Advertisement

Marine Biology

, Volume 158, Issue 11, pp 2589–2602 | Cite as

Brooding and development of Anasterias minuta (Asteroidea: Forcipulata) in Patagonia, Argentina

  • Damián G. Gil
  • Graciela Escudero
  • Héctor E. Zaixso
Original Paper

Abstract

Brooding, embryonic and larval development, and the influence of environmental and biological factors in tidepool habitats were studied in the sea star, Anasterias minuta, at various sites along ~220 km of the Patagonian coast. This species has a benthic, lecithotrophic development that includes eight distinct developmental stages. A larval organ, the connection cord, is developed from a small preoral lobe at early stages of development and becomes larger and thinner at advanced stages. Fecundity and average egg size increased with female body size. The regression of log egg number to log sea-star size and weight at different sites had a slope significantly less than 3.0, resulting in negative allometry and indicating that brood capacity was limited in large females. Development was generally synchronous among sites, but varied within each brood at advanced stages, with more developed brooded larvae located at the periphery of the brood mass. Brooding was synchronous among various populations at different years and spatial scales, and extended over a period of 8 months. The highest proportion of brooding females occurred during May and June (austral winter). Juveniles were released mainly during September. The likelihood of finding brooding sea stars decreased with increasing sea water temperature, tidal height, and wave exposure, and increased with increasing body size. Both body size of brooding females and brooding rate were higher in the infralittoral fringe than at midlittoral levels. A revision of the current model of brooding behavior and development among forcipulate sea stars is given.

Keywords

Tidal Height Wave Exposure Shore Zone Brooding Female Brood Mass 
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

The authors would like to thank Silvina Rosales and Maria Belén Reartes for their support during field surveys and Bárbara Kotoucek (UNPSJB) for assistance with German translation. This manuscript was further improved by comments of Howard Feder and two anonymous reviewers.

Supplementary material

227_2011_1760_MOESM1_ESM.pdf (396 kb)
Supplementary material 1 (PDF 395 kb)

References

  1. Agresti A (2007) An introduction to categorical data analysis, 2nd edn. Wiley, New YorkGoogle Scholar
  2. Aiken LS, West SG (1991) Multiple regression: testing and interpreting interactions. Newbury Park, SageGoogle Scholar
  3. Arnaud PM (1974) Contribution à la bionomie marine benthique des regions antarctiques et subantarctiques. Tethys 6:465–556Google Scholar
  4. Baker P, Mann R (1997) The postlarval phase of bivalve mollusks: a review of functional ecology and new records of postlarval drifting of Chesapeake Bay bivalves. Bull Mar Sci 61:409–430Google Scholar
  5. Bernasconi I (1964) Distribución geográfica de los Equinoideos y Asteroideos de la extremidad austral de Sudamérica. Boletín del Instituto de Biología Marina (Mar del Plata) 7:43–50Google Scholar
  6. Bertness MD, Gaines SD, Stephens EG, Yund PO (1992) Components of recruitment in populations of the acorn barnacle Semibalanus balanoides (Linnaeus). J Exp Mar Biol Ecol 156:199–215Google Scholar
  7. Bertness MD, Crain CM, Silliman BR, Bazterrica MC, Reyna V, Hildago F, Farina JK (2006) The community structure of western Atlantic Patagonian rocky shores. Ecol Monogr 76:439–460Google Scholar
  8. Bingham BL, Giles K, Jaeckle W (2004) Variability of broods of the seastar Leptasterias aequalis. Can J Zool 82:457–463. doi: 10.1139/Z04-009 Google Scholar
  9. Blankley WO, Branch GM (1984) Co-operative prey capture and unusual brooding habits of Anasterias rupicola (Verrill) (Asteroidea) at sub-Antarctic Marion Island. Mar Ecol Prog Ser 20:171–176Google Scholar
  10. Boivin YY, Larrivée D, Himmelman JH (1986) Reproductive cycle of the subarctic brooding asteroid Leptasterias polaris. Mar Biol 92:329–337. doi: 10.1007/BF00392673 Google Scholar
  11. Bosch I, Pearse JS (1990) Developmental types of shallow-water asteroids of McMurdo Sound, Antarctica. Mar Biol 104:41–46. doi: 10.1007/BF01313155 Google Scholar
  12. Bosch I, Slattery M (1999) Costs of extended brood protection in the Antarctic sea star, Neosmilaster georgianus (Echinodermata: Asteroidea). Mar Biol 134:449–459. doi: 10.1007/s002270050561 Google Scholar
  13. Byrne M (1992) Reproduction of sympatric populations of Patiriella gunnii, P. calcar and P. exigua in New South Wales, asterinid seastars with direct development. Mar Biol 114:297–316. doi: 10.1007/BF00349533 Google Scholar
  14. 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 188:293–305PubMedGoogle Scholar
  15. Byrne M (1996) Viviparity and intragonadal cannibalism in the diminuitive sea stars Patiriella vivipara and P. parvivipara (Family Asterinidae). Mar Biol 125:551–567. doi: 10.1007/BF00353268 Google Scholar
  16. Byrne M (2005) Viviparity in the sea star Cryptasterina hystera (Asterinidae)—conserved and modified features in reproduction and development. Biol Bull 208:81–91. doi: 10.2307/3593116 PubMedGoogle Scholar
  17. Chen BY, Chen CP (1992) Reproductive cycle, larval development, juvenile growth and population dynamics of biology of Patiriella pseudoexigua (Echinodermata: Asteroidea) in Taiwan. Mar Biol 113:271–280Google Scholar
  18. Chia FS (1966) Brooding behavior of a six rayed starfish, Leptasterias hexactis. Biol Bull 130:304–315Google Scholar
  19. Chia FS (1968) The embryology of a brooding starfish, Leptasterias hexactis. Acta Zool Stockh 49:321–364Google Scholar
  20. Chia FS, Walker CW (1991) Echinodermata: Asteroidea. In: Giese A, Pearse J, Pearse V (eds) Reproduction of marine invertebrates, vol VI. Boxwood Press, California, pp 301–353Google Scholar
  21. Clark HES (1962) The fauna of the Ross Sea. Part 3, Asteroidea. Bull NZ Dep Scient Ind Res 151:1–84Google Scholar
  22. Clark A, Downey M (1992) Starfish of the Atlantic. An illustrated key. Koeltz Scientific Book, CambridgeGoogle Scholar
  23. Clarke A, Crame JA (2010) Evolutionary dynamics at high latitudes: Speciation and extinction in polar marine faunas. Phil Trans R Soc B 365:3655–3666. doi: 10.1098/rstb.2010.0270 PubMedGoogle Scholar
  24. Cohen C, Strathmann R (1996) Embryos at the edge of tolerance: effects of environment and structure of egg masses on supply of oxygen to embryos. Biol Bull 190:8–15PubMedGoogle Scholar
  25. Eernisse DJ, Strathmann MF, Strathmann RR (2010) Henricia pumila sp. nov.: A brooding seastar (Asteroidea) from the coastal northeastern Pacific. Zootaxa 2329:22–36Google Scholar
  26. Everingham JW (1961) The intra-ovarian embryology of Leptosynapta clarki. MS Thesis, University of Washington, Seattle, USAGoogle Scholar
  27. Fernández M, Ruiz-Tagle N, Cifuentes S, Pörtner HO, Arntz W (2003) Oxygen-dependent asynchrony of embryonic development in embryo masses of brachyuran crabs. Mar Biol 42:559–565. doi: 10.1007/s00227-002-0965-8 Google Scholar
  28. Fisher WK (1930) Asteroidea of the North Pacific and Adjacent Waters, Pt. 3: Forcipulata. Bull US Nat Mus 76:1–356Google Scholar
  29. Fisher WK (1940) Asteroidea. Discov Rep 20:1–305Google Scholar
  30. George SB (1994a) Population differences in maternal size and offspring quality for Leptasterias epichlora (Brandt) (Echinodermata: Asteroidea). J Exp Mar Biol Ecol 175:121–131. doi: 10.1016/0022-0981(94)90179-1 Google Scholar
  31. George SB (1994b) The Leptasterias (Echinodermata: Asteroidea) species complex: variation in reproductive investment. Mar Ecol Prog Ser 109:95–98Google Scholar
  32. Gil DG, Zaixso HE (2007) The relation between feeding and reproduction in Anasterias minuta (Asteroidea: Forcipulata). Mar Biol Res 3:256–264. doi: 10.1080/17451000701472035 Google Scholar
  33. Gil DG, Zaixso HE (2008) Feeding ecology of the sub-Antarctic sea star Anasterias minuta within tide pools in Patagonia, Argentina. Rev Biol Trop 56:311–328Google Scholar
  34. Gil DG, Zaixso HE, Tolosano JA (2009) Brooding of the sub-Antarctic heart urchin, Abatus cavernosus (Spatangoida: Schizasteridae), in southern Patagonia. Mar Biol 156:1647–1657. doi: 10.1007/s00227-009-1200-7 Google Scholar
  35. Gould SJ (1966) Allometry and size in ontogeny and phylogeny. Biol Rev Camb Philos Soc 41:587–640PubMedGoogle Scholar
  36. Haesaerts D, Jangoux M, Flammang P (2006) Adaptations to benthic development: functional morphology of the attachment complex of the brachiolaria larva in the sea star Asterina gibbosa. Biol Bull 211:172–182. doi: 10.2307/4134591 PubMedGoogle Scholar
  37. Hamel JF, Mercier A (1995) Prespawning behavior, spawning, and development of the brooding starfish Leptasterias polaris. Biol Bull 188:32–45PubMedGoogle Scholar
  38. Hayashi R (1943) Contributions to the classification of the sea-stars of Japan. II. Forcipulata, with the note on the relationships between the skeletal structure and respiratory organs of the sea-stars. J Fac Sci Hokkaido Univ Ser 6 Zool 8:13–281Google Scholar
  39. Hendler G (1979) Sex-reversal and viviparity in Ophiolepis kieri, n. sp., with notes on viviparous brittlestars from the Caribbean (Echinodermata: Ophiuroidea). Proc Biol Soc Wash 92:783–795Google Scholar
  40. Hendler G, Franz DR (1982) The biology of a brooding seastar, Leptasterias tenera, in Block Island sound. Biol Bull 162:273–289Google Scholar
  41. Hernández DA, Tablado A (1985) Asteroidea de Puerto Deseado (Santa Cruz, Argentina). Contribución No104. CENPAT, ArgentinaGoogle Scholar
  42. Himmelman JH, Lavergne Y, Cardinal A, Martel G, Jalbert P (1982) Brooding behaviour of the Northern sea star Leptasterias polaris. Mar Biol 68:235–240. doi: 10.1007/BF00409590 Google Scholar
  43. Hines AH (1982) Allometric constraints and variables of reproductive effort in brachyuran crabs. Mar Biol 69:309–320. doi: 10.1007/BF00397496 Google Scholar
  44. Hosmer DW, Lemeshow S (2000) Applied logistic regression, 2nd edn. Wiley, New YorkGoogle Scholar
  45. Hyman LH (1955) Echinodemata. The Invertebrates. IV. McGraw-Hill, New YorkGoogle Scholar
  46. Kamel SJ, Grosberg RK, Marshall DJ (2010) Family conflicts in the sea. Trends Ecol Evol 5:442–449. doi: 10.1016/j.tree.2010.05.008 Google Scholar
  47. Koehler R (1906) Echinodermes. Exped Ant Française (1903–1905), 41 pGoogle Scholar
  48. Komatsu M, Kano YT, Yoshizawa H, Akabane S, Oguro C (1979) Reproduction and development of the hermaphroditic sea-star, Asterina minor Hayashi. Biol Bull 157:258–274Google Scholar
  49. Komatsu M, O’Loughlin PM, Bruce B, Yoshizawa H, Tanaka K, Murakami C (2006) A gastric-brooding asteroid, Smilasterias multipara. Zool Sci 23:699–705PubMedGoogle Scholar
  50. Lane DJW, Beaumont AR, Hunter JR (1985) Byssus drifting and the drifting threads of the young post-larval mussel Mytilus edulis. Mar Biol 84:301–308. doi: 10.1007/BF00392500 Google Scholar
  51. Lawrence JM, Herrera J (2000) Stress and deviant reproduction in echinoderms. Zool Stud 39:151–171Google Scholar
  52. Lawrence JM, McClintock JB, Guille A (1984) Organic level and caloric caloric content of eggs of brooding asteroids and an echinoid (Echinodermata) from Kerguelen (South Indian Ocean). Int J Invert Reprod Dev 7:249–257Google Scholar
  53. Lieberkind I (1920) On a starfish (Asterias groenlandica) which hatches its young in its stomach. Vidensk Medd Dan Naturhist Foren 72:121–126Google Scholar
  54. Lindegarth M, Gamfeldt L (2005) Comparing categorical and continuous ecological analyses: effects of “wave exposure” on rocky shores. Ecology 86:1346–1357Google Scholar
  55. Litulo C (2005) Fecundity and size at sexual maturity of the fiddler crab Uca vocans (Linnaeus, 1758) (Brachyura: Ocypodidae). Thalassas 21:59–65Google Scholar
  56. Ludwig H (1903) Seesterne. Résultats du voyage du S.Y. Belgica en 1897-1898-1899. Rapp Sci, Zool R20:1–72Google Scholar
  57. Macbride EW, Simpson JC (1908) Echinoderma II. Echinoderm larvae. Nat Ant Exp (1901–1904) 4 (Zool):1–9Google Scholar
  58. McClary DJ, Mladenov PV (1990) Brooding biology of the sea star Pteraster militaris (O.F. Müller): energetic and histological evidence for nutrient translocation to brooded juveniles. J Exp Mar Biol Ecol 142:183–199. doi: 10.1016/0022-0981(90)90090-Y Google Scholar
  59. McClintock JB, Pearse JS (1986) Organic and energetic content of eggs and juveniles of antarctic echinoids and asterids with lecithotrophic development. Comp Bioch Physiol A 85:341–345Google Scholar
  60. McEdward LR, Janies DA (1993) Life cycle evolution in asteroids: What is a larva? Biol Bull 184:255–268PubMedGoogle Scholar
  61. McEdward LR, Janies DA (1997) Relationships among development, ecology, morphology in the evolution of echinoderm larvae and life cycles. Biol J Linn Soc 60:381–400Google Scholar
  62. McEdward LR, Miner BG (2001) Larval and life-cycle patterns in echinoderms. Can J Zool 79:1125–1170. doi: 10.1139/cjz-79-7-1125 Google Scholar
  63. Menge BA (1974) Effect of wave action and competition on brooding and reproductive effort in the seastar, Leptasterias hexactis. Ecology 55:84–93Google Scholar
  64. Menge BA (1976) Organization of the New England rocky intertidal community: role of predation, competition, and environmental heterogeneity. Ecol Monogr 46:355–393Google Scholar
  65. Mercier A, Hamel JF (2008) Depth-related shift in life history strategies of a brooding and broadcasting deep-sea asteroid. Mar Biol 156:205–223. doi: 10.1007/s00227-008-1077-x Google Scholar
  66. Metaxas A, Scheibling RE (1993) Community structure and organization of tidepools. Mar Ecol Prog Ser 98:187–198Google Scholar
  67. Meyer E, Manahan DT (2009) Nutrient uptake by marine invertebrates: cloning and functional analysis of amino acid transporter genes in developing sea urchins (Strongylocentrotus purpuratus). Biol Bull 217:6–24PubMedGoogle Scholar
  68. Mortensen T (1920) Studies in the development of crinoids. Pap Department of Marine Biology, Carnegie Institution of Washington, vol 16, pp 1–94Google Scholar
  69. Naughton KM, O’Hara TD (2009) A new brooding species of the biscuit star Tosia (Echinodermata: Asteroidea: Goniasteridae), distinguished by molecular, morphological and larval characters. Invertebr Syst 23:348–366Google Scholar
  70. Niesen TM (1973) Population and reproductive biology of the six-rayed sea star Leptasterias hexactis on the protected outer coast. PhD Thesis, University of Oregon, USAGoogle Scholar
  71. O’Brien FX (1976) Some adaptations of the seastar, Leptasterias littoralis (Stimpson) to life in the intertidal zone. Thalassia Jugoslavica 12:237–243Google Scholar
  72. O′Loughlin PM, O′Hara DT (1990) A review of the genus Smilasterias (Echinodermata, Asteroidea) with descriptions of two new species from south-eastern Australia, one a gastric brooder, and a new species from Maqcuarie Island. Mem mus Victoria 50:307–329Google Scholar
  73. Osterud HL (1918) Preliminary observations on the development of Leptasterias hexactis. Publ Puget Sound St 2:1–15Google Scholar
  74. Pearse JS, Bosch I (1994) Brooding in the Antarctic: Östergren had it nearly right. In: David B, Guille A, Féral JP, Roux M (eds) Echinoderms through time. Balkema, Rotterdam, pp 111–120Google Scholar
  75. Pearse JS, Mooi R, Lockhart SJ, Brandt A (2009) 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. Smithsonian Institution, Washington, pp 181–196Google Scholar
  76. Perrier E (1891) Echinodermes de la mission scientifique du Cap Horn. Stellérides. Miss Sci Cap Horn Zool 6:1–168Google Scholar
  77. Philippi RA (1870) Neue Seesterne aus Chile. Arch Naturges 36:268–275Google Scholar
  78. Prowse TAA, Pile AJ (2005) Phenotypic homogeneity of two intertidal snails across a wave exposure gradient in South Australia. Mar Biol Res 1:176–185Google Scholar
  79. Prowse TAA, Sewell MA, Byrne M (2008) Fuels for development: evolution of maternal provisioning in asterinid sea stars. Mar Biol 153:337–349. doi: 10.1007/s00227-007-0809-7 Google Scholar
  80. Raff RA, Byrne M (2006) The active evolutionary lives of echinoderm larvae. Heredity 97:244–252PubMedGoogle Scholar
  81. Raymond JF, Himmelman JH, Guderley HE (2004) Sex differences in biochemical composition, energy content and allocation to reproductive effort in the brooding sea star Leptasterias polaris. Mar Ecol Prog Ser 283:179–190Google Scholar
  82. Salvat MB (1985) Biología de la reproducción de Anasterias minuta Perrier (Echinodermata, Asteroidea), especie incubadora de las costas patagonicas. PhD thesis. Universidad de Buenos Aires, ArgentinaGoogle Scholar
  83. Sewell MA (1996) Mortality of pentactulae during intraovarian brooding in the apodid sea cucumber Leptosynapta clarki. Biol Bull 190:188–194PubMedGoogle Scholar
  84. Simpson RD (1982) The reproduction of some echinoderms from Macquarie Island. Austr Mus Mem 16:39–52Google Scholar
  85. Smith EA (1876) Descriptions of species of Asteriidae and Ophiuridae from Kerguelen′s Island. Ann and Mag Nat Hist ser 4(17):105–113Google Scholar
  86. Sokal RR, Rohlf FJ (1995) Biometry. The principles and practice of statistics in biological research, 3rd edn. WH Freeman and Company, New YorkGoogle Scholar
  87. Soliman ES, Nojima S (1984) Some observations on dispersal behavior of the early juvenile of the sea-star, Asterina minor. Publ Anakrrsa Mar Biol Lab 7:81–93Google Scholar
  88. Strathmann RR (1975) Larval feeding in echinoderms. Am Zool 15:717–730Google Scholar
  89. Strathmann RR, Strathmann MF (1982) The relationship between adult size and brooding in marine invertebrates. Am Nat 119:91–101Google Scholar
  90. Strathmann RR, Strathmann MF (1995) Oxygen supply and limits on aggregation of embryos. J Mar Biol Assoc UK 75:413–428. doi: 10.1017/S0025315400018270 Google Scholar
  91. 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
  92. Turner RL, Dearborn JH (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
  93. Turner RL, Lawrence JM (1979) Volume and composition of echinoderm eggs: implications for use of egg size in life-history models. In: Stancky SE (ed) Reproductive ecology of marine invertebrates. Univ South Carolina Press, Columbia, pp 25–40Google Scholar
  94. Vadas RL, Wright WA, Mille SL (1990) Recruitment of Ascophyllum nodosum: wave action as a source of mortality. Mar Ecol Prog Ser 61:263–272Google Scholar
  95. Vance RR (1973) On reproductive strategies in marine benthic invertebrates. Am Nat 107:339–352Google Scholar
  96. Verrill AE (1914) Monograph of the shallow-water starfishes of the North Pacific coast from the Arctic Ocean to California. Harriman Alaska Ser US Nat Mus 14:1–408Google Scholar
  97. Villinski JT, Villinski JC, Byrne M, Raff RA (2002) Convergent maternal provisioning and life-history evolution in echinoderms. Evolution 56:1764–1775. doi: 10.1111/j.0014-3820.2002.tb00190.x PubMedGoogle Scholar
  98. Worley EK, Franz DR, Hendler G (1977) Seasonal patterns of gametogenesis in a North Atlantic brooding asteroid, Leptasterias tenera. Biol Bull 153:237–253PubMedGoogle Scholar
  99. Zaixso HE (1975) Distribución vertical de los moluscos marinos de la ria Deseado (Santa Cruz, Argentina): sustratos con fracción limosa. Physis 34:229–243Google Scholar
  100. Zaixso HE, Pastor CT (1977) Observaciones sobre la ecología de los mitílidos de la ría Deseado. I. Distribución y análisis biocenótico. Ecosur 4:1–46Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Damián G. Gil
    • 1
    • 2
  • Graciela Escudero
    • 3
  • Héctor E. Zaixso
    • 1
    • 4
  1. 1.Instituto de Desarrollo CosteroUniversidad Nacional de la Patagonia San Juan Bosco (UNPSJB)Comodoro RivadaviaArgentina
  2. 2.Departamento de Biología GeneralFCN—UNPSJBComodoro RivadaviaArgentina
  3. 3.Centro Nacional Patagónico (CENPAT)Puerto MadrynArgentina
  4. 4.Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Buenos AiresArgentina

Personalised recommendations