Starving seabirds: unprofitable foraging and its fitness consequences in Cape gannets competing with fisheries in the Benguela upwelling ecosystem

An Erratum to this article was published on 29 November 2016

Abstract

Fisheries are often accused of starving vulnerable seabirds, yet evidence for this claim is scarce. Foraging energetics may provide efficient, short-term indicators of the fitness status of seabirds competing with fisheries. We used this approach in Cape gannets (Morus capensis) from Malgas Island, South Africa, which feed primarily on small pelagic fish in the southern Benguela upwelling region, thereby competing with purse-seine fisheries. During their 2011–2014 breeding seasons, we determined body condition of breeding adult Cape gannets and measured their chick growth rates. In addition to these conventional fitness indices, we assessed the daily energy expenditure of breeding adults using a high-resolution time-energy budget derived from GPS-tracking and accelerometry data. For these same individuals, we also determined prey intake rates using stomach temperature recordings. We found that adult body condition and chick growth rates declined significantly during the study period. Crucially, most birds (73 %) studied with electronic recorders spent more energy than they gained through foraging, and 80–95 % of their feeding dives were unsuccessful. Our results therefore point to unprofitable foraging in Cape gannets, with a longer-term fitness cost in terms of adult body condition and reproductive performance that corresponds to a local population decline. Based on this evidence, we advocate a revision of regional fishing quotas for small pelagic fish and discuss the possibility of an experimental cessation of purse-seine fishing activities off the west coast of South Africa. These measures are needed for the ecological and socio-economical persistence of the broader southern Benguela upwelling ecosystem.

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References

  1. Ancel A, Horning M, Kooyman GL (1997) Prey ingestion revealed by oesophagus and stomach temperature recordings in cormorants. J Exp Biol 200:149–154

    CAS  Google Scholar 

  2. Anderson HB, Evans PG, Potts JM et al (2014) The diet of Common Guillemot Uria aalge chicks provides evidence of changing prey communities in the North Sea. Ibis 156:23–34

    Article  Google Scholar 

  3. Baillie J, Hilton-Taylor C, Stuart SN (2004) 2004 IUCN red list of threatened species: a global species assessment. IUCN, Gland

    Google Scholar 

  4. Batchelor A, Ross G (1984) The diet and implications of dietary change of Cape gannets on Bird Island, Algoa Bay. Ostrich 55:45–63

    Article  Google Scholar 

  5. Beaugrand G, McQuatters-Gollop A, Edwards M, Goberville E (2013) Long-term responses of North Atlantic calcifying plankton to climate change. Nat Clim Change 3:263–267

    CAS  Article  Google Scholar 

  6. Belhabib D, Sumaila UR, Pauly D (2015) Feeding the poor: contribution of West African fisheries to employment and food security. Ocean Coast Manag 111:72–81

    Article  Google Scholar 

  7. Bijleveld AI, Mullers RH (2009) Reproductive effort in biparental care: an experimental study in long-lived Cape gannets. Behav Ecol 20:736–744

    Article  Google Scholar 

  8. Blamey LK, Shannon LJ, Bolton JJ et al (2015) Ecosystem change in the southern Benguela and the underlying processes. J Mar Syst 144:9–29

    Article  Google Scholar 

  9. Blight LK, Ainley DG, Ackley SF et al (2010) Fishing for data in the Ross Sea. Science 330:1316

    CAS  Article  Google Scholar 

  10. Bost C-A, Handrich Y, Butler PJ et al (2007) Changes in dive profiles as an indicator of feeding success in king and Adélie penguins. Deep Sea Res Part II Top Stud Oceanogr 54:248–255

    Article  Google Scholar 

  11. Capuska GEM, Vaughn RL, Würsig B et al (2011) Dive strategies and foraging effort in the Australasian gannet Morus serrator revealed by underwater videography. Mar Ecol Prog Ser 442:255–261

    Article  Google Scholar 

  12. Carson R (1951) The sea around us. Oxford University Press, New York

    Google Scholar 

  13. Chaurand T, Weimerskirch H (1994) The regular alternation of short and long foraging trips in the blue petrel Halobaena caerulea: a previously undescribed strategy of food provisioning in a pelagic seabird. J Anim Ecol 63:275–282

    Article  Google Scholar 

  14. Coetzee J (2000) Use of a shoal analysis and patch estimation system (SHAPES) to characterise sardine schools. Aquat Living Resour 13:1–10

    Article  Google Scholar 

  15. Coetzee JC, Van der Lingen CD, Hutchings L, Fairweather TP (2008) Has the fishery contributed to a major shift in the distribution of South African sardine? ICES J Mar Sci J Cons 65:1676–1688

    Article  Google Scholar 

  16. Cohen LA, Pichegru L, Grémillet D et al (2014) Changes in prey availability impact the foraging behaviour and fitness of Cape gannets over a decade. Mar Ecol Prog Ser 505:281–293

    Article  Google Scholar 

  17. Constable AJ, de la Mare WK, Agnew DJ et al (2000) Managing fisheries to conserve the Antarctic marine ecosystem: practical implementation of the convention on the conservation of antarctic marine living resources (CCAMLR). ICES J Mar Sci J Cons 57:778–791

    Article  Google Scholar 

  18. Crawford RJ (2013) Long-term change in the population sizes and conservation status of South Africa’s seabirds. Ostrich 84:v–ix

    Article  Google Scholar 

  19. Crawford RJM, Altwegg R, Barham BJ et al (2011) Collapse of South Africa’s penguins in the early 21st century. Afr J Mar Sci 33:139–156

    Article  Google Scholar 

  20. Crawford RJ, Makhado AB, Waller LJ, Whittington PA (2014) Winners and losers–responses to recent environmental change by South African seabirds that compete with purse-seine fisheries for food. Ostrich 85:111–117

    Article  Google Scholar 

  21. Croll DA, Gaston AJ, Noble DG (1991) Adaptive loss of mass in thick-billed murres. Condor 93:496–502

    Article  Google Scholar 

  22. Cury P, Bakun A, Crawford RJ et al (2000) Small pelagics in upwelling systems: patterns of interaction and structural changes in “wasp-waist” ecosystems. ICES J Mar Sci J Cons 57:603–618

    Article  Google Scholar 

  23. Cury PM, Boyd IL, Bonhommeau S et al (2011) Global seabird response to forage fish depletion—one-third for the birds. Science 334:1703–1706

    CAS  Article  Google Scholar 

  24. de Moor CL, Butterworth DS (2015) Assessing the South African sardine resource: two stocks rather than one? Afr J Mar Sci 37:41–51

    Article  Google Scholar 

  25. Drent R, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252

    Google Scholar 

  26. Enstipp MR, Grémillet D, Jones DR (2006) The effects of depth, temperature and food ingestion on the foraging energetics of a diving endotherm, the double-crested cormorant (Phalacrocorax auritus). J Exp Biol 209:845–859

    Article  Google Scholar 

  27. Fairweather TP, Van Der Lingen CD, Booth AJ et al (2006) Indicators of sustainable fishing for South African sardine Sardinops sagax and anchovy Engraulis encrasicolus. Afr J Mar Sci 28:661–680

    Article  Google Scholar 

  28. Fort J, Porter WP, Grémillet D (2011) Energetic modelling: a comparison of the different approaches used in seabirds. Comp Biochem Physiol A: Mol Integr Physiol 158:358–365

    Article  Google Scholar 

  29. Frederiksen M, Wanless S, Harris MP et al (2004) The role of industrial fisheries and oceanographic change in the decline of North Sea black-legged kittiwakes. J Appl Ecol 41:1129–1139

    Article  Google Scholar 

  30. Fréon P, Bouchon M, Mullon C et al (2008) Interdecadal variability of anchoveta abundance and overcapacity of the fishery in Peru. Prog Oceanogr 79:401–412

    Article  Google Scholar 

  31. Green JA, Boyd IL, Woakes AJ et al (2009a) Evaluating the prudence of parents: daily energy expenditure throughout the annual cycle of a free-ranging bird, the macaroni penguin Eudyptes chrysolophus. J Avian Biol 40:529–538

    Article  Google Scholar 

  32. Green JA, White CR, Bunce A et al (2009b) Energetic consequences of plunge diving in gannets. Endanger Species Res 10:269–279

    Article  Google Scholar 

  33. Green JA, Aitken-Simpson EJ, White CR et al (2013) An increase in minimum metabolic rate and not activity explains field metabolic rate changes in a breeding seabird. J Exp Biol 216:1726–1735

    CAS  Article  Google Scholar 

  34. Grémillet D, Charmantier A (2010) Shifts in phenotypic plasticity constrain the value of seabirds as ecological indicators of marine ecosystems. Ecol Appl 20:1498–1503. doi:10.1890/09-1586.1

    Article  Google Scholar 

  35. Grémillet D, Storch S, Peters G (2000) Determining food requirements in marine top predators: a comparison of three independent techniques in Great Cormorants, Phalacrocorax carbo carbo. Can J Zool 78:1567–1579

    Article  Google Scholar 

  36. Grémillet D, Wanless S, Carss DN et al (2001) Foraging energetics of arctic cormorants and the evolution of diving birds. Ecol Lett 4:180–184

    Article  Google Scholar 

  37. Grémillet D, Wright G, Lauder A et al (2003) Modelling the daily food requirements of wintering great cormorants: a bioenergetics tool for wildlife management. J Appl Ecol 40:266–277

    Article  Google Scholar 

  38. Grémillet D, Lewis S, Drapeau L et al (2008a) Spatial match–mismatch in the Benguela upwelling zone: should we expect chlorophyll and sea-surface temperature to predict marine predator distributions? J Appl Ecol 45:610–621

    Article  Google Scholar 

  39. Grémillet D, Pichegru L, Kuntz G et al (2008b) A junk-food hypothesis for gannets feeding on fishery waste. Proc R Soc B Biol Sci 275:1149–1156

    Article  Google Scholar 

  40. Grémillet D, Prudor A, Le Maho Y, Weimerskirch H (2012) Vultures of the seas: hyperacidic stomachs in wandering albatrosses as an adaptation to dispersed food resources, including fishery wastes. PLoS ONE 7:e37834

    Article  Google Scholar 

  41. Grémillet D, Fort J, Amélineau F et al (2015) Arctic warming: nonlinear impacts of sea-ice and glacier melt on seabird foraging. Glob Change Biol 21:1116–1123. doi:10.1111/gcb.12811

    Article  Google Scholar 

  42. Halpern BS, Walbridge S, Selkoe KA et al (2008) A global map of human impact on marine ecosystems. Science 319:948–952

    CAS  Article  Google Scholar 

  43. Hamann MH, Grémillet D, Ryan PG et al (2012) A hard-knock life: the foraging ecology of Cape cormorants amidst shifting prey resources and industrial fishing pressure. Afr J Mar Sci 34:233–240

    Article  Google Scholar 

  44. Heymans JJ, Shannon LJ, Jarre A (2004) Changes in the northern Benguela ecosystem over three decades: 1970s, 1980s, and 1990s. Ecol Model 172:175–195

    Article  Google Scholar 

  45. Hockey PAR, Dean WRJ, Ryan PG (2005) Birds of Southern Africa. In: Hockey PAR, Dean WRJ, Ryan PG (eds) Birds of Southern Africa, 7th edn. Trustees of the John Voelcker Bird Book Fund, Cape Town

  46. Jarre A, Ragaller SM, Hutchings L (2013) Long-term, ecosystem-scale changes in the southern Benguela marine pelagic social-ecological system–interaction of natural and human drivers. Ecol Soc 18:55

    Article  Google Scholar 

  47. Jarre A, Hutchings L, Kirkman SP et al (2015) Synthesis: climate effects on biodiversity, abundance and distribution of marine organisms in the Benguela. Fish Oceanogr 24:122–149

    Article  Google Scholar 

  48. Lewis S, Benvenuti S, Dall-Antonia L et al (2002) Sex-specific foraging behaviour in a monomorphic seabird. Proc R Soc Lond B Biol Sci 269:1687–1693. doi:10.1098/rspb.2002.2083

    CAS  Article  Google Scholar 

  49. Lewis S, Gremillet D, Daunt F et al (2006) Using behavioural and state variables to identify proximate causes of population change in a seabird. Oecologia 147:606–614

    Article  Google Scholar 

  50. Lewis SEF, Turpie JK, Ryan PG (2012) Are African penguins worth saving? The ecotourism value of the Boulders Beach colony. Afr J Mar Sci 34:497–504

    Article  Google Scholar 

  51. Lewison R, Oro D, Godley B et al (2012) Research priorities for seabirds: improving seabird conservation and management in the 21st century. Endanger Species Res 17:93–121

    Article  Google Scholar 

  52. Lovvorn JR, Gillingham MP (1996) Food dispersion and foraging energetics: a mechanistic synthesis for field studies of avian benthivores. Ecology 77:435–451

  53. Manly BFJ (1997) Randomization, bootstrap and Monte Carlo methods in biology. Chapman Hall, London

    Google Scholar 

  54. Moloney C, Fennessy S, Gibbons M et al (2013) Reviewing evidence of marine ecosystem change off South Africa. Afr J Mar Sci 35:427–448

    Article  Google Scholar 

  55. Moseley C, Grémillet D, Connan M et al (2012) Foraging ecology and ecophysiology of Cape gannets from colonies in contrasting feeding environments. J Exp Mar Biol Ecol 422:29–38

    Article  Google Scholar 

  56. Mullers RHE, Tinbergen JM (2009) Individual variation in parental provisioning behaviour predicts survival of Cape gannet chicks under poor conditions. Ardea 97:89–98

    Article  Google Scholar 

  57. Navarro RA, Mullers RH, Meijer HA, Underhill LG (2015) Energy expenditure of free-ranging chicks of the cape gannet Morus capensis. Physiol Biochem Zool 88:406–415

    Article  Google Scholar 

  58. Okes NC, Hockey PA, Pichegru L et al (2009) Competition for shifting resources in the southern Benguela upwelling: seabirds versus purse-seine fisheries. Biol Conserv 142:2361–2368

    Article  Google Scholar 

  59. Patrick SC, Bearhop S, Grémillet D et al (2014) Individual differences in searching behaviour and spatial foraging consistency in a central place marine predator. Oikos 123:33–40

    Article  Google Scholar 

  60. Pauly D, Christensen V, Dalsgaard J et al (1998) Fishing down marine food webs. Science 279:860–863

    CAS  Article  Google Scholar 

  61. Pauly D, Watson R, Alder J (2005) Global trends in world fisheries: impacts on marine ecosystems and food security. Philos Trans R Soc B Biol Sci 360:5–12

    Article  Google Scholar 

  62. Pettex E, Lorentsen S-H, Grémillet D et al (2012) Multi-scale foraging variability in Northern gannet (Morus bassanus) fuels potential foraging plasticity. Mar Biol 159:2743–2756

    Google Scholar 

  63. Pichegru L, Ryan PG, van der Lingen CD et al (2007) Foraging behaviour and energetics of Cape gannets Morus capensis feeding on live prey and fishery discards in the Benguela upwelling system. Mar Ecol Prog Ser 350:127

    Article  Google Scholar 

  64. Pichegru L, Ryan PG, Le Bohec C et al (2009) Overlap between vulnerable top predators and fisheries in the Benguela upwelling system: implications for marine protected areas. Mar Ecol Prog Ser 391:199–208

    Article  Google Scholar 

  65. Pichegru L, Grémillet D, Crawford RJM, Ryan PG (2010a) Marine no-take zone rapidly benefits endangered penguin. Biol Lett 6:498–501

    CAS  Article  Google Scholar 

  66. Pichegru L, Ryan PG, Crawford RJ et al (2010b) Behavioural inertia places a top marine predator at risk from environmental change in the Benguela upwelling system. Mar Biol 157:537–544

    Article  Google Scholar 

  67. Pichegru L, Ryan PG, van Eeden R et al (2012) Industrial fishing, no-take zones and endangered penguins. Biol Conserv 156:117–125

    Article  Google Scholar 

  68. Rishworth GM, Tremblay Y, Green DB et al (2014) Drivers of time-activity budget variability during breeding in a pelagic seabird. PLoS ONE 9:e116544

    Article  Google Scholar 

  69. Ropert-Coudert Y, Grémillet D, Kato A et al (2004) A fine-scale time budget of Cape gannets provides insights into the foraging strategies of coastal seabirds. Anim Behav 67:985–992

    Article  Google Scholar 

  70. Sabarros PS, Durant JM, Grémillet D et al (2012) Differential responses of three sympatric seabirds to spatio-temporal variability in shared resources. Mar Ecol Prog Ser 468:291

    Article  Google Scholar 

  71. Sauer WHH, Hecht T, Britz PJ, Mather D (2003) An economic and sectoral study of the South African fishing industry, vol 2: Fishery profiles. Report prepared for MCM by Rhodes University, Grahamstown

  72. Shannon LJ, Moloney CL (2004) An ecosystem framework for fisheries management in the southern Benguela upwelling system. Afr J Mar Sci 26:63–77

    Article  Google Scholar 

  73. Tew Kai E, Benhamou S, Lingen CD et al (2013) Are Cape gannets dependent upon fishery waste? A multi-scale analysis using seabird GPS-tracking, hydro-acoustic surveys of pelagic fish and vessel monitoring systems. J Appl Ecol 50:659–670

    Article  Google Scholar 

  74. Travers-Trolet M, Shin Y-J, Shannon LJ et al (2014) Combined fishing and climate forcing in the southern Benguela upwelling ecosystem: an end-to-end modelling approach reveals dampened effects. PLoS ONE 9:e94286

    Article  Google Scholar 

  75. Turpie JK (2003) The existence value of biodiversity in South Africa: how interest, experience, knowledge, income and perceived level of threat influence local willingness to pay. Ecol Econ 46:199–216

    Article  Google Scholar 

  76. Wanless S, Frederiksen M, Daunt F et al (2007) Black-legged kittiwakes as indicators of environmental change in the North Sea: evidence from long-term studies. Prog Oceanogr 72:30–38

    Article  Google Scholar 

  77. Watanabe YY, Takahashi A (2013) Linking animal-borne video to accelerometers reveals prey capture variability. Proc Natl Acad Sci 110:2199–2204

    CAS  Article  Google Scholar 

  78. Wilson RP, Pütz K, Grémillet D et al (1995) Reliability of stomach temperature changes in determining feeding characteristics of seabirds. J Exp Biol 198:1115–1135

    Google Scholar 

  79. Wilson R, Peters G, Regel J et al (1998) Short retention times of stomach temperature loggers in free-living seabirds: is there hope in the spring? Mar Biol 130:559–566

    Article  Google Scholar 

  80. Wilson R, Steinfurth A, Ropert-Coudert Y et al (2002) Lip-reading in remote subjects: an attempt to quantify and separate ingestion, breathing and vocalisation in free-living animals using penguins as a model. Mar Biol 140:17–27

    Article  Google Scholar 

  81. Wilson RP, White CR, Quintana F et al (2006) Moving towards acceleration for estimates of activity-specific metabolic rate in free-living animals: the case of the cormorant. J Anim Ecol 75:1081–1090

    Article  Google Scholar 

  82. Worm B, Hilborn R, Baum JK et al (2009) Rebuilding global fisheries. Science 325:578–585

    CAS  Article  Google Scholar 

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Acknowledgments

This study was funded by the FitzPatrick Institute, DST-NRF Centre of Excellence at the University of Cape Town (South Africa) and the Centre National de la Recherche Scientifique (CEFE-CNRS, UMR5175 Montpellier, France). We warmly thank Pierre Nel and SANParks for accommodation and logistical support. We are also particularly grateful to Lea Cohen, Itai Mukutyu, Emilie Tew Kai, Timothée Cook, Bruce Dyer, Rabi’a Ryklief, Leshia Upfold and Plaxedes Vimbai-Rukuni for their help in the field, to Jonathan Green for essential input on seabird energetics and to Carl van der Lingen for comments upon an initial draft version.

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Correspondence to David Grémillet.

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All experiments were performed under permits from South African National Parks with respect to animal ethics (No. CRC/2015/001—2002), and all protocols were validated by the French Direction des Services Vétérinaires (Permit No. 34-369).

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An erratum to this article is available at http://dx.doi.org/10.1007/s00227-016-3003-y.

Responsible Editor: V.H. Paiva.

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Grémillet, D., Péron, C., Kato, A. et al. Starving seabirds: unprofitable foraging and its fitness consequences in Cape gannets competing with fisheries in the Benguela upwelling ecosystem. Mar Biol 163, 35 (2016). https://doi.org/10.1007/s00227-015-2798-2

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Keywords

  • West Coast
  • Daily Food Intake
  • Negative Energy Balance
  • Positive Energy Balance
  • Total Allowable Catch