Aquatic Ecology

, Volume 51, Issue 1, pp 17–31 | Cite as

Distribution and microhabitat associations of the juveniles of a high-value sea cucumber, Stichopus cf. horrens, in northern Philippines

  • N. Palomar-Abesamis
  • R. A. Abesamis
  • M. A. Juinio-Meñez
Article

Abstract

There is considerable global interest in rebuilding depleted populations of sea cucumbers (Echinodermata, Holothuroidea) to address conservation and economic goals. For the vast majority of holothurian species, the habitat and food requirements of the juvenile stage are poorly understood. We investigated the distribution and microhabitat associations of juveniles of a commercially important sea cucumber, Stichopus cf. horrens, in the shallow, shoreward side of a coral reef (or backreef) in northern Philippines (16°21′38.7″N, 119°59′47.9″E). Relationships between juvenile density and the physical, chemical and biological characteristics of their habitat were examined. Potential food sources of the juveniles were also investigated using elemental and stable isotope analysis. Results showed that juveniles are more abundant in seagrass areas and the transition zone between seagrass and the rubble-dominated reef flat. A non-metric multidimensional scaling (MDS) plot indicated that juvenile density was most positively associated with coarser sand and rubble (>0.5 mm) and seagrass (Thalassia hemprichii) abundance (2D stress = 0.11). Juvenile density was also positively associated with sediment organic matter from plant detritus to a lesser extent. Elemental and isotope analysis of one site indicated that epiphytes were the primary food source of juveniles, while sediment detritus from microalgae and seagrass was a secondary food source. This study corroborates anecdotal evidence regarding the importance of seagrass to S. cf. horrens as potential refugia and source of high-quality food for its juveniles. These findings underscore the need to protect the nursery habitats of wild juveniles and provide critical information for the selection of suitable natural habitats for releasing cultured juveniles of this important species.

Keywords

Holothurian Seagrass Nursery Epiphyte Detritus Stable isotope 

Notes

Acknowledgments

This research was supported by grants to NPA from the Philippine Department of Science and Technology Accelerated Science and Technology Human Resource Development Program and the University of the Philippines Bolinao Marine Laboratory. We are grateful to the Silliman University Biology Department, Angelo King Center for Research and Environmental Management and the Institute of Environmental and Marine Sciences for the use of facilities, Allan Abuan, Renato Adolfo, Ronald de Guzman, Christine Edullantes and Minin Sinsona for assistance in the field and laboratory, Jasper Maypa for the map and Dr. Matthew J. Slater for scientific advice. We also thank the local government officials of Anda, Pangasinan for supporting this research.

Compliance with ethical standards

All procedures performed on animals were in accordance with Philippine laws (Republic Act 9147, Wildlife Act).

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Akamine J (2002) Trepang exploitation in the Philippines: updated information. SPC Bêche-de-mer Inf Bull 17:17–21. doi: 10.3759/tropics.10.591 Google Scholar
  2. Aminot A, Rey F (2000) Standard procedure for the determination of chlorophyll a by spectroscopic methods. ICES techniques in environmental sciences. International Council for the Exploration of the Sea (ICES), DenmarkGoogle Scholar
  3. Anderson SC, Flemming JM, Watson R, Lotze HK (2011) Serial exploitation of global sea cucumber fisheries. Fish Fish 12(3):317–339. doi: 10.1111/j.1467-2979.2010.00397.x CrossRefGoogle Scholar
  4. Battaglene SC (1999) Culture of tropical sea cucumbers for stock restoration and enhancement, Naga. ICLARM Q 22(4):4–11Google Scholar
  5. Battaglene SC, Seymour JE, Ramofafia C (1999) Survival and growth of cultured juvenile sea cucumbers Holothuria scabra. Aquaculture 178(3):293–322. doi: 10.1016/s0044-8486(99)00130-1 CrossRefGoogle Scholar
  6. Bell JD, Nash WJ (2004) When should restocking and stock enhancement be used to manage sea cucumber fisheries? In: Lovatelli A, Conand C, Purcell S, Uthicke S, Hamel JF, Mercier A (eds) Advances in sea cucumber aquaculture and management. FAO fisheries technical paper no. 463. United Nations Food and Agriculture Organisation, Rome, pp 173–80Google Scholar
  7. Bell JD, Purcell SW, Nash WJ (2008) Restoring small-scale fisheries for tropical sea cucumbers. Ocean Coast Manage 51(8):589–593. doi: 10.1016/j.ocecoaman.2008.06.011 CrossRefGoogle Scholar
  8. Bond AB (2007) The evolution of color polymorphism: crypticity, searching images, and apostatic selection. Annu Rev Ecol Evol Syst 38:489–514. doi: 10.1146/annurev.ecolsys.38.091206.095728 CrossRefGoogle Scholar
  9. Bordbar S, Anwar F, Saari N (2011) High-value components and bioactives from sea cucumbers for functional foods—a review. Mar Drugs 9(10):1761–1805. doi: 10.3390/md9101761 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Buchanan J (1984) Sediment analysis. In: Holme N, McIntyre A (eds) Methods for the study of marine benthos, 2nd edn. Blackwell Scientific Publications, Oxford, pp 41–65Google Scholar
  11. Bulteel P, Jangoux M, Coulon P (1992) Biometry, bathymetric distribution and reproductive cycle of the holothuroid Holothuria tubulosa (Echinodermata) from Mediterranean sea grass beds. PSZNI Mar Ecol 13(1):53–62. doi: 10.1111/j.1439-0485.1992.tb00339.x CrossRefGoogle Scholar
  12. Byrne M, Rowe F, Uthicke S (2010) Molecular taxonomy, phylogeny and evolution in the family Stichopodidae (Aspidochirotida: Holothuroidea) based on COI and 16S mitochondrial DNA. Mol Phylogenet Evol 56(3):1068–1081. doi: 10.1016/j.ympev.2010.04.013 CrossRefPubMedGoogle Scholar
  13. Cameron JL, Fankboner PV (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. J Exp Mar Biol Ecol 127(1):43–67. doi: 10.1139/z86-027 CrossRefGoogle Scholar
  14. Cebrián J, Duarte CM (1998) Patterns in leaf herbivory on seagrasses. Aquat Bot 60(1):67–82. doi: 10.1016/s0304-3770(97)00070-3 CrossRefGoogle Scholar
  15. Chiu SH, Huang YH, Lin HJ (2013) Carbon budget of leaves of the tropical intertidal seagrass Thalassia hemprichii. Estuar Coast Shelf Sci 125:27–35. doi: 10.1016/j.ecss.2013.03.026 CrossRefGoogle Scholar
  16. Choo PS (2008) The Philippines: a hotspot of sea cucumber fisheries in Asia. In: Toral-Granda V, Lovatelli A, Vasconcellos M (eds) Sea cucumbers: a global review of fisheries and trade. FAO fisheries and aquaculture technical paper, vol 516, pp 119–140Google Scholar
  17. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E, PlymouthGoogle Scholar
  18. Conand C (1981) Sexual cycle of three commercially important holothurian species (Echinodermata) from the lagoon of New Caledonia. Bull Mar Sci 31(3):523–543Google Scholar
  19. Conand C (1993) Ecology and reproductive biology of Stichopus variegatus an Indo-Pacific coral reef sea cucumber (Echinodermata: Holothuroidea). Bull Mar Sci 52(3):970–981Google Scholar
  20. Cuthill IC, Stevens M, Sheppard J, Maddocks T, Párraga CA, Troscianko TS (2005) Disruptive coloration and background pattern matching. Nature 434:72–74. doi: 10.1038/nature03312 CrossRefPubMedGoogle Scholar
  21. Daehnick AE, Sullivan MJ, Moncreiff CA (1992) Primary production of the sand microflora in seagrass beds of Mississippi sound. Bot Mar 35(2):131–140. doi: 10.1515/botm.1992.35.2.131 CrossRefGoogle Scholar
  22. Dawes CJ, Lawrence JM (1980) Seasonal changes in the proximate constituents of the seagrasses Thalassia testudinum, Halodule wrightii and Syringodium filiforme. Aquat Bot 8:371–380. doi: 10.1016/0304-3770(80)90066-2 CrossRefGoogle Scholar
  23. Edullantes C (2015) Reproductive ecology and larval development of the sea cucumber Stichopus cf. horrens. Master thesis, University of the Philippines, DilimanGoogle Scholar
  24. Endler JA (1978) A predator’s view of animal color patterns. In: Hecht MK, Steere WC, Wallace B (eds) Evolutionary biology, vol 11. Plenum Press, New York, pp 319–364. doi: 10.1007/978-1-4615-6956-5_5 CrossRefGoogle Scholar
  25. Endler JA, Greenwood JD (1988) Frequency-dependent predation, crypsis and aposematic coloration [and discussion]. Philos Trans R Soc Biol Sci 319:505–523. doi: 10.1098/rstb.1988.0062 CrossRefGoogle Scholar
  26. Eriksson H, Friedman K, Solofa A, Mulipola AT (2007) A pilot study to investigate the survival of stichopus horrens after viscera harvest in Samoa. SPC Bêche-de-mer Information Bulletin 26:2–4Google Scholar
  27. Eriksson H, Jamon A, Wickel J (2012) Observations on habitat utilization by the sea cucumber Stichopus chloronotus. SPC Bêche-de-mer Inf Bull 32:39–42Google Scholar
  28. Eriksson H, Thorne BV, Byrne M (2013) Population metrics in protected commercial sea cucumber populations (curryfish: Stichopus herrmanni) on one tree reef, Great Barrier Reef. Mar Ecol Prog Ser 473:225–234. doi: 10.3354/meps10054 CrossRefGoogle Scholar
  29. Fourqurean JW, Willsie A, Rose CD, Rutten LM (2001) Spatial and temporal pattern in seagrass community composition and productivity in south Florida. Mar Biol 138(2):341–354. doi: 10.1007/s002270000448 CrossRefGoogle Scholar
  30. Friedman K, Eriksson H, Tardy E, Pakoa K (2010) Management of sea cucumber stocks: patterns of vulnerability and recovery of sea cucumber stocks impacted by fishing. Fish Fish 12(1):75–93. doi: 10.1111/j.1467-2979.2010.00384.x CrossRefGoogle Scholar
  31. Fry B (1984) 13C/12C ratios and the trophic importance of algae in florida Syringodium filiforme seagrass meadows. Mar Biol 79(1):11–19. doi: 10.1007/bf00404980 CrossRefGoogle Scholar
  32. Hamel JF, Mercier A (1996) Early development, settlement, growth, and spatial distribution of the sea cucumber Cucumaria frondosa (Echinodermata: Holothuroidea). Can J Fish Aquat Sci 53(2):253–271. doi: 10.1139/f95-186 CrossRefGoogle Scholar
  33. Hamel JF, Conand C, Pawson DL, Mercier A (2001) The sea cucumber Holothuria scabra (Holothuroidea: Echinodermata): its biology and exploitation as beche-de-mer. Adv Mar Biol 41:129–223. doi: 10.1016/s0065-2881(01)41003-0 CrossRefGoogle Scholar
  34. Hearn A, Pinillos F (2006) Baseline information on the warty sea cucumber Stichopus horrens in Santa Cruz, Galápagos, prior to the commencement of an illegal fishery. SPC Bêche-de-mer Inf Bull 24:3–10Google Scholar
  35. Heijs FM (1984) Annual biomass and production of epiphytes in three monospecific seagrass communities of Thalassia hemprichii (Ehrenb.) Aschers. Aquat Bot 20:195–218. doi: 10.1016/0304-3770(84)90087-1 CrossRefGoogle Scholar
  36. James DB (2005) Information on juvenile holothurians. SPC Bêche-de-mer Inf Bull 21:26–27Google Scholar
  37. Jaschinski S, Aberle N, Gohse-Reimann S, Brendelberger H, Wiltshire KH, Sommer U (2009) Grazer diversity effects in an eelgrass–epiphyte–microphytobenthos system. Oecologia 159(3):607–615. doi: 10.1007/s00442-008-1236-2 CrossRefPubMedGoogle Scholar
  38. Kennedy H, Beggins J, Duarte CM, Fourqurean JW, Holmer M, Marbà N, Middelburg JJ (2010) Seagrass sediments as a global carbon sink: isotopic constraints. Glob Biogeochem Cycles 24(4):1–8. doi: 10.1029/2010gb003848 CrossRefGoogle Scholar
  39. Kinch J (2012) Observation of juvenile Stichopus vastus in Pohnpei Lagoon, Federated States of Micronesia. SPC Bêche-de-mer Inf Bull 32:62Google Scholar
  40. Klumpp DW, Howard RK, Pollard DA (1989) Trophodynamics and nutritional ecology of seagrass communities. In: Larkum AWD, McComb AJ, Shepaherd SA (eds) Biology of seagrasses: a treatise on the biology of seagrasses with special reference to the Australian region. Elsevier, Amsterdam, pp 394–457Google Scholar
  41. Klumpp DW, Salita-Espinosa JS, Fortes MD (1992) The role of epiphytic periphyton and macroinvertebrate grazers in the trophic flux of a tropical seagrass community. Aquat Bot 43(4):327–349. doi: 10.1016/0304-3770(92)90046-l CrossRefGoogle Scholar
  42. Lepoint G, Nyssen F, Gobert S, Dauby P, Bouquegneau JM (2000) Relative impact of a seagrass bed and its adjacent epilithic algal community in consumer diets. Mar Biol 136(3):513–518. doi: 10.1007/s002270050711 CrossRefGoogle Scholar
  43. Lindeboom HJ, Sandee AJJ (1989) Production and consumption of tropical seagrass fields in eastern Indonesia measured with bell jars and microelectrodes. Neth J Sea Res 23(2):181–190. doi: 10.1016/0077-7579(89)90012-4 CrossRefGoogle Scholar
  44. Liu X, Zhou Y, Yang H, Ru S (2013) Eelgrass detritus as a food source for the sea cucumber Apostichopus japonicus Selenka (Echinidermata: Holothuroidea) in coastal waters of north China: an experimental study in flow-through systems. PLoS One 8(3):e58293. doi: 10.1371/journal.pone.0058293 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Lorenzen K, Leber KM, Blankenship HL (2010) Responsible approach to marine stock enhancement: an update. Rev Fish Sci 18(2): 189–210. doi: 10.1080/10641262.2010.491564 CrossRefGoogle Scholar
  46. Lovatelli A, Conand C (eds) (2004) Advances in sea cucumber aquaculture and management no. 463. FAO, RomeGoogle Scholar
  47. Mann KH (1988) Production and use of detritus in various freshwater, estuarine, and coastal marine ecosystems. Limnol Oceanogr 33:910–930. doi: 10.4319/lo.1988.33.4_part_2.0910 Google Scholar
  48. Mercier A, Battaglene SC, Hamel JF (1999) Daily burrowing cycle and feeding activity of juvenile sea cucumbers Holothuria scabra in response to environmental factors. J Exp Mar Biol Ecol 239(1):125–156. doi: 10.1016/s0022-0981(99)00034-9 CrossRefGoogle Scholar
  49. Mercier A, Battaglene SC, Hamel JF (2000a) Periodic movement, recruitment and size-related distribution of the sea cucumber Holothuria scabra in Solomon Islands. Hydrobiologia 440:81–100. doi: 10.1007/978-94-017-1982-7_8 CrossRefGoogle Scholar
  50. Mercier A, Battaglene SC, Hamel JF (2000b) Settlement preferences and early migration of the tropical sea cucumber Holothuria scabra. J Exp Mar Biol Ecol 249(1):89–110. doi: 10.1016/s0022-0981(00)00187-8 CrossRefPubMedGoogle Scholar
  51. Merilaita S (2003) Visual background complexity facilitates the evolution of camouflage. Evolution 57(6):1248–1254. doi: 10.1554/03-011 CrossRefPubMedGoogle Scholar
  52. Merilaita S, Tuomi J, Jormalainen V (1999) Optimization of cryptic coloration in heterogeneous habitats. Biol J Linn Soc 67(2):151–161. doi: 10.1111/j.1095-8312.1999.tb01858.x CrossRefGoogle Scholar
  53. Merilaita S, Lyytinen A, Mappes J (2001) Selection for cryptic coloration in a visually heterogeneous habitat. Proc R Soc Lond B Biol 268:1925–1929. doi: 10.1098/rspb.2001.1747 CrossRefGoogle Scholar
  54. Michio K, Kengo K, Yasunori K, Hitoshi M, Takayuki Y, Hideaki Y, Hiroshi S (2003) Effects of deposit feeder Stichopus japonicus on algal bloom and organic matter contents of bottom sediments of the enclosed sea. Mar Poll Bull 47(1):118–125. doi: 10.1016/s0025-326x(02)00411-3 CrossRefGoogle Scholar
  55. Miyajima T, Suzumura M, Umezawa Y, Koike I (2001) Microbiological nitrogen transformation in carbonate sediments of a coral-reef lagoon and associated seagrass beds. Mar Ecol Prog Ser 217:273–286. doi: 10.3354/meps217273 CrossRefGoogle Scholar
  56. Moncreiff CA, Sullivan MJ, Daehnick AE (1992) Primary production dynamics in seagrass beds of Mississippi Sound: the contributions of seagrass epiphytic algae, sand microflora, and phytoplankton. Mar Ecol Prog Ser 87(1):161–171. doi: 10.3354/meps087161 CrossRefGoogle Scholar
  57. Moriarty DJW (1982) Feeding of Holothuria atra and Stichopus chloronotus on bacteria, organic carbon and organic nitrogen in sediments of the Great Barrier Reef. Mar Freshw Res 33(2):255–263. doi: 10.1071/mf9820255 CrossRefGoogle Scholar
  58. Purcell SW (2012) Principles and science of stocking marine areas with sea cucumbers. In: Hair CA, Pickering TD, Mills DJ (eds) Asia–Pacific tropical sea cucumber aquaculture, ACIAR proceedings no. 136. Australian Centre for International Agricultural Research, Canberra, pp 92–103Google Scholar
  59. Purcell SW (2014) Value, market preferences and trade of beche-de-mer from Pacific Island sea cucumbers. PLoS One. doi: 10.1371/journal.pone.0095075 Google Scholar
  60. Purcell SW, Samyn Y, Conand C (2012a) Commercially important sea cucumbers of the world. FAO, RomeGoogle Scholar
  61. Purcell SW, Hair CA, Mills DJ (2012b) Sea cucumber culture, farming and sea ranching in the tropics: progress, problems and opportunities. Aquaculture 368:68–81. doi: 10.1016/j.aquaculture.2012.08.053 CrossRefGoogle Scholar
  62. Purcell SW, Mercier A, Conand C, Hamel JF, Toral-Granda MV, Lovatelli A, Uthicke S (2013) Sea cucumber fisheries: global analysis of stocks, management measures and drivers of overfishing. Fish Fish 14(1):34–59. doi: 10.1111/j.1467-2979.2011.00443.x CrossRefGoogle Scholar
  63. Purcell SW, Choo PS, Akamine J, Fabinyi M (2014) Alternative product forms, consumer packaging and extracted derivatives of tropical sea cucumbers. SPC Bêche-de-mer Inf Bull 34:47–52Google Scholar
  64. Ramofafia C, Foyle TP, Bell JD (1997) Growth of juvenile Actinopyga mauritiana (Holothuroidea) in captivity. Aquaculture 152(1):119–128. doi: 10.1016/s0044-8486(96)01525-6 CrossRefGoogle Scholar
  65. Reichenbach N (1999) Ecology and fishery biology of Holothuria fuscogilva (Echinodermata: Holothuroidea) in the Maldives, Indian Ocean. Bull Mar Sci 64(1):103–114Google Scholar
  66. Roberts D, Gebruk A, Levin V, Manship BAD (2000) Feeding and digestive strategies in deposit-feeding holothurians: Oceanogr Mar Biol Annu Rev 38:257–310Google Scholar
  67. Segal B, Castro CB (2001) A proposed method for coral cover assessment: a case study in Abrolhos, Brazil. Bull Mar Sci 69(2):487–496Google Scholar
  68. Shiell G (2004) Field observations of juvenile sea cucumbers. SPC Bêche-de-mer Inf Bull 20:6–11Google Scholar
  69. Slater MJ, Jeffs AG (2010) Do benthic sediment characteristics explain the distribution of juveniles of the deposit-feeding sea cucumber Australostichopus mollis? J Sea Res 64(3):241–249. doi: 10.1016/j.seares.2010.03.005 CrossRefGoogle Scholar
  70. Slater MJ, Carton AG, Jeffs AG (2010) Highly localised distribution patterns of juvenile sea cucumber Australostichopus mollis. N Z J Mar Freshw 44(4):201–216. doi: 10.1080/00288330.2010.504526 CrossRefGoogle Scholar
  71. Slater MJ, Jeffs AG, Sewell MA (2011) Organically selective movement and deposit-feeding in juvenile sea cucumber Australostichopus mollis determined in situ and in the laboratory. J Exp Mar Biol Ecol 409(1):315–323. doi: 10.1016/j.jembe.2011.09.010 CrossRefGoogle Scholar
  72. Sloan NA, Von Bodungen B (1980) Distribution and feeding of the sea cucumber Isostichopus badionotus in relation to shelter and sediment criteria of the Bermuda platform. Mar Ecol Prog Ser 2:257–264. doi: 10.3354/meps002257 CrossRefGoogle Scholar
  73. Southward AJ, Young CM, Fuiman LA (2005) Restocking initiatives. Adv Mar Biol 49:9–41. doi: 10.1016/s0065-2881(05)49002-1 CrossRefGoogle Scholar
  74. Todd PA, Briers RA, Ladle RJ, Middleton F (2006) Phenotype-environment matching in the shore crab (Carcinus maenas). Mar Biol 148(6):1357–1367. doi: 10.1007/s00227-005-0159-2 CrossRefGoogle Scholar
  75. Toral-Granda MV, Martínez PC (2007) Reproductive biology and population structure of the sea cucumber Isostichopus fuscus (Ludwig, 1875) (Holothuroidea) in Caamaño, Galápagos Islands, Ecuador. Mar Biol 151(6):2091–2098. doi: 10.1007/s00227-007-0640-1 CrossRefGoogle Scholar
  76. Toral-Granda V, Lovatelli A, Vasconcellos M (eds) (2008) Sea cucumbers: a global review of fisheries and trade. FAO, RomeGoogle Scholar
  77. Uthicke S (1999) Sediment bioturbation and impact of feeding activity of Holothuria (Halodeima) atra and Stichopus chloronotus, two sediment feeding holothurians, at Lizard Island, Great Barrier Reef. Bull Mar Sci 64(1):129–141Google Scholar
  78. Uthicke S, Karez R (1999) Sediment patch selectivity in tropical sea cucumbers (Holothurioidea: Aspidochirotida) analysed with multiple choice experiments. J Exp Mar Biol Ecol 236(1):69–87. doi: 10.1016/s0022-0981(98)00190-7 CrossRefGoogle Scholar
  79. Van Tussenbroek BI, Vonk JA, Stapel J, Erftemeijer PL, Middelburg JJ, Zieman JC (2007) The biology of Thalassia: paradigms and recent advances in research. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Berlin, pp 409–439. doi: 10.1007/978-1-4020-2983-7_18 Google Scholar
  80. Vonk JA, Christianen MJ, Stapel J (2008) Redefining the trophic importance of seagrasses for fauna in tropical Indo-Pacific meadows. Estuar Coast Shelf Sci 79(4):653–660. doi: 10.1016/j.ecss.2008.06.002 CrossRefGoogle Scholar
  81. Wiedemeyer WL (1994) Biology of small juveniles of the tropical holothurian Actinopyga echinites: growth, mortality, and habitat preferences. Mar Biol 120(1):81–93Google Scholar
  82. Yamana Y, Hamano T, Miki K (2006) Distribution of the Japanese sea cucumber Apostichopus japonicus in the intertidal zone of Hirao Bay, Eastern Yamaguchi Pref., Japan: suitable environmental factors for juvenile habitats. J Natl Fish Univ (Japan) 54(3):111–120Google Scholar
  83. Yamana Y, Hamano T, 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. Fish Sci 76(4):585–593. doi: 10.1007/s12562-010-0245-3 CrossRefGoogle Scholar
  84. Yingst JY (1976) The utilization of organic matter in shallow marine sediments by an epibenthic deposit-feeding holothurian. J Exp Mar Biol Ecol 23(1):55–69. doi: 10.1016/0022-0981(76)90085-x CrossRefGoogle Scholar
  85. Zaidnuddin I (2009) Observation of the first grow out activities with Stichopus horrens juveniles in Malaysia. SPC Bêche-de-mer Inf Bull 29:48Google Scholar
  86. Zamora LN, Jeffs AG (2011) Feeding, selection, digestion and absorption of the organic matter from mussel waste by juveniles of the deposit-feeding sea cucumber, Australostichopus mollis. Aquaculture 317(1):223–228. doi: 10.1016/j.aquaculture.2011.04.011 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • N. Palomar-Abesamis
    • 1
    • 2
  • R. A. Abesamis
    • 3
    • 4
  • M. A. Juinio-Meñez
    • 1
  1. 1.The Marine Science InstituteUniversity of the PhilippinesQuezon CityPhilippines
  2. 2.Biology DepartmentSilliman UniversityDumaguete CityPhilippines
  3. 3.College of Marine and Environmental ScienceJames Cook UniversityTownsvilleAustralia
  4. 4.Silliman University - Angelo King Center for Research and Environmental Management (SUAKCREM)Dumaguete CityPhilippines

Personalised recommendations