Population connectivity of neon damsel, Pomacentrus coelestis, inferred from otolith microchemistry and mtDNA
Shang-Yin Vanson Liu A , Chia-Hui Wang B , Jen-Chieh Shiao A and Chang-Feng Dai A C
+ Author Affiliations
- Author Affiliations
A Institute of Oceanography, National Taiwan University, Taipei, Taiwan 10617,Republic of China.
B Department of Environmental Biology and Fisheries Science, National Taiwan Ocean University, Keelung, Taiwan 20224, Republic of China.
C Corresponding author. Email: corallab@ntu.edu.tw
Marine and Freshwater Research 61(12) 1416-1424 https://doi.org/10.1071/MF10079
Submitted: 24 March 2010 Accepted: 7 August 2010 Published: 13 December 2010
Abstract
Understanding dispersal patterns and population connectivity is crucial to the conservation and management of fish assemblages in reef ecosystems. To reveal the population connectivity of reef fishes in the northern West Pacific, we examined the otolith chemistry and the mtDNA control region of Pomacentrus coelestis collected from six localities between Hainan Island (China) and Okinawa (Japan). The results of otolith chemistry analyses on pre-settlement signatures showed that fishes in north-west Taiwan may have a similar origin, whereas those in southern Taiwan might have a separate origin from the South China Sea. Furthermore, the elemental ratios of post-settlement signatures showed clear separation among localities, reflecting their sedentary behaviour after settlement and the influence of local environment. Population genetic analyses revealed that significant genetic differentiation occurred between populations in north-west Taiwan and populations in the South China Sea and the Kuroshio ecosystems. This study demonstrated that otolith chemistry and mtDNA analyses revealed consistent and complementary results of the dispersal and connectivity of P. coelestis populations, and provided evidence supporting that fish populations around Taiwan should be considered as two stocks. Thus, two marine protected area networks should be established for the conservation and management of reef fishes in this area.
Additional keywords: gene flow, marine protected areas, mtDNA, Neon damselfish, otolith microchemistry, population connectivity.
References
Allen, G. R. (1991). ‘Damselfishes of the World.’ (Mergus Publishers: Melle.)Ashford, J. R., Arkhipkin, A. I., and Jones, C. M. (2006). Can the chemistry of otolith nuclei determine population structure of Patagonian toothfish Dissostichus eleginoides? Journal of Fish Biology 69, 708–721.
| Can the chemistry of otolith nuclei determine population structure of Patagonian toothfish Dissostichus eleginoides?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFamtLrP&md5=997e749d552cc6c2fd57c3fbee9991c2CAS |
Bainbridge, Z. T., Brodie, J. E., Faithful, J. W., Sydes, D. A., and Lewis, S. E. (2009). Identifying the land-based sources of suspended sediments, nutrients and pesticides discharged to the Great Barrier Reef from the Tully–Murray Basin, Queensland, Australia. Marine and Freshwater Research 60, 1081–1090.
| Identifying the land-based sources of suspended sediments, nutrients and pesticides discharged to the Great Barrier Reef from the Tully–Murray Basin, Queensland, Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVWqtL3N&md5=62d3ad65dd17145b86aec2869f8e6a72CAS |
Campana, S. E. (1999). Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Marine Ecology Progress Series 188, 263–297.
| Chemistry and composition of fish otoliths: pathways, mechanisms and applications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtFKmtA%3D%3D&md5=351807662fcd172d51ae8119a535e579CAS |
Chen, C. A. (1999). Analysis of scleractinian distribution in Taiwan indicating a pattern congruent with sea surface temperatures and currents: examples from Acropora and Faviidae corals. Zoological Studies 38, 119–129..
Christie, M. R., Johnson, D. W., Stallings, C. D., and Hixon, M. A. (2010). Self-recruitment and sweepstakes reproduction amid extensive gene flow in a coral-reef fish. Molecular Ecology 19, 1042–1057.
| Self-recruitment and sweepstakes reproduction amid extensive gene flow in a coral-reef fish.Crossref | GoogleScholarGoogle Scholar | 20089121PubMed |
Clarke, L. M., Walther, B. D., Munch, S. B., Thorrold, S. R., and Conover, D. O. (2009). Chemical signatures in the otoliths of a coastal marine fish, Menidia menidia, from the northeastern United States: spatial and temporal differences. Marine Ecology Progress Series 384, 261–271.
| Chemical signatures in the otoliths of a coastal marine fish, Menidia menidia, from the northeastern United States: spatial and temporal differences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosl2jtLY%3D&md5=2636f20dad24814d58f0da894310526bCAS |
Cook, B. D., Bunn, S. E., and Hughes, J. M. (2007). Molecular genetic and stable isotope signatures reveal complementary patterns of population connectivity in the regionally vulnerable southern pygmy perch (Nannoperca australis). Biological Conservation 138, 60–72.
| Molecular genetic and stable isotope signatures reveal complementary patterns of population connectivity in the regionally vulnerable southern pygmy perch (Nannoperca australis).Crossref | GoogleScholarGoogle Scholar |
Cowen, R. K., and Sponaugle, S. (2009). Larval dispersal and marine population connectivity. Annual Review of Materials Science 1, 443–466.
| Larval dispersal and marine population connectivity.Crossref | GoogleScholarGoogle Scholar |
Cowen, R. K., Paris, C. B., and Srinivasan, A. (2006). Scaling of connectivity in marine populations. Science 311, 522–527.
| Scaling of connectivity in marine populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmvVymtg%3D%3D&md5=d44a442a682c6697fe0c967984bc8fbbCAS | 16357224PubMed |
Elsdon, T. S., and Gillanders, B. M. (2004). Fish otolith chemistry influenced by exposure to multiple environmental variables. Journal of Experimental Marine Biology and Ecology 313, 269–284.
| Fish otolith chemistry influenced by exposure to multiple environmental variables.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpslGmur4%3D&md5=b8ca46beb601f8028da835455f03745cCAS |
Excoffier, L., Smouse, P. E., and Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application of human mitochondrial DNA restriction data. Genetics 131, 479–491..
| 1:CAS:528:DyaK38XlsVCntro%3D&md5=bcf0104f9e068f3bc18f11bee6e4bfaeCAS | 1644282PubMed |
Excoffier, L., Laval, G., and Schneider, S. (2005). Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50..
| 1:CAS:528:DC%2BD28XjsFSltg%3D%3D&md5=eed1ab2526c3755e0be15b2cf5ce4123CAS | 19325852PubMed |
Feyrer, F., Hobbs, J., Baerwald, M., Sommer, T., Yin, Q. Z., Clark, K., May, B., and Bennett, W. (2007). Otolith microchemistry provides information complementary to microsatellite DNA for a migratory fish. Transactions of the American Fisheries Society 136, 469–476.
| Otolith microchemistry provides information complementary to microsatellite DNA for a migratory fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvVOkurw%3D&md5=1117f6d67f36fafea46e928f642e5965CAS |
Fu, Y. X. (1996). New statistical tests for DNA samples from a population. Genetics 143, 557–570..
| 1:CAS:528:DyaK28XjtVKjsL0%3D&md5=3fa9e8d9731adfe454327ced0a7b56d9CAS | 8722804PubMed |
Fu, Y. X., and Li, W. H. (1993). Statistical tests of neutrality of mutation. Genetics 133, 693–709..
| 1:STN:280:DyaK3s3gt1Crsw%3D%3D&md5=c93a02192b6406f2be83d97370316c44CAS | 8454210PubMed |
Hedgecock, D., Barber, P. H., and Edmands, S. (2007). Genetic approaches to measuring connectivity. Oceanography (Washington, D.C.) 20, 22–31..
Irisson, J. O., LeVan, A., De Lara, M., and Planes, S. (2004). Strategies and trajectories of coral reef fish larvae optimizing self-recruitment. Journal of Theoretical Biology 227, 205–218.
| Strategies and trajectories of coral reef fish larvae optimizing self-recruitment.Crossref | GoogleScholarGoogle Scholar | 14990385PubMed |
Jan, S., Sheu, D. D., and Kuo, H. M. (2006). Water mass and throughflow transport variability in the Taiwan Strait. Journal of Geophysical Research C 111, C12012.
| Water mass and throughflow transport variability in the Taiwan Strait.Crossref | GoogleScholarGoogle Scholar |
Jones, G. P., Almany, G. R., Russ, G. R., Sale, P. F., Steneck, R. S., Van Oppen, M. J. H., and Willis, B. L. (2009). Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28, 307–325.
| Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges.Crossref | GoogleScholarGoogle Scholar |
Kingsford, M. J., Hughes, J. M., and Patterson, H. M. (2009). Otolith chemistry of the non-dispersing reef fish Acanthochromis polyacanthus: cross-shelf patterns from the central Great Barrier Reef. Marine Ecology Progress Series 377, 279–288.
| Otolith chemistry of the non-dispersing reef fish Acanthochromis polyacanthus: cross-shelf patterns from the central Great Barrier Reef.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXks1Olu78%3D&md5=1e99195ec706d4766e7a1543d0463303CAS |
Lee, W. J., Conroy, J., Howell, W. H., and Kocher, T. D. (1995). Structure and evolution of teleost mitochondrial control regions. Journal of Molecular Evolution 41, 54–66.
| Structure and evolution of teleost mitochondrial control regions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmt1yktrw%3D&md5=455d0babaffc60cc438b558deb232e6dCAS | 7608989PubMed |
Lee, H. J., Chao, S. Y., Fan, K. L., Wang, Y. H., and Liang, N. K. (1997). Tidally induced upwelling in a semi-enclosed basin: Nan Wan Bay. Journal of Oceanography 53, 467–480..
Leis, J. M., Piola, R. F., Hay, A. C., Wen, C., and Kan, K.-P. (2009). Ontogeny of behaviour relevant to dispersal and connectivity in the larvae of two non-reef demersal, tropical fish species. Marine and Freshwater Research 60, 211–223.
| Ontogeny of behaviour relevant to dispersal and connectivity in the larvae of two non-reef demersal, tropical fish species.Crossref | GoogleScholarGoogle Scholar |
Liu, S. Y. V., Kokita, T., and Dai, C. F. (2008). Population genetic structure of the neon damselfish (Pomacentrus coelestis) in the northwestern Pacific Ocean. Marine Biology 154, 745–753.
| Population genetic structure of the neon damselfish (Pomacentrus coelestis) in the northwestern Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |
Lo-Yat, A., Meekan, M., Munksgaard, N., Parry, D., Planes, S., Wolter, M., and Carleton, J. (2005). Small-scale spatial variation in the elemental composition of otoliths of Stegastes nigricans (Pomacentridae) in French Polynesia. Coral Reefs 24, 646–653.
| Small-scale spatial variation in the elemental composition of otoliths of Stegastes nigricans (Pomacentridae) in French Polynesia.Crossref | GoogleScholarGoogle Scholar |
Miller, J. A., Bank, M. A., Gomez-Uchida, D., and Shanks, A. L. (2005). A comparison of population structure in black rockfish (Sebastes melanops) as determined with otolith microchemistry and microsatellite DNA. Canadian Journal of Fisheries and Aquatic Sciences 62, 2189–2198.
| A comparison of population structure in black rockfish (Sebastes melanops) as determined with otolith microchemistry and microsatellite DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlWmtr3J&md5=7a5cb5d8be8e0f24af521194144037d8CAS |
Mora, C., and Sale, P. E. (2002). Are populations of coral reef fish open or closed? Trends in Ecology & Evolution 17, 422–428.
| Are populations of coral reef fish open or closed?Crossref | GoogleScholarGoogle Scholar |
Palumbi, S. R. (2003). Population genetics, demographic connectivity, and the design of marine reserves. Ecological Applications 13, 146–158.
| Population genetics, demographic connectivity, and the design of marine reserves.Crossref | GoogleScholarGoogle Scholar |
Palumbi, S. R. (2004). Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Annual Review of Environment and Resources 29, 31–68.
| Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management.Crossref | GoogleScholarGoogle Scholar |
Patterson, H. M., Kingsford, M. J., and McCulloch, M. T. (2004). Elemental signatures of Pomacentrus coelestis otoliths at multiple spatial scales on the Great Barrier Reef, Australia. Marine Ecology Progress Series 270, 229–239.
| Elemental signatures of Pomacentrus coelestis otoliths at multiple spatial scales on the Great Barrier Reef, Australia.Crossref | GoogleScholarGoogle Scholar |
Patterson, H. M., Kingsford, M. J., and McCulloch, M. T. (2005). Resolution of the early life of a reef fish using otolith chemistry. Coral Reefs 24, 222–229.
| Resolution of the early life of a reef fish using otolith chemistry.Crossref | GoogleScholarGoogle Scholar |
Planes, S., Jones, G. P., and Thorrold, S. R. (2009). Larval dispersal connects fish populations in a network of marine protected areas. Proceedings of the National Academy of Sciences of the United States of America 106, 5693–5697.
| Larval dispersal connects fish populations in a network of marine protected areas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkvFOns70%3D&md5=ace1f9805bfa95e2564f5f777e8dbea1CAS | 19307588PubMed |
Rocha, L. A., Craig, M. T., and Bowen, B. W. (2007). Phylogeography and the conservation of coral reef fishes. Coral Reefs 26, 501–512.
| Phylogeography and the conservation of coral reef fishes.Crossref | GoogleScholarGoogle Scholar |
Ruttenberg, B. I., Hamilton, S. L., Hickford, M. J. H., Paradis, G. L., Sheehy, M. S., Standish, J. D., Ofer, B.-T., and Warner, R. R. (2005). Elevated levels of trace elements in core of otoliths and their potential for use as natural tags. Marine Ecology Progress Series 297, 273–281.
| Elevated levels of trace elements in core of otoliths and their potential for use as natural tags.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFeltrrO&md5=013c7957e0f87bdf1c30dfb1eb083f9aCAS |
Shao, K. T., Chen, J. P., and Wang, S. C. (1999). Biogeography and database of marine fishes in Taiwan waters. In ‘Proceedings of 5th Indo-Pacific Fish Conference, Noumea – New Caledonia, 3–8 November 1997’. (Eds B. Séret and J. Y. Sire.) pp. 673–680. (French Society of Ichthyology: Paris.)
Standish, J. D., Sheehy, M., and Warner, R. R. (2008). Use of otolith natal elemental signatures as natural tags to evaluate connectivity among open-coast fish populations. Marine Ecology Progress Series 356, 259–268.
| Use of otolith natal elemental signatures as natural tags to evaluate connectivity among open-coast fish populations.Crossref | GoogleScholarGoogle Scholar |
StatSoft Inc. (2003). ‘STATISTICA (Version 6).’ Available at http://www.statsoft.com [Verified 26 August 2010].
Tanaka, Y, and Nitta, M. (1997). Reproduction and rearing of damselfish, Pomacentrus coelestis, in the aquarium. Bulletin of Institute of Oceanic Research and Development. Tokai University 18, 51–62.
Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
| CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitlSgu74%3D&md5=028950b6ecdb3b8d9171fc36ff4c4037CAS | 7984417PubMed |
Thresher, R. E., Colin, P. L., and Bell, L. J. (1989). Planktonic duration, distribution and population structure of western and central Pacific damselfishes (Pomacentridae). Copeia 1989, 420–434.
| Planktonic duration, distribution and population structure of western and central Pacific damselfishes (Pomacentridae).Crossref | GoogleScholarGoogle Scholar |
Wang, C. H., Shao, J. C., You, C. F., and Tzeng, W. N. (2009). Spatio-temporal variation in the elemental compositions of otoliths of southern bluefin tuna Thunnus maccoyii in the Indian Ocean and its ecological implication. Journal of Fish Biology 75, 1173–1193.
| Spatio-temporal variation in the elemental compositions of otoliths of southern bluefin tuna Thunnus maccoyii in the Indian Ocean and its ecological implication.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1SltbfL&md5=a419f29654c600ea48576d6815df50a3CAS | 20738607PubMed |
Wilson, D. T., and McCormick, M. I. (1999). Microstructure of settlement-marks in the otoliths of tropical reef fishes. Marine Biology 134, 29–41.
| Microstructure of settlement-marks in the otoliths of tropical reef fishes.Crossref | GoogleScholarGoogle Scholar |
Worm, B., Barbier, E. B., Beaumont, N., Duffy, J. E., Folke, C., Halpern, B. S., Jackson, J. B. C., Lotzke, H. K., Micheli, F., Palumbi, S. R., Sala, E., Selkoe, K. A., Stachowicz, J. J., and Watson, R. (2006). Impacts of biodiversity loss on ocean ecosystem services. Science 314, 787–790.
| Impacts of biodiversity loss on ocean ecosystem services.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFKit73J&md5=b04532f5e5725a8488be9e3a70620ff2CAS | 17082450PubMed |
Yu, J. K., Wang, H. Y., Lee, S. C., and Dai, C. F. (1999). Genetic structure of a scleractinian coral, Mycedium elephantotus, in Taiwan. Marine Biology 133, 21–28.
| Genetic structure of a scleractinian coral, Mycedium elephantotus, in Taiwan.Crossref | GoogleScholarGoogle Scholar |
