Form and function of tentacles in pteriomorphian bivalves

Abstract

Tentacles are remarkable anatomical structures in invertebrates for their diversity of form and function. In bivalves, tentacular organs are commonly associated with protective, secretory, and sensory roles. However, anatomical details are available for only a few species, rendering the diversity and evolution of bivalve tentacles still obscure. In Pteriomorphia, a clade including oysters, scallops, pearl oysters, and relatives, tentacles are abundant and diverse. We investigated tentacle anatomy in the group to understand variation, infer functions, and investigate patterns in tentacle diversity. Six species from four pteriomorphian families (Ostreidae, Pinnidae, Pteriidae, and Spondylidae) were collected and thoroughly investigated with integrative microscopy techniques, including histology, scanning electron microscopy, and confocal microscopy. Tentacles can be classified as middle fold tentacles (MFT) and inner fold tentacles (IFT) according to their position with respect to the folds of the mantle margin. While MFT morphology indicates intense secretion of mucosubstances, no evidence for secretory activity was found for IFT. However, both tentacle types have appropriate ciliary distribution and length to promote mucus transportation for cleaning and lubrication. Protective and sensory functions are discussed based on different lines of evidence, including secretion, cilia distribution, musculature, and innervation. Our results support the homology of MFT and IFT only for Pterioidea and Ostreoidea, considering their morphology, the presence of ciliated receptors at the tips, and branched innervation pattern. This is in accordance with recent phylogenetic hypotheses that support the close relationship between these superfamilies. In contrast, major structural differences indicate that MFT and IFT are probably not homologous across all pteriomorphians. By applying integrative microscopy, we were able to reveal anatomical elements that are essential for the understanding of homology and function when dealing with such superficially similar structures.

Untangling the diversity and evolution of tentacles in scallops, oysters, and their relatives (Bivalvia: Pteriomorphia)

“…Detailed anatomy seems to support this hypothesis, due to similarities in cilia distribution and innervation between the tentacles of these two clades (Audino and Marian 2020). However, in a broader taxonomic context, detailed anatomical data suggests that tentacles might not have a single, common origin in Pteriomorphia, possibly including independent acquisitions in scallops and relatives 6 (Pectinoidea) (Audino and Marian 2020). To test the hypothesis that tentacles represent evolutionary convergences, i.e., similar phenotypes with independent evolution (Agrawal 2017), comparative morphological study within the phylogenetic framework of Pteriomorphia is necessary.…”

“…IFT also have numerous nerves associated with ciliary tufts on the tentacle surface. These structures are likely sensory receptors, suggesting that IFT in oysters and relatives have sensory functions (Audino and Marian 2020).…”

“…Similarly, several lines of evidence suggest that MFT have sensory roles, as expected for organs located on the middle mantle fold (Yonge 1983). For example, MFT in Ostreoidea and Pterioidea are organs provided with multiple tentacular nerves and sensory receptors, particularly at the tip of the tentacle where a group of ciliary receptors is located (Audino and Marian 2020). In scallops (Pectinidae), long MFT were observed in Argopecten irradians (Lamarck, 1819) (Wilkens 2006), Nodipecten nodosus (Linnaeus, 1758) (Audino et al 2015), Pecten maximus (Linnaeus, 1758) (Dakin 1909), and Placopecten magellanicus (Gmelin, 1791) (Moir 1977).…”

“…Conversely, a later morphological and phylogenetic investigation has suggested that tentacles on the middle mantle fold of Pterioidea and Ostreoidea are homologous (Tëmkin 2006), i.e., share a common, phylogenetic origin. Detailed anatomy seems to support this hypothesis, due to similarities in cilia distribution and innervation between the tentacles of these two clades (Audino and Marian 2020). However, in a broader taxonomic context, detailed anatomical data suggests that tentacles might not have a single, common origin in Pteriomorphia, possibly including independent acquisitions in scallops and relatives 6 (Pectinoidea) (Audino and Marian 2020).…”

“…Interestingly, tentacles share some gross similarities across pteriomorphian lineages, including location at the mantle margin, abundance and distribution along the margin, and slender morphology. In functional terms, tentacles are supposed to be sensory organs, also acting as secretory and protective structures in oysters, scallops, and file clams (Gilmour 1967;Waller 1976;Moir 1977;Audino et al 2015;Audino and Marian 2020).…”