-prey and parasitoid-host interactions, while in monocultures predators and parasitoids drive their prey or host populations to extinction and become extinct themselves shortly thereafter. Prey or host populations will recolonize these monocultures and rapidly increase (Andow, 1991). Finally, both generalist and specialist natural enemies should be more abundant in polycultures than monocultures because more pollen and nectar resources are available at more times during the season in polycultures than monocultures (Altieri and Letourneau, 1982). Sheehan (1986) and Russell (1989) have questioned the universal validity of the natural enemy hypothesis that explains the effects of agroecosystem diversification on searching behavior and success of arthropod natural enemies, and claims

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that such interactions are still poorly understood. Fifty per cent of the 18 studies reviewed by Russell (1989) found higher herbivore mortality from predation or parasitism in diverse systems, but according to Russell, a lack of adequate control in all but one study prevented researchers from concluding that the above difference in mortality is what really reduces the numbers of herbivores in complex systems. He further argues that the enemies hypothesis and the resource concentration hypothesis act as complementary mechanisms in reducing numbers of herbivores in polycultures, and that, therefore, both should be enhanced simultaneously to achieve maximum control. According to Sheehan (1986), the enemies hypothesis is simplistic in several respects. Victim location by generalist enemies may be hindered by increased plant density or patchiness in diverse agricultural systems. In fact, crop diversification may reduce enemy-searching efficiency and destabilize predator/prey interactions. Specialist enemies, often important in biological control programs, may be particularly sensitive to vegetation texture. Pest control by specialist enemies may be more effective in less diverse agroecosystems if concentration of host plants increases attraction or retention of these enemies. Thus, it is possible that certain specialist enemies may not necessarily respond to habitat diversification in the same way as generalists. Sheehan (1986) suggested that specialist parasitoids might be less abundant in polycultures than monocuhures because (1) chemical cues used in host finding will be disrupted and the parasitoids will be less able to find hosts to parasitize and feed upon in polycuhures; and (2) the indistinct boundary at the edges of polycultures will be hard to recognize and they will be more likely to leave polycultural habitats than monocultures. In addition, Andow and Prokrym (1990) showed that structural complexity, or the connectedness of the surface on which a parasitoid searches, can strongly influence parasitoid host-finding rates. An implication of their study is that structurally complex polycultures would have less parasitism than structurally simple monocultures. Factors that increase immigration to, and decrease emigration from, host-plant areas by specialist enemies (e.g. large patch size, close plant spacing, the presence of specific chemical or visual stimuli, and lower chemical or structural diversity of associated vegetation) may cause those enemies to remain longer and hunt more effectively in simple than in diverse agroecosystems, at least in those that are not too extensive.

III. AGROECOSYSTEM BIODIVERSIFICATION AND BIOLOGICAL CONTROL Crop monocultures are difficult environments in which to induce efficient biological pest control because these systems lack adequate resources for effective performance of natural enemies and because of the disturbing cultural practices often utilized in such systems. More diversified cropping systems already contain

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certain specific resources for natural enemies provided by plant diversity, and are usually not disturbed with pesticides (Altieri and Letourneau, 1984). Thus, by replacing or adding diversity to existing systems, it may be possible to exert changes in habitat diversity that enhance natural enemy abundance and effectiveness by (van den Bosch and Telford, 1964; Powell, 1986): 1. 2. 3. 4.

Providing alternative hosts/prey at times of pest host scarcity. Providing food (pollen and nectar) for adult parasitoids and predators. Providing refuges for overwintering, nesting, and so on. Maintaining acceptable populations of the pest over extended periods to ensure continued survival of beneficial insects.

The specific resulting effect or the strategy to use will depend on the species of herbivores and associated natural enemies, as well as on properties of the vegetation, the physiological condition of the crop, or the nature of the direct effects of particular plant species (Letourneau, 1987). In addition, the success of enhancement measures can be influenced by the scale upon which they are implemented (i.e. field scale, farming unit or region) since field size, within-field and surrounding vegetation composition, and the level of field isolation (i.e. distance from source of colonizers) will all affect immigration rates, emigration rates, and the effective tenure time of a particular natural enemy in a crop field. Perhaps one of the best strategies to increase effectiveness of predators and parasitoids is the manipulation of non-target food resources (i.e. alternate hostsprey and pollen-nectar) (Rabbet al., 1976). Here it is not only important that the density of the non-target resource be high to influence enemy populations, but that the spatial distribution and temporal dispersion of the resource be adequate also. Proper manipulation of the non-target resource should result in the enemies colonizing the habitat earlier in the season than the pest, and frequently encountering an evenly distributed resource in the field, thus increasing the probability of the enemy to remain in the habitat and reproduce (Andow and Risch, 1985). Certain polycultural arrangements increase and others reduce the spatial heterogeneity of specific food resources; thus particular species of natural enemies may be more or less abundant in a specific polyculture. These effects and responses can only be determined experimentally across a whole range of agroecosystems. The task is indeed overwhelming since enhancement techniques must necessarily be site-specific. The literature is full of examples of experiments documenting that diversification of cropping systems often leads to reduced herbivore populations. The studies suggest that the more diverse the agroecosystem and the longer this diversity remains undisturbed, the more internal links develop to promote greater insect stability. It is clear, however, that the stability of the insect community depends not only on its trophic diversity, but on the actual density-dependence nature of the trophic levels (Southwood and May, 1970). In other words, stability will depend on the precision of the response of any particular trophic link to an increase in the population from a lower level.

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Although most experiments have documented insect population trends in single versus complex crop habitats, a few have concentrated on elucidating the nature and dynamics of the trophic relationships between plants-herbivores and natural enemies in diversified agroecosystems. Several lines of studies have developed:

a. Crop-weed-insect interaction studies Evidence indicates that weeds influence the diversity and abundance of insect herbivores and associated natural enemies in crop systems. Certain weeds (mostly Umbelliferae, Leguminosae and Compositae) play an important ecological role by harboring and supporting a complex of beneficial arthropods that aid in suppressing pest populations (Beingolea, 1957; Leius, 1967; Altieri et al., 1977; Young and Teetes, 1977; Ahieri and Whitcomb, 1979). Specific examples of crop-weed associations that enhance biocontrol are provided in Table 1. b. Insect dynamics in annual polycultures Overwhelming evidence suggests that polycultures support a lower herbivore load than monocuhures. One factor explaining this trend is that relatively more stable natural enemy populations can persist in polycultures due to the more continuous availability of food sources and microhabitats (Risch, 1981; Helenius, 1989). The other possibility is that specialized herbivores are more likely to find and remain on pure crop stands, which provide concentrated resources and monotonous physical conditions (Root, 1973). Specific examples of insect suppressant polycultures are provided in Table 2. c. Herbivores in complex perennial crop systems Most of these studies have explored the effects of the manipulation of ground cover vegetation on insect pests and associated enemies. The data indicate that orchards with rich floral undergrowth exhibit a lower incidence of insect pests than clean-cultivated orchards, mainly because of an increased abundance and efficiency of predators and parasitoids (Altieri and Schmidt, 1985). In some cases, ground cover directly affects herbivore species which discriminate among trees with and without cover beneath. d. The effects of adjacent vegetation These studies have documented the dynamics of colonizing insect pests that invade crop fields from edge vegetation, especially when the vegetation is botanically related to the crop. A number of studies document the importance of adjoining wild vegetation in providing alternate food and habitat to natural enemies which move into nearby crops (van Emden, 1965; Wainhouse and Coaker, 1981). The available literature suggests that the design of vegetation management strategies must include knowledge and consideration of (1) crop arrangement in time and space; (2) the composition and abundance of non-crop vegetation within and around fields; (3) the soil type; (4) the surrounding environment; and (5) the type and intensity of management. The response of insect populations to

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Table 1. Selected example of cropping systems in which the presence of weeds enhanced the biological control of specific crop pests (based on Altieri and Letourneau, 1982; Andow, 1991). , .,.,,.,

Cropping systems Alfalfa

Alfalfa Apple

Weed species

Pest(s) regulated

Natural blooming weed complex

Alfalfa caterpillar

Grass weeds

Empoasca fabae

Phacelia sp. and Eryngium sp.

(Colias eurytheme)

San Jose scale

(Quadraspidio tus perniciosus) and aphids

Apple

Natural weed complex

Tent caterpillar

(Malacosoma americanum) and codling moth

Beans

Goosegrass

(Eleusine indica

and red sprangletop Broccolli Brussels sprouts

(Leptochloa filliformis)

Wild mustard Natural weed complex

(carpocapsa pomonella)

Increased activity of the parasitic wasp

Apanteles medicaginis ?

Increased activity and abundance of parasitic wasps

(Aphelinus mali

and Aphytis

proclia)

Increased activity and abundance of parasitic wasps

Leafhoppers

Chemical repellency or masking

Phyllotreta cruciferae

Trap cropping Alteration of colonization background and increase of predators

(Empoasca kraemer)

Imported cabbage butterfly ( P i e r i s rapae) and aphids

(Brevicoryne brassicae ) Delia brassicae Mamestra brassicae, Evergestis forficalis, Brevicoryne brassicae

Brussels sprouts Brussels sprouts

Sperpula arvensis Spergula arvensis

Cabbage

Crateagus sp.

Citrus

Hedera helix

Lachnosterna spp.

Citrus

Natural weed complex

Mites

Citrus

Natural weed complex Natural weed complex

Diaspidid scales

Coffee

Factor(s)involved

Diamondback moth

(Plutella rnaculipennis)

(Eotetranychus, Panonychus cirri, Metatetranychus cirri)

Pentatomid

Antestiopus intricata

?

Increaseof predators and interference with colonization Provision of alternate hosts for parasitic wasps (Herogenes sp.) Enhancement of

Aphytis lingnanensis ?

M. A. Altieri

198

Table II. (continued) Cropping systems

Weed species

Collards

Ragweed (Ambrosia artemisiifolia)

Collards

Amaranthus retroflexus, Chenopodium album, Xanthium strumarium Giant ragweed

Corn

Corn

Natural weed complex

Corn

Setaria viridis and S. feberii Ragweed

Cotton

Pest(s) regulated Flea beetle (Phyllotreta cruciferae) Green peach aphid (Muzus persicae)

European corn borer (Ostrinia nubilalis)

Heliothis zea, Spodop tera frugiperda Diabrotica virgifera and D. barberi Boll weevil (Anthonomus grandis)

Cotton

Ragweed and Rumex crispus

He/iothis spp.

Cotton

Salvia coccinae, Cissus adenecaulis Quick-flowering mustards

L ypus sp.

Mungbeans

Natural weed complex

Beanfly (Ophlomyia phaseol/~

Oil palm

Pueraria sp., Flemingia sp., ferns, grasses and creepers Ragweed

Scarab beetles (Oryctes rhinoceros and Chalcosoma atlas) Oriental fruit moth

Peach

Rosaceous weeds and Dactylis glomerata

Sorghum

Halianthus spp.

Leafhoppers ( Paraphlepsius irrorotus and Scaphytopius sp.) Schizophis graminun

Soybean

Broodleaf weeds and grasses Cassia obtusifolia

Cruciferous crops

Peach

Soybean

Cabbageworms (Pieris spp.)

Epilachira varivestis Nezara viridula, Anticarsia gemmatalis

Factor(s) involved Chemical repellency or masking Increased abundance of predators (Chrysopa carnea, Coccinellidae, Syrphidae) Provision of alternate hosts for the tachinid parasite L ydella grisescens Enhancement of predators

Provision of alternate hosts for the parasite Eurytoma tylodermatis Increased populations of predators ? Increased activity of parasitic wasps (Apanteles glomeratus) Alteration of colonization background ?

Provision of alternate hosts for the parasite Macrocen trus ancyliverus ?

Enhancement of Aphelinus spp. parasitoids Enhancement of predators Increased abundance of predators

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Table II. (continued) Cropping systems

Weed species

Pest(s) regulated

Soybean

Crotalaria sp.

Nezara viridula

Sugar cane

Euphorbia spp. weeds

Sugar-cane weevil (Rhubdosie/us obscurus)

Sugar cane

Grrssy weeds

Sugar cane

Berreria verticillata and Hyptis atrorubens Morning glory (Ipomoea sp.)

Aphid (Rhopalosiphum maidis) Cricket (Scapteriscus vicinus)

Sweet potatoes

Argus tortoise beetle (Chelymorpha cassidea )

Vegetable crops

Wild carrot (Daucus curola)

Japanese beetle (Popillia japonica)

Vineyards

Wild blackberry (Rubus sp.)

Grape leafhopper (Erythroneura elegantula)

Vineyards

Johnson grass (Sorghum halepense)

Pacific mite (Eotetranychus willamettel~

Factor(s)involved Enhancement of tachinid Trichopoda sp. Provision of nectar and pollen for the parasite Lixophaga sphenopheri Destruction of alternate host plants Provision of nectar for the parasite Larra americana Provision of alternate hosts for the parasite Emersonella sp. Increasedactivity of the parasitic wasp Tiphia popilliavera Increaseof alternate hosts for the parasitic wasp Amagrus epos Build-up of predaceous mites (Metaseiulus occidentalis)

Table II. Selected examples of multiple cropping systems that effectively prevent insect-pest outbreaks (based on Altieri et al., 1978; Altieri and Letourneau, 1982; Andow 1991 ). Multiple cropping system Beans grown in relay intercropping with winter wheat Brassica crops and beans Brussels sprouts intercropped with fava beans and/or mustard Cabbage intercropped with white and red clover Intercropping of Cajanus cajan with red, black and green gram Cassava intercropped with cowpeas

Pest(s) regulated

Empoasca fabae and Aphis fabae Brevicoryne brassicae and Delia brassicae

Factor(s) involved Impairment of visual searching behavior of dispersing aphids Higher predation and disruption of oviposition behavior Reduced plant apparency trap cropping, enhanced biological control

Flea beetle Phyllotreta crucifecae and cabbage aphid Brevicoryne brassicae Erioischia brassicae, cabbage aphids, and imported cabbage butterfly (Pieris rapae) Podborers, jassids and membracids

Delayed colonization of herbivores

Whiteflies Aleurotrachelus socialis and Trialeurodes variabilis

Changes in plant vigor and increased abundance of natural enemies

Interference with colonization and increase of ground beetles

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M. A. Altieri

Table II. (continued) Multiple cropping system

Pest(s) regulated

Factor(s) involved

Cauliflower strip-cropped with rape and/or marigold Corn intercropped with beans

Blossom beetle Meligethes

Trap cropping

Leafhoppers (Empoasca kraemen~ leaf beetle (Diabrotica balteata) and fall armyworm

Increase in beneficial insects and interference with colonization

Corn intercropped with fava beans and squash Corn intercropped with clover Corn intercropped with soybean Corn intercropped with sweet potatoes

Aphids, Tetranychus urticae and Macrodactylus sp.

Enhanced abundance of predators ?

European corn borer

Differences in corn varietal resistance Increase in parasitic wasps

Intercropping corn and beans Cotton intercropped with forage cowpea Intercropping cotton with sorghum or maize Cotton intercropped with okra Strip cropping of cotton and alfalfa

Strip cropping of cotton and alfalfa on one side and maize and soybean on the other Intercropping cowpea and sorghum Cucumbers intercropped with maize and broccoli Groundnuts intercropped with field beans Maize intercropped with canavalia Maize-bean intercropping Strip cropping of muskmelons with wheat Oats intercropped with field beans Peaches intercropped with strawberries

aeneus

(Spodoptera frugiperda)

Ostrinia nubilalis

Ostrinia nubilalis Leaf beetles (Diabrotica

spp.) and leafhoppers

(Ag aIlia lingula ) Dalbulus maidis

Boll weevil (Anthonomus

grandis)

Corn earworm (Heliothis

zea) Podagrica sp.

Interference with leafhopper movement Population increase of parasitic wasps (Eurytoma sp.) Increased abundance of predators Trap cropping

Corn earworm (Heliothis zea) and cabbage looper

Prevention of emigration and synchrony in the relationship between pests and natural enemies Increased abundance of predators

Leaf beetle (Oetheca

Interference of air currents

Plant bugs (Lygus hesperus + and L. elisus)

( Trichoplusia n/~

bennigsenl~ Acalymma vittatta Aphis craccivora

Prorachia daria and fall armyworm (Spodoptera frugiperda) Spodoptera frugiperda and Diatraea lineolata Myzus persicae Rophalosiphum padi Strawberry leafroller

(Ancylis comptana) Oriental fruit moth

(Grapholita molesta)

Interference with movement and tenure time on host plants Aphids trapped on epidermal hairs of beans Not reported Lower oviposition rates, trap cropping Interference with aphid dispersal Interference with secondary dispersal after alighting on the crop Population increase of parasites (Macrocentrus

ancylivora, Microbracon gelechise and Lixophaga variabilis)

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201

Table II. (continued) Multiple cropping system Peanut intercropped with maize Sesame intercropped with corn or sorghum Sesame intercropped with cotton Soybean strip cropped with snap beans Squash intercropped with maize

Tomato and tobacco intercropped with cabbage Tomato intercropped with cabbage 9, L

,

,,,,,

,,,'

Pest(s) regulated

Factor(s) involved

Corn borer (Ostrinia furnacalis) Webworms (Antigostra sp.)

Abundance of spiders (L ycosa sp.) Shading by the taller companion crop Increase of beneficial insects and trap cropping Trap cropping

Heliothis spp. Epilachna varivestis

Flea beetles (Phyllotreta cruciferae)

Increased dispersion due to avoidance of host plants shaded by maize and interference with flight movements by maize stalks Feeding inhibition by odors from non-host plants

Diamondback moth (Plutella xylostella)

Chemical repellency or masking

Acalymma thiemei, Diabrotica balteata

'

"

'"'

"

,,

,,,,,

,,

,,

environmental manipulations depends upon their degree of association with one or more of the vegetational components of the system. Extension of the cropping period, or planning temporal or spatial cropping sequences may allow naturally occurring biological control agents to sustain higher population levels on alternate host or prey and to persist in the agricultural environment throughout the year. Since farming systems in a region are managed over a range of energy inputs, levels of crop diversity and successional stages, variations in insect dynamics are likely to occur and may be difficult to predict. However, based on current ecological and agronomic theory, low pest potentials may be expected in agroecosystems that exhibit the following characteristics (Litsinger and Moody, 1976; Huffaker and Messenger, 1976; Perrin, 1977, 1980; Altieri and Letourneau, 1982; Andow, 1991): 1. High crop diversity through mixtures in time and space. 2. Discontinuity of monoculture in time through rotations, use of short maturing varieties, use of crop-free or preferred host-free periods, etc. 3. Small, scattered fields creating a structural mosaic of adjoining crops, and uncultivated land which potentially provides shelter and alternative food for natural enemies. Pests also may proliferate in these environments depending on plant species composition, however, the presence of low levels of pest populations and/or alternate hosts may be necessary to maintain natural enemies in the area. 4. Farms with a dominant perennial crop component. Orchards are considered to be semi-permanent ecosystems, and more stable than annual crop systems. Since orchards suffer less disturbance and are characterized by greater structural diversity, possibilities for the establishment of biological control agents are generally higher, especially if floral undergrowth diversity is encouraged.

202

M. A. Altieri

5. High crop densities or presence of tolerable levels of weed background. 6. High genetic diversity resulting from the use of variety mixtures or multilines of the same crop. These generalizations can serve in the planning of a vegetation management strategy in agroecosystems; however, they must take into account local variations in climate, geography, crops, local vegetation, inputs, pest complexes, etc., which might increase or decrease the potential for pest development under some vegetation management conditions. The selection of component plant species can also be critical. Systematic studies on the 'quality' of plant diversification with respect to the abundance and efficiency of natural enemies are needed. As pointed out by Southwood and Way (1970), what seems to matter is 'functional' diversity and not diversity per se. Mechanistic studies to determine the underlying elements of plant mixtures that disrupt pest invasion and that favor colonization and population growth of natural enemies will allow more precise planning of cropping schemes and increase the chances of a beneficial effect beyond the current levels.

IV. ENHANCING NATURAL ENEMY BIODIVERSITY IN AGROECOSYSTEMS: THE CASE OF PARASITIC HYMENOPTERA There are several environmental factors that influence the diversity, abundance and activity of parasitoids in agroecosystems" microclimatic conditions, availability of food (water, hosts, pollen and nectar), habitat requirements (refuges, nesting and reproduction sites, etc.), intra- and interspecific competition and other organisms (hyperparasites, predators, humans, etc.). The effect of each of these factors will vary according to the spatial and temporary arrangement of crops and the intensity of crop management. Since agroecosystems are dynamic and subjected to different kinds of management, crop mixes continually change in the face of biological and socioeconomic factors. Such landscape variations determine the degree of spatial and temporal heterogeneity characteristic of agroecosystems, which, in turn, may or may not benefit parasitic Hymenoptera diversity in specific cropping systems. Although parasitoids seem to vary widely in their response to crop distribution, density and dispersion, experimental evidence suggests that structural (i.e. spatial and temporal crop arrangement) and management (i.e. crop diversity, input levels, etc.) attributes of agroecosystems influence parasitoid diversity and dynamics. Based on the available information, parasitoid biodiversity can be enhanced and effectiveness improved in the following ways (van den Bosch and Telford, 1964; Wilson, 1966; Rabb etal., 1976; Carroll, 1978; Altieri and Letourneau, 1982; Powell, 1986).

Biod/versity and Biocontrol

203

A. Multiple Introductions of Parasitoids Importation of parasitoids has been used since 1906 as a strategy to reach longterm suppression of pests. The practice of classical biological control could be regarded as a global experiment in restoring natural enemy biodiversity in agroecosystems where exotic insects reach pest status because they have been introduced from a geographic distance without their regulating natural enemies. According to Greathead (1986) there are records of 860 successful establishments of 393 species ofparasitoids against some 274 pest insects in 99 countries. In many of these cases, introduction of some 250 species of hymenopterous parasitoids has been rated as achieving satisfactory pest suppression in either a limited or substantial part of the pest's distribution range. Hymenopterous parasitoids were also aided by introduction of other parasitoid or predator species to achieve a useful reduction in pest numbers (Ehler, 1990). This fact gives support to the multiple-species introduction strategy (MSI) in classical biological control. Longtime practitioners such as Huffaker et al. (1971) have already argued in favor of MSI and have stated that 'importation of a diverse complex of natural enemies is the only practical manner of obtaining the best species for a given habitat, or the best combination for such habitat, or the best combination for the entire host range'. Clearly, enhancing or restoring natural enemy biodiversity through importation assures a better chance of success than single species introduction; the challenge is determining which species or combination of species to introduce in order to control a given target species in a specific situation (Ehler, 1990).

B. Reducing Direct Mortality by Eliminating Pesticides The use of chemical pesticides has often created complex and serious problems by immediate and time-lag effects on natural enemies. Non-selective insecticides have created pest problems by eliminating parasitoids. D D T and parathion have been particularly deleterious to various parasitoids in several agroecosystems. Organophosphorus insecticides such as azinphosmethyl, parathion, diazinon, dimethoate and malathion are particularly toxic to hymenopterous parasites of citrus scales and mealybugs. Total removal of pesticides can restore parasitoid diversity and lead to renewed biological control of specific pests. Within 2 years, virtually all banana insect pests in Golfito, Costa Rica dropped to below economic threshold levels, due to enhanced parasitization and predation, after stopping insecticide (dieldrin and carbaryl) sprays (Stephens, 1984). Similarly, in California's walnut orchards, natural biological control of the frosted scale and the calico scale was soon achieved by encyrtid parasitoids after removal of D D T sprays (Hagen et al., 1971).

204

M. A. Altieri

C. Provision of Supplementary Resources Most parasitoids have resource requirements such as hosts, food other than hosts, water, refuges, etc., which often are not available or found in sufficiency within a given cropping system. Several researchers have demonstrated that manipulating such resources can enhance parasitoid diversity and abundance and also improve their efficacy (Rabb ttal., 1976). Addition of host populations proved effective in controlling Pieris rapae in cabbage. The continuous release of fertile P/ms eggs increased the pest population nearly ten-fold above normal spring populations, enabling the parasites Trichogramma evanescens Westwood and Cotesia rubecula (Marshall) to increase early and maintain themselves at an effective level throughout the season (Parker and Pinnell, 1972).

D. Increasing Adjacent Vegetational Diversity Researchers are well aware of the importance of adjacent vegetational settings in determining the diversity of parasitoid species as well as their maintenance and effectiveness within agroecosystems (van den Bosch and Telford, 1964; Alteri and Todd, 1981; Altieri and Letourneau, 1982, 1984). Successful colonization by parasites depends upon the presence of the appropriate kind and abundance of primary hosts, alternative hosts, pollen and/or nectar in hedgerows and other neighboring habitats. For example, in Armenia, scelionid egg parasites of the sun pest Eu~ygaster integriceps Puton are very efficient in areas with small wheat fields surrounded by diverse vegetation. Under these conditions, the polyvoltine egg parasites have a number of other pentatomid hosts and favorable hibernating places. In California, Doutt and Nakata (1973) found that the egg parasite Anagrus epos Girault, was effective in controlling the grape leafhopper E(ythroneura elegantula Osborn, in vineyards adjacent to wild blackberries which harbor a non-economic leafhopper, Dikrella cruentata Gillette, whose eggs serve as the only overwintering resources for Anagrus. Also in California, Allen and Smith (1958) found that parasitization of the alfalfa caterpillar, Colias eutytheme, by Apanteles medicaginis was far greater in California's San Joaquin Valley where weeds were in bloom along irrigation canals in contrast to areas where the weeds were destroyed. In England, the proximity of certain flowering weeds increased the activity of parasitic Hymenoptera in wheat and cabbage fields (van Emden and Williams, 1974).

E. Increasing Within-field Plant Diversity Considerable plants within increase their showed that

work in the USSR has been devoted to the use of nectar-bearing orchards as a source of adult food for entomophagous insects to effectiveness. Field experiments conducted in the North Caucasus the growing of Phacdia spp. in orchards greatly increased the

Biodiversity and Biocontrol

205

parasitization of Quadraspidiotus perniciosus (Comstock) by its parasite Aphytis proclia (Walker). These same plants have been shown to increase the abundance of the wasp Aphelinus mali for the control of apple aphids and improve the activity of Trichogramma spp. in apple orchards (Chumakova, 1977).

F. Manipulating Host-plant Attributes Several chemical, genetic and architectural attributes of plants can influence parasitoid action on insect pests. Rabb and Bradley (1968) found that parasitization of Manduca sexta (L.) eggs by Trichogramma minutum Riley and Telenomus sphingis (Ashmead) was inhibited by sticky exudates of tobacco leaves. Encarsia formosa Gahan, a normally effective parasitoid of the greenhouse whitefly, is greatly hindered by the hairs produced by cucumber (Price et al., 1980). It is also known that the nature of the host-plant habitat affects the degree of parasitization obtained from certain parasitoids. In northern Florida, parasitization rates of Heliothis spp. and plusiinae eggs by Trichogramma pretiosum Riley showed considerable variation in various crops grown in the same field (Martin et al., 1976). Moderate to high rates of parasitization were attained in tomatoes, collards and okra. The released parasites were ineffective against the target pests in tobacco. Although these differences could have been due to differences in host egg densities, various chemical and physical cues emitted by the different crops were significant in affecting the location of the host habitat by Trichogramma wasps. Similar results were obtained in New York state where parasitism by DiaeretieUa rapae was much higher when the aphid Myzus persicae (Sulzer) was on collard than when it was on beet (Read etal., 1970).

G. Manipulations with Semiochemicals Chemicals that stimulate host-searching behavior in parasitoids have been identified for a number of Hymenoptera species: Cardiochiles niciriceps, Trichogramma evanescens, T. pretiosum, Trissolcus sp., Telenomus sp., Microplitis croceips and Aphidius nigripes (Nordlund et al., 1981). Hexane extracts sprayed in field trials have consistently improved parasitization rates of H. zea eggs by T. pretiosum. The greatest utility of such kairomonal applications appears to be for aggregating or retaining released parasites in target locations (Lewis and Nordlund, 1985). Taking advantage of the fact that many parasitoids seek out particular habitats and are guided by volatiles emanating from plants, some researchers have applied certain plant extracts on crop plants to reinforce the host location behavior of parasitoids and have improved parasitization rates (Altieri et al., 1981). Spraying of plant-produced synomones attracted ovipositioning female parasitoids, enhancing the parasitization of H. zea and Anagasta kuehnieUa (Zeller) by Trichogramma wasps under soyabean field and greenhouse conditions respectively

206

M. A. Altieri

(Altieri et al., 1981; Altieri and Letourneau, 1982). Similar results were obtained by Titayavan and Altieri (1990) in broccoli plots. Direct application of an allylisothiocyanate emulsion at a rate of 0.25 ml per broccoli plant consistently gave higher parasitization rates of the cabbage aphid and/or number ofDiaeretiella rapae wasps per plant, than those observed on plants treated with 0.25 ml of water or with 0.25 ml of wild mustard extract. V. CONCLUSIONS Agroecosystems are complex and dynamic systems subjected to a whole range of vegetational designs and management intensities depending on farmers' preferences, environmental factors and socioeconomic constraints. Changes in plant diversity, plant density, crop dispersion and patch size will increase or reduce resources for natural enemies. Therefore, the size and structure of natural enemy communities should be expected to vary according to the biodiversity and heterogeneity of specific agroecosystems. When considering ways of enhancing natural enemy diversity and efficiency, what is difficult is that each agricultural situation must be assessed separately. Diversified vegetational settings will generally result in enhanced diversity and abundance of predators and parasitoids, although specifically which species will be enhanced will vary depending on the diversity and availability of primary and alternative host preys, location and size of the field, plant composition, floral diversity and phenology, surrounding environments and management technologies. One can only hope to elucidate the basic ecology of natural enemies, their relationships with other components of the agroecosystem and the ecological principles governing natural enemy biodiversity in crop fields. In this regard, manipulating agroecosystem components (habitat diversity, pesticide-free space, alternate food, semiochemicals, etc.) to provide the basic requirements needed by parasitoids and predators (hosts and prey, pollen and nectar, refuges, reproduction and nesting sites, etc.) is an effective way to apply ecological theory to improve biological control in agroecosystems. REFERENCES Allen, W. W. and Smith, R. F. (1958). Some factors influencing the efficiency of Apanteles medicaginis Muesebeck (Hymenoptera: Braconidae) as a parasite of the alfalfa caterpillar Colias eu~ytheme Boisduval. Hilgardia 28, 1-42. Altieri, M.A. (1987). 'Agroecology: the Scientific Basis of Alternative Agriculture. Westview Press, Boulder, CO. Altieri, M.A. and Letourneau, D. K. (1982). Vegetation management and biological control in agroecosystems. Crop Protection 1,405-1430. Altieri, M.A. and Letourneau, D.K. (1984). Vegetation diversity and insect pest outbreaks. CRC Critical Reviews in Plant Sciences 2, 131-169.

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Altieri, M. A. and Schmidt, L. L. (1985). Cover crop manipulation in northern California orchards and vineyards: effects on arthropod communities. Biological Agriculture and

Horticulturer 3, 1- 24. Altieri, M. A. and Todd, J. W. (1981). Some influences of vegetational diversity on insect communities of Georgia soybean fields. Protection Ecology 3,333-338. Altieri, M.A. and Whitcomb, W. H. (1979). The potential use of weeds in the manipulation of beneficial insects. Hortscience 14, 12-18. Altieri, M. A., van Schoonhoven, A. and Doll J. D. (1977). The ecological role of weeds in insect pest management systems: A review illustrated with bean (Phaseolus vulgaris L.) cropping systems. PANS 23, 195-205. Altieri, M. A., Francis, C. A., van Schoonhoven, A. and Doll, J. (1978). A review of insect prevalence in maize (Zea mays L.) and bean (Phaseolus vulgaris L.) polycultural systems. Field Crops Research 1, 33-49. Altieri, M. A., Lewis, W.J., Nordlund, D. A., Gueldner, R. C. and Todd, J. W. (1981). Chemical interactions between plants and Trichogramma wasps in Georgia soybean fields. Protection Ecology 3, 259-263. Andow, D. A. (1991). Vegetational diversity and arthropod population response. Annual Review of Entomology 36, 561-586. Andow, D. A. and Prokrym, D. R. (1990). Plant structural complexity and host finding by a parasitoid. Oecologia 62, 162-165. Andow, D. and Risch, S.J. (1985). Predation in diversified agroecosystems: relations between a coccinellid predator Coleomegilla maculata and its food. Journal of Applied Ecology 22, 357-372. Beingolea, O. (1957) 'El Sembrio del Maiz y la Fauna Benefica del Algodonero'. Estacion Experimental Agricola, La Molina, Lima. Carroll, C. R. (1978). Beetles, parasitoids and tropical morning glories: a study in host discrimination. Ecological Entomology 3, 79-85. Chumakova, B. M. (1977). Ecological principles associated with augmentation of natural enemies. In 'Biological Control by Augmentation of Natural Enemies' (R. L. Ridgway and S. B. Vinson, eds), pp. 39-78. Plenum, NY. Doutt, R. L. and Nakata,J. (1973). The Rubus leaflaopper and its egg parasitoid: an endemic biotic system useful in grape-pest management. Environmental Entomology 2, 381-386. Ehler, L. E. (1990). Introduction strategies in biological control of insects. In 'Critical Issues in Biological Control' (M. Mackauer, L.E. Ehler and J. Roland, eds), pp. 111-134. Intercept, Andover, UK. Flint, M. L. and Roberts, P. A. (1988). Using crop diversity to manage pest problems: some California examples. American Journal of Alternative Agriculture 3, 164-167. Greathead, D.J. (1986). Parasitoids in classical biological control. In 'Insect Parasitoids' (J. Waage and D. Greathead, eds), pp. 290-318. Academic Press, London. Hagen, K.S., van den Bosch, R., and Dahlsten, D.L. (1971). The importance of naturally-occurring biological control in the Western United States. In 'Biological Control' (C. B. Huffaker, ed.), pp. 253-287. Plenum, NY. Helenius, J. (1989). The influence of mixed intercropping of oats with field beans and on the abundance of and spatial distribution of cereal aphids (Homoptera: Aphididae). Agricultural Ecosystems and the Environment 25, 53-73. Huffaker, C. B. and Messenger, P. S. (eds). (1976). 'Theory and Practice of Biological Control'. Academic Press, New York. Huffaker, C. B., Messenger, P. S. and DeBach, P. (1971). The natural enemy component in natural enemy control and the theory of biological control. In 'Biological Control' (C. B. Huffaker, ed.), pp. 16-67. Plenum, NY. Leius, K. (1967). Influence of wild flowers on parasitism of tent caterpillar and codling moth. Canadian Entomologist 99, 444-446.

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Letourneau, D. K. (1987). The enemies hypothesis: tritrophic interaction and vegetational diversity in tropical agroecosystems. Ecolog? 68, 1616-1622. Litsinger, J. A. and Moody, K. (1976). Integrated pest management in multiple cropping systems. In 'Multiple Cropping Systems' (P. A. Sanchez, ed.), pp. 293-316. ASA Publication 27. Madison, Wisconsin. Lewis, W.J. and Nordlund, D.A. (1985). Behavior-modifying chemicals to enhance natural enemy effectiveness. In 'Biological Control in Agricultural Integrated Pest Management Systems' (M. A. Hoy and D. C. Herzog, eds), pp. 89-101. Academic Press, NY. Martin, P. B., Lingren, P. D., Greene, G. L. and Ridgway, R. L. (1976). Parasitization of two species of Plusiinae and Heliothis spp. after releases of Trichogramma pretiosum in seven crops. Environmental Entomology 5, 991-995. Nordlund, D. A., Lewis, W.J. and Gross, H. R. (1981). Elucidation and employment of semiochemicals in the manipulation of entomophagous insects. In 'Management of Insect Pests with Semiochemicals Concepts and Practice' (E. R. Mitchell, ed.), pp. 463-475. Plenum, NY. Parker, F.D. and Pinnell, R.E. (1972). Further studies of the biological control of Pieris rapae using supplemental host and parasite releases. Environmental Entomology 1, 150-157. Perrin, R. M. (1977). Pest management in multiple cropping systems. Agro-Ecosystems 3, 93-118. Perrin, R. M. (1980). The role of environmental diversity in crop protection. Protection Ecology 2, 77-114. Powell, W. (1986). Enhancing parasitoid activity in crops. In 'Insect Parasitoids' (J. Waage and D. Greathead, eds), pp. 319-335. Academic Press, London. Price, P. W., Bouton, C. E., Gross, P., McPheron, B. A., Thompson, J. N. and Weis, A.E. (1980). Interactions among three trophic levels. Annual Review of Ecology and Systematics 11, 41-65. Rabb, R. L. and Bradley, J. R. Jr. (1968). The influence of host plants on parsitism of eggs of the tobacco hornworrn. Journal of Economic Entomology 61, 1249-1252. Rabb, R. L., Stinner, R. E. and van den Bosch, R. (1976). Conservation and augmentation of natural enemies. In 'Theory and Practice of Biological Control' (C. B. Huffaker and P. Messenger, eds), pp. 233-254. Academic Press, New York. Read, D. P., Feeny, P. P. and Root, R. B. (1970). Habitat selection by the aphid parasite Diaretiella rapae (Hymnenoptera: Braconidae) and hyperparasite Charips brassica (Hymenoptera: Cynipidae). Canadian Entomologist 102, 1567-1578. Risch, S. J. (1981). Insect herbivore abundance in tropical monocultures and polycultures. An experimental test of two hypotheses. Ecology 62, 1325-1340. Root, R. B. (1973). Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecological Monographs 43, 95-124. Russell, E. P. (1989). Enemies hypothesis: a review of the effect of vegetational diversity on predatory insects and parasitoids. Environmental Entomology 18, 590-599. Sheehan, W. (1985). Response by specialist and generalist natural enemies to agroecosystem diversification: a selective review. Environmental Entomology 15,456-461. Southwood, T. R. E., and Way, M . J . (1970). Ecological background to pest management. In 'Concepts of Pest management' (R. L. Rabb and F.E. Guthrie, eds), pp. 6-29. North Carolina State University, Raleigh, NC. Stephens, C. S. (1934). Ecological upset and recuperation of natural control of insect pests in some Costa R ican banana plantations. Turrialba 34, 101-105. Titayavan, M. and Altieri, M. A. (1990). Synomone-mediated interactions between the parasitoid Diaeretiella rapae and Brevicoryne brassicaunder field conditions. Entomophaga 35, 499-507.

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Tumbull, A. L. (1969). The ecological role of pest populations. Proceedings of the Tall Timbers Conference on Ecological Animal Control by Habitat Management 1, 219-232. van den Bosch, R. and Telford, A. D. (1964). Environmental modification and biological control. In 'Biological Control of Insect Pests and Weeds' (P. DeBach, ed.), pp. 459-488. Chapman & Hall, London. van Emden, H. F. (1965). The role of uncultivated land in the biology of crop pests and beneficial insects. Scientific Horticulture 17, 121-136. van Emden H. F. and Williams, G . F . (1974). Insect stability and diversity in agroecosystems. Annual Review of Entomolog7 19, 455-475. Wainhouse, D. and Coaker, T. H. (1981). The distribution of carrot fly (Psila rosae) in relation to the fauna of field boundaries. In 'Pests, Pathogens and Vegetation: The Role of Weeds and Wild Plants in the Ecology of Crop Pests and Diseases' (J. H. Thresh, ed.), pp. 263-272. Pitman, MA. Wilson, F. (1966). The conservation and augmentation of natural enemies. Proceedings of the Food and Agriculture Organization Symposium on Integrated Pest Control 3, 21-26. Young, W. R. and Teetes, G. L. (1977). Sorghum entomology. Annual Review of Entomology 72, 193-218.

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11 PLANT PROTECTION USING NATURAL DEFENCE SYSTEMS OF PLANTS B.J. Deverall Department of Crop Sciences, University of Sydney, N S W 2006, Australia

I. Introduction II. Evidence from Laboratory TriMs A. Using Pathogens as Inducers B. Using Chemicals as Inducers III. Evidence from Field TriMs IV. Prospects for Sustainable Use Acknowledgements References

211 212 212 216 220 221 225 225

I. I N T R O D U C T I O N The idea of inducing plants to use their natural defence systems at threatening times for disease development is attractive. It suggests the prospect of alternatives or supplements to present methods of plant protection in forestry, agriculture and horticulture. These present methods are largely the planting of resistant cultivars or the application of control agents. Resistant cultivars are produced by plant breeding after selection of recognitional genes for countering harmful strains of pathogens. Control agents are mainly fungicides developed in the chemical industry. Concerns about depleting genetic resources, evolution of new strains of pathogens and use of fungicides encourage exploration for other methods. There is a worldwide mission to use 'integrated pest and disease management' in plant protection. This means the selection and use of as many procedures as possible for minimizing loss caused by pests and diseases in a balanced way. A desirable component of such management would be manipulation of the active defence systems in plants. This review is about current ability and prospects in activating defence systems in plants with effective control of disease in mind. It focuses mainly on the induction of systemic resistance in plants. This means the heightening of resistance throughout a plant after an earlier localized inoculation with a pathogen or attenuated pathogen, or after treatment of the plant with a chemical agent that is not itself a fungicide, bactericide or viricide. Resistance can be ADVANCES IN PLANT PATHOLOGY--VOL. 11 Copyright 9 1995 Academic Press Limited ISBN 0-12-033711-8 All rights of reproduaion in any form reserved

212

B. J. Deverall

induced close to the point of the earlier treatment or throughout a plant (i.e. systemically) (Sequeira, 1983). Systemic induced resistance seems more likely to be useful in plant protection and is therefore my preferred major theme. Many potential defence systems can be activated in plants by inoculation and infection. These systems include the formation of structures such as cell wall depositions (e.g. silicon, callose, lignin and suberin) and new cellular structures (e.g. tyloses) and layers (e.g. periderm) (Aist, 1983), the synthesis of antimicrobial substances (e.g. phytoalexins) (Barley and Mansfield, 1982) and the production of pathogenesis-related proteins amongst which are glucanases and chitinases active on fungal cell walls (Linthorst, 1991). Systemic induced resistance may involve the particularly rapid reactivation of some or all of these systems in response to a second or challenge inoculation. It also involves the production and movement of signals from the site of the first or inducing inoculation. These signals either activate one or several of the defence systems directly or, in a largely unknown way, render remote cells sensitive to challenge so that they respond more rapidly than normal in producing defences to the challenge (Hammerschmidt and Ku~, 1995). This review does not deal in depth with the processes of induced resistance, but rather with the extent and strength of evidence for contributions of the processes to plant protection. Many earlier reviews describe the history and extent of development of knowledge of systemic induced resistance up to their respective dates (Chester, 1933; Goodman, 1978; Matta, 1980; Suzuki, 1980; Ku~., 1983, 1990; Sequeira, 1983). A comprehensive book on induced resistance to disease in plants is about to be published (Hammerschmidt and Ku~, 1995). This present review starts with evidence for effective disease control in laboratory and glasshouse/ growth room experiments, firstly using pathogens or other micro-organisms and secondly using chemical agents as inducers. It then deals with extents and duration of control in field trials that are directed towards commercial practice. Based on this evidence, prospects for application are evaluated.

II. EVIDENCE FROM LABORATORY TRIALS A. Using Pathogens as Inducers Substantial increases in resistance were brought about in a range of economically important plants (from legumes to grasses) by earlier inoculations with particular viruses, bacteria and fungi (Table II). The resistance was appreciable but never complete in these growth room and glasshouse tests. The persistence of the induced resistance was usually confirmed for periods up to 7 days, but in some cases for much longer. The resistance was usually manifest as a decrease in numbers of sites of infection in challenged plant parts and in a decrease in disease development at each of these sites. Most tests were done on leaves that emerged immediately above a first-inoculated leaf, but some were done with root systems

Plant Protection Using Natural Defence Systems

213

revealing induction of resistance towards vascular wilt diseases caused by forms of Fusarium oxysporurn. Resisted foliar pathogens were of many types ranging from some viruses, lower fungi, including the potato blight pathogen and a downy mildew fungus, to representatives of the higher fungi such as powdery mildew and rust fungi. The results suggest that useful resistance should be capable of being brought about in many types of plants against many pathogens by these means. Effective inducing organisms tested were mainly plant pathogens, often those that caused local lesions. Most of the earlier work (Ross, 1961; Ku6, 1983) suggested that cellular incompatibility between inducer and host was a key factor in leading first to cellular disruption and then local lesion formation. As a consequence, systemic signals were thought to be released from the disrupted cells to the rest of the plant. The recent evidence in Table I that a rust fungus in broad bean and an endophytic fungus in tomato induced systemic resistance questions the idea that limited disruption of host cells is always an essential first step. From general understanding of their infection processes, both of these fungi would be expected to develop compatibly with the plant cells and not to cause local damage, at least until a much later stage in development. If close examination of the infections by the rust fungus and the endophyte confirms cellular compatibility with host cells during the inducing phase, then some new vistas of the activating steps in biologically induced resistance will be opened. The work with the endophyte also indicates prospects of choosing micro-organisms that are not pathogens for the special purpose of systemically bringing about induced resistance. Particularly interesting work on induction by a micro-organism is that of Smith et al. (1991) who found a highly effective strain of the bacterium Pseudomonas syringae pv. syringae that induced resistance in the next leaves of cucumber within the unusually short time of 1 day. By removing the first leaves at increasingly brief intervals after inoculation with the strain, it was deduced that a signal passed to the next leaves 6 h after inoculation. The signal was sent before the inducing bacterium caused cell death and hypersensitivity in the first leaf. A mutant of the bacterium that did not cause hypersensitivity failed to induce systemic resistance. Transformation of the mutant with a cosmid bearing a genetic sequence from the original strain restored the capacity to cause both hypersensitivity and systemic induced resistance. This work emphasizes the usual understanding that the inducing organism needs to have potential to cause limited cell death in the plant. It also indicates prospects for selecting micro-organisms with high ability for inducing resistance. Further work on inducing systemic resistance with a strain of P. syringae pv. syringae, but in this case in rice (Smith and M6traux, 1991), needs special emphasis for the way in which the resistance is brought about. No widespread enhancement of enzyme activities, including glucanases and chitinases, could be detected, in contrast to the prechallenge situation where resistance was induced systemically in tobacco (Pan et al., 1991) and some other plants. The rice work

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Peronospora tabacina

Stem

TMV

Leaves 1 t o 3 Leaves 2 t o 6

Tomato

Endophyte Acrernoniurn kiliense

Ph ytophthora infestans

Fusariurn oxysporurn f .sp. dianthi

Transplant into inoculated peat soil

First t w o leaves

Peronospora tabacina

Leaves 5-10

TMV and some other viruses Phytophthora parasitica var . nicotianae

Leaves 4 and 5

Fusariurn ox ysporurn f .sp. lycopersici Clavibacter rnichiganense Phytophthora infestans

Fusariurn oxysporurn f .sp. cucurnerinurn Fusariurn ox ysporurn f .sp. niveurn (avir.)

Pan etal.

High

To 21 days

Ross (1961)

Leaves 8 and 9

25-fold

25 days

Transplant t o infested soil Poured into soil

7-fold

7 days

c 50%

3 days t o

Mclntyre and Dodds ( 1 979) Mclntyre and Dodds ( 1 979) Bargmann and Schonbeck

20%

Leaves 3-6

Number down from 90 t o 68 Dry lesions down from 78 t o 15 80% decrease in necrosis

Fourth leaf

One half of split Fusariurn root system oxysporurn immersed for f .sp. lycopersici 10 min in l o 7 conidia m l -

Other half of Delay in root system symptom immersed for development 10 min in 1 o6 and less conidia ml-' disease 1 week later Leaves 2 and 3 c 50%

Roots dipped

Colletotrichurn lagenariurn Fusariurn oxysporurn f .sp. niveurn (vir.)

weeks

Root dipped

40-81 % less wilt

(1991)

( 1 992)

7 days t o

Bargmann and Schonbeck

10 days

Heller and Gessler

weeks

First three leaves

'

Watermelon

At least 21 days

Leaf area with lesions down from 90 t o

(1992) ( 1 986)

7 days tested

Christ and Mosinger

To 24 days after challenge

Kroon et al.

5 days

Biles and Martyn

40 days

Biles and Martyn

( 1 989)

(1991)

( 1 989) ( 1 989)

216

B. J. Deverall

leaves open the possibility that induced resistance can result from a heightened sensitivity to challenge as distinct from, or in addition to, an increased activity of defensive enzymes before challenge.

B. Using Chemicals as Inducers Substantial resistance to some fungal and bacterial pathogens in a few crop species representative of a potentially wide range has been brought about by application of chemical agents (Table II). The earliest of these successes in laboratory and growth room/glasshouse situations were with dichlorocyclopropane (Langcake and Wickens, 1975) and probenazole (Watanabe etal., 1977, 1979) against the blast disease in rice. Later came the report that carboxyalkenyl hydrazinium salts appeared to act systemically in preventing vascular wilt symptoms in tomato (Phillips et al., 1981). The activity of these compounds had become apparent in screening for potential systemic fungicides, coupled with the realization that they were more effective in controlling the disease than in affecting the germination and growth of the fungal pathogen in vitro. As described for many un-named chemical agents tested on rice and wheat in the ICI company (Rathmell, 1984), it is likely that numerous compounds were synthesized and found effective in the chemical industry for countering diseases in growth room and glasshouse trials, and that they may not have been antimicrobial in direct tests on pathogens in the laboratory. In a significant number of these cases, the chemical agents were damaging to plant tissues and Rathmell (1984) speculated that the damage may have been related to their disease-control ability, perhaps through inducing resistance. Partly because of this observed damage (phytotoxicity), but also for reasons of cost and other strategic considerations, companies have been slow in developing and releasing chemical agents of this type as plant protectants (Baldwin and Rathmell, 1988). Until recently there has been little outward sign of the plant protection industry attempting to use chemical agents for bringing about resistance. Omitted from Table II and of questionable relevance to the main theme of this review are the phosphonates, which have been classified as systemic fungicides with good activity against diseases caused by downy mildew fungi and Phytophthora spp. (Cohen and Coffey, 1986). There is evidence that these fungicides affect the fungi directly acting through the conversion product, phosphorous acid. There is also evidence, as discussed by Nemestothy and Guest (1990), that the defence mechanisms of infected plants are enhanced in the presence of these fungicides. Some controversy continues about the direct versus indirect mode of action of the phosphonates in controlling diseases, but it seems to be unlikely that they are working directly on host defence and that they are inducers of resistance in the sense used in this review. Apart from these past products of the chemical industry, interest in researching chemical agents as inducers of systemic resistance has resumed in three ways in recent years.

Plant Protection Using Natural Defence Systems

217

One is through the use of pathogen products that act as, or are related to, elicitors of defence in pathogen-host interactions. This comes the evidence (Table II) that resistance can be induced systemically to Phytophthora infestans in potato by hyphal wall fragments and unsaturated fatty acids. Proteinaceous elicitors of necrosis from several Phytophthora spp. induced resistance, at least locally, to the black shank disease of tobacco (Ricci etal., 1992). There is abundant evidence that many agents including a range of macromolecular products of pathogens will elicit defensive systems in plants, the elicitation of phytoalexin synthesis having been studied most frequently (Darvill and Albersheim, 1984; Ebel, 1986). Glucan elicitors have received most attention because of their high activity and there has been research and development in the plant protection industry inspired by the idea that glucans or a modification of them could be used to activate host defence. Highly active oligomers of both glucans and galacturonic acids have been synthesized as elicitors of phytoalexin synthesis (e.g. Hong and Ogawa, 1990; Nakahara and Ogawa, 1990). It is reasonable to expect that systemically mobile forms of such elicitors can be made and developed. No reports of their successful use in inducing resistance systemically have been found for inclusion in Table II. In most pathogen-plant interactions, phytoalexin formation is known only as a localized event and neither the natural elicitors nor the elicited phytoalexins have been shown to move from the site of the interactions. Some difficulty might be experienced in using these processes for plant protection, unless the active agents also affect systemic mechanisms as may be the case for the successful examples cited above for potato and tobacco plants. A second way is through the investigation of components of plants believed to be beneficial in controlling disease. For example, natural extracts of some plants, such as oxalate, have also been shown to cause systemic resistance in cucumber (Table II). A third way is through investigating the activity of chemical agents (Table II) that are not likely to be products of pathogens or plants. This has brought evidence that tripotassium phosphate will induce systemic resistance in broad bean and cucumber, as will EDTA in broad bean. A more deliberate examination of compounds produced in the chemical industry for capacity to induce resistance has led, for example, to interesting work with dichloro-isonicotinic acid, formulated for experimentation by Ciba-Geigy as CGA 41396. Following demonstrations of its effectiveness against some fungal pathogens in cucumber and tobacco (Ahl Goy etal., 1990; M6traux etal., 1990), further work showed CGA 41396 to induce resistance also to a bacterial pathogen in cucumber and to fungal and bacterial pathogens in beans (Table II). M6traux et al. (1991) also showed that dichloro-isonicotinic acid moved very rapidly from the point of application on the first leaf of cucumber to the young leaves, growing point and roots. It increased the activities of chitinase and glucanase in both the first leaf and the younger leaves of cucumber before they were challengeinoculated. At the present state of understanding, dichloro-isonicotinic acid

Table /I. Systemic resistance induced by chemical compounds in laboratory trials. Induction Plant species

Agent

Challenge Site

Beans Dichloroisonicotinic acid

First leaf

Broad bean

K3 PO4 or EDTA

Leaves 1 and 2

Cucumber

K3 Po4 Phosphates

Leaves

Oxalate

Leaves 1 and 2

Dichloroisonicotinic acid or its ester

Foliar spray

Dichloroisonicotinic acid or its ester

Organism

Pseudomonas phaseolicola Uromyces viciae-fabae lagenarium

Colletotrichum lagenarium Colletotrichum lagenarium

Soil drench

Soil drench

Site

Extent

Pseudomonas lachrymans

Duration

Reference cited

17 days tested

Colletotrichum lindemuthianum Second leaf Uromyces appendiculatus

I and 2 Colletotrichum

Foliar spray

Protection

12 days tested

Dann (1991) Deverall and Dann (1 995)

> 75%

7 days tested

Leaves 3 and 4

c 25% to > 50%

12 days

Walters and Murray

Leaves 3 and 4

c. 80%

7 days

New leaves above leaf 4 Leaves 3 and 4

85-90%

5 weeks

Gottstein and KuC (1 989)

30-85%

7 days

2 days later at leaf 2 stage

90% at 20 ppm

2 days later at leaf 2 stage 2 days later at leaf 2 stage

90% at 2 ppm

MBtraux et a/.

70% at 20 ppm

MBtraux et al.

2 days later at leaf 2 stage

?

(1992)

Doubrava et a/.

(1 988)

MBtraux et al.

(1 991)

(1991)

(1991)

MBtraux et al.

(1991)

Potato

Rice

Tomato

Wheat

Hyphal wall fragments Unsaturated fatty acids

Leaves 1-3

Dichlorocyclopropane

Soil drench

Probenazole

Soil treatment or drench Root drench

Pyricularia oryzae

Dispersal in sand layer above soil

Fusariurn Root dip ox ysporurn f .sp. lycopersici Soil inoculation

Prevention of vascular symptoms

Puccinia recondita

Variable

Diverse chemical compounds Carboxyalkenyl hydrazinium salts Diverse chemical compounds

Root drench

Phytophthora infestans

Leaves 4- 1 1

Wound inoculation of leaf 4 Leaves

84%

2 0 days

Up t o 100%

5 days, decreased at 12 days t o 18 days from drench

75% decrease in lesion elongation ? Variable

Leaves

Doke eta/. (1987) Cohen et a/. (1991 ) Langcake and Wickens (1975) Watanabe et a/. (1977, 1979) Rathmell ( 1984)

1 4 days

Phillips et a/. (1981)

2 4 days

Phillips et a/. (1981) Rathmell ( 1984)

220

B. J. Deverall

may be regarded as an artificial signal molecule moving rapidly from sites of application and contributing to systemic resistance by heightening the activities of defensive enzymes before challenge. It may be mimicking the action of natural signals, one of which may be salicylic acid, at least in tobacco, where it moves from sites of biological induction (Malamy et al., 1990) enhancing glucanase and chitinase activities in more distant parts of the plant (Yalpani etal., 1991). Chemical induction of resistance can be achieved, therefore, and is at a most promising stage in development for its application in plant protection.

III. EVIDENCE FROM FIELD TRIALS In his comprehensive review of theory and practice to that date, Sequeira (1983) observed that induced resistance was being used only minimally for the control of plant diseases. He referred to the use of lowly virulent strains of T M V to protect tomatoes against virulent strains of the virus in Japan and the Netherlands. He also cited the accidental but effective protection of potatoes against virulent strains of potato virus X as a result of continuous roguing that selected the bestlooking seed potatoes; these seed potatoes would have been infected naturally with mild strains of the virus. He also described the results of a very few field and commercial glasshouse trials on the use of induced resistance against fungal and bacterial diseases. Following the continued success in protecting plants against pathogens using pathogens, other micro-organisms and some chemicals under laboratory conditions (Tables I and II), the results of a limited number of trials in at least semi-commercial situations have been published (see Table III). The relatively early work on tobacco and bean showed significant protection in field trials for several weeks after the stems and first leaves respectively had been inoculated with pathogens. The recent reports on cucumber, grapevines, rice and watermelon describe work that is being targeted to commercial practice. Under the conditions of commercial growing of cucumbers in glasshouses, substantial protection against CoUetotrichum lagenarium was induced by the same pathogen and found to be effective for at least a week, but no protection was provided against the important powdery mildew pathogen (Descalzo etal., 1990). This last result is disappointing because management of the powdery mildew fungus is necessary under glasshouse conditions. Other induction techniques described in the report also failed to induce resistance against the powdery mildew fungus, leaving only the success against CoUetotrichum. Success in minimizing loss of watermelons to vascular wilt disease was achieved by sole reliance on application of an avirulent form of Fusarium oxysporum to root systems before planting them in soil infested with a virulent form of the pathogen (Martyn et al., 1991). Marketable fruit were produced in contrast to the situation where no application was made. Two important diseases of rice, fungal blast and bacterial blight, were con-

Plant Protection Using Natural Defence Systems

221

trolled by application of dichloro-isonicotinic acid or its ester to field water (M~traux et al., 1991). The success of this chemical inducer of resistance is most encouraging because it was demonstrated in comparison with the effects of normally used fungicides and bactericides. Success was also reported for foliar applications of the acid in the field control of important bacterial diseases of pear and pepper and fungal blue mould of tobacco. More detail of these field trials would be welcome and will doubtless become available if the chemical inducer is brought forward for registration for use in plant protection. Commercial vineyards were the sites for trials of induced resistance towards natural infestations of the Pacific spider mite (Karban and English-Loeb, 1990). Major decreases in population build-up of this damaging mite were brought about by limited feeding damage late in the previous season caused by deliberate introductions of the much less damaging Willamette spider mite. These trials followed earlier work by Karban and colleagues showing that feeding damage by mites can induce systemic resistance in grapevines and cotton. This type of work is most encouraging for development of integrated pest and disease management. The skilled manipulation of biological components of orchards, plantations and crops in order to decrease pest and disease problems is a clear goal.

IV. PROSPECTS FOR SUSTAINABLE USE Biological means of activating defence are abundant at the laboratory level and a wide selection of them are effective in labour-intensive and short-term field trials. The extents to which they will be used in sustainable systems depends upon the pressures against current methods and the costs and practicability of the alternatives. Major changes in outlooks and procedures would have to be forced by these pressures before the use of local lesion-causing pathogens could be considered as control procedures for diseases of aerial parts of plants. The use of avirulent strains of pathogens in protection is a more immediate prospect for highly managed situations such as intensive growing where soilborne pathogens require control and in glasshouse crops. Avirulent or mildly damaging strains of pathogens or pests may be considered for use in other highly managed places such as orchards and small plantations, including vineyards. Major advances in research and development are needed before organisms such as endophytes, root symbionts and biological additives to seeds are used for the specialized purpose of plant protection via the induction of defence mechanisms. The use of biological agents would require skilled direction and labour, constant monitoring and other activities that seem to be implicit for the adoption of integrated pest and disease management. Chemical means of inducing resistance throughout plants are available and some of them offer immediate prospects of use in plant protection. Subject to the lack of undesirable side effects on plants and the environment and to costs,

Table Ill. Systemic induced resistance tested in field trials. Induction Plant species

Agent

Challenge Application

Agent

Application

Bean

Colletotrichum lindemuthianum

Leaf 1 dipped in conidial suspension

Colletotrichum lindemuthianum

Plants sprayed to run-off 12 days later

Cucumber

Colletotrichum lagenarium

Droplets to surface of leaf 1 on 2-week-old plants

Colletotrichum lagenarium

Leaf 2 sprayed with inoculum 7 days later. Simulated commercial greenhouse conditions

Sphaerotheca fuliginea

Grapevines

Eotetranychus willamettei (Willamene spider mite)

Leaves with mites placed on vines in November 1987 (autumn)

Whole plants sprayed with spore suspensions 14 days later Tetranychus Natural infestation pacificus (Pacific in 1988 season spider mite)

Effectiveness

Reference cited

Light disease after Sutton (1982) 7 days, extensive disease in controls. Greater survival at 5 weeks and occurrence of flowering and pod-set, in contrast to controls Lesion numbers Descalzo et a/. decreased by (1990) 66% and lesion diameters smaller compared with controls, 7 days after challenge No induced Descalzo et a/. resistance 7, 14 (1990) and 21 days after challenge Nine-fold decrease in challenge populations in early June on treated vines. Acaricide used in late June reducing all mite populations to

Karban and English-Loeb (1 990)

Pear Pepper Rice

Tobacco

Watermelon

Dichloroisonicotinic acid or its ester Dichloroisonicotinic acid Dichloroisonicotinic acid or its ester

25 g hlspray

' foliar

25 g ha-' foliar spray2 kg ha to field water

near zero. Threefold decrease in challenge populations in September on vines first treated in November 1987. > 50% over unstated period

Erwinia amylovora

7

Xanthomonas vesicatoria Pyricularia oryzae

7 7

unstated period > 90% over unstated period

Xanthomonas oryzae

7

> 95% over

Peronospora tabacina

Stem injection 44-60 days after planting out

Peronospora tabacina

Dichloroisonicotinic acid Fusarium oxysporum f.sp. niveum race 1

20 g hl-' foliar spray To root system 3 days before transplant to challengeinfested soil

Peronospora tabacina Fusarium oxysporum f.sp. niveum race 2

Foliar spray 67 davs after pla.nting out

7 Present at 750 cfu g-' in soil receiving transplants

> 80% over

unstated period

MBtraux et al. (1991 ) MBtraux et al. (1991) MBtraux et a/. (1991) MBtraux et al. (1991) Cruickshank and Mandrvk (1960)

Significant decreases in foliar infection at 81 days in plants stem injected at 4 4 and 53 days; greater at 44 days > 50% over MBtraux et al. (1991) unstated period Symptoms Martyn et al. delayed. 35% (1991) fewer plants died compared with controls. Some marketable fruit produced; none in controls

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dichloro-isonicotinic acid and related compounds are likely candidates to be used as activators of plant defence in plant protection for the reasons summarized in Tables II and III and discussed earlier. Because of the attractiveness of these prospects, a short account of the procedures used in discovering these agents is given in order to present some perspective. Following the convincing demonstration of systemic induced resistance in cucurbits using fungal pathogens (Ku~ et al., 1975), Ciba-Geigy started a policy of triple-screening among some large numbers of new chemical products each year for ability to induce resistance. The first step in the screen is capacity to control selected and common diseases in seedling plants. The effective control agents are then screened for absence of direct effects on selected fungal pathogens in culture on laboratory growth media. The few compounds that emerge from this second screen are tested for their ability to cause the formation of pathogenesis-related proteins in uninfected plants. Dichloro-isonicotinic acid and its methyl ester were two of very few compounds that passed all three screens. They were patented on the basis of these properties, some of which were reported by M~traux et al. (1991). Approximately 8 years elapsed between discovery of their potential and this report and several more are likely to elapse before a decision is made about their registration and use. Related compounds, two chloroisonicotinamides, have been reported to have similar protective properties when tested against the rice blast disease (Yoshida et al., 1990; Seguchi etal., 1992). It can be anticipated that a few other compounds with similar properties are likely to come from Ciba-Geigy and other plant protection companies in the next few years. From this information, it can be seen that a considerable effort is undergone before any chemical agent becomes available for consideration for use in plant protection. When one emerges that has the special ability to induce resistance, it has advantages over biological agents of relative ease of application as a foliar spray or as a soil drench. There is now a very strong possibility of being able to protect a range of plants through their natural defence systems by using such a chemical agent. The protection is likely to be effective against a broad spectrum of pathogens and may be quite long lasting, with a possibility of being extended in duration through a growing season after a second ('boosting') induction. There is also the prospect of being able to return to use some of the older cultivars that had desirable qualities apart form their susceptibility to common diseases. The tecl~nology for using natural defence systems in plant protection is almost ready for use. Research and development on its durability under environmental stresses and on any negative effects for growth, yield and quality are proceeding. The choice of another major procedure for integration into plant protection towards sustainability can then be made.

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A CKN O WLEDG EM EN TS I thank S . E . C o l e m a n for help in literature searching, V . F . Moschione for word-processing the text and tables and E. K. D a n n for c o m m e n t s on the text.

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International Symposium on the Molecular Genetics of Plant-Microbe Interactions, Interlaken, Switzerland. (abstract) Aist, J. R. (1983). Structural responses as resistance mechanisms. In 'The Dynamics of Host Defence' (J. A. Bailey and B.J. Deverall, eds), pp. 33-70. Academic Press, Sydney. Bailey, J. A. and Mansfield, J. W. (1982). 'Phytoalexins'. Blackie, Glasgow. Baldwin, B. C. and Rathmell, W. G. (1988). Evolution of concepts for chemical control of plant disease. Annual Review of Phytopathology 26, 265-283. Bargmann, C. and Sch/Snbeck, F. (1992). Acremonium kiliense as inducer of resistance to wilt diseases on tomatoes. Journal of Plant Diseases and Protection 99, 266-272. Biles, C. L. and Martyn, R. D. (1989). Local and systemic resistance induced in watermelon by formae speciales of Fusarium oxysporum. Phytopathology 79, 856-860. Chester, K.S. (1933). The problem of acquired physiological immunity in plants. Quarterly Review of Biology 8, 119-154; 275-324. Christ, U. and Mosinger, E. (1989). Pathogenesis-related proteins of tomato: I. Induction by Phytophthora infestans and other biotic and abiotic inducers and correlations with resistance. Physiological and Molecular Plant Pathology 35, 53-65. Cloud, A. M . E . and Deverall, B.J. (1987). Induction and expression of systemic resistance to the anthracnose disease in bean. Plant Pathology 36, 551-557. Cohen, Y. and Coffey, M. D. (1986). Systemic fungicides and the control of Oomycetes. Annual Review of Phytopathology 24, 311-338. Cohen, Y., Gisi, U. and Mosinger, E. (1991). Systemic resistance of potato plants against Phytophthora infestans induced by unsaturated fatty acids. Physiological and Molecular Plant Pathology 38, 255-263. Cohen, Y., Reuveni, M. and Kenneth, R. (1975). Resistance to powdery mildew in tobacco induced by Peronospora tabacina. Phytopathology 65, 1313-1315. Cruickshank, I. A. M. and Mandryk, M. (1960). The effect of stem infestation of tobacco with Peronospora tabacina Adam. on foliage reaction to blue mold. Journal of the Australian Institute of Agricultural Science 26, 369-372. Dann, E. K. (1991). Studies on inducing systemic resistance in beans and broad beans by biological and chemical means. BSc Agr Thesis, University of Sydney. Darvill, A. G. and Albersheim, P. (1984). Phytoalexins and their elicitors - a defence against microbial infection in plants. Annual Review of Plant Physiology 35, 243-275. Descalzo, R. C., Rahe, J. E. and Mauza, B. (1990). Comparative efficacy of induced resistance for selected diseases of greenhouse cucumber. Canadian Journal of Plant Pathology 12, 16-24. Deverall, B. J. and Dann, E. K. (1995). Induced resistance in legumes. In 'Induced Resistance to Disease' (R. Harnmerschmidt and J. Ku~, eds). Kluwer, Dordrecht, in press. Doke, N., Rarnirez, A. V. and Tomiyama, K. (1987). Systemic induction of resistance in potato plants against Phytophthora infestans by local treatment with hyphal wall fragments of the fungus. Journal of Phytopathology 119, 232-239.

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Doubrava, N. S., Dean, R . A . and Ku6, J. (1988). Induction of sytemic resistance to anthracnose caused by Colletotrichum lagenarium in cucumber by oxalate and extracts from spinach and rhubarb leaves. Physiological and Molecular Plant Pathology 33, 69-79. Ebel, J. (1986). Phytoalexin synthesis: the biochemical analysis of the induction process. Annual Review of Phytopathology 24, 235-264. Goodman, R. N. (1978). Inducible resistance responses in plants to plant pathogenic bacteria. Mycopathologia 65, 107-113. Gottstein, H. D. and Ku~, J. (1989). Induction of systemic resistance to anthracnose in cucumber by phosphates. Phytopathology 79, 176-179. Hammerschmidt, R. and Ku~, J. (1995). 'Induced Resistance to Disease'. Kluwer, Dordrecht, in press. Hecht, E. I. and Bateman, D. F. (1964). Nonspecific acquired resistance to pathogens resulting from localised infections by Thielaviopsis basicola or viruses in tobacco leaves. Phytopathology 54, 523-530. Heller, W . E . and Gessler, C. (1986). Induced systemic resistance in tomato plants against Phytophthora infestans. Journal of Phytopathology 116, 323-328. Hong, N. and Ogawa, T. (1990). Stereocontrolled syntheses of phytoalexin elicitor-active 3-D-glucohexaoside and 13-D-glucononaoside. Tetrahedron Letters 31, 3179-3182. Karban, R. and English-Loeb, G. M. (1990). A 'vaccination' of Willamette spider mites (Acari: Tetranychidae) to prevent large populations of Pacific spider mites on grapevines. Journal of Economic Entomology 83, 2252-2257. Kroon, B. A. M., Scheffer, R . J . and Elgersma, D . M . (1991) Induced resistance in tomato plants against Fusarium wilt invoked by Fusarium oxysporum f.sp. dianthi. Netherlands Journal of Plant Pathology 97, 401-408. Ku~, J. (1983). Induced systemic resistance in plants to diseases caused by fungi and bacteria. In 'The Dynamics of Host Defence' (J. A. Bailey and B.J. Deverall, eds), pp. 191-221. Academic Press, Sydney. Ku~, J. (1990). Immunization for the control of plant disease. In 'Biological Control of Soil-borne Plant Pathogens' (D.J. Hornby, ed.), pp. 355-373. CAB International, Wallingford. Ku~, J., Shockley, G. and Kearney, K. (1975). Protection of cucumber against CoUetotrichum lagenarium by Colletotrichum lagenarium. Physiological Plant Pathology 7, 195-199. Langcake, P. and Wickens, S. G. A. (1975). Studies on the action of the dichlorocyclopropanes on the host-parasite relationship in the rice blast disease. Physiological Plant Pathology 7, 113-126. Linthorst, H . J . M . (1991). Pathogenesis-related proteins of plants. Critical Reviews in Plant Sciences 10, 123-150. Malamy, J., Carr, J. P., Klesig, D . F . and Raskin, I. (1990). Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250, 1002-1004. Martyn, R. D., Biles, C. L. and DiUard III, E. A. (1991). Induced resistance to Fusarium wilt of watermelon under simulated field conditions. Plant Disease 75, 874-877. Matta, A. (1980). Defenses triggered by previous diverse invaders. In 'Plant Disease, an Advanced Treatise' (J. G. Horsfall and E. B. Cowling, eds), pp. 345-361. Academic Press, New York. McIntyre, J. L. and Dodds, J. A. (1979). Induction of localized and systemic protection against Phytophthora parasitica var. nicotianae by tobacco mosaic virus infection of tobacco hypersensitive to the virus. Physiological Plant Pathology 15, 321-330. M~traux, J. P., Ahl Goy, P., Staub, T., Speich, J., Steinmann, A., Ryals, J. and Ward, E. (1990). Induced systemic resistance in cucumber in response to 2,6-dichloroisonicotinic acid and pathogens. Proceedings of the 5th International Symposium on the Molecular Genetics of Plant-Microbe Interactions, Interlaken, Switzerland. (abstract)

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M~traux, J. P., Ahl Goy, P., Staub, T., Speich, J., Steinemann, A., Ryals, J. and Ward, E. (1991). Induced systemic resistance in cucumber in response to 2,6-dichloroisonicotinic acid and pathogens. In 'Advances in Molecular Genetics of Plant-Microbe Interactions, Vol. 1' (H. Hennecke and D. P. S. Verma, eds), pp. 432-439. Kluwer, Dordrecht. Murray, D.C. and Walters, D. R. (1992). Increased photosynthesis and resistance to rust infection in upper, uninfected leaves of rusted broad bean (Vicia faba L.). New Phytologist 120, 235-242. Nakahara, Y. and Ogawa, T. (1990). Stereoselective total synthesis of dodecagalacturonic acid, a phytoalexin elicitor of soybean. Carbohydrate Research 205, 147-159. Nemestothy, G. S. and Guest, D. I. (1990). Phytoalexin accumulation, phenylalanine ammonia lyase activity and ethylene biosynthesis in fosetyl-A1 treated resistant and susceptible tobacco cultivars infected with Phytophthora nicotianae var. nicotianae. Physiological and Molecular Plant Pathology 37, 207-219. Pan, S. Q., Ye, X.-S. and Ku6, J. (1991). Association of/3-1,3-glucanase activity and isoforrn pattern with systemic resistance to blue mould in tobacco induced by stem injection with Peronospora tabacina or leaf inoculation with tobacco mosaic virus. Physiological and Molecular Plant Pathology 39, 25-39. Phillips, J. N., Witrzens, B., Dalton, L. K. and Elmes, B. C. (1981). Induced resistance to Fusarium wilt in tomato seedlings. Phytopathologische Zeitschrift 101, 189-195. Rathmell, W.G. (1984). The discovery of new methods of chemical disease control: current developments, future prospects and the role of biochemical and physiological research. Advances in Plant Pathology 2, 260-288. Ricci, P., Trentin, F., Bonnet, P., Venard, P., Mouton-Perronet, F. and Bruneteau, M. (1992). Differential production of parasiticein, an elicitor of necrosis and resistance in tobacco, by isolates of Phytophthora parasitica. Plant Pathology 41, 298-307. Ross, A. F. (1961). Systemic acquired resistance induced by localized virus infections in plants. Virology 14, 340-358. Seguchi, K., Kurotaki, M., Sekido, S. and Yamaguchi, I. (1992). Action mechanism of N-cyanomethyl-2-chloroisonicotinamide in controlling rice blast disease. Journal of Pesticide Science 17, 107-113. Sequeira, L. (1983). Mechanisms of induced resistance in plants. Annual Review of Microbiology 37, 51-79. Smith, J. A. and M6traux, J.-P. (1991). Pseudomonas syringae pv. syringae induces systemic resistance to Pyricularia oryzae in rice. Physiological and Molecular Plant Pathology 39, 451-461. Smith, J . A . , Hammerschmidt, R. and Fulbright, D.W. (1991). Rapid induction of systemic resistance in cucumber. Physiological and Molecular Plant Pathology 38, 223-235. Sutton, D. C. (1979). Systemic cross protection in bean against Colletotrichum lindemuthianum by Colletotrichum lindemuthianum. Australasian Plant Pathology 8, 4-5. Sutton, D.C. (1982). Field protection in bean against Colletotrichum lindemuthianum by Colletotrichum lindemuthianum. Australasian Plant Pathology 11, 50-51. Suzuki, H. (1980). Defenses triggered by previous invaders: fungi. In 'Plant Disease, an Advanced Treatise' (J. G. Horsfall and E. B. Cowling, eds), pp. 319-332. Academic Press, New York. Walters, D. R. and Murray, D.C. (1992). Induction of systemic resistance to rust in Vicia faba by phosphate and EDTA: effects of calcium. Plant Pathology 41, 444-448. Watanabe, T., Igarashi, H., Matsumoto, K., Seki, S., Mase, S. and Sekizawa, Y. (1977). The characteristics of probenazole (Oryzemate) for the control of rice blast. Journal of Pesticide Science 2, 291-296. Watanabe, T., Sekizawa, Y., Shimura, M., Susuki, Y., Matsumoto, K., Iwata, M. and

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Mase, S. (1979). Effects of probenazole (Oryzemate) on rice plants with reference to controlling rice blast. Journal of Pesticide Science 4, 53-59. Yalpani, N., Silverman, P., Wilson, T. M. A., Kleier, D.A. and Raskin, I. (1991). Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. The Plant Cell 3, 809-818. Yoshida, H., Koishi, K., Nakagawa, T., Sekido, S. and Yamaguchi, I. (1990). Characteristics of N-phenylsulfonyl-2-chloroisonicotinamide as an anti-rice blast agent. Journal of Pesticide Science 15, 199-203.

12 THE ROLE OF SOIL MICROBIOLOGY IN SUSTAINABLE INTENSIVE AGRICULTURE C.E. Pankhurst* and J. M. Lynch T *CSIRO, Division of Soils, Glen Osmond, South Australia, 5064, Australia t School of Biological Sciences, University of Surrey, Guildford, Surrey G U2 5 X l l , UK

I. II. III. IV. V.

Introduction Numbers and Biodiversity of Micro-organisms in Soil Role of Soil Micro-organisms in the Conservation of Soil Structure Soil Micro-organisms and Nutrient Recycling in Soils Interactions of Soil Micro-organisms with Plants A. Nitrogen fixation B. Mycorrhizal Fungi C. Plant Growth-promoting Rhizobacteria D. Biological Control of Plant Root Diseases VI. Integrated Management and Control of Pests and Diseases VII. Opportunities for Soil Microbiological Inputs into Sustainable Agricultural Systems A. On-going Opportunities B. New Opportunities VIII. Potential Use of Soil Micro-organisms as Indicators of Soil Quality and Sustainability References

229 230 232 233 235 235 237 238 239 241 242 242 243 243 244

I. I N T R O D U C T I O N Sustainable agriculture embraces several forms of non-convential agriculture that are often referred to as organic, alternative, ecological or low-input. However, these terms are not synonymous with sustainable agriculture, because each has a special focus of its own. To be sustainable the farm must produce adequate amounts of high-quality food, protect its resources and be both environmentally safe and profitable. Instead of depending on purchased materials such as fertilizers, a sustainable farm relies as much as possible on beneficial natural processes and renewable resources drawn from the farm itself. Reductions of chemical energy inputs to agriculture could lead to more economical production systems while minimizing pollution. This might be achieved by modifying farming systems (e.g. reduction of tillage), the use of improved efficiency organic ADVANCES IN PLANT PATHOLOGY~VOL. 11 ISBN 0-12-033711-8

Copyright9 1995 AcademicPressLimited All rightsof reproductionin anyform reserved

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C. E. Pankhurst and J. M. Lynch

fertilizers and the partial replacement of crop protection chemicals with microorganisms (including those that have been genetically modified). To understand the rationale for sustainable agriculture, one must appreciate the critical importance of soft. Soil is not just another component of crop production, like pesticides or fertilizers. Rather it is a complex, living, fragile medium that must be protected and nurtured to ensure its long-term productivity and stability. A healthy soil is a hospitable world for growth. It is composed of mineral particles and organic materials that combine and are held together as aggregates providing a three-dimensional fabric that retains moisture, allows air to circulate freely and to which plant nutrients may cling. It also contains vast populations of soil organisms, including micro-organisms (bacteria, fungi, actinomycetes and algae) and soil fauna (protozoa, nematodes, microarthropods, arthropods and earthworms), most of which are involved in the decomposition of organic matter. Decomposition of organic matter results in the formation of humus and the release of many nutrients important for plant growth. Some soil organisms contribute directly to soil fertility by fixing atmospheric nitrogen into forms of nitrogen that plants and other organisms use for growth. Others contribute to soil health by producing polysaccharides which help to bind soil particles together and help the soil resist erosion. To remain healthy, the soil must be fed organic materials such as various manures and crop residues. Because the maintenance of soil structure and fertility is of paramount importance for plant growth and because this in turn is dependent on the activities of soil organisms (especially soil micro-organisms), soil microbiology has a significant role to play in intensive sustainable agriculture. Consideration of this role will focus on those aspects of soil microbiology that contribute directly and indirectly to plant growth. This will include discussion of the importance of soil micro-organisms to: (1) the maintenance of soil structure; (2) their role in nutrient recycling; and (3) their beneficial and detrimental interactions with plants. Consideration will also be given to prospects for the management of soil micro-organisms in sustainable agricultural systems and the potential of using microbial activities and/or populations of soil micro-organisms as indicators of sustainability.

II. NUMBERS A N D BIODIVERSITY OF MICRO-ORGANISMS IN SOIL

Soil micro-organisms, including bacteria, actinomycetes, fungi, algae (mostly blue-green algae (cyanobacteria)) and protozoa constitute the major part of the soil biomass. In a fertile temperate soil, the microbial biomass may exceed 20 t ha-1. The diversity of this population of micro-organisms can only be estimated as current culturing methods are able to distinguish only a small proportion, probably