Bitten spines reveal unique evidence for fish predation on Middle Jurassic echinoids

Abstract

Predation and other biotic interactions are critical factors in organismal evolution, yet direct evidence of predator-prey relationships is relatively rare in the fossil record (see Kowalewski & Kelley 2002; Kelley et al. 2003). Predators play important ecological roles in controlling population densities, species distributions, morphology, body size and the life habits as well as life strategies, and they are strong selective forces driving both predator and prey adaptation (Vermeij 1987, 1994; Dietl & Kelley 2002; Bambach 2003). The Jurassic was a time when marine communities were stabilizing after the first pulse of the Mesozoic Marine Revolution (Vermeij 1977, 1987, 2008; Aberhan et al. 2006; Tackett & Bottjer 2012; especially see Madin et al. 2006), and echinoids were undergoing significant evolutionary changes (especially infaunalization with its associated test flattening, spine size reduction, etc.), presumably in part as response to predation pressure (Smith 1984). The opening of new niches could also have triggered their infaunal lifestyle (Borszcz & Zato n 2013). According to Walker & Brett (2002), who comprehensively reviewed the post-Palaeozoic history of predators and prey, the Jurassic seas were dominated by pelagic and benthic predators such as decapod crustaceans with crushing claws, carnivorous sea stars, shellcrushing sharks and bony fish, as well as marine reptiles. The Jurassic is thus an important interval for studying predation on echinoids because of their rapid evolutionary innovations (Kier 1974, 1982; Simms 1991), as well as growing evidence for biotic interactions (Vermeij 2008; Borszcz & Zato n 2013). Echinoderms are attractive model organisms to study biotic interactions because their long fossil record has much data on predation and parasitism (Neumann 2000; Donovan & Jagt 2002; Baumiller & Gahn 2002, 2004; Radwa nska & Radwa nski 2005; Neumann & Wisshak 2006, 2009; Deline 2008; Villier 2008; Wisshak & Neumann 2006; Radwa nska & Poirot 2010; Borszcz & Zato n 2013) extending into the Recent (Schultz 2005; Baumiller et al. 2008, 2010). Crinoids in particular are well established as valuable organisms for tracking predation in deep time (Baumiller & Gahn 2004; Sallan et al. 2011; Gorzelak et al. 2012; Ausich & Kammer 2013; Syverson & Baumiller 2014), whereas other classes are relatively understudied. We demonstrate here the earliest direct evidence of fish predation on echinoids with a large number of Rhabdocidaris primary spines showing distinct bite marks in the Matmor Formation (Middle Jurassic, Callovian) in southern Israel. During the Jurassic, cidaroid echinoids slowly diversified, leaving a highly heterogeneous fossil record (Greenstein 1992). Rhabdocidaris Desor 1855–1858; is an extinct, speciose echinoid genus (e.g. Greenstein 1992; Kroh 2014) that originated in the Early Jurassic (Aalenian) and last appeared in the Early Cretaceous (Smith & Kroh 2011). They were a common component of epifauna in shallow water carbonate habitats (e.g. Radwa nska 1999, 2003). Rhabdocidaris was characterized by strong motile spines of various shapes, occasionally reaching 30 cm in length (and up to 7 cm in our assemblage). They had no epidermis on their spines like other cidaroids, thereby promoting syn vivo encrustation as with modern relatives (David et al. 2009). As suggested by functional morphological interpretations (Baumeister & Leinfelder 1998; Baumeister 1999), they most likely preferred low-energy firmground environments. Previous evidence of predation on echinoids in the fossil record is composed primarily of echinoid remains recovered from regurgitates (since the Middle Jurassic; see Baumeister et al. 2000; Borszcz & Zato n 2013), spines in vertebrate gut contents (since the Middle Jurassic; Kriwet 2001), tooth marks (since the Late Cretaceous; Thies 1985) and drill holes in sea urchin tests (since the Cretaceous; McNamara 1994; Ceranka & Zlotnik 2003; Zlotnik & Ceranka 2005; Grun et al. 2013, 2014; see review in Kowalewski & Nebelsick 2003). Other examples of bitten and/or regenerated tests and spines are known from the Miocene onward (Zinsmeister 1980; Kroh 2005). Kowalewski & Nebelsick (2003) pointed out that evidence of predation by fish on echinoids is scarce in the fossil record. This article, along with Borszcz & Zato n (2013), fills this need. It is also the oldest record of bite traces on echinoids, about 80 million years older than that previously reported by Thies (1985) from the Late Cretaceous genus Echinocorys. It is also the first fossil record of tooth impressions on the remains of ‘regular’ echinoids.