Volume 13 Issue 1
Mar.  2022
Turn off MathJax
Article Contents
Yanyan Zhao, Emilio Pagani-Núñez, Yu Liu, Xiaoying Xing, Zhiqiang Zhang, Guangji Pan, Luting Song, Xiang Li, Zhuoya Zhou, Yanqiu Chen, Donglai Li, Yang Liu, Rebecca J. Safran. 2022: The effect of urbanization and exposure to multiple environmental factors on life-history traits and breeding success of Barn Swallows (Hirundo rustica) across China. Avian Research, 13(1): 100048. doi: 10.1016/j.avrs.2022.100048
Citation: Yanyan Zhao, Emilio Pagani-Núñez, Yu Liu, Xiaoying Xing, Zhiqiang Zhang, Guangji Pan, Luting Song, Xiang Li, Zhuoya Zhou, Yanqiu Chen, Donglai Li, Yang Liu, Rebecca J. Safran. 2022: The effect of urbanization and exposure to multiple environmental factors on life-history traits and breeding success of Barn Swallows (Hirundo rustica) across China. Avian Research, 13(1): 100048. doi: 10.1016/j.avrs.2022.100048

The effect of urbanization and exposure to multiple environmental factors on life-history traits and breeding success of Barn Swallows (Hirundo rustica) across China

doi: 10.1016/j.avrs.2022.100048
More Information
  • Corresponding author: E-mail address: emilio.pnunez@xjtlu.edu.cn (E. Pagani-Núñez)
  • Received Date: 10 Mar 2022
  • Accepted Date: 27 Jun 2022
  • Rev Recd Date: 27 Jun 2022
  • Available Online: 11 Oct 2022
  • Publish Date: 31 Jul 2022
  • In addition to landscape changes, urbanization also brings about changes in environmental factors that can affect wildlife. Despite the common referral in the published literature to multiple environmental factors such as light and noise pollution, there is a gap in knowledge about their combined impact. We developed a multidimensional environmental framework to assess the effect of urbanization and multiple environmental factors (light, noise, and temperature) on life-history traits and breeding success of Barn Swallows (Hirundo rustica) across rural to urban gradients in four locations spanning over 2500 ​km from North to South China. Over a single breeding season, we measured these environmental factors nearby nests and quantified landscape urbanization over a 1 ​km2 radius. We then analysed the relationships between these multiple environmental factors through a principal component analysis and conducted spatially explicit linear-mixed effects models to assess their effect on life-history traits and breeding success. We were particularly interested in understanding whether and how Barn Swallows were able to adapt to such environmental conditions associated with urbanization. The results show that there is significant variation in the exposure to environmental conditions experienced by Barn Swallows breeding across urbanization gradients in China. These changes and their effects are complex due to the behavioural responses ameliorating potential negative effects by selecting nesting sites that minimize exposure to environmental factors. However, significant relationships between landscape urbanization, exposure to environmental factors, and life-history traits such as laying date and clutch size were pervasive. Still, the impact on breeding success was, at least in our sample, negligible, suggesting that Barn Swallows are extremely adaptable to a wide range of environmental features.

     

  • 1 These authors contributed equally to the paper.
  • loading
  • Ambrosini, R., Saino, N., 2010. Environmental effects at two nested spatial scales on habitat choice and breeding performance of barn swallow. Evol. Ecol. 24, 491-508. doi: 10.1007/s10682-009-9321-5
    Ambrosini, R., Ferrari, R.P., Martinelli, R., Romano, M., Saino, N., 2006. Seasonal, meteorological, and microhabitat effects on breeding success and offspring phenotype in the barn swallow, Hirundo rustica. Ecoscience 13, 298-307. doi: 10.2980/i1195-6860-13-3-298.1
    Badgley, C., Fox, D.L., 2000. Ecological biogeography of North American mammals: species density and ecological structure in relation to environmental gradients. J. Biogeogr. 27, 1437-1467. doi: 10.1046/j.1365-2699.2000.00498.x
    Barber, J.R., Crooks, K.R., Fristrup, K.M., 2010. The costs of chronic noise exposure for terrestrial organisms. Trends Ecol. Evol. 25, 180-189. doi: 10.1016/j.tree.2009.08.002
    Barton, K., 2022. MuMIn: multi-model inference. R package, version 1.46.0. http://r-forge.r-project.org/projects/ mumin/.
    Both, C., Artemyev, A.V., Blaauw, B., Cowie, R.J., Dekhuijzen, A.J., Eeva, T., et al., 2004. Large-scale geographical variation confirms that climate change causes birds to lay earlier. Proc R. Soc. B-Biol Sci. 271, 1657-1662. doi: 10.1098/rspb.2004.2770
    Brans, K.I., Govaert, L., Engelen, J.M.T., Gianuca, A.T., Souffreau, C., De Meester, L., 2017. Eco-evolutionary dynamics in urbanized landscapes: evolution, species sorting and the change in zooplankton body size along urbanization gradients. Philos. Trans. R. Soc. B-Biol Sci. 372, 20160030. doi: 10.1098/rstb.2016.0030
    Caizergues, A.E., Gregoire, A., Charmantier, A., 2018. Urban versus forest ecotypes are not explained by divergent reproductive selection. Proc. R. Soc. B-Biol Sci. 285, 20180261. doi: 10.1098/rspb.2018.0261
    Casasole, G., Raap, T., Costantini, D., AbdElgawad, H., Asard, H., Pinxten, R., et al., 2017. Neither artificial light at night, anthropogenic noise nor distance from roads are associated with oxidative status of nestlings in an urban population of songbirds. Comp. Biochem. Physiol. Integr Physiol. 210, 14-21. doi: 10.1016/j.cbpa.2017.05.003
    Chamberlain, D.E., Cannon, A.R., Toms, M.P., Leech, D.I., Hatchwell, B.J., Gaston, K.J., 2009. Avian productivity in urban landscapes: a review and meta-analysis. Ibis 151, 1-18. doi: 10.1111/j.1474-919X.2008.00899.x
    Ciach, M., Fröhlich, A., 2017. Habitat type, food resources, noise and light pollution explain the species composition, abundance and stability of a winter bird assemblage in an urban environment. Urban Ecosyst. 20, 547-559. doi: 10.1007/s11252-016-0613-6
    Cirelli, C., Tononi, G., 2008. Is sleep essential? PLoS Biol. 6, e216. doi: 10.1371/journal.pbio.0060216
    Clarke, K.R., 1993. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18, 117-143. doi: 10.1111/j.1442-9993.1993.tb00438.x
    Crain, C.M., Kroeker, K., Halpern, B.S., 2008. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11, 1304-1315. doi: 10.1111/j.1461-0248.2008.01253.x
    Crick, H.Q.P., Dudley, C., Glue, D.E., Thomson, D.L., 1997. UK birds are laying eggs earlier. Nature, 388, 526.
    Da Silva, A., Samplonius, J.M., Schlicht, E., Valcu, M., Kempenaers, B., 2014. Artificial night lighting rather than traffic noise affects the daily timing of dawn and dusk singing in common European songbirds. Behav. Ecol. 25, 1037-1047. doi: 10.1093/beheco/aru103
    de Jong, M., van den Eertwegh, L., Beskers, R.E., de Vries, P.P., Spoelstra, K., Visser, M.E., 2018. Timing of avian breeding in an urbanised world. Ardea 106, 31. doi: 10.5253/arde.v106i1.a4
    De Laet, J., Summers-Smith, J.D., 2007. The status of the urban House Sparrow Passer domesticus in north-western Europe: A review. J. Ornithol. 148, 275-278. doi: 10.1007/s10336-007-0154-0
    de Satgé, J., Strubbe, D., Elst, J., De Laet, J., Adriaensen, F., Matthysen, E., 2019. Urbanisation lowers great tit Parus major breeding success at multiple spatial scales. J. Avian Biol. 50, e02108. doi: 10.1111/jav.02108
    Dominoni, D.M., Partecke, J., 2015. Does light pollution alter daylength? A test using light loggers on free-ranging European blackbirds (Turdus merula). Philos. Trans. R. Soc. B-Biol. Sci. 370, 20140118. doi: 10.1098/rstb.2014.0118
    Dominoni, D., Quetting, M., Partecke, J., 2013. Artificial light at night advances avian reproductive physiology. Proc. R. Soc. B-Biol. Sci. 280, 20123017. doi: 10.1098/rspb.2012.3017
    Dor, R., Safran, R.J., Sheldon, F.H., Winkler, D.W., Lovette, I.J., 2010. Phylogeny of the genus Hirundo and the Barn Swallow subspecies complex. Mol. Phylogenet. Evol. 56, 409-418. doi: 10.1016/j.ympev.2010.02.008
    Dormann, C.F., Elith, J., Bacher, S., Buchmann, C., Carl, G., Carré, G., et al., 2013. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36, 27-46. doi: 10.1111/j.1600-0587.2012.07348.x
    Fox, J., Weisberg, S., Adler, D., Bates, D., Baud-Bovy, G., Ellison, S., et al., 2012. Package 'car. '. R Foundation for Statistical Computing, Vienna.
    García-Navas, V., Sanz, J.J., 2011. Seasonal decline in provisioning effort and nestling mass of Blue Tits Cyanistes caeruleus: experimental support for the parent quality hypothesis: Seasonal decline in parental care in Blue Tits. Ibis 153, 59-69. doi: 10.1111/j.1474-919X.2010.01077.x
    Gaston, K.J., 2018. Lighting up the nighttime. Science 362, 744-746. doi: 10.1126/science.aau8226
    Grüebler, M.U., Naef-Daenzer, B., 2008. Fitness consequences of pre- and post-fledging timing decisions in a double-brooded passerine. Ecology 89, 2736-2745. doi: 10.1890/07-0786.1
    Grüebler, M.U., Korner-Nievergelt, F., Von Hirschheydt, J., 2010. The reproductive benefits of livestock farming in barn swallows Hirundo rustica: quality of nest site or foraging habitat?: Benefits of livestock farming. J. Appl. Ecol. 47, 1340-1347. doi: 10.1111/j.1365-2664.2010.01873.x
    Guo, F., Bonebrake, T.C., Dingle, C., 2016. Low frequency dove coos vary across noise gradients in an urbanized environment. Behav. Process 129, 86-93. doi: 10.1016/j.beproc.2016.06.002
    Halfwerk, W., Holleman, L.J.M., Lessells, C.K.M., Slabbekoorn, H., 2011. Negative impact of traffic noise on avian reproductive success: Traffic noise and avian reproductive success. J. Appl. Ecol. 48, 210-219. doi: 10.1111/j.1365-2664.2010.01914.x
    Håstad, O., Ödeen, A., 2014. A vision physiological estimation of ultraviolet window marking visibility to birds. PeerJ 2, e621. doi: 10.7717/peerj.621
    Henseler, J., Ringle, C.M., Sinkovics, R.R., 2009. The use of partial least squares path modeling in international marketing. In: Sinkovics, R.R., Ghauri, P.N. (Eds. ), Advances in International Marketing. Emerald Group Publishing Limited, pp. 277-319. https://www.emerald.com/insight/content/doi/10.1108/S1474-7979(2009)0000020014/full/html. (Accessed 10 Feb 2022).
    Huchler, K., Schulze, C.H., Gamauf, A., Sumasgutner, P., 2020. Shifting breeding phenology in Eurasian Kestrels Falco tinnunculus: Effects of weather and urbanization. Front. Ecol. Evol. 8, 247. https://doi.org/10.3389/fevo.2020.00247.
    Huet des Aunay, G., Grenna, M., Slabbekoorn, H., Nicolas, P., Nagle, L., Leboucher, G., et al., 2017. Negative impact of urban noise on sexual receptivity and clutch size in female domestic canaries. Ethology 123, 843-853. doi: 10.1111/eth.12659
    Imhoff, M.L., Zhang, P., Wolfe, R.E., Bounoua, L., 2010. Remote sensing of the urban heat island effect across biomes in the continental USA. Remote Sens. Environ. 114, 504-513. doi: 10.1016/j.rse.2009.10.008
    Injaian, A.S., Poon, L.Y., Patricelli, G.L., 2018. Effects of experimental anthropogenic noise on avian settlement patterns and reproductive success. Behav. Ecol. 29, 1181-1189. doi: 10.1093/beheco/ary097
    Jokimäki, J., Suhonen, J., Vuorisalo, T., Kövér, L., Kaisanlahti-Jokimäki, M. -L., 2017. Urbanization and nest-site selection of the Black-billed Magpie (Pica pica) populations in two Finnish cities: From a persecuted species to an urban exploiter. Lands Urban Plan. 157, 577-585. doi: 10.1016/j.landurbplan.2016.08.001
    Jones, T., Cresswell, W., 2010. The phenology mismatch hypothesis: are declines of migrant birds linked to uneven global climate change? J. Anim. Ecol. 79, 98-108. doi: 10.1111/j.1365-2656.2009.01610.x
    Kight, C.R., Swaddle, J.P., 2011. How and why environmental noise impacts animals: an integrative, mechanistic review: Environmental noise and animals. Ecol. Lett. 14, 1052-1061. doi: 10.1111/j.1461-0248.2011.01664.x
    Kight, C.R., Saha, M.S., Swaddle, J.P., 2012. Anthropogenic noise is associated with reductions in the productivity of breeding Eastern Bluebirds (Sialia sialis). Ecol. Appl. 22, 1989-1996. doi: 10.1890/12-0133.1
    Kosiński, Z., 2001. Effects of urbanization on nest site selection and nesting success of the Greenfinch Carduelis chloris in Krotoszyn, Poland. Ornis Fenn. 78, 175-183.
    Lê, S., Josse, J., Husson, F., 2008. FactoMineR: An R package for multivariate analysis. J. Stat. Softw. 25, 1-18.
    McKinney, M.L., 2008. Effects of urbanization on species richness: A review of plants and animals. Urban Ecosyst. 11, 161-176. doi: 10.1007/s11252-007-0045-4
    Merckx, T., Souffreau, C., Kaiser, A., Baardsen, L.F., Backeljau, T., Bonte, D., et al., 2018. Body-size shifts in aquatic and terrestrial urban communities. Nature 558, 113-116. doi: 10.1038/s41586-018-0140-0
    Moeller, A.P., 2010. The fitness benefit of association with humans: elevated success of birds breeding indoors. Behav, Ecol. 21, 913-918. doi: 10.1093/beheco/arq079
    Møller, A.P., Rubolini, D., Lehikoinen, E., 2008. Populations of migratory bird species that did not show a phenological response to climate change are declining. Proc. Natl. Acad. Sci. 105, 16195-16200. doi: 10.1073/pnas.0803825105
    Møller, A.P., Díaz, M., Grim, T., Dvorská, A., Flensted-Jensen, E., Ibáñez-Álamo, J., et al., 2015. Effects of urbanization on bird phenology: A continental study of paired urban and rural populations. Clim. Res. 66, 185-199. doi: 10.3354/cr01344
    Nebel, S., Mills, A., McCracken, J.D., Taylor, P.D., 2010. Declines of aerial insectivores in North America follow a geographic gradient. Avian Conserv. Ecol. 5, 1. doi: 10.1109/RAMS.2010.5448067
    Oksanen, J., Kindt, R., Legendre, P., O'Hara, B., Stevens, M.H.H., Oksanen, M.J., et al., 2007. The vegan package. Commun. Ecol. Pack. 10, 719.
    Ouyang, J.Q., de Jong, M., van Grunsven, R.H.A., Matson, K.D., Haussmann, M.F., Meerlo, P., et al., 2017. Restless roosts: Light pollution affects behavior, sleep, and physiology in a free-living songbird. Glob. Change Biol. 23, 4987-4994. doi: 10.1111/gcb.13756
    Pagani-Núñez, E., Uribe, F., Hernández-Gómez, S., Muñoz, G., Senar, J.C., 2014. Habitat structure and prey composition generate contrasting effects on carotenoid-based coloration of great tit Parus major nestlings: determinants of nestling coloration. Biol. J. Linn. Soc. 113, 547-555. doi: 10.1111/bij.12352
    Pagani-Nunez, E., He, C., Li, B., Li, M., He, R., Jiang, A., et al., 2016. The breeding ecology of the barn swallow Hirundo rustica gutturalis in South China. J. Trop. Ecol. 32, 260-263. doi: 10.1017/S0266467416000201
    Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., Team, R.C., 2007. Linear and nonlinear mixed effects models. R Package Version 3, 1-89.
    R Core Team, 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/.
    Raja-aho, S., Eeva, T., Suorsa, P., Valkama, J., Lehikoinen, E., 2017. Juvenile Barn Swallows Hirundo rustica L. from late broods start autumn migration younger, fuel less effectively and show lower return rates than juveniles from early broods. Ibis 159, 892-901. doi: 10.1111/ibi.12492
    Ramirez, F., Coll, M., Navarro, J., Bustamante, J., Green, A.J., 2018. Spatial congruence between multiple stressors in the Mediterranean Sea may reduce its resilience to climate impacts. Sci. Rep. 8, 14871. doi: 10.1038/s41598-018-33237-w
    Schlesinger, M.D., Manley, P.N., Holyoak, M., 2008. Distinguishing stressors acting on land bird communities in an urbanizing environment. Ecology 89, 2302-2314. doi: 10.1890/07-0256.1
    Schroeder, J., Nakagawa, S., Cleasby, I.R., Burke, T., 2012. Passerine birds breeding under chronic noise experience reduced fitness. PLoS One 7, e39200. doi: 10.1371/journal.pone.0039200
    Senzaki, M., Barber, J.R., Phillips, J.N., Carter, N.H., Cooper, C.B., Ditmer, M.A., et al., 2020. Sensory pollutants alter bird phenology and fitness across a continent. Nature 587, 605-609. doi: 10.1038/s41586-020-2903-7
    Seress, G., Hammer, T., Bókony, V., Vincze, E., Preiszner, B., Pipoly, I., et al., 2018. Impact of urbanization on abundance and phenology of caterpillars and consequences for breeding in an insectivorous bird. Ecol. Appl. 28, 1143-1156. doi: 10.1002/eap.1730
    Seress, G., Sándor, K., Evans, K.L., Liker, A., 2020. Food availability limits avian reproduction in the city: An experimental study on great tits Parus major. J. Anim. Ecol. 89, 1570-1580. doi: 10.1111/1365-2656.13211
    Seto, K.C., Fragkias, M., Güneralp, B., Reilly, M.K., 2011. A meta-analysis of global urban land expansion. PLoS One 6, e23777. doi: 10.1371/journal.pone.0023777
    Shannon, G., McKenna, M.F., Angeloni, L.M., Crooks, K.R., Fristrup, K.M., Brown, E., et al., 2016. A synthesis of two decades of research documenting the effects of noise on wildlife: Effects of anthropogenic noise on wildlife. Biol. Rev. 91, 982-1005. doi: 10.1111/brv.12207
    Sievers, M., Hale, R., Parris, K.M., Swearer, S.E., 2018. Impacts of human-induced environmental change in wetlands on aquatic animals: Animal communities, populations and individuals in human-impacted wetlands. Biol. Rev. 93, 529-554. doi: 10.1111/brv.12358
    Sol, D., Lapiedra, O., González-Lagos, C., 2013. Behavioural adjustments for a life in the city. Anim. Behav. 85, 1101-1112. doi: 10.1016/j.anbehav.2013.01.023
    Sprau, P., Mouchet, A., Dingemanse, N.J., 2017. Multidimensional environmental predictors of variation in avian forest and city life histories. Behav. Ecol. 28, 59-68. doi: 10.1093/beheco/arw130
    Stoleson, S.H., Beissinger, S.R., 1999. Egg viability as a constraint on hatching synchrony at high ambient temperatures. J. Anim. Ecol. 68, 951-962. doi: 10.1046/j.1365-2656.1999.00342.x
    Strasser, E.H., Heath, J.A., 2013. Reproductive failure of a human-tolerant species, the American kestrel, is associated with stress and human disturbance. J. Appl. Ecol. 50, 912-919. doi: 10.1111/1365-2664.12103
    Summers-Smith, J.D., 2003. The decline of the House Sparrow: A review. Br. Birds 96, 439-446.
    Symonds, M.R.E., Moussalli, A., 2011. A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike's information criterion. Behav. Ecol. Sociobiol. 65, 13-21. doi: 10.1007/s00265-010-1037-6
    Teglhøj, P.G., 2017. A comparative study of insect abundance and reproductive success of barn swallows Hirundo rustica in two urban habitats. J. Avian Biol. 48, 846-853. doi: 10.1111/jav.01086
    Tuanmu, M. -N., Jetz, W., 2014. A global 1-km consensus land-cover product for biodiversity and ecosystem modelling: Consensus land cover. Glob. Ecol. Biogeogr. 23, 1031-1045. doi: 10.1111/geb.12182
    Verhulst, S., Nilsson, J. -Å., 2008. The timing of birds' breeding seasons: a review of experiments that manipulated timing of breeding. Philos. Trans. R. Soc. B-Biol. Sci. 363, 399-410. doi: 10.1098/rstb.2007.2146
    Visser, M.E., Holleman, L.J.M., Gienapp, P., 2006. Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird. Oecologia 147, 164-172. doi: 10.1007/s00442-005-0299-6
    Wang, J. -S., Tuanmu, M. -N., Hung, C. -M., 2021. Effects of artificial light at night on the nest-site selection, reproductive success and behavior of a synanthropic bird. Environ. Pollut. 288, 117805. doi: 10.1016/j.envpol.2021.117805
    Welbers, A.A.M.H., van Dis, N.E., Kolvoort, A.M., Ouyang, J., Visser, M.E., Spoelstra, K., et al., 2017. Artificial light at night reduces daily energy expenditure in breeding Great Tits (Parus major). Front. Ecol. Evol. 5, 55. doi: 10.3389/fevo.2017.00055
    World Health Organization (Ed. ), 1999. The World Health Report 1999: making a difference. WHO, Geneva.
    Xu, Y., Cao, Z., Wang, B., 2020. Effect of urbanization intensity on nest-site selection by Eurasian Magpies (Pica pica). Urban Ecosyst. 23, 1099-1105. doi: 10.1007/s11252-020-00996-2
    Zhang, K., Wang, R., Shen, C., Da, L., 2010. Temporal and spatial characteristics of the urban heat island during rapid urbanization in Shanghai, China. Environ. Monit. Assess. 169, 101-112. doi: 10.1007/s10661-009-1154-8
    Zhao, Y., Liu, Y., Scordato, E.S.C., Lee, M., Xing, X., Pan, X., et al., 2021. The impact of urbanization on body size of Barn Swallows Hirundo rustica gutturalis. Ecol. Evol. 11, 612-625. doi: 10.1002/ece3.7088
    Zink, R.M., Pavlova, A., Rohwer, S., Drovetski, S.V., 2006. Barn swallows before barns: Population histories and intercontinental colonization. Proc. R. Soc. B-Biol. Sci. 273, 1245-1251. doi: 10.1098/rspb.2005.3414
    Zuur, A.F., Ieno, E.N., Walker, N., Saveliev, A.A., Smith, G.M., 2009. Mixed effects models and extensions in ecology with R. Springer, New York. http://link.springer.com/10.1007/978-0-387-87458-6. (Accessed 1 Feb 2022).
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(4)  / Tables(4)

    Article Metrics

    Article views (146) PDF downloads(8) Cited by()
    Proportional views

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return