Within an avian breeding population, there can be considerable variation in egg and nest site characteristics that have implications for individual reproductive success. Here we present a detailed case study of Lesser Black-backed Gulls Larus fuscus nesting on Flat Holm island, Wales, at a time when the colony was growing. This species is ground-nesting, with a modal clutch size of three. We surveyed 714 nests across the island during two consecutive years and recorded data on nest and egg characteristics, along with hatching success. We modelled how hatching success was associated with clutch size, egg volume, egg laying order and local habitat features, i.e. the amount of vegetation surrounding the nest and each nest's proximity to neighbouring nests. Eggs were most likely to hatch when they were laid in the middle of the season, were large in size, part of big clutches and in nests with a substantial amount of surrounding vegetation. Lesser Black-backed Gull productivity is currently low in many protected rural and coastal colonies throughout this species' range. Detailed information on factors influencing reproductive success could therefore indicate ways in which this species could be better managed to help maintain and conserve breeding populations.

Two key components of a bird's reproductive success in any particular breeding attempt are hatching success and chick survival to fledging (Lack 1968). Although chick survival is often the more important factor determining reproductive success in seabirds that nest in the open (Nelson 1980; Camphuysen 2013), hatching success is also important (Paludan 1951; Schreiber 1970). The latter is influenced by intrinsic factors, including parental quality and condition, which in turn contribute to egg viability (e.g. Bolton 1991; Oro et al. 2014), together with extrinsic factors such as predation and climatic conditions (e.g. Jones et al. 2008; van de Pol et al. 2010). Many birds construct nests to protect their eggs, and thereby increase their reproductive success. In seabirds, nests can range from none at all e.g. the White Tern Gygis alba (Nelson 1980) to quite elaborate structures such as those made by kittiwakes Rissa spp. (Coulson 2011).

Nests of the Lesser Black-backed Gull Larus fuscus, like those of most gulls, tend to be simple, ranging from a scrape with little gathered nesting material, to a small bed of vegetation arranged in a shallow cup. These ground-nesting seabirds, which breed primarily in northwest Europe (Malling Olsen & Larsson 2004), have traditionally occupied colonies at coastal nesting sites on flat or moderately sloping ground, which may be towards the top of cliffs, or in open, sometimes low-lying areas. Nests are therefore often quite accessible, leaving eggs (and chicks) vulnerable to predation, for example by conspecifics and other gull species that often nest nearby, or by mammalian predators such as Red Foxes Vulpes vulpes (Davis & Dunn 1976; Camphuysen et al. 2010). Predation has been found to be responsible for up to 30% of Lesser Black-backed Gull egg losses at particular sites (Paludan 1951; Camphuysen 2013). This risk can be partially offset by the benefits of colonial defence and vigilance (e.g. Götmark & Andersson 1984; Beauchamp 2009), and by nesting close to vegetation that conceals eggs from potential predators (Haycock & Threlfall 1975; Hunt & Hunt 1975; Burger & Shisler 1978). Open nest sites also leave eggs exposed to cold and inclement weather conditions, and large numbers of eggs can fail to hatch because of this (Paludan 1951; Fox et al. 1978). However, pairs can again compensate by choosing to nest in an area with shelter, for instance tall vegetation around the nest (e.g. Kim & Monaghan 2005a). The extent to which gulls are able to counteract the disadvantages of their ground-nesting breeding behaviour is thought to be influenced by aspects of their phenotypic quality (Kim & Monaghan 2005b; Oro 2008).

Establishing and maintaining a breeding territory is energetically taxing for gulls. Competition can be intense, especially for first time breeders (Chabrzyk & Coulson 1976), whilst costly aggressive interactions, including fighting, calling and displacement activities such as grass pulling, are regularly seen between even established pairs (e.g. Tinbergen 1953; Butler & Janes-Bulter 1982; Pierotti & Annett 1994). These behaviours appear to be necessary throughout the season to prevent territorial encroachments, such as the theft of nesting materials, predation of eggs or chicks and extra-pair copulations (e.g. Burger & Beer 1975; Bukacińska & Bukaciński 1994). Poor quality birds not only struggle to secure and successfully breed at a nest site in habitats favoured by superior birds, but lack the surplus energy to produce and successfully incubate the large and fertile eggs and clutches necessary to match the reproductive success of high quality individuals. Measures of nesting habitat, egg size and hatching success can therefore indicate an individual's phenotypic quality.

Breeding Lesser Black-backed Gull numbers are currently declining at many 'traditional' rural coastal sites across this species' range, including in protected areas, while breeding populations in urban areas are increasing in number and range (e.g. Camphuysen et al. 2010; Balmer et al. 2013). A thorough understanding of this species' breeding ecology is necessary to facilitate effective conservation management (for a review, see Ross-Smith et al. 2014). This is especially vital given that Lesser Black-backed Gulls that breed on rooftops in urban areas (e.g. Raven & Coulson 1997; Rock 2005) are causing an increasing public nuisance, leading to calls for ever stricter controls.

In this study, we assessed Lesser Black-backed Gull hatching success, and explored the reasons underlying hatching failure, for approximately 350 pairs each year over two consecutive seasons, across a range of nesting habitats at an island breeding colony. This colony is free of mammalian predators, and at the time of this study, the breeding population was steadily increasing and there was no apparent food stress or other external pressures known to be detrimentally affecting breeding success (Ross-Smith et al. 2013). For each egg found, we measured a number of variables.We noted the size of the clutch it was part of, as eggs from small clutches are less likely to hatch than those from large clutches (Harris 1964; Brown 1967). We recorded laying date, as hatching success has been shown to vary throughout the breeding season (Brown 1967; Davis & Dunn 1976; García Borboroglu et al. 2008), along with laying order, as within-clutch variation in egg composition, with potential implications for egg outcome, has been demonstrated in a number of studies (e.g. Royle et al. 1999). We calculated egg volume, as large eggs are more likely to hatch than small eggs (Parsons 1970; Bolton 1991).We also measured the amount of vegetation around nests, because of its influence on hatching success, as discussed above, and we calculated how nests were distributed relative to others in the colony, as proximity to conspecific nests has been found to influence reproductive success in gulls (e.g. Ewald et al. 1980; Butler & Trivelpiece 1981). We discuss the relative importance of each factor in determining hatching success and place this information in a conservation context.

We thank Dewi Langlet, Jeff Davey and the Flat Holm Project for their assistance with this project. VR-S was funded by a Cardiff University Research Studentship. Work was carried out under licences OTH:SB:02:2007/2008 from the Countryside Council for Wales. We are grateful to Ruedi Nager and an anonymous referee, whose comments greatly improved this paper. Thank you also to Kees Camphuysen for encouraging the idea of revisiting and trying to publish this work so many years after it was carried out.

Balmer, D. E., Gillings, S., Caffrey, B. J., Swann, R. L., Downie, I. S. & Fuller, R. J. 2013. Bird Atlas 2007-11: the breeding and wintering birds of Britain and Ireland. BTO Books, Thetford.

Beauchamp, G. 2009. Sleeping gulls monitor the vigilance behaviour of their neighbours. Biology Letters 5: 9-11. [Crossref]

Beer, C. G. 1961. Incubation and nest building behaviour of Black-headed Gulls. I: Incubation behaviour in the incubation period. Behaviour 18: 62-106. [Crossref]

Beer, C. G. 1965. Clutch size and incubation behavior in Black-billed Gulls (Larus bulleri). Auk 82: 1-18. [Crossref]

Bolton, M. 1991. Determinants of chick survival in the lesser black-backed gull: relative contributions of egg size and parental quality. Journal of Animal Ecology 60: 949-960. [Crossref]

Bosch, M. & Sol, D. 1998. Habitat selection and breeding success in Yellow-legged Gulls Larus cachinnans. Ibis 140: 415-421. [Crossref]

Brouwer, A., Spaans, A. L. & Dewit, A. A. N. 1995. Survival of Herring Gull Larus argentatus chicks: an experimental analysis of the need for early breeding. Ibis 137: 272-278. [Crossref]

Brown, R. G. B. 1967. Breeding success and population growth in a colony of Herring and Lesser Black-backed Gulls Larus argentatus and L. fuscus. Ibis 109: 502-515. [Crossref]

Bukacińska, M. & Bukaciński, D. 1994. Seasonal and diurnal changes in aggression and territory size in the Black-headed Gull (Larus ridibundus L.) on islands in the middle reaches of the Vistula River. Ethology 97: 329-339. [Crossref]

Burger, J. & Beer, C. G. 1975. Territoriality in the Laughing Gull (L. atricilla). Behaviour 55: 301-320. [Crossref]

Burger, J. & Shisler, J. 1978. Nest site selection and competitive interactions of Herring and Laughing Gulls in New Jersey. Auk 95: 252-266.

Butler, R. G. & Janes-Butler, S. 1982. Territoriality and behavioral correlates of reproductive success of Great Black-backed Gulls. Auk 99: 58-66. [Crossref]

Butler, R. G. & Trivelpiece, W. 1981. Nest spacing, reproductive success, and behavior of the Great Black-backed Gull (Larus marinus). Auk 98: 99-107. [Crossref]

Calladine, J. 2004. Lesser Black-backed Gull Larus fuscus. In: Mitchell, P. I., Newton, S. F., Ratcliffe, N. & Dunn, T. E. (eds.) Seabird Populations of Britain and Ireland: 226-241. Poyser, London.

Camphuysen, C. J., 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.

Camphuysen, C. J. 2013. 'A historical ecology of two closely related gull species (Laridae): multiple adaptations to a man made environment.' PhD thesis, University of Groningen.

Chabrzyk, G. & Coulson, J. C. 1976. Survival and recruitment in the Herring Gull Larus argentatus. Journal of Animal Ecology 45: 187-203. [Crossref]

Coulson, J. C. 2011. The Kittiwake. Poyser, London.

Crawley, M. J. 2007. The R Book. Wiley, New York. [Crossref]

Davis, J. W. F. & Dunn, E. K. 1976. Intraspecific predation and colonial breeding in Lesser Black-backed Gulls Larus fuscus. Ibis 118: 65-77. [Crossref]

Dexheimer, M. & Southern, W. E. 1974. Breeding success relative to nest location and density in Ring-billed Gull colonies. Wilson Bulletin 86: 288-290.

Eaton, M. A., Aebischer, N. J., Brown, A. F., Hearn, R. D., Lock, L., Musgrove, A. J., Noble, D. G., Stroud, D. A. & Gregory, R. D. 2015. Birds of Conservation Concern 4: the population status of birds in the United Kingdom, Channel Islands and Isle of Man. British Birds 108: 708-746.

Ewald, P. W., Hunt, G. L. & Warner, M. 1980. Territory size in Western Gulls: importance of intrusion pressure, defense investments, and vegetation structure. Ecology 61: 80-87. [Crossref]

Fetterolf, P. M. 1984. Aggression, nesting synchrony, and reproductive fitness in ring-billed gulls. Animal Behaviour 32: 1004-1010. [Crossref]

Fox, G. A., Gilman, A. P., Peakall, D. B., & Ankerka, F. W. 1978. Behavioral abnormalities of nesting Lake Ontario herring gulls. Journal of Wildlife Management 42: 477-483. [Crossref]

García Borboroglu, P. & Yorio, P. 2004. Effects of microhabitat preferences on kelp gull Larus dominicanus breeding performance. Journal of Avian Biology 35: 162-169. [Crossref]

García Borboroglu, P., Yorio, P., Moreno, J. & Potti, J. 2008. Seasonal decline in breeding performance of the Kelp Gull Larus dominicanus. Marine Ornithology 36: 153-157.

Good, T. P. 2002. Breeding success in the Western Gull x Glaucous-winged Gull complex: the influence of habitat and nest site characteristics. Condor 104: 353-365. [Crossref]

Götmark, F. & Andersson, M. 1984. Colonial breeding reduces nest predation in the common gull (Larus canus). Animal Behaviour 32: 485-492. [Crossref]

Grafen, A. & Hails, R. 2002. Modern statistics for the life sciences. Oxford University Press, Oxford.

Harper, C. A. 1971. Breeding biology of a small colony of Western Gulls (Larus occidentalis wymani) in California. Condor 73: 337-341. [Crossref]

Harris, M. P. 1964. Aspects of the breeding biology of the gulls Larus argentatus, L. fuscus and L. marinus. Ibis 106: 432-456. [Crossref]

Haycock, K. A. & Threlfall, W. 1975. The breeding biology of the Herring Gull in Newfoundland. Auk 92: 678-697. [Crossref]

Hunt, G. L. & Hunt, M. W. 1975. Reproductive ecology of the Western Gull: the importance of nest spacing. Auk 92: 270-279. [Crossref]

Jehl, J. R. 1994. Absence of nest density effects in a growing colony of California Gulls. Journal of Avian Biology 25: 224-230. [Crossref]

JNCC 2014. Seabird Population Trends and Causes of Change: 1986-2013 Report. (http://www.jncc.defra.gov.uk/page-3201). Joint Nature Conservation Committee. Updated August 2014. Accessed 15 October 2015.

Jones, H. P., Tershy, B. R., Zavaleta, E. S., Croll, D. A., Keitt, B. S., Finkelstein, M. E. & Howard, G. R. 2008. Severity of the effects of invasive rats on seabirds: a global review. Conservation Biology 22: 16-26. [Crossref]

Kim, S. Y. & Monaghan, P. 2005a. Effects of vegetation on nest microclimate and breeding performance of Lesser Black-backed Gulls (Larus fuscus). Journal of Ornithology 146: 176-183. [Crossref]

Kim, S. Y. & Monaghan, P. 2005b. Interacting effects of nest shelter and breeder quality on behaviour and breeding performance of Herring Gulls. Animal Behaviour 69: 301-306. [Crossref]

Kim, S.Y. & Monaghan, P. 2006. Interspecific differences in foraging preferences, breeding performance and demography in herring (Larus argentatus) and lesser black-backed gulls (Larus fuscus) at a mixed colony. Journal of Zoology 270: 664-671. [Crossref]

Lack, D. 1968. Ecological adaptations for breeding in birds. Methuen, London.

Lundberg, C. A. & Väisänen, R. A. 1979. elective correlation of egg size with chick mortality in the Black-headed Gull (Larus ridibundus). Condor 81: 146-156. [Crossref]

Malling Olsen, K. & Larsson, H. 2004. Gulls of North America, Europe and Asia. Princeton University Press, Princeton.

Martínez-Abraín, A., Oro, D., Conesa, D. & Jiménez, J. 2008. Compromise between seabird enjoyment and disturbance: the role of observed and observers. Environmental Conservation 35: 104-108. [Crossref]

Montevecchi, W. A. 1977. Predation in a salt marsh Laughing Gull colony. Auk 94: 583-585.

Murphy, E. C., Hoovermiller, A. A., Day, R. H. & Oakley, K. L. 1992. Intracolony variability during periods of poor reproductive performance at a Glaucous-winged Gull colony. Condor 94: 598-607. [Crossref]

Nager, R. G., Monaghan, P. & Houston, D. C. 2000. Within-clutch trade-offs between the number and quality of eggs: experimental manipulations in gulls. Ecology 81: 1339-1350. [Crossref]

Nelson, J. B. 1980. Seabirds. Their Biology and Ecology. Hamlyn, London.

Niizuma, Y., Takagi, M., Senda, M., Chochi, M. & Watanuki, Y. 2005. Incubation capacity limits maximum clutch size in black-tailed gulls Larus crassirostris. Journal of Avian Biology 36: 421-427. [Crossref]

Oro, D. 2008. Living in a ghetto within a local population: an empirical example of an ideal despotic distribution. Ecology 89: 838-846. [Crossref]

Oro, D., Hernandes, N., Jover, L. & Genovart, M. 2014. From recruitment to senescence: food shapes the age-dependent pattern of breeding performance in a long-lived bird. Ecology 95: 446-457. [Crossref]

Paludan, K. 1951. Contributions to the breeding biology of Larus argentatus and Larus fuscus. Videnskabelige Meddelelser fra Dansk naturhistorik Forening i Kjøbenhavn 114: 1-128.

Parsons, J. 1970. Relationship between egg size and post-hatching chick mortality in the Herring Gull (Larus argentatus). Nature 228: 1221-1222. [Crossref]

Parsons, J. 1975. Asynchronous hatching and chick mortality in the Herring Gull Larus argentatus. Ibis 117: 517-520. [Crossref]

Perrins, C. M., & Smith, S. B. 2000. The breeding Larus gulls on Skomer Island National Nature Reserve, Pembrokeshire. Atlantic Seabirds 2: 195-210

Pierotti, R. & Annett, C. 1994. Patterns of aggression in gulls: asymmetries and tactics in different social categories. Condor 96: 590-599. [Crossref]

Pierotti, R. & Bellrose, C. A. 1986. Proximate and ultimate causation of egg size and the “third-chick disadvantage” in the Western Gull. Auk 103: 401-407. [Crossref]

Pinheiro, J. C., Bates, D. M., DebRoy, S., Sarkar, D. & the R Core Team. 2015. nlme: linear and nonlinear mixed effects models. R package version 3.1-122.

R Core Team. 2015. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

Raven, S. J. & Coulson, J. C. 1997. The distribution and abundance of Larus gulls nesting on buildings in Britain and Ireland. Bird Study 44: 13-34. [Crossref]

Reid, W. V. 1988. Age-specific patterns of reproduction in the Glaucous-winged Gull: increased effort with age. Ecology 69: 1454-1465. [Crossref]

Robert, H. C. & Ralph, C. J. 1975. Effects of human disturbance on the breeding success of gulls. Condor 77: 495-499. [Crossref]

Rock, P. 2005. Urban gulls: problems and solutions. British Birds 98: 338-355.

Ross-Smith, V. H., Conway, G. J., Facey, R. J., Bailey, B. H., Lipton, M., Whitfield, S. A. & Ferns, P. N. 2013. Population size, ecology and movements of gulls breeding on Flat Holm Island. Birds in Wales 10: 7-21.

Ross-Smith, V. H., Robinson, R. A., Banks, A. N., Frayling, T. D., Gibson, C. C. & Clark, J. A. 2014. The Lesser Black-backed Gull Larus fuscus in England: how to resolve a conservation conundrum. Seabird 27: 41-61. [Crossref]

Royle, N. J., Surai, P. F., McCartney, R. J. & Speake, B. K. 1999. Parental investment and egg yolk lipid composition in gulls. Functional Ecology 13: 298-306. [Crossref]

Salzer, D. W. & Larkin, G. J. 1990. Impact of courtship feeding on clutch and third egg size in Glaucous-winged Gulls. Animal Behaviour 39: 1149-1162. [Crossref]

Schreiber, R. W. 1970. Breeding biology of Western Gulls (Larus occidentalis) on San Nicolas Island, California, 1968. Condor 72: 133-140. [Crossref]

Skórka, P., Martyka, R., Wójcik, J. D., Babiarz, T. & Skórka, J. 2006. Habitat and nest site selection in the Common Gull Larus canus in southern Poland: significance of man-made habitats for conservation of an endangered species. Acta Ornithologica 41: 137-144. [Crossref]

Sydeman, W. J., Penniman, J. F., Penniman, T. M., Pyle, P. & Ainley, D. G. 1991. Breeding performance in the western gull: effects of parental age, timing of breeding and year in relation to food availability. Journal of Animal Ecology 60: 135-149. [Crossref]

Tinbergen, N. 1953. The Herring Gull's world: a study of the social behaviour of birds. Collins Clear-Type Press, London.

van de Pol, M., Ens, B. J., Heg, D., Brouwer, L., Krol, J., Maier, M., Exo, K.-M., Oosterbeek, K., Lok, T., Eising, C. M. & Koffijberg, K. 2010. Do changes in the frequency, magnitude and timing of extreme climatic events threaten the population viability of coastal birds? Journal of Applied Ecology 47: 720-730. [Crossref]

Wood, S. N. 2006. Generalized Additive Models: An Introduction with R. Chapman and Hall/CRC, Boca Raton.