Leveraging Small Biodiversity Reserves to Prevent Zoonotic Disease: Insights from Dilution Effect and Pathogen Adaptation Theories

Benjamin, Roche

doi:10.53941/dbgs.2025.100006

Open Access

Communication

Leveraging Small Biodiversity Reserves to Prevent Zoonotic Disease: Insights from Dilution Effect and Pathogen Adaptation Theories

Audrey Arnal^{1, 2, 3}

,

Rodolphe Elie Gozlan⁴

,

Nathalie Charbonnel⁵

,

Marie Bouilloud^{1, 5}

,

Andrea Chaves^{6, 7}

,

Manon Lounnas^{1, 2}

,

Michel Gauthier-Clerc⁸

,

Ana L. Vigueras-Galván^{2, 3}

,

Céline Arnathau^{1, 2}

,

David Roiz^{1, 2}

,

Ana I. Bento⁹

,

Serge Morand^{10, 11, 12}

,

Chris Walzer^{13, 14}

,

Gerardo Suzán^{2, 15}

,

Rosa Elena Sarmiento Silva^{2, 3, *, †}

,

Benjamin Roche^{1, 2, 3, †}

Author Information

Submitted: 22 Feb 2025 | Revised: 12 Mar 2025 | Accepted: 12 Mar 2025 | Published: 2 Apr 2025

Abstract

In today’s landscape of zoonotic pathogen outbreaks, the dilution effect theory, i.e., the theory that greater biodiversity can help curb pathogen transmission among wildlife, has gained significant attention. However, the positive link between animal diversity and pathogen richness urges us to apply this concept with caution. It is crucial to explore how conservation biology can safeguard human health by preventing the emergence of zoonotic diseases. By investigating the implications of conservation strategies on animal communities and pathogen transmission as well as the adaptive capabilities of pathogens, we propose that biodiversity conservation based on small reserves can effectively reduce pathogen spread in wildlife, provided certain measurable conditions are met. Given the urgent need to tackle both zoonoses disease emergence and biodiversity loss, these interventions should be prioritized and implemented without delay.

Keywords

References

1.

Ripple, W.J.; Wolf, C.; Newsome, T.M.; et al. World Scientists’ Warning to Humanity: A Second Notice. Bioscience 2017, 67, 1026–1028. https://doi.org/10.1093/biosci/bix125.

2.

Robinson, J.G. Conservation Biology and Real-World Conservation. Conserv. Biol. 2006, 20, 658–669. https://doi.org/10.1111/j.1523-1739.2006.00469.x.

3.

Daszak, P.; Amuasi, J.; das Neves, C.G.; et al. IPBES (2020) Workshop Report on Biodiversity and Pandemics of the Intergovernmental Platform on Biodiversity and Ecosystem Services; IPBES Secretariat: Bonn, Germany, 2020. https://doi.org/10.5281/zenodo.4147317.

4.

Ostfeld, R.S.; Keesing, F. Biodiversity and Disease Risk: The Case of Lyme Disease. Conserv. Biol. 2000, 14, 722–728. https://doi.org/10.1046/j.1523-1739.2000.99014.x.

5.

Johnson, P.T.J.; Preston, D.L.; Hoverman, J.T.; et al. Biodiversity Decreases Disease through Predictable Changes in Host Community Competence. Nature 2013, 494, 230–233. https://doi.org/10.1038/nature11883.

6.

Keesing, F.; Ostfeld, R.S. Impacts of Biodiversity and Biodiversity Loss on Zoonotic Diseases. Proc. Natl. Acad. Sci. USA 2021, 118, e2023540118. https://doi.org/10.1073/pnas.2023540118.

7.

Ostfeld, R.S.; Keesing, F. Effects of Host Diversity on Infectious Disease. Annu. Rev. Ecol. Evol. Syst. 2012, 43, 157–182. https://doi.org/10.1146/annurev-ecolsys-102710-145022.

8.

Halliday, F.W.; Rohr, J.R. Measuring the Shape of the Biodiversity-Disease Relationship across Systems Reveals New Findings and Key Gaps. Nat. Commun. 2019, 10, 5032. https://doi.org/10.1038/s41467-019-13049-w.

9.

Khalil, H.; Ecke, F.; Evander, M.; et al. Declining Ecosystem Health and the Dilution Effect. Sci. Rep. 2016, 6, 31314. https://doi.org/10.1038/srep31314.

10.

Ferraguti, M.; Martínez-De la Puente, J.; Jiménez–Clavero, M.Á.; et al. A Field Test of the Dilution Effect Hypothesis in Four Avian Multi-Host Pathogens. PLoS Pathog. 2021, 17, e1009637. https://doi.org/10.1371/journal.ppat.1009637.

11.

Wood, C.L.; Lafferty, K.D.; DeLeo, G.; et al. Does Biodiversity Protect Humans against Infectious Disease? Ecology 2014, 95, 817–832. https://doi.org/10.1890/13-1041.1.

12.

Civitello, D.J.; Cohen, J.; Fatima, H.; et al. Biodiversity Inhibits Parasites: Broad Evidence for the Dilution Effect. Proc. Natl. Acad. Sci. USA 2015, 112, 8667–8671. https://doi.org/10.1073/pnas.1506279112.

13.

Halliday, F.W.; Rohr, J.R.; Laine, A. Biodiversity Loss Underlies the Dilution Effect of Biodiversity. Ecol. Lett. 2020, 23, 1611–1622. https://doi.org/10.1111/ele.13590.

14.

Mahon, M.B.; Sack, A.; Aleuy, O.A.; et al. A Meta-Analysis on Global Change Drivers and the Risk of Infectious Disease. Nature 2024, 629, 830–836.

15.

Young, H.S.; Wood, C.L.; Marm Kilpatrick, A.; et al. Conservation, Biodiversity and Infectious Disease: Scientific Evidence and Policy Implications. Philos. Trans. R. Soc. B Biol. Sci. 2017, 372, 20160124.

16.

Albers, H.J.; Lee, K.D.; Rushlow, J.R.; et al. Disease Risk from Human–Environment Interactions: Environment and Development Economics for Joint Conservation-Health Policy. Environ. Resour. Econ. 2020, 76, 929–944. https://doi.org/10.1007/s10640-020-00449-6.

17.

Hopkins, S.R.; Lafferty, K.D.; Wood, C.L.; et al. Evidence Gaps and Diversity among Potential Win–Win Solutions for Conservation and Human Infectious Disease Control. Lancet Planet Health 2022, 6, e694–e705.

18.

Gibb, R.; Redding, D.W.; Chin, K.Q.; et al. Zoonotic Host Diversity Increases in Human-Dominated Ecosystems. Nature 2020, 584, 398–402. https://doi.org/10.1038/s41586-020-2562-8.

19.

Connell, J. On the Role of Natural Enemies in Preventing Competitive Exclusion in Some Marine Animals and in Rain Forest Trees. Dyn. Popul. 1971, 298, 312.

20.

Janzen, D.H. Herbivores and the Number of Tree Species in Tropical Forests. Am. Nat. 1970, 104, 501–528. https://doi.org/10.1086/282687.

21.

Allan, B.F.; Keesing, F.; Ostfeld, R.S. Effect of Forest Fragmentation on Lyme Disease Risk. Conserv. Biol. 2003, 17, 267–272. https://doi.org/10.1046/j.1523-1739.2003.01260.x.

22.

Kilpatrick, A.M.; Salkeld, D.J.; Titcomb, G.; et al. Conservation of Biodiversity as a Strategy for Improving Human Health and Well-Being. Philos. Trans. R. Soc. B Biol. Sci. 2017, 372, 20160131. https://doi.org/10.1098/rstb.2016.0131.

23.

Simberloff, D.; Abele, L.G. Refuge Design and Island Biogeographic Theory: Effects of Fragmentation. Am. Nat. 1982, 120, 41–50. https://doi.org/10.1086/283968.

24.

Hosseini, P.R.; Mills, J.N.; Prieur-Richard, A.H.; et al. Does the Impact of Biodiversity Differ between Emerging and Endemic Pathogens? The Need to Separate the Concepts of Hazard and Risk. Philos. Trans. R. Soc. B Biol. Sci. 2017, 372, 20160129. https://doi.org/10.1098/rstb.2016.0129.

25.

Lambert, S.; Gilot-Fromont, E.; Toïgo, C.; et al. An Individual-Based Model to Assess the Spatial and Individual Heterogeneity of Brucella Melitensis Transmission in Alpine Ibex. Ecol. Modell. 2020, 425, 109009. https://doi.org/10.1016/j.ecolmodel.2020.109009.

26.

Boecklen, W.J. Nestedness, Biogeographic Theory, and the Design of Nature Reserves. Oecologia 1997, 112, 123–142. https://doi.org/10.1007/s004420050292.

27.

Skaggs, R.W.; Boecklen, W.J. Extinctions of Montane Mammals Reconsidered: Putting a Global-Warming Scenario on Ice. Biodivers. Conserv. 1996, 5, 759–778. https://doi.org/10.1007/BF00051785.

28.

Etienne, R.S.; Heesterbeek, J.A.P. On Optimal Size and Number of Reserves for Metapopulation Persistence. J. Theor. Biol. 2000, 203, 33–50. https://doi.org/10.1006/jtbi.1999.1060.

29.

Ovaskainen, O. Long-Term Persistence of Species and the SLOSS Problem. J. Theor. Biol. 2002, 218, 419–433. https://doi.org/10.1016/S0022-5193(02)93089-4.

30.

Connor, E.F.; McCoy, E.D. The Statistics and Biology of the Species-Area Relationship. Am. Nat. 1979, 113, 791–833. https://doi.org/10.1086/283438.

31.

Diamond, J.M. The island dilemma: Lessons of modern biogeographic studies for the design of natural reserves. Biol. Conserv. 1975, 7, 129–146. https://doi.org/10.1016/0006-3207(75)90052-X.

32.

Mittermeier, R.A.; Gil, P.G.; Hoffman, M.; et al. Hotspots Revisited. Earth’s Biologically Richest and Most Endangered Terrestrial Ecoregions; Cemex: San Pedro Garza Garcia, Mexico, 2004.

33.

Mittermeier, R.A.; Turner, W.R.; Larsen, F.W.; et al. Global Biodiversity Conservation: The Critical Role of Hotpots. In Biodiversity Hotspost; Springer: Berlin/Heidelberg, Germany, 2011; pp. 3–22. ISBN 978-3-642-20991-8.

34.

Eken, G.; Bennun, L.; Brooks, T.M.; et al. Key Biodiversity Areas as Site Conservation Targets. Bioscience 2004, 54, 1110–1118. https://doi.org/10.1641/0006-3568(2004)054[1110:kbaasc]2.0.co;2.

35.

Langhammer, P.F.; Bakarr, M.I.; Bennun, L.A.; et al. Identification and Gap Analysis of Key Biodiversity Areas: Targets for Comprehensive Protected Area Systems; IUCN: Gland, Switzerland, 2007.

36.

VanAcker, M.C.; Little, E.A.H.; Molaei, G.; et al. Enhancement of Risk for Lyme Disease by Landscape Connectivity, New York, New York, USA. Emerg. Infect. Dis. 2019, 25, 1136. https://doi.org/10.3201/eid2506.181741.

37.

McCallum, H.; Dobson, A. Disease, Habitat Fragmentation and Conservation. Proc. R. Soc. London. Ser. B Biol. Sci. 2002, 269, 2041–2049. https://doi.org/10.1098/rspb.2002.2079.

38.

Gandon, S.; Capowiez, Y.; Dubois, Y.; et al. Local Adaptation and Gene-for-Gene Coevolution in a Metapopulation Model. Proc. R. Soc. B Biol. Sci. 1996, 263, 1003–1009. https://doi.org/10.1098/rspb.1996.0148.

39.

Rubio, A.V.; Ávila-Flores, R.; Suzán, G. Responses of Small Mammals to Habitat Fragmentation: Epidemiological Considerations for Rodent-Borne Hantaviruses in the Americas. Ecohealth 2014, 11, 526–533. https://doi.org/10.1007/s10393-014-0944-9.

40.

Thompson, J.N. Specific Hypotheses on the Geographic Mosaic of Coevolution. Am. Nat. 1999, 153, S1–S14. https://doi.org/10.1086/303208.

41.

Laikre, L. Genetic Diversity Is Overlooked in International Conservation Policy Implementation. Conserv. Genet. 2010, 11, 349–354. https://doi.org/10.1007/s10592-009-0037-4.

42.

Courchamp, F.; Angulo, E.; Rivalan, P.; et al. Rarity Value and Species Extinction: The Anthropogenic Allee Effect. PLoS Biol. 2006, 4, e415. https://doi.org/10.1371/journal.pbio.0040415.

43.

Fischer, J.; Abson, D.J.; Butsic, V.; et al. Land Sparing versus Land Sharing: Moving Forward. Conserv. Lett. 2014, 7, 149–157. https://doi.org/10.1111/conl.12084.

44.

Hudson, P.J.; Dobson, A.P.; Lafferty, K.D. Is a Healthy Ecosystem One That Is Rich in Parasites? Trends Ecol. Evol. 2006, 21, 381–385.

45.

Koltz, A.M.; Civitello, D.J.; Becker, D.J.; et al. Sublethal Effects of Parasitism on Ruminants Can Have Cascading Consequences for Ecosystems. Proc. Natl. Acad. Sci. USA 2022, 119, e2117381119. https://doi.org/10.1073/pnas.2117381119.

46.

Keesing, F.; Ostfeld, R.S. Dilution Effects in Disease Ecology. Ecol. Lett. 2021, 24, 2490–2505. https://doi.org/10.1111/ele.13875.

47.

Estavillo, C.; Weyland, F.; Herrera, L. Zoonotic Disease Risk and Life-History Traits: Are Reservoirs Fast Life Species? Ecohealth 2022, 19, 390–401. https://doi.org/10.1007/s10393-022-01608-5.

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DOI

10.53941/dbgs.2025.100006

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Volume 1, Issue 2

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Arnal, A., Gozlan, R. E., Charbonnel, N., Bouilloud, M., Chaves, A., Lounnas , M., Gauthier-Clerc, M., Vigueras-Galván, A. L., Arnathau, C., Roiz, D., Bento, A. I., Morand, S., Walzer, C., Suzán, G., Sarmiento Silva, R. E., & Roche, B. (2025). Leveraging Small Biodiversity Reserves to Prevent Zoonotic Disease: Insights from Dilution Effect and Pathogen Adaptation Theories. Disease Biology, Genetics, and Socioecology, 1(2), 6. https://doi.org/10.53941/dbgs.2025.100006

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