scholarly journals Toward a unified dilution effect theory: How competence, competition, and the transmission mechanism influence disease prevalence

2020 ◽  
Author(s):  
Michael H. Cortez ◽  
Meghan A. Duffy

ABSTRACTBiodiversity in communities is changing globally, including the gain and loss of host species in host-pathogen communities. The dilution effect argues for a mechanistic link between increased host diversity and decreased disease in a focal host. However, we currently have a limited understanding of how the pathogen transmission mechanism and between-host interactions influence whether increased host diversity leads to increased (amplification) or decreased (dilution) infection prevalence. We use a two-host-one-pathogen model to unify theory for pathogens with environmental transmission and density-dependent and frequency-dependent direct transmission. We then identify general rules governing how the pathogen transmission mechanism and characteristics of the introduced host (disease competence and competitive ability) influence whether the introduction of a second host species increases or decreases disease prevalence in a focal host. We discuss how our results yield insight into how specific biological mechanisms shape host biodiversity-disease patterns.

Parasitology ◽  
2016 ◽  
Vol 143 (10) ◽  
pp. 1310-1319 ◽  
Author(s):  
SANNE C. RUYTS ◽  
EVY AMPOORTER ◽  
ELENA C. COIPAN ◽  
LANDER BAETEN ◽  
DIETER HEYLEN ◽  
...  

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.


2017 ◽  
Author(s):  
Brian J. Tornabene ◽  
Andrew R. Blaustein ◽  
Cheryl J. Briggs ◽  
Dana M. Calhoun ◽  
Pieter T. J. Johnson ◽  
...  

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.


Parasitology ◽  
2005 ◽  
Vol 130 (6) ◽  
pp. 661-668 ◽  
Author(s):  
S. TELFER ◽  
K. J. BOWN ◽  
R. SEKULES ◽  
M. BEGON ◽  
T. HAYDEN ◽  
...  

The potential of biological invasions to threaten native ecosystems is well recognized. Here we describe how an introduced species impacts on native host-parasite dynamics by acting as an alternative host. By sampling sites across an invasion front in Ireland, we quantified the influence of the introduced bank vole (Clethrionomys glareolus) on the epidemiology of infections caused by flea-transmitted haemoparasites of the genusBartonellain native wood mice (Apodemus sylvaticus).Bartonellainfections were detected on either side of the front but occurred exclusively in wood mice, despite being highly prevalent in both rodent species elsewhere in Europe. Bank vole introduction has, however, affected the wood mouse-Bartonellainteraction, with the infection prevalence of bothBartonella birtlesiiandBartonella tayloriideclining significantly with increasing bank vole density. Whilst flea prevalence in wood mice increases with wood mouse density in areas without bank voles, no such relationship is detected in invaded areas. The results are consistent with the dilution effect hypothesis. This predicts that for vector-transmitted parasites, the presence of less competent host species may reduce infection prevalence in the principal host. In addition we found a negative relationship betweenB. birtlesiiandB. tayloriiprevalences, indicating that these two microparasites may compete within hosts.


2017 ◽  
Vol 372 (1722) ◽  
pp. 20160173 ◽  
Author(s):  
Christina L. Faust ◽  
Andrew P. Dobson ◽  
Nicole Gottdenker ◽  
Laura S. P. Bloomfield ◽  
Hamish I. McCallum ◽  
...  

As biodiversity declines with anthropogenic land-use change, it is increasingly important to understand how changing biodiversity affects infectious disease risk. The dilution effect hypothesis, which points to decreases in biodiversity as critical to an increase in infection risk, has received considerable attention due to the allure of a win–win scenario for conservation and human well-being. Yet some empirical data suggest that the dilution effect is not a generalizable phenomenon. We explore the response of pathogen transmission dynamics to changes in biodiversity that are driven by habitat loss using an allometrically scaled multi-host model. With this model, we show that declining habitat, and thus declining biodiversity, can lead to either increasing or decreasing infectious-disease risk, measured as endemic prevalence. Whether larger habitats, and thus greater biodiversity, lead to a decrease (dilution effect) or increase (amplification effect) in infection prevalence depends upon the pathogen transmission mode and how host competence scales with body size. Dilution effects were detected for most frequency-transmitted pathogens and amplification effects were detected for density-dependent pathogens. Amplification effects were also observed over a particular range of habitat loss in frequency-dependent pathogens when we assumed that host competence was greatest in large-bodied species. By contrast, only amplification effects were observed for density-dependent pathogens; host competency only affected the magnitude of the effect. These models can be used to guide future empirical studies of biodiversity–disease relationships across gradients of habitat loss. The type of transmission, the relationship between host competence and community assembly, the identity of hosts contributing to transmission, and how transmission scales with area are essential factors to consider when elucidating the mechanisms driving disease risk in shrinking habitat. This article is part of the themed issue ‘Conservation, biodiversity and infectious disease: scientific evidence and policy implications'.


Author(s):  
Robert Creed ◽  
Gretchen L. Bailey ◽  
James Skelton ◽  
Bryan L. Brown

The dilution effect was originally proposed to describe the negative effect of increased host diversity on parasite abundance; with greater host diversity, parasite levels per host are predicted to be lower due to a higher probability of dispersing parasites encountering non-competent hosts. Dilution effects could also occur in many mutualisms if dispersing symbionts encounter hosts that vary in their competency. The introduction of non-native hosts can change community competency of a local group of host species. Crayfish introductions are occurring world-wide and these introductions are likely disrupting native crayfish-symbiont systems. Branchiobdellidan symbionts declined on native Cambarus crayfish occurring in the presence and absence of non-native Faxonius crayfish in the New River, USA. We performed an experiment investigating the effect of host density (1 vs 2 native hosts) and host diversity (1 native host and 1 introduced host) on branchiobdellidan abundance. The introduced F. cristavarius is a non-competent host for these worms. Six C. ingens were stocked on a C. chasmodactylus in each treatment and worm numbers were followed over 34 days. Worm numbers decreased over time on C. chasmodactylus alone and in the treatment in which a C. chasmodactylus was paired with an F. cristavarius. Worm numbers remained highest in the 2 C. chasmodactylus treatment . There was no significant effect of host diversity on worm reproduction. Crayfish invasions may have negative effects on mutualistic symbionts depending on the competence of introduced hosts. Loss of native symbionts is one of the potential hidden, negative effects of invasions on native freshwater diversity.


2000 ◽  
Vol 78 (12) ◽  
pp. 2061-2078 ◽  
Author(s):  
Richard S Ostfeld ◽  
Felicia Keesing

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.


2019 ◽  
Vol 7 (6) ◽  
pp. 182 ◽  
Author(s):  
Jose Angel Barasona ◽  
Christian Gortázar ◽  
José de la Fuente ◽  
Joaquín Vicente

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.


Author(s):  
Heather Ferguson ◽  
Patrick Brock ◽  
Steve Torr

The term “dilution effect” describes scenarios where pathogen transmission is reduced as host diversity increases. Theoretical frameworks exist to predict conditions under which dilution effects may arise, with vector-borne diseases (VBDs) being particularly susceptible to host diversity. However, to date, empirical investigation of dilution effects has been restricted to a few temperate VBD systems. We review the potential contribution of dilution effects for VBDs of greatest public health importance in low-income, typically tropical, countries. Using examples, we discuss how the underlying ecology of pathogen and vector species combine to determine the response of the disease system to biodiversity. We review cases demonstrating how manipulation of host-species diversity has altered human exposure risk. We caution that attempts to control VBDs by manipulating host diversity are unlikely to succeed, and may even be detrimental, without having a detailed understanding of the local ecology of the specific VBD and environmental setting.


Parasitology ◽  
2004 ◽  
Vol 129 (S1) ◽  
pp. S177-S189 ◽  
Author(s):  
P. A. NUTTALL ◽  
M. LABUDA

The skin site at which ticks attach to their hosts to feed is the critical interface between the tick and its host, and tick-borne pathogens. This site is highly modified by the pharmacologically active molecules secreted in tick saliva. For pathogens, it is an ecologically privileged niche that many exploit. Such exploitation is referred to as saliva-activated transmission (SAT) – the indirect promotion of tick-borne pathogen transmission via the actions of bioactive tick saliva molecules on the vertebrate host. Here we review evidence for SAT and consider what are the most likely candidates for SAT factors among the tick pharmacopoeia of anti-haemostatic, anti-inflammatory and immunomodulatory molecules identified to date. SAT factors appear to differ for different pathogens and tick vector species, and possibly even depend on the vertebrate host species. Most likely we are searching for a suite of molecules that act together to overcome the redundancy in host response mechanisms. Whatever they turn out to be, the quest to identify the tick molecules that mediate SAT is an exciting one, and offers new insights to controlling ticks and tick-borne diseases.


2014 ◽  
Vol 281 (1795) ◽  
pp. 20141796 ◽  
Author(s):  
C. Guilherme Becker ◽  
David Rodriguez ◽  
L. Felipe Toledo ◽  
Ana V. Longo ◽  
Carolina Lambertini ◽  
...  

The ‘dilution effect’ (DE) hypothesis predicts that diverse host communities will show reduced disease. The underlying causes of pathogen dilution are complex, because they involve non-additive (driven by host interactions and differential habitat use) and additive (controlled by host species composition) mechanisms. Here, we used measures of complementarity and selection traditionally employed in the field of biodiversity–ecosystem function (BEF) to quantify the net effect of host diversity on disease dynamics of the amphibian-killing fungus Batrachochytrium dendrobatidis ( Bd ). Complementarity occurs when average infection load in diverse host assemblages departs from that of each component species in uniform populations. Selection measures the disproportionate impact of a particular species in diverse assemblages compared with its performance in uniform populations, and therefore has strong additive and non-additive properties. We experimentally infected tropical amphibian species of varying life histories, in single- and multi-host treatments, and measured individual Bd infection loads. Host diversity reduced Bd infection in amphibians through a mechanism analogous to complementarity ( sensu BEF), potentially by reducing shared habitat use and transmission among hosts. Additionally, the selection component indicated that one particular terrestrial species showed reduced infection loads in diverse assemblages at the expense of neighbouring aquatic hosts becoming heavily infected. By partitioning components of diversity, our findings underscore the importance of additive and non-additive mechanisms underlying the DE.


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