Drilling Intensity Varies among Neogene Tropical American Bivalvia in Relation to Shell Form and Life Habit

We calculated the incidence of drilling on bivalve genera from the Neogene fossil record of Panama and Costa Rica to determine differences in predation intensity among groups based on shell architecture, life habit, mobility, and taxonomic affinity. Bulk samples from 28 localities yielded >106,000 bivalve specimens, which were examined for characteristic drilling traces of muricid and naticid gastropods. We calculated the drilling intensity for the 90 most common genera, and characterized the size, ornament, life habit, and mobility for each genus. Large size confers considerable protection from drilling, but shell ornamentation does not. Life habit is strongly linked with drilling intensity. Epifaunal bivalves experience higher predation than infaunal bivalves and shallow burrowers experience higher drilling than deep burrowers. Mobility is also important for epifaunal bivalves; cemented taxa are twice as likely to be drilled as their uncemented counterparts. Our results suggest that bivalve behavior and life habits are more important than shell architecture for defense against drilling predators. Interactions between predators and prey have long been recognized as major drivers of community evolution and diversification (Darwin 1859, Dawkins and Krebs 1979, Vermeij 1977, 1983, Bambach 1983, Steneck 1983, Roy 1996, Thompson 1998). In the marine realm, escalation, or enemy-driven evolution (Vermeij 1987, 1994), appears to occur more often than does coevolution, or reciprocal evolution (Vermeij 1994, Kelley and Hansen 2001, Dietl and Kelley 2002). The response of molluscan prey to shell-damaging (durophagous) predators is particularly well suited to macroevolutionary studies of predation because of the abundant fossil record of mollusks and the potential for preservation of direct evidence of predation, especially traces such as drill holes and repair scars (Kowalewski 2002 and references therein, Alexander and Dietl 2003, Kelley and Hansen 2003). Several traits related to shell architecture and life habit are hypothesized to confer protection against predators (Vermeij 1977, 1983, Bambach 1983, Stanley 1988, Alexander and Dietl 2003, Kelley and Hansen 2003). Among bivalves, thick, robust shells and ornamentation such as spines, knobs, and crenulations of valve margins are thought to reduce the probability of a fatal attack by crushing or drilling predators (Stanley 1970, Logan 1974, Vermeij 1978, 1983, Bertness and Cunningham 1981, Kelley 1989, Harper and Skelton 1993, Smith and Jennings 2000, Kelley and Hansen 2001, Alexander and Dietl 2003). Organic rich laminae within bivalve shells (conchiolin) also appear to inhibit drilling and shell breakage (Harper and Skelton 1993, Kardon 1998). Rapid burrowing and the ability of some bivalves to swim by jet propulsion are also interpreted as adaptations to reduce predation. Epifaunal bivalves cemented to a hard substrate may be more difficult for predators to manipulate (Harper 1991). Still other bivalves may escape BULLETIN OF MARINE SCIENCE. VOL 89, NO 4. 2013 906 predation by boring into hard substrates, nestling (occupying crevices or holes abandoned by other organisms), burrowing deeply into the sediment, or camouflaging themselves with sponges or other encrusting organisms (Stanley 1970, Vermeij 1983, Harper and Skelton 1993, Alexander and Dietl 2003). These interpretations are compromised, however, because they are based largely upon experimental manipulations of bivalve shells and predators (Harper 1991, Smith and Jennings 2000) or are anecdotal. To address these problems, we used a large quantitative data set of fossil bivalve assemblages to calculate drilling intensities for 90 common genera in the context of data on shell architecture and life mode for the same specimens. Specifically, we tested the hypothesis that bivalves with smaller, less ornamented shells should experience higher predation than their larger, more highly ornamented counterparts. Secondly, we tested the hypothesis that bivalves that can move freely by deep/rapid burrowing or swimming should be drilled less often than bivalves that are epifaunal, cemented, or have otherwise reduced mobility.