Marine Biology

, Volume 156, Issue 8, pp 1647–1657 | Cite as

Brooding of the sub-Antarctic heart urchin, Abatus cavernosus (Spatangoida: Schizasteridae), in southern Patagonia

  • Damián G. GilEmail author
  • Héctor E. Zaixso
  • Javier A. Tolosano
Original Paper


The reproductive cycle of the sub-Antarctic spatangoid sea urchin, Abatus cavernosus, was examined during a 2-year period in southern Patagonia, Argentina. The population studied is the northernmost known coastal population in the austral oceans, and is influenced by a greater annual range of seawater temperature than other Abatus species. The sex ratio of the overall A. cavernosus population did not differ significantly from 1:1, but was not homogeneous across size classes. A clearly defined annual reproductive cycle was found. Spawning occurred from May to July and was synchronous between sexes. Females were observed to be brooding within a 9-month period, from May to February. Juveniles were released during the austral summer, from January to February. The length at which 50% of the females were brooding occurred at a test length of 25.9 mm. A. cavernosus had a large egg size (mean diameter = 1.4 mm) and low fecundity (maximum = 57 eggs per female) compared to closely related species. The number of eggs within each brood pouch was highest in larger anterior brood pouch, which is close to two gonopores, as opposed to the other anterior and two smaller posterior pouches. Significant interannual variation was observed in gonad cycles, fecundity, and embryo development such as: brood size decreased during 2001; adjusted gonad dry weight and fecundity were higher during 2003. Hypotheses concerning the gonadal and brooding cycles and fecundity of sub-Antarctic and Antarctic Schizasteridae are discussed.


Brood Size Seawater Temperature Test Length Brood Pouch Brooding Female 
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.



The authors are grateful to Eva Bogetti and Hernán Mazon for their assistance in the fieldwork. We also thank three anonymous reviewers for reading and improving earlier versions of this manuscript. The study was conducted at the Instituto de Desarrollo Costero (IDC-UNPSJB).

Supplementary material

227_2009_1200_MOESM1_ESM.pdf (92 kb)
Supplementary material S1 (PDF 92 kb)


  1. Arnaud PM (1974) Contribution à la bionomie marine benthique antarctique des régions antactiques et subantarctiques. Téthys 6:465–656Google Scholar
  2. Arntz WE (1999) Magellan–Antarctic: ecosystems that drifted apart. Sci Mar 63:503–511 (summary review)CrossRefGoogle Scholar
  3. Baeza JA, Fernández M (2002) Active brood care in Cancer setosus (Crustacea: Decapoda): the relationship between female behaviour, embryo oxygen consumption and the cost of brooding. Funct Ecol 16:241–251. doi: CrossRefGoogle Scholar
  4. Bernasconi I (1953) Monografía de los equinoideos argentinos. An Mus Hist Nat Montev 6(2):1–58Google Scholar
  5. Bernasconi I (1966) Los Equinoideos y Asteroideos colectados por el buque oceanográfico R/V “Vema”, frente a las costas argentinas, uruguayas y sur de Chile. Rev Mus Argent Cienc Nat “Bernandino Rivadavia Zool” 9:147–175Google Scholar
  6. Bingham BL, Giles K, Jaeckle WB (2004) Variability in broods of the seastar Leptasterias aequalis. Can J Zool 82:457–463. doi: CrossRefGoogle Scholar
  7. Bouvy M, Soyer J (1989) Benthic seasonality in an intertidal mud flat at Kerguelen Islands (Austral Ocean). The relationships between meiofaunal abundance and their potential microbial food. Polar Biol 10:19–27. doi: CrossRefGoogle Scholar
  8. Brockwell PJ, Davis RA (1987) Time series: theory and methods. Springer, New YorkCrossRefGoogle Scholar
  9. Carreto JI, Carignan MO, Montoya NG, Cucchi Colleoni AD (2007) Ecología del fitoplancton en los sistemas frontales del Mar Argentino. In: Carreto JI, Bremec C (eds) El Mar Argentino y sus recursos pesqueros. Tomo 5. El ecosistema marino. Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP), Mar del Plata, pp 11–31Google Scholar
  10. Chiantore M, Guidetti M, Cavallero M, De Domenico F, Albertelli G, Cattaneo-Vietti R (2006) Sea urchins, sea stars and brittle stars from Terra Nova Bay (Ross Sea, Antarctica). Polar Biol 29:467–475. doi: CrossRefGoogle Scholar
  11. Cox DR (1958) Planning of experiments. Wiley, New YorkGoogle Scholar
  12. Crame JA (1999) An evolutionary perspective on marine faunal connections between southernmost South America and Antarctica. Sci Mar 63:1–14CrossRefGoogle Scholar
  13. Figueiredo J, Penha-Lopes G, Anto J, Narciso L, Lin J (2008) Fecundity, brood loss and egg development through embryogenesis of Armases cinereum (Decapoda: Grapsidae). Mar Biol 154:287–294. doi: CrossRefGoogle Scholar
  14. Fischer G, Wiencke C (1992) Stable carbon isotope composition, depth distribution and fate of macroalgae from the Antarctic Peninsula region. Polar Biol 12:341–348. doi: CrossRefGoogle Scholar
  15. Galley EA, Tyler PA, Clarke A, Smith CR (2005) Reproductive biology and biochemical composition of the brooding echinoid Amphipneustes lorioli on the Antarctic continental shelf. Mar Biol 148:59–71. doi: CrossRefGoogle Scholar
  16. Gambi MC, Patti FP (1999) Reproductive biology of Perkinsiana antarctica (Kinberg) (Polychaeta, Sabellidae) in the Straits of Magellan (South America): systematic and ecological implications. Sci Mar 63:253–259CrossRefGoogle Scholar
  17. Gil DG, Zaixso HE (2007) The relation between feeding and reproduction in Anasterias minuta (Asteroidea, Forcipulata). Mar Biol Res 3:256–264. doi: CrossRefGoogle Scholar
  18. Gladfelter WB (1978) General ecology of the cassiduloid urchin Cassidulus caribearum. Mar Biol 47:149–160. doi: CrossRefGoogle Scholar
  19. Hamel JF, Mercier A (1995) Prespawning behaviour, spawning and development of the brooding starfish Leptasterias polaris. Biol Bull 188:32–45CrossRefPubMedGoogle Scholar
  20. 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
  21. Hendler G, Franz DR (1982) The biology of a brooding seastar, Leptasterias tenera, in Block Island Sound. Biol Bull 162:273–289CrossRefGoogle Scholar
  22. Hollertz K, Duchêne JC (2001) Burrowing behaviour and sediment reworking in the heart urchin Brissopsis lyrifera Forbes (Spatangoida). Mar Biol 139:951–957. doi: CrossRefGoogle Scholar
  23. Isla F, Iantanos N, Estrada E (2004) Dinámica submareal y condiciones ambientales de la ría Deseado, Santa Cruz. Rev Asoc Geol Argent 59:237–375Google Scholar
  24. Kaehler S, Pakhomov EA, McQuaid CD (2000) Trophic structure of the marine food web at the Prince Edward Islands (Southern Ocean) determined by 13C and δ15N analysis. Mar Ecol Prog Ser 208:13–20. doi: CrossRefGoogle Scholar
  25. Kasyanov VL (2001) Reproductive strategy of marine bivalves and echinoderms. Science Publishers, Enfield, NHGoogle Scholar
  26. Lawrence JM (1987) A functional biology of echinoderms. Johns Hopkins University Press, BaltimoreGoogle Scholar
  27. Lawrence JM, McClintock JB (1994) Energy acquisition and allocation by echinoderms (Echinodermata) in polar seas: adaptations for success? In: David B, Guille A, Féral JP, Roux M (eds) Echinoderms through time. Balkema, Rotterdam, pp 39–52Google Scholar
  28. Lawrence JM, McClintock JB, Guille A (1984) Organic level and caloric content of eggs of brooding asteroids and an echinoid (Echinodermata) from Kerguelen (South Indian Ocean). Int J Invertebr Reprod Dev 7:249–257CrossRefGoogle Scholar
  29. Legendre P, Legendre L (1998) Numerical ecology. Elsevier, AmsterdamGoogle Scholar
  30. Lovén S (1874) Etudes sur les échinoïdées. Kongl Sve Vetens Akad Handl 11:1–91Google Scholar
  31. MacCord FS, Ventura CRR (2004) Reproductive cycle of the endemic cassiduloid Cassidulus mitis (Echinoidea: Cassiduloida) on the Brazilian coast. Mar Biol 145:603–612. doi: CrossRefGoogle Scholar
  32. Madsen FJ (1955) Echinoderms other than Holothurians collected in sub-Antarctic and Antarctic seas, mainly by the “Norvegia” Expeditions 1928–1930. Sci Res Norw Antarct Exped 1927–1928 (Oslo) 3:1–17Google Scholar
  33. Magniez P (1980) Modalités de l’incubation chez Abatus cordatus (Verrill), oursin endémique des íles Kerguelen. In: Jangoux M (ed) Echinoderms: present and past. Balkema, Rotterdam, pp 399–403Google Scholar
  34. 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 74:55–64. doi: CrossRefGoogle Scholar
  35. McClintock JB, Pearse JS (1986) Organic and energetic content of eggs and juveniles of Antarctic echinoids and asteroids with lecithotrophic development. Comp Biochem Physiol 85A(2):341–345CrossRefGoogle Scholar
  36. McEdward LR, Janies DA (1997) Relationships among development, ecology, and morphology in the evolution of echinoderm larvae and life cycles. Biol J Linn Soc 60:381–400CrossRefGoogle Scholar
  37. Menge BA (1974) Effect of wave action and competition on brooding and reproductive effort in the seastar, Leptasterias hexactis. Ecology 55:84–93. doi: CrossRefGoogle Scholar
  38. Menge BA (1975) Brood or broadcast? The adaptative significance of different reproductive strategies in the two Intertidal sea stars Leptasterias hexactis and Pisaster ochraceus. Mar Biol 31:87–100. doi: CrossRefGoogle Scholar
  39. Mesphoulhé P, David B (1992) Strategie de croissance d’un oursin subantactique: Abatus cordatus des Iles Kerguelen. C R Acad Sci Paris 314:205–211Google Scholar
  40. Moore HB (1936) The biology of Echinocardium cordatum. J Mar Biol Assoc UK 20:655–672CrossRefGoogle Scholar
  41. Mortensen T (1910) The Echinoidea of the Swedish South polar expedition. Wiss Ergebn Schwed Südpolar Exped 1901–1903(6):1–114Google Scholar
  42. Mortensen T (1951) A monograph of the Echinoidea, vol 2, Spatangoida. Reitzel, CopenhagenGoogle Scholar
  43. Nakamura Y (2001) Autoecology of the heart urchin, Echinocardium cordatum, in the muddy sediment of the Seto Inland Sea, Japan. J Mar Biol Assoc UK 81:289–297CrossRefGoogle Scholar
  44. Packard GC, Boardman TJ (1999) The use of percentages and size-specific indices to normalize physiological data for variation in body size: wasted time, wasted effort? Comp Biochem Physiol A 122:37–44. doi: CrossRefGoogle Scholar
  45. 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
  46. 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
  47. Schatt P (1985) L’edificacion de la face orale au cours du développement direct d’Abatus cordatus, oursin incubant subantarctique. In: Keegan BF, O’Connor BDS (eds) Echinodermata. Balkema, Rotterdam, pp 339–345Google Scholar
  48. Schatt P (1988) Embryonic growth of the brooding sea urchin Abatus cordatus. In: Burke RD, Mladenov PV, Lambert P, Parsley RL (eds) Echinoderm biology. Balkema, Rotterdam, pp 225–228Google Scholar
  49. Schatt P, Féral JP (1991) The brooding cycle of Abatus cordatus (Echinodermata: Spatangoida) at Kerguelen Islands. Polar Biol 11:283–292. doi: CrossRefGoogle Scholar
  50. 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 190:24–44CrossRefPubMedGoogle Scholar
  51. Schinner GO, McClintock JB (1993) Structural characteristics of marsupial brood pouches of the Antarctic sea urchins Abatus nimrodi and Abatus shackletoni (Echinoidea: Spatangoida). J Morphol 216:79–93. doi: CrossRefPubMedGoogle Scholar
  52. Sewell MA (1996) Mortality of pentactulae during intraovarian brooding in the apodid sea cucumber Leptosynapta clarki. Biol Bull 190:188–194CrossRefPubMedGoogle Scholar
  53. Sokal RR, Rohlf FJ (1995) Biometry. The principles and practice of statistics in biological research, 3rd edn. Freeman, New YorkGoogle Scholar
  54. Strathmann RR, Chaffee C (1984) Constraints on egg masses. 2. Effect of spacing, size and number of egg on ventilation of embryos in jelly, adherent groups, or thin walled capsules. J Exp Mar Biol Ecol 84:85–93. doi: CrossRefGoogle Scholar
  55. Strathmann RR, Strathmann MF (1995) Oxygen supply and limits on aggregation of embryos. J Mar Biol Assoc UK 75:413–428CrossRefGoogle 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. ter Braak CJF, Smilauer P (1998) CANOCO reference manual and user’s guide to Canoco for Windows. Software for canonical community ordination (version 4). Microcomputer Power, Ithaca, NYGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Damián G. Gil
    • 1
    • 2
    Email author
  • Héctor E. Zaixso
    • 1
    • 3
  • Javier A. Tolosano
    • 1
  1. 1.Instituto de Desarrollo Costero (IDC)Universidad Nacional de la Patagonia San Juan Bosco (UNPSJB)Comodoro RivadaviaArgentina
  2. 2.Departamento de Biología GeneralFCN-UNPSJBComodoro RivadaviaArgentina
  3. 3.Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Buenos AiresArgentina

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