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Larval fish dispersal in a coral-reef seascape

Nature Ecology & Evolution volume 1, Article number: 0148 (2017) Cite this article

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Abstract

Larval dispersal is a critical yet enigmatic process in the persistence and productivity of marine metapopulations. Empirical data on larval dispersal remain scarce, hindering the use of spatial management tools in efforts to sustain ocean biodiversity and fisheries. Here we document dispersal among subpopulations of clownfish (Amphiprion percula) and butterflyfish (Chaetodon vagabundus) from eight sites across a large seascape (10,000 km2) in Papua New Guinea across 2 years. Dispersal of clownfish was consistent between years, with mean observed dispersal distances of 15 km and 10 km in 2009 and 2011, respectively. A Laplacian statistical distribution (the dispersal kernel) predicted a mean dispersal distance of 13–19 km, with 90% of settlement occurring within 31–43 km. Mean dispersal distances were considerably greater (43–64 km) for butterflyfish, with kernels declining only gradually from spawning locations. We demonstrate that dispersal can be measured on spatial scales sufficient to inform the design of and test the performance of marine reserve networks.

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Figure 1: Network diagram of larval dispersal of two reef fish species among study sites within Kimbe Bay, Papua New Guinea.
Figure 2: Larval dispersal kernels for two reef fish species from Kimbe Bay, Papua New Guinea.
Figure 3: Larval connectivity matrices for A. percula in Kimbe Bay.

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References

  1. Botsford, L. W. et al. Connectivity, sustainability, and yield: bridging the gap between conventional fisheries management and marine protected areas. Rev. Fish. Biol. Fish. 19, 69–95 (2009).

    Article  Google Scholar 

  2. Kritzer, J. & Sale, P. F. Metapopulation ecology in the sea: from Levin’s model to marine ecology and fisheries science. Fish Fisheries 5, 131–140 (2004).

    Article  Google Scholar 

  3. Gell, F. R. & Roberts, C. M. Benefits beyond boundaries: the fishery effects of marine reserves. Trends Ecol. Evol. 18, 448–455 (2003).

    Article  Google Scholar 

  4. Sale, P. F. et al. Critical science gaps impede use of no-take marine reserves. Trends Ecol. Evol. 20, 74–80 (2005).

    Article  Google Scholar 

  5. Beger, M. et al. Incorporating asymmetric connectivity into spatial decision making for conservation. Cons. Lett. 3, 359–368 (2010).

    Article  Google Scholar 

  6. Magris, R. A., Pressey, R. L., Weeks, R. & Ban, N. C. Integrating connectivity and climate change into marine conservation planning. Biol. Cons. 170, 207–221 (2014).

    Article  Google Scholar 

  7. Roberts, C. M. Connectivity and management of Caribbean coral reefs. Science 278, 1454–1457 (1997).

    Article  CAS  Google Scholar 

  8. Cowen, R. K. & Sponaugle, S. Larval dispersal and marine population connectivity. Annu. Rev. Mar. Sci. 1, 443–466 (2009).

    Article  Google Scholar 

  9. Cowen, R. K., Paris, C. B. & Srinivasan, A. Scaling of connectivity in marine populations. Science 311, 522–527 (2006).

    Article  CAS  Google Scholar 

  10. Levin, L. A. Recent progress in understanding larval dispersal: new directions and digressions. Integr. Comp. Biol. 46, 282–297 (2006).

    Article  CAS  Google Scholar 

  11. Pinsky, M. L., Palumbi, S. R., Andrefouet, S. & Purkis, S. J. Open and closed seascapes: where does habitat patchiness create populations with high fractions of self-recruitment? Ecol. Applic. 22, 1257–1267 (2012).

    Article  Google Scholar 

  12. Lett, C., Nguyen-Huu, T., Cuif, M., Saenz-Agudelo, P. & Kaplan, D. M. Linking local retention, self-recruitment, and persistence in marine metapopulations. Ecology 96, 2236–2244 (2015).

    Article  Google Scholar 

  13. Burgess, S. C. et al. Beyond connectivity: how empirical methods can quantify population persistence to improve marine protected area design. Ecol. Appl. 24, 257–270 (2014).

    Article  Google Scholar 

  14. Simpson, S. D., Harrison, H. B., Claereboudt, M. R. & Planes, S. Long-distance dispersal via ocean currents connects clownfish populations throughout entire species range. PLoS ONE 9, e107610 (2014).

    Article  Google Scholar 

  15. Jones, G. P. et al. Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28, 307–325 (2009).

    Article  Google Scholar 

  16. Jones, G. P. in Ecology of Fishes on Coral Reefs: The Functioning of an Ecosystem in a Changing World (ed. Mora, C. ) 16–27 (Cambridge Univ. Press, 2015).

    Book  Google Scholar 

  17. Jones, G. P., Milicich, M. J., Emslie, M. J. & Lunow, C. Self-recruitment in a coral reef fish population. Nature 402, 802–804 (1999).

    Article  CAS  Google Scholar 

  18. Almany, G. R., Berumen, M. L., Thorrold, S. R., Planes, S. & Jones, G. P. Local replenishment of coral reef fish populations in a marine reserve. Science 316, 742–744 (2007).

    Article  CAS  Google Scholar 

  19. Jones, G. P., Thorrold, S. R. & Planes, S. Coral reef fish larvae settle close to home. Curr. Biol. 15, 1314–1318 (2005).

    Article  CAS  Google Scholar 

  20. Planes, S., Jones, G. P. & Thorrold, S. R. Larval dispersal connects fish populations in a network of marine protected areas. Proc. Natl Acad. Sci. USA 106, 5693–5697 (2009).

    Article  CAS  Google Scholar 

  21. Christie, M. R. et al. Larval connectivity in an effective network of marine protected areas. PLoS ONE 5, e15715 (2010).

    Article  CAS  Google Scholar 

  22. Berumen, M. L. et al. Persistence of self-recruitment and patterns of larval connectivity in a marine protected area network. Ecol. Evol. 2, 444–452 (2012).

    Article  Google Scholar 

  23. Saenz Agudelo, P., Jones, G. P., Thorrold, S. R. & Planes, S. Connectivity dominates larval replenishment in a coastal coral reef fish metapopulation. Proc. R. Soc. B. 278, 2954–2961 (2010).

    Article  Google Scholar 

  24. Harrison, H. B. et al. Larval export from marine reserves and the recruitment benefit for fish and fisheries. Curr. Biol. 22, 1023–1028 (2012).

    Article  CAS  Google Scholar 

  25. D’Aloia, C. C. et al. Patterns, causes, and consequences of marine larval dispersal. Proc. Natl Acad. Sci. USA 112, 13940–19945 (2015).

    Article  Google Scholar 

  26. Almany, G. R. et al. Dispersal of grouper larvae drives local resource sharing in a coral reef fishery. Curr. Biol. 23, 626–630 (2013).

    Article  CAS  Google Scholar 

  27. Bonin, M. C. et al. The role of marine reserves in the replenishment of a locally impacted population of anemonefish on the Great Barrier Reef. Mol. Ecol. 25, 487–499 (2016).

    Article  Google Scholar 

  28. Wabnitz, C ., Taylor, M ., Green, E & Razak, T. From Ocean to Aquarium: The Global Trade in Marine Ornamental Species (UNEP-WCMC, 2003).

    Google Scholar 

  29. Jones, G. P., McCormick, M. I., Srinivasan, M. & Eagle, J. V. Coral decline threatens fish biodiversity in marine reserves. Proc. Natl Acad. Sci. USA 101, 8251–8253 (2004).

    Article  CAS  Google Scholar 

  30. Green, A. et al. Designing a resilient network of marine protected areas for Kimbe Bay, Papua New Guinea. Oryx 43, 488–498 (2009).

    Article  Google Scholar 

  31. Gerber, S., Chabrier, P. & Kremer, A. Famoz: a software for parentage analysis using dominant, codominant and uniparentally inherited markers. Mol. Ecol. Notes 3, 479–481 (2003).

    Article  CAS  Google Scholar 

  32. Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742 (2007).

    Article  CAS  Google Scholar 

  33. Nanninga, G. B., Saenz-Agudelo, P., Zhan, P., Hoteit, I. & Berumen, M. L. Not finding Nemo: limited reef-scale retention in a coral reef fish. Coral Reefs 34, 383–392 (2015).

    Article  Google Scholar 

  34. Salles, O. C. et al. Coral reef populations can persist without immigration. Proc. R. Soc. B. 282, 2015131 (2015).

    Article  Google Scholar 

  35. Williamson, D. H. et al. Large-scale, multidirectional larval connectivity among coral reef fish populations in the Great Barrier Reef Marine Park. Mol. Ecol. 25, 6039–6054 (2016).

    Article  Google Scholar 

  36. Pinsky, M. L. et al. Marine dispersal scales are congruent over evolutionary and ecological time. Curr. Biol. 27, 1–6 (2017).

    Article  Google Scholar 

  37. Steinberg, C. R ., Choukroun, S. M ., Slivkoff, M. M ., Mahoney, M. V. & Brinkman, R. M. Currents in the Bismarck Sea and Kimbe Bay, Papua New Guinea. TNC Pacific Islands Countries Report 6/06 (Australian Institute of Marine Science/The Nature Conservancy, 2006).

  38. Lobel, P. S. & Robinson, A. R. Transport and entrainment of fish larvae by ocean mesoscale eddies and currents. Deep-Sea Res. 33, 483–500 (1986).

    Article  Google Scholar 

  39. Shulzitski, K., Sponaugle, S., Hauf, M., Walter, K. D. & Cowen, R. K. Encounter with mesoscale eddies enhances survival in larval coral reef fishes. Proc. Natl Acad. Sci. USA 113, 6928–6933 (2016).

    Article  CAS  Google Scholar 

  40. Gerlach, G., Atema, J., Kingsford, M. J., Black, K. P. & Miller-Sims, V. Smelling home can prevent dispersal of reef fish larvae. Proc. Natl Acad. Sci. USA 104, 858–863 (2007).

    Article  CAS  Google Scholar 

  41. Dixson, D. L. et al. Coral reef fish smell leaves to find island homes. Proc. R. Soc. B 275, 2831–2839 (2008).

    Article  Google Scholar 

  42. Berumen, M. L. et al. Otolith geochemistry does not reflect dispersal history of clownfish larvae. Coral Reefs 29, 883–891 (2010).

    Article  Google Scholar 

  43. Lester, S. E. et al. Biological effects within no-take reserves: a global synthesis. Mar. Ecol. Prog. Ser. 384, 33–46 (2009).

    Article  Google Scholar 

  44. Emslie, M. J. et al. Expectation and outcomes of reserve network performance following re-zoning of the Great Barrier Reef Park. Curr. Biol. 25, 983–992 (2015).

    Article  CAS  Google Scholar 

  45. Cowen, R. K., Gawarkiewicz, G., Pineda, J., Thorrold, S. R. & Werner, F. E. Population connectivity in marine systems: an overview. Oceanography 20, 14–21 (2009).

    Article  Google Scholar 

  46. Kaplan, D. M., Botsford, L. W. & Jorgensen, S. Dispersal-per-recruit: an efficient method for assessing sustainability in networks of marine reserves. Ecol. Appl. 16, 2248–2263 (2006).

    Article  Google Scholar 

  47. Almany, G. R. Marine ecology: reserves are necessary, but not sufficient. Curr. Biol. 25, R328–R347 (1998).

    Article  Google Scholar 

  48. Harrison, H. B., Saenz-Agudelo, P., Planes, S., Jones, G. P. & Berumen, M. L. Relative accuracy of three common methods of parentage analysis in natural populations. Mol. Ecol. 22, 1158–1170 (2013).

    Article  Google Scholar 

  49. McCormick, M. I. & Choat, J. H. Estimating total abundance of a large temperate reef fish using visual strip-transects. Mar. Biol. 96, 469–478 (1987).

    Article  Google Scholar 

Download references

Acknowledgements

We thank the volunteers who dedicated long hours in the water collecting tissue samples: R. Brooker, S. Choukroun, P. Costello, J. Davies, D. Dixson, K. Furby, M. Giru, B. Grover, J. Hill, N. Jones, K. McMahon, M. Noble, S. Noonan, N. Raventos Klein, M. Pinsky, J. Roberts, J. Smith, N. Tolou, M. Takahashi, P. Waldie and M. White; and the people of the villages on the shores of Kimbe Bay who welcomed us into their communities and supported this research: Kilu-Tamare, Lolobau, Tairobe and Vaiaku. This research would not have been possible without the support of the Walindi Plantation Resort, the skipper and crew of MV Febrina, Mahonia Na Dari Research and Conservation Centre, and The Nature Conservancy. This work was supported by Australian Research Council funding to G.P.J., the King Abdullah University of Science and Technology (baseline research funds to M.L.B. and a Special Partnership Collaborative Fellowship to M.L.B. and P.S.-A.) and NSF grants OCE0928442 and OCE1031256 to S.R.T.

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Author notes

  1. Glenn R. Almany: Deceased.

Authors and Affiliations

  1. Laboratoire d’Excellence CORAIL EPHE, PSL Research University, UPVD, CNRS, USR 3278 CRIOBE, BP 1013, 98729 Papetoai, Moorea, French Polynesia

    Glenn R. Almany, Serge Planes & Pablo Saenz-Agudelo

  2. Biology Department, Woods Hole Oceanographic Institution, Woods Hole, 02543, Massachusetts, USA

    Simon R. Thorrold

  3. Division of Biological and Environmental Science and Engineering, Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, 23955, Saudi Arabia

    Michael L. Berumen, Pablo Saenz-Agudelo, Gerrit B. Nanninga, Mark A. Priest & Tane Sinclair-Taylor

  4. ARC Centre of Excellence for Environmental Decisions, School of BioSciences, University of Melbourne, Parkville, Melbourne, 3010, Victoria, Australia

    Michael Bode

  5. Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Chile

    Pablo Saenz-Agudelo

  6. ARC Centre of Excellence for Coral Reef Studies, and College of Science and Engineering, James Cook University, Townsville, 4811, Queensland, Australia

    Mary C. Bonin, Ashley J. Frisch, Hugo B. Harrison, Vanessa Messmer, Maya Srinivasan, David H. Williamson & Geoffrey P. Jones

  7. Reef HQ, Great Barrier Reef Marine Park Authority, Townsville, 4810, Queensland, Australia

    Ashley J. Frisch

  8. Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK

    Gerrit B. Nanninga

  9. Marine Spatial Ecology Lab, School of Biological Sciences, University of Queensland, 4072, Queensland, Australia

    Mark A. Priest

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  1. Glenn R. Almany
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Contributions

G.R.A., M.L.B., G.P.J., S.P. and S.R.T designed the study. All authors contributed to field work and editing of the manuscript. M.B., H.B.H., S.P., M.A.P., P.S.-A. and S.P. conducted microsatellite DNA analyses. G.R.A. and M.B. developed the dispersal kernel model. M.B., H.H. and S.R.T. created figures.

Corresponding author

Correspondence to Simon R. Thorrold.

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The authors declare no competing financial interests.

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Supplementary Information

Supplementary Tables 1–6; Supplementary Figures 1,2; Supplementary Methods (PDF 618 kb)

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Almany, G., Planes, S., Thorrold, S. et al. Larval fish dispersal in a coral-reef seascape. Nat Ecol Evol 1, 0148 (2017). https://doi.org/10.1038/s41559-017-0148

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