High frequency and severity of breakage-induced shell repair in western Atlantic Pinnidae (Bivalvia)

For many bivalved animals, shell damage creates a temporary breach through which metabolites signalling the location of an injured animal might pass even when the valves are shut. Thus, shell injuries that expose soft tissues are generally thought to increase susceptibility to other causes of death, especially predators, resulting in low frequencies of shell repair. An exception to this generalization is hypothesized to be species with a highly retractable mantle edge and a thin and flexible valve margin, such as many pinnoidean and pteriodean bivalves. When the valve edges of species with these traits are broken the mantle may be withdrawn without injury. Moreover, a broad seal is created when the flattened flexible valve margins are squeezed together as the shell is shut. These traits might also permit large parts of the shell near the growing edge to be broken off without injury to the mantle. If mantle retraction and flexible margins are advantageous in increasing survivorship of marginal injuries (however caused), species with these traits should have relatively high frequencies of shell repair compared with species from similar environments that lack them. Anecdotal accounts suggest that the Pinnidae, or pen shells, which have the capacity to withdraw the mantle and squeeze the shell edge together, are often heavily scarred from breakage at the growing edge of the shell. But quantification of repair frequency and the extent of breakage in members of this group are lacking to test the prediction of a survivorship advantage: do the Pinnidae have higher incidences and severity of shell repair than coexisting bivalves that lack flexible valve margins and the capacity for deep mantle withdrawal? To evaluate the advantage of flexible valve margins and deep mantle withdrawal in damage control, we examined the pinnid species Atrina rigida, Servatrina serrata, Pinna carnea and Pinna rudis for evidence of breakage-induced shell repair. Shells of A. rigida (n 1⁄4 73) and S. serrata (n 1⁄4 9) were collected in situ from an intertidal muddy sand flat near Masonboro Inlet, North Carolina. A second sample (n 1⁄4 24) of A. rigida was collected from within seagrass beds in St. Joseph’s Bay, Florida. Samples of P. carnea (n 1⁄4 16) and P. rudis (n 1⁄4 23) from the Florida Keys were obtained from the collections of the Academy of Natural Sciences, Philadelphia. We defined repair frequency as the number of repairs in a sample divided by the number of specimens. For comparison with the semi-infaunal Pinnidae, we also calculated repair frequency for 29 other co-occurring shallow infaunal and semi-infaunal bivalve species lacking flexible valve margins and deep mantle withdrawal (Table 1). We categorized repairs as scalloped if the dorsal–ventral width of the scar exceeded its anterior–posterior length (e.g. Fig. 1A, C), or embayed if the scar was shaped like a piewedge, with the anterior–posterior dimension of the scar greater in length than the dorsal–ventral dimension, or vice versa depending on the species (e.g. Fig. 1B, D); gradations between these scar types exist (Fig. 1E). When the designation of shape was borderline between these categories, scars were scored as the less severe damage type. Our results support the hypothesis that flexible valve margins and deep mantle withdrawal are advantageous traits to survive breakage-induced shell injury. Repair frequencies (range 1⁄4 0.31–1.14) for the pen shell species exceed values for all other species we examined that lack flexible valve margins and deep mantle withdrawal, except for two venerid species (Fig. 2; Table 1). Over 60% of species with inflexible valve margins and non-retractable mantle edges had repair frequencies less than 0.1. A Mann–Whitney U-test indicates that the mean rank of repair frequencies for pinnids exceeds the mean rank value for species with inflexible valve margins and nonretractable mantle edges (U0 1⁄4 152, P, 0.01). The percentage of embayed breaks (Fig. 1B, D), the most severe type of shell repair, ranged between 38% and 100% among the pinnid species (Fig. 3; Table 1). The lowest of these values is nearly 10 times the maximum percentage (4%) found for species with inflexible margins and non-retractable mantle edges, suggesting a poor capacity to sustain and repair extensive marginal damage (Table 1). A high incidence of embayed repairs is associated with the capacity for deep mantle withdrawal and flexible valve margins (Pearson chi-square test of independence; x 1⁄4 124.7, df 1⁄4 1, P 0.001). Scars may extend more than half the anterior–posterior length (Fig. 1B); such breaks encroached near the posterior adductor muscle, but do not extend into the nacreous layer surrounding the adductor muscle scar (Fig. 3). Some scalloped breaks meander across the entire dorsal–ventral width of the shell (Fig. 1A), which suggests removal and re-secretion of the entire posterior margin of the shell. We conclude that the highly retractable mantle edges of the Pinnidae, coupled with the flexible nature of their shell, contribute to their unusually high tolerance of extensive shell breakage. We believe that this interpretation is robust and unlikely to change if a more constrained test standardized comparisons of repair frequency between species better, for instance by size, age or habit. Despite the wide variation of these factors in the current dataset, results within pinnids and species lacking flexible valve margins and deep mantle withdrawal are consistent with each other, suggesting that additional data are unlikely to alter our conclusions. An avenue of study that might prove fruitful is to evaluate repair frequency in species with similar traits as the Pinnidae, such as members of the Pteriidae, Malleidae and Isognomonidae. Our results predict these groups should also display higher frequencies of shell repair than co-occurring species lacking flexible margins and deep mantle withdrawal. From an evolutionary perspective, the high frequency and severity of injuries in the Pinnidae indicates that the evolution of breakage resistance is not constrained by the bivalved condition. An evolutionary change that might be interpreted as a response to increased predation pressure is a reduction in the number of nacreous layers of the pinnid shell. This reduction (or regression towards the valve anterior) and consequent increase in area of the calcitic outer shell layer not Correspondence: G.P. Dietl; e-mail: gregory.dietl@yale.edu *Present address: Department of Geology and Geophysics, Yale University, New Haven, CT 06520, USA RESEARCH NOTES