Strong and consistent effects of waterbird composition on HPAI H5 occurrences across Europe.

Since 2014, highly pathogenic avian influenza (HPAI) H5 viruses of clade 2.3.4.4 have been dominating the outbreaks across Europe, causing massive deaths among poultry and wild birds. However, the factors shaping these broad-scale outbreak patterns, especially those related to waterbird community composition, remain unclear. In particular, we do not know whether these risk factors differ from those of other H5 clades. Addressing this knowledge gap is important for predicting and preventing future HPAI outbreaks. Using extensive waterbird survey datasets from about 6883 sites, we here explored the effect of waterbird community composition on HPAI H5Nx (clade 2.3.4.4) spatial patterns in the 2016/2017 and 2020/2021 epidemics in Europe, and compared it with the 2005/2006 HPAI H5N1 (clade 2.2) epidemic. We showed that HPAI H5 occurrences in wild birds in the three epidemics were strongly associated with very similar waterbird community attributes, which suggested that, in nature, similar interspecific transmission processes operate between the HPAI H5 subtypes or clades. Importantly, community phylogenetic diversity consistently showed a negative association with H5 occurrence in all three epidemics, suggesting a dilution effect of phylogenetic diversity. In contrast, waterbird community variables showed much weaker associations with HPAI H5Nx occurrence in poultry. Our results demonstrate that models based on previous epidemics can predict future HPAI H5 patterns in wild birds, implying that it is important to include waterbird community factors in future HPAI studies to predict outbreaks and improve surveillance activities.

Inconsistent dilution: experimental but not field evidence for a dilution effect in Daphnia-bacteria interactions.

The dilution effect hypothesis, which suggests greater host biodiversity can reduce infectious disease transmission, occurs in many systems but is not universal. Most studies only investigate the dilution of a single parasite in a community, but many host communities have multiple parasites circulating. We studied a zooplankton host community with prior support for a dilution effect in laboratory- and field-based studies of a fungal parasite, Metschnikowia bicuspidata. We used paired experiments and field studies to ask whether dilution also occurred for a bacterial parasite, Pasteuria ramosa. We hypothesized that the similarities between the parasites might mean the dilution pattern seen in Metschnikowia would also be seen in Pasteuria. However, because Daphnia-Pasteuria interactions have strong host-parasite genotype specificity, dilution may be less likely if diluter host genotypes vary in their capacity to dilute Pasteuria. In a lab experiment, Pasteuria prevalence in susceptible Daphnia dentifera was reduced strongly by higher densities of D. pulicaria and marginally by higher densities of D. retrocurva. In a second experiment, different D. pulicaria genotypes had a similar capacity to dilute both Metschnikowia and Pasteuria, suggesting that Pasteuria's strong host-parasite genotype specificity should not prevent dilution. However, we found no evidence of an impact of the dilution effect on the size of Pasteuria epidemics in D. dentifera in Midwestern U.S. lakes. Our finding that a second parasite infecting the same host community does not show a similar dilution effect in the field suggests the impact of biodiversity can differ even among parasites in the same host community.

Functional traits explain waterbirds' host status, subtype richness, and community-level infection risk for avian influenza.

Species functional traits can influence pathogen transmission processes, and consequently affect species' host status, pathogen diversity, and community-level infection risk. We here investigated, for 143 European waterbird species, effects of functional traits on host status and pathogen diversity (subtype richness) for avian influenza virus at species level. We then explored the association between functional diversity and HPAI H5Nx occurrence at the community level for 2016/17 and 2021/22 epidemics in Europe. We found that both host status and subtype richness were shaped by several traits, such as diet guild and dispersal ability, and that the community-weighted means of these traits were also correlated with community-level risk of H5Nx occurrence. Moreover, functional divergence was negatively associated with H5Nx occurrence, indicating that functional diversity can reduce infection risk. Our findings highlight the value of integrating trait-based ecology into the framework of diversity-disease relationship, and provide new insights for HPAI prediction and prevention.

Host diversity positively affects the temporal stability of foliar fungal diseases in a Tibetan alpine meadow.

BACKGROUND AND AIMS: Plant disease can dramatically affect population dynamics, community composition and ecosystem functions. However, most empirical studies focus on diseases at a certain time point and largely ignore their temporal stability, which directly affects our ability to predict when and where disease outbreaks will occur. METHODS: Using a removal experiment that manipulates plant diversity (i.e. a plant biodiversity and ecosystem function experiment) and a fertilization experiment in a Tibetan alpine meadow, we investigated how different plant biodiversity indices and nitrogen fertilization affect the temporal stability of foliar fungal diseases (measured as the mean value of community pathogen load divided by its standard deviation) over seven consecutive years. KEY RESULTS: We found that the temporal stability of foliar fungal diseases increased with plant diversity indices in the plant biodiversity and ecosystem function experiment. Meanwhile, we observed a weakly positive relationship between host diversity and temporal stability in the fertilization experiment. However, the nitrogen treatment did not affect temporal stability, given that fertilization increased both the mean and standard deviation of pathogen load by roughly the same magnitude. CONCLUSIONS: We conclude that host diversity regulates the temporal stability of pathogen load, but we note that this effect may be attenuated under rapid biodiversity loss in the Anthropocene.

The dilution effect behind the scenes: testing the underlying assumptions of its mechanisms through quantifying the long-term dynamics and effects of a pathogen in multiple host species.

Disentangling the mechanisms that mediate the relationships between species diversity and disease risk has both theoretical and applied implications. We employed a model system of rodents and their Mycoplasma pathogens, in which an extreme negative diversity-disease relationship was demonstrated, to test the assumptions underlying three mechanisms that may explain this field pattern. Through quantifying the long-term dynamics and effects of the pathogen in its three host species, we estimated the between-host differences in pathogen spreading and transmission potentials, and host recovery potential and vulnerability to infection. The results suggest that one of the hosts is a pathogen amplifier and the other two hosts function as diluters. Considering the similarity in infection success and intensity among hosts, and the failure to detect any pathogen-induced damage, we could not validate the assumption underlying the hypotheses that diluters reduce the overall transmission or increase the mortality of infected hosts in the system. Instead, the results demonstrate that diluters clear the infection faster than amplifiers, supporting the possibility that the addition of diluters to the community may reduce the overall number of infected hosts through this mechanism. This study highlights the contribution of experimental studies that simultaneously explore different aspects of host-pathogen interactions in multiple hosts, in diversity-disease research.

How intraguild predation affects the host diversity-disease relationship in a multihost community.

Broad evidence has shown that host diversity can impede disease invasion and reduce the eventual prevalence, but little is known on how species interactions play in shaping this host diversity-disease relationship. Previous work has illustrated that intraguild predation (IGP), combined with parasite-mediated indirect effects, can have strong influences on parasitic infection. Following this line of thinking, we here examine the role of predatory interactions in the disease transmission within a multihost community. Through varying fractions of IGP in a competitive community, we show that, dependent on the fraction of predatory interactions, species richness can switch from enhancing to inhibiting disease establishment/prevalence. Without IGP interactions, high host species richness can likely weaken the 'dilution effect' and in some cases even enhance the disease establishment (and/or prevalence) due to the existence of alternative sources for infection, whereas IGP can generally heighten the negative diversity-disease relationship due to the reduction of encounter rate between prospective hosts and parasites. Although trait-mediated interactions (captured as the infection-induced changes in predation rate) only weakly affect disease prevalence, density-mediated interactions (captured as the additional infection-induced mortality) can pose a relatively strong influence on disease transmission. Our results thus underline the importance of considering species interactions when investigating the host diversity-disease relationship.

Contrasting effects of host species and phylogenetic diversity on the occurrence of HPAI H5N1 in European wild birds.

Studies on the highly pathogenic avian influenza (HPAI) H5N1 suggest that wild bird migration may facilitate its long-distance spread, yet the role of wild bird community composition in its transmission risk remains poorly understood. Furthermore, most studies on the diversity-disease relationship focused on host species diversity without considering hosts' phylogenetic relationships, which may lead to rejecting a species diversity effect when the community has host species that are only distantly related. Here, we explored the influence of waterbird community composition for determining HPAI H5N1 occurrence in wild birds in a continental-scale study across Europe. In particular, we tested the diversity-disease relationship using both host species diversity and host phylogenetic diversity. Our results provide the first demonstration that host community composition-compared with previously identified environmental risk factors-can also effectively explain the spatial pattern of H5N1 occurrence in wild birds. We further show that communities with more higher risk host species and more closely related species have a higher risk of H5N1 outbreaks. Thus, both host species diversity and community phylogenetic structure, in addition to environmental factors, jointly influence H5N1 occurrence. Our work not only extends the current theory on the diversity-disease relationship, but also has important implications for future monitoring of H5N1 and other HPAI subtypes.

Species decline under nitrogen fertilization increases community-level competence of fungal diseases.

The artificial fertilization of soils can alter the structure of natural plant communities and exacerbate pathogen emergence and transmission. Although the direct effects of fertilization on disease resistance in plants have received some research attention, its indirect effects of altered community structure on the severity of fungal disease infection remain largely uninvestigated. We designed manipulation experiments in natural assemblages of Tibetan alpine meadow vegetation along a nitrogen-fertilization gradient over 5 years to compare the relative importance of direct and indirect effects of fertilization on foliar fungal infections at the community level. We found that species with lower proneness to pathogens were more likely to be extirpated following fertilization, such that community-level competence of disease, and thus community pathogen load, increased with the intensity of fertilization. The amount of nitrogen added (direct effect) and community disease competence (indirect effect) provided the most parsimonious combination of parameters explaining the variation in disease severity. Our experiment provides a mechanistic explanation for the dilution effect in fertilized, natural assemblages in a highly specific pathogen-host system, and thus insights into the consequences of human ecosystem modifications on the dynamics of infectious diseases.

Does the dilution effect generally occur in animal diseases?

The dilution effect (DE) has been reported in many diseases, but its generality is still highly disputed. Most current criticisms of DE are related to animal diseases. Particularly, some critical studies argued that DE is less likely to occur in complex environments. Here our meta-analyses demonstrated that the magnitude of DE did not differ between animal vs plant diseases. Moreover, DE generally occurs in all three subgroups of animal diseases, namely direct-transmitted diseases, vector-borne diseases and diseases caused by parasites with free-living stages. Our findings serve as an important contribution to understanding the generality of DE.

Warming and fertilization alter the dilution effect of host diversity on disease severity.

An essential ecosystem service is the dilution effect of biodiversity on disease severity, yet we do not fully understand how this relationship might change with continued climate warming and ecosystem degradation. We designed removal experiments in natural assemblages of Tibetan alpine meadow vegetation by manipulating plot-level plant diversity to investigate the relationship between different plant biodiversity indices and foliar fungal pathogen infection, and how artificial fertilization and warming affect this relationship. Although pathogen group diversity increased with host species richness, disease severity decreased as host diversity rose (dilution effect). The dilution effect of phylogenetic diversity on disease held across different levels of host species richness (and equal abundances), meaning that the effect arises mainly in association with enhanced diversity itself rather than from shifting abundances. However, the dilution effect was weakened by fertilization. Among indices, phylogenetic diversity was the most parsimonious predictor of infection severity. Experimental warming and fertilization shifted species richness to the most supported predictor. Compared to planting experiments where artificial communities are constructed from scratch, our removal experiment in natural communities more realistically demonstrate that increasing perturbation adjusts natural community resistance to disease severity.

Dilution versus facilitation: Impact of connectivity on disease risk in metapopulations.

Epidemiological studies have suggested that increasing connectivity in metapopulations usually facilitates pathogen transmission. However, these studies focusing on single-host systems usually neglect that increasing connectivity can increase species diversity which might reduce pathogen transmission via the 'dilution effect', a hypothesis whose generality is still disputed. On the other hand, studies investigating the generality of the dilution effect were usually conducted without considering habitat structure, which is surprising as species loss is often driven by habitat fragmentation. Using a simple general model to link fragmentation to the dilution effect, we determined the effect of connectivity on disease risk and explored when the dilution effect can be detected. We showed that landscape structure can largely modify the diversity-disease relationship. The net impact of connectivity on disease risk can be either positive or negative, depending on the relative importance of the facilitation effect (through increasing contact rates among patches) versus the dilution effect (via increasing species richness). We also demonstrated that different risk indices (i.e. infection prevalence and abundance of infected hosts) react differently to increasing connectivity and species richness. Our study may contribute to the current debate on the dilution effect, and a better understanding of the impacts of fragmentation on disease risks.

Partitioning the net effect of host diversity on an emerging amphibian pathogen.

The 'dilution effect' (DE) hypothesis predicts that diverse host communities will show reduced disease. The underlying causes of pathogen dilution are complex, because they involve non-additive (driven by host interactions and differential habitat use) and additive (controlled by host species composition) mechanisms. Here, we used measures of complementarity and selection traditionally employed in the field of biodiversity-ecosystem function (BEF) to quantify the net effect of host diversity on disease dynamics of the amphibian-killing fungus Batrachochytrium dendrobatidis (Bd). Complementarity occurs when average infection load in diverse host assemblages departs from that of each component species in uniform populations. Selection measures the disproportionate impact of a particular species in diverse assemblages compared with its performance in uniform populations, and therefore has strong additive and non-additive properties. We experimentally infected tropical amphibian species of varying life histories, in single- and multi-host treatments, and measured individual Bd infection loads. Host diversity reduced Bd infection in amphibians through a mechanism analogous to complementarity (sensu BEF), potentially by reducing shared habitat use and transmission among hosts. Additionally, the selection component indicated that one particular terrestrial species showed reduced infection loads in diverse assemblages at the expense of neighbouring aquatic hosts becoming heavily infected. By partitioning components of diversity, our findings underscore the importance of additive and non-additive mechanisms underlying the DE.

Impact of vector richness on the risk of vector-borne disease: The role of vector competence.

A central goal of disease ecology is to identify the factors that drive the spread of infectious diseases. Changes in vector richness can have complex effects on disease risk, but little is known about the role of vector competence in the relationship between vector richness and disease risk. In this study, we firstly investigated the combined effects of vector competence, interspecific competition, and feeding interference on disease risk through a two-vector, one-host SIR-SI model, and obtained threshold conditions for the occurrence of dilution and amplification effects. Secondly, we extended the above model to the case of N vectors and assumed that all vectors were homogeneous to obtain analytic expressions for disease risk. It was found that in the two-vector model, disease risk declined more rapidly as interspecific competition of the high-competence vector increased. When vector richness increases, the positive effects of adding a high-competence vector species on disease transmission may outweigh the negative effects of feeding interference due to increased vector richness, making an amplification effect more likely to occur. While the addition of a highly competitive vector species may exacerbate the negative effects of feeding interference, making a dilution effect more likely to occur. In the N-vector model, the effect of increased vector richness on disease risk was fully driven by the strength of feeding interference and interspecific competition, and changes in vector competence only quantitatively but not qualitatively altered the vector richness-disease risk relationship. This work clarifies the role of vector competence in the relationship between vector richness and disease risk and provides a new perspective for studying the diversity-disease relationship. It also provides theoretical guidance for vector management and disease prevention strategies.

Host-Population Microbial Diversity Scaling of Chinese Gut Microbiomes in Gout Patients.

Gout is a prevalent chronic inflammatory disease that affects the life of tens of millions of people worldwide, and it typically presents as gout arthritis, gout stone, or even kidney damage. Research has revealed its connection with the gut microbiome, although exact mechanism is still unclear. Studies have shown the decline of microbiome diversity in gout patients and change of microbiome compositions between the gout patients and healthy controls. Nevertheless, how diversity changes across host individuals at a cohort (population) level has not been investigated to the best of our knowledge. Here we apply the diversity-area relationship (DAR), which is an extension to the classic SAR (species-area relationship) and establishes the power-function model between microbiome diversity and the number of individuals within cohort, to comparatively investigate diversity scaling (changes) of gut microbiome in gout patients and healthy controls. The DAR modeling with a study involving 83 subjects (41 gout patients) revealed that the potential number of microbial species in gout patients is only 70% of that in the healthy control (2790 vs 3900) although the difference may not be statistically significant. The other DAR parameters including diversity scaling and similarity parameters did not show statistically significant differences. We postulate that the high resilience of gut microbiome may explain the lack of significant gout-disease effects on gut microbial diversity at the population level. The lack of statistically significant difference between the gout patients and healthy controls at host population (cohort) level is different from the previous findings at individual level in the existing literature.

Re-emphasizing mechanism in the community ecology of disease.

1. Hosts and their parasites exist within complex ecological communities. However, the role that non-focal community members, species which cannot be infected by a focal pathogen, may play in altering parasite transmission is often only studied in the lens of the "diversity-disease" relationship by focusing on species richness. This approach largely ignores mechanistic species interactions and risks collapsing our understanding of the community ecology of disease down to defining the prominence of "amplification" vs. "dilution" effects. 2. However, non-focal species vary in their traits, densities, and types of interactions with focal hosts and parasites. Therefore, a community ecology approach based on the mechanisms underlying parasite transmission, host harm, and dynamic species interactions may better advance our understanding of parasite transmission in complex communities. 3. Using the concept of the parasite's basic reproductive ratio, R0, as a generalizable framework, we examine several critical mechanisms by which interactions among hosts, parasites, and non-focal species modulate transmission and provide examples from relevant literature. 4. By focusing on the mechanism by which non-focal species impact transmission, we can emphasize the similarities among classic paradigms in the community ecology of disease, gain new insights into parasite invasion and persistence, community traits correlated with disease dilution or amplification, and the feasibility of biocontrol for parasites of conservation, agricultural, or human health concern.

Population-level diversity-disease relationship (p-DDR) in the human microbiome associated diseases.

Diversity-disease relationship (DDR) is a de facto standard analysis in the studies of human microbiome associated diseases (MADs). For example, the species richness or Shannon entropy are routinely compared between the healthy and diseased groups. Nevertheless, the basic scale of the standard diversity analysis is individual subject rather than a cohort or population because the diversity is computed for individual samples, not for the group. Here we aim to expand the current DDR study from individual focus to population level, which can offer important insights for understanding the epidemiology of MADs. We analyzed the diversity-disease relationship at cohort scale based on a collection of 23 datasets covering the major human MADs. Methodologically, we harness the power of a recent extension to the classic species-area relationship (SAR), i.e., the diversity-area relationship (DAR), to achieve the expansion from individual DDR to inter-subject diversity scaling analysis. Specifically, we apply the DAR analysis to estimate and compare the potentially maximal accrual diversities of the healthy and diseases groups, as well as the inter-subject diversity scaling parameters and the individual-to-population diversity ratios. It was shown that, except for the potential diversity (D max) at the cohort level in approximately 5.4% cases of MADs, DAR parameters displayed no significant differences between healthy and diseased treatments. That is, the DAR parameters are rather resilient against MADs, except for the potential diversity in some diseases. We compared our population-level DDR with the existing individual-level DDR patterns and proposed a hypothesis to interpret their differences.

Heterogeneity-disease relationship in the human microbiome-associated diseases.

Space is a critical and also challenging frontier in human microbiome research. It has been found that lack of consideration of scales beyond individual and ignoring of microbe dispersal are two crucial roadblocks in preventing deep understanding of the spatial heterogeneity of human microbiome. Assessing and interpreting the heterogeneity and dispersal in microbiomes explicitly are particularly challenging, but implicit approaches such as Taylor's power law (TPL) can be rather effective. Based on TPL, which achieved a rare status of ecological laws, we introduce a general methodology for characterizing the spatial heterogeneity of microbiome (i.e. characterization of microbial spatial distribution) and further apply it for investigating the heterogeneity-disease relationship (HDR) via analyzing a big dataset of 26 MAD (microbiome-associated disease) studies covering nearly all high-profile MADs including obesity, diabetes and gout. It was found that in majority of the MAD cases, the microbiome was sufficiently resilient to endure the disease disturbances. Specifically, in ∼10-16% cases, disease effects were significant-the healthy and diseased cohorts exhibited statistically significant differences in the TPL heterogeneity parameters. We further compared HDR with classic diversity-disease relationship (DDR) and explained their mechanistic differences. Both HDR and DDR cross-verified remarkable resilience of the human microbiomes against MADs.