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Advances in

ECOLOGICAL RESEARCH VOLUME 23

This Page Intentionally Left Blank

Advances in

ECOLOGICAL RESEARCH Edited by

M. BEGON Department of Zoology, University of Liverpool, Liverpool, L69 3BX, UK

A. H. FITTER Department of Biology, University of York, York, YO1 SDD, UK

VOLUME 23

ACADEMIC PRESS Harcourt Brace Jovanovich, Publishers London San Diego New York Boston Sydney Tokyo Toronto

ACADEMIC PRESS LTD 24/28 Oval Road London NWI 7DX United States Edition published by

ACADEMIC PRESS INC. San Diego, CA 92101

Copyright 0 1992 by ACADEMIC PRESS LIMITED

AN 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

British Library Cataloguing in Publication Data Advances in ecological research. Vol. 23 I . Ecology 1. Begon, Michael 574.5 ISBN&l2413923-5

This book is printed on acid-free paper Typeset by Latimer Trend & Company Ltd, Plymouth Printed in Great Britain by T. J. Press (Padstow) Ltd, Padstow, Cornwall.

Contributors to Volume 23 A. D. Q. AGNEW, Department of Biological Sciences, University College of Wales, Aherystwyth SY23 3DA, UK. J. BASTOW WILSON, Botany Department. University of Otago, PO Box 56, Dunedin, New Zealand. M . L. CIPOLLINI, Department of Biological Sciences, Rutgers University, New Brunswick, NJ 08855-1059, USA. R. M . M. CRAWFORD, Department of Biology and Preclinical Medicine, Sir Harold Mitchell Building, The University, St Andrews. Fife KY16 9AL, UK. H. LAMBERS, Department of Plant Ecology and Evolutionary Biology, PO Box 800.84, NL-3508 T B Utrecht. The Netherlands. J . LUSSENHOP, Department of Biological Sciences, University of Illinois at Chicago, Box 4348, Chicago, I L 60680, USA. H. POORTER, Department of Plant Ecology and Evolutionary Biology, PO Box 800.84, NL-3508 T B Utrecht, The Netherlands. E. W. STILES, Department of Biological Sciences, Rutgers University, New Brunswick, N J 08855-1059. USA.


Preface The contributions to this volume are linked by their concern with topics or questions that have suffered a degree of neglect. Nobody can now seriously doubt the crucial importance of biotic interactions, hidden from the sight of most ecologists, within the soil, nor of the increasing necessity of conscious management of the soil biota, within agricultural and forest soils at least. Interactions between micro-organisms and micro-arthropods are central to many, if not most, soil processes. Lussenhop reviews what is known of the mechanisms through which these interactions occur, focusing separately on saprophytic systems and the rhizosphere, and ranging from simple grazing and dispersal, through the stimulation of microbial activity, to the potential regulation of pathogens. The conclusion, as so often, seems to be that the steps from description to useful quantification have yet to be taken. The co-evolutionary pressures connecting plants and their potential consumers are rarely if ever straightforward. Certainly, those addressed by Cipollini and Stiles, between fleshy fruits, their vertebrate dispersers and fruit-rot fungi are complex and subtle. In the past, studies of the secondary chemicals of fleshy fruits have concentrated on the almost certainly atypical, highly-selected cultivated species. By contrast, these authors evaluate selection pressures in a more general and natural context, generate a number of broad hypotheses, and then, using their own work with Ericaceous species as a springboard, show how these predictions may be given added specificity. When the distinction is drawn in introductory ecological texts between limiting and non-limiting resources, oxygen is sometimes advanced as a good example of the latter: crucially necessary, but always available in abundance to those aerobic organisms that require it. As Crawford shows, however, for plants at least, there are many situations where this view is quite simply wrong. Physiological and distributional data are combined to demonstrate that during the life cycle of most species of higher plants, there are critical periods when oxygen is a resource that is frequently limiting for germination, growth and survival. From the Arctic to the Tropics, the pattern of plant distribution frequently bears the imprint of oxygen as a limiting factor. It is no great surprise that plants growing on nutrient-poor soils have a lower growth rate than those on fertile soils. But even when grown under optimum conditions, species that naturally occur on nutrient-poor soils still have relatively low growth rates, as do those species (and ecotypes) charac-

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teristic of shaded environments, dry habitats, saline conditions and other habitats intrinsically unsupportive of plant growth. Lambers and Poorter, therefore, ask two related questions. What are the physiological causes of these differing growth rates? And what are their ecological consequences? Their provisional answers are framed, perhaps not surprisingly, in the language of trade-offs, but the need remains for quantitative data that might fully support their contentions. Views of community (especially plant community) dynamics have been much influenced by Clements’ facilitation theory of succession and Watt’s theory of cyclic succession, both based on the idea of plants making their environments less suitable for themselves. The thrust of Wilson and Agnews’s argument, on the other hand, is that this has led to the comparative neglect of processes that do, broadly, just the opposite, where a community modifies the environment, making it more suitable for that community. They call these positive-feedback switches. Four types of switch and four effects of switches are distinguished, before their mediation by water, pH, soil-elements, light, temperature, wind, fire, allelopathy, microbes, termites and herbivores are reviewed. Many of the examples are speculative, but if community ecologists are persuaded to re-examine their perspectives, as seems likely, then such speculation will have been fruitful and constructive. Hence, the papers in this volume contribute to the series’ main aim: not to provide a vehicle for specialists to review topics of interest only to other specialists in the same field, but to allow ecologists in general to remain aware not only of the advances that are made, but of the lacunae that remain in a subject that grows every more diverse. M. Begon A. H. Fitter

Contents Contributors to Volume 23 . . . . . . . . . . . . . . . . . Preface . . . . . . . . . . . . . . . . . . . . . . .

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Mechanisms of Microarthropod-Microbial Interactions in Soil JOHN LUSSENHOP

I . Summary . . . . . . . . . . . . . . . . . . I1 . Introduction . . . . . . . . . . . . . . . . . 111. Historical and Biological Reasons for Interactions . . . . IV . Interactions in the Saprophytic System . . . . . . . . A . Competition . . . . . . . . . . . . . . . . B . Foraging . . . . . . . . . . . . . . . . . C . Microarthropods as Food of Bacteria and Fungi . . . D . Bacteria and Fungi as Food of Microarthropods . . . E . Fungal and Bacterial Response to Grazing . . . . . F. Microarthropod Digestion . . . . . . . . . . G . Microarthropod Excreta . . . . . . . . . . H . Dispersal . . . . . . . . . . . . . . . . I . Summary for the Saprophytic System . . . . . . V . Microarthropod-Microbial Interactions in the Rhizosphere A . Saprophyte-Pathogen-Microarthropod Interactions . B. Vesicular-Arbuscular Mycorrhizal-Microarthropod Interactions . . . . . . . . . . . . . . . C . Ectomycorrhizal-Microarthropod Interactions . . . D . Summary for Rhizosphere . . . . . . . . . . VI . Conclusions . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . .

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Relative Risks of Microbial Rot for Fleshy Fruits: Significance with Respect to Dispersal and Selection for Secondary Defense MARTIN L . CIPOLLINI and E D M U N D W . STILES

I . Summary . . . . . . . . . . . . . . . . . . I1 . Introduction . . . . . . . . . . . . . . . . A . Questions and Objectives . . . . . . . . . . B . Variations in Characteristics of Fleshy Fruits . . . C . lnterspecific Variation in Secondary Defense Chemistry 111. Fruit Rot and Effects on Dispersal . . . . . . . . .

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A . Influence of Fruit Rot on Dispersal . . . . B. Factors that Affect Risk of Microbial Rot . . C . Natural Selection for Fruit Defenses . . . IV . General Hypotheses and Predictions . . . . . A . General Deterrent Nature of Fruit Rot . . . B . Microbe-specific Defenses . . . . . . . C . Interspecific Variation in Defense Effectiveness V. Predictions for Temperate Seed Dispersal Systems A . Temperate Fruiting Classes . . . . . . . B. Predictions for Temperature Species . . . . VI . Conclusions . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . .

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Oxygen Availability as an Ecological Limit to Plant Distribution R . M . M . CRAWFORD I . Introduction . . . . . . . . . . . . . . . . . . I1. Plant Organs Liable to Oxygen Deprivation . . . . . . . A . The Hypoxic Seed . . . . . . . . . . . . . . . B. Underground Organs . . . . . . . . . . . . . . C. Above-ground Organs with Limited Access to Oxygen . . Ill . Plant Structure and Oxygen Supply . . . . . . . . . . A . Distribution and Function of Aerenchyma . . . . . . B . Mass Movement of Air in Aquatic Species . . . . . . IV . Symbiosis and Oxygen Supply . . . . . . . . . . . . A . Root Nodules . . . . . . . . . . . . . . . . B. Nitrogen Fixation in the Rhizosphere of Aquatic Plants . . C . Mycorrhizas . . . . . . . . . . . . . . . . . V . Consequences of Oxygen Deprivation for Survival and Metabolism A . Sensing Oxygen Deficiency in Plant Tissues . . . . . . B . Cellular Effects of Oxygen Deprivation . . . . . . . . C . Metabolic Adaptations to Anoxia . . . . . . . . . D . Causes and Prevention of Post-anoxic Injury . . . . . . E . Mineral Nutrition and Flooding Tolerance . . . . . . VI . Oxygen and Plant Competition . . . . . . . . . . . . VII . Consequences of Climatic Change for the Vegetation of Oxygen-deficient Habitats . . . . . . . . . . . . . . VIII . Conclusions . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . .

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Inherent Variation in Growth Rate Between Higher Plants: A Search for Physiological Causes and Ecological Consequences HANS LAMBERS and HENDRIK POORTER I . Summary . . . . . . . . . . . . . . . . . . . . I1 . Introduction . . . . . . . . . . . . . . . . . . .

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111. Growth Analyses .

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IV . Net Assimilation Rate and Leaf Area Ratio . . . . . . . . V. Specific Leaf Area . . . . . . . . . . . . . . . . . A . Components of SLA . . . . . . . . . . . . . . . B. Plasticity in SLA . . . . . . . . . . . . . . . . VI . Biomass Allocation . . . . . . . . . . . . . . . . . A . Biomass Allocation at an Optimum Nutrient Supply . . . . B. Plasticity in Biomass Allocation . . . . . . . . . . . VII . Growth. Morphology and Nutrient Acquisition of Roots . . . . A . Root Growth and Nutrient Acquisition at an Optimum Nutrient Supply . . . . . . . . . . . . . . . . B. The Plasticity of Parameters Related to Root Growth and Nutrient Acquisition . . . . . . . . . . . . . . . C . Other Root Characteristics Related to Nutrient Acquisition . . D . Conclusions . . . . . . . . . . . . . . . . . . VIII . Chemical Composition . . . . . . . . . . . . . . . . A . Primary Compounds . . . . . . . . . . . . . . . B. Secondary Compounds . . . . . . . . . . . . . . C . Defence under Suboptimal Conditions . . . . . . . . . D . Effects of Chemical Defence on Growth Potential . . . . . E . The Construction Costs of Plant Material . . . . . . . . F . Conclusions . . . . . . . . . . . . . . . . . . IX . Photosynthesis . . . . . . . . . . . . . . . . . . A . Species-specific Variation in the Rate of Photosynthesis . . . B. Photosynthetic Nitrogen Use Efficiency . . . . . . . . C . Is There a Compromise between Photosynthetic Nitrogen Use Efficiency and Water Use Efficiency? . . . . . . . . . D . Photosynthesis under Suboptimal Conditions . . . . . . E . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . X . Respiration A . Species-specific Variation in the Rate of Respiration . . . . B. Respiration at Suboptimal Nitrogen Supply or Quantum Flux Density . . . . . . . . . . . . . . . . . . . C . Conclusions . . . . . . . . . . . . . . . . . . XI . Exudation and Volatile Losses . . . . . . . . . . . . . A . The Quantitative and Qualitative Importance of Exudation . . B. The Quantitative and Qualitative Importance of Volatile Losses . C . Conclusions . . . . . . . . . . . . . . . . . . XI1. Other Differences between Fast- and Slow-growing Species . . . A . Hormonal Aspects . . . . . . . . . . . . . . . B. Miscellaneous Traits . . . . . . . . . . . . . . . XI11. An Integration of Various Physiological and Morphological Aspects . A . Carbon Budget . . . . . . . . . . . . . . . . . B . Interrelations . . . . . . . . . . . . . . . . . XIV . Species-specific Performance under Suboptimal Conditions . . .' xv . The Ecological Consequences of Variation in Potential Growth Rate A . What Ecological Advantage can be Conferred by a Plant's Growth Potential? . . . . . . . . . . . . . . . . B. Selection of Traits Associated with a Low SLA . . . . . . C . Selection for Other Traits Underlying R G R . . . . . . . D . Consequences of a High Growth Potential for Plant Performance in Specific Environments . . . . . . . . .

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E . A Low Growth Potential and Plant Performance in Adverse Environments. Other than Nutrient-poor Habitats . . . . F. Conclusions . . . . . . . . . . . . . . . . . XVI . Concluding Remarks and Perspectives . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . .

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Positive-feedback Switches in Plant Communities

J . BASTOW WILSON and ANDREW D . Q . AGNEW I . Summary . . . . . . . . . . . . . . . I1 . Introduction . . . . . . . . . . . . . . A . Switches . . . . . . . . . . . . . . B . Types of Switch . . . . . . . . . . . C . Boundaries . . . . . . . . . . . . . D . Vegetational Situations Produced by Switches . E . Agencies . . . . . . . . . . . . . . 111. Water-mediated Switches . . . . . . . . . . A . Concept . . . . . . . . . . . . . . B. Fog Precipitation . . . . . . . . . . . C . Infiltration . . . . . . . . . . . . . D . Sediment Entrapment: Salt Marsh Pans . . . E . Ombrogenous Bog Growth . . . . . . . . F. Snow Accumulation . . . . . . . . . . IV . pH-mediated Switches . . . . . . . . . . . V. Soil-element-mediated Switches . . . . . . . . A . NPK Increase . . . . . . . . . . . . B . NPK Decrease . . . . . . . . . . . . C . Heavy Metals . . . . . . . . . . . . D . Salt . . . . . . . . . . . . . . . . VI . Light-mediated Switches . . . . . . . . . . VII . Temperature-mediated Switches . . . . . . . . A . Concept . . . . . . . . . . . . . . B. Treeline . . . . . . . . . . . . . . C . Graminoid Tussocks . . . . . . . . . . VIII . Wind-mediated Switches . . . . . . . . . . A . Concept . . . . . . . . . . . . . . B. Soil Erosion and Trapping . . . . . . . . C . Wind Damage to Plants . . . . . . . . . IX . Fire-mediated Switches . . . . . . . . . . . A . Concept . . . . . . . . . . . . . . B . Australian Closed-forest/Savannah . . . . . C . African Closed-forest/Savannah . . . . . . D . Conclusion . . . . . . . . . . . . . X . Allelopathy-mediated Switches . . . . . . . . XI . Microbe-mediated Switches . . . . . . . . . A . Oldfield Succession and Nitrogen-fixing Microbes B. Forests and Mycorrhizas . . . . . . . . XI1 . Termite-mediated Switches . . . . . . . . .

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XI11. Herbivore-mediated Switches . . . A . Concept . . . . . . . . . B . Grass/Grass Boundary . . . . C . Grass/Woodland Boundary . . D . Grazing and Nitrogen Cycling .

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E . Insects in Pine F. Conclusions . XIV . Discussion . . . Acknowledgements . . References . . . . .

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Mechanisms of Microarthropod-Microbial Interactions in Soil JOHN LUSSENHOP

I. I1. I11. IV .

Summary . . . . . . . . . . . . . . . . . Introduction . . . . . . . . . . . . . . . . Historical and Biological Reasons for Interactions . . . Interactions in the Saprophytic System . . . . . . . A . Competition . . . . . . . . . . . . . . . B. Foraging . . . . . . . . . . . . . . . . C . Microarthropods as Food of Bacteria and Fungi . . D . Bacteria and Fungi as Food of Microarthropods . . E . Fungal and Bacterial Response to Grazing . . . . F. Microarthropod Digestion . . . . . . . . . . G . Microarthropod Excreta . . . . . . . . . . H . Dispersal . . . . . . . . . . . . . . . . I . Summary for the Saprophytic System . . . . . . V. Microarthropod-Microbial Interactions in the Rhizosphere A . Saprophyte-Pathogen-Microarthropod Interactions . B. Vesicular-Arbuscular Mycorrhizal-Microarthropod Interactions . . . . . . . . . . . . . . . C . Ectomycorrhizal-Microarthropod Interactions . . . D . Summary for Rhizosphere . . . . . . . . . . VI . Conclusions . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . .

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I. SUMMARY Many aspects of the distribution. abundance. and activity of soil fungi and bacteria are controlled by microarthropods . In saprophytic successions. six mechanisms of interaction are important. Two control fungal distribution and abundance: (a) selective grazing of fungi by microarthropods. and (b) dispersal of fungal inoculum by microarthropods . Four additional mechanisms stimulate microbial activity: (a) direct supply of mineral nutrients in ADVANCES IN ECOLOGICAL RESEARCH VOL . 23

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urine and feces, (b) stimulation of bacterial activity by microarthropod activity, (c) compensatory fungal growth due to periodic microarthropod grazing, and (d) release of fungi from competitive stasis due to microarthropod disruption of competing mycelial networks. Selective grazing can control species distribution and favor either efficient or inefficient decomposer fungi. Moderate grazing may stimulate microbial activity, thus augmenting either mineralization or immobilization of nutrients by micro-organisms. In the rhizosphere, the demonstrated mechanisms of interaction are dispersal and selective grazing. Microarthropods carry fungal propagules, including those of root pathogens, to root surfaces. Microarthropods also graze fungi on root surfaces, and they selectively consume saprophytic fungi. It has not been shown whether dispersal of pathogens to the rhizosphere is less important than preferential grazing o n pathogens. Vesicular-arbuscular mycorrhizal hyphae and germ tubes are also grazed preferentially, hence microarthropods are associated with fewer and less effective vesicular-arbuscular fungi. Ectomycorrhizal roots and their perennial networks in the soil may be physically and chemically protected from microarthropod grazing.

11. INTRODUCTION Interactions among fungi, bacteria, and invertebrates are central to many processes in soil ranging from decomposition to the functioning of the rhizosphere. The possible mechanisms of these interactions, including grazing, disturbance, and dispersal, have been little studied. It is important that these mechanisms be understood because in the future, conscious management of the soil biota in agricultural and forest soils will require knowledge of them. Grazing is the mechanism of interaction given most attention since Coleman et al. (1983) showed that mineral nitrogen and phosphorus levels in the rhizosphere were raised due to nutrients in excreta of bacterivorous nematodes and protozoa. But grazing, which is the consumption of parts of living organisms, is a complex phenomenon because of the modular nature of many grazed organisms, and because of the behavior of grazers. Grazers may be selective, and affect competition among grazed species. Grazers may cause disturbance that affects recovery of grazed species. Grazers may disperse propagules of the grazed species, and their excretions may control the rate and proportion of nutrient return to the grazed site. This complexity exists in grazed higher plant and algal systems, and it is likely that it exists in grazed microbial systems also. Seastedt (1984), for example, showed that while the presence of arthropods in litter bags increased mass loss by 23% on average, it had a smaller effect on mineral nutrient mineralization. Seastedt (1984) speculated that this smaller mineral nutrient effect might be due to arthropod

MECHANISMS OF MICROARTHROPOD-MICROBIAL INTERACTIONS IN SOIL

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stimulation of microbial growth. Anderson ( I 988) suggested the importance of dispersal and control of fungal species composition. The present chapter focuses on these and additional mechanisms of interaction between fungi, bacteria, and microarthropods. Microarthropods (collembola, protura, mites, pauropods) form a distinct group when their mass is compared with that of macroarthropods (millipedes, isopods) and nematodes (Fig. 1). Since mass is correlated with density, resource use, movement, and reproductive rate (Peters, 1983), microarthropods should interact with micro-organisms as grazers and transporters, while macroarthropods are primarily comminutors of litter, and nematodes and protozoa are primarily bacterivores. The goal of this chapter is to describe and evaluate the importance of mechanisms by which micro-organisms and microarthropods interact in soil. It is a first step towards making quantitative predictions about functioning of saprophytic and rhizosphere foodwebs. This is a demanding goal for a biota whose natural history is poorly known. The present chapter builds on recent additions to the knowledge of natural history of soil fungi (Domsch et a[., 1980; Wicklow and Carroll, 1981; Cooke and Rayner, 1984; Rayner and Boddy, 1988), and microarthropods (Dindal, 1990; Norton, 1992).

111. HISTORICAL AND BIOLOGICAL REASONS FOR INTERACTIONS Soil micro-organisms and microarthropods have interacted since the Devonian when foodwebs developed in soil around the first terrestrial plants. Just as insect herbivores radiated in response to angiosperm evolution in the Cretaceous, soil microarthropods and fungi represent an earlier radiation in response to tracheophyte evolution. Microarthropod fecal pellets containing hyphae are known from the Silurian (Sherwood-Pike and Gray, 1985). By the Devonian, fossil oribatids (Shear et al., 1984), prostigmatids and collembola (Kevan et al., 1975) were present. In the Devonian, damaged Rhynia tissue (Kevan et al., 1975) suggests that arthropod herbivores had evolved, and the presence of branching septate hyphae in the secondary xylem of a fossil, arborescent, progymnosperm indicates that saprophytic fungi had evolved (Stubblefield and Taylor, 1988). Devonian terrestrial plants may have been aided in water and nutrient uptake by endomycorrhizal symbionts (Pirozynski and Malloch, 1975), although the first unquestioned fossil mycorrhizal arbuscules are from the Triassic (Stubblefield et a[., 1987). Protective tissue, spore ornamentation, and presence of cutin and suberin in Devonian fossils suggest a need for protection from herbivores as well as for water conservation. Later development of lignins, terpenoids and flavonoids in the Carboniferous is interpreted

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Fig. 1. Average live mass of soil invertebrate taxa shows three distinct groups when graphed on a logarithmic scale. Values are averages for species from many communities tabulated by Edwards (1967) and Peterson (1982).


5

as defense against pathogenic and decay fungi as well as from herbivorous insects; these compounds must have changed the chemical ecology of decomposers, including microarthropods (Swain and Cooper-Driver, 1981). The long history of co-occurrence of microarthropods with fungi and bacteria is one reason to expect interactions. Digestive and transport mutualisms are not likely to be as well-developed among soil as among terrestrial arthropods. For example, soil microarthropods appear to lack mycetomes-groups of specialized cells containing symbiotic micro-organisms-which aid digestion in many insects. Soil microarthropods may not need mycetomes since they ingest so many micro-organisms and microbial exoenzymes. Soil microarthropods also lack external cavities (mycangia) and internal sacs (sporothecae) for transport of fungal propagules. Soil microarthropods may not need these specialized transport structures as much as terrestrial arthropods, but they may have primitive forms of mycangia. The highly sculptured integument of 75% of the higher oribatid superfamilies may function as mycangia: figs 4 . 5 4 . 6 in Blackwell ( 1 984) show a Carahodes sp. with spores of the myxomycete Lycopalu epidendrum in cuticular depressions. On the other hand, well-developed reciprocal chemical interactions between microarthropods and micro-organisms should be expected. A suggestive example is the observation of Wicklow (1988) that detritivorous arthropods are more tolerant of mycotoxins than herbivorous arthropods. A second reason for expecting interactions between microarthropods and micro-organisms is the contrasting biology of the groups. Microarthropods, fungi, and many bacteria are heterotrophs, and so compete for similar resources, yet differences in their size, method of ingesting food, and population growth result in interactions. Soil bacteria are the smallest and most biochemically diverse of the three groups. They have the highest intrinsic rate of increase ( r ) , but due to limited carbon availability, Jenkinson and Ladd (198 1) estimated that the average cell divides once every 2.5 years in an English soil. Predominance of bacteria or fungi determines the invertebrate foodweb present. Bacterial biomass may sometimes be greater than fungal (Ingham et al., 1989), and bacterial activity may be briefly or locally greater than that of fungi. On a whole soil basis, Anderson and Domsch (1975) used selective inhibitors to show that fungal metabolic activity accounted for more than half the carbon mineralization in agricultural and forest soils. Hyphal growth is a central adaptation of fungi that determines much of their biology. The high surface to volume ratio of hyphae allows efficient utilization of the products of external enzymes, and hyphal networks allow translocation of nutrients to sites of active decomposition where growing hyphae are able to penetrate solid substrates. In contrast, bacteria occupy surfaces. It is the vulnerability of hyphal networks that is the basis for competitive interactions with invertebrates. Hyphae may form interwoven

6

J . LUSSENHOP

cords and rhizomorphs (Fig. 3C, p.19) as well as resting structures such as stroma, sclerotia, and pseudosclerotia: these are resistant to physical extremes as well as to animals. Because of their ability to grow at lower water potentials than bacteria, fungal-based foodwebs predominate in arid habitats (Whitford, 1989). Microarthropods are the right size to graze fungi and bacteria. Their mouthparts function by plucking and scraping (collembola, mites), shearing (mites), or piercing (prostigmatid mites and protura). They exhibit a range of life histories reflecting their strategy for utilizing micro-organisms or detritus. Microarthropod life histories include species with explosive reproductive rates (collembola with r as high as 0.15 (Gregoire-Wibo and Snider, 1977) to 0.3 (Rapoport and Aguirre, 1973)) allowing a numerical response to fungal growth. Other groups exhibit great population persistence-some oribatids with r close to zero (Cancela da Fonseca, 1980)-they are already present when fungal growth starts.

IV. INTERACTIONS IN THE SAPROPHYTIC SYSTEM A. Competition Among fungi, interspecific and even intraspecific competition between mutually antagonistic dicaryons is strong and slows decomposition. This is because saprophytic fungi gain access to resources by occupying volume with their hyphae. In the process hyphal networks compete by a number of mechanisms which have been summarized by Cooke and Rayner (1984). Effects on hyphae some distance away may be caused by chemicals; contact effects include parasitism, hyphal interference, hyphal fusion, or the production of dense zones of mycelia. As a result of these strong fungal competitive interactions, there is an inverse relationship between fungal species number and decomposition. Wicklow and Yocom (198 1) measured mass loss of rabbit feces by six species of coprophilous fungi growing singly or in combinations. They found that as species number increased, decomposition declined by 4.6%. The same result was obtained earlier by Norman (1930) who measured heat produced by Aspergillus, Trichoderma, and an actinomycete species growing singly and in combinations in a thermos. Similarly, in the field, Coates and Rayner (1985) compared decomposition of beech logs that were naturally colonized by saprophytic fungi, inoculated with four strong competitors, or recut to increase the number of colonizing species. Logs with the most species were least decomposed. Early in saprophytic succession microarthropods are strong competitors of fungi, and control fungal distribution and abundance by selective grazing


7

and carrying inoculum. In addition, microarthropods benefit from the resources not utilized by competing fungi. Due to competition, unoccupied zones of substrate are left between those occupied by fungi, and these may be used by microarthropods. There are two suggestive examples involving fly larvae. Boddy et a/. (1983) found that unoccupied zones of agar between competing basidiomycetes and ascomycetes were colonized by fungus gnat larvae (Bradysiu sp.). Using coprophilous fungal species combinations in rabbit feces, Lussenhop and Wicklow (1985) found that as the number of fungal species increased, the numbers of fungus gnat larvae (Lycoriella mali) increased. They interpreted this to mean that as numbers of fungal species increased, there was more unoccupied space between competing fungi available to the larvae. Since much of the fecal material was easily digestible, larval numbers increased as number of fungal species increased. In saprophytic successions, later-appearing fungi are stronger competitors of microarthropods than early species. In addition to sometimes presenting an impenetrable weft of mycelia (Binns, 1980), many late successional species are defended against herbivores. For example, the coprophilous fungus Chuetomium bostrycodes disperses spores relatively slowly from terminal hairs on perithecia. C . bostrycodes has lacerate terminal hairs on its perithecia that prevent grazing. Chaetomium species also produce chemical defenses (anthraquinones and chaetomin) (Wicklow, 1979).

B. Foraging Understanding the grazing interactions between microarthropods and fungi will require knowledge of the foraging behaviour of both groups. Fungi forage by varying growth patterns from diffuse, perennial networks to shortlived colonies, and by rhizomorphs. Dowson et al. (1988) offered baits to cord-forming basidiomycetes and demonstrated that Steccherinum fimbriatum switched growth pattern from slow-diffuse to fast-effuse exploration after contact with bait. Other basidiomycete species had longer-range foraging patterns. Foraging behavior of the hyphomycete Mortierellu isubelfina was shown to change in response to grazing by the collembolan Onychiurus armatus. Hedlund et al. (1991) showed that grazing caused slowgrowing appressed hyphae to switch to non-sporulating aerial hyphae. Foraging strategy and ability to respond to chemical cues are important for microarthropods. Streit and Reutimann et al. (1983) showed alternation between a searching and feeding mode of foraging using a surface-dwelling oribatid that was offered colonies of six different micro-organisms in petri dish experiments. Bengtsson et a/. (1988) found that the collembolan Onychiurus armatus was attracted to Mortierella isabellina and Penicillium spinulosum by odors.

8

J. LUSSENHOP

C. Microarthropods as Food of Bacteria and Fungi Microarthropods are surrounded by spores and conidia many of which can, if they lodge on the integument, germinate and grow into the animal, eventually killing it (Evans, 1988). These include specialized entomopathogenic species such as Acremonium sp., Beauveria bassiana, Conidiobolus coronatus, Metarrhizium anisopliae, and Verticillium lecanii (Domsch et a/., 1980; Keller and Zimmerman, 1989), as well as facultative pathogens such as Aspergillus frclvus and species of Fusarium. The impact of entomopathogenic fungi on natural populations of microarthropods is unknown. Purrini (1983) found only 0.7% of the collembola in European forests were infected with fungi; another 0.7% were infected with bacteria, and 2% with microsporidia. In the same study, Purrini and Bukva (1984) found that among oribatids, fungal and protozoan infections increased considerably in areas receiving high sulfur dioxide fallout. Microarthropods may be of great importance as vectors of the approximately 13 species of specialized entomopathogenic fungi that attack holometabolous insects. By using a Berlese funnel to force microarthropods to move through inoculated soil, Zimmerman and Bode (1983) showed that collembola and mites transport spores of Metarrhizium anisopliae. Adaptations to avoid touching the medium, and to prevent spore lodging, are important defenses against entomopathogenic fungi (Rawlins, 1984). This is because spores or conidia of entomopathogenic species germinate upon contact with arthropod cuticle. It may be no accident that 24% of collembola, and 40-56% of oribatids listed in Table 1 carried no inoculum. Further defensive adaptations include cuticular melanin which is believed to be toxic to fungi (Charnley, 1984), and fungitoxic secretions. The sex pheromone of the stored product mite, Caloglyphus polyphyllae is fungitoxic (Kuwahara et al., 1989). Collembola are flexible and are able to remove surface spores. The elaborate cuticular sculpture and setation of euedaphic collembola may be an adaptation to minimize contact with fungi.

D. Bacteria and Fungi as Food of Microarthropods A model for soil microarthropod grazing on saprophytic fungal colonies comes from observations of stream invertebrates grazing on leaves. Stream invertebrates selectively graze portions of leaves with fungal colonies (Barlocher, 1980; Arsuffi and Suberkropp, 1985). Similarly, isopods (Oniscus asellus) feed on pockets of mycelium of the leaf pathogen Rhytisma acerinum Fr. on maple leaves (Gunnarsson, 1987). It is likely that microarthropods selectively graze soil fungi in the same way. There is evidence that resource partitioning among microarthropods results in small species and juveniles grazing bacteria, and larger individuals grazing fungi (Bakonyi, 1989).

MECHANISMS OF MICROARTHROPOD-MICROBIAL

INTERACTIONS IN SOIL

9

Table 1 Numbers of fungal propagules carried by microarthropods Habitat/group Arctic and Subarctic Acari: Oribatida L. F, H horizons in aspen woodland Collembola Onychiurus subtenuis

L, F, H horizons in beech-maple woods Acari: Oribatida Collembola Diplopoda Coleoptera Staphylinidae

Number of fungal % Individuals species carried without inoculum 1.4

40

Reference Behan and Hill ( 1 978) Visser (1985)

2.4

ND"

Number of fungal genera carried 0.5 1.2 1.3

56 24 19

1 -4

14

Pherson and Beattie ( 1979)

N D= not determined.

Microarthropod grazing intensity is strong enough to control abundance and distribution of fungi. In early fall, ascospores of the saprophytic fungus Coniochaeta nepalica are briefly common in soil of the oak-birch forest in New York; Gochenaur (1987) recorded an 80% decline in frequency of C . nepalica spores during fall. Gochenaur (1987) placed ascospores of C. nepalica as well as Sordariajimicola in the A horizon on membrane filters and found that they disappeared at a rate of 60% per day. Since microarthropod fecal pellets accumulated on the filters at a similar rate, Gochenaur (1987) concluded that microarthropod feeding was responsible. In a second example, microarthropod feeding limited production of primary infective inoculum of two pathogens of black walnut (Juglans nigra): Mycosphaerella juglandis which causes mycosphaerella leaf spot, and Gnomonia leptostyla which causes walnut anthracnose. The primary inoculum of both fungi is produced by perithecia on fallen leaves. Kessler (1990) found that when perithecia-bearing walnut leaves fell into heavy leaf litter supporting microarthropod populations, the perithecia were eaten, primarily by collembola. Leaves falling into grassy areas with poor litter and low microarthropod populations were not subjected to intense grazing, and in these habitats walnut trees became infected the next year. Collembolan grazing controlled the vertical distribution of two perennial basidiomycetes in the litter of a 32-year-old Sitka spruce (Picea sitchensis) plantation in England. Newell (1984a,b) studied the two basidiomycetes that produced over 99% of the sporocarps at the site. Sporocarp depths showed

10

J. LUSSENHOP

that Marasmius androsaceus occurred naturally in the L horizon, and Mycena galopus in the F horizon. Newell (l984a) showed that the collemboIan Onychiurus latus preferred Marasmius androsaceus to Mycena galopus in laboratory feeding trials. When numbers of 0. l a m were experimentally increased in the field, density of M . androsaceus declined (Newell, 1984b). Because the competitively inferior fungus was the best decomposer, limitation of its distribution to the L horizon resulted in slower decomposition (Newell, 1984b). Some sclerotia are chemically protected (Wicklow, 1988) and collembola will graze on their conidial apparati but not on the sclerotia themselves (Aspergillusjavus; Lussenhop, personal observation). In other cases (Sclerotinia sclerotiorum) collembola apparently eat sclerotia in the field (Anas and Reeleder, 1987).

E. Fungal and Bacterial Response to Grazing 1 . Eflects of Grazing on Decomposition Microarthropod activity favors growth of bacteria, probably by mixing cells with fresh substrate. Even if microarthropods do not graze fungi, their activity may break hyphae just by walking through them (Lussenhop, personal observation; J. C . Moore, personal communication). Hanlon and Anderson (1 979) inoculated leached oak leaves with the basidiomycete Coriolus versicolor and added 0, 5, 10, or 20 collembola (Folsomia candida). Bacterial biomass exceeded fungal biomass when 10 or more collembola were present. The same results were obtained in a field experiment by Lussenhop et al. (1980). They found that beetle and/or fly larvae in cattle dung were associated with increases in bacteria and decreases in fungi even though mouthparts of the beetle and fly larvae made it impossible for them to ingest fungal hyphae. The possibility that invertebrate grazing stimulates fungal growth was suggested when the minor contribution of arthropods to soil respiration was recognized (Macfadyen, 1961). Such stimulation could occur as a result of what is called compensatory growth in studies of plant response to grazing (reviewed by Belsky, 1986). Compensatory growth is increased productivity or mass relative to a control due to grazing. Possible mechanisms include (a) fungal growth after senescent hyphae are grazed, and (b) regrowth after periodic grazing of actively growing mycelia. Periodic grazing is the mechanism associated with experiments showing compensatory response of fungi in Table 2. Bengtsson and Rundgren (1983) modeled what may happen in nature by alternating 2-day grazing bouts with 5-day growth periods; this increased fungal CO, output by about 5 % relative to ungrazed controls. In a more realistic physical setting, Bengtsson et al.



II

Table 2 Compensatory growth of micro-organisms in response to microarthropod grazing

Fungal species Laboratory Soil dilution Botrytis cinerea Coriolus versicolor Mortierella isabellina Vert icillium bulbillosum Penicillium spinulosum Millipede faecal flora Field Soil dilution

a

Fob[somiaJimetaria F. candida F. candidu

~

-/+h -a

+

Reference Andren and Schnurer (1985) Hanlon (198 1a) Hanlon and Anderson (1979) Bengtsson and Rundgren (1983)

Ony ch iurus armatus 0. armatus

+

Bengtsson et al. (unpublished)

0 . armatus

+

Bengtsson et al. (unpublished)

0. quadr iocella tus

+"

Drift and Jansen (1977)

+ a.c

Addison and Parkinson (1978)

+ a.c

Addison and Parkinson ( 1 978)

Hypogastrura tullbergi Folsomia regularis

Soil dilution ~

Growth relative to Arthropod species controls

~~

Bacteria were present. Increase with fungi grown on high nutrient medium, otherwise decrease. In the less severe of the two field sites on Devon Island.

(unpublished) connected fungal colonies with tubing so that collembola could move from one colony to another: this resulted in periodic grazing and compensatory growth which increased CO, output by 4-5 times. Laboratory experiments listed in Table 2 as not showing compensatory growth had constant, relatively intense grazing by individuals belonging to species of Folsomia which tend to be larger than Onychiurus individuals. In addition, presence of bacteria may have affected the results in many of the experiments. The stimulating effect of microarthropods on fungal and bacterial growth effects nutrient transformation. The litter-inhabiting collembolan, Tomocerus minor, was associated with nitrogen immobilization in litter but with nitrogen mobilization in the fermentation layer by stimulating fungal growth in the different nutrient regimes (Verhoef et ul., 1989). Both T . minor and an isopod, Philosciu muscorum, in microcosms containing pine litter increased CO, output and exchangable phosphate, but only T . minor increased dehydrogenase, cellulase activity, and nitrate concentration, due to the collembolan's greater stimulation of microbial activity (Teuben and Roelofsma, 1990).

12

J. LUSSENHOP

2. Eflects of Grazing on Fungal Species Numbers Wicklow and Yocom (1982) showed that the number of species of coprophilous fungi on rabbit feces declined as the density of larvae of the sciarid fly, Lycoriella mali, increased. Whether the reduced species number was a result of grazing favoring competitive dominants, or of reversing the competitive superiority of competitive inferiors is not known. Collembolan grazing reversed the outcome of competition between two basidiomycetes studied by Newell (1 984a, b). In contrast, collembolan grazing favored a competitively superior fungus in Parkinson et al.’s (1979) study of two saprophytic fungi growing in aspen leaves when snow was melting. They isolated a competitively inferior, sterile, dark fungus that was grazed by the collembolan Onychiurus subtenius, and a competitively superior basidiomycete in whose presence in culture 0. subtenius died. They showed that collembolan grazing reinforced the competitive effects of the basidiomycete. Whittaker (1981) confirmed these interactions in the field.

F. Microarthropod Digestion Microarthropod habitats are rich in micro-organisms, microbial exoenzymes, and products of microbial degradation. For this reason ingestion of a variety of microbially conditioned materials and trituration of food materials may be the most important digestive adaptations of microarthropods. Mouthparts of oribatids (Phthiracarus sp.: Dinsdale, 1974b), and collembola (Tomocerus longicornis: Manton, 1977) function to minimize the size of food particles; this probably enhances activity of microbial and endogenous enzymes in the gut, and contributes in a minor way to comminution. Gut micro-organisms of microarthropods are derived from the microorganisms they ingest (Seniczak and Stefaniak; 1978; Haq and Konikkara, 1988). The particular microbial species present in the gut effect time to maturity and number of eggs laid in oribatids (Stefaniak and Seniczak, 1981). It is not surprising that collembola in culture can select hyphae with the highest nutrient content (Leonard, 1984; Amelsvoort and Usher, 1989), and that collembola produce more eggs when fed on fungi with higher nitrogen content (Booth and Anderson, 1979). Presence of fungi in microarthropod guts is associated with cellulases, while bacteria are associated with proteases, amylases, and chitinases (Stefaniak and Seniczak, 1981). Borkott and Insam (1990) presented evidence that chitinolytic bacteria and Folsomia candida have a mutualistic relationship. They fed F. candida microbially conditioned or unconditioned chitin, with and without antibiotics: the collembola gained the most mass on microbially conditioned chitin without antibiotics; numbers of chitinolytic bacteria were


13

greater in feces than in food. Although some microarthropods are believed to be bacterivores, two polyphagous collembola (Proisotoma minuta, Hypogastrura tullhergi) did not survive on diets of any of seven soil bacteria isolated from their habitat (Harasymek and Sinha, 1974). Microarthropods may facilitate the activity of fungal enzymes in their guts by maintaining basic pH, but this is poorly documented. If the basic gut pH ascribed to oribatids (Dinsdale, 1974a; Seniczak and Stefaniak, 1978) is general, then they may be similar to the sporocarp-inhabiting beetles studied by Martin (1987). Martin (1987) described a series of adaptations allowing arthropods to benefit from ingested fungal enzymes in digestion of plant structural carbohydrates. The adaptations range from (a) favoring activity of fungal enzymes by basic gut pH as illustrated by sporocarp-inhabiting beetles, to (b) transport and inoculation of wood-decomposing fungi as well as maintaining favorable gut conditions for their enzymes by siricid wood wasps and scolytid beetles, to (c) culture of fungi whose enzymes will be used in digestion by attine ants or harvesting termites. Microarthropods may have additional adaptations for benefiting from microbial enzymes. For example some collembola ingest clay to which bacterial enzymes are adsorbed. Kilbertus and Vannier (1981) showed that a cavernicolous collembolan lost mass without a dietary source of clay, and that clay was associated with bacterial cells in the gut. Touchot et al. (1983) later showed that dietary clay was important to the collembolan Folsomia candida, possibly because phenolic compounds were adsorbed to clay surfaces and did not inhibit bacterial activity.

G. Microarthropod Excreta The possibility that microarthropods return significant amounts of mineral nutrients in urine and feces was raised by Verhoef et al. ( 1 988). They fed the collembolan Tomocerus minor a diet of laboratory-grown hyphae, and estimated that 50% of the dietary nitrogen was released as urea, and that the nitrogen concentration of fecal pellets was 56% higher than the hyphae. In nature, the contribution of microarthropod urine to mineral pools may be significant but has not yet been quantified. Most experiments with soil arthropod fecal pellets were done with those of macroarthropods. Conclusions from experiments with millipede and isopod fecal pellets are that (a) bacterial activity is favored in fecal pellets due to the small size of particles (Webb, 1977; Hanlon, 1981b), and by gut conditions (Reyes and Tiedje, 1976; Anderson and Bignell, 1980), but that (b) fecal material does not decompose faster than uneaten material (Nicholson et al., 1966). These conclusions are supported by Grossbard’s ( 1 969) experiment showing that fecal pellets of oribatid mites fed I4Clabeled grass decomposed at the same rate as uningested grass.

14

J. LUSSENHOP

The possibility that microarthropod fecal pellets contribute to the formation of water-stable soil aggregates is of considerable interest. Tisdall and Oades (1982) pointed out that the smallest aggregates are formed from mineral particles held together by physical forces, but as smaller aggregates combine into larger, the importance of biological binding agents increases. In Tisdall and Oades’ (1 982) scheme, aggregates > 2000 pm are formed from aggregates between 20 and 250 pm in diameter and are held together by microbial- and plant-derived polysaccharides, as well as by fibrous plant roots and fungal hyphae, particularly those of vesicular-arbuscular mycorrhizal fungi. Since microarthropod fecal pellets are 30-90 pm in diameter (Rusek, 1975), it is not hard to imagine them forming nuclei of soil aggregates.

H. Dispersal Bacterial and fungal spores are dispersed through soil by physical mechanisms, but microarthropods modify natural distribution patterns by dispersing propagules from concentrations around sites of sporulation. In litter, fungal spores and bacteria are dispersed horizontally and vertically by the spreading pressure of monolayer-forming substances on aqueous films (Bandoni and Koske, 1974). Wettable surfaces of spores of some conidial fungi allow them to be moved a few millimeters by advancing water fronts (Hepple, 1960). Finally, hyphal growth, particularly along roots, is extensive enough to maintain propagules throughout soil. Microarthropod ingestion damages fungal spores, but the small fraction that survives is probably important (Table 3). Pherson (1980) speculated that some fungi are adapted for dispersal by microarthropods. He found that viable spores of Alternaria, Epicoccum, and Penicillium were most frequent in feces of litter microarthropods. When microarthropods were excluded from sterile leaf discs by 5-pm mesh bags, colonies of these three genera were significantly less frequent than other fungal genera compared with control disks in 500-pm mesh bags incubated in the F layer of a Michigan beechmaple forest. In their study of grazing selectivity, Moore et al. (1987) found that by sporulating quickly, Penicillium citrinum had more spores eaten and dispersed than other species in the study. Dispersal of microbial propagules by microarthropods appears to be passive, and thus a number of simple patterns exist:

(i) Microarthropods carry more propagules and species in litter than in mineral soil (Visser, 1985). (ii) Body-size is proportional to number of fungal genera carried (Table 1 : Pherson and Beattie, 1979). (iii) Aggregations of spores at sporulation sites are dispersed rapidly by microarthropods (Lussenhop and Wicklow, 1984). Visser et al. ( 1 981)


15

Table 3 Per cent survival of fungal propagules ingested by microarthropods and macroarthropods

Microarthropod species

Fungal species

Laboratory Collembola Entomobrya purpurascens Pseudosinella alba

Penicilliurn sp.

Onychiurus quadrocellatus

%Faecal pellets with viable propagules

Reference

2 (YOof spores) Cervek (1971)

11 species

Cladosporium sp.

2-25

Ponge and Charpentie (1981)

13

Drift (1965)

(control = 83) Acarina: Astigmata Rhizoglyphus echinopus Caloglyphus sp.

Vert icillium albo-atrum conidia microsclerotia Pythium myriotylum

Price (1976) 94 57-86 90

Field Collem bola Onychiurus subtenuis Aspen woodland Arctic soils Acarina: Oribatei microarthropods Oak-birch forest

50 13

8-30

Shew and Beute ( 1 979)

Visser (1985) Behan and Hill ( 1 978) Gochenaur (1987)

suggest that microarthropods bring fresh inoculum to sites they have grazed, with the overall effect of increasing nutrient immobilization.

I. Summary for the Saprophytic System Five mechanisms of interaction between microarthropods and micro-organisms occur in saprophytic systems. Two mechanisms affect distribution and abundance of fungi; three affect bacterial and fungal metabolic activity. Two mechanisms by which microarthropods affect fungal distribution and abundance are selective grazing and dispersal of fungal propagules: (i) Control of fungal species distribution by selective grazing is well supported by field observation and experiment (Parkinson et al., 1979; Whittaker, 1981; Newell, 1984a,b; Gochenaur, 1987; Kessler, 1990). However, generalizations as to effects of selective grazing cannot be

16

J . LUSSENHOP

drawn yet. If microarthropods always selectively grazed the competitively dominant fungus, decomposition would be slowed. But this only happened in Newell’s (1984a,b) study; in the study by Parkinson et a/. (1 979) the opposite occurred, and decomposition probably increased. (ii) Dispersal of fungal propagules seems particularly important early in saprophytic succession when it may increase the rate of decomposition. Cultural methods used to assess fungi associated with microarthropods lead to an underestimate of total fungal species numbers, and an overestimate of the importance of fast growing fungal species. Studies listed in Tables 1 and 3 have not quantified numbers of propagules carried by microarthropods, only numbers of different species or genera carried. A more appropriate cultural technique would be dilution plating of individual microarthropods on media that retard colony spread; this would give numbers of propagules carried per individual. Four mechanisms affect metabolic activity of micro-organisms: (i) Direct return of mineral nutrients in urine and feces has not been quantified, but is potentially an important mechanism stimulating microbial growth (Verhoef et a/., 1988). (ii) Bacterial growth is briefly stimulated by mixing and comminution of microarthropods. It is likely that interference with fungal growth indirectly benefits bacteria. The disturbance of cultivation favors bacteria in the same way though on a much larger scale (Hendrix et a/., 1986). (iii) Compensatory growth of fungi in response to episodic microarthropod grazing increases the decomposition rate above what it would be without grazing. Compensatory growth is likely to be important in the field, and is likely to be associated with nutrient immobilization by fungi. Compensatory growth has only been demonstrated in laboratory experiments designed to mimic episodic grazing; careful observation of grazing in situ is needed to substantiate this as an important mechanism. (iv) Decomposition rate is inversely proportional to fungal species number in the absence of microarthropods, because by competing for volume of substrate, fungi slow each other’s growth rates. Invertebrates thus increase decomposition rate by reducing competitive stasis among fungi. The effect increased decomposition rate by about 5% in laboratory studies.

In nature bouts of grazing would involve all of these mechanisms. Selective grazing by a microarthropod would add mineral nutrients, reduce fungal competition, stimulate bacterial growth and disperse fungal propagules (Fig.


17

2). Frequency of grazing bouts would determine whether compensatory growth occurred. The importance of each mechanism will change during saprophytic succession. With newly fallen leaves, introduction of fungal inoculum, selective grazing, and stimulation of bacteria by microarthropods are likely to be the most important mechanisms. As leaves age and enter the fermentation layer, compensatory growth response to microarthropod grazing and the mineral nutrients in excreta are likely to be important. Finally, as leaf fragments enter the humus layer, selective grazing and release of fungi from competitive stasis will be important. These mechanisms predict that microarthropods will stimulate fungal growth and magnify effects fungi have on limiting nutrients. In an immobilizing environment such as leaf litter, microarthropods should stimulate fungal growth which will reduce mineral nutrient concentrations of limiting nutrients. Lower in the soil horizons, in a mobilizing environment such as humus, microarthropods should stimulate fungal growth which will increase mineral nutrient concentration. An example is the decrease in ammonium-N in the L layer and the increase in ammonium-N in the F layer of a relatively lownutrient Pinus nigra forest caused by Tomocerus minor in microcosms (Verhoef et al., 1989). A second example is the increased inorganic-N concentration in response to reduced fungivores and reduced hyphal lengths in a Pinus contorta forest soil experimentally manipulated with biocides by Ingham et al. (1989). This pattern is not predictable, however, for even within the same study other variables affect the link between microarthropod stimulation of micro-organisms and nutrient mineralization. These additional variables include overgrazing, soil nutrient concentration, and numbers of bacteria relative to fungi.

V. MICROARTHROPOD-MICROBIAL INTERACTIONS IN THE RHIZOSPHERE Microarthropods interact with three groups of micro-organisms in the rhizosphere. These three groups-saprophytic and pathogenic bacteria and fungi, vesicular-arbuscular mycorrhizal fungi (VAM), and ectomycorrhizal fungi (ECM)-have distinct biologies and life histories, hence microarthropods interact differently with each (Fig. 3).

A. Saprophyte-Pathogen-Microarthropod Interactions Bacterial and fungal numbers are orders of magnitude higher around roots than in soil away from roots (Curl and Truelove, 1986). Microarthropod density is also higher around roots, though core sampling methods have

18

I. LUSSENHOP

FUNGI COLONIZE SUBSTRATE, OU TCO MPET E BACTERIA

FUNGAL GROWTH SLOWS DUE TO INTENSE COMPETITION AMONG FUNGI

GRAZING MICROARTHROPODS DESTROY COMPETING HYPHAL NETWORKS, ADD NUTRIENTS IN EXCRETA

BACTER AL POPULATIONS INCREASE

NEW FUNGAL SPECIES DISPERSED BY MICROARTHROPODS OUTCOMPETE BACTERIA

Fig. 2. Flow chart showing effects of microarthropod grazing on saprophytic micro-organisms.


19

A. NEMATODES

t PROTOZOA

t

BACTERIA

FUNGI

f

A \ EXUDATE

6.

DEAD CORTICAL CELLS

SLOUGHED

TISSUE

C.

Fig. 3. Three rhizosphere models based on Fogel (1991):A, Bacterial-based foodweb at root tip, and fungal-based foodweb along mature root; B, vesicular-arbuscular mycorrhiza; C, endomycorrhiza.

made this difficult to show. Curry and Ganley (1977) identified roots of pasture plants in soil cores and showed that grass roots were associated with higher microarthropod numbers, but could not distinguish rhizosphere from non-rhizosphere populations. Core samples collected in grid patterns between Picea abies trees showed highest collembola numbers in areas with the greatest density of fine, mycorrhizal roots (Poole, 1964). Wiggins et al. (1979) took 2.2- cm core samples next to and 20 cm away from tap roots of cotton plants in the field; they found statistically higher rhizosphere collembola densities, and a suggestion that the rhizosphere effect was greater in fertilized than in unfertilized soil. In pots, Wiggins et al. (1979) found an

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increase of 13 collembola for every gram of root mass, and that collembola aggregated around roots as the soil dried. Spatial relationships of microarthropods with roots can be directly observed in rhizotrons, minirhizotrons (Snider et al., 1990), borescopes, and behind glass plates sunk in the soil (Bohm, 1979). Microarthropod groups observed in a rhizotron in a mixed deciduous forest in Michigan were at least two orders of magnitude more dense on roots than in soil (Lussenhop et al., 1991). Microarthropods carry fungal and probably bacterial inoculum to roots. Collembola from Alabama cotton fields carried nine genera of fungi including Aspergillus, Fusarium, Verticillium (Wiggins and Curl, 1979). In laboratory experiments, collembola (Proisotoma minuta and Onychiurus encarpatus) transported fungal spores and bacteria through sterile soil to cotton seedling roots (Wiggins and Curl, 1979). Astigmatid mites (Rhizoglyphus sp.) carried Aspergillus J a w s to peanuts (Aucamp, 1969), and Verticillium alboatrum to bulbs (Price, 1976) and another astigmatid mite species (Caloglyphus micheali) transported Pythium myriotylum to peanuts (Shew and Beute, 1979). In an important and revealing part of their review, Beute and Benson (1979) showed that transport of pathogen inoculum to roots increases disease. Wounding of roots would still further increase disease, although it is not likely that microarthropods eat healthy tissue (Kooistra, 1964). Microarthropod grazing in the rhizosphere has a much more beneficial effect than dispersal of inoculum. This is because pathogenic fungi apparently lack antiherbivore defenses that saprophytic species have, and collembola prefer grazing pathogens (Curl et al., 1983; Lartey et al., 1989). Mankau and Mankau (1963) similarly found that the nematode Aphelenchus avenue had the strongest affect on pathogenic fungi. In petri dish experiments, Curl (1979) showed that both Proisotoma minuta and Onychiurus encarpatus preferred Rhizoctonia solani over Trichoderma harzianum. They ate the latter only when young. In pots containing R . solani-infested soil, presence of P . minuta and 0. encarpatus was associated with emergence of 58-83% more cotton seedlings, depending on collembolan density. Ulber (1983) obtained similar results, and in addition showed in pot experiments that sugar beet survival could be increased by 45% by adding Onychiurus j m a t u s to soil contaminated with Pythium ultimum 20 days before planting. The possibility that microbial-invertebrate interactions in the rhizosphere might contribute to nitrogen mineralization and its uptake by roots was demonstrated in a series of microcosm experiments performed by Coleman and his associates using bacteria, amoebae, nematodes, and blue grama grass (Bouteloua gracilis) (Coleman et al., 1978; Elliot et al., 1979). Mineral nitrogen was released from excreta of bacterivorous nematodes and amoebae, as well as from bacteria due to disturbance by the nematodes and amoebae. When Ingham et al. (1985) reported results of more extensive


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microcosm experiments, they listed 17 studies associating nitrogen or phosphorus mineralization with amoebal or nematode bacterivory. In the field, Clarholm (1989) estimated that amoebal grazing contributed 1-17% of the nitrogen taken up by barley. Microarthropods have not been shown to increase mineralization in the rhizosphere as have bacterivorous protozoa and nematodes. This may be due to the association of microarthropods with the fungal-based food web that develops along older root segments behind the bacterial-based protozoan, nematode food web (Fig. 3A). Most microarthropods feed on suberized portions of roots, behind the nutrient-absorbing region (Lussenhop, personal observation of mixed deciduous forest tree and herb roots). Further, Wright and Coleman (1988) suggested that rhizosphere fungi are net mineralizers, and that fungivores decreased mineralization in microcosms they studied. Wright and Coleman (1988) used intact cores of field soil, applied factorial combinations of biocides to reduce densities of fungi, nematodes, arthropods, and mesofauna, and then planted Sorghum hicolor in the cores. Neither sorghum nutrient concentration or mass was raised by any invertebrate group, including microarthropods. Setala and Huhta (I99 1) increased mass and nitrogen concentration of birch (Betula pendula) seedlings by adding all groups of soil fauna to microcosms. They did not test microarthropods separately, and it is possible that microarthropods were not responsible for the improved seedling growth.

B. Vesicular-Arbuscular Mycorrhizal-Microarthropod Interactions As fungivores, microarthropods strongly affect all aspects of mycorrhizal growth and functioning, except dispersal. VAM spores and chlamydospores are too large to be dispersed by microarthropods; they are dispersed by wind (Warner et al., 1987), and macroarthropods (Rabatin and Rhodes, 1982). VAM spores, their germination tubes, and extramatrical hyphae are vulnerable to microarthropods. Collembola eat spores of some VAM species. Moore et al. (1985) showed that the collembolan Folsomia candida ate spores of Gigaspora margarita, but not spores of Gigasporafasciculatum or Glomus mosseae, in petri dish feeding trials. Mycorrhizas are established by germ tubes that grow from spores each time soil is moistened, and these germ tubes are susceptible to grazing (Koske, 1981). Grazing of germ tubes may be the reason Kaiser and Lussenhop (1991) found that F. candida reduced the number of infection sites if added to pots when soybeans (Glycine max) were planted, but not if the collembola were added 15 days after planting. Collembolan selectivity in grazing VAM hyphae was shown in Moore et al.’s (1985) petri dish experiments. Four species of collembola (F. candida,

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Onychiurus encarpatus, 0 .folsomi, and Proisotoma minuta) ate Gigaspora rosea hyphae. None ate G . mosseae hyphae, and only F. candida ate Glomus fasciculatum. Collembolan grazing of extramatrical hyphae reduces mycorrhizal benefits to plants, but the effect of collembolan grazing is least at intermediate densities of collembola. Warnock et al. (1982) demonstrated the response of collembolan populations to extramatrical hyphae. They added F. candida to pots with leeks (Allium porrum) and the mycobiont Glomus.fasiculatus. In the presence of collembola, mycorrhizal leeks weighed 50% less and contained 55% less phosphorus than mycorrhizal controls after 12 weeks. Collembola populations increased more in pots with mycorrhizal leeks and more individual collembola were observed with hyphae in their guts in these pots. Finlay (1985) grew leeks in pots with a range of densities of the collembolan Onychiurus ambulans. He found that collembola lowered the beneficial effect of mycorrhizal fungi, but that they had the least effect at intermediate densities. A similar compensatory response to collembola at intermediate densities was also observed by Harris and Boerner (1990) who added F. candida to pots containing Geranium robertianum and the endophyte Glomus fasicula tum . Collembola reduce the benefits of mycorrhizal infection to plants in the field. Finlay (1985) grew Trifolium pratense in field plots using chlorfenvinphos to reduce indigenous collembolan density, and benomyl to reduce infection by the mycobiont Glomus occultus. He found that reduced collembolan density was associated with the highest shoot mass and shoot phosphorus. By sampling four times during the experiment he showed that phosphorus accumulation per shoot mass was highest in treatments where collembolan density was lowest. Similarly, McGonigle and Fitter (1987) found that a two-thirds reduction in collembolan numbers was associated with higher phosphorus concentration in the grass Holcus lanatus. The impact of microarthropods on VAM is likely to be small in highly fertilized agricultural systems. But the literature just reviewed shows that microarthropods decrease benefits of VAM both in natural habitats where VAM may benefit members of plant populations locally or during brief periods (Fitter, 1986), and in low-input agriculture where soil phosphorus levels are low.

C. Ectomycorrhizal-Microarthropod Interactions The rhizosphere of short, ectomycorrhizal roots is controlled by the mycobiont. Ectomycorrhizal short roots are covered by the fungal mantle; they have no epidermis or root hairs, and have a reduced meristematic zone (Fig. 3C). Exudates and sloughed tissue from these short roots are fungal. Protection from herbivory may be very important for ECM fungi because


23

they can be perennial, and food reserves and phosphorus are stored in the mantle. Aphid and nematode feeding on ECM in the field was reviewed by Fogel (1988). There are no observations of microarthropods feeding on ECM in nature. In culture, protura feed on ECM fungi (Sturm, 1959). Shaw (1988) allowed the collembolan Onychiurus armatus to choose between agar plugs of 12 ECM fungi, and found a consistent hierarchy of preference. The least preferred ECM fungi were those with sporocarps toxic to 0. armatus. Other ECM fungi, such as Coenococcum geophilum, may be physically protected by thick-walled, knobby, melanic hyphae. Some ectomycorrhizas form mats of hyphae large enough to alter soil chemistry and biology. For example, hyphal density is 2.5 times greater in mats of Hysterangium setchellii than outside (Cromack et al., 1988) Calcium availability may be especially increased within mats. Many fungi produce oxalic acid as a waste product that forms crystals of calcium oxalate on hyphae and ectomycorrhizal mantles (Malajczuk and Cromack, 1982). Cromack et al. (1977) suggested that calcium oxalate is a source of calcium for soil biota, and that it may be broken down by micro-organisms in guts of arthropods including collembola (Sinella sp.) and oribatids (Pelopoidea sp.). Among microarthropods, calcium is especially important for oribatids; three groups of ptychoid oritabids harden their cuticle with calcium oxalate probably obtained from fungal hyphae (Norton and Behan-Pelletier, 1991). Comparing H . setchellii mat soil with adjacent soil, Cromack et al. (1988) found higher exchangeable calcium, organic nitrogen, and carbon as well as 3.2 times more oribatids. and 2.6 times more collembola.

D. Summary for Rhizosphere In the rhizosphere, microarthropods have their primary effect on microorganisms through dispersal and selective grazing. Microarthropods selectively graze pathogens in the rhizosphere. But they also move pathogens and saprophytes alike to root surfaces. In the future it will be important to know the net effect of these two activities. Beneficial bacteria such as plant-growth promoting rhizobacteria and rhizobia could be vectored to root surfaces as well as pathogens. Additional mechanisms of interaction between microarthropods and microorganisms and/or roots probably exist and would help explain Edwards and Lofty’s (1978) field experiment showing that the presence of arthropods (micro- and macroarthropods) leads to the production of greater root mass. They fumigated soil monoliths from fields cropped to cereals, planted barley in each, and added back natural densities of arthropods (microarthropods plus millipedes, insect larvae, etc.), and earthworms. Both earthworms and arthropods were associated with higher seed germination (relative to controls). In addition, arthropods were associated

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with the largest root mass: 1.2 times that associated with earthworms, 2.3 times fumigated controls, and only 0.8 times the root mass of unfumigated, ploughed soil.

VI. CONCLUSIONS Microarthropods control the distribution and abundance of fungi in soil, and they also stimulate microbial metabolic activity, thereby amplifying microbial immobilization or mineralization of nutrients. It is possible that microarthropods may be important as vectors of entomopathogenic fungi to holometabolous insects. Chemical interactions among the soil biota are probably extensive, yet are poorly known. In soils where fungi dominate there are six mechanisms of interaction with microarthropods. Litter microarthropod species selectively graze and disperse fungi. Deeper in the horizon, the same microarthropod species may stimulate bacterial activity; by grazing fungi they may control species occurrence, cause compensatory growth, and allow increased growth by disrupting competing hyphal networks and adding mineral nutrients in urine and feces. These stimulating effects on microbial growth will affect mineral nutrient concentrations in soil. If periods of plant nutrient uptake are synchronized with microbial immobilization or mobilization of nutrients, plant growth could be affected. The same microarthropod species may move inoculum to roots, and preferentially graze fungal pathogens. In soils dominated by bacterial foodwebs, e.g. agricultural soils, stimulation of bacterial activity and dispersal of bacteria by microarthropods are likely to be important, but there is much less information on microarthropod interactions with bacteria than with fungi. There is also little information on arid soils where prostigmatid mites may be important, or late in succession where oribatid mites may be important. A major obstacle to understanding how microarthropods and microorganisms interact is lack of spatiotemporal information. In the present chapter analogies with aquatic, coprophilous, and wood-decomposer systems were used to gain insight. But analogies are not sufficient for the saprophytic system and inappropriate for the rhizosphere, hence the need for new observation methods including direct observation with borescopes, minirhizotrons, and rhizotrons. None of the mechanisms reviewed is well quantified. In the future the effects of these mechanisms should be incorporated into regression and simulation models of soil microbial processes. Anderson er al. (1985) used temperature and arthropod density to predict nitrogen mineralization rate. Regression models might incorporate the mechanisms discussed in the present chapter to relate microarthropod density in the rhizosphere to the

MECHANISMS OF MICROARTHROPOD-MICROBIAL INTERACTIONSI N SOIL

25

number of rhizoplane pathogen colonies, or to VAM benefits to plants in the field. Simulation models of soil foodwebs might include responses to microarthropods. The simulation model of Hunt et a/. (1987) includes density-dependent control of microbial growth, thus roughly incorporating the retarding effect of fungal species number on decomposition. But the model omits selective grazing, dispersal of propagules, stimulation of bacteria by grazing and, compensatory growth. It is to be hoped that mechanisms just reviewed are quantified and included in future simulation models.

ACKNOWLEDGEMENTS I am most grateful to D.T. Wicklow, R. Fogel, and R.M. Miller for many years of stimulating interactions and for reviewing the manuscript. The advice and review by V. Behan-Pelletier, the review by H. A. Verhoef, and G. Bengtsson’s permission to cite unpublished research are much appreciated. I thank Helen Badawi and Gladys Odegaard of the UIC Science Library for their help.

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Relative Risks of Microbial Rot For Fleshy Fruits: Significance with Respect to Dispersal and Selection for Secondary Defense MARTIN L . CIPOLLINI* and EDMUND W . STILES

I . Summary . . . . . . . . . . . . . . . . . I1 . Introduction . . . . . . . . . . . . . . . . A . Questions and Objectives . . . . . . . . . . B . Variations in Characteristics of Fleshy Fruits . . . C . Interspecific Variation in Secondary Defense Chemistry 111. Fruit Rot and Effects on Dispersal . . . . . . . . . A . Influence of Fruit Rot on Dispersal . . . . . . . B . Factors that Affect Risk of Microbial Rot . . . . . C . Natural Selection for Fruit Defenses . . . . . . IV . General Hypotheses and Predictions . . . . . . . . A . General Deterrent Nature of Fruit Rot . . . . . . B . Microbe-specific Defenses . . . . . . . . . . C . Interspecific Variation in Defense Effectiveness . . . V. Predictions for Temperate Seed Dispersal Systems . . . A . Temperate Fruiting Classes . . . . . . . . . . B . Predictions for Temperature Species . . . . . . . VI . Conclusions . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . .

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I SUMMARY Secondary plant chemicals are commonly thought to have evolved as feeding deterrents for herbivores. attractants for pollinators and seed-dispersal agents. and inhibitors of pathogens. and much evidence exists for such roles in various tissues of plants . Although a few hypotheses have been generated concerning ecological roles of secondary chemicals (other than pigments) in fleshy vertebrate-dispersed fruits. few empirical data refine these hypotheses

* Smithsonian Environmental Research Center. P.O. Box 28. Edgewater. MD 21037. ADVANCES IN ECOLOGICAL RESEARCH VOL. 23 lSBNCkl24l3923-5

Copyrighi 0 I992 Academic Press Limried A// righis of reproduction in an.v/orm reserved

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or test their predictions. To date, virtually all data concerning secondary chemicals of fleshy fruits have come from studies of highly-selected cultivated species. In these species, secondary chemicals present in high concentrations in immature fruits diminish considerably during ripening, but patterns for wild species remain practically unexplored. Because wild plants bearing fleshy fruits benefit from the consumption of fruit by vertebrate seed-dispersal agents, but presumably d o not benefit from consumption by other organisms, an evolutionary conflict seems evident with respect to attraction of dispersers and defense against non-dispersers. Selection for specific secondary chemical patterns in ripe fleshy fruits may result from the need to provide palatable and non-toxic pulp for dispersers, while retaining defense against various non-disperser “frugivores”, including seed predators and microbial fruit-rot agents. Here we examine the specific case of fleshy fruits, their vertebrate dispersers, and fruit-rot fungi, and review the parameters necessary to evaluate selection pressures for secondary chemical defense. We arrive at three general hypotheses: (i) In addition to causing early drop, fruit rotted by fungi should be generally deterrent to frugivores, and thus antifungal defenses should be maintained in ripe fruit. However, considerable interspecific variation may exist in the effects of fungi upon dispersal, and thus fruit defense may vary considerably with respect to fungal species. (ii) Microbe-specific chemical agents, with little or no negative effects on frugivores, should be common for plants under strong selection to provide nutritious or otherwise palatable fruits as a means of attracting frugivores. (iii) The degree of antifungal activity present in ripe fruit may vary among plant species, dependent upon selection pressure for persistence. Within this latter hypothesis, we present two alternative models: (a) The removal-rate model, which states that fruit defenses should be low for plant species whose fruits are generally removed rapidly upon maturation, and (b) the relative-risk model, which states that fruit defenses should be allocated in proportion to the risk of microbial degradation resulting from other intrinsic and extrinsic variables, including time of ripening, ripening synchrony, pulp nutrient content and physical design, and environmental factors influencing patterns of microbial colonization. We define more specific predictions for temperate vertebrate-dispersed species of eastern North America, based upon our own work with Ericaceous species. We suggest that, despite evidence that plant-frugivorefungus interactions are generally complex (i.e. “diffuse”) in nature, broadscale patterns of ripe-fruit defense chemistry may reflect selective pressures

RELATIVE RISKS OF MICROBIAL ROT FOR FLESHY FRUITS

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relating to seed dispersal. The hypotheses and predictions generated in this chapter provide a focus for elucidating the evolutionary significance of secondary chemicals of ripe fleshy fruits, and their potential effects in mediating plant-frugivore-fungus interactions.

11. INTRODUCTION A. Questions and Objectives This chapter concerns the defense of ripe fruit from microbial fruit-rot agents, and the degree to which characteristics relating to seed dispersal can be used to predict patterns of secondary chemical defense. We concentrate specifically on vertebrate-dispersed fruits of the temperate United States, and potential defense-attraction conflicts arising from the retention of defenses in ripe fruits. Few data are available on the importance of chemical defenses in increasing fruit persistence, or on the effects of these defenses on frugivorous animals, and only limited data exist concerning evolutionary patterns of plant-animal-microbe relationships for wild plants (Batra and Batra, 1985; Clay, 1988a, b; Pirozynski and Hawksworth, 1988; Barbosa et al., 1991). We first present a comprehensive review of the literature concerning fungal fruit rot as a factor in seed dispersal and as a selective pressure for fruit defense. We then use this information to generate general predictions concerning patterns of antifungal defense in ripe fruit with respect to fruit dispersal characteristics. These hypotheses and predictions are based primarily upon the “optimal defense” hypothesis that defenses are costly and should be allocated in direct relationship to fitness benefits accrued for particular plants and plant tissues (Rhoades, 1979, 1985).

B. Variation in Characteristics of Fleshy Fruits Following Ridley’s (1930) compendium on seed dispersal mechanisms, numerous researchers have recorded extensive variation in chemical and physical characteristics of fleshy fruits of vertebrate-dispersed plant species. Fruits vary in nutrient content, physical structure, color, size, seed number and size, seedlpulp ratio, water content, season of ripening, and ripening phenology (cf. McAtee, 1947; van der Pijl, 1969; Della-Bianca, 1979; Snodderly, 1979; Stiles, 1980; Burkhardt, 1982; Herrera, 1982b, 1984, 1987; Stiles and White, 1982; Janson, 1983; McDonnell et al., 1984; Gautier-Hion et al., 1985; Gorchov, 1985, 1990; Izhaki and Safriel, 1985; Johnson et al., 1985; Rathcke and Lacey, 1985; Van Roosmalen, 1985; Wheelwright, 1985; Platt and Hermann, 1986; DeBussche et al., 1987; Fleming et al., 1987; Levey, 1987a, b; Jordano, 1987a; Borowicz, 1988a, b; Lee et al., 1988; Poston and Middendorf, 1988; Lambert, 1989; White, 1989; Willson et al., 1989; Willson

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and O’Dowd, 1989; Willson and Whelan, 1989). Many of these attributes are suspected of influencing the dispersal of seeds by animals, and thus a large number of hypotheses have been proposed concerning the potential selective influence of frugivores on such fruit traits (cf. Harper et af., 1970; Snow, 1970; McKey, 1973; Morton, 1973; Regal, 1977; Howe, 1979, 1984, 1985; Janzen, 1979, 1981a, b; Thompson and Wilson, 1979; Stiles, 1980, 1982; Herrera, 1982a, 1985; Wheelwright and Orians, 1982; Willson and Thompson, 1982; Sorenson, 1983; Tiffney, 1984; Herbst, 1986; Murray, 1987; Gorchov, 1988; Willson and Whelan, 1990a). Field studies concerning fruits and frugivores suggest that complex, multi-species interactions may be the rule rather than the exception (cf. Howe and Primack, 1975; Howe and Estabrook, 1977; Howe and Smallwood, 1982; Moore and Wilson, 1982; Davidar, 1983; Pratt and Stiles, 1983; Levey et al., 1984; Sorensen, 1984; Janzen, 1985; Beehler, 1986; Fleming, 1986; Herrera, 1986, 1988a, b; KeelerWolf, 1988; Murray, 1988; O’Donnell, 1989; Palmeirim et af., 1989; Willson et al., 1989; Loiselle, 1990; Willson and Whelan, 1990b; Willson et al., 1990; Loiselle and Blake, 1991; Witmer, 1991). The general consensus is that pairwise coevolution is an unlikely result of such “diffuse” fruit-frugivore interaction, and that only consistent broad-scale interactions may be expected to result in coadaptive evolutionary patterns in fruit traits (Janzen, 1980; Stiles, 1980; Wheelwright and Orians, 1982; Gould, 1988; Spencer, 1988; Thompson, 1989). Through broad-scale differences in their selection of fruits and treatment of seeds, frugivores certainly have the potential to influence fruit traits, although it has been suggested that the converse (i.e. frugivores adapting to fruit traits) may be more likely (Herrera, 1985). Yet, due to the lack of empirical data concerning these relationships, hypotheses concerning the degree (or lack) of coadaptation among plants and frugivores remain largely untested (Howe, 1984; Herrera, 1986; Jordano, 1987b; Berenbaum and Zangerl, 1988; Thompson, 1989; Witmer, 1991). We suggest that consideration of the selective influence of other players in the game (i.e. fungi), and of the influence of secondary chemistry in mediating multi-way interactions, may help to answer some of these general questions.

C. Interspecific Variation in Secondary Defense Chemistry Interspecific variation in chemical and physical characteristics suggests that fruits may vary in susceptibility to microbes, seed predators and pests, and thus in their response to selective pressure for the evolution of secondary defenses (Stiles, 1980; Herrera, 1982a). Extensive evidence from horticultural and medicinal plants indicates that ripe fruits vary considerably in secondary chemistry (cf. Nelson, 1927; Goldstein and Swain, 1963; Chirboga and Francis, 1970; Hulme, 1971; Somers, 1971; Du and Francis, 1973; Jankowski, 1973; Stohr and Herrmann, 1975; Aoki et al., 1976; Starke and


39

Herrmann, 1976; Lea, 1978; Wang et al., 1978; Baj et al., 1983; Ivanic et al., 1983; Moller, 1983; Narstedt et al., 1983; Ojewole and Adesina, 1983; Samanta et al., 1983; Hikino et al., 1984; Perera et al., 1984; Jaworski and Lee, 1987; Roddick, 1987; Edwards, 1988; Morozumi et al., 1989; Bandyopadhyay et al., 1990; Janovitz-Klapp et al., 1990a, b). Outside of detailed and taxonomically significant knowledge of the anthocyanin pigments of fleshy fruits in the family Ericaceae (Francis et al., 1966; Fuleki and Francis, 1967; Harborne, 1967; Ballinger et al., 1972, 1979; Sapers et al., 1984; Andersen, 1985, 1987; Ballington et al., 1987), general patterns of secondary chemistry for fruits of wild species remain virtually unknown (Dement and Mooney, 1974; Janzen, 1979, 1983; McKey, 1979; Wrangham and Waterman, 1983). The extent to which dispersal characteristics relate to patterns of secondary chemistry is also virtually unexplored (Herrera, 1982a). Focusing specifically upon the question of antimicrobial defense chemistry, we base this chapter upon the following general questions: (i) To what extent does secondary chemistry influence the antimicrobial activity and persistence time of ripe fruit? (ii) How is ripe fruit choice by avian frugivores affected by factors relating to microbial degradation, including: (a) microbial modification of the pulp substrate, (b) accumulation of microbial metabolites, and (c) presence of constitutive and induced antimicrobial defenses? (iii) What are the evolutionary consequences for plants using different modes of antimicrobial defense (e.g. physical defenses, secondary chemicals, escape through time)? (iv) Can variation in antimicrobial chemistry be related to differences in other fruit characteristics, particularly those associated with temperate seasonality and fruit phenology? In order to evaluate these questions, we first present background information and indirect evidence that can be used to estimate the intrinsic risks of fruit rot for particular plant species, and thus the degree of selective pressure for antimicrobial defense. Using this background information, we then generate several predictions concerning variation in selection pressure for antifungal defense, with particular reference to fruits and fruit-rot fungi of eastern North America.

111. FRUIT ROT AND EFFECTS ON DISPERSAL

A. Influence of Fruit Rot on Dispersal 1. Variation in Fruit Quality and Persistence Fruit persistence is necessarily estimated from counts of fruits present in discrete quality categories such as “green”, “ripe”, “rotted” and “dropped”

40

M. L . CIPOLLINI A N D E. W . STILES

(cf. Gorchov, 1990). In the eyes of the actual consumer, however, these discrete categories do not exist. True fruit “quality” varies throughout the ripening period in a continuous fashion, and independently with respect to individual fruiting plants and their frugivores. Variation in quality can occur through actual chemical and physiological changes in the fruit, or by extrinsic changes occurring within the plant-frugivore community that alter general patterns of resource availability. Fruit ripening involves changes in many metabolic pathways, usually resulting in an increase in volume and water content, and changes in pigmentation, texture, firmness, cell wall composition, nutrient chemistry, and secondary chemistry (Tukey and Young, 1939; Goldstein and Swain, 1963; Crane, 1964; Boland et al., 1968; Hulme, 1971; Makus and Ballinger, 1973; Stohr and Herrmann, 1975; Starke and Herrmann, 1976; Samanta et al., 1983; Gross and Sams, 1984; Brady, 1987; Gross, 1987; Blanke and Lenz, 1989). These changes are brought about by changes in various hormone levels, especially increases of ethylene (Biale, 1975; Bruinisma et al., 1975; Pratt, 1975; Rhodes and Reid, 1975; Yang, 1975; Young et al., 1975; Lieberman, 1979; Shimokawa, 1983; Yang and Hoffman, 1984; Brady, 1987), and decreases in indole acetic acid (Frenkel, 1972, 1975; Cohen and Bandurski, 1982), gibberellin (Hedden et al., 1978), and cytokinin (Crane, 1964; Letham and Palni, 1983). Ripening may be abrupt or gradual in its initiation, and may vary in synchrony among plants and among fruits on a plant (Stiles, 1980; Janzen, 1983; Gorchov, 1990). Abscission of ripe fruit is also highly variable among and within plant species (Gough and Litke, 1980; Stephenson, 1981; Janzen, 1983; Sutherland, 1986). The intrinsic changes in fruit pulp due to natural maturation do not necessarily represent tightlylinked phase changes; many physiological traits have been shown to vary independently during the ripening process (Goldstein and Swain, 1963; Ballinger and Kushman, 1970; Moore et al., 1972; Makus and Ballinger, 1973; Markakis et al., 1963; Stohr and Herrmann, 1975; Starke and Herrmann, 1976; Willson and Thompson, 1982; Gross and Sams, 1984; Eck, 1988, 1990; Poston and Middendorf, 1988). Moreover, variation in frugivore community composition, frugivore experience and hunger level, presence of predators, spatial display pattern, and presence of other available fruiting plants may each independently affect the perception of fruit quality by an individual frugivore (Howe and Primack, 1975; Howe and Estabrook, 1977; Howe, 1979; Howe and Vande Kerchove, 1979; Herrera, 1982b, 1985, 1988a,b; Moore and Willson, 1982; Real et al., 1982; Stapanian, 1982; Wheelwright and Orians, 1982; Pratt and Stiles, 1983; Levey et al., 1984; Izhaki and Safriel, 1985; Murray, 1987; Levey, 1988a, b; White, 1989). Variation in relative quality toward dispersers and damaging agents may thus be a key factor influencing selection on pulp secondary chemistry.


41

2. Definition of “Fruit Rot” Fruit rot may be defined as the chemical and physical alteration of fruit pulp tissue due to infection by microbes (Janzen, 1977). Because the high acidity of fruit tissue tends to inhibit bacterial growth, and because dispersal and tissue penetration capabilities of bacteria may be limited, filamentous fungi are the most important agents of fruit rot (Stevens, 1913; Stevens and Hall, 1926; Ainsworth, 1971; Dennis, 1983; Nel, 1985; Rossman et al., 1987; Agrios, 1988; Farr et al., 1989). Infection by various insect-dispersed yeasts, particularly Saccharomyces spp., is also very common (Begon, 1982; Dennis, 1983; Nel, 1985; Starmer et al., 1990). While recognizing the potential importance of other organisms as fruit degraders, we restrict our remaining discussion to filamentous fungi and yeasts, which we refer to as “fungi”. Fungal fruit rot results in the alteration of pulp nutrient patterns (Hawkins, 1915; Schiffman-Nadel, 1975; Cooke, 1979; Pucheu-Plante and Mercier, 1982; Dennis, 1983; Pitt and Hocking, 1985; Snowdon, 1990; Starmer et al., 1990), physical breakdown of tissues (White and Fabian, 1953; Cooke, 1979; Rujkenberg et al., 1980; Cooper and Wood, 1975; Ceponis and Stretch, 1983; Barmore and Ngyen, 1985; Pitt and Hocking, 1985), accumulation of mycotoxins (Bilai, 1963; Rodricks, 1976; Pitt and Hocking, 1985; Marasas and Nelson, 1987; Hsieh, 1989), alteration of ripening rates (Cohen and Schiffman-Nadel, 1971 ; Zauberman and Schiffman-Nadel, 1973), and changes in taste, odor and color (Dennis, 1983; Nel, 1985; Pitt and Hocking, 1985; Leistner et al., 1989; Newsome, 1990). In general, therefore, fruit rot should be detrimental to seed dispersal.

3. Relationship to Seed Dispersal It has been suggested that saprophytic fungi attacking senescent tissues should exert little selection pressure upon the plants they infect, e.g. Drosophila-dispersed yeasts infecting cactus tissues (Starmer and Fogelman, 1986; Starmer et al., 1990). We suggest that the case of ripe fruit rot is an exception to this general assertion, because variation among individual plants in their ability to prevent or delay ripe fruit rot should have decided fitness consequences, due to variation in seed dispersal. Thus, selective pressure for plants to prevent fruit rot should relate directly to variation in the probability of seed dispersal (Janzen, 1977). Fitness benefits due to successful dispersal may include: (a) reduction in local seedling density or intraspecific competition (Howe and Smallwood, 1982; Augspurger, 1984; Howe and Schupp, 1985), (b) removal away from the competitively dominant maternal plant (Janzen, 1970; Howe, 1979), (c) increased colonization of spatially distant or ephemeral habitats (Smith, 1975; McDonnell and Stiles, 1983; Denslow, 1987; Hoppes, 1988; Levey, 1988b; Murray, 1988; Schupp et al., 1989), (d) escape from density- and distance-dependent predators and

42

M. L. CIPOLLINI AND E. W. STILES

diseases (Janzen, 1970; Connell, 1971; Augspurger, 1984; but see Hubbell, 1979), (e) dispersal to microenvironmental “safe-sites’’ (Harper et al., 1970; Davidar, 1983; Piper, 1986; Schneider and Sharitz, 1988), and (f) removal of inhibitory effects of surrounding pulp or fulfillment of the need for seed scarification (Lieberman and Lieberman, 1986; Robinson, 1986; Janzen, 1977; Barnea er al., 1991). Alterations of fruit tissue via fungal degradation can negatively affect dispersal in two important ways: (a) by decreasing fruit retention time by hastening ripening and abscission, and (b) by direct and indirect negative effects upon foraging by frugivores. Fungi may hasten fruit ripening and abscission via the production or induction of plant hormones critically associated with senescence and ripening. For instance, the autocatalytic release of ethylene may be induced by fungal infection (Cohen and Schiffman-Nadel, 1971; Zauberman and Schiffman-Nadel, 1973; Fleuriet and Macheix, 1975; Schiffman-Nadel, 1975; Yang and Hoffman, 1984). Fruit drop from the plant does not necessarily preclude dispersal, because potential dispersal agents may forage for fallen fruits on the ground (Howe and Smallwood, 1982), and seeds commonly germinate beneath parent plants (Hubble, 1979). However, dropped fruits may be subjected to increased fungal rot and seed predation (Janzen, 1970). Fruit rot can also directly and indirectly discourage foraging by dispersal agents (Janzen, 1977; Herrera, 1982a). Direct effects include the alteration of the physical structure, odor, appearance, and palatability of the fruit, such that frugwores are discouraged specifically from feeding upon the infected fruit (Borowicz, 1988b; Buchholz and Levey, 1990). Indirect effects may include a decrease in the dispersal of non-infected fruit brought about by associative feeding aversions (Chapman and Blaney, 1979; Wicklow, 1988), or by alterations in overall fruit display pattern (Murray, 1988). Although fruit-rot fungi may alter pulp chemistry and physical structure by any or all of these mechanisms, such changes cannot be considered in absolute terms, because interactions among fruit characteristics and various extrinsic factors may make rotted (or otherwise “poor” quality) fruit acceptable at certain times or under certain conditions. This may be especially true during times of resource depletion (cf. Foster, 1977), when animals may be less discriminating while feeding. Yeast rots that produce acids and ethanol may even delay fruit abscission (M. Cipollini, personal observation of Vaccinium macrocarpon), and it is possible that physical and chemical changes produced by these and other fungi may actually enhance the apparent attractiveness of fruit under some circumstances (Janzen, 1977; Pirozynski and Hawksworth, 1988). Some fungal rots (e.g. “noble” rot produced by Botrytis cinerea on Sauterne grapes) may actually increase levels


43

of simple sugars within the pulp (Pucheu-Plante and Mercier, 1982). Pirozynski and Hawksworth (1988) go so far as to suggest that fungal intermediaries may be necessary to enhance fruit quality for dispersers, and thus act to promote dispersal. It is clear, therefore, that study of the effects of fungal rot on fruit “quality” must take into account not only measures of fruit persistence under field conditions, but must also evaluate potential effects of specific fungi upon dispersal. One method of accomplishing this is to estimate removal rates by foragers in the field for naturally rotted and unrotted fruits. Aside from logistical problems, this method suffers from the difficulty of simultaneously determining physical and chemical fruit parameters, determining fruit-rot status, measuring dispersal rates, and controlling for extrinsic factors that may account for a large degree of the variation that occurs in dispersal from year to year. Additionally, the fungal agents responsible for fruit rot usually remain unidentified (cf. Borowicz, 1988b; Buchholz and Levey, 1990). Feeding trials with captive frugivores provide an alternative method of evaluating the degree of deterrence produced by particular fruitrot agents, while experimentally controlling many potentially interacting extrinsic factors. Field experimentation (artificial inoculations, etc.) may also provide pertinent empirical data.

B. Factors that Affect Risk of Microbial Rot 1. Pulp Nutrient Chemistry Much evidence exists for interspecific variation in the primary nutrient content of ripe fruit pulp, including water, simple sugars, polysaccharides, protein, lipids, and minerals (Boland et al., 1968; Snow, 1970; Hulme, 1971; Landers et al., 1979; Stiles, 1980; Herrera, 1982b, 1984, 1987; Stiles and White, 1982; Sorensen, 1984; Gautier-Hion et al., 1985; Izhaki and Safriel, 1985; Johnson et al., 1985; Wheelwright and Janson, 1985; Herbst, 1986; DeBussche et al., 1987; Eck, 1988, 1990; White, 1989; Peters and Hammond, 1990; Cipollini, 1991; Gagiullo and Stiles, 1991). Evidence is also accumulating which shows potentially important levels of intraspecific variation in nutrient content, as well as important qualitative differences in pulp constituents (Galleta et al., 1971; Vander Kloet and Austin-Smith, 1986; Herrera, 1988a, b; Keeler-Wolf, 1988; Poston and Middendorf, 1988; Gargiullo and Stiles, 1991; E. Stiles and M. Cipollini, unpublished). Growth of fungi has been shown to respond to variation in the chemical nutrient make-up of media and host plants (Trelease and Trelease, 1929; Bilai, 1963; Muys et al., 1966; Ballinger and Kushman, 1970; Ballinger et al., 1978; Parkinson, 1981; Vanderplank, 1984; Dhingra and Sinclair, 1985; Pitt and Hocking, 1985; Cihlar and Hoberg, 1987; Kerwin, 1987; Verhoeff et al., 1988; Lacey, 1989; Cipollini, 1991). It

44


follows that variation in fruit-pulp nutrient chemistry should be related to variation in the intrinsic potential for fungal growth. Although it is generally expected that higher nutrient levels should enhance microbial growth rates, non-linear responses may be common. For instance, increases in sugar content of host tissues may increase susceptibility to certain fungi, but only up to the point at which osmotic effects of high sugar content begin to inhibit hyphal growth (Trelease and Trelease, 1929; Janzen, 1983; Vanderplank, 1984; Cipollini, 1991). Due to substrate specialization, fungi may vary interspecifically in their utilization of particular nutrient components, and thus in their response to quantitative variation in these components. For example, mutualistic interactions among yeasts have apparently resulted in complementary metabolic capabilities that may facilitate nutrient degradation within fruits (Starmer and Fogelman, 1986). It should be noted that the allocation of plant constituents has been conventionally reported as per cent dry mass, but from the perspective of fungal growth potential, per cent wet mass may be a more appropriate measure. A succession of microbes generally accompanies the saprophytic decomposition of senescent plant tissue (e.g. rapid colonizers that reduce simple sugars, followed by slower reducers of lipids, cellulose, and finally lignins; Cooke, 1979). Growth studies suggest that, despite their heterotrophic nature, fungi are generally less limited in growth by quantitative variation in organic substrates, and more limited by variation in the mineral content of the medium (Ballinger and Kushman, 1970; Cooke, 1979; Cihlar and Hoberg, 1987; Kerwin, 1987). This is apparently especially true for available nitrogen. Fruit-pulp tissue is generally low in nitrogen and other minerals, despite considerable variation in organic constituents (Ballinger and Kushman, 1966; Boland et al., 1968; Hulme, 1971; Landers et al., 1979; Stiles, 1980; Herrera, 1982b, 1984, 1987; Stiles and White, 1982; Izhaki and Safriel, 1985; Johnson et al., 1985; Herbst, 1986; DeBussche et al., 1987; Poston and Middendorf, 1988; White, 1989). The rate of hyphal growth may be very important in influencing the rate at which the physical structure and nutrient patterns of the pulp are altered (White and Fabian, 1953; Cooper and Wood, 1975; Verhoeff et al., 1988; Lacey, 1989), and the overall ability of the fruit pulp to sustain fungal growth (total available nutrients) may influence the degree of mycotoxin production (Bilai, 1963; Rodricks, 1976; Pitt and Hocking, 1985; Marasas and Nelson, 1987; Wicklow, 1988; Lacey, 1989; Scott, 1989). Thus the effect of fungal growth on fruit chemistry may be considered in both absolute and relative terms, that is, similar absolute changes in nutrient level may differentially affect the relative quality of fruit for dispersers. For instance, fruits with a low initial level of pulp sugar may be more rapidly reduced to a nonacceptable sugar threshold than fruits of high initial sugar content. A higher rate of fungal growth could offset such an effect by reducing sugar content


45

more quickly in high-sugar fruits, but this is unlikely to ameliorate completely differences between initially high- and low-sugar fruits (Janzen, 1977; Herrera, 1982a). High-sugar fruits should thus always be more profitable for dispersers than low-sugar fruits, and they should therefore be preferred when availabilities are equal (cf. Lundberg and Astrom, 1990). This is where variation in toxin production by fungi may be critically important (Janzen, 1977). Increased toxin production by fungi on nutrient-rich substrates may reduce pulp quality to a greater degree than may be apparent from simple examination of fungal growth rates (Rodricks, 1976; Marasas and Nelson, 1987; Lacey, 1989; Leistner et al., 1989). Fungal species may vary in the quality of toxins produced on various substrates (Marasas and Nelson, 1987; Mills, 1989; Tanaka and Ueno, 1989; Yabe et af., 1989), in the effect of quantitative nutrient variation on toxin production (Cooke, 1979), and in the effects of their toxins upon different frugivore species (Janzen, 1977; Marasas and Nelson, 1987; Wicklow, 1988; Kiessling, 1989). Additionally, synergistic toxin interactions may occur due to coinfection by toxigenic fungi (Janzen, 1977; Wicklow, 1988). In short, the influence of primary nutrient variation on the rates and effects of fungal decomposition may be very dependent upon the particular plant-frugivore-fungus species combination under consideration, and experimental tests should employ media that reflect the basic nutrient and chemical background of the plant tissue of concern.

2. Ambient Environmental Conditions Extrinsic environmental factors that vary among plant species should result in variation in the risk of fungal rot. Extrinsic factors that may affect colonization, spore germination, mycelial growth, and toxin production include temperature, light regime (including UV irradiation), humidity, rainfall, and disease vectors (McKeen, 1958; Bilai, 1963; Cappellini et al., 1972, 1982, 1983; Rodricks, 1976; Ballinger et af., 1978; Cooke, 1979; Hartung et a[., 1981; Ceponis and Stretch, 1983; Jarvis and Traquair, 1984; Pitt and Hocking, 1985; Marasas and Nelson, 1987; Agrios, 1988; Biggs and Northover, 1988; Lacey, 1989; Snowdon, 1990; Starmer et al., 1990). Environmental conditions during the time of colonization may be just as important in influencing fruit rot as conditions during colony growth and sporulation (Varney and Stretch, 1966; Hartung et al., 1981; Cappellini et al., 1983; Milholland and Daykin, 1983; Daykin, 1984; Agrios, 1988; Dashwood and Fox, 1988; Arauz and Sutton, 1990; Daykin and Milholland, 1990; Yang et al., 1990). Also, some environmental effects, such as bruising, insect damage, abscission scarring, sun-scald and freeze-rupturing, may predispose fruits to rot at later times (Graham et al., 1967; Cappellini and Ceponis, 1977; Dennis, 1983; Jarvis and Traquair, 1984; Howard er al., 1985; Nel, 1985; Schwarz and Boone, 1985; Starmer et al., 1990).

46


Interactions among various abiotic and biotic factors may be important influences on fungal growth and toxin production (Lacey, 1989; Scott, 1989). For instance, climatic variation may affect the abundance and activities of insect vectors of various fruit diseases (Batra, 1983; Dennis, 1983; Batra and Batra, 1985; Nel, 1985). Climatic variables may themselves interact, resulting in non-linear effects on fungal growth. For instance, high temperatures may be commonly associated with low levels of humidity and high levels of potentially fungicidal UV radiation. Generally speaking, warm ( f 25” C), humid or moist conditions are optimum for spore germination and mycelial growth of fruit-rot fungi (Cappellini et al., 1972; Ballinger et al., 1978; Cooke, 1979; Hartung et al., 1981; Johnson and Booth, 1983; Jarvis and Traquair, 1984; Agrios, 1988; Biggs and Northover, 1988; Lacey, 1989; Scott, 1989; Arauz and Sutton, 1990; Snowdon, 1990), but exceptions to this general pattern may occur (Scott, 1989). Experimental work should attempt to account for potential environmental variation, or such variation may form the focus of testable predictions.

3. Identity and Quantity of Spore Inoculum Initiation of fruit rot necessarily begins with inoculation of fruit tissue by microbes. Seasonal, habitat-associated, and environmental effects may all contribute to variation in the abundance and species composition of fungal inoculum (Dye and Vernon, 1952; Pady, 1957; Williams et al., 1957; Leben et al., 1968; Cooke, 1979; Wong and Kwan, 1980; Lacey, 1981; Wicklow, 1981; Shivas and Brown, 1984; Pandey, 1990; Starmer et al., 1990; Yang et al., 1990). Ripe fruit rot is most commonly associated with “opportunistic”, or “generalist” fungal species (Varney and Stretch, 1966; Dennis, 1983; Nel, 1985; Rossman et al., 1987; Agrios, 1988; Farr et al., 1989; Snowdon, 1990). Fungal species noted for causing ripe fruit rot belong to: Alternaria (Cappellini et al., 1972), Aspergillus (Raper and Fennell, 1965; Christensen and Tuthill, 1986), Botrytis (Cappellini et al., 1972; Rujkenberg et al., 1980; Pucheu-Plante and Mercier, 1982; Dashwood and Fox, 1988; Malathrakis, 1989), Cladosporium (Dennis, 1983; Nel, 1985), Colletotrichum (Gloeosporium) (Stanghellini and Aragaki, 1966; Cappellini et al., 1972; Hartung et al., 1981; Daykin, 1984; Yang et al., 1990), Fusarium (Zauberman and Schiffman-Nadel, 1973; Nelson et al., 1983), Ceotrichum (Cooke, 1979), Monilinia (Hawkins, 19 15; Biggs and Northover, 1988), Penicillium, Phoma (Malloch, 198l), Phomopsis (Wilcox, 1939, 1940; Cappellini et al., 1982; Milholland and Daykin, 1983), Rhizopus (Nel, 1985), Saccharomyces and other yeasts (Cappellini et al., 1972; Starmer and Fogelman, 1986), and various Mycelia sterilia (Barnett and Hunter, 1972). Latent (endophytic) fungal infections may be a very important and widespread mechanism of fruit-rot initiation (McKeen, 1958; Stanghellini and Aragaki, 1966; Graham et al., 1967;


47

Schiffman-Nadel, 1975; Rujkenberg et al., 1980; Hartung et al., 1981; Pucheu-Plante and Mercier, 1982; Daykin, 1984; Agrios, 1988; Biggs and Northover, 1988; Carroll, 1988; Dashwood and Fox, 1988). Latent infections result from fungal spore germination and penetration in the flower bud, flower, or green fruit stages, but d o not cause symptoms of rot until fruits mature (Agrios, 1988; Snowdon, 1990). For latent fungi especially, environmental conditions at the time of spore germination may be as important as conditions at the time fruit rot commences (Snowdon, 1990). Highly host-specific fungi may be important pathogens associated with the loss of green fruit, but apparently rarely cause ripe fruit rot (Nel, 1985; Agrios, 1988; Farr et al., 1989). For example, the Monilinia spp. that cause Mummy-berry disease of Vaccinium and Gaylussacia spp. are the only well known host-specific blueberry fruit pathogens (Varney and Stretch, 1966; Batra, 1983; Batra and Batra, 1985). All of these Monilinia fungi cause loss of green fruit prior to ripening (Batra, 1983). Although primarily generalists, saprophytic fungal species associated with ripe fruit rot may vary considerably in the mechanisms by which they infect fruit tissue, in the breadth of their plant species and tissue affinities, and in their ability to produce changes in fruit pulp (cf. Starmer et al., 1990). Fungi may likewise vary considerably in the manner and extent to which they affect fruit dispersal. Experimental work should focus on fruit-associated organisms that both d o and do not typically cause rot, because it is equally important to elucidate mechanisms responsible for general defense, as it is to identify variation in resistance to known pathogens.

4 . Synchrony and Other Display Characteristics Synchronous ripening increases the physical proximity of susceptible fruits, and may thus facilitate the within-plant spread of fruit-rot agents. Examples from commercial fruits include webbing and nesting that occurs with several post-harvest fungi (Dennis, 1983; Nel, 1985), the enhancement via physical proximity of splash-dispersal infection of strawberry fruits by the anthraconose fungus Colletotrichum acutatum (Yang et al., 1990), and the increased likelihood of bunch rot (Aspergillus acleatus) within tight, synchronously ripening grape clusters (Jarvis and Traquair, 1984). As susceptible host plants and their fruits may be thought of as “islands” in space and time (Janzen, 1968, 1973; Kuris et al., 1980; but see Janzen, 1979), synchronous within- and among-plant fruit ripening should accelerate colonization rates, and thus increase the epidemiological spread from fruit to fruit and plant to plant (Wicklow, 1981; Vanderplank, 1984). As with extrinsic risk variables, the degree of synchrony or clustering may be controlled in experimental work by the selection of comparable plant species, or such variation may form the focus of testable hypotheses.

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5 . Removal Rate, or Time of Exposure Other factors being equal, the risk of fruit rot should be directly proportional to the rate at which susceptible fruits are removed by frugivores (Herrera, 1982a). Plants whose fruits are normally removed quickly should be under less risk of becoming colonized. Even if the fruit is colonized, rapid removal should allow less time for fruit-rot agents to grow and thereby negatively affect fruit characteristics. Because plant, fruit, and environmental characteristics may each independently influence removal rates, as well as fruit-rot rates, interactions among these factors must be taken into account when generating predictions concerning fruit defense patterns (Pirozynski and Hawksworth, 1988).

C. Natural Selection for Fruit Defenses I . Secondary Chemicals as Defense Agents The recognition that secondary chemicals may act as defense agents revolutionized studies of plant-herbivore and plant-pathogen interactions (Rhoades, 1985). We propose that the study of fruit secondary defenses will be equally informative and stimulating to the field of dispersal ecology. Although fruit chemistry has been little studied from this perspective, patterns of immature fruit defenses are likely to be basically similar to the broad-spectrum defenses of leaves. Thus, as a background to the discussion of potential chemical patterns in ripe fruit, we present the following general description of plant defenses. ( a ) Constitutive defenses. Secondary chemicals that may defend plants against pests, herbivores, other plants, and pathogens can be placed into two major classes: constitutive and induced (Harborne and Ingham, 1978; Vanderplank, 1984; Agrios, 1988). Constitutive defenses are present in plant tissue prior to feeding damage or the invasion of pathogens (Stoessl, 1970; Mitscher, 1975; Schonbeck and Schlosser, 1976; Harborne and Ingham, 1978). Examples of structural constituents include cellulose, lignin (Vance et af., 1980), epicuticular waxes (Franich et al., 1983), and trichomes (Levin, 1973; Rathcke and Poole, 1975). A variety of toxic compounds may enhance structural constituents (Nickell, 1959; Raffauf, 1970; Stoessl, 1970; Freeland and Janzen, 1974; McKey, 1974; Robinson, 1975; Levin, 1976; Swain, 1977; Harborne and Ingham, 1978). Specific examples of biologically active constituents include numerous classes of phenolic compounds (Hulme and Edney, 1960; Cruikshank and Perrin, 1964; Mathis, 1966; Towers et al., 1966; Feeny, 1968; Levin, 1971; Janzen, 1974; Bate-Smith, 1977; Rhoades, 1977; Harborne, 1979, 1980, 1989; McClure, 1979; Swain, 1979a, b; Gartlan et af., 1980; Berenbaum, 1981; Lane and Shuster, 1981; Johnson, 1983;


49

Jaworski and Lee, 1987; Lee et al., 1987; Laks, 1989; Meyer and Karasov, 1989; Morozumi et al., 1989; Van den Berg and Labadie, 1989; Van Sumere, 1989; Williams and Harborne, 1989a, b; Bandyopadhyay et al., 1990; Henderson, 1990), organic acids (Markakis et al., 1963; Moller, 1983), alkaloids (Raffauf, 1970; McKey, 1974; Robinson, 1979; Manske and Rodrigo, 1981; Giral and Hidalgo, 1983; Ojewole and Adesina, 1983; Samanta et al., 1983; Perera et al., 1984; Roddick, 1987), terpenes (Mabry and Gill, 1979; Camazine et al., 1983; Hubbell et al., 1983; Ivanic et al., 1983; Hubbell and Howard, 1984), terpenoid and steroidal saponins (Aoki et al., 1976; Applebaum and Birk, 1979; Roddick, 1987), fatty and resin acids (Seigler, 1979; Franich et al., 1983), phytohemagglutinins (Liener, 1979), and non-protein amino acids (Janzen, 1969; Rosenthal and Bell, 1979; Blieler et al., 1988). Condensed and hydrolyzable tannins, two classes of polyphenolic compounds, are among the most important secondary constituents because of their general antifungal, antibacterial, and antiherbivore activities, and widespread occurrence among plant species (Levin, 1971, 1976; Bate-Smith, 1972, 1977; Freeland and Jazen, 1974; Swain, 1978, 1979a,b; Lane and Schuster, 198I ; Galloway, 1989; Porter, 1989; Walkinshaw, 1989). Tannins complex with a broad spectrum of biomolecules, especially proteins and polymeric carbohydrates, and thus have astringent properties (Bate-Smith, 1977; Wang et al., 1978; Hagerman and Butler, 1980; Martin and Martin, 1982; Asquith and Butler, 1986; Hagerman, 1987, 1989; Mole and Waterman, 1987a,b; Laks, 1989; Lewis and Yamamoto, 1989). Apparently due to their astringency, tannins are distasteful for many herbivores, and ingestion has been hypothesized to interfere with digestion by binding digestive enzymes, food proteins, and digestive membranes (Goldstein and Swain, 1963; Feeny, 1968, 1969, 1973; Bate-Smith, 1972, 1977; Reese, 1979; Wrangham and Waterman, 1983; Faeth, 1985; Coley, 1986; Bernays and Janzen, 1988; Rossiter et al., 1988; Bernays et al., 1989; Butler, 1989; Karowe, 1989; Meyer and Karazov, 1989; Schultz, 1989; Clausen et al., 1990; Koenig, 1991). Other constitutive chemicals are less generally deterrent for herbivores (Feeny, 1969; Bate-Smith, 1972; Chapman and Blaney, 1979; Crawley, 1984). In fact, for specialist herbivores, specific secondary constituents may be responsible for evolved feeding preferences (Benson et al., 1975; Rhoades and Cates, 1976; Janzen, 1979; Rhoades, 1979, 1985; McDonald, 1983; but see Jermy, 1984; Smiley, 1985). ( b ) Induced defenses. Induced defenses are elicited by physical damage or by microbial entry into plant tissues (Fleuriet and Macheix, 1975; Harborne and Ingham, 1978). Induced structural responses include cell wall lignification and callose formation (Stanghellini and Aragaki, 1966; Allison and Shalla, 1973; Rujkenberg et al., 1980; Vance et al., 1980), deposition of silica

50


(Heath, 1981), and hypersensitive death of cells (Maclean et al., 1974; Bailey et al., 1980). Bioactive agents that can be induced include bound toxins that are released upon damage or microbial entry (post-inhibitins: Harborne and Ingham, 1978), various other phenolics (Harborne, 1980; Rossiter et al., 1988; Tuomi et al., 1990; Zangerl, 1990), cyanogenic glycosides (Dement and Mooney, 1974; Conn, 1979; Narstedt et al., 1983; Briggs and Schultz, 1990), glucosinolates (Van Etten and Tookey, 1979), various enzymatic proteins (Esquerre-Tugaye et al., 1979; Ryan, 1979; Malamy et al., 1990; Metraux et al., 1990), alkaloids (Baldwin, 1988), and small molecular weight phenolics synthesized de novo following damage or invasion (phytoalexins: Bailey and Deverall, 1971; Mansfield and Hargreaves, 1974; Paxton et al., 1974; Anderson-Prouty and Albersheim, 1975; Albersheim and Valent, 1978; Anderson, 1978; Hahn and Albersheim, 1978; DeWit and Roseboom, 1980; Burdon and Marshall, 1981; DeWit and Kodde, 1981; Hahlbrock et al., 1981; Bruce and West, 1982; Yamazaki et al., 1983; Darvill and Albersheim, 1984). Induction of defense is not necessarily restricted to the damage site of infected tissues, as various transduction signals may induce systemic resistance (Lynn and Chang, 1990; Malamy et al., 1990; Metraux et al., 1990), and it had even been suggested that resistance in nearby conspecifics may be induced via airborne chemical signals (Baldwin and Schultz, 1984; Rhoades, 1985). The importance of metabolically induced defenses in the resistance of plants to leaf and stem pathogens is well established (Keen, 1975). These defenses can be overcome by host-specific pathogens, thus paving the way for coevolutionary feedback (Bailey and Deverall, 1971; Denny and Van Etten, 1983). Such host-specific pathogens are commonly associated with immature fruits (Agrios, 1988). In having photosynthetic capability, active cell division, and active anabolic metabolism, immature fruits may be physiologically similar to green leaves, and may be quite capable of responding to fungal infection via de novo induced defenses. As discussed previously, infection of ripe fruit is more commonly due to facultative or opportunistically saprophytic fungi. The catabolic changes that accompany fruit ripening may render mature fruit susceptible to generalist saprophytes, and may thus diminish the opportunity for coevolutionary feedback between host and fungus necessary for reciprocal selection leading to host-specificity (Rhoades, 1985; Roddick, 1987; Thompson, 1989). Defense induction in ripe fruits is thus likely to result primarily from the release of less specific bound toxins (post-inhibitins) following fungal invasion or tissue damage. The epidermal layers of the fruit pericarp (fruit skin) are important structural barriers to microbial invasion, but as with most physical features, epidermal structure may be enhanced by bioactive agents (Croteau and Fagerson, 1971; Croteau, 1977; Franich et al., 1983; Janzen, 1983). There are several reasons to expect that defense should be concentrated in fruit skin:


51

(i) Direct intra- and inter-cellular penetration through the epidermis is a primary source of fungal infection (White and Fabian, 1953; Stanghellini and Aragaki, 1966; Stiles and Abdalla, 1966; Graham et al., 1967; Cappellini and Ceponis, 1977; Cooke, 1979; Rujkenberg et al., 1980; Pucheu-Plante and Mercier, 1982; Ceponis and Stretch, 1983; Milholland and Daykin, 1983; Daykin, 1984; Jarvis and Traqair, 1984; Schwarz and Boone, 1985; Agrios, 1988). Only a few fruit infections are systemic, and are commonly transmitted through vascular tissues (e.g. Xanthomonas infecting plum fruit (Du Plessis, 1990)). (ii) Because fruit skin comprises a relatively small fraction of fruit mass, concentrating chemicals there is unlikely to result in a total fruit concentration that is toxic to frugivores (Janzen, 1979, 1983). (iii) Animals may avoid detrimental effects by regurgitating or defecating relatively intact fruit skins (M. Cipollini, personal observation). Indirect evidence for the importance of fruit skin as a defense stems from studies showing that host-specific fruit pathogens may depend upon insect vectors for entry into fruit tissue. For instance, Monilinia (Mummy-berry) diseases of Vaccinium spp. are transferred to flower stamens via bees acting as pollen vectors (Batra, 1983; Batra and Batra, 1985), and specific bacterial and yeast rots are introduced into fruits by foraging Drosophila and Rhagoletis fruit-flies (Howard et al., 1985; Starmer and Fogelman, 1986; Pirozynski and Hawksworth, 1988; Starmer et al., 1990). ( c ) Interaction among plant chemicals. Because plant tissues contain a mixture of potentially interacting chemicals, synergistic or counteractive interactions among various components may be common (McKey, 1979; Reese, 1979; Berenbaum and Zangerl, 1988; Cipollini, 1991). For instance, the toxicity of many small phenolics is enhanced at low pH by high concentrations of organic acids such as citric acid (Hoffman et al., 1941; Cruikshank and Perrin, 1964; Constantine et al., 1966; Graham et al., 1967; Swartz and Medrick, 1968; Stoessl, 1970; Lacey, 1989; Davidson and Juneja, 1990). Although phenolics are commonly held at medium pH within vacuoles (Robinson, 1975; McKey, 1979; Harborne, 1980), cellular disruption following physical damage or microbial entry may allow them to come in contact with the acidic cytoplasm. For example, the level of organic acid in cultivated blueberry fruit is known to be related to its resistance to fungal rot (Ballinger and Kushman, 1970; Galleta et al., 1971; Ballinger et al., 1978). This occurs in spite of the fact that equivalent in vitro variation in organic acids alone has only a small negative or even a positive effect on growth of the causative agents of these rots (Ballinger and Kushman, 1970; Galleta et al., 1971; Cipollini, 1991). This suggests that interactions of acids with small phenolics in the fruit tissue may be partially responsible for the antifungal activity.

52


Fungi may counter this pH/phenolic interaction effect by utilizing organic acids as substrates during hyphal extension, and thus increasing tissue pH to levels at which phenolics are less active (Verhoeff et al., 1988). Further increases in pH may result in phenolic oxidation products (e.g. quinones) that may be more toxic to fungi (Cilliers and Singleton, 1990). Many other synergistic defense patterns have emerged in the literature: (i) The activity of the most effective phenolic within grape (Vitis vinifera) berries, pterostilbene, against the fungus Botrytis cinerea, depends in part upon its association with glycolic, tartaric and malic acids (Pont and Pezet, 1990). (ii) The antimicrobial properties of bearberry leaf extract (Arctostaphy10s spp.) and cranberries (Vaccinium spp.) have been attributed to a complex synergism among various organic acids and small phenolics (Clague and Fellers, 1934; Constantine et al., 1966; Papas et al., 1966; Graham et al., 1967; Swartz and Medrick, 1968; Frohne, 1969; Matzner, 1971; Eck, 1990). (iii) The antifungal activity of Citrus spp. fruit skin has been attributed to a synergistic interaction between nootkatene and citric acid (Morozumi et al., 1989). (iv) Complexing of plant protein with tannins in protein-rich tissues during consumption may reduce the negative effects of tannins on digestion by herbivores (Asquith and Butler, 1986; Bernays et al., 1989). (v) Storage lipids act in an unknown fashion to enhance the effect of condensed tannins in reducing digestive efficiencies for the acorn woodpecker, Melanerpes formicivorus (Koenig, 1991). (vi) Coingestion of saponins and tannins by rodents has been shown to reduce the negative effects of these compounds on growth, and rodents may balance intake of each compound so as to ameliorate toxic effects (Freeland et al., 1985). (vii) Fusaric acid, a toxin produced by Fusarium spp., acts synergistically to increase the antifungal activity of plant phytoalexins (Wicklow, 1988). (viii) Increased pH levels may reduce growth of fungi attacking Lycoperiscon esculentum fruits, due to a positive effect on the antifungal activity of the steroid glycoalkaloids solanine, tomatine, and demissine (Roddick, 1987). (ix) The overall inhibitory effects of the mixture of furanocoumarins present in the herb Pastinaca sativa toward insect herbivores is greater than the sum of the activities of the individual compounds (Berenbaum et al., 1991).


53

Coupled with our generally poor knowledge of the compartmentalization of various chemical constituents within plant cells and tissues, as well as our limited understanding of mechanisms of toxicity, these potential interactions make it very difficult to attribute in vivo antifungal defense, and/or feeding patterns of herbivores and frugivores to individual isolated chemicals (Janzen, 1979; Berenbaum and Zangerl, 1988).

2. Biotic Defenses Much interest has been generated recently concerning the potential role of phylloplane and endophytic microbes as antiherbivore and antidisease agents in plants (Blakeman and Fokema, 1982; Cooke and Baker, 1983; Windels and Lindow, 1985; Carroll, 1988; Scott, 1989; Wilson et al., 1991). Endophytic fungi may be very important as antiherbivore defense agents in grasses via ergot alkaloid production (Clay, 1988a, b; Buckley and Halisky, 1990). Additionally: (i) Phylloplane micro-organisms have been shown to be antagonistic toward plant pathogens via both competitive and antibiotic mechanisms (Newhook, 1957; Upadhyay, 1981; Anagnostakis, 1982; Mercier and Reeleder, 1985; Wilson and Lawrence, 1985; Boland and Hunter, 1988; Janisiewicz, 1988; Stretch, 1989). (ii) Mycoparasites, notably Trichoderma species, have likewise been shown to be antagonistic towards potential plant pathogens (Agrios, 1988). (iii) Growth of mycotoxin-producing fungi has been controlled by inoculations of grain products with non-toxic, but more competitive, fungal strains (Scott, 1989). (iv) Non-pathogenic fungi have been shown to induce defense responses that protect plants against pathogenic organisms (Bailey and Deverall, 1971; Keen, 1975; Bailey et al., 1980; Pirozynski and Hawksworth, 1988; Stretch, 1989). (v) Horizontal gene flow may occur between fungi and plants (Pirozynski, 1988). For instance, genes putatively transferred from Myrothecium fungi to the tropical shrub Baccharis are responsible for the plant’s ability to produce mycotoxins in the seed coat (Jarvis et al., 1989). Such interactions among plants, phylloplane, endophytic and potentially pathogenic micro-organisms are presently poorly understood, and virtually all information has been derived from applied horticultural studies (Pirozynski and Hawksworth, 1988; Pandey, 1990). The distinction between

54


pathogens and mutualists may become blurred in nature, as intermediary and facultative interactions may be common (Carroll, 1988). Nevertheless, the potential exists for positive interactions among plants and microbial associates with respect to defense against herbivores and pathogens (Pirozynski and Hawksworth, 1988; Wicklow, 1988). The commonness of superficial yeast-like, bacterial, and latent (endophytic) infections of fleshy fruit suggests possible roles for these micro-organisms in the inhibition of predators and pathogens that may entirely destroy flowers or immature fruits (Newhook, 1957; Janisiewicz, 1988; Stretch, 1989; Cipollini, 1991; Wilson er al., 1991). If so, plants may tolerate infection by micro-organisms that provide fitness benefits through their negative effects upon more damaging biotic agents (Carroll, 1988).

3. Selection for Antimicrobial Defense of Ripe Fruit As discussed at the outset, selection pressure by frugivores on fruiting plants is likely to be due to broad-scale disperser selective pressure, rather than by species-specific coevolution. Although fruit-frugivore interactions appear to be complex in nature, numerous laboratory and field studies have demonstrated that vertebrates can be very selective when foraging. Animals commonly make foraging choices that reflect slight differences in nutrient chemistry, palatability, size, design, color, and presentation pattern (cf. Duncan, 1960; Turcek, 1963; Berthold, 1976; Sorensen, 1983, 1984; Levey et al., 1984; Blem and Shelor, 1986; Herbst, 1986; Bairlein, 1987; Levey, 1987a, b, c; Borowicz, 1988a, b; Chai, 1988; Levey and Karasov, 1989; Martinez del Rio et al., 1989; Roper and Cook, 1989; Whelan, 1989; Willson and Whelan, 1989; Willson et al., 1990; Buchholz and Levey, 1991; Cipollini, 1991; E. Stiles, unpublished). Despite these observations, we are still uncertain about the extent to which even broadly divergent selective pressures due to frugivore foraging preferences and patterns effect variation in chemical and physical characteristics of fleshy fruits. Like plant-animal interactions, plant-animal-fungus interactions in seed dispersal systems may be complex (Pirozynski and Hawksworth, 1988). Fruits that remain undispersed eventually succumb to microbial attack; like most defenses of plant organs, fruit defenses are often overcome by microbes in nature (Janzen, 1977; Stiles, 1980; Herrera, 1982a). Assuming that foraging animals make choices among available fruits, differential seed dispersal (fitness) among individual plants, resulting from differences in their susceptibility to fruit rot, should result in selection for protection from microbial degradation. Generally speaking, plants should be under selection pressure to avoid fruit rot in order to increase retention time, or to otherwise enhance dispersal by volent or arboreal dispersal agents.


55

4. Retention of Structural and Chemical Defenses Selection pressure for the avoidance of fruit rot can result in diverse adaptive defense mechanisms. According to Herrera (1 982a), there are four basic mechanisms for the defense of ripe fruit: (i) To ripen fruits when pest pressure is lowest. (ii) To reduce the exposure time of ripe fruits to damaging agents. (iii) To reduce the nutritive quality of tissue for pests and pathogens by providing unbalanced, or poor quality fruits. (iv) To retain some degree of structural or chemical defense. Because many traits of fleshy fruits, unlike those of most other plant parts, are thought to have evolved specifically for the attraction of vertebrates (Bate-Smith, 1972; Swain, 1978; but see Pirozynski, 1988), retention of toxic compounds during fruit ripening has been generally considered to be a compromise between optimal defense and optimal attraction (Dement and Mooney, 1974; Herrera, 1982a; but see Janzen, 1975). Plants may vary in their ability to recover defense chemicals from senescent leaf and stem tissues, and microbial growth may be affected by the residual chemical make-up long after abscission (Wong and Kwan, 1980; Bernays et al., 1989; Harper, 1989; Blair et al., 1990). Reduction or alteration of secondary defense constituents during fruit ripening may be a similar non-adaptive result of senescence. Alternatively, patterns of secondary chemistry in ripe fruits may be influenced by selective pressures relating to dispersal. If dispersal-related selective pressures are an important influence on defense traits of ripe fruit, then interspecific variation in defense should be related to broad differences in dispersal patterns, or “syndromes” (sensu van der Pijl, 1969). Janzen (1979, for instance, suggested that secondary chemicals within fruit tissue may act to “filter” out non-effective dispersers or seed predators from more functional dispersal agents. In the sense of this discussion, fruit-rot agents may be thought of as seed predators (Janzen, 1977; Janzen, 1979). Secondary chemistry of plant tissues may also vary with respect to extrinsic environmental conditions via proximate physiological mechanisms (Ballinger and Kushman, 1963; Devlin et al., 1969; Rossiter, 1969; Lawanson et al., 1971; Kushman and Ballinger, 1975; Camm and Towers, 1977; Margna, 1977; Chew and Rodman, 1979; McClure, 1979; Jones, 1984; Mancinelli and Rabino, 1984; Jensen, 1985). However, such variation may be a response to evolutionary pressures (Rhoades, 1979; Coley et al., 1985; Coley, 1986). For instance, Vanderplank (1984) suggests that the susceptibility of cultivated plants to pathogenic disease is primarily a result of artificial selection for high reproductive output, which results in tradeoffs with resistance factors. According to Vanderplank, the “low-sugar’’

56

M. L. CJPOLLJNI A N D E. W. STJLES

disease syndrome in cultivated species is caused by artificially high levels of reproduction that tax carbohydrate supplies, and thus make reproductive plants more susceptible to pathogens. When plants are further stressed due to poor growth conditions or damage, defenses against pathogens may be compromised. Vanderplank also suggests that under natural selective regimes plants are much more in balance with their disease agents, and thus rampant disease is rare. These observations indirectly support the hypothesis that defenses are costly, and that they should be expressed in direct relation to fitness benefits relative to those costs (sensu Rhoades, 1979).

IV. GENERAL HYPOTHESES AND PREDICTIONS

A. General Deterrent Nature of Fruit Rot Although anecdotal evidence suggests that animals may sometimes be attracted to rotting fruit (Janzen, 1977; Pirozynski and Hawksworth, 1988), the nutrient alteration and secondary metabolites produced by fruit-rot fungi should generally result in fitness costs to consumers (Janzen, 1977). When rotting ripe fruit, fungi should generally exhibit negative effects upon potential consumers (Borowicz, 198813; Buchholz and Levey, 1990; Cipollini, 1991). Nevertheless, fungi that cause rot may vary considerably in the degree of deterrence produced, and in the degree of defense allocated against them by plants. Although all fungi should demonstrate direct negative effects at the time fruit rot occurs, indirect positive effects upon plant fitness may result from fungi acting as biotic defenses against pathogens during flowering and green fruit stages, and against more deterrent fruit-rot fungi in the ripe fruit stage.

B. Microbe-specific Defenses Retention of chemical defense in ripe fruits has been considered a compromise of simultaneous selection for the maintenance of palatable and nontoxic fruit pulp for frugivores, and defense against pests and pathogens (Janzen, 1977; Herrera, 1982a). It is well known that immature fruits accumulate various classes of defensive compounds, many of which are catabolized, translocated, or detoxified by complexation during ripening (Goldstein and Swain, 1974; Dement and Mooney, 1974; Janzen, 1977, 1983; McKey, 1979; Eltayeb and Roddick, 1984; Roddick, 1987). Because secondary compounds are often toxic and deter vertebrates, retention of chemicals with these properties is considered to be maladaptive. It follows that chemicals with


57

antifrugivore effects should be at a low level in ripe fruit (McKey, 1979), with an accompanying increase in nutrients and attractants (e.g. non-bioactive colors, odors and flavors (van der Pijl, 1969; Batesmith, 1972; Wilson and Thompson, 1982; Newsome, 1990; Sinki and Schlegel, 1990). But as we have discussed, microbial pathogens likewise have the potential of reducing the palatability and increasing the toxicity of fruits to frugivores. Retention of features that have little or no effect upon dispersal agents (microbe-specific defense) should result from dispersal-driven selection for antimicrobial defense (Janzen, 1975, 1983). Simple examples of microbe-specific defenses include the concentration of defenses in fruit skin (for reasons addressed previously), osmotically high levels of organic metabolites, and waxy ‘blooms’ that promote water-shedding or otherwise inhibit fungal spore germination and penetration (Burkhardt, 1982; Janzen, 1983; Willson and Whelan, 1989). The evolution of microbe-specific toxins is also within the range of possible results (Janzen, 1983). Palatability is not a unique feature of a specific chemical or chemical group, but most likely a manifestation of selection in animals to recognize resources that provide large fitness benefits, with little or no toxic effects (Bate-Smith, 1972; Janzen, 1979; McKey, 1979). Thus, plant species under selection pressure to provide nutrient-rich fruits as a means of attracting frugivores, should likewise be under selection pressure to defend pulp with secondary chemicals having little or no negative effects to dispersers. Microbe-specific chemical defense should thus be likely in plants that require high palatability for effective dispersal, yet are at high risk of fungal attack due to intrinsic or environmental factors. Conversely, plant species that depend upon mimicry of high-quality species, or that are otherwise under low selection pressure to provide rich resources to obtain dispersal, may be under less selection for palatability in defense chemistry (Rhoades, 1979; Lundberg and Astrom, 1990).

C. Interspecific Variation in Defense Effectiveness Selective pressure for antifungal defense in ripe fruit can result in at least two outcomes: (a) quantitative increases during ripening in the retention of secondary compounds already present in immature fruit, or (b) qualitative chemical changes that arise de n o w during fruit maturation. Assuming that a response to selection in either direction may increase overall defense effectiveness, we propose two alternate models for predicting the magnitude of the result.

1 . Relative-risk Model This model assumes that variation in chemical and physical characteristics of vertebrate-dispersed plants primarily influences the relative risk of microbial

58


rot (potential rotting rate), and thus the degree of selection pressure for antimicrobial defense. Under this model, selection for antimicrobial defense should be highest for plants whose fruits are at high risk of rotting due to nutrient content, water content, season of ripening (environmental conditions), or ripening synchrony.

2. Removal-rate Model This model assumes that variation in chemical and physical characteristics primarily influences preferences and removal rates by frugivores, and thus the degree of selection for antimicrobial defense. Under this model, selection for antimicrobial defense should be high for fruits that are less preferred due to low nutrient quality, or are for other reasons removed slowly by frugivores. Being more “apparent” to fungal rot agents (sensu Feeny, 1973), such fruits are expected to exhibit a higher level of defense. While these models are not necessarily mutually exclusive, they provide an appropriate initial framework for making predictions concerning the relative influence of selective factors upon secondary defense of ripe fruits.

V. PREDICTIONS FOR TEMPERATE SEED DISPERSAL SYSTEMS

A. Temperate Fruiting Classes Fleshy-fruited plant species of eastern North America have fruiting patterns that are influenced by many factors, including temporal fluctuations in frugivore type and availability, and temperature, humidity, and moisture (Stiles, 1980; Stiles and White, 1982; Willson and Thompson, 1982; Rathcke and Lacey, 1985; White, 1989). While some plants have fruits available for dispersal by resident frugivores (summer and mid-winter), the majority of species ripen fruit during fall migration, when highly mobile birds are in need of high-energy food sources (Thompson and Willson, 1979; Stiles, 1980). Stiles (1980) and Stiles and White (1982) suggested that vertebratedispersed plants of the northeastern United States differ enough in ripening patterns, fruit design, and fruit nutrient quality to fall into four broad fruiting classes: (a) summer small-seeded ( S S ) , (b) summer large-seeded (SL), (c) fall high-quality (FQ), and (d) fall low-quality (FL). The characteristics and the significance of this temporal classification were extensively reexamined by White (1989). Table 1 provides a summary of the physical and chemical characteristics of these classes as determined in this reanalysis. Both Stiles (1980) and White (1989) included the majority of temperate species in the nutrient-poor FL class. Fruits of FL plants were reported to be slowly or sporadically removed by fall migrant, winter resident, or spring migrant

Table 1 Mean chemical and physical characteristics of fleshy fruits of temperate northeastern North America (adapted from Stiles, 1980; Stiles and White, 1982; White, 1989). Chemical data are mean estimates for water-soluble carbohydrates (CHO), petroleum ether-soluble lipids (lipid), and protein from micro-Kjeldahl analyses of total nitrogen (protein) presented as per cent of dry pulp mass Fruiting class Summer species: Small-seeded (SS) Large-seeded (SL) Fall high-quality (FQ) Fall low-quality species (FL): Herbaceous Deciduous Evergreen Waxy Sumac

Fruit mass (mg)

Pulp water

CHO

Lipid

(%)

(%I

(%I 0.4 29.7

590 515 248

3 89 81

86 81 65

62.8 49.5 20.2

375 317 321 26 18

58 36 48 15 10

87 76 62 13 14

26.5 42.7 40.2

1.1

1 .O

1.2 2.4 1.2 44.0

8.8

15.1

Protein

3.5 3.4 6.7 5.4 4.0 4.1

3.3 2.6

6 ZE

60

M . L. CIPOLLINI AND E. W . STILES

birds. The FL class includes such species as Ilex opaca, Crataegus crusgalli, Rhus fyphina and Smilax rotundifolia. A small group of other fall-fruiting species, including Cornus Jlorida, Lindera benzoin, Nyssa sylvatica, and Sassafras albidum, were placed in the FQ class. The FQ class was noted for rather synchronous ripening patterns coinciding with peak fall migration, and high-lipid pulp. The summer groups (SS and SL), notably Vaccinium spp., Gaylussacia spp., Rubus spp., and Prunus spp., are reportedly taken by summer resident birds and mammals, tend to ripen asynchronously, and contain high levels of carbohydrates and water. Within this chapter, we refer to this seasonal classification primarily to focus arguments concerning the potential influence of interspecific variation on selection for defense characteristics, and not in an attempt to evaluate the significance of the grouping per se.

B. Predictions for Temperate Species I . Deterrence ox and Defense against Fruit-rot Fungi Regardless of fruit nutrient chemistry or season of fruiting, fruit-rot fungi should always produce direct negative effects upon feeding by frugivores. Antifungal characteristics and chemical defense should thus be common in fruit tissues. However, fungi may vary considerably in their negative effects, and thus fruit defenses should be allocated in direct relationship to costs to seed dispersal resulting from particular fungal infections. Thus: (a) higher levels of defense should be allocated against agents causing loss of immature fruit, relative to those infecting ripe fruit, (b) antifungal defenses should fall for ripening fruit, as removal by frugivores and successful seed dispersal becomes probable, (c) within ripe fruit, defense should be directed primarily against fungi that are toxic and deterrent, with lower levels of defense directed towards agents with only slight deterrent effects, and (d) fungal species having indirect positive effects because of interactions with other micro-organisms or pests should be tolerated more than fungal species with strictly negative effects. In a study of temperate Ericaceous species bearing avian-dispersed fleshy fruits, we have accumulated data that generally support the prediction of variation among fungal species. Plant species examined in this study included three summer (SS) species: Vaccinium corymbosum (VC), V. vacillans (W), and Gaylussacia frondosa (GF), and three fall (FL) species: Vaccinium macrocarpon (VM), Caultheria procumbens (GP), and Arctostaphylos uva-ursi (AU). Based upon feeding trials in which surface-sterilized fruits were inoculated with a suite of fruit-rot fungi (Table 2), fruit rot was generally deterrent to avian frugivores (Fig. I ) . However, consumption of rotted fruits varied significantly among the fungal species used to inoculate the fruits (Fig. 2), with putatively toxic fungi being more deterrent to frugivores than

Table 2 Fungi used in fruit rot and antifungal tests. For identification of plant species, refer to text. “Field plate” refers to aerial spore collection plates placed in the field during the ripening season ~

Species name

Plant source

Symbol

Groupa

Alternaria tenuis Nees. Aspergillus niger Tiegh. Botrytis cinerea Pers.: Fr. Colletotrichum gloeosporioides De Vries Cladosporium cladosporioides Penz. & Sacc. Fusarium sporotrichioides Sherb. Geotrichum candidum Link. Penicillium spp. No. 65 Penicillium rubrum 0. Stoll Pestalotiopsis maculans Nag Raj Phoma vaccinii Dearn & House Rhizopus stolonifer Vuill. Saccharomyces cerevisiae Sacc. Phomopsis spp.

Rotted VC fruit Rotted VC fruit Rotted VC fruit Rotted VC fruit Rotted AU fruit Field plate Rotted G F fruit Rotted G F fruit Field plate Rotted VM fruit Rotted VM fruit Rotted G F fruit Rotted VC fruit Rotted VC fruit

ALT ASP BOT COL CLD FUS GEO PNU PNR PES PHM RHP SAC UNK

TOX TOX NON NON NON TOX NON TOX TOX NON NON NON NON TOX

Putative toxicity status (TOX= “toxic”, NON= “non-toxic”) based upon literature reports for each genus (Rodricks, 1976; Marasas and Nelson, 1987; Hsieh, 1989; Mills, 1989; Tanaka and Ueno, 1989; Yabe et al., 1989).

a

62


SUMMER- SPECIES: AUG.-SEPT. 1986

0

5

ROlTEDFRUlT INTACT FRUIT

4

3

A

2

F

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PLANT SPECIES Fig. 1. Effect of artificially induced fruit rot on consumption of summer (SS) and fall (FL) Ericaceous fruits by captive birds in 1986. Data are mean numbers of fruits consumed in pairwise (five rotted: five intact) 15-min feeding trials with summer fruit species using catbirds and veeries, and fall fruit species using robins, across nine fungal species (n=6-16 replicates of each fruit: fungus combination). The effect of fruit state (rotted vs. intact) was significant in full factorial ANOVA for both summer (F= 1354.15, P < 0.0001) and fall (F=425.83, P < 0.0001) fruits. Identical letters denote means that did not differ significantly ( P > 0.05) based upon Bonferroni Ttests. For key to plant species, refer to text.

z W

2 w P

w

t

0 U

FUNGAL SPECIES Fig. 2. Proportion of rotted fruit eaten by captive birds during feeding trials in 1986 (refer to Fig. I ) , showing differences among fungal species. Results are means for each fungus across all birds. The effect of fungal species was significant in full factorial ANOVA for both summer (F= 179-56, P

40

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20

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PLANT SPECIES Fig. 4. The effect of fungal toxicity status on the degree of antifungal activity present in secondary extracts of ripe fruit pulp. Data are mean radial mycelial growth of “toxic” and “non-toxic” fungi on media containing secondary ethanolic extracts (test agars), relative to growth on media (control agars) that mimicked the nutrient makeup of each fruit species (n = 2 replicates for each fruit: fungus pair). The effect of fungal toxicity status was significant in nested ANOVA (i.e. toxicity status, with fungal species nested within toxicity status: F = 6.33, PI >

.'without switch

Time

Successional change m vegetationlenvironmenl ~n accelerated b y the action 01 a switch

Successional change in vegelal~on/environmen! 8s delayed b y Ihe a c l m 01 a switch

Fig. 2. Four possible vegetational switches produced by switches (outcomes).

the edge of water bodies or lava flows, or between ultramafic and normal soils. Gleason (1939) denied that there were ever sharp vegetational changes without a causative sharp environmental change (or change in immigration pressure). However, it is not always possible to find environmental changes sharp enough to explain observed sharp vegetational changes. We suggest here that many sharp vegetation changes are due to a boundary between two systems being reinforced or sharpened by a switch. Sharp temporal boundaries are also seen, when one type of vegetation is stable for a long period, and then is relatively quickly replaced by another type. We suggest many sharp temporal boundaries are due to switches.

D. Vegetational Situations Produced by Switches There are four possible ecological outcomes of the operation of positivefeedback switches:

POSITIVE-FEEDBACK SWITCHES IN PLANT COMMUNITIES

269

(A) Stable mosaic situation (Fig. 2A). Where there was previously a uniform environment, switches can produce different communities, separated by sharp and stable boundaries, probably in a mosaic. Community X establishes at some sites by chance, and its modification of the environment ensures it holds the sites. Elsewhere, community Y establishes, and probably because of its different modification of the environment also holds its sites. Thus the mosaic is stable. This is similar to the theoretical concept of “several stable points” (Lewontin, 1969) or “multiple stable points from one initial condition” (Sutherland, 1974), though in such papers the involvement of the environment has not generally been elaborated. Some plant ecologists have discussed such mechanisms. Nicholson et al. ( 1 970) referred to “pasture differentiation”, Jackson (1 968) to an “unstable point” in succession (i.e. a switch between alternative pathways), Westoby (1980), Westoby et al. (1989) and Wedin and Tilman (1990) to “alternative stable states” caused by feedback. Wilson and Fitter (1984) speculated on “an element of unpredictability [in] the successional sequence”, and Bornkamm (1988) suggested that seasonal events could act as a switch, affecting the course of succession for several years. Type 1 switches cannot lead to stable mosaics, because community X can always expand. However, there can be a temporary mosaic when invasion is incomplete. Switch types 2 4 can produce stable mosaic situations, because the environment simultaneously changes in community Y (or bare) patches. (B) Sharpening situation (Fig. 2b). Where there was originally a gradual environmental boundary, a switch can produce a sharp vegetational boundary. All four switch types could have a sharpening effect. ( C ) Acceleration situation (Fig. 2c). If a switch is operated by invading species, their invasion can be accelerated. This operates by invading community (e.g. sera1 stage) Y changing the environment to make it more suitable for community Y, and less suitable for the previous community, X. If there is patchy initial invasion by community Y, a temporary mosaic may result, or the switch effect may allow some lateral spread from random invasion by Y, again giving a temporary mosaic. Any of the four types of switch could produce an acceleration situation. (D) Delay situation (Fig. 2d). Existing species, by operating a switch, could delay vegetational change; for example, a switch could delay succession, prolong the effect of initial patch composition, or delay the response to climate change. This operates by community X changing the environment to keep it more suitable for community

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J. B. WILSON AND A. D. Q. AGNEW

Table 1 Mediating agencies in switches Physicakhemical switches: Water PH Soil elements Light Temperature Wind Fire Allelopath y Biological switches: Microbes Termites Herbivores

(e.g. seral stage) X, and less suitable for the succeeding community, Y. In a multi-stage succession, a community that modifies its environment to its own benefit could both accelerate its own invasion and delay its replacement by the next seral stage. A delay situation could result in a temporary mosaic if there is some patchiness in community X. Any of the four types of switch could produce a delay situation. The delaying effect of switches has been observed by Nicholson (1970) (“the inertia of Nardetum to successional change”), and on a longer timescale by Cole (1985) (“Vegetation inertia is . . . enhanced because a climax vegetation type . . . can create a microclimate favourable to its own members”).

E. Agencies We have attempted to categorize switches as far as possible by the agency involved. We can distinguish between physicakhemical switches and biological switches (Table 1). However, the distinction is not always clear cut. For example, some allelopathy hypotheses involve direct toxicity, others are suggested to involve effects on soil microbes, and some may do both. We give examples of the four types of switch and the four outcome situations described above, as we discuss switches caused by different agencies. Some examples will be speculative, and these we offer as hypotheses for testing, as a plan for a research programme.


27 1

111. WATER-MEDIATED SWITCHES A. Concept Increased water availability, up to an optimum, generally increases vegetation mass, and increased vegetation mass can sometimes increase water availability, producing a positive-feedback switch. Enhancement of water availability by vegetation can take place through two mechanisms: fog precipitation (Section B) or increased infiltration (Section C). A water-mediated switch can also operate through sediment entrapment (Section D), ombrogenous bog growth (Section E), or snow accumulation (Section F).

B. Fog Precipitation 1. Concept Fog precipitation (occult precipitation, fog drip, fog trapping) is the impaction of small droplets from low cloud or fog. This process can enhance water input to tall vegetation, compared to adjacent low plant cover (Vogelmann, 1973). This could be a significant source of water input in arid areas with frequent fog (Vogelmann et al., 1968). If the increased water input favours the growth of taller vegetation, the elements of a switch are present, and a sharp boundary can develop between the two vegetation types (Figs 3, 4). Such a switch might explain the very existence of forest in an arid zone (Kummerow, 1962).

2. Evidence: Vegetation Boundaries The presence of a sharp vegetation boundary often indicates that a switch is operating. There are many landscapes in the tropics with hilltop forest patches amid grassland, often with the boundary abrupt (van Someren, 1939; Miller et af., 1988-Chyulu hills, Kenya; Sugden, 1982-coastal hills, Caribbean coast of South America). Probably, the primary factors are higher rainfall precipitation and lower evapo-transpiration on the hills, but fog precipitation may reinforce the environmental difference, and sharpen the boundary (Fig. 3). Often, the boundary coincides with the lower limit of frequent cloud, as in parts of the Ecuadorian Andes (Grubb and Whitmore, 1966). If the boundary is due to fog precipitation, moisture availability should also show a sharp boundary (Fig. 3). This has sometimes been seen: for example, Means (1927) found the soil of a Californian hillside to be wetter beneath trees than 3 m away from the trees, in grassland.

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J . B. WILSON AND A . D. Q. AGNEW

Higher precipitation and reduced evapotranspiration higher up the hill allows taller vegetation.

The taller vegetation traps fog precipitation, and further increases water status higher up the hill.

Higher water status allows taller vegetation.

.- .* . . . *

*

Fig. 3. A fog precipitation switch.

3. Evidence: Tall Vegetation Enhances Water Input Evidence for water enhancement comes from observations of gr 3 er water collection in gauges that have plant shoots fixed into them (Phillips, 1926) or those with gauze/wire placed in the gauge to catch fog (Marloth, 1904; de Forest, 1923; Nagel, 1956; Twomey, 1957; Vogelmann et a/., 1968; Vogelmann, 1973; Merriam, 1973; Cavelier and Goldstein, 1989). The water input enhancement can be quite large: for example, 67% in the case of Vogelmann

273


0 Water input greater

Tall Vegetation

1.

LJ vegetation

Fig. 4. A water (fog precipitation) switch on a hillside in the montane tropics (type 1, one-sided).

et al.'s (1968) experiment at 1100 m in mountain cloud forest of Vermont.

Kummerow (1962) suggested an extraordinarily high rainfall enhancement (from 0.9mm to 50mm) under a forest patch in Chile. Often, it has been observed that enhancement is greater in periods of low rainfall (e.g. Vogelmann et al., 1968; Vogelmann, 1973), making it clear that the water enhancement is from fog, not from rain. Lysimeters can also give evidence when those containing plants, or containing taller species, collect more precipitation. For example, in upland tussock grasslands in New Zealand, 2&60% more water is collected under tall Chionochloa rigida tussocks than under lower Poa colensoi cover or bare soil (Mark and Rowley, 1976; Holdsworth and Mark, 1990). Other evidence comes from observations that effective precipitation under trees is greater than that in the open (Oberlander, 1956; Costin and Wimbush, 1961; Ekern, 1964; Harr, 1982; Vis, 1986; Wright and MuellerDombois, 1988). Sugden (1982) observed drips from the vegetation during fog, with wet soil beneath. Where records are detailed enough, it can often be seen that such effects occur even in periods with no rain (Marloth, 1907; Parsons, 1960), again making it clear that the precipitation enhancement is from fog, not from rain. Results with isolated gauges/lysimeters/trees, or on the edge of forest, may be misleading if they are merely catching water that would have fallen nearby anyway. Some studies have suggested this, reporting fog drip to be much greater at the edge of a forest than further in (Rutter, 1975). However,

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J . B. WILSON AND A. D . Q. AGNEW

Marloth ( I 907) discounted this by showing that some precipitation enhancement was recorded by gauges in the centre of a bush thicket or a reed field, be it lesser enhancement than with gauges in the open. Fog precipitation may also input nutrients (Holdsworth and Mark, 1990) or salt, which could contribute to the switch.

4 . Evidence: Enhanced Water Input Results in Taller Vegetation Phytomass, vegetation height and density are all normally higher under higher rainfall (Beard, 1969; Branson, 1975; Shmida and Burgess, 1988), especially in arid climates, though the link between rainfall and vegetation height declines once the vegetation becomes woody (Webb et al., 1978). It is difficult to obtain more than circumstantial evidence of this in fogliable situations. There is spatial correlative evidence, such as Marloth’s (1 904) observation that the higher mountains, where he obtained his fogcatching results, bore much denser vegetation than at lower altitudes. Oberlander ( 1 956) suggested from casual observation that fog catch enabled orchids and tree seedlings to grow beneath trees. Prat (1953) observed that the dune vegetation was not nearly so luxuriant in southern California as on the Monterey Peninsula, where fogs are more frequent. Temporal correlative evidence was obtained by Means ( 1 927), who found that “pine” and Eucalyptus sp. trees were slow-growing at first, but faster subsequently (even though it was during dry years), and attributed this to the water they collected (the larger the trees were, the better fog collectors they were). It is possible that ontogenetic changes were also involved, or perhaps an accumulation of litter.

5. Rainfall Interception by Impaction In a similar way, plants can intercept near-horizontal rainfall, and thus increase local water input. However, since this rain would have fallen nearby anyway, there can be only a local increase in water input. Such a process might cause a temporary, small-scale mosaic. If forest cover in an area increases total rainfall, the process might operate on a landscape scale.

6. Conclusion We see this as a type 1 (one-sided), switch, because tall vegetation traps fog precipitation and short vegetation does not. The elements of the switch are: (i) the taller community changes the environment by increasing the water input: this has been demonstrated; and (ii) this change is relatively more favourable for the taller community than for the shorter one: this has been surmised.


275

The switch seems generally to result in a situation B, sharpening, situation, though on a landscape scale mosaics can result, as in the Chyulu Hills, Kenya (van Someren, 1939; Miller et al., 1988). In theory, the switch could lead to accelerating (C) or delaying (D) situations, but these are harder to observe. To the extent that the fog precipitation caught would have fallen in an adjacent area anyway, the switch can be seen as a reaction (type 2) switch.

C. Infiltration 1. Concept Vegetation may trap surface rainfall runoff on gentle slopes, increase its infiltration, and perhaps reduce evaporation, thus increasing water availability to plants. This has been documented from many arid countries (White, 1971). The process can be seen with a patch of vegetation, or around a single plant base. Increasing infiltration will lead, in arid areas, to increased plant cover.

2. Evidence Belsky (1986) described a possibly “endogenous” mosaic in Serengeri grasslands of East Africa, attributing it mainly to rainfall infiltration effects. The dense Andropogon greenwayi community produces more phytomass, with higher soil organic matter content and infiltration rates, than the open Chloris pycnothrix community. This gives a possibility of a water switch, in which the Andropogon state has higher phytomass, which increases the water input, which favours the Andropogon state-positive feedback. The missing link would be experimental evidence that the wetter soil favours the Andropogon. Belsky suggests that the mosaic is initiated by patchiness in soil leaching. The mosaic disappears if grazing is prevented, so a grazing switch may also be involved. Mosaics apparently caused by an infiltration switch can be in the form of bands/arcs of vegetation alternating with bare ground (e.g. Tongway et al., 1989-semi-arid eastern Australia; Cornet et al., 1988-Chihuahuan Desert, Mexico). In Somalia, Boaler and Hodge (1964) found that the vegetation/ bare boundary in such a mosaic is sharp on the uphill edge of the vegetation band, but more diffuse on the downhill margin. When the soil crust of bare areas is dry, heavy rainfall can run downhill in a sheet and collect against the uphill edge of a vegetated arc. Water infiltration under the vegetation can be five times deeper than in bare areas, further assisted by “potholes” in vegetated areas (Boaler and Hodge, 1964), and perhaps soil cracks and higher soil organic matter (Cornet et al., 1988). However, Glover et al. (1 962) found that water infiltration occurred more readily beneath bare areas, and attributed the higher water status below grass cover to funnelling of rainfall

276


by grass leaves, the rain being caught by the leaves and running down them to the base of the plant. This mechanism suggests that expansion of the vegetation should take place at the uphill boundary, and drought-induced dying off at the downhill boundary, so the arcs should advance uphill. There is evidence for advance at rates of 0.3-1 myear-’ (Worrall, 1959; Glover et al., 1962; Boaler and Hodge, 1964; Cornet et af.,1988), though in some areas there seems to be no movement (Boaler and Hodge, 1964). The vegetation mosaic can be of many different shapes, perhaps with different origins, but apparently always caused by an infiltration switch (Wickens and Collier, 1971). The initiation and maintenance of such a mosaic often occurs together with other switch mechanisms, including termites, grazing (Glover et al., 1964), soil structure, aeolian soil/sand accretion (Boaler and Hodge, 1962), nutrient accumulation (Tongway et al., 1989), and salt accumulation (Boaler and Hodge, 1964), though the latter workers suggested initiation by random gaps appearing in vegetation as the climate became drier.

3. Conclusion This can be seen as a type 2 (reaction) switch, in which: (i) dense vegetation increases infiltration, and hence water availability, and also stops runoff, reducing water availability downslope of it; and (ii) increased water availability favours (or enables) the growth of the dense vegetation. There is still only limited water, which is absorbed by the stripes. This prevents the vegetation extending to cover the area, so that in a sense the vegetation makes the bare areas drier, the type 2, reaction effect. The result is usually situation (A), a mosaic, though there could also be situation (B), a sharpening of an altitudinal trend.

D. Sediment Entrapment: Salt Marsh Pans 1. Concept Vegetation can trap water-borne sediment, and sediment deposition can increase vegetation growth by nutrient input, by decreasing waterlogging or by decreasing salinity, giving a switch (Fig. 5).

2. Evidence Yapp and Johns (1917) commented that intertwined shoots of the salt marsh “meadow” sward are very effective in silt binding. Depressions in the bare silt before colonization represent, they suggested, incipient primary bare pans.

Bare pan

Salt meadow

I I I I I Bare pan

meadow spp. favoured

I

conditions for salt meadow spp.

I

Fig. 5. A water (sediment entrapment)/salt switch with salt pans on a salt marsh (type 2, reaction).

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J . B . WILSON AND A. D. Q. AGNEW

They tend to remain filled with tidal water for longer, the silt in the bottom is mobile, and salinities will tend to be more extreme, all of which inhibit the growth of vegetation, and the pans therefore remain bare. Such pans are effectively permanent unless the drainage system changes. Although Yapp and Johns saw cases of pans filling in with vegetation, in every case it was because a drainage outlet had been established. On the salt meadow, sediment entrapment can raise the soil level and allow other communities to invade, so facilitation succession can occur simultaneously. Pethick (1 974) suggested that secondary pans could also arise, when a patch of turf died and the silt eroded, but this supports the switch concept: when the vegetation can no longer mediate, the environment reverts.

3. Conclusion This is a type 2, reaction switch in which: (i) vegetation traps silt, builds up the soil surface and thus reduces tidal inundation, whilst increasing water ponding and maximum salinity in the pans; and (ii) a higher surface in the salt meadow provides more favourable growth conditions for the salt meadow vegetation there, and more unfavourable conditions in the pans. It is a reaction switch because the silt buildup both reduces inundation on the salt meadow, and by building up the pan walls increases it in the pans. It produces a mosaic (A) situation, or at least sharpens (situation B) and makes permanent small initial substrate differences. There are elements of a salt switch here too.

E. Ombrogenous Bog Growth 1. Bog Growth Ombrogenous bogs are those, often dominated by Sphagnum spp., that are dependent for their water and nutrient inputs on precipitation. Once peat buildup raises the bog surface beyond influence of the water table, the rainleached substrate becomes nutrient-deficient and acid (Tallis, 1983). Sphagnum spp. can tolerate, or even require, such conditions (Clymo, 1973). Their growth and peat accumulation raises the bog surface even further from water table influence, completing a landscape-scale switch. Tallis (1983) suggests that the entry of Sphagnum is the critical stage, because of the ability of Sphagnum species to lower the pH of the substratum, though he cites evidence that other mosses can d o this too, perhaps acting as precursors for Sphagnum species. The cycle is broken only if the climate changes or perhaps


279

if the bog “bursts” (Barber, 1981). The Sphagnum also acts as a “sponge”, retaining water. Because of the long time-scale involved, the processes have been inferred rather than observed. Bellamy and Rieley (1967) obtained evidence close to the event by examining a small ombrogenous Sphagnum hummock that had established in a fen. Stratigraphy suggested that two non-Sphagnum mosses had established a low hummock, which “deflected the main flow of ground water”. They may also have started acidification. When the hummock was about 0.05 m high, Sphagnum spp. invaded, leading rapidly to acid peat that was above the influence of the ground water, perhaps within 10 years. The mechanism has elements of water, pH and nutrient switches.

2. Hummocks, Hollows and Pools It is possible that a similar switch sometimes operates on a much smaller scale. Many bogs comprise a mosaic of hummocks, hollows, and perhaps deeper pools. Early suggestions were of cyclic succession between hummocks and hollows (Osvald, 1923; Watt, 1947). However, several workers have found that, at least in the bogs they examined, stratigraphic evidence did not support such a cycle (Walker and Walker, 1961; Barber, 1981); rather the whole bog surface responded to climatic change. Some have found evidence that, directly contrary to the cyclic succession hypothesis, the sites of hummocks continue to be hummocks, likewise those of hollows and pools to be hollows and pools, for thousands of years, in some cases through the life of a bog (Casparie, 1972; Boatman and Tomlinson, 1977; Moore, 1977; Barber, 1981; Svensson, 1988; Foster and Wright, 1990), and perhaps reflecting the underlying topography (Boatman et al., 1981; Boatman, 1983). Thus hummocks, hollows and pools could be alternative stable states, indicating the existence of a switch. (Distinction should be made between small vegetated hollows and large bare pools, but the principle is similar for our purpose, and the distinction is not clear-cut.) The switch could be based on greater productivity by the species of a hummock (Wallen et al., 1988), resulting in a surface buildup on hummocks at least as fast as that in the hollows (Boatman and Tomlinson, 1977, though the evidence from their different methods is equivocal-Barber, 1981; Moore, 1989). Probably more importantly, dead hummock material tends to decompose more slowly (Clymo, 1965; Moore, 1989; Johnson et al., 1990; Rochefort et al., 1990; Johnson and Damman, 1991). In larger pools, bare of vegetation, surface buildup is due to gyttja accumulation, which can be at a lesser rate than peat accumulation on hummocks (Foster and Wright, 1990). The story is confused, with some experimental evidence not supporting either the cyclic succession or the switch interpretations (Clymo, 1973; Hayward and Clymo, 1983). Possibly, several factors are involved, with different results on different bogs.

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(--A

0

I

Soil pH

Calluna etc.

lower

favoured Fig. 6. A pH switch controlled by Calluna vulgaris, CJ1e.u europaeus, etc. (type 1, onesided).

F. Snow Accumulation If the vegetation affects snow lie, and the community which attracts the deepest snow is also the most tolerant of it, a switch is possible. Payette (1988), in northern Quebec, gave stratigraphic evidence for rapid changes in vegetation cover, after long periods during which he suggests a selfmaintaining state of a Picea marina and Sphagnum fuscum cycle. The snow accumulation by the krummholz-type Picea stands increases the moisture available to the Sphagnum, which allows peat to be deposited, with a consequent rise in the surface level. Eventually a “dramatic change” (his words) occurs when the surface is raised level with the central plateau of the ombrotrophic mire system. At this point, the Picea is no longer able to layer, the peat becomes “fossil” without current addition, and the permafrost layer rises. This leads to tundra yegetation dominated by Cladina spp. (mainly C . rangijierina and C . stellaris) and Alectoria ochroleuca. This is a one-sided switch (type I), where the PicealSphagnum maintains itself until a limit imposes fragility. The tundra lichen vegetation does not operate a positive feedback mechanism, except in so far as it does not trap snow.

IV. pH-MEDIATED SWITCHES 1. Concept Species of low base-capacity soils may have litter or roots which acidify the soil, and be tolerant of acidity and its associated conditions, producing a positive-feedback switch (Fig. 6 ) .


28 1

2. Evidence Pigott ( 1 970) suggested that Deschampsia flexuosa invades Festuca ovinal Agrostis capillaris grassland by producing an unpalatable litter which eliminates the soil comminution organisms (e.g. earthworms, thrips). This changes the humus type from mull, with large pore spaces, to mor, with small, easily waterlogged spaces. The resulting hypoxic conditions reduces the pH, releasing manganese, to which the Deschampsia may be tolerant (Ernst and Nelissen, 1979), but not the Festuca nor the Agrostis. Grazing checks the invasion, and the resulting balance is a mosaic of grassland types. Calluna vulgaris, Erica cinerea and Ulex europaeus produce litter which can acidify the soil (Wilson, 1960; Grubb et al., 1969; Miles, 1985), probably by removing calcium and other bases (Grubb and Suter, 1971). The former two are acidophilous species, growing well on acid soils (Marrs and Bannister, 1978). Ulex europaeus often occurs on soils of pH 4-5 (Etherington, 1981), is tolerant of the high aluminium availability that is associated with low pH, and is susceptible to lime chlorosis (Grime and Hodgson, 1969). The competitive ability of all three species, compared to more calciphilous species, would therefore be greater after the acidification process. Similarly, Corynephorus canescens acidifies the soil in which it grows, and from its distribution appears to be acidophilic (Rychnovska, 1963). It is therefore confined in some areas to soils of low pH-buffering capacity, the pH of which it can modify. A similar process is seen in ombrogenous bog formation as described above.

3. Conclusion These are apparently type 1 (one-sided) switches, with elements: (i) species X acidifies the soil; and (ii) species X is more tolerant of acid soil than the species previously dominant. Records are sparse of the spatial arrangement of these communities. With a type 1 switch, one would not expect to find a stable mosaic. If a grazing switch were present too, the switch could be of type 4 (two-factor), capable of producing a permanent mosaic.

V. SOIL-ELEMENT-MEDIATED SWITCHES

A. NPK Increase 1 . Concept The possibility exists for a species to increase the nutrient content (especially N) of the soil, and to be favoured by that change because it is more

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responsive in its growth to enhanced nutrient supply-a switch.

positive-feedback

2. Evidence Often the soil below savannah trees is more nutrient-rich than that below the matrix grassland (Parker and Muller, 1982; Belsky et al., 1989). Kellman (1979) ascribed this to differential capture of precipitation NPK inputs. Charley (1972) found that Atriplex vescaria in arid parts of Australia withdrew N from the surrounding soil, adding it to the soil directly beneath its canopy. J.J. Barkman (personal communication) suggested that the invasion of Dutch heathlands by Juniperus communis is accelerated and stabilized by its ability to raise the pH, P and K of the soil. However, for none of these examples is there evidence that the nutrient-accumulating species is more responsive to nutrients. Wedin and Tilman (1990) and Tilman and Wedin (1 991a) found different soil nitrogen availability in plots planted with different species. The two species which produced the lowest N availability were those which had a high competitive ability for N (Tilman and Wedin, 1991b). This seems to be good documentation of an NPK switch, though it is not clear whether the switch is an increase or decrease in NPK.

3. Conclusion There is evidence for a one-sided (type I ) switch in which: (i) a plant species raises the NPK status of the soil; and (ii) the increase in NPK status favours that species. It is not clear what vegetation situations it leads to.

B. N P K Decrease 1 . Concept A species that lowered NPK availability, and could tolerate low availability, could operate a positive-feedback switch.

2. Evidence Heilman (1966, 1968) recorded abrupt boundaries between Alaskan woodland on mineral soil and that on Sphagnum. He suggested that Sphagnum invaded woodland. This led to a reduction in the N, P and K status of the surface layers, largely because the low specific gravity of the Sphagnum peat resulted in a low nutrient content per volume, the nutrients being situated in the lower, colder layers of the soil. Moreover, the insulating properties of Sphagnum peat resulted in permafrost much nearer the surface. Thus, the nutrients present were much less available to the trees. There was a pH


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change too. Lower nutrient availability lowered tree growth and switched the woodland into muskeg bog. The disappearance of the trees increased light levels, favouring the Sphagnum again. Heinselman (1970) suggested the same effect for North Minnesota. Bonan and Korzuhin (1989) modelled such a boreal system. In their simulation the system was very sensitive to interactions between mosses, trees and the environment; the insulating property of the moss layer was particularly important. These effects are switches from minerotrophic to ombrotrophic, from young to old successional types and are often triggered by small changes in climate or geomorphological balance. Wilson and Fitter (1984) proposed an effect of Sphagnum in a bog in northern England. They suggest that, where Sphagnum colonizes, pH is reduced. This reduces P availability, largely by suppressing microbial cycling. Lower P availability favours the Sphagnum. Where LoniceralRubus vegetation colonizes, the higher pH enhances P availability, favouring the species present. Thus, pH, nutrients and microbes are part of the switch.

3. Conclusion These are one-sided (type 1 ) switches, in which: (i) Sphagnum reduces nutrient availability, and lowers pH; and (ii) the lower nutrients and pH favour Sphagnum. There are elements of NPK, pH, temperature and microbial switches. In the North American examples, the switch is suggested to lead to situation ( C ) , acceleration of (“retrograde”) succession. There are some indications of an (A) mosaic situation, which could not be explained by a one-sided switch, but the shading effect of the trees could possibly make this a two-factor (type 4) switch, theoretically capable of generating a permanent mosaic. The English example could be a symmetric (type 3) switch, capable of producing a permanent mosaic.

C. Heavy Metals 1. Concept Among plants tolerant of heavy metals, e.g. those found on ultramafic soils, some accumulate heavy metals to considerable concentrations. Such plants are termed “hyperaccumulators”. They have the potential to build up toxic elements in surface litter and soil, and thus prevent invasion by an alternative, less-tolerant community, producing a positive-feedback switch (Fig. 7).

2. Evidence Several elements have been found to be hyperaccumulated (Table 2). The concentration of heavy metal in the plant dry material can exceed the total concentration of heavy metal in the parent rock or in the soil (Table 3).

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accumulated in hence in litter I

0 Available heavy metal in soil greater

Hyperaccumulator dominated patch

species suppressed

Fig. 7. A soil nutrient (heavy metal) switch controlled by plants that hyperaccumulate heavy metals (type 1 , one-sided).

Concentrations in the plant ash are even higher in comparison with rock or soil, and it is the plant ash content that is more relevant once the leaves fall and decay. Even values below 1.0 in Table 3 may represent an increase in plant-available heavy metal if the litter-derived heavy metal is in a simple soluble mineral form. This suggests that litter from heavy metal accumulators may increase the soil levels of available heavy metal, though we know of no investigation of this. (However, litter decomposition may be slow, and lower specific gravity of litter, in comparison with mineral soil, might counteract the effect.) The accumulators are presumably tolerant of high internal levels of the heavy-metal they accumulate, though there may be some internal compartmentalization. Many hyperaccumulators are confined to metalliferous ground (Brooks et a/., 1981). Psychotria dourarrei,which can contain 2.2% nickel in its leaves, can tolerate I % nickel in solution in its root medium (Baker et al., 1985). Hyperaccumulators might therefore be favoured, in competition with other species, by an increase in heavy-metal availability. If such a switch operated, we would expect to find that communities dominated by hyperaccumulators formed pure stands, and they often do (Baker and Brooks, 1989). We would expect sharp edges, and possibly temporary mosaics. We know of little information on this, though Duvigneaud and Denaeyer-de Smet (1963) describe “copper clearings” of herb communities in forest, and their photographs show sharp boundaries. It is possible that this reflects an equally sharp change in the original soil, though


285

Table 2 Records of hyperaccumulation. Element concentrations are the maximum found, usually of leaf material (weight:weight basis) Element

Concentration

Source

(%I In dry matter

1 .o

Cobalt Copper Lead Manganese Nickel Selenium Zinc

Brooks et al. (1987) Malaise et al. (1979) Reeves and Brooks (1983) Jaffre (1 979) Jaffre and Schmid (1974) Cannon ( 1960) Reeves and Brooks (1983)

0.6 0.8 5.5 4.7 0.6 4.0

In plant ash Chromium Molybdenum

4.8 1.7

Uranium

2.5

Wild ( 1 974) Warren and Delavault (1 965) Whitehead and Brooks ( 1 969)

Table 3 Values reported for hyperaccumulators of the ratio of the element concentration in the plant to that in the soil in which the plant is growing (weight:weight basis) Element

In dry matter Lead Manganese Nickel Zinc In plant ash Chromium Copper Nickel Uranium

Concentration Concentration in in plant soil W) (Yo) 0.8 3.3 2.3 2.0 4.7 1.7

4.8 1.2 0.02 40.6 15.3 2.5

0.30 1.50

0.46 0.33 0.37 1.70 12.50 c. 1 . 1

0.00 1 0.37 0.55 3.65

Ratio

2.7 2.2 5.0 6.1 12.7 1 .o

0.4 c. 1 . 1 20.0 109.7 27.8 0.7

Source

Reeves and Brooks (1983) Jaffri (1977) Jaffre ( 1 977) Baker et al. (1985) Jaffre and Schmid ( 1 974) Reeves and Brooks (1983) Wild (1974) Wild (1 974) Wild ( 1 974) Jaffre and Schmid (1974) Wild (1974) Whitehead and Brooks ( 1969)

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J. B. WILSON AND A . D. Q. AGNEW

the process of upward diffusion of copper that they describe makes this less likely.

3. Conclusion This would be a one-sided (type 1) switch in which: (i) the hyperaccumulator produces litter, and hence soil, high in available heavy metals; and (ii) it can tolerate this, but less tolerant species cannot. We do not know what situations it would lead to, but it should tend to sharpen soil boundaries (situation B).

D. Salt 1. Concept Species that salinify the soil, and are tolerant of salinity, could operate a positive-feedback switch.

2. Evidence: Cohune Palm The cohune palm, Orbignya cohune, dominates patches of woodland on lowlying, deep soils in Belize, sharply demarcated from dicotyledonous forest on slopes (Arnason et al., 1984). This palm produces a dense shade. Its abundant leaf litter has a very low nitrogen content but a salinity “approaching values for mangrove forests in brackish water”. This gives a soil sodium content greater than in the “high bush forest”. Some palms are tolerant of salinity (Arnason et al., 1984), and, if this applies to the Orbignya, a switch could be operating. On the rather different grounds of soil turnover and humus accumulation, Furley (1975) suggests that the Orbignya “appears to develop the soil in which it is best suited to grow”-a clear suggestion that there is a positivefeedback switch operated by this palm through the soil environment. Low light at the soil surface, caused by the palm litter, may also be part of the switch mechanism.

3. Evidence: Arid Shrubland Kovda et al. (1979) suggested that in arid regions worldwide the vegetation tends to cause the accumulation of soluble salts in the upper soil layers. He particularly cited an example from the Karakum Desert where Haloxylon aphyllum and H. persicum litter adds up to 80 g m-* year-’ of salts to the soil surface, mostly sodium carbonate and bicarbonate. This gives a pH of 8.59.0. If the Ha/o.xy/on species are more tolerant of such salts than other species nearby, a switch could result, though that has not been demonstrated. Westoby (1980) suggested that in the inter-mountain region of the USA the exotic annual Halogeton glomeratus absorbs salt from lower soil layers,


287

and by its litter creates high salinity at the surface that it can tolerate, but that the native shrub Kochia americana cannot. Soils in such areas are indeed salty at depth (Kearney et al., 1914; Cook, 1961). The succulent leaves of the Halogeton are high in minerals, especially sodium oxalate (Morton et al., 1959; Cronin, 1965). Thus it has the potential to add salt to the surface in litter, as shown by comparison of Halogeton areas with non-Halogeton areas, and by experimental addition of Halogeton litter (Eckert and Kinsinger, 1960). However, such an increase in salinity by the Halogeton has not yet been unequivocally demonstrated. Cook (1961) found the percentage of total soluble salts in soils below a community of the Halogeton with scattered Kochia shrubs to be higher than in soils below Artemisia tridentata, but since this difference was more pronounced at the deeper soil depth it was probably due to pre-existing conditions. Charley and West (1975) did demonstrate that plants of Atriplex confertifolia, in the same part of the USA, increased the salinity of soil around their canopies. The demonstration of a switch would also require evidence that Halogeton glomeratum is more salt-tolerant than Kochia americana, etc., and indeed it is, at least at germination (Williams, 1960; Cronin, 1965; Clarke and West, 1969). This has been used to explain why re-invasion of the Kochia is prevented in areas where it could re-establish before the advent of the Halogeton (Kearney et al., 1914; M. Westoby, personal communication). Other species, sown into Halogeton swards, have failed to germinate (Eckert and Kinsinger, 1960). One sign of the operation of a switch is a mosaic (situation A), and this can occur, with islands of dense Halogeton amongst Artemisia tridentata (Cook, 1961).

4 . Evidence: Mesembryanthemum in Grassland In South Australia, Kloot (1983) showed by field and plot experiment that the exotic Mesembryanthemum crystallinum, invading annual pasture, increased the salinity of the soil below its canopy. This reduced the growth of other species in the community. It also reduced its own growth, though to a lesser degree. Vivrette and Muller (1977) provided similar evidence from annual grassland in California, showing that salt was released from dead, dry Mesembryanthemum by rain or fog-precipitation leaching. Again, the Mesembryanthemum was more tolerant of such leachate than other species of the community. They suggested that the Mesembryanthemum invaded when climate and grazing had opened the community, and that the salt switch retarded re-invasion of the grassland species-a delay (D) situation.

5 . Conclusion This seems, if operative, to be a type 1, one-sided, switch, in which:

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J . B. WILSON AND A. D. Q. AGNEW

Closed canopy

I Light at ground level

Fig. 8. A light switch on a NSW (Australia) salt marsh (type 1, one-sided).

(i) the salt-accumulator absorbs salt from a distance around itself, or from depth, and by its litter increases the salinity of the nearby surface soil; and (ii) the salt-accumulator is better able to tolerate this salinity than other species. A one-sided switch can explain the sharp boundary of the Orbignya forest. It can delay vegetation change (situation D), as in the Mesembryanthemum situations. It can lead to mosaics as in the Halogeton example, but these are only temporary because there is nothing to stop the continued invasion of the salt-accumulator. However, when accumulation of salt is from areas lateral to the plant, salt is reduced in the unoccupied areas, forming a type 2, reaction, switch, capable of producing the mosaics observed.

VI. LIGHT-MEDIATED SWITCHES 1. Concept A theoretical construct for a positive-feedback light switch would be two communities, one open, one closed, where the species belonging to the open community could establish only in full light, and those of the closed community could establish only in shade (Fig. 8).

2. Evidence In the Sierra Madre, Mexico, Goldberg (1982) describes how an open woodland of Quercus spp. with almost evergreen leaves occurs on ridges with


289

dry acid soils, separated by a very narrow ecotone (2-18 m) from more mesic deciduous woodland on deeper, more nutrient rich soils. The soil pH changes much more gradually than the vegetation across the boundary. She suggests that the boundary is sharpened by the inability of both the deciduous flora to establish in the poor acid soils below evergreens, and the seedlings of the evergreen trees to establish in the shade of the mesic woodland. Her observations indicate a similar light environment under both canopies, and she hypothesises that a slow growth rate of evergreen seedlings, and possibly higher shade cast by the richer ground flora of herbs in the deciduous woodland, are enough to account for the effect. Red/far-red ratios may also play a part. Another example of a soil-induced gradient, sharpened by a light switch, is seen in the very sharp boundaries between communities along a salt marsh gradient near Sydney, Australia (Clarke and Hannon, 1971). Although the species differ in salinity tolerance, this cannot account for the sharpness of the boundaries. Clarke and Hannon found that the low herb Arthrocnemum australasicum (= Salicornia australis) was very intolerant of shade and this was a major cause of the abrupt change from Arthrocnemum meadow to Avicennia woodland on the seaward side, and from the Arthrocnemum to Juncus maritimus fen on the upper margin (Fig. 8). Thus, a salinity gradient establishes the species’ positions, but the boundary between communities is sharpened by a light switch; the tall species create shade, and can regenerate under it. In other cases, the initial boundary may be formed by chance establishment. Niering and Egler (1955) described a Viburnum lentago thicket which had established in an oldfield about 30 years earlier. Once the Viburnum canopy was established by “fortuitous distribution of . . . propagules”, low subcanopy light levels (and rabbit grazing) prevented the entry of other species. The Viburnum could reproduce by root suckers. However, Niering and Egler admitted that the exclusion was not complete, and that eventually trees would invade, and later found evidence of this (Niering et al., 1986). Westoby (1980) describes a desert grassland in the southwest USA where, without grazing, Prosopis velutina (mesquite) shrubs cannot invade. Grazing opens the grass cover, and Prosopis shrubs establish. When grazing is removed, the Prosopis shrubs prevent re-establishment of the grass cover. Prosopis can regenerate in its own shade, perhaps because of its large seed. The existence under no-grazing conditions of two alternative stable states, depending on previous conditions, suggests that a switch is operating. Westoby suggests competition for light, and fire, as factors, though wind erosion and competition for water could also be involved. Westoby (1980) also reports a very similar situation in the understorey of some Callitris and Eucalyptus woodlands in arid parts of eastern Australia, where grazing of the grass understorey has led to an increase of Cassia and

290


Eremophilu shrubs. When stocking rates are reduced, the grass is unable to return, probably because of shading by the shrubs. Harrington and Johns (1990) gave indirect evidence for such suppression. Light switches can also occur via litter. For example, below Mt Hiuchidake, Japan, bamboo (Susa spp.) can inhibit the regeneration of Fugus crenutu (Tanaka, 1988). This is probably due to litter, not the shade of living plants, since light intensity in Susa thickets is higher than in shrub or tree communities at 1.5 m above the ground, but much lower than in these other communities at the soil surface. Root competition, and perhaps allelopathy by the Sum litter, may also be factors. However, the Susa patches can become smaller due to edge invasion by trees, and periodic flowering and death of Sum might disable the switch.

3. Conclusion Goldberg’s example could be a two-factor (type 4)switch, involving pH and light, though leading only to a sharpening (B) situation. The other examples are type 1, one-sided switches, in which: (i) a woody species reduces the light intensity on the ground, (ii) the woody species can tolerate this low light, and regenerate, but other species cannot. This can give a sharpening situation (B) or in the case of the Viburnum and Prosopis examples a delay situation (D).

VII. TEMPERATURE-MEDIATED SWITCHES A. Concept Tall vegetation can reduce fluctuations in air temperature near the soil surface. If this favours gtowth or re-establishment of the same species because they are less cold-tolerant than their neighbours, a positive-feedback switch can occur. We consider this for treeline and for graminoid tussocks.

B. Treeline 1 . Concept The altitude of alpine timberline is correlated in many parts of the world with a mean air temperature of 10°Cduring the warmest month (Schroeter, 192326; Daubenmire, 1954) (though temperature may be partly a proxy for other factors). Sometimes, treeline is sharp, suggesting a switch is operating.


29 1

0 Frost less severe

Forest

A

LJ Tree seedlings

Fig. 9. A temperature switch at treeline (type I , one-sided).

2. Evidence An explanation of the mechanism might be that the tree cover ameliorates the microclimate, so that temperatures on clear calm nights are lower in the open than under a tree canopy, and lower than the limits of cold tolerance for the tree species (Fig. 9). Wardle (1985b) demonstrated this in New Zealand for Nothofagus solundri, which can form a very sharp timberline (Wardle, 1965). In that case the low temperatures in the open are known to be lower than the cold tolerance of the species. Therefore, seedlings survive under trees but not amongst low vegetation at the same altitude, unless they are experimentally sheltered from frost when young (Wardle, 1965, 1985a). One sign of a switch is that a vegetational pattern, once disturbed, is not restored, or only very slowly. The treeline temperature switch would therefore explain why after fire, etc. treelines are often much lower than previously (e.g. Plesnik, 1978).

3. Conclusion This is a type 1 (one-sided) switch, in which: (i) trees ameliorate frosts beneath them, (ii) the tree species’ seedlings are less tolerant of frost than those of abovetimberline species. As a type I, one-sided switch, it cannot produce a mosaic in a uniform environment, but it can sharpen (situation B) the effects of an altitudinal (or other environmental) gradient. Apparent inertia of treeline to climate change

292


(Kullman, 1989) suggests a delay (D) situation can arise too, though slow invasion, e.g. limited by mycorrhizal availability, could be important.

C. Graminoid Tussocks Chapin et al. (1979) show that tussocks of Eriophorum vaginatum in the Alaskan Arctic tundra have a higher temperature during late spring and summer than does inter-tussock vegetation, while Oberbauer and Miller (1979) demonstrate that tussocks of this species have a buffering effect against temperature (and water) fluctuations. Both effects lead to a longer growing season. Tussock growth is limited mainly by temperature and light, not nutrients (Fetcher, 1985), and is thus correlated with the number of degree days (Mark et al., 1985). Therefore the plants’ environmental modification can lead to increased plant growth, representing a switch. However, it has not been shown that the Eriophorum is more able to respond to increased temperature than the surrounding species. The temperature buffering would give a type I , one-sided switch, perhaps leading to a (C) acceleration situation if the Eriophorum were invading, and explaining the dense tussock fields reported (e.g. Oberbauer and Miller, 1979). Alternatively, radiation interception would lead to shading of other plants, a type 2 (reaction) switch, capable of producing a vegetation mosaic, though there seem to be no reports of this.

VIII. WIND-MEDIATED SWITCHES A. Concept Vegetation can dissipate, concentrate or redirect wind energy and thus (section B) change the aeolian erosion, transport and trapping of soil materials, or (section C) reduce direct damage to vegetation, in either case potentially producing a positive-feedback switch.

B. Soil Erosion and Trapping 1 . Concept Vegetation can trap soil, and deeper soil encourages plant growth, giving the possibility of a switch.

2. Evidence Marshall (1970) provides a model of the relations between shrub height and width and its effect on wind speed, showing that there is a minimum density for shrubs of each size class below which soil erosion will occur. His field


293

stands were in the winter-rainfall saline rangeland of southern Australia where mainly Chenopodiaceous shrubs form stands with patchy openings which are very slow to revegetate due to topsoil loss. The shrubs trap soil, and therefore grow better-a switch. Agnew and Haines (1960) and Agnew (1961) showed that the trapped soil around shrubs in Iraqi desert had a higher nutrient content than the surrounding soil, and that this led to increased production and presumably more entrapment of dust. This was especially the case under Haloxylon salicornicum, a Chenopodiaceous shrub forming patches of vegetation in hollows in an otherwise stony subdesert surface. The switch sharpens the topographic effect, so that scattered shrubs in hollows become small dune systems in the hollows, with sharp edges. The shrubs eventually degenerate and seedlings re-establish better on the deposited soil than on the open desert surface. The patch of dunes bearing the Haloxylon may not spread indefinitely because there is not enough blown material, and the life of a plant of the Haloxylon on the open stony desert surface is too short, but in any case the observed stands were limited by grazing pressure. Westoby (1980) suggests that in some arid perennial grasslands, the root mat can prevent soil erosion by wind and water. If overgrazing occurs, perennials are replaced by ephemerals which cannot hold the soil, which is therefore eroded. It is difficult for the perennials to become re-established. Harrington and Johns (1990) suggest an interaction with fire, in that the reduced herbaceous growth could not produce enough standing crop to sustain a fire. The lack of fire favours shrubs, which suppress the herbaceous plants further. Westoby (1980) points out that a wind-mediated switch occurs without grazing on sand dunes: when vegetation is removed the dunes become mobile, and vegetation cannot readily re-establish. In secondary succession in the New Zealand alpine, the grass Poa colensoi can form mounds by trapping aeolian silt (Roxburgh et al., 1988).

3. Conclusion The elements of the switch are: (i) the plants trap and/or hold the soil; and (ii) this favours plant growth. This is basically a type 1, one-sided, switch. However, the limited amount of fine material may produce a type 2, reaction, switch, capable of producing the mosaic (A) situation seen in the southern Australian shrublands. The Iraqi desert example is a sharpening (B) situation, with the initial differences caused by topography. Westoby’s grassland example seems to be a delay (D) situation, since recovery from grazing is delayed.

294

J . B. WILSON A N D A. D. Q. AGNEW

C. Wind Damage to Plants 1. Concept Wind damage is very significant near alpine tree lines and in Arctic taiga. We may postulate that the presence of shrubs or trees creates an ameliorated microclimate within the canopy which allows those species to grow and reestablish (Fig. 10).

2. Evidence In the alpine tundra, wind-deformed trees (e.g. Picea engelmannii, spruce), occur as compact islands of krummholz (Wardle, 1968). Sometimes, the plants are arranged in lines parallel to storm winds, showing the importance of wind (Minnich, 1984), which is high above treeline, especially in winter (Wardle, 1968). Sometimes other species are associated with the islands (e.g. Ribes montigeum-Marr, 1977). The islands are packed with snow in winter, whereas much of the open tundra is blown free of snow (Wardle, 1968). This snow accumulation has considerable sheltering effect; above the snow there is basipetal death of exposed needles and shoots during the winter, a process highly correlated with wind (Hadley and Smith, 1983). The krummholz is also self-sheltering, with much less damage (stem breakage, needle death and crown dieback) on undercanopy and leeward branches (Minnich, 1984). It is not clear which effect of wind is most important. Temperatures are higher within a krummholz plant, at least in terminal meristems (Grace, 1989), than in the open tundra (Wardle, 1968; Hadley and Smith, 1986). Low winter temperatures could kill needle tissue directly (Wardle, 1981; McCracken et al., 1985; Tranquillini and Plank, 1989), though others have doubted this explanation (Hadley and Smith, 1983). Wardle (1968) hypothesized that low summer needle temperatures resulted in incomplete needle maturation, and hence winter damage. Though there is evidence for this (Baig and Tranquillini, 1980), Hadley and Smith (1986) disproved it, at least in their situation. Tranquillini (1980) suggested the damage is caused primarily by desiccation. Windward needles can have lower winter water content, lower water potentials, lower cuticular resistance and faster transpiration (Hadley and Smith, 1983, 1986). Others have doubted this explanation (Marchand, 1972; Marchand and Chabot, 1978; Kincaid and Lyons, 1981; Hadley and Smith, 1986). There is also a direct mechanical effect of wind, especially of ice crystals on cuticular wax (Hadley and Smith, 1983, 1989). However, Wardle (1968) doubted whether this was a significant cause of needle mortality, and Hadley and Smith’s (1989) results show only weak correlations between wax erosion and leaf death. Inter-branch rubbing and rime ice also cause damage (Marchand and Chabot, 1978).

Krummholz

Tundra

I I I

I I

I

I Fig. 10. A wind switch in alpine krummholz/tundra (type 2, reaction).

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J . B . WILSON A N D A. D. Q. AGNEW

It seems likely that more than one environmental factor is involved (Hadley and Smith, 1986); treeline is marginal for tree growth, making the plant susceptible to a range of adverse factors that may differ from place to place and from species to species. In any case branches and leaves can ameliorate wind abrasion and/or low temperature and/or desiccation, directly and via snow accumulation, and this enhances plant growth. If this were simply a type I , one-sided, switch, there could be no permanent mosaic, since patches could expand. Increased wind speeds between the shrub/tree patches due to funnelling could produce a type 2, reaction, switch. However, we have found no confirmation of this. If conditions in the open tundra prevent plant growth, there is a question of how tree islands become established. Marr (1977) had evidence for the intriguing suggestion that tree islands form in more sheltered microsites, in which a seed has germinated, but then by vegetative reproduction climb out and move along the ground onto exposed microsites. The islands can move at 1-2 cm year-' (Benedict, 1984).

3. Conclusion The elements are: (i) krummholz islands reduce wind and thus increase temperature and/or reduce desiccation and/or reduce abrasion, (ii) this favours the tree species, rather than the tundra species which are more tolerant of cold and/or desiccation and/or abrasion. The presence of an apparently long-term mosaic (A) situation suggests a reaction (type 3) switch is indeed operating.

IX. FIRE-MEDIATED SWITCHES

A. Concept Vegetation adapted to burning may be very sharply distinct from an adjacent non-flammable community because of an abrupt change in fire regime at the boundary. Boundaries between the two vegetation types could of course shift, depending on fire frequency and rainfall fluctuations, and yet in many places in the dry subtropics seem to be very stable (Lawton, 1964; van Zinderen Bakker, 1973), suggesting the delaying (D) outcome of a positivefeedback switch. A fire boundary often occurs where there is an underlying gradual change in soil nutrient or water status, so that fire is forcing an ecocline (limes divergens of van Leeuwen, 1966) into a linear edge, producing a limes


297

convergens, an ecotone. This suggests the sharpening (A) outcome of a switch. Nevertheless, in order to demonstrate a switch, vegetation must be shown to maintain itself by either encouraging or limiting fire (Fig. 11). There is evidence for both these features. Firstly, Mutch (1970) suggests that certain vegetation is adapted to promote and survive fire better than alternative vegetation. Mutch points to the higher calorific content and lower water content of Eucalyptus spp. and Pinus ponderosa, compared with mesophytic vegetation, as evidence of this. However, Bowman and Wilson (1988) failed to find evidence to support Mutch’s hypothesis, and Snyder (1984) and Troumbis and Trabaud (1989) questioned its logic. Jackson (1 968) and Kellman ( 1 984) suggest another mechanism: the progressive loss of nutrients during a long history of fires in vegetation. Moreover, Kellman reviews neotropical savannahs and suggests that nutrientdeficiency can lead to vegetation of higher flammability. The opposing feature, the maintenance of non-flammability, is shown by certain forest types which are difficult to burn except in rare very dry years, due to lack of fuel for the fire because of fast litter humification in a humid microclimate (Ewel, 1976; Kessel, 1976; Bowman and Minchin, 1987). The best evidence for a fire switch comes from the closed-forest/savannah ecotones of Australia and Africa, and they will therefore be discussed in detail.

B. Australian Closed-forest/Savannah 1. Introduction In parts of Australia, closed rainforests and Eucalyptus-dominated sclerophyll savannah occur side-by-side, with boundaries perhaps only a few metres wide (Stocker, 1969; Unwin et al., 1985; Ash, 1988; Unwin, 1989). (We use the term “savannah” for consistency, though “woodland” would also be appropriate. Distinction could also be made between dry and wet sclerophyll communities.) The boundary can be floristically absolute: Smith and Guyer (1983) found that no tree species occurred in both savannah and closed-forest. In some cases, there can be a specific ecotone community also (Unwin, 1989). Such boundaries might remain stable for several thousand years (Mount, 1964; but see Unwin, 1989). Jackson (1968) described this boundary as an “unstable point, with ecological drift”, meaning that vegetation tends to drift to one or other of two stable states, each side of the “unstable point”, a concept very close to that of the switch. Usually, the general position of the closed-forest/savannah boundary is determined edaphically (e.g. with closed-forest on basaltic rocks and deep, fertile, well-drained soils), and/or climatically (Ash, 1988), with the fire

Closed-forest

Savannah I

I

litter

I I I Low light at ground level

Closed-forest

n

T9

0 Savannah

tires

II

tL> I

suppressed

I

\

pressed

/

Fig. 11. A fire/light(/nutrient) switch at the closed-rainforestjsavannahboundary in Africa or Australia (type 4,two-factor).


299

switch sharpening the boundary (Bowman and Minchin, 1987), though the nature of the boundary and the factors involved may differ across Australia (Bowman, 1988).

2. Evidence: Closed-forest Conditions One element of the switch is that fire does not occur in the closed-forest, or only on the outer edge (Gilbert, 1959; Smith and Guyer, 1983). When fires sweep across the savannah, the dense evergreen vegetation of closed-forest presents a fire barrier (Bowman and Minchin, 1987). Direct evidence for this comes from an experimental fire lit by Unwin et al. (1985): it became slow burning and of low intensity as it approached the closed-forest. Scorch and fire deaths declined across the boundary into the closed-forest. Under the shade of the closed-forest, closed-forest species can presumably regenerate, perhaps in small gaps. In contrast, savannah eucalypts cannot regenerate in low light (Jackson, 1968; Ashton, 1981; Fig. l l ) , Jackson suggesting that clearings of 25 m diameter were necessary before there was enough light for eucalypt seedling survival.

3 Evidence: Savannah Conditions In the savannah, fire is frequent now (Braithwaite and Estbergs, 1985), was frequent during settlement by Aboriginals (Stocker, 1971; Singh et al., 1981), and may have been almost as frequent before that due to natural fires (Kemp, 198 1; Walker and Singh, 198 I ) . Savannah species accumulate fuel faster than closed-forest species, though the fuel mass can be higher in closed-forest (Mount, 1964; Bowman and Wilson, 1988). Savannah species and fuel components also show lower water contents (Bowman and Wilson, 1988). Dickinson and Kirkpatrick (1985) found that the dry sclerophyll savannah species of Tasmania had a greater tendency to propagate fire, though Bowman and Wilson (1 988) found such species from Northern Territory had a lower energy content than closed-forest species, and were less flammable. It has been suggested that closed-forest species cannot regenerate in a regime of frequent fire (Fig. 11). For example, Clayton-Greene and Beard (1985) found more closed-forest and less savannah on Bougainville Peninsula, Western Australia, than on the mainland. The closed forest appeared to be invading the grassland, and they suggested this was because fire was less frequent on the peninsula (no evidence presented). On some offshore islands, not burnt for some time (they state) there were saplings of closed forest species. Stocker (1966) found that an area of closed-forest disturbed and burnt had no regeneration of typically closed-forest species, though he later observed that many closed-forest species can sprout after less severe fire (Stocker, 1981). In contrast, savannah eucalypts are thought to be able to cope with fire, by surviving as adults (Gill, 1981), by vegetative recovery, especially from

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J. B. WILSON A N D A. D. Q. AGNEW

lignotubers (Bowman and Minchin, 1987), or regenerating from seed (Cremer, 1962). Bowman (1986) suggested Eucalyptus tetrodonta regeneration was stimulated by fire; this may occur in other species too. An additional complication is that fire might reduce the nutrient content of the ecosystem by volatization, leaching and/or runoff, though the effect seems to be small (Norman and Wetselaar, 1960; Harwood and Jackson, 1975; Lacey et al., 1982). Jackson (1968) suggested this would favour eucalypts. In the short term, levels of other nutrients, especially P, can be higher after a fire (Humphreys and Lambert, 1965; Grove, 1977). Fire can also affect the microflora (Florence and Crocker, 1962). An interaction with termites may be important here, since Eucalyptus tetrodonta is very prone to termite attack (H. Gitay, personal communication), and fire might ameliorate this. Grazing can also interact, e.g. reducing fuel accumulation or preventing regeneration (Lacey et al., 1982), though at least Eucalyptus populnea density can be increased by grazing (Moore and Walker, 1972).

C. African Closed-forest/Savannah 1. Introduction For Africa, there is a rich literature on the role of fire in the maintenance of abrupt boundaries between closed-rainforest and savannah (Hopkins, 1983). Disturbance and grazing can reinforce the fire effect.

2. Evidence: Anthropogenic Savannah The present savannahs in Africa are largely derived by agricultural clearance of closed-forest. The sequence of events seems to be as follows: (i) Closed-forest is cleared for agricultural use, and after some years left fallow. (ii) The grassland which then develops is burnt by human agency. Grass is an ideal substrate for fire, especially after flowering, because standing culms form a fuel-air mixture. (iii) Fires at first erode the edge of the closed-forest, and can even enter the closed forest, but burn only the thin dry litter layers, damaging little within the canopy (Hopkins, 1965). (iv) The edge is sharpened firstly by rearrangement of flora to form a specialized, semi fire-resistant closed-forest border zone, particularly of evergreen lianas (e.g. Landolphia spp. -Trapnell, 1959; Hypoestes fastigiata-West, 1972). Secondly the grassland can alter soil water relations, making it more difficult for forest to re-invade. There is decreased infiltration of the high-density rainfall (Lawton, 1964) and thus lower effective precipitation, and also more effective use of surface soil water, denying it to the deeper tree roots (Knoop and Walker, 1985).


30 1

(v) The final result is a mosaic of closed-forest and grassland, sharply defined (Keay, 1951; Hopkins, 1983).

3. Evidence: Natural Savannah In view of the largely anthropomorphic origin of the present vegetation of the Sudanian Zone, it is doubtful whether the contention that this was the natural, pre-disturbance state of the closed-forest/grassland boundary can be proven (Clayton, 1958). However, Keay (1951) proposed that the present situation is one which formerly existed at the climatic boundary of closedforest vegetation and gave rise there to a mosaic of forest and grassland. van Zinderen Bakker (1973) describes relict forest patches in South Africa on steep slopes and in ravines, which have affinities with more equatorial montane forest. He demonstrates an ameliorated microclimate in which litter can decompose more quickly into a soil of high organic content. A mosaic could probably develop from grassland, as early or no burning leads, at least in West Africa, to establishment of fire-intolerant trees and a suppression of the fuel grasses, so that it becomes progressively more difficult to burn (Innes, 1972).

D. Conclusion In both the Australian and African examples, this is a type 4 (two-factor) switch, with elements for one factor: (i) the savannah increases the probability of fire by being drier and more flammable, (ii) the savannah is more tolerant of fire, and for the other factor: (i) the closed-forest decreases the light level on the ground, (ii) seedlings of species of the closed-forest are more tolerant of shade than those of the savannah. However, other switches are often involved, especially grazing ones. The switches can lead to mosaic (A) and,sharpening (B) situations. In theory they could produce a delay (D) situation, which the permanence of the boundaries suggests. The buildup of non-flammable litter in closed-forest could be seen as producing a type 3, symmetric, switch, depending on what is taken as the baseline.

X. ALLELOPATHY-MEDIATED SWITCHES 1. Concept Many plant species are suspected of maintaining the integrity of their own stand by allelopathic influence (Rice, 1984). This process represents a

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J . B. WILSON AND A . D. Q. AGNEW

toxins leached

Toxins temporarily in soil

other species Fig. 12. An allelopathy switch in southern Californian annual grassland (type I , onesided).

positive-feedback switch (Fig. 12). Allelopathy has especially been used to explain mosaics, and almost pure stands of one species, sometimes seen in semi-arid environments. The allelopathy has to be allo-allelopathy, rather than auto-allelopathy (Newman, 1978).

2. Evidence Bell and Muller (1973) describe a situation in southern Californian annual grassland (comprising species such as Avena fatua, Bromus mollis and B. rigidus), with patches of almost pure Brassica nigra reseeding themselves each year. Boundaries between grassland and the Brassica were often sharp. Bell and Muller failed to find explanation for the existence of the patches in soil pH, texture or temperature. Competition for water, nutrients or light seemed unlikely. They suggested that toxins from Brassica nigra were washed from dead standing Brassica by the first rainfall, and the toxins suppressed germination of the grasses at this critical time. Such toxicity was shown in vitro and also in soil. Removal of dead Brassica removed the suppression of grass germination. The existence of a mosaic with no apparent environmental correlation, and the sharp boundaries between communities, are suggestive of a switch. Williamson (1 990) suggests that in the chaparral of the southeastern USA coastal plain, allelopathy by the shrubs inhibits the growth of grasses and young pines, therefore reducing the fire risk to the benefit of the shrubs. This could be an allelopathy/fire switch, capable of producing the sharp ecotone that is seen.

POSITIVE-FEEDBACK SWITCHES IN P L A N T COMMUNITIES

303

However, many examples of allelopathy are suspect because they can be demonstrated in the laboratory but not in the field, where other environmental effects such as herbivory may be more important than any plant vs. plant toxin (Harper, 1977; Heisey and Delwiche, 1985), and where toxins may be broken down by the soil flora or absorbed by soil colloids. Bell and Muller’s (1973) study is not free from such criticisms. However, it seems extreme to dismiss allelopathy because the evidence is partial; evidence in ecology is rarely complete. A comparable switch could operate by one species bearing a virus, pest or disease, to which a second species was more susceptible (van den Bergh and Elberse, 1962; Rice and Westoby, 1982; Price et al., 1988). This moves the mechanism into the category of a biological switch.

3. Conclusion This seems to be a one-sided (type 1) switch: (i) a species produces an allotoxin; and (ii) the toxin inhibits the growth of other species, allowing greater growth of the toxin-producer. The literature often gives the impression of a mosaic (A) situation. However, a one-sided switch cannot give this. Perhaps there is an unobserved underlying environmental difference, and the situation is a sharpening (B) one.

XI. MICROBE-MEDIATED SWITCHES A. Oldfield Succession and Nitrogen-fixing Microbes 1. Concept Rice et a f . (1960) suggested that pioneer species in oldfields might tolerate low soil nitrogen. If they inhibited bacteria which fixed atmospheric nitrogen, soil N would remain low, favouring the pioneers over the later successional, and more N-requiring, species, halting or at least slowing succession (Fig. 13)-a positive-feedback switch.

2. Evidence In Oklahoma oldfields, succession after abandonment starts with an annual weed stage [Pl] (Booth, 1941; Kapustka and Rice, 1976). The annual grass stage [P2] follows, dominated by Aristida oligantha. The latter stage lasts 1124 years; attempts to reduce this time by seeding-in later successional species have not been successful (Booth, 1941). The following perennial bunch-grass

304


Inhibitors of N-fixing bacteria released

Soil N

L-

Bunch grasses of P2 stage cannot invade.

Fig. 13. A microbe switch in Oklahoma oldfields (type 1, one-sided).

stage [P3], often dominated by Andropogon scoparius, is eventually replaced by climax prairie [P4]. Succession to climax is incomplete after 40 years (Savage and Runyon, 1937). Rice et al. (1960) and Rice (1971) saw it as an ecological problem that the P2 annual grass stage so quickly displaced the robust species of the PI annual weed stage, and remained so long before invaded by the P3 perennial bunchgrass stage. They suggested that in this system cultivation led to a decrease in the N and P in the soil, so recently abandoned land was low in soil N. (Rice et al. (1960) refers to some evidence for this: a preliminary experiment at his site, and experiments by others at other, comparable sites.) N-fixation was then inhibited by substances from the P2 species. Plant extracts and sometimes leachates, inhibitory of the free-living Nfixer Azotobacter spp., can be found from species of the PI and P2 stages (Bromus japonicus, Digitaria sanguinalis. Chenopodium album, Conyza canadensis), though also in Andropogon scoparius and Erigeron strigosus of the P3 and P4 stages (Rice, 1964a, 1965b). Although the toxins were tested in vitro, the inhibitors were stable against auto-oxidation and decomposition by microbes (Rice, 1964a, 1968). Inhibition of bacteria of this genus may not be important, since Azotobacter generally makes little contribution to soil N (Evans and Barber, 1977), but overall N-fixing ability (measured by acetylene reduction) is indeed low in the field in the PI and especially P2 stages (Kapustka and Rice, 1976). Rice (1 968) also considered inhibition of Fabaceae/Rhizobium N-fixation. Extracts, dried plant material, root exudates and living plants of stage PI species Bromusjaponicus and Digitaria sanguinalis, and also the P2 dominant


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Aristida oligantha, reduced the nodulation of bean and clover plants. Unfortunately for the argument, there is no significant presence by Fabaceae in stages P1 or P2, though that could conceivably be due to Rhizobium inhibition. For some species, partial chemical identification of the inhibitors has been made (Rice, 1964b, 1965a,b; Rice and Parenti, 1967). However, questions must remain as to the reality of these effects in the field. The other link in demonstrating a switch would be to show that species of the early stages are more tolerant of low-nutrient conditions. Rice et ai. (1960) found that Aristida oligantha (P2) was less affected by N- or Pdeficiency than Andropogon scoparius (P3), which was in turn less affected than Panicum virgatum (P3 and P4). The low-nutrient tolerance of Aristida oligantha is supported by its low N- and P-concentration in the field (Harper et al., 1934). Effects of plant exudates in inhibiting nitrification are also possible. The soil concentration of ammonium N is highest in the climax, and nitrate N the lowest (Rice and Pancholy, 1972, 1973). This correlates with low Nitrosomonas and Nitrobacter numbers in climax soil. Extracts of species from P1, P3 and P4 stages are inhibitory to Nitrobacter and Nitrosomonas (Rice, 1964a, 1965b). However, no differential ability by species of different stages to use ammonium vs. nitrate has been shown. Other possible explanations for the speed of succession between the P2 and P3 stages include dispersal limitation (Rice et al., 1960), allo-allelopathy (Rice, 1984) and auto-allelopathy (Rice, 1971).

3. Conclusion This would be a type 1, one-sided, switch, in which: (i) the pioneers produce toxins, which inhibit N-fixing (etc.) bacteria, which keeps the soil N low, (ii) the low soil N favours the pioneer species in comparison to later successional species. One would not expect a mosaic (A) situation from a one-sided switch, and Rice does not mention mosaics. The situation is a delay (D) one.

B. Forests and Mycorrhizas Many plants, including forest trees, are dependent on mycorrhizal symbiosis for satisfactory growth. If the mycorrhizal fungus is not present in the soil at a site, they could not establish. Yet, the mycorrhizal fungi could not establish without a higher-plant host. This represents a positive-feedback switch. Perry et al. (1989) suggest that such a switch may operate when forest is removed;

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J . B. WILSON AND A . D . Q. AGNEW

enrich soil

increased

trees

Thicket with

I

nests in thickets

Fig. 14. One possibility of a termite switch in African savannah (type 1, one-sided).

the mycorrhizal fungi could be lost too, making it very difficult and slow for the trees to re-establish.

XII. TERMITE-MEDIATED SWITCHES 1. Concept Termites of many genera make a nest or hive in the centre of their foraging area. Sometimes, it is a raised mound. Plant material, litter and soil from the foraging area are brought back to the hive. This, and the termites’ creation of subterranean passages, amend the soil structure. These soil conditions may enhance the growth of woody vegetation. If the termites are themselves favoured by the higher productivity of the woody vegetation, then a positivefeedback switch exists (Fig. 14).

2. Evidence In many parts of dry tropical/subtropical Africa, scattered mounds occur in grassland. They are often referred to as Mima-like mounds, because of their superficial similarity to mounds on the Mima Prairie, Washington State, and in other North American grasslands, which may have been caused by gopher burrowing (Cox, 1984; Lovegrove and Siegfried, 1986). It seems likely that Mima-like mounds in Africa are occupied or abandoned termite (mainly Mucrotermes spp.) mounds (Darlington, 1985). The system has been called Termitensavanna (Darlington, 1985). However, this interpretation is surprisingly controversial (Gakahu and Cox, 1984; Berg, 1990).


307

In many areas, there is a mosaic with patches of trees/shrubs, often evergreen, scattered in the grassland, with a sharp ecotone (Morison et al., 1948; Lee and Wood, 1971a). Often, the patches are on Mima-like mounds. This suggests that mound conditions promote either colonization or survival of woody plants (Okali et al., 1973). The difference in mound conditions could be: (i) Nutrients: The soil of termitaria contains material harvested from the surroundings and from the subsoil (Hesse, 1955; Lee and Wood, 1971b). It is often nutrient-enriched (in N, Ca and perhaps P and K) compared to the surrounding grasslands (Watson, 1967; Lee and Wood, 1971a; Trapnell et al., 1976; Nutting et al., 1987; LopezHernandez er al., 1989). (ii) Soil aeration: The soil of termitaria is often finer and better aerated (Lee and Wood, 1971a). (iii) Soil moisture: This is often higher in termitaria, perhaps because of differences in rainfall infiltration (Glover et al., 1964) and in waterholding capacity (Lee and Wood, 1971a). (iv) Drainage: On some sites the intermound surface is seasonally waterlogged. (v) Temperature: Higher temperatures on mounds could encourage woody vegetation (Wild, 1952). (vi) Grazing: The height of the mounds might protect saplings from grazing (Lind and Morrison, 1974). (vii) Fire: The zone of bare soil at the base of the mounds can act as a fire break (Lind and Morrison, 1974). Any or all of these factors might make termitaria better sites for tree establishment and growth, and explain the presence of the thickets. There are two ways in which the woody vegetation could favour termite colonies, thus closing the positive-feedback loop, and constituting a switch: (i) Higher productivity of vegetation on the mound could be a resource of leaf or wood litter food for the termites. This explanation would not hold in communities where termites forage far from their nests out into the grassland, or where their primary food is grass and/or grass litter (Darlington, 1982). However, Darlington (1985) suggests that the mounds of Termitensavanna in the Kenya Highlands are built by Odontotermes spp., for which wood is a major diet component (Wood, 1978). (ii) Termites might be more likely to create new nests in the shade of a thicket, as Morison et al. (1948) suggested. Their evidence was weak, and the suggestion is difficult to investigate because nests are established rarely, persisting for decades or centuries (Watson, 1967; Goudie, 1988), but especially because termites tend to create new nests

308


in or near old nests, even in the absence of woody vegetation on the mound (Goudie, 1988). Although the association between mounds and woody plants is well established, and explicable, and the sharp boundaries suggest a switch, mutual relations between the vegetation and the energetics of the termite nest d o not appear to have been investigated. If a switch does operate in the way we envisage, this would benefit the termites, and could have arisen as coevolution of a mutualism. Our suggestion of a switch would fail if the woody vegetation grows on a termite mound only after the colony dies, as Lind and Morrison (1974) suggest, but Morison et af. (1948) reported that one of the thicket-topped termite mounds that they excavated had at least been recently occupied. In Australia, abandoned termite mounds persist only for 3-10 years (depending on the species of termite), but we know of no such estimates for Africa.

3. Conclusion There is a possible one-sided (type 1) switch, in which: (i) once termites form a mound, woody vegetation can invade because of higher nutrient levels (or higher temperature, or freedom from grazing, fire, etc.); and (ii) woody vegetation may favour the formation or success of termite mounds. Superficially, this would be a type 1, one-sided, switch. If, however, there were an overall limitation in food supply for the termites, or in nutrients, etc., the areas between the mounds might become impoverished, producing a type 2, reaction, switch, able to produce the mosaics seen. We must regard the existence of a termite switch as unproven.

XIII. HERBIVORE-MEDIATED SWITCHES A. Concept If a grazer avoids species X, preferentially grazing species Y, and species X is less tolerant of grazing than species Y, a positive-feedback switch is possible in which areas with species X are less grazed, therefore species X has a relative advantage in them, therefore those areas are even less grazed (Fig. 15). Grazers also have the ability, where micturition/defaecation occurs in the same patches as grazing, to create vegetation mosaics by enhancing nutrient availability. This sometimes represents a positive feedback switch

FestudAgrostis patch

I I

I I

Nardusdominated

dominated patch

I

suppressed

I Fig. 15. A herbivore switch in British upland grassland (type 2, reaction; or type 3, symmetric).


Nardus patch

2 E!

309

w

0 \o

310


because the enriched vegetation is more palatable, at least after the initial smell has disappeared.

B. Grass/Grass Boundary In the British uplands, Nardus stricta is less palatable to most stock than the other grass species it grows with. Cattle and especially sheep avoid Nardus patches almost completely in spring and summer, in favour of Agrostis spp., Festuca spp., etc. (Milton, 1953; Hunter, 1954; Rawes, 1961; Hunter, 1962; Nicholson et al., 1970; Grant et al., 1987). Even when the grasses grow intermixed, sheep avoid the Nardus (Grant et al., 1985). Nardus stricta is also slow to recover from clipping (Rawes, 1961; Atkinson, 1986), and therefore on some soils close or repeated clipping will result in a decrease in the cover of Nardus (Chadwick, 1960a; Nicholson et al., 1970). The net result is, sometimes, for grazing to increase the relative amount of Nardus in the sward because it is unpalatable (Welch and Rawes, 1964; Welch, 1986), and sometimes to decrease it because it is intolerant of defoliation (Nicholson et al., 1970; Rawes, 1981), or the two may balance (Floate et al., 1973; Rawes, 1981). Once patchiness in species composition arises, the potential exists for a switch, in which patches of Nardus are less grazed, therefore Nardus is favoured in them, and therefore they are less grazed (Fig. 15). A switch might result in a mosaic (A) situation, and mosaics have been seen in Nardus communities (Kershaw, 1957; Chadwick, 1960b), though Chadwick interpreted the Nardus patches as colonization. The switch alone would lead to small-scale mosaics, but the flocking behaviour of the sheep can enlarge the mosaic to landscape scale. There is also a difference in the soils on which the two states occur, though that difference is caused par;tly by the nature of the litter produced by the two types. Nicholson et al. (1970) almost recognized this situation as a switch under the term “pasture differentiation” which “maintains the stability of the plant community”, though they misleadingly called it cyclic succession. A similar switch may be operating to help maintain the Andropogon greenwayi mosaic in the Serengeti grasslands of East Africa (Belsky, 1986). Belsky suggests that the mosaic is primarily determined by rainfall infiltration (see above), but the Andropogon is more tolerant of the defoliation caused by antelope grazing than is the alternative-phase Chloris pycnothrix (Banyikwa, 1987). Without grazing the Andropogon disappears. Nutrient enrichment of the Andropogon patches may also be involved.


31 I

C. Grass/Woodland Boundary Browsers maintain edges where broad-leaved woody vegetation is presented at an available height, and thus prevent the woody plant community from expanding into grassland. Successional species are said to be more palatable and less chemically protected than climax woodland species (Cates and Orians, 1975), although others doubt this (Crawley, 1983). Vesey-Fitzgerald ( I 972) suggests that grazers can sharpen boundaries between Tanzanian grassland and forest. Fire follows grass cover into and through forest. Fully burnt patches then differentiate into pure grassland which is grazed, adjacent to relict forest which is not. The grazing removes so much litter from forest edges that fire is unable to repeat, or it favours creeping grass such as Pennisetum kikuyorum. Litter of the Pennisetum decomposes fast, so it does not carry fire. The species grows along forest margins, stopping fire damaging trees at the edge, and the forest thickens, with enhancement of the boundary. This scenario seems to be special to high but variable rainfall conditions in montane Africa where the initial burn is associated with exceptionally dry years after a period of undisturbed forest growth and litter accumulation. Lock (1977) gives a similar example in the Ruwenzori National Park, Uganda, in which Capparis tomentosa thickets are ringed by grassland, with an abrupt boundary. Spread of the Capparis is apparently prevented by heavy, and selective, herbivore pressure, perhaps related to the high protein and other nutrient content of the Capparis (Field, 1971). The trampling leads to a bare zone around the thicket, lowering the fire risk for the thicket.

D. Grazing and Nitrogen Cycling Trumble and Woodroffe (1954) suggested that, in arid Australian shrubland, grazing could stimulate shrub growth by increasing nitrogen input. They also suggested that the shrub species responded more to this increase in N than did associated species, which would produce a switch. There is considerable evidence for a similar switch, operated by lesser snow geese, on the salt marshes of Hudson Bay, Canada. Exclosures show that goose grazing increases shoot productivity by 7&80% (Cargill and Jefferies, 1984; Hik and Jefferies, 1990). There is evidence this is due to increased N supply: clipping without the deposition of faeces does not increase productivity, and experimental removal of naturally deposited faeces removes the increase that occurs naturally (Hik and Jefferies, 1990); N contents of Puccinellia phryganodes and Carex subspathacea are higher in grazed patches (Cargill and Jefferies, 1984); and experimental addition of goose faeces stimulates production and raises the N concentration of the herbage (Bazely and Jefferies, 1985).

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J . B . WILSON AND A . D. Q. AGNEW

There must be some removal of N from the grazed patches, but Cargill and Jefferies (1984) estimated this at less than 2.2 g m-' year-'. It is probably about balanced by greater N fixation by blue-green algae, higher in grazed areas because there is more bare ground. Bazely and Jefferies (1985) attribute the effects of grazing to faster N cycling rather than to an increased quantity of N in the system. For this to operate as a switch, the grazed areas must attract the grazers. Not only are the faster-growing plants likely to be more palatable, but the higher N content will itself attract them (Cargill and Jefferies, 1984). Grazing is certainly intense in grazed patches, geese removing 8&98% of the annual shoot production (Cargill and Jefferies, 1984). Patchiness is heightened by the behaviour of snow geese, nesting in dense colonies and feeding nearby (Cargill and Jefferies, 1984). This is not strictly a vegetation switch unless there is an effect on species composition, and experiments show Carex subspathacea, characteristic of the grazed areas, to be less abundant when grazing is allowed (Bazely and Jefferies, 1986).

E. Insects in Pine Forests In the southeastern USA, where the climax is thought to be hardwood forest, there is a pyric subclimax of pine. After storm disturbance, southern pine beetle invades the damaged pine trees, killing a patch of trees (Coulson, 1979; Schowalter, 1985). The dead wood is easily ignited by lightening fires. Fire destroys any hardwoods present, and pines re-establish.

F. Conclusion The majority of these examples are basically one-sided (type 1) switches, in which:

(i) areas with abundance of the unpalatable and grazing-intolerant species are avoided, ' (ii) reduced grazing increases the abundance of the species in those areas. At least in the Nardus case, where stock numbers are agriculturally manipulated, the tendency for stock to avoid the Nardus patches will concentrate them on the other areas, producing a reaction (type 2 ) switch, or it could be said to be a symmetric (type 3) switch, depending on the baseline. Either has the potential to create a mosaic, which is observed. The same effect could arise in natural ecosystems if animal numbers were limited by a factor other than forage supply. In the other cases, the switch seems to be a simple onesided one, and only a sharpening (B) situation occurs. (The grazing switch differs from the pest pressure mechanism of coexist-


313

ence (Connell, 1978; Fowler, 1988; Wilson, 1990) in that the coexistence is between patches, not within, and in that there is no requirement for a herbivore with frequency-dependent preferences or for multiple herbivores with different preferences.)

XIV. DISCUSSION 1. The Concept The switch concept has not been widely recognized as a general principle in plant ecology, but several ecologists have referred to aspects of the process. For example, Daubenmire (1968) said of ecotones: “While sharp differences in the physical environment may be demonstrated on either side of the ecotones, they are all secondary factors wholly attributable to community influence”. Dice (1952), an ecologist with an integrated concept of the plant community similar to Daubenmire’s, wrote: “Community boundaries are likely to be sharper where the community exerts considerable control over the habitat”. Thus, even workers strongly espousing an integrated concept of plant communities, who would expect sharp boundaries for phytosociological reasons (i.e. community assembly rules), admit that sharp boundaries are generally caused by the process we have called the switch. Gleason (1917), a worker with a concept of plant communities very different from Daubenmire’s or Dice’s, said that sometimes modification of the environment by plants caused a sharp boundary between associations where there was originally only a gradual change in the physical environment, or none.

2. Switches and Community Structure Gleason (1939) listed three possible concepts of the plant community, which we can see as combinations of deterministic vs. stochastic organization, and discrete vs. continuous variation: (i) “The association is a quasi-organism”, i.e. the community is deterministic and discrete, or “integrated”. This view is normally associated with Clements (e.g. 1905). (ii) “The association is a series of separate similar units . . . , repeated in numerous examples”, i.e. deterministic and continuous. This coincides with the views of Whittaker (Whittaker and Woodwell, 1970; Whittaker, 1975; Whittaker and Levin, 1975), in which coevolution is important, but acts to spread species out along an environmental gradient, not to aggregate them. (iii) “The vegetation-unit is a temporary and fluctuating phenomenon”, i.e. stochastic and continuous. This is Gleason’s own Individualistic theory.

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J. B. WILSON AND A. D. Q. ACNEW

I

altitude Key - - -

= =

1

=

gradient in abiotic environment gradient in the environment after biotic modification position of ecotone

Fig. 16. The gradient with a temperature switch at treeline. Below the ecotone, frosts are moderated by the tree canopy.

This leaves open the fourth possible combination, stochastic organization but with discrete boundaries. Gleason may have omitted it because it seems, at first sight, an illogical combination. Yet this combination represents the view of many plant ecologjsts that community structure is loose, combined with their observation that boundaries are sometimes sharp. If communities are not tightly structured, how can they have sharp boundaries? We suggest the answer is that the sharp boundaries arise by switches.

3. Types of Switch We have shown that four types of vegetation switch are possible. For example, fog-precipitation mediated forest (e.g. Kummerow, 1962, in Chile) is bounded by grassland that is relatively passive in its effect on water balance, so this is a one-sided switch (type l), as are hyperaccumulation of heavy-metals (e.g. Wild, 1974) and microbe-mediated allelopathy (e.g. Rice, 1971).


I

315

altitude

Fig. 17. The gradient with a fog-precipitation switch on a hillside in the montane tropics. Above the ecotone, the tall tree canopy traps fog as precipitation. Just below the ecotone, precipitation may be somewhat reduced by interception by the nearby trees. Symbols as Fig. 16.

Reaction switches (type 2) can be suggested for East African infiltrationinduced mosaics (e.g. Belsky, 1986), for salt pans (Yapp and Johns, 1917), for alpine krummholz islands (Marr, 1977), and for grazing when overall grazer numbers are externally controlled. We have found only one example that we consider a symmetric (type 3) switch-the savannah/forest boundary. If Kellman’s (1984) hypothesis is correct, the savannah provides flammable fuels, while the forest provides a fast humification environment so that fuel is removed quickly. Our only probable example of a two-factor (type 4) switch has been the same savannah/forest boundary, but with light effects considered. We cannot tell to what extent the apparent rarity of type 3 and 4 switches is due to lack of investigation, but unless switches are very common it is likely that the several switch elements required will come together but rarely.

4 . Boundaries in Space and Time The temperature switch at alpine treeline (Fig. 16) may give a simple onesided (type 1) sharpening of an environmental gradient in temperature. The fog precipitation switch can similarly sharpen a precipitation gradient (Fig.

316


I

I Q

Calluna etc. I

distance/mosaic Fig. 18. The gradient with a pH switch. At one side of the ecotone, pH is lowered by the Calluna (etc.). Symbols as Fig. 16.

17), though possible reduction in precipitation in grassland nearby would create almost a reaction (type 2) switch. We envisage the same switch could, from random colonization, produce a mosaic where the underlying physical environment shows no trend. This situation may be the norm for the pH switch with Calluna vulgaris (etc.) (Fig. 18). Alternatively, an underlying environmental gradient may establish species’ positions, but the boundary between communities be sharpened by a switch mechanism in a quite different environmental/resource factor. An example is Clarke and Hannon’s (1971) salt marsh salinity gradient (Fig. 19), where the switch to the Avicennia is mediated through the light resource. In a few cases, such as the closed-forestlsavannah boundary (Fig. 20), the sides of a boundary can be mediated by different environmental features (two-factor, type 4, switches). Often, a difference in physiognomy is seen between the two states of a switch. However, this may to some extent be an artefact, in that ecologists have sought explanations for vegetation patterns where they are most striking.


317

Arthrocnemum

distance upshore

distance upshore

Fig. 19. The gradient with a light switch on NSW (Australia) salt marshes. Light at ground level is reduced more by Avicennia tree cover than by Arthrocnemum shrubs. Symbols as Fig. 16.

Environmental/vegetational gradients may occur at various spatial scales and be of various ages. These are correlated. Old patterns are generally spatially large-scale. Thus, processes on a geological time scale generally cause landscape features, a clear example of which is the gradual leaching and impoverishment of soils following a glaciation (Walker, 1965). We suggest a soil element (NPK) switch may hasten the final impoverishment. At the smallest spatial scales, with generally young patterns, resources can be patterned by individual populations of plants or animals, such as by allelopathic dominant plants or by termites. We have described ecological outcomes in terms of the creation of spatial boundaries (situation A) or their sharpening (situation B), and also of the sharpening of time boundaries in succession, either by acceleration (C) or by delay (D). In some cases, the same alternative states may be found across either a spatial boundary, or a time boundary. Indeed, as Smith and Huston ( 1 989) suggest, spatial and temporal zonation can be seen as products of the same process. Drake (1990) and Case (1990) have produced theoretical evidence that alternative stable community states could also arise from direct interactions between species. No environmental change is involved, so the process would not be included in our definition of a switch. However, in the real world, interactions between plant species are mediated by the environment (Clements et al., 1929), so it is likely that a switch would be operating.

1

Savannah

(b)

I

- 3 j

(c) 3osedforest

I

1

Savannah

Closed forest/

Savannah distance

distance

distance

Fig. 20. The gradient with a fire/light(/nutrient) switch at the closed-rainforest/savannah boundary in Africa or Australia. Symbols as Fig. 16. (a) In the closed-forest, wet non-flammable litter rarely carries fire; in the savannah, dry flammable litter leads to frequent fire. (b) In the closed-forest, the dense canopy creates shade at ground level; in the savannah, the open canopy allows much light through. (c) In the closed-forest, nutrients accumulate; in the savannah, frequent fire may lead to some nutrient loss by volatilization and runoff.


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5 . Switches and Landscape Landscapes where large-scale spatial switches are operating are often mosaics. Either there are multiple stable conditions from one starting condition (Sutherland, 1974), or an initial environmental heterogeneity is stabilized and magnified by the plant communities occupying each state. The effect is seen as a mosaic of vegetation types, most frequently a mosaic of physiognomic types. Because a mosaic landscape is one in which diversity is perceived to be great, it is of value in recreation areas, and to conservation. Geomorphological, geological and climatically imposed mosaics can look very similar to those caused or enhanced by switches. For instance, a krummholz/alpine grassland mosaic can be caused either by an erosion pattern, by a snow cover pattern, or by fire. Any of these may have their ultimate origin in the underlying geology. Like many other features of plant ecology, human influence is a major current cause of ecotones, but the switch principle presents the ecotone as a potentially ancient feature of landscapes. It is therefore important to extend our knowledge of the processes involved, and to recognize the importance of the switch principle in mosaic initiation and maintenance.

6. Keystone Species In many cases a single species of plant may be the prime initiator of a switch mechanism, for instance Orbignya cohune (salinity switch), Calluna vulgaris (soil pH switch) or Picea engelmannii (wind switch). In these cases the plant species involved is a “keystone species” (Paine, 1969; Grabherr, 1989). In the grazing or termite-mediated switches we have discussed, the animal can be seen as a keystone species. If the concept is enlarged by adding the idea of “keystone factors” (Williams, 1980), it would include many of the switch mechanisms described here.

7. Switches vs. Succession It is not always easy from observation of vegetation to distinguish a switch from flora replacement due to some other process, e.g. facilitation succession. Conway (1949), working in the area where Heilman (1968) and Heinselman (1970) described Sphagnum as a switch species from forest to bog, suggested that succession was stepwise, a series of punctuated equilibria in ecological time, with transitions between them triggered by rainfall swings, or raising or lowering of the water table. Perhaps a closer investigation of the timing of events in facilitation successions would often show punctuated equilibria, with each equilibrium made temporarily stable by the delaying (D) outcome of a switch. Facilitation succession has traditionally been viewed as due to autogenic environmental change making conditions less suitable for the present inhabitants and more suitable for their successors. Perhaps it is the latter aspect

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that is important in most cases, and the present inhabitants decline only because of competition from their successors (Connell and Slatyer, 1977). One way or another, Connell and Slatyer’s (1977) tolerance and inhibition models follow the facilitation model in that “early occupants modify the environment so that it is unsuitable for further recruitment of these earlysuccession species”. However, in the inhibition model, recruitment of all species is .equally inhibited, late-successional species dominating only because of their longevity. The concept of a plant holding its site, presumably because competition is mainly for light and therefore cumulative (Wilson, 1988), is superficially similar to a switch, but differs in that the plant inhibits its own species equally. An indicator of the operation of a switch, rather than facilitation succession, is the presence of boundaries between vegetation types that are sharp in space or time, since switches can produce sharp boundaries, but facilitation succession cannot. We could extend the punctuated equilibrium idea to spatial arrangements. This is another way of looking at a mosaic of vegetation types. The operation of a switch in succession could lead to a temporary mosaic if succession is accelerated in some patches. Yarranton and Morrison (1974) described such a mosaic. They attributed it to facilitation succession, though this leaves open the origin for the patches. It is possible that a switch occurs at the level of bare ground vs. vegetation, but that facilitation succession occurs within vegetated patches. Cyclic succession is also a process contrasting with switches. In cyclic succession, the species/communities modify the environment to make it less suitable for themselves, the opposite of switches. Yet cyclic succession, like switches, can generate mosaics (Watt, 1947). An interesting case is the “regeneration complex” (e.g. Osvald, 1923), previously interpreted as cyclic succession, but now believed by many mire ecologists to be a switch. We might expect cyclic succession mosaics to have fuzzier boundaries between patches than switch mosaics, but neither have been quantified. The scale of switch mosaics will probably tend to coarsen through time, but it is not clear what Watt envisaged for cyclic succession mosaics. The crucial difference is that the states of a switch mosaic will be stable, those of a cyclic succession mosaic will oscillate. Westoby et al. (1989) envisaged alternative stable states, but with oscillation between them. Our concept of switches does not involve such oscillation; often patches will be stable almost indefinitely. However, the difference is one of degree. In our concept, the vegetation of a patch will be changed by drastic disturbance, depending on the magnitude of the disturbance and the degree and reversibility of environmental modification effected by the switch. A test of whether a switch is operating should be that when a switchcaused boundary or mosaic is disturbed, it should re-impose itself only very

32 I slowly, and then probably not by direct replacement of the original species. For example, if our suggested termite switch operates, and the termite mounds were destroyed, the thicket should disappear in time too. POSITIVE-FEEDBACK SWITCHES IN PLANT COMMUNITIES

8. Importance of Switches We cannot estimate how common switches are, but we have been able to find many examples, in spite of the concept often not being recognized by the original authors. It is generally accepted that plants modify their environment (e.g. Miles, 1985), and it would be strange if this were always in the direction that disfavoured their persistence. We therefore expect switches are quite widespread. If natural selection is important in structuring plant communities, one would expect that genotypes that modified their environment in their favour would be selected, and switches would therefore become common. In most of the examples given above, a link is missing in the chain of evidence, probably because the switch principle has not been recognized, and the evidence has not been sought. In fact, the evidence for switches is firmer than that for facilitation succession or for cyclic succession. Egler (1977) dramatized, with his $10000 challenge, the paucity of any evidence for facilitation succession. And although Watt (1 947) offered evidence for cyclic succession, it was circumstantial, and further investigation has shown some of Watt’s own examples to be more complex than he suggested (de Hullu and Gimingham, 1984; Marrs and Hicks, 1986; Gimingham, 1988; Svensson, 1988). In contrast, although some of our examples of switches are speculative, there is firm evidence for the elements of many, and there are cases of mosaics and sharp boundaries that are hard to explain any other way.

ACKNOWLEDGEMENTS For comments on drafts we thank A.J.M. Baker, the late J.J. Barkman, P. Bannister, K.J.M. Dickinson, A.H. Fitter, C.H. Gimingham, H. Gitay, S.A. Grant, W.McG. King, W.G. Lee, A.F. Mark, T.R. Partridge, S.H. Roxburgh, R.S. Tangney, P. Wardle and M. Westoby.

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Index Above-ground organs and oxygen Allelopathy-mediated switches, 30 1-3 deprivation, 1 18-20 Allium porrum, 22 fruits, 118 Ahus glutinosa, 1254, 128, 154 wood, I 18-20 Alocasia macrorrhiza, 2 17 Abscisic acid, 199 Alternaria, 14, 46 Acacia mearnsii, 1 19 A . tenuis, 61 Acarina, 4, 15 Altitude and positive-feedback switches, Acceleration vegetation situation, 265, 2 7 1 4 , 290-2, 314-15 269, 283, 292, 317 Amino acids, 227 Acer rubrum, 120 and oxygen deprivation, 148-50 Acetaldehyde production and oxygen Ammonium uptake, 154-5, 157 deprivation, 125, 1 4 5 4 , 147-8, 151 Amoebae, 2&1 Acid rain, 167 Andropogon Acidity A . greenwayi, 275, 310 and oxygen deprivation, 137-9, 150 A . scoparius, 304, 305 and positive-feedback switches, 278, Animals 280-3 as dispersal agents see Microbial rot Acorus calamus, 1 14, 144 and dispersal of fruits Acremonium, 8 and wetlands, 136-7, 144, 158 Acrotelm, 162, 165 see also Herbivores Actinomycetes, 126 Anthriscus sylvestris, 190, 197 Actinorhizal nitrogen fixers, 128 Antioxidants, 152 ADH see Alcohol dehydrogenase Aphelenchus avenae, 20 induction Aphids, 23 Aerenchyma distribution and function, Arctostaphylos, 52 94, 116, 120-3, 145 A . uva-ursi, 6&5, 67 Aesculus hippocastanum, 126 Arid and semi-arid areas and Agropyron, 204 positive-feedback switches, 2 8 6 7 , Agrostis, 197, 309, 310 289, 293 A . capillaris, 281 water-mediated, 27 1, 274, 275 A . magellanica, 237 Aristida oligantha, 303, 305 A . stolonfera, 204, 237 Artemisia tridentata, 287 A . vinealis, 226 Arthrocnemon, 288, 3 17 Air A . australasicum, 289 mass movement in aquatic spheres, Arthropods see Macroarthropods; 1234 Microarthropod-microbial see also Oxygen; Respiration interactions in soil Alcohol dehydrogenase activity and Ascomycetes, 7 oxygen deprivation, 112, 114, 119, Aspergillus, 6, 20, 46 1447 A . aculeatus 47 see also Ethanol A.Jlavus, 8, 10, 20 Alectoria ochroleuca, 280 A . niger, 61 Allelopathic interactions, 229 Astigmata, 15, 20

338

INDEX

ATP, 101, 126, 141-2 and growth rate variations in higher plants, 212, 2 2 3 4 A triplex A . confert$olia, 287 A . vesicaria, 282 Avena fatua 302 Avicennia, 137, 288, 3 1 6 1 7 A . nitida, 126 Azotobacter, 304 Baccharis, 53 Bacteria, 41, 304 and microarthropod-microbial interactions in soil, 5-6, 14 as food for microarthropods, 8-10 microarthropods as food for, 8 response to grazing, 10-12, 15-16, 17 in rhizosphere, 18-20, 23 Barley and oxygen deprivation, 102, 137-8, 151, 153 Basidiomycetes, 7, 9, 10, 1 I , 12 Beans, 97, 100 Beauveria bassiana, 8 Beetles, 13 Beta vulgaris, 239 Betula B. nigra, 120 B. pendula, 21 Bidens tripartita, 106 Biomass allocation, 199-200 at optimum nutrient supply, 199 plasticity in, 200 Birds, 144, 31 1 and seed dispersal, 39, 52, 60, 66 Bogs, 283. 319 ombrogenous, 278-9 , raised, 162-70 Boletus wriegatus, 130 Botrytis, 46 B. cinerea, I I , 42, 52, 61 Boundaries of switches, 267-8, 3 15-16 Bouteloua gracilis, 20 Bradysia, 7 Brassica B. nigra, 302 B. r a p , 199, 230 Bromus B. japonicus, 304 B. mollis, 146, 302

B. rigidus, 302 Bruguiera, 137 Bulbs, 20 Bulrush, 112-13, 141, 142, 144, 161 Bunch rot, 47

Cabbage, 102-3 Cadmium, 239 Calcium, 23, 154 Callitriche hamulata, 13I , 133 Callitris, 289 Calluna vulgaris, 162, 280, 28 I , 3 16, 3 I9 Caloglyphus, 15 C. micheali, 20 C . polyphyllae, 8 Capparis tomentosa, 3 1 1 Carabodes, 5 Carbohydrates and sugars in fruit, 43, 44-5, 56, 64 and growth rate variations in higher plants, 196, 224, 2 2 6 7 , 235 chemical composition, 2 0 6 7 , 210-11, 213 photosynthesis, 217-18 and oxygen deprivation, 1 0 1 4 , I 1 I , 130, 142, 144, 149, 154-5 Carbon dioxide and growth rate variations in higher plants concentration within leaf, 218-19, 22 I , 233 release, 213, 224 and oxygen deprivation, 112, 119, 125-16 and climate change, 161-2, 164, 165 consequences of, 13- I , I47 Carbon and growth rate variations in higher plants, 188, 191-2, 208-9, 21 1-13, 221-2, 227, 241 budget, 23 1-2 losses, 228-9 Carex, 202, 203, 223 C . acutiformis. C . elata, C . elongata, C . pseudocarpus and C . remota, 155 C . diandra, 221 C. gracilis, 122 C . riparia, 145 C . rostrata, 1 1 1 C . subspathacea, 31 1-12

INDEX

Cassia, 289 Casuarina, 127 catatelm, 162 Cecropia, 106 C . obtusifolia, 234 C . peltata, 21 1-12 Cellular effects of oxygen deprivation, 1414 immediate, 141-2 long-term, 1 4 2 4 Cellulose and (hemi) cellulose and growth rate variations in higher plants, 206, 207, 211, 213, 216 Celosia argentea, 100 Cereals and microarthropod-microbial interactions in soil, 23 and oxygen deprivation, 100, 101-3, 106, 112, 115-18 consequences of, 134, 139, 141-2, 146, 148, 15&1, 154-5 see also Grasses; Maize; Rice Chaetomium bostrycodes, 7 Chemicals composition and growth rate variations in higher plants, 206-14, 24 1 see also Secondary plant chemicals Chenopodium album, 304 Chickpeas and oxygen deprivation, 97, 102, 137-8, 151, 153 Chilopoda, 4 Chionochloa rigida, 273 Chloris pycnothrix, 275, 3 I0 Chlorophyll concentration and growth, 215, 217, 221 Chloroplast, partitioning of nitrogen within, 216-17 Chorisia speciosa, 100 Chromium, 285 Cicer arietinum see Chickpeas Citrus, 52 Cladina rangiferina and C . stellaris, 280 Cladosporium, 46 C . cladosporioides, 6 1 Climate change and bogs, 161-70, 279 and fruit rot, 45-6 see also Arid and semi-arid areas Closed forestjsavannah switches. 297-301, 315-16, 318

339

Cobalt, 285 Coenococcum geophilum, 23 Coleoptera, 9 Collembola and microarthropod-microbial interactions in soil, 3 4 in rhizosphere, 19-23 in saprophytic system, 6, 7-13, 15 Colletotrichum, 46 C . acutatum, 47 C . gloeosporioides, 6 1 Communities see Positive-feedback switches Competition and growth rate variations in higher plants, 2 3 5 4 plant, and oxygen deprivation, 94-5, 1 58-6 1 in saprophytic system, 6-7 see also Positive-feedback switches Conidia, 15 Conidiobolus coronatus, 8 Coniochaeta nepalica, 9 Constitutive defences of fruit, 48-9 Construction costs of plant materials, 212-14 Conyza canadensis, 304 COP (critical oxygen pressure), 1 3 4 5 Copper, 227, 2 8 4 5 Coprophilous fungi, 7, 12 Coriolus versicolor, 10, 1 1 CornusJorida, 60 Corynephorus canescens, 190, 197, 226, 232, 281 costs construction, of plant materials, 212-14 of energy-requiring processes, variations in, 224-5 Cotton, 20, 1 1 1 Crataegus crusgalli, 60 Critical oxygen pressure, I 3 4 5 Crops cotton, 20, 1 1 1 grass see Grasses and growth rate variations in higher plants, 194, 204, 205, 214 irrigation, 134, 152 susceptibility to disease, 5 5 4 vegetables and root crops, 32, 100, 102-3

340

INDEX

Cucumis sativus, 100 Cultivated plants see Crops Cyclic succession, 320 Cyperus odoratus, 106 Cytochrome oxidase, 94, 135

Defence chemical see Toxins of ripe fruit see Microbial rot delay vegetation situation, 265, 269-70, 317 biological mediation, 305 physicakhemical mediation, 290, 292, 293, 301 Denitrification, 228 Deprivation indifference, 16&1 DeschampsiaJiexuosa, 154, 198, 20 1-2, 226, 234, 281 Deserts see Arid and semi-arid areas Deterrence and fruit rot, 56-8, 6&7 interspecies variation in effectiveness, 57-8, 66-7 microbe-specific defences, 56-7, 64-5 Detoxification of harmful ions in anaerobic soils, 157-8 Digestion of microarthropods, 12-1 3, 16 Digitaria sanguinalis, 304 Diplanthera wrightii, 129 Diplopoda, 4, 9 Dispersal of fruit seeds see Microbial rot of microarthropods, 14-15, 16, 21 Display characteristics and risk of fruit rot, 47 Distribution of plants see Oxygen deprivation; Positive-feedback switches Drosophila, 41, 51, 68 Drought sensitivity, 128 see also Arid and semi-arid areas Earthworms, 23 Echinochloa, 100 Ectomycorrhizal-microarthropod interactions, 22-3 Efficiency of nitrogen use see Photosynthetic nitrogen use efficiency respiratory, variations in, 223-4

Eleocharis palustris, 133 Elymus repens, 137, 140 Empetrum nigrum, 162 Encelia farinosa, 198 Endogone, I3 1 Endophytic microbes, 53 Energy metabolism and hypoxic seed, 1 0 1 4 -requiring processes, variations in costs of, 2 2 4 5 Entomobrya purpurascens, 15 Entornopathogenic species, 8 Environment and fruit rot, 45-6 modification, see Positive-feedback switches signals of oxygen deprivation, 136-7 Epicoccum, 14 Epilobium hirsutum, 158 Eremophila, 290 Ericaceous species Erica cinerea, 28 1 see also Microbial rot and dispersal of fruits Erigeron strigosus, 304 Eriophorum vaginatum, 292 Erythrina caflra. 100 Espeletia, 198 Ethanol production, 42 and oxygen deprivation, 97, 1 12, 11416, 118-20, 138, 145-9, 151 Ethylene (hormone), 40,42, 151 Eucalyptus, 194, 21 1, 274, 289, 297, 299 E. populnea, 300 E. tetrodonta, 300 Eupatorium odoratum, 13I Evolution patterns and microbial rot and dispersal of fruits, 38, 68 see also Natural selection Excreta of microarthropods, 3, 11, 13-14, 16, 18 of rabbits, 6, 12 “Extensin”, 21 6 Exudation and volatile losses, 227-9, 238 rate (EXU and VOL), 192, 194

Facilitation succession, 265-6, 319-21 Fagopyrum esculentum, 97

INDEX

Fagus crenata, 290 Fast-growing and slow-growing species compared see Growth rate variations Feces see Excreta Feedback inhibition of photosynthesis, 218-19 see also Positive-feedback switches Fertility of soil and growth see Growth rate variations in higher plants Festuca, 200, 309, 3 10 F. ovina, 190, 197, 281 Filipendula ulmaria, 145 Fire-mediated switches, 293, 296301, 307, 315-16, 318 Flavonoids, 228 Flax, 102, 103 Flies fruit, 41, 51, 68 larvae, 7 sciarid, 12 Fog precipitation and switches, 271-5, 314, 315 Folsomia F. candida, 10, 1 1 , 12, 13, 21-2 F. jimetaria and F. regularis, 1 1 Foraging, see Herbivores Foreign species, introduction of, 137 Forests see Trees Frankia, 128 Frost, 291 Fruit and oxygen deprivation, 137, 152 Fruit rot defences interspecific variations in effectiveness, 57-8 microbe-specific, 5&7 natural selection for, 48-56 defined, 41 effects on dispersal, 3 9 4 3 factors affecting risk of see Risk of fruit rot general deterrent nature of, 56 see also Microbial rot and dispersal of fruits Fungi and fruit rot see Microbial rot and dispersal of fruits and growth rate variations in higher plants, 205, 228 and microarthropod-microbial

341

interactions in soil, 3, 5 as food for microarthropods, 8-10 microarthropods as food for, 8 response to grazing, 10-12, 15-16, 17 in rhizosphere, 17-24 in saprophytic system, 6 9 , 12, 14-17 and oxygen deprivation, 129-33 Fungivores see Microbial rot Fusarium, 8, 20, 46, 52 F. sporotrichioides, 6 1 Galinsoga parviyora, 190, 197, 232 Gases see Carbon dioxide; Oxygen Gaultheria procumbens, 60, 65 Gaylussacia, 47, 60 G ..frondosa, 6G5, 67 Genetics horizontal gene flow, 53 see also Natural selection Geotrichum, 46 G. candidum, 61 Geranium robertianum, 22 Germination and oxygen deprivation, 100-1 and energy metabolism, 10 1 4 Gibberellins and growth rate variations in higher plants, 199, 229-30, 240, 24 1 Gigaspora G . fasciculatum and G . margarita, 2 1 G . rosea, 22 Gloeosporium, 46 GIomus G . ,fasciculatus, 122 G . macrocarpus, 131 G . mosseae, 2 I , 22 G. occultus, 22 Glucose and toxin production, 21 1-13 Glyceria maxima, 1 1 I , 1 14, 144, 149, 154, 157, 159-60 Glycine max, 2 I Glycolysis, 137-9 end-products of, 147-8 rate and A D H induction, 144-7 see also Carbon dioxide and oxygen deprivation; Ethanol production Glycosides, 2 1 1 Gnat larvae, fungus, 7 Gnornonia leptostyla, 9

342

INDEX

Graminoid tussocks, 292 Grapes and fruit rot, 42, 52 Grasses and pasture plants and growth rate variations in higher plants, 201, 204, 237 and oxygen deprivation, 104, 129, 149, 155, 157, 159 and pasture plants and microarthropod-microbial interactions in soil, 19-20, 22 and positive-feedback switches allelopathy-mediated, 302-3 fire-mediated, 297-301 herbivore-mediated, 308-1 2 light-mediated, 289 microbe-mediated, 303-5 soil-element-mediated, 28 1-2, 287 termite-mediated, 3 0 6 7 water-mediated, 271-3, 315 wind-mediated, 293 see also Cereals Gratiola viscidula, 106 Grazing and microarthropod-microbial interactions in soil, 2, 3, 21-2 in microarthropod-microbial interactions in soilbacterial and fungal response to l(r12, 15-16, 17 see also Grasses; Herbivores Greenhouse gases and climate change, 164, 165 Grenzhorizont, 162 Growth rate variations in higher plants, 187-242 biomass allocation, 199-200 chemical composition, 206-14, 241 ecological consequences of ,variations, 235-9 exudation and volatile losses, 227-9 growth analysis, 1 9 1 4 hormonal differences, 229-30 integration of various aspects, 23 I 4 net assimilation rate and leaf area ratio, 1 9 4 6 roots, growth, morphology and nutrient acquisition, 2OCL6, 241 species-specific performance under sub-optimal conditions, 234 specific leaf area, 196-9 see also under Photosynthesis; Respiration

Growth respiration, 222, 224 Haemoglobin and oxygen deprivation, 127, 136 Halogeton glomeratus, 2 8 6 8 HaloxyIon H. aphyllum and H. persicum, 286 H. salicornicum, 293 Heavy metals and growth rate variations in higher plants, 190, 216, 228, 239 Hebeloma crustuliniforme and H. mesophaeum, 131 Herbaceous plants see in particular Growth rate variations Herbivores, 7 and growth rate variations in higher plants, 210, 217, 229, 233, 236, 238 herbivore-mediated switches, 276, 289, 300, 303, 307, 308-13 protection against see Toxins see also Defence; Grazing Holcus lunatus, 22, 198, 226, 234 Hordeum vulgare, 225, 228 Hormones and growth rate variations in higher plants, 229-30 see also Ethylene; Gibberellins Hydrocharis, 1 10 Hyperaccumulators, 2 8 3 4 Hyphomycetes, 7, 1 I Hypoestes fastigiatu, 300 Hypogastrura tullbergi, 1 I , 13 H ypoxia hypoxic seed and oxygen deprivation, 9 5 9 7 , 100-10 aquatic seed, 104-10 energy metabolism and oxygen availability for germination, 1014 germination, 100-1 root apex, 114-18 see also Oxygen deprivation Hysterangium setchellii, 23 Igapo forests, 106, 107 IIex opaca, 60, 210 Induced defences of fruit, 49-51 Infiltration switches, 275-6, 315 Inhibition model of succession, 3 19-20 Insects and dispersal of yeasts, 41

INDEX

and growth rate variations in higher plants, 210 herbivorous, 52 in pine forests, 3 12 Interspecies variation in effectiveness of fruit defences, 57-8, 66-7 Introduction of foreign species, 137 Ions in anaerobic soils, detoxification of 157-8 uptake see Nutrients Iris I . germanica, 147, 15&1 I . pseudacorus, 137, 143, 147, 151, 154, 156 Iron and growth rate variations, 227 and oxygen deprivation, 157-8 Irrigation, 134, 152 Isoetes lacustris, 133 Isopoda, 3, 4, 8, 11 Isoprene, 229 Juglans nigra, 9 Juncus conglomeratus and J. effusus, 111 Juniperus communis, 282 Kampfzonen, 161 Keystone species and switches, 319 Knudsen diffusion, 124 Kochia americana, 287 Krummholz, 2 9 4 5 , 3 15 Laccaria laccata and L . proxima, 130 Lactate dehydrogenase activity (LDH), 145 Lactuca saliva, 207 Landolphia, 300 LAR see under Leaves Lead, 285 Leaves and growth rate variations in higher plants, 230-1 area ratio (LAR), 191-6, 200, 230, 234, 238, 240, 241 and net assimilation rate, 1 9 4 6 see also Specific leaf area respiration rate (LR), 191, 192, 194, 223, 226 toxins, 21 1-12

343

weight ratio (LWR), 191-7, 199-200, 226, 232-3, 241 Ledum groenlandicum, 229 Leeks, 22 Leghaemoglobin, 127 Legumes, 106, 126-7, 228 see also Beans; Peas; Nitrogen fixing Lenticels, 1 19-20, 128 Lettuce, 100, 102, 103 Light-mediated switches, 288-90, 3 15, 318 Lignin and growth rate variations in higher plants, 196, 206, 207, 210, 213, 216 Limnocharis, 1 10 Lindera benzoin, 60 Lipids and fruit rot, 59, 64 and growth rate variations in higher plants, 206, 212, 213 and oxygen deprivation, 1 0 2 4 Litorella unijlora, 131 Lobelia dortmanna, 131 Lonicera, 283 LR see under Leaves “Luxury consumption”, 207 LWR see under Leaves Lycopala epidendrum, 5 Lycopersicon esculentum, 52, 199, 230 Lycopus europaeus, 106 Lycoriella mali, 7 Lythrum salicaria, 106

Macroarthropods, 3, 4, 8, 11 Macrotermes, 306 Maintenance respiration, 222, 224 Maize and oxygen deprivation, 100, 102-3, 115-18 consequences of, 139, 141-2, 146 Manganese, 227, 281, 285 manganous ions and oxygen deprivation, 157-8 Mangroves, 126, 137, 288, 31617 Marasmius androsaceus, 10 Mass movement of air in aquatic spheres, 123-6 Mauritia jlexuosa, 98 Melanerpes formicivorous, 52 Mentha spicata, 2 I 1 Mesembryanthemum crystallinum, 287-8

344

INDEX

Metabolism/metabolic adaptation to oxygen deprivation, 144-50 effects of root anoxia on whole plant physiology, 148-50 end-products of glycolysis, 147-8 glycolytic rate and A D H induction, 144-7 consequences of oxygen deprivation see under Oxygen deprivation energy, and germination, 1 0 1 4 oxygen sensing, 135-6 Metarrhizium anisopliae 8 Microarthropod-microbial interactions in soil, 1-25 historical and biological reasons for, 3-6 in rhizosphere, 2, 17-24 in saprophytic system, 6-1 7 see also in particular Collembola; Mites Microbe-mediated switches, 303-6, 3 14 Microbe-specific defences of fruit, 5 6 7 , 646 Microbial rot and dispersal of fruits: selection for secondary defence, 35-68 fruit rot and effects on dispersal, 39-56 hypotheses and predictions, 5&8 predictions for temperate seed dispersal, 58-67 variations in characteristics of fruits, 37-8 variations in secondary defence chemistry, 38-9 Microsclerotia, I5 Millipedes, 3, 1 1 Mineralization of soil, 17, 20, 2 I see also Nutrients Mites and microarthropod-microbial interactions in soil, 3 in rhizosphere, 20, 23 in saprophytic system, 6, 8-9, 12-13, 15 Molybdenum, 285 Monilinia, 47, 5 I , 67 Monocots as dominant species in wetlands, 96 see also Oxygen deprivation Mortierella isabellina, 7, 1 1

Mosaic vegetation situation, stable, 265. 269, 3 17-20 biological mediation, 307 physicakhemical mediation fire, 301 soil-element, 283, 287, 288 water, 275-6, 278 wind, 293, 296 Mosses, 162, 278-280, 282-3, 319 Mummy-berry disease, 47, 67 Mycelia sterilia, 46 Mycena galopus, 10 Mycorrhizal fungi, 17, 21-2 and growth rate variations in higher plants, 205, 228 and oxygen deprivation, 129-33 Myrosphaerella juglandis, 9 Mycotoxin-producing fungi, 53 Myrica, 127 M . gale, 128 Myriophyllum, 1 I0 M . alterniforum, 133 Myrothecium, 53 myxomycete, 5 Nujas marina, 109 NAR see Net assimilation rate Nardus stricta, 1 54, 309- 10, 3 1 2 Natural selection for defences against fruit rot, 48-56 antimicrobial, 54 biotic, 5 3 4 secondary chemicals as agents, 48-53 structural and chemical defences retained, 55-6 and growth rate variations in higher plants, 2 3 6 8 Nelumbo nucrfera, 100 Nematoda in soil, 3, 4, 19, 20-1, 23 Net assimilation rate, 191-5, 200, 234 and leaf area ratio, 1 9 4 6 Net nitrogen uptake rate, 192, 194, 20&1, 223, 226 Nickel, 284-5 NIR see Net nitrogen uptake rate Nitrates, 154 and growth rate variations in higher plants, 201-3, 206-7, 213, 222, 225 Nitrobacter, 305

INDEX

Nitrogen in anaerobic environments, 152-7 fixation, 228 in oldfields, 303-5 and oxygen deprivation, 126-8, 129 and growth rate variations in higher plants, 189-90, 194, 201-2, 206, 208-9, 21 I , 238, 241 and biomass allocation, 199-200 and respiration, 224-6 see also Photosynthetic nitrogen use efficiency and microarthropod-microbial interactions in soil, 17, 20 and positive-feedback switches, 281-3, 303-5, 11-12 Nitrosomonas, 305 “Noble” rot, 42 Nodulation see Nitrogen fixation Nothofagus solandri, 29 1 Nuphar lutea, 123, 124-5 Nutrients and flooding tolerance and oxygen deprivation, 152-8 detoxification of harmful ions in anaerobic soils, 157-8 nitrogen nutrition in anaerobic environments, 152-7 and growth rate variations in higher plants, 188-90, 194, 207-9, 21 1-14, 233, 238, 240-1 biomass allocation, 199-200 exudation, 227-9 and photosynthesis, 214-15, 2 19-22 and respiration, 222-6 and roots, 200-6 and positive-feedback switches, 274, 276, 281-8, 307 see also in particular Nitrogen Nvmphoides, 1 10 Nyssa sylvatica, 60, 104, 149 Oceanic climate, changes in, 161-70 Odontotermes, 307 Oil glands in plants, 21 1 Oldfield succession and nitrogen-fixing microbes, 303-5 Ombrogenous bog switches, 278-9

345

One-sided switch, 257, 264, 314 biological, 303-1 3 physicakhemical, 271-5, 280-8, 290-3, 301-3 Oniscus asellus, 8 Ony ch iurus 0. ambulans, 21 0. armatus, 9, 1 I , 22 0. encarpatus, 20, 22 0.jirmatus, 20 0.folsomi, 22 0. latus, 10 0. quadrocellatus, 1 I , 15 0. subtenuis, 9, 12, 15 Orbignya cohune, 286, 288, 319 Organic acids as fruit defence, 42, 51-2 and growth rate variations in higher plants, 206, 207, 213, 227-8 and oxygen deprivation, 146, 148 Oribatids see Mites Osmosis, thermal, 124-5 Over-grazing, 167 Oxygen content of atmosphere, fluctuation in, 95-6 deprivation as ecological limit to plant distribution, 93-171 and climate change, 161-70 consequences for survival and metabolism, 133-58 cellular effects, 1 4 1 4 metabolic adaptation to, 144-50 mineral nutrition and flooding tolerance, 152-8 post-anoxic injury, 15&2 sensing oxygen deficiency, 134-41 and plant competition, 94-5, 15841 plant organs liable to, 97-120 see also Above-ground organs; Hypoxia; Underground organs and plant structure, 120-6 and symbiosis, 1 2 6 3 3 see also Respiration Panicum P . laxum, 104 P . virgatum, 305 Parkia auriculata, 106

346

INDEX

Pastinaca sativa, 52 Pasture plants see Grasses Pathogens: saprophyte-pathogenmicroarthropod interactions, 17-21 Pauropods, 3, 4 Paxillus involutus, 130-1 Peanuts, 20 Peas and oxygen deprivation, 97, 100, 102, 103, 114 consequences of, 127, 137-8, 149, 151, 153 see also Chickpeas Peat, 162-70, 280, 282 Pelopoidea, 23 Penicillium, 1 4 1 5 , 46, 61 P. citrinum, 14 P . rubrum, 61 P. spinulosum, 7, 1 1 Pennisetum kikuyorum, 3 1 1 Penthorum sedoides, 106 Perennating organs, anoxia-tolerance variation in, 1 10-1 1 Persistence of fruit, variation in, 39-40 Pestalotiopsis maculans, 61 pH-mediated switches, 280-1, 316 see also Acids; Salts Phaseolus, I27 P . lunatus, 21 1 P . vulgaris, 97 Phasic theory of bog growth, 164 Phenols and fruit rot, 48-9, 51-2 and growth rate variations in higher plants, 196, 21 I , 228 Philoscia muscorum, 1 1 Phleum pratense, 190, 197 Phoma, 46 P. vaccinii, 61 Phomopsis, 46, 61 Phosphates and growth rate variations in higher plants, 201-2, 204, 207, 227 Phosphorus, 199, 206, 281-3, 317 Photosynthesis and growth rate variations in higher plants, 191-2, 21 I , 232-3, 238, 241 described, 214-22 species-specific variation in rate of, 214-15 under suboptimal conditions, 221-2 see also Photosynthetic nitrogen

Photosynthetic nitrogen use efficiency, 192, 215-22, 233, 240 carbon dioxide concentration within leaf, 218-19 feedback inhibition of, 218-19 partitioning of nitrogen within chloroplast, 21 6 1 7 Rubisco activation and variations, 217-18 and water use efficiency, 219-21 Phragmites australis, 106, 1 1 I , 1 12, 1 14, 125, 133, 159-60 Phthiracarus, 12 Phylloplane microbes, 53 Phytosiderophores, 227 Picea, 295 P . abies, 19, 119 P. engelmannii, 294, 3 19 P . marina, 280 P . sitchensis, 9, 130, 132 Pimpinella saxifraga, 190, 1': Pinus P. contorta, 17, 120, 121 P . nigra, 17 P. ponderosa, 207 P. sylvestris, 119 Pisum sativum, 97, 127 Plant nitrogen concentration, 192, 194, 200 Plantago major, 204, 206, 21 5 Plants communities see Positive-feedback switches distribution see Oxygen deprivation fruit see Fruit rot growth see Growth rate variations Plasticity and growth rate variations in higher plants biomass allocation, 22 root growth and nutrient acquisition, 202-5, 241 specific leaf area, 198-9 P N C see Plant nitrogen concentration Poa P . annua, 190, 197, 231 P. colensoi, 273, 293 Podophyllurn peltatum, 198 Polyamines, 150-1, 216 Populus P . deltoides, 119, 231 P. trernuloides, 229 P. trichocarpa, 231

INDEX

Positive-feedback switches in plant communities, 263-321 agencies listed, 271 allelopathy-mediated, 301-3 boundaries, 267-8, 3 15-1 6 community structure, 31 3-14 defined, 265-6 fire-mediated, 293, 296301, 307, 315-16, 318 herbivore-mediated, 276, 289, 300, 303, 307, 308-13 importance of, 321 keystone species, 3 19 and landscape, 317 light-mediated, 288-90, 3 15, 318 microbe-mediated, 303-6, 3 14 pH-mediated, 280-1, 3 I6 and soil see Soils, soil-element-mediated temperature-mediated, 290-2, 307 termite-mediated, 276, 300, 3 0 6 8 types of, 267, 3 1 4 1 5 vegetation situations produced by, 268-70 see also Acceleration; Delay; Mosaic; Sharpening versus succession, 3 19-20 and water see Water, water-mediated wind-mediated, 276, 292-6 Post-anoxic injury, 15&2 Potamogetonjliformis, 1 10, 129 Potassium, 28 1-3, 3 17 Potential growth, 238-9 Potentilla pafustris, 122 Precipitation, 166, 167 change see Climate change rainfall and positive-feedback switches, 271, 2 7 4 5 , 278 snow accumulation, 280 see also Fog Predictions of temperate seed dispersal systems, 5 6 8 , 6&7 Primary chemical compounds and growth rate variations in higher plants, 20&7 Proisotoma minuta, 13, 20, 22 Prosopis velutina, 289-90 Prostigmatids, see Mites Proteaceae, 205 Protein and growth rate variations in higher plants, 206, 212-13, 21617, 221-2, 224, 233

341

Protozoa, 19 Protura, 3, 4, 6 Prunus, 60 PS see Photosynthesis Pseudoscorpionidae, 4 Pseudosinella alba, 15 Psychotria dourarrei, 284 Puccinellia phryganodes, 3 1 1 pulp nutrient chemistry, 43-5 putrescine, 150-1 Pythium P. myriotylum, 15, 20 P. ultimum. 20 Qualitative defence compounds, 207, 209- 10, 24 1 Quality of fruit, variation in, 39-40 Quantitative defence compounds, 207, 24 1 Quantum flux density and growth rate variations in higher plants high, 214, 226 low, 198-200, 2 0 6 7 , 211, 215, 222, 225-6, 234 Quercus, 288-9 Rabbits, excreta of, 6, 12 Rainfall see Precipitation Raised peat bogs, 162-70 Ranunculus sceleratus, 148 Reaction switch, 264, 267, 315 biological, 3068, 3 I2 physicakhemical, 275-8, 293 Recurrence surfaces, 162 Reeds and oxygen deprivation, 106, 111, 112, 114, 125, 133, 159-60 Relative growth rate see Growth rate variations Relative-risk model of interspecific variation in defence effectiveness, 57-8, 66 Removal-rate model of interspecific variation in defence effectiveness, 58, 6 6 7 Resource denial, 160-1 Respiration and growth rate variations in higher plants, 188, 213 at suboptimal nitrogen supply or quantum flux density, 2 2 5 6 and growth of plants, 2 2 2 4

348

INDEX

Respiration and growth rate (cont.) root, 192, 232 see also under Species-specific RGR (relative growth rate) see Growth rate variations Rhagoletis, 5 1 Rhizobium, 128, 228, 304, 305 Rhizoctonia solani, 20 Rhizoglyphus echinopus, 15, 20 Rhizophora, 137 Rhizopus, 46 R. stolonifer, 61 Rhizosphere microarthropod-microbial interactions in, 2, 17-24 and oxygen deprivation, 128-9 consequences of, 140, 1 4 2 4 , 147, 150-1, 157 see also Underground organs Rhus typhina, 60 Rhynia, 3 Rhvtisma acerinum, 8 Ribes montigeum, 294 Rice and oxygen deprivation, 100, 101-3, 112, 116 consequences of, 134, 139, 148, 150-1, 1 5 4 5 Ripening, fruit, 40 Risk of fruit rot, factors affecting, 43-8 ambient environmental conditions, 45-6 pulp nutrient chemistry, 43-5 removal rate of time of exposure, 48 spore inoculum, identity and quantity of. 46-7 synchrony and display characteristics, 47 Roots crops, 102-3 and growth rate variations in higher plants, 200-6, 240-1 exudation, 227-8 nutrient acquisition, 200-5 respiration, 2 2 2 4 , 226 respiration rate (RR), 191, 192, 232 root weight ratio (RWR), 1 9 2 4 , 199, 200, 202, 205, 230, 232, 237, 24 1 specific root length (SRL), 192, 201,202

nodules and symbiosis and oxygen supply, 126-8 root apex hypoxia, 114-18 Rot see Fruit rot Rubisco activation and variations in higher plants, 217-18, 222, 233 Rubus, 60, 283 Ruderals, 223 Rumex, 120 R. acetosa, 154 R. crispus, 190, 197 RWR see under Roots and growth rate

Saccharomyces, 4 I , 46 S. cerevisiae, 6 1 Sagittaria, 110 Salicornia australis, 289 Salt and growth rate variations in higher plants, 190, 239 and switches, 286-8 salt marsh pans, 2768, 289, 315, 316 Saponins, 52, 210 Saprophytic system, 41 microarthropod-microbial interactions in, 617 saprophyte-pathogenmicroarthropod interactions, 17-21 Sasa, 290 Sassafras albidum, 60 Scheuchzeria palustris, 162 Schoenoplectus lacustris, 112-13, 141, 142, 144, 161 Sciarid fly, 12 Scirpus S. americanus, 112, 137, 144 S. lineatus, 106 S . maritimus, 1 12, 1 15 S. sylvaticus, 204 Sclerotinia sclerotiorum, 10 Scrophularia nodosa, 190, 197 Secondary plant chemicals and fruit rot, 35-6, 37-9, 56-7, 59 and dispersal, 42, 43-5, 48-53 pulp nutrient chemistry, 43-5 and growth rate variations in higher plants, 207-10, 21 1-12, 241

INDEX

Sediment entrapment and switches, 2 7 6 8 , 289, 3 15, 3 16 Seeds dispersal see Microbial rot and dispersal of fruits see also under Hypoxia Selection see Natural selection Selenium, 285 Senecio aquaticus, 148 Sensing oxygen deficiency in plant tissues, 1 3 4 4 1 environmental signals, 136-7 metabolic, 135-6 signal molecules, 136 Shade and sun species compared set> Growth rate variations Sharpening vegetation situation, 265. 269. 317 biological mediation, 3 12 physicakhemical mediation, 290, 291, 293, 301, 303 soil-element, 286, 288 water, 271-6 Signal molecules for oxygen deprivation, 136 Silene vulgarisicucubalus, 239 Sinella, 23 Skins of fruit, 50-1, 52 SLA see Specific leaf area Slow-growing and fast-growing species compared see Growth rate variations Smilax rotundijolia, 60 Snow accumulation, 280 SOD (superoxide dismutase), 151, I58 Sodium, 2 8 6 7 Soils, 307 anaerobic, detoxification of harmful ions in, 157-8 erosion and trapping, 292-3 fertility and growth see Growth rate variations soil-element-mediated switches, 276, 281-8, 307 heavy metals, 283-6, 3 14 NPK decrease, 282-3 NPK increase, 281-2, 317 salt, 2 8 6 8 see also Microarthropod-microbial interactions in soil Sordaria jimicola, 9

349

Sorghum bicolor, 21 Soybeans, 21 and oxygen deprivation, 103, 1 1I , 127-8 Sparganium, 1 10 Spartina alterniflora, 129, 142 Species-specific variations in growth rate of photosynthesis, 21415 respiration rate, 222-5 costs of energy-requiring processes, 224-5 efficiency, 2 2 3 4 under sub-optimal conditions, 234 Specific leaf area and growth rate variations in higher plants, 189, 199, 230, 2 3 2 4 components of, 196-8 high, 238, 240-1 low, 236-7 plasticity, 198-9 Specific root length, 192, 201, 202 Sphagnum, 162, 278-9 282-3, 319 S. jiuscum, 280 Spirillum lipoferum, 129 SRL see Specific root length Stable vegetation see Mosaic vegetation Staphylinidae, 9 Starch see Carbohydrates Steccherinum jimbriatum, 7 Stems and growth rate variations in higher plants respiration rate (SR), 191, 192, 232 weight ratio (SWR), 1 9 2 4 , 199 Stephanomeria malheurensis and S. exigua, 237 Stratiotes, 110 Structure of plants and oxygen deprivation, 120-6 aerenchyma distribution and function, 94, 116, 120-3, 145 mass movement of air in aquatic spheres, 123-6 Suboptimal conditions and plant growth, 210-1 I , 221-2, 2 2 5 4 Succession versus positive-feedbak switches, 3 19-20 Sucroseisugars see Carbohydrates Sun species see Shade and sun Sunflower, 103, 146 Superoxide dismutase, 15 I , 158

350

INDEX

Survival consequences of oxygen deprivation see under Oxygen deprivation Switches see Positive-feedback switches SWR see under Stems and growth rate Symbiosis and oxygen supply, 1 2 6 3 3 and mycorrhizas, 129-33 nitrogen fixation in rhizosphere of aquatic plants, 129 root nodules, 1 2 6 8 Symmetric switch, 264, 267, 315 biological, 312 physical-chemical, 283, 294-6 Synchrony and risk of fruit rot, 47 Syringodium ,filijorme, 1 29 Tannins and fruit rot, 49, 52 and growth rate variations in higher plants, 196, 21&-12 Taxodium distichum, 104-5 Temperate seed dispersal systems, 58-67 fruiting classes, 58-60 predictions, 6&7 Temperate vertebrate-dispersed species see Microbial rot and dispersal of fruits Temperature change see Climate change -mediated switches, 29&2, 307 Termite-mediated switches, 276, 300, 3068 Terpenoids, volatile, 2 10, 2 13 Tetrahymena pyrijormis, 135 Thalassia testudinium, 129 Thelophora terrestris, 132 Thermal transpiration (-osmosis), 124-5 Thlaspi arvense, 230 Thorns, 236 Tomocerus T. longicornis, 12 T . minor, 1 I , 13, 17 Toxins in anaerbic soil, 157-8 and fruit rot, 45, 48, 5 I , 55, 5 6 7 and growth rate variations in higher plants, 196, 2 0 S I 3, 21 7, 228 and positive-feedback switches, 283-6, 302-5, 314 I

Trampling, 236 Transpiration, thermal, 124-5 Trapa, 110 Trees and growth rate variations in higher plants, 193, 194, 196, 210, 214, 216, 219, 230-1 and microarthropod-microbial interactions in soil, 6, 8-10, 14-15, 17, 19, 21 and oxygen deprivation, 100, 104-8, I 18-20 and climate change, 162, 1 6 6 9 consequences of, 121, 125-6, 129-30, 134, 149, 154-5 removed before peat formation, 163, 1 6 6 9 tree mycorrhizas, 129-30 and positive-feedback switches fire-mediated, 297-301, 318 herbivore-mediated, 31 2 light-mediated, 288-9, 318 microbe-mediated, 305-6 soil-element-mediated, 282-3, 286 temperature-mediated, 29&2 termite-mediated, 307-31 I tree-line, 29&1, 294, 314, 315 water-mediated, 2 7 1 4 , 3 14, 3 15 wind-mediated, 294-6 Trichoderma, 6, 53 T . harzianum, 20 Trifolium, 127 T . pratense, 22, 146 Triticum aestivum, 142, I98 Tubers see Underground organs Tundra, 280, 292, 294-6 Tussilagofarfara, 137, 139 Two-factor switch, 264, 267, 315 physicakhemical, 281, 283, 288-90, 29630 I Typha, 110 T. angustijolia, 112, 142 T . latifolia, 106, 112, 114, 142, 16&1

Ulex europaeus, 280, 28 1 Underground organs and oxygen deprivation, 95, 11&18 anoxia-tolerance variation in perennating organs, 1 1 0 - 1 1

INDEX

re-emergence fom anaerobic habitats, 112-14 root apex hypoxia, 114-18 Uranium, 285 Urtica dioica, 201-2 Utricularia, 110

Vaccinium, 47, 51, 52, 60 V. corymbosum, 60-5, 67 V . macrocarpon, 42, 60-5, 67 V. vacillans, 60, 65 Vallisneria, 1I0 VAM see Vesicular-arbuscular m ycorrhiza Vapour-pressure deficit, 2 19 Variations in growth, see Growth rate variations Varzea forests, 106, 109 Vegetables, 32, 100, 102-3 see also Beans; Peas Veronica montana and V. persica, 198 Vertebrates and seed dispersal see Microbial rot and dispersal of fruits Vert icillium, 20 V. albo-atrum, 15, 20 V. bulbillosum, 1 1 V . lecanii, 8 Vesicular-arbuscular mycorrhizas, 130-3 microarthropod interactions, 17, 21-2, 25 Viburnum lentago, 289-90

35 1

Victoria amazonica, 109 Vigna unguiculata, 127, 128 Vitis vinifera, 52 VOL see under Exudation Volatile losses, see Exudation

Water and growth rate variations in higher plants, 199, 218-21, 241 water use efficiency (WUE), 219-21 water-mediated switches, 271-80 fog precipitation, 271-5, 314, 315 infiltration, 2754, 3 15 ombrogenous bogs, 278-9 salt marsh, 276-8, 289, 315, 316 snow accumulation, 280 Weight of roots see under Roots and growth rate variations Whet and oxygen deprivation 102-3, 116, 118, 142 Wild rice, 100, 106 Wind and growth rate variations in higher plants, 236, 237 -mediated switches, 276, 292-6 Wood and woodland, see Trees WUE see under Water and growth rate Yeasts and fruit rot, 41, 42, 68 Zea mays, 141, 199, 230 Zinc, 227, 285 Zizania aquatica, 100, 106 Zostera marina, 129, 149, 155, 157


Advances in Ecological Research Volumes 1-23 Cumulative List of Titles Aerial heavy metal pollution and terrestrial ecosystems, 11, 218 Analysis of processes involved in the natural control of insects, 2, 1 Ant-plant-homopteran interactions, 16, 53 Biological strategies of nutrient cycling in soil systems, 13, 1 Bray-Curtis ordination: an effective strategy for analysis of multivariate ecological data, 14, 1 Can a general hypothesis explain population cycles of forest lepidoptera? 18, 179 A century of evolution in Sparrina anglica, 21, 1 The climatic response to greenhouse gases, 22, 1 Communities of parasitoids associated with leafhoppers and planthoppers in Europe, 17, 282 Community structure and interaction webs in shallow marine hard-bottom communities: Tests of an environmental stress model, 19, 189 The decomposition of emergent macrophytes in fresh water, 14, 115 Dendroecology: A tool for evaluating variations in past and present forest environments, 19, 1 1 1 The development of regional climate scenarios and the ecological impact of greenhouse gas warming, 22, 33 Developments in ecophysiological research on soil invertebrates, 16, 175 The direct effects of increase in the global atmospheric CO, concentration on natural and commercial temperate trees and forests, 19, 2 The distribution and abundance of lake-dwelling Triclads - towards a hypothesis, 3, 1 The dynamics of aquatic ecosystems, 6, 1 The dynamics of field population of the pine looper, Bupalus piniarius L. (Lep., Geom.), 3, 207 Earthworm biotechnology, and global biogeochemistry, 15, 379 Ecological aspects of fishery research, 7, 114 Ecological conditions affecting the production of wild herbivorous mammals on grasslands, 6, 137 Ecological implications of dividing plants into groups with distinct photosynthetic production capabilities, 7, 87 Ecological implications of specificity between plants and rhizosphere micro-organisms, 21, 122 Ecological studies at Lough h e , 4, 198 Ecological studies at Lough Hyne, 17, 11 5 The ecology of the Cinnabar moth, 12, 1 Ecology of the coarse woody debris in temperate ecosystems, 15, 133 Ecology, evolution and energetics: a study in metabolic adaptation, 10, 1 Ecology of fire in grasslands, 5 , 209 Ecology of mushroom-feeding Drosophilidae, 20, 225 The ecology of pierid butterflies: dynamics and interactions, 15, 51

354

CUMULATIVE LIST OF TITLES

The ecology of serpentine soils, 9, 255 Ecology, systematics and evolution of Australian frogs, 5, 37 Effects of climatic change on the population dynamics of crop pests, 22, I 17 The effects of modern agriculture, nest predation and game management on the population ecology of partridges (Perdix perdix and Alectoris rufa), 11, 2 El Nifio effects on Southern California kelp forest communities, 17, 243 Energetics, terestrial field studies and animal productivity, 3, 73 Energy in animal ecology, 1, 69 Estimating forest growth and efficiency in relation to canopy leaf area, 13, 327 Evolutionary and ecophysiological responses of mountain plants to the growing season environment, 20, 60 The evolutionary consequences of interspecific competition, 12, 127 Forty years of genecology, 2, 159 The general biology and thermal balance of penguins, 4, 131 General ecological principles which are illustrated by population studies of Uropod mites, 19, 304 Genetic and phenotypic aspects of life-history evolution in animals, 21, 63 Geochemical monitoring of atmospheric heavy metal pollution: theory and applications, 18, 65 Heavy metal tolerance in plants, 7,2 Herbivores and plant tannins, 19, 263 Human ecology as an interdisciplinary concept: a critical inquiry, 8, 2 Industrial melanism and the urban environment, 11, 373 Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences, 23, 187 Insect herbivory below ground, 20, 1 Integration, identity and stability in the plant association, 6, 84 Isopods and their terrestrial environment, 17, 188 Landscape ecology as an emerging branch of human ecosystems science, 12, 189 Litter production in forests of the world, 2, 101 Mathematical model building with an application to determine the distribution of Dursbane insecticide added to a simulated ecosystem, 9, 133 Mechanisms of microarthropod-microbial interactions in soil, 23, 1 The method of successive approximation in descriptive ecology, 1, 35 Modeling the potential response of vegetation to global climate change, 22, 93 Mutualistic interactions in freshwater modular systems with molluscan components, 20, 126 Mycorrhizal links between plants: their functioning and ecological significance, 18, 243 Mycorrhizas in natural ecosystems, 21, 171 Nutrient cycles and H' budgets of forest ecosystems, 16, 1 On the evolutionary pathways resulting in C, photosynthesis and crassulacean acid metabolism (CAM), 19, 58 Oxygen availability as an ecological limit to plant distribution, 23, 93 The past as a key to the future: The use of palaeoenvironmental understanding to predict the effects of man on the biosphere, 22, 257 Pattern and process in competition, 4, 1 Phytophages of xylem and phloem: a comparison of animal and plant sap-feeders, 13, 135 The population biology and turbellaria with special reference to the freshwater triclads of the British Isles, 13, 235

CUMULATIVE LIST OF TITLES

355

Population cycles in small mammals, 8, 268 Population regulation in animals with complex life-histories: formulation and analysis of a damselfly model, 17, I Positive-feedback switches in plant communities, 23, 263 The potential effect of climate changes on agriculture and land use, 22, 63 Predation and population stability, 9, 1 Predicting the responses of the coastal zone to global change, 22, 212 The pressure chamber as an instrument for ecological research, 9, 165 Principles of predator-prey interaction in theoretical experimental and natural population systems, 16, 249 The production of marine plankton, 3, 117 Production, turnover, and nutrient dynamics of above- and below-ground detritus of world forests, 15, 303 Quantitative ecology and the woodland ecosystem concept, 1, 103 Realistic models in population ecology, 8, 200 Relative risks of microbial rot for fleshy fruits: significance with respect to dispersal and selection for secondary defense, 23, 35 Renewable energy from plants: bypassing fossilization, 14, 57 Responses of soils to climate change, 22, 163 Rodent long distance orientation (“homing”), 10, 63 Secondary production in inland waters, 10, 91 The self-thinning rule, 14, 167 A simulation model of animal movement patterns, 6, 185 Soil arthropod sampling, 1, 1 Soil diversity in the tropics, 21, 316 Stomata1 control of transpiration: Scaling up from leaf to region, 15, 1 Structure and function of microphytic soil crusts in wildland ecosystems of arid to semi-arid regions, 20, 180 Studies on the cereal ecosystem, 8, 108 Studies on grassland leafhoppers (Auchenorrhyncha, Homoptera) and their natural enemies, 11, 82 Studies on the insect fauna on Scotch Broom Sarothamnus scoparius (L.) Wimmer, 5, 88 Sunflecks and their importance to forest understorey plants, 18, 1 A synopsis of the pesticide problem, 4, 75 Theories dealing with the ecology of landbirds on islands, 11, 329 A theory of gradient analysis, 18, 271 Throughfall and stemflow in the forest nutrient cycle, 13, 57 Towards understanding ecosystems, 5, 1 The use of statistics in phytosociology, 2, 59 Vegetation, fire and herbivore interactions in heathland, 16, 87 Vegetational distribution, tree growth and crop success in relation to recent climate change, 7, 177 The zonation of plants in freshwater lakes, 12, 37


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