Coral Reefs

, Volume 34, Issue 2, pp 383–392 | Cite as

Not finding Nemo: limited reef-scale retention in a coral reef fish

  • G. B. NanningaEmail author
  • P. Saenz-Agudelo
  • P. Zhan
  • I. Hoteit
  • M. L. Berumen


The spatial scale of larval dispersal is a key predictor of marine metapopulation dynamics and an important factor in the design of reserve networks. Over the past 15 yr, studies of larval dispersal in coral reef fishes have generated accumulating evidence of consistently high levels of self-recruitment and local retention at various spatial scales. These findings have, to a certain degree, created a paradigm shift toward the perception that large fractions of locally produced recruitment may be the rule rather than the exception. Here we examined the degree of localized settlement in an anemonefish, Amphiprion bicinctus, at a solitary coral reef in the central Red Sea by integrating estimates of self-recruitment obtained from genetic parentage analysis with predictions of local retention derived from a biophysical dispersal model parameterized with real-time physical forcing. Self-recruitment at the reef scale (c. 0.7 km2) was virtually absent during two consecutive January spawning events (1.4 % in 2012 and 0 % in 2013). Predicted levels of local retention at the reef scale varied temporally, but were comparatively low for both simulations (7 % in 2012 and 0 % in 2013). At the same time, the spatial scale of simulated dispersal was restricted to approximately 20 km from the source. Model predictions of reef-scale larval retention were highly dependent on biological parameters, underlining the need for further empirical validations of larval traits over a range of species. Overall, our findings present an urgent caution when assuming the potential for self-replenishment in small marine reserves.


Larval dispersal Self-recruitment Local retention Parentage analysis Biophysical model Red Sea 



We thank Glenn Almany, Simon Thorrold, Andrea Manica, and two anonymous reviewers for discussions and comments on earlier drafts of the paper; Maha Khalil for the preparation of reef charts and polygon files; and the numerous volunteers who assisted with fieldwork. Financial support was provided in part by KAUST baseline research funds (to MLB) and the Saudi-ARAMCO Marine Environmental Research Center.

Supplementary material

338_2015_1266_MOESM1_ESM.docx (1.1 mb)
Supplementary material 1 (DOCX 1081 kb)


  1. Ahlroth P, Alatalo RV, Suhonen J (2010) Reduced dispersal propensity in the wingless waterstrider Aquarius najas in a highly fragmented landscape. Oecologia 162:323–330CrossRefPubMedGoogle Scholar
  2. Almany GR, Webster MS (2006) The predation gauntlet: early post-settlement mortality in reef fishes. Coral Reefs 25:19–22CrossRefGoogle Scholar
  3. Almany GR, Berumen ML, Thorrold SR, Planes S, Jones GP (2007) Local replenishment of coral reef fish populations in a marine reserve. Science 316:742–744CrossRefPubMedGoogle Scholar
  4. Almany GR, Hamilton RJ, Bode M, Matawai M, Potuku T, Saenz-Agudelo P, Planes S, Berumen ML, Rhodes KL, Thorrold SR, Russ GR, Jones GP (2013) Dispersal of grouper larvae drives local resource sharing in a coral reef fishery. Curr Biol 23:626–630CrossRefPubMedGoogle Scholar
  5. Andutta FP, Kingsford MJ, Wolanski E (2012) “Sticky water” enables the retention of larvae in a reef mosaic. Estuar Coast Shelf Sci 101:54–63CrossRefGoogle Scholar
  6. Atema J, Kingsford MJ, Gerlach G (2002) Larval reef fish could use odour for detection, retention and orientation to reefs. Mar Ecol Prog Ser 241:151–160CrossRefGoogle Scholar
  7. Baguette M, Legrand D, Fréville H, Van Dyck H, Ducatez S (2012) Evolutionary ecology of dispersal in fragmented landscape. In: Clobert J, Baguette M, Benton TG, and Bullock JM (eds) Dispersal ecology and evolution. Oxford University Press, pp 381–391Google Scholar
  8. Baskett ML, Weitz JS, Levin SA (2007) The evolution of dispersal in reserve networks. Am Nat 170:59–78CrossRefPubMedGoogle Scholar
  9. Berumen ML, Almany GR, Planes S, Jones GP, Saenz-Agudelo P, Thorrold SR (2012) Persistence of self-recruitment and patterns of larval connectivity in a marine protected area network. Ecol Evol 2:444–452CrossRefPubMedCentralPubMedGoogle Scholar
  10. Bitume EV, Bonte D, Magalhães S, San Martin G, Van Dongen S, Bach F, Anderson JM, Olivieri I, Nieberding CM (2011) Heritability and artificial selection on ambulatory dispersal distance in Tetranychus urticae: effects of density and maternal effects. PLoS One 6:e26927CrossRefPubMedCentralPubMedGoogle Scholar
  11. Bonte D, Van Dyck H, Bullock JM, Coulon A, Delgado M, Gibbs M, Lehouck V, Matthysen E, Mustin K, Saastamoinen M, Schtickzelle N, Stevens VM, Vandewoestijne S, Baguette M, Barton K, Benton TG, Chaput-Bardy A, Clobert J, Dytham C, Hovestadt T, Meier CM, Palmer SCF, Turlure C, Travis JMJ (2012) Costs of dispersal. Biol Rev Camb Philos Soc 87:290–312CrossRefPubMedGoogle Scholar
  12. Botsford LW, White JW, Coffroth M, Paris CB, Planes S, Shearer TL, Thorrold SR, Jones GP (2009) Connectivity and resilience of coral reef metapopulations in marine protected areas: matching empirical efforts to predictive needs. Coral Reefs 28:327–337CrossRefPubMedCentralPubMedGoogle Scholar
  13. Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev Camb Philos Soc 80:205–225CrossRefPubMedGoogle Scholar
  14. Bowler DE, Benton TG (2011) Testing the interaction between environmental variation and dispersal strategy on population dynamics using a soil mite experimental system. Oecologia 166:111–119CrossRefPubMedGoogle Scholar
  15. Burgess SC, Nickols KJ, Griesemer CD, Barnett LAK, Dedrick AG, Satterthwaite EV, Yamane L, Morgan SG, White JW, Botsford LW (2014) Beyond connectivity: how empirical methods can quantify population persistence to improve marine protected-area design. Ecol Appl 24:257–270CrossRefPubMedGoogle Scholar
  16. Buston PM, D’Aloia CC (2013) Marine ecology: reaping the benefits of local dispersal. Curr Biol 23:R351–R353CrossRefPubMedGoogle Scholar
  17. Buston PM, Jones GP, Planes S, Thorrold SR (2011) Probability of successful larval dispersal declines fivefold over 1 km in a coral reef fish. Proc Biol Sci 279:1883–1888CrossRefPubMedCentralPubMedGoogle Scholar
  18. Caley MJ, Carr MH, Hixon MA, Hughes TP, Jones GP, Menge BA (1996) Recruitment and the local dynamics of open marine populations. Annu Rev Ecol Syst 27:477–500CrossRefGoogle Scholar
  19. Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Ann Rev Mar Sci 1:443–466CrossRefPubMedGoogle Scholar
  20. Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527CrossRefPubMedGoogle Scholar
  21. Cowen RK, Lwiza KMM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Science 287:857–859 Cowen RK, Paris C (2003) The role of long distance dispersal versus local retention in replenishing marine populations. Gulf Caribb 14:129–138Google Scholar
  22. Cowen R, Gawarkiewicz G, Pineda J, Thorrold S, Werner F (2007) Population connectivity in marine systems: an overview. Oceanography 20:14–21CrossRefGoogle Scholar
  23. Cuif M, Kaplan DM, Lefèvre J, Faure VM, Caillaud M, Verley P, Vigliola L, Lett C (2014) Wind-induced variability in larval retention in a coral reef system: a biophysical modelling study in the South-West Lagoon of New Caledonia. Prog Oceanogr 122:105–115CrossRefGoogle Scholar
  24. D’Aloia CC, Bogdanowicz SM, Majoris JE, Harrison RG, Buston PM (2013) Self-recruitment in a Caribbean reef fish: a method for approximating dispersal kernels accounting for seascape. Mol Ecol 22:2563–2572CrossRefPubMedGoogle Scholar
  25. Dee DP, Uppala SM, Simmons AJ, Berrisford P, Poli P, Kobayashi S, Andrae U, Balmaseda MA, Balsamo G, Bauer P (2011) The ERA-Interim reanalysis: Configuration and performance of the data assimilation system. Q J R Meteorol Soc 137:553–597CrossRefGoogle Scholar
  26. Dixson DL, Munday PL, Pratchett M, Jones GP (2011) Ontogenetic changes in responses to settlement cues by Anemonefish. Coral Reefs 30:903–910CrossRefGoogle Scholar
  27. Fisher R, Bellwood D (2002) The influence of swimming speed on sustained swimming performance of late-stage reef fish larvae. Mar Biol 140:801–807CrossRefGoogle Scholar
  28. Fisher R, Leis JM, Clark DL, Wilson SK (2005) Critical swimming speeds of late-stage coral reef fish larvae: variation within species, among species and between locations. Mar Biol 147:1201–1212CrossRefGoogle Scholar
  29. Gawarkiewicz G, Monismith S, Largier J (2007) Observing larval transport processes affecting population connectivity: progress and challenges. Oceanography 20:40–53CrossRefGoogle Scholar
  30. Gerber S, Chabrier P, Kremer A (2003) FAMOZ: a software for parentage analysis using dominant, codominant and uniparentally inherited markers. Mol Ecol Notes 3:479–481CrossRefGoogle Scholar
  31. Gerlach G, Atema J, Kingsford MJ, Black KP, Miller-Sims V (2007) Smelling home can prevent dispersal of reef fish larvae. Proc Natl Acad Sci 104:858–863CrossRefPubMedCentralPubMedGoogle Scholar
  32. Haag CR, Saastamoinen M, Marden JH, Hanski I (2005) A candidate locus for variation in dispersal rate in a butterfly metapopulation. Proc Biol Sci 272:2449–2456CrossRefPubMedCentralPubMedGoogle Scholar
  33. Hamilton SL (2008) Larval history influences post-metamorphic condition in a coral-reef fish. Oecologia 158:449–461CrossRefPubMedGoogle Scholar
  34. Harrison HB, Williamson DH, Evans RD, Almany GR, Thorrold SR, Russ GR, Feldheim K, van Herwerden L, Planes S, Srinivasan M, Berumen ML, Jones GP (2012) Larval export from marine reserves and the recruitment benefit for fish and fisheries. Curr Biol 22:1023–1028CrossRefPubMedGoogle Scholar
  35. Hixon MA (2011) 60 years of coral reef fish ecology: past, present, future. Bull Mar Sci 87:727–765CrossRefGoogle Scholar
  36. Huebert KB, Cowen RK, Sponaugle S (2011) Vertical migrations of reef fish larvae in the Straits of Florida and effects on larval transport. Limnol Oceanogr 56:1653–1666CrossRefGoogle Scholar
  37. Irisson J-O, Paris CB, Guigand C, Planesa S (2010) Vertical distribution and ontogenetic “migration” in coral reef fish larvae. Limnol Oceanogr 55:909–919CrossRefGoogle Scholar
  38. James MK, Armsworth PR, Mason LB, Bode L (2002) The structure of reef fish metapopulations: modelling larval dispersal and retention patterns. Proc R Soc London Ser B Biol Sci 269:2079–2086CrossRefGoogle Scholar
  39. Jones GP, Planes S, Thorrold SR (2005) Coral reef fish larvae settle close to home. Curr Biol 15:1314–1318CrossRefPubMedGoogle Scholar
  40. Jones GP, Milicich MJ, Emslie MJ, Lunow C (1999) Self-recruitment in a coral reef fish population. Nature 402:802–804CrossRefGoogle Scholar
  41. Jones GP, Almany GR, Russ GR, Sale PF, Steneck RS, Oppen MJH, Willis BL (2009) Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28:307–325CrossRefGoogle Scholar
  42. Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555CrossRefPubMedGoogle Scholar
  43. Lecchini D, Planes S, Galzin R (2005) Experimental assessment of sensory modalities of coral-reef fish larvae in the recognition of their settlement habitat. Behav Ecol Sociobiol 58:18–26CrossRefGoogle Scholar
  44. Marshall J, Adcroft A, Hill C, Perelman L, Heisey C (1997) A finite-volume, incompressible Navier Stokes model for studies of the ocean on parallel computers. J Geophys Res Ocean 102:5753–5766CrossRefGoogle Scholar
  45. Mora C, Sale PF (2002) Are populations of coral reef fish open or closed? Trends Ecol Evol 17:422–428CrossRefGoogle Scholar
  46. Nanninga GB, Berumen ML (2014) The role of individual variation in marine larval dispersal. Front Mar Sci. doi: 10.3389/fmars.2014.00071 Google Scholar
  47. Nanninga G, Mughal M, Saenz-Agudelo P, Bayer T, Berumen M (2012) Development of 35 novel microsatellite markers for the two-band anemonefish Amphiprion bicinctus. Conserv Genet Resour 5:515–518CrossRefGoogle Scholar
  48. Nosil P, Vines TH, Funk DJ (2005) Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59:705–719PubMedGoogle Scholar
  49. Paris CB, Cowen RK (2004) Direct evidence of a biophysical retention mechanism for coral reef fish larvae. Limnol Oceanogr 49:1964–1979CrossRefGoogle Scholar
  50. Paris CB, Chèrubin LM, Cowen RK (2007) Surfing, spinning, or diving from reef to reef: effects on population connectivity. Mar Ecol Prog Ser 347:285–300CrossRefGoogle Scholar
  51. Paris CB, Helgers J, Van Sebille E, Srinivasan A (2013) Connectivity Modeling System: A probabilistic modeling tool for the multi-scale tracking of biotic and abiotic variability in the ocean. Environ Model Softw 42:47–54CrossRefGoogle Scholar
  52. Patterson HM, Swearer SE (2007) Long-distance dispersal and local retention of larvae as mechanisms of recruitment in an island population of a coral reef fish. Austral Ecol 32:122–130CrossRefGoogle Scholar
  53. Patterson HM, Kingsford MJ, McCulloch MT (2005) Resolution of the early life history of a reef fish using otolith chemistry. Coral Reefs 24:222–229CrossRefGoogle Scholar
  54. Pineda J, Hare JA, Sponaungle S (2007) Larval transport and dispersal in the coastal ocean and consequences for population connectivity. Oceanography 20:22–39CrossRefGoogle Scholar
  55. Pinsky ML, Palumbi SR, Andréfouët S, Purkis SJ (2012) Open and closed seascapes: where does habitat patchiness create populations with high fractions of self-recruitment? Ecol Appl 22:1257–1267CrossRefPubMedGoogle Scholar
  56. Planes S, Jones GP, Thorrold SR (2009) Larval dispersal connects fish populations in a network of marine protected areas. Proc Natl Acad Sci 106:5693–5697CrossRefPubMedCentralPubMedGoogle Scholar
  57. Roberts CM (1997) Connectivity and management of Caribbean coral reefs. Science 278:1454–1457CrossRefPubMedGoogle Scholar
  58. Saenz-Agudelo P, Jones GP, Thorrold SR, Planes S (2011) Connectivity dominates larval replenishment in a coastal reef fish metapopulation. Proc R Soc B Biol Sci 278:2954–2961Google Scholar
  59. Saenz-Agudelo P, Jones GP, Thorrold SR, Planes S (2012) Patterns and persistence of larval retention and connectivity in a marine fish metapopulation. Mol Ecol 21:4695–4705CrossRefPubMedGoogle Scholar
  60. Schunter C, Pascual M, Garza JC, Raventos N, Macpherson E (2014) Kinship analyses identify fish dispersal events on a temperate coastline. Proc R Soc Lond B Biol Sci 281:20140556CrossRefGoogle Scholar
  61. Shulman M (1998) What can population genetics tell us about dispersal and biogeographic history of coral reef fishes? Aust J Ecol 23:216–225CrossRefGoogle Scholar
  62. Shulman M, Bermingham E (1995) Early life histories, ocean currents, and the population genetics of Caribbean reef fishes. Evolution 49:897–910CrossRefGoogle Scholar
  63. Sponaugle S, Cowen RK, Shanks A, Morgan SG, Leis JM, Pineda J, Boehlert GW, Kingsford MJ, Lindeman KC, Grimes C, Munro JL (2002) Predicting self-recruitment in marine populations: biophysical correlates and mechanisms. Bull Mar Sci 70:341–375Google Scholar
  64. Stobutzki IC, Bellwood DR (1994) An analysis of the sustained swimming abilities of pre-and post-settlement coral reef fishes. J Exp Mar Bio Ecol 175:275–286CrossRefGoogle Scholar
  65. Stobutzki IC, Bellwood DR (1997) Sustained swimming abilities of the late pelagic stages of coral reef fishes. Mar Ecol Prog Ser 149:35–41CrossRefGoogle Scholar
  66. Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402:799–802CrossRefGoogle Scholar
  67. Swearer SE, Shima JS, Hellberg ME, Thorrold SR, Jones GP, Robertson DR, Morgan SG, Selkoe KA, Ruiz GM, Warner RR (2002) Evidence of self-recruitment in demersal marine populations. Bull Mar Sci 70:251–271Google Scholar
  68. Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109CrossRefPubMedGoogle Scholar
  69. Tolimieri N, Jeffs A, Montgomery JC (2000) Ambient sound as a cue for navigation by the pelagic larvae of reef fishes. Mar Ecol Prog Ser 207:219–224CrossRefGoogle Scholar
  70. Treml EA, Roberts JJ, Chao Y, Halpin PN, Possingham HP, Riginos C (2012) Reproductive output and duration of the pelagic larval stage determine seascape-wide connectivity of marine populations. Integr Comp Biol 52:525–537CrossRefPubMedGoogle Scholar
  71. Tschirren B, Fitze PS, Richner H (2007) Maternal modulation of natal dispersal in a passerine bird: an adaptive strategy to cope with parasitism? Am Nat 169:87–93CrossRefPubMedGoogle Scholar
  72. Warner RR, Cowen RK (2002) Local retention of production in marine populations: evidence, mechanisms, and consequences. Bull Mar Sci 70:245–249Google Scholar
  73. Werner FE, Cowen RK, Paris CB (2007) Coupled biological and physical models: present capabilities and necessary developments for future studies of population connectivity. Oceanography 20:54–69CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • G. B. Nanninga
    • 1
    Email author
  • P. Saenz-Agudelo
    • 1
    • 3
  • P. Zhan
    • 2
  • I. Hoteit
    • 2
  • M. L. Berumen
    • 1
  1. 1.Red Sea Research CenterKing Abdullah University of Science and TechnologyThuwalSaudi Arabia
  2. 2.Earth Sciences and EngineeringKing Abdullah University of Science and TechnologyThuwalSaudi Arabia
  3. 3.Instituto de Ciencias Ambientales y EvolutivasUniversidad Austral de ChileValdiviaChile

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