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Analysis of Optimal Habitat for Captive Release of the Sea Cucumber Holothuria Scabra

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Analysis of Optimal Habitat for Captive Release of the Sea Cucumber Holothuria Scabra Vol. 588: 85–100, 2018 MARINE ECOLOGY PROGRESS SERIES Published February 8 https://doi.org/10.3354/meps12444 Mar Ecol Prog Ser OPENPEN ACCESSCCESS Analysis of optimal habitat for captive release of the sea cucumber Holothuria scabra Daniela M. Ceccarelli1, Murray Logan2, Steven W. Purcell1,3,* 1National Marine Science Centre, Southern Cross University, PO Box 4321, Coffs Harbour, NSW 2450, Australia 2Australian Institute of Marine Science, PMB No. 3, Townsville MC, QLD 4810, Australia 3WorldFish, PO Box 500, Penang 10670, Malaysia ABSTRACT: The success of marine stocking programs hinges on releasing hatchery-produced juvenile animals into the optimal marine habitat. This study sought to identify optimal microhabi- tat features of coastal seagrass meadows for juvenile sea cucumbers Holothuria scabra, a species cultured widely for stock restoration, sea ranching and sea farming. Groups of 25 juveniles were released into 30 replicate 1 m2 open sea pens embedded into sediments in a coastal bay of New Caledonia at sites with varying biotic and physical features. Survival after 8 to 10 d ranged from 0 to 100% and averaged 77%. Boosted regression tree analyses found that different variables affected survival, growth and burying behaviour. Survival was significantly higher at shallow depths with intermediate seagrass cover (~42%). Growth rate was significantly higher at compa- rable intermediate seagrass cover (~34%) and for smaller juveniles, presumably displaying com- pensatory growth. Burying frequency of juveniles was largely explained by habitat variables, notably a high organic carbon content of sediments and shallow seawater depths. Juveniles sur- vived better where they buried more frequently, providing empirical evidence of a predator- avoidance mechanism. Our findings reveal that marine animals can display non-linear responses to habitat features such as seagrass cover. These marine invertebrates should be released in habi- tats that optimize survival, growth and behaviours and be spread among multiple sites to mitigate against stochastic mortality events. This experimental approach offers clear advantages over factorial designs for identifying optimal habitats for captive-release programs. KEY WORDS: Stock enhancement · Sea cucumber · Habitat requirements · Regression modelling · Survival · Predation · Invertebrate · Seagrass INTRODUCTION al. 2005, Hines et al. 2008, Zohar et al. 2008), mud crabs (Okuzawa et al. 2008), lobsters and crayfish Rising global demand for marine resources and (Bannister & Addison 1998), queen conch (Brown- overfishing of wild stocks have led to widespread scombe et al. 2015), giant clams (Andréfouet et al. interest in stocking aquaculture-reared animals into 2005, Gomez & Mingoa-Licuanan 2006, Okuzawa et the wild for restocking, sea ranching and sea farming al. 2008), topshell gastropods (Castell et al. 1996, Pur- (Bell et al. 2005, 2008). There is a long history of cell 2004a, Purcell & Cheng 2010) and sea cucumbers stocking finfish into the sea, but invertebrate stock- (Lovatelli et al. 2004, Battaglene & Bell 2008, Purcell ing is a relatively recent endeavour (Bell et al. 2005, 2012, Juinio-Meñez et al. 2017). Initial efforts were Bartley & Bell 2008, Leber 2012). Well-documented plagued by high mortality of released juveniles and programs include the restocking and sea ranching of low economic returns due to a lack of knowledge scallops, sea urchins, abalone and other bivalves (Ar - about the technology and ecology of releasing juve- nold 2008, Okuzawa et al. 2008), blue crabs (Davis et niles into the wild, leading to studies to improve © The authors 2018. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 86 Mar Ecol Prog Ser 588: 85–100, 2018 release strategies and track the survival of released rates because predation risk declines as juveniles animals (Bartley & Bell 2008). Experimental designs grow larger, but releasing larger juveniles is more and scientific approaches to determine the habitats costly (Molony et al. 2003, Leber et al. 2005, Roberts to release juvenile invertebrates have been basic et al. 2007, Purcell & Simutoga 2008). Animals (Table 1) and need improvement to optimise the suc- released in suboptimal habitats either migrate out of cess of stocking programs. the areas in search of more suitable conditions, are Mortality in the wild of hatchery-produced juve- eaten rapidly because they are vulnerable to preda- niles of a variety of invertebrate taxa is typically high tors (Bartley & Bell 2008) or perish through environ- soon after release, often occuring during the first day mental stress or malnutrition (Dance et al. 2003), or within the first month (Crowe et al. 2002, Oliver et competitive exclusion and other stressful conditions al. 2005, Dixon et al. 2006, Purcell & Simutoga 2008). (Childress & Herrnkind 2001, Purcell 2004b, Purcell Key determinants of survival of the juveniles include & Cheng 2010). Density of released individuals can the size at release and the density and habitat in also be important, as mortality can be density-depen- which animals are released (Munro & Bell 1997, Bell dent for many invertebrate species (Beal & Kraus et al. 2005). Size at release can influence mortality 2002, Hines et al. 2008). Table 1. Examples of captive release studies on marine invertebrates that specifically tested the effects of habitat Species Common name Location Design Reference Holothuria scabra Sandfish Solomon Islands Factorial design (habitat types, Dance et al. (2003) mangrove−seagrass combinations and coral reef types) New Caledonia Exploratory; effects of microhabitat Purcell & Simutoga (2008) (seagrass composition, sediment size, organic content) examined in multi- variable biplot Papua New Guinea Exploratory; effects of microhabitat Hair et al. (2016) (seagrass composition, sediment size, organic content) examined in multi- variable biplot Penaeus esculentus Brown tiger prawn Northern Australia Factorial design, substratum types Kenyon et al. (1995) (2 seagrass habitats and 1 bare substratum), effects on predation Penaeus semisulcatus Green tiger prawn Northern Australia Factorial design, comparing growth Loneragan et al. (2001) rates between 2 levels of plant biomass Callinectes sapidus Chesapeake Bay Chesapeake Bay Factorial design, 3 depths, 4 coves, Hines et al. (2008) blue crab 2 positions in the river Carcinus maenas Shore crab Western Sweden Factorial design, habitat types Moksnes (2002) (mussels, algae, eelgrass, open sand) Jasus edwardsii Red rock lobster New Zealand Factorial design, 3 shelter shapes, Booth & Ayers (2005) 4 hole sizes, pairwise tests Panulirus argus Caribbean spiny Florida Factorial design, hard bottom vs. Behringer et al. (2009) lobster seagrass habitats Palinurus elephas European spiny Sicily Factorial design, 3 shelter shapes, Gristina et al. (2009) lobster 5 shelter sizes, 2 substrate slopes Mercenaria mercenaria Hard clam North Carolina Factorial design, 3 levels of Irlandi (1994) seagrass % cover Lobatus gigas Queen conch Bahamas Factorial design, 3 levels of Ray & Stoner (1995) seagrass % cover Bahamas Factorial design, habitat types Brownscombe et al. (2015) (seagrass, rubble) and regression Haliotis laevigata Greenlip abalone South Australia Factorial design, 2 habitat types Dixon et al. (2006) (layers of boulders) Ceccarelli et al.: Optimal habitat for stocking sea cucumbers 87 A key knowledge gap still hindering the success of post-release survival and growth) and the various stocking for many invertebrate taxa is the specific physical conditions that exist in likely habitats for (micro)-habitat requirements of newly released juve- captive release (Purcell & Simutoga 2008, Hair et al. niles. Finding the ideal habitat for releasing juveniles 2016). Responses will still be variable for any rela- is more critical for slow-moving invertebrates than tionship with these features, since many spatially for fishes, which can easily move away from un- variable processes, like predation, can occur stochas- favourable habitats (Gillanders et al. 2003). Specific tically. However, a multiple-variable approach can nursery habitats occupied most by wild juveniles provide better resolution for future captive-release would point to suitable habitats for release, but data programs because the habitat-related variations in on habitat preferences of wild juveniles are lacking responses are measured. This can allow a restocking for many invertebrate taxa (Conand 1989, Shiell program to better pinpoint specific habitat features to 2004, Wolfe & Byrne 2017). Equally, identified juve- target for releasing captive-reared juveniles. nile habitats might not be optimal, as they can be In this study, we applied a regression-based exper- extremely limited in size, thus limiting area sizes for imental field-release design, and we used gradient juvenile release, or may be determined by current- boos ted regression tree (BRT) models to evaluate driven larval distribution or stochastic events rather optimal habitat features for restocking and sea than specific environmental characteristics (Slater & ranching of a tropical sea cucumber, the sandfish Jeffs 2010, Slater et al. 2010). Owing to ontogenetic Holothuria scabra. Among tropical sea cucumber habitat shifts, the habitats most preferred by adults species, the sandfish commands the highest maxi-
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