Metapopulation Biology: Ecology, Genetics, and Evolution

Contributors

Numbers parentheses indicate the pages on which which the authors' authors' contributions begin. Numbers in parentheses indicate the pages on contributions begin.

N. H. Barton ((183) 1 83 ) Institute of Cell, Animal, and Population Biology, University

of Edinburgh, Edinburgh EH9 3JT, Scotland Patrick 2 1 5 ) Department of Biological Sciences, California State Uni­ Patrick Foley ((215) Uni-

versity, Sacramento, Sacramento, California 958 19 95819 Steven A. Frank Uni­ Frank (325) Department of Ecology and Evolutionary Biology, Uni-

versity of California, Irvine, Irvine, California 927 17 92717 Barbara Barbara E E.. Giles (429) Department of Genetics, Umea Ume~i University, S-90 S-9011 87

Umea, UmeL Sweden Michael E. Gilpin 1 65, 407) Department of Biology, University of California, Gilpin ((165,407)

San Diego, La Jolla, California 92093 Jerome J~rbme Goudet Goudet (429) Institut de Zoologie et d'Ecologie Animale, Universite Universit6 de

Lausanne, CH 0 1 5 Lausanne, Switzerland CH-- 11015 Pierre-Henri Pierre-Henri Gouyon (293) Evolution et Systematique Syst6matique des Vegetaux, V6g6taux,,, Univ­ Univ-

ersite 1405 Orsay Cedex, France ersit6 Paris-Sud, 991405 Mats Gyllenberg (93) Department of Mathematics, University of Turku, FIN-

200 1 4 Turku, Finland 20014

xi

Contributors Contributors

xii xii

I1kka 359) Department Ilkka Hanski Hanski (5, (5, 69, 69, 93, 93,359) Department of of Ecology Ecology and and Systematics, Systematics, Division Division

of 14 Helsinki, of Population Population Biology, Biology, University University of of Helsinki, Helsinki, FIN-000 FIN-00014 Helsinki, Finland Finland Susan Susan Harrison (27) (27) Division Division of of Environmental Environmental Studies and and Center Center for for Popu­ Popu-

lation 16 lation Biology, Biology, University University of of California, California, Davis, Davis, Davis, Davis, California California 956 95616 Michael P. 1 23) Department of P. Hassell Hasseli ((123) of Biology, Imperial College at Silwood

Park, Park, Ascot, Berkshire SL5 7PY, United United Kingdom Alan Alan Hastings (93) Division Division of of Environmental Studies and and Institute of Theoret­ Theoret-

ical Dynamics, University of California, Davis, Davis, California 956 16 95616 Philip W. Hedrick 1 65) Department of Zoology, Arizona State University, Hedriek ((165)

Tempe, Arizona 85287 Robert D. Holt 1 49) Department of Systematics and Ecology, Natural History Holt ((149)

Museum, The University of Kansas, Lawrence, Kansas 66045 Rolf A. Ims Ires (247) Department of Biology, Division of Zoology, University of

Oslo, N-03 N-0316 1 6 Oslo 3, Norway Veronica A. Johnson Johnson (267) Program in Ecology, Evolution and Conservation

89512 Biology, University of Nevada, Reno, Nevada 895 12 Robert 1 23) Department ooff Zoology, Oxford OXI Robert M. May ((123) OX1 3PS, United King­ King-

dom Sean Nee ((123) 1 23) Department of Zoology, Oxford OXI OX1 3PS, United Kingdom

' Evolution, Universit6 Universite Montpel­ Isabelle Olivieri (293) Institut des Sciences de ll'Evolution, Montpellier 2, 34095 Montpellier cedex 05, France Daniel Simberloff Univer­ Simberloff (5) Department of Biological Sciences, Florida State Univer-

sity, Tallahassee, Florida Florida 32306 Andrew T. Smith Andrew Smith (407) (407) Department of Zoology, Arizona State University, Tempe, Arizona 85287 Peter B. Staeey Stacey (267) Program in Ecology, Evolution and Conservation Biology, Peter University of Nevada, Reno, Nevada Nevada 89512 895 12 Mark L. L . Taper Taper (267) Department of Boze­ Mark of Biology, Montana State University, Bozeman, Montana 59717 597 1 7 Andrew D. Taylor Taylor (27) Department o Andrew offZoology, University ooffHawaii, Honolulu, Hawaii 96822 Chris D. D. Thomas Thomas (359) (359) Department of of Biology, University University of of Leeds, Leeds, Leeds Leeds LS2 Chris 9JT, United United Kingdom Kingdom Ed van van der der Meijden Meijden (387) (387) Institute Institute of of Evolutionary Evolutionary and and Ecological Ecological Sciences, Sciences, Ed Leiden University, University, 2300 2300 RA RA Leiden, Leiden, The The Netherlands Netherlands Leiden Catharina A. A. M. M. van van der der Veen-van Veen-van Wijk Wijk (387) (387) Institute Institute of of Evolutionary Evolutionary and and Catharina Ecological Sciences, Sciences, Leiden Leiden University, University, 2300 2300 RA RA Leiden, Leiden, The The Netherlands Netherlands Ecological Michael C. C. Whitloek Whitlock (183) ( 1 83) Department Department of of Zoology, Zoology, University University of of British British CoCo­ Michael lumbia, Vancouver, Vancouver, British British Columbia, Columbia, Canada Canada V6T V6T 1Z4 l Z4 lumbia,

Contributors

xiii xiii

John A. Wiens Wiens (43) (43) Department of of Biology Biology and Graduate Degree Program in John Ecology, Colorado Colorado State State University, University, Fort Collins, Collins, Colorado Colorado 80521 805 2 1 Ecology, G . Yoccoz Yoccoz (247) (247) Laboratoire de d e Biom6trie, Biometrie, G6n6tique Genetique et e t Biologie Biologie des des PopPop­ Nigel G. ulations, URA URA CNRS 2055, 2055, Universit6 Universite Claude Bernard, Bernard, F-69622 F-69622 Villeurbanne Villeurbanne ulations, of Zoology, University Cedex, France; and Department of Biology, Division of of Oslo, N-0316 N-03 1 6 Oslo 3, Norway of

sdfsdf

Preface

the past past few few years, the metapopulation concept has has become become widely and and In the firmly established population biology and in conservation. conservation. The The number number firmly established both in population of papers papers on metapopulations metapopulations is growing growing exponentially, with with a doubling doubling time time of of of less than than two years. The The metapopulation metapopulation concept concept is beginning beginning to appear appear in text­ textbooks, and the metapopulation replaced the dynamic metapopulation theory has has to a large large extent replaced dynamic theory theory of of island biogeography biogeography in conservation conservation biology. As observed observed by Science magazine, metapopulation approaches approaches are are now "all the rage." rage." Our Our previous previous book, Metapopulation Dynamics: Empirical Empirical and Theoretical 99 1 ), brought together a Investigations (Gilpin and Hanski, Hanski, Academic Academic Press, 11991), range of of viewpoints and ecological models bearing bearing on spatially fragmented fragmented pop­ populations. The unmet demand. The book book sold out rapidly, leaving leaving an unmet demand. In considering considering the the need updated need for for aa new new book book on on the the same same subject, subject, we we had had aa choice choice between between an an updated second edition and an entirely new new volume. We We chose the second second alternative for two reasons. First, the fi eld of metapopulation biology has advanced field advanced considerably, with a vigorous interplay among theory, models, and fi eld studies, and we wanted field to ect the to refl reflect the depth depth and and the the breadth breadth of of this this growth growth in in the the new new volume. volume. Second, Second, we wanted wanted to shift some emphases emphases and expand expand along new lines of of inquiry. The The first volume was biased toward toward a conceptual conceptual analysis of metapopulation ecology. In this volume, we cover more more thoroughly both empirical empirical studies and more ad­ adgevanced theories, and we have now included more information pertaining to ge­ netics and evolution. The rapid progress that has occurred in field field studies is ev-

Xu xv

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Preface Preface

ident on the covers of the two volumes. Whereas the cover of the previous book butterfly madepicted a metapopulation of a hypothetical butterfl y species, Euphydryas ma­ cintoshus G., the cover of this volume illustrates the fragmented landscape of a butterfly Melitaea cinxia). real butterfl y metapopulation (the Glanville fritillary, Melitaea This volume consists of solicited chapters from selected authors working in This the general area of metapopulation biology. We are pleased that everyone whom we asked to contribute did contribute. Several chapters chapters in this volume are pri­ prichapters practically marily empirical, while others are highly theoretical. Some chapters chapignore ecology; many more ignore genetics and evolution. However, a few chap­ ters describe both theory and empirical results, and others cover both ecology and genetics, a trend that we hope will become more prominent in the near future. readers will equally appreciate every chapter, chapter, but we would be very dis­ disNot all readers appointed (and truly surprised) if most readers would not be better informed and indeed stimulated by most of the chapters. The scope of the chapters in this represents our attempt to sketch the general limits of metapopulation volume represents biology. We We hope that this volume will disseminate disseminate ideas, results, and and conclusions conclusions across the customary academic academic confi confines. across nes. One recent nite broadening broadening of recent trend trend that that we have noted is a defi definite of the meaning meaning of the term term "metapopulation." In the first volume, population turnover, local ex­ exof tinctions and and colonizations, was considered to be the key and and practically indis­ indistinctions pensable feature of of metapopulation dynamics. In this interpretation we followed pensable conceptual guidance guidance of of the root of of all metapopulation metapopulation models, the Levins Levins the conceptual continue to think think that metapopulation dynamics dynamics in this nar­ narmodel. Although we continue conceptual core of of this area of of population biology, it is row sense forms the hard conceptual accept that that a broader broader perspective perspective is needed. needed. This volume promotes promotes now time to accept such of the such a view. Inevitably, an expansion expansion of the metapopulation concept concept will attract attract applications to an even wider of situations can foresee, and some wider range range of situations than than we can foresee, and some of these applications will not turn of these applications tum out to be productive. productive. During During a period period of of rapid rapid growth, excesses excesses may occur and crossed. This is the time-honored and limits limits may be crossed. time-honored process of any worthprocess by which which the the scientific scientific community tests the the applicability of worth­ while idea or model. idea or We thank Chuck Crumly of Academic Press for for encouraging this We thank Chuck Crumly of Academic Press encouraging us to edit this second and for for all his assistance assistance during during the the process. following col­ colsecond volume volume and process. The The following leagues greatly helped chapters: Milo Adkinson, Richleagues greatly helped us in reviewing individual individual chapters: Milo Adkinson, Rich­ ard Barnes, Barton, Jan Jan Bengtsson, Berkson, Ian Ian B illick, Ted Ted Case, ard Barnes, Nick Nick Barton, Bengtsson, Jim Berkson, Billick, Case, Diane Gordon Fox, Andy Hansen, Diane Debinski, Debinski, Torbj6rn Torbjorn Ebenhard, Ebenhard, Gordon Fox, Andy Hansen, Alan Alan Hastings, Hastings, Phil Tad Kawecki, Phil Hedrick, Hedrick, Anthony Anthony Ives, Tad Kawecki, Joshua Joshua Kohn, Kohn, Russ Russ Lande, Lande, Simon Simon Levin, Trevor Price, Levin, Sean Sean Nee, Nee, Isabelle Isabelle Olivieri, Olivieri, Trevor Price, Jonathan Jonathan Silvertown, Dan Dan SimSim­ berloff, berloff, Monte Monte Slatkin, Slatkin, Peter Peter Stacey, Stacey, Mark Mark Taper, Taper, Chris Chris Thomas, Thomas, Rick Rick Walker, Walker, Christian Wissel, Wissel, and and Greg Greg Witteman. Witteman. We We also also thank Pia Vikman Vikman for her secresecre­ Christian thank Pia for her tarial contribution to Deborah Moses tarial contribution to the the project. project. Chuck Chuck Crumly Crumly and and Deborah Moses of of Academic Academic Press Press have have been been a pleasure pleasure to work work with.

Ilkka Hanski Hanski Ilkka Michael E. Gilpin Gilpin Michael

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CONCEPTUAL CONCEPTUALFOUNDATIONS FOUNDATIONS

The three chapters in this section explore the scope of of the applications. Hanski and SimSim­ metapopulation concept and its applications. berloff the history of studies and and the berloff sketch the of metapopulation metapopulation studies of approaches, both both theoretical and empirical, empirical, that have range of been used in single-species single-species studies. Harrison and Taylor assess assess critically the pertinence the metapopulation critically pertinence of of the metapopulation approach approach to field studies situations. studies and and expand expand their review review to multispecies multispecies situations. Wiens more more directly connects connects the metapopulation metapopulation concept concept to the complexities of of real landscapes. landscapes. Hanski and Simberloff Simberloff outout­ line in some detail the use (and misuse) misuse) of of the metapopulation metapopulation concept conservation, where an apparent paradigm shift concept in conservation, apparent paradigm shift has occurred from the dynamic theory of island biogeography to occurred from the dynamic theory of island biogeography to the metapopulation metapopulation theories. theories. The gradual gradual unfolding unfolding and and evolution evolution of of the the metapopulation metapopulation The concept from from the the pioneering pioneering studies studies of of Sewall Sewall Wright, Wright, AndreAndre­ concept wartha and Birch, Huffaker, Huffaker, Den Den Boer, Ehrlich, Gadgil, and and wartha have been been narrated narrated previously previously and and are are summarized summarized here here Levins have Hanski and and Simberloff Simberloff and and by by Harrison Harrison and and Taylor. Harrison Harrison by Hanski and and Taylor Taylor make make the the interesting interesting point point that that the the origin origin of of the the metapopulation metapopulation idea idea is different different in single-species single-species and and in mulmul-

tispecies tispecies studies. studies. Single-species Single-species studies have tended tended to empha­ emphats of size the benefi benefits of migration in leading to the establishment establishment of of new populations populations and thereby compensating compensating for for extinctions extinctions in small habitat species metapopulation habitat patches. patches. In the multi multispecies metapopulation sce­ scenarios, narios, the key issue has been been the locally locally unstable unstable interaction interaction among competitors competitors and between between a prey and its predator. predator. Habitat fragmentation beneficial in creating the possibility fragmentation can be beneficial possibility for asynchronuous uctuations, which asynchronuous fl fluctuations, which can enhance enhance regional sta­ stability. A high rate of of migration may eliminate eliminate such asynchrony, asynchrony, and is hence potentially harmful for for regional persistence persistence in mul­ multispecies tispecies metapopulations. metapopulations. Multispecies Multispecies metapopulation metapopulation theory is further further discussed discussed by Nee, May, and Hassell and by Holt in Part Part II. etapopulation Dynam­ In the predecessor predecessor of of this volume, M Metapopulation Dynamics: Empirical and Theoretical Investigations (Gilpin and Han­ Han99 1 ), metapopulation ski, 11991), metapopulation dynamics dynamics was seen to imply signif­ significant turnover turnover of of local populations, populations, local extinctions, extinctions, and ' s orig­ colonizations. colonizations. This notion notion follows follows directly from Levins Levins's original concept concept of of a metapopulation metapopulation as a population population of of populations, populations, analogous analogous to a population population of of individuals individuals with finite lifetimes. lifetimes. This narrow classical view of of metapopulations metapopulations has now now become become superceded superceded by a broader broader view, where where any assemblage assemblage of of dis­ discrete local local populations populations with with migration migration among among them them is consid­ considered ered to be a metapopulation, metapopulation, regardless regardless of of the rate of of population population turnover. turnover. (In a nonequilibrium nonequilibrium metapopulation metapopulation declining declining toward extinction extinction even among-population among-population migration is not a necessary criterion, but a system with no turnover mi­ turnover and no no migration would not classify as a metapopulation.) im­ metapopulation.) There are important portant questions questions to be asked about the role of of migration migration in (local) population dynamics, and these questions questions are most most nat­ naturally asked in a metapopulation (regional) (regional) context. Meta­ Metapopulation dynamics in the narrow narrow sense, with significant significant pop­ population turnover, turnover, is of of course course included included in metapopulation metapopulation dynamics in the broad broad sense. The realization that natural natural populations populations exemplify many many kinds of of spatial population population structures structures has stimulated stimulated a termi­ terminology, originally due to Susan Susan Harrison, Harrison, and including including entries such as patchy populations populations (not really metapopulations), metapopulations), clas­ classical (Levins) metapopulations, island metapopula­ metapopulations, mainlandmainland-island metapopulations, source - sink metapopulations, source-sink metapopulations, and nonequilibrium nonequilibrium metapopulations. metapopulations. These These concepts concepts and types of of metapopulation metapopulation structures structures are discussed discussed by Hanski and Simberloff Simberloff and and by Har­ Harrison and Taylor. The danger danger here is that too much much emphasis is cation, defi nition of given to classifi classification, definition of ideal types, which which in itself itself

does not guarantee any better understanding understanding of of the ecology, genetics, and evolution evolution of of metapopulations. What What matters is what what works. Does the "metapopulation approach" approach" help answer answer important questions questions about about spatially structured populations? populations? Does Does it provide provide us with scientific insight to the problems problems in which we are are interested? All this being said, there still is a need need to be concerned concerned with the type of of spatial spatial structure of of populations populations in any empirical study and in an application of of the metapopu­ metapopulation concept and models to real populations. populations. One should avoid the temptation of of pigeonholing every population with some form of of patchiness as a "metapopulation," as Harrison Harrison and Tay­ Taylor warn. In the worst case, this may obscure what what is important and draw attention to elements that are less critical. Unfortu­ Unfortunately, there are no easy answers answers here; one simply has to know the species and one has to understand the interactions interactions between the populations and their environment. Metapopulation biology may be a multifaceted subject, but there is one common element that characterizes characterizes this approach approach to population biology. The The metapopulation approach approach is based on the notion notion that space is not only discrete but that there is a binary distinction between suitable and unsuitable unsuitable habitat types. If this does not fi fitt one's one's idea of of a particular environment, one is probably better off off in using some approach approach other other than than the metapopulation metapopulation approach. An An important reason reason for the appeal of con­ of the metapopulation metapopulation concept concept comes from our our subjective conviction that natural lansdscapes truly are, for for many species, patchworks patchworks of of one or several several habitat types. Though Though the metapopulation view of of nature nature is complex enough, enough, it appears to be hopelessly hopelessly simplified in comparison of of how landscape ecologists view reality. Wiens in his chapter chapter lists four four components components that characterize landscape landscape ecology: variation in patch quality, variation in the quality of of the surrounding surrounding en­ environment, boundary boundary effects, and how how the landscape affects patch patch connectivity. Wiens Wiens is correct in suggesting that that most of of these elements are by and and large missing missing from from metapopulation models, which which are typically focused focused on idealized habitat patches in a featureless featureless landscape. Recent studies of of Andren Andr6n and Green (cited by Wiens) appear appear to suggest that where the suitable habitat fragments for for some species species cover only a rela­ relatively small fraction fraction of of total area (let us call these LC land­ landscapes, for for low coverage), patch area and isolation effects tend to be signifi cant; but where significant; where much of of the area is covered by more or less suitable habitat (HC landscapes, landscapes, for for high coverage), coverage), other a comother factor", factors, such as exactly how how individuals move in acom-

plex landscape, landscape, begin to dominate. Now, it so happens that the classical metapopulation concept implicitly assumes a LC land­ landscape, hence the tradition of of representing representing habitat patches as dots on maps, rather rather than drawing them as realistic habitat frag­ fragments. There appears to be a real difference difference between between the two traditions here, as they have been largely concerned concerned with either LC landscapes landscapes (metapopulation ecology) or HC landscapes (landscape ecology). As Wiens stresses, it is imperative for for the practical application land­ application of of both metapopulation biology and landscape ecology in conservation and planning that more common ground is established by developing appropriate appropriate theory and de­ designing appropriate field studies. Some necessary constituents of a more more unified approach seem relatively easy to achieve. For instance, it should not be too diffi cult to correct among-patch distances by taking into difficult account how the features of landscape affect of the intervening landscape ovement behavior. On the individual individual m movement the other hand, hand, when con­ considering HC landscapes, landscapes, patch inade­ patch models models are likely to be inadequate anyway. Metapopulation theory may well remain a useful practical tool for LC landscapes, landscapes, with with relatively small and iso­ isolated lated fragments of of suitable suitable habitat, habitat, but the "reserve "reserve mentality" that that this approach approach implies should give away, as Wiens Wiens argues, to "mosaic management" management" of of the the environment in HC landscapes. landscapes. Today, we do not yet have a conceptual and practical practical synthesis of of metapopulation biology and landscape landscape ecology, but no doubt the time will come when we will.

The Metapopulation Approach, Approach, Its History, History, Conceptual Conceptual Domain, and Application Application to Conservation Conservation Ilkka llanski Hanski

Daniel Simberloff

I. INTRODUGION INTRODUCTION At no period in the history of of ecology has the spatial structure of of populations populations and communities been entirely ignored, but the role that space plays in forming ecological patterns patterns and in molding processes has been viewed very differently in different times ((Mclntosh, McIntosh, 11991). 99 1 ). In the 11960s 960s and 1 970s, theoretical ecology and 1970s, was largely focused on issues other May, 11976a), 976a), with other than than spatial spatial dynamics dynamics ((May, notable MacArthur and Wilson, 11967), 967), and notable exceptions exceptions ((MacArthur and field ecologists tended tended to and space is introduced introduced in various follow suit. Today, space is in the forefront and ways into all fields of ecology and population biology more generally. Whether Whether one is interested in processes occurring at the level of genes, individuals, popu­ populations, or communities, spatial structure is widely seen as a vital ingredient ingredient of of better and more powerful theories, and good empirical work involving space is seen as a great challenge ((Kareiva, Kareiva, 11990). 990). Five years ago, before the publication of the predecessor of this volume (Metapopulation (Metapopulation Dynamics: Dynamics: Empirical and Theoretical TheoreticalInvestigations, Investigations, Gilpin and Hanski, 11991), 99 1 ), the metapopulation concept concept was new to most biologists. Since then, literature on metapopulations has grown exponentially, with a doubling time of less than Fig. 11). ). The metapopulation concept than 2 years ((Fig. concept has by now been firmly established established in population population biology and beyond; we review and analyze in this

Metapopulation Metapopulation Biology Biology

Copyright Academic Press, Inc. Inc. All onn reserved. Copyright © 9 1997 1997 by Academic All rights rights of of reproduction reproduction in in any any fform reserved.

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chapter the spread spread of of the metapopulation metapopulation concept concept to conservation conservation biology and and chapter applications. applications. What is the metapopulation metapopulation approach? approach? A more more complete complete explication is given What nutshell the two key premises premises in this approach approach to popUlation population below, but in a nutshell biology are that populations populations are spatially structured structured into assemblages assemblages of of local biology breeding breeding populations populations and that that migration among among the local populations populations has some some effect on local dynamics, including including the possibility of population population reestablishment reestablishment effect contrast with those of of standard models of following extinction. These premises contrast demography, population population growth, genetics, and community interaction interaction that assume demography, a panmictic popUlation population structure, with all individuals equally likely to interact

1 The The Metapopuiation MetapopulationApproach Approach

7 7

with any others. Population Population biology has has made productive use of of such models models for for at least 1100 00 years, but need to account for position of of but today today there is a distinct need for the position individuals populations in space. This need individuals and and populations need has arisen from from the intrinsic intrinsic development development of of population population biology as a science, science, but the trend trend has has clearly been been strengthened strengthened by the demand demand for for professional professional advice on environmental environmental issues typ­ typically involving space. space. In the past few few years, metapopulation metapopulation studies studies have have shed shed new new light on such phenomena phenomena as patterns patterns of of distribution distribution and and population population turnover turnover dynamics dynamics in frag­ fragmented Hanski, this volume; mented landscapes ((Hanski, volume; Harrison Harrison and Taylor, this volume; volume; Thomas volume; van der Thomas and and Hanski, Hanski, this volume; volume; Smith Smith and and Gilpin, Gilpin, this volume; der Meijden Meijden and vol­ and van der der Veen-van Veen-van Wijk, Wijk, this volume), landscape landscape ecology (Wiens, (Wiens, this volume) Holt, this volume), population population viability and ume) and and community community structure structure ((Holt, and time to extinction volume), coexistence extinction (Gyllenberg (Gyllenberg et et ai., al., this volume; Foley, this this volume), coexistence of of competing Nee et volume), competing species, species, and and of of prey and and their their natural natural enemies enemies ((Nee et ai., al., this volume), evolution evolution of of migration migration rate and and other other life-history life-history traits (Olivieri and and Gouyon, Gouyon, this volume), Ims and volume), ecological ecological consequences consequences of of migration migration ((Ims and Yoccoz, Yoccoz, this this volume; Stacey Stacey and and Taper, this volume), volume), unexpectedly unexpectedly high high levels of of inbreeding inbreeding and and low heterozygosity in natural Hedrick and volume), patterns patterns natural populations populations ((Hedrick and Gilpin, Gilpin, this this volume), of (Barton and of genetic differentiation differentiation (Giles and Goudet, this volume), volume), adaptation adaptation (Barton and Whitlock, Frank, this volume). As Whitlock, this volume), volume), and coevolutionary coevolutionary processes processes ((Frank, is apparent apparent from from the citations, citations, these these developments developments are are well represented represented in the the chapters literature at chapters in this volume, volume, which which provide provide an excellent entree entree to the the literature large. There are many advantages metapopulation approach, advantages of of a metapopulation approach, but success success may also breed breed problems. problems. As As in any scientifi scientificc field experiencing experiencing rapid rapid growth, growth, there there is the danger danger of of blurring blurring of of concepts. There There is the temptation temptation to view any system with any kind of of patchiness patchiness at any spatial spatial or or even temporal temporal scale as a "metapop­ "metapopulation." 1 99 1 , 11994b; 994b; Harrison ulation." Harrison Harrison ((1991, Harrison and Taylor, this volume) volume) cautions us about this tendency. Anticipating the kind kind of of verbal entropy that has has enveloped enveloped many terms 1 99 1 volvol­ terms in population population biology, Hanski Hanski and and Gilpin Gilpin sketched sketched in the 1991 ume of scale, hihi­ ume the meaning meaning of of the term term "metapopulation," "metapopulation," highlighting highlighting issues of erarchy, and and a requirement requirement for some population population turnover. turnover. We We feel a need need to dwell on the same same issues in this chapter, chapter, and and we provide provide a revised revised succinct succinct glossary glossary of of the commonly commonly used used terms in the literature. literature. First, however, however, let us examine examine briefl brieflyy the history of of the metapopulation metapopulation concept. concept.

II. BRIEF OF METAPOPULATION BRIEFHISTORY HISTORYOF METAPOPULATIONSTUDIES STUDIES The metapopulation metapopulation concept concept has has a pedigree dating dating back back to the early part of of this century, but but until recently this tradition tradition played only a minor minor and and episodic episodic role in the intellectual population biology. For For a long time, the pre­ intellectual advance advance of of population prevailing view was one one emphasizing emphasizing persistence persistence and and stability of of local populations, populations, or as McIntosh 1 99 1 ) put it, "the Mclntosh ((1991) "the great great tradition tradition of of balance balance of of nature, nature, going going back back

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IIkko Honski and Daniel Simberloff Ilkko Honski and Daniel Simberloff

to antiquity, imputed imputed to nature nature homogeneity, homogeneity, constancy, or equilibrium equilibrium and ab­ abhored hored thoughts thoughts of of extinction and randomness." randomness." In evolutionary 1 93 1 , 11940) 940) had the insight that evolutionary biology, Sewall Sewall Wright ((1931, evolution evolution might proceed proceed rapidly in spatially structured structured popUlations, populations, especially if there are are local local extinctions extinctions and and recolonizations. recolonizations. Wright's Wright's shifting balance balance theory has remained an intriguing, understood, and little tested model intriguing, imperfectly understood, model ever since since (Barton (Barton and and Whitlock, Whitlock, this volume). Wright's Wright's work work may may have stimulated stimulated popUlations in the fi rst half interest in spatially structured structured populations first half of of this century, repre­ represented for instance by studies of Boycott ( 1 930), Diver ( 1 938), and Lamotte studies of Boycott (1930), Diver (1938), ((1951) 1 95 1 ) on ecology and genetics of of snail populations populations (for a more thorough thorough dis­ discussion, 996a). Pioneering cussion, see Hanski, Hanski, 11996a). Pioneering quantitative quantitative studies studies in epidemiology epidemiology ((Ross, Ross, 11909, 909, Kermack and 927; see Anderson 1 99 1 ; and McKendrick, McKendrick, 11927; Anderson and and May, 1991; theo­ Nee et et al., al., this volume) volume) are now seen as closely linked linked conceptually and theometapopulation studies, retically to metapopulation studies, but that connection connection remained remained without com­ comment May, 11991; 99 1 ; Lawton Lawton et 994; Nee, 1994). 1 994). ment until recently recently ((May, et al., al., 11994; The The ecological ecological implications implications of of the metapopulation metapopulation concept concept were were not consid­ considered 954, when ered before before 11954, when Andrewartha Andrewartha and and Birch Birch published published their their distinguished distinguished text text on animal animal ecology. Drawing Drawing on their wide experience experience from insect population population ecology, Andrewartha factors" Andrewartha and Birch found found the "dogma "dogma of of density-dependent density-dependent factors" unacceptable. They emphasized popUlations, documented unacceptable. emphasized wild oscillations oscillations of of populations, documented fre­ frequent quent local extinctions, extinctions, but also recognized recognized the possibility possibility of of reestablishment reestablishment of populations 1 954) advo­ populations at vacated vacated localities. localities. In brief, Andrewartha Andrewartha and Birch ((1954) advocated the view that phenomenon: that local population population extinction extinction was a common common phenomenon: "spots that that are occupied today may become become vacant vacant tomorrow tomorrow and and reoccupied reoccupied next week 954, p.87). week or next year" year" (Andrewartha (Andrewartha and and Birch, 11954, p.87). However, However, why did their their ideas fail to gain wider acceptance? acceptance? We We believe the reason reason is their nearly nearly cate­ categorical rejection rejection of of the concept concept of of density-dependent density-dependent population population regulation. regulation. The The Andrewartha Andrewartha and Birch notion about population population dynamics in space was largely ignored ignored and eventually forgotton. forgotton. The incipient metapopulation metapopulation concept concept nonethe­ nonethe950s and 960s, in works works of Huffaker ((1958), 1 95 8), less had a quiet existence existence in the 11950s and 11960s, of Huffaker den 1 968), Ehrlich and Raven 1 969), Gadgil ((1971), 1 97 1 ), and undoubtedly den Boer Boer ((1968), Raven ((1969), undoubtedly a few others. The 1 963, 11967) 967) dynamic theory of The MacArthur MacArthur and Wilson ((1963, of island biogeography metapopulation concept, even if biogeography has much much in common common with the metapopulation MacArthur multi species communities, MacArthur and Wilson were primarily concerned with multispecies communities, as we discuss discuss below. below. The The term term "metapopulation" "metapopulation" was introduced introduced in the works works of of Richard Richard Levins Levins in 11969 969 ((1969a) 1 969a) and 970. The and 11970. The word word itself itself suggests suggests a population population of of populations, populations, with colonization metapopulation likened colonization and and extinction extinction of of local populations populations in a metapopulation likened to births hence the to births and deaths deaths of of individuals individuals in a local population population ((hence the emphasis emphasis on population population turnover turnover in "classical" "classical" metapopulation metapopulation studies). Levins' Levins'ss work work marks the beginning though, beginning of of contemporary contemporary metapopulation metapopulation biology. It is puzzling, puzzling, though, that the early lead that that Levins provided provided was followed followed by a period period of of nearly 20 years of Fig. 11). ). We return to the possible below, of recess ((Fig. possible reasons reasons for for this delay below, in the the section section on metapopulations metapopulations and and conservation conservation biology.

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CONCEPTUAL DOMAIN DOMAIN AND AND METAPOPULATION METAPOPULATION APPROACHES APPROACHES III. CONCEPTUAL A fundamental fundamental assumption assumption of of the the original original metapopulation metapopulation concept concept (Levins, ( Levins, A 1 969a) is that that space space is discrete discrete and and that that it it is is possible possible and and useful useful to to distinguish distinguish 1969a) between habitat patches that suitable for for the the focal focal species species and and the the rest rest of of the the between habitat patches that are are suitable environment, often called called the the matrix. matrix. In this this respect respect the the metapopulation approach environment, often metapopulation approach akin to to the the dynamic theory of of island island biogeography (MacArthur ( MacArthur and and is closely akin Wilson, 1967) 1 967) but but differs differs from from landscape landscape ecology (Wiens, ( Wiens, this volume). The The Wilson, metapopulation concept concept also presumes that that the the habitat habitat patches patches are are large large enough enough metapopulation to accommodate accommodate panmictic panmictic local populations, popUlations, but but not not larger. larger. Other Other fields fields of of ecolecol­ with spatial spatial patchiness, patchiness, but but either either at a smaller smaller (foraging (foraging thethe­ ogy are are concerned concerned with Krebs and and Davies, Davies, 1984) 1 984) or or at a larger larger scale (e.g., (e.g., much much of of landscape landscape ories; Krebs Forman and and Godron, Godron, 1986; 1 986; GAP GAP analyses: Scott Scott et et al., ai., 1991; 1 99 1 ; ecology: Forman geographical ecology: Ricklefs Ricklefs and and Schluter, Schluter, 1993) 1 993) than than the the scale scale of of (panmictic) ( panmictic) geographical local populations. The The concept concept of of an ideal ideal metapopulation metapopulation a la Levins includes local three habitat patches patches have equal areas isola­ three other simplifying assumptions: habitat areas and isolametapopulation have entirely independent independent (uncor(uncor­ tion, local populations in the metapopulation related) dynamics, and the exchange exchange rate of individuals among populations related) rate of among local populations migration has no real effect effect on local dynamics in the the existing existing is so low that migration populations: local dynamics occur occur on a fast fast time scale scale in comparison comparison with metameta­ population dynamics. dynamics. No real metapopulation metapopulation completely satisfies all these these requirements. requirements. However, However, No assumptions, such as equal patch isolation, can can be the more more specific specific assumptions, patch areas areas and and isolation, relaxed without need for a major major conceptual conceptual amendment. amendment. This is not unlike how relaxed without need unlike how com­ the popUlation population concept concept is used in population population biology: no real population population completely satisfies all the criteria panmictic, population. What criteria of an ideal, closed and panmictic, really matters is the notion of of discrete local breeding populations connected by migration. We We suggest that if this assumption cannot be defended, defended, some other approach should be used instead of the metapopulation approach; and conversely, the more more distinct distinct and and smaller the local breeding breeding populations populations are, the more more useful the metapopulation approach 1 99 1 ) used poppop­ approach is likely to be. Hanski and Gilpin ((1991) ulation turnover, local extinctions and colonizations, as the hallmark hallmark of of true meta­ metapopulations. By this definition, the mainland-island mainland-island systems studied in the dy­ dynamic theory of island biogeography and in recent metapopulation models 99 1 ; Hanski and 993) would not count as metapopula­ (Gotelli, 11991; and Gyllenberg, 11993) metapopulations. Following the current usage of the term, we now include mainlandisland mainland-island structures among other metapopulation structures. It has been suggested that "much" migration among local populations popUlations makes the metapopulation approach less useful ((Harrison, Harrison, 11994b). 994b). While it is true that the classical concept (Levins, 11969a) 969a) implicitly assumes a low migration rate, so low that migration plays no role in the dynamics of existing local populations, more recent theoretical Hassell et 99 1 a, 11994, 994, Gyllenberg and Hanski, 11992; 992; theoretical ((Hassell et ai. al.,, 11991 Nee Hanski et 995a,b) has made Nee et et ai. al.,, this volume) and empirical work ((Hanski et ai., al., 11995a,b) good use of the metapopulation concept even when some tens of percents of

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individuals per per generation generation leave leave their their natal natal patch. patch. An An important important issue here here is is the the individuals spatial scale scale of of migration. migration. Theoretical Theoretical studies studies suggest suggest that that aa low low rate rate of of longlong­ spatial distance migration migration has has often often about about the the same same consequences consequences as as aa high high rate rate of of shortshort­ distance distance migration migration (Nachman, (Nachman, 1991). 1 99 1 ). Clearly, Clearly, if if migration migration rate rate is is very very high, high, say say distance > 50%, 50%, and and if if migration migration distances distances are are not not limited, limited, a metapopulation metapopulation approach approach is is > unlikely to be helpful. The fundamental criterion, however, is whether or not the unlikely to be helpful. The fundamental criterion, however, whether or not the metapopulation approach approach is useful useful in in elucidating elucidating the the questions questions in in which which we we haphap­ metapopulation pen to to be be interested, interested, not not whether whether migration migration rate rate is high high or or low. From From the the perper­ pen spective of of traditional traditional population population biology, the the question question is whether whether the the implicit implicit spective assumption that that migration migration makes makes no no difference difference to to the the dynamics dynamics of of the the focal focal poppop­ assumption ulation useful approximation approximation or or not. not. ulation is a useful Our remarks have Our remarks have been been directed directed at at the the population population ecological ecological properties properties of of metapopulations. Genetic Genetic and and evolutionary consequences consequences of of these these metapopulation metapopulation metapopulations. structures enlarge enlarge the the biological domain domain of of the the metapopulation metapopulation concept concept as dede­ structures scribed and Whitlock Whitlock (this scribed by Olivieri and Gouyon (this volume) and Barton Barton and volume). volume). metapopulation book, 199 1 ) defined defined a set In the the previous metapopulation book, Hanski Hanski and and Gilpin Gilpin ((1991) set of key metapopulation metapopulation terms terms in the terminol­ of the hope hope of of promoting a more uniform terminolWe repeat exercise here, here, with a of terms terms (Table (Table ogy. We repeat this exercise a revised and expanded expanded list of but a few comments are warranted. The The I). This list is largely self-explanatory, self-explanatory, but few comments are warranted. source-sink concept literature. Pulliam (1988) ( 1 988) source-sink concept continues continues to cause cause confusion in the literature. efined sources sources and sinks on whether emigration emigration exceeds exceeds immigraimmigra­ d defined on the basis of of whether or vice versa, at equilibrium. equilibrium. This definition definition is useful for population genetic genetic tion, or for population emphasizing asymmetry in gene flow, which which may have important purposes, in emphasizing consequences for consequences for genetic structure structure and adaptation adaptation (Barton (Barton and Whitlock, this volume; Giles and Goudet, this volume). The definition definition given in Table Table I, which is based on the expected expected population growth growth rate at low density, in the absence absence of of intraspecifi intraspecificc density dependence, dependence, may often be preferable preferable for ecological purposes. In the latter latter case, sinks are populations that that would go extinct in the absence absence of of immigration (by Pulliam's Pulliam's definition, a sink population may decline to a low but positive equilibrium Suth­ equilibrium value in the absence of immigration; Watkinson and Suth995). A third and potentially misleading sense in which the sourcesink erland, 11995). source-sink concept is often used is for a mixture of of small and large large habitat habitat patches. Popu­ Populations in small patches patches typically have a high risk of of extinction, extinction, but they are not necessarily "sinks" in the sense of 1 988) or Table I; small populations of Pulliam ((1988) have a high risk of stochastic extinction, even if the expected growth rate at low density and the expected equilibrium population size are positive ((Foley, Foley, this volume). volume).

A. Modeling Modeling Approaches Approaches The traditional approach to population biology assumes spatially unstruc­ unstructured populations. Modeling approaches to spatially structured populations can be divided conveniently into two classes, based on whether the model deals with

1 The The Metapopulation Metapopulation Approach Approach TABLE I

1II1

Metopopulotion Metapopulation Terminology Terminologya a

Term Term

Synonyms and and definition Synonyms

Patch Patch

Synonyms: Habitat Habitat patch, (habitat) (habitat) island, (population) (population) site, locality Definition: A continuous continuous area area of of space with all necessary resources resources for unsuit­ for the persistence of of a local population and and separated by unsuitable habitat from from other other patches (at any given time, a patch patch may be occupied occupied or empty) empty) Synonyms: Population, Population, subpopulation, subpopulation, deme deme Definition: Set of of individuals individuals that that live in the same habitat habitat patch patch and therefore interact with each other; most most naturally applied to "pop­ "populations" living in such small patches that all individuals individuals practi­ practically share a common common environment environment Synonyms: Composite Composite population, population, assemblage (of (of populations) populations) [pop­ [population (when "local populations" are called "subpopulations")] "subpopulations")] Definition: Set of of local populations populations within some some larger larger area, area, where where typically migration migration from from one local population population to at least some some other patches is possible (but see nonequilibrium nonequilibrium metapopulation) metapopulation) Synonyms: Metapopulation Metapopulation type Definition: Network Network of of habitat habitat patches patches which is occupied by a meta­ metapopulation population and which which has a certain distribution distribution of of patch patch areas areas and interpatch migration migration rates Synonyms: Classical metapopulation metapopulation Definition: Metapopulation Metapopulation structure structure assumed assumed in the Levins model: a large network network of of similar small patches, with local dynamics oc­ occurring curring at a much faster time scale than than metapopulation metapopulation dynamics; dynamics; in a broader sense used for systems systems in which all local populations, populations, even even if they may differ in size, have a significant risk of of extinction Synonyms: Boorman-Levitt Boorman- Levitt metapopulation metapopulation Definition: System of of habitat habitat patches (islands) located within dis­ dispersal distance distance from a very large habitat habitat patch (mainland) where where the local population never goes extinct extinct (hence (hence mainland-island mainland-island metapopulations metapopulations do not go extinct) extinct) Definition: Metapopulation Metapopulation in which there there are are patches patches in which the population population growth rate rate at low density and in the absence absence of of im­ immigration migration is negative (sinks) and patches patches in which the growth growth rate at low density is positive (sources) (sources) Definition: Metapopulation Metapopulation in which which (long-term) extinction rate rate ex­ exceeds ceeds colonization colonization rate or or vice versa; versa; an extreme extreme case is where local populations populations are located so far far from from each other other that there is no migration migration between between them and hence no no possibility for for recoloni­ recolonization Synonyms: Colonization-extinction Colonization-extinction events events (or dynamics) Definition: Extinction Extinction of of local populations populations and establishment establishment of of new local populations ex­ populations in empty habitat patches patches by migrants migrants from from existing local populations populations Synonyms: Expected Expected life-time of of a metapopulation metapopulation Definition: The Definition: The length of of time until all local populations populations in a meta­ metapopulation population have gone gone extinct

Local population population

Metapopulation Metapopulation

Metapopulation Metapopulation structure

Levins metapopulation metapopulation

Mainland- island Mainland-island metapopulation metapopulation

Source-sink Source-sink metapopulation metapopulation

Nonequilibrium Nonequilibrium meta population metapopulation

Turnover Turnover

Metapopulation Metapopulation persistence persistence time

(continues)

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TABLE TABLE II (continued) Term

Synonyms and definition

Patch Patch model

Synonyms: Occupancy Occupancy model, presence/absence presence/absence model Definition: A metapopulation metapopulation model in which local population population size is ignored patches ignored and the number number (or fraction) of of occupied occupied habitat habitat patches is modeled modeled Definition: 1 969a; see Hanski, this Definition: The The model presented presented by Levins ((1969a; volume) volume) Definition: A model population sizes model in which the distribution distribution oflocal of local population sizes modeled is modeled Definition: A model model of of the stationary probabilities probabilities (incidences) (incidences) of of patches functions of patches being occupied, occupied, generally generally assumed assumed to be functions of the sizes and isolations isolations of of the patches Synonyms: Island model Definition: Model in which all local populations populations are equally con­ connected; patch models are patch models and structured metapopulation metapopulation models spatially implicit implicit models Synonyms: Lattice (grid) model, model, cellular automata automata model, stepping­ steppingmodel stone model migration is distance-dependent, Definition: Model in which which migration distance-dependent, often restricted to the nearest habitat habitat patches; the patches patches are typically identical identical cells on a regular regular grid, and only presence presence or absence absence of of species in considered (the model is called a coupled the species in a cell is considered map continuous map lattice model if population population size in a patch is a continuous variable) Synonyms: Spatially explicit model (note that we make make a distinction distinction between spatially explicit and spatially spatially realistic realistic models) between Definition: Model that assigns assigns particular areas, spatial spatial locations, locations, and possibly other other attributes attributes to habitat patches, patches, in agreement with real real patch networks; spatially realistic models include simulation mod­ models and the incidence function model model

Levins Levins model model Structured Structured metapopulation model Incidence Incidence function function model Spatially implicit implicit metapopulation metapopulation model model

Spatially Spatially explicit explicit metapopulation metapopulation model

Spatially realistic metapopulation model metapopulation

a

Modified from Hanski and Gilpin, 11991, 99 1 , and Hanski, 11996a. 996a. "Modified

interactions populations connected interactions among among two conspecific populations connected by migration, migration, or with interactions interactions among among many many local populations. populations. The former former approach approach is useful useful when when the focus focus of of the study is specifically on the effect effect of of migration migration on local dynamics dynamics and one is willing to assume assume that that populations populations are so effectively regulated regulated that that extinctions Levin, 11974; 974; Holt, 11985; 985; Gyllenberg 993). In extinctions do not occur occur ((Levin, Gyllenberg et et a!. al.,, 11993). metapopulation metapopulation studies in the narrow narrow sense, when there there is population population turnover, turnover, it is necessary to resort resort to modeling modeling approaches approaches assuming assuming many many habitat habitat patches patches and and local populations. populations. Among Among these these approaches, approaches, we distinguish distinguish between between spatially im­ imHanski, 1994c). 1 994c). plicit, spatially explicit, and spatially realistic realistic approaches approaches ((Hanski, 1. Spatially Implicit Approaches Approaches

Truly signifi cant insights cation of significant insights are are often often based based on a critical critical simplifi simplification of what what at fi rst appears first appears a hopelessly hopelessly complex complex problem. problem. The model model that that Levins Levins (l969a, (1969a,

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11970) 970) constructed constructed to caricature caricature metapopulation dynamics is an excellent excellent example. example. Instead of attempting to extend a model of a single population to many popula­ Instead of attempting of population populations connected by migration, Levins modeled the changes in the number connected changes number of of such populations, effectively ignoring what what happens happens in each one of them and where where in space they happen to be located ((Hanski, Hanski, this volume). For the latter latter reason, reason, the Levins model and other related patch models (Table (Table I) are spatially implicit; the habitat patches and local populations are discrete (and are generally assumed to have independent independent dynamics), but they are are assumed to be all equally connected connected to each other. In spite of of this simplifying assumption, which can be generally de­ defended only for metapopulations close to steady state and with no strong spatial for strong aggregation, the patch models allow us to analyze many interesting questions about metapopulation dynamics, starting with the conditions of of metapopulation persistence persistence in a balance balance between between local extinctions and colonizations. The advan­ advantage of of the spatially implicit approach approach is that it greatly facilitates facilitates the mathematical mathematical and conceptual analysis; the disadvantage is that it can be used to study only a subset of of all interesting questions. Thinking about the restrictive assumptions assumptions of the Levins model and other patch models, ecologists have asked what happens when local dynamics are inin­ cluded in the metapopulation metapopulation model. What happens when the habitat patches are of different sizes and when the local populations have different extinction prob­ probabilities? abilities? What if migration rate rate is high enough to "rescue" local populations before extinction? What are are the consequences consequences of of real real spatial locations of of local populations? metapopu­ populations? What if extinction events are are correlated over the entire entire metapopulation? What What if there there is spatial asymmetry and source and sink populations? populations? Some of of these questions have been explored in the context of of spatially implicit models 988; Harrison and Quinn, 1989; 1 989; Hanski and 1 993; Gyl­ (Pulliam, 11988; and Gyllenberg, 1993; Gyllenberg et et at. al.,, this volume), but it comes as no surprise that that at some point we have to tum turn to models that that incorporate specific specific information on the spatial loca­ locahave tions of of populations. populations. Incidentally, most analyses of metapopulation genetics genetics (Bar­ (Barton and Whitlock, this volume; Hedrick and Gilpin, this volume) have been based on the Levins model, which is essentially equivalent to what population population geneti­ geneticists call the "island model." As in ecology, there there is an increasing increasing need to add space in a more explicit manner manner to metapopulation metapopulation genetic models. 2. Spatially Explicit Approaches

Under Under the rubric rubric of spatially explicit approaches approaches are are several related modeling modeling frameworks, such as cellular 1 993), interinter­ cellular automata automata models (Caswell and and Etter, Etter, 1993), acting particle systems ((Durrett, Durrett, 11989), 989), and coupled map lattice models ((Hassell Hassell et at., 11991a). 99 1 a). These et al., These modeling modeling approaches approaches assume that that "local populations" are arranged as cells on a regular lattice), with popUlation regular grid ((lattice), population sizes modeled as either discrete discrete or continuous variables. The key feature that distinguishes spatially localized interactions: explicit approaches from spatially implicit approaches is localized populations are assumed to interact only with populations in the nearby "cells." "cells." Localized interactions can have have profound dynamic consequences, consequences, such as very

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long times before the metapopulation settles to a steady state Hastings and Hig­ state ((Hastings Hig99 1 a; Nee et aI., this gins, 11994) 994) and spatially chaotic Hassell et chaotic dynamics ((Hassell et ai., al., 11991a; et al., volume). The disadvantage is that the the state state of of the metapopulation cannot cannot be de­ described presences and scribed simply by the fraction of of cells occupied; an entire vector vector of presences absences absences is needed. Such models require considerable considerable computation. An advantage is that, since each cell on the grid has a constant area area and constant spacing, the mathematical mathematical rules that govern local behavior are the same from cell to cell, and it is easy to write a computer program to model the dynamics. Lattice-based models and raster-based raster-based GIS descriptions descriptions in landscape landscape ecology share the the same format of representing space. Thus it is possible to develop com­ complex models that blur the distinction between between spatially explicit and spatially re­ realistic models ((below). below). From raster-based raster-based description of habitat suitability, one can aggregate "cells" "cells" into patches on which local populations may exist, thus reverting to a patch-based patch-based metapopulation model for for a dynamic analysis (Burg­ (Burgman et et al., 993; Ak�akaya, 994). al., 11993; Akqakaya, 11994). 3. 3. Spatially Spatially Realistic Realistic Models Models

Spatially realistic realistic models allow one to include in the model the specifi specificc ge­ geometry of particular particular patch networks: how many patches are there in the network, how large are they, and where infor­ where exactly are are they located? located? Including all this information in the model is necessary if one is interested interested in making specific quanti­ quantitative predictions about the dynamics of of real metapopulations. For instance, if we want to assess the likely consequences of destroying some particular particular patches patches in patch network, we need a spatially spatially realistic model. For For obvious reasons, the a patch spatially realistic field studies. realistic approach is closely linked with empirical field The incidence IF ) model ((Hanski, Hanski, 11994a,b, 994a,b, this volume) is perhaps incidence function ((IF) the simplest spatially realistic metapopulation model. The IF model is concep­ conceptually related related to the Levins model, but with the following critical differences: differences: there is a fi nite number finite number of of habitat habitat patches, and hence hence the model is stochastic stochastic in contrast to the deterministic Levins model; the patches are allowed to differ in area, which is assumed assumed to affect local extinction probabilities; probabilities; and and the the patches have specific spatial locations, which affect their probabilities probabilities of recolonization. Alternative Alternative spatially realistic approaches are based on extensive simulation of of many local populations connected by migration ((Hanski Hanski and Thomas, 11994; 994; Ak­ Ak�akaya, 994). Several generic models of this type are already available (Ak�ak­ qakaya, 11994). (Akqakaya, 11994; 994; Sjogren 996). Not surprisingly, meaningful appli­ Sjtigren Gulve and Ray, 11996). meaningful application of these models assumes much data. The extreme extreme approach approach is to simulate the birth, movements, reproduction, and death of individuals ((DeAngelis DeAngelis and Gross, 11992), 992), but this approach, which can be used for for any population structure, does not really take advantage of of the metapopulation concept. An individually based based modeling approach may nonetheless provide provide valuable insight into key pro­ processes affecting metapopulation dynamics, such as migration among populations ((Kindvall, Kindvall , 11995). 995).

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B. Empirical Empirical Approaches Approaches In a standard metapopulation study, a key initial task is to make standard ecological ecological metapopulation make a practical distinction between between habitat habitat and nonhabitat nonhabitat and and to delimit delimit the suitable habitat habitat patches patches in the study area. Suitable Suitable habitat habitat may be defined subjectively subjectively or or with the help Lawton and 1 99 1 ). An help of of statistical statistical methods methods ((Lawton and Woodroffe, Woodroffe, 1991). An experi­ experimental approach approach may be used used to test the accuracy accuracy of of an existing existing habitat habitat classifi­ classification: experimental ( Harrison, experimental introductions introductions to empty habitat habitat should should succeed succeed (Harrison, 11989; 989; Oates 990; Thomas, 992; Massot 994); introductions introductions Oates and and Warren, Warren, 11990; Thomas, 11992; Massot et et al., al., 11994); to nonhabitat Metapopulation studies focused nonhabitat should fail. Metapopulation focused on assemblages of of ex­ extinction-prone tinction-prone local local populations populations typically proceed proceed to record the the presence presence or ab­ absence of habitat patches of the focal species in the habitat patches and then then to analyze the effects effects of Verboom et al., 1991b; 1 99 1 b; of various various environmental environmental factors factors on patch patch occupancy occupancy ((Verboom et al., al., 11995a,b) 995a,b) and on the rates of Thomas 992; Hanski Thomas and Harrison, 11992; Hanski et et al., of extinction extinction and 99 1 ; Eber 994; Hanski 995b). and colonization colonization (Sjogren, (Sj/3gren, 11991; Eber and and Brandl, Brandl, 11994; Hanski et et al., al., 11995b). Other Other field studies have have been been concerned concerned with with more more permanent permanent local populations, populations, but ones migration (Stacey and ones whose whose dynamics dynamics are are significantly affected by migration Taper, this volume). volume). Experimental Experimental studies studies have attempted attempted to demonstrate demonstrate the pre­ predicted populations in a metapopulation dicted temporal stability of of local populations metapopulation as opposed opposed to that Murdoch et 1 996; Harrison that in isolated isolated local populations populations ((Murdoch et ai., al., 1996; Harrison and and Taylor, this volume). Landscape ecology ((Forman and Godron, Godron, 11986; Turner, 11989; Landscape Forman and 986; Turner, 989; Wiens, Wiens, this volume) volume) and and metapopulation metapopulation ecology share share a common common focus focus on space space and patchiness. The difference difference is primarily in the complex complex mosaic structure of of patchiness. mosaic structure object of volume). real landscapes landscapes that is the object of landscape landscape ecology ecology (Wiens, (Wiens, this volume). In contrast, contrast, metapopulation metapopulation studies studies typically typically assume assume that that the the patches patches which which are though this assumption used by the focal species species are of of the same type, though assumption is made made primarily for the sake of of keeping the models reasonably simple simple (see Holt, Holt, this re­ volume, for for metapopulation metapopulation models with two patch patch types). types). Empirical research in landscape landscape ecology has been been reluctant to use the the population population dynamic dynamic theory even if if in a rudimentrudiment­ theory that that metapopulation metapopulation ecology ecology purports purports to provide, provide, even ary form, two fields have form, and and consequently the two have developed largely independ­ independently. One One trend trend that is beginning beginning to change change this situation situation is the use of of GIS­ GISbased models based landscape landscape descriptions descriptions in generic metapopulation metapopulation simulation simulation models (Ak�akaya, 994). Today, ecologists have bases of digi­ (Ak~akaya, 11994). have access to huge data data bases of digitized information imminent arrival of low-cost information about about landscape landscape structure, and and the imminent arrival of low-cost global research in this global positioning positioning systems systems will greatly greatly facilitate further further empirical empirical research area. It should should come come as no no surprise surprise that the bulk bulk of of current current empirical empirical research research that is conceptually conceptually related related to the metapopulation metapopulation notion is conducted conducted in conservation conservation biology. We We therefore therefore devote devote the rest of of this chapter chapter to a more more thorough thorough scrutiny of conservation of the past past and present present links between between metapopulation metapopulation biology and and conservation biology.

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IV. METAPOPULATIONS METAPOPULATIONSAND AND CONSERVATION CONSERVATIONBIOLOGY BIOLOGY Conservation biology changed dramatically, beginning ca. 11975, 975, from a heavy emphasis on habitat relationships of individual species to a focus on refuge refuge design, guided by the dynamic theory of of island biogeography and the genetic deterioration 988). The two halves deterioration owing to drift drift and inbreeding (Simberloff, 11988). of this "new "new conservation biology" did not fi fitt together well, as the former dealt with species richness richness of communities, while the latter latter aimed at the population level. Currently, a replacement replacement of the island biogeographic component of of con­ conservation biology by metapopulation thinking is providing a more comfortable metapopulation fi t. Although fit. Although the incorporation of metapopulation models models into conservation bi­ biology has spurred spurred important insights, it has also led to some misfocused proposals.

A. The and Fall Fall of the Theory Island Biogeography The Rise Rise and Theory of Island Biogeography The theory of island biogeography ((MacArthur MacArthur and Wilson, 11963, 963, 11967) 967) quickly attracted Fig. 11)) by using attracted much attention from ecologists ((Fig. using simple math­ mathematics to focus on an easily obtained statistic (species richness) and depicting a dynamic nature that is nonetheless readily understood because because it is divided into small units, namely real or habitat 974, 11978a). 978a). The theory habitat islands (Simberloff, 11974, posits species richness on each island as a dynamic equilibrium maintained by continuing immigration of of all species, balanced by ongoing local extinctions on the island, primarily owing to demographic and genetic stochasticity. Clearly the island biogeographic theory shares key underpinnings underpinnings with meta­ metapopulation modelsmodelsmthe of nature nature into discrete entities, with movement the division of of of individuals among relatively unstable local populations. There is also an an ap­ apparent island biogeographic individ­ parent differencedifferencemisland biogeographic theory treats communities, not individual species. Its key statistic biogeo­ statistic is species richness. However, some island biogeographic graphic models are formally composites of of models for for individual species, with the community-wide immigration and extinction rates being simply sums of of the respective species-specific 969, 11983; 983; Gilpin and Diamond, species-specific rates (Simberloff, 11969, Diamond, 11981). 98 1 ). In these latter models, the underlying underlying conception conception of of what what is happening in nature - island version of Levins's Levins 's metapopulation nature is just a mainland mainland-island metapopulation concept (Hanski, (Hanski, this volume). However, even a species-based model of of this type, and even one with migration from from several sources, is still focused on a single island and on questions about the number number of of species and immigration and extinction rates on that island. A metapopulation model, even one in which the different sites and local populations are not modeled explicitly, focuses on the entire meta­ metapopulation population of of one or two species, using statistics such as the number of of sites occupied. In both types of models, an element element of arbitrariness arbitrariness is just how much move­ movement there there is between between sites for the models to remain remain useful. For For metapopulations, the bone of of contention is whether whether the movement is so frequent that one is dealing with a single population rather than a metapopulation, even if that that population

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may may be be so so large large that that individuals individuals are are likely likely to to interact interact with with their their neighbors neighbors only only ((Harrison, Harrison, 11991). 99 1 ). For For island biogeographic biogeographic models, models, the the argument argument is is whether whether groups of of conspecific conspecific individuals individuals on on sets sets of of islands islands are are separate separate populations populations or or groups just transient 975; Simberloff, transient parts parts of of one one widely widely ranging ranging population population (Smith, 11975; Simberloff, The latter argument has recrudesced recently with important conservation 11976). 976). The 1 988), extrapolating implications. Pimm et et al. al. ((1988), extrapolating from records of of breeding birds on small British islands, suggested suggested guidelines for how many individuals should should con­ constitute stitute propagules propagules for for reintroduction reintroduction efforts efforts based based on on the the body body size size of of the the species. species. Aside Aside from problems problems with the statistics statistics of extrapolation (Tracy (Tracy and and George, George, 11992), 992), Haila and 1 993) saw a more fundamental fl aw: the assumption and Hanski ((1993) flaw: that the birds on each island constituted a population, and their disappearance an are parts of wide-ranging, large large popula­ populaextinction. In their view, all these birds are tions and their disappearances from specifi specificc islands within the range are not pop­ population phenomena. Diamond and Pimm ((1993) 1 993) retorted that the birds of each island could be viewed as a population within a metapopulation. Within about a decade ((Fig. Fig. 11), ), the theory of island biogeography came to dominate much of conservation biology, with a series of nearly simultaneous papers (Terborgh, 11974, 974, 11975; 975; Diamond, 11975a; 975a; Wilson and Willis, 11975) 975) all advocating a set of "rules" of refuge design ostensibly based on the theory ((Fig. Fig. guration that would maximize 2). The rules each suggest a refuge confi configuration maximize species richness, and the papers describing the rules rules apparently stemmed stemmed from lectures given by E. O. Willis beginning in 11971 97 1 (Willis, 11984). 984). Although some of of the rules in fact were not based on the theory (references 1 988); they (references in Simberloff, Simberloff, 1988); publication in 1980 1 980 became popular in conservation circles, circles, particularly after their publication rst synthetic plan for dealing first dealing with a perceived disastrous wave of of extinc in the fi Union tions, World World Conservation Strategy, jointly authored by the International International Union for of Nature Nature and Natural Resources, the United United Nations, and for the Conservation of Natural Resources, and World Wildlife Wildlife Fund. With this imprimatur, imprimatur, it is unsurprising un surprising that that these these rules, the World and the the theory theory that that supposedly supposedly supported became the the governing paradigm and supported them, them, became paradigm conservation biology, reproduced in textbooks and published published in newspapers. newspapers. in conservation The The dominance dominance of of the the island island biogeographic biogeographic paradigm paradigm was was so strong strong that that even even studies that that today would would be be seen seen as metapopulation metapopulation research research were were published published as studies island island biogeographic studies, studies, with no no mention mention of of the the term term "metapopulation" "metapopulation" (e.g., (e.g., Fritz, Fritz, 1979). 1 979). was noted noted early that that most most ecological ecological publications publications citing citing island island biogeobiogeo­ It was graphic theory theory simply simply interpreted interpreted aa species-area species-area relationship relationship in in terms terms of of the the thethe­ graphic ory, ory, when when alternative alternative explanations explanations were were also also possible possible (Simberloff, (Simberloff, 1974), 1 974), and and that that there there was was little little empirical empirical evidence evidence for for continuing continuing local local extinctions extinctions of of the the sort sort envisioned by by the the theory theory (Lynch (Lynch and and Johnson, Johnson, 1974; 1 974; Simberloff, Simberloff, 1974). 1 974). Further, Further, envisioned as noted noted by by Smith (1975) ( 1 975) and and Simberloff Simberloff (1976), ( 1 976), by by defining defining the the comings comings to to and and as goings goings from from local local sites sites of of individuals individuals within within continuous continuous populations populations as as "immi"immi­ gration" and and "extinction," "extinction," one one could could almost almost always always claim claim that that extinctions extinctions and and gration" colonizations were were occurring, occurring, even even if if the the theory theory really really envisioned envisioned most most recruitrecruit­ colonizations ment to to local local populations populations as as being being by by in in situ situ reproduction reproduction rather rather than than immigration. immigration. ment

1188

IIkka Ilkka Hanski Hanski and and Daniel Daniel Simberloff Simberloff a

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The 1 975; The "island "island biogeographic" biogeographic" rules rules for for refuge refuge design design (after Wilson Wilson and Willis, 1975; International Union Union for for the the Conservation Conservation of of Nature Nature and and Natural Resources, each rule, the International Resources, 11980). 980). For each design on alternative on design on the the left left is is seen seen as as superior superior to to the the alternative on the the right. right.

Nevertheless, Nevertheless, ecologists ecologists on the whole tended tended to view the theory theory favorably until around 11980, doubt about about the existence existence of widespread local extinction extinction be­ bearound 980, when doubt of widespread came pervasive (Gilbert, 1980; 1 980; Schoener 1 987b; Williamson, 989). Schoener and Spiller, 1987b; Williamson, 11989). The involves a subset The prevailing prevailing view view now now is that, in most most systems, "turnover "turnover involves subset of of fugitive fugitive populations, populations, with with many others, others, mostly much much larger, being permanent" permanent" (Schoener 987b). The decline (Schoener and Spiller, Spiller, 11987b). decline in citations of of "island "island biogeography" biogeography" ((Fig. Fig. 1) 1 ) reflects the declining longer seen as declining faith faith in the theory. Though Though it is no longer a model for biogeographic theory provided theoretical for much much of of nature, nature, island biogeographic provided a theoretical perspective from which to view a number number of - area perspective from of patterns, patterns, such as the species species-area relationship Haila and Jarvinen, 1982). 1 982). relationship ((Haila The biogeography The key key conservation conservation legacies of of the the dynamic theory of of island biogeography were ((1) 1 ) the interest in the the metaphor metaphor of of a refuge refuge as an island island or spaceship, (2) interest fragility of refuges and causes of of the biota of of individual refuges of this fragility (Soule (Soul6 and Simberloff, 986; Simberloff, 994a), and Fig. 2). Simberloff, 11986; Simberloff, 11994a), and (3) the rules of of refuge refuge design design ((Fig. The The recognition recognition that some of of the the rules, including including the the most most widely debated debated one (SLOSS, related to the theory (Soule (SLOSS, single large or several small; Fig. 2b) are not not related theory (Soul6 and 986, and and Simberloff, Simberloff, 11986, and references references therein), lessened lessened conservation conservation interest in

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the theory, while documented exceptions to some of the rules, including SLOSS, led to their fall from status of conventional wisdom. For example, the the third edition Ecology ((Krebs, of one of the most widely used introductory ecology textbooks, Ecology Krebs, popularized by the IUCN and 11985, 985, p. 559), reprinted the figure of the rules as popularized described them as flowing from island biogeographic theory. The fourth edition figure, of the rules, and cites the ((Krebs, Krebs, 11994) 994) omits the fi gure, makes no mention of criticism of the theory as "true but trivial" by Williamson ((1989). 1989).

B. Paradigm Shift waning of the theory theory of island biogeography as a dominant conservation The waning paradigm in the late 11980s 980s coincided with the burgeoning burgeoning interest among biolo­ biologists in the metapopulation concept ((Fig. Fig. 11). ). As does Hanski ((1989), 1 989), Merriam "Metapopulation models have ((1991, 1 99 1 , p. 1134) 34) explicitly claims a paradigm shift: "Metapopu1ation of thinking thinking about largely replaced equilibrium island biogeography as a way of heterogeneous terrestrial en­ enterrestrial habitat islands, fragmented habitats and heterogeneous conservation biologists, the shift is tacit vironments in general . . . " For other conservation of an assertion that nature nature is structured structured as metapopulations metapopulations and consists simply of discussion of of what actions are required required to preserve followed by discussion preserve metapopulations Perhaps most telling is The Diversity of of Life, (e.g., Noss, 11993). 993). Perhaps Life by Wilson ((1992), 1992), founder of of the the theory of of island biogeography, biogeography, in which species species are typically a founder seen as structured as metapopulations consequences of metapopulations and and the consequences of this structure for conservation are explored. The causes of lit­ of the shift shift are are many. One One must be the growing growing ecological litdescribed above, doubting doubting the verisimilitude of of island biogeographic biogeographic the­ theerature, described ory. However, data and However, scientific data and the weakness of of a prevailing prevailing paradigm paradigm alone are paradigm shift (Kuhn, ( Kuhn, 1970; 1 970; Haila, 1988), 1 988), and and we are unlikely to precipitate a paradigm must seek other other prevailing that, fundamentally, prevailing currents. currents. It is worth worth recalling recalling that, fundamentally, the the theory can be construed multispecies version version of theory of of island biogeography biogeography can construed as just just a mUltispecies of an analogous to imagine objective objective scientific scientific analogous metapopulation metapopulation theory, so it is hard hard to reasons for accepting one while rejecting other. reasons for accepting one rejecting the other. One among conservation One possible possible explanation explanation is a shift among conservation biologists biologists and and ecolecol­ ogists from conception of of nature that of ogists from the the conception nature as an equilibrium equilibrium world world to to that of a nonnon­ equilibrium equilibrium one one ((Wiens, Wiens, 1977, 1 977, 1984; 1 984; Chesson Chesson and and Case, 1986). 1 986). Island Island biogeobiogeo­ graphic of course, course, but but the emphasis emphasis is on on equilibrium equilibrium species graphic theory theory is dynamic, of richness, richness, hence hence the the nickname, nickname, "equilibrium "equilibrium theory," theory," and and even even the the underlying underlying imim­ migration and are seen migration and extinction extinction rates rates are seen as constant. constant. Though Though metapopulation metapopulation thethe­ ories are are not not any more, more, or or less, "equilibrium" "equilibrium" theories theories than than the the theory of island island ories theory of biogeography, biogeography, the the emphasis emphasis in in the the latter latter on on equilibrium equilibrium species species richness richness and and in in the created the the former former on on population population turnover turnover may may have have created the sense sense of of aa conflict conflict bebe­ tween tween an an equilibrium equilibrium and and aa nonequilibrium nonequilibrium theory. theory. The The key key point, point, of of course, course, is that that in both both theories theories there there is no no equilibrium equilibrium at the the population population level. However, However, the the modus operandi operandi of of the the island island biogeographic biogeographic theory theory is to to ignore ignore the the changes changes in in modus the the presences presences and and absences absences of of individual individual species species and and to to focus focus on on the the equilibrium equilibrium ,

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IIkka Hanski Hanski and and Daniel Daniel Simbedoff Simberloff Ilkka

pattern of of species species richnesses; richnesses; this this theory theory is is spatially spatially implicit implicit in in our our taxonomy. taxonomy. pattern Yet two two growing growing interests interests in in conservation conservation are are spatially spatially explicit explicit models, models, to to aa large large Yet extent fostered fostered by by an an increase increase in in spatial data data and and the the use use of of GIS, GIS, and and maintenance maintenance extent of species species that that are are destined destined to to be be locally locally ephemeral, ephemeral, such such as as fugitive fugitive species species and and of successional ones. The The metapopulation metapopulation theory fits fits well with these interests. interests. early successional Indeed, a critical critical difference difference between between the the models models of of MacArthur MacArthur and and Wilson Wilson (1967) ( 1 967) Indeed, and Levins Levins (1969a) ( l 969a) is the presence of of a permanent permanent mainland mainland population population in the the and the presence former but not in the latter. former but not the latter. addition to to island island biogeographic theory, the the other other main main component of of the the In addition "new conservation conservation biology" is population population genetics, genetics, particularly particularly the study of of drift drift "new and and inbreeding inbreeding in small populations populations (Simberloff, (Simberloff, 1988). 1 988). This research research tended tended to the focus of of conservation conservation biologists biologists from communities to species species and and poppop­ shift the from communities ulations. Ecological Ecological aspects of of conservation conservation began also to be be seen in terms terms of of ulations. populations rather than than species--the populations rather species -the role role of of demographic demographic and and environmental environmental stosto­ chasticity in setting minimum viable population population sizes is the the prime prime example example (Sim(Sim­ berloff, 1988). 1 988). Again, a focus on populations populations rather rather than on communities communities is bound bound berloff, island biogeographic theory relevant. to make island theory seem seem less relevant. rescued small sites from their devaluation Finally, metapopulation metapopulation models models rescued devaluation by island biogeographic theory. The The main main ecological data interpreted island interpreted in ter.TIS tev,~as of of island biogeographic theory were species- area relationships, relationships, showing island were simply species-area other things things being equal, equal, large tend to have more species than that, all other large sites tend more species than small of refuge relationship as a ones. The The first rule of refuge design (Fig. 2a) expresses expresses this relationship mandate for planners. The The rules, and the theory, were widely used used mandate for conservation planners. to argue that that large refuges are needed needed and and the the elevated elevated extinction rates in small small refuges are extinction rates render them depauperate (e.g., Diamond, 1972; 1 972; Soul6 Soule et et al., al. , ones will inevitably render them depauperate 1 979). Indeed, to the extent that environmental stochasticity and catastrophies 1979). extinguish small populations, mathematical mathematical modeling suggested that even popu­ popuparks in the United lations in enormous refuges, the size of the largest national parks States, would would be States, be subject subject to to collapse. collapse. Conservationists eventually recognized recognized that that astute opponents could tum turn this emphasis on inviable small populations populations against against conservation. conservation. For example, the refuge system of of the small nation of Israel consists of some 200 reserves, many managed to various degrees by of which are very small. These are protected and managed the Nature Conservation Authority, and and the Authority was under under great pressure during the 11980s 980s to abandon abandon some small refuges, not because specifi specificc research research showed declining populations within them but because island biogeographic the­ theory, ory, codified in the refuge design rules, shows that they will inevitably lose species ((R. R. Ortal, 984). Ortal, personal personal communication, communication, 11984). This threat from island biogeographic theory to the maintenance of small reserves area relationship was reserves was forestalled in several ways. The speciesspecies-area shown to have such wide confi dence limits that an assertion of imminent faunal confidence collapse could not be sustained (Boecklen and Simberloff, 11986). 986). Some popu­ populations that had persisted as very small populations for millennia were adduced as cautions against taking the theory too literally (e.g., Walter, 11990). 990). However,

1 The Metapopulation Metopopulotion Approach Approach

21 21

the the main main salvation salvation of o f small small sites sites was was the the shift shift by b y conservationists conservationists to to the the metameta­ population paradigm. paradigm. In In the the Levins Levins model, model, at at least, least, small small sites sites containing containing small small population populations were were the the only only homes homes of of aa species species and and thus thus the the proper proper locus locus of of concon­ populations servation concern. concern. The The model model even even suggests suggests that that aa certain certain number number of of unoccupied unoccupied servation required for metapopulation persistence persistence (Lande, (Lande, 1988a; 1 9 88a; Hanski, this volvol­ sites is required for metapopulation thus relieving relieving beleaguered beleaguered conservation biologists from having to to justify justify aa ume), thus conservation biologists from having refuge for for a given species by by confirmed confirmed residence. A A famous famous example example in which which refuge local extinction extinction rates high and and aa supply supply of of suitable suitable empty empty sites sites is necessary necessary local rates are high is Pedicularisfurbishae, Pedicularis furhishae, the Furbish Furbish lousewort lousewort (Menges, ( Menges, 1990). 1 990). In sum, sum, from from a conservation conservation standpoint, standpoint, it is not not surprising surprising that that citations citations of of metapopulation studies increase exactly when those of island biogeography de­ metapopulation studies increase exactly when those of island biogeography decline (Fig. (Fig. 1). 1 ) . These trends represent represent aa paradigm paradigm shift. shift. cline These trends

Misuse of the Metapopulation Concept Concept in Conservation Conservation Biology C. Use and Misuse Hanski and 1 99 1 ) observed have recently Hanski and Gilpin ((1991) observed that that "metapopulation "metapopulation ideas have become become the vogue in conservation biology," and and numerous numerous conservation strategies strategies are explicitly explicitly based based on metapopulation models (references metapopulation models (references in Harrison, Harrison, 1994b). 1 994b). The general effect been to draw draw attention to landscapes and networks, The effect has has been landscapes and networks, as opposed individual reserves reserves in isolation, isolation, for metaphor of of island opposed to individual for which the island metaphor biogeographic theory is appropriate. This is a salutary development. Even Even if if there biogeographic appropriate. This were no different refuges, no significant significant interactions interactions among populations populations in different refuges, it would would be good good to have have multiple refuges refuges simply as insurance insurance against against local catastrophes catastrophes (Soule and 1 986). Doak Doak and and Mills (1994) ( 1 994) and and Harrison Harrison (1994b) ( 1 994b) argue (Soul6 and Simberloff, Simberloff, 1986). argue not structured that, even if most species species are are not structured as Levins-type metapopulations in nature, the rise of of the metapopulation paradigm has served and continues continues to serve function by forcing conservation conservation biologists to gather gather data that are imim­ a useful function portant to effective conservation strategies of of individual speciesspecies--movement portant movement rates at different different sites, rates from site to site, relative reproduction reproduction and mortality rates and 1 982) for and the like. This is precisely the the view of of Haila and and Jarvinen J~irvinen ((1982) for island biogeographic biogeographic theory. theory. The problems arise, for for metapopulation models as for for island biogeographic theory, when it is assumed without empirical evidence that all species, or all species in a large class, conform to some particular model ((Doak Doak and Mills, 11994; 994; Harrison, 11994b). 994b). If a conservation conservation strategy is based based on metapopulation dynamics that do not exist, it can misfire. Thus, for example, Murphy et al. ((1990) 1 990) suggested that small-bodied, short-lived species with high reproductive rates and high hab­ habitat specificity typically constitute Levins metapopulations, but there there are are simply insuffi cient data to evaluate this claim ((Harrison, Harrison, 11991, 99 1 , 11994b). 994b). To focus auto­ insufficient automatically on metapopulation dynamics for such species would not constitute ef­ effective science. No wide-ranging generalizations are yet possible, because few data really demonstrate the existence of classical metapopulations. Harrison ((1991) 1 99 1 ) could cite only pool frogs (Rana lessoniae) in Sweden and waterfties waterflies (Daphnia) in rock pools as unequivocal cases (for some new examples, see Har-

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Ilkka Hanski HanskJand and Daniel DanielSimberloff Simberloff IIkka

rison and Taylor, this volume). The endangered endangered Glanville fritillary butterfly (Mel­ (Melitaea Hanski et al., 11995a,b) 995a,b) and itaea cinxia) cinxia) in Finland is another another good example ((Hanski may represent many other butterfly species ((Hanski Hanski and Thomas, 11994; 994; Hanski and Kuussaari, 11995; Thomas and Hanski, this volume). In such instances, an 995; understanding of metapopulation dynamics is crucial to effective conservation. understanding metapopulation Research is required required on local extinction and migration rates rates and how these are Research affected by patch size and isolation (c. (C. D. Thomas et al., al., 11993; et al., al., 993; Hanski et affected D. Thomas 11995b). 995b). Harrison ((1994b) l 994b) suggests that the the species most most convincingly conforming conforming to the Levins model occupy habitats that inevitably change because of of succession succession the (see also Thomas Thomas and and Hanski, Hanski, this volume). In many such species, the extinction populations is deterministic deterministic rather rather than stochastic, stochastic, but this fact fact does not of local populations conception of metapopulation metapopulation dynamics. The fundamentally undercut the Levins conception lousewort, for example, requires a riverside habitat that is endangered Furbish lousewort, neither too little nor too heavily disturbed disturbed (Menges, (Menges, 11990). However, any local 990). However, population is ultimately destroyed destroyed by ice scour and and bank bank slumping, slumping, so the metapopulation meta­ population requires a supply of of temporarily suitable suitable sites that are not not too isolated isolated population colonized. A metapopulation to be colonized. metapopulation analysis ((Menges, Menges, 11990) 990) including including observaobserva­ and recolonization suggests that the species is in decline decline tions on local extinction and rather than than at equilibrium equilibrium and and that that tempering of the disturbance disturbance (flow) regime rather tempering of exacerbate the situation. situation. Further, Further, in this species species as in the Levins scewill likely exacerbate Levins sce­ nario (Lande, 1988a; 1 988a; Hanski, this volume; Nee et al., this volume), volume), nario in general general (Lande, et al., restriction of of conservation conservation measures measures to occupied occupied sites only would would be fatal. A restriction of nature nature would not have have led to the recognition recognition static, nonmetapopulation nonmetapopulation view of of the importance importance of of currently currently unoccupied habitat. Much Much of of the history of of refuge refuge of unoccupied habitat. establishment simply of apparently healthy populations and preestablishment consists consists simply of locating locating apparently populations and pre­ serving their sites sites (Simberloff, (Simberloff, 1988). 1 988). Metapopulation Metapopulation models models have have been been used used to to deduce deduce the the minimum minimum viable viable metameta­ population population (MVM) ( MVM) size under under certain certain assumptions assumptions (Hanski ( Hanski et et al., al., 1996b). 1 996b). This This concept analogous to the concept is analogous the minimum minimum viable viable population population (MVP) ( MVP) size (Shaffer, (Shaffer, 1981), 1 98 1 ), but with the the critical difference difference that MVM MVM involves involves both the the minimum minimum viable number number of of populations of suitable suitable habitat habitat patches ( Han­ viable populations and and the availability availability of patches (Hanski et et al., al., 1996b). 1 996b). In practice, practice, use use of of these these concepts concepts may degenerate degenerate into specious specious "magic more constructive constructive approach approach is to use "magic numbers." numbers." A more use metapopulation metapopulation models models to rank scenarios of of landscape landscape change persistence of of a focal focal to rank alternative alternative scenarios change in terms terms of of persistence species. entire removal species. One One may may ask, ask, for for instance, instance, whether whether the the entire removal of of one one large large habitat habitat patch is more more detrimental detrimental to to aa metapopulation metapopulation than than reducing reducing the the areas areas of of several several patch patches patches (Hanski, (Hanski, 1994a,b; 1 994a,b; Hanski Hanski et et al., al., 1996c; 1 996c; Wahlberg Wahlberg et et al., al., 1996; 1 996; note note the the connection to to the the SLOSS SLOSS rule, Fig. 2b). The The theory theory of of island island biogeography biogeography inin­ connection spired spired the the rules rules of of refuge refuge design design discussed discussed above above (Fig. ( Fig. 2). The The analogous analogous contricontri­ bution from from metapopulation metapopulation theory theory is predictions predictions about about the the relative relative performance performance bution of particular particular species species in particular particular fragmented fragmented landscapes landscapes based based on on relatively simsim­ of ple ple but but spatially realistic realistic models models (Fig. ( Fig. 3, 3 , Hanski, Hanski, 1996b). 1 996b). There There are are two two reasons reasons to to expect expect the the latter latter sorts sorts of of predictions predictions to to be be more more helpful helpful than than the the island island biogebioge-

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FIGURE examples of the same FIGURE 3 Four Fourexamples same landscape landscape fragmented fragmented in different different ways ways (scenarios (scenarios a to d). Spatially model (Hanski, 1 994a), can Spatially realistic realistic metapopulation metapopulation models, models,such such as the incidence incidence function function model (Hanski, 1994a), be used time of the focal used to rank rank the alternative alternative scenarios scenarios in terms terms of the persistence persistence time focal species. species. Note Note the conceptual link to the SLOSS 2b). conceptual link SLOSS rule rule (Fig. (Fig. 2b).

ographic Fig. 2) ographic rules rules of of refuge refuge design. First, First, the the rules rules of of refuge refuge design ((Fig. 2) are are static, static, even even those those actually actually flowing flowing from from the the theory. theory. For For example, example, the the fundamental fundamental con­ concept Fig. 2a) which in applications is cept in in rule rule aa ((Fig. 2a) is is the the species-area species-area relationship, relationship, which in applications is seen xed area. seen as as meaning meaning aa fixed fixed number number of of species in in aa fi fixed area. In In contrast, contrast, the the meta­ metapopulation predictions explicitly address the dynamics of of species survival. Sec­ Second, the rules of refuge design contrast fixed general alternatives (such as in Fig. 2b), 2b), whereas whereas the the spatially spatially realistic realistic metapopulation metapopulation models models practically practically force force one one to Fig. 3). to compare compare specific specific fragmented fragmented landscapes landscapes ((Fig. 3). We We now now tum turn to to potential misuses of of the metapopulation concept in conser­ conservation. island (Levitt­ vation. To To start start with, with, if if aa species species is is structured structured as as aa mainlandmainland-island (LevittBoorman) Boorman) metapopulation, metapopulation, population population turnover turnover in in the the peripheral peripheral "island" "island" popu­ populations lations may may be be irrelevant irrelevant to to the the persistence persistence of of the the metapopulation metapopulation as as aa whole, whole, though though the the dynamics dynamics are are crucial crucial to to the the persistence persistence of of the the peripheral peripheral populations populations ((Doak Doak and 994; Harrison, 994b, Simberloff, 994b). More and Mills, Mills, 11994; Harrison, 11994b, Simberloff, 11994b). More generally, generally, emphasis emphasis on on metapopulation metapopulation models models can can potentially potentially harm harm conservation conservation by by draw­ drawing ing attention attention away away from from single single populations populations on on the the grounds grounds that that no no one one of of these these is Harrison, is crucial crucial to to aa species species'' persistence persistence and and it it is is the the ensemble ensemble that that matters matters ((Harrison, 11994b). 994b). Another Another example example of of the the metapopulation metapopulation concept concept used used in in misguided misguided attempts attempts

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Ilkka Hanski Hanskiand and Daniel DanielSimberloff Simberloff IIkka

to to deemphasize deemphasize single single populations is is the the hype hype surrounding surrounding movement corridors corridors we observe observe that, that, strictly strictly speaking, speaking, metapopulation models tend tend to to em­ em(though we phasize phasize connectance connectance among among habitat habitat patches, patches, not not corridors). corridors). One One rule rule of of refuge refuge design associated associated with island island biogeographic biogeographic theory theory is is that that aa set set of of refuges refuges con­ condesign nected nected by corridors corridors will contain contain more more species than than an an otherwise otherwise identical set set without corridors corridors (Fig. 2f). 2f). In the original original formulation of of this rule, the focus was on on aa community-level community-level statistic, species species richness, and corridors were were assumed to to increase increase this statistic statistic by increasing increasing immigration rate. rate. However, for most proposed corridor systems, systems, there there is scant evidence that that the corridors corridors would be used for movement or that they would actually forestall extinction Hobbs, 11992; 992; Sim­ movement or that they would actually forestall extinction ((Hobbs, Sim992). Even more berloff et et at., al., 11992). more troubling, investment in corridors can be expen­ expensive and can detract from efforts to protect particular populations that require a 992). specific refuge that is not part of a network (Simberloff et at., al., 11992). Some examples of classical metapopulations in human-fragmented land­ landscapes may represent transient, nonequilibrium situations, in which a previously more continuous population becomes divided into smaller units, with consequent consequent assemlocal extinctions, but no functional metapopulation was created, merely an assem­ blage blage of of populations populations all all slowly slowly declining declining to to extinction. extinction. It It seems seems likely likely that that almost almost any any gradual gradual extinction extinction would would appear, appear, during during some some parts parts of of the the decline, decline, as as aa non­ non994b ). Even in this case, unun­ equilibrium metapopulation situation (Simberloff, I1994b). derstanding derstanding its current current dynamics can aid in the maintenance maintenance of of the species species in a fragmented Harrison, 11991). 99 1 ). In SLOSS fragmented or otherwise changed changed landscape landscape ((Harrison, SLOSS termi­ terminology ((Fig. Fig. 2b), a single large large population might might have been better, better, but if all we small ones, their their interactions may be crucial to their their survival. have left is several small For example, the the metapopulation analysis by Beier of cougars (Felis con1 993) of (Felis con­ For Beier ((1993) color) color) in the the Santa Santa Ana Ana Mountains Mountains of of California California showed showed that that the the species species currently exists as a collection of populations loosely linked linked by riparian riparian corridors, corridors, exists of small populations and radiotelemetry data and his radiotelemetry data on movement combined combined with a simulation model model of particular particular populations populations and could affect the entire entire suggested how loss of and corridors corridors could affect the Data on sources sinks in source-sink source- sink metapopulation metapopulation can metapopulation. Data sources and and sinks can also also be be key key to to maintaining maintaining a species. species. A A particular particular worry about about nonequilibrium nonequilibrium metapopulations in increasingly increasingly fragmented fragmented landscapes landscapes is that that we we might might not not recrec­ metapopulations ognize them them as as such such (Hanski, ( Hanski, this this volume), volume), which which would would give give us us a misleadingly misleadingly ognize rosy picture picture of of the the ability of of species species to to persist persist in present present landscapes. landscapes. rosy Attempts to to model model the the minimum minimum number number of of populations populations necessary necessary to to mainmain­ Attempts tain tain aa viable viable metapopulation metapopulation are are hampered hampered by by assumptions assumptions that that are are hard hard to to verify verify and and data data that that are are difficult difficult to to gather. gather. These These are, are, of of course, course, problems problems with with all all poppop­ ulation models models that that aim aim at at quantitative quantitative predictions, predictions, and and the the problems problems become become even even ulation more severe severe with with spatially spatially realistic realistic models models that that might might guide guide specific specific management management more 1 994). The The history history of of conservation conservation biology biology is is marked marked by by plans (Doak ( Doak and and Mills, Mills, 1994). plans many examples examples of of misused misused minima minima (Simberloff, (Simberloff, 1988; 1 988; Crome, Crome, 1993): 1 993): as as soon soon as as many minimum is is set set for for any any variable, variable, forces forces opposed opposed to to conservation conservation use use itit to to see see aa minimum how much much of of nature nature they they can can get get rid rid of. of. Thus, Thus, as as tentative tentative and and general general as as the the how MYM model model is, is, someone someone may may attempt attempt to to manage manage for for aa specific specific minimum minimum based based MVM

Metapopulation Approach 1 The The AAetapopulation Approach

25

discussed above, a less controversial controversial use of of spatially realistic on this model. As discussed metapopulation Fig. metapopulation models models is simply to rank rank alternative alternative management management scenarios scenarios ((Fig. 3) and recognize that making long-term predictions predictions about and to recognize making long-term about (meta)population (meta)population persistence persistence time time in our our rapidly changing changing world is practically practically hopeless. hopeless. The The shift from from island island biogeographic biogeographic to metapopulation metapopulation thinking thinking united united ecol­ ecologists and and geneticists geneticists in focusing focusing on populations. populations. Genetic Genetic concerns concerns have have been prominent 1 963) fi rst prominent in the interest in metapopulations. metapopulations. Kimura Kimura and Crow Crow ((1963) first pointed populations can maintain pointed out that occasional occasional migration migration between between local populations maintain genetic variation population, essentially because variation better better than would would a single large population, drift is likely to fi populations. However, the situ­ fixx different different alleles in different different populations. situation becomes becomes more complicated complicated when we allow for for local extinctions extinctions and recol­ recolonizations, modeling the way that such onizations, and recently much much effort effort has gone into modeling population turnover affects the maintenance of genetic diversity in metapopula­ population turnover affects maintenance of metapopulations (Wade and McCauley, 1 988; Hastings and Harrison, 1 994; Barton Barton and Whit­ (Wade McCauley, 1988; Harrison, 1994; and Whitlock, this volume). volume). On theoretical grounds, one might expect species species that naturally metapopulations not to be prone inbreeding depression because they exist in metapopulations prone to inbreeding lack genetic Harrison, 1994b), 1 994b), while local populations populations in a recently frag­ genetic load ((Harrison, fragmented mented large population population might might be particularly susceptible susceptible to inbreeding inbreeding depres­ depression because heterozygosity would 988; Hedrick would quickly decline (Simberloff, (Simberloff, 11988; Hedrick and Gilpin, this volume). movement volume). Under Under the latter latter circumstances, maintaining maintaining movement among among populations populations might seem particularly particularly important, important, and indeed indeed many man­ management plans for for declining declining populations call for for measures to enhance enhance population population agement interaction, cally to avoid inbreeding inbreeding interaction, such as translocation translocation and corridors, corridors, specifi specifically depression (e.g. 995). However, eld evidence (e.g.,, U.S. Department Department of of Agriculture, 11995). However, fi field evidence inbreeding depression depression or other other problems problems in recently fragmented fragmented populations populations for inbreeding Harrison, 1994). 1 994). Lande l 988b) argues more generally that the imporimpor­ is scarce scarce ((Harrison, Lande ((1988b) tance of of genetic threats in conservation conservation has been overblown. overblown. His view is that, in naturally small populations, populations, the genes genes causing causing threatening inbreeding inbreeding depression depression would populations, ecological would have have been been selected out, while in recently reduced reduced populations, threats are immediate. Despite are more more immediate. Despite this widely cited statement, statement, genetic principles principles still underpin Harrison, 1994b). 1 994b). underpin many viability analyses and management management plans plans ((Harrison, Perhaps Perhaps the the very fact that genetic genetic modeling modeling is feasible feasible ensures ensures that it will be done. done, particularly if ecological prob­ ecological modeling, modeling, even if potentially more more useful, useful, is more prob1 995) appears lematic. The latest round round of of papers papers (e.g., Lynch et et al. al.,, 1995) appears to strengthen strengthen the genetic argument, but eld studies. but the most urgent urgent need need is for for relevant fi field studies. Thompson 1 996) contends Thompson ((1996) contends that that metapopulations metapopulations may be crucial crucial to the con­ conservation servation of of various various coevolutionary coevolutionary interactions, interactions, such as those those between between pathogens pathogens or parasites parasites and their hosts. In models, models, locally unstable unstable population population dynamics dynamics can 99 1 a; be stabilized by the addition Hassell et addition of of metapopulation metapopulation structure ((Hassell et al., al., 11991a; Nee metapopulation structure Nee et et al. al.,, this this volume). volume). In other other cases, the metapopulation structure stabilizes stabilizes evolutionary dynamics under certain dynamics of of the interaction. interaction. For For example, example, under certain circum­ circumstances, between a pathogen stances, the coevolutionary coevolutionary dialog dialog between pathogen and its host host can lead to the extinction extinction of of the host, if if a new virulence virulence gene gene in the pathogen pathogen spreads spreads rapidly rapidly enough. enough. A metapopulation metapopulation structure structure can then prevent the gene from eliminating eliminating

26 26

IIkka Hanski Hanski and and Daniel Ilkka Daniel Simberloff SJrnberloff

the entire ax (Unum ax rust (Melampsora entire species. Wild fl flax (Linum marginale) and flflax (Melampsora lini) may be a natural natural example example in which the host metapopulation metapopulation structure serves this function B urdon and Thompson, 1995). 1 995). Frank (this volume) presents function ((Burdon presents a thorough discussion of these issues. The focus on metapopulations, combined combined with that that on genetics, has led to the population and the species becoming the dominant con­ dominant levels of of concern in conservation. It is striking that the recent explosion of man­ of interest interest in ecosystem management agement is quite antithetic antithetic to a primary interest in populations and to single­ singlespecies management (Simberloff, 11996). 996). In fact, a key motivation of of ecosystem management management is that that research on species after species will be hopelessly expensive and inefficient, inefficient, and so will management management based on such research. Of Of course, course, both ecosystem management management and metapopulation metapopulation models share a concern with land­ landscapes and regions, rather than than highly local settings, and and one could imagine a landscape with a distribution of of habitat habitat patches that would maintain many meta­ metapopulations simultaneously. Also, the emphasis in ecosystem management management on maintaining processes rather 996) can accommodate rather than species (Simberloff, 11996)can concerns about the coevolutionary processes. Nevertheless, Nevertheless, the research research programs programs and primary goals of of these two approaches differ differ fundamentally and they will surely compete compete for both research funding and and influence in specific management management plans in the future.

V. CONCLUSIONS CONCLUSIONS The The changing pattern of of citations citations of of the the key words "island biogeography" and "metapopulation" represents a fascinating example of of a paradigm paradigm shift in population biology. This example example is the more more striking striking because the respective respective theories are are so closely related related that whatever evidence can be mustered for, or against, against, one theory is likely to serve serve the same function with respect to the other other theory. We We have discussed in this chapter chapter how it is largely the wider context that has made the difference. One apparently important important issue is the spatial scale. The dynamic theory of island biogeography was originally developed to explain explain pat­ patterns at large spatial scales, whereas the metapopulation concept is associated with fragmentation of of our ordinary landscapes. landscapes. Though the difference is in per­ perception ception only, it it matters. matters. Metapopulation Metapopulation models have contributed important insights to conservation, and they have inspired eld studies focused on collecting key data inspired fi field data on demography and movement. Nonetheless, the temptation to apply the metapopulation approach approach blindly to systems for for which there is no supporting evidence evidence can be counterpro­ counterproductive. Metapopulation Metapopulation maintenance maintenance may be crucial to a limited range of of species, probably dominated by those those characteristic characteristic of successional successional habitats. The The role of of metapopulation metapopulation dynamics in forestalling genetic deterioration is particularly particularly un­ unverified. verified.

II

Empirical Evidence Evidence for Empiricol Metopopulotion Metapopulation Dynomics Dynamics Susan Susan Harrison Harrison

Andrew Andrew D. Taylor Taylor

I. INTRODUCTION INTRODUCTION Underlying nements and elaborations metapopulation theory Underlying the many refi refinements elaborations of of metapopulation is the fundamental depends on their fundamental idea that the persistence of of species species depends their existence existence as sets of migration. of local populations, populations, largely independent independent yet interconnected interconnected by migration. Population Population structure structure at this large spatial scale is thought thought to alleviate the risks of of widespread widespread extinction extinction that that arise arise from from unpredictable unpredictable physical environments environments and from strong interactions interactions among among species. This concept concept has long attracted attracted many ecologists, ecologists, but more more for its plausibility plausibility than because because of of any compelling compelling empirical empirical evidence. evidence. Support Support for for metapopulation metapopulation theory theory has mostly consisted of of anecdotal anecdotal accounts uctuations, combined accounts of of local extinctions extinctions or asynchronous asynchronous population population fl fluctuations, combined with much much theoretical theoretical evidence evidence that that metapopulation metapopulation effects effects could occur. occur. Recently, however, however, as interest interest in metapopulation metapopulation dynamics dynamics and its conservation conservation applications applications has grown, grown, the number number of of more more substantial substantial studies studies has steadily increased. increased. Here we review review the current current body of of empirical empirical evidence evidence and ask whether whether and and how it supports brief review supports metapopulation metapopulation theory. We We begin with a brief review of of the theory and its origins, origins, to lay the groundwork for for specifi specificc criteria by which which to evaluate evaluate the evidence. In this review, we highlight differences differences between between metapopulation metapopulation theory theory for for single and multiple multiple species, species, which which will lead to somewhat somewhat different different criteria in the two cases. We We leave aside the genetic genetic and evolutionary evolutionary aspects aspects of Metapopu/alion g\! Metapopulation Bi% Biology

Copyright reproduction in any fonn Copyright © 9 1997 1997 by Academic Press. Press, Inc. All rights rights of of reproduction form reserved. reserved.

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Susan and Andrew Susan Harrison Harrison and Andrew D. D. Taylor Taylor

metapopulation dynamics, which have received comparatively little empirical work ((but but see Olivieri et a!., 1 990; Olivieri and Gouyon, this volume; McCauley, al., 1990; 11991; 99 1 ; Harrison and Hastings, 11996; 996; Barton Barton and Whitlock, this volume, for for re­ reviews). Single-species metapopulation theory arose largely from early observations of species in patchy and unpredictable unpredictable environments. The archetypal "shifting mosaic" or "blinking lights" species were insects whose populations populations were small and were prone prone to extinction extinction either either because of cli­ clior insular, fluctuated widely, and matic events or because Andrewartha and because their habitat habitat was transient (e.g., Andrewartha and Birch, 11954; 954; Ehrlich 1 972). Recent Ehrlich and Birch, 1967; Ehrlich Ehrlich et et al. at.,, 1972). Recent examples in the same Menges, 11990), 990), amphibians in small ponds vein include herbs on riverbanks ((Menges, (Gill, 11978a; 978a; Sjogren, 99 1 ; Sjogren 1 994), snails on rocky outcrops Sj6gren, 11991; Sj6gren Gulve, 1994), (Spight, 1974), 1 974), insects on weedy plants (van der Meijden, 1 979a; van der Meijden,1979a; der Meijden Meijden and van der Veen-van vulner­ Veen-van Wijk, this volume), and many cases of butterflies vulnerable to bad weather 979; Harrison et et al. 1 988; weather or habitat change (Shapiro, 11979; al.,, 1988; 994; Hanski Thomas and Harrison, 11992; 992; Thomas and Jones, 1993; 1 993; Hanski et et al. al.,, 11994; and Kuussaari, 995; Hanski, this volume; Thomas Kuussaari, 11995; Thomas and Hanski, this volume). Single-species metapopulation models, beginning 1 970), dem­ beginning with Levins ((1970), demonstrate that that such sets of transient demes may persist through a balance between 1 994; local extinction and recolonization (reviewed by Hastings and Harrison, 1994; Hanski, this volume). metapopula­ volume). Here we denote as "classical" "classical" single-species metapopulations sets of local populations that are all subject to extinction and persist at the metapopulation metapopulation level through through recolonization (Fig. 1l a). A very basic property of

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Different types of cir­ of metapopulation. Filled circles, occupied habitat patches; empty circles, vacant habitat patches; dotted lines, boundaries boundaries of of local populations; arrows, dispersal. (a) Classic (Levins); (b) mainlandisland; (c) patchy inter­ mainland-island; patchy population; population; (d) nonequilibrium nonequilibrium metapopulation; (e) intermediate case combining features of of (a), (b), (c), and (d).

22

Empirical Evidence Evidence for Metapopulation Empirical MetapopulationDynamics Dynamics

29

classical metapopulations metapopulations is that persistence requires requires an adequate rate of of migration among patches. Probabilities of of metapopulation metapopulation persistence also increase with the number of of habitat patches and local populations. populations. Besides resonating resonating with ecolo­ ecologists gists'' interpretations interpretations of of many natural systems, this verbal verbal and mathematical model is increasingly seen as relevant to how species persist, or fail to do so, in landland­ scapes recently fragmented by humans (Opdam, 11990; 990; Fahrig 994; Fahrig and Merriam, 11994; Harrison, 994b). Harrison, I1994b). Theory on the the metapopulation metapopulation dynamics of of multiple interacting species arose not so much from from natural history as from from mathematical and laboratory studies showing the instability of predatory predatory or competitive interactions interactions in simple envi­ environments Nicholson and Bailey, 1935; Gause, 11935; 935; Huffaker, 1 958). What ronments ((Nicholson Huffaker, 1958). What we may now all the "classical" multispecies model was fi rst demonstrated Huf­ first demonstrated in Huf' s ((1958) faker 1 958) mite experiments, showing undergo faker's showing that a predator and its prey undergo oscillations and crashes within patches patches of of habitat, yet coexist stably in a universe of of interconnected interconnected patches. Mathematical models building building on the same extinction­ extinctionand-colonization and-colonization format developed developed for for single species, as well as models of of other other types, have explored force in explored many aspects aspects of of spatial spatial subdivision as a stabilizing force both predatory and competitive interactions Harrison, interactions (reviewed by Hastings Hastings and Harrison, 11994; 994; Nee Nee et et at. al.,, this this volume). volume). Metapopulation Metapopulation theories for single single and and multiple multiple species thus address address related issues and are expressed in similar models, yet arose from different different concerns and arrive at partly confl icting answers. In single-species theory, the problem is the conflicting patchiness of habitats and the harshness harshness of of the abiotic environment, and the so­ solution is migration migration and recolonization. recolonization. Multispecies theory theory addresses addresses the the problem problem of intrinsically unstable interactions and identifi identifies subdivision as a soluof es spatial subdivision solu­ tion. Therefore, Therefore, migration among among patches patches always promotes promotes persistence in models models of metapopulations (though models that of classical single-species metapopulations (though less so in models that include the effects of 1 993; Olivieri of emigration on local populations; Hanski and Zhang, Zhang, 1993; and and Gouyon, Gouyon, this volume), but too too much much migration leads to instability in multispe­ multispecies meta populations. metapopulations. We note note that that the above above difference difference is not really due to the the number number of of species involved, but rather rather to the assumed causes of of local instability or extinction. If local local dynamics dynamics are are intrinsically unstable, high rates of of migration may destabilize metapopulation (Allen et et at., al., 1993). if multispecies a single-species metapopulation 1 993). Conversely, if systems are are subject subject to frequent frequent local extinctions from external causes, subdivision may possibly lose its stabilizing effect, an issue that that deserves deserves more more investigation. We may now now identify criteria for for jUdging judging the empirical evidence on meta­ metapopulations. rst whether whether all local populations populations populations. For single-species studies, we ask fi first are prone prone to local extinction and, second, whether whether persistence at the metapopu­ metapopurequires recolonization. first, lation level requires recolonization. For multispecies mUltispecies systems, we ask, fi rst, whether whether strong interactions interactions between between either competitors competitors or predators predators and prey cause local extinctions or popUlation population oscillations oscillations and, second, second, whether subdivi­ subdivipersistence or the temporal stability of of the system as a whole. sion increases the persistence Metapopulations ned more have just done, Metapopulations may be defi defined more broadly than than we have done, to include include any systems in which popUlations populations are are subdivided subdivided but exchange exchange some

30

Susan Susan Harrison Harrisonand and Andrew Andrew D. D. Taylor Taylor

migrants. In fact, since we find find few few systems that that conform well to the classical classical broader models, we we return return under under Discussion Discussion to to consider consider the the implications implications of of aa broader view. However, However, like Hanski (this volume), we take the classical classical models as a point of of departure, departure, since their their assumptions assumptions are are implicit in most cases cases in which the term term is used, including many of the more elaborate metapopulation models. Moreover, is used, including many of the more elaborate metapopulation models. Moreover, classical models yield the classical models the strongest strongest predictions predictions about about metapopulation metapopulation dynamics; in other other types of of metapopulation, metapopulation, as we will show, the causes causes of of persistence persistence or coexistence coexistence lie lie more more at at the the local level. level. Finally, Finally, we note note some some important practical practical reasons reasons for giving giving careful scrutiny to to metapopulation metapopulation ideas. ideas. In In conservation conservation biology, the the metapopulation metapopulation model model is sometimes used to support support the need for for numerous numerous reserves, corridors, or a land­ landscape-level How­ scape-level approach, approach, goals goals with with which which few few conservationists would would argue. argue. However, in in other other cases cases this this model model is is used more controversially, controversially, to to justify justify strategies strategies that would preserve only a handful handful of of well-spaced fragments fragments of of a habitat that is presently 993; Harrison, 994b; Doak and Mills, presently continuous continuous (see (see Harrison Harrison et et al al., 11993; Harrison, 11994b; Doak and 11994; 994; Noon 996; Gutierrez 1 996). Noon and and McKelvey, McKelvey, 11996; Gutierrez and and Harrison, Harrison, 1996). ..

II. SINGLE-SPECIES SINGLE-SPECIESMETAPOPULATIONS METAPOPULATIONS In reviewing empirical studies, we examine each each of of the critical assumptions assumptions of rst identifying of classical classical metapopulation models in tum, turn, fi first identifying studies that that appear appear not to meet them and then proceeding toward studies that appear appear to exemplify most or all of of them. Our purpose is not to criticize individual studies, studies, nor nor to impose categories categories for their own sake, but to ask whether available evidence sug­ suggests any systematic systematic pattern.

A. Are All Local Local Populations Subject to Frequent Populations Subject Frequent Extinction? Extinction? 1. Definition Definition and and Causes Causes of of Local Local Extinction Extinction

Since populations show spatial spatial structure at a hierarchy of of scales scales (e.g., Amar­ Amarasekare, 1 994), the definitions definitions of asekare, 1994), of local populations and hence hence local extinction are usually usually partly partly arbitrary. arbitrary. However, However, as as aa minimal minimal criterion, criterion, local local extinction may be be defi ned as the extirpation of ciently closed im­ defined of any population segment segment suffi sufficiently closed to immigration migration that, once extinct, typically remains remains so for for several generations generations or more. This This serves to exclude sUbpopulations subpopulations so tightly connected connected to others others that that their their "extinction" is caused caused more by the movement of of organisms organisms than than by their their mortality (to see why this is an important distinction, distinction, imagine birds in an orchard, orchard, under­ undergoing "local extinction" every time they fl y out of fly of a tree). In the much-used scheme 1 98 1 ), local extinction has scheme devised by Shaffer Shaffer ((1981), has four four general general causes. One of of these, demographic demographic stochasticity, is expected expected to affect affect only popUlations populations below a threshold size, and another, loss of of genetic variation, acts

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Empirical Evidence for Metapopulotion EmpiricalEvidence Metapopulation Dynamics Dynamics

31

comparatively finish off population comparatively slowly. These These factors factors may help help to to finish off a declining declining population or or impede impede the establishment establishment of of new new ones, ones, but but are are unlikely to be ultimate ultimate causes causes of (including "catastro­ of local extinctions. extinctions. In contrast, contrast, environmental environmental stochasticity stochasticity (including "catastrophes") and and deterministic deterministic threats threats (e.g., loss of of habitat) may extirpate extirpate popUlations populations phes") habitat) may of a wide wide range range of of sizes and and thus are the most causes of of natural natural of thus are most likely ultimate ultimate causes rms ((Leigh, Leigh, 11981; 98 1 ; Karr, local extinctions, extinctions, as a variety of of empirical empirical evidence evidence confi confirms Karr, 11982; 982; Pimm et 988; Schoener, 983; C. D. Thomas 1 992; Thomas et al. al.,, 11988; Schoener, 11983; Thomas et et al. al.,, 1992; Thomas and and Hanski, this volume). volume). Environmental Environmental stochasticity stochasticity often often operates operates at a regional regional scale; for for example, example, weather synchrony over weather causes causes insect insect populations populations to fluctuate fluctuate in synchrony over broad broad geographic geographic areas Hanski and Woiwod, 1 993), and freeze may eliminate areas ((Hanski Woiwod, 1993), and a single drought drought or or freeze eliminate 972, 1980). 1 980). Such "re­ multiple conspecifi conspecificc butterfly populations populations (Ehrlich (Ehrlich et et al. al.,, 11972, "remetapopu­ gional stochasticity" stochasticity" reduces the likelihood likelihood of of persistence persistence for for classical classical metapopulations ((Hanski, Hanski, 11991). 99 1 ). In tum, importance of turn, it increases increases the potential potential importance of other other resistant life stages. mechanisms that enable enable persistence, persistence, such such as refuge refuge habitats habitats or or resistant Price 1 989) concluded undergoes Price and and Endo Endo ((1989) concluded that that because because Stephens Stephens'' kangaroo kangaroo rat rat undergoes extreme regionwide population fluctuations in response regionwide population response to weather, weather, a single large reserve is much preferable preferable to a proposed proposed design design of of multiple multiple small reserves reserves con­ connected nected by corridors. corridors. suc­ Deterministic causes of of local extinction include natural natural disturbance disturbance and succession cession and human human destruction destruction of of natural natural habitats. These These may may lead to classical metapopulation metapopulation dynamics, dynamics, but do do not always do do so, for for several reasons. reasons. Species Species adapted popula­ adapted to successional successional habitats habitats may be such such good good dispersers dispersers that that their their populations tions are are not not very subdivided. Species subjected subjected to longer-term longer-term habitat habitat change change shift their their spatial distributions distributions over over time without without ever approaching a dynamic dynamic may shift ever approaching balance Habitat fragmentation fragmentation may balance between between extinction extinction and and recolonization. recolonization. Habitat may pro­ produce populations or duce patches patches that that are too small to support support populations or too too isolated isolated to interact other patches. patches. with other 2. Some Some Populations Populations Are Are Highly Persistent Persistent

Most Most studies studies of of natural natural local extinctions extinctions have have taken taken place place on on small islands islands near 1 98 1 ; Peltonen Peltonen and 1 99 1 ; near the shore shore of of a lake or ocean ocean (e.g., Pokki, 1981; and Hanski, 1991; reviews 983; Diamond, 984). Local reviews in Schoener, Schoener, 11983; Diamond, 11984). Local extinctions extinctions affect affect the small (island) (island) populations, populations, but but the the system persists persists for for essentially the the same same length length of of time as do its larger Fig. 1l b). Many larger and and more more persistent persistent (mainland) (mainland) populations populations ((Fig. Many metapopulations metapopulations have have an essentially similar, similar, mainland mainland and and island island structure, structure, owing owing to high high variation variation in the the sizes of of habitat habitat patches patches or or populations. populations. Examples Examples include include metapopulations metapopulations of of spiders spiders on Bahamanian Bahamanian islands islands (Schoener (Schoener and and Spiller, Spiller, 11987a,b; 987a,b; Spiller 990), checkerspot patches of Spiller and and Schoener, Schoener, 11990), checkerspot butterflies butterflies on patches of ser­ serHarrison et 988), and pentine soil ((Harrison et al. al.,, 11988), and many others others (reviewed (reviewed by Schoener, Schoener, Harrison, 11991). For a system to have have mainlandmainland-island there 11991; 99 1 ; Harrison, 99 1 ). For island dynamics, there need not be a single single mainland of of extreme size. Substantial Substantial variance in patch patch or population pop­ population size means means that local extinctions extinctions will tend to strike the smallest populations, which are the ones with the least impact on metapopulation persistence. which are ones with impact on metapopulation persistence.

32 32

Susan Susan Harrison Harrisonand and Andrew Andrew O. D. Taylor Taylor

Heterogeneity in habitat quality, rather rather than patch or population size, may produce a similar effect. A recently popular idea is that dispersal from "source" "source" populations in high-quality high-quality habitat habitat may permit permit "sink" "sink" populations to exist in inferior habitat 988; Pulliam and Danielson, 1991). 1 99 1 ). Unlike island pop­ habitat (Pulliam, (Pulliam, 11988; populations, which are are merely small, sinks cannot cannot support support positive population population growth because of their poor quality. This idea remains largely untested, but several insect studies provide suggestive examples, with the sinks ranging from marginal marginal hab­ habitats that are occupied only during rare 1 979; Mur­ rare favorable years (e.g., Shapiro, 1979; Murphy and White, 11984), 984), to areas areas in which populations flourish most of of the time but cannot survive catastrophes (e.g., Strong et al. , 11990; 990; Singer et al., 11994). 994). et al., et al., 3. 3. Populations Populations Are Are Not Not Subdivided Subdivided Enough Enough to Permit Permit True True Local Extinction Extinction Local

extinction to occur, popUlations populations on separate patches must be rea­ reaFor local extinction sonably isolated from one another, with most recruitment recruitment coming from within the patch patch rather rather than than from immigration. At the opposite extreme extreme are are systems in which progeny from all patches patches are completely mixed and and reassorted among patches patches in each generation. Here the term term "patchy "patchy popUlation" population" is used for for systems toward the latter end of the continuum (Fig. l c). Sharp Sharp distinctions distinctions are are difficult in practice, practice, but if the average average individual inhabits more than a single patch in its lifetime, the patches clearly do not support separate populations. Local "extinc"extinc­ tions," presences presences followed by absences, may simply be the result of of individuals individuals'' foraging behavior or responses to conspecifics (e.g., the birds in an orchard). Importantly, unlike a metapopulation, the persistence of a patchy population is not not highly sensitive to the distances or rates of of movement among patches. patches. Invertebrates Invertebrates that specialize on fallen fruit, rotting logs, dung, carrion, or water-filled tree holes are sometimes regarded as forming classical metapopula­ metapopulations, colonizing and becoming extinct on their transient resource patches. How­ However, such species are typically highly mobile; each patch patch supports only one generation of the insect, and adults adults oviposit on numerous numerous patches in their their lifetimes (e.g., Kitching, 11971; 97 1 ; Kaitala, 11987; 987; Hanski, 1987). 1 987). Although weedy host plants are a slightly more permanent permanent habitat habitat than dung or carrion, the specialist insects feeding on milkweed (Solbreck, 1991; 1 99 1 ; Solbreck and Sillen-Tullberg, 990) and Sillen-Tullberg, 11990) 1 995) appeared ragwort ((Harrison Harrison et et al. al.,, 1995) appeared to disperse so well that their populations were effectively unsubdivided across large arrays of of patches (but see below and van der Meijden Meijden and van der Veen-van Wijk, this volume). Of Of course, at some larger scale (e.g., among different fields or forests) they may possibly show clas­ classical or nonclassical metapopulation structure. structure. Migration has long been been considered an important adaptation to environments that vary in space and time (e.g., den Boer, 11968; 968; Southwood, 1977). 1 977). Sessile marine invertebrates invertebrates with planktonic larvae show perhaps highest highest migration of of any organisms, relative relative to the scale of of the patches patches on which recruitment and growth growth occur, and they appear to persist longer in evolutionary time than than com­ comparable 99 1 ). Conversely, the parable taxa with nonplanktonic larvae (Jablonski, 11991). the evo-

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Empirical Evidence Empirical Evidencefor Metapopulation MetapopulationDynamics Dynamics

33 33

lution of of flightlessness flightlessness in insects insects is strongly linked linked to stable, stable, continuous continuous habitats (Wagner 992). Thus, it is perhaps to be expected that in many (Wagner and Liebherr, 11992). cases, species in patchy and risky environments will disperse too well to form classical classical metapopulations on patches of of their habitat.

B. Does Does Recolonization Recolonization Balance Balance local Local Extinction? Extinction? Migration Migration and colonization colonization in metapopulations metapopulations have been reviewed by Eben­ Ebenhard 1 99 1 ), Hansson ((1991), 1 99 1 ), and Ims and Yoccoz (this volume). In classical hard ((1991), models, there there is a threshold rate of migration for the metapopulation metapopulation to persist. Above this level, patch patch occupancy achieves a stable stable equilibrium, equilibrium, arising arising from the fact that that every local extinction extinction makes an empty habitat available for colonization, in strict analogy to a density-dependent birth rate. There There are several reasons why this this assumption assumption may may not not always always hold. hold. 1. Nonequilibrium Declining) Metapopulations Nonequilibrium ((Declining) Metapopulations

Rather Rather than than being part part of a steady-state process, local extinctions may occur occur in the course of a species species'' decline decline to regional extinction, extinction, with recolonization occuring infrequently or not at all ((Fig. Fig. Il d), typically as the species species'' habitat habitat is undergoing reduction and fragmentation. ex­ fragmentation. A natural natural example is the series of of extinctions of mammal populations caused by the isolation of of mountaintop habitats habitats during post-Pleistocene 97 1 ). Many more examples can post-Pleistocene climate change (Brown, 11971). be found among species in habitats fragmented by humans, such as salamanders (Welsh, 11990) 990) and woodpeckers (Stangel et 1 992) on remnant et at., al., 1992) remnant patches of old­ oldgrowth forest. Hanski (this volume) discusses nonequilibrium dynamics in a butbut­ terfly metapopulation. The conservation of species in fragmented habitats habitats is an important area for the application of metapopulation concepts. In some cases, however, remnant populations are so isolated that there is little potential to manage manage them as an interconnected Harrison, 11994b), 994b), while in others, creating corridors or interconnected network ((Harrison, a dispersal-friendly matrix may be feasible (e.g., Noon and McKelvey, 11996). 996). 2. Nonequilibrium Habitat-Tracking) Metapopulations Nonequilibrium ((Habitat-Tracking) Metapopulations

Local extinctions are not always stochastic stochastic as most metapopulation theory assumes, but rather may occur when disturbance, disturbance, succession, or long-term habitat habitat change cause the loss of tum, colonization may occur only of suitable habitats. In turn, when new patches of of habitat are created near existing populations. populations. For example, example, the spatial spatial distribution distribution of many butterflies butterflies appears to be sensitive to vegetation age and and height, which are governed by grazing and other transient disturbances disturbances (Thomas and Harrison, 1992; 1 992; Thomas and Jones, 11993; 993; Thomas Thomas and Hanski, this volume). Thomas ((1994c) 1 994c) argues that deterministic extinction may be the rule and stochastic extinction the exception exception in real metapopulations. The spatial dynamics created created by disturbance disturbance and succession are interesting in their own right and are a subject of importance for of key importance for the conservation of of

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SusanHarrison Harrisonand ond Andrew AndrewD.D. Taylor Taylor Susan

many species. However, local extinctions caused by habitat loss violate an im­ important premise of the classical model, namely that extinctions make habitats metapopulation-level equilibrium pre­ preavailable for recolonization. The stable metapopulation-level from the inverse relationship between patch dicted by the classical model arises from density-dependent regulation of occupancy and patch availability, which creates density-dependent patch occupancy. In contrast, when patches are created created and destroyed destroyed by extrinsic species'' abundance abundance and distribution distribution will forces, no such regulation occurs. The species simply track the availability of habitat and and will remain roughly constant constant only if the rates of habitat 994c). habitat loss and renewal happen happen to be roughly equal (Thomas, (Thomas, 11994c).

C. C. Classical ClassicalMetapopulations, Intermediate Intermediate Cases, Cases, and Other Possibilities Possibilities Rana lessonae lessonae in ponds ponds along the Baltic coast of of Sweden The pool frog Rana (Sj6gren, 11991; Sj6gren Gulve, 11994) and the butterfly Melitaea Melitaea cinxia ((Hanski Hanski (Sjogren, 99 1 ; Sjogren 994) and al.,, 11994, and this volume) volume) on granite outcrops outcrops in southwest southwest Finland, Finland, form form et al. 994, and metapopulations metapopulations in which which all populations populations are susceptible susceptible to relatively frequent frequent extinction, migration migration among among popUlations populations is limited limited (i.e., most recruitment recruitment is lolo­ well­ cal), and extinctions extinctions create create vacant vacant habitats habitats which which are recolonized. recolonized. These These two two wellstudied systems appear appear to conform conform reasonably closely to the classical concept concept of of studied metapopulations in an extinction extinction-colonization balance. metapopulations -colonization balance. other systems resemble resemble classical metapopulations metapopulations in certain certain ways, for Many other example having having patchy distributions distributions with no obvious obvious "mainland" "mainland" patches patches ((Hanski example Hanski populations that that do not appear appear to be self­ selfand Kuussaari, 11995), 995), or having local populations sustaining (Stacey and Taper, 11992, volume). However, However, based based on the fore­ foresustaining 992, this volume). going evidence, we would argue that only only after after much detailed study can any going evidence, natural system be classical metapopulation. be described described as a classical metapopulation. 1. Mixed Structures Mixed Structures

Many of species patchy habitats habitats reveal Many studies studies of species distributions distributions in patchy reveal that that patches patciles are to other are more more likely to be occupied occupied the nearer nearer they are other occupied occupied patches patches (Brown and Kodric-Brown, Laan and and Verboom, (Brown and Kodric-Brown, 1977; 1 977; Fritz, 1979; 1 979; Opdam, Opdam, 1990; 1 990; Laan Verboom, 1990; 1 990; Lawton Lawton and and Woodroffe, Woodroffe, 1991; 1 99 1 ; C. D. D. Thomas Thomas et et al., at., 1992). 1 992). This This suggests suggests the of all different the possibility possibility that that many many real metapopulations metapopulations combine combine features features of different kinds of from clustered of metapopulation metapopulation structure, along gradients gradients from clustered central central patches patches to isolated ones (Fig. lI e). Central Central patches are united isolated peripheral peripheral ones patches are united by dispersal dispersal into into a single population, population, slightly more more isolated isolated ones ones undergo undergo extinction extinction and and recolonrecolon­ ization, ization, and and still more more isolated isolated patches patches are are usually vacant. vacant. other cases, cases, the the metapopulation metapopulation structure structure of of aa species species may may vary among among In other regions, regions, because because of of differences differences in the the configuration configuration of of habitat. habitat. Nine Nine metapopumetapopu­ lations lations of of the the silver-studded silver-studded blue blue butterfly butterfly (Plebejus (Plebejus argus) argus) in Wales Wales show show a continuum from nearly continuum from nearly equal-sized equal-sized patches patches to to aa mainland-island mainland -island configuration configuration (Thomas edithaa forms (Thomas and and Harrison, Harrison, 1992). 1 992). The The butterfly butterfly Euphydryas Euphydryas edith forms a mainmain­ land - island metapopulation metapopulation in coastal coastal California, California, but but shows shows a mixture mixture of of classical classical land-island and patchy patchy population population features et al., al. , 1988; 1 988; and features in montane montane California California (Harrison ( Harrison et Singer on patches Singer and and Thomas, Thomas, 1996). 1 996). Insects Insects on patches of of ragwort ragwort show show little little population popUlation

Empirical Evidence Evidence for Metapopulation Dynamics Dynamics 22 Empirical

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subdivision in in British British grasslands grasslands (Harrison ( Harrison et et al., al., 1995), 1 995), but but the the effects effects of of subsub­ subdivision division are are significant significant in in Dutch Dutch dunes dunes (van (van der der Meijden, Meijden, 1979; 1 979; van van der der Meijden Meijden division and van van der der Veen-van Veen-van Wijk, Wijk, this this volume). volume). and The northern northern spotted spotted owl owl (Strix (Strix occidentalis occidentalis caurina) caurina) occupies occupies aa once-cononce-con­ The tinuous tinuous but but now now coarsely coarsely fragmented fragmented forest forest habitat, habitat, while while the the Californian Californian subsub­ (S. o. o. occidentalis) occidentalis) lives (in part) part) in still-continuous still-continuous but but selectively logged logged species (S. species forests, and and the the Mexican Mexican subspecies subspecies (S. (S. o. o. lucida) lucida) inhabits inhabits insular insular mountaintops. mountaintops. forests, This natural natural and and unnatural unnatural variation variation in in habitat habitat structure, and presumed presumed metapopumetapopu­ This structure, and lation structure, feature of of conservation conservation strategies strategies for for the the spotted spotted owl owl lation structure, is a central central feature ( Noon and and McKelvey, McKelvey, 1996; 1 996; Gutierrez and Harrison, Harrison, 1996). 1 996). (Noon Gutierrez and 2. Metapopulations Metapopulations with with Little Little Turnover Turnover 2.

If local local populations populations fluctuate fluctuate fairly fairly independently independently of of one one another, another, but but exex­ If change low to moderate numbers of immigrants, metapopulation structure may change low to moderate numbers of immigrants, metapopulation structure may have an important important stabilizing stabilizing effect effect at the the regional level even even without without population population have regional level turnover. We We know know of of no no good good examples of this possibility, possibility, but but it could could be be tested tested turnover. examples of comparing the the magnitude magnitude of fluctuations in conspecific conspecific populations popUlations varying by comparing of fluctuations their degree degree of of isolation. isolation. in their Dynamics 3. "Local" 3. "Local" Spatial Spatial Dynamics

A growing number of studies suggest even in relatively concon­ A growing number of empirical empirical studies suggest that that even tinuous habitat, may be strongly tinuous habitat, the dynamics dynamics and and persistence persistence of of popUlations populations may affected small-scale habitat habitat heterogeneity, heterogeneity, localized interactions, interactions, and limited affected by small-scale and limited et al. 1 988; Harrison, Harrison, 1994a; 1 994a; Amarasekare, Amarasekare, 1994). 1 994). This This migration (e.g., Weiss Weiss et migration al.,, 1988; important class class of one that conceptual is an important of phenomena, phenomena, but one that lies outside outside the conceptual domain domain of of metapopulation metapopulation dynamics.

III. MULTISPECIES MULTISPECIESMETAPOPULATIONS METAPOPULATIONS We now now review empirical studies studies in which which it has been been proposed We proposed that predators predators competitors coexist coexist through through multispecies multispecies metapopulation metapopulation dynamics and prey or competitors earlier reviews by Bengtsson, 11991, "clas(see earlier 99 1 , and Taylor, 11991). 99 1 ). Here, the two "clas­ sical" conditions conditions we examine examine are that that the interspecific interspecific interaction interaction leads to local extinction extinction or instability and that that both both (or all) species have have something something like a clas­ classical metapopulation metapopulation structure at similar spatial scales, leading to greater stability or persistence at the regional regional level than than within each local patch. Once again, we begin by identifying ways in which these conditions conditions may not be met in some some natural systems.

A. Is the Interaction Locally Locally Unstable? Unstable? 1. All Local Populations Populations Are Stable or Persistent Persistent

Several recent studies have tested the metapopulation metapopulation explanation explanation for for coex­ coexistence by asking whether whether local populations populations of of predators and prey are are destabilized destabilized

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Susan and Andrew Susan Harrison Harrison and Andrew D. D. Taylor Taylor

by being isolated. Murdoch 1 996) found Murdoch et al. ((1996) found that populations populations of of the red scale Aonidella uctuate more more on Aonidella aurantii aurantii and and its parasitoid parasitoid Aphytis Aphytis melinus melinus did not fl fluctuate caged than on uncaged uncaged citrus trees. Similarly, C. J. Briggs (unpublished (unpublished manu­ manuscript) did not fi nd a signifi cant increase temporal variability populations find significant increase in the temporal variability of of populations of of the midge midge Rhopalomyia Rhopalomyia californica californica or its parasitoids parasitoids on caged versus uncaged uncaged coyote bushes (Baccharis (Baccharis pilularis). pilularis). However, the latter latter experiments experiments lasted only 3 --1100 insect generations, become generations, possibly too short for for the anticipated anticipated effects effects to become statistically signifi cant. significant. The interaction interaction between between prickly-pear cactus cactus (Opuntia (Opuntia spp.) and the moth moth Cactoblastis Cactoblastis cactorum, cactorum, which which was successfully successfully introduced introduced to control control the cactus cactus in Australia, Australia, has been described described as a classical case of of coexistence coexistence through through ex­ extinction Dodd, 11959; 959; A. J. Nicholson, tinction and and colonization colonization dynamics dynamics ((Dodd, Nicholson, as quoted quoted in Monro, 967). However, Monro, 11967). However, more more recent recent observations observations suggest that both both species species per­ perplants always survive sist locally and that the interaction interaction is stable because some plants attack Monro, 11967, 967, 1975; 1 975; Caughley, 11976; 976; Osmond Monro, attack by the moth moth ((Monro, Osmond and and Monro, 98 1 ). 1 98 1 ; Myers 1981; Myers et al., 11981). Local populations populations may survive survive strong predation predation or competition competition because of of a cryptic life stage. For example, early-successional early-successional plants may coexist coexist with su­ superior competitors by "recolonizing" perior competitors "recolonizing" newly disturbed disturbed sites from seed banks, rather than by dispersal. Resting stages appeared recolonization by appeared to explain the recolonization waterfl eas (Daphnia waterfleas (Daphnia spp.) of of cattle tanks from from which which they had been eliminated eliminated Murdoch et al. 1 984). Alternatively, prey by predatory bugs (Notonecta (Notonecta spp.) ((Murdoch al.,, 1984). populations may survive simply because predators predators leave a patch before before eliminat­ eliminating all prey; examples examples include include olive scales and their parasitoids parasitoids ((Huffaker ai., Huffaker et al., 1 986; Taylor, 11991) 99 1 ) and cottony cushion parasitoids 1986; cushion scale, scale, vedalia vedalia beetles, beetles, and and parasitoids 969). (Quezada, 11969). extinctions may may occur occur primarily for for reasons reasons other other than the inter­ interLocal extinctions specific interaction. Hanski and Ranta 1 983) and Bengtsson 1 989, 11993) 993) hyhy­ Ranta ((1983) Bengtsson ((1989, pothesized pothesized that three competing Daphnia Daphnia species in rock pools in the Baltic Sea coexisted cial pools, coexisted through through extinction extinction and and recolonization. recolonization. In studies studies with with artifi artificial pools, Bengtsson 1 989, 11993) 993) showed Bengtsson ((1989, showed that that extinction extinction rates rates were were higher higher in three-species three-species pools pools than than in two- or one-species one-species pools. However, However, species pairs and and even triplets could coexist coexist for for 44- 77 years even in very small pools. Bengtsson concluded concluded that that some apparent apparent extinctions were really pseudoextinctions pseudoextinctions caused by a cryptic rest­ resting stage, and that most natural natural extinctions were probably probably caused caused by predation, predation, low resource We note that if extinctions resource levels, salinity, or desiccation. We extinctions are caused caused by both both the the competitive competitive interaction interaction and and the extrinsic forces, forces, it creates creates the inter­ interesting possibility possibility that subdivision subdivision has both both positive positive and negative effects effects on sta­ stability. The parasitoids parasitoids Hyposoter Hyposoter horticola horticola and and Cotesia Cotesia melitaearum melitaearum parasitize The parasitize up to 90% of of the larvae of of the butterfl butterflyy Melitaea Melitaea cinxia, cinxia, and may contribute contribute to the observed Hanski et al., 11994; 994; Lei and Hanski, Hanski, observed local extinctions extinctions of of M. cinxia ((Hanski 11997), 997), but their importance importance relative relative to drought drought and and other other factors factors is not yet clear. Other parasitoid interaction include include spatial Other factors factors which which may stabilize stabilize this hosthost-parasitoid

22 Empirical Empirical Evidence Evidence for MetGpopulation Metapopulation Dynamics Dynamics

37 37

density dependence dependence in in the the mortality mortality caused caused by by aa generalist generalist hyperparasitoid hyperparasitoid (Lei ( Lei density and Hanski, 1997). 1 997). and Hanski, et al. al. (1994) ( 1 994) has has shown shown that that the the extinction extinction and and Recent work work by by Antonovics Antonovics et Recent alba) affects affects both both the the inin­ colonization of of populations populations of of white white campion campion (Silene alba) colonization (Ustilago violacea) and and the the distribution distribution of of the the cidence of of its anther anther smut smut disease disease (Ustilago cidence plant ' s disease-resistance disease-resistance genotypes genotypes among among populations. populations. However, However, there there is no no plant's evidence yet yet that that the the disease disease affects affects rates rates of of local local extinction extinction in the the plant. plant. evidence 2. Some Some Prey Prey Populations Populations Are Are Stable Stable or or Persistent Persistent ("Refuges") ("Refuges") 2.

analogy to to source-sink source - sink dynamics, dynamics, a prey prey or or inferior inferior competitor competitor In a close analogy may may persist persist because because it has has a particular particular type type of of habitat habitat in which which it escapes escapes its Balanus balanoides balanoides suffers suffers heavy heavy predator or or superior superior competitor. competitor. The The barnacle barnacle Balanus predator Urosalpinix cinerea cinerea in the the subtidal subtidal zone, zone, but but persists persists and and predation the snail snail Urosalpinix predation by the recruits in the the intertidal intertidal zone zone where where the the snail snail is absent absent (Katz, ( Katz, 1985). 1 985). European European recruits have a refuge refuge from predation in sprayed orchards orchards where where their their main main red mites have from predation predators are scarce Walde, 1991, 1 99 1 , 1994). 1 994). However, However, experiments experiments showed showed that that predators scarce ((Walde, refuges do do not explain the stability of interaction between between red red scale and and the the refuges of the interaction Aphytis melinus ( Murdoch et al. , 1 996). parasitoid parasitoid Aphytis (Murdoch al., 1996). In a slight modification modification of refuge pattern, pattern, interactions interactions may be stable stable in in of the the refuge may be Opheroptera some habitat types but not in others. For example, the winter moth some habitat types but not others. For example, the winter moth Opheroptera appears to coexist coexist stably with its parasitoids parasitoids in apple orchards, orchards, and and to brumata appears disperse from orchards orchards into into forests forests where where local extinctions extinctions are frequent (Murdoch (Murdoch disperse from are frequent 1 985; MacPhee MacPhee et al., 1988). 1 988). et al. al.,, 1985; Finally, patch effective refuges. patch size may may create create effective refuges. Lizards Lizards (Anolis spp.) concon­ tribute tribute to local extinctions extinctions of of spider spider popUlations, populations, but sufficiently sufficiently large large islands support (Schoener and Spiller, support stable popUlations populations of of both spiders spiders and lizards (Schoener Spiller, 11987a,b; 987a,b; Schoener, 99 1 ). Conversely, pool frogs frogs (Rana lessonae) persist Schoener, 11991). Conversely, pool persist better better ponds support pike (Esox lucius), which in small than in large ponds, since large ponds support pike major cause of of local extinctions of of the frog (Sjogren, (Sj6gren, 11991; Sj6gren Gulve, Gulve, are a major 99 1 ; Sjogren 11994). 994). 3. 3. Predator Predator Populations Populations Are Are Stable Stable (Generalists) (Generalists) Even Even if if a prey species species exists exists as a metapopulation, metapopulation, and its predator predator causes local extinctions extinctions or instability, the predator predator may persist persist stably if if it has alternate alternate prey. The predatory mite Typhlodromus frequently eliminates Typhlodromus pyri pyri frequently eliminates the European European red mite (Panonychus ulmi) from from individual apple trees, and migration among trees enhances enhances the persistence persistence of P. ulmi. Nonetheless, Nonetheless, T. pyri pyri is consistently abundant, abundant, since it can feed on pollen and the apple apple rust mite (Aculus schlectendali) as well as P. ulmi ((Walde, Walde, 11991, 99 1 , 11994; 994; Walde et al. 992). Similar examples al.,, 11992). examples include Daphnia and Notonecta ((Murdoch Murdoch et al., 11984), 984), the oak gall wasp wasp Xan­ Xantho teras politum and its parasitoids 98 1 ), and spiders thoteras parasitoids (Washburn (Washburn and Cornell, Cornell, 11981), and lizards (Schoener 987a,b; Spiller and Schoener, 990). It is (Schoener and Spiller, 11987a,b; Schoener, 11990). possible, possible, though though by no means means proven, that these systems function function as single-spe­ single-species metapopulations metapopulations for for the prey.

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Susan Harrison Harrisonand and Andrew Andrew D.D. Taylor Taylor Susan

B. B. Do Do Both Both (All) Species SpeciesShow Show Metapopulation Metapopulation Structures Structuresat Similar Similar Spatial Spatial Scales? Scales? Prey Is Subdivided Subdivided but Predator Predator Is Not Not 1. Prey Interacting species often differ in their mobility, with predators or parasitoids usually being better dispersers than their hosts or prey. This is clearly the case for goldenrod goldenrod aphids (Uroleucon nigrotuberculatum) nigrotuberculatum) and their ladybird beetle predator (Coccinella septempunctata) septempunctata) ((Kareiva, Kareiva, 11984, 984, 11987) 987) and may also be true predator for the red scale, olive scale, cottony cushion scale, gall midges, and their re­ respective parasitoids, parasitoids, discussed discussed above. In subdivided subdivided experimental populations populations of the intertidal snail Nucella Nucella ((= Thais) emarginata, emarginata, local extinctions extinctions were caused by predators predators (gulls, geese, and crabs) that are both mobile and generalists (Quinn et al., 11989). 989). If a predator predator is either very mobile or a generalist, generalist, it will be present present appear to on most prey patches most of the time, and subdivision would not appear for such a system to act as a single­ singleexplain coexistence. Again, it is possible for metapopulation for for the prey. species metapopulation =

None of of the the Species Species Is Subdivided Subdivided 2. None Mosquitos described as coexisting coexisting with their aquatic aquatic predators predators Mosquitos have been described through extinction extinction and recolonization, recolonization, but all individuals individuals disperse from from their natal through patch Murdoch et al. 985). A metapopulation patch and and oviposit oviposit on many patches patches ((Murdoch al.,, 11985). metapopulation explanation explanation for for coexistence coexistence has been been proposed proposed for for kangaroo kangaroo rats rats and smaller seed­ seedeating rodents 1 995), but these authors note that "the rodents by Valone and Brown Brown ((1995), "the responses observed observed largely represent represent habitat habitat selection selection by individual individual rodents" rodents" and and responses that typical persistence persistence times are on the order order of of a few few months, indicating that that months, indicating these dynamics dynamics take place within rather rather than among local populations. populations. Some suggests that cinnabar cinnabar moths (Tyria jacobaeae) may coSome evidence evidence suggests moths (Tyria jacobaeae) may co­ exist with distributed host (ragwort, Senecio and Senecio jacobaea), jacobaea), and with their their patchily distributed host plant plant (ragwort, with certain of their parasitoids parasitoids and competitors, through with certain of their and competitors, through classical classical multimulti­ species metapopulation metapopulation dynamics dynamics (van der Meijden species der Meijden, Meijden, 1979a; 1 979a; van van der der Meijden and and van van der der Veen-van Veen-van Wijk, Wijk, this this volume; Crawley Crawley and and Pattrasudhi, Pattrasudhi, 1988; 1 988; McEvoy al.,, 11993). in British McEvoy et ai. 993). However, However, one one test test of of this hypothesis hypothesis in British grasslands grasslands found found that that the moth moth disperses disperses so well, relative relative to the the distances distances between between ragwort ragwort patches, patches, as to preclude a metapopulation metapopulation explanation explanation for for coexistence coexistence (Harrison ( Harrison al.,, 1995). et al. 1 995).

C. Classical Classical Multispecies Multispecies Metapopulation Metapopulation Dynamics Dynamics Interactions between herbivorous Interactions between herbivorous and and predatory predatory mites mites in greenhouses greenhouses present present an an interesting interesting mixture mixture of of patchy-population patchy-population and and metapopulation metapopulation features features (e.g. Nachman, and Laane, et al., al., 1991; 1 99 1 ; van van de de Nachman, 1988, 1 988, 1991; 1 99 1 ; Sabelis Sabelis and Laane, 1986; 1 986; Sabelis Sabelis et Klashorst Klashorst et et al., al., 1992). 1 992). Metapopulation Metapopulation dynamics dynamics are are suggested suggested by by the the facts facts that mites between adjacent plants, and that mites have have very very limited limited mobility mobility between adjacent plants, and suitable suitable plants plants are are frequently frequently unoccupied. unoccupied. However, However, movement movement is more more frequent frequent and and more more directed directed than than most metapopulation metapopulation models models assume: assume: individuals individuals may may ococ-

22 Empirical Empirical Evidence Evidence for Metapopulation Metapopulation Dynamics Dynamics

39 39

cupy many many plants plants in in their their lifetimes, lifetimes, emigration emigration by by both both predators predators and and prey prey is is cupy density-dependent, and and predator predator dispersal dispersal may may respond respond to to chemical chemical signals signals by by density-dependent, the prey. prey. To To date date there there has has been been no no direct, direct, conclusive conclusive test test of of the the importance importance the of metapopulation metapopulation structure structure in in stabilizing stabilizing mite mite and and plant plant systems, systems, e.g., e.g., by by comcom­ of paring the the persistence persistence of of predators predators and and prey prey on on closely closely versus versus widely widely spaced spaced paring arrays of of plants. plants. arrays Conclusive experimental tests of of classical classical multispecies multispecies metapopulation metapopulation dydy­ Conclusive experimental tests namics are are exceptionally exceptionally difficult, difficult, and and few few have have been been done. done. (However, ( However, see see HolHol­ namics yoak and and Lawler, Lawler, 1996, 1 996, for for an an excellent excellent recent recent example.) example.) In In certain certain studies studies menmen­ yoak tioned above, above, such such as as that that of of Baccharis-feeding insects, insects, there there is is aa tantalizing tantalizing tioned suggestion of of metapopulation metapopulation effects, effects, but but strong strong tests tests are are precluded precluded by by too too few few suggestion patches and/or and/or generations. generations. In In others, others, such such as as that that of of Melitaea cinxia and and its its patches parasitoids, suggestive suggestive patterns patterns are beginning to to emerge. emerge. Finally, Finally, in in such such studies studies parasitoids, are beginning as that of rock rock pool pool Daphnia, some some of of the the conditions for metapopulation coex­ as that of conditions for metapopulation coexistence are met, but but it is difficult difficult to assess their their importance importance relative relative to to other factors, istence are met, to assess other factors, such as as dormant life stages stages and and abiotic causes of of extinction. such dormant life abiotic causes extinction.

IV. DISCUSSION IV. DISCUSSION Large-scale -metapopulation structure Large-scale spatial popUlation population structure structuremmetapopulation structure in the broad natural sys­ broad sense s e n s e-is m i s clearly important in a large number and and variety of of natural systems. Real populations populations often often behave behave very differently differently than than they they would would if if they they were were unsubdivided, habitats unsubdivided, and and both both the natural natural and and the human-caused human-caused discontinuity discontinuity of of habitats have large effects metapopulation approach effects on on how how populations populations function. function. Thus, a metapopulation approach is understanding and is essential essential to to understanding and managing managing many many natural natural phenomena. Our Our aim aim here is not to discount such an approach, approach, but rather rather to use empirical evidence to refine and clarify our our notions notions of of how how real metapopulations metapopulations work. The results cast some doubt species metapopu­ doubt on the classical models models of of both both single- and multi multispecies metapopulations. lations. We find that natural metapopulations Fig. 11), ), metapopulations have a variety variety of structures ((Fig. with implications for for persistence and coexistence coexistence that are correspondingly correspondingly varied. These different structures are are of of course not discrete entities, but rather lie along continuua in terms of patch structure and migration rates ((Fig. Fig. 2). Our review illustrates that when natural systems deviate substantially from the classical, ex­ extinction-and-colonization structure, their essential behavior behavior changes considerably as as well; well; in in all all cases, cases, persistence persistence and/or and/or coexistence coexistence become become more more dependent dependent on on local (within-population) (within-population) processes and and less so on on metapopulation ones. It is there­ therefore fore crucial crucial to to avoid avoid labeling labeling aa system system as as aa metapopulation metapopulation under under aa broad broad defi­ deftnition - e.g., because habitat is patchy, nitionme.g., patchy, some some local extinctions occur, occur, or or popu­ populations and then lations in in different different areas areas fluctuate fluctuate out out of of synchronysynchronymand then applying applying to to itit conclusions that nition. that follow follow from from aa narrower narrower (classical) (classical) defi definition. We We also also conclude conclude that that classical metapopulations metapopulations form form aa minority, minority, even even among among the the modest modest number number of of systems systems that that have have been been well well studied studied in in metapopumetapopu-

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SusanHarrison Harrisonand and Andrew AndrewD.D. Taylor Taylor Susan

Variance Variance patchsize size inin patch (or other other (or determinant determinant of population population of persistence) persistence)

MAINLAND-ISLAND MAINLAND-ISLAND ",_ .. - .. .. ..

NON­ NONEQUILIBRIUM EQUILIBRIUM

s , , , s

*, , , .

:'[ "CLASSIC" "CLASSIC" \", (LEVINS) :: �I (LEVINS) \ I

\�

9

.. ..

" ... '

s

"

PATCHY PATCHY POPULATIONS POPULATIONS

Dispersal Dispersal distance distance (relative (relative to to interpatch interpatch distances) distances)

FIGURE22 Relationships among among different different types of metapopulation. FIGURE

lation terms. tenns. We fi nd only a few find few examples of single species existing in a balance balance between the extinction and colonization colonization of populations populations and almost none none of of sys­ systems in which multiple species coexist through through tightly coupled coupled metapopulation metapopulation dynamics at comparable comparable spatial scales. Is this apparent apparent scarcity real? Clearly, the great difficulty of among-population processes of studying among-population processes in nature nature is aa major major ob­ obstacle to reaching reaching finn firm conclusions. conclusions. However, However, it may also be that systems in which migration too low, or which some populations migration among among patches patches is too high high or or too or in which some populations are much more more common approxi­ are highly persistent persistent (Fig. 2), are are truly much common than than ones ones approxistructure. mating the classical structure. If metapopulations sufficiently to include include the nonnon­ If we we broaden broaden our our view of of metapopulations classical how does perception of prevalence and imporimpor­ classical kinds, kinds, how does this affect affect our our perception of the prevalence tance of metapopulations? This This is clearly an an area area of of active work, work, as this volume volume tance of metapopulations? illustrates, but but we we will advance some of of our our own own speculations. speculations. Regional illustrates, advance some Regional persist­ persistence may may be be an overemphasized concern, concern, arising from models models that were based based ence an overemphasized arising from that were on a simple analogy and and that that overlooked overlooked variation patch size, on simple birth-and-death birth-and-death analogy variation in patch detailed local local population dynamics, explicit explicit spatial patches, and and detailed population dynamics, spatial relations relations among among patches, spatio-temporal correlation correlation in in the the environment. environment. Adding Adding such such real-world real-world refinerefine­ spatio-temporal ments to to models models may may have have the the general general effect effect of of reducing reducing the the relative relative importance importance ments of migration migration and and recolonization, recolonization, and and increasing increasing that that of of local population population processes, processes, of for regional regional persistence. persistence. If If this this is true, true, then then what what other other types of "metapopulation "metapopulation for types of effect" effect" may may we we seek seek in in nature? nature? When levels levels of of migration migration among among patches patches are are moderate, moderate, and and patches patches vary vary in in When their degree degree of of spatial spatial isolation, isolation, aa system system may may be be demographically demographically unified unified in in their central patches patches and and exhibit exhibit rescue rescue effects effects or or extinction extinction and and recolonization recolonization on on central increasingly marginal marginal ones. ones. The The defining defining feature feature of of such such aa metapopulation metapopulation is is not not increasingly the dependence dependence of of regional regional persistence persistence upon upon local local extinction extinction and and recolonization, recolonization, the but the the strong strong effect effect of of patch patch structure structure and and dispersal dispersal on on local local population population persistpersist­ but ence and/or and/or regional regional distribution. distribution. This This type type of of metapopulation metapopulation structure structure seems seems to to ence us us aa highly highly plausible plausible one. one. Consideration of of variation variation in in patch patch size size or or quality quality leads leads into into the the realm realm of of Consideration mainland - island and and source-sink source- sink dynamics, dynamics, where where again again the the appropriate appropriate quesquesmainland-island

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Empirical EmpiricalEvidence Evidencefor Metapopulation MetapopulationDynamics Dynamics

41

tions are not about regional persistence, but about regional distribution, and about local persistence in habitats too small (islands) or poor in quality (sinks) to support Mainland-island are well documented, but long-lived populations. Mainland -island dynamics are source-sink source - sink dynamics are virtually untested; how frequently species are found in habitats where they are unable to replace themselves without immigration, and how much this affects their overall demography, remains a very open area for empirical research. The related refuge models of predation and competition, in which coexistence is made possible by the net dispersal of the victim species from habitats of low to those of high predation or competition (e.g., Hochberg and Holt, 11995), 995), also deserve more empirical study. another important area for for exploration is the For multispecies systems, another effect of trophic complexity. Both theory and empirical work have emphasized two or three tightly coupled species, but real food webs are nearly always more M. cinxia cinxia system comprises four important species on complex than this. The M. three three trophic trophic levels, plus some eight minor species of which some are gener­ generalists (G. Lei and Hanski, unpublished manuscript). manuscript). Four spider and three lizard Bahamanian islands (Schoener and species and their shared prey interact on Bahamanian sevSpiller, 11987a,b). 987a,b). Even relatively simple biocontrol systems typically include sev­ enemies (e.g., Quezada, Quezada, 1969; Murdoch et et at. al.,, 1996). eral important natural enemies 1 969; Murdoch 1 996). have yet to address systems of many species at multiple Metapopulation models have charactertrophic levels, each with different population dynamics and dispersal character­ istics, each coupled to other species to varying degrees (but see Holt, this volume). sitWhether spatial subdivision retains its potentially stabilizing effect in these sit­ other important important consequences, is an open area area for theoretical and uations, or has other empirical work. empirical In all of of these these extensions of of metapopulation metapopulation dynamics, an approach that comcom­ bines empirical general empirical work and modeling will be very helpful. helpful. For For example, example, no general guidelines are are available available for for empiricists empiricists to decide decide how much much migration migration is enough, too little or too much for metapopulation occur. Merely observing some metapopulation effects effects to occur. asynchrony in local population adequate, since this will be population fluctuations fluctuations is not adequate, shaped not only by migration, but by patterns patterns of of environmental variability and by the sampling regime. Moreover, the critical critical level of of migration will depend depend greatly on the exact hypothesis, or type of of metapopulation behavior, behavior, that is of of interest. Thus, combining combining field moderately detailed detailed system-specific interest. field work with moderately system-specific models models will be valuable valuable in many cases. In conclusion, this review review of of empirical empirical studies studies makes makes it clear clear that that a great great of spatial population structures exists exists in nature, nature, and and recognition of of this this variety of diversity suggests and theoretical suggests changes changes in how how both both empirical empirical and theoretical metapopumetapopu­ lation lation research research are are approached. approached. Whether Whether experimental experimental or or observational, singlesingle­ or or multispecies, empirical empirical studies studies need need to to take take fully into account account the the different different types of of metapopulation metapopulation structure structure that that are are possible, possible, perhaps perhaps treating them them as alternative alternative hypotheses to test. While empiricists empiricists attempt attempt to better better characterize characterize metapopulations for theorists metapopulations in nature, nature, an important important task for theorists is to to continue exploring exploring the ways ways in which which metapopulation metapopulation behavior behavior changes changes as as patch patch configuration, configuration, disdis­ persal, and local population dynamics are altered persal, and population dynamics altered in realistic realistic ways. Through Through this this

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SusanHarrison Harrisonand and Andrew AndrewD.D. Taylor Taylor Susan

combined c o m b i n e d effort, effort, we we will will be be much m u c h better better able able to to identify identify the the ways ways that that within­ withinand and between-population b e t w e e n - p o p u l a t i o n processes p r o c e s s e s interact interact to to determine d e t e r m i n e the the behavior b e h a v i o r of of natural natural systems. systems.

ACKNOWLEDGMENTS ACKNOWLEDGMENTS We We thank thank Ilkka Ilkka Hanski. Hanski, Daniel Daniel Simberloff, Simberloff, Chris Chris Thomas, and and an an anonymous reviewer reviewer for helpful comments comments on on an an earlier earlier draft. draft. helpful

II

Metapopulation Dynamics and Landscape LandscapeEcology Ecology John A. A. Wiens Wiens John

INTRODUCTION II.. INTRODUGION The fusion of metapopulation metapopulation studies studies and and landscape ecology should should make make for for an exciting exciting fusion of landscape ecology scientific and Gilpin, Gilpin, 1991) 1 99 1 ) scientific synthesis synthesis (( HHanski a n s k i and

The synthesis o metapopulation studies and landscape landscape ecology anticipated anticipated The off metapopulation Hanski and and Gilpin Gilpin has has barely barely yet yet begun. There There are are at least two reasons reasons for for this by by Hanski ( Wiens, 1995a). 1 995a). First, First, as many many of of the the chapters chapters in this this volume volume illustrate, illustrate, metameta­ (Wiens, population theory theory continues continues to to be be tied tied to to a view of of spatial spatial patterning patterning of of environenviron­ population ments in which which patches patches are are embedded embedded in in a featureless featureless background background matrix. matrix. Second, Second, ments landscape ecology seems seems still to to be be in the the process process of of defining defining what what it is about and landscape ecology about and describing complex complex spatial spatial patterns, patterns, but but it it has has not not developed developed much much theory theory to to deal deal describing with spatial spatial patterning. patterning. By By focusing focusing on on some some shared shared areas areas of of interest, interest, perhaps perhaps the the with synthesis synthesis of of these these disciplines disciplines can can be be accelerated. accelerated. In this this chapter, chapter, I consider consider the the relationship relationship between between the the emerging emerging (but (but yet yet In immature) discipline discipline of of landscape landscape ecology ecology and and the the emerged emerged (but (but perhaps perhaps adolesadoles­ immature) cent) discipline discipline of of metapopulation metapopulation dynamics. dynamics. I will will argue argue that that considerations considerations of of cent) metapopulation structure structure may may often often be be incomplete incomplete unless unless they they are are framed framed in in the the metapopulation context context of of the the underlying underlying landscape landscape mosaic. mosaic. Metapopulation Metapopulation Biology Biology

Copyright Copyright 9 © 1997 1997 by by Academic Academic Press, Press, Inc. Inc. All All rights rights of ofreproduction reproduction in in any any form form reserved. reserved.

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John A. John A. Wiens Wiens

II. II. APPROACHES APPROACHESTO TO PATCHINESS PATCHINESS Ecologists have always known known that nature nature is patchy and heterogeneous, heterogeneous, even Ecologists if much much of of their their theory has not not treated it so. Habitats Habitats in areas used by humans if humans fragments, and the patchwork occur as sharply defined defined blocks blocks or fragments, patchwork nature nature of of the landscape landscape mosaic mosaic is especially evident in such environments. environments. Even in more more natural natural settings, habitats are heterogeneous heterogeneous at virtually any scale of settings, however, however, habitats of resolution. resolution. Although indistinct gragra­ Although patch patch boundaries boundaries in such situations situations may sometimes sometimes be indistinct dients 992b), the spatially variable dients rather than sharp discontinuities discontinuities (Wiens, (Wiens, 11992b), variable character follow the convenconven­ character of of environments environments still remains. remains. In this chapter chapter I will follow tion that has become become widespread under widespread in ecology of of considering considering such variation variation under the rubric though "patches" "patches" are not always evident rubric of of "patchiness," "patchiness," even though evident in nature. nature. Dealing Dealing with such spatial heterogeneity heterogeneity has been been a major major challenge challenge in both empirical and theoretical ecology. Faced with the daunting daunting complexity of of spatial patterns patterns in the real world, world, field ecologists ecologists historically tended tended to focus focus on patterns and dynamics dynamics of of ecological systems within relatively homogeneous homogeneous habitat habitat types (e.g., watersheds, watersheds, woodlots) woodlots) or aggregated spatial spatial variation into into dimensionless dimensionless indices indices of of heterogeneity heterogeneity or dispersion. dispersion. More More recently, recently, it has become become fashionable fashionable to map map spatial patterns patterns at broad broad scales using geographic geographic information information systems systems and impor­ spatial statistics, statistics, but the link between between such technologies technologies and ecologically important questions questions is not always apparent. apparent. Spatial variance also strains the capacities of of analytical models models and theory if it is viewed viewed explicitly (i.e., by location) location) rather than averaged as "noise." "noise." As a consequence, consequence, many theoreticians theoreticians concerned concerned with heterogeneity have contented themselves themselves with simple models in which which spatial patterning is collapsed into patches Kareiva, 11990b; 990b; Wiens, 1995a). 1 995a). patches and an ecologically neutral neutral "matrix" "matrix" ((Kareiva, Such patchmatrix theory is usually spatially implicit ( Hanski, 1994c), 1 994c), in that patch-matrix implicit (Hanski, the locations 996a). The inin­ locations of of patches patches in the matrix are not specified (Wiens, (Wiens, 11996a). teresting in­ teresting dynamics occur in the patches, patches, which are usually considered considered to be internally homogeneous; homogeneous; the matrix is viewed viewed as inhibiting inhibiting interactions interactions among among predators). patches (e.g., migration, migration, colonization, colonization, gene flow, prey discovery by predators). Traditional -matrix Traditional metapopulation metapopulation theory is an elaboration elaboration on this patch patch-matrix theme. 1 970; Hanski, theme. Levins' Levins' metapopulation model ((1970; Hanski, this volume) volume) considered the patches habitat of of a population population to be subdivided subdivided into an infinite number of of similar similar patches undefined locations mod­ occupying undefined locations in a background background matrix. As metapopulation metapopulation modeling has progressed, progressed, however, details about patch sizes, patch clumping, indi­ individual movement movement capacities, capacities, local patch dynamics, and explicit patch locations locations have been Hanski, 11994a,c; 994a,c; see Hanski, been incorporated incorporated ((Hanski, Hanski, this volume; Gyllenberg Gyllenberg et et al. al.,, this volume). volume). Most Most patch theory deals deals with with the the dynamics dynamics of of populations populations occupying occupying a patchy environment (Wiens, 976; Levin, 11976; 976; Kareiva, 11990b; 990b; Shorrocks Swing­ environment (Wiens, 11976; Shorrocks and Swingland, 990). Another heterogeneity has focused land, 11990). Another approach approach to heterogeneity focused on the the dynamics dynamics of of the patches patches themselves. themselves. Although Although the spatial pattern pattern of of some patches, patches, such as the islands islands considered considered in island biogeography biogeography theory, may be relatively static in ec-

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4S 45

ological time, the patch structure of most environments is not. Patches are de­ destroyed and generated by disturbances at multiple scales. They undergo change through successional development. These "patch dynamics" ((Pickett Pickett and White, 11985) 985) produce changes in the spatial patterns and relationships of patches in a matrix. Attempts to model these dynamics have generally followed analytical approaches 974; Hastings, 11991)or 99 1 ) or have approaches (patch demography; Levin and Paine, 11974; simulated the spatial and temporal dynamics of patchy environments (e.g., Fahrig, 11990). 990). Most of this work has followed the patch-matrix patch-matrix conceptualization of spatial patterns. The recent Risser et recent emergence of landscape ecology as a discipline ((Risser et al. al.,, 11984; 984; Forman and Godron, 11986; 986; Merriam, 11988; 988; Turner, 11989; 989; Wiens, 1992a; 1 992a; 993; Hobbs, 11995) 995) offers the prospect Wiens et et al. al.,, 11993; prospect for for going beyond a simple patch -matrix approach to adopt a more realistic, spatially textured patch-matrix textured view of het­ heterogeneity. In landscape ecology, the "matrix" is itself spatially structured, structured, and spatial relationships play an active role in determining determining the dynamics within the "patches" of interest. Patches are viewed as components in a landscape mosaic, and what happens happens within and among the patches patches in a landscape may be contingent on the composition and dynamics of other elements of of the landscape mosaic 993; Andren, 1 994; Wiens, 1995a, 1 995a, 11996a). 996a). (Wiens et et al. al.,, 11993; Andr6n, 1994;

III. WHAT WHATIS IS LANDSCAPE LANDSCAPEECOLOGY? ECOLOGY? One of the first first tasks of an emerging emerging discipline is to define its topic and itself. "Landscape" has been defi ned as "a heterogeneous land area composed of a clus­ defined cluster of interacting ecosystems" Forman and Godron, 11986), 986), "a mosaic of hetero­ ecosystems" ((Forman heteroUrban et 987), or "a geneous land forms, vegetation types, and land uses" ((Urban et al., al., 11987), (Turner, 11989). spatially heterogeneous area" (Turner, 989). Accordingly, "landscape ecology" is "a study of of the structure, function, and change change in a heterogeneous land area composed of interacting ecosystems" ((Forman Forman and Godron, 1986) 1 986) or "the inves­ investigation of ecosystem structure and function at the landscape scale" (Pojar (Pojar et et al. al.,, 1 994). It emphasizes "broad spatial scales and the ecological effects of the spatial 1994). patterning of ecosystems" (Turner, 11989) 989) and "offers a way to consider environ­ environmental heterogeneity or patchiness in spatially explicit terms" (Wiens et et al. al.,, 11993). 993). If these definitions are a bit nebulous, it may reflect the multifarious historical development of landscape ecology and continuing uncertainty or disagreement over what it is really about. Landscape ecology began in northern Europe during the 11960s 960s as a merging of holistic ecology with human geography, with infusions from land-use planning, landscape architecture, architecture, sociology, and other other disciplines 993) ((Fig. Fig. 11,, top). From (Turner, 11989; 989; Wiens et et al. al.,, 11993) From the outset, the emphasis was practical and applied: the focus was on the interaction of humans with their environment at a broad ((landscape) landscape) spatial scale. In the early 11980s, 980s, the discipline colonized North America (and other continents, most notably Australia). The

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JohnA.A.Wiens Wiens John Human Geography~

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Functional (holistic) Ecology

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Land-use e Policy

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FIGURF development of landscape ecology in Europe FIGURE |1 Contributors Contributors to the historical historical development landscape ecology Europe (top) (top) and North America America (bottom).

beachheads in in North North America America were were small small and somewhat isolated. isolated. Perhaps Perhaps beachheads and initially somewhat through founder founder effects effects or or mutations, mutations, the the development development of of landscape landscape ecology ecology there there through followed aa somewhat somewhat different different trajectory trajectory (Fig. ( Fig. 1, 1 , bottom). bottom). The The linkage linkage with with tratra­ followed ditional ecology ecology was was much much stronger stronger than than in in Europe, Europe, and and as as aa consequence consequence the the ditional questions asked asked and and approaches approaches used used differed differed considerably. considerably. There There was was aa more more questions self-conscious emphasis emphasis on on concepts concepts (Wiens, (Wiens, 1995a), 1 995a), aa greater greater reliance reliance on on quanquan­ self-conscious titative procedures procedures (Turner (Turner and and Gardner, Gardner, 1991), 1 99 1 ), and and an an application application of of the the landland­ titative scape scape perspective perspective to to aa broad broad range range of of basic basic as as well well as as applied applied problems. problems. These pathways pathways of of historical historical development development have have led led to to three three rather rather different different These views of of the the primary primary focus focus of of landscape landscape ecology. ecology. Continuing Continuing in in the the European European views

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Metapopulation Metopopulation Dynamics Dynamics and and landscape LandscapeEcology Ecology

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tradition, one view portrays landscape ecology as "a new holistic, holistic, problem-solv­ problem-solving approach to resource management" ( Barrett and Bohlen, 99 1 ). It is a syn­ management" (Barrett and Bohlen, 11991). synthetic, thetic, holistic, human human ecology. The The second second view, which has become become most prev­ prev' Neill alent among ecologists, treats treats "landscape" "landscape" as a level of of organization organization (e.g., O O'Neill et 986; Gosz, 11993) 993) or as a scale et al. al.,, 11986; scale of investigation (i.e., tens to thousands thousands of of 993; Hobbs, 1 994; Pojar et ha; Forman and 986; Hansen et and Godron, 11986; et al. al.,, 11993; Hobbs, 1994; et al., al., 11994). 994). In the the latter latter case, case, the the questions are often no different different from those that ecologists have always asked; they are just asked at a much broader broader scale. The third view more explicitly emphasizes the structure and dynamics of of landscape 989; Wiens et mosaics and their their effects on ecological phenomena (Turner, (Turner, 11989; et al., al., 11993; 993; Wiens, 11995a). 995a). Rather than restricting the the focus to broad scales, the the scale of investigation investigation is dictated dictated by the organisms studied and the questions asked ((Wiens, Wiens, 11989a; 989a; Haila, 11991; 99 1 ; Pearson et al., 1996). 1 996). In this view, landscape et al., landscape ecology is more than than just spatially explicit ecology, because because the patterns patterns and interactions interactions of entire mosaics are the focus of of investigations. This diversity of of views suggests that that landscape landscape ecology is "a science science in search of itself" Hobbs, 11994). 994). In addition to being a young discipline, intel­ itself" ((Hobbs, discipline, it is also intellectually immature, in that 987; Hagen, that it lacks conceptual unity (cf. Loehle, 11987; Hagen, 11989). 989). It has no well-defined theoretical framework (Turner, 989; Wiens, 11995a) 995a) (Turner, 11989; and 992a). Despite and tends to be more qualitative than quantitative quantitative (Wiens, (Wiens, 11992a). Despite all of of this, several prevailing prevailing themes of of landscape landscape ecology have emerged: •

patches) vary in quality in both space and 9 Elements in a landscape landscape mosaic ((patches) and time. In a landscape, landscape, patch quality is a continuous rather rather than than a categorical categorical (i.e., suitable vs unsuitable, or or patch-matrix) patch-matrix) variable. Patch quality can be viewed as a spatially dependent benefit function (Wiens et al., 993; Wiens, 11996a). 996a). dependent costcost-benefit (Wiens et al., 11993; 9 Patch edges edges or boundaries may play critical roles roles in controlling or filtering et al. 985; Holland flows of of organisms, nutrients, or materials over space (Wiens et al.,, 11985; et 99 1 ; Hansen and di Castri, 11992). 992). What happens at boundaries may have et ai., al., 11991; important effects on both within-patch within-patch and between-patch between-patch dynamics. landscape mosaic has 9 The The degree degree of of connectivity connectivity among among elements in a landscape major consequences Lefkovitch consequences on patch interactions and landscape landscape dynamics dynamics ((Lefkovitch 1 993). How disturbances and Fahrig, 11985; 985; Taylor et et al., al., 1993). disturbances propagate over a landscape, for for example, may be dictated by landscape landscape connectivity as well as boundary effects (Turner et 1 989). Connectivity involves much more than et al. al.,, 1989). corridors. 9 Patch context matters. What happens happens within a patch is contingent on its location, relative to the structure of of the surrounding mosaic. A patch of of the same habitat habitat may be of of quite different different quality, depending on the features features of of adjacent or nearby 993). Contrary to island nearby elements of the landscape landscape (Wiens et et al., al., 11993). island biogeography theory (or, implicitly, patch-matrix patch-matrix theory), no patch patch is an island (cf. Janzen, 11983). 983). It is this contextual dependency that requires requires landscape ecol­ ecology to be spatially explicit. •

•

•

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John A. Wiens John A. Wiens

IV. HOW IS IV. HOW IS LANDSCAPE LANDSCAPEECOLOGY ECOLOGYRElEVANT RELEVANTTO TO METAPOPULATION METAPOPULATIONDYNAMICS? DYNAMICS? To metapopulation dynamics, we must must To see see how how these these themes themes may may relate relate to to metapopulation dynamics, we review metapopulation theory theory (see Hanski and review briefl brieflyy the the essential essential features features of of metapopulation (see Hanski and Simberloff, ned in various Simberloff, this volume). volume). "Metapopulations" "Metapopulations" have been been defi defined various ways, but metapopulation is local (patch) but generally generally aa metapopulation is spatially spatially subdivided subdivided into into aa series series of of local (patch) populations. The view emphasizes populations. The classical classical view emphasizes aa balance balance between between extinctions extinctions and and recolonizations populations that long-term persistence recolonizations of of local local populations that facilitates facilitates long-term persistence of of the the 970; Hanski and Thomas, 1 994; Hanski, Hanski, this volume). volume). metapopulation Levins, 11970; metapopulation ((Levins, Hanski and Thomas, 1994; The dynamics dynamics of of local local popUlations populations are density-dependent density-dependent within within patches asynThe patches but but asyn­ chronous among among patches, patches, and and migration migration (dispersal (dispersal I1)) among among patches patches links them them chronous together. inter­ together. Interpatch Interpatch movement movement is the key. If If migration migration is large large relative to interpatch uncorrelated sources sources of popUlation variability variability patch distances distances (and (and other other spatially spatially uncorrelated of population are populations will be mixed are not not important), important), the dynamics dynamics of of local populations mixed together together and and they will act population. On the other hand, if if movement they will act as as aa single single large large population. On the other hand, movement among among patches recolonization of patches is infrequent infrequent it may not be adequate adequate to ensure ensure recolonization of habitat habitat patches have suffered extinction, dooming dooming the the entire patches in in which which local local populations populations have suffered extinction, entire metapopulation global extinction. metapopulation to to global extinction. The classical view view of metapopulations and The contrast contrast between between this this classical of metapopulations and aa landscape­ landscapebased view is perhaps most apparent graphically. In a traditional based perhaps apparent graphically. traditional (theoretical) (theoretical) metapopulation, metapopulation, local local populations populations occur occur in in habitat habitat patches patches in in aa featureless featureless matrix matrix ((Fig. Fig. 2A). Not all patches are occupied at a given time, and populations Not patches are given and local populations wink wink into into and and out out of of existence existence as as extinction extinction and and recolonization recolonization occur. occur. Patches Patches may vary in size or shape, patch-colonization shape, but but the primary determinants determinants of of patch-colonization probability Making a metapopula­ probability are are movement movement rates rates and and interpatch interpatch distances. Making metapopulation model not sufficient, to cast it in model spatially explicit is therefore therefore necessary, but not a landscape populations of metapopulation occur landscape context. context. In reality, the local populations of a metapopulation occur in in aa complex of other habitat patches, in habitat habitat patches patches that that are are immersed immersed in complex mosaic mosaic of other habitat patches, corridors, corridors, boundaries, boundaries, and the like (Fig. (Fig. 2B). The The most most obvious obvious effects of of this landscape landscape structure structure are are on on individual individual movement movement patterns patterns among among patches patches and, and, consequently, consequently, on patch-recolonization patch-recolonization probabilities. probabilities. In a landscape landscape mosaic, inter­ interpatch Fig. 2A), complex function function of patch distances distances are are not not Euclidean Euclidean (e.g., (e.g., Fig. 2A), but but are are aa complex of boundary boundary permeabilities permeabilities and and relative relative patch patch viscosities viscosities to to moving moving organisms organisms (e.g., (e.g., 993). Other Fig. Fig. 2B; Wiens Wiens et et al., al., 11993). Other aspects of of metapopulation metapopulation structure, structure, such as the dynamics of the patches themselves (and, consequently, patch-extinction dynamics of the patches consequently, patch-extinction probabilities), uenced by landscape probabilities), may also be infl influenced landscape structure. structure. Because very little empirical work that that directly directly links landscape landscape ecology to Because I

with usage this volume, "migration" rather rather than ITo be consistent consistent with usage elsewhere elsewhere in this volume, I use "migration" than "dispersal" "dispersal" to refer one-way movements Although "migration" refer to one-way movements of individuals individuals beyond beyond their their home home ranges. ranges. Although "migration" is customarily myself the customarily used used in this this sense sense by geneticists geneticists and entomologists, entomologists, to an ornithologist ornithologist like like myself term with birds, I will will term has a specific specificmeaning meaning that that is different different from from "dispersal." "dispersal." In examples examplesdealing dealing with therefore ( 1 992b) discuss therefore use "dispersal" "dispersal" rather rather than than "migration." "migration." Stenseth Stenseth and Lidicker Lidicker (1992b) discuss these these ter­ terminological minological issues. issues.

A

B

FIGURE inter­ FIGURE22 (A) Metapopulations Metapopulations in theory. The The solid patches patches are occupied occupied and are linked linked by intermittent migration, migration, whereas whereas the hatched hatched patch is suitable habitat habitat that is presently unoccupied. The The mittent background matrix has no effect on interpatch movements, movements, although the distance distance between patches patches background and their arrangement arrangement may. (B) Metapopulations in reality. The The patches patches are the same, but the "matrix" is a landscape various patches Movement pathways pathways among among suitable patches, landscape mosaic mosaic of of various patches and corridors. corridors. Movement patches, and the probability that migrating patches, are affected by the explicit migrating individuals individuals will reach reach the patches, spatial landscape. spatial configuration configuration of of the landscape.

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John John A. A. Wiens Wiens

metapopulation metapopulation dynamics dynamics has been been done, done, a discussion discussion of of how how the major major themes themes of of landscape landscape ecology m spatial and temporal temporal variations variations in patch patch quality, boundary boundary effects, landscape connectivity, patch context-affect connectivity, and and patch context--affect the three components components of local extinction, of metapopulation metapopulation dynamics dynamics ((local extinction, interpatch interpatch movement, movement, and recolo­ recolonization) nization) must must necessarily be somewhat somewhat abstract abstract and and conceptual. conceptual. It may be useful, therefore, therefore, to preface preface this discussion discussion with a few few examples of of the effects effects of of land­ landscape structure provided by Angelstam Angelstam structure in the real world. Additional Additional examples examples are are provided ((1992), 1 992), Fahrig and Freemark 1 993), and Hobbs ((1995). 1 995). Freemark ((1993), and Hobbs

A. Some Some Examples Examples of landscape LandscapeEffects Effects Some Some of of the effects effects of of landscape landscape structure are related related to patch characteristics characteristics such as patch patch size or spacing. spacing. For For example, the size of of habitat habitat patches patches has been been related Verboom et related to the persistence persistence of of local populations populations of of forest forest birds birds ((Verboom et al. al.,, 11991a; 99 1 a; Villard 992), and the degree habitat patches patches has been Villard et et al., al., 11992), degree of of spacing of of habitat has been shown shown to affect affect the likelihood likelihood of of recolonization recolonization of of vacant vacant patches patches by the Glanville Glanville fritillary (Melitaea Hanski et 995a). Both Both patch (Melitaea cinxia) cinxia) in Finland ((Hanski et al. al.,, 11995a). patch size and remnant forest spacing spacing influenced influenced the use by brown brown kiwis (Apteryx (Apteryx australis) australis) of of remnant forest fragments New Zealand Zealand (Potter, 990). Kiwis fragments in an agricultural matrix in New (Potter, 11990). Kiwis are flightless, isolated remnants. remnants. All fragments flightless, so they must must walk between between isolated fragments less than regardless of 80 m from from other other forest forest remnants remnants were used by the birds, regardless of their size. Movements Movements of of more more than than a kilometer kilometer from the reserve, reserve, however, however, were were accom­ accom"stepping stones." situation, the spatial plished by using small fragments fragments as "stepping stones." In this situation, interspersion of of habitat habitat patches patches was a critical factor factor in determining determining the effects effects of of patch isolation and, consequently, consequently, the potential for for metapopulation metapopulation dynamics. Patch guration may also be important. important. The emigration Patch edges edges and and their their confi configuration emigration of from patches of GIanviIIe Glanville fritillaries from patches of of suitable suitable habitat, habitat, for for example, increases increases with Kuus­ with the proportion proportion of of the patch patch boundary boundary that is bordered bordered by open open fields ((Kuussaari et 996). Gates 1 978) found passerine et al. al.,, 11996). Gates and and Gysel ((1978) found that that the abundance abundance of of passerine birds elds and forests, birds increased increased at the boundary boundary between between fi fields forests, and they suggested suggested that that individuals individuals might be drawn drawn to the edge edge as nesting nesting habitat habitat because because of of greater greater food 992; Andren, 992, food availability there. Numerous Numerous studies (e.g., Angelstam, Angelstam, 11992; Andr6n, 11992, 11995), 995), however, however, have have documented documented that predation predation rates may may be greater at such ecotones, ecotones, presumably presumably due to predators predators living in adjacent adjacent areas. For For some some species, species, edges individuals to areas in edges may function function as an "ecological "ecological trap" trap" by attracting attracting individuals which 978). Predation hab­ which predation predation losses are great (Gates and and Gysel, 11978). Predation risks at habitat edges 985; Angelstam, edges vary as a function function of of the surroundings (Wi1cove, (Wilcove, 11985; Angelstam, 11992; 992; Wiens, 11995b), 995b), so the landscape Pear­ landscape context context of of patches patches is also important. important. Pear' s ((1993) son 1 993) work on habitat occupancy also son's occupancy by birds in the Georgia Piedmont also illustrates illustrates the effects effects of of landscape landscape context. context. There, There, the composition composition of of the sur­ surrounding 74% of of the variance rounding matrix matrix explained explained as much much as 74% variance in habitat habitat occupancy occupancy by some but was unimportant unimportant for some species but for other other species. The The demographic demographic con­ consequences of sequences of such edge- and context-related context-related effects have have received received very little at­ attention, tention, but but they may have have important important effects effects on metapopulation metapopulation dynamics, es-

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pecially where where populations populations are subdivided subdivided among among many small habitat habitat patches patches and cant. predation risk is signifi significant. The effects landscape mosaic have effects of of corridors corridors linking linking elements in a landscape have also been eld studies been documented documented by by fi field studies (although (although not not to the degree degree that that the the widespread widespread adoption management option adoption of of corridors corridors as a management option would lead one to believe; Bennett, Bennett, ' s cock­ 11990, 990, 11991; 99 1 ; Hobbs, 992). In Western Hobbs, 11992). Western Australia, Australia, for for example, example, Carnaby Carnaby's cockfor­ atoos (Calyptorhynchus (Calyptorhynchus funereus) funereus) use roadside roadside vegetation vegetation as a pathway pathway for for foraging movements movements among among woodland woodland patches patches in their their large home home ranges ranges (Saunders, (Saunders, 11990). 990). Where linked or are Where woodland woodland patches patches are not linked are not visually apparent apparent to the cockatoos, they are not used, even though though food food may be available available there. On the other other hand, hand, singing honeyeaters honeyeaters (Lichenostomus (Lichenostomus virescens), virescens), which are habitat habitat generalists, y across farmland Merriam and Saun­ generalists, readily fl fly farmland with little vegetation ((Merriam Saunders, 11993) 993) and 1 984) found and apparently make make little use of of corridors. Osborne ((1984) found that richness in an area that hedgerow hedgerow area area was the best predictor predictor of of bird bird species species richness area of of Great Great Britain, and the presence presence of of red squirrels squirrels (Sciuris (Sciuris vulgaris) vulgaris) in wooded wooded fragments fragments in The Netherlands Netherlands was positively related related to the the amount amount of of hedgerow hedgerow surrounding Verboom and van Apeldoorn, 1990). 1 990). In Australia, surrounding the fragments fragments ((Verboom van Apeldoorn, the occupancy occupancy of of corridors corridors by arboreal arboreal marsupials could not be predicted predicted by habitat habitat features features within the corridor corridor but required required additional information information on the composition Lindenmayer and 1 993). composition of of the surrounding surrounding landscape landscape ((Lindenmayer and Nix, 1993).

B. B. Movement Movement and and Migration Migration Individual meta­ Individual movement movement is the most most important important unifying unifying element element in both both metapopUlation 1 99 1 ; Wiens, 1 992b, population dynamics dynamics and landscape ecology (Saunders (Saunders et al. al.,, 1991; Wiens, 1992b, 11995a; 995a; Wiens 993; Ims, 11995). 995). Moreover, Wiens et al. al.,, 11993; Moreover, how fast fast and and how how far organisms organisms move het­ move imposes imposes a scale on the the environment: environment: highly highly vagile animals animals integrate integrate heterogeneity over therefore perceive over broader broader scales than do sessile sessile individuals individuals and therefore the environment lter or "grain" Wiens, 11985; 985; Fahrig environment with a coarser coarser fi filter "grain" ((Wiens, Fahrig and and Palo­ Paloheimo, 988; Kotliar and Wiens, 990; De 99 1 ; With, 994). At the heimo, 11988; Wiens, 11990; De Roos Roos et aI., al., 11991; With, 11994). outset of of any field study or modeling modeling exercise, then, the mean mean and shape of of a species migration function responses species'' migration function determine determine the the scale(s) at which population responses to environmental environmental patchiness patchiness must must be investigated. investigated. In the tradition most metapopulation tradition of of island island biogeography biogeography theory, most metapopulation models models use interpatch migration rates major determinants patch­ interpatch distance distance and and migration rates as the major determinants of of patch1 994a). The 1 988) colonization probabilities (e.g., Hanski, 1994a). The Fahrig and and Paloheimo Paloheimo ((1988) simulation guration of popu­ simulation studies studies of of the effects effects of of the the spatial confi configuration of patches patches on population indicated that migration lation abundances abundances in a metapopulation, metapopulation, for for example, indicated migration distance, distance, rather rather than migration migration rates alone alone (or demographic demographic features features such as birth birth rate), was critically important, when interpatch important, especially especially when interpatch distances distances were great. 1 995) modeled Bachman's Bachman ' s sparrow In contrast, contrast, when Liu et al., ((1995) sparrow (Aimophila (Aimophila aestivalis) aestivalis) population population dynamics, dynamics, they found found that demographic demographic parameters parameters were more important important than mortality during during dispersal dispersal (although (although not not necessarily necessarily dispersal dispersal

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John JohnA. A. Wiens Wiens

rate rate or distance). These These differences differences may stem from differences differences in model structure, structure, but they may also refl ect basic reflect basic differences differences in the life histories of of the organisms organisms modeled. Traditional Traditional metapopulation metapopulation models usually usually do do not consider consider the the details details of of movement movement in in even even an an abstract abstract sense. sense. Movement Movement is is modeled modeled as as transition proba­ probabilities among cells in a grid ((Liu Liu et ai., 1995) 1 995) or et al., or movement rates rates and distances distances are ed or are distributions. Whether move­ are simply specifi specified are drawn drawn from frequency distributions. Whether movement ment through through the matrix matrix between between patches patches is directional directional (e.g., Fig. 2A) or follows aa diffusion, 980; diffusion, correlated correlated random random walk, walk, or or some some other other algorithm algorithm (e.g., Okubo, Okubo, 11980; Turchin, 1 989; Johnson et ai., 1 992a) is not considered, even though the differ­ Turchin, 1989; Johnson et al., 1992a) is not considered, even though the differences ences among among these these movement movement patterns patterns can can produce produce substantial substantial differences differences in in the the mi­ probability of of encountering encountering a patch in the matrix. This is especially true if if migration gration rates are low or if the number number of of individuals individuals available available to migrate migrate is quite limited (as may occur when local populations populations are are small). Movement Movement patterns patterns such such as as diffusion diffusion or or random random walks walks are are handy handy modeling modeling devices that that may have some relevance relevance to how real real organisms organisms move through through a featureless featureless matrix, but they are of of limited value (other than as neutral neutral models) in specifying specifying how individuals might respond respond to a complex landscape landscape mosaic (e.g., Fig. 2B). Conceptually, the movements movements of of individuals individuals through a landscape landscape may may be viewed as a consequence consequence of of their movements movements within individual patches patches and and 993). Within-patch their movements between patches Fig. 3A; Wiens patches ((Fig. Wiens et et ai. al.,, 11993). Within-patch movement patterns patterns vary vary among among different different patch patch types. The The probability that that an an ed time interval is a individual will encounter encounter a patch patch boundary boundary during during a specifi specified function function of of these patch-specific patch-specific movements and of of patch size and shape shape (perimeter Whether or not an individual will cross a patch (perimeter:: area area ratio). Whether patch boundary boundary upon bound­ upon encountering encountering it is a function both of of features features of of the boundary boundary itself ((boundet al., and of of the characteristics characteristics ai., 1987; 1 987; Wiens, 11992b) 992b) and ary "permeability"; Stamps et of of the adjoining adjoining patch patch (patch context). [This is where where another another behavior, behavior, patch patch or habitat habitat choice, choice, becomes important.] important.] Both Both costs (e.g., (e.g., predation predation risk, risk, physiological physiological stress) and benefi ts (e.g., shelter, benefits shelter, food availability, mating mating opportunities) may differ among among elements elements in a mosaic, and and movement patterns patterns within and and between patches ect these relative costs and benefits (i.e., patch quality), at least patches may refl reflect 993; Wiens, 11996a). 996a). Some simulation models of of metapopmetapop­ in part ((Wiens Wiens et et ai., al., 11993; 1 992; Adler ulation migration migration in in patchy patchy environments environments (e.g., (e.g., Pulliam et et ai., al., 1992; Adler and and Nuernberger, 994) vary migration costs incorporate Nuernberger, 11994) costs as a function of of distance distance or incorporate differences differences in in patch patch quality. quality. To make such an individual-based conceptualization movements conceptualization of of mosaic movements relevant to metapopulation popu­ metapopulation dynamics, it must be extended extended to the scale of of population Fig. 3B). matter lation rather rather than than individual individual patches patches ((Fig. 3B). In In simple simple terms, terms, this this is is aa matter of of movements and patches of shifting shifting the scale from that of patches defined by individual home home ranges ranges to to the the broader-scale broader-scale movements movements of of populations populations (i.e., (i.e., migration) migration) and and the the scale scale of of patchiness patchiness represented represented by by interactions interactions within within aa local local population population (i.e., (i.e., nodes nodes in a metapopulation). Exactly how how the translation translation from individual move­ movements ments to to population population distribution distribution and and interactions interactions should should be be accomplished accomplished is is one one

33

A A

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Individual Individual

Metapopulation MetapopulationDynamics Dynamicsand ond Landscape LandscapeEcology Ecology

53 53

B ' Population Population B

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FIGURE33 (A) (A) Patterns Patterns of movement movement of an individual individual among among elements elements of a landscape landscape in its home FIGURE range. The movement movement pathway pathway consists consists of within-patch within-patch and between-patch between-patch components; components; both both may range. affected by the characteristics characteristics of patches patches and by their their spatial spatial configuration be affected configuration ((patch patch context). context). (B) Extension of individual individual movements movements to the the population population level. level. A local local population population may may occupy occupy patch patch i,i, Extension which individuals individuals move according according to the local local habitat heterogeneity heterogeneity within within that patch. These within which movements (characterized probability that individuals individuals will will encounter movements (characterized by a function, function, IJ,) 0;) determine the probability boundary between between patch i and patchj patch j during a given given time time interval. interval. The probability that individuals the boundary encountering the boundary will cross into into patchj, j, ' ~b0, boundary 1 ' is a function of the permeability permeability of the boundary encountering (e.g., patch patch choice). choice). Within and the behavior of the organisms organisms (e.g., Within patch j, a proportion of the dispersing individuals ((l-p) residency in the patch. Movements (0j) determine individuals l -p) may die or establish establish residency Movements within within patch patchjj (IJ ) determine probability that that the boundary boundary between between patch jj and another element the probability element in the landscape landscape (patch k) will encountered; lk ~bjkdetermines p, p, the proportion of dispersers dispersers from from patch i that move move into patch be encountered; patch k. 0 and ~bare patch-specifi patch-specific which may have density-dependent density-dependent effects Values of IJ c (as is patch density, which on movement movement and migration). migration). Developed 1 993). Developed from Wiens Wiens et al. ((1993).

of the most vexing vexing problems problems confronting confronting aa metapopulation-Iandscape of the most metapopulation-landscape synthesis. synthesis. It more general general problem problem of of translating across scales It is is part part of of the the more translating across scales in in ecology ecology (Wiens, et al., al., 1992). 1 992). (Wiens, 1989a; 1 989a; King, King, 1991; 1 99 1 ; Rastetter Rastetter et My colleagues and and II have have used used systems systems of small animals My colleagues of small animals (insects) (insects) moving moving through grassland "microlandscapes" as through grassland "microlandscapes" as experimental experimental model model systems systems (Ims ( lms et et al., al. , 1 993; Ims, Ims, 1995) 1 995) to to investigate investigate how how movements movements are affected by by mosaic mosaic structure, structure, 1993; are affected following following the the framework framework of of the the model model of of Wiens Wiens et et al. al. (1993). ( 1 993). Initial Initial studies studies of of tenebrionid beetles E l e o d e s spp.) that individuals o v e d differently tenebrionid beetles ((Eleodes spp.) indicated indicated that individuals m moved differently in in microlandscapes a few square meters differed in microlandscapes of of a few square meters that that differed in internal internal heterogeneity, heterogeneity, as as measured measured by by the the fractal fractal dimension dimension of of the the landscape landscape pattern pattern (Wiens (Wiens and and Milne, Milne, 1989). o v e m e n t alternated 1 989). M Movement alternated between between matching matching the the predictions predictions of of an an ordinary ordinary diffusion ovement diffusion model model and and those those of of anomalous anomalous diffusion diffusion depending depending on on m movement "rules," "rules," landscape landscape pattern, pattern, and and spatial spatial and and temporal temporal scales scales (Johnson (Johnson et et al., at. , 1992a). 1 992a). In particular, particular, diffusion diffusion exponents exponents changed changed significantly significantly at at spatial spatial scales scales correcorre­ In sponding 42 cm), cm), suggesting suggesting that that sponding to to the the size size of of vegetation vegetation patches patches (a (a radius radius of of ~= 42 the effects effects of of spatial spatial heterogeneity heterogeneity on on beetle beetle movements movements at at finer finer scales scales differed differed the fundamentally et al., al. , 1992) 1 992) demdem­ fundamentally from from those those at at broader broader scales. scales. Other Other work work (Crist (Crist et onstrated that structure within onstrated that variations variations in in vegetation vegetation structure within 25 25 m: m2 areas areas had had significant significant

54 54

John A. John A. Wiens Wiens

effects on beetle movements and that that these effects differed among among Eleodes Eleodes spe­ species. The net displacement displacement of of individuals per unit time, for for example, was greater in areas dominated dominated by bare ground and by continuous low grass cover than in more heterogeneous areas that contained cacti or shrubs, and larger beetle species exhibited exhibited greater displacements in a given habitat type than did smaller beetles. The The relative relative complexity (fractal dimension) of of the movement movement pathways, however, however, was insensitive to variation among among species or habitat types, at least at the 25 m2 m2 scale of of resolution. On the other hand, broader broader comparisons among beetles, har­ harlandscape mosaics revealed significant significant vester ants, and grasshoppers in the same landscape 1 995), indicating differences differences in fractal dimensions of pathways (Wiens (Wiens et al., 1995), fundamental fundamental differences differences in the ways these taxa respond to landscape heterogeneity at this scale. These studies ne, "within-patch" studies were were conducted conducted at relatively fi fine, "within-patch" scales and recorded how individual animals responded to landscape patterns. To determine how such movements might translate translate into patterns patterns of of population distribution distribution at broader spatial scales, With and Crist ((1995) 1 995) used a cell-based simulation model to project the dispersion dispersion patterns patterns of populations populations of of grasshoppers over a broader mosaic. Individuals moved within a cell of of a given habitat type according to the empirically observed movement parameters parameters for for that habitat. Movement charac­ characteristics changed when individuals entered cells of of a different habitat type, ac­ aced transition probability (this corresponds to the between-patch cording to a specifi specified between-patch component, , 05, of of Fig. 3B). The landscape mosaic was dominated dominated (65% coverage) by a single habitat type. Under certain certain specifications specifications of transition transition probabilities, a Xanthippus corallipes, corallipes, moved rapidly through this cover type. As large species, Xanthippus a consequence, consequence, it had increased patch-residence patch-residence time (and an aggregated distri­ distribution) in the remaining Psoloessa remaining 35% of of the landscape. landscape. A smaller species, Psoloessa delicatula, was much more sedentary and preferred delicatula, preferred a habitat comprising only 8% of of the landscape. landscape. Given its low vagility, there was a low likelihood of of individuals of of this species locating locating and aggregating within cells of of the relatively rare, pre­ preferred spe­ ferred habitat. The model simulations suggested that the distribution of of this species would not diverge from the random distribution used to initiate the simula­ simulations. In fact, in the field both species exhibited the general general dispersion patterns predicted predicted by the model. How do these observations and and model analyses of patch-specific patch-specific movements movements relate patch quality, boundary ef­ relate to the four components of of landscape landscape ecology ((patch effects, patch context, and connectivity)? The differences within-patch movement differences in within-patch patterns patterns may indicate differences differences in patch quality, but the sensitivity of of model predictions probabilities between patch indicates predictions to the value of transition probabilities patch types indicates that knowledge of within-patch within-patch movement patterns by itself is not adequate adequate to predict predict broad-scale broad-scale population distributions. Something else is needed. The most likely factors affecting the translation within-patch movements translation from individual, within-patch to population distribution over a landscape are patch patch boundary effects and the influences of patch context. If individual beetles react behaviorally to the patch influences

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Metapopulation Dynamics and and Landscape Landscape Ecology MetapopulationDynamics Ecology

SS 55

boundary another will be al­ boundary itself, the likelihood of of moving from one patch patch to another altered. particular characteristics of tered. If If patch patch context context is important, then then the particular of what what is beyond beyond a given patch boundary boundary will further further modify transition transition probabilities. Landscape Landscape controls controls over over movement patterns have have yet to receive receive detailed at­ attention in either field studies. Moreover, Moreover, all of either models models or field of these approaches approaches con­ consider the structure structure of of the landscape landscape mosaic to be fixed; patch dynamics in time would add another another level of of realism (and further further computational complications) to the research program. One aspect of of landscape structure that is implicit in the spatial arrangement of of mosaic elements and the transition probabilities probabilities among among them is connectivity. Landscape Landscape connectivity refers to the degree degree to which the landscape facilitates or 993). Corridors impedes movement among patches patches (Taylor (Taylor et et al. al.,, 11993). Corridors of of similar habitat 990; habitat linked together together are are thought thought to enhance enhance connectivity (Bennett, (Bennett, 11990; Hobbs, 1992), patches among among which transition probabilities Hobbs, 1 992), but dissimilar habitat patches probabilities are Through the patterns are high may also result result in high connectivity. Through patterns of of connectivity that characterize a landscape, landscape, movement pathways pathways are directed in spatially non­ nonrandom random manners manners (Fig. 2B), which can either increase increase or or decrease decrease the likelihood that movement among specifi specificc patches in the landscape landscape (e.g., subpopulations subpopulations in a metapopulation) metapopulation) will occur. Connectivity is related related to the coverage coverage of of a given habitat habitat type in the land­ landIf a continuous scape, but the relationship is strongly nonlinear. If continuous habitat is broken broken into fragments by habitat conversion, conversion, the initial effects are due primarily to the below some threshold threshold value, loss of of habitat coverage alone. As coverage coverage drops drops below however, landscapes however, the effects of of patch patch isolation begin to be more more important. In landscapes with a low proportion further decreases proportion of of suitable habitat, further decreases in coverage coverage result in a rapidly increasing distance between between habitat habitat patches patches and even even greater isolation effects (Fig. 4). For example, Andren 1 994) found that habitat loss was a good Andr6n ((1994) predictor landscapes with predictor of of fragmentation effects on birds birds and mammals in landscapes > > 30% coverage coverage of of suitable habitats, but in more highly fragmented fragmented landscapes the effects of of patch isolation and size also became important. threshold effects also emerge in simulation studies based based on percolation Such threshold theory. In simple percolation percolation models, a landscape landscape mosaic is divided divided into suitable and unsuitable habitat patches (cells) that are distributed distributed over the landscape at random, random, with a specified coverage or proportion, proportion, p, p, of of the suitable patches (Gard­ (Gard987, 11989). 989). Above Above some ner ner et et al. al.,, 11987, some critical critical threshold, threshold, Peril' Pcrit, cells cells of of the the suitable suitable habitat An or­ habitat are likely to form a continuous continuous cluster that that spans the landscape. An organism in this "percolating cluster" will be able to move or "percolate" "percolate" across ' Neill et 1 988). For the landscape; landscape; connectivity is high (O (O'Neill et ai. al.,, 1988). For a random landscape has aa in Perit has in which which organisms organisms move only to to adjacent adjacent (but not not diagonal) cells, cells, Pcrit nomandom algo­ value of of 0.5928. 0.5928. If If the landscape pattern is generated generated using a nonrandom algo993; With et press), the value rithm (e.g., fractal curdling; Lavorel et et ai. al.,, 11993; et ai. al.,, in press), in the the of - 0.50). Similar in Pcrit Perit occur of P Pc,.it is lower lower (0.29 (0.29-0.50). Similar reductions reductions in occur with with changes changes in crit is movement patterns patterns to allow individuals individuals to move to any adjacent cell or to cross cross

S6 56

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0% 0% Proportion of of Suitable Suitable Habitat Habitat Proportion FIGURE 44 A hypothesized hypothesized relationship between the the proportion of suitable habitat in a landscape FIGURE importance of habitat loss and patch isolation to individual individual movement or population and the relative importance availability of suitable habitat decreases, decreases. the importance of habitat loss increases dynamics. As the availability monotonically. The effects effects of patch isolation (the (the inverse of landscape connectivity) connectivity) are relatively monotonically. suitable habitat is high, but increase sharply when a connectivity threshold slight when coverage coverage of suitable percolation theory parlance). Increases Increases in individual individual vagility vagility will will move this threshold is passed (P,.,.i, (Pent in percolation values of the suitable habitat. to lower coverage values

gaps where where suitable suitable cells cells are are not not immediately adjacent ((Dale et al. al.,, 1994; Pearson gaps immediately adjacent Dale et 1 994; Pearson et 996). Field beetles moving moving through et al. al.,, 11996). Field experiments experiments with with Eleodes Eleodes beetles through random random landscapes landscapes (Wiens (Wiens et et al., al., in in press) press) indicated indicated aa threshold threshold change change in in movement movement patterns patterns when when coverage coverage of of grass grass in in aa bare-ground bare-ground matrix matrix increased increased from from 0 0 to to 20%. 20%. Changes Changes in in either either the the spatial spatial pattern pattern of of the the landscape landscape or or the the scale scale over over which which individual individual organisms organisms "perceive" "perceive" landscape landscape patterns patterns (as (as judged judged by by their their move­ movements) ments) can can therefore therefore produce produce high high connectivity connectivity in in aa mosaic mosaic even even when when the the favored favored habitat habitat type type occupies occupies aa relatively relatively small small proportion proportion of of the the landscape. landscape. Differences Differences in in vagility vagility among among organisms organisms (e.g., (e.g., the the grasshoppers grasshoppers studied studied by by With With and and Crist, Crist, 11995) 995) may may also also affect affect the the location location of of aa percolation percolation threshold threshold (Fig. (Fig. 4), 4), as as Fahrig Fahrig and 1 988) also and Paloheimo Paloheimo ((1988) also suggested suggested in in aa somewhat somewhat different different context. context. Details Details of of the the spatial spatial arrangement arrangement of of habitat habitat patches patches in in the the mosaic, mosaic, such such as as those those modeled modeled by 1 985) or 1 994), are by Lefkovitch Lefkovitch and and Fahrig Fahrig ((1985) or Adler Adler and and Nuernberger Nuernberger ((1994), are likely likely to to become become important important only only around around or or below below this this threshold. threshold. Most Most models models that that link link animal animal movements movements to to landscape landscape structure structure assume assume that that movement xed species movement parameters parameters are are fi fixed species traits traits and and that that migration migration can can adequately adequately be be represented represented using using average average values. values. Individuals Individuals do do vary vary in in movement movement charac­ characteristics, teristics, of of course, course, and and the the effects effects of of this this variation variation may may be be profound. profound. For For example, example, 1 994) found Lens Lens and and Dhondt Dhondt ((1994) found that that crested crested tit tit (Parus (Parus cristatus) cristatus) young young dispersed dispersed 11 week week later later from from small, small, isolated isolated pine pine stands stands than than did did those those in in large large pine pine forests. forests.

33

Metapopulation and Landscape landscape Ecology MetapopulationDynamics Dynamicsand Ecology

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Chicks Chicks from second second broods were were also more more likely to disperse disperse into less suitable habitat fragments than were young from rst broods. Collectively, these move­ from fi first movement ment characteristics characteristics reduced reduced the probability that second-brood young would be integrated into winter flocks, which would affect affect their overwinter survival prob­ prob( 1 994) sug­ abilities. In another vein, the simulation studies of of Goldwasser et et al. al. (1994) suggested that that variability among among individuals could markedly increase the rate of of spread spread of of a population, even if if only a few few individuals in the population population migrated rapidly. The prospect that individual movement behavior may be facultatively adjusted to landscape landscape patterns patterns such as the interspersion or isolation of of suitable suitable 995; Fahrig and Merriam, 1 994) may further habitat patches ((Matthysen Matthysen et et al. al.,, 11995; Merriam, 1994) further complicate attempts to model migration dynamics in heterogeneous heterogeneous landscapes. Nonetheless, it is apparent between fine-scale movemove­ apparent that the complex interplay interplay between ment patterns, broad-scale nonlinear effects of broad-scale migration dynamics, and the nonlinear of land­ landscape-mosaic structure may have fundamentally important effects on the inter­ interpatch movements that lie at the heart of of metapopulation dynamics.

C. C. Locol Local Extinction Extinction and Recolonization Recolonization In addition addition to interpatch interpatch movement, the extinction of local populations populations in habitat patches and the subsequent recolonization of of those patches are are what drive metapopulation dynamics. Local popUlation population extinctions are often associated associated with the stochastic stochastic dynamics that that characterize characterize small populations. Deterministic Deterministic local habitat changes, however, can produce produce patch patch dynamics in the landscape landscape that that also result in the extinction of 994c). If of local populations (Thomas, 11994c). If this is the case, the local patch environment may remain unsuitable unsuitable for for some time after extinction occurs. Under these conditions, the persistence of the metapopulation depends Under of depends on how well the organisms can track the shifting spatial locations of of suitable habitat unpredictable in time patches. Because Because the location of suitable patches may be unpredictable as well as in space, how organisms move through the landscape mosaic and the scales on which they perceive environmental patchiness become all the more important. The pattern of interspersion of of suitable habitat patches through a landscape mosaic also influences extinction and colonization probabilities. The degree to which a patch is connected connected to other suitable areas or is isolated may have little direct effect on extinction, uence the immigration flow and extinction, although it may infl influence therefore determine Brown and Kodric­ determine the magnitude magnitude of the "rescue "rescue effect" effect" ((Brown KodricBrown, 11977). 977). Colonization, on the other hand, is clearly related related to the interplay between individual migration abilities and both both the distribution (i.e., isolation) and the connectivity of habitats in the landscape. landscape. If If fragmentation alters the land­ landscape so that the interspersion of of habitat patches patches no longer coincides with the migration patterns patterns of of a species, metapopulation dynamics may be disrupted. To some degree, this situation characterizes Hanski characterizes the Glanville fritillary in Finland ((Hanski et al. al.,, 11995a). et 995a).

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D. When When IsIs aa landscape LandscapeApproach ApproachNecessary? Necessary? D. few situations, landscapes, rather rather than patches in a featureless featureless In all but a few are reality. Given this, one one might might conclude that any any attempt to model or matrix, are understand understand metapopulation dynamics that that does not explicitly include landscape landscape structure would would be futile. The essence of of theory, however, however, is simplifi simplification of structure cation of reality. Good es in a way that does not violate reality too much, Good theory simplifi simplifies incorporating its essential features. In this sense, patch patch-matrix theory rep­ repwhile incorporating -matrix theory resents a significant improvement over over theories theories based based on spatial homogeneity homogeneity resents When can the details of of landscape landscape structure reasonably reasonably be ig­ ig((Wiens, Wiens, 11995a). 995a). When nored or simplifi simplified? nored ed? Green ((1994) and Paloheimo, Paloheimo, 11988, personal communi­ communiGreen 1 994) and Fahrig ((Fahrig Fahrig and 988, personal addressed this question question using simulation models. Green Green considered considered cation) have addressed of habitat connectivity in relation relation to population population and community per­ perthe effects of sistence and concluded concluded that in highly connected connected landscapes landscapes one could treat treat the entire landscape landscape as a single element (in which which case metapopulation metapopulation theory is no no entire longer very relevant). relevant). If If the landscape landscape is strongly strongly disconnected, disconnected, on the other other hand, hand, longer it may but the may be possible possible to treat treat each each element as a separate separate unit and and ignore ignore all but most basic descriptors descriptors of of patch patch structure structure (e.g., patch patch size and and separation). separation). Closer Closer the percolation percolation threshold threshold ((Fig. the other other hand, hand, the the explicit explicit spatial ar­ arto the Fig. 4), on the rangement of of patches patches in the landscape landscape and and the details of of individual individual movements movements rangement 's and patch patch transition transition probabilities probabilities may become become much much more more important. important. Fahrig Fahrig's and simulation analyses suggested that a landscape landscape approach approach may not not be required required when when suitable habitat habitat is abundant abundant and and widespread, widespread, when when individual movement movement distances are are large relative relative to interpatch interpatch distances distances (i.e., the "grain" "grain" of of the the envi­ envidistances ronment finer than than that that of when movement movement patterns do not not ronment is finer of the the organisms), organisms), when patterns do differ greatly greatly among different elements elements of of the differ among different the landscape landscape (i.e., transition transition probaproba­ bilities or when bilities are roughly equal equal and and high), high), or when the the habitat habitat pattern pattern is ephemeral. In most of of these situations, situations, either environment approaches approaches homogeneity or or the either the environment the organisms treat it as such. such. If organisms treat If this occurs occurs at a broad, broad, population population scale, then then it is unlikely develop. The unlikely that that metapopulation metapopulation dynamics will develop. The kind kind of of interplay bebe­ tween patch structure, and re­ retween local local patch structure, individual individual movements, movements, and and local local extinction extinction and colonization that is the essence of metapopulation metapopulation dynamics recolonization that essence of dynamics would would seem seem to to re­ quire a certain certain form form of one that that is in the the vicinity connectivity quire of patchiness, patchiness, one vicinity of of the the connectivity threshold analysis. Unthreshold and and does does not not meet meet the conditions conditions specified specified in Fahrig's Fahrig ' s analysis. Un­ der attention must der these these conditions, conditions, attention must be be given given to to the the details details of of landscape landscape strucstruc­ ture. ture.

V. METAPOPULATIONS, METAPOPULATIONS, LANDSCAPES, LANDSCAPES, AND CONSERVATION CONSERVATION The relevance The relevance of of metapopulation metapopulation dynamics dynamics to to conservation conservation issues issues is is treated treated in detail in many other chapters in this volume, so I will not dwell on it here. If in in many other chapters in this volume, so will not dwell on here. If

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metapopulations impli­ metapopulations are to be viewed viewed in a landscape landscape context, however, however, some some implications cations for for conservation conservation practice cannot cannot be ignored. The The traditional traditional focus focus of of conservation has been on reserves, reserves, and much of of the debate about number of about reserve reserve design has dealt with the size, shape, and and number of reserves. reserves. Reserves patches) in a background Reserves have have usually usually been been viewed viewed as habitat habitat islands ((patches) background matrix. Metapopulation Metapopulation theory has become important important in conservation biology because matrix tradition and because it fits neatly into this patchpatch-matrix and because because the widespread widespread occurrence 995b, occurrence of of habitat habitat fragmentation fragmentation has subdivided subdivided populations populations (Wiens, (Wiens, 11995b, 11996b), 996b), creating spatial patterns patterns that appear appear to match those those of of metapopulations. metapopulations. Metapopulation Metapopulation theory also predicts predicts stability solutions, solutions, offering offering the hope hope of of pop­ population persistence persistence in the face face of of local extinctions. extinctions. Habitat Habitat fragmentation, fragmentation, however, however, involves involves much much more more than than changes changes in the size and and isolation isolation of of habitat habitat patches. patches. When When a landscape landscape is fragmented, fragmented, habitats habitats are replaced by other habitats, habitats, patch patch boundaries boundaries are often often sharpened sharpened and patch patch context context changed, changed, connectivity patterns patterns are altered, and and the cost-benefi cost-benefitt contours contours of of the landscape landscape shift. Simple Simple island biogeography biogeography theory does does not not deal with such complexity of of spatial patterns, patterns, and this is one one reason reason why its value in conservation conservation efforts 982, 11984; 984; Sober6n, 992; Haila efforts is quite limited (Simberloff (Simberloff and Abele, Abele, 11982, Sober6n, 11992; et 993; and Wiens, 11995b, 995b, give other example, et al. al.,, 11993; other reasons). reasons). Island theory, for for example, predicts predicts a loss of of species species with a reduction reduction in island (patch) (patch) area-the area--the well-known well-known species -area (S-A) points above species-area ( S - A ) relationship. relationship. A scatter scatter of of points above the S - AA curve curve has has been interpreted interpreted as evidence evidence of of community community "supersaturation," "supersaturation," which which will inevi­ inevitably lead to a loss of relaxation"), whereas points lying much of species species ("faunal ("faunal relaxation"), whereas points much below island disturbance vol­ below the curve curve have have been been explained explained as results of of island disturbance (e.g., volcanic eruptions) eruptions) or extreme 1 989b). Because Because terrestrial hab­ extreme isolation isolation (see Wiens, Wiens, 1989b). habitat patches landscape mosaic, patches are are immersed immersed in a landscape mosaic, it seems seems more more likely that that such such scatter represents (at least in part) scatter represents part) the effects effects of of connectivity, connectivity, patch patch context, context, or or edge conditions Fig. 5). The which landscape conditions ((Fig. The specific specific ways in which landscape configuration configuration area relationships not been might affect affect speciesspecies-area relationships have have not been explored. explored. These These and and other other considerations considerations have led to challenges challenges to the "reserve "reserve men­ menBrussard et 992), the belief tality" ((Brussard et al. al.,, 11992), belief that that conservation conservation problems problems are are solved solved by establishing necessary, establishing reserves reserves and and ignoring ignoring the surroundings. surroundings. Reserves Reserves are are necessary, to be sure, but areas Noss and areas outside outside of of reserves may also play important important roles ((Noss and 1 99 1 ; Woinarski 992; Barrett et 1 994; Harris, 11986; 986; Saunders Saunders et et al. al.,, 1991; Woinarski et et al. al.,, 11992; et al. al.,, 1994; 1 995; Wiens, 995b, 1996b). 1 996b). For Hanski 1 994; Turner Hanski and and Thomas, Thomas, 1994; Turner et et al. al.,, 1995; Wiens, 11995b, For habitat habitat generalists or species that move move widely, management management of of landscape landscape mosaics over over large large areas areas may be essential. essential. In Australia, Australia, for for example, example, the endangered endangered Gouldian Gouldian (W oinarski et finch (Erythura (Erythura gouldiae) gouldiae) has has a limited and patchy distribution distribution (Woinarski et at. al.,, 11992). 992). Large breeding breeding populations populations still exist in several areas, areas, and these these can can be protected popUlation leaves these areas in postbreeding protected by reserves. reserves. However, However, the population postbreeding movements, with transient transient groups groups appearing appearing in widely spaced spaced (and unpredictable) unpredictable) locations locations over the landscape. Management Management by a series series of of static reserves will not not work work during during this phase, phase, when when considerable considerable mortality occurs. occurs.

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The reduced (e.g., The species-area species-area relationship. If the area of of a habitat in the landscape landscape is reduced by fragmentation), number of fragmentation), island biogeography theory predicts predicts that a new new equilibrium number of species species that is appropriate Landscape effects (e.g., connectivity, patch appropriate to the new new habitat area will be reached. reached. Landscape context), however, can reduce reduce the species loss by providing habitat refugia or increasing the likelihood that that local habitat habitat patches patches will be rapidly recolonized. On the other other hand, hand, edge effects (e.g., low boundary number boundary permeability, increased increased predation predation mortality in habitat habitat edges) edges) may reduce reduce species number below that expected from equilibrium island theory. Some of the scatter scatter of of points about reported reported speciesarea relationships may reflect the effects of species-area of such mosaic features.

The solution to such problems may be to shift from reserve management to combined with areas that receive "mosaic management," in which reserves are combined varied (and perhaps perhaps intense) human human use. If If one wishes to enhance enhance a metapopu­ metapopufor example, it may be necessary to manage not only lation structure in an area, for the habitat patches populations but the land­ patches that contain (or could contain) contain) local populations landscape features features that facilitate or impede interpatch interpatch movement as well. Too Too often, such considerations considerations are cast in terms of of corridors corridors of of like habitat habitat linking patches patches together together (e.g., the management management plan for for northern northern spotted spotted owls (Strix (Strix occidentalis occidentalis caurina); J. W. Thomas et al. al.,, 11990), landscape 990), rather than evaluating overall landscape caurina); connectivity. Proper Proper mosaic management requires that attention be given to all all of of the features features of a landscape landscape and how how they interact interact to determine the fate of of local populations populations in habitat habitat patches. I maintain that the key to accomplishing accomplishing this ob­ objective lies in understanding understanding how landscape landscape structure structure affects movement patterns patterns within and among patches 996b). patches (Wiens, I1996b).

VI. CONClUSIONS CONCLUSIONS The The main message of of this chapter chapter is that landscape structure may may often be an important component component of of metapopulation dynamics. Variations in patch quality in space and time, the form and permeability of of patch patch boundaries, boundaries, the composition and characteristics of of surrounding surrounding mosaic elements, and the connectivity among

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Metapopulation Dynamics and and Landscape Landscape Ecology MetapopuhtionDynamics Ecology

6611

landscape uence the dynamics populations and, landscape components components may all infl influence dynamics of of local populations especially, especially, the ways in which which populations populations are linked by movements of of organisms. organisms. The The synthesis synthesis of of landscape landscape ecology ecology with metapopulation metapopulation dynamics dynamics is impor­ important. Although I have emphasized emphasized the contributions contributions that landscape landscape ecology can can Although make make in developing developing an understanding understanding of of metapopulation metapopulation dynamics, the relation­ relationship between between these these disciplines disciplines should should not be one-sided. one-sided. Metapopulation Metapopulation dynamics may also contribute to the development of landscape ecology, in two ways. One contribute development of landscape emphasizing the dynamics dynamics that that occur occur in a landscape. landscape. The The spatiotemporal spatiotemporal is by emphasizing patterns patterns of of local extinctions extinctions and and patch patch recolonizations recolonizations create a shifting distribution of populations among patches. Understanding Understanding what controls controls these dynamics ad­ adof populations among dresses dresses issues of of spatial relationships relationships and mosaic mosaic composition composition that are at the heart of emphasis on these dynamics of landscape ecology. Moreover, Moreover, an emphasis dynamics can draw atten­ attention away from from the map-based map-based descriptions descriptions that characterize characterize some approaches approaches to landscape landscape ecology. The The second second way in which which metapopulation metapopulation dynamics dynamics can contribute contribute to land­ landscape ecology is in the area of of ecology, of theory. In contrast to many other other areas of landscape landscape ecology has developed developed rather little little theory. The lack of of theory may stem stem in part from the diverse Fig. 11), ), but it may also diverse historical historical roots of of the discipline discipline ((Fig. refl ect the complexity of landscape reflect of landscapes landscapes and their linkages. The variety of of landscape patterns is virtually unlimited, unlimited, and thus thus there is no single mosaic pattern pattern (or small set of Wiens, 1995a). 1 995a). In contrast, of patterns) patterns) about about which which theory can be generated generated ((Wiens, contrast, patch patch theory has developed developed at least in part part because "patchiness" "patchiness" can be collapsed collapsed into simple patterns patterns of of patches patches and matrix matrix (or so we believe). Further Further development development of predictive rather of landscape landscape ecology as a predictive rather than than a descriptive descriptive science science requires requires concepts patterns to their concepts or theories theories that that link landscape landscape patterns their consequences. consequences. As metapopulation metapopulation theorists theorists continue continue to add add complexity complexity and and realism realism to simple simple patch-matrix patch-matrix models, models, they they come come closer closer and and closer closer to developing developing true true mosaic mosaic models. models in enhancing understanding models. Quite beyond beyond the the value value of of such such models enhancing our our understanding of of metapopulation metapopulation dynamics, they may provide provide a wedge that landscape landscape ecolo­ ecologists can use to develop interactions. A linkage of develop models models of of landscape landscape interactions. of meta­ metapopulation theory with percolation theory might be especially fruitful fruitful (see With, With, in press). Throughout Throughout this chapter chapter I have have emphasized emphasized the importance importance of of understanding understanding movement. movement. Whether Whether or not a spatially subdivided subdivided population population functions functions as a meta­ metaindividuals move among population depends on how individuals among patches. patches. How individuals individuals migrate migrate is, in tum, turn, affected in a myriad myriad of of ways by landscape landscape structure. structure. Under­ Understanding standing these effects effects on movements movements is of of fundamental fundamental importance, importance, yet we know know very little about May and Southwood, Southwood, 11990; 990; about movement in an ecological context context ((May 1 995). Existing provide much Opdam, 99 1 ; Dunning Opdam, 11991; Dunning et al. al.,, 1995). Existing theory will not provide much help help here. here. Instead, Instead, we must must focus focus our our attention attention on well-designed well-designed empirical empirical studies studies of of how how individual individual movements movements are are affected by the explicit spatial patterning patterning of of en­ eninsights necesneces­ vironments. Such Such investigations can provide provide the information information and and insights sary to bring metapopulation metapopulation dynamics and and landscape landscape ecology together. together.

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ACKNOWLEDGMENTS ACKNOWLEDGMENTS Mcintyre, and an anonymous Diane Debinski, Mike Gilpin, Andy Hansen, Ilkka Hanski, Nancy Mclntyre, reviewer offered a wide variety of helpful comments on an initial draft of the manuscript, and con­ conversations with Ilkka were particularly useful in focusing my thinking about metapopulations and u.s. landscapes. My research on landscapes and spatial heterogeneity has been supported by the U.S. National Science Foundation, most recently through Grant DEB-9207010. DEB-9207010.

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II III

METAPOPULATION THEORY THEORY METAPOPULATION

The six chapters chapters in this section review much much of of the existing existing metapopulation biology, covering both both ecology and theory in metapopulation genetics and single-species and multispecies multispecies theory. Theory is developed and discussed in Part III, but with a focus on also developed particular processes rather rather than on metapopulation metapopulation dynamics in general. The fi nal chapter final chapter by Giles and Goudet Goudet in Part IV adds a useful discussion on the theory underlying genetic population differentiation in metapopulations. metapopulations. first chapters ascend from simple (Hanski) and The fi rst four chapters more complex ecological models (Gyllenberg, Hanski, and preHastings) of single species to models of competition and pre­ and Hassell) to models of communities communities dation ((Nee, Nee, May, and ((Holt). Holt). The The first first two two chapters chapters are are entirely entirely rewritten rewritten versions of respective chapters chapters in the the previous previous volume (Metapopulation (Metapopulation Dynamics, 11991), reader aa very concrete concrete Dynamics, 99 1 ), giving the interested reader opportunity to to judge the the kind of change change and and even progress that that has has occurred occurred in in the the past past 55 years. ' s chapter Hanski Hanski's chapter covers some some of of the the basic issues issues about about the the ecological dynamics dynamics of of single-species single-species metapopulations. metapopulations. To To start start ecological with, with, how commonly commonly do do species species persist persist in in fragmented fragmented landland-

scapes as classical metapopulations? metapopulations? As also highlighted by Harrison Harrison and Taylor in their their chapter, chapter, the answer answer is not well known known because because of of scarcity of appropriate appropriate field studies studies on large enough enough spatial scale for for long enough time. What is clear by now, however, is that some very good good examples examples of of species per­ permetapopulations do exist (see also Part sisting as classical metapopulations Part IV). What is the minimum habitat necessary for minimum amount amount of of suitable suitable habitat for metapopulation metapopulation survival, and what what is the minimum minimum viable meta­ metapopulation population size? These are likely to be controversial controversial questions, questions, like questions about the minimum viable population questions about the minimum population size in un­ unbroken habitats. These These are, however, however, the kinds kinds of of quantitative quantitative questions questions that ecologists will be asked, asked, and and it is our our duty to clarify not only the answers to these questions questions but also the various kinds of of uncertainties that are associated with particular particular answers answers and the risks associated associated with practical applications. applications. More More generally, ecologists ecologists will be asked to predict, in quanti­ quantitative terms, the dynamics dynamics of of particular particular species in particular particular fragmented fragmented landscapes, landscapes, including including the expected expected time to meta­ metapopulation population extinction. extinction. Hanski reviews reviews some of of the modeling modeling approaches approaches that that have been been developed developed for this purpose. purpose. Among Among other other things, these models models clearly clearly demonstrate demonstrate that that it may be very misleading population occurs misleading to assume assume that that a meta metapopulation occurs at a stochastic stochastic steady state in a rapidly changing changing landscape, landscape, a con­ conthat has weighty implications implications for for conservation. conservation. clusion that Patch Patch models models of of metapopulation metapopulation dynamics, such as the well-known well-known Levins Levins model, are often criticized for excessive excessive simplicity. The The chapter chapter by Gyllenberg, Gyllenberg, Hanski, Hanski, and and Hastings Hastings extends extends the deterministic deterministic single-species single-species theory to structured models, models, where the quantity of of interest interest is not just the fraction fraction of of occupied occupied patches, patches, like in the Levins model, model, but rather the dis­ distribution tribution of of local population population sizes. The The structured structured models models in­ include the effects of of birth, death, immigration immigration and emigration emigration on metapopulation metapopulation dynamics, though though still retaining retaining the abstraction abstraction of infinitely infinitely many patches and equal connectance connectance among the cations, the mathematics bebe­ patches. Even with these simplifi simplifications, come very complicated. predic­ complicated. It is encouraging that one key prediction, the possibility possibility of multiple equilibria, equilibria, stemming from the theory of of structured structured populations, populations, has been recently supported supported by a large-scale field study (Gyllenberg, (Gyllenberg, Hanski, and Hastings). Hastings). Nee, Nee, May, May, and Hassell Hassell extend the single-species single-species models models to pairs of of competitors competitors and mutualists mutualists and to predator-prey predator-prey in­ interactions broadly interpreted). teractions ((broadly interpreted). Theory makes makes it clear clear that the spatial structure of populations populations often often matters matters and often often makes makes it easier for for species species to coexist, which has been the main incen-

tive for for developing much of this theory in the first place (see also the chapter chapter by Harrison and and Taylor in Part I). Metapopu­ Metapopulation-Ievel lation-level coexistence may take striking forms, such as the emergence emergence of spatially chaotic patterns of of local abundance abundance in predator-prey models with restricted restricted movespatially explicit predator-prey move­ ments. A great great challenge challenge here remains remains to relate the theory to the dynamics of real metapopulations. Another Another central central theme addressed by Nee, May, and Hassell is the consequences of of habitat habitat destruction destruction on persistence persistence of single-species, single-species, competitive and predator-prey predator-prey metapopulations. metapopulations. Observing that that an analo­ analogous issue has for for a long time been in the center of of epidemio­ epidemiological theory, Nee, May, and Hassell discuss under under which cir­ circumstances the "eradication threshold" of a metapopulation, cumstances "eradication threshold" of metapopulation, essentially the minimum amount of of suitable habitat habitat as discussed discussed amount by Hanski, can be estimated simply by measuring the amount of equilibrium, the limiting resource for of unused habitat habitat at equilibrium, for meta­ metapopulation population growth. This is clearly a theme theme of of great great importance importance to conservation biologists, but also an area area where extra caution is needed in translating the theoretical results to practical rec­ recommendations ((Hanski). Hanski). Holt extends metapopulation models to extends the predator-prey predator-prey metapopulation chains of of three species, and to landscapes with two kinds of of habitat patches, with a possibility of habitat patches, of habitat habitat specialization. specialization. His analysis confirms that it is diffi cult to survive in sparse habitats, difficult habitats, and the species doing so are either extreme low extreme specialists ((low extinction rate, high high colonization rate) or, on the the contrary, hab­ habitat generalists. Species Species at higher trophic levels are are even more constrained, constrained, as the suitable suitable patches for for specific predators predators are always subsets of of patches available for for the prey (prey is gen­ generally absent absent in some patches). patches). In a spatial mosaic of of several habitat types, surprising patterns are possible, such as a gen­ generalist predator predator excluding excluding a specialist prey from particular particular hab­ habitself surviving on the alternative itat type and itself alternative prey in some other patch types. This outcome would be difficult to observe, predator are as both the prey and the predator are now absent from the focal habitat type! Including both complex landscapes and complex habitat ' s analyses complement communities in the same same models, Holt Holt's complement the results of of Nee, May, and Hassell and take a step toward a better understanding of better of metapopulation and metacommunity of mosaic landscapes that Wiens painted dynamics in the kind of in his chapter chapter in Part Part I. One increased habitat habitat fragmenta­ One of of the consequences consequences of of increased fragmentareduced potential for maintaining tion is often thought to be reduced for maintaining genetic variation in local populations and across the entire entire

metapopulation. metapopulation. The equilibrium equilibrium level and rate rate of of change change in genetic variation, measured measured for for instance instance by heterozygosity lev­ levels, are generally functions functions of of the effective effective size of of the popula­ population; hence one important important way habitat habitat fragmentation fragmentation may affect genetic variation is by changing changing the effective population population sizes. In metapopulations, metapopulations, one one may distinguish distinguish between between effective effective population respec­ population sizes at the local and and metapopulation metapopulation levels, respectively. Hedrick Hedrick and Gilpin explore with numerical numerical simulations simulations the effective effective metapopulation metapopulation size, taking taking as their their starting point point the Levins model with a fi n ite number of habitat patches. They Levins model finite number of habitat patches. examine how how the various various model model parameters, parameters, such as the number number of of patches, patches, population population turnover turnover rate, rate, patch patch carrying capacity and gene gene flow affect affect the effective effective sizes of of local populations populations and and the entire metapopulation. metapopulation. Consistent Consistent with theory (Barton (Barton and and Whitlock), Whitlock), they find that, under under the assumptions assumptions of of their model, model, the effective effective metapopulation metapopulation size is greatly reduced reduced by high high extinction extinction rate and and a small number number of of founders founders originating originating from from just just one one or a few existing existing populations. populations. Thus, Thus, metapopulation metapopulation dynamics per se and its key parameters, parameters, such as propagule propagule size, have have significant genetic consequences. consequences. This This theme is explored explored further further in the context of of an empirical empirical case study by Gilet Gilet and Goudet Goudet in Part IV. Hedrick Hedrick and Gilpin infer from from the generally high levels of of heterozygosity observed observed in nature nature for for allozyme markers that that metapopulation metapopulation dynamics in the form explored explored in their their model model have not been been of of overriding overriding importance importance in many species; otherwise heterozygosity levels should be much lower. lower. However, However, they caution that that increased increased habitat fragmentation fragmentation may have recently forced forced species species to conform conform to a metapopulation metapopulation structure, possibly possibly triggering triggering a course of of rapidly declining g.:: ge-­ netic variation. This is an argument analogous to that advanced argument analogous advanced by Hanski and by Nee, May, and Hassell Hassell in their chapters about about nonequilibrium nonequilibrium metapopulations metapopulations on their way to extinction; extinction; past habitat habitat destruction destruction may already have reduced reduced the amount amount of of suitable habitat habitat below a critical treshold, treshold, and it is only a matter of time before before the actual extinctions extinctions will occur. These conclusions ect the relatively slow time scale of conclusions refl reflect of metapop­ metapopulation dynamics. Barton Barton and and Whitlock Whitlock present present a comprehensive comprehensive review of of the consequences consequences of of spatial population population structure structure on the genetic composition composition of of metapopulations. metapopulations. The consequences consequences of of spatial structuring of of populations populations on adaptation adaptation and speciation have have been been a controversial controversial issue ever since Fisher and Sewall Wright Wright established established the fundamental fundamental results. In the metapopulation metapopulation con­ con' s shifting text, Wright Wright's shifting balance balance between between the processes processes of of random random

drift, selection, and migration is particularly intriguing. Barton and Whitlock conclude that though the shifting balance process is possible, there there are several factors which make it unlikely. Migration rate should not be too great to prevent populations from drifting to the domain of of new adaptive adaptive peaks; but migra­ migration rate must be sufficiently high to allow the new peaks to spread spread in the metapopulation. metapopulation. Small population size is generally beneficial for for a peak shift, but small populations are prone prone to local extinction, and generally send out fewer fewer emigrants, than large populations, which makes spreading of the new peak into the metapopulation more difficult. No grand conclusion on the shifting balance process is yet possible. The message that BarBar­ ton and Whitlock put forward is that the standard standard simple mea­ measures of of genetic population structure, structure, such as effective effective size or Fs, Fst,' are are not sufficient, but empirical studies studies should strive strive toward a much more comprehensive picture of geno­ of the distribution of of genotypes across populations in a metapopulation and of of the eco­ ecological and selective forces that that are are responsible responsible of of these these distri­ distributions. Studies of of population differentiation differentiation based on neutral markers have only a limited value.

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4 II

Metapopulation MetapopulationDynamics Dynamics From From Concepts Conceptsand Observations Observationsto Predictive Predictive Models Models IIkka Ilkka Hanski

I. INTRODumON INTRODUCTION The concepts of metapopulation dynamics and metapopulation persistence in fragmented landscapes have become well established in ecology during the past 5 years (Hastings and Harrison, 11994; 994; May, 11994; 994; Harrison, 11994b; 994b; Hanski, 11994b; 994b; Kareiva and Wennergren, 11995). 995). The accelerating loss and fragmentation of natural habitats ((Morris, Morris, 11995), 995), of of which most of us are personally and pain­ painfully aware, makes it tempting to suggest that, in an increasing number of of species, the spatial structure of populations populations is somehow somehow consequential to their their dynamics. Many studies have demonstrated that that small populations populations in small habitat fragments have a high risk of extinction (Schoener 1 987b; Kindvall and Ahl6n, Ahlen, (Schoener and Spiller, 1987b; 1 992; Hanski, 11994b); 994b); hence if 1992; if only small fragments remain, long-term persist­ persistence becomes necessarily a regional issue. We have now an extensive theoretical Hanski, 11985, 985, 11994a,b; 994a,b; Gilpin and Han­ literature on metapopulation dynamics ((Hanski, Han99 1 ; Hastings, 1991; 1 99 1 ; Gyllenberg and Hanski, 11992; 992; Hanski and Gyllenberg, ski, 11991; 1 993; Hastings and Higgins, 11994; 994; Tilman et 994; Hassell et 994; 1993; et al., al., 11994; et al., al., 11994; Durrett and Levin, 11994; 994; Hastings and Harrison, 1 994) and a large number Harrison, 1994) number of of useful empirical studies ((Harrison Harrison et 989; Nachman, 11991; 99 1 ; et at. al.,, 1988; McCauley, 11989; Harrison, 11991; 99 1 ; Sjogren, 99 1 ; Sjogren 1 994; Whitlock, 1992b; 1 992b; Thomas Sj6gren, 11991; Sj6gren Gulve, 1994; 1 994, 1995a; 1 995a; many chapters and Harrison, 11992; 992; Bengtsson, 1 993; Hanski et Bengtsson, 1993; et al., al., 1994, Metapopulation Metapopulation Biology Biology

1997 by Academic Copyright © 9 1997 Academic Press. Press, Inc. All rights of of reproduction reproduction in any form reserved. reserved.

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Ilkka Hanski HonskJ IIkka

that our understanding understanding of metapop­ metapopin this volume). Nonetheless, it is fair to say that ulation dynamics in real fragmented landscapes is still restricted ((Harrison Harrison and Taylor, this volume), largely because of the practical problems of conducting large spatial scale. sound empirical research at a sufficiently large publication of the previous previous volume on metapopulation metapopulation dynamics Since the publication (Gilpin and Hanski, 11991), 99 1 ) , it has become ned concept become evident that a broadly defi defined concept of of metapopulations metapopulations is needed to embrace the range of existing spatial population population structures ((Harrison, SimHarrison, 11994b; 994b; Harrison and Taylor, this volume; Hanski and Sim­ The classical classical metapopulation metapopulation concept of of Levins Levins ((1969a, berloff, this volume). The 1969a, number of of small and and hence extinction-prone extinction-prone local 11970), 970), which assumes a large number populations populations connected connected by not-too-much not-too-much migration, migration, is now seen as a special special case, possibly an uncommon Harrison, 11991, 99 1 , 11994b). 994b). This chapter uncommon special case ((Harrison, chapter is nonetheless focused focused on metapopulations metapopulations essentially agreeing with with the classical nonetheless concept. concept. This is for two reasons: reasons: First, it is too early early to conclude conclude that that Levins-type metapopulations are are exceptional; exceptional; a large large fraction fraction of rare and and specialized species metapopulations specialized species many lanscapes lanscapes may fall into into this category ((Hanski, Hanski and and Ham­ Hamin many Hanski, 11994c; 994c; Hanski mond, 1995). Second, a better better understanding understanding of of the the classical case should should enhance enhance mond, 1 995). Second, our understanding of metapopulation dynamics dynamics more more generally. our understanding of this chapter, chapter, I pose four broad broad questions: questions: In this pose four 1. commonly do species persist persist in fragmented fragmented landscapes landscapes as classical 1 . How How commonly metapopulations? This is the fundamental empirical question which I cannot cannot an­ anmetapopu1ations? the fundamental empirical question which swer here, here, but but I give one well-researched well-researched example example which which highlights of the swer highlights some of reasons why the answer is not better better known. known. 2. What What is the the minimum minimum amount amount of of suitable suitable habitat habitat necessary necessary for for metapop­ metapopulation survival, survival, and and what what is the the minimum minimum viable viable metapopulation metapopulation size? 3. Can Can we we make make quantitative quantitative predictions predictions about about the the dynamics dynamics of of particular particular metapopulations in particular metapopulations particular fragmented fragmented landscapes? landscapes? How common common are nonequilibrium nonequilibrium metapopulations, metapopulations, in which which the the rates of 4. How rates of local local extinction extinction and and recolonization recolonization are not not in balance? balance? Recognizing Recognizing the the wide wide interest interest that these these issues have have aroused aroused in conservation conservation biology biology (Western ( Western and and Pearl, 1989; 1 989; Falk Falk and and Holsinger, Holsinger, 1991; 1 99 1 ; Fiedler Fiedler and and Jain, Jain, 1992; the end four mes1 992; Harrison, Harrison, 1994b), 1 994b), I summarize, summarize, toward toward the end of of this this chapter, chapter, four mes­ sages stemming from the answers The final sages for for conservation conservation stemming from the answers to these these questions. questions. The final remarks are concerned remarks are concerned with with the the perennial perennial question question about about density density dependence dependence in population population dynamics. dynamics.

II. AN AN EXAMPLE EXAMPLE OF OF CLASSICAL CLASSICAL METAPOPULATION METAPOPULATION DYNAMICS DYNAMICS WITH WITH RAMPANT RAMPANT POPULATION TURNOVER TURNOVER POPULATION One One could could argue argue that that it is futile futile to to search search for for criteria criteria by by which which metapopulametapopula­ tions tions of of various various kinds kinds (Hanski ( Hanski and and Simberloff, Simberloff, this this volume; volume; Harrison Harrison and and Taylor, Taylor, this this volume) volume) could could be be identified, identified, to to answer answer whether whether aa particular particular system system is a "meta"meta-

44

Metapopulation MetapopulationDynamics Dynamics

71 71

population" populations in nature population" or not. This is futile because because populations nature exhibit continuous continuous variation variation in their spatial structures structures and also because because the real issue is not not so much much to classify populations populations living in fragmented landscapes but to find find ways of of un­ understanding derstanding and predicting their their dynamics. This being said, it is also clear that different different approaches approaches to population population dynamics are likely to be most effective in different satisfies the the different kinds of of systems. In this spirit, I suggest that if a system satisfies 's following following four four "conditions" "conditions" then a metapopulation approach approach based based on Levins Levins's ((1969a) l 969a) original concept is likely to be helpful. I apply these conditions conditions to an example from the work work of research group of my my research group on a species of of butterfly, the Glan­ Glanland islands in ville fritillary Melitaea Melitaea cinxia, cinxia, which we have studied on the A ~land southwestern southwestern Finland.

Condition Condition 11 The The suitable habitat occurs occurs in discrete patches which may be occupied by mead­ local breeding breeding populations. populations. The habitat type suitable for for M. M. cinxia cinxia is dry meadAland islands ows, which occur as discrete and small patches patches on islands (Fig. 1), 1 ), with on/~land the mean, median, and maximum areas of 1 3 , 0.03, and 6.80 of 0. 0.13, 6.80 ha, respectively (n = 11502; 502; Hanski et ai., 1995a). 1 995a). An estimated 60of butterflies butterfties spend their et al., 6 0 - 880% 0 % of entire lifetime in the natal Hanski et 994; Kuussaari et et al., 996); natal patch ((Hanski et al. al.,, 11994; al., 11996); hence meadows have local popUlations, populations, not not just just ephemeral aggregations of of in­ individuals. =

Condition Condition 22 Even the largest local populations populations have a substantial risk of of extinction. If If not, then then the metapopulation would would persist simply because because of of the persistence of of the largest population(s), mainland- island population(s), and we would have an example of of mainland-island metapopulations 99 1 , 1994b). 1 994b). In M. metapopulations (which are are common in nature; nature; Harrison, Harrison, 11991, cinxia, populations in 11994 994 had had ca 500 cinxia, the largest largest local population population of of 377 extant extant populations butterflies. In this and related butterflies, butterflies, populations populations with several several hundred hundred indi­ indial., viduals Harrison et viduals have been been observed observed to go extinct in only a few few years years ((Harrison et al., 11991; 99 1 ; Foley, 11994; 994; Hanski 1 995a), hence Hanski et et al. al.,, 1995a), hence the large large metapopulation metapopulation in Fig. 11 has no "mainland" populations. populations.

Condition Condition 33 Habitat patches must not be too too isolated to prevent recolonization. recolonization. If they were, we would have a nonequilibrium metapopulation metapopulation heading toward toward global 1 995) con­ extinction. Such metapopulations metapopulations are are common; Hanski Hanski and Kuussaari ((1995) conclude that 110 0 of of the 94 resident butterfl butterflyy species in Finland represent represent the non­ nonAland equilibrium case due to recent loss of M. cinxia of habitat. However, However, M. cinxia on Aland islands is not one one of of them, as the mean mean nearest-neighbor nearest-neighbor distance between between suitable habitat patches is only 240 28 m, maximum 3870 1 ), and the 240 m (median 1128 3870 m; Fig. 1),

IIkko Hanski Honski Ilkka

72 72

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FIGURE land islands in southwestern habitat FIGURE 1! Map of of A ]kland southwestem Finland, showing the locations of of the habitat patches Melitaea cinxia cinxia (dots). Patches Patches that that were patches (dry meadows) suitable for for the Glanville fritillary Melitaea occupied 00 km2 occupied in late summer summer 1993 are shown by black dots. The size of the grid is 1100 km 2 (modified from 995a). from Hanski Hanski et et al al.,.. 11995a). mean, median, and maximum distances moved by migrating butterflies among habitat habitat patches in one 50-patch network were 590, 330, and 3050 m respectively 994). ((Hanski Hanski et et at. al.,, 11994).

Condition Condition44 Local populations do do not have completely synchronous dynamics. If they have, the the metapopulation metapopulation would would not persist persist for for much much longer than than the the local local pop­ population with the M. cinxia, cinxia, we we have have demonstrated demonstrated the smallest risk risk of of extinction. extinction. In In M. substantial asynchrony asynchrony in in the the dynamics of of populations within within an an area area of of 55 by by 55 km2 Hanski et 995a). The et al., al., 11995a). The most most recent recent results results suggest dynamics dynamics that that may may km 2 ((Hanski be be somewhat somewhat correlated correlated across across areas areas up up to to some some tens tens of of square square kilometers, kilometers, but but at at the the scale scale of of the the entire entire metapopulation metapopulation changes changes in in population population size size occur occur in in opposite opposite directions Fig. 2). directions ((Fig. 2). The The question question about about spatial spatial synchrony synchrony and and its its causes causes is is aa com­ complex plex one one (Thomas (Thomas and and Hanski, Hanski, this this volume), volume), but but the the point point which which II wish wish to to make make here here is is that that in in our our butterfly butterfly metapopulation metapopulation there there is is certainly certainly enough enough asynchrony asynchrony to to make make simultaneous simultaneous extinction extinction of of all all local local populations populations aa very very unlikely unlikely event event under under the the prevailing prevailing environmental environmental conditions. conditions.

44 Metapopulation Metopopuiotion Dynamics Dynamics

73 73

Aland islands from 11993 993 till FIGURE FIGURE22 Observed Observedchanges changes in the population population sizes sizes of M. M. cinxia cinxia on Aland islands from 11994. 994. The study study area area was divided divided into 2 by 2 km2 km2squares squares for the purpose purpose of this this analysis. analysis.The symbol symbol indicates indicates the the sign sign and the magnitude magnitudeof the change change in the number number of larval larval groups groups per 4 km2 km2 square square between between the 22 years years (stippled (stippled triangles, triangles, decrease; decrease; black black triangles, triangles, increase; increase; logarithmic logarithmic scale) scale) (data (data from from I.I. Hanski, Hanski, J. Pogry, P6gry, and T. Pakkala, Pakkala, unpublished). unpublished).

III. III. CLASSICAL CLASSICALMETAPOPULATION METAPOPULATIONDYNAMICS: DYNAMICS:THE THE lEVINS LEVINSMODEL MODEL The purpose and and "validity" of simple simple models in population ecology is often The misunderstood. misunderstood. Their Their purpose purpose is is not not to to replicate replicate in in the the model model as as many many details details of of real real populations populations as as possible. possible. Models Models which which do do that that are are not not simple simple and and their their pur­ purpose ). The pose is is different different (Section (Section V V). The purpose purpose of of simple simple models models is is to to isolate, isolate, for for aa theoretical theoretical study, study, some some feature feature of of real real populations populations that that happens happens to to be be of of interest. interest. A A simple simple model model is is not not invalid invalid just just because because all all known known real real examples examples deviate deviate in in some some respect respect from from model model assumptions; assumptions; these these differences differences may may be be immaterial immaterial for for the the purpose purpose that that the the model model was was constructed. constructed. A A simple simple model model is is defective defective if if itit fails fails to to incorporate incorporate the the critical critical variables variables and and processes processes affecting affecting the the phenomenon phenomenon under under scrutiny scrutiny or or if if itit makes makes some some critically critically unrealistic unrealistic assumptions. assumptions. 1 969a, 11970), 970), the In In this this spirit, spirit, II suggest suggest that that the the well-known well-known Levins Levins model model ((1969a, the mother mother of of all all metapopulation metapopulation models models with with population population turnover, turnover, provides provides aa valu­ valuable able theoretical theoretical framework framework for for studying studying systems systems such such as as shown shown in in Fig. Fig. 11 and and satisfying satisfying the the four four conditions conditions detailed detailed in in the the previous previous section. section. The The Levins Levins model model assumes assumes aa large large number number of of discrete discrete habitat habitat patches, patches, ideally ideally of of the the same same size, size, and and

74 14

IIkka Ilkka Hanski Hanski

all connected connected to each other other via migration. migration. In reality, not all populations populations are are directly directly connected restricted, but but this makes connected to each other, other, because because migration migration distances distances are are restricted, makes no behavior of unless the no important important difference difference to to the the steady-state steady-state behavior of the the model model unless the net­ network heterogeneous. In the Levins model, model, work of of habitat habitat patches patches is strongly strongly spatially heterogeneous. the Levins habitat habitat patches patches are are scored scored only as occupied occupied or or not, as shown shown in Fig. 11,, and and the the actual best actual sizes of of the the local populations populations are are ignored. ignored. The The model model therefore therefore applies applies best to situations situations in which which local dynamics dynamics occur occur at a fast fast time scale compared compared with with metapopulation metapopulation dynamics, either either because because the the habitat habitat patches patches are are relatively small and and hence hence local populations populations quickly reach reach the local "carrying capacity" capacity" or or because because colonization colonization rate rate is low. All extant extant popUlations populations are are assumed assumed to have have a constant constant risk risk of of extinction. extinction. The The rate rate of of colonization colonization is assumed assumed to be proportional proportional to the fraction P, and fraction of of currently occupied patches patches (sources of of colonists), colonists), denoted denoted by P, and With to the fraction fraction of of currently currently empty patches patches (targets of of colonization), colonization), 11 - P. With continuous time is given by these these assumptions, assumptions, the rate rate of of change change in P P in continuous -

dP

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P = = 11 f>

e e. cC

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The fraction of habitat at equilibrium The Levins Levins model model thus thus predicts predicts that the the fraction of occupied occupied habitat equilibrium metapopulation is prepre­ the ratio e/c. increases with with decreasing decreasing value of of the e/c, and and the metapopulation < 1. 1 . In spite of dicted to persist persist (P (P is positive) positive) as long long as e/c e/c < of its simplicity, the Levins feature of metapopulation Levins model is most useful useful in highlighting highlighting a key feature of metapopulation dynamics: for for the metapopulation metapopulation to persist, recolonization recolonization must must occur occur at a suf­ sufdynamics: ficiently high increase from from high rate rate to compensate compensate for extinctions and and to allow an increase small metapopulation im­ metapopulation size. More More specifically, condition condition e/c < < 11,, or 11 < < cle. c/e, implies that that a local local population population surrounded surrounded by empty patches patches must must cause cause the estab­ estabfor the metapopmetapop­ lishment lishment of of at least one new new population population during during its lifetime lifetime (lIe) (l/e) for ulation to persist. persist. Equation important predictions Equation (2) leads leads to some some straightforward straightforward but but important predictions when when we we recognize recognize that, very generally generally and and not surprisingly, the risk of of population population extinction extinction decreases decreases with increasing increasing patch patch area, area, and and the probability probability of of coloniza­ colonization decreases Hanski, 1991, 1 99 1 , decreases with increasing increasing distance distance from from the extant extant popUlations populations ((Hanski, I1994b). 994b) . The predicts that the fraction habitat at equi­ The Levins Levins model model predicts fraction of of occupied occupied habitat equilibrium librium (P) (P) decreases decreases with decreasing decreasing average average size and and decreasing decreasing density of of habitat these predictions habitat patches patches in a patch patch network. network. The The results in Fig. 3 support support these predictions for 970s for M. cinxia. cinxia. This This species species went went extinct on the Finnish Finnish mainland mainland in the late 11970s and Hanski and from from many many other other regions regions in northern northern Europe Europe during during the the past past decades decades ((Hanski and Kuussaari, 11995). 995). The and Kuussaari, The most most probable probable reason reason for for these metapopulation-Ievel metapopulation-level

Metapopulation MetapopulationDynamics Dynamics

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FIGURE FIGURE33 Effects Effects of of average patch patch size and and regional density on the the fraction of of occupied patches A land islands (Fig. 11). ). The was divided into into 2 by by 2 km km22 patches in M. M. cinxia cinxia on on/~land The study area was patches (as in Fig. 2). (a) Squares patch area in the square; Squares are divided into into four four classes based on the average patch square; (b) squares number of per square (patch Note squares are divided into four four classes based based on the number of patches patches per (patch density). Note that the fraction of patches are large of occupied occupied patches patches is high in the squares squares where where patches large and where where patch patch 995a). density is high (both Hanski et (both effects are are highly significant; statistical analysis in Hanski et al., al., 11995a).

extinctions is decreased decreased density of of suitable habitat habitat patches, patches, forcing the equilib­ equilibrium metapopulation size to zero ). > 11). zero (e/c > The large M. cinxia cinxia metapopulation metapopulation shown in Fig. 11 is a good example of of Levins-type metapopulations. However, how representative representative is this example? example? Han­ Hanski and Kuussaari ((1995) 1 995) attempted to answer this question for Finnish butterflies. butterflies. By our count, 57 of of the the 94 resident Finnish species may may belong to this this category. This fi gure includes much uncertainty, though, because because the spatial population figure structures cinxia are not well known. Collecting structures of of all the 93 species apart apart from from M. cinxia the kind of of large-scale information we have collected collected for for M. cinxia cinxia (Fig. 11)) is expensive, obtaining obtaining funding for for this kind of of work is difficult, and the life cycles and and larval biologies of of most species make them much harder harder to study than than M. large spatial scale. These These are are some of the reasons why we do not cinxia on a large know how common common Levins-type metapopulations metapopulations are are in nature. Promising candidates candidates for species with Levins-type metapopulations can be found in forest insects living in small and patchy microhabitats such as dead tree trunks. trunks. One One such such example involving involving beetles specializing specializing on on dead dead aspen aspen trees trees in boreal forests is described 1994; see also described in detail by Siitonen and Martikainen ((1994; Hanski and Hammond, 995). As most insects live in forests, and as most forest­ Hammond, 11995). forestliving insects are more or less specialized specialized on discrete discrete microhabitats, Levins-type metapopulation metapopulation structures structures may be common in insects (see also van der Meijden Meijden and van der Veen-van Wijk, this volume). Other Daphnia water Other examples examples include include Daphnia fl eas in rock pools ((Hanski Hanski and Ranta, 11983), 983), frogs in ponds (Sj6gren, (Sjogren, 11991; 99 1 ; fleas

76 76

IIkka Ilkka Hanski HanskJ

Sjogren 994), passerine Sj6gren Gulve, 11994), passerine birds in small woodlots (nuthatch; (nuthatch; Verboom Verboom et et aI. 99 lb), 1 b), and small mammals al.,, 1199 mammals in small patches patches of of suitable habitat (pika; Smith, 11980; 980; Smith and Gilpin, this volume).

IV. SIZE IV. MINIMUM MINIMUM VIABLE VIABLEMETAPOPULATION METAPOPULATIONSIZE The minimum MVP) size has become a well-established well-established minimum viable population ((MVP) concept in population and conservation biology. MVP esti­ MVP is intended intended to be an estimate of of the minimum number number of individuals in a population population which has a good chance of of surviving for for some relatively long period of of time, for for instance, 95% chance of 1 00 years (Soule, 980). Though MVP of surviving for at least 100 (Soul6, 11980). MVP is difficult to apply