diversity, utilization of resources, and adaptive ...

DIVERSITY, UTILIZATION OF RESOURCES, AND ADAPTIVE RADIATION IN SHALLOW-WATER MARINE INVERTEBRATES OF TROPICAL OCEANIC ISLANDS Alan J. Kohn2 Department

of Zoology,

University

of Washington,

Scattlc

98105

AHSTRACT

Important features of the inshore marine benthic invertebrate fauna of tropical islands are very high species diversity and the gcomorphological role of reef-building and sediment-gcncrating animals in contributing the structural framework of habitats. The former is due to the adaptive radiation and pcrsistcnt co-occurrence of large numbers of species in a number of genera, particularly of molluscs, echinoderms, and crustaceans. Among the molluscs, epifaunal gastropod genera contribute importantly to the high species diversity. On tropical Indo-West Pacific island shores and coral reefs, 80% of prosobranch gastropods belong to genera having more than three sympatric species; in diverse temperate faunas the corresponding figure is 20%. Features of the environment and of the animals tending to promote both speciation and high faunal diversity are listed: environmental heterogeneity and ecological and behavioral specialization are the most approachable. In a reprcscntative gastropod genus (Co?zus) with available quantitative ecological data, topographically complex, climatically equable subtidal coral reefs support more species, lower population density, and animals of larger size than do intertidal marine benches that are topographically uniform but subject to more severe weather conditions. Recurrent group analysis shows strong affinity among six common species on reefs and three on benches spanning most of the longitudinal extent of the Indo-West Pacific region, demonstrating wide species distribution and constancy of spccics composition in these habitat types. Degree of specialization and overlap in resource utilization by co-occurring congeneric speciesare discussed with reference to the theory of limiting similarity. Conus species arc demonstrated to specialize more to different prey species than to substrate type. A more that co-occurring, ecologically similar predator species tend to adopt general hypothesis, this strategy, while detritus feeders are more likely to specialize to microhabitat than food type, is only partially supported by the limited data available on other benthic invertebrate taxa.

INTRODUCTION

Like tropical wet forests among terresthe coral reefs surtrial environments, rounding tropical oceanic islands are small portions of the marine realm with very high faunal diversity. Despite this common feature, viewed as wholes these two l Supported by National Science Foundation Grant GB-17735. Fieldwork supported by National Science Foundation Grant Cl7465 as part of U.S. Program in Biology, International Indian Portions of this paper were Ocean Expedition. presented at the Association for Tropical Biology Symposium on Adaptive Aspects of Insular Evolution, 1969. 2 I thank Margaret Lloyd and Natalie Melcnrck for technical assistance, Dr. J. Felsenstcin for aid with the community matrix analyses, and Drs. R. T. Paine and G. II. Orians for discussion and criticism of the manuscript. LIMNOLOGY

AND

OCEANOGRAPHY

community types differ strikingly in habitat structure and ecosys tern organization, aside from the obvious contrasts in physicochemical properties of fluid medium and solid substratum. In the wet forest, massive primary producer organisms, characterized by low production : biolmass ratios and high biomass : unit of energy flow ratios provide the habitat structure of the community, enhancing spatial complexity and ameliorating the effects of fluctuating external physical factors. Both aspects may be prerequisites for high biotic diversity. On the coral reef, the primary producers are mainly small and inconspicuous algae, with high productivity : biomass and low biomass : unit of energy flow ratios, and habitat structural complexity results mainly

332

MARCH

1971,

V. 16(2)

DIVERSITY

OF

TROPICAI

from elaboration of calcareous cxoskeletons by secondary producers, molluscs and cchinodcrms as well as the corals. Few have attempted to document the occurrence of high faunal diversity in these assemblages, and no satisfactory evaluation exists of tic factors that gcnerate and maintain it. In this paper, I attempt to quantify some aspects of this diversity and to apply some recent contributions to the theory of the ecological niche to evaluate thlc importance of certain factors that can lead to incrcascd Except in broad outline faunal diversity. the community is too complex to be acccssiblc as a who,le. At the prcscnt time it is more profitable to examine picccs of it in detail, and it is of considerable interest to examine taxa containing numerous co-occurring similar species, bccausc they contribute importantly to faunal diversity and bccausc their spccics are likely to have similar environmental rcquircments. I limit most of the detailed consideration to one prominent group of invcrtcbratcs of tropical inshore marine habitats, but available information from other taxa is summarized and evaluated. The . research to bc discussed has attempted mainly to apply data from the study of natural populations to two qucstions: How similar in utilization of resources arc co-occurring, taxonomically similar species in assemblages of varying diversity? And how do the numbers of such species compare with the maximum that could thcorctically coexist in stable rcsourcc-limited populations? NATURE

OF

TROPICAL

INVERTEBRATE

MARINE

DIVERSITY

A general increase in numbers of marinc invertebrate species from Arctic to tropical regions was attributed until recently to diffcrcnces in the cpifauna, animals living on or associated with rocks and other hard substrates; infaunal invertebrates inhabiting sand and mud bottoms were thought not to have pronounced latitudinal diversity gradients (Thorson 1952, 1957). More

MARINE

333

INVERTEBRATES

TABLE 1. Proportions of marine gastropod and bivalve molluscs in temperate and tropical regions. (Data from Kay 1967, and other sources available from author)

Teinpcratc Friday IIarbor, Washington Woods IIole, Massachusetts Plymouth, England Mean Tropical continental islands Philippines Krusadai, India New South Wales Okinawa Mean Tropical oceanic Maldives Hawaii Seychelles Ellicc Kermadec Society Mean

57 59 63

43 41 37

60

40

63 E 79

37 38 29 21

69

31

77 82 82 82 86 87

23 18 18 18 14 13

83

17

islands

rcccntly Sanders (1968) reported pronounced increases in diversity with dccreasing latitude in the bivalve and polychaete assemblages of soft estuarine and marinc oozes (see also Bakus 1969). Bccausc I have obtained detailed comparativc ecological information for one family of largely cpifaunal prosobranch gastropod molluscs, ‘and because this order is an important contributor to increased faunal diversity in the tropics (Thorson 1952), I chose this group as an example for particular emphasis. Table 1 shows that the ratio of species of inshore, shallow-water gastropods and bivalves, the two largest molluscan classes, is about 60 : 40 in temperate and boreal regions but is skewed strongly toward the primarily epifaunal gastropods throughout the tropics (Kay 1967). Moreover, as Kay pointed out the bivalve families with the largest number of species in such habitats in the tropics are primarily epifaunal.

334

ALAN

TEMPERATE 701 -

$701 k

-I

/

J. KOI-IN

TROPICAL CONTINENTAL A

Friday Harb a

West America

“,:g

,“:E=6.5

=I.8

\

TROPICAL OCEANIC L

r

Tropical

Pacific

\

Islands

S= F6.4.4 .:.:.:. G= H; :::::: ;:$$ .:.:.: x .:.:.:. $$$ ?g;:; .;.:.:. ::::::: :.:.:.: :;>;.c ...A.

.g:: :$g; \y$ y.:.:. .gg; $$ .A... ::::::: :::::: y:::: g;g. :::;::: . ..i..:::::::: @ ::::::: .:a:.:.: :.: 111 1

Ma ldive Islands

Krusadai S=250 G=xs=2.5

FIG. 1. The number of genera containing gastropod molluscs in different regions. (Data

“,:?$=4.2

different numbers of sympatric from various sources available

The relative contribution to diversity by genera also rcvcals a pattern of geographic variation. In temperate regions, the number of co-occurring species in a genus or family is usually low even in the most diverse faunas ( Fig. 1) . Contras tingly, a number of primarily tropical families and genera have undergone remarkable adaptive radiations, so that they arc character-

species of prosobranch from author.)

ized by large numbers of co-occurring species. For example, at Woods Hole ( Massachusetts), Friday Harbo,r (Washington ) , and Plymouth ( England ) , where large marine laboratories were sited to take advantage of the rich marine biota, 80% of all species of prosobranch gastropods belong to genera having three or fcwcr sympatric species, while in the Indo-

DIVERSlTY

OF

TROPICAL

West Pacific tropics, 80% of species belong to genera having more than three sympatric species (Fig. 2). The same phcnomenon characterizes other invertebrate taxa. In the coral family Acroporidae, for example, 54 species of Acroporn and 30 of Montipora occur in the Marshall Islands (Wells 1954). In tropical Indo-West Pacific Crustacea, “there are about 100 endemic gcncra, among them many with large numbers of species” (Ekman 1953, p, 14). To some extent this reflects the degree of splitting in our classification systcm; in any cast it also reflects phenetic similarity. Although the extant species asscmblagcs presumably result fro’m radiations relatively recent in geologic time, some of the genera involved are known to have had similarly large numbers of co-occurring species as far back as the mid-Tertiary (Hall 1964; see also Stehli et al. 1969). What factors have influenced these strikingly different patterns of adaptive radiation in marine invertcbratc taxa? And what can the comparative ecology of such groups tell us of patterns of tropical insular evolution? One might expect the following features of the environment to promote speciation and high faunal diversity. This hypothesis could be tested by correlation of divcrsity with gradients of the cnvironmcntal variables. 1. Stability of the tropical oceanic environment in ecological and probably evolutionary or geological time; equable physical conditions of insolation, tcmpcrature, salinity, etc. without climatic cxtrcmes. 2. Isolation of appropriate habitats for shallow-water cpifauna; restrictioa to narrow bathymetric and horizontal bands along the edges of oceanic islands, This is especially true of the Indo-West Pacific region, where suitable habitats comprise an infinitesimal fraction of a biogeographic region covering a fourth of the world ocean, 3. Complexity of environments; a prio’ri we cxpcct the most heterogeneous habitats

MARINE

INVERTEBRATES

percent of species of prosFIG. 2. Cumulative to genera ohranch gastropod molluscs belonging containing varying numbers of sympatric species in different regions characterized by marine faunas of high diversity. (Data from various sources available from author. )

to support the largest numbers of species. Since the coral reef structure is entirely biogenic, a positive feedback is possible bctwccn biotic diversity and topographic hetcrogencity of reef structure. 4. Vulcanism and subsidence, resulting in changing dispersion patterns of islands an d archipelagoes in geologic time, contributes to providing new cand changing habitats for colonization and to isolating populations, a requisite for geographic speciation. 5. Surfnce currents of the ocean, including the persistent gyres and equatorial countercurrent in the Pacific and the semiannual shift of current direction >90” with the monsoon in the Indian Ocean, provide transport for pelagic propagules. Traits of animals expected to promote both speciation and high faunal diversity include: I. Pelagic distributive larval stage in the lift history, with II. Large numbers of propagules or larvae, and III. Long-hued Zarvae that feed during dispersal. IV. Extentlecl breeding season; larvae may bc released subject to varying current patterns.

336

ALAN

V. Abundance of predators, which keep prey populations below densities that would lead to competitive exclusion. VI. Specialization of the ecological and behavioral characteristics of the species prcscn t. Taken together, this combination of factors permits Indo-West Pacific species particularly to extend their ranges over a vast region, and to form distinct geographic populations occupying new adaptive zones in rcsponsc to local selective pressures, with the potential for speciation given extrinsic isolating mechanisms, Factors (3) and (VI) are most approachable quantitatively as dimensions of ecological niches, and I have emphasized them in my studies of the comparative ecology of Conus, a primarily tropical prosobranch gastropod genus of several hundred species. Large numbers of spctics (up to 24) co-occur on coral reefs in the tropical Indo-West Pacific; assemblages of fcwcr sp&es, including some single-species populations ( Kohn 1966)) provide comparisons, The group has a number of attributes that are advantageous for comparative ecological study, enumcratcd elsewhere (Kohn lQ68). Here I ask how do the ecological characteristics of Conus species vary (from specialized to generalized in utilization of resources ) in assemblages varying in diversity. I have used this comparative approach, and the advances in theory of the ecological niche due to MacArthur and Levins (1964, 1967), Lcvins ( 1968)) and MacArthur ( 1969) to relate species diversity, resource utilization and habitat complexity in one perhaps exemplary taxoccne” of invertebrates of inshore marine habitats of tropical islands. The model of expected ecological characteristics of Conus in two distinct habitat types (Table 2) is partly a priori, insofar as it is based on factors (3) and (VI) above and rcccnt hypothcscs of adaptive 3 In this paper the terms taxocene and assemblage are used as defined by Hutchinson ( 1067 >.

J.

KOIIN

TABLE

Conus bawd

-

Expected ecological characteristics of populations in different habitat types, on expected selective pressures of the environments 2.

-___

Habitat

type:

HzLbitat Habitat

topography: climate:

--

------

Intertidal marine bench

(type II)

Snbtidal coral reef

Uniform Severe

Expected adaptive strategy with respect to: Species diversity

low

high

Population

high

low

Body

density

size

small

large

Ecological niche breadth with respect to resource utilization

narrow

wide

Ecological niche breadth with respect to climatic variables

wide

narrow

strategies in environments of varying patchiness (MacArthur and Pianka. 1966; Emlen 1966), and partly a posteriori, insofar as it is based on analyses of natural populations of Conus studied to date ( Kohn 1959, 1968). Selection of the two habitat types indicated (Table 2; see also Kohn 1967) for comparison is based oln the facts that 1) both occur commonly throughout the tropical Indo-West Pacific region, the arca of study; 2) both support Conus populations dcnsc enough to warrant quantitative analysis; and 3) they illustrate contrasting environmental conditions. Intertidal marine benches (type II habitats) are topographically rather uniform smooth platforms subject to desiccation and wetting by rain at low tide and heavy wave action at high tide; climatic conditions are thus variable and often severe. In contrast, subtidal coral reef platforms (type III habitats ) are topographically more complex, with patches of different substrate types, but arc always submerged; their “climate” is thus more equable and benign. Intermediate and other habitat types support Conus but these will be treated in more detail clscwherc.

DIVERSITY

OF

TROPICAL

MARINE

337

INVERTEBRATES

C. frigidus (8,6), C. flavidus (93). The first six species listed form a recurrent group. Members of recurrent groups are Species composition of the Conus asfrcqucnt components of each other’s envibenches an d semblages of intertidal ronmcnt; they can be considered as groups subtidal coral reefs is quite constant whose interspecific relationships are likely throughout the Indo-West Pacific tropics. to bc of particular intcrcst. The size of the Most species are widely distributed, and groups indicates the degree of trans-Indodistribution restricted endemism-species West Pacific homogeneity of species comto one archipelago-is low. Nine benches position. Since all species of the sm,aller in five geographic regions have been ccn- bench group belong to the karger reef suscd, mainly by counting all individuals group, some interhabitat homogeneity also found in transects of quadrats across the occurs. Thcsc groupings are based on bench; 17 species were found, of which prescncc or absence of species only; they 5-9 occur on any one bench (Kohn 1967). do not consider relative abundance. When The nine most frcqucntly occurring spc- relative abundance as well as spccics comtics, with the number of occurrences by position is considered in a measure of simibenches and regions respectively (maxima larity ( R. of Horn 1966)) the polpulations = 9,s) indicated in parenthcscs are: C. of bench stations and of reef stations are sponsalis (9,5), C. ehraeus (8,5), C. chulseen to be more similar to each other (9 daeus, ( 8,4), C. lividus ( 6,s) , C. miliaris bench censuses : mean R. = 0.54; 19 reef ( 4,4), C. catus ( 5,3), C. coronatius ( 4,3), censnses : mean R. = 0.41) than bench C. r&us (5,2), C. ftuauidus ($2). The first populations are to reef populations ( 171 three species listed form a recurrent group, comparisons : mean R. = 0.32). All of the the largest group within which all pairs of means differ significantly ( t tests : p < species show affinity according to the cri0.005 ) . terion of Fager and McGowan (1963). On Until this point I have used the simplest 19 subtidal reefs censuscd, 58 spccics oc- index-number of species-as the measure currcd; 9-24 occur on any one reef (Kohn of spccics diversity; in most cases it was 1967), although substrate complexity and the only available datum. However, if all low population density gcncrally made individuals in a population or sample have quantitative sampling unfeasible. The 12 been identified and counted, it is desirable most frequently occurring species, with to USC “information content,” or the unthe number of occurrences by reefs and certainty regarding the species identity of regions rcspcctivcly (maxim,a 19, 9) indiany randomly selected individual (Pielou catcd in parenthcscs are: C. lividus (l&9), 1966a). The value of this index increases C. ehraeus (17,9), C. rat&s (17,9), C. &sboth with increasing numbers of species tans (12,9), C. chaldaeus (12,8), C. sponand increasing equitability or cvcnncss of salis ( ll,S), C. miles ( 12,7), C. leopardus their proportions. (9,6), C. milinris (9,6), C. imperidis (8,6), In Table 3, both measures are used to CONUS POPULATIONS: DENSITY,

TAULE 3. subtidul

DIVERSITY,

AND

SIZE

Species tliva~&zj of Corms assembluges of intwtidal marine benches (habitat type II) and coral rcwfs (habjtat type III) in the Indo-West Pacific tropics. (Data from Kohn 1967) No. of assemblages studied

Intertidal marine benches ( type II ) Subtidal coral reefs (type III )

Mean sample size

No.

of co-occurring Mean

9

221

7.5

191

110

13.7

species Range

Species Mean

diversity

(H”) Range

5-9

1.2

0.4-l .7

9-24

2.1

1.6-2.7

338

ALAN

J.

KOHN

compare species diversity of Conus assemblages in the two major habitat types throughout the Indo-West Pacific tropics and to provide a partial basis for the predicted directions of species diversity given in Table 2. Species diversity is measured bY

‘x i I.O2 9 9 2 .95-

.90!

0

I

I 2

1 1 I I 1 I 1 1 1 ’ 1 ’ 1 ’ IO 4 6 8 12 14 16 Number of collections

FIG. 3. Cumulative values of Cmu.s species diversity II” plotted against number of collections, A. Data for two subtidal fringing reefs in Hawaii. Upper curve, Maili: H” = 1.90; mean H” after last 4 samples, 1.90; 95% confidence limits for population diversity are 1.86 < II’,,, < 2.03. The 10 collections were made 1954-1968 and include 299 individuals of nine species. Lower curve, Diamond Head: H” = 1.87; mean H” after last 3 samples, 1.85; 95% confidence limits are 1.82 < II’,,, < 1.87. The 16 collections were made 1954-1956 and include 187 individuals of 10 species (Kahn 19,59). B. Data for an intertidal bench, Kahuku, Oahu: H” = 1.32; mean H” after last 6 samples, 1.34; 95% confidence limits are 1.31 < H’,,,a < 1.36. The 16 collections were made 1954-1968 and include 525 individuals of eight species. Leveling off of the curves to the right as more collections are added indicates that little further change in diversity would be expected if sample size were further enlarged and permits computation of the variance and confidence limits of II’,,,, in asscmblages that cannot bc sampled randomly (Pielou 1966b ) .

where s = the number of species, iVi = the number of individuals of the it11 species, and N = the total number of individuals in the sample. Since the number of species in the population is unknown, H” is the “maximum likelihood estimator of the unknown populatioa diversity H”’ ( Piclou 1966a, p. 464). However, it can be shown by applying the method of Pielou (1966b) to repeatedly sampled populations that H” is likely to be a close estimator of H’ for Conus. In cumulative graphs of H” vs. number of samples (Fig. 3), the curves tend to level off after 7-11 collecindividuals), inditions ( about 150450 cating that in samples added thereafter any reduction of diversity due to addition of common species is balanced by additional rare species that increase diversity. Thus further enlargement of samples of this size is unlikely to alter diversity values. Diversity and density can both bc estimated more reliably in bench ( type II) than in reef ( type III) habitats, because benches have homomgencous substrates and they arc lacking topographic features with a vertical component. Representative valucs of density (Table 4)) drawn from the most reliable estimates in published and unpubhshcd work, indicate that densities in type II habitats are characteristically several times those in type III habitats. Why this is so remains obscure. It is possibly due to the more homogeneous or less patchy nature of type II substrate or prey populations or both to reduced predation in a harsher environment, or to the relative advantage of small body size, but

DIVERSITY

TABLE

4.

OF

TROPICAL

MABINE

Population density of Conus spp, in intertidal bench (type II) and subtidal habitats (selected for geographic dispersion and large areas censused) Total arca censused (m2)

Hawaii: Kahuku, Oahu Hawaii: Nanakuli, Oahu IIawaii: Milolii, Kauai Marshall Is. : Parry Is., Eniwetok Marshall Is.: Uliga Is., Majuro Maldive Is. : Funidu Is., North Ma16 Seychelles Is. : Police Pt., Mah6

567 307 74 325 75 37 19

Type III Kekcpa Is., Oahu Hawaii: Hawaii: Kapaa, Kauai Heron Is., Australia Maldive Is. : Male Is., North Male Maldivc Is. : Gan Is., Addu Chagos Is. : Ilc du Coin, Peros Banhos Similan Is., Thailand: Goh Huyong Butang Is., Thailand: Pulos Ta Ngah Mcntawei Is.. Indonesia: Pulo Bai

56 669 5,000 167” 780” 613” 892” 697” 1,338”

* Estimated

339

INVERTEBMTES

from

duration

of

No. of co-occurring species

Density ( No./m2)

Reference

0.24 0.44 0.59 0.77 8.61 1.00 1.18 5 4 2 9 13 8 15 12 18

0.23 0.02 0.03 0.12 0.11 0.10 0.04 0.03 0.04

reef (type III)

Kohn

( 1959 )

Kahn, unpublished Kohn, unpublished Kohn ( 1968 ) Kahn, unpublished Kahn, unpublished Kohn ( 1959 > Frank ( 1969 ) Kohn

I

( 1968 >

Kohn and Nybakken, in prep.

census.

other hypotheses could bc advanced and none has been tested ( Kohn 1968). The conical shell and long narrow foot of Conus do not adapt the animal well to withstand heavy waves or strong currents. These, togcthcr with the stronger effect of wave action on the substrate in intertidal than subtidal habitats, and lack of shelter on a topographically simple and unifo’rm substrate, probably select for small body size in populations of bench habitats (Kohn 1968). 0 ccurrcnce on subtidal reefs of larger individuals of the same species, and of large individuals of species absent from benches, both contribute to the displacement of cumulative size-frcqucncy distributions (Fig. 4) in all areas for which comparative data are at hand. In all casts, the differences are significant at the 0.001 level ( Kolmogorov-Smirnov onctailed two-sample test; Siegel 1956). How generalized ( or specialized ) arc the co-occurring species in their USC of resources, particularly in habitats of types II and III that vary in diversity of spccics assemblages ? The measure of gencralization or “niche breadth” ( B ) used is

where Ni is the number of individuals of species i in the sample and Niw is the number of these using resource unit 72 (Levins 1968). B ranges from 1 to h, the number of resource units. It is biased in that it assumes all resources to be equally available; this could not bc determined but is unlikely. The reciprocal is a convenient index of specialization for the resource under consideration. Subtidal coral reefs are patchy environments; Kohn (1968) dcscribcd 9 substrate types cxploitcd by Conus as microhabitats. A similar analysis gives 6 types cxploitcd on benches. Table 5A indicates that Conus species representing a broad range of breadth of microhabitat type utilization occur in reef habitats. The most specializcd spccics (C. pulicarius, C. arenatus) occupy only or mainly one substrate type (patches of sand); the most gencralizcd spccics have values of B more than half the maximum possible value, i.e., if all

340

ALAN

Shell

J.

length

KOIIN

(mm)

4. Cumulative shell length-frequency distributions of Conus species on intertidal benches subtidal coral reefs in several parts of the Indo-West Pacific tropics. A. Seychelles; B. Maldivc Chagos Islands; C. Hawaii. In all cases, P < 0.001 (Kolmogorov-Smirnov test: Siegel 1956). FIG.

and and

DIVERSITY

OF

TROPICAL

MnRINE

341

INVERTEBRATES

Pacific Coaus species in two niche dimensions, substrate type 5. Niche breadth of Indo-West and prey species composition of diet, in two habitat types, subticlal coral reefs and intertidal benches. Data from more than one locale were combined to give mean values of B and B/B,,,, except where reef and bench samples of the same species from the same locale are compared. Locales: H, Hawaii; I, Indonesia and west Thailand (other than S); M, Maldives; S, Sanding Is., Indonesia. Ranges of B and B/B,,, values are given beneath means

TABLE

Benches

Reefs

Corms

Sample

species

Locale

size

sponsalis lividus

II II, M, I

61 231

f lavidus rattus

II

130 72

miliaris

M, S

ebraeus

I-1, M, S

153

chaldaeus imperialis coronatus

M H I, s

13 17 223

frigidus

M, S

95

musicus pennaceus

M II, I

71 152

aristophanes catus abbreviatus distans arenatus

M S II H M, 1

14 20 70 13 36

pulicarius

II

12

B

A.

H, M, 1

Microhabitat: * 5.02 + 4.77 3.82-5.58 4.69 * 4.62 3.51-5.32 4.04 3.164.92 * 3.90 3.03469 * 3.76 2.75 2.60 1.24-3.95 2.44 1.58-3.29 2.39 2.05 1.28-2.81 2.00 2.00 1.98 1.94 * 1.26 1.11-1.41 1.00

69

Range of B,,,, M H S I-1, M, S

pennaceus

H, I

f lavidus abbreviatus vexillum rattus rattus f rigidus

1-I 11

II H M M, S

substrate 0.55 0.48 0.38-0.62 0.52 0.45 0.39-0.56 0.45 0.35-0.55 0.43 0.34-0.52 0.42 0.31 0.22 0.14-0.30 0.27 0.18-0.37 0.27 0.21 0.10-0.31 0.22 0.22 0.22 0.22 0.12 0.09-0.16 0.11

40 24 64 136 81 102 42 19 35 12 67

B

B Al,x

type *

0.36

211

2.16

I-1

45

2.79

II

96

3.65

*

0.61

II

29

3.55

*

0.59

II

96

2.55

II

9-13 B.

musicus sponsahs coronatus lividus

Locdo

S mnple size

Food: prey species composition 0.35 6.62 II * 0.31 6.41 0.28 5.38 0.25 * 4.89 2.24-6.80 0.11-0.36 0.30 4.50 4.05-4.95 0.29-0.31 0.21 4.39 1-I 0.15 3.25 0.10 2.00 II 0.13 * 2.79 0.05 1.00 0.09 1.70 1.22-2.19 0.06-0.12

0.47

0.43

6

142

5.78

81

4.72

0.36

26

2.16

0.17

*

0.44

-

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TABI,E

J.

5.

KOIIN

Continued -----___

-_--

Reefs

Corms species

Sample size

Locale

miliaris ebraeus ebraeus ebraeus chaldaeus chaldaeus distans imperialis

M H M S M S H H

Range

of B,,,,

Benches

B

30 38 39 122 31 14 13 11

1.49 1.63 1.30 1.41 1.71 1.15 1.17 1.00

B~%,,x 0.08 0.08 0.07 0.07 0.09 0.06 0.06 0.05

* * * * * *

13-21

c(’ h recurrent

group

of

most

A

Bmn,x

M I-1 M

27 122 31

1.00 1.12 1.07

* +

0.17 0.09 0.18

H

53

1.34

*

0.10

B mnx=h N lh

of

Sample size

6-13

B=

* Member

Locale

frequently

Nl occurring

substrate types were utilized equally. On benches, the range of B is narrower. The values are generally lower than those of the dominant ( recurrent) reef species; when all spccics arc considered, the bctwcen-habitat difference is not significant ( Mann-Whitney U-test: P = 0.4). Holwever, the significantly higher B/B,,?( values (P < 0.02) indicate that bench species as a group are more generalized with respect to their USC of available substrate types. In one geographic region, the species most abundant in and characteristic of bench habitats were more specialized predators than those characteristic of reef habitats (Kohn 1968). As in the case of substrate type utilization, the dcgrec of food specialization ranges broadly when data for more species and regions are considered (Table 5B). Since the type II environment is more homogeneous, reducing environmental resistance to movement, and appropriate food items are more acccssiblc (and their population densities are probably greater: Kohn and Lloyd, in prep.), food specialization is expcctcd as the more efficient feeding strategy (MacArthur and Pianka 1966; Emlen 1966). The fact that five of

’ > species.

the six species represented in both parts of Table 5B are more specialized predators on benches than reefs in the same locale provides additional evidence in support of this hypothesis from other regions and species. However, the values for dominant ( recurrent ) species are spread throughout the column, and the difference in food niche breadth between habitats is likcwisc not significant (P = 0.2). As in the case of microhabitat type, bench spcties as a whole arc more generalized with respect to their USC of the total array of prey species exploited in the habitat (P = 0.04). In general, the species considered arc more specialized as predators than with respect to microhabitat. With few exccptions the highest values of B for food Care less than I/ the maximum value based on consumption in equal proportions of all prey species represented more than once in diets, Such values of B for food are also biased upward compared to substrate values, since all substrate resource units present are used to some extent by some species. This is not true of potential food resources, since all but one species listed in Table 5 prey only or mainly on polychaetc annclids, and somlc polychaetes oc-

DIVERSITY

OF

TROPICAL

cur abundantly and are not catcn at all by Conus ( Kohn and Lloyd, in prep. ) . ECOLOGICAL CO-OCCURRING

SIMILARITY

OF

SPECIXS

How similar ecologically arc co-occurring, taxonomically similar species in assemblages of varying diversity? And how many species that similar could theoretically persist in a resource-limited assemblage? Considering the latter question first, the current status of theory of the ecological niche may be traced to the introduction of the concept of dimcnsionality of the niche by Hutchinson ( 1958, 1965) and to his early concern with limitation of diversity and how different potentially competing species must bc to coexist ( Hutchinson 1959). Subsequently, MacArthur and Lcvins (1967) derived a theoretical criterion for the maximal similarity that three species may have and continue to coexist, based on the Voltcrra equations. Levins ( 1968) proposed substituting values of niche overlap for cy, the competition coefficient in the Voltcrra equations, and proposed the “community matrix” as a way to calculate the thcorctical maximum number of similar species that could co-occur, given the limiting resource set and all values of a. Because the theory assumes a number of conditions unlikely to be realized or difficult to determine in nature, tests of predictions deduced from it have little real value at the present time. The assumptions include those of the Voltcrra cquations, that only carrying capacity, intrinsic rate of natural increase, number initially present, and effect of the numbers of the other species present affect the rate of population size change of a species, and that its responses to these factors arc instantaneous. In addition, use of the formula of Levins ( 1968) for calculating a assumes that 1) the niche dimensions considered are those that serve to separate species (Levins 1968); 2) overlap in resource utilization is equivalent to competition; 3) usable resources are equally available and rapidly - -

MARINE

INVERTEBRATES

343

renewed; 4) spccics abundances arc identical or differcnccs are unimportant; and 5) additional spccics considcrcd for entrance into the community matrix have the same mean values of cx and the same covariance of aii and ajt as those aheady prcscnt. In the only applications of data from natural populations to this theory to date, where the utilization of resources by three or more species can bc measured an d arrayed, the predicted limiting similarity is not cxcecded (Orians and IIorn 1969; Pianka. 1969)) or is slightly exceeded (4 spccics present, 3 predicted: Culver 1970)) when 2-3 niche dimensions (microhabitat, foosd, time of activity) arc included in the analyses. In the following analysis of real situations the dimensions used are assumed to meet the criteria listed above; the descriptive-correlative approach used dots not permit an indcpcndcnt determination. Howcvcr, I have selected as dimensions food resources that could be used up: an d microhabitat space. Morcovcr, there is no independent cvidcncc that any of the assumptions of the model are met. The “test” of the theory thus takes on the character of a “this is what would happen iY game or simulation. However, it is just possible that tropical marine invertebrate genera having several to many cooccurring spccics, like tropical forest Drosophila perhaps ( Lcvins 1968)) approach the assumed conditions more closely than other taxocencs that could be considered. The simplest comparison of overlap of Conus spccics with rcspcct to resources would bc utilization of the two majo’r habitat types-reefs vs. benches. However, this comparison would be meaningless, because to test the theory the numbcr of distinct resources must equal or cxcecd the number of species in the assemblage; Lcvins ( 1968) gives proof of this theorem, TO compare the dcgrec of subdivision of microhabitat and food resources with the theoretical limiting similarity, I computed overlap values for all polssible species pairs in assemblages from all geographic regions

344 TABLE

from

ALAN

J.

KOHN

6. Observed numbers of co-occurring species of Corms and their overlap statistics derived a matrices compared with maximum ,numbers predicted for species packing, based on the community matrix of Levins (1968)

-Overlap from Region

Ihbitnt

A. Hawaii IIawaii Maldive Is. Indonesia and Thailand Sanding Is., Indonesia

Microhabitat: Reefs Benches Reefs Reds Rt?d B.

IIawaii Hawaii Maldives Sanding Hawaii IIawaii Hawaii Maldive Sanding

Mean

Occu.pation

Is. Is., Indonesia

Food: Reefs Benches Reefs Reefs

Is. Is., Indonesia

C. Microhabitat Reefs vs. benches Reefs Benches Reefs Reef

Covariance

of substrate types 0.63 0.014 0.79 0.007 0.50 0.050 0.32 0.067 0.34 0.086

Species composition 0.18 0.41 0.12 0.15

studied from data such as those shown in Fig. 1 and Tables 3 and 4 of my earlier report (Kohn 1968). Thcsc and all succeeding overlap (a) measurements rcfcrred to (Table 6) wcrc made according to the method of Levins ( 196$). When overlap with respect to microhabitat (occupation of different substrate types ) is considered ( Table 6A), the numbers of species actually present in most cases considerably exceed the maximum numbers for species packing in the community matrix (Levins 1968)) if the latter are calculated from observed overlap values and their means and covariances. The predicted values would bc increased if across differences in local distribution benches (Ko,hn 1959; Kohn and Orians 1962; Kohn and Nybakkcn, in prep.) and diffcrenccs in depth on reefs (Kohn 1968) had been considered in the analysis. Calculations based on overlap with respect to food (species composition of diet in nature) ( Table 6B ) give predicted maximum numbers of species that match or are slightly lower than the numbers ob-

statistics N matrix

x food 0.14 0.05 0.20 0.07 0.002

No. of species observed (in annlysis)

10 6 9 10 6

of diet 0.048 0.028 0.047 0.071 0.031 0.006 0.040 0.014, E 8 21 >34

served. Combining the two niche dimensions (for each species pair the overall a is the product of the individual ones: Lcvins 1968) Table 6C gives predicted maximum numbers that in all cases equal or exceed obscrvcd numbers. If all assumptions of the theory were met, this would indicate that subdivision of microhabitat alone is insufficient to separate species, subdivision of the food resource alone is, or is nearly, sufficient, but that the two resources taken together provide adcquatc niche dimensionality so that the co-occurring species can subdivide them adequately to accommodate the numbers of species present and avoid comThe assumptions arc petitive exclusion. not met. Thus the data show only that cooccurring Conus species spccializc more to different foods than to substrate types, and the former specialization is likely to be somewhat more important in avoiding potential interspecific competition among adults. In addition to the difficulties mentioned above as inherent in applying the commu-

DIVERSITY

OF

TROPICAL

nity matrix model to real situations, two problems specific to these analyses should be indicated here. First, I assume that I have identified the units of resources (food according to prey spccics; microhabitat according to substrate patch types : see Kohn 1968) appropriately as far as the animals’ responses to them are concerned. Secondly, the analysis in Table 6C suggests that some of the species present could be more generalized predators (or microhabitat occupiers ) , or more species could co-occur. In fact, more spccics do co-occur (Kohn 1959, 1967, 1968) but they are rarer and the samples studied were too small to include in the analyses. The generally lower overlap values for food than for microhabitat (Table 6) suggest a more general hypothesis: that cooccurring predatory invertebrates might tend to adopt a strategy of apportioning resources by specializing more on different prey spccics rather than subdividing habitats distinctly. On the other hand, co-occurring congcncrs that feed less selectively, especially those ca tine; mainly particulate organic detritus, might spccializc more to different microhabitat patch types, while apparently overlapping more with respect to the nature of their food. One would expect suspension- and dcposit-feeding animals to be less efficient than predators at specializing to food type, because in the former the nature of the feeding mechanisms and the size of the food particles require the animal to ingest or at least contact the particles before it can evaluate their desirability. Since additional energy must bc expended in handling inedible material, one might expect sclcctive particulate feeding to bc a succcssful strategy only if food abundance were extremely prcdictablc. It is more efficient for a predator, o,r an herbivore feeding on large plants (relative to its body size), to respond only to appropriate food items. How specialized to microhabitat and food type are other predatory tropical marinc invertebrates? The gastrolpod M&a Zitterata, which co-occurs with Conus spc-

MARINE

INVERTEBRATES

345

ties on the intertidal benches discussed above, probably preys cxchrsively on a worms, not few spccics of sipunculan catcn at all by Conus ( Kahn 1970) s In IIastuZa, a genus of toxoglossan gastropods in a family closely related to the Co,nidac, two species co-occurring in the same zone on surf-swept beaches in Hawaii, where Corms is absent, are specialized predators Howon diffcrcnt spionid polychaetes. cvcr, a third species occurring higher on the beach than these, and a fourth occurring lower, are equally specialized prcdators on different spionids (Miller 1970). In the related genus Terebra, two COoccurring spccics in patches of sand on reefs specialize on different prey worms ( Miller 1970); one of the prey species is also eaten by the co-occurring but uncommon Conus pdicarius, which also eats cchiuroids (Kohn 1959). On subtidal sandflats, however, four species of Terebra, also specialized predators on different polychaotcs and cnteropneusts, occupy generally distinct microhabitat patches ( Miller 1970). Like the Conus species discussed above, these predators are pursuers of large food items rather than searchers for small items that cannot afford to bypass many. Food specialization is therefore an especially advantageous strategy for them ( MacArthur and Levins 1964)) and scvera1 similar species, often of different sizes, tend to co-occur (Fig, 3 and Kohn 1959, 1968; Miller 1970), As to detritus feeders, Mr. M. A. Chartack is currently investigating seven spetics of the brittle-star genus Ophiocom co-occurring on Marshall Island reefs. The four commonest species appear to bc nonselective dc tritus feeders, although some differcnccs in feeding method and particle size prcfcrencc were noted, However, they feed in diffcrcnt microhabitats and in laboratory experiments they show active prefcrcncc for the type of substrate occupied in nature. The limited data available thus offer only modest suppo,rt to the hypothesis that co-occurring predatory congeners are more likely to spccializc to different prey spc-

346

ALAN

tics than to microhabitats, while animals feeding on small particles are more likely to spccializc to type o,f substrate pa,tch. DISCUSSION

AND

CONCLUSIONS

My thesis here is that the comparative ecological approach to groups of co-occurring, similar spccics can generate data pertinent to hypotheses relating species diversity, resource utilization, and habitat complexity and can thus help to elucidate patterns of adaptive radiation and the organization of at least subunits or componen ts of communities. Assemblages of inshore marine invcrtebrates of tropical islands in the Indo-West Pacific region share a number of common features. Faunal diversity is high and has a typical taxonomic pattern of a high average number of species per genus, because several to many genera have many (5-30 or more) sympatric species. The species composition of taxocen.cs and their population density are similar in similar habitats throughout the region. This similarity of faunal composition (Ekman 1953) is due in large part to the common, effective dispersal mechanism of long-lived, pelagic, planktotrophic larvae, which renders distance less important than is the case with other dispersal mcchca.nisms ( IMacArthur and Wilson 1967). Strand plants of tropical islands provide evidence of the same phenomenon (Whitehead and Jones 1969). The absence of species with such dispersal mechanisms suggests an unfavorable habitat rather than lack of immigration, Marine invertebrate taxa such as gammarid amphipods that lack larval stages and whose assumed primary dispersal mechanism is rafting on detached vegetation and debris have fewer co-occurring species per genus and a higher degree of endemism on tropical Indo-West Pacific islands ( Barnard 1970). In the gastropod genus Conus, assemblagcs varying widely in species diversity occur along the shores of tropical IndoWest Pacific oceanic islands. Marc species co-occur, but at lower populatio,n densities, in tonoeranhicallv comnlex but climati-

J.

KOIIN

tally equable subtidal coral reef habitats than in topographically simple, climatically more scverc intertidal bench habitats, where physical factors and restrictions of foot and shell form also select for small body size. As a group, Conus expands ecologically to exploit the wider range of microhabitats and prey species available on reefs compared to benches. All species occurring on benches also occur on reefs, probably because only reefs provide suitable oviposition sites (Kohn 1959). Adults on benches arc thus probably derived from larvae produced on reefs. Species occurring in both habitat types are more generalized with regard to both prey ‘and substrate type utilization on reefs, although they must tolerate a greater amplitude of fluctuation of climatic variables (wave action, temperature, desiccation) on benches. Reef species that do not occur on benches range broadly fro,m relatively gcneralizcd to very specialized in microhabitat and food utilization (Tables 2 and 6). The assumptions of the theory of limiting similarity of co-occurring species arc not met in the natural populations that I have studied. However, there have been few applications of data to this recent theoretical advance (Orians and Horn 1969; Pianka 1969; Culver 1970) and none dealing with assemblages of marine invertebrates. Moreover, genera of predatory benthic invertebrates with many co-occurring species, such as Conus, m.ay approach the assumed conditions relatively closely, compared with other assemblages of organisms. Co-occurring species of Corms overlap more with respect to microhabitat (utilization of substrate type) than in utilization of prey species (Table 6)) suggesting that differences in prey taxa are not due only to foraging in different microhabitats, Comparison of observed numbers of spcties with numbers expected by the theory of limiting similarity to persist in a community of competing species (the community matrix of Levins 1968) indicates that, as analyzed, subdivision of the two resources, food and substrate type, would

TXCVERSITY

OF

TROT.‘ICAL

accommodate the numbers of spccics prcscnt if the assumptions of the theory wcrc met. This result is csscntially similar to those of Orians and Horn - (1969) for blackbirds, Pianka ( 1969) for dcscrt liza1.ds,1 and Culver (1970) for cave crustaccans, although the limited applicability of all of these data to the theory, as discussed in the previous section, must bc strcsscd. Although high spccics diversity makes studying tropical marinc invertcbratc taxoccncs difficult because large samples arc rcquircd whcrc the information content per individual is high, the availability of a set of assemblages varying in diversity, and of a set of species ranging from spccialized to gencralizcd in their ecological characteristics, enhances the value of the comparative approach, particularly when the stronger inferential method of manipulation experiments is technically difficult, The dcscriptivc comparative ecolo,gical studies discussed hcrc indicate that habitat hctcrogencity and ccolo8gical spccialization are correlated with the high spccics diversity of assemblages of some genera of marinc invcrtcbratcs inhabiting tropical island shorts and coral reefs, and may thcrcforc bc important determinants of diversity. This approach also helps to distinguish attributes of cvolvcd rcsponscs to environmental variables that arc gcncral and may be considered principles from those that are special adaptations characteristic only of particular taxa. It would now seem fcasiblc to obtain stronecr infcrcnccs by manipulating populatioL in naturc, and to evaluate the role of certain other features of tho environment and of the animals that arc likely to influcncc spcties diversity and population size, such as the distribution, availability and rate of utilization of suitable resources, predation, and perhaps recruitment success. Study of these aspects of the ecology of tropical inshore marine invcrtcbratcs would clearly help to elucidate the structure and functioning of the complex ecosystems to which they belong.

MARINE

1NVERTERRATES

347

REFERENCES

and feeding in hKUS, c:. J. 1969. Energctics shallow marine waters. Int. Rev. Cen. Exp. Zool. 4: 275-369. Gammnriclcn BAIWARII, .1. L. 1970. Sublittoral of the IIawaiian Islands. ( hmphipodn) Smithson. Contrib. Zool. 34. 286 p. Cutvm, D. C. 1970. Analysis of simple cave niche separation and species communities: packing. Ecology 51: 949-958. Zoogcography of the sea. 1953. EKMAN, S. Sidgwick and Jackson. 417 p. 1966. The role of time and enEMLEN, J. M. Amer. Natur. 100: ergy in food preference, 611-617. 1963. l?~am, l3. W., AND J. A. MCGOWAN. Zooplankton species groups in the North Science 140 : 45S-460. Pacific. 1969. Growth rates ancl longevFRANK, I'. W. ity of some gastropocl mollusks on the coral reef at IIeron Island. Occologin 2: 232-250. SHALT., C. A., JR. 1964. Middle Miocene Colzlls ( Class Gastropoda) from Piedmont, northern Italy. Boll, Sot. Paleontol. Ital. 3: 111-171. of “overlap” JIOltN, 11. s. 1966. Measurement Anler. in comparative ecological studies. Natur. 100: 419-424. remarks. IIUTCIIINSON, C. E. 1958. Concluding Cold Spring IIarbor Symp. @ant. Bid. 22: 415-427. -. IIomagc to Santa Rosdin or 1959. why are there so many kinds of animals? Amer. Natur. 93: 145-159. -. 1965. The ecological theater nncl the evolutionary play. Yale Univ. Press. 139 p. -. 1967. A treatise on limnology, v. 2. Wiley. 2115 p. 1967. KAY, E:. A. The composition and rclationships of marine molluscan fauna of the Hawaiian Islands. Venus 25: 96-104. KOEIN, A. J, 1959. The ecology of Conzrs in IIawaii. Ecol. Monogr. 29: 47-90. -. 1966. Food specialization in Conus in IIawaii and California. Ecology 47: 10411043. 1967. Environmental complexity and ----* species clivcrsity in the gastropod gauns Corms on Indo-West Pacific reef platforms. Amer. Natur. 101: 251-259. 1968. Microhabitats, abundance and ---’ food of CO~XZCSon atoll reefs in the Maldivc ad Chagos Islands. Ecology 49: 1046-

1062.

-.

1970. Foocl habits of the gastropod Mitra Zitteratcc Lamnrck: Relation to trophic structure of the intertidal marine bench community in Hawaii. Pac. Sci. 24: 483-

486.

-,

AND c. II. hIAN% 1962. Ecological data in the classification of closely rclntecl species. Syst. Zool. 11: 119-127.

348

ALAN

LEVINS, R. 1968. Evolution in changing environments. Princeton Univ. Press. 120 p. MACARTHUR, R. II, 1969. Species packing, and what interspecies competition minimizes. Proc. Nat. Acad. Sci. U.S. 64: 1369-1371. AND R. LEVINS. 1964. Gompetition, habitat selection, and character displacement in a patchy environment. Proc. Nat. Acad. Sci. U.S. 51: 1207-1210. -,AND--. 1967. The limiting similarity, convergence, and divergence of coexisting species. Amer. Natur. 101: 377-385. -, AND E. R. PIANKA. 1966. On optimal use of a patchy environment. Amer. Natur.

100: 603-609. -,

AND E. 0. WILSON. 1967. The theory Princeton Univ. of island biogeography. Press. 203 p. MILLER, B. A. 1970. Studies on the biology of Indo-Pacific Terebridac. Ph.D. thesis, Univ. New IIampshire. 207 p. ORIANS, G. H., AND H. S. HORN. 1969. Overlap in foods of four species of blackbirds in the potholes of central Washington. Ecology 50: 930-938. of desert lizPIANKA, E. R. 1969. Sympatry Ecolards (Ctenotus) in Western Australia. ogy 50: 1012-1030.

J.

KOHN

PIELOU, E. C. 196&. Shannon’s formula as a measure of specific diversity: Its use and misuse. Amer. Natur. 100: 463-466. -. 1966b. The measurement of diversity in different types of biological collections. J. Theor. Biol. 13: 131-144. SANDERS, H. L. 1968. Marine benthic divessity: A comparative study. Amer. Natur. 102 : 243-2$2. SIEGEL, S. 1956. Nonparametric statistics for the behavioral sciences. McGraw-Hill. 312 p. S~EHLI, F. G., R. G. DOUGLAS, AND N. D. NEWELL. 1969. Generation and maintenance of gradients in taxonomic diversity. Science 164 : 947-949. THORSON, G. 1952. Zur jetzigen Lage der marinen Bodenticr-Ukologie. Verh. Deut. Zool. Ges. 1951: 276-327. -. 1957. Bottom communities (sublittoral or shallow shelf). Geol. Sot. Amer. Mem. 67, p, 461-543. WELLS, J. W. 1954. Recent corals of the Marshall Islands. U.S. Geol. Surv. Prof. Pap. 260-1, p. 385-486. WHITEHEAD, D. R., AND C. E. JONES. 1969. Small islands and the equilibrium theory of Evolution 23: 171insular biogeography. 179.