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Biodiversity inhibits parasites: Broad evidence for the dilution effect
Open accessAbstract
Significance: The dilution effect hypothesis suggests that diverse ecological communities limit disease spread via several mechanisms. Therefore, biodiversity losses could worsen epidemics that harm humans and wildlife. However, there is contentious debate over whether the hypothesis applies broadly, especially for parasites that infect humans. We address this fundamental question with a formal meta-analysis of >200 assessments relating biodiversity to disease in >60 host–parasite systems. We find overwhelming evidence of dilution, which is independent of host density, study design, and type and specialization of parasites. A second analysis identified similar effects of diversity in plant–herbivore systems. Thus, biodiversity generally decreases parasitism and herbivory. Consequently, human-induced declines in biodiversity could increase human and wildlife diseases and decrease crop and forest production.
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“A rich literature on infectious diseases of wildlife, livestock, and plants demonstrates increased pathogen transmission when biodiversity is lost from some ecological communities (9, 53), supporting the generality of this relationship across nonzoonotic disease systems as well.”
From Impacts of biodiversity and biodiversity loss on zoonotic diseases (2021) · cites this paper as [9]
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“In contrast, biodiversity loss has been shown to often increase the risk of zoonotic diseases, for example, through the dilution effect (9).”
From Impacts of biodiversity and biodiversity loss on zoonotic diseases (2021) · cites this paper as [9]
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“But for decades, we have also known that under some conditions, high biological diversity can decrease the transmission of zoonotic diseases that have already become established (8, 9).”
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“However, a larger metaanalysis found that the dilution effect was as strong for zoonoses as for other types of diseases (9), a conclusion that was robust to criticisms from the authors of the earlier study (57, 58).”
From Impacts of biodiversity and biodiversity loss on zoonotic diseases (2021) · cites this paper as [9]
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Does the dilution effect generally occur in animal diseases?
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“Here we extracted the dataset from (Civitello et al. 2015), and tested whether the mean effect of host diversity on disease abundance differs between animal and plant diseases.”
BackgroundMethodInfluentialLambertini, C., Becker, C. G., Belasen, A. M., Valencia‐Aguilar, A., Nunes-de-Almeida, C. H. L., Betancourt‐Román, C. M., Rodríguez, D., Leite, D. D. S., Oliveira, I., Gasparini, J. L. R., et al. (2020) · Fungal ecology · doi:10.1016/j.funeco.2020.100995 · Cited by 41
Sun, Y., Chen, L., Zhang, S., Miao, Y., Zhang, Y., Li, Z., Zhao, J., Yu, L., Zhang, J., Qin, X., et al. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.888789 · Cited by 42
Esteve‐Gasent, M. D., Castro-Arellano, I., Feria-Arroyo, T. P., Patino, R., Li, A. Y., Medina, R. F., de León, A. Á. P., & Rodríguez‐Vivas, R. I. (2016) · Archives of Insect Biochemistry and Physiology · doi:10.1002/arch.21327 · Cited by 42
“This response has been named as the “dilution effect” (Civitello et al., 2015; LoGiudice et al., 2003; Lou et al., 2014; Turney et al., 2014).”
BackgroundBiodiversity loss and the ecology of infectious disease
Ostfeld, R. S. (2017) · The Lancet Planetary Health · doi:10.1016/s2542-5196(17)30010-4 · Cited by 45
Evans, T. S., Shi, Z., Boots, M., Liu, W., Olival, K. J., Xiao, X., VandeWoude, S., Brown, H. E., Chen, J., Civitello, D. J., et al. (2020) · EcoHealth · doi:10.1007/s10393-020-01471-2 · Cited by 39
“2) apply (Jones et al. 2008; Keesing et al. 2010; Murray and Daszak 2013; Morse 1995; Ostfeld and Keesing 2012; Civitello et al. 2015).”
MethodSelf-citationMass-flowering monoculture attracts bees, amplifying parasite prevalence
Cohen, H., Smith, G. P., Sardiñas, H., Zorn, J. F., McFrederick, Q. S., Woodard, S. H., & Ponisio, L. C. (2021) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2021.1369 · Cited by 40
“Because we screened for seven different parasites, the possible values for parasite richness within an individual ranged from 0 (no parasites 0 500 1000 1500 2000 2500 0 10 20 30 40 50 weedy margin hedgerow fr eq ue nc y non-crop floral abundance 0 20 40 60 80 100 120 140 0 0.2 0.4 0.6 0.8 1.0 pa…”
BackgroundInfluentialYamada, K., Valderrama, A., Gottdenker, N. L., Cerezo, L., Minakawa, N., Saldaña, A., Calzada, J. E., & Chaves, L. F. (2016) · Parasite Epidemiology and Control · doi:10.1016/j.parepi.2016.03.003 · Cited by 39
The Role of Ecological Linkage Mechanisms in Plasmodium knowlesi Transmission and Spread
Davidson, G., Chua, T. H., Cook, A. G., Speldewinde, P., & Weinstein, P. (2019) · EcoHealth · doi:10.1007/s10393-019-01395-6 · Cited by 38
Biogeographic historical legacies in the net primary productivity of Northern Hemisphere forests
Conradi, T., Meerbeek, K. V., Ordóñez, A., & Svenning, J. (2020) · Ecology Letters · doi:10.1111/ele.13481 · Cited by 38
“In addition, the presence of a range of seed, leaf and wood characteristics within a forest may prevent high abundances of consumers and pathogens (Civitello et al. 2015), and may contribute to stabilise NPP across years with variable environmental conditions (Allan et al.”
BackgroundInfluentialA survey of the pursuit–evasion problem in swarm intelligence
Mu, Z., Pan, J., Zhou, Z., Yu, J., & Cao, L. (2023) · Frontiers of Information Technology & Electronic Engineering · doi:10.1631/fitee.2200590 · Cited by 38
Quantifying landscape connectivity gaps between protected area and natural habitat
Mu, H., Guo, S., Li, X., Zhou, Y., Lü, Y., Du, X., Huang, J., Ma, C., Zhang, X., Xia, Z., et al. (2024) · Journal of Cleaner Production · doi:10.1016/j.jclepro.2024.140729 · Cited by 39
Parasite responses to large mammal loss in an African savanna
Weinstein, S. B., Titcomb, G., Agwanda, B. R., Riginos, C., & Young, H. S. (2017) · Ecology · doi:10.1002/ecy.1858 · Cited by 38
Huang, Z. Y. X., Xu, C., van Langevelde, F., Ma, Y., Langendoen, T., Mundkur, T., Si, Y., Tian, H., Kraus, R. H. S., Gilbert, M., et al. (2019) · Journal of Animal Ecology · doi:10.1111/1365-2656.12997 · Cited by 37
“Despite much evidence for the dilution effect (Ostfeld & Keesing 2012; 106 Civitello et al. 2015; Huang et al. 2017), its generality is still highly disputed (Randolph 107 & Dobson 2012; Young et al. 2013; Wood et al. 2014; Huang et al. 2016).”
BackgroundFloral resources shape parasite and pathogen dynamics in bees facing urbanization
Cohen, H., Ponisio, L. C., Russell, K. A., Philpott, S. M., & McFrederick, Q. S. (2022) · Molecular Ecology · doi:10.1111/mec.16374 · Cited by 42
“92 ± 0 .5 1 a success; Civitello et al., 2015; Keesing et al., 2006).”
Scale dependencies and generalism in host use shape virus prevalence
McLeish, M., Sacristán, S., Fraile, A., & García‐Arenal, F. (2017) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2017.2066 · Cited by 39
Evolving Food Safety Pressures in California's Central Coast Region
Olimpi, E. M., Baur, P., Echeverri, A., Gonthier, D. J., Karp, D. S., Kremen, C., Sciligo, A. R., & Master, K. T. D. (2019) · Frontiers in Sustainable Food Systems · doi:10.3389/fsufs.2019.00102 · Cited by 37
Does biodiversity protect humans against infectious disease? Comment
Levi, T., Massey, A. L., Holt, R. D., Keesing, F., Ostfeld, R. S., & Peres, C. A. (2016) · Ecology · doi:10.1890/15-354.1 · Cited by 36
“…authors have recently found in careful surveys of the literature increasing evidence, across a wide range of systems, to support the proposition that the conservation of biodiversity can also serve to reduce the transmission of infectious diseases (Civitello et al. 2015 ; Johnson et al. in press ).”
Liu, X., Chen, F., Lyu, S., Sun, D., & Zhou, S. (2018) · Ecology and Evolution · doi:10.1002/ece3.3749 · Cited by 35
“, 1999; Liu, Lyu, Zhou, & Bradshaw, 2016; Mitchell, Tilman, & Groth, 2002; Rottstock, Joshi, Kummer, & Fischer, 2014), and also meta- analysis (Civitello et al., 2015), have overwhelmingly documented dilution rather than amplification effects; however, the underlying mechanisms remain unclear.”
BackgroundInfluentialA field test of the dilution effect hypothesis in four avian multi-host pathogens
Ferraguti, M., la Puente, J. M., Jiménez‐Clavero, M. Á., Llorente, F., Roiz, D., Ruíz, S., Soriguer, R. C., & Figuerola, J. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009637 · Cited by 38
“[26] undertook a meta-analysis that found support for DEH in a wide range of host-parasite systems including pathogens with different transmission pathways, lifecycles, and host ranges, in both parasites that affect humans and others that only infect wildlife.”
BackgroundEvolution of interdisciplinarity in biodiversity science
Craven, D., Winter, M., Hotzel, K., Gaikwad, J., Eisenhauer, N., Hohmuth, M., König‐Ries, B., & Wirth, C. (2019) · Ecology and Evolution · doi:10.1002/ece3.5244 · Cited by 36
“…spatial scales (Chase et al., 2018; Price & Schmitz, 2016) as well as their implications for and linkages to other global political and societal challenges, such as climate change, human health, and poverty (Adams et al., 2004; Barnosky et al., 2012; Cardinale et al., 2012; Civitello et al., 2015).”
Santos, F. M., Barreto, W. T. G., de Macedo, G. C., Barros, J. H. D. S., Xavier, S. C. D. C., Garcia, C. M., Mourão, G. M., de Oliveira, J., Ribeiro, A. R., Porfírio, G. E. D. O., et al. (2019) · Acta Tropica · doi:10.1016/j.actatropica.2019.105098 · Cited by 34
Evidence that Passerine Birds Act as Amplifying Hosts for Usutu Virus Circulation
Roiz, D., Vázquez, A., Ruíz, S., Tenório, A., Soriguer, R. C., & Figuerola, J. (2019) · EcoHealth · doi:10.1007/s10393-019-01441-3 · Cited by 38
Gupta, P., Robin, V. V., & Dharmarajan, G. (2020) · Journal of Genetics · doi:10.1007/s12041-020-01225-7 · Cited by 36
Scott, J. L. (2020) · Tropical Medicine and Infectious Disease · doi:10.3390/tropicalmed5040175 · Cited by 34
“knowlesi and altered the behavior and transmission dynamics between the macaque, the vectors and humans [58,59,64].”
BackgroundOn the benefits of systematic reviews for wildlife parasitology
Haddaway, N. R., & Watson, M. J. (2016) · International Journal for Parasitology: Parasites and Wildlife · doi:10.1016/j.ijppaw.2016.05.002 · Cited by 31
“This may be a result of limitations in search method or of the studies (too small, poor methods, insufficient dose) Tompkins (2015) Aggregative full literature review Details of search strings used and databases searched, however no details of number of relevant publications identified through searching or screening,…”
BackgroundStevenson, P. (2023) · Animal Research and One Health · doi:10.1002/aro2.19 · Cited by 33
Pérez‐Rodríguez, A., Khimoun, A., Ollivier, A., Éraud, C., Faivre, B., & Garnier, S. (2018) · Ecography · doi:10.1111/ecog.03189 · Cited by 34
Hantavirus infection and biodiversity in the Americas
Vadell, M. V., Villafañe, I. E. G., & Carbajo, A. E. (2019) · Oecologia · doi:10.1007/s00442-019-04564-0 · Cited by 33
Giacinto, J. J., Fricker, G. A., Ritter, M. K., Yost, J., & Doremus, J. M. (2021) · PLoS ONE · doi:10.1371/journal.pone.0254973 · Cited by 33
How Individual Variation in Host Tolerance Affects Competence to Transmit Parasites
Burgan, S. C., Gervasi, S. S., Johnson, L. R., & Martin, L. B. (2018) · Physiological and Biochemical Zoology · doi:10.1086/701169 · Cited by 34
“This phenomenon is functionally equivalent to a dilution effect (Keesing et al. 2010; Civitello et al. 2015).”
BackgroundEvolutionary and ecological insights into the emergence of arthropod-borne viruses
Marklewitz, M., & Junglen, S. (2018) · Acta Tropica · doi:10.1016/j.actatropica.2018.10.006 · Cited by 32
Ecology of Fungal Plant Pathogens
Termorshuizen, A. J. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.funk-0013-2016 · Cited by 35
“The dilution effect hypothesis predicts a lower abundance of pathogens if their hosts occur in biodiverse plant communities (46).”
BackgroundStrauss, A. T., Bowling, A. M., Duffy, M. A., Cáceres, C. E., & Hall, S. R. (2018) · Functional Ecology · doi:10.1111/1365-2435.13066 · Cited by 39
“Dilution effects arise broadly (Civitello et al., 2015) when resistant “diluter” taxa interfere with transmission among more competent focal hosts (Ostfeld & Keesing, 2000), frequently via one or two mechanisms.”
BackgroundHernández-Martínez, J., Morales‐Malacara, J. B., Álvarez-Añorve, M. Y., Amador-Hernández, S., Oyama, K., & Ávila-Cabadilla, L. D. (2018) · Parasitology · doi:10.1017/s0031182018000732 · Cited by 32
Collins, C. D., Bever, J. D., & Hersh, M. H. (2020) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14325 · Cited by 34
Public health perspective on patterns of biodiversity and zoonotic disease
Salkeld, D. J., Padgett, K. A., Jones, J. H., & Antolin, M. F. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1517640112 · Cited by 31
Metadata
- Authors
- 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., & Rohr, J. R.
- Affiliations
- University of South Florida (US)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2015-06-11
- Volume
- 112
- Issue
- 28
- Pages
- 8667-8671
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4507196
- OpenAlex
- W1787861744
- Semantic Scholar
- 30ae28188a18cd22709c7ef13c462acd9260a5ea
- Cited by
- 758
- References
- 34
- Citations by year
- 2026: 38 · 2025: 72 · 2024: 83 · 2023: 61 · 2022: 81 · 2021: 114 · 2020: 78 · 2019: 61 · 2018: 54 · 2017: 51 · 2016: 49 · 2015: 14
- FWCI
- 50.68
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (EF-1241889, 1144244)
- HHS | National Institutes of Health (R01GM109499, F32AI112255)
- U.S. Department of Agriculture (NRI 2006-01370, 2009-35102-0543)
- U.S. Environmental Protection Agency (CAREER 83518801)
- Topics
- Life Sciences › Immunology and Microbiology › Parasitology › Parasite Biology and Host Interactions
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Zoonotic diseases and public health
- Physical Sciences › Environmental Science › Nature and Landscape Conservation › Ecology and Vegetation Dynamics Studies
- Keywords
- dilution effect, biodiversity, parasite abundance, host diversity, zoonoses, disease risk, host-parasite interactions, plant-herbivore interactions, herbivory, biodiversity loss, human disease, wildlife disease
- MeSH terms
- Animals, Disease Susceptibility, Host-Parasite Interactions, Humans, Parasitic Diseases, Biodiversity
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