Changes in host species diversity have been described as important factors influencing transmission risk of infectious diseases. More diverse assemblages would support a greater fraction of low-competence hosts, and therefore biodiversity losses may have the potential to increase disease (“dilution effect”) [1
]. However, the principle underlying this phenomenon remains unknown. Some studies have claimed that healthy ecosystems may actually be richer in parasite diversity and biodiversity, even on a global scale, with this being associated with increased risk of zoonotic pathogens [3
]; while others argue that preserving intact ecosystems and their endemic biodiversity should generally reduce the prevalence of infectious diseases [6
]. In order to establish whether disease emergence, maintenance and risk of transmission maybe determined by particular host community assemblages, specific but diverse examples are required [8
The outcome of host richness changes for infectious disease risk depends on a community´s ability to support infection–community competence [1
]. In this study, we aimed to establish the correlation between host species richness and the competence of the whole community [1
] to maintain and transmit tuberculosis (TB) in managed scenarios from Mediterranean Spain. We used a multi-host pathogen system that is well suited to address questions involving assembly because it provided replicate assemblages and a gradient of host richness (here, 1 to 4 species). TB caused by members of the Mycobacterium tuberculosis
complex (MTC) affects a wide range of susceptible mammal species [7
]. TB infection presents particularities: it usually develops into chronic infections, with long-term persistence in populations and low induced immunity. MTC is therefore able to induce a period of infectiousness in which direct contact between individuals occurs, which may favour transmission by both direct and indirect contact. However, the role of wildlife species has often been evaluated in single-species studies, neglecting the effects of multiple hosts and community structure on the MTC dynamics [11
]. Studies which adopt a community perspective are therefore needed to better understand the complex effect of the structure of livestock and wildlife populations on MTC transmission scenarios [7
]. This study thus aims to demonstrate whether ungulate host species richness operates with increased or decreased community competence to maintain and transmit the MTC.
We found a 46% increase in community competence for transmitting and maintaining TB (realized transmission) in richer assemblages with three or four species (average ± SE, 18.96 ± 9.63) compared with estates where only one species is present (10.29 ± 2.87; LM, f.d. = 2, F = 3.32, p
= 0.046; Figure 1
a). However, no effect in community competence was related to host abundance rates (LM, f.d. = 1, F = 1.349, p
Reservoir competence for TB varied widely among ungulate species (Kruskal–Wallis test, Z = 34.88, p
< 0.001), remarking the higher values for wild boar all over the gradient of community richness (Figure 1
b). The introduction of less frequent but still highly competent hosts in more rich assemblages increased host community competence for TB (Figure 1
b). This was not attributable to changes in the abundance of the most competent hosts as infection increased without changes in general or specific host abundance (Spearman’s rank correlations, p
> 0.05, Figure 1
c and Figure 2
This study set out with the aim of assessing the importance of the host–pathogen interaction paradigm in a host rich community. While highlighting the benefit of a community-based approach to the study of infectious diseases [1
], our findings provide evidence that increases in biodiversity do not necessarily reduce disease risk, at least in managed scenarios. Major factors distinguished some infectious agents from others [23
] since life history affects parasite virulence, transmissibility, specificity as well as host defenses, and life strategies [24
]. For example, a recent study [1
] has provided seminal empirical and experimental evidence that amphibian species richness in natural communities negatively moderates the transmission and disease caused by the trematode, Ribeiroia ondatrae
, which could be explained by the fact that defenses are costly and incur in trade-offs with resource investment.
However, many of the infection patterns of microparasites such as mycobacteria causing TB are determined by their ability to directly multiply in in the host, regardless of the host life history traits. A possible explanation is that a mass-action mode of transmission would benefit from increased niches offered by higher host diversity, resulting also in increased and more diverse networks of direct and indirect contacts (trophic relationships and host aggregation) [19
], preventing the dilution effect. This evidence applies in particular to multi-host pathogens such as mycobacteria capable of persisting in the environment [25
]. Most infections with these pathogens increase fitness costs only at very advanced stages, thus posing no important risk for species extinction in the community during most of their life span.
While existing studies have provided excellent scientifically supported examples with contrasting results, they often refer to very specific host communities and parasite assemblages. However, the TB case examined in this study demonstrates how a pathogen can interact in different ways with host communities, since parasite transmission and persistence is a complex interplay between hosts and parasites [14
]. Furthermore, our findings contrast with similar approaches in Africa where the incompetent host species for MTC transmission are more likely to be present in high-diversity communities rather than in low-diversity communities [7
]. Results from different epidemiological scenarios confer an additional value to the study of multi-host pathogens in wildlife populations. Although communities´ assembled richness is desirable for ecosystems function and conservation, its role in controlling infectious diseases remains debatable. It is also necessary to provide a deeper understanding of the epidemiology, because the plethora of associated pathogens may respond differently to changes in biodiversity.
In sum, if there is an argument to be made for redirecting scarce public health or conservation resources, it is critical to understand whether the relationship between biodiversity and disease risk is as general as has been suggested. However, we are unaware of any formal assessment of the generality of the dilution effect [28
]. If there is no straight forward relationship between biodiversity and risk of zoonotic disease, then integrated approaches to disease control may require a more detailed understanding of the transmission ecology of a specific pathogen, vector and host species.