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Reproductive cycle of the sea cucumber Holothuria floridana in the littorals of Campeche, Mexico

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Abstract

The reproduction of Holothuria floridana in Campeche bay, southern Gulf of Mexico, was investigated over a period of 12 months by macroscopic and histological examination of the gonad and gametogenesis. A total of 1938 specimens were collected. Their body gutted weight and body gutted length ranged from 15 to 225 g and 5 to 21 cm, respectively. Percentage of the gonad weight to the gutted body weight (gonad index, GI) increased steadily from December to April, rapidly declined in May, and remained low during the following months. GI displayed a negative correlation with temperature of the habitat and no correlation with salinity. The gonad maturity scale with five stages was developed from macroscopic and microscopic observations; I, recovery; II, growing; III, early mature; IV, mature and V, spent. Stages III to V were observed all around the year, suggesting that this species displays continuous reproduction with two peaks of spawning events; from March to April and in September. The presence of viscera regurgitated individuals caused high variability in GI. The sex-ratio varied from 1:1 (December 2013 to June 2014), to 1.37:1 (November 2013); we suggest that this may be the consequence of unintentional selective fishing. The body length and body weight at the first maturity were calculated to be 13.4 cm and 87.0 g, respectively. For resource management it will be necessary to address some reference points like harvest season and avoidance of catches shorter than length at first maturity.

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References

  1. Purcell S, Samyn S, Conand C (2012) Commercially important sea cucumbers of the world. FAO Species Catalogue for Fishery Purposes No. 6 Rome

  2. Purcell SW, Lovatelli A, Vasconcellos M (2010) Managing sea cucumber fisheries with an ecosystem approach. FAO Fish and Aquac Tech Pap. No. 520 Rome

  3. Lovatelli A, Conand C, Purcell, Hamel JF, Mercer A (eds) (2014) Advances in sea cucumber aquaculture and management. FAO Fish Tech Pap No. 463 Rome

  4. SAGARPA (2013) Statistical yearbook of aquaculture and fisheries. National Board of Aquaculture and Fisheries, México (In Spanish)

    Google Scholar 

  5. Hernández-Flores A, Ardisson Herrera PL, Poot Salazar CA, Espinoza Méndez JC (2012) Baseline for ban establishment of sea cucumbers from the coasts of the Yucatan Peninsula. Technical Report, SAGARPA, National Board of Fisheries, pp 8 (In Spanish)

  6. Ramos-Miranda J, Flores-Hernández D, Flores Ramos EF, Pech D, Soto JL, Solís FS, Ayala L, del Río R, Rendón J, Pacheco M, Can F, Duarte A, Aguilar F (2012) The sea cucumber (H. floridana) from the coasts of Campeche, final report. EPOMEX Institute, Campeche University, pp 78 (In Spanish)

  7. Poot-Salazar A (2010) Growth, reproduction and feeding habits of Isostichopus badionotus Selenka, 1867 (Echinodermata: Holothuroidea) from the western coasts of Yucatan State, doctoral dissertation. CINVESTAV-Mérida, México (In Spanish)

    Google Scholar 

  8. Conand C (1993) Reproductive biology of the holothurians from the major communities of the New Caledonian lagoon. Mar Biol 116:439–450

    Article  Google Scholar 

  9. Conand C (1993) Ecology and reproductive biology of Stichopus variegatus an Indo-Pacific Coral Reef sea cucumber (Echinodermata: Holothuroidea). Bull Mar Sci 52(3):970–981

    Google Scholar 

  10. Chao SM, Chen CP, Alexander PS (1995) Reproductive cycles of tropical sea cucumbers (Echinodermata: Holothuroidea) in Southern Taiwan. Mar Biol 122:289–295

    Google Scholar 

  11. Engstrom NA (1980) Reproductive cycles of Holothuria (Halodeima) floridana, H. (H) mexicana and their hybrids (Echinodermata: Holothuroidea) in southern Florida. Invertebr Reprod Dev 2:237–244

    Article  Google Scholar 

  12. Villalobos-Figueroa A, Zamora EM (1975) Biological aspects of Campeche Bay. Memoirs of the I Latin American Simp Oceano Biol México 1974:375–394 (In Spanish)

    Google Scholar 

  13. Licea S, Luna R (1999) Spatio-temporal variation of phytoplankton on the continental margin in the SW Gulf of Mexico. Rev Soc Mex His Nat 48:83–99

    Google Scholar 

  14. Pacheco-Cervera MC, Pacheco-Ruíz I, Ramos-Miranda J, Cetz-Navarro NP, Soto-Ávila JL (2010) Presence of Caulerpa genus from the bay of Campeche. Hidrobiologica 20:57–69 (In Spanish)

    Google Scholar 

  15. Hendler G, Miller JE, Pawson DL, Kier PM (1995) Sea stars, sea urchins, and allies. Smithsonian Institution, Washington

    Google Scholar 

  16. Conand C (1986) Les ressources halieuthiques des pays insulaires du Pacifique. Deuxième partie: Les holothuries. FAO. Doc Tech sur les pêches. 272.2. Roma

  17. Hamel J, Himmelman J, Dufresne L (1993) Gametogenesis and spawning of the sea cucumber Psolus fabricii. Biol Bull 148:125–143

    Article  Google Scholar 

  18. 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

    Article  Google Scholar 

  19. Ramofafía 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

    Article  Google Scholar 

  20. Shiell G, Uthicke S (2006) Reproduction of the commercial sea cucumber Holothuria whitmaei (Holoturoidea: Aspidochirotida) in the Indian and Pacific Ocean regions of Australia. Mar Biol 148:973–986

    Article  Google Scholar 

  21. Conand C (1981) Sexual cycles of three commercially important holothurian species (Echinodermata) from the lagoon of New Caledonia. Bull Mar Sci 31:523–543

    Google Scholar 

  22. Ramofafia C, Battaglene SC, Byrne M (2001) Reproductive biology of Actinopyga mauritiana (Echinodermata: Holothuridae) in the Solomon Islands. J Mar Biol Assoc UK 81:523–531

    Article  Google Scholar 

  23. Boolootian RA (1966) Reproductive Physiology. In: Boolootian RA (ed) Physiology of Echinodermata. Wiley-Interscience, New York, pp 561–613

    Google Scholar 

  24. Giese AC, Pearse JS (1974) Introduction: general principals. In: Giese AC, Pearse JS (eds) Reproduction of marine invertebrates. Blackwell SCI Pub, Palo Alto, pp 1–49

    Google Scholar 

  25. Conand C (1982) Reproductive cycle and biometric relations in a population of Actinopyga echinites (Echinodermata: Holothuroidea) from the lagoon on New Caledonia, western tropical Pacific. In: Lawrence JM (ed) Proc. Int’l. Echinoderm Conf. Univ, South Florida, Tampa, Florida, pp 437–442

    Google Scholar 

  26. Conand C (1989) The fishery resources of Pacific island countries. Part 2: Holothurians. FAO Fish Tech Pap 272.2. Roma

  27. Harriot VJ (1985) Reproductive biology of three congeneric sea cucumber species, Holothuria atra, H. impatiens, and H. edulis, at Heron Reef, Great Barrier Reef. Aust J Mar Freshw Res 36:51–57

    Article  Google Scholar 

  28. Sewell MA, Berquist PR (1990) Variability in the reproductive cycle of Stichopus mollis (Echinodermata: Holothuroidea). Invertebr Reprod Dev 17:1–7

    Article  Google Scholar 

  29. Smiley S, McEuen F, Chaffee C, Krishnen S (1991) Echinodermata: Holothuroidea. In: Giese AC et al (eds) Reproduction of marine invertebrates. Vol. 6: Echinoderms and lophophorats. Boxwood Press, Pacific Grove, pp 663–750

    Google Scholar 

  30. Sparre P, Venema SC (1992) Introduction to topical fish stock assessment. FAO, Fish Tech Pap 306.1 Rome

  31. Fuente-Betancourt G, Jesús-Navarrete A, Sosa-Cordero E, Herrero-Perezrul MD (2001) Assessment of the sea cucumber (Echinodermata: Holothuroidea) as potential fishery resource in Banco Chinchorro, Quintana Roo. Mexico Bull Mar Sci 68(1):59–67

    Google Scholar 

  32. Muthiga NA (2006) The reproductive biology of a new species of sea cucumber, Holothuria (Mertensiothuria) arenacava in a Kenyan marine protected area: the possible role of light and temperature on gametogenesis and spawning. Mar Biol 149:585–593

    Article  Google Scholar 

  33. Muthiga NA, Kawaka JA, Ndirangu S (2009) The timing and reproductive output of the commercial sea cucumber Holothuria scraba on the Kenyan coast. Estuar Coast Shelf Sci 84:353–360

    Article  Google Scholar 

  34. Nguyen VN, Britaev TA (1992) Reproductive cycle of sea cucumber Holothuria leucospilota in Nha Trang Bay (Southern Vietnam). Russ J Mar Biol 5–6:70–77

    Google Scholar 

  35. Gonor JJ (1972) Gonad growth in the sea urchin, Strongylocentrotus purpuratus (Stimpson) (Echinodermata: Echinoidea) and the assumptions of gonad index methods. J Exp Mar Biol Ecol 10:89–103

    Article  Google Scholar 

  36. Mezali KD, Soualili L, Neghli L, Conand C (2014) Reproductive cycle of the sea cucumber Holothuria (Platyperona) sanctori (Holothuroidea: Echinodermata) in the southwestern Mediterranean Sea: interpopulation variability. Invertebr Reprod Dev. doi:10.1080/07924259.2014.883337

    Google Scholar 

  37. Hopper D, Hunter C, Richmond R (1998) Sexual reproduction of the tropical sea cucumber, Actinopyga mauritiana (Echinodermata: Holothuroidea). Guam Bull Mar Sci 63(1):1–9

    Google Scholar 

  38. Cameron JL, Fankboner PV (1986) Reproductive biology of the commercial sea cucumber Parastichopus californicus (Stimpson) (Echinodermata: Holothuroidea). I Reproductive periodicity and spawning behavior. Can J Zool 64:168–175

    Article  Google Scholar 

  39. Starr M, Himmelman JH, Therriault JC (1990) Direct coupling of marine invertebrates spawning with phytoplankton blooms. Science 247:1071–1074

    Article  CAS  PubMed  Google Scholar 

  40. Kithakeni T, Ndaro S (2002) Some aspects of sea cucumber, Holothuria scabra (Jaeger, 1935), along the coast of Dar es Salaam. West. Indian Ocean. J Mar Sci 1:163–168

    Google Scholar 

  41. Navarro PG, García-Sanz S, Tuya F (2012) Reproductive biology of the sea cucumber Holothuria sanctori (Echinodermata: Holothuroidea). Sci Mar 76:741–752

    Google Scholar 

  42. Drumm DJ, Loneragan NR (2005) Reproductive biology of Holothuria leucospilota in the Cook Islands and the implication of traditional fishing of gonads on the population. N Z J Mar Freshw Res 39:141–146

    Article  Google Scholar 

  43. Ramofafía C, Byrne M (2001) Assessment of the tubule recruitment model in three tropical Aspidochirote holothurians. SPC Beche-de-mer Inf Bull 5:13–16

    Google Scholar 

  44. Guzmán H, Guevara C, Hernández I (2003) Reproductive cycle of two commercial species of sea cucumber (Echinodermatha: Holothuroidea) from Caribbean Panama. Mar Biol 142:271–279

    Article  Google Scholar 

  45. Rasolofonirina R, Vaïtilingon D, Eeckhaut I, Jangoux M (2005) Reproductive cycle of edible echinoderms from the south-western Indian Ocean II: The sandfish Holothuria scabra (Jaëger, 1983) Western Indean Ocean. J Mar Sci 4:61–75

    Google Scholar 

  46. Asha PS, Muthiah P (2008) Reproductive biology of the commercial sea cucumber Holothuria spinifera (Echinodermata: Holothuroidea) from Tuticorin, Tami Nadu, India. Aquac Int 16:231–242

    Article  Google Scholar 

  47. Swan EF (1961) Seasonal evisceration in the sea cucumber Parastichopus californicus (Stimpson). Science 133:1078–1079

    Article  CAS  PubMed  Google Scholar 

  48. Byrne M (2001) The morphology of autotomy structues in the sea cucumber Eupentacta quinquesemita before and during evisceration. J Exp Biol 204:849–863

    CAS  PubMed  Google Scholar 

  49. Emson RH, Wilkie IC (1980) Fission and autotomy in echinoderms. Oceanogr Mar Biol 18:155–250

    Google Scholar 

  50. Byrne M (1986) The ultrastucture of the morula cells of Eupentacta quinquesemita (Echinodermata Holothuroidaea) and their role in the maintenance of the extracellular matrix. J Morphol 188:179–189

    Article  Google Scholar 

  51. Fankboner PV, Cameron JL (1985) Seasonal atrophy of the visceral organs in a sea cucumber. Can J Zool 63:2888–2892

    Article  Google Scholar 

  52. Shinn GL (1985) Reproduction of Anoplodium hymanae, a turbellarian flatworm (Niophabdocoela, Umagillidae) inhabiting the coelom of sea cucumbers: production of egg capsules, and escape of infective stages without evisceration of the host. Biol Bull 169:182–198

    Article  Google Scholar 

  53. Shinn GL, Stricker SA, Cavey MJ (1990) Ultrastructure of transrectal coelomoducts in the sea cucumber Parastichopus californicus (Echinodermata, Holothuroidea). Zoomorphology 109:189–199

    Article  Google Scholar 

  54. Toral-Granada MV, Martínez PC (2007) Reproductive biology and population structure of the sea cucumber Isostichopus fuscus (Ludwig, 1987) (Holoturoidea) in Caamaño, Galápagos Islands. Ecuador Mar Biol 151:2091–2098

    Article  Google Scholar 

  55. Ghobadyan F, Morovvati H, Ghazvineh L, Tavassolpour E (2012) An investigation of the macroscopic and microscopic characteristics of gonadal tubules in the sea cucumber Holothuria leucospilota (Persian Gulf, Iran). SPC Beche-de-mer Inf Bull 32:6–12

    Google Scholar 

  56. Purwati P, Luong-van JT (2003) Sexual reproduction in a fissiparous holothurian species, Holothuria leucospilota Clark 1920 (Echinodermata: Holothuroidea). SPC Beche-de-mer Inf Bull 18:33–38

    Google Scholar 

  57. Edwards C (1908) Variation, development and growth in Holothuria floridana Portualés and in Holothuria atra Jager. Biometrika 6:236–301

    Article  Google Scholar 

  58. Sewell MA, Tyler P, Young C, Connand C (1997) Ovarian development in the class Holothuroidea: a reassessment of the tubule recruitment model. Biol Bull 192:17–26

    Article  CAS  PubMed  Google Scholar 

  59. Purwati P, Luong-van JT (2003) Sexual reproduction in a fissiparous holothurian species, Holothuria leucospilota Clark 1920 (Echinodermata: Holothuroidea). SPC Beche-de-mer Inf Bull 18:33–38

    Google Scholar 

  60. Keshavarz M, Mohammadikia D, Dabbagh AR, Kamrani E (2012) Reproductive biology of the sea cucumbers for successful breeding: a review. J Anim Prod Adv 2(2):208–2013

    Google Scholar 

  61. Rojas González RI, Ramos Miranda J, Flores Hernández D, del Río Rodríguez R, Sosa López A, Espinoza Méndez JC, Poot Salazar AV (2014) Stock assessment of the sea cucumber Holothuria floridana from the coasts of Campeche. Final Report. 2013. National Institute of Fisheries, SAGARPA, pp 103 (In Spanish)

  62. Foglietta LM, Camejo MI, Gallardo L, Herrera FC (2004) A maturity index for holothurians exhibiting asynchronous development of gonad tubules. J Exp Mar Biol Ecol 303:19–30

    Article  Google Scholar 

  63. Caddy JF, Mahon R (1995) Reference points for fisheries management. Series: FAO Fish Tech Pap. 347. FAO. Roma

  64. Gaudron S, Kohler S, Conand C (2008) Reproduction of the sea cucumber Holothuria leucospilota in the fringing reef of Reunion Island (Western Indian Ocean): biological and ecological aspects. Invertebr Reprod Dev 51:19–31

    Article  Google Scholar 

  65. Lokani P (1995) Fishery dynamics, ecology and management of Beche de mer at Worrior Reefs, Torres Straight protected zone. Papua New Guinea SPC Beche de Mer Info Bull 9:42

    Google Scholar 

  66. Abdel-Razek FA, Abdel-Rahman SH, El-Shimy NA, Omar HA (2005) Reproductive biology of the tropical sea cucumber Holothuria atra (Echinodermata: Holothuroidea) in the Red Sea coast of Egypt. Egyptian J Aqua Res 31:383–402

    Google Scholar 

  67. Fajardo-León MC, Suárez-Higuera MCL, Manríquez A, López A (2008) Reproductive biology of the sea cucumber Parastichopus parvimensis (Echinodermata: Holothuroidea) from Isla Natividad and Bahía Tortugas, Baja California Sur, Mexico. Autonomous University of Baja California. Cienc Mar 34:165–177 (In Spanish)

    Article  Google Scholar 

  68. Reichenbach N (1999) Ecology and Fishery Biology of Holothuria fuscolgiva (Echinodermata: Holothuroidea) in the Maldives Indian Ocean. Bull of Mar Sci 64:103–113

    Google Scholar 

  69. Herrero-Pérezrul M (2004) Analysis of the sea cucumber fishery in the Baja California Peninsula, Mexico. Doctoral Dissertation in Marine Sciences. National Polytechnic Institute. Interdisciplinary Center for Marine Sciences, p 143 (In Spanish)

  70. Kazanidis G, Lolas A, Vafidis D (2014) Reproductive cycle of the traditionally exploited sea cucumber Holothuria tubulosa (Holothuroidea: Aspidochirotida) in Pagasitikos Gulf, western Aegean Sea, Greece. Turkish J Zool 38:306–315

    Article  Google Scholar 

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Acknowledgements

The authors would like to acknowledge Campeche Produce Foundation (Fundación Produce Campeche), for sponsoring the project “Evaluación de Pepino Holothuria floridana en Costas de Campeche” corresponding to Component Transfer of Technology and Innovation (Innovación y Transferencia de Tecnología 2013). Also, we acknowledge Francisco Cab Noh, Daniel Santana, Ismael Carrillo, Diego Hau, Maricela Ake Suastes, and E. Flores Ramos who supported this work through sample collection.

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Authors and Affiliations

  1. Instituto EPOMEX, Universidad Autónoma de Campeche, Av. Héroe de Nacozari. No. 480, Campus VI de Investigación-UAC, San Francisco de Campeche, 24020, Campeche, Mexico

    Julia Ramos-Miranda, Rodolfo del Río-Rodríguez, Domingo Flores-Hernández, Ana Delia Cu-Escamilla, Francisco Gómez-Criollo, Atahualpa Sosa-López, Yassir Eden Torres-Rojas & Paloma Juárez-Camargo

  2. Facultad de Ciencias Quimico-Biológicas, Universidad Autónoma de Campeche, Av. Agustín Melgar s/n. Col. Buenavista, 24030, Campeche, Mexico

    Mónica Gómez-Solano

  3. Centro Regional de Investigación Pesquera Lerma, Instituto Nacional de la Pesca, Kilómetro 5, Carretera Campeche-Lerma, 24500, Campeche, Mexico

    Ramón Isaac Rojas-González

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  1. Julia Ramos-Miranda
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  2. Rodolfo del Río-Rodríguez
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  3. Domingo Flores-Hernández
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Correspondence to Julia Ramos-Miranda.

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Ramos-Miranda, J., del Río-Rodríguez, R., Flores-Hernández, D. et al. Reproductive cycle of the sea cucumber Holothuria floridana in the littorals of Campeche, Mexico. Fish Sci 83, 699–714 (2017). https://doi.org/10.1007/s12562-017-1100-6

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