J. <‘.YP,n~ur. Biol. Ecol., 1981, Vol. 50, pp. 213-230 0 Elsevier,‘North-Holland Biomedical Press CRAB SHELL-CRUSHING PREDATION AND GASTROPOD ARCHITECTURAL DEFENSE MARK D. BERTNESS Division of Biolo,q and Medicitle, Box G. Brobcw lJnirw.~i/~~. Providcwce, RI 02912, U.S.A. and CLIFFORD CUNNINGHAM Bio1og.r Department, Yale Utzivcr.sii~~, Nebt, Haven. C’TO65/l, U.S.A Abstract: The shell-breaking behavior of the crabs 0:iu.y verrec~uxri Saussure 1853 and Eriphia .squtmwta. Stimpson 1859 from the Bay of Panama is described. The master claws of both these crabs are well designed for breaking shells. Small shells, relative to the size of a crab predator, are crushed by progres- sively breaking off larger segments of a shell’s apex, while larger shells are peeled by inserting a large dactyl molar into the aperture of a shell and progressively chipping away the lip of the shell. Heavy gastropod shells are shown to be less vulnerable to crab predators than lighter shells, and narrow shell apertures and axial shell sculpture are demonstrated to be architectural features that deter crab predation. The incidence of architectural features which deter crab predation appears to be higher for smaller gastropod species than for larger gastropods which are too large for most crab predators. Large fish predators prey upon both gastropods and shell-crushing crabs. To avoid fish predators. both these prey groups seek refuge under rocks when covered by the tide. Fish predation thus appears to enforce a close sympatry between smaller gastropods and their crab predators. Shell-crushing predation by decapod crustaceans has been shown to be an important process in the evolution of shell (Kitching & Lockwood, 1974; Vermeij, 1976, 1977, 1978; Zipser & Vermeij, 1978) and crab claw design (Shoup, 1968; Vermeij, 1977). This coevolutionary relationship has been shown to vary latitudin- ally with heavier predation pressure by crabs in tropical latitudes (Vermeij, 1977. 1978), leading to heavier shells and shell armor in tropical gastropods (see Vermeij, 1978, for review). In addition, it has been suggested that interpopulation variation in the shell thickness of direct-developing littoral gastropods is correlated with the occurrence of predatory crabs, such that individuals in populations subject to heavy predation have thicker shells than conspecifics from populations where predation is not as severe (Bertness, 1977; Kitching & Lockwood, 1974). Teleost fish such as the spiny puffer fish (Diodon spp.) and smooth puffer fish (Arothron spp.) also prey upon shelled organisms by crushing them in their strong mouthparts or pharyngeal mills (Vermeij, 1978; Palmer, 1979). Palmer (1979) has shown that spines on some gastropod shells protect them from teleost predators 213 214 MARK D. BERTNESS AND CLIFFORD CUNNINGHAM and demonstrated that the occurrence both of shell-crushing fish and spinose shell sculpture increases from temperate to tropical seas. In the Bay of Panama, predation by teleost fish on littoral gastropods left exposed on open rock surfaces during high tide has been experimentally shown to be as high as 28’:b every 24-h tidal cycle (Bertness. 1980~). To cope with this extremely high predation pressure. littoral gastropods in the Bay of Panama and other tropical areas seek refuge under rocks or in fissures during high tide or avoid being covered by the incoming tide by always staying immediately above the water (pers. obs.). All shell architectural modifications used to escape from teleost predators appear to be related to reaching a size too large to be handled by fish. With the exception of extremely thick and heavy-shelled gastropod species, e.g. Thais mrlones, Diodon spp., are capable of crushing any shell that they are able to fit into their crushing mouthparts (unpubl. data). All littoral rocky shore gastropods that forage in the open in the Bay of Panama exposed to teleost predators are either large individuals that have escaped the brunt of fish predation because of their large size or are species that have spinose shell architecture which effectively increases their external dimen- sions (Palmer, 1979). Shell architectural features which appear to deter crab predators of gastropods are common in smaller snail species. Such features include narrow apertures, short spires, and axial ribbing (Vermeij, 1978) all features which have been postulated to hamper the effective handling of gastropod shells by the crushing claws of crab predators. These smaller gastropod species avoid fish predation by retreating to cryptic habitats during high tide (unpubl. data). In this paper the shell-breaking behavior of two tropical Eastern Pacific intertidal crabs on the most commonly available gastropod prey in their natural environment is examined. We describe different shell-crushing behaviors and the functional morphology of the crushing claws of the predators. Then we examine the vulnera- bility to predation of the sympatric gastropod species as a function of shell architectural form and the investment in shell material as a defensive measure. Finally. we examine the frequency of shell damage in shells worn by hermit crabs in the Bay of Panama to assess the success of shell architectural defensive measures in these gastropods. METHODS The predatory crabs Eriphiu squamata Stimpson 1859, and Ozius vwrecruxii Saussure 1853, were collected in rocky intertidal areas near the Smithsonian Tropical Research Institute Naos Marine Laboratory in the Bay of Panama from June to August 1978. Each crab was maintained in a separate shaded aquarium and its water was changed daily. To determine the largest shell each individual crab was capable of crushing for each of several gastropod species (critical size, sensu Vermeij, 1976) a wide size range of five to eight freshly collected shells occupied by hermit crabs was introduced to each predator. Hermit crab occupied shells were CRAB SHELL-CRUSHING PREDATION 215 used to standardize the availability of each shell type to the predators and to avoid the potential effects of differential gastropod behavior and palatability on the laboratory results. On each of the following 7 days or when no predation had been observed in 2 days, broken shells were removed and examined, and either all shells smaller than those broken were removed, or larger shells were added if the predator had broken the largest shell offered. Each individual predator/shell species size refuge determination required from 7 to 14 days to complete. Only shells which had no previous injuries or encrustations were used to avoid the influence of these variables on a shell’s vulnerability to predation. Each shell offered to the predators was measured to 0.1 mm with vernier calipers using columellar length as a size standard for all gastropod species examined except Nerifu ,fitniczduta. With N. firniculutu, aperture width was found to be a more reliable, replicable measure. During these tests, observations were also made on the feeding behavior of the crabs. In order to examine the critical shell sizes among shells that differ in shape, allometric relationships were determined for each gastropod species examined to convert the shell length measurements determined in the size refuge tests into shell weights and gastropod tissue weights. For each gastropod species, a wide size range of 20 to 30 individuals was collected and measured. The snails were then boiled and their tissues removed with forceps. The tissues and shells were then dried at 100 “C for 12 h and weighed to 0.001 g on an analytical balance. To experimentally test the antipredation value of the large terminal axial varices of Cunthurus ringens, size refuge tests were made with laboratory predators given both shells from which the varices had been artificially removed and normal (control) shells. The varices of experimental shells were removed with a grinding wheel to form a uniformly smooth-surfaced shell. Microscopic examination of the ground edge of altered shells indicated that the structure of the remaining shell material was not altered and that there was no structural difference between the removed and remaining shell material. Predator preference for gastropod or hermit crab occupied shells was determined by offering predators size-matched shells with either hermit crab or gastropod occupants. To prevent the gastropods from avoiding predators by moving above the water in the aquaria, the water level was kept at 5 cm and the inside wall of the aquaria was coated with an adhesive (Tanglefoot) at the water’s edge. To examine the influence of hermit crab occupation on the predation size refuge of a shell, critical size determinations were made on live Acunthinu hrevidentata, using the same experimental procedures and predators that had been used to determine the size refuge for Acanrhina shells occupied by hermit crabs. Field collections of hermit crab occupied shells were made at Culebra and Flamenco Islands, Panama and examined for the incidence of identifiable predator damage (see Bertness 1980a for the sampling methods used and for a description of the study areas). Shells which were badly eroded or encrusted with epiphytes 216 MARK D. BERTNESS AND CLIFFORD CUNNINGHAM could not be reasonably scored for injury and were not included in the final data analysis. THE SPECIES The crabs used in the laboratory predation tests, Ozius verreauxii and Eriphia squamufa, are the two most common shell-crushing intertidal crabs in the Bay of Panama (pers. obs.). Throughout the remaining text these two species will be referred to by their generic names. Ozius, a relatively large crab reaching sizes of C E F Fig. I. Shells of gastropod species used in the predation size refuge determinations: A. Planrrsk ~la~icosta~ff; B, Nerita fu~~icul~~~;C, Anuchis ,~uctuatff; D, Cerithium ‘~te~~u.~~~us~ar~rn~E, Ae~nt~li~~ brevide~t~ta; F, Ca~thurMsringens. CRAB SHELL-CRUSHING PREDATION 217 81.7 mm carapace width (Rathbun, 1930), is generally found in groups of 2 to 10 individuals under rocks at tidal levels from + 1 m to - I m.