Abstract
Emerging infectious disease outbreaks are increasingly suspected to be a consequence of human pressures exerted on natural ecosystems. Previously, host taxonomic communities have been used as indicators of infectious disease emergence, and the loss of their diversity has been implicated as a driver of increased presence. The mechanistic details in how such pathogen–host systems function, however, may not always be explained by taxonomic variation or loss. Here we used machine learning and methods based on Gower’s dissimilarity to quantify metrics of invertebrate functional diversity, in addition to functional groups and their taxonomic diversity at sites endemic and non-endemic for the model generalist pathogen Mycobacterium ulcerans, the causative agent of Buruli ulcer. Changes in these metrics allowed the rapid categorisation of the ecological niche of the mycobacterium’s hosts and the ability to relate specific host traits to its presence in aquatic ecosystems. We found that taxonomic diversity of hosts and overall functional diversity loss and evenness had no bearing on the mycobacterium’s presence, or whether the site was in an endemic area. These findings, however, provide strong evidence that generalist environmentally persistent bacteria such as M. ulcerans can be associated with specific functional traits rather than taxonomic groups of organisms, increasing our understanding of emerging disease ecology and origin.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. arXiv:1406.5823
Benbow ME, Williamson H, Kimbirauskas R, McIntosh MD, Kolar R, Quaye C, et al. (2008). Aquatic Invertebrates as Unlikely Vectors of Buruli Ulcer Disease. Emerging Infectious Diseases 14:1247-1254.
Benbow ME, Kimbirauskas R, McIntosh MD, Williamson H, Quaye C, Boakye D, et al. (2013). Aquatic macroinvertebrate assemblages of Ghana, West Africa: understanding the ecology of a neglected tropical disease. EcoHealth 2013:1-16.
BjØrnstad ON, and Falck W (2001). Nonparametric spatial covariance functions: Estimation and testing. Environmental and Ecological Statistics 8:53-70.
Botta-Dukát Z (2005). Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. Journal of Vegetation Science 16:533-540.
Chapin FS, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, et al. (2000). Consequences of changing biodiversity. Nature 405:234-242.
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.
Cummins KW, Merritt RW, and Andrade PCN (2005). The use of invertebrate functional groups to characterize ecosystem attributes in selected streams and rivers in south Brazil. Studies on Neotropical Fauna and Environment 40:69-89.
Dolnicar S, Grabler K, Mazanec JA, Woodside AG, Crouch GI, Oppermann M, et al. (1999). A tale of three cities: perceptual charting for analysing destination images. CABI Publishing, Wallingford.
Fyfe JAM, Lavender CJ, Handasyde KA, Legione AR, O’Brien CR, Stinear TP, et al. (2010). A Major Role for Mammals in the Ecology of Mycobacterium ulcerans. PLoS Negl Trop Dis 4:e791.
García‐Peña GE, Garchitorena A, Carolan K, Canard E, Prieur‐Richard AH, Suzán G, et al. (2016) Niche‐based host extinction increases prevalence of an environmentally acquired pathogen. Oikos
George KM, Chatterjee D, Gunawardana G, Welty D, Hayman J, Lee R, et al. (1999). Mycolactone: A Polyketide Toxin from Mycobacterium ulcerans Required for Virulence. Science 283:854.
George KM, Pascopella L, Welty DM, and Small PLC (2000). A Mycobacterium ulcerans Toxin, Mycolactone, Causes Apoptosis in Guinea Pig Ulcers and Tissue Culture Cells. Infect. Immun. 68:877-883.
Gower JC, and Legendre P (1986). Metric and Euclidean properties of dissimilarity coefficients. Journal of Classification 3:5-48.
Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, et al. (2002). Climate Warming and Disease Risks for Terrestrial and Marine Biota. Science 296:2158-2162.
Johnson PTJ, De Roode JC, and Fenton A (2015). Why infectious disease research needs community ecology. Science 349:1259504.
Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, et al. (2008). Global trends in emerging infectious diseases. Nature 451:990-993.
Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, et al. (2010). Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647-652.
Laliberté E, and Legendre P (2010). A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299-305.
Laliberté E, Shipley B (2011) FD: Measuring Functional Diversity from Multiple Traits, and Other Tools for Functional Ecology. R package version 1.0-11
LoGiudice K, Ostfeld RS, Schmidt KA, 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 100:567-571.
Marsollier L, Robert R, Aubry J, Saint Andre J-P, Kouakou H, Legras P, et al. (2002). Aquatic Insects as a Vector for Mycobacterium ulcerans. Appl. Environ. Microbiol. 68:4623-4628.
Marston BJ, Diallo MO, Horsburgh CR, Diomande I, Saki MZ, Kanga JM, et al. (1995). Emergence of Buruli ulcer disease in the Daloa region of Cote d’Ivoire. The American journal of tropical medicine and hygiene 52:219-224.
McKinney ML (2006). Urbanization as a major cause of biotic homogenization. Biological Conservation 127:247-260.
McKinney M (2008). Effects of urbanization on species richness: A review of plants and animals. Urban Ecosystems 11:161-176.
Merritt RW, Walker ED, Small PLC, Wallace JR, Johnson PDR, Benbow ME, et al. (2010). Ecology and Transmission of Buruli Ulcer Disease: A Systematic Review. PLoS Negl Trop Dis 4:e911.
Meyers WM, Tignokpa N, Priuli GB, and Portaels F (1996). Mycobacterium ulcerans infection (Buruli ulcer): first reported patients in Togo. British Journal of Dermatology 134:1116-1121.
Morris A, Gozlan RE, Hassani H, Andreou D, Couppié P, and Guégan J-F (2014). Complex temporal climate signals drive the emergence of human water-borne disease. Emerging Microbes & Infections 3:e56.
Nakagawa S, Schielzeth H (2012) A general and simple method for obtaining R2 from generalized linear mixed‐effects models. Methods in Ecology and Evolution 4, 133-142.
Ostfeld RS, and Keesing F (2000). Biodiversity series: the function of biodiversity in the ecology of vector-borne zoonotic diseases. Canadian Journal of Zoology 78:2061-2078.
Petchey OL, and Gaston KJ (2002). Functional diversity (FD), species richness and community composition. Ecology Letters 5:402-411.
Petchey OL, and Gaston KJ (2006). Functional diversity: back to basics and looking forward. Ecology letters 9:741-758.
Portaels F, Meyers WM, Ablordey A, Castro AG, Chemlal K, de Rijk P, et al. (2008). First Cultivation and Characterization of Mycobacterium ulcerans from the Environment. PLoS Negl Trop Dis 2:e178.
R Development Team (2014). R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing
Rahel FJ (2002). Homogenization of freshwater faunas. Annual Review of Ecology and Systematics 33:291-315.
Randolph SE, and Dobson ADM (2012). Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139:847-863.
Roche B, and Guégan J-F (2011). Ecosystem dynamics, biological diversity and emerging infectious diseases. Comptes Rendus Biologies 334:385-392.
Roche B, Benbow ME, Merritt R, Kimbirauskas R, McIntosh M, Small PLC, et al. (2013). Identifying the Achilles heel of multi-host pathogens: the concept of keystone ‘host’ species illustrated by Mycobacterium ulcerans transmission. Environmental Research Letters 8:045009.
Schmidt KA, and Ostfeld RS (2001). Biodiversity and the dilution effect in disease ecology. Ecology 82:609-619.
Stienstra Y, van der Graaf WTA, Asamoa K, and van der Werf TS (2002). Beliefs and attitudes toward Buruli ulcer in Ghana. American Journal of Tropical Medicine and Hygiene 67:207-213.
Stinear TP, Seemann T, Pidot S, Frigui W, Reysset G, Garnier T, et al. (2007). Reductive evolution and niche adaptation inferred from the genome of Mycobacterium ulcerans, the causative agent of Buruli ulcer. Genome Research 17:192-200.
Stinear TP, Seemann T, Harrison PF, Jenkin GA, Davies JK, Johnson PDR, et al. (2008). Insights from the complete genome sequence of Mycobacterium marinum on the evolution of Mycobacterium tuberculosis. Genome research 18:729-741.
Toft C, and Andersson SGE (2010). Evolutionary microbial genomics: insights into bacterial host adaptation. Nature Reviews Genetics 11:465-475.
Villéger S, Mason NWH, and Mouillot D (2008). New Multidimensional Functional Diversity Indices for a Multifaceted Framework in Functional Ecology. Ecology 89:2290-2301.
Vorosmarty CJ, McIntyre PB, Gessner MO, Dudgeon D, Prusevich A, Green P, et al. (2010). Global threats to human water security and river biodiversity. Nature 467:555-561.
Webb CT, Hoeting JA, Ames GM, Pyne MI, and LeRoy Poff N (2010). A structured and dynamic framework to advance traits‐based theory and prediction in ecology. Ecology Letters 13:267-283.
Williamson HR, Benbow ME, Nguyen KD, Beachboard DC, Kimbirauskas RK, McIntosh MD, et al. (2008). Distribution of Mycobacterium ulcerans in Buruli Ulcer Endemic and Non-Endemic Aquatic Sites in Ghana. PLoS Negl Trop Dis 2:e205.
Woolhouse ME, and Gowtage-Sequeria S (2005). Host range and emerging and reemerging pathogens. Emerging infectious diseases 11:1842-1847.
World Health Organisation (2001) Buruli ulcer management of Mycobacterium ulcerans disease. http://whqlibdoc.who.int/hq/2001/WHO_CDS_CPE_GBUI_2001.3.pdf. Accessed 01/06/2013
Acknowledgments
This work has benefited from a 3-year Bournemouth University PhD fellowship grant to Aaron Morris. AM, REG and JFG have benefited from an ‘Investissement d’Avenir’ grant managed by Agence Nationale de la Recherche (CEBA, Ref. ANR-10-LABX-2501). JFG is sponsored by the Institut de Recherche pour le Développement (IRD) and the Centre National de la Recherche Scientifique, and REG by IRD. The work and support of R.K. Kimbirauskas, M.D. McIntosh, T. White, and R. Kolar for invertebrate field collections and identification is gratefully acknowledged. MEB, RWM, PLCS and HW were funded by Grant Number R01TW007550 from the Fogarty International Center through the NIH/NSF Ecology of Infectious Diseases Program. The content is solely the responsibility of the authors and does not necessarily represent the official views of the Fogarty International Center or the National Institutes of Health.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Morris, A., Guégan, JF., Benbow, M.E. et al. Functional Diversity as a New Framework for Understanding the Ecology of an Emerging Generalist Pathogen. EcoHealth 13, 570–581 (2016). https://doi.org/10.1007/s10393-016-1140-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10393-016-1140-x