Marine Biology

, 165:188 | Cite as

Pronounced long-term trends in year-round diet composition of the European shag Phalacrocorax aristotelis

  • Richard J. Howells
  • Sarah J. Burthe
  • Jonathan A. Green
  • Michael P. Harris
  • Mark A. Newell
  • Adam Butler
  • Sarah Wanless
  • Francis Daunt
Original paper


Populations of marine top predators are exhibiting pronounced demographic changes due to alterations in prey availability and quality. Changes in diet composition is a key potential mechanism whereby alterations in prey availability can affect predator demography. Studies of long-term trends in diet have focused on the breeding season. However, long-term changes in non-breeding season diet is an important knowledge gap, since this is generally the most critical period of the year for the demography of marine top predators. In this study, we analysed 495,239 otoliths from 5888 regurgitated pellets collected throughout the annual cycle over three decades (1985–2014) from European shags Phalacrocorax aristotelis on the Isle of May, Scotland (56°11′N, 02°33′W). We identified dramatic reductions in the frequency of lesser sandeel Ammodytes marinus occurrence over the study, which was more pronounced during the non-breeding period (96% in 1988 to 45% in 2014), than the breeding period (91–67%). The relative numerical abundance of sandeel per pellet also reduced markedly (100–13% of all otoliths), with similar trends apparent during breeding and non-breeding periods. In contrast, the frequencies of Gadidae, Cottidae, Pleuronectidae and Gobiidae all increased, resulting in a doubling in annual prey richness from 6 prey types per year in 1988 to 12 in 2014. Our study demonstrates that the declining importance of the previously most prominent prey and marked increase in diet diversity is apparent throughout the annual cycle, suggesting that substantial temporal changes in prey populations have occurred, which may have important implications for seabird population dynamics.



We thank the many people who helped with fieldwork and lab work over the last three decades, in particular Jenny Bull, Linda Wilson and Carrie Gunn; we also thank Sam Tomlinson and Edward Carnell for help with manipulation of the data. We thank two anonymous referees for comments on an earlier version of the manuscript. We thank Scottish Natural Heritage (SNH) for access to the Isle of May National Nature Reserve. The work was conducted under research licences from Scottish Natural Heritage.


This study was funded by the Natural Environment Research Council (NERC; Adapting to the Challenges of a Changing Environment Doctoral Training Partnership, NERC National Capability, NERC/Department for Environment, Food and Rural Affairs Marine Ecosystems Research Programme Ref NE/L003082/1) and Joint Nature Conservation Committee (JNCC).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and animals

This article does not contain any studies with animals performed by any of the authors.

Supplementary material

227_2018_3433_MOESM1_ESM.pdf (681 kb)
Supplementary material 1 (PDF 681 kb)


  1. Aebischer NJ (1986) Retrospective investigation of an ecological disaster in the shag, Phalacrocorax aristotelis: a general method based on long-term marking. J Anim Ecol 55:613–629CrossRefGoogle Scholar
  2. Ainley DG, Spear LB, Allen SG, Ribic CA (1996) Temporal and spatial patterns in the diet of the common murre in California waters. Condor 98:691–705CrossRefGoogle Scholar
  3. Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manag 74:1175–1178CrossRefGoogle Scholar
  4. Arnott SA, Ruxton GD (2002) Sandeel recruitment in the North Sea: demographic, climatic and trophic effects. Mar Ecol Prog Ser 238:199–210CrossRefGoogle Scholar
  5. Barrett RT, Camphuysen K, Anker-Nilssen T, Chardine JW, Furness RW, Garthe S, Hüppop O, Leopold MF, Montevecchi WA, Veit RR (2007) Diet studies of seabirds: a review and recommendations. ICES J Mar Sci 64:1675–1691CrossRefGoogle Scholar
  6. Bartoń K (2016) MuMIn: Multi-Model Inference. R package version 1.15.6.
  7. Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  8. Bergstad OA, Jørgensen T, Dragesund O (1987) Life history and ecology of the gadoid resources of the Barents Sea. Fish Res 5:119–161CrossRefGoogle Scholar
  9. Blake BF (1984) Diet and fish stock availability as possible factors in the mass death of auks in the North Sea. J Exp Mar Biol Ecol 76:89–103CrossRefGoogle Scholar
  10. Bogdanova MI, Wanless S, Harris MP, Lindström J, Butler A, Newell MA, Sato K, Watanuki Y, Parsons M, Daunt F (2014) Among-year and within-population variation in foraging distribution of European shags Phalacrocorax aristotelis over two decades: implications for marine spatial planning. Biol Conserv 170:292–299CrossRefGoogle Scholar
  11. Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The Ecology of Individuals: incidence and Implications of Individual Specialization. Am Nat 161:1–28CrossRefGoogle Scholar
  12. Boulcott P, Wright PJ, Gibb FM, Jensen H, Gibb IM (2007) Regional variation in maturation of sandeels in the North Sea. ICES J Mar Sci 64:369–376CrossRefGoogle Scholar
  13. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. In: Burnham KP, Anderson DR (eds) Information and Likelihood Theory: A Basis for Model Selection, 2nd edn. Springer, New YorkGoogle Scholar
  14. Cormon X, Loots C, Vaz S, Vermard Y, Marchal P (2014) Spatial interactions between saithe (Pollachius virens) and hake (Merluccius merluccius) in the North Sea. ICES J Mar Sci 71:1342–1355CrossRefGoogle Scholar
  15. Cury P, Bakun A, Crawford RJM, Jarre A, Quiñones RA, Shannon L, Verheye HM (2000) Small pelagics in upwelling systems: patterns of interaction and structural changes in “wasp-waist” ecosystems. ICES J Mar Sci 57:603–618CrossRefGoogle Scholar
  16. Cury PM, Boyd IL, Bonhommeau S, Anker-Nilssen T, Crawford RJM, Furness RW, Mills JA, Murphy EJ, Österblom H, Paleczny M, Piatt JF, Roux J-P, Shannon L, Sydeman WJ (2011) Global seabird response to forage fish depletion—one-third for the birds. Science 334:1703–1706CrossRefGoogle Scholar
  17. Daunt F, Monaghan P, Wanless S, Harris MP, Griffiths R (2001) Sons and daughters: age-specific differences in parental rearing capacities. Funct Ecol 15:211–216CrossRefGoogle Scholar
  18. Daunt F, Afanasyev V, Silk JRD, Wanless S (2006) Extrinsic and intrinsic determinants of winter foraging and breeding phenology in a temperate seabird. Behav Ecol Sociobiol 59:381–388CrossRefGoogle Scholar
  19. Daunt F, Wanless S, Harris MP, Money L, Monaghan P (2007) Older and wiser: improvements in breeding success are linked to better foraging performance in European shags. Funct Ecol 21:561–567CrossRefGoogle Scholar
  20. Daunt F, Wanless S, Greenstreet SPR, Jensen H, Hamer KC, Harris MP (2008) The impact of the sandeel fishery closure in the northwestern North Sea on seabird food consumption, distribution and productivity. Can J Fish Aquat Sci 65:362–381CrossRefGoogle Scholar
  21. Daunt F, Reed TE, Newell M, Burthe S, Phillips RA, Lewis S, Wanless S (2014) Longitudinal bio-logging reveals interplay between extrinsic and intrinsic carry-over effects in a long-lived vertebrate. Ecology 95:2077–2083CrossRefGoogle Scholar
  22. Dulvy NK, Rogers SI, Jennings S, Stelzenmüller V, Dye SR, Skjoldal HR (2008) Climate change and deepening of the North Sea fish assemblage: a biotic indicator of warming seas. J Appl Ecol 45:1029–1039CrossRefGoogle Scholar
  23. Frederiksen M, Edwards M, Richardson AJ, Halliday NC, Wanless S (2006) From plankton to top predators: bottom-up control of a marine food web across four trophic levels. J Anim Ecol 75:1259–1268CrossRefGoogle Scholar
  24. Frederiksen M, Mavor RA, Wanless S (2007) Seabirds as environmental indicators: the advantages of combining data sets. Mar Ecol Prog Ser 352:205–211CrossRefGoogle Scholar
  25. Frederiksen M, Daunt F, Harris MP, Wanless S (2008) The demographic impact of extreme events: stochastic weather drives survival and population dynamics in a long-lived seabird. J Anim Ecol 77:1020–1029CrossRefGoogle Scholar
  26. Gaston A, Elliott K (2014) Seabird diet changes in northern Hudson Bay, 1981–2013, reflect the availability of schooling prey. Mar Ecol Prog Ser 513:211–223CrossRefGoogle Scholar
  27. Green DB, Klages NTW, Crawford RJM, Coetzee JC, Dyer BM, Rishworth GM, Pistorius PA (2015) Dietary change in Cape gannets reflects distributional and demographic shifts in two South African commercial fish stocks. ICES J Mar Sci 72:771–781CrossRefGoogle Scholar
  28. Grist H, Daunt F, Wanless S, Nelson EJ, Harris MP, Newell M, Burthe S, Reid JM (2014) Site fidelity and individual variation in winter location in partially migratory European shags. PLoS One 9:e98562CrossRefGoogle Scholar
  29. Halpern BS (2009) A global map of human impact on marine ecosystems. Science 319:948–952CrossRefGoogle Scholar
  30. Härkönen T (1986) Guide to the otoliths of the bony fishes of the northeast Atlantic. Danbiu ApS, HellerupGoogle Scholar
  31. Harris MP, Wanless S (1991) The importance of the lesser sandeel Ammodytes marinus in the diet of the shag Phalacrocorax aristotelis. Ornis Scand 22:375–382CrossRefGoogle Scholar
  32. Harris MP, Wanless S (1993) The diet of shags Phalacrocorax aristotelis during the chick-rearing period assessed by three methods. Bird Study 40:135–139CrossRefGoogle Scholar
  33. Harris MP, Wanless S (1996) Differential responses of guillemot Uria aalge and shag Phalacrocorax aristotelis to a late winter wreck. Bird Study 43:37–41Google Scholar
  34. Harris MP, Leopold MF, Jensen JK, Meesters EH, Wanless S (2015) The winter diet of the Atlantic Puffin Fratercula arctica around the Faroe Islands. Ibis 57:468–479CrossRefGoogle Scholar
  35. Harrison XA (2015) A comparison of observation-level random effect and Beta-binomial models for modelling overdispersion in Binomial data in ecology & evolution. PeerJ 3:e1114CrossRefGoogle Scholar
  36. Heessen HJL, Daan N, Ellis JR (2015) Fish atlas of the Celtic Sea, North Sea, and Baltic Sea, 1st edn. KNNV Publishing; Wageningen Academic Publishers, WageningenCrossRefGoogle Scholar
  37. Hislop JRG, Harris MP, Smith JGM (1991) Variation in the calorific value and total energy content of the lesser sandeel (Ammodytes marinus) and other fish preyed on by seabirds. J Zool 224:501–517CrossRefGoogle Scholar
  38. Holland GJ, Greenstreet SPR, Gibb IM, Fraser HM, Robertson MR (2005) Identifying sandeel Ammodytes marinus sediment habitat preferences in the marine environment. Mar Ecol Prog Ser 303:269–282CrossRefGoogle Scholar
  39. Howells R, Burthe S, Green J, Harris M, Newell M, Butler A, Johns D, Carnell E, Wanless S, Daunt F (2017) From days to decades: short- and long-term variation in environmental conditions affect offspring diet composition of a marine top predator. Mar Ecol Prog Ser 583:227–242CrossRefGoogle Scholar
  40. Høyer JL, Karagali I (2016) Sea Surface Temperature climate data record for the North Sea and Baltic Sea. J Clim 29:2529–2541CrossRefGoogle Scholar
  41. Johnstone IG, Harris MP, Wanless S, Graves JA (1990) The usefulness of pellets for assessing the diet of adult shags Phalacrocorax aristotelis. Bird Study 37:37–41CrossRefGoogle Scholar
  42. Kowalczyk ND, Chiaradia A, Preston TJ, Reina RD (2014) Linking dietary shifts and reproductive failure in seabirds: a stable isotope approach. Funct Ecol 28:755–765CrossRefGoogle Scholar
  43. Kowalczyk ND, Chiaradia A, Preston TJ, Reina RD (2015) Fine-scale dietary changes between the breeding and non-breeding diet of a resident seabird. R Soc Open Sci 2:1–17CrossRefGoogle Scholar
  44. Lewis S, Phillips RA, Burthe SJ, Wanless S, Daunt F (2015) Contrasting responses of male and female foraging effort to year-round wind conditions. J Anim Ecol 84:1490–1496CrossRefGoogle Scholar
  45. Lilliendahl K, Solmundsson J (2006) Feeding ecology of sympatric European shags Phalacrocorax aristotelis and great cormorants P. carbo in Iceland. Mar Biol 149:979–990CrossRefGoogle Scholar
  46. Litzow MA, Piatt JF, Abookire AA, Robards MD (2004) Energy density and variability in abundance of pigeon guillemot prey: support for the quality-variability trade-off hypothesis. J Anim Ecol 73:1149–1156CrossRefGoogle Scholar
  47. Lorentsen S-H, Anker-Nilssen T, Erikstad KE (2018) Seabirds as guides for fisheries management: european shag Phalacrocorax aristotelis diet as indicator of saithe Pollachius virens recruitment. Mar Ecol Prog Ser 586:193–201CrossRefGoogle Scholar
  48. Markones N, Dierschke V, Garthe S (2010) Seasonal differences in at-sea activity of seabirds underline high energetic demands during the breeding period. J Ornithol 151:329–336CrossRefGoogle Scholar
  49. Michelot C, Pinaud D, Fortin M, Maes P, Callard B, Leicher M, Barbraud C (2017) Seasonal variation in coastal marine habitat use by the European shag: insights from fine scale habitat selection modeling and diet. Deep Sea Res Part II Top Stud Oceanogr 141:224–236CrossRefGoogle Scholar
  50. Miller AK, Sydeman WJ (2004) Rockfish response to low-frequency ocean climate change as revealed by the diet of a marine bird over multiple time scales. Mar Ecol Prog Ser 281:207–216CrossRefGoogle Scholar
  51. Newell M, Wanless S, Harris M, Daunt F (2015) Effects of an extreme weather event on seabird breeding success at a North Sea colony. Mar Ecol Prog Ser 532:257–268CrossRefGoogle Scholar
  52. Owen E, Daunt F, Moffat C, Elston DA, Wanless S, Thompson P (2013) Analysis of fatty acids and fatty alcohols reveals seasonal and sex-specific changes in the diets of seabirds. Mar Biol 160:987–999CrossRefGoogle Scholar
  53. Paleczny M, Hammill E, Karpouzi V, Pauly D (2015) Population trend of the world’s monitored seabirds, 1950–2010. PLoS One 10:e0129342CrossRefGoogle Scholar
  54. Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915CrossRefGoogle Scholar
  55. Poloczanska ES, Brown CJ, Sydeman WJ, Kiessling W, Schoeman DS, Moore PJ, Brander K, Bruno JF, Buckley LB, Burrows MT, Duarte CM, Halpern BS, Holding J, Kappel CV, O’Connor MI, Pandolfi JM, Parmesan C, Schwing F, Thompson SA, Richardson AJ (2013) Global imprint of climate change on marine life. Nat Clim Change 3:919–925CrossRefGoogle Scholar
  56. Potts G, Coulson J, Deans I (1980) Population dynamics and breeding success of the shag, Phalacrocorax aristotelis, on the Farne Islands, Northumberland. J Anim Ecol 49:465–484CrossRefGoogle Scholar
  57. R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Google Scholar
  58. Reid K, Croxall JP (2001) Environmental response of upper trophic-level predators reveals a system change in an Antarctic marine ecosystem. Proc Biol Sci 268:377–384CrossRefGoogle Scholar
  59. Ronconi RA, Koopman HN, McKinstry CAE, Wong SNP, Westgate AJ (2010) Inter-annual variability in diet of non-breeding pelagic seabirds Puffinus spp. at migratory staging areas: evidence from stable isotopes and fatty acids. Mar Ecol Prog Ser 419:267–282CrossRefGoogle Scholar
  60. Russell AF, Wanless S, Harris MP (1995) Factors affecting the production of pellets by Shags Phalacrocorax aristotelis. Seabird 17:44–49Google Scholar
  61. Sorensen MC, Hipfner JM, Kyser TK, Norris DR (2009) Carry-over effects in a Pacific seabird: stable isotope evidence that pre-breeding diet quality influences reproductive success. J Anim Ecol 78:460–467CrossRefGoogle Scholar
  62. Spitz J, Mourocq E, Schoen V, Ridoux V (2010) Proximate composition and energy content of forage species from the Bay of Biscay: high-or low-quality food? ICES J Mar Sci J du Cons 67:909–915CrossRefGoogle Scholar
  63. Swann RL, Harris MP, Aiton DG (2008) The diet of European shag Phalacrocorax aristotelis, black-legged kittiwake Rissa tridactyla and common guillemot Uria aalge on Canna during the chick-rearing period 1981–2007. Seabird 21:44–54Google Scholar
  64. Sydeman WJ, Poloczanska ES, Reed TE, Thompson SA (2015) Climate change and marine vertebrates. Science 350:772–777CrossRefGoogle Scholar
  65. ter Hofstede R, Hiddink J, Rijnsdorp A (2010) Regional warming changes fish species richness in the eastern North Atlantic Ocean. Mar Ecol Prog Ser 414:1–9CrossRefGoogle Scholar
  66. Van Deurs M, VanHal R, Tomczak MT, Jónasdóttir SH (2009) Recruitment of lesser sandeel Ammodytes marinus in relation to density dependence and zooplankton composition. Mar Ecol Prog Ser 381:249–258CrossRefGoogle Scholar
  67. Velando A, Freire J (1999) Intercolony and seasonal differences in the breeding diet of European shags on the Galician coast (NW Spain). Mar Ecol Prog Ser 188:225–236CrossRefGoogle Scholar
  68. Wanless S, Harris MP (1997) Phalacrocorax aristotelis shag. BWP update. Oxford University Press, Oxford, pp 3–13Google Scholar
  69. Wanless S, Harris MP, Redman P, Speakman JR (2005) Low energy values of fish as a probable cause of a major seabird breeding failure in the North Sea. Mar Ecol Prog Ser 294:1–8CrossRefGoogle Scholar
  70. Wanless S, Harris MP, Newell MA, Speakman JR, Daunt F (2018) A community wide decline in the importance of lesser sandeels Ammodytes marinus in seabird chick diet at a North Sea colony. Mar Ecol Prog Ser 600:193–206CrossRefGoogle Scholar
  71. Watanuki Y, Daunt F, Takahashi A, Newell M, Wanless S, Sato K, Miyazaki N (2008) Microhabitat use and prey capture of a bottom-feeding top predator, the European shag, shown by camera loggers. Mar Ecol Prog Ser 356:283–293CrossRefGoogle Scholar
  72. Watt J, Pierce GJ, Boyle PR (1997) Guide to the identification of North Sea fish using Prernaxillae and Vertebrae. Denmark, CopenhagenGoogle Scholar
  73. Weimerskirch H (2002) Seabird demography and its relationship with the marine environment. In: Schreiber EA, Burger J (eds) The biology of marine birds. CRC Press, Boca Raton, pp 115–137Google Scholar
  74. Winslade P (1974) Behavioural studies on the lesser sandeel Ammodytes marinus (Raitt) III. The effect of temperature on activity and the environmental control of the annual cycle of activity. J Fish Biol 6:587–599CrossRefGoogle Scholar
  75. Wright P, Bailey M (1993) Biology of sandeels in the vicinity of seabird colonies at Shetland. Scottish Office Agriculture and Fisheries Department, Marine Laboratory, AberdeenGoogle Scholar
  76. Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar
  77. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Richard J. Howells
    • 1
  • Sarah J. Burthe
    • 1
  • Jonathan A. Green
    • 2
  • Michael P. Harris
    • 1
  • Mark A. Newell
    • 1
  • Adam Butler
    • 3
  • Sarah Wanless
    • 1
  • Francis Daunt
    • 1
  1. 1.Centre for Ecology & HydrologyPenicuikUK
  2. 2.School of Environmental SciencesUniversity of LiverpoolLiverpoolUK
  3. 3.Biomathematics and Statistics ScotlandEdinburghUK

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