Polar Biology

, Volume 36, Issue 1, pp 1–11 | Cite as

An unusual hermaphrodite reproductive trait in the Antarctic brooding bivalve Lissarca miliaris (Philobryidae) from the Scotia Sea, Southern Ocean

Original Paper

Abstract

The Antarctic marine environment is extreme in its low temperatures and short periods of primary productivity. Invertebrates must therefore adapt to maximise reproductive output where low temperature and limited food slow larval development. Brooding is a common reproductive trait in Antarctic marine bivalves; larval development occurs within the mantle cavity, and larvae are released as fully developed young. Lissarca miliaris is a small, short-lived, shallow-water brooding bivalve of circum-Antarctic distribution and found most abundant in the sub-Antarctic Magellan Region and islands of the Scotia Arc. Here, an unusual hermaphrodite reproductive trait is described for L. miliaris from King George Island (62°14′S, 58°38′W) and Signy Island (60°42′S, 45°36′W), Antarctica, using histological and dissection techniques. Specimens demonstrate simultaneous and sequential hermaphrodite traits; male and female gonads develop simultaneously, but the production of oocytes is reduced while testes are ripe. Functional females are more abundant in specimens above 3 mm shell length, although male reproductive tissue persists and functional males are found in all size classes. The number of previtellogenic oocytes produced by far exceeds the number of oocytes extruded and brooded, which may indicate an ancestral link to a planktotrophic past. Hermaphroditism in L. miliaris maximises reproductive efficiency in a short-lived species, in which the female’s capacity to brood its young is limited, and demonstrates a specialised adaptation to a cold stenothermal and food-limited environment prevailing in the Southern Ocean.

Keywords

Antarctica Invertebrate reproduction Cold adaption Hermaphrodite Early ontogeny 

Notes

Acknowledgments

Adam J. Reed was supported through an NERC PhD studentship. Thanks are due to captain and crew of R/V Polarstern for assistance at sea, Prof. Paul Tyler for helpful discussion and interpretation of the results and Huw Griffiths for help with maps. The authors would also like to thank the three anonymous reviewers for helping to improve this manuscript. This study is part of the British Antarctic Survey Polar Science for Planet Earth Programme.

References

  1. Aldea C, Olabarria C, Troncoso JS (2008) Bathymetric zonation and diversity gradient of gastropods and bivalves in West Antarctica from the South Shetland Islands to the Bellingshausen Sea. Deep Sea Res I 55:350–368CrossRefGoogle Scholar
  2. Arntz WE (1999) Magellan-Antarctic: ecosystems that drifted apart. Summary review. Sci Mar 63:503–511Google Scholar
  3. Arntz WE, Brey T (2003) The expedition ANTARKTIS XIX/5 (LAMPOS) of RV Polarstern in 2002. Rep Polar Mar Res 462:1–120Google Scholar
  4. Arntz WE, Gili JM (2001) A case for tolerance in marine ecology: let us not put out the baby with the bathwater. Sci Mar 65:283–299CrossRefGoogle Scholar
  5. Arntz WE, Gutt J, Klages M (1997) Antarctic marine biodiversity: an overview. In: Battaglia B, Valencia J, Walton DWH (eds) Antarctic communities: species, structure and survival. Cambridge University Press, Cambridge, pp 3–14Google Scholar
  6. Asif M (1979) Hermaphroditism and sex reversal in the four common oviparous species of oysters from the coast of Karachi. Hydrobiologia 66:49–55CrossRefGoogle Scholar
  7. Barnes DKA, Conlan KE (2007) Disturbance, colonization and development of Antarctic benthic communities. Phil Trans R Soc B Biol Sci 362:11–38CrossRefGoogle Scholar
  8. Beaumont AR, Barnes DA (1992) Aspects of veliger larval growth and byssus drifting of the spat of Pectin maximus and Aequipectin (Chlamys) opercularis. J Mar Sci 49:417–423Google Scholar
  9. Bosch I, Pearse JS (1988) Seasonal pelagic development and juvenile recruitment of the bivalve Laternula elliptica in McMurdo Sound, Antarctica. Am Zool 28:A89Google Scholar
  10. Brey T, Hain S (1992) Growth, reproduction and production of Lissarca notorcadensis (Bivalvia: Philobryidae) in the Weddell Sea, Antarctica. Mar Ecol Prog Ser 82:219–226CrossRefGoogle Scholar
  11. Clarke A, Johnston NM (2003) Antarctic marine benthic diversity. Oceanogr Mar Biol 41:47–114Google Scholar
  12. Clarke A, Holmes LJ, White MG (1988) The annual cycle of temperature, chlorophyll and major nutrients at Signy Island, South Orkney Islands, 1969–82. Br Antarct Surv Bull 80:65–86Google Scholar
  13. Coe WR (1943) Sexual differentiation in mollusks. I. Pelecypods. Q Rev Biol 18:154–164CrossRefGoogle Scholar
  14. Cope T, Linse K (2006) Morphological differences in Lissarca notorcadensis Melvill and Standen, 1907 from the Scotia, Weddell and Ross Seas. Deep Sea Res II 53:903–911CrossRefGoogle Scholar
  15. Dell RK (1964) Antarctic and sub-Antarctic Mollusca: Amphineura, Scaphapoda and Bivalvia. Discov Rep 33:93–250Google Scholar
  16. Dell RK (1972) Antarctic benthos. In: Russell FS, Yonge M (eds) Advances in marine biology, vol X. Academic, London, pp 1–216Google Scholar
  17. Emlet RB, McEdward LR, Strathmann RR (1985) Echinoderm larval ecology viewed from the egg. In: Lawrence J (ed) Echinoderm studies, vol 1. Balkema, Rotterdam, pp 55–136Google Scholar
  18. Gallardo CS, Penchaszadeh PE (2001) Hatching mode and latitude in marine gastropods: revisiting Thorson’s paradigm in the southern hemisphere. Mar Biol 138:547–552CrossRefGoogle Scholar
  19. Ghiselin MT (1969) The evolution of hermaphroditism among animals. Q Rev Biol 44:189–208PubMedCrossRefGoogle Scholar
  20. Guo XM, Hedgecock D, Hershberger WK, Cooper K, Allen SK (1998) Genetic determinants of protandric sex in the Pacific oyster, Crassostrea gigas. Evolution 52:394–402CrossRefGoogle Scholar
  21. Gutt J (2001) On the direct impact of ice on marine benthic communities, a review. Polar Biol 24:553–564CrossRefGoogle Scholar
  22. Hain S, Arnaud PM (1992) Notes on the reproduction of high-Antarctic molluscs from the Weddell Sea. Polar Biol 12:303–312CrossRefGoogle Scholar
  23. Heath DJ (1977) Simultaneous hermaphroditism; cost and benefit. J Theor Biol 64:363–373PubMedCrossRefGoogle Scholar
  24. Held C (2003) Molecular evidence for cryptic speciation within the widespread Antarctic crustacean Ceratoserolis trilobitoides (Crustacea, Isopoda). In: Huiskes AH, Gieskes WW, Rozema J, Schorno RM, van der Vies SM, Wolff WJ (eds) Antarctic biology in a global context. Backhuys, Leiden, pp 135–139Google Scholar
  25. Held C, Wagele JW (2005) Cryptic speciation in the giant Antarctic isopod Glyptonotus antarcticus (Isopoda: Valvifera: Chaetiliidae). Sci Mar 69:175–181CrossRefGoogle Scholar
  26. Heller J (1993) Hermaphroditism in molluscs. Biol J Linn Soc 48:19–42CrossRefGoogle Scholar
  27. Higgs ND, Reed AJ, Hooke R, Honey DJ, Heilmayer O, Thatje S (2009) Growth and reproduction in the Antarctic brooding bivalve Adacnarca nitens (Philobryidae) from the Ross Sea. Mar Biol 156:1073–1081CrossRefGoogle Scholar
  28. Highsmith RC (1985) Floating and algal rafting as potential dispersal mechanisms in brooding invertebrates. Mar Ecol Prog Ser 25:169–179CrossRefGoogle Scholar
  29. Huber M (2010) Lissarca miliaris (Philippi, 1845). In: De Broyer C, Clarke A, Koubbi P, Pakhomov E, Scott F, Vanden Berghe E, Danis B (eds) The SCAR-MarBIN register of Antarctic marine species (RAMS). http://www.scarmarbin.be/rams.php?p=taxdetails&id=197240 on 2011-11-10
  30. Hunter RL, Halanych KM (2008) Evaluating connectivity in the brooding brittle star Astrotoma agassizii across the Drake Passage in the Southern Ocean. J Hered 99:137–148PubMedCrossRefGoogle Scholar
  31. Klöser H, Ferreyra G, Schloss I, Mercuri G, Laturnus F, Curtosi A (1994) Hydrography of Potter Cove, a small fjord-like inlet on King George Island (South Shetland). Estuar Coast Shelf Sci 38:523–537CrossRefGoogle Scholar
  32. Leese F, Kop A, Wagele JW, Held C (2008) Cryptic speciation in a benthic isopod from Patagonian and Falkland Island waters and the impact of glaciations on its population structure. Front Zool 5:1–15CrossRefGoogle Scholar
  33. Linse K (2004) Scotia Arc deep-water bivalves: composition, distribution and relationship to the Antarctic shelf fauna. Deep Sea Res II 51:1827–1837CrossRefGoogle Scholar
  34. Linse K, Cope T, Lörz A-N, Sands CJ (2007) Is the Scotia Sea a center of Antarctic marine diversification? Some evidence of cryptic speciation in the circum-Antarctic bivalve Lissarca notorcadensis (Arcoidea: Philobryidae). Polar Biol 30:1059–1068CrossRefGoogle Scholar
  35. Martel A, Chia FS (1991) Drifting and dispersal of small bivalves and gastropods with direct development. J Exp Mar Biol Ecol 150:131–147CrossRefGoogle Scholar
  36. Mileikovsky SA (1971) Types of larval development in marine bottom invertebrates, their distribution and ecological significance: a re-evaluation. Mar Biol 10:193–213CrossRefGoogle Scholar
  37. Morton B (1978) Biology and functional-morphology of Philobrya munita (Bivalvia Philobryidae). J Zool 185:173–196CrossRefGoogle Scholar
  38. Nikula R, Fraser CI, Spencer HG, Waters JM (2010) Circumpolar dispersal by rafting in two subantarctic kelp-dwelling crustaceans. Mar Ecol Prog Ser 405:221–230CrossRefGoogle Scholar
  39. Passos FD, Domaneschi O (2009) The anatomical characters related to the brooding behavior of two Antarctic species of Mysella Angas, 1877 (Bivalvia, Galeommatoidea, Lasaeidae), with direct and indirect evidences of ovoviviparity. Polar Biol 32:271–280CrossRefGoogle Scholar
  40. Pearse JS, Lockhart SJ (2004) Reproduction in cold water: paradigm changes in the 20th century and a role for cidaroid sea urchins. Deep Sea Res II 51:1533–1549CrossRefGoogle Scholar
  41. Pearse JS, Mooi R, Lockhart SJ, Brandt A (2008) Brooding and species diversity in the Southern Ocean: selection for brooders or speciation within brooding clades? In: Krupnik I, Lang MA, Miller SE (eds) Smithsonian at the poles: contributions to international polar year science. Proceedings of the Smithsonian at the Poles Symposium, Smithsonian Institution Scholarly Press, Washington, DC, pp 181–196Google Scholar
  42. Poulin E, Palma AT, Feral JP (2002) Evolutionary versus ecological success in Antarctic benthic invertebrates. Trends Ecol Evol 17:218–222CrossRefGoogle Scholar
  43. Prezant RS, Showers M, Winstead RL, Cleveland C (1992) Reproductive ecology of the Antarctic bivalve Lissarca notorcadensis (Philobryidae). Am Malacol Bull 9:173–186Google Scholar
  44. Raupach MJ, Thatje S, Dambach J, Rehm P, Misof B, Leese F (2010) Genetic homogeneity and circum-Antarctic distribution of two benthic shrimp species of the Southern Ocean, Chorismus antarcticus and Nematocarcinus lanceopes. Mar Biol 157:1783–1797CrossRefGoogle Scholar
  45. Richardson MG (1979) The ecology and reproduction of the brooding Antarctic bivalve Lissarca miliaris. Brit Antarct Surv B 49:91–115Google Scholar
  46. Ripley BJ, Caswell H (2008) Contributions of growth, stasis, and reproduction to fitness in brooding and broadcast spawning marine bivalves. Popul Ecol 50:207–214CrossRefGoogle Scholar
  47. Ruiz-Verdugo CA, Ramirez JL, Allen SK, Ibarra AM (2000) Triploid catarina scallop (Argopecten ventricosus Sowerby II, 1842): growth, gametogenesis, and suppression of functional hermaphroditism. Aquaculture 186:13–32CrossRefGoogle Scholar
  48. Sartori AF, Domaneschi O (2005) The functional morphology of the Antarctic bivalve Thracia meridionalis Smith, 1885 (Anomalodesmata: Thraciidae). J Mollusc Stud 71:199–210CrossRefGoogle Scholar
  49. Schloss IR, Ferreyra GA, Ruiz-Pino D (2002) Phytoplankton biomass in Antarctic shelf zones: a conceptual model based on Potter Cove, King George Island. J Mar Syst 36:129–143CrossRefGoogle Scholar
  50. Sigurdsson JB, Titman CW, Davies PA (1976) The dispersal of young post-larval bivalve molluscs by byssus threads. Nature 262:386–387CrossRefGoogle Scholar
  51. Smith SDA (2002) Kelp rafts in the Southern Ocean. Glob Ecol Biogeogr 11:67–69CrossRefGoogle Scholar
  52. Strathmann RR (1974) Spread of sibling larvae of sedentary marine invertebrates. Am Nat 108:29–44CrossRefGoogle Scholar
  53. Strathmann RR (1978) The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32:894–906CrossRefGoogle Scholar
  54. Strathmann RR (1985) Feeding and nonfeeding larval development and life-history evolution in marine invertebrates. Ann Rev Ecol Syst 16:339–361CrossRefGoogle Scholar
  55. Strathmann RR, Strathmann MF (1982) The relationship between adult size and brooding in marine-invertebrates. Am Nat 119:91–101CrossRefGoogle Scholar
  56. Strathmann RR, Strathmann MF, Emson RH (1984) Does limited brood capacity link adult size, brooding, and simultaneous hermaphroditism? A test with the starfish Asterina phylactica. Am Nat 123:796–818CrossRefGoogle Scholar
  57. Tatian M, Sahade R, Kowalke J, Kivatinitz SC, Esnal GB (2002) Food availability and gut contents in the ascidian Cnemidocarpa verrucosa at Potter Cove, Antarctica. Polar Biol 25:58–64CrossRefGoogle Scholar
  58. Tevesz MJS (1977) Taxonomy and ecology of the Philobryidae and Limopsidae (Molusca: Pelecypoda). Postilla 171:1–64Google Scholar
  59. Thatje S (2012) Effects of capability for dispersal on the evolution of diversity in Antarctic benthos. Integr Comp Biol. doi:10.1093/icb/ics/ics105
  60. Thatje S, Schnack-Schiel S, Arntz WE (2003) Developmental trade-offs in subantarctic meroplankton communities and the enigma of low decapod diversity in high southern latitudes. Mar Ecol Prog Ser 260:195–207CrossRefGoogle Scholar
  61. Thatje S, Hillenbrand CD, Larter R (2005) On the origin of Antarctic marine benthic community structure. Trends Ecol Evol 20:534–540PubMedCrossRefGoogle Scholar
  62. Thatje S, Hillenbrand CD, Mackensen A, Larter R (2008) Life hung by a thread: endurance of Antarctic fauna in glacial periods. Ecology 89:682–692PubMedCrossRefGoogle Scholar
  63. Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev 25:1–45CrossRefGoogle Scholar
  64. Vance RR (1973) Reproductive strategies in marine benthic invertebrates. Am Nat 107:339–352CrossRefGoogle Scholar
  65. Wright WG (1988) Sex change in the mollusca. Trends Ecol Evol 3:137–140PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.Ocean and Earth Science, National Oceanography Centre, SouthamptonUniversity of SouthamptonSouthamptonUK
  2. 2.British Antarctic SurveyNatural Environment Research CouncilCambridgeUK

Personalised recommendations