Feeding Behavior of the Hawaiian Slipper Lobster, <I>Scyllarides Squammosus,</I> with a Review of Decapod Crustacean

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Feeding Behavior of the Hawaiian Slipper Lobster, <I>Scyllarides Squammosus,</I> with a Review of Decapod Crustacean BULLETIN OF MARINE SCIENCE, 41(2): 378-391, 1987 FEEDING BEHAVIOR OF THE HAW AllAN SLIPPER LOBSTER, SCYLLARIDES SQUAMMOSUS, WITH A REVIEW OF DECAPOD CRUSTACEAN FEEDING TACTICS ON MOLLUSCAN PREY Colin J. Lau ABSTRACT Despite the lack of a complex prey-opening apparatus, the non-chelate slipper lobster, Scylfarides squammosus, opens bivalves by a novel attack tactic known as "wedging." At least two variations of the wedging tactic have been observed: direct wedging and a patience attack. Direct wedging involves a simple insertion of the dactyli between the prey valves. A prying effect is achieved by the pulling of one valve by the second pereiopods in tandem, while the opposite valve is pressed outward by the first pereiopods. The third pair of pereiopods is used to scrape free the attachment of the bivalve adductor muscles. Opening by the patience attack involves the probing of cemented, sessile bivalves with the pereiopods accompanied by antennal flicking. After ascertaining the precise location of the edge of the shell, the pereiopods are held poised above the shell, plunged downward upon sensing the re-opening of the shell, wedging it open. A comparison of attack tactics used by decapod crustaceans includes a number of mechanistic solutions ranging from simple, mouth-oriented tactics to more complex functional morphologies and behaviors. Specialization in a behavioral tactic may be one method for increasing prey yield despite a limited investment in armament. The opening of bivalves by chelate predators usually involves the outright crushing of the shell (Ebling et al., 1964; Seed, 1969; Beal, 1983) or, depending on the strength of the claw relative to the thickness of the bivalve shell, chipping the outer edge of the bivalve until the soft body parts can be reached (Hughes, 1966; Seed, 1969). In some cases specialized chela morphology and shell-opening behavior are utilized: Shoup (1968) described the use of a tubercle on the chela of various species of the box crab, Genus Calappa, to "peel" the margin of gastropod shells. Dactylar teeth (tubercles) on the cutting edge of the claw of the mud crab, Scylla serrata, are specialized for the forcing open of mussels by exerting a shearing force along the plane of connection of the halves (Williams, 1978). Similarly, Du Preez (1984) examined the chela dentition of Ovalipes punctatus for the crushing, shearing, cutting, and grasping of mollusks. Non-chelate crustaceans which prey on bivalves have adopted alternate tactics for the opening of the shell. Panu/irus argus uses mandibles (Randall, 1964) in the place of a claw, to chip the edge of mussels and pen shells (Modiolus ameri- canus; Pinna carnea, Atrina seminuda respectively) and then remove the meat by scraping with the dactyli ofthe pereiopods. Similarly, Panu/irus homarus crushes the thin shell lip of the mussel, Perna perna, with its mandibles, then inserts the first walking legs to sever the adductor muscle of the bivalve (Smale, 1978). An investigation of the feeding biology of the Hawaiian slipper lobster, Scyllarides squammosus, indicated that bivalves of various species are eaten by this species. METHODS Observations were conducted in a semi-darkened room with 10-gallon glass aquaria and running filtered seawater (annual water temperatures 23° to 28°C). Light intensities were kept between <5 x 1012 - I X 10'4 Quanta sec-I cm-2 (QSL 100 Quantum Light Meter, Biosphericallnstruments, San Diego, California) since preliminary observations indicated that animals fed most readily under dark- 378 LAU: FEEDING TACTICS OF A SLIPPER LOBSTER 379 ened conditions during which the observer remained as motionless as possible. Ten S. squammosus were starved for a week, then presented with rocks upon which live oysters of the species, Ostrea sandvicensis, were attached (shell lengths 10 mm to 35 mm). This species firmly cements one valve to a hard substrate. After at least 15 min, S. squammosus used its walking legs to pry open the shells. Two other bivalve species, Isognomon perna and I. incisum, which attach themselves to rocks by means of byssal threads, were also used (shell lengths 20 mm to 54 mm). Each lobster was presented with a single bivalve during any observation period and a total of 25 feedings observed (2-3 feedings per animal). The beginning of a predation episode was marked by active searching by the lobster during which the pereiopods were held in spread fashion, probing the substrate, and the aesthetasc hairs of the antennae were flicked rapidly. The removal of the soft parts of a bivalve marked the end of a feeding episode. Episodes which did not result in the opening and consumption of the prey were not included. RESULTS The slipper lobster, Scylla rides squammosus, was observed to open three species of bivalves by two basic attack tactics and variations on the central themes (a third tactic is suggested by the presence of gastropod prey in the stomach contents of wild-caught lobsters). The bivalves opened in the laboratory were the oyster, Ostrea sandvicensis, and the toothed pearl shells, Isognomon incisum and I. perna. The general attack behavior involves a process of wedging the shells of the prey open by using the flaring dactyli of the first two pairs of pereiopods to pry apart the shell lips. The third pair of pereiopods were employed to sever the adductor muscles while the fourth and fifth pairs of pereiopods were used to brace both the bivalve and the substrate. Wedging Attack Tactics: Direct Wedging. - The first tactic observed on bivalves was termed a direct wedging attack. After probing the shell, dactyli were simply inserted into the bivalve. For bivalves cemented to the substrate, such as O. sandvicensis, this was often accompanied by a forward and backward rocking motion by the lobster as wedging progressed, presumably to take advantage of exhaustion of the tiring bivalve adductor muscle. As each pulse of pulls occurred, the dactyli wedged the shell open minutely further before the oysters' muscles could recover. The adductor muscles of the oyster worked against compression of the inelastic material of the dactyl. For the toothed pearl shells, I. incisum and I. perna, which live attached by byssal threads to the undersides of rocks, the lobster attempted to tum over the smaller rocks before pulling off the pearl shell. This was followed by a direct wedging attack (Fig. 1) or, if the lobster failed to insert the dactyli immediately, the shell was maneuvered so that the thin edges of the valves were facing the mouthparts. The mandibles were used to chip the edge of the shell until a suitable gap in the curving shells was obtained for the previously described wedging behavior. The first pereiopods were pressed outward from the lobster while the second and third pairs pulled the nearer valve inward toward the body of the lobster. As the first pair of walking legs were wedged progressively inward, the adductor muscle was usually severed by the dactyli of the second or third pereiopods, and the soft-bodied parts of the mollusk were lifted out and consumed. The attached adductor muscles were scraped from the shell by the dactyli of the first and second pereiopods. Wedging Attack: Patience Attack. - The second attack program involved an un- usual behavior associated with the opening of the well-attached O. sandvicensis, called here the "patience attack." This involved a surprise wedging attack preceded by probing the lip of the aperture with the dactyli of the first three pairs of 380 BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2, 1987 Figure I. The orientation and direction of movement of the pereiopods during the wedging of Isognomon incisum by the slipper lobster, Scylla rides squammosus. a) antennae are continually flicked up and down, b) the dactyls of the first pereiopods create a wedge which is forced in the lip of the shell, and the shell is pushed outwards, c) the second pereiopods pull the opposite valve toward the lobster, and d) the third pereiopods scrape the adductor muscle. pereiopods. The dactyli were then held poised 2 to 3 cm above the opening. Aesthetasc hairs were flicked as the antennae were moved downward over the edge of the bivalve, possibly sensing the release of metabolites by the oyster with the opening of the shell. After approximately 15 min the oyster re-opened and the lobster quickly, and quite suddenly, plunged the dactyli of its walking legs into the opening, wedged the valves open, and severed the adductor muscles. The soft parts of the oyster were then removed and consumed. Lengths of predation episodes ranged from 10 min to over 40 min and some- times resulted in the chipping of a bivalve without the entire animal being re- moved, although lobsters generally had a high attack success rate. A lobster was also observed to miss on its initial pounce during a patience attack, but opened the bivalve on the second attempt. DISCUSSION Interestingly, within the Gastropoda are certain snails which themselves employ a wedging technique in opening bivalves. Colton (1908) described the technique by which Busycon opens Mercenaria. The prey clam is grasped by the foot of Busycon and the shell margins are brought together. Busycon then forces the margins of the shells together until a chip results by contracting the columellar muscle. The crack between the prey valves is enlarged until the shells can be wedged by the conch's shell lip or the proboscis inserted so that body parts can be rasped away by the radula. In the molluscan version ofa waiting attack (Colton, 1908; Magalhaes, 1948; Menzel and Nichy, 1958), Busycon was observed to crawl on its prey, wait for the clam or oyster to open, and then thrust its own shell lip through an arc forcing the shell margins of the prey apart until the proboscis of LAU: FEEDING TACTICS OF A SLIPPER LOBSTER 381 the snail could be inserted.
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