Volume 13 Issue 1
Mar.  2022
Turn off MathJax
Article Contents
Abstract
Background
Methods
Results
Discussion
Conclusions
Additional file
Authors' contributions
Acknowledgements
Competing interests
References
Related Articles
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
shu

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

  • a.

    State Key Laboratory of Biocontrol, School of Ecology, Sun Yat-sen University, Guangzhou, 510006, China

  • b.

    Institute of Eco-Environmental Research, Guangxi Academy of Sciences, Nanning, 530007, China

  • c.

    Department of Health and Environmental Sciences, Xi'an Jiaotong-Liverpool University, Suzhou, 215028, China

  • d.

    Key Laboratory for Biodiversity Science and Ecological Engineering, Ministry of Education, College of Life Sciences, Beijing Normal University, Beijing, 100091, China

  • e.

    College of Wildlife and Protected Area, Northeast Forestry University, Harbin, 150006, China

  • f.

    Institute of Wildlife Conservation, Central South University of Forestry and Technology, Changsha, 410004, China

  • g.

    College of Life Science, Liaoning University, Shenyang, 110036, China

  • h.

    Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, USA

More Information
  • Corresponding author:

    E-mail address: emilio.pnunez@xjtlu.edu.cn (E. Pagani-Núñez)

  • 1 These authors contributed equally to the paper.

  • Received Date: 09 Mar 2022
  • Rev Recd Date: 26 Jun 2022
  • Accepted Date: 26 Jun 2022
  • Available Online: 10 Oct 2022
  • Publish Date: 30 Jul 2022
    Graphical Abstract
    • Abstract

  • 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.

    • FullText(HTML)

  • Hearing the sound, 'cu-coo', a simple but charismatic call produced by the Common Cuckoo, Cuculus canorus, indicates the arrival of spring to people who live in the northern hemisphere of the Eurasian continent. However, it also indicates imminent fitness loss to the family of other bird species (hosts) in the area, because they will soon lose all their progeny while gaining an alien cuckoo chick in their nests. The evolutionary arms race between avian brood parasites and their hosts to maximize their respective fitness has been a model system for co-evolutionary studies for over a century (Davies 2000; Erritzøe et al. 2012). From these studies, we know that such a co-evolutionary relationship results in profound effects, directly or indirectly, on various aspects of the biological evolution of brood parasites, for example, egg mimicry, reduced female body size and accelerated phenotypic diversification (Sorenson et al. 2003; Stoddard and Stevens 2011; Medina and Langmore 2015). However, little is known about how this behavior is associated with the vocal evolution of brood parasites.

    Circumstantial evidence suggests that brood parasitic behavior could be associated with the vocal evolution of parasitic species. For example, Sorenson et al. (2003) showed that the male song types of adult indigobirds, Vidua spp., could vary according to the host species that raise them as they mimic the host's song. Fuisz and de Kort (2007) proposed that the calls of the Common Cuckoo diverge according to the types of habitats that they occupy. Similarly, some generalist brood parasitic species are known to be composed of multiple lineages of host-specific races within a species (Davies 2000), and if the host-specific divergence results in vocal divergence, we may see increased intraspecific variation in the vocal characteristics in the parasitic species. Other life history traits that appear to be derived with brood parasitism such as reduced body size (Medina and Langmore 2015) and increased breeding home range size (Krüger and Davies 2002), may also be associated directly or indirectly with vocal evolution. In this study, we analysed male calls produced by species belonging to the subfamily Cuculinae to explore the evolutionary patterns of vocalization between the lineage of parasitic and nonparasitic species, which may have implications for understanding the vocal evolution of non-oscine birds.

    Data collection

    We collected acoustic and phylogenetic data for the species belonging to the subfamily Cuculinae, in which 56 parasitic and 32 nonparasitic species are currently recognized (Payne and Sorenson 2005). Among these we obtained acoustic data for 80 species from online repositories (see below). Phylogenetic tress were generated using BirdTree (birdtree.org, http://www.birdtree.org, Jetz et al. 2012) for 76 species. As a result, both acoustic and phylogenetic data were available for 67 species (42 parasitic and 25 nonparasitic species), with which we conducted further analyses.

    Acoustic samples of the typical male calls were collected from mainly Xeno-Canto (www.xeno-canto.org) and AVoCet (Avian Vocalizations Center, www.avocet.zoology.msu.edu). We referred to Payne and Sorenson (2005) to determine a typical male call type for each of the species. On average, we collected 13.57 ± 6.19 different high quality calls across species (see Additional file 1: Table S1). In this study, we followed the scientific names used by and Sorenson (2005) because these are consistent with those used in Xeno-Canto.

    Acoustic data measurement

    Acoustic parameters were measured using the software Raven Pro 1.4 (Cornell Lab of Ornithology 2010). We measured five parameters for each sample: high frequency (HF), low frequency (LF), delta frequency (DF), delta time (DT), and number of notes (NN) (Fig. 1). HF and LF represent the highest and lowest pitch of selected ranges of syllables, respectively, and DF is the difference between them. DT is the time duration of the syllable, and NN, the number of notes involved in a single syllable. All definitions of parameters follow the manual of Raven Pro 1.4. (Charif et al. 2010).

    Figure  1.  Spectrograms of brood parasitic and nonparasitic species illustrating five parameters measured in this study. a Cuculus canorus and b Chrysococcyx caprius as brood parasitic species. Likewise, c Coccyzus minuta and d Coccyzus americanus as nonparasitic species. HF, LF, DF, DT and NN represent high frequency, low frequency, delta frequency, delta time, and the number of notes, respectively. The number of black dots above spectrograms indicates the number of notes
    DownLoad: Full-Size Img PowerPoint

    Statistical analysis

    Analyses were conducted in two ways, with and without phylogenetic consideration. For the original data without phylogenetic consideration, the distribution patterns of vocal parameters between the parasitic and nonparasitic groups were compared using the Kolmogorov–Smirnov tests. The Wilcoxon rank sum tests were applied to examine the median difference between the two groups. On the other hand, phylogenetic independent contrast (PIC) analyses were conducted for each parameters using the function "brunch" in the package "Caper" (Orme et al. 2013) in R 3.2.1 (R Development Core Team 2011), which calculates the contrast values of the continuous variable on the nodes where two different categorical variables diverge. For phylogenetic information used in the analysis, we first obtained a total of 1000 possible phylogenetic trees of the 67 Cuculinae species from BirdTree (Rubolini et al. 2015), and then we randomly selected a tree from these to meet the condition of the phylogenetic tree format for the analysis (Additional file 1: Fig. S1). The choice of trees may not change the results qualitatively as shown in other studies (e.g., Medina and Langmore 2015). Statistical significance of the difference in the mean of the contrast values from zero was tested using a one-sample t test. Models were checked for the robustness of the contrast using 'caic.diagnostics' function in 'Caper'. Acoustic data were averaged according to species, and log-transformed before the analysis. All statistical analyses were performed in R 3.2.1 (R Development Core Team 2011).

    The original data exhibited that the nonparasitic group showed larger variation in DF (D = 0.465, p = 0.002), DT (D = 0.352, p = 0.04), HF (D = 0.377, p = 0.02), and NN (D = 0.465, p = 0.002). LF was the exception in that the parasitic group showed larger variation (D = 0.762, p < 0.001), albeit over small ranges (Fig. 2a-e). Likewise, harmonic structures were observed to a greater extent in the nonparasitic cuckoos (20 species out of 25) than in the parasitic group (7 species out of 42; χ2 = 26.8, df = 3, p < 0.0001; see Additional file 1: Table S1). As a result, the median values of vocal parameters except LF tended to be smaller in the parasitic group, although statistical significances varied among parameters (DF: W = 789, p < 0.001; DT: W = 548, p = 0.78; HF: W = 647, p = 0.12; LF: W = 105, p < 0.001; NN: W = 676, p = 0.05). Consistently with the results of the original data, the phylogenetically independent contrasts test showed significant difference in vocal parameters between the parasitic and nonparasitic groups (Fig. 2f). The mean contrasts were significantly below zero for most parameters (DF: t2 = − 4.07, p = 0.06; DT: t2 = − 7.51, p = 0.02; HF: t2 = − 3.84, p = 0.06; NN: t2 = − 4.28, p = 0.05), indicating that the parasitic group tends to have smaller average values than the nonparasitic group for these parameters. On the other hand, the average contrasts value of LF was significantly above zero (t2 = 7.90, p = 0.02), implying that the parasitic group had higher LF than the nonparasitic group, as shown with the original data.

    Figure  2.  Comparison of vocal parameters between the parasitic and nonparasitic groups in Cuculinae. Both the original data without phylogenetic consideration (a‒e) and the result of phylogenetic independent contrasts (f) are shown. DF, DT, HF, NN, and LF represent delta frequency, delta time, high frequency, number of notes and low frequency, respectively. Each dot represents different species, and the data are summarized with box and whiskers plots
    DownLoad: Full-Size Img PowerPoint

    Our results indicate that interspecific differences in vocalization are much larger in the nonparasitic than in the parasitic group, and that the parasitic species of Cuculinae tend to have simpler and lower-frequency calls than the nonparasitic species. This imply that vocal evolution occurs much more slowly among the parasitic species in the sub-family Cuculinae with the acoustic structures converging to be simple with lower-frequency ranges, overall suggesting the potential association between brood parasitic behavior and vocal evolution. The reason for the difference in the spectral features of the call between the two groups remain unknown. Krüger and Davies (2002) suggested that parasitic species appear to have an increased breeding-range size in the family Cuculinae, and the intraspecific vocal competition is intensive in the parasitic cuckoos (J.-W. L. unpublished data). In these situations, simple and low-frequency calls may facilitate their ability to manage relatively large breeding ranges. Ecological characteristics of breeding area such as habitat openness and humidity could also favour low-frequency calls (McCracken and Sheldon 1997; Bertelli and Tubaro 2002; Brumm 2004). Unlike the nonparasitic species, many of the parasitic species belonging to the family Cuculidae migrate from a humid tropical zone to a relatively dry temperate zone to breed, and they tend to occupy open habitats (Krüger and Davies 2002). These ecological conditions may select for lower-frequency calls with simple structures in the parasitic species. However, selection pressures that generate vocal differences between the two groups and the role of brood parasitism in there are major issues that remain to be resolved. It would be worthwhile to extend the comparative analysis that we have done in this study to other parasitic lineages such as Icteridae (Fraga 2008). Experimental studies to reveal the underlying reasons for the differences that we found in this study are also necessary to verify our conclusions.

    Overall, our results imply the probability that brood parasitism may play a role in vocal evolution, especially for males. However, it is well recognized in some parasitic species that females also produce calls during the breeding season, such as the bubbling call produced by female Common Cuckoos (Kim et al. 2017). Our knowledge on the variation in female calls and the contribution of brood parasitism to the evolution of female calls is also very limited (York and Davies 2017). Collectively, a better understanding of the vocal evolution in brood parasites may greatly improve our knowledge of vocal diversification in non-oscine birds.

    Additional file 1: Table S1. A list for scientific names of 67 species, code numbers of raw files in Xeno-Canto (XC) or AVoCet (AV), the number of vocal samples obtained from each species, and the presence of harmonic structures. According to Birdlife V5, which "Birdtree.org" referred to, there are different scientific names for 11 species (see comments). Figure S1. A phylogenetic tree showing the relationship among 67 species in Cuculinae examined in this study.

    HK and JWL conceived and designed the study; HK and JWL collected and analysed the data; HK, JWL and JCY wrote the manuscript. All authors read and approved the final manuscript.

    We are grateful to all the people who recorded bird songs in the field and shared those through online repositories. We also thanks to Hye-Kyoung Moon for phylogenetic advice, and Hee-Jin Noh, Kyung-Hoe Kim, Ha-Na Yoo, Sung-Ho Yoon, Hae-Ni Kim, and So-Hyeon Yoo for constructive discussions about the idea of this study.

    The authors declare that they have no competing interests.

    • References (82)
  • 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.
    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.
    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.
    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.
    Barton, K., 2022. MuMIn: multi-model inference. R package, version 1.46.0. .
    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.
    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.
    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.
    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.
    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.
    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.
    Cirelli, C., Tononi, G., 2008. Is sleep essential? PLoS Biol. 6, e216.
    Clarke, K.R., 1993. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18, 117-143.
    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.
    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.
    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.
    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.
    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.
    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.
    Dominoni, D., Quetting, M., Partecke, J., 2013. Artificial light at night advances avian reproductive physiology. Proc. R. Soc. B-Biol. Sci. 280, 20123017.
    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.
    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.
    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.
    Gaston, K.J., 2018. Lighting up the nighttime. Science 362, 744-746.
    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.
    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.
    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.
    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.
    Håstad, O., Ödeen, A., 2014. A vision physiological estimation of ultraviolet window marking visibility to birds. PeerJ 2, e621.
    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. . (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. .
    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.
    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.
    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.
    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.
    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.
    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.
    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.
    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.
    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.
    Moeller, A.P., 2010. The fitness benefit of association with humans: elevated success of birds breeding indoors. Behav, Ecol. 21, 913-918.
    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.
    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.
    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.
    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.
    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.
    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.
    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. .
    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.
    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.
    Schlesinger, M.D., Manley, P.N., Holyoak, M., 2008. Distinguishing stressors acting on land bird communities in an urbanizing environment. Ecology 89, 2302-2314.
    Schroeder, J., Nakagawa, S., Cleasby, I.R., Burke, T., 2012. Passerine birds breeding under chronic noise experience reduced fitness. PLoS One 7, e39200.
    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.
    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.
    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.
    Seto, K.C., Fragkias, M., Güneralp, B., Reilly, M.K., 2011. A meta-analysis of global urban land expansion. PLoS One 6, e23777.
    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.
    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.
    Sol, D., Lapiedra, O., González-Lagos, C., 2013. Behavioural adjustments for a life in the city. Anim. Behav. 85, 1101-1112.
    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.
    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.
    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.
    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.
    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.
    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.
    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.
    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.
    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.
    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.
    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.
    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.
    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.
    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.
    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. . (Accessed 1 Feb 2022).
    • Related Articles

  • Related Articles

    Jian Ding, Shengnan Wang, Wenzhi Yang, Huijie Zhang, Ni Wang, Yingmei Zhang. 2025: How does asymmetric sibling rivalry respond under environmental metal pollution? A case study of the Tree Sparrow (Passer montanus). Avian Research, 16(1): 100225. DOI: 10.1016/j.avrs.2025.100225
    Joana S. Costa, Steffen Hahn, José A. Alves. 2024: Variation of parental and chick diet in opportunistic insectivorous European Bee-eaters. Avian Research, 15(1): 100211. DOI: 10.1016/j.avrs.2024.100211
    Xiaogang Yao, Neng Wu, Yan Cai, Canchao Yang. 2023: The effects of anthropogenic noise on nest predation with respect to predator species across different habitats and seasons. Avian Research, 14(1): 100121. DOI: 10.1016/j.avrs.2023.100121
    Juan A. Amat, Nico Varo, Marta I. Sánchez, Andy J. Green, Dámaso Hornero-Méndez, Juan Garrido-Fernández, Cristina Ramo. 2023: Physiological strategies of moult-migrating Black-necked Grebes (Podiceps nigricollis) in a polluted staging site according to blood chemistry. Avian Research, 14(1): 100118. DOI: 10.1016/j.avrs.2023.100118
    Alfred-Ștefan Cicort-Lucaciu, Hanem-Vera Keshta, Paula-Vanda Popovici, David Munkácsi, Ilie-Cătălin Telcean, Carmen Gache. 2022: Urban avifauna distribution explained by road noise in an Eastern European city. Avian Research, 13(1): 100067. DOI: 10.1016/j.avrs.2022.100067
    Limin Wang, Ghulam Nabi, Liyun Yin, Yanqin Wang, Shuxin Li, Zhuang Hao, Dongming Li. 2021: Birds and plastic pollution: recent advances. Avian Research, 12(1): 59. DOI: 10.1186/s40657-021-00293-2
    Donghui Ma, Mengjie Lu, Zhichang Cheng, Xingnan Du, Xiaoyu Zou, Xingxing Yao, Xinkang Bao. 2021: Male parent birds exert more effort to reproduce in two desert passerines. Avian Research, 12(1): 37. DOI: 10.1186/s40657-021-00273-6
    Cecilia Odette Carral-Murrieta, Michelle García-Arroyo, Oscar H. Marín-Gómez, J. Roberto Sosa-López, Ian MacGregor-Fors. 2020: Noisy environments: untangling the role of anthropogenic noise on bird species richness in a Neotropical city. Avian Research, 11(1): 32. DOI: 10.1186/s40657-020-00218-5
    Xinkang Bao, Wei Zhao, Fangqing Liu, Jianliang Li, Donghui Ma. 2020: Egg investment strategies adopted by a desertic passerine, the Saxaul Sparrow (Passer ammodendri). Avian Research, 11(1): 15. DOI: 10.1186/s40657-020-00201-0
    Nan Lyu, Jinlin Li, Yue-Hua Sun. 2016: Can simple songs express useful signals for mate choice?. Avian Research, 7(1): 10. DOI: 10.1186/s40657-016-0045-2

Catalog

    Figures(4)  /  Tables(4)

    Get Citation
    PDF
    XML

    Article Metrics

    Article has an altmetric score of 3
    Article has an altmetric score of 3
    Article views (246) PDF downloads (18) Cited by()
    Supported by: Beijing Renhe Information Technology Co. Ltd.   Technical support: info@rhhz.net

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return