A Tale of Two Urchins - Implications for In-Situ Breeding of the Endangered Banggai Cardinalfish (Pterapogon kauderni)

Samliok Ndobe; Jamaluddin Jompa; Abigail Moore

doi:10.21534/ai.v19i2.110

A Tale of Two Urchins - Implications for In-Situ Breeding of the Endangered Banggai Cardinalfish (Pterapogon kauderni)

Samliok Ndobe, Jamaluddin Jompa, Abigail Moore

Abstract

The endangered Banggai cardinalfish Pterapogon kauderni, endemic to the Banggai Archipelago in Central Sulawesi, Indonesia, is a national and global priority conservation species. To support stock recovery based on in-situ breeding, using the symbiosis between the Banggai cardinalfish and its microhabitat (especially urchins of Genus Diadema), specific research objectives were: (i) identify the Diadema species associated with Banggai cardinalfish in the wild; (ii) investigate Banggai cardinalfish preference between these Diadema species. Belt transect data (5 sites) found wild Banggai cardinalfish of all size classes associated with Diadema setosum and Diadema savignyi. Preference trials were conducted in a controlled environment (concrete tanks) with three replicates. Nine sub-adult Banggai cardinalfish (35-42 mm SL), 12 D. setosum and 12 D. savignyi were placed in each tank. Banggai cardinalfish association (D. savignyi, D. setosum, none) was recorded hourly (06:00-18:00) for three days and results analysed in RStudio-1.0.143. Banggai cardinalfish did not show significant preference for either D. savignyi or D. setosum. These results indicate that D. savignyi and D. setosum can be used impartially in further research on in-situ breeding to facilitate recovery of Banggai cardinalfish stocks. However stock recovery measures should consider genetic connectivity and the natural balance between the two urchin species.

Keywords

Banggai cardinalfish; Diadema; In-situ Breeding; Microhabitat preference; Stock recovery; Symbiosis

Full Text:

Fulltext

References

Allen, G.R. and T.J. Donaldson. 2007. Pterapogon kauderni. The IUCN Red List of Threatened Species 2007: e.T63572A12692964. Doi: 10.2305/IUCN.UK.2007.RLTS.T63572A12692964.en.

Barnosky, A.D. 2014. Palaeontological evidence for defining the Anthropocene. In: Waters, C. N., J.A. Zalasiewicz, M. Williams, M.A. Ellis, A.M. Snelling (Eds), A Stratigraphical Basis for the Anthropocene. Geological Society, London, Special Publications, 395:149–165. http://dx.doi.org/10.1144/SP395.6.

Bernardi, G. and A. Vagelli. 2004. Population structure in Banggai cardinalfish, Pterapogon kauderni, a coral reef species lacking a pelagic larval phase. Marine Biology, 145: 803–810.

Brennand, H.S., N. Soars, S.A. Dworjanyn, A.R. Davis, and M. Byrne. 2010. Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. PLoS One, 5(6): e11372. https://doi.org/10.1371/journal.pone.0011372.

Carpenter, R.C., and P.J. Edmunds. 2006. Local and regional scale recovery of Diadema promotes recruitment of scleractinian corals. Ecology Letters, 9(3): 268-277. Doi: 10.1111/j.1461-0248.2005.00866.x.

Cheung W.W.L., V.W.Y. Lam, J.L. Sarmiento, K. Kearney, R. Watson, and D. Pauly. 2009. Projecting global marine biodiversity impacts under climate change scenarios. Fish and Fisheries, 10: 235–251. DOI: 10.1111/j.1467-2979.2008.00315.x.

Chow, S., Y. Kajigaya, H. Kurogi, K. Niwa, and T. Shibuno. 2014. On the Fourth Diadema Species (Diadema-sp) from Japan. Plos One, 9(7):1-9. e102376(1-9).

CITES (Convention on International Trade in Endangered Species of Wild Fauna and Flora). 2016a. CoP 17 Proposal 46 - Inclusion of Pterapogon kauderni in Appendix II. European Union. https://cites.org/sites/default/files/eng/cop/17/prop/060216/E-CoP17-Prop-46.pdf.

CITES (Convention on International Trade in Endangered Species of Wild Fauna and Flora). 2016c. CoP17 Com. I. 32. Draft decisions on the Banggai cardinalfish (Pterapogon kauderni). https://cites.org/sites/default/files/eng/cop/17/Com_I/E-CoP17-Com-I-32.pdf.

Conant, T.A. 2014. Banggai Cardinalfish, Pterapogon kauderni. Endangered Species Act Draft Status Review Report. National Marine Fisheries Service. National Oceanic and Atmospheric Administration (NOAA), Silverspring, Maryland, USA. 40 pp. http://www.fisheries. noaa.gov/pr/species/Status%20Reviews/banggaii_cardinalfish_sr_2015.pdf.

Coppard, S.E., and A.C. Campbell. 2007. Grazing preferences of diadematid echinoids in Fiji. Aquatic Botany, 86(3): 204–212. https://doi.org/10.1016/j.aquabot.2006.10.005.

Crutzen, P.J. 2002. Geology of mankind: the anthropocene. Nature, 415: 23. Doi: 10.1038/415023a

de Beer, M. 1990. Distribution patterns of regular sea urchins (Echinodermata: Echinoidea) across the Spermonde Shelf, SW Sulawesi (Indonesia). In: D. Ridder, Dubois, Lahaye, & Jangoux (Eds.), Echinoderm Research. Balkerna, Rotterdam, pp. 165-169.

Dirzo, R., H.S. Young, M. Galetti, G. Ceballos, N.J.B. Isaac and B. Collen. 2014. Defaunation in the Anthropocene. Science, 345: 401-406. Doi: 10.1126/science.1251817.

Dorey, N., P. Lançon, M. Thorndyke, and S. Dupont. 2013. Assessing physiological tipping point of sea urchin larvae exposed to a broad range of pH. Global Change Biology, 19: 3355–3367. https://doi.org/10.1111/gcb.12276.

Ellis, E.C. 2011. Anthropogenic transformation of the terrestrial biosphere. Philosophical Transactions of the Royal Society of London Series A, 369: 1010-1035. Doi: 10.1098/rsta.2010.0331

FAO (Food and Agriculture Organisation of the United Nations). 1988. Definition of aquaculture, Seventh Session of the IPFC Working Party of Expects on Aquaculture, IPFC/WPA/WPZ, p.1-3, RAPA/FAO, Bangkok, Thailand.

Hoegh-Guldberg, O., E.S. Poloczanska, W. Skirving, and S. Dove. 2017. Coral reef ecosystems under climate change and ocean acidification. Frontiers in Marine Science, 4(158):1-20. Doi: 10.3389/fmars.2017.00158.

Hoegh-Guldberg, O., H. Hoegh-Guldberg, J.E.N. Veron, A. Green, E.D. Gomez, J. Lough, M. King, H.L. Ambariyanto, J. Cinner, G., Dews, G., Russ, H.Z. Schuttenberg, E.L. Penaflor, C.M. Eakin, T.R.L. Christensen, M. Abbey, F. Areki, R.A. Kosaka, A. Tewfik, and J. Oliver. 2009. The Coral Triangle and Climate Change: Ecosystems, People and Societies at Risk. WWF Australia, Brisbane, Australia. 276 pp.

Hoffman, E.A., N. Kolm, A. Berglund, J.R. Arguello, and A.G. Jones. 2005. Genetic structure in the coral-reef-associated Banggai cardinalfish, Pterapogon kauderni. Molecular Ecology, 14: 1367–1375.

IPCC (International Panel on Climate Change). 2014. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team, R.K. Pachauri and L.A. Meyer (Eds.)]. IPCC, Geneva, Switzerland, 151 pp.

Jackson, J.B.C. 2008. Ecological extinction and evolution in the brave new ocean. Proceedings of the National Academy of Sciences, 105(S1): 11458–11465. Doi: 10.1073/pnas.0802812105

Jones, M.C. and W.W. Cheung. 2014. Multi-model ensemble projections of climate change effects on global marine biodiversity. ICES Journal of Marine Science, 72(3): 741-752.

Kolm, N., and A. Berglund. 2003. Wild populations of a reef fish suffer from the “nondestructive” aquarium trade fishery. Conservation Biology, 17(3): 910-914.

Lessios, H.A. 2007. Reproductive isolation between species of sea urchins. Bulletin of Marine Science, 81(2), 191–208.

Lessios, H.A., and J.S. Pearse. 1996. Hybridization and introgression between Indo-Pacific species of Diadema. Marine Biology, 126(4): 715-723.

Lessios, H.A., B.D. Kessing, and J.S. Pearse. 2001. Population Structure and Speciation in Tropical Seas: Global Phylogeography of the Sea Urchin Diadema. Evolution, 55(5): 955–975. https://doi.org/10.1554/0014-3820(2001)055[0955: PSASIT]2.0.CO;2.

Lunn, K.E., and A.M. Moreau. 2004. Unmonitored trade in Marine Ornamental Fishes: the Case of Indonesia's Banggai Cardinalfish (Pterapogon kauderni). Coral Reefs, 23: 344-341. Doi: 10.1007/s00338-004-0393-y.

Maciá S., M.P. Robinson, and A. Nalevanko. 2007. Experimental dispersal of recovering Diadema antillarum increases grazing intensity and reduces macroalgal abundance on a coral reef. Marine Ecology Progress Series, 348: 173-182. https://doi.org/10.3354/meps06962.

MMAF (Ministry for Marine Affairs and Fisheries of the Republic of Indonesia). 2015. Peraturan Menteri Kelautan dan Perikanan Repulik Indonesia Nomor 45 Tahun 2015. Rencana Strategis Kementerian Kelautan dan Perikanan 2015-2019. Kementerian Kelautan dan Perikanan, Jakarta, Indonesia. http://roren.kkp.go.id/arsip/file/137/renstra-kkp-2015-2019-permen-kp-no.-45-th.-2015.pdf/.

Molinos, J.G., B.S. Halpern, D.S. Schoeman, C.J., Brown, W. Kiessling, P.J. Moore, J.M. Pandolfi, E.S. Poloczanska, A.J. Richardson, and M.T. Burrows. 2016. Climate velocity and the future global redistribution of marine biodiversity. Nature Climate Change, 6(1): 83-88.

Moore, A., S. Ndobe, and M. Zamrud. 2011. Monitoring the banggai cardinalfish, an endangered restricted range endemic species. Journal of Indonesian Coral Reefs, 1(2): 99-113.

Moore, A., S. Ndobe, A.I.M. Salanggon, Ederyan, and A. Rahman. 2012. Banggai Cardinalfish Ornamental Fishery: The Importance of Microhabitat. Proceedings of the 12th International Coral Reef Symposium, Cairns, Australia, 9-13 July 2012, 13C_1. 5 pages. http://www.icrs2012.com/proceedings/manuscripts/ICRS2012_13C_1.pdf.

Moore, A., S. Ndobe, and J. Jompa. 2017a. Konsep konservasi berbasis kawasan dalam rangka pemulihan populasi endemik Banggai cardinalfish (Pterapogon kauderni). Coastal and Ocean Journal, under review.

Moore, A., S. Ndobe, and J. Jompa. 2017b. Fingerprints of the Anthropocene: the 2016 Coral Bleaching Event in an Equatorial Archipelago. Proceedings of the 4th International Marine and Fisheries Symposium, Makassar, 20 May 2017. Hasanuddin University, Makassar, Indonesia. In press.

Mumby, P.J., J.D. Hedley, K. Zychaluk, A.R. Harborne, and P.G. Blackwell. 2006. Revisiting the catastrophic die-off of the urchin Diadema antillarum on Caribbean coral reefs: Fresh insights on resilience from a simulation model. Ecological Modelling, 196: 131-149. Doi: 10.1016/j.ecolmodel.2005.11.035.

Mumby, P.J., A. Hastings, and H.J. Edwards. 2007. Thresholds and the resilience of Caribbean coral reefs. Nature, 450: 98-101.

Muthiga, N.A. 2003. Coexistence and reproductive isolation of the sympatric echinoids Diadema savignyi Michelin and Diadema setosum (Leske) on Kenyan coral reefs. Marine Biology, 143: 669–677. https://doi.org/10.1007/s00227-003-1095-7.

Muthiga, N.A., and T.R. McClanahan. 2007. Ecology of Diadema. Chapter 11 in Lawrence, J.M. (2007). Edible Sea Urchins: Biology and Ecology. Developments in Aquaculture and Fisheries Science, 37: 205-225.

Muthiga, N.A., and T.R. McClanahan. 2013. Diadema. In J. M. Lawrence (Ed.), Edible Sea Urchins: Biology and Ecology (pp. 257–274). Elsevier. https://doi.org/10.1016/B978-0-12-396491-5.00018-6.

Ndobe, S. 2013. Biologi dan Ekologi Banggai Cardinalfish, Pterapogon kauderni (Suatu Kajian Dalam Upaya Pengelolaan Perikanan Berbasis Konservasi. Doctoral Dissertation. Postgraduate Program, Faculty of Fisheries and Marine Science, Brawijaya University, Malang, Indonesia. 397+xxviii pp.

Ndobe S. and A. Moore. 2005. Potensi dan Pentingnya Pengembangan Budidaya In-situ Pterapogon kauderni (Banggai Cardinalfish). InfoMAI,4 (2) : 9-14.

Ndobe, S., A. Moore, and A. Supu. 2005. Sulawesi Case Study - Banggai Kepulauan. Pages 5-143 & 165-229 In The Indonesian Ornamental Fish Trade: Case Studies and Options for Improving Livelihoods while Promoting Sustainability in Banggai and

Banyuwangi. The International Seafood Trade: Supporting Sustainable Livelihoods Among Poor Aquatic Resource Users in Asia (EC Prep Project EP/RO3/R14). Poseidon and Network of Aquaculture Centres in Asia (NACA) STREAM. 286 pages. Retrieved from: http://www.enaca.org/publications/livelihoods-gender-social/stream/regional/EcprepIndonesia.pdf.

Ndobe, S., Madinawati, and A. Moore. 2008 Pengkajian Ontogenetic Shift pada Ikan Endemik Pterapogon kauderni. Jurnal Mitra Bahari, 2(2): 32-55.

Ndobe, S., D. Setyohadi, E.Y. Herawati, Soemarno, A. Moore, M.D. Palomares, and D. Pauly. 2013a. Life History of Banggai Cardinalfish (Pterapogon kauderni; Pisces, Apogonidae) in Banggai Islands and Palu Bay, Sulawesi, Indonesia. Acta Ichthyologica Et Piscatoria, 43(3): 237–250. Doi: 10.3750/AIP2013.43.3.08.

Ndobe, S., A. Moore, Nasmia, Madinawati, and N. Serdiati. 2013b. The Banggai cardinalfish: an overview of local research (2007-2009). Galaxea, Journal of Coral Reef Studies (2013, Special Issue): 243-252.

Ndobe, S., I. Widiastuti, and A. Moore. 2013c. Sex ratio dan Pemangsaan terhadap Rekrut pada Ikan Hias Banggai Cardinalfish (Pterapogon kauderni). Prosiding Konferensi Akuakultur Indonesia 2013. http://epaper.aquaculture-mai.org/upload/2.%20Ndobe%20dkk%20KAI% 202013.pdf.

Ndobe, S.; Moore, A., Salanggon, A.I.M., Muslihudin, Setyohadi, D., Herawati, E.Y., Soemarno. 2013d. Banggai cardinalfish (Pterapogon kauderni) Management - an Ecosystem-Based Approach. Marine Fisheries, 4(2): 115-126.

Ndobe, S., A. Moore, and J. Jompa. 2017. Status dan ancaman terhadap mikrohabitat ikan endemik terancam punah Banggai cardinalfish (Pterapogon kauderni). Coastal and Ocean Journal, under review.

Pearse. J.S. 1970. Reproductive perodicities of Indo-Pacific Invertebrates in the Gulf of Suez. III. The Echinoid Diadema setosum (Leske). Bulletin of Marine Science, 20(3): 697-720.

Pearse. J.S. 1998. Distribution of Diadema savignyi and D. setosum in the tropical Pacific. Echinoderms: San Francisco. AA Balkema, Rotterdam. 1998:777-82.

Pendleton, L., A. Comte, C. Langdon, J.A. Ekstrom, S.R. Cooley, L. Suatoni, M.W. Beck, L.M. Brander, L. Burke, J.E. Cinner, C. Doherty, P.E.T. Edwards, D. Gledhill, L-Q. Jiang, R.J. van Hooidonk, L. Teh, G.G. Waldbusser, and J. Ritter. 2016. Coral Reefs and People in a High-CO2 World: Where Can Science Make a Difference to People. Plos One, 11(11): e0164699. Doi: 10.1371/journal.pone.0164699.

Precht, L.L., and W.F. Precht. 2015. The sea urchin Diadema antillarum – keystone herbivore or redundant species. Peer J. Preprints, 1–48 pp. https://doi.org/10.7287/peerj.preprints.1565v2

Schwägerl, C. 2014. The Anthropocene: the human era and how it shapes our planet. Synergetic Press, London. 249 pp.

Sherman, E. 2015. Can sea urchins beat the heat? Sea urchins, thermal tolerance and climate change. PeerJ, 3, e1006. Doi: 10.7717/peerj.1006.

Steffen, W., J. Grinevald, P. Crutzen, and J. McNeill. 2011. The Anthropocene: conceptual and historical perspectives. Philosophical Transactions of the Royal Society Series A, 369: 842-867. Doi: 10.1098/rsta.2010.0327.

Vagelli, A.A. 2004. Ontogenetic shift in habitat preference by pterapogon kauderni, a shallow water coral reef apogonid with direct development. Copeia, (2): 364-369. Doi: 10.1643/CE-03-059R2.

Vagelli A.A. 2008. The unfortunate journey of pterapogon kauderni: a remarkable apogonid endangered by the international ornamental fish trade, and its case in CITES. SPC Live Reef Fish Information Bulletin,18:17-28.

Vagelli, A.A. 2011. The banggai cardinalfish: natural history, conservation, and culture of Pterapogon kauderni. John Wiley & Sons, Ltd., Chichester, UK. Doi: 10.1002/9781119950387.

Vagelli A.A., M. Burford, and G. Bernardi. 2009. Fine scale dispersal in Banggai Cardinalfish, Pterapogon kauderni, a coral reef species lacking a pelagic larval phase. Marine Genomics, 1: 129–134.

Zalasiewicz, J., M. Williams, A. Haywood, and M. Ellis. 2011. The Anthropocene: a new epoch of geological time? Philosophical Transactions of the Royal Society Series A, 369: 835-841. Doi: 10.1098/rsta.2010.0339.

DOI: http://dx.doi.org/10.21534/ai.v19i2.110