BULLETIN OF MARINE SCIENCE, 36(3): 701-715, 1985 CORAL REEF PAPER

NICHE SEPARATION IN THREE SPECIES OF OPHIOCOMA (ECHINODERMATA: OPHIUROIDEA) IN JAMAICA, WEST INDIES

E. M. Sides and J, D. Woodley

ABSTRACT The brittle-stars Ophiocoma wendtii, O. echinata and O. pumila occur under rubble and in crevices in coral heads shoreward of the reef crest. To determine if the three species differed in use of resources, the sizes of crevice openings used were measured, feeding methods and behavior were observed, and stomach contents examined. The three species were found to use crevices of different sizes, which in part may be a function of their difference in size: but size alone is unlikely to be the reason for the use of such large crevices by O. wendtii. All three species were observed to suspension- and deposit-feed, but differed in the degree to which they exposed themselves, and in the feeding areas used in relation to their crevices. The analysis of stomach contents revealed a broad overlap in diet and particle size, but those of O. wendtii had the highest amount of very fine flocculent material, and O. pumila. the smallest species, contained the largest particles. Thus these three closely related species, which appear to co-exist, when studied in detail show striking and subtle differences in several aspects of their life habits. The availability of suitable sized crevices is likely to be a major determinant of the distribution of the species.

" ... about these cays we waded .... and turned over stones till the sea breeze drove us home wondering at the strange sights we had glimpsed, such as the gorgon-like writhings of batches of serpent-stars dispersing from under a stone." E. A. Andrews (1946), on the Johns Hopkins University expedition to Jamaica, 1891. Coral reef communities are well known for their diversity; even the backreef, periodically exposed to salinity and sediment stresses, is inhabited by numerous species. Brittle-stars are abundant backreef organisms, but are usually cryptic during the day. In Jamaica, nine species (Ophiocoma wendtii, O. echinata, O. pumila. Ophioderma appressum. O. cinereum, Ophiomyxa jlaccida. Ophiofepis impressa, Ophionereis reticulata, and Ophiothrix angulata) are commonly found shoreward of the reef crest in shallow water, under slabs of coral rubble and in crevices within coral heads. Another five or six species occur locally or rarely in the same habitat (Sides, 1981). To see many individuals of several species crawling away from beneath a single lifted slab prompts the questions: how do these animals co-exist within so small a space? Do their niches differ? Two of these genera are represented by more than one species, and biological interactions are likely to be, or to have been, greatest between closely related species (Darwin, 1859). Therefore, one of these groups, the three species of Ophiocoma, was selected for the present study. The confusion between observed patterns of distribution and the interpre- tation of biological roles in determining these patterns has caused much current debate (Connell, 1975; Schoener, 1983). Thus, this paper will simply document patterns of resource use to determine if there are differences between the species in their use of habitats, feeding methods and food, similar to that found for birds (Lack, 1971; MacArthur, 1958) and for lizards (Schoener, 1968) and reviewed by Schoener (1974) and Hutchinson (1978). Future papers will examine the roles of habitat selection, competition and predation in these and other sympatric species in determining their observed distributions (Sides, in prep.). The Ophiocomidae are the most abundant and diverse family in tropical shallow

701 702 BULLETIN OF MARINE SCIENCE. VOL. 36. NO.3. 1985 waters (Clark, 1976). At Enewetak seven species and at Aldabra nine species have been shown to exhibit habitat separation (Chartock, 1972; Sloan, 1982), which is consistent with Kohn's (1971) hypothesis that "co-occurring detritus feeders are more likely to specialize in microhabitat than food type." It has been suggested that the distribution of these other ophiuroids is affected by differences in their size (Chartock, 1972; Sloan, 1982), the availability of suitable crevices (Sloan et aI., 1979; Sloan, 1982), competition between species (Sloan et aI., 1979; Lewis and Bray, 1983) and physical factors (Kissling and Taylor, 1977), but there are no quantitative data to support these ideas. In the Caribbean, only three species of Ophiocoma are found commonly in shallow water and they show a very broad overlap in distribution (Kissling and Taylor, 1977; Lewis and Bray, 1983). Ophiocoma wendt ii, O. echinata and O. pumila have been recorded in Jamaica as commonly occurring under the same slabs of rubble (Grave, 1898), but Clark (1933) noted that O. pumila was more frequently found in the "nooks and crannies of coral heads." A similar observation was made by Fontaine (1953) and he also recorded O. pumila occurring in coralline algae. Kissling and Taylor (1977) also found considerable overlap between these species in Horida; however, in Barbados (Lewis and Bray, 1983) O. wendtii and O. pumila were not common under rubble where O. echinata was most abundant. All three species were common in the "reef' areas. Preliminary observations, i.e., turning over many coral slabs to see what brittle- stars were under them, gave the impression that the relative abundance of the three Ophiocoma species might be related to the size of the concealed cavity. This is hard to measure; instead we measured the openings of the crevices occupied by individuals of the different species. The three species also differ in size and shape and so a number of morphological measurements were made to quantify these differences since size alone might be an important factor (Wilson, 1975; Hutchinson, 1978) determining the size of crevice used as well as influencing food, feeding methods and the likelihood of being preyed upon. In addition, feeding methods were observed in the field and in aquaria, and stomach contents were examined. Studies have also been made ofthe histochemistry of their spines and tube-feet (Sides, 1976), of predation on these and other brittle-stars (Sides, 1976; 1981) and of competition between them (Sides, 1981; and in prep.).

STUDY AREA

The study area was the western lagoon in Discovery Bay, Jamaica, which has been described by Woodley and Robinson (1977). The study sites were opposite the Marine Laboratory and located within the Transitional Zone of Hammond (1980) which consists mainly of large scattered heads of Siderastrea siderea interspersed with turtle grass (Thalassia testudinum), dead coral rubble and sand. Many of the coral heads have large dead areas, particularly in the center, which are covered with a fine algal turf. The crevices in these coral heads and under slabs, mostly of Acropora palmata rubble, are inhabited by numerous ophiuroids. The depth of the water is approximately 1.5 m.

METHODS

Morphology. - Fifty, randomly collected, individuals of each species were collected and narcotized in 7.5% MgCI26H20 diluted 1:1 with sea water (Pantin, 1969). The disc diameters and maximum arm lengths were measured with a simple pair of dividers and ruler. The maximum diameter of the arm with the spines laid against the arm (approximately 1.0 em from the disc) and, also in this region, the distance from the tip of the uppermost spine to the tip of the lowermost spine (the spine span) were measured with a pair of calipers. General Field Observations. - The majority of observations were made using SCUBA and were re- corded on plastic slates. At night, flashlights with red filters were used because the ophiuroids did not retract into their crevices as rapidly when illuminated with a red light (Crump, 1965). SIDES AND WOODLEY: NICHE SEPARATION IN THREE BRITTLE-STARS 703

Table 1. A summary of the morphological measurements made on the three species of Ophiocoma

XArm length! ~ disc Maximum Disc diameter Disc height Arm length Arm height diameter spine span Species x ± s X ± S x ± s X ± S ratio x ± s N O. wendtii 2.17 ± 0.39 0.45 ± 0.39 11.5 ± 2.6 0.34 ± 0.06 5.3 1.33 ± 0.22 50 O. echinata 1.74 ± 0.38 0.37 ± 0.08 8.3 ± 2.1 0.30 ± 0.06 4.8 0.77 ± 0.14 50 O. pumila 1.18 ± 0.22 0.24 ± 0.05 8.4 ± 2.3 0.17 ± 0.03 7.1 0.38 ± 0.22 50

Habitals.- The micro-habitats occupied by the three species were determined by day and night ob- servations. To quantify the differences between the crevices occupied by each species, the length and height of each crevice opening were measured. Fifty crevice openings were measured for each species. General Behavior. -Observations were made on the diel activity cycles of the three species. A single complex coral head of Siderastrea siderea, 3.0 by 1.5 m, was chosen. The exposed length of every arm of each individual of Ophiocoma echinala and O. pumila was measured, and the position of O. wendtii with respect to its crevice was noted over approximately a 1- to 2-h period at dusk and dawn and 0.5 to 2 h at midnight. The time of each observation was noted. Initial observations were made in 1973 (Sides, 1976), but the data presented in this paper were collected on a total of 7 nights for O. wendtii, 5 nights for O. echinata and 2 nights for O. pumila in 1977 and 1978, and represents in total a minimum of 48 h of underwater observations. The data are represented as (1) the degree of exposure and (2) the median total arm length extended, with time. Exposure was divided into the following eight categories: 0, 1, 2, 3, 4, 5 arms exposed, disc and some arms exposed, and fully exposed. For each period of continuous observation, the number of individuals in each category was plotted. To combine the data taken on different nights and at different times of the year, readings were taken from each graph ofthe number of individuals in each category at sunset, sunrise and midnight (the midpoint between sunset and sunrise) and lO-min intervals from these points. The number of individuals in each category at each time interval was then plotted as the percentage of the total number of observations made at that time. For the second measure of exposure, the tota1length of the arm exposed by each individual was plotted with time for each night. To amalgamate the data the length of the arm exposed by each individual was read off the graph at sunrise, midnight, sunset, and at 10-min intervals before and after these points. The median and 50 percentile about the median of arm length extended for all individuals observed at each reading were then plotted. Feeding Methods.-Feeding methods were observed while monitoring exposure, and additional ob- servations were made on other occasions at different times of the day and night in a number of habitats. More detailed observations ofthe activities of tube-feet were made on animals in glass aquaria in the laboratory. The animals were fed on newly hatched brine shrimp or pieces of macerated marine snail tissue. Slomach Contents. - Ten specimens of each species were collected between midnight and dawn and quickly preserved. As each individual was captured it was brought to the surface with the mouth held shut between the collector's fore-finger and thumb to prevent the stomach contents from being re- gurgitated. The arms were cut off the disc, which was then put into a 28-ml plastic pot of strong formaldehyde solution. The next day the formalin in each pot was changed and later it was replaced with 70% alcohol. To remove the stomach contents the wall of the disc was cut off along with the stomach lining; the contents were washed or picked out. The samples were examined under a binocular microscope with an eye-piece scale. Ash weight/dry weight ratios were determined for the gut contents of 3 O. wendtii and O. echinata and 4 O. pumi/a.

RESULTS Morphology.-Morphological measurements are summarised in Table 1, and show the similarity in size between O. wendtii and O. echinata. However O. wendtii had slightly longer arms and a greater spine span (Fig. 1). The fourth and upper- most spine in both species generally occurs on opposite sides of adjacent segments (Devaney, 1970) and was usually held erect (Fig. 1). On O. echinata this spine is swollen at the base (Fig. 1) and on O. wendtii it is club-shaped. Ophiocoma pumila had a much smaller disc diameter but a greater arm length to disc diameter ratio, 704 BULLETIN OF MARINE SCIENCE. VOL. 36, NO.3, 1985

o echinola o pllmilo

Figure I. Diagrammatic cross sections of the arms of Ophiocoma wendtii, O. echinata and O. pumila in the proximal region. as the arms were as long as those of O. echinata (Table I). In cross section the arms are more flattened than in the other species with the uppermost spine being held out laterally rather than erect. The species were readily distinguished on the basis of color. During the day adults of O. wendtii appeared to be a uniform reddish-black with red tube-feet (the juveniles are bright red), but close examination revealed that the arms were banded with black. These bands became more pronounced at night (Fig. 2); the rest of the arm surface becoming a pale greyish-brown. Ophiocoma echinata adults were generally dark brown with the distal parts of the arms banded pale yellow and dark brown. However, specimens were also found with a variety of cream and yellow markings on the disc. In contrast O. pumila was pale brown, with arm tips green, which is the color of the juveniles. Habitats. - That the three species use crevices with different sized openings was

Figure 2. Ophiocoma wendtii fully exposed at night. Note the distinct banding of the arms. Ophio- derma cinereum in the background. SIDES AND WOODLEY: NICHE SEPARATION IN THREE BRITTLE-STARS 705

>15·0 I 14·1-15-0

13·1-14·0 SCALE I-----< = 20% ::;; 12·1-13·0 8 11-1-12·0 zC> I I > 10·0 Z 10·1-1J·O ~ w 8 0- 9'1-10'0 0 9·1-10·0 C> z 8'1-9·0 w 8,1-9,0 z u w >: 0- 7·) -8·0 w 7-1-8·0 0 a:: u w 6'1-70 6·1-7·0 u LL 0 , :> w 5·1-6·0 5'1-6·0 a:: I u I- 4'1-5{) I I 4·1-5·0 C> LL z • 0 3'1-4·0 w 3·1-4·0 ...J • I- 2·1-3-0 I I 2·1-3·0 Z C> • w H -2·0 1·1-2{) I • 0-1·0 0-1·0 , A +B ...•..C A B •C Figure 3. Bar diagram showing the distribution of height and length of the openings of 50 crevices occupied by A, Ophiocoma wendtii; B, O. echinata; C, O. pumila. substantiated by quantitative observations at night. The measured heights of the openings are given in Figure 3 and show a clear and highly significant separation of the three species (Kruskal- Wallis one-way analysis of variance, H = 122.347, df = 2, P < 0.00 1; Siegel, 1956). Although there is some overlap by O. echinata with O. wendtii and 0. pumila a nonparametric multiple comparison by stepwise test procedure (STP; Sokal and Rohlf, 1969) showed that the three species differed significantly from each other (P < 0.001). The median height of crevice opening used by O. wendt ii, O. echinata and O. pumila were 6.0, 2.0 and 0.5 cm respec- tively. Although the lengths of crevices used were also significantly different (Krus- kal-Wallis, H = 69.706, df= 2, P < 0.001) and the three species were significantly different from each other (STP, P < 0.001) the separation is not as clear (Fig. 3). The median crevice length for O. wendtii was 12.0 cm and 3.0 cm for O. echinata and O. pumila. The longest crevices measured for O. pumila may have been occupied by two adjacent individuals. General Behavioral Patterns. - All three species were generally cryptic in their behavior but emerged, partially or wholly, through their crevice openings at dusk, retracting at dawn (Fig. 4). Individuals of O. wendtii commonly came out into the open each night; O. echinata could be almost completely exposed but was rarely seen away from a crevice, although there is evidence of migration (Sides, 1981), while O. pumila exposed only its arms and was never seen in the open (Fig. 4). The arms of the three species were extended at night and used for feeding (see below). O. wendtii.-During the day, O. wendtii remained hidden in large dark crevices under and within coral heads and under slabs of coral rubble. They were generally 706 BULLETIN OF MARINE SCIENCE, YOLo 36, NO.3, 1985

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TIME OF NIGHT (MIN)

Figure 4. Bar diagram showing the exposure of individuals of A, Ophiocoma wendtii, B, O. echinata and C, O. pumila at lO-min intervals before (-) and after (+) sunset, middle ofthe night, and sunrise (dotted lines). Data obtained from up to 15 O. wendtii on 7 nights, up to 10 O. echinata on 5 nights and up to 7 O. pumila on 2 nights. SIDES AND WOODLEY: NICHE SEPARATION IN THREE BRITTLE-STARS 707

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TIME OF NIGHT (MIN)

Figure 5. Graphs showing the median total arm length exposed by individuals of Ophiocoma echinata and O. pumila at IO-min intervals before (-) and after (+) sunset, middle of the night, and sunrise (dotted lines). The vertical bars represent the 50 percentile about the median; the numbers above the bars are the total number of observations and those below the bars are the number of nights of observation. clinging to the upper surface of the crevice or underside of the slab with the arms retracted. At this time they were very dark with a reddish tinge. Late in the afternoon they became a pale grey-brown with black bands around the arms. As dusk approached they slowly stretched out their arms so that 2-3 of the arm tips extended beyond the edge of the crevice. The arm tips moved about as if searching the substratum. Gradually the animals moved down from under the roof of the crevice to the floor, and the arms were further extended from the crevices. By this time, approximately 30 min after the first signs of activity, the arm tips were held off the surface and the animals could have fully emerged from their crevices (Fig. 2). The majority of individuals were usually fully exposed for at least some part of the night (Fig. 4). The length of arm exposed by O. wendtii was not measured because its crevices were often wide and their limits ill-defined. Extensive obser- vations on the same individuals over several months showed that individuals differed in the amount that they exposed themselves and that they had quite set behavioral patterns. Such consistent individual differences in behavior have also been observed for basket stars (Hendler, 1982). Some individuals fed in the immediate vicinity of the crevice entrance or on the rocky surfaces of an adjacent coral head; others regularly moved away from the crevice into nearby turtle grass (Thalassia testudinum). In each situation individuals showed consistent differ- 708 BULLETIN OF MARINE SCIENCE, VOL. 36, NO.3, 1985 ences in feeding behavior. These variations in habit may have been partly a function of the location and immediate surroundings of the occupied crevice. The animals fed throughout the night; at dawn each individual generally retreated into the hole from which it had emerged. There is evidence that individuals used the same refuge for several months (Sides, unpubl.). O. echinata.-During the day, some arm tips of O. echinata were just visible, emergent through their crevice openings. At dusk, they and others were quite rapidly protracted. Usually each individual extended three or four arms, though all five could be extended. Not infrequently, the disc was seen partially exposed at the entrance to the crevice. Occasionally O. echinata fully exposed itself (Fig. 4), but often had one arm tip in or at the crevice entrance. Plotting the total length of arm extended per individual showed that the median length exposed by in- dividuals of O. echinata increased rapidly from 10 min before sunset to 40 min after sunset (Fig. 5). The length of arm extended varied through the night and diminished almost to zero at dawn. The fluctuations may be due to the fact that each arm is not always employed in the feeding method all the time but moves around searching or may be retracted at times and another arm extended. When O. echinata occupied a crevice over a sandy substratum, the opening sometimes became blocked with sand by wave action or by the activities of another animal. To enable free movement of the arms, the gap had to be widened; an activity that took place at any time of night, but was most frequently observed at dusk, when the arms were newly emerged. The tube-feet were used to move sand grains with a kicking motion and by transferring grains from foot to foot. The sand was moved towards the tip of the arm where it was deposited until the arm became raised on a ridge of sand. When this occurred, the arm moved to one side and the process continued until the entrance was cleared. Alternatively, if the opening had been greatly enlarged, the reverse occurred; the arms were well extended and sand grains were carried towards the entrance until the gap was narrowed. Thus when over a sandy substratum, O. echinata may be able to maintain its crevice opening at a suitable height. No doubt the process is also used to clear out sediment from within the crevice. O. pumila.-Individuals of O. pumila were generally invisible by day. At dusk, their slender arms emerged from tiny crevice openings and sought food on the adjacent surfaces or in the water column. Although all five arms were sometimes exposed, generally only two to four arms were seen (Fig. 4). The disc was never visible and the animals did not come out into the open (Fig. 4). The graph of median total arm length extended per individual with time shows a very similar pattern to that of O. echinata, but the length of arm extended was less (Fig. 5). The majority of individuals on which detailed observations were made in the field were in crevices in a coral head and not on sand floored crevices, though these commonly occur. However, when occupying such a crevice in the laboratory O. pumila was observed to alter its crevice dimensions, much as described for O. echinata above.

Feeding Behavior General Observations. -All three species were observed to deposit- and suspen- sion-feed. When individuals were suspension-feeding no orientation of the arms to water currents was observed, and no mucus net was seen, but the spines and tube-feet were used as sticky rods for trapping material. The tube-feet of deposit- feeding arms were seen to pick and pluck material from the substrate and were SIDES AND WOODLEY: NICHE SEPARATION IN THREE BRITTLE-STARS 709

Figure 6. Spine wiping by a tube-foot of Ophiocorna wendtii: A, three spines being cleaned at once; B, a single spine being cleaned. helped by the arms. Bolus formation and transport along the arms was the same in O. wendtii and O. echinata but was not observed in O. pumila.

Suspension -feeding Ophiocoma wendtii.- This species was seen to suspension-feed by holding its arms well up into the water column with the tube-feet extended ventro-Iaterally. Usually only one or two arms were involved and not more than three. There did not seem to be any orientation of the arms to water movement. Mucus was seen adhering to the spines but did not form a mucus net between them; rather it made them into sticky rods. The tube-feet periodically reached up, touching the dorsal arm-plates, and wiped the spines, particularly the lowermost ones. Only the base of the uppermost spine was wiped, although detritus was seen adhering to the rest of this spine. It was generally the spines of the arm segment proximal to each tube-foot that were wiped, and they were cleaned with the proximal side of the foot, the side of the tube-foot at the base of which lie the tentacle scales. The wiping was done by curling the foot around the spines near the base and rubbing along them to their tips. In doing this, the spines were bent down (Fig. 6). The spines were cleaned both singly and together. The particles were compacted with mucus, by the rubbing and twisting of the feet, to form a bolus which was passed along the arm to the mouth. The bolus was held between the mid-portions of the two tube-feet of the same segment. To move the bolus towards the mouth, the tube-feet first bent proximally at their bases, and then unrolled, which rotated the bolus which was held inside the curve of the feet. The proximal pair offeet which were already reaching forwards waiting to take the bolus swung in towards the center of the arm, rubbed against the feet and bolus, and clasped the bolus between them. As these feet bent proximally at their bases the tips of the first pair, now nearly straight, were flattened against the arm plates. They immediately started to contract, i.e., shorten, so they could extract themselves from under the pair which held the bolus (Fig. 7). This movement of the bolus appears to be very similar to that described for Ophiothrixfragilis (Warner and Woodley, 1975). The number of tube-feet involved depended on the size of the bolus. When the bolus 710 BULLETIN OF MARINE SCIENCE, VOL. 36, NO.3. 1985

Figure 7. Positions of the tube-feet passing a food bolus down the arm ofOphiocoma wendtii. Spines and lateral arm-plates omitted; the edge of the arm shown (unrealistically) by a straight line. was small only two pairs were involved at anyone time, as described above. Larger boli often had two to three pairs of tube-feet clasping them simultaneously. The most active part of the arm appeared to be the distal 2-3 cm and in the laboratory the tube-feet in this region were seen to be capable of catching freshly hatched brine shrimp that had been fed to them. As the shrimp were being packed into a bolus, the spines were periodically wiped and the bolus was passed up and down the tip ofthe arm several times as if being coated with mucus before being passed along the arm to the mouth. When a current was created in the tank, the suspension-feeding posture became more pronounced but this was not maintained for long, nor was there any orientation of the arms with respect to the current. No planktonic organisms were seen to be caught by the tube-feet in the field; however O. wendtii is light sensitive and only short observations could be made before they were disturbed. Ophiocoma echinata. - When suspension-feeding O. echinata could be seen to adopt a posture similar to that described for Ophiocomina nigra (Fontaine, 1965). That is to say, the arms were curved upwards (abo rally) and the tube-feet, extended to about twice the length of the second arm-spines, were held out ventro-Iaterally. The arms were moved from side to side through a small angle. At other times, the arms were held horizontally above the substrate with just the arm tips curved up. There did not seem to be any orientation of the arms to water movements. As in O. wendtii the spines appeared to be coated with mucus and acted as sticky rods; no mucus net was observed. The spines were wiped by the tube-feet in a similar manner to those of O. wendtii (Fig. 6), and formation and transport of boli occurred the same way. Only the base of the uppermost (aboral) spine was wiped by the tube-foot. Laboratory observations showed that the arm tips were very active and the tube-feet were capable of catching young brine shrimp. Ophiocoma pumila. - This cryptic species, when suspension-feeding, extended only the distal third or less of each arm vertically into the water column from its very narrow crevices. The tube-feet were held out ventra-laterally and extended a little beyond the third spine. Particles were seen to adhere to them and to the spines. The arms in this region were extremely fine and very hard to observe SIDES AND WOODLEY: NICHE SEPARATION IN THREE BRITTLE-STARS 711 because ofthe photo-sensitivity of the animals. No mucus net was observed nor were the details of spine wiping and bolus formation. Laboratory observations yielded no more information as the animals retracted very rapidly even if dimly illuminated.

Deposit- feeding Ophiocoma wendtii.-Individuals of O. wendtii were active feeders, using their tube-feet to pick and pluck material from rock surfaces, Thalassia blades or to gather silty material that had collected between live coral heads or in the depres- sions on the surface of the corals. Much of the material was ofa flocculent nature and appeared to be already bound with mucus, in which case it was passed directly along the arm, as described above, being formed into a bolus as it was transported. The removal of attached material by the tube-feet was aided by the arm suddenly arching at the point where the tube-feet were pulling and also contracting very slightly. Depending on the nature of the material collected it was either formed into a bolus before moving along the arm, or passed directly along the arm being compacted as it was carried on. On occasion several boli could be seen moving along an arm at the same time. As described above, individuals followed different behavioral patterns. Those that moved into adjacent stands of Thalassia climbed up on the plants to feed on material adhering to the leaves. They were never seen to use this elevated perch as a base for suspension-feeding. O. wendtii that were collected from beneath coral rubble during the day were frequently clinging to the underside of the slabs and were seen to have one or more boli on several arms suggesting that they feed within the crevice, and that feeding is not entirely a nocturnal activity. Ophiocoma echinata.-As explained above, O. echinata individuals, unlike O. wendtii, were commonly seen to transport sand grains into and out of their crevices. As their stomach contents consisted largely of sand, the inward transport of grains, whatever its architectural function, may be a form of deposit-feeding. In aquaria, when an algal bloom occurred on the substratum around an occupied crevice, a cleared semi-circle was often seen in front ofit. Some individuals did not extend their arms as frequently beyond the edge of the crevice as others, but some arms could be seen stretched out within the crevice, suggesting that some feeding may take place within it. This probably depends on the structure of the crevice. All substrata within reach from the crevice were liable to be fed upon, including those above the crevice opening; in those cases, the arms were twisted so that the extended tube-feet could be applied to the surface. Sometimes, blades of Thalassia occurred near enough to the crevice opening for the arms to be stretched out to feed from their surfaces. Occasionally, an O. echinata was seen to leave its crevice and sit beneath the grass blades with arms stretched up to feed on material adhering to them. It was never observed to climb up on to the blades as did O. wendtii. O. echinata employed two methods for the collection of particles from the sub- stratum. First, picking up particles by simple adhesion to the tube-feet, which would periodically form a bolus by the method described above. Secondly, par- ticularly when feeding on a rock surface colonised by fine algal turf, material would be forcibly plucked from the surface, in a manner similar to that described for O. wendtii.

Ophiocoma pumila.-When deposit-feeding O. pumila extended considerably more of each arm than when it was suspension-feeding, up to three quarters of 712 BULLETIN OF MARINE SCIENCE, VOL. 36, NO.3, 1985 the arm length. Similar to O. wendtii and O. echinata the arms were frequently employed in plucking material from the substratum. However the removal of material by the tube-feet was aided not by the arching of the arm at the point of pulling but by the sudden lateral contraction into a zigzag thereby shortening the arm. The transport of sand grains to and from the crevice, similar to that observed for O. echinata, has been observed in the field and in the laboratory (Sides, 1981) and may be a form of deposit-feeding.

Stomach Contents. - The stomach contents of all three species included recog- nizable pieces of plant material and calcareous particles, often bound together by mucoid material. Ash weight to dry weight ratios indicated that the contents were 70-90% organic material. In O. wendtii the bulk of the material was rather fine sand/silt «0.1 mm), organically bound; no calcareous particles larger that 0.3 mm were present. The majority of stomachs contained pieces of Thalassia and only a few had pieces of fleshy algae. In O. echinata fine to medium sand pre- dominated, with more particles in the 0.1-0.3 mm range (often clumped) and some larger ones. All the stomachs contained pieces of fleshy algae; only one had pieces of Thalassia. In O. pumila calcareous particles of a wide range in size (up to several mm), and large organic particles were present: every stomach contained pieces of fleshy algae.

DISCUSSION Despite the broad overlap in the distribution of the three Ophiocoma species among reef habitats, it is clear that there is microhabitat separation based on the occupation of differently sized crevices, a situation similar to that observed in birds (Lack, 1971; MacArthur, 1958) and lizards (Schoener, 1968; 1974). That alone could achieve niche separation, but in addition there are differences in feeding behavior. In particular O. wendtii leaves its crevice to forage at night, while the others do not. O. pumila had relatively longer arms than O. echinata and yet extended less when feeding. Thus the areas foraged around the crevices by the three species were different. The different sizes of the crevices occupied by the three species may partly be a reflection of their different body sizes. It is reasonable to suppose that, for protection from predation, each individual would choose to lie behind the smallest opening through which it could conveniently feed. The smallest animal, O. pumila, occupies the smallest crevices and the largest, O. wendtii occupies the largest crevices. Moreover, it is clear from the measurements of disc height and spine span (Table 1) that the two largest species are mostly unable to use the small crevice openings (median height 0.5 cm) used by O. pumila. There could, however, be competition for space between small individuals of those species and O. pumila. Very few O. pumila were found behind crevices higher than 1.0 cm. This suggests either that they have an aversion to wide crevices or that they are excluded from them by the other species; larger size has often been considered to confer com- petitive dominance (Wilson, 1975; Krebs and Davies, 1981). The measurements of O. wendtii suggest that it would have no difficulty in occupying the crevices inhabited by O. echinata, but it actually used crevices that were considerably larger; much larger than could be explained only by their dif- ference in size. Either O. wendtii prefers roomy crevices or more suitable crevices are limited and it is excluded from them by competition with O. echinata or other species. Thus the availability of suitable sized crevices will affect the distribution SIDES AND WOODLEY: NICHE SEPARATION IN THREE BRITTLE-STARS 713

of these three species and may account for observed differences in their distribution (Kissling and Taylor, 1977; Lewis and Bray, 1983). The three species were found to be active at night. This type of restricted activity period is common among shallow water echinoderms (Crump, 1965; Ebling et aI., 1966; Magnus, 1967; Clark, 1976; Nelson and Vance, 1979; Sloan, 1980; Sides, 1981; Hammond, 1982; Hendler, 1982; 1984; Meyer, 1982) and is generally considered to be means of avoiding diurnal predators (Bakus, 1968; Ogden et aI., 1973; Sides, 1976; Nelson and Vance, 1979; Hendler, 1984). However, the three species were also seen to differ in the degrees that they exposed themselves at night, suggesting that nocturnal predators may also be important. Ophiocoma pumila has been found to be readily attacked by diurnal and nocturnal predators (Sides, 1976; 1981; Hendler, in press), whereas O. wendtii was rarely attacked in the field. The susceptibility of O. echinata to attack was intermediate (Sides, 1976; 1981; Hendler, in press). Differences in palatability to predators may affect the behavior of these brittle-stars, and may also be important in determining the size of crevice openings used. The ability of ophiuroids to use several feeding methods is well documented (Warner, 1982) thus it is not surprising that the three species used the same general feeding methods. Each species was capable of using several methods, the pre- dominant method varying and was probably dependent on the location of the crevice that the individual occupied. Chartock (1972) found considerable overlap between the seven species of Ophiocoma at Enewetak and suggested that this type of versatility allows the species to adapt readily to their immediate surroundings and so utilize a wide variety of resources. One of the major differences between the Atlantic and Pacific species of Ophiocoma is that none of the Atlantic species were observed to use a mucus net; rather they used their spines as sticky rods. This method of feeding has been described before (Austin, 1966; Woodley, 1966; Pentreath, 1970; Chartock, 1972; Warner and Woodley, 1975). Ophiuroids have also been observed to use their tube-feet for the collection of particles but active pulling by the feet aided by the arms has only been described for Ophiocoma scolopendrina (Magnus, 1967). Chartock (1972) found that the stomach contents of the Ophiocoma species at Enewetak showed a very broad overlap in both size and type of particles ingested; 90% of the contents were sand and pieces of algae. O. wendtii. O. echinata and O. pumila also showed a broad overlap in particle size and type ingested and their stomach contents consisted largely of sand and plant material. In contrast to what might be expected on the basis of the size difference between them, a larger proportion of very fine particles was found in the stomachs of O. wendtii. the largest of the three species, and larger particles in O. pumila. the smallest of them. Bray (1975) noted that the stomachs of O. wendtii contained more fine material and less binding mucus than the stomachs of O. echinata. In conclusion, we can state that the brittle-stars O. wendtii. O. echinata and O. pumila like most other closely related species that appear to co-exist, show striking and subtle differences in several aspects of their life habits when these are studied in detail. The most distinct separation between these three species was spatial, based on the size of crevice openings used; this was further enhanced by differences in behavior, feeding methods and food selection.

ACKNOWLEDGMENTS

Financial support to E.M.S. came from the Inter-University Council for Higher Education Over Seas, Mrs. E. M. Sides, and from employment to Dr. J. B. C. Jackson. E.M.S. also wishes to thank 714 BULLETIN OF MARINE SCIENCE, VOL. 36, NO.3. 1985

the Department of Earth and Planetary Sciences of The Johns Hopkins University for the use of their facilities and their hospitality while earlier drafts of the manuscript were in preparation. J.D.W. is similarly grateful to Prof. N. A. Mitchison and the Dept. of Zoology, University College London. We are grateful to Drs. J. B. C. Jackson, G. Hendler, and S. A. Woodin for critically reading earlier drafts of the paper. Parts of the manuscript were presented as partial fulfillment for a M.Sc. to E.M.S. This is contribution number 340 from the Discovery Bay Marine Laboratory, University of the West Indies.

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DATEACCEPTED: November 29, 1984.

ADDRESSES:Department oj Zoology, University oj the West Indies. Kingston 7, Jamaica; MAILING ADDRESS:(E.M.S.) 45 Hainault Road, Foxrock, Dublin 18, Ireland.