Marine Biology

, 164:114 | Cite as

Giant embryos and hatchlings of Antarctic nudibranchs (Mollusca: Gastropoda: Heterobranchia)

  • Juan MolesEmail author
  • Heike Wägele
  • Adele Cutignano
  • Angelo Fontana
  • Manuel Ballesteros
  • Conxita Avila
Original Paper


Bathydoris hodgsoni and Doris kerguelenensis are two of the largest Antarctic nudibranchs. They are both common circumpolar species with broad bathymetric distributions, although B. hodgsoni is restricted to deep waters in the Antarctic high latitude. Egg masses and juveniles of these species were collected over multiple years (1998–2012) in the eastern Weddell Sea and the South Shetland Islands, and here new data are provided about egg mass characteristics and ontogeny using histological techniques. The egg mass of B. hodgsoni has a maximum length of 12.4 cm with one or two egg capsules with a mean diameter of 4.9 cm. The capsules either contained non-developing eggs or ready-to-hatch juveniles up to 2.9 cm long. The egg mass of D. kerguelenensis is a semicircular ribbon-like structure including 1,500–2,400 oval capsules (~1.7 × 1.2 mm) containing various stages of development up to ready-to-hatch juveniles 2.5 mm in length. Based on their morphology and development in egg masses maintained in the laboratory, the embryonic period for B. hodgsoni is estimated to be up to 10 years, and for D. kerguelenensis 13 months. Thus, B. hodgsoni has the largest egg capsules and probably the largest hatchlings of any mollusc. Chemical analyses of D. kerguelenensis egg masses showed no trace of terpenoid acylglycerols, although these compounds were present in field-collected juveniles and adults. None of four sponges that likely serve as food for D. kerguelenensis had the glycerides, or their precursors, found in the nudibranch.


Sponge Digestive Gland Embryonic Period Capsule Element Early Juvenile 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Y. Grzymbowski, L. Núñez-Pons, C. Debenham, M. Lavaleye, M. Rauschert, U. Jacobs, K. Beyer, T. Brey, W. Arntz, and the crew of the RV Polarstern for their help during sampling and rearing of the nudibranchs. Thanks are due to J. Cristobo, J. Vázquez, and the crew of BIO Las Palmas for their support while diving at Livingston Is. Funding was provided by the Spanish Government through the ECOQUIM (REN2003-00545, REN2002-12006E ANT, CGL2004-03356/ANT), ACTIQUIM (CGL2007-65453, CTM2010-17415/ANT), and DISTANTCOM (CTM2013-42667/ANT) projects. J. Moles was supported by a PhD grant from the Spanish Government (MEC; BES-2011-045325). This work is part of the AntEco (State of the Antarctic Ecosystem) Scientific Research Programme.

Compliance with ethical standards


This study was funded by the Spanish Government through the ECOQUIM (REN2003-00545, REN2002-12006E ANT, CGL2004-03356/ANT), ACTIQUIM (CGL2007-65453, CTM2010-17415/ANT), and DISTANTCOM (CTM2013-42667/ANT) Projects. J. Moles was supported by a PhD Grant of the Spanish Government (MEC; BES-2011-045325).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Informed consent

 “Informed consent was obtained from all individual participants included in the study.”

Supplementary material

227_2017_3143_MOESM1_ESM.pdf (201 kb)
Supplementary material 1 (PDF 201 kb)
227_2017_3143_MOESM2_ESM.pdf (119 kb)
Supplementary material 2 (PDF 119 kb)


  1. Animal Base Project Group (2016) 2005–2016 Animal Base. Early zoological literature online. World wide web electronic publication Accessed 01 Dec 2016
  2. Avila C, Iken K, Fontana A, Cimino G (2000) Chemical ecology of the Antarctic nudibranch Bathydoris hodgsoni Eliot, 1907: defensive role and origin of its natural products. J Exp Mar Bio Ecol 252:27–44CrossRefGoogle Scholar
  3. Avila C, Núñez-Pons L, Moles J (in press) From the tropics to the poles: chemical defensive strategies in sea slugs (Mollusca: Heterobranchia). In: Puglisi-Weening M, Becerro MA, Paul VJ (Eds) Chemical ecology: the ecological impacts of marine natural products. Taylor & Francis GroupGoogle Scholar
  4. Bergh R (1884) Report on the nudibranchiata. Chall Rep Zool 10:1–151Google Scholar
  5. Blunt J, Copp BR, Keyzers R, Munro M, Prinsep M (2016) Marine natural products. Nat Prod Rep 33:382–431. doi: 10.1039/C4NP00144C CrossRefGoogle Scholar
  6. Chaban EM (2016) New genus of opisthobranch molluscs Antarctophiline gen. nov. (Cephalaspidea: Philinoidea) from the cooperation sea, Antarctica. Ruthenica 26:49Google Scholar
  7. Cimino G, Ghiselin MT (2009) Chemical defense and the evolution of opisthobranch gastropods. Proc Calif Acad Sci 60:175–422Google Scholar
  8. Clark KB, Goetzfried A (1978) Zoogeographic influences on development patterns of North Atlantic Ascoglossa and Nudibranchia, with a discussion of factors affecting egg size and number. J Molluscan Stud 44:283–294Google Scholar
  9. Clarke A (1992) Is there a latitudinal diversity cline in the sea? Trends Ecol Evol 7:286–287. doi: 10.1016/0169-5347(92)90222-W CrossRefGoogle Scholar
  10. Clarke A (2003) Costs and consequences of evolutionary temperature adaptation. Trends Ecol Evol 18:573–581. doi: 10.1016/j.tree.2003.08.007 CrossRefGoogle Scholar
  11. Clarke A (2008) Antarctic marine benthic diversity: patterns and processes. J Exp Mar Bio Ecol 366:48–55CrossRefGoogle Scholar
  12. Clarke A, Aronson RB, Crame JA, Gili J-M, Blake DB (2004) Evolution and diversity of the benthic fauna of the Southern Ocean continental shelf. Antarct Sci 16:559–568CrossRefGoogle Scholar
  13. Cutignano A, Zhang W, Avila C, Cimino G, Fontana A (2011) Intrapopulation variability in the terpene metabolism of the Antarctic opisthobranch mollusc Austrodoris kerguelenensis. Eur J Org Chem 2011:5383–5389. doi: 10.1002/ejoc.201100552 CrossRefGoogle Scholar
  14. Dayton PK, Mordida BJ, Bacon F (1994) Polar marine communities. Am Zool 34:90–99Google Scholar
  15. Diyabalanage T, Iken KB, McClintock JB, AmslerCD Baker BJ (2010) Palmadorins A-C, diterpene glycerides from the Antarctic nudibranch Austrodoris kerguelenensis. J Nat Prod 73:416–421. doi: 10.1021/np900617m CrossRefGoogle Scholar
  16. Eliot C (1907) Mollusca IV Nudibranchiata. National Antarctic expedition 1901–1904. Nat Hist 2:1–28Google Scholar
  17. Fontana A (2006) Biogenetic proposals and biosynthetic studies on secondary metabolites of marine molluscs. In: Cimino G, Gavagnin M (eds) Marine molecular biotechnology, series progress in molecular and subcellular biology, vol. Molluscs. Springer, Heidelberg, pp 303–332Google Scholar
  18. Gavagnin M, Trivellone E, Castelluccio F, Cimino G (1995) Glyceryl ester of a new halimane diterpenoic acid from the skin of the Antarctic nudibranch Austrodoris kerguelenensis. Tetrahedron Lett 36:7319–7322CrossRefGoogle Scholar
  19. Gavagnin M, Castelluccio F, Cimino G (1999a) Austrodorin-A and -B: first tricyclic diterpenoid 2′-monoglyceryl esters from an Antarctic nudibranch. Tetrahedron Lett 40:8471–8475CrossRefGoogle Scholar
  20. Gavagnin M, De Napoli A, Cimino G, Iken K, Avila C, García FJ (1999b) Absolute configuration of diterpenoid diacylglycerols from the Antarctic nudibranch Austrodoris kerguelenensis. Tetrahedron 10:2647–2650. doi: 10.1016/S0957-4166(99)00273-6 CrossRefGoogle Scholar
  21. Gavagnin M, Carbone M, Mollo E, Cimino G (2003a) Austrodoral and austrodoric acid: nor-sesquiterpenes with a new carbon skeleton from the Antarctic nudibranch Austrodoris kerguelenensis. Tetrahedron Lett 44:1495–1498CrossRefGoogle Scholar
  22. Gavagnin M, Carbone M, Mollo E, Cimino G (2003b) Further chemical studies on the Antarctic nudibranch Austrodoris kerguelenensis: new terpenoid acylglycerols and revision of the previous stereochemistry. Tetrahedron 59:5579–5583. doi: 10.1016/S0040-4020(03)00775-0 CrossRefGoogle Scholar
  23. Gibson RAY, Thompson TE, Robilliard GA (1970) Structure of the spawn of an Antarctic dorid nudibranch Austrodoris macmurdensis Odhner. Proc Malacol Soc London 39:221–226Google Scholar
  24. Hain S (1989) Beiträge zur Biologie der beschalten Mollusken (Kl. Bremen University, Gastropoda and Bivalvia) des Weddellmeeres, AntarktisGoogle Scholar
  25. Hain S (1992) Maintenance and culture of living benthic molluscs from high Antarctic shelf areas. Aquac Fish Manag 23:1–11Google Scholar
  26. Hain S, Arnaud PM (1992) Notes on the reproduction of high-Antarctic molluscs from the Weddell Sea. Polar Biol 12:303–312CrossRefGoogle Scholar
  27. Iken K, Avila C, Ciavatta ML, Fontana A, Cimino G (1998) Hodgsonal, a new drimane sesquiterpene from the mantle of the Antarctic nudibranch Bathydoris hodgsoni. Tetrahedron Lett 39:5635–5638. doi: 10.1016/S0040-4039(98)01095-8 CrossRefGoogle Scholar
  28. Iken K, Avila C, Fontana A, Gavagnin M (2002) Chemical ecology and origin of defensive compounds in the Antarctic nudibranch Austrodoris kerguelenensis (Opisthobranchia: Gastropoda). Mar Biol 141:101–109. doi: 10.1007/s00227-002-0816-7 CrossRefGoogle Scholar
  29. Klussmann-Kolb A, Wägele H (2001) On the fine structure of opisthobranch egg masses (Mollusca, Gastropoda). Zool Anz 240:101–118CrossRefGoogle Scholar
  30. Levin LA, Bridges TS (1995) Pattern and diversity in reproduction and development. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC Press, FloridaGoogle Scholar
  31. Martynov AV (2011) From “Tree-Thinking” to “Cycle-Thinking”: ontogenetic systematics of nudibranch molluscs. Thalassas 27:193–224Google Scholar
  32. Maschek JA, Mevers E, Diyabalanage T, Chen L, Ren Y, McClintock JB, Amsler CD, Wu J, Baker BJ (2012) Palmadorin chemodiversity from the Antarctic nudibranch Austrodoris kerguelenensis and inhibition of Jak2/STAT5-dependent HEL leukemia cells. Tetrahedron 68:9095–9104. doi: 10.1016/j.tet.2012.08.045 CrossRefGoogle Scholar
  33. McDonald GR, Nybakken JW (1997) A list of the worldwide food habits of nudibranchs. I. Introduction and the suborder Arminacea. Veliger 40:1–764Google Scholar
  34. Moles J, Wägele H, Cutignano A, Fontana A, Avila C (2016) Distribution of granuloside in the Antarctic nudibranch Charcotia granulosa (Gastropoda: Heterobranchia: Charcotiidae). Mar Biol 163:1–11CrossRefGoogle Scholar
  35. Moran AL, Woods HA (2012) Why might they be giants? Towards an understanding of polar gigantism. J Exp Biol 215:1995–2002CrossRefGoogle Scholar
  36. Palmer AR (1994) Temperature sensitivity, rate of development, and time to maturity: geographic variation in laboratory-reared Nucella and a cross-phyletic overview. In: Wilson WH (ed) Reproduction and development of marine invertebrates. Johns Hopkins University Press, Baltimore, pp 177–194Google Scholar
  37. Pearse JS, McClintock JB, Bosch I (1991) Reproduction of Antarctic benthic marine invertebrates: tempos, modes, and timing. Am Zool 31:65–80CrossRefGoogle Scholar
  38. Peck LS, Clarke A, Chapman AL (2006) Metabolism and development of pelagic larvae of Antarctic gastropods with mixed reproductive strategies. Mar Ecol Prog Ser 318:213–220. doi: 10.3354/meps318213 CrossRefGoogle Scholar
  39. Peck LS, Powell DK, Tyler PA (2007) Very slow development in two Antarctic bivalve molluscs, the infaunal clam Laternula elliptica and the scallop Adamussium colbecki. Mar Biol 150:1191–1197. doi: 10.1007/s00227-006-0428-8 CrossRefGoogle Scholar
  40. Rivas LR (1964) A reinterpretation of the concepts “sympatric” and “allopatric” with proposal of the additional terms “syntopic” and “allotopic”. Syst Biol 13:42–43CrossRefGoogle Scholar
  41. Ros J (1981) Desarrollo y estrategias bionómicas en los Opistobranquios. Oecologia Aquat 5:147–183Google Scholar
  42. Saunders WB (1984) Nautilus growth and longevity: evidence from marked and recaptured animals. Science 224:990–992. doi: 10.1126/science.224.4652.990 CrossRefGoogle Scholar
  43. Schaefer K (1996) Review of data on cephalaspid reproduction, with special reference to the genus Haminaea (Gastropoda, Opisthobranchia). Ophelia 45:17–37CrossRefGoogle Scholar
  44. Seager JR (1979) Reproductive biology of the Antarctic opistobranch Philine gibba Strebel. J Exp Mar Bio Ecol 41:51–74CrossRefGoogle Scholar
  45. Thompson TE (1967) Direct development in a nudibranch, Cadlina laevis, with a discussion of developmental processes in opisthobranchia. J Mar Biol Assoc UK 47:1–22CrossRefGoogle Scholar
  46. Thompson TE, Jarman GM (1986) Factors bearing upon egg size and embryonic period in opisthobranch molluscs. Bol Zool Univ São Paulo 10:9–18Google Scholar
  47. Thorson G (1936) The larval development, growth, and metabolism of arctic marine bottom invertebrates compared with those of other seas. Medd Grönl 100:1–155Google Scholar
  48. Todd CD, Doyle RW (1981) Reproductive strategies of marine benthic invertebrates: a settlement-timing hypothesis. Mar Ecol Prog Ser 4:75–83. doi: 10.3354/meps004075 CrossRefGoogle Scholar
  49. Ungvari Z, Csiszar A, Sosnowska D, Philipp EE, Campbell CM, McQuary PR, Chow TT, Coelho M, Didier ES, Gelino S, Holmbeck MA, Kim I, Levy E, Sonntag WE, Whitby PW, Austad SN (2012) Testing predictions of the oxidative stress hypothesis of aging using a novel invertebrate model of longevity: the giant clam (Tridacna derasa). J Gerontol A Biol Sci Med Sci. doi: 10.1093/gerona/gls159 Google Scholar
  50. Valdés Á (2002) Phylogenetic systematics of “Bathydoris” s.l. Bergh, 1884 (Mollusca, Nudibranchia), with the description of a new species from New Caledonian deep waters. Can J Zool 80:1084–1099. doi: 10.1139/Z02-085 CrossRefGoogle Scholar
  51. Wägele H (1989a) On the morphology and ultrastucture of some egg-clutches of Antarctic nudibranchs (Gastropoda). Zool Anz 222:225–243Google Scholar
  52. Wägele H (1989b) Diet of some Antarctic nudibranchs (Gastropoda, Opisthobranchia, Nudibranchia). Mar Biol 100:439–441CrossRefGoogle Scholar
  53. Wägele H (1989c) A revision of the Antarctic species of Bathydoris Bergh, 1884 and comparison with other known Bathydoris (Opisthobranchia, Nudibranchia). J Molluscan Stud 55:343–364CrossRefGoogle Scholar
  54. Wägele H (1996) On egg clutches of some Antarctic Opisthobranchia. Molluscan Reprod Malacol Rev Suppl. 6:21–30Google Scholar
  55. Wägele H (1997) Histological investigation of some organs and specialised cellular structures in Opisthobranchia (Gastropoda) with the potential to yield phylogenetically significant characters. Zool Anz 236:119–131Google Scholar
  56. Wilson NG, Schrödl M, Halanych KM (2009) Ocean barriers and glaciation: evidence for explosive radiation of mitochondrial lineages in the Antarctic sea slug Doris kerguelenensis (Mollusca, Nudibranchia). Mol Ecol 18:965–984CrossRefGoogle Scholar
  57. Wilson NG, Maschek JA, Baker BJ (2013) A species flock driven by predation? Secondary metabolites support diversification of slugs in Antarctica. PLoS One 8:e80277. doi: 10.1371/journal.pone.0080277 CrossRefGoogle Scholar
  58. Wray GA, Raff RA (1991) The evolution of developmental strategy in marine invertebrates. Trends Ecol Evol 6:45–50. doi: 10.1016/0169-5347(91)90121-D CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Evolutionary Biology, Ecology, and Environmental Sciences and Biodiversity Research Institute (IrBIO)University of BarcelonaBarcelonaSpain
  2. 2.Zoological Research Museum Alexander KoenigBonnGermany
  3. 3.Bio-Organic Chemistry Unit, Istituto di Chimica BiomolecolareConsiglio Nazionale delle RicerchePozzuoliItaly

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