Article

Larval fish dispersal in a coral-reef seascape

  • Nature Ecology & Evolution 1, Article number: 0148 (2017)
  • doi:10.1038/s41559-017-0148
  • Download Citation
Received:
Accepted:
Published online:

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.

  • Subscribe to Nature Ecology & Evolution for full access:

    $99

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    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).

  2. 2.

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

  3. 3.

    & Benefits beyond boundaries: the fishery effects of marine reserves. Trends Ecol. Evol. 18, 448–455 (2003).

  4. 4.

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

  5. 5.

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

  6. 6.

    , , & Integrating connectivity and climate change into marine conservation planning. Biol. Cons. 170, 207–221 (2014).

  7. 7.

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

  8. 8.

    & Larval dispersal and marine population connectivity. Annu. Rev. Mar. Sci. 1, 443–466 (2009).

  9. 9.

    , & Scaling of connectivity in marine populations. Science 311, 522–527 (2006).

  10. 10.

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

  11. 11.

    , , & Open and closed seascapes: where does habitat patchiness create populations with high fractions of self-recruitment? Ecol. Applic. 22, 1257–1267 (2012).

  12. 12.

    , , , & Linking local retention, self-recruitment, and persistence in marine metapopulations. Ecology 96, 2236–2244 (2015).

  13. 13.

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

  14. 14.

    , , & Long-distance dispersal via ocean currents connects clownfish populations throughout entire species range. PLoS ONE 9, e107610 (2014).

  15. 15.

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

  16. 16.

    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).

  17. 17.

    , , & Self-recruitment in a coral reef fish population. Nature 402, 802–804 (1999).

  18. 18.

    , , , & Local replenishment of coral reef fish populations in a marine reserve. Science 316, 742–744 (2007).

  19. 19.

    , & Coral reef fish larvae settle close to home. Curr. Biol. 15, 1314–1318 (2005).

  20. 20.

    , & Larval dispersal connects fish populations in a network of marine protected areas. Proc. Natl Acad. Sci. USA 106, 5693–5697 (2009).

  21. 21.

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

  22. 22.

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

  23. 23.

    , , & Connectivity dominates larval replenishment in a coastal coral reef fish metapopulation. Proc. R. Soc. B. 278, 2954–2961 (2010).

  24. 24.

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

  25. 25.

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

  26. 26.

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

  27. 27.

    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).

  28. 28.

    ., ., & From Ocean to Aquarium: The Global Trade in Marine Ornamental Species (UNEP-WCMC, 2003).

  29. 29.

    , , & Coral decline threatens fish biodiversity in marine reserves. Proc. Natl Acad. Sci. USA 101, 8251–8253 (2004).

  30. 30.

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

  31. 31.

    , & Famoz: a software for parentage analysis using dominant, codominant and uniparentally inherited markers. Mol. Ecol. Notes 3, 479–481 (2003).

  32. 32.

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

  33. 33.

    , , , & Not finding Nemo: limited reef-scale retention in a coral reef fish. Coral Reefs 34, 383–392 (2015).

  34. 34.

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

  35. 35.

    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).

  36. 36.

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

  37. 37.

    ., ., ., & 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. 38.

    & Transport and entrainment of fish larvae by ocean mesoscale eddies and currents. Deep-Sea Res. 33, 483–500 (1986).

  39. 39.

    , , , & Encounter with mesoscale eddies enhances survival in larval coral reef fishes. Proc. Natl Acad. Sci. USA 113, 6928–6933 (2016).

  40. 40.

    , , , & Smelling home can prevent dispersal of reef fish larvae. Proc. Natl Acad. Sci. USA 104, 858–863 (2007).

  41. 41.

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

  42. 42.

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

  43. 43.

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

  44. 44.

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

  45. 45.

    , , , & Population connectivity in marine systems: an overview. Oceanography 20, 14–21 (2009).

  46. 46.

    , & Dispersal-per-recruit: an efficient method for assessing sustainability in networks of marine reserves. Ecol. Appl. 16, 2248–2263 (2006).

  47. 47.

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

  48. 48.

    , , , & Relative accuracy of three common methods of parentage analysis in natural populations. Mol. Ecol. 22, 1158–1170 (2013).

  49. 49.

    & Estimating total abundance of a large temperate reef fish using visual strip-transects. Mar. Biol. 96, 469–478 (1987).

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.

Author information

Author notes

    • Glenn R. Almany

    Deceased.

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, Massachusetts 02543, USA.

    • Simon R. Thorrold
  3. Red Sea Research Center, Division of Biological and Environmental Science and Engineering, 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, Victoria 3010, 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, Queensland 4811, 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, Queensland 4810, 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, Queensland 4072, Australia.

    • Mark A. Priest

Authors

  1. Search for Glenn R. Almany in:

  2. Search for Serge Planes in:

  3. Search for Simon R. Thorrold in:

  4. Search for Michael L. Berumen in:

  5. Search for Michael Bode in:

  6. Search for Pablo Saenz-Agudelo in:

  7. Search for Mary C. Bonin in:

  8. Search for Ashley J. Frisch in:

  9. Search for Hugo B. Harrison in:

  10. Search for Vanessa Messmer in:

  11. Search for Gerrit B. Nanninga in:

  12. Search for Mark A. Priest in:

  13. Search for Maya Srinivasan in:

  14. Search for Tane Sinclair-Taylor in:

  15. Search for David H. Williamson in:

  16. Search for Geoffrey P. Jones in:

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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Simon R. Thorrold.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Tables 1–6; Supplementary Figures 1,2; Supplementary Methods