niques is taking place, and new informa-tion is already yielding fresh insights intochemical, physical, and biological sys-tems.

Refereces and Notes

1. B. M. Kincaid, J. App!. Phys. 48, 2684 (1977); J.P. Blewett and F. Chasman, ibid., p. 2692.

2. D. A. G. Deacon, L. R. Elias, J. M. J. Madey,G. J. Ramian, H. A. Schwettman, T. I. Smith,Phys. Rev. Lett. 38, 892,fi977).

3. D. Iwanenko and 1. Pomeranchuk, Phys. Rev.65, 343 (1944).

4. J. P. Blewett, ibid. 69, 87 (1946).5. J. S. Schwinger' ibid. 70, 798 (1946); ibid. 75,

1912 (1949).6. B. Alpert and R. Lopez-Delgado, Nature (Lon-

don) 263, 445 (1976).7. 0. B. d'Azy, R. Lopez-Delgado, A. Tramer,

Chem. Phys. 9, 327 (1975).

8. L. F. Wagner and W. E. Spicer, Phys. Rev.Lett. 28, 1381 (1972).

9. D. E. Eastman and W. D. Grobman, ibid., p.1379.

10. I. Lindau, in Synchrotron Radiation Research,A. N. Mancini and I. F. Quercia, Eds. (Inter-national Colloquium on Applied Physics, Isti-tuto Nazionale di Fisica Nucleare, Rome, inpress).

11. R. J. Smith, J. Anderson, G. J. Lapeyre, Phys.Rev. Lett. 37, 1081 (1976).

12. E. Spiller, R. Feder, J. Topalian, D. Eastman,W. Gudat, D. Sayre, Science 191, 1172 (1976);R. Feder, E. Spiller, J. Topalian, A. N. Broers,W. Gudat, B. J. Panessa, Z. A. Zadunaisky, J.Sedat, ibid. 197, 259 (1977); E. Spiller, D. E.Eastman, R. Feder, W. D. Grobman, W. Gudat,J. Topalian, J. Appl. Phys. 47, 5450 (1976); E.Spiller and R. 'Feder, in X-ray Optics, H. J.Quesser, Ed. (Springer-Verlag, Berlin, in press);B. Fay, J. Trotel, Y. Petroff, R. Pinchaux, P.Thiry, Appl. Phys. Lett. 29, 370 (1976). For ageneral review of x-ray lithography with con-ventional $ources see S. E. Bernacki and H. I.

Smith, IEEE Trans. Electron Devices, ED-22,421 (1975).

13. P. Horowitz and J. A. Howell, Science 178, 608(1972).

14. B. M. Kincaid, P. Eisenberger, K. 0. Hodgson,S. Doniach, Proc. Natl. Acad. Sci. U.S.A. 72,2340 (1975).

15. K. D. Watenpaugh, L. C. Sieker, J. R. Herriott,L. H. Jensen, Acta Crystallogr. Sect. B 29, 943(1973).

16. See, for example, R. G. Shulman, P. Eisen-berger, W. E. Blumberg, N. A. Stombaugh,Proc. Natl. Acad. Sci. U.S.A. 72, 4003 (1975).

17. R. S. Goody, K. C. Holmes, H. G. Mannherz, J.Barrington Leigh, G. Rosenbaum, Biophys. J.15, 687J1975).

18. T. Tuomi, K. Naukkarian, P. Rabe, Phys. Stat-us SolidiA 25, 93 (1974); M. Hart,J. Appl. Crys-tallogr. 8, 436 (1975); J. Bordas, S. M. Glazer,H. Hauser, Philos. Mag. 32, 471 (1975); B. Bur-as anl J. Staun Olsen, Nuc. Instrum. Methods135, 193 (197t).

19. Research was performed at Brookhaven Nation-al Laborator'y ynder contract with ERDA.

Diversity in Tropical RainForests and Coral Reefs

High diversity of trees and corals is maintainedonly in a nonequilibrium state.

Joseph H. Connell

The great variety of species in localareas of tropical rain forests and coralreefs is legendary. Until recently, theusual explanation began with the as-

sumption that the species composition ofsuch assemblages is maintained near

equilibrium (1). The question thus be-came: "how is high diversity maintainednear equilibrium?" One recent answer

communities is a consequence of pastand present interspecific competition, re-

sulting in each species occupying thehabitat or resource on which it is themost effective competitor. Without per-

turbation this species composition per-

sists; after perturbation it is restored tothe original state (3).

Id recent years it has become clear

Summary. The commonly observed high diversity of trees in tropical rain forestsand corals on tropical reefs is a nonequilibrium state which, if not disturbed further, willprogress toward a low-diversity equilibrium community. This may not happen if gradu-al changes in climate favor different species. If equilibrium is reached, a lesser degreeof diversity may be sustained by niche diversification or by a compensatory mortalitythat favors inferior competitors. However, tropical forests and reefs are subject tosevere disturbances often enough that equilibrium may never be attained.

for tropical bird communities is given as

follows: "The working hypothesis is that,through diffuse competition, the com-

ponent species of a community are se-

lected, and coadjusted in their nichesand abundances, so as to fit with eachother and to resist invaders" (2). In thisview, the species composition of tropical

that the frequency of natural disturbanceand the rate of environmental change are

often much faster than the rates of recov-ery from perturbations. In particular,competitive elimination of the less effi-cient or less well adapted species is notthe inexorable and predictable processwe once thought it was. Instead, other

0036-8075/78/0324-1302$02.00/0 Copyright 1978 AAAS

forces, often abrupt and unpredictable,set back, deflect, or slow the process ofreturn to equilibrium (4). If such forcesare the norm, we may question the use-fulness of the application of equilibriumtheory to much of community ecology.

In this article I examine several hy-potheses concerning one aspect of com-munity structure, that is, species rich-ness or diversity (5). I first explore theview that communities seldom or neverreach an equilibrium state, and that highdiversity is a consequence of continuallychanging conditions. Then 1 discuss theopposing view that, once a communityrecovers from a severe perturbation,high diversity is maintained in the equi-librium state by various mechanisms.Here I apply these hypotheses to or-

ganisms such as plants or sessile animalsthat occupy most of the surface of theland or the firm substrates in aquatichabitats. I consider two tropical commu-nities, rain forests and coral reefs, con-centrating on the organisms that deter-mine much of the structure, in thesecases, trees and corals. Whether my ar-guments apply to the mobile species,such as insects, birds, fish, and crabs,that use these structures as shelteror food, or to nontropical regions, re-mains to be seen. I deal only with varia-tions in diversity within local areas, notwith large-scale geographical gradientssuch as tropical to temperate differ-ences. While the hypotheses I presentmay help explain them, such gradientsare just as likely to be produced bymechanisms not covered in the presentarticle (6).

Various hypotheses have been pro-posed to explain how local diversity isproduced or maintained (or both). I havereduced the number to six, which fall in-to two general categories:Joseph H. Connell is a professor of biology at the

University of California, Santa Barbara 93106.

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1) The species composition of com-munities is seldom in a state of equilibri-um. High diversity is maintained onlywhen the species composition is contin-ually changing. (i) Diversity is higherwhen disturbances are intermediate onthe scales of frequency and intensity (the"intermediate disturbance" hypothesis).(ii) Species are approximately equal inability to colonize, exclude invaders, andresist environmental vicissitudes. Localdiversity depends only on the number ofspecies available in the geographical areaand the local population density (the"equal chance" hypothesis). (iii) Gradu-al environmental changes, that alter theranking of competitive abilities, occur ata rate high enough so that the process ofcompetitive elimination is seldom if evercompleted (the "gradual change" hy-pothesis).

2) The species composition of com-munities is usually in a state of equilibri-um; after a disturbance it recovers tothat state. High diversity is then main-tained without continual -changes in spe-cies composition. (iv) At equilibrium eachspecies is competitively superior in ex-ploiting a particular subdivision of thehabitat. Diversity is a function of the to-tal range of habitats and of the degree ofspecialization of the species to parts ofthat range (the "niche diversification"hypothesis). (v) At equilibrium, eachspecies uses interference mechanismswhich cause it to win over some com-petitors but lose to others (the "circularnetworks" hypothesis). (vi) Mortalityfrom causes unrelated to the competitiveinteraction falls heaviest on whicheverspecies ranks highest in competitive abil-ity (the "compensatory mortality" hy-pothesis).

Nonequilibrium Hypotheses

The intermediate disturbance hypoth-esis. Organisms are killed or badly dam-aged in all communities by disturbancesthat happen at various scales of frequen-cy and intensity. Trees are killed or bro-ken in tropical rain forests by wind-storms, landslips, lightning strikes,plagues of insects, and so on; corals aredestroyed by agents such as stormwaves, freshwater floods, sediments, orherds of predators. This hypothesis sug-gests that the highest diversity is main-tained at intermediate scales of distur-bance (Fig. 1).The best evidence comes from studies

of ecological succession. Soon after a se-vere disturbance, propagules (for ex-ample, seeds, spores, larvae) of a fewspecies arrive in the open space. Diver-24 MARCH 1978

HIGH

I-

co

Fig. 1. The "inter-mediate disturbance"hypothesis. The pat-terns in species compo-sition of adults andyoung proposed byEggeling (8) for the dif-ferent successionalstages of the Budongoforest are shown dia-grammatically at thebottom.

LOW

DI STURBANCES FREQUENT INFREQUENT

SOON AFTER A DISTURBANCE - LONG AFTER

DISTURBANCE LARGE

A. COLONIZING

sity is low because the time for coloniza-tion is short; only those few species thatboth happen to be producing propagulesand are within dispersal range will colo-nize. If disturbances continue to happenfrequently, the community will consist ofonly those few species capable of quick-ly reaching maturity.As the interval between disturbances

increases, diversity will also increase,because more time is available for the in-vasion of more species. New specieswith lower powers of dispersal and slow-er growth, that were excluded by morefrequent disturbances, can now reachtnaturity. As the frequency declines fur-ther and the interludes between catastro-phes lengthen, diversity will decline, forone of two reasons. First, the competitorthat is either the most efficient in ex-ploiting limited resources or the most ef-fective in interfering with other species(or both) will eliminate the rest. Second,even if all species were equal in com-petitive ability, the one that is the mostresistant to damage or to death causedby physical extremes or natural enemieswill eventually fill much of the space.This process rests on the assumptionthat once a site is held by any occupant,it blocks all further invasion until it isdamaged or killed. Thus it competitivelyexcludes all potential invaders, whichare by assumption incapable of com-petitively eliminating it (7).

Thus, diversity will decline duringlong interludes between disturbances un-less other mechanisms, such as thosegiven in the other hypotheses below, in-tervene to maintain diversity. Distur-bances interrupt and set back the pro-

SMALL

B. MIXED C. CLIMAX

cess of competitive elimination, or re-move occupants that are competitivelyexcluding further invaders. Thus, theykeep local assemblages in a nonequi-librium state, although large geographicareas may be stable in the sense that spe-cies are gained or lost at an impercep-tible rate.

Evidence that this model applies totropical rain forests comes from severalsources. Eggeling (8) classified differentparts of the Budongo forest of Ugandainto three stages: colonizing, mixed, andclimax stands. Using observations mademany years apart, he showed that thecolonizing forest was spreading in-to neighboring grassland. In these colo-nizing stands the canopy was dominatedby a few species (class A in Fig. 1), butthe juveniles (class B in Fig. 1) were ofentirely different species. Adults of theclass B species occurred elsewhere ascanopy trees in mixed stands of manyspecies. In these mixed stands, the juve-niles were also mainly of different spe-cies (class C, Fig. 1), those with evengreater shade tolerance. Adults of classC species occurred in the canopy of oth-er climax stands where a few speciesdominated (mainly ironwood, Cyno-metra alexandrei, which comprised 75to 90 percent of the canopy trees). How-ever, in these stands, the understory wascomposed mainly ofjuveniles of the can-opy species. Thus, an assemblage of self-replacing species (that is, a climaxcommunity of low diversity) had beenachieved. This is not a special case; theBudongo forest is the largest rain forestin Uganda, and one-quarter of it is domi-nated by ironwood. Later and more ex-

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Table 1. Mortality of young trees (between 0.2 and 6.1 meters tall) in relation to their abundancefor two rain forests in Queensland. Not all species had enough young trees to analyze; onlythose whose adults were capable of reaching the canopy and that had at least six young trees areincluded. The mortality rate between 1965 and 1974 was plotted against the original numbersmapped in 1965; the least-squares regression slope and correlation coefficient are shown.

Regression ofNumber mortality (%)

Site of on abundancespecies

Slope r*

Tropical, North Queensland, 16°S 49 0.039 0.217Subtropical, South Queensland, 260S 46 0.002 0

*Neither correlation coefficient is significantly different from zero at P < .05

tensive surveys (9) showed that the pro-

portion so dominated in other forests inUganda is even higher and have con-

firmed that, where Cynometra dominatesthe canopy, its juveniles also dominatethe understory.Another excellent example is the work

of Jones (10) in Nigeria. In this diversetropical forest, many of the larger trees,aged about 200 years, were dying. Theyprobably became established in aban-doned fields in the first half of the 18thcentury, a time when the countrysidewas depopulated by the collapse of theBenin civilization. These trees had fewoffspring; most regeneration was by oth-er species, shade-tolerant and of moder-ate stature. This mixed forest was in factan "old secondary" forest that had in-vaded after agricultural disturbances. Itwas in about the same state as Eggeling'smixed forest in Uganda. In both Nigeriaand Uganda, high diversity was found ina nonequilibrium intermediate stage inthe forest succession.

In many studies of forest dynamics,the abundance of juvenile stages consti-tutes the evidence as to whether a spe-

cies is expected to increase or to die out.Such inferences are of course open to thecriticism that, if the mortality rate of ju-veniles increases with their abundance,it is not necessarily a good indicator ofmore successful recruitment. I testedthis for young trees in two rain forestplots in Queensland that several col-leagues and I have been studying since1963 (11). Over a 9-year period, mortali-ty showed no correlation with abun-dance (Table 1). Thus, it seems safe toassume that species which now havemany offspring will be more abundant inthe next generation of adult trees as com-

pared to those species which now havefew offspring.

In most of the mixed, highly diversestands of tropical rain forests that havebeen studied, some species are repre-sented by many large trees with few or

no offspring, whereas others have a su-

perabundance of offspring (8, 10-12). (Ofcourse, many species are so rare as

1304

adults that one would not expect to findmany offspring.) My interpretation ofthis finding is that these mixed tropicalforests represent a nonequilibrium inter-mediate stage in a succession after a dis-turbance, in which some species popu-lations are decreasing whereas others are

increasing. Since mixed rain forests are

common in the tropics, this hypothesissuggests that disturbance is frequentenough to maintain much of the region inthe nonequilibrium state.

If this is so, tropical forests dominatedby a single canopy species that has abun-dant offspring in the understory must nothave been disturbed for several genera-

tions. Such forests, similar to the iron-wood climax of Eggeling (8), also occur

commonly elsewhere in Africa as well as

in tropical America and Southeast Asia(13). Two lines of evidence indicate thatthey have been less frequently disturbedthan have mixed forests. First, the onlypapers that I have found in which the in-cidence of storms was described in rela-tion to single-dominant forests state thatdestructive storms "never occur" inthese regions (8, 14). Second, many ofthese forests are unlikely to have beendisturbed by man, because they lie on

poor soils, in swamps or along creekmargins, on steep stony slopes, or on

highly leached white sands (12, 15). Allof these are soils that the farmers ofshifting cultivation in forests avoid sincethey produce very poor crops (12). Suchagriculture is confined mainly to the well-drained good soils, and these are thesoils where the mixed diverse forests ex-

ist. Thus, mixed forests occur in theplaces most likely to have been disturbedby man, whereas single-dominant forestsoccur in those least likely to have beendisturbed.

Since single-dominant forests often(though not always) lie on poor soils, ithas usually been assumed that this is be-cause only a few species have evolvedadaptations to tolerate them (12, 15).However, the difference between forestson good soils and those on poor soils liesin the dominance of a single species in

the canopy rather than in the total num-ber of species. Thus, in comparing plotsin rain forests in Guyana, the commonestspecies constituted 16 percent of thelarge trees (more than 41 centimeters indiameter) on good soils and 67 percenton poor soils (leached white sands), yetthe number of species of trees more than20 centimeters in diameter was 55 and49, respectively [table 27 in (12)]. Thus, alarge number of moderate- to large-sizedtree species occupy poor soils, eventhough only a few are common. The bestevidence that single-species dominanceis not necessarily due to poor soils is theexample of the Budongo forest. Here,various forest stands, ranging from onesof mixed high diversity to those withsingle-species dominance, each occur onsimilar soils. Single-species dominanceseems to be explained more satisfac-torily by the absence of disturbancerather than by poor soil quality.On coral reefs, the relation between

disturbance and diversity is similar tothat in tropical forests. At Heron Island,Queensland, the highest number of spe-cies of corals occurs on the crests andouter slopes that are exposed to dam-aging storms. Since I began studying thisreef in 1962, two hurricanes have passedclose to it, one in 1967 and one in 1972.Each destroyed much coral on the crestand outer slopes but failed to damageanother slope protected by an adjacentreef. The disturbed areas have been re-colonized by many species after eachhurricane, but colonization has not beenso dense that competitive exclusion hasyet begun to reduce the diversity (Fig.2A). Other workers on corals have wit-nessed the same phenomenon; distur-bances caused both by the physical envi-ronment and by predation remove coralsand then recolonization by many speciesfollows (16, 17).

In contrast, in permanently markedquadrats observed over several yearswithout disturbance at Heron Island, Ifound that competitive elimination ofneighboring colonies was a regular fea-ture, either by one colony overshad-owing or overgrowing another, or bydirect aggressive interactions (18). Herecompetition is by interference, ratherthan by more efficient exploitation ofresources. On one region of the southouter slope, protected from storm distur-bance by an adjacent reef, huge old colo-nies of a few species of "staghorn" cor-als occupy most of the surface (Fig. 2B).Since these are able to overshadowneighbors (18) at a height sufficient to beout of reach of the mesenteric filamentsused as defenses (19), I infer that suchstaghorns have in fact competitively

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eliminated many neighbors during theirgrowth. Here competitive eliminationhas apparently gone to completion, witha consequent reduction in local diver-sity. A similar situation has been de-scribed for Hawaii (16) and for the Pacif-ic coast of Panama (17).The discussion so far has concerned

mainly the frequency of disturbance.However, the same reasoning applies tovariations in intensity and area per-turbed; diversity is highest when distur-bances are intermediate in intensity orsize, and lower when disturbances are ateither extreme. For example, if a distur-bance kills all organisms over a verylarge area, recolonization in the centercomes only from propagules that cantravel relatively great distances and thatcan then become established in open, ex-posed conditions. Species with suchpropagules are a small subset of the totalpool of species, so diversity is low. Incontrast, in very small openings, mobil-ity is less advantageous: the ability to be-come established and grow in the pres-ence of resident competitors and naturalenemies is critical. In addition, recolo-nizing propagules are more likely tocome from adults adjacent to the smallopening. Therefore, colonizers will againbe a small subset of the available pool ofspecies, and diversity will tend to below. When disturbances create inter-mediate-sized openings, both types ofspecies can colonize and the diversityshould be higher than at either extreme.Not only the size, but also the in-

tensity of disturbances makes a dif-ference. If the disturbance was less in-tense so that some residents were dam-aged and not killed, in a large area re-colonization would come both frompropagules and from regeneration of sur-vivors, so that diversity would be greaterthan was the case when all residentswere killed and colonization came onlyfrom new propagules.

Direct evidence linking diversity withvariations in intensity and total area ofdisturbance in tropical communities ismeager. However, there is evidence thatthe processes described above do occur.For example, a 40-kilometer-wide swathof reef in Belize was heavily damaged bya hurricane in 1961, with lesser damageon both sides. Four years later, in themiddle of the swath, new colonies of afew species were present, but the onlysignificant frame-building corals, mainlyAcropora palmata, were the survivors ofthe original storm (20). Ten years latermany of the new colonies were of thisspecies. In contrast, in the zone of lesserdamage, colonies and broken fragmentsof many species had survived the storm24 MARCH 1978

and had regenerated quickly so that re-covery was complete.

Likewise, in rain forests, the size andintensity of a disturbance influences theprocess of recolonization. In a long-termstudy of a small experimental openingmade in a Queensland rain forest, themost successful colonists after 12 yearswere either stump sprouts from survi-vors of the initial bulldozing or seedlingsthat came from adult trees at the edge ofthe clearing (21). Farther from the forestedge, in a much larger clearing, only spe-cies with great powers of seed dispersalhad colonized (22).

It has recently been suggested (23) thatin a nonequilibrium situation, any condi-tions that increase the population growthrates of a community of competitorsshould result in decreased diversity(since faster growth produces fastercompetitive displacement). In placeswith a lower rate of competitive elimina-tion, there is also a greater chance for in-terruption by further disturbances. This"rate of competitive displacement" hy-pothesis is an extension of the inter-mediate disturbance hypothesis andshould be true, other things being equal.How relevant it is for explaining dif-ferences in local diversity remains to beseen. However, present evidence fromtropical communities does not support it.Forests on extreme soils (such as

Fig. 2. Species diver-sity of corals in thesubtidal outer reefslopes at Heron Is-land, Queensland. (A)Changes over 11years on one of thepermanently markedplots on the northslope. The number ateach point gives theyears since the firstcensus at year 0 (nocensuses were madein years 3, 5, and 10).The dashed lines in-dicate changes causedby hurricanes in 1967and 1972. (B) Resultsfrom line transectsdone 3 to 4 months af-ter the 1972 hurri-cane. (A) Data fromthe heavily damagednorth slopes; (0) datafrom the undamagedsouth slope; the linedrawn by eye. Wheredisturbances had ei-ther great or little ef-fect (very low or highpercent cover, respec-tively) there were fewspecies, with maxi-mum numbers ofspecies at intermediatelevels of disturbance.

If

0

E0u 6-0

0U

C 24-0

x, 18-Ez

12-0

0

10 30 50% Cover of Live Coral

70 90

1305

leached white sands, heavy silt, or steepstony slopes) that have slower growthrates than those on less extreme soilshave either few species or strong single-species dominance (24). Likewise, coraldiversity shows little correlation withgrowth rates. Coral diversity varies withincreasing depth, sometimes decreasing,sometimes increasing, or sometimesbeing greatest at intermediate depths.Coral growth rates tend to be faster atintermediate depths (24). Thus, amongneither tropical rain forest trees nor cor-als is there a consistent correlation ofdiversity and growth rates, as predictedby the hypothesis.

In summary, variations in diversity be-tween local stands of these tropical com-munities are more likely to be due to dif-ferences in the degree of past distur-bances than to differences in the rate ofcompetitive displacement during recov-ery from the disturbances. The high di-versities observed in tropical rain foresttrees and in corals on reefs appear to be aconsequence of disturbances intermedi-ate in the scales of frequency and in-tensity.The equal chance hypothesis. In con-

trast to the previous model, let us as-sume that all species are equal in theirabilities to colonize empty spaces, holdthem against invaders, and survive the vi-cissitudes of physical extremes and natu-

ASquare meter plot

1963- 1974

A B20 meter line transects

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ral enemies. Then local diversity wouldsimply be a function of the number ofspecies available and the local popu-lation densities. The species compositionat any site would be unpredictable, de-pending upon the history of chance colo-nization.What conditions would produce this?

First, for all species the number of young(such as larvae and seeds) invading emp-ty places must be independent of thenumber produced by the parent popu-lation. Otherwise, any species that in-creased its production of offspring perparent would progressively increase atthe expense of those with lesser produc-tion. Second, any occupant must be ableto hold its place against invaders until itis damaged or killed. Otherwise, anyspecies that evolved the ability to oust anoccupant would also progressively in-crease. Last, all species must be equal inability to resist physical extremes andnatural enemies. Otherwise, the most re-sistant species will gradually increase, aswas discussed in the previous hypothe-sis.Do communities exist that satisfy

these conditions? Sale (25) has proposedthat certain guilds of coral reef fish do.He assumes that, as with some temper-ate fish, recruitment to newly vacatedsites is independent of the stock of eggsreleased into the plankton. One mustprobably assume that the fecundity andmortality of all species are equal. The ju-veniles grow quickly after they colonizeto vacant places, and thus they are ableto hold their territory against further in-vasion by smaller juveniles of any spe-cies from the plankton. Space is limiting,as judged from the rapid colonization ofvacated sites. Since the juvenile fishseem to be generalists in the use of foodand space, Sale suggests that local diver-sity would be a function of chance colo-nization from the available pool of spe-cies. Clearly, the initial assumption of in-dependence of stock and recruitment iscritical and needs to be tested for thesetropical fish.

Likewise, for rain forest trees, Aubre-ville (26) has suggested that many spe-cies have such similar ecological require-ments that it would be impossible to pre-dict which subset would occur togetheron a site. He based this suggestion on theobservation that some of the commonerlarge trees on his study plot in the IvoryCoast had few or no offspring on theplot. He inferred that their offspringmust be elsewhere, so that the speciescomposition of the forest would contin-ually shift in space and time. While thismight be so, his original observation offew offspring could be explained if the

1306

forest was an old secondary one, similarto Jones' (10) in Nigeria.Other characteristics of trees and cor-

als do not satisfy the requirements of theequal chance hypothesis. For example,dispersal of propagules of many treesand corals is quite restricted so that localrecruitment of juveniles may not be asindependent of local production of prop-agules as it apparently is in some fishpopulations. Likewise, species differ infecundity, competitive ability, and resist-ance to environmental stresses, and thedifferences often result in predictablepatterns of species distribution along en-vironmental gradients (27). Therefore, itseems unlikely that either rain foresttrees or corals conform to the equalchance hypothesis.The gradual change hypothesis. This

model was suggested by Hutchinson (28)to explain why many species coexist inphytoplankton assemblages. Seasonalchanges in, for example, temperatureand light, occur in a lake, and differentspecies are assumed to be competitivelysuperior at different times. It is pos-tulated that no species has time to elim-inate others before its ability to winin competition is reduced below thatof another species by changes in theenvironment.

Climates change on all time scalesfrom seasonal to annual to millennial andlonger, and hence, this hypothesis mayapply to organisms with any length ofgeneration. With long-lived organismssuch as trees or corals, gradual changesin climate over several hundred yearsrepresent the same scale as seasons do toa phytoplankton community. Drier peri-ods producing a savanna vegetation inregions now covered with rain forest oc-curred about 3000 and 11,000 years agoin the Amazon basin; similar changes oc-curred in Africa and Australia (29). AsLivingstone (30) pointed out, "Climateschange and vegetational adjustments arenot rare and isolated events, they are thenorm." As climates changed, marinetransgressions shifted and altered coralreef environments (31).Whether such gradual transitions

would also produce the highly intermin-gled diverse assemblages seen in presentforests and reefs depends on the rate ofcompetitive elimination compared to therate of environmental change. If the timerequired for one tree species to eliminateanother in competition is much shorterthan the time taken for an environmentalchange that reversed their positions inthe hierarchy, they would not coexist.Therefore, very slow changes would notmaintain diversity, but higher ratesmight do so.

Equilibrium Hypotheses

The niche diversification hypothesis.The key point in this model is the degreeof specialization to subdivisions of thehabitat. For a given range of habitat vari-ation, more species can be packed in themore they are specialized. The questionis: Are the species so often observed liv-ing in diverse local assemblages suffi-ciently specialized to coexist at equilibri-um? Some ecologists believe that motileanimals have reached the required de-gree of specialization, particularly if dif-ferent aspects of habitat subdivision areconsidered (32). The different aspectssuch as food, habitat space, and time ofactivity are called "niche axes."

Specialization along niche axes doesnot seem to have evolved to this extentin plants and in sessile aquatic animalssuch as corals. For long-lived organismsthere exists no regular temporal varia-tion to which they could have special-ized. Plants in general have not special-ized along the food niche axis. They allhave similar basic resource requirements(such as light, water, carbon dioxide,and mineral nutrients). Niche sub-divisions are made on degrees of toler-ance to different quantities of these re-sources. As a consequence, plants sub-divide space along gradients of quan-titative variations in light, water, andnutrients. These variations are often as-sociated with variations in elevation,slope, aspect, soil type, understory posi-tion, and so on. Exceptions to this ideaare marine algae that have adapted to thequalitative changes in wavelength oflight at different depths. General obser-vations and some statistical analyses (12,15, 33) have revealed associations be-tween sets of species and certain sub-divisions of the habitat in tropical rainforests, for example, to broad variationsin soil properties (such as parent materi-al, drainage, and tip-up mounds and hol-lows at the roots of fallen trees), and to-pography (ridges, steep slopes, creekmargins, and so on). Other analyses haveshown little association between speciesand local soil types (15, p. 188). As wasdiscussed earlier, plants are also special-ized according to differences in habitatscaused by variations in the frequencyand intensity of disturbance. The after-math of a disturbance presents a new lo-cal environment in which species withdifferent traits are at an advantage. It hasbeen suggested that tropical trees mayhave subdivided this niche axis finely(34); at present there is little direct evi-dence to support this view. It seems un-likely that tropical trees are so highlyspecialized to such small differences in

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the local physical environment that morethan 100 species of trees could coexist atequilibrium on a single hectare of rainforest. In fact, the forests closest to equi-librium are those dominated by a singletree species, as was discussed earlier.

Corals seem as general in their re-quirements as trees; for example, al-though some of their energy comes fromfeeding on zooplankton, much comesfrom photosynthesis by their symbioticzooxanthellae, which consist of a singlespecies in all coral species studied todate, although several different strainsdetected by electrophoresis show somedegree of specificity (35). It has beensuggested (36) that corals have dif-ferentiated along the food niche axis be-tween the extremes of autotrophy andheterotrophy. However, in shallow wa-ter where both light and species diversityis high, this differentiation could pro-mote the coexistence of several specieson the same space only if they werestratified vertically, autotrophs above,heterotrophs in the understory. Yet thelayering observed thus far has not re-vealed specialized "shade" speciesadapted for life in the understory. Coralshave been seen beneath open-branchedspecies such as the Caribbean Acroporacervicornis (37) but, to my knowledge,never beneath close-branched species.One might expect that hetertrophywould be advantageous where light is re-duced by deeper water. Yet there is evi-dence that a predominantly autotrophiccoral was able, over a day's time, tomeet its energy requirements down to awater depth of 25 meters (38). Thus, theproposed niche differentiation along thefood axis has apparently contributedlittle to coexistence, and corals seemvery generalized in their use of re-sources. On the habitat niche axis, coralsare also generalized. Although some spe-cies are confined to certain zones, mostcorals have broad ranges of distributionwith respect to depth and location onreefs, which indicates little precise spe-cialization in habitat (39). Thus, like rainforest trees, corals do not seem to havespecialized to the degree required tomaintain the observed high diversities atequilibrium.The circular networks hypothesis.

This model suggests that, instead of thelinear and transitive hierarchy (A elimi-nates B, B eliminates C, implying Aeliminates C) presumed in the other hy-potheses, the competitive hierarchy iscircular (A > B > C, but C eliminates Adirectly). This hypothesis was first ap-plied to sessile invertebrates living be-neath ledges on coral reefs (40). Since itseems unlikely that the same competitive24 MARCH 1978

mechanism could apply throughout suchcircular interactions, the reverse path-way acting against the highest rankedspecies is likely to be a different mecha-nism. For example, if species A and Bovershadow the species below them inthe hierarchy, but C poisons A, the net-work is biologically more plausible. Adifficulty arises if the interactions are notexactly balanced: if A eliminated B first,then C, no longer reduced by B, wouldquickly eliminate A. However, if thespecies in this network competed only inpairs, none would be eliminated.

I tested this hypothesis (18) for inter-actions between adjacent coral colonieson a permanently marked plot (12 spe-cies, 55 colonies, 82 interactions ob-served over 9 years) and found no circu-lar pathways, even though two mecha-nisms, overshadowing and direct extra-coelenteric digestion, were acting. It ismore likely that these networks wouldoperate between more distantly relatedorganisms. The original observations in-volved different phyla of invertebrates(40).Among trees of the rain forest this hy-

pothesis has not been examined. Shad-ing, root competition, and allelopathyare different mechanisms, so that somecircular networks might be possible.However, trees may also be too similarfor this to maintain diversity.The compensatory mortality hypothe-

sis. If mortality falls most heavily onwhichever species is ranked highest incompetitive ability, or, if they are all ofapproximately equal rank and it fallsheaviest on whichever species is com-monest (that is, mortality is frequency-dependent), competitive elimination maybe prevented indefinitely. In tropical for-ests, if herbivores attack and kill seedsor seedlings of common species morefrequently and to a greater extent thanthey attack those of less common or rarespecies competitive elimination could beprevented. For example, if herbivoresattack the offspring of a species moreheavily nearer than farther from the par-ent tree, that species would probably notbe able to form a single-species grove(41). This possibility has been tested byeither observations or field experimentsand rejected for four out of five speciesof seeds of rain forest trees and vines,but not rejected for seedlings in two oth-er species (41, 42). In the analysis report-ed in Table 1, the mortality of seedlingsor saplings did not increase significantlywith their abundance. Thus, mortality ofyoung trees is not generally frequency-dependent. Destruction of trees by ele-phants also does not seem to be com-pensatory. In Ugandan rain forests it has

been observed (43) that elephants prefer-entially destroy young of the fast-grow-ing early and middle succession trees,leaving the young of the late successionironwood alone, thus hastening progres-sion toward the low-diversity forest.Therefore, contrary to my own earlierwork on this aspect (41), I feel that whilecompensatory mortality may occur insome instances it does not seem to be agenerally important factor in maintainingthe high diversity of mixed tropical rainforests.

Watt's (44) "cyclic succession" isprobably an example of this mechanism.The dominant species does not replaceitself; other species intervene before thedominant becomes reestablished. Thisprocess has never, to my knowledge,been demonstrated in the tropics, butthere seems no reason not to expect it tohappen there.

In coral reefs, some predation doesnot act in a frequency-dependent fash-ion. An earlier claim (45) that the starfishAcanthaster planci might act in this wayhas now been demonstrated to be in er-ror. Studies in Hawaii and Panama (46)indicate that the starfish attacks rarerspecies preferentially, which would re-duce diversity. Studies in a much morediverse coral community on Saipan (47)suggest that Acanthaster might eliminatecertain preferred species, although nodata were given which indicated whetherthese were the common or rare species.In Panama, evidence indicates that othertypes of predators may possibly act in acompensatory manner, increasing diver-sity (17, 46).

In my studies of corals I found that thephysical environment can inflict mortali-ty in a manner that compensates for thecompetitive advantage of branching spe-cies that overshadow others. I measuredthe mortality of corals over a 4-year peri-od that included a hurricane at Heron Is-land in Queensland (18). As describedabove, I had ranked these species incompetitive ability by observing dynam-ic interactions over a period of 9 years onpermanent quadrats. On the part of thereef crest that was badly damaged by thehurricane, the mortality of those speciesof corals that ranked high in the com-petitive hierarchy was much greater thanthose that ranked low. In contrast, thehigh-ranked species on an undamagedpart of the reef crest had a lower mortali-ty than low-ranked species, over thesame period. The reason for the dif-ference was that the high-ranked coralswere branching species observed togrow above their neighbors, over-shadowing and thus killing them. How-ever, these branching species were more

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heavily damaged in the storms. Thus,species of corals that ordinarily win incompetition suffer proportionately morefrom storm damage, compensating fortheir advantage.

In certain situations, diversity, insteadof decreasing with high coral cover (Fig.2), increases. This occurs on the veryshallow reef crests at Heron Island and isdue to compensatory mortality. Thelarger colonies that are spreading hori-zontally and eliminating their neighborstend to die in the center, where theyhave grown up above the low tide level.This provides open spaces in which newspecies can colonize. Thus, on the reefcrest no species is capable of monopo-lizing the space, in contrast to the slopesituations shown in Fig. 2B.High diversity at high cover has also

been found in the Caribbean, and it wasproposed that a balance in competitiveabilities exists at equilibrium (48). Last,it occurred in the deepest samples atEilat, Red Sea (49). Although no ex-planation was suggested for this last-mentioned instance, it and the Caribbeanone could be explained by the inter-mediate disturbance hypothesis. In bothcases, the slope is steep where diversityis highest. In such places, small-scaledisturbances occur by slumping of coralblocks (17, 46). The deep corals at Eilatare very small (more than 100 colonies insome 10-meter line transects), whichmight indicate that they are recent colo-nists after local disturbances.

Tests of the Hypotheses

Hypotheses are made to be tested,and, in ecology, field experiments are of-ten an excellent way to do so (50). Theintermediate disturbance hypothesis canbe tested in various ways. It will be nec-essary to verify that the sequence ob-served by Eggeling (8) also occurs in oth-er rain forests. Probably the best way todo this would be to examine gaps of vari-ous sizes within forests dominated by asingle species. In very small openingsthe shade-tolerant offspring of the domi-nant should grow and survive better thanother species, whereas in larger open-ings, juveniles of less shade-tolerant spe-cies should perform better. To estimatethe probability of replacement, onewould need to measure the abundanceand sizes of each species having juve-niles in the light gap, and if possible theirrates of growth and mortality.Even better than such observations

are experimental transplants into dif-ferent-sized light gaps of seedlings ofspecies whose adults live in mixed and in

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single-dominant stands. These experi-ments would test the prediction that thespecies of the single-dominant standswill be more successful in small openingsnear the parent tree, whereas those ofmixed stands will be more successful inlarger openings. The alternative hypoth-esis, that single-dominant stands are dueto poor soils, could be tested by experi-mentally improving soils (by draining,for example, or by fertilizing) and thenplanting seedlings of species that do ordo not live in poor soils, in these plotsand in unmodified control plots.

Tests of the equal chance hypothesisinvolve determining whether recruitmentis (i) independent of adult stock, and (ii)equal among the different species. This isa difficult problem if propagules are dis-tributed widely. In addition, equality inability to resist invaders, extremes of thephysical environment, and natural ene-mies must be established. Sale (25) hasmade a start on this in his experimentswith coral reef fish.The hypothesis of continual change is

difficult to test because of the impracti-cality of determining the fate of orga-nisms as long-lived as trees or corals.Pollen records in lake sediments are sel-dom precise enough to distinguish spe-cies, although genera are often identi-fiable.Attempts to test the niche-diversifica-

tion hypothesis are sometimes made bypostulating how the different speciescould divide up resources and thenseeing whether the coexisting speciesoverlap significantly in their use of re-sources. The degree of overlap is some-times judged indirectly by the range ofvariation in those aspects of morphologyassociated with resource use, such asroot depth in plants, or degree of branch-ing and polyp size in corals. However,these indirect measures are open to thecriticism that the particular resourcechosen (or the structure used to indicateit) may not be the one for which the spe-cies are competing. Another criticism isthat competition may not be taking placethrough superior efficiency in exploitingresources, but by superior ability in in-terfering with competitors. Until a pre-cise definition of the range of resourcesof each species is specified, this hypothe-sis will remain untestable.The circular networks hypothesis

might be tested either by observing asmany interactions as possible, or better,by transplanting individuals into mixedand single-species groups. Since circularnetworks are apparently rare, many rep-licate observations must be made if sucha network is found. For example, if asingle set of observations indicated that

(A > B > C > A), further observationsmight uncover an instance where(A > C), indicating "equal chance,"which I found in observing coral inter-actions (18).The compensatory mortality hypothe-

sis can be tested in various ways. Obser-vations of density and mortality beforeand after storms or predator attackswould reveal whether highly ranked spe-cies suffered greater mortality (18). Ex-periments in which seeds were placedboth near and far from adult trees, or inboth dense clumps and sparsely, havebeen done with several species of tropi-cal trees (41, 42). Observations on themortality of naturally occurring seed-lings and on experimental plantings bothnear and far from adults have also beenmade (11). In addition, I have used cagesto exclude insects and larger herbivoresfrom seeds and seedlings, using open-sided cages as controls. The purpose wasto establish whether natural enemies actin a compensatory way. The experi-ments done so far should be regarded aspilot ones, since they were done withfew replicates on a few species. More ex-periments need to be done before therole of compensatory mortality can beestablished.

Conclusion

This article discusses two opposingviews of the organization of assemblagesof competing species such as tropicaltrees or corals. One is that stability usu-ally prevails, and, when a community isdisturbed, it quickly returns to the origi-nal state. Natural selection fits and ad-justs species into this ordered system.Therefore, ecological communities arehighly organized, biologically accommo-dated, coevolved species assemblages inwhich efficiency is maximized, life his-tory strategies are optimized, popu-lations are regulated, and species com-position is stabilized. Tropical rain for-ests and coral reefs are generally re-garded as the epitomes of such orderedsystems. The last three hypotheses pre-sented in this article detail the mecha-nisms that may maintain these systems.

In the contrasting view, equilibrium isseldom attained: disruptions are so com-mon that species assemblages seldomreach an ordered state. Communities ofcompeting species are not highly orga-nized by coevolution into systems inwhich optimal strategies produce highlyefficient associations whose speciescomposition is stabilized. The first threehypotheses represent this view.My argument is that the assemblages

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of those organisms which determine thebasic physical structure of two tropicalcommunities (rain forest trees and cor-als) conform more closely to the non-equilibrium model. For these organisms,resource requirements are very general:inorganic substances (water, carbondioxide, minerals) plus light and space,and, for corals, some zooplankton. It ishighly unlikely that these can be parti-tioned finely enough to allow 100 or morespecies of trees to be packed, at equilib-rium, on a single hectare (12). Instead, ifcompetition is allowed to proceed un-checked, a few species eliminate therest. The existence of high local diversityin the face of such overlap in resourcerequirements is a problem only if one as-sumes equilibrium conditions. Discardthe assumption and the problem van-ishes.

Although I have presented these ideasas separate hypotheses, they are not mu-tually exclusive. Within a local area,there are usually enough variations inhabitats and resources to enable severalspecies to coexist at equilibrium as a re-sult of niche differentiation. In addition,a certain amount of compensatory mor-tality probably occurs, as some evidencefrom rain forests indicates (41, 42). Inspecial circumstances, circular networksmight also increase diversity. Thus, acertain amount of local diversity wouldexist under equilibrium conditions.However, climates do change gradu-

ally, which probably results in changesin the competitive hierarchy. On a short-er time scale, disturbances frequently in-terrupt the competitive process. Thesevariations prevent most communitiesfrom ever reaching equilibrium. In cer-tain special cases, species may be soalike in their competitive abilities and lifehistory characteristics that diversity ismaintained by chance replacements.Thus, all six hypotheses may contrib-

ute to maintaining high diversity. Mycontention is that the relative importanceof each is very different. Rather thanstaying at or near equilibrium, most localassemblages change, either as a result offrequent disturbances or as a result ofmore gradual climatic changes. Thechanges maintain diversity by preventingthe elimination of inferior competitors.Without gradual climatic change or sud-den disturbances, equilibrium may bereached; diversity will then be main-tained by the processes described in thehypotheses of niche diversification, ofcircular networks, and of compensatorymortality, but at a much lower level thanis usually observed in diverse tropicalforests and in coral reefs.

Although tropical rain forests and cor-24 MARCH 1978

al reefs require disturbances to maintainhigh species diversity, it is important toemphasize that adaptation to these natu-ral disturbances developed over a longevolutionary period. In contrast, someperturbations caused by man are of aqualitatively new sort to which these or-ganisms are not necessarily adapted. Inparticular, the large-scale removal oftropical forests with consequent soil de-struction (51), or massive pollution bybiocides, heavy metals, or oil, are quali-tatively new kinds of disturbances,against which organisms usually havenot yet evolved defenses. Tropical com-munities are diverse, thus species popu-lations are usually smaller than those intemperate latitudes, which increases thechances that such new disturbances willcause many species extinctions.

References and Notes

1. Equilibrium of species composition is usuallydefined as follows: (i) if perturbed away from theexisting state (equilibrium point or stable limitcycle), the species composition would return toit; (ii) without further perturbations, it persists inthe existing state. A perturbation is usually re-garded as a marked change; death and replace-ment of single trees or coral colonies would notqualify.

2. J. Diamond, in Ecology and Evolution of Com-munities, M. L. Cody and J. Diamond, Eds.(Belknap, Cambridge, Mass., 1975), p. 343.

3. For discussions on ecological stability, naturalbalance, and related topics, see F. E. Clements,Carnegie Inst. Wash. Publ. 242, 1 X1916); A. J.Nicholson, J. Anim. Ecol. 2, 132 (1933); L. B.Slobodkin, Growth and Regulation of AnimalPopulations (Holt, Rinehart and Winston, NewYork, 1961), p. 46; R. M. May, Stability andComplexity in Model Ecosystems (PrincetonUniv. Press, Princeton, N.J., 1973); R. M. May,Ed., Theoretical Ecology (Saunders, Phila-delphia, 1976), pp. 158-162.

4. For discussions of nonequilibrium communities,see H. A. Gleason [Bull. Torrey Bot. Club 43,463 (1917)] and H. G. Andrewartha and L. C.Birch [The Distribution and Abundance ofAni-mals (Univ. of Chicago Press, Chicago, 1954),pp. 648-65]. The case for the importance of ca-tastrophes in keeping forests away from an equi-librium state is discussed in several of the sub-sequent references. See also J. D. Henry and J.M. A. Swan, Ecology 55, 772 (1974); H. E.Wright and M. L. Heinselman, Quat. Res.(N. Y.) 3, 319 (973). For corals, see D. W. Stod-dart [in Applied Coastal Geomorphology, J. A.Steers, Ed. (Macmillan, New York, 1971), pp.155-197; Nature (London) 239, 51 (1972)]. Thecase for catastrophes on a geological scale isconvincingly presented by C. Vita-Finzi [RecentEarth History (Wiley, New York, 1973)] and D.V. Ager [The Nature of the Stratigraphical Rec-ord (Wiley, New York, 1973)].

5. It has been suggested that the term diversity berestricted to measures that include the relativeabundance of species. However, since speciesnumber is certainly an indicator of diversity inthe common usage of the word and since it isalmost always closely correlated with indicesbased on relative abundance (16), I use the num-ber of species as a measure of diversity.

6. R. W. Osman and R. B. Whitlatch, Paleobiol-ogy, in press.

7. A recent summary of various models of ecologi-cal succession is given by J. H. Connell and R.0. Slatyer [Am. Nat. 111, 1119 (1977)].

8. W. J. Eggeling, J. Ecol. 34, 20 (1947).9. Later surveys are summarized by I. Langdale-

Brown, H. A. Osmaston, and J. G. Wilson [TheVegetation of Uganda and Its Bearing on Land-Use (Government of Uganda, Kampala, 1964)];they point out that in certain smaller forests inUganda, the ironwood occurs in pure standsmainly on poorer soils. However, this is not thecase in the Budongo forest, by far the most ex-tensive in Uganda.

10. E. W. Jones, J. Ecol. 44, 83 (1956).11. J. H. Connell, J. G. Tracey, L. J. Webb, in prep-

aration.

12. P. W. Richards, The Tropical Rain Forest (Cam-bridge Univ. Press, Cambridge, 1952).

13. Forests dominated by single species are com-mon in northern South America; examples arespecies ofMora, Eperua, Ocotea, Dicymbe, Di-morphandra, Aspidosperma, and Peltogyne. InAfrica, the dominants are species of Mac-rolobium, Cynometra, Berlinia, Brachystegia,Tessmannia, and Parinari. In Southeast Asia,they are species of Eusideroxylon, Dryobala-nops, Shorea, and Diospyros. It is important todistinguish climax stands from colonizing for-ests that are also often dominated by a singlecanopy species that, in contrast, has few or nooffspring in the understory (Fig. 1).

14. T. A. W. Davis, J. Ecol. 29, 1 (1941).15. T. C. Whitmore, Tropical Raih Forests of the

Far East (Clarendon, Oxford, 1975).16. R. W. Grigg and J. E. Maragos, Ecology 55, 387

(1974); Y. Loya, ibid. 57, 278 (1976).17. P. W. Glynn, R. H. Stewart, J. E. McCosker,

Geol. Rundsch. 61, 483 (1972).18. J. H. Connell, in Coelenterate Ecology and Be-

havior, G. 0. Mackie, Ed. (Plenum, New York,1976), pp. 51-58.

19. J. Lang, Bull. Mar. Sci. 23, 260 (1973).20. D. R. Stoddart, in Proceedings of the Second

International Coral Reef Symposium, P. Mather,Ed. (Great Barrier Reef Committee, Brisbane,Australia, 1974), vol. 2, p. 473.

21. L. J. Webb, J. G. Tracey, W. T. Williams, J.Ecol. 60, 675 (1972).

22. M. Hopkins, thesis, University of Queensland,Brisbane, Australia (1976).

23. M. Huston, Am. Nat., in press.24. For variations in tropical tree diversity and

growth rates, see (12) and D. H. Janzen,Biotropica 6, 69 (1974). Coral diversity may ei-ther increase or decrease with depth or be high-est at intermediate depths. See J. W. Wells,U.S. Geol. Surv. Prof. Pap. 260, 385 (1954); D.R. Stoddart, Biol. Rev. 44, 433 (1969); J. E. Ma-ragos, Pac. Sci. 28, 257 (1974); T. F. Dana,thesis, University of California at San Diego(1975); Y. Loya, Mar. Biol. 13, 100 (1972); T. J.Done, in Proceedings ofthe Third InternationalCoral Reef Symposium, D. L. Taylor, Ed.(Univ. of Miami, Fla., 1977), vol. 1, p. 9.Growth of corals has been found to be greaterat intermediate depths: see P. H. Baker and J.N. Weber, Earth Planet. Sci. Lett. 27, 57 (1975);S. Neudecker, in Proceedings ofthe Third Inter-national Coral Reef Symposium, D. L. Taylor,Ed. (Univ. of Miami, Fla., 1977), vol. 1, p.317.

25. P. Sale, Am. Nat. 111, 337 (1977).26. A. Aubreville, Ann. Acad. Sci. Colon. Paris 9,

1 (1938).27. R. H. Whittaker, Taxon 21, 213 (1972).28. G. E. Hutchinson,Am. Nat. 75, 406 (1941); ibid.

95, 137 (1961).29. J. Haffer, Science 165, 131 (1969); B. S. Vuilleu-

mier, ibid. 173, 771 (1971); A. Kearst, R.L. Crocker, C. S. Christian, Biogeographyand Ecology in Australia Monogr, Biol. 8 (1959).

30. D. A. Livingstone, Ann. Rev. Ecol. Syst. 6, 249(1975).

31. D. R. Stoddart, Symp. Zool. Soc. London 28, 3(1971); J. G. Tracey and H. S. Ladd, in Pro-ceedings ofthe Second International Coral ReefSymposium, P. Mather, Ed. (Great Barrier ReefCommittee, Brisbane, Australia, 1974), vol. 2,p. 537; D. Hopley, in ibid., p. 551.

32. T. W. Schoener, Science 185, 27 (1974).33. W. T. Williams, G. N. Lance, L. J. Webb, J. G.

Tracey, J. H. Connell, J. Ecol. 57, 635 (1969);M. P. Austin, P. S. Ashton, P. Grieg-Smith,ibid. 60, 305 (1972).

34. R. Ricklefs, Am. Nat. 111, 376 (1977).35. D. A. Schoenberg and R. K. Trench, in Coe-

lenterate Ecology and Behavior, G. 0. Mackie,Ed. (Plenum, New York, 1976), pp. 423-432.

36. R. K. Trench, Helgol. Wiss. Meeres 26, 174(1974); J. W. Porter, Am. Nat. 110, 731 (1976).

37. J. Lang, personal communication.38. D. S. Wethey and J. W. Porter, in Coelenterate

Ecology and Behavior, G. 0. Mackie, Ed. (Ple-num, New York, 1976), pp. 59-66.

39. T. F. Goreau, Ecology 40, 67 (1959). See also(17) and (24).

40. J. B. C. Jackson and L. Buss, Proc. Natl. Acad.Sci. U.S.A. 72, 5160 (1975); M. Gilpin, Am. Nat.109, 51 (1975).

41. D. H. Janzen, Am. Nat. 14, 501 (1970); J. H.Connell, in Dynamics of Populations, P. J. denBoer and GR.R Gradwell, Eds. (PUDOC, Wa-geningen, 1970), pp. 298-312. This mechanismcould also produce the mosaic pattern envisagedby Aubreville (26).

42. D. H. Janzen, Ecology 53, 258 (1972); D. E. Wil-son and D. H. Janzen, ibid., p. 955; D. H. Jan-zen, ibid. p. 350.

43. R. M. Laws, I. S. C. Parker, R. 0. B. John-

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stone, Elephants and Their Habitats (Claren-don, Oxford, 1975).

44. A. S. Watt, J. Ecol. 35, 1 (1947).45. J. Porter, Am. Nat. 106, 487 (1972).46. J. M. Branham, S. A. Reed, J. H. Bailey, J.

Caperon, Science 172, 1155 (1971); P. W. Glynn,Environ. Conserv. 1, 295 (1974); Ecol. Monogr.46, 431 (1976).

47. T. E. Goreau, J. C. Lang, E. A. Graham, P. D.Goreau, Bull. Mar. Sci. 22, 113 (1972).

48. J. W. Porter, Science 186, 543 (1974): "thereappears to be a balance of abilities dividedamong the Caribbean corals such that no one

species is competitively superior in acquiringand holding space. The effect of this balance ofcompetitive abilities is to retard, even in high-density situations, the rapid competitive ex-clusion that takes place on undisturbed easternPacific reefs" (p. 544); L. A. Maguire and J. W.Porter, Ecol. Modelling 3, 249 (1977).

49. Y. Loya, Mar. Biol. 13, 100 (1972).50. J. H. Connell, in Experimental Marine Biology,

R. Mariscal, Ed. (Academic Press, New York,1974), pp. 21-54.

51. A. G6mez-Pompa, C. Vizquez-Yanes, S. Gue-vara, Science 177, 762 (1972).

52. I thank the foliowing for critical discussions andreadings of earlier drafts: J. Chesson, P. Ches-son, J. Dixon, M. Fawcett, L. Fox, S. Hol-brook, J. Kastendiek, A. Kuris, D. Land-enberger, B. Mahall, P. Mather, J. Melack, W.Murdoch, A. Oaten, C. Onuf, R. Osman, D.Potts, P. Regal, S. Rothstein, W. Schlesinger, S.Schroeter, A. Sih, W. Sousa, R. Trench, R.Warner, G. Wellington, and two anonymous re-viewers. Supported by NSF grants GB-3667,GB-6678, GB-23432, and DEB-73-01357, and byfellowships from the J. S. Guggenheim Memo-rial Foundation.

Undoubtedly the best-known effortsto assess the quality of doctoral pro-grams in recent years have been the col-lection of prestige or reputational ratingsby the American Council on Education(ACE) in 1964 (1) and 1969 (2). In thosesurveys the ACE obtained from samplesof university faculty members ratings ofthe quality of graduate faculties in theirown fields at other U.S. institutions. Inaddition to serving their primary purposein the graduate education community,these surveys produced data that havebeen used to gain a better understandingof the meaning of reputational ratings,particularly how they are related to othercharacteristics of doctoral programs. Asa result, we have learned that the reputa-tional ratings-often called peer rat-ings-tend to be fairly highly related toprogram size (3, 4) and various indices ofresearch productivity (4, 5), though themagnitude of these relationships variesconsiderably across disciplines. In par-ticular, it appears that the ratings aremore highly correlated with various tra-ditional measurements (for example,number of Ph.D.'s produced, levels offunding) in the biological and physicalsciences than in the social sciences orthe humanities. One plausible explana-tion for this is that in the biological andphysical sciences there tends to be great-er consensus about accepted knowledgeand standards (6).There has been a good deal of concern

The authors are research psychologists at Educa-tional Testing Service, Princeton, New Jersey08540.

about the use of reputational ratings inmaking judgments about program quali-ty. The chief objections have been (i)that the ratings are unfair to doctoralprograms which do not place primaryemphasis on doing research and pre-paring their students to do research; (ii)that there is a strong halo effect, the rat-ings of a department being unduly af-fected by the prestige or reputation ofthe university of which it is a part; (iii)that there is a time lag, that is, the ratingsare usually based on impressions of whata department used to be like, not onknowledge of its current strengths andweaknesses; and (iv) that the rating in-formation seldom makes for a betterunderstanding of a specific program'sstrengths and weaknesses and thereforeis not useful for program improvement.

It was largely in response to some ofthese dissatisfactions with reputationalratings that the Council of GraduateSchools (CGS) and Educational TestingService (ETS), in 1975, conducted a mul-tidimensional study of quality in doctoralprograms in three disciplines (7). Thisproject was designed primarily as a studyof the feasibility of employing informa-tion about a wide variety of character-istics in making judgments about thequality of programs. An important fea-ture of the project was the idea that asingle ranking is too simplistic, that itdoes not allow for the possibility thatdoctoral programs relatively strong inone respect (such as publication rates ofthe faculty) might be less strong in anoth-er (such as the quality of their teaching).

A major procedural characteristic wasthat most of the information collectedfrom respondents had to do with theirown departments; for example, facultymembers reported their own publicationrates or journal-refereeing activities, stu-dents their opinions about the quality ofteaching they received, alumni their dis-sertation experiences, and so on. Thesereports were obtained from students,faculty, and alumni by means of ques-tionnaires. A general conclusion of thestudy was that such reports can be ob-tained without great difficulty, are usual-ly reliable, and augment the descriptionof characteristics relevant to appraisalsof doctoral program quality.Though they were not a crucial ele-

ment in the CGSIETS study, peer ratingswere also obtained from the faculty re-spondents, each of whom was asked torate the quality of the faculties of the oth-er departments in his or her disciplinewhich participated in the study. This as-pect of the CGS/ETS study paralleledth-e two earlier ACE surveys, and it isthis aspect of the CGS/ETS study that isthe focus of this article.The primary reason for obtaining the

peer ratings was to examine their rela-tionship to the broader array of programcharacteristics reported in the main partof the survey, a line of inquiry that wasnot possible with either of the earlierACE studies. But interest in peer ratingsper se remains strong. The ConferenceBoard of the Associated Research Coun-cils convened a planning conference, inthe fall of 1976, to investigate issues in-volved in conducting another peer ratingsurvey (8). In spite of ACE's announcedintention of refraining from further ef-forts of this kind, it appears likely thatsome agency concerned with graduateeducation in the United States will con-duct some kind of reputational ratingsurvey in the not too distant future. Ourinterest in an improved understanding ofthe nature and meaning of peer ratingstherefore goes beyond pure intellectualcuriosity.

This article draws on the data gatheredin the CGS/ETS study (7) and the twoearlier ACE studies (1, 2) to address

SCIENCE, VOL. 199, 24 MARCH 1978

Reputational Ratings ofDoctoral Programs

Rodney T. Hartnett, Mary Jo Clark, Leonard L. Baird

0036-8075/78/0324-1310$0l.MO/0 Copyright C 1978 AAAS1310

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