Responses of tropical reef fauna to brittle-star luminescence (Echinodermata: Ophiuroidea)

J. Exp. Mar. Biol. Ecol., 1988, Vol. 115, pp. 157-168 Elsevier

157

JEM 01011

Responses of tropical reef fauna to brittle-star luminescence (Echinodermata : Ophiuroidea) Matthew S. Grober Department of Biology, University of Calfornia at Los Angeles, Los Angeles, Cal$omia, U.S. (Received

13 July 1987; revision

received

16 October

1987; accepted

23 October

1987)

Abstract: The behavior ofcaribbean reef animals was observed in response to luminescent signals produced by the brittle-star Ophiopsila rikei (Liltken). Field observations on various species and laboratory observations on decapod crustaceans showed differences between species in responsiveness to contact-elicited luminescent flashes. Actively foraging predators and scavengers, including an octopus, Octopus briareus (Robson), two species of shrimp, Rhynchocinetes rigens (Gordon) and Brachycarpus biunguiculatus (Lucas), a blenny, Malacoctenus sp., and a number of small decapod crabs, primarily produced avoidance behaviors towards luminescent flashes in the field. Other smaller scavengers, hermit crabs and small shrimps, and a cleaner shrimp, Stenopus hispidus (Oliver), showed minimal responses to field flashes. In laboratory experiments, a lobster, Panulirus argus (Latreille), and Brachycarpus biunguiculatus exhibited increased avoidance and decreased predatory responses to luminescent brittle-stars vs. nonluminescent controls. Stenopus hispidus, however, did not show any significant changes in predatory or avoidance behaviors between luminescent and nonluminescent ophiuroids. The differences in species responsiveness is statistically related to their feeding behavior, and is associated with their proximity to dense aggregations of luminescent brittle-stars. The differing responses of reef animals to luminescent flashes may affect their spatial and temporal distribution and in turn have an effect on the structure of nocturnal reef communities. Key words: Behavior;

Bioluminescence;

Coral-reef

fauna;

Ophiuroidea

INTRODUCTION

A diverse group of coastal benthic invertebrates produces bioluminescent signals (Morin, 1983). Although much is known about the biochemical, physiological, and

morphological

aspects of light production

in these species (Herring,

1978), few studies

have addressed the behavioral and ecological significance of bioluminescence to coastal light emitters. Based on the similar emission characteristics of coastal luminescent signals, Morin (1983) proposed that most of these signals function as predator deterrents. Esaias & Curl (1972) and White (1979) have shown that dinoflagellate bioluminescence functions decrease herbivory by copepods, and Buskey et al. (1983) showed that copepods exhibit avoidance behaviors in response to dinoflagellate flashes. These studies provide support for Morin’s proposal, but they involved pelagic species only. Basch (1985) reported that luminescent signals produced by a temperate sandCorrespondence address: M. S. Grober, Los Angeles, CA 90024, U.S. 0022-0981/88/$03.50

0

1988 Elsevier

Department

Science

of Biology, University

Publishers

B.V. (Biomedical

of California

Division)

at Los Angeles,

158

M. S. GROBER

dwelling ophiuroid elicits avoidance responses from various nocturnally active predators, and Grober (in press) has shown that luminescence in a tropical reef brittle-star functions as an aposematic predator deterrent against three species of portunid crabs. The current study expands on this work to address the effects of brittle-star luminescence on an ecologically diverse suite of nocturnally active reef animals. Ophiopsila riisei (Lutken) is a luminescent brittle-star found in shallow reefs throughout the Caribbean Sea. 0. riisei takes refuge by day in crevices on coral heads or in coral rubble, forms dense aggregations (normally consisting of 100-200 ind. * m - *, but sometimes > 1000 ind. . me2), that are predictable in space and time, and feeds exclusively at night by extending its long arms (arm length z 10 cm and disc diameter s 1 cm) into the water column to catch suspended matter (Grober, in prep.). While feeding at night, it exhibits a graded response when disturbed. A minor mechanical disturbance triggers a faint luminescent flash, while more vigorous stimulation elicits a bright flash that travels along the arms, coupled with withdrawal into the substratum. Flashes are always produced in response to mechanical stimulation and the intensity of a flash is proportional to the intensity of stimulation. Although some luminescent displays may be elicited by mechanical stimuli from water currents or other physical factors, the majority (at least 70 %, see Results) are apparently caused by nocturnally active reef animals. The purpose of this study was to investigate the responses of a diverse group of such animals to Ophiopsila luminescence. Specifically, this study addresses the differences in responsiveness of a variety of nocturnally active species to luminescent flashes, and attempts to identify the ecological and behavioral correlates that may give rise to these differences.

MATERIALS

AND

METHODS

All collections and observations were made between November 1984 and February 1985. The crustaceans and ophiuroids used for laboratory observations were collected in 1.5-5 m of water in the shallow reefs and sand flats surrounding the Smithsonian Tropical Research Institute field station in the San Blas Islands, Panama (9”33’14”N: 78”55’23”W). The crustaceans studied were all active at night in the vicinity of 0. riisei aggregations (some species were active throughout the day and night) (Grober, unpubl. data). They were collected by hand or with hand-held nets, and maintained in large aquaria. The water in these aquaria was changed daily and all animals were fed crab tissues (various species of small crabs) every two days. 0. riisei was collected at night by squirting dilute vinegar (50 : 50 with sea water) into their crevices. This caused SO-90% of the individuals to emerge from the reef. The ophiuroids were maintained in aquaria provided with ceramic tiles (30.5 cm’) that had 16 equidistant holes (0.84 cm diameter) drilled through them. Similar to their natural behavior patterns, the ophiuroids stayed under the tiles during the day and extended

BRITTLE-STAR

LUMINESCENCE

IN CORAL

REEFS

159

their arms out through the holes or around the edges of the tiles at night. They showed no ill effects of the collection treatment. Ophioderma cinereum (MUller et Troschel) was used as a control in these experiments because they coexist with Ophiopsilariisei, are a common nocturnally active species, and are not luminescent. Ophioderma was collected by hand, maintained in a large aquarium, and used within 1 wk of collection.

LABORATORY

OBSERVATIONS

Observations were made at night in moonlight or using a dim red light (wavelength >660 nm, Kodak Wratten Filter 70). Crustaceans have poor vision in these long red wavelengths (Goldsmith & Femandez, 1968) and red lighting had no obvious effects on the crustaceans or ophiuroids both in the laboratory and in the field. Because of their abundance in the study area, two species of shrimp, Stenopus hispidus (Oliver) and Brachycarpus biunguiculatus (Lucas), and one species of lobster, Pam&us argus (Latreille), were chosen for laboratory observations. Each shrimp or lobster (respondent) was isolated in an opaque aquarium (29.8 cm diameter x 9 cm water depth) for 24 h before the experiment and deprived of food for this period. An individual Ophiopsila riisei was then gently lowered into the aquarium at a point farthest from the respondent. No luminescent flashes were produced as the brittle-stars were placed into the aquaria. To control for nonluminescent stimuli (i.e., chemosensory), individuals of 0. riisei were anesthetized for 5 min in magnesium chloride (isotonic to sea water), which inhibited the production of luminescence for the duration of the trial. Since anesthetization also immobilized 0. riisei, Ophioderma was used as a control to provide a nonluminescent ophiuroid that was not immobilized. All respondent behaviors were observed for 30 min and verbally described (and recorded in a hand-held tape recorder). Each respondent was given 1 h between ophiuroid types and the order of presentation of the ophiuroids was randomized, except that no preparation was given twice in succession. Five individuals of each respondent species were tested, and each had a total of five interaction periods with each ophiuroid preparation. All ofthe trials with one respondent were completed over a 5-night period. Following the experiments, the tapes were transcribed with reference to a 30-min time base. I noted all behaviors that followed a contact between a respondent and an ophiuroid. I present here only the analysis of the total numbers of each of the behaviors occurring in the 30-min period. To facilitate interpretation of the results, behaviors were placed into predatory, avoidance, or no-response categories. Behaviors were categorized based on their effect on the ophiuroids, and thus any behaviors that were harmful to ophiuroids were grouped as predatory, regardless of whether the crustacean was a known predator or scavenger. Cheliped Grab/Hold and Cheliped Grab/Eat (Leg Grab/Hold and Leg Grab/Eat for Pan&w argus) were grouped as predatory behaviors because they consistently had damaging effects on the ophiuroids. Cheliped Grab/ Retract, Change Direction, Swim Away (Flip Away for P. argus), and Stop/Move Away

160

M. S. GROBER

were grouped as avoidance behaviors because they rarely produced harmful effects to the ophiuroids and normally resulted in the respondent being displaced with respect to the ophiuroid. The final two categories, No Response and Stop/Stay, were placed into a variable behavior category. The No Response behavior was considered to have a variable effect because the lack of a response cannot be grouped in either the predatory or avoidance categories. The Stop/Stay behavior was also equivocal because the respondent usually ended up next to or touching the ophiuroid, but in no cases was the ophiuroid damaged. Data were normalized for analysis using a log transformation. The differences between the means for each behavior in response to the three ophiuroids were tested with a l-way ANOVA. Unplanned comparisons between means were performed using the T’ method with an experimentwise error rate of 0.05 (Sokal & Rohlf, 1981). FIELD

OBSERVATIONS

Field observations were conducted to assess the relative frequency of Ophiopsilariisei flashes, which animals elicit flashes, and any behavioral responses of these animals to the flashes. Previous observations showed that 0. riisei can be found in a variety of habitats, including reef slopes, rubble/pavement areas, and isolated patch reefs (see Dal11 et al., 1974, for habitat descriptions). Two different observation methods were used so that 0. riisei could be observed across the range of its local habitats and within a habitat where it occurs in dense patches. Fifteen 30-min swims were conducted across the full range of 0. riiseihabitats, ranging from shallow patch reefs (1.5 m) to reef slopes down to a depth of 25 m. Dive sites were chosen haphazardly from areas with known 0. riisei populations, and the swims were done by skin or scuba diving at night without the use of white lights. All medium to large flashes were noted and then the flash producer and other interactants were identified by swimming to the point of the flash and observing, with the use of red filtered lights, all subsequent behaviors. Although this technique was successful for flashes produced close to the observer, it was sometimes impossible to arrive at the point of the flash before the interaction was over, and thus in some cases (28 out of 95, see Results) the cause of the flash was unknown. A series of fifteen 30-min focal observation periods was conducted from a distance of 3-4 m on isolated patch reefs. These reefs were at a depth of 1.5-5 m, and had 0. riisei populations occupying < 1 m2 with average densities of 60 ind. .0.25 m ‘. All medium to large ophiuroid flashes (see Results) were immediately investigated and subsequent behaviors by ophiuroids and interactants were observed. Behaviors from both observation methods were recorded on underwater slates and placed into three general categories. Avoidance behaviors included all those that resulted in a respondent moving away from the ophiuroids. Potentially predatory behaviors were those resulting in the respondent moving towards the ophiuroids. The absence of any behavioral changes comprised the no-response category. Previous observations and existing studies were used to provide relative assessments

BRITTLE-STAR LUMINESCENCE

of the feeding guild for the visually orienting interactions

IN CORAL REEFS

animals

that had luminescence-associated

with 0. riisei (Table I). Using the Kruskal-Wallis

individual

species within groupings

responses nonvisual

vs. no responses echinoderms.

161

rank analysis

treated

as replicates),

the proportion

was compared

for predators,

scavengers

(with the

of avoidance

or cleaners,

and

TABLE I Primary feeding mode and general movement patterns of animals involved in flash-mediated interactions with Ophiopsilu riisei during focal and haphazard observation periods.* Species/group

Primary feeding mode

Movement patterns

Octopus briareus

Predatora,”

Malacoctenus sp.

Predator’

Live in den with long range nocturnal forays”,b Territorial’

Portunus sebae Rhynchocinetes rigens Brachycarpus biunguiculatus

Prediatord Predator” Cleanerf/predatorj

Home-ranging/territorialJ Unknown TerritorialfJ

Small decapod crabs Small hermit crabs

Unknown Scavengersg*h Deposit-feedertip.” Cleaners’ Cleaner’

Unknown Site-specific’

(blenny)

Periclimenid shrimp Stenopus hispidus

Site-specific’ Site-specific’

* Letter superscripts refer to appropriate references for each group: a Wells (1978), b Ambrose & Nelson (l983), ‘Thresher (1980), d Williams (1982), “Manning (1961), rcorredor (1978), s Schembri (1982) h Kunze & Anderson (1979), i Limbaugh et al. (1961) j pers. obs.

RESULTS LABORATORY OBSERVATIONS

Brachycarpus biunguiculatus produced

more avoidance

behaviors

during interactions

with luminescent Ophiopsila riisei than with the two nonluminescent controls (Fig. 1). Conversely, in Stenopus hispidus, there were no significant differences in the production of avoidance behaviors between luminescent and nonluminescent ophiuroids (Fig. 1). Both species of shrimp showed greater numbers of predatory (or scavenging) behaviors towards immobile Ophiopsila than to active Ophiopsila and Ophioderma (Fig. 1). Luminescent Ophiopsila riisei elicited the lowest frequency of predatory behaviors in all but one case (Cheliped Grab/Hold in Stenopus hispidus). Neither shrimp showed significant differences in the production of the Stop/Stay behavior among the three ophiuroids. Finally, both shrimps showed significantly more No Responses towards immobile compared with active ophiuroids (Fig. 1).

162

M. S. GROBER

The behavioral responses of Panulims argus were similar to those of Brachycarpus biunguiculatus. More avoidance behaviors were elicted by luminescent than by non-

luminescent ophiuroids (Fig. 1). There were no significant differences in the production S tenopus hispidus

6

Brachycarpus

VARIABLE

biunguiculatus

PREDATORY

BEHAVIOR

AVODANCE

I

Ophioderma cinereum

0

Anesthetized

Ophiopsila

I

Luminescent

Ophiopsila

Panulirus argus

VARIABLE

PREDATORY

AVOIDANCE

BEHAVIOR

Fig. 1. Frequency histograms of behavioral responses oftwo shrimp and one lobster species to interactions with luminescent and nonluminescent ophiuroids. Each bar represents mean of that response from five 30-min trials. Error bars represent f 1 SE of mean. Nonluminescent preparations were Ophioderma cinereum and anesthetized Ophiopsila riisei. Normal 0. rikei was single luminescent preparation. Means for three ophiuroid preparations were compared for each behavior using a l-way ANOVA.

of Panulirus argus predatory behaviors between ophiuroid types. However, luminescent Ophiopsilariisei elicted the lowest frequency of predatory behaviors. Finally, luminescent ophiuroids elicited significantly fewer Stop/Stay and No Response behaviors compared with nonluminescent ophiuroids (Fig. 1). FIELD

OBSERVATIONS

The flashes produced by Ophiopsila riisei in the field can be broken down into minor and major flash groupings. Minor flashes are produced by current induced collisions of plankton and other particulates with ophiuroid arms, whereas major flashes were

BRITTLE-STAR

LUMINESCENCE

IN CORAL

REEFS

163

normally the result of an animal mechanically disturbing one or a few 0. riisei. The majority of these flashes (68%) was elicited by crustaceans, although a diverse group of animals, including moIIuscs, e~hinode~s, and fishes, was seen to cause flashes (Table II). Aggregations of 0. riisei produced an average of 3.16 -r_3.19 (F + SD) major TABLE II Animals

seen to elicit luminescent

Annelida Unidentified polychaete Arthropoda (crustaceans) Cirolana sp. Lysmata grabhami (Gordon) Perklimenes pedersoni (Chace) P. yucate~~ (Ives) Brachycarpus biunguiculatus (Lucas) Stenopus hispidus (Oliver) Rhynchocinetes rigens (Gordon) Unidentified penaeid shrimps Porcellana sayana (Leach) Portun~ sebae (Milne”Edwards) Small hermit crabs Small decapod crabs

flashes from OphiopsiZarikei in field. Mollusca Octopus briareus (Robson) Echinodermata Astropecten duplicatus (Gray) Ophiothti suensonii (Liitken) Ophjocuma echinata (Lamarck) Ophioderma ~bicMndum (~~tken) Echinometra sp. Diadema antfllarum (Phillipi) Vertebrata Apogon maculatus (Poey) Mulacoctenus sp. (small crevice-dwelling

blenny)

flashes .30 min - ’ when all 30 observation periods were considered. However, major flashes occurred in only 19 of the 30 periods, and the mean flash rate for these I9 periods was 4.99 + 2.59 flashes * 30 min- ’ * aggregation- ‘. In general, flash intensity was roughly correlated with the size of the animal that elicited a flash. Because of the overal low frequency of major flashes (95 flash events during 15 h of observations), data from the two different observation methods were combined for analysis. Behavior data were obtained from 67 of the 95 flash-associated interactions, There were only two instances of behaviors that resulted in the respondent moving towards the ophiuroids (potential predatory behaviors). One of these involved Brachycarpus biunguiculatus and resulted in no damage to Ophiopsila.The other involved a small decapod crab and in this case the crab did remove the terminal l-2 cm of one Ophj~p~j~aarm. Because of the small proportion of predatory behaviors, they were not used in the statistical analysis. The results of the analysis of the responses to luminescent flashes showed significant differences between predators, scavengers or cleaners, and nonvisually orienting echinoderms (Fig. 2, P c 0.01). Visually orienting predatory species consistently responded to luminescent flashes with avoidance responses, while nonvisual echinoderms never produced an observable response to Ophiapsila ritiei lum~es~e~ce (Fig. 2). The visually o~enti~g scavengers and cleaners were more variable in their responses with some species producing primarily avoidance behaviors, some characterized by a lack of responsiveness, and some showed a mixture of both behavior

164

categories

M. S. GROBER

(Fig. 2). Finally,

the responses

Stenopus hispidus to field flashes

with the results

experiments (Figs. 1,2), which suggests that the laboratory realistic indication of what occurs under natural conditions.

SCAVENGERS/ CLEANERS

PREDATORS

I

2

3

6

biunguiculutus and

of both Bruchycarpus

were consistent

15

2

1 I 312

results

of the laboratory probably

were a

NON-VISUAL ECHINODERMS 11

2

3

4

,/. ,.

Fig. 2. Percent of avoidance vs. no response behaviors produced in field by variety of coral reef animals in response to luminescent flashes from Ophiopsila riisei. Animals are grouped either in accordance with information in Table II or from personal observations, and these groupings were used for statistical analysis. Numbers above each bar represent sample sizes. Initials following common names of animals represent following: P.S., Portunus sebae; R.r., Rhynchocinetes rigens; O.b., Octopus briareus, M.sp., Malacoctenus sp.; B.b., Brachycarpus biunguiculatus; s.d., small decapod crabs; s.h., small hermit crabs; S.h., Stenopus hispidus; P.sp., Periclimenes sp.; A.d., Astropecten duplicatus; a.o., assorted ophiuroids; Esp, Echinometra sp.; D.a., Diadema antillarum.

DISCUSSION

The luminescent signals and their expression in Ophiopsilariisei are relatively simple, and are representative of the majority of benthic coastal emitters (Morin, 1983). The high degree of signal convergence in coastal emitters may be the result of a large-scale mimicry complex (Porter & Porter, 1979), and suggests that a diverse assemblage of luminescent emitters in coastal ecosystems may have similar effects on the behavior of nocturnally active animals. This report demonstrates that the relatively simple light signal produced by a representative coastal emitter can have a variety of effects on the behavior of visually orienting organisms. This variability in response characteristics can

BRITTLE-STAR

be assessed structure

in terms of possible

of nocturnal

In a previous study, to decrease predation triggered significantly potentially allowing the

LUMINESCENCE

IN CORAL REEFS

effects on the emitters

165

and the overall effects on the

communities. Grober (in press) showed that 0. riisei luminescence functions from three species of portunid crab predators. Luminescence higher frequencies of avoidance behaviors from these crabs, ophiuroids to spend more time suspension feeding. The evidence

reported here shows that 0. riisei luminescence also triggers avoidance from a variety of other nocturnally active predators and thereby provides ,a concomitant increase in overall feeding time, and a potential decrease in body damage caused by predators. Field studies support this conclusion. Populations of 0. riisei exhibit near-maximal use of available feeding time (Grober, in prep.), suggesting low levels of disturbances. However, some proportion of the population should be retracted into the reef because of disturbances caused by nonvisually orienting nocturnally active species, such as echinoderms. Luminescence is not an effective deterrent against these species (Fig. 2), and in most of these interactions 0. riisei retracts into the substratum. Finally, populations of 0. riisei experience very low levels of arm damage compared with a number of other Caribbean brittle-star species (Hendler, 1984; Aronson, 1986; Sides, 1987; Grober, in prep.). Luminescence has been shown to have a number of effects on predators (Basch, 1985; Grober, in press), herbivorous copepods (Esaias & Curl, 1972; White, 1979; Buskey et al., 1983), and various species of reef fauna (present study). However, there have been few empirical demonstrations of the behavioral mechanisms underlying these signals. Grober (in press) demonstrated that 0. riisei was very unpalatable to portunid crabs, showing that luminescence functions as an aposematic or warning signal to deter crab predators. Schantz (1971) suggested that dinoflagellate luminescence also functioned aposematically since many dinoflagellates produce toxins. 0. riisei luminescence could also function to startle crabs, thus allowing the ophiuroids time to withdraw into their crevices. Since no information is available on the palatability of 0. riisei to the predators considered in this report, it is unknown whether the mechanism of predator deterrence is aposematic, startle or any other of the proposed mechanisms. The differences in responses to light flashes between species may be related to the foraging behavior and the proximity of a given species to dense beds of 0. riisei. Predators showed more avoidance behaviors in response to luminescence in both the field and in the laboratory than did nonpredatory species (Figs. 1,2). Brachycarpus biunguiculatus appears to be an exception to this rule. Corredor (1978) states that this shrimp is a nocturnal fish cleaner and he never observed them feeding in any other way. For this reason, Bruchycapus was treated as a scavenger/cleaner (Fig. 2) in the statistical analyses. However, I never observed B. biunguiculatus cleaning a fish in the San Blas region and I saw them take prey on two occasions. Specifically, they preyed on an ostracod and a polychaete, and in both cases the prey were actively captured out of the water column. The differences in Bruchycaps feeding behavior between the present study and that of Corredor’s (1978) may be due to the use of bright white illumination

166

M. S. GROBER

in the previous study which could alter the natural behavior of the shrimp or fish. Alternatively, there may be habitat or range specialization of foraging behavior within this species resulting in the different behaviors found in these disparate populations. The majority of the visually orienting species observed in the field interactions is either site-specific (territorial) or home-ranging (Table I). This is true both for the predatory and primarily nonpredatory species. In either case, it is likely that these animals become familiar with their territories or home sites, thus allowing them to seek shelter by orienting to prominent landmarks (Rebach, 1983). Since dense beds of Ophiopsilariisei are very predictable in space and time, it seems probable that nocturnally active animals would be able to locate 0. riisei beds in and around their home site; this could have two important effects on community structure. First, since predators usually produce avoidance responses to luminescent flashes (Figs. 1,2; Grober, in press), they may learn to avoid the 0. riisei aggregations within their territories or home ranges. The significant decrease in Panulirus argus Stop and Stay behaviors during interactions with luminescent Ophiopsilariisei (Fig. 1) also suggest that some nocturnal predators are very sensitive to luminescence and avoid close associations with 0. riisei aggregations. This avoidance would result in an overall lower abundance of predators in close proximity to groups of luminescent ophiuroids, providing a refuge for organisms that could fall prey to these predators. Panulirus argus is known to prey on small hermit crabs (Kanciruk, 1980), and some portunids eat hermit crabs (Williams, 1982). The family Portunidae has been characterized as generalist predators whose diet is largely dependent upon local availability of prey species (Williams, 1982), and it may well be that the three common species of portunids in the San Blas prey on hermit crabs. The refugium hypothesis could account for the large aggregations of hermit crabs found in and around 0. riisei beds (pers. obs.). In addition, Stenopus hispidus and the periclimenid shrimps are also found close to or even on top of Ophiopsila riisei in the field. The lack of responsiveness to contact-induced luminescent flashes in these small crustaceans (Figs. 1,2) makes sense in light of the fact that they are in very close proximity to the ophiuroids and therefore may habituate to the flashes that they trigger. Similar use of refugia has been shown in studies of diurnal communities, in which a number of small crustaceans take refuge around or on a variety of protective echinoderms and cnidarians (Limbaugh et al., 1961; Bruce, 1975 ; Corredor, 1978). Secondly, the small crustaceans associated with 0. riisei may use the ophiuroids as a “luminous fence” that provides a warning of impending danger. When a predator moves into an 0. riisei bed, it usually produces a series of bright flashes, and small “attendant” crustaceans may use this flash as an early warning to seek shelter. Thus, these attendant crustaceans would ignore self-elicited flashes (these are usually limited and at very close proximity) and may respond vigorously to larger and more distant flashes that are produced by potential predators. In summary, luminescence can deter predators or intruders (non-Ophiopsila predators) from preying on or damaging 0. riisei. In addition, the dense aggregations of these

BRI?TLE-STAR

LUMINESCENCE

IN CORAL REEFS

167

ophiuroids and the differential responses of nocturnally active reef fauna to ophiuroid flashes may affect the distribution of both predator and prey organisms in nocturnal, tropical reef environments, and this may have important implications in terms of the structure of these communities.

ACKNOWLEDGMENTS

I am indebted to J. Morin, K. Niessen, N. Sturm, A. Huvard, M. Shulman, J. Smith, C. Tsuchida, and M. Kowalczyk. Special thanks to H. Lessios and D. R. Robertson of the Smithsonian Tropical Research Institute, the Kuna People of the Comarca de San Blas, and the Republic of Panama for the use of the field station in the San Blas Islands, Panama. This research was supported by a Smithsonian Tropical Research Institute Short-Term Fellowship, A Sigma-Xi Grant-in-Aid of Research, and the University of California at Los Angeles Patent Fund. REFERENCES

AMBROSE,R.F. & B.V. NELSON, 1983. Predation by Octopus vulgaris in the Mediterranean. P. S. Z. N. I. Mar. Ecol., Vol. 4,

pp. 251-261.

ARONSON,R. B., 1986. Predation of ophiuroids at Carrie Bow Cay. In, Caribbean coral reef ecosystems, edited by K. Riitzler, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia, p. 46. BASCH, L.V., 1985. Ecology, behavior, and functions of bioluminescence in the subtidal sand-dwelling brittle-star, Ophiopsila cal@rnica (Echinodermata : Ophiuroidea : Ophiocomidae). M.Sc. thesis, University of California at Los Angeles, Los Angeles, California. BRUCE,A.J., 1975. Coral reef shrimps and their colour patterns. Endeavour, Vol. 34, pp. 23-27. BUSKEY,E. J., L. MILLS & E. SWIFT, 1983. The effects of dinoflagellate luminescence on the swimming behavior of a marine copepod. Limnol. Oceanogr., Vol. 28, pp. 575-579. CORREDOR,L., 1978. Notes on the behavior and ecology of the new fish cleaner shrimp Brachycarpus biunguiculatus (Lucas) (Decapoda Natantia, Palaemonidae). Crustaceana, Vol. 35, pp. 35-40. DAHL, A. L., I. G. MAC~NTYRE & A. ANTONIUS,1974. A comparative survey of coral reef research sites. Atoll Res. Bull., Vol. 112, pp. 37-122. ESAIAS, W. E. & H. C. CURL, 1972. Effect of dinoflagellate bioluminescence on copepod ingestion rates. Limnol. Oceanogr., Vol. 17, pp. 901-906. GOLDSMITH,T. H. & H. R. FERNANDEZ,1968. Comparative studies of crustacean spectral sensitivity. Z. V.I. Phrriol., Vol. 60, pp. 156-175. GROBECR, M. S., in press. Brittle-star bioluminescence functions as an aposematic signal to deter crustacean predators. Anim. Behav., Vol. 36, pp. 493-501. HENDI.ER,G., 1984. The association of Ophiothrix lineata with Callyspongia vaginalis: a brittlestar-sponge cleaning symbiosis? P. S. Z. N. I. Mar. Ecol., Vol. 5, pp. 9-27. HERRING, P. J., 1978. Editor. Bioluminescence in action. Academic Press, New York, New York, 570 pp. KANCIRUK, P., 1980. Ecology of juvenile and adult Palinuridae (spiny lobsters). In, The biology and management of lobsters, Vol. 2, edited by J. S. Cobb & B.F. Phillips, Academic Press, New York, New York, pp. 59-96. KUNZE:,J. & D.T. ANDERSON,1979. Functional morphology of the mouthparts and gastric mill in the hermit crabs Clibinarius taeniatus, Clibinarius virescens, Paguristes squamosus, and Dardanus setifer (Anomura : Paguridae). Aust. J. Mar. Freshwater Res., Vol. 30, pp. 683-722. LIMBAUGH,C., H. PEDERSON& F.A. CHACE,JR., 1961. Shrimps that clean fishes. Bull. Mar. Sci. Gulf Car&b., Vol. 11, pp. 237-257.

168

M. S. GROBER

MANNING,R. B., 1961.Notes on the caridean sh~p,Rhynchocinesesr Gordon (Crustacea, Decapoda), in the western Atlantic. Not. Nat. Aead. Nat. Sci. Philadelphia, No. 348. MORIN,J. G., 1983. Coastal bioluminescence: patterns and functions. Bull. Mar. Sci., Vol. 33, pp. 787-817. PORTER, K. G. & J. W. PORTER, 1979. Bioluminescence in marine plankton: a coevolved antipredator system. Am. Nat., Vol. 114, pp. 458-461. REBACH,S., 1983. Orientation and migration in crustacea. In, Studies in adaption: the behavior of higher Crustucea, edited by S. Rebach &. D.W. Dunham, John Wiley & Sons, New York, New York, pp. 217-264. SCHANTZ, E.J., 1971. The dinoflagellate poisons. In, Microbial toxins, Vol. 7, edited by S. Kadis et al., Academic Press, New York, New York, pp. 3-25. SCHEMBRI,P. J., 1982. Feeding behaviour oftifteen species of hermit crabs (Crustacea : Decapoda : Anomura) from the Otago region, southeastern New Zealand. J. Nat. His., Vol. 16, pp. 859-878. SIDES, E. M., 1987. An experimental study of the use of arm regeneration in estimating rates of sublethal injury on brittle-stars. J. Exp. Mar. Biot. Ecol., Vol. 106, pp. I-16. SOKAL, R.R. & F. J. ROHLF, 1981. Biometry. W.H. Freeman & Co., San Francisco, California, second edition, 859 pp. THRESHER,R.E., 1980. Reeffish. Palmetto Publishing Co., Saint Petersburg, Florida, 171 pp. WELIS, M.J., 1978. Octopus. Chapman & Hall, London, 417 pp. WHITE, H.H., 1979. Effects of dinoflagellate bioluminescence on the ingestion rates of herbivorous zooplankton. J. Exp. Mar. Biol. Ecol., Vol. 36, pp. 217-224. WILLIAMS,M., 1982. Natural food and feeding in the commercial sand crab Portunuspelagicus Linnaeus, 1776 (Crustacea: Decapoda: Portunidae) in Moreton Bay, Queensland. J. Exp. Mar. Biol. Ecol., Vol. 59, pp. 165-176.