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Marine Biology

, Volume 159, Issue 2, pp 455–465 | Cite as

A new quantitative analysis of ovarian development in echinoderms: the maturity stage index

  • Gina M. Doyle
  • Jean-François Hamel
  • Annie MercierEmail author
Original Paper

Abstract

This study developed an objective quantitative method for detecting small-scale temporal or spatial differences in gametogenesis in echinoderms. The method was applied to conventional monthly samples of the planktotrophic brittle star, Ophiopholis aculeata, collected at a single site in Newfoundland (eastern Canada) at 10–15 m depth. The samples were analysed to determine gonad index, oocyte size and gonadal stage using histology. The maturity stage index (MSI) was developed to integrate a measure of brittle star size (disc diameter), oocyte size and oocyte density. The MSIs ranged from 0 to 800 and had significantly different means among the four gametogenic stages (early growth, growth, mature and spent). The MSI was more sensitive in revealing significant differences between consecutive stages than any of its individual constituents. The MSI was also applied to gametogenic data from the lecithotrophic holothuroid, Mesothuria lactea, again revealing significant differences between successive oogenic stages. This method is expected to be useful in field and experimental studies of gametogenesis in echinoderms (and possibly other taxa), where it is important to detect not just the timing of annual peaks in reproduction but small differences in reproductive status among individuals or populations (e.g. from different habitats or feeding regimes).

Keywords

Gonad Index Oocyte Diameter Germinal Epithelium Oocyte Size Large Oocyte 
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

Acknowledgments

Special thanks to P. Gagnon for logistic support, guidance and valued help in the field, and to S. Caines, W. Coffey, R. Guest, R. Hooper, K. Matheson, R. O’Donnell, P. Sargent, and C. Vickers for assistance with field work and sample collection. Many thanks as well to OSC Laboratory Services, the MI Centre for Aquaculture and Development, J. Foote, N. Laite, C. Short, J. So and Z. Sun for technical and moral support and to S. Baillon for her work on M. lactea. This study was financially supported by grants from the Natural Sciences and Engineering Research Council of Canada (NSERC) and the Canada Foundation for Innovation (CFI) to A. Mercier. It was conducted in partial fulfilment of the MSc degree of G. Doyle, who wishes to thank examiners for helping to improve earlier versions of this manuscript. We also thank two anonymous reviewers for constructive comments.

Supplementary material

227_2011_1823_MOESM1_ESM.pdf (137 kb)
Supplementary material 1 (PDF 136 kb)

References

  1. Baillon S, Hamel J-F, Mercier A (2011) Comparative study of reproductive synchrony at various scales in deep-sea echinoderms. Deep-Sea Res Part I 58:260–272CrossRefGoogle Scholar
  2. Bayne BL, Holland DL, Moore MN, Lowe DM, Widdows J (1978) Further studies on the effects of stress in the adult on the eggs of Mytilus edulis. J Mar Biol Assoc UK 58:825–842CrossRefGoogle Scholar
  3. Blake SEJ (1978) The reproductive cycle of Ophiopholis aculeata (Echinodermata: Ophiuroidea) in the Northwestern Atlantic. Ph.D. dissertation, University of Maine, OronoGoogle Scholar
  4. Boolootian RA (1966) Reproductive physiology. In: Boolootian RA (ed) Physiology of Echinodermata. Interscience, New York, pp 561–613Google Scholar
  5. Bowmer T (1982) Reproduction in Amphiura filiformis (Echinodermata: Ophiuroidea): seasonality in gonad development. Mar Biol 69:281–290CrossRefGoogle Scholar
  6. Buchanan S (2001) Measuring reproductive condition in the Greenshell™ mussel Perna canaliculus. NZ J Mar Freshw Res 35:859–870CrossRefGoogle Scholar
  7. Devlaming V, Grossman G, Chapman F (1982) On the use of the gonosomatic index. Comp Biochem Phys A 73:31–39CrossRefGoogle Scholar
  8. Doyle G (2011) Effect of spatial and environmental factors on the reproductive cycle of the brittle star, Ophiopholis aculeata, based on a new maturity stage index. M.Sc. dissertation, Memorial University, St. John’sGoogle Scholar
  9. Ebert TA, Hernandez JC, Russell MP (2011) Problems of the gonad index and what can be done: analysis of the purple sea urchin Strongylocentrotus purpuratus. Mar Biol 158:47–58CrossRefGoogle Scholar
  10. Enríquez-Díaz M, Pouvreau S, Chávez-Villalba J, Le Pennec M (2009) Gametogenesis, reproductive investment, and spawning behavior of the Pacific giant oyster Crassostrea gigas: evidence of an environment-dependent strategy. Aquac Int 17:491–506CrossRefGoogle Scholar
  11. Falk-Petersen IB (1982) Breeding season and egg morphology of echinoderms in Balsfjorden, Northern Norway. Sarsia 67:215–221 Google Scholar
  12. Falkner I, Byrne M (2003) Reproduction of Ophiactis resiliens (Echinodermata: Ophiuroidea) in New South Wales with observations on recruitment. Mar Biol 143:459–466CrossRefGoogle Scholar
  13. Fenaux L (1970) Maturation of the gonads and seasonal cycle of the planktonic larvae of the ophiuroid Amphiura chiajei Forbes. Biol Bull 138:262–271CrossRefGoogle Scholar
  14. Fuji A (1960) Studies on the biology of the sea urchin. I. Superficial and histological gonadal changes in gametogenic process of two sea urchins, Strongylocentrotus nudus and Strongylocentrotus intermedius. Bull Fac Fish Hokkaido Univ 11:1–14Google Scholar
  15. Giese AC, Pearse JS (1974) Introduction: general principles. In: Giese AC, Pearse JS (eds) Reproduction of marine invertebrates. Academic Press, New York, pp 1–49Google Scholar
  16. Gómez-Robles E, Rodríguez-Jaramillo C, Saucedo PE (2005) Digital image analysis of lipid and protein histochemical markers for measuring oocyte development and quality in pearl oyster Pinctada mazatlantica (Hanley, 1856). J Shellfish Res 24:1197–1202Google Scholar
  17. Gosner KL (1978) Atlantic Seashore. Houghton Mifflin, BostonGoogle Scholar
  18. Grant A (1986) The biometry of asteroid oogenesis: some observations. Int J Invert Rep Dev 10:113–116Google Scholar
  19. Grant A, Tyler PA (1986) An analysis of the reproductive pattern in the sea star Astropecten irregularis (Pennant) from the Bristol Channel. Int J Invert Rep Dev 9:345–361Google Scholar
  20. Hamel J-F, Mercier A (1996) Evidence of chemical communication during the gametogenesis of holothuroids. Ecology 77:1600–1616CrossRefGoogle Scholar
  21. Hendler G (1991) Chapter 6: Echinodermata: Ophiuroidea. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates. The Boxwood Press, Pacific Grove, pp 355–511Google Scholar
  22. Himmelman JH, Dumont CP, Gaymer CF, Vallières C, Drolet D (2008) Spawning synchrony and aggregative behaviour of cold-water echinoderms during multi-species mass spawnings. Mar Ecol Prog Ser 361:161–168Google Scholar
  23. Hughes AD, Kelly MS, Barnes DKA, Catarino AI, Black KD (2006) The dual functions of sea urchin gonads are reflected in the temporal variations of their biochemistry. Mar Biol 148:789–798CrossRefGoogle Scholar
  24. Junqueira LC, Carneiro J, Long JA (1986) Basic histology. Appleton-Century-Crofts, NorwalkGoogle Scholar
  25. Lowe DM, Moore MN, Bayne BL (1982) Aspects of gametogenesis in the marine mussel Mytilus edulis (L.). J Mar Biol Assoc UK 62:133–145CrossRefGoogle Scholar
  26. MacDonald BA, Thompson RJ (1986) Influence of temperature and food availability on the ecological energetics of the giant scallop Placopecten magellanicus. Mar Biol 93:37–48CrossRefGoogle Scholar
  27. Mercier A, Hamel JF (2009) Endogenous and exogenous control of gametogenesis and spawning in echinoderms. Adv Mar Biol 55:1–302CrossRefGoogle Scholar
  28. Newell RIE, Hilbish TJ, Koehn RK, Newell CJ (1982) Temporal variation in the reproductive cycle of Mytilus edulis (Bivalvia, Mytilidae) from localities on the east coast of the United States. Biol Bull 162:299–310CrossRefGoogle Scholar
  29. Osada M, Nakamura S, Kijima A (2007) Quantitative analysis of pattern of gonial proliferation during sexual maturation in Japanese scallop Patinopecten yessoensis. Fish Sci 73:1318–1324Google Scholar
  30. Patent DH (1969) The reproductive cycle of Gorgonocephalus caryi (Echinodermata: Ophiuroidea). Biol Bull 136:241–252CrossRefGoogle Scholar
  31. Schoenmakers HJN, Goedhart MJ, Voogt PA (1984) Biometrical and histological aspects of the reproductive cycle of the ovaries of Asterias rubens (Echinodermata). Biol Bull 166:328–348CrossRefGoogle Scholar
  32. Singh R, MacDonald BA, Lawton P, Thomas MLH (2001) The reproductive biology of the dendrochirote sea cucumber Cucumaria frondosa (Echinodermata: Holothuroidea) using new quantitative methods. Invertebr Reprod Dev 40:125–141CrossRefGoogle Scholar
  33. Toro JE, Thompson RJ, Innes DJ (2002) Reproductive isolation and reproductive output in two sympatric mussel species (Mytilus edulis, M. trossulus) and their hybrids from Newfoundland. Mar Biol 141:897–909CrossRefGoogle Scholar
  34. Tyler PA (1977) Seasonal variation and ecology of gametogenesis in the genus Ophiura (Ophiuroidea: Echinodermata) from the Bristol Channel. J Exp Mar Biol Ecol 30:185–197CrossRefGoogle Scholar
  35. Urrutia MB, Ibarrola I, Iglesias JIP, Navarro E (1999) Energetics of growth and reproduction in a high-tidal population of the clam Ruditapes decussatus from Urdaibai Estuary (Basque Country, N. Spain). J Sea Res 42:35–48CrossRefGoogle Scholar
  36. Yoshida M (1952) Some observations on the maturation of the sea-urchin, Diadema setosum. Annot Zool Jpn 25:265–271Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Gina M. Doyle
    • 1
  • Jean-François Hamel
    • 2
  • Annie Mercier
    • 1
    Email author
  1. 1.Ocean Sciences Centre (OSC)Memorial UniversitySt. John’sCanada
  2. 2.Society for the Exploration and Valuing of the Environment (SEVE)St. PhilipsCanada

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