Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm

Randolph, Sarah; Dobson, Andrew D. M.

doi:10.1017/s0031182012000200

Cited by 330 publications

(436 citation statements)

References 149 publications

(232 reference statements)

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“…If increasing the number of species in a community reduces the density of competent hosts or the frequency of infected vectors, then biodiversity shows a suppressive 'dilution effect' on disease 16 . On the other hand, biodiversity may increase disease through a variety of mechanisms 15,17 . Pathogen spillover from one host species to another means that community composition as well as species diversity can influence disease dynamics 18 .…”

mentioning

confidence: 99%

Phylogenetic structure and host abundance drive disease pressure in communities

Parker

Saunders

Bontrager

et al. 2015

Nature

284

325

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Pathogens play an important part in shaping the structure and dynamics of natural communities, because species are not affected by them equally 1,2 . A shared goal of ecology and epidemiology is to predict when a species is most vulnerable to disease. A leading hypothesis asserts that the impact of disease should increase with host abundance, producing a 'rare-species advantage' 3-5 . However, the impact of a pathogen may be decoupled from host abundance, because most pathogens infect more than one species, leading to pathogen spillover onto closely related species 6,7 . Here we show that the phylogenetic and ecological structure of the surrounding community can be important predictors of disease pressure. We found that the amount of tissue lost to disease increased with the relative abundance of a species across a grassland plant community, and that this rare-species advantage had an additional phylogenetic component: disease pressure was stronger on species with many close relatives. We used a global model of pathogen sharing as a function of relatedness between hosts, which provided a robust predictor of relative disease pressure at the local scale. In our grassland, the total amount of disease was most accurately explained not by the abundance of the focal host alone, but by the abundance of all species in the community weighted by their phylogenetic distance to the host. Furthermore, the model strongly predicted observed disease pressure for 44 novel host species we introduced experimentally to our study site, providing evidence for a mechanism to explain why phylogenetically rare species are more likely to become invasive when introduced 8,9 . Our results demonstrate how the phylogenetic and ecological structure of communities can have a key role in disease dynamics, with implications for the maintenance of biodiversity, biotic resistance against introduced weeds, and the success of managed plants in agriculture and forestry.Plant pathogens can be important drivers of community diversity, structure and dynamics 1,2,10,11 . A basic premise of epidemiology is that pathogen transmission often increases with host density 12,13 . Densitydependent disease provides a mechanism for the maintenance of plant diversity in natural communities, in which locally uncommon species enjoy a rare-species advantage-based on lower enemy pressure-that mitigates the competitive impacts of dominant species 3-5 . Reports of density-dependent disease dynamics generally infer the potential effects on communities from studies of one or a few species 2 , while community-level studies 1 are scarce but essential to evaluate whether such a rarespecies advantage predicts patterns of disease across a community.An ongoing debate concerns how community context influences disease, and particularly whether biodiversity suppresses infection and emerging diseases 14,15 . If increasing the number of species in a community reduces the density of competent hosts or the frequency of infected vectors, then biodiversity shows a suppressive 'dilution e...

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mentioning

confidence: 99%

Phylogenetic structure and host abundance drive disease pressure in communities

Parker

Saunders

Bontrager

et al. 2015

Nature

284

325

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“…However, in such investigations, sound statistical inference can be hampered by a number of biological and perception issues that, if ignored, could lead to distorted representations of density variation patterns (Randolph and Dobson, 2012;Schulze et al, 1997). Two such issues are low and variable individual detection probabilities and aggregated spatial distributions.…”

Section: Discussionmentioning

confidence: 99%

“…However, tick survival and reproductive success on African wild hosts are currently poorly documented in the literature. Without such information it is difficult to evaluate the relevance of the dilution effect hypothesis in the present study (Randolph and Dobson, 2012).…”

Section: Host Diversity and Availabilitymentioning

confidence: 92%

Characterising African tick communities at a wild–domestic interface using repeated sampling protocols and models

Miguel¹,

Boulinier²,

Garine‐Wichatitsky³

et al. 2014

Acta Tropica

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The sharing of habitat by wild and domestic animals may result in pathogen transmission, notably via ectoparasite vectors such as ticks. Interfaces between protected and communal lands constitute sharp transitions between areas occupied by host communities that are extremely contrasted in terms of com-position, diversity and density. Empirical characterizations of tick communities and of their vertebrate hosts are strongly relevant for understanding the mechanisms leading to disease transmission between wild and domestic animals. In the present study we aimed at depicting the pattern of spatial variation in the density of immature ticks at such an interface located in Zimbabwe. At the end of the 2011 rainy season, we applied a hierarchical repeated protocol to collect ticks. We used the dragsampling method in the vegetation surrounding water pans used by ungulates in 3 distinct landscape compartments (i.e. national park, mixed compartment and communal lands) characterized by a differential use by wild and domestic hosts. We combined generalized linear mixed models with site occupancy models to (1) assess tick aggregation levels at different spatial scales, (2) identify and disentangle factors which influence the density and probability of tick detection, and (3) compare robust estimations of tick densities among the landscape compartments. Ticks belonging to the Amblyomma and Riphicephalus genuses were found to be the most abundant. At small scale, ticks were more often detected in the afternoon and were more abun-dant close to water pans for Amblyomma and Riphicephalus genuses. Riphicephalus spp. density was also higher in grassland and bushland vegetation types as compared to woodland vegetation type. At large scale, for the three detected genuses, density was much higher near water pans located in the communal lands as compared to the national park and mixed compartment. Given that host community's diversity is much lower in the communal areas than in the two other landscape compartments, these results are compatible with a dilution effect but not sufficient to demonstrate this effect without additional studies. Up to date, it is the first utilization of these rigorous sampling and statistical modelling methodologies to estimate tick density in African ecosystem simultaneously at large and small scales.

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“…This hypothesis has been highly debated, especially in the context of ticks from the I. ricinus complex and Lyme borreliosis 158,159 . Although our analysis did not examine the effect of differences in species richness, our methods could be used to quantify the relative contributions of different species in different assemblages, as long as differences in tick burden and density are accounted for.…”

Section: Host Species Diversitymentioning

confidence: 99%

The wild life of tick-borne pathogens

Hofmeester

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Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm

Cited by 330 publications

References 149 publications

Phylogenetic structure and host abundance drive disease pressure in communities

Phylogenetic structure and host abundance drive disease pressure in communities

Characterising African tick communities at a wild–domestic interface using repeated sampling protocols and models

The wild life of tick-borne pathogens

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