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

Abstract

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.

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References

  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

    CAS  Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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 63:285–296

    Google 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

    Article  Google 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

    Article  Google Scholar 

  9. Desurmont A (1996) Spawning and asexual reproduction of tropical holothurians. SPC Beche-de-mer Inf Bull 8:41

    Google Scholar 

  10. Desurmont A (2004) Natural spawning observations Bohadschia similis. SPC Beche-de-mer Inf Bull 20:37

    Google 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, Brazil

  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

    Article  Google 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

    Article  Google 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

    Article  Google 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, 1997

  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 7:12–18

    Google 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

    Article  Google 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

    Article  Google Scholar 

  20. Hamel J-F, Mercier A (1996b) Gonad morphology and gametogenesis of the sea cucumber Cucumaria frondosa. SPC Beche-de-mer Inf Bull 8:22–33

    Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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):1–9

    Google 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):97–111

    Google 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

    Article  Google Scholar 

  28. Levitan DR (1995) Interspecific variation in fertilization success: the influence of gamete traits on sea urchin spawning success. Am Zool 35:136

    Google Scholar 

  29. McDowall RM (1969) Lunar rhythms in aquatic animals, a general review. Tuatata 17:133–144

    Google 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

    Article  Google 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 23:5–10

    Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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

    CAS  Article  Google 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

    Article  Google Scholar 

  41. Ong-Che RG, Gomez ED (1985) Reproductive periodicity of Holothuria scabra Jaeger at Calatagan, Batangas, Philippines. Asian Mar Biol 2:21–30

    Google 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

    Article  Google 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

    Article  Google 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 York

    Google 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

    Article  Google 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

    Article  Google 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

    Article  Google 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

    CAS  Article  Google 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

    Article  Google Scholar 

  52. Tommasi LR (1969) Lista dos holothuroidea recentes do Brasil. Contr Inst Oceanogr Univ São Paulo Ser Oceanogr Biol 15:15–129

    Google 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

    Article  Google 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

    Article  Google Scholar 

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Acknowledgments

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.

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Correspondence to Liliane Veras Leite-Castro.

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Responsible Editor: S. Uthicke.

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Leite-Castro, L.V., de Souza Junior, J., Salmito-Vanderley, C.S.B. et al. Reproductive biology of the sea cucumber Holothuria grisea in Brazil: importance of social and environmental factors in breeding coordination. Mar Biol 163, 67 (2016). https://doi.org/10.1007/s00227-016-2842-x

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Keywords

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