Predation on two , 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

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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- 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 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, , respectively. The large, irregular holes were may have been responsible, at least in part, for the dramatic the most common type in both 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 ( ) P. G. Albano 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. In the second method, following a strategy two sediment samples were collected by hand at the base of proposed by Deline et al. (2003), the same grid was used, a coralligenous wall and nearby small P. oceanica mea- and two tests were performed. In the first test, each chosen dow. A total of 1,208 dead complete brachiopod specimens image of ventral and dorsal valves of both species was were found, 730 belonging to J. cordata (Risso, 1826) and subdivided into an anterior and a posterior half, each of 478 to A. cuneata (Risso, 1826) with detritic and equal area (each covering half of the squares in the grid). 123 Author's personal copy

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Fig. 1 Distribution of holes on ventral valves of Joania cordata (a, b); on dorsal valves of J. cordata (c, d); on ventral valves of Argyrotheca cuneata (e, f). Each circle corresponds to geometric centre of one hole

Then, the number of holes in each half was counted, and J. cordata holed on the ventral valve and dorsal valve were the binomial test and the chi-square test were used to then compared in their shape and median sizes, using, evaluate whether there was a significant difference between respectively, the Kolmogorov–Smirnov test and Mann– them. In the second test, each valve was subdivided into a Whitney U test, computed with the program Past (Hammer central and a marginal region, which were marked using a et al. 2001). smaller outline of the valves. As before, the number of For all statistical analyses, a significance level of 5 % holes in each region was counted, and the binomial test and (a = 0.05) was applied. All material from the present study the chi-square test were used to evaluate whether there was is housed in the Zoological Museum of the University of a significant difference between them. Bologna, Italy. To estimate size selectivity, frequency distributions of length for holed and un-holed individuals of both species (Fig. 2)andforJ. cordata holed on theventral valve and dorsal Results valve (Fig. 3) were computed. For each frequency histogram, a Shapiro test and Skewness Index were computed using the Hole frequencies program R (R Development Core Team 2008), in order to investigate their shape. Length frequency distributions of Of the 1,208 dead brachiopods examined, 67 were holed and un-holed individuals of both species and of holed, 49 J. cordata and 18 A. cuneata (Table 1).

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the shell surface, circular to sub-circular in outline, small, and penetrated only one valve. There was no evidence for repaired holes or attachment scars on the shell surfaces. The shapes of holes were easily categorized into four types: (1) a cylindrical hole with regular circular outline, smooth sides, and the inner perforation of a smaller diameter (Fig. 4a, b); (2) a larger hole with an irregular, jagged, and broken outline (Fig. 4c, d); (3) a very small hole found at the bottom of a conical depression (Fig. 4e, f); (4) one small and irregular hole with an obvious narrow groove oriented perpendicular to the center of the hole (Fig. 4g–i). Most of the holes belonged to the second category: 44 out 49 of J. cordata (89.7 %) and 15 out 17 of A. cuneata (88.2 %). Only two individuals of each species had cylin- drical holes (4.1 % J. cordata and 11.7 % A. cuneata), while holes of the third type were found in two J. cordata (4.1 %). The fourth type of hole was found in only one specimen of J. cordata (2 %); the hole and the groove were probably made by the same excavating organism. Fig. 2 Length frequency histograms of holed (black) and un-holed (gray) Joania cordata (a) and Argyrotheca cuneata (b) Taxon selectivity and valve selectivity

Joania cordata was preferentially holed, as evidenced by both the binomial test (P \ 0.02, with P the probability for each individual to be holed) and the chi-square test 2 (v1 = 14.34, P \ 0.05, performed assuming half of the holed shells belonged to J. cordata and half to A. cuneata). In both species, holes were found on either the ventral or the dorsal valve, while no holes were found on both valves of the same individual. Of the 49 holed individuals of J. cordata, 34 (69.4 %) were holed on the ventral valve and 15 (30.6 %) on the dorsal valve. Of the 16 holed individuals Fig. 3 Length frequency histograms of Joania cordata holed on of A. cuneata (one individual was excluded from compu- ventral valve (gray) and dorsal valve (black) tation because the hole was likely from breakage rather than perforation), 14 (87.5 %) were holed on the ventral valve The Assemblage Frequency Metric, given by the ratio and 2 (12.5 %) on the dorsal valve (Table 1). The apparent between total number of holed individuals and the total preference for the ventral valve was statistically significant number of individuals expressed as a percentage, was equal for both species, as indicated by both the binomial test to 5.5 %, while the Lower Taxon Frequency values, given (P = 0.0047 for J. cordata, and P = 0.0011 for A. cuneata) 2 by the total number of holed individuals of each species and the chi-square test (v1 = 7.36, P \ 0.05 for J. cordata, 2 divided by the total number of individuals of each species and v1 = 9.94, P \ 0.05 for A. cuneata). The binomial test expressed as a percentage, were 6.7 % for J. cordata and was performed assuming equal probability of a hole on the 3.8 % for A. cuneata. This shows that holes frequencies ventral and dorsal valves. were higher in J. cordata, the most abundant species. Site selectivity Holes shape Both tests used to detect site selectivity revealed the In both species, most specimens had only one hole, with presence of a highly non-random pattern of hole distribu- only seven J. cordata having multiple holes (five with 2 tions in the valves. First, there was significant site selec- holes on the ventral valve, one with 2 holes on the dorsal tivity on the ventral valve of both species and on the dorsal 2 valve, and one with 4 holes on the ventral valve) and only valve of J. cordata (v4 = 218.96, P \ 0.05 for J. cordata 2 one A. cuneata having 2 holes on the ventral valve. In both ventral valve; v2 = 17.19, P \ 0.05 for J. cordata dorsal 2 J. cordata and A. cuneata, all holes were perpendicular to valve; v3 = 32.06, P \ 0.05 for A. cuneata ventral valve). 123 Author's personal copy

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Table 1 Hole data for dead Joania cordata and Argyrotheca cuneata from ‘‘Secche di Tor Paterno’’ Central Tyrrhenian Sea Species Number undrilled Number drilled Drilled on ventral Drilled on dorsal Drilled on margin

Joania cordata 681 49 34 15 0 Argyrotheca cuneata 460 18 15 2 1 Total 1,141 67 49 17 1

Second, in J. cordata, the posterior half and the central part and median size (Kolmogorov–Smirnov test, D = 0.19, of the ventral valve were preferentially holed (P = 0.0004 P [ 0.05; Mann–Whitney U test, U = 3,993, N1 = 460, and P = 0.001, respectively, using the binomial test, P = N2 = 18, P [ 0.05). Un-holed individuals showed a right 2 Q = 0.5; v1 = 11.56, P \ 0.05 for anterior–posterior skewed distribution (Skew Index = 0.39, P = 0.005), while 2 parts; v1 = 9.14, P \ 0.05 for central–marginal parts) holed individuals showed a distribution that was approxi- (Fig. 1a, b). No selectivity was detected between the pos- mately normal (Skew Index =-0.45, P = 0.098). Holed terior and anterior halves of the dorsal valve of J. cordata individuals ranged in length from 1.5 to 2.5 mm, with two (Fig. 1c; P = 0.39 using the binomial test, P = Q = 0.5, modes at 1.8 and 2.1 mm. Similar to J. cordata, the un-holed 2 and v1 = 0.28, P \ 0.05), while the central part was individuals showed a polymodal pattern. preferentially holed (Fig. 1d; P = 0.006 using the binomial 2 test, P = Q = 0.5, and v1 = 7.14, P \ 0.05). Finally, the posterior half of the ventral valve of A. cuneata was Discussion preferentially holed (Fig. 1e; P = 0.006 using the binomial 2 test, P = Q = 0.5, and v1 = 8.21, P \ 0.05), while no Potential predators preference was detected between the central and marginal parts (Fig. 1f; P = 0.25 using the binomial test, P = Q = The holes documented for J. cordata and A. cuneata most 2 0.5, and v1 = 0.31, P \ 0.05). likely record biotic interactions. This is because they are typically singular, small, circular to sub-circular to oval in Size selectivity outline, perpendicular to the shell surface, and penetrate only one valve (Kelley and Hansen 2003). The simulta- Joania cordata neous presence of multiple stereotypic patterns observed for both species is further evidence that the holes are of The size frequency distributions of holed and un-holed biological origin (Hoffmeister et al. 2003). J. cordata were statistically different in their shape and Establishing the kind of biotic interaction is more diffi- median size (Fig. 2a; Kolmogorov–Smirnov test, D = 0.31, cult, but it is likely that the holes of both species are the

P \0.05; Mann–Whitney U test, U = 0.00012, N1 = 681, result of predations, as no repaired or incomplete holes, or N2 = 49, P \ 0.05). Un-holed individuals had a left skewed attachment scars on the shell surface, were found and only a size frequency distribution (Skew Index =-0.53, P = few specimens had more than one hole (Kowalewski 2002). 0.024), while it was only slightly left skewed for holed Although the nature of the predator cannot be established individuals (Skew Index =-0.37, P = 0.046). Apart from unequivocally, the shapes of holes provide information one small individual of 1.5 mm, all holed individuals were about the identity of the predator or predators (Bromley [1.9 mm long, with two modes, at 1.9 and 2.8 mm. The 1981; Kabat 1990; Kowalewski 1993). In this study, the pattern for un-holed individuals was polymodal. Size fre- four different kinds of holes suggest that they might have quency distributions for J. cordata holed on the ventral valve been produced by four different species; possible variation and on the dorsal valve (Fig. 3) were statistically indistin- in the activity of the same predator can be excluded, as no guishable in their shape and mean value (Kolmogorov– significant overlaps in hole size or shape were observed. Smirnov test, D = 0.26, P [ 0.05; Mann–Whitney U test, The cylindrical holes with a regular circular outline are

U = 222.5, N1 = 34, N2 = 15, P [ 0.05). Individuals probably the result of drilling by gastropods (Jonkers holed on dorsal valve were [1.9 mm long, while some 2000). Other groups of invertebrates can drill the shells of smaller specimens were holed on the ventral valve. Both the prey, including flatworms, cephalopods, and nematodes distributions were clearly polymodal. (Kowalewski 2002), but they normally generate holes with a different outline, such as the oval holes made by octopods Argyrotheca cuneata (Bromley 1993). Among gastropods, members of the and are common drillers, but muricids Size frequency distributions of holed and un-holed A. cuneata are the most likely predators responsible for these drill (Fig. 2b) were statistically indistinguishable in their shape holes, as they typically produce holes with a cylindrical to 123 Author's personal copy

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Fig. 4 SEM of Joania cordata valves with four types of holes with enlargements on right: (1) cylindrical holes (a, b); (2) hole with irregular, jagged, and broken outline (c, d); (3) holes at the bottoms of conical depressions (e, f); (4) irregular hole with groove leading toward it (i). Scale bars 1mm (a, c, e, g) and 100 lm (b, d, f, h, i)

steep-sided vertical profile and the outer diameter beveled and the vertical profile appears clearly parabolic exceeding the inner one (Bromley 1981; Carriker 1981; (Carriker 1981). For brachiopods, drill holes are the most Harper and Peck 2003). Naticids also produce holes with a documented traces of predation and muricids are known to circular outline, but in this case, the edge of the hole is prey on brachiopods, both fossil (e.g., Baumiller and Bitner

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2004; Harper 2005; Baumiller et al. 2006; Taddei Ruggiero species. There are also numerous species of crabs, with and Bitner 2008; Schimmel et al. 2012) and recent (e.g., Xantho pilipes, Parthenope massena, and Ebalia edwardsi Taddei Ruggiero et al. 2006; Taddei Ruggiero and Bitner the most common. These species might have been 2008). In this study, however, only a few holes were made responsible for the crustaceans’ holes. However, without by muricids (4.1 % J. cordata and 11.7 % A. cuneata). catching the predator in the act, the holes cannot unam- The bigger holes with jagged, broken outlines are more biguously be assigned to a specific organism (Bromley difficult to interpret. They are similar to the damage made 1981). by crushing predators, such as decapod crustaceans (Seed 1982, 1990; Ramsay et al. 2001). In particular, the holes Stereotypy patterns are similar to the large punch holes produced by crabs (e.g., Bourdeau and O’Connor 2003; Harper 2005; Morton and Joania cordata was holed more often than A. cuneata.This Harper 2008). However, the position of the holes is unu- preference could be due to its generally greater size and sual. Crabs typically produce breakages along the margin smoother shell surface, which would make attacks by of the valves or in the umbonal region of the prey as they predators easier. In J. cordata and A. cuneata, most holes attempt to open the shell looking for food (e.g., Ameyaw- occurred on the ventral valve and this preference may be Akumfi and Hughes 1987; Taddei Ruggiero et al. 2006; due to the larger size of this valve, which provides a larger Morton and Harper 2008). The present holes occupied a platform, and because of the life position of the two spe- postero-central position on both valves of the two species. cies. Both J. cordata and A. cuneata live with their ventral The size and life position of J. cordata and A. cuneata valve attached to hard substrates, while the dorsal valve is suggest a possible explanation. As the two species are very close to or directly in contact with the substrate. Obviously, small and live with the dorsal valve attached to the sub- this position prevents or strongly reduces any action on the strate, the opening of the shell by predators is difficult; dorsal valve, while activities on the ventral valve are instead, the crab crushes the shell with one claw, holding favored. The preference for the posterior part of the valves on with the other claw to the substrate, to obtain purchase in both species can be explained by the fact that the pos- for the crushing action. This would be consistent with the tero-medial area of the brachiopod shell corresponds to the reduction in predation costs shown by decapods (Juanes body cavity with the body and muscles. Any hole in the 1992; Yamada and Boulding 1998). Some cases of crab postero-medial part of any valve (the so-called fleshy zone) predation on brachiopods have been reported for both provides direct access to food. Anterior holes would pro- ancient (Harper 2005) and recent forms (Paine 1969; vide direct access only to the mantle cavity with the mantle Simo˜es et al. 2001; Taddei Ruggiero et al. 2006); however, tissue and lophophore, but these parts are of low food value crab attacks are usually less frequent than those by gas- (e.g., McClintock et al. 1993; Mahon et al. 2003). tropods. In this study, most holes were made by crusta- In A. cuneata, a size preference by the predator is sug- ceans (89.7 % J. cordata and 88.2 % A. cuneata). gested by the fact that holed individuals ranged in length The third type of hole, the very small hole at the bottom from 1.5 to 2.5 mm, smaller and larger individuals being of a conical depression in the shell, seems to be related to un-holed. The bimodal pattern shown by holed individuals predation by encrusting Foraminifera. These organisms of both species indicates that two size classes are much attach to a variety of substrates, including the shells more commonly holed. This may suggest, assuming a of various molluscs (e.g., Browne and Berkman 1992; correlation between prey size and predator size, two dif- Cedhagen 1994; Beuck et al. 2008; Richardson-White and ferent predators or, alternatively, the presence of two age Walker 2011) and also brachiopods (e.g., Alvarez and classes of the same predator. The polymodal patterns Taylor 1987; Barnes and Peck 1996), often leaving bioe- shown by the un-holed individuals of both species, as well rosion on their shells to enhance food gathering (Ve´nec- as the polymodal patterns shown by the J. cordata holed Peyre´ 1996). As encrusting Foraminifera are known to use dorsally and ventrally, may represent successive age clas- structures to support their pseudopodial nets during feeding ses of specimens. This contrasts with the findings of Asg- (Lipps 1983), the conical depressions we observed could be aard and Bromley (1990), who suggested J. cordata and related to increasing the surface area for feeding and pro- A. cuneata may have a two-year life spans. tecting the pseudopodia from predation. Finally, the small hole with a rut toward it was probably Predation intensity made by an excavator organism, which left a trace with its movement on the shell surface. However, its identity Given the likely predatory origin of the holes in J. cordata remains unknown and no further observations were made. and A. cuneata, the hole frequencies were used as an index Muricid gastropods are very common in the marine of predation intensity on the two species (Leighton protected area, with Muricopsis cristata the most abundant 2002), 6.7 % for J. cordata and 3.8 % for A. cuneata. 123 Author's personal copy

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This indicates a low predation intensity when compared Ameyaw-Akumfi C, Hughes RN (1987) Behaviour of Carcinus with previous studies on fossil and present-day brachio- maenas feeding on large Mytilus edulis. How do they assess the optimal diet? Mar Ecol 38:213–216 pods. Typically, predation levels [15 % are considered Asgaard U, Bromley RG (1990) Colonization by micromorph high (e.g., Deline et al. 2003; Baumiller et al. 2006; brachiopods in the shallow subtidal of the eastern Mediterranean Rodrigues 2007; Tuura et al. 2008; Schimmel et al. 2012), Sea. In: MacKinnon DI, Lee DE, Campbell JD (eds) Brachio- although lower values have also been reported (e.g., Taddei pods through time. Balkema, Rotterdam, pp 261–264 Asgaard U, Stentoft N (1984) Recent micromorphic brachiopods from Ruggiero 1990; Delance and Emig 2004; Hoffmeister et al. Barbados: paleoecological and evolutionary implications. Geo- 2004; Simo˜es et al. 2007). biol 17:29–37 Previous studies reported different predation intensities Barnes DKA, Peck LS (1996) Epibiota and attachment substrata of in the two studied species. Taddei Ruggiero and Bitner deep-water brachiopods from Antarctica and New Zealand. Philos Trans R Soc Lond 351:677–687 (2008) studied bioerosion traces on brachiopod shells in 20 Baumiller TK, Bitner MA (2004) A case of intense predatory drilling assemblages of different ages (from to Recent) of brachiopods from the middle of southeastern Poland. from various Mediterranean areas and found predation Palaeogeogr Palaeoclimatol Palaeoecol 214:85–96 values of 2.1 % for J. cordata and 4.3 % for A. cuneata.In Baumiller TK, Kowalewski M, Deline BL, Hoffmeister AP, Ame´zi- ane N, Ele´aume M, D’Hondt JL (2003) Drillholes in extant this case, A. cuneata was preyed on more often, while brachiopods and their implications for the history of predation. predation intensity for J. cordata was lower than in our Geol Soc Amer, Abstracts with Programs, pp. 35–7 study. 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Berlin, Heidelberg, pp 329–360 preyed on more often, and only the values of 3.1 % for Bitner MA (2010) Biodiversity of shallow-water brachiopods from A. cuneata and 4.2 % for J. cordata were similar to the New Caledonia, SW Pacific, with description of a new species. frequencies we herein report. These data, together with the Sci Mar 74:643–657 present study, show that predation occurs in brachiopods Bourdeau PE, O’Connor NJ (2003) Predation by the nonindigenous Asian shore crab Hemigrapsus sanguineus on macroalgae and with characters which should prevent or reduce predation, molluscs. Northeast Nat 10:319–334 and that wide variation in predation frequencies exists Bromley RG (1981) Concepts in ichnotaxonomy illustrated by small among sites. round holes in shells. Acta Geol Hisp 16:55–64 Bromley RG (1993) Predation habits of Octopus past and present and Acknowledgments Field work was supported by RomaNatura a new ichnospecies, Oichnus ovalis. 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