Gregory P. Dietl

The Fossil Record of Shell-Breaking Predation on Marine Bivalves and Gastropods

Any treatment of durophagous (shell-breaking) predation on bivalves and gastropods through geologic time must address the molluscivore’s signature preserved in the victim’s skeleton. Pre-ingestive breakage or crushing is only one of four methods of molluscivory (Vermeij, 1987; Harper and Skelton, 1993), the others being whole-organism ingestion, insertion and extraction, and boring. Other authors in this volume treat the last behavior, whereas whole-organism ingestion, and insertion and extraction, however common, are unlikely to leave preservable evidence. Bivalve and gastropod ecologists and paleoecologists reconstruct predator-prey relationships based primarily on two, although not equally useful, categories of pre-ingestive breakage, namely lethal and sublethal (repaired) damage. Peeling crabs may leave incriminating serrated, helical fractures in whorls of high-spired gastropods (Bishop, 1975), but unfortunately most lethal fractures are far less diagnostic of the causal agent and often indistinguishable from abiotically induced, taphonomic agents of shell degradation.

Post-Miocene Shift in Stereotypic Naticid Predation on Confamilial Prey from the Mid-Atlantic Shelf: Coevolution with Dangerous Prey

Abstract Of More than 4000 specimens of the naticid gastropods Euspira heros (Say) and Neverita duplicata (Say) from southern New Jersey, the lower Pleistocene of North Carolina, upper Miocene of Maryland, and the lower Miocene of Delaware, subsamples with complete and incomplete boreholes (n = 613) were compared for borehole-site stereotypy, prey size-selectivity, prey profitability, and prey effectiveness. In confamilial encounters, adaptation of naticid predators is evidenced by a shift in borehole-site stereotypy on the body whorl toward the umbilicus during the last 18 my, particularly for N. duplicata. Inferentially, an umbilical drilling position enabled the base of the predators foot to occlude the prey aperture and prevent egress of the dangerous preys foot, thereby reducing the preys escape potential. The tradeoff was that the umbilical site required the predator to drill through a thicker shell location. Prey effectiveness, the ratio of incomplete boreholes to total attempts, was initially low (0.03) for both species in the lower Miocene, but increased appreciably from the Pleistocene to the Recent for N. duplicata (0.32). Such increase in successful prey escape indirectly may reflect prey adaptation since the Miocene. Cost/benefit curves, i.e., log of the ratio of apertural lip thickness /internal shell volume regressed on whorl diameter (WD), have significantly greater negative slopes for Miocene versus Recent conspecifics. Lower cost/benefit ratios for successive size classes of modern naticids suggest that confamilial prey have become increasingly profitable molluscan options as they increased in size, despite increased risk of fatality to the predator. Decreasing naticid prey size-selectivity, as evidenced by lower regression correlation coefficients since the Miocene, reflects increasing mismatches between predator and prey size. Outcomes of size mismatches in predatory encounters between E. heros and N. duplicata were not predictable necessarily given potential differences in species agressiveness and foot size. This unpredictability fueled coevolution between these cannibalistic moonsnails and their dangerous intraspecific and interspecific prey.

Shell Repair Frequencies in New Jersey Bivalves: A Recent Baseline for Tests of Escalation with Tertiary, Mid-Atlantic Congeners

Abstract Articulated and disarticulated shells of Anadara ovalis, Anomia simplex, Argopecten irradians, Astarte castanea, Crassostrea virginica, Divalinga quadrisulcata, Donax variabilis, Ensis directus, Geukensia demissa, Mercenaria mercenaria, Mya arenaria, Mytilus edulis, Petricola pholadiformis, Spisula solidissima, and Tagelus plebeius collected from New Jersey intertidal life and death assemblages were measured, and the frequency, type (scalloped, divoted, cleft, embayed), location (ventral, anterior, posterior), and shell size at inception of repair determined. Repair frequency ranges from zero (D. quadrisulcata) to 0.30 (M. arenaria). Size refuge from sublethal breakage was attained by S. solidissima and C. virginica. Posterior repairs necessitated by siphon-nipping characterize M. mercenaria and E. directus. Ventral repairs associate with species subjected to valve-wedging (S. solidissima, M. mercenaria) or with ventral egress of the foot (A. ovalis). Ventral repairs among deep infaunal clams (M. arenaria, E. directus, T. plebeius) may have been induced by sediment-loading stress during burrowing. Anterior repairs are characteristic of deep infaunal species with foot exposure (M. arenaria, T. plebeius). Repair frequencies were compared statistically with valve surface area, ventral margin thickness, burrowing rate, depth of sediment penetration, shell microstructure, shell ornament, and tissue exposure when valves adducted. Of these comparisons, the only significant correlation was between frequency of embayed repairs and valve surface area. The complex relationship between repair frequency and these variables is underscored by factor analysis. New quantitative approaches are employed that advocate phyletic rather than assemblage-level tests of escalation involving Tertiary congeners from the Atlantic Coastal Plain.

Crab scars reveal survival advantage of left-handed snails

Biological asymmetries are important elements of the structure and function of many living organisms. Using the Plio–Pleistocene fossil record of crab predation on morphologically similar pairs of right- and left-handed snail species, we show here for the first time, contrary to traditional wisdom, that rare left-handed coiling promotes survival from attacks by right-handed crabs. This frequency-dependent result influences the balance of selection processes that maintain left-handedness at the species level and parallels some social interactions in human cultures, such as sports that involve dual contests between opponents of opposite handedness.

Mid-Paleozoic latitudinal predation gradient: Distribution of brachiopod ornamentation reflects shifting Carboniferous climate

Shell ornamentation in modern oceans increases toward the tropics in conjunction with an equatorward increase in shell-breaking predation. Latitudinal gradients in antipredatory ornamentation were previously documented for Devonian brachiopods. We examined the latitudinal distribution of shell ornamentation in Tournaisian, Visean, and Namurian articulate brachiopods to test the hypothesis that the latitudinal gradient in antipredatory ornamentation was present in the Carboniferous. We found a statistically significant latitudinal ornamentation gradient, which was most pronounced in the Tournaisian, when the latitudinal temperature gradient was most steep. These results support the hypothesis that a latitudinal gradient in defensive morphology occurred as a result of the mid-Paleozoic increase in predation. Although the mid-Paleozoic and late Mesozoic intervals of predator-prey escalation may have differed in dynamics and intensity, both episodes produced adaptations in prey morphology that varied along a latitudinal gradient.

Can Naticid Gastropod Predators Be Identified by the Holes They Drill

We tested the hypothesis that drillholes made by different species of predatory naticid gastropods can be differentiated by variability in the inner (IBD) and outer borehole diameters (OBD) of the holes they drill. We compared two samples of Mya arenaria that were drilled by different predators, Euspira heros and Neverita duplicata, under experimental conditions. Mean IBD:OBD ratio was significantly greater for holes drilled by Euspira compared to Neverita, indicating that Euspira drills a steeper drillhole than Neverita. We also found consistent differences between the two naticids for slopes of regression lines of IBD on OBD after standardization for predator size and prey size and thickness, with slopes for Euspira being steeper, but results were not statistically significant. However, the range of IBD:OBD ratios was wide and overlapped considerably for each species, which decreases confidence in assignment of individual drillholes to a particular predator species. At least in the case of these two naticid species, interspecific differences in variation of the inner and outer diameters of the holes they drill have limited utility in identifying the maker of individual boring traces in the fossil record.

Interaction strength between a predator and dangerous prey: Sinistrofulgur predation on Mercenaria

Abstract The lack of direct empirical evidence of predator evolution in response to prey adaptation is a fundamental weakness of the arms race analogy of predator–prey coevolution. I examined the interaction between the predatory busyconine whelk Sinistrofulgur sinistrum and its bivalve prey Mercenaria mercenaria to evaluate whether reciprocal adaptation was likely in this predator–prey system. Thick-lipped whelks use their shell lip to chip open the shell of their prey, often resulting in breakage to their own shell. Thus, hard-shelled prey, such as Mercenaria , may be considered dangerous because they are able to inflict damage to the predator as a consequence of the interaction. The strength of interaction between whelks and their bivalve prey was viewed by regressing predator performance (the incidence of shell breakage in encounters with prey) on prey phenotype (a function of size). Interaction with Mercenaria of varying sizes has strong and predictable consequences ( r 2 =0.946; p =0.028) for Sinistrofulgur . Predators that select large, thick bivalve prey increase the likelihood that their shell lip will be broken in the process of attempting to open their prey. Ecological consequences of feeding-induced breakage may include reduced growth rate, reproductive success, and survivorship. These results suggest that natural selection should favor predator phenotypes that reduce feeding-induced breakage when interactions with damage-inducing prey occur.

Traces of Naticid Predation on the Gryphaeid Oyster Pycnodonte dissimilaris: Epifaunal Drilling of Prey in the Paleocene

Traces of drilling predation by naticid gastropods were observed on 51 valves of the free-lying, semi-infaunal oyster Pycnodonte dissimilaris (Gryphaeidae) from the Paleocene Hornerstown Formation, in New Jersey. Stereotypic behavior of the predator is indicated by the highly constrained placement of drill holes, 94% of which are centrally located on the oyster shells. Predator—prey mismatches in size, involving small predators that drilled through the upper valves of relatively large oysters, are documented by comparison of outer borehole diameter, as an index of predator size, with the sizes of the oyster shells. Results of this analysis suggest that at least some prey were drilled epifaunally, as they were too large to be manipulated and buried by the predator. This indicates, together with reports of epifaunal drilling by living naticids, that such behavior is geographically and stratigraphically more widespread in the Naticidae than has previously been acknowledged. This in turn suggests that epifaunal drilling of prey is a plesiomorphic, opportunistic mode of behavior, conserved in the evolution of the Naticidae, that has permitted subsequent escalation or expansion in range of naticid foraging from a more narrowly defined infaunal paradigm into exposed intertidal refugia.

ESCALATION AND EXTINCTION SELECTIVITY: MORPHOLOGY VERSUS ISOTOPIC RECONSTRUCTION OF BIVALVE METABOLISM

Abstract Studies that have tested and failed to support the hypothesis that escalated species (e.g., those with predation‐resistant adaptations) are more susceptible to elimination during mass extinctions have concentrated on the distribution and degree of morphological defenses in molluscan species. This morphological approach to determining level of escalation in bivalves may be oversimplified because it does not account for metabolic rate, which is an important measure of escalation that is less readily accessible for fossils. Shell growth rates in living bivalves are positively correlated with metabolic rate and thus are potential indicators of level of escalation. To evaluate this approach, we used oxygen isotopes to reconstruct shell growth rates for two bivalve species (Macrocallista marylandica and Glossus markoei) from Miocene‐aged sediments of Maryland. Although both species are classified as non‐escalated based on morphology, the isotopic data indicate thatM. marylandica was a faster‐growing species with a higher metabolic rate and G. markoei was a slower‐growing species with a lower metabolic rate. Based on these results, we predict that some morphologically non‐escalated species in previous tests of extinction selectivity should be reclassified as escalated because of their fast shell growth rates (i.e., high metabolic rates). Studies that evaluate the level of escalation of a fauna should take into account the energetic physiology of taxa to avoid misleading results.

The Escalation Hypothesis: One Long Argument

Ever since Darwin, we have asked: Do predictable rules govern the evolutionary process? The question has attracted the attention of countless evolutionary biologists, paleontologists, and philosophers alike. As with so much of our evolutionary thinking, we go back to Darwin and the Origin of Species , and the ideologies of his “one long argument,” as a starting point. Darwin (1859, p. 477) was well aware that ecology is important in shaping the evolution of life—“the relation of organism to organism is the most important of all relations”—but, perhaps more importantly, he realized the consequences of such a view for the history of life (see Ghiselin, 1995). Today, this Darwinian view of the evolutionary process, hardened by the architects of the Modern Synthesis, argues for long-term directionality in evolution. Directionality is the consequence of ecological struggles among metabolizing entities with energy-intensive forms of life exacting primary top-down control over, and replacement of, less energetic forms (Vermeij, 1999). This inherent directionality in the history of life, however, does not imply that living species, with more specialized and energy-demanding adaptations, are “better able to cope” with their biological environment than species in the geologic past were with theirs (Vermeij, 1987, p. 421). The most sophisticated modern version of Darwins view of the efficacy of biological agents of selection, and, to me, arguably one of the most significant paleontological hypotheses of the last 25 years, is Geerat Vermeijs (1987) hypothesis of escalation, which states that the history of life has been characterized by two simultaneous long-term directional trends within similar environments: increasing biological hazards (predation and competition), and increasing incidence and expression of enemy-related adaptations to these biological hazards. In the limited space of this essay, I will attempt first to define briefly what is meant by escalation, stress two of the …