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International audience; Spicules are mineral-based biocomposites skeletal structures that are widely distributed among phylogenetically distant groups of invertebrates (Porifera, Cnidaria, Mollusca, Echinodermata). Subepidermal spicules are formed under the ectodermal epithelium and are characterized for all groups except mollusks (Aplacophora, Polyplacophora, Bivalvia), their spicules are located on the surface of the body. However, one group of mollusks (Gastropoda: Heterobranchia) have unique subepidermal spicules that have never been detected above the ectodermal epithelium and similarly to those characterized for Porifera, Cnidaria and Echinodermata. Understanding subepidermal spicule formation in mollusks could help solve the question on the origin of spicules. Spicules in nudibranchs have been described for more than 150 years, yet ontogenetic dynamics of spicules have never been studied and the full mechanism of their formation remains unknown. Herein we investigate the spicule formation in different stages of postlarval development of the nudibranch Onchidoris muricata (O.F. Müller, 1776). For the first time, ontogenetic transformations of the spicule complex are described using experiments and different morphological methods. Our studies demonstrate that spicules of O. muricata form in the subepidermal space in early developmental stages immediately after veliger settlement. A single spicule forms inside a huge vacuole within a sclerocyte and remains there throughout the entire life of the specimen. Signs of spicule or sclerocyte migration under the epithelium in postlarval development was not found. Spicules only form during larval settlement, increasing only in size as development furthers. For the first time, spicule mineralization zones were detected at the tips of the spicules as well as the presence of collagen I in the overall composition of the spicules. Thus, our findings suggest that spicules form by an ectodermal cell that emerged under the ectodermal epithelium during the earliest stages of postlarval development.

The nudibranch mollusk Onchidoris muricata known from boreal waters of the western Pacific, North American Pacific shore, and both coasts of the northern Atlantic was first recorded from the Sea of Japan (East Sea). This discovery extends its distribution range southwards along the Asian Pacific coast from cool temperate waters of Kamchatka and Kommander’s Islands to cool temperate sub-zone of the Sea of Japan. Three discovered populations in the northern Sea of Japan are confirmed to be conspecific with other Pacific and Atlantic populations of O. muricata because of external and radular morphology along with low interpopulation genetic variation (

Invasion of the bryozoan Membranipora membranacea to the Gulf of Maine provided an additional prey resource to the dorid nudibranch Onchidoris muricata (Muller, 1776). We examined prey choice based on past diet history and compared growth and reproductive output among laboratory-reared O. muricata on exclusive bryozoan diets of M. membranacea and the native, historically preferred prey, Electra pilosa. Adult nudibranchs were collected from Cape Neddick, York, Maine for the prey choice experiment and post-metamorphic juveniles were collected from Jaffery Point, Newcastle, New Hampshire for the growth and reproduction experiments. Nudibranchs were laboratory reared under controlled conditions for up to 10 months until completion of spawning. Growth was monitored biweekly, and reproductive performance was assessed with a weight-adjusted dimensionless reproductive index (ΣRI) of each individual's spawn summed over the reproductive period. Prey choice experiments showed nudibranchs tended to select p...

The invasion of the bryozoan Membranipora membranacea to the Gulf of Maine in 1987 eventually provided an additional prey resource to the dorid nudibranch Onchidoris muricata (Muller, 1776). The impact of this novel prey on the population and reproductive biology of O. muricata was investigated at an intertidal site in the southern Gulf of Maine from January 2005 to October 2009. Nudibranchs were found associated with a variety of bryozoans, with a seasonal shift from Electra pilosa (December to May) to M. membranacea (June to November). Juveniles (< 3 mm) were found in all months except May, June, and July and mature nudibranchs were present in all months. Copulating pairs were observed between lanuary and July and spawn masses were found between March and September on the undersides of rocks usually attached to the surface of bryozoans. The population structure and reproductive phenology of O. muricata at this intertidal site shows changes from historical reports. Whether adaptive change of th...

Membranipora membranacea is an invasive bryozoan that was first found in the Gulf of Maine in 1987 and within two years became the dominant organism living on kelps. Membranipora may have become dominant so quickly because it had little competition in a relatively unoccupied niche; however, lack of predation has also probably played a major role. Where Membranipora is native, there is usually a specialist nudibranch predator that keeps the population in check. For example, in European populations, the nudibranch Polycera quadrilineata prefers Membranipora while Onchidoris muricata is known to prefer another bryozoan, Electra pilosa. Electra, Membranipora, and Onchidoris are all now found in the Gulf of Maine while Polycera is not. We tested whether Onchidoris would (1) eat Membranipora at all, (2) eat Membranipora and Electra at different rates, and (3) show a preference for eating Membranipora or Electra when given a choice. We found that Onchidoris does eat Membranipora, and it generally eats Membranipora faster than Electra. However, when given a choice, Onchidoris prefers Electra. Onchidoris typically reproduces in the spring and grows over the fall and winter, but has recently been found reproducing in the winter in New Hampshire. Although it does not survive the winter as well as Electra, Membranipora is the dominant organism living on many macroalgae in the late summer and fall. Thus, the large Membranipora food source now available in the summer and fall may allow Onchidoris to reproduce earlier.

Although theory pinpoints the reliability of cues as an important condition for the evo- lution of inducible defenses, the specificity of cues is poorly known in most systems. The bryozoan Membranipora membranacea produces long, energetically-costly spines in response to a trophically specialized nudibranch Doridella steinbergae, but the range of nudibranchs that trigger this response is unknown. We tested chemical cues from 14 nudibranch species from 4 suborders, the snail species Lacuna vincta, and an abiotic treatment (desiccation) for their ability to induce spines. Both corner spines (arising from the corners of the zoecium) and membranous spines (arising from the frontal membrane of the zooid) were observed. Of the nudibranch species tested, 57% induced corner spines in at least 1 trial: 4 predators of M. membranacea (Onchidoris muricata, Polycera zosterae, Triopha catalinae, and D. steinbergae) and 4 non-predators (Coryphella sp., Archidoris odhneri, Cadlina luteomarginata, and Dirona albolineata). Although many nudibranchs occasionally triggered spines, the spine response was most reliably and fully developed in response to the bryozoan's primary predator, D. steinbergae. All other species that induced corner spines, except Coryphella sp., failed to induce spines in all trials. Membranous spines were sometimes produced in response to D. stein- bergae, O. muricata, P. zosterae, A. odhneri, and Coryphella sp. The last 2 species are not known to prey on M. membranacea. Neither corner nor membranous spines were ever induced by Discodoris sandiegensis, Dendronotus frondosus, Dendronotus diversicolor, Tritonia festiva, Flabellina trilineata, Phidiana crassicornis, or desiccation. Of these non-inducers, only P. crassicornis feeds on M. mem- branacea, and this species typically causes little damage. There was no phylogenetic pattern among nudibranchs inducing spines. The production of corner and membranous spines were correlated. Corner spines appeared to have a lower induction threshold than membranous spines; the latter are therefore a more conservative indication of induction. Counter to the hypothesis of Adler & Grun- baum, the spine-inducing chemical cue(s) from D. steinbergae is probably not a mating pheromone, as D. steinbergae egg masses and pre-reproductive slugs induced spines. We conclude that M. mem- branacea often produces spines in response to predators that are deterred by spines, but seems surprisingly responsive to cues from some benign nudibranch species.

Skin structures of nine different species of dorid nudibranchs were examined at the scanning electron microscope and the light microscope levels. From these observations the animals are grouped into three categories.1. Dorids with spicule-supported tubercles carrying a sensory knob (Rostanga rubra, Jorunna tomentosa, Onchidoris sparsa, Onchidoris pusilla).2. Dorids with small sensory papillae set in pits and distributed randomly between projecting spicules (Aegires punctilucens).3. Dorids with tubercles differing in shape from one species to another, invested with numerous spicules but without conspicuous sensory structures. The tips of the tubercles do, however, contain single sensory epithelium cells (Archidoris pseudoargus, Acanthodoris pilosa, Onchidoris muricata, Onchidoris bilamellata).

The nudibranch molluscs Adalaria proxima (Alder et Hancock) and Onchidoris muricata (Muller) are annual, semelparous, simultaneous hermaphrodites which are largely sympatric and preferentially graze the same bryozoan Electro pilosa (L.). Ecologically, morphologically, and taxonomically, these species are similar, however, they reproduce by means of contrasting larval types: O. muricata has long-term planktotrophic larvae and A. proxima has short-term pelagic lecithotrophic larvae. The present paper is the first of a series which aims to analyse these contrasting larval types within the context of detailed dynamic energy budgets. Here we present data on the rates of feeding, prespawning growth, and respiration for laboratoryheld “populations” of both species. Nudibranchs were collected from the field as juveniles and maintained at near-ambient (not constant) temperatures. For both O. muricata and A. proximo feeding rate displayed an asymptotic increase with body size. Both the observed mean and (fitted) estimates of feeding rates for A. proxima exceeded those for comparable-sized O. muricata . Correspondingly, A. proxima individuals demonstrated greater somatic growth rates, and attained greater maximum body sizes than did O. muricata . Furthermore, growth of A. proxima was approximately linear whilst that of O. muricata followed an increasing curvilinear pattern. Respiration rates were relatively constant within any given individual, however significant differences between individuals were observed for both species. O. muricata individuals displayed a more rapid increase in respiratory rate with increasing body size than did A. proxima . Respiration rates of either species were not significantly affected by (seasonal) flucuations in water temperatures, with the exception of A. proxima individuals during the spawning period.

Onchidoris muricata (Muller) and Adalaria proxima (Alder and Hancock) are sympatric, potentially competing species of dorid nudibranchs, which preferentially graze the cheilostome polyzoan Electra pilosa (L.). O. muricata is small and lays small eggs which hatch as poorly-developed planktotrophic veliger larvae. A. proxima is larger and reproduces by means of larger eggs which hatch, as well-developed lecithotrophic larvae, that can metamorphose within approximately 24 h of release. A. proxima larvae can feed in the plankton, but do not require extrinsic nutrition to undergo complete development. Both species spawn in February–april, and have a strictly annual life-cycle. Comparisons of the calorific content of spawn have shown that A. proxima apportions a greater number of calories to reproduction, but that O. muricata makes a greater relative effort. A. proxima shown considerable individual variability in reproductive effort, which fails to correlate with, body size or rate of spawning. A more deterministic situation applies to O. muricata, because body size and fecundity follow an allometric relationship. It appears that there is a threshold of absolute energy required to support the lecithotrophic larval strategy in nudibranchs, and that this is not attained by the smaller species, O. muricata. A. proxima thus appears to have both reproductive strategies open to it, and to have adopted lecithotrophy in order to offset the unpredictability of energy available for reproduction.

A total of 13 enzymes, coded by 14 loci, were successfully examined by horizontal starch gel electrophoresis in the intertidal dorid nudibranchs Adalaria proxima (Alder & Hancock) and Onchidoris muricata (Muller). The derived genetic identity and similarity values provided estimates more typical of congeneric, than only confamilial, species. The suggestion is that these two species hold a recent common ancestry, and that Adalaria proxima (with its more advanced, pelagic lecithotrophic larva) is an evolutionary derivative of the Onchidoris muricata stock. At least three loci ( Pgm and Fum, A. proxima; Pep-2, O. muricata ) are all highly polymorphic.

The long-necked cells of the foot on Onchidoris muricata were found distributed among the shorter secretory cells which composed most of the epidermal tissue. The long-necked cells extend through the basement membrane on which the smaller cells lie. The ultrastructure of the cell body at the base of the cell shows the nucleus, large amounts of rough endoplasmic reticulum, and an extensive Golgi body that produces large numbers of secretory granules. The periodic acid-thiosemicarbazide silver protein (PA-TSC-SP) test for polysaccharides was negative for the secretory material. These results are consistent with polysaccharides having large obstructing groups such as sulfates. The high iron diamine (HID) test for sulfated carbohy drates was positive in the Golgi saccules and secretory granules at the base of the cell. Tannic acid fixation for glucosaminoglycans was only slightly positive in the extracellular matrix. Alcian blue stained tissue for light microscopy complimented the ultrastructural cytochemical tests and indicated that the secretory materials are sulfated mucopolysaccharides.

The nudibranch molluscs Adalaria proxima and Onchidoris muricata are semelparous annuals. Although these species are ecologically, morphologically, and taxonomically similar, their reproductive characteristics differ markedly. In the present study, A. proxima individuals generally attained a larger size and commenced spawning later in the spring than O. muricata . The total energy invested in spawn production by A. proxima individuals was ≈ 1.5 times that for O. muricata , however, A. proxima produced this in fewer spawn masses and over a shorter spawning period. Correspondingly, the mean energy content of A. proxima spawn masses was greater (≈ 3 times) than that of O. muricata spawn. Nonetheless, the “average” A. proxima spawn mass contained only an estimated 675 ova in comparison to the 3300 ova in an “average” O. muricata spawn mass. This difference was due to the contrasting larval types exhibited by these species. A. proxima produces large well-provisioned ova which hatch as pelagic lecithotrophic veligers, whereas O. muricata ova are relatively small and develop into long-term planktotrophic larvae. Individuals of both species were observed to undergo degrowth throughout their spawning periods, but total production (soma plus cumulative spawn) continued to rise at a rate equal to, or slightly greater than, prespawning growth rate. Overall production patterns showed considerable intraspecific consistency, but differed between species. Degrowth rate (per day) for A. proxima was in excess ofthat for O. muricata , however, all individuals died after ≈33% of the maximum somatic weight had been lost.

The annual cycles of the intertidal nudibranchs Onchidoris muricata (Muller) and O. bilamellata (L.) were followed through three generations at Robin Hood's Bay, North Yorkshire. O. muricata , a generalist polyzoan grazer, occurs throughout the range of its preferred prey species - Electra pilosa (L.) - and exhibits a simple annual cycle. O. bilamellata , on the other hand, is narrowly restricted within the distribution of its major prey species ( Balanus balanoides (L.)), and shows local variations in growth rate, levels of fecundity, timing of spawning and, in some localities, precocious maturation. Although the life cycle of O. bilamellata is generally annual, individuals undergoing precocious development spawn and die within approximately 3 months of settling. The planktotrophic larval phase of O. bilamellata is of some 3 months duration, with settlement and metamorphosis of the pediveliger only in the presence of live barnacles. The major aspects of the population ecology of these 2 species are compared and contrasted, and related to the differing pressures placed upon the predators by the morphology and life-cycles of their respective prey items.