Selective exploitation of spatially structured coastal fish populations by recreational anglers may lead to evolutionary downsizing of adults

Marine Ecology Progress Series

Volumn 503, Issue , 2014, Pages 219-233

  Alós, Josep ^a,b   Palmer, Miquel ^a   Catalan, Ignacio A ^a   Alonso Fernández, Alexandre ^c   Basterretxea, Gotzon ^a   Jordi, Antoni ^a   Buttay, Lucie ^d   Morales Nin, Beatriz ^a   Arlinghaus, Robert ^b,e  

^a INSTITUTO MEDITERRÁNEO DE ESTUDIOS AVANZADOS   (Spain)

^b LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

^c INSTITUTO DE INVESTIGACIONES MARINAS   (Spain)

^d INSTITUTO ESPAÑOL DE OCEANOGRAFÍA   (Spain)

^e HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Body size; Function valued approach; Life history traits; Population connectivity; Recreational fishing; Selective fisheries

Indexed keywords

ADULT; ANGLING; BODY SIZE; COASTAL ZONE; CONNECTIVITY; DEVELOPMENTAL STAGE; EXPLOITATION; FISHING EFFORT; FISHING GEAR; GENOTYPE; HYDRODYNAMICS; ISOLATED POPULATION; LIFE HISTORY TRAIT; METAPOPULATION; PELAGIC ENVIRONMENT; PERCIFORM; POPULATION STRUCTURE;

EID: 84901218515     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps10745     Document Type: Article

References (94)

1. Allendorf FW, Hard JJ (2009) Human-induced evolution caused by unnatural selection through harvest of wild animals. Proc Natl Acad Sci USA 106: 9987-9994
2. Allendorf FW, England PR, Luikart G, Ritchie PA, Ryman N (2008) Genetic effects of harvest on wild animal populations. Trends Ecol Evol 23: 327-337
3. Alonso-Fernández A, Alós J, Grau A, Dominguez-Petit R, Saborido-Rey F (2011) The use of histological techniques to study the reproductive biology of the hermaphroditic Mediterranean fishes Coris julis, Serranus scriba, and Diplodus annularis. Mar Coast Fish 3: 145-159
4. Alós J, Arlinghaus R (2013) Impacts of partial marine protected areas on coastal fish communities exploited by recreational angling. Fish Res 137: 88-96
5. Alós J, Arlinghaus R, Palmer M, March D, Alvarez I (2009) The influence of type of natural bait on fish catches and hooking location in a mixed-species marine recreational fishery, with implications for management. Fish Res 97: 270-277
6. Alós J, Palmer M, Balle S, Grau AM, Morales-Nin B (2010) Individual growth pattern and variability in Serranus scriba: a Bayesian analysis. ICES J Mar Sci 67: 502-512
7. Alós J, Palmer M, Arlinghaus R (2012) Consistent selection towards low activity phenotypes when catchability depends on encounters among human predators and fish. PLoS ONE 7: e48030
8. Alós J, Alonso-Fernández A, Catalan I, Palmer M, Lowerre-Barbieri S (2013) Reproductive output traits of the simultaneous hermaphrodite Serranus scriba in the Western Mediterranean. Sci Mar 77: 331-340
9. Arlinghaus R, Matsumura S, Dieckmann U (2009) Quantifying selection differentials caused by recreational fishing: development of modeling framework and application to reproductive investment in pike (Esox lucius). Evol Appl 2: 335-355
10. Arnason E, Hernandez UB, Kristinsson K (2009) Intense habitat-specific fisheries-induced selection at the molecular Pan I Locus predicts imminent collapse of a major Cod fishery. PLoS ONE 4: e5529
11. Audzijonyte A, Kuparinen A, Fulton EA (2013a) How fast is fisheries-induced evolution? Quantitative analysis of modelling and empirical studies. Evol Appl 6: 585-595
12. Audzijonyte A, Kuparinen A, Gorton R, Fulton EA (2013b) Ecological consequences of body size decline in harvested fish species: positive feedback loops in trophic interactions amplify human impact. Biol Lett 9: 20121103
13. Basterretxea G, Jordi A, Catalán IA, Sabatés A (2012) Model-based assessment of local-scale fish larval connectivity in a network of marine protected areas. Fish Oceanogr 21: 291-306
14. Bevacqua D, Capoccioni F, Melià P, Vincenzi S, Pujolar JM, De Leo GA, Ciccotti E (2012) Fishery-induced selection for slow somatic growth in European eel. PLoS ONE 7: e37622
15. Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23: 361-368
16. Browman HI, Law R, Marshall CT (2008) The role of fisheries-induced evolution. Science 320: 47-50
17. Brunel T, Ernande B, Mollet FM, Rijnsdorp AD (2013) Estimating age at maturation and energy-based life-history traits from individual growth trajectories with nonlinear mixed-effects models. Oecologia 172: 631-643
18. Cabanellas-Reboredo M, Alós J, Palmer M, March D, Dor R (2012) Movement patterns of the European squid Loligo vulgaris during the inshore spawning season. Mar Ecol Prog Ser 466: 133-144
19. Carreras-Carbonell J, Macpherson E, Pascual M (2007) High self-recruitment levels in a Mediterranean littoral fish population revealed by microsatellite markers. Mar Biol 151: 719-727
20. Casabianca S, Penna A, Pecchioli E, Jordi A, Basterretxea G, Vernesi C (2012) Population genetic structure and connectivity of the harmful dinoflagellate Alexandrium minutum in the Mediterranean Sea. Proc R Soc Lond B Biol Sci 279: 129-138
21. Charnov EL (2005) Reproductive effort is inversely proportional to average adult life span. Evol Ecol Res 7: 1221-1222
22. Conover DO, Baumann H (2009) The role of experiments in understanding fishery-induced evolution. Evol Appl 2: 276-290
23. Conover DO, Munch SB (2002) Sustaining fisheries yields over evolutionary time scales. Science 297: 94-96
24. Cooke SJ, Suski CD, Ostrand KG, Wahl DH, Philipp DP (2007) Physiological and behavioral consequences of long-term artificial selection for vulnerability to recreational angling in a teleost fish. Physiol Biochem Zool 80: 480-490
25. Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311: 522-527
26. Craig JF, Kipling C (1983) Reproduction effort versus the environment; case histories of windermere perch, Perca fluviatilis L., and pike, Esox lucius L. J Fish Biol 22: 713-727
27. Cuveliers EL, Volckaert FAM, Rijnsdorp AD, Larmuseau MHD, Maes GE (2011) Temporal genetic stability and high effective population size despite fisheries-induced life-history trait evolution in the North Sea sole.Mol Ecol 20: 3555-3568
28. Deudero S, Morey G, Frau A, Moranta J, Moreno I (2008) Temporal trends of littoral fishes at deep Posidonia oceanica seagrass meadows in a temperate coastal zone. J Mar Syst 70: 182-195
29. Drake MT, Claussen JE, Philipp DP, Pereira DL (1997) A comparison of bluegill reproductive strategies and growth among lakes with different fishing intensities. N Am J Fish Manag 17: 496-507
30. Dunlop ES, Orendorff JA, Shuter BJ, Rodd FH, Ridgway MS (2005) Diet and divergence of introduced smallmouth bass (Micropterus dolomieu) populations. Can J Fish Aquat Sci 62: 1720-1732
31. Dunlop ES, Baskett ML, Heino M, Dieckmann U (2009) Propensity of marine reserves to reduce the evolutionary effects of fishing in a migratory species. Evol Appl 2: 371-393
32. Edeline E, Carlson SM, Stige LC, Winfield IJ and others (2007) Trait changes in a harvested population are driven by a dynamic tug-of-war between natural and harvest selection. Proc Natl Acad Sci USA 104: 15799-15804
33. Eikeset AM, Richter A, Dunlop ES, Dieckmann U, Stenseth NC (2013) Economic repercussions of fisheries-induced evolution. Proc Natl Acad Sci USA 110: 12259-12264
34. Ellison AM(2004) Bayesian inference in ecology. Ecol Lett 7: 509-520
35. Enberg K, Jørgensen C, Dunlop ES, Varpe O and others (2012) Fishing-induced evolution of growth: concepts, mechanisms and the empirical evidence. Mar Ecol 33: 1-25
36. 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. Aquat Conserv 11: 155-188
37. Galarza JA, Carreras-Carbonell J, Macpherson E, Pascual M, Roques S, Turner GF, Rico C (2009) The influence of oceanographic fronts and early-life-history traits on connectivity among littoral fish species. Proc Natl Acad Sci USA 106: 1473-1478
38. Heino M, Godo OR (2002) Fisheries-induced selection pressures in the context of sustainable fisheries. Bull Mar Sci 70: 639-656
39. Heino M, Baulier L, Bouka DS, Ernande B and others (2013) Can fisheries-induced evolution shift reference points for fisheries management? ICES J Mar Sci 70: 707-721
40. Hutchings JA (1993) Adaptive life histories effected by agespecific survival and growth rate. Ecology 74: 673-684
41. Jakobsdóttir KB, Pardoe H, Magnússon A, Björnsson H, Pampoulie C, Ruzzante DE, Marteinsdóttir G (2011) Historical changes in genotypic frequencies at the Pantophysin locus in Atlantic cod (Gadus morhua) in Icelandic waters: evidence of fisheries-induced selection? Evol Appl 4: 562-573
42. Johnston FD, Arlinghaus R, Dieckmann U (2013) Fish life history, angler behaviour and optimal management of recreational fisheries. Fish Fish 14: 554-579
43. Jones GP, Planes S, Thorrold SR (2005) Coral reef fish larvae settle close to home. Curr Biol 15: 1314-1318
44. Jørgensen C, Fiksen O (2009) Modelling fishing-induced adaptations and consequences for natural mortality. Can J Fish Aquat Sci 67: 1086-1097
45. Jørgensen C, Holt RE (2013) Natural mortality: its ecology, how it shapes fish life histories, and why it may be increased by fishing. J Sea Res 75: 8-18
46. Jørgensen C, Enberg K, Dunlop ES, Arlinghaus R and others (2007) Managing evolving fish stocks. Science 318: 1247-1248
47. Jørgensen C, Enberg K, Dunlop ES, Arlinghaus R and others (2008) Managing evolving fish stocks (Response). Science 320: 48-50
48. Kendall NW, Quinn TP (2011) Length and age trends of Chinook salmon in the Nushagak River, Alaska, related to commercial and recreational fishery selection and exploitation. Trans Am Fish Soc 140: 611-622
49. Klefoth T, Skov C, Krause J, Arlinghaus R (2012) The role of ecological context and predation risk-stimuli in revealing the true picture about the genetic basis of boldness evolution in fish. Behav Ecol Sociobiol 66: 547-559
50. Klefoth T, Pieterek T, Arlinghaus R (2013) Impacts of domestication on angling vulnerability of common carp (Cyprinus carpio L.): the role of learning, foraging behaviour and food preferences. Fish Manag Ecol 20: 174-186
51. Kough AS, Paris CB, Butler MJ (2013) Larval connectivity and the international management of fisheries. PLoS ONE 8: e64970
52. Kuparinen A, Merilä J (2007) Detecting and managing fisheries-induced evolution. Trends Ecol Evol 22: 652-659
53. Laugen AT, Engelhard GH, Whitlock R, Arlinghaus R and others (2014) Evolutionary impact assessment: accounting for evolutionary consequences of fishing in an ecosystem approach to fisheries management. Fish Fish 15: 65-96
54. Law R (2000) Fishing, selection, and phenotypic evolution. ICES J Mar Sci 57: 659-668
55. Lester NP, Shuter BJ, Abrams PA (2004) Interpreting the von Bertalanffy model of somatic growth in fishes: the cost of reproduction. Proc R Soc Lond B Biol Sci 271: 1625-1631
56. Lorenzen K, Enberg K (2002) Density-dependent growth as a key mechanism in the regulation of fish populations: evidence from among-population comparisons. Proc R Soc Lond B Biol Sci 269: 49-54
57. Macpherson E, Raventos N (2006) Relationship between pelagic larval duration and geographic distribution of Mediterranean littoral fishes. Mar Ecol Prog Ser 327: 257-265
58. March D, PalmerM, Alós J, Grau A, Cardona F (2010) Shortterm residence, home range size and diel patterns of the painted comber Serranus scriba in a temperate marine reserve. Mar Ecol Prog Ser 400: 195-206
59. Matsumura S, Arlinghaus R, Dieckmann U (2011) Assessing evolutionary consequences of size-selective recreational fishing on multiple life-history traits, with an application to northern pike (Esox lucius). Evol Ecol 25: 711-735
60. McDermid JL, Shuter BJ, Lester NP (2010) Life history differences parallel environmental differences among North American lake trout (Salvelinus namaycush) populations. Can J Fish Aquat Sci 67: 314-325
61. Mollet FM, Ernande B, Brunel T, Rijnsdorp AD (2010) Multiple growth-correlated life history traits estimated simultaneously in individuals. Oikos 119: 10-26
62. Mora C, Sale PF (2002) Are populations of coral reef fish open or closed? Trends Ecol Evol 17: 422-428
63. Morales-Nin B, Moranta J, Garcia C, Tugores MP, Grau AM, Riera F, Cerda M (2005) The recreational fishery off Majorca Island (western Mediterranean): some implications for coastal resource management. ICES J Mar Sci 62: 727-739
64. Moranta J, Palmer M, Morey G, Ruiz A, Morales-Nin B (2006) Multi-scale spatial variability in fish assemblages associated with Posidonia oceanica meadows in the Western Mediterranean Sea. Estuar Coast Shelf Sci 68: 579-592
65. Olsen E, Moland E (2011) Fitness landscape of Atlantic cod shaped by harvest selection and natural selection. Evol Ecol 25: 695-710
66. Olsen EM, Heino M, Lilly GR, Morgan MJ, Brattey J, Ernande B, Dieckmann U (2004) Maturation trends indicative of rapid evolution preceded the collapse of northern cod. Nature 428: 932-935
67. Palumbi SR, Warner RR (2003) Why gobies are like hobbits. Science 299: 51-52
68. Pelc RA, Warner RR, Gaines SD, Paris CB (2010) Detecting larval export from marine reserves. Proc Natl Acad Sci USA 107: 18266-18271
69. Philipp DP, Cooke SJ, Claussen JE, Koppelman JB, Suski CD, Burkett DP (2009) Selection for vulnerability to angling in Largemouth Bass. Trans Am Fish Soc 138: 189-199
70. Pilling GM, Kirkwood GP, Walker SG (2002) An improved method for estimating individual growth variability in fish, and the correlation between von Bertalanffy growth parameters. Can J Fish Aquat Sci 59: 424-432
71. Plummer M, Best N, Cowles K, Vines K (2006) CODA: convergence diagnosis and output analysis for MCMC. R News 6: 7-11
72. Pukk L, Kuparinen A, Järv L, Gross R, Vasemägi A (2013) Genetic and life-history changes associated with fisheries-induced population collapse. Evol Appl 6: 749-760
73. Quince C, Abrams PA, Shuter BJ, Lester NP (2008a) Biphasic growth in fish. I. Theoretical foundations. J Theor Biol 254: 197-206
74. Quince C, Shuter BJ, Abrams PA, Lester NP (2008b) Biphasic growth in fish. II. Empirical assessment. J Theor Biol 254: 207-214
75. Redpath TD, Cooke SJ, Arlinghaus R, Wahl DH, Philipp DP (2009) Life-history traits and energetic status in relation to vulnerability to angling in an experimentally selected teleost fish. Evol Appl 2: 312-323
76. Redpath TD, Cooke SJ, Suski CD, Arlinghaus R, Couture P, Wahl DH, Philipp DP (2010) The metabolic and biochemical basis of vulnerability to recreational angling after three generations of angling-induced selection in a teleost fish. Can J Fish Aquat Sci 67: 1983-1992
77. Reñones O, Goñi R, Pozo M, Deudero S, Moranta J (1999) Effects of protection on the demographic structure and abundance of Epinephelus marginatus (Lowe, 1834). Evidence from Cabrera Archipelago National Park (West-central Mediterranean). Mar Life 9: 45-53
78. Reznick D (1982) The impact of predation on life history evolution in Trinidadian guppies: genetic basis of observed life history patterns. Evolution 36: 1236-1250
79. Reznick DA, Bryga H, Endler JA (1990) Experimentally induced life-history evolution in a natural population. Nature 346: 357-359
80. Roberts CM (1997) Connectivity and management of Caribbean coral reefs. Science 278: 1454-1457
81. Roff DA (1984) The evolution of life history parameters in teleosts. Can J Fish Aquat Sci 41: 989-1000
82. Saura M, Moran P, Brotherstone S, Caballero A, Alvarez J, Villanueva B (2010) Predictions of response to selection caused by angling in a wild population of Atlantic salmon (Salmo salar). Freshw Biol 55: 923-930
83. Shuter BJ, Lester NP, LaRose J, Purchase CF and others (2005) Optimal life histories and food web position: linkages among somatic growth, reproductive investment, and mortality. Can J Fish Aquat Sci 62: 738-746
84. Stinchcombe JR, Kirkpatrick M (2012) Genetics and evolution of function-valued traits: understanding environmentally responsive phenotypes. Trends Ecol Evol 27: 637-647
85. Sutter DAH, Suski CD, Philipp DP, Klefoth T and others (2012) Recreational fishing selectively captures individuals with the highest fitness potential. Proc Natl Acad Sci USA 109: 20960-20965
86. Swain DP, Sinclair AF, Mark Hanson J (2007) Evolutionary response to size-selective mortality in an exploited fish population. Proc R Soc Lond B 274: 1015-1022
87. Teacher AGF, André C, Jonsson PR, Merilä J (2013) Oceanographic connectivity and environmental correlates of genetic structuring in Atlantic herring in the Baltic Sea. Evol Appl 6: 549-567
88. Uusi-Heikkilä S, Wolter C, Klefoth T, Arlinghaus R (2008) A behavioral perspective on fishing-induced evolution. Trends Ecol Evol 23: 419-421
89. Walsh MR, Munch SB, Chiba S, Conover DO (2006) Maladaptive changes in multiple traits caused by fishing: impediments to population recovery. Ecol Lett 9: 142-148
90. Walters C, Martell SJD (2004) Fisheries ecology and management. Princeton University Press, Princeton, NJ
91. Watson JR, Hays CG, Raimondi PT, Mitarai S and others (2011) Currents connecting communities: nearshore community similarity and ocean circulation. Ecology 92: 1193-1200
92. Wilson ADM, Binder TR, McGrath KP, Cooke SJ, Godin JGJ (2011) Capture technique and fish personality: angling targets timid bluegill sunfish, Lepomis macrochirus. Can J Fish Aquat Sci 68: 749-757
93. Wright PJ, Millar CP, Gibb FM (2011) Intrastock differences in maturation schedules of Atlantic cod, Gadus morhua. ICES J Mar Sci 68: 1918-1927
94. Zuur AF, Leno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer-Verlag, New York, NY