Marine Biology

, 163:67 | Cite as

Reproductive biology of the sea cucumber Holothuria grisea in Brazil: importance of social and environmental factors in breeding coordination

  • Liliane Veras Leite-CastroEmail author
  • José de Souza Junior
  • Carminda Sandra Brito Salmito-Vanderley
  • José Ferreira Nunes
  • Jean-François Hamel
  • Annie Mercier
Original paper


Sea cucumbers (Echinodermata: Holothuroidea) can contribute to the cycling of nutrients and play important roles as ecosystem engineers; many also have high commercial value. Their success at colonizing marine habitats from the shore to the abyss makes them ideal models for the study of breeding patterns. Here, the reproductive biology of the sea cucumber Holothuria grisea was studied at large and fine scales over 13 months on the northeastern Brazilian coast, to investigate the role of environmental and aggregative factors in this process. Gametogenic maturity peaked in December–February, as indices of spawning activity appeared and aggregative behavior was minimal. Mature individuals disappeared in June–July in both sexes, as the highest frequencies of aggregation and post-spawning stage were recorded. In August–September, gamete synthesis started to increase again in correlation with a higher frequency of individuals in the early gametogenic growth, while the degree of aggregation among individuals in the field was still high. Spawning occurred during the rainy season when chlorophyll-a concentrations were maximal, and the highest frequency of solitary individuals was recorded. The data are consistent with pre-spawning aggregative behavior as a strategy to help synchronize gametogenesis and phytoplankton bloom as a trigger of gamete release to optimize larval feeding. At finer scale, spawning occurred when high water levels coincided with sunset or night time, providing favorable conditions for free spawning and external fertilization. The influence of environmental factors and aggregation in the reproduction of H. grisea could potentially exacerbate its vulnerability to anthropogenic pressures (e.g., fisheries, pollution, habitat loss) along the coast of Brazil.


High Water Level Full Moon Oyster Reef Gonad Index Aggregative Behavior 
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.



Special thanks to M. E. M. Souza, R. V. Nascimento, V. A. Pereira, R. R. R. Pinheiro and J. T. Lopes for their help in the field. Many thanks as well to the reviewers for helping improve the manuscript, to the company which funded and supported the project (Cristália Laboratory Chemicals and Pharmaceuticals, São Paulo, Brazil) and to Cearense Foundation for the Support of Research—FUNCP and CAPES—Brazilian Federal Agency for Support and Evaluation of Graduate Education within the Ministry of Education of Brazil.

Supplementary material

227_2016_2842_MOESM1_ESM.pdf (96 kb)
Supplementary material 1 (PDF 95 kb)
227_2016_2842_MOESM2_ESM.pdf (223 kb)
Supplementary material 2 (PDF 223 kb)
227_2016_2842_MOESM3_ESM.pdf (193 kb)
Supplementary material 3 (PDF 193 kb)


  1. Asha OS, Muthiah P (2005) Effects of temperature, salinity and pH on larval growth, survival and development of the sea cucumber Holothuria spinifera Theel. Aquaculture 250:823–829. doi: 10.1016/j.aquaculture.2005.04.075 CrossRefGoogle Scholar
  2. Asha OS, Muthiah P (2008) Reproductive biology of the commercial sea cucumber Holothuria spinifera (Echinodermata: Holothuroidea) from Tuticorin, Tamil Nadu, India. Aquacult Int 16:231–242. doi: 10.1007/s10499-007-9140-z CrossRefGoogle Scholar
  3. Babcock R, Mundy C, Keesing J, Oliver J (1992) Predictable and unpredictable spawning events: in situ behavioural data from free-spawning coral reef invertebrates. Invertebr Reprod Dev 22:213–227. doi: 10.1080/07924259.1992.9672274 CrossRefGoogle Scholar
  4. Benítez-Villalobos F, Avila-Poveda OH, Gutiérrez-Méndez IS (2013) Reproductive biology of Holothuria fuscocinerea (Echinodermata: Holothuroidea) from Oaxaca, Mexico. Sex Early Dev Aquat Org 1:13–24. doi: 10.3354/sedao00003 CrossRefGoogle Scholar
  5. Bueno ML, Tavares YAT, Domenico MD, Borges M (2015) Gametogenesis and weight change of body organs of the sea cucumber Holothuria (Halodeima) grisea Aspidochirotida: Holothuriidae) in Southern Brazil. Rev Biol Trop 63:285–296Google Scholar
  6. Chao SM, Chen CP, Alexander PS (1995) Reproductive cycles of tropical sea cucumbers (Echinodermata: Holothuroidea) in southern Taiwan. Mar Biol 122:289–295. doi: 10.1007/BF00348942 Google Scholar
  7. Conand C (1993) Reproductive biology of the holothurians from the major communities of the New Caledonian Lagoon. Mar Biol 116:439–450. doi: 10.1007/BF00350061 CrossRefGoogle Scholar
  8. Conand C, Uthicke S, Hoareau T (2002) Sexual and asexual reproduction of the holothurian Stichopus chloronotus (Echinodermata): a comparison between La Réunion (Indian Ocean) and east Australia (Pacific Ocean). Invertebr Reprod Dev 41:235–242. doi: 10.1080/07924259.2002.9652756 CrossRefGoogle Scholar
  9. Desurmont A (1996) Spawning and asexual reproduction of tropical holothurians. SPC Beche-de-mer Inf Bull 8:41Google Scholar
  10. Desurmont A (2004) Natural spawning observations Bohadschia similis. SPC Beche-de-mer Inf Bull 20:37Google Scholar
  11. Dias IF (2012) Distribuição espaço-temporal e densidade populacional de Holothuria (Halodeima) grisea (Holothuroidea: Aspidochirotida) na praia de Bitupitá, Ceará, Nordeste do Brasil. Dissertation, Federal University of Ceará, BrazilGoogle Scholar
  12. Dissanayake DCT, Stefanssong G (2010) Reproductive biology of the commercial sea cucumber Holothuria atra (Holothuroidea: Aspidochirotida) in the northwestern coastal waters of Sri Lanka. Invertebr Reprod Dev 54:65–76. doi: 10.1080/07924259.2010.9652318 CrossRefGoogle Scholar
  13. Doyle GM, Hamel J-F, Mercier A (2012) A new quantitative analysis of ovarian development in echinoderms: the maturity stage index. Mar Biol 159:455–465. doi: 10.1007/s00227-011-1823-3 CrossRefGoogle Scholar
  14. Gaudron SM, Kohler SA, Conand C (2008) Reproduction of the sea cucumber Holothuria leucospilota in the Western Indian Ocean: biological and ecological aspects. Invertebr Reprod Dev 51:19–31. doi: 10.1080/07924259.2008.9652253 CrossRefGoogle Scholar
  15. Guzman HM, Guevara CA, Hernandez IC (2003) Reproductive cycle of two commercial species of sea cucumber (Echinodermata: Holothuroidea) from Caribbean Panama. Mar Biol 142:271–279. doi: 10.1007/s00227-002-0939-x Google Scholar
  16. Hadel FV, Monteiro AMV, Ditadi ASF, Tiago CG, Tommasi R (1999) Invertebrados Marinhos: Echinodermata. In: Joly CA, Bicudo CEM (eds) Biodiversidade do Estado de São Paulo, Brasil: síntese ao conhecimento ao final do século XX. Workshop “Foundations for conservation of biodiversity of the State of Sao Paulo” held in Serra Negra, SP, Brazil, from July 30 to August 2, 1997Google Scholar
  17. Hamel J-F, Mercier A (1995a) Spawning of the sea cucumber Cucumaria frondosa in the St Lawrence Estuary, eastern Canada. SPC Beche-de-mer Inf Bull 7:12–18Google Scholar
  18. Hamel J-F, Mercier A (1995b) Prespawning behavior, spawning, and development of the brooding starfish Leptasterias polaris. Bio Bull 188(1):32–45. doi: 10.2307/1542065 CrossRefGoogle Scholar
  19. Hamel J-F, Mercier A (1996a) Evidence of chemical communication during the gametogenesis of holothuroids. Ecology 77:1600–1616. doi: 10.2307/2265555 CrossRefGoogle Scholar
  20. Hamel J-F, Mercier A (1996b) Gonad morphology and gametogenesis of the sea cucumber Cucumaria frondosa. SPC Beche-de-mer Inf Bull 8:22–33Google Scholar
  21. Hamel J-F, Mercier A (1999) Mucus as a mediator of gametogenic synchrony in the sea cucumber Cucumaria frondosa (Holothuroidea: Echinodermata). J Mar Biol Assoc UK 79(1):121–129. doi: 10.1017/S0025315498000137 CrossRefGoogle Scholar
  22. Hamel J-F, Himmelman JH, Dufresne L (1993) Gametogenesis and spawning of the sea cucumber Psolus fabricii (Duben and Koren). Biol Bull 184(2):125–143. doi: 10.2307/1542223 CrossRefGoogle Scholar
  23. Hendler G, Miller JE, Pawson DL, Kier PM (1997) Sea stars, sea urchins and allies: Echinoderms of Florida and the Caribbean. J Exp Mar Biol Ecol 209:312–313. doi: 10.1016/S0022-0981(96)02646-9 CrossRefGoogle Scholar
  24. Herrero-Perezrul MD, Reyes-Bonilla H, Garcia-Dominguez F, Cintra-Buenrostro CE (1999) Reproduction and growth of Isostichopus fuscus (Echinodermata: Holothuroidea) in the Southern Gulf of California, Mexico. Mar Biol 135:521–532. doi: 10.1007/s002270050653 CrossRefGoogle Scholar
  25. Hooper DL, Hunter CR, Richmond RH (1998) Sexual reproduction of the tropical sea cucumber, Actinopyga mauritiana (Echinodermata: Holothuroidea), in Guam. Bull Mar Sci 63(1):1–9Google Scholar
  26. Kohler S, Gaudron S, Conand C (2009) Reproductive biology of Actinopyga echinites and other sea cucumbers from Reunion Island (Western Indian Ocean): a contribution for a regional management of the fishery. WIOJMS 8(1):97–111Google Scholar
  27. Kubota T, Tomari M (1998) Reproduction in the apodid sea cucumber Polycheira rufescens: semilunar spawning rhythm and sex change. J Mar Biol Assoc UK 78:249–267. doi: 10.1017/S0025315400040078 CrossRefGoogle Scholar
  28. Levitan DR (1995) Interspecific variation in fertilization success: the influence of gamete traits on sea urchin spawning success. Am Zool 35:136Google Scholar
  29. McDowall RM (1969) Lunar rhythms in aquatic animals, a general review. Tuatata 17:133–144Google Scholar
  30. Melo AA, Carneiro FR, Silva WM, Moura RM, Silva GC, Sousa OV, Saboya JPS, Nascimento KS, Saker-Sampaio S, Nagano CS, Cavada BS, Sampaio AH (2014) HGA-2, a novel galactoside-binding lectin from the sea cucumber Holothuria grisea binds to bacterial cells. Int J Biol Macromol 64:435–442. doi: 10.1016/j.ijbiomac.2013.12.035 CrossRefGoogle Scholar
  31. Mendes FM, Marenzi AWC, Domenico MD (2006) Population patterns and seasonal observations on density and distribution of Holothuria grisea (Holothuroidea: Aspidochirotida) on the Santa Catarina Coast, Brazil. SPC Beche-de-mer Inf Bull 23:5–10Google Scholar
  32. Mercier A, Hamel J-F (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 CrossRefGoogle Scholar
  33. Mercier A, Hamel J-F (2009) Endogenous and exogenous control of gametogenesis and spawning in echinoderms. Adv Mar Biol 55:1–302. doi: 10.1016/S0065-2881(09)55001-8 CrossRefGoogle Scholar
  34. Mercier A, Battaglene SC, Hamel J-F (2000a) Periodic movement, recruitment and size-related distribution of the sea cucumber Holothuria scabra in Solomon Islands. Hydrobiologia 440:81–100. doi: 10.1023/A:1004121818691 CrossRefGoogle Scholar
  35. Mercier A, Battaglene SC, Hamel J-F (2000b) Settlement preferences and early migration of the tropical sea cucumber Holothuria scabra. J Exp Mar Biol Ecol 249:89–110. doi: 10.1016/S0022-0981(00)00187-8 CrossRefGoogle Scholar
  36. Mercier A, Ycaza RH, Hamel J-F (2007) Long-term study of gamete release in a broadcast-spawning holothurian: predictable lunar and diel periodicities. Mar Ecol Prog Ser 329:179–189. doi: 10.3354/meps329179 CrossRefGoogle Scholar
  37. Mezali K, Thandar A (2014) First record of Holothuria (Roweothuria) arguinensis (Echinodermata: Holothuroidea: Aspidochirotida: Holothuriidae) from the Algerian coastal waters. Mar Biodivers Rec 7:1–4. doi: 10.1017/S175526721400043 CrossRefGoogle Scholar
  38. Moura RM, Aragão KS, Melo AA, Carneiro RF, Osório CBH, Luz PB, Queiroz AFS, Santos EA, Alencar NMN, Cavada BS (2013) Holothuria grisea agglutinin (HGA): the first invertebrate lectin with anti-inflammatory effects. Fundam Clin Pharm 27:656–668. doi: 10.1111/j.1472-8206.2012.01073.x CrossRefGoogle Scholar
  39. Navarro PG, García-Sanz S, Tuya F (2012) Reproductive biology of the sea cucumber Holothuria sanctori (Echinodermata: Holothuroidea). Sci Mar 76(4):741–752. doi: 10.3989/scimar.03543.15B Google Scholar
  40. Omar HA, Abdel-Razek FA, Abdel-Rahman SH, El-Shimy NA (2013) Reproductive periodicity of sea cucumber Bohadschia vitiensis (Echinodermata: Holothuroidea) in Hurghada area, Red Sea, Egypt. Egypt J Aquat Res 39:115–123. doi: 10.1016/j.ejar.2013.06.002 CrossRefGoogle Scholar
  41. Ong-Che RG, Gomez ED (1985) Reproductive periodicity of Holothuria scabra Jaeger at Calatagan, Batangas, Philippines. Asian Mar Biol 2:21–30Google Scholar
  42. Ramofafia C, Battaglene SC, Bell JD, Byrne M (2000) Reproductive biology of the commercial sea cucumber Holothuria fuscogilva in the Solomon Islands. Mar Biol 136:1045–1056. doi: 10.1007/s002270000310 CrossRefGoogle Scholar
  43. Ramofafia C, Byrne M, Battaglene SC (2001) Reproductive biology of the intertidal sea cucumber Actinopyga mauritiana in the Solomon Islands. J Mar Biol Assoc UK 81:523–531. doi: 10.1017/S0025315401004179 CrossRefGoogle Scholar
  44. Ramofafia C, Byrne M, Battaglene CS (2003) Reproduction of the commercial sea cucumber Holothuria scabra (Echinodermata: Holothuroidea) in the Solomon Islands. Mar Biol 142:281–288. doi: 10.1007/s00227-002-0947-x Google Scholar
  45. Reese ES (1966) The complex behaviour of echinoderms. In: Boolootian RA (ed) Physiology of echinodermata. Wiley, New YorkGoogle Scholar
  46. Reitzel AM, Miner BG, McEdward LR (2004) Relationships between spawning date and larval development time for benthic marine invertebrates: a modeling approach. Mar Ecol Prog Ser 280:13–23. doi: 10.3354/meps280013 CrossRefGoogle Scholar
  47. Roller RA, Stickle WB (1993) Effects of temperature and salinity acclimation of adults on larval survival, physiology, and early development of Lytechinus variegatus (Echinodermata: Echinoidea). Mar Biol 116:583–591. doi: 10.1007/BF00355477 CrossRefGoogle Scholar
  48. Santos R, Dias S, Pinteus S, Silva J, Alves C, Tecelão C, Pedrosa R, Pombo A (2015) Sea cucumber Holothuria forskali, a new resource for aquaculture? Reproductive biology and nutraceutical approach. Aquac Res. doi: 10.1111/are.12683 Google Scholar
  49. Shiell GR, Uthicke S (2006) Reproduction of the commercial sea cucumber Holothuria whitmaei (Holothuroidea: Aspidochirotida) in the Indian and Pacific Ocean regions of Australia. Mar Biol 148:973–986. doi: 10.1007/s00227-005-0113-3 CrossRefGoogle Scholar
  50. Sun GQ, Li L, Yi YH, Yuana WH, Liua BS, Wenga YY, Zhanga SL, Suna P, Wanga ZL (2008) Two new cytotoxic nonsulfated pentasaccharide holostane (20-hydroxylanostan-18-oic acid γ-lactone) glycosides from the sea cucumber Holothuria grisea. Helv Chim Acta 91:1453–1460. doi: 10.1002/hlca.200890158 CrossRefGoogle Scholar
  51. Tominaga H, Nakamura S, Komatsu M (2004) Reproduction and development of the conspicuously dimorphic brittle star Ophiodaphne formata (Ophiuroidea). Biol Bull 206:25–34. doi: 10.2307/1543195 CrossRefGoogle Scholar
  52. Tommasi LR (1969) Lista dos holothuroidea recentes do Brasil. Contr Inst Oceanogr Univ São Paulo Ser Oceanogr Biol 15:15–129Google Scholar
  53. Tyler PA, Young CM (1992) Reproduction in marine invertebrates in “stable” environments: the deep-sea model. Invertebr Reprod Dev 22:185–192. doi: 10.1080/07924259.1992.9672271 CrossRefGoogle Scholar
  54. Wigham BD, Hudson I, Billett DSM, Wolff GA (2003) Is long-term change in the abyssal Northeast Atlantic driven by qualitative changes in export flux? Evidence from selective feeding in deep-sea holothurians. Prog Oceanogr 59:409–441. doi: 10.1016/j.pocean.2003.11.0 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Liliane Veras Leite-Castro
    • 1
    Email author
  • José de Souza Junior
    • 2
  • Carminda Sandra Brito Salmito-Vanderley
    • 1
  • José Ferreira Nunes
    • 1
  • Jean-François Hamel
    • 3
  • Annie Mercier
    • 4
  1. 1.State University of CearáFortalezaBrazil
  2. 2.Federal University of CearáFortalezaBrazil
  3. 3.Society for the Exploration and Valuing of the Environment (SEVE)St. PhilipsCanada
  4. 4.Department of Ocean Sciences (OSC)Memorial UniversitySt. John’sCanada

Personalised recommendations