Did shell-crushing crabs trigger an escalatory arms race in the aftermath of a Late Neogene regional mass extinction event? An experimental test

Abstract

A regional mass extinction event in the late Neogene western Atlantic is widely thought to have generated evolutionary opportunities for survivors, including enemy-related adaptation (escalation). The Strombus alatus species complex is one potential example of this phenomenon. Strombid gastropods are abundant in the PlioPleistocene fossil record and Recent in subtropical Florida, and the percentage of these shells bearing a row of short spines on the last whorl increased from nearly zero to almost 100% over this time. As shell ornamentation is one of the most frequently cited defenses against both peeling and crushing predators, we exposed live spined and spineless S. alatus to the stone crab Menippe, one of its natural enemies and the predator responsible for shells scars commonly found on modern and fossil S. alatus shells, to test whether the increase in expression of shell spines in this species complex is consistent with an adaptive or induced response to intensifying predation pressure from durophagous crabs. We also utilize random variation in prey shell length, diameter, and lip thickness to quantify the relative importance of additional shell parameters thought to deter attacks from durophagous crabs. The central finding of this study is that neither thicker shell lips nor the modern configuration of spines determine whether S. alatus will be more likely to survive Menippe attacks or have less severe shell damage. In our experiments, the only shell trait associated with reduced damage and increased probability of survival was whorl diameter. We conclude that menippid crabs, at least those crabs within the range of large, adult sizes used in this experiment, probably did not play a primary role in the changing expression of Strombus spines on the last whorl in the post-Pliocene of Florida or elsewhere in tropical America. This conclusion is consistent with the position that faunal-scale increases in expression of defensive shell traits in the post-Pliocene of Florida were driven more by differential extinction of lightly armored species than escalatory responses to increasing crab predation pressure. However this conclusion is tentative and additional data are needed to explore this hypothesis fully.

Morphology does not predict performance: jaw curvature and prey crushing in durophagous stingrays

“…The main determinant of predator success is the ability to exert high loads (Pfaller et al, 2011). For this reason it is possible to explore the implications of different predator and prey morphologies and to determine their interactions (Bertness and Cunningham, 1981;Whitenack and Herbert, 2015). Not only is there variation in the crushing jaws of the predators, but there are also material and structural differences in the shells of the prey.…”

Macroecology and evolution of a crab ‘super predator’,Menippe mercenaria(Menippidae), and its gastropod prey

“…Because many whelks lacking a tumid ridge experienced fatal body whorl punctures (Kosloski, 2012), this particular kind of localized thickening may be useful against outright crushing attempts. Repeated reorientation of shells was also observed (Kosloski, 2012), and spines, which increase the effective diameter of the shell and vary in expression from the Pliocene to Recent (Kosloski, 2012), appeared to provide no benefits in encounters with stone crabs, as also observed by Whitenack & Herbert (2015). Spines instead appeared to facilitate crabs gaining a better purchase on whelk shells (Kosloski, 2012).…”

“…Menippe mercenaria can generate crushing forces of at least 380 N at the tip of the dactyl (Blundon, 1988), with some estimates of force production as high as 1500 N (Whitenack & Herbert, 2015) ( Table 1). This force production is much higher than other crabs in the western Atlantic and is in line with force production of more heavily armored IndoPacific durophagous crabs (Vermeij, 1977b).…”

“…Although the tumid ridge does not increase the effective diameter of the shell, it does result in a localized region of increased shell thickness (Kosloski, 2012). When offered whelks ranging in size from 80 to 110 mm, stone crabs were mainly observed trying to outright crush shells (Kosloski, 2012;Kosloski, personal observations) vs. attempting to peel shells, as observed in Whitenack & Herbert (2015). Because many whelks lacking a tumid ridge experienced fatal body whorl punctures (Kosloski, 2012), this particular kind of localized thickening may be useful against outright crushing attempts.…”

“…In the Recent, the differential development of antipredator morphologies is a common feature for many marine invertebrates over varying temporal and spatial scales (Kitching, Muntz & Ebling, 1966;Seeley, 1986;Johannesson & Johannesson, 1996;Stachowicz & Hay, 2000;Trussell & Smith, 2000;Dalziel & Boulding, 2005;Hollander, Lindegarth & Johannesson, 2005;Sanford & Kelly, 2011;Bourdeau, 2012). With few exceptions (Vermeij & Covich, 1978;West, Cohen & Baron, 1991;Dietl & Alexander, 2000;Dietl, 2003;Whitenack & Herbert, 2015), however, this smaller scale has seldom been studied in the fossil record. Here, we explore one such example of the potential evolutionary effect of an unusually strong enemy: the durophagous predator, Menippe mercenaria Say, 1818, on shallow marine fauna on the southeastern Atlantic coast of North America (North Carolina to Florida) during the Pliocene.…”