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Species diversity concurrently dilutes and amplifies transmission in a zoonotic host-pathogen system through competing mechanisms.

ABSTRACT: In this era of unprecedented biodiversity loss and increased zoonotic disease emergence, it is imperative to understand the effects of biodiversity on zoonotic pathogen dynamics in wildlife. Whether increasing biodiversity should lead to a decrease or increase in infection prevalence, termed the dilution and amplification effects, respectively, has been hotly debated in disease ecology. Sin Nombre hantavirus, which has an ?35% mortality rate when it spills over into humans, occurs at a lower prevalence in the reservoir host, the North American deermouse, in areas with higher small mammal diversity-a dilution effect. However, the mechanism driving this relationship is not understood. Using a mechanistic mathematical model of infection dynamics and a unique long-term, high-resolution, multisite dataset, it appears that the observed dilution effect is a result of increasing small-mammal diversity leading to decreased deermouse population density and, subsequently, prevalence (a result of density-dependent transmission). However, once density is taken into account, there is an increase in the transmission rate at sites with higher diversity-a component amplification effect. Therefore, dilution and amplification are occurring at the same time in the same host-pathogen system; there is a component amplification effect (increase in transmission rate), but overall a net dilution because the effect of diversity on reservoir host population density is stronger. These results suggest we should focus on how biodiversity affects individual mechanisms that drive prevalence and their relative strengths if we want to make generalizable predictions across host-pathogen systems.

SUBMITTER: Luis AD

PROVIDER: S-EPMC6077700 | biostudies-literature | 2018 Jul

REPOSITORIES: biostudies-literature

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Species diversity concurrently dilutes and amplifies transmission in a zoonotic host-pathogen system through competing mechanisms.

Luis Angela D AD Kuenzi Amy J AJ Mills James N JN

Proceedings of the National Academy of Sciences of the United States of America 20180716 31

In this era of unprecedented biodiversity loss and increased zoonotic disease emergence, it is imperative to understand the effects of biodiversity on zoonotic pathogen dynamics in wildlife. Whether increasing biodiversity should lead to a decrease or increase in infection prevalence, termed the dilution and amplification effects, respectively, has been hotly debated in disease ecology. Sin Nombre hantavirus, which has an ∼35% mortality rate when it spills over into humans, occurs at a lower pre ...[more]

PMID: 30012590

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Project description:BACKGROUND:Vector-borne pathogens must overcome arthropod infection and escape barriers (e.g. midgut and salivary glands) during the extrinsic incubation period (EIP) before subsequent transmission to another host. This particular timespan is undetermined for the etiological agent of flea-borne spotted fever (Rickettsia felis). Artificial acquisition of R. felis by blood-feeding cat fleas revealed dissemination to the salivary glands after seven days; however, this length of time is inconsistent with co-feeding studies that produced infectious cat fleas within 24 h of infection. In the current study, we demonstrated that an alternative mechanism is responsible for the early-phase transmission that typifies flea-borne R. felis spread. METHODS:Co-feeding transmission bioassays were constructed to assess temporal dynamics of R. felis amongst cat fleas, including exposure time to produce infectious fleas and association time to transmit infection to naïve fleas. Additional experiments examined the proportion of R. felis-exposed cat fleas with contaminated mouthparts, as well as the likelihood for cat fleas to release R. felis from their mouthparts following exposure to an infectious bloodmeal. The potential for mechanical transmission of R. felis by co-feeding cat fleas was further examined using fluorescent latex beads, as opposed to a live pathogen, which would not require a biological mechanism to achieve transmission. RESULTS:Analyses revealed that R. felis-infected cat fleas were infectious to naïve fleas less than 24 h after exposure to the pathogen, but showed no rickettsial dissemination to the salivary glands during this early-phase transmission. Additionally, the current study revealed that R. felis-infected cat fleas must co-feed with naïve fleas for more than 12 h in order for early-phase transmission to occur. Further evidence supported that contaminated flea mouthparts may be the source of the bacteria transmitted early, and demonstrated that R. felis is released from the mouthparts during brief probing events. Moreover, the use of fluorescent latex beads supports the notion that early-phase transmission of R. felis is a mechanical mechanism. CONCLUSIONS:Determination of the transmission mechanisms utilized by R. felis is essential to fully understand the vulnerability of susceptible vertebrate hosts, including humans, to this pathogen.

Project description:The degree to which plant pathogen infestation occurs in a host plant is expected to be strongly influenced by the level of species diversity among neighbouring host and non-host plant species. Since pathogen infestation can negatively affect host plant performance, it can mediate the effects of local biodiversity on ecosystem functioning.We tested the effects of tree diversity and the proportion of neighbouring host and non-host species with respect to the foliar fungal pathogens of Tilia cordata and Quercus petraea in the Kreinitz tree diversity experiment in Germany. We hypothesized that fungal pathogen richness increases while infestation decreases with increasing local tree diversity. In addition, we tested whether fungal pathogen richness and infestation are dependent on the proportion of host plant species present or on the proportion of particular non-host neighbouring tree species.Leaves of the two target species were sampled across three consecutive years with visible foliar fungal pathogens on the leaf surface being identified macro- and microscopically. Effects of diversity among neighbouring trees were analysed: (i) for total fungal species richness and fungal infestation on host trees and (ii) for infestation by individual fungal species.We detected four and five fungal species on T. cordata and Q. petraea, respectively. High local tree diversity reduced (i) total fungal species richness and infestation of T. cordata and fungal infestation of Q. petraea and (ii) infestation by three host-specialized fungal pathogen species. These effects were brought about by local tree diversity and were independent of host species proportion. In general, host species proportion had almost no effect on fungal species richness and infestation. Strong effects associated with the proportion of particular non-host neighbouring tree species on fungal species richness and infestation were, however, recorded.Synthesis. For the first time, we experimentally demonstrated that for two common forestry tree species, foliar fungal pathogen richness and infestation depend on local biodiversity. Thus, local tree diversity can have positive impacts on ecosystem functioning in managed forests by decreasing the level of fungal pathogen infestation.

Dataset Information

Species diversity concurrently dilutes and amplifies transmission in a zoonotic host-pathogen system through competing mechanisms.

Publications

Species diversity concurrently dilutes and amplifies transmission in a zoonotic host-pathogen system through competing mechanisms.

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