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Marine Biology

, Volume 148, Issue 1, pp 59–71 | Cite as

Reproductive biology and biochemical composition of the brooding echinoid Amphipneustes lorioli on the Antarctic continental shelf

  • Elizabeth A. Galley
  • Paul A. Tyler
  • Andrew Clarke
  • Craig R. Smith
Research Article

Abstract

The bathyal West Antarctic Peninsula (WAP) shelf experiences intense seasonal variability in primary production, with summer phytoplankton blooms yielding intense pulse of phytodetritus to shelf sediments. Echinoderms form a conspicuous proportion of the deposit-feeding megabenthos on the shelf and of these Amphipneustes lorioli was the most abundant irregular echinoid. To explore the reproductive response of A. lorioli to this seasonal production cycle, A. Lorioli was sampled at one location on the WAP shelf during four separate cruises between March 2000 and March 2001. Reproductive patterns were determined by histological analyses of gonad tissue, and elemental (CHN) analyses were used to estimate the nutritional and energetic status of the body tissues. Histological analysis of the brooding echinoid A. lorioli suggested a quasi-continuous gametogenic pattern in both the ovaries and the testes. Biochemical analysis of the gonads and the gut tissues were consistent with a continuous gametogenic cycle, showing no significant changes in the biochemical composition of the tissues among seasons. Size-frequency distributions of the embryo and juvenile echinoids within the adults’ brood pouches revealed a synchronous recruitment of embryos and juveniles in specific cohorts between different adult specimens. Whilst this occurrence of different cohorts of the developing brood may be an adaptation to limited brood space, there may also be an external factor influencing the synchrony between adult individuals. Nonetheless, a continuous gametogenic cycle and the lack of seasonal variation in the biochemical composition of gonad and gut tissues suggest that this deposit-feeding irregular urchin is exploiting a persistent sediment food bank in WAP shelf sediments throughout much of the year.

Keywords

Food Bank Brooding Pouch Gonad Index Vitellogenic Oocyte Test Diameter 
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.

Notes

Acknowledgements

This work was carried out with funding from an NERC studentship, and from the NSF funded FOODBANCS programme 1999–2003 (NSF grant no. OPP-9816049 to C.R.S and D.J. DeMaster). Thanks also to the British Antarctic Survey for their funding and use of facilities during the biochemical analysis. Thanks to the crew and scientists on the RV L.M. Gould and the RV N.B. Palmer for their assistance during sample collection. This is contribution 6609 from SOEST, University of Hawaii at Manoa.

References

  1. Arntz WE, Brey T, Gallardo VA (1994) Antarctic zoobenthos. Oceanogr Mar Biol 32:241–304Google Scholar
  2. Barker MF (1984) Reproduction and development in Goniocidaris umbraculum, a brooding echinoid. In: Keegan BF, O’Connor R (eds) Echinodermata: proceedings of the fifth international echinoderm conference galway. Balkema, Rotterdam, pp 207–214Google Scholar
  3. Bosch I, Pearse JS (1990) Developmental types of shallow-water asteroids of McMurdo Sound, Antarctica. Mar Biol 104:41–46CrossRefGoogle Scholar
  4. Brockington S, Clarke A, Chapman ALG (2001) Seasonality of feeding and nutritional status during the austral winter in the Antarctic sea urchin Sterechinus neumayeri. Mar Biol 139:127–138CrossRefGoogle Scholar
  5. Clarke A (1983) Life in cold water: the physiological ecology of polar marine ectotherms. Oceanogr Mar Biol 21:341–453Google Scholar
  6. Clarke A (1985) Energy flow in the Southern Ocean food web. In: Siegfried W, Condy P, Laws R (eds) Antarctic nutrient cycles and food webs. Springer, Berlin Heidelberg New York, pp 573–580CrossRefGoogle Scholar
  7. Clarke A (1988) Seasonality in the Antarctic marine environment. Comp Biochem Phys B 90B:461–473CrossRefGoogle Scholar
  8. Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905CrossRefGoogle Scholar
  9. Clarke A, Peck LS (1991) The physiology of polar marine zooplankton. Polar Res 10:355–369CrossRefGoogle Scholar
  10. Culling CFA (1974) Handbook of histopathological and biochemical techniques. Butterworth and Co. Ltd, LondonGoogle Scholar
  11. Eckelbarger KJ, Watling L (1995) Role of phylogenetic constraints in determining reproductive patterns in deep-sea invertebrates. Invertebr Biol 114:256–269CrossRefGoogle Scholar
  12. Emlet RB, McEdward L, Strathmann RR (1987) Echinoderm larval ecology viewed from the egg. In: Jangoux M, Lawrence JM (eds) Echinoderm studies vol 2. Balkema, Rotterdam, pp 55–136Google Scholar
  13. Gnaiger E, Bitterlitch G (1984) Proximate biochemical composition and caloric content calculated from elemental CHN analysis: a stoichiometric concept. Oecologia 62:289–298CrossRefGoogle Scholar
  14. Grant A, Tyler PA (1983) The analysis of data in studies of invertebrate reproduction 2 the analysis of oocyte size-frequency data, and comparison of different types of data. Int J Inver Rep 6:271–283CrossRefGoogle Scholar
  15. Grebmeier JM, McRoy CP, Feder HM (1988) Pelagic-benthic coupling on the shelf of the northern Bering and Chukchi Seas. I. Food supply source and benthic biomass. Mar Ecol Prog Ser 48:57–67CrossRefGoogle Scholar
  16. Karl DM, Christian J, Letelier RM (1996) Microbiological oceanography in the region west of the Antarctic Peninsula: microbial dynamics, nitrogen cycle and carbon flux. In: Ross R, Hoffman E, Quetin L (eds) Foundations for ecosystem research west of the Antarctic Peninsula. Antarct Res Ser 70:303–332Google Scholar
  17. Knox G (1994). The biology of the Southern Ocean. Cambridge University Press, New YorkGoogle Scholar
  18. Lockhart SJ, O’Loughlin PM, Tutera P (1994) Brood-protection and diversity in echinoids from Prydz Bay, Antarctica. In: David B, Guille A, Féral JP, Roux M (eds) Echinoderms through time: proceedings of the eighth international echinoderm conference. Balkema, Rotterdam, pp 749–756Google Scholar
  19. Magniez P (1980) Modalites de l’incubation chez Abatus cordatus (Verrill), oursin endemique des iles Kerguelen. In: Jangoux M (ed) Echinoderms: present and past. A. A. Balkema, RotterdamGoogle Scholar
  20. Magniez P (1983) Reproductive cycle of the brooding echinoid Abatus cordatus (Echinodermata) in Kerguelen (Antarctic Ocean): changes in the organ indices, biochemical composition and caloric content of the gonads. Mar Biol 74:55–64CrossRefGoogle Scholar
  21. McClintock JB, Pearse JS (1988) Reproductive biology of the Antarctic brooding sea urchins Abatus shackletoni and Abatus nimrodi. Am Zool 28:151AGoogle Scholar
  22. Mincks SL, Smith CR, DeMaster DJ (2005) Persistence of labile organic matter and microbial biomass in Antarctic shelf sediments: evidence of a sediment “food bank.” Mar Ecol Prog Ser (in press)Google Scholar
  23. Mortensen TH (1951) A monograph of the echinoidea. V:2 Spatangoida II. Reitzel, CopenhagenGoogle Scholar
  24. Pearse JS (1965) Reproductive periodicities in several contrasting populations of Odontaster validus Koehler, a common Antarctic asteroid. Antarct Res Ser 5:39–85Google Scholar
  25. Pearse JS, McClintock JB (1990) A comparison of reproduction by the brooding spatangoid echinoids Abatus shackletoni and A. nimrodi in McMurdo Sound, Antarctica. Invertebr Reprod Dev 17:181–191CrossRefGoogle Scholar
  26. Pearse JS, Bosch I, McClintock JB (1985) Contrasting modes of reproduction by common shallow-water Antarctic invertebrates. Antarct J US 30:138–139Google Scholar
  27. Pearse JS, Bosch I, McClintock JB, Marinovic B, Britton R (1986) Contrasting tempos of reproduction by shallow water animals in McMurdo Sound, Antarctica. Antarct J US 21:82–84Google Scholar
  28. Pearse JS, McClintock JB, Bosch I (1991) Reproduction of Antarctic benthic marine invertebrates: tempos, modes, and timing. Am Zool 31:65–80CrossRefGoogle Scholar
  29. Schatt P (1988) Embryonic growth of the brooding sea urchin Abatus cordatus. In: Burke RD, Mladenov PV, Lambert P, Parsley RL (eds) Echinoderm biology: proceedings of the sixth international echinoderm conference, Victoria. RotterdamGoogle Scholar
  30. Schatt P, Féral JP (1991) The brooding cycle of Abatus cordatus (Echinodermata: Spatangoida) at Kerguelen Islands. Polar Biol 11:283–292CrossRefGoogle Scholar
  31. Schatt P, Féral JP (1996) Completely direct development of Abatus cordatus, a brooding Schizasterid (Echinodermata: Echinoidea) from Kerguelen, with description of perigastrulation, a hypothetical new mode of gastrulation. Biol Bull 190:24–44CrossRefGoogle Scholar
  32. Smith RC, Baker KS, Fraser WR, Hofmann EE, Karl DM, Klinck JM, Quetin LB, Prezelin BB, Ross RM, Trivelpiece WZ, Vernet M (1995) The Palmer LTER: a long term ecological research program at Palmer station, Antarctica. Oceanography 8:77–86CrossRefGoogle Scholar
  33. Tyler PA (1986) Studies of a benthic time series: reproductive biology of benthic invertebrates in the Rockall Trough. P Roy Soc Edin B 88:175–190Google Scholar
  34. Tyler PA, Billet DSM (1987) The reproductive ecology of Elasipodid holothurians from the northeast Atlantic. Biol Oceanography 5:273–296Google Scholar
  35. Tyler PA, Reeves S, Peck L, Clarke A, Powell D (2003) Seasonal variation in the gametogenic ecology of the Antarctic scallop Adamussium colbecki. Polar Biol 26:727–733CrossRefGoogle Scholar
  36. Wardlaw AC (2002) Practical statistics for experimental biologists, 2nd edn. Wiley, ChichesterGoogle Scholar
  37. Young C (2003) Reproduction, development and life history traits. In: Tyler PA (eds) Ecosystems of the World, vol 28 ecosystems of the deep sea. Elsevier, Amsterdam, pp 381–426Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Elizabeth A. Galley
    • 1
  • Paul A. Tyler
    • 1
  • Andrew Clarke
    • 2
  • Craig R. Smith
    • 3
  1. 1.Southampton Oceanography CentreSouthamptonUK
  2. 2.British Antarctic SurveyNERCCambridgeUK
  3. 3.Department of OceanographyUniversity of Hawaii at ManoaHonoluluUSA

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