Effects of urbanization on animals: From community to individual level

doi:10.17520/biods.2023489

Abstract

Abstract:

Background & Aims: Urbanization is a global process accompanied by rapid environmental changes, which accelerates the evolutionary process of urban organisms and reshapes community structure and species interactions in urban ecosystems. In this paper, we reviewed relevant researches on the effects of urbanization on animals at community, population, and individual level. Then we summarized both the advances and shortcomings in the scientific urbanization literature. Finally, we provided an outlook for research in the related fields.

Review Results: Currently, relevant studies primarily reflect the level of urbanization by using the proportion of impervious area or the urban-rural gradient. By replacing time with space, the studies explore the changing trend of species composition and diversity, population demographics, genetic structure of animals, biological traits, phenology, and behavior under urbanization. Most studies focus on descriptive analysis, while mechanism-based research and applied research are relatively lacking.

Prospect: (1) Based on the observed phenomena under urbanization, future studies should conduct controlled experiments to identify the key factors affecting different animals under urbanization and explore the molecular genetic basis of urban biological evolution with molecular methods. (2) Particular attention needs to be paid to adaptive species in urban grey habitats, which are often associated with humans, pets, or food. Understanding how urban species adapt may provide direction and help predict the future effects of urbanization on animals, including human beings. (3) Since complex interspecific interaction networks can buffer the impacts of the change of animal abundance and behavior on ecological services such as pollination, seed dispersal, and pest control to a certain extent, the effects of urbanization on multitrophic networks should be studied further. (4) Finally, basic research on animal diversity and genetic structure should be extended to urban ecological planning and restoration.

Key words: urbanization, adaptation, species diversity, interspecific relationship, traits

Hongyu Niu, Lu Chen, Hengyue Zhao, Gulzar Abdukirim, Hongmao Zhang. Effects of urbanization on animals: From community to individual level[J]. Biodiv Sci, 2024, 32(8): 23489.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.biodiversity-science.net/EN/10.17520/biods.2023489

https://www.biodiversity-science.net/EN/Y2024/V32/I8/23489

Figures/Tables 1

References 75

[1]	Altermatt F, Ebert D (2016) Reduced flight-to-light behaviour of moth populations exposed to long-term urban light pollution. Biology Letters, 12, 20160111.
[2]	Amaya-Espinel JD, Hostetler M, Henriquez C, Bonacic C (2019) The influence of building density on Neotropical bird communities found in small urban parks. Landscape and Urban Planning, 190, 103578.
[3]	Angilletta MJ Jr, Wilson RS, Niehaus AC, Sears MW, Navas CA, Ribeiro PL (2007) Urban physiology: City ants possess high heat tolerance. PLoS ONE, 2, e258.
[4]	Azhar B, Razi N, Sanusi R, Lechner A, Ashraf M, Zaki WMW, Jafni F (2024) Vegetation structure and relative humidity drive the diurnal foraging activity of Malaysian giant ant workers in urban fragmented forests. Insect Conservation and Diversity, 17, 334-344.
[5]	Biondi LM, Fuentes GM, Córdoba RS, Bó MS, Cavalli M, Paterlini CA, Castano MV, García GO (2020) Variation in boldness and novelty response between rural and urban predatory birds: The chimango caracara, Milvago chimangoas study case. Behavioural Processes, 173, 104064.
[6]	Brans KI, Jansen M, Vanoverbeke J, Tüzün N, Stoks R, de Meester L (2017) The heat is on: Genetic adaptation to urbanization mediated by thermal tolerance and body size. Global Change Biology, 23, 5218-5227. DOI PMID
[7]	Breitbart S, Tomchyshyn A, Wagner HH, Johnson MTJ (2023) Urbanization and a green corridor influence reproductive success and pollinators of common milkweed. Urban Ecosystems, 26, 31-43.
[8]	Capilla-Lasheras P, Thompson MJ, Sanchez-Tojar A, Haddou Y, Branston CJ, Reale D, Charmantier A, Dominoni DM (2022) A global meta-analysis reveals higher variation in breeding phenology in urban birds than in their non-urban neighbours. Ecology Letters, 25, 2552-2570. DOI PMID
[9]	Chen SH, Liu Y, Patrick SC, Goodale E, Safran RJ, Pagani-Núñez E (2023) A multidimensional framework to quantify the effects of urbanization on avian breeding fitness. Ecology and Evolution, 13, e10259.
[10]	Cheng JM, He HM, Niu HY, Zhang HM (2023) Research progress on the effect of intraspecific personality differences on seed dispersal in rodents. Biodiversity Science, 31, 22446. (in Chinese with English abstract) DOI
	[程继铭, 何慧敏, 牛红玉, 张洪茂 (2023) 鼠类种内个性差异对种子传播影响的研究进展. 生物多样性, 31, 22446.] DOI
[11]	Cheng ZB, Zhong ZY, Bai JD, Duan JB, Guo G, Meng YP, Shan YF, Li YK, Xu L, Guo XX, Pan QQ, Wang LB (2023) Bird biodiversity increased with the area of urban green spaces expanding after 40 years of tree planting in Beijing. Ecosystem Health and Sustainability, 9, 0068.
[12]	Chick LD, Strickler SA, Perez A, Martin RA, Diamond SE (2019) Urban heat islands advance the timing of reproduction in a social insect. Journal of Thermal Biology, 80, 119-125. DOI PMID
[13]	DeCandia AL, Brzeski KE, Heppenheimer E, Caro CV, Camenisch G, Wandeler P, Driscoll C, vonHoldt BM (2019) Urban colonization through multiple genetic lenses: The city-fox phenomenon revisited. Ecology and Evolution, 9, 2046-2060.
[14]	Deng ZD, Ding ZF, Zeng XY, Zhang CL, Li XE, He ZQ, Liang JC, Hu HJ (2023) Landscape characteristics of urban green spaces and their effects on bird diversity: The case of Guangzhou. Sichuan Journal of Zoology, 42, 568-578. (in Chinese with English abstract)
	[邓卓迪, 丁志锋, 曾小悦, 张春兰, 李孝恩, 何子晴, 梁健超, 胡慧建 (2023) 广州城市绿地景观特征及其对鸟类多样性的影响. 四川动物, 42, 568-578.]
[15]	DePasquale C, Li X, Harold M, Mueller S, McLaren S, Mahan C (2020) Selection for increased cranial capacity in small mammals during a century of urbanization. Journal of Mammalogy, 101, 1706-1710.
[16]	Dominoni DM, Quetting M, Partecke J (2013) Artificial light at night advances avian reproductive physiology. Proceeding of the Royal Society B: Biological Sciences, 280, 20123017.
[17]	Dunn RR, Burger JR, Carlen EJ, Koltz AM, Light JE, Martin RA, Munshi-South J, Nichols LM, Vargo EL, Yitbarek S, Zhao Y, Cibrian-Jaramillo A (2022) A theory of city biogeography and the origin of urban species. Frontiers in Conservation Science, 3, 761449.
[18]	Ellis EE, Edmondson JL, Maher KH, Hipperson H, Campbell SA (2023) Negative effects of urbanisation on diurnal and nocturnal pollen-transport networks. Ecology Letters, 26, 1382-1393. DOI PMID
[19]	Fattorini S, Mantoni C, de Simoni L, Galassi DMP (2018) Island biogeography of insect conservation in urban green spaces. Environmental Conservation, 45, 1-10.
[20]	Fisogni A, Hautekèete N, Piquot Y, Brun M, Vanappelghem C, Ohlmann M, Franchomme M, Hinnewinkel C, Massol F (2022) Seasonal trajectories of plant-pollinator interaction networks differ following phenological mismatches along an urbanization gradient. Landscape and Urban Planning, 226, 104512.
[21]	Fortuna MA, Bascompte J (2006) Habitat loss and the structure of plant-animal mutualistic networks. Ecology Letters, 9, 278-283.
[22]	Franzén M, Betzholtz PE, Pettersson LB, Forsman A (2020) Urban moth communities suggest that life in the city favours thermophilic multi-dimensional generalists. Proceedings of the Royal Society B: Biological Sciences, 287, 20193014.
[23]	Gao YH, Yu JP, Zhou L, Bao R, Gao JF (2018) Breeding behavior of wild spotted doves in urban area of Wuhan, China. Chinese Journal of Wildlife, 39, 689-692. (in Chinese with English abstract)
	[高翊航, 于锦萍, 周立, 包容, 高建峰 (2018) 武汉城区野生珠颈斑鸠繁殖生态学初步研究. 野生动物学报, 39, 689-692.]
[24]	González-Varo JP, Carvalho CS, Arroyo JM, Jordano P (2017) Unravelling seed dispersal through fragmented landscapes: Frugivore species operate unevenly as mobile links. Molecular Ecology, 26, 4309-4321. DOI PMID
[25]	Hahs AK, Fournier B, Aronson MFJ, Nilon CH, Herrera- Montes A, Salisbury AB, Threlfall CG, Rega-Brodsky CC, Lepczyk CA, La Sorte FA, Macgregor-Fors I, Macivor JS, Jung K, Piana MR, Williams NSG, Knapp S, Vergnes A, Acevedo AA, Gainsbury AM, Rainho A, Hamer AJ, Shwartz A, Voigt CC, Lewanzik D, Lowenstein DM, O’Brien D, Tommasi D, Pineda E, Carpenter ES, Belskaya E, Lövei GL, Makinson JC, Coleman JL, Sadler JP, Shroyer J, Shapiro JT, Baldock KCR, Ksiazek-Mikenas K, Matteson KC, Barrett K, Siles L, Aguirre LF, Armesto LO, Zalewski M, Herrera-Montes MI, Obrist MK, Tonietto RK, Gagné SA, Hinners SJ, Latty T, Surasinghe TD, Sattler T, Magura T, Ulrich W, Elek Z, Castañeda-Oviedo J, Torrado R, Kotze DJ, Moretti M (2023) Urbanisation generates multiple trait syndromes for terrestrial animal taxa worldwide. Nature Communications, 14, 4751. DOI PMID
[26]	Hantak MM, McLean BS, Li DJ, Guralnick RP (2021) Mammalian body size is determined by interactions between climate, urbanization, and ecological traits. Communications Biology, 4, 972. DOI PMID
[27]	Hastedt A, Tietze DT (2023) The importance of unsealed areas in the urban core and periphery for bird diversity in a large central European city. Urban Ecosystems, 26, 1015-1028.
[28]	Herr J, Schley L, Engel E, Roper TJ (2010) Den preferences and denning behaviour in urban stone martens (Martes foina). Mammalian Biology, 75, 138-145.
[29]	Hope SF, Stabile FA, Butler LK (2016) Urban living alters moult dynamics in a passerine. Journal of Avian Biology, 47, 304-311.
[30]	Hurtado G, Mabry KE (2019) Genetic structure of an abundant small mammal is influenced by low intensity urbanization. Conservation Genetics, 20, 705-715.
[31]	Kharouba HM, Ehrlen J, Gelman A, Bolmgren K, Allen JM, Travers SE, Wolkovich EM (2018) Global shifts in the phenological synchrony of species interactions over recent decades. Proceedings of the National Academy of Sciences, USA, 115, 5211-5216.
[32]	Kucera AJ, Smith MC, Wagnon GS, Cantwell C, Eaton-Clark A, Elliott B, Ghanem L, Ko E, Waggener M, Brown CR (2019) Group size and singing phenology of northern cardinals (Cardinalis cardinalis) varies between urban and rural habitats. Southwestern Naturalist, 64, 56-60.
[33]	Lan FY, Ma XJ, Lu JY, Li YG, Chai RS, Li X, Luo YO, Zhang YZ, Ye ZL, Fu CJ, Bao WS, Li L, Xing XY (2021) Effects of urbanization on bird nesting: A review. Biodiversity Science, 29, 1539-1553. (in Chinese with English abstract) DOI
	[蓝方源, 马行健, 逯金瑶, 李雨果, 柴汝松, 李翔, 罗亦欧, 张宇泽, 叶子凌, 付昌健, 暴文爽, 李立, 邢晓莹 (2021) 城市化对鸟类筑巢的影响. 生物多样性, 29, 1539-1553.] DOI
[34]	Li B, Zhang W, Shu XX, Pei EL, Yuan X, Sun YJ, Wang TH, Wang ZH (2016) The impacts of urbanization on the distribution and body condition of the rice-paddy frog (Fejervarya multistriata) and gold-striped pond frog (Pelophylax plancy) in Shanghai, China. Asian Herpetological Research, 7, 200-209.
[35]	Li TY, Liu YM, Wang DL, Zhong ZW (2022) Concepts, research progresses and prospects of animal personality. Acta Ecologica Sinica, 42, 37-44. (in Chinese with English abstract)
	[李天韵, 刘依明, 王德利, 钟志伟 (2022) 动物个性研究进展. 生态学报, 42, 37-44.]
[36]	Liang H, He YD, Theodorou P, Yang CF (2023) The effects of urbanization on pollinators and pollination: A meta-analysis. Ecology Letters, 26, 1629-1642. DOI PMID
[37]	Liu Z, He C, Wu J (2016) The relationship between habitat loss and fragmentation during urbanization: An empirical evaluation from 16 world cities. PLoS ONE, 11, e0154613.
[38]	Lourenco A, Alvarez D, Wang IJ, Velo-Anton G (2017) Trapped within the city: Integrating demography, time since isolation and population-specific traits to assess the genetic effects of urbanization. Molecular Ecology, 26, 1498-1514. DOI PMID
[39]	McKinney ML (2002) Urbanization, biodiversity, and conservation. BioScience, 52, 883-890.
[40]	McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biological Conservation, 127, 247-260.
[41]	Merckx T, Kaiser A, van Dyck H (2018a) Increased body size along urbanization gradients at both community and intraspecific level in macro-moths. Global Change Biology, 24, 3837-3848.
[42]	Merckx T, Souffreau C, Kaiser A, Baardsen LF, Backeljau T, Bonte D, Brans KI, Cours M, Dahirel M, Debortoli N, de Wolf K, Engelen JMT, Fontaneto D, Gianuca AT, Govaert L, Hendrickx F, Higuti J, Lens L, Martens K, Matheve H, Matthysen E, Piano E, Sablon R, Schon I, van Doninck K, de Meester L, van Dyck H (2018b) Body-size shifts in aquatic and terrestrial urban communities. Nature, 558, 113-116.
[43]	Merckx T, van Dyck H (2019) Urbanization-driven homogenization is more pronounced and happens at wider spatial scales in nocturnal and mobile flying insects. Global Ecology and Biogeography, 28, 1440-1455.
[44]	Moller AP, Diaz M, Grim T, Dvorska A, Flensted-Jensens E, Ibanez-Alamo JD, Jokimaki J, Maend R, Marko G, Szymanski P, Tryjanowski P (2015) Effects of urbanization on bird phenology: A continental study of paired urban and rural populations. Climate Research, 66, 185-199.
[45]	Moller AP, Jokimaki J, Skorka P, Tryjanowski P (2014) Loss of migration and urbanization in birds: A case study of the blackbird (Turdus merula). Oecologia, 175, 1019-1027. DOI PMID
[46]	Munoz-Pacheco CB, Villasenor NR (2023) Is there a relationship between socioeconomic level, vegetation cover, free-roaming cats and dogs, and the diversity of native birds? A study in a Latin American capital city. Science of the Total Environment, 891, 164378.
[47]	Neate-Clegg MHC, Tonelli BA, Youngflesh C, Wu JX, Montgomery GA, Sxekercioglu CH, Tingley MW (2023) Traits shaping urban tolerance in birds differ around the world. Current Biology, 33, 1677-1688.
[48]	Niu HY, Wang XR, Wu SQ, Xing JJ, Peng C, Chen ZW, Li YC, Zhang HM (2021) Granivorous rodent loss poses greater threats to oak trees with large acorns than those with small ones in urban forests. Urban Forestry & Urban Greening, 62, 127185.
[49]	Patankar S, Jambhekar R, Suryawanshi KR, Nagendra H (2021) Which traits influence bird survival in the city? A review. Land, 10, 92.
[50]	Pfeiffer V, Crowder DW, Silbernagel J (2023) Urban development reduces bee abundance and diversity. Urban Ecosystems, 26, 1535-1544.
[51]	Piano E, Souffreau C, Merckx T, Baardsen LF, Backeljau T, Bonte D, Brans KI, Cours M, Dahirel M, Debortoli N, Decaestecker E, de Wolf K, Engelen JMT, Fontaneto D, Gianuca AT, Govaert L, Hanashiro FTT, Higuti J, Lens L, Martens K, Matheve H, Matthysen E, Pinseel E, Sablon R, Schön I, Stoks R, van Doninck K, van Dyck H, Vanormelingen P, van Wichelen J, Vyverman W, de Meester L, Hendrickx F (2020) Urbanization drives cross-taxon declines in abundance and diversity at multiple spatial scales. Global Change Biology, 26, 1196-1211. DOI PMID
[52]	Pike M, Spennemann DHR, Watson MJ (2017) Building use by urban commensal avifauna in Melbourne central business district, Australia. Emu-Austral Ornithology, 117, 284-289.
[53]	Putman BJ, Gasca M, Blumstein DT, Pauly GB (2019) Downsizing for downtown: Limb lengths, toe lengths, and scale counts decrease with urbanization in western fence lizards (Sceloporus occidentalis). Urban Ecosystems, 22, 1071-1081.
[54]	Putman BJ, Tippie ZA (2020) Big city living: A global meta- analysis reveals positive impact of urbanization on body size in lizards. Frontiers in Ecology and Evolution, 8, 580745.
[55]	Schlaepfer DR, Braschler B, Rusterholz HP, Baur B (2018) Genetic effects of anthropogenic habitat fragmentation on remnant animal and plant populations: A meta-analysis. Ecosphere, 9, e02488.
[56]	Schmidt C, Domaratzki M, Kinnunen RP, Bowman J, Garroway CJ (2020) Continent-wide effects of urbanization on bird and mammal genetic diversity. Proceedings of the Royal Society B: Biological Sciences, 287, 20192497.
[57]	Schneiberg I, Boscolo D, Devoto M, Marcilio-Silva V, Dalmaso CA, Ribeiro JW, Ribeiro MC, de Camargo Guaraldo A, Niebuhr BB, Varassin IG (2020) Urbanization homogenizes the interactions of plant-frugivore bird networks. Urban Ecosystems, 23, 457-470.
[58]	Schuett W, Delfs B, Haller R, Kruber S, Roolfs S, Timm D, Willmann M, Drees C (2018) Ground beetles in city forests: Does urbanization predict a personality trait? PeerJ, 6, e4360.
[59]	Seki Y, Hara K, Minami Y (2024) The use of seismically isolated buildings by urban wildlife in Japan. Journal of Veterinary Medical Science, 86, 290-294. DOI PMID
[60]	Seress G, Hammer T, Bókony V, Vincze E, Preiszner B, Pipoly I, Sinkovics C, Evans KL, Liker A (2018) Impact of urbanization on abundance and phenology of caterpillars and consequences for breeding in an insectivorous bird. Ecological Applications, 28, 1143-1156. DOI PMID
[61]	Sharma S, Amritphale D (2007) Effect of urbanization on the population density of aak weevil. Current Science, 93, 1130-1134.
[62]	Souza FL, Valente-Neto F, Severo-Neto F, Bueno B, Ochoa-Quintero JM, Laps RR, Bolzan F, de Oliveira Roque F (2019) Impervious surface and heterogeneity are opposite drivers to maintain bird richness in a Cerrado city. Landscape and Urban Planning, 192, 103643.
[63]	Tee SL, Samantha LD, Kamarudin N, Akbar Z, Lechner AM, Ashton-Butt A, Azhar B (2018) Urban forest fragmentation impoverishes native mammalian biodiversity in the tropics. Ecology and Evolution, 8, 12506-12521. DOI PMID
[64]	Theodorou P, Radzeviciute R, Kahnt B, Soro A, Grosse I, Paxton RJ (2018) Genome-wide single nucleotide polymorphism scan suggests adaptation to urbanization in an important pollinator, the red-tailed bumblebee (Bombus lapidarius L.). Proceedings of the Royal Society B: Biological Sciences, 285, 20172806.
[65]	Trentanovi G, von der Lippe M, Sitzia T, Ziechmann U, Kowarik I, Cierjacks A, Pyšek P (2013) Biotic homogenization at the community scale: Disentangling the roles of urbanization and plant invasion. Diversity and Distributions, 19, 738-748.
[66]	van Dis NE, Sieperda GJ, Bansal V, van Lith B, Wertheim B, Visser ME (2023) Phenological mismatch affects individual fitness and population growth in the winter moth. Proceedings of the Royal Society B: Biological Sciences, 290, 20230414.
[67]	van Geffen KG, van Eck E, de Boer RA, Salis L, Berendse F, Veenendaal EM (2015) Artificial light at night inhibits mating in a Geometrid moth. Insect Conservation and Diversity, 8, 282-287.
[68]	van Langevelde F, Veenendaal EM, Fijen TPM (2017) Artificial night lighting inhibits feeding in moths. Biology Letters, 13, 20160874.
[69]	Vaz S, Manes S, Khattar G, Mendes M, Silveira L, Mendes E, Rodrigues ED, Gama-Maia D, Loo M, Paiva PC (2023) Global meta-analysis of urbanization stressors on insect abundance, richness, and traits. Science of the Total Environment, 903, 165967.
[70]	Vizentin-Bugoni J, Tarwater CE, Foster JT, Drake DR, Gleditsch JM, Hruska AM, Kelley JP, Sperry JH (2019) Structure, spatial dynamics, and stability of novel seed dispersal mutualistic networks in Hawai‘i. Science, 364, 78-82. DOI PMID
[71]	Wang QW, Zhao HY, Liu Q, Wan N, Zhu ZB, Niu HY, Zhang HM (2023) Mammal diversity in the forest fragments of Wuhan City. Acta Theriologica Sinica, 43, 258-269. (in Chinese with English abstract) DOI
	[汪琪薇, 赵恒月, 刘勤, 万能, 朱志兵, 牛红玉, 张洪茂 (2023) 武汉市城市破碎化森林中野生哺乳动物的多样性. 兽类学报, 43, 258-269.] DOI
[72]	Wang YC, Lu XH, Wang RJ (2023) Influence of green spaces in central area of Shanghai on bird diversity and its marginal effect. Journal of Chinese Urban Forests, 21(4), 1-7. (in Chinese with English abstract)
	[王云才, 卢星昊, 王若静 (2023) 上海主城区绿地对鸟类多样性的影响及其边际效应. 中国城市林业, 21(4), 1-7.]
[73]	Wilson A, Fenton B, Malloch G, Boag B, Hubbard S, Begg G (2016) Urbanisation versus agriculture: A comparison of local genetic diversity and gene flow between wood mouse Apodemus sylvaticus populations in human-modified landscapes. Ecography, 39, 87-97.
[74]	Zhou DC, Zhao SQ, Zhang LX, Liu SG (2016) Remotely sensed assessment of urbanization effects on vegetation phenology in China’s 32 major cities. Remote Sensing of Environment, 176, 272-281.
[75]	Ziemianski MA, Zych M (2016) Pollination biology of the urban populations of an ancient forest, spring ephemeral plant. Acta Societatis Botanicorum Poloniae, 85, 3489.