Marine reserves help preserve genetic diversity after impacts derived from climate variability: Lessons from the pink abalone in Baja California

Global Ecology and Conservation

Volumn 4, Issue , 2015, Pages 264-276

  Munguía Vega, Adrián ^a,b   Sáenz Arroyo, Andrea ^c   Greenley, Ashley P ^d   Espinoza Montes, Jose Antonio ^e   Palumbi, Stephen R ^d   Rossetto, Marisa ^f   Micheli, Fiorenza ^d  

^a UNIVERSITY OF ARIZONA   (United States)

^b Colonia Centro   (Mexico)

^c DEPARTAMENTO DE CONSERVACIÓN DE LA BIODIVERSIDAD   (Mexico)

^d STANFORD UNIVERSITY   (United States)

^e Sociedad Cooperativa de Produccion Pesquera Buzos y Pescadores   (Mexico)

^f POLITECNICO DI MILANO   (Italy)

Author keywords

Haliotis; Larval dispersal; Marine reserve; Microsatellite; Overfishing; Restocking

Indexed keywords

ANIMALIA; HALIOTIS; HALIOTIS CORRUGATA;

EID: 84938064155     PISSN: None     EISSN: 23519894     Source Type: Journal    
DOI: 10.1016/j.gecco.2015.07.005     Document Type: Article

References (75)

1. Almany G.R., Connolly S.R., Heath D.D., Hogan J.D., Jones G.P., Mccook L.J., Mills M., Pressey R.L., Williamson D.H. Connectivity, biodiversity conservation and the design of marine reserve networks for coral reefs. Coral Reefs 2009, 28:339-351.
2. Barnosky A.D., Hadly E.A., Bascompte J., Berlow E.L., Brown J.H., Fortelius M., Getz W.M., Harte J., Hastings A., Marquet P.A., Martinez N.D., Mooers A., Roopnarine P., Vermeij G., Williams J.W., Gillespie R., Kitzes J., Marshall C., Matzke N., Mindell D.P., Revilla E., Smith A.B. Approaching a state shift in Earth's biosphere. Nature 2012, 486:52-58.
3. Barton N.H., Slatkin M. A quasi-equilibrium theory of the distribution of rare alleles in a subdivided population. Heredity 1986, 56:409-415.
4. Bell J. Connectivity between island Marine Protected Areas and the mainland. Biol. Conserv. 2008, 141:2807-2820.
5. Bell J.J., Okamura B. Low genetic diversity in a marine nature reserve: Re-evaluating diversity criteria in reserve design. Proc. R. Soc. Biol. Sci. 2005, 272:1067-1074.
6. Campana M.G., Hunt H.V., Jones H., White J. Corrsieve: Software for summarizing and evaluating structure output. Mol. Ecol. Resour. 2011, 11:349-352.
7. Carballo G.L., Mucino-Diaz M. Pesqueria De Abulon. Estudio Del Potencial Pesquero Y Acuicola De Baja California Sur 1996, 15-41. Centro de Investigaciones Biologicas del Noroeste, SC, La Paz. M. Casas-Valdez, G. Ponce-Díaz (Eds.).
8. Christie M.R., Johnson D.W., Stallings C.D., Hixon M.A. Self-recruitment and sweepstakes reproduction amid extensive gene flow in a coral-reef fish. Mol. Ecol. 2010, 19:1042-1057.
9. Diaz-Viloria N., Cruz P., Guzman-Del Proo S.A., Perez-Enriquez R. Genetic connectivity among pink abalone haliotis corrugata populations. J. Shellfish Res. 2009, 28:599-608.
10. Doney S.C., Ruckelshaus M., Duffy J.E., Barry J.P., Chan F., English C.A., Galindo H.M., Grebmeier J.M., Hollowed A.B., Knowlton N., Polovina J., Rabalais N.N., Sydeman W.J., Talley L.D. Climate change impacts on marine ecosystems. Annu. Rev. Mar. Sci. 2012, 4:11-37.
11. Edwards, C.L., 1913. The abalone industry in California. Fish bulletin 1. California Department of Fish and Game, Sacramento, CA, USA, pp. 5-15.
12. Gaines S.D., White C., Carr M.H., Palumbi S.R. Designing marine reserve networks for both conservation and fisheries management. Proc. Natl. Acad. Sci. 2010, 107:18286-18293.
13. Garza J.C., Williamson E.G. Detection of reduction in population size using data from microsatellite loci. Mol. Ecol. 2001, 10:305-318.
14. Gleason M., Fox E., Ashcraft S., Vasques J., Whiteman E., Serpa P., Saarman E., Caldwell M., Frimodig A., Miller-Henson M., Kirlin J., Ota B., Pope E., Weber M., Wiseman K. Designing a network of marine protected areas in california: Achievements, costs, lessons learned, and challenges ahead. Ocean Coast. Manag. 2013, 74:90-101.
15. Green A.L., Fernandes L., Almany G., Abesamis R., Mcleod E., Aliño P.M., White A.T., Salm R., Tanzer J., Pressey R.L. Designing marine reserves for fisheries management, biodiversity conservation, and climate change adaptation. Coast. Manag. 2014, 42:143-159.
16. Greenley A.P., Munguia-Vega A., Saenz-Arroyo A., Micheli F. New tetranucleotide microsatellite loci in pink abalone (Haliotis corrugata) isolated via 454 pyrosequencing. Conserv. Genet. Resour. 2012, 4:265-268.
17. Gruenthal K.M., Witting D.A., Ford T., Neuman M.J., Williams J.P., Pondella D.J., Bird A., Caruso N., Hyde J.R., Seeb L.W., Larson W.A. Development and application of genomic tools to the restoration of green abalone in southern California. Conserv. Genet. 2014, 15:109-121.
18. Guillot G. Inference of structure in subdivided populations at low levels of genetic differentiation. The correlated allele frequencies model revisited. Bioinformatics 2008, 24:2222-2228.
19. Guillot G., Santos F., Estoup A. Analysing georeferenced population genetics data with Geneland: A new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics 2008, 24:1406-1407.
20. Gutierrez-Gonzalez J.L., Cruz P., Del Rio-Portilla M.A., Perez-Enriquez R. Genetic structure of green abalone haliotis fulgens population off Baja California, Mexico. J. Shellfish Res. 2007, 26:839-846.
21. Hamasaki K., Kitada S. The enhancement of abalone stocks: Lessons from Japanese case studies. Fish Fish. 2008, 9:243-260.
22. Haupt A.J., Micheli F., Palumbi S.R. Dispersal at a Snail's Pace: Historical processes affect contemporary genetic structure in the exploited wavy top snail (Megastraea undosa). J. Hered. 2013, 104:327-340.
23. Haupt A.J., Woodson C.B., Micheli F., Palumbi S.R. Subtle genetic structure translates to limited ecological connectivity in a commercially fished invertebrate species. Mar. Biol. 2015, submitted for publication.
24. Hubisz M.J., Falush D., Stephens M., Pritchard J.K. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Resour. 2009, 9:1322-1332.
25. Hutchings J.A., Reynolds J.D. Marine fish population collapses: Consequences for recovery and extinction risk. BioScience 2004, 54:297-309.
26. Jones O.R., Wang J. Colony: A program for parentage and sibship inference from multilocus genotype data. Mol. Ecol. Resour. 2010, 10:551-555.
27. Jost L. GST and its relatives do not measure differentiation. Mol. Ecol. 2008, 17:4015-4026.
28. Kalinowski S.T. Hp-Rare 1.0: A computer program for performing rarefaction on measures of allelic richness. Mol. Ecol. Notes 2005, 5:187-189.
29. Keller L.F., Waller D.M. Inbreeding effects in wild populations. Trends Ecol. Evolut. 2002, 17:230-241.
30. Klinger D., Naylor R. Searching for solutions in aquaculture: Charting a sustainable course. Annu. Rev. Environ. Resour. 2012, 37:247-276.
31. Koh K.S., Matz C., Tan C.H., Le H.L., Rice S.A., Marshall D.J., Steinberg P.D., Kjelleberg S. Minimal increase in genetic diversity enhances predation resistance. Mol. Ecol. 2012, 21:1741-1753.
32. Kool J.T., Paris C.B., Barber P.H., Cowen R.K. Connectivity and the development of population genetic structure in Indo-West Pacific coral reef communities. Glob. Ecol. Biogeogr. 2011, 20:695-706.
33. Laikre L. Genetic diversity is overlooked in international conservation policy implementation. Conserv. Genet. 2010, 11:349-354.
34. Leighton D.L. The influence of temperature on larval and juvenile growth in three species of southern California abalones. Fish. Bull. 1974, 72.
35. Lemer S., Planes S. Translocation of wild populations: Conservation implications for the genetic diversity of the black-lipped pearl oyster Pinctada margaritifera. Mol. Ecol. 2012, 21:2949-2962.
36. Lester S.E., Halpern B.S., Grorud-Colvert K., Lubchenco J., Ruttenberg B.I., Gaines S.D., Airamé S., Warner R.R. Biological effects within no-take marine reserves: A global synthesis. Mar. Ecol. Prog. Ser. 2009, 384:33-46.
37. Lotze H.K., Coll M., Magera A.M., Ward-Paige C., Airoldi L. Recovery of marine animal populations and ecosystems. Trends Ecol. Evolut. 2011, 26:595-605.
38. Luikart G., Cournet J.M. Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv. Biol. 1998, 12:228-237.
39. Lynn R.J. The California current system: The seasonal variability of its physical characteristics. J. Geophys. Res. 1987, 92:12947-12966.
40. Meirmans P.G., Hedrick P.W. Assessing population structure: F(St) and related measures. Mol. Ecol. Resour. 2011, 11:5-18.
41. Meirmans P.G., Van Tienderen P.H. Genotype and genodive: Two programs for the analysis of genetic diversity of asexual organisms. Mol. Ecol. Notes 2004, 4:792-794.
42. Micheli F., Saenz-Arroyo A., Greenley A., Vazquez L., Espinoza Montes J.A., Rossetto M., De Leo G.A. Evidence that marine reserves enhance resilience to climatic impacts. PLoS One 2012, 7:e40832.
43. Micheli F., Shelton A., Bushinsky S., Chiu A., Haupt A., Heiman K., Kappel C., Lynch M., Martone R., Dunbar R. Persistence of depleted abalones in marine reserves of central California. Biol. Conserv. 2008, 141:1078-1090.
44. Miller K.J., Ayre D.J. Protection of genetic diversity and maintenance of connectivity among reef corals within marine protected areas. Conserv. Biol. 2008, 22:1245-1254.
45. Miyake Y., Kimura S., Kawamura T., Kitagawa T., Hara M., Hoshikawa H. Estimating larval supply of Ezo abalone Haliotis discus nannai in a small bay using a coupled particle-tracking and hydrodynamic model: Insights into the establishment of harvest refugia. Fish. Sci. 2010, 76:561-570.
46. Morales-Bojorquez E., Mucino-Diaz M.O., Velez-Barajas J.A. Analysis of the decline of the abalone fishery (Haliotis fulgens and H. corrugata) along the westcentral coast of the Baja California Peninsula, Mexico. J. Shellfish Res. 2008, 27:865-870.
47. Nei M. Molecular Evolutionary Genetics 1987, Columbia University Press, New York.
48. Paetkau D., Slade R., Burdens M., Estoup A. Genetic assignment methods for the direct, real-time estimation of migration rate: A simulation-based exploration of accuracy and power. Mol. Ecol. 2004, 13:55-65.
49. Park C.-J., Hara M., Lee J.-H., Noh J.K., Kim H.C., Park J.W., Kim S.Y. Genetic population structure of the wild pacific abalone (Haliotis discus) in Korea and Japan based on microsatellite DNA markers. Biochem. Sys. Ecol. 2012, 44:86-95.
50. Parnell P.E., Lennert-Cody C.E., Geelen L., Stanley L.D., Dayton P.K. Effectiveness of a small marine reserve in southern California. Mar. Ecol. Prog. Ser. 2005, 296:39-52.
51. Peakall R.O.D., Smouse P.E. Genalex 6: Genetic analysis in excel. Population genetic software for teaching and research. Mol. Ecol. Notes 2006, 6:288-295.
52. Pespeni M.H., Al E. Evolutionary change during experimental ocean acidification. Proc. Natl. Acad. Sci. 2013, 110:6937-6942.
53. Pinsky M.L., Palumbi S.R. Meta-analysis reveals lower genetic diversity in overfished populations. Mol. Ecol. 2014, 23:29-39.
54. Piry S., Alapetite A., Cornuet J.M., Paetkau D., Baudouin L., Estoup A. Geneclass2: A software for genetic assignment and first-generation migrant detection. J. Hered. 2004, 95:536-539.
55. Piry S., Luikart G., Cournet J.M. Bottleneck: A computer program for detecting recent reductions in effective population size using allele frequency data. J. Hered. 1999, 90:502-503.
56. Queller D.C., Goodnight K.F. Estimating relatedness using genetic markers. Evolution 1989, 43:258-275.
57. Rannala B., Mountain J.L. Detecting immigration by using multilocus genotypes. Proc. Natl. Acad. Sci. 1997, 94:9197-9201.
58. Raymond M., Rousset F. Genepop (version 1.2): Population genetics software for exact tests and ecumenicism. J. Hered. 1995, 86:248-249.
59. Rice W.R. Analyzing tables of statistical tests. Evolution 1989, 43:223-225.
60. Roodt-Wilding R. Abalone ranching: A review on genetic considerations. Aquacult. Res. 2007, 38:1229-1241.
61. Rossetto M., Leo G.a.D., Greenley A., Vazquez L., Saenz-Arroyo A., Montes J.a.E., Micheli F. Reproductive potential can predict recruitment rates in abalone. J. Shellfish Res. 2013, 32:161-169.
62. Rossetto M., Micheli F., Saenz-Arroyo A., Espinoza-Montes J.A., De Leo G. No-take marine reserves can enhance population persistence and support the fishery of abalone. Canad. J. Aquatic Fish. Sci. 2015, in press.
63. Ryman N., Palm S., Andre C., Carvalho G.R., Dahlgren T.G., Jorde P.E., Laikre L., Larsson L.C., Palme A., Ruzzante D.E. Power for detecting genetic divergence: Differences between statistical methods and marker loci. Mol. Ecol. 2006, 15:2031-2045.
64. Schwartz M.K., Luikart G., Waples R.S. Genetic monitoring as a promising tool for conservation and management. Trends Ecol. Evolut. 2007, 22:25-33.
65. Searcy-Bernal R., Ramade-Villanueva M.R., Altamira B. Current status of abalone fisheries and culture in Mexico. J. Shellfish Res. 2010, 29:573-576.
66. Sgrò C.M., Lowe A.J., Hoffmann A.A. Building evolutionary resilience for conserving biodiversity under climate change. Evol. Appl. 2011, 4:326-337.
67. Shepherd S.A., Turrubiates J.R., Hall K. Decline of the abalone fishery at La Natividad, Mexico: Overfishing or climate change. J. Shellfish Res. 1998, 17:839-846.
68. Smith, M., Milic-Frayling, N., Shneiderman, B., Mendes-Rodriguez, E., Leskovec, J., Dunne, C., 2010. Nodexl: A free and open network overview, Discovery and Exploration Add-in for Excel 2007/2010 . http://nodexl.codeplex.com.
69. Stierhoff K.L., Neuman M., Butler J.L. On the road to extinction? Population declines of the endangered white abalone, Haliotis sorenseni. Biol. Conserv. 2012, 152:46-52.
70. Wang J. A new method for estimating effective population sizes from a single sample of multilocus genotypes. Mol. Ecol. 2009, 18:2148-2164.
71. Waples R.S. A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv. Genet. 2006, 7:167-184.
72. Waples R.S., Do C.H.I. Ldne: A program for estimating effective population size from data on linkage disequilibrium. Mol. Ecol. Resour. 2008, 8:753-756.
73. Watson J.R., Siegel D.A., Kendall B.E., Mitarai S., Rassweiller A., Gaines S.D. Identifying critical regions in small-world marine metapopulations. Proc. Natl. Acad. Sci. 2011, 108:E907-E913.
74. Worm B., Barbier E.B., Beaumont N., Duffy J.E., Folke C., Halpern B.S., Jackson J.B., Lotze H.K., Micheli F., Palumbi S.R., Sala E., Selkoe K.A., Stachowicz J.J., Watson R. Impacts of biodiversity loss on ocean ecosystem services. Science 2006, 314:787-790.
75. Wright S. The genetical structure of populations. Ann. Eugenics 1951, 15:323-354.