Onchidoris Bilamellata Class: Gastropoda, Heterobranchia, Euthyneura, Ringipleura

Home , Acanthodoris, Duvaucelia, Notum, Onchidella borealis, Onchidorididae, Onchidoris

Onchidoris bilamellata Class: Gastropoda, Heterobranchia, Euthyneura, Ringipleura

Order: Nudipleura, Nudibranchia, Doridina, Doridoidei Many-gilled onchidoris nudibranch Family: Onchidoridoidea, Onchidorididae

Description the dorid, with a variable number of lateral Size: Usual length 15 mm (McDonald 1980); pinnules. Proximal pinnules are larger than this specimen 15.5 mm long, 11 mm wide, 6 distal (Potts 1981). Unipinnate. Simple pin- mm high. Far northern and Atlantic speci- nate gills form almost erect branchial plumes mens can reach 31 mm length (Marcus arranged in two semicircles just anterior to the 1961). anus. Gills are not completely retractable Color: Translucent brownish-white with ir- (Kozloff 1974) (Fig. 1). While there is no bran- regular dark or rusty brown splotches, some- chial pocket into which the gills can be with- times as irregular longitudinal stripes. Com- drawn, there are localized muscle fibers monly a light spot between the dark rhino- around the base of each gill; contraction caus- phores; gills dull white, underside a dull es a depression in the mantle surface, and white (Marcus 1961). No yellow pigment, but gills can be brought in closer to the body some specimens without brown color (Potts 1981). Countercurrent exchange (Kozloff 1974). Cryptic coloration (Potts through the gills (Potts 1981). Clusters of 1981). branchial glands between every two gills Body: Doridiform: oval; slightly broadened (Marcus 1961). towards front. With a broad flat foot, thick Eggs: Type A, defined as an egg mass in rib- fleshy mantle, and conspicuous double cir- bon form, attached along the length of one clet of gills dorsally (Figs. 1, 2). Dorsum cov- edge, with capsules occurring throughout ered with many large round papillae, becom- (Hurst 1967). With a short, stout spiral ribbon ing smaller at edges. Surface firm. No large attached along one edge, flaring out on the processes except rhinophores, gills, and pa- other (O’Donoghue and O’Donoghue 1922) pillae. (Fig. 5); capsules have a smooth wall and Rhinophores: A single pair, with 15-20 leaf- contain 1-3 eggs; 60,000 eggs in a ribbon 4 lets on either side (Marcus 1961) (Fig. 1). cm long (Hadfield 1963). Eggs 100µm. Eggs Rhinophores not especially long. laid preferentially near conspecifics, masses Papillae: Mushroom-shaped, with protruding are common only in winter (Hurst 1967). spicules (Fig. 3). Numerous club-like tuber- Possible Misidentifications cles of unequal size with a slight convex top. There are other oval dorid nudi- 10-15 spicules covered with epithelium pro- branchs of the same general coloration and ject out over the surface. Spicules are thick shape as Onchidoris: Discocordis, Anisodoris, with blunt tips and are centrally bent, sloping Archidoris, and especially Acanthodoris brun- obliquely toward the base of the tubercle nea are all found in our area. None of these (Kress 1981). Spicules support the body and have 16-32 single, branchial plumes arranged make it unpalatable (Potts 1981). in the unusual two semicircles. Acanthodoris Oral Tentacles: None; fused as an oral veil. brunnea can be distinguished immediately by Gills: 16-32 (or more: 36 this specimen); its very long rhinophores and conical papillae The number of gills depends on the size of (not round ones), and by its seven branchial

A publication of the University of Oregon Libraries and the Oregon Institute of Marine Biology Individual species: https://oimb.uoregon.edu/oregon-estuarine-invertebrates and full 3rd edition: http://hdl.handle.net/1794/18839 Email corrections to: [email protected]

Ellison, C. and Hardy, M. 2017. Onchidoris bilamellata. In: Oregon Estuarine Invertebrates: Rudys' Illustrated Guide to Common Spe- cies, 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.

gills. Life-History Information A pulmonate, Onchidella borealis, re- Reproduction: Hermaphroditic, but not self- sembling a small shell-less limpet, is colored fertilizing; internal fertilization (Hurst 1967). quite like Onchidoris. Close inspection re- Reproductive output increases allometrically veals it to have stalked eyes, and only 20-24 with size (Todd 1979). Individuals may lay papillae dorsally (Morris et al. 1980). more than one egg ribbon (Potts 1970). Copu- Ecological Information lation takes place before each spawning Range: Aleutian Islands south to Morro Bay, (Hadfield 1963). Eggs are laid in ribbons dur- California (McDonald 1980). Widely distrib- ing February-March, and October-December uted in temperate and arctic seas of north- (Puget Sound) (Hurst 1967); May to mid-June (British Columbia) (O’Donoghue and O’Dono- ern hemisphere. Found as far north as Ice- land and Greenland (lat. 60-70 N), the Ber- ghue 1922). Annual species, with pattern not ing Sea (lat. 70 N), Alaska (lat. 60 N) and rigidly fitted to calendar month (Bleakney and Japan (lat. 45N). In Europe, found north of Saunders 1978). Breeding populations have a lat. 50 N, through Scandinavia and the North similar size and structure from year to year in Sea, on E and W coasts of Scotland and Ire- spite of variation in annual recruitment (Todd Onchidoris land and on both sides of the English Chan- 1979). Larval settlement of both B. balanoides nel. Found as far south as California (lat. 39) and determines level of recruit- (Potts 1970). ment (Todd 1979). Newly metamorphosed Onchidoris settle below rock overhangs dur- Local Distribution: Coos Bay: Pigeon Point. ing summer months and are likely to remain Habitat: Usually found with barnacle on the rock where they first settle. Growing Balanus balanoides; at Pigeon Point on and dorids migrate to the upper sides of rocks lat- under rocks; mudflats. Requires shade and er in the season and spawn on these surfac- dampness. Does not extend as high in the es. This migration explains cited “sudden ap- intertidal as its prey, Balanus, as exposure is pearance” of animals on shore, though they a limiting factor (Miller 1961). Range is lim- have been there for several months. This mi- ited by desiccation (Todd 1979). gration up the rock surface may be motivated by a lack of food, reduction in temperature, or Salinity: Collected at 30. Temperature: 8-11° C (Hurst 1967). a physiological change associated with the Tidal Level: Intertidal to 250 m (McDonald onset of maturity (Potts 1970). Aside from this 1980); collected at mid-intertidal. maturity-associated event, on-shore migra- Associates: Balanus, chiton Mopalia, crabs tions do not occur, and colonization of the Hemigrapsus and Cancer oregonensis, gas- shore is achieved by pelagic larvae, not by tropods Tegula and Nucella, sea star juvenile animals moving up from deeper water Pisaster ochraceus, anthozoans Anthopleu- (Potts 1970). ra elegantissima and A. artemisia, as well as These animals stop feeding during isopod ldotea P. wosnesenskii. Nucella is a spawning, and become weakened during this main competitor for food, which consumes period; a reduction of pigmentation on the B. balanoides at a rate of up to 8 times that dorsal mantle has been observed. After this of O. bilamellata (Potts 1970). annual spawning event, animals are washed Weight: 0.7 gm., wet. away and die (Potts 1970). Abundance: "Frequent" (McDonald 1980); Larva: Shell dimensions, on average, are seasonally common. 146.9µm length, 95µm width, and 108µm depth. The shell is typically sinistral (Hurst A publication of the University of Oregon Libraries and the Oregon Institute of Marine Biology Individual species: https://oimb.uoregon.edu/oregon-estuarine-invertebrates and full 3rd edition: http://hdl.handle.net/1794/18839 Email corrections to: [email protected]

1967, Table 9). Type C shells (Hadfield Majority of larvae hatch in February and 1963), defined as “egg shaped ‘inflated’ spend 2-3 months feeding and growing before shells” (Vestergaard and Thorson 1938). settling. Fully grown by December (Todd Planktotrophic (Goddard 1992). Long larval 1979). Some rapidly growing individuals un- life facilitates wide distribution (Potts 1970). dergo spawning and death in August. (Todd Ability to delay metamorphosis until suitable 1979). settlement substrate is reached (Potts Food: Barnacles, mostly Balanus (McDonald 1970). Larvae exhibit positive phototaxis 1980). Only feeds on soft parts of barnacle. (Hadfield 1963). Planktotrophic veliger lar- Until they can take adult prey, newly meta- vae only metamorphose in the presence of morphosed dorids eat barnacle cyprids and/or live barnacles (Todd 1979). Settlement and spat (Todd 1981), and debris associated with metamorphosis are separable events. Set- barnacles (Todd, unpublished, in Chia and tlement is reversible and can be repeated Koss 1988). (Chia and Koss 1988). Propodia of the ad- Predators: Many opisthobranchs are toxic or vanced veliger larva contain a unique set of bad-tasting; predators are mostly other nudi- anterolateral ganglia (Chia and Koss 1989). branchs (Morris et al. 1980). Currents gener- The primary receptor cells on the propodia ated by cilia on the body and gills, coupled of metamorphically competent veligers have with the continuous discharge of epithelial been identified and implicated in the settle- glands, branchial glands, and mucus, creates ment response to cues found in barnacle an unpleasant “envelope” surrounding the water (Arkett et al. 1989). Cells in the apical dorid (Potts 1981). Tactile stimulation of the sensory organ of the veliger are thought to dorsum triggers the release of a large amount contain receptors for inducers of metamor- of colorless, viscous mucus containing dis- phosis (Hadfield et al. 2000). Metamorphosis tasteful or toxic substances, which play a de- involves the resorption of the velum, loss of fensive role (Potts 1981). the larval shell, and incorporation of the vis- Behavior: When reared in the laboratory, vel- ceral mass into the cephalopedal mass igers are observed to actively feed off the bot- (Chia and Koss 1988). Chia and Koss tom of the dish, inverting onto their velum and (1988) emphasize the hardiness and dura- using it to plough through food accumulations bility of these larvae, suggesting they be (Chia and Koss 1988). used in teaching at inland universities to Settlement behavior involves a descent demonstrate the morphological and behav- to the bottom, in the normal swimming posi- ioral changes associated with metamorpho- tion, with the velum pointed upward. Upon sis. Large numbers of larvae can be cultured contact, the larval foot undergoes contortions. in the laboratory on a variety of phytoflagel- The top of the foot extends downward, be- lates and diatoms, at various temperatures, yond the operculum, and contacts the sub- without excessive media changes. stratum. The veliger then inverts onto the pe- Juvenile: dal sole, and a period of crawling ensues. Ac- Longevity: Most opisthobranchs live less tive crawling varies from minutes to several than a year (Morris et al. 1980). Not ob- hours before metamorphosis is triggered, and served to live past 9-10 months (Todd may be continuous or involve stationary peri- 1979). ods. While crawling, the velum is retracted, Growth Rate: Embryonic period 12-13 days folded into the larval shell. Crawling will take (Hurst 1967). Spawning December-April place for a maximum of 30 minutes if no bar- (Potts 1970) with a peak in mid-January. nacles are encountered, and the larva will re-

sume swimming (Chia and Koss 1988). gon. Feeding behavior involves entry by 7. HADFIELD, M. 1963. The Biology of nudi- rupture and downward displacement of the branch larvae. Oikos. 14(1): 85-95. barnacle operculum. The dorid comes to lie 8. HADFIELD, M., MELESHKEVITCH, E., on top of the opercular orifice by gliding up and BOUDKO, D. 2000. The apical senso- over the side of the barnacle capitulum at ry organ of a gastropod veliger is a recep- the rostral end (even if initial contact is made tor for settlement cues. The Biological Bul- with carinal end) and remains in this position letin. 198(1): 67-76. for several hours. Afterwards, it moves off 9. HURST, A. 1967. The egg masses and and is inactive during a period of digestion. veligers of thirty northeast Pacific opistho- Soft barnacle tissue may be removed by the branchs. The Veliger. 9:255-288. action of the radula (reduced), or the buccal 10. KOZLOFF, E.N. 1974. Keys to the marine crop may function as a suction organ in the invertebrates of Puget Sound, the San feeding process (Barnes and Powell 1954). Juan Archipelago, and adjacent regions. University of Washington Press, Seattle & Bibliography London. 1. ARKETT, S., CHIA, F., GOLDBERG, J., 11. KRESS, A. 1981. A scanning electron mi- and KOSS, R. 1989. Identified settlement croscope study of notum structures in receptor cells in a nudibranch veliger re- some dorid nudibranchs (Gastropoda: spond to specific cue. Biological Bulletin. Opisthobranchia). Journal of the Marine 176(2): 155-160. Biological Association of the United King- 2. BARNES, H., and POWELL, H. 1954. dom. 61(1): 177-191. Onchidoris fusca (Müller): a predator of 12. MARCUS, E. 1961. Opisthobranch mol- barnacles. Journal of Animal Ecology. 23 lusks from California. The Veliger. 3 (2): 361-363. (Supplement 1). 3. BLEAKNEY, J., and SAUNDERS, C. 13. MCDONALD, G.R. 1980. Guide to the nu- 1978. Life-history observations on nudi- dibranchs of California. American Malacol- branch mollusk Onchidoris bilamellata in ogists, Inc., Melbourne, FL. intertidal zone of Nova-Scotia. The Ca- 14. MILLER, M. 1961. Distribution and food of nadian Field-Naturalist. 92(1): 82-85. the nudibranchiate mollusca of the south 4. CHIA, F.S., and KOSS, R. 1988. Induc- of the Isle of Man. Journal of Animal Ecol- tion of settlement and metamorphosis of ogy. 30(1): 95-116. the veliger larvae of the nudibranch, 15. MORRIS, R. H., D. P. ABBOTT, and E. C. Onchidoris bilamellata. International HADERLIE. 1980. Intertidal invertebrates Journal of Invertebrate Reproduction and of California. Stanford University Press, Development. 14(1): 53-69. Stanford, California. 5. CHIA, F.S., and KOSS, R. 1989. The fine 16. O'DONOGHUE, C. H., and E. O'DONO- structure of the newly discovered propo- GHUE. 1922. Notes on the nudibranchiate dial ganglia of the veliger larva of the nu- mollusca from the Vancourver Island re- dibranch Onchidoris bilamellata. Cell and gion. Transactions of the Royal Society of Tissue Research. 256(1):17-26. Canada. 14:131-143. 6. GODDARD, J. 1992. Patterns of devel- 17. POTTS, G. 1970. The Ecology of Onchi- opment in nudibranch mollusks from the doris fusca [Nudibranchia]. Journal of the northeast Pacific Ocean, with regional Marine Biological Association of the United comparisons. Ph.D., University of Ore- Kingdom. 50(2): 269-292.

18. POTTS, G. 1981. The anatomy of respir- atory structures in the dorid nudibranchs, Onchidoris bilamellata and Archidoris pseudoargus, with details of the epider- mal glands. Journal of the Marine Biolog- ical Association of the United Kingdom. 61(4): 959-982. 19. TODD, C. 1979. The population ecology of Onchidoris bilamellata (L.) (Gastropoda: Nudibranchia). Journal of Experimental Marine Biology and Ecolo- gy. 41(3): 213-255. 20. VESTERGAARD, K. and G. THORSON, 1938. Über den Laich und die Larven von Duvaucelia plebeja, Polycera quadri- lineata, Eubranchus pallidus und Limapontia capitate.(Gastropoda Opis- thobranchiata.). Zoologischer Anzeiger. 124: 129-138. Updated 2017 C. Ellison and M. Hardy