Complex patterns of genetic structure in the sea cucumber Holothuria (Metriatyla) scabra from the Philippines: implications for aquaculture and fishery management

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmars.2024.1396016/full#supplementary-materialThe sandfish Holothuria (Metriatyla) scabra, is a high-value tropical sea cucumber harvested from wild stocks for over four centuries in multi-species fisheries across its Indo-Pacific distribution, for the global bêche-de-mer (BDM) trade. Within Southeast Asia, the Philippines is an important centre of the BDM trade, however overharvesting and largely open fishery management have resulted in declining catch volumes. Sandfish mariculture has been developed to supplement BDM supply and assist restocking efforts; however, it is heavily reliant on wild populations for broodstock supply. Consequently, to inform fishery, mariculture, germplasm and translocation management policies for both wild and captive resources, a high-resolution genomic audit of 16 wild sandfish populations was conducted, employing a proven genotyping-by-sequencing approach for this species (DArTseq). Genomic data (8,266 selectively-neutral and 117 putatively-adaptive SNPs) were used to assess fine-scale genetic structure, diversity, relatedness, population connectivity and local adaptation at both broad (biogeographic region) and local (within-biogeographic region) scales. An independent hydrodynamic particle dispersal model was also used to assess population connectivity. The overall pattern of population differentiation at the country level for H. scabra in the Philippines is complex, with nine genetic stocks and respective management units delineated across 5 biogeographic regions: (1) Celebes Sea, (2) North and (3) South Philippine Seas, (4) South China and Internal Seas and (5) Sulu Sea. Genetic connectivity is highest within proximate marine biogeographic regions (mean Fst=0.016), with greater separation evident between geographically distant sites (Fst range=0.041–0.045). Signatures of local adaptation were detected among six biogeographic regions, with genetic bottlenecks at 5 sites, particularly within historically heavily-exploited locations in the western and central Philippines. Genetic structure is influenced by geographic distance, larval dispersal capacity, species-specific larval development and settlement attributes, variable ocean current-mediated gene flow, source and sink location geography and habitat heterogeneity across the archipelago. Data reported here will inform accurate and sustainable fishery regulation, conservation of genetic diversity, direct broodstock sourcing for mariculture and guide restocking interventions across the Philippines.The author(s) declare financial support was received for the research, authorship, and/or publication of this article. Australian Centre for International Agriculture Research (ACIAR) project FIS/2016/122: “Increasing technical skills supporting community-based sea cucumber production in Vietnam and the Philippines”. Philippine Council for Agriculture, Aquatic and Natural Resources Research and Development of the Department of Science and Technology (DOST-PCAARRD: Project Numbers QSR-MR-CUC.02.01 and QSR-MR-CUC.02.02)

Nursery culture of sandfish Holothuria scabra in sea-based floating hapa nets: Effects of initial stocking density, size grading and net replacement frequency

Sea-based culture of early juvenile sandfish Holothuria scabra up to fingerling size (>2 g) using floating hapa nets has been confirmed as a viable nursery system in tropical countries such as the Philippines. However, production can be further optimized through more efficient rearing practices. In this study, we demonstrate the effects of initial stocking density, size grading and net replacement frequency during the culture of early juvenile sandfish in sea-based floating hapa nets (2 × 1 × 1 m). Testing different initial stocking density treatments ranging from 150 to 2000 early juveniles (4–10 mm; 0.02–0.06 g) per hapa net, we confirmed significantly faster growth (0.06–0.08 g d−1) and higher survival (72–97%) in low densities (≤500 hapa−1), compared to high densities (≥700 hapa−1: 0.02–0.04 g d−1; 67–80%). Low density culture can produce 2 g sandfish in about a month, while higher densities will require a 2–3 mo culture period to reach this size. Culture performance following size grading was also compared using three initial size classes (small, 0.05–0.99 g; medium, 1–1.99 g; and large, 2–3 g) and a mixed group (0.05–3.00 g). At 45 d, juveniles in pooled size-graded groups grew significantly faster (0.11–0.13 g d−1) than those in the mixed group (0.01 g d−1). Survival was significantly higher in the medium (85.3%) and large (84.7%) groups, than those in the small (54.4%) and mixed (45.6%) groups. However, size variation was not significantly mitigated by grading during the 45-d culture. Culture performance of sandfish was not significantly enhanced by more frequent net replacement for short-term rearing (30–45 d). Optimal results were gained from an initial stocking density of ≤500 early juveniles (5–10 mm) per floating hapa net which may be cultured in a month, without requiring net replacement and size grading to produce ≥2 g sandfish. However, in cases of high hatchery production, it is also feasible to adopt higher density stocking (e.g. >1000 hapa−1), but will require longer culture duration (60–85 d), monthly net replacement and size-grading to attain the same size. Results of this study can help fine-tune management practices for nursery culture of sandfish in sea-based floating hapa net nurseries in order to boost production of fingerlings needed for aquaculture and restocking.This study was funded by the Australian Centre for International Agriculture Research (ACIAR) through the project FIS/2010/042 “Expansion and Diversification of Production and Management Systems for Sea Cucumbers in the Philippines, Vietnam and Northern Australia” with counterpart funding support by SEAFDEC/AQD through study code FS-03-Y2014T. Special thanks to MRB Altamirano for valuable help in developing the manuscript in the early stages. We also appreciate the useful suggestions from M Lal and P Southgate, as well as the constructive comments from anonymous reviewers, all contributed in improving this paper. We are grateful to CP Recente, JC Rodriguez, Jr., H Figurado, and N Tibubos for the assistance in sandfish hatchery production, experimental setup and monitoring

Establishment of a community-based sandfish sea ranch in Barangay Polopiña, Concepcion, Iloilo (Western Visayas node case study)

This study was primarily funded by ACIAR through the project ‘Expansion and Diversification of Production and Management Systems for Sea Cucumbers in the Philippines, Vietnam and Northern Australia’ (FIS/2010/042) with counterpart funding support by SEAFDEC/AQD through study codes FS-10-Y2010T and FS-03-Y2014T

Factors affecting the spatio-temporal variability in the production of sandfish Holothuria scabra juveniles in floating hapa ocean nursery systems

Hatchery production of the tropical sea cucumber Holothuria scabra or sandfish has been successfully demonstrated in various countries, especially during the past decade. However, the main bottleneck in up-scaling production of larger sandfish juveniles is in the nursery phase where land-based facilities are limited in the Philippines compared to other countries. This has led to some promising pioneering research in ocean-based sandfish nurseries in the Philippines. However, site-specific and seasonal inconsistencies in production levels were observed. In this study, a comprehensive experiment comparing 17 replicated nursery culture operations of sandfish juveniles using floating hapas, was conducted across four sites with distinct geo-climatic zones in the Philippines and at different months from 2013 to 2016. We evaluated the performance of the ocean-based floating hapa nursery system by determining the effects of periphyton characteristics and broad-scale differences in meteorological variables to growth and survival of juvenile sandfish within different geo-climatic zones. Our data confirmed high spatial (across site) and temporal (among trials within site) variability in sandfish culture performances. Wind stress was the most significant driver of this variation, which negatively influenced growth and survival of juveniles especially during Cycle 1 (first 30 d). Sandfish growth was positively related to Chl-a and mean temperature, but was negatively impacted by Wind stress, Autotropic Index (AI), total rainfall (∑Rain), and sea-surface atmospheric pressure; while survival was positively affected by phaeophytin and Ash-Free Dry Weight (AFDW) content of the hapa biofilm. In Cycle 2 (succeeding 31–60 d), growth and survival was greatly influenced negatively by the re-stocked density (number of individuals surviving from Cycle 1), while survival was further affected negatively by ∑Rain and AFDW. Our results provide significant information on suitable ocean nursery conditions, periphyton/biofilm characteristics, and spatial-temporal considerations for optimizing production of H. scabra juveniles in floating hapas. We also highlight the negative effects of increasing biomass density when on-growing larger juveniles in this system. These insights are valuable in optimizing management and operation of ocean nurseries for sandfish, not only in various potential sites in the Philippines, but also in many developing tropical countries in the Indo-Pacific.This study was funded by the Australian Centre for International Agriculture Research (ACIAR) through the project FIS/2010/042 “Expansion and Diversification of Production and Management Systems for Sea Cucumbers in the Philippines, Vietnam and Northern Australia” and FIS/2016/122 “Increasing technical skills supporting community-based sea cucumber production in Vietnam and the Philippines” with counterpart funding support from the University of the Philippines Marine Science Institute (UP-MSI) and administrative support from the Marine Environment and Resources Foundation (MERF), Inc.; SEAFDEC/AQD with the study code FS-01-Y2019T; Guiuan Development Foundation, Inc. (GDFI) with the Bureau of Fisheries and Aquatic Resources (BFAR) Region 8; and the Mindanao State University at Naawan (MSU-Naawan)

Integrated production of abalone, Haliotis asinina, and sandfish, Holothuria scabra, through Community-Based Resource Enhancement (CBRE) in Molocaboc Island in Sagay Marine Reserve, Philippines

This study conducted participatory enhancement of abalone Haliotis asinina and sandfish Holothuria scabra stocks using hatchery-bred and reared seeds released in the shores of Molocaboc Island in multi-use buffer zone of Sagay Marine Reserve, Philippines. The Community-Based Resource Enhancement (CBRE) process, implemented continuously from 2006 to 2019, include social and biophysical preparation, formulation of fisheries management and governance strategies, release of hatchery-reared juveniles, monitoring and periodic assessment, and socioeconomic impact assessment. CBRE was implemented through a tri-party collaboration involving fisherfolks, local government and research institutions. The abalone and sandfish enhancement procedures comprised of breeding in hatcheries, rearing of juveniles either in nursery facilities or net cages in coastal areas, and release in enhancement areas. A total of 11,500 tagged abalone juveniles were released in 11 batches in a protected coralline site from 2011 to 2015. Monthly monitoring showed increase in abalone catch per unit effort (3 divers, 1 hour fishing) in the release site from 0–2 individuals during baseline in 2011 to up to 150 individuals until 2019, including spill-overs without tags. Meanwhile, 96,400 hatchery-bred and reared sandfish juveniles were stocked in floating netcages in 15 batches and later released in sea ranch where mean density increased significantly from 3 to 138 individuals/ha in 2015 to 2019. Gleaning should comply with locally instituted catch-size regulation to sustain the fishery. Additional project activities include the construction and operationalization of a smallscale solar-powered hatchery on-site; freeze-drying trials of abalone meat to improve market reach; and initiatives to replicate the project in Lahuy Islands in Caramoan, Camarines Sur. Aquaculture, through seed production, therefore plays a key role in enhancement of threatened high-value species. Resource enhancement benefitted the fisheries through participatory management and eventually provided spill-overs to supplement income of marginalized fishers.The authors thank SEAFDEC/AQD and collaborators such as the Barangay Molocaboc FARMC/MOSRA and PAMBSMR of Sagay City. Funds and program support were provided by the GOJTF (8100-T-RD-SE0105, SE0110, and SE0015). The authors acknowledge the inputs from GOJTF Co-Managers Dr. Koichi Okuzawa, Dr. Hiroshi Ogata, Dr. Teruo Azuma, Dr. Takuro Shibuno, Dr. Chihaya Nakayasu, and Dr. Koh-ichiro Mori