Biodiversity series: The function of biodiversity in the ecology of vector-borne zoonotic diseases

2000 ◽  
Vol 78 (12) ◽  
pp. 2061-2078 ◽  
Author(s):  
Richard S Ostfeld ◽  
Felicia Keesing
Keyword(s):  
Species Diversity ◽  
Lyme Disease ◽  
Host Species ◽  
Disease Risk ◽  
Feeding Habits ◽  
Dilution Effect ◽  
Tick Population ◽  
Infection Prevalence ◽  
Vector Borne ◽  
The Impact

This is a critical evaluation of the influence of species diversity within communities of vertebrates on the risk of human exposure to vector-borne zoonoses. Vertebrates serve as natural reservoirs of many disease agents (viral, bacterial, protozoal) that are transmitted to humans by blood-feeding arthropod vectors. We describe the natural history of the Lyme disease zoonosis to illustrate interactions among pathogens, vectors, vertebrate hosts, and risk to humans. We then describe how the presence of a diverse assemblage of vertebrates can dilute the impact of the principal reservoir (the white-footed mouse, Peromyscus leucopus) of Lyme disease spirochetes (Borrelia burgdorferi), thereby reducing the disease risk to humans. Exploring the logic of what we call the dilution effect reveals four conditions that are necessary for it to apply generally to vector-borne zoonoses: (1) the feeding habits of the vector are generalized; (2) the pathogen is acquired by the vector from hosts (as opposed to exclusively transovarial transmission); (3) reservoir competence (the ability of a particular host species to infect a vector) varies among host species; and (4) the most competent reservoir host tends to be a community dominant, as defined by the proportion of the tick population fed by that species. When these conditions are met, vertebrate communities with high species diversity will contain a greater proportion of incompetent reservoir hosts that deflect vector meals away from the most competent reservoirs, thereby reducing infection prevalence and disease risk. Incorporating the likelihood that the abundance of competent reservoirs is reduced in more diverse communities, owing to the presence of predators and competitors, reinforces the impact of the dilution effect on the density of infected vectors. A review of the literature reveals the generality, though not the universality, of these conditions, which suggests that the effects of diversity on disease risk may be widespread. Issues in need of further exploration include (i) the relative importance of diversity per se versus fluctuating numbers of particular species; (ii) the relevance of species richness versus evenness to the dilution effect; (iii) whether the dilution effect operates at both local and regional scales; and (iv) the shape of empirically determined curves relating diversity to measures of disease risk. Further studies linking community ecology with epidemiology are warranted.

scholarly journals Experimental Evidence for Opposing Effects of High Deer Density on Tick-Borne Pathogen Prevalence and Hazard

2021 ◽  
Author(s):  
Sara Louise Gandy ◽  
Elizabeth Kilbride ◽  
Roman Biek ◽  
Caroline Millins ◽  
Lucy Gilbert
Keyword(s):  
Lyme Disease ◽  
Disease Risk ◽  
Dilution Effect ◽  
High Density ◽  
Infection Prevalence ◽  
Vegetation Height ◽  
Deer Density ◽  
Pathogen Prevalence ◽  
Tick Reproduction ◽  
The Impact

Abstract Background: Identifying the mechanisms driving disease risk is challenging for multi-host pathogens, such as Borrelia burgdorferi s.l., the tick-borne bacteria causing Lyme disease. Deer are tick reproduction hosts but do not transmit B. burgdorferi s.l., whereas rodents and birds are competent transmission hosts. Here, we use a long-term deer exclosure experiment to test three mechanisms for how high deer density might shape B. burgdorferi s.l. prevalence in ticks: increased prevalence due to higher larval tick densities facilitating high transmission on rodents (M1); alternatively, reduced B. burgdorferi s.l. prevalence because more larval ticks feed on deer rather than transmission-competent rodents (dilution effect) (M2), potentially due to ecological cascades, whereby higher deer grazing pressure lowers vegetation which decreases rodent abundance thus reducing transmission (M3).Methods: In a large enclosure where red deer stags were kept at high density (32.5 deer/km²), we used an experimental design consisting of eight plots of 0.23ha, four being fenced to simulate the absence of deer and four that were accessible to deer. In each plot we measured the density of questing nymphs and nymphal infection prevalence in spring, summer and autumn and quantified vegetation height and density, and small mammal abundance Results: Prevalence tended to be lower, though not conclusively so, in high deer density plots compared to exclosures (predicted prevalence of 1.0% vs 2.2%), suggesting that the dilution (M2) and cascade (M3) mechanisms might outweigh the increased opportunities for transmission (M1). Presence of deer at high density led to lower vegetation and fewer rodents, consistent with an ecological cascade. However, Lyme disease hazard (density of infected I. ricinus nymphs) was five times higher in high deer density plots due to tick density being 18 times higher.Conclusion: High densities of tick reproduction hosts such as deer can drive up vector-borne disease hazard, despite the potential to simultaneously reduce pathogen prevalence. This has implications for environmental pathogen management and for deer management, although the impact of intermediate deer densities now needs testing.

scholarly journals Experimental evidence for opposing effects of high deer density on tick-borne pathogen prevalence and hazard

2021 ◽  
Vol 14 (1) ◽  
Author(s):  
Sara Gandy ◽  
Elizabeth Kilbride ◽  
Roman Biek ◽  
Caroline Millins ◽  
Lucy Gilbert
Keyword(s):  
Lyme Disease ◽  
Disease Risk ◽  
Dilution Effect ◽  
High Density ◽  
Infection Prevalence ◽  
Vegetation Height ◽  
Deer Density ◽  
Pathogen Prevalence ◽  
Tick Reproduction ◽  
The Impact

Abstract Background Identifying the mechanisms driving disease risk is challenging for multi-host pathogens, such as Borrelia burgdorferi sensu lato (s.l.), the tick-borne bacteria causing Lyme disease. Deer are tick reproduction hosts but do not transmit B. burgdorferi s.l., whereas rodents and birds are competent transmission hosts. Here, we use a long-term deer exclosure experiment to test three mechanisms for how high deer density might shape B. burgdorferi s.l. prevalence in ticks: increased prevalence due to higher larval tick densities facilitating high transmission on rodents (M1); alternatively, reduced B. burgdorferi s.l. prevalence because more larval ticks feed on deer rather than transmission-competent rodents (dilution effect) (M2), potentially due to ecological cascades, whereby higher deer grazing pressure shortens vegetation which decreases rodent abundance thus reducing transmission (M3). Methods In a large enclosure where red deer stags were kept at high density (35.5 deer km−2), we used an experimental design consisting of eight plots of 0.23 ha, four of which were fenced to simulate the absence of deer and four that were accessible to deer. In each plot we measured the density of questing nymphs and nymphal infection prevalence in spring, summer and autumn, and quantified vegetation height and density, and small mammal abundance. Results Prevalence tended to be lower, though not conclusively so, in high deer density plots compared to exclosures (predicted prevalence of 1.0% vs 2.2%), suggesting that the dilution and cascade mechanisms might outweigh the increased opportunities for transmission mechanism. Presence of deer at high density led to shorter vegetation and fewer rodents, consistent with an ecological cascade. However, Lyme disease hazard (density of infected I. ricinus nymphs) was five times higher in high deer density plots due to tick density being 18 times higher. Conclusions High densities of tick reproduction hosts such as deer can drive up vector-borne disease hazard, despite the potential to simultaneously reduce pathogen prevalence. This has implications for environmental pathogen management and for deer management, although the impact of intermediate deer densities now needs testing. Graphical abstract

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

Parasitology ◽  
2016 ◽  
Vol 143 (10) ◽  
pp. 1310-1319 ◽  
Author(s):  
SANNE C. RUYTS ◽  
EVY AMPOORTER ◽  
ELENA C. COIPAN ◽  
LANDER BAETEN ◽  
DIETER HEYLEN ◽  
...  
Keyword(s):  
North America ◽  
Lyme Disease ◽  
Borrelia Burgdorferi ◽  
Disease Risk ◽  
Severe Disease ◽  
Dilution Effect ◽  
Ixodid Ticks ◽  
Infection Prevalence ◽  
Host Diversity ◽  
Pine Stands

SUMMARYLyme disease is caused by bacteria of theBorrelia burgdorferigenospecies 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 analysedBorreliainfection 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 harbourBorrelia afzeliiinfection more often in pine stands whileBorrelia gariniiandBorrelia burgdorferiss. 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.

The diversity–disease relationship: evidence for and criticisms of the dilution effect

Parasitology ◽  
2016 ◽  
Vol 143 (9) ◽  
pp. 1075-1086 ◽  
Author(s):  
Z. Y. X. HUANG ◽  
F. VAN LANGEVELDE ◽  
A. ESTRADA-PEÑA ◽  
G. SUZÁN ◽  
W. F. DE BOER
Keyword(s):  
Species Diversity ◽  
Host Species ◽  
Disease Risk ◽  
Current Knowledge ◽  
Risk Measures ◽  
Extinction Risk ◽  
Meta Analysis ◽  
Negative Relationship ◽  
Dilution Effect ◽  
Landscape Fragmentation

SUMMARYThe dilution effect, that high host species diversity can reduce disease risk, has attracted much attention in the context of global biodiversity decline and increasing disease emergence. Recent studies have criticized the generality of the dilution effect and argued that it only occurs under certain circumstances. Nevertheless, evidence for the existence of a dilution effect was reported in about 80% of the studies that addressed the diversity–disease relationship, and a recent meta-analysis found that the dilution effect is widespread. We here review supporting and critical studies, point out the causes underlying the current disputes. The dilution is expected to be strong when the competent host species tend to remain when species diversity declines, characterized as a negative relationship between species’ reservoir competence and local extinction risk. We here conclude that most studies support a negative competence–extinction relationship. We then synthesize the current knowledge on how the diversity–disease relationship can be modified by particular species in community, by the scales of analyses, and by the disease risk measures. We also highlight the complex role of habitat fragmentation in the diversity–disease relationship from epidemiological, evolutionary and ecological perspectives, and construct a synthetic framework integrating these three perspectives. We suggest that future studies should test the diversity–disease relationship across different scales and consider the multiple effects of landscape fragmentation.

Snail species diversity impacts the infection patterns of Echinostoma spp.: Examples from field collected data

2017 ◽  
Vol 62 (3) ◽  
Author(s):  
Michael R. Zimmermann ◽  
Kyle E. Luth ◽  
Gerald W. Esch
Keyword(s):  
Species Diversity ◽  
Disease Risk ◽  
Dilution Effect ◽  
Field Studies ◽  
Snail Species ◽  
Larval Stages ◽  
Infection Dynamics ◽  
Risk Of Disease ◽  
The Impact

AbstractRapid losses of biodiversity due to the changing landscape have spurred increased interest in the role of species diversity and disease risk. A leading hypothesis for the importance of biodiversity in disease reduction is the dilution effect, which suggests that increasing species diversity within a system decreases the risk of disease among the organisms inhabiting it. The role of species diversity in trematode infection was investigated using field studies from sites across the U.S. to examine the impact of snail diversity in the infection dynamics of both first and second intermediate larval stages of

scholarly journals Host Richness Increases Tuberculosis Disease Risk in Game-Managed Areas

2019 ◽  
Vol 7 (6) ◽  
pp. 182 ◽  
Author(s):  
Jose Angel Barasona ◽  
Christian Gortázar ◽  
José de la Fuente ◽  
Joaquín Vicente
Keyword(s):  
Species Richness ◽  
Host Species ◽  
Life Histories ◽  
Disease Risk ◽  
Dilution Effect ◽  
Pathogen Transmission ◽  
Trade Offs ◽  
Community Assemblages ◽  
Animal Communities ◽  
The Impact

Current scientific debate addresses whether species richness in animal communities may negatively moderate pathogen transmission and disease outcome (dilution effect), or to the contrary, if disease emergence benefits from more diverse community assemblages (amplification effect). The result may not depend exclusively on patterns of host species biodiversity but may depend on the specific composition of reservoir hosts and vectors, and their ecology. Host–pathogen interactions have shaped variations in parasite virulence, transmissibility and specificity. In the same way the importance of factors related to host exposure or to life history trade-offs are expected to vary. In this study, we demonstrate that ungulate host species richness correlates with increased community competence to maintain and transmit pathogens of the Mycobacterium tuberculosis complex (MTC) in game-managed areas in Mediterranean Spain. Therefore, we should consider natural and artificial variations in life histories of pathogens and host communities to characterize the impact of biodiversity on the health of diverse assemblages of human and animal communities. Since most approaches assessing epidemiology and transmission of shared pathogens only involve single- or pair-species, further research is needed to better understand the infection dynamics from complete community assemblages, at least in chronic diseases such as tuberculosis and in non-natural animal communities.

scholarly journals Modelling the seasonality of Lyme disease risk and the potential impacts of a warming climate within the heterogeneous landscapes of Scotland

2016 ◽  
Vol 13 (116) ◽  
pp. 20160140 ◽  
Author(s):  
Sen Li ◽  
Lucy Gilbert ◽  
Paula A. Harrison ◽  
Mark D. A. Rounsevell
Keyword(s):  
Lyme Disease ◽  
Disease Risk ◽  
Pathogen Transmission ◽  
Borrelia Burgdorferi Sensu Lato ◽  
Tick Population ◽  
Risk Indicator ◽  
Risk Area ◽  
Heterogeneous Landscapes ◽  
Vector Borne ◽  
Lyme Disease Risk

Lyme disease is the most prevalent vector-borne disease in the temperate Northern Hemisphere. The abundance of infected nymphal ticks is commonly used as a Lyme disease risk indicator. Temperature can influence the dynamics of disease by shaping the activity and development of ticks and, hence, altering the contact pattern and pathogen transmission between ticks and their host animals. A mechanistic, agent-based model was developed to study the temperature-driven seasonality of Ixodes ricinus ticks and transmission of Borrelia burgdorferi sensu lato across mainland Scotland. Based on 12-year averaged temperature surfaces, our model predicted that Lyme disease risk currently peaks in autumn, approximately six weeks after the temperature peak. The risk was predicted to decrease with increasing altitude. Increases in temperature were predicted to prolong the duration of the tick questing season and expand the risk area to higher altitudinal and latitudinal regions. These predicted impacts on tick population ecology may be expected to lead to greater tick–host contacts under climate warming and, hence, greater risks of pathogen transmission. The model is useful in improving understanding of the spatial determinants and system mechanisms of Lyme disease pathogen transmission and its sensitivity to temperature changes.

scholarly journals Experimental Evidence for Opposing Effects of High Deer Density on Tick-Borne Disease Prevalence and Hazard

2021 ◽  
Author(s):  
Sara Louise Gandy ◽  
Elizabeth Kilbride ◽  
Roman Biek ◽  
Caroline Millins ◽  
Lucy Gilbert
Keyword(s):  
Lyme Disease ◽  
Disease Risk ◽  
Dilution Effect ◽  
Exclosure Experiment ◽  
Deer Density ◽  
Pathogen Prevalence ◽  
Tick Reproduction ◽  
Tick Borne Disease ◽  
Vector Borne ◽  
Opposing Effects

Abstract Identifying the mechanisms driving disease risk is challenging for multi-host pathogens, such as Borrelia. burgdorferi s.l., the tick-borne bacteria causing Lyme disease. Deer are tick reproduction hosts but do not transmit B. burgdorferi s.l., resulting in potentially opposing effects on transmission. Here, we use a deer exclosure experiment to test three hypotheses for how high deer density shapes B. burgdorferi s.l. prevalence in ticks: (H1) high transmission on rodents due to higher tick densities; alternatively, (H2) low B. burgdorferi s.l. prevalence because more ticks feed on deer rather than transmission-competent rodents (dilution effect); (H3) ecological cascades, whereby lower vegetation decreases rodent abundance thus reducing transmission. Although we found support for all three mechanisms, prevalence was reduced almost 3-fold in high deer density plots compared to exclosures, suggesting that the dilution (H2) and cascade (H3) mechanisms outweighed the increased opportunities for transmission (H1). High deer density led to lower vegetation and fewer rodents, providing evidence for an ecological cascade. However, Lyme disease hazard (density of infected ticks) was increased 5-fold at high deer densities due to an 18-fold rise in tick density. This demonstrates that reproduction hosts like deer can drive up vector-borne disease hazard at high densities, despite simultaneously reducing pathogen prevalence.

scholarly journals Impact of the experimental removal of lizards on Lyme disease risk

2011 ◽  
Vol 278 (1720) ◽  
pp. 2970-2978 ◽  
Author(s):  
Andrea Swei ◽  
Richard S. Ostfeld ◽  
Robert S. Lane ◽  
Cheryl J. Briggs
Keyword(s):  
Lyme Disease ◽  
Disease Ecology ◽  
Disease Risk ◽  
Large Fraction ◽  
Host Community ◽  
Deer Mice ◽  
Infection Prevalence ◽  
Alternate Host ◽  
Experimental Removal ◽  
Tick Infection

The distribution of vector meals in the host community is an important element of understanding and predicting vector-borne disease risk. Lizards (such as the western fence lizard; Sceloporus occidentalis ) play a unique role in Lyme disease ecology in the far-western United States. Lizards rather than mammals serve as the blood meal hosts for a large fraction of larval and nymphal western black-legged ticks ( Ixodes pacificus —the vector for Lyme disease in that region) but are not competent reservoirs for the pathogen, Borrelia burgdorferi . Prior studies have suggested that the net effect of lizards is to reduce risk of human exposure to Lyme disease, a hypothesis that we tested experimentally. Following experimental removal of lizards, we documented incomplete host switching by larval ticks (5.19%) from lizards to other hosts. Larval tick burdens increased on woodrats, a competent reservoir, but not on deer mice, a less competent pathogen reservoir. However, most larvae failed to find an alternate host. This resulted in significantly lower densities of nymphal ticks the following year. Unexpectedly, the removal of reservoir-incompetent lizards did not cause an increase in nymphal tick infection prevalence. The net result of lizard removal was a decrease in the density of infected nymphal ticks, and therefore a decreased risk to humans of Lyme disease. Our results indicate that an incompetent reservoir for a pathogen may, in fact, increase disease risk through the maintenance of higher vector density and therefore, higher density of infected vectors.

The influence of landscape and environmental factors on ranavirus epidemiology in amphibian assemblages

2017 ◽  
Author(s):  
Brian J. Tornabene ◽  
Andrew R. Blaustein ◽  
Cheryl J. Briggs ◽  
Dana M. Calhoun ◽  
Pieter T. J. Johnson ◽  
...  
Keyword(s):  
Environmental Factors ◽  
Host Species ◽  
Dilution Effect ◽  
Variance Partitioning ◽  
Lower Probability ◽  
Infection Prevalence ◽  
Taxonomic Richness ◽  
Amphibian Disease ◽  
Competing Models ◽  
Reservoir Hosts

ABSTRACTAimTo quantify the influence of a suite of landscape, abiotic, biotic, and host-level variables on ranavirus disease dynamics in amphibian assemblages at two biological levels (site and host-level).LocationWetlands within the East Bay region of California, USA.MethodsWe used competing models, multimodel inference, and variance partitioning to examine the influence of 16 landscape and environmental factors on patterns in site-level ranavirus presence and host-level ranavirus infection in 76 wetlands and 1,377 amphibian hosts representing five species.ResultsThe landscape factor explained more variation than any other factors in site-level ranavirus presence, but biotic and host-level factors explained more variation in host-level ranavirus infection. At both the site- and host-level, the probability of ranavirus presence correlated negatively with distance to nearest ranavirus-positive wetland. At the site-level, ranavirus presence was associated positively with taxonomic richness. However, infection prevalence within the amphibian population correlated negatively with vertebrate richness. Finally, amphibian host species differed in their likelihood of ranavirus infection: American Bullfrogs had the weakest association with infection while Western Toads had the strongest. After accounting for host species effects, hosts with greater snout-vent length had a lower probability of infection.Main conclusionsStrong spatial influences at both biological levels suggest that mobile taxa (e.g., adult amphibians, birds, reptiles) may facilitate the movement of ranavirus among hosts and across the landscape. Higher taxonomic richness at sites may provide more opportunities for colonization or the presence of reservoir hosts that may influence ranavirus presence. Higher host richness correlating with higher ranavirus infection is suggestive of a dilution effect that has been observed for other amphibian disease systems and warrants further investigation. Our study demonstrates that an array of landscape, environmental, and host-level factors were associated with ranavirus epidemiology and illustrates that their importance vary with biological level.

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