Assessing avian incubation behavior in response to environmental pollution with temperature-humidity loggers
DOI:
https://doi.org/10.51812/of.144957Keywords:
air pollution, female behavior, incubation rhythm, temperature-humidity logger, Ficedula hypoleucaAbstract
The negative impact of environmental pollution on avian physiology and breeding success is well documented. However, pollution-related behavioral changes during reproduction remain underexplored, despite behavior often being one of the earliest indicators of environmental disturbances and having significant life-history consequences. For example, altered food availability in a polluted environment could potentially perturb the incubation behavior of income breeders. These birds typically alternate between staying in the nest and heating eggs (on-bout) and taking foraging trips (off-bout). In this two-year study (2020 and 2022), we investigated how the incubation behavior of an insectivorous passerine, the pied flycatcher (Ficedula hypoleuca), varied with environmental pollution levels around a Cu-Ni smelter. Additionally, we compared two different metrics – temperature and humidity within the nest – to evaluate their use as indicators of incubation rhythm. We found that temperature- and humidity-based incubation rhythm parameters correlated, but those based on humidity matched better the true incubation behavior documented by simultaneous video recording. This was because the humidity curve showed a more immediate and intensive response to the female's incubation behavior. Birds in the polluted area took slightly more (11%) but shorter (11%) off-bouts, possibly reflecting smaller energetic constraints or better food availability in the polluted area. However, we found no difference in total incubation intensity between polluted and control areas, with F. hypoleuca females incubating their eggs 75% of the daytime in both environments. Hence, incubating females in the polluted area did not allocate more time for gathering their energy reserves than the birds in the control area, and there was also no difference in the hatching success. Our study is the first to use humidity variation to record incubation rhythm, and our results indicate that measuring humidity inside the nest is a promising technique to test and develop further. For example, further studies are needed to test if this method would work in different types of nests. From an environmental protection standpoint, our results also contribute valuable insights to the relatively limited information on pollution-related behavioral changes.
References
Amininasab, S. M., Birker, M., Kingma, S. A., Hildenbrandt, H. & Komdeur, J. 2017. The effect of male incubation feeding on female nest attendance and reproductive performance in a socially monogamous bird. — Journal of Ornithology 158: 687–696. https://doi.org/10.1007/s10336-016-1427-2
Ar, A. & Rahn, H. 1980. Water in the Avian Egg: Overall Budget of Incubation. — American Zoologist 20: 373–384. https://doi.org/10.1093/icb/20.2.373
Arct, A., Drobniak, S. M., Dubiec, A., Martyka, R., Sudyka, J., Gustafsson, L. & Cichoń, M. 2022. The interactive effect of ambient temperature and brood size manipulation on nestling body mass in blue tits: an exploratory analysis of a long-term study. — Frontiers in Zoology 19: 9. https://doi.org/10.1186/s12983-022-00456-x
Belskii, E. & Belskaya, E. 2013. Diet composition as a cause of different contaminant exposure in two sympatric
passerines in the Middle Urals, Russia. — Ecotoxicology and Environmental Safety 97: 67–72. https://doi.org/10.1016/j.ecoenv.2013.07.014
Belskii, E. A., Bezel, V. S. & Polents, E. A. 1995. Early stages of the nesting period of hollow-nesting birds under conditions of industrial pollution. — Russian Journal of Ecology 26: 38–43.
Berglund, Å. M. M., Koivula, M. J. & Eeva, T. 2011. Species- and age-related variation in metal exposure and accumulation of two passerine bird species. — Environmental Pollution 159: 2368–2374. https://doi.org/10.1016/j.envpol.2011.07.001
Biddle, L. E., Dickinson, A. M., Broughton, R. E., Gray, L. A., Bennett, S. L., Goodman, A. M. & Deeming, D. C. 2019. Construction materials affect the hydrological properties of bird nests. — Journal of Zoology 309: 161–171. https://doi.org/10.1111/jzo.12713
Boulton, R. L. & Cassey, P. 2012. How avian incubation behaviour influences egg surface temperatures: relationships with egg position, development and clutch size. — Journal of Avian Biology 43: 289–296. https://doi.org/10.1111/j.1600-048X.2012.05657.x
Bryan, S. M. & Bryant, D. M. 1999. Heating nest-boxes reveals an energetic constraint on incubation behaviour in great tits, Parus major. — Proceedings of the Royal Society of London Series B — Biological Sciences 266: 157–162. https://doi.org/10.1098/rspb.1999.0616
Bueno-Enciso, J., Barrientos, R. & Jose Sanz, J. 2017. Incubation behaviour of Blue Cyanistes caeruleus and Great Tits Parus major in a Mediterranean habitat. — Acta Ornithologica 52: 21–34. https://doi.org/10.3161/00016454AO2017.52.1.003
Burnham, K. P., Anderson, D. R. & Huyvaert, K. P. 2011. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. — Behavioral Ecology and Sociobiology 65: 23–35. https://doi.org/10.1007/s00265-010-1029-6
Camfield, A. F. & Martin, K. 2009. The influence of ambient temperature on horned lark incubation behaviour in an alpine environment. — Behaviour 146: 1615–1633. http://dx.doi.org/10.1163/156853909X463335
Cantarero, A., López-Arrabé, J., Palma, A., Redondo, A. J. & Moreno, J. 2014. Males respond to female begging signals of need: a handicapping experiment in the pied flycatcher, Ficedula hypoleuca. — Animal Behaviour 94: 167–173. https://doi.org/10.1016/j.anbehav.2014.05.002
Cauchard, L., Macqueen, E. I., Lilley, R., Bize, P. & Doligez, B. 2021. Inter-individual variation in provisioning rate, prey size and number, and links to total prey biomass delivered to nestlings in the Collared Flycatcher (Ficedula albicollis). — Avian Research 12: 15. https://doi.org/10.1186/s40657-021-00247-8
Çelik, E., Durmus, A., Adizel, O. & Nergiz Uyar, H. 2021. A bibliometric analysis: what do we know about metals(loids) accumulation in wild birds? — Environmental Science and Pollution Research 28: 10302–10334. https://doi.org/10.1007/s11356-021-12344-8
Conway, C. & Martin, T. E. 2000. Effects of ambient temperature on avian incubation behavior. — Behavioral Ecology 11: 178–188. https://doi.org/10.1093/beheco/11.2.178
Cooper, C. B. & Voss, M. A. 2013. Avian Incubation Patterns Reflect Temporal Changes in Developing Clutches. — PLOS ONE 8: e65521. https://doi.org/10.1371/journal.pone.0065521
Cramp, S. 1988. The Birds of the Western Palearctic V — Tyrant Flycatchers to Thrushes. — Oxford University Press.
Dawson, W. R. 1982. Evaporative losses of water by birds. — Comparative Biochemistry and Physiology Part A: Physiology 71: 495–509. https://doi.org/10.1016/0300-9629(82)90198-0
Deeming, D. C. 2002. Avian Incubation: Behaviour, Environment and Evolution. — Oxford University Press.
DuRant, S. E., Hopkins, W. A., Hepp, G. R. & Walters, J. R. 2013. Ecological, evolutionary, and conservation implications of incubation temperature-dependent phenotypes in birds. — Biological Reviews of the Cambridge Philosophical Society 88: 499–509. https://doi.org/10.1111/brv.12015
Eeva, T. & Lehikoinen, E. 1995. Egg shell quality, clutch size and hatching success of the great tit (Parus major) and the pied flycatcher (Ficedula hypoleuca) in an air pollution gradient. — Oecologia 102: 312–323. https://doi.org/10.1007/bf00329798
Eeva, T. & Lehikoinen, E. 1996. Growth and mortality of nestling great tits (Parus major) and pied flycatchers (Ficedula hypoleuca) in a heavy metal pollution gradient. — Oecologia 108: 631–639. https://doi.org/10.1007/bf00329036
Eeva, T. & Lehikoinen, E. 2004. Rich calcium availability diminishes heavy metal toxicity in Pied Flycatcher. — Functional Ecology 18: 548–553. https://doi.org/10.1111/j.0269-8463.2004.00875.x
Eeva, T. & Lehikoinen, E. 2010. Polluted environment and cold weather induce laying gaps in great tit and pied flycatcher. — Oecologia 162: 533–539. https://doi.org/10.1007/s00442-009-1468-9
Eeva, T. & Lehikoinen, E. 2015. Long-term recovery of clutch size and egg shell quality of the pied flycatcher (Ficedula hypoleuca) in a metal polluted area. — Environmental Pollution 201: 26–33. https://doi.org/10.1016/j.envpol.2015.02.027
Eeva, T., Lehikoinen, E. & Pohjalainen, T. 1997. Pollution-related variation in food supply and breeding success in two hole-nesting passerines. — Ecology 78: 1120–1131. https://doi.org/10.1890/0012-9658(1997)078[1120:PRVIFS]2.0.CO;2
Eeva, T., Ryömä, M. & Riihimäki, J. 2005. Pollution-related changes in diets of two insectivorous passerines. — Oecologia 145: 629–639. https://doi.org/10.1007/s00442-005-0145-x
Eeva, T., Espín, S., Ruiz, S., Sánchez-Virosta, P. & Rainio, M. 2018. Polluted environment does not speed up age-related change in reproductive performance of the pied flycatcher. — Journal of Ornithology 159: 173–182. http://dx.doi.org/10.1007/s10336-017-1487-y
Eeva, T., Espín, S., Sánchez-Virosta, P. & Rainio, M. 2020. Weather effects on breeding parameters of two insectivorous passerines in a polluted area. — Science of the Total Environment 729: 138913. https://doi.org/10.1016/j.scitotenv.2020.138913
Ekman, J. B. & Hake, M. K. 1990. Monitoring starvation risk: adjustments of body reserves in greenfinches (Carduelis chloris L.) during periods of unpredictable foraging success. — Behavioral Ecology 1: 62–67. https://doi.org/10.1093/beheco/1.1.62
Espín, S., Ruiz, S., Sánchez-Virosta, P. & Eeva, T. 2016. Effects of calcium supplementation on growth and biochemistry in two passerine species breeding in a Ca-poor and metal-polluted area. — Environmental Science and Pollution Research 23: 9809–9821. https://doi.org/10.1007/s11356-016-6219-y
Espín, S., Ruiz, S., Sánchez-Virosta, P., Lilley, T. & Eeva, T. 2017. Oxidative status in relation to metal pollution and calcium availability in pied flycatcher nestlings — A calcium manipulation experiment. — Environmental Pollution 229: 448–458. https://doi.org/10.1016/j.envpol.2017.05.094
Furness, R. W. & Greenwood, J. J. D. 1993. Birds as Monitors of Environmental Change. — Chapman & Hall.
Glądalski, M., Mainwaring, M. C., Bańbura, M., Kaliński, A., Markowski, M., Skwarska, J., Wawrzyniak, J., Bańbura, J. & Hartley, I. R. 2020. Consequences of hatching deviations for breeding success: a long-term study on blue tits Cyanistes caeruleus. — The European Zoological Journal 87: 385–394. https://doi.org/10.1080/24750263.2020.1787532
Hawkins, W. D. & DuRant, S. E. 2020. Applications of machine learning in behavioral ecology: Quantifying avian incubation behavior and nest conditions in relation to environmental temperature. — PLOS ONE 15: e0236925. https://doi.org/10.1371/journal.pone.0236925
Heppner, J. J. & Ouyang, J. Q. 2021. Incubation Behavior Differences in urban and rural house wrens, Troglodytes aedon. — Frontiers in Ecology and Evolution 9: 59069. https://doi.org/10.3389/fevo.2021.590069
Hope, S. F., Hopkins, W. A. & Angelier, F. 2022. Parenting in the city: effects of urbanization on incubation behaviour and egg temperature in great tits, Parus major. — Animal behaviour 194: 1–11. https://doi.org/10.1016/j.anbehav.2022.09.004
Hu, Q., Wang, Y., Yu, G., Lv, L., Wang, P., Wen, Y., Xu, J., Wang, Y., Zhang, Z. & Li, J. 2024. The effect of ambient temperature on bird embryonic development: a comparison between uniparental incubating silver-throated tits and biparental incubating black-throated tits. — Journal of Avian Biology: e03168. https://doi.org/10.1111/jav.03168
Ilmonen, P., Taarna, T. & Hasselquist, D. 2002. Are incubation costs in female pied flycatchers expressed in humoral immune responsiveness or breeding success? — Oecologia 130: 199–204. https://doi.org/10.1007/s004420100804
Joyce, E. M., Sillett, T. S. & Holmes, R. T. 2001. An inexpensive method for quantifying incubation patterns of open-cup nesting birds, with data for black-throated blue warblers. — Journal of Field Ornithology 72: 369–379. https://doi.org/10.1648/0273-8570-72.3.369
Kiikkilä, O. 2003. Heavy-metal pollution and remediation of forest soil around the Harjavalta Cu-Ni smelter, in SW Finland. — Silva Fennica 37: 399–415. https://doi.org/10.14214/sf.497
Koski, T.-M., Sirkiä, P. M., McFarlane, S. E., Alund, M. & Qvarnström, A. 2020. Differences in incubation behaviour and niche separation of two competing flycatcher species. — Behavioral Ecology and Sociobiology 74: 105. https://doi.org/10.1007/s00265-020-02883-4
Lambrechts, M. M., Adriaensen, F., Ardia, D. R., Artemyev, A. V., Ziane, N., et al. 2010. The design of artificial nestboxes for the study of secondary hole-nesting birds: a review of methodological inconsistencies and potential biases. — Acta Ornithologica 45: 1–26. https://doi.org/10.3161/000164510X516047
Lifjeld, J. T. & Slagsvold, T. 1986. The function of courtship feeding during incubation in the pied flycatcher Ficedula hypoleuca. — Animal Behaviour 34: 1441–1453. https://doi.org/10.1016/S0003-3472(86)80215-9
Lima, S. L. 1986. Predation risk and unpredictable feeding conditions: determinants of body mass in birds. — Ecology 67: 377–385. https://doi.org/10.2307/1938580
Lundberg, A. & Alatalo, R. V. 1992. The Pied Flycatcher. — T & A D Poyser.
Ma, L., Liu, Y., Lu, W., Zhang, Z., Li, W., Zhang, Z., Zhang, X., Zhu, C., Bai, J., Xu, Z., Han, Y. & Ruan, L. 2023. A highly effective incubation strategy enhanced the urban bird hatch success. — Avian Research 14: 100074. https://doi.org/10.1016/j.avrs.2022.100074
Mari, L., Šulc, M., Szala, K., Troscianko, J., Eeva, T. & Ruuskanen, S. 2024. Heavy metal pollution exposure affects egg coloration but not male provisioning effort in the pied flycatcher Ficedula hypoleuca. — Journal of Avian Biology: e03283. https://doi.org/10.1111/jav.03283
Maxim Integrated Products 2020. iButton Devices. https://www.maximintegrated.com/en/products/ibutton-one-wire/ibutton.html. Web site visited: 18.11.2022.
Morrison, M. L. 1986. Bird populations as indicators of environmental change. — Current Ornithology 3: 429–451. https://doi.org/10.1007/978-1-4615-6784-4_10
Nord, A., Sandell, M. I. & Nilsson, J.-Å. 2010. Female zebra finches compromise clutch temperature in energetically demanding incubation conditions. — Functional Ecology 24: 1031–1036. https://doi.org/10.1111/j.1365-2435.
01719.x
Price, M. 2008. The impact of human disturbance on birds: a selective review. — Australian Zoologist 34: 163–179. http://dx.doi.org/10.7882/FS.2008.023
Rainio, M., Ruuskanen, S. & Eeva, T. 2017. Spatio-temporal variation in the body condition of female pied flycatcher (Ficedula hypoleuca) in a polluted environment. — Urban Ecosystems 20: 1035–1043. https://doi.org/ 10.1007/s11252-017-0657-2
Sanderfoot, O. V. & Holloway, T. 2017. Air pollution impacts on avian species via inhalation exposure and associated outcomes. — Environmental Research Letters 12: 083002. https://doi.org/10.1088/1748-9326/aa8051
SAS Institute Inc. 2013. Base SAS 9.4 Procedures Guide: Statistical Procedures.
Schöll, E. M., Aparisi, M. P. & Hille, S. M. 2020. Diurnal patterns of ambient temperature but not precipitation influence incubation behavior in Great Tits. — Journal of Ornithology 161: 529–538. https://doi.org/10.1007/s10336-019-01737-9
Smith, J. A., Cooper, C. B. & Reynolds, S. J. 2015. Advances in techniques to study incubation. — In Nests, Eggs, and Incubation: New ideas about avian reproduction (ed. Deeming D.C, & S. Reynolds, J.): 179–195. Oxford University Press.
Svensson, L. 1992. Identification Guide to European Passerines. — Fingraf AB.
Tieleman, B. I., Williams, J. B. & Ricklefs, R. E. 2004. Nest attentiveness and egg temperature do not explain the variation in incubation periods in tropical birds. — Functional Ecology 18: 571–577. https://doi.org/10.1111/j.0269-8463.2004.00882.x
Vincze, E., Papp, S., Preiszner, B., Seress, G., Bókony, V. & Liker, A. 2016. Habituation to human disturbance is faster in urban than rural house sparrows. — Behavioral Ecology 27: 1304–1313. https://doi.org/10.1093/beheco/arw047
Vincze, E., Bókony, V., Garamszegi, L. Z., Seress, G., Pipoly, I., Sinkovics, C., Sándor, K. & Liker, A. 2021. Consistency and plasticity of risk-taking behaviour towards humans at the nest in urban and forest great tits, Parus major. — Animal Behaviour 179: 161–172. https://doi.org/10.1016/j.anbehav.2021.06.032
von Haartman, L. 1958. The incubation rhythm of the female Pied Flycatcher (Ficedula hypoleuca) in the presence and absence of the male. — Ornis Fennica 35: 71–76.
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