Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-22T15:07:04.806Z Has data issue: false hasContentIssue false
  • English
  • Français

Diversifying forest communities may change Lyme disease risk: extra dimension to the dilution effect in Europe

Published online by Cambridge University Press:  13 May 2016

SANNE C. RUYTS ,
EVY AMPOORTER ,
ELENA C. COIPAN ,
LANDER BAETEN ,
DIETER HEYLEN ,
HEIN SPRONG ,
ERIK MATTHYSEN  and
KRIS VERHEYEN
SANNE C. RUYTS*
Affiliation:
Forest & Nature Laboratory, Department of Forest and Water Management, Ghent University, Geraardsbergsesteenweg 267, 9090 Melle-Gontrode, Belgium
EVY AMPOORTER
Affiliation:
Forest & Nature Laboratory, Department of Forest and Water Management, Ghent University, Geraardsbergsesteenweg 267, 9090 Melle-Gontrode, Belgium
ELENA C. COIPAN
Affiliation:
Centre for Infectious Disease Control Netherlands, National Institute for Public Health and Environment, P.O. Box 1, 3720 BA Bilthoven, The Netherlands
LANDER BAETEN
Affiliation:
Forest & Nature Laboratory, Department of Forest and Water Management, Ghent University, Geraardsbergsesteenweg 267, 9090 Melle-Gontrode, Belgium
DIETER HEYLEN
Affiliation:
Evolutionary Ecology Group, Department of Biology, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerp, Belgium
HEIN SPRONG
Affiliation:
Centre for Infectious Disease Control Netherlands, National Institute for Public Health and Environment, P.O. Box 1, 3720 BA Bilthoven, The Netherlands
ERIK MATTHYSEN
Affiliation:
Evolutionary Ecology Group, Department of Biology, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerp, Belgium
KRIS VERHEYEN
Affiliation:
Forest & Nature Laboratory, Department of Forest and Water Management, Ghent University, Geraardsbergsesteenweg 267, 9090 Melle-Gontrode, Belgium
*
*Corresponding author: Forest & Nature Laboratory, Department of Forest and Water Management, Ghent University, Geraardsbergsesteenweg 267, 9090 Melle-Gontrode, Belgium. Tel: +32 (0)9 264 90 36. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Lyme disease is caused by bacteria of the Borrelia burgdorferi genospecies complex and transmitted by Ixodid ticks. In North America only one pathogenic genospecies occurs, in Europe there are several. According to the dilution effect hypothesis (DEH), formulated in North America, nymphal infection prevalence (NIP) decreases with increasing host diversity since host species differ in transmission potential. We analysed Borrelia infection in nymphs from 94 forest stands in Belgium, which are part of a diversification gradient with a supposedly related increasing host diversity: from pine stands without to oak stands with a shrub layer. We expected changing tree species and forest structure to increase host diversity and decrease NIP. In contrast with the DEH, NIP did not differ between different forest types. Genospecies diversity however, and presumably also host diversity, was higher in oak than in pine stands. Infected nymphs tended to harbour Borrelia afzelii infection more often in pine stands while Borrelia garinii and Borrelia burgdorferi ss. infection appeared to be more prevalent in oak stands. This has important health consequences, since the latter two cause more severe disease manifestations. We show that the DEH must be nuanced for Europe and should consider the response of multiple pathogenic genospecies.

Keywords

BiodiversityBorrelia burgdorferi genospeciesdilution effectdisease ecologyforest diversificationpublic healthIxodes ricinusLyme disease
Type
Research Article
Information
Parasitology , Volume 143 , Issue 10 , September 2016 , pp. 1310 - 1319
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

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

Alexander, K., Butler, J. and Green, T. (2006). The value of different tree and shrub species to wildlife. British Wildlife 18, 18–28.Google Scholar
Allan, B. F. and Ostfeld, R. S. (2003). Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17, 267–272.CrossRefGoogle Scholar
Balmelli, T. and Piffaretti, J. I. (1995). Association between different clinical manifestations of Lyme disease and different species of Borrelia burgdorferi sensu lato. Research in Microbiology 146, 329–340.CrossRefGoogle ScholarPubMed
Barbour, A. and Fish, D. (1993). The biological and social phenomenon of Lyme disease. Science 260, 1610–1616.CrossRefGoogle ScholarPubMed
Begon, M. (2008). Effects of host diversity on disease dynamics. In Infectious Disease Ecology: Effects of Ecosystems on Disease and of Disease on Ecosystems (ed. Ostfeld, R. S., Keesing, F. and Eviner, V.), pp. 12–29. Princeton University Press, Princeton, USA.Google Scholar
Bingsohn, L., Beckert, A., Zehner, R., Kuch, U., Oehme, R., Kraiczy, P. and Amendt, J. (2013). Prevalences of tick-borne encephalitis virus and Borrelia burgdorferi sensu lato in Ixodes ricinus populations of the Rhine-Main region, Germany. Ticks and Tick-borne Diseases 4, 207–213.CrossRefGoogle ScholarPubMed
Brockerhoff, E. G., Jactel, H., Parrotta, J. A., Quine, C. P. and Sayer, J. (2008). Plantation forests and biodiversity: oxymoron or opportunity? Biodiversity and Conservation 17, 925–951.CrossRefGoogle Scholar
Brunner, J. L., LoGiudice, K. and Ostfeld, R. S. (2008). Estimating reservoir competence of Borrelia burgdorferi hosts: prevalence and infectivity, sensitivity, and specificity. Journal of Medical Entomology 45, 139–147.CrossRefGoogle ScholarPubMed
Burri, C., Cadenas, F. M., Douet, V., Moret, J. and Gern, L. (2007). Ixodes ricinus density and infection prevalence of Borrelia burgdorferi sensu lato along a north-facing altitudinal gradient in the Rhône valley (Switzerland). Vector-Borne and Zoonotic Diseases 7, 50–58.CrossRefGoogle ScholarPubMed
Carnus, J.-M., Parrotta, J., Brockerhoff, E., Arbez, M., Jactel, H., Kremer, A., Lamb, D., O'Hara, K. and Walters, B. (2006). Planted forests and biodiversity. Journal of Forestry 104, 65–77.Google Scholar
Coipan, E. C., Fonville, M., Tijsse-Klasen, E., van der Giessen, J. W. B., Takken, W., Sprong, H. and Takumi, K. (2013). Geodemographic analysis of Borrelia burgdorferi sensu lato using the 5S-23S rDNA spacer region. Infection, Genetics and Evolution 17, 216–222.CrossRefGoogle ScholarPubMed
Comstedt, P., Bergström, S., Olsen, B., Garpmo, U., Marjavaara, L., Mejlon, H., Barbour, A. G. and Bunikis, J. (2006). Migratory passerine birds as reservoirs of Lyme borreliosis in Europe. Emerging Infectious Diseases 12, 1087–1096.CrossRefGoogle ScholarPubMed
Du Bus de Warnaffe, G. and Deconchat, M. (2008). Impact of four silicultural systems on birds in the Belgian Ardenne: implication for biodiversity in plantation forests. Biodiversity & Conservation 17, 1041–1055.CrossRefGoogle Scholar
Gray, J. (1998). Review of ticks transmitting Lyme borreliosis. Experimental & Applied Acarology 22, 249–258.CrossRefGoogle Scholar
Gray, J. S., Kahl, O., Robertson, J. N., Daniel, M., Estrada-Peña, A., Gettinby, G., Jaenson, T. G. T., Jensen, P., Jongejan, F., Korenberg, E., Kurtenbach, K. and Zeman, P. (1998). Lyme borreliosis habitat assessment. Zentralblatt für Bakteriologie 287, 211–228.CrossRefGoogle ScholarPubMed
Heylen, D., Tijsse, E., Fonville, M., Matthysen, E. and Sprong, H. (2013). Transmission dynamics of Borrelia burgdorferi s.l. in a bird tick community. Environmental Microbiology 15, 663–673.CrossRefGoogle Scholar
Heylen, D., Matthysen, E., Fonville, M. and Sprong, H. (2014). Songbirds as general transmitters but selective amplifiers of Borrelia burgdorferi sensu lato genotypes in Ixodes rinicus ticks. Environmental Microbiology 16, 2859–2868.CrossRefGoogle ScholarPubMed
Humair, P.-F. and Gern, L. (1998). Relationship between Borrelia burgdorferi sensu lato species, red squirrels (Sciurus vulgaris) and Ixodes ricinus in enzootic areas in Switzerland. Acta Tropica 69, 213–227.CrossRefGoogle ScholarPubMed
Humair, P. F., Peter, O., Wallich, R. and Gern, L. (1995). Strain variation of Lyme disease spirochetes isolated from Ixodes ricinus ticks and rodents collected in two endemic areas in Switzerland. Journal of Medical Entomology 32, 433–438.CrossRefGoogle ScholarPubMed
Humair, P.-F., Postic, D., Wallich, R. and Gem, L. (1998). An avian reservoir (Turdus merula) of the Lyme borreliosis spirochetes. Zentralblatt für Bakteriologie 287, 521–538.CrossRefGoogle ScholarPubMed
Kennedy, C. E. J. and Southwood, T. R. E. (1984). The number of species of insects associated with British trees: a re-analysis. Journal of Animal Ecology 53, 455–478.CrossRefGoogle Scholar
Kurtenbach, K., De Michelis, S., Etti, S., Schäfer, S. M., Sewell, H.-S., Brade, V. and Kraiczy, P. (2002). Host association of Borrelia burgdorferi sensu lato – the key role of host complement. Trends in Microbiology 10, 74–79.CrossRefGoogle ScholarPubMed
Kurtenbach, K., Hanincová, K., Tsao, J. I., Margos, G., Fish, D. and Ogden, N. H. (2006). Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nature Reviews Microbiology 4, 660–669.CrossRefGoogle ScholarPubMed
Laiolo, P. (2002). Effects of habitat structure, floral composition and diversity on a forest bird community in north-western Italy. Folia Zoologica 51, 121–128.Google Scholar
Laiolo, P., Caprio, E. and Rolando, A. (2004). Can forest management have season-dependent effects on bird diversity? Biodiversity and Conservation 13, 1925–1941.CrossRefGoogle Scholar
Linard, C., Lamarque, P., Heyman, P., Ducoffre, G., Luyasu, V., Tersago, K., Vanwambeke, S. O. and Lambin, E. F. (2007). Determinants of the geographic distribution of Puumala virus and Lyme borreliosis infections in Belgium. International Journal of Health Geographics 6, 15–29.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Margos, G., Hojgaard, A., Lane, R. S., Cornet, M., Fingerle, V., Rudenko, N., Ogden, N., Aanensen, D. M., Fish, D. and Piesman, J. (2010). Multilocus sequence analysis of Borrelia bissettii strains from North America reveals a new Borrelia species, Borrelia kurtenbachii . Ticks and Tick-borne Diseases 1, 151–158.CrossRefGoogle ScholarPubMed
Margos, G., Vollmer, S. a, Ogden, N. H. and Fish, D. (2011). Population genetics, taxonomy, phylogeny and evolution of Borrelia burgdorferi sensu lato. Infection, Genetics and Evolution 11, 1545–1563.CrossRefGoogle ScholarPubMed
Marsot, M., Henry, P. Y., Vourc'h, G., Gasqui, P., Ferquel, E., Laignel, J., Grysan, M. and Chapuis, J. L. (2012). Which forest bird species are the main hosts of the tick, Ixodes ricinus, the vector of Borrelia burgdorferi sensu lato, during the breeding season? International Journal for Parasitology 42, 781–788.CrossRefGoogle ScholarPubMed
Matuschka, F.-R., Fischer, P., Heiler, M., Richter, D. and Spielman, A. (1992). Capacity of European animals as reservoir hosts for the Lyme disease spirochete. Journal of Infectious Diseases 165, 479–483.CrossRefGoogle ScholarPubMed
Needham, G. R. and Teel, P. D. (1991). Off-host physiological ecology of ixodid ticks. Annual Review of Entomology 36, 659–681.CrossRefGoogle ScholarPubMed
Norman, R., Bowers, R. G., Begon, M. and Hudson, P. J. (1999). Persistence of tick-borne virus in the presence of multiple host species: tick reservoirs and parasite mediated competition. Journal of Theoretical Biology 200, 111–118.CrossRefGoogle ScholarPubMed
Ogden, N. H. and Tsao, J. I. (2009). Biodiversity and Lyme disease: dilution or amplification? Epidemics 1, 196–206.CrossRefGoogle ScholarPubMed
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H. and Wagner, H. (2015). vegan: Community Ecology Package. R package version 2.2-1. http://CRAN.R-project.org/package=vegan Google Scholar
Olsthoorn, A. F. M., Bertelink, H. H., Gardenir, J. J., Pretzch, H., Hekhuis, H. J. and Franc, A. (1999). Management of Mixed-Species Forest: Silviculture and Economics. IBN Science Contribution 15, Wageningen, The Netherlands.Google Scholar
Ostfeld, R. S. and Keesing, F. (2000 a). The function of biodiversity in the ecology of vector-borne zoonotic diseases. Canadian Journal of Zoology 78, 2061–2078.CrossRefGoogle Scholar
Ostfeld, R. S. and Keesing, F. (2000 b). Biodiversity and disease risk: the case of Lyme disease. Conservation Biology 14, 722–728.CrossRefGoogle Scholar
Parola, P. and Raoult, D. (2001). Ticks and tickborne bacterial diseases in humans: an emerging infectious threat. Clinical Infectious Diseases 32, 897–928.CrossRefGoogle ScholarPubMed
Peel, M. C., Finlayson, B. L. and McMahon, T. A. (2007). Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences 11, 1633–1644.CrossRefGoogle Scholar
Pérez, D., Kneubühler, Y., Rais, O. and Gern, L. (2012). Seasonality of Ixodes ricinus ticks on vegetation and on rodents and Borrelia burgdorferi sensu lato genospecies diversity in two Lyme borreliosis-endemic areas in Switzerland. Vector Borne and Zoonotic Diseases 12, 633–644.CrossRefGoogle ScholarPubMed
Piesman, J. and Gern, L. (2004). Lyme borreliosis in Europe and North America. Parasitology 129, S191–S220.CrossRefGoogle ScholarPubMed
Pisanu, B., Chapuis, J. L., Dozières, A., Basset, F., Poux, V. and Vourc'h, G. (2014). High prevalence of Borrelia burgdorferi s.l. in the European red squirrel Sciurus vulgaris in France. Ticks and Tick-borne Diseases 5, 1–6.CrossRefGoogle ScholarPubMed
R Core Team (2015). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.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.CrossRefGoogle ScholarPubMed
Rauter, C. and Hartung, T. (2005). Prevalence of Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks in Europe: a metaanalysis. Applied and Environmental Microbiology 71, 7203–7216.CrossRefGoogle ScholarPubMed
Rudenko, N., Golovchenko, M., Grubhoffer, L. and Oliver, J. H. (2011). Updates on Borrelia burgdorferi sensu lato complex with respect to public health. Ticks and Tick-borne Diseases 2, 123–128.CrossRefGoogle ScholarPubMed
Ruiz-Fons, F., Fernández-de-Mera, I. G., Acevedo, P., Gortázar, C. and de la Fuente, J. (2012). Factors driving the abundance of Ixodes ricinus ticks and the prevalence of zoonotic I. ricinus-borne pathogens in natural foci. Applied and Environmental Microbiology 78, 2669–2676.CrossRefGoogle ScholarPubMed
Sanger, F., Nicklen, S. and Coulson, R. (1977). DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences of the United States of America 74, 5463–5467.CrossRefGoogle ScholarPubMed
Schmidt, K. A. and Ostfeld, R. S. (2001). Biodiversity and the dilution effect in disease ecology. Ecology 82, 609–619.CrossRefGoogle Scholar
Schouls, L. M., Pol, I. Van De, Rijpkema, S. G. T. and Schot, C. S. (1999). Detection and identification of Ehrlichia, Borrelia burgdorferi sensu lato, and Bartonella species in Dutch Ixodes ricinus ticks. Journal of Clinical Microbiology 37, 2215–2222.CrossRefGoogle ScholarPubMed
Spiecker, H., Hansen, J., Klimo, E., Skovsgaard, J. P., Sterba, H. and von Teuffel, K. (2004). Norway Spruce Conversion – Options and Consequences. EFI Research Report 18. Koninklijke Brill NV, Leiden, The Netherlands.CrossRefGoogle Scholar
Stanek, G., Wormser, G. P., Gray, J. and Strle, F. (2012). Lyme borreliosis. Lancet 379, 461–473.CrossRefGoogle ScholarPubMed
Strle, F. and Stanek, G. (2009). Clinical manifestations and diagnosis of Lyme borreliosis. Current Problems in Dermatology 37, 51–110.CrossRefGoogle ScholarPubMed
Tack, W. (2013). Impact of forest conversion on the abundance of Ixodes ricinus ticks. PhD thesis, Ghent University, Ghent, Belgium.Google Scholar
Tack, W., Madder, M., Baeten, L., Vanhellemont, M., Gruwez, R. and Verheyen, K. (2012 a). Local habitat and landscape affect Ixodes ricinus tick abundances in forests on poor, sandy soils. Forest Ecology and Management 265, 30–36.CrossRefGoogle Scholar
Tack, W., Madder, M., Baeten, L., De Frenne, P. and Verheyen, K. (2012 b). The abundance of Ixodes ricinus ticks depends on tree species composition and shrub cover. Parasitology 139, 1273–1281.CrossRefGoogle ScholarPubMed
Tack, W., Madder, M., Baeten, L., Vanhellemont, M. and Verheyen, K. (2013). Shrub clearing adversely affects the abundance of Ixodes ricinus ticks. Experimental and Applied Acarology 60, 411–420.CrossRefGoogle ScholarPubMed
Vanthomme, K., Bossuyt, N., Boffin, N. and Van Casteren, V. (2012). Incidence and management of presumption of Lyme borreliosis in Belgium: recent data from the sentinel network of general practitioners. European Journal of Clinical Microbiology & Infectious Disease 31, 2385–2390.CrossRefGoogle ScholarPubMed
Venables, W. N. and Ripley, B. D. (2002). Modern Applied Statistics with S, 4th Edn. Springer, New York, USA.CrossRefGoogle Scholar
Verheyen, K., De Schrijver, A., Wuyts, K., Gielis, M., Van Gossum, P., Geudens, G., Van Herzele, A., De Boever, L. and Vanhellemont, M. (2007). Van dennenplantages naar een beloofd land? Theoretische en praktische aspecten van bosomvorming. Silva Belgica 114, 20–26.Google Scholar
Verkem, S., De Maeseneer, J., Vandendriessche, B., Verbeylen, G. and Yskout, S. (2003). Zoogdieren in Vlaanderen. Ecologie en verspreiding van 1987 tot 2002. Natuurpunt Studie & JNM-Zoogdierenwerkgroep, Mechelen & Gent, België.Google Scholar
Wang, Y., Naumann, U., Wright, S. T. and Warton, D. I. (2012). mvabund - an R package for model-based analysis of multivariate abundance data. Methods in Ecology and Evolution 3, 471–474.CrossRefGoogle Scholar
Warton, D. I., Wright, S. T. and Wang, Y. (2012). Distance-based multivariate analyses confound location and dispersion effects. Methods in Ecology and Evolution 3, 89–101.CrossRefGoogle Scholar
Waterinckx, M. and Roelandt, B. (2001). De bosinventarisatie van het Vlaamse Gewest. Ministerie van de Vlaamse Gemeenschap, Afdeling Bos & Groen, Brussel, België.Google Scholar
Wickham, H. (2009). ggplot2: Elegant Graphics for Data Analysis. Springer, New York, USA.CrossRefGoogle Scholar
Wood, C. L. and Lafferty, K. D. (2013). Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trends in Ecology & Evolution 28, 239–247.CrossRefGoogle ScholarPubMed
World Health Organization (2004). The Vector - Borne Human Infections of Europe. Their Distribution and Burden on Public Health. WHO Regional Office for Europe, Copenhagen, Denmark.Google Scholar
Wormser, G. P., Dattwyler, R. J., Shapiro, E. D., Halperin, J. J., Steere, A. C., Klempner, M. S., Krause, P. J., Bakken, J. S., Strle, F., Stanek, G., Bockenstedt, L., Fish, D., Dumler, J. S. and Nadelman, R. B. (2006). The clinical assessment, treatment, and prevention of lyme disease, human granulocytic anaplasmosis, and babesiosis: clinical practice guidelines by the Infectious Diseases Society of America. Clinical Infectious Diseases: An Official Publication of The Infectious Diseases Society of America 43, 1089–1134.CrossRefGoogle ScholarPubMed
Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. a and Smith, G. M. (2009). Mixed Effects Models and Extensions in Ecology with R. Springer, New York, USA.CrossRefGoogle Scholar