Abstract
Ecology of many sea cucumbers, including the world’s heaviest holothuroid Thelenota anax, remains understudied, hindering effective fisheries management and conservation. We located, measured and weighed 38 T. anax over 10 days at Lizard Island, northeast Australia. Body length alone was a suitable predictor of body weight for this species. Short-term (1–4 h) rates of displacement and sediment defecation were measured on 30 animals across three sites. The animals were highly mobile, moving, on average, 57 cm h−1 (± 11 SE), and reworking 34 g dry weight of sediment h−1 (± 7 SE). The animals moved more and defecated more sediments in areas where surrounding sediments had lower levels of organic matter. Defecation rates increased through daytime hours. The high mobility of T. anax should confer an advantage for mate-finding but also could increase spillover from small marine reserves into fishing grounds. Our findings galvanise a pattern of high mobility in larger holothuroids and show that food resources and time of day modulate the extent of sediment reworking by deposit feeding holothuroids. The high sediment turnover rate highlights the detrimental effect that overfishing of these large holothuroids will have on the health of coastal marine ecosystems.





Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
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
Bell JD, Purcell SW, Nash WJ (2008) Restoring small-scale fisheries for tropical sea cucumbers. Ocean Coast Manage 51:589–593
Buxton CD, Hartmann K, Kearney R, Gardner C (2014) When is spillover from marine reserves likely to benefit fisheries? PLoS ONE 9:e107032
Choo PS (2008) Population status, fisheries and trade of sea cucumbers 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, Rome, pp 81–118
Conand C (1989) Les Holothuries Aspidochirotes du Lagon de Nouvelle-Calédonie: Biologie, Écologie et Exploitation. ORSTOM, Noumea
Conand C, Polidoro B, Mercier A, Gamboa R, Hamel J-F, Purcell S (2014) The IUCN Red List assessment of aspidochirotid sea cucumbers and its implications. SPC Beche-de-mer Inf Bull 34:3–7
Conand C, Purcell S, Gamboa R (2013) Thelenota anax. The IUCN Red List of Threatened Species 2013. www.iucnredlist.org/species/180324/1615023. Accessed 18 Nov 2019
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 92:201–204
Dissanayake D, Athukorala S, Amarasiri C (2010) Present status of the sea cucumber fishery in Sri Lanka. SPC Beche-de-mer Inf Bull 30:14–20
Dissanayake D, Stefansson G (2010) Abundance and distribution of commercial sea cucumber species in the coastal waters of Sri Lanka. Aquat Living Resour 23:303–313
Dissanayake D, Stefansson G (2012) Present status of the commercial sea cucumber fishery off the north-west and east coasts of Sri Lanka. J Mar Biol Assoc UK 92:831–841
Friedman K, Eriksson H, Tardy E, Pakoa K (2011) Management of sea cucumber stocks: Patterns of vulnerability and recovery of sea cucumber stocks impacted by fishing. Fish Fish 12:75–93
Friedman K, Pinca S, Boblin P, Magron F, Vunisea A, Labrosse P, Chapman L, Kronen M (2009) Tonga country report: profiles and results from survey work at Ha’atafu, Manuka, Koulo and Lofanga (November and December 2001; March–June 2002; April–June, September and October 2008). Pacific Regional Oceanic and Coastal Fisheries Development Programme (PROCFish/C/CoFish). SPC, Noumea
Froese R (2006) Cube law, condition factor and weight–length relationships: history, meta-analysis and recommendations. J Appl Ichthyol 22:241–253
Graham JC, Battaglene SC (2004) Periodic movement and sheltering behaviour of Actinopyga mauritiana (Holothuroidea: Aspidochirotidae) in Solomon Islands. SPC Beche-de-mer Inf Bull 19:23–31
Hammond LS (1982) Patterns of feeding and activity in deposit-feeding holothurians and echinoids (Echinodermata) from a shallow back-reef lagoon, Discovery Bay, Jamaica. Bull Mar Sci 32:549–571
Hastings A, Botsford LW (2003) Comparing designs of marine reserves for fisheries and for biodiversity. Ecol Appl 13:65–70
Hopf JK, Jones GP, Williamson DH, Connolly SR (2016) Synergistic effects of marine reserves and harvest controls on the abundance and catch dynamics of a coral reef fishery. Curr Biol 26:1543–1548
Jupiter S, Saladrau W, Vave R (2013) Assessment of sea cucumber fisheries through targeted surveys of Lau Province, Fiji. Wildlife Conservation Society/University of the South Pacific/Fiji Department of Fisheries/Khaled bin Sultan Living Oceans Foundation, Suva, p 22
Karachle PK, Stergiou KI (2012) Morphometrics and allometry in fishes. In: Wahl C (ed) Morphometrics. IntechOpen, Rijeka, pp 65–86
Kerwath SE, Winker H, Götz A, Attwood CG (2013) Marine protected area improves yield without disadvantaging fishers. Nat Commun 4:2347
Khan A (2017) Adapt: How We Can Learn From Nature's Strangest Inventions. Atlantic Books, Great Britain
Kinch J, Purcell S, Uthicke S, Friedman K (2008) Population status, fisheries and trade of sea cucumbers in the Western Central Pacific. In: Toral-Granda V, Lovatelli A, Vasconcellos M (eds) Sea Cucumbers: A Global Review of Fisheries and Trade. FAO Fisheries and Aquaculture Technical Paper No 516. FAO, Rome, pp 7–55
Lane DJ, Limbong D (2015) Catastrophic depletion of reef-associated sea cucumbers: resource management/reef resilience issues for an Indonesian marine park and the wider Indo-Pacific. Aquatic Conserv: Mar Freshw Ecosyst 25:505–517
Lee S, Ford AK, Mangubhai S, Wild C, Ferse SC (2018) Effects of sandfish (Holothuria scabra) removal on shallow-water sediments in Fiji. PeerJ 6:e4773
Marquet N, Hubbard PC, da Silva JP, Afonso J, Canário AV (2018) Chemicals released by male sea cucumber mediate aggregation and spawning behaviours. Sci Rep 8:239
Massin C (1982) Food and feeding mechanism: Holothuroidea. In: Jangoux M, Lawrence J (eds) Echinoderm Nutrition. AA Balkema, Rotterdam, pp 43–55
Maye A, Hsieh C-h, Sugihara G, Brembs B (2007) Order in spontaneous behavior. PLoS ONE 2:e443
Muthiga N, Ochiewo J, Kawaka J (2007) Sea cucumbers in Kenya. In: Conand C, Muthiga N (eds) Commercial Sea Cucumbers: A Review for the Western Indian Ocean. WIOMSA, Zanzibar, pp 8–20
Navarro P, García-Sanz S, Barrio J, Tuya F (2013) Feeding and movement patterns of the sea cucumber Holothuria sanctori. Mar Biol 160:2957–2966
Pakoa K, Saladrau W, Lalavanua W, Valotu D, Tuinasavusavu I, Sharp M, Bertram I (2013) Status of Sea Cucumber Resources and Fisheries Management in Fiji. SPC, Noumea
Pinca S, Kronen M, Friedman K, Magron F, Chapman L, Tardy E, Pakoa K, Awira R, Boblin P, Lasi F (2010) Regional assessment report: profiles and results from survey work at 63 sites across 17 pacific island countries and territories. Secretariat of the Pacific Community, Noumea
Prescott J, Zhou S, Prasetyo AP (2015) Soft bodies make estimation hard: correlations among body dimensions and weights of multiple species of sea cucumbers. Mar Freshw Res 66:857–865
Purcell SW, Conand C, Uthicke S, Byrne M (2016a) Ecological roles of exploited sea cucumbers. Oceanogr Mar Biol 54:367–386
Purcell SW, Eriksson H (2015) Echinoderms piggybacking on sea cucumbers: benign effects on sediment turnover and movement of hosts. Mar Biol Res 11:666–670
Purcell SW, Gossuin H, Agudo NS (2009) Status and management of the sea cucumber fishery of La Grande Terre, New Caledonia. WorldFish Centre Studies and Reviews No. 1901. WorldFish Centre, Penang
Purcell SW, Kirby DS (2006) Restocking the sea cucumber Holothuria scabra: sizing no-take zones through individual-based movement modelling. Fish Res 80:53–61
Purcell SW (2010) Managing Sea Cucumber Fisheries with an Ecosystem Approach. FAO, Rome
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 14:34–59
Purcell SW, Piddocke TP, Dalton SJ, Wang Y-G (2016b) Movement and growth of the coral reef holothuroids Bohadschia argus and Thelenota ananas. Mar Ecol Prog Ser 551:201–214
Purcell SW, Samyn Y, Conand C (2012) Commercially Important Sea Cucumbers of the World. FAO, Rome
Purcell SW, Williamson DH, Ngaluafe P (2018) Chinese market prices of beche-de-mer: implications for fisheries and aquaculture. Mar Policy 91:58–65
Sala E, Giakoumi S (2017) No-take marine reserves are the most effective protected areas in the ocean. ICES J Mar Sci 75:1166–1168
Sale PF, Cowen RK, Danilowicz BS, Jones GP, Kritzer JP, Lindeman KC, Planes S, Polunin NV, Russ GR, Sadovy YJ (2005) Critical science gaps impede use of no-take fishery reserves. Trends Ecol Evol 20:74–80
Sani R, Gupta B, Sarkar U, Pandey A, Dubey V, Singh Lakra W (2010) Length–weight relationships of 14 Indian freshwater fish species from the Betwa (Yamuna River tributary) and Gomti (Ganga River tributary) rivers. J Appl Ichthyol 26:456–459
Schneider K, Silverman J, Woolsey E, Eriksson H, Byrne M, Caldeira K (2011) Potential influence of sea cucumbers on coral reef CaCO3 budget: a case study at One Tree Reef. J Geophys Res Biogeosci 116:G04032
Shiell GR, Knott B (2010) Aggregations and temporal changes in the activity and bioturbation contribution of the sea cucumber Holothuria whitmaei (Echinodermata: Holothuroidea). Mar Ecol Prog Ser 415:127–139
Siegenthaler A, Cánovas F, González-Wangüemert M (2015) Spatial distribution patterns and movements of Holothuria arguinensis in the Ria Formosa (Portugal). J Sea Res 102:33–40
Singh R, MacDonald BA, Thomas ML, Lawton P (1999) Patterns of seasonal and tidal feeding activity in the dendrochirote sea cucumber Cucumaria frondosa (Echinodermata: Holothuroidea) in the Bay of Fundy, Canada. Mar Ecol Prog Ser 187:133–145
Skewes T, Smith L, Dennis D, Rawlinson N, Donovan A, Ellis N (2004) Conversion Ratios for Commercial Beche-de-mer Species in Torres Strait. Australian Fisheries Management Authority, Torres Strait Research Program, Canberra
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 409:315–323
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 64:129–141
Uthicke S (2001) Nutrient regeneration by abundant coral reef holothurians. J Exp Mar Biol Ecol 265:153–170
Uthicke S (2004) Overfishing of holothurians: lessons from the Great Barrier Reef. In: Lovatelli A, Conand C, Purcell S, Uthicke S, Hamel J-F, Mercier A (eds) Advances in sea cucumber aquaculture and management. FAO, Rome, pp 163–171
Wolfe K, Vidal-Ramirez F, Dove S, Deaker D, Byrne M (2018) Altered sediment biota and lagoon habitat carbonate dynamics due to sea cucumber bioturbation in a high-pCO2 environment. Glob Change Biol 24:465–480
Wolkenhauer S, Skewes T (2008) Temperature control of burying and feeding activity of Holothuria scabra (Echinodermata: Holothuroidea). Mem Queensl Mus 54:293–301
Yamanouchi T (1956) The daily activity rhythms of the holothurians in the coral reef of Palao Islands. Publ Seto Mar Biol Lab 5:347–362
Yingst JY (1982) Factors influencing rates of sediment ingestion by Parastichopus parvimensis (Clark), an epibenthic deposit-feeding holothurian. Estuar Coast Shelf Sci 14:119–134
Acknowledgements
We thank the Lizard Island Research Station managers and caretakes, and National Marine Science Centre staff for facilitating the field and laboratory work. Thanks also to A. Bowling for her advice on statistical analyses. We thank S. Uthicke and one anonymous reviewer for their constructive suggestions on the manuscript. This research was financially supported by the Marine Ecology Research Centre, Southern Cross University, and conducted under Lizard Island Research Station collection permit GBRMPA G14/36625.1. For the purpose of verifying the validity of the results presented, the raw data and photographs are available from the authors upon request.
Funding
This study was funded through an internal grant by the Marine Ecology Research Centre of Southern Cross University.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
ARH declares that she has no conflict of interest. LM declares that she has no conflict of interest. SWP declares that he has no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Within Australia, animal ethics permits are not required for research on echinoderms. Nonetheless, we held the animals out of water for only 6 min for weighing them, and returned them back to the habitats at the same sites thereafter.
Additional information
Responsible Editor: S. Uthicke.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewed by undisclosed experts.
Rights and permissions
About this article
Cite this article
Hammond, A.R., Meyers, L. & Purcell, S.W. Not so sluggish: movement and sediment turnover of the world’s heaviest holothuroid, Thelenota anax. Mar Biol 167, 60 (2020). https://doi.org/10.1007/s00227-020-3671-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-020-3671-5


