Skip to main content
Log in

Sexually distinct foraging strategies in an omnivorous seabird

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Intra-specific differences in foraging behaviour can have fitness consequences, especially during breeding. We combined GPS tracking data from 34 lesser black-backed gulls (Larus fuscus) encompassing 2029 foraging trips with dietary information and morphometric measurements to test the effect of breeding status and sex as well as body size on foraging behaviour. We found sexually distinct foraging strategies in this generalist seabird, which were maintained throughout the breeding season. The larger males travelled further from the colony than females, spent more time offshore, and remained longer at the nest during nest bouts. Males fed mostly on fisheries discards at offshore trawlers with few alternative resources nearby. Females foraged predominantly on land or nearshore and in the Wadden Sea, where they had multiple foraging options. Individuals differed in foraging behaviour along a continuum of predominantly terrestrial to predominantly marine foragers. Foraging range, trip duration, and the proportion of time at sea increased with wing length. Our findings did not support the usual inference that sexual segregation is mediated primarily by differences in competitive strength as both sexes foraged substantially in competitive settings around fishing vessels, but in different habitats. Females accessed a wider variety of resources and a broad prey spectrum, by exploring a whole suite of foraging opportunities and habitats nearer the colony. Different behavioural strategies (a combination of individual specialisation and sexual segregation) during breeding could reduce intra-specific resource competition, competition between the sexes (and hence within a pair), or alternatively, reduce the risk of unbalanced food provisioning.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alerstam T, Rosén M, Bäckman J, Ericson PGP, Hellgren O (2007) Flight speeds among bird species: allometric and phylogenetic effects. PLoS Biol 5:1656–1662

    Article  CAS  Google Scholar 

  • Barrett RT, Camphuysen CJ, 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 64:1675–1691

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1-7, http://CRAN.R-project.org/package=lme4

  • Bearhop S, Phillips RA, McGill R, Cherel Y, Dawson DA, Croxall JP (2006) Stable isotopes indicate sex-specific and long-term individual foraging specialisation in diving seabirds. Mar Ecol Progr Ser 311:157–164

    Article  Google Scholar 

  • Bennett PM, Owens PF (2002) Evolutionary ecology of birds. Life histories, mating systems and extinction. Oxford Univ Press, Oxford

    Google Scholar 

  • Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialisation. Am Nat 161:1–28

    Article  Google Scholar 

  • Bouten W, Baaij E, Shamoun-Baranes J, Camphuysen CJ (2013) A flexible GPS tracking system for studying bird behaviour at multiple scales. J Ornithol 154:571–580

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information–theoretic approach. Springer, New York

    Google Scholar 

  • Camphuysen CJ (1994) Flatfish selection by Herring Gulls Larus argentatus and Lesser Black-backed Gulls Larus fuscus scavenging at commercial beamtrawlers in the southern North Sea. Neth J Sea Res 32:91–98

    Article  Google Scholar 

  • Camphuysen CJ (1995) Herring Gull Larus argentatus and Lesser Black-backed Gulls Larus fuscus feeding at fishing vessels in the breeding season: competitive scavenging versus efficient flying. Ardea 83:365–380

    Google Scholar 

  • Camphuysen CJ (2013) A historical ecology of two closely related gull species (Laridae): multiple adaptations to a man-made environment. Ph.D. Thesis, Univ Groningen. http://dissertations.ub.rug.nl/faculties/science/2013/c.j.camphuijsen/

  • Camphuysen CJ, Calvo B, Durinck J, Ensor K, Follestad A, Furness RW, Garthe S, Leaper G, Skov H, Tasker ML, Winter CJN (1995) Consumption of discards by seabirds in the North Sea. Final report to the European Commission, study contr. BIOECO/93/10, NIOZ Report 1995-5, Netherlands Institute for Sea Research, Den Burg, Texel

  • Camphuysen CJ, Dijk J van, Witte H, Spaans N (2008) De voedselkeuze van Kleine Mantelmeeuwen en Zilvermeeuwen en andere indicaties die aanwijzingen geven over het ruimtegebruik van deze vogelsoorten in de Noord-Hollandse kustwateren. NIOZ Report 2008–2012, Royal Netherlands Institute for Sea Research, Den Burg, Texel

  • Camphuysen CJ, de Boer P, Bouten W, Gronert A, Shamoun-Baranes J (2010) Mammalian prey in Laridae: increased predation pressure on mammal populations expected. Lutra 53:5–20

    Google Scholar 

  • Chapman JW, Klaassen RHG, Drake VA, Fossette S, Hays GC, Metcalfe JD, Reynolds AM, Reynolds DR, Alerstam T (2011) Animal orientation strategies for movement in flows. Curr Biol 21:R861–R870

    Article  CAS  Google Scholar 

  • Clarke J, Manly B, Kerry K, Gardner H, Franchi E, Corsolini S, Focardi S (1998) Sex differences in Adélie penguin foraging strategies. Polar Biol 20:248–258

    Article  Google Scholar 

  • Conradt L, Clutton-Brock TH, Thomson D (1999) Habitat segregation in ungulates: Are males forced into suboptimal foraging habitats through indirect competition by females? Oecologia 119:367–377

    Article  Google Scholar 

  • Coulson JC, Thomas CS, Butterfield JEL, Duncan N, Monaghan PC (1983) The use of head and bill length to sex live gulls Laridae. Ibis 125:549–557

    Article  Google Scholar 

  • Cramp S, Simmons KEL (eds) (1983) The birds of the western Palearctic, vol 3. Oxford Univ Press, Oxford

    Google Scholar 

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

    Google Scholar 

  • Elliott KH, Gaston AJ, Crump D (2010) Sex-specific behaviour by a monomorphic seabird represents risk partitioning. Behav Ecol 21:1024–1032

    Article  Google Scholar 

  • Flore B-O (1999) High numbers of Lesser Black-backed Gulls Larus fuscus foraging at trawlers and in natural feeding flocks in the Southeastern North Sea. Atl Seabirds 1:182–186

    Google Scholar 

  • Furness RW, Hudson AV, Ensor K (1988) Interactions between scavenging seabirds and commercial fisheries around the British Isles. In: Burger J (ed) Seabirds and other vertebrates: competition, predation and other interactions. Columbia University Press, New York, pp 240–268

    Google Scholar 

  • Furness RW, Ensor K, Hudson AV (1992) The use of fishery waste by gull populations around the British Isles. Ardea 80:105–113

    Google Scholar 

  • Gallien L (1936) Observations sur l’essaimage de Nereis (Eunereis) longissima Johnston sur la côte Boulonnaise. Bull Soc Zool Fr 61:407–411

    Google Scholar 

  • Garthe S, Hüppop O (1998) Foraging success, kleptoparasitism and feeding techniques in scavenging seabirds: does crime pay? Helgol Meeresunters 52:187–196

    Article  Google Scholar 

  • González-Solís J, Croxall JP, Wood JP (2000) Sexual dimorphism and sexual segregation in foraging strategies of northern giant petrels, Macronectes halli, during incubation. Oikos 90:390–398

    Article  Google Scholar 

  • Götmark F (1984) Food and foraging in five species of Larus gulls in the breeding season: a comparative review. Orn Fenn 61:9–18

    Google Scholar 

  • Greig S, Coulson JC, Monaghan P (1985) Feeding strategies of male and female adult Herring Gulls (Larus argentatus). Behaviour 94:41–59

    Article  Google Scholar 

  • Hagemeijer EJM, Blair MJ (eds) (1997) The EBCC Atlas of European breeding birds, their distribution and abundance. T & AD Poyser, London

    Google Scholar 

  • Hinde RA (1956) The biological significance of the territories of birds. Ibis 98:340–369

    Article  Google Scholar 

  • Hudson AV (1989) Interspecific and age-related differences in the handling time of discarded fish by scavenging seabirds. Seabird 12:40–44

    Google Scholar 

  • Igual JM, Forero MG, Tavecchia G, Gonzalez-Solis J, Martinez-Abrain A, Hobson KA, Ruiz X, Oro D (2005) Short-term effects of data-loggers on Cory’s shearwater (Calonectris diomedea). Mar Biol 146:619–624

    Article  Google Scholar 

  • Ingolfsson A (1969) Sexual dimorphism of large gulls (Larus spp). Auk 86:732–737

    Article  Google Scholar 

  • Lewis S, Benvenuti S, Dall-Antonia L, Griffiths R, Money L, Sherratt TN, Wanless S, Hamer KC (2002) Sex-specific foraging behaviour in a monomorphic seabird. Proc R Soc B Biol Sci 269:1687–1693

    Article  CAS  Google Scholar 

  • Lewis S, Schreiber EA, Daunt F, Schenk GA, Orr K, Adam A, Wanless S, Hamer KC (2005) Sex-specific foraging behaviour in tropical boobies: Does size matter? Ibis 147:408–414

    Article  Google Scholar 

  • Lewis R, O’Connell TC, Lewis M, Campagna C, Hoelzel AR (2006) Sex-specific foraging strategies and resource partitioning in the southern elephant seal (Mirounga leonina). Proc R Soc B Biol Sci 273:2901–2907

    Article  Google Scholar 

  • Mazerolle MJ (2014) AICcmodavg: Model selection and multimodel inference based on (Q)AIC(c). R package version 2.00. http://CRAN.R-project.org/package=AICcmodavg

  • Morse Nice M (1941) The role of territory in bird life. Am Midl Nat 26:441–487

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Norberg UM (1990) Vertebrate flight: mechanics, physiology, morphology, ecology and evolution. Springer, Berlin

    Book  Google Scholar 

  • Paiva VH, Ramos JA, Martins J, Almeida A, Carvalho A (2008) Foraging habitat selection by Little Terns Sternula albifrons in an estuarine lagoon system of southern Portugal. Ibis 150:18–31

    Article  Google Scholar 

  • Pennycuick CJ (2008) Modelling the flying bird. Academic Press, Amsterdam

    Google Scholar 

  • Phillips RA, Xavier JC, Croxall JP (2003) Effects of satellite transmitters on albatrosses and petrels. Auk 120:1082–1090

    Article  Google Scholar 

  • Phillips RA, Silk JRD, Phalan B, Catry P, Croxall JP (2004) Seasonal sexual segregation in two Thalassarche albatross species: Competitive exclusion, reproductive role specialisation or foraging niche divergence? Proc R Soc B Biol Sci 271:1283–1291

    Article  CAS  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York

    Book  Google Scholar 

  • Pinheiro JC, Bates DM, DebRoy S, Sarkar D (2012) R Development Core Team 2012. nlme: linear and nonlinear mixed effects models. R package version 3.1-103

  • Probst G (1933) Studien über die Regeneration der Anneliden II. Die Anfangstadien der Regeneration des Körperendes von Owenie fusiformis d. ch. nebst einigen Beobachtungen über strukurelle Umgestaltungen in unverletzten Abdominalsegmenten zur Zeit der Gonadenreifung. Wilhelm Roux’ Arch Entwicklungsmech Org 127:105–150

    Article  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org/

  • Rock P (2005) Urban gulls: problems and solutions. Br Birds 98:338–355

    Google Scholar 

  • Royle NJ, Hartley IR, Parker GA (2004) Parental investment and family dynamics: interactions between theory and empirical tests. Popul Ecol 46:231–241

    Article  Google Scholar 

  • Schwemmer P, Garthe S (2005) At-sea distribution and behaviour of a surface-feeding seabird, the lesser black-backed gull Larus fuscus, and its association with different prey. Mar Ecol Progr Ser 285:245–258

    Article  Google Scholar 

  • Shaffer SA, Weimerskirch H, Costa DP (2001) Functional significance of sexual dimorphism in Wandering Albatross, Diomedea exulans. Funct Ecol 15:203–210

    Article  Google Scholar 

  • Smith NG (1966) Evolution of some arctic gulls (Larus): an experimental study of isolating mechanisms. Orn Monogr 4, American Ornithological Union

  • Sokal RR, Rohlf F (1981) Biometry. Freeman, New York

    Google Scholar 

  • Strann K-B, Vader W (1992) The nominate Lesser Black-backed Gull Larus fuscus fuscus, a gull with a tern-like feeding biology, and its recent decrease in northern Norway. Ardea 80:33–142

    Google Scholar 

  • Stull RB (1988) An introduction to boundary layer meteorology. Kluwer, Dordrecht

    Book  Google Scholar 

  • Székely T, Lislevand T, Figuerola J (2007) Sexual size dimorphism in birds. In: Fairbairn DJ, Blanckenhorn WU, Székely T (eds) Sex, size and gender roles—evolutionary studies of sexual size dimorphism. Oxford Univ Press, Oxford, pp 27–37

    Google Scholar 

  • Thaxter CB, Daunt F, Hamer KC, Watanuki Y, Harris MP, Grémillet D, Peters G, Wanless S (2009) Sex-specific food provisioning in a monomorphic seabird, the common guillemot Uria aalge: Nest defence, foraging efficiency or parental effort? J Avian Biol 40:75–84

    Article  Google Scholar 

  • Tiews K (1978) Non-commercial fish species in the German Bight: records of by-catches of the Brown Shrimp fishery. Rapp Pr verb Réun Cons Int Expl du Mer 172:259–265

    Google Scholar 

  • Tyson C, Shamoun-Baranes J, van Loon EE, Camphuysen CJ, Hintzen NT (2014) Individual specialization on fishery discards by lesser black-backed gulls (Larus fuscus). ICES J Mar Sci. doi:10.1093/icesjms/fsv021

    Google Scholar 

  • van Beek FA, van Leeuwen PI, Rijnsdorp AD (1990) On the survival of plaice and sole discards in the otter trawl and beamtrawl fisheries in the North Sea. Neth J Sea Res 26:151–160

    Article  Google Scholar 

  • van de Kam J, Ens BJ, Piersma T, Zwarts L (1999) Ecologische Atlas van de Nederlandse Wadvogels. Schuyt and Co, Haarlem

    Google Scholar 

  • Walter U (1997) Quantitative analysis of discards from brown shrimp trawlers in the coastal area of the East Frisian islands. Arch Fish Mar Res 45:61–76

    Google Scholar 

  • Walter U, Becker P (1994) The significance of discards by the Brown Shrimp fisheries for seabirds in the Wadden Sea—preliminary results. Ophelia Suppl 6:253–262

    Google Scholar 

  • Weimerskirch H, Cherel Y, Cuenot-Chaillet F, Ridoux V (1997) Alternative foraging strategies and resource allocation by male and female Wandering Albatrosses. Ecology 78:2051–2063

    Article  Google Scholar 

Download references

Acknowledgments

These studies are part of a long-term demographical and ecological study on sympatric breeding gulls by the Royal Netherlands Institute for Sea Research (NIOZ) at Texel. We are grateful to Staatsbosbeheer Texel for permission to work in Kelderhuispolder, a nature reserve closed for the general public. We are particularly thankful to Aris Ellen, Marcel Groenendaal, and Erik van der Spek for help and cooperation. A ringing licence was supplied every year by Vogeltrekstation, Heteren. The Royal NIOZ provided the necessary facilities and finances for these studies, and many NIOZ staff have contributed one way or the other. Cosme Damian Romay, Rim Lucassen, and Janne Ouwehand, all as students, assisted with field operations. We are grateful to Arnold Gronert who skilfully assisted with fieldwork during all years. We thank Edwin Baaij for technical support with UvA-BiTS and Michael Kemp for initial R scripts. The research infrastructure was supported by BiG-grid, LifeWatch, and the Dutch national e-science centre. We thank two anonymous referees for useful and constructive comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kees C. J. Camphuysen.

Additional information

Communicated by S. Garthe.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Camphuysen, K.C.J., Shamoun-Baranes, J., van Loon, E.E. et al. Sexually distinct foraging strategies in an omnivorous seabird. Mar Biol 162, 1417–1428 (2015). https://doi.org/10.1007/s00227-015-2678-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-015-2678-9

Keywords

Navigation