Biodiversity inhibits parasites: Broad evidence for the dilution effect

Abstract

Infectious diseases of humans, wildlife, and domesticated species are increasing worldwide, driving the need to understand the mechanisms that shape outbreaks. Simultaneously, human activities are drastically reducing biodiversity. These concurrent patterns have prompted repeated suggestions that biodiversity and disease are linked. For example, the dilution effect hypothesis posits that these patterns are causally related; diverse host communities inhibit the spread of parasites via several mechanisms, such as by regulating populations of susceptible hosts or interfering with parasite transmission. However, the generality of the dilution effect hypothesis remains controversial, especially for zoonotic diseases of humans. Here we provide broad evidence that host diversity inhibits parasite abundance using a metaanalysis of 202 effect sizes on 61 parasite species. The magnitude of these effects was independent of host density, study design, and type and specialization of parasites, indicating that dilution was robust across all ecological contexts examined. However, the magnitude of dilution was more closely related to the frequency, rather than density, of focal host species. Importantly, observational studies overwhelmingly documented dilution effects, and there was also significant evidence for dilution effects of zoonotic parasites of humans. Thus, dilution effects occur commonly in nature, and they may modulate human disease risk. A second analysis identified similar effects of diversity in plant-herbivore systems. Thus, although there can be exceptions, our results indicate that biodiversity generally decreases parasitism and herbivory. Consequently, anthropogenic declines in biodiversity could increase human and wildlife diseases and decrease crop and forest production.H uman activities are dramatically reducing biodiversity (1), and the frequency and severity of infectious disease outbreaks in human, wildlife, and domesticated species are increasing (2-5). These concurrent patterns have prompted suggestions that biodiversity and the spread of diseases may be causally linked. For example, the dilution effect hypothesis proposes that diverse host communities inhibit the abundance of parasites through several mechanisms, such as regulating populations of susceptible hosts or interfering with the transmission process (6-8). Thus, diverse communities may inhibit the proliferation of parasites, thereby promoting the stability of ecological communities and ecosystem services (e.g., nutrient cycling, carbon sequestration, and natural product production) (9).Understanding the generality of these dilution effects is crucial for projections of future disease outbreaks, which can threaten human health, species conservation, and ecosystem services (3, 9). If biodiversity generally inhibits parasites, then human-driven biodiversity loss could exacerbate disease risk for humans and wildlife. Biodiversity conservation might then limit the abundance of many parasites of wildlife and humans (10-12). However, if parasites a...

Spatial scale modulates the strength of ecological processes driving disease distributions

“…The third pathogen, the chytrid fungus Batrachochytrium dendrobatidis (Bd), is considered one of the deadliest organisms on the planet because of its association with hundreds of amphibian extinctions in the last half century (21,22). We chose to model the spatial factors affecting these pathogens because (i) spatially explicit datasets of their distributions were available (but were not available for other pathogens or other organisms in general; see Methods); (ii) they span a diversity of taxa (a virus, bacterium, and fungus) and transmission modes (WNV and Lyme are mosquito-and tick-borne, respectively, and Bd is a directly transmitted, water-borne pathogen), and infect various types of hosts (endothermic and ectothermic), increasing the generality of our findings; (iii) they are widespread generalists throughout the United States, providing a spatial extent great enough to conduct largescale analyses; (iv) their abundances or prevalences appear to be partially controlled by a common biotic factor, the richness of potential hosts (19,21,23,24), and by common abiotic factors, including climate and vegetation (20,25,26); and, finally, (v) understanding emerging diseases is of critical importance to biodiversity conservation and human health. Our goal was not to develop and put forth the best possible model to explain the spread of these diseases but rather to test whether spatial scale influences which types of ecological processes are important.…”

“…Because the abundance of all three pathogens has been shown previously to be affected by a common biotic factor, the richness of potential hosts (defined as the richness of all species that receive either successful or failed transmission attempts from a generalist pathogen or vector) (19,21,23,24), we chose to use this factor in our models to represent the subset of biotic interactions that drive the processes causing dilution or amplification effects (5). We used total amphibian richness to predict the spread of Bd, avian richness for WNV, and mammalian richness for Lyme disease (we also initially tested the richness of other taxa for B. burgdorferi; see Methods).…”

Biodiversity promotes primary productivity and growing season lengthening at the landscape scale

“…These biodiversity-ecosystem functioning (BEF) studies have revealed generally positive effects of species richness on primary productivity and also shed light on the mechanisms that promote productivity under these conditions (3). Niche differentiation among species can enhance community-level productivity through complementary resource use, decreased competition (3), and reduced density-dependent herbivore and pathogen pressure (4). Facilitation can increase community-level productivity via positive effects of one species on another.…”

The wild life of tick-borne pathogens

“…However, systems might not always meet these conditions, which has sparked an intense debate over the generality of the dilution effect of host species richness 158,270,271 . A recent meta-analysis concluded that the majority of studies showed a decrease of pathogen prevalence with increasing species richness 251 . Of course this is good news for conservationists trying to convince governments to preserve biodiversity.…”

“…For tick-borne pathogens vectored by a generalist species, the main conditions for a dilution effect to occur are that 1) pathogen prevalence increases with the density of host species with the highest reservoir competence and that 2) the density of these host species decreases with host species richness 3 . It has been shown that a dilution effect of host species richness occurs in many disease systems 251 , including the Lyme borreliosis system in North America, where a dilution effect of host species richness was found both at a small 230 and a large spatial scale 248 . However, the mechanisms underlying any negative correlation with host species richness remain relatively unstudied 218 .…”