Recently, some researchers have emphasized the potential for undisturbed ecosystems to be sources of disservices and outright harm to humans (Burgin et al. 2013 , von Doehren and Haase 2015 ). Natural ecosystems certainly contain dangerous elements—venomous snakes, allergens, and natural fire regimes—that can, even when undisturbed, compromise human well‐being. Recently, it has been suggested that native biodiversity may be dangerous because it increases the probability that a new zoonotic disease will emerge, constituting an important ecosystem disservice (Jones et al. 2008 , Dunn 2010 , Dunn et al. 2010 , Johnson et al. 2015a ). If biodiversity poses a real health risk to humans, then enthusiasm for the conservation of biodiversity might be dampened by concerns about disease emergence. Here, we explore the evidence that high native biodiversity increases the likelihood of emergence of human infectious diseases. We compare the evidence concerning the effects of native biodiversity to that concerning anthropogenic changes in biodiversity affecting disease emergence and dynamics, and we reflect on the policy and management consequences of this evidence.

Natural ecosystems absorb and recycle nutrients; produce biomass, food, and water; modulate the impacts of physical forces on living organisms; and support the life cycles of myriad species of plants, animals, and microbes. When these functions are considered useful for humans, we term them “ecosystem services” (Millennium Ecosystem Assessment Program 2005 , Daily and Matson 2008 , Guerry et al. 2015 ). Natural ecosystems can also endanger human well‐being, for example, when fires and floods destroy lives and property or when dangerous animals and plants compromise human health. These negative effects of ecosystems on humans, sometimes termed “ecosystem disservices,” often arise when humans have altered natural ecosystems, inadvertently converting their positive effects into detriments (Dunn 2010 ). For example, the eutrophication of coastal waters can undermine the ability of these waters to support fisheries and recreation—an ecosystem service—and compromise human and animal health through harmful algal blooms—an ecosystem disservice.

Jeschke et al. ( 2013 ) described how a spillover event, or species jump from a non‐human vertebrate host to humans, is the first of several sequential steps required for emergence. Following spillover, establishment, spread, and impact on hosts are required to constitute an EID. For the latter three steps, evidence is accumulating that high biodiversity is strongly inhibitory (Keesing et al. 2010 , Ostfeld and Keesing 2012 , Civitello et al. 2015a , Johnson et al. 2015b ). Here, our main focus is on the first step—the spillover process.

Infectious diseases of humans can emerge through a variety of pathways, only some of which are related to biodiversity. For example, Rosenthal et al. ( 2015 ) identified seven mechanisms, or pathways, that have been used to identify emerging diseases or pathogens in humans: (1) when a disease increases in incidence, (2) when a disease increases in impact, (3) when a disease increases in geographic range, (4) when a pathogen has undergone recent evolutionary change, (5) when a pathogen is detected in the human population for the first time, (6) when a pathogen significantly changes its pathology or clinical presentation, or (7) when a pathogen is discovered for the first time. Despite the diversity of these mechanisms, most attention has been devoted to the “spillover” process, whereby a pathogen that is typically restricted to non‐human vertebrate hosts is transmitted to humans. Spillover to humans seems most compatible with pathways 4 or 5 above. However, these two pathways rank third and fifth of the seven in terms of frequency of occurrence in human emerging infectious disease (EID) events (Rosenthal et al. 2015 ). Despite the dominance by pathways that do not necessarily involve spillover, many conceptual models of human disease emergence emphasize the spillover pathways (e.g., Wolfe et al. 2007 , Jones et al. 2008 , Hatcher et al. 2012 , Gortazar et al. 2014 ).

The Logical Basis for the Argument that High Diversity Increases Disease Emergence

The notion that high native biodiversity increases the threat of human exposure to zoonotic diseases rests on the assumption that all vertebrates are potentially dangerous because any one might be the source of spillover that results in the next deadly EID (see Jones et al. 2008, Dunn et al. 2010). The precise mechanisms proposed to link high vertebrate diversity to high risk of zoonotic emergence are typically not specified. Here, we provide a logical structure and evaluate the evidence for this connection. In a later section, we evaluate an alternative causal pathway involving vertebrate diversity and the host range of pathogens.

The primary logic by which greater diversity could lead to higher zoonotic risk requires a three‐part causal chain connecting vertebrate diversity to pathogen diversity to risk of human exposure to a zoonotic EID (Fig. 1). First, the logic requires that the more species of mammals and birds there are in any given location, the more total vertebrate‐borne pathogen species will occur there. In order for this to be the case, each species of mammal or bird must host at least some unique pathogens. Alternatively, if most pathogens are widely distributed across hosts, then the number of host species will be less important. The second necessary link in the causal chain is that the more total species of pathogens there are in an area, the more potentially zoonotic species should occur there. This supposition requires that the zoonotic pathogens are roughly equally distributed across all vertebrate pathogens. If the zoonotic pathogens are found predominantly in a few host taxa, then the number of host species will be less important. And finally, the logic of this connection requires that the more potentially zoonotic pathogens that exist in an area, the more human disease we can expect (with human disease variously measured as prevalence, severity, or the probability of a new emergence event). What is the evidence for the three links in this causal chain (Fig. 1) connecting vertebrate diversity to zoonotic EIDs?

Figure 1 Open in figure viewer PowerPoint The necessary logical steps underlying the argument that high host diversity leads to high probability of the emergence of a zoonotic disease. High diversity of vertebrate hosts must result in high total diversity of pathogens within the vertebrate community, which in turn must lead to high diversity of actual or potential zoonotic pathogens (those that can infect humans and cause disease), which in turn must increase the probability of new emergence events. Although a link between host diversity and parasite diversity is relatively well established, effect of host diversity on viral and bacterial pathogens (arrow 1) is not. Evidence does not support a link between overall pathogen diversity and that of actual or potential zoonotic pathogens (arrow 2). Some evidence supports correlations between diversity of zoonotic pathogens and the likelihood of zoonotic emergence (arrow 3), but with important caveats described in the text.

The first link: Does higher vertebrate diversity lead to more total pathogen diversity? Natural ecosystems are rich in parasites and pathogens (Hudson et al. 2006). To the extent that each free‐living species has at least some unique pathogens, high diversity of free‐living species should lead to high diversity of pathogens; in other words, diversity begets diversity (Hechinger and Lafferty 2005, Dunn et al. 2010, Johnson et al. 2015a). However, because pathogens may be shared among several or many hosts, adding more species of hosts might not lead to a linear or even a predictable increase in species richness of pathogens. For example, Koh et al. (2004) found that the correlation between vertebrate diversity and parasite diversity was considerably weaker when the parasites had low host specificity. Johnson et al. (2016) found that the diversity of amphibian parasites increased with that of their hosts, but whereas parasite diversity increased consistently with the area sampled, host diversity saturated at larger areas. In a synthesis of the available evidence concerning helminths, Dobson et al. (2008) argued that “patterns of parasite diversity do not clearly map onto patterns of host diversity,” pointing out, for example, that some parasites of fish (e.g., monogeneans) are more diverse, but others (e.g., gut parasites) less so, where hosts are more diverse. Focusing on North American carnivores, Harris and Dunn (2010) found that in general, the species richness of carnivore parasites increased with increasing host species richness. However, in some geographic areas, such as the northern portion of North America, the correlation between host and pathogen diversity was weak. Examining 38 case studies of protozoan and metazoan parasites infecting animal hosts (both vertebrates and invertebrates) identified through literature searches, Kamiya et al. (2014) found significant positive correlations between parasite and host diversity (effect size [r] = 0.55). Their meta‐analytic methods suggested that the correlation was somewhat weaker for mammals (N = 7 host taxa, r = 0.43) than for birds (N = 11 host taxa, r = 0.65), although both relationships were statistically significant. Whether diversity of viral and bacterial parasites correlates with diversity of their hosts has not been similarly analyzed. Based on these studies, there appears to be moderate support for the supposition that greater species richness of vertebrates leads to greater richness of vertebrate‐borne pathogens, but there are caveats. One key limitation is that the effect of vertebrate diversity on that of viruses and bacteria, which remain the dominant groups of emerging infectious diseases of humans (Jones et al. 2008), is largely unknown. Another caveat is that nonlinear relationships caused by host sharing (non‐specificity by pathogens) or by different species–area curves for hosts and pathogens might weaken the correlation within some regions of parameter space. For instance, with extensive host sharing among pathogens, pathogen richness might rise with increases in host richness from low to moderate levels. But above those moderate levels of host richness, pathogen richness might increase modestly or not at all, as few unique pathogens are added (Fig. 2). Future studies should incorporate the relationship between host diversity and the diversity of bacteria and viruses specifically, and also explore the shape of the relationship between host and pathogen diversity. Figure 2 Open in figure viewer PowerPoint Schematic diagram of how parasite diversity is expected to vary with host diversity when parasites show high host specificity (upper curve) and when they show low host specificity (lower curve). In the latter case, the sharing of parasites between hosts means that the diversity of parasites will saturate as host diversity increases, resulting in little or no additional increases in parasite species at high levels of host diversity.

The second link: Higher diversity of all pathogens leads to higher diversity of potentially zoonotic pathogens? If communities with more species of vertebrates support more total species of pathogens, we might expect these diverse communities to pose a higher risk of zoonotic emergence. But this would be true only if communities supporting more total species of pathogens also support more potentially zoonotic pathogens. To what degree is total pathogen richness correlated with the richness of potentially zoonotic pathogens? We are not aware of any direct tests of possible correlations between total pathogen richness within vertebrate communities and the richness of potential or actual zoonotic pathogens. Such tests would require reliable estimates of total pathogen richness within vertebrate communities, which appear to be rare or absent. Nevertheless, if zoonotic pathogens are equally likely to arise from any host species within the vertebrate community, then this correlation would be plausible and even expected. However, some host taxa are much more likely than others to act as sources of zoonotic transmission. In particular, rodents, and secondarily carnivorans, are more likely to act as hosts for zoonotic pathogens than are birds, other mammals, or other vertebrate taxa (Johnson et al. 2015a, Han et al. 2016). Far more species of rodents (N = 244) host zoonotic pathogens than do species in other mammalian orders, and rodents carry 85 unique zoonotic pathogens, which is more than the number hosted by any other mammalian order (carnivorans are second in both respects, with 139 species hosting 83 unique zoonotic pathogens; Han et al. 2016). Other well‐studied groups of mammals, including the chiropterans, ungulates, and primates, are the sources of far fewer zoonotic pathogens, although chiropterans might be particularly important hosts for zoonotic viruses (Luis et al. 2013). Within the rodents, species with fast life history traits (e.g., early age at maturity, large litters, short life span) are more likely than those with slow life history traits to act as reservoirs for zoonotic pathogens (Han et al. 2015). These life history traits tend to be correlated with commonness rather than rarity (Stearns 1992, Blackburn et al. 1996). Similarly, Johnson et al. (2015a) found that wild rodents were the reservoirs for most (55/95) zoonotic viruses, that zoonotic virus spillover from wildlife to humans was most frequent in and around human dwellings and in agricultural fields, and that rodents were the most likely hosts to be implicated in transmission that occurred around human dwellings and agricultural fields. As a consequence, the pathogens occurring within some elements of the vertebrate host community, namely those in chiropterans, ungulates, and primates (and within most other mammalian orders; Han et al. 2016), appear to be less important to zoonotic disease emergence than those occurring in the rodents and carnivorans. It is therefore critical to ask whether communities with high vertebrate diversity necessarily contain more species of hosts for pathogens with high zoonotic potential. Ecologists have traditionally compared species diversity between different communities using rank–abundance curves, also called dominance–density curves or Whittaker plots (Whittaker 1965, Krebs 1999), which are frequency distributions of species ordered by their abundance (or the log of their abundance). Most, if not all, communities are characterized by a few highly abundant species and many more rare species (Fig. 3). When communities differing in species richness are compared using rank–abundance curves, more diverse communities frequently have longer tails; in other words, more diverse communities have relatively more rare species (Magurran 2004). One would expect, therefore, that moving along a gradient from less diverse to more diverse vertebrate communities, one would see an accumulation of rare species, with the more abundant species becoming proportionally less dominant (Magurran 2004; Fig. 3). If these rare species were likely to act as hosts for actual or potential zoonotic pathogens, then one would expect more diverse vertebrate communities, potentially with more species of pathogens overall, to be sources of more zoonotic pathogens. However, the evidence suggests that the more common and widespread species of vertebrates, such as rodents, rather than the rare ones occurring only in high‐diversity communities, are more likely to act as reservoir hosts for zoonotic pathogens. This pattern has now been observed repeatedly in nature (Keesing et al. 2010, Ostfeld et al. 2014, Han et al. 2015, Johnson et al. 2015b). Not only do rare species appear less likely to act as zoonotic reservoirs, but their very rarity will often reduce their potential for zoonotic spillover into humans. Figure 3 Open in figure viewer PowerPoint Schematic representation of typical rank–abundance curves, in which the relative abundance of each species is represented on the vertical axis and the rank of each species, from highest to lowest abundance, is given on the horizontal axis. Contrasted are two scenarios, a relatively low‐diversity community in blue and a relatively high‐diversity community in green. The curves represent the common observation that higher‐diversity communities include more species that are rare and fewer that are common. The species added (right‐hand orange circle) in higher‐diversity communities are not likely to be the sources of zoonotic pathogens, whereas the most abundant species in lower‐diversity communities (left‐hand orange circle) are often the sources of zoonotic infection. Han et al. (2016) found a positive correlation across mammalian orders between the total number of species and the number of species known to host zoonotic pathogens. In other words, the more species there are within a mammalian order, the more species within that order host zoonotic pathogens. Based on Figure 2 in Han et al. (2016), about 10% of species within any given mammalian order act as hosts for zoonotic pathogens, with somewhat lower percentages for chiropterans and soricomorphs and somewhat higher percentages for carnivorans and artiodactyls. Thus, in general, the more species‐rich orders are expected to host more zoonotic pathogens, but this observation is not directly relevant to the question of whether more diverse vertebrate communities necessarily contain more species that serve as zoonotic reservoirs. On the basis of this evidence, we suggest that increases in total pathogen richness that likely accompany increases in species richness of vertebrate hosts generally do not cause increases in the richness of potential or actual zoonotic species, severing the causal chain linking high diversity to high human disease potential. At the very least, this necessary link in the causal chain currently has no support. A rigorous evaluation of the hypothesis that areas with higher diversity of vertebrates have higher diversity of zoonotic pathogens will require new information on hosts and pathogens along diversity gradients. A two‐part process could potentially provide the necessary data. The first step would be to determine how frequently lower‐diversity communities of vertebrates consist of random, vs. non‐random, subsets of higher‐diversity communities. Existing evidence suggests that low‐diversity communities typically contain nested subsets of their higher‐diversity analogs (Wright et al. 1998), but these investigations are typically based on presence–absence data about each species. Data on changes in the relative abundance of species along the diversity gradient would be even more helpful for quantifying community structure, particularly to see whether it conforms to the hypothesis illustrated in Fig. 3. The second key step for evaluating the connection between diversity and zoonotic species richness would be to determine, for most or all of the species present in these communities, which species transmit which zoonotic pathogens, and how efficiently. Available databases of pathogens detected in members of vertebrate communities are inadequate for addressing the hypothesis. These databases (e.g., Johnson et al. 2015a) consist of both direct and indirect (e.g., immunoassay) measures of pathogens in potential hosts, but cannot by themselves determine whether pathogen‐positive hosts are reservoirs (amplifying hosts) or dead‐ends (buffering, or dilution hosts). Consequently, the mere detection of pathogen exposure within a particular host should not be considered evidence that the host transmits the pathogen. For example, for the many zoonotic pathogens transmitted by generalist vectors, most species within a vertebrate community might test seropositive, indicating exposure, but few permit pathogen amplification and onward transmission (Ostfeld and Keesing 2012). Together, these two sets of data—the community composition of species across diversity gradients and the transmission potential of these host species for zoonotic pathogens—would indicate how the risk of human exposure to emerging or recognized zoonotic pathogens changes along gradients in vertebrate diversity.