Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

DNA barcoding of fish larvae reveals uncharacterised biodiversity in tropical peat swamps of New Guinea, Indonesia

Arif Wibowo A E , Niklas Wahlberg B D and Anti Vasemägi B C

A Research Institute for Inland Fisheries, Agency for Marine and Fisheries Research, Ministry of Marine Affairs and Fisheries, Jalan Beringin 08 Mariana, Palembang, 30763, South Sumatera, Indonesia.

B Department of Biology, University of Turku, Pharmacity Itäinen Pitkäkatu 4, FI-20014 Turku, Finland.

C Department of Aquaculture, Institute of Veterinary Medicine and Animal Sciences, Estonian University of Life Sciences, Kreutzwaldi 1, EE-51014 Tartu, Estonia.

D Department of Biology, Lund University, Sölvegatan 35, SE-223 62 Lund, Sweden.

E Corresponding author. Email: wibowo@daad-alumni.de

Marine and Freshwater Research - https://doi.org/10.1071/MF16078
Submitted: 14 March 2016  Accepted: 5 August 2016   Published online: 13 September 2016

Abstract

The Indonesian archipelago, Borneo, Sumatra and West New Guinea (Papua), hosts half of the world’s known tropical peat swamps, which support a significant proportion of the estimated biodiversity on Earth. However, several species groups that inhabit peat swamp environments remain poorly characterised and their biology, particularly during early life stages, is not well understood. In the present study we characterised larval and juvenile fish biodiversity, as well as spatial and temporal variability, in a pristine peat swamp environment of the River Kumbe in West New Guinea, Indonesia, based on analysis of the mitochondrial cytochrome-c oxidase subunit 1 (COI) sequence (501 bp). Altogether, 10 fish species were detected in the peat swamp habitat during the larval and juvenile stages, whereas 13 additional species were caught at older stages. Twelve species were detected only in a single site, whereas some species, such as the Western archerfish (Toxotes oligolepis) and Lorentz’s grunter (Pingalla lorentzi), were observed in all sampling sites. The occurrence of fish larvae also varied temporally for several species. In contrast with many earlier DNA barcoding studies in fish, we were not able to determine the species identity for a large proportion of sequenced larvae (68%) because of the lack of corresponding COI sequences in the reference dataset. Unidentified sequences clustered into five separate monophyletic clades. Based on genetic divergences, the putative taxonomic origin for the five morphotypes are Atherinidae, Osteoglossidae, Terapontidae and Gobiidae.


References

Ahmad, A., Ali, A. B., and Mansor, M. (2002). Conserving a highly diverse aquatic ecosystem of Malaysia: a case study of freshwater fish diversity in peat swamp habitat. In ‘TROPEAT 2002 – International Symposium on Land Management and Biodiversity in Southeast Asia’, 17–20 September 2002, Bali, Indonesia. Paper S7 09. (Suda Printing Co., Ltd: Sapporo, Japan.)

Aljanabi, S. M., and Martinez, I. (1997). Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research 25, 4692–4693.
Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques.CrossRef | 1:CAS:528:DyaK1cXhsFWrsA%3D%3D&md5=328094094bc8a54471b531d1fc4c56e1CAS | 9358185PubMed | open url image1

Allen, G. R. (1991). Hardyheads, family Atherinidae. In ‘Field Guide to the Freshwater Fishes of New Guinea’. pp. 103–123. (Christensen Research Institute, University of California: San Diego, CA, USA.)

Allen, G. R., Midgley, S. H., and Allen, M. (2002). ‘Field Guide to the Freshwater Fishes of Australia.’ (Western Australian Museum: Perth, WA, Australia.)

Andriesse, J. P. (1988). Nature and management of tropical peat soils. Soils Bulletin number 59, Food and Agriculture Organization of the United Nations, Rome, Italy.

Baldwin, C. C., Brito, B. J., Smith, D. G., Weigt, L. A., and Escobar-Briones, E. (2011). Identification of early life-history stages of Caribbean apogon (Perciformes: Apogonidae) through DNA Barcoding. Zootaxa 3133, 1–36. open url image1

Baumgartner, G., Nakatani, K. K., and Gomes, L. C. (2004). Identification of spawning sites and natural nurseries of fishes in the upper Parana River, Brazil. Environmental Biology of Fishes 71, 115–125.
Identification of spawning sites and natural nurseries of fishes in the upper Parana River, Brazil.CrossRef | open url image1

Beamish, F. W. H., Beamish, R. B., and Lim, S. L. H. (2003). Fish assemblages and habitat in a Malaysian Blackwater peat swamp. Environmental Biology of Fishes 68, 1–13.
Fish assemblages and habitat in a Malaysian Blackwater peat swamp.CrossRef | open url image1

Bialetzki, A., Nakatani, K., Sanches, P. V., Baumgartner, G., and Gomes, L. C. (2005). Larval fish assemblage in the Baıa River (Mato Grosso do Sul State, Brazil): temporal and spatial patterns. Environmental Biology of Fishes 73, 37–47.
Larval fish assemblage in the Baıa River (Mato Grosso do Sul State, Brazil): temporal and spatial patterns.CrossRef | open url image1

Butcher, B. A., Smith, M. A., Sharkey, M. J., and Quicke, D. L. J. (2012). A turbotaxonomic study of Thai Aleiodes (Aleiodes) and Aleiodes (Arcaleiodes) (Hymenoptera: Braconidae: Rogadiniae) based largely on COI barcoded specimens, with rapid descriptions of 179 new species. Zootaxa 3457, 1–232. open url image1

Chimner, R. A., and Ewel, K. C. (2005). A tropical freshwater wetland, II: production, decomposition and peat formation. Wetlands Ecology and Management 13, 671–684.
A tropical freshwater wetland, II: production, decomposition and peat formation.CrossRef | open url image1

Collins, R. A., and Cruickshank, R. H. (2013). The seven deadly sins of DNA barcoding. Molecular Ecology Resources 13, 969–975.
| 1:STN:280:DC%2BC3s3lvVOqug%3D%3D&md5=e21e2fdb2ea7b548c5412f763f52c98cCAS | 23280099PubMed | open url image1

Collins, R. A., Armstrong, K. F., Meier, R., Yi, Y., Brown, S. D. J., and Cruickshank, R. H. (2012). Barcoding and border biosecurity: identifying cyprinid fishes in the aquarium trade. PLoS One 7, e28381.
Barcoding and border biosecurity: identifying cyprinid fishes in the aquarium trade.CrossRef | 1:CAS:528:DC%2BC38XitVGht7c%3D&md5=c251a199e1b31d3be3f3c291fbb81f8fCAS | 22276096PubMed | open url image1

Dennis, C., and Aldhous, P. (2004). A tragedy with many players. Nature 430, 396–398.
A tragedy with many players.CrossRef | 1:CAS:528:DC%2BD2cXlvVaksr0%3D&md5=cf3b49b4fa0cc599a4e1eb13d0d2a87cCAS | 15269738PubMed | open url image1

Dereeper, A., Guignon, V., Blanc, G., Audic, S. S., Buffet, F., Chevenet, F., Dufayard, J. F., Guindon, S., Lefort, V., Lescot, M., Claverie, J. M., and Gascuel, O. (2004). Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research 1, 465–469. open url image1

Frantine-Silva, W., Sofia, S. H., Orsi, M. L., and Almeida, F. S. (2015). DNA barcoding of freshwater ichthyoplankton in the Neotropics as a tool for ecological monitoring. Molecular Ecology Resources 15, 1226–1237.
DNA barcoding of freshwater ichthyoplankton in the Neotropics as a tool for ecological monitoring.CrossRef | 1:CAS:528:DC%2BC2MXhtlSmtL3M&md5=725bbe19172df16cb09d873b9a4d86dfCAS | 25655460PubMed | open url image1

Fujita, M. K., Leach, A. D., Burbrink, F. T., McGuire, J. A., and Moritz, C. (2012). Coalescent-based species delimitation in an integrative taxonomy. Trends in Ecology & Evolution 27, 480–488.
Coalescent-based species delimitation in an integrative taxonomy.CrossRef | open url image1

Hebert, P. D. N., Cywinska, A., Ball, S. L., and DeWaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London – B. Biological Sciences 270, 313–321.
Biological identifications through DNA barcodes.CrossRef | 1:CAS:528:DC%2BD3sXktVWiu7g%3D&md5=b88e7363ce05476caedb06b7bd8886f2CAS | open url image1

Hubert, N., Espiau, B., Meyer, C., and Planes, S. (2015a). Identifying the ichthyoplankton of a coral reef using DNA barcodes. Molecular Ecology Resources 15, 57–67.
Identifying the ichthyoplankton of a coral reef using DNA barcodes.CrossRef | 1:CAS:528:DC%2BC2cXitFWlsrbE&md5=723f7565625e5c85016770586e764023CAS | 24935524PubMed | open url image1

Hubert, N., Kadarusman, , Wibowo, A., Busson, F., Caruso, D., Sulandari, S., Nafiqoh, N., Pouyaud, L., Rüber, L., Avarre, J. C., Herder, F., Hanner, R., Keith, P., and Hadiaty, R. K. (2015b). DNA barcoding Indonesian freshwater fishes: challenges and prospects. DNA Barcodes 3, 144–169.
DNA barcoding Indonesian freshwater fishes: challenges and prospects.CrossRef | open url image1

Ivanova, N. V., Zemlak, T. S., Hanner, R. H., and Hebert, P. D. N. (2007). Universal primer cocktails for fish DNA barcoding. Molecular Ecology Notes 7, 544–548.
Universal primer cocktails for fish DNA barcoding.CrossRef | 1:CAS:528:DC%2BD2sXpslOhtbo%3D&md5=0b55b5f016d9c155538bdf3c626af718CAS | open url image1

Kaat, A., and Joosten, H. (2008). ‘Fact Book for UNFCCC Policies on Peat Carbon Emissions.’ (Wetlands International: Wageningen, Netherlands.)

Kadarusman, , Hubert, N., Hadiaty, R. K., Sudarto, , Paradis, E., and Pouyaud, L. (2012). Cryptic diversity in Indo-Australian rainbowfishes revealed by DNA barcoding: implications for conservation in a biodiversity hotspot candidate. PLoS One 7, e40627.
Cryptic diversity in Indo-Australian rainbowfishes revealed by DNA barcoding: implications for conservation in a biodiversity hotspot candidate.CrossRef | 1:CAS:528:DC%2BC38XhtFSksb7F&md5=ab0c6fcf6e917d12ba866ab3e2453d50CAS | 22829879PubMed | open url image1

Ko, H.-L., Wang, Y.-T., Chiu, T.-S., Lee, M.-A., Leu, M.-Y., Chang, K.-Z., Chen, W.-Y., and Shao, K.-T. (2013). Evaluating the accuracy of morphological identification of larval fishes by applying DNA barcoding. PLoS One 8, e53451.
Evaluating the accuracy of morphological identification of larval fishes by applying DNA barcoding.CrossRef | 1:CAS:528:DC%2BC3sXis1ymsrc%3D&md5=0d0dcf3449afeed162e44e61854df0afCAS | 23382845PubMed | open url image1

Kochzius, M. (2009). Trends in fishery genetics. In ‘The Future of Fishery Science in North America’, 1st edn. (Eds R. Beamish and B. Rothschild.) Fish & Fisheries Series, pp. 453–493. (The Future of Fishery Science in North America, Springer Science + Business Media B.V.) https://doi.org/10.1007/978-1-4020-9210-7

Landi, M., Dimech, M., Arculeo, M., Biondo, G., Martins, R., and Carneiro, M. (2014). DNA barcoding for species assignment: the case of Mediterranean marine fishes. PLoS One 9, e106135.
DNA barcoding for species assignment: the case of Mediterranean marine fishes.CrossRef | 25222272PubMed | open url image1

Loh, W. K. W., Bond, P., Ashton, K. J., Roberts, D. T., and Tibbetts, I. R. (2014). DNA barcoding of freshwater fishes and the development of a quantitative qPCR assay for the species-specific detection and quantification of fish larvae from plankton samples. Journal of Fish Biology 85, 307–328.
DNA barcoding of freshwater fishes and the development of a quantitative qPCR assay for the species-specific detection and quantification of fish larvae from plankton samples.CrossRef | 1:CAS:528:DC%2BC2cXht1GitrnN&md5=11626dc4e93b8cc4e1d9092dcb48314fCAS | open url image1

Marshall, A. J., and Beehler, B. M. (2007). ‘The Ecology of Papua, Part Two.’ (Periplus Editions: Singapore.)

Miettinen, J., Shi, C., and Liew, S. C. (2011). Deforestation rates in insular Southeast Asia between 2000 and 2010. Global Change Biology 17, 2261–2270.
Deforestation rates in insular Southeast Asia between 2000 and 2010.CrossRef | open url image1

Monaghan, M. T., Wild, R., and Elliot, M. (2009). Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Systematic Biology 58, 298–311.
Accelerated species inventory on Madagascar using coalescent-based models of species delineation.CrossRef | 1:CAS:528:DC%2BD1MXht1Wqu7%2FO&md5=a8202400ccf4b918d9fd93eff1138c95CAS | 20525585PubMed | open url image1

Ng, P. K. L. (1994). Peat swamp fishes of Southeast Asia: diversity under threat. Wallaceana 73, 1–5. open url image1

Ng, P. K. L., Tay, J. B., Lim, K. K. P., and Yang, C. M. (1992). The conservation of the fish and other aquatic fauna of the north Selangor peat swamp forest and adjacent areas. Asian Wetland Bureau Publication number 81, World Wildlife Fund, Malaysia.

Ng, P. K. L., Tay, J. B., and Lim, K. K. P. (1994). Diversity and conservation of blackwater fishes in peninsular Malaysia, particularly in the north Selangor peat swamp forest. Hydrobiologia 285, 203–218.
Diversity and conservation of blackwater fishes in peninsular Malaysia, particularly in the north Selangor peat swamp forest.CrossRef | open url image1

Page, S. E., Hoscilo, A., Langner, A., Tansey, K., Siegert, F., Limin, S., and Rieley, J. O. (2009). Tropical peatland fires in Southeast Asia. In ‘Tropical Fire Ecology: Climate Change, Land Use and Ecosystem Dynamics’. (Ed. M. A. Cochrane.) pp. 263–287. (Springer: Berlin.)

Parish, F., Sirin, A., Charman, D., Joosten, H., Minayeva, T., Silvius, M., and Stringer, L. (2008). Assessment on peatlands, biodiversity and climate change: main report. Global Environment Centre, Kuala Lumpur and Wetlands International, Wageningen, Netherlands.

Pearce, F. (2007). The bog barons. New Scientist 2632, 50–53. open url image1

Pegg, G. G., Sinclair, B., Briskey, L., and Aspden, W. J. (2006). mtDNA barcode identification of fish larvae in the southern Great Barrier Reef, Australia. Scientia Marina 70, 7–12.
mtDNA barcode identification of fish larvae in the southern Great Barrier Reef, Australia.CrossRef | 1:CAS:528:DC%2BD28XhtlSlu77P&md5=a19d6d63407265c85e2b974a4e937298CAS | open url image1

Polhemus, D. A., England, R. A., and Allen, G. R. (2004). Freshwater biotas of New Guinea and nearby islands: analysis of endemism, richness, and threats. Bishop Museum Technical Report 31, Bishop Museum, Honolulu, HI.

Posa, M. R. C., Wijedasa, S. L. S., and Corlett, T. R. T. (2011). Biodiversity and conservation of tropical peat swamp forests. Bioscience 61, 49–57.
Biodiversity and conservation of tropical peat swamp forests.CrossRef | open url image1

Prentice, C., and Parish, D. (1990). Conservation of peat swamp forest: a forgotten ecosystem. In ‘In Harmony with Nature: Proceedings of the International Conference on Conservation of Tropical Biodiversity’, 12–16 June 1990, Kuala Lumpur, Malaysia. (Eds Y. S. Kheong and L. S. Win.) pp. 128–144. (FAO: Rome.)

Reynalte-Tataje, D. A., Nakatani, K., Fernandes, R., Agostinho, A. A., and Bialetzki, A. (2011). Temporal distribution of ichthyoplankton in the Ivinhema River (Mato Grosso do Sul State/Brazil): influence of environmental variables. Neotropical Ichthyology 9, 427–436.
Temporal distribution of ichthyoplankton in the Ivinhema River (Mato Grosso do Sul State/Brazil): influence of environmental variables.CrossRef | open url image1

Riedel, A., Sagata, K., Suhardjono, Y. R., Tänzler, R., and Balke, M. (2013). Integrative taxonomy on the fast track: towards more sustainability in biodiversity research. Frontiers in Zoology 10, 15.
Integrative taxonomy on the fast track: towards more sustainability in biodiversity research.CrossRef | 23537182PubMed | open url image1

Smith, P. E., and Richardson, S. L. (1977). Standard techniques for pelagic fish egg and larva surveys. Southwest Fisheries Center NMFS, NOM, US Department of Commerce, La Jolla, CA, USA, and Sally L. Richardson Department of Oceanography, Oregon State University, Corvallis, OR, USA.

Smith, A. M., Rodriguez, J. J., Whitfield, J. B., Deans, A. R., Janzen, D. H., Hallwachs, W., and Hebert, P. D. N. (2008). Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Proceedings of the National Academy of Sciences of the United States of America 105, 12359–12364.
Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections.CrossRef | 1:CAS:528:DC%2BD1cXhtVOhtrjN&md5=a1245d45274eb55cc72a7d1b2b01ee22CAS | open url image1

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). Mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
Mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.CrossRef | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=914d847cf771db39fd24019cd6b28bffCAS | 21546353PubMed | open url image1

Trivedi, S., Aloufi, A. A., Ansari, A. A., and Ghosh, S. K. (2016). Role of DNA barcoding in marine biodiversity assessment and conservation: an update. Saudi Journal of Biological Sciences 23, 161–171.
Role of DNA barcoding in marine biodiversity assessment and conservation: an update.CrossRef | 1:CAS:528:DC%2BC2MXhtVOksLY%3D&md5=1e003d7fe731efbdbced7e909a83dee8CAS | 26980996PubMed | open url image1

Valdez-Moreno, M. V., Asquez-Yeomans, L., Elıas-Gutierrez, M., Ivanova, N. V., and Hebert, P. D. N. (2010). Using DNA barcodes to connect adults and early life stages of marine fishes from the Yucatan Peninsula, Mexico: potential in fisheries management. Marine and Frewshwater Research 61, 655–671.
Using DNA barcodes to connect adults and early life stages of marine fishes from the Yucatan Peninsula, Mexico: potential in fisheries management.CrossRef | open url image1

Victor, B. C. (2007). Coryphopterus kuna, a new goby (Perciformes: Gobiidae: Gobinae) from the western Caribbean, with the identification of the late larval stage and an estimate of the pelagic larval duration. Zootaxa 1526, 51–61. open url image1

Ward, R. D., Zemlak, T. S., and Innes, B. H. (2005). DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 360, 1847–1857.
DNA barcoding Australia’s fish species.CrossRef | 1:CAS:528:DC%2BD2MXhtlSjsrjK&md5=e4118da0d630db8132a5c27238f82448CAS | 16214743PubMed | open url image1

Yoshino, K., Ishida, T., Nagano, T., and Setiawan, Y. (2010). Land cover pattern analysis of peat swamp lands in Southeast Asia. The International Archives of the Photogrammetry, Remote Sensing and Spatial Information Sciences 38, 941–946. open url image1

Yule, C. M. (2010). Loss of biodiversity and ecosystem functioning in Indo-Malayan peat swamp forests. Biodiversity and Conservation 19, 393–409.
Loss of biodiversity and ecosystem functioning in Indo-Malayan peat swamp forests.CrossRef | open url image1



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