Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-24T01:15:45.580Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of host diversity and species assemblage composition on bovine tuberculosis (bTB) risk in Ethiopian cattle

Published online by Cambridge University Press:  30 January 2017

DEJENE W. SINTAYEHU ,
IGNAS M. A. HEITKÖNIG ,
HERBERT H. T. PRINS ,
ZEWDU K. TESSEMA  and
WILLEM F. DE BOER
DEJENE W. SINTAYEHU*
Affiliation:
Resource Ecology Group, Wageningen University, Droevendaalsesteeg 3a, 6708PB Wageningen, The Netherlands College of Agriculture and Environmental Sciences, Haramaya University, P.O. Box 38, Dire Dawa, Ethiopia
IGNAS M. A. HEITKÖNIG
Affiliation:
Resource Ecology Group, Wageningen University, Droevendaalsesteeg 3a, 6708PB Wageningen, The Netherlands
HERBERT H. T. PRINS
Affiliation:
Resource Ecology Group, Wageningen University, Droevendaalsesteeg 3a, 6708PB Wageningen, The Netherlands
ZEWDU K. TESSEMA
Affiliation:
College of Agriculture and Environmental Sciences, Haramaya University, P.O. Box 38, Dire Dawa, Ethiopia
WILLEM 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: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Current theories on diversity–disease relationships describe host species diversity and species identity as important factors influencing disease risk, either diluting or amplifying disease prevalence in a community. Whereas the simple term ‘diversity’ embodies a set of animal community characteristics, it is not clear how different measures of species diversity are correlated with disease risk. We therefore tested the effects of species richness, Pielou's evenness and Shannon's diversity on bovine tuberculosis (bTB) risk in cattle in the Afar Region and Awash National Park between November 2013 and April 2015. We also analysed the identity effect of a particular species and the effect of host habitat use overlap on bTB risk. We used the comparative intradermal tuberculin test to assess the number of bTB-infected cattle. Our results suggested a dilution effect through species evenness. We found that the identity effect of greater kudu – a maintenance host – confounded the dilution effect of species diversity on bTB risk. bTB infection was positively correlated with habitat use overlap between greater kudu and cattle. Different diversity indices have to be considered together for assessing diversity–disease relationships, for understanding the underlying causal mechanisms. We posit that unpacking diversity metrics is also relevant for formulating disease control strategies to manage cattle in ecosystems characterized by seasonally limited resources and intense wildlife–livestock interactions.

Keywords

evennessdiversitygreater kuduidentity effectmaintenance hostsmulti-host disease ecologyhabitat use overlap
Type
Research Article
Information
Parasitology , Volume 144 , Issue 6 , May 2017 , pp. 783 - 792
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

Anderson, D. R., Burnham, K. P. and Thompson, W. L. (2000). Model hypothesis and testing: problems, prevalence, and an alternative. Journal of Wildlife Management 64, 912–923.Google Scholar
Artois, M. (2003). Wildlife infectious disease control in Europe. Journal Mountain Ecology 7, 89–97.Google Scholar
Böhm, M., Hutchings, M. and White, P. (2009). Contact networks in a wildlife-livestock host community: identifying high-risk individuals in the transmission of bovine TB among badgers and cattle. PLoS ONE 4, e5016.Google Scholar
Bonnington, C., Weaver, D. and Fanning, E. (2007). Livestock and large wild mammals in Kilombero Valley, in southern Tanzania. African Journal of Ecology 45, 658–663.CrossRefGoogle Scholar
Bouchard, C., Beauchamp, G., Leighton, P. A., Lindsay, R., Belanger, D. and Ogden, N. H. (2013). Does high biodiversity reduce the risk of Lyme disease invasion? Parasites and Vectors 6, 195.Google Scholar
Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Inference: a Practical Information-Theoretic Approach, 2nd Edn. Springer-Verlag, New York.Google Scholar
Cardinale, B. J., Duffy, J. E., Gonzalez, A., Hooper, D. U., Perrings, C., Venail, P., Narwani, A., Mace, G. M., Tilman, D. and Wardle, D. A. (2012). Biodiversity loss and its impact on humanity. Nature 486, 59–67.Google Scholar
Central Statistical Agency (CSA) (2008). Agricultural Sample Survey 2006/07, Vol II: Report on Livestock and Livestock Characteristics. Statistical Bulletin 388, Addis Ababa, Ethiopia.Google Scholar
Chen, L. and Zhou, S. (2015). A Combination of species evenness and functional diversity is the best predictor of disease risk in multihost communities. The American Naturalist 186, 755–765.Google Scholar
Civitello, D. J., Cohen, J., Fatima, H., Halstead, N. T., Liriano, J., McMahon, T. A., Ortega, C. N., Sauer, E. L., Sehgal, T., Young, S. and Rohr, J. R. (2015). Biodiversity inhibits parasites: broad evidence for the dilution effect. Proceedings of the National Academy of Sciences of the United States of America 112, 8667–8671.CrossRefGoogle ScholarPubMed
Cleaveland, S., Shaw, D. J., Mfinanga, S. G., Shirima, G., Kazwala, R. R., Eblate, E. and Sharp, M. (2007). Mycobacterium bovis in rural Tanzania: risk factors for infection in human and cattle populations. Tuberculosis 87, 30–43.Google Scholar
Cooper, S. M., Scott, H. M., de la Garza, G. R., Deck, A. L. and Cathey, J. C. (2010). Distribution and interspecies contact of feral swine and cattle on rangeland in south Texas: implications for disease transmission. Journal of Wildlife Disease 46, 152–164.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, 303–312.Google Scholar
Cosivi, O., Meslin, F., Daborn, C. and Grange, J. M. (1995). Epidemiology of Mycobacterium bovis infection in animals and humans, with particular reference to Africa. Scientific and Technical Review of the Office International des Epizooties 14, 733–746.Google Scholar
Cosivi, O., Grange, J., Daborn, C., Raviglione, M., Fujikura, T., Cousins, D., Robinson, R., Huchzermeyer, H., Kantor, I. and Meslin, F. (1998). Zoonotic tuberculosis due to Mycobacterium bovis in developing countries. Emerging Infectious Disease 4, 59–70.CrossRefGoogle ScholarPubMed
Courtenay, O., Reilly, L. A., Sweeney, F. P., Hibberd, V., Bryan, S., Ul-Hassan, A., Newman, C., Macdonald, D. W., Delahay, R. J., Wilson, G. J. and Wellington, E. M. H. (2006). Is Mycobacterium bovis in the environment important for the persistence of bovine tuberculosis? Biology Letters 2, 460–462.Google Scholar
de Garine-Wichatitsky, M., Caron, A., Kock, R., Tschopp, R., Munyeme, M., Hofmeyr, M. and Michel, A. (2013). Review of bovine tuberculosis at the wildlife-livestock-human interface in sub-Saharan Africa. Epidemiology and Infection 147, 1342–1358.Google Scholar
Dejene, S. W., Heitkönig, I. M. A., Prins, H. H. T., Fitsum, A., Daniel, A., Zelalem, E., Kelkay, Z. T. and de Boer, W. F. (2016). Risk factors for bovine tuberculosis (bTB) in cattle in Ethiopia. PLoS ONE 11, e0159083.Google Scholar
de Leeuw, J., Waweru, M. N., Okello, O. O., Maloba, M., Nguru, P., Said, M. Y., Aligula, H. M., Heitkonig, I. M. A. and Reid, R. S. (2001). Distribution and diversity of wildlife in northern Kenya in relation to livestock and permanent water points. Biological Conservation 100, 297–306.Google Scholar
Di Marco, M., Boitani, L., Mallon, D., Hoffmann, M., Iacucci, A., Meijaard, E., Visconti, P., Schipper, J. and Rondinini, C. (2014). A retrospective evaluation of the global decline of carnivores and ungulates. Conservation Biology 28, 1109–1118.Google Scholar
Fenton, A. and Pedersen, A. B. (2005). Community epidemiology framework for classifying disease threats. Emerging Infectious Diseases 11, 1815–1821.Google Scholar
Fine, A. E., Bolin, C. A., Gardiner, J. C. and Kaneene, J. B. (2011). A study of the persistence of Mycobacterium bovis in the environment under natural weather conditions in Michigan, USA. Veterinary Medicine International 2011, 1–12.Google Scholar
Fritz, H., De Garine-Wichatitsky, M. and Georges, L. (1996). Habitat use by sympatric wild and domestic herbivores in an African Savanna Woodland: the influence of cattle spatial behaviour. Journal of Applied Ecology 33, 589–598.CrossRefGoogle Scholar
Frohlich, K., Thiede, S., Kozikowski, T. and Jakob, W. (2002). A review of mutual transmission of important infectious diseases between livestock and wildlife in Europe. Annals of the New York Academy of Sciences 969, 4–13.Google Scholar
Gorenfloa, L. J., Romaineb, S., Russell, A., Mittermeierc, A. R. and Walker-Painemilla, K. (2012). Co-occurrence of linguistic and biological diversity in biodiversity hotspots and high biodiversity wilderness areas. Proceedings of the National Academy of Sciences of the United States of America 109, 8032–8037.Google Scholar
Gortazar, C., Ferroglio, E., Hofle, U., Frolich, K. and Vicente, J. (2007). Diseases shared between wildlife and livestock: a European perspective. European Journal of Wildlife Research 53, 241–256.CrossRefGoogle Scholar
Gosselin, F. (2006). An assessment of the dependence of evenness indices on species richness. Journal of Theoretical Biology 242, 591–597.CrossRefGoogle ScholarPubMed
Haines-Young, R. and Chopping, M. (1996). Quantifying landscape structure: a review of landscape indices and their application to forested landscapes. Progress in Physical Geography 20, 418–445.Google Scholar
Hamer, G., Chaves, L., Anderson, T., Kitron, U. D., Brawn, J. D., Ruiz, M. O., Loss, S. R., Walker, E. D. and Goldberg, T. L. (2011). Fine-scale variation in vector host use and force of infection drive localized patterns of West Nile Virus transmission. PLoS ONE 6, e23767.Google Scholar
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, 1–12.Google Scholar
Hill, M. (1973). Diversity and evenness: a unifying notation and its consequences. Ecology 54, 427–432.Google Scholar
Hofmeester, T. R., Coipan, E. C., van Wieren, S. E., Prins, H. H. T., Takken, W. and Sprong, H. (2016). Few vertebrate species dominate the Borrelia burgdorferi s.l. life cycle. Environmental Research Letters 11, 1–16.CrossRefGoogle Scholar
Huang, Z. Y. X., de Boer, W. F., van Langevelde, F., Xu, C., Ben Jebara, K., Berlingieri, F. and Prins, H. H. T. (2013). Dilution effect in bovine tuberculosis: risk factors for regional disease occurrence in Africa. Proceedings of the Royal Society B – Biological Sciences 280, 1–6.Google Scholar
Huang, Z. Y. X., Xu, C., van Langevelde, F., Prins, H. H. T., ben Jebara, K. and de Boer, W. F. (2014). Dilution effect and identity effect by wildlife in the persistence and recurrence of bovine tuberculosis. Parasitology 141, 981–987.Google Scholar
Huang, Z. Y. X., van Langevelde, F., Estrada-Peña, A., Suzán, G. and de Boer, W. F. (2016). The diversity-disease relationship: evidence for and criticisms of the dilution effect. Parasitology 143, 1075–1086.Google Scholar
Hudson, P. J., Rizzoli, A. P., Grenfell, B. T., Heesterbeek, J. P. and Dobson, A. P. (2002). Ecology of Wildlife Diseases. Oxford University Press, Oxford, UK.Google Scholar
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, 50–63.Google Scholar
Jackson, R., De Lisle, G. W. and Morris, R. S. (1995). A study of the environmental survival of Mycobacterium bovis on a farm in New Zealand. New Zealand Veterinary Journal 43, 346–352.Google Scholar
Johnson, P. T., Ostfeld, R. S. and Keesing, F. (2015). Frontiers in research on biodiversity and disease. Ecology Letters 18, 1119–1133.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, 230–233.Google Scholar
Keesing, F., Holt, R. D. and Ostfeld, R. S. (2006). Effects of species diversity on disease risk. Ecology Letters 9, 485–498.Google Scholar
Keesing, F., Brunner, J., Duerr, S., Killilea, M., LoGiudice, K., Schmidt, K., Vuong, H. and Ostfeld, R. (2009). Hosts as ecological traps for the vector of Lyme disease. Proceedings of the Royal Society B – Biological Sciences 276, 3911–3919.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, 647–652.Google Scholar
Kelly, W. R. and Collins, J. D. (1978). The health significance of some infectious agents present in animal effluents. Veterinary Science Communications 2, 95–103.Google Scholar
Legendre, P. and Legendre, L. (1998). Numerical Ecology. Elsevier, Oxford.Google Scholar
LoGiudice, K., Ostfeld, R. S., Schmidt, K. A. and Keesing, F. (2003). The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proceedings of the National Academy of Sciences of the United States of America 100, 567–571.Google Scholar
Magurran, A. E. (1988). Ecological Diversity and its Measurement. Princeton University Press, Princeton, USA.Google Scholar
Magurran, A. E. (2004). Measuring Biological Diversity. Blackwell, Oxford.Google Scholar
Maleko, D. D., Mbassa, G. N., Maanga, W. F. and Sisya, E. S. (2012). Impacts of Wildlife-Livestock Interactions in and around Arusha National Park, Tanzania. Current Research Journal of Biological Sciences 4, 471–476.Google Scholar
Martin, C., Pastoret, P. P., Brochier, B., Humblet, M. F. and Saegerman, C. (2011). A survey of the transmission of infectious diseases/infections between wild and domestic ungulates in Europe. Veterinary Research 42, 70–81.CrossRefGoogle ScholarPubMed
McGarigal, K. and Marks, B. J. (1994). FRAGSTATS: Spatial Analysis Program for Quantifying Landscape Structure. Unpublished report, Oregon State University, Portland, Oregon, USA.Google Scholar
Miller, E. and Huppert, A. (2013). The effects of host diversity on vector borne disease: the conditions under which diversity will amplify or dilute the disease risk. PLoS ONE 8, e80279.Google Scholar
Morens, M. D., Folkers, K. G. and Fauci, S. A. (2004). The challenge of emerging and re-emerging infectious diseases. Nature 430, 242–249.Google Scholar
Munyeme, M., Muma, J. B., Skjerve, E., Nambota, A. M., Phiri, I. G., Samui, K. L., Dorny, P. and Tryland, M. (2008). Risk factors associated with bovine tuberculosis in traditional cattle of the livestock/wildlife interface areas in the Kafue basin of Zambia. Preventive Veterinary Medicine 85, 317–328.Google Scholar
Munyeme, M., Muma, J., Samui, K., Skjerve, E., Nambota, A., Phiri, I., Rigouts, L. and Tryland, M. (2009). Prevalence of bovine tuberculosis and animal level risk factors for indigenous cattle under different grazing strategies in the livestock/wildlife interface areas of Zambia. Tropical Animal Health and Production 41, 345–352.Google Scholar
Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. and Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature 403, 853–858.Google Scholar
Myersa, S. S., Gaffikin, L., Golden, C. D., Ostfeld, R. S., Redford, K. H., Ricketts, T. H., Turner, W. R. and Osofsky, S. A. (2013). Human health impacts of ecosystem alteration. Proceedings of the National Academy of Sciences of the United States of America 110, 18753–18760.Google Scholar
Oda, E., Solari, A. and Botto-mahan, C. (2014). Effects of mammal host diversity and density on the infection level of Trypanosoma cruzi in sylvatic kissing bugs. Medical and Veterinary Entomology 28, 384–390.Google Scholar
Odadi, W. O., Young, T. P. and Okeyo-Owuor, J. B. (2007). Effects of wildlife on cattle diets in Laikipia rangeland, Kenya. Rangeland Ecology & Management 60, 179–185.Google Scholar
Oksanen, J., Guillaume, F. B., Roeland, K., Pierre, L., Minchin, P. R., O'Hara, R. B., Simpson, L. G., Peter, S., Henry, M., Stevens, H. and Helene, W. (2016). Community Ecology Package. Package ‘vegan. http://CRAN.R-project.Google Scholar
Olff, H., Ritchie, M. E. and Prins, H. H. T. (2002). Global environmental controls of diversity in large herbivores. Nature 415, 901–904.CrossRefGoogle ScholarPubMed
Osofsky, S. A., Cleaveland, S., Karesh, W. B., Kock, M. D., Nyhus, P. J., Starr, L. and Yang, A. (eds) (2005). Conservation and Development Interventions at the Wildlife/Livestock Interface: Implications for Wildlife, Livestock and Human Health. IUCN, Gland, Switzerland and Cambridge, UK.Google Scholar
Ostfeld, R. and Keesing, F. (2000). The function of biodiversity in the ecology of vector-borne zoonotic diseases. Canadian Journal of Zoology 78, 2061–2078.Google Scholar
Ostfeld, R. S. (2013). A Candide response to Panglossian accusations by Randolph and Dobson: biodiversity buffers disease. Parasitology 140(10), 1196–1198.Google Scholar
Ostfeld, R. S. and Keesing, F. (2012). Effects of host diversity on infectious disease. Annual Review of Ecology, Evolution, and Systematics 43, 157–182.Google Scholar
Pianka, E. R. (1973). The structure of lizard communities. Annual Review of Ecology and Systematics 4, 53–74.CrossRefGoogle Scholar
Power, A. G. and Mitchell, C. E. (2004). Pathogen spillover in disease epidemics. The American Naturalist 164, 79–89.Google Scholar
Prins, H. H. T. (2000). Competition between wildlife and livestock in Africa. In Wildlife Conservation by Sustainable Use (ed. Prins, H. H. T., Grootenhuis, J. G. and Dolan, T. T.), pp 51–80. Kluwer Academic Publishers, Norwell.CrossRefGoogle Scholar
Proffitt, K. M., Gude, J. A., Hamlin, K. L., Garrott, R. A., Cunningham, J. A. and Grigg, J. L. (2011). Elk distribution and spatial overlap with livestock during the brucellosis transmission risk period. Journal of Applied Ecology 48, 471–478.Google Scholar
R Core Team (2015). R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://R-project.org/.Google Scholar
Randolph, S. E. and Dobson, A. D. M. (2012). Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139, 847–863.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, 529–540.Google Scholar
Riitters, K. H., Wickham, J. D., Vogelmann, J. E. and Jones, K. B. (2000). National land-cover pattern data. Ecology 81, 604–612.Google Scholar
Riley, S. P. D., Hadidian, J. and Manski, D. A. (1998). Population density, survival, and rabies in raccoons in an urban national park. Canadian Journal of Zoology 76, 1153–1164.Google Scholar
Roper, T. J., Garnett, B. T. and Delahay, R. J. (2003). Visits to farm buildings and cattle troughs by badgers (Meles meles): a potential route for transmission of bovine tuberculosis (Mycobacterium bovis) between badgers and cattle. Cattle Practice 11, 9–12.Google Scholar
Roug, A., Clifford, D., Mazet, J., Kazwala, R., John, J., Coppolillo, P. and Smith, W. (2014). Spatial predictors of bovine tuberculosis infection and Brucella spp. exposure in pastoralist and agro pastoralist livestock herds in the Ruaha ecosystem of Tanzania. Tropical Animal Health and Production 46, 837–843.CrossRefGoogle Scholar
Sheldon, A. L. (1969). Equitability indices: dependence on the species count. Ecology 50, 466–467.Google Scholar
Sitters, J., Heitkönig, I. M. A., Holmgren, M. and Ojwang, G. S. O. (2009). Herded cattle and wild grazers partition water but share forage resources during dry years in East African savannas. Biological Conservation 142, 738–750.CrossRefGoogle Scholar
Skuce, R. A., Allen, A. R. and Stanley, W. (2012). Herd level risk factors for bovine tuberculosis. Veterinary Medicine International 2012, 1–10.Google Scholar
Smith, B. and Wilson, J. B. (1996). A consumer's guide to evenness indices. Oikos 1, 70–82.Google Scholar
Stuart, C. and Stuart, T. (2000). A Field Guide to the Tracks and Signs of Southern and East African Wildlife. Struik Publishers, Cape Town.Google Scholar
Symonds, M. R. E. and Johnson, C. N. (2008). Species richness and evenness in Australian birds. The American Naturalist 171, 480–490.Google Scholar
Treydte, A. C., Bernasconi, S. M., Kreuzer, M. and Edwards, P. J. (2006). Diet of the common warthog (Phacochoerus africanus) on former cattle grounds in a Tanzanian savanna. Journal of Mammalogy 87, 889–898.Google Scholar
Tschopp, R. (2015). Bovine tuberculosis at the human–livestock–wildlife interface in sub-Saharan Africa. In One Health: The Theory and Practice of Integrated Health Approaches (ed. Zinsstag, J., Schelling, E., Waltner-Toews, D., Whittaker, M. and Tanner, M.), pp. 163–175. CABI, Wallingford.Google Scholar
Tucker, C. M. and Cadotte, M. W. (2013). Unifying measures of biodiversity: understanding when richness and phylogenetic diversity should be congruent. Diversity and Distributions 19, 845–854.Google Scholar
Vicente, J., Segalés, J., Balasch, M., Plana-Durán, J., Domingo, M. and Gortázar, C. (2004). Epidemiological study on porcine circovirus type 2 (PCV2) infection in the European wild boar (Sus scrofa). Veterinary Research 35, 243–253.Google Scholar
Voeten, M. M. and Prins, H. T. T. (1999). Resource partitioning between sympatric wild and domestic herbivores in the Tarangire region of Tanzania. Oecologia 120, 287–294.Google Scholar
Ward, A. I., Tolhurst, B. A. and Delahay, R. J. (2006). Farm husbandry and the risks of disease transmission between wild and domestic mammals: a brief review focusing on bovine tuberculosis in badgers and cattle. Animal Science 82, 767–773.Google Scholar
Wood, C. L. and Lafferty, K. D. (2013). Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trends in Ecology and Evolution 28, 239–247.Google Scholar
World Health Organization (2012). Global tuberculosis report 2012. http://www.stop.org/wg/news_vaccines/ Google Scholar
Zhang, H., John, R., Peng, Z., Yuan, J., Chu, C., Guozhen, D. and Shurong, Z. (2012). The relationship between species richness and evenness in plant communities along a successional gradient: a study from Sub-Alpine Meadows of the Eastern Qinghai-Tibetan Plateau, China. PLoS ONE 7, e49024.CrossRefGoogle ScholarPubMed
Supplementary material: File

Sintayehu supplementary material

Tables S1-S5

Download Sintayehu supplementary material(File)
File 35.2 KB