BULLETIN OF MARINE SCIENCE, 55(2-3): 375-382, 1994

ANTI-PREDATOR BEHAVIORS OF THE MEDITERRANEAN SLIPPER , LATUS

Diana E. Barshaw and Ehud Spanier

ABSTRACT Mediterranean slipper were tethered inside and outside an artificial reef to test shelter-based protection against . Mortality was significantly lower among the lob- sters in the reef (7%) compared to those in the open area (77%), indicating that sheltering is an effective protective strategy, All predation was found to occur during the daylight. Lobsters tethered in the open were observed to by placing themselves alongside rocks, thus enhancing the effectiveness of their cryptic coloration. When detected, lobsters tended to initially cling to the substrate. Gray triggerfish were observed to prey upon lobsters in the open, but were only able to kill a lobster after breaking its hold on the substrate, catching it as it tried to swim away, and biting through its ventral .

Slipper lobsters, family Scyllaridae, lack obvious protective morphological fea- tures, e.g., powerful claws like Nephropidae (clawed lobsters) or sharp spines like Palinuridae (spiny lobsters) (Cobb, 1981; Zimmer-Faust et a!., 1985). Experiments on the effect of predation on clawed and spiny lobsters have been done almost exclusively on the juvenile stages of these organisms because the adults are less vulnerable (Marx and Herrnkind, 1985; Lavalli and Barshaw, 1986; Herrnkind and Butler, 1986; Ford et a!., 1988; Barshaw and Lavalli, 1988; Eggleston et a!., 1990; Wahle and Steneck, 1991). Indeed, there is evidence that as the protective morphology of clawed and spiny lobsters develop their behavior changes from being escape-oriented to being defensive and able to stand their ground (Lang et aI., 1977; Kanciruk, 1980; Zimmer-Faust et aI., 1985; Zimmer-Faust and Spanier, 1987; Barshaw and Bryant-Rich, 1988; Spanier and Zimmer-Faust, 1988). For example, adult spiny lobsters, during migration, form protective pods with their spines pointing outward in a defensive circle (Kanciruk, 1980) and clawed lobsters change from quickly fleeing to standing their ground when their crusher claws start to develop (Lang et a!., 1977; Barshaw and Bryant-Rich, 1988). Slipper lobsters, however, do not possess morphological weaponry and it has been sug- gested that even as adults they continue to rely on sheltering (Spanier et aI., 1988), camouflage (Ogren, 1977), and escape (Spanier et aI., 1991) to avoid being preyed upon. Slipper lobsters can swim more efficiently than palinurid lobsters (Jacklyn and Ritz, 1986) or than the cumbersome clawed lobsters (Newland et aI., 1988, 1992). Laboratory experiments demonstrate that the escape swimming of the Med- iterranean can be fast (up to 3.6 body lengths·s-I), although it is of short duration and consumes much energy compared to open water fish (Span- ier et a!., 1991). In the past, experiments on the behavior and ecology of slipper lobsters were thwarted by the wide spread and deep water distribution of these lobsters and the difficultly of finding a stable population. To overcome these problems artificial reefs were built and placed at a depth of 18.5 m off the coast of Haifa, Israel. There, continuous studies could be conducted because the diving was relatively easy. The reefs were constructed of used car tires connected with 18 mm steel bars and weighed with concrete (see Spanier et a!., 1988, 1990). Suitable natural shelters for the Mediterranean slipper lobster are rare and probably limiting off the coast of Israel. Lobsters were, therefore, quickly attracted to the artificial reefs

375 376 BULLETIN OF MARINE SCIENCE, VOL. 55, NO. 2-3, 1994

Figure I. Remains of lobster after being preyed upon by the triggerfish Batistes carotinensis, notice that the lobster was killed from ventral side and that the flipper was bitten.

which provided such shelter. Using these artificial reefs, long-term studies on the ecology and behavior of S. latus were conducted, and it has thus been possible to monitor seasonal migration patterns and shelter preference of this rarely studied . These field observations combined with laboratory studies (Spanier et aI., 1988; Spanier and Almog-Shtayer, 1992) show that adult slipper lobster prefer horizontal shelters close to the substrate and with at least two small openings. Herein we (1) examine how sheltering behavior protects lobsters from preda- tion, (2) whether predation occurs during the day or at night and (3) we describe the behavior of slipper lobsters when under attack by a fish predator.

METHODS AND MATERIALS

General Procedures.-Slipper lobsters collected from artificial and natural reefs off Haifa Bay, Israel, were kept in tanks with running seawater and fed ad libitum with live pearl Pinctada radiata until needed for each run of the field experiment. Prior to each run we recorded the carapace length (CL), measured from the eye socket to the posterior margin of the carapace (lobster CL ranged from 83 to 130 mm) and sex of 18-20 lobsters. The lobsters were marked by puncturing small holes in the telson in specified patterns which identified each lobster. We then tethered the lobsters using techniques similar to Wilson et al. (1987) and Barshaw and Able (1990). In summary, 1.5 m of monofilament line (30 kg test) was tied at one end twice around the carapace of the lobstcr and secured there with "Super" glue (cyanoacrylate). In a preliminary experiment five lobsters were tethered and observed for 3 days in aquaria in the laboratory. These lobster ate the oysters provided them and sheltered in PVC tubes just as did free lobsters. Afterwards five lobsters were tethered in the field to the artificial reef. We found that these were ablc to entcr deeply into crevices in the reef and (probably during the night between dives) were able to come out of the reef and feed on oysters which had been placed outside within their reach. We concluded that lobsters were able to feed, shelter and behave in a natural way while tethered, Habitat-specific Predation.- The 18-20 lobsters were randomly separated into two groups, we then dove to the artificial reef site and tied one group of the lobsters to the reef where they could shelter and the other group to stakes placed an average of 6 m away from the reef and from each other. Lobster tethered to these stakes had no true shelter (anyplace with cover, the terrain did have mac- roalgae and protruding rocks). We returned to thc site after 24, 48 and 72 h to record how many lobsters survived to that time, and thc position of the surviving lobsters in each treatment. After 72 h (or when no lobsters remained in either of the treatments) thc run was endcd and the surviving lobsters were retrieved. This procedure was repeated five times from May through Scptember 1990 BARSHAW AND SPANIER: BEHAVIOR OF SLIPPER LOBSTERS 377

Table I. The number of slipper lobsters preyed upon during the day versus night periods, when tethered to the reef or without shelter (eaten lobsters were replaced, thus there was initially 10 lobsters tethered for each treatment) and the results of the chi-square analysis. There was a significantly greater amount of predation during the day versus the night period in the treatment without shelter.

Reef No Shelter

Nighl Day Nighl Day 0/10 1110 0110 3/10 0/10 0/10 0/]0 3/10 0110 0110 0/]0 10/10 0/10 0110 0/]0 5/10 A verage percent preyed upon ± SE a 2.5 ± 2.5 a 52.5 ± ].65 X2 1.0] 25.8 p NS <0.001

with a total of 90 lobsters being tethered. The water temperature varied from 18°_28°C during these runs. We considered a predation event to have occurred if the carapace of the lobster remained on the tether (Fig. I). If the tether was broken that data point was disregarded (we did not count broken tethers as predation by a different type of predator, such as sharks, because three of these escaped lobsters were later found alive in the reef).

Statistical Analysis I.-The data were organized into three 2 X 2 contigency tables corresponding to 24 h, 48 hand 72 h after initially being tethered. We did a heterogeneity Chi-Square analysis (Zar, 1984) showing that the data from the five runs could be pooled (24 h X2 = 2.98, P > 0.25; 48 h X2 = 5.8, P > 0.1; 72 h X2 = 5.4, P > 0.1). These tables were then analyzed using Chi Square tests. Day versus Night Predation.-In an additional experiment to reveal whether predation occurred during the daytime or nighttime, we repeated the previous procedure with the following modifications. The lobsters were initially tethered after sunset and then were checked at the next dawn, sunset and dawn. Finally, at sunset 48 h after the onset of the run, the surviving lobsters were retrieved. In this exper- iment any lobster that was eaten was replaced. Thus, every time we checked the sites we left 10 live tethered lobsters in each treatment. This procedure was repeated twice from May to June ]991, a total of 54 lobsters were tethered, with one escaping from the reef. The water temperature varied from 18°_ 20°C during these runs.

Statistical Analysis 11.- The data were organized into two 2 X 2 contigency tables corresponding to (I) the lobsters in the reef and (2) the lobsters tethered outside the reef. We did a heterogeneity Chi- Square analysis (Zar, ]984) showing that the data could be pooled (reef X2 = 0.04, P > 0.995; no shelter X2 = 1.1, P> 0.95). After pooling the data were analyzed using Chi Square tests (Table I).

RESULTS Sheltering Behavior.-Similar to previous results (Spanier et aI., 1988; Spanier and Almog-Shtayer, 1992), the lobsters tethered in the reef were found in shelters with small openings near to the substrate in 73% of the observations. The rest of the lobsters were found in shelters with larger openings. Lobsters that were teth- ered in the open placed themselves along the sides of rocks where their cryptic coloration made them difficult to detect, or under whatever macroalgae were in the vicinity in an attempt to hide. During three of the runs we observed the actual predation. Small groups (3-4) of gray triggerfish, Batistes carotinensis, attacked the lobsters. During two complete attack sequences that we were able to observe, the largest triggerfish initiated the attack by biting the flattened second antennae (flippers) of the lobster while the lobster held on to the substrate. We found bites taken out of the flippers of most of the lobster remains (Fig. ]). Triggerfish were unable to kill a lobster until they had forced the lobster to release its hold on the substrate and attempt to tailflip away. The fish then caught the lobster by a leg, 378 BULLETIN OF MARINE SCIENCE. VOL. 55. NO. 2~3. 1994

Figure 2. A triggerfish, Balistes carolinensis. killing a lobster by piercing the ventral portion of the exoskeleton after it released its hold on the substrate. flipped it over while biting off the leg, bit through the ventral exoskeleton (Fig. 2), and commenced feeding. Similar behavior was recorded in a preliminary lab- oratory experiment when a triggerfish was introduced into a large tank containing three lobsters. The consistent similarity in the types of bites and damage evident on the lobster remains led us to the conclusion that all predation in our experiment was done by B. caro/inensis. The remains of a lobster killed in the "typical" way (bitten through the ventral exoskeleton) is seen in Figure 1. Habitat-specific Predation.-There was significantly higher mOltality among the lobsters tethered outside the reef compared to those tethered to the reef (Fig. 3). Of the 46 lobsters that were tethered in the reef: 1 molted out of the tether, 3 were eaten and 42 survived and were retrieved. The remains of the lobsters that were eaten from the reef were actually found out of the reef tangled in such a way that they could not have returned. These results might have been an artifact of the tethering or they could have occurred after predation. We included these data to be conservative, but they might not indicate a realistic predation rate for the animals in the reef. Of the 44 lobsters tethered without shelter: 4 escaped (2 on the second day and 2 on the last day, they were only used in analysis of the earlier days, 3 of them were later found in the reet), 30 lobsters were eaten and BARSHAW AND SPANIER: BEHAVIOR OF SLIPPER LOBSTERS 379

C 100 U M _ WITH SHELTER U ~ WITHOUT SHELTER L 80 .------.-.------A T I V E 60

% 40 .------M a R T 20 ------A L I T o Y o 24 48 72 HOURS •••• p ( 0.0011

Figure 3. Cumulative average percent mortality of lobsters tethered in the artificial reef (with shelter) and outside the reef (without shelter). The error lines represent Standard Error. Chi-square analysis, X2 after 24 h = 16.4, P < 0.001; X2 after 48 h = 12.47, P < 0.001; X2 after 72 h = 32.0, P < 0.00].

10 survived and were retrieved. These 10 surviving lobsters were not bigger or smaller than the average tethered and at least to us they did not seem to be better camouflaged or hidden. The fact that the strategy of avoiding detection was not effective in the present study could be an experimental artifact since the activities of the divers necessarily drew attention to the approximate location of the lobster. Day versus Night Predation.-No lobsters were eaten during the night in either treatment and significantly greater numbers of lobsters without shelters were eaten during the day than during the night (Table I). There was no significant difference between day versus night for the lobsters tethered to the reef. If day and night were combined, however, just as in the previous experiment there was a greater amount of predation upon lobsters tethered without shelter versus those tethered to the reef (Chi-Square test, X2 = 22.6, P < 0.001). During this experiment pre- dation was never observed. This is not surprising since all the dives were done at night.

DISCUSSION Mortality due to predation was significantly greater for lobsters that were teth- ered without shelter compared to those with access to shelter. Thus, sheltering behavior protects lobsters from predation. Tethering of prey measures the relative rates of predation between different situations such as different habitats and is not intended to measure the absolute rate of predation in a particular environment. It was for this reason that we placed the group of lobsters without shelter outside the reef, but within the same general area. Both groups of lobsters were, therefore, exposed to the same predation pressure, i.e., fish that saw the lobsters outside could see the reef. We also provide clear evidence that predation, at least in our location, is pri- marily diurnal. Slipper lobsters like most other lobster species are assumed to be nocturnal, leaving their shelters only during the dark. However, there is only 380 BULLETIN OF MARINE SCIENCE, VOL. 55, NO. 2-3, 1994 indirect evidence supporting this assertion, for example, during frequent field ob- servations of both S. latus, and S. nodifer they were always found in shelter during the day, except on rare occasions when they were seen during their migration period (Ogren, 1977). Thus, by only leaving their protective shelter at night when predators are least active, slipper lobsters have evolved another (very common) adaptation to avoid being preyed upon. Our experiments tethering the lobsters without shelter are not hypothetical; however, since as mentioned above, in nature slipper lobsters are completely without shelter during migration. Herrnkind and Butler (1986) and Eggleston et al. (1990) used similar tethering techniques to investigate predation upon juvenile spiny lobsters. Although these investigators also showed that shelters protect juvenile spiny lobsters from pre- dation, they never observed the predation event occurring. Among the large decapod , lobsters of the genus Scylla rides are perhaps the most adapted by their morphology for passive defense. The dorsal surface of the slipper lobster presents a continuous, broad and flattened protective carapace. Moreover, the eyes are retractable into deep pocket-like orbits; the soft mouthparts fit into a protected pocket (Holthuis, 1985); the first antennae can be placed underneath the flippers which are folded down to protect the lobster from attack from the front; the relatively short, stout legs end in sharp points that enable the lobster to cling tenaciously to rough substrates; and when clinging, the legs are curled beneath the overhanging carapace, thereby shielding them from pred- ators. In this position S. latus is analogous to a and even the highly evolved triggerfish with its large pointed teeth has difficulty penetrating these morpholog- ical and behavioral defense mechanisms. However, the ventral surface of the lob- ster surrounding the legs exhibits soft, uncalcified membrane, If the leg is bitten off, the is vulnerable. It is not surprising, therefore, that in only few of the remains (complete enough to distinguish) did we find a hole in the dorsal surface of the carapace. A Red Sea triggerfish Pseudobalistes fuscus (reported as Balistes fuscus) dem- onstrates similar strategy by turning over its principal prey, sea urchins and at- tacking their more vulnerable ventral surface (Fricke, 1975). S. latus behaved similarly to spiny and clawed lobsters and initially assumed a defensive position using its ability to cling and its heavily armored dorsal surface as protection. They eventually gave up this defensive strategy and attempted to escape using their backward tailflip. The fact that they were tethered and could not flee very far might have predisposed these experimental animals to initially take this defensive strategy. However, the tendency of this species to sometimes cling instead of flee has been observed in the field (pers. observation, E.S.) and in the laboratory (Spanier et aI., 1991) with free animals. This scenario implies that once a predator has detected it, the lobster has two choices: (1) to swim and risk being flipped over and attacked on the more vulnerable ventral surface, (2) or to cling to the substrate and risk eventual puncture even to the dorsal portion of the exoskeleton. We conclude that S. latus has evolved at least five strategies against predation. They shelter, which we have shown is effective in enhancing survival. More specifically diurnal shelter residence and nocturnal foraging also enhance survival. However, during the migration period from June through February the lobsters leave their shelters and have been found in featureless terrain (Spanier et aI., 1988; Hardwick and Cline, 1990). In such circumstances, S. latus relies on its cryptic coloration to avoid predation. We commonly observed lobsters camouflaging themselves against rocks as did Ogren (1977) with S. nodifer. Finally, if detected BARSHAW AND SPANIER: BEHAVIOR OF SLIPPER LOBSTERS 381

by a predator lobsters have two behavioral choices: cling and depend on their passive defenses, or use their powerful tail flip and attempt to flee the predator.

ACKNOWLEDGMENTS This study was supported in part by the Aviezer Foundation and by grants from the Israeli Ministry of Absorption and the Israeli Ministry of Science. We thank S. Breitstein and Y. Tur-Caspa for their expert underwater assistance and P. Fabian for his all around help. D. Bryant-Rich, B. Ga]il, L. Fishelson, I. Karplus and D. Weihs provided helpful comments on the manuscript.

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DATEACCEPTED: March 22, 1993.

ADDRESSES: (D. E. B.)The Recanati Center for Maritime Studies, University of Haifa, Mount Carmel, Haifa 31905. 1srael; (E. S.) The Recanati Center for Maritime Studies and Department for Maritime Civilizations, University of Haifa, Mount Carmel, Haifa 31905, 1srael.