1. Host animal biodiversity and Regulation of Human diseases BORDES Frédéric DVM, PhD ISEM CNRS Université de Montpellier 2 Montpellier, France Phnom Pen 18-19 Novembre 2014

2. WHY BIODIVERSITY MATTERS FOR HUMAN DISEASES OR What are the links between animal biodiversity and human diseases ? 2

3. 1 ) 61% of human infectious diseases ARE ZOONOTIC DISEASES implying many different animal hosts ( pathogens are often generalists) MULTI-HOST DISEASES 2)HOST SPECIES ARE NOT HOMOGENEOUS in terms of parasites’ susceptibility and potential of transmission: « COMPETENT » OR « INCOMPETENT » HOSTS MAY PLAY DIFFERENT ROLES 3

4. 4 PATHOGEN TRANSMISSION/DISEASE RISK ALTERATION OF INTERACTIONS, BIOLOGY, ABUNDANCE AND DIVERSITY OF HOSTS (VECTORS/ INTERMEDIATE HOSTS/DEFINITIVE HOSTS) Agricultural and land uses changes ( crops, cattle, pesticides) Deforestation, roads building,alteration habitatsDams, irrigation 3) « Anthropocene »: biodiversity loss is increasing. Whether and how biodiversity can protect humans against infectious diseases became crucial Urbanization

5. How biodiversity can theoretically be linked to human diseases? 5

6. 6

7. Global approach: dilution or amplification? 7

8. 8 Global drivers of human pathogen richness and prevalence, Dunn et al.2010 Proceedings Royal Society London B AMPLIFICATION AT WORK ? Mammal species richness Davies & Bucley, 2011, Phil. Trans.Roy. Soc Lond B Mammal species richness Davies & Bucley, 2011, Phil. Trans.Roy. Soc Lond B Geographical variation in Human pathogen richness, Dunn et al.2009, Procs

9. s …….OR DILUTION AT WORK? 9 Hot spots for emerging diseases (Jones et al.2008, Nature) Hot spots for erosion in mammals’ diversity (Schipper et al.2009,Science) Focus on Asia-Pacific area: similar pattern Biodiversity loss seems linked to an increase in zoonotic outbreaks (Morand et al.2014, Plos One) Focus on Asia-Pacific area: similar pattern Biodiversity loss seems linked to an increase in zoonotic outbreaks (Morand et al.2014, Plos One) ?

10. REGIONAL APPROACH 10

11. “ Lyme disease in USA: dilution Ostfeld & Keesing, Conservation Biology 2000

12. 1°) Associations between non passerine species richness and mosquito infection rates West Nile in USA (Lousiana): dilution at work 2° ) Relationship between human WNV disease and non-passerine Species Richness Ezenwa V O et al. 2006 Ezenwa et al.2008

13. 13 Hantavirus prevalence Rodents’ richness Panama (Suzan et al.2009) ; USA (Clay et al.2009; Dizney et Ruedas, 2009), Belgium (Tersago et al.2008) Blasdell et al.2011 Ecohealth Rodents Hantaviruses: dilution at work USA, Europe Panama, SE ASIA

14. 14 Xavier et al. (2012) Lower Richness of Small Wild Mammal Species and Chagas Disease Risk. PLoS Negl Trop Dis Dogs as sentinels of epidemiological risk for Humans for Chagas disease in Brazil Chagas disease risk is higher when mammalian diversity is low Geospatial analysis : reduction of the small mammal fauna (richness and abundance) is linked to higher exposure of dogs to infection.

15. 15 « Borrelia burgdorferi nymphal infection prevalence (NIP) was similar between island …contrary to what is predicted by the dilution effect hypothese » States et al.2014 Infection Genetics and Evolution Mammalian community on Block Island : 5 rodent Species and white tailed deer Mammalian community on mainland : 35 species Density of nymphs Density of infected nymphs Prevalence d’infection of nymphs But Lyme disease is not always amplified in species –poor community

16. 16 Spatial analysis of a large data set (Valle & Clark, 2013) Malaria burden in the Brazilean Amazon: rather amplification at work Almost half of the death attributed to malaria in Americas occured in Brazil b b Forest cover (and biodiversity) is the strongest predictor of malaria Risk in The Brazilian Amazon

17. Pattern for tropical parasites : dilution is not expected at all Focus on 69 tropical zoonotic protozoa and helminths ( including Leishmnia, Trypanosoma sp., Plasmodium sp.,Toxoplasma, Taenia sp., Trichuris, Schistosoma ) * Projected link between biodiversity and these parasites (Wood et al.Ecology 2014) 17 Negative = dilution effect Positive= amplification effect

18. 18 Parasitoloy,2012: DILUTION AND DISEASES: A HOT AND CONTROVERSIAL DEBATE…… DILUTION AND DISEASES: A HOT AND CONTROVERSIAL DEBATE…… Trend s in Ecology and Evolution, 2013: 2013: Ecology, 2014:

19. 19 Hosts diversity and richness is only one parameter 1.Vectors’ ecology and landscapes matter 2.Vectors’ amplification matters 3. Abundance of susceptible hosts matters

20. 20 EASTERN PERU BRAZILEAN AMAZON ShrubsSecondary vegetation soyaCattle,Pasture Deforestation Anopheles darlingi Landscapes and Vectors’ ecology matter MALARIA RISK

21. 21 VECTORS AMPLIFICATION : LYME DISEASE IN MASSACHUSSETS Deers are not competent hosts for B. Burgorferi but important hosts for ticks adult and mymphs (blood meals).Despite limiting pathogen transmission they amplify vectors populations… This non competent host increases disease risk for humans Kilpatrick et al.2014, J. Med Entomology Hunting

22. Abundance of susceptible hosts matters 22 Sites investigated for Lyme disease differed in -small mammal richness and -relative abundance of deer mice Peromyscus maniculatus Werden et al. (2014) PLoS ONE At sites where the relative abundance of mice is higher, species richness had little apparent effect on nymph infection

23. Conclusion: No generality at all Biodiversity is only one parameter of Human regulation diseases Thank you 23

24. 24 PATHOGEN TRANSMISSION/DISEASE RISK ALTERATION OF INTERACTIONS, BIOLOGY, ABUNDANCE AND DIVERSITY OF HOSTS (VECTORS/ INTERMEDIATE HOSTS/DEFINITIVE HOSTS) Agricultural and land uses changes ( crops, cattle, pesticides) Deforestation, roads building,alteration habitatsDams, irrigation 3) « Anthropocene »: biodiversity loss is increasing. Whether and how biodiversity can protect humans against infectious diseases became crucial Hunting Urbanization

25. 25

26. How dilution works ? Two primary mechanisms: 1. Transmission interference ( mainly for vector borne diseases) 2. Susceptible host regulation ( mainly for directly transmitted diseases) 26

27. Transmission interference : some less competent hosts can decrease human disease risk by intercepting pathogen transmission stages 27 High Biodiversity With different competence among hosts Reduced infected larval and nymhs Reduced human risk

28. Susceptible host regulation: when the presence of non-competent competitors in high –biodiversity context - REDUCED the competent hosts’ density that results in less intraspecific transmission of a pathogen and hence a lower risk for humans and/or - REDUCED hosts’ encounter rates between susceptible hosts and then pathogen transmission 28 Rodent species diversity - EX: Clay et al.2009 Ecohealth Pathogen prevalence contacts

29. 29 Chiclero's ulcer, caused by the sandfly-vectored protozoan parasite Leishmania mexicana an other example of a decline in disease risk with loss of biodiversity This parasite primarily infect « chicleros », the men who spend months in the forest collecting chicle, the latex produced by sapodilla trees. Chiclero's ulcer