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Pecten Maximus) – a Palaeontological Perspective

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Pecten Maximus) – a Palaeontological Perspective GEOSCIENCE RECORDS Original Paper • DOI: 10.1515/georec-2015-0002 • Geosci. Rec. • 1–2 • 2015 • 16–20 Anti-predator adaptations in a great scallop (Pecten maximus) – a palaeontological perspective Krzysztof Roman Brom, Krzysztof Szopa, Tomasz Krzykawski, Tomasz Brachaniec, Mariusz Andrzej SalamonA* Krzysztof Roman Brom: Department of Paleontology and Stratigraphy, Faculty of Earth Sciences, University of Silesia in Katowice Krzysztof Szopa: Department of Geochemistry, Mineralogy and Petrography, Faculty of Earth Sciences, University of Silesia in Katowice Tomasz Krzykawski: Department of Geochemistry, Mineralogy and Petrography, Faculty of Earth Sciences, University of Silesia in Katowice Tomasz Brachaniec: Department of Geochemistry, Mineralogy and Petrography, Faculty of Earth Sciences, University of Silesia in Katowice Mariusz Andrzej Salamon: Department of Paleontology and Stratigraphy, Faculty of Earth Sciences, University of Silesia in Katowice* Record Internal durable microstructures in great scallop (Pecten maximus) shell probably record adaptations to increased predation pressure during the so-called Mesozoic Marine Revolution. Abstract Key words Shelly fauna was exposed to increased pressure exerted by shell-crushing durophagous Pecten maximus • shell • microstructure • adaptation • predation. predators during the so-called Mesozoic Marine Revolution that was initiated in the Triassic. As a result of evolutionary ‘arms race’, prey animals such as bivalves, developed many adaptations to reduce predation pressure (e.g. they changed lifestyle and shell Received: 5 December 2014 morphology in order to increase their mechanical strength). For instance, it was sug- Accepted: 26 January 2015 gested that Pectinidae had acquired the ability to actively swim to avoid predator attack during the early Mesozoic. However, pectinids are also know to have a specific shell microstructure that may effectively protect them against predators. For instance, we highlight that the shells of some recent pectinid species (e.g. Pecten maximus) that display cross-lamellar structures in the middle part playing a significant role in the en- ergy dissipation, improve the mechanical strength. In contrast, the outer layers of these bivalves are highly porous, which allow them to swim more efficiently by reducing the shell weight. Pectinids are thus perfect examples of animals optimising their skeletons for several functions. We suggest that such an optimisation of their skeletons for mul- tiple functions likely occurred as a results of increased predation pressure during the so-called Mesozoic Marine Revolution. 1. Introduction thickening and covering by spines), which likely increased their mechanical strength and consequently provided better protec- Coevolution of various predators and Conchifera is a classic ex- tion from predators (e.g. Vermeij, 1977, 1987; Kosnik et al., 2011), ample of an ‘arms race’. Such interdependence relies on the inter- including flatworms, drilling gastropods, asteroids, crustaceans action between two groups of species, in which group A evolves and carnivorous fish. In addition, development of appropriate appropriate adjustments to better exploit the species from group microstructures occurring in shells is also thought to increase the B, in response, group B evolves better adaptation for efficient re- mechanical strength (e.g. Ragaini & Di Celma, 2009). duction of pressure from the species of group A (e.g. Futuyma, Adaptations in morphology and lifestyle in bivalve molluscs 2008; Krebs, 2011). In order to reduce pressure from predators, have a critical impact on their survival. For instance, by increas- molluscs at the beginning of their evolutionary history needed to ing the mechanical strength of shells, molluscs may significantly adopt many anti-predator strategies. It has been argued that the reduce the pressure from predators (e.g. Harper & Skelton, 1993). formation of a shell during the so-called “Cambrian explosion” During the periods of increased pressure from shell-crushing was directly connected with the necessity of mechanical protec- predators, such as during the Mesozoic Marine Revolution tion of tissues with impaired ability to regeneration (Bengtson & (MMR), many adaptions to durophagous and boring predation Morris, 2009; Pokryszko, 2009; Jackson et al., 2010; Vendrasco et occurred in benthic organisms (Harper & Skelton, 1993). For al., 2010). The shell of an early Conchifera was likely formed via instance, some bivalves adopted an infaunal habit, using their the fusion of sclerites into larger structural units and then into a siphons to gather nutrients from the sediment–water interface coherent shell, which increased the fossilisation potential of early whilst remaining safe, the others evolved the ability to fuse to molluscs. the substrate, which made them more difficult to consume by During the periods of increased predation pressure, shells of smaller predators. The latter adaptation occurred in some spe- some molluscs underwent substantial modifications (such as cies of Ostreoida during the Late Triassic (Norian stage) referred * E-mail: [email protected], tel: +48600356268 16 GEOSCIENCE RECORDS Original Paper • DOI: 10.1515/georec-2015-0002 • Geosci. Rec. • 1–2 • 2015 • 16–20 to as the Early Mesozoic Marine Revolution (Salamon et al., 2012; valve shows well-evident porous microstructure of the ribs (Fig- Tackett & Bottjer, 2012). ure 1 E, F) consisting of numerous pores with a diameter rang- Shell of the molluscs is the product of mantle (pallium) and it is ing from 5 to 7 μm. Amount of pores is approximately 1300 per composed mainly of calcium carbonate (in the form of calcite 1 mm3. The middle layer, in turn, displays the hierarchical cross- and/or aragonite), which constitutes at least 95% of its weight and lamellar structure (Figure 1 C, D). various biopolymers forming the organic matrix (e.g. Dyduch- Falinowska & Piechocki, 1993; Barthelat et al., 2009; Piechocki, 2009; Katti et al., 2010; Meyers et al., 2011). It can be divided into 3. Discussion three main structural layers. The outermost layer, called periostra- cum, is made mainly of conchiolin. The next (middle) layer (meso- Defense mechanisms of prey against predator may be divided stracum) is mainly composed of calcium carbonate crystals. The into two main groups – passive and active. Passive defenses are third (inner) layer (hypostracum) is constructed by calcareous associated with morphological and anatomical adaptations, such plates. The first two layers are generally formed by the edge of as modifications in shell structure, whereas active defenses are the mantle, whereas the third one on the entire surface of epithe- related to direct responses to predator occurrence, for example, lial tissue (Urbański, 1989; Dyduch-Falinowska & Piechocki, 1993; active escape or rapid burrowing (e.g. Harper & Skelton, 1993). Jura, 2005; Piechocki, 2009). P. maximus exhibits both active and passive defensive traits. Bivalves may be divided into two main ecological categories: (i) As highlighted earlier, the shell structure of P. maximus exhib- infaunal forms, which live within the sediment, and (ii) epifaunal its highly hierarchical cross-lamellar microstructure. This type forms, which live on the bottom substratum (Raup & Stanley, of microstructure is responsible for increasing the mechanical 1984). Amongst epifaunal bivalves, three groups may be also dis- strength of the shell by efficient energy dissipation (e.g. Meyers tinguished: (i) species that attach to the substratum by an organic et al., 2008). It has been argued that about 60% of bivalve species byssus spun (such as Mytilus edulis), (ii) species that attach to the and 90% of gastropod species display this microstructure, thus it hard substratum by cementing valve (such as many species of Os- seems that it is the most common structural spatial organisation treidae), and (iii) species that are free lying, some of them with the occurring in the shells of molluscs (Barthelat et al., 2009; Salinas ability to swim (e.g. Pectinidae) (Harper & Skelton, 1993). & Kisailus, 2013). This hierarchical cross-lamellar microstructure The great scallop (Pecten maximus), so-called the king scallop, is has been thoroughly documented, for example, in queen conch a recent bivalve species belonging to Pteriomorphia bivalves of (Strombus gigas) (Salinas & Kisailus, 2013 and literature cited Ostreoida, order and Pectinidae family. This family has a very long therein), ark clams (Arcidae), cockles (Cardiidae), sunset clams and rich fossil record extending back to the Triassic period (e.g. (Psammobiidae), Venus clams (Veneridae), Lucinidae, Tellinidae Hautmann, 2010), which provides unique perspectives in under- and many others (Chavan, 1969; Taylor et al., 1969; Popov, 1986). standing the impact of increased predation pressure on prey evo- The detailed construction of hierarchical cross-lamellar structure lution. The unusual morphologies and (bio)geochemistry of the combined with the description of energy dissipation mechanism shell of this species have become an interest of many researchers were provided by Barthelat et al. (2009) and Espinosa et al. (2010). (e.g. Cuif & Dauphin, 1996; Chauvaud et al., 2005; Grefsrud et al., These data showed that the application of external forces to such 2008). In this paper, we discuss the specific microstructure of this shells instead of producing one large crack induce many minor species in the context of anti-predatory adaptation. channel cracks that are not
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