Abstract
Classical swine fever (CSF) has been widespread among wild boars in Japan since the first outbreak in September 2018 after 26 years of absence. Although oral vaccination against CSF has been implemented, CSF infections are ongoing in the wild boar population. Therefore, increasing the effectiveness of oral vaccination in wild boars by distributing the vaccine in an environment where wild boars are likely to ingest the vaccine is necessary. This study aimed to investigate the landscape elements that facilitate the uptake of oral vaccines by wild boars. We used data from the oral vaccine campaign in Gunma and Tochigi prefectures in eastern Japan and analyzed the vaccine uptake rate and landscape structure at the vaccine distribution sites in two seasons. The uptake rate of the oral vaccine was significantly higher in the first season (Gunma: 41.5%, Tochigi: 37.1%) than in the second season (Gunma: 28.5%, Tochigi: 25.7%). We also found that broadleaf forest and bamboo woodland were negatively associated with vaccine uptake in Gumma Prefecture in the first and second seasons, respectively. These results indicate that vaccine uptake may be influenced by seasonal changes in wild boar food resources. Moreover, the results suggest that the uptake of oral vaccination may increase in environments with high landscape diversity, i.e., forest edge environments, which contain mainly forest elements and a small amount of cultivated land and city areas, whereas it may decrease in environments with mainly cultivated land and city areas and less forest elements due to the influence of human activities.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and analyzed during the current study are available from the corresponding author on reasonable request.
References
Abaigar T, Barrio G, Vericad J (1994) Habitat preference of wild boar (Sus scrofa L., 1758) in a mediterranean environment. Indir Eval Signs Mammalia 58:201–210. https://doi.org/10.1515/mamm.1994.58.2.201
Acevedo P, Escudero MA, Muńoz R, Gortázar C (2006) Factors affecting wild boar abundance across an environmental gradient in Spain. Acta Theriol (warsz) 51:327–336. https://doi.org/10.1007/BF03192685
Acevedo P, Quirós-Fernández F, Casal J, Vicente J (2014) Spatial distribution of wild boar population abundance: basic information for spatial epidemiology and wildlife management. Ecol Indic 36:594–600. https://doi.org/10.1016/j.ecolind.2013.09.019
Ballesteros C, Carrasco-García R, Vicente J et al (2009) Selective piglet feeders improve age-related bait specificity and uptake rate in overabundant Eurasian wild boar populations. Wildl Res 36:203–212. https://doi.org/10.1071/WR08127
Ballesteros C, Vicente J, Morriss G et al (2011) Acceptance and palatability for domestic and wildlife hosts of baits designed to deliver a tuberculosis vaccine to wild boar piglets. Prev Vet Med 98:198–203. https://doi.org/10.1016/j.prevetmed.2010.10.012
Barrios-Garcia MN, Ballari SA (2012) Impact of wild boar (Sus scrofa) in its introduced and native range: a review. Biol Invasions 14:2283–2300. https://doi.org/10.1007/s10530-012-0229-6
Bazarragchaa E, Isoda N, Kim T et al (2021) Efficacy of oral vaccine against classical swine fever in wild boar and estimation of the disease dynamics in the quantitative approach. Viruses 13:319. https://doi.org/10.3390/v13020319
Boitani L, Mattei L, Nonis D, Corsi F (1994) Spatial and activity patterns of wild boars in Tuscany, Italy. J Mammal 75:600–612. https://doi.org/10.2307/1382507
Calenge C, Rossi S (2014) Bayesian modelling of hunting data may improve the understanding of host–parasite systems: wild boar diseases and vaccination as an example. J Theor Biol 343:32–43. https://doi.org/10.1016/j.jtbi.2013.11.011
Fernanda Cuevas M, Ojeda RA, Jaksic FM (2013) Multi-scale patterns of habitat use by wild boar in the Monte Desert of Argentina. Basic Appl Ecol 14:320–328. https://doi.org/10.1016/j.baae.2013.03.001
Fritzemeier J, Teuffert J, Greiser-Wilke I et al (2000) Epidemiology of classical swine fever in Germany in the 1990s. Vet Microbiol 77:29–41. https://doi.org/10.1016/S0378-1135(00)00254-6
Geospatial Information Authority of Japan (2016) Fundamental geospatial data: digital elevation model (in Japanese). http://www.gsi.go.jp/kiban/index.html
Gunma Prefecture (2020) Gunma Prefecture wild boar appropriate management plan. https://www.pref.gunma.jp/page/7126.html. Accessed 6 Sep 2023
Gunma Prefecture (2022) About classical swine fever countermeasures. https://www.pref.gunma.jp/page/9515.html. Accessed 20 Dec 2022
Hayama Y, Shimizu Y, Murato Y et al (2020) Estimation of infection risk on pig farms in infected wild boar areas-epidemiological analysis for the reemergence of classical swine fever in Japan in 2018. Prev Vet Med 175:104873. https://doi.org/10.1016/j.prevetmed.2019.104873
Hayashi N, Takayama karin, Yoshinaga S, Koizumi T (2021) Soil characteristics of feeding sites in wild boar (Sus scrofa) inhabiting suburban forest. Bull For For Prod Res Inst 20:263–275. https://doi.org/10.20756/ffpri.20.4_263
Ikeda T, Higashide D, Suzuki T, Asano M (2022) Efficient oral vaccination program against classical swine fever in wild boar population. Prev Vet Med 205:105700. https://doi.org/10.1016/j.prevetmed.2022.105700
Ikeda T, Kuninaga N, Suzuki T et al (2019) Tourist-wild boar (Sus scrofa) interactions in urban wildlife management. Glob Ecol Conserv 18:e00617. https://doi.org/10.1016/j.gecco.2019.e00617
Isoda N, Baba K, Ito S et al (2020) Dynamics of classical swine fever spread in wild boar in 2018–2019. Japan Pathogens 9:119. https://doi.org/10.3390/pathogens9020119
Ito S, Bosch J, Aguilar-Vega C et al (2023) Development of an effective oral vaccine dissemination strategy against classical swine fever for wild boar in Gifu Prefecture, Japan. Transbound Emerg Dis 2023:e9484441. https://doi.org/10.1155/2023/9484441
Ito S, Jurado C, Bosch J et al (2019) Role of wild boar in the spread of classical swine fever in Japan. Pathogens 8:206. https://doi.org/10.3390/pathogens8040206
Kaden V, Heyne H, Kiupel H et al (2002) Oral immunisation of wild boar against classical swine fever: concluding analysis of the recent field trials in Germany. Berl Munch Tierarztl Wochenschr 115:179–185
Kaden V, Lange E, Fischer U, Strebelow G (2000) Oral immunisation of wild boar against classical swine fever: evaluation of the first field study in Germany. Vet Microbiol 73:239–252. https://doi.org/10.1016/S0378-1135(00)00148-6
Kodera Y, Kanzaki N (2001) Food habitsand nutritional condition of Japanese wild boar in Iwami District, Shimane Prefecture,western Japan. Wildl conserv Jpn 6:109–117. https://doi.org/10.20798/wildlifeconsjp.6.2_109
Kodera Y, Kanzaki N, Ishikawa N, Minagawa A (2013) Food habits of wild boar (Sus scrofa) inhabiting Iwami District, Shimane Prefecture, western Japan. Mamm Sci 53:279–287. https://doi.org/10.11238/mammalianscience.53.279
Kodera Y, Nagatsuma T, Sawada S et al (2010) How does spreading maize on fields influence behavior of wild boars (Sus scrofa)? Mamm Sci 50:137–144. https://doi.org/10.11238/mammalianscience.50.137
Kramer-Schadt S, Fernández N, Thulke H-H (2007) Potential ecological and epidemiological factors affecting the persistence of classical swine fever in wild boar Sus scrofa populations. Mammal Rev 37:1–20. https://doi.org/10.1111/j.1365-2907.2007.00097.x
Laddomada A (2000) Incidence and control of CSF in wild boar in Europe. Vet Microbiol 73:121–130. https://doi.org/10.1016/S0378-1135(00)00139-5
Lindgren F, Rue H, Lindström J (2011) An explicit link between Gaussian fields and Gaussian Markov random fields: the stochastic partial differential equation approach. J R Stat Soc Ser B Stat Methodol 73:423–498. https://doi.org/10.1111/j.1467-9868.2011.00777.x
Massei G, Genov P (2004) The environmental impact of wild boar. Galemys Bol Inf Soc Esp Para Conserv Estud Los Mamíferos ISSN 1137–8700 16(1):135–145 16
Massei G, Kindberg J, Licoppe A et al (2015) Wild boar populations up, numbers of hunters down? A review of trends and implications for Europe. Pest Manag Sci 71:492–500. https://doi.org/10.1002/ps.3965
Ministry of Agriculture, and Forestry and Fisheries (2020) Guidelines for the implementation of field vaccination program of oral swine fever vaccine (in Japanese). https://www.maff.go.jp/j/syouan/douei/csf/wildboar/inosisitaisaku.html. Accessed 16 Jan 2023
Ministry of Agriculture, and Forestry and Fisheries (2021) About outbreak situation in Japan (in Japanese). In: https://www.maff.go.jp/j/syouan/douei/csf/domestic.html. Accessed 1 Aug 2022
Ministry of Land (2008) National land numerical information: river data. In: Google docs. https://nlftp.mlit.go.jp/ksj/gml/datalist/KsjTmplt-W05.html. Accessed 16 Jan 2023
Ministry of the Environment (2008) The 6th-7th national survey on the natural environment. https://www.biodic.go.jp/trialSystem/EN/info/vg67.html. Accessed 1 Aug 2022
Moennig V (2015) The control of classical swine fever in wild boar. Front Microbiol 6. https://doi.org/10.3389/fmicb.2015.01211
Ohashi H, Saito M, Horie R et al (2013) Differences in the activity pattern of the wild boar Sus scrofa related to human disturbance. Eur J Wildl Res 59:167–177. https://doi.org/10.1007/s10344-012-0661-z
Oksanen J, Simpson GL, Blanchet FG et al (2022) Vegan: community ecology package
Podgórski T, Baś G, Jędrzejewska B et al (2013) Spatiotemporal behavioral plasticity of wild boar (Sus scrofa) under contrasting conditions of human pressure: primeval forest and metropolitan area. J Mammal 94:109–119. https://doi.org/10.1644/12-MAMM-A-038.1
R Core Team (2022) R: A language and environment for statistical computing
Rossi S, Artois M, Pontier D et al (2005) Long-term monitoring of classical swine fever in wild boar (Sus scrofa sp.) using serological data. Vet Res 36:27–42. https://doi.org/10.1051/vetres:2004050
Rossi S, Pol F, Forot B et al (2010) Preventive vaccination contributes to control classical swine fever in wild boar (Sus scrofa sp.). Vet Microbiol 142:99–107. https://doi.org/10.1016/j.vetmic.2009.09.050
Rossi S, Staubach C, Blome S et al (2015) Controlling of CSFV in European wild boar using oral vaccination: a review. Front microbiol 6. https://doi.org/10.3389/fmicb.2015.01141
Rue H, Martino S, Chopin N (2009) Approximate Bayesian inference for latent Gaussian models by using integrated nested Laplace approximations. J R Stat Soc Ser B Stat Methodol 71:319–392. https://doi.org/10.1111/j.1467-9868.2008.00700.x
Saito M, Momose H, Mihira T (2011) Both environmental factors and countermeasures affect wild boar damage to rice paddies in Boso Peninsula, Japan. Crop Prot 30:1048–1054. https://doi.org/10.1016/j.cropro.2011.02.017
Schley L, Dufrêne M, Krier A, Frantz AC (2008) Patterns of crop damage by wild boar (Sus scrofa)in Luxembourg over a 10-year period. Eur J Wildl Res 54:589–599. https://doi.org/10.1007/s10344-008-0183-x
Shimizu Y, Hayama Y, Murato Y et al (2021) Epidemiological analysis of classical swine fever in wild boars in Japan. BMC Vet Res 17:188. https://doi.org/10.1186/s12917-021-02891-0
Simpson EH (1949) Measurement of diversity. Nature 163:688–688. https://doi.org/10.1038/163688a0
Tochigi Prefecture (2021) Tochigi Prefecture wild boar management plan. https://www.pref.tochigi.lg.jp/d04/eco/shizenkankyou/shizen/inosisihogokannri3.html. Accessed 6 Sep 2023
Tochigi Prefecture (2022) About classical swine fever. https://www.pref.tochigi.lg.jp/g06/csfinfo.html. Accessed 20 Dec 2022
von Rüden S, Staubach C, Kaden V et al (2008) Retrospective analysis of the oral immunisation of wild boar populations against classical swine fever virus (CSFV) in region Eifel of Rhineland-Palatinate. Vet Microbiol 132:29–38. https://doi.org/10.1016/j.vetmic.2008.04.022
Acknowledgements
Data for this study were provided by the Livestock Production Division, Department of Agriculture, Gunma Prefecture, and the Livestock Promotion Division, Department of Agriculture, Tochigi Prefecture.
Funding
This work is supported by the Project for Establishment of Emergency Quarantine System for African Swine Fever, Japan [no grant number].
Author information
Authors and Affiliations
Contributions
All authors contributed to the conception and design of the study. Documentation, data collection, and analysis were performed by Tomohiko Endo and Yoko Hayama. Tomohiko Endo wrote the first draft of the manuscript, and all authors commented on earlier drafts. The final manuscript was read and approved by all authors.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
We declare that there have been no ethical violations in this work.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Endo, T., Hirata, S., Hayama, Y. et al. Landscape elements affecting the ingestion of oral vaccine against classical swine fever in wild boar. Eur J Wildl Res 69, 102 (2023). https://doi.org/10.1007/s10344-023-01733-8
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10344-023-01733-8