Diet and habitat selection of raccoon dogs (Nyctereutes procyonoides) in Shanghai, a rapidly urbanizing megacity in eastern China

doi:10.17520/biods.2024131

Abstract

Abstract:

Aims: Species with high behavioral plasticity are able to utilize resources in urban environments, successfully colonizing and adapting to cities. Researching key behavioral changes in carnivorous species, such as foraging behavior and habitat selection, helps our understanding of how species respond to urban environments. This study focused on raccoon dogs (Nyctereutes procyonoides) in Shanghai with the objective to (1) understand the food composition of raccoon dogs and how raccoon dogs adjust their feeding strategies to respond to urban environments in Shanghai, and (2) evaluate how raccoon dogs change their habitat selection within their home range when colonizing urban environments.

Methods: We sampled from May 2021 to December 2023 in two different urbanized environments of Shanghai: highly urbanized residential environments (residential areas) and semi-natural habitats (forest parks) with lower urbanization. Fecal samples were collected, processed, and analyzed using logistic regression and Chi square tests to measure differences in food components. Wildlife bio-trackers were used to collect raccoon dog activity data, and autocorrelated kernel density estimation was used to approximate their home range. Finally, a resource selection function was developed to evaluate raccoon dog habitat selection within their home ranges.

Results: A total of 568 fecal samples were processed, and logistic regression results showed that raccoon dogs in residential areas ate significantly more human-derived products (P < 0.001) and mammals (P < 0.01) compared with raccoon dogs living in less urbanized forest parks. A total of 32 individuals were collared, and tracked with satellite positioning, and results from a resource selection function revealed that while raccoon dogs in forest parks avoided buildings within their home range (β = -0.222), those in residential areas selected for buildings within their home range (β = 0.021).

Conclusion: This study provides the first assessment of behavioral changes of raccoon dogs in urban environments within Shanghai, including their habitat selection and feeding tendencies, which revealed their behavioral plasticity. Based on these results, we propose adaptive management strategies to reduce human-derived food consumption through community-based urban wildlife conservation planning. Long-term assessment of raccoon dog behavior is needed to further elucidate how raccoon dogs respond to urban environments, and to provide information for ecology-based protection and management of urban wildlife.

Key words: urban animals, urbanization, behavioral plasticity, diets, habitat selection

Jiaqi Li, Yidi Feng, Lei Wang, Penyan Pan, Xiaoru Liu, Xueyang Li, Yihan Wang, Fang Wang. Diet and habitat selection of raccoon dogs (Nyctereutes procyonoides) in Shanghai, a rapidly urbanizing megacity in eastern China[J]. Biodiv Sci, 2024, 32(8): 24131.

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URL: https://www.biodiversity-science.net/EN/10.17520/biods.2024131

https://www.biodiversity-science.net/EN/Y2024/V32/I8/24131

Figures/Tables 5

References 44

[1]	Adams CE (2009) Urban Wildlife Management, 2nd edn. CRC Press, Boca Raton.
[2]	Adjei IA, Karim R (2016) An application of bootstrapping in logistic regression model. Open Access Library Journal, 3, 1-9.
[3]	Anwar MB, Nadeem MS, Kayani AR, Mazhar Q (2011) Is mammalian hair fiber analysis by optical fiber diameter analyzer helpful to identify prey from scats of carnivores? Pakistan Journal of Zoology, 43, 1218-1220.
[4]	Bateman PW, Fleming PA (2012) Big city life: Carnivores in urban environments. Journal of Zoology, 287, 1-23.
[5]	Blair RB, Launer AE (1997) Butterfly diversity and human land use: Species assemblages along an urban gradient. Biology Conservation, 80, 113-125.
[6]	Bozdogan H (1987) Model selection and Akaike’s information criterion (AIC): The general theory and its analytical extensions. Psychometrika, 52, 345-370.
[7]	Bozek CK, Prange S, Gehrt SD (2007) The influence of anthropogenic resources on multi-scale habitat selection by raccoons. Urban Ecosystems, 10, 413-425.
[8]	Buonaccorsi JP, Romeo G, Thoresen M (2018) Model-based bootstrapping when correcting for measurement error with application to logistic regression. Biometrics, 74, 135-144. DOI PMID
[9]	Calabrese JM, Fleming CH, Gurarie E (2016) ctmm: An R package for analyzing animal relocation data as a continuous- time stochastic process. Methods in Ecology and Evolution, 7, 1124-1132.
[10]	Campbell SJ, Ashley W, Gil-Fernandez M, Newsome TM, Di Giallonardo F, Ortiz-Baez AS, Mahar JE, Towerton AL, Gillings M, Holmes EC, Carthey AJR, Geoghegan JL (2020) Red fox viromes in urban and rural landscapes. Virus Evolution, 6, veaa065.
[11]	Cui YY, Xie ZG, Xu X, Chu KL, Jiang WZ, Pei EL, Yuan X, Xu HF (2013) Activity laws and feeding behavior of introduced badgers. Journal of Anhui Agricultural Science, 41, 3407-3409. (in Chinese with English abstract)
	[崔勇勇, 谢志刚, 徐循, 褚可龙, 蒋文忠, 裴恩乐, 袁晓, 徐宏发 (2013) 引入狗獾活动规律和取食行为的研究. 安徽农业科学, 41, 3407-3409.]
[12]	Diao YX, Zhao QQ, Weng Y, Huang ZX, Wu YQ, Gu BJ, Zhao Q, Wang F (2022) Predicting current and future species distribution of the raccoon dog (Nyctereutes procyonoides) in Shanghai, China. Landscape and Urban Planning, 228, 104581.
[13]	Dong TW, Huang ML, Wei X, Ma S, Yue Q, Liu WL, Zheng JX, Wang G, Ma R, Ding YZ, Bo SQ, Wang ZH (2023) Potential spatial distribution pattern and landscape connectivity of Pelophylax plancyi in Shanghai, China. Biodiversity Science, 31, 22692. (in Chinese with English abstract)
	[董廷玮, 黄美玲, 韦旭, 马硕, 岳衢, 刘文丽, 郑佳鑫, 王刚, 马蕊, 丁由中, 薄顺奇, 王正寰 (2023) 上海地区金线侧褶蛙种群的潜在空间分布格局及其景观连通性. 生物多样性, 31, 22692.] DOI
[14]	Dorning J, Harris S (2019) Individual and seasonal variation in contact rate, connectivity and centrality in red fox (Vulpes vulpes) social groups. Scientific Reports, 9, 20095. DOI PMID
[15]	Drygala F, Werner U, Zoller H (2013) Diet composition of the invasive raccoon dog (Nyctereutes procyonoides) and the native red fox (Vulpes vulpes) in northeast Germany. Hystrix, 24, 190-194.
[16]	Fischer JD, Cleeton SH, Lyons TP, Miller JR (2012) Urbanization and the predation paradox: The role of trophic dynamics in structuring vertebrate communities. BioScience, 62, 809-818.
[17]	Guo XQ, Yu XY, Li ZR, Li ZC, Lü TT, Cao HX, Song HY, Zhao CF (2021) Isolation, identification and VP2 gene sequence analysis of raccoon dog parvovirus RDPV-JL3. Special Wild Economic Animal and Plant Research, 43(5), 13-18. (in Chinese with English abstract)
	[郭晓芹, 于小亚, 李滋睿, 李卓宸, 吕甜甜, 曹海旭, 宋海岩, 赵传芳 (2021) 貉细小病毒RDPV-JL3株的分离鉴定及VP2基因序列分析. 特产研究, 43(5), 13-18.]
[18]	Herr J (2008) Ecology and Behaviour of Urban Stone Martens (Martes foina) in Luxembourg. PhD dissertation, University of Sussex, Brighton.
[19]	Hubert P, Julliard R, Biagianti S, Poulle ML (2011) Ecological factors driving the higher hedgehog (Erinaceus europeaus) density in an urban area compared to the adjacent rural area. Landscape and Urban Planning, 103, 34-43.
[20]	Jia WH (2022) Key points of breeding and management techniques for raccoon dogs during breeding period. Special Economic Animals and Plants, 25(12), 52-59. (in Chinese with English abstract)
	[贾文会 (2022) 貉配种期的饲养管理技术要点. 特种经济动植物, 25(12), 52-59.]
[21]	Kirkland GL (1998) Guidelines for the Capture, Handling, and Care of Mammals as approved by the American Society of Mammalogists. Journal of Mammalogy, 79, 1416-1431.
[22]	Ladle A, Galpern P, Doyle-Baker P (2018) Measuring the use of green space with urban resource selection functions: An application using smartphone GPS locations. Landscape and Urban Planning, 179, 107-115.
[23]	Manly B, McDonald L, Thomas DL, McDonald TL, Erickson WP (2002) Resource Selection by Animals: Statistical Design and Analysis for Field Studies. Kluwer Academic Publishers, Dordrecht.
[24]	McKinney ML (2002) Urbanization, biodiversity, and conservation: The impacts of urbanization on native species are poorly studied, but educating a highly urbanized human population about these impacts can greatly improve species conservation in all ecosystems. BioScience, 52, 883-890.
[25]	Mukherjee F, Singh D (2020) Assessing land use-land cover change and its impact on land surface temperature using LANDSAT data: A comparison of two urban areas in India. Earth Systems and Environment, 4, 385-407.
[26]	Murray M, Cembrowski A, Latham ADM, Lukasik VM, Pruss S, St Clair CC (2015) Greater consumption of protein-poor anthropogenic food by urban relative to rural coyotes increases diet breadth and potential for human-wildlife conflict. Ecography, 38, 1235-1242.
[27]	Murray MH, Becker DJ, Hall RJ, Hernandez SM (2016) Wildlife health and supplemental feeding: A review and management recommendations. Biological Conservation, 204, 163-174.
[28]	Newsome SD, Garbe HM, Wilson EC, Gehrt SD (2015) Individual variation in anthropogenic resource use in an urban carnivore. Oecologia, 178, 115-128. DOI PMID
[29]	Newsome TM, Ballard GA, Crowther MS, Fleming PJS, Dickman CR (2014a) Dietary niche overlap of free-roaming dingoes and domestic dogs: The role of human-provided food. Journal of Mammalogy, 95, 392-403.
[30]	Newsome TM, Ballard GA, Fleming PJS, van de Ven R, Story GL, Dickman CR (2014b) Human-resource subsidies alter the dietary preferences of a mammalian top predator. Oecologia, 175, 139-150.
[31]	Prange S, Gehrt SD, Wiggers EP (2004) Influences of anthropogenic resources on raccoon (Procyon lotor) movements and spatial distribution. Journal of Mammalogy, 85, 483-490.
[32]	Redpath SM, Bhatia S, Young J (2015) Tilting at wildlife: Reconsidering human-wildlife conflict. Oryx, 49, 222-225.
[33]	Rodewald AD, Kearns LJ (2011) Shifts in dominant nest predators along a rural-to-urban landscape gradient. The Condor, 113, 899-906.
[34]	Šálek M, Drahníková L, Tkadlec E (2015) Changes in home range sizes and population densities of carnivore species along the natural to urban habitat gradient. Mammal Review, 45, 1-14.
[35]	Salmerón Gómez R, García Pérez J, López Martín MDM, García CG (2016) Collinearity diagnostic applied in ridge estimation through the variance inflation factor. Journal of Applied Statistics, 43, 1831-1849.
[36]	Schulte-Hostedde AI, Mazal Z, Jardine CM, Gagnon J (2018) Enhanced access to anthropogenic food waste is related to hyperglycemia in raccoons (Procyon lotor). Conservation Physiology, 6, coy026.
[37]	Tsunoda M, Kaneko Y, Sako T, Koizumi R, Iwasaki K, Mitsuhashi I, Saito MU, Hisano M, Newman C, Macdonald DW, Buesching CD (2019) Human disturbance affects latrine-use patterns of raccoon dogs. The Journal of Wildlife Management, 83, 728-736.
[38]	Turner J, Freeman R, Carbone C (2022) Using citizen science to understand and map habitat suitability for a synurbic mammal in an urban landscape: The hedgehog Erinaceus europaeus. Mammal Review, 52, 291-303.
[39]	Wang YH, Zhao QQ, Diao YX, Gu BJ, Weng Y, Zhang ZJ, Chen YB, Wang F (2023) Diel activity, habitat utilization, and response to anthropogenic interference of small Indian civets (Viverricula indica) in Shanghai urban areas based on camera trapping. Biodiversity Science, 31, 22294. (in Chinese with English abstract)
	[王怡涵, 赵倩倩, 刁奕欣, 顾伯健, 翁悦, 张卓锦, 陈泳滨, 王放 (2023) 基于红外相机调查上海市区小灵猫的活动节律、栖息地利用及其对人类活动的响应. 生物多样性, 31, 22294.] DOI
[40]	Wu T, Chu KL, Jiang WZ, Gu GL, Yuan X, Xu HF (2017) Setts habitat features of reintroduced Meles meles after release. Sichuan Journal of Zoology, 36, 94-99. (in Chinese with English abstract)
	[吴彤, 褚可龙, 蒋文忠, 顾国林, 袁晓, 徐宏发 (2017) 重引入狗獾释放后定居巢的生境特征. 四川动物, 36, 94-99.]
[41]	Zhang W, Li B, Shu XX, Pei EL, Yuan X, Sun YJ, Wang TH, Wang ZH (2016) Responses of anuran communities to rapid urban growth in Shanghai, China. Urban Forestry & Urban Greening, 20, 365-374.
[42]	Zhao QQ, Diao YX, Weng Y, Huang ZX, Gu BJ, Wu Y, Wang YH, Zhao Q, Wang F (2022) Predicting future distributions and dispersal pathways for precautionary management of human-raccoon dog conflicts in metropolitan landscapes. Environmental Research Letters, 17, 104036.
[43]	Zhao QQ, Wang YH, Wu LJ, Feng YD, Li YH, Zhang ZJ, Zhao Q, Wang F (2024) A path to human-raccoon dog harmony: Identifying factors influencing the tolerance of urban residents in Shanghai towards a neglected species. People and Nature, 6, 1277-1287.
[44]	Zhou XF, Chen H (2018) Impact of urbanization-related land use land cover changes and urban morphology changes on the urban heat island phenomenon. Science of the Total Environment, 635, 1467-1476.

模型构建 Model formula	与最佳模型的差值 ΔAIC	AIC 权重 AIC weight
居民住宅区 Residential areas
used ~ dis_w + dis_r + forestland + imprevious + (1 \| ID)	0	0.56
used ~ dis_w + dis_r + forestland + building + imprevious + (1 \| ID)	0.487	0.44
used ~ dis_w + dis_r + imprevious + (1 \| ID)	10.572	0
used ~ dis_w + dis_r + building + imprevious + (1 \| ID)	11.302	0
used ~ dis_w + dis_r + forestland + building + (1 \| ID)	25.132	0
森林公园 Forest parks
used ~ dis_w + dis_r + farmland + forestland + grassland + building + imprevious + bareland + (1 \| ID)	0	1.00
used ~ dis_w + dis_r + farmland + forestland + grassland + building + bareland + (1 \| ID)	3.447	0
used ~ dis_w + dis_r + forestland + grassland + bareland + (1 \| ID)	3.462	0
used ~ dis_w + dis_r + forestland + grassland + imprevious + bareland + (1 \| ID)	3.930	0
used ~ dis_r + farmland + forestland + grassland + building + bareland + (1 \| ID)	9.975	0

模型构建 Model formula	与最佳模型的差值 ΔAIC	AIC 权重 AIC weight
居民住宅区 Residential areas
used ~ dis_w + dis_r + forestland + imprevious + (1 \| ID)	0	0.56
used ~ dis_w + dis_r + forestland + building + imprevious + (1 \| ID)	0.487	0.44
used ~ dis_w + dis_r + imprevious + (1 \| ID)	10.572	0
used ~ dis_w + dis_r + building + imprevious + (1 \| ID)	11.302	0
used ~ dis_w + dis_r + forestland + building + (1 \| ID)	25.132	0
森林公园 Forest parks
used ~ dis_w + dis_r + farmland + forestland + grassland + building + imprevious + bareland + (1 \| ID)	0	1.00
used ~ dis_w + dis_r + farmland + forestland + grassland + building + bareland + (1 \| ID)	3.447	0
used ~ dis_w + dis_r + forestland + grassland + bareland + (1 \| ID)	3.462	0
used ~ dis_w + dis_r + forestland + grassland + imprevious + bareland + (1 \| ID)	3.930	0
used ~ dis_r + farmland + forestland + grassland + building + bareland + (1 \| ID)	9.975	0

预测变量 Predictor variable	居民住宅区 Residential areas		森林公园 Forest parks
预测变量 Predictor variable	β系数 β coefficient	标准误 Standard error	β系数 β coefficient	标准误 Standard error
截距 Intercept	-15.304^***	1.907	-1.282	0.056
道路接近程度 Proximity to road	-0.138^***	0.015	-0.117^***	0.012
水源接近程度 Proximity to water	-0.163^***	0.014	-0.047^***	0.013
林地 Forestland	0.095^***	0.023	0.397^***	0.042
草地 Grassland			0.401^***	0.042
建筑 Building	0.021	0.031	-0.185^***	0.050
不透水面 Impervious	-0.203^***	0.034	-0.137^*	0.059
耕地 Farmland			-0.103^*	0.042
裸地 Bareland			1.796^***	0.164

预测变量 Predictor variable	居民住宅区 Residential areas		森林公园 Forest parks
预测变量 Predictor variable	β系数 β coefficient	标准误 Standard error	β系数 β coefficient	标准误 Standard error
截距 Intercept	-15.304^***	1.907	-1.282	0.056
道路接近程度 Proximity to road	-0.138^***	0.015	-0.117^***	0.012
水源接近程度 Proximity to water	-0.163^***	0.014	-0.047^***	0.013
林地 Forestland	0.095^***	0.023	0.397^***	0.042
草地 Grassland			0.401^***	0.042
建筑 Building	0.021	0.031	-0.185^***	0.050
不透水面 Impervious	-0.203^***	0.034	-0.137^*	0.059
耕地 Farmland			-0.103^*	0.042
裸地 Bareland			1.796^***	0.164