Hostname: page-component-848d4c4894-cjp7w Total loading time: 0 Render date: 2024-06-19T03:43:11.299Z Has data issue: false hasContentIssue false

Dilution effect and identity effect by wildlife in the persistence and recurrence of bovine tuberculosis

Published online by Cambridge University Press:  10 March 2014

Z. Y. X. HUANG*
Affiliation:
Resource Ecology Group, Wageningen University, Droevendaalsesteeg 3a, 6708PB Wageningen, the Netherlands
C. XU
Affiliation:
School of Life Sciences, Nanjing University, 22 Hankou Road, 210093 Nanjing, China
F. VAN LANGEVELDE
Affiliation:
Resource Ecology Group, Wageningen University, Droevendaalsesteeg 3a, 6708PB Wageningen, the Netherlands
H. H. T. PRINS
Affiliation:
Resource Ecology Group, Wageningen University, Droevendaalsesteeg 3a, 6708PB Wageningen, the Netherlands
K. BEN JEBARA
Affiliation:
Animal Health Information Department, World Organisation for Animal Health, 12 rue de Prony, 75017 Paris, France
W. F. DE BOER
Affiliation:
Resource Ecology Group, Wageningen University, Droevendaalsesteeg 3a, 6708PB Wageningen, the Netherlands
*
*Corresponding author. Resource Ecology Group, Wageningen University, Droevendaalsesteeg 3a, 6708PB Wageningen, the Netherlands. E-mail: zheng.huang@wur.nl

Summary

Current theories on disease-diversity relationships predict a strong influence of host richness on disease transmission. In addition, identity effect, caused by the occurrence of particular species, can also modify disease risk. We tested the richness effect and the identity effects of mammal species on bovine tuberculosis (bTB), based on the regional bTB outbreak data in cattle from 2005–2010 in Africa. Besides, we also tested which other factors were associated with the regional bTB persistence and recurrence in cattle. Our results suggested a dilution effect, where higher mammal species richness (MSR) was associated with reduced probabilities of bTB persistence and recurrence in interaction with cattle density. African buffalo had a positive effect on bTB recurrence and a positive interaction effect with cattle density on bTB persistence, indicating an additive positive identity effect of buffalo. The presence of greater kudu had no effect on bTB recurrence or bTB persistence. Climatic variables only act as risk factors for bTB persistence. In summary, our study identified both a dilution effect and identity effect of wildlife and showed that bTB persistence and recurrence were correlated with different sets of risk factors. These results are relevant for more effective control strategies and better targeted surveillance measures in bTB.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Allepuz, A., Casal, J., Napp, S., Saez, M., Alba, A., Vilar, M., Domingo, M., Gonzalez, M. A., Duran-Ferrer, M., Vicente, J., Alvarez, J., Munoz, M. and Saez, J. L. (2011). Analysis of the spatial variation of bovine tuberculosis disease risk in Spain (2006–2009). Preventive Veterinary Medicine 100, 4452. doi: 10.1016/j.prevetmed.2011.02.012.Google Scholar
Ben Jebara, K., Caceres, P., Berlingieri, F. and Weber-Vintzel, L. (2012). Ten years’ work on the World Organisation for Animal Health (OIE) Worldwide Animal Disease Notification System. Preventive Veterinary Medicine 107, 149159. doi: 10.1016/j.prevetmed.2012.08.008.CrossRefGoogle Scholar
Biotani, L. (ed.) (1998). A Databank for the Conservation and Management of the African Mammals. Institute of Applied Ecology, Rome, Italy.Google Scholar
Boitani, L., Sinibaldi, I., Corsi, F., De Biase, A., Carranza, I. D., Ravagli, M., Reggiani, G., Rondinini, C. and Trapanese, P. (2008). Distribution of medium- to large-sized African mammals based on habitat suitability models. Biodiversity and Conservation 17, 605621. doi: 10.1007/s10531-007-9285-0.Google Scholar
Brooks-Pollock, E. and Keeling, M. (2009). Herd size and bovine tuberculosis persistence in cattle farms in Great Britain. Preventive Veterinary Medicine 92, 360365. doi: 10.1016/j.prevetmed.2009.08.022.Google Scholar
Corner, L. A. L. (2006). The role of wild animal populations in the epidemiology of tuberculosis in domestic animals: how to assess the risk. Veterinary Microbiology 112, 303312. doi: 10.1016/j.vetmic.2005.11.015.Google Scholar
De Garine-Wichatitsky, M., Caron, A., Kock, R., Tschopp, R., Munyeme, M., Hofmeyr, M. and Michel, A. (2013). A review of bovine tuberculosis at the wildlife-livestock-human interface in sub-Saharan Africa. Epidemiology and Infection 141, 13421356. doi: 10.1017/S0950268813000708.Google Scholar
Gilbert, M., Mitchell, A., Bourn, D., Mawdsley, J., Cliton-Hadley, R. and Wint, W. (2005). Cattle movements and bovine tuberculosis in Great Britain. Nature 435, 491496. doi: 10.1038/Nature03548.Google Scholar
Gilbert, M., Xiao, X. M., Pfeiffer, D. U., Epprecht, M., Boles, S., Czarnecki, C., Chaitaweesub, P., Kalpravidh, W., Minh, P. Q., Otte, M. J., Martin, V. and Slingenbergh, J. (2008). Mapping H5N1 highly pathogenic avian influenza risk in Southeast Asia. Proceedings of the National Academy of Sciences USA 105, 47694774. doi: 10.1073/pnas.0710581105.CrossRefGoogle ScholarPubMed
Hantsch, L., Braun, U., Scherer-Lorenzen, M. and Bruelheide, H. (2013). Species richness and species identity effects on occurrence of foliar fungal pathogens in a tree diversity experiment. Ecosphere 4, art81. doi: 10.1890/es13-00103.1.Google Scholar
Harris, I., Jones, P. D., Osborn, T. J. and Lister, D. H. (2013). Updated high-resolution grids of monthly climatic observations – the CRU TS3.10 Dataset. International Journal of Climatology, in press. doi: 10.1002/joc.3711.Google Scholar
Howery, L. D. and DeLiberto, T. J. (2004). Indirect effects of carnivores on livestock foraging behavior and production. Sheep and Goat Research Journal Paper 8.Google Scholar
Huang, Z. Y. X., de Boer, W. F., van Langevelde, F., Olson, V., Blackburn, T. M. and Prins, H. H. T. (2013 a). Species’ life-history traits explain interspecific variation in reservoir competence: a possible mechanism underlying the dilution effect. Plos ONE 8, e54341. doi: 10.1371/journal.pone.0054341.CrossRefGoogle ScholarPubMed
Huang, Z. Y. X., de Boer, W. F., van Langevelde, F., Xu, C., Ben Jebara, K., Berlingieri, F. and Prins, H. H. T. (2013 b). Dilution effect in bovine tuberculosis: risk factors for regional disease occurrence in Africa. Proceedings of the Royal Society B – Biological Sciences 280, 20130624. doi: 10.1098/rspb.2013.0624.CrossRefGoogle ScholarPubMed
Humblet, M. F., Boschiroli, M. L. and Saegerman, C. (2009). Classification of worldwide bovine tuberculosis risk factors in cattle: a stratified approach. Veterinary Research 40, 50. doi: 10.1051/Vetres/2009033.Google Scholar
Humblet, M. F., Gilbert, M., Govaerts, M., Fauville-Dufaux, M., Walravens, K. and Saegerman, C. (2010). New assessment of bovine tuberculosis risk factors in Belgium based on nationwide molecular epidemiology. Journal of Clinical Microbiology 48, 28022808. doi: 10.1128/Jcm.00293-10.Google Scholar
Johnson, P. T. J., Rohr, J. R., Hoverman, J. T., Kellermanns, E., Bowerman, J. and Lunde, K. B. (2012). Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk. Ecology Letters 15, 235242. doi: 10.1111/j.1461-0248.2011.01730.x.Google Scholar
Johnson, P. T. J., Preston, D. L., Hoverman, J. T. and Richgels, K. L. D. (2013). Biodiversity decreases disease through predictable changes in host community competence. Nature 494, 230233.CrossRefGoogle ScholarPubMed
Joseph, M. B., Mihaljevic, J. R., Orlofske, S. A. and Paull, S. H. (2013). Does life history mediate changing disease risk when communities disassemble? Ecology Letters 16, 14051412. doi: 10.1111/ele.12180.CrossRefGoogle ScholarPubMed
Karolemeas, K., McKinley, T. J., Clifton-Hadley, R. S., Goodchild, A. V., Mitchell, A., Johnston, W. T., Conlan, A. J. K., Donnelly, C. A. and Wood, J. L. N. (2011). Recurrence of bovine tuberculosis breakdowns in Great Britain: risk factors and prediction. Preventive Veterinary Medicine 102, 2229. doi: 10.1016/j.prevetmed.2011.06.004.CrossRefGoogle ScholarPubMed
Keesing, F., Holt, R. D. and Ostfeld, R. S. (2006). Effects of species diversity on disease risk. Ecology Letters 9, 485498. doi: 10.1111/j.1461-0248.2006.00885.x.Google Scholar
Keesing, F., Belden, L. K., Daszak, P., Dobson, A., Harvell, C. D., Holt, R. D., Hudson, P., Jolles, A., Jones, K. E., Mitchell, C. E., Myers, S. S., Bogich, T. and Ostfeld, R. S. (2010). Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647652. doi: 10.1038/Nature09575.CrossRefGoogle ScholarPubMed
Lloyd-Smith, J. O., Cross, P. C., Briggs, C. J., Daugherty, M., Getz, W. M., Latto, J., Sanchez, M. S., Smith, A. B. and Swei, A. (2005). Should we expect population thresholds for wildlife disease? TRENDS in Ecology and Evolution 20, 511519. doi: 10.1016/j.tree.2005.07.004.Google Scholar
Martin, V., Pfeiffer, D. U., Zhou, X. Y., Xiao, X. M., Prosser, D. J., Guo, F. S. and Gilbert, M. (2011). Spatial distribution and risk factors of Highly Pathogenic Avian Influenza (HPAI) H5N1 in China. PLOS Pathogens 7, e1001308. doi: 10.1371/journal.ppat.1001308.Google Scholar
Mathews, F., Lovett, L., Rushton, S. and Macdonald, D. W. (2006). Bovine tuberculosis in cattle: reduced risk on wildlife-friendly farms. Biology Letters 2, 271274. doi: 10.1098/rsbl.2006.0461.CrossRefGoogle ScholarPubMed
O'Brien, D. J., Schmitt, S. M., Rudolph, B. A. and Nugent, G. (2011). Recent advances in the management of bovine tuberculosis in free-ranging wildlife. Veterinary Microbiology 151, 2333. doi: 10.1016/j.vetmic.2011.02.022.Google Scholar
Ostfeld, R. S. (2013). A Candide response to Panglossian accusations by Randolph and Dobson: biodiversity buffers disease. Parasitology 140, 11961198. doi: 10.1017/S0031182013000541.Google Scholar
Ostfeld, R. S. and Keesing, F. (2012). Effects of host diversity on infectious disease. Annual Review of Ecology, Evolution, and Systematics 43, 157182. doi: 10.1146/annurev-ecolsys-102710-145022.Google Scholar
Randolph, S. E. and Dobson, A. D. (2012). Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139, 847863. doi: 10.1017/S0031182012000200.Google Scholar
Renwick, A. R., White, P. C. L. and Bengis, R. G. (2007). Bovine tuberculosis in southern Africa wildlife: a multi-species host-pathogen system. Epidemiology and Infection 135, 529540.Google Scholar
Rhodes, S. G., De Leij, F. A. A. M. and Dale, J. W. (2007). Protozoa as an environmental reservoir of bovine tuberculosis. Trends in Microbiology 15, 338339. doi: 10.1016/j.tim.2007.06.001.CrossRefGoogle ScholarPubMed
Skuce, R. A., Allen, A. R. and McDowell, S. W. (2012). Herd-level risk factors for bovine tuberculosis: a literature review. Veterinary Medicine International 2012, 621210. doi: 10.1155/2012/621210.Google Scholar
Vial, F. and Donnelly, C. A. (2012). Localized reactive badger culling increases risk of bovine tuberculosis in nearby cattle herds. Biology Letters 8, 5053. doi: 10.1098/rsbl.2011.0554.Google Scholar
White, P. W., Martin, S. W., De Jong, M. C. M., O'Keeffe, J. J., More, S. J. and Frankena, K. (2013). The importance of ‘neighbourhood’ in the persistence of bovine tuberculosis in Irish cattle herds. Preventive Veterinary Medicine 110, 346355. doi: 10.1016/j.prevetmed.2013.02.012.Google Scholar
Wint, G. R. W., Robinson, T. P., Bourn, D. M., Durr, P. A., Hay, S. I., Randolph, S. E. and Rogers, D. J. (2002). Mapping bovine tuberculosis in Great Britain using environmental data. Trends in Microbiology 10, 441444.Google Scholar
Supplementary material: File

Huang Supplementary Material

Tables

Download Huang Supplementary Material(File)
File 52.7 KB