The Scientific Naturalist Ecology, 100(12), 2019, e02818 © 2019 by the Ecological Society of America entirely benthic development (Ockelman 1958, Collin and Giribet 2010). The next question is, obviously: What makes it? Because the bivalve germinal epithelium has no secre- tory cells, and no auxiliary cells have been observed con- Cloaked bivalve oocytes: lessons in structing such a feature around developing oocytes, the evolution, ecology, and scientific most likely origin is the oocyte itself—and this has also been reported in unpublished work (cited in Gros et al. awareness 1997). Histological sections show a thin cloak around young oocytes (not shown), and a very thick one around 1 PETER G. BENINGER AND DAPHNE CHEREL mature oocytes (Fig. 1B). Manuscript received 20 March 2019; revised 15 May 2019; With respect to evolutionary lessons, coated oocytes accepted 17 June 2019. Corresponding Editor: John Pastor. have been observed in species from four of the six Faculte des Sciences, Universite de Nantes, 2 rue de la subclasses of the Bivalvia. There appears to be no Houssiniere, 44322 Nantes Cedex, France. taxonomic or evolutionary pattern in their occurrence; 1 E-mail: [email protected] they are found both in the primitive Cryptodonta and in the much later Heterodonta and Anomalodesmata Citation: Beninger, P. G., and D. Cherel. 2019. Cloaked (Table 1). In each of these subclasses, there are also bivalve oocytes: lessons in evolution, ecology, and scien- many species without coated oocytes, even within the tific awareness. Ecology 100(12):e02818. 10.1002/ecy.2818 same family (e.g., Pectinidae and Veneridae). The possi- bility that this is the result of multiple convergent evolu- Key words: bivalves; coat; mucopolysaccharides; oocytes; scien- tions of an identical character seems so remote as to be tific awareness. highly improbable. Conversely, if all bivalves possess the genetic and metabolomic equipment to produce such We have recently observed a gelatinous coat surround- coats (i.e., this is a pleisiomorphic character), why have ing the oocytes of Cerastoderma edule within which the so few such examples been observed? Assuming that it is development of early larval stages takes place (Fig. 1). a differentially expressed pleisiomorphic character, why Although variously coated oocytes are common in the is there no phylogenetic or taxonomic footprint? wider marine world, and among other molluscs, most If there is no phylogenetic relationship for the expres- bivalve researchers have never encountered such a thing. sion of this character, we might ask if there is an ecologi- And when they do, many simply ignore it, while others cal one. There is no indication that any ecological mislabel it as a “perivitelline space” (Gustafson and Reid parameter can switch this character on or off. All Ceras- 1986, Kandeel et al. 2013). Of course, the immediate toderma edule, as well as its sister species Cerastoderma question is: Why should we care? We should care first glaucum, present this character. Table 1 recapitulates because of the ecological and evolutionary lessons and some of the most important ecological parameters for perspectives this feature holds. And we should care marine bivalves: water temperature, depth, and habitat. because it tells us something very important about how Again, no pattern is evident; coated oocytes are found in the process of science funding can shape our view of the bivalves living at all temperatures, at all depths to the natural world. edge of the continental shelf, and in both epibenthic and First of all, what is this cloak? Of the few authors who endobenthic habitats. The endobenthic preponderance have actually reported its existence, most simply desig- of the 14 coated species is easily explained by the fact nate it as a “gelatinous covering” (Creek 1960), “jelly that the vast majority of all bivalve species are endoben- coat” (Hodgson and Burke 1988, Gros et al. 1997), or thic; similarly, the preponderance of reports from shal- “adhesive gelatinous egg capsule” (Gustafson and Lutz low depths probably represents material constraints: 1992). Unpublished data indicate that in Codakia orbicu- easily accessible bivalves are sampled more often than laris, the coat is composed of glycoproteins and proteo- those which require shipboard procedures. glycans (cited in Gros et al. 1997); this is consistent with Having ascertained that the presence of coated bivalve the staining we recently obtained using Alcian blue, and oocytes is not related to the major abiotic characteristics the lack of any periodic acid–Schiff staining in the com- of the marine habitat, we naturally proceed to question mon cockle, Cerastoderma edule (Fig. 1B). Although what selective advantage such a character might present. some bivalve species deposit gelatinous egg masses on We may set aside the possibility that the sheath con- the substratum, these are functionally and morphologi- tributes to the energy reserves necessary for the first cally different structures, characteristic of species with developmental stages, because it does not decrease in Article e02818; page 1 Article e02818; page 2 THE SCIENTIFIC NATURALIST Ecology, Vol. 100, No. 12 in (A) (B) ex c n nu hl p 5 mm 20 µm (C) (D) I d o c c 20 µm 30 µm FIG.1. Cerastoderma edule. (A) External view, showing both inhalant (in) and exhalant (ex) siphons. (B) Histological section of pedunculated (i.e., young) oocyte. Nucleus (n), nucleolus (nu), peduncle (p) and jelly coat (c) stained with Alcian blue, indicating acid mucopolysaccharides (AMPS). (C) Unstained, spawned oocyte surrounded by jelly coat (c). (D) Young veliger larva (l, approx- imately 24 h in laboratory) developing within Alcian blue–stained jelly coat (c). Note adhering detritus particles (d). size over the course of larval development (Fig. 1C, D). mucopolysaccharide (AMPS) oocyte coat is Four alternative possibilities come to mind: undoubtedly resistant to digestion conditions (the intestine and stomach are themselves protected by a 1) Mechanical protection. Especially in the shallow coating of AMPS), such that even if swallowed, a fer- coastal habitats, currents can bring planktonic larvae tilized oocyte or larva may survive passage through into abrasive contact with topographic features. The the gut, as has been observed for copepod eggs sticky oocyte coat rapidly accumulates detrital parti- (Flinkman et al. 1994). cles (Fig. 1D), giving it a layer of nonliving protec- 4) Microbial protection—AMPS is well-known as both tion, supported by a shock-absorbing mucus layer. a physical and a chemical barrier to opportunistic 2) Predator protection. The 50-lm oocyte becomes a microorganisms (Romo et al. 2016), and the marine 200-lm spawned oocyte/larva once the mucus coat is environment is a veritable soup of hungry microor- fully hydrated (Fig. 1C, D), removing it from the ganisms. And finally, for spermatozoa which already prey size range of many copepods, which are the function at low Reynolds numbers (i.e., even swim- most numerous and voracious planktonic predators. ming in water is like swimming in honey for us), this Larger predators are fewer in number, further reduc- thick, viscous coat will impose severe challenges to ing predation pressure. In addition, the jelly coat successful fertilization, opening the possibility of itself, as well as the accumulated seston particles, sperm competition and sperm selection. may be unappealing or poorly recognized visually or olfactorily, resembling detritus or inorganic particu- The advantages provided by the jelly coat appear to be late matter rather than living food. substantial, but all biologists know that they must have 3) Postpredation protection. Many invertebrate oocytes a cost. Among the angles that could be investigated, are swallowed whole during spawns, for example, fecundity immediately comes to mind. The oocyte coat by fish (Fuiman et al. 2015). The acid occupies a very significant amount of space in the gonad December 2019 THE SCIENTIFIC NATURALIST Article e02818; page 3 TABLE 1. Occurrence of gelatinous oocyte coat among bivalve taxa, arranged from most primitive to most recent. Habitat Genus and Subclass Family species Cold Temp Warm Shallow Shelf Epi Endo References Protobranchia Solemyidae Solemya reidi 999Gustafson and Reid (1986) S. velum 99 9Gustafson and Lutz (1992) Pteriomorphia Pectinidae Chlamys hastata 999Hodgson and Burke (1988) Paleoheterodonta NR Heterodonta Astartidae Astarte sulcata 99 9 9 9Saleuddin (1965)† Cardiidae Cerastoderma 99 9Kingston (1974), glaucum Kandeel et al. (2013)† C. edule 99 9 9Creek (1960), present study Donacidae Dona9 vittatus 99 9Frenkiel and Mou€eza (1979) Lucinidae Lucinoma 99 9Gros et al. (1999) aequizonata Codakia 99 9Alatalo et al. orbicularis (1984); Gros et al. (1997) Thyasiridae Thysasira gouldi 99999Blacknell and Ansell (1974) Semelidae Scrobicularia 99 9Frenkiel and plana Mou€eza (1979) Veneridae Mercenaria 99 9 9 9Loosanoff and mercenaria Davis (1950) M. camechiensis 99 9Loosanoff and Davis (1963) Venus striatula 99 9 9 9Ansell (1961) Arcticidae Arctica islandica 999Lutz et al. (1982) Anomalodesmata Laternulidae Laternula 999Ansell and Harvey elliptica (1997); Peck et al. (2007) Pandoridae Pandora 99 9 99Allen (1961) inaequivalvis Note: Epi, epibenthic; Endo, endobenthic; NR, none reported to date; Temp, temperate; Shelf, found over the depth range of the continental shelf. † Not reporzted, but visible in drawings/micrographs. acinus, which could otherwise be occupied by more that nobody works