Marine Biology

, Volume 152, Issue 2, pp 297–305 | Cite as

Diel cycles of activity, metabolism, and ammonium concentration in tropical holothurians

  • Robert J. Wheeling
  • E. Alan Verde
  • James R. NestlerEmail author
Research Article


Movement rate, oxygen consumption, and respiratory tree ammonium concentration were measured in situ in the holothurians Pearsonothuria graeffei and Holothuria edulis in the Agan-an Marine Reserve, Sibulan, Philippines (9°20′30″N, 123°18′31″E). Measurements were made both day and night for both species during April–July 2005. P. graeffei had significantly higher movement rate during the day than at night (1.14 and 0.27 m h−1, respectively; three-way ANOVA, P < 0.05) while H. edulis had higher movement rate at night compared to the day (0.83 and 0.07 m h−1, respectively), spending the daylight hours sheltering under coral. More than 80% of H. edulis had movement rate of zero during the day. Oxygen consumption of P. graeffei was significantly higher during the day than at night (1.61 and 0.83 μmol O2 g−1 h−1, respectively; two-way ANCOVA, P < 0.05), but the reduction at night was not as pronounced as the reduction in movement. H. edulis had a 75% reduction in oxygen consumption during the day compared to night (0.51 and 1.96 μmol O2 g−1 h−1, respectively), matching this species’ reduced movement rates during the day. Ammonium concentration in water withdrawn from the respiratory trees of P. graeffei during the day (12.0 μM) was three times higher than in respiratory tree water sampled at night (4.3 μM) and 15 times higher than ambient seawater (0.8 μM; three-way ANOVA, P < 0.05). Ammonium concentration in the respiratory tree water of H. edulis was six times higher at night (14.6 μM) than during the day (2.2 μM) and 16 times higher than that of ambient seawater (0.9 μM). Even though H. edulis and P. graeffei are found within the same coral reef environment, they may affect different substrates and reef organisms due to their different habitats and distinct but opposite diel cycles.


Ammonium Concentration Great Barrier Reef Movement Rate Oxygen Consumption Rate Ambient Seawater 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank the faculty and staff of the Silliman University Marine Laboratory, especially Hilconida Calumpong, for their assistance in the field and laboratory. We also thank the mayor, city council, and Bantay Dagat of Sibulan for permission to use their marine reserve for this research. Kara Cromwell, Robin Dennison, and Andrea Wolffing provided invaluable assistance in data collection. The manuscript greatly benefitted from the comments of three anonymous reviewers. Funding was provided by the Walla Walla University faculty grants program and a grant from the Project AWARE Foundation.


  1. Amon RMW, Herndl GJ (1991) Deposit feeding and sediment: I. Interrelationships between Holothuria tubulosa (Holothurioidea, Echinodermata) and the sediment microbial community. Mar Ecol 12:163–174CrossRefGoogle Scholar
  2. Barnes DKA, Crook AC (2001) Quantifying behavioural determinants of the coastal European sea-urchin Paracentrotus lividus. Mar Biol 138:1205–1212CrossRefGoogle Scholar
  3. Bennington CC, Thayne WV (1994) Use and misuse of mixed model analysis of variance in ecological studies. Ecology 75:717–722CrossRefGoogle Scholar
  4. Birkeland C (1988) The influence of echinoderms on coral-reef communities. Echin Stud 3:1–79Google Scholar
  5. Blevins E, Johnsen S (2004) Spatial vision in the echinoid genus Echinometra. J Exp Biol 207:4249–4253CrossRefGoogle Scholar
  6. Chen G, Lockhart RA, Stephens MA (2002) Box–Cox transformations in linear models: large sample theory and tests of normality. Can J Stat 30:177–234CrossRefGoogle Scholar
  7. Clark AM, Rowe FWE (1971) Monograph of shallow water Indo-West Pacific echinoderms. Trustees of the British Museum (Natural History), LondonGoogle Scholar
  8. Coulon P, Jangoux M (1993) Feeding rate and sediment reworking by the holothuroid Holothuria tubulosa (Echinodermata) in a Mediterranean seagrass bed off Ischia island, Italy. Mar Ecol Prog Ser 92:201–204CrossRefGoogle Scholar
  9. Crozier WJ (1914) The orientation of a holothurian by light. Am J Physiol 36:8–20Google Scholar
  10. Da Silva J, Cameron JL, Fankboner PV (1986) Movement and orientation patterns in the commercial sea cucumber Parastichopus californicus (Stimpson) (Holothuroidea: Aspidochirotida). Mar Behav Physiol 12:133–147CrossRefGoogle Scholar
  11. Dance C (1987) Patterns of activity of the sea urchin Paracentrotus lividus in the bay of Port-Cros (Var, France, Mediterranean). Mar Ecol 8:131–142CrossRefGoogle Scholar
  12. Francour P (1997) Predation on holothurians: a literature review. Invert Biol 116:52–60CrossRefGoogle Scholar
  13. Fraser KPP, Peck LS, Clarke A (2004) Protein synthesis, RNA concentrations, nitrogen excretion, and metabolism vary seasonally in the Antarctic holothurian Heterocucumis steineni (Ludwig 1898). Physiol Biochem Zool 77:556–569CrossRefGoogle Scholar
  14. Graham JCH, Battaglene SC (2004) Periodic movement and sheltering behavior of Actinopyga mauritiana (Holothuroidea: Aspidochirotidae) in Solomon Islands. SPC Beche-de-mer Info Bull 19:23–31Google Scholar
  15. Grasshoff K, Kremling K (1999) Methods of seawater analysis. Wiley-VCH, WeinheimCrossRefGoogle Scholar
  16. Hamel J-F, Mercier A (1998) Diet and feeding behaviour of the sea cucumber Cucumaria frondosa in the St. Lawrence estuary, eastern Canada. Can J Zool 76:1194–1198CrossRefGoogle Scholar
  17. Hereu B (2005) Movement patterns of the sea urchin Paracentrotus lividus in a marine reserve and an unprotected area in the NW Mediterranean. Mar Ecol 26:54–62CrossRefGoogle Scholar
  18. Jangoux M (1982) Excretion. In: Jangoux M, Lawrence JM (eds) Echinoderm nutrition. Balkema, Rotterdam, pp 437–445Google Scholar
  19. Jangoux M, Lawrence JM (1982) Echinoderm nutrition. Balkema, RotterdamGoogle Scholar
  20. Kerr AM, Janies DA, Clouse RM, Samyn Y, Kuszak J, Kim J (2005) Molecular phylogeny of coral-reef sea cucumbers (Holothuriidae:Aspidochirotida) based on 16S mitochondrial ribosomal DNA sequence. Mar Biotech 7:53–60CrossRefGoogle Scholar
  21. Klinger TS, Johnson CR (1998) Spatial and temporal distribution of feeding of Aspirochirotida (Holothuroidea) on Heron Island, Great Barrier Reef. In: Mooi R, Telford M (eds) Echinoderms: San Francisco. Proceedings of 9th international echinoderm conference, Balkema, Rotterdam, pp 467–471Google Scholar
  22. Laboy-Nieves EN, Conde JE (2006) A new approach for measuring Holothuria mexicana and Isostichopus badionotus for stock assessments. SPC Beche-de-mer Info Bull 24:39–44Google Scholar
  23. Levy O, Mizrahi L, Chadwick-Furman NE, Achituv Y (2001) Factors controlling the expansion behavior of Favia favus (Cnidaria: Scleractinia): effects of light, flow, and planktonic prey. Biol Bull 200:118–126CrossRefGoogle Scholar
  24. Mercier A, Battaglene SC, Hamel J-F (1999) Daily burrowing cycle and feeding activity of juvenile sea cucumbers Holothuria scabra in response to environmental factors. J Exp Mar Biol Ecol 239:125–156CrossRefGoogle Scholar
  25. Mercier A, Battaglene SC, Hamel J-F (2000) Period movement, recruitment and size-related distribution of the sea cucumber Holothuria scabra in Solomon Islands. Hydrobiol 44:81–100CrossRefGoogle Scholar
  26. Meyer JL, Schultz ET (1985) Tissue condition and growth rates of corals associated with schooling fish. Limnol Oceanogr 30:157–166CrossRefGoogle Scholar
  27. Meyer JL, Schultz ET, Helfman GS (1983) Fish schools: an asset to corals. Science 220:1047–1049CrossRefGoogle Scholar
  28. Samyn Y (2000) Conservation of aspidochirotid holothurians in the littoral waters of Kenya. SPC Beche-de-mer Info Bull 13:12–17Google Scholar
  29. Samyn Y, Appeltans W, Kerr AM (2005) Phylogeny of Labidodemas and the Holothuriidae (Holothuroidea: Aspidochirotida) as inferred from morphology. Zool J Linn Soc 144:103–120CrossRefGoogle Scholar
  30. Sewell MA, Tyler PA, Young CM, Conand C (1997) Ovarian development in the class Holothuroidea: a reassessment of the “Tubule Recruitment Model”. Biol Bull 192:17–26CrossRefGoogle Scholar
  31. Shick JM, Dunlap WC (2002) Mycosporine-like amino acids and related gadulsols: biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu Rev Physiol 64:223–262CrossRefGoogle Scholar
  32. Shick JM, Dunlap WC, Chalker BE, Banaszak AT, Rosenzweig TK (1992) Survey of ultraviolet radiation-absorbing mycosporine-like amino acids in organs of coral reef holothuroids. Mar Ecol Prog Ser 90:139–148CrossRefGoogle Scholar
  33. Shiell GR (2006) Effect of invasive tagging on the activity of Holothuria whitmaei [Echinodermata: Holothuroidea]: a suitable mark-recapture method for short-term field studies of holothurian behavior. Mar Fresh Behav Physiol 39:153–162CrossRefGoogle Scholar
  34. Underwood AJ (1981) Techniques of analysis of variance in experimental marine biology and ecology. Oceanogr Mar Biol Ann Rev 19:513–603Google Scholar
  35. Uthicke S (2001a) Interactions between sediment-feeders and microalgae on coral reefs: grazing losses versus production enhancement. Mar Ecol Prog Ser 210:125–138CrossRefGoogle Scholar
  36. Uthicke S (2001b) Nutrient regeneration by abundant coral reef holothurians. J Exp Mar Biol Ecol 265:153–170CrossRefGoogle Scholar
  37. Uthicke S (1998) Respiration of Holothuria (Halodeima) atra, Holothuria (Halodeima) edulis and Stichopus choloronotus: Intact individuals and products of asexual reproduction. In: Mooi R, Telford M (eds) Echinoderms: San Francisco. Proceedings of 9th international echinoderm conference, Balkema, Rotterdam, pp531–536Google Scholar
  38. Uthicke S, Klumpp DW (1998) Microbenthos community production in sediments of a near shore coral reef: seasonal variation and response to ammonium recycled by holothurians. Mar Ecol Prog Ser 169:1–11CrossRefGoogle Scholar
  39. Webb KL, Du Paul WD, D’elia CF (1977) Biomass and nutrient flux measurements on Holothuria atra populations on windward reef flats at Enewetak, Marshall Islands. In: Taylor DL (ed) Proceedings of 3rd international coral reef symposium vol 1, biology. Rosenstiel school of marine and atmospheric science, Miami, pp 409– 415Google Scholar
  40. West GB, Brown JH (2005) The origin of allometric scaling laws in biology from genomes to ecosystems: towards a quantitative unifying theory of biological structure and organization. J Exp Biol 208:1575–1592CrossRefGoogle Scholar
  41. White AT (2001) Philippine coral reefs: a natural history guide, 2nd edn. Bookmark Inc and Sulu Fund for Marine Conservation Foundation Inc, ManilaGoogle Scholar
  42. Yamamoto M, Yoshida M (1978) Fine structure of the ocelli of a synaptid holothurian, Opheodesoma spectabilis, and the effects of light and darkness. Zoomorphology 90:1–17CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Robert J. Wheeling
    • 1
  • E. Alan Verde
    • 2
  • James R. Nestler
    • 1
    Email author
  1. 1.Department of BiologyWalla Walla UniversityCollege PlaceUSA
  2. 2.Corning School of Ocean StudiesMaine Maritime AcademyCastineUSA

Personalised recommendations