Phenology: An Integrative Environmental Science

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PHENOLOGY: AN INTEGRATIVE ENVIRONMENTAL SCIENCE

Tasks for vegetation science 39 SERIES EDITORS A. Kratochwil, University of Osnabrück, Germany H. Lieth, University of Osnabrück, Germany

The titles published in this series are listed at the end of this volume.

PHENOLOGY: An Integrative Environmental Science

Edited by

MARK D. SCHWARTZ Department of Geography, University of Wisconsin – Milwaukee, Milwaukee, WI, U.S.A.

KLUWER ACADEMIC PUBLISHERS DORDRECHT / BOSTON / LONDON

A C.I.P. Catalogue record for this book is available from the Library of Congress.

ISBN 1-4020-1580-1

Published by Kluwer Academic Publishers, P.O. Box 17, 3300 AA Dordrecht, The Netherlands. Sold and distributed in North, Central and South America by Kluwer Academic Publishers, 101 Philip Drive, Norwell, MA 02061, U.S.A. In all other countries, sold and distributed by Kluwer Academic Publishers, P.O. Box 322, 3300 AH Dordrecht, The Netherlands.

Printed on acid-free paper

All Rights Reserved © 2003 Kluwer Academic Publishers No part of this work may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording or otherwise, without written permission from the Publisher, with the exception of any material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work. Printed in the Netherlands

Dedication

This book is dedicated to my parents, Marjorie H. and the late Donald J. Schwartz, who nurtured my early interest in science

v

Contents

Dedication

v

Contributing Authors

xi

Preface

xvii

Color Plates

xxi

Foreword

xxvii

Part 1: INTRODUCTION

1

1.1 Introduction MARK D. SCHWARTZ

3

Part 2: PHENOLOGICAL DATA, NETWORKS, AND RESEARCH

9

2.1 East Asia XIAOQIU CHEN

11

2.2 Australia MARIE R. KEATLEY AND TIM D. FLETCHER

27

vii

viii 2.3 Europe ANNETTE MENZEL

45

2.4 North America MARK D. SCHWARTZ AND ELISABETH G. BEAUBIEN

57

2.5 South America L. PATRÍCIA C. MORELLATO

75

2.6 The Global Phenological Monitoring Concept 93 EKKO BRUNS, FRANK-M. CHMIELEWSKI, AND ARNOLD J. H. VANVLIET 2.7 Toward a Multifunctional European Phenology Network ARNOLD J. H. VANVLIET AND RUDOLF S. DEGROOT

105

Part 3: PHENOLOGY OF SELECTED BIOCLIMATIC ZONES

119

3.1 Tropical Dry Climates 121 ARTURO SANCHEZ-AZOFEIFA, MARGARET E. KALACSKA, MAURICIO QUESADA, KATHRYN E. STONER, JORGE A. LOBO, AND PABLO ARROYO-MORA 3.2 Mediterranean Climates 139 DONATELLA SPANO, RICHARD L. SNYDER, AND CARLA CESARACCIO 3.3 Grasslands of the North American Great Plains GEOFFREY M. HENEBRY

157

3.4 High Latitude Climates FRANS E. WIELGOLASKI AND DAVID W. INOUYE

175

3.5 High Altitude Climates DAVID W. INOUYE AND FRANS E. WIELGOLASKI

195

Part 4: PHENOLOGICAL MODELS AND TECHNIQUES

215

4.1 Plant Development Models ISABELLE CHUINE, KOEN KRAMER, AND HEIKKI HÄNNINEN

217

ix 4.2 Animal Life Cycle Models JACQUES RÉGNIÈRE AND JESSE A. LOGAN

237

4.3 Phenological Variation of Forest Trees 255 ROBERT BRÜGGER, MATTHIAS DOBBERTIN, AND NORBERT KRÄUCHI 4.4 Phenological Growth Stages UWE MEIER

269

4.5 Assessing Phenology at the Biome Level XIAOQIU CHEN

285

4.6 Developing Comparative Phenological Calendars REIN AHAS AND ANTO AASA

301

4.7 Plant Phenological "Fingerprints" ANNETTE MENZEL

319

4.8 Phenoclimatic Measures MARK D. SCHWARTZ

331

4.9 Weather Station Siting 345 RICHARD L. SNYDER, DONATELLA SPANO, AND PIERPAOLO DUCE Part 5: REMOTE SENSING PHENOLOGY

363

5.1 Remote Sensing Phenology BRADLEY C. REED, MICHAEL WHITE, AND JESSLYN F. BROWN

365

Part 6: PHENOLOGY OF SELECTED LIFEFORMS

383

6.1 Aquatic Plants and Animals WULF GREVE

385

6.2 Insects KAREN DELAHAUT

405

6.3 Birds 421 TIM H. SPARKS, HUMPHREY Q. P. CRICK, PETER O. DUNN, AND LEONID V. SOKOLOV

x 6.4 Timing of Reproduction in Large Mammals ERIC POST

437

Part 7: APPLICATIONS OF PHENOLOGY

451

7.1 Vegetation Phenology inn Global Change Studies 453 MICHAEL A. WHITE, NATHANIEL BRUNSELL, AND MARK D. SCHWARTZ 7.2 Phenology of Vegetation Photosynthesis 467 LIANHONG GU, WILFRED M. POST, DENNIS BALDOCCHI, T. ANDY BLACK, SHASHI B. VERMA, TIMO VESALA, AND STEVE C. WOFSY 7.3 Radiation Measurements JIE SONG

487

7.4 Phenology and Agriculture FRANK-M. CHMIELEWSKI

505

7.5 Winegrape Phenology GREGORY V. JONES

523

7.6 Long-Term Urban-Rural Comparisons CLAUDIO DEFILA AND BERNARD CLOT

541

Acknowledgments

555

Index

557

Contributing Authors

Aasa, Anto, Institute of Geography, University of Tartu, Tartu, Estonia Ahas, Rein, Institute of Geography, University of Tartu, Tartu, Estonia Arroyo-Mora, Pablo, Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT, USA Baldocchi, Dennis, Department of Environmental Science, Policy & Management, University of California, Berkeley, CA, USA Beaubien, Elisabeth G., Devonian Botanic Garden, University of Alberta, Edmonton, Alberta, Canada Black, T. Andy, Faculty of Agricultural Sciences, University of British Columbia, Vancouver, Canada Brown, Jesslyn F., SAIC, USGS EROS Data Center, Sioux Falls, SD, USA Brügger, Robert, PHENOTOP, Institute off Geography of the University of Berne, Berne, Switzerland Brunns, Ekko, Department of Networks and Data, German Meteorological Service, Offenbach, Germany Brunsell, Nathaniel, Department of Civil Engineering, Duke University, Research Triangle, NC, USA

xi

xii Cesaraccio, Carla, Agroecosystem Monitoring Laboratory, Institute of Biometeorology, National Research Council, Sassari, Italy Chen, Xiaoqiu, Department of Geography, College of Environmental Sciences, Peking University, Beijing, China Chmielewski, Frank-M., Subdivision of Agricultural Meteorology, Institute of Crop Sciences, Faculty of Agriculture and Horticulture, HumboldtUniversity, Berlin, Germany Chuine, Isabelle, CEFE-CNRS, Montpellier, France Clot, Bernard, Biometeorology, MeteoSwiss, Zürich and Payerne, Switzerland Crick, Humphrey Q. P., British Trust for Ornithology, Thetford, UK Defila, Claudio, Biometeorology, MeteoSwiss, Zürich and Payerne, Switzerland deGroot, Rudolf S., Environmental Systems Analysis Group, Department of Environmental Sciences, Wageningen University, Wageningen, The Netherlands Delahaut, Karen, Department of Horticulture, University of WisconsinMadison, Madison, WI, USA Dobbertin, Matthias, WSL Swiss Federal Institute for Forest, Snow and Landscape Research, Forest Ecosystems and Ecological Risks Division, Birmensdorf, Switzerland Duce, Pierpaolo, Agroecosystem Monitoring Laboratory, Institute of Biometeorology, National Research Council, Sassari, Italy Dunn, Peter O., Department of Biological Sciences, University of Wisconsin-Milwaukee, Milwaukee, WI, USA Fletcher, Tim D., Department of Civil Engineering, Monash University, Clayton, Victoria, Australia Greve, Wulf, German Center for Marine Biodiversity Research (Senckenberg Research Institute), Hamburg, Germany

xiii Gu, Lianhong, Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA Hänninen, Heikki, Department of Ecology and Systematics, University of Helsinki, Helsinki, Finland Henebry, Geoffrey M., Center for Advanced Land Management Information Technologies (CALMIT), School of Natural Resources, University of Nebraska, Lincoln, NE, USA Inouye, David W., Department of Biology, University of Maryland, College Park, MD, USA Jones, Gregory V., Department of Geography, Southern Oregon University, Ashland, OR, USA Kalacska, Margaret E., Earth and Atmospheric Sciences Department, University of Alberta, Edmonton, Alberta, Canada Keatley, Marie R., School of Resource Management, University of Melbourne, Creswick, Victoria, Australia Kramer, Koen, Alterra, Department of Ecology and Environment, Wageningen University, Wageningen, The Netherlands Kräuchi, Norbert, WSL Swiss Federal Institute for Forest, Snow and Landscape Research, Forest Ecosystems and Ecological Risks Division, Birmensdorf, Switzerland Lobo, Jorge A., Biology Department, Universidad de Costa Rica, San Jose, Costa Rica Logan, Jesse A., USDA Forest Service, Logan, Utah, USA Meier, Uwe, Federal Biological Research Center for Agriculture and Forestry, Braunschweig, Germany Menzel, Annette, Department of Ecology, TU Munich, Freising, Germany Morellato, L. Patrícia C., Departmento de Botânica, Plant Phenology and Seed Dispersal Research Group, Universidade Estadual Paulista, São Paulo, Brasil

xiv Post, Eric, Department of Biology, The Pennsylvania State University, University Park, PA, USA Post, Wilfred M., Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA Quesada, Mauricio, Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Morelia, México Reed, Bradley C., SAIC, USGS EROS Data Center, Sioux Falls, SD, USA Régnière, Jacques, Natural Resources Canada, Canadian Forest Service, Quebec, Canada Sanchez-Azofeifa, Arturo, Earth and Atmospheric Sciences Department, University of Alberta, Edmonton, Alberta, Canada Schwartz, Mark D., Department of Geography, University of WisconsinMilwaukee, Milwaukee, WI, USA Snyder, Richard L., Department of Land, Air, and Water Resources, University of California, Davis, CA, USA Sokolov, Leonid V., Russian Academy of Sciences, St. Petersburg, Russia Song, Jie, Department of Geography, Northern Illinois University, Dekalb, IL, USA Spano, Donatella, Department of Economics and Woody Plant Ecosystems, University of Sassari, Sassari, Italy Sparks, Tim H., Centre for Ecology and Hydrology, Monks Wood, UK Stoner, Kathryn E., Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Morelia, México vanVliet, Arnold J. H., Environmental Systems Analysis Group, Department of Environmental Sciences, Wageningen University, Wageningen, The Netherlands Verma, Shashi B., School of Natural Resource Sciences, University of Nebraska, Lincoln NE, USA

xv Vesala, Timo, Department of Physical Sciences, University of Helsinki, Helsinki, Finland White, Michael, Department of Aquatic, Watershed, and Earth Resources, Utah State University, Logan, UT, USA Wielgolaski, Frans E., Department of Biology, University of Oslo, Oslo, Norway Wofsy, Steve C., Department of Earth and Planetary Sciences, Harvard University, Cambridge, MA, USA

Preface

I recall as a doctoral student at the University of Kansas discussing dissertation topics with my advisor, Prof. Glen A. Marotz, one day in 1983. He had just suggested to me that phenology was an interesting topic, and one that held promise for important research contributions in the future. “What’s that?” I asked, thus beginning my career as a phenologist, and the long path that led to my editorship of this volume. Skipping ahead a decade, I was encouraged by my colleague Elisabeth Beaubien to attend the 13th International Congress of Biometeorology, which was being held in Calgary, Alberta, Canada that year. I did attend, and also met Prof. Dr. Helmut Lieth there for the first time. I had corresponded with him while writing my dissertation, having gained much insight from his seminal book, Phenology and Seasonality Modeling g at that time. At the Calgary meetings Prof. Lieth helped Elisabeth and I reactivate a Phenology Study Group within the International Society of Biometeorology (ISB). The first workshop of the new group was organized by Dipl.-Met. Hartmut Scharrer of the German Weather Service (DWD) Phenology unit, and scheduled for May 1995. As a UW-Milwaukee assistant professor in the Geography Department at the time, I had never traveled outside of North America, and further did not have a source of travel funding for the trip to Offenbach (just outside Frankfurt), Germany. So I consulted the associate dean responsible for our department, G. Richard Meadows (now Dean of the College of Letters and Science) and he was able to provide me with funds to cover the airfare (after I assured him that this trip would be an important one for establishing my connection to international phenological research). At the Offenbach workshop the thirteen participants proposed an organizational structure and laid out a set of objectives for the Phenology Study Group.

xvii

xviii Some subsequent early activities included the launching of a new journal Phenology and Seasonality (unfortunately discontinued after one issue), and participation in the 14th International Congress of Biometeorology (Ljubljana, Slovenia) in 1996. The study group’s first international scientific meeting was a “Phenology Symposium” that I organized in 1998 as a group of four paper, one poster and one discussion sessions (21 participants) held within the Association of American Geographers Annual meeting in Boston, MA, USA. The number of individuals involved with, amount of research being conducted in, and level of interest by scientists from other disciplines for phenology had all been slowly rising since the early 1990s. However, a series of papers published in Nature (over the 1997-2000 period) dramatically accelerated these trends, especially the interest of global change researchers in remote sensing and biology for phenological data and techniques. In recent years, this surge in interest from the global change research community, and corresponding funding by the European Union of several projects (POSITIVE and EPN, European Phenology Network) have led to a greater number of scientific conferences with increasing numbers of participants. Specifically, a first “stand alone” international phenology conference, organized by Dr. Annette Menzel and colleagues (2000, Freising, Germany, 70 participants), and two subsequent international conferences (organized by Arnold vanVliet and associates) held in Wageningen, The Netherlands in 2001 and 2003 connected with the EPN project (each had just over 100 participants). The two European projects have also supported a large number of workshops on specialized phenology topics for smaller groups of participants (including individuals from other parts of the world). Within the ISB, the study group participated in the 15th International Congress of Biometeorology (held in Sydney, Australia in 1999) and due to reorganization within the society was renamed the Vegetation Dynamics, Climate, and Biodiversity Commission after that meeting. Members of the new ISB commission also participated in the most recent ISB Congress (16th International Congress of Biometeorology, held in Kansas City, MO, USA in 2002). During that meeting the group requested, and was subsequently granted by ISB, the simplified current name “Phenology Commission.” So the sequence of events I have described created the conditions and provided resources to make development of this book possible, namely sufficient interest in the topic by the general scientific community, and an interconnected community of phenological researchers with the necessary diversity of research expertise to cover the range of required topics. Jacco Flipsen, a Kluwer editor, who wrote me a letter in early 2001 stating the need for and asking if I was interested in editing a book on plant phenology,

xix initiated the actual development of this volume. After some negotiation, specifically to allow the book to cover a broader range of phenological topics, the project began in earnest during the first months of 2002. The book was seamlessly transferred into Prof. Lieth’s “Tasks for Vegetation Science” series at Kluwer (supervised by Helen Buitenkamp) in early 2003, and completed later that year.

Mark D. Schwartz Milwaukee, March 2003

xxi

xxii

xxiii

xxvi

Foreword

I was pleased when Mark Schwartz invited me to write a foreword to his volume. And even more so after I had read the content and many of the papers contributed to the volume. My own book on the subject matter (Lieth 1974) appeared as vol. 8 in the famous ecological studies series by Springer, and a contribution to the then fully operating Analysis of Ecosystem program of the U.S. International Biological Program (US-IBP). Phenology was a rather quiet scientific objective at that time. Some operational networks existed in Europe and America mainly in agriculture. Only a few researchers in biology, ecology and meteorology were using the accumulated datasets at that point. Satellite image analyses and the development of new remote sensing techniques were of interest then, but the ground truth observation of biological fluctuating phenomena were regarded as outmoded. The common thrust of the papers presented at the 1972 phenology symposium of the American Institute of Biological Sciences conference in Minneapolis gave phenology work in the U.S. and Europe a big push, and ground truth observations in ecosystems studies were initiated in many parts of the world. The initial successes in modeling phenological events, the comparisons with meteorological parameters, and the correlation attempts with global remote sensing data sets caught the attention of the scientists, working at that time on global change initiated directly and indirectly by humans. This interest continues, and a book presenting the achievements of the last 30 years (two or three generations of graduate students) is very much needed. I followed the results with interest, because I had earlier made predictions that had to be tested, verified or modified through field

xxvii

xxviii observations. Phenological observations and experiments undertaken during the last 30 years have greatly improved insights into ecosystems operation. One of the major values for phenological data is their validation value for seasonality models. These models have gained prominence in global climatic change models to predict biosphere responses to climatic parameter changes. This, however, is by no means the only value of phenological work. The book presented here by Dr. Schwartz includes many other fields of biology for which phenological investigations are needed. The reliance of species association in ecosystems upon a quasi-correct seasonal behavior in a seasonal climate is so prominent, that most investigations and experiments include phenological aspects, be they climatic, physiologic or biochemical. Throughout the historical development of phenology, its practical applications in agriculture and forestry have dominated the field. The chapters in this volume dealing with the history of phenology by Menzel (Chapter 2.3) and Chen (Chapter 2.1) uncovered many local networks that I had not found in the early 1970s. While this is a valuable addition to the field, I found that several important networks and papers had still been neglected. The 1974 volume has, therefore, not completely lost its relevance for future generations of phenologists. The history of European phenology emphasizes agricultural and forest phenology and neglects the body of work started by Heinrich Walter, whose students and coworkers (e.g., Kreeb and Ellenberg) and these together with their coworkers made substantial contributions to phenology in Europe (see Walter 1960, which shows that he had much more influence on phenology than providing the widely used climate diagrams which are so easily available in the climate diagram world atlas by Walter and Lieth 1960ff., and now available on CD by Lieth et al. 1999). The Russian work on phenology is only partly recognized. For me a major omission appears to be the book by Alexander Podolski, which appeared about 2 decades ago in English (1984). His approach to identifying the start of a phenologically valid period from physiological data, rather than an arbitrary chosen, convenient calendar date, still warrants further analyses in relevant cases. Podolski’s volume also includes a wealth of literature otherwise not mentioned in Russian books that mostly refer to papers from west Russian institutes (covered by Dr. Menzel’s historical treatment in this volume). It appears to me that students interested in phenology should be encouraged to read some of the older papers by Hopkins (1938), Thornthwaite (several papers), Hopp, Caprio, a Schnelle and Volkert, and all the others as cited in Lieth (1974) and in this volume, as well as Walter (1960) and Podolski (1984). The literature on remote sensing and global change applications is so new, that for the purpose of this book’s users, the

xxix authors in this area of research will be available in current relevant journals. Many authors of these papers will not include their contribution as part of phenology, but their work deals very often with topics that would be included in seasonality, climate and species fluctuations, global change and methods for the investigation of these topics. All this is phenology in the wider sense. The historical assessment in another 30 years will evaluate the importance of these authors and developments for phenological work. Work on satellite remote sensing had just started around the time I compiled my phenology book. The same was true for computer mapping, which was in its infancy as well. But the combination of data available from different phenological networks in the U.S. through computer modeling and computer mapping was so attractive to graduate students, that many of them choose phenological topics for their degree papers. When I developed my volume in the early 1970s I was greatly supported by Forrest Stearns who was a professor at the University of Wisconsin-Milwaukee. Wisconsin was an intellectual center for phenology at that time where the Lettaus (Heinz and Katharina) provided guidance in meteorological and phenological observations. No wonder then that phenology received new impulses from Wisconsin. In summary I can say that this book edited by Dr. Schwartz shows that phenology is as alive and important as ever. Like any other field of research it undergoes peaks and valleys in recognition. As long as planet earth tumbles around the sun, there will be ecologists and meteorologists, foresters and agronomists, insurance people and a wealth of other specialists observing, measuring and evaluating phenological data. Many of them will use this book. I thank also the responsible persons in Kluwer academic publishers for their interest in presenting this volume with the usual Kluwer quality. I am sure that the book will obtain the worldwide reception accorded many of other previous volumes of the T:VS series.

Helmut Lieth Osnabrück, February 2003

REFERENCES CITED Hopkins, A. D., Bioclimatics–A science of life and climate relations, U.S. Dept. Agr. Misc. Publ. 280, 1938. Lieth, H., editor, Phenology and Seasonality Modeling, Springer-Verlag, New York, 444 pp., 1974.

xxx Lieth, H., J. Berlekamp, S. Fuest, and S. Riediger, Climate Diagram World Atlas on CD (unpaginated electronic publication), Backhuys Publishers, Leiden, Netherlands, 1999. Podolski, A. S., New Phenology: Elements of mathematical forecasting in ecology, John Wiley and Sons, New York, 504 pp., 1984. Walter, H., Grundlagen der Pflanzenverbreitung, part 1 Standortslehre, Eugen Ulmer Verlag, Stuttgart, Germany, 566pp., 1960. Walter, H. and H. Lieth, Klimadiagramm-Weltatlas (unpaginated), VEB Gustav Fischer, Jena, 1960ff.

PART 1

INTRODUCTION

Chapter 1.1 INTRODUCTION Mark D. Schwartz Department of Geography, University of Wisconsin-Milwaukee, Milwaukee, WI, USA

Key words:

1.

Definitions, Environment, Organization, Modeling, Global Change

BASIC CONCEPTS AND BACKGROUND

Phenology, which is derived from the Greek word phaino meaning to show or to appear, is the study of periodic biological events in the animal and plant world as influenced by the environment, especially temperature changes driven by weather and climate. Sprouting and flowering of plants in the spring, color changes of leaves in the fall, bird migration and nesting, insect hatches, and animal hibernation are all examples of phenological events (Dubé et al. 1984). Seasonality is a related term, referring to similar non-biological events, such as timing of the fall formation and spring breakup of ice on fresh water lakes. Human knowledge and activities connected to what is now called phenology are probably as old as civilization itself. Surely, soon after farmers began to continuously dwell in one place—planting seeds, observing crop growth, and carrying out the harvest year after year—they quickly became aware of the connection of changes in their environment to plant development. Ancient records and literature, such as observations taken up to 3000 years ago in China (see Chapter 2.1), and references in the Christian Bible, testify to a common level of understanding about phenology among early peoples: “Learn a lesson from the fig tree. Once the sap of its branches runs high and it begins to sprout leaves, you know that summer is near.” Gospel of Mark 13:28 Schwartz (ed.), PHENOLOGY: AN INTEGRATIVE ENVIRONMENTAL SCIENCE, 3-7 © 2003 Kluwer Academic Publishers. Printed in the Netherlands.

4

Phenology: An Integrative Environmental Science

Unfortunately, these ancient “roots” did not translate into systematic data collection across large areas over the centuries, nor did they provide impetus for the early development of phenology as a scientific endeavor and discipline. For a long time the field remained tied almost exclusively to agricultural applications, and even those were only deemed practical on the local scale (i.e., every place was different, and generalizations difficult or impossible). With the establishment of continuous and continental-scale observation networks by the mid-1900s (though still largely confined to Europe, see Chapter 2.3), and contributions of early researchers such as Schnelle (1955), phenology began to emerge as an environmental science. Lieth’s (1974) book was the first modern synthesis to chart the interdisciplinary extent of the field, and demonstrate its potential for addressing a variety of ecological system and management issues. These foundations have prepared the way for this volume.

2.

ORGANIZATION AND USE

Phenological research has traditionally been identified with studies of mid-latitude plants (mostly trees and shrubs) in seasonal climates, but other areas of the field are also progressing. Thus, a principal goal in organizing this book was to overcome this mid-latitude plant bias with a structure that would facilitate a thorough examination of wider aspects of phenology. After this introduction, the second section, Phenological Data, Networks, and Research, adopts a regional approach to assess the state and scope of phenological research with chapters on East Asia (2.1), Australia (2.2), Europe (2.3), North America (2.4, excluding Mexico), and South America (2.5). Several major regions, most notably Africa and central Asia were not included due to my inability to identify researchers working in these geographical areas. While some efforts were made in these chapters to survey the history of regional data collection and research, more emphasis was given to an assessment of recent developments. My assumption was that since Lieth’s (1974) book had make an extensive survey of the history of phenological research up to the early 1970s, there was no great need to reproduce all that historical information in this volume. Two other chapters in this section explore a plan for a global monitoring network (2.6), and the multifunctional capabilities and uses of continental-scale phenological network data (2.7). Section 3, Phenology of Selected Bioclimatic Zones, examines phenological research in areas outside of mid-latitudes, with chapters on Tropical Dry Climates (3.1) and High Latitude Climates (3.4). Other chapters document phenology in drier mid-latitude biomes, including

Chapter 1.1: Introduction

5

Mediterranean Climates (3.2) and Grasslands of the North American Great Plains (3.3). Lastly, the special phenological responses of High Altitude Climates are explored in Chapter 3.5. Phenological Models and Techniques (Section 4) presents a survey of phenological research methodologies and strategies. Model building and development is outlined in chapters addressing plants (4.1), animal life cycles (4.2, concentrating on insects), and Phenoclimatic Measures (4.8). The challenges of phenological variability within species are explored in Chapter 3.3, and other chapters address the issues of temperature measurement (4.9), standardization of phenological event definitions (4.4), and development of phenological calendars (4.6). The remaining chapters in this section detail methods to detect climate change (4.7) and assess biome level phenology (4.5). The next section (5) is devoted entirely to the emerging area of remote sensing phenology. Section 6, Phenology of Selected Lifeforms looks at research and developments in animal phenology, including chapters on Aquatic Plants and Animals (6.1), Insects (6.2), Birds (6.3), and Timing of Reproduction in Large Mammals (6.4). The final section of the book (7) details Applications of Phenology to a variety of topics. Chapter 7.1 looks specifically at Vegetation Phenology in Global Change Studies, Chapter 7.2 explores frontiers related to the Phenology of Vegetation Photosynthesis, and Chapter 7.3 Phenological Effect on Radiation Measurements. Several remaining chapters in this section explore applications in traditional field agriculture (7.4) and winegrape growth and care (7.5). Lastly, phenological applications to Long-Term Urban-Rural Comparisons are examined in the final chapter of this section (7.6). Therefore, this volume’s structure is primarily designed to serve the basic reference needs of phenological researchers and students interested in learning more about specific aspects off the field, or evaluating the feasibility of new ideas and projects. However, it is also an ideal primer for ecologists, climatologists, remote sensing specialists, global change scientists, and motivated members of the public who wish to gain a deeper understanding of phenology and its potentials.

3.

FUTURE DIRECTIONS AND CHALLENGES

When I chose the name for this book, I deliberately selected the word “integrative” because of its implication of a process. Phenology is an interdisciplinary environmental science, and as such brings together individuals from many different scientific backgrounds, but the full benefits of their combined disciplinary perspectives to enrich phenological research

6


have yet to be realized. Thus, the term “integrative” as in moving together, rather than “integrated,” implying already being together. The last five years have seen rapid progress in the transmission of “phenological perspectives” into the mainstream of science, especially related to the needs of global change research. While other parts of phenological research are still important and need to progress, it is global change science that will stimulate, challenge, and transform the discipline of phenology most in the coming decades. In order to maximize the benefits of phenology for global change research as rapidly as possible, commitments to integrative thinking and large-scale data collection must continue. First of all, the limitations of the primary forms of data collection (remote sensing derived, native species, cloned indicator species, and model output) must be accepted. None of these data sources can meet the needs of all research questions, and an “integrative approach” that combines data types provides synergistic benefits (Schwartz 1994, 1999). The most needed data are traditional native and cloned plant species observations. Networks that select a small number of common plants for coordinated observation among national and global scale networks will prove the most useful. These networks should be embraced and integrated into the missions of national weather services around the world, as is now the case in many European countries (see Chapter 2.3). A little more than one hundred years ago, the countries of the world began to cooperate in a global-scale network of weather and climate monitoring stations. The results of this long-term investment are the considerable progress that has been made in understanding the workings of the earth’s climate systems. I believe that we have a similar opportunity with phenological data, and that small investments in national and global-scale observation networks are crucial to global change science, and will yield an impressive return in the years ahead.

REFERENCES CITED Dubé, P. A., L. P. Perry, and M. T. Vittum, Instructions for phenological observations: Lilac and honeysuckle, Vermont Agricultural Experiment Station Bulletin 692, University of Vermont, Burlington, 7 pp., 1984. Lieth, H., editor, Phenology and Seasonality Modeling, Springer-Verlag, New York, 444 pp., 1974. Schnelle, F., Pflanzen-Phänologie, Akademische Verlagsgesellschaft, Geest and Portig, Leipzig, 299 pp., 1955. Schwartz, M. D., Monitoring global change with phenology: the case of the spring green wave, Int. J. Biometeorol., 38, 18-22, 1994.

Chapter 1.1: Introduction

7

Schwartz, M. D., Advancing to full bloom: planning phenological research for the 21st century, Int. J. Biometeorol., 42, 113-118, 1999.

PART 2

PHENOLOGICAL DATA, NETWORKS, AND RESEARCH

Chapter 2.1 EAST ASIA Xiaoqiu Chen Department of Geography, College of Environmental Sciences, Peking University, Beijing, China

Key words:

China, Japan, Networks, Models, Data

1.

PHENOLOGICAL OBSERVATION AND RESEARCH IN CHINA

1.1

Historical Background

Modern phenological observation and research in China started in the 1920s with Dr. Kezhen Zhu (1890-1974), who may be regarded as the founder of modern Chinese phenology. As early as 1921 he observed spring phenophases of several trees and birds in Nanjing. In 1931, he summarized phenological knowledge from the last 3000 years in China. He also introduced phenological principles (e.g. species selection, criteria of phenological observations and phenological laws) developed in Europe and the United States from the middle of the eighteenth to the early twentieth century (Zhu 1931). In 1934, he organized and established the first phenological network in China. Observations of some 21 species of wild plants, 9 species of fauna, some crops, and several hydro-meteorological events ceased in 1937 because of the War of Resistance Against Japan (1937-1945). Twenty-five years later the Chinese Academy of Sciences (CAS) established a countrywide phenological network under the guidance of Dr. Zhu. The observations began in 1963 and continued until 1996. Observations resumed in 2003, but with a reduced number of stations, Schwartz (ed.), PHENOLOGY: AN INTEGRATIVE ENVIRONMENTAL SCIENCE, 11-25 © 2003 Kluwer Academic Publishers. Printed in the Netherlands.

12


species, and phenophases. In addition, the Chinese Meteorological Administration (CMA) established a countrywide phenological network in the 1980s.

1.2

Networks and Data

The observation program of the CAS network included a total of 173 observed species. Of these, 127 species of woody and herbaceous plants had a localized distribution. Table 1 lists the 33 species of woody plants, two species of herbaceous plants, and 11 species of fauna that were observed across the network (Institute of Geography at the Chinese Academy of Sciences 1965, Table 1). Since 1973, several stations added phenological observation of major crops. These observations were carried out mainly by botanical gardens, research institutes, universities and middle schools according to uniform observation criteria (Institute of Geography at the Chinese Academy of Sciences 1965; Wan and Liu 1979). The phenophases of woody plants included bud-burst, first leaf unfolding, 50% leaf unfolding, flower bud or inflorescence appearance, first bloom, 50% bloom, the end of blooming, fruit or seed maturing, fruit orr seed shedding, first leaf coloration, full leaf coloration, first defoliation, and the end of defoliation. The Institute of Geography at the Chinese Academy of Sciences took responsibility for collecting the phenological data and publishing them. Changes to the stations and in observers over the years resulted in data that were spatially and temporally inhomogeneous. The number of active stations has varied over time. The largest number of stations operating was 69 in 1964 and the lowest number occurred between 1969 and 1972 with only four to six stations active. The phenological data from 1963 to 1988 were published in form of Yearbooks of Chinese Animal and Plant Phenological Observation. Table 2.1-1. Common observation species of the CAS phenological network in China. Woody plants Ginkgo biloba L. Metasequoia glyptostroboides Hu et Cheng Thuja orientalis L. Juniperus chinensis L. Populus simoniii Carr. Populus canadensis Moench. Salix babylonica L. Juglans regia L. Castanea mollissima Blume. Quercus variabilis Blume.

Chapter 2.1: East Asia

13

Woody plants Ulmus pumila L. Morus alba L. Broussonetia papyrifera (L.) Vent. Paeonia suffruticosa Andr. Magnolia denudata Desr. Firmiana simplex W. F. Wight. Malus pumila Mill. Prunus armeniaca L. Prunus persica Stokes. Prunus davidiana (Carr.) Franch. Albizzia julibrissin Durazz. Cercis chinensis Bge. Sophora japonica L. Robinia pseudoacacia L. Wisteria sinensis Sweet. Melia azedarach L. Koelreuteria paniculata Laxm. Zizyphus jujuba Thunb. Hibiscus syriacus L. Lagerstroemia indica L. Osmanthus fragrans Lour. Syringa oblata Lindl. Fraxinus chinensis Roxb. Herbaceous plants Paeonia lactiflora Pall. Chrysanthemum indicum L. Fauna Apis mellifera L. Apus apus pekinensis (Swinhoe) Hirundo rustica gutturalis Scopoli. Hirundo daurica japonica Temminck et Schlegel. Cuculus canorus Subspp. Cuculus micropterus micropterus Gould. Cryptotympana atrata Fabr. Gryllulus chinensis Weber (Gryllus berthallus Sauss.) Anser fabalis Subspp. Oriolus chinensis diffusus Sharpe. Rana esculenta L.

The CMA phenological network is affiliated with the national-level agrometeorological monitoring network and came into operation in 1980.

14


The phenological observation criteria for woody and herbaceous plants, and fauna were adopted from the CAS network. r There are 28 common species of woody plants, one common species of herbaceous plant and 11 common species of fauna. The main phenophases are the same as those of the CAS network. In addition to the natural phenological observations, the network also carries out professional phenological observation of crops on the basis of a specific observation criterion (National Meteorological Administration 1993). The main crop varieties include rice, wheat, corn, grain sorghum, millet, sweet potato, potato, cotton, soybean, rape, peanut, sesame, sunflower, sugarcane, sugar beet, and tobacco. The CMA network is the largest phenological observation system in China at present. There were 587 agrometeorological measurement stations in 1990, of these about 400 stations were undertaking phenological observations. As the phenological and meteorological observations are parallel in this network, the data are especially valuable for understanding phenology-climate relationships. These data can also be used to provide agrometeorological service and prediction on crop yield, soil moisture and irrigation amounts, plant diseases and insect pests, and forest fire danger (Cheng et al. 1993). Guodong Yang and Xiaoqiu Chen established another phenological observation network in 1979, which operated until 1990. The network consisted of approximately 30 stations in the Beijing area under a research project financially supported by the Beijing Higher Education Bureau. Using these data, they worked out and published a series of phenological calendars of the Beijing area (Yang and Chen 1995).

1.3

Research and Applications

Modern phenology research in China focuses mainly on the following: – The development and application of phenological calendars, – Defining phenological seasons and phenological growing seasons, – Phenological mapping, – Phenological modeling and prediction, – Phenology and historical climate change, – Remote sensing of phenophases, and etc. Some important aspects are summarized below. 1.3.1

Phenological calendars

After obtaining the raw phenological data, the primary aim is to compile local phenological calendars that can be used as biological indicators to detect seasonality and do farm work in the right season. Kezhen Zhu and

Chapter 2.1: East Asia

15

Minwei Wan compiled the first phenological calendar based on observational data from 1950 to 1972 in Beijing. This phenological calendar was published in the book Phenology (Zhu and Wan 1973) and consisted of the average, earliest, and latest dates of 129 phenological events. In the 1980s, the Institute of Geography at CAS devised uniform criteria to compile phenological calendar at stations of the CAS network. All together 45 phenological calendars in China were published (Wan 1986, 1987). In each phenological calendar, the main phenological events of plants and fauna, and hydro-climatic events were chosen to represent an ordinal succession of phenophases in the annual cycle at each station. In order to detect the spatial difference of phenological occurrence dates in a relatively small area, a specific observation network was established in the Beijing area (16807.8 km2), which operated between 1979 and 1990. Based on the observed data of this network, 16 phenological calendars were compiled, about one phenological calendar per 1000 km2 (Yang and Chen 1995). In contrast to the phenological calendars of the CAS observation network, each phenological calendar in the Beijing area included almost all observed phenological occurrence dates in order to represent a more detailed and continuous succession of phenophases at the location. In addition, except for the average, the earliest and latest dates of phenological events as well as the standard deviation were calculated to describe the general temporal fluctuation of each phenological event. The results showed that the spatial difference of the average occurrence dates of a spring phenophase was 3-7 days between urban and rural areas on the plain, but it reached 10 days to one month between plain and mountain areas. Generally speaking, phenophases during spring and summer appeared first in the urban area and then in rural and mountainous areas; in contrast, phenophases during autumn and early winter appeared first in mountainous and rural areas and then in the urban area. 1.3.2

Phenological seasons

Phenological calendars describe the occurrence dates of various phenophases and their sequence in the annual cycle, whereas the phenological season represents characteristic stages of the phenological landscape. Several methods have been developed to determine phenological seasons at a station. An earlier method selected representative phenophases as indicators of particular seasons (Schnelle 1955). Since there were few common species of plants at some stations, using the same phenophase to identify a phenological season in a large region like China, is difficult. In order to be able to compare phenological seasons among different stations, both temperature and phenology indicators were applied to determine

16


seasons. According to Wan (1986), daily mean temperatures of 3°C and 19°C were thresholds indicating the beginning dates of spring and summer, whereas 19°C and 10°C were thresholds indicating the beginning dates of autumn and winter in China. Beginning dates of sub-seasons were also defined using other specific temperature thresholds. Based on beginning dates of the temperature seasons, corresponding phenological indicators were fixed by referring to the local phenological calendar. The phenological seasons in Beijing are shown in Table 2. However, observations showed that the same plant phenophase occurred under different air temperatures in different areas (Japanese Agrometeorological Society 1963; Reader et al. 1974). This indicates that the occurrence date of a phenophase results from the influence of a combination of environmental factors, including air temperature, precipitation, atmospheric humidity, radiation, soil conditions, etc. Therefore, in order to determine phenological seasons accurately, we should use pure phenological data. The relevant methods will be introduced in Chapter 4.5. Table 2.1-2. Phenological seasons in Beijing (1931-1982). Season

Temperature

Phenological indicator

Period (m/d)

Days

Early spring >3°C Prunus davidiana bb 3/8 – 3/14 7 Mid-spring >5°C Ulmus pumila fb 3/15 – 4/3 20 Late spring >10°C Prunus armeniaca fb 4/4 – 5/7 34 Early summer >19°C Robinia pseudoacacia 50%b 5/8 – 6/11 35 Mid-summer >24°C Albizzia julibrissin 50%b 6/12 – 7/18 37 Late summer 102 S (wild Society plants, trees, crops, animals, agrometeorlogical events), >32 P

Estonian Hydrometeorlogical Institute Environmental Agency of Slovenia

1948today

68* S 7P

9S 16 P

1951today

38 S

23 S

MeteoSchweiz

1951today

11 + 11S 6P 60 Ptot

1P

* The selection of native species is voluntary for the observers.

8S 11 P

3 + 1S 3P 8 Ptot

50


Unfortunately, the number of stations decreased from around 500 in the 1970s to 80 currently. The Swiss phenological observation network was founded in 1951 and initially consisted of 70 observation posts; the phenological observation program was slightly modified in 1996. The first phenological record in Slovenia is Scopoli's work Calendarium Florae Carniolicae from 1761. Modern phenology data collection started in 1950/1951 with the establishment of a phenological network within the Agrometeorological service, thus data are mainly used for research and applicable agriculture purposes. The recent network consists of 61 phenological stations, well distributed by a regional climatic key over the whole territory of Slovenia. The observations are carried out on species of non-cultivated plants (herbaceous plants, forest trees and bushes, clover and grasses) and of cultivated plants, such as field crops and fruit trees. In some portions of the Slovak and the Czech Republic, phenological observation was also conducted for a short time in the last half of the 19th century, but regular and managed phenological observation did not start until the 20th century. From 1923-1955, the observational program comprised more than 80 plant species (crops, fruit trees, native plants), but also some migratory birds, insects, as well as agro-technical data. From 1956 to 1985 observations were made following the first instruction guide edited by the Hydrometeorological Institute, with an enlarged program including, for example, agro-meteorological observations and crop diseases. In 1985/1986 a new system of phenological observation (including new guides) was instituted with three special sub-networks for field crops, fruit trees, and forest plants, and respective stations in regions with intensive agricultural production, in orchards and vineyard regions, and in forest regions. Three developmental stages (10%, 50%, and 100%) are now observed. In Slovakia, some historical stations were maintained in the (so called) “common” phenological network. In that network, general phenological observations (crops, fruit trees and grapevine, forest plants, migrating birds, some agro-meteorological and agro-technical data) are made by volunteers, in contrast to the “special” networks, where experts (e.g., with agronomic education) do the recording. In 1996 the guides for the common and special observation of forest plants were modified. The species and scales of phenophases are now very close to those in use before 1985. R area has many phenological observation programs The former USSR supervised mainly by Russian organizations. The Russian Geographical Society started phenological studies in 1850s with more than 600 observers, mostly in European Russia. Today, the archive of this voluntary network in St. Petersburg is one of the most important phenological centers in Russia, with more than two thousand observation sites all over the former USSR area, and regional subprograms which have different observation manuals

Chapter 2.3: Europe

51

and species lists (Hydrometeorological Printing House 1965; Schultz 1981). The second important network is the Hydrometeorological Service’s agrimeteorological observation program, organized by Schigolev in 1930, with a unique and strict methodology and very detailed observations of agricultural crops and some natural trees species, including climate parameters, such as soil temperature and moisture, snow and precipitation, at same site (Hydrometeorological Printing House 1973; Davitaja 1958). Today, the database at the central archive in Obninsk is not actively used, because the data is not digitized. Several other phenological observation programs exist that are run by the plant protection service, agricultural selection service, forestry department (Schultz 1982) or in Nature Conservation areas that use their materials for study and educational purposes (Kokorin et al. 2001). In Estonia, the first scientific phenological observation program (with more than 30 observed species) was set up in the botanical garden of University of Tartu in 1869, by the Estonian Naturalists Society (Oettingen 1882). The Estonian Naturalists Society started organized phenological studies in the 1920s / 1930s and a broad observation program in 1951 (Eilart, 1959). Today, the society is the most active voluntary observer of plant, bird, fish, phenology and seasonal phenomena in the country (Eilart 1968, ENS http://www.loodus.ee/lus/). The agri-phenological network of the Estonian Meteorological and Hydrometeorological Institute (started in 1948) used standard observation methods similar to those used in the former USSR (Hydrometeorological Printing House 1973; EMHI 1987). Their observation list consisted of agricultural plants, selected tree species, and main characteristics of the physical environment. Until the 1990s, 21 stations were still in operation (Ahas 2001), but that number diminished to 10 in 2001, and six in 2002. In Poland, the Hydrometeorological Institute ran a phenological network from 1951-1990 composed of around 70 stations. In the manual by Sokolowska (1980), phenological observations are described, and the main results are reported by Tomsazewska, and Rutkowski (1999). In Spain, the phenological network organized by the Spanish Meteorological Institute is characterized by an enormous number of stations, species, and phases, but less continuity of observations at single sites. The two examples of the British “Nature’s Calendar” and the Dutch “De Natuurkalender” stand as examples of phenological networks which have been set up recently, mostly run on the Internet, and organized by nongovernmental organizations (NGOs), media, and research institutions. They include a lot of observations on animals (e.g., birds and butterflies). A national phenological network in the United Kingdom was established by the Royal Meteorological Society in 1857. However, the subsequent development of British phenology was quite different from the continental

52


central European countries, as annual reports were published only up until 1948. In 1998 a pilot scheme to revive a phenology network in the UK was started by Tim Sparks, research biologist at the Centre for Ecology & Hydrology in Cambridge, comprising both plant and animal phases. In autumn 2000 the Woodland Trust forces joined with the Centre for Ecology & Hydrology to promote phenology to a far wider and larger audience. In 2001 the number of registered recorders across the UK rose to over 11,700, and by August 2002 it was 16,809 and still growing, with around half of these being online observers. The Nature’s calendar’s website (http://www.phenology.org.uk) provides information about the species observed, an online list of observations, and graphic presentations of trends. In February 2001, Wageningen University and the national radio program VARA Vroege Vogels (Early Birds) started a phenological monitoring network in the Netherlands, called De Natuurkalender. This network aimed to increase understanding of changes in the onset of phenological phases, also due to climate change, for human health, agriculture, and forestry. Other aims were to strengthen the engagement of the public in their natural surroundings and to develop interactive educational programs for school children and adults. The observation program includes over 100 species of plants, birds, and butterflies with at least one phenophase per species. The phenophases are clearly defined in an observation manual. Over 2000 volunteers subscribed to the program, and send their observations via the Internet, a paper form, or a special telephone line (Fenolijn) to the coordinators of the network. The observers and other potentially interested people are informed about the results of the observations by a weekly report during the radio program, which is followed by 500,000 people every Sunday morning. Furthermore, the network uses an interactive website to provide direct feedback to the observers.

4.

OTHER NETWORKS

This rough overview of phenological networks leaves many regions in Europe blank, due to the lack of current phenological networks in those places (e.g., Portugal, Greece). Other countries only have local networks due to regional organized research structure (e.g., Italy), current networks that are run by other institutions (e.g. Finland METLA, Norway), or they mainly have historical networks (e.g. Norway, Finland). Thus, this overview does not claim to be exhaustive, and it is fairly certain that in many other countries, national or regional networks existed, or are still running. An evaluation of the World Meteorological Organization (WMO) RA VI agro-meteorological questionnaire on phenological observations and

Chapter 2.3: Europe

53

networks revealed that from 28 replying countries only six countries (Belgium, Bosnia and Herzegovina, Denmark, Luxembourg, Portugal and the United Kingdom) had no regular (agro-meteorological) phenological network, whereas 22 countries (Armenia, Austria, Croatia, Czech Republic, Estonia, France, Germany, Hungary, Ireland, Italy, Israel, Latvia, Lithuania, Macedonia, Moldavia, Romania, Russia, Slovakia, Slovenia, Spain, Switzerland, Syrian Arabic Republic) have regular phenological networks (WMO 2000). However, following this WMO evaluation, the phenological observations, the applied observations methods, the structure of the networks, the coding systems, and the practical usage of data are highly diverse. The French phenological network that started in 1880 under the care of Meteo France may represent observations “fallen into oblivion.” Phenological observations have been reported continuously up to 1960 for most stations adjacent to meteorological stations, but only three of them continued their observations after that date, with the last one stopping in 2002. The conception of this network was similar to other central European ones still in operation, as the observational program comprised perennial wild species including trees (25 species), crops (10), and fruit trees (eight), and an instruction booklet was provided to observers to standardize observations. Observations are contained in archives, but have not been digitized. These data have not been analyzed, except at the very beginning of the network by C.A. Angot from Meteo France (in a few Annales du Bureau Central Météorologique) who mapped isolines of the onset of phenophases for the decade 1881-1891.

5.

CONCLUSIONS

The scientific community has a long list of requirements for monitoring. Long-term continuous data records of high quality are needed with good documentation, many auxiliary data, and often much more. Thus, special characteristics of the networks may be of interest to them. In general, observations are made by volunteers interested in nature, in special networks (Slovakia) or special stations (Germany, IPGs), or by experts. In the IPGs, observations are made on 3 specimens of each clone, whereas national networks’ rules describe how the observing area is defined and how the specimens have to be chosen in the near surroundings of a phenological station. Constant specimen and locations are desired, however only in Slovenia forest trees, shrubs, fruit trees, and vines are they permanently marked. All networks possess paper forms to note observations (even the new established networks in the UK and in the Netherlands do not want to

54


exclude “offline” recorders and developed forms). The requested frequency of submitting forms differs between once a year to weekly, and event-based information immediately. Data consistency and quality is difficult to evaluate. Most of the networks analyzed have monitoring guidelines, however they are very different, ranging from brand-new instructions, also available on the Internet (such as complete manual of ICP Forests, species and/or phenophase information of the Nature’s Calendar or the German Weather Service) or substantial printed manuals (Germany Weather Service), to descriptions used since the beginning of the network (IPG). Quality control of the data mostly consists of only simple plausibility control. Accompanying disaster information does not exist at the moment, but could be available in the future (e.g., ICP Forests). The general data release policy varies as well, and in most cases data are open on an individual decision basis only. Data formats are also quite different. In some countries older records still need to be digitized from paper, but most networks do have their data in ASCII files or databases. The Nature’s Calendar (with almost 50% online observers) offers quick data access for registered observers and allows different kinds of data comparisons. In the National Weather Services’ networks, observations on cultivated species are generally accompanied by information about varieties. However, associated data about the site (such as meteorology, soil, relief, and slope) are not available and (due to the coarse information about the station location) it is nearly impossible to gather exact auxiliary data. Two initiatives of the European Phenological Network (EPN project, see Chapter 2.7) may facilitate phenological research in the nearer future. The meta-database will hopefully provide a complete overview of all phenological networks in Europe including information about spatial and temporal extent, monitored species and classes, data consistency, data usage, and additional data. Coding of phenophases following the BBCH code (Chapter 4.4, Biologische Bundesanstalt 1997) may assist in understanding phenophase definitions in different languages and making observations comparable.

ACKNOWLEDGEMENTS I kindly thank my phenology colleagues Rein Ahas (Estonia), Olga Braslavska (Slovak Republic), Isabelle Chuine (France), Zoltan Dunkel (Hungary), Elisabeth Koch (Austria), Jiri Nekovar (Czech Republic), Tim Sparks (United Kingdom), Andreja Susnik (Slovenia), and Arnold vanVliet (The Netherlands) for their valuable support and information.

Chapter 2.3: Europe

55

REFERENCES CITED Ahas, R., Spatial and temporal variability of phenological phases in Estonia, Dissertationes Geographicae Universitatis Tartuensis 10, 1999. Ahas R. (Editor), Estonian phenological calendar, Publicationes Instituti Geographici Universitatis Tartuensis, 90, 206 pp., 2001. Baumgartner, A. and F. Schnelle, International Phenological Gardens (Purpose, results, and development), 16thh IUFRO World Congress Oslo Subject Group S1.03, 7 pp., 1976. Biologische Bundesanstalt für Land- und Forstwirtschaft (Editor), Growth Stages of Plants BBCH Monograph, Blackwell Wissenschafts-Verlag Berlin Wien, 622 pp., 1997. Chmielewski, F. M., The International Phenological Gardens across Europe. Present state and perspectives, Phenology and Seasonality, 1(1), 19-23, 1996. Chmielewski, F. M. and T. Rötzer, Response of tree phenology to climate change across Europe, Agricult. Forest Meteorol., 108, 101-112, 2001. Chmielewski F. M. and T. Rötzer, Annual and spatial variability of the beginning of growing season in Europe in relation to air temperature changes, Clim. Res., 19, 257-264, 2002. Davitaja, F. F., Agrometeorological problems, Moscow (in Russian with English Contents), Hydrometeorological Publishing House, 160 pp., 1958. Deutscher Wetterdienst (Ed.), Anleitung für die phänologischen Beobachter des Deutschen Wetterdienstes (BAPH), Offenbach am Main, 155 pp., 1991. Eilart, J., Phytophenological observation manual (in Estonian), Estonian Naturalists Society, Tartu, 16 pp., 1959. Eilart, J., Teaduse ajaloo ehekülgi Eestis, in Some aspects of history of phenology in Estonia, edited by Ü. Ü Lumiste (in Estonian with summary in German and Russian), Tallinn, Academy of Sciences, 1, 169-176, 1968. EMHI, Manual for Hydrometeorological Observation Stations and Points, Estonian Department of Hydrometeorology and Environmental Monitoring 11, I-II, Tallinn, 164 pp., 1987. Hydrometeorological Printing House, Natural calendars of North Western USSR (in Russian), Geographical Society of USSR, Hydrometeorological Printing House, Leningrad, 71 pp., 1965. Hydrometeorological Printing House, Methodology for hydrometeorological stations and observation points 11, Agri-meteorological observations in stations and observation points, 3rd edition (in Russian), Hydrometeorological Printing House, Leningrad, 186 pp., 1973. Kokorin A. O., A. V. Kozharinov, and A. A. Minin (Eds.), Climate change impact on Ecosystems, Nature protected areas in Russia, analyses of long-term observations, WWF Russia policy book No. 4 (in Russian with English Summaries), World Wildlife Foundation, 174 pp., 2001. Menzel, A., Phänologie von Waldbäumen unter sich ändernden Klimabedingungen, Dissertation at the Forest Faculty of the LMU Munich, Forstlicher Forschungsbericht 164, 1997. Menzel, A., Trends in phenological phases in Europe between 1951 and 1996. Int. J. Biometeorol., 44, 76-81, 2000. Menzel, A., Phenology, its importance to the global change community, Climatic Change, 54, 379-385, 2002. Menzel, A., and P. Fabian, Growing season extended in Europe, Nature, 397, 659, 1999. MeteoSchweiz (Editor), Pflanzen im Wandel der Jahreszeiten – Anleitung für phänologische Beobachtungen, Geographica Bernensia, 287 pp., 2003

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Oettingen, A.J. von, Phänologie der Dorpater Lignosen, in Archiv Naturk. Liv-, Est- u. Kurlands, II Serie. Bd. 8, pp. 241-352, Dorpat, 1882. Schnelle, F., Pflanzen-Phänologie, Akademische Verlagsgesellschaft, Geest and Portig, Leipzig, 299 pp., 1955. Schultz, G. E., General phenology (in Russian), Nauka, Leningrad, 186 pp., 1981. Schultz, G. E., Geographische Phänologie in der USSR (in German), Wetter und Leben, 34, 160-168, 1982. þ Ģ fenologických staníc PoĐné Đ SHMÚ Bratislava (Editor), Metodický predpis 2 Návod na þinnos plodiny (Manual for special crop station), 120 pp., 1988a. þ Ģ fenologických staníc SHMÚ Bratislava (Editor), Metodický predpis 3 Návod na þinnos Ovocné plodiny (Manual for special fruit and grapevine station), 136 pp., 1988b. SHMÚ Bratislava (Editor), Fenologické pozorovanie všeobecnej fenológie, Metodický predpis. (Manual for general stations), 126 pp., 1996a. SHMÚ Bratislava (Editor), Fenologické pozorovanie lesných rastlín, Metodický predpis (Manual for forest stations), 16 pp., 1996b. Sokolowska, J., Przewodnik fenologiczny, Instytut Meteorologii i Gospodarki Wodnej, Wydawnictwa Komunikacji i Lacznosci, Warszawa, 163 pp., 1980. Sparks, T.H. and P. D. Carey, The responses of species to climate over two centuries: an analysis of the Marsham phenological record, 1936-1947, J. Ecology, 83, 321-329, 1995. Tomsazewska, T., and Z. Rutkowski, Fenologiczne pory roku u uch zmiennosc w wieloleciu 1951-1990, Materialy Badawcze, Seris Meteorlogia – 28, Instytut Meteorologii i Gospodarki Wodnej, Warszawa, 39 pp., 1999. World Meteorological Organization, Commission for Agricultural Meteorology (Editor), Report of the RA VI Working Group on Agricultural Meteorology, CAgM report No. 82, WMO/TD No. 1022, 274 pp., 2000. Zentralanstalt für Meteorologie und Geodynamik, Anleitung zur phänologischen Beobachtung in Österreich, Anleitungen und Betriebsunterlagen Nr 1 der ZAMG, Wien, 31 pp., 2000.

Chapter 2.4 NORTH AMERICA Mark D. Schwartz1 and Elisabeth G. Beaubien2 1

Department of Geography, University of Wisconsin-Milwaukee, Milwaukee, WI, USA; Devonian Botanic Garden, University of Alberta, Edmonton, Alberta, Canada

2

Key words:

Agricultural Experiment Station networks, Lilacs, Royal Society, Plantwatch, Environment Canada

1.

UNITED STATES

1.1

Early Observations and Research

Throughout the early history of the United States, extending into the first years of the 20th century, there were few attempts to create organized phenological networks. One of the most noteworthy in this period was started by the Smithsonian Institution in 1851, and included observations on eighty-six plant species, birds, and insects in thirty-three states, but only lasted till 1859 (Hough 1864; Hopp 1974). A few individuals who were part of this and subsequent weather/climate observation networks did record phenological data at selected sites during other periods. For example, Dr. Samuel D. Martin’s April 1865 report (from Pine Grove, Kentucky) contains the dates of numerous phenological events (Martin 1865). Thomas Mikesell at Wauseon, Ohio, compiled another important local record over the period 1873-1912 (Smith 1915). Later instructions to Weather Bureau observers included lists of phenological phenomena to record (concentrating on agricultural crops, but also including timing of leaf opening and fall in deciduous forests, Weather Bureau 1899). However, there is little evidence to suggest that large numbers of observations were taken based on these Schwartz (ed.), PHENOLOGY: AN INTEGRATIVE ENVIRONMENTAL SCIENCE, 57-73 © 2003 Kluwer Academic Publishers. Printed in the Netherlands.

58


instructions. Hopp (1974) notes that the Weather Bureau made a final limited attempt to start a phenological network at twenty cooperative sites in the state of Indiana, during 1904-1908, and lists several other extensive local records taken in Indiana, Kansas, and Minnesota. An important phenological research contribution from the United States during the first half of the 20thh century was Hopkins’ (1938) “Bioclimatic Law.” The most well-known part of this law states that (other conditions being equal) the south to north progression of spring phenological events in temperate portions of North America is delayed by four days for each degree of latitude northward, for each five degrees of longitude eastward, and for each 400-foot increase in elevation. This model was developed from data available around the northern hemisphere at the time. Hopp (1974) observed that the law is highly generalized, has geographical limitations, and is difficult to apply to individual plant species in any one season. Despite these limitations, Hopkins’ Bioclimatic Law became one of the best-understood concepts of phenology for other scientists and the public. Paradoxically, its simplicity could have made phenology seem too easily predictable, which may have hindered and delayed efforts to develop new data collection networks, especially in the United States.

1.2

Agricultural Experiment Station Regional Networks

The first extensive U.S. phenological observation networks began in the 1950s with a series of regional agricultural experiment station projects, designed to employ phenology to characterize seasonal weather patterns and improve predictions of crop yield (Schwartz 1994). J. M. Caprio at Montana State University began the first of these projects, W-48 “Climate and Phenological Patterns for Agriculture in the Western Region” in 1957. This network contained up to 2500 volunteer observers distributed throughout 12 Western states (Caprio 1957, Figure 1). Common purple lilac plants (Syringa vulgaris) were observed initially, with two honeysuckle cultivars ((Lonicera tatarica ‘Arnold Red’ and L. korolkowiii ‘Zabeli’ added later. Observations ended in 1994, however, a few observers have again reported data since the later 1990s (Cayan et al. 2001). Encouraged by Caprio’s program, similar projects were started in the central U.S. (NC-26 “Weather Information for Agriculture”) by W. L. Colville at the University of Nebraska in 1961, and in the northeastern U.S. with the renewal of NE-35 (“Climate of the Northeast—Analysis and Relationships to Crop Response”) by R. Hopp at the University of Vermont in 1965. Both of these networks observed cloned plants of the lilac cultivar Syringa chinensis ‘Red Rothomagensis’ and the two honeysuckle cultivars from W-48. In 1970, NC-26 and NE-35 were combined as part of a new

Chapter 2.4: North America

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regional project, NE-69 “Atmospheric Influences on Ecosystems and Satellite Sensing.” The program expanded to about 300 observation sites (Figure 1), with three individuals as unofficial leaders: B. Blair (Purdue University), R. Hopp (University off Vermont), and P. Dubé (Laval University). In 1975 NE-69 was replaced by another new project, NE-95, “Phenology, Weather and Crop Yields,” which was replaced by still another, NE-135, “Impacts of Climatic Variability t on Agriculture” in 1980. This project was coordinated by M. T. Vittum (Cornell University) until 1985, when responsibility was turned over to R. C. Wakefield (University of Rhode Island). The phenology portion of NE-135 was briefly supervised by W. Kennard (University of Connecticut) until the eastern U.S. network lost funding and was terminated at the end of 1986.

Figure 2.4-1. Locations in North America with five years or more of lilac phenology data, 1956-2001 (Québec stations not included).

As an extension of the lilac/honeysuckle regional networks, a statewide phenological garden system of 12 stations operated in Indiana during the 1960s and 1970s. Numerous protocols were developed, and observations were taken on up to 14 species at each site (Blair et al. 1974). Also, an extensive phenology network observing redbud (Cercis canadensis),

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dogwood (Cornus florida), and red maple ((Acer rubrum) operated in North Carolina during the 1970s (Reader et al. 1974).

1.3

Network-Related Phenological Research

A large number of horticultural and physiological studies have reported results regarding site-specific phenological characteristics of (commercially important) fruit tree species, and general phenological responses of woody plants. These are adequately summarized elsewhere, and will not be addressed here (e.g., Flint 1974; Schwartz 1985; Schwartz et al. 1997). Relatively few researchers have taken advantage of the Agricultural Experiment Station Regional Network data to examine phenological relationships on the continental scale. Caprio (1974) was the first, developing the Solar Thermal Unit Concept from lilac phenological data recorded in the western U. S. These data were also used in a recent study to examine the relationship between lilac-honeysuckle phenology and the timing of spring snowmelt-runoff pulses, in the context of global change. Earlier spring onsets since the late 1970s are reported throughout most of the region (Cayan et al. 2001). Schwartz (1985) began an extensive phenological research program in the mid-1980s that has made intense use of lilac-honeysuckle network data from the eastern U. S. Areas explored include modeling, resulting in the Spring Indices (e.g., Schwartz 1998; Schwartz and Reiter 2000, and detailed discussion in Chapter 4.8), spring plant growth impacts on the lower atmosphere (e.g., Schwartz 1992; Schwartz and Crawford 2001), and analyses and comparisons to remote sensing measurements (discussed in Chapter 5.1)

1.4

Current Networks

After the “decommissioning” of eastern U. S. lilac-honeysuckle phenology network operations by the Agricultural Experiment Stations in 1986, M. D. Schwartz corresponded with the most recent network supervisors (Schwartz 1994). They granted him permission to contact the observers and invite them to continue participating in an “interim” network, pending new funding. Approximately 75 observers responded to a renewed survey form sent out in March 1988, returning data for 1988 and in many cases 1987 as well. From that time to the present, Schwartz has continued to operate this interim “Eastern North American Phenology Network” with approximately 50 observers reporting lilac or honeysuckle event dates each year (http://www.uwm.edu/~mds/enanet.html). Plans are underway to expand this network across the entire country, and add observation of events


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from a small number of appropriate native species at each site, following the example of Plantwatch Canada (see section 2.1.5). Another operational network of note is run by the Wisconsin Phenological Society (http://www.naturenet.com/alnc/wps/). Data for a large number of native and cultivated flowers and shrubs extend back to the early 1960s. Unfortunately, there is considerable variation in the number and types of plants observed at each site (selected from a standard form), and most individual station records are less than 10 years long. However, these data are now largely in digital form, and have contributed to an innovative methodological study exploring ways to “fill-in” the gaps in such incomplete Lastly, the GLOBE program records (Zhao and Schwartz 2003). (http://www.globe.gov), which works to get primary and secondary students involved in taking measurements and interacting with scientists has developed a number of phenology protocols (including a lilac phenology “special measurement” based on the Agricultural Experiment Station event descriptions).

2.

CANADA

Canada has a long and rich history of phenological observations. Since deglaciation some eight to ten thousand years ago, First Nations and Inuit have perfected their oral knowledge of “nature’s calendar” to maximize their survival and find resources efficiently across a wide landscape. The earliest recorded observations will likely be found in the journals of fur traders and missionaries. Phenological data “serve as a check of season against season, and region against region” (Minshall 1947, p.56). Phenological studies vary in the size of area surveyed and in the duration of observations, but they can basically be divided into three types: – the “snapshot” study, in which many observers survey phenology over a large area at one point in time. – the intensive study, in which one or a small number of people survey a small area over a period of one or more growing seasons. – the extensive study, in which a network of observers surveys a large area over a period of years. This article concentrates mainly on involvement of Canadians in such networks. The studies described here focus mostly on plant phenology and are divided into two major sections, national and regional networks. Firstly, the national networks described include extensive studies such as the Royal Society of Canada survey launched in 1881, participation by eastern Canadian observers in the NE Agricultural Project in the United States in the 1950s, and more recently Plantwatch, a program engaging Canadians with

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coordinators in each province and territory. Secondly, the regional and localized networks and research are described by region, from east to west, and in the north.

2.1

National Networks in Canada

2.1.1

First Nations and Inuit: traditional phenological knowledge

For Canada’s First Nations, phenology was a well-honed tool. The Blackfoot in Alberta used the flowering time of Thermopsis rhombifolia (golden bean or buffalo bean) to indicate the best time in spring to hunt bison bulls (Johnston 1987). In British Columbia more than twenty cultural/linguistic groups used over 140 indicators (Lantz and Turner, in press). These authors note that phenological indicators permitted the most efficient use of human resources in acquiring food or materials from the land. One example is that the west coast Nuu-Chah-Nulth peoples use the ripening of salmonberries (Rubus ( spectabilis) to indicate that adult sockeye salmon are starting to run in freshwater streams. Also the interior Stl’atl’imx peoples used the blooming of wild rose (Rosa spp.) to indicate the best time to collect cedar roots and basket grass. A third: the west coast Comox peoples used the bloom time of oceanspray (Holodiscus ( discolor) to alert them to dig for butter clams. In the Okanagan area, First Peoples observed that female black bears generally headed to dens when the western larch needles turned gold in the fall. Later denning often meant these bears would miscarry and not produce cubs (perhaps due to poor berry crops and thus insufficient weight gain). Across North America accurate timing was the key to survival, and phenology was “common sense” to those who lived so close to the land. 2.1.2

Royal Society of Canada survey

Only twenty-three years after Confederation in 1867, a countrywide phenology survey was initiated. In 1890 the Royal Society of Canada passed a resolution requesting affiliated natural history and scientific societies to: “obtain accurate records in their individual localities of meteorological phenomena, dates of the first appearance of birds, of the leafing and flowering of certain plants, and of any events of scientific interest for collation and publication in the ‘Transactions of the Society’” (Proceedings 1893, p. 54).


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In the following year, 1891, the Botanical Club of Canada was formed, affiliated with the Royal Society (MacKay 1899). One of its departments was responsible for promoting the nation-wide phenology survey, which initially included observations of 67 events. In 1897 this number increased to 100 events. These included recording the first bloom dates of many species of native plants, as well as the timing of migratory bird arrivals, thunderstorms, and ice melt on rivers. Blank schedules were distributed annually to past and potential observers with instructions to submit them by the end of January for compilation. In the first year, 1892, nine observers from Nova Scotia reported. In 1895, 25 reports were received from nine provinces. In general, the numbers of events and the diversity of locations increased over the duration of this extensive survey. The secretary of the Botanical Club, Dr. A. H. MacKay, coordinated the survey up until 1910 when the club was dissolved, and F.F. Payne of the Meteorological Service then coordinated the survey until 1922. With this change of coordination the number of events observed dropped to 50. Observations for 1892-1922 were published annually in the Proceedings and Transactions of the Royal Society of Canada. 2.1.3

Participation of Atlantic and Central provinces in U.S. Agricultural Experiment networks

The U.S. regional agricultural experiment station northeast project, NE69, added stations in several Canadian provinces in 1970 (see also section 1.2). The next year Quebec initiated a large observer network to track these plant species. Observations were made until 1977 at over 300 locations, of which 51 were adjacent to meteorological stations (Dubé and Chevrette 1978). Three indices (earliness index, summer index, and growing season index) were derived from the data, which were used to define bioclimatic zones. By 1977 observers in the six eastern provinces were involved. Quebec had the largest number of observers by far, with 268 active observation sites in 1977 versus New York State, the next largest, at 84 sites (Vittum and Hopp 1978). Pierre André Dubé of Laval University coordinated the Quebec participants and also computerized results for the whole project. Analysis of the phenological and meteorological data confirmed the existence of significant differences between phenological zones in Quebec (Castonguay and Dubé 1985). The resulting maps were used to modify agricultural taxation zones.

64 2.1.4

Phenology: An Integrative Environmental Science Canadian Forest Service (Natural Resources Canada): intensive studies

Several Forestry Centers have done intensive studies of the phenology of trees and insects, such as Parry et. al. (1997) but large networks of observations have not been established. Several historic data series of the phenology of three conifer species exist for New Brunswick and Quebec for 1975-2001. The phenology of the spring development of spruce budworm (Choristoneura fumiferana) in New Brunswick for 1950-1985 has been studied, by the Canadian Forest Service, the Quebec Ministry of Natural Resources, and the New Brunswick Department of Natural Resources and Energy. The data were being modeled and published at the time of writing (J. Regnière, Canadian Forest Service, Québec, personal communication, 2002). 2.1.5

Plantwatch: national network

Plantwatch began in 1995 based at the University of Alberta’s Devonian Botanic Garden. It has enlisted volunteers in North America and internationally to track spring bloom times of indicator plant species useful as key indicators for phenology (Beaubien 1997; Beaubien and Freeland 2000). Reporting has been via the Internet: (http://www.devonian.ualberta.ca/pwatch) where tables and maps of data were updated regularly, up to and including 2001 (see “archives” at this website). Initially the focus of this extensive survey was on students (ages eight to eleven years), reporting bloom dates for three plant species across the Prairie Provinces. By 1997 the survey had expanded to a Canada-wide program for both adults and youth, with seven indicator plants. For more information see the article posted at: http:// eqb-dqe.cciw.ca/eman/reports/publications/nm97_abstracts/part-31.htm (Beaubien 1997). International data were also gathered for one species Syringa vulgaris: common purple lilac. Beginning in the early 1990s Elisabeth Beaubien gave talks across Canada to encourage the formation of provincial plant phenology programs. A teacher guide was posted on the University of Alberta website (above) in 2001, providing curriculum applications in science, mathematics, social studies, etc. for students from elementary to high school level. In 2000-2002 Plantwatch expanded with assistance from Environment Canada’s Ecological Monitoring and Assessment Network Coordinating Office (EMAN CO). Elisabeth Beaubien, as national coordinator, made contacts to find coordinators for each of the provinces and territories. The coordinators met in Ottawa in May 2000 and in Winnipeg in November


65

2001. The national coordinator developed 14 criteria to select plant species best suited to a cross-Canada spring phenology survey by the public, and applied these to select 15 species. Each province and territory selected species from this list, with some coordinators adding more species suitable for their particular ecozones. The national coordinator researched phenology protocols used by the Deutscher Wetterdienst (weather service in Germany), and other European networks, to simplify and standardize the phenophase descriptions for first, full bloom, and leafing. First bloom was defined as “in at least three places on the observed tree or shrub, or patch of smaller plants, the first flowers have just opened.” Mid bloom (called full bloom in Germany) was when “50% of the flower buds were now open”. Leafing was defined as “when, in at least three places on the tree or shrub, the first leaves have emerged and unfurled completely.” In the spring of 2002 a booklet “Plantwatch: Canada in Bloom” was produced through the Canadian Nature Federation (CNF) and a webpage (http://www.plantwatch.ca) posted. Plantwatch is one of several environmental monitoring or “NatureWatch” programs currently sponsored by EMAN CO and CNF. Others are FrogWatch, WormWatch, and IceWatch.

2.2

Atlantic Region

2.2.1

Nova Scotia

2.2.1.1 Student network 1897 to 1923 Dr. A.H. MacKay (see section 2.1.2) was not only secretary for the Botanical Club of Canada, but also Superintendent of Education for Nova Scotia. He promoted phenology very successfully. The popularity of the program was such that in 1898, 800 sets of observations on up to 100 events were submitted by school classes (MacKay 1899). Observations by Nova Scotia schools continued as part of the Nature Studies curriculum until at least 1923 (MacKay 1927). 2.2.1.2 Recent networks This interest in Nova Scotia for tracking nature’s calendar has been rekindled through a number of programs. A “Peeper Program” started in 1994 based at the Nova Scotia Museum of Natural History, for the public to report calling dates of spring peeper frogs. Nova Scotia Plantwatch began in the spring of 1996, tracking bloom times for 12 plant species at about 200 sites. Liette Vasseur, Peta Mudie, Bob Guscott and others formed the initial team to promote and coordinate Plantwatch. They produced an observer’s guide, a webpage on the EMAN CO website, and a colorful newsprint poster of the 12 plant species. In 2001 Ed Reekie of Acadia University took over

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Liette Vasseur’s functions, summarizing the data and sending out annual newsletters. Fifteen plant species are now tracked. The results of the first three years (1996-1998) were compared with the MacKay data for the same species. For most species significant differences in bloom times were not found. (Vasseur et. al. 2001). It is interesting to note that climate records for Atlantic Canada show a cooling trend for 1948 to 1995. The “Thousand Eyes” project started in 2000 based at the Nova Scotia Museum of Natural History (http://www.thousandeyes.ca), first coordinated by Elizabeth Kilvert and later by Chris Majka. It gathers records via the Internet from students in Nova Scotia on timing of 50 events selected from the MacKay program. These include first blooms, bird migrations and weather events. Results are compared with student observations from a century ago. 2.2.2

New Brunswick

Dr. Liette Vasseur moved to the University of New Brunswick in 2001 and started a New Brunswick Plantwatch that tracks 12 species. Liette Vasseur and Diane Pruneau have worked with Atlantic region teachers to encourage participation by school classes in the NatureWatch programs. 2.2.3

Prince Edward Island

The Bedeque Bay Environmental Management Association started a PEI Plantwatch in 2000 with Ilana Kunelius promoting the project to students and volunteers. In 2002 Charmaine Noonan took Ilana Kunelius’ place as Plantwatch coordinator, promoting the tracking of 12 plant species. In 2003 a Plantwatch video as well as a PEI Plantwatch Guide were being produced. Three school classes and several members of the public were observers in 2002. The PEI Natural History Society gathers phenology data from members and publishes it annually in the Island Naturalistt newsletter. 2.2.4

Newfoundland and Labrador

Luise Hermanutz and Madonna Bishop of Memorial University started Newfoundland and Labrador Plantwatch in 1998. The number of plants observed has grown from five species in 1998 to 13 species in 2002. They produced an observer’s guide, a webpage (http://www.mun.ca/biology/plantwatch), and an annual newsletter for observers.


2.3

Central Canada

2.3.1

Quebec

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Dr. P. A. Dubé coordinated a large phenology network in the 1970s (see section 2.1.3). Intensive studies of tree phenology have been done by Dr. Martin Lechowicz and his students at McGill University (Hunter and Lechowicz 1992; Lechowicz 1995), and he continues to promote phenology as an essential method to monitor ecosystems for the effects of climate change (Lechowicz 2001). Since 2001 “Opération floraison” or Quebec Plantwatch has been based at the Montréal Botanical Garden, coordinated by botanist Stéphane Bailleul. Fifteen species of plants are tracked. Detailed observations of bloom times were made at the botanical garden in 20012002. Promotion to the public in Quebec will begin in 2003, once the French translation of the booklet “Plantwatch: Canada in Bloom” becomes available. 2.3.2

Ontario

Starting in 1932 dates for the Ottawa district of flowering and fruiting for weeds and native plants were gathered by the Division of Botany and Plant Pathology of the (federal) Department of Agriculture (Minshall 1947). Minshall provides a brief review of early Canadian phenology research, and notes that in 1939-1940 an interdepartmental federal committee presented recommendations to coordinate all federal projects in phenology. Unfortunately the subsequent war prevented action on these recommendations. Bassett et al. (1961) of the federal Department of Agriculture, analyzed this data for selected trees, shrubs, herbs and grasses for 1936-1960 and calculated the effective base temperatures for spring development of 10 early-blooming tree species. The Royal Botanical Garden in Hamilton gathered lilac data as part of the NE Network described in section 1.3 in the 1970s. This is the base for the Plantwatch program for Ontario that began in 2002 and now tracks 14 plant species. Carl Rothfels replaced initial coordinator Bruce Peart r in 2003. No promotional products have been produced as yet. In 1995 Don MacIver of the Headwaters Coalition (Grand River Valley Conservation Authority) launched a program called Green Wave Ontario. Observers tracked phenology of existing lilacs, honeysuckles, and wildflowers for a few years.

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2.4


Western Canada

Research on first bloom dates for 50 native plants was carried out by Agriculture Canada’s Laboratory of Plant Pathology in three prairie cities, Winnipeg, Saskatoon, and Edmonton, from 1936 to 1961. Wheat phenology (time of seeding, emergence, heading, maturity) was also recorded for comparison, and results of this intensive study were published annually (Russell 1962). Erskine (1985) presents data for first bloom of native plants and bird arrival for five boreal sites across Canada, at a different site for each year from 1971 to 1975. He also notes the appeal of phenology observations: “such visible events as the flowering of plants and the arrival of birds have an appeal that is lacking in the cold statistics of the meteorological record.” (p. 188). He lists many phenology references previously published in the Canadian Field Naturalist, commenting that most phenology studies at that time were done as extra studies, which were related to but were not the main task of field workers. 2.4.1

Manitoba

Criddle (1927) observed 400 prairie species over 20 years in southern Manitoba and published flowering and seed-ripening times valuable for present-day use in reclamation work. Mitchener (1948) presented data on flowering times and pollen availability from beekeepers. In 2001 Kim Monson became coordinator of Manitoba Plantwatch, which is cosponsored by the University of Winnipeg Geography Department and the Manitoba Naturalists’ Society. Sixteen plants are tracked and products include a promotional pamphlet, an observer guide, a teacher guide, and annual newsletters. Observers receive a certificate with space for an annual sticker to thank them for data submitted. 2.4.2

Saskatchewan

Budd and Campbell (1959) report first bloom dates for 145 prairie native plants recorded at Agriculture Canada’s Experimental Farm in Swift Current. They recommend using the bloom of Wood’s rose (Rosa woodsii) as the best indicator of “range readiness” (i.e., pasture plants can now withstand grazing). Saskatchewan Plantwatch began in 2001, coordinated by Kerry Hecker and affiliated with Nature Saskatchewan. Eleven plant species are tracked, and promotional articles have been produced.

Chapter 2.4: North America 2.4.3

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Alberta

Moss (1960) recorded "height of bloom" dates for 25 spring-blooming shrubs and trees near the University in Edmonton, Alberta from 1926 to1958. These flowering data were correlated with degree-days to determine the average amount of warmth the plants were exposed to before flowering. Dr. Charles Bird, Professor of Botany at the University of Calgary, established a volunteer network to record the flowering of native plants, and results were published annually in Alberta Naturalist, the journal of the Federation of Alberta Naturalists, from 1973-1982 (Bird 1974). This survey was revived and revised in 1987 (Beaubien 1991) as the Alberta Wildflower Survey, based at the University of Alberta. Between 150-200 volunteers per year reported dates of first (10%), mid (50%), and full (90%) flowering for 15 native plant species from 1987-2001. Training was provided using printed program information with tips on site selection, protocols, and species identification, including color photographs and sketches. These data have been used in preliminary determinations of growing degree-days required for flowering (Beaubien and Johnson 1994). In 2002 the program was renamed Alberta Plantwatch. Some later-blooming species were dropped and others added for a total of 21 species, and phenophase definitions were changed to match the updated national program. Newsletters have been sent out each fall and spring since 1987 by mail and more recently, also by email. The May Species Count is a “snapshot phenology” study, which has been coordinated by the Federation of Alberta Naturalists on the last weekend of May every year since 1976. It includes a count of wildlife including plants (species in bloom), birds, mammals, butterflies, etc. Numbers of plant species found in bloom indicate the relative earliness or lateness of the spring season. 2.4.4

British Columbia

The entomologist R. Glendenning (1943) summarized some methods, history and uses of phenology and recommended certain species as suitable across Canada. Based on his own observations over 34 years, he suggested phenological events to observe in each month of the year for the British Columbia coast. In 1984 Bill Merrilees of the Federation of British Columbia Naturalists launched a study of the flowering of vascular plants, requesting 16 phenophases for up to 50 native species of the observer's choice. In 2000 he modified the survey, requesting bloom times for a shorter list of plants found in southeastern Vancouver Island. In 2001 Dave Williams of the University College of the Cariboo in Kamloops took on the

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task of coordinating Plantwatch in British Columbia, tracking the phenology of 15 plant species.

2.5

Northern Canada

Erskine (1985) describes articles in northern phenology research published in the Canadian Field Naturalist. Climate warming is predicted to show the biggest effects in arctic regions. In 1990 the International Tundra Experiment (ITEX) began, linking arctic and alpine scientists to study the effects of climate change on northern ecosystems (Henry and Molau 1997). In 1999 the Canadian researchers in this group started CANTTEX, the Canadian Tundra and Taiga Experiment (http://www.emannorth.ca/canttex) to develop a strategy for studying climatic and ecological change in Canada’s north. Presently there are 13 research and monitoring sites which track phenology using ITEX protocols, and/or carry out experimental manipulations such as warming or fertilizing. The three northern territories, Yukon, Northwest Territories and Nunavut, all started Plantwatch programs in 2001. In the Yukon Lori Schroeder is coordinator through the Yukon Conservation Society, promoting tracking of 16 species. In the Northwest Territories Jen Morin coordinates through Ecology North, tracking 15 species. In Nunavut, Paula Hughson of Parks Canada is assisted by Guy d’Argencourt and Jamal Shirley of the Nunavut Research Institute in promoting the tracking of seven plant species (see http://pooka.nunanet.com/~research/plantwatch.htm). The coordinators from the three territories and northern Manitoba (Kim Monson) with assistance from E. Beaubien and Leslie Wakelyn of Environment Canada’s Ecological Monitoring and Assessment Network North (EMAN-North) applied as “Plantwatch North” and received funds from Environment Canada’s Northern Ecosystems Initiative in 2001 and 2002. As a result each region now has an observer’s guide, and use the “Plantwatch North” poster produced in 2002 (versions in English, French and Inuktitut), as well as recognition pins for observers. The funding also permitted several workshop meetings. In 2003 a full color booklet describing the Plantwatch North program was in preparation.

2.6

Conclusions

Canada enjoys a wealth of phenological studies, starting with early applications by First Nations and continued today by naturalists, gardeners, students and scientists. Environment Canada has now embraced phenology via its “NatureWatch” programs, to involve the public in finding out what is changing in the environment and why. Plantwatch has a bright future in


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engaging the public as “eyes of science”, tracking nature’s plant calendar and boosting awareness of the biotic response to climate change. Historically, many Canadians have enjoyed noting down the timing of seasonal events such as the appearance of wildflower blooms, spring birds, calling of frogs, and melt or freeze-up of lakes and rivers. If the reader is aware of records of such “closet phenologists”, or of other phenology studies in Canada not mentioned in this article, the author would be delighted to learn of these (see Beaubien’s address). These data are important as a baseline against which to compare current timing in our increasingly variable climate.

ACKNOWLEDGEMENTS United States section: Thanks to Glen Conner for information on Dr. Samuel D. Martin and other early phenological observers and networks. Canada section: Thanks to these regional coordinators for review of the text: S. Bailleul, M. Bishop, L. Hermanutz, C. Noonan, C. Rothfels, L. Shroeder, and L. Vasseur. L. Seale kindly edited the article. Thanks to EMANCO and the Canadian Nature Federation for their help in promoting the Plantwatch program. Dr. Geoffrey Holroyd, Canadian Wildlife Service, has financially supported much work in phenology.

REFERENCES CITED Bassett, I. J., R. M. Holmes, and K. H. MacKay, Phenology of several plant species at Ottawa, Ontario, and an examination of the influence of air temperatures, Can. J. Plant Sci., 41, 643-652, 1961. Beaubien, E. G., Phenology of vascular plant flowering in Edmonton and across Alberta, MSc. thesis, Dept. of Botany, University of Alberta, Edmonton, 1991. Beaubien, E. G., Plantwatch: Tracking the biotic effects of climate change using students and volunteers. Is spring arriving earlier on the prairies?, in Ecological Monitoring and Assessment Network Report on the 3rd National Science Meeting, pp. 66-68, Environment Canada, Saskatoon, January 1997. Beaubien, E. G., and H. J. Freeland, Spring phenology trends in Alberta, Canada: links to ocean temperature, Int. J. Biometeorol., 44, 53-59, 2000. Beaubien, E. G., and D. L. Johnson, Flowering plant phenology and weather in Alberta, Canada, Int. J. Biometeorol., 38, 23-27, 1994. Blair, R. J., J. E. Newman, and J. R. Fenwick, Phenology Gardens in Indiana, in Phenology and Seasonality Modeling, edited by H. Lieth, pp. 45-54, Springer-Verlag, New York, 1974. Bird, C. D., 1973 flowering dates, Alta. Nat., 4(1), 7-14, 1974.

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Budd, A. C., and J. B. Campbell, Flowering sequence of a local flora, J. Range Manage., 12, 127-132, 1959. Caprio, J. M., Phenology of lilac bloom in Montana, Science, 126, 1344-1345, 1957. Caprio, J. M., The Solar Thermal Unit Concept in Problems Related to Plant Development and Potential Evapotranspiration, in Phenology and Seasonality Modeling, edited by H. Lieth, pp. 353-364, Springer-Verlag, New York, 1974. Castonguay, Y., and P. A. Dubé, Climatic analysis of a phenological zonation: a mutivariate approach, Agric. and Forest Met., 35, 31-45, 1985. Cayan, D. R., S. A. Kammerdiener, M. D. Dettinger, J. M. Caprio, and D. H. Peterson, Changes in the Onset of Spring in the Western United States, Bull. Amer. Met. Soc., 82, 399-415, 2001. Criddle, N., A calendar of flowers, Can. Field Nat., 41, 48-55, 1927. Dubé, P. A., and J. E Chevrette, Phenology applied to bioclimatic zonation in Québec, in Phenology: an aid to agricultural technology, Vt. Agric. Exper. Sta. Bull., 684, edited by R.J. Hopp, pp. 33-43, Vermont Agricultural Experiment Station, Burlington, 1978. Erskine, A. J., Some phenological observations across Canada's boreal regions, Can. Field Nat., 99(2), 185-195, 1985. Flint, H. L., Phenology and Genecology of Woody Plants, in Phenology and Seasonality Modeling, edited by H. Lieth, pp. 83-97, Springer-Verlag, New York, 1974. Glendenning, R., Phenology, the most natural of sciences, Can. Field Nat., 57, 75-78, 1943. Henry, G. H. R., and U. Molau, Tundra plants and climate change: The International Tundra Experiment (ITEX), Global Change Biol., 3(Suppl. 1), 1-9, 1997. Hopkins, A. D., Bioclimatics–A science of life and climate relations, U.S. Dept. Agr. Misc. Publ. 280, 1938. Hopp, R. J., Plant Phenology Observation Networks, in Phenology and Seasonality Modeling, edited by H. Lieth, pp. 25-43, Springer-Verlag, New York, 1974. Hopp, R. J., ed., Phenology: an aid to agricultural technology, Vt. Agric. Exper. Sta. Bull., 684, Vermont Agricultural Experiment Station, Burlington, 51 pp., 1978. Hough, F. B., Observations upon periodical phenomena in plants and animals from 1851 to 1859, with tables of the dates of opening and closing of lakes, rivers, harbors, etc., in Results of Meteorological Observations, Made Under the Direction of the United States Patent Office and the Smithsonian Institution, from the year 1854 to 1859, inclusive, Rept. of the Commissioner of Patents, Vol. 2, Part 1, Exec. Doc. 55, 36th Congress, 1st Session, U.S. Government Printing Office, Washington, 1864. Hunter, A. F., and M.J. Lechowicz, Predicting the timing of budburst in temperate trees, J. Appl. Ecol., 29, 597-604, 1992. Johnston, A., Plants and the Blackfoot, Occas. Paper No. 15, Lethbridge Historical Society, Historical Society of Alberta, Lethbridge, 1987. Lantz, T. C., and N. J. Turner, Traditional phenological knowledge (TPK) of aboriginal peoples in British Columbia, Jour. of Ethnobiol., (in press), 2003. Lechowicz, M. J., Seasonality of flowering and fruiting in temperate forest trees, Can. J. Bot., 73, 175-182, 1995. Lechowicz, M. J., Phenology, in Encyclopedia of Global Environmental Change, vol. 2, Biological and ecological dimensions of global environmental change, edited by J. G. Canadell, pp. 461-465, Wiley, London, 2001. MacKay, A. H., Phenological observations in Canada, Can. Record of Sci., 8(2), 71-84, 1899. MacKay, A. H., The phenology of Nova Scotia, 1923, Trans. Nova Scotia Inst. Sci., 16(Pt. 2), 104-113, 1927.


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Martin, S. D., Register of Meteorological Observations, Pine Grove, Kentucky, Smithsonian Institution, Washington, April 1865. Minshall, W. H., First dates of anthesis for four trees at Ottawa, Ontario, for the period of 1936 to 1945, Can. Field Nat., 61, 56-59, 1947. Mitchener, A.V., Nectar & pollen producing plants of Manitoba, Sci. Agric., 28, 475-480, 1948. Moss, E. H., Spring phenological records at Edmonton, Alberta, Can. Field Nat., 74, 13-118, 1960. Parry, D., W. J. A. Volney, and C. R. Currie, The relationship between trembling aspen phenology and larval development of the large aspen tortrix, Information report NOR-X30, Canadian Forest Service, Natural Resources Canada, Edmonton, 1997. Proceedings, Proc. and Trans. of the Royal Soc. of Canada, 10 (Session 3), 53-55, 1893. Reader, R., J. S. Radford, and H. L. Lieth, Modeling Important Phytophenological Events in Eastern North America, in Phenology and Seasonality Modeling, edited by H. Lieth, pp. 329-342, Springer-Verlag, New York, 1974. Russell, R. C., Phenological records of the prairie flora, Can. Plant Disease Survey, 42(3), 162-166, 1962. Schwartz, M. D., The Advance of Phenological Spring Across Eastern and Central North America, Ph.D. dissertation, Dept. of Geography, University of Kansas, Lawrence, 1985. Schwartz, M. D., Phenology and Springtime Surface Layer Change, Mon. Wea. Review, 120(11), 2570-2578, 1992. Schwartz, M. D., Monitoring global change with phenology: the case of the spring green wave, Int. J. Biometeorol., 38, 18-22, 1994. Schwartz, M. D., Green-wave phenology, Nature, 394(6696), 839-840, 1998. Schwartz, M. D., and T. M. Crawford, Detecting Energy-Balance Modifications at the Onset of Spring, Phys. Geography, 21(5), 394-409, 2001. Schwartz, M. D., and B. E. Reiter, Changes in North American Spring, Int. J. Climatology, 20(8), 929-932, 2000. Schwartz, M. D., G. J. Carbone, G. L. Reighard, and W. R. Okie, Models to Predict Peach Phenology from Meteorological Variables, HortScience, 32(2), 213-216, 1997. Smith, J. W., Phenological dates and meteorological data recorded by Thomas Mikesell between 1873 and 1912 at Wauseon, Ohio, Mon. Wea. Review Suppl., 2, 23-93, 1915. Vasseur, L., R. L. Guscott, and P. J. Mudie, Monitoring of spring flower phenology in Nova Scotia: comparison over the last century, Northeast. Nat., 8(4), 393-402, 2001. Vittum, M. T., and R. J. Hopp, The N.E.- 95 lilac phenology network, in Phenology, an aid to agricultural technology, Vt. Agric. Exper. Sta. Bull., 684, edited by R.J. Hopp, pp. 1-5, Vermont Agricultural Station, Burlington, 1978. Weather Bureau, Instructions for Voluntary Observers, U. S. Department of Agriculture, Washington, 1899. Zhao, T., and M. D. Schwartz, Examining the Onset of Spring in Wisconsin, Clim. Res., 24(1), 59-70, 2003.

Chapter 2.5 SOUTH AMERICA L. Patrícia C. Morellato Departamento de Botânica, Plant Phenology and Seed Dispersal Research Group, Universidade Estadual Paulista, São Paulo, Brasil

Key words:

1.

Phenological patterns, Flowering, Fruiting, Tropical, Climate zones

INTRODUCTION

Comprising about one eighth of the earth’s land surface, the South American continent is situated between 12°N-55°S latitude and 80°-35°W longitude. It covers an area of about 17,500,000 km2 divided between 13 countries. Eighty percent of its land is within the tropical zone, yet it extends into the subantarctic (Davis et al. 1997). Essentially, all life zones and vegetation formations are represented. The principal vegetation types are tropical evergreen and semi-evergreen moist forest, dry forest to woodland (cerrado or woody savanna), open grassy savanna, desert and arid steppe, Mediterranean-climate communities, temperate evergreen forest, and several montane formations (e.g. páramo, stone fields or campos rupestres, puna). The large array of vegetation types comprises some of the most diverse in the world. This includes the upper Amazon forest and Atlantic forest, as well as vegetation types with great concentrations of local endemism, the Andean montane forests and the Mediterranean-climate region of central Chile (Davis et al. 1997). At least 46 sites distributed over eight large regions have been recognized as centers of plant diversity (Davis et al. 1997), and several are considered biodiversity hotspots for conservation priorities (Myers et al. 2000).

Schwartz (ed.), PHENOLOGY: AN INTEGRATIVE ENVIRONMENTAL SCIENCE, 75-92 © 2003 Kluwer Academic Publishers. Printed in the Netherlands.

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All this diversity of species and vegetation types has not been completely studied in respect to its floristic diversity. Consequently, just a small percentage of its species and vegetation has been examined from the point of view of their seasonal changes. Phenological studies are uncommon, although the number of papers a published has increased over the last 20 years. However, long-term phenological data are rare and just a few longterm monitoring systems are known. I searched the major electronic databases (Web of Science, Current Contents, Scielo, Biological Abstracts), for phenological studies of South American native species or vegetation. Phenological data from studies on agricultural or introduced species or those from studies on herbivory, pollination, frugivory and seed dispersal were excluded when the main focus of the paper was the examination of animal feeding behavior. I also searched, using mainly some electronic and internet search tools and the database of South American main research agencies and institutions, for groups, universities, institutions or researchers doing phenological work. Finally, I looked for historical phenological data. However, this information was not easily found in the databases searched. The information is biased towards Brazil for two reasons. First, my 15 years of phenological research in Brazil, and second, the Brazilian Federal Agency for Science CNPq (National Counsel for Scientific and Technological Research) maintains a very well organized database of all active researchers and research groups in Brazil (http://www.cnpq.br). The main goal of this chapter is provide an overview of phenological work carried out on South American vegetation. I describe the phenological patterns of the main vegetation types studied up to the present, and point out areas where there is a lack of phenological information. To make descriptions more comparable, the overview is based largely on community studies that include information on flowering and fruiting patterns. I have tried to map the actual ongoing research and research groups and discuss the actual data collection to explore the future of phenological research on South America. As far as I am aware the phenology of South American vegetation has not been compared and analyzed from this perspective.

2.

BRIEF HISTORY OF PHENOLOGICAL DATA COLLECTION IN SOUTH AMERICA

The oldest phenological information surveyed was a description of the annual cycle of plants and animals in two Atlantic forests at Rio de Janeiro, Southeast Brazil (Davis 1945). Otherwise, the phenological data found, out of the electronic databases surveyed, were information included in

Chapter 2.5: South America

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comprehensive papers describing the plant community (Veloso 1945; Andrade 1967), or just phenological notes, where the authors recorded the dates of flowering or fruiting for several tropical species from a particular site or botanical garden (Silveira 1935; Lima 1957; Santos 1979). Alvin (1964) was one of the first researchers to describe and analyze the phenology of native tropical forest trees from Bahia, Brazil (Alvin 1964; Alvim and Alvim 1976), although most of his work focused on the flowering of coffee and cocoa trees. The work of Araujo (1970) on the phenology of 36 species of Amazon lowland forest trees marks the beginning of the contemporary studies on phenology on South America. This paper is especially important because it represents the primary report of the first and oldest as well as possibly unique long-term phenological data collection for South America tropical forest trees. The INPA (Instituto Nacional de Pesquisas da Amazônia) phenological work started in 1965, at Reserva Florestal Ducke (Manaus, Amazonas State, Brazil). Trees were systematically selected with up to a total number of 300 trees (three per species) marked over an area of 140.5 hectares of native Amazon lowland tropical forest. In 1970 the sample size was extended to 500 trees (five per species), which are still monitored today. In 1974, INPA researchers replicated the phenology study. They marked 500 trees of another 100 species from an Amazon lowland forest at Estação Experimental de Silvicultura Tropical, about 30 km from Reserva Florestal Ducke. Both studies performed monthly observations for changes on reproductive and vegetative phenology of 10 defined phenophases (Araújo 1970; Alencar et al. 1979). A similar program of phenological data collection was established by Companhia Vale do Rio Doce (CVRD) at Reserva Natural de Linhares (Northeast Espírito Santo State, Brazil), a lowland evergreen forest reserve locally known as “Tabuleiro forest.” They employed the same methodology proposed by Araújo (1970), selecting 41 species and marking 205 trees (five per species). The project started in 1982 and seems to be active up to the present. Another interesting South American long-term database, although not active, is the one analyzed by Ter Steege and Persaud (1991). The authors compiled data on the flowering and fruiting of Guyanese forest trees collected over about 100 nonconsecutive years. I did not find any other long-term data set or project undertaking systematic phenological observations on South American vegetation. All information obtained refers to the collection of phenological data during a defined time span, usually between one to three years. Several Institutions and Universities conducting agronomic-related research have phenology programs for crops and some economically valuable species. For example, in Argentina, many of the National Universities have a discipline on

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climatology and agricultural phenology, and several plant species are investigated for phenological changes. Brazilian research institutions such as INPA, EMBRABA (Empresa Brasileira de Agropecuária) and IAC (Instituto Agronomico de Campinas) perform phenological observation of crop plants and native or exotic fruit trees. However, it was not possible to define the type of phenological data collected or their duration, and if some could be a long-term data set. Finally, I was unable to find any kind of phenology network, besides the GLOBE educational project, involving nine South American countries (for more information, see http://www.globe.gov). Therefore, there is a need for long-term phenological studies in South America. After Araujo’s (1970) work, just a few more papers were published in the 1970s (eight), even though the number increased during the 1980s (15 papers). The great production of phenological information for South American vegetation was in the 1990s (1990-1999), with at least 70 papers in the electronic databases surveyed. The papers are not evenly distributed over the 13 South American countries. Almost half of the production are from Brazil (30), followed by Venezuela (12) and Chile (12), and with some papers from Argentina (seven), Colombia (five), French Guyana (two) and Guyana (one). The number of published papers stays elevated from the year 2000 until the present, with about 36 papers surveyed in just three years, 22 of those from Brazil. Surprisingly, there are no recent papers from Chile, and Bolivia has two papers. Therefore, there is an increasing trend in publication of phenology studies in South America. If we considered other sources of information (books, journals not indexed, etc), the number of papers would be much higher (about twice) but the countries producing papers are nearly the same. A complete list of all papers surveyed can be obtained from the author.

2.1

Actual state of phenological research

Among the more than 150 papers researched, approximately half of them are phenology studies at the community level, describing the phenological patterns of several species belonging to one or different life-forms, from a defined geographic region and vegetation type. These papers are a good source of information for a large number of native species from different South American vegetation (Table 1). The other papers are studies focused on one or few species, or on a group of species belonging to the same plant family. The tendency is the same if just the papers produced recently, from year 2000 to date, are analyzed, with almost half focused on community studies. However, some of these recent studies start to address climatic


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changes, relating satellite observation, “El Niño” effects and CO2 assimilation to plant phenology (Asner et al. 2000; Parolin 2000). Specifically for Brazil, I was able to locate at least 40 universities or institutions carrying out phenological research on almost every type of native vegetation across the country, from the Amazon forest around the equator to the Araucaria forest and subtropical vegetation of South Brazil. Some vegetation types have been the focus of researchers, such as the Amazon lowland forest or terra-firme forest, Atlantic forest, semideciduous forest and cerrado. However, in the last five years I found papers and ongoing projects focused on seasonal changes of plant species from caatinga, gallery forest, swamp forest, Amazon-inundated and seasonallyinundated forest, coastal plain vegetation and dunes, among others. Another interesting point is that almost any paper, project or ongoing research is concerned with the effects of climatic change and its evaluation using plant phenology.

3.

OVERVIEW OF PHENOLOGICAL PATTERNS FOR SOUTH AMERICAN VEGETATION

Summarizing the phenology of South American vegetation is difficult, due to the diversity of vegetation and species. To see how the phenological information is distributed over the different vegetation and to compare the phenological patterns observed, the land vegetation of South America was subdivided into six large vegetation groups (Table 1), plus the more complex montane formations occurring along the Andean cordillera, the Tepuis and in the coastal cordillera of Brazil (Davis et al. 1997). I only considered community studies including information on flowering and fruiting patterns, preferably for a large number of species. Studies that focused on just one plant family were excluded. Patterns are described based on the number of species flowering and fruiting per month unless otherwise noted. I. Tropical moist forest - In spite of the more or less non-seasonal climate and being an evergreen or semi-evergreen (semideciduous) forest, a marked seasonal pattern of flowering was observed for the majority of moist forests surveyed (Table 2). Amazon lowland evergreen forest species tend to flower during the dry season (Araújo 1970; Alencar et al. 1979; Sabatier 1985; Ter Steege and Persaud 1991; Peres 1994a; Wallace and Painter 2002, Figure 1). The same pattern is observed for Amazon “Campina” forest (Alencar 1990). Most species of semideciduous forest are flowering by the end of the dry season and beginning of wet season (Morellato et al. 1989; Stranghetti and Ranga 1997; Mikich and Silva 2001, Figure 1); Venezuelan semideciduous

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forest have species flowering in both seasons (Monasterio and Sarmiento 1976), the same is observed for climbers from Brazilian semideciduous Table 2.5-1. Number of published phenology studies at community level in the six large lowland vegetation groups of South America (adapted from Davis et al. 1997), plus montane formations. Vegetation group Plant formations Number of papers included I. Tropical moist forest Amazon Forest, 20 (evergreen or Brazilian Atlantic semi-evergreen Rain Forest, rain forest) Semideciduous forest, Gallery Forest and Swamp forest, Premontane/montane Pacific rain forest, Chocó and lower Magdalena Valley 9 II. Dry forest Chaco, Cerrado, (integrating into Caatinga, Woody woodland) Savanna Northern Colombia and Venezuela, coastal Equator and Peru, and the Deciduous (dry) forests III. Open grassy savanna Pampas region, the 2 Llanos, Cerrado grassland, Pantanal and Gran Sabana and Sipaliwini savanna in the Guyana region IV. Desert and arid step Sechura and 4 Atacama regions along west coast and in the Monte and Patagonian Steppes in the Southern Cone of South America V. MediterraneanCentral Chile 1 climate region


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Vegetation group

Plant formations included

Number of papers

VI.

Temperate evergreen forest

Chile and Argentina

1

VII.

Montane formations

Complex montane formations along the Andean Cordillera, the Tepuis, and in the coastal cordillera of Brazil

5

forest (Morellato and Leitao 1996). Brazilian evergreen Atlantic rain forest and montane forest trees flower mainly in the wet season (Davis 1945; Morellato et al. 2000; Talora and Morellato 2000). Gallery forest shows a flowering pattern similar to Atlantic forest, flower peak occurring in the wet season (Funch et al. 2002). Two papers addressing swampy forest phenology were surveyed (Ramirez and Brito 1987; Spina et al. 2001). The swamp forest show flowering patterns similar to those observed for semideciduous forests (Spina et al. 2001). The Bolivian Sartanejal forest, a vegetation type influenced by forest streams, has a flower peak in the dry season (Wallace and Painter 2002). Fruiting patterns were more variable than flowering patterns across forest types and locations (Table 2, Figure 1). Some Amazon forests show seasonal fruiting patterns, peaking during the wet season (Alencarr et al. 1979; Sabatier 1985; Peres 1994a), while other present a bimodal pattern, with both peaks occurring in the dry season (Ter Steege and Persaud 1991). For Colombian lowland forests and Campina forest fruiting is non-seasonal (Alencar 1990; Wallace and Painter 2002). The fruiting patterns for semideciduous forests are not as seasonal as the flowering patterns, even though most species bear ripe fruits in the dry season or in the transition from dry to wet season (Morellato et al. 1989; Stranghetti and Ranga 1997; Mikich and Silva 2001). Fruiting is not seasonal for most of the Atlantic forest (Morellato et al. 2000), but a seasonal pattern is observed for Coastal Plain forest and montane forest, peaking in the less wet season (Davis 1945; Morellato et al. 2000; Talora and Morellato 2000). Gallery and Sartanejal forest present a fruiting peak in the wet season (Funch et al. 2002; Wallace and Painter 2002), and swamp forest fruiting was nearly non-seasonal (Spina et al. 2001). For the only Amazon floodplain forest surveyed the peak of flowering and fruiting occurs during the aquatic (flooded) phase (Schongart et al. 2002). Finally, Colombian Premontane rain forest presents a relatively constant number of species in flower or fruit through the year (Hilty 1980).

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Figure 2.5-1. Flowering (black line) and fruiting (gray line) patterns of Brazilian forest types: Amazon (AM, n = 36 species), data source Araujo (1970); Semideciduous (SD, n = 103), data source Morellato (1995); and Atlantic (AT, n = 214), data source Morellato et al. (2000). The dry season period is shown in gray.


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II. Dry forest (integrating into woodland) – Savanna-forest mosaic on the Venezuelan Central Plain shows a marked seasonality of flower and fruit production for all habitats except forest (Table 2, Ramirez 2002). Flowering peaked during the rainy season, and fruiting peaked toward the end of the rainy season (Ramirez 2002). Woody savannas or cerrado vegetation comprises trees, shrubs and herbs. It includes at least two structural vegetation types: cerrado sensu stricto or woody savanna, an open landscape dominated by shrubs and trees at different densities, and Cerradão, a welldeveloped forest form of cerrado with canopy trees up to 20m tall (Ribeiro and Tabarelli 2002). Generally, the woody flora of cerrado present a seasonal phenology, although flowering and fruiting are not restricted to any particular season (Figure 2). Flowering is clearly associated with the end of the dry season and beginning of the rainy season (Monasterio and Sarmiento 1976; Batalha and Mantovani 2000; Oliveira and Gibbs 2000; Silberbauer-Gottsberger 2001; Ribeiro and Tabarelli 2002; Wallace and Painter 2002). Fruiting is more widespread over the year (Oliveira and Gibbs 2000), however, in some studies a middle-to-late rainy or dry season fruit peak is detected (Batalha and Mantovani 2000; Ribeiro and Tabarelli 2002; Wallace and Painter 2002). Herbaceous plants show a different pattern, flowering peak occurring at the end of the rainy season and fruiting peak in the dry season (Batalha and Mantovani 2000). Flowering peak in the Bolivian dry forest occurs at the transition between the dry and the rainy seasons. There is a major peak of fruiting in the dry season and a minor one during the rainy season (Justiniano and Fredericksen 2000). Caatinga, a deciduous tree-shrub vegetation from Northeastern Brazil, has a low rainfall climate, which is very seasonal and variable between years (Machado et al. 1997). Reproductive events are concentrated in the rainy season. The flowering peak occurs early and the fruiting peak late in the rainy period (Machado et al. 1997). Table 2.5-2. Main phenological patterns and peak season for South American vegetation. Patterns are ranked as seasonal or non-seasonal. The time of flowering and fruiting peak is indicated as dry season and wet season for tropical climates, and as spring, fall, winter or summer for temperate climates. Main phenological pattern Vegetation Type*

Group*

Flowering Pattern/peak season

Amazon lowland forest

I

Seasonal/dry

Amazon floodplain forest

I

Seasonal/flooding

Fruiting Pattern/peak season Seasonal to nonseasonal Seasonal/flooding

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Phenology: An Integrative Environmental Science Main phenological pattern Vegetation Type*

Semideciduous forest Atlantic rain forest Gallery forest Swamp forest Sartanejal forest Pre-montane Rain forest Savanna-forest mosaic Cerrado (woody flora)

Group*

Flowering Pattern/peak season

I

Seasonal/dry-to-wet

I I I I I II II

Seasonal/wet Seasonal/wet Seasonal/dry-to-wet Seasonal/dry Non-seasonal Seasonal/wet Seasonal/dry-to-wet

Fruiting Pattern/peak season Seasonal/Dry or dryto-wet Non-seasonal Seasonal/wet Non-seasonal Seasonal/wet Non-seasonal Seasonal/wet Seasonal to nonseasonal Seasonal/dry Seasonal/rain Seasonal/dry Seasonal/after rain Seasonal/after rain

Dry forest II Seasonal/dry-to-wet Caatinga II Seasonal/rain III Seasonal/rain Campo cerrado Desert IV Seasonal/after rain Mediterranean-climate V Seasonal/after rain region Temperate Valdivian rain VI Seasonal/early summer Seasonal/late summer forest (dry) Chile Andean Zone (2000VII Seasonal/summer Seasonal/late 3600m altitude) summer-to-fall Montane grassland VII Seasonal/summer Seasonal/summer Pre-montane sub-tropical VII Seasonal/dry Seasonal/wet forest * See Table 1 and text for more detailed description of vegetation and source data.

III. Open grassy savanna – Few studies describe the phenology of open savanna. Dominant perennial grasses from Brazilian campo cerrado (open savanna) show a flower peak during the rainy season and fruit peak in the dry season (De Almeida 1995). A similar pattern is described for the Venezuelan Central Plain with fruiting more widespread over the year (Ramirez 2002). IV. Desert and arid step – Phenology studies were undertaken in four different places: arid Patagonia (Bertiller et al. 1991) and Monte Phytogeographical Province (Giorgetti et al. 2000) in Argentina, and the Chilean Coastal Desert and Southern Atacama Desert in Chile (Squeo et al. 1988; Vidiella et al. 1999). Phenology is highly constrained by rainfall, which determines the onset of reproduction for most of the species.


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V. Mediterranean-climate region – The phenology of shrub species from the coastal desert in North-Central Chile indicates the existence of at least two groups of species, with phenological patterns more or less dependent on precipitation (Olivares and Squeo 1999).

Figure 2.5-2. Flowering (black line) and fruiting (gray line) phenology of woody flora in a Central Brazil cerrado community (n = 54 species), data source Oliveira and Gibbs (2000). The dry season period is shown in gray.

VI. Temperate evergreen forest – The timing of reproductive events and their ecological and climatic constraints in a Valdivian rain forest of Chiloé, Chile, one of the most widespread and species-rich forest types in austral South America, is discussed by Smith-Ramirez and Armesto (1994). Peak flowering for most species occurs in the dry season (late spring to early summer, Figure 3). Ripe fruits are available all year round, but the number of species is lowest in early spring with the maximum in late summer (Smith-Ramirez and Armesto 1994). VII. Montane formations – Includes a wide range of austral vegetation types, from distinct vegetation belts in the Andean zone to pre-montane subtropical forest. Phenological changes in flowering and fruiting of distinct vegetation belts in the Chile Andean zone (Andean scrub, cushion communities and fell-fiel) ranging from 2000 to 3600 m, have been described (Arroyo et al. 1979; Arroyo et al. 1981; Riveros 1983). The growing season lasts five to eight months, peak flowering coinciding with the period of maximum temperature at lower altitudes and after this period at higher altitudes, while fruiting peak takes place in the late summer and fall (Figure 4, Arroyo et al. 1981). Pre-montane subtropical forests in Argentina have a seasonal reproductive phenology (Malizia 2001). Flowers

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are present throughout the dry season and the number of species with ripe fruits peaks during the wet season (Malizia 2001). In Argentina montane grassland flowering and fruiting are concentrated in a short period during the summer (Diaz et al. 1994).

Figure 2.5-3. Percent of species (trees, shrubs, and miscellaneous - epiphytes, vines, and hemi parasites) flowering (black line) and fruiting (gray line) in the temperate rain forest of Chiloé, Chile, data source Smith-Ramírez and Armesto (1994). Summer is shown in gray.

Figure 2.5-4. Percent of species flowering (black lines) and fruiting (gray lines) at Andean scrub (AS), and Cushion communities (CC) sites (altitudinal Andean vegetation), data source Arroyo et al. (1981). Summer is shown in gray.

Additional studies - One paper from the Caribbean region describes flowering and fruiting phenology in tropical semi-arid vegetation of Northeastern Venezuela (Delampe et al. 1992). Venezuelan thorn woodland and thorn scrub desert formation show seasonality in their flowering and fruiting phenology (Delampe et al. 1992). Flowering activity is concentrated in the rainy season. Mature fruit index peaks in the dry season for trees and


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tall shrubs, and is concentrated in the wet season for low shrubs and herbs (Delampe et al. 1992). Phenological patterns of Brazilian coastal dune vegetation were described by Cordazzo and Seeliger (1988). Most species of Southern Brazil coastal dune vegetation, under a warm temperate climate, flower during spring, summer and fall, while fruiting is concentrated in fall and winter (Cordazzo and Seeliger 1988).

4.

FUTURE DEVELOPMENTS AND CONCLUDING REMARKS

The distribution of phenological studies on South American vegetation is very uneven over the different vegetation types and life forms. Tropical forest is by far the better studied ecosystem and the tree is the life-form observed in almost all papers surveyed. By contrast a single study surveyed temperate forest (Smith-Ramirez and Armesto 1994). Studies focused on climbers, epiphytes and specially understory herbs are uncommon (Seres and Ramirez 1993; Putz et al. 1995; Morellato and Leitao 1996), although some studies include different life forms besides trees (Peres 1994a). If studies concentrated on just one phenophase, (those not included in Table 1) are considered, the number of papers on tropical forests is even higher. Several papers focused on fruiting patterns (Zhang and Wang 1995; Stevenson et al. 1998; Develey and Peres 2000; Grombone-Guaratini and Rodrigues 2002), and some on leafing behavior (Jackson 1978; Loubry 1994) or flowering (van Dulmen 2001). A number of studies on tropical and temperate forests are focused on just one family (Sist 1989; Peres 1994b; Riveros et al. 1995; Smith-Ramirez et al. 1998; Listabarth 1999; Henderson et al. 2000; Ruiz et al. 2000). Dry forests, savannas and cerrados are the second most studied vegetation group. Most of the studies were developed in savannas, and again the phenology of woody lifeforms dominates, but more studies include other lifeforms if compared to tropical forests. Very few studies were undertaken on open savannas, deserts, Mediterranean-climate region, and montane formations. Although a number of studies focused on one phenophase (Rozzi et al. 1989), or one or few species were surveyed (Silva and Ataroff 1985; Rusch 1993; Fedorenko et al. 1996; Löewe et al. 1996; Jaramillo and Cavelier 1998; Velez et al. 1998; Rosello and Belmonte 1999; Rossi et al. 1999; Damascos and Prado 2001). Therefore, there is a need for phenological studies on South America’s vegetation. The condition is quite critical if we consider that some vegetation types or regions have a high species diversity and an elevated number of endemic species. For example, the Mediterranean climatic region and Andean montane forest are basically unknown with respect to their seasonal

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patterns. Community studies should be undertaken, making it possible to understand the seasonal changes in those vegetation types. For the betterstudied tropical forests, investigations exploring different lifeforms are necessary. Long-term phenological observations are required in order to better comprehend the effects of climatic changes on plant phenology. Finally, there is a growing number of scientists interested in plant phenology. Building some phenology networks is the great challenge for South American phenologists, demanding an effort from and cooperation among universities, research institutions, governmental, and nongovernmental agencies.

ACKNOWLEDGMENTS I am grateful to Eliana Gressler for help in many ways during the literature and data survey, and V. B. Zipparro and A. Mantovani for assistance with the figures and literature. The author was supported by a research grant from FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo; # 95/09626-6), and received a research fellowship from the Brazilian Research Council (CNPq). The manuscript was improved by suggestions from E. Beaubien, M.R. Keatley, and M. A. Pizo.

REFERENCES CITED Alencar, J. d. C., Interpretação fenológica de espécies lenhosas de campina na Reserva Biológica de Campina do Inpa ao norte de Manaus, Acta Amazonica, 20, 145-183, 1990. Alencar, J. d. C., R. A. Almeida, and N. P. Fernandes, Fenologia de espécies arbóreas em floresta tropical úmida de terra-firme na Amazônia Central, Acta Amazonica, 9, 163-198, 1979. Alvim, P. T., and R. Alvim, Relation of climate to growth periodicity in tropical trees. in Tropical trees as living sistems, edited by Zimmermann, M. H., pp. 445-464, Cambridge University Press-London, 1976. Alvin, P. T., Periodicidade do crescimento das árvores em climas tropicais, Anais do XV Congresso da Sociedade Botânica do Brasil, 405-422, 1964. Andrade, M. A. B., Contribuição ao conhecimento da ecologia de plantas do litoral do estado de São Paulo, Boletim da Faculdade de Filosfia, Ciencias e Letras - Botânica, 22, 1-169, 1967. Araújo, V. C. d., Fenologia de essências florestais amazônicas I, Boletim do INPA - Série Pesquisas florestais, 1-25, 1970. Arroyo, M. T. K., J. Armesto, C. Villagran, and P. Uslar, High Andean Plant Phenology in Central Chile, Archivos De Biologia Y Medicina Experimentales, 12, 497-497, 1979. Arroyo, M. T. K., J. J. Armesto, and C. Villagran, Plant Phenological Patterns in the High Andean Cordillera of Central Chile, J. Ecol., 69, 205-223, 1981.


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Asner, G. P., A. R. Townsend, and B. H. Braswell, Satellite observation of El Niño effects on Amazon forest phenology and productivity, Geophys. Res. Lett., 27, 981-984, 2000. Batalha, M. A., and W. Mantovani, Reproductive phenological patterns of cerrado plant species at the Pe-de-Gigante reserve (Santa Rita do Passa Quatro, SP, Brazil): A comparison between the herbaceous and woody floras, Revista Brasil. Biol., 60, 129-145, 2000. Bertiller, M. B., A. M. Beeskow, and F. Coronato, Seasonal Environmental Variation and Plant Phenology in Arid Patagonia (Argentina), J. Arid. Environ., 21, 1-11, 1991. Cordazzo, C. V., and U. Seeliger, Phenological and Biogeographical Aspects of Coastal Dune Plant Communities in Southern Brazil, Vegetatio, 75, 169-173, 1988. Damascos, M. A., and C. Prado, Leaf phenology and its associated traits in the wintergreen species Aristotelia chilensis (Mol.) Stuntz (Elaeocarpaceae), Rev. Chil. Hist. Nat., 74, 805815, 2001. Davis, D. E., The Annual Cycle of Plants, Mosquitoes, Birds, and Mammals in 2 Brazilian Forests, Ecol. Monogr., 15, 243-295, 1945. Davis, S. D., V. H. Heywood, O. Herrera-MacBride, J. Villa-Lobos, and A. C. Hamilton, Centres of Plant Diversity: a guide and strategy for their conservation, vol. 3, The Americas, IUCN Publications Unit, Cambridge, 562 pp., 1997. De Almeida, S. P., Phenological groups of perennial grass community on “campo-cerrado” area in the Federal District of Brazil, Pesqui. Agropecu. Bras., 30, 1067-1073, 1995. Delampe, M. G., Y. Bergeron, R. McNeil, and A. Leduc, Seasonal Flowering and Fruiting Patterns in Tropical Semiarid Vegetation of Northeastern Venezuela, Biotropica, 24, 6476, 1992. Develey, P. F., and C. A. Peres, Resource seasonality and the structure of mixed species bird flocks in a coastal Atlantic forest of southeastern Brazil, J. Trop. Ecol., 16, 33-53, 2000. Diaz, S., A. Acosta, and M. Cabido, Grazing and the Phenology of Flowering and Fruiting in a Montane Grassland in Argentina - a Niche Approach, Oikos, 70, 287-295, 1994. Fedorenko, D. E. F., O. A. Fernandez, C. A. Busso, and I. E. Elia, Phenology of Medicago minima and Erodium cicutarium in semiarid Argentina, J. Arid. Environ., 33, 409-416, 1996. Funch, L. S., R. Funch, and G. M. Barroso, Phenology of gallery and montane forest in the Chapada Diamantina, Bahia, Brazil, Biotropica, 34, 40-50, 2002. Giorgetti, H. D., Z. Manuel, O. A. Montenegro, G. D. Rodriguez, and C. A. Busso, Phenology of some herbaceous and woody species in central, semiarid Argentina, Phyton-Int. J. Exp. Bot., 69, 91-108, 2000. Grombone-Guaratini, M. T., and R. R. Rodrigues, Seed bank and seed rain in a seasonal semi-deciduous forest in south-eastern Brazil, J. Trop. Ecol., 18, 759-774, 2002. Henderson, A., B. Fischer, A. Scariot, M. A. W. Pacheco, and R. Pardini, Flowering phenology of a palm community in a central Amazon forest, Brittonia, 52, 149-159, 2000. Hilty, S. L., Flowering and Fruiting Periodicity in a Premontane Rain-Forest in Pacific Colombia, Biotropica, 12, 292-306, 1980. Jackson, J. F., Seasonality of Flowering and Leaf-Fall in a Brazilian Sub-Tropical Lower Montane Moist Forest, Biotropica, 10, 38-42, 1978. Jaramillo, M. A., and J. Cavelier, Fenologia de dos especies de Tillandsia (Bromeliaceae) en un bosque montano alto de la Cordillera Oriental Colombiana, Selbyana, 19, 44-51, 1998. Justiniano, M. J., and T. S. Fredericksen, Phenology of tree species in Bolivian dry forests, Biotropica, 32, 276-281, 2000. Lima, D. A., Notas para fenologia da zona da Mata de Pernambuco, Revista de Biologia Lisboa, 1, 125-135, 1957.

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Listabarth, C., The palms of the surumoni area (Amazonas, Venezuela). II. Phenology and pollination of two flooded forest palms, Mauritiella aculeata and Leopoldinia pulchra, Acta Botanica Venezuelica, 22, 153-165, 1999. Löewe, V., C. Alvear, and F. Salinas, Fenología de E. globulus, E. nitens y E. camaldulensis en la Zona Central de Chile: Estudio preliminar., Ciencia e Investigación Forestal, 10, 7398, 1996. Loubry, D., Phenology of Deciduous Trees in a French-Guianan Forest (5 Degrees Latitude North) - Case of a Determinism with Endogenous and Exogenous Components, Can. J. Bot.-Rev. Can. Bot., 72, 1843-1857, 1994. Machado, I. C. S., L. M. Barros, and E. Sampaio, Phenology of caatinga species at Serra Talhada, PE, northeastern Brazil, Biotropica, 29, 57-68, 1997. Malizia, L. R., Seasonal fluctuations of birds, fruits, and flowers in a subtropical forest of Argentina, Condor, 103, 45-61, 2001. Mikich, S. B., and S. M. Silva, Composição florística e fenologia das espécies zoocóricas de remanescentes de floresta estacional semidecidual no centro-oeste do Paraná, Brasil., Acta Botanica Brasilica, 15, 89-113, 2001. Monasterio, M., and G. Sarmiento, Phenological strategies of plants species in the tropical savanna and semi-deciduous forest of the Venezuelan Lianos., J. Biogeography, 3, 325356, 1976. Morellato, L. P. C., As estações do ano na floresta. in Ecologia e preservação de uma floresta tropical urbana, edited by Morellato, L. P. C. and H. F. Leitão-Filho, pp. 37-41, Editora da Unicamp, Campinas, 1995. Morellato, L. P. C., R. R. Rodrigues, H. F. Leitão-Filho, and A. C. Joly, Estudo comparativo da fenologia de espécies arbóreas de floresta de altitude e floresta mesófila semidecídua na Serra do Japi, Jundiaí, São Paulo., Revista Brasileira de Botânica, 12, 85-98, 1989. Morellato, L. P. C., D. C. Talora, A. Takahasi, C. C. Bencke, E. C. Romera, and V. B. Zipparro, Phenology of Atlantic rain forest trees: A comparative study, Biotropica, 32, 811-823, 2000. Morellato, P. C., and H. F. Leitao, Reproductive phenology of climbers in a Southeastern Brazilian forest, Biotropica, 28, 180-191, 1996. Myers, N., R. A. Mittermeier, C. G. Mittermeier, G. A. B. Fonseca, and J. Kent, Biodiversity hotspots for conservation priorities, Nature, 403, 853-858, 2000. Olivares, S. P., and F. A. Squeo, Phenological patterns in shrubs species from coastal desert in north-central Chile, Rev. Chil. Hist. Nat., 72, 353-370, 1999. Oliveira, P. E., and P. E. Gibbs, Reproductive biology of woody plants in a cerrado community of Central Brazil, Flora, 195, 311-329, 2000. Parolin, P., Phenology and CO2-assimilation of trees in Central Amazonian floodplains, J. Trop. Ecol., 16, 465-473, 2000. Peres, C. A., Primate Responses to Phenological Changes in an Amazonian Terra-Firme Forest, Biotropica, 26, 98-112, 1994a. Peres, C. A., Composition, Density, and Fruiting Phenology of Arborescent Palms in an Amazonian Terra-Firme Forest, Biotropica, 26, 285-294, 1994b. Putz, F. E., G. B. Romano, and N. M. Holbrook, Comparative Phenology of Epiphytic and Tree-Phase Strangler Figs in a Venezuelan Palm Savanna, Biotropica, 27, 183-189, 1995. Ramirez, N., Reproductive phenology, life-forms and habitats of the Venezuelan Central Plain, Amer. J. Botany, 89, 836-842, 2002. Ramirez, N., and Y. Brito, Patterns of Flowering and Fructification in a Swampy Community, Morichal Type (Calabozo, Edo Guarico, Venezuela), Acta Cientifica Venezolana, 38, 376381, 1987.


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Ribeiro, L. F., and M. Tabarelli, A structural gradient in cerrado vegetation of Brazil: changes in woody plant density, species richness, life history and plant composition, Journal of Tropical Ecology, 18, 775-794, 2002. Riveros, M., Andean Plant Phenology, Volcan Casablanca, 40-Degrees-S, X- Region, Chile, Archivos De Biologia Y Medicina Experimentales, 16, R181-R181, 1983. Riveros, M., B. Palma, S. Erazo, and S. Oreilly, Phenology and Pollination in Species of the Genus Nothofagus, Phyton-Int. J. Exp. Bot., 57, 45-54, 1995. Rosello, N. E., and S. E. Belmonte, Fenologia de Browningia candelaris (Meyen) Britt. et Rose en la Quebrada de Cardones, Norte de Chile, Idesia, 47-55, 1999. Rossi, B. E., G. O. Debandi, I. E. Peralta, and E. M. Palle, Comparative phenology and floral patterns in Larrea species (Zygophyllaceae) in the Monte desert (Mendoza, Argentina), J. Arid. Environ., 43, 213-226, 1999. Rozzi, R., J. D. Molina, and P. Miranda, Microclimate and Flowering Periods on Equatorial and Polar- Facing Slopes in the Central Chilean Andes, Rev. Chil. Hist. Nat., 62, 75-84, 1989. Ruiz, A., M. Santos, J. Cavelier, and P. J. Soriano, Phenological study of Cactaceae in the dry enclave of Tatacoa, Colombia, Biotropica, 32, 397-407, 2000. Rusch, V. E., Altitudinal Variation in the Phenology of Nothofagus-Pumilio in Argentina, Rev. Chil. Hist. Nat., 66, 131-141, 1993. Sabatier, D., Fruiting Periodicity and Its Determinants in a Lowland Rain- Forest of FrenchGuyana, Rev. Ecol.-Terre Vie, 40, 289-320, 1985. Santos, N., Fenologia, Rodriguesia, 31, 223-226, 1979. Schongart, J., M. T. F. Piedade, S. Ludwigshausen, V. Horna, and M. Worbes, Phenology and stem-growth periodicity of tree species in Amazonian floodplain forests, J. Trop. Ecol., 18, 581-597, 2002. Seres, A., and N. Ramirez, Flowering and Fructification of Monocotyledons in a Venezuelan Cloud Forest, Rev. Biol. Trop., 41, 27-36, 1993. Silberbauer-Gottsberger, I., A hectare of cerrado. II. Flowering and fruiting of thick- stemmed woody species, Phyton-Ann. REI Bot., 41, 129-158, 2001. Silva, J. F., and M. Ataroff, Phenology, Seed Crop and Germination of Coexisting Grass Species from a Tropical Savanna in Western Venezuela, Acta Oecologica-Oecologia Plantarum, 6, 41-51, 1985. Silveira, F. R., Queda de Folhas, Rodriguesia, 1, 1-6, 1935. Sist, P., Structure and Phenology of the Palm Community of a French Guiana Rain-Forest (Piste-De-St-Elie), Rev. Ecol.-Terre Vie, 44, 113-151, 1989. Smith-Ramirez, C., and J. J. Armesto, Flowering and Fruiting Patterns in the Temperate RainForest of Chiloe, Chile - Ecologies and Climatic Constraints, J. Ecol., 82, 353-365, 1994. Smith-Ramirez, C., J. J. Armesto, and J. Figueroa, Flowering, fruiting and seed germination in Chilean rain forest myrtaceae: ecological and phylogenetic constraints, Plant Ecol., 136, 119-131, 1998. Spina, A. P., W. M. Ferreira, and H. d. F. Leitão Filho, Floração, frutificação e síndromes de dispersão de ma comunidade de floresta de brejo na região de Campinas (SP). Acta Botanica Brasilica, 15, 349-368, 2001. Squeo, F. A., N. Olivares, and F. Espinoza, Studies of Plant Phenology in the Chilean Coastal Desert, Iv Region, Archivos De Biologia Y Medicina Experimentales, 21, R334-R334, 1988. Stevenson, P. R., M. J. Quinones, and J. A. Ahumada, Annual variation in fruiting pattern using two different methods in a lowland tropical forest, Tinigua National Park, Colombia, Biotropica, 30, 129-134, 1998.

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Stranghetti, V., and N. T. Ranga, Phenological aspects of flowering and fruiting at the Ecological Station of Paulo de Faria-SP-Brazil, Tropical Ecology, 38, 323-327, 1997. Talora, D. C., and L. P. C. Morellato, Fenologia de especies arboreas em floresta de planicie litoranea do sudeste do Brasil, Revista Brasil. Bot., 23, 13-26, 2000. Ter Steege, H., and C. A. Persaud, The Phenology of Guyanese Timber Species - a Compilation of a Century of Observations, Vegetatio, 95, 177-198, 1991. van Dulmen, A., Pollination and phenology of flowers in the canopy of two contrasting rain forest types in Amazonia, Colombia, Plant Ecol., 153, 73-85, 2001. Velez, V., J. Cavelier, and B. Devia, Ecological traits of the tropical treeline species Polylepis quadrijuga (Rosaceae) in the Andes of Colombia, J. Trop. Ecol., 14, 771-787, 1998. Veloso, H. P., As comunidades e as estações botânicas de Teresópolis, RJ., Boletim do Museu Nacional do Rio de Janeiro, 3, 3-95, 1945. Vidiella, P. E., J. J. Armesto, and J. R. Gutierrez, Vegetation changes and sequential flowering after rain in the southern Atacama Desert, J. Arid. Environ., 43, 449-458, 1999. Wallace, R. B., and R. L. E. Painter, Phenological patterns in a southern Amazonian tropical forest: implications for sustainable management, For. Ecol. Manage., 160, 19-33, 2002. Zhang, S. Y., and L. X. Wang, Comparison of 3 Fruit Census Methods in French-Guiana, J. Trop. Ecol., 11, 281-294, 1995.

Chapter 2.6 THE GLOBAL PHENOLOGICAL MONITORING CONCEPT Towards International Standardization of Phenological Networks Ekko Bruns1, Frank-M. Chmielewski2, and Arnold J. H. vanVliet3 1

Department of Networks and Data, German Meteorological Service, Offenbach, Germany; Subdivision of Agricultural Meteorology, Institute of Crop Sciences, Faculty of Agriculture and Horticulture, Humboldt-University, Berlin, Germany; 3Environmental Systems Analysis Group, Department of Environmental Sciences, Wageningen University, Wageningen, The Netherlands 2

Key words:

1.

Global, Monitoring, Network, Observation program, Fruit trees

BACKGROUND AND OBJECTIVES OF GPM

In the 1990s interest in phenological research and thus demand for phenological observations has increased substantially. Mainly, rising air temperatures in recent decades and the clear phenological response of plants and animals to this increase have caused the growing interest. Many studies have shown that the timing of life cycle events is able to provide a good indicator for climate change impacts (Schwartz 1994; Menzel and Fabian 1999; Chmielewski and Rötzer 2001, 2002). Furthermore, the potential use of these data in other fields like remote sensing (to calibrate and evaluate NDVI satellite information) has added value to phenological data (Reed et al. 1994; Carleton and O'Neal 1995; Schwartz 1999; Schwartz and Reed 1999; Tucker et al. 1999; Chen et al. 2000). So, climate researchers have accepted the values of phenological data, and this renewed interest has increased demand for international cooperation in this area. In 1991, this Schwartz (ed.), PHENOLOGY: AN INTEGRATIVE ENVIRONMENTAL SCIENCE, 93-104 © 2003 Kluwer Academic Publishers. Printed in the Netherlands.

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demand was illustrated by a quote in the Proceedings of the International Conference on Climatic Impacts onn the Environment and Society: “ is necessary for all of us to consider an establishment of a global “It phenological observation network for monitoring of changing climate and its impact to ecosystem” (University of Tsukuba, Ibaraki, Japan January 27–February 1, 1991). The plans for establishing a new global phenological monitoring network were started by the “Phenology “ Study Group” of the International Society for Biometeorology (ISB) at a 1993 meeting in Canada. The objectives of the Phenology Study group were: – To promote a global dialogue among phenologists, by compiling information on phenological research and databanks, – To use this global forum to encourage establishment and expansion of phenological networks, data exchange, and international cooperation, – To encourage research that correlates phenological trends with climatic trends, especially in the context of global change monitoring, – To explore methods of using phenology to stimulate public interest in science, especially among pupils and students. At a second meeting in May 1995 (hosted by the German Meteorological Service in Offenbach), the Phenology Study Group drew up concrete benchmarks that facilitated network implementation. In 1996, the preparations of a Global Phenological Monitoring program (GPM) were completed at the 14th ISB Congress in Ljubljana, Slovenia. Phenologists from all over the world discussed the set-up of GPM. They agreed that the establishment of a Global Phenological Monitoring program was an important tool to meet the objectives of the ISB Phenology Study Group. A main objective of GPM is to form a global standard phenological backbone that can link “local” phenological networks and encourage establishment and expansion of phenological networks throughout the world. GPM can actively increase cooperation. Furthermore, data generated by GPM provide a basis for communication, research, and public relations.

2.

CONSTRUCTION AND SET UP OF GPM

During the design of the GPM program a number of details had to be considered, including the following issues: – What climate-biosphere relations should GPM address? – Which areas of the earth should be covered by GPM? – What species should be included in the monitoring program?

Chapter 2.6: The Global Phenological Monitoring Concept

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– How should the GPM gardens obtain their plants? – What specific site conditions could be tolerated? – How should the observations instructions be formulated? Each of these questions is examined in more detail in the following sections.

2.1

Climate-Biosphere Relations and Geographical Focus in GPM

The timing of phenological phases depends on numerous environmental conditions: temperature, precipitation, soil type, soil moisture, and insolation. However, in mid- and high latitudes, with vegetation-rest (dormancy) in winter and an active growing period in summer, air temperature has the greatest influence on phenology (Fitter et al. 1995; Sparks et al. 2000; Chmielewski 2002). This is especially true for spring phenological phases (Figure 1).

Figure 2.6-1. Beginning of Forsythia suspensa flowering (right axis, yearly dates: dashed gray line with dot symbols, ten year running mean: solid black line, 59-year mean: dashed black line) at Hamburg (Lombardsbrücke 53º33’N, 10º00’E, 10m elev.), 1945-2003, and mean temperature over the three months before the beginning of flowering date (left axis, ten year running mean: solid gray line) at Hamburg-Fuhlsbüttel (53º38’N, 09º59’E, 16m elev.).

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Therefore, GPM focused mainly on temperature impacts on the timing of life cycle events. The influence of temperature is not quite so pronounced for autumnal phases (Estrella 2000). In the arid and semiarid tropics and subtropics, phenology is mainly driven by precipitation, because in these regions air temperature is never a limiting factor. Thus the global network will be mainly restricted to mid-latitudes (about 35° north to the Arctic Circle, and the Tropic of Capricorn to 50° south).

2.2

Selection of Species

The selection of plants is an important factor in determining the success of the monitoring program. A number of criteria were used to choose species: – Plants should have phenological phases that are easy to recognize and observe; – The start of the phases should be sensitive to air temperature; – Plants should be economically important; – Plants should have a broad geographic distribution and/or ecological amplitude; – Plants should be easy to propagate and vegetative propagation of these plants should be common practice; – The whole set of phenophases from the selected plants should cover with flowering stages as many months as possible during the growing season. Based on these criteria 14 species were selected for the GPM-program (Tables 1 and 2). These species consist mainly of fruit trees (specified varieties), some park bushes, and spring flowers. The fruit species represent the so-called “Standard Program”, which is required for each GPM-garden that will be established. The “Standard Program” can be supplemented by the “Flowering Phase Program” (ornamental shrubs and snowdrops) to obtain the “Maximum Program”. Due to different environmental conditions it is not possible to have all plants in the program at all stations in mid- and high latitudes.

2.3

Supply of Plant Species: GPM-Parent Gardens

A global network for plant observations depends, among other things, on the quality of observation objects. Unhealthy plants will disturb the measurements. Furthermore, since genetic differences can have a profound influence on the timing of life cycle events, a mechanism must be in place to guarantee the plant’s genetic identity. The best option is to work with one or several so called “parent gardens”, which are specialized in growing plants, and which are able to distribute the plant material. In 1996, the “Müller“


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Platz” nursery in Germany was engaged for this task, and now acts as parent garden for Europe. In the future, parentt gardens need to be established in other regions of the world like Asia and North America.

2.4

Site and Planting Conditions

Although temperature is the main forcing factor affecting plant development, other environmental factors also play a role. Therefore, to improve data analysis, a number of requirements for phenological garden site conditions were specified to standardize the monitoring program. With the focus on temperature, precipitation impacts were excluded by allowing irrigation in case of extreme water shortage. Another requirement was that the location should be characteristic of the larger region around the observation area. Sites are to be avoided which, due to specific sun exposure (e.g., southern slope), shady side, topographical conditions, (e.g., frost hollow), or urban development, are known to have climatic anomalies, or where deviations from characteristic conditions can be expected. The plants should be planted on level ground (slopes of up to 3 degrees in all directions are still acceptable). The trees and shrubs do not have to be planted in a specified order. The optimum growing site is open ground without obstacles, traffic routes, detrimental (for example, herbivory) or favorable influences (for example, artificial light), or other factors affecting the plants Table 2.6-1. Standard GPM-Observation Program and minimum distances between plants. Species Variety Rootstock Minimum Tree support distance required? Almond Perle der St. Julien A 3.0 while taking Weinstrasse root Red currant Werdavia own-rooted 1.5 none Sweet cherry Hedelfinger GiSelA 5 3.0 while taking root Morello Vladimirskaja own-rooted 3.0 while taking root Pear Doyenne de OHF 333 3.0 while taking Merode root Malus Apple Yellow 2.5 permanent Transparent transitoria Apple Golden M26 3.0 permanent Delicious European Dore de Lyon seedling detached while taking chestnut root

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(shading). As such conditions are certainly not always met; minimum standards were defined (Tables 1 and 2). The minimum distances (Tables 1 and 2) are only valid when plants have been placed taking into account the direction in which the different species of the GPM program are set relative to each other. Larger distances are desirable and consequently not an issue. Table 2.6-2. Flowering Phase GPM-Observation Program and minimum distances between plants. Species Variety Rootstock Minimum Tree support distance required? Witch hazel Snowdrop Forsythia Lilac Mock-orange Heather Heather Witch hazel

Jelena (genuine) Fortunei Red Rothomagensis (genuine) Allegro Long White (genuine)

own-rooted own-rooted

2.5 1.5 2.5

no no no

own-rooted own-rooted own-rooted own-rooted

3.0 0.5 0.5 2.5

no no

If the observed plants are located near obstacles the following issues apply. The minimum distance from the base of any obstacle (building, tree, wall, etc.) should be at least 1.5 times the height of the obstacle (more, two times, from the edge of forested areas). The distance from a two-lane road should be at least 8 m, and from any larger (eight-lane) highway, at least 25 m. All plants must be protected against herbivory (consumption by wild or domestic animals) by a wire-netting fence or individually by an anti-game protective agent. So-called “plant protection covers” (e.g., tube protection and growth covers) are unsuitable, as they can accelerate growth considerably (heat congestion). Thus, preference should be given to wirenetting systems.

2.5

Observation Instructions

Clear and understandable observation instructions help observers accurately monitor the plants and improve the quality of observations. GPM observers are asked to monitor the different phases of each species variety on only one plant. The other plants of the same variety serve to check the observation results, as well as being a reserve in case of loss. Thus, if a plant fails, another is ready to be used without any loss in the data quality. During the main growing season when temperatures are favorable, plants


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may develop at a tremendous rate. In order to obtain the exact date of the beginning of a phase, observations should be made at least 3-4 hours after the sun has passed zenith (midday). This helps to eliminate the possibility that phase onsets were missed during previous plant development. 2.5.1

Definition of phases

Phenological phases are recorded according to a BBCH1 code, which classifies plant growth phases of a lot of species according to a standardized system. The BBCH scale is an internationally recognized standard in the agricultural sector, and is thus an excellent source of standardized guidelines (the BBCH system is explained more in detail in Chapter 4.4). BBCH codes are available for all cultivated plants with economic importance. Consequently, the phases for apples, pears, cherries, and currants can be compared directly with their appropriate scales. For species that are not explicitly considered in a specific BBCH scale, the general BBCH scale can be used, which allows determination of phenological phases for all plants according to the standardized BBCH code. The following descriptions of the phenological phases are a complement to the BBCH definitions. They are somewhat more “traditional” than the short BBCH definitions, giving more detailed descriptions (illustrations of the phases by means of either photos or sketches are included in GPM2 web pages and literature). The descriptions here and definitions in the BBCH monograph3 should in no way contradict each other. Ultimately, the BBCH definitions are to be used. SL = Sprouting of leaves ((bud break: BBCH 07, bud burst: BBCH 53): The buds begin to open in at least 3 places on the object under observation. In the case of flower buds (bud burst) the green leaf tips enclosing flowers are visible; in the case of leaf buds (bud break) the first green is visible. UL = Beginning of the unfolding of leaves (BBCH 11): In at least 3 places on the object under observation, first leaves have pushed themselves completely out of the bud or leaf sheath and have unfolded completely, so that the leaf stalk or leaf base is visible. This phase is sometimes only recognizable by bending back the young leaf. The individual leaf has taken on its ultimate form, but has not yet reached its ultimate size. BF = First flowers open, Beginning of flowering/blossom (BBCH 60): In at least 3 places on the object under observation the first flowers have opened completely. Exceptions:

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Snowdrops (Galanthus nivalis): the first 3 flowers have opened at the plantation. The flower is considered open only when the outer leaves have spread and the stamens are visible. Heather (Calluna vulgaris): on 3 places of the plantation the first flowers have opened completely. FF = Full flowering, General flowering, Full blossom (BBCH 65): Approximately 50% of the flowers are open. EF = End of flowering/blossom (BBCH 69): This phase occurs when the flowers have faded. In some existing networks “flowers have faded” is equated with “approximately 95% of the total petals have fallen”. This rule is somewhat different in formulation to the BBCH69 definition but in practice “de facto” identical. RP = Fruit ripe for picking (for apple, pear, sweet cherry, morello, red currant, BBCH 87): The fruits show the coloring characteristic for their variety and can be removed easily from the fruiting lateral. Exception: Premature ripening should not be reported. RP = First ripe fruits (for almond, European chestnut, BBCH 864): The first ripe fruits fall from the tree naturally. Exception: Premature ripening should not be reported. CL = Coloring of leaves (BBCH 944): Approximately 50% of the leaves have taken on the colors of autumn. Coloring of leaves, caused by drought, should nott be reported. FL = Leaf falll (BBCH 95): Approximately 50% of the leaves have fallen off. Falling of leaves, caused by drought, should not be reported.

3.

ESTABLISHMENT OF THE GPM NETWORK

There are two ways to establish the Global Phenological Monitoring network: setting up new gardens, or adapting existing networks to the proposed standardization. In recent years, both approaches have been pursued.

3.1

Setting Up New GPM Gardens

The first GPM network garden was started in 1998 at Deuselbach (Germany). It is located at a measuring station of the Federal Environmental Agency. Further gardens quickly followed (at the beginning only in Germany), but now also in other countries of the northern hemisphere. The current network includes 15 gardens located in Asia,


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Europe, and North America (Table 3). More gardens are required before the data can be effectively analyzed. At the moment the data from the German GPM-stations are gathered at the Humboldt-University of Berlin. In the near future decisions need to be made on how the network will be administrated in terms of data storage and access. Two existing networks give an idea of the number of stations required for acquiring observational data from genetically homogeneous plants, i.e. the European IPG network5 and the lilac/honeysuckle network6 in the USA. Both networks currently consist of approximately 50 sites and both networks do not cover all of their respective continents. Based on the experience of these networks (and other factors like region, climate, and altitude gradation), we propose at least 75 stations for Europe. It will be an especially effective network if the stations are optimally distributed between Gibraltar and the Ural Mountains. Numbers of needed stations for other continents have yet to be assessed. Table 2.6-3 Established GPM gardens Number of sites Country China Estonia Germany

1 1 9

The Netherlands Slovakia USA

2 1 1

3.2

Locations Beijing Jögeva Blumberg, Brunswick, Deuselbach, Erbeskopf, Geisenheim, Linden Schleswig, Tharandt, Zingst Amsterdam, Wageningen Banska Bystrica Milwaukee

Adaptation of Existing Networks: Linking Networks

The second way of establishing the GPM network is by adapting existing networks into the new network. In the last years, the GPM program expanded because several existing networks added some GPM plants to their own program. In 2001, the “Red Rothomagensis” lilac variety (also used in the USA) and the “Fortunei” forsythia variety were incorporated into the International Phenological Gardens program (from the GPM program). At the same time the first “link gardens” were laid out in Schleswig, Deuselbach and Tharandt (Germany). These are gardens in which both the IPG and the GPM assortments are planted. The link between IPG and GPM will continue, and the present three combined IPG/GPM gardens (as of 2002) will be followed by others. In autumn 2000, the Wageningen Agricultural University distributed bulbs of the snowdrop clone, which is

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also contained in the GPM program, to 700 observers in the Netherlands. In 2002, a standardized phenological garden plan was introduced into the GLOBE program for schools (http://www.globe.gov). The suggested garden consists of the “Flowering Phase Program” of GPM, as these stages are easy for students to observe. Thus, schools around the world can now help to extend the GPM program, fulfilling one of the aims of the original ISB Phenology Study Group: “To stimulate public interest in science, especially among pupils and students.” Finally, some countries have considered using concepts from the GPM program to set up their own national networks. Scientists from Peking University (Beijing) would like to build up a phenological observation network in botanical gardens across China, in which GPM will play a central role. At present the GPM assortment is being propagated at the Beijing Botanical Garden. If these network plans are successful, it will be the first time that a national organization has adopted the full GPM program. By standardizing observations, it becomes possible to link the different networks. Standardization can be applied to the species included in the programs, to the stand of the observation objects (for example, solitary plants or a stand of forest/woodland) as well as to the observation area (for example, maximum distance from the reference point), even to the object (for example, the same individual year to year) and to the definitions used for phenological stages. In recent years, progress has been made in standardizing definitions for phenological stages in Europe, based on European Phenology Network (EPN) activities. EPN has applied BBCHmethodology to the definitions used in twelve phenological networks in Europe so far. This analysis has made it possible to identify to what extent the existing networks are compatible among each other and with the GPM program. In addition to the EPN standardization activities, several other developments have contributed to these efforts. For example, the Meteorological and Hydrological Service of Croatia modified their phenological guidelines in 1996, orienting them more towards the German program, which necessarily meant higher compatibility with BBCH. In 2000, the Central Institute for Meteorology, Austria, proceeded in the same way, and with the same effect. The Dutch phenological network (revived in February 2001) also modeled itself around the German program, so that Dutch plant phases are in complete agreement with those of Germany, and (due to the phase selection) are almost completely in agreement with BBCH. The Canada Plantwatch program was expanded in 2002 and an instruction booklet was published. More plant species were added and phenophases modified to better match European protocols and the BBCH system. MeteoSwiss also has new instructions, which are nearly identical to the


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German program. In all, six European networks now work de facto according to compatible rules, where phenological phases overlap. In the Swiss guide the phenological phases are compared to the corresponding BBCH codes for the first time in national instructions (Brügger and Vassella 2003), and that is at least the intention of the Slovak Hydrometeorological Institute in 2003. This list is not complete, but documents the tendency toward greater standardization, which is not limited to Europe, but also Before the applies to the North American continent, and China. development of the BBCH scales (in the 1990s) and prior to GPM, there were no internationally recognized standards, apart from Zadoks et al.’s (1974) cereal grain scales.

4.

CONCLUSIONS

In recent years, the Global Phenological Monitoring network has steadily increased in size. Set-up issues have been thoroughly explored, and sites successfully implemented in different parts of the world. GPM has demonstrated that it can play a significant role in standardization of phenological networks, as the BBCH-coding system is being adopted by other phenological networks. The first phase of the GPM network also improved cooperation between groups all over the world, and formed the basis for several successful initiatives, such as reviving the Dutch phenological network and the European Phenology Network. GPM will continue to contribute to the further expansion of existing networks, and the establishment of new networks, both to improve the use of phenological information, and improve cooperation and communication between the many actors involved in phenology. The program is now poised for future expansion into other parts of the world. Hopefully, GPM will be just as successful in gaining acceptance from phenologists internationally, as BBCH has been in worldwide agricultural experiments.

NOTES 1

BBCH = Biologische Bundesanstalt, Bundessortenamt, Chemische Industrie (Federal Biological Research Centre for Agriculture and Forestry, Federal Office of Plant Varieties, Chemical Industry) 2 http://www.dow.wau.nl/msa/gpm/ 3 BBCH-Monograph, Blackwell Science, 622 pp., 1997. 4 The reference numbers BBCH 86 and BBCH 94 were defined for this purpose. They fit into the context and do not violate the BBCH principle.

104 5 6


http://www.agrar.hu-berlin.de/pflanzenbau/agrarmet/ipg.html http://www.uwm.edu/~mds/enanet.html

REFERENCES CITED Brügger, R., and A. Vassella, Pflanzen im Wandel der Jahreszeiten, Geographica Bernensia, Bern, Switzerland, 287 pp., 2003. Carleton, A. M., and M. O'Neal, Satellite-derived land surface climate “signal” for the Midwest U.S.A., Int. J. Remote Sensing, 16, 3195-3202, 1995. Chen, X., Z. Tan, M. D. Schwartz, and C. Xu, Determining the growing season of land vegetation on the basis of plant phenology and satellite data in northern China, Int. J. Biometeorol., 44, 97–101, 2000. Chmielewski, F.-M., Trends in the seasons, Bull. Amer. Met. Soc., 10, 1464-1465, 2002. Chmielewski, F.-M., and T. Rötzer, Response of tree phenology to climate change across Europe, Agricultural and Forest Meteorology, 108, 101-112, 2001. Chmielewski, F.-M., and T. Rötzer, Annual and spatial variability of the beginning of growing season in Europe in relation to air temperature changes, Clim. Res., 19(1), 257264, 2002. Estrella, N., On modeling of phenological autumn phases, in Progress in phenology: Monitoring, data analysis, and global change impacts, edited by A. Menzel, p. 49, Conference abstract booklet, 2000. Fitter, A. H., R. S. R. Fitter, I. T. B. Harris, and M. H. Williamson, Relationships between first flowering date and temperature in the flora of a locality in central England, Funct. Ecol., 9, 55, 1995. Menzel, A., and P. Fabian, Growing season extended in Europe, Nature, 397, 659, 1999 Reed, B. C., J. F. Brown, D. Vander Zee, T. R. Loveland, J. W. Merchant, and D. O. Ohlen, Variability of land cover phenology in the United States, J. Veg. Sci., 5, 703-714, 1994. Sparks, T. H., E. P. Jeffree, and C. E. Jeffree, f An examination of relationships between flowering times and temperature at the national scale using long-term phenological record from the UK, Int. J. Biometeorol., 44, 82–87, 2000. Schwartz, M. D., Monitoring global change with phenology: the case of spring green wave, Int. J. Biometeorol., 38, 18–22, 1994. Schwartz, M. D., Advancing to full bloom: planning phenological research for the 21st century, Int. J. Biometeorol., 42, 113–118, 1999. Schwartz, M. D., and B. C. Reed, Surface phenology and satellite sensor-derived onset of greenness: an initial comparison, Int. J. Remote Sensing, 20, 3451–3457, 1999. Tucker, C. J., D. A. Slayback, J. E. Pinzon, S. O. Los, R. B. Myneni, and M. G. Taylor, Higher northern latitude normalized difference vegetation index and growing season trends from 1982 to 1999, Int. J. Biometeorol., 45, 191-195, 1999. Zadoks, J. C., T. T. Chang, and C. F. Konzak, A Decimal code for the growth stages of cereals, Weed Res., 14, 415-421, 1974.

Chapter 2.7 TOWARD A MULTIFUNCTIONAL EUROPEAN PHENOLOGY NETWORK Arnold J. H. vanVliet and Rudolf S. deGroot Environmental Systems Analysis Group, Department of Environmental Sciences, Wageningen University, Wageningen, The Netherlands

Key words:

1.

Network, European, Users, Communication, Cooperation

WHY A EUROPEAN PHENOLOGY NETWORK?

Phenology as a scientific discipline has a very long history. Many local, regional, and national networks exist (see Chapters 2.1-2.6), and the number of disciplines that deal with phenological processes in their own profession is large and diverse (see, for example, the diversity of topics in this book). The phenological community, however, faces a number of problems: – There is insufficient cooperation and communication between the existing regional and national phenological monitoring networks in Europe. – There is a lack of access to and integration of data. This is partly caused by the lack of information on what datasets a are available, the different definitions and techniques used, and the quality of the data. – There is inefficient use and exchange of existing knowledge within and between the different scientific disciplines on tools and techniques already available for monitoring, data storage, and data analysis. – There is insufficient insight in and awareness of the potential practical uses of phenological data. These problems lead to sub-optimal production of data (both in quantity and quality) and inefficient use of phenological information. The many possibilities for data use and production techniques are not fully exploited. Schwartz (ed.), PHENOLOGY: AN INTEGRATIVE ENVIRONMENTAL SCIENCE, 105-117 © 2003 Kluwer Academic Publishers. Printed in the Netherlands.

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More importantly, the low recognition of the multifunctional uses and socioeconomic values of phenological observations has led to a lack of financial support for existing phenological networks. At the same time, there is a strong increase in demand for phenological observations in the past decade, caused by the observed changes in climate and possible consequences for biodiversity and society (see Chapter 2.6). Integration of phenological networks can provide valuable input in large European initiatives like the Global Change and Ecosystems program of the European Commission Sixth Framework Program1, which aims to strengthen the capacity to understand, detect and predict global change. Other initiatives like the Global Monitoring of Environment and Security program (GMES) will also benefit from the input of phenological networks. To address the above-mentioned problems, a European Phenology Network (EPN) was set up in 2001. This chapter presents how this network is helping to improve communication and cooperation between the many disciplines involved, and in the production and use of phenological data. EPN is a Thematic Network (2001-2003), in which 13 partners2 from seven countries participate. The European Commission3 finances the network. EPN aims to “improve monitoring, assessment and prediction of climate induced phenological changes and their effects in Europe.” Its overall objective is to increase the efficiency, added value, and use of phenological monitoring and research, and to promote the practical use of phenological data in European member states in assessing the impact of global (climate) change, and possible adaptation measures. It realizes this objective by focusing on three different areas, which this chapter addresses. First, it demonstrates the variety of possible applications of phenological research and its benefits for biodiversity conservation and society (section 2). Second, it identifies the many different user groups involved (section 3). Third, it provides a number of tools that directly facilitated communication and cooperation (section 4).

2.

APPLICATIONS OF PHENOLOGY

The timing of life cycle events is a fundamental ecological process. In order to identify phenological data and actors that work on phenological issues, it is important to determine for which natural and socio-economic processes phenological information has relevance. Only then is it possible to improve the collection and use of phenological observations. The following sections give an overview of the range of applications of phenological data, demonstrating the diversity of subjects involved and the need and

Chapter 2.7: Toward a Multifunc. European Phenology Network

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opportunities for cooperation and communication between the different actors.

2.1

Biodiversity Science

Biodiversity is defined by the Convention on Biological Diversity (CBD) as: “the variability among living organisms from all sources including, among other things, terrestrial, marine and other aquatic ecosystems and the ecological complexes of which they are part; this includes diversity within species, between species and of ecosystems” (CBD 2001). To maintain biodiversity, plants and animals have to survive until they have reproduced. Thereby, the variability off the timing of life cycle events plays an important role in determining the reproductive success of plants and animals. During their life cycle, they face many abiotic and biotic lifethreatening factors that often only occur during certain times of the year. One of the best ways to cope with these threats is by not being there when they occur. Therefore, for many species, timing of migration, hiding, or transformation in another, less vulnerable, phase is essential. Just as it is important to avoid life-threatening situations, species should also be able to be active when there is enough food and water available for growth. In many cases, life-supporting resources of sufficient quality are not constantly available during the whole year and species have to adjust their timing to optimal periods. Especially in extreme abiotic conditions (like a very cold year), the total productivity and the quality of food (for example plant material) might be low. This directly affects the ability of other species to find enough resources. Furthermore, the ability of plants and animals to find enough resources also depends on the timing of life cycle events of competitors of individuals of the same species or of other species. When organisms have been able to reach the reproductive phase, the success of reproduction still depends to a large extent on timing. First of all, if reproduction takes place by mating of males and females, the timing of reproductive ability of both sexes should be synchronized. Furthermore, the timing of the appearance of juveniles should coincide with the presence of nutrients and water. Migratory birds, for example, have to produce young early enough to give the young sufficient time to gain enough strength to migrate to other areas. If they leave too late, the young will not survive. The above-mentioned examples illustrate the importance of understanding the causes and consequences of variation in timing of life cycle events for biodiversity science. Phenological studies significantly contribute to studies on productivity, reproduction and survival of individual organisms and contribute to studies on the consequences for a whole range

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of species interactions like competition, predation, parasitism, and mutualism.

2.2

Agriculture/Forestry/Fisheries

From the previous section, it is clearr that growth and reproduction of plants and animals are closely linked to abiotic and biotic factors that are strongly controlled and determined by the timing of life cycle events. Because agriculture, forestry, and fishery strongly depend on the productivity and reproduction of certain plant and animal species, these economic sectors have to clearly take due account of the timing of a large number of life cycle events. The length of the growing season, for example, determines the growth potential for crops and potentially the number of rotations within a year. It, however, also determines the amount of production loss caused by “extreme” weather events or by pests and diseases. An early start of the growing season in combination with a late spring frost event can, for example, cause significant damage to crops. Given the importance of the variation in timing of life cycle events for productivity, the agricultural, forestry, and fisheries sectors try to continuously adjust their management activities and techniques (like sowing/planting, harvesting, nutrient supply, pests and diseases control measures, and water supply) to the timing of life cycle events. Because of the long-term experience with the timing of life cycle events, the sectors mentioned in this section have the potential to significantly contribute to other disciplines that have to deal withh the study of phenological processes.

2.3

Human Health

The timing of life cycle events of plants and animals also directly influence many aspects of human health such as allergies, diseases, pests, and water quality. Many people are allergic to allergens that are connected to particles in the air, especially pollen. The timing of pollen release by plants determines the start and length of the pollen season, and thus affects the timing of taking precautions or the occurrence of illness (Huynen et al. 2003). The occurrence and timing of many diseases is also closely related to the timing of the appearance of other organisms, especially insects. The clearest examples are vector borne diseases like malaria. The distribution and occurrence of the insects (vectors) that are able to distribute these diseases strongly depend on environmental variables. In addition to diseases, many organisms and especially insects are considered to be pests that cause distress to people. For example, mosquitoes and ants cause many problems during the time they are active. In addition to cases where plants


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and animals cause direct impacts on human health, there are also many examples where plants and insects cause indirect impacts to human health by affecting agricultural production (quality and quantity), as mentioned in the previous section, leading to health problems.

2.4

Transportation

A good understanding of the variation of timing of life cycle events is also of relevance for transportation. For example, timing of bird migration directly influences the frequency of collisions between birds and airplanes. Another issue is the timing of leaf fall and thus the maintenance activities to remove leaves from roads and rail tracks. If the timing of the maintenance activity is not adjusted to the timing of leaf fall, significant delays in (public) transport can be the result.

2.5

Tourism and Recreation

Many people spend significant amounts of their free time in natural areas. In the Netherlands, for example, the yearly number of day excursions of more than two hours per day (without visits to family, or visits from holiday destinations) is 935 million (http://www.cbs.nl). More and more people adjust their vacation or short visits to nature reserves to the timing of certain life cycle events like coloring of leaves, appearance of migratory birds, or flowering of specific plants. By having a better understanding of the variation in and changes of the timing of life cycle events, the tourism sector should be able to better inform the public on when certain events take place. Based on phenological information, the sector will also be better able to prepare themselves for busy and/or quiet periods.

3.

PHENOLOGY USER GROUPS

As we have seen in the previous section, a large number of ecological and socio-economic sectors are affected by phenological events. In order to improve practical use of phenological data, communication, and cooperation, it is important to realize that within each sector a large number of different user groups are, or potentially can be, involved. In this section we briefly describe the main user groups (see Table 1). These user groups interact by exchanging money, knowledge, data, tools, public relation, and consumables to improve and “sell” their products (in this case phenological information and their applications).

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Effective communication and cooperation between user groups can only take place if they are aware of each other’s roles and objectives. In Table 1 an overview is given of how the different user groups interact through the main “products” they provide. Table 2.7-1. Interaction between user groups: Each cell contains an overview of the product that is provided by the user groups listed in the top row to a specific user group in the first column.

Data

Data provider

Research

Policy

NGOs

Commerce

Media

Public

Kno

Kno,

Fin

Fin, PR

Fin, Too

PR, Kno

Fin, Data

Fin, PR

Fin, PR,

Fin, Kno,

PR, Kno

Fin

Kno

Too

Kno, PR

Fin, Kno,

PR, Kno

Fin

Too, Fin

provider Research

Data

Kno, Too, Fin

Policy

Data

Kno, Too

Kno

Too NGOs

Data

Kno, Too

Fin

Kno, PR

Fin, Too

PR, Kno

Fin

Commerce

Data

Kno, Too

Fin

Kno, PR

Fin, Kno,

PR, Kno

Fin

Kno

Fin

Kno

Data, Kno

Too Media

Data

Kno, Too

Fin,

Kno

Kno Public

Data

Kno, Too

Kno

Fin, Kno, Too

Kno

Kno, Too, Con

Fin = Financial support; Kno = Knowledge: information about processes, problems, and solutions; Data: quantitative and qualitative representation of phenological events and applications; Too = Tools that can be used to find, analyze, and exchange data, or knowledge or to facilitate communication; PR = Public Relations: information on activities of the network of people and organizations included in phenological data collection, analyses and application; Con = Consumables (e.g., food, medicines): the production of which is influenced in quality and/or quantity by phenological information.

3.1

Data Providers

Data providers record at what date and time a predefined (phenological) activity of a specific species takes place in a specific year at a specific location. Data providers should constantly be aware of the specific demands of the users of the data and assess whether they still provide the data that the users need and in what format the users want to receive the data. Researchers will undoubtedly have other demands than the media. Phenological monitoring networks should also be aware of the fact that the same information can be used in many different ways. For almost all user groups the quality of the observations is important and increases if the number of observations and the geographical coverage is increased. Phenological networks have demonstrated that involvement of the public is


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an important help in realizing this objective, provided that the observation technologies applied are standardized. The usefulness of the data also increases if the observations are easy and quickly accessible (see for example the Nature’s Calendar network in the United Kingdom and the Dutch network De Natuurkalenderr4).

3.2

Research

Research is essential to develop and improve tools for monitoring, data analysis, modeling, forecasting, and decision support. Research is also important to interpret the outcome and application possibilities of phenological observations, for example: – What (a)biotic factors determine the timing of life cycle events; – What is the impact of (changes in) the timing of life cycle events on ecological and socio-cultural processes; – How can we control or influence the timing in such a way that we can mitigate adverse effects or better benefit from it. The knowledge and tools provided by the research community have relevance for all user groups because many of the underlying processes related to timing are universal. The research community adds content and relevance to the original phenological observations and makes the data easier to use. In many cases, researchers can apply the tools developed for one sector to other sectors. For example, ecological models developed to assess the start of flowering of tree species are of direct relevance for those users that assess the start of pollen release in the context of human health. Communication between scientific communities is required to improve efficient use and exchange of knowledge and tools.

3.3

Policy Makers

Policy makers are usually specialized by theme or sector, each with their own objectives: for example, environmental policy (to protect the environment); nature policy (to protect nature); and human health (to provide good health care). To monitor the effects of policy decisions and the degree to which certain objectives are achieved, phenological information is essential. In addition to the thematic specialization, it is also important to realize that policy makers address issues at different scales: local, regional, national, or international level. This has implications for the type of information they require and the actions that they will undertake to obtain this information, and the willingness to provide financial support for data collection, analyses, and dissemination.

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3.4


Non Governmental Organizations

The objective of Non-Governmental Organizations (NGOs) is to inform society on issues for which they (i.e., their constituency) think that the government or industry is not paying enough attention. In order to do this, NGOs gather information on the issues and disseminate this knowledge to user groups that can undertake action to prevent or solve the problems. NGOs often gather knowledge themselves or they support individuals or organizations in their activities. This support can be financial but also through public relations to raise attention for the issue.

3.5

Commerce

Commercial products can be consumables (e.g., food or wood produced by agriculture, fisheries, and forestry). Phenological data and knowledge can significantly improve the quality and/or efficiency of the production process of consumables, as explained in section 2. Phenological information helps to understand and deal with processes like crop growth, frost damage, and pests and diseases, and also carbon sequestration. Another commercial sector of relevance is the Information and Communication Technology (ICT) sector that develops tools and techniques (e.g., database and communication technologies). Commercial companies can provide the tools and techniques that can be used for gathering, storage, analysis, and exchange of phenological data and information. The different commercial sectors mentioned can also use phenology as a public relation tool since many people and organizations are interested in phenology. By working together with phenological networks and by applying phenological information they can show that they care about the environment by improving their production process (for example, use of phenological information to reduce pesticide use) or by supporting activities that are seen as a general public interest.

3.6

Media

The aim of the media is to provide the public with information and news in which the public (or specific target groups) is interested, so that people are willing to pay for their news, overviews, or listen/look at their programs. Only then, they can attract advertisements or government support and thus money to continue to exist. Phenology has proven to be an interesting subject for the media as it can closely meet the requirements of different media (newspapers, television, radio). As competition for attention in the


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media is strong, providers of phenological information should deliver the information in a way that it can easily be incorporated into news items.

3.7

General Public

Phenology can provide non-commercial information that the public can use to improve their welfare. With access to phenological information, people will become better aware of their own surroundings, both the things that happen and the actions taken. With phenological information, people will become better aware of the many interactions between changes in, for example, weather and climate and the effects on nature and their own welfare (for example human health). With this information, people will be able to better understand causes and effects of their personal behavior and the consequences of corporate and government decisions.

4.

TOOLS FOR IMPROVING COOPERATION AND COMMUNICATION

An important aim of the European Phenology Network is to provide the phenological community, with its many different sectors, with a common platform for better cooperation and communication. A variety of activities contribute to achieving the goals: international meetings, databases, standardization, and ICT-technologies and media.

4.1

International Meetings

During the EPN project (2001-2003), international conferences and workshops played an important role in bringing people together from many different networks, sectors, and user groups who normally would not meet each other. These meetings facilitated direct exchange of knowledge, data, and tools and techniques. These meetings discussed the changes in timing that are going on as a result of the observed change in climate, and focused on demonstrating the many application possibilities of phenological information. In addition to two conferences, several specialist workshops, attended by up to 30 people, provided the opportunity to discuss several main subjects in more detail. Six themes were selected: bird migration, agriculture, human health, modeling, remote sensing, and communication, dissemination, and capacity building (reports are available at the EPN website, http://www.dow.wau.nl/msa/epn/).

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4.2


Databases

Well-structured databases that are easily accessible and up to date are essential to facilitate the exchange of information on what organizations and products are available. The European Phenology Network developed two on-line freely available databases: a meta-database and a bibliographical database. The meta-database aims to provide easy access to information on what phenological networks exist or have existed in the past. Formerly, it was unclear what networks existed or who was the contact person for a specific network. This, of course, hampered cooperation, communication and effective use of the data. The bibliographical database aims to provide an overview of the publications that exist related to phenology. References in this database contain publications on: botany, zoology, ornothology, entomology, geography and history, and also agronomy, forestry, environment and medical sciences (Jeanneret 1997). Each of these disciplines has its own publication forum, which makes publications difficult to find. Furthermore, much fundamental work was done a long time ago and is no longer accessible. By bringing together these scientific disciplines in one database, scientists are able to find existing expertise that they might need more quickly and more efficiently.

4.3

Standardization

Use of data from different networks for making large-scale analyses of, for example, climate change impacts, is only possible if the data are in the right format. Because the history of the various networks is often quite different, there are contrasting standards and procedures used. For example, definitions of how to determine the start of leaf unfolding could differ from network to network. Standardization has to be applied in order to make cooperation and exchange of data possible. The European Phenology Network provided a standardization key to harmonize and interpret the different definitions used for phenological phases (see Chapter 4.4).

4.4

ICT Technologies and Media

Very promising tools for the phenological community are the recent developments in ICT and cooperation with the media. A few phenological networks have started to develop on-line information systems4. These systems have been very successful as they provide observers the ability to enter their phenological observations and to directly provide a detailed


115

visualization of all observations made within the network. The system provides “live” maps, tables, and graphs of the changes that occur in natural systems. Although EPN has not been directly involved in the development of these tools, its partners2 are. The information systems have proven to be a very (cost) efficient way to run phenological networks with thousands of active observers. These tools provide new ways to meet the information and data requirements of many users.

5.

CONCLUSION AND DISCUSSION

The objective of the EPN project was to increase the efficiency, value, and use of phenological monitoring and research, and to promote the practical use of phenological data in Europe. To achieve these objectives, EPN provided a systematic overview of the large number of application possibilities of phenological information, made contact with the many data providers and user groups involved, and improved communication tools. The two International Conferences held in 2001 and 2003 and the six workshops significantly increased the potential for cooperation within the phenology-community in Europe and beyond. In this chapter, we have shown that phenological information is valuable to a large number of environmental and socio-economic sectors. Data, knowledge, and techniques gathered for one sector often has high relevance for other sectors. Models that assess the date of insect appearance, for example, have relevance for agriculture, forestry, ecology, and human health. Therefore, when people involved in one sector expand their network, they can increase the importance of, and interest in their work, and provide their product to more customers. This chapter also highlighted that the groups of people that are (potentially) interested in phenological data, information, and technologies is very diverse, even within one sector. We identified many different user groups and demonstrated that each of these groups has its own objectives and role in the phenological community. Often, these different groups can benefit from each other since they all have their own specialization. There is a large potential for increased cooperation, both within and between different user groups. To improve collaboration, it is very important that actors (stakeholders) specify and communicate their needs (for example, data, information, tools) as well as their own products. Ideally, each actor group should carry out a stakeholder analysis that identifies potentially interested collaborators and products that are available. Based on the stakeholder analysis in this chapter we would like to emphasize the important role of data providers in the phenological

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community. Without data, there will be no research that can show the importance of phenology, which will reduce the interest in phenology, both from the public and (commercial) users and which will make it difficult to maintain existing and develop new networks. In addition, communication tools provide the “lubricant” of the network. People and organizations must be able to easily and quickly exchange their data, knowledge, and techniques. From our analyses we are convinced that the phenological community has an enormous potential to grow in the future and contribute significantly to environmental monitoring programs and applications. However, this can only be realized if the actors involved increase their internal and external communication and cooperation through better use of existing facilities and investment in the further development of new instruments and active participation in networks.

NOTES 1

Sixth Framework Program website: http://www.cordis.lu/fp6/ EPN Partners are: Environmental Systems Analysis Group, Wageningen University, the Netherlands (coordinator); German Weather Service, Germany; SME-Milieuadviseurs (GLOBE-the Netherlands), the Netherlands; Department Data & Computation, Potsdam Institute for Climate Impact Research, Germany; Institute of Geography, University of Berne, Switzerland; Lehrstuhl für Bioklimatologie, Technical University Munich, Germany; Institute for Environment and Sustainability, Unit Land Management, Joint Research Center, Italy; Centre for Geoinformation, Wageningen University, the Netherlands; International Center for Integrative Studies, the Netherlands; World Health Organization, Italy; Department of Agricultural Sciences, Royal Veterinary and Agricultural University, Denmark; Centre for Ecology and Hydrology Monks Wood, United Kingdom, International Center for Environmental Assessment, Foundation for Sustainable Development, the Netherlands. 3 Energy Environment and Sustainable Development Program, subsection “Better Exploitation of existing data and adaptation of existing observing systems.” 4 Nature’s Calendar in the UK (http://www.phenology.org.uk/) and Natuurkalender in The Netherlands (http://www.natuurkalender.nl). 2

REFERENCES CITED Convention on biological diversity (CBD), Convention text, Secretariat of the Convention on Biological Diversity, United Nations Environmental Program, 2001.


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Huynen, M., B. Menne, H. Behrendt, R. Bertollini, S. Bonini, R. Brandao, C. BrownFahrlaender, B. Clot, C. D'Ambrosio, P. de Nuntiis, K.L. Ebi, J. Emberlin, E. Erdei Orbanne, C. Galan, S. Jaeger, S. Kovats, P. Mandioli, P. Martens, A. Menzel, B. Nyenzi, A. Rantio-Lehtimaeki, J. Ring, O. Rybnicek, C. Traidl-Hoffmann, A. vanVliet, T. Voigt, S. Weiland, and M. Wickman, Phenology and human health: allergic disorders, Health and Global Environmental Change Series No.1., EUR/o3/5036791, Rome, Italy, 55 pp., 2003. Jeanneret, F., International bibliography of phenology, Institute of Geography, University of Berne, Switzerland, 68 pp., 1997.

PART 3

PHENOLOGY OF SELECTED BIOCLIMATIC ZONES

Chapter 3.1 TROPICAL DRY CLIMATES Arturo Sanchez-Azofeifa1, Margaret E. Kalacska1, Mauricio Quesada2, Kathryn E. Stoner2, Jorge A. Lobo3, and Pablo Arroyo-Mora4 1

Earth and Atmospheric Sciences Department, University of Alberta, Edmonton, Alberta, Canada; 2Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Morelia, México; 3Biology Department, Universidad de Costa Rica, San Jose, Costa Rica; 4Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT, USA

Key words:

1.

Tropical, Remote Sensing, Dry Forest, Conservation, Land cover change

INTRODUCTION

Based on the Holdridge life zone system (Holdridge 1967) approximately 111,599,269 km2 around the world have a climate favorable for dry forest (Leemans 1992, Figure 1). Of that area, 94% is located in the tropics. Tropical dry forests are found between the two parallels of latitude, the Tropics of Cancer and Capricorn (23º27’ N and S) where there are several months of little or no precipitation (Holdridge 1967). In general, three to seven month’s dry season duration has been quoted for seasonally dry forests (Janzen 1983; Murphy and Lugo 1986; Luttge 1997; Piperno and Pearsall 2000). The tropical dry forest ecosystem is one of the most fragile and least protected ecosystems in the world. In general, Neotropical dry forests are less species rich than moist or wet forests. For example, 430 species of woody plants have been recorded in the wet forest of La Selva Biological Station, Costa Rica (Hartshorn and Hammel 1994), while in the dry forest of the Santa Rosa National Park, Costa Rica, 160 species (51 families) have been inventoried (Kalácska and Sánchez-Azofeifa, unpublished data). In addition, Gentry (1995) reports a Schwartz (ed.), PHENOLOGY: AN INTEGRATIVE ENVIRONMENTAL SCIENCE, 121-137 © 2003 Kluwer Academic Publishers. Printed in the Netherlands.

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range of 21–121 species (nine and 41 families) from various 0.1ha plots around the Neotropics. However, there is more structural (e.g., wood specific gravity) and physiological (e.g., growth seasonality) diversity in the plant life forms of dry forests than in wet forests (Medina 1995).

Figure 3.1-1. Areas around the world with a climate favorable for supporting a dry forest ecosystem. Spatial resolution: 0.5 degrees latitude by 0.5 degrees longitude (modified after Leemans 1992).

Tropical forests that once formed a continuous habitat across Mesoamerica and some regions of the Pacific and Atlantic regions of South America, are now found in fragmented patches (Whitmore and Sayer 1992; Heywood et al. 1994; Trejo and Dirzo 2000). Tropical deforestation is likely to affect both biotic and abiotic factors that control the phenological expression of plant communities with severe consequences to plant populations and the communities that interact or depend on them (Cascante et al. 2002; Fuchs et al. 2003). However, fortunately in certain regions of the Neotropics such as in Costa Rica, the secondary forests are in a state of regeneration through which the dry forests are also starting to recuperate (Arroyo-Mora 2002). Both savannahs and dry forests (T-df) can co-occur in areas with the same climate, but the dry deciduous forests have a a tendency to be found in areas with greater soil fertility (Ratter et al. 1973; Mooney et al. 1995). In many areas however, the occurrence of either savannah or dry forest is principally controlled by human disturbance (Maass 1995; Menaut et al. 1995). Due to the favorable climatic conditions in which they are found, tropical dry forests have been heavily exploited for agriculture (Ewel 1999). Piperno and Pearsall (2000) argue that historically, tropical wet and dry forests had completely different associations with human activities. They state that the

Chapter 3.1: Tropical Dry Climates

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deciduous and semi-evergreen forests (especially the T-df) were the locations of the majority of the early human settlements in addition to being the home of the wild ancestors of many crop plants as well as the origin of animal husbandry. Even today, in most tropical countries, the majority of the agriculture and pasturelands are located in areas that used to be dry and moist forest. This pattern of both higher population density as well as higher intensity food production in the T-df as compared to wetter life zones may be a reflection of the historical tendency for humans to settle these areas (Piperno and Pearsall 2000). It appears that the tuberous plants that are rich in starch for human consumption seem to be more common in the seasonal forests, since the tuber is developed in part for energy storage during the dry season. The long dry season aided in burning of the vegetative cover in order to prepare the fields for agriculture (Piperno and Pearsall 2000). In addition, weeds and pests are less aggressive in the drier environments (Murphy and Lugo 1986). Tropical dry forest phenology is an area that is still in its early stages of academic discovery, since historically more emphasis has been placed on tropical evergreen forests, especially the Amazon Basin (Luttge 1997). Therefore, there is a need for continuous and systematic efforts to understand its phenological patterns and integrate its phenological mechanisms at two basic levels: 1) In the context of conservation biology and 2) the context of land use and land cover change that are taking place on this rich agricultural frontier. In this chapter we document different aspects related to leaf phenology in the tropical dry forest ecosystem and its implications for satellite remote sensing. Emphasis is placed on presenting a description of the causes of leaf phenological change in this threatened ecosystem, and how these can be linked with conservation biology and land use/land cover change at the regional level.

2.

CAUSES OF PHENOLOGICAL CHANGE

Several studies have indicated that the phenological expression of leaves, flowers and fruits are affected by biotic and abiotic factors. Abiotic factors such as changes in water level stored by plants (Reich and Borchert 1984; Borchert 1994, but also see Wrightt and Cornejo 1990; Wright 1991), seasonal variations in rainfall (Opler et al. 1976), changes in temperature (Ashton et al. 1988; Williams-Linera 1997) photoperiod (Leopold 1951; Tallak et al. 1981; van Schaik 1986), irradiance (Wright and van Schaik 1994) or sporadic climatic events (Sakai et al.1999), have been proposed as the main causes of leaf production or leaf abscission in tropical dry forest plants. In contrast, biotic factors, such as competition for pollinators or

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pollinator attraction (Robertson 1895; Janzen 1967; Gentry 1974; Stiles 1975; Appanah 1985; Murray et al. 1987; Sakai et al. 1999; Lobo et al., in press), competition for seed dispersers, and avoidance of herbivory (Marquis 1988; Aide 1993; van Schaik et al. 1993) have been considered as the factors regulating the intensity and duration of leaf and flower production. The abiotic and biotic factors are not mutually exclusive, and it is likely that several are interacting to regulate the expression of each phenological phase. In tropical dry forests, apart from foliage seasonality, relationships between water availability and the structural and physiological characteristics such as hydraulic architecture or sensitivity to water stress produce a variety of phenological behaviors (Murphy and Lugo 1986; Bullock 1995; Holbrook et al. 1995; Luttge 1997, among others). However, due to the remote sensing component of this chapter, the discussion in this section will be largely limited to phenological changes in leaf cover, even though most studies that evaluate the effect of abiotic and biotic factors on the phenological expression of tropical plants (both dry and wet forests) have mainly studied leaf, but not flower or fruit phenology. One of the major causes of the leaf phenological patterns (as mentioned above) in all tropical dry forest is the length of the dry season. This difference may be partly responsible for the differences in physical characteristics such as canopy height or biomass. Apart from leaf phenology, the length of the dry season and the seasonality of precipitation are also important for evolutionary adaptations of gene and seed dispersal, which are distinct in dry forests from the wet forests. In general, in dry forests most trees have conspicuous flowers and wind-dispersed seeds. Dry forests also have a lower biomass and a smaller stature than wet forests (Gentry 1995). Two other main factors that influence leaf phenological patterns are edaphic associations and topography since they determine the spatial heterogeneity of the available water (Murphy and Lugo 1995). Water stress can vary at both regional and local scales. This variability induces a multitude of tree life forms with different leaf phenological patterns (Mooney et al. 1995). At the regional scale, the structure of the forest is greatly affected. It has been shown that as water availability decreases, so does the number of canopy stories as well as the horizontal continuity of the canopy (Murphy and Lugo 1995). Figure 2 compares the climate diagrams (Walter 1971) for fourteen sites from different life zones, ranging from wet to dry forests in Costa Rica as well as the dry forest in Chamela, Mexico. The mean monthly temperature (ºC) and the monthly precipitation (mm) are scaled to represent the potential evapotranspiration. Dry months are represented by dotted areas, humid months by the vertical lines, and months with rain in excess of 100 mm are in solid black. Differences in the severity of the dry season as well as the pattern of the


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rainfall can cause the different leaf phenological patterns observed at various sites. For example, in Guanacaste, Costa Rica, Gentry (1995) estimates that 40-60% of the tree species are deciduous whereas over 70% are deciduous in Chamela, Mexico, where the severity of the dry season is more pronounced (Figure 2).

Figure 3.1-2. Climate diagrams for fourteen representative sites in Costa Rica and Chamela, Mexico.

The general leaf phenological response to the dry season is drought deciduousness where the woody plants lose their leaves in the dry season, but there are exceptions (wet season deciduous, Fanjul and Barradas 1987) as well as dry evergreen forests and evergreen succulent plants in dry forests (Gentry 1995; Holbrook et al. 1995). Occasional anomalous rains in the dry season and drought spells in the wet season complicate this variation in resource availability in the rainy season. The growing periods are thus affected by the variability in flushing as it occurs in response to anomalous rains in the dry season or variation in the drying out process (Murphy and Lugo 1995). In a comparison between wet (La Selva) and dry (Comelco) sites in Costa Rica, Frankie et al. (1974) found that the forest at La Selva maintained its evergreen appearance throughout the year. However, even this wet forest experienced increased leaf flushing with the onset of the wet

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season. In Comelco they found that while leaf fall began as early as October, the majority of the trees lost their leaves in the dry season, with the peak in leaf fall occurring in March. Of the 113 species they inventoried at Comelco, 83 partially or completely lost their leaves and 19 were evergreen (ex. Clusia rosea, Styrax argenteus). The trees in the Riparian zones lost their leaves, but were simultaneously replaced. One species, Lysiloma seemannii had an unusual leaf-flushing pattern in that after it lost its leaves in the dry season, the new leaves did not appear until one month after the rainy season began. Certain species also brought new leaves in January and March but most of these species (for example, Anacardium excelsum, Coccoloba padiformis) were from the Riparian zones. In total, Frankie et al. (1974) found that 75% of the species are affected by the seasonality of the precipitation in the dry forest, compared to 17% in the wet forest. The timing of leaf flushing was also found to be very different: in the wet forest, most of the leaves were produced in the dry season, whereas in the dry forest the leaves were produced at the beginning of the wet season.

3.

PHENOLOGY AND CONSERVATION BIOLOGY

In this section, we review the literature and present some of the main consequences that change or disruption of plant phenology may have on the viability of plant populations and animal communities that interact with them. Biotic factors, such as competition for f pollinators or pollinator attraction have been interpreted as important adaptive forces responsible for phenological patterns in tropical plants (Robertson 1895; Janzen 1967; Gentry 1974; Stiles 1975; Appanah 1985; Murray et al. 1987; Zimmerman et al. 1989; Sakai et al. 1999; Lobo et al., in press). A disruption of the flowering phenological patterns caused by disturbance or fragmentation is likely to affect the behavior and visitation rate of pollinators. Fragmented landscapes reduce the amount of resources available, as well as appropriate areas for roosting and perching for nectarivorous bats and birds that serve as important pollinators for many tropical plant species (Feinsinger et al. 1982; Andren and Angelstran 1988; Bierregaard and Lovejoy 1989; Rolstad 1991; Saunders et al. 1991; Helverson 1993; Quesada et al. 2003). If the flowering pattern of plants that share pollinators of the same guild is displaced over time (Frankie et al. 1974; Stiles 1975; Fleming 1988), competition for the same pollinators will occur, resulting in negative consequences for the reproductive success of the plants and the ability of the pollinators to obtain resources over time. For example, in the tropical dry forest of the ChamelaCuixmala Biosphere Reserve, Mexico, trees of the family Bombacaceae


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provided the main resource to the nectarivorous bats Leptonycteris curasoae during eight months and Glossophaga soricina during six months. Both bat species concentrated on one bombacaceous species each month (Stoner et al. 2003). The sequential use of bombacaceous species by these bats coincided with the flowering phenology of the tree species. These data suggest that changes in the flower phenology caused by habitat disruption may result in competition between these bat species and ultimately may result in local extinction, especially of endemic species that are common in this dry forest. A rare endemic nectarivorous bat that is only found in four states in Mexico, Musonycteris harrisoni, foraged on the bombacaceous tree Ceiba grandiflora during three months of the year (Stoner et al. 2002). Since this species has such a restricted distribution and is a specialist nectarivore, changes in flower phenology could be catastrophic for populations of this bat. Timing of leaf flushing directly affects insect herbivores that depend upon flushing species to complete part a of their life cycle (Janzen 1970, 1983; Dirzo and Dominguez 1995). Phenological changes caused by habitat loss will also disrupt the pollination patterns of many long-distance pollinators and trap-liners such as some large bees, hawkmoths, nectarivorous bats, and hummingbirds that have been shown to follow the flowering phenology of plants (Stiles 1977; Haber and Frankie 1989; Frankie et al. 1998; Fleming et al. 1993; Haber and Stevenson 2003). For example, in Costa Rica, hawkmoths regularly move from the lowland tropical dry forest to surrounding areas at higher elevations, following patterns of flowering resources (Haber and Stevenson 2003). Similarly, in México and the southwestern U.S. some nectarivorous bats have been shown to migrate following the availability of flower resources, mainly from the family Cactaceae and Agavaceae (Fleming et al. 1993). Intra-specific variation in the frequency, duration, amplitude and synchrony of flowering by individuals also has been proposed as an important factor that affects the reproduction and the genetic structure of tropical plant populations in disturbed r habitats (Murawski et al. 1990; Murawski and Hamrick 1992; Newstrom et al. 1994; Doligez and Joly 1997; Nason and Hamrick 1997). Flowering phenology directly determines the effective number of pollen donors and the density of flowering individuals, both of which affect the patterns of pollen flow between trees (Stephenson 1982; Murawski and Hamrick 1992). Plants with asynchronous flowering may experience a decrease in reproductive output, the amount of pollen, the number of pollen donors and the levels of outcrossing compared to individuals blooming during the same period. Fuchs et al. (2003) suggested that pollinator behavior is likely to change the mating patterns of P. quinata. This study showed that in disturbed fragmented habitats or in trees with

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early or late peak flowering, bat pollinators are more likely to promote selfing within trees (i.e., geitonogamy) and they have a tendency to produce singly sired fruits, whereas in undisturbed natural forests outcrossing is higher and multiple paternity is more common. The long-tongued bat (Glossophaga soricina), one of the main pollinators of P. quinata, has been shown to adopt a territorial behavior within a single plant in disturbed isolated environments with limited resources (Lemke 1984, 1985). The timing of fruiting during the year, which may be altered as a result of environmental changes associated with habitat disturbance, may affect potential vertebrate seed dispersers that, in turn, may affect the reproductive success of the plants they disperse (Flemming and Sosa 1994). Frugivorous Old World and New World bats are known to migrate or change habitats depending on the availability of fruit resources (Eby 1991; Stoner 2001). Similarly, the abundance of temperate and altitudinal migrant birds in tropical forests is closely associatedd with fruit abundance (Levey et al. 1994). Furthermore, displacement of fruiting phenology of tree species that are keystone resources because they provide fruits when resources are relatively scarce, could have negative consequences on populations of birds and mammals that disperse their seeds and ultimately negative effects on recruitment of the species they disperse (Howe 1984). Seed dispersal by animals is negatively affected by deforestation and results in lower recruitment in forest fragments. Another factor affected by forest fragmentation is seed predation. In a tropical dry forest seed predation by bruchid beetles on the tree Samanea saman was higher in populations of trees found in continuous forest and found to be much less in isolated trees (Janzen 1978). The bruchid beetles, Merobruchus columbinus and Stator limbatus (Bruchidae) are specific seed predators of S. saman. It is likely that the populations of these bruchid species are affected by density dependent factors related to the availability and fluctuation of food resources within fragments, including seeds and flowers. Another explanation is that adult bruchids have to fly greater distances to find isolated trees than trees in continuous populations. This pattern of higher seed predation in populations from continuous forest also has been observed in the dry forest tree, Bahuinia pauletia. Finally, the ultimate consequences of habitat reduction and phenological disruption is a decrease in reproductive plants, increasing the negative effects of endogamy, reducing the quantity and quality of pollen, and lowering the genetic variability of the progeny (Cascante et al. 2002). This likely will affect the viability and establishment of plant populations over time.


4.

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PHENOLOGY AND LAND USE / COVER CHANGE

Remote sensing data provides the possibility for an instantaneous look at a large area with the opportunity of acquiring frequent repeat imagery for the same area. This is important for phenological studies because the temporal variability of the ecosystem can be captured at large scales. In particular, it is essential to consider leaf phenology in order to correctly characterize areas of deciduous forest. Since they measure surface reflectance, optical sensors have been widely used for land cover classification and characterization. However, it must be taken into consideration that one of the greatest limitations to optical sensors is cloud cover. And in the tropics, cloud cover is especially prevalent in the wet season. Cloud free imagery is more easily acquired during the dry season, where in deciduous forests, the majority of the trees are leafless (Arroyo-Mora 2002). In addition, vegetation studies using reflectance data have generally focused on green leaves, with both dry vegetation and non-green components being neglected in comparison (van der Meer 1999). However, in areas of deciduous forest green leaves will not always dominate the spectral signature of the forest. In the dry season, only a small fraction of the spectra will be representative of green foliage. The majority of the pixels will be representing leaf litter, bark, branches and soil in various combinations. Therefore, this temporal variability of the spectral signatures that can be extracted from imagery must be taken into consideration in such environments. As an example, two false color composite images of the same area of dry forest surrounding the Chamela Biological Station, Mexico, were acquired during the dry (March) and wet (August) seasons from the Landsat 7 ETM+ sensor (not shown). While the two images visually look completely different, more importantly, the spectral signature of the forest also changes with the seasons. This is key because many algorithms rely on spectral signatures to classify areas. If the same unsupervised classification algorithm (Isodata) is run on the two images, 180 km2 of forest cover is extracted from the wet season image, while only 26 km2 of land cover exhibits the spectral signature of forest in the dry season (Kalacska et al. 2001). In the dry season image, only the Riparian areas appear to have forest cover. In a similar case study from the Santa Rosa National Park, Costa Rica, two images (dry season – April and wet season – October) of Landsat TM 5 were classified using an unsupervised classification into forest and nonforest classes. From the wet season image, 61 km2 of forest were extracted, whereas from the dry season image only 18 km2 were classified as forest (Kalacska et al. 2001). The discrepancy in the amount of forest extracted

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from the images in the two seasons is because dry deciduous forests where trees lose their leaves, may seem to have the spectral signature of pasturelands or agricultural fields in the dry season (Figure 3).

Figure 3.1-3. Spectral signatures of the dry forest at the Santa Rosa National Park from Landsat TM 5 images. a) wet season (October) and b) dry season (April). Solid line deciduous forest, dashed line - evergreen forest.

In the wet season (Figure 3a), the spectra for both the evergreen and deciduous components of the forest are similar. However, in the dry season (Figure 3b), the spectral signature of the deciduous forest no longer resembles that of the evergreen forest. In fact, there is more than a 20% difference in the near infrared band (band 4) between the two forest classes in the dry season. While these results are important at a local scale, their implications become more profound if regional or global scales are considered. For example, Sader and Joyce (1988) reported the total forest cover for Costa Rica as 17%. If their map of forest distribution is examined, it can be seen that the province of Guanacaste and the Nicoya Peninsula, both with large extents of deciduous forest, are shown as almost completely non-forest. In a more recent classification of Guanacaste and the Nicoya Peninsula, using Landsat 7 ETM+ imagery, Arroyo-Mora (2002) shows that the forest cover is actually 45%. At the national scale, in the most recent remotely sensed forest cover inventory to date of the entire country of Costa Rica, Sanchez-Azofeifa et al. (2002) report a total forest extent 58% greater than the other previous studies (Castro-Salazar and Arias-Murillo 1998). Seasonal changes in leaf phenology in the deciduous forest are part of the reason for those differences. Even at the spatial resolution of most global monitoring systems (1km) significant areas of forest can be missed if only dry season images are used or if the phenological changes in leaf cover are


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not taken into consideration. This forest, which has been ignored by previous remote sensing analysis, is not uniform and includes different stages of succession with different levels of deciduousness (Arroyo-Mora 2002). For example, in the recent global land cover classification from the MODIS Land Cover Classification Program, neither the area encompassing the Chamela Biological Station, México nor the Santa Rosa National Park, Costa Rica is classified as forest. These complications are important not only for classification purposes, but also in many cases outputs from such data sets are used in global models like CENTURY. The calculations from such models are then further used to calculate baselines and benefits of a given policy for carbon sequestration, for example.

5.

FINAL REMARKS

Since so many organisms depend upon phenological patterns in tropical forests, it is crucial to document how these phenological patterns may be changed by deforestation and the resulting habitat fragmentation. Future studies on phenological patterns of tropical plants should attempt to document intra-specific variation within distinct habitat types and under different levels of disturbance, in order to provide a clear understanding of ecosystem phenological response to different levels and types of disturbance. This information will be important in quantifying the effects of forest fragmentation on phenological patterns and ultimately on tropical ecosystems. A wealth of information is available on studies conducted with remotely sensed data in both the temperate and tropical regions. And while the image processing techniques may be similar, the ground validation techniques are very different in certain aspects. The complexity (structural and temporal) of the tropical deciduous forests also requires special consideration when field data are being collected. In certain cases, for example when collecting Leaf Area Index (LAI), new sampling techniques need to be developed to account for the spatial and temporal heterogeneity of the forest. This is also the case if there are certain specific phenological patterns of interest. Both the scale of the sampling, as well as the technique should be determined by the required data. For example, biophysical parameters of the canopy such as LAI, vegetation fraction (VF) and the fraction of photosynthetically active radiation (f (fPAR) have been successfully linked to remotely sensed data in many studies in conifer stands, temperate broad leaf forests and agricultural fields (Chen and Black 1991; Price and Bausch 1995; Chen and Cihlar 1996; Chen et al. 1997). However, similar techniques have not been as thoroughly explored in tropical dry forest environments, nor is there a clear

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understanding of the impact of phenology in these important biophysical variables. In addition, with the exception of a few studies such as ArroyoMora (2002) or Clark (2002), optical remote sensing studies in tropical environments have been predominantly conducted with either the Landsat (TM and ETM+) or AVHRR sensors. However, high spatial resolution multispectral sensors such as IKONOS (4 and 1 m spatial resolution and four spectral bands) and Quickbird (2 m and 60 cm spatial resolution, four spectral bands) have begun acquiring substantial worldwide archives and can play a key role in monitoring phenological processes in tropical dry forest environments. Also, with the introduction of ASTER (15 m spatial resolution, 14 spectral bands) data can be obtained quite economically. All three of these sensors may be used to capture detailed temporal changes in the dry deciduous forest. In addition, ALI (Advanced Land Imager), a new sensor from the EO-1 platform provides a more cost effective alternative for acquiring Landsat-type data. Increased spectral resolution may also be an option to characterize deciduous forests from a remote sensing point of view. Hyperspectral sensors such as Hyperion (30 m spatial resolution and 220 spectral bands) or the airborne sensor HYDICE (1 m spatial resolution and 220 bands) offer new possibilities for describing the phenological changes in the deciduous forest, but their application will be limited to the short life span of this sensor type. More small changes at the canopy level can be observed with these sensors than can be captured by multispectral sensors. These changes can be correlated to ground measurements such as chlorophyll concentrations as a function of age and complexity in order to begin modelling the seasonal changes in the ecosystem in greater detail. Hyperspectral data sets will provide a greater range of possibilities for deriving indices that may be more sensitive to the vegetation characteristics, as well as to phenological changes in dynamic environments.

REFERENCES CITED Aide, T. M., Patterns of leaf development and herbivory in a tropical understory community, Ecology, 74, 455-466, 1993. Andren, H., and P. Angelstarn, Elevated predation rates as an edge effect in habitat islands, Ecology, 69, 544-547, 1988. Appanah, S., General flowering in the climax rain forest of Southeast Asia, Journal of Tropical Ecology,1, 225–240, 1985. Arroyo-Mora, P., Forest cover assessment, Chorotega Region, Costa Rica, Unpublished M.Sc. Thesis, Department of Earth and Atmospheric Sciences, University of Alberta, Canada, 2002.


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Ashton, P. S., T. J. Givnish, and S. Appanah, Staggered flowering in the Dipterocarpaceae: new insights into floral induction and the evolution of mast fruiting in the aseasonal tropics, The American Naturalist, 231, 44–66, 1988. Bierregaard, R. O., and T. E. Lovejoy, Effects of forest fragmentation on Amazonian understory bird communities, Acta Amazonica 19, 215-241, 1989. Borchert, R., Soil and stem water storage determine phenology and distribution of tropical dry forest trees, Ecology, 75, 1437–1449, 1994. Bullock, S. H., Plant reproduction in Neotropical dry forests, in Seasonally Tropical Forests, edited by H. A. Mooney, S. H. Bullock, and E. Medina, pp. 277-303, Cambridge University Press, Cambridge, UK, 1995. Cascante, A., M. Quesada, J. A. Lobo, and E. J. Fuchs, Effects of dry tropical forest fragmentation on the reproductive success and genetic structure of the tree, Samanea saman, Conserv. Biol., 16, 137-147, 2002. Castro-Salazar, R., and G. Arias-Murillo, Costa Rica: Toward the sustainability of its forest resources, Technical Report Fonda Nacional de Financiamiento Foresta (FONAFIFO), San Jose, Costa Rica, 1998. Chen, J. M., and T. A. Black, Measuring leaf area index of plant canopies with branch architecture, Agricult. Forest Met., 57, 1-12, 1991. Chen, J. M., and J. Chilar, Retrieving leaf area index of boreal forests using Landsat TM images, Remote Sens. Environ., 55, 153-162, 1996. Chen, J. M., P. M. Rich, S. T. Gower, J. M. Norman, and S. Plummer, Leaf area index of boreal forests: Theory, techniques and measurements, J. Geophys. Res. 102, 429-443, 1997. Clark, D., Applications of 1m and 4m resolution satellite imagery to studies of tropical forest ecology, management and secondary forest detection, in Tropical Forests: Past, Present, Future, p. 20, The Association of Tropical Biology Annual Meeting, Smithsonian Tropical Research Institute, 2002. Dirzo, R., and C. A. Dominguez, Plant-herbivore interactions in Mesoamerican tropical dry forests, in Seasonally dry tropical forests, edited by S. H. Bullock, H. A. Mooney, and E. Medina, pp. 277-303, Cambridge University Press, Cambridge, 1995. Doligez A., and H. Joly, Genetic diversity and spatial structure within a natural stand of a tropical forest tree species, Carapa procera (Meliaceae), in French Guiana, Heredity, 79,72-82, 1997. Eby, P., Seasonal movements of grey-headed flying-foxes, Pteropus poliocephalus (Chirpotera: Pteropodidae), from two maternity camps in northern New South Wales, Wildlife Research, 18, 547-559, 1991. Ewel, J., Natural systems as models for the design of sustainable systems of land use, Agroforestry Systems, 45, 1-21, 1999. Fanjul, L. and V.L. Barradas, Diurnal and seasonal variation in the water relations of some deciduous and evergreen trees of a deciduous dry forest of the western coast of Mexico, J. Appl. Ecol., 24, 289-303, 1987. Feinsinger, P., J. A. Wolfe, and L. A. Swarm, Island ecology: reduced hummingbird diversity and the pollination biology of plants on Trinidad and Tobago, West Indies, Ecology, 63, 494-506, 1982. Fleming, T. H., The short-tailed fruit bat: A study in plant-animal interactions, University of Chicago Press, Chicago, 365 pp., 1988. Fleming, T. H., R. A. Nuñez, and L. S. L. Sternberg, Seasonal changes in the diets of migrant and non-migrant nectarivorous bats as revealed by carbon stable isotope analysis, Oecologia, 94, 72-75, 1993.

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Flemming, T. H. and V. J. Sosa, Effects of nectarivorous and frugiviorous mammals on reproductive success of plants, J. Mammalogy, 75, 845-851, 1994. Frankie, G. W., H. G. Baker, and P. A. Opler, Comparative phenological studies of tress in a tropical lowland wet and dry forest sites of Costa Rica, J. Ecology, 62, 881-913, 1974. Frankie, G. W., S. B. Vinson, M. A. Rizzardi, T. L. Griswold, Diversity and abundance of bees visiting a mass flowering tree species in disturbed seasonal dry forest, Costa Rica, a Journal of the Kansas Entomological Society, 70, 281-296, 1998. Fuchs, E. J, J. A. Lobo, and M. Quesada, Effects of forest fragmentation and flowering phenology on the reproductive success and mating patterns on the tropical dry forest tree, Pachira quinata (Bombacaceae), Conserv. Biol., 17, 149-157, 2003. Gentry, A. H., Flowering phenology and diversity in tropical Bignoniaceae, Biotropica, 6, 6468, 1974. Gentry, A. H., Diversity of floristic composition of Neotropical dry forests, in Seasonally Tropical Forests, edited by H. A. Mooney, S. H. Bullock, and E. Medina, pp. 146-194, Cambridge University Press, Cambridge, UK, 1995. Haber, W. A. and G. W. Frankie, A tropical hawkmoth community: Costa Rican dry forest Sphingidae, Biotropica, 21, 155-172, 1989. Haber, W. A., and R. Stevenson, Diversity, migration, and conservation of butterflies in northern Costa Rica, in Biodiversity Conservation in Costa Rica: Learning the Lessons in a Seasonal Dry Forest, edited by G.W. Frankie, A. Mata, and S.B. Vinson, University of California Press, Berkeley, California, 2003. Hartshorn, G., and B. E. Hammel, Vegetation types and floristic patterns, in La Selva, Ecology and Natural History of a Neotropical Rain Forest, edited by L. McDade, K. S. Bawa, H. A. Hespenheide, and G. Hartshorn, pp. 73-89, University of Chicago Press, Chicago, 1994. Helversen, O. V., Adaptations of flowers to the pollination by Glossophaginae bats, Animalplant interactions in tropical environments, edited by W. Barthlott, pp. 41-49, Alexander Koenig Museum, Bonn, Germany, 1993. Heywood, V. H., G. M. Mace, R. M. May, and S. N. Stuart, Uncertainties in extinction rates, Nature, 368, 105, 1994. Holbrook, N. M., J. L. Witbeck, and H. A. Mooney, Drought responses of Neotropical dry forest trees, in Seasonally Tropical Forests, edited by H. A. Mooney, S. H. Bullock, and E. Medina, pp. 243-276, Cambridge University Press, Cambridge, UK, 1995. Holdridge L., Life Zone Ecology, Tropical Science Centre, San Jose, Costa Rica, 206 pp., 1967. Howe, H. F., Implications of seed dispersal by animals for tropical reserve management, Biological Conservation, 30, 261-281, 1984. Janzen, D. H., Synchronization of sexual reproduction of trees within dry season in Central America, Ecology, 21, 620–637, 1967. Janzen, D. H., Herbivores and the number of tree species in tropical forests, American Naturalist, 104, 501-528, 1970. Janzen, D. H., Reduction of seed predation on Bauhinia pauletia (Leguminosae) through habitat destruction in a Costa Rican deciduous forest, Brenesia 14/15, 325-336, 1978. Janzen, D. H., Costa Rica Natural History, University of Chicago Press, Chicago, 816 pp., 1983. Kalacska, M., G. A. Sánchez-Azofeifa, B. Rivard, P. Arroyo-Mora, R. Hall, J. Zhang, and K. Dutchak, Implications of phenological changes in the extraction of Mesoamerican Tropical Dry Forests through remote sensing: A case study from Costa Rica and Mexico, Proceedings of the International Conference, pp. 84-85, Wageningen University, The Netherlands, 2001.


135

Leemans, R., Global Holdridge Life Zone Classifications, Digital Raster Data, in Global Ecosystems Database Version 2.0, NOAA National Geophysical Data Center, Boulder, Colorado, 1992. Lemke, T. O., Foraging ecology of the long-nosed bat Glossophaga soricina with respect to food availability, Ecology, 65, 538-548, 1984. Lemke, T. O., Pollen carrying by the nectar-feeding bat Glossophaga soricina in a suburban environment, Biotropica, 17, 107-111, 1985. Levey, D. J., T. C. Moermond, and J. S. Denslow, Frugivory: an overview, in La Selva, Ecology and Natural History of a Neotropical Rain Forest, edited by L. McDade, K. S. Bawa, H. A. Hespenheide, and G. Hartshorn, pp. 282-294, University of Chicago Press, Chicago, 1994. Leopold, A. C., Photoperiodism in plants, Quarterly Review of Biology, 26, 247-263, 1951. Lobo, J. A., M. Quesada, K. E. Stoner, E. J. Fuchs, and Y. Herrerías-Diego, Latitudinal variation of phenological patterns of bombacaceous species in seasonal forests in Costa Rica and Mexico, Amer. J. Botany, (in press), 2003. Luttge, U., Physiological ecology of tropical plants, Springer-Verlag, Heidelberg, 384 pp., 1997. Marquis, R. J., Phenological variation in the Neotropical understory shrub Piper arieianum: causes and consequences, Ecology, 69, 1552-1565, 1988. Maass, J. M., Conversion of tropical dry forest to pasture and agriculture, in Seasonally Tropical Forests, edited by H. A. Mooney, S. H. Bullock, and E. Medina, pp. 399-422, Cambridge University Press, Cambridge, UK, 1995. Medina, E., Diversity of life forms of higher plants in Neotropical dry forests, in Seasonally Tropical Forests, edited by H. A. Mooney, S. H. Bullock, and E. Medina, pp. 221-242, Cambridge University Press, Cambridge, UK, 1995. Menaut, J. C., M. Lepage, and L. Abbadie L., Savannas, woodlands and dry forests in Africa, in Seasonally Tropical Forests, edited by H. A. Mooney, S. H. Bullock, and E. Medina, pp. 64-92, Cambridge University Press, Cambridge, UK, 1995. Mooney, H.A., S. H. Bullock, and E. Medina, Seasonally Tropical Forests, Cambridge University Press, Cambridge, UK, 450 pp., 1995. Murphy, P.G. and A. E. Lugo, Ecology of tropical dry forest, Annual Review of Ecology and Systematics, 17, 67-88, 1986. Murphy, P.G., and A. E. Lugo, Dry forests of Central America and the Caribbean, in Seasonally Tropical Forests, edited by H. A. Mooney, S. H. Bullock, and E. Medina, pp. 9-34, Cambridge University Press, Cambridge, UK, 1995. Murawski, D. A., J. L. Hamrick, S. P. Hubbell, and R. B. Foster, Mating systems of two bombacaceous trees of a Neotropical moist forest. Oecologia, 82, 501-506, 1990. Murawski, D. A., and J. L. Hamrick, Mating system and phenology of Ceiba pentandra (Bombacaceae) in Central Panama, J. Heredity, 83, 401-404, 1992. Murray, K. G., P. Feinsinger, W. H. Busby, Y. B. Linhart, J. H. Beach, P. Kinsman, Evaluation of character displacement among plants in two tropical pollination guilds, Ecology, 68, 1283–1293, 1987. Nason, J. D., and J. L. Hamrick, Reproductive and genetic consequences of forest fragmentation: two case studies of neotropical canopy trees, J. Heredity, 88, 264-276, 1997. Newstrom, L. E., G. W. Frankie, H. G. Baker, and R. K. Colwell, Diversity of long-term flowering patterns, in La Selva, Ecology and Natural History of a Neotropical Rain Forest, edited by L. McDade, K. S. Bawa, H. A. Hespenheide, and G. Hartshorn, pp. 142160, University of Chicago Press, Chicago, 1994.

136


Opler, P. A., G. W. Frankie, and H. G. Baker, Rainfall as a factor in the release, timing, and sychronization of anthesis by tropical tress and shrubs, J. Biogeography, 3, 231-236, 1976. Piperno, D. R., and D. M. Pearsall, Origins of Agriculture in the Neotropics, Academic Press, New York, 400 pp., 2000. Price, J. C., and W. C. Bausch, Leaf area index estimation from visible and near-infrared reflectance data, Remote Sens. of Environ., 52, 55-65, 1995. Quesada, M., K. E. Stoner, V. Rosas-Guerrero, C. Palacios-Guevara, and J. Lobo, Effects of habitat disruption on the activity of nectarivorous bats (Chiroptera: Phyllostomidae) in a dry tropical forest: implications for the reproductive success of the neotropical tree Ceiba grandiflora, Oecología, 135, 400-406, 2003. Ratter, J.A., P. W. Richards, G. Argent, and D. R. Gifford, Observations of the vegetation of northeastern Mato Frosso. I. The woody vegetation types of the Xavantina-Cachimbo expedition area, Philosophical Transactions of the Royal Society of London, Series B, 266, 449-492, 1973. Reich, P. B. and R. Borchert, Water stress and tree phenology in a tropical dry forest in the tropical dry forest lowlands of Costa Rica, J. Ecology, 72, 61-74, 1984. Robertson, C., The philosophy of flower seasons, and the phenological relations of the entomophilous flora and the anthophilous insect fauna, American Naturalist, 29, 97-117, 1895. Rolstad, J., Consequences of forest fragmentation for the dynamics of bird populations: Concelptual issues and the evidence, Biological Journal of the Linnean Society, 42, 149163, 1991. Sader, S., and A. T. Joyce, Deforestation rates and trends in Costa Rica, 1940 to 1983, Biotropica, 20(1), 11-19, 1988. Sakai, S., K. Momose, T. Yumoto, T. Nagamitsu, H. Nagamasu, A. A. Hamid, and T. Nakasiiizuka, Plant reproductive phenology over four years including an episode of general flowering in a lowland Dipterocarp forest, Sarwak, Malaysia, Amer. J. Botany, 86, 1414–1436, 1999. Sanchez-Azofeifa, G.A. and Calvo J., Final report on the extent to Costa Rica forest cover: Year 2002, Costa Rican National Forest Financing Fund, 20 pp., 2002. Saunders, P. A., Jr., R. J. Hobbs and C. R. Margules, Biological consequences of ecosystem fragmentation: a review, Conservation Biology, 5, 18-32, 1991. Stephenson, A. G., The role of extrafloral nectaries of Catalpa speciosa in limiting herbivory and increasing fruit production, Ecology, 63, 663-669, 1982. Stiles, G. F., Ecology, flowering phenology, and hummingbird pollination of some Costa Rican Heliconia species, Ecology, 56, 285–301, 1975. Stiles, G. F., Coadapted competitors: the flowering seasons of hummingbird-pollinated plants in a tropical forest, Science, 198, 1177-1178, 1977. Stoner, K. E., Seasonal changes in abundance of tropical dry forest frugivorous and nectarivorous bats in northwestern Costa Rica, Canadian Journal of Zoology, 79, 16261633, 2001. Stoner, K. E., M. Quesada, V. Rosas-Guerrero, and J. A. Lobo, Effects of forest fragmentation on Colima long-nosed bat foraging in tropical dry forest in Jalisco, Mexico, Biotropica, 34, 462-467, 2002. Stoner, K. E., O. Salazar, K. A., R. C. Fernández,, and M. Quesada Population dynamics, reproduction, and diet of the lesser long-nosed bat ((Leptonycteris curasoae) in Jalisco, Mexico: implications for conservation, Biodiversity and Conservation, 12, 357-373, 2003.


137

Tallak Nilsen, E., and W. H. Muller, Phenology of the drought-deciduous shrub Lotus scoparius: climatic controls and adaptive significance, Ecological Monographs, 51, 323– 341, 1981. Trejo, I., and R. Dirzo, Deforestation of seasonally dry tropical forest: a national and local analysis in Mexico, Biological Conservation, 94, 133-142, 2000. van der Meer, F., Physical Principals of Optical Remote Sensing, in Spatial Statistics for Remote Sensing (Remote Sensing and Digital Image Processing Vol. 1), edited by A. Stein, F. van der Meer, and B. Gorte, pp. 27-40, Kluwer Academic Publishers, New York, 1999. van Schaik, C. P., Phenological changes in a Sumatran rain forest, Journal of Tropical Ecology, 2, 327–347, 1986. van Schaik, C. P., J. W. Terborgh, and S. J. Wright, The phenology of tropical forests: Adaptive significance and consequences for primary consumers, Annual Review of Ecology and Systematic, 24, 353–377, 1993. Walter, H., Ecology of tropical and subtropical vegetation, Oliver and Boyd, Edinburgh, 539 pp., 1971. Williams-Linera, G., Phenology of deciduous and broad leaf evergreen tree species in a Mexican tropical lower montane forest, Global Ecology and Biogeography Letters, 6, 115127, 1997. Whitmore, T. C., and J. A. Sayer, Deforestation and species extinction in tropical moist forests, in Tropical deforestation and species extinction, edited by T. C. Whitmore and J. A. Sayer, pp. 1-14, Chapman and Hall, London, 1992. Wright, S. J., Seasonal drought and the phenology of shrubs in a tropical moist forest, Ecology, 72, 1643-1657, 1991. Wright, S. J., and C. P. van Schaik, Light and the phenology of tropical trees, The American Naturalist, 143, 192–199, 1994. Wright, S. J., and F. H. Cornejo, Seasonal drought and leaf fall in a tropical forest, Ecology 71, 1165–1175, 1990. Zimmerman, J. K., D. W. Roubik, J. D. Ackerman, Asynchronous phenology of a neotropical orchid and its euglossine bee pollinators, Ecology, 70, 1192–1195, 1989.

Chapter 3.2 MEDITERRANEAN CLIMATES Donatella Spano1, Richard L. Snyder2, and Carla Cesaraccio3 1

Department of Economics and Woody Plant Ecosystems, University of Sassari, Sassari, Italy; 2Department of Land, Air, and Water Resources, University of California, Davis, CA, USA; 3Agroecosystem Monitoring Laboratory, Institute of Biometeorology, National Research Council, Sassari, Italy

Key words:

Mediterranean ecosystems, Drought, Temperature, Climate variability, Plant communities

1.

MEDITERRANEAN CHARACTERISTICS

1.1

Zones

Mediterranean-type ecosystems are found in the far west regions of continents between 30° and 40° north and south latitude (Figure 1). They cover about 2.73 million km2 (IUCN 1999), with the majority (i.e., 73%) of the ecosystem in the Mediterranean Basin including parts of Spain, Turkey, Morocco, and Italy (Rundel 1998). Areas are also found in California, Chile, Southwest and Southern Australia, and South Africa. In response to the climate, similar woody, shrubby plants, with evergreen sclerophyll leaves, have developed in communities of varying density. The names for the shrub vegetation vary by region because of language and plant structure. Common names for the vegetation include: maquis and garrigue in the Mediterranean Basin, chaparrall in California, matorrall in Chile, fynbos or renosterveldd in South Africa, and mallee (kwongan or heathlands) in Australia.

Schwartz (ed.), PHENOLOGY: AN INTEGRATIVE ENVIRONMENTAL SCIENCE, 139-156 © 2003 Kluwer Academic Publishers. Printed in the Netherlands.

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1.2


Climate

Mediterranean ecosystems formed as a result of the unique climate, which falls in a transition between dry, tropical and temperate zones. The

Figure 3.2-1. Geographical distribution of Mediterranean-type ecosystems.

main characteristics are (1) variable winter rainfall, (2) summer droughts of variable length, (3) intensive summer sunshine, (4) mild to hot summers, and (5) cool to cold winters. Commonly, there is a cold ocean current off the West coast of regions with a Mediterranean climate that strongly influences the weather. The range of summer and winter temperatures mainly depends on proximity to the ocean (or sea) with higher temperatures near the coast during cooler periods and higher temperatures inland during warmer periods. Temperatures also vary with elevation having consistently cooler temperature in the mountains. Excluding mountains, the annual precipitation range at lower elevations typically varies between 250-900 mm with most falling in the winter and spring (i.e., November – April in the Northern Hemisphere and May – October in the Southern Hemisphere). Westerly winds over cold ocean currents often lead to heavy marine fog that maintain low temperatures on the coast during summers. In the winter, the coastal areas tend to be fog free, whereas inland valleys that receive winter rainfall are prone to high-inversion, radiation fog. Differences in relative humidity are mainly related to temperature variations over the zone rather than absolute humidity. The Mediterranean climate is dominated by westerly winds over the ocean, so the water vapor pressure (or dew point temperature) tends to be similar over most of the zone.

Chapter 3.2: Mediterranean Climates

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The five Mediterranean zones have similar characteristics, but there are important differences within each of the regions. Differences within a region are mainly related to the length of the summer drought period, which generally decreases as one moves poleward. For example, di Castri (1973, 1981) described a six-zone climate classification based on the length of drought period after Emberger (1962), as shown in Table 1. Table 3.2-1. Climate classification based on length of summer drought period. Classification Drought Period (months) Perarid Arid Semiarid Subhumid Humid Perhumid

1.3

11-12 9-10 7-8 5-6 3-4 1-2

Soil

Soil and climate both influence the development of natural vegetation, so a short discussion of soils is included here. More extensive discussions are presented by Thrower and Bradbury (1973), Zinke (1973), and di Castri et al. (1981). Most Mediterranean soils exhibit (1) considerable erosion, (2) alluvial deposition, (3) limited profile development, and (4) decreased soil development with increasing elevation. Because limestone is deficient in some areas, most soils often tend to have water infiltration problems. Due to the lower precipitation, parent materials weather slower in Mediterranean zones than in more humid regions. Because of seasonal drying some soils are dominated by invertization processes and produce Vertisols. The soils tend to vary from reddish to brownish with increasing elevation. Higher precipitation and cooler temperatures at higher elevations have led to the development of predominant brownish podzolic soils with higher organic matter and moderate lime accumulations at middle elevations (500-1000 m). At lower elevations (0-500 m) with less precipitation and higher temperature, the older terra rossa soils, having lower organic matter and a reddish color due to iron oxidation, developed from limestone. In the river valleys, alluvial soils are found as highly weathered soils in terraces, light and well-drained in alluvial fans, and heavy and poorly drained in the valley floors. In some valley basins, fine textured soils have greatly inhibited drainage. In many areas within Mediterranean zones, older paleosoils, which were formed under different climate conditions, are prevalent.

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2.

VEGETATION TYPES

2.1

Structure

Although the Mediterranean climate developed relatively recently over a small part of the Earth’s land surface, the distinctive flora have evolved with similar characteristics in widely different parts of the world. The climate is similar in each of the five zones, but, within a small area of a Mediterranean ecosystem, high heterogeneity in plant communities is common. This heterogeneity developed because of large variations in landforms, microclimate, soils, phyllogenetic origin, evolutionary strategy, ecological tolerance, and land use within the ecosystem. The appearance of natural vegetation and landscape forms is strikingly similar between the five Mediterranean zones. The shrubland plants are woody, shrubby, and evergreen. The plant leaves tend to be small, broad, stiff, thick, and waxy or oily. In some locations, there are small trees with or without an understory of annual and herbaceous perennials. The vegetation represents different successional stages in relation to climate, topographical features, and human impact (di Castri 1981), and it is prone to wildfires. di Castri (1981) presented a classification of the six Mediterranean (summer drought based) climate types (Table 1) and provided information on the structure of vegetation in each of the climate types. He noted that there were several overlapping clusters of characteristics between all five regions. However, the similarities between vegetation structures were most apparent between California and Chile, and between Australia and South Africa.

2.2

Floristic Composition

Mediterranean ecosystems have large species diversity including about 48,250 plant species, which is approximately 20% of the world total (Cowling et al. 1996). The Mediterranean Basin, South Africa, Southwestern Australia, and California have about 25,000; 8550; 8000; and 900 species, respectively (Archibold 1995; Rundel 1998). The Mediterranean Basin is mainly covered by scrub, sparse grass, or bare rock. However, there are scattered evergreen trees that suggest earlier presence of mixed forests. Several species of Quercus including the holm oak (Quercus ilex) prevail in the west with cork oak (Q. suber) dominant on non-calcareous soils. Arbutus unedo and other shrubs are found in the same plant communities. As the climate becomes more arid to the east, Kermes oak (Q. coccifera) becomes more prevalent than holm oak. Stone pine ((Pinus pinea), cluster pine (P. ( pinaster), and Aleppo pine (P. ( halepensis) are


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common at higher elevations in the west. In the drier eastern region (e.g., Syria, Lebanon, and Israel), Q. calliprinos, an evergreen oak, and deciduous oaks are common. Corsican pine (P. nigra) and P. brutia often dominate in locations where wildfires occurred. Q. ilex is also found on the Atlas Mountains of North Africa at the elevation of 2000 m. Shrublands are divided into maquis, which comprises evergreen shrubs and small trees about 2.0 m tall, garrigue on calcareous soils, and jarall on siliceous soils. All communities have representative species and the size depends on local conditions. South African sclerophyll plant communities include mountain and coastal types (Moll et al. 1984). The mountain fynbos mainly consists of broad-leaved proteoid shrubs, which are found at elevations up to about 1000 m and grow to heights between 1.5-2.5 m. At higher elevations, 0.21.5 m tall ericoid shrubs are dominant. In addition, 0.2-0.4 m tall shrubs and tussocky hemicryptophytes are present in the high elevation communities. Tussocky restioid shrubs, which reach 0.3 m, dominate communities at higher elevations. In arid, high-elevation regions, the vegetation is mainly karoo with abundant succulent forms. An open ericoid cover with shrubs growing to 1.0 m tall, dominates the west coast. Small shrubs, grasses, and annuals form an open heath with 1-2 m tall proteoids along the south coast. Western Australia is dominated by forests of karri (Eucalyptus ( diversicolor) and jarrah (E. marginata). Karri is restricted to regions with acidic soils (Rossiter and Ozanne 1970) and it grows in association with other tall eucalyptus. Casuarina decussata and species of Banksia are common in the understory of these forests. Jarrah forests occur on lateritic soils in areas with lower precipitation. These forests change to wandoo (E. rudunca) woodland as the annual precipitation decreases. The western region is separated from South Australia by the acacia shrubland. Mallee is the dominant cover in the southeastern Mediterranean zone. The prevalent species are E. diversifolia and E. incrassata. In more favorable sites, species such E. behriana grow with ground cover of herbs and grasses with few sclerophyllous shrubs (Specht 1981). These communities integrate with sclerophyll forests of stryngbark (E. baxteri) and messmate (E. ( obliqua). The Chilean matorrall communities occur in the coastal lowlands and on the west facing slopes of the Andes. Most matorrall species are 1-3 m tall, evergreen shrubs with small sclerophyllous leaves. Many spinescent species and drought-deciduous shrubs are also important in these regions (Rundel 1981). Salix chilensis, Cryptocarya alba, and other trees are found in wetter regions with shrubs forming a cover. Matorrall evergreen shrubs (e.g., Lithaea caustica and Quillaja saponaria) dominate coastal regions. In more arid locations, succulent species and Fluorensia thurifera are common. The

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central valley of Chile is dominated by Acacia caven (Ovalle et al. 1990, 1996). California chaparrall typically consists of a dense cover of 1-4 m tall, evergreen shrubs. In California, and particularly in the south, chamise ((Adenostoma fasciculatum) is common and California lilac (Ceanothus cuneatus) is sometimes associated. In the Sierra Nevada foothills, chaparral occurs above 500 m elevation. Pure stands of California lilac are considered a fire-successional form in Southern California, but it is a dominant species of chaparrall in Northern California (Hanes 1981). Manzanita ((Arctostaphylos spp.) occurs throughout California, especially where there is snow and temperatures drop below freezing in winter. Various Quercus species may be present on lower hillsides. Coastal sage scrub (e.g., Artemisia californica) is the main vegetation along the coast.

2.3

Environmental Effects

Common characteristics of Mediterranean zones are summer drought, fire, tectonic instability, and variable floods and erosion during winter. Perhaps the most important of these is summer drought; however, drought tends to be more severe in California, Chile, and the subarid region of the Mediterranean Basin (Rundel 1995, 1998). In fact, the Mediterranean climate exhibits extreme year-to-year variability. In the last century, the rainfall trends have been relatively consistent showing a general decrease and similar or more intense tendency is expected in the future (Cubasch 2001; IPCC 2001). Dense cover and high woody biomass of shrublands make them prone to wildfire, which is an important disturbance regime in Mediterranean climates. Frequency of natural wildfire differs greatly between and within Mediterranean zones (Mooney and Conrad 1977; Rundel 1981, 1983; Trabaud and Prodon 1993; Oechel and Moreno 1994) depending on many factors. Anthropogenic disturbance is one of the biggest factors affecting Deforestation, grazing, agricultural Mediterranean ecosystems. development, and fire starting and suppression have changed vegetation community structure, especially in recent decades. One of the main factors is deforestation, in order to permit more intensive agriculture. Increased urbanization and land abandonment has led to uneven management and greater frequency and extent of wildfire as a disturbance (Rundel 1998). Fire is a natural disturbance in Mediterranean ecosystems, and the vegetation has adapted. However, the frequency and intensity of wildfires increased dramatically in the last few decades (Rundel R 1998). This has led to reduced forest vigor and degradation of forest structure and soil stability (Kuzucuoglu 1989; Naveh 1990).


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Grazing of livestock has greatly influenced Mediterranean ecosystems. A good example is in California, where livestock grazing converted much of the grassland from native perennials to exotic annuals from the Mediterranean Basin even prior to immigration by large numbers of people of European ancestry (Rundel 1998). In the late 1800s, agricultural expansion into the central valley and southern California caused extensive changes in natural communities. Later, agricultural and urban expansion led to large changes in vegetation along the coast. Human activities influenced grassland and oak woodlands of the State mainly by replacing native perennial grasses with introduced annual grasses from Europe. Native Americans purposely set fires to control vegetation, but European immigrants introduced fire suppression as a management strategy in the late 1800s. This change in management has led to fewer but more intense wildfires (Minnich 1983; Rundel and Vankat 1989). When Spanish settlers arrived in Chile in the mid-1500s, they introduced grazing and agriculture that greatly changed the natural ecosystems. The impact is most obvious in the semi-arid transition region where over-grazing has caused devegetation and desertification (Ovalle et al. 1990, 1996). Also, much of the central valley now is covered with exotic annual grasses rather than the native grasses (Gulmon 1977). Recently, Chile has become more urban and there has been an abandonment of farms and ranches as the population leaves rural areas. This has led to a big increase in mainly anthropogenic wildfires that have grown in size and intensity. Even more recently, the planting of winegrape vineyards has expanded dramatically in Chile and in California at the expense of native woodlands (Rundel 1998). Agricultural development in Southwest Australia has resulted in widespread fragmentation of mallee ecosystems mixed in with agricultural lands (Rundel 1998). The fragmented habitats tend to be too small to maintain viable plant populations, which are also impacting on animal diversity. Deforestation is a big problem in native eucalypt forests, and the resulting rise in water tables has led to problems with saline paleosoil profiles (Rundel 1998), which threatens agriculture as well as the replanting of forests. The introduction of exotic species has resulted in problems with biological diversity in the Mediterranean climate zones. Anthropogenic impacts on the Mediterranean ecosystems in South Africa are less obvious than in the other regions to a large extent because the soils of the region are not conducive to support cereal and vegetable production (Rundel 1998). However, large animal hunting and deforestation have impacted on the vegetation. There has been a large introduction of nonnative trees, especially Australian acacias along rivers and streams.

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3.

PHENOLOGY IN THE MEDITERRANEAN CLIMATE

3.1

An Overview of Past Studies

Mediterranean regions show seasonal changes in resource availability, which affect growth and reproductive activities of vegetation. Resource fluctuations have a strong influence not only on the structure and composition of the vegetation but also on the seasonal behavior pattern of the species. For example, the sclerophyllous forest can remain active throughout the year, but there is a distinct annual growth rhythm because photosynthesis is limited by a variety of environmental and physiological constraints (i.e., drought and nutrients). However, several other species shed leaves during summer drought period. Over the last three decades, the economic, ecological, and cultural value of Mediterranean vegetation has been increasingly recognized (Quezel 1977) and many studies were devoted to improving management and protection of Mediterranean areas. In particular, there has been comparative research on the structure of Mediterranean region ecosystems, which included a detailed assessment of phenological species behavior in the different areas. The first systematic study on Mediterranean vegetation was presented by Mooney et al. (1977) within the International Biological Program (IBP), which started in 1970. The authors summarized the results of the comparison of the structural, functional, and evolutionary features of California and Chile ecosystems. At the plant community level, there is a longer protraction of each phenological event in Chile than in California due to both the greater diversity of growth form and more moderate climate in Chile (Mooney et al. 1977). In addition, di Castri (1981) pointed out that there were more species with non-overlapping phenological activities in Chile. As more information on the phenology of ecosystems in the Mediterranean Basin, South Africa and Australia became available, it was noted that there is a pronounced seasonal rhythm in the vegetative growth throughout the year in Mediterranean regions. However, less similarity in phenological pattern was found when comparing Chile, California, and Mediterranean Basin with South Africa and Australia. In South Africa and Australia, shrubs grow in the summer as well as in the spring (Cody and Mooney 1978) because of differences in origin of the biota (Specht 1973) and nutrient availability in the soils (Specht 1979, 1981). Comparative analysis of Mediterranean species development was intensified during the 1980s with more emphasis on the interactions between temperature and water as limiting factors. Tenhunen et al. (1987) summarized the results of years of cooperative work between several


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scientists on functional analysis in Mediterranean ecosystems. The work included recent studies on plant growth and development. Montenegro (1987) discussed the difficulty in comparing these ecosystems because of different methodologies used to quantifying phenology and growth. In Portugal, phenological observations conducted on different species (Quercus coccifera and Q. suber, Arbutus unedo, and Cistus salvifolius) showed that flowering stage occurred during all times of the year except the driest months in late summer and the coldest months in winter. Shoot growth was intense in the absence of water stress, and leaf drop was possibly more intense during drought (Pereira et al. 1987). Similar results were obtained on Q. coccifera and Arbutus unedo in Greece (Arianoutsou and Mardilis 1987), although the responses to the physical environment were not synchronous for the two species. Moll (1987) observed that the differences between vegetation in South Africa and in other Mediterranean regions reported by Mooney and Kummerow (1981) were mostly due to the fact that they compared non-heath shrubland in Chile, California, and the Mediterranean Basin with heath shrubland in South Africa. In the last decade, more attention was directed to the relationship between phenological events and seasonal fluctuations in nutrient and water uptake. A phenological survey conducted in central Italy (de Lillis and Fontanella 1992) showed the effect of increasing water stress and nutrient content on several species (Cistus monspeliensis, Pistacia lentiscus, Calicotoma villosa, Quercus ilex, Erica arborea, Arbutus unedo, Phillyrea media, Smilax aspera, and Ruscus aculeatus). Phenological rhythm of the community was closely correlated with changes in environmental conditions, and large variation occurred among species. In all species, peak growth was reached between March and early July, flowering occurred before July except A. unedo and S. aspera, which flowered in autumn and winter, and fructification was unrelated to summer aridity. An analysis of water availability and growth modulation allowed for division into droughttolerant species ((Pistacia lentiscus, Phillyrea media, Arbutus unedo, and Ruscus aculeatus), drought deciduous species (Calicotoma villosa), and semi-deciduous species (Cistus monspeliensis). Carbon leaf concentration peaked and nitrogen decreased when growth stopped. Correia et al. (1992) compared the phenological characteristics of four summer semi-deciduous (species of Cistus) and evergreen ((Pistacia lentiscus) shrubs in Portugal, corresponding to earlier and later successional stages of vegetation. The Cistus species were similar in growth, flowering, and fruiting phenology, showing a long period of leaf emergence relative to P. lentiscus, which had a flush-type leaf emergence and an almost simultaneous leaf fall. In general, Pistacia showed lower leaf nitrogen contents than the Cistus species, with minimum value in winter, when the Cistus species had the highest

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concentrations of nitrogen. However, increased drought frequency and intensity, is likely to greatly affect phenology of these species in the future.

3.2

Phenology and Drought

Many researchers have reported studies on the phenology of various Mediterranean species; however, little information was presented on the relationship between phenological stage occurrence and duration and intensity of drought period. Because the Mediterranean climate is highly variable and there are emerging problems of water scarcity, Spano et al. (1999) reported phenological observations of native and exotic species, on the island of Sardinia, with an emphasis on the impact of drought on phenology. They recorded weekly phenology observations for a period of 11 years on the common species Pistacia lentiscus, Olea europea, Myrtus communis, Quercus ilex, Spartium junceum, and Cercis siliquastrum, and on the exotic species Robinia pseudoacacia, Salix chrysocoma, and Tilia cordata. The climate during the study and the historical averages for 19511981 (Figure 2) show that the temperatures were similar, but there was markedly less winter rainfall during the observation period from 1986-1996. The canopy drought stress index CDSI (Baldocchi 1997) was calculated to look at differences in evaporative demand and precipitation between years. The CDSI is the ratio of cumulative precipitation and cumulative reference evapotranspiration. The range of phenological event dates for the nine species varied widely (Figure 3), especially for flowering of the exotic species. The authors showed that difference in accumulated degree-days could not explain the variations in observed phenological development. Regardless of the CDSI, during the winter and spring, there seemed to be little difference in the flowering dates of common species. However, the non-native species Salix chrysocoma and Tilia cordata showed more interannual variability and both exhibited later flowering when there was more rainfall during March (i.e., prior to flowering). There was no relationship with rainfall recorded two or more months prior to flowering. With the purpose to investigate the effects of temperature, rainfall, and evapotranspiration variability on phenology, Duce et al. (2000) conducted phenological observations on three maquis species and oak trees over the period 1997 to 1999 at Giara di Gesturi, a nature reserve located in Southern Sardinia, Italy. About 46% oak trees (Quercus suber) and about 32% successional Mediterranean maquis with four dominant species ((Arbutus unedo, Pistacia lentiscus, Phillyrea angustifolia, and Myrtus communis) cover the reserve. In Figure 4, daily rainfall amount and occurrence dates of flowering and full ripe fruit of Quercus suberr and Pistacia lentiscus are shown for 1997 and 1998. Flowering and full ripe fruit stages occurred


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about 1 month later in 1997 for both species. Sensitivity of the two species seemed to be related to rainfall distribution and the onset and duration of water deficit. In 1997, both species were affected by the lack of spring rainfall, which led to a longer and more intense drought period. Moreover, Duce et al. (2002) studied the effect of temperature and water availability on the flowering date of several natural species growing in Sardinia, Italy to explain year-to-year variation of the flowering data. The results showed a large variation by species in terms of observed flowering

Figure 3.2-2. Climate diagram (Walter and Lieth 1967) for Oristano, Italy for 1951-1981 (upper graph) and for 1986-1996 (lower graph).

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Figure 3.2-3. Range of dates of flowering ( ), full ripe fruit ( ), and leaf drop ( nine species growing in Oristano, Italy during the period 1986-1996.

) for

Figure 3.2-4. Daily precipitation and dates for flowering and full ripe fruit in 1997 (upper graph) and 1998 (lower graph) for Quercus suberr L. (Q) and Pistacia lentiscus L. (P) at Giara di Gesturi, Sardinia, Italy.


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dates and cumulative degree-day values, indicating that other factors in addition to heat units affected plant development. A significant factor in the prediction of flowering dates was obtained by adjusting the degree-day model for accumulated precipitation from the period when available soil water content was at maximum to the earliest flowering date typical of each species. In general the flowering date was postponed when the soil water was not limiting and flowering occurred earlier during drought years.

3.3

Phenology and Climate Change

During the 21st century, there will be more concern about climate change and especially drought in Mediterranean regions. In the past century, the overall global warming was about 0.5°C (IPCC 1996; Nicholls et al. 1996; IPCC 2001). Temperature records for Mediterranean areas show similar trends (Rambal and Hoff 1998). However, it is more difficult to see definite trends in rainfall patterns. Le Houèrou (1996) reported that there were no changes in rainfall patterns in Europe. However, Gregory and Mitchell (1995) showed that the regionally averaged total annual rainfall increased at latitudes greater than 45°N, and decreased at middle latitudes (35–40°N) with a decrease in the number of rain-days. Climate variation and change will likely occur at a number of scales in time and space, influencing plant physiology, competition between species, and global distribution of major ecosystems (Lindner et al. 1997). Several investigations were conducted on the impacts of climate change on different forest ecosystems, mainly focusing on the eco-physiological level (Mooney et al. 1991; Lindner et al. 1997). However, there is a lack of information on the potential effects of climate variability and change on Mediterranean forests. In Mediterranean climates, where the structural and functional f characteristics of ecosystems are determined by annual variability of temperature and precipitation, plant response to climate change is a crucial aspect of monitoring programs (Hope 1995). Several papers have presented the possible effects of changing climate factors (i.e., temperature and water availability) on the growth of forest ecosystems. Kramer et al. (2000) presented models simulating physiological features of the annual cycle for boreal coniferous, temperate-zone deciduous, and Mediterranean forest ecosystems. The phenology was mainly water driven and the ecosystem was a maritime pine forest (Pinus ( pinaster) located in southern France. The phenological models were coupled with the process-based forest growth model FORGRO (Mohren 1987, 1994; Kramer 1995) to evaluate the effect of different climate change scenarios. The study confirmed that phenology is mainly affected by seasonality in water availability. A dry year influences the growth of conifers for several years

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because both initiation and elongation of needles are affected by the availability of water, and the phenology of each of the forest types shows growth responses to a given climate change scenario. Recently, Peñuelas et al. (2002) compared phenological data from 1952 and 2000 providing a complete record of abundant plant and migratory birds species and a common butterfly. The data were collected in Catalonia, Spain. A conservative linear treatment of data showed that, in 2000, leaves unfolded on average 16 days earlier, leaf fall occurred about 13 days later, and plants flowered an average of six days earlier than in 1952. In addition, fruiting occurred about nine days earlier in 2002 than in 1974. Butterflies appeared 11 days earlier and spring migratory birds arrived 15 days later than 1952. The biggest change in both temperature and phenophase timing occurred in the last 25 years. The observed phenological changes, among the different species, may alter their competitive ability, ecology, and conservation, as well as the structure and functioning of the ecosystem.

4.

CONCLUSIONS

There are five Mediterranean zones around the world that are located near the west coasts of continents between 30o and 40o latitude. The climate represents a unique transition between arid zones towards the equator and temperate zones poleward. It is characterized by cold to cool, wet winters and warm to hot summers with varying periods of drought. The vegetation is similar in each region with woody, shrubby, and evergreen shrubland plants, sparse grass, scattered evergreen trees, and many species of oak trees. In all zones, anthropogenic disturbances including deforestation, grazing, agricultural development, and fire starting and suppression have changed the vegetation community structure. In general, phenology in the five Mediterranean zones presents a pronounced seasonal rhythm related to vegetation and environmental characteristics, with large variation among species. Whereas heat unit accumulation is the main factor affecting phenology of well-watered plants, phenology of natural Mediterranean vegetation is influenced by drought and plant nutrition in addition to heat units. Climatic fluctuations and drought in particular, directly influence resources availability and indirectly phenology. Like other climate regions, more research is needed to better understand the interaction between weather factors and phenology.


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REFERENCES CITED Archibold, O. W., Ecology of World Vegetation, Chapman and Hall, London, 510 pp., 1995. Arianoutsou, M., and Th. A. Mardilis, Observations on the phenology of two dominant plants of the Greek maquis, in Plant Response to Stress: Functional Analysis in Mediterranean Ecosystems, vol. 15, edited by J. D. Tenhunen, F. M. Catarino, O. L. Lange, and W. C. Oechel, NATO Adv. Sci. Inst. Ser. G Ecol. Sci., pp. 515-519, Springer-Verlag, Berlin, Heidelberg, 1987. Baldocchi, D., Measuring and modelling carbon dioxide and water vapour exchange over a temperate broad–leaved forest during the 1995 summer drought, Plant, Cell and Environ., 20, 1108–1122, 1997. Cody, M. L., and H. A. Mooney, Convergence versus non-convergence in Mediterraneanclimate ecosystems, Annu. Rev. Ecol. Syst., 9, 265-321, 1978. Correia, O. A., A. C. Martins., and F.M. Catarino, Comparative phenology and seasonal foliar nitrogen variation in mediterranean species of Portugal, Ecol. Mediterranea, 18, 7-18, 1992. Cowling, R. M., P. W. Rundel, B. B. Lamont, M. K. Arroyo, and M. Arianoutsou, Plant diversity in Mediterranean-climate regions, Trends Ecol. Evol., 11, 352-360, 1996. Cubasch U., G. A. Meehl, G. J. Boer, R. J. Stouffer, M. Dix, A. Noda, C. A. Senior, S. Raper, and K. S. Yap, Projections on future climate change, in Climate Change 2001: The Scientific Basis, Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change, edited by J. T Houghton, Y. Ding, D. J. Griggs, M. Noguer, P. van der Linden, X. Dai, K. Maskell, C. I. Johnson, pp. 526-582, Cambridge University Press, Cambridge, 2001. de Lillis, M., and A. Fontanella, Comparative phenology and growth in different species of the Mediterranean maquis of central Italy, Vegetatio, 99-100, 83-96, 1992. di Castri, F., Climatographical comparison between Chile and the Western Coast of North America, in Mediterranean Type Ecosystems, Origin and Structure, edited by F. di Castri and H.A. Mooney, pp. 21-36, Springer-Verlag, Berlin, Heidelberg, 1973. di Castri, F., Mediterranean-type shrublands of the world, in Ecosystems of the world. Mediterranean-type shrublands, vol. 11, edited by F. di Castri, D. W. Goodall, and R. L. Specht, pp 1-45, Elsevier Scientific Publishing Company, Amsterdam, 1981. di Castri, F., D. W. Goodall, and R. L. Specht, Ecosystems of the world: Mediterranean-type shrublands, vol. 11, Elsevier Scientific Publishing Company, Amsterdam, 643 pp., 1981. Duce, P., C. Cesaraccio, D. Spano, and R. L. Snyder, Weather variability effect on phenological events in a Mediterranean-type climate, paper presented at 15th Conference on Biometeorology / Aerobiology and 16th International Congress of Biometeorology, Kansas City, USA, 2002. Duce, P., D. Spano, C. Asunis, C. Cesaraccio, C. Sirca, and A. Motroni, Effect of climate variability on phenology and physiology of Mediterranean vegetation, paper presented at 3rd European Conference on Applied Climatology, Pisa, Italy, 2000. Emberger, L., Comment comprendre le territoire phytogéographique méditerranéen francaiú et la position “systématique” de celui-ci. Nationalia Monspeliensia. Série Botanica, 14, 47-54, 1962. Gregory, J. M., and J. F. B. Mitchell, Simulation of daily variability of surface temperature and precipitation over Europe in the current and 2xCO2 climates using the UKMO climate model, Q. J. R. Meteorol. Soc, 121, 1451-1476, 1995. Gulmon, S. L., A comparative study of grasslands of California and Chile, Flora, 166, 261278, 1977.

154


Hanes, T. L., California Chaparral, in Ecosystems of the world: Mediterranean-type shrublands, vol. 11, edited by F. di Castri, D. W. Goodall, and R. L. Specht, pp. 139-174, Elsevier Scientific Publishing Company, Amsterdam, 1981. Hope, A. S., Monitoring ecosystem response to global change: high spatial resolution digital imagery, in Ecological Studies: Global change and Mediterranean-type ecosystems, vol. 117, edited by J. M. Moreno, and W. C. Oechel, pp. 43-85, Springer-Verlag, New York, 1995. Intergovernmental Panel on Climate Change, Climate change 1995: The Science of Climate Change, edited by J. E. Houghton, L. G. Meira Filho, B. A. Callander, N. Harris, A. Kattenberg, and K. Maskell, Cambridge University Press, Cambridge, 572 pp., 1996. Intergovernmental Panel on Climate Change, Climate Change 2001: Impacts, Adaptation and Vulnerability, edited by J. J. McCarthy, O. F. Canziani, N. A. Leary, D. J. Dokken, and K. S. White, Cambridge University Press, Cambridge, 1032 pp., 2001. International Union for the Conservation of Nature, Biological diversity of dry land, Mediterranean, arid, semiarid, savanna, and grassland ecosystems, World Conservation Union: Fourth meeting of subsidiary body on scientific, technical, and technological advice, Montreal, Canada, 1999. Kramer, K., Modelling comparison to evaluate the importance of phenology for the effects of climate change on growth of temperate-zone deciduous trees, Clim. Res., 5, 119-130, 1995. Kramer, K., I. Leinonen, and D. Loustau, The importance of phenology for the evaluation of impact of climate change on growth of boreal, temperate and Mediterranean forest ecosystems: an overview, Int. J. Biometeorol., 44, 67-75, 2000. Kuzucuoglu, C., Fires in Mediterranean region, Blue Planet Ecol., 72, 371-412, 1989. Le Houèrou, H. N., Climate change, drought and desertification, J. Arid Envirin., 34, 133185, 1996. Lindner, M., H. Bugmann, P. Lasch, M. Flechsig, and W. Cramer, Regional impacts of climatic change on forests in the state of Brandenburg, Germany, Agric. For. Meteorol., 84, 123-135, 1997. Minnich, R. A., Fire mosaics in southern California and northern Baja California, Science, 219, 1287-1294, 1983. Mohren, G. M. J., Simulation of forest growth, applied to Douglas fir stands in The Netherlands, Thesis, Agricultural University Wageningen, The Netherlands, 1987. Mohren, G. M. J. Modelling Norway spruce growth in relation to site conditions and atmospheric CO2, in Vegetation, modelling and climate change effects, edited by F. Veroustraete, and R. Ceulemans, pp. 7-22, SPB Academic Publishing, The Hague, 1994. Moll, E. J., Phenology of Mediterranean plants in relation to fire season: with special reference to the Cape Province South Africa, in Plant Response to Stress: Functional Analysis in Mediterranean Ecosystems, vol. 15, edited by J. D. Tenhunen, F. M. Catarino, O. L. Lange, and W. C. Oechel, NATO Adv. Sci. Inst. Ser. G Ecol. Sci., pp. 489-502, Springer-Verlag, Berlin, Heidelberg, 1987. Moll, E. J., B. M. Campbell, R.M. Cowling, L. Bossi, M. L. Karman, and C. Boucher, A description of major vegetation categories in and adjacent to the Fynbos biome, Report No. 83, S. Afr. Nat. Sci. Program, 210 pp., 1984. Montenegro, G., Quantification of Mediterranean plant phenology and growth, in Plant Response to Stress: Functional Analysis in Mediterranean Ecosystems, vol. 15, edited by J. D. Tenhunen, F. M. Catarino, O. L. Lange, and W. C. Oechel, NATO Adv. Sci. Inst. Ser. G Ecol. Sci., pp. 469-488, Springer-Verlag, Berlin, Heidelberg, 1987.


155

Mooney, H. A., and C. E. Conrad, Symposium on the environmental consequences of fire and fuel management in Mediterranean ecosystem, USDA Forest Service General, Technical Report WO-3, U.S. Government Printing Office, 498 pp., 1977. Mooney, H. A., and J. Kummerow, Phenological development of plants in mediterranean climate regions, in Ecosystems of the world: Mediterranean-type shrublands, vol. 11, edited by F. di Castri, D. W. Goodall, and R. L. Specht, pp. 303-307, Elsevier Scientific Publishing Company, Amsterdam, 1981. Mooney, H. A., B. G. Drake, R. J. Luxmoore, W. C. Oechel, and L. F. Pitelka, Predicting ecosystem response to elevated CO2 concentrantions, BioScience, 41, 96-104, 1991. Mooney, H. A., A. Johnson, D. Parson, S. Keeley, A. Hoffman, R. Hays, J. Giliberto, and C. Chu, The producers-their resources and adaptive response, in Convergent evolution in Chile and California Mediterranean Climate Ecosystems, edited by H. A. Mooney, p. 224, Dowden, Hutchinson and Ross, Stroudsburg, Pennsylvania, 1977. Naveh, Z., Fire in the Mediterranean: a landscape perspective, in Fire in ecosystem dynamics, edited by J. G. Goldhammer, and M. J. Jenkins, pp. 401-434, SPB Academic Publ., The Hague, 1990. Nicholls, N., G. V. Gruza, J. Jouzel, T. R. Karl, L. A. Ogallo, and D. E. Parker, Observed climate variability and change, in Climate change 1995: The science of climate change, edited by J. E. Houghton, L. G. Meira Filho, B. A. Callander, N. Harris, A. Kattenberg, and K. Maskell, pp. 133-192, Cambridge University Press, Cambridge, 1996. Oechel, W. C., and M. J. Moreno, The role of fire in Mediterranean ecosystems, SpringerVerlag, Berlin, Heidelberg, 527 pp., 1994. Ovalle, C., J. Aronson, A. Del Pozo, and J. Avendano, The espinal: agroforestry system of the mediterranean-type climate region of Chile, Agrof. Syst., 10, 213-239, 1990. Ovalle, C., J. Avendano, A. Del Pozo, and J. Aronson, Land occupation patterns and vegetation structure of the anthropogenic savannas (espinales) of central Chile, For. Ecol. Manage., 86, 129-139, 1996. Penuelas, J., I. Filella, and P. Comas, Changed plant and animal life cycles from 1952 to 2000 in the mediterranean region, Global Change Biol., 8, 532-544, 2002. Pereira, J. S., G. Beyschlag, O. L. Lange, W. Beyschlag, and J. D. Tenhunen, Comparative phenology of four Mediterranean shrub species growing in Portugal, in Plant Response to Stress: Functional Analysis in Mediterranean Ecosystems, vol. 15, edited by J.D. Tenhunen, F. M. Catarino, O. L. Lange, and W. C. Oechel, NATO Adv. Sci. Inst. Ser. G Ecol. Sci., pp. 503-513, Springer-Verlag, Berlin, Heidelberg, 1987. Quezel, P., Forests of the Mediterranean basin, in Mediterranean forests and maquis: Ecology conservation and management, pp. 9-33, Unesco, Paris, 1977. Rambal, S., and C. Hoff, Mediterranean ecosystems and fire: the threats of global change, in Large forest fires, edited by J. M. Moreno, pp. 187-213, Backhuys Publishers, Leiden, The Netherlands, 1998. Rossiter, R. C., and P. G. Ozanne, South-western temperate forests, woodlands and heaths, in Australian Grassland, edited by R. M. Moore, pp. 199-218, Australian National University Press, Canberra, 1970. Rundel, P. W., The matorral zone of central Chile, in Ecosystems of the world: Mediterranean-type shrublands, vol. 11, edited by F. di Castri, D. W. Goodall, and R. L. Specht, pp. 175-201, Elsevier Scientific Publishing Company, Amsterdam, 1981. Rundel, P.W., Impact of fire on nutrient cycles in Mediterranean-type ecosystems, with reference to chaparral, in Mediterranean-type ecosystems: the role of nutrients, edited by F. J. Kruger, D. T. Mitchell, and J. U. M. Jarvis, pp.192-207, Springer-Verlag, Berlin, Heidelberg, 1983.

156


Rundel, P. W., Adaptive significance of some morphological and physiological characteristics in mediterranean plants: facts and fallacies, in Time scales of biological responses to water constraints: the case of mediterranean biota, edited by J. Roy, J. Aronson, and F. di Castri, pp. 119-139, SPB Academic Publishers, Amsterdam, 1995. Rundel, P. W., Landscape disturbance in Mediterranean-type Ecosystems: an overview, in Ecological Studies: Landscape Degradation and Biodiversity in Mediterranean-Type Ecosystems, vol. 136, edited by P. W. Rundel, G. Montenegro, and F. M. Jaksic, pp. 3-22, Springer-Verlag, Berlin, Heidelberg, 1998. Rundel, P. W., and J. L. Vankat, Chaparral communities and ecosystems, in The California chaparral: paradigms reexamined, edited by S. Keeley, pp. 127-139, Los Angeles County Museum of Natural History, Los Angeles, California, 1989. Spano, D., C. Cesaraccio, P. Duce, and R. L. Snyder, Phenological Stages of Natural Species and their use as Climate Indicators, Int. J. Biometeorol., 42, 124-133, 1999. Specht, R. L., Structure and functional response of ecosystems in the Mediterranean climate of Australia, in Mediterranean-type ecosystems, Origin and Structure, edited by F. Castri, and H. A. Mooney, pp. 113-120, Springer-Verlag Berlin, Heidelberg, 1973. Specht, R. L., Ecosystems of the world: Heathlands and related shrublands, vol. 9A, Elsevier, Amsterdam, 497 pp., 1979. Specht, R. L., Mallee ecosystem in Southern Australia, in Mediterranean-type shrublands, edited by F. Castri, D. W. Goodall, and R. L. Specht, pp. 203-231. Elsevier, Amsterdam, 1981. Tenhunen, J. D., F. M. Catarino, O. L. Lange, and W. C. Oechel, Plant Response to Stress: Functional Analysis in Mediterranean Ecosystems, vol. 15, NATO Adv. Sci. Inst. Ser. G Ecol. Sci., Springer-Verlag, Berlin, Heidelberg, 1987. Thrower, N. J. W., and D. E. Bradbury, The physiography of the Mediterranean lands with special emphasis on California and Chile, in Mediterranean Type Ecosystems, Origin and Structure, edited by F. di Castri and H. A. Mooney, pp. 37-52, Springer-Verlag, Berlin, Heidelberg, 1973. Trabaud, L., and R. Prodon, Fire in Mediterranean ecosystems, Commission of European Communities, Brussels, 441 pp., 1993. Walter, H., and H. Lieth, Klimadiagramm Weltatlas, G Fischer Verlag, Jena, irreg. pp., 1967. Zinke, P. J., Analogies between the soil and vegetation types in Italy, Greece and California, in Mediterranean Type Ecosystem, Origin and Structure, edited by F. di Castri, and A. H. Mooney, pp. 61-80, Springer-Verlag, Berlin, Heidelberg, 1973.

Chapter 3.3 GRASSLANDS OF THE NORTH AMERICAN GREAT PLAINS Geoffrey M. Henebry Center for Advanced Land Management Information Technologies (CALMIT), School of Natural Resources, University of Nebraska, Lincoln, NE, USA

Key words:

1.

Tallgrass prairie, Anthesis, Transient Maxima Hypothesis, Great Plains

INTRODUCTION Question: What is Spring?— Growth in everything— Flesh and fleece, fur and feather, Grass and greenworld all together Gerard Manley Hopkins, The May Magnificat

The study of appearances of growth, development, and senescence in grassland communities is not an enterprise commonly pursued. Phenology of mid-latitude grasslands is, nevertheless, too large and diverse a collection of phenomena to cover within a single chapter, as it ought to embrace at once the vast Kazakh steppe, the chalk grasslands of southern England, and myriad other grassy landscapes. Thus, the view here shall be on the grasslands of the North American Great Plains, with particular reference to the tallgrass prairie as a type model. This chapter approaches phenological observations of grasslands from a perspective on ecological dynamics that is informed by hierarchy theory. A survey of the literature on what constitutes the expected phenological patterns of the grasses—rather than the forbs—within grasslands is provided. Schwartz (ed.), PHENOLOGY: AN INTEGRATIVE ENVIRONMENTAL SCIENCE, 157-174 © 2003 Kluwer Academic Publishers. Printed in the Netherlands.

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Various influences on grassland phenology are reviewed and the chapter concludes with an eye to future research directions.

2.

CHARACTERIZING GRASSLAND DYNAMICS

The grassland biome of North America emerges from interaction of vegetation with a particular climatic regime and a panoply of quasi-periodic influences, including drought, fire, and grazing by large ungulates (Bragg 1995). Four major types of grasslands can be distinguished within the Great Plains: (1) the tallgrass prairie that occurs principally east of 97°W; (2) the shortgrass prairie that occurs principally west of 101°W; (3) the mixed grass prairie that intergrades between these extremes; and (4) the sandhills prairie, which occurs on the inland sand dune system of the central Great Plains, principally in Nebraska, Colorado, and South Dakota (Joern and Keeler 1995). These prairies occur along two environmental gradients: the east-west gradient of diminishing total annual precipitation and the south-north gradient of diminishing average annual temperature. Stature of the community decreases as precipitation declines westward. Composition of the grass community shifts from dominance by C4 species in the southern and central Great Plains to increasing prevalence by C3 species, with a crossover near 44°N latitude (Sims 1988). The edaphic constraints that distinguish the sandhills prairie lead to a distinctive community composition and responsiveness to disturbances (Bragg 1995). From what perspective ought grassland phenology be approached? The Transient Maxima Hypothesis (TMH) posed by Seastedt and Knapp (1993) portrays subhumid grasslands in general and tallgrass prairies in particular as subject to the dynamic availability of multiple limiting resources. Thus, the interannual variation observed in primary production (Briggs and Knapp 1995; Knapp and Smith 2001) emerges from the interactivity of processes at different tempos: recent weather and atmospheric teleconnections; soil texture, nutrients, and moisture; topographic relief and fire frequency; and grazing by vertebrates and invertebrates above and below ground. When various windows of opportunity for resource capture develop from this interactivity, the vegetation exploits these transitory releases from constraints (Blair 1997). In effect, the “transient maxima” emerge from the constructive and destructive inference of constraints and forcings. However, which factors limit net primary production in a grassland at a given time and place depends strongly on recent and past events and the landscape context. Such a complex dynamic suggests that long-term study is required to articulate the boundaries of ecosystem behavior and develop an “ecological

Chapter 3.3: Grasslands of the N. American Great Plains

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expectation” of a location, analogous to the operational definition of climate as the “meteorological expectation” based on thirty years of weather data. Indeed, Fuhlendorf et al. (2001) found that canopy structural attributes from a 44-year grazing experiment lent support to both equilibrium and nonequilibrium models of vegetation dynamics, depending on the temporal scale considered. A temporal corollary of the TMH predicts non-transitivity in constraint sequencing, e.g., drought followed by fire is not equivalent in ecological effect to fire followed by drought (Collins et al. 1998a). A spatial corollary of the TMH predicts that differential phasing of resource availability across the landscape can generate self-reinforcing patches of vegetation assemblages and maintain or increase heterogeneity in space and species (Fuhlendorf and Smeins 1997; Collins et al. 1998b). Coffin et al. (1996) reached similar conclusions examining community composition 53 years after disturbance in shortgrass prairie. Burke et al. (1998) further argued that since dry grasslands are water-limited, they are not characterized by the “indeterminate dominance” of the tallgrass prairie but by “below ground dominance” that leads to the development of resource islands and discontinuous ground cover across the landscape. However, resource islands are a particular dynamical basin of attraction within the predictive purview of the TMH. This understanding of grassland ecosystem dynamics has significant implications for the study of phenological patterns in grasslands and for linking these patterns to appropriate regulatory influences and constraints. Spatial observations of grassland dynamics cover the landscape setting, composition, and configuration, including edaphic and terrain factors. Temporal observations describe current and recent conditions in terms of the energy and moisture regimes of the climate—long-term averages, variances, and extremes—and the characteristics of quasi-periodic disturbances that structure the grassland, including disturbance intensity, extent, duration, time since event, and the mean and variance of the return interval. In the study of appearances that is phenology, hierarchy theory (Allen and Starr 1982) provides a conceptual tool to organize various factors that affect phenology in grasslands. By considering the characteristic frequencies of these factors in space and/or time, constraints that change slowly in space and/or time relative to growing season phenology can be distinguished from forcings that change rapidly in space and/or time (Allen and Hoekstra 1986). Meteorological forcings on grassland phenology include the onset, severity, and duration of drought (Weaver 1968), excess precipitation, hail, snow, and frost (Inouye 2000), in addition to recent and current weather, including the pace and tempo of insolation (Frank and Hoffmann 1989; Goodin and Henebry 1997). Climatic constraints include regional climatic complexes

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(Hayden 1998), atmospheric teleconnections (Goodin et al. 2003), and the seasonality of plant-atmosphere interactions (Schwartz and Marotz 1986). Perturbations affecting primary production—fire, grazing, disease or pest outbreak, and air pollution/atmospheric deposition—are forcings that can affect phenology. However, the characteristic return intervals of these forcings may be considered to constitute constraints on the system. Frequently encountered events may be called perturbations to the system with the implication that their familiarity enables some degree of system resistance or resilience. Infrequently encountered events in terms of extent, duration, or severity may be called disturbances with the implication that their unusual aspect leads to system stress. Both terrain features—elevation, slope, aspect, landscape position—and edaphic properties, such as soil texture and geochemical composition, are constraints. However, the dynamics of soil moisture, soil nutrients, and surface energy balance are all forcings relative to the phenology of a prairie canopy. One final example of this distinction is germane to the spatiotemporal duality of forcings and constraints: the seasonality of daylength is a temporal forcing but the maximum daylength at a location is a constraint that is a function of both latitude and time of year. For a given limiting resource, phenology will be strongly modulated by slowly changing constraints on resource availability. Forcings affecting resource availability that change rapidly in time and/or space may exert less influence on grassland phenology. Yet, in the presence of multiple limiting resources, phenology can be strongly affected within a given growing season by abrupt switching between what constitutes the current constraint on plant growth and development (Figure 1, Seastedt and Knapp 1993; Blair 1997). This switching between primary controls, as predicted by the TMH, leads to a diversity of potential spatio-temporal modulations on canopy development, which translates into significant breadth for the coexistence of different phenological patterns, even among the dominant species of the grassland matrix. Although the TMH was formulated to understand specifically the above ground biomass dynamics in the tallgrass prairie, mid-latitude grasslands across the planet can be understood, to lesser or greater degrees, within the dynamical complexity available through the TMH framework.

3.

OBSERVING PHENOLOGY IN GRASSLANDS

Phenology is a field of inquiry where the role of the observer is made quite explicit. While the primary challenge to phenological study in grasslands is the range of forcings and constraints that can influence plant growth and development, an additional related challenge is the relative lack


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of what Leopold and Jones (1947) identified as desirable qualities in items used for phenological survey: sharpness, visibility, and recurrence.

Figure 3.3-1. Grasslands phenology emerges from the interactivity of multiple influences as filtered through the specifics of spatial relationships and genetic heritage and the process of observation.

Sharpness is the relative distinctiveness in the item that reduces variation between observers. Leopold and Jones (1947) point to grasses that do not extrude their pollen as an example of lack of item sharpness for the detection of first bloom. Visibility may be best illustrated by its deficit: Rice (1950) resorted to dissection and microscopic examination to determine whether inflorescences had initiated in principal grasses of a mixed grass prairie. Recurrence relates to low interannual variation in the phenological item. Phenological studies of the grasses that compose the ecosystemic matrix of the prairies must face low recurrence, poor visibility, and blunted sharpness. In contrast, focus on the forbs and woody plants that dwell within the prairie yields phenological items that display sharpness, visibility, and recurrence. Not surprisingly, the scant literature on grasslands phenology tends to focus on showy forbs embedded within grass matrices, rather than the grasses per se. Tallgrass prairies have received more phenological study than other prairies, possibly due to their diversity and productivity. Leopold and Jones (1947) gathered cross-taxa phenological data over 11 years on the average blooming dates of 52 forbs and 7 grasses typical of the sandy soils of

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Wisconsin prairies. The 7 grasses, which are typical species of tallgrass prairie, and their flowering sequence were: (1) Scribner’s panicum, Dichanthelium oligosanthes var. scribnerianum (Nash) Gould—early June to mid-July; (2) junegrass, Koeleria macrantha (Ledeb.) J.A. Schultes— mid-June to early July; (3) switchgrass, Panicum virgatum L.—late July to mid-September; (4) big bluestem, Andropogon gerardii Vitman—late July to late August; (5) sideoats grama, Bouteloua curtipendula (Michx.) Torr.— early August to mid-September; (6) little bluestem, Schizachyrium scoparium (Michx.) Nash—mid-August to mid-September; and (7) indiangrass, Sorghastrum nutans (L.) Nash—mid-August to early September. Scribner’s panicum and junegrass are C3 species and the rest are C4 species. Noting that some prairie grasses and forbs commence growth relatively late in the season, they opined: “Could this be an evolutionary device for avoiding damage from spring fires?” Ahshapenek (1962) described grass phenology during 1957-1958 in an unburned, ungrazed tallgrass prairie in central Oklahoma dominated by C4 species. The sequence of anthesis of these grasses was switchgrass (late July), little bluestem (early August), big bluestem (late August), indiangrass (early September), and tall dropseed, Sporobolus compositus (Poir.) Merr. (mid-September). Proportion of flowering tillers ranged from 1.5% (tall dropseed) and 3.6% (big bluestem) to 21% (switchgrass) and 26% (little bluestem). Duration of phenological events in the prairie exhibits a range of variation. Leopold and Jones (1947) noted that the prairie has a “peculiar” interspersion of long and short blooming plants, primarily forbs. To examine the hypothesis that prairie plants “stagger” flowering times to reduce competition for pollinators, Anderson and Schelfhout (1980) analyzed flowering patterns of 77 tallgrass prairie plants (primarily forbs) from the Curtis Prairie at the University of Wisconsin Arboretum during 1950-1951. They found consistency in blooming sequences and duration over two years and speculated that many prairie plants use precise environmental cues such as photoperiod to initiate blooming. In a related study, Anderson and Adams (1981) compared flowering patterns of the Curtis Prairie with one year (1974) of observation at a tallgrass prairie in central Oklahoma dominated by little bluestem. The Oklahoma site had been formerly grazed and hayed, but not otherwise disturbed for five years prior to the study. From midMarch to mid-November, a clear bimodality was evident in the number of species flowering in Oklahoma. One peak occurred from May to early June and a second in early September. In contrast, the Wisconsin data suggested bimodality only weakly, with a broad peak occurring in mid-July. Extending this investigation, Kebart and Anderson (1987) examined flowering patterns in a tallgrass prairie community in Illinois in 1983 and


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compared those data with the Wisconsin and Oklahoma data. The Illinois pattern was distinct from the other two and suggested trimodality, with the principal peak in mid-July and minor peaks in mid-March and mid-August through mid-September. Parrish and Bazzaz (1979) also found trimodality in forb flowering sequences in a remnant tallgrass prairie in Illinois. Correlation analysis for the Wisconsin, Oklahoma, and Illinois sites revealed moderate to strong significant positive correlations between the number of species flowering per month with the mean monthly precipitation and temperature. However, there was not a consistent pattern in the correlation coefficients across sites and environmental variables. In addition, Rabinowitz et al. (1981) found no significant differences in phenological curves for 82 tallgrass species pollinated by either wind or insect, concluding that community flowering sequences were indistinguishable from random assemblages. In other words, distinct differences among species’ phenologies did not translate into ensemble flowering patterns that exhibit either temporal convergence or divergence that might support hypotheses regarding competition for pollinators. Speculating that combinations of soil moisture availability and daylength differentially trigger flowering, Anderson and Adams (1981) concluded that prairie species’ phenological patterns respond both to the environmental conditions of a particular growing season and across a latitudinal gradient of photoperiod and temperature. Phenological studies have also been conducted in shortgrass prairie with similarly inconclusive results. Dickinson and Dodd (1976) investigated phenological pattern in a shortgrass prairie in northeastern Colorado. The phenological timing of 34 species (12 grasses and sedges; 17 forbs; four half shrubs; and one succulent) was observed in the first study year (1972). These observations were extended to a second year for a subset of six species. One study objective was the identification of a single species that could indicate the phenological behavior of distinct groups of vegetation. Six phenological groups were identified from the 1972 survey. Their indicator species and time of flowering were (1) spike-rush sedge, Carex duriuscula C.A. Mey.—late April to mid-May; (2) prairie pepperweed, Lepidium densiflorum Schrad.—mid-May to early June; (3) needle and thread, Hesperostipa comata (Trin. & Rupr.) Barkworth—June; (4) red threeawn, Aristida purpurea var. longiseta (Steud.) Vasey—June to July; (5) blue grama, Bouteloua gracilis (Willd. ex Kunth) Lag. ex Griffith—July to August; and (6) fringed sagebrush, Artemisia frigida Willd.—late August to early September. Results showed the conventional division between warm-season and cool-season grasses was not a reliable predictor of flowering period. In particular, the nominally warm-season C4 species buffalograss, Buchloe dactyloides (Nutt.) Engelm., flowered at similar times

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to the cool-season C3 species western wheatgrass, Pascopyrum smithii (Rydb.) A. Löve. Another example of a C4 species that flowers early like a cool-season grass is eastern gamagrass, Tripsacum dactyloides (L.) L. (Dewald and Louthan 1979). From their survey, Dickinson and Dodd (1976) distinguished four groups of shortgrass prairie plants based on flowering pattern: very early single bloom; double bloom requiring a summer dormancy; drought-retarded midsummer single bloom; and late season single bloom. Given the importance of water in limiting productivity in the shortgrass prairie, particular attention has been given to its effect on phenology. To assess this response, Dickinson and Dodd (1976) applied water amendments to study plots by. Blue grama was found to be particularly responsive to a manipulated moisture regime: a delay of flowering followed by synchronization of flowering and acceleration of seed dispersal. For example, multiple blooms were observed on blue grama following downpours from convective thunderstorms that occurred approximately every 10 d. However, the secondary blooms observed following natural precipitation were not observed in the well-watered plots, suggesting that serial blooming requires wet-dry environmental cueing. A common thread running through many of these phenological studies in grasslands is their short duration relative to the high interannual variation in weather experienced across the Great Plains grasslands (Hayden 1998). While the broad patterns of phenology have been described, there are many variations on those themes that can serve to confound brief observational studies of communities of these long-lived perennials.

4.

FACTORS AFFECTING PHENOLOGY IN GRASSLANDS

4.1

Ecotypic Variation

During the middle of the last century, a significant body of research focused on the effect of photoperiod on phenology of rangeland grasses and the variation in that effect among geographic clones (Benedict 1941; Olmsted 1943, 1944, 1945; Rice 1950). Building on this work through a series of experiments on geographic clones of dominant and subordinate grasses transplanted to uniform gardens and in reciprocal transplants, McMillan found a strong gradient of more rapid phenological development from south to north and to a lesser extent from east to west (McMillan 1956a,b, 1957, 1959a,b). The longer growing seasons and more mesic


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environments toward the south and east of the Great Plains allowed grasses to initiate growth earlier and flower later than more northerly or westerly clones. McMillan (1960) argued that these patterns of ecotypic variation within species emerge from natural selection through the continuing interaction between the “habitat variable”, i.e., variation in local environmental forcings and constraints, and the “genetic variable”, i.e., the differential responses to the same habitat arising from the differential genetic potential among individual members of a population. Heide (1994) provides a contemporary review on the role of daylength and ecotypic variation on induction of flowering in temperate C3 temperate grasses.

4.2

Fire

Fire has substantial effects on grassland physiognomy, productivity, and phenology. In the tallgrass prairie, a disturbance-maintained ecosystem, periodic fire is required to prevent the encroachment by woody plants (Collins et al. 1998a). Moreover, dormant season fire following a few years of no burning can produce significant increases in the productivity of the dominant grasses, especially if the burn occurs in late spring. Frequent dormant season fire in the tallgrass prairie, however, can decrease species diversity (Knapp et al. 1998). Research indicates that the Nebraska sandhills prairie is also fire-adapted, with shifts in fire-positive and fire-negative species occurring subsequent to occasional wildfires (Bragg 1995). In the northern mixed-grass prairies dominated by C3 species, fire at any time of year generally decreases net primary production, even in years of normal precipitation, which is a response opposite to that observed in tallgrass prairie (Bragg 1995). Similarly, in the southern mixed-grass prairie dominated by C4 species, fire decreases production. In the water-limited shortgrass prairie of the western and southern Great Plains, fire during a dry year can have lasting impacts, although recovery from fire in normal-to-wet years can be relatively rapid (Bragg 1995; Burke et al. 1998). Fire frequency in these prairies is limited due to by accumulation and spatially patchy distribution of flammable litter (Bragg 1995). The timing and frequency of fire can affect various aspects of plant phenology but the effect of fire on subsequent flowering of dominant tallgrass species has been a focus of recurrent interest since the middle of the last century. Most of this work has centered on the responses of big bluestem under a regime of late spring burning, although some attention has been given to other prevalent species. Frequent burning can decrease the prevalence of flowering but long fire return intervals can also attenuate the flowering (Ehrenreich and Aikman 1963; Hulbert and Wilson 1983; Towne 1995). Significant interannual variations in flowering responses have been observed inn tallgrass prairies

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under annual burning. Knapp and Hulbert (1986) suggested that this variability points to shifts in controlling factors. Other investigators have contended that significant variation in intraspecific n responses to fire point to the importance of current site conditions (Zedler and Loucks 1969; Pemble et al. 1981). All these interpretations fall within the expected range of behaviors emerging from switching among primary controls as predicted by the TMH (Seastedt and Knapp 1993). The fire return interval also yields species-specific plant responses. Hulbert and Wilson (1983) found highly significant differences between annual and biennial burns for flowering density, flower stem biomass and height of big bluestem and indiangrass: the biennial burn yielded greater stem density and biomass. In contrast, there was no significant difference in inflorescence density or biomass in little bluestem. Furthermore, the significant differences between two-year and six-year spring burns were not uniform across species. The longer time between burns translated into taller, heavier, and more flowering stems for big bluestem. Fewer, smaller flowering stems in both indiangrass and little bluestem resulted from the longer fire interval. Towne (1995) observed that, during two uncharacteristically wet years, annual burning stimulated 15% of big bluestem and indiangrass tillers to flower. In contrast, only 3% of tillers developed inflorescences in unburned prairie. Flowering of big bluestem peaked (44%) in the year of burning following three years without burning (a quadrennial fire return interval), but indiangrass flowering was greatly diminished with this burning regime. Season of fire also affects flowering response. Henderson et al. (1983) examined the interaction of site condition and seasonality of burning for three C3 and four C4 grasses. They found that the C3 species flowered significantly less vigorously following late spring burns. A range of flowering responses in the C4 species were observed with a general—though not universal—trend toward greater flowering with late spring burns. Towne (1995) found the percentage of reproductive indiangrass tillers to be significantly less when annual burning occurred in November or March. Big bluestem, in contrast, showed no significant effect of the season of annual burning. Benning and Bragg (1993) found that the specific timing of burning within late spring could yield significantly different flowering responses, suggesting that the proximate environmental context (i.e., constraint sequencing) of the burning event is important in floral induction. Flowering stalks of dominant tallgrasses increase in number, density, and stature following spring fire in areas where prior years’ growth has formed a thick litter layer (Curtis and Partch 1950; Kucera and Ehrenreich 1962; Ehrenreich and Aikman 1963; Old 1969; Knapp 1984a; Knapp and Hulbert 1986). Petersen (1983) suggested that the presence of fire is a more


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important environmental cue for flowering in big bluestem than the removal of the litter layer or the addition of nutrient-rich surface-darkening ash as argued by others (Curtis and Partch 1950; Ehrenreich and Aikman 1963). Current thinking points to changes in microclimate, particularly due to the removal of the litter layer, as the primary stimuli to flowering following spring burns. The grassland detritus layer composed of previous years’ growth acts as a biotic buffer, which limits irradiance, increases the threshold for effective precipitation, and retards bare soil evaporation, thus reducing productivity (Knapp and Seastedt 1986; Knapp et al. 1998). Burning removes the accumulation of previous years’ growth, thereby increasing the quality of the light environment, the potential rate of evapotranspiration, and the variability of the surface energy balance. Furthermore, for all the biomass that has accumulated above ground, there is even more biomass below ground as fine root material. The pulse in primary production is fueled by the interaction of favorable light environment with a pool of organic nitrogen that can be mineralized and made available for canopy development, if the soil moisture is favorable (Blair 1997; Blair et al. 1998). The resulting pulse of available nitrogen can support relatively high flowering rates (Towne 1995). However, burning over the long term reduces nitrogen availability. Big bluestem has high nitrogen use efficiency and becomes a superior competitor under suboptimal conditions for its growth and development (Seastedt et al. 1991; Seastedt 1995).

4.3

Water Stress

Deficits of water leading to plant stress can affect phenological development. Investigating the effect of water stress in the tallgrass prairie on growth of big bluestem, little bluestem, and switchgrass in wet and droughty years, Knapp (1984b) found that reproductive effort (density, height, and biomass of flowering stems) could be significantly diminished during drought. Supplemental irrigation during a wetter year increased reproductive effort of switchgrass but not big bluestem or little bluestem. During a droughty year, however, irrigation increased primary production and reproduction in all three species. Big bluestem had a greater capacity for osmotic adjustment than little bluestem or switchgrass; however, big bluestem exhibited no reproductive effort in the droughty year of 1983. Late season water stress can reduce flowering in semi-arid C4 grasses (Alcocer-Ruthling et al. 1989). Dickinson and Dodd (1976) found that several shortgrass species could flower multiple times during a single season when short dry spells were followed by sufficient precipitation. Similarly, Beatley (1974) described how heavy rains trigger phenological events in vegetation of the Mojave Desert vegetation, including its perennial grasses.

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4.4


Spatial Influences

Topographic position can affect microclimate, including insolation, drainage, deposition, and exposure to wind. Although topoposition has been shown to have a significant effect on the phenological development of spring wildflowers (Jackson 1966), the influence for grassland species is variable. Rice (1950) saw no topographic effect on flowering in little bluestem in Oklahoma. McMillan (1956b) found that little bluestem clones from different topopositions in steep loess bluffs exhibited variations in flowering date after transplanting to a uniform garden. Topoposition has been shown to interact with fire to results in different plant responses. Zedler and Loucks (1969) found topoposition influences the susceptibility of grass production and flowering response to fire in a disturbed prairie. Pemble et al. (1981) attributed the significant intraspecific variations they found in the flowering responses for grasses at a Minnesota prairie to site-specific modulation of moisture conditions following a spring burn. Similarly, Knapp (1985) found that early season production in big bluestem in the more mesic lowlands of Konza Prairie were significantly greater than in the more exposed, warmer, and windier uplands.

4.5

Herbivory and Other Influences

Other influences on phenological timing and pace may include any disturbance that removes or kills above ground biomass, including herbivory, mowing, and hail. Hover and Bragg (1981), for example, found that summer mowing significantly decreased big bluestem flowering stem density compared to spring mowing or burning. Herbivory, which is a more selective process to remove plant biomass both above ground and below ground, affects plant growth, development, and reproduction in myriad ways, including through indirect influences and delayed effects. The literature on grazing in grasslands is too extensive to engage here. The primary effect of grazing is the reduction in flowering stem density as a result of the removal of apical meristems that may produce inflorescences. However, an indicative study (Vinton and Hartnett 1992) points to the complexities of interactions that may found. For example, bison grazing and simulated herbivory by clipping of big bluestem and switchgrass increased relative growth rates during the growing season that compensated for the lost tissue. In contrast, big bluestem tillers that had been repeatedly grazed in the previous growing season exhibited reductions in relative growth rates, survival and accumulated biomass in the subsequent growing season, although one was distinguished by a severe drought. In fire-related interactions, increases in relative growth rates of big bluestem following


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defoliation were greater in unburned than burned prairie; a topographic effect was also noted. Switchgrass, in contrast, was less responsive to environmental conditions, showing similar responses to defoliation in burned and unburned prairie (Vinton and Hartnett 1992).

5.

FUTURE DIRECTIONS

Phenological observations in mid-latitude grasslands have intrinsically low information density because of the high interannual variation in weather patterns. Only from several years of data can robust patterns emerge. Yet many studies of grassland phenology in the North American Great Plains have relied on only one or two years of observation. Dedicated, intensive phenological observations are expensive and thus rare—even the seminal cross-taxa phenology of Leopold and Jones (1947) was constructed from data collected largely in passing. Moreover, the sensitivity of some dominant species to topoposition and disturbance history complicates simple surveying. What then may be future directions for observing, monitoring, and modeling the phenologies found in grassland ecosystems? One bottom-up direction is in situ wireless sensor networks (Withey et al. 2001), which promise distributed monitoring capabilities of perisurficial environments. The use of spaceborne sensors to measure and monitor land surface phenology, including grasslands, is reviewed in Chapter 5.1. One further top-down direction stems from recent advances in the use of fine spectral resolution sensing to retrieve pigment concentrations, including anthocyanins (Gitelson et al. 2001), chlorophylls (Gitelson et al. 2002a), and carotenoids (Gitelson et al. 2002b). These techniques hold promise for the detection of anthesis and senescence as well as the onset of spring. However, it is important to note that, given the critical role of the scale of observation in phenological studies, the translations from remote observations to canopy dynamics as well as from leaf phenomena to vegetated landscape are intrinsically difficult and likely require site-specific rather than generic solutions. The question of whatt Spring is may be addressed more readily than the dual when questions about Springs past and Springs future. Indeed, it may be fair to characterize this simple question—When will Spring arrive?—as a canonical query for ecological forecasting (Clark et al. 2001; Henebry and Goodin 2002) and global change research (Myneni et al. 1997; Schwartz 1999). To integrate the various phenologies of “grass and greenworld” within the purview of ecosystem ecology and biogeosciences, the myriad ecophysiological responses of grassland canopies must be placed within the

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contexts of their landscapes, land uses, and disturbance regimes, by means of longer term empirical investigations—using field-based and space-based monitoring—modeling studies, and the development of ecological forecasting techniques.

ACKNOWLEDGEMENTS The accuracy and clarity of this chapter were significantly enhanced by comments and suggestions from an anonymous reviewer, Mark Schwartz, Andrés Viña, and especially from the careful readings by Tom Bragg and Gene Towne. Thanks to Ana Braga-Henebry for assistance with the figure. This survey was partially supported through the NSF Biodiversity and Ecosystem Informatics (BDEI) program (EIA #0131937).

REFERENCES CITED Ahshapanek, D., Phenology of a native tall-grass prairie in Central Oklahoma, Ecology, 43, 135-138, 1962. Alcocer-Ruthling, M., R. Robberecht, and D. C. Thill, The response of Bouteloua scorpioides to water stress at two phenological stages, Botanical Gazette, 150, 454-461, 1989. Allen, T. F. H., and T.W. Hoekstra, Description of complexity in prairies through hierarchy theory, in Proceedings of the Ninth North American Prairie Conference edited by G.K. Clambey and R.H. Pemble, pp. 71-73, Tri-college University Center for Environmental Studies, Fargo, ND, 1986. Allen, T. F. H., and T. B. Starr, Hierarchy: Perspectives for Ecological Complexity, University of Chicago Press, Chicago, 310 pp., 1982. Anderson, R. C., and D. E. Adams, Flowering patterns in a central Oklahoma grassland, Ohio Biological Survey Biological Notes, 15, 232-235, 1981. Anderson, R. C., and S. Schelfhout, Phenological patterns among tallgrass prairie plants and their implications for pollinator competition, Amer. Midland Naturalist, 104, 253-263, 1980. Beatley, J. C., Phenological events and their environmental triggers in Mojave Desert ecosystems, Ecology, 55, 856-863, 1974. Benedict, H. M., Growth of some range grasses in reduced light intensities at Cheyenne, Wyoming, Botanical Gazette, 102, 582-589, 1941. Benning, T. L., and T. B. Bragg, Response of big bluestem ((Andropogon gerardii Vitman) to timing of spring burning, Amer. Midland Naturalist, 130, 127-132, 1993. Blair, J. M., Fire, N availability, and plant response in grasslands: A test of the transient maxima hypothesis, Ecology, 78, 2359-2368, 1997. Blair, J. M., T. R. Seastedt, C.W. Rice and R.A. Ramundo, Terrestrial nutrient cycling in tallgrass prairie, in Grassland Dynamics: Long-Term Ecological Research in Tallgrass Prairie edited by A. K. Knapp, D. C. Hartnett, J. M. Briggs, and S. Collins, pp. 222-243, Oxford University Press, New York, 1998.


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Bragg, T. B., The physical environment of great plains grasslands, in The Changing Prairie, edited by A. Joern and K. H. Keeler, pp. 49-81, Oxford University Press, New York, 1995. Briggs, J. M., and A. K. Knapp, Interannual variability in primary production in tallgrass prairie: climate, soil moisture, topographic position and fire as determinants of aboveground biomass, Amer. J. Botany, 82, 1024-1030, 1995. Burke, I. C., W. K. Lauenroth, M. A. Vinton, P. B. Hook, R. H. Kelly, H. E. Epstein, M. R. Aguiar, M. D. Robles, M. O. Aguilera, K. L. Murphy, and R. A. Gill, Plant-soil interactions in temperate grasslands, Biogeochemistry, 42, 121-143, 1998 Clark J. S., R. Carpenter, M. Barber, S. Collins, A. Dobson, J. Foley, D. Lodge, M. Pascual, R. Pielke Jr., W. Pizer, C. Pringle, W. V. Reid, K. A. Rose, O. Sala, W. H. Schlesinger, D. Wall, and D. Wear, Ecological forecasts: an emerging imperative, Science, 293, 657–660, 2001. Coffin, D. C., W. K. Lauenroth, and I. C. Burke, Recovery of vegetation in a semiarid grassland 53 years after disturbance, Ecol. Applications, 6, 538-555, 1996. Collins, S., A. K. Knapp, D. C. Hartnett, and J. M. Briggs, The dynamic tallgrass prairie. Synthesis and research opportunities, in Grassland Dynamics: Long-Term Ecological Research in Tallgrass Prairie, edited by A. K. Knapp, D. C. Hartnett, J. M. Briggs, S. Collins, pp. 301-315, Oxford University Press, New York, 1998a. Collins, S. L., A. K. Knapp, J. M. Briggs, J. M. Blair, and E. M. Steinauer, Modulation of diversity by grazing and mowing in native tallgrass prairie, Science, 280, 745-747, 1998b. Curtis, J. T. and M. L. Partch, Some factors affecting flower production in Andropogon gerardi, Ecology, 31, 488-489, 1950. Dewald, C.L, and V. H. Louthan, Sequential development of shoot system components in eastern gamagrass, J. Range Management, 32, 147-151, 1979. Dickinson, C. E., and J. L. Dodd, Phenological pattern in the shortgrass prairie, Amer. Midland Naturalist, 96, 367-378, 1976. Ehrenreich, J. H., and J. M. Aikman, An ecological study of the effect of certain management practices on native prairie in Iowa, Ecol. Monographs, 33, 113-130, 1963. Frank, A. B., and L. Hofmann, Grazing management, growing degree-days, and morphological development for native grasses on the northern Great Plains, J. Range Management, 42, 199-202, 1989. Fuhlendorf, S. D., and F. E. Smeins, Long-term vegetation dynamics mediated by herbivores, weather and fire in a Juniperus-Quercus savanna, J. Veg. Science, 8, 819-828, 1997. Fuhlendorf, S. D., D. D. Briske, and F.E. Smeins, Herbaceous vegetation change in variable rangeland environments: The relative contribution of grazing and climatic variability, Appl. J. Veg. Science, 4, 177-188, 2001. Gitelson, A. A., M. N. Merzlyak, O. B. Chivkunova, Optical properties and nondestructive estimation of anthocyanin content in plant leaves, Photochemistry and Photobiology, 74, 38-45, 2001. Gitelson, A. A., Y. J. Kaufman, R. Stark, and D. Rundquist, Novel algorithms for remote estimation of vegetation fraction, Remote Sens. Environ., 80, 76-87, 2002a. Gitelson, A. A., Y. Zur, O. B. Chivkunova, and M.N. Merzlyak, Assessing carotenoid content in plant leaves with reflectance spectroscopy, Photochemistry and Photobiology, 75, 272281, 2002b. Goodin, D. G., and G. M. Henebry, Monitoring ecological disturbance in tallgrass prairie using seasonal NDVI trajectories and a discriminant function mixture model, Remote Sens. Environ., 61, 270-278, 1997.

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Goodin, D. G., P. A. Fay, and M. J. McHugh, Climate variability in tallgrass prairie at multiple time scales: Konza Prairie Biological Station, USA, in Climate Variability and Ecosystem Response, edited by D. E. Greenland, D. G. Goodin, and R. Smith, pp. 411423, Oxford University Press, New York, 2003. Hayden, B. P., Regional climate and the distribution of tallgrass prairie, in Grassland Dynamics: Long-Term Ecological Research in Tallgrass Prairie, edited by A. K. Knapp, D. C. Hartnett, J. M. Briggs, and S. Collins, pp. 19-34, Oxford University Press, New York, 1998. Heide, O. M., Control of flowering and reproduction in temperate grasses, New Phytologist, 128, 347-362, 1994. Henderson, R. A., D. L. Lovell, and E. A. Howell, The flowering responses of 7 grasses to seasonal timing of prescribed burns in remnant Wisconsin prairie, in Proceedings of the Eighth North American Prairie Conference, edited by R. Brewer, pp. 7-10, Western Michigan University, Kalamazoo, MI, 1983. Henebry, G. M., and D. G. Goodin, Landscape trajectory analysis: toward spatio-temporal models of biogeophysical fields for ecological forecasting, in Workshop on Spatiotemporal Data Models of Biogeophysical Fields for Ecological Forecasting: April 8-10, 2002, San Diego Supercomputer Center, La Jolla, California, edited by G. M. Henebry, pp. 9-13, CALMIT, University of Nebraska, Lincoln, NE, 2002. Hover, E. I. and T. B. Bragg, Effect of season of burning and mowing on an eastern Nebraska Stipa-Andropogon prairie, Amer. Midland Naturalist, 105, 13-18, 1981. Hulbert, L. C., and J. K. Wilson, Fire interval effects on flowering of grasses in Kansas Bluestem Prairie, in Proceedings of the Seventh North American Prairie Conference; 1980 August 4-6; Springfield, MO, edited by C. L. Kucera, pp. 255-257, University of Missouri, Columbia, MO, 1983. Inouye, D. W., The ecological and evolutionary significance of frost in the context of climate change, Ecol. Letters, 3, 457-463, 2000. Jackson, M., Effects of microclimate on spring flowering phenology, Ecology, 47, 407-415, 1966. Joern, A., and K. H. Keeler, Getting the lay of the land: Introducing North American native grasslands, in The Changing Prairie, edited by A. Joern and K. H. Keeler, pp. 11-24, Oxford University Press, New York, 1995. Kebart, K. K., and R. C. Anderson, Phenological and climatic patterns in three tallgrass prairies, Southwestern Naturalist, 32, 29-37, 1987. Knapp, A. K., Post-burn differences in solar radiation, leaf temperature and water stress influencing production in a lowland tallgrass prairie, American Journal of Botany, 71, 220-227, 1984a. Knapp, A. K., Water relations and growth of three grasses during wet and drought years in tallgrass prairie, Oecologia, 65, 35-43, 1984b. Knapp, A. K., Early season production and microclimate associated with topography in a C4 dominated grassland, Acta Oecologica/ Oecologica Plantarum, 6, 337-346, 1985. Knapp, A. K., J. M. Briggs, J. M. Blair, and C. L. Turner, Patterns and controls of aboveground net primary production in tallgrass prairie, in Grassland Dynamics: LongTerm Ecological Research in Tallgrass Prairie edited by A. K. Knapp, D. C. Hartnett, J. M. Briggs, and S. Collins, pp. 193-221, Oxford University Press, New York, 1998. Knapp, A. K., and L. C. Hulbert, Production, density and height of flower stalks of three grasses in annually burned and unburned eastern Kansas tallgrass prairie: a four year record, Southwestern Naturalist, 31, 235-241, 1986.


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Knapp, A. K., and T. R. Seastedt. Detritus accumulation limits productivity of tallgrass prairie, BioScience, 36, 662-668, 1986. Knapp, A. K., and M. D. Smith, Variation among biomes in temporal dynamics of aboveground primary production, Science, 291, 481-484, 2001. Kucera, C. L., and J. H. Ehrenreich, Some effects of annual burning on central Missouri prairie, Ecology, 43, 334-336, 1962. Leopold, A., and E. Jones, A phenological record for Sauk and Dane Counties, Wisconsin, 1935-1945, Ecol. Monographs, 17, 83-122, 1947. McMillan, C., Nature of the plant community. I. Uniform garden and light period studies of five grass taxa in Nebraska, Ecology, 37, 330-340, 1956a. McMillan, C., Nature of the plant community. II. Variation in flowering behavior within populations of Andropogon scoparius, Ecology, 43, 429-436, 1956b. McMillan, C., Nature of the plant community. III. Flowering behavior within two grassland communities under reciprocal transplanting, Amer. J. Botany, 44, 144-153, 1957. McMillan, C., Nature of the plant community. V. Variation within the true prairie community-type, Amer. J. Botany, 46, 418-424, 1959a. McMillan, C., The role of ecotypic variation in the distribution of the central grassland of North America, Ecol. Monographs, 29, 285-308, 1959b. McMillan, C., Ecotypes and community function, Amer. Naturalist, 94, 245-255, 1960. Myneni, R. B., C. D. Keeling, C. J. Tucker, G. Asrar, R. R. Nemani, Increased plant growth in the northern high latitudes from 1981 to 1991. Nature, 386, 698-701, 1997. Old, S. M., Microclimate, fire, and plant production in an Illinois prairie, Ecol. Monographs, 39, 355-384, 1969. Olmsted, C. E., Growth and development in range grasses. III. Photoperiodic responses in the genus Bouteloua, Botanical Gazette, 105, 165-181, 1943. Olmsted, C. E., Growth and development in range grasses. IV. Photoperiodic responses in twelve geographic strains of side-oats gramma, Botanical Gazette, 106, 46-74, 1944. Olmsted, C. E., Growth and development in range grasses. V. Photoperiodic responses of clonal divisions of three latitudinal strains of side-oats gramma, Botanical Gazette, 106, 382-401, 1945. Parrish, J. A. D., and F. A. Bazzaz, Difference in pollination niche relationships in early and late successional plant communities, Ecology, 60, 597-610, 1979. Pemble, R. H., G. L. Van Amburg, and L. Mattson, Intraspecific variation in flowering activity following a spring burn on a Northwestern Minnesota prairie, Ohio Biological Survey Biological Notes, 15, 235-239, 1981. Petersen, N. J., The effects of fire, litter, and ash on flowering in Andropogon gerardii, in Proceedings of the Eighth North American Prairie Conference, 1982, Aug 1-4, Kalamazoo, Michigan, edited by R. Brewer, pp. 21-24, Western Michigan University, Department of Biology, Kalamazoo, MI, 1983. Rabinowitz, D., J. K. Rapp, V. L. Sork, B. J. Rathcke, G. A. Reese, and J. C. Weaver, Phenological properties of wind- and insect-pollinated prairie plants, Ecology, 62, 49-56, 1981. Rice, E. L., Growth and floral development of five species of range grass in central Oklahoma, Botanical Gazette, 111, 361-377, 1950. Schwartz, M. D., Advancing to full bloom: planning phenological research for the 21st century, Int. J. Biometeorol., 42, 113-118, 1999. Schwartz, M. D. and G. A. Marotz, An approach to examining regional atmosphere-plant interaction with phenological data, J. Biogeography, 13, 551-560, 1986.

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Seastedt, T. R., Soil systems and nutrient cycles of the North American prairie, in The Changing Prairie, edited by A. Joern and K. H. Keeler, pp. 49-81, Oxford University Press, New York, 1995. Seastedt, T. R., J. M. Briggs, and D. J. Gibson, Controls of nitrogen limitation in tallgrass prairie, Oecologia, 87, 72-79, 1991. Seastedt, T. R., and A. K. Knapp, Consequences of non-equilibrium resource availability across multiple time scales: the transient maxima hypothesis, Amer. Naturalist, 141, 621633, 1993. Sims, P. L., Grasslands, in North American Terrestrial Vegetation, edited by M. G. Barbour, and W. D. Billings, pp. 265-286, Cambridge University Press, New York, 1988. Towne, E. G., Influence of fire frequency and burning date on the proportion of reproductive tillers in big bluestem and indiangrass, in Proceedings of the 14th Annual North American Prairie Conference, edited by D. C. Hartnett, pp. 75-78, Kansas State University, Manhattan, Kansas, 1995. Vinton, M. A., and D. C. Hartnett, Effects of bison grazing on Andropogon gerardii and Panicum virgatum in burned and unburned tallgrass prairie, Oecologia 90:374-382, 1992. Weaver, J. E., Prairie Plants and Their Environment: a Fifty-Year Study in the Midwest, University of Nebraska Press, Lincoln and London, 276 pp., 1968. Withey, A., W. Michener, and P. Tooby, Scalable Information Networks for the Environment (SINE), Report of an NSF-sponsored workshop, San Diego Supercomputer Center, October 29-31, 2001. Zedler, J. B., and O. L. Loucks, Differential burning responses of Poa pratensis fields and Andropogon scoparius prairies in central Wisconsin, Amer. Midland Naturalist, 81, 341352, 1969.

Chapter 3.4 HIGH LATITUDE CLIMATES Frans E. Wielgolaski1 and David W. Inouye2 1

Department of Biology, University of Oslo, Oslo, Norway; University of Maryland, College Park, MD, USA

Key words:

1.

2

Department of Biology,

Biocalendar, Climate change, Experimental phenology, interception, Prediction, Species-specific responses

Phenological

INTRODUCTION

High latitudes are characterized by strong variation in day-length during different seasons of the year. North of the Arctic Circle there is sun 24 hours of the day near the Summer Solstice, but no sun at all six months earlier or later. The sun angle is always low compared to further south, which means that the aspect of slopes strongly influences light conditions. Temperatures generally decrease towards the poles and the growing seasons are shorter; e.g., at the northernmost coast of Norway there are fewer than 100 days with a daily mean temperature above 5°C (Aune 1993). In many parts of northern lowland Fennoscandia, the snow-free period is less than 120 days (Björbekk 1993). Therefore, organisms living at high latitudes have to be adapted to these conditions. This means that plants have to flower relatively soon after snowmelt (Bliss 1971) in order to ripen seeds successfully. Growth of many plant species may start even before all snow has disappeared as observed in maritime Norway (Wielgolaski, pers. obs.). Heide (1985) stated that the more severe the environment, the more important survival adaptations seemed to be, while biological competition tended to be less important. It is difficult to decide where to place the southern limit of “High Latitudes.” The Arctic Circle might be one possibility, but in many ways Schwartz (ed.), PHENOLOGY: AN INTEGRATIVE ENVIRONMENTAL SCIENCE, 175-194 © 2003 Kluwer Academic Publishers. Printed in the Netherlands.

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this definition is too narrow. Summer days are long even further south (Figure 1), and plant photosynthetic activity during the important early summer goes on for many hours every day. In Europe, warm ocean currents keep temperatures higher, particularly near the west coast, compared to North America, and this of course is very important for phenology, especially in spring. Therefore in this paper “High Latitudes” are arbitrarily set to 60°N in western Eurasia, but close to 50°N in North America.

Figure 3.4-1. Variation in sun hours during a year at various high latitudes in Norway.

“Modern” phenology was started in European high latitudes by the Swedish botanist Linné (1751). He presented definitions for the study of bud break, flowering, fruit ripening and leaf coloring in autumn. He also established the first regional phenological network. His main aim was to prepare phenological plant calendars that could be cheap supplements to meteorological measurements for delineating biological zones. Ever since, this has been an important purpose of making phenological observations, particularly in the sparsely populated high latitude regions of the world. However, mainly after the First World War, phenological information was also used in agrometeorology for selection of districts for cultivation of certain crops and fruits, especially in Central Europe (Schnelle 1955), but also at higher latitudes. Many phenological networks were established after the Second World War, e.g. the International Phenological Gardens (IPG) in Europe from the

Chapter 3.4: High Latitude Climates

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early 1960s (see Chapter 2.3 in this volume). Some stations in Fennoscandia were active in this network. Particularly during the 1970s and the 1980s, the interest in phenology decreased in large parts of the world, including Fennoscandia. Therefore, IPG observations were often not continued. A change came in the 1990s because of interest in the effect of Global Change (e.g., Lieth 1997). In this context the old phenological observations, even in remote areas of sparsely populated districts of high latitudes, could be very important (e.g., Klaveness and Wielgolaski 1996), by providing baselines for new phenological information, for example by satellite techniques (Myneni et al. 1997; Högda et al. 2001, 2002). Within the International Tundra Experiment (ITEX) several studies have been carried out in various Arctic areas to see whether experimentally changed microclimate would influence phenology and growth of plants over a few years (e.g., Arft et al. 1999).

2.

HISTORY

The first organized phenological observation program, or network, in the world was established at 18 stations in Sweden and Finland in 1751 by the Swedish botanist Carl von Linné (Johansson 1946, 1953). Most of the older data collections at high latitudes did not last for long periods, and often years are missing in between the periods of observations. However, in Finland phenological data of both plants and animals from the last part of the 1700s and the first part of the 1800s were recovered by Moberg (1857, 1894). Here, it is possible to find, e.g., that, Betula bud break occurred on 9 May 1751 in Turku and 3 May the next year; while in 1797 the same event happened on 25 June in Utsjoki, in northernmost Finland. Phenological observations at high latitudes in Europe (including Russia) have been more common since the mid-1850s. In Finland (then a country within Russia), a monitoring program was started in 1846 by the Finnish Society of Sciences and Letters and continued by the Finnish Meteorological Institute (when it was established in 1881). The Finnish phenological plant observations for the period 1896-1965 were entered into a database by Lappalainen and Heikinheimo (1992). Apparently, phenological data in Finland have been collected more widely than in other countries in Fennoscandia, although in Sweden such data have been presented monthly through many years in reports from the Swedish Meteorological and Hydrological Institute (SMHI). Mean phenological values for various parts of Sweden from 1873 to the 1920s are presented by H.W. Arnell (1923), K. Arnell (1927), and K. Arnell and S. Arnell (1930). In Norway, the first observations of plant phenology for a more scientific purpose took place starting about 1850 (Printz 1865). During the period

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1851-1859 phenological data of both plants and migratory birds were collected in north easternmost Norway (about 70°N). Both these data, and data from the capitol of Norway (now Oslo) for the period 1860-1884, were published by Schübeler (1885). For the end of the 1800s and beginning of the 1900s, long-term phenological observations are mainly known from the southern part of the country (Moe 1928; Lie 1931), but some observations were carried out in Troms County in northern Norway in the same period and particularly from 1910-1911 (Holmboe 1913). Later, however, in 1928, a phenological network was established that lasted to 1952 with some continuation to 1977 (Lauscher 1980; Lauscher et al. 1955, 1959, 1978; Lauscher and Lauscher 1990), and at a few Norwegian sites in the European Phenological Garden using vegetatively propagated plants (Lauscher 1985). There are no references to older phenological studies in Iceland, but recently Thórhallsdóttir (1998) has studied flowering phenology for 11 years. The best-known phenological observations on Greenland were carried out by Sörensen (1941) in the Northeast, mainly through three years in the 1930s. However, Böcher (1938) has also reported some phenological information in his plant studies from Greenland. In North America phenological observations started later than in Europe, although the field has been very active in more recent times (see Chapter 2.4 in this volume). In North American higher latitudes, the only older long-term phenological study on plants and birds was a survey in western Canada by the Royal Society of Canada from the 1890s to 1922, published annually in Proceedings and Transactions of the Royal Society (Beaubien and Freeland 2000). Since then, some phenological studies in higher North American latitudes were carried out in eastern Canada with the lilac/honeysuckle surveys of eastern USA, and some studies in western Canada (Beaubien and Johnson 1994; Beaubien 1996). However, more local phenological observations have been performed (e.g. brief overview in Erskine 1985).

3.

RECENT PHENOLOGY STUDIES

Several phenological studies have been initiated recently at high latitudes, both regionally and in international networks. Some of them are mainly descriptive and form traditional biocalendars. These can be used for agricultural planning and for educational purposes as described in more detail in other chapters of the present volume. Others are mainly experimental studies in controlled chambers and open top chambers, or transplant studies of various ecotypes, or modeling studies. Climate change is a key reason behind studies of phenology today, and the old data are of the


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greatest importance for comparisons with newer ones collected in a traditional way or by satellites. Although phenological studies on plants are mainly reported here, phenological observations have also been made on animals at high latitudes, mainly on migration of birds, but on other animal groups as well (see Chapter 3.5 in this book). Forchhammer et al. (2002) reported that in northern Europe, generally migrants arrived earlier in a district after high NAO winters (mild) than after colder ones. According to Barrett (2002) and Jonzén et al. (2002), however, there has not been a significant long-term trend in the arrival dates in the north for all birds through the last 30 years of the last century.

3.1

Phenological Biocalendars and their Applications

In the tundra projects of the International Biological Program (IBP) in the early 1970s, phenological information was collected in Arctic Canada (Wielgolaski 1974; Bliss 1977). More recently, there have also been phenological studies in the Canadian Arctic (e.g., Woodley and Svoboda 1994) and in forested land in northern Canada (e.g., Colombo 1998). In Russia, phenological spectra or phenograms are given for some plant species on the Kola Peninsula for the period 1994-2000 (Makarova et al. 2001). The time of snowmelt is often considered to be the primary initiator of phenological events in tundra plants (Böcher 1938; Sörensen 1941; Wielgolaski and Kärenlampi 1975; Eriksen et al. 1993; Woodley and Svoboda 1994; Chapter 3.5 in this volume). This seems particularly to be true in the less oceanic alpine and arctic regions, as was shown experimentally by Woodley and Svoboda (1994) by snow removal at sites on Ellesmere Island, Arctic Canada. In more oceanic, snow-rich regions, however, such as the outer Troms County in northern Norway, mountain birch may have green leaves before melting of the winter snow in spring. Growth in herbaceous plants may also start before snowmelt when there is enough light through the snow, if snowmelt is slow as often occurs in maritime high-latitude climates. Thórhallsdóttir (1998) stated that time of snowmelt was likely to influence flowering only after very cold springs with exceptionally late ablation. She says that flowering in oceanic cold climates is normally not linked to snow-free conditions at all. In a survey of the flora of sub-arctic Sweden, Molau (1993) found that populations with normal pollination and seed setting flowered early, while apomictic and viviparous species were found among the later flowering ones. In short and cool summers, he found there was a low proportion of seeds ripening and a reduced seed quality and power of germination. Therefore, vegetative reproduction is very common at high latitudes (e.g.,

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Bliss 1971) and annuals are few, as in high-altitude regions (see Chapter 3.5 in this volume). Most of the current international phenological networks, such as the European Phenological Gardens (Chmielewski and Rötzer 2001; Chmielewski and Rötzer 2002), have few high latitude sites. One reason for this is that many of the plant species chosen for international use cannot stand the harsh climate at high latitudes. Norwegian schools have been involved since 2001 in the GLOBE network for education of school children and data have been submitted to the database from 10 schools. Other regional networks have also been established in northern latitudes in Europe, like the Norwegian Environmental Education Network launched in 2001, with about 70 participating schools by the end of 2002. Most often, the newer time series in phenology at higher latitudes have been short (e.g., Woodley and Svoboda 1994; Diekmann 1996; Karlsen et al. 1998; Wielgolaski 1999; Arft et al. 1999). It is then important that the observations be combined with other approaches, e.g. experiments, to provide insights into phenology. Another valuable approach is to collect information from stations with great differences in climate, which has to be studied at each site, and in other environmental factors, to facilitate correlations between phenology and environmental variables. For example, this approach was used in a three-year study at nearly 60 sites in western Norway along a 300km long fjord penetrating the country from west to east with strong variation from maritime to continental conditions and with steep mountains both to the north and the south of the fjord (e.g., Wielgolaski 1999, 2001). The sites included all aspects from sea level nearly to the tree line, with a climate station at each site. Several plants were studied, both native and cultivated, and woody as well as herbaceous (Wielgolaski 1999). The plants reacted differently to day and night temperatures in various developmental phenophases (Wielgolaski 1974). As expected, the plants also clearly showed different temperature requirements for development, both by plant types and phenophases (Wielgolaski 1999), but temperature requirements were generally lowest for spring phases of early plants. In that study, the author found the lowest air temperature for development (basic or threshold temperature) to leaf bud burst in Prunus padus and flowering in Salix caprea (Figure 2). Leaf bud break of the late sprouting Fraxinus excelsiorr on the other hand was found to have considerably higher basic air temperature, as did both bud break and flowering of pear (‘Moltke’). While Prunus padus showed a low basic temperature for leaf bud break, it needed a relatively high basic air temperature for flowering. Plants growing at low temperatures in high latitudes and altitudes have to be adapted to relatively low basic temperatures to be able to finish their life


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cycle in a short period and/or to be restricted to the warmest places of a district. When the same crop plant variety is cultivated at different latitudes, mean annual temperature sums to reach a specific phenophase normally decreased with increasing latitude (e.g., Strand 1965). In addition to the

Figure 3.4-2. Basic air temperatures found for several plant species in western Norway from the starting date in spring, to leaf bud break and flowering (based on Wielgolaski 1999).

temperature, the photoperiod might have an influence as observed in specific varieties of grass species (e.g., Skjellvåg 1998). Although temperature clearly was the most important environmental factor for phenology in all plants studied at high latitudes, edaphic factors (Wielgolaski 2001) also played some role. Strand (1965) pointed out that in Norway heat sums for plant development in agriculture were higher in clay than in sandy soil and that fertilization also influenced the necessary heat sums. Similarly, Woodley and Svoboda (1994) in Arctic Canada found that fertilization caused an earlier flowering of Salix arctica. Water conditions are also of some importance to phenology even in high latitudes. Wielgolaski (in press) has found in his studies in western Norway that precipitation was important for the development of many plants, even in relatively oceanic areas. For instance a higher number of days with precipitation caused an acceleration of bud break in Betula pubescens. This is probably due to softening of the bud scale in moist air as was also observed by Junttila et al. (1983). Flowering of the extremely early Corylus avellana and the early Salix caprea also seemed to be favored by increased precipitation, probably for the same reasons. In later flowering species, increased precipitation most often delayed the blooming, particularly in

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plants found to have high basic air temperatures (Figure 2). A 12-year study of herb phenology in a Swedish temperate deciduous forest showed that precipitation may be even more important than temperature for flowering the year after (Tyler 2001). In most cases high precipitation during the previous autumn was favorable for flowering, but in Anemone nemorosa low precipitation resulted in more flowers. In Arctic Canada, Woodley and Svoboda (1994) found that irrigation of a dry riverside during the growing season caused a phenological shift in Papaver lapponicum, and an increased length of the budding and flowering periods. It is clear that various plant species react differently to diverse environmental factors (Köppen 1927), sometimes called “phenological interception”, and even in different phenophases within the same species. Therefore, timing of one specific phase in a species can vary between districts of diverse day lengths (i.e., latitude), but also different continentality (e.g., climates with high humidity and moderate temperatures can have different timing for the same phase than climates with high temperatures and lower humidity). This was obvious in the study along the fjord of western Norway (Wielgolaski, in press). Studies like this are important in phenology of all parts of the world, but more so in high latitude and altitude districts with short growing seasons and low temperatures, than in districts with less environmental variation between nearby areas. Phenological interception is found both in native plants, e. g. in leaf bud break of Fraxinus excelsior in relation to Quercus roburr (Batta 1969), and in agricultural ones. Knowledge about such variation in response to environmental factors can be a valuable tool to indicate districts with the best climate for certain plants (e.g., Wielgolaski, in press). In temperate regions, leaf and flower buds of woody plants are normally initiated in the last part of the previous summer (Kramer 1922; Guimond et al. 1998). It might, therefore, be possible to predict the timing of leaf bud burst and flowering in spring based on late phenophases the year before. Wielgolaski (2000) has carried out predictions of leaf bud break and flowering of several native and cultivated woody plants in his three-year study at several sites in western Norway. He correlated these spring phenophases with time of visible bud (mean August 21), bud with color (mean September 20), and flowering (mean September 30) of the perennial plant Aster novi-belgii in the previous autumn. In all cases, the last phase (flowering) showed the highest correlation (often highly significant), and visible bud the lowest and normally insignificant correlations with both leaf bud break and flowering of plants the year after. In Arctic Greenland, Böcher (1938) and Sörensen (1941) found that flower buds were often initiated two and more years before flowering. This indicates that energy is


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built up in the short Arctic growing seasons through one or more years before it is high enough to start the flower initiation.

3.2

Experimental Phenology

In forestry it has been known for many years that transplantation of coniferous tree provenances between southern and northern latitudes has a considerable impact on both phenology and productivity of the trees (Hagem 1931, Kalela 1938, Heikinheimo 1949, Magnesen 1992, Beuker 1994). Planting in the north of southern provenances may cause continuous growth too long in the summer and, therefore, a weak hardening of the shoots by the end of the season. This often has led to frost damage during winter and spring. The well-hardened buds in coniferous trees of the northernmost ecotypes flushed earlier in spring than plants of more southern origin (Beuker 1994). It has also been observed that high latitude populations of Picea abies ended growth earliest in autumn (Morgenstern 1996). Generally, the photoperiod at the site of origin was a dominant factor in determining the timing of cessation in northern plants (Partanen and Beuker 1999). Recently, similar transplant studies have been carried out on Nordic mountain birch ((Betula pubescens ssp. czerepanovii) between oceanic and continental districts in northern Fennoscandia, and by transplantation of southern birch provenances to the north. Phenological observations over ten years have shown that the northernmost mountain birch ecotypes (from 7071°N) also ended growth earliest in the autumn when grown at the same site (Ovaska et al., in press). Oceanic northern provenances probably were somewhat earlier in ending growth in autumn than the more continental ones from similar latitudes. Both oceanic and relatively continental ecotypes of mountain birch from southern latitudes (60-64°N) showed a longer growing season when planted in more northern districts (e.g. about 68°N) than the northern provenances, being nearly green on September 10 when the northern ones were yellow and red (Ovaska et al., in press). In transplantation to oceanic districts, survival was better for oceanic provenances, while for transplantation to a continental region the survival rate was lowest in the southernmost and westernmost ecotypes where the height growth was also lower. Also, in an oceanic district, the northernmost plants were tallest after ten years. As found in coniferous plants the leaf bud break of mountain birch in spring was later in plants of southern and in particular oceanic origins, than in northern provenances transplanted and grown both in oceanic and continental districts at about 68°N (Ovaska et al., in press). The bud-burst of Betula pubescens provenances of various latitudes and continentality has also been studied in controlled climate (Myking and Heide

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1995; Myking 1997). It was found that plants native to mild and unstable winters (as in the south and along the coast of Norway) were released later from dormancy than those from regions with cold and stable winters (Figure 3), probably due to adaptation to avoid frost damage. The early dormancy in northern ecotypes (about 69°N), Myking (1999) stated, could be a decisive adaptation to a short growing season and hardening of the shoots at short days in time to avoid autumn frost. He also found that a period of chilling (below 10°C) was necessary for bud-burst of B. pubescens, but the natural chilling period is normally long enough even in southern and oceanic sites at latitudes above 60°N. Long photoperiods significantly reduced time to leaf bud break in partly dormant buds, but not when dormancy was fully released. However, there may be increasing experimental evidence that light conditions play some role in the timing of spring phenology (Linkosalo et al. 2000). According to Heide (1993) dormancy in B. pubescens, as well as in B. pendula and Prunus padus was released as early as December, while in Alnus sp. it was not until February.

Figure 3.4-3. Days to bud-burst in an eight-hour (short-day) photoperiod, after different periods of chilling at 5°C in Betula pubescens provenances along two gradients. a. Latitudinal gradient from 56°N (Denmark), 64°N (Mid – Norway) to 69°N (North – Norway). b. Coastalinland gradient in Norway below 150 m a.s.l. at about 60°N (reprinted from Myking 1999, Figure 2, p. 142, in Phyton, 39, used with permission).


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Similarly, Hannerz (1999) suggested that a chilling requirement for Picea abies was fulfilled in December even somewhat south of 60°N in Fennoscandia. Leinonen (1996), however, generally observed that chilling requirements increased in Pinus sylvestris and Betula pendula for coastal populations compared to the more continental ones. Hänninen (1995) concluded that chilling temperature is the major environmental factor regulating rest break, but premature leaf bud break seemed not to be any serious problem for frost damage, according to models of bud-burst phenology of trees from cool and temperate regions. In North America, the arctic deciduous shrub species Salix pulchra and Betula nana were also found to have a chilling requirement before bud burst (Pop et al. 2000). According to studies in growth chambers, however, this probably played a lesser role in bud break in nature because the plants easily met their chilling requirement during winter. The ITEX (International Tundra Experiment) project was established at several sites in the Northern Hemisphere to study the influence of temperature and wind shields on vegetative and reproductive growth and development in arctic and alpine plants. Open top chambers with transparent walls were placed in the field for one to four years (Arft et al. 1999). In addition to increasing the temperature, the chambers also altered the light, moisture and gas exchange somewhat, but these side effects were minimized. It was observed that in the warmer, Low Arctic sites, the strongest response was in vegetative growth, particularly by herbaceous plants, while colder High Arctic sites produced a greater reproductive response. The better opportunities to use energy for investment in flowering and development of seeds afforded by increased temperatures in the High Arctic may provide an opportunity for species to colonize patches of bare ground (Robinson et al. 1998). At the semi-desert Svalbard site, there was a strong effect of temperature increment on the flowering of Dryas octopetala and also on seed setting (Wookey et al. 1993). While the key phenological events such as leaf bud burst and flowering occurred earlier in the warmer chambers throughout the study period, there was little impact on growth cessation at the end of the season. This may show that the photoperiod plays a more important role than temperature in late-season phenology of high latitudes (e. g., Barnes et al. 1998). Some studies, however, may also indicate a possible delayed senescence in the ITEX chambers (e.g., Molau 1997; Stenström et al. 1997).

3.3

Climate Change

Global warming is expected to cause greater increases in temperatures and precipitation during winter than summer (Dickinson 1986; Maxwell

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1997). The most pronounced predicted changes are in models of northern latitudes. The North Atlantic Oscillation (NAO) seems to be responsible for a large component of the increased temperature in Europe (Post and Stenseth 1999). According to Chmielewski and Rötzer (2001) the positive phase of NAO has increased clearly in Europe in the period February-April through the past several years, leading to prevailing westerly winds and thus to higher temperatures, particularly since the end of the 1980s. In most of the higher latitudes an increased winter precipitation has caused stronger snow accumulation. Despite that, increased temperature has led to earlier snowmelt and longer annual snow-free season in most regions (Maxwell 1992), an earlier and longer growing season (Bliss and Matveyeva 1992; Oechel and Billings 1992) and increased rates of plant population growth (Carlsson and Callaghan 1994). However, in areas of Fennoscandia with low winter temperatures, as in high mountain areas of Norway and inner parts of northern Fennoscandia, the higher winter precipitation (predicted to increase about 1.5% per decade

Figure 3.4-4. Change in onset of spring in Fennoscandia from 1992 to 1998 on the basis of the GIMMS NDVI dataset (reprinted from Högda et al. 2001, used with permission of the first author, NORUT IT, Tromsö).


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at Finnmarksvidda according to Hanssen-Bauer et al. 2001) may have caused longer lasting snow cover in spring. This was observed by satellite inventory (GIMMS) NDVI maximum values (Myneni et al. 1997) despite higher temperatures (predicted as 0.5°C per decade at Finnmarksvidda, according to Hanssen-Bauer et al. 2000). Thus, a later onset of spring (Figure 4) was observed in some places during 17 years (1982-1998) of study (Högda et al. 2001). The strongest delay (approximately one week) occurred in the most continental areas of northern Fennoscandia and correlated well with colder April and May and with an increased snow cover. In most of Fennoscandia, the autumn was delayed and, therefore, the growing season generally increased in the region, again except for the northern continental section, where a decrease of approximately one week was observed (Högda et al. 2001). Using a similar technique it was demonstrated that starting dates of birch pollen seasons were delayed in the same regions as the delay of spring, but earlier in all other parts of Fennoscandia (Högda et al 2002). Plant responses to climate change in northern latitudes can be predicted by modeling phenological data from experiments studying the effect of temperature changes in growth chambers (e. g., Hänninen 1995; Hannerz 1999; Pop et al. 2000), studies of changes in weather variables as described above, and by models or indices of biosphere response, e. g. based on some average of plant phenology of various species (Schwartz 1997; Schwartz 1998; Chmielewski and Rötzer 2001). In high latitudes a warmer climate has caused a higher altitude tree line (Kullman 2000; Skre 2001), and an increased biodiversity is expected in many districts because of global warming, e.g. in the High Arctic due to better seed production (Philipp et al. 1990; Arft et al. 1999). Late-flowering arctic species that now only rarely ripen their seed may do so more regularly with increasing temperatures (Thórhallsdóttir 1998). Kramer et al. (2000) concluded that there are significant differences between the ways various tree species respond to climate change. Earlier in this chapter, it was stated that various plants reacted differently to environmental factors, also during various phenophases (Wielgolaski, in press). All this means that there might be rather large changes in biodiversity because of climate change, even in the more southern and temperate parts of high latitudes. By comparison of plant phenology from old data sets with the same phenophase of more recent observations at a site, it is possible to see changes that may be a result of climate change. In Norway this has been done for the first flowering date of some species in the second half of the 1800s compared with the same species in the second quarter of the 1900s (1928-1952) and the third quarter of the century (1952-1972) in three areas: south-eastern coastal district (Oslo) at about 60°N, an elevated inland district

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Figure 3.4-5. Scatter-plot of mean first flowering days (FFDs) in various plant species at stations in Finnmark (y-axis), 1928-52 (dots) and 1952-72 (triangles), plotted against mFFDs from Finnmark (Nyborg) 1851-59 (x-axis) (reprinted from Klaveness and Wielgolaski 1996, used with permission).

Figure 3.4-6. Scatter-plot of mean first flowering days (FFDs) in various plant species at 10 stations in Oslo plotted against mFFDs from Christiania (Oslo) 1860-84, with 95% C.I. calculated for n=25 years (reprinted from Klaveness and Wielgolaski 1996, used with permission).


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of southern Norway at about 61°N, and in the far north-east at about 71°N (Klaveness and Wielgolaski 1996). The species responded differently between the periods. However, most later-flowering species were earlier in Oslo and in north-easternmost Norway (Figures 5 and 6) in the 1900s and particularly in the last period of the century. In early spring, on the other hand, there were no differences between the periods. In the inland district of southern Norway, no differences were seen between the various periods. Menzel (2000) and Chmielewski and Rötzer (2001) have reported from Central Europe that generally the leaf bud break in spring of trees from 1960 to the end of the century was more than 0.2 days/year earlier, while the autumn phases were delayed by about 0.15 days/year, causing longer growing seasons. Similarly, Beaubien and Freeland (2000) reported the first bloom of the early flowering Populus tremuloides to be 0.27 days/year earlier in a long term-study (1900-1977) at Edmonton, Canada. In Finland, however, phenological data did not permit reliable estimates of the effect of climate change on spring in boreal trees (Linkosalo 2000).

4.

CONCLUSION

At high latitudes, there are large differences between species-specific responses to environmental factors. The responses also vary between geographical districts or continentality and within a species at different times of the year. In many cases phenology may be used in climate change studies, but then there must be a clear description of the sites used in the study: geographically, climatically and edaphically, as well as clear definitions of the phenophases studied and the state of the organism.

REFERENCES CITED Arft, A. M., M. D. Walker, J. Gurevitch, J. M. Alatalo, M. S. Bret-Harte, M. Dale, M. Diemer, F. Gugerli, G. H. R. Henry, M. H. Jones, R. D. Hollister, I. S. Jonsdottir, K. Laine, E. Levesque, G. M. Marion, U. Molau, P. Mölgaard, U. Nordenhäll, V. Raszhivin, C. H. Robinson, G. Starr, A. Stenström, M. Stenström, Ö. Totland, P. L. Turner, L. J. Walker, P. J. Webber, J. M. Welker, and P. A. Wookey, Responses of tundra plants to experimental warming: Meta-analyses of the International Tundra Experiment, Ecol. Monographs 69, 491-511, 1999. Arnell, H. W., Vegetationens aarliga utvecklingsgaang i Svealand. Medd. Statens Meteorologisk - Hydrografiska Anstalt, 2, 1-80, (German abstr. 74-80), 1923. Arnell, K., Vegetationens utvecklingsgaang i Norrland. Medd. Statens Meteorologisk – Hydrografiska Anstalt, 4, 1-28, (German abstr. 28), 1927. Arnell, K., and S. Arnell, Vegetationens utveckling i Götaland. Medd. Statens Meteorologisk – Hydrografiska Anstalt, 6, 1-70, (German abstr. 69-70), 1930.

190


Aune, B., Aarstider og vekstsesong. Kartblad (Map) 3.1.7., scale 1:7 mill., in Nasjonalatlas for Norge, Det norske meteorologiske institutt – Statens kartverk, Oslo – Hönefoss, 1993. Barnes, B. V., D. R. Zak, S. R. Denton, and S. H. Spurr, Forest tree variation, in Forest Ecology, pp. 63-93, John Wiley, New York, 1998. Barrett, R.T., The phenology of spring bird migration to north Norway, Bird Study, 49, 270277, 2002. Batta, J., Variasjoner i tid for bladsprett hos ask og eik, (Engl. summary), Aarsskr. Planteskoledrift Dendrologi, 14-15, 78-85, 1969. Beaubien, E. G., Plantwatch, a model to initiate phenology in school classes, Phenol. Season., 1, 33-35, 1996. Beaubien, E. G., and H. J. Freeland, Spring phenology trends in Alberta, Canada: links to ocean temperature, Int. J. Biometeorol., 44, 53-59, 2000. Beaubien, E.G., and D. L. Johnson, Flowering plant phenology and weather in Alberta, Canada, Int. J. Biometeorol., 38, 23-27, 1994. Beuker, E., Adaptation to climatic changes of the timing of bud burst in populations of Pinus sylvestris L. and Picea abies (L.) Karst., Tree physiology, 14, 961-970, 1994. Björbekk, G., Snö. Kartblad (Map) 3.1.4., scale 1.7 mill., in Nasjonalatlas for Norge, Det norske meteorologiske – Statens kartverk, Oslo – Hönefoss, 1993. Bliss, L.C., Arctic and alpine life cycles, Ann. Rev. Ecol. Syst., 2, 405-438, 1971. Bliss, L.C. (Editor), Truelove Lowland, Devon Island, Canada: A High Arctic Ecosystem, University of Alberta Press, Edmonton, 714 pp., 1977. Bliss, L.C., and N. V. Matveyeva, Circumpolar arctic vegetation, in Arctic Ecosystems in a Changing Climate, edited by F. S. Chapin III, R. L. Jefferies, J. F. Reynolds, G. R. Shaver and J. Svoboda, pp. 59-89, Academic, New York, 1992. Böcher, T. W., Studies on the vegetation of the east coast of Greenland, Medd. Grönl., 104, 132, 1938. Carlsson, B.A., and T. V. Callaghan, Impact of climate change factors on the clonal sedge Carex bigelowii: implication for population growth and vegetative spread, Ecography, 17, 321-330, 1994. Chmielewski, F.-M., and T. Rötzer, Response of tree phenology to climate change across Europe, Agricul. Forest Meteorol., 108, 101-112, 2001. Chmielewski, F.-M., and T. Rötzer, Annual and spatial variability of the beginning of growing season in Europe in relation to air temperature changes, Clim. Res., 19, 257-264, 2002. Colombo, S. J., Climatic warming and its effect on bud burst and risk of frost damage to white spruce in Canada, For. Chron., 74, 567-577, 1998. Dickinson, R., The climate system and modelling of future climate, in The Greenhouse Effect, Climate Change, and Ecosystem, edited by B. Bolin, B. Doos, J. Jager and R.A. Warrick, pp. 207-270, Wiley, Chichester, UK, 1986. Diekmann, M., Relationship between flowering phenology of perennial herbs and meteorological date in deciduous forests of Sweden, Can. J. Bot. 74, 528-537, 1996. Eriksen, B., U. Molau, and M. Svensson, Reproductive strategies in two arctic Pedicularis species (Scrophulariaceae), Ecography, 16, 154-166, 1993. Forchhammer, M. C., E. Post, and N. C. Stenseth, North Atlantic Oscillation timing of longand short-distance migration, J. Animal Ecol., 71,1002-1014, 2002. Erskine, A. J., Some phenological observations across Canada’s boreal regions, Can. FieldNat., 99, 188-195, 1985. Guimond, C. M., P. K. Andrews, G. A. Lang, Scanning electron microscopy of floral initiation in sweet cherry, J. Am. Soc. Hort. Sci., 123, 509-512, 1998.


191

Hagem, O., Forsök med vestamerikanske traeslag, (German summary), Medd. Vestl. Forstl. Forst., 12, 1-217, 1931. Hannerz, M., Evaluation of temperature models for predicting bud burst in Norway spruce, Can. J. For. Res., 29, 9-19, 1999. Hänninen, H., Effects of climate change on trees from cool and temperate regions: an ecophysiological approach to modelling of bud burst phenology, Can. J. Bot. 73, 183-199, 1995. Hanssen-Bauer, I., O. E. Tveito, and E. J. Förland, Temperature scenarios for Norway: Empirical downscaling from the ECHAM4/OPYC3 GSDIO integration, Det norske meteorologiske institutt, Report 24, 1-53, 2000. Hanssen-Bauer, I., O. E. Tveito, and E. J. Förland, Precipitation scenarios for Norway: Empirical downscaling from the ECHAM4/OPYC3 GSDIO integration, Det norske meteorologiske institutt, Report 10, 1-39, 2001. Heide, O. M., Physiological aspects of climatic adaptation in plants with special references to high-latitude environments, in Plant Production in the North, edited by Aa. Kaurin, O. Junttila and J. Nilsen, pp. 1-22, Norwegian University Press, Tromsö, 1985. Heide, O. M., Daylength and thermal time response of budburst during dormancy release in some northern deciduous trees, Physiol. Plant., 88, 531-540, 1993. Heikinheimo, O., Results of the experiments on the geographical races of spruce and pine, (in Finnish with English summary), Comm. Inst. For. Fenn., 37, 1-44, 1949. Högda, K. A., S. R. Karlsen, and I. Solheim, Climatic change impact on growing season in Fennoscandia studied by a time series of NOAA AVHRR NDVI data, Proc. IGARSS 2001, Sydney, Australia, ISBN 0-7803-7033-3, pp. 1-3, 2001. Högda, K. A., S. R. Karlsen, I. Solheim, H. Tömmervik, and H. Ramfjord, The start dates of birch pollen seasons in Fennoscandia studied by NOAA AVHRR NDVI data, Proc. IGARSS 2002, Toronto, Canada, ISBN 0-7803-7536-X, pp. 1-3, 2002. Holmboe, J., Vaarens utvikling i Tromsö amt, (in Norwegian), Bergens Mus. Aarb., 1912, 1248, 1913. Johansson, O. V., Det fenologiska observationsmaterialet i Finland och provstudier av detsamma, (in Swedish), Finlands Natur och Folk, 88(8), 1-118, 1946. Johansson, O. V., Die Phänologie in Finland, Soc. Sci. Fenn., Comm. Biol., 11(1), 1-55, 1953. Jonzén, N., A. Hedenström, C. Hjort, Å. Lindström, P. Lundberg, and A. Andersson, Climate patterns and the stochastic dynamics of migratory birds, Oikos, 97, 329-336, 2002. Junttila, O., C. Stushnoff, and L. V. Gusta, Dehardening in flower buds of saskatoon-berry, Amelanchier alnifolia, in relation to temperature, moisture content, and spring bud development, Can. J. Bot., 61, 164-170, 1983. Kalela, A., Zur Synthese der experimentellen Untersuchungen über Klimarassen der Holzarten, Comm. Inst. For. Fenn., 26, 1-445, 1938. Karlsen, S. R., H. Tömmervik, I. Solheim, B. Johansen, K. A. Högda, and O. Engelsen, Satellite based phenology study in eastern part of Finnmark, northern Norway, NORUT IT 450/15-98, ISBN 82-7747-094-0, pp. 1-35, NORUT, Tromsö, 1998. Klaveness, D., and F. E. Wielgolaski, Plant phenology in Norway – a summary of past and present first flowering dates (FFDs) with emphasis on conditions within three different areas, Phenol. Season., 1, 47-61, 1996. Köppen, W., Wechsel der phänologischen Zeitenfolge, Meteorol. Z., 44, 175-177, 1927. Kramer, K., I. Leinonen, and D. Loustau, The importance of phenology for the evaluation of impact of climate change on growth of boreal, temperate and Mediterranean forests ecosystems: an overview, Int. J. Biometeorol., 44, 67-75, 2000.

192


Kramer, O., Über die Blütenknospen und der Zeitpunkt der Entstehung von Blütenanlagen bei einigen Obstsorten, Dtsch. Obstbauztg., 68, 306-308. 1922. Kullman, L., Tree-limit rise and recent warming: a geoecological case study from the Swedish Scandes. Norsk geogr. Tidsskr., 54, 49-59, 2000. Lappalainen, H., and M. Heikinheimo, Relations between climate and plant phenology. Part 1. Survey of plant phenological observations in Finland from 1896 to 1965, Meteorol. Publ. Finland, 20, 1-74, 1992. Lauscher, F., Klima, Klimaschwankungen und phänologischer Jahresablauf am europäischen Nordkap, Mitt. Österr. Geogr. Ges., 122, 193-220, 1980. Lauscher, F., Zur Phänologie vegetativ vermehrter Pflanzen einheitlicher Herkunft – Beobachtungen in phänologischen Pflanzgärten in Norwegen 1963-1982, Phyton (Horn, Austria), 25, 253-272, 1985. Lauscher, A., and F. Lauscher, Phänologie Norwegens, Teil IV, Private edition, pp. 1-13 + Anhang 1-3 (16+103+120 pp.), 1990. Lauscher, A., F. Lauscher, and H. Printz, Die Phänologie Norwegens, Teil I, Allgemeine Übersicht, Skr. Det Norske Videnskaps-Akademi Oslo, 1, Mat.-Naturv. Kl., No. 1 1955, 199, 1955. Lauscher, A., F. Lauscher, and H. Printz, Die Phänologie Norwegens, Teil II, Phänologische Mittelwerte für 260 Orte, Skr. Det Norske Videnskaps-Akademi Oslo, 1, Mat.-Naturv. Kl. No.1 1959, 1-176, 1959. Lauscher, A., F. Lauscher, and H. Printz, Die Phänologie Norwegens, Teil III, TabellenKarten der Mittelwerte, Skr. Det Norske Videnskaps-Akademi Oslo, 1, Mat.-Naturv. Kl. Ny Serie No.37, 1-253, 1978. Leinonen, I., Dependence of dormancy release on temperature in different origins of Pinus sylvestris and Betula pendula seedlings, Scand. J. For. Res., 11, 122-128, 1996. Lie, H., Faenologiske noteringar fraa Telemark, (in Norwegian), Tidsskr. Norske Landbruk, 38, 204-206, 1931. Lieth, H., Aims and methods in phenological monitoring, in Phenology in Seasonal Climates II, edited by H. Lieth and M. D. Schwartz, pp. 1-21, Backhuys Publ., Leiden, 1997. Linkosalo, T., Analyses of the spring phenology of boreal trees and its response to climate change, Univ. Helsinki Dept. For. Ecol., Publ. 22, ISBN 951-45-9362-6, ISSN 1235-4449, 1-55. 2000. Linkosalo, T., T. R. Carter, R. Häkkinen, and P. Hari, Predicting spring phenology and frost damage risk of Betula spp. Under climatic warming: a comparison of two models, Tree Physiol., 20, 1175-1182, 2000. Linne, C., Philosophia Botanica, (in Latin), Kiesewetter, Stockholm, Climate and phenology pp. 263-277, 1751. Magnesen, S., Injuries on forest trees related to choice of the species and provenances: A literature survey of a one hundred year epoch in Norwegian forestry, Rep. Skogforsk, 7, 146, 1992. Makarova, O.A., A. A. Pohilko, and J. A. Kushel, Seasonal life of the nature in Kola Peninsula, (in Russian, translated in English), Murmansk, ISBN 5-7744-0102-2, 1-68, 2001. Maxwell, B., Arctic climate: potential for change under global warming, in Arctic Ecosystems in a Changing Climate, edited by F. S. Chapin III, R. L. Jefferies, J. F. Reynolds, G. R. Shaver and J. Svoboda, pp. 11-34, Academic Press, New York, 1992. Maxwell, B., Recent climate patterns in the Arctic, in Global Change and Arctic Terrestrial Ecosystems, edited by W. C. Oechel, T. Callaghan, T. Gilmanov, J. I. Holten, B. Maxwell, U. Molau and B. Sveinbjörnsson, pp. 21-46, Springer-Verlag, Heidelberg, 1997.


193

Menzel, A., Trends in phenological phases in Europe between 1951 and 1996, Int. J. Biometeorol. 44, 76-81, 2000. Moberg, A., Naturalhistoriska daganteckningar gjorda i Finland aaren 1750-1845, (in Swedish), Förh. Sällsk. Fauna Flora Fenn., 3, 95-250, 1857. Moberg, A., Fenologiska iakttagelser i Finland aaren 1750-1845 (in Swedish), Finlands Natur Folk, 55, 1-165, 1894. Moe, A., Dates of flowering for native and garden plants at Stavanger 1897-1926, Skr. Det Norske Videnskaps-Akademi Oslo, 1, Mat.-Naturv. Kl. No.3, 1-50, 1928. Molau, U., Relationship between flowering phenology and life history strategies in tundra plants, Arctic Alpine Res., 25, 391-402, 1993. Molau, U., Responses to natural climatic variation and experimental warming in two tundra plant species with contrasting life forms: Cassiope tetragona and Ranunculus nivalis, Global Change Biology, 3, (Suppl. 1), 97-107, 1997. Morgenstern, E. K., Environmental influences and geographic variation, in Geographic variation in forest trees, pp.45-89, UBC Press, Vancouver, 1996. Myking, T., Dormancy, budburst and impacts of climatic warming in coastal-inland and altitudinal Betula pendula and B. pubescens ecotypes, in Phenology in Seasonal Climates I, edited by H. Lieth and M. D. Schwartz, pp. 51-66, Backhuys Publ., Leiden, 1997. Myking, T., Winter dormancy release and budburst in Betula pendula ROTH and B. pubescens EHRH. ecotypes, Phyton (Horn, Austria), 39(4), 139-145, 1999. Myking, T., and O. M. Heide, Dormancy release and chilling requirement of buds of latitudinal ecotypes of Betula pendula and B. pubescens, Tree Physiol. 15, 697-704, 1995. Myneni, R. B., C. D. Keeling, C. J. Tucker, G. Asrar, and R. R. Nemani, Increased plant growth in the northern latitudes from 1981 to 1991, Nature, 386, 698-702, 1997. Oechel, W. C., and W. D. Billings, Effects of global change on the carbon balance of arctic plants and ecosystems, in Arctic Ecosystems in a Changing Climate, edited by F.S. Chapin III, R. L. Jefferies, J. F. Reynolds, G. R. Shaver and J. Svoboda, pp. 139-168, Academic Press, New York, 1992. Ovaska, J. A., J. Nilsen, F. E. Wielgolaski, H. Kauhanen, R. Partanen, S. Neuvonen, L. Kapari, O. Skre, and K. Laine, Phenology and performance of mountain birch provenances in transplant gardens: latitudinal, altitudinal and oceanity-continentality gradients, in Plant Ecology, Herbivory and Human Impact in Nordic Mountain Birch Forests, edited by F. E. Wielgolaski (in press), Springer-Verlag, Heidelberg, (anticipated in 2004). Partanen, J., and E. Beuker, Effects of photoperiod and thermal time on the growth rhythm of Pinus sylvestris seedlings, Scand. J. For. Res., 14, 487-497, 1999. Philipp, M., J. Böcher, O. Mattson, and S. R. J. Woodell, A quantitative approach to the sexual reproductive biology and population structure in some arctic flowering plants: Dryas integrifolia, Silene acaulis and Ranunculus nivalis, Medd. Grönland, Biosci., 34, 160, 1990. Pop, E. W., S. F. Oberbauer, G. Starr, Predicting vegetative bud break in two arctic deciduous shrub species, Salix pulchra and Betula nana, Oecologia, 124, 176-184, 2000. Post, E., and N. C. Stenseth, Climatic variability, plant phenology, and northern ungulates, Ecology, 80, 1322-1339, 1999. Printz, H. C., Beretning om en i Sommeren 1864 foretagen botanisk Reise i Valders, (in Norwegian), Nyt Mag. Naturv., 14, 51-96, 1865. Robinson, C. H., P. A. Wookey, J. A. Lee, T. V. Callaghan, and M. C. Press, Plant community responses to simulated environmental change at a High Arctic polar semidesert, Ecology, 79, 856-866, 1998.

194


Rötzer, T., and F. -M. Chmielewski, Phenological maps of Europe, Clim. Res., 18, 249-257, 2001. Schnelle, F., Pflanzen-Phänologie, Geest & Portig, Leipzig, 299 pp., 1955. Schübeler, F. C., Viridarium Norvegicum, Norges Vaextrige, Et Bidrag til Nord-Europas Natur-og Kulturhistorie, 1ste bind, (in Norwegian), Phenology etc., pp. 1-184, Climatic, pp. 185-195, W. C. Fabritius, Christiania, 610 pp., 1885. Schwartz, M. D., Spring index models: an approach to connecting satellite and surface phenology, in Phenology in Seasonal Climates II, edited by H. Lieth and M. D. Schwartz, pp. 23-38, Backhuys Publ., Leiden, Netherlands, 1997. Schwartz, M. D., Green-wave phenology, Nature, 394, 839-840, 1998. Skjellvåg, A. O., Climatic conditions for crop production in Nordic countries, Agr. Food Sci. Finland, 7, 149-160, 1998. Skre, O., Climate change impact on mountain birch ecosystems, inn Nordic Mountain birch ecosystems, edited by F. E. Wielgolaski, pp. 343-357, UNESCO, Paris and Parthenon Publ. Group, New York and London, 2001. Sörensen, T., Temperature relations and phenology of the Northeast Greenland flowering plants, Medd. Grönl., 125, 1-307, 1941. Stenström, M., F. Gugerli, and G. H. R. Henry, Response of Saxifraga oppositifolia L. to simulated climate change at three contrasting latitudes, Global Change Biology, 3, (Suppl. 1), 44-54, 1997. Strand, E., Forelesning i plantekultur, (in Norwegian), Norges landbrukshögskole, Aas, 73 pp., 1965. Thórhallsdóttir, T. E., Flowering phenology in the central highland of Iceland and implications for climatic warming in the Arctic, Oecologia, 114, 43-49, 1998. Tyler, G., Relationships between climate and flowering of eight herbs in a Swedish deciduous forest, Ann. Bot. 87, 623-630, 2001. Wielgolaski, F. E., Phenology in agriculture in Phenology and Seasonality Modeling, edited by H. Lieth, pp. 369-381, Springer-Verlag, New York, 1974. Wielgolaski, F. E., Starting dates and basic temperatures in phenological observations of plants, Int. J. Biometeorol., 42, 158-168, 1999. Wielgolaski, F. E., Predictions in plant phenology, paper presented at Int. Congress: Progress in Phenology, Freising, Germany, October 2000. Wielgolaski, F. E., Phenological modifications in plants by various edaphic factors, Int. J. Biometeorol., 45, 196-202, 2001a. Wielgolaski, F. E., Climatic factors governing plant phenological phases along a Norwegian fjord, Int. J. Biometeorol., 47(4), in press, 2003. Wielgolaski, F. E., and L. Kärenlampi, Plant phenology of Fennoscandian tundra areas, in Fennoscandian Tundra Ecosystems. Part1: Plants and Microorganisms, edited by F. E. Wielgolaski, pp. 94-102, Springer-Verlag, Heidelberg, 1975. Woodley, E.J., Svoboda, J. Effects of habitat on variations of phenology and nutrient concentration among four common plant species of the Alexandra Fiord Lowland, in Ecology of a Polar Oasis, Alexandra Fiord, Ellesmere Island, Canada, edited by J. Svoboda and B. Freedman, pp. 157-175, Captus Univ. Press, Toronto, 1994. Wookey, P. A., A. N. Parsons, J. M. Welker, J. A. Potter, T. V. Callaghan, and M. C. Press, Comparative responses of phenology and reproductive development to simulated environmental change in sub-arctic and high arctic plants, Oikos, 67, 490-502, 1993.

Chapter 3.5 HIGH ALTITUDE CLIMATES David W. Inouye1 and Frans E. Wielgolaski2 1

Department of Biology, University of Maryland, College Park, MD, USA; 2Department of Biology, University of Oslo, Oslo, Norway

Key words:

1.

Alpine, Montane, Snowpack, Subalpine, Rocky Mountains

INTRODUCTION

Phenology at high altitudes differs from that in most other habitats in four significant ways. First, for much (sometimes the majority) of the calendar year these habitats may be under snow or ice, and there is little photosynthetic activity. Consequently (and second), there is a very short growing season delimited by a combination of temperature and snowpack. Third, this may be one of a few habitats where almost all phenology is tied to a single highly variable event, the timing of snowmelt; few high-altitude plants appear to exhibit photoperiodic responses for phenological events. And finally, high altitudes may differ from other habitats in the way that global climate change is affecting phenology. What is a high altitude? The answer is not as obvious as it might seem. It probably makes more sense to use an ecosystem definition rather than an absolute altitude, as what constitutes a high altitude at high latitudes differs from a high altitude at mid- or low latitudes. For the purposes of this chapter we will consider “high altitude” to refer to alpine or montane ecosystems. Alpine is defined as the area above the natural limit of trees, and it extends over a wide latitudinal and altitudinal range. Another way of defining it, in climatic terms, is that its lower elevational limit corresponds well to the 10°C isotherm for the warmest summer month (Wardle 1974). The alpine Schwartz (ed.), PHENOLOGY: AN INTEGRATIVE ENVIRONMENTAL SCIENCE, 195-214 © 2003 Kluwer Academic Publishers. Printed in the Netherlands.

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shares many characteristics with high-latitude or arctic ecosystems (Bliss 1971, and see Chapter 3.4 in this book), but from a phenological perspective one big difference is the much longer day lengths during the arctic growing season. Montane ecosystems are less clearly defined, but would include the ecosystem between grasslands on the lower end and the alpine on the upper end; the term subalpine applies to the upper end of the montane. There are not as many long-term studies of phenology at high altitudes as there are of low altitudes. In fact, there do not appear to be any studies longer than the one described in this chapter that was initiated in 1973. Thus some of the discussion in this chapter will be colored by the fact that Inouye has worked for most of his research career at a single high-altitude field station, the Rocky Mountain Biological Laboratory (RMBL). Perhaps the information in this chapter will help to stimulate the initiation of other studies.

2.

THE HIGH-ALTITUDE CLIMATE

Mountains have been described as “generating their own climate”, due to the effect of their mass on circulation patterns, precipitation, and radiation. This creates abundant variation of the climate within mountain regions, but also some general patterns that help to differentiate high altitude climate, and hence phenology, from that at lower altitudes. Kittel et al. (2002) go into detail about elevation dependence of climate, which can be attributed to factors at high altitudes such as closer contact to the free troposphere, decoupling from convective mixing of the lower troposphere, and snowalbedo feedback. Within the Rocky Mountains, there is a classic orographic precipitation pattern that creates increased precipitation on the west (windward) side of the mountains and a rain shadow on the east, although some winter air masses create up-slope conditions on the east side that generate precipitation there. In all areas of the Rocky Mountains, total precipitation increases significantly with elevation (Kittel et al. 2002), with the highest precipitation occurring near the peak elevations (this is true for the Alps also, Theurillat and Guisan 2001, and in the Scandinavian mountains). Maximum and minimum temperatures decrease strongly with increasing altitude throughout the Rocky Mountains (Kittel et al. 2002), although there are some interesting variations. For example, variation of maximum temperatures decreases with elevation in the winter while that of minimum temperatures increases during the summer, and at lower elevations in the central Rockies, temperatures can be colder than those at similar elevations in the north (due to the influence of continental vs. maritime air masses).

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An analysis of historical data shows that there are significant centuryscale positive trends for annual and seasonal precipitation and mean minimum temperature in the U.S. Rocky Mountains (Kittel et al. 2002). Some of these are quite striking; in the northern and central Rockies summer precipitation has increased by 30% and 33% over the past century. There has also been a trend for increasing annual mean minimum temperature (0.7 – 0.9ºC for the northern and central mountains). It is probable that these changes, and those forecast for the future, will have consequences for phenology at high altitudes. Giorgi et al. (1997) predicted similar changes for temperature over an altitudinal range in the Swiss Alps, and suggested “... that high elevation temperature change could be used as an early detection tool for global warming.” Both large- and small-scale events can affect high-altitude phenology. For example, the El Niño Southern Oscillation (ENSO) and the North Pacific Oscillation (or Pacific Decadal Oscillation) can affect winter precipitation in the Rocky Mountains. At the other extreme, microclimate can have very large effects. Areas where snow is deposited by wind (on the lee side of ridges, trees, etc.) can melt out much later than nearby sites, and deposition by snow slides and avalanches may create such deep snow depths that certain areas may not melt out at all in a given summer. Wagner and Reichegger (1997) found that a north-facing study site subject to deep snow deposition took about a month longer to melt out than sunlit sites. The cold water from melting snowbanks can have an effect on the phenology of plants it reaches. Holway and Ward (1963) found in an experimental study that meltwater resulted in delays of flowering in 12 of 14 species growing in irrigated plots (typically of about a week, but up to a month). Another aspect of high-altitude phenology that is unique to areas with great topographic relief is the potential for phenological inversions. Thermal inversions through cold air drainage can have phenological consequences. Lynov (1984) reported statistically significant effects of such phenological inversions for eight species of trees and shrubs, with delays of 2 – 5 days in times of bud opening and flowering. Areas where this cold air collects are also described as frost hollows or frost pockets. In the southern Colorado Rocky Mountains the ecosystem at 2900 m is sub-alpine, or montane, as trees are still common at this altitude. The date of first permanent winter snowpack at the RMBL averages about 4 November (range 15 October-24 November, data from 1974-2001), and the length of snowcover is about 200 days (range 165-233, data from 1975-2001). The mean date of first bare ground at a permanent snow measurement station is 21 May, with a range of 25 May to 19 June (data from 1975-2002). Summer precipitation also appears to play a role in some aspects of phenology at the RMBL. Precipitation for June-August at the NOAA weather station in

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Crested Butte (2704 m, 9.5 km from RMBL) has averaged 13.5cm (range 5.3-22.3 cm, data from 1973-2001; the data for 2002 will probably set a new record low). The influence of climate on the growing season, and hence on phenology, can also be seen by transplant experiments. Plants transplanted to lower altitudes will typically develop much sooner than those left in their native high-altitude sites (e.g., Wagner and Reichegger 1997).

3.

LITERATURE REVIEW

Perhaps more than any other bioclimatic zone except high latitudes, phenological events at high altitudes are constrained by a short growing season, delimited by cold temperatures and snowpack. Time of snowmelt appears to have an almost universal effect on high-altitude phenology, and variation in phenology can usually be linked to variation in accumulation and then melting of snow, whether this is across time or space. This interaction has been reported by many studies, including Bliss (1956), Holway and Ward (1963, 1965), and Mark (1970). Canaday and Fonda (1974) found that the timing and duration of phenophases of a variety of subalpine plants in the Olympic Mountains (WA) were a function of snowmelt. In general terms Ratcliffe and Turkington (1989) found the same results, although they argue that the identity of dominant species and, to a lesser degree, aspect, are responsible for variations they observed in phenology. Some species tended to flower earlier on south-facing slopes, indicating the potential importance of aspect and microenvironment. Most studies of phenology at high altitudes have been short (e.g., (Wielgolaski and Kärenlampi 1975); such studies can probably define relatively well the spatial pattern of snowmelt and hence phenology in a particular site, but longer studies are required to gain insights into the effects of climate variables on phenology. In one relatively long study, Walker et al. (1995) followed the phenology of two forbs for six years in five different plant communities and found significant differences among years and plant communities. Phenophase condensation has been observed in several studies of alpine plants, with full development being accomplished more rapidly where snow persists longer. Examples of this have been reported by Knight et al. (1977, and references therein), and Billings and Bliss (1959). Snowmelt gradients are a common phenomenon at high altitude, as some areas will receive more or less snow and receive more or less insolation and result in earlier or later snowmelt. The consequences of these gradients have been investigated in several studies. Kudo (1992) investigated five herbaceous species along a

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snowmelt gradient on Mt. Kaun in the Taisetsu Mountains of Hokkaido, where the snowfree period ranged from 55 to 95 days. The later snowmelt occurred, the later flowering and fruiting began, and in the plot that melted out last no species was able to mature all fruits because of the short growing season. In a study of 56 species over three years, Kudo also found that a shorter snow-free period reduced flowering and seeding (Kudo 1991). Plants found in alpine tundra are often remarkable for the speed with which they can flower and fruit, but this adaptation is required for success given the short growing season (Bliss 1971; Wielgolaski and Kärenlampi, 1975). This early flowering is facilitated by the fact that floral initiation often occurs one or more years in advance of flowering; preformation of flower buds is characteristic of many high-altitude plants (e.g., Resvoll 1917; Forbis and Diggle 2001; Meloche and Diggle 2001, and see references in Bliss 1971). The climate constraints of high altitudes could result in significant selection against late flowering, to allow sufficient time for the development of seeds before the first killing frost in the fall, and this may be why annual and even biennial plants are relatively uncommon at high altitudes (Bliss 1971; Jackson and Bliss 1982). Annuals may be restricted to sites that melt out early or that don’t dry out early in the summer (Reynolds 1984). Some studies do show that most species in alpine communities initiate flowering rapidly after snowmelt, with relatively few species flowering late (e.g., Holway and Ward 1965; Billings and Mooney 1968; Totland 1993). In a few cases, plants may be able to initiate growth under the snow and get a head start on the growing season. Billings and Bliss (1959) found Geum turbinatum, Carex elynoides, and Deschampsia caespitosa growing under 15 cm of snow near the edge of a melting snowbank, and observed that the latter two of these had started growth under 50 cm of snow that did not become snow free for another four days. Young red leaves of Polygonum bistortoides were found under 110 cm of old snow (Mooney et al. 1981). Williams and Cronin (1968) found that Delphinium species could emerge and develop green cotyledons when snow melted to a depth of 30 cm or less, and Spomer (cited in Richardson and Salisbury 1977) found green plants of Ranunculus adoneus under 1m of snow. Arroyo et al. (1981) recorded the earliest-flowering alpine species in the Chilean Andes as actually blooming precociously under 5-6 cm of snow, and Bliss (1971) reported flowering by species of Caltha and Ranunculus under 10 cm or more of snow. Theurillat and Schlüssel (2000) studied seven subalpine-alpine species in the Alps and characterized them by the number of degree-days to bud burst and the end of flowering. Each species differed in its requirements, but only Vaccinium myrtillus was closely tied to snowmelt, while the others fit heat sum models that depended on degree-days after a chilling requirement,

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intensity of chilling from a threshold, or constant degree-days following thaw (Heide 1993; Myking and Heide 1995). It would be interesting to have some studies that have compared models of heat sums and time since snowmelt to see which works best for predicting phenology of a variety of species.

3.1

Temporal, Spatial, and Altitudinal Gradients

Plants growing in microsites with shorter growing seasons may be able to compensate somewhat by shortening the time before flowering starts, allowing them to complete seed production before the weather becomes unfavorable. Jackson and Bliss (1984) studied Polygonum minimum, a very small (

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