Predation on Two Brachiopods, Joania Cordata and Argyrotheca Cuneata, from an Offshore Reef in the Tyrrhenian Sea

Predation on two brachiopods, Joania cordata and Argyrotheca cuneata, from an offshore reef in the Tyrrhenian Sea Francesca Evangelisti, Paolo G. Albano & Bruno Sabelli Marine Biology International Journal on Life in Oceans and Coastal Waters ISSN 0025-3162 Volume 159 Number 10 Mar Biol (2012) 159:2349-2358 DOI 10.1007/s00227-012-2019-1 1 23 Your article is protected by copyright and all rights are held exclusively by Springer- Verlag. This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your work, please use the accepted author’s version for posting to your own website or your institution’s repository. You may further deposit the accepted author’s version on a funder’s repository at a funder’s request, provided it is not made publicly available until 12 months after publication. 1 23 Author's personal copy Mar Biol (2012) 159:2349–2358 DOI 10.1007/s00227-012-2019-1 ORIGINAL PAPER Predation on two brachiopods, Joania cordata and Argyrotheca cuneata, from an offshore reef in the Tyrrhenian Sea Francesca Evangelisti • Paolo G. Albano • Bruno Sabelli Received: 17 February 2012 / Accepted: 12 July 2012 / Published online: 31 July 2012 Ó Springer-Verlag 2012 Abstract Predator holes in empty shells of Joania end-Permian mass extinction, their importance decreased cordata and Argyrotheca cuneata (Brachiopoda: Mega- dramatically (Gould and Calloway 1980). Today, they are a thyrididae) collected in the marine protected area ‘‘Secche relict group dominated by micromorphic species restricted di Tor Paterno’’, central Tyrrhenian Sea, Italy (41°350N– to shallow, cryptic, hard-bottom environments of tropical, 12°200E, at depths of 20–28 m), were analyzed. Predation subtropical, and temperate shelves (e.g., Asgaard and intensity was low but appreciable, with the more common Stentoft 1984; Kowalewski et al. 2002; Rodland et al. species J. cordata preyed on more frequently (6.7 %) than 2004; Logan et al. 2008), with only some medium and A. cuneata (3.8 %). Three main types of holes were rec- large-sized species living on the open shelf in cool tem- ognized: (1) cylindrical drill holes with a circular outline, perate (e.g., Noble et al. 1976; Tunnicliffe and Wilson (2) larger irregular holes with a jagged outline, and (3) 1988; Emig 1989) and polar regions (Peck et al. 2005; Gili small holes at the bottom of depressions in the shell. They et al. 2006). Some authors think that increased predation were probably produced by muricid gastropods, crabs, and pressure, associated with the Mesozoic Marine Revolution, Foraminifera, respectively. The large, irregular holes were may have been responsible, at least in part, for the dramatic the most common type in both brachiopod species. Evi- decrease in diversity of brachiopods in the post-Palaeozoic dence for predator selectivity with respect to which valve, the and their retreat to refugial environments to escape pre- position of the hole on the valve, and the size of the bra- dators (e.g., Stanley 1974, 1977; Vermeij 1977; Donovan chiopod with respect to those available was assessed. The and Gale 1990; Harper and Wharton 2000; Aberhan et al. ventral valve, the postero-medial portions of both valves, and 2006; Lee 2008;Vo¨ro¨s 2010). larger (J. cordata) or medium-sized (A. cuneata) shells were Paleoecologists are testing this hypothesis by studying more frequently holed. predation frequencies in fossil and present-day death assemblages and through the analysis of traces of predation on brachiopod shells, in the form of drill holes, breakage, and Introduction repair scars (reviewed by Harper 2011). Previous studies indicate generally low predation pressure (Harper 2011), Brachiopods are marine invertebrates with a long and rich although high predation frequencies have occasionally been paleontological history. They were extremely abundant and reported from the Palaeozoic (e.g., Kowalewski et al. 1998; diversified during the Palaeozoic (e.g., Ziegler et al. 1968; Hoffmeister et al. 2003), Mesozoic (e.g., Harper et al. 1998; Leighton 1999; Olszewski and Erwin 2004) but with the Harper and Wharton 2000), Cenozoic (e.g., Taddei Ruggiero and Annunziata 2002; Harper 2005; Schimmel et al. 2012), and also from the present (Kowalewski et al. 1997; Baumiller Communicated by J. P. Grassle. et al. 2003; Bitner 2010; Harper 2011). This condition, together with the assumed low palatability of brachiopods & F. Evangelisti ( ) Á P. G. Albano Á B. Sabelli due to their low flesh yield, spicule content, and possible Department of Evolutionary Experimental Biology, University of Bologna, Via Selmi 3, 40126 Bologna, Italy toxins (Thayer 1985; Thayer and Allmon 1990; Peck 1993; e-mail: [email protected] McClintock et al. 1993; Mahon et al. 2003), seems to indicate 123 Author's personal copy 2350 Mar Biol (2012) 159:2349–2358 an unlikely role of predation in the evolutionary history of the coralligenous samples providing most of the material for group (James et al. 1992; Kowalewski et al. 2005). both species. Only a few living specimens were found, 8 were However, the available data are insufficient to under- J. cordata and 3 were A. cuneata (Evangelisti et al. 2011). stand whether predation pressure can have an important Other taxa mainly gastropods, bivalves, crustaceans, and impact on the evolution of brachiopods and more investi- polychaetes were also collected (Albano and Sabelli 2011). gations are required, especially on modern brachiopods All individuals of J. cordata and A. cuneata were (Harper 2011; Harper et al. 2011). Here, we report preda- inspected for evidence of holes, and all holed specimens tion data on two living micromorphic brachiopod species, were counted and measured under a stereomicroscope with Joania cordata and Argyrotheca cuneata. These brachio- an ocular micrometer. Specifically, all three dimensions of pods were part of a death assemblage collected from dif- the shells were measured and length and width were recorded ferent substrates in the marine protected area ‘‘Secche di as defined by Williams et al. (2007) so that they represent Tor Paterno’’, an offshore reef in the central Tyrrhenian those of the ventral valve, which is usually the larger of the Sea. Predation data for J. cordata and A. cuneata are two valves. All holed shells were photographed with a digital particularly interesting for several reasons. First, both camera mounted on a stereomicroscope. For each species, species are small, and thus provide a low amount of food holes were characterized by their shape and the best pre- for potential predators. Second, they are typically cryptic, served shells of each kind were selected, ultra-sound washed, living in protected habitats such as on cave walls and roofs, gold-coated, and photographed with a scanning electron under boulders, and in coralline substrate, making them microscope. Hole frequencies as well as selectivity patterns difficult for predators to access. Finally, they are typically such as taxon, valve, site, and size selectivity were recorded. found in shallow waters, where other more attractive prey, Following the method of Baumiller and Bitner (2004), such as bivalve molluscs, and diverse predators are abun- hole frequencies were computed both on the total sample dant. The study goals were the following: (1) to identify and on each species separately, using, respectively, the traces of predation on empty shells of J. cordata and Assemblage Frequency Metric AF (Kowalewski 2002) and A. cuneata and identify the possible predators; (2) to the Lower Taxon Frequency LTF (Kowalewski 2002). investigate specific stereotypy patterns such as taxon Taxon selectivity and valve selectivity were evaluated selectivity, valve selectivity, site selectivity, and size using the binomial and the chi-square statistical tests. selectivity; and (3) to evaluate predation intensity. To evaluate shell site selectivity, two methods were used. In the first, following Baumiller and Bitner (2004), a uniform grid placed over the images of holed individuals Materials and methods was used to quantify the geometric position of the center of the holes (Fig. 1). This was accomplished by first nor- The material examined in this study was collected in the malizing all images to a common size, then selecting the Italian marine protected area ‘‘Secche di Tor Paterno’’,in the most representative image of the ventral valves of both central Tyrrhenian Sea, 12 km off the coast of Lazio. This is species and the dorsal valve of J. cordata. The dorsal valve a 27-hectare offshore reef with the top at -18 m and a of A. cuneata was excluded from the analysis because only maximum depth of *70 m; the perimeter is a rectangle with two individuals were holed on this valve. A uniform grid of the following corner coordinates: 41°3701800N–12°2003000E; at least 50 equal-sized squares was superimposed on each 41°3600000N–12°2105400;41°3403000–12°1903000;41°3504800– of the three chosen images. Next, the geometric center of 12°1800000. It hosts two important biocoenoses typical of the each hole was projected onto the three valves covered by Mediterranean Sea: a coralligenous one composed of the grid, and the total number of squares covering each encrusting calcareous algae, and patches of the endemic valve, as well as the number of holes falling inside each Mediterranean seagrass Posidonia oceanica, on the coral- square of the grid, was counted. The observed frequencies ligenous substrate. of squares with holes were compared to the expected fre- As part of a biodiversity project in the area, 11 sites quencies, obtained by assuming a random distribution so were sampled in May and June 2007, at depths of 20–28 m. that P, the probability of a hole, was equal to the total At each site, three samples of the coralligenous biocoe- number of holes divided by the total number of squares. nosis, the seagrass rhizomes, and the detritic bottom were The two frequency distributions were compared using the collected by diver-operated airlift suction samplers, while chi-square test.

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