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EQUILIBRIUM THEORYOF ISLAND BIOGEOGRAPHYAND ECOLOGY

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Daniel S. SimberloffDepartment f Biological Science, Florida State University, Tallahassee, Florida 32306THE BIOLOGICAL IMPORTANCE OF ISLANDSOceanic islands and archipelagoes are intrinsically important to biologists; 5%ofthe land surface of the earth is insular, and if South America, which has been anisland throughout most of its existence, is included the figure rises to 19%.Signifi-cant portions of the evolutionary histories of manyeconomically and biologicallyimportant species occurred on oceanic islands, and if the earth were not liberallysprinkled with isolated bits of land in addition to the "world continent," its biotawould be much poorer.

But the intrinsic importance of islands, scientific or economic,has not inspiredthe intense research in island biogeography which justifies this review of recentadvances. Rather it is the realization that oceanic islands are paradigms for geo-graphic entities ranging in size from tiny habitat patches (52, 53) to continents (86,92, 112) or even the entire earth (74). It is almost a platitude that Darwinsobserva-tions in the Galapagos Archipelago and Wallaces in the MalayArchipelago crystal-lized the then nascent concept of organic evolution by natural selection (13, 110),and manyother classical evolutionary advances rest originally on insular observa-tions. Because slands are so clearly isolated from other land masses, island popula-tion data contributed heavily to the realization that most speciation is allopatric(54). Wallaces Malaysian observations allowed strong inferences about changingsea levels, past land connections, and the position of a line separating two greatbiogeographic provinces (110). Insular isolation is important ecologically becauseit allows us to be virtually certain that an organism encountered on an island is atrue nesiote. Consequently, problems in Communitytructure and function, such asthe distribution of individuals into species or the trophic relationships among opu-lations, are more eadily attacked in an island setting; any organism found there isassuredly a memberof the biotic community.

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162 SIMBERLOFFThis first salient island characteristic, isolation, leads to the second, biotic depaup-

erization. The relative simplicity of insular biotas allows interactions among opula-tions to be deduced which would be obscured in a more complex mainland context.For example, that addition of a predator trophic level can impart stability to anotherwise unstable herbivore-plant association (63) is indicated in the simplified IsleRoyale ecosystem, in which a moosepopulation feeding on vegetation was stabilizedby the addition of wolves. Suchclarity wouldbe diffacult to achieve on the mainland,where alternate food sources and other agents of mortality abound. Similarly,regional pest control schemes are frequently tested on islands because e~cacy andthe presence of unexpected ide effects are moreeasily assessed on simplified insularcommunities.That release of sterile male .,icrew-wormscould eradicate this dipteranlivestock pest over wide areas was first confirmed on tiny Sanibel Island and thenon Curacao (3). Potential ecosystem dis~uption through use of a molluscicidecontrol the snail vector of the cattle liver-fluke was tested on the small island ofShapinsay, in the Orkneys (39).

From an evolutionary standpoint the importance of insular depauperization hasbeen to allow .the continued existence of forms which would have been selectivelyeliminated through various sorts of interactions in a richer biota. The depauperiza-tion is generally not random,but rather, poorly dispersing species are differentiallyabsent, causing island biotas to be "disharmonious" n their composition, i.e. overlyrich in certain groups and disproportionately poor in others, vis-fi-vis the mainland(6). Large predators, for example, are relatively rare on islands and a major main-land selective pressure is consequentlyabsent or severely reduced. One esult of suchslackened selection has been the frequent evolution of bizarre plants and animalson islands (6), while another is the notorious fragility of island communities, heirrapid destruction with the arrival of,Western man, and the great numberof extinc-tions of island endemics upon interaction with introduced species (6, 22). But totheoretician looking for nomothetic importance in his observations, the key featureof evolution in a depauperate communitys that co-evolutionary selective pressuresare easier to deduce and the rek~)ons for a species particular morphology,behavior,and general niche characteristics more easily determined. The very introductionsthat endanger island communities may yield information on such phenomenaasecological release, species replacement, and niche shift (60) muchmore quickly andclearly than on the mainland.Anypatch of habitat isolated from similar habitat by different, relatively inhospi-table terrain traversed only with difficul~:y by organisms of the habitat patch maybe considered an island; in this sense much f the biotic world is insular, for habitatsare often not homogeneousbut rather are arranged as patches in a crazy quilt.Consequently, any model of island biology should be relevangto small scale, localsystems, as well as to larger ones. General theories of the essential insularity ofmainland communitydynamics (40, 52, 53) remain untested except for a groupcaves as islands colonized by arthropod:~ (10) and a single application to antstruly oceanic islands (55); however,aspec:ts of an hypothesis originally proposedforoceanic islands (59, 60) have been tested with somesuccess in the field on several


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EQUILIBRIUM ISLAND BIOGEOGRAPHY 163"habitat islands": fresh water colonized by assemblagesof both plants and animals(41, 62, 87), artificial and natural substrates colonized by aquatic (5, 70) and marine(68, 79) organisms, caves for both aquatic and terrestrial animals (9, 11, 109),montaneareas for birds (108) and mammals4). Such clearly insular microhabitatsas cowpats, sand dunes, and bromeliad containers can also be viewed as islands.THE ECOLOGY OF ISLAND COMMUNITIESThe Equilibrium Theory of lsland BiogeographyA decade ago, Preston (72) and MacArthur & Wilson (59, 60) revolutionizedbiogeographywith the suggestion that the biota of any island is a dynamicequilib-rium between immigration of newspecies onto the island and extinction of speciesalready present. Species numberwould hen be constant over ecological time, whileevolution would act gradually over geological time to increase the equilibriumnumber f species (1 i9). Althougha few voices (50, 78) still call for an idiographicapproach to biogeography, with each island examined as a unique locus of speciesassembled or idiosyncratic reasons that can tell us little about other islands, theequilibrium hypothesis has been experimentally confirmed for oceanic islands,proved useful in interpreting manyother insular situations, and spawned mass ofresearch which has given biogeographygeneral laws of both didactic and predictivepower. It has been both a partial cause and a major result of two contiauing trends:an increasing emphasis on extinction as a common, ocal, ecologically importantevent, rather than a rare, global, evolutionary one, and a shift of focus from theindividual and the species to the local population as the fundamental unit in bothecology and evolution (91, 93).

The oceanic island data originally available to test directly the basic assertions ofthe equilibrium theory, i.e. that "turnover" of species constantly occurs but numberof species remains unchanged, were consistent with the hypothesis but did notconfirm it. The colonization of Krakatau occurred without a preeruption census andinvolved few and differentially exhaustive monitorings, while the data on plants ofthe Dry Tortugas proved only that natural extinction occurs frequently in thatarchipelago. Much tronger evidence has recently been published.A direct test was performed by Simberloff & Wilson (88, 94, 95, 120), who"defaunated" a group of six small red mangrove slands in Florida Bay by methylbromide ent-fumigation, while leaving two similar islands as untreated controls.These islands were different distances from the main Florida Keys, and, becausethey had no supratidal ground, their animal communities consisted of only 20-50arboreal arthropods (of hundreds in the Keys species pool), primarily insects. Ex-haustive censuses were made before the defaunation and periodically afterwards.The numbe/"of species remained unchangedon the control islands, though composi-tion changedcontinually. That the dynamicequilibrium model s generally accuratewas ndicated explicitly by the following facts:1. Onall islands but the most distant, species number ose slightly above thepredefaunation number, then fell and oscillated about that number. The characteris-


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164 SIMBERLOFFtic overshootwas nterpreted as causedby the small populationsizes in the earlystages of colonization, allowingmore pecies to coexist than wouldbe possible ona more rowded,untreated island. On he most distant island, the relatively fewerspecies that wereable to invadeearly buil.t up abnormallyarge population izes inthe absenceof competitorsand predators, eliminating the overshootand retardingattainmentof the equilibrium.2. Theequilibria were dynamic; urnover rate at equilibrium on an island 200mfrompotential source areas was0.5-1.0 species (~ 2% f the biota) per day. Mostturnover was produced by propagules obliged to be transients on these simpleislands for wantof suitable food or habitat, but extinctions of bona ide mangrovecolonists were requently observed.If the mathematics f the simple equilibrium modelare manipulatedappropri-ately, further qualitative predictionsare generated or testing against the results ofthe mangrovesland experiment. Both Simberloff (88) and MacArthur56)shown hat the samequalitative predictions hold if the original model,based onequivalence f all species n the species pool in abilities to disperse to and maintainpopulations on islands, is mademoresophisticated by assuming ifferent invasionand colonization apabilities for different species.First, it is clear fromeven he simplest equilibriummodel hat distant islandsought to have fewer species than near isl~mds,and that small islands ought to havefewer species than large ones (Figure I). The experimentalmangroveslands con-form o this pattern, but since anynatural historian waswell aware ifty years before

nearf~r

DISTANCEFFECT

-- small~-- large

nearNUMBERF SPECIES

AREA FFECT

NUMBER F SPECIES

Figure 1 An island biota is an equilibrium i:a ecological time between immigration of newspecies and extinction of those already present. (Left) Distance effect; a near island has largerequilibrium numberof species (~) and turnover rate (.~). (Right) Area effect; a large islandhas larger ~ and smaller ~.


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EQUILIBRIUM ISLAND BIOGEOGRAPHY 165the equilibrium theory that distant islands were depauperate and that large areastended to have more species than small ones, this observation should not be con-strued as yielding strong support to the details of the equilibrium model. Otherinterpretations maybe given to both the distance and area effects.

However, he dynamicnature of the modelallows further, less intuitively obviouspredictions about rates and time scales. For example, the equilibrium model equa-tions can be rearranged to show hat distant islands not only ought to have fewerspecies but also should take longer to reach any fraction of the equilibrium numberfrom a sterile or defaunated condition. MacArthur& Wilson suggested 90%as astandard fraction, and t0.9o, the time required to reach 90%of equilibrium, as thestandard time period for comparison of colonization episodes. Diamond 19) hasrecently generalized the concept of return to equilibrium from a perturbed state toinclude perturbations, such as area reduction or mass invasion by a group of immi-grant species, resulting in an islands being oversaturated with species, in additionto those (like defaunation) that leave it undersaturated. The generalized intervalproposed for the asymptotic return to equilibrium is the "relaxation time," (tr),which he suggests should be the time required for the displacement from equilibriumto fall to 1/e (36.8%) of the value caused by the perturbation. This time intervalis a natural one only if immigration and extinction rates are constant, and seemsnot to constitute a conceptual advance over to.9o. In any event, on the defaunatedmangroveslands t0.9o wasconsistently greater on the more distant islands, in accordwith equilibrium theory.

The theory yields a prediction for the shape of the colonization curve of numberof species vs time, St = ~(1 - e-tTt), whereSt is the numberof species at time t,~ is the equilibrium numberof species, and G is a constant. [A modification of thetheory to allow for differences in invasion and survival proficiencies among peciespredicts a sumof terms, each of whichhas an equation formally similar to the aboveone (88). The summed urve is shaped like the MacArthur-Wilson urve, asymptoti-cally approaching an equilibrium.] The colonization curves of the experimentalislands were all consistent with this mathematical shape except for the small over-shoot, but could not be construed as validating the theory because of the largestandard deviation of the predicted curve (88).

Finally, an equation can be dedu~ced,relating to.9o, ~, and equilibrium turnoverrate ~" for any island, to.9o = 1.15 S/X. When bserved values of ,(" and ~ for thedefaunated islands were inserted into this equation, the resultant to.9o waswithin therange of the observed t0.9o allowed by the errors of approximation or all variables.

Hubbell (42) recently constructed a Laplace-transformed linear systems versionof the equilibrium model that allows inferences concerning whenan islands speciesnumber hould be oscillatory even with constant propagule invasion rates. In partic-ular he demonstrated mathematically that for any distance from a source area thereis a range of island sizes that will have oscillatory species numbers,and that thegreater the distance from the source area, the narrower the area range for oscilla-tions. This is compatible with the Simberloff-Wilson xperimental data, in which hemost distant island showed no overshoot. However, this is not surprising sinceHubbells model assumes competition to increase as population sizes increase, and


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166 SIMBERLOFFSimberloff &Wilson(88, 94) explain the c, vershoots or lack thereof as consequencesof observed population increases. Hubbells model goes further, however, and treatsthe results of an oscillatory invasion rate a~ well as the fluctuations in species numberto be expected in archipelagoes. Although he defaunated islands provided no datato test this aspect of the model, Simberloff has recently created a series of ar-chipelagoes by dividing large mangrove ~slands into groups of small ones, and asdata from this experiment are gathered they may be compared to Hubbells predic-tions.

Heatwole & Levins (37) have reexamined the colonization data for the defaunatedislands and have shown hat, if the arthropod colonists are divided into broad nichetypes (detritus-feeders, herbivores, wood-borers, etc), the defaunated islands notonly gradually achieved their original numberof species, but also their originalbroad trophic structure, or distribution of species into the different niche types. Thisobservation is exciting, for it implies tb.at the groups on these islands are trueinteracting communities, and not just haphazard assemblages which arrived andwere extinguished fortuitously. Although the arboreal red mangrove system doesnot appear to be one in whichspecies ini;eractions are particularly pronounced, itis possible that evolution has gradually molded the source fauna so that the man:grove resource is utilized in somecanonical, nearly optimal way, with the result thatrandomsubsets of this source biota are likely to be rather close to the canonicalstructure.

MacArthur(56) demonstrated that a group of competitors would be expectedevolve so as to minimize he squared deviation of resource usage from availability,while May 63) has shown that the trophic relationships amongany collectionspecies are constrained within severe limits if the collection is to be stable. Ifconsiderations such as these force even the initial colonists to fall within a circum-scribed set of distributions into niche types, continued immigration and extinctionwould be expected to produce ever more highly coadapted sets of species. Forwhenever urnover results in a more stable group of species, that group is expectedto persist longer than its predecessor. Wilson&Simberloff(95, 119) termed he initialrelatively stable numberof species the "noninteractive equilibrium," and viewed hesequence of increasingly coadapted groups as "interactive equilibria" leading to an"assortative equilibrium" with a lower turnover rate. They also proposed that theinteractive equilibria will be successively larger on the grounds that the componentspecies in a more highly coadapted cornplex might be expected to have smallerniches. MacArthur(56) and May 63) showed that minimization of squared unusedresources is indeed facilitated by morespecies, but that a limit to species packingis set by increased probability of extinction as niches are narrowed.

Data gathered on birds and plants of the Channel Islands off Southern Californiaprovide yet another test, both direct and indirect, of the equilibrium theory of islandbiogeography. The clearest evidence for its essential truth is that presented byDiamond14), whoshowed hat numberof species of land an d freshwater birds (foreach island but a fraction of the California. pool) changedonly slightly between1917and 1968, while composition changed naarkedly; turnover was between 0.3 and1.2% per .year, and these are extreme minima since immigration and extinction


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EQUILIBRIUM ISLAND BIOGEOGRAPHY 167probably occurred between the two censuses without having been recorded. In workwith just a single taxon (birds, in this study), one must alwaysconsider whether theobservations are not an artifact of the taxon, or whether, for example, the entirefauna of these islands might not be in equilibrium. Other than major changesrecently wroughtby man 49), there is no reason to disbelieve the implication thatthe islands are in equilibrium, and birds probably constitute such a large, distinct,and unified ecological group that observations on birds alone are a valid test of theequilibrium model. Johnson (49) believes that avian turnover in the ChannelIslandsis not nearly so high as Diamond tates, presumably because one or both censuseswere deficient. But since Diamonds igures are probably underestimates for reasonsalready given, his claim of considerable turnover in ecological time is almost cer-tainly correct.

Figure 1 shows hat, all other things being equal, one wouldexpect higher relativeturnover rates the smaller the island and the nearer the island to the mainland.Diamondsdata for Channel Island birds show no correlation between avian turn-over and island size or isolation. If the turnover rate data are in error, as Johnsonclaims, this finding need not contradict the equilibrium theory. Diamond ffers twoother explanations. Thefirst is that the mainland-islanddistances in this systemareso small (61 miles maximum)elative to the flight capabilities of the birds that allislands are equally attainable; Johnson points out that somemembers f the Califor-nia species pool would be limited by distances in this range, but concurs withDiamondscontention so long as it is limited to those species that are likely toattempt island colonization at all.Diamonds econd suggestion is that the effects of distance and area on turnoverrates and equilibrium numbersmay be masked if islands differ in other importantparameters. Since 1835, over a century before the publication of the equilibriumtheory, it has been observed that numberof species tends to increase with area,whether one examines mainland quadrats or an archipelago of islands (21), buthas only been recently that area per se has been accorded a role in the determinationof species number 91). Rather, area has been thought to act primarily or exclusivelythrough habitat diversity; as area increases, so usually does the numberof h~bitats,each with its complementof species. Johnson et al performed multiple regressionanalyses of plant species number on the Channel Islands plus adjacent mainlandareas (46). Although area was the single best predictor of species number, theyviewed his as a result of its high correlation with ecological diversity, and elevationrange and latitude (indicators of ecological diversity and ecological richness, respec-tively) contributed significantly to the prediction of species number.So did isolationof the islands, moredistant islands having fewer plant species, all other things beingequal. This last observation is consistent with equilibrium theory predictions, butsince no data on turnover were presented the study cannot be considered a directtest of the theory.Power (71) constructed a path diagram to model the regulation of numbersplant and bird species on the Channel Islands, again using multiple regression asa test for significant effect of various environmental ariables. His results for plantspecies agreed with those of Johnson t al, except that island isolation had little effect


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168 SIMBERLOFFin his analysis. Plant species numberwas the best predictor of bird species number,although insular isolation also accounted for significant variation in numberof birdspecies. So Diamondshypothesis--that t.urnover rates do not correlate with areaand distance as predicted by the equilibriu:m model because an even more importantfactor, ecological diversity, varies somewhatndependently of them--is consistentwith available data:

Before leaving the Channel Islands I should point out a shortcoming of multipleregression analysis as a test of the equilibrium model. At best, such an analysis canrender the model plausible, if species, nunaber correlates appropriately with islandisolation and area. But regression cannot demonstrate causality; we have alreadyseen that a correlation between area and species number can be (and has been)construed as demonstrating the effect of habitat diversity, without reference to anydynamicequilibrium, while fewer species on more distant islands can be interpretedas the result of the distant islands not yet being full. Furthermore, a path diagramsuch as Powers, even if based on a stepw~se multiple regression analysis, is subjec-tive. Without our own biological insights we could as well have viewed bird speciesnumberas a determinant of plant species number, than vice versa. Paine (69) andJanzen (44) have done something very similar in ascribing numberof species introphic level to amountof predation on that level. A regression analysis might alsoomit subtle environmental variables important to the organismsunder investigation.Diamondswork, on the other hand, constitutes an objective test of part of themodel; turnover was demonstrated.

A slight deductive step from the equilibrium theory provides a means by whicharea mayaffect species number completely independently of habitat diversity. Ifextinction is, in fact, a commonvent, its frequency should increase as populationsizes decrease. That is, on a small island with lower carrying capacities, any extantpopulation will likely be extinguished morequickly from either interactive or nonin-teractive causes than would a conspecific population on a larger island with largercarrying capacities; this is the basis for the raised extinction curve in Figure 1.MacArthur& Wilson (60) claim that for every combination of per capita birth (k)and death (/x) rates there is some carrying capacity (K) such that a propagulelanding on an island with carrying capacity greater than K is much ess likely tobe extinguished than if the carrying capacity were lower. Put another way, for everyspecies there is a critical carrying capa~ity (and presumably, associated criticalisland area) such that extinction is muchmore ikely on islands of less than criticalsize than on those of greater than critk:al size. The key quantity in calculatingcritical size is ~.//x, rather than the intrinsic rate of increase r = h - p,. A eexamina-tion of this hypothesis (75) confirms its general conclusion of a critical size, abovewhich successful colonization is muchmore likely, and shows that if 1~< 1.5, the expected time to extinction even for an established population is notextremely long; that is, extinction may well be a common vent even on largeislands.

Crowell (8), in extensive experiments on three rodent species on small islandsPenobscot Bay, provided evidence not ,~nly that turnover occurs, but that thehypothesis of a critical population size determined by per capita birth and death


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EQUILIBRIUM ISLAND BIOGEOGRAPHY 169rates is valid. The fates of introduced populations of various sizes were monitored,as were those of extant populations and of islands from which the resident popula-tions were removedby trapping and poison. Per capita birth and death rates wereestimated, and the pattern of turnover on these islands accorded well with theequilibrium model. A further conclusion was that competition is much ess likelyto prevent colonization in this ecosystem han is poor dispersal aptitude.Critical population sizes wouldproduce a clear, dynamic ffect of area on speciesnumber, but so long as extinction probability decreases monotonically with popula-tion size and population size increases monotonically with area, area per se wouldbe expected to influence island species number ndependently of an effect throughhabitat diversity (30, 60). Simberloffhas demonstratedhis effect directly by census-ing nine homogeneousmangrove slands, then removing various fractions on all butone control island, and recensusing~ fter a period for reequilibration had passed. Thesize of the control fauna was unchanged, while species number ell by ~ 5-10%onall the reduced islands. Since no microhabitats were removed nd the microhabitatproportions were virtually unchanged, area clearly had an independent effect onspecies number. For very small islands one can probably separate the effects ofincreased area and added habitats because it may be obvious, as in the mangroveisland colonization experiment, whichspecies are precluded by absence of appropri-ate habitat. Sucha distinction has been drawn or plants of tiny atoll islands (113)and animals of sand cays (54). Each habitat maybe viewedas possessing an equilib-rium number of species, though for species which span two or more habitats thisis an oversimplification.

In addition to these three direct demonstrations(in the Florida Keys, the ChannelIslands, and Penobscot Bay) of equilibrium maintained on oceanic islands by fre-quent extinction and immigration, observations of turnover and apparent equilib-rium have been reported for birds on Karkar Island in NewGuinea (17) and MonaIsland in the Caribbean 105), and for invertebrates and plants on small islands nearPuerto Rico (38, 54, 55). (The Puerto Rican studies also present data relating lifehistory parameters to expected length of colonization, and demonstrating an ap-proximate trophic structure equilibrium as well as a species numberequilibrium.)But clearly nonequilibrium situations can also yield relevant data, both lendingsupport to the dynamicequilibrium hypothesis and allowing interpretation of appar-ently anomalousd~stnbutlons m light of the hypothesis.

The Florida Keys defaunation experiment is an example of how he dynamics ofa nonequilibrium situation, the presence of a series of "empty" islands capable ofsupporting animals, can verify the equilibrium hypothesis. But natural occurrencessuch as the production of a new sland (the volcanic island of Surtsey off Iceland,various "fill" islands such as the Dutchpolders, or islands risen from intertidal sandbanks such as Memmertn the North Sea) or sterilization of preexisting islands (thevolcanic defaunation of Krakatau in the East Indies and Long Island near NewGuinea) also leave undersaturation.By comparison to a regression equation for NewGuinea satellite islands, witharea, distance from NewGuinea, and maximum levation (a partial measure ofinsular habitat diversity) the independent variables, Diamond 18) calculated


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170 SIMBERLOFFequilibrium numberof bird species for islands suspected of being out of equilibrium.Using these numbers, he estimated that t0.9o for LongIsland is less than 300 yearsand for Krakatau less than 80 years (presumably because reforestation occurredmore quickly on Krakatau; the relationship between plant and bird species numbershas already been discussed). He pointed out that these are probably underestimatessince they rest on the assumption hat imraigration rate is a constant fraction of thespecies that have not yet colonized. Actually it is biologically evident (56, 59, 60)that dispersal differences amongpecies of potential colonists cause this fraction todecrease, as the good dispersers are differentially removed rom the pool of speciesthat have not yet colonized.

Diamondalso examined the islands of the DEntrecasteaux Shelf, which was asingle island of about 7430square miles in the Pleistocene, but has been fractionatedinto several small islands by rising seas. One might expect these islands to beoversaturated for their areas, with increased extinction, fostered by the decreasedarea, gradually reducing species number. n fact, large islands of this shelf all fallabove Diamonds egression, supporting the contention that they are oversaturated.Calculated relaxation times for these islands were in the range of 15,000 years. Thatthe approach to equilibrium after oversa*uration should be so muchslower thanafter defaunation (or undersaturation generally) is probably partly due to differenttime scales for the underlying biological process (extinction and colonization, re-spectively) and partly to differences in the extinction probabilities among pecies inthe pool (18, 59, 60). The east suited island colonists are extinguishedfirst, loweringisland extinction rates both because they can no longer be extinguished (they nolonger exist on the island!) and because their absence lessens competition. Smallislands on this shelf have much ower relaxation times, presumably because extinc-tion probabilities increase with decreasing area, as discussed above.

Islands which have once been connected by land bridges to NewGuinea are alsooversaturated, as evidenced by their positions above the regression equation. Againthe larger islands have relaxation times estimated in the range of 7000 years, whilethe small island estimates are much ower. Similar results were produced by analyz-ing islands that had been connected by land bridges not to NewGuinea proper, butto satellite islands. Terborgh 103) has used a related kinetic analysis to explain thegradual reduction in bird species number on Barro Colorado Island, formed somesixty years ago during the construction of the PanamaCanal.

Simberloff (92) has demonstrated that the mass extinction of more than half themarine invertebrate families during the Permo-Triassic maybe interpreted as relaxa-tion to a new and lower equilibrium; the extinctions coincided with a two-thirdsdecrease in area of the shallow marine sea,i, possibly fostered by sea-floor spreading(86). The model is fundamentally different from Diamonds n two regards. First,origination must replace local immigration as the force tending to increase familynumber, and so the number of families present increases rather than decreases thenumberof opportunities for further families to exist, since each family must arisefrom a preexisting family. Second, extinction and origination rates varied with thesquare of the deviation of number of families from an equilibrium estimated fromarea.


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EQUILIBRIUM SLAND BIOGEOGRAPHY 17Terborgh 102), analyzing he evolution of plant species number, uggested hatlocal patches of somehabitat will support a local equilibrium number f speciesdeterminedby immigration romother patches of the samehabitat and competitive

extinction proportional to the square of the number f species present. [Similarhypothesesof local patch diversity maintained n equilibrium through nterpatchmigration have been proposed 40, 52, 53).] Thenumber f species in the habitatas a whole, however, s viewed s a function of area, the speed of evolutionaryresponse o changed onditions, and the patchiness of the habitat, and is thoughtto evolve througha series of nonequilibrium tates. Extinction, independentofspecies number, s believed o be causedby majorclimatic or topographic hanges.Webb112) has shown hat the number f genera of North American and mammalsthrough he late Cenozoicwas determined y balancedextinction and origination,with occasional nonequilibrium pisodes causedby habitat fractionation, loweredsea levels, and other environmental hanges.Many nalyses have been performed hat regress numbers f species of differenttaxa on oceanic slands of an archipelago n area, isolation, and a variety of parame-ters related to habitat diversity, suchas elevation ange, numberf plant species forbirds), number f soil types, and latitude (2, 31-36,46-48, 111). Similar egressionshave been doneon caves, rivers, and mountaintopss habitat islands (4, 87, 108,109). The primary pattern that emerges s that area is usually the best singlepredictor of species number, hough he degree to which t accountsfor variationin species number ecreasesmarkedly s better indicators of habitat diversity areused. I have alreadydiscussed he limitations of multiple egressionand the indepen-dent evidence hat area is important,but these studies are neverthelessconsistentwith the equilibriummodel.Early indications that area did not contribute signifi-cantly to the determinationof bird (33, 34) and plant (35) species numbernGalapagos ave proven ncorrect when morecomplete lora was used (36, 47); theinference may owbe made hat bird and plant species numbers re determinedbythe same actors as in the ChannelIslands. Browns vidence that mammalsnmountaintopslands are not in equilibrium (4) may qually well be interpretedshowingonly that relaxation times are very long..Interactions ~tmong sland PopulationsIn the equilibrium model, species number s assumed sufficient parameterfordescribing nd predicting he courseof island colonization; ll speciesare consideredequivalent members f a species pool. An analogy maybe made o a chemicalequilibrium of the form A + B ~---AB.Underconstant conditions, the amountsofthe moleculesA, B, and AB re approximately onstant. If we actually counted henumber f each kind of moleculewewould ee minor fluctuations, but these wouldbe so small comparedo the total numbers f molecules hat it wouldbe virtuallyimpossible o observe hem; the statistical means f the amounts re sufficient formostpurposes. That different individual molecules f A and B are randomly oundin AB t different times is unimportant; ll comparativereas of biologyemphasizedifferencesamongpecies, and it is intuitively clear that the equilibrium onstella-tion of species foundon an island is not a randomubset of those available in the


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172 SIMBERLOFFpool. The observation (37) that the faunas of the fumigated mangrove islandsconverged to a canonical distribution into trophic classes is perhaps the clearestexperimental demonstration of this fact.

The data adducedas evidence for the nonequivaleneeof species colonizing poten-tial are often inappropriate, however. Althoughbetter dispersers might be expectedto reach islands more than other species, ~tnd better competitors ought to persist onthem longer once established, numerical analyses, as opposed to detailed observa-tion and experiment on the species of inlerest, may be misleading. MacArthuretal (57), examining he 59 land bird species of the Pearl Islands, listed 19 of thePanamanian amilies as absent, including 6 with 11-22 mainland species. (Actually,their data show 18 families absent; the Sylviidae are represented by Polioptilaplumbea on Rey.) They state, "While the absence of families with one or twomainland representatives might be merely a result of randomsampling of species,the absences of families with 11-22 mainland species is very unlikely to be acciden-tal." In fact, in 20 randomcomputer draws of 59 species from the 642 in Panama,only three times was no family with 20 or more species omitted, while three timesfamilies of 30 or more species were missed, and one draw did not include familieswith 23, 22, 17, 17, 16, and 13 species, respectively! The expected number f familiesin a random draw of 59 species from the Panamanian pool is 26.16 with standarddeviation 2.31 (106); the Pearl Islands actually contain 29 families. If anything, then,there are more families present than there ought to be in an avifauna this size. Insum, evidence of nonrandom olonization is not to be found in the Pearl Islandspresence or absence data alone. Rather, the important observation is that manyofthe same families that are absent from the, Pearl Archipelago are also missing fromother islands (57).A similarly inaccurate inference, that the relative paucity of congeneric specieson islands is caused by increased difficulty of coexistence in typically resource-poorisland ecosystems (23), was shown by identical methods to be artifactual (89).Actually, island biotas tend to have slightly more congeneric pairs than would arandomly drawn, equal-sized subset of the mainland pool. In both instances, thetendency of confamilial and congeneric species toward increased competition andrather similar dispersal powers is probably insufficiently strong to allow majorinsights. In this area of biogeography, n contrast to the equilibrium theory, labori-ous autecological studies are more likely than statistics to be illuminating. In anyevent, as both Simberloff (89) and Terborgh (101) have pointed out, degreecongeneric sympatry must itself be an equilibrium between the increased probabilitythat near relatives will be able to disperse to the same places and their increaseddifficulty in coexisting. Terborghs method s to construct species-area curves fordifferent families of birds in the West Indies, then to intercept all these curves byvertical lines drawn through given areas and to read off the numberof species ineach family. Fromsuch an analysis he ob~erved that changing degrees of sympatry[or "disharmony," to use Carlquists (6) term] are expected with changes in islandsize. As it is a trival computer exercise to draw randomly any numberof speciesfrom a species pool and then to calculate expected degree of sympatry, species-areacurves for individual families are a tortuous wayof demonstrating disharmony, and


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EQUILIBRIUM ISLAND BIO~EOGRAPHY 173since the data on which the curves are based come from the islands about whichthe predictions are to be made, this methoddoes not actually explain disharmony.But an autecologieal examination of the families, combinedwith historical dataabout the islands, allowed Terborgh to rationalize the apparent rough equilibriumlevels of sympatryand the existence of a few aberrant islands. The extent of deter-minism n West Indian bird faunas turns out to be quite high; Terborgh calculatedsimilarity coefficients between he avifaunas of different islands, extrapolated to findwhat the coefficients wouldbe if the islands were in the same ocation, and concludedthat perhaps 88 % of the fauna, species for species, of a small or medium-sizedslandcan be predicted from area and location alone.Several detailed autecological studies have attempted to explain observed levelsof sympatry on islands as a consequenceof competition for limited resources. Suchwork tacitly assumes that immigration is a negligible force in that islands aresaturated with all the species they can contain, given the available resources; ahigher immigration rate would only be balanced by a higher extinction rate, withthe species equilibrium re~naining unchanged. Competition and resource limitationare also assumed,and direct evidence is only rarely a~;ailable. Widervariability introphie structures for island species has been adduced as evidence for wider nichesupon release from competition, but relationships amongmorphological variability,niche width, and numberof coexisting species remain unproven(25, 98, 107, 116).Onewould hope that either the level of some limited resource could be changed,with concomitant changes in population sizes of putative competitors, or that re-movalor addition of a putative competitor should affect the population size of somespecies. But the techniques required for such experimentsare difficult, and research-ers are usually forced to infer competitionfrom differences in a species niche amongdifferent sets of other species or from morphological differences among oexistingspecies.

Lack claims that hummingbirdsdisperse readily among he West Indies, and thatthe nearly universal existence of two species on low islands and three species onmountainousones is due to competition for food (51). That the two species on lowislands are always comprised of one large and one small form is strong circumstan-tial evidence for this hypothesis, as is the restriction of the third species on moun-tainous islands to the montanehumidforest. Further indirect confirmation comesfrom observed habitat expansion for two species on islands where apparent com-petitiors are absent, and the observed replacement in the Virgin Islao.ds of onehummingbirdby another, similar one.

Lizards of the genusAnolis in the West Indies have been exhaustively studied byWilliams (115) and Schoener (80-85). Islands have up to 23 species, and the numberon a given island is not directly limited by immigration rate; one can infer manyfailed invasions. Rather, these lizards partition resources by habitat and size differ-ences and apparently exclude by competition potential immigrants. Although theniche has many ubtle dimensions, perch size, height, insolation, and time of perchutilization appear to be most important; it is possible for any island to construct forAnolis as Lack did for hummingbir~ls a fundamental fauna with an approximatenumberof species of certain size, habitat, and feeding characteristics, and to view


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174 SIMBERLOFFdeviations from the predicted, fundamental fauna as variations on a theme. Addi-tional strong evidence that competition structures the insular subsets of anolesconsists of different niche parameters for a given species coexisting with differentgroups of congeners; ecological release .and various kinds of niche shift, someinvolving sexual dimorphism, have been documented. McNab 61) constructedsimilar fundamental bat faunas for tropical islands, with food size (inferred frombody size) and food type as key parameters.

Niche shifts in birds of the Pearl Islands (57), West ndies (104, 105), and islandsnear NewGuinea (15, 19), and in ants of the Puerto Rico region (55) andTortugas (60) have been reported, and MacArthur & Wilson (60) discussedearlier examplesof niche shift and ecological release on islands. But as MacArthur& Wilson pointed out, in many nstances there is no evidence whatsoever of nicheshift in depauperate faunas, and perhaps absence of striking changes in resourceutilization is more the rule than the exception. Evolution of increased niche widthduring ecological release should be particuJarly slow in sexual species (77). Diamond(15) has shown or the southwest Pacific islands that changes in habitat are mostfrequent and immediate, changes in foraging behavior rarer and dependent or~evolution of appropriate morphology,and changes in food rarer still, while half ofall colonizing populations undergono cb :nges in niche. Part of the explanation forthe apparent inability to utilize newlyavailable food supplies lies in degree of initialpreadaptation to the new resource and differences in genetic plasticity (15), butanother possible explanation is that competition is not always important and popula-tions need not be limited by resource shortages. The yellow-faced grassquit onJamaica ought to be released from competition with manyseed-eaters in CentralAmerica, yet is less abundant, occupies the same numberof habitats, and has thesame morphology 73). The only observed difference was less stereotypy in seed sizeamong Jamaican birds.

Twometiculous studies on island colonization have indicated a nearly determinis-tic pattern completely predictable from ~. knowledgeof the pairwise interactionsamongspecies. Morse(65, 66) observed that whenone warbler was found on a smallisland off the coast of Maine t was always the Parula Warbler; when wo specieswere present they were always the Parula and Myrtle. The Black-throated Greenwas only present with the other two on slightly larger islands. The numberof speciesdepended on forest size, and the order of colonization was due to the greaterplasticity of foraging behavior of the Parula and Myrtle Warblers, allowing themto expand their habitat usage and thus to survive on small, resource-poor islands.The Black-throated Green, by contrast, has highly stereotyped behavior (a conse-quence of its high population densities and dominant position on the mainland),whichprevents adjustment to small-island life. Apparently the subordinate positionsof the Parula and Myrtle Warblers preadapt them to successful colonization. Therewasno evidence of interspecific competitic,n on the islands amonghe three species;rather, their short-term success or failure on small islands depends on intrinsicbehavioral traits evolved over long time !periods on the mainland, possibly in re-sponse to long-term competitive pressure there. The stylized behavioral resourcepartitioning also allows these three species to coexist on larger islands while the


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EQUILIBRIUM ISLAND BIOGEOGRAPHY 175American Redstart and Yellow Warbler, lacking such a well-defined interspecificsocial hierarchy, exclude one another.

Myomorphodents exist on islands in a variety of combinations. Crowells studyin the Gulf of Maine (8) demonstrated that the joint distribution of Microtus,Peromyscus,and Clethrionomyscould be satisfactorily explained by intrinsic dis-persal and survival capabilities, and that competition appeared to be unimportant.Grant examined species of the same genera plus Apodemus nd decided that com-petitive exclusions are more mportant than dispersal and establishment abilities, aconclusion whichhe has buttressed by cage studies of pairwise interactions (26, 27).Crowellsuggested that different immigration ates for different archipelagoes are thebasis for his and Grants conflicting results. It should be added that Grants islanddata do not evidence competition directly (through population size changes) andthat his competition experiments showing population size changes were in a main-land setting very different from Crowells tiny islands.Differences in avian population density between islands ~nd mainland have alsobeen related to competition. Niche expaasions upon release from competition havebeen inferred as the reason that island densities are higher than or equal to mainlanddensities in the Paarl Islands (57, 58), Tres Marias (24), Mona sland (105),Antilles (104), and Bermuda 7), despite reductions in species number. OnGuineasatellite islands, however, otal densities are severely reduced (16). Diamondhas suggested (16) that one must examine he species involved; where insular densi-ties exceed those of the mainland, the nesiotes are largely found in their mainlandhabitat or one quite similar, while on NewGuinea satellites habitat expansion hasbeen greater, resulting in occupancy of major parts of the islands by relativelymala:Japted birds. The claim that insular resource paucity causes population sizesof potentially competingcongeneric species to be more disparate than those on themainland (24) has been questioned (90), and population density statistics are gener-ally not likely to illuminate island ecology without detailed niche data on thecomponentspecies. Recent work on island vs mainland insect abundance suggeststhat disproportionate insular depauperization of predators can profoundly and com-plexly affect densities of lower trophic levels (1, 45).

ISLAND SPECIES AND EVOLUTIONThe Taxon CycleWehave seen that insular disharmony is a consequence of more than just theinevitable statistical changes in species-genus-family distribution whenspeciesnumber s reduced. Certain species are preadapted to insular colonization becausethey are adept at either overwater dispersal or survival on islands. Wilsonproposedthat the distribution of ants in Melanesia s due to a taxon cycle (117, 118) in whichwidespreadAsian species adapt evolutionarily to marginal habitats, especially shoreconditions that facilitate dispersal to islands. Some ropagules reach similar littoralhabitats on NewGuinea and surrounding islands, where they either die or invade(in evolutionary time) the inner rain forests and mountains. If they are not extin-


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176 SIMBERLOFFguished in the rain forests, their evolutionary divergence ultimately results in newspecies. Most are restricted, but there maybe habitat expansion including readapta-tion to littoral habitats from which the cycle mayonce again be started. Largerislands are more likely to produce expan,-ling species which may nitiate the cycle.presumablybecause the competition from greater numbersof species leads to fitterspecies and produces more pressure to occupy marginal habitats.

The taxon cycle is itself a dynamic ong-term equilibrium process dictating whichspecies contribute to the immigrationand extinction rates that establish the short-term island equilibrium numberof species. It is also ultimately responsible for thedegree of sympatry or disharmonywhich 1[ have already described as an equilibrium,within the island equilibrium, between increased probability of related speciesjointly colonizing an island and increased likelihood of exclusionary competitiononce they do. In a sense, we have three equilibria dependingon the scale with whichwe view islands: the taxon cycle is a long-term equilibrium flux of species involvingspeciation, immigration, and extinction, and generates pressures the short-termlocal expressions of which are dynamicequilibria of numberof species and degreeof sympatry. The taxon cycle has been shown, with minor local modifications, tobe consistent with distributional and ecological data on birds, lizards, and insectsof several island groups (12, 15-17, 20, :28-30, 76, 115).

Overlaying this strictly biotic-based dynamic scheme for determination of howmanyand which species will be present on any island are geological and sea levelchanges hat create and destroy land bridges, join several shelf islands to one anotherand/or the mainland, and fractionate a single land mass. During periods of connec-tion entirely new hort-term equilibria prevail and dispersal is facilitated. Expandingspecies inhabiting marginal regions are still more likely to to reach areas that wereor are destined to be parts of different islands, so that the equilibrium level ofsympatry maynot be disturbed. But if an entire taxon with poor over-water disper-sive powers is precluded from some slands that are never united to the mainlandand allowed on others that have periods of connection, very different faunas mayresult, both in species number and type of disharmony. These effects have beendemonstrated from paleontological evidence for Pleistocene mammalsof theAegean Sea (96, 97). MacArthur and Diamond (18, 56, 57) have emphasizedimportant the geological history of an island group is in explaining the distributionof so mobile an order as the birds. They distinguish between and-bridge and oceanicislands, and from island distributions anti autecological data deduce the species inthe Pearl Islands and the NewGuinea satellites that are likely to require a connec-tion in order to immigrate. The main conclusion has already been stated in thecontext of Diamonds sland relaxation time work: higher extinction rates on smallislands decrease the time until a newshort-term equilibrium number of species isachieved after a geological event change.i immigration rates, In other words, verysmall land bridges and oceanic islands mayhave very similar biotas.

A final factor affecting the short-term immigration-extinction balance is a gradualrise in the equilibrium as species evolve :3o as to be morehighly coadapted to oneanother and to the local environment (95, 119). This "finer tuning" of an islandcommunity hould decrease niche widths, and extinction rates, thus permitting thecoexistence of more species. Yet another equilibrium is ultimately reached, however,


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EQUILIBRIUM ISLAND BIOGEOGRAPHY 177Table 1 Nested, interdependent equilibria whichsimultaneouslydetermine he status ofan island biota. Geological vents and ntroductions act particularly on asterisked equili-bria to produce emporary onequilibrial states.

Equilibrium TimeScale Balanced ForcesBiogeographicRegionIsland

Evolutionary* Evolutionary

Taxon cycle Evolutionary

Evolutionary Evolutionary

Assortative and EcologicalInteractive (long)

Noninteractive* Ecological(short)Sympatry of Ecologicalclose relatives*

+ Speciationo Extinction+ Immigration of expanding

mainlandspecies- Extinction of contractingspecies on island+ Increased adaptation to local

physical conditions andcoadaptation among pecies- Increasedextinction as nichesevolve to be narrower+ Increased coadaptation ofsuccessivecolonizingsubsets- Increased extinction because ofpresent narrowniches+ hnmigration- Extinction+ Similarity of dispersal powers- Tendencyo increasedcompetition

as there is a limit to hownarrow niches maybe before extinction rates rise dramati-cally (56, 63). The exact capacity for evolutionary increase in the short-term equilib-rium must depend on the taxon, biogeographic region, and island size. Acomparisonbetween small Pacific islands with recently colonizing, widely ranging"tramp" ant species and those with old, presumably coadapted native ant faunassuggested that a doublingof species numbers possible (121). The various equilibrialprocesses that determine the instantaneous status of an island biota are listed inTable 1.Distance and Time in Host Plant IslandsJanzen (43) has suggested that the equilibrium theory of island biogeographyshouldbe applicable in evolutionary time to plant species as host plant islands for phytopha-gous insects, with phylogenetic distance betweenplant species an additional parame-ter that must be considered in assessing whether a particular plant has itsequilibrium numberof insects. Anexamination of the tree species of Great Britainand several other regions led Southwood99) to conclude that the numberof insectpest species for each tree species increases with the range of the tre~, but that if anequilibrium exists, it is achievedonly in evolutionary time; introduced plant speciesthus have relatively few insects. Whittaker (114) even claimed that phytophagousinsect communities may never reach equilibrium, but rather species number in-


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178 SIMBERLOFFcreases indefinitely, unlike vertebrate assemblages. Strong (100) disputed both as-pects of this hypothesis, presenting evidence that initial phytophagous insectcommunity quilibration occurs in ecological time, and the equilibrium reached [an"assortative" equilibrium in Wilsons (119) terms] depends largely on the presentrange of the plant. Opler (67) demonstrated that eighteen species of oaks wereindeed islands in evolutionary time, with numberof species of leaf-miners an equilib-rium between speciation and extinction. Plant range was the chief determinant ofthis number, and the data lit an equation of the form S ---- kAz just as they do forvarious taxa on oceanic islands. The appropriate distance parameter is unclear;geographic distance from other "islands" is important, as the apparent source formost colonizations is a sympatric tree species. Taxonomicdistance between treespecies is not monotonically related to ease of inter-island colonization by insectsof the trees as islands, but Opler dealt with a single closely related group of plants.Relaxation time for an oak "island" isolated from larger islands and left with manymore nsect species than the equilibrium predicted by its area is at least half a millionyears, but Opler presented no evidence on tree species islands that are suddenly"undersaturated," such as by an introduction, so that his hypothesis need notconflict with Strongs claim that introduced host plants equilibrate rapidly. Onemust recall the difference in relaxation tirr~es for birds on over- and undersaturatedislands off NewGuinea.CONCLUSIONSIsland biogeography has changed in a decade from an idiographic discipline withfew organizing principles to a nomothetic :~cience with predictive general laws. Thedynamicequilibrium theory which effected this transformation has been shown todescribe one level of a multi-level process occurring in both ecological and evolution-ary time; the major nsight leading to the theory is that local extinction and immigra.tion are relatively frequent events. Both ,,;pecies numberand species compositionresult from the interactions of several concurrent equilibria, though departures fromone or more of the equilibria frequently arise from Singular events such as introduc-tions or geological changes. The equilibria are ultimately quasiequilibria (119) then,since they are subject to long-term change. "Equilibrium" in this sense is synony-mous with "compromise," and the realization that island communities are compro-mises parallels the view that individual species are compromises nd the applicationof optimization theory in an attempt to understand the particular compromisesachieved by natural selection.

Even more important than an increased understanding of oceanic island biotasis the realization that manyhabitats are somewhatnsular and their biotas are inequilibrium just as are those of oceanic isl~nds. We an therefore use island biogeo-graphic theory to further our understanding of a variety of evolutionary and ecologi-cal phenomena nd even to aid in the preservation of the earths biotic diversity inthe face of mans ecological despoliation (103).


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EQUILIBRIUM ISLAND BIOGEOGRAPHY 179Literature Cited

1. Allan, J. D., Barnthouse, L. W., Prest-bye, R. A., Strong, D. R. 1973. On foli-age arthropod communities of PuertoRiean second growth vegetation.Ecology 54:628-322. Baroni Urbani, C. 1971. Studien zurAmeisenfauna Italiens. XI. DieAmeisen des Toskanischen Archipels.Betrachtungen zur Herkunft der Insel-faunen. Rev. Suisse Zool. 78:1037-673. Baumhover, A. H. et al 1955. Screw-worm ontrol through release of steril-ized flies. ,/.. Econ. Entomol.48:462-664. Brown, J. 1971. Mammalson moun-taintops: nonequilibrium insularbiogeography. Am. Natur. 105:467-785. Cairns, J., Dahlberg, M. L., Diekson,K. L., Smith, N., Waller, W. T. 1969.The relationship of fresh-water proto-zoan communities to the MacArthur-Wilson equilibrium model. Am. Natur,103:439-546. Carlquist, S. 1965. Island Life. GardenCity, NY: Natural History Press. 451PP.7. Crowell, K. L. 1962. Reduced inter-specific competition among he birds ofBermuda. Ecology 43:75-888. Crowell, K. L. 1973. Experimentalzoogeography: Introductions of mice tosmall islands. Am. Natur. 107:535-589. Culver, D. C. 1970. Analysis of simplecave communities. I. Caves as islands.Evolution 24:463-7410. Culver, D. C. 1971. Caves as ar-chipelagoes. Nat. Speleol. Soc. Bull.33:97-10011. Culver, D. C., Holsinger, J. R.,Baroody, R. 1973. Towarda predictivecave biogeography: The GreenbrierValley as a case study. Evolution. Inpress12. Darlington, P. J. 1970. Carabidae ontropical islands, especially in the WestIndies. Biotropica 2:7-1513. Darwin, C. 1859. On he Origin of Spe-cies by Means of Natural Selection.London: John Murray. 490 pp.14. Diamond, J. M. 1969. Avifaunal equi-libria and species turnover rates on theChannel Islands of California. Proc.Nat. Acad. Sci. USA64:57-6315. Diamond, . M. 1970. Ecological conse-quences of island colonization bySouthwest Pacific birds. I. Types ofniche shifts. Proc. Nat. Acad. Sci. USA67:529-3616. Diamond, . M. 1970. Ecological conse-quences of island colonization bySouthwestPacific birds. II. Theeffect of

(Literature search ended September 1973)species diversity on total populationdensity. Proc, Nat. Acad. Sci. USA67:1715-2117. Diamond, J. M. 1971. Comparison offaunal equilibrium turnover rates on atropical and a temperate island. Proc.Nat. Acad. Sci. USA68:2742-4518. Diamond, J. M. 1972. Biogeographickinetics: estimation of relaxation timesfor avifaunas of Southwest Pacific is-lands. Proc. Nat. Acad. Sci. USA69:3199-320319, Diamond, J, M, 1973. Distributionalecology of NewGuinea birds. Science179:759-69

20. Diamond, J. M. 1973. Colonization ofexploded volcanic islands by birds: Thesupertramp strategy. Submitted forpublication21. Dony, J. G. 1963. The expectation ofplant records from prescribed areas.Watsonia 5:377-8522. Elton, C. S. 1958. The Ecology of Inva-sions by Animals and Plants. London:Methuen. 181 pp.23. Grant, P. R. 1966. Ecological compati-bility of bird species on islands. Am.Natur. 100:451-6224. Grant, P. R. 1966. The density of landbirds on Tres Marias Islands in Mexico.I. Numbers nd biomass.-Can. J. Zool.44:391--40025. Grant, P. R. 1967. Bill length variabil-ity in birds of the Tres Marias Islands,Mexico. Can. J.. Zool. 45:805-1526. Grant, P. R. 1970. Colonization of is-lands by ecologically dissimilar speciesof mammals.Can. J. Zool. 48:545-5327. Grant, P. R. 1971. Experimental studiesof competitive interaction in a two-spe-.cies system. III. Microtus and Peromys-

cus species in enclosures. J. Anim. Ecol.40:323-5028. Greenslade, P. J.M. 1968. Island pat-terns in the Solomonslands bird fauna.Evolution 22:751-6129. Greenslade, P. J. M. 1968. The distribu-tion of some insects of the SolomonIslands. Proc. Linn. Soc. London179:189-9630. Greenslade, P. J. M. 1969. Insect distri-bution patterns in the Solomonslands.Phil. Trans. Roy. Soc. London B225:271-8531. Hamilton, T. H., Barth, R. H., Rubi-noff, I. 1964. The environmentalcontrolof insular variation in bird species abun-dance. Proc. Nat. Acad. Sci. USA52:132-40


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