Skip to main content

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

Marine Biology volume 164, Article number: 114 (2017) Cite this article

Abstract

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.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Animal Base Project Group (2016) 2005–2016 Animal Base. Early zoological literature online. World wide web electronic publication http://www.animalbase.uni-goettingen.de. Accessed 01 Dec 2016

  • 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 252:27–44

    CAS  Article  Google Scholar 

  • 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 Group

  • Bergh R (1884) Report on the nudibranchiata. Chall Rep Zool 10:1–151

    Google Scholar 

  • Blunt J, Copp BR, Keyzers R, Munro M, Prinsep M (2016) Marine natural products. Nat Prod Rep 33:382–431. doi:10.1039/C4NP00144C

    CAS  Article  Google Scholar 

  • Chaban EM (2016) New genus of opisthobranch molluscs Antarctophiline gen. nov. (Cephalaspidea: Philinoidea) from the cooperation sea, Antarctica. Ruthenica 26:49

    Google Scholar 

  • Cimino G, Ghiselin MT (2009) Chemical defense and the evolution of opisthobranch gastropods. Proc Calif Acad Sci 60:175–422

    Google Scholar 

  • 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 44:283–294

    Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • Clarke A (2003) Costs and consequences of evolutionary temperature adaptation. Trends Ecol Evol 18:573–581. doi:10.1016/j.tree.2003.08.007

    Article  Google Scholar 

  • Clarke A (2008) Antarctic marine benthic diversity: patterns and processes. J Exp Mar Bio Ecol 366:48–55

    Article  Google Scholar 

  • 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 16:559–568

    Article  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • Dayton PK, Mordida BJ, Bacon F (1994) Polar marine communities. Am Zool 34:90–99

    Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • Eliot C (1907) Mollusca IV Nudibranchiata. National Antarctic expedition 1901–1904. Nat Hist 2:1–28

    Google Scholar 

  • 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 303–332

    Google Scholar 

  • 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 36:7319–7322

    CAS  Article  Google Scholar 

  • Gavagnin M, Castelluccio F, Cimino G (1999a) Austrodorin-A and -B: first tricyclic diterpenoid 2′-monoglyceryl esters from an Antarctic nudibranch. Tetrahedron Lett 40:8471–8475

    CAS  Article  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • 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 44:1495–1498

    CAS  Article  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • Gibson RAY, Thompson TE, Robilliard GA (1970) Structure of the spawn of an Antarctic dorid nudibranch Austrodoris macmurdensis Odhner. Proc Malacol Soc London 39:221–226

    Google Scholar 

  • Hain S (1989) Beiträge zur Biologie der beschalten Mollusken (Kl. Bremen University, Gastropoda and Bivalvia) des Weddellmeeres, Antarktis

    Google Scholar 

  • Hain S (1992) Maintenance and culture of living benthic molluscs from high Antarctic shelf areas. Aquac Fish Manag 23:1–11

    Google Scholar 

  • Hain S, Arnaud PM (1992) Notes on the reproduction of high-Antarctic molluscs from the Weddell Sea. Polar Biol 12:303–312

    Article  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Klussmann-Kolb A, Wägele H (2001) On the fine structure of opisthobranch egg masses (Mollusca, Gastropoda). Zool Anz 240:101–118

    Article  Google Scholar 

  • Levin LA, Bridges TS (1995) Pattern and diversity in reproduction and development. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC Press, Florida

    Google Scholar 

  • Martynov AV (2011) From “Tree-Thinking” to “Cycle-Thinking”: ontogenetic systematics of nudibranch molluscs. Thalassas 27:193–224

    Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • McDonald GR, Nybakken JW (1997) A list of the worldwide food habits of nudibranchs. I. Introduction and the suborder Arminacea. Veliger 40:1–764

  • 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 163:1–11

    CAS  Article  Google Scholar 

  • Moran AL, Woods HA (2012) Why might they be giants? Towards an understanding of polar gigantism. J Exp Biol 215:1995–2002

    Article  Google Scholar 

  • 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 177–194

    Google Scholar 

  • Pearse JS, McClintock JB, Bosch I (1991) Reproduction of Antarctic benthic marine invertebrates: tempos, modes, and timing. Am Zool 31:65–80

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Rivas LR (1964) A reinterpretation of the concepts “sympatric” and “allopatric” with proposal of the additional terms “syntopic” and “allotopic”. Syst Biol 13:42–43

    Article  Google Scholar 

  • Ros J (1981) Desarrollo y estrategias bionómicas en los Opistobranquios. Oecologia Aquat 5:147–183

    Google Scholar 

  • Saunders WB (1984) Nautilus growth and longevity: evidence from marked and recaptured animals. Science 224:990–992. doi:10.1126/science.224.4652.990

    CAS  Article  Google Scholar 

  • Schaefer K (1996) Review of data on cephalaspid reproduction, with special reference to the genus Haminaea (Gastropoda, Opisthobranchia). Ophelia 45:17–37

    Article  Google Scholar 

  • Seager JR (1979) Reproductive biology of the Antarctic opistobranch Philine gibba Strebel. J Exp Mar Bio Ecol 41:51–74

    Article  Google Scholar 

  • Thompson TE (1967) Direct development in a nudibranch, Cadlina laevis, with a discussion of developmental processes in opisthobranchia. J Mar Biol Assoc UK 47:1–22

    Article  Google Scholar 

  • Thompson TE, Jarman GM (1986) Factors bearing upon egg size and embryonic period in opisthobranch molluscs. Bol Zool Univ São Paulo 10:9–18

    Google Scholar 

  • Thorson G (1936) The larval development, growth, and metabolism of arctic marine bottom invertebrates compared with those of other seas. Medd Grönl 100:1–155

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 

  • 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

    Article  Google Scholar 

  • Wägele H (1989a) On the morphology and ultrastucture of some egg-clutches of Antarctic nudibranchs (Gastropoda). Zool Anz 222:225–243

    Google Scholar 

  • Wägele H (1989b) Diet of some Antarctic nudibranchs (Gastropoda, Opisthobranchia, Nudibranchia). Mar Biol 100:439–441

    Article  Google Scholar 

  • Wägele H (1989c) A revision of the Antarctic species of Bathydoris Bergh, 1884 and comparison with other known Bathydoris (Opisthobranchia, Nudibranchia). J Molluscan Stud 55:343–364

    Article  Google Scholar 

  • Wägele H (1996) On egg clutches of some Antarctic Opisthobranchia. Molluscan Reprod Malacol Rev Suppl. 6:21–30

    Google Scholar 

  • 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 236:119–131

    Google Scholar 

  • 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 18:965–984

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Department of Evolutionary Biology, Ecology, and Environmental Sciences and Biodiversity Research Institute (IrBIO), University of Barcelona, Avinguda Diagonal 643, 08028, Barcelona, Catalonia, Spain

    Juan Moles, Manuel Ballesteros & Conxita Avila

  2. Zoological Research Museum Alexander Koenig, Adenauerallee 160, 53113, Bonn, Germany

    Heike Wägele

  3. Bio-Organic Chemistry Unit, Istituto di Chimica Biomolecolare, Consiglio Nazionale delle Ricerche, Via Campi Flegrei, 34, 80078, Pozzuoli, Naples, Italy

    Adele Cutignano & Angelo Fontana

Authors
  1. Juan Moles
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heike Wägele
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adele Cutignano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Angelo Fontana
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Manuel Ballesteros
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Conxita Avila
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juan Moles.

Ethics declarations

Funding

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.”

Additional information

Reviewed by undisclosed experts.

Responsible Editor: J. Grassle.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 201 kb)

Supplementary material 2 (PDF 119 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Moles, J., Wägele, H., Cutignano, A. et al. Giant embryos and hatchlings of Antarctic nudibranchs (Mollusca: Gastropoda: Heterobranchia). Mar Biol 164, 114 (2017). https://doi.org/10.1007/s00227-017-3143-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-017-3143-8

Keywords

  • Sponge
  • Digestive Gland
  • Embryonic Period
  • Capsule Element
  • Early Juvenile