Coral reef fish assemblages: intra- and interspecific competition for shelter sites

Environmental Biology of Fishes Vol. 13, No. 2. pp. XI-C)?. IO85 0 Dr W. Junk Publishers, Dordrccht.

Coral reef fish assemblages: intra- and interspecific competition for shelter sites

Myra J. Shulman Department of Zoology, University of Washington, Seattle, WA 98195, U.S.A. Present address: Smithsonian Tropical Research Institute, APO Miami, FL 34002, U.S.A.

Keywords: Aggression, Caribbean, Interference, Refuges, Predation, Territoriality

Synopsis

Observations were made on intra- and interspecific aggressive interactions among the fishes living in the rubble/sand coral reef habitat in St. Croix, U. S. Virgin Islands. Four species (beaugregory - Stegastes leucostictus; ocean surgeonfish - Acanthurus bahianus; doctor fish - A. chirurgus; common squirrelfish - Holocentrus rufus) which sheltered in holes on the reef all actively defended one to several shelter sites at dusk. Short-term shelter side fidelity was observed in three of these four species. Agonistic interactions over both food and shelter occurred during the daytime but much less frequently than agonistic interactions over shelter at dusk. Dominance in intraspecific aggression was determined almost completely by the relative sizes of the individuals involved, with the larger individuals dominating in 95-98% of all encounters. A similar, but less strong, relationship between size and dominance existed for interactions between closely related species. For aggressive encounters between unrelated species, however, both relative sizes and species identity determined the outcome. Species, both diurnal and nocturnal, which strongly defend several shelter sites may have a strong and disproportionate impact on the sheltering behavior of other fishes. Intraspecific and interspecific defense of shelter sites may determine the patterns of mortality that result from predation, thereby influencing population abundances and assemblage composition.

Introduction

Refuges from predation have been shown, for a wide variety of organisms, to be important in deter- mining the abundance as well as the spatial distribution of individuals (Emson & Faller-Fritsch 1976, Nelson & Vance 1979, Stewart & Pough 1983). For coral reef fishes, recruitment and early survivorship (Shulman 1984), movement patterns (Gladfelter 1979), and use of food resources (Ran- dall 1963) have been demonstrated or suggested to be related to availability and positioning of suitable shelter sites.

If predation is an important source of mortality

and shelter sites can provide protection from predation, then the ways in which individuals acquire and maintain access to shelter sites can modify patterns of mortality. In particular, behavioral defense of shelter sites can provide exclusive access to an otherwise unpredictably available resource; species and individuals which are less able or unable to defend shelter sites may suffer increased predation.

In this report, I examine aggressive interactions among coral reef fishes in one habitat type; I ask the following specific questions: (1) What are the die1 patterns in the frequency of aggressive interactions? (2) What resources are being defended? (3)

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Which species and size classes initiate the most aggression? (4) Which species and size classes re- ceive the most aggression? (5) How do aggressive interactions modify the use of resources, particularly shelter sites? This characterization of the nature and extent of interference competition for resources, particularly refuges, allows the con- sideration of how this process may interact with predation and shelter site availability to determine patterns of abundance and species composition of the fish assemblage.

Methods

Behavioral observations on seven species of coral reef fishes were made during June - July 1980 and May - October 1981 on St. Croix, U. S. Virgin Islands. The fish assemblages on small artificial reefs, built from Strombus shells, were the focus of these observations. These reefs, placed on sand at the lagoon edge of Tague Bay backreef, had been constructed for studies on the effects of habitat structure on recruitment. They consisted of 16 Strombus shells placed in a square meter, and were colonized by an average of approximately 80 individuals. The fish fauna on these reefs was charac- teristic of that found in the rubble/sand habitat. For detailed descriptions of the study site, the experimental reefs, and the fish fauna, see Shulman (1984).

Behavioral observations were made during two times of the day: (1) Daytime - anywhere from 0900-1600 h; (2) Dusk - the 45 min preceding night sheltering behavior by diurnal fishes. This corre- sponds to the period between 30min before and 15 min after sunset.

Individual fishes of six species (beaugregory - Stegastes leucostictus, goldspot goby - Gnatholepis thompsoni, bridled goby - Coryphopterus glaucofraenum, ocean surgeonfish - Acanthurus bahianus, doctorfish - A. chirurgus, french grunt - Haemulon flavolineatum) were observed for two minute periods, during which time all aggressive interactions with other individuals were noted. For each interaction I recorded whether the fish I was observing was the aggressor or the object of aggres-

sion and the species identity and relative size (com- paring total lengths) of the fishes with which it interacted. The observation periods were rotated between the 6 species being observed. For species with large abundance (>5), observations were rotated between three size classes with individuals within a size class chosen haphazardly. For species with 5 or fewer individuals on a reef, I recognized and rotated observations between individuals. Whenever possible, qualitative notes were also made on the resource being defended, the particular behaviors involved, and the location of the interaction.

During June - July, 1980 and May - September, 1981, observations were made on a number of different artificial reefs. Careful visual censuses were made on these reefs so that interaction rates as a function of species abundances could be determined. During October 1981, however, aggressive interactions were studied intensively on one Strom- bus reef for a three-week period during which a total of 734 observations were made. This body of data was used here to examine aggressive interactions of beaugregories, goldspot gobies, bridled gobies, and doctorfish. Ocean surgeonfish were absent or only one individual was present on this reef so interaction rates for this species were determined from the observations made earlier on the larger number of reefs.

In addition to quantitative observations, qualitative observations, during both daytime and dusk, were made on a number of occasions. During ten days in May 1981, aggression and sheltering behavior were observed on a small corner of one reef and all interactions and shelter site uses recorded. This provided some information on shelter site fidelity and number of holes defended.

Only a small number of quantitative observations was made on french grunts, all during the June - July, 1980 period. It became clear from casual observations that only a very small propor- tion of the grunt population was involved in initiat- ing aggression. The technique of randomly choos- ing individuals for observation is insufficient for characterizing this pattern of interaction. Aggres- sion among grunts described here was determined from qualitative rather than quantitative observa-

tions. In addition, McFarland & Hillis (1982) de- scribe in detail aggressive interactions among juvenile french grunts occurring in a very similar habitat and location.

Results

The following sections are species-specific ac- counts of aggressive interactions on the reef, in- cluding a description of the general biology of each species, aggressive behavior, aggression as a function of time of day, resources defended, and intra- and interspecific dominance relationships. Rates of interactions and the results of statistical tests are given in Tables l-6.

Beaugregory

The beaugregory, Stegastes leucostictw, is a small, relatively slender pomacentrid (damselfish) that feeds principally on algae as an adult but feeds on both invertebrates and algae as a juvenile (Emery 1973). Adults are strongly aggressive, defending territories against conspecifics, heterospecific her- bivores, and egg predators (Ebersole 1977). The individuals studied here were all small juveniles (15mm to 40mm SL) relatively recently settled

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from the planktonic larva period (probably within the previous 2 months).

Juvenile beaugregories were involved in frequent aggressive interactions with both conspecifics and heterospecifics. During the daytime, interactions occurred at a rate of 0.9 per minute, while during the dusk period, they occurred at a rate of 1.6 per minute (Table 1, Fig. 1).

The vast majority of beaugregory aggression was directed towards conspecifics (Table 2, Fig. 2). Each individual occupied a particular area of the reef and remained closely associated with one or two holes in that area. The smallest individuals rarely moved from their areas; the medium sized and larger juvenile would, at intervals, explore further from their territories. This frequently re- sulted in aggressive interactions between neighbors consisting of short darts at the victim or in long chases around the Strombus shells. The smallest individuals would retire at the first threat; interactions between large individuals, or similar sized individuals, produced the chases and occasional counter-attacks.

Juvenile beaugregories also attack, and are attacked by a number of other species. Juvenile acanthurids (both doctorfish and ocean surgeonfish) and beaugregories attacked one another fairly frequently, particularly at dusk (Tables 1 and 2).

Table 1. Rates of aggressive interactions (per minute) between beaugregories and other species on the reef are given for daytime and dusk observations. These interactions are divided into attacks by. and attacks against beaugregories. These data are means of 129 daytime and 64 dusk two minute observations.

Interacting species

Slippery dick, Halichoeres bivittatus Beaugregory, Stegastes leucostictus Goldspot goby, Gnatholepis thompsoni Bridled goby, Coryphoptew glaucofraenum Ocean Acanthurw bahianus surgeon, Doctorfish, Acanfhurw chirurgw French grunt, Haemulon jlavolineatum

Squirrelfish, Holocentrus rufus Other species

Total

Attacks by Attacks against Attacks by and against beaugregory beaugregory beaugregory

Day Dusk Day Dusk Day Dusk

0.04 0.10 0.005 0.03 0.05 0.13 0.31 0.57 0.17 0.38 0.48 0.95 0.10 0.09 0.04 0.01 0.14 0.10 0.12 0.04 0.005 0.03 0.12 0.07 0 0 0 0.05 0 0 0.04 0.03 0.01 0.10 0.05 0.13 0.05 0.14 0.005 0 0.06 0.19 0.005 0.01 0 0.02 0.005 0.03 0.02 0 0.01 0.01 0.03 0.01

0.67 0.97 0.24 0.61 0.91 1.59

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Fig. 1. Rates of aggressive interactions (per capita per minute) during the daytime and at dusk for five species of fishes.

When the beaugregories were very small, the acanthurids, which are considerably larger as juveniles, always ‘won’ the aggressive encounters. However, the largest juvenile beaugregories, and the medium sized acanthurids occasionally had standoffs, or the beaugregory, the smaller of the two, would win.

Juvenile beaugregories also attacked grunts, gobies, and particularly slippery dicks which ven- tured into their territories (Table 2). The grunts were almost always larger than the beaugregory and the gobies and slippery dicks frequently so

Ocean Doctorfish rurgaon

Fig. 2. Rates of aggressive interactions (per capita per minute) with conspecifics, confamilials and unrelated species for each of five species of fishes.

(Table 3). Beaugregories were also attacked by these three species, but much less frequently than the reverse.

The number of attacks beaugregories initiated increased significantly with increasing fish size (l-way ANOVA; p<O.O5). The smallest size class initiated 0.27 attacks per minute while the largest juveniles initiated 1.73 attacks per minute. Larger individuals suffered the fewest attacks (0.12 min-l)

Table 2. Rates of aggressive interactions (per minute) by beaugregories against other species and by other species against beaugregories. Both absolute rates and per capita rates (dividing by the number of individuals of that species present on the reef) are given. Differences between rates of attacks by and against beaugregories are determined with a paired T-test. These data are means of 193 two minute observations on beaugregories (see text). (* * * = p<O.OOl; * * = ~~0.01; * = p<O.OS; n.s. = not significant, p >0.05).

Interacting species Attacks by beaugregory Attacks against beaugregory T-test p

Absolute rate Per capita rate Absolute rate Per capita rate

Halichoeres bivittatus 0.06 0.005 0.01 0.001 Stegastes leucostictus 0.40 0.13 0.24 0.08 Gnatholepis thompsoni 0.10 0.0045 0.03 0.002 Coryphopterus glaucofraenum 0.09 0.002 0.01 0.0002 Acanthurus bahianus 0 0 0.015 0.04 Acanthurus chirurgus 0.035 0.01 0.04 0.01 Haemulon flavolineatum 0.075 0.0005 0.0025 0.00005 Holocentrus rufus 0.005 0.0025 0.005 0.0025 Other species 0.015 0.004 0.01 0.0025

** * * *** n.s. n.s. *** n.s. n.s.

*** Total 0.765 0.355

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Tuble3. Rates of aggressive interactions (per minute) between beaugregories and other species in which the attacker was larger than the victim and in which the attacker was smaller than the victim. Differences between these two rates were determined using a T-test. (* * * = p<O.OOl; * * = p<O.Ol; * = p-CO.05; n.s. = not significant, psO.05.)

Interacting species Attacker larger than victim Attacker smaller than victim

R SD x SD

T-test p

Halichoeres bivittatus 0.03 0.17 Stegastes leucostictus 0.60 0.93 Gnatholepis thompsoni 0.06 0.26 Coryphopterus glaucofraenum 0.04 0.19 Acanthurus bahianus 0.02 0.19 Acanthurus chirurgus 0.04 0.17 Haernulon flavolineatum 0.01 0.05 Holocentrus rufus 0.01 0.06 Other species 0.01 0.11

Total 0.80 1.05

0.04 0.01 0.04 0.04 0 0.04 0.07 0.003 0.015

0.25

0.21 0.09 0.16 0.17 0 0.21 0.26 0.04 0.11

0.55

n.s. ***

n.s. n.s. n.s. n.s. ***

n.s. ns.

***

while the smallest and medium sized beaugregories were attacked 0.43-0.45 times per minute. Qualita- tive observations suggested that the fish spend more time attacking individuals that are smaller, but close to their own size, rather than attacking just the smallest or all smaller individuals equally. This observation is supported by the nearly equal attack rates against small and medium sized juvenile beaugregories.

Ocean surgeonfish and doctor-fish

These two species, members of the family Acanthuridae (surgeonfish), are deep-bodied, lat- erally compressed fishes of very similar external morphology and coloration. The common family name comes from the sharp, razor like spine set into a horizontal groove along the side of the caudal peduncle. The spine can be flicked out by bending the tail, and is presumably used both defensively and offensively. Despite this weapon, juvenile surgeonfishes are not uncommonly preyed upon by piscivorous fishes on the reef (personal observations). Ocean surgeonfish and doctorfish are her- bivorous, both as juveniles and adults; in my study area they were observed feeding on both drift algae and benthic algae, particularly epiphytes on seagrass and Strombus shells. Ocean surgeonfish and doctorfish feed in schools, sometimes monotypic,

but more frequently, particularly for juveniles, they feed schooling with congeners and/or parrotfishes (Scaridae). Surgeonfishes settle out from the plankton as transparent metamorphosing larvae and appear to acquire pigmentation within a few days. On the Strombus reefs on which acanthurids occurred, there were usually 3-20 individuals.

Juvenile doctorfish were involved in large numbers of aggressive interactions (Fig. 1). During the daytime, the average doctorfish attacked another fish, or was itself attacked 0.65 times per minute. At dusk, interaction rates were more than three times higher, 1.98 interactions per minute, a statistically significant increase over daytime interaction rates. Juvenile ocean surgeonfish were involved in similar rates of interactions: 1.14 per minute during daytime and 1.78 per minute at dusk.

Doctorfish interacted most frequently with conspecifics and congeners (Fig. 2, Table 4). The average rate of attacks between doctorfish was 0.83 min-l (combining both day and dusk observations) (Table 4), while for ocean surgeonfish it was l.l4min-i (Table 5).

Individual acanthurids were approximately equally (or slightly more) aggressive towards their congeners as they were towards their conspecifics (Fig. 2). For observations on ocean surgeonfish, the per capita rate of aggression with other ocean surgeonfish was 0.24 attacks per min while aggres-

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Table 4. Rates of aggressive interactions (per minute) by doctorfish against other species and by other species against doctorfish. Both absolute rates and per capita (dividing by the number of individuals of that species present on the reef) are given. Differences between rates of attack by and against doctorfish are determined with a paired T-test. These data are means of 219 two minute observations on doctorfish (see text). (* * * = p<O.OOl; * * = p<O.Ol; * = p<O.O5; n.s. = not significant, p>O.O5.)

Interacting species Attacks by doctorfish Attacks against doctorfish T-test p

Absolute rate Per capita rate Absolute rate Per capita rate

Halichoeres bivittatus 0.005 0.0005 0 0 Stegastes leucostictus 0.08 0.02 0.01 0.0025 Gnatholepis thompsoni 0 0 0.005 0.0003 Coryphopterus glaucofraenum 0.005 0.0001 0.005 0.0001 Acanthurus bahianus 0.025 0.08 0.09 0.28 Acanthurus chirurgus 0.45 0.14 0.38 0.11 Haemulon flavolineatum 0.02 0.0002 0 0 Holocentrus rufus 0.0025 0.0015 0.08 0.04 Other species 0.005 0.001 0.003 0.0005

Total 0.56 0.60

0.08 *** 0.08 n.s. 0.06 n.s. * *** n.s.

ns.

sion with doctorfish occurred at a rate of 0.27 attacks per min (Table 5). For observations on doctorfish, per capita rates of interactions between doctorfish were 0.25 min-i; between doctor-fish and ocean surgeonfish per capita attack rates were 0.39 min-l (Table 4).

Aggressive interactions between different sized individuals (and frequently between similar sized individuals) are head-on attacks; presumably the attacker is threatening to bite. Response from the victim is almost always an evasive movement. Sometimes, particularly between similar sized individuals, or on the rare occasions when a smaller individual attacks a larger one, the victim will attack back.

In addition to direct attacks, avoidance behavior occurs often as well. Frequently, larger individuals would just feint in the direction of a smaller one and it would leave or not approach. Even when a nearby larger individual didn’t appear to be look- ing at the smaller individual, the smaller fish appeared to be taking evasive action.

Attacks between similar sized individuals (frequently) and different sized individuals (sometimes) can involve tail beating or pushing; presumably, in these encounters, the caudal peduncle spine is being used as a threat or an actual weapon. This kind of interaction also occurs with beau-

gregories, and by the largest ocean surgeonfish against a larger common squirrelfish (Holucenrrus rufus) .

In attacks between acanthurids there appears to be a very strong dominance hierarchy based on size; in 98% of the acanthurid-acanthurid interactions, a larger individual was attacking a smaller individual (Table 6, Fig. 3). There also appears to be more aggression between individuals of similar size than between individuals on the hierarchy ex- tremes. The largest acanthurids experience a relatively low rate of aggression (0.30 attacks per min) while the smallest two size categories experience aggression at a nearly equal and high rate of 0.72 attacks per minute (differences between largest and smallest two size categories are statistically significant, Student-Newman-Keuls Test, ~~0.05).

Dusk and daytime interactions differed mark- edly in character. Daytime aggression between acanthurids was almost always over food items; dusk aggression was entirely related to shelter sites. During the day, the acanthurids would move as a loose school around the reef, or several meters away, feeding on algae. When smaller individuals were feeding on a ‘good’ algal clump, larger individuals would frequently dart at them and chase them off. If the larger individual was feeding first, it would often scare off smaller individuals that

87

Table 5. Rates of aggressive interactions (per minute) by ocean surgeonfish against other species and by other species against ocean surgeonfish. Both absolute rates and per capita (dividing by the number of individuals of that species present on the reef) are given. Differences between rates of attack by and against ocean surgeonfish are determined with a paired T-test. These data are means of 71 two minute observations on ocean surgeonfish (see text). (* * * = p<O.OOl; * * = p<O.Ol; * = p-CO.05; n.s. = not significant, p>O.OS.)

Interacting species Attacks by ocean surgeonfish

Absolute rate Per capita rate

Attacks against ocean surgeonfish

Absolute rate Per capita rate

T-test p

Halichoeres bivittatus 0.015 0.008 0 0 Stegastes leucostictus 0.09 0.013 0.02 0.005 Gnatholepis thompsoni 0.015 0.002 0.005 0.0005 Coryphopterus glaucofraenum 0.005 o.ooix 0.015 0.0015 Acanthurus bahianus 0.50 0.1 1 0.64 0.14 Acanthurus chirurgus 0.03 0.08 0.07 0.19 Haemulon flavolineatum 0.005 0.0005 0.005 0.0005 Other species 0.005 0.002 0 0

n.s.

n.s.

“.S.

n.s. n.s. n.s. n.s.

0.76 0.66 ll.S.

attempted to join it. Larger individuals would occa- ones) would enter and defend several nearby holes. sionally dash a meter or more to attack a smaller Frequently, a larger individual would chase a feeding individual. smaller one from several holes in succession.

At dusk, the acanthurids had completely stop- ped feeding, or fed only rarely. They kept closer to the reef and frequently entered the holes in the Strombus shells. Individuals appeared to prefer one or two holes and would defend them against all intruders that they were capable of attacking. In addition however, individuals (particularly larger

Qualitative observations revealed that for acanthurids, shelter site fidelity exists over at least a short period of time (5-20 days). Two individuals were observed changing holes during the study period. The potential new hole was vigorously defended over a period of days, along with the old hole (and several nearby holes were defended

Table 6. Rates of aggressive interactions (per minute) between acanthurids and other species in which the attacker was larger than the victim and in which the attacker was smaller than the victim. Differences between these two rates were determined using a T-test. (* * * = p<O.OOl; * * = p<O.Ol; * = p<O.O5; n.s. = not significant. p>O.OS.)

Halichoeres bivittatus Stegastes leucostictus Gnatholepis thompsoni Coryphopterus glaucofraenum Acanthurus bahianus .~1ccmthuru.s chirurgus Haemulon flavolineatum Holocentrus rufus Other species

Interacting species Attacker larger than victim

R SD

0 0.28

0.035 0 0.55 0.86

0.05 0.25

0.035

0 0.08 0.003 0 0.11 0.77 0.005 0.08 0.003

Attacker smaller than victim - R SD

0.003 0.035 0.01 0.09

0.003 0.035 0.005 0.05 0 0 0.015 0.10

0.015 0.12 0.003 0.04

0.003 0.035

T-test p

ns ***

n.s. n.s. *** ***

ns. ***

ns.

Total 1.04 1.23 0.06 0.22 ***

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Hdspot goby

Bri 0

. died Burgeontwws oh

0 Conspecifics

q Confamilials

q Others

Fig. 3. For five species of fishes, the percent of aggressive interactions with conspecifics, confamilials, and unrelated species in which the attacking fish was larger than the individual being attacked.

mildly), after which the fish switched sleeping holes. Both holes continued to be defended even after the transfer had taken place, although the new hole appeared to be defended more strongly.

Goldspot and bridled gobies

Goldspot and bridled gobies (family Gobiidae) are bottom dwelling fishes living almost exclusively in sand and rubble habitats. They lack a swimbladder and sit on the bottom, using their pelvic fins and tail for support. They move by ‘hopping’ off the bottom with the pelvic fins and propelling themselves forward with the pectoral and caudal fins. They feed by picking up mouthfuls of sand and filtering out both animal and plant material with the gill rakers. Both species are white and cryptic against the white sand background, although bridled gobies are somewhat more transparent. The gobies are restricted to sand areas that have structure that provides holes for shelter and nesting (Shulman 1984). When frightened by predators or divers, the gobies move close to, or into shelter holes.

Gobies are involved in aggressive interactions just as frequently during the day (0.41 interactions per min for goldspot; 0.18 min-‘for bridled) than as at dusk (0.40min-1 for goldspot; O.l7min-’ for bridled) (Fig. 1).

The majority of goldspot gobies’ aggressive ac- tivities are directed towards conspecifics (Fig. 2); on average, a goldspot goby will attack, or be attacked by another goldspot goby once every 3.3 minutes. Bridled gobies are less intraspecifically aggressive, interacting at a rate of once every 5.9 minutes.

While moving around on the sand, gobies appear to demonstrate a great deal of avoidance behavior, both of conspecifics and the other species of goby. Smaller gobies in particular will move off in another direction if a larger goby is moving towards them, or will change feeding directions if heading towards another fish. A few of the largest individuals (usually goldspot gobies) spend the majority of their time close to, or in holes (conch shell holes or holes formed by the shell surface and the sand). These individuals are frequently the most aggressive, attacking not only gobies but other species that wander by as well. These individuals are presumably males, guarding and tending nests within the holes. They will ‘hop’ up and attempt to bite the intruder as it swims overhead. Some large gobies will also do this to beaugregories or acanthurids which are attempting to chase them away.

The majority of the goby individuals did not shelter in the shell holes at night. The few individuals that did move into the shelter arena at dusk were often attacked by the beaugregories defending holes there.

A size dominance hierarchy exists among gobies (Fig. 3). In 98% of intraspecific attacks among goldspot gobies, the attacker was larger than the victim. The same was true for 95% of aggressive interactions among bridled gobies. When goldspot and bridled gobies attacked one another, however, the larger individual was the aggressor only 76% of the time (Fig. 3). The majority of the reversals were cases of smaller bridled gobies attacking larger goldspot gobies. The largest size class of bridled gobies suffered far fewer attacks than the smaller two size classes (Student-Newman-Keuls Test; ~~0.05). Individuals in the smallest size class were attacked 17 times more frequently than the largest size class, and those in the intermediate size class suffered 28 times more attacks than individuals in the largest size class.

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The number of aggressive acts initiated increases with increasing fish size; the largest goldspot gobies initiated over twice as many attacks as the smallest, the largest bridled initiated almost three times as much aggression as the smallest. Again, as was true for the beaugregories and acanthurids, it was the individuals who were closest in size that appeared to interact the most frequently. Medium sized gobies suffered high rates of attacks compared to the smallest size class, although these differences were not statistically significant.

French grunts

French grunts (family Haemulidae) school over the reef during the day and migrate out into sand and/ or seagrass habitats at night. Adults feed on benthic invertebrates in the sand/seagrass at night; small juveniles feed during the day on plankton while schooling on the reef and do not feed at night (McFarland 1979, Brothers & McFarland 1981).

Only a few quantitative behavioral observations of grunts were made as part of this study. These, and the qualitative observations, indicated that intraspecific agonism was not uncommon, but was most often initiated by only a few individuals. On the Strombus reef studied extensively during Octo- ber, 1981 there were approximately 110 grunts. Of these, only one, the largest individual, was aggressive, defending a territory close to the substrate on one side of a Strombus shell. The rest of the individuals in the school were non-territorial, and engaged in agonistic interactions with one another fairly rarely. Grunts were attacked not uncommonly but not often by more aggressive species on the reef such as the beaugregories, acanthurids, and squirrelfish (Tables 1, 2, 4 and 5).

The mainly qualitative observations made on grunts here are in accord with the extensive study on the behavior of juvenile grunt schools by McFarland & Hillis (1982). They found that the largest individuals in a school defended territories on the schooling site; these territories appeared to be the areas most protected from predators and currents. They also found that aggression rates among grunts are highest at dawn as the grunts return to their daytime schooling site, are low during the day, and rise again in the late afternoon.

Common squirrelfish

There were two adult common squirrelfish, Holo- centrus rufus (Holocentridae) present on the reef studied intensively during October 1981. No quantitative, but extensive qualitative observations were made during that time period. Squirrelfish spend daylight hours in holes or caves on reefs, emerging at night to feed on benthic invertebrates. On the Strombus reef, each of the two squirrelfish occupied the aperture of a shell during the day, remaining far inside the shell and just visible to an observer. As twilight approached, the squirrelfish slowly emerged from the shell, hovering just above their daytime refuge. They defended this hole against all the other fishes on the reef; in addition, fishes were also vigorously chased out of nearby holes by the squirrelfish. A large number of interactions occurred between squirrelfish and acanthurids (Tables 4 and 5) and beaugregories (Tables 1 and 2), although no species was completely immune. The holes the squirrelfish were defending were completely unavailable to other fishes, whether nocturnal or diurnal; observations indicated that no other fishes ever entered the holes defended by the squirrelfish although similar, undefended holes on the reef were frequently occupied by many fishes during the dusk period. Squirrelfish appear to have a strong impact on availability of holes to diurnally active fishes attempting to enter nocturnal shelter sites. It is probable that observations at dawn would reveal that squirrelfish are intra- and interspecifically aggressive when entering their daytime shelter sites as well.

Discussion

Agonistic interactions, both intraspecific and interspecific, are common among the juvenile and older coral reef fishes studied here. Aggression occurring during the daytime appears to be mainly over food or feeding areas, with occasional aggression over shelter sites. For species that shelter in holes on the reef, rates of aggression are higher during dusk than during daytime (Fig. l), and aggression at

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dusk appears to be entirely related to shelter site defense. These interactions occur between diurnal fishes attempting to enter holes for the night and between diurnal fishes and nocturnal fishes that are just emerging from their daytime shelter sites. Other studies have noted shelter site defense by various species of fishes (Hobson 1972, Reinboth 1973, Myrberg & Thresher 1974, Smith 1978, Robertson & Sheldon 1979).

Among the fishes studied here, beaugregories, ocean surgeonfish, doctorfish, and squirrelfish all defend holes at dusk. A notable aspect of this shelter site defense is that not just one hole is defended; individuals appear to prefer (that is, enter most frequently, and sleep in) one hole, but vigorously defend nearby holes as well. Other fishes are attacked and chased out of defended holes and, not uncommonly, pursued and evicted from several holes in quick succession.

There are at least two possible reasons for fishes defending several, rather than just one hole: (1) A predator may enter the hole during the night, driv- ing the occupant out and forcing it to occupy another hole; (2) The defender may itself be evicted from its preferred hole by a more dominant fish; defending other holes gives the expulsed fish some- where else to take refuge.

Preliminary observations suggest that acanthurids sleep in the same hole for up to a week. Transfer to a new sleeping shelter site was made gradually, with both the new and the old holes defended for a period of days before the fish trans- ferred from one hole to the other. Hole site fidelity was also observed in the two squirrelfish that occupied the reef for the entire three week observation period. Other authors have found evidence for at least short-term shelter site fidelity in various groups of coral reef fishes: wrasses - Labridae (Hobson 1972)) damselfish and wrasses (Robertson & Sheldon 1979); comb blennies - Clinidae, wrasses, glasseyes - Priacanthidae (Clarke, personal communication); juvenile parrotfishes - Scaridae, and acanthurids (Wolf, personal communication); and grunts (Ogden & Ehrlich 1977, McFarland et al. 1979, McFarland & Hillis 1982).

Dominance in intraspecific aggression appears to be almost completely determined by size (Fig.

3). Larger individuals initiated between 95 and 98% of all intraspecific attacks. Within a species, the largest individuals initiated the most aggression, while small and intermediate sized individuals suffered equal, and large numbers of attacks. It appears that aggression may occur most frequently between individuals that are closest in ranking on the dominance (= size) hierarchy.

Dominance in interspecific interactions is a much more complex phenomenon. Between species with similar morphology and behavior, dominance hierarchies seem to be based mainly on size (goldspot versus bridled gobies; ocean surgeonfish versus doctor-fish). For dissimilar species pairs, however, the species identity and size differences of the particular individuals involved appear to have a strong effect on the outcome of aggressive interactions. The common squirrelfish on the reef could effectively chase small doctorfish and ocean surgeonfish out of holes but was successfully fended off by the largest juvenile ocean surgeonfish, even though it was still considerably smaller than the squirrelfish. Similarly, the largest sized juvenile beaugregories studied were capable of successfully attacking larger doctorfish, but the small and medium sized beaugregories were unable to do so.

The consequence of high rates of aggression over shelter sites (Fig. 2) and a dominance hierarchy based roughly on size (Fig. 3) is that smaller fishes suffer frequent eviction from shelter sites during the dusk period. Hobson (1965, 1968, 1972) has suggested that twilight periods represent the time of greatest risk of predation for coral reef fishes. The orderly process of shelter seeking by diurnal fishes, tightly linked to light levels, and the care- fully timed emergence and/or migrations of nocturnal fishes have been interpreted as evolving in response to intense predation pressure at dusk (Starck & Davis 1966, Hobson 1969,1972, Collette & Talbot 1972). Munz & McFarland (1973) have hypothesized that during twilight periods, the piscivores have a visual advantage over their prey, which leaves the prey especially vulnerable at this time of day.

Smaller fish probably suffer an increased and high risk of predation at dusk for four reasons: (1)

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Smaller fish swim more slowly than larger ones (within a species) and are less likely to escape from predators (Mum & McFarland 1973); (2) smaller fish are in the size range of acceptable prey for more predators; (3) smaller fishes are more frequently evicted from shelter sites and presumably spend more time outside of shelter sites at dusk; (4) the probability that smaller fish will detect predators may be lower because (a) they have to watch out for attacking competitors as well and (b) visual acuity is reduced in smaller fish (Munz & McFar- land 1973).

It appears probable that, within a habitat type, recruitment and early survival of coral reef fishes are strongly influenced by three interacting factors: (1) the availability of appropriate shelter sites; (2) predation pressure; and (3) intra- and interspecific aggression among fishes using and defending shelter sites or territories.

There is some direct, and some inferential evidence supporting the importance of these three factors. Experiments involving manipulations of shelter site availability demonstrated that recruitment and early survival of coral reef fishes increases with increases in the density of shelter holes (Shulman 1984). Shulman (1985) showed that the spatial distribution of predators (as a function of distance from the reef) results in increased successful recruitment in areas of lowered predation pressure. Reaka et al. (personal communication) have found that recruitment is higher on caged artificial reefs compared to those from which predators are not excluded. Stimpson (1981) found changes in reef fish assemblage composition on a patch reef from which moray eels had been removed.

The evidence that aggressive interactions affect recruitment success is more inferential. A number of studies have shown that occupied reefs have lower recruitment rates than unoccupied reefs (Talbot et al. 1978, Molles 1978). Shulman et al. (1983) demonstrated that a resident adult damselfish decreased successful recruitment of three other species. The observations reported here indi- cate that aggression over shelter sites occurs frequently among juvenile fishes, particularly at dusk, the time of presumed greatest vulnerability to predation. The smallest (most recently recruited)

fishes suffer the most aggression and presumably suffer increased predation on reefs that are occupied by larger juvenile and adult fishes. These observations do not, however, directly test the hy- pothesis that these interactions limit population sizes and influence assemblage composition. The experiments on shelter site limitation (Shulman 1984), however, do suggest that this may be occurring. The relationship between number of holes and number of fishes (with area kept constant) is not linear; as hole density increases the fish per hole ratio decreases. Since these fishes are defending a number of holes within an area, it is probable that as the distance between holes decreases the number of holes any one fish can successfully defend will increase. If this is true, shelter site defense can explain the shape of the relationship between hole density and fish density.

The fact that much of intra- and interspecific aggression among coral reef fishes is size depen- dent means that reversals of dominance can occur between species. These reversals in competitive ability may provide a partial explanation for main- tenance of high species diversity of coral reef fishes; similar mechanisms have been proposed to be of importance in communities of benthic organisms (Jackson 1979).

Acknowledgements

Assistance in collecting the data was provided by J.G. Morin and N.G. Wolf to whom I offer my thanks. Valuable contributions to the manuscript were made by R.T. Paine, S. Palumbi, G. van Vliet, N.G. Wolf, and an anonymous reviewer. Funding was provided by a NSF Predoctoral Fel- lowship, a NSF Dissertation Improvement Award, grants from Sigma-Xi and the Lerner-Gray Fund for Marine Research, and two NSF grants (OCE 7726901 and OCE 8025578) to R.T. Paine. This is contribution number 113 from the West Indies Lab- oratory.

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Accepted 25.5.1984

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Coral reef fish assemblages: intra- and interspecific competition for shelter sites