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
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
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
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
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
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
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
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
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
Desurmont A (1996) Spawning and asexual reproduction of tropical holothurians. SPC Beche-de-mer Inf Bull 8:41
Desurmont A (2004) Natural spawning observations Bohadschia similis. SPC Beche-de-mer Inf Bull 20:37
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
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
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
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
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
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
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
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
Hamel J-F, Mercier A (1996a) Evidence of chemical communication during the gametogenesis of holothuroids. Ecology 77:1600–1616. doi:10.2307/2265555
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
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
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
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
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
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
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
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
Levitan DR (1995) Interspecific variation in fertilization success: the influence of gamete traits on sea urchin spawning success. Am Zool 35:136
McDowall RM (1969) Lunar rhythms in aquatic animals, a general review. Tuatata 17:133–144
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
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
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
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
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
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
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
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
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
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
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
Ong-Che RG, Gomez ED (1985) Reproductive periodicity of Holothuria scabra Jaeger at Calatagan, Batangas, Philippines. Asian Mar Biol 2:21–30
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
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
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
Reese ES (1966) The complex behaviour of echinoderms. In: Boolootian RA (ed) Physiology of echinodermata. Wiley, New York
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
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
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
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
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
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
Tommasi LR (1969) Lista dos holothuroidea recentes do Brasil. Contr Inst Oceanogr Univ São Paulo Ser Oceanogr Biol 15:15–129
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
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
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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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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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DOI: https://doi.org/10.1007/s00227-016-2842-x