(Echinodermata) from a Shallow Back-Reef Lagoon, Discovery Bay, Jamaica

BULLETIN OF MARINE SCIENCE, 32(2): 549-571,1982 CORAL REEF PAPER

PATTERNS OF FEEDING AND ACTIVITY IN DEPOSIT-FEEDING HOLOTHURIANS AND ECHINOIDS (ECHINODERMATA) FROM A SHALLOW BACK-REEF LAGOON, DISCOVERY BAY, JAMAICA

L. S. Hammond

ABSTRACT The holothurians Isostichopus badionotus Selenka, Holothuria mexicana Ludwig, H. thomasi Pawson and Caycedo, Actinopyga agassizi Selenka and Euapta lappa Miiller, and the c1ypeastroid echinoid Clypeaster rosaceus L., had distinctly nocturnal patterns of activity and feeding. The spatangoid echinoid Meoma ventricosa Lamarck was more active at night than by day. Except in E.lappa, which was strictly nocturnal, activity increased during the afternoon, peaked before midnight, then declined to a minimum before midday. All species exhibited some form of diurnal concealment except I. badiono/Us and H. mexicana, which remained fully exposed at all times. These and other data suggest nocturnal activity, which may have evolved as a predation avoidance mechanism, as the paradigm of ancestral holothurian behavior. Evidence in support of a similar explanation for the behavior of the irregular echinoids is slight. Of the "permanently" infaunal species, the holothurian H. arenicola Semper did not vary its feeding throughout the 24-h cycle, while data suggesting diel variations in activity in the spatangoid echinoid Plagiobrissus grandis Gmelin were equivocal. The two spatangoid species and H. arenicola were major agents of bioturbation where they occurred at maximum densities, but the other holothurian species did not disturb or transport large quantities of sediment. In the short-term «I day), movements of I. badionotus, H. mexicana, M. ventricosa and P. grandis were random. Over a IO-day period, I. badionotus and H. mexicana moved less than predicted by the random walk theorem; this was attributed to boundary effects in an heterogeneous environment, and may explain how the patchy dispersion of each species is maintained. Over 9 days, in an apparently uniform environment, both species of spatangoid moved distances similar to those predicted for random walking. The density of the cryptic H. thomasi in a patch of coral heads may have been limited by the number of available, suitable crevices; the frequency with which animals changed crevices was considered an index of microhabitat suitability. The stability of burrows of H. arenicola over long periods of time can be related to their association with buried rubble, which provides a physical refuge from disturbance by bioturbation.

Patterns of predominantly nocturnal activity, usually associated with feeding, are widespread in the Phylum Echinodermata (Reese, 1966). Semper (1868) pos .. tulated that nocturnal activity and feeding characterized most holothurians, and there is much evidence to support this generalization (Crozier, 1915; Stier, 1933; Yanamouti, 1939; Crump, 1965; Berrill, 1966; Bakus, 1968; Konnecker and Kee .. gan, 1973). However, some species are thought to feed uniformly both day and night (Yanamouti, 1939; Bakus, 1973). Diel rhythms of feeding and activity an: also widely known in echinoids (Thornton, 1956; Sinclair, 1959; Ogden et aI., 1973a; Abbott et al., 1974; Nelson and Vance, 1979), but have been recorded in few species of deposit-feeding echinoids (Chesher, 1969; Gladfelter, 1978). Despite recognition of the general prevalence of diel rhythms of activity and feeding, previous studies of holothurians have attempted only gross assessments of movement or sediment processing through the guts, with varying degrees of exactitude (Guppy, 1882; Crozier, 1918; Mayor, 1918; Yanamouti, 1939; Trefz, 1958; Yingst, 1974; Webb et al., 1977). None of these studies, nor the more 549 550 BULLETIN OF MARINE SCIENCE, VOL. 32. NO.2. 1982

detailed ones of Chesher (1969) and Gladfelter (1978) on echinoids, involved continuous monitoring in the field, Traditionally, such studies were concerned with elucidating the role of deposit feeders in modification of reef sediments, by dissolution and attrition, and their influence on the physical disposition of sediments, by bioturbation and transport. However, there are further consequences of deposit feeding for which detailed studies of the diel variation of activity and feeding have major implications. These include the structuring of infaunal com- munities through predation and disturbance (Rhoads and Young, 1970; Woodin, 1978), and regulation of nutrient fluxes between sediments and the overlying water through either physical disturbance (Rhoads, 1973; Aller, 1978), or influence on the activities of the microfauna (Aller, 1978; Gerlach, 1978). Definition of optimum feeding strategies for deposit feeders, and of mechanisms of resource partition.ing between co-existing species (Levinton, 1972; Levinton and Lopez, 1977; Taghon et aI., 1978) require detailed knowledge of feeding patterns and processes. This study examined patterns of activity and feeding in six species of holothurians and two spatangoid and one clypeastroid echinoid species in the shal10w back-reef lagoon, Discovery Bay, on the north coast of Jamaica.

MATERIALS AND METHODS Study Area and Species A useful description of the marine habitats of Discovery Bay may be found in Woodley and Rob- inson (1977). The dispersion patterns and habitat associations of the aspidochirote holothurians Ho- lothuria mexicana Ludwig, H. arenicola Semper, H. thomasi Pawson and Caycedo, Isostichopus badionotus Selenka and Actinopyga agassizi Selenka, the apodous holothurian Euapta lappa Miiller, and the spatangoid echinoids Meoma ventricosa Lamark and Plagiobrissus grandis Gmelin in the western lagoon (Fig. I) were reported by Hammond (in prep!). The c1ypeastroid echinoid Clypeaster rosaceus L. was found only in the eastern lagoon. The study utilized two areas in the western lagoon (Fig. I): Site I, an "heterogeneous" habitat (Hammond, in prep.)' consisting of a mosaic of mounded sand, rubble, coral heads and light macro- algal growth, and; Site 2, an open, relatively homogeneous sandy area, adjacent to which were large patches of dead coral heads and mounds formed by the infaunal funnel feeder, H. arenicola. Site 3, in the eastern lagoon (Fig. I), comprised a stand of the seagrass, Thalassia testudinum. surrounded by sand and coral heads. Site 4, also in the eastern lagoon, was a lithified Pleistocene pavement covered by a felt-like algal turf, with intermittent coral heads and crevices. All sites were in 1-3 m of water. Twenty-four-hour Surveys Similar approaches were employed for six species; these are summarized in Table I. The straight line distance traveled by each specimen of each species was measured at approximately 4-h intervals during the 24-h survey. All surveys of each species were done on different dates, at approximately the same phase of the moon, except the last four surveys of P. grandis, in which two groups of 10 animals were followed for 2 consecutive days. H. arenicola showed no detectable daily movements, except irrigation of its burrow and defecation. The cylindrical feces of J. badionotus were collected at each interval, dried and weighed. Holothuria mexicana and H. arenicola produce regular sized fecal pellets. Within a sample of 10 animals of each species, it was found that pellet number and dry weight were highly correlated for each animal (r from 0.92 to 1.0, P <0.01), so on all surveys counts of pellets were recorded and the dry weight of a sample of pellets from each animal was used to calculate weight defecated in each interval. Since the echinoids do not produce discrete feces, bound by a mucous envelope, and the spatangoids defecate below the sediment surface, the amount of sediment passed was not determined. The length of all animals, except the infaunal H. arenicola, was measured. The echinoids posed no problems, but holothurians contract markedly and unpredictably when handled. Several times during each survey the length of each holothurian was measured by holding a flexible tape above it, avoiding disturbing the animal. The length was taken as the average of these measurements .

• Hammond, L. S. Dispersion and habitat relations of deposit·feeding holothurians and echinoids (Echinodermata) from a shallow reef lagoon, Discovery Bay. Jamaica. In preparation. HAMMOND: ACTIVITY AND FEEDING IN DEPOSIT-FEEDING ECHINODERMS 551

, \ \ \ \ DISCOVERY BAY \ t -' "'- .... , I I / / .•. / - ---'"

, . 300 M

Figure I. Map of Discovery Bay, showing the eastern and smaller western lagoon behind the fringing reef (cross-hatched), bounded by the -10 m contour. The locations of the study sites 1-4 are marked.

On each survey, the number of changes of direction greater than 450 made by individuals of five species (Table I) was recorded. Smaller changes were often ambiguous, so were excluded. Direction changes were detected by the trail of disturbed sand left by the burrowing spatangoids, or by the feces trail and orientation of the animal in the other three species. To test for randomness, on one survey for each species in which long term patterns of movement were studied (below), the net direction of travel by an individual during each interval was allocated to one of the four quadrants of an underwater compass. Travels along the north-south or east-west axes were assigned to the next quadrant clockwise. A Chi-squared analysis was constructed, to test the hypothesis that the direction of travel did not deviate from that predicted by randomness (i.e., an equal number in each quadrant). In only one interval for each of M. ventricosa and P. grandis, and in none for the holothurian species, was the Chi-square significant (P < 0.05). To test whether the shoots of Thalassia testudinum restrict the activity of C. rosaceus in seagrass, the overnight (1800-0600 h) travel of 20 animals in an area of dense grass blades, and a further 20 in an area of sparser blades, was measured. In each area, the animals were subdivided into two groups, one of high density and the other lower. The grass blade densities were determined from counts within three O.lm' quadrats thrown in each area. The habits of the other three holothurian species necessitated a different approach. Holothuria thomasi and E. lappa were studied in an area of dead coral heads, approximately 20 x 20 m, adjacent to Site 2. The former species lives in crevices under heads of live or dead coral, from which it extends to feed on the adjacent sand, with its posterior end wedged within the crevice (Pawson and Caycedo, 1980). The positions of up to 31 H. thomasi were mapped, and at approximately 4-h intervals on each of eight 24-h surveys, the number of animals extended in a feeding posture, and the distance extended (measured from the crevice to the anterior end of the animal) were recorded. Since the posterior end of each animal was located in a crevice, it was not possible to collect the feces. Changes in position were noted, but on occasions when several animals relocated, it was not always possible to determine where each had moved, as individuals were difficult to identify with confidence. This limitation was compounded in E. lappa by the mobility of the animals during hours of darkness. Tagging by appli- cation or injection of vital stains proved unsuccessful, since the animals developed lesions and ulti- 552 BULLETIN OF MARINE SCIENCE, VOL. 32, NO.2, 1982

Table I. Sampling protocol to determine 24-h activity andlor feeding patterns in three holothurian and three echinoid species (Methods are given in text)

Animalsl Distance Feces Direction Species Site No. Surveys Survey Recorded Collected? Recorded?

Holothurians H. mexicana 1 2 10, 10 yes yes yes I. badiono/Us 1 3 10, 10, 10 yes yes yes H. arenicola 2 3 20,20, 10 no yes no Echinoids M. ventricosa 2 3 20,20,20 yes no yes P. grandis 2 6 10, 20, 10 yes no yes 10, 10, 10 C. rosaceus 3 2 20, 20 yes no yes (in seagrass) C. rosaceus 3 3 20, 20 yes no yes (on sand)

mately autotomized that section of the body. Thus, in E. lappa. only the number of animals present during each interval was recorded, along with incidental notes on feeding and movement. Feces were not collected as they are not consolidated by a mucous envelope, and are rapidly dispersed. At Site 4 in the eastern lagoon, the positions of 18 A. agassizi were marked, and at irregular intervals (five or six times per day) over 3 days, the number of animals emerged from their crevices to feed was recorded. The crevice occupied by each animal by day was also noted. Feces were not collected. The substrate upon which individuals of the five epibenthic species of holothurians were observed to feed was classified as: sand, bare hard surfaces (rubble, dead coral and pavement), erect macroalgae, and algal turf growing on dead heads and rubble. Note was taken of the frequency with which each type was used by each species. In the last three categories, the animals feed on fine sediments which adhere to the substrate. The levels of dissolved oxygen in the sediment pore water, sampled by syringe from 4 cm below the surface, and in the seawater at the sediment-water interface were recorded at Site 2 over two 24-h periods using a portable oxygen meter.

Gut Passage Times

The time taken for sediment ingested at different hours of the day to pass through the guts of H. mexicana. I. badionotus and H. arenicola was measured. For the last species, measurements were made easily in the field. Sand stained red with nontoxic commercial paint was placed at the bottom of the feeding funnels of 10 individuals at each of the following times: 0430, 1030, 1630 and 2230 h, and the time taken for it to appear at the top of each mound was recorded. The other two species of holothurians proved difficult to manipulate in the field, since any method that would cause ingestion of quantities of stained sand or dye sufficient to be detected in the feces involved considerable disturbance of each animal. With animals that had become acclimatized to laboratory conditions during feeding experiments (Hammond, 1979), it was found that gut passage time could be assessed by transferring animals from tanks containing relatively fine sediments to tanks containing relatively coarse sand, or vice versa. In either case, the time taken for the new substrate to appear in the feces was recorded. Animals were found to resume feeding quickly after transfer, and observations of their behavior indicated that it did not radically depart from that of animals in the field. Gut passage times for the other three species were not determined. Incidental observations were made on E.lappa, in both the field and the laboratory. The colored sand technique was unsuccessfully attempted with the two spatangoid species in the field, and laboratory procedures used for the holothurians were not readily applicable to the burrowing spatangoids. Chesher (1969) measured gut passage time in M. venlricosa by feeding dye, then dissecting animals at intervals. His data are considered in discussion here. The density of feces of 10 specimens each of H. mexicana, I. badionolus, and H. arenicola, and sediment taken adjacent to each animal, was calculated as gm dry wt/cc wet volume. The diameter of the fecal pellets was also measured. The gut lengths of at least 10 animals of each species were HAMMOND: ACTIVITY AND FEEDING IN DEPOSIT-FEEDING ECHINODERMS 553 recorded. By assuming the gut to be a relatively uniform tube (Yanamouti, 1939; Hyman, 1955), equal in diameter to the feces, its volume may be calculated as that of a cylinder.

Long Term Movements

The movements of 12 animals each of H. mexicana and I. badionotus at Site I were recorded for 10 and II days, respectively, by measuring the straight line distance traveled, and the distance in a straight line from the original starting point, at mid-day of each day. Employing similar methods, 20 M. ventricosa and 20 P. grandis were monitored at Site 2 for 7 days. The total daily distance traveled (measured along the disturbance path) was recorded for the spatangoids, but could not be determined for the holothurians. The sum of the distances traveled during each time interval of the 24-h surveys was taken as a measure of total distance traveled by the holothurians. Measurements of the distance from feeding funnel to the apex of the mound, and the orientation of this axis, were made on 10 H. arenicola mounds on five occasions spread over I month, at intervals ranging from 3 days to 2 weeks. To detect longer term movements, 10 steel stakes were driven into the sediment in a crudely polygona] arrangement so as to surround an area of approximately 6 m2, in which ]7 H. arenicola mounds were located. Distances from the apex of each mound to the threl~ adjacent stakes provided co-ordinates from fixed points to each mound. Measurements were made on six occasions over a period of II months, at intervals ranging from I week to 7 months. The eight surveys of H. thomasi were spread over a 3-week period, with I to 6 days between surveys. Changes of position were mapped. Limited data were also gathered on E. lappa and, at Sit,~ 6, A. agassizi.

RESULTS Twenty-four-hour Surveys The daily pattern of activity, egestion and gut passage time for H. mexicana and I. babionotus are shown in Figures 2 (A, B, C) and 3 (A, B, C), respectively .. The egestion of feces by H. arenicola, and the distances travelled by M. ventri-· cosa, P. grandis and C. rosaceus during each interval are shown in Figure 4 (A, B, C, D, respectively). The size of the animals, the total daily travel, the number of turns made per day, and the amount of material defecated each day are sum .. marized, where applicable, for each species on each survey in Table 2. Four species, H. mexicana, I. badionotus, M. ventricosa and C. rosaceus, showed marked diel differences in activity and, where measured, in feeding. In each species, the pattern was one of increasing activity during the afternoon, peaking prior to midnight, then declining through the morning to a period of relative immobility before midday. Despite the high variation within each data set, evidenced by the wide standard deviations, the maximum of the curve from each survey was significantly different from the minimum (Table 3, P < 0.05). The averaged daily data from each survey (Table 2) also showed considerable variability. Differences between surveys were in most cases not significant (P < 0.05), but where they were (Table 4), they resulted from factors other than pu·· tative lunar cycles, as these were controlled for during sampling. In H. mexicana and I. badionotus, the pattern of production of feces approx·· imated that of activity. Both species passed sediment at variable rates, which on average depended upon the time of day at which the sediment was ingested (Figs. 2C, 3C). Since the period of maximum egestion coincided with the period of maximum passage rate through the gut, it follows that ingestion must have been greatest at that time. Thus, cycles of activity and feeding coincide. The averagt: duration of gut passage in an actively feeding animal of either species was about 5 h. During daylight hours, M. ventricosa was found buried in the sediment to the apex of the test. Specimens were not observed to bury deeper in clean coarse sand, or during storms, as reported by Chesher (1969). At dusk, the urchins 554 BULLETIN OF MARINE SCIENCE. VOL. 32. NO.2. 1982

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'" • •••., '"=> 10 . '"=> 10 0 • 0 .3 ••• .3 • • • • Ii\! •. • LW • '. ~ 0·'. A•• 0 0:: , t- ••• 0 00 '. • 0 • ••• ". • •.'

0400 1200 2000 0400 1200 2000

TIME OF DAY (HOURS) TIME OF DAY (HOURS) Figure 2. (Left) Activity and feeding patterns of H%thuria mexicana during the two 24-h surveys at Site I (dots = first survey, triangles = second survey) and during laboratory experiments. A, Dis- tance traveled (cm ·animal-I• h-'); B, Amount of sediment egested (g·animal-1• h-I); C, Time taken for sediment to pass through gut (h). In figures (A) and (B), each data point represents the mean of observations of 10 animals, and is plotted at the mid-point of the period during which the observations were made. In figure (C), each point represents a single observation. Figure 3. (Right) Activity and feeding patterns of lsostichopus badionotus during three 24-h surveys at Site I (dots = first survey, triangles = second survey, open circles = third survey) and during laboratory experiments. For further explanation, refer to the legend of Figure 2. emerged from the sediment and remained active on the surface until burrowing again between first light and sunrise. This period coincides with that of greatest activity in (Fig. 4B). The average rates of movement by day and night compare well with those recorded by Chesher (1969). The specimens were larger (Table I: maximum size 20.2 em) than recorded in other studies (Kier and Grant, 1965; Chesher, 1969; Telford, 1978). Measurements of oxygen content of the sediment pore-water and at the sediment-water interface (Fig. 5) are consistent with Chesh- er's (1969) hypothesis that emergence is a response to lowered oxygen tensions in the sediment. Further support lies in observations that animals in coarse, welJ- aerated sediments of the rear zone and the fore-reef did not emerge at night. An alternative hypothesis, that the animals emerge at night to feed on the organically- HAMMOND: ACTIVITY AND FEEDING IN DEPOSIT-FEEDING ECHINODERMS 555

150 z 0 10 0- ~ ] 0- ;;\ 100 :oj - V) N ;:; '" 50

0400 1200 2000 0400 1200 2000 TIME OF DAY (HOURS) TIME OF DAY (HOURS) Figure 4. (Left) Patterns of feeding or activity in four species of deposit-feeding echinoderms during 24-h surveys at Sites 2 and 3. A, Amount of sediment egested by Holothuria arenicola (gm· animal-I. h-1) during three surveys. Symbols as in Figure 3A, B; B, Distance traveled by Meoma ventricosa (cm' animal-I. h-1) during three surveys. Symbols as in Figure 3A, B; C, Distance traveled by Plagiobrissus grandis (cm·animal-1.h-l) during six surveys. (Dots, triangles and open circles are the lirst three surveys respectively,lilled squares = fourth survey, open triangles = lifth survey, open squares = sixth survey); D, Distance traveled by Clypeaster rosaceus (cm' animal-I. h-I) during two surveys in seagrass (solid lines) and two surveys on sand (broken lines). Symbols as in Figure 2A, B. In all ligures, each data point represents the mean of observations of at least ten animals (see Table I), and is plotted at the mid-point of the period in which the observations were made. Figure 5. (Right) Oxygen concentrations (% saturation) in sediment pore water (dots and open circles), at the sediment-water interface (lilled and open squares) and one meter above the bottom (lilled and open triangles) over two 24-h periods at Site 2. rich surface layers of sediment, was not substantiated by analysis of the organic content and total plant pigment levels in the fore-guts of animals collected at 0200 h. These did not differ from daytime levels (Hammond, 1979). A well developed covering response (Reese, 1966) was found in C. rosaceus during daylight hours, mainly utilizing fragments of Thalassia when inhabiting the seagrass, or shells or pieces of coral rubble when living on sand. In the latter habitat, animals burrowed into the sediment at daybreak to a depth of about three-quarters of the test height. The distance traveled per day on sand was significantly greater in both surveys than in the Thalassia meadow (t3R = 6.11, 556 BULLETIN OF MARINE SCIENCE. VOL. 32, NO.2. 1982

Table 2. The mean and standard deviation of length of the animals, total distance traveled, total dry weight of material egested, and the mean number of turns made during 24-h surveys of three holothurian and three echinoid species

Length Distance Feces Species Site Survey (em) (em) (gm) (1 Turns

Holothurians H. mexicana I 36.1 ± 6.9 455 ± 215 119 ± 18 5.9 2 34.3 ± 3.2 579 ± 267 112 :!: 55 I. badionotus I 27.4 ± 5.5 420 ± 182 95 ± 13 6.4 2 29.3 ± 6.3 397 ± 115 118 ± 35 3 31.9:!:3.4 438 :!: 237 68 :!: 34 H. arenico/a 2 1 40:!: 12 2 64 :!: 22 3 70 ± 25 Echinoids M. ventricosa 2 1 16.6:!: .9 93 :!: 48 3.0 2 16.5:!: 1 160 :!: 69 3 16.9 ± .9 118:!: 56 P. grandis 2 I 16.0 ± 2.4 60 ± 16 1.1 2 16.5 ± 2.6 42 ± 12 3 49::!: II 4 43 ± 20 5 44 ± 12 6 53 ± 20 C. rosaceus 3 I 13.1 ± 1.1 134 ± 59 3.] (in seagrass) 2 11.6 ± 2.6 169 ± 61 C, rosaceus 3 I 12.9:!: 2.6 288 ± 96 3.2 (on sand) 2 12.1 :!: 2.1 312 :!: 123

P < 0.001; t38 = 3.25, P < 0.005, respectively). There was no evidence that this was due to physical impediment to movement by shoots of the seagrass. Animals in relatively sparse seagrass at Site 3 did not move significantly further than animals in relatively dense seagrass (Table 5; tl8 = 1.19, P > 0.20). The similar number of turns made daily by animals in seagrass or on sand (Table 2) also suggest that Thalassia shoots do not restrict travel. There were no significantly different rates of movement in areas with different densities of animals, at either high or low concentrations of Thalassia blades (Table 5; tl8 = 1.06, P > 0.20 and t18 = 0.05, P > 0.50, respectively). However, the higher rates of travel on sand may be related to food availability. The guts of animals from the seagrass area contained many fragments of plant material and some sediment, whereas those from the sand contained only sediment. Analyses conducted in conjunction with other studies (Hammond, 1979) showed 2.46 and .96% of organic carbon, and 1.89 and .60 mg' gm-I dry weight of total plant pigment in the guts of animals from the two habitats respectively. Support for this hypothesis may be found in the dispersion patterns of the animals (Hammond, in prep.)I. In the seagrass, they were aggregated, but on the sand they were uniformly dispersed, implying intra- specific competition, possibly for food (Connell, 1963). In both habitats, the guts were found to be empty by day, and only partially full even at midnight, as studies of other clypeastroid urchins have also found (Bell and Frey, 1969). A different diel pattern of activity was found in P. grandis, which remains buried in the sediment at all times unless disturbed. Five of the six surveys HAMMOND: ACTIVITY AND FEEDING IN DEPOSIT-FEEDING ECHINODERMS 557

Table 3. Values of student's t statistics, and their levels of significance, p, used to evaluate within- survey differences between the maxima and minima of (a) distance traveled per hour, or (b) amount of sediment egested per hour, for H. mexicana, I. badionotus, M. ventricosa. P. grandis. and C. rosaceus (Fig. 2-4) (The degrees of freedom may be inferred from Table I)

Species Survey Parameter P

H. mexicana 1 a 3.22 <.005 2 a 3.64 <.002 I b 3.30 <.005 2 b 5.20 <.001 I. badionotus 1 a 2.99 <.01 2 a 2.18 <.05 3 a 2.70 <.02 1 b 4.36 <.001 2 b 5.52 <.001 3 b 7.07 <.001 M. ventricosa 1 a 2.49 <.02 2 a 2.12 <.05 3 a 2.27 <.05 P. grandis 1 a ns 2 a 2.68 <.02 3 a 2.30 <.05 4 a 1.52 >.10 5 a 2.89 <.01 6 a 1.66 >.10 C. rosaceus (grass) 1 a 2.61 <.02 2 a 5.40 <.001 C. rosaceus (sand) I a 3.24 <.005 2 a 5.12 <.001 showed an increase in activity during the middle of the day (Fig. 4C), but this was significant in only three of the surveys (Table 3). Therefore, the data must be considered equivocal on the question of diel cycles of activity in P. grandis. As Table 2 shows, only a narrow size range of each of the five species considered above was represented in the surveys; this reflects the predominately left- skewed size frequency distributions of these species in the lagoon (Hammond, 1979; Jeal, pers. comm.) Accordingly, there were few significant correlations between size of the animal and distance traveled per day (Table 6). They occurred in two of the four surveys of C. rosaceus and the third survey of I. badionotus. There were no significant correlations between the size of specimens of either epibenthic holothurian species and the amount of material defecated daily. Holothuria arenicola, which is permanently infaunal, showed no daily rhythm in the egestion of feces (Fig. 4A). This accords with a consistent gut passage rate of about 6 h at all times of the day. There was some variability in gut passage rate on each occasion (range: 4.5-12 h) but the standard deviation is not pre .. sented, as the animals were monitored in the field only at approximately 2-h intervals. The variability may result, in part, from natural differences between individuals, but much should be attributed to the experimental technique. Un- doubtedly, when colored sand was placed in the feeding funnels, the degree to which it was accessible to the holothurian varied, depending on whether sand collapsed into the funnel in the process. However, the results provide a clear indication that H. arenicola does not possess a daily feeding rhythm. The number of H. thomasi extended from crevices to feed at each interval 558 BULLETIN OF MARINE SCIENCE, VOL. 32, NO.2, 1982

Table 4. Values of student's t statistics, and their levels of significance, P, used to evaluate differences in (a) total distance traveled, or (b) total amount of sediment egested, between surveys of H. mexicana, I. badionolus, H. arenico/a, M. venlricosa, P. grandis and C. rosaceus (Table 2) (The degrees of freedom may be inferred from Table 1)

Species Survey Pair Parameter P

H. mexicana 1,2 a l.14 >.20 1,2 b .38 >.50 I. badionotus 1,2 a .33 >.50 1,3 a .20 >.50 2, 3 a .49 >.50 1,2 b l.94 >.05 1,3 b 2.35 <.05 2, 3 b 3.24 <.005 H. arenico/a 1,2 b 4.28 <.001 1,3 b 4.48 <.001 2, 3 b .67 >.40 M. venlricosa 1,2 a 3.63 <.001 1,3 a 2.14 <.05 2, 3 a 1.54 >.10 P. grandis 1,2 a 3.47 <.002 1,3 a 1.74 >.05 1,4 a 2.13 <.05 1,5 a 2.53 <.05 1,6 a .91 >.20 2,3 a 1.66 >.10 2,4 a .14 >.50 2, 5 a .43 >.50 2,6 a 1.85 >.05 3,4 a 1.05 >.20 3, 5 a 1.07 >.20 3,6 a .46 >.50 4, 5 a .16 >.50 4,6 a 1.12 >.40 5, 6 a 1.19 >.40 C. rosaceus (grass) 1,2 a 1.84 >.05 C. rosaceus (sand) 1,2 a 0.69 >.40 C. rosaceus (grass, sand) I, I a 6.11 <.001 C. rosaceus (grass, sand) 2, 2 a 3.25 <.005 during the 24-h cycle is shown in Figure 6A. The species had a marked diel rhythm, feeding mainly at night and withdrawing into crevices approximately at sunrise, but it was not strictly nocturnal. A few specimens were tardy in retiring, so that a progressively smaller percentage of the population could be observed through the morning. None was seen by the middle of the day. There was a progressive appearance of animals from their crevices during the afternoon, and as darkness fell all animals were found to be feeding. These results help reconcile the conflicting observations reported by Pawson and Caycedo (1980), where in some locations the specimens were observed at night, while at others the animals were also seen to feed between 1100 and 1700 h. The average distance extended from the crevice during the 24-h surveys follows a very similar pattern (Fig. 6B), except that there appears to be a sharp peak in the curve immediately following the fall of darkness. A further measure of the nocturnal activity of the species is shown in Figure 6C: when animals relocated HAMMOND: ACTIVITY AND FEEDING IN DEPOSIT-FEEDING ECHINODERMS 559

Table 5. Mean and standard deviation of distance traveled between 1800 hand 0600 h at Site 3, by 10 C. rosaceus in each combination of high and low density of Thalassia testudinum blades and high and low density of animals

Thalassia Blades (nm-') C. rosaceus (nm-2) Distance Tmveled (cm)

2,890 1.76 152 :!: 82 2,890 0.70 118 ± 59 1,095 0.78 92 ± 36 1,095 0.28 93 ± 51 position, an movements occurred during the night, with a suggestion of a peak of activity in the first hours of darkness, followed by a more stable situation during the remainder of the night. At different times during the surveys, seven individuals of H. thomasi were observed on open sand, moving between heads. On two such occasions, the animals, about 75 cm long, were advancing about 0.25 m' min-I. This is similar to the "crawling" rate of large Astichopus multifidus described by Glynn (1965) and much faster than rates reported for other large aspidochirotes (Parker, 1921; Yanamouti, 1939). Forward motion was effected by slow waves of direct arching peristalsis (Heffernan and Wainwright, 1974) which took between 40 and 80 sec to travel the length of the animals. The tube feet were involved in grasping the substratum but appeared to have very limited utility. Euapta lappa was strictly nocturnal. None was seen before total darkness fell, and during the day, all were totally concealed. Emergence occurred rapidly, with all specimens known to occupy a given area (e.g., a coral head) appearing from concealment over a period of 15 to 30 min, between the hours of 2015 and 2045 (OST). Return to concealment, at about 0445-0515 h (OST), was equally rapid

Tab]e 6. Values of the correlation coefficient, r, and its level of significance, P, between length of specimens of H. mexicana, I. badionotus, M. ventricosa, P. grandis and C. rosaceus, and (a) total distance traveled, or (b) total amount of sediment egested, on 24-h surveys (The degrees of freedom may be inferred from Table 1)

Species Survey Parameter P

H. mexicana a .069 >.50 b .321 >.20 2 a -.]47 >.50 b -.446 >.10 I. badionotus a .382 >.20 b .245 >.20 2 a .004 >.50 b .429 >.20 3 a .699 <.05 b -.076 >.50 M. ventricosa 2 a .259 >.20 3 a -.]28 >.50 P. grandis I a -.272 >.20 2 a .283 >.20 C. rosaceus (grass) 1 a .428 >.05 2 a .567 <.0] C. rosaceus (sand) 1 a -.136 >.50 2 a .632 <.005 560 BULLETIN OF MARINE SCIENCE. VOL. 32. NO.2. 1982

(fl:J 100 ••••• • . . ~ • • •• Q • UJ .. UJ u.. so •• •• • (fl:J • / 200 . 100 ~ .:::: ./ // UJ ~ u / 0/ .:::: z "" Q t;:; UJ r Q 100 ./~ z: Q UJ 'Ill r I Iii II UJ'< ·11 fO UJ l. ~ 50 11 !~iI 1 "" ! iiI I 1 111 1 g IJ II!~!1 j ~ II j (B) ~.•T • 1 1 1 200 0'/ ./ ] • (D /

0400 1200 2000 10

TIME OF DAY (HOURS) DAYS Figure 6. (Left) Activity patterns of H%thuria thomasi during eight 24-h surveys near Site 2. The total number of animals in the study area varied from 27 to 31 on different surveys. A, Percentage of the population found extended from crevices; B, Mean and standard deviation (cm) of distance extended from the crevices. Dots without standard deviation represent single observations; C, Num- ber of animals which changed location, plotted at the mid-point of the period in which the relocations occurred (changes' h-1). . Figure 7. (Right) Distance travelled (cm) at Site I by at least ten specimens of: A, H. mexicana, observed over 10 days; B, I. badionotus, observed over II days. Dots are cumulative daily straight line distance travelled per day, triangles are distance (mean, standard deviation) traveled from the original starting point, squares are the distances from original starting point each day as predicted by the random walk theorem. and synchronous, and on all 10 occasions observed, preceded any sign (underwater) of first light. Incidental information on gut passage time was also collected. Animals observed within 0.5 h of emergence had already passed feces, while animals collected with full guts while actively feeding were found to totally void their gut contents within about 1 h. Since all animals found during the day had empty guts, and were not seen to feed, either in the field or the laboratory, it is apparent that ingested material is processed very rapidly, in approximately 0.5- 1 h. The third cryptic species, Actinopyga agassizi, also had strongly nocturnal habits. All specimens were active at night, feeding on open substrate. They re- HAMMOND: ACTIVITY AND FEEDING IN DEPOSIT-FEEDING ECHINODERMS 561

Table 7. Mean and standard deviation of animal length, gut length and diameter offeces, from which the volume of the gut has been calculated, in three species of holothurians

Length Gut Length Feces Diam. Gut Volume Species Number (em) (em) (em) (em')

H. mexicana II 26.9 ± 2.4 87 ± 15 .82 ± .J 46 I. badionotus 12 27.3 ± 5.1 85 ± 10 .73 ± .07 36 H. arenicola 10 21.\ ± 2.2 77 ± 12 .51 ± .08 16 turned abruptly to crevices at first light so that all were concealed by sunrise. They did not require total concealment (Hammond, in prep.)l, as specimens were found by day inactive in seagrass swards or wrapped around quite small coral heads or pieces of rubble. No animals were observed to feed before mid-afternoon, but then progressively larger numbers were seen to leave concealment to commence feeding. The percentages of a population of 18 A. agassizi concealed among coral heads and rubble at selected times of day during a 3-day period were: 1200 h, 100%; 1600 h, 89%; 1800 h, 73%; 1830 h, 67% and 2000 h, 0%. All animals were out feeding after sunset but before the fall of darkness. The average density of the samples of feces of H. mexicana, I. badionotus and H. arenicola were 0.97 ± 0.2, 1.03 ± 0.12 and 1.12 ± 0.21 gm dry wtlcc wet 1 volume, or approximately 1 gm' cc- • The sediment samples had approximately the same density (1.03 ± 0.15), indicating that no packing of grains results from passage through the gut. The average diameter of feces, and the average gut length of dissected animals, were used in Table 7 to calculate the gut volume of each species. Since only a narrow size range of animals was found in the epibenthic species (Table 2), and no significant correlation existed between animal length and gut length in the data used to construct Table 7 (r = 0.005, P > 0.50, and r = -0.348, P > 0.10, for H. mexicana and I. badionotus, respectively), the calculated volumes may be considered representative of the population. At Site 2, where H. arenicola was studied, most animals were of fairly standard size (20-25 cm when turgid, 15-20 cm when relaxed), and produced fairly uniform fecal pelIets (Table 7), so gut volumes are representative of the animals from which the data in Table 2 were gathered. It should be noted that only the guts of actively feeding animals should be measured in studies such as this. Ten H. arenicola, approximately the same size as the animals represented by Table 2, were starved in aquaria for use in other studies. The average gut length after one week was found to be 47 ± 5 cm, which is significantly lower than the value reported in Table 7 (t14 = 5.27, P < 0.001). The observations of the feeding substrate of the holothurian species are shown in Table 8.

Table 8. Percent frequency with which five species ofholothurians were observed to ingest sediment on five substratum types

Substratum Types No. Species Observations Sand Macroalgae Algal Turf PavementlRubble

H. mexicana 188 90 5 0 4 I. badionotus 207 69 9 2 21 H. thomasi 409 64 12 18 6 E. lappa 220 36 28 35 2 A. agassizi 48 8 II 43 38 562 BULLETIN OF MARINE SCIENCE. VOL. 32, NO.2, 1982

Long Term Movements The daily straight line travel, and distance from the original starting point on each day, are plotted for H. mexicana (Fig. 7A), I. badionotus (Fig. 7B), M. ventricosa (Fig. 8A) and P. grandis (Fig. 8B). For each species, the cumulative total of the daily straight line travel follows a linear relationship with time, showing no evidence of variation due to the occurrence of full moon in the middle of the survey period of the holothurians. The daily displacement from the origin describes a parabolic curve, in which the daily increment of displacement de- creased with time. This result is analogous to solution of the classic "random walk" problem (Feynman et at., 1963), which describes, among other phenomena, the movement of particles in Brownian motion. Therein, (D)2 = nU where (D) is the root mean square distance (displacement) from the origin, n is cumulative number of turns, and L is the average distance between turns. Using the data from the 24-h surveys, it is possible, with some assumptions, to calculate (D) on successive days. The assumptions are: (1) the randomness of direction changes by animals in a given period of time can be taken as evidence that successive changes by an individual over a longer time will also be random, and; (2) the average distance between turns (L) may be taken as the mean total daily distance traveled, divided by the number of turns. The values of L for the four species are: H. mexicana, 88 em; I. badionotus, 65 cm; M. ventricosa, 77 cm; P. grandis, 54 em. The curve calculated from the random walk equation is included in Figures 7 (A, B) and 8 (A, B). There were few indications of mobility from the I-month study of mound-funnel distance and orientation in H. arenicola. Six of the 10 animals relocated the position of the funnel relative to the mound by distances of 2-8 em (4.6 ± 2.1). The average funnel-mound distance was 42.1 ± 8.1 em, suggesting that very long periods of time are required before an animal reworks all the sediment within its presumed "reach." The measurements from the mound apices to fixed stakes showed that H. arenicola burrows were generally stationary over long periods. During the shortest time between measurements (1 week), there were no detectable changes in the location of any of the mounds. In each of three separate periods of 4, 5 and 7 weeks, there was only one change of position of a mound. Two were very minor (6 and 7 em) while the third was the largest shift recorded, 3 I em. Two animals were also lost from the area, but it is not known if these represented migration or mortality. Over the longest interval, 7 months, there were only five changes in the locations of mounds, of 8, 11, 12, 16 and 27 em. Ten specimens, 67% of the total number of H. arenicola in the area, remained stationary for the 7 months, and of these, all but one maintained the same position over the 11 months of study. This stability may be related to the observation that, in sandy areas, burrows of H. arenicola are usually associated with patches of buried rubble, which have been construed as refuges from disturbance by other organisms, principally spatangoid echinoids and the thalassined shrimp, Calli- anassa sp. (Hammond, in prep.)1. The data from eight 24-h surveys of H. thomasi indicated that 32 ± 10% of the individuals within the study area moved to a new location during each night. This provides for an average residence time of approximately 3 days; however, Figure 9A, plotting % of animals still in their original position against time, indicates that some animals, 13% of the total, remained in the same crevice for the whole 3 weeks they were under observation. The average duration of residence, calculated from 110 observed relocations, was 3.8 ± 4.0 days, close to that predicted above, but the modal duration was only 1 day (39% of the observations). Clearly, HAMMOND: ACTIVITY AND FEEDING IN DEPOSIT-FEEDING ECHINODERMS 563

(AJ 100 • (AJ /'

~ 60 /' ~ ~ /'/1 1 I = /i 1_1-~---f 20 ~~--~--I 1 1 - 1 j .. --.-e_e_,. /. 100 ./ ..... (B) z "" ~>- CB' 00 >- ~ ~= ] Z~ 60 .-----. 20::: ~ ~. >- co :5 t: 50 :;: 00 t;; = ~r~l 1 1 v--i ~_l-i§i 20 yLi-f--f-1 1 ~ .1

10 211

DAYS DAYS Figure 8. (Left) Distance travelled (em) over seven days at site 2 by: A, M. ventricosa, and B, P. grandis. Symbols as in Figure 7. Figure 9. (Right) Long term activity patterns of H. thomasi: A, Percentage of total population (N = 27-31) remaining in the crevice in which they were originally observed, on successive surveys over 3 weeks; B, Percenlage of lOlal daily relocations which were lo a crevice previously occupied by another animal, over a 3-week period. a large proportion of the animals in the study area moved frequently, whereas a few did not relocate at all. Figure 9B shows that over time, a higher percentage of relocations were to positions that had previously been occupied, at some time during the survey period, by another animal. This implies that within the study area, there was only a limited number of crevices suitable for occupation by H. thomasi. Only 58 different positions were occupied over the 3 weeks. The fact that some animals moved very frequently, and others rarely or not at all, further suggests that some crevices are "better" than others, providing a more suitable habitat. An attempt was made to determine which crevices were preferred and which were sub-optimal. Animals occupying crevices around the perimeters of the two large patches of dead coral heads in the study area, with direct access to large areas of sand, had an average residence duration of approximately 6 days, whereas those in crevices in the centers of the patches, with access to only small areas of sand and larger areas ofturf and macro-algae, moved at intervals of little more than a day. These data are in accord with the feeding habits of the species (Table 9) which show that the animals prefer to ingest sand, rather than the finer material adhering to the other surfaces. Where an animal was readily identifiable, it was found that relocations were usually to crevices within 1-2 m of the original position. A similar observation was reported by Pawson and Caycedo (1980). However, on one occasion an animal was observed to slowly travel about 10 m during the 8 to 9 h of darkness. 564 BULLETIN OF MARINE SCIENCE, VOL. 32, NO.2, 1982

Long travels such as this may not be uncommon; the number of animals within the study area varied from 28 to 31, apparently as a result of migration to and from adjacent areas of dead heads. The observations of animals (above) moving on sand confirm that H. thomas; will move across open areas. Observations over 3 days of 18 A. agassizi showed that 72 ± 1% were found hiding in the same position on consecutive days. This high level of site fidelity is probably due in part to circumstances peculiar to that area, which had only isolated patches of cover. The animals, which moved only 1-2 m during the night, thus had a high probability of returning to the same place of concealment. This may also be the case for E. lappa in an habitat with patchily dispersed cover (Sides, pers comm.). However, in the H. thomasi study area, where there were many available crevices, E. lappa appeared to change concealment positions frequently. A few distinctively colored specimens were observed to travel freely between adjacent heads on successive nights.

DISCUSSION With the exception of the two infaunal species, H. arenicola and P. grandis, all species were significantly more active at night than by day. The most pronounced diel differences in activity were shown by E. lappa, which was strictly nocturnal, remaining totally concealed from before dawn until after dark. Most other nocturnal species were characterized by some form of diurnal crypsis, through hiding in crevices (A. agassizi and H. thomasi), burying in sediment (M. ventricosa) or attaching loose cover (C. rosaceus), but equally marked diel cycles of activity were present in H. mexicana and I. badionotus, which remained fully exposed on open bottoms at all times. All nocturnal species except E. lappa, for which the appropriate data were not taken, had in common a pattern of gradually increasing activity throughout the afternoon, with a peak prior to midnight. In particular, the early evening peak in activity of the cryptic H. thomasi is similar to patterns found in cryptic Pacific (Berrill, 1966) and Mediterranean holothurians (Crump, 1965), and in cryptic ophiuroids which extend their arms from crevices to feed at night (Sides, pers. comm.). Further studies are warranted to determine if this is a general characteristic of nocturnal behavior in marine animals. Nocturnal activity has been reported in many species of holothurians, with a variety of habits: e.g., permanently infaunal (Stier, 1933; Konnecker and Keegan, 1973); diurnally infaunal (Crozier, 1915; Yanamouti, 1939); diurnally cryptic (Yan- amouti, 1939; Berrill, 1966; Bakus, 1968; Pawson and Caycedo, 1980), or diurnally exposed (Gardiner, 1904; Crump, 1965). In all these reports, nocturnal activity was associated with feeding. Yanamouti (1939) did not identify any cycle of activity or feeding in three species of aspidochirote holothurians which were always found exposed on open areas at Palau. However, Yanamouti's data are inappro- priate to any conclusion (Bakus, 1973) that a diel rhythm does not exist also in these species. Yanamouti noted only that the species fed both day and night, and that the gut was always full, which does not preclude variable ingestion rates (Chesher, 1969). Gardiner (1904; 1931) stated that surface dwellers, induding one of Yanamouti's species, H. atra, feed predominantly at night. Evidence from Quatrafages (1842), Berrill (1966) and this study belies the opinion of Clark (1907) that apodous holothurians are not more active nocturnally. The available literature provides strong support for Semper's (1868) contention that nocturnal activity and feeding are general attributes of holothurians. In most animal groups, such diel behavior is endogenous, entrained by the light/dark transition, and is nullified by continuous light, while persisting in continuous darkness (Bruce, HAMMOND: ACTIVITY AND FEEDING IN DEPOSIT-FEEDING ECHINODERMS 565

1960; Pittendrigh, 1960). These characteristics have been demonstrated previously only for H. vitiens (now Bodhaschia vitiensis) by Yanamouti (1939; 1956), but were also evident in E. lappa maintained under laboratory conditions during feeding experiments (Hammond, unpublished data). Most evidence of nocturnal activity and feeding in the Echinoidea is from studies of regular, nondeposit-feeding species (Reese, 1966; Ogden et aI., 1973a; Abbott et aI., 1974). Among irregular echinoids, the nocturnal increase in activity of C. rosaceus was clearly associated with feeding. Cassidulus caribbearum ingests sediment at a faster rate at night (Gladfelter, 1978), while Mellita (Leodia) quinquiesperjorata (Salsman and Tolbert, 1965) and C. subdepressus (Hammond, unpublished observations) are more active at night, possibly in association with feeding. The nocturnal emergence and activity of M. ventricosa was not associated with increased feeding (Chesher, 1969), nor with exploitation of the organically-rich superficial layers of sediment. The significance of the daytime increase in activity of P. grandis and its relation to any feeding cycle remains unappraised. The adaptive significance of nocturnal behavior in each group is not clear. Cloudsley- Thompson (1960) listed a number of possibilities, including reproduc- tive synchrony, food availability, competitive release, and avoidance of predation. The first is unlikely, since all species of holothurian observed spawning (H. mexicana, I. badionotus, H. thomasi, A. agassizi, Astichopus multifidus) did so at dusk, maintaining a stationary, raised posture, while spawning in M. ventricosa was observed from midday to dusk. Little is known of the trophic requirements of these deposit feeders, or of the temporal variability of their food resource; however, they do not appear to be food limited at Discovery Bay (Hammond, in prep.)l. Competition avoidance is an unlikely contingency, since the most obvious competitors are the other nocturnal deposit feeders. Predation has been invoked as a major selective pressure for the evolution of nocturnal feeding in many reef- dwelling organisms, such as demersal plankton (Porter and Porter, 1977), anthozoans (Sebens and DeRiemer, 1977), crinoids (Magnus, 1963), echinoids (Ogden et al., 1973b) and fish (Hobson, 1972; 1974), and may be relevant to the nocturnal activity of the deposit feeding holothurians and echinoids. Low levels of predation on tropical holothurians by their purported major predators, fish, have been attributed to the high level and frequency of toxicity of holothurian body wall to fish (Bakus, 1968; 1973; 1974). Toxicity is considered the major predator deterrent (Bakus, 1973) although the nocturnal activity of H. difficilis was interpreted as an adaptation to avoid predation by Bakus (1968). The following phenomena may be considered indicative of a wider role for nocturnal behavior as a predator avoidance mechanism than has previously been allowed: (1) Despite the prevalence of toxicity in tropical holothurians, there are many species, particularly those of the order Apoda, in which toxicity has yet to be reported. The apodans generally have pronounced diel cycles with complete daytime concealment in some species. (2) Among holothurians from temperate waters, in which there is a very low incidence of toxicity to fishes (Bakus, 1974), diel rhythms are common (Stier, 1933; Crump, 1965; Konnecker and Keegan, 1973). (3) Marked patterns of nocturnal activity and diurnal crypsis are retained by many species which are known also to be toxic: A. agassizi (Nigrelli and Jakowska, 1960), H. difficilis (Bakus, 1968), H. bivittatus, H. lecanora, S. var- iegatus and S. chloronotus (Yanamouti, 1956). (4) Diel cycles are present in toxic species such as H. mexicana and I. badionotus, which are found exposed on open substrates by both day and night. These phenomena suggest nocturnal activity as the paradigm of ancestral holo .. 566 BULLETIN OF MARINE SCIENCE, VOL. 32, NO.2. 1982 thurian behavior, perhaps evolved in response to the feeding habits of predatory fish, which are predominantly diurnal (Bakus, 1968; 1974; Hobson, 1974), The anomalous persistence of diel rhythms in H. mexicana and I. badionotus might be considered an ethological vestige of past selection pressures, as Bakus (1968; 1969) proposed for some aspects of the diel behavior of H. difficilus. This hypothesis requires toxicity to be a more recent addition to the holothurian anti- predation repertoire. In contrast, it has been widely postulated that nocturnal activity in echinoids serves to enhance security against predation (Ogden et a1., 1973b; Fricke, 1974; Garnick, 1978; Nelson and Vance, 1979). However, evidence for this hypothesis from the deposit-feeding irregular echinoids is slight. The covering response of echinoids has been explained by some authors (Reese, 1966) as an exercise in concealment to avoid predation, but the idea is not current. Only C. rosaceus has a daily covering response, and no predation of that species was identified during this study, although dead, undamaged tests were not uncommon. A major predator of M. ventricosa, P. grandis and C. subdepressus in both the lagoon and fore-reef environments was the large gastropod Cassis tuberosa, a common predator on irregular echinoids (Gladfelter, 1978). It is also nocturnal (Hughes and Hughes, 1971), burying into the sand by day. The other predators of M. ventricosa listed by Chesher (1969) were not observed during this study. The average amount of sediment passed daily by I. badionotus (Table 2) agrees closely with the values reported by Crozier (1918) (as Stich opus moebii-92 gm' day-I, average length 27 em) and is much higher than the 25 mg' day-I passed by a slightly smaller specimen kept in the laboratory by Mayor (1918). H. fiori- dana, which is closely related to H. mexicana (Rowe, 1969) and was sometimes confused with it (Clark, 1933) passed 72-94 gm' day-I in the laboratory (Mayor, 1918). The high variability of the present data is paralleled by the wide range of values reported for the much studied H. atra (Guppy, 1882; Gardiner, 1931; Yanamouti, 1939; Trefz, 1958; Webb et aL, 1977). There have been no other studies of the variation in the rate of passage of material through the guts ofholothurians. The average duration in actively feeding animals of the three species studied here compares well with figures reported for large animals of various species by Crozier (1918), Yanamouti (1939) and Massin and Jangoux (1976). Trefz (1958) presented data for H. atra which conflict with Yanamouti's, but the differences are difficult to resolve, as Trefz's experimental technique is unclear. Longer gut passage times were reported by Yanamouti (1939), Tanaka (1958) and Bakus (1968), but these are not comparable because the animals were retained without access to further food. Gardiner (1904) cited the extreme example of retention of sediment for 3 or 4 days in the gut by Stichopus chloronotus deprived of further food. The variable gut passage times of H. mexicana and I. badionotus, if integrated over 24 h, provide for the gut to be filled about three to four times per day; the constant rate of gut passage time in H. arenicola gives a similar figure. Calculation of the gut volume (Table 7), and comparison with the volume of feces ejected per day (Table 2, where 1 gm = 1 cc) give values of 2.5,2.6 and 3.6 gut fillings per day, respectively. Allowing for errors in the methodology (including an inability to assess the effects of substrate heterogeneity at Site 1 on ingestion rates), it is apparent that feeding is approximately continuous, and that the gut is usually maintained in a full condition (H. atra; Yanamouti, 1939; Trefz, 1958), although animals were sometimes found with only partially full guts (Crozier, 1918). Both M. ventricosa and P. grandis, dissected during the day and at night, invariably had completely full guts. The former species is known to feed more rapidly by HAMMOND: ACTIVITY AND FEEDING IN DEPOSIT-FEEDING ECHINODERMS 567 day than by night (Chesher, 1969). Continuous feeding may be necessary to keep sediment moving through the spatangoid gut, since the weakly muscular gut wall may be inadequate to move the gut contents by peristalsis. Buchanan et al. (1980) found that Echinocardiurn cordaturn soon died when deprived of food, due to poisoning following changes in the redox potential of the gut contents. In the present study, only in C. rosaceus was the gut not continuously nor completely full, but details of the rate and pattern of food processing are not known. The observed pattern of long-term movements of H. rnexicana and I. badionotus clearly deviate from that predicted by the random walk equation (Fig. 7A, B). Casual observation of several specimens of I. badionotus (individuals of which are easily recognizable) over many months, supports the trend of the field data in Figure 7B. Each animal was frequently found within a small area some meters in diameter. Ebert (1978) thought that H. atro did not move out of a small area during a year. The high rates of movement reported for several species by Yan- amouti (1939) are irrelevant, as his animals were observed in a disturbed condition in an unnatural habitat. The nonrandom pattern of movement is considered to be the result of heterogeneity of the study area. Both species showed a preference for areas with some plant cover (Hammond, in prep.)1 , and for feeding on sandy substrates (Table 8). As these resources are patchily distributed within the study area (Hammond, in prep.)!, it is suggested that other substrate types act as natural "boundaries," circumscribing any tendency to ramdom motion. The resultant non-random pattern of movement may provide a mechanism for the maintenance of the populations of each species within the general area of Site 1. The relative homogeneity of the environment at Site 2 offers no such impediment to random movement; this is reflected in the results shown in Figure 8 (A, B). The predicted random walk curve of each species of spatangoid closely approx- imates that obtained from the field data. Since the behavior of the boundaries of a population of randomly-walking spatangoids should also conform to the random walk equation, the patch identified at Site 2 may be expanding. Alternatively, since Chesher (1969) has found that herds of M. ventricosa maintained their integrity over long periods, patterns of movement at the margins of populations may differ from those at the center, where the present data were taken. The importance of these deposit feeders in reworking sediment in the shallow lagoon may be determined as follows. At the measured densities of 0.1 .m-2 animals of both species (Hammond, in prep.)1 and food processing rates (Table 1), assuming the top 3 mm of sediment are ingested, a time of approximately one year is required for the epibenthic holothurians H. rnexicana and I. badionotus to completely rework the most superficial layers of sediment. Given their unse- lective feeding (Hammond, 1979) and tendency not to move great distances, the effect on sediment distribution and transport should be minimal. Holothuria ar·· enicola may significantly rework the sediment in areas where it occurs at high densities. Assuming, after Powell (1977), that it ingests predominantly the top 3 cm of sediment, and that animals in patches ingest the same amount of sediment per day as recorded in Table 2, the time required to rework the top 3 cm of sediment is less than a month. However, judging by the relative size of the fecal pellets, animals living in the dense patches may be smaller, so the time is probably longer. Chesher (1969) found that ingestion of sediment by M. ventricosa at densities of 3· m-2 reworked sediment to a depth of 6 cm in about one month, and that only a few days were required to disturb all the sediment to the same depth by moving through it. At Site 2, these calculations must be adjusted for the presence 568 BULLETIN OF MARINE SCIENCE, VOL. 32, NO.2, 1982 of P. grandis and the lower densities of both species. Assuming similar ingestion rates for both species but only one third the rate of disturbance of sediment by P. grandis (Table 2), the figures suggest that about 8 months are required to process all the sediment to a depth of 6 cm through the guts of the spatangoids, and that about 24 days are required to disturb all the sediment by locomotion. Cadee (1976) and Powell (1977) tabulated reworking rates of deposit feeders of diverse taxa from a variety of environments. Comparison with these data indicates that the spatangoids and H. arenicola are among the most prodigious reworkers of sediment. Only other burrowing holothurians, arenicolid polychaetes, enteropneusts, and thalassinid shrimps appear to have comparable rates. The last group may be the most vigorous reworkers of sediment in many environments (Cadee, 1976; Ott et al., 1976) including the Discovery Bay lagoon (Aller and Dodge, 1974). Despite the apparent insignificance of the epibenthic holothurians in reworking sediment at Discovery Bay, at other locations they may be important agents of bioturbation. The average density of the common epibenthic holothurians of Pa- cific reef flats, H. atra and H. LeucospiLota, may be one or two orders of mag- nitude higher than for the species reported here (Bakus, 1968; 1973; Webb et al., 1977). Since these species ingest similar amounts of sediment to H. mexicana and I. badionotus (Yanamouti, 1939; Webb et aL, 1977), their reworking rates are probably as high as the major groups listed by Cadee (1976) and Powell (1977).

ACKNOWLEDGMENTS

R. Aronson, M. Gore, M. Haley, E. Richardson, C. Soukup, V. Tunnicliffe and R. Warnock assisted with the night work. S. Daniels tutored me in the subtleties of the "drunkenman's walk," C. Miller provided the carbon analyses, and 1. Sandeman kindly loaned his oxygen meter. J. Bundy assisted in the preparation of the figures. I benefited from discussions with R. Brown, J. Buchanan, F. Jea], 1. Poiner and J. Woodley. This research was supported by a Jamaican award under the Commonwealth Scholarship and Fellowship Plan. The facilities of the Discovery Bay Marine Labo- ratory and the Zoology Department, University of the West Indies, are gratefully acknowledged. This is Contribution Number ]76 from the Discovery Bay Marine Laboratory.

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DATE ACCEPTED: November 26, 1980.

ADDRESS: Zoology Department, University of the West Indies, Mona, Kingston 7, Jamaica. PRESENT ADDRESS: Australian Institute of Marine Science, PMB N° 3, MSO Townsville, Queensland 48/0, Australia.