AMER. ZOOL., 39:104-112 (1999)

Integration of Local and Regional Perspectives on the Species Richness ofCoral Assemblages'

RONALD H. KARLSON2 AND HOWARD V. CORNELL

Department of Biological Sciences, University of Delaware, Newark, Delaware 19716

SYNOPSIS. We have evaluated the relationship between regional species richnessand the number of species occurring within local, quantitatively sampled assem-blages of scleractinian corals. Our data have been extracted from the publishedliterature describing richness patterns from over 100 locations around the world.In general, we find a positive relationship between local and regional richness.Local richness is not independent of regional richness as posited by conventionaltheory and there is no hard upper limit indicating saturation. Instead, local coralassemblages are regionally enriched. This result suggests that these assemblagesare open to regional sources of species. The degree of regional enrichment is geo-graphically variable. In the Indo-Pacific, assemblages in speciose regions appearto be less open and much more sensitive to local depth and habitat gradients thanthose in more depauperate regions. Other large-scale geographical and historicaleffects on local richness in the Indo-Pacific include the degree of isolation fromhigh-diversity regions and distance from the equator. In contrast, local richness inthe relatively homogeneous and depauperate western Atlantic is insensitive to thelarge-scale variables we examined. As in most ecological communities, membershipin local assemblages of corals is not absolutely limited (by biotic interactions orlocal environmental factors) nor is it totally open to regional pools of species.Understanding the dynamics of coral communities will require integrating the localecological perspective with large-scale phenomena {i.e., physical TECO processes[Myers, 1994] and evolutionary history [Hugueny et al. 1997]). Such an integrationwill necessarily encompass multiple spatial and temporal scales.

INTRODUCTION lenge of integrating the effects of these lo-in recent years, community ecologists cal factors with much larger scale processes

have begun to recognize the influence of i n o r d e r t o understand community structurelarge-scale phenomena on the structure of a n d dynamics.local communities {e.g., Ricklefs and Expectations based on conventional the-Schluter, 1993; Giller et al., 1994). These o r y i n c l u d e t h e Prediction from MacArthurcomprise a wide variety of historical and <1965> t h a t t h e h i g h diversity exhibited bygeographical factors including such things m a n y t a x a i n t h e t r o P l c s 1S d u e t o h a b l t a t

as regional climate, geological disturbances, specialization (i.e., there are relatively largeunique speciation and extinction events, differences in species composition amongoceanographic transport processes, atmo- habitats). Within habitats, species member-spheric-oceanographic coupling, and even s h iP w a s t h o u g h t t o b e restricted primarilyorbital forcing of global climate. Traditional because of strong biological interactions,notions regarding the structure of ecological h a b i t a t stratification, and partitioning ofcommunities invoked local resource com- f o o d resources. Consequently, MacArthurpetition and niche diversification as central <1965> predicted that tropical habitats areparadigms. We are now faced with the chal- saturated with species.

The notion that habitats are saturateddates back at least to Elton (1933). Based

1 From the Symposium Coral Reefs and Environ- on animal surveys in similar habitats inmental Changes—Adaptation. Acclimation, or Extinc- q u j t e different places, he noted that the(ton presented at the annual Meeting of the Society for n u m b e r o f e c i e s co.Occurring in oneComparative and Integrative Biology, 3-7 January r i .1998, at Boston, Massachusetts. place was far below the number occurring

2 E-mail: rkarison@udel.edu in the general area. Thus he suggested that

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SPECIES RICHNESS OF CORAL ASSEMBLAGES 105

the species composition (i.e., membership)within local assemblages is limited to rela-tively few species rather than being open toall. Conventional theory predicts that lim-ited membership is a consequence of bio-logical interactions (competition and pre-dation) and physical environmental factorscharacteristic of the local habitat. This the-ory also predicts the following: 1) "localdiversity should be correlated with featuresof the environment, especially the diversityof resources," 2) "independently assem-bled communities in similar habitats on dif-ferent continents (or in different oceans)should contain similar numbers of species"(i.e., convergence), and 3) local "diversitywithin any habitat should reach a ceilingthat is independent of the number of speciesin the regional pool" (Schluter and Rick-lefs, 1993a). This last prediction describesthe quantitative relationship between localand regional species richness and providesthe focus for our work on coral speciesrichness.

Species richness is the component of spe-cies diversity referring only to the numberof species. At very large spatiotemporalscales, species richness describes biogeo-graphical assemblages and is indicative ofthe influence of evolutionary phenomenaand large-scale variation in the physical en-vironment. We define regional richness forcorals as the number of species measuredover large geographical scales (102-104

km). At much smaller spatiotemporalscales, species richness describes ecologicalassemblages and is indicative of the effectsof biological interactions and the localphysical environment. We define local rich-ness for corals at small spatial scales (10°—103 m). At these scales, samples provide es-timates of the within-habitat component ofspecies diversity. Although local richness issampled at one point in time, the recent his-tory of the assemblage over the life span ofthe resident organisms is reflected in suchsamples. As recognized by Done (1999)and many others, local richness in ecolog-ical assemblages is highly dynamic. By ex-amining the relationship between local andregional richness, we explore potentialcross-scale linkages between ecological andbiogeographical phenomena.

oic"5oo

boundary

Type I

Type II

Regional Richness

FIG. 1. Two theoretical models for the relationshipbetween local and regional richness in ecological as-semblages. In the Type I model (proportional sam-pling), local richness is independent of biotic interac-tions. The Type II model depicts saturation as localrichness reaches an upper limit and becomes indepen-dent of regional richness (from Cornell and Lawton,1992).

The theoretical relationship between lo-cal and regional richness for a saturated lo-cal assemblage is depicted as a curve inwhich local richness reaches an upper limitand becomes independent of regional rich-ness (Fig. 1; Cornell and Lawton, 1992).This saturation or Type II model is contrast-ed with a Type I model in which local rich-ness is independent of biotic interactions asit increases proportionately with regionalrichness. This pattern has been called "pro-portional sampling" by Cornell and Lawton(1992). It is equivalent to earlier "pool en-richment" (Cornell, 1985) and "regionalenrichment" (Ricklefs, 1987) models. Realassemblages are thought to fall betweenthese two theoretical extremes.

To date, empirical evidence supports theconclusion that "unsaturated patterns arecommon and widespread in natural com-munities" (Cornell and Karlson, 1997). Themajority of studies are consistent with theproportional sampling model or provide ev-idence for a curvilinear relationship be-tween local and regional richness, but notsaturation (Table 1). Early reports suggest-ing saturation among Caribbean birds (Ter-borgh and Faaborg, 1980; but see Wiens,1989) and freshwater fishes (Tonn et ah.

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106 R. H. KARLSON AND H. V. CORNELL

TABLE 1. Studies reporting sufficient local and re-gional richness values for regression analyses. A sig-nificant linear relationship is consistent with the TypeI model in Figure 1. Significant quadratic relation-ships indicate curvilinearity and possible saturationwhen local richness levels off (after Cornell and Karl-son, 1997).

Linear relationship (Type I model)Cynipid wasps (Cornell, 1985); Bracken insects

(Lawton, 1990); Parasitoid wasps (Dawah et al.,1995; Gaston and Gauld, 1993); Freshwater fishes(Griffiths, 1997; Hugueny and Paugy, 1995); Para-sitic worms (Kennedy and Guegan, 1994); Mixedtaxa including vertebrates, insects, corals, and trees(Caley and Schluter, 1997)

Curvilinear relationship but not saturationCaribbean birds (Ricklefs, 1987), Fig wasps (Haw-

kins and Compton, 1992), Deep-sea gastropods(Stuart and Rex, 1994)

Curvilinear relationship and saturation (Type II model)Fig wasp parasitoids (Hawkins and Compton, 1992);

Banksia (Richardson et al., 1995); Parasitic worms(Aho, 1990; Aho and Bush, 1993; Kennedy andGuegan, 1994)

1990) provided limited data unsuitable forregression analyses. More extensive datafrom studies on fig wasps, Australian bank-sias, and parasitic worms (see Table 1) in-dicate saturation as local richness levels offwith increasing regional richness (Cornelland Karlson, 1997). Among the quantitativestudies to date, there are few which havebeen conducted in marine environments andnone of these provide evidence for satura-tion. These include studies of deep-sea gas-tropods (Stuart and Rex, 1994), several taxaof encrusting marine invertebrates (personalcommunication, J. D. Witman), fishes (Ca-ley, 1997), and corals (Cornell and Karlson,1996, Caley and Schluter, 1997, Karlsonand Cornell, 1998).

REGIONAL ENRICHMENT OFCORAL ASSEMBLAGES

We conducted a survey of the publishedliterature in search of quantitative estimatesof the number of species occurring withinlocal coral assemblages. Prior to 1970, suchquantitative studies were not common(Stoddart, 1969). We found over eightypublications reporting local richness data,but sampling methods were so variable thatnot all of these were useful to us. Sixty

three sources published between 1918 and1993 reported the data as individual sam-ples or as means of replicate samples col-lected in the same vicinity. These provided1329 estimates of local richness from over100 sites located throughout the Indo-Pa-cific and Atlantic Oceans (they are cited inKarlson and Cornell, 1998).

These estimates were collected primarilyusing quadrat, line-transect, and point-inter-cept techniques and sample sizes for eachwere highly variable. We factored out var-iation among methods and that due to sam-pling effort by first regressing the logarithmof local richness against the logarithm ofsample size for each method separately(these relationships are typically linear). Wethen pooled the unexplained residuals fromthese regressions for further analysis. Theywere used as the dependent variable in a setof simple and stepwise regressions exam-ining the sensitivity of local richness to sev-eral independent variables (see below).

Our analysis of the quantitative relation-ship between local and regional richness us-ing data pooled across methods indicatesthat coral assemblages are not saturated(Cornell and Karlson, 1996; Karlson andCornell, 1998, Table 2). Furthermore, wefound no evidence for saturation when weanalyzed quadrat, line-transect, and point-intercept data separately (Cornell and Karl-son, 1996). Local richness was most sen-sitive to regional richness using data col-lected from line transects and least sensitiveusing point-intercept data (Cornell andKarlson, 1996).

As an example of regional variation inlocal richness, we contrast the mean num-ber of coral species observed along 10-mline transects. In the Philippines and Indo-nesia, where regional richness has been es-timated to be at least 350 species (Best etal, 1989; Veron, 1993) or even higher(over 450 species, Veron, 1995), the pub-lished literature supports an estimate of16.7 species per transect (from Sy et al,1982; Moll, 1986). A comparable value forthe relatively depauperate eastern Pacific(with only 19 species in the region) is 2.5species per transect (from Porter, 1972;Glynn, 1976; Guzman and Cortds, 1989).The mean across all regions in the Indo-

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TABLE 2. Selected results for the slope of the relationship between log-transformed local richness against log-transformed regional richness (from Karlson and Cornell [1998f and unpublished analyses). Residuals (R)were used as the dependent variable to account for variation due to multiple sampling methods (Q = quadrats,L = line transects, P = points) and effort. IP indicates the Indo-Pacific.

Spatial scaleSlope

(mean ± ISE)

GlobalGlobalGlobalGlobalGlobalGlobalGlobalIPAtlanticDepauperate IPSpeciose IPGreat Barrier Reef

Q, L and P', R1-m2 quadratsall small quadrats, Rall large quadrats, Rall quadrats, R10-m line transectsall line transects, RQ, L and P', RQ, L and P1, RQ, L and P', RQ, L and P1, RQ. L and P1, R

0.21 ± 0.03***0.15 ± 0.09 n.s0.14 ± 0.04 n.s0.30 ± 0.04***0.18 ± 0.03***0.81 ± 0.04***0.32 ± 0.03***0.27 ± 0.04***0.06 ± 0.07 n.s0.60 ± 0.06***0.24 ± 0.05**0.27 ± 0.07*

r-tests: *** P < 0.00001, ** P < 0.00005, * P < 0.0005, n.s. = not significant.

Pacific and Atlantic Oceans is 8.5 speciesper transect (Karlson and Cornell, unpub-lished data); the maximum is 33 species pertransect (from Moll, 1986).

This pattern of regional enrichment ismuch less evident when local richness issampled at smaller local scales. Althoughthe coefficients of variation for local rich-ness are similar at commonly used 10-mand 1-m2 scales (80% and 73%, respective-ly), the slope of the simple regression be-tween local and regional richness in the lat-ter is not significantly different from zero(Table 2). At this scale, the mean local rich-ness globally is 3.2 species per quadrat(Karlson and Cornell, unpublished data);the maximum is 13 species per quadrat(Connell, 1973; Grassle, 1973). Regionalenrichment was also not detected usingpooled data from all small quadrats (<6.7m2), whereas it was quite significant whenlocal richness was estimated using largerquadrats or line transects (Table 2). Thuswe speculate that local processes operatingat these larger spatial scales contribute toregional enrichment and species coexis-tence by offsetting factors typically thoughtto generate saturation (i.e., competitive ex-clusion and niche partitioning). Such pro-cesses may also operate at smaller spatialscales, but are likely to be much more dif-ficult to detect. After evaluating the putativeexplanations for the generation of spatialheterogeneity in local assemblages (re-

viewed in Cornell and Lawton, 1992), wesuggest that some combination of three pro-cesses may operate in coral assemblages.These include small-scale disturbances andpredation (Connell etal, 1997; Sale, 1977),neighborhood competition (Tilman, 1994;Pacala, 1986a, b), and intraspecific aggre-gation (Shorrocks, 1990). We suggest thatthese local phenomena operate in concertwith much larger scale processes to controlthe magnitude of regional enrichment.

LOCAL AND REGIONAL INFLUENCES ONLOCAL RICHNESS

Unlike the majority of studies examiningthe relationship between local and regionalrichness (see Table 1), our studies have ex-plored the simultaneous influences of localand regional variables on local species rich-ness (see Schluter [1986] and Schluter andRicklefs [19936] for a comparable ap-proach). We used depth (measured relativeto mean low water) and habitat categories(ranked by relative distance from shorethrough habitats in reef flat, crest, and slopeenvironments) as proxies for local environ-mental variation. Using stepwise regressionprocedures, we found that regional speciesrichness and these two local variables eachaccounted for approximately one third ofthe explained variation in the regressionmodel (Table 3); the total explained varia-tion (R2) was 37% (Cornell and Karlson,1996). Therefore, the processes contribut-

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108 R. H. KARLSON AND H. V. CORNELL

TABLE 3. Selected ANOVA results from stepwise regression analyses of local richness residuals vs. multipleindependent variables (from Cornell and Karlson [1996]' and Karlson and Cornell [1998]2). Only results fromthe global scale of analysis are reported here. Q = Quadratic term.

Source of variation

Model I1

DepthRegional speciesHabitat, QRegional species, Q

ErrorTotal

Model IPDepthRegional speciesHabitat, QDistance to nearest high-diversity regionDistance to equatorRegional generaRegional species, Q

ErrorTotal

df ss

4 336.55

90 556.60905 903.15

7 362.95

898 540.20905 903.15

MS

84.14**125.38**102.22**100.92**

8.04*0.63

51.85**125.38**98.92**95.82**24.91**9.54*7.79*0.60 n.s.0.60

F-tests: ** P < 0.0005, * P < 0.0001, n.s. = not significant.

ing to the regional enrichment of coral as-semblages would appear to be at least asimportant as those generating zonation pat-terns along depth or habitat gradients (e.g.,see Huston, 1985). Nevertheless, two thirdsof the observed variation in local richnesswas attributed to the local environment.This argues for continued emphasis on localprocesses as determinants of communitystructure, but also indicates the need to in-tegrate local and regional perspectives. Theregional species pool influencing local as-semblages is directly controlled by specia-tion, extinction events, transport processesinfluencing species dispersal, and the frag-mentation of biogeographical assemblages(Myers and Giller, 1989).

To explore the possible influence of mul-tiple large-scale variables on the local rich-ness of coral assemblages, we again usedstepwise regression analysis to screendepth, habitat, regional species richness,and five additional variables (the distanceto the nearest high-diversity region, dis-tance to the equator, the number of generain a region, the average age of genera in aregion, and a simple contrast between theIndo-Pacific and Atlantic provinces). Inspite of being highly intercorrelated, fourlarge-scale variables entered the multipleregression model along with depth and hab-

itat (Karlson and Cornell, 1998). These in-cluded the two geographical variables forthe distances to the nearest high-diversityregion and to the equator as well as regionalrichness in terms of numbers of species andgenera (Table 3). Although it is prematureto designate causal relationships betweenlocal richness and the influences of regionalrichness, location, regional climate, degreeof isolation, sea surface temperatures, etc.(see Fraser and Currie, 1996), it is clear thatlocal community structure is sensitive to theregional setting in which coral assemblagesoccur. Thus we urge that comparative stud-ies of local communities across regionalscales be conducted in order to explore thecross-scale linkage between local and re-gional phenomena.

We also found that the sensitivity of localrichness to regional richness varied with thegeographical scale of our analysis (seeDone, [1999] for a comparable argumentstressing the need to understand the region-al dynamics of coral communities). The in-ference that coral assemblages are region-ally enriched (based on a "global" analysisof data collected in both the Indo-Pacificand Atlantic provinces) did not apply to allcoral assemblages (Karlson and Cornell,1998). Significant enrichment was detectedthroughout the Indo-Pacific province at

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SPECIES RICHNESS OF CORAL ASSEMBLAGES 109

three different spatial scales (the entireprovince, speciose vs. depauperate regions,and the Great Barrier Reef), but was totallyabsent in the Atlantic province (Table 2).Enrichment was stronger in depauperate re-gions of the Indo-Pacific where local vari-ables explained little of the variation in lo-cal richness (e.g., the eastern Pacific), andweaker in the speciose, central Indo-Pacificwhere assemblages appear to approach sat-uration. Most of the coral assemblageswhich have been studied in the Atlanticprovince occur in the relatively homoge-neous Caribbean Sea where strong regionalgradients in species richness are not knownto occur. Thus detection of significant re-gional enrichment in the Atlantic was pre-cluded. In addition, Atlantic assemblagesare probably not saturated. The mean localrichness in the Atlantic is nearly identicalwith that in the Indo-Pacific (Karlson andCornell, 1998) and approximately half ofthat described for more diverse sites in In-donesia and the Philippines (see above).Along 10-m line transects, there were 9.5± 0.4 and 8.2 ± 0.6 species (means ± 1SE,t = 1.286, P > 0.05) in the Atlantic andIndo-Pacific provinces, respectively. Fur-thermore, the regional richness in the Ca-ribbean Sea was severely depleted follow-ing the closure of the Isthmus of Panama.The present 50 species represents approxi-mately 62% of the regional species richnessin the Caribbean 4 MYA and more than halfof the extant species originated 1-4 MYA(see Budd et al., 1996).

INTEGRATION

The extreme perspectives of coral assem-blages being completely closed or totallyopen to all potential colonists have beensupported by recent arguments based on pa-leontological evidence, colonization stud-ies, and modelling efforts. Here we brieflysummarize some of this evidence as we be-gin the integration of these divergent per-spectives. On the one hand, niche-based ex-planations for community structure are em-phasized as a consequence of Pleistoceneevidence for limited membership (Pandolfi,1996, 1999). On the other hand, dispersal-based explanations for community structureare supported by colonization studies sug-

gesting unlimited membership (Tomascik etal., 1996) and a metacommunity theoryunifying island biogeography with localcommunity dynamics (Hubbell, 1997). Ourown analyses indicate the importance offinding the "middle ground" (as suggestedby Roughgarden, 1989) where both dis-persal and niche attributes of corals are in-tegrated.

Pandolfi (1996, 1999) examined se-quences of fossil corals on the Huon Pen-insula of Papua New Guinea. Because oftectonic uplifting and sea level changes,nine distinct reef-building episodes span-ning a 95-ky Pleistocene interval were rep-resented by 122 coral species on a set ofraised terraces. While finding significantdifferences in species composition and rel-ative abundances of corals both within andamong reefs, there were no significant tem-poral differences. The same assemblages re-formed at each site during repeated reef-building episodes. Using a theoretical col-onization model, Pandolfi (1996) concludedthat the high temporal similarity exhibitedby these assemblages could not be ex-plained by random colonization processes.Membership in local assemblages appearedto be restricted rather than totally open toall. Furthermore, he invoked niche differ-ences among species as an explanation forthis apparent limited membership.

Elsewhere in the speciose central Indo-Pacific, Tomascik et al. (1996) examinedthe colonization by corals of a 5-year oldlava flow in the Banda Islands of Indonesia.A total of 124 coral species colonized thissubstrate including a diverse set of 45 Ac-ropora spp. Over half of the Acropora spp.were judged to be relatively uncommon inIndonesian waters. Their presence in theBanda Islands was attributed to transportprocesses and immigration from the region-al pool of available species. Thus at thisshort temporal scale, the coral assemblageappears to have had much less restrictedmembership with respect to this genus com-pared to the fossil assemblages describedby Pandolfi (1996). Although Acropora isthe most speciose genus of scleractiniancorals with at least 150 species (Veron,1995), many species are not well repre-sented in the fossil record. Pandolfi (1996)

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110 R. H. KARLSON AND H. V. CORNELL

reported only four. Given that limited mem-bership results from niche differences (in-fluencing colonization or post-colonizationresponses to the local environment), per-haps many of the successful acroporid col-onists in the Banda Islands will be excludedat some time in the future. Alternatively,the notion of limited membership may notapply to this highly successful coral taxon.Acropora spp. may be adapted primarily forsuccessful colonization under nonequilibrialenvironmental conditions rather than tomore stable local environments. Veron(1995) attributed their success to morpho-logical attributes favoring rapid growth, adiverse range of integrated architectures,and fragmentation. "These characteristicswould be particularly advantageous duringtimes of climatic change, when sea levels,wave turbulence, surface circulations andinorganic nutrients are all in states of flux."

At the extreme, niche differences amongspecies may have little influence on localcommunity structure. Hubbell (1997) re-cently illustrated how species richness andrelative abundance patterns can be gener-ated in ecological communities in a "per-fectly homogeneous environment inhabitedby perfectly identical species . . . ." Usinga theoretical model, realistic patterns ofcommunity structure emerged in the com-plete absence of niche differentiation. Localassemblages were linked together into "me-tacommunities" and dispersal across thislandscape determined the membership ofspecies at the local scale. Only "moderaterates of dispersal" were sufficient to "en-sure that these species are nearly every-where nearly all the time." Thus dispersal-based explanations of community structuremay be just as valid as niche-based expla-nations, yet they can be extremely difficultto falsify (Hubbell, 1997).

Again we emphasize the importance ofboth niche-based attributes and dispersalprocesses. "Real species are not identical,and they have niches" (Hubbell, 1997).Furthermore, dispersal is an extremely im-portant aspect of the dynamics of popula-tions and communities. In the marine realm,we are only just beginning to examine dis-persal models at regional scales {e.g., Rob-erts, 1997; Benzie, 1999). We suspect that

a full understanding of how both niche dif-ferences and dispersal control communitystructure will require continued efforts tointegrate community ecology with system-atics, biogeography, and paleontology (assuggested by Ricklefs, 1987). The relativeinfluence of local and regional phenomenaon coral species richness and other com-munity attributes are likely to vary amongregions in response to their unique histories,regional landscapes, and transport mecha-nisms.

ACKNOWLEDGMENTS

We thank the organizers of this sympo-sium, R. W. Buddemeier and H. R. Lasker,and the SCOR Working Group 104 for thisopportunity to present our work on coralrichness patterns. In addition, we acknowl-edge the sponsorship and support ofLOICZ, the SICB, and financial supportfrom the Coastal Ocean Program of NOAAand the University of Delaware. R. W. Bud-demeier, M. J. Caley, and two anonymousreviewers made helpful suggestions for im-proving the manuscript. During final revi-sions, the authors were funded by NSFGrant No. INT-9724759 and ARC GrantNo. A19801508 with T. P. Hughes, M. J.Caley, and C. C. Wallace.

REFERENCES

Aho. I. M. 1990. Helminth communities of amphibiansand reptiles: Comparative approaches to under-standing patterns and processes. In G. W. Esch, A.O. Bush, and J. M. Aho (eds.), Parasite commu-nities: Patterns and processes, pp. 157-195.Chapman and Hall, London.

Aho, J. M. and A. O. Bush. 1993. Community richnessin parasites of some freshwater fishes from NorthAmerica. In R. E. Ricklefs and D. Schluter (eds.),Species diversity in ecological communities: His-torical and geographical perspectives, pp. 185—193. The University of Chicago Press, Chicago,Illinois.

Benzie, J. A. H. 1999. Genetic structure of coral reeforganisms: Ghosts of dispersal past. Amer. Zool.39:131-145.

Best. M. B., B. W. Hoeksema, W. Moka, H. Moll, Su-harsono, and I. Nyoman Sutarna. 1989. Recentscleractinian coral species collected during theSnellius-Il Expedition in eastern Indonesia. Neth.J. Sea Res. 23:107-115.

Budd, A. E, K. G. Johnson, and T. A. Stemann. 1996.Pleistocene turnover and extinctions in the Carib-bean reef coral fauna. In J. B. C. Jackson, A. F.Budd, and A. G. Coates (eds.). Evolution and en-

by guest on July 6, 2011icb.oxfordjournals.org

Dow

nloaded from

SPECIES RICHNESS OF CORAL ASSEMBLAGES 111

vironment in tropical America, pp. 168—204. TheUniversity of Chicago Press, Chicago, Illinois.

Caley, M. J. 1997. Are local patterns of reef fish di-versity related to patterns of diversity at a largerscale? Proc. 8th Int. Coral Reef Symp. 1:993-998.

Caley, M. J. and D. Schluter. 1997. The relationshipbetween local and regional diversity. Ecology 78:70-80.

Connell, J. H. 1973. Population ecology of reef-build-ing corals. In O. A. Jones and R. Endean (eds.),Biology and geology of coral reefs, Vol. II, Biol-ogy 1, pp. 205-245. Academic Press, New York,New York.

Connell, J. H., T. P. Hughes, and C. C. Wallace. 1997.A 30-year study of coral abundance, recruitment,and disturbance in space and time. Ecol. Monogr.67:461-488.

Cornell, H. V. 1985. Local and regional richness ofcynipine gall wasps on California oaks. Ecology66:1247-1260.

Cornell, H. V. and R. H. Karlson. 1996. Diversity ofreef-building corals determined by local and re-gional processes. J. Anim. Ecol. 65:233—241.

Cornell, H. V. and R. H. Karlson. 1997. Local andregional processes as controls of species richness.In D. Tilman and P. Kareiva (eds.), Spatial ecol-ogy: The role of space in population dynamicsand interspecific interactions, pp. 250—268.Monographs in Population Biology 30. PrincetonUniversity Press, Princeton, New Jersey.

Cornell, H. V. and J. H. Lawton. 1992. Species inter-actions, local and regional processes, and limits tothe richness of ecological communities: A theo-retical perspective. J. Anim. Ecol. 61:1—12.

Dawah, H. A., B. A. Hawkins, and M. F. Claridge.1995. Structure of the parasitoid communities ofgrass-feeding chalcid wasps. J. Anim. Ecol. 64:708-720.

Done, T. J. 1999. Coral community adaptability to en-vironmental change at the scales of regions, reefs,and reef zones. Amer. Zool. 39:66-79.

Elton, C. 1933. The ecology of animals. Methuen, Lon-don, U.K.

Fraser, R. H. and D. J. Currie. 1996. The species rich-ness-energy hypothesis in a system where histor-ical factors are thought to prevail: Coral reefs.Am. Nat. 148:138-159.

Gaston, K. J. and I. D. Gauld. 1993. How many spe-cies of pimplines (Hymenoptera: Ichneumonidae)are there in Costa Rica? J. Trop. Biol. 9:491-499.

Giller, P. S., A. G. Hildrew, and D. G. Raffaelli (eds.).1994. Aquatic ecology: Scale, pattern and pro-cess. Blackwell Scientific Publications, Oxford.

Glynn, P. W. 1976. Some physical and biological de-terminants of coral community structure in theeastern Pacific. Ecol. Monogr. 46:431-456.

Grassle, J. E 1973. Variety in coral communities. InO. A. Jones and R. Endean (eds.), Biology andgeology of coral reefs, Vol. II, Biology 1, pp. 247-270. Academic Press, New York, New York.

Griffiths, D. 1997. Local and regional diversity inNorth American lacustrine fish species. J. Anim.Ecol. 66:49-56.

Guzman, H. M. and J. Cortes. 1989. Coral reef com-

munity structure at Cano Island, Pacific CostaRica. Mar. Ecol.—P. S. Z. Napoli I 10:23-41.

Hawkins, B. A. and S. G. Compton. 1992. African figwasp communities: vacant niches and latitudinalgradients in species richness. J. Anim. Ecol. 61:361-372.

Hubbell, S. P. 1997. A unified theory of biogeographyand relative species abundance and its applicationto tropical rain forests and coral reefs. Coral Reefs16:S9-S21.

Hugueny, B. and D. Paugy. 1995. Unsaturated fishcommunities in African rivers. Am. Nat. 146:162-169.

Hugueny, B., L. Tito de Morais, B. de Merona, and D.Ponton. 1997. The relationship between local andregional species richness: Comparing biotas withdifferent evolutionary histories. Oikos 80:583—587.

Huston, M. A. 1985. Patterns of species diversity oncoral reefs. Ann. Rev. Ecol. Syst. 16:149-177.

Karlson, R. H. and H. V. Cornell. 1998. Scale-depen-dent variation in local vs. regional effects on coralspecies richness. Ecol. Monogr. 68:259—274.

Kennedy, C. R. and J.-E Gu6gan. 1994. Regional vs.local helminth parasite richness in British fresh-water fish: Saturated or unsaturated parasite com-munities? Parasitology 109:175-185.

Lawton, J. H. 1990. Local and regional species-rich-ness of bracken-feeding insects. In J. A. Thomp-son and R. T. Smith (eds.), Bracken biology andmanagement, pp. 197—202. Australian Institute ofAgricultural Science, Sydney.

MacArthur, R. H. 1965. Patterns of species diversity.Biol. Rev. 40:510-533.

Moll, H. 1986. The coral community structure on thereefs visited during the Snellius II Expedition ineastern Indonesia. Zool. Med. Leiden 60:1—25.

Myers, A. A. 1994. Biogeographic patterns in shallow-water marine systems and the controlling process-es at different scales, In P. S. Giller, A. G. Hildrew,and D. G. Raffaelli (eds), Aquatic ecology: Scale,pattern and process, pp. 547—574. Blackwell Sci-entific Publications, Oxford.

Myers, A. A. and P. S. Giller (eds.) 1989. Analyticalbiogeography. An integrated approach to thestudy of animal and plant distributions. Chapmanand Hall, London.

Pacala, S. W. 1986a. Neighborhood models of plantpopulation dynamics: 2. Multispecies models ofannuals. Theor. Pop. Biol. 29:262-292.

Pacala, S. W. 1986fc. Neighborhood models of plantpopulation dynamics: 4. Single-species and mul-tispecies models of annuals with dormant seeds.Am. Nat. 128:859-878.

Pandolfi, J. M. 1996. Limited membership in Pleisto-cene reef coral assemblages from the Huon Pen-insula, Papua New Guinea: Constancy duringglobal change. Paleobiology 22:152-176.

Pandolfi, J. M. 1999. Response of Pleistocene coralreefs to environmental change over long temporalscales. Amer. Zool. 39:113-130.

Porter, J. W. 1972. Predation by Acanthaster and itseffect on coral species diversity. Am. Nat. 106:487-492.

by guest on July 6, 2011icb.oxfordjournals.org

Dow

nloaded from

112 R. H. KARLSON AND H. V. CORNELL

Richardson, D. M., R. M. Cowling, B. B. Lamont, andH. J. van Hensbergen. 1995. Coexistence of Bank-sia species in southwestern Australia: the role oflocal and regional processes. J. Veg. Sci. 6:329-342.

Ricklefs, R. E. 1987. Community diversity: relativeroles of local and regional processes. Science 235:167-171.

Ricklefs, R. E. and D. Schluter. (eds.) 1993. Speciesdiversity in ecological communities. Historicaland geographical perspectives. The University ofChicago Press, Chicago, Illinois.

Roberts, C. M. 1997. Connectivity and management ofCaribbean coral reefs. Science 278:1454-1457.

Roughgarden, J. 1989. The structure and assembly ofcommunities. In J. Roughgarden, R. M. May, andS. A. Levin (eds.), Perspectives in ecological the-ory, pp. 203-226. Princeton University Press,Princeton.

Sale, P. F. 1977. The maintenance of high diversity incoral reef fish communities. Am. Nat. 111:337—359.

Schluter, D. 1986. Tests for similarity and convergenceof finch communities. Ecology 67:1073-1085.

Schluter, D. and R. E. Ricklefs. 1993a. Species diver-sity. An introduction to the problem. In R. E.Ricklefs and D. Schluter (eds.), Species diversityin ecological communities. Historical and geo-graphical perspectives, pp. 1-10. The Universityof Chicago Press, Chicago, Illinois.

Schluter, D. and R. E. Ricklefs. 1993fc. Convergenceand the regional component of species diversity.In R. E. Ricklefs and D. Schluter (eds.), Speciesdiversity in ecological communities. Historicaland geographical perspectives, pp. 230—240. TheUniversity of Chicago Press, Chicago, Illinois.

Shorrocks, B. 1990. Coexistence in a patchy environ-ment, In B. Shorrocks and I. R. Swingland (eds.),

Living in a patchy environment, pp. 91—106. Ox-ford University Press, Oxford.

Stoddart, D. R. 1969. Ecology and morphology of Re-cent coral reefs. Biol. Rev. 44:433-498.

Stuart, C. T. and M. A. Rex. 1994. The relationshipbetween developmental pattern and species diver-sity in deep-sea prosobranch snails, In C. M.Young and K. J. Eckelbarger (eds.), Reproduction,larval biology and recruitment in the deep seabenthos, pp. 118-139. Columbia University Press,New York.

Sy, J. C, E S. Herrera, and J. W. McManus. 1982.Coral community structure of a fringing reef atMactan Island, Cebu, Philippines. Proc. 4th Int.Coral Reef Symp. 2:263-269.

Terborgh, J. W. and J. Faaborg. 1980. Saturation ofbird communities in the West Indies. Am. Nat.116:178-195.

Tilman, D. 1994. Competition and biodiversity in spa-tially structured habitats. Ecology 75:2—16.

Tomascik. T, R. van Woesik, and A. J. Mah. 1996.Rapid coral colonization of a recent lava flow fol-lowing a volcanic eruption, Banda Islands, Indo-nesia. Coral Reefs 15:169-175.

Tonn, W. M., J. J. Magnuson, M. Rask, and J. Toivo-nen. 1990. Intercontinental comparison of small-lake fish assemblages: the balance between localand regional processes. Am. Nat. 136:345—375.

Veron, J. E. N. 1993. A biogeographic database of her-matypic corals; species of the central Indo-Pacific,genera of the world. Aust. Inst. Mar. Sci. Monogr.Ser. 10:1-433.

Veron, J. E. N. 1995. Corals in space and time. Thebiogeography and evolution of the Scleractinia.Cornell University Press, Ithaca, New York.

Wiens, J. A. 1989. The ecology of bird communities.Volume 1. Foundations and patterns. CambridgeUniversity Press, Cambridge.

Corresponding Editor: Kirk Miller

by guest on July 6, 2011icb.oxfordjournals.org

Dow

nloaded from