Phylum: bilamellata Class: , Opisthobranchia Order: Nudibranchia Many-gilled onchidoris Family: Onchidoridae

Description Papillae: Mushroom-shaped, with protruding Size: Usual length 15 mm (McDonald 1980); spicules (Fig. 3). Numerous club-like this specimen 15.5 mm long, 11 mm wide, 6 tubercles of unequal size with a slight convex mm high. Far northern and Atlantic specimens top. 10-15 spicules covered with epithelium can reach 31 mm length (Marcus 1961). project out over the surface. Spicules are Color: Translucent brownish-white with thick with blunt tips and are centrally bent, irregular dark or rusty brown splotches, sloping obliquely toward the base of the sometimes as irregular longitudinal stripes. tubercle (Kress 1981). Spicules support the Commonly a light spot between the dark body and make it unpalatable (Potts 1981). rhinophores; gills dull white, underside a dull Eggs: Type A, defined as an egg mass in white (Marcus 1961). No yellow pigment, but ribbon form, attached along the length of one some specimens without brown color (Kozloff edge, with capsules occurring throughout 1974). Cryptic coloration (Potts 1981). (Hurst 1967). With a short, stout spiral ribbon Body Shape: Doridiform: oval; slightly attached along one edge, flaring out on the broadened towards front. With a broad flat other (O’Donoghue and O’Donoghue 1922) foot, thick fleshy mantle, and conspicuous (Fig. 5); capsules have a smooth wall and double circlet of gills dorsally (Figs. 1, 2). contain 1-3 eggs; 60,000 eggs in a ribbon 4 Dorsum covered with many large round cm long (Hadfield 1963). Eggs 100µm. Eggs papillae, becoming smaller at edges. Surface laid preferentially near conspecifics, masses firm. No large processes except rhinophores, are common only in winter (Hurst 1967). gills, and papillae. Veliger: Shell dimensions, on average, are Rhinophores: A single pair, with 15-20 146.9µm length, 95µm width, and 108µm leaflets on either side (Marcus 1961) (Fig. 1). depth. The shell is typically sinistral (Hurst Rhinophores not especially long. 1967, Table 9). Type C shells (Hadfield Gills: 16-32 (or more: 36 this specimen); The 1963), defined as “egg shaped ‘inflated’ number of gills depends on the size of the shells” (Vestergaard and Thorson 1938). dorid, with a variable number of lateral Planktotrophic (Goddard 1992). Long larval pinnules. Proximal pinnules are larger than life facilitates wide distribution (Potts 1970). distal (Potts 1981). Unipinnate. Simple Ability to delay metamorphosis until suitable pinnate gills form almost erect branchial settlement substrate is reached (Potts 1970). plumes arranged in two semicircles just Larvae exhibit positive phototaxis (Hadfield anterior to the anus. Gills are not completely 1963). Planktotrophic veliger larvae only retractable (Kozloff 1974) (Fig. 1). While there metamorphose in the presence of live is no branchial pocket into which the gills can (Todd 1979). Settlement and be withdrawn, there are localized muscle metamorphosis are separable events. fibers around the base of each gill; Settlement is reversible and can be repeated contraction causes a depression in the mantle (Chia and Koss 1988). Propodia of the surface, and gills can be brought in closer to advanced veliger larva contain a unique set of the body (Potts 1981). Countercurrent anterolateral ganglia (Chia and Koss 1989). exchange through the gills (Potts 1981). The primary receptor cells on the propodia of Clusters of branchial glands between every metamorphically competent veligers have two gills (Marcus 1961). been identified and implicated in the Labial Tentacles: None; fused as an oral settlement response to cues found in veil. water (Arkett et al. 1989). Cells in the apical sensory organ of the veliger are thought to contain receptors for inducers of

Ellison, C. and Hardy, M. 2017. . In: Oregon Estuarine Invertebrates: Rudys' Illustrated Guide to Common , 3rd ed. T.C. Hiebert, B.A. Butler and A.L. Shanks (eds.). University of Oregon Libraries and Oregon Institute of Marine Biology, Charleston, OR.

A publication of the University of Oregon Libraries and the Oregon Institute of Marine Biology Individual species: http://hdl.handle.net/1794/12916 and full 3rd edition: http://hdl.handle.net/1794/18839 Email corrections to [email protected] metamorphosis (Hadfield et al. 2000). intertidal as its prey, , as exposure is Metamorphosis involves the resorption of the a limiting factor (Miller 1961). Range is limited velum, loss of the larval shell, and by desiccation (Todd 1979). incorporation of the visceral mass into the Salinity: Collected at 30. cephalopedal mass (Chia and Koss 1988). Temperature: 8-11° C (Hurst 1967). Chia and Koss (1988) emphasize the Tidal Level: Intertidal to 250 m (McDonald hardiness and durability of these larvae, 1980); collected at mid-intertidal. suggesting they be used in teaching at inland Associates: Balanus, chiton Mopalia, crabs universities to demonstrate the morphological Hemigrapsus and Cancer oregonensis, and behavioral changes associated with gastropods Tegula and Nucella, sea star metamorphosis. Large numbers of larvae can Pisaster ochraceus, anthozoans Anthopleura be cultured in the laboratory on a variety of elegantissima and A. artemisia, as well as phytoflagellates and diatoms, at various isopod ldotea P. wosnesenskii. Nucella is a temperatures, without excessive media main competitor for food, which consumes B. changes. balanoides at a rate of up to 8 times that of O. bilamellata (Potts 1970). Possible Misidentifications Weight: 0.7 gm., wet. There are other oval dorid nudibranchs of Abundance: "Frequent" (McDonald 1980); the same general coloration and shape as seasonally common. Onchidoris: Discocordis, Anisodoris, Archidoris, and especially Life History Information brunnea are all found in our area. None of Reproduction: Hermaphroditic, but not self- these have 16-32 single, branchial plumes fertilizing; internal fertilization (Hurst 1967). arranged in the unusual two semicircles. Reproductive output increases allometrically Acanthodoris brunnea can be distinguished with size (Todd 1979). Individuals may lay immediately by its very long rhinophores and more than one egg ribbon (Potts 1970). conical papillae (not round ones), and by its Copulation takes place before each spawning seven branchial gills. (Hadfield 1963). Eggs are laid in ribbons A pulmonate, borealis, during February-March, and October- resembling a small shell-less limpet, is December (Puget Sound) (Hurst 1967); May colored quite like Onchidoris. Close to mid-June (British Columbia) (O’Donoghue inspection reveals it to have stalked eyes, and and O’Donoghue 1922). Annual species, with only 20-24 papillae dorsally (Morris et al. pattern not rigidly fitted to calendar month 1980). (Bleakney and Saunders 1978). Breeding populations have a similar size and structure Ecological Information from year to year in spite of variation in Range: Aleutian Islands south to Morro Bay, annual recruitment (Todd 1979). Larval California (McDonald 1980). Widely settlement of both Onchidoris and B. distributed in temperate and arctic seas of balanoides determines level of recruitment northern hemisphere. Found as far north as (Todd 1979). Newly metamorphosed Iceland and Greenland (lat. 60-70 N), the Onchidoris settle below rock overhangs Bering Sea (lat. 70 N), (lat. 60 N) and during summer months and are likely to Japan (lat. 45N). In Europe, found north of lat. remain on the rock where they first settle. 50 N, through Scandinavia and the North Growing dorids migrate to the upper sides of Sea, on E and W coasts of Scotland and rocks later in the season and spawn on these Ireland and on both sides of the English surfaces. This migration explains cited Channel. Found as far south as California (lat. “sudden appearance” of on shore, 39) (Potts 1970). though they have been there for several Local Distribution: Coos Bay: Pigeon Point. months. This migration up the rock surface Habitat: Usually found with barnacle Balanus may be motivated by a lack of food, reduction balanoides; at Pigeon Point on and under in temperature, or a physiological change rocks; mudflats. Requires shade and associated with the onset of maturity (Potts dampness. Does not extend as high in the 1970). Aside from this maturity-associated

Ellison, C. and Hardy, M. 2017. Onchidoris bilamellata. In: Oregon Estuarine Invertebrates: Rudys' Illustrated Guide to Common Species, 3rd ed. T.C. Hiebert, B.A. Butler and A.L. Shanks (eds.). University of Oregon Libraries and Oregon Institute of Marine Biology, Charleston, OR. event, on-shore migrations do not occur, and period of crawling ensues. Active crawling colonization of the shore is achieved by varies from minutes to several hours before pelagic larvae, not by juvenile animals moving metamorphosis is triggered, and may be up from deeper water (Potts 1970). continuous or involve stationary periods. These animals stop feeding during spawning, While crawling, the velum is retracted, folded and become weakened during this period; a into the larval shell. Crawling will take place reduction of pigmentation on the dorsal for a maximum of 30 minutes if no barnacles mantle has been observed. After this annual are encountered, and the larva will resume spawning event, animals are washed away swimming (Chia and Koss 1988). and die (Potts 1970). Growth Rate: Embryonic period 12-13 days Feeding Behavior: Entry by rupture and (Hurst 1967). Spawning December-April downward displacement of the barnacle (Potts 1970) with a peak in mid-January. operculum. The dorid comes to lie on top of Majority of larvae hatch in February and the opercular orifice by gliding up over the spend 2-3 months feeding and growing before side of the barnacle capitulum at the rostral settling. Fully grown by December (Todd end (even if initial contact is made with carinal 1979). Some rapidly growing individuals end) and remains in this position for several undergo spawning and death in August. hours. Afterwards, it moves off and is inactive (Todd 1979). during a period of digestion. Soft barnacle Longevity: Most opisthobranchs live less tissue may be removed by the action of the than a year (Morris et al. 1980). Not observed radula (reduced), or the buccal crop may to live past 9-10 months (Todd 1979). function as a suction organ in the feeding Food: Barnacles, mostly Balanus (McDonald process (Barnes and Powell 1954). 1980). Only feeds on soft parts of barnacle. Until they can take adult prey, newly Literature Cited metamorphosed dorids eat barnacle cyprids and/or spat (Todd 1981), and debris 1. ARKETT, S., CHIA, F., GOLDBERG, associated with barnacles (Todd, J., and KOSS, R. 1989. Identified unpublished, in Chia and Koss 1988). settlement receptor cells in a Predators: Many opisthobranchs are toxic or nudibranch veliger respond to bad-tasting; predators are mostly other specific cue. Biological Bulletin. nudibranchs (Morris et al. 1980). Currents 176(2): 155-160. generated by cilia on the body and gills, 2. BARNES, H., and POWELL, H. coupled with the continuous discharge of 1954. Onchidoris fusca (Müller): a epithelial glands, branchial glands, and predator of barnacles. Journal of mucus, creates an unpleasant “envelope” Ecology. 23(2): 361-363. surrounding the dorid (Potts 1981). Tactile 3. BLEAKNEY, J., and SAUNDERS, C. stimulation of the dorsum triggers the release 1978. Life-history observations on of a large amount of colorless, viscous mucus nudibranch mollusk Onchidoris containing distasteful or toxic substances, bilamellata in intertidal zone of which play a defensive role (Potts 1981). Nova-Scotia. The Canadian Field- Behavior: When reared in the laboratory, Naturalist. 92(1): 82-85. veligers are observed to actively feed off the 4. CHIA, F.S., and KOSS, R. 1988. bottom of the dish, inverting onto their velum Induction of settlement and and using it to plough through food metamorphosis of the veliger larvae accumulations (Chia and Koss 1988). of the nudibranch, Onchidoris Settlement behavior: Involves a descent to bilamellata. International Journal of the bottom, in the normal swimming position, Invertebrate Reproduction and with the velum pointed upward. Upon contact, Development. 14(1): 53-69. the larval foot undergoes contortions. The top 5. CHIA, F.S., and KOSS, R. 1989. of the foot extends downward, beyond the The fine structure of the newly operculum, and contacts the substratum. The discovered propodial ganglia of the veliger then inverts onto the pedal sole, and a veliger larva of the nudibranch

A publication of the University of Oregon Libraries and the Oregon Institute of Marine Biology Individual species: http://hdl.handle.net/1794/12916 and full 3rd edition: http://hdl.handle.net/1794/18839 Email corrections to [email protected] Onchidoris bilamellata. Cell and Vancourver Island region. Tissue Research. 256(1):17-26. Transactions of the Royal Society of 6. GODDARD, J. 1992. Patterns of Canada. 14:131-143. development in nudibranch mollusks 17. POTTS, G. 1970. The Ecology of from the northeast Pacific , Onchidoris fusca [Nudibranchia]. with regional comparisons. Ph.D., Journal of the Marine Biological University of Oregon. Association of the United Kingdom. 7. HADFIELD, M. 1963. The Biology of 50(2): 269-292. nudibranch larvae. Oikos. 14(1): 85- 18. POTTS, G. 1981. The anatomy of 95. respiratory structures in the dorid 8. HADFIELD, M., MELESHKEVITCH, nudibranchs, Onchidoris bilamellata E., and BOUDKO, D. 2000. The and Archidoris pseudoargus, with apical sensory organ of a gastropod details of the epidermal glands. veliger is a receptor for settlement Journal of the Marine Biological cues. The Biological Bulletin. 198(1): Association of the United Kingdom. 67-76. 61(4): 959-982. 9. HURST, A. 1967. The egg masses 19. TODD, C. 1979. The population and veligers of thirty northeast ecology of Onchidoris bilamellata Pacific opisthobranchs. The Veliger. (L.) (Gastropoda: Nudibranchia). 9:255-288. Journal of Experimental Marine 10. KOZLOFF, E.N. 1974. Keys to the Biology and Ecology. 41(3): 213- marine invertebrates of Puget 255. Sound, the San Juan Archipelago, 20. VESTERGAARD, K. and G. and adjacent regions. University of THORSON, 1938. Über den Laich Washington Press, Seattle & und die Larven von Duvaucelia London. plebeja, Polycera quadrilineata, 11. KRESS, A. 1981. A scanning Eubranchus pallidus und Limapontia electron microscope study of notum capitate.(Gastropoda structures in some dorid Opisthobranchiata.). Zoologischer nudibranchs (Gastropoda: Anzeiger. 124: 129-138. Opisthobranchia). Journal of the Marine Biological Association of the United Kingdom. 61(1): 177-191. 12. MARCUS, E. 1961. Opisthobranch mollusks from California. The Veliger. 3 (Supplement 1). 13. MCDONALD, G.R. 1980. Guide to the nudibranchs of California. American Malacologists, Inc., Melbourne, FL. 14. MILLER, M. 1961. Distribution and food of the nudibranchiate mollusca of the south of the Isle of Man. Journal of Animal Ecology. 30(1): 95-116. 15. MORRIS, R. H., D. P. ABBOTT, and E. C. HADERLIE. 1980. Intertidal invertebrates of California. Stanford University Press, Stanford, California. 16. O'DONOGHUE, C. H., and E. O'DONOGHUE. 1922. Notes on the nudibranchiate mollusca from the

Ellison, C. and Hardy, M. 2017. Onchidoris bilamellata. In: Oregon Estuarine Invertebrates: Rudys' Illustrated Guide to Common Species, 3rd ed. T.C. Hiebert, B.A. Butler and A.L. Shanks (eds.). University of Oregon Libraries and Oregon Institute of Marine Biology, Charleston, OR.