Patterns of habitat and food utilization in two coral-reef sandperches (Mugiloididae): competitive or noncompetitive coexistence?

J. Exp. Mar. Biol. Ecol., 1990, Vol. 140, pp. 209-223

209

Elsevier

JEMBE 01454

Patterns of habitat and food utilization in two coral-reef sandperches (Mugiloididae): competitive or noncompetitive coexistence? Mitsuhiko Department of Fisheries, Faculty of Agridure.

Sane University of Tokyo, Tokyo, Japan

(Received 8 December 1989; revision received 5 March 1990; accepted 4 April 1990) Abstract: Use offood and habitat of the two sympatric, territorial mugiloidid fishes Parapercispolyophthalma (Cuvier) and P. clathrata Ogilby, which have similar body size and morphology, were examined in the fringing coral reef area at Iriomote Island, one of the Ryukyu Islands of Japan. Both species preyed mainly on decapod crustaceans, and the dietary overlap value was intermediate (0.528). Differences in resource utilization between the two species were conspicuous in habitat rather than in food. ~60% of the P. polyophthalma population was found on sandy flats of the reef flat zone, while z 90% of the P. clathrata population occurred at channel areas. In addition to this macrohabitat segregation, both species showed a substantial microhabitat separation at channels where they coexisted with nearly the same densities: P. polyophthalma was numerically dominant on a sandy rubble substratum, whereas P. clathrata was abundant on a rubble substratum. A reciprocal removal experiment demonstrated that this microhabitat separation was an outcome of current competitive interactions between them. P.polyophthalma is an aggressively dominant species and so can predominantly occupy its optimal microhabitat, i.e., sandy rubble substratum, at channels, while the subordinate P. clathrata is constrained to shift its microhabitat to a rubble substratum unsuitable for the dominant. Although a density-manipulation experiment for the macrohabitat segregation was not carried out in this study, circumstantial evidence suggested that the segregation is probably attributable to differences in habitat adaptation between the species which need not be the consequence of competition. These results indicate that the structure of the two-species guild may be determined by both competitive and noncompetitive mechanisms.

Key words: Density-manipulation experiment; Diet; Habitat adaptation; Interspecific competition; Macroand microhabitat separation; Parapercis

INTRODUCTION

As summarized by a number of workers (e.g., Sale, 1980,1984,1989; Warner, 1984; Doherty & Williams, 1988; Mapstone & Fowler, 1988), there is at present a noticeable disagreement over understanding of the mechanisms permitting the coexistence of large numbers of fish species on coral reefs. The traditional view suggests that these assemblages exist at or near stable equilibrium, characterized by fine partitioning of limited resources such as food and habitat and increasing specialization through competitive Correspondence address: M. Sano, Department of Fisheries, Faculty of Agriculture, University ofTokyo, l-l-l Yayoi, Bunkyo-ku, Tokyo 113, Japan. 0022-0981/90/$03.50 0 1990 Elsevier Science Publishers B.V. (Biomedical Division)

interactions Gladfelter,

(Smith & Tyler, 1972, 1973, 1975; Smith, 1973. 1978; Gladfelter Kr 1978; Molles. 1978; Brock et al., 1979; Gladfelter et al., 1980; Anderson

et al.. 198 1: Ogden & Ebersole, Johnson, Clarke,

1983; Ebersole,

1981; Greenfield

1985; Bouchon-Navaro,

& Greenfield, 1986; Robertson

1988). Other views suggest that species composition

in fish assemblages

vary randomly

and are unstable.

1982; Gladfelter & Gaines,

&

1986;

and relative abundances

These explanations

include

two

different theories, i.e., the lottery hypothesis and the nonequilibrium hypothesis. The lottery hypothesis predicts that differential competitive abilities or niche diversification is not a necessary feature for coexistence, even though the availability of suitable living space may limit the total density of several competing species. Fish assemblages are structured by chance colonization of juveniles into vacant space which is unpredictably generated by agents including predators which remove residents from sites (Sale, 1974a, 1977, 1978, 1979. 1980). The nonequilibrium hypothesis states, on the other hand, that populations are maintained below their carrying capacities because of external disturbances such as an inadequate supply of larval recruits and predation. Hence, this hypothesis does not emphasize the importance of competition within or between species in assemblage organization (Talbot et al., 1978; Williams, 1980; Doherty, 1981, 1982, 1983; Victor, 1983, 1986; Wellington & Victor, 1985; Doherty & Williams, 1988). To test these hypotheses, recent studies have been focussed on detecting and assessing the magnitude of density-dependent effect by competitive interactions or densityindependent effect in determining population size (e.g., Doherty, 1982, 1983; Shulman et al., 1983; Victor, 1983, 1986; Sweatman, 1985; Eckert, 1987; Jones, 1987a,b; Shulman & Ogden, 1987). If the adult density of each species in an assemblage is not limited through density-dependent processes on recruitment and/or postrecruitment survival or growth, the traditional equilibrium model which stresses the importance of intra- and interspecific competitive interactions can be falsified and the nonequilibrium model validated. If density-dependent effects are limited to the rates of recruitment of guild members, the lottery hypothesis may be indicated, although Doherty & Williams (1988) have recently suggested that there is little evidence supporting this hypothesis on the basis of the extensive review of literature on the recruitment of tropical reef fishes. The equilibrium model can also be explored by a different approach investigating whether resource-partitioning patterns structured by competition occur along main resource axes in the assemblage or guild of taxonomically close species. The most popular and facile method of this approach is to measure the degree of resource overlap among coexisting species. If sufficiently small overlapping is detected, it is generally concluded that such resource use is an evolutionary response to competitive processes and is responsible for the coexistence of species within the assemblage. Competitionderived resource partitioning, however, cannot be really demonstrated by such passive measurement, because a direct correlation between the degree of competition and the amount of overlap does not necessarily exist (Sale, 1974b; Connell, 1980; Pimm & Rosenzweig, 198 1; Strong, 1983 ; Keddy, 1989). The surest method, to detect the occurrence of competition and the resulting resource partitioning, i.e.. niche shifts, is

211

RESOURCE SEPARATION IN CORAL REEF FISHES

a field removal experiment (Connell, 1980,1983; Underwood, 1986). Although this type of experiment is not often technically feasible, it may be relatively easy to make for territorial resident fishes living on topographically flat areas because of ease of capture and observations on population density and behavior. The primary purposes of this study are: (1) to examine the degree of overlap between two territorial mugiloidid species with respect to their main resource uses, i.e., habitat and food (Schoener, 1974; Ross, 1986); (2) to ascertain whether competitive interactions between the species are existing, by conducting a field experiment and behavior observations; and (3) to elucidate the principal determinants of their coexistence.

MATERIALS

AND METHODS

STUDY AREA AND SPECIES

This study was carried out in the fringing coral reef area of Amitori Bay (24”20’N, 123 “42’E) on the western side of Iriomote Island, one of the Ryukyu Islands of Japan, during September 1988 and June 1989. Maps of the study area appear in Sano et al. (1987) and Yokochi & Ogura (1987). Most hermatypic corals, especially Acropora and Pocillopora spp., in the bay are dead due to extensive outbreaks of the coral-feeding starfish Acanthasterplanci (Linnaeus) between 1981 and 1982. The dead corals of some reefs on the reef flat have been strikingly degraded by biological and physical erosion (see Sano et al., 1987), but some outer marginal reefs are initiating natural recovery by the recolonization of Acropora. Two species of shallow-water sandperches (Mugiloididae), Parapercispoiyophthalma (Cuvier) and P. clathrata Ogilby, both of similar body size and morphology, commonly inhabit coral reef areas at Amitori Bay. These two fishes have a social system based on male territoriality and a male-dominated harem. Each male defends a large area within which one to three females smaller than the male have individual home areas and forage (Table I). Sexual dichromatism is not conspicuous, but some clear differences

TABLE I

Social group composition of P. polyophthalma and P. clathrata at Iriomote Island, Ryukyu Islands. Species

Number of male territories observed

P. polyophthalma P. clathrata

23 23

Mean size of male territories (&lSE,rn2) 193 * 10* 98 f 7*

Range of male territory size (m2)

Mean number of females per harem (kl SE)

128-290

1.7 f 0.1 1.8 + 0.2

40-152

Range of female number per harem

l-3 l-3

*Male territory size of P. clathrata was significantly smaller than that of P. polyophthalma (two-tailed Mann-Whitney u test, U = 502, P < 0.001).

in

the body coloration

females. Males

among

the sexes allow to discriminate

ofP. po(vophthafma, for example,

between

have more numerous

males

and

small dark brown

spots on the cheek than females, and P. clathrata males have a black ocellus encircled with a white line above the operculum and dichromatism reefs (Thresher,

1984; Nakazono

hermaphrodites, although Shapiro. 1987). ANALYSIS

OF

which is absent in females. Such a social system

suggest that, like some other congeneric

SPATIAL

species living on shallow

et al., 1985). both species are probably

we lack a histological

study of their gonads

protogynous

(see Sadovy &

DISTRIBUTION

Large-scale distributions Preliminary observations showed that P. polyophthalma and P. clathrata were found in at least three reef habitats at Amitori Bay. Characteristics of these habitats are summarized in Table II. At each habitat, visual censuses were carried out by swimming slowly using a mask and snorkel, along a nonoverlapping zigzag pattern. All censuses were made at high tide between 1000 and 1600. Census data were standardized to the number of individuals counted per hour of census. To assess the degree of overlap in use of habitat between the species, I used the proportional similarity index (Schoener, 1968; Linton et al., 1981): 3 H=

Characteristics Habitat name

Reef zone

of habitats

Distance from the shore

i j Pxi--Pyi~, , ii ,

l-0.5

censused

Substratum type

for mugiloidid Water depth

abundance. Remarks

(m)

(m) Sandy flat

Reef flat

100-500

Fine sand

1-2

Rubble reef

Reef flat

100-500

Coarse rubble

1-2

Channel

-

500-600

Rubble and sandy rubble

3-7

Exposed sand plains adjacent to coral reefs; scattered small dead colonies of Acropora and Pocillopora and living colonies of Porites Unstructured dead coral reefs and patches consisting mainly of debris of staghorn Acropora interface with sandy flats (see Sano et al., 1987) Channels connecting sand plains on reef flat with open ocean, lo-30 m wide; scattered dead broken coral blocks of various sizes; strong tidal currents

RESOURCE

SEPARATION

IN CORAL

REEF

FISHES

213

where P, and Pyi are proportional occurrences of species x and y in the ith habitat for n habitats. This index ranges from 0 (no overlap) to 1 (complete overlap). Microhabitat distributions

The observations

of large-scale distributions

suggested that, although P. poly-

ophthalma was most numerous on sandy flats, both fishes coexisted at channels to a

considerable extent (see Results). To determine whether these two species partitioned shared habitats on a line scale, I examined the distributions of male territories of each species by mapping the territory boundaries obtained from their swimming paths (see Nakazono et al., 1985) and then described the nature of their substrata (i.e., rubble or sandy rubble). I also counted the number of females within the territories. EXPERIMENTAL

MANIPULATION

OF MICROHABITAT

USE

If P. polyophthalma and P. clathrata showed a microhabitat difference, it is necessary to ascertain whether such a difference was due to competitive interactions. Consequently, I conducted a density-manipulation experiment at three selected channels where both species commonly coexisted and territory boundaries of males were partially contiguous or slightly overlapped between the species. All P. polyophthalma were removed from one channel ( GZ0.17 ha) with the density of P. clathrata unaltered, all P. clathrata from another (0.20 ha) with P. polyophthalma unchanged, and both species at the third (0.18 ha) were left intact as a control. 2 wk after removal, the utilization of vacated space by the populations remaining at each experimental channel was measured in two ways: (1) expansion of territorial borders into vacated sites by neighbouring males, and (2) establishment of new territories on the sites by intrusions of males which previously lived elsewhere near the experimental channels. When these phenomena were found, a stronger suggestion could be made, namely that competitive interactions between the two species were occurring (Connell, 1980,1983). When vacated areas were reoccupied by immigrants of removed species during the experimental period, they were captured immediately. ANALYSIS

OF FEEDING

HABITS

After the census all individuals were collected from channel areas between 1000 and 1600, using a monofilament net. Immediately after collection, specimens were placed in 10% formalin and the stomach contents preserved by injecting concentrated formalin directly into the body cavity. The standard length was measured for each specimen in the laboratory. Food items from the stomach contents were sorted and identified under a low-power binocular microscope. Each sorted item was weighed in wet condition to the nearest 1 mg. The relative importance of each food item to the diet of each species was expressed by two methods: (1) percentage occurrence ofthe item and (2) percentage composition of each item by wet weight. The latter was calculated by dividing the sum total of the individual weight for the item by the total weight (Hyslop, 1980).

To estimate niche breadth in the utilization of food resources for each species, the Shannon diversity index was employed (Berg, 1979; Magurran, 1988):

where Pi is the proportion by weight of a particular prey category, for n prey categories. H’ varies from 0 to In n and the largest values indicate wider use of food resources. Dietary overlap between the two species was determined using the above proportional similarity index (CC,,)where Pxi and PYi are the proportions by weight of the ith prey category in the diets of species x and y, and n is the total number of food categories in the diet.

RESULTS

FEEDING

HABITS

Of the 23 P. polyophthalma and the 21 P. cluthratu collected, all had stomachs full of food, including a variety of small benthic invertebrates and fish (Table III). Decapod crustaceans ranked highest in importance in the diets of both species, accounting for 60.4% (P. polyophthalma) and 84.8 % (P. clathratu) of the total diets by weight. Among decapods, crabs were the most prevalent prey taxon of both species, but were relatively more important to P. clathrata. These prey constituted 72.1 y0 of the stomach content weight for P. clathrata, compared to 38.0% for P. polyophthalma. Inversely, shrimps were more abundant in P. polyophthalma (22.4 vs. 12.7%). Other than decapods, fish were an important item for both species, and polychaetes and gastropods for P. polyophthalma, as indicated by both the percentage by weight and the frequency of occurrence. The remaining prey categories contributed little to the diets of the two species. The niche breadth values (Zf’) calculated for the diets of both species indicated that P. polyophthalma had a slightly higher food breadth (2.25) than P. cluthratu (1.87). The dietary overlap value (0~~)between the two species was intermediate (0.528). SPATIAL

DISTRIBUTIONS

As indicated in Table IV, data from censuses illustrated the pattern of differential macrohabitat use between the two sandperches. Although P. polyophthalma had a broad habitat distribution, it was the most common on sandy flats, while P. cluthrata predominantly occurred in channels and not on sandy flats. The habitat overlap value (cc~) was low (0.369), and a x2 test for heterogeneity showed a highly significant difference in density by habitat type between the two species (1’ = 35.5, P < 0.001). Although P. polyophthalma and P. clathrata revealed a clear macrohabitat difference, they coexisted with nearly the same densities in channels where rubble areas were patchily distributed in sandy rubbIe areas with dead broken coral blocks of various sizes

RESOURCE SEPARATION IN CORAL REEF FISHES

215

TABLE III Percentage frequency of occurrence and percentage weight of food items in diets of P. polyophthalma and P. clathrata. P. polyophthalma

Food item

%F

Fish Decapods Portunid crabs Xanthid crabs Majid crabs Galatheid crabs Porcelain crabs Hermit crabs Alpheid shrimps Palaemonid shrimps Hippolytid shrimps Stomatopods Euphausids Tanaids Gammaridean amphipods Ophiuroids Sipunculids Errant polychaetes Sedentary polychaetes Gastropods Pelecypods Squids Number of fish examined Standard length (mm)

P. clathrata

%W

%F

%W

35

8.4

38

10.1

32 32

24.9 5.4

22 4 4 43 4 4 13 9

5.9 1.1 0.7 20.7 1.2 0.5 3.2 0.4

62 29 10 57

25.2 28.3 3.6 15.0

24 38

6.8 5.9

13 4 17 22 22 13

0.2 2.2 0.9 10.1 7.0 7.2

23 109-183

0.1 0.1

5 5 10 21 97-166

0.1 0.4 4.4

-, not consumed.

TABLE IV Densities of P. polyophthalma and P. clathrata observed in three habitats. Density is represented as number of fish censused per hour at each habitat. Percentage use of each habitat in parentheses. Habitat

P. polyophthalma

P. clathrata

Sandy flat Rubble reef Channel Total

47.2 (58.9) 7.4 (9.2) 25.5 (31.8) 80.1

0 (0) 1.5 (5.1) 27.9 (94.9) 29.4

(Table IV). However, the two species were not randomly distributed over channel sites. P. polyophthalma numerically dominated sandy rubble areas, whereas P. clathrata pre-

dominantly occurred in rubble areas (Table V). The x2 test showed this difference to be highly significant (2’ = 20.6, P < 0.001 for the number of male territories; x2 = 71.8,

M. SAN0

?Ih

Utilization of substratum types by P. polyophthalma and P. clarhrata at channel habitat. Values indicate total numbers of male territories and individuals of each species counted on each substratum at five charm&. Percentage use of each substratum in parentheses. Total area of each substratum examined was z 0.53 and 0.3 I ha for sandy rubble and rubble, respectively. Although some male territories included both sandy rubble and rubble substrata, either substratum predominated in each territory and so substratum nature of these territories was represented by predominant substratum type. P. polvophthalmu

Substratum type

Sandy rubble Rubble Total

I’. clathratri

Number of male territories

Number of tish (male t female)

Number of male territories

Number of fish (male + female)

21 (87.5) 3 (12.5) 24

57 (89.1) I (10.9) 64

5 (19.2) 21 (80.8) 26

10 (14.3) 60 (85.7) 70

P < 0.001 for the number of fish), suggesting that there is a differential microhabitat utilization between the two species at channels where both species coexist. TERRITORIALITY

AND

AGGRESSIVE

INTERACTIONS

All males observed in Table V occupied a territorial area which exhibited no overlap with conspecific males, and frequently patrolled along the borders of their territories. Heterospecific overlap of territories between P. polyophthalma and P. clathrata was only rarely found, except that peripheral areas of some territories overlapped with peripheries of congeneric neighboring territories. Aggressive interactions were intra- and interspecifically infrequent and usually limited to border encounters between neighboring males. However, intraspecific aggression between males was often intense when a territory was invaded. The home male invariably chased the intruder out of the territory at sight. When a P. clathrata male invaded the territory of a P. polyophthafma male, usuaily the former was aggressively attacked, causing it to flee immediately into his own territory. In the reverse case, however, attacks by a P. clathrata male were usually too weak, or lacking, to result in the eviction of the congeneric intruder from his territory. The intruder mostly stayed there for a few minutes and then returned to his own territory. DENSITY-MANIPULATION

EXPERIMENT

A removal experiment was conducted to elucidate whether the difference in microhabitat utilization is due to differences in microhabitat preference between the two species, or competitive interactions depending on microhabitat between them (see Discussion). The experimental results are summarized in Table VI. The data collected prior to density reduction at each of three experimental channels indicated a significant microhabitat diRerence between P. pofyoptihalma and P. clathrata (two-tailed Fisher

RESOURCE

SEPARATION

IN CORAL REEF

FISHES

217

exact test, P < 0.05 for number of male territories at each channel). Areas of available rubble and sandy rubble substrata were filled by closely packed territories of the two species. At Channel A from which P. cluthrutu was removed, no territory expansions into vacated sites after the removal experiment were found among five males of P. polyophthalmu. The size and location of territories held by these males were quite constant during the experimental period, like conspecifics at the control channel. At Channel B where P. polyophthulmu was removed, on the other hand, the data collected after removal suggested significant increase in utilization of vacated areas by P. cluthruta males relative to the control (one-tailed Fisher exact test, P = 0.015). That is, territory expansions into sandy rubble areas were observed in four males out of five at Channel B, but never at the control channel. The expanded territories were 1.29-2.58 (F = 1.80) times larger than territories prior to manipulation. In addition, two new territories were established on vacated areas at Channel B by incursions of P. cfuthruta males (Nos. 11 and 12 in Table VI) which had probably inhabited suboptimal habitats near the channel. However, such a phenomenon was not found at the remaining two channels. Densities of females did not change before and after the experimental manipulation at all channels (Table VI). At Channel B, however, two females of P. cluthrata transferred their home areas from rubble to sandy rubble substrata following the territory expansion and new territory establishment by males (Nos. 8 and 12, respectively).

DISCUSSION

My data suggest that differences in resource utilization between P. polyophthulma and P. cfuthratu at the study area are conspicuous in habitat rather than in food, although the dietary overlap value was 0.528. Most (59%) of the P.polyophthulmu population were found on sandy flats of the reef flat zone, while the great majority (95 % ) of the P. clathrutu population occurred at channel areas. In addition to this macrohabitat segregation, both species showed an apparent microhabitat separation at channels where they coexisted: P. polyophthulma was numerically dominant on a sandy rubble substratum, whereas P. clathrata was abundant on a rubble substratum. As pointed out by Connell (1980), there are two general ways in which these habitat separations may have come about. First, competition occurred between the two species due to their similar resource requirements, so each then occupied a different part of the habitat through niche shifts. Second, they were able to coexist without any significant interspecific competition at time of meeting, because each had already become adapted to a different part of the habitat. It is noteworthy that the second type of segregation can take place even under nonequilibrial situations. Thus, to ascertain whether the habitat segregation observed is attributed to competitive interactions between the two species is an important and inevitable point in determining principal factors permitting their coexistence.

A

Channel

P. clathrata

P. clathrata

3 4 5 1 2 3 4 5 6 7 8 9 10 11** 12*

L

1

(No.)

160 180 240 232 204 100 148 64 68 84 92 152 76 136 88

(a)

Territory size (m*)

SR SR SR SR SR R R SR R R R R R R R

type

Substratum

types by each of two mugiloidid

Male

of substratum

P. polyophthalma

Species

Utilization

VI

No. of females

fishes at channel

TABLE

168 152 196 176 132 112 64

160 180 240 232 204 Removed Removed Removed Removed Yes No Yes Yes Yes

No No No No No

SR SR SR SR SR SR

(2.58) (1.29) (1.50)

tory

(1.83)

(b/o)

(b)

experiment.

Substratum type of expanded or newly established terri-

After

and after removal

Territory expansion

before

Territory size (m2)

habitat

1 0 1”’

2$ 2

2

I

1 2 1 2 2

No. of females

P. clathrara

P. polyophthalma

6 I 8 9 10 11 12 13 14 15 16 13 14 15 16 11 18 290 144 258 220 132 192 128 216 164 220 180 40 152 108 64 12 16

SR SR SR SR SR SR SR SR SR SR SR SR R R R R R

1 1 2 1 2 1 2 2 2 2 2 1 2 1 1 1 2 Removed Removed Removed Removed Removed Removed 128 216 164 220 180 40 152 108 64 12 16 No No No No No No No No No No No

-

-

SR, sandy rubble; R, rubble. *Males which established new territories on vacated sites. **This female moved from harem of No. 9 male of P. clarhrata. Territory of No. 12 male was contiguous to No. 9 male’s territory. l This male defended a territory within which no females could be found during experimental period. $ Of these two females, one shifted her home area from rubble to sandy rubble substrata following territory expansion by her male.

(CControl)

P. polyophrhalma

Fi 2 E

1 1 1 2

m

?

G g

22 2 1 2

2 2

The results of the reciprocal removal experiment demonstrate that the microhabitat occupied by P. cluthrucu on channel areas is an outcome of current competitive interactions with P. polyophthalma. P. cluthruta broadened its use of microhabitat following removal of the competitor, but P. polyophthalmu did not. This finding and the observations of aggressive and territorial behavior suggest that there is a competitive dominance relation between these two species which is distinctly asymmetrical. P. pd~vphthafmu is an aggressively dominant species and so can predominately occupy its optimal microhabitat (sandy rubble substratum) at channels, while the subordinate P. clathrutm is compelled to shift its microhabitat to a rubble substratum which the dominant does not prefer. I conclude, therefore, that interspecific competition is a major determinant of coexistence between the two sandperches at channels, by promoting microhabitat partitioning between them. According to the taxonomy of Schoener (1983) the mechanism of competition between P. po&ophthulmu and P. cluthrata is most likely territorial, which is considered as part of interference and has been described among some other coral reef fishes, especially herbivorous damselfishes (Ebersole, 1985) and surgeonfishes (Robertson & Gaines, 1986). Although available space in channels was filled by closely packed territories of the two species, it is not clear what resource (e.g., food, refusing shelter, resting or spawning sites) they compete for or what resource is saturated (cf. Robertson et al., 198 1). The macrohabitat segregation between the two species, on the other hand, probably results from differences in their habitat adaptation which need not be the result of competition. This seems to be possibly explained by the following circumstantial evidence (Table IV), although a density-manipulation experiment was not carried out in this study. First, if P. cluthrutu was forced to shift its habitat to channel areas as the outcome of competition, it should occur in a considerable degree of density on rubble reefs unsuitable for P. polyophthulmu, because P. cluthruta was abundant on a rubble substratum at channel areas. Second, all individuals of P. cluthruta observed on rubble reefs were juveniles. Third, neither adult nor juvenile P. cluthrutu was found on sandy flats in spite of there being some small vacant space unoccupied by P. po&ophthalma. It appears, therefore, that the reef flat area (i.e., sandy flats and rubble reefs) is an unsuitable habitat for juvenile and/or adult P. clathruta, probably due to the absence of physiological and/or behavioral adaptation to that environment. The nonexistence of juvenile P. cluthruta on sandy flats may be attributable to habitat discrimination and selection by larvae (Shulman, 1984; Sale & Steel, 1986; Victor, 1986). Water depth may be a limiting environmental factor for the large-scale distribution of P. clnthmrtr. The general conclusion that can be drawn from my observational and experimental data is that interspecific competition is a major factor structuring small-scale habitat use, by reducing overlap between the two Purupercis species at Iriomote Island, but that in large-scale coexistence, differences in habitat adaptation between them may be important rather than competition. 1 do not think that this conclusion is equally applicable in all cases of other fish assemblages on coral reefs because there has been

RESOURCE SEPARATION IN CORAL REEF FISHES

221

some evidence to the contrary. For example, Doherty’s (1983) manipulative work on territorial, herbivorous damselfishes on the Great Barrier Reef showed no evidence for competitive interactions between members of this guild which partitioned microhabitat. Robertson & Gaines (1986) demonstrated that asymmetrical interference competition can have a strong influence on patterns of large-scale habitat use in a surgeonfish assemblage at Aldabra Atoll, Indian Ocean, by reducing overlap among competitors. All available evidence, including my results, indicate that mechanisms structuring coral reef fish assemblages vary among assemblages or among geographical locations. Furthermore, my study reveals that no single mechanism suffices in all situations even for a single assemblage within a location. Thus the structure of coral reef fish assemblages may be determined by the complex mixture of competitive and noncompetitive mechanisms such as species’ differential habitat preference (Waldner & Robertson, 1980; this study), insufficient recruitment (Doherty & Williams, 1988), or predation (Shulman, 1985; Doherty & Sale, 1985).

ACKNOWLEDGEMENTS

I am grateful to Makoto Shimizu for helpful suggestions and cooperation. I also would like to thank Hiroyuki Yokochi, Hiroyoshi Kohno, Hideo Sunagawa, and the Okinawa Regional Research Center, Tokai University, for assisting in the field work and sharing valuable information with me. Comments from J. T. Moyer, P. F. Sale, and two anonymous reviewers were very helpful. This study was made possible by Grantsin-Aid for Scientific Research from the Ministry of Education, Science and Culture, Japan (Nos. 63760145 and 01760148).

REFERENCES Anderson, G. R. V., A. H. Ehrlich, P.R. Ehrlich, J. D. Roughgarden, B.C. Russell & F. H. Talbot, 1981. The community structure of coral reef fishes. Am. Nat., Vol. 117, pp. 476-495. Berg, J., 1979. Discussion ofmethods ofinvestigating the food offishes, with reference to a preliminary study of the prey of Gobiusculwflavescens (Gobiidae). Mar. Biol., Vol. 50, pp. 263-273. Bouchon-Navaro, Y., 1986. Partitioning of food and space resources by chaetodontid fishes on coral reefs. J. Exp. Mar. Biol. Ecol., Vol. 103, pp. 21-40. Brock, R. E., C. Lewis L R. C. Wass, 1979. Stability and structure of a fish community on a coral patch reef in Hawaii. Mar. Biol., Vol. 54, pp. 281-292. Clarke, R.D., 1988. Chance and order in determining fish-species composition on small coral patches. J. Exp. Mar. Biol. Ecol., Vol. 115, pp. 197-212. Connell, J. H., 1980. Diversity and the coevolution of competitors, or the ghost of competition past. Oikos, Vol. 35, pp. 131-138. Connell, J. H., 1983. On the prevalence and relative importance of interspecific competition: evidence from field experiments. Am. Nat., Vol. 122, pp. 661-696. Doherty, P. J., 1981. Coral reef fishes: recruitment-limited assemblages? Proc. Fourth Znt. Coral Reef Symp., Vol. 2, pp. 465-470. Doherty, P. J., 1982. Some effects ofdensity on the juveniles of two species oftropical, territorial damselfish. J. Exp. Mar. Biol. Ecol., Vol. 65, pp. 249-261.

7’7 __.-

M. SAN0

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