Advertisement

Marine Biology

, Volume 125, Issue 3, pp 551–567 | Cite as

Viviparity and intragonadal cannibalism in the diminutive sea stars Patiriella vivipara and P. parvivipara (family Asterinidae)

  • M. Byrne
Article

Abstract

The Australian asterinid sea stars Patiriella vivipara and P. parvivipara have the most derived lifehistory pattern seen in the Asteroidea. They are simultaneous hermaphrodites, have intragonadal fertilisation, and incubate their young in the gonads to an advanced juvenile stage. As characteristic of brooding echinoderms, P. vivipara and P. parvivipara are diminutive, with P. parvivipara being the smallest known sea star. These species have the most restricted distribution known in the Asteroidea. Reproduction of two populations P. vivipara in Tasmania, Midway Point and Tesselated Pavement, was examined in specimens collected in 1991, 1992 and 1995. Reproduction of P. parvivipara in South Australia was examined in specimens collected from one population in 1991 and 1994. The gonads are ovotestes. Both species typically contain 6 to 8 predominantly female gonads and 1 predominantly male gonad. In the predominantly female gonads, only a few eggs and a small amount of sperm are produced at a time. Detection of sperm in these gonads requires histological examination. The amount of sperm in the predominantly female gonads appears sufficient to fertilise all the ova produced. The low allocation to male function and the simultaneous presence of mature eggs and sperm suggests that both species may be self-fertile. The amount of sperm in the predominantly male gonads however, would not be expected in exclusively self-fertilisers, suggesting that some outcrossing occurs. The significantly higher reproductive output of P. vivipara at Midway Point than at the Tesselated Pavement indicates that the Midway Point population is particularly important for the conservation of this species. P. vivipara and P. parvivipara have small, 140 to 150 μm-diam eggs. Embryogenesis is asynchronous, with progeny at different stages of development in the gonads. The end-point of brooding is variable in P. vivipara, with juveniles emerging from the parent at sizes ranging between 1.5 and 5.0 mm diam. Juvenile P. parvivipara are born at a diameter of up to 2.5 mm. At birth the juveniles of both species are up to 25–30% of the parent's diameter. Birth involves distension of the gonopore, with a marked separation of the ossicles and softening of the connective tissue around the pore. The juveniles are considerably larger than the ova and depend on extraembryonic nutrition to support their growth. Once the mouth opens, the juveniles prey on their intragonadal siblings. Cannibalism accounts for the substantial post-metamorphic growth. Viviparity lies at the extreme end of the broadcasting-brooding continuum of life histories in Patiriella, and the life-history traits of P. vivipara and P. par-vivipara are compared with those of other Patiriella spp. to assess the changes associated with evolution of viviparity.

Keywords

Reproductive Output Simultaneous Presence Juvenile Stage Restricted Distribution Male Function 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Byrne M (1985) The mechanical properties of the autotomy tissues of Eupentacta quinquesemita (Echinodermata: Holothuroidea) and the effects of certain physico-chemical agents. J exp Biol 117: 69–86Google Scholar
  2. Byrne M (1991a) Developmental diversity in the starfish genus Patiriella. In: Yanagisawa T, Yasumasu I, Oguro C, Suzuki N, Motokawa T (eds) Biology of Echinodermata. Balkema, Rotterdam, pp 499–508Google Scholar
  3. Byrne M (1991b) Reproduction, development and population biology of the Caribbean ophiuroid Ophionereis olivacea, a protandric hermaphrodite that broods its young. Mar Biol 111: 387–399Google Scholar
  4. Byrne M (1992) Reproduction of sympatric populations of Patiriella gunnii P. calcar and, P. exigua in New South Wales, asterinid sea stars with direct development. Mar Biol 114: 297–316Google Scholar
  5. Byrne M (1995) Changes in larval morphology in the evolution of benthic development by Patiriella exigua (Asteroidea: Asterinidae), a comparison with the larvae of Patiriella species with planktonic development. Biol Bull mar biol Lab, Woods Hole 188: 293–305Google Scholar
  6. Byrne M, Anderson MJ (1994) Hybridization of sympatric Patiriella species (Echinodermata: Asteroidea) in New South Wales. Evolution 48: 564–576Google Scholar
  7. Byrne M, Barker MF (1991) Embryogenesis and larval development of the asteroid Patiriella regularis viewed by light and scanning electron microscopy. Biol Bull mar biol Lab, Woods Hole 180: 332–345Google Scholar
  8. Byrne M, Cerra A (1996) Evolution of intragonadal development in the diminutive asterinid sea stars Patiriella vivipara and P. par-vivipara with an overview of development in the Asterinidae. Biol Bull 191, Mar Biol Lab, Woods Hole (in press)Google Scholar
  9. Cerra A, Byrne M (1995a) Cellular events of wrinkled blastula formation and the influence of the fertilisation envelope on wrinkling in the sea star Patiriella exigua. Acta zool, Stock 76: 155–165Google Scholar
  10. Cerra A, Byrne M (1995b) The structure of the extraembryonic matrices around the embryos and larvae of Patiriella exigua (Asteroidea) and their role in benthic development, a comparison with the planktonic larvae of P. regularis. J Morph 225: 1–13Google Scholar
  11. Charnov EL (1982) The theory of sex allocation. Monogr Popul Biol 18: 1–355Google Scholar
  12. Chen B-Y, Chen C-P (1992) Reproductive cycle, larval development, juvenile growth and population dynamics of Patiriella pseudoexigua (Echinodermata: Asteroidea) in Taiwan. Mar Biol 113: 271–280Google Scholar
  13. Chia FS (1974) Classification and adaptive significance of developmental patterns in marine invertebrates. Thalassia jugosl 10: 121–130Google Scholar
  14. Chia FS, Walker CW (1991) Echinodermata: Asteroidea. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates. Vol VI. Echinoderms and lophophorates. Boxwood Press, Pacific Grove, California, pp 301–353Google Scholar
  15. Dartnall AJ (1969) A viviparous species of Patiriella (Asteroidea, Asterinidae) from Tasmania. Proc Linn Soc NSW 93: 294–296Google Scholar
  16. Dartnall AJ (1971) Australian sea stars of the genus Patiriella (Asteroidea, Asterinidae). Proc Linn Soc NSW 96: 39–51Google Scholar
  17. Eernisse DJ (1988) Reproductive patterns in six species of Lepidochitona (Mollusca: Polyplacophora) from the Pacific Coast of North America. Biol Bull mar biol Lab, Woods Hole 174: 287–302Google Scholar
  18. Emlet RB, McEdward LR, Strathmann RR (1987) Echinoderm larval ecology viewed from the egg. In: Jangoux M, Lawrence JM (eds) Echinoderm studies. Vol 2. Balkema, Rotterdam, pp 55–134Google Scholar
  19. Fell HB (1946) The embryology of the viviparous ophiuroid Amphipholis squamata Delle Chiaje. Trans R Soc NZ 75: 419–464Google Scholar
  20. Heath DJ (1977) Simultaeous hermaphroditism; cost and benefit. J theor Biol 64: 363–373Google Scholar
  21. Hess HC (1993) The evolution of parental care in brooding spirorbid polychaetes: the effects of scaling constraints. Am Nat 141: 577–596Google Scholar
  22. Hoggins DD (1976) Comparative ecological studies of two intertidal sea stars Patiriella vivipara, Dartnall, 1969 and P. regularis Verrill, 1913, B.Sc (Honours) thesis. University of Tasmania, HobartGoogle Scholar
  23. Hunt A (1993) Effects of contrasting patterns of larval dispersal on the genetic connectedness of local populations of two intertidal starfish, Patiriella calcar and P. exigua. Mar Ecol Prog Ser 92: 179–186Google Scholar
  24. Keough MJ, Dartnall AJ (1978) A new species of viviparous asterinid asteroid from Eyre Peninsula, South Australia. Rec S Aust Mus 28: 407–416Google Scholar
  25. Knowlton N, Jackson JBC (1993) Inbreeding and outbreeding in marine invertebrates. In: Thornhill NW (ed) The natural history of inbreeding and outbreeding. University of Chicago Press, Chicago, pp 200–249Google Scholar
  26. Komatsu M, Kano YT, Oguro C (1990) Development of a true ovoviviparous sea star, Asterina pseudoexigua exigua Hayashi. Biol Bull mar biol Lab, Woods Hole 179: 254–263Google Scholar
  27. Lawson-Kerr C, Anderson DT (1978) Reproduction, spawning and development of the starfish Patiriella exigua (Lamarck) (Asteroidea, Asterinidae) and some comparisons with P. calcar (Lamarck). Aust J mar Freshwat Res 29: 45–53Google Scholar
  28. McArdle BH (1988) The structural relationship: regression in biology. Can J Zool 66: 2329–2339Google Scholar
  29. McGrath D, Ó Foighil D (1986) Population dynamics and reproduction in the hermaphroditic Lasaea rubra (Montague) (Bivalvia, Galeommatacea). Ophelia 25: 209–219Google Scholar
  30. Sewell MA (1994a) Small size, brooding, and protandry in the apodid sea cucumber Leptosynapta clarki. Biol Bull mar biol Lab, Woods Hole 187: 112–123Google Scholar
  31. Sewell MA (1994b) Birth, recruitment and juvenile growth in the intraovarian brooding sea cucumber Leptosynapta clarki. Mar Ecol Prog Ser 114: 149–156Google Scholar
  32. Sewell MA, Chia F-S (1994) Reproduction of the intraovarian brooding apodid Leptosynapta clarki (Echinodermata. Holothuroidea) in British Columbia. Mar Biol 121: 285–300Google Scholar
  33. Sokal RR, Rohlf FJ. (1981) Biometry. The principles and practice of statistics in biological research. 2nd edn. W. H. Freeman & Co, New YorkGoogle Scholar
  34. Strathmann RR (1978) The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32: 894–906Google Scholar
  35. Strathmann RR, Strathmann MF (1982) The relationship between adult size and brooding in marine invertebrates. Am Nat 119: 91–101Google Scholar
  36. 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: 796–818Google Scholar
  37. Turner, R. L., Dearborn, J. H. (1979) Organic and inorganic composition of post-metamorphic growth stages of Ophionotus hexactis (E.A. Smith) (Echinodermata: Ophiuroidea) during intraovarian incubation. J exp mar Biol Ecol 36: 41–51Google Scholar
  38. Walker CW, Lesser MP (1989) Nutrition and development of brooded embryos in the brittlestar Amphipholis squamata: do endosymbiotic bacteria play a role? Mar Biol 103: 519–530Google Scholar
  39. Wilkie IC (1984) Variable tensility in echinoderm connective tissues: a review. Mar behav Physiol 11: 1–34Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • M. Byrne
    • 1
  1. 1.Department of Anatomy and Histology, F13University of SydneySydneyAustralia

Personalised recommendations