Abstract
Birds face the challenge of avoiding predators, yet the postural adjustments they use to aid their thermoregulation (resting the bill on their back plumage and standing on one leg), may diminish their capacity to detect and escape from approaching predators. This may lead to a temperature-mediated trade-off between anti-predator and thermoregulatory behaviour. In this study, we examine the effect of posture, orientation of the bird relative to their ‘blind sector’ (gap in their visual field) and temperature on the alert and escape distances of ten shorebird species (273 experimental ‘approaches’ by an investigator). We predicted that (1) heat-conserving postures would be associated with shorter FIDs (flight initiation distances: the distance at which the bird commenced fleeing from the investigator); (2) low temperatures would be linked to shorter FIDs; and (3) approaches from a bird’s blind sector would result in shorter FIDs. Phylogenetically controlled mixed models revealed head posture (backrest or forward facing) did not significantly influence alert distance (AD) or FID. Standing on two legs was associated with longer ADs. Individual species’ models revealed two significant relationships. Approaches from within the blind sector were associated with shorter ADs and FIDs in Australian Pied Oystercatcher (Haematopus longirostris), while higher temperatures were associated with shorter FIDs in Red-necked Stint (Calidris ruficollis). Despite this, we reveal no strong evidence that wild-living shorebirds trade-off antipredator capacity and thermoregulatory behaviours. However, further investigation is warranted across a wider variety of birds.
Zusammenfassung
Der Einfluss von Ruhestellung und Körperausrichtung auf Wachsamkeit und Flucht bei Küstenvögeln
Vögel müssen Räubern aus dem Weg gehen, aber ihre Körperhaltung zur Unterstützung ihrer Temperaturregulation (den Schnabel auf dem Rückengefieder abstützen und auf einem Bein stehen) verringern möglicherweise ihre Fähigkeit, nahende Räuber zu erkennen und ihnen zu entkommen. Dies kann zu einem temperaturbeeinflussten Kompromiss zwischen Räuber-Vermeidung und Thermoregulationsverhalten führen. In dieser Studie untersuchten wir für zehn Küstenvogelarten (mit 273 experimentellen „Annäherungen “ durch einen Versuchsleiter) die Auswirkungen der Körperhaltung, der Ausrichtung des Vogels relativ zu seinem „blinden Bereich “ (Lücke in seinem Gesichtsfeld) und der Temperatur auf die Alarm- und Fluchtdistanzen. Wir sagten voraus, dass: 1) wärmesparende Körperhaltungen mit kürzeren FIDs (Flugauslösedistanzen: die Entfernung, in der ein Vogel die Flucht vor einem sich Nähernden beginnt) verbunden sind; 2) niedrige Temperaturen mit kürzeren FIDs verknüpft sind; und 3) Annäherungen aus dem „blinden Bereich “ eines Vogels zu kürzeren FIDs führen. Phylogenetisch kontrollierte gemischte Modelle zeigten, dass die Kopfhaltung (nach hinten oder nach vorne gerichtet) keinen signifikanten Einfluss auf die Aufmerksamkeitsdistanz (AD) oder den FID hatte. Auf zwei Beinen zu stehen war mit längeren ADs verbunden. Die Modelle für die einzelnen Arten ergaben zwei signifikante Zusammenhänge. Beim Australausternfischer (Haematopus longirostris) hingen Annäherungen aus dem blinden Bereich mit kürzeren ADs und FIDs zusammen, während beim Rotkehl-Strandläufer (Calidris ruficollis) höhere Temperaturen mit kürzeren FIDs verknüpft waren. Abgesehen hiervon fanden wir keine eindeutigen Beweise dafür, dass freilebende Küstenvögel ihre Fähigkeit zur Vermeidung von Räubern gegen ihr Thermoregulationsverhalten abwägen. Weitere Untersuchungen bei einer größeren Anzahl von Vögeln wären jedoch wünschenswert.
Similar content being viewed by others
References
Antos MJ, Ehmke GE, Tzaros CL, Weston MA (2007) Unauthorised human use of an urban coastal wetland sanctuary: current and future patterns. Landsc Urban Plan 80:173–183
Atkinson PW, Clark NA, Bell MC, Dare PJ, Clark JA, Ireland PL (2003) Changes in commercially fished shellfish stocks and shorebird populations in the Wash, England. Biol Conserv 114:127–141
Azaki DB, Cresswell W (2021) Level of local human disturbance and feeding state determines escape behaviour in Eurasian Oystercatchers. Ethology 127:986–994
Bartoń K (2020) MuMIn: multi-model inference. R package version 1.43.17. https://CRAN.R-project.org/package=MuMIn
Basso E, Fonseca J, Drever MC, Navedo JG (2018) Effects of intertidal habitat availability on the use of anthropogenic habitats as foraging grounds by shorebirds: a case study on semi-intensive shrimp farms. Hydrobiologia 809:19–29
Bernays EA, Wcislo WT (1994) Sensory capabilities, information processing, and resource specialization. Q Rev Biol 69:187–204
Blumstein DT (2003) Flight-Initiation distance in birds is dependent on intruder starting distance. J Wildl Manag 67:852–857
Blumstein DT (2006) Developing an evolutionary ecology of fear: how life history and natural history traits affect disturbance tolerance in birds. Anim Behav 71:389–399
Blumstein DT (2014) Attention, habituation, and antipredator behaviour: implications for urban birds. In: Gill D, Brumm H (eds) Avian urban ecology: behavioural and physiological adaptations. Oxford University Press, pp 41–53
Blumstein DT (2016) Habituation and sensitization: new thoughts about old ideas. Anim Behav 120:255–262
Blumstein DT, Anthony LL, Harcourt R, Ross G (2003) Testing a key assumption of wildlife buffer zones: is flight initiation distance a species-specific trait? Biol Conserv 110:97–100
Brodsky LM, Weatherhead PJ (1984) Behavioural thermoregulation in wintering black ducks: roosting and resting. Can J Zool 62:1223–1226
Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer
Campos DP, Bander LA, Raksi A, Blumstein DT (2009) Perch exposure and predation risk: a comparative study in passerines. Acta Ethol 12:93–98
Cantlay JC, Portugak SJ, Martin GR (2019) Visual fields and foraging ecology of Blacksmith Lapwings Vanellus armatus. Ibis 161:895–900
Caro TM (2005) Antipredator defences in birds and mammals. Chicago Press
Carr JM, Lima SL (2012) Heat-conserving postures hinder escape: a thermoregulation–predation trade-off in wintering birds. Behav Ecol 23:434–441
Carrascal LM, Alonso CL (2006) Habitat use under latent predation risk. A case study with wintering forest birds. Oikos 112:51–62
Carrascal LM, Díaz JA, Huertas DL, Mozetich I (2001) Behavioral thermoregulation by treecreepers: trade-off between saving energy and reducing crypsis. Ecology 82:1642–1654
Clemens R, Oldland J, Berry L, Purnell C (2009) Migratory shorebird population monitoring project. In: Report to Department of Environment, Water, Heritage and Arts and World Wildlife Fund. Birds Australia
Colwell MA, Danufsky T, Fox-Fernandez NW, Roth JE, Conklin JR (2003) Variation in shorebird use of diurnal, high-tide roosts: how consistently are roosts used? Waterbirds 26:484–493
Dawson W, Whittow G (1999) Regulation of body temperature. In: Whittow G (ed) Sturkie’s avian physiology. Academic Press, pp 343–390
De Villemereuil P, Nakagawa S (2014) General quantitative genetic methods for comparative biology. In: Garamszegii LZ (ed) Modern phylogenetic comparative methods and their application in evolutionary biology. Springer, pp 287–303
Dekker D, Dekker I, Christie D, Ydenberg R (2011) Do staging Semipalmated Sandpipers spend the high-tide period in flight over the ocean to avoid falcon attacks along shore? Waterbirds 34:195–201
Devereux CL, Fernández-Juricic E, Krebs JR, Whittingham MJ (2008) Habitat affects escape behaviour and alarm calling in Common Starlings Sturnus vulgaris. Ibis 150:191–198
Dias MP, Granadeiro JP, Lecoq M, Santos CD, Palmeirim JM (2006) Distance to high-tide roosts constrains the use of foraging areas by Dunlins: implications for the management of estuarine wetlands. Biol Conserv 131:446–452
Domínguez J, Vidal M (2007) Vigilance behaviour of preening black-tailed Godwit Limosa limosa in roosting flocks. Ardeola 54:227–235
Dowding JE, Murphy EC (2001) The impact of predation by introduced mammals on endemic shorebirds in New Zealand: a conservation perspective. Biol Conserv 99:47–64
Durrell S (2000) Individual feeding specialisation in shorebirds: population consequences and conservation implications. Biol Rev 75:503–518
Ekanayake KB, Weston MA, Nimmo DG, Maguire GS, Endler JA, Küpper C (2015) The bright incubate at night: sexual dichromatism and adaptive incubation division in an open-nesting shorebird. Proc R Soc B 282:20143026
Fernández-Juricic E (2012) Sensory basis of vigilance behavior in birds: synthesis and prospects. Behav Process 89:143–152
Fernández-Juricic E, Gall MD, Dolan T, O’Rourke C, Thomas S, Lynch JR (2011) Visual systems and vigilance behaviour of two ground-foraging avian prey species: white-crowned Sparrows and California Towhees. Anim Behav 81:705–713
Ferretti A, Rattenborg NC, Ruf T, McWilliams SR, Cardinale M, Fusani L (2019) Sleeping unsafely tucked to conserve energy in a nocturnal migratory songbird. Curr Biol 29:2766–2772
Fortin D, Larochelle J, Gauthier G (2000) The effect of wind, radiation and body orientation on the thermal environment of Greater Snow Goose goslings. J Therm Biol 25:227–238
Glover HK, Weston MA, Maguire GS, Miller KK, Christie BA (2011) Towards ecologically meaningful and socially acceptable buffers: response distances of shorebirds in Victoria, Australia, to human disturbance. Landsc Urban Plan 103:326–334
Goodale E, Kotagama SW, Holberton RL (2005) Alarm calling in Sri Lankan mixed-species bird flocks. Auk 122:108–120
Goss-Custard JD, Stillman RA, West AD, Caldow RWG, Triplet P, le Durrell SEA, McGrorty S (2004) When enough is not enough: shorebirds and shellfishing. Proc R Soc B 271:233–237
Griesser M, Nystrand M (2009) Vigilance and predation of a forest-living bird species depend on large-scale habitat structure. Behav Ecol 20:709–715
Guillemain M, Martin GR, Fritz H (2002) Feeding methods, visual fields and vigilance in dabbling ducks (Anatidae). Funct Ecol 16:522–529
Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22
Javůrková V, Hořák D, Kreisinger J, Klvaňa P, Albrecht T (2011) Factors affecting sleep/vigilance behaviour in incubating Mallards. Ethology 117:345–355
Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO (2012) The global diversity of birds in space and time. Nature 491:444–448
Jiang Y, Mølle AP (2017) Escape from predators and genetic variance in birds. J Evol Biol 30:2059–2067
King JR (1974) Seasonal allocation of time and energy resources in birds. In: Paynter RAJ (ed) Avian energetics. Nuttall Ornithological Club, pp 4–85
Kullberg C, Lafrenz M (2007) Escape take-off strategies in birds: the significance of protective cover. Behav Ecol Sociobiol 61:1555–1560
Landeau L, Terborgh J (1986) Oddity and the “confusion effect” in predation. Anim Behav 34:372–1380
Lazarus J (1979) The early warning function of flocking in birds: an experimental study with captive quelea. Anim Behav 27:855–865
Li C, Beauchamp G, Wang Z, Cui P (2016) Collective vigilance in the wintering hooded crane: the role of flock size and anthropogenic disturbances in a human-dominated landscape. Ethology 122:999–1008
Lima SL, Bednekoff PA (1999) Back to the basics of antipredatory vigilance: can nonvigilant animals detect attack? Anim Behav 58:537–543
Lima SL, Dill LM (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640
Lima SL, Rattenborg NC, Lesku JA, Amlaner CJ (2005) Sleeping under the risk of predation. Anim Behav 70:723–736
Lind J (2004) What determines probability of surviving predator attacks in bird migration? The relative importance of vigilance and fuel load. J Theor Biol 231:223–227
Lindström Å (1989) Finch flock size and rise of hawk predation at a migratory stopover site. Auk 106:225–232
Martin GR (1994) Visual fields in Woodcocks Scolopax rusticola (Scolopacidae; Charadriiformes). J Comp Physiol A 174:787–793
Martin GR (2007) Visual fields and their functions in birds. J Ornithol 148:547–562
Martin GR, Piersma T (2008) Vision and touch in relation to foraging and predator detection: insightful contrasts between a plover and a sandpiper. Proc R Soc B 276:437–445
Morelli F, Mikula P, Benedetti Y, Bussière R, Jerzak L, Tryjanowski P (2018) Escape behaviour of birds in urban parks and cemeteries across Europe: evidence of behavioural adaptation to human activity. Sci Total Environ 631–632:803–810
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
Navedo JG, Verdugo C, Rodrıguez-Jorquera IA, Abad-Gomez JM, Suazo CG, Casta LE, Araya V, Ruiz J, Gutierrez JS (2019) Assessing the effects of human activities on the foraging opportunities of migratory shorebirds in Austral high-latitude bays. PLoS ONE 14:e0212441
Nocera JJ, Ratcliffe LM (2010) Migrant and resident birds adjust antipredator behavior in response to social information accuracy. Behav Ecol 21:121–128
Novcic I (2020) Nearest-neighbor distances change over short time intervals in foraging flocks of shorebirds. Ornithol Sci 19:107–113
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290
Pavlovic G, Weston MA, Symonds MRE (2019) Morphology and geography predict the use of heat conservation behaviours across birds. Funct Ecol 33:286–296
Potvin DA, Ratnayake CP, Radford AN, Magrath RD (2018) Birds learn socially to recognize heterospecific alarm calls by acoustic association. Curr Biol 28:2632–2637
Provini P, Tobalske BW, Crandell KE, Abourachid A (2012) Transition from leg to wing forces during take-off in birds. J Exp Biol 215:4115–4124
Randler C, Kalb J (2020) Predator avoidance behavior of nocturnal and diurnal rodents. Behav Proc 179:104214
Roberts G (1996) Why individual vigilance declines as group size increases. Anim Behav 51:1077–1086
Rogers DI, Piersma T, Hassell CJ (2006) Roost availability may constrain shorebird distribution: exploring the energetic costs of roosting and disturbance around a tropical bay. Biol Conserv 133:225–235
Rogers D, Herrod A, Menkhorst P, Loyn R (2010) Local movements of shorebirds and high-resolution mapping of shorebird habitat in the Port Phillip Bay (Western Shoreline) and Bellarine Peninsula Ramsar site. Arthur Rylah Institute
Rose M, Nol E (2010) Foraging behavior of non-breeding Semipalamated Plovers. Waterbirds 33:59–69
Roth TC, Lima SL, Vetter WE (2006) Determinants of predation risk in small wintering birds: the hawk’s perspective. Behav Ecol Sociobiol 60:195–204
Roth TC, Cox JG, Lima ST (2008) Can foraging birds assess predation risk by scent? Anim Behav 76:2021–2027
Ryeland J, Weston MA, Symonds MRE (2017) Bill size mediates behavioural thermoregulation in birds. Funct Ecol 3:885–893
Ryeland J, Weston MA, Symonds MRE (2019) Leg length and temperature determine the use of unipedal roosting in birds. J Avian Biol 50:1–9
Ryeland J, Weston MA, Symonds MRE (2020) The importance of wetland margin microhabitat mosaics; the case of shorebirds and thermoregulation. J Appl Ecol. https://doi.org/10.1111/1365-2664.13769
Samia DSM, Nomura F, Blumstein DT (2013) Do animals generally flush early and avoid the rush? A meta-analysis. Biol Lett 9:20130016
Samia DS, Blumstein DT, Díaz M, Grim T, Ibáñez-Álamo JD, Jokimäki J, Tätte K, Markó G, Tryjanowski P, Møller AP (2017) Rural-urban differences in escape behavior of European birds across a latitudinal gradient. Front Ecol Evol 5:66
Sih A, Del Giudice M (2012) Linking behavioural syndromes and cognition: a behavioural ecology perspective. Philos Trans R Soc B 367:2762–2772
Sirot E (2006) Social information, antipredatory vigilance and flight in bird flocks. Anim Behav 72:373–382
Stankowich T, Blumstein DT (2005) Fear in animals: a meta-analysis and review of risk assessment. Proc R Soc B 272:2627–2634
Tätte K, Ibáñez-Álamo JD, Markó G, Mänd R, Møller AP (2019a) Antipredator function of vigilance re-examined: vigilant birds delay escape. Anim Behav 156:97–110
Tätte K, Ibáñez-Álamo JD, Markó G, Mänd R, Møller AP, Lima SL, Bednekoff PA, Beauchamp G, Blumstein DT, Fernández-Juricic E, Morrison EB (2019b) Sensory basis of vigilance behavior in birds: synthesis and future prospects. Anim Behav 148:389–399
Tattersall G, Cadena V (2010) Insights into animal temperature adaptations revealed through thermal imaging. Imaging Sci J 58:261–268
Tattersall G, Andrade D, Abe A (2009) Heat exchange from the toucan bill reveals a controllable vascular thermal radiator. Science 325:468–470
Tisdale V, Fernández-Juricic E (2009) Vigilance and predator detection vary between avian species with different visual acuity and coverage. Behav Ecol 20:936–945
Tyrrell LP, Fernández-Juricic E (2015) Sensory systems and escape behavior. In: CooperBlumstein WEDT (ed) Escaping from predators: an intergrative view of escape decisions. Cambridge University Press, pp 322–342
Van Den Hout P, Spaans B, Piersma T (2008) Differential mortality of wintering shorebirds on the Banc d’ Arguin, Mauritania, due to predation by large falcons. Ibis 150:219–230
Van Dongen WFD, Robinson RW, Weston MA, Mulder RA, Guay P (2015) Variation at the DRD4 locus is associated with wariness and local site selection in urban Black Swans. BMC Evol Biol 15:253
Weston MA (2019) Human disturbance. The population ecology and conservation of Charadrius Plovers. Routledge, pp 277–308
Whittingham MJ, Butler S, Quinn JL, Cresswell W (2004) The effect of limited visibility on vigilance behaviour and speed of predator detection: implications for the conservation of granivorous passerines. Oikos 106:377–385
Winter RE, Shields WM (2021) Effects of weather on foraging success and hunting frequency in winter-irruptive Snowy Owls (Bubo scandiacus) in upstate New York. J Raptor Res 55:584–593
Wolf BO, Walsberg GE (2000) The role of the plumage in heat transfer processes of birds. Am Zool 40:575–584
Ydenberg RC, Dill LM (1986) The economics of fleeing from predators. Adv Study Behav 16:229–249
Yorzinski JL, Lam J, Schultz R, Davis M (2018) Thermoregulatory postures limit antipredator responses in Peafowl. Biol Open 7:bio031005
Zharikov Y, Milton DA (2009) Valuing coastal habitats: predicting high-tide roosts of non-breeding migratory shorebirds from landscape composition. Emu 109:107–120
Zuberbühler K (2009) Survivor signals: the biology and psychology of animal alarm calling. Adv Study Behav 40:589–604
Acknowledgements
Thanks to the rangers at Point Cook Coastal Park (Ron Cuthbert, Russell Brooks, Mark Cullen and Bernie McCarrick), with a special thanks to Bernie McCarrick for his expertise and assistance. Thank you to Kevin Gillett and Heather Graham (Melbourne Water) for facilitating access to the Western Treatment Plant and to Toby Stringer (Parks Victoria) for allowing access the Avalon Coastal Park. MAW was supported by BEACH (Venus Bay).
Funding
No external funding was obtained.
Author information
Authors and Affiliations
Contributions
All authors contributed to conceptualisation, design and write up. MRES and MAW supervised the project, MRES led the analysis. AT and MAW collected data.
Corresponding author
Ethics declarations
Conflict of interest
We declare no conflict of interest.
Ethical approvals
Work was approved by the Deakin University Animal Ethics Committee (B10-2018), DEWLP (10008731) and Melbourne Water (MWCIF-4736-11314-S).
Consent for publication
All authors consent for publication.
Additional information
Communicated by A. Hedenström.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Timmis, A.D., Symonds, M.R.E. & Weston, M.A. The influence of resting posture and orientation on alertness and escape in shorebirds. J Ornithol 163, 509–521 (2022). https://doi.org/10.1007/s10336-021-01957-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10336-021-01957-y