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Population connectivity and the effectiveness of marine protected areas to protect vulnerable, exploited and endemic coral reef fishes at an endemic hotspot

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Abstract

Marine protected areas (MPAs) aim to mitigate anthropogenic impacts by conserving biodiversity and preventing overfishing. The effectiveness of MPAs depends on population connectivity patterns between protected and non-protected areas. Remote islands are endemism hotspots for coral reef fishes and provide rare examples of coral reefs with limited fishing pressure. This study explored population genetic connectivity across a network of protected and non-protected areas for the endemic wrasse, Coris bulbifrons, which is listed as “vulnerable” by the IUCN due to its small, decreasing geographic range and declining abundance. Mitochondrial DNA (mtDNA) and microsatellite DNA (msatDNA) markers were used to estimate historic and contemporary gene flow to determine the level of population self-replenishment and to measure genetic and genotypic diversity among all four locations in the species range (south-west Pacific Ocean)—Middleton Reef (MR), Elizabeth Reef (ER), Lord Howe Island (LHI) and Norfolk Island (NI). MPAs exist at MR and LHI and are limited or non-existent at ER and NI, respectively. There was no obvious differentiation in mtDNA among locations, however, msatDNA revealed differentiation between the most peripheral (NI) and all remaining locations (MR, ER and LHI). Despite high mtDNA connectivity (M = 259–1,144), msatDNA connectivity was limited (M = 3–9) with high self-replenishment (68–93 %) at all locations. NI is the least connected and heavily reliant on self-replenishment, and the absence of MPAs at NI needs to be rectified to ensure the persistence of endemic species at this location. Other endemic fishes exhibit similar patterns of high self-replenishment across the four locations, indicating that a single spatial management approach consisting of a MPA network protecting part of each location could provide reasonable protection for these species. Thus, the existing network of MPAs at this endemic hotspot appears adequate at some locations, but not at all.

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References

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Barber PH, Bellwood DR (2005) Biodiversity hotspots: Evolutionary origins of biodiversity in wrasses Halichoeres in the Indo–Pacific and New World Tropics. Mol Phylogenet Evol 35:235–253

    Article  PubMed  Google Scholar 

  • Beerli P (2004) Effect of unsampled populations on the estimation of population sizes and migration rates between sampled populations. Mol Ecol 13:827–836

    Article  PubMed  Google Scholar 

  • Bell JJ, Okamura B (2005) Low genetic diversity in a marine nature reserve: re-evaluating diversity criteria in reserve design. Proc R Soc B 272:1067–1074

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

    Google Scholar 

  • Bowen BW, Rocha LA, Toonen RJ, Karl SA, ToBo Laboratory (2013) The origins of tropical marine biodiversity. Trends Ecol Evol 28:359–366

    Article  PubMed  Google Scholar 

  • Choat JH, Pollard D (2010) Coris bulbifrons. In: IUCN 2012 IUCN Red List of Threatened Species, Version 2012.1. http://www.iucnredlist.org/details/187392/0

  • Choat JH, Davies CR, Ackerman JL, Mapstone BD (2006a) Age structure and growth in a large teleost, Cheilinus undulatus, with a review of size distribution in labrid fishes. Marine Ecol Prog Ser 318:237–246

    Article  Google Scholar 

  • Choat JH, van Herwerden L, Robbins WD, Hobbs J-PA, Ayling AM (2006b) A report on the ecological surveys conducted at Middleton and Elizabeth Reefs, February 2006. Report to the Australian Government Department of Environment and Heritage, Canberra

  • Cowen RK, Sponaugle Su (2009) Larval dispersal and marine population connectivity. Annu Rev Mar Sci 1:443–466

    Article  Google Scholar 

  • Drew J, Allen G, Kaufman L, Barber PH (2008) Endemism and regional color and genetic differences in five putatively cosmopolitan reef fishes. Conserv Biol 22:965–975

    Article  PubMed  Google Scholar 

  • Evans RD, Russ L, van Herwerden GR, Frisch AJ (2010) Strong genetic but not spatial subdivision of two reef fish species targeted by fishers on the Great Barrier Reef. Fish Res 102:16–25

    Article  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin version 30, an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    PubMed Central  CAS  Google Scholar 

  • Francis MP (1993) Checklist of the coastal fishes of Lord Howe, Norfolk, and Kermadec Islands, south-west Pacific Ocean Pacific. Pac Sci 47:136–170

    Google Scholar 

  • Friedlander AM, DeMartini EE (2002) Contrasts in density, size, and biomass of reef fishes between the northwestern and the main Hawaiian islands: the effects of fishing down apex predators. Mar Ecol Prog Ser 230:253–264

    Article  Google Scholar 

  • Grant WS, Bowen BM (1998) Shallow population histories in deep evolutionary lineages of marine fishes, insights from the sardines and anchovies and lessons for conservation. J Hered 89:415–426

    Article  Google Scholar 

  • Harrison HB, Williamson DH, Evans RD, Almany GR, Thorrold SR, Russ GR, Feldheim KA, 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 22:1023–1028

    Article  CAS  PubMed  Google Scholar 

  • Hellberg ME (2009) Gene flow and isolation among populations of marine Aanimals. Annual Review of Ecology, Evolution and Systematics 40:291–310

    Article  Google Scholar 

  • Hobbs J-PA, Feary DA (2007) Monitoring the ecological status of Elizabeth and Middleton Reefs. Report to Australian Government Department of The Environment and Water Resources, Canberra

    Google Scholar 

  • Hobbs J-PA, Neilson J, Gilligan JJ (2009) Distribution, abundance, habitat association and extinction risk of marine fishes endemic to the Lord Howe Island region. Report to Lord Howe Island Marine Park

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332

    Article  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  CAS  PubMed  Google Scholar 

  • Jackson JB, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–637

    Article  CAS  PubMed  Google Scholar 

  • Johannes RE, Weibe WJ, Crossland CJ, Rimmer DW, Smith SAV (1983) Latitudinal limits of coral reef growth. Mar Ecol Prog Ser 11:105–111

    Article  Google Scholar 

  • Johannesson K, Andre C (2006) Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea. Mol Ecol 15:2013–2029

    Article  CAS  PubMed  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94

    Article  PubMed Central  PubMed  Google Scholar 

  • Jones GP, Caley MJ, Munday PL (2002) Rarity in coral reef fish communities. In: Sale PF (ed) Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic Press, San Diego, pp 81–101

    Chapter  Google Scholar 

  • Jones GP, Planes S, Thorrold SR (2005) Coral reef fish larvae settle close to home. Curr Biol 15:1314–1318

    Article  CAS  PubMed  Google Scholar 

  • Leis JM, van Herwerden L, Patterson HM (2011) Estimating connectivity in marine fish populations: What works best? Oceanogr Mar Biol 49:193–234

    Google Scholar 

  • Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Genetics 4:981–994

    CAS  PubMed  Google Scholar 

  • McCook LJ, Almany GR, Berumen ML, Day JC, Green AL, Jones GP, Leis JM, Planes S, Russ GR, Sale PF, Thorrold SR (2009) Management under uncertainty: guide-lines for incorporating connectivity into the protection of coral reefs. Coral Reefs 28:353–366

    Article  Google Scholar 

  • McNeely JA, Miller KR, Reid WV, Mittermeier RA, Werner TB (1990) Conserving the world’s biological diversity. World Conservation Union, World Resources Institute, Conservation International, World Wildlife Fund-US, and the World Bank, Washington, DC

  • Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first generation migrants detection. J Hered 95:536–539

    Article  CAS  PubMed  Google Scholar 

  • Planes S (2002) Biogeography and larval dispersal inferred from population genetic analysis. In: Sale PF (ed) Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic Press, San Diego, pp 201–220

    Chapter  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed Central  CAS  PubMed  Google Scholar 

  • Posada D (2008) jModelTest: Phylogenetic Model Averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Randall JE (1998) Zoogeography of shore fishes of the Indo-Pacific region. Zool Stud 37:227–268

    Google Scholar 

  • Randall JE (2001) Four new cardinalfishes Perciformes: Apogonidae from the Marquesas Islands. Pac Sci 55:47–64

    Article  Google Scholar 

  • Randall JE (2007) Reef and shore fishes of the Hawaiian Islands. Sea Grant College Program, University of Hawaii, Honolulu

    Google Scholar 

  • Randall JE, Kuiter RH (1982) Three new labrid fishes of the Genus Coris from the Western Pacific. Pac Sci 36:159–173

    Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  • Rocha LA (2004) Mitochondrial DNA and color pattern variation in three western Atlantic Halichoeres Labridae, with the revalidation of two species. Copeia 2004:770–782

    Article  Google Scholar 

  • Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629

    Article  PubMed  Google Scholar 

  • Shanks AL (2009) Pelagic larval duration and dispersal distance revisited. Biol Bull 216:373–385

    PubMed  Google Scholar 

  • Shulman MJ (1998) What can population genetics tell us about dispersal and biogeographic history of coral–reef fishes. Aust J Ecol 23:216–225

    Article  Google Scholar 

  • Steffen W, Crutzen PJ, McNeill JR (2007) The Anthropocene: Are humans now overwhelming the great forces of nature. Ambio 36:614–621

    Article  CAS  PubMed  Google Scholar 

  • Suthers IM, Young JM, Roughan MR, Everett JD, Brassington GB, Byrne M, Condie SA, Hartog JR, Hassler CS, Hobday AJ, Holbrook NJ, Malcolm HA, Oke PR, Thompson PA, Ridgway K (2011) The strengthening East Australian Current, its eddies and biological effects–an introduction and overview. Deep–Sea Res 58:538–546

    Article  Google Scholar 

  • Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of coral-reef fish. Nature 402:799–802

    Article  CAS  Google Scholar 

  • Toonen RJ, Andrews KR, Baums IB, Bird CE, Concepcion GT, Daly-Engel TS, Eble JE, Faucci A, Gaither MR, Iacchei M, Puritz JB, Schultz JK, Skillings DJ, Timmers MA, Bowen BW (2011) Defining boundaries for ecosystem-based management: A multispecies case study of marine connectivity across the Hawaiian Archipelago. Mar Biol 2011:1–13

    Article  Google Scholar 

  • van der Meer MH, Hobbs J-PA, Jones GP, van Herwerden L (2012a) Genetic connectivity among and self-replenishment within island populations of a restricted range subtropical reef fish. PLoS ONE 7(11): e49660. doi:10.1371/journalpone0049660

  • van der Meer MH, Hobbs J-PA, Jones GP, van Herwerden L (2012b) Historic hybridisation between two Australian anemonefish species Amphiprion and present–day patterns of connectivity. Ecol Evol 2:1592–1604

    Article  PubMed Central  PubMed  Google Scholar 

  • van der Meer MH, Gardner MG, Berumen ML, Hobbs J-PA, van Herwerden L (2013a) Identification of seventeen microsatellite loci for conservation genetic studies of the endemic wrasse Coris bulbifrons. Conserv Genet Res 4:243–246

    Article  Google Scholar 

  • van der Meer MH, Horne JB, Gardner MG, Hobbs J-PA, Pratchett M, van Herwerden L (2013b) Limited contemporary gene flow and high self-replenishment drives peripheral isolation in an endemic coral reef fish. Ecol Evol 3:1653–1666

    Article  PubMed Central  PubMed  Google Scholar 

  • Waples RS, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439

    Article  CAS  PubMed  Google Scholar 

  • Whittaker RJ (1998) Islands biogeography: Ecology, evolution, and conservation. Oxford University Press, Oxford

    Google Scholar 

  • Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    PubMed Central  PubMed  Google Scholar 

  • Winters KL, van Herwerden L, Choat JH, Robertson DR (2010) Phylogeography of the Indo-Pacific parrotfish Scarus psittacus, isolation generates distinctive peripheral populations in two oceans. Mar Biol 157:1679–1691

    Article  CAS  Google Scholar 

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Acknowledgments

We thank the LHI Board, LHI Park, Envirofund Australia (Natural Heritage Trust), Australian Department of the Environment and Water Resources and the Capricorn Star for either financial and/or logistical support. We also thank Sallyann Gudge and Ian Kerr (LHI Marine Park), Gary Crombie (donation of 15 Coris samples, LHI), Sivakumar Neelamegam (KAUST) and at NI: Dave Biggs (Charter Marine), James Edward (Bounty Divers), Doug Creek, Michael Smith, Jack Marges, Karlene Christian and Judith and Peter Davidson (Reserves and Forestry) for their assistance.

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Authors and Affiliations

  1. Molecular Ecology and Evolution Laboratory, School of Marine and Tropical Biology, James Cook University, Townsville, 4811, Australia

    M. H. van der Meer & L. van Herwerden

  2. ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, 4811, Australia

    M. H. van der Meer

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

    M. L. Berumen

  4. Department of Environment and Agriculture, Curtin University, Perth, WA, 6845, Australia

    J.-P. A. Hobbs

  5. Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, Townsville, 4811, Australia

    L. van Herwerden

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  1. M. H. van der Meer
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  2. M. L. Berumen
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  3. J.-P. A. Hobbs
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  4. L. van Herwerden
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Correspondence to M. H. van der Meer.

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Communicated by Biology Editor Dr. Mark Vermeij

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van der Meer, M.H., Berumen, M.L., Hobbs, JP.A. et al. Population connectivity and the effectiveness of marine protected areas to protect vulnerable, exploited and endemic coral reef fishes at an endemic hotspot. Coral Reefs 34, 393–402 (2015). https://doi.org/10.1007/s00338-014-1242-2

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  • DOI: https://doi.org/10.1007/s00338-014-1242-2

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