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Effects of light and microhabitat on activity pattern and behaviour of wild and hatchery-reared juveniles of Stichopus cf. horrens

Published online by Cambridge University Press:  23 June 2017

Nadia Palomar-Abesamis Open the ORCID record for Nadia Palomar-Abesamis [Opens in a new window] ,
Marie Antonette Juinio-Meñez  and
Matthew James Slater
Nadia Palomar-Abesamis*
Affiliation:
The Marine Science Institute, University of the Philippines, Diliman, Quezon City 1101, Philippines Biology Department, Silliman University, Dumaguete City, Negros Oriental 6200, Philippines
Marie Antonette Juinio-Meñez
Affiliation:
The Marine Science Institute, University of the Philippines, Diliman, Quezon City 1101, Philippines
Matthew James Slater
Affiliation:
Alfred-Wegener-Institute Helmholtz Center for Polar and Marine Research, Am Handelshafen 12 Bremerhaven 27570, Germany
*
Correspondence should be addressed to: N. Palomar-Abesamis, The Marine Science Institute, University of the Philippines, Diliman, Quezon City 1101, Philippines email: nadia.abesamis@gmail.com
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Abstract

Animals develop behavioural strategies throughout life to improve their survival in nature. Juvenile activity and behaviour of the commercial tropical sea cucumber Stichopus cf. horrens were examined considering factors that may influence survival at this critical developmental stage. Wild juveniles were observed in situ to describe diel activity and movement. Wild and hatchery-reared juveniles were observed in the laboratory to evaluate the influence of different light-dark cycles and microhabitats on feeding and sheltering behaviour. All juveniles (4–54 g) displayed a distinct nocturnal activity pattern both in the field and laboratory. Nocturnal activity was strongly associated with feeding and locomotion. Wild and hatchery-reared juveniles were most active at night, displayed intermediate activity during twilight, and minimal to no activity during daytime. Movement rates of wild juveniles in situ were significantly influenced by time and size to a lesser extent. Under constant light and constant dark for 48 h, juvenile feeding rhythm was endogenously controlled and strongly entrained to natural light-dark cycles. Sheltering was directly affected by light and linked to strong phototactic and thigmotactic reflexes. Juveniles preferred vegetation as shelter compared to coral, sand or open space, and showed equal preference for seagrass and macroalgae. Deviations in behaviour of hatchery-reared juveniles under laboratory conditions indicate some degree of acclimation to an artificial environment with minimal threats and a decreased sensitivity to light. The implications of nocturnal feeding, light-induced sheltering, shelter preferences and acclimation to artificial conditions are discussed in relation to juvenile survival in nature and potential restocking of the species.

Keywords

sea cucumberfeedingshelteringnocturnalphototaxisthigmotaxisseagrassmacroalgaerestocking
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 7 , November 2018 , pp. 1703 - 1713
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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References

REFERENCES

Abedin, M.Z., Karim, A.A., Ahmed, F., Latiff, A.A., Gan, C.Y., Che Ghazali, F., Sarker, I. and Zaidul, M. (2013) Isolation and characterization of pepsin-solubilized collagen from the integument of sea cucumber (Stichopus vastus). Journal of the Science of Food and Agriculture 93, 1083–1088.Google Scholar
Adams, N.L. (2001) UV radiation evokes negative phototaxis and covering behavior in the sea urchin Strongylocentrotus droebachiensis. Marine Ecology Progress Series 213, 87–95.Google Scholar
Akamine, J. (2002) Trepang exploitation in the Philippines: updated information. SPC Bêche-de-mer Information Bulletin 17, 17–21.Google Scholar
Aschoff, J. (1981) Free-running and entrained circadian rhythms. In Aschoff, J. (ed.) Handbook of behavioral neurobiology. Vol. 4, biological rhythms. New York, NY: Plenum Press, pp. 81–92.Google Scholar
Bakus, G.J. (1968) Defensive mechanisms and ecology of some tropical holothurians. Marine Biology 2, 23–32.Google Scholar
Bazes, A., Silkina, A., Douzenel, P., Faÿ, F., Kervarec, N., Morin, D., Berge, J.P. and Bourgougnon, N. (2009) Investigation of the antifouling constituents from the brown alga Sargassum muticum (Yendo) Fensholt. Journal of Applied Phycology 21, 395–403.Google Scholar
Bell, J.D., Leber, K.M., Lee Blankenship, H., Loneragan, N.R. and Masuda, R. (2008) A new era for restocking, stock enhancement and sea ranching of coastal fisheries resources. Reviews in Fisheries Science 16, 1–9.Google Scholar
Bordbar, S., Anwar, F. and Saari, N. (2011) High-value components and bioactives from sea cucumbers for functional foods – a review. Marine Drugs 9, 1761–1805.Google Scholar
Brokordt, K.B., Fernández, M. and Gaymer, C.F. (2006) Domestication reduces the capacity to escape from predators. Journal of Experimental Marine Biology and Ecology 329, 11–19.Google Scholar
Burnham, K.P., Anderson, D.R. and Huyvaert, K.P. (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behavioral Ecology and Sociobiology 65, 23–35.Google Scholar
Byrne, M., Rowe, F. and Uthicke, S. (2010) Molecular taxonomy, phylogeny and evolution in the family Stichopodidae (Aspidochirotida: Holothuroidea) based on COI and 16S mitochondrial DNA. Molecular Phylogenetics and Evolution 56, 1068–1081.Google Scholar
Cameron, J.L. and Fankboner, P.V. (1989) Reproductive biology of the commercial sea cucumber Parastichopus californicus (Stimpson) (Echinodermata: Holothuroidea). II. Observations on the ecology of development, recruitment, and the juvenile life stage. Journal of Experimental Marine Biology and Ecology 127, 43–67.Google Scholar
Cho, J.Y. (2013) Antifouling chromanols isolated from brown alga Sargassum horneri. Journal of Applied Phycology 25, 299–309.Google Scholar
Choo, P.S. (2008) The Philippines: a hotspot of sea cucumber fisheries in Asia. In Toral-Granda, V., Lovatelli, A. and Vasconcellos, M. (eds) Sea cucumbers: a global review of fisheries and trade. Fisheries and Aquaculture Technical Paper No. 516. Rome: FAO, pp. 119–140.Google Scholar
Conand, C. (1993) Ecology and reproductive biology of Stichopus variegatus, an Indo-Pacific coral reef sea cucumber (Echinodermata: Holothuroidea). Bulletin of Marine Science 52, 970–981.Google Scholar
Conand, C. (2006) Sea cucumber biology: taxonomy; distribution; biology; conservation status. In Bruckner, A.W. (ed.) Proceedings of the CITES workshop on the conservation of sea cucumbers in the families Holothuriidae and Stichopodidae. NOAA Technical Memorandum NMFSOPR 34. Silver Spring, MD: National Oceanic and Atmospheric Administration, p. 33.Google Scholar
Cronin, T.W. (1986) Photoreception in marine invertebrates. American Zoologist 26, 403–415.Google Scholar
Cui, F.X., Xue, C.H., Li, Z.J., Zhang, Y.Q., Dong, P., Fu, X.Y. and Gao, X. (2007) Characterization and subunit composition of collagen from the body wall of sea cucumber Stichopus japonicus. Food Chemistry 100, 1120–1125.Google Scholar
Dance, S.K., Lane, I. and Bell, J.D. (2003) Variation in short-term survival of cultured sandfish (Holothuria scabra) released in mangrove-seagrass and coral reef flat habitats in Solomon Islands. Aquaculture 220, 495–505.Google Scholar
Dong, G., Dong, S., Wang, F. and Tian, X. (2010) Effects of light intensity on daily activity rhythm of juvenile sea cucumber, Apostichopus japonicus (Selenka). Aquaculture Research 41, 1640–1647.Google Scholar
Edullantes, C. (2015) Reproductive ecology and larval development of the sea cucumber Stichopus cf. horrens. Master's thesis, University of the Philippines, Diliman, Philippines.Google Scholar
Eriksson, H., Friedman, K., Solofa, A. and Mulipola, A.T. (2007) A pilot study to investigate the survival of Stichopus horrens after viscera harvest in Samoa. SPC Bêche-de-mer Information Bulletin 26, 2–4.Google Scholar
Eriksson, H., Jamon, A. and Wickel, J. (2012) Observations on habitat utilization by the sea cucumber Stichopus chloronotus. SPC Bêche-de-mer Information Bulletin 32, 39–42.Google Scholar
Francour, P. (1997) Predation on holothurians: a literature review. Invertebrate Biology 1, 52–60.Google Scholar
Friedman, K., Eriksson, H., Tardy, E. and Pakoa, K. (2010) Management of sea cucumber stocks: patterns of vulnerability and recovery of sea cucumber stocks impacted by fishing. Fish and Fisheries 12, 75–93.Google Scholar
Garrigue, C. (1998) Distribution and biomass of microphytes measured by benthic chlorophyll a in a tropical lagoon (New Caledonia, South Pacific). Hydrobiologia 385, 1–10.Google Scholar
Gutiérrez-García, A. (1999) Potential culture of sea cucumber in Mexico. SPC Bêche-de-mer Information Bulletin 11, 26–29.Google Scholar
Hamel, J.F. and Mercier, A. (1996) Early development, settlement, growth, and spatial distribution of the sea cucumber Cucumaria frondosa (Echinodermata: Holothuroidea). Canadian Journal of Fisheries and Aquatic Sciences 53, 253–271.Google Scholar
Hatanaka, H., Uwaoku, H. and Yasuda, T. (1994) Experimental studies on the predation of juvenile sea cucumber, Stichopus japonicus by sea star, Asterina pectinifera. Suisanzoshoku 42, 563–566 (in Japanese with English abstract).Google Scholar
Hendler, G. (1984) Brittlestar colour-change and phototaxis (Echinodermata: Ophiuroidea: Ophiocomidae). Marine Ecology 5, 379–401.Google Scholar
Hereu, B., Zabala, M., Linares, C. and Sala, E. (2005) The effects of predator abundance and habitat structural complexity on survival of juvenile sea urchins. Marine Biology 146, 293–299.Google Scholar
Hu, C., Li, H., Xia, J., Zhang, L., Luo, P., Fan, S., Peng, P., Yang, H. and Wen, J. (2013) Spawning, larval development and juvenile growth of the sea cucumber Stichopus horrens. Aquaculture 404, 47–54.Google Scholar
Hu, C., Xu, Y., Wen, J., Zhang, L., Fan, S. and Su, T. (2010) Larval development and juvenile growth of the sea cucumber Stichopus sp. (Curry fish). Aquaculture 300, 73–79.Google Scholar
Huntingford, F.A. (2004) Implications of domestication and rearing conditions for the behaviour of cultivated fishes. Journal of Fish Biology 65, 122–142.Google Scholar
Jackman, S. (2015) PSCL package: Political Science Computational Laboratory. Version 1.4. 8. Stanford, CA: Arq. Mus. Nac. Stanford University.Google Scholar
James, D.B. (2005) Information on juvenile holothurians. SPC Bêche-de-mer Information Bulletin 21, 26–27.Google Scholar
Jariashvili, K., Madhan, B., Brodsky, B., Kuchava, A., Namicheishvili, L. and Metreveli, N. (2012) UV damage of collagen: insights from model collagen peptides. Biopolymers 97, 189–198.Google Scholar
Johnsen, S. and Kier, W.M. (1999) Shade-seeking behaviour under polarized light by the brittlestar Ophioderma brevispinum (Echinodermata: Ophiuroidea). Journal of the Marine Biological Association of the United Kingdom 79, 761–763.Google Scholar
Kalinin, V.I., Aminin, D.L., Avilov, S.A., Silchenko, A.S. and Stonik, V.A. (2008) Triterpene glycosides from sea cucumbers (Holothurioidea, Echinodermata). Biological activities and functions. Studies in Natural Products Chemistry 35, 135–196.Google Scholar
Kiew, P.L. and Don, M.M. (2012) Jewel of the seabed: sea cucumbers as nutritional and drug candidates. International Journal of Food Sciences and Nutrition 63, 616–636.Google Scholar
Kronfeld-Schor, N., Bloch, G. and Schwartz, W.J. (2013) Animal clocks: when science meets nature. Proceedings of the Royal Society B 280, 1–4.Google Scholar
Lovatelli, A., Conand, C., Purcell, S., Uthicke, S., Hamel, J.F. and Mercier, A. (eds) (2004) Advances in sea cucumber aquaculture and management. Fisheries and Aquaculture Technical Paper No. 516. Rome: FAO, 425 pp.Google Scholar
Lürig, M.D., Best, R.J. and Stachowicz, J.J. (2016) Microhabitat partitioning in seagrass mesograzers is driven by consistent species choices across multiple predator and competitor contexts. Oikos 125, 1324–1333.Google Scholar
MacTavish, T., Stenton-Dozey, J., Vopel, K. and Savage, C. (2012) Deposit-feeding sea cucumbers enhance mineralization and nutrient cycling in organically-enriched coastal sediments. PLoS ONE 7, e50031.Google Scholar
Mercier, A., Battaglene, S.C. and Hamel, J.F. (1999) Daily burrowing cycle and feeding activity of juvenile sea cucumbers Holothuria scabra in response to environmental factors. Journal of Experimental Marine Biology and Ecology 239, 125–156.Google Scholar
Mercier, A., Battaglene, S.C. and Hamel, J.F. (2000a) Periodic movement, recruitment and size-related distribution of the sea cucumber Holothuria scabra in Solomon Islands. Hydrobiologia 440, 81–100.Google Scholar
Mercier, A., Battaglene, S.C. and Hamel, J.F. (2000b) Settlement preferences and early migration of the tropical sea cucumber Holothuria scabra. Journal of Experimental Marine Biology and Ecology 249, 89–110.Google Scholar
Mercier, A. and Hamel, J.F. (2013) Sea cucumber aquaculture: hatchery production, juvenile growth and industry challenges. In Allan, G. and Burnell, G. (eds) Advances in aquaculture hatchery technology. Cambridge: Woodhead Publishing, pp. 431–454.Google Scholar
Miles, C.A., Sionkowska, A., Hulin, S.L., Sims, T.J., Avery, N.C. and Bailey, A.J. (2000) Identification of an intermediate state in the helix-coil degradation of collagen by ultraviolet light. Journal of Biological Chemistry 275, 33014–33020.Google Scholar
Millott, N. (1955) The covering reaction in a tropical sea urchin. Nature 175, 561.Google Scholar
Moriarty, D.J.W., Roberts, D.G. and Pollard, P.C. (1990) Primary and bacterial productivity of tropical seagrass communities in the Gulf of Carpentaria, Australia. Marine Ecology Progress Series 61, 145–157.Google Scholar
Palomar-Abesamis, N., Abesamis, R.A. and Juinio-Meñez, M.A. (2017) Distribution and microhabitat associations of the juveniles of a high-value sea cucumber, Stichopus cf. horrens, in northern Philippines. Aquatic Ecology 51, 17–31.Google Scholar
Purcell, S.W. (2014) Value, market preferences and trade of bêche-de-mer from Pacific Island sea cucumbers. PLoS ONE 9, e95075.Google Scholar
Purcell, S.W., Choo, P.S., Akamine, J. and Fabinyi, M. (2014) Alternative product forms, consumer packaging and extracted derivatives of tropical sea cucumbers. SPC Bêche-de-mer Information Bulletin 34, 47–52.Google Scholar
Purcell, S.W., Conand, C., Uthicke, S. and Byrne, M. (2016) Ecological roles of exploited sea cucumbers. Oceanography and Marine Biology: an Annual Review 54, 367–386.Google Scholar
Purcell, S.W., Hair, C.A. and Mills, D.J. (2012a) Sea cucumber culture, farming and sea ranching in the tropics: progress, problems and opportunities. Aquaculture 368, 68–81.Google Scholar
Purcell, S.W., Samyn, Y. and Conand, C. (2012b) Commercially important sea cucumbers of the world. FAO Species Catalogue for Fishery Purposes. No. 6. Rome: FAO, 150 pp.Google Scholar
R Core Team (2013) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Available at http://www.R-project.org/.Google Scholar
Sewell, M.A. (1990) Aspects of the ecology of Stichopus mollis (Echinodermata: Holothuroidea) in north-eastern New Zealand. New Zealand Journal of Marine and Freshwater Research 24, 97–103.Google Scholar
Sharma, S., Coombs, S., Patton, P. and de Perera, T.B. (2009) The function of wall-following behaviors in the Mexican blind cavefish and a sighted relative, the Mexican tetra (Astyanax). Journal of Comparative Physiology A 195, 225–240.Google Scholar
Shiell, G. (2004) Field observations of juvenile sea cucumbers. SPC Bêche-de-mer Information Bulletin 20, 6–11.Google Scholar
Slater, M.J. (2006) Polyculture of the sea cucumber Stichopus mollis with green-lipped mussels. Master's thesis, University of Auckland, Auckland, New Zealand.Google Scholar
Slater, M.J. (2009) The sea cucumber Australostichopus mollis: juvenile feeding ecology and habitat. PhD thesis, University of Auckland, Auckland, New Zealand.Google Scholar
Slater, M.J., Carton, A.G. and Jeffs, A.G. (2010) Highly localised distribution patterns of juvenile sea cucumber Australostichopus mollis. New Zealand Journal of Marine and Freshwater Research 44, 201–216.Google Scholar
Sun, J., Zhang, L., Pan, Y., Lin, C., Wang, F., Kan, R. and Yang, H. (2015) Feeding behavior and digestive physiology in sea cucumber Apostichopus japonicus. Physiology and Behavior 139, 336–343.Google Scholar
Tanaka, M. (2000) Diminution of sea cucumber Stichopus japonicus juveniles released on artificial reefs. Bulletin of the Ishikawa Prefecture Fisheries Research Center 2, 19–29.Google Scholar
Trono, G.C. Jr and Lluisma, A.O. (1990) Seasonality of standing crop of a Sargassum (Fucales, Phaeophyta) bed in Bolinao, Pangasinan, Philippines. In Lindstrom, S.C. and Gabrielson, P.W. (eds) Proceedings of the Thirteenth International Seaweed Symposium, 13–18 August 1989. Dordrecht: Springer, pp. 331–338.Google Scholar
Wiedemeyer, W.L. (1994) Biology of small juveniles of the tropical holothurian Actinopyga echinites: growth, mortality, and habitat preferences. Marine Biology 120, 81–93.Google Scholar
Wolken, J.J. (1988) Photobehavior of marine invertebrates: extraocular photoreception. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology 91, 145–149.Google Scholar
Wolkenhauer, S.M., Uthicke, S., Burridge, C., Skewes, T. and Pitcher, R. (2010) The ecological role of Holothuria scabra (Echinodermata: Holothuroidea) within subtropical seagrass beds. Journal of the Marine Biological Association of the United Kingdom 90, 215–223.Google Scholar
Yamamoto, M. and Yoshida, M. (1978) Fine structure of the ocelli of a synaptid holothurian, Opheodesoma spectabilis, and the effects of light and darkness. Zoomorphology 90, 1–17.Google Scholar
Yamana, Y., Hamano, T. and Goshima, S. (2009) Laboratory observations of habitat selection in aestivating and active adult sea cucumber Apostichopus japonicus. Fisheries Science 75, 1097–1102.Google Scholar
Yamana, Y., Hamano, T. and Goshima, S. (2010) Natural growth of juveniles of the sea cucumber Apostichopus japonicus: studying juveniles in the intertidal habitat in Hirao Bay, eastern Yamaguchi Prefecture, Japan. Fisheries Science 76, 585–593.Google Scholar
Yamana, Y., Hamano, T. and Miki, K. (2006) Distribution of the Japanese sea cucumber Apostichopus japonicus in the intertidal zone of Hirao Bay, eastern Yamaguchi Prefecture, Japan: suitable environmental factors for juvenile habitats. Journal of National Fisheries University (Japan) 54, 111–120. [In Japanese with English abstract]Google Scholar
Zaidnuddin, I. (2009) Observation of the first grow out activities with Stichopus horrens juveniles in Malaysia. SPC Bêche-de-mer Information Bulletin 29, 48.Google Scholar
Zar, J.H. (1998) Biostatistical analysis, 4th edition. Upper Saddle River, NJ: Prentice Hall.Google Scholar
Zeileis, A., Kleiber, C. and Jackman, S. (2008) Regression models for count data in R. Journal of Statistical Software 27, 1–25.Google Scholar
Zeilinger, A.R., Olson, D.M. and Andow, D.A. (2014) A likelihood-based biostatistical model for analyzing consumer movement in simultaneous choice experiments. Environmental Entomology 43, 977–988.Google Scholar
Zhong, M., Chen, T., Hu, C. and Ren, C. (2015) Isolation and characterization of collagen from the body wall of sea cucumber Stichopus monotuberculatus. Journal of Food Science 80, C671–C679.Google Scholar