BULLETIN OF MARINE SCIENCE, 41(2): 378-391, 1987

FEEDING BEHAVIOR OF THE HAW AllAN SLIPPER , SQUAMMOSUS, WITH A REVIEW OF DECAPOD FEEDING TACTICS ON MOLLUSCAN PREY

Colin J. Lau

ABSTRACT Despite the lack of a complex prey-opening apparatus, the non-chelate , 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 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 of the box , Genus Calappa, to "peel" the margin of gastropod shells. Dactylar teeth (tubercles) on the cutting edge of the claw of the mud crab, , are specialized for the forcing open of 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 , 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, , 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 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 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 ). The beginning of a 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 ). The bivalves opened in the laboratory were the , 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. Such tactics are not without risks; Colton (1908) and Paine (1962) observed that chipping of the attacking snail's shell, followed by shell repair, is not uncommon. A comparison offour common species of Hawaiian slipper lobsters reveals that the pereiopods of both Scyllarides squammosus and have es- pecially flaring dactyli that can be appropriate for wedging bivalve shells open and should have a higher mechanical advantage than other species with longer, more tapering dactyli. Aquarium observations have been made which show that S. haanii is also capable of wedging bivalves open. regalis and antarcticus have more tapered dactyli which seem to indicate that while these species may open bivalves, they are likely to possess a more generalized attack behavior. Observations made at the Waikiki Aquarium demonstrate thatA. regalis can open Isognomon perna by a similar kind of wedging attack; however, the time required to open a bivalve is typically much longer than for Scylla rides. In a 1968 paper on , L. B. Holthuis includes C. Lewinsohn's account of the opening of an approximately 10 cm long Tridacna by the described species, Scyllarides tridacnophaga. S. tridacnophaga manipulates the giant clam so that the dorsal surface from which the byssal thread attachments protrude is exposed. The lobster plunges it walking legs into this vulnerable part of the clam's anatomy causing the shell to gape. After turning the shell over, the pereiopods are inserted (Lewinsohn speculates that the adductor muscle or nerves may be injured) and remove the flesh to the mouthparts. In a more general context, bivalve wedging represents a novel approach to the age-old problem of gaining access to the nutritious part of a well-protected prey. Except for the mantis (Order Stomatopoda) which use subchelate ap- pendages to bludgeon or smash their prey open (Caldwell and Dingle, 1976), the majority of crustaceans that feed on shelled mollusks belong to the Order De- capoda. Table I summarizes the majority of decapod attack tactics for opening mollusks and groups them according to the primary orientation and relative efficiency of the attack mechanism involved. Many decapods employ more than one tactic, which depends on the prey species, and the animal may change attack tactics according to variability in prey morphology such as shell size, thickness, and aperture width.

Decapod Predatory Tactics for Opening Mollusks Swallowing Who/e.-One of the simplest tactics of decapod crustacean predation involves the animal engulfing its prey entirely. No specialized opening are required, but the prey must be small enough to be swallowed whole (intact or crushed completely by the mandibles). The amount of energy gained is likely to be limited due to the small prey size relative to the opening of the captor's mouth and because of the largely indigestible nature of the shell. Vermeij (1978) speculates that gastropods with tightly-fitting apertures may even foil such pred- ators-perhaps by resisting complete digestion. Several complete molluscan re- mains were observed in the stomach contents of in a related study (unpublished data), but they consisted mostly of gastropod shells with a large aperture or prey with little protection of the viscera from exposure (such as , nudibranchs, and chitons). Chipping/Biting. - The mandibles are used to create access to the soft parts of a bivalve (or gastropod) by reducing the edges of the shell to cause a gap. The use of mandibles to chip the edges of bivalve and gastropod shells was postulated by Randall (1964) who saw the remains of these shells in association with spiny lobsters (). Heydorn (1969) found that lalandii opened mus- 382 BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2, 1987

Table I. A comparison of decapod crustacean attack tactics in opening mollusks

Relative Relative handling Structural prey size Tactic Description Orientation lime investment (to predator) Swallow Devour prey completely Mouth short low small whole Chipping! Mandibles aid in chip- Mouth moderate low med. biting ping edge of shell Bivalve Bivalve shell wedged Dactyl short to low med. wedging open with dactyli, ad- moderate ductor muscle cut Prying Dactyli of first pereio- Dactyl moderate low med. pods used to pull valves apart Opercular Gastropod soft parts re- Dactyl moderate moderately med./large wedging! moved without break- low blocking ing shell by holding operculum open, scooping out soft tis- sues, pulling out body Crushing out- Chela used to break Chela short high med./large right shell entirely open Chipping! Chela breaks off edges of Chela long moderate med./large peeling shell to expose muscle and soft tissues. U su- ally follows failed crushing attempt Boring Chela bores through Chela tip long moderate med. hinge Tubercular Dentition on chelae spe- Chela tuber- long moderate med./large peeling cialized for peeling or cles chipping Shearing Chela tubercles exert Chela tuber- short moderate med. shearing force along c1es plane where valves meet

sels by chipping the wide end of the shell with the mandibles and then using the first pereiopods to pull the shell apart and consume the soft parts. Berry (1971) observed Perna perna being chipped by Panu/irus hamarus, following which the first walking legs were used to "lever" open the mussel. Hickman (1972) described captive opening Ostrea lutraria although it was concluded (pos- sibly erroneously) that oysters were probably not important diet items to this lobster species since fewer lobsters were being dredged by oystermen than pre- viously. Herrnkind et al. (1975) states that Panu/irus argus can open shells such as Fascialaria by biting the shell edges progressively with the mandibles. Elner and Jamieson (1979) found that juvenile Hamarus americanus used their man- dibles on the hinges of the scallop, Placapecten magellanicus, The fast-growing, thin edges of such mollusks are broken off until the soft parts are exposed. This tactic appears to be an alternate form of the "chipping or peeling" tactic by clawed predators. Bivalve Wedging. -A low degree of specialization of appendages is required for this tactic which most often leaves the shells of the bivalve intact. Flaring, tri- angular-shaped appendages are used to progressively widen the gap between valves. Variability in effectiveness of this tactic is apparently related to the degree of LAU: FEEDING TACTICS OF A SLIPPER LOBSTER 383

simple ------) complex

Opercular Wedging

Chipping/Biting Chipping/Peeling ~o ~'{J

~~ Pry ing Boring

Shearing Swallow Whole Crushing Outright

Bivalve Wedging

Figure 2. A comparison of complexity of attack tactics.

tapering of the dactyli of the appendages in question. As previously described in this study, variations in attack programs exist which are dependent, in part, upon the morphology of bivalves and type of attachment to the substrate. S. squam- mosus attempts direct wedging upon encountering bivalve prey, but may quickly switch to a chipping (biting) by mandibles tactic and back to wedging in the case of bysally attached, thin-shelled species of Isognomon. While attacking cemented bivalve species such as Ostrea. the direct wedging tactic can be replaced by the patience (surprise) attack. Even though chemosensory data were not studied, it is probable that antennal flicking is instrumental in sensing the opening of the bivalve and concomitant release of metabolites. Palmer et al. (1982) have speculated that increased closure times in sessile prey are an adaptation to avoid predation by decreasing release of such chemosensory cues. The wedging tactic represents a change in orientation from a mouth-oriented approach toward a thoracic -based attack. While the mouthparts are still useful in probing and manipulating prey, the actual initial opening is effected by the pereiopods which are associated with increasingly complex behavior (Fig. 2). Prying. - Both chelate and non-chelate predators have been described pulling apart the shells of bivalves by inserting the dactyli of the first pereiopods and prying the valves apart. Menzel and Nichy (1958) described a prey probing behavior of the blue crab, on oysters (Crassostrea virginica) in the field, during which mostly small oysters were tested by pinching until "a weak or gaping" oyster was found and "pried and pinched open." Later observers working with the same species described other tactics but did not observe this. Evidently, the 384 BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2, 1987 incidence of this type of tactic may be low depending on species examined. In feeding trials, Liocarcinus puber pried open Mytilus edulis in about 1% of cases observed, by "insertion of the dactyli of both chelae between the valves" (ap Rheinallt and Hughes, 1985). In contrast, pried open M. edulis in 20% of attacks observed in the laboratory (Cunningham and Hughes, 1984). Besides wholesale crushing of bivalve shells, another portunid, Ovalipes punc- tatus, opened the clams, Donax serra and D. sordidus, by "prising the valves apart" by first forcing one finger of a chela between the valves to bore by pivoting the dactylar tip at the ventral margin and then inserting the finger of the other chela and pulling the valves apart (Du Preez, 1984). A third variant of the prying tactic used by O. punctatus involved inserting one or both fingers of the chelae into the siphon openings and then prying the shells apart. Paterson (1968) observed the , , pulling open small mussels (Aulacomya magellanica) in aquaria by facing the posterior end and dorsal surface of the shell toward the lobster's mouth and inserting the dactyli of the first pereiopods between the lower edges of the shell valves and pulling them apart. The second pereiopods sometimes were utilized in pulling the valves apart and removing parts of the posterior adductor muscle and mantle. Spiny lobsters sometimes combined the chipping/biting and prying tactics to open mussels (see "chipping/biting"-Heydom, 1969; Berry, 1971). Jasus lalandii used its man- dibles to crack open the umbonal end of the congener, A. ater, and pry apart the remaining shell until the soft parts could be removed by the maxillipeds (Pollock, 1979). While these observations resemble the bivalve wedging procedure to some degree, the notable differences between bivalve wedging and prying tactics include (1) pairs of pereiopods working in concert rather than opposition, (2) the initial attack differs in how the insertion of appendages within the gape is accomplished, and (3) the objective of shell insertion is merely to hold the shell wide enough to allow severance of the adductor muscles while in the prying tactic this is done to lever the valves apart. Although limits may be predicted to the maximum size of bivalve prey that may be opened in this manner, it appears to be an alternative tactic to lip-chipping or crushing and a refinement of the wedging tactic by slipper lobsters. In fact, all predators listed as examples of this tactic were observed to use at least one other tactic (either chipping or crushing prey). While the dactylar shape must limit the kinds of prey the animal is capable of opening, a different set of muscles is used than for those needed for crushing. As a tactic, prying open is time-consuming since the initial opening of the shell by the dactyl may be difficult to accomplish. The shells of smaller bivalve prey are sometimes broken off while prying, neces- sitating the removal of shell fragments piece by piece (Du Preez, 1984). Opercular Wedging/Blocking. - Vermeij (1978) described a predatory tactic which leaves the gastropod shell intact. The actual mechanism of removal involves some method of preventing the closure of the operculum. An appendage such as a cheliped is used to block the operculum by grasping the body behind the operculum (as with Pachygrapsus crassipes on Tegulafunebralis-Hiatt, 1948) or by wedging the operculum open (Synalpheus fritz muelleri on the coral-associated gastropod Coralliophila caribaea-Goldberg, 1971; Pagurus novae-zealandiae on Turbo smaragda and Melagraphia methiops-Greenwood, 1972) while the second che- liped is free to pick at the exposed body tissue. The importance of the operculum in resisting predation cannot be too highly stressed. Ebling et al. (1964) and later Kitching et al. (1966) described the attempts of Carcinus maenas and Liocarcinus (=Portunus) puber to pull Nucella (=Thais) LAU: FEEDING TACTICS OF A SLIPPER LOBSTER 385 lapillus from its shell. These observations were described as an alternate tactic, with a limited success rate, to that of crushing the shell. Gibson (1970) concluded that the chief function of the operculum in N. lapillus is as a defense against crab predation rather than to prevent desiccation since C. maenas ate whelks most readily when opercula were experimentally removed. Shepherd (1973) recorded the scooping out of juvenile abalone, Haliotis roei, by the grapsid, Plagusia chabrus which lives in the same crevice habitat of the abalone. Despite the abalone's lack of an operculum, the mode of removal of the soft parts while leaving the shell intact is similar enough to warrant categorization with other wedging tactics on gastropod opercula. The remaining predatory tactics require the possession of a claw (chela or cheliped). This represents an investment (in some cases a major expenditure) of chemical energy and mineral resources into a versatile structure for obtaining food and for other uses. To some extent, the remaining tactics also represent a continuum in complexity of behavior resulting from an economy in structure. The degree of success in finding and opening an optimal size of prey is proportional to the amount of "allocation" of resources (e.g., large claw-large prey) as well as a favorable disposition of materials (e.g., specialized structures). Crushing Outright. -One of the most powerful and basic of these attack tactics is to simply crush the shell of the prey. The force exerted by the chela exceeds the compressive strength ofthe shell, cracking it, and allowing the predator access to the soft parts. To differentiate this from other tactics, outright crushing is defined here as the reduction of the major structural components of the shell by direct and immediate breakage. Brachyuran examples of this tactic abound: Menippe mercenaria finely fragmented Crassostrea virginica (Menzel and Nichy, 1958), Carcinus maenas, Cancer pagurus, and Liocarcinus (=Portunus) puber all broke open both Mytilus edulis and Nucella (=Thais) lapillus (Ebling et at, 1964); Scylla serrata crushed Trichomya hirsuta (Williams, 1978), Carpilius maculatus, Car- pilius convexus, Eriphia sebana, Daldorfia horrida, and Cancer oregonensis all crushed various gastropods (Zipser and Vermeij, 1978); and Homarus americanus both cracked open Placopecten magellanicus (Elner and Jamieson, 1979), Ca/linectes sapidus broke open Geukensia demissa (Hughes and Seed, 1981), and Ovalipes punctatus crushed both mussels and gas- tropods (Du Preez, 1984). Even the snapping shrimps, Alpheus heterochaelis and Alpheus normanni, can crush small Mercenaria mercenaria (Beal, 1983). Elner (1978) described the attempts by Carcinus maenas to crush small « 1.0- cm length) Mytilus edulis outright. As prey became larger (1.0-3.0 cm length) the crab selected the umbonal region for its crushing attempts. Failing that, the pos- terior edge of the shell was crushed over the adductor muscle. With increasing size of the mussel, Geukensia demissa, Callinectes sapidus switched tactics from outright crushing to umbone-oriented attacks to edge-chipping (Seed, 1980; 1982). In aquaria, Seed (1969) observed Carcinus maenas attempting to crush the pos- terior region before attempting the umbone. Cancer pagurus also crushed Mytilus but both claws were used to crush simultaneously as Zipser and Vermeij (1978) had also observed with the congeners Cancer productus and Cancer oregonensis. Ability to crush the prey is determined in part by the relative sizes of predator chela and prey shell. Brachyuran claws are commonly dimorphic (Vermeij, 1977) with a master (crusher) chela and a smaller (cutter) chela. The master chela is appropriately massive and often armed with molariform teeth for crushing, while the smaller chela is equipped with cutting teeth for holding, manipulating, and sawing the muscle of the prey. The respective musculature allows for a slow but powerful force being delivered by the master chela and a quick but less forceful 386 BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2, 1987

closure by the cutting chela (Warner and Jones, 1976; Elner, 1978). Warner and Jones also found that with rapid capture apparatus (e.g., claws of port unids) used to catch fast-moving prey have a low mechanical advantage and relatively shorter sarcomere lengths than crabs with heavy, crushing chelae (e.g., Cancer pagurus), which have a higher mechanical advantage and longer sarcomere lengths. They noted, however, that such portunid claws possessing a tooth midway on the dactylus of the chela could significantly increase the mechanical advantage at such a point (as is the case with such crabs as Calappa which are categorized with the tubercular peeling tactic). Of five observed breakage patterns on Littorina rudis by Liocarcinus puber, the tactic most commonly employed involved crushing across the base of the shell. This was usually initiated by punching a hole through the center of the shell lip with teeth located midway along the dactyl of the chela (ap Rheinallt and Hughes, 1985). The morphology of the prey is a second consideration in the ability to crush prey outright. Vermeij (1978) explains that shell morphology is in part a function of chemical limitations in the composition of molluscan calcium carbonate (i.e., calcite/aragonite content) is affected by latitudinal temperature differences. Such characteristics as a narrow-sized or toothed aperture, short spire length, increased shell thickness, structural reinforcement and complexity (strong external sculpture) of the shell are predation resistant features (Vermeij, 1976; 1979) and the inter- active results of selection by predators overlaying the form constraints dictated by chemical composition and temperature. Harger (1972) observed that smooth Mytilus edulis shells pop out of a crab's claw more readily than in attempts to break the thicker but ridged shell of M. calljornianus. The "degree of inflation" was identified as a determinant in the degree of vulnerability of a bivalve (Boulding, 1984). Similarly, large periwinkles (Littorina rudis) were difficult for Liocarcinus puber to handle because of the wide gape of the chela required and the slippage of dactylar teeth over the round, smooth surface of the shell (ap Rheinallt and Hughes, 1985). Another consideration in success rates of crushing (and peeling) attacks involves the presence ofepifauna on the shell of the prey. Menippe mercenaria was deterred from predation on hydroid-colonized shells. When the potential prey was brought to the mouthparts of the crab, the crab reacted as if stung and promptly released the shell (Brooks and Mariscal, 1985). The possession of an effective food capture structure (e.g., claw or other ap- pendage) has a similar cost for the crustacean predator. Energy and mineral content may be important to maintaining the structure of these appendages. Compromises in size and structure are often made in Vermeij's "arms race" and are directly related to the existence of other crushing variations and tactics employed by a predator. Moreover, an optimal-sized prey exists from an energetic standpoint when prey are able to avoid being eaten by outgrowing their potential predators and making handling time prohibitive at either end of the size range. ap Rheinallt and Hughes (1985) found that ingestion time was commonly the rate-limiting step for all but the largest prey and may be directly related to mouthpart and stomach size of the predator. With Nucella lapillus, Hughes and Elner (1979) indicated that the energy gained per unit handling time by Carcinus maenas increased for very small whelks to moderate-sized whelks beyond which handling time became too costly in at- tempts to break large whelks. ap Rheinallt (1986) noted that very small Mytilus were suboptimal for Liocarcinus puber because they involved considerable dex- terity for handling and were frequently dropped or failed to evoke a grasping LAU: FEEDING TACTICS OF A SLIPPER LOBSTER 387 attempt at all. Gleaning the flesh from the crushed shell was often time-consuming for the crab, and the assumption may be made that volume considerations alone will limit the amount of prey that can be consumed by swallowing both shell and flesh. Hughes and Elner (1979) also found that crabs had different optima de- pending upon whether whelks from exposed coasts (which possessed a charac- teristically thinner shell, larger aperture) or protected coasts (areas in which crabs also occurred) were eaten. But Cancer pagurus was found to persist in handling and damaging large gastropod prey despite a low attack success rate, thus causing Lawton and Hughes (1985) to conclude that a passive mechanical selection rather than an active behavioral selection of prey size was involved. Thinner-shelled prey can presumably be easier to handle and puncture than thicker-shelled gastropods from crab-inhabited areas. Carcinus maenas broke open allopatric whelks from the crab-free open coast with relative ease compared to that of Nucella from crab-infested waters (Ebling et a1., 1964; Kitching et aI., 1966). Similar experimental paradigms have yielded comparable results. In lab tests Hemigrapsus edwardsi, preying upon Lepsiella albomarginata and L. scobina, crushed the thinner-shelled whelks from areas without crabs (Kitching and Lock- wood, 1974). Periwinkle shells (Littorina littorea) from areas north of Cape Cod were thinner and more vulnerable to crushing by Cancer borealis than periwinkles from the south (although Dudley (1980) inferred that water temperature was the probable reason for differences in shell thickness between regions). However, the employment of more than one attack tactic does not always imply an ordered attack program unless such attack tactics are inherently size-related. Depending on its ability to achieve an immediate breach in the shell defenses, crabs (notably Carcinus maenas-Elner, 1978) employ alternate attack tactics in opening prey. The crab often exhibits trial and error behavior, moving from one attack tactic to the next. Carcinus, after attempting to crush Mytilus and failing to do so, will attempt to chip the lip of the shell. For large mussels, the crab attempts to bore through the shell at the hinge ligament using the lower dactylus of the master chela. The phases of these trial and error attacks are largely size- related. However, Blundon and Kennedy (1982) found that failure load testing on four regions of the shell of Mya arenaria indicate that the region of the umbo was significantly stronger than other shell areas. Yet Elner (1978) found Careinus directly focussed its attack on this region on larger mussel shells.

ChippingIPeeling.-Chipping the edge or lip of molluscan shells is a common tactic used when prey are not readily crushed. This time-consuming method involves the use of a chela to peel the thin, expanding edge of the shell to expose the viscera or adductor muscle of the prey. The main benefit of this tactic is that by proper placement of the chela on the shell, larger prey can be opened than with a crushing attack alone. This may represent a kind of compromise in energy and material investment since neither an extremely large nor specialized master claw is needed. The amount of handling time also increases since the ratio of the area of the actual crushing edge ofthe claw (on the expanding area of shell growth) to the accessible area of the viscera, must decrease for this method. In the laboratory, Chapin (1968) observed Pachygrapsus crassipes chipping the edge of the shell of Acmaea and pinching the flesh of the mantle. Elner (1978) records the lip-crushing of Carcinus maenas on Mytilus edulis, Krantz and Cham- berlin (1978) describe the opening of oysters by Callinectes sapidus, Boynton (1979) records the edge-chipping attack of Carcinus maenas on Littorina littorea, Elner and Jamieson (1979) list lip-chipping as one of the attack methods of Cancer irroratus on Placopecten magellanicus and Du Preez (1984) includes edge-peeling 388 BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2, 1987 as an attack behavior of Ova/ipes punctatus on the snail, Bullia sp. The edge- peeling behavior of Callinectes sapidus on large specimens of Geukensia demissa created access to the adductor muscle for severance by the chelipeds (Hughes and Seed, 1981; Seed, 1982). Vermeij and Veil (1978) believe that a biogeographical pattern exists in bivalve form such that the gape between the posterior edges of shells decreases equatorward. Shell closure becomes emphasized as predation intensity increases toward the equator. Chipping probably represents the major shell opening method affecting the size of the gape. Boring. -An unusual method of opening large mussels was described by Elner (1978) in which the crab, Carcinus maenas, used the tip of its chela to bore a hole at the hinge of Mytilus edu/is and enlarge the hole by using the teeth on the chelae. Eventually the adductor muscle was exposed and severed by the chela. In compensating for "inadequate" equipment, experience is likely to be of paramount importance to proper employment of this tactic. Tubercular Peeling. -Shoup (1968) states the classic case ofa specialized structure (a tubercle) opening prey by peeling. Box crabs of the Genus Calappa possess a protruding tubercle on the dactylus which fits into a depression on the propodus. The tubercle is instrumental in chipping off small pieces in the edge of gastropods. By placing the leading edge of the shell over the depression, the tubercle can smash through the shell. Such a tactic requires a relatively low investment in materials, since the efficiency of use is increased to compensate for lack of heavy armor and the accompanying musculature. But the effect ofloss of the specialized appendage (e.g., by autotomy) may be especially debilitating to efficiency in food procure- ment. While Hamilton (1976) observed that the largest molar tooth of the crushing claw of Callinectes sapidus was used to crush the body whorl of the snail, Littorina irrorata, by inserting the tooth in the shell aperture after orienting the shell, it was also noticed that individual differences in opening behavior occurred. Ver- satility in opening tactics may compensate for a lesser degree of specialization in claw tubercles. The variety of tactics employed may indicate that the tubercles of Callinectes are not as advanced as the efficient but uniform method of opening of prey of Calappa. The degree to which C. sapidus regenerated dimorphic chelae was also examined (Hamilton et al., 1976). Crabs with two cutter claws were not uncommon and subsequent changes in handedness (laterality) of the crusher from the right side to the left side frequently occurred. Crabs lacking the specialized crushing chelae could apparently function with little loss in food procuring ability. Conversely, use of a presumably unsuitable appendage in a specialized role in- dicates that a degree of compensatory plasticity (Reese, 1983) may be occurring. A combination of the edge-chipping and tubercular peeling tactics were used in sequence on the oyster. Both mud crabs, Panopeus obesus and P. simpsoni, opened Crassostrea virginica by chipping the edges of the valve with the major chela until an opening was formed that enabled the fingers of the major chela to be inserted. The basal tubercle of the dactyl was used to repeatedly crush one of the valves until the soft parts were exposed (Reames and Williams, 1983). Pan- opeus herbstii crushed smaller C. virginica but chipped the edges in unsuccessful attempts to open larger prey (McDermott, 1960). The crabs Ozius verreauxii and Eriphia squamata which open large shells by inserting a large dactylar molar into the shell of the aperture and progressively chipping away at the lip of the shell (Bertness and Cunningham, 1981) can be considered examples of an intermediate degree of specialization compared to the lever arm created by the tubercle of Calappa. Yet tubercular peeling is not always LAU: FEEDING TACTICS OF A SLIPPER LOBSTER 389 especially effective: Vermeij (1982) observed that the highly specialized shell- opener, Calappa, had a high percentage of unsuccessful attacks. A thickened outer lip and varices prevented lethal peeling, and snails often repaired their shells following such attacks. The scars left by such shell repair did not affect shell strength (Blundon and Vermeij, 1983). Shearing. -An advanced molluscan attack tactic is described from Scylla serrata on the bivalve, Trichomya hirsuta, by Williams (1978). The mussel is manipulated between the larger of the two chelae and the tubercles used to exert a shearing force along the plane of contact of the bivalve, thus allowing the displaced, opened shells to be manipulated and body parts rapidly gleaned by the mouthparts. While the rapidity ofthis technique must be impressive, it also brings to mind that some degree of development of the claw musculature must be present to allow sufficient force to be exerted. Also, Vermeij (1978) suggests that certain bivalves may possess defensive morphology against such shear forces: plicate, crenulate or interlocking valve margins; complex hinge dentition; a well-developed adductor muscle and a strong hinge ligament. In general, decapod attack tactics on mollusks can be divided into those in which no chela is required: swallowing whole and chipping/biting; the presence or absence of a chela: opercular and bivalve wedging, prying; and those for which a chela is strictly required: outright crushing, chipping/peeling, tubercular peeling, boring, and shearing. Complex attack behavior or specialized structures appear to compensate for lack of overwhelming attack mechanisms.

ACKNOWLEDGMENTS

I am grateful to Dr. E. S. Reese for use of facilities at the Hawaii Institute of Marine Biology. Drs. J. Bailey-Brock and W. J. Walsh made useful comments on the manuscript. I would also like to thank the Waikiki Aquarium and the Coral Foundation. This work represents part of a thesis submitted in partial fulfillment of the requirements for the M.Sc. dcgree at the University of Hawaii.

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DATEACCEPTED: December I, 1986.

ADDRESS: Department of Zoology, 2538 The Mall, University of Hawaii, Honolulu, Hawaii 96822.