Post-release fishing mortality of blue (Prionace glauca) and silky shark (Carcharhinus falciformes) from a Palauan-based commercial longline fishery

Abstract

Accounting for components of fishing mortality, including post-release mortality (Fr), is necessary for robust assessments of the effects of fishing. Forty-eight blue (Prionace glauca) and 35 silky sharks (Carcharhinus falciformes) were tagged with pop-up satellite archival tags to monitor Fr rates from pelagic longline vessels in the western tropical Pacific Ocean. There is a paucity of Fr studies at low latitudes and identifying factors that significantly explain Fr is critical for understanding fishing mortality. Mean Fr rates were 0.17 [95% CI 0.09–0.30] for blue shark and 0.20 [95% CI 0.10–0.36] for silky shark. When it occurred, Fr was acute with 87% of mortalities within 2 days of release. Several prognostic operational, environmental, biological and handling variables were evaluated to assess their influence on survival outcomes. Using Kaplan–Meier survival curves, logistic regression, accelerated failure time and Cox proportional hazards models to screen variables, the only significant prognostic or risk variable was health condition at haulback. There was close correspondence (~ 83% accuracy) between condition at capture and survival outcomes. Reliable methods to classify at-vessel condition represent an inexpensive and simple metric for estimating both Fr and at-vessel (Fc) mortality rates. Examining Fc rates in detail in longline fisheries using capture information on depth, temperature and dissolved oxygen that may act in synergy with condition code and hooking duration is a research priority. Results suggest that a large proportion of shark survive following release and that Fr rates can be increased by improving the haulback condition of captured sharks.

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References

  1. Achhammer BG, Reinhart FW, Kline GM (1951) Mechanism of the degradation of polyamides. J Res Nat Bur Stan 46(5):391–421

    CAS  Article  Google Scholar 

  2. Adams DH, Borucinska JD, Maillett K, Whitburn K, Sander TE (2015) Mortality due to a retained circle hook in a longfin mako shark Isurus paucus (Guitart-Manday). J Fish Dis 38:621–628. https://doi.org/10.1111/jfd.12277

    PubMed  CAS  Article  Google Scholar 

  3. Agresti A (2002) Categorical data analysis, 2nd edn. Wiley, Hoboken

    Google Scholar 

  4. Aires-da-Silva A, Taylor I, Punt AE, Gallucci VF, Kohler NE, Turner Turner PA, Briggs R, Hoey JJ (2005) A framework for estimating movement and fishing mortality rates of the blue shark, Prionace glauca, in the North Atlantic from tag-recapture data. Col Vol Sci Pap ICCAT 58:1073–1086

    Google Scholar 

  5. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723

    Article  Google Scholar 

  6. Allain V, Kerandel J, Andrefouet S, Magron F, Clark M, Kirby D, Muller-Karger F (2008) Enhanced seamount location database for the Western and Central Pacific Ocean: screening and crosschecking of 20 existing datasets. Deep-Sea Res I 55:1035–1047

    Article  Google Scholar 

  7. Allison PD (2010) Survival analysis using SAS®: a practical guide, 2nd edn. SAS Institute, Cary

    Google Scholar 

  8. Angilletta MJ Jr (2009) Thermal adaptation, a theoretical and empirical synthesis. Oxford University Press, Oxford

    Google Scholar 

  9. Awruch CA, Simpfendorfer C, Pankhurst NW (2011) Evaluation and use of a portable field kit for measuring whole-blood lactate in sharks. Mar Freshw Res 62:694–699

    CAS  Article  Google Scholar 

  10. Bartholomew A, Bohnsack JA (2005) A review of catch-and-release angling mortality with implications for no-take reserves. Rev Fish Biol Fish 15:129–154

    Article  Google Scholar 

  11. Baum JK, Worm B (2009) Cascading top-down effects of changing oceanic predator abundances. J Anim Ecol 78:699–714

    PubMed  Article  Google Scholar 

  12. Baum JK, Myers RA, Kehler DG, Worm B, Harley SJ, Doherty PA (2003) Collapse and conservation of shark populations in the Northwest Atlantic. Science 299:389–392

    PubMed  CAS  Article  Google Scholar 

  13. Bell JP, Satchell GH (1963) An undescribed unilateral ocular reflex in the dogfish Squalus acanthias L. Aust J Exp Biol Med Sci 41:221–234

    PubMed  CAS  Article  Google Scholar 

  14. Benoît HP, Hurlbut T, Chasse J, Jonsen ID (2012) Estimating fishery-scale rates of discard mortality using conditional reasoning. Fish Res 125–126:318–330

    Article  Google Scholar 

  15. Benoît HP, Capizzano CW, Knotek RJ, Rudders DB, Sulikowski JA, Dean MJ, Hoffman W, Zemeckis DR, Mandelman JW (2015) A generalized model for longitudinal short- and long-term mortality data for commercial fishery discards and recreational fishery catch-and-releases. ICES J Mar Sci 72:1834–1847

    Article  Google Scholar 

  16. Borucinska JD, Martin J, Skomal G (2001) Peritonitis and pericarditis associated with gastric perforation by a retained fishing hook in a blue shark (Prionace glauca). J Aquat Animal Health 13(4):347–354

    Article  Google Scholar 

  17. Borucinska J, Kohler N, Natanson L, Skomal G (2002) Pathology associated with retained fishing hooks in blue sharks, Prionace glauca (L.), with implications for their conservation. J Fish Diseases 25(9):515–521

    Article  Google Scholar 

  18. Braccini M, Van Rijn J, Frick L (2012) High post-capture survival for sharks, rays and chimaeras discarded in the main shark fishery of Australia? PLoS ONE 7(2):e32547. https://doi.org/10.1371/journal.pone.0032547

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  19. Brodziak J, Gedamke T, Porch C, Walter J, Courtney D, O’Malley J, Richards B (2012) A workshop on methods to estimate total and natural mortality rates using mean length observations and life history parameters. U.S. Dep. Commer., NOAA Tech. Memo., NOAA-TM-NMFS-PIFSC-32, 26 p. + Appendix

  20. Burgess MG, Polasky S, Tilman D (2013) Predicting overfishing and extinction threats in multispecies fisheries. Proc Natl Acad Sci 110:15943–15948. https://doi.org/10.1073/pnas.1314472110

    PubMed  Article  Google Scholar 

  21. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  22. Butcher PA, Peddemors VM, Mandelman JW, McGrath SP, Cullis BR (2015) At-vessel mortality and blood biochemical status of elasmobranchs caught in an Australian commercial longline fishery. Global Ecol Con 3:878–889. https://doi.org/10.1016/j.gecco.2015.04.012

    Article  Google Scholar 

  23. Camhi MD (2008) Conservation status of pelagic elasmobranchs. In: Camhi MD, Pikitch EK, Babcock EA (eds) Sharks of the open ocean: biology, fisheries and conservation. Blackwell, Oxford, pp 397–417

    Google Scholar 

  24. Campana S, Joyce W, Manning M (2009a) Bycatch and discard mortality in commercially caught blue sharks Prionace glauca assessed using archival satellite pop-up tags. Mar Ecol Prog Ser 387:241–253. https://doi.org/10.3354/meps08109

    Article  Google Scholar 

  25. Campana SE, Joyce W, Francis MP, Manning MJ (2009b) Comparability of blue shark mortality estimates for the Atlantic and Pacific longline fisheries. Mar Ecol Prog Ser 396:161–164

    Article  Google Scholar 

  26. Campana SE, Joyce W, Fowler M, Showell M (2015) Discards, hooking, and post-release mortality of porbeagle (Lamna nasus), shortfin mako (Isurus oxyrinchus), and blue shark (Prionace glauca) in the Canadian pelagic longline fishery. ICES J Mar Sci. https://doi.org/10.1093/icesjms/fsv234

    Article  Google Scholar 

  27. Carey FG, Scharold JV (1990) Movements of blue sharks (Prionace glauca) in depth and course. Mar Biol 106:329–342

    Article  Google Scholar 

  28. Carruthers EH, Schneider DC, Neilson JD (2009) Estimating the odds of survival and identifying mitigation opportunities for common bycatch in pelagic longline fisheries. Biol Conserv 142(11):2620–2630. https://doi.org/10.1016/j.biocon.2009.06.010

    Article  Google Scholar 

  29. Carver RP (1978) The case against statistical significance testing. Harv Educ Rev 48(3):378–399. https://doi.org/10.2307/20152382

    Article  Google Scholar 

  30. Carver RP (1993) The case against statistical significance testing, revisited. J Exp Educ 61(4):287–292. https://doi.org/10.1080/00220973.1993.10806591

    Article  Google Scholar 

  31. Clarke S, Sato M, Small C, Sullivan B, Inoue Y, Ochi D (2014) Bycatch in longline fisheries for tuna and tuna-like species: a global review of status and mitigation measures. FAO Fisheries and Aquaculture Technical Paper, N°588, 125 pp. FAO Fisheries and Aquaculture Technical Paper, 588, Rome

  32. Clarke CR, Karl SA, Horn RL, Bernard AM, Lea JL, Hazin FH, Prodöhl PA, Shivji MS (2015) Global mitochondrial DNA phylogeography and population structure of silky shark Carcharhinus falciformis. Mar Biol. https://doi.org/10.1007/s00227-015-2636-6

    Article  Google Scholar 

  33. Collett D (2014) Modelling survival data in medical research, 3rd edn. Chapman and Hall, New York

    Google Scholar 

  34. Cortés E (2002) Incorporating uncertainty into demographic modeling: application to shark populations and their conservation. Consev Biol 16:1048–1062

    Article  Google Scholar 

  35. Courchamp F, Berec L, Gascoigne (2008) Allee effects in ecology and conservation. Oxford University Press, Oxford

    Google Scholar 

  36. Cowan N (2001) The magical number 4 in short term memory. A reconsideration of storage capacity. Behav Brain Sci 24(4):87–186. https://doi.org/10.1017/S0140525X01003922

    PubMed  CAS  Article  Google Scholar 

  37. Cox DR (1972) Regression models and life-tables. J R Stat Soc Ser B (Method) 34:187–220

    Google Scholar 

  38. Dalziel AC, Rogers SM, Schulte PM (2009) Linking genotypes to phenotypes and fitness: how mechanistic biology can inform molecular ecology. Mol Ecol 18:4997–5017

    PubMed  CAS  Article  Google Scholar 

  39. Dapp DR, Walker TI, Huveneers C, Reina RD (2015) Respiratory mode and gear type are important determinants of elasmobranch immediate and post-release mortality. Fish Fish 17:507–524. https://doi.org/10.1111/faf.12124

    Article  Google Scholar 

  40. Dapp DR, Huveneers C, Walker TI, Drew M, Reina RD (2016) Moving from measuring to predicting bycatch mortality: predicting the capture condition of a longline-caught pelagic shark. Front Mar Sci 2:126. https://doi.org/10.3389/fmars.2015.00126

    Article  Google Scholar 

  41. Dapp DR, Huveneers C, Walker TI, Mandelman J, Kerstetter DW, Reina RD (2017) Using logbook data to determine the immediate mortality of blue sharks (Prionace glauca) and tiger sharks (Galeocerdo cuvier) caught in the commercial U.S. pelagic longline fishery. Fish Bull 115:27–41. https://doi.org/10.7755/FB.115.1.3

    Article  Google Scholar 

  42. Davis MW (2002) Key principles for understanding fish bycatch discard mortality. Can J Fish Aquat Sci 59:1834–1843. https://doi.org/10.1139/f02-139

    Article  Google Scholar 

  43. Diaz GA, Serafy JE (2005) Longline-caught blue shark (Prionace glauca): factors affecting the numbers available for live release Fish. Bull 103:720–724

    Google Scholar 

  44. Dibattista JD, Feldheim KA, Garant D, Gruber SH, Hendry AP (2009) Evolutionary potential of a large marine vertebrate: quantitative genetic parameters in a wild population. Evolution 63:1051–1067. https://doi.org/10.1111/j.1558-5646.2008.00605.x

    PubMed  Article  Google Scholar 

  45. Domeier ML, Dewar H, Nasby-Lucas N (2003) Mortality rate of striped marlin (Tetrapturus audax) caught with recreational tackle. Mar Freshw Res 54:435–445. https://doi.org/10.1071/MF01270

    Article  Google Scholar 

  46. Dulvy NK, Baum JK, Clarke S, Compagno LVJ, Cortés E, Domingo A, Fordham S, Fowler S, Francis MP, Gibson C, Martínez J, Musick JA, Soldo A, Stevens JD, Valenti S (2008) You can swim but you can’t hide: the global status and conservation of oceanic pelagic sharks. Aquat Cons Mar Freshw Ecosys 18:459–482

    Article  Google Scholar 

  47. Dulvy NK, Fowler SL, Musick JA, Cavanagh RD, Kyne PM, Harrison LR et al (2014) Extinction risk and conservation of the world’s sharks and rays. eLife 3:e00590. https://doi.org/10.7554/elife.00590

    PubMed  PubMed Central  Article  Google Scholar 

  48. Eddy C, Brill R, Bernal D (2016) Rates of at-vessel mortality and post-release survival of pelagic sharks captured with tuna purse seines around drifting fish aggregating devices (FADs) in the equatorial eastern Pacific Ocean. Fish Res 174:109–117

    Article  Google Scholar 

  49. Ellis PD (2010) The essential guide to effect sizes. Cambridge University Press, Cambridge

    Google Scholar 

  50. Ellis JR, Phillips SRM, Poisson F (2016) A review of capture and post-release mortality of elasmobranchs. J Fish Biol. https://doi.org/10.1111/jfb.13197

    PubMed  Article  Google Scholar 

  51. Elshove-Bolk J, Mencl F, van Rijswijck BTF, Simons M, van Vugt AB (2007) Validation of the Emergency Severity Index (ESI) in self-referred patients in a European emergency department. Emerg Med J 24:170–174. https://doi.org/10.1136/emj.2006.039883

    PubMed  PubMed Central  Article  Google Scholar 

  52. Enberg K, Jørgensen C, Dunlop ES, Heino M, Dieckmann U (2009) Implications of fisheries-induced evolution for stock rebuilding and recovery. Evol Appl 2:394–414. https://doi.org/10.1111/j.1752-4571.2009.00077.x

    PubMed  PubMed Central  Article  Google Scholar 

  53. Favaro B, Côté IM (2013) Do by-catch reduction devices in longline fisheries reduce capture of sharks and rays? A global meta-analysis. Fish Fish 16:300–309. https://doi.org/10.1111/faf.12055

    Article  Google Scholar 

  54. Filmalter JD, Capello M, Deneubourg JL, Cowley PD, Dagorn L (2013) Looking behind the curtain: quantifying massive shark mortality in fish aggregating devices. Front Ecol Environ 11:291–296. https://doi.org/10.1890/130045

    Article  Google Scholar 

  55. Fowler SL (2016) Draft best practice mitigation guidelines for sharks and rays taken in purse-seine and long-line fisheries. First Workshop of the Conservation Working Group Bristol, United Kingdom, 31 October. Memorandum of Understanding on the conservation of migratory sharks. CMS/Sharks/CWG1/Doc.3.2

  56. French RP, Lyle J, Tracey S, Currie S, Semmens JM (2015) High survivorship after catch-and-release fishing suggests physiological resilience in the endothermic shortfin mako shark (Isurus oxyrinchus). Con Phys 3:1–15

    Google Scholar 

  57. Frick LH, Reina RD, Walker TI (2010) Stress related physiological changes and post-release survival of Port Jackson sharks (Heterodontus portusjacksoni) and gummy sharks (Mustelus antarcticus) following gill-net and longline capture in captivity. J Exp Mar Biol Ecol 385:29–37. https://doi.org/10.1016/j.jembe.2010.01.013

    Article  Google Scholar 

  58. Fry FEJ (1971) The effect of environmental factors on the physiology of fish. In: Hoar WS, Randall DJ (eds) Fish physiology. Academic Press, New York, pp 1–98

    Google Scholar 

  59. Gallagher AJ, Kyne PM, Hammerschlag N (2012) Ecological risk assessment and its application to elasmobranch conservation and management. J Fish Biol 80:1727–1748

    PubMed  CAS  Article  Google Scholar 

  60. Gallagher AJ, Orbesen ES, Hammerschlag N, Serafy JE (2014) Vulnerability of oceanic sharks as pelagic longline bycatch. Glob Ecol Conserv 1:50–59. https://doi.org/10.1016/j.gecco.2014.06.003

    Article  Google Scholar 

  61. Gallagher AJ, Staaterman ER, Cooke SJ, Hammerschlag N (2017) Behavioral responses to fisheries capture among sharks caught using experimental fishery gear. Can J Fish Aquat Sci 74:1–7. https://doi.org/10.1139/cjfas-2016-0165

    Article  Google Scholar 

  62. Genner MJ, Sims DW, Southwood AJ, Budd GC, Masterson P, McHugh M, Rendle P, Southall EJ, Wearmouth VJ, Hawkins SJ (2009) Body size-dependent responses of a marine fish assemblage to climate change and fishing over a century-long scale. Glob Change Biol. https://doi.org/10.1111/j.1365-2486.2009.02027.x

    Article  Google Scholar 

  63. Gilman EL (2011) Bycatch governance and best practice mitigation technology in global tuna fisheries. Mar Policy 35:590–609

    Article  Google Scholar 

  64. Gilman E, Suuronen P, Hall M, Kennelly S (2013) Causes and methods to estimate cryptic sources of fishing mortalitya. J Fish Biol 83(4):766–803. https://doi.org/10.1111/jfb.12148

    PubMed  CAS  Article  Google Scholar 

  65. Gilman E, Owens M, Kraft T (2014) Ecological risk assessment of the Marshall Islands longline tuna fishery. Mar Pol 44:239–255. https://doi.org/10.1016/j.marpol.2013.08.029

    Article  Google Scholar 

  66. Gilman E, Chaloupka M, Merrifield M, Malsol ND, Cook C (2015) Standardized catch and survival rates, and effect of a ban on shark retention, Palau pelagic longline fishery. Aquat Con Mar Freshw Ecosys. https://doi.org/10.1002/aqc.2599

    Article  Google Scholar 

  67. Gilman E, Chaloupka M, Swimmer Y, Piovano S (2016) A cross-taxa assessment of pelagic longline by-catch mitigation measures: conflicts and mutual benefits to elasmobranchs. Fish Fish 17:748–784. https://doi.org/10.1111/faf.12143

    Article  Google Scholar 

  68. Gilman E, Chaloupka M, Musyl M (2017) Effects of pelagic longline hook size on species- and size-selectivity and survival. Rev Fish Biol Fisheries. https://doi.org/10.1007/s11160-017-9509-7

  69. Graves JE, Horodysky AZ (2008) Does hook choice matter? Effects of three circle hook models on postrelease survival of white marlin. N Am J Fish Manag 28:471–480. https://doi.org/10.1577/M07-107.1

    Article  Google Scholar 

  70. Graves JE, Horodysky AZ (2010) Asymmetric conservation benefits of circle hooks in multispecies billfish recreational fisheries: a synthesis of hook performance and analysis of blue marlin (Makaira nigricans) postrelease survival. Fish Bull 108:433–441

    Google Scholar 

  71. Graves JE, Luckhurst BE, Prince ED (2002) An evaluation of pop-up satellite tags for estimating postrelease survival of blue marlin (Makaira nigricans) from a recreational fishery. Fish Bull 100:134–142

    Google Scholar 

  72. Graves JE, Marcek BJ, Goldsmith WM (2016) Effects of air exposure on postrelease mortality rates of white marlin caught in the U.S. offshore recreational fishery. N Am J Fish Manag 36:1221–1228

    Article  Google Scholar 

  73. Guida L (2016) The effects of fishing on Chondrichthyans. Dissertation, Monash University

  74. Harrell FE Jr (2001) Regression modelling strategies. Springer, New York

    Google Scholar 

  75. Heberer C, Aalbers SA, Bernal D, Kohin S, DiFiore B, Sepulveda CA (2010) Insights into catch-and-release survivorship and stress-induced blood biochemistry of common thresher sharks (Alopias vulpinus) captured in the southern California recreational fishery. Fish Res 106:495–500. https://doi.org/10.1016/j.fishres.2010.09.024

    Article  Google Scholar 

  76. Heino M, Díaz Pauli B, Dieckmann U (2015) Fisheries-induced evolution. Ann Rev Ecol Evol Syst 46:461–480

    Article  Google Scholar 

  77. Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202–210. https://doi.org/10.1016/j.tree.2008.01.003

    PubMed  Article  Google Scholar 

  78. Hight BV, Holts D, Graham JB, Kennedy BP, Taylor V, Sepulveda CA, Bernal D, Ramon D, Rasmussen R, Lai NC (2007) Plasma catecholamine levels as indicators of the post-release survivorship of juvenile pelagic sharks caught on experimental drift longlines in the Southern California Bight. Mar Freshw Res 58:145. https://doi.org/10.1071/MF05260

    CAS  Article  Google Scholar 

  79. Hilbe J (2016) Practical guide to logistic regression. CRC Press, New York

    Google Scholar 

  80. Hilborn R, Walters CJ (1992) Quantitative fisheries stock assessment: choice, dynamics and uncertainty. Chapman and Hall, New York

    Google Scholar 

  81. Hobday AJ, Smith ADM, Stobutzki IC, Bulman C, Daley R, Dambacher JM et al (2011) Ecological risk assessment for the effects of fishing. Fish Res 108:372–384. https://doi.org/10.1016/j.fishres.2011.01.013

    Article  Google Scholar 

  82. Hochachka PW, Somero GN (2002) Biochemical adaptation, mechanism and process in physiological evolution. Oxford University Press, Oxford

    Google Scholar 

  83. Holden MJ (1973) Are long-term sustainable fisheries for elasmobranchs possible? Rapp P.-V. Réun Cons Int Explor Mer 64:360–367

    Google Scholar 

  84. Hollins J, Thambithurai D, Köeck B, Crespel A, Bailey DM, Cooke SJ, Lindström J, Parsons KJ, Killen SS (2018) A physiological erspective on fisheries-induced evolution. Ecol Apps. https://doi.org/10.1111/eva.12597

    Article  Google Scholar 

  85. Hosmer DW, Lemeshow S (1999) Applied survival analysis. Wiley, New York

    Google Scholar 

  86. Howey LA, Wetherbee BM, Tolentino ER, Shivji MS (2017) Biogeophysical and physiological processes drive movement patterns in a marine predator. Mov Ecol 5:16. https://doi.org/10.1186/s40462-017-0107-z

    PubMed  PubMed Central  Article  Google Scholar 

  87. Hueter RE, Manire CA, Tyminski JP, Hoenig JM, Hepworth DA (2006) Assessing mortality of released or discarded fish using a logistic model of relative survival derived from tagging data. Trans Am Fish Soc 135:500–508

    Article  Google Scholar 

  88. Hutchinson MR, Itano DG, Muir JA, Holland KN (2015) Post-release survival of juvenile silky sharks captured in a tropical tuna purse seine fishery. Mar Ecol Prog Ser 521:143–154. https://doi.org/10.3354/meps11073

    Article  Google Scholar 

  89. ICCAT (2011) Recommendation by ICCAT on the conservation of silky sharks caught in association with ICCAT fisheries recommendation 11-08. International Commission for the Conservation of Atlantic Tunas, Madrid

    Google Scholar 

  90. Jackson JBC, 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 293:629–638

    PubMed  CAS  Article  Google Scholar 

  91. James JC, Lewison RL, Dillingham PW, Curtis KA, Moore JE (2016) Drivers of retention and discards of elasmobranch non-target catch. Environ Conserv 43:3–12. https://doi.org/10.1017/S0376892915000168

    Article  Google Scholar 

  92. Jørgensen C, Ernande B, Fiksen Ø, Dieckmann U (2006) The logic of skipped spawning in fish. Can J Fish Aquat Sci 63:200–211

    Article  Google Scholar 

  93. Jørgensen C, Ernande B, Fiksen Ø (2009) Size-selective fishing gear and life history evolution in the Northeast Arctic cod. Evol Apps 2:356–370

    Article  Google Scholar 

  94. Kalbfleisch JD, Prentice RL (1980) The statistical analysis of failure time data. Wiley, New York

    Google Scholar 

  95. Kelleher K (2005) Discards in the world’s marine fisheries. An update. FAO Fisheries Technical Paper. No. 470. Rome, FAO

  96. Kerstetter DW, Graves JE (2008) Postrelease survival of sailfish caught by commercial pelagic longline gear in the southern Gulf of Mexico. N Am J Fish Mgmt 28(5):1578–1586. https://doi.org/10.1577/M07-202.1

    Article  Google Scholar 

  97. Kerstetter DW, Polovina JJ, Graves JE (2004) Evidence of shark predation and scavenging on fishes equipped with pop-up satellite archival tags. Fish Bull 102:750–756

    Google Scholar 

  98. Kleinbaum DG, Klein M (2005) Survival analysis, a self-learning text, 2nd edn. Springer, New York

    Google Scholar 

  99. Kuparinen A, Kuikka S, Merilä J (2009) Estimating fisheries-induced selection: traditional gear selectivity research meets fisheries-induced evolution. Evol App 2:234–243. https://doi.org/10.1111/j.1752-4571.2009.00070.x

    Article  Google Scholar 

  100. Law R (2000) Fishing, selection, and phenotypic evolution. ICES J Mar Sci 57:659–668. https://doi.org/10.1006/jmsc.2000.0731

    Article  Google Scholar 

  101. Lee ET, Wang JW (2003) Statistical methods for survival data analysis. Wiley, Hoboken

    Google Scholar 

  102. Li W, Dai X, Zhu J, Tian S, He S, Wu F (2017) Genetic differentiation in blue shark, Prionace glauca, from the central Pacific Ocean, as inferred by mitochondrial cytochrome b region. Mitochondrial DNA Part A 28(4):575–578. https://doi.org/10.3109/19401736.2015.1137903

    CAS  Article  Google Scholar 

  103. Lotti MJ, Wetherbee BM, Grace MA, Driggers WB (2011) Factors influencing at-vessel shark mortality during fishery-independent bottom longline surveys in the U. S. Gulf of Mexico and the western North Atlantic Ocean. A major paper submitted in partial fulfillment of the requirements for the degree Master of Environmental Science and Management, University of Rhode Island

  104. Lozano LM, García-Cueto E, Muñiz J (2008) Effect of the number of response categories on the reliability and validity of rating scales. Methodology 4:73–79. https://doi.org/10.1027/1614-2241.4.2.73

    Article  Google Scholar 

  105. Machin D, Campbell MJ, Tan SB, Tan SH (2009) Sample size tables for clinical studies, 3rd edn. Wiley-Blackwell, Chichester

    Google Scholar 

  106. Mandelman JW, Skomal GB (2009) Differential sensitivity to capture stress assessed by blood acid-base status in five carcharhinid sharks. J Comp Physiol B Biochem Syst Environ Physiol 179:267–277

    Article  Google Scholar 

  107. Marçalo A, Marques TA, Araújo J, Pousão-Ferreira P, Erzini K, Stratoudakis Y (2010) Fishing simulation experiments for predicting the effects of purse-seine capture on sardine (Sardina pilchardus). ICES J Mar Sci 67:334–344

    Article  Google Scholar 

  108. Marshall H, Field L, Afiadata A, Sepulveda C, Skomal G, Bernal D (2012) Hematological indicators of stress in longline-captured sharks. Comp Biochem Physiol Part A 162:121–129

    CAS  Article  Google Scholar 

  109. Marshall H, Skomal G, Ross PG, Bernal D (2015) At-vessel and post-release mortality of dusky (Carcharhinus obscurus) and sandbar (C. plumbeus) sharks after longline capture. Fish Res 172:373–384

    Article  Google Scholar 

  110. Meeker WQ, Escobar LA (1999) Statistical methods for reliability data. Wiley, New York

    Google Scholar 

  111. Meeremans P, Yochum N, Kochzius M, Tuyttens FAM, Uhlmann SS (2017) Inter-rater reliability of categorical versus continuous scoring of fish vitality: does it affect the utility of the reflex action mortality predictor (RAMP) approach? PLoS ONE 12:e0179092. https://doi.org/10.1371/journal.pone.0179092

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  112. Miller GA (1956) The magical number seven, plus or minus two: some limits on our capacity for processing information. Psychol Rev 63:81–97. https://doi.org/10.1037/h0043158

    PubMed  CAS  Article  Google Scholar 

  113. Molin G (1959) Test with PA fishing tackle in Swedwash inland fisheries. In: Krwastjonsson H (ed) Modern fishing gear of the world, vol 1. Fishing News Books Ltd., London, pp 156–158

    Google Scholar 

  114. Molina JM, Cooke SJ (2012) Trends in shark bycatch research: current status and research needs. Rev Fish Biol Fish 22:719–737. https://doi.org/10.1007/s11160-012-9269-3

    Article  Google Scholar 

  115. Morgan A, Burgess GH (2007) At-vessel fishing mortality for six species of sharks caught in the Northwest Atlantic and Gulf of Mexico. Gulf Carib Res 19:123–129. https://doi.org/10.18785/gcr.1902.15

    Article  Google Scholar 

  116. Morgan A, Carlson JK (2010) Capture time, size and hooking mortality of bottom longline-caught sharks. Fish Res 101:32–37

    Article  Google Scholar 

  117. Motta PJ, Wilga CD (2001) Advances in the study of feeding behaviors, mechanisms, and mechanics of sharks. Environ Biol Fish 60:131–156

    Article  Google Scholar 

  118. Moyes CD, Fragoso NM, Musyl MK, Brill RW (2006) Predicting postrelease survival in large pelagic fish. Trans Am Fish Soc 135:1389–1397. https://doi.org/10.1577/T05-224.1

    Article  Google Scholar 

  119. Muoneke MI, Childress WM (1994) Hooking mortality: a review for recreational fisheries. Rev Fish Sci 2:123–156. https://doi.org/10.1080/10641269409388555

    Article  Google Scholar 

  120. Musyl MK, Moyes CD, Brill RW, Fragoso NM (2009) Factors influencing mortality estimates in post-release survival studies. Mar Ecol Prog Ser 396:157–159. https://doi.org/10.3354/meps08432

    Article  Google Scholar 

  121. Musyl MK, Brill RW, Curran DS, McNaughton LM, Kikkawa B, Fragoso N, Moyes CD (2011a) Postrelease survival, vertical movements and thermal niche partitioning in five species pelagic sharks released from longline fishing gear in the central Pacific Ocean. Fish Bull 109:341–368

    Google Scholar 

  122. Musyl MK, Domeier ML, Nasby-Lucas N, Brill RW, McNaughton LM, Swimmer JY, Lutcavage MS, Wilson SG, Galuardi B, Liddle JB (2011b) Performance of pop-up satellite archival tags. Mar Ecol Prog Ser 433:1–28. https://doi.org/10.3354/meps09202

    Article  Google Scholar 

  123. Musyl MK, Moyes CD, Brill RW, Mourato BL, West A, McNaughton LM, Chiang W-C, Sun C-L (2015) Postrelease mortality in istiophorid billfish. Can J Fish Aquat Sci 72:1–19. https://doi.org/10.1139/cjfas-2014-0323

    Article  Google Scholar 

  124. Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1846–1850

    PubMed  CAS  Article  Google Scholar 

  125. Ogundimu EO, Altman DG, Collins GS (2016) Adequate sample size for developing prediction models is not simply related to events per variable. J Clin Epidem 76:175–182. https://doi.org/10.1016/j.jclinepi.2016.02.031

    Article  Google Scholar 

  126. Oliver S, Braccini M, Newman SJ, Harvey ES (2015) Global patterns in the bycatch of sharks and rays. Mar Pol 54:86–97. https://doi.org/10.1016/j.marpol.2014.12.017

    Article  Google Scholar 

  127. Parga ML (2012) Hooks and sea turtles: a veterinarian’s perspective. Bull Mar Sci 88:731–741

    Article  Google Scholar 

  128. Pauly D, Zeller D (2016) Catch reconstructions reveal that global marine fisheries catches are higher than reported and declining. Nat Commun 7:10244. https://doi.org/10.1038/ncomms10244

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  129. Peduzzi P, Concato J, Feinstein AR, Holford TR (1995) Importance of events per independent variable in proportional hazards regression analysis. II. Accuracy and precision of regression estimates. J Clin Epidemiol 48:1503–1510

    PubMed  CAS  Article  Google Scholar 

  130. Perdersen EJ, Thompson PL, Ball AR, Fortin M-J, Gouhier TC, Link H, Moritz C, Nenzen H, Stanley RRE, Taranu ZE, Gonzalez A, Guichard F, Pepin P (2017) Signatures of the collapse and incipient recovery of an overexploited marine ecosystem. R Soc 4:170215. https://doi.org/10.1098/rsos.170215

    Article  Google Scholar 

  131. Poisson F, Gaertner J-C, Taquet M, Durbec J-P, Bigelow D (2010) Effects of lunar cycle and fishing operations on longline-caught pelagic fish: fishing performance, capture time, and survival of fish. Fish Bull 108:268–281

    Google Scholar 

  132. Poisson F, Filmalter JD, Vernet A, Dagorn L (2014) Mortality rate of silky sharks (Carcharhinus falciformis) caught in the tropical tuna purse seine fishery in the Indian Ocean. Can J Fish Aquat Sci 71:795–798

    Article  Google Scholar 

  133. Poisson F, Crespo FA, Ellis JR, Chavance P, Pascal B, Santos MN, Séret B, Korta M, Coelho R, Ariz J, Murua H (2016) Technical mitigation measures for sharks and rays in fisheries for tuna and tuna-like species: turning possibility into reality. Aquat Liv Res 29:45. https://doi.org/10.1051/alr/2016030

    Article  Google Scholar 

  134. Powers DA, Place AR (1978) Biochemical genetics of Fundulus heteroclitus: temporal and spatial variation in gene frequencies of LDH-B, MDH-A, GPI-B, and PGM-A. Biochem Genet 16:593–607

    PubMed  CAS  Article  Google Scholar 

  135. Powers DA, Laureman T, Crawford D, Dimichele L (1991) Genetic mechanisms for adapting to a changing environment. Ann Rev Genet 25:629–659

    PubMed  CAS  Article  Google Scholar 

  136. Preston CC, Colman AM (2000) Optimal number of response categories in rating scales: reliability, validity, discriminating power, and respondent preferences. Acta Physiol (Oxf) 104:1–15

    CAS  Google Scholar 

  137. Punt AE, Smith DC, Tuck GN, Methot RD (2006) Including discard data in fisheries stock assessments: two case studies from south-eastern Australia. Fish Res 79:239–250

    Article  Google Scholar 

  138. Rice J, Harley S (2013) Updated stock assessment of silky sharks in the Western and Central Pacific Ocean. WCPFC-SC9-2013/SA-WP-03

  139. Rice J, Semba Y (2014) Age and sex specific natural mortality of the blue shark (Prionace glauca) in the North Pacific. WCPFC‐SC9‐2014/SA‐IP‐13, ISC/14/SHARKWG-1/03

  140. Rice J, Harley S, Kai M (2014) Stock assessment of blue shark in the North Pacific using stock synthesis. WCPFC‐SC10‐2014/SA‐WP‐08, ISC/14/SHARKWG‐2/02

  141. Ryan T (2013) Sample size determination and power. Wiley, Hoboken

    Google Scholar 

  142. Sauls B (2014) Relative survival of gags Mycteroperca microlepis released within a recreational hook-and-line fishery: application of the Cox Regression Model to control for heterogeneity in a large-scale mark–recapture study. Fish Res 150:18–27

    Article  Google Scholar 

  143. Schindler DE, Essington TE, Kitchell JF, Boggs C, Hilborn R (2002) Sharks and tunas: fisheries impacts on predators with contrasting life histories. Ecol Appl 12:735–748

    Article  Google Scholar 

  144. Schlenker LS, Latour RJ, Brill RW, Graves JE (2016) Physiological stress and post-release mortality of white marlin (Kajikia albida) caught in the United States recreational fishery. Conserv Physiol 4:1–15. https://doi.org/10.1093/conphys/cov066.Introduction

    Article  Google Scholar 

  145. Sepulveda CA, Heberer C, Aalbers SA, Spear N, Kinney M, Bernal D, Kohin S (2015) Post-release survivorship studies on common thresher sharks (Alopias vulpinus) captured in the southern California recreational fishery. Fish Res 161:102–108

    Article  Google Scholar 

  146. Simpfendorfer CA, Dulvy NK (2017) Bright spots of sustainable shark fishing. Curr Biol 27:R83–R102. https://doi.org/10.1016/j.cub.2016.12.017

    CAS  Article  Google Scholar 

  147. Stevens J (2000) The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES J Mar Sci 57:476–494. https://doi.org/10.1006/jmsc.2000.0724

    Article  Google Scholar 

  148. Stevens JD, Bradford RW, West GJ (2009) Satellite tagging of blue sharks (Prionace glauca) and other pelagic sharks off eastern Australia: depth behaviour, temperature experience and movements. Mar Biol. https://doi.org/10.1007/s00227-1343-6

    Article  Google Scholar 

  149. Sutter DA, Suski CD, Philipp DP, Klefoth T, Wahl DH, Kersten P, Cooke SJ, Arlinghaus R (2012) Recreational fishing selectively captures individuals with the highest fitness potential. Proc Natl Acad Sci 109:20960–20965. https://doi.org/10.1073/pnas.1212536109

    PubMed  Article  Google Scholar 

  150. Taguchi M, King JR, Wetklo M, Withler RE, Yokawa K (2017) Population genetic structure and demographic history of Pacific blue sharks (Prionace glauca) inferred from mitochondrial DNA analysis. Mar Freshw Res 66:267–275. https://doi.org/10.1071/MF14075

    CAS  Article  Google Scholar 

  151. Thomas SN, Hridayanathan C (2006) The effect of natural sunlight on the strength of polyamide 6 multifilament and monofilament fishing net materials. Fish Res 81:326–330

    Article  Google Scholar 

  152. Viana M, Graham N, Wilson JG, Jackson AL (2011) Fishery discards in the Irish Sea exhibit temporal oscillations and trends reflecting underlying processes at an annual scale. ICES J Mar Sci 68:221–227

    Article  Google Scholar 

  153. Viana M, McNally L, Graham N, Reid DG, Jackson AL (2013) Ignoring discards biases the assessment of fisheries’ ecological fingerprint. Biol Lett 9:20130812. https://doi.org/10.1098/rsbl.2013.0812

    PubMed  PubMed Central  Article  Google Scholar 

  154. Walsh WA, Bigelow KA, Sender KL (2009) Decreases in shark catches and mortality in the Hawaii-based longline fishery as documented by fishery observers. Mar Coast Fisheries 1(1):270–282

    Article  Google Scholar 

  155. WCPFC (2013) Conservation and management measure for silky sharks. CMM 2013-08. Western and Central Pacific Fisheries Commission, Kolonia, Federated States of Micronesia

  156. Wells RS, Hofmann S, Moors TL (1998) Entanglement and mortality of bottlenose dolphins, Tursiops truncates, in recreational fishing gear in Florida. Fish Bull 96:647–650

    Google Scholar 

  157. Weng KC, Castilho PC, Morrissette JM, Landeira-Fernandez AM, Holts DB, Schallert RJ, Goldman KJ, Block BA (2005) Satellite tagging and cardiac physiology reveal niche expansion in salmon sharks. Science 310:104–106

    PubMed  CAS  Article  Google Scholar 

  158. Worm B, Davis B, Kettemer L, Ward-Paige CA, Chapman D, Heithaus MR, Kessel ST, Gruber SH (2013) Global catches, exploitation rates, and rebuilding options for sharks. Mar Pol 40:194–204. https://doi.org/10.1016/j.marpol.2012.12.034

    Article  Google Scholar 

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Acknowledgements

We are grateful for at-sea data collection and tagging conducted by Ivan Sesebo and Sone Misross, MRAG Asia Pacific. We are thankful for the participation of Captains Zhang Ding Xin, Lin Quan Gui and Lu Jing De; and crew of F/V SLC901 and F/V HNY769. Logistical support was kindly provided by Terry Huang, Palau International Traders Inc.; Derrick Wang, Luen Thai Fishing Venture; Shane McGrath, MRAG Asia Pacific; Mark Zimring, Lotus Vermeer, Yvonne Ueda, Bibbie Kumangai, Steven Victor and Noah Idechong, The Nature Conservancy and Hon. F. Umiich Sengebau, Minister of Natural Resources, Environment and Tourism, Bureau of Marine Resources, Palau. We thank two anonymous reviewers for making suggestions that greatly improved the manuscript and Joe Liddle for running the SAS code.

Funding

A grant from The Nature Conservancy Indo-Pacific Tuna Program made this study possible.

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Correspondence to Michael K. Musyl.

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Project personnel were granted permission to conduct research and tagging activities under the auspices of Hon. F. Umiich Sengebau, Minister of Natural Resources, Environment and Tourism, Bureau of Marine Resources, Palau.

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Musyl, M.K., Gilman, E.L. Post-release fishing mortality of blue (Prionace glauca) and silky shark (Carcharhinus falciformes) from a Palauan-based commercial longline fishery. Rev Fish Biol Fisheries 28, 567–586 (2018). https://doi.org/10.1007/s11160-018-9517-2

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Keywords

  • Bycatch
  • Condition
  • Discard
  • Fishing mortality
  • Pelagic sharks
  • Prognostic variables
  • Risk