Journal Home > Volume 14 , Issue 2
Avian Research 2023, 14(2): 100100 https://doi.org/10.1016/j.avrs.2023.100100
Research Article | Open Access | Issue | Published: 07 April 2023

Variation in reproductive life-history traits of Chinese Bulbuls (Pycnonotus sinensis) along the urbanization gradient in Hangzhou, China

Show Author's Information Xingmin Chena,  Qin Zhangb,  Sisi Lanb,  Qin Huangc,  Shuihua Chenc,d( ),  Yanping Wanga( )
Laboratory of Island Biogeography and Conservation Biology, College of Life Sciences, Nanjing Normal University, Nanjing, 210023, China
College of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, 321004, China
Zhejiang Museum of Natural History, Hangzhou, 310012, China
Zhejiang Provincial Museum, Hangzhou, 310007, China
Keywords:
Laying date, Urbanization, Nest predation, Feeding frequency, Life-history trait, Urbanization synthetic index (USI)
Cite this article:
Chen X, Zhang Q, Lan S, et al. Variation in reproductive life-history traits of Chinese Bulbuls (Pycnonotus sinensis) along the urbanization gradient in Hangzhou, China. Avian Research, 2023, 14(2): 100100. https://doi.org/10.1016/j.avrs.2023.100100
Download citation
EndNote(RIS)
BibTeX

673

Views

7

Downloads

Citations

0

Crossref

0

WoS

0

Scopus

0

CSCD

Abstract Full text About this article

Urbanization brings new selection pressures to wildlife living in cities, and changes in the life-history traits of urban species can reflect their responses to such pressures. To date, most of the studies investigating the impacts of urbanization on avian life-history traits are conducted in Europe and North America, while such studies are often lacking in quickly developing countries in Asia (e.g., China). In this study, we examined the variations in reproductive life-history traits of Chinese Bulbuls (Pycnonotus sinensis) along the urbanization gradient in Hangzhou, China. We detected 234 natural nests of Chinese Bulbuls and continuously monitored them in two continuous breeding seasons from 2012 to 2013. We collected data on seven life-history traits (laying date, incubation period, nestling period, clutch size, egg volume, hatching success rate, and fledging success rate). We used infrared cameras to record the number of feedings per hour as the measure of food resources for the nestlings. We measured nest predation pressure by monitoring 148 natural breeding nests during breeding seasons and 54 artificial nests immediately after breeding seasons. We then calculated the urbanization synthetic index (USI) as a measure of the level of urbanization and examined its relationship with the seven life-history traits. We found that Chinese Bulbuls laid eggs significantly earlier with increasing USI. However, the other six life-history traits did not vary significantly with the USI. Moreover, the feeding frequency of chicks increased significantly with the USI, but the nest predation pressure of Chinese Bulbuls decreased significantly with the USI. Increased food resources and reduced nest predation pressure in cities may lead to earlier laying date of Chinese Bulbuls. Further study should test whether the earlier laying date of Chinese Bulbuls is the result of phenotypic plasticity or genetic change.


menu
Abstract
Full text
Outline
About this article

Variation in reproductive life-history traits of Chinese Bulbuls (Pycnonotus sinensis) along the urbanization gradient in Hangzhou, China

Show Author's information Xingmin Chena, Qin Zhangb, Sisi Lanb, Qin Huangc, Shuihua Chenc,d( ), Yanping Wanga( )
Laboratory of Island Biogeography and Conservation Biology, College of Life Sciences, Nanjing Normal University, Nanjing, 210023, China
College of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, 321004, China
Zhejiang Museum of Natural History, Hangzhou, 310012, China
Zhejiang Provincial Museum, Hangzhou, 310007, China

Abstract

Urbanization brings new selection pressures to wildlife living in cities, and changes in the life-history traits of urban species can reflect their responses to such pressures. To date, most of the studies investigating the impacts of urbanization on avian life-history traits are conducted in Europe and North America, while such studies are often lacking in quickly developing countries in Asia (e.g., China). In this study, we examined the variations in reproductive life-history traits of Chinese Bulbuls (Pycnonotus sinensis) along the urbanization gradient in Hangzhou, China. We detected 234 natural nests of Chinese Bulbuls and continuously monitored them in two continuous breeding seasons from 2012 to 2013. We collected data on seven life-history traits (laying date, incubation period, nestling period, clutch size, egg volume, hatching success rate, and fledging success rate). We used infrared cameras to record the number of feedings per hour as the measure of food resources for the nestlings. We measured nest predation pressure by monitoring 148 natural breeding nests during breeding seasons and 54 artificial nests immediately after breeding seasons. We then calculated the urbanization synthetic index (USI) as a measure of the level of urbanization and examined its relationship with the seven life-history traits. We found that Chinese Bulbuls laid eggs significantly earlier with increasing USI. However, the other six life-history traits did not vary significantly with the USI. Moreover, the feeding frequency of chicks increased significantly with the USI, but the nest predation pressure of Chinese Bulbuls decreased significantly with the USI. Increased food resources and reduced nest predation pressure in cities may lead to earlier laying date of Chinese Bulbuls. Further study should test whether the earlier laying date of Chinese Bulbuls is the result of phenotypic plasticity or genetic change.

Keywords: Laying date, Urbanization, Nest predation, Feeding frequency, Life-history trait, Urbanization synthetic index (USI)

References(72)

Arnfield, A.J., 2003. Two decades of urban climate research: a review of turbulence, exchanges of energy and water, and the urban heat island. Int. J. Climatol. 23, 1-26.
DOI Google Scholar

Bailly, J., Scheifler, R., Berthe, S., Clement-Demange, V., Leblond, M., Pasteur, B., et al., 2015. From eggs to fledging: negative impact of urban habitat on reproduction in two tit species. J. Ornithol. 157, 377-392.
DOI Google Scholar

Batisteli, A.F., Costiuc, M.Y., Santieff, I.Z., Costa, R.O., Sarmento, H., Pizo, M.A., et al., 2020. Breeding biology of the Creamy-bellied Thrush (Turdus amaurochalinus) in southeast Brazil. Stud. Neotrop. Fauna Environ. 55, 233-241.
DOI Google Scholar

Benharzallah, N., Bachir, A.S., Barbraud, C., 2022. Nest characteristics and food supply affect reproductive output of white storks Ciconia ciconia in semi-arid areas. Biologia 77, 997-1006.
DOI Google Scholar

Bolger, D.T., Scott, T.A., Rotenberry, J.T., 1997. Breeding bird abundance in an urbanizing landscape in coastal southern California. Conserv. Biol. 11, 406-421.
DOI Google Scholar

Bolker, B.M., Brooks, M.E., Clark, C.J., Geange, S.W., Poulsen, J.R., Stevens, M.H.H., White, J.S.S., 2008. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol. Evol. 24, 127–135.
DOI Google Scholar

Bridge, E.S., Schoech, S.J., Bowman, R., Wingfield, J.C., 2009. Temporal predictability in food availability: effects upon the reproductive axis in Scrub-Jays. J. Exp. Zool. 311, 35-44.
DOI Google Scholar

Caizergues, A.E., Gregoire, A., Charmantier, A., 2018. Urban versus forest ecotypes are not explained by divergent reproductive selection. Proc. R. Soc. B 285, 20180261.
DOI Google Scholar

Callaghan, C.T., Major, R.E., Wilshire, J.H., Martin, J.M., Kingsford, R.T., Cornwell, W.K., et al., 2019. Generalists are the most urban-tolerant of birds: a phylogenetically controlled analysis of ecological and life history traits using a novel continuous measure of bird responses to urbanization. Oikos 128, 845-858.
DOI Google Scholar

Capilla-Lasheras, P., Thompson, M.J., Sánchez-Tójar, A., Haddou, Y., Branston, C.J., Réale, D., et al., 2022. A global meta-analysis reveals higher variation in breeding phenology in urban birds than in their non-urban neighbours. Ecol. Lett. 25, 2552–2570.
DOI Google Scholar

Castro, I., Brunton, D.H., Mason, K.M., Ebert, B., Griffiths, R., 2003. Life history traits and food supplementation affect productivity in a translocated population of the endangered Hihi (Stitchbird, Notiomystis cincta). Biol. Conserv. 114, 271-280.
DOI Google Scholar

Chamberlain, D.E., Cannon, A.R., Toms, M., Leech, D., Hatchwell, B.J., Gaston, K.J., et al., 2009. Avian productivity in urban landscapes: a review and meta-analysis. Ibis 151, 1-18.
DOI Google Scholar

Chen, S., Ding, P., Zheng, G., Zhuge, Y., 2000. Effects of urbanization on wetland waterbird communities in Hangzhou. Zool. Res. 21, 279-285.
DOI Google Scholar

Chen, W., Wu, Y., Hu, J., Yu, Z., Guo, Z., 2006. Nest site selection and materials of Pycnonotus sinensis in Nanchong, Sichuan. Sichuan J. Zool. 25, 590-593.
Google Scholar

Chen, X., Zhang, Q., Lan, S., Chen, S., Wang, Y., 2022. Nest predation pressure on Chinese Bulbuls decreases along the urbanization gradient in Hangzhou, China. Avian Res. 13, 100049.
DOI Google Scholar

Chick, L.D., Strickler, S.A., Perez, A., Martin, R.A., Diamond, S.E., 2019. Urban heat islands advance the timing of reproduction in a social insect. J. Therm. Biol. 80, 119-125.
DOI Google Scholar

Corsini, M., Dubiec, A., Marrot, P., Szulkin, M., 2017. Humans and tits in the city: quantifying the effects of human presence on great tit and blue tit reproductive trait variation. Front. Ecol. Evol. 5, 82.
DOI Google Scholar

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, 31-38.
DOI Google Scholar

Delignette-Muller, M.L., Dutang, C., 2015. Fitdistrplus: an R package for fitting distributions. J. Stat. Softw. 64, 1-34.
DOI Google Scholar

de Neve, L., Soler, J.J., Soler, M., Perez-Contreras, T., Martin-Vivaldi, M., Martinez, J.G., et al., 2004. Effects of a food supplementation experiment on reproductive investment and a post-mating sexually selected trait in magpies Pica pica. J. Avian Biol. 35, 246-251.
DOI Google Scholar

Drent, R.H., 1970. Functional aspects of incubation in the herring gull (Larus argentatus Pont.). Behaviour 17, 1-132.
Google Scholar

Eden, S.F., 1985. The comparative breeding biology of magpies Pica pica in an urban and a rural habitat (Aves: Corvidae). J. Zool. 205, 325-334.
DOI Google Scholar

Feng, C., Liang, W., 2020. Behavioral responses of Black-headed Gulls (Chroicocephalus ridibundus) to artificial provisioning in China. Global Ecol. Conserv. 21, e00873.
DOI Google Scholar

Fernandez-Juricic, E., 2000. Local and regional effects of pedestrians on forest birds in a fragmented landscape. Condor 102, 247-255.
DOI Google Scholar

Ghalambor, C.K., Martin, T.E., 2000. Parental investment strategies in two species of nuthatch vary with stage-specific predation risk and reproductive effort. Anim. Behav. 60, 263-267.
DOI Google Scholar

Ghalambor, C.K., Martin, T.E., 2001. Fecundity-survival trade-offs and parental risk-taking in birds. Science 292, 494-497.
DOI Google Scholar

Gaston, K.J., Bennie, J., Davies, T.W., Hopkins, J., 2013. The ecological impacts of nighttime light pollution: a mechanistic appraisal. Biol. Rev. 88, 912-927.
DOI Google Scholar

Hanmer, H.J., Thomas, R.L., Fellowes, M.D.E., 2017. Provision of supplementary food for wild birds may increase the risk of local nest predation. Ibis 159, 158-167.
DOI Google Scholar

Hawkins, C.E., Ritrovato, I.T., Swaddle, J.P., 2020. Traffic noise alters individual social connectivity, but not space-use, of Red-backed Fairywrens. Emu 120, 313-321.
DOI Google Scholar

Hoyt, D.F., 1979. Practical methods of estimating volume and fresh weight of bird eggs. Auk 96, 73-77.
Google Scholar

Ibanez-Alamo, J.D., Soler, M., 2010. Does urbanization affect selective pressures and life-history strategies in the common blackbird (Turdus merula L.)? Biol. J. Linn. Soc. 101, 759-766.
DOI Google Scholar

Kettel, E.F., Gentle, L.K., Quinn, J.L., Yarnell, R.W., 2018. The breeding performance of raptors in urban landscapes: a review and meta-analysis. J. Ornithol. 159, 1–18.
DOI Google Scholar

Kumar, V., Sharma, A., Tripathi, V., 2022. Physiological effects of food availability times in higher vertebrates. J. Exp. Biol. 225, jeb239004.
DOI Google Scholar

Lack, D., 1947. The significance of clutch-size. Ibis 89, 302-352.
DOI Google Scholar

Lan, S.S., Zhang, Q., Huang, Q., Chen, S., 2013. Breeding ecology of Chinese Bulbul in the urban environment of Hangzhou, China. Zool. Res. 34, 182-189.
Google Scholar

Lewis, K.P., 2004. How important is the statistical approach for analysing categorical data? A critique using artificial nests. Oikos 104, 305-315.
DOI Google Scholar

Lothery, C.J., Thompson, C.F., Lawler, M.L., Sakaluk, S.K., 2014. Food supplementation fails to reveal a trade-off between incubation and self-maintenance in female House Wrens. PLoS One 9, e106260.
DOI Google Scholar

Lowry, H., Lill, A., Wong, B.B., 2013. Behavioural responses of wildlife to urban environments. Biol. Rev. 88, 537-549.
DOI Google Scholar

Martin, T.E., 1987. Food as a limit on breeding birds: a life-history perspective. Ann. Rev. Ecol. Syst. 18, 453-487.
DOI Google Scholar

Martin, T.E., 2004. Avian life-history evolution has an eminent past: does it have a bright future? Auk 121, 289-301.
DOI Google Scholar
Marzluff, J.M., Bowman, R., Donelly, R., 2001. A historical perspective on urbanbirdresearch: trends, terms, and approaches. In: Marzluff, J.M., Bowman, R., Donelly, R. (Eds.), Avian Ecology and Conservation in an Urbanizing World. KluwerAcademic Publishers, Boston, pp. 1–17.
DOI

McDonnell, M.J., Pickett, S.T.A., 1990, Ecosystem structure and function along urban-rural gradients: an unexploited opportunity for ecology. Ecology 71, 1232-1237.
DOI Google Scholar

Miller, J., Hobbs, R., 2002. Conservation where people live and work. Conserv. Biol. 16, 330-337.
DOI Google Scholar

Millon, A., Arroyo, B.E., Bretagnolle, V., 2008. Variable but predictable prey availability affects predator breeding success: natural versus experimental evidence. J. Zool. 275, 349-358.
DOI Google Scholar

Morgan, D.K.J., Waas, J.R., Innes, J., Fitzgerald, N., 2011. Identification of nest predators using continuous time-lapse recording in a New Zealand city. New Zealand J. Zool. 38, 343-347.
DOI Google Scholar

Nana, E.D., Sedlacek, O., Vokurkova, J., Horak, D., 2014. Nest position and type affect predation rates of artificial avian nests in the tropical lowland forest on Mount Cameroon. Ostrich 85, 93-96.
DOI Google Scholar

Partecke, J., Schwabl, I., Gwinner, E., 2006. Stress and the city: urbanization and its effects on the stress physiology in European blackbirds. Ecology 87, 1945-1952.
DOI Google Scholar

Patankar, S., Jambhekar, R., Suryawanshi, K.R., Nagendra, H., 2021. Which traits influence bird survival in the city? A Review. Land 10, 92.
DOI Google Scholar

Peach, W.J., Vincent, K.E., Fowler, J.A., Grice, P.V., 2008. Reproductive success of House Sparrows along an urban gradient. Anim. Conserv. 11, 493-503.
DOI Google Scholar
R Core Team, 2021. R: a Language and Environment for Statistical Computing. RFoundation for Statistical Computing, Vienna. URL. https://www.R-project.org/.

Ricklefs, R., 1969. Analysis of nesting mortality in birds. Smithsonian Contrib. Zool. 9, 1-48.
DOI Google Scholar

Robinson, W.D., Robinson, T.R., Robinson, S.K., Brawn, J.D., 2000. Nesting success of understory forest birds in central Panama. J. Avian Biol. 31, 151-164.
DOI Google Scholar

Roper, J.J., Sullivan, K.A., Ricklefs, R.E., 2010. Avoid nest predation when predation rates are low, and other lessons: testing the tropical-temperate nest predation paradigm. Oikos 119, 719-729.
DOI Google Scholar

Seress, G., Sandor, 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 Google Scholar

Sepp, T., McGraw, K.J., Kaasik, A., Giraudeau, M., 2017. A review of urban impacts on avian life-history evolution: does city living lead to slower pace of life? Global Change Biol. 24, 1452-1469.
DOI Google Scholar

Shochat, E., Warren, P.S., Faeth, S.H., McIntyre, N.E., Hope, D., 2006. From patterns to emerging processes in mechanistic urban ecology. Trends Ecol. Evol. 21, 187-191.
DOI Google Scholar

Slabbekoorn, H., Peet, M., 2003. Birds sing at a higher pitch in urban noise. Nature 424, 267.
DOI Google Scholar

Tryjanowski, P., Sparks, T.H., Kuzniak, S., Czechowski, P., Jerzak, L., 2013. Bird migration advances more strongly in urban environments. PLoS One 8, e63482.
DOI Google Scholar

Tuzun, N., de Beeck, L.O., Brans, K.I., Janssens, L., Stoks, R., 2017, Microgeographic differentiation in thermal performance curves between rural and urban populations of an aquatic insect. Evol. Appl. 10, 1067-1075.
DOI Google Scholar

van Doren, B.M., Horton, K.G., Dokter, A.M., Klinck, H., Elbin, S.B., Farnsworth, A., et al., 2017. High-intensity urban light installation dramatically alters nocturnal bird migration. P. Nat. Acad. Sci. USA 114, 11175-11180.
DOI Google Scholar

Vincze, E., Seress, G., Lagisz, M., Nakagawa, S., Dingemanse, N.J., Sprau, P., et al., 2017. Does urbanization affect predation of bird nests? A meta-analysis. Front. Ecol. Evol. 5, 29.
DOI Google Scholar
Wang, Y., 2003. A Study of the Adaptability of Birds to Urbanization. Master’s Thesis..Zhejiang University, Hangzhou.

Wang, Y., Chen, S., Ding, P., 2004. Flush distance: birds tolerance to human intrusion in Hangzhou. Zool. Res. 25, 214-220.
Google Scholar

Wang, Y., Chen, S., Jiang, P., Ding, P., 2008. Black-billed Magpies (Pica Pica) adjust nest characteristics to adapt to urbanization in Hangzhou, China. Can. J. Zool. 86, 676-684.
DOI Google Scholar

Wang, Y., Chen, S., Blair, R.B., Jiang, P., Ding, P., 2009. Nest composition adjustments by Chinese Bulbuls (Pycnonotus Sinensis) in an urbanized landscape of Hangzhou (E China). Acta Ornithol. 44, 185-192.
DOI Google Scholar

Wang, Y., Ding, P., Chen, S., Zheng, G., 2013. Nestedness of bird assemblages on urbanwoodlots: implications for conservation. Lands. Urban Plan. 111, 59-67.
DOI Google Scholar

Wang, Y., Song, Y., Zhong, Y., Chen, C., Zhao, Y., Zeng, D., et al., 2021. A dataset on the life-history and ecological traits of Chinese birds. Biodivers. Sci. 29, 1149-1153. (in Chinese).
DOI Google Scholar

Yang, X., Tan, X., Chen, C., Wang, Y., 2020. The influence of urban park characteristics on bird diversity in Nanjing, China. Avian Res. 11, 45.
DOI Google Scholar

Young, C.M., Cain, K.E., Svedin, N., Backwell, P.R.Y., Pryke, S.R., 2017. Nesting success in Crimson Finches: chance or choice? Ethology 123, 41-50.
DOI Google Scholar
Zar, J.H., 1999. Biostatistic Analysis, fourth ed. Prentice Hall Inc., Upper Saddle River, New Jersey.
Zhang, Q., 2014. Responses of Life History Traits of Chinese Bulbul to Urbanization.Master’s Thesis.. Zhejiang Normal University, Jinhua.
Zhuge, Y., 1990. Fauna of Zhejiang: Aves. Zhejiang Science and Technology Press, Hangzhou.
Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 01 November 2022
Revised: 23 March 2023
Accepted: 28 March 2023
Published: 07 April 2023
Issue date: June 2023

Copyright

© 2023 The Authors.

Acknowledgements

Acknowledgements

We are grateful for Tengda Zhu, Yafei Ma, Jianwei Zhou, Chao Chen, Xiang Yu, Wen Xu, Mingming Hu and Chenchen Zhu for their field assistance in finding and monitoring bird nests. We thank two anonymous reviewers for their helpful comments on the manuscript.

Rights and permissions

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return