Extreme increases in natural mortality prevent recovery of collapsed fish populations in a Northwest Atlantic ecosystem

Marine Ecology Progress Series

Volumn 519, Issue , 2015, Pages 165-182

  Swain, Douglas P ^a   Benoît, Hugues P ^a  

^a GULF FISHERIES CENTRE   (Canada)

Author keywords

Allee effect; Marine fishes; Natural mortality; Population recovery; Predation

Indexed keywords

ABUNDANCE; ADAPTATION; DEMERSAL FISH; EXPLOITATION; MARINE ECOSYSTEM; MORTALITY RISK; POPULATION DECLINE; PREDATION RISK;

ATLANTIC OCEAN; ATLANTIC OCEAN (NORTHWEST);

HALICHOERUS GRYPUS; MAMMALIA; PISCES;

EID: 84921902101     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps11012     Document Type: Article

References (94)

1. Beck CA, Iverson SJ, Bowen WD, Blanchard W (2007) Sex differences in grey seal diet reflect seasonal variation in foraging behaviour and reproductive expenditure: evidence from quantitative fatty acid signature analysis. J Anim Ecol 76:490-502
2. Benoît HP (2006) Standardizing the southern Gulf of St. Lawrence bottom-trawl survey time series: results of the 2004-2005 comparative fishing experiments and other recommendations for the analysis of the survey data. DFO Can Sci Adv Sec Res Doc 2006/008. Fisheries and Oceans Canada, Ottawa
3. Benoît HP (2013a) An empirical model of seasonal depth-dependent fish assemblage structure to predict the species composition of mixed catches. Can J Fish Aquat Sci 70:220-232
4. Benoît HP (2013b) Two decades of annual landed and discarded catches of three southern Gulf of St. Lawrence skate species estimated under multiple sources of uncertainty. ICES J Mar Sci 70:554-563
5. Benoît D, Bowen WD (1990) Seasonal and geographic variation in the diet of grey seals (Halichoerus grypus) in eastern Canada. Can Bull Fish Aquat Sci 222:215-226
6. Benoît HP, Swain DP (2003) Standardizing the southern Gulf of St. Lawrence bottom-trawl survey time series: adjusting for changes in research vessel, gear and survey protocol. Can Tech Rep Fish Aquat Sci No. 2505. Fisheries and Oceans Canada, Ottawa
7. Benoît HP, Swain DP (2008) Impacts of environmental change and direct and indirect harvesting effects on the dynamics of a marine fish community. Can J Fish Aquat Sci 65:2088-2104
8. Benoît HP, Hammill MO, Swain, DP (2011a) Estimated consumption of southern Gulf of St. Lawrence cod by grey seals: bias, uncertainty and two proposed approaches. DFO Can Sci Advis Sec Res Doc 2011/041. Fisheries and Oceans Canada, Ottawa
9. Benoît HP, Swain DP, Bowen WD, Breed GA, Hammill MO, Harvey V (2011b) Evaluating the potential for grey seal predation to explain elevated natural mortality in three fish species in the southern Gulf of St. Lawrence. Mar Ecol Prog Ser 442:149-167
10. Benoît HP, Swain DP, Hammill MO (2011c) A risk analysis of the potential effects of selective and non-selective reductions in grey seal abundance on the population status of two species at risk of extirpation, white hake and winter skate in the southern Gulf of St. Lawrence. DFO Can Sci Advis Sec Res Doc 2011/033. Fisheries and Oceans Canada, Ottawa
11. Benoît HP, Swain DP, Hammill MO (2011d) Seasonal patterns in the spatial overlap of southern Gulf of St. Lawrence cod and grey seals, with a discussion of sources of error and possible bias. DFO Can Sci Advis Sec Res Doc 2011/018. Fisheries and Oceans Canada, Ottawa
12. Benoît HP, Gagné JA, Savenkoff C, Ouellet P, Bourassa MN (eds) (2012) State-of-the-Ocean Report for the Gulf of St. Lawrence Integrated Management (GOSLIM) Area. Can Manuscr Rep Fish Aquat Sci 2986. Fisheries and Oceans Canada, Ottawa
13. Beverton RJH (1965) Catch effort of some ICNAF fisheries. Res Bull Int Comm Northwest Atl Fish 2:59-72
14. Beverton RJH, Hylen A, Ostvedt OJ (1994) Growth, maturation, and longevity of maturation cohorts of Northeast Arctic cod. ICES J Mar Sci Symp 198:482-501
15. Bourbeau-Lemieux A, Festa-Bianchet M, Gaillard JM, Pelletier F (2011) Predation-driven component Allee effects in a wild ungulate. Ecol Lett 14:358-363
16. Bousquet N, Cadigan N, Duchesne T, Rivest LP (2010) Detecting and correcting underreported catches in fish stock assessment: trial of a new method. Can J Fish Aquat Sci 67:1247-1261
17. Butchart SHM, Walpole M, Collen B, van Strien A and others (2010) Global biodiversity: indicators of recent declines. Science 328:1164-1168
18. Chouinard GA, Swain DP, Hammill MO, Poirier GA (2005) Covariation between grey seal (Halichoerus grypus) abundance and natural mortality of cod (Gadus morhua) in the southern Gulf of St. Lawrence. Can J Fish Aquat Sci 62:1991-2000
19. Clay D (1991) Seasonal distribution of demersal fish (Osteichthyes) and skates (Chondrichthyes) in the southeastern Gulf of St. Lawrence. In: Therriault JC (ed) The Gulf of St Lawrence: small ocean or big estuary? Can Spec Publ Fish Aquat Sci 113:241-259
20. COSEWIC (2005) COSEWIC assessment and status report on the winter skate Leucoraja ocellata in Canada. Committee on the Status of Endangered Wildlife in Canada, Ottawa. Available at www.sararegistry.gc.ca/status/ status-e.cfm
21. Costa DP, Weise MJ, Arnould JPY (2006) Potential influences of whaling on the status and trends of pinniped populations. In: Estes JA, DeMaster DP, Doak DF, Williams TM, Brownell RLJ (eds) Whales, whaling and ocean ecosystems. University of California Press, Berkeley, CA, p 344-359
22. Courchamp F, Clutton-Brock T, Grenfell B (1999) Inverse density dependence and the Allee effect. Trends Ecol Evol 14:405-410
23. Courchamp F, Berek L, Gascoigne J (2008) Allee effects in ecology and conservation. Oxford University Press, Oxford
24. DFO (Fisheries and Oceans Canada) (2011) Impacts of grey seals on fish populations in eastern Canada. DFO Can Sci Advis Sec Sci Advis Rep 2010/071. Fisheries and Oceans Canada, Ottawa
25. DFO (Fisheries and Oceans Canada) (2014) Stock Assessment of Canadian Grey Seals (Halichoerus grypus). DFO Can Sci Advis Sec Sci Advis Rep 2014/010. Fisheries and Oceans Canada, Ottawa
26. Dickie LM (1963) Estimation of mortality rates of Gulf of St. Lawrence cod from results of a tagging experiment. Spec Publ Int Comm Northwest Atl Fish 4:71-80
27. Dutil JD, Lambert Y (2000) Natural mortality from poor condition in Atlantic cod (Gadus morhua). Can J Fish Aquat Sci 57:826-836
28. Ernande B, Dieckmann U, Heino M (2004) Adaptive changes in harvested populations: plasticity and evolution of age and size at maturation. Proc R Soc B 271:415-423
29. Fournier DA, Skaug HJ, Ancheta J, Ianelli J and others (2011) AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:233-249
30. Fu C, Quinn TJ II (2000) Estimability of natural mortality and other population parameters in a length based model: Pandalus borealis in Kachemak Bay, Alaska. Can J Fish Aquat Sci 57:2420-2432
31. Gascoigne JC, Lipcius RN (2004) Allee effects driven by predation. J Appl Ecol 41:801-810
32. Gislason H, Daan N, Rice JC, Pope JG (2010) Size, growth, temperature and the natural mortality of marine fish. Fish Fish 11:149-158
33. Hammill MO, Stenson GB, Proust F, Carter P, McKinnon D (2007) Feeding by grey seals in the Gulf of St. Lawrence and around Newfoundland. In: Haug T, Hammill M, Olafsdottir D (eds) Grey seals in the North Atlantic and the Baltic. NAMMCO Sci Publ 6, Tromsø, p 135-152
34. Hammill MO, Stenson GB, Swain DP, Benoît HP (2014) Feeding by grey seals on endangered stocks of Atlantic cod and white hake. ICES J Mar Sci 71:1332-1341
35. Harvey V, Hammill MO, Swain DP, Breed GA, Lydersen C, Kovacs KM (2012) Winter foraging by a top predator, the grey seal Halichoerus grypus, in relation to the distribution of prey. Mar Ecol Prog Ser 462:273-286
36. Hilborn R, Litzinger E (2009) Causes of decline and potential for recovery of Atlantic cod populations. Open Fish Sci J 2:32-38
37. Hoenig JM (1983) Empirical use of longevity data to estimate mortality rates. Fish Bull 81:898-903
38. Hutchings JA (1994) Age- and size-specific costs of reproduction within populations of brook trout, Salvelinus fontinalis. Oikos 70:12-20
39. Hutchings JA (2000) Collapse and recovery of marine fishes. Nature 406:882-885
40. Hutchings JA (2005) Life history consequences of overexploitation to population recovery in Northwest Atlantic cod (Gadus morhua). Can J Fish Aquat Sci 62:824-832
41. Hutchings JA (2014) Renaissance of a caveat: Allee effects in marine fish. ICES J Mar Sci 71:2152-2157
42. Hutchings JA, Baum JK (2005) Measuring marine fish biodiversity: temporal changes in abundance, life history and demography. Philos Trans R Soc B Biol Sci 360:315-338
43. Hutchings JA, Fraser DF (2008) The nature of fisheries- and farming-induced evolution. Mol Ecol 17:294-313
44. Hutchings JA, Rangeley RW (2011) Correlates of recovery for Canadian Atlantic cod. Can J Zool 89:386-400
45. Hutchings JA, Reynolds JD (2004) Marine fish population collapses: consequences for recovery and extinction risk. Bioscience 54:297-309
46. Hutchings JA, Butchart SHM, Collen B, Schwartz MK, Waples RS (2012) Red flags: correlates of impaired species recovery. Trends Ecol Evol 27:542-546
47. Jiao Y, Smith EP, O'Reilly R, Orth DJ (2012) Modelling non-stationary natural mortality in catch-at-age models. ICES J Mar Sci 69:105-118
48. Jørgensen C, Fiksen Ø (2010) Modelling fishing-induced adaptations and consequences for natural mortality. Can J Fish Aquat Sci 67:1086-1097
49. Jørgensen C, Holt R (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
50. Keith DM, Hutchings JA (2012) Population dynamics of marine fishes at low abundance. Can J Fish Aquat Sci 69:1150-1163
51. Kuparinen A, Merilä J (2007) Detecting and managing fisheries-induced evolution. Trends Ecol Evol 22:652-659
52. Lambert Y, Dutil JD (1997) Condition and energy reserves of Atlantic cod (Gadusmorhua) during the collapse of the northern Gulf of St. Lawrence stock. Can J Fish Aquat Sci 54:2388-2400
53. Lavigueur L, Hammill MO (1993) Distribution and seasonal movements of grey seals, Halichoerus grypus, born in the Gulf of St. Lawrence and eastern Nova Scotia shore. Can Field Nat 107:329-340
54. Lee HH, Maunder MN, Piner KR, Methot RD (2011) Estimating natural mortality within a fisheries stock assessment model: an evaluation using simulation analysis based on twelve stock assessments. Fish Res 109:89-94
55. McIntyre TM, Hutchings JA (2003) Small-scale temporal and spatial variation in Atlantic cod (Gadus morhua) life history. Can J Fish Aquat Sci 60:1111-1121
56. Minto C, Worm B (2012) Interactions between small pelagic fish and young cod across the North Atlantic. Ecology 93:2139-2154
57. Minto C, Mills Flemming J, Britten GL, Worm B (2014) Productivity dynamics of Atlantic cod. Can J Fish Aquat Sci 71:203-216
58. Morin R (2012) Estimating the age composition of discards in the NAFO 4T American plaice fishery. DFO Can Sci Advis Sec Res Doc 2012/081. Fisheries and Oceans Canada, Ottawa
59. Morin R, LeBlanc SG (2012) Assessment of the southern Gulf of St. Lawrence (NAFO Division 4T) American plaice (Hippoglossoides platessoides). DFO Can Sci Advis Sec Res Doc 2012/099. Fisheries and Oceans Canada, Ottawa
60. Morin R, Swain DP, LeBlanc SG (2012) A biomass Limit Reference Point for the NAFO 4T American plaice (Hippo glos so ides platessoides) fishery. DFO Can Sci Advis Sec Res Doc 2012/108. Fisheries and Oceans Canada, Ottawa
61. Neubauer P, Jensen OP, Hutchings JA, Baum JK (2013) Resilience and recovery of overexploited marine populations. Science 340:347-349
62. Nicholson AJ (1933) The balance of animal populations. J Anim Ecol 2:131-178
63. O'Boyle R, Sinclair M (2012) Seal-cod interactions on the Eastern Scotian Shelf: reconsideration of modelling assumptions. Fish Res 115-116:1-13
64. 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
65. Paloheimo JE, Kohler AC (1968) Analysis of the southern Gulf of St. Lawrence cod population. J Fish Res Board Can 25:555-578
66. Pauly D (1980) On the interrelationships between natural mortality, growth parameters, and mean environmental temperature in 175 fish stocks. J Cons Int Explor Mer 39:175-192
67. Power D, Morgan J, Murphy EF, Brattey J, Healey B (2010) An assessment of the cod stock in NAFO Divisions 3NO. NAFO SCR Doc No 10/42. Fisheries and Oceans Canada, Ottawa
68. Reznick D (1985) Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257-267
69. Roff DA (2002) Life history evolution. Sinauer, Sunderland, MA
70. Rosenberg AA, Bolster WJ, Alexander KE, Leavenworth WB, Cooper AB, McKenzie MG (2005) The history of ocean resources: modeling cod biomass using historical records. Front Ecol Environ 3:84-90
71. Rowe S, Hutchings JA, Bekkevold D, Rakitin A (2004) Depensation, probability of fertilization, and the mating system of Atlantic cod (Gadus morhua L.). ICES J Mar Sci 61:1144-1150
72. Shelton PA, Sinclair AF, Chouinard GA, Mohn R, Duplisea DE (2006) Fishing under low productivity conditions is further delaying recovery of Northwest Atlantic cod (Gadus morhua). Can J Fish Aquat Sci 63:235-238
73. Sih A (1980) Optimal foraging: partial consumption of prey. Am Nat 116:281-290
74. Sinclair AF (1998) Estimating trends in fishing mortality at age and length directly from research surveys and commercial catch data. Can J Fish Aquat Sci 55:1248-1263
75. Sinclair AF (2001) Natural mortality of cod (Gadus morhua) in the Southern Gulf of St. Lawrence. ICES J Mar Sci 58:1-10
76. Smout S, Rindorf A, Hammond PS, Harwood J, Matthiopoulos J (2014) Modelling prey consumption and switching by UK grey seals. ICES J Mar Sci 71:81-89
77. Stephens PA, Sutherland WJ (1999) Consequences of the Allee effect for behaviour, ecology and conservation. Trends Ecol Evol 14:401-405
78. Swain DP (1993) Age- and density-dependent bathymetric pattern of Atlantic cod (Gadus morhua) in the southern Gulf of St. Lawrence. Can J Fish Aquat Sci 50:1255-1264
79. Swain DP (1999) Changes in the distribution of Atlantic cod (Gadus morhua) in the southern Gulf of St. Lawrence - effects of environmental change or change in environmental preferences? Fish Oceanogr 8:1-17
80. Swain DP (2011a) Natural mortality and projected biomass of southern Gulf of St. Lawrence cod. DFO Can Sci Advis Sec Res Doc 2011/040. Fisheries and Oceans Canada, Ottawa
81. Swain DP (2011b) Life-history evolution and elevated natural mortality in a population of Atlantic cod (Gadus morhua). Evol Appl 4:18-29
82. Swain DP, Benoît HP (2006) Change in habitat associations and geographic distribution of thorny skate (Amblyraja radiata) in the southern Gulf of St. Lawrence: density-dependent habitat selection or response to environmental change? Fish Oceanogr 15:166-182
83. Swain DP, Chouinard GA (2008) Predicted extirpation of the dominant demersal fish in a large marine ecosystem: Atlantic cod (Gadus morhua) in the southern Gulf of St. Lawrence. Can J Fish Aquat Sci 65:2315-2319
84. Swain DP, Mohn RK (2012) Forage fish and the factors governing recovery of Atlantic cod (Gadus morhua) on the eastern Scotian Shelf. Can J Fish Aquat Sci 69:997-1001
85. Swain DP, Sinclair AF (2000) Pelagic fishes and the cod recruitment dilemma in the Northwest Atlantic. Can J Fish Aquat Sci 57:1321-1325
86. Swain DP, Hurlbut T, Benoît HP (2005) Changes in the abundance and size of skates in the southern Gulf of St. Lawrence, 1971-2002. J Northwest Atl Fish Sci 36:19-30
87. Swain DP, Jonsen ID, Simon JE, Myers RA (2009) Assessing threats to species-at-risk using stage-structured state-space models: mortality trends in skate populations. Ecol Appl 19:1347-1364
88. Swain DP, Benoît HP, Hammill MO, McClelland G, Aubry É (2011a) Alternative hypotheses for causes of the elevated natural mortality of cod (Gadus morhua) in the southern Gulf of St. Lawrence: the weight of evidence. DFO Can Sci Advis Sec Res Doc 2011/036. Fisheries and Oceans Canada, Ottawa
89. Swain DP, Benoît HP, Savoie L, Surette T (2011b) Can poor fish condition explain the elevated natural mortality of cod and other marine fish in the southern Gulf of St. Lawrence? DFO Can Sci Advis Sec Res Doc 2011/037. Fisheries and Oceans Canada, Ottawa
90. Swain DP, Hurlbut TR, Benoît HP (2012a) Pre-COSEWIC review of variation in the abundance, distribution and productivity of white hake (Urophycis tenuis) in the southern Gulf of St. Lawrence, 1971-2010. DFO Can Sci Advis Sec Res Doc 2012/066. Fisheries and Oceans Canada, Ottawa
91. Swain DP, Savoie L, Aubry É (2012b) Recovery Potential Assessment for the Laurentian South designatable unit of Atlantic Cod (Gadus morhua): the southern Gulf of St. Lawrence cod stock (NAFO Div. 4T-4Vn(Nov-Apr)). DFO Can Sci Advis Sec Res Doc 2012/052. Fisheries and Oceans Canada, Ottawa
92. Swain DP, Jonsen ID, Simon JE, Davies TD (2013) Contrasting decadal trends in mortality between large and small individuals in skate populations in Atlantic Canada. Can J Fish Aquat Sci 70:74-89
93. Walters C, Kitchell JF (2001) Cultivation/depensation effects on juvenile survival and recruitment: implications for the theory of fishing. Can J Fish Aquat Sci 58:39-50
94. Worm B, Hilborn R, Baum JK, Branch TA and others (2009) Rebuilding global fisheries. Science 325:578-585