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RESEARCH ARTICLE (Open Access)

Distress responses during handling in urban and exurban bandiny, the New Holland honeyeater (Phylidonyris novaehollandiae), in southwestern Western Australia

M. Pearmain-Fenton https://orcid.org/0000-0002-9600-1416 A B * , L. N. Gilson https://orcid.org/0000-0002-5454-2038 B , B. J. Saunders A and P. W. Bateman https://orcid.org/0000-0002-3036-5479 B
+ Author Affiliations
- Author Affiliations

A School of Molecular and Life Sciences, Curtin University, Perth, WA, Australia.

B Behavioural Ecology Laboratory, School of Molecular and Life Sciences, Curtin University, Perth, WA, Australia.


Handling Editor: Rob Davis

Pacific Conservation Biology 29(5) 419-428 https://doi.org/10.1071/PC22014
Submitted: 22 March 2022  Accepted: 12 September 2022   Published: 7 October 2022

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context: Birds appear to be better suited than mammals or reptiles to adapt to fast-changing landscapes because of their greater mobility; however, the behavioural effects of urbanisation on birds in Australia remain broadly unexplored.

Aims: This study aimed to investigate the effects of urbanisation on behavioural responses exhibited by a common and widespread meliphagid, the bandiny or New Holland honeyeater (Phylidonyris novaehollandiae) while undergoing standard bird banding processes.

Methods: Five non-invasive techniques (alarm calling, wriggling, biting, breathing rate, and tonic immobility) were explored for efficacy in identifying underlying differences in distress arising from mist-netting at urban and exurban localities in southwestern Western Australia.

Key results: Breathing rate was the most important variable for identifying differences in post-capture distress response. The breathing rate of urban bandiny following capture was lower than those of exurban areas. All other parameters proved suboptimal for detecting differential behavioural responses to handling between urban and exurban populations, despite having been successfully used in other international studies.

Conclusions: We suggest that urban honeyeaters exhibit lower mean breathing rates due to chronic overstimulation in response to urban lifestyles and are not able to further elevate this behaviour in response to stressful stimuli. The failure of other approaches explored highlights the need to apply ecosystem-appropriate methods for investigating urbanisation within an Australian context.

Implications: Our results suggest that behavioural approaches to quantifying avian stress developed internationally require additional consideration when applied to the ecosystems of Australia, whose birds are evolved to accommodate a different regime of seasonality that has shaped them behaviourally and morphologically.

Keywords: adaptive, behaviour, bird banding, distress, handling stress, Meliphagidae, passerine, urbanisation.


References

Abolins-Abols, M, Hope, SF, and Ketterson, ED (2016). Effect of acute stressor on reproductive behavior differs between urban and rural birds. Ecology and Evolution 6, 6546–6555.
Effect of acute stressor on reproductive behavior differs between urban and rural birds.Crossref | GoogleScholarGoogle Scholar |

Aharon-Rotman, Y, Buchanan, KL, Clark, NJ, Klaassen, M, and Buttemer, WA (2016). Why fly the extra mile? Using stress biomarkers to assess wintering habitat quality in migratory shorebirds. Oecologia 182, 385–395.
Why fly the extra mile? Using stress biomarkers to assess wintering habitat quality in migratory shorebirds.Crossref | GoogleScholarGoogle Scholar |

Amos, JN, Balasubramaniam, S, Grootendorst, L, Harrisson, KA, Lill, A, Mac Nally, R, Pavlova, A, Radford, JQ, Takeuchi, N, Thomson, JR, and Sunnucks, P (2013). Little evidence that condition, stress indicators, sex ratio, or homozygosity are related to landscape or habitat attributes in declining woodland birds. Journal of Avian Biology 44, 45–54.
Little evidence that condition, stress indicators, sex ratio, or homozygosity are related to landscape or habitat attributes in declining woodland birds.Crossref | GoogleScholarGoogle Scholar |

Arnold, GW, and Weeldenburg, JR (1990). Factors determining the number and species of birds in road verges in the wheatbelt of Western Australia. Biological Conservation 53, 295–315.
Factors determining the number and species of birds in road verges in the wheatbelt of Western Australia.Crossref | GoogleScholarGoogle Scholar |

Astheimer, LB, and Buttemer, WA (2002). Changes in latitude, changes in attitude: a perspective on ecophysiological studies of Australian birds. Emu - Austral Ornithology 102, 19–27.
Changes in latitude, changes in attitude: a perspective on ecophysiological studies of Australian birds.Crossref | GoogleScholarGoogle Scholar |

Atwell, JW, Cardoso, GC, Whittaker, DJ, Campbell-Nelson, S, Robertson, KW, and Ketterson, ED (2012). Boldness behavior and stress physiology in a novel urban environment suggest rapid correlated evolutionary adaptation. Behavioral Ecology 23, 960–969.
Boldness behavior and stress physiology in a novel urban environment suggest rapid correlated evolutionary adaptation.Crossref | GoogleScholarGoogle Scholar |

Australian Institute of Aboriginal and Torres Strait Islander Studies (1996) Map of Indigenous Australia. Available at https://aiatsis.gov.au/explore/map-indigenous-australia

Birdlife Australia (2021) Key biodiversity areas: nature’s hotspots. Available at https://www.keybiodiversityareas.org.au

Boissy, A (1995). Fear and fearfulness in animals. The Quarterly Review of Biology 70, 165–191.
Fear and fearfulness in animals.Crossref | GoogleScholarGoogle Scholar |

Brearley, G, Rhodes, J, Bradley, A, Baxter, G, Seabrook, L, Lunney, D, Liu, Y, and McAlpine, C (2013). Wildlife disease prevalence in human-modified landscapes. Biological Reviews 88, 427–442.
Wildlife disease prevalence in human-modified landscapes.Crossref | GoogleScholarGoogle Scholar |

Brunton C (2001) CALM Regional Parks usage survey. Department of Conservation and Land Management, Perth.

Carere, C, and van Oers, K (2004). Shy and bold great tits (Parus major): body temperature and breath rate in response to handling stress. Physiology & Behavior 82, 905–912.
Shy and bold great tits (Parus major): body temperature and breath rate in response to handling stress.Crossref | GoogleScholarGoogle Scholar |

Charmantier, A, Demeyrier, V, Lambrechts, M, Perret, S, and Grégoire, A (2017). Urbanization is associated with divergence in pace-of-life in great tits. Frontiers in Ecology and Evolution 5, 53.
Urbanization is associated with divergence in pace-of-life in great tits.Crossref | GoogleScholarGoogle Scholar |

Cleary, GP, Parsons, H, Davis, A, Coleman, BR, Jones, DN, Miller, KK, and Weston, MA (2016). Avian assemblages at bird baths: a comparison of urban and rural bird baths in Australia. PLoS ONE 11, e0150899.
Avian assemblages at bird baths: a comparison of urban and rural bird baths in Australia.Crossref | GoogleScholarGoogle Scholar |

Conover MR (1994) How birds interpret distress calls: implications for applied uses of distress call playbacks. Proceedings of the Vertebrate Pest Conference 16, 232–234.

Crino, OL, Buchanan, KL, Trompf, L, Mainwaring, MC, and Griffith, SC (2017). Stress reactivity, condition, and foraging behavior in zebra finches: effects on boldness, exploration, and sociality. General and Comparative Endocrinology 244, 101–107.
Stress reactivity, condition, and foraging behavior in zebra finches: effects on boldness, exploration, and sociality.Crossref | GoogleScholarGoogle Scholar |

Davies, S, and Sewall, KB (2016). Correction to ‘Agonistic urban birds: elevated territorial aggression of urban song sparrows is individually consistent within a breeding period’. Biology Letters 12, 20160900.
Correction to ‘Agonistic urban birds: elevated territorial aggression of urban song sparrows is individually consistent within a breeding period’.Crossref | GoogleScholarGoogle Scholar |

Davis, RA, and Wilcox, JA (2013). Adapting to suburbia: bird ecology on an urban-bushland interface in Perth, Western Australia. Pacific Conservation Biology 19, 110–120.
Adapting to suburbia: bird ecology on an urban-bushland interface in Perth, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Davis, RA, Gole, C, and Roberts, JD (2013). Impacts of urbanisation on the native avifauna of Perth, Western Australia. Urban Ecosystems 16, 427–452.
Impacts of urbanisation on the native avifauna of Perth, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Demeyrier, V, Lambrechts, MM, Perret, P, and Grégoire, A (2016). Experimental demonstration of an ecological trap for a wild bird in a human-transformed environment. Animal Behaviour 118, 181–190.
Experimental demonstration of an ecological trap for a wild bird in a human-transformed environment.Crossref | GoogleScholarGoogle Scholar |

Department of Planning and Urban Development, Western Australia (1993) The natural resources of the Darling Ranges. Darling Range Regional Park supplementary report, no. 2. Department of Planning and Urban Development, Western Australia, Perth, WA.

Ducatez, S, Audet, J-N, Rodriguez, JR, Kayello, L, and Lefebvre, L (2017). Innovativeness and the effects of urbanization on risk-taking behaviors in wild Barbados birds. Animal Cognition 20, 33–42.
Innovativeness and the effects of urbanization on risk-taking behaviors in wild Barbados birds.Crossref | GoogleScholarGoogle Scholar |

Evans, KL, Gaston, KJ, Frantz, AC, and Simeoni, M (2009). Independent colonization of multiple urban centres by a formerly forest specialist bird species. Proceedings of the Royal Society B: Biological Sciences 276, 2403–2410.
Independent colonization of multiple urban centres by a formerly forest specialist bird species.Crossref | GoogleScholarGoogle Scholar |

Flores, R, Penna, M, Wingfield, JC, Cuevas, E, Vásquez, RA, and Quirici, V (2019). Effects of traffic noise exposure on corticosterone, glutathione and tonic immobility in chicks of a precocial bird. Conservation Physiology 7, coz061.
Effects of traffic noise exposure on corticosterone, glutathione and tonic immobility in chicks of a precocial bird.Crossref | GoogleScholarGoogle Scholar |

Gentilli J, Bekle H (1993) ‘History of the Perth Lakes. Vol. 10.’ (Royal Western Australian Historical Society)

Griffith, SC, Ton, R, Hurley, LL, McDiarmid, CS, and Pacheco-Fuentes, H (2021). The ecology of the Zebra Finch makes it a great laboratory model but an outlier amongst passerine birds. Birds 2, 60–76.
The ecology of the Zebra Finch makes it a great laboratory model but an outlier amongst passerine birds.Crossref | GoogleScholarGoogle Scholar |

Hazard, D, Couty, M, Richard, S, and Guémené, D (2008). Intensity and duration of corticosterone response to stressful situations in Japanese quail divergently selected for tonic immobility. General and Comparative Endocrinology 155, 288–297.
Intensity and duration of corticosterone response to stressful situations in Japanese quail divergently selected for tonic immobility.Crossref | GoogleScholarGoogle Scholar |

Higgins P, Peter JM, Steele WK (2001) ‘Handbook of Australia, New Zealand and Antarctic birds: tyrant-flycatchers to chats. Vol. 5.’ 2nd edn. (Oxford University Press Australia & New Zealand: Melbourne)

Hollander, FA, Van Overveld, T, Tokka, I, and Matthysen, E (2008). Personality and nest defence in the great tit (Parus major). Ethology 114, 405–412.
Personality and nest defence in the great tit (Parus major).Crossref | GoogleScholarGoogle Scholar |

Keast, A (1968). Seasonal movements in the Australian honeyeaters (Meliphagidae) and their ecological significance. Emu - Austral Ornithology 67, 159–209.
Seasonal movements in the Australian honeyeaters (Meliphagidae) and their ecological significance.Crossref | GoogleScholarGoogle Scholar |

Kinnear, A, and Garnett, P (1999). Water chemistry of the wetlands of the Yellagonga Regional Park, Western Australia. Journal of the Royal Society of Western Australia 82, 79–87.

Klesch M, Spehn-Jackson L (2014) ‘Djerap: Noongar birds.’ (Batchelor Institute Press: Perth, WA)

Lowe KW (1989) ‘The Australian bird bander’s manual’. (CPP Communications Ltd).

Luck GW, Smallbone LT (2010) Chapter 5: Species diversity and urbanisation: patterns, drivers and implications. In ‘Urban ecology’. (Ed. KJ Gaston) pp. 88–119. (Cambridge University Press: Cambridge)

McFarland, DC (1994). Responses of territorial New Holland honeyeaters Phylidonyris novaehollandiae to short-term fluctuations in nectar productivity. Emu - Austral Ornithology 94, 193–200.
Responses of territorial New Holland honeyeaters Phylidonyris novaehollandiae to short-term fluctuations in nectar productivity.Crossref | GoogleScholarGoogle Scholar |

McFarland, DC (1996). Aggression and nectar use in territorial non-breeding New Holland honeyeaters Phylidonyris novaehollandiae in eastern Australia. Emu - Austral Ornithology 96, 181–188.
Aggression and nectar use in territorial non-breeding New Holland honeyeaters Phylidonyris novaehollandiae in eastern Australia.Crossref | GoogleScholarGoogle Scholar |

McFarland, DC (2002). Non-breeding territoriality in the New Holland honeyeater, Phylidonyris novaehollandiae, in an unpredictable environment—short-term energy costs for possible long-term reproductive benefits. Emu - Austral Ornithology 102, 315–321.
Non-breeding territoriality in the New Holland honeyeater, Phylidonyris novaehollandiae, in an unpredictable environment—short-term energy costs for possible long-term reproductive benefits.Crossref | GoogleScholarGoogle Scholar |

McGiffin, A, Lill, A, Beckman, J, and Johnstone, CP (2013). Tolerance of human approaches by Common Mynas along an urban-rural gradient. Emu - Austral Ornithology 113, 154–160.
Tolerance of human approaches by Common Mynas along an urban-rural gradient.Crossref | GoogleScholarGoogle Scholar |

Mills, AD, and Faure, J-M (1991). Divergent selection for duration of tonic immobility and social reinstatement behavior in Japanese quail (Coturnix coturnix japonica) chicks. Journal of Comparative Psychology 105, 25–38.
Divergent selection for duration of tonic immobility and social reinstatement behavior in Japanese quail (Coturnix coturnix japonica) chicks.Crossref | GoogleScholarGoogle Scholar |

Møller, AP (2009). Successful city dwellers: a comparative study of the ecological characteristics of urban birds in the Western Palearctic. Oecologia 159, 849–858.
Successful city dwellers: a comparative study of the ecological characteristics of urban birds in the Western Palearctic.Crossref | GoogleScholarGoogle Scholar |

Møller, AP, and Ibáñez-Álamo, JD (2012). Escape behaviour of birds provides evidence of predation being involved in urbanization. Animal Behaviour 84, 341–348.
Escape behaviour of birds provides evidence of predation being involved in urbanization.Crossref | GoogleScholarGoogle Scholar |

Myers, S, Brown, G, and Kleindorfer, S (2010). Divergence in New Holland honeyeaters (Phylidonyris novaehollandiae): evidence from morphology and feeding behavior. Journal of Ornithology 151, 287–296.
Divergence in New Holland honeyeaters (Phylidonyris novaehollandiae): evidence from morphology and feeding behavior.Crossref | GoogleScholarGoogle Scholar |

Preiszner, B, Papp, S, Pipoly, I, Seress, G, Vincze, E, Liker, A, and Bókony, V (2017). Problem-solving performance and reproductive success of great tits in urban and forest habitats. Animal Cognition 20, 53–63.
Problem-solving performance and reproductive success of great tits in urban and forest habitats.Crossref | GoogleScholarGoogle Scholar |

R Core Team (2021) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna) Available at https://www.rstudio.com/products/rstudio/

Recher, HF, Calver, MC, and Davis, WE (2016). Ecology of honeyeaters (Meliphagidae) in Western Australian Eucalypt Woodlands I: resource allocation among species in the Great Western Woodland during spring. Australian Zoologist 38, 130–146.
Ecology of honeyeaters (Meliphagidae) in Western Australian Eucalypt Woodlands I: resource allocation among species in the Great Western Woodland during spring.Crossref | GoogleScholarGoogle Scholar |

Sandström, UG, Angelstam, P, and Mikusiński, G (2006). Ecological diversity of birds in relation to the structure of urban green space. Landscape and Urban Planning 77, 39–53.
Ecological diversity of birds in relation to the structure of urban green space.Crossref | GoogleScholarGoogle Scholar |

Saunders, DA (1989). Changes in the Avifauna of a region, district and remnant as a result of fragmentation of native vegetation: the wheatbelt of western Australia. A case study. Biological Conservation 50, 99––135.

Serrano-Davies, E, O’Shea, W, and Quinn, JL (2017). Individual foraging preferences are linked to innovativeness and personality in the great tit. Behavioral Ecology and Sociobiology 71, 161.
Individual foraging preferences are linked to innovativeness and personality in the great tit.Crossref | GoogleScholarGoogle Scholar |

Smith H, McCracken J, Shepherd D, Velez P (1997) ‘The mist netter’s bird safety handbook.’ (The Institute for Bird Populations)

Sol, D, Bartomeus, I, and Griffin, AS (2012). The paradox of invasion in birds: competitive superiority or ecological opportunism? Oecologia 169, 553––564.

South-west Aboriginal Land and Sea Council (2021) Six seasons - Nyungar life on the Coastal Plain. Available at https://www.derbalnara.org.au/boodjar-six-seasons

Starkey, EE, and Starkey, JF (1973). Description of an aerial predator alarm call for mallard (Anas platyrhynchos) ducklings. The Condor 75, 364–366.
Description of an aerial predator alarm call for mallard (Anas platyrhynchos) ducklings.Crossref | GoogleScholarGoogle Scholar |

Stefanski, RA, and Falls, JB (1972). A study of distress calls of song, swamp, and white-throated sparrows (Aves: Fringillidae). I. Intraspecific responses and functions. Canadian Journal of Zoology 50, 1501–1512.
A study of distress calls of song, swamp, and white-throated sparrows (Aves: Fringillidae). I. Intraspecific responses and functions.Crossref | GoogleScholarGoogle Scholar |

Torné-Noguera, A, Pagani-Núñez, E, and Senar, JC (2014). Great tit (Parus major) breath rate in response to handling stress: urban and forest birds differ. Journal of Ornithology 155, 315–318.
Great tit (Parus major) breath rate in response to handling stress: urban and forest birds differ.Crossref | GoogleScholarGoogle Scholar |

Tsurim, I, Abramsky, Z, and Kotler, BP (2008). Foraging behavior of urban birds: are human commensals less sensitive to predation risk than their nonurban counterparts? The Condor 110, 772–776.
Foraging behavior of urban birds: are human commensals less sensitive to predation risk than their nonurban counterparts?Crossref | GoogleScholarGoogle Scholar |

Wang, S, Ni, Y, Guo, F, Fu, W, Grossmann, R, and Zhao, R (2013). Effect of corticosterone on growth and welfare of broiler chickens showing long or short tonic immobility. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 164, 537–543.
Effect of corticosterone on growth and welfare of broiler chickens showing long or short tonic immobility.Crossref | GoogleScholarGoogle Scholar |

Western Australian Planning Commission (2017) Whiteman Park strategic plan 2017–2021. Western Australian Planning Commission.

Yates, CJ, Coates, DJ, Elliott, C, and Byrne, M (2007). Composition of the pollinator community, pollination and the mating system for a shrub in fragments of species rich kwongan in south-west Western Australia. Biodiversity and Conservation 16, 1379–1395.
Composition of the pollinator community, pollination and the mating system for a shrub in fragments of species rich kwongan in south-west Western Australia.Crossref | GoogleScholarGoogle Scholar |

Zuur AF, Ieno EN, Smith GM (2007) Chapter 7: Additive and generalised additive modelling. In ‘Analysing ecological data. Statistics for biology and health’. (Eds AF Zuur, EN Ieno, GM Smith) pp. 97–124. (Springer, New York, NY)