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Persistent bimodal activity patterns in wild and captive black-tailed godwit Limosa limosa under different environmental conditions

A role for circadian rhythm?

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Abstract

There is a large literature dealing with daily foraging routines of wild birds during the non-breeding season. While different laboratory studies have showed that some bird activity patterns are a persistent property of the circadian system, most of field studies preclude the potential role of an endogenous circadian rhythm in controlling bird’s foraging routines. In this study we compared the patterns of diurnal foraging activity and intake rates of migrating black-tailed godwits, Limosa limosa (radio-tagged and non-tagged individuals) at two stopover sites (habitats) with different environmental characteristics, aiming at identifying proximate factors of bird activity routines. To gain insights into the role of food availability in control of such foraging routines, we also estimated foraging activity patterns in captive godwits subjected to constant food availability. Captive and wild black-tailed godwits showed a persistent bimodal activity pattern through daylight period. Food availability had a significant effect on the intake rates, but had a subtler effect on foraging and intake rate rhythms. Temperature and wind speed (combined in a weather index) showed non-significant effects on both rhythms. Although we could not discard a role for natural diurnal changes in light intensity, an important timing cue, our findings support the idea that an endogenous circadian rhythm could be an important proximate factor regulating foraging activity and food items taken per unit time of wild black-tailed godwits during migration.

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References

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267

    Article  PubMed  CAS  Google Scholar 

  • Aschoff J (1966) Circadian activity patterns with two peaks. Ecology 47:657–662

    Article  Google Scholar 

  • Aschoff J (1981) Biological clocks in birds. Proc Int Ornithol Congress 17:113–136

    Google Scholar 

  • Barbosa A (1997) Foraging strategy and predator avoidance behaviour: an intraspecific approach. Acta Oecol 18:615–620

    Article  Google Scholar 

  • Bednekoff PA, Houston AI (1994) Avian daily foraging patterns—effects of digestive constraints and variability. Evol Ecol 8:36–52

    Article  Google Scholar 

  • Bhatt D, Sengupta S (1991) Evidence for the contribution from a circadian oscillator to the feeding rhythm in a tropical bird, Lonchura punctulata. J Interdiscipl Cycle 22:367–371

    Article  Google Scholar 

  • Brackenbury J (2006) Swimming kinematics and wake elements in a worm-like insect: the larva of the midge Chironomus plumosus (Diptera). J Zool 260:195–201

    Article  Google Scholar 

  • Brandt MJ, Cresswell W (2009) Diurnal foraging routines in a tropical bird, the rock finch Lagonosticta sanguinodorsalis: how important is predation risk? J Avian Biol 40:90–94

    Article  Google Scholar 

  • Brodin A (2007) Theoretical models of adaptative energy management in small wintering birds. Phil Trans R Soc B 362:1857–1871

    Article  PubMed  Google Scholar 

  • Burger J, Gochfeld M (1991) Human activity influences diurnal and nocturnal foraging of Sanderlings (Calidris alba). Condor 93:259–269

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer-Verlag, New York

    Google Scholar 

  • Caudell JN, Conover MR (2006) Energy content and digestibility of Brine Shrimp (Artemia franciscana) and other prey items of Pared Grebes (Podiceps nigricollis) on the Great Salt Lake, Utah. Biol Conserv 130:251–254

    Article  Google Scholar 

  • Cope DR (2006) Variation in daily and seasonal foraging routines of non-breeding barnacle geese (Branta leucopsis): working harder does not overcome environmental constraints. J Zool 260:65–71

    Article  Google Scholar 

  • Cresswell W (1994) Age-dependent choice of redshank (Tringa totanus) feeding location. Profitability or risk. J Anim Ecol 63:589–600

    Article  Google Scholar 

  • Davidson AJ, Menaker M (2003) Birds of a feather clock together—sometimes: social synchronization of circadian rhythms. Curr Opin Neurobiol 13:765–769

    Article  PubMed  CAS  Google Scholar 

  • Davis CA, Smith LM (2001) Foraging strategies and niche dynamics of coexisting shorebirds at stopover sites in the southern Great Plains. Auk 118:484–495

    Article  Google Scholar 

  • Downs CT (2000) Ingestion patterns and daily energy intake on a sugary diet: the Red Lory Eos bornea and the Malachite Sunbird Nectarinia famosa. Ibis 142:359–364

    Article  Google Scholar 

  • Dugan PJ (1981) The importance of nocturnal feeding in shorebirds: a consequence of increased invertebrate prey activity. In: Jones NV, Wolf WJ (eds) Feeding and survival strategies of estuarine organisms. Plenum, New York, pp 251–260

    Chapter  Google Scholar 

  • Engelmoer M, Piersma T, Altenburg W, Mes R (1984) The Banc d’Arguin (Mauritania). In: Evans PR, Goss-Custard JD, Hale WG (eds) Coastal waders and wildfowl in winter. BOU, Cambridge

    Google Scholar 

  • Estrella SM (2001) Comportamiento alimentario, selección de presas y balance energético de la Aguja Colinegra Limosa limosa en hábitats supramareales de la Bahía de Cádiz. Universidad de Cádiz, Tesis de licenciatura

    Google Scholar 

  • Estrella SM, Masero JA (2010) Prey and prey size selection by the near-threatened Black-tailed Godwit foraging on supratidal habitats during migration. Waterbirds 33:293–299

    Article  Google Scholar 

  • Evans PR (1976) Energy balance and optimal strategies in shorebirds: some implications for their distributions and movements in the non-breeding season. Ardea 64:117–139

    Google Scholar 

  • Fasola M, Canova L (1993) Diel activity of resident and immigrant waterbirds at Lake Turkana, Kenya. Ibis 135:442–450

    Article  Google Scholar 

  • Gillings S, Fuller RJ, Sutherland WJ (2005) Diurnal studies do not predict nocturnal habitat and site selection of European Golden Plovers (Pluvialis apricaria) and Northern Lawings (Vanellus vanellus). Auk 122:1249–1260

    Article  Google Scholar 

  • Gilling S, Sutherland WJ (2007) Comparative diurnal and nocturnal diet and foraging in Eurasian Plovers Pluvialis apricaria and Northern Lapwings Vanellus vanellus wintering on arable farmland. Ardea 95:243–257

    Article  Google Scholar 

  • Granadeiro JP, Nunes M, Silva MC, Furness RW (1998) Flexible foraging strategy of Cory’s shearwater, Calonectris diomedea, during the chick-rearing period. Anim Behav 56:1169–1176

    Article  PubMed  Google Scholar 

  • Gwinner E, Hau M (2000) Pineal gland, circadian rhythms and photoperiodism. In: Whittow CG (ed) Sturkie’s avian physiology. Academic Press, pp. 557–658

  • Herichová I, Zeman M, Juráni M, Lamosová D (2004) Daily rhythms of melatonin and selected biochemical parameters in plasma of Japanese Quail. Avian Poult Biol Rev 15:205–210

    Article  Google Scholar 

  • Hortas F (1997) Evolución de las comunidades de aves limícolas en salinas del suroeste de España. Estructura espacio-temporal de las comunidades y uso del hábitat. Doctoral thesis, University of Cadiz, Spain

    Google Scholar 

  • Jacquet JM, Launay F (1997) Diurnal behavioural patterns in the Houbara Bustard (Clamydotis undulata) in captivity: effects of temperature and daylength. Appl Anim Behav Sci 55:137–151

    Article  Google Scholar 

  • Kronfeld-Schor N, Dayan T (2003) Partitioning of time as an ecological resource. Annu Rev Ecol Evol Syst 34:153–181

    Article  Google Scholar 

  • Kuijper DPJ, Wymenga E, van der Kamp J, Tanger D (2006)

  • Kuwae T (2007) Diurnal and nocturnal feeding rate in Kentish Plovers Charadrius alexandrinus on an intertidal flat as recorded by telescopic video systems. Mar Biol 151:663–673

    Article  Google Scholar 

  • Lazzari CR, Insausti TC (2008) Circadian rhythms in insects. In: Fanjul-Moles ML, Aguilar R (eds) Comparative aspects of circadian rhythms. Transworld Research Network, Kerala, India, pp 75–92

    Google Scholar 

  • Lindström A (1991) Maximum fat deposition rates in migrating birds. Ornis Scand 22:12–19

    Article  Google Scholar 

  • Lourenço PM, Piersma T (2008) Stopover ecology of Black-tailed Godwits Limosa limosa limosa in Portuguese rice fields: a guide on where to feed in winter. Bird Study 55:194–202

    Article  Google Scholar 

  • Lourenço PM, Mandema FS, Hooijmeijer JCEW, Granadeiro JP, Piersma T (2010) Site selection and resource depletion in Black-tailed Godwits Limosa l. limosa eating rice during northward migration. J Anim Ecol 79:522–528

    Article  PubMed  Google Scholar 

  • Masero JA (2002) Why don’t Knots Calidris canutus feed extensively on the crustacean Artemia? Bird Study 49:304–306

    Article  Google Scholar 

  • Masero JA (2003) Assessing alternative anthropogenic habitats for conserving waterbirds: Salinas as buffer areas against the impact of natural habitat loss for shorebirds. Biodiv Conserv 12:1157–1173

    Article  Google Scholar 

  • Masero JA, Pérez-Hurtado A, Castro M, Arroyo GM (2000) Complementary use of intertidal mudflats and adjacent salinas by foraging waders. Ardea 88:177–191

    Google Scholar 

  • Masero JA, Santiago-Quesada F, Sánchez-Guzmán JM, Abad-Gómez JM, Villegas A, Albano N (2009) Geographical origin, between-years site fidelity, and movements of the near-threatened Black-tailed Godwits Limosa limosa staying at a major stopover site of Iberia. Ardeola 56:253–258

    Google Scholar 

  • Masero JA, Santiago-Quesada F, Sánchez-Guzmán JM, Villegas A, Abad-Gómez JM, Lopes RJ, Encarnação V, Corbacho C, Morán R (2011) Long lengths of stay and large numbers of the near-threatened Black-tailed Godwit Limosa limosa in rice fields during spring migration. Bird Conserv Int 21:12–24

    Article  Google Scholar 

  • McNamara JM, Houston AI, Lima SL (1994) Foraging routines in small birds in winter: a theoretical investigation. J Avian Biol 25:287–302

    Article  Google Scholar 

  • McNeil R, Diaz OD, Linero I, Rodríguez JR (1995) Day-time and night-time prey availability for waterbirds in a tropical lagoon. Can J Zool 73:869–878

    Article  Google Scholar 

  • Ntiamoa-Baidu Y, Piersma T, Wiersma P, Poot M, Battley P, Gordon C (1998) Water depth selection, daily feeding routines and diets of waterbirds in coastal lagoons in Ghana. Ibis 140:89–103

    Article  Google Scholar 

  • Olsson O, Wittander U, Nilsson SG (2000) Daily foraging routines and feeding effort of a small bird feeding on a predictable resource. Proc R Soc Lond B 267:1457–1461

    Article  CAS  Google Scholar 

  • Pienkowski MW (1983) Changes in the foraging pattern of plovers in relation to environmental factors. Anim Behav 31:244–264

    Article  Google Scholar 

  • Piersma T, De Goeij P, Tulp I (1993) An evaluation of intertidal feeding habitats from a shorebird perspective: towards relevant comparisons between temperate and tropical mudflats. Neth J Sea Res 31:503–512

    Article  Google Scholar 

  • Piersma T, Verkuil Y, Tulp I (1994) Resources for long-distance migration of knots Calidris canutus islandica and C.c. canutus: how broad is the temporal exploitation window of benthic prey in the western and eastern Wadden Sea. Oikos 71:393–407

    Article  Google Scholar 

  • Reebs SG (2002) Plasticity of daily and circadian activity rhythms in fishes. Rev Fish Biol Fisher 12:349–371

    Article  Google Scholar 

  • Robert M, McNeil R (1989) Comparative day and night feeding strategies of shorebirds species in a tropical environment. Ibis 131:69–79

    Article  Google Scholar 

  • Roth TC, Lima SL, Vetter WE (2006) Determinants of predation risk in small wintering birds: a hawk’s perspective. Behav Ecol Sociobiol 60:195–204

    Article  Google Scholar 

  • Roth TC, Lima SL (2007) The predatory behavior of wintering Accipiter hawks: temporal patterns in activity of predators and prey. Oecologia 152:169–178

    Article  PubMed  Google Scholar 

  • Sánchez JM, Sánchez A, Fernández A, Muñoz A (1993) La grulla común (Grus grus) en Extremadura. Status y relación con el uso del suelo. University of Extremadura, Spain

    Google Scholar 

  • Sánchez-Guzmán JM, Morán R, Masero JA, Corbacho C, Costillo E, Villegas A, Santiago-Quesada F (2007) Identifying new buffer areas for conserving waterbirds in the Mediterranean basin: the importance of the rice fields in Extremadura, Spain. Biodiv Conserv 16:3333–3344

    Article  Google Scholar 

  • Santiago-Quesada F, Masero JA, Albano N, Villegas A, Sánchez-Guzmán JM (2009) Sex differences in digestive traits in sexually size-dimorphic birds: insights from an assimilation efficiency experiment on Black-tailed Godwit. Comp Biochem Phys A 152:565–568

    Article  Google Scholar 

  • Savory CJ (1980) Diurnal feeding patterns in domestic fowls: a review. Appl Anim Ethol 6:71–82

    Article  Google Scholar 

  • Savory CJ (1988) Rates of eating by domestic fowls in relation to changing food deficits. Appetite 10:57–65

    Article  PubMed  CAS  Google Scholar 

  • Stelzer RJ, Stanewsky R, Chittka L (2010) Circadian foraging rhythms of Bumblebees monitored by radio-frequency identification. J Biol Rhythm 25:257–267

    Article  Google Scholar 

  • Swennen C, Leopold MF, de Bruijn LLM (1989) Time-stressed oystercatchers, Haematopus ostralegus, can increase their intake rate. Anim Behav 38:8–22

    Article  Google Scholar 

  • Taylor SG, Paul WL (2006) Minimal diurnal change in foraging time in an Australian passerine, the white-browed babbler Pomatostomus superciliosus. J Avian Biol 37:527–531

    Article  Google Scholar 

  • Van der Veen IT (1999) Effects of predation risk on diurnal mass dynamics and foraging routines of yellowhammers (Emberiza citrinella). Behav Ecol 10:545–551

    Article  Google Scholar 

  • Van der Veen IT (2000) Daily routines and predator encounters in Yellowhammers Emberiza citronella in the field during winter. Ibis 142:413–420

    Article  Google Scholar 

  • Vila C, Rodríguez-Teijeiro JD, Oliva F (1996) Diurnal cycles in microhabitat use by forest passerines: consequences for community structure. Ibis 138:308–314

    Article  Google Scholar 

  • Warnock N, Takekawa JY (2003) Use of radio telemetry in studies of shorebirds: past contributions and future directions. Wader Study Group Bull 100:138–150

    Google Scholar 

  • Welcker J, Harding AMA, Karnovsky NJ, Steen H, Strom H, Gabrielsen GW (2009) Flexibility in the bimodal foraging strategy of a high Arctic alcid, the Little auk Alle alle. J Avian Biol 40:388–399

    Article  Google Scholar 

  • Woelfle MA, Johnson CH (2009) The adaptive value of the circadian clock system in cyanobacteria. In: Ditty LJ, Mackey RS, Johnson CH (eds) Bacterial circadian programs. Springer, Berlin, pp 205–211

    Chapter  Google Scholar 

  • Yasué M, Quinn JL, Cresswell W (2003) Multiple effects of weather on the starvation and predation risk tradeoff in choice of feeding location in redshanks. Funct Ecol 17:727–736

    Article  Google Scholar 

  • Yasué M (2005) The effects of human presence, flock size and prey density on shorebird foraging rates. J Ethol 23:199–204

    Article  Google Scholar 

  • Zwarts L, Blomert AM, Hupkes R (1990) Increase of feeding time in waders preparing for spring migration from the Banc d’Arguin, Mauritania. Ardea 78:237–256

    Google Scholar 

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Acknowledgments

We are very grateful to Noelia Albano, José M. Abad-Gómez, Auxiliadora Villegas, Fátima Sanz, and Macarena Castro for their most useful help during capture, tracking activities, and counts of foraging activity. Guillermo Fernandez and Will Creswell provided useful comments on a first draft of the manuscript. Project PRI 2PR03A010 (Junta de Extremadura), and a grant to F. Santiago-Quesada from the Spanish Ministry of Education and Science provided financial support for this study.

Ethical standards

Black-tailed godwit captures, ringing and tagging procedures and the experiment in captivity were performed under licence CN04/1224 of Junta Extremadura, in the frame of the project PRI 2PR03A010 and following general ethical guidelines for animal welfare and nature conservation. Captive birds were released at the capture site once experiment was completed (3 weeks after capture), coinciding with the peak of migration in the study site (mid February; Masero et al. 2011).

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The authors declare that they have no conflict of interest.

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Correspondence to Francisco Santiago-Quesada.

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Communicated by W. Wiltschko

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Santiago-Quesada, F., Masero, J.A., Estrella, S.M. et al. Persistent bimodal activity patterns in wild and captive black-tailed godwit Limosa limosa under different environmental conditions. Behav Ecol Sociobiol 66, 397–405 (2012). https://doi.org/10.1007/s00265-011-1285-0

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