Advertisement

Marine Biology

, Volume 156, Issue 4, pp 753–761 | Cite as

Laboratory culture of the aeolid nudibranch Spurilla neapolitana (Mollusca, Opisthobranchia): life history aspects

  • Ami SchlesingerEmail author
  • Rotem Goldshmid
  • Michael G. Hadfield
  • Esti Kramarsky-Winter
  • Yossi Loya
Original Paper

Abstract

Spurilla neapolitana from the Eastern Mediterranean was cultured in a self-sustained, temperature-controlled laboratory culture system, and its life cycle is described. Adults were collected from three field sites situated 120 km apart, along the Israeli Mediterranean coastline, between March 2006 and August 2007. Cultures of the life-cycle stages were raised at 24°C. S. neapolitana deposited white, coiled, spiral egg masses containing zygotes. Veliger larvae hatched 3.0 ± 0.4 days post oviposition. The veliger larvae are obligatory planktotrophs, with a minimal larval phase of 22 days. In the lab, larvae settled and metamorphosed following exposure to metabolites derived from distinct prey sea anemone species. Reproductive maturity was reached 42 ± 5 days post metamorphosis, resulting in a laboratory generation time of 67 days (egg to egg). The average life span of reproductive specimens in this study was 157 ± 13 days post-oviposition and they reached a length of 7–10 cm. During this period, an average adult deposited ca. 40 × 106 zygotes. This species has several characteristics that suggest it will be a useful model for laboratory-oriented research.

Keywords

Shell Diameter Larval Metamorphosis Competent Larva Veliger Larva Anemone Species 

Notes

Acknowledgments

The authors would like to thank H. Ohana from the Ruppin Academic Center, School of Marine Sciences, Michmoret for assistance with the sea water systems, S. Kelly and C. Tran from the Kewalo Marine Laboratory, Hawaii for their helpful tutorials on nudibranch culture, R. Holtzman and S. Einbinder for advice on the statistical analysis and R. Yavetz for assistance with the field work. We would also like to thank M. Ucko at the National Centre for Mariculture, Eilat for the alga inoculates and invaluable advice. We would like to thank N. Paz for helpful commenting on this manuscript. The critical reading and constructive suggestions of three anonymous reviewers are gratefully acknowledged. This work was supported in part by the Tel-Aviv University Fund for Applied Research and in part by the Raynor Chair for Environmental Conservation Research (to YL). All experiments undertaken within this study comply with the current laws of Israel, the country in which they were performed.

Supplementary material

227_2009_1126_MOESM1_ESM.doc (152 kb)
Supplementary material 1 (DOC 151 kb)

References

  1. Bonar DB (1976) Molluscan metamorphosis: a study in tissue transformation. Am Zool 16:573–591CrossRefGoogle Scholar
  2. Bonar DB, Hadfield MG (1974) Metamorphosis of the marine gastropod Phestilla sibogae Bergh (Nudibranchia: Aeolidacea). 1. Light and electron microscopic analysis of larval and metamorphic stages. J Exp Mar Biol Ecol 16:221–255CrossRefGoogle Scholar
  3. Carroll DJ, Kempf SC (1990) Laboratory culture of the aeolid nudibranch Berghia verrucicornis (Mollusca, Opisthobranchia)—some aspects of its development and life-history. Biol Bull 179:243–253CrossRefGoogle Scholar
  4. Chia F-S (1971) Oviposition, fecundity, and larval development of three sacoglossan opisthobranch from the Northumberland coast, England. Veliger 13:319–325Google Scholar
  5. Cohen A, Shappir J, Yitzchaik S, Spira ME (2006) Experimental and theoretical analysis of neuron-transistor hybrid electrical coupling: the relationships between the electro-anatomy of cultured Aplysia neurons and the recorded field potentials. Biosens Bioelectron 22:656–663CrossRefGoogle Scholar
  6. Faucci A, Toonen RJ, Hadfield MG (2007) Host shift and speciation in a coral-feeding nudibranch. Proc R Soc Lond B 274:111–119CrossRefGoogle Scholar
  7. Frick K (2003) Response in nematocyst uptake by the nudibranch Flabellina verrucosa to the presence of various predators in the southern Gulf of Maine. Biol Bull 205:367–376CrossRefGoogle Scholar
  8. Greenwood PG, Mariscal RN (1984) The utilization of cnidarian nematocysts by aeolid nudibranchs: nematocyst maintenance and release in Spurilla. Tissue Cell 16:719–730CrossRefGoogle Scholar
  9. Hadfield MG (1984) Settlement requirements of marine molluscan larvae: new data on chemical and genetic roles. Aquaculture 30:283–298CrossRefGoogle Scholar
  10. Hadfield MG, Miller SE (1987) On developmental patterns of opisthobranchs. Am Malacol Bull 5:197–214Google Scholar
  11. Hadfield MG, Paul VJ (2001) Natural chemical cues for settlement and metamorphosis of marine invertebrate larvae. In: McClintock JB, Baker W (eds) Marine chemical ecology. CRC Press, Boca RatonGoogle Scholar
  12. Hadfield MG, Pennington JT (1990) Nature of the metamorphic signal and its internal transduction in the larvae of the nudibranch, Phestilla siboge. Bull Mar Sci 46:455–464Google Scholar
  13. Hadfield MG, Switzer-Dunlap M (1984) The mollusca. Academic Press, Inc., OrlandoGoogle Scholar
  14. Harrigan JF, Alkon DL (1978) Larval rearing metamorphosis, growth and reproduction of the eolid nudibranch Hermissenda crassicornis (Escholtz, 1831) (Gastropoda: Opisthobranchia). Biol Bull 154:430–439CrossRefGoogle Scholar
  15. Hurst A (1967) The egg masses and veligers of thirty northeast Pacific opisthobranchs. Veliger 9:255–288Google Scholar
  16. Ilan M (1995) Reproductive biology, taxonomy, and aspects of chemical ecology of Latrunculiidae (Porifera). Biol Bull 188:306–312CrossRefGoogle Scholar
  17. Kandel ER (1979) Behavioral biology of Aplysia. W. H. Freeman and Co., San FranciscoGoogle Scholar
  18. Kress N, Frede Thingstad T, Pitta P, Psarra S, Tanaka T, Zohary T, Groom S, Herut B, Fauzi C, Mantoura R, Polychronaki T, Rassoulzadegan F, Spyres G (2005) Effect of P and N addition to oligotrophic Eastern Mediterranean waters influenced by near-shore waters: a microcosm experiment. Deep Sea Res Part II Top Stud Oceanogr 52:3054–3059CrossRefGoogle Scholar
  19. Kriegstein AR (1977a) Development of the nervous system of Aplysia californica. PNAS 74:375–378CrossRefGoogle Scholar
  20. Kriegstein AR (1977b) Stages in the post-hatching development of Aplysia californica. J Exp Zool 199:275–288CrossRefGoogle Scholar
  21. Kriegstein AR, Castellucci V, Kandel ER (1974) Metamorphosis of Aplysia californica in laboratory culture. PNAS 71:3654–3658CrossRefGoogle Scholar
  22. Kuzirian A, Capo T, McPhie D, Tamse CT (1999) The sea slug, Hermissenda crassicornis: phylogeny, mariculture, and use as a model system for neurobiological research on learning and memory. Mar Mod Elec Rec. https://doi.org/www.mbl.edu/html/BB/MMER/KUZ/KuzTit.html
  23. MEDAR Group (2002) MEDATLAS/2002 database. Mediterranean and Black Sea database of temperature salinity and bio-chemical parameters. Climatological Atlas. IFREMER Edition (4 CD roms)Google Scholar
  24. McDonald GR, Nybakken JW (1996) A list of the worldwide food habits of nudibranchs. https://doi.org/people.ucsc.edu/~mcduck/nudifood.htm
  25. Mebs D (1994) Anemonefish symbiosis: vulnerability and resistance of fish to the toxin of the sea anemone. Toxicon 32:1059–1068CrossRefGoogle Scholar
  26. Miller SE (1993) Larval period and its influence on post-larval life-history—comparison of lecithotrophy and facultative planktotrophy in the aeolid nudibranch Phestilla sibogae. Mar Biol 117:635–645CrossRefGoogle Scholar
  27. Miller SE, Hadfield MG (1986) Ontogeny of phototaxis and metamorphic competence in larvae of the nudibranch Phestilla sibogae Bergh (Gastropoda: Opisthobranchia). J Exp Mar Biol Ecol 97:95–112CrossRefGoogle Scholar
  28. Perron FE, Turner RD (1977) Development, metamorphosis, and natural history of the nudibranch Doridella obscura Verill (Corambidae: Opisthobranchia). J Exp Mar Biol Ecol 27:171–185CrossRefGoogle Scholar
  29. Rudman WB (1999) Spurilla neapolitana (Delle Chiaje, 1823). Australian Museum, Sydney, https://doi.org/www.seaslugforum.net/factsheet.cfm?base=spurneap
  30. Schlesinger A, Kramarsky-Winter E, Loya Y (2007) Method and apparatus for propagating benthic marine invertebrates. World Intellectual Property OrganizationGoogle Scholar
  31. Schlesinger A, Kramarski-Winter E, Loya Y (2009) Active nematocyst isolation via nudibranchs. Mar Biotechnol (in press)Google Scholar
  32. Strathman MF (1987) Reproduction and development of marine invertebrates of the northern pacific coast, data and methods for the study of eggs, embryos and larvae. University of Washington Press, Seattle and LondonGoogle Scholar
  33. Switzer-Dunlap M, Hadfield MG (1977) Observations on development, larval growth and metamorphosis of four species of Aplisiidae (Gastropod: Opisthobranchia) in laboratory culture. J Exp Mar Biol Ecol 29:245–261CrossRefGoogle Scholar
  34. Switzer-Dunlap M, Hadfield MG (1979) Reproductive patterns of Hawaiian aplysiid gastropods. University of South Carolina Press, ColombiaGoogle Scholar
  35. Taylor FJR (1983) Some eco-evolutionary aspects of intracellular symbiosis. Int Rev Cytol Suppl 14:1–28Google Scholar
  36. Thompson TE (1961) The importance of larval shell in the classification of the Sacoglossa and Acoela (Gastropoda Opisthobranchia). Proc Malacol Soc Lond 34:233–238Google Scholar
  37. Todd CD (1991) Larval strategies of nudibranch molluscs: similar means to the same end? Malacologia 32:272–289Google Scholar
  38. Todd CD, Lambert WJ, Davies J (2001) Some perspectives on the biology and ecology of nudibranch molluscs: generalizations and variations on the theme that prove the rule. Boll Malacol 37:105–120Google Scholar
  39. Yavetz R (2007) The effect of ambient temperature on larval development and population dynamics of Spurilla neapolitana. George S. Wise Faculty of Life Science Graduate School Thesis, Ramat-AvivGoogle Scholar
  40. Zohary T, Herut B, Krom MD, Fauzi C, Mantoura R, Pitta P, Psarra S, Rassoulzadegan F, Stambler N, Tanaka T, Frede Thingstad T, Malcolm S, Woodward E (2005) P-limited bacteria but N and P co-limited phytoplankton in the Eastern Mediterranean—a microcosm experiment. Deep Sea Res Part II Top Stud Oceanogr 52:3011–3018CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Ami Schlesinger
    • 1
    • 2
    Email author
  • Rotem Goldshmid
    • 3
  • Michael G. Hadfield
    • 4
  • Esti Kramarsky-Winter
    • 1
  • Yossi Loya
    • 1
  1. 1.Department of ZoologyTel Aviv UniversityTel AvivIsrael
  2. 2.School of Marine SciencesRuppin Academic CenterMichmoretIsrael
  3. 3.Faculty of EducationQueens UniversityKingstonCanada
  4. 4.Kewalo Marine LaboratoryUniversity of Hawaii at ManoaHonoluluUSA

Personalised recommendations