Abstract
Studies of seabird–prey interactions often focus on biotic factors, such as prey abundance, seabird biomechanics and competition. In contrast, we examined the influence of abiotic factors, particularly weather, light and tide, on the diving behaviour of thick-billed murre (Uria lomvia) foraging in the Canadian Low Arctic. We found little evidence that tide and weather influenced dive behaviour. As visual predators, light availability limits foraging opportunities; however, prey often surface at night so there may be a trade-off between increased food availability and reduced foraging ability during low-light conditions. Our data lent support to both ideas, as dive depth increased with light availability and the proportion of vertically migrating schooling prey was highest during sunup and sundown. There was no difference in dive depth between sexes outside the period of sundown; males, which forage at night, dove shallower than females in the late afternoon, which we suggest is because they specialize on shallow prey often caught at night. Apparently, adaptation for higher oxygen stores or lower oxygen consumption in deeper-diving females overrode any adaptation for improved vision in night-specialist males. We concluded that light availability interacted with prey vertical migration to impact underwater foraging abilities of breath-hold divers.
Similar content being viewed by others
References
Birkhead TR (1976) Effects of sea conditions on rates at which Guillemots feed their chicks. Brit Birds 69:490–492
Bornemann H, Mohr E, Plötz Krause G (1998) The tide as zeitgeber for Weddell seals. Polar Biol 20:396–403
Boyd IL, Staniland IJ, Martin AR (2002) Distribution of foraging by female Antarctic fur seals. Mar Ecol Prog Ser 242:285–294
Burger AE, Powell DW (1990) Diving depths and diet of Cassin’s auklet at Reef Island, British Columbia. Can J Zool 68:1572–1577
Cairns DK, Schneider DC (1990) Hot spots in cold water: feeding habitat selection by thick-billed murres. Stud Avian Biol 14:52–60
Cannell BL, Cullen JM (1998) The foraging behaviour of little penguins Eudyptula minor at different light levels. Ibis 140(3):467–471
Cook TR, Cherel Y, Bost CA, Tremblay Y (2007) Chick-rearing Crozet shags (Phalacrocorax melanogenis) display sex-specific foraging behaviour. Antarctic Science 19(01):55–63
Cottin M, Raymond B, Kato A, Amélineau F, Le Maho Y, Raclot T, Galton-Fenzi B, Meijers A, Ropert-Coudert Y (2012) Foraging strategies of male Adélie penguins during their first incubation trip in relation to environmental conditions. Mar Biol 159:1843–1852
Croll DA, Gaston AJ, Burger AE, Konnoff D (1992) Foraging behavior and physiological adaptation for diving in thick-billed murres. Ecol 344–356
Croll DA, McLaren E (1993) Diving metabolism and thermoregulation in common and thick-billed murres. J Comp Physiol B 163(2):160–166
Davoren GK, Montevecchi WA, Anderson JT (2003) Search strategies of a pursuit-diving marine bird and the persistence of prey patches. Ecol Monogr 73:463–481
Elliott KH, Gaston AJ (2008) Mass–length relationships and energy content of fishes and invertebrates delivered to nestling thick-billed murres Uria lomvia in the Canadian Arctic, 1981–2007. Marine Ornithol 36:25–34
Elliott KH, Struik CL, Elliott JE (2003) Bald eagles, Haliaeetus leucocephalus, feeding on plainfin midshipman, Porichthys notatus, at Crescent Beach. Can Field-Nat 117:601–604
Elliott KH, Gill CE, Elliott JE (2005) The influence of tide and weather on provisioning rates of chick-rearing Bald Eagles in Vancouver Island, British Columbia. J Raptor Res 39:1–10
Elliott KH, Woo K, Gaston AJ, Benvenuti S, Dall’Antonia L, Davoren GK (2008a) Seabird foraging behaviour indicates prey type. Mar Ecol Prog Ser 354:289–303
Elliott KH, Davoren GK, Gaston AJ (2008b) Sources of bias in observations of murre provisioning behavior. J Field Ornithol 79(3):298–307
Elliott KH, Woo KJ, Gaston AJ, Benvenuti S, Dall’Antonia L, Davoren GK (2009) Central-place foraging in an arctic seabird provides evidence for Storer-Ashmole’s halo. Auk 126:613–625
Elliott KH, Shoji A, Campbell KL, Gaston AJ (2010a) Oxygen stores and foraging behavior of two sympatric, planktivorous alcids. Aquat Biol 8:221–235
Elliott KH, Gaston AJ, Crump D (2010b) Sex-specific behavior by a monomorphic seabird represents risk partitioning. Behav Ecol 21:1024–1032
Elliott KH, Chivers LS, Bessey L, Gaston AJ, Hatch SA, Kato A, Osborne O, Ropert-Coudert Y, Hare JF (2014) Windscapes shape seabird instantaneous energy costs but adult behavior buffers impact on offspring. Mov Ecol 2:17
Elliott KH, Hare JF, Le Vaillant M, Gaston AJ, Ropert-Coudert Y, Anderson WG (2015) Ageing gracefully: physiology but not behaviour declines with age in a diving seabird. Funct Ecol 29:219–228
Enstipp MR, Grémillet D, Jones DR (2007) The effects of depth, temperature and food ingestion on the foraging energetic of a diving endotherm, the double-crested cormorant (Phalacrocorax auritus). J Ornithol 148:593–600
Falk K, Benvenuti S, Dall’Antonia L, Kampp K, Ribolini A (2000) Time allocation and foraging behaviour of chick-rearing Brunnich’s guillemots Uria lomvia in high-arctic Greenland. Ibis 142:82–92
Fernández-Juricic E, Ojeda A, Deisher M, Burry B, Baumhardt P, Stark A, Ensminger AL (2013) Do male and female cowbirds see their world differently? Implications for sex differences in the sensory system of an avian brood parasite. PLoS One 8:e58985
Finney SK, Wanless S, Harris MP (1999) The effect of weather on the feeding behaviour of a diving bird, the common guillemot Uria aalge. J Avian Biol 30:23–30
Fraser NHC, Metcalfe NB (1997) The cost of becoming nocturnal: feeding efficiency in relation to light intensity in juvenile Atlantic salmon. Funct Ecol 11:385–391
Frere E, Quintana F, Gandini P (2002) Diving behavior of the Red-legged Cormorant in southeastern Patagonia, Argentina. Condor 104:440–444
Furness RW, Bryant DM (1996) Effect of wind on field metabolic rates of breeding northern fulmars. Ecology 77:1181–1188
Gandini P, Frere E, Quintana F (2005) Feeding performance and foraging area of the Red-legged Cormorant. Waterbirds 28:41–45
Garthe S, Montevecchi WA, Davoren GK (2007) Flight destinations and foraging behaviour of northern gannets (Sula bassana) preying on a small forage fish in a low-Arctic ecosystem. Deep Sea Res II 54:311–320
Gaston AJ, Elliott KH (2014) Seabird diet changes in northern Hudson Bay, 1981–2013, reflect the availability of schooling prey. Mar Ecol Prog Ser 513:211–223
Gaston AJ, Gilchrist HG, Mallory ML, Smith PA (2009) Changes in seasonal events, peak food availability, and consequent breeding adjustment in a marine bird: a case of progressive mismatching. Condor 111(1):111–119
Gaston AJ, Woo K, Hipfner JM (2003) Trends in forage fish populations in northern Hudson Bay since 1981, as determined from the diet of nestling thick-billed murres Uria lomvia. Arctic 56:227–233
Gaston AJ, Gilchrist HG, Hipfner JM (2005) Climate change, ice conditions and reproduction in an Arctic nesting marine bird: the thick-billed murre (Uria lomvia L.). J Anim Ecol 74:832–841
Gende SM, Wilson MF, Jacobsen M (1997) Reproductive success of bald eagles (Haliaeetus leucocephalus) and its association with habitat or landscape features and weather in southeast Alaska. Can J Zool 75:1595–1604
Gilchrist HG, Gaston AJ, Smith JNM (1998) Wind and prey nest sites as foraging constraints on an avian predator, the glaucous gull. Ecology 79:2403–2414
Gray CM, Hamer KC (2001) Food-provisioning behaviour of male and female Manx shearwaters, Puffinus puffinus. Anim Behav 62(1):117–121
Grigg GC, Farwell W, Kinney J, Harlow P, Taplin LE, Johansen K, Johansen K (1985) Diving and amphibious behavior in free-living Crocodylus porosus. Aust Zool 21:599–605
Grubb TGJ (1977) Weather-dependent foraging in ospreys. Auk 94:146–149
Haney JC, Schauer AES (1994) Environmental variability facilitates coexistence within an alcid community at sea. Mar Ecol Prog Ser 103:221–237
Harding A, Paredes R, Suryan R, Roby D, Irons D, Orben R, Renner H, Young R, Kitaysky A (2013) Does location really matter? An inter-colony comparison of seabirds breeding at varying distances from productive oceanographic features in the Bering Sea. Deep Sea Res Part II 94:178–191
Harter BB (2007) Black guillemots as indicators of change in the near-shore arctic marine ecosystem. University of Manitoba M.Sc. thesis
Hatch SA (1984) Nestling diet and feeding rates of rhinoceros auklets in Alaska. Marine birds: their feeding ecology and commercial fisheries relationships. In: Proceedings of the Pacific Seabird group symposium, Seattle, January 1982, pp 106–115
Heath JP, Gilchrist HG (2010) When foraging becomes unprofitable: energetic of diving in tidal currents by common eiders wintering in the Arctic. Mar Ecol Prog Ser 403:279–290
Heath JP, Gilchrist HG, Ydenberg RC (2006) Regulation of stroke pattern and swim speed across a range of current velocities: diving by common eiders wintering in polynyas in the Canadian Arctic. J Exp biol 209(20):3974–3983
Heath JP, Gilchrist HG, Ydenberg RC (2010) Interactions between rate processes with different timescales explain counterintuitive foraging patterns of arctic wintering eiders. Proceedings of the Royal Society of London B: Biol Sci rspb20100812
Hedd A, Regular PM, Montevecchi WA, Buren AD, Burke CM, Fifield DA (2009) Going deep: common murres dive into frigid water for aggregated, persistent and slow-moving capelin. Mar Biol 156:741–751
Holm KJ, Burger AE (2002) Foraging behavior and resource partitioning by diving birds during winter in areas of strong tidal currents. Waterbirds 25(3):312–325
Horning M, Trillmich F (1999) Lunar cycles in diel prey migrations exert a stronger effect on the diving of juveniles than adult Galapagos fur seals. Proc R Soc B 266:1127–1132
Jetz W, Steffen J, Linsenmair KE (2003) Effects of light and prey availability on nocturnal, lunar and seasonal activity of tropical nightjars. Oikos 103:627–639
Jones IL, Rowe S, Carr SM, Fraser G, Taylor P (2002) Different patterns of parental effort during chick-rearing by female and male thick-billed murres (Uria lomvia) at a low-arctic colony. Auk 119:1064–1074
Konarzewski M, Taylor JRE (1989) The influence of weather conditions on growth of little auk Alle alle chicks. Ornis Scand 20:12–16
Kooyman GL (1975) A comparison between day and night diving in the Weddell seal. J Mammal 56:563–574
Luque SP, Arnould JPY, Miller EH, Cherel Y, Guinet C (2007) Foraging behaviour of sympatric Antarctic and subantarctic fur seals: does their contrasting duration of lactation make a difference? Mar Biol 152:213–224
Mallory ML, Gaston AJ, Forbes MR, Gilchrist HG (2009) Influence of weather on reproductive success of northern fulmars in the Canadian high Arctic. Polar Biol 32:529–538
McMahon TE, Holanov SH (1995) Foraging success of largemouth bass at different light intensities: implications for time and depth of feeding. J Fish Biol 46:759–767
Mehlum F, Watanuki Y, Takahashi A (2001) Diving behaviour and foraging habitats of Brunnich’s guillemots (Uria lomvia) breeding in the high-arctic. J Zool (Lond) 255:413–423
Montevecchi WA (2007) Binary dietary responses of northern gannets Sula bassana indicate changing food web and oceanographic conditions. Mar Ecol Prog Ser 352:213–220
Nevins HM (2004) Diet, demography, and diving behaviour of the common murre (Uria aalge) in central California. M.Sc. thesis, San Francisco State University, CA
Paredes R, Jones IL, Boness DJ, Tremblay Y, Renner M (2008) Sex-specific differences in diving behaviour of two sympatric Alcini species: thick-billed murres and razorbills. Can J Zool 86:610–622
Piatt JF, McLagan RL (1987) Common murre (Uria aalge) attendance patterns at Cape St. Mary’s, Newfoundland. Can J Zool 65:1530–1534
Piatt JF, Harding AMA, Shultz M, Speckman SG, Van Pelt TI, Drew GS, Kettle AB (2007) Seabirds as indicators of marine food supplies: cairns revisited. Mar Ecol Prog Ser 352:221–234
Piersma T, Lindeboom R, Van Eerden MR (1988) Foraging rhythm of great created grebes Podiceps cristatus adjusted to diel variations in the vertical distribution of their prey Osmerus eperlanus in a shallow eutrophic lake in the Netherlands. Oecologia 76:481–486
Regular PM, Davoren GK, Hedd A, Montevecchi WA (2010) Crepuscular foraging by a pursuit-diving seabird: tactics of common murres in response to the diel vertical migration of capelin. Mar Ecol Prog Ser 415:295–304
Regular PM, Hedd A, Montevecchi WA (2011) Fishing the dark: a pursuit-diving seabird modifies foraging behavior in response to nocturnal light levels. PLoS One 6:e26763
Riou S, Hamer KC (2008) Predation risk and reproductive effort: impacts of moonlight on food provisioning and chick growth in Manx shearwaters. Anim Behav 76:1743–1748
Robinson JA, Hamer KC, Chivers LS (2002) Developmental plasticity in Arctic Terns Sterna paradisaea and Common Terns S. hirundo in response to a period of extremely bad weather. Ibis 144:344–346
Rubolini D, Maggini I, Ambrosini R, Imperio S, Paiva VH, Gaibani G, Saino N, Cecere JG (2015) The effect of moonlight on scopoli's shearwater calonectris diomedea colony attendance patterns and nocturnal foraging: a test of the foraging efficiency hypothesis. Ethol 121(3):284–299
Ropert-Coudert Y, Wilson RP, Daunt F, Kato A (2004) Patterns of energy acquisition by a central place forager: benefits of alternating short and long foraging trips. Behav Ecol 15:824–830
Schwemmer P, Garthe S (2010) Spatial and temporal patterns of habitat use by Eurasian oystercatchers (Haematopus ostralegus) in the eastern Wadden Sea revealed using GPS data loggers. Mar Biol 158:541–550
Shoji A, Elliott KH, Aris-Brosou S, Crump D, Gaston AJ (2010) Incubation patterns in a central-place forager affect lifetime reproductive success: scaling of patterns from a foraging bout to a lifetime. PLoS One 6:e17760
Tarlow EM, Hau M, Anderson DJ, Wikelski M (2003) Diel changes in plasma melatonin and corticosterone concentrations in tropical Nazca boobies (Sual granti) in relation to moon phase and age. Gen Comp Endocrinol 133:297–304
Thaxter CB, Daunt F, Hamer KC, Watanuki Y et al (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
Tremblay Y, Cherel Y, Oremus M, Tveraa T, Chastel O (2003) Unconventional ventral attachment of time-depth recorders as a new method for investigating time budget and diving behaviour of seabirds. J Exp Biol 206:1929–1940
Watson JW, Garrett MG, Anthony RG (1991) Foraging ecology of bald eagles in the Columbia River estuary. J Wildl Manag 55:492–499
Weimerskirch H, Chastel O, Ackermann L, Chaurand T, Cuenot-Chaillet F, Hindermeyer X, Judas J (1994) Alternate long and short foraging trips in pelagic seabird parents. Anim Behav 47(2):472–476
Welcker J, Harding A, Karnovsky NJ, Steen H, Strøm H, Gabrielsen GW (2009) Flexibility in the bimodal foraging strategy of a high Arctic alcid, the little auk Alle alle. J Avian Biol 40(4):388–399
White CR, Day N, Butler PJ, Martin GR (2007) Vision and foraging in cormorants: more like herons than hawks? PLoS One 2:e639
Wilson RP, Puetz K, Bost CA, Culik BM, Bannasch R, Reins T, Adelung D (1993) Diel dive depth in penguins in relation to diel vertical migration of prey: whose dinner by candlelight? Mar Ecol Prog Ser 94:101–104
Wilson RP, Locca R, Scolaro JA, Laurenti S, Upton J, Gallelli H, Frere E, Gandini P (2001) Magellanic penguins Spheniscus magellanicus commuting through San Julian Bay; do currents induce tidal tactics? J Avian Biol 32:83–89
Wilson RP, McMahon CR, Quintana F, Frere E, Scolaro A, Hays GC, Bradshaw CJA (2011) N-dimensional animal energetic niches clarify behavioural options in a variable marine environment. J Exp Biol 214:646–656
Zeenath C, Zacharias VJ (2010) Foraging behavior and diving pattern of little cormorant Phalacrocorax niger (Vieillot) (Pelecaniformes: Phalacrocoracidae) at Kallampara backwaters, Kerala, India. J Threat Taxa 2:1382–1386
Zimmer I, Wilson RP, Beaulieu M, Ancel A, Ploetz J (2008) Seeing the light: depth and time restrictions in the foraging capacity of emperor penguins at Pointe Geologie, Antarctica. Aquat Biol 3:217–226
Acknowledgments
We especially thank P. Regular for providing a copy of his R script. K. Ashbrook, M. Barrueto, K. Elner, A. Hargreaves, S. Jacobs, G. Lancton, M. LeVaillant, E. Grosbellet, A. Moody, R. Rankin, A. Ronston, J. Provencher, P. Smith, K. Woo and P. Woodward helped in the field. Two reviewers provided helpful comments on an earlier version of the manuscript. J. Nakoolak kept us safe from bears. R. Armstrong at the Nunavut Research Institute, M. Mallory at the Canadian Wildlife Service Northern Research Division and C. Eberl at National Wildlife Research Centre in Ottawa provided logistical support. KHE received financial support through a NSERC Vanier Canada Graduate Scholarship, ACUNS Garfield Weston Northern Studies scholarship and AINA Jennifer Robinson Scholarship. All procedures were approved under the guidelines of the Canadian Council for Animal Care.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by V. Paiva.
Reviewed by J. Ramos and an undisclosed expert.
Rights and permissions
About this article
Cite this article
Elliott, K.H., Gaston, A.J. Diel vertical migration of prey and light availability constrain foraging in an Arctic seabird. Mar Biol 162, 1739–1748 (2015). https://doi.org/10.1007/s00227-015-2701-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-015-2701-1