Low Connectivity between Mediterranean Marine Protected Areas: A Biophysical Modeling Approach for the Dusky Grouper Epinephelus marginatus

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Andrello, Marco ^a,b   Mouillot, David ^c,d   Beuvier, Jonathan ^e,f   Albouy, Camille ^g   Thuiller, Wilfried ^b   Manel, Stéphanie ^a,h  

^a Aix Marseille University Marseille   (France)

^b UNIVERSITÉ JOSEPH FOURIER   (France)

^c UNIVERSITÉ MONTPELLIER 2   (France)

^d JAMES COOK UNIVERSITY   (Australia)

^e MERCATOR OCÉAN   (France)

^f CNRS   (France)

^g UNIVERSITÉ DU QUÉBEC À RIMOUSKI   (Canada)

^h UMR AMAP   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL DISPERSAL; ARTICLE; CONTINENTAL SHELF; ENVIRONMENTAL PROTECTION; ENVIRONMENTAL TEMPERATURE; EPINEPHELUS MARGINATUS; GENE TRANSFER; LARVA; MARINE ENVIRONMENT; MARINE PROTECTED AREA; MEDITERRANEAN SEA; NONHUMAN; POPULATION MIGRATION; SPAWNING;

ANIMAL MIGRATION; ANIMALS; BIOPHYSICAL PHENOMENA; CLUSTER ANALYSIS; CONSERVATION OF NATURAL RESOURCES; ECOSYSTEM; FISHES; GEOGRAPHY; LARVA; MEDITERRANEAN SEA; MODELS, THEORETICAL; REPRODUCTION; SEASONS;

EPINEPHELUS MARGINATUS;

EID: 84879902100     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068564     Document Type: Article

References (108)

1. Srinivasan UT, Watson R, Sumaila UR, (2012) Global fisheries losses at the exclusive economic zone level, 1950 to present. Marine Policy 36: 544-549.
2. Halpern BS, (2003) The impact of marine reserves: Do reserves work and does reserve size matter? Ecological Applications 13: S117-S137.
3. Guidetti P, Milazzo M, Bussotti S, Molinari A, Murenu M, et al. (2008) Italian marine reserve effectiveness: Does enforcement matter? Biological Conservation 141: 699-709.
4. Claudet J, Osenberg CW, Benedetti-Cecchi L, Domenici P, Garcia-Charton J-A, et al. (2008) Marine reserves: size and age do matter. Ecology Letters 11: 481-489.
5. Sala E, Ballesteros E, Dendrinos P, Di Franco A, Ferretti F, et al. (2012) The Structure of Mediterranean Rocky Reef Ecosystems across Environmental and Human Gradients, and Conservation Implications. Plos One 7.
6. Garcia-Charton JA, Perez-Ruzafa A, Marcos C, Claudet J, Badalamenti F, et al. (2008) Effectiveness of European Atlanto-Mediterranean MPAs: Do they accomplish the expected effects on populations, communities and ecosystems? Journal for Nature Conservation 16: 193-221.
7. Bell JJ, (2008) Connectivity between island Marine Protected Areas and the mainland. Biological Conservation 141: 2807-2820.
8. Di Franco A, Coppini G, Pujolar JM, De Leo GA, Gatto M, et al. (2012) Assessing Dispersal Patterns of Fish Propagules from an Effective Mediterranean Marine Protected Area. PLoS ONE 7: e52108.
9. Gaines SD, White C, Carr MH, Palumbi SR, (2010) Designing marine reserve networks for both conservation and fisheries management. Proceedings of the National Academy of Sciences 107: 18286-18293.
10. Di Franco A, Gillanders BM, De Benedetto G, Pennetta A, De Leo GA, et al. (2012) Dispersal Patterns of Coastal Fish: Implications for Designing Networks of Marine Protected Areas. Plos One 7.
11. Kaplan DM, Botsford LW, O'Farrell MR, Gaines SD, Jorgensen S, (2009) Model-based assessment of persistence in proposed marine protected area designs. Ecological Applications 19: 433-448.
12. Almany GR, Connolly SR, Heath DD, Hogan JD, Jones GP, et al. (2009) Connectivity, biodiversity conservation and the design of marine reserve networks for coral reefs. Coral Reefs 28: 339-351.
13. Botsford LW, Brumbaugh DR, Grimes C, Kellner JB, Largier J, et al. (2009) Connectivity, sustainability, and yield: bridging the gap between conventional fisheries management and marine protected areas. Reviews in Fish Biology and Fisheries 19: 69-95.
14. Gerber LR, Heppell SS, Ballantyne F, Sala E, (2005) The role of dispersal and demography in determining the efficacy of marine reserves. Canadian Journal of Fisheries and Aquatic Sciences 62: 863-871.
15. Grüss A, Kaplan DM, Hart DR, (2011) Relative Impacts of Adult Movement, Larval Dispersal and Harvester Movement on the Effectiveness of Reserve Networks. Plos One 6: e19960.
16. Jones GP, Planes S, Thorrold SR, (2005) Coral Reef Fish Larvae Settle Close to Home. Current biology: CB 15: 1314-1318.
17. Almany GR, Berumen ML, Thorrold SR, Planes S, Jones GP, (2007) Local Replenishment of Coral Reef Fish Populations in a Marine Reserve. Science 316: 742-744.
18. Swearer SE, Shima JS, Hellberg ME, Thorrold SR, Jones GP, et al. (2002) Evidence of self-recruitment in demersal marine populations. Bulletin of Marine Science 70: 251-271.
19. Buston PM, Jones GP, Planes S, Thorrold SR (2011) Probability of successful larval dispersal declines fivefold over 1 km in a coral reef fish. Proceedings of the Royal Society B: Biological Sciences.
20. Christie MR, Tissot BN, Albins MA, Beets JP, Jia Y, et al. (2010) Larval Connectivity in an Effective Network of Marine Protected Areas. Plos One 5: e15715.
21. Harrison Hugo B, Williamson David H, Evans Richard D, Almany Glenn R, Thorrold Simon R, et al. (2012) Larval Export from Marine Reserves and the Recruitment Benefit for Fish and Fisheries. Current biology: CB 22: 1023-1028.
22. Saenz-Agudelo P, Jones GP, Thorrold SR, Planes S, (2009) Estimating connectivity in marine populations: an empirical evaluation of assignment tests and parentage analysis under different gene flow scenarios. Molecular Ecology 18: 1765-1776.
23. Saenz-Agudelo P, Jones GP, Thorrold SR, Planes S, (2011) Connectivity dominates larval replenishment in a coastal reef fish metapopulation. Proceedings of the Royal Society B-Biological Sciences 278: 2954-2961.
24. James MK, Armsworth PR, Mason LB, Bode L, (2002) The structure of reef fish metapopulations: modelling larval dispersal and retention patterns. Proceedings of the Royal Society of London Series B-Biological Sciences 269: 2079-2086.
25. Cowen RK, Lwiza KMM, Sponaugle S, Paris CB, Olson DB, (2000) Connectivity of marine populations: Open or closed? Science 287: 857-859.
26. Albert CH, Yoccoz NG, Edwards TC Jr, Graham CH, Zimmermann NE, et al. (2010) Sampling in ecology and evolution- bridging the gap between theory and practice. Ecography 33: 1028-1037.
27. Coll M, Piroddi C, Steenbeek J, Kaschner K, Lasram FBR, et al. (2010) The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats. Plos One 5.
28. Coll M, Piroddi C, Albouy C, Lasram FB, Cheung WWL, et al. (2012) The Mediterranean Sea under siege: spatial overlap between marine biodiversity, cumulative threats and marine reserves. Global Ecology and Biogeography 21: 465-480.
29. Abdulla A, Gomei M, Hyrenbach D, Notarbartolo-di-Sciara G, Agardy T, (2009) Challenges facing a network of representative marine protected areas in the Mediterranean: prioritizing the protection of underrepresented habitats. Ices Journal of Marine Science 66: 22-28.
30. Mouillot D, Albouy C, Guilhaumon F, Lasram FBR, Coll M, et al. (2011) Protected and Threatened Components of Fish Biodiversity in the Mediterranean Sea. Current Biology 21: 1044-1050.
31. Lembo G, Fleming IA,Økland F, Carbonara P, Spedicato MT, (1999) Site fidelity of the dusky grouper Epinephelus marginatus (Lowe, 1834) studied by acoustic telemetry. Marine Life 9: 37-43.
32. Afonso P, Fontes J, Santos RS, (2011) Small marine reserves can offer long term protection to an endangered fish. Biological Conservation 144: 2739-2744.
33. Pastor J, Verdoit-Jarraya M, Astruch P, Dalias N, Nelva Pasqual J, et al. (2009) Acoustic telemetry survey of the dusky grouper (Epinephelus marginatus) in the Marine Reserve of Cerbère-Banyuls: informations on the territoriality of this emblematic species. Comptes Rendus Biologies 332: 732-740.
34. Francour P, Harmelin JG, Pollard D, Sartoretto S, (2001) A review of marine protected areas in the northwestern Mediterranean region: siting, usage, zonation and management. Aquatic Conservation-Marine and Freshwater Ecosystems 11: 155-188.
35. de Almeida Rodrigues Filho J, Gomes Sanches E, de Oliveira Garcia C, Viana Pannuti C, Figueiredo Sebastiani E, et al. (2009) Threatened fishes of the world: Epinephelus marginatus (Lowe, 1834) (Serranidae: Epinephelinae). Environmental Biology of Fishes 85: 301-302.
36. Renones O, Grau A, Mas X, Riera F, Saborido-Rey F, (2010) Reproductive pattern of an exploited dusky grouper Epinephelus marginatus (Lowe 1834) (Pisces: Serranidae) population in the western Mediterranean. Scientia Marina 74: 523-537.
37. Renones O, Pineiro C, Mas X, Goni R, (2007) Age and growth of the dusky grouper Epinephelus marginatus (Lowe 1834) in an exploited population of the western Mediterranean Sea. Journal of Fish Biology 71: 346-362.
38. Garcia-Charton JA, Perez-Ruzafa A, Saanchez-Jerez P, Bayle-Sempere JT, Renones O, et al. (2004) Multi-scale spatial heterogeneity, habitat structure, and the effect of marine reserves on Western Mediterranean rocky reef fish assemblages. Marine Biology 144: 161-182.
39. Kininmonth SJ, De'ath G, Possingham HP, (2010) Graph theoretic topology of the Great but small Barrier Reef world. Theoretical Ecology 3: 75-88.
40. Treml EA, Halpin PN, Urban DL, Pratson LF, (2008) Modeling population connectivity by ocean currents, a graph-theoretic approach for marine conservation. Landscape Ecology 23: 19-36.
41. Rozenfeld AF, Arnaud-Haond S, Hernandez-Garcia E, Eguiluz VM, Serrao EA, et al. (2008) Network analysis identifies weak and strong links in a metapopulation system. Proceedings of the National Academy of Sciences of the United States of America 105: 18824-18829.
42. Heemstra PC, Randall JE (1993) Groupers of the world (Family Serranidae, subfamily Epinephelinae). An annotated and illustrated catalogue of the grouper, rockcod, hind, coral grouper and lyretail species known to date: FAO Fish. Synop.
43. Whitehead PJP, Bauchot L, Hureau JC, Nielsen J, Tortonese E (1986) Fishes of the north-eastern Atlantic and the Mediterranean: UNESCO, Paris.
44. Hereu B, Diaz D, Pasqual J, Zabala M, Sala E, (2006) Temporal patterns of spawning of the dusky grouper Epinephelus marginatus in relation to environmental factors. Marine Ecology-Progress Series 325: 187-194.
45. Zabala M, GarciaRubies A, Louisy P, Sala E, (1997) Spawning behaviour of the Mediterranean dusky grouper Epinephelus marginatus (Lowe, 1834) (Piscea, Serranidae) in the Medes Islands Marine Reserve (NW Mediterranean, Spain). Scientia Marina 61: 65-77.
46. Macpherson E, Raventos N, (2006) Relationship between pelagic larval duration and geographic distribution of Mediterranean littoral fishes. Marine Ecology-Progress Series 327: 257-265.
47. Boglione C, Marino G, Giganti M, Longobardi A, De Marzi P, et al. (2009) Skeletal anomalies in dusky grouper Epinephelus marginatus (Lowe 1834) juveniles reared with different methodologies and larval densities. Aquaculture 291: 48-60.
48. Cunha ME, Quental H, Barradas A, Pousão-Ferreira P, Cabrita E, et al. (2009) Rearing larvae of dusky grouper, Epinephelus marginatus (Lowe, 1834), (Pisces: Serranidae) in a semi-extensive mesocosm. Scientia Marina 73S1: 201-212.
49. Glamuzina B, Skaramuca B, Glavic N, Kozul V, Dulcic J, et al. (1998) Egg and early larval development of laboratory reared dusky grouper, Epinephelus marginatus (Lowe, 1834) (Pisces, Serranidae). Scientia Marina 62: 373-378.
50. Spedicato MT, Boglione C, (2000) Main constraints in the artificial propagation of the dusky grouper Epinephelus marginatus (Lowe, 1834): three years experimental trials on induced spawning and larval rearing. Cahiers Options Méditerranéennes 47: 227-234.
51. Beuvier J, Béranger K, Lebeaupin Brossier C, Somot S, Sevault F, et al. (2012) Spreading of the Western Mediterranean Deep Water after winter 2005: time-scales and deep cyclone transport. Journal of Geophysical Research 117: C07022.
52. Beuvier J, Lebeaupin Brossier C, Béranger K, Arsouze T, Bourdallé-Badie R, et al. (2012) MED12, oceanic component for the modeling of the regional Mediterannean Earth system. Mercator Ocean Quarterly Newsletter 46: 60-66.
53. Madec G, the Nemo team (2008) NEMO ocean engine. Note du Pôle de modélisation. Institut Pierre-Simon Laplace (IPSL), France.
54. Largier J, (2003) Considerations in Estimating Larval Dispersal Distances from Oceanographic Data. Ecological Applications 13: S71-S89.
55. Medimap Group (2005) Morpho-bathymetry of the Mediterranean Sea, scale 1/2000000. CIESM/Ifremer, Brest, France.
56. Berné S, Carré D, Loubrieu B, Mazé J-P, Morvan L, et al. (2004) Le golfe du Lion - Carte morpho-bathymétrique. Ifremer, Brest, France.
57. Arakawa A, Lamb VR, (1981) A potential energy and enstrophy conserving scheme for the shallow water equations. Monthly Weather Review 109: 18-36.
58. Barnier B, Madec G, Penduff T, Molines J-M, Treguier A-M, et al. (2006) Impact of partial steps and momentum advection schemes in a global ocean circulation model at eddy-permitting resolution. Ocean Dynamics 56: 543-567.
59. Blanke B, Delecluse P, (1993) Low frequency variability of the tropical Atlantic Ocean simulated by a general circulation model with mixed layer physics. Journal of Physical Oceanography 23: 1363-1388.
60. Herrmann MJ, Somot S, (2008) Relevance of ERA40 dynamical downscaling for modeling deep convection in the Mediterranean Sea. Geophysical Research Letters 35: L04607.
61. Beuvier J (2011) Modelling the long-term variability of circulation and water masses in the Mediteranean Sea: impacts of the ocean-atmosphere exchanges: PhD Thesis. Ecole Polytechnique, Palaiseau, France. 290 p.
62. Rixen M, Beckers JM, Levitus S, Antonov J, Boyer T, et al. (2005) The Western Mediterranean Deep Water: A proxy for climate change. Geophysical Research Letters 32.
63. Ingleby B, Huddleston M, (2007) Quality control of ocean temperature and salinity profiles- Historical and real-time data. Journal of Marine Systems 65: 158-175.
64. Millot C, Taupier-Letage I (2005) Circulation in the Mediterranean Sea. In: Saliot A, editor. The Mediterranean Sea: Springer.
65. Pinardi N, Navarra A, (1993) Baroclinic wind adjustment processes in the Mediterranean Sea. Deep Sea Research Part II: Topical Studies in Oceanography 40: 1299-1326.
66. Testor P, Send U, Gascard JC, Millot C, Taupier-Letage I, et al. (2005) The mean circulation of the southwestern Mediterranean Sea: Algerian Gyres. Journal of Geophysical Research: Oceans 110: C11017.
67. Lett C, Verley P, Mullon C, Parada C, Brochier T, et al. (2008) A Lagrangian tool for modelling ichthyoplankton dynamics. Environmental Modelling & Software 23: 1210-1214.
68. Peliz A, Marchesiello P, Dubert J, Marta-Almeida M, Roy C, et al. (2007) A study of crab larvae dispersal on the Western Iberian Shelf: Physical processes. Journal of Marine Systems 68: 215-236.
69. Monin AS, Ozmidov RV (1982) Turbulence in the Ocean. Tennekes H, translator. Reidel, Boston.
70. 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: 54-69.
71. Bonhommeau S, Le Pape O, Gascuel D, Blanke B, Treguier AM, et al. (2009) Estimates of the mortality and the duration of the trans-Atlantic migration of European eel Anguilla anguilla leptocephali using a particle tracking model. Journal of Fish Biology 74: 1891-1914.
72. Lampert W, (1989) The Adaptive Significance of Diel Vertical Migration of Zooplankton. Functional Ecology 3: 21-27.
73. Botsford LW, Hastings A, Gaines SD, (2001) Dependence of sustainability on the configuration of marine reserves and larval dispersal distance. Ecology Letters 4: 144-150.
74. Kaplan DM, Botsford LW, Jorgensen S, (2006) Dispersal per recruit: An efficient method for assessing sustainability in marine reserve networks. Ecological Applications 16: 2248-2263.
75. Urban DL, Minor ES, Treml EA, Schick RS, (2009) Graph models of habitat mosaics. Ecology Letters 12: 260-273.
76. Bode M, Bode L, Armsworth PR, (2006) Larval dispersal reveals regional sources and sinks in the Great Barrier Reef. Marine Ecology-Progress Series 308: 17-25.
77. R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
78. Pebesma EJ, Bivand RS (2005) Classes and methods for spatial data in R. R News 5.
79. Csardi G, Nepusz T (2006) The igraph software package for complex network research. InterJournal, Complex Systems 1695.
80. Tonani M, Pinardi N, Dobricic S, Pujol I, Fratianni C, (2008) A high-resolution free-surface model of the Mediterranean Sea. Ocean Science 4: 1-14.
81. Pairaud IL, Gatti J, Bensoussan N, Verney R, Garreau P, (2011) Hydrology and circulation in a coastal area off Marseille: Validation of a nested 3D model with observations. Journal of Marine Systems 88: 20-33.
82. Basterretxea G, Jordi A, Catalan IA, Sabates A, (2012) Model-based assessment of local-scale fish larval connectivity in a network of marine protected areas. Fisheries Oceanography 21: 291-306.
83. Leis JM (2006) Are larvae of demersal fishes plankton or nekton? In: Southward AJ, Sims DW, editors. Advances in Marine Biology, Vol 51. London: Academic Press Ltd-Elsevier Science Ltd. 57-141.
84. Treml EA, Roberts JJ, Chao Y, Halpin PN, Possingham HP, et al. (2012) Reproductive Output and Duration of the Pelagic Larval Stage Determine Seascape-Wide Connectivity of Marine Populations. Integrative and Comparative Biology 52: 525-537.
85. Cowen RK, Paris CB, Srinivasan A, (2006) Scaling of connectivity in marine populations. Science 311: 522-527.
86. Jacobi MN, Jonsson PR, (2011) Optimal networks of nature reserves can be found through eigenvalue perturbation theory of the connectivity matrix. Ecological Applications 21: 1861-1870.
87. Kininmonth S, Beger M, Bode M, Peterson E, Adams VM, et al. (2011) Dispersal connectivity and reserve selection for marine conservation. Ecological Modelling 222: 1272-1282.
88. Jacobi MN, Andre C, Doos K, Jonsson PR, (2012) Identification of subpopulations from connectivity matrices. Ecography 35: 1004-1016.
89. Berglund M, Jacobi MN, Jonsson PR, (2012) Optimal selection of marine protected areas based on connectivity and habitat quality. Ecological Modelling 240: 105-112.
90. 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. Molecular Ecology 15: 1419-1439.
91. Treml EA, Halpin PN, (2012) Marine population connectivity identifies ecological neighbors for conservation planning in the Coral Triangle. Conservation Letters 5: 441-449.
92. Hastings A, Botsford LW, (2006) Persistence of spatial populations depends on returning home. Proceedings of the National Academy of Sciences of the United States of America 103: 6067-6072.
93. Armsworth PR, (2002) Recruitment limitation, population regulation, and larval connectivity in reef fish metapopulations. Ecology 83: 1092-1104.
94. Gerber LR, Botsford LW, Hastings A, Possingham HP, Gaines SD, et al. (2003) Population models for marine reserve design: a retrospective and prospective synthesis. Ecological Applications 13: 47-64.
95. Selkoe KA, Toonen RJ, (2011) Marine connectivity: a new look at pelagic larval duration and genetic metrics of dispersal. Marine Ecology-Progress Series 436: 291-305.
96. Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Malden, Mass.; Oxford: Blackwell. xix, 642 p. p.
97. Reusch TBH, Ehlers A, Hammerli A, Worm B, (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proceedings of the National Academy of Sciences of the United States of America 102: 2826-2831.
98. Mumby PJ, Elliott IA, Eakin CM, Skirving W, Paris CB, et al. (2011) Reserve design for uncertain responses of coral reefs to climate change. Ecology Letters 14: 132-140.
99. Somot S, Sevault F, Deque M, (2006) Transient climate change scenario simulation of the Mediterranean Sea for the twenty-first century using a high-resolution ocean circulation model. Climate Dynamics 27: 851-879.
100. Somot S, Sevault F, Deque M, Crepon M, (2008) 21st century climate change scenario for the Mediterranean using a coupled atmosphere-ocean regional climate model. Global and Planetary Change 63: 112-126.
101. Lasram FB, Guilhaumon F, Albouy C, Somot S, Thuiller W, et al. (2010) The Mediterranean Sea as a 'cul-de-sac' for endemic fishes facing climate change. Global Change Biology 16: 3233-3245.
102. Albouy C, Guilhaumon F, Araujo MB, Mouillot D, Leprieur F, (2012) Combining projected changes in species richness and composition reveals climate change impacts on coastal Mediterranean fish assemblages. Global Change Biology 18: 2995-3003.
103. Bodilis P, Ganteaume A, Francour P, (2003) Recruitment of the dusky grouper (Epinephelus marginatus) in the north-western Mediterranean Sea. Cybium 27: 123-129.
104. Schunter C, Carreras-Carbonell J, Planes S, Sala E, Ballesteros E, et al. (2011) Genetic connectivity patterns in an endangered species: The dusky grouper (Epinephelus marginatus). Journal of Experimental Marine Biology and Ecology 401: 126-133.
105. Maggio T, Andaloro F, Arculeo M, (2006) Genetic population structure of Epinephelus marginatus (Pisces, Serranidae) revealed by two molecular markers. Italian Journal of Zoology 73: 275-283.
106. Hedgecock D, Barber PH, Edmands S, (2007) Genetic Approaches to Measuring Connectivity. Oceanography 20: 70-79.
107. Pelc RA, Warner RR, Gaines SD, Paris CB, (2010) Detecting larval export from marine reserves. Proceedings of the National Academy of Sciences of the United States of America 107: 18266-18271.
108. Spalding MD, Fox HE, Allen GR, Davidson N, Ferdana ZA, et al. (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57: 573-583.