dynamic disequilibrium: a long-term, large-scale

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ISLAND BIOGEOGRAPHY SPECIAL ISSUE

Global Ecology & Biogeography

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Dynamic disequilibrium: a long-term, large-scale perspective on the equilibrium model of island biogeography

LAWRENCE R. HEANEY

Department of Zoology, Field Museum of Natural History, Roosevelt Road at Lake Shore Drive, Chicago, IL 60605, U.S.A. E-mail:

[email protected]

ABSTRACT

1

The equilibrium model of island biogeographydeveloped in the 1960s by MacArthur andWilson has provided an excellent framework inwhich to investigate the dynamics of speciesrichness in island and island-like systems. It iscomparable in many respects to the Hardy–Weinberg equilibrium model used in geneticsas the basis for defining a point of reference,thus allowing one to discover the factors thatprevent equilibrium from being achieved. Hun-dreds of studies have used the model effectively,especially those dealing with brief spans of timeand limited geographical areas. In spite of thisutility, however, there are important limitationsto the MacArthur–Wilson model, especiallywhen we consider long-term and large-scalecircumstances.

2

Although their general theory is more com-plex, the MacArthur–Wilson equilibrium modeltreats colonization and extinction as the onlytwo processes that are relevant to determiningspecies richness. However, it is likely that phylo-genetic diversification (phylogenesis) often takesplace on the same time-scale as colonization andextinction; for example, colonization, extinction,and phylogenesis among mammals on oceanicand/or old land-bridge islands in South-east Asiaare all measured in units of time in the rangeof 10 000–1 million years, most often in units of100 000 years.

3

Phylogenesis is not a process that can betreated simply as ‘another form of colonization’,as it behaves differently than colonization. Itinteracts in a complex manner with both colon-ization and extinction, and can generate patterns

of species richness almost independently of theother two processes. In addition, contrary tothe implication of the MacArthur–Wilson model,extinction does not drive species richness inhighly isolated archipelagoes (those that receivevery few colonists) to progressively lower values;rather, phylogenesis is a common outcome insuch archipelagoes, and species richness risesover time. In some specific instances, phylogenesismay have produced an average of 14 times asmany species as direct colonization, and perhaps36 species from one such colonization event.Old, stable, large archipelagoes should typicallysupport not just endemic species but endemicclades, and the total number of species and thesize of the endemic clades should increase withage of the archipelago.

4

The existence of long-term equilibrium inactual island archipelagoes is unlikely. The landmasses that make up island archipelagoes areintrinsically unstable because the geological pro-cesses that cause their formation are dynamic,and substantial changes can occur (under somecircumstances) on a time-scale comparable to theprocesses of colonization, phylogenesis, and extinc-tion. Large-scale island-like archipelagoes oncontinents also are unstable, in the mediumterm because of global climatic fluctuations,and in the long term because of the geologicallyephemeral existence of, for example, individualmountain ranges.

5

Examples of these phenomena using themammals of South-east Asia, especially thePhilippines, make it clear that the best con-ceptual model of the long-term dynamics ofspecies richness in island archipelagoes wouldbe one in which colonization, extinction, and

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phylogenesis are recognized to be of equivalentconceptual importance. Furthermore, we shouldexpect species richness to be always in a dynamicstate of disequilibrium due to the constantlychanging geological/geographical circumstancesin which that diversity exists, always a step or

two out of phase with the constantly changingequilibrium point for species richness.

Key words

Colonization, equilibrium model, extinc-tion, island biogeography, large-scale processes,long-term processes, mammals, phylogenesis.

INTRODUCTION

Few models in ecology and evolutionary biologyhave had impact equal to that of the graphicalrepresentation of the equilibrium model ofisland biogeography developed by MacArthur &Wilson (1963, 1967) as part of their more generaltheory of island biogeography. Hundreds ofresearchers have found it to provide a stimulatingand productive means of identifying importantquestions about the dynamics of species richnessin the systems that they have studied, and dozensof textbook authors have found the model to bea superb aid in helping students to understandthe complexities of biological diversity and itsdistribution (e.g. Brown & Lomolino, 1998).

The impact, indeed the popularity, of the equi

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librium model is surprising in some respects; itis, after all, remarkably simple. Only two vari

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able processes (colonization and extinction) areconsidered, and very few discrete predictionsare generated. The examples MacArthur andWilson cited in their discussion of the modelall involved phenomena that took place overless than a few hundred years, and most indecades or less, thereby implying limits to itsapplicability. Likewise, most of their examplesinvolved small areas, small populations, andlimited isolation (the few exceptions involvesimple documentation of a correlation betweenarea and species richness, not measures of pro

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cesses), again implying limitations.I believe that the impact of the MacArthur–

Wilson equilibrium model stems from the excite

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ment among field biologists, especially ecologists,that was generated by two inherent aspects ofthe model. First, prior to the introduction ofthe MacArthur–Wilson model, communitiesof organisms, especially those in isolated archi-pelagoes, usually were viewed as being eitherstatic (Dexter, 1978), with many archaic speciesrepresenting taxa long extinct on continents,

or changing only slowly and unpredictably due tothe forces of geology and perhaps climate. TheMacArthur–Wilson model presented a diamet

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rically opposed perspective, one in which speciesrichness was the dynamic outcome of ongoingcolonization and extinction, in which the long-term geological history of the islands was con-sidered by many practitioners to be virtuallyirrelevant. Second, the model brought biologiststo see for the first time that global ecosystemsare effectively entirely insular, with habitat patchesand fragments of varying sizes representing astrong analogue of true marine islands. Thus,rather than seeing an entire continent made upof a small number of life zones (as ecologistsemphasized in the 1940s and 1950s), the ‘newecologists’ of the late 1960s and 1970s weredrawn to see almost infinite fragmentation on acontinent, in which local colonization, extinction,and re-colonization determined species richness.Stability in species richness and communitystructure came to be regarded not as the out-come of broad-scale, long-term historical pro

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cesses, but rather as the dynamic outcome ofcurrent processes that operate on a much brieferand more local scale. In the view of many bio

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logists, the MacArthur–Wilson equilibrium modelheld the promise that all aspects of speciesrichness were determined by processes that couldbe measured directly during a matter of years,rather than only inferred from data about eventsthat took place in the distant past.

In evaluating both the impact of theMacArthur–Wilson equilibrium model and itsvalue for guiding future research, it is import

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ant to recognize that the model has been used andviewed in many different ways. Some researchershave concluded that their study systems werefound to be in a dynamic equilibrium likethe one described in the MacArthur–Wilsonmodel (e.g. Simberloff & Wilson, 1970; Crowell,1986; most papers cited in Shafer, 1990), thus


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confirming its validity. Others have emphasizedthe value of the model in identifying andmeasuring important processes that influencespecies richness, especially when they havefound nonequilibrium conditions (Brown, 1971;Case & Cody, 1983; Heaney, 1984, , 1986; Lawlor,1986; Lomolino, 1986, , 1994). A few authorshave proclaimed that instances of nonequilib-rium constitute falsification of the model, andhave recommended that it be discarded (e.g. Sauer,1969; Gilbert, 1980; Williamson, 1989).

I believe that some of the diversity of opinionabout the utility of the model, especially thecritical opinions, is due to a misunderstandingof the manner in which models are best used— or at least the manner in which this modelis best used. A model is not simply a way togenerate a single prediction, or set of predictions.Rather, it is a deliberately oversimplified repres

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entation of how some system should functionif only a few major factors are at work. In thissense, it is a way of saying ‘all other thingsbeing equal, this is the outcome that should beexpected. Now,

why

do we

not

see the predictedresult?’ It is the deviation from the simplifiedprediction, and the reasons for the deviation,that are of interest, not the oversimplified pre

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diction itself. The prime example of such amodel is the Hardy–Weinberg equilibrium modelof population genetics. No one expects to findgenetic equilibrium in a population — and ifthey do find it, it is considered to be anuninteresting result. Rather, the Hardy–Weinbergmodel allows us to ask why the equilibriumcondition does

not

exist, and thereby we gain astronger understanding of the genetic dynamicsof a population. MacArthur & Wilson (1967,pp. 5–6) explicitly intended that their model beused in this manner, stating ‘A theory attemptsto identify the factors that determine a classof phenomena and to state the permissiblerelationships among the factors … substitutingone theory for many facts. A good theory pointsto possible factors and relationships in the realworld that would otherwise remain hidden andthus stimulates new forms of empirical research… If it can also account for, say, 85% of thevariation in some phenomenon of interest, itwill have served its purpose well.’ ‘A perfectbalance between immigration and extinctionmight never be reached. But to the extent that

the assumption of a balance has enabled us tomake certain valid new predictions, the equilibriumconcept is useful as a step beyond the morepurely descriptive techniques …’ (pp. 20–21).

Viewed in the context of this definition of anideal theoretical model, the reasons for thepopularity of the MacArthur–Wilson graphicalequilibrium model are evident. The MacArthur–Wilson model identifies two fundamentallyimportant processes that can be measured dir

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ectly, or that can be inferred from patterns ofdiversity. In so doing, it generates dozens ofinteresting and important questions. Such amodel cannot be ‘falsified’ any more than theHardy–Weinberg model can be falsified, becauseits prediction is not actually expected to be foundin the system under study — rather, the modeland the predictions that it generates are intendedas a means of asking important questions aboutwhy the system is

not

in equilibrium, therebyfocusing on process, rather than solely on pattern.

We might ultimately decide that such amodel is not useful or is misleading, and mightdiscard it for those reasons, but we should notdiscard it because we find that the predictionof equilibrium often is not borne out — it isprecisely the point that the ‘predictions’ are

not

expected to be found in nature that makes themodel valuable. In this context, the MacArthur–Wilson equilibrium model is unlikely ever to bediscarded; the experience of the last 30 years hasshown that it is too valuable a tool for dir

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ecting questions in research and for teachingstudents for it to be discarded as being ofno value.

This is not to imply, however, that the modelis perfect in the sense of always helping toidentify all of the most important questions tobe asked about the dynamics of species richness.As noted in other papers in this volume, thereare a number of ways in which the MacArthur–Wilson equilibrium model can be misleading(e.g. Fox & Fox, 2000; Lomolino, 2000a,b; Ward& Thornton, 2000). My own interests lead meto focus on issues that involve the evolution ofbiodiversity. As discussed above, the model wasformulated with examples in mind that involveprocesses that operate over short distances andbrief periods of time. What may we learn aboutthe utility of the model if we consider largerscales and longer periods of time? What happens


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to our view of species richness patterns if weconsider not years or centuries, but tens ofthousands to millions of years, and large oceanicarchipelagoes rather than forest fragments orsmall land-bridge islands? Are there processesother than colonization and extinction that areequally important? Are there questions that theequilibrium model does not lead us to ask — inother words, does the model mislead us under someconditions into asking fewer questions than weshould, and therefore mislead us into developingoverly simplistic understandings of the origins ofpatterns of biological diversity? It is these ques-tions about long-term and large-scale dynamicsthat this paper is intended to address.

SPECIATION, PHYLOGENESIS, AND PATTERNS OF SPECIES RICHNESS

Only a moment’s consideration is needed torecognize that patterns of species richness mustbe influenced by the process that produces spe-cies. It is ironic that MacArthur and Wilsonchose to explicitly exclude speciation from theirgraphical equilibrium model. They did so inspite of their familiarity with the topic andWilson’s previous development of a differentkind of model (the taxon cycle) that deals withspeciation explicitly (Wilson, 1961), but theychose to develop their graphical model (and mostof their general theory) ‘at the species level’(MacArthur & Wilson, 1967, p. 5), and referredto it as a ‘population theory’ (p. 6), contrastingtheir ‘biogeography of the species’ with histor

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ical biogeography (p. 183). To their credit, boththe 1967 monograph and MacArthur’s

GeographicalEcology

(1972) explicitly discussed speciation,principally in the sense of isolated populationsbecoming genetically distinct (this process ofdifferentiation from an ancestor in which thereis no diversification is termed ‘anagenesis’;‘phylogenesis’ is defined as differentiation withdiversification). Also, their 1963 paper included asection on phylogenesis (which they referred tounder the rubric of a ‘zone of radiation’), inwhich they predicted that archipelagoes ‘closeto the outermost range of the taxon’ would showthe highest levels of

in situ

adaptive radiation,demonstrating their awareness of and interest inthe issue. However, in the 1967 monograph, this

topic was mentioned rather briefly near the endof the volume, and no attempt was made toincorporate it into their graphical model.MacArthur (1972, p. 245) subsequently modelledlong-term control of species richness as includ-ing ‘immigration plus speciation’, implyingthat they were additive functions. In the mainportion of his text, he mentioned speciationonly in the context of this process creatingthe ideal circumstances in which to study com-petitive exclusion (pp. 71–74), and not in hisdiscussion of the dynamics of species richnesson islands (pp. 79–120). It should be noted thatthe earlier, but until recently overlooked, inde-pendent development of an equilibrium modelof island biogeography by Munroe (1948, seeBrown & Lomolino, 1989) included speciationmore explicitly and fully, but his inclusion ofthis process was lost for four decades, alongwith the rest of his contributions.

To return to the primary issue: Is speciation,and especially that outcome of speciation thatproduces diversification (i.e. phylogenesis), afactor that is likely to be an important processinfluencing current patterns of species richnessin island systems? To answer this question, wemust determine whether phylogenesis can takeplace over the same time scale as colonizationand extinction. If this is the case, we must askif it can be treated simply as another form ofcolonization, as MacArthur & Wilson (1963,1967) and MacArthur (1972, p. 245) implied.Finally, we must determine whether phylogenesiscan predominate under some nontrivial circum-stances, thus demonstrating that it deserves equalconceptual weight as a process influencingpatterns of species richness.

Most studies that have utilized the MacArthur–Wilson equilibrium model have measured orinferred colonization and extinction rates overperiods of time measured in days or years,sometimes referred to as ‘ecological time’. Veryfew studies have been done in a context thatwould permit measurements (or inference) over‘geological time’. The studies of the mammals ofSouth-east Asia, especially the Philippines, thatI and my colleagues have conducted have beendeveloped explicitly to address these questions.Our studies will form the bulk of my examples,and have strongly influenced my viewpoint onthis topic. The area is ideal in many respects



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because of the vast range of size (up to100 000 km

2

), geological age (up to 35 millionyears), and relative isolation of the islands(from a few to hundreds of km), and becausethe fauna is now reasonably well known. Over10 000 islands lie within Malaysia and Indonesia,and over 7000 in the Philippines (Fig. 1), theprimary site of the studies described here.

Part of the study area is the Sunda Shelf, thebroad, shallow continental shelf extendingsouth from the Asian continent that supportsBorneo, the Malay Peninsula, Palawan Islandin the Philippines, and thousands of othersmaller islands. Included are mainland areas,land-bridge islands isolated from the continentsince the most recent glacial episode (and theattendant period of low sea level) that endedabout 10 000 years ago, and land-bridge islandsisolated since the penultimate glacial episodeabout 165 000 years ago (Heaney, 1984, 1985,1986, 1991a, b). From analysis of the mammalfauna (excluding bats, which were investigatedby Heaney, 1991b), I inferred that extinctionwas fairly rapid after any given island was isol

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ated from the mainland (Fig. 2); roughly 50%of the fauna of nonflying mammals becameextinct during the first 10 000 years of isolationon an island of 10 000 km

2

. Subsequently, therate of extinction declined to a long-term averageof about 11% per 100 000 years, so that islandsisolated for 165 000 years (in the Palawanregion) still maintained fairly large and diversemammalian faunas (Fig. 2; Heaney, 1986). Itseems likely that the rate of extinction washighest soon after isolation and has now reacheda level much lower than the long-term aver

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age. None of these islands showed detectableevidence of receiving any colonists during thisperiod (i.e. there was no correlation of distancewith residuals from the species-area correlation).On the other hand, a group of tree squirrelsshowed evidence of phylogenesis having takenplace on Palawan Island (area = 11 785 km

2

)during its 165 000 years of isolation, adding oneindigenous species on the island (out of 23,which is about 4.4%), yielding a rate of about3% per 100 000 years (Heaney, 1986). The presenceof many morphologically distinctive popula-tions within single species in the Palawan region(many of which are recognized as subspecies;Sanborn, 1952) suggests that phylogenesis in the

fauna is continuing, so that 3% per 100 000years may be regarded as a long-term minimum.This single example suggests that phylogenesismight be as important as colonization or extinc

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tion in influencing the current dynamics ofspecies richness on these large, very old land-bridge islands. Off the north-eastern edge ofthe Sunda Shelf lie the majority of the Philippineislands (Fig. 1), isolated by sea channels exceed-ing at least 215 m deep (and often more), adepth that is quite unlikely to have been reachedat any time during the Pleistocene glacial episodes(Gascoyne

et al.

, 1979; Heaney, 1991a). DuringPleistocene periods of low sea level, groups ofthese islands would have merged together toform single larger islands. The configurationduring the most recent glacial episode is shownin Fig. 1. The geological age of these islandsvaries greatly, from Luzon which originated atleast 35 million years ago, to small islands suchas Camiguin that are composed largely ofactive or recently extinct volcanic cones (Hall,1996, 1998). All of these islands have indigen

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ous mammal faunas, regardless of how smallor geologically young they are. Moreover, onnearly every Pleistocene island, between 50 and85% of the nonflying mammals are endemic —an extraordinarily high value that indicates thatthe rate of colonization is likely to be verylow (Heaney, 1986; Heaney & Rickart, 1990;Heaney & Regalado, 1998). Examination of thenumber of species and the geological ages ofthese islands leads to the inference that suc

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cessful colonization took place roughly at arate of once per 250 000–500 000 years (Heaney,1986).

To summarize, these data, which are the onlydata for such long periods of which I am aware(but see also, e.g. Case & Cody, 1983; Berry,1984, 1998; Grant, 1986, 1998; Williamson, 1989;Wagner & Funk, 1995), indicate long-termrates for colonization by nonflying mammalsof once per 250 000–500 000 years to oceanicislands, for extinction of 11% per 100 000 yearson old land-bridge islands, and speciation of3% per 100 000 years on old land-bridge islands.Although these estimates must be treated asfirst, rough approximations, they suggest thatall three processes operate on a similar temporalscale in communities of mammals that occur onlarge, isolated island groups.


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Fig. 1

Map of the Philippine Islands, showing the modern islands in light grey, deep-sea areas in white,and areas exposed as dry land during the most recent Pleistocene period of low sea level in dark grey.Heaney

et al

. (1998).

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THE ROLE OF PHYLOGENESIS IN OCEANIC ARCHIPELAGOES

More recent data have provided another sourceof information about the processes that influ-ence species richness in the Philippine Islands.Preliminary analyses of the phylogenetic rela-tionships of one of the most diverse groupsof endemic mammals, the murid rodents, havenot yet produced a robust phylogeny, but theyhave produced a working hypothesis that clearlydemonstrates several important points (Fig. 3;Musser & Heaney, 1992; Heaney & Rickart, 1990;Rickart & Musser, 1993; Heaney

et al.

, 1998;unpublished data). These rodents (Fig. 4) includelarge animals (approximately 2.5 kg) that feed ontender young leaves in the tree-tops; small(approximately 120 g) elephant-shrew-like speciesthat feed almost exclusively on earthworms; anddozens of species that specialize on seeds, fruit,or insects, and which have a remarkably wide

range in body forms. My working hypothesis ofphylogenetic relationships (Fig. 3) indicates thatthere have been at least four, and perhaps asmany as six to eight colonization events thathave produced 56 species. Current data indicatethat of these, about 36 species are members ofa single large monophyletic clade that containsas much or more morphological and ecologicaldiversity (Fig. 4) than the more famous examplesof ‘adaptive radiation’ such as Darwin’s finchesin the Galapagos Islands or the lemurs ofMadagascar. In this case, we estimate that fromfour to eight colonization events have producedan average of 7–14 species, but one of these mighthave produced as many as 36 species (Fig. 3).As modern murine rodents originated no earlierthan the late Miocene, approximately 10 millionyears ago (Carleton & Musser, 1984, p. 356),we can take that as an upper limit on the timeduring which phylogenesis has taken place.However, as murine rodents are not recorded in

Fig. 2 Species richness of non-flying indigenous mammals on the mainland of the Malay Peninsula, on islandson shallow portions of the Sunda Shelf separated from the mainland about 10 000 years ago, and on islands inthe Palawan chain that were separated from the mainland about 165 000 years ago. Heaney (1986).


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the fossil record from South-east Asia or Aus-tralasia until the early Pliocene, approximately5 million years ago (Carleton & Musser, 1984,p. 358), that may be a more accurate estimatein this case. Given the estimate of four to eightsuccessful colonization events to the Philip-pines from the Asian mainland, this indicates arate of 0.4–0.8 successful colonization eventsper million years using 10 million years, or 0.8–1.6 successful colonizations events per millionyears using 5 million years as the base line. Itis interesting to note that Morgan & Woods(1986) estimated a colonization rate of once per0.4 million years for mammals to reach islandsin the West Indies, although about three-fourthsof those involved bats.

These basal colonization events to the Philip-pines from Asia almost certainly took place atdifferent times; in Fig. 3, the relative age of theclade is indicated by its position on the graph,

from oldest (most basal in murine phylogeny) onthe right to youngest (most derived) on the left.The oldest, represented by the genus

Phloeomys

,are Philippine endemic species that may bethe most basal living members of the rodentsubfamily Murinae (virtually all of their mor-phological characters that have been studied areeither autapomorphies or they are plesiomorphiesfor the subfamily; Musser & Heaney, 1992) andmay therefore have originated up to 10 millionyears ago. The largest clades are more derived,and probably fit into the 5-million-year periodmentioned above. The youngest, members ofthe highly derived genus

Rattus

(Musser & Heaney,1992), are likely to have differentiated recently,perhaps less than a million years ago. It isinteresting to note that there is a tendency fora correlation between the age of the clade andthe diversity of the clade, with diversitymeasured by number of species as well as by

Fig. 3 Phylogenetic relationships of the murid rodents of the oceanic portions of the Philippines, based ondata and assessment in Musser & Heaney (1992), topology in Heaney & Rickart (1991), data in Rickart &Musser (1993) and Heaney et al. (1998), and unpublished data. The dashed line indicates largely unknownrelationships to clades outside of the Philippines; question marks indicate uncertainty regarding individualnodes and their possible independent arrival in the Philippines. Brackets indicate the likely endemicmonophyletic clades that developed from single colonization events, and the number of species in eachclade (the four Rattus species probably have each arrived independently). A single poorly known species ofthe genus Crunomys on Sulawesi likely represents a colonization from the Philippines to Sulawesi, if thespecies does indeed belong in Crunomys (Musser & Heaney, 1992; Rickart et al., 1998).



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the ecological and morphological diversity ofthe member species (the oldest clade, made uponly of two species of

Phloeomys

, is an apparentexception to this pattern). The implication isthat the longer a monophyletic clade has beenin the Philippines, the more phylogenesis hastaken place. If this poorly documented butplausible hypothesis is true, extremely raresuccessful colonization of these islands from the

mainland has not been followed by extinctionas anticipated under the MacArthur–Wilsonmodel, but by progressive diversification. In thiscase,

in situ

phylogenesis has resulted in two toas many as 36 species per original colonizationevent, averaging 7–14 species per event, or about3–12 species of Philippine murid rodents permillion years, with the number of species increasingover time. Although these figures are rough first

Fig. 4 Heads of representative murid rodents from Luzon (not to the same scale). A, Archboldomysluzonensis (a generalized insectivore, 35 g), B, Phloeomys cumingi (an arboreal folivore, 2.1 kg),C, Rhynchomys isarogensis (a primary vermivore, 120 g), D, Rattus everetti (an omnivore, 250 g). FromHeaney et al. (1998).


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approximations (in particular, they lack docu-mentation through a fossil record), the examplesof ‘adaptive radiation’ cited above, and hundredsof others involving mammals, birds, reptiles,insects, and plants from archipelagoes aroundthe world (e.g. Heaney & Ruedi, 1994; Wagner& Funk, 1995; Grant, 1998; Whittaker, 1998),lead me to believe that such

in situ

phylogenesisis typical in oceanic archipelagoes.

CAN PHYLOGENESIS BE SUBSUMED AS ‘ANOTHER FORM OF COLONIZATION’?

The potential exclusion of phylogenesis fromdiscussion of the important processes that influ-ence patterns of species richness must rest ontwo issues. First, if it were the case that colon-ization and extinction always occur at rates thatare so much higher than phylogenesis that theysimply swamp or eliminate any potential geneticdifferentiation, then phylogenesis would be unim-portant. This is clearly untrue. In many biotason large, old land-bridge islands, as discussedabove, phylogenesis can take place on the sametemporal scale as colonization and extinction,and phylogenesis may produce more than 10times as many species as direct colonization inlarge, old, oceanic archipelagoes.

Second, if phylogenesis does not interact

independently with colonization and/or extinc-tion (or with isolation and area), then it canaccurately be viewed as a form of colonizationand can be subsumed under that heading. Thissecond condition also is unlikely to be true.Consider the case of a group of islands off thecoast of a mainland, initially uninhabited bythe focal taxon, that begins to undergo coloniza

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tion, with the following hypothetical processesoperating (Fig. 5). For islands that are verynear to the mainland, colonization rates will beso high that few extinctions take place becauseof the ‘rescue effect’ (Brown & Kodric-Brown,1977). With a small increase in isolation, themeasured rate of colonization (defined as thearrival and establishment of a species not atthat time present on the islands) will actuallyrise, as fewer populations will be ‘rescued’, andtherefore some species will colonize repeatedlyand become extinct repeatedly. As distanceincreases further, the rate of colonization willdrop off, reaching the level of extreme rarity,then being absent altogether. In the MacArthur–Wilson equilibrium model, as shown in theirfamous graphical model and adopted by mostsubsequent authors, this would be virtually theend of the story — species richness would bevery low on a distant island unless the islandwas so large that the rate of extinction wassubstantially lower than the rate of colonization.

Fig. 5 Conceptual model of the rate curves for colonization and phylogenesis on a series of islands ofvarying area and distance from a species-rich source. The rate of phylogenesis should vary with island size;only two of an infinite series of potential curves are shown. The approximate position of Nm = 1 (geneflow equal to one individual per generation) is shown as ‘A’.



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In this model, in which speciation is insignificant,each species present in the distant archipelagowould represent a separate successful colonization.

Consider next what might happen if phylo-genesis also takes place, as MacArthur andWilson proposed (but did not develop) undertheir rubric of a ‘zone of radiation’. On islandsnear to the mainland where the rate of colon

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ization is very high, phylogenesis would bevirtually impossible, as gene flow rates wouldbe so high as to swamp out any genetic changethat takes place on the islands (as on eithervery near islands, e.g. Lomolino, 1986, 1993,1994; or on recent land-bridge islands where geneflow was recently high, Case & Cody, 1983). But,as isolation increases to the point that geneticdifferences can persist (especially on islands offthe edge of the continental shelf; Case & Cody,1983; Heaney, 1986; Berry, 1998), the potentialfor phylogenesis (and anagenesis) increasesdramatically (Fig. 5). At moderate levels ofisolation, direct colonization may still accountfor more species than phylogenesis, but as isola-tion increases still further and colonizationbecomes an extremely rare event (i.e. where geneflow (Nm) is much less than one per genera-tion, as in the oceanic Philippines; Peterson &Heaney, 1993; Walsh

et al

. unpublished data),phylogenesis will begin to predominate. Becausethe maximum possible rate of phylogenesis seemsunlikely ever to reach the maximum rates ofcolonization achieved under optimal conditions,I model these curves as having conspicuouslydifferent maxima. This is essentially the sameprediction made by MacArthur & Wilson (1963,1967; see also Whittaker, 1998, pp. 110–111)under the rubric of the ‘zone of radiation’, asdiscussed above, but which they did not incor-porate into their equilibrium model. (The complexmechanisms of phylogenesis are not discussedhere. Among Philippine mammals, it is likely thatboth habitat vicariance and repeated inter-islandcolonization are involved: Heaney & Rickart,1990; Peterson & Heaney, 1993; Rickart

et al.

,1998; see also Grant, 1998a,b).

In addition to distance, it is likely that thesize of the oceanic archipelago will impact theinteraction between phylogenesis and coloniza-tion. Consider the case of a set of islands whichvary substantially in isolation and area, andtherefore in colonization and extinction rates

as well (Fig. 5). On a large island (or withina large archipelago), the rate of phylogenesisshould be virtually nil where the rate of colon

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ization exceeds one individual per generation(the approximate interval at which Nm = 1 isshown as ‘A’ in Fig. 5). Thereafter, as the rateof colonization declines and progressively fewerspecies are added directly to the island pool,the rate of phylogenesis should increase, andshould exceed the rate of colonization over somesignificant range of distances. Small islands arelikely to reach saturation from colonization morequickly than are large islands, and opportunitiesfor phylogenesis are likely to be few. The twocurves shown in Fig. 5 could be generalized toa family of possible curves for islands and archi-pelagoes of varying sizes and degrees of com

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plexity. The actual rate of phylogenesis is likelyto vary substantially among taxa, but the generalpattern should be found in all taxa.

The prediction that most species will originateby

in situ

phylogenesis (rather than by directcolonization) in large, old, stable archipelagoesthat are near the upper limits of their colon

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ization abilities (Whittaker, 1998, pp. 110–111),can be developed further in a manner that dis-tiguishes single endemic species from endemicclades. A conceptual model (Fig. 6) shows thepredicted pattern. On islands near a source,colonization will take place so rapidly that allspecies will be nonendemic species, i.e. thosefound in the source area. At the point at whichsource taxa reach the archipelago less oftenthan once per generation on average (roughlyapproximated as Nm less than 1.0, shown as‘A’ in Fig. 6), some populations will undergoanagenesis, and endemic species will be present.I predict that there should be some range ofcolonization rates at which anagenesis takes placebut at which colonization still contributes asignificant number of species, leaving little or noopportunity for the evolution of new species by

in situ

speciation; this is shown as the regionbetween ‘A’ and ‘B’ in Fig. 6. At still lowerrates of colonization from the source area,phylogenesis within large, complex archipelagoesshould begin to take place; this is the area tothe right of ‘B’ in Fig. 6. On large, isolated

denovo

oceanic archipelagoes that are geologicallynew, or that have experienced a recent significantincrease in size, I predict that there would be


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species of several types: a few nonendemicspecies (recent invaders from the source area;the area below line 1); a set of endemic specieswhose sister taxa are present in the source area(the area between lines 1 and 2); and a fewspecies whose sister-taxa are other endemicspecies within the archipelago (i.e. small endemicclades; the area between lines 2 and 3). Onprogressively older archipelagoes, I predict thatthese same sets will be present, as well as speciesthat are members of larger, older endemic clades(between lines 3 and 4), and on still olderarchipelagoes there should be still larger andolder clades (between lines 4 and 5). I predictthat, typically, the oldest clades within a giventaxon (in this case, the family Muridae) will bethe most speciose.

Finally, in island groups so isolated that nocolonization takes place (e.g. there are no nativerodents in the Hawaiian islands), there are nospecies to undergo phylogenesis, and so bothendemic and nonendemic species will be absent.In other words, both colonization and phylo-genesis curves will reach zero at the same point.

I conclude that phylogenesis interacts withcolonization in a complex manner, having thegreatest impact where colonization is rare (thoughnot absent) and being influenced by degree ofisolation and by island (or archipelago) area(and complexity) in a manner different to col-onization. Because of this, and contra theequilibrium theory of MacArthur and Wilson,phylogenesis cannot be viewed as a processthat is simply additive to colonization; rather,

Fig. 6 Conceptual model showing the development of species richness on large islands or archipelagoesthat experience varying rates of colonization due to varying degrees of isolation. On islands near a species-rich source that initially lack the study taxon, all species will be present through direct colonizationbecause high rates of gene flow will swamp out any potential speciation; thus, no endemic species will bepresent, but many non-endemics will be present. As the average rate of gene flow drops belowapproximately the level of Nm = 1 for the study taxon (point A), anagenesis will begin to take place, andendemic species will develop, although they will be outnumbered by non-endemic species. These endemicspecies (between lines 1 and 2) will have their sister-taxon in the source area, not on the island/archipelago. As colonization becomes still less frequent, and as time passes, phylogenesis will produceendemic clades in which the endemic taxa have their sister taxon on the island/archipelago, not in the sourcearea (species between lines 2 and 3). As more time passes, the oldest clades will become progressively morespeciose (between lines 3 and 5).



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phylogenesis must be given equal conceptual weightin any model that purports to predict patternsof diversity or that serves to aid investigators inasking all of the relevant questions about theorigin and maintenance of biological diversity,especially in large insular systems.

IS EQUILIBRIUM A LIKELY OUTCOME IN ISLAND ARCHIPELAGOES?

The preceding discussion posits that a large,isolated archipelago might be expected to experi

-

ence gradually increasing species richness dueto rare colonization events and subsequentphylogenesis. As species richness rises, onemight expect the rate of extinction to rise, dueto the same ecological factors that MacArthurand Wilson discussed (see also Whittaker, 1998,pp. 136–137). This could result in an equilib-rium condition which is parallel to that in theMacArthur–Wilson model, in which colonization,phylogenesis, and extinction combine to producea dynamic condition of turn-over, albeit onethat operates on a vastly longer time-scale thanMacArthur and Wilson discussed. Indeed, a tri-variate equilibrium might seem inevitable, giventhe longevity of such island archipelagoes —parts of the Philippines, for example, haveexisted as islands above the sea for at least 35million years (Hall, 1996, 1998).

Indeed, one might reasonably argue that atrivariate model would be most effective if con-structed as an equilibrium model and used inthe manner I described above for the MacArthur–Wilson model, namely to establish points ofreference and as an aid to asking informativequestions. Lomolino (2000a) briefly discussedthe need for such a model, and graphed thecircumstances under which phylogenesis mightpredominate and therefore require a trivariate,rather than bivariate, equilibrium model. Hisgraphical presentation, and those included here,point the way toward development of such amodel, but rigorous mathematical and graphicaldevelopment of such a model remains to be car-ried out.

Development of such a trivariate model willcertainly have great heuristic value. However, Ipredict that such trivariate equilibrium condi-tions will actually be found to exist only quite

rarely on islands in nature. The oceanic archi-pelagoes where such conditions might developare geologically unstable; they are virtually alwaysamong the most geologically dynamic places onearth, whether in the Antilles, the GalapagosIslands, or in South-east Asia. The geologicalprocesses that drive these systems — plate tec-tonics, volcanism, etc. — are processes that takeplace on the same scale of time as colonization,phylogenesis, and extinction within such archi-pelagoes — tens of thousands to millions ofyears. In the Philippines, during the last three tofour million years, virtually the entire southernpeninsula of Luzon has arisen; Sibuyan andCamiguin islands have come into existence; and,in all likelihood, some previous islands havesunk beneath the sea. That being the case, the‘equilibrium point’ for a given archipelago willchange as rapidly or more rapidly than thebiological processes can adjust. The appropriateconceptual model thus becomes one of dynamicdisequilibrium, in which species richness is alwaysslightly out of phase with the equilibriumpoint because of the constantly changing phys

-

ical conditions, sometimes exceeding saturation,and at other times below it (Heaney, 1986;Whittaker, 1998, pp. 141–143). At times of under-saturation, phylogenesis may especially experi-ence rate increases, adding further to the dynamicaspect of interaction among the three processes.

On a shorter time-scale, repeated changes insea level during the Pleistocene associated withepisodes of continental glaciation add anotherdynamic aspect, as islands such as those in thePhilippines (Fig. 1) experienced huge and repeatedchanges in area due to periodically mergingwith and separating from islands nearby, whiletemperature and rainfall patterns shifted in concert(Heaney, 1991a). These short-term changes arelikely to drive changes in rates of extinction, col

-onization, and phylogenesis (through vicariance).

Large-scale continental island-like habitats maybe expected to show similar dynamic disequilib-rium, again because of the intrinsic instabilityof the places where island-like conditions develop.Mountain ranges are the premier examples ofsuch island-like conditions, at least on a largegeographical scale, and mountain ranges are nowknown to result largely from the same kinds oftectonic forces that are responsible for thedevelopment of island arcs, rising and eroding


72 L. R. Heaney

© 2000 Blackwell Science Ltd, Global Ecology & Biogeography, 9, 59–74

in much the same fashion as oceanic islands.Pleistocene variation in global climate thatcaused changes in sea level that affected oceanicislands like the Philippines also affected mountainchains because of the changes in temperature. Inthe Rocky Mountain area of North America,for example, changes in temperature and precip-itation during glacial periods caused wholesalechanges in the distribution of the conifer forestthat now forms the classic habitat for mountaintopsin the region, allowing such habitat (and themammals associated with it) to drop to lowerelevations and disperse widely over much of theSouth-west (Grayson, 1993).

CONCLUSION

Clearly, because all species ultimately originatethrough phylogenesis, any discussion of speciesdiversity must recognize phylogenesis in at leastsome fashion. More specifically, any attempt tomodel the processes that influence patterns ofspecies richness in island-like conditions mustbe cognisant of the potential for rates of col-onization and extinction to operate on a time-scale that is equivalent to those under whichphylogenesis and major geological and climaticchange may take place. Because much of thebiological diversity on earth exists on tropicalisland archipelagoes, and much of the remain-der in continental montane areas, any generalmodel must therefore acknowledge and includephylogenesis.

Considered in this light, the MacArthur–Wilson equilibrium model must be judged to beinadequate. For this reason, along with the otherscited by authors of other papers in this issue,I believe that it is time to develop more fullythe concept of dynamic change that has madethe MacArthur–Wilson equilibrium model soimportant in evolutionary ecology. It is anexciting prospect that calls for the same kindof creativity shown by MacArthur and Wilson,expanding into crucial and complex concep-tualization of the origin and maintenance ofbiological diversity. I predict that the originalMacArthur–Wilson equilibrium model will remaina primary cornerstone of the new development,not discarded or superceded, but instead forminga crucial component of future conceptual develop-ment. Its strengths — clarity, simplicity, and ability

to induce inquisitiveness — should continue tobe the hallmark of island biogeography.

ACKNOWLEDGMENTS

A brief version of this paper was initially pre-sented at the Seventh International TheriologicalCongress, in a symposium on island biogeo-graphy of mammals organized by Ticul Alvarezand myself; I thank Ticul for his collaborationand encouragement, and the organizers of theITC for the opportunity. Danilo S. Balete,James H. Brown, Paul D. Heideman, Mark V.Lomolino, Thomas J. McIntyre, Victor Sanchez-Cordero, Blas R. Tabaranza, Jr., Richard W.Thorington, Jr., Ruth B. Utzurrum, and espe-cially Eric A. Rickart, have made substantialcontributions to my thinking on this topic, andI am grateful to them all. This paper benefitedgreatly from insightful comments on earlier draftsby John Bates, Mark Lomolino, Eric Rickart,Joseph Walsh, Robert Whittaker, and an anonym-ous reviewer. Permits for field work in thePhilippines were provided by the Protected Areasand Wildlife Bureau of the Department of Envir-onment and Natural Resources. This researchhas been supported by the National ScienceFoundation (BSR-8514223), the Smithsonian Officeof Fellowships and Grants, the Marshall Field,Barbara Brown, and Ellen Thorne Smith Fundsof The Field Museum, and the John D. andCatherine T. MacArthur Foundation (90–09272 A).

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