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.

Pathways linking nutrient enrichment, habitat structure, and parasitism to host-resource interactions.

Human activities simultaneously alter nutrient levels, habitat structure, and levels of parasitism. These activities likely have individual and joint impacts on food webs. Furthermore, there is particular concern that nutrient additions and changes to habitat structure might exacerbate the size of epidemics and impacts on host density. We used a well-studied zooplankton-fungus host-parasite system and experimental whole water column enclosures to factorially manipulate nutrient levels, habitat structure (specifically: mixing), and presence of parasites. Nutrient addition increased infection prevalence, density of infected hosts, and total host density. We hypothesized that nutrients, mixing, and parasitism were linked in multiple ways, including via their combined effects on phytoplankton (resource) abundance, and we used structural equation modeling to disentangle these pathways. In the absence of the parasite, both nutrients and mixing increased abundance of phytoplankton, whereas host density was negatively related to phytoplankton abundance, suggesting a mixture of bottom-up and top-down control of phytoplankton. In the presence of the parasite, nutrients still increased phytoplankton abundance but mixing no longer did, and there was no longer a significant relationship between host density and phytoplankton. This decoupling of host-resource dynamics may have resulted from reduced grazing due to illness-mediated changes in feeding behavior. Overall, our results show that the impact of one human activity (e.g., altered habitat structure) might depend on other human impacts (e.g., parasite introduction). Fortunately, carefully designed experiments and analyses can help tease apart these multifaceted relationships, allowing us to understand how human activities alter food webs, including interactions between hosts and their parasites and resources.

Rapid juvenile hormone downregulation in subordinate wasp queens facilitates stable cooperation.

In many cooperatively breeding animals, subordinate group members have lower reproductive capacity than dominant group members. Theory suggests subordinates may downregulate their reproductive capacity because dominants punish subordinates who maintain high fertility. However, there is little direct experimental evidence that dominants cause physiological suppression in subordinates. Here, we experimentally test how social interactions influence subordinate reproductive hormones in Polistes dominula paper wasps. Polistes dominula queens commonly found nests in cooperative groups where the dominant queen is more fertile than the subordinate queen. In this study, we randomly assigned wasps to cooperative groups, assessed dominance behaviour during group formation, then measured levels of juvenile hormone (JH), a hormone that mediates Polistes fertility. Within three hours, lowest ranking subordinates had less JH than dominants or solitary controls, indicating that group formation caused rapid JH reduction in low-ranking subordinates. In a second experiment, we measured the behavioural consequences of experimentally increasing subordinate JH. Subordinates with high JH-titres received significantly more aggression than control subordinates or subordinates from groups where the dominant's JH was increased. These results suggest that dominants aggressively punished subordinates who attempted to maintain high fertility. Low-ranked subordinates may rapidly downregulate reproductive capacity to reduce costly social interactions with dominants. Rapid modulation of subordinate reproductive physiology may be an important adaptation to facilitate the formation of stable, cooperative groups.

Habitat quality influences pollinator pathogen prevalence through both habitat-disease and biodiversity-disease pathways.

The dilution effect hypothesis posits that increasing biodiversity reduces infectious disease transmission. Here, we propose that habitat quality might modulate this negative biodiversity-disease relationship. Habitat may influence pathogen prevalence directly by affecting host traits like nutrition and immune response (we coined the term "habitat-disease relationship" to describe this phenomenon) or indirectly by changing host biodiversity (biodiversity-disease relationship). We used a path model to test the relative strength of links between habitat, biodiversity, and pathogen prevalence in a pollinator-virus system. High-quality habitat metrics were directly associated with viral prevalence, providing evidence for a habitat-disease relationship. However, the strength and direction of specific habitat effects on viral prevalence varied based on the characteristics of the habitat, host, and pathogen. In general, more natural area and richness of land-cover types were directly associated with increased viral prevalence, whereas greater floral density was associated with reduced viral prevalence. More natural habitat was also indirectly associated with reduced prevalence of two key viruses (black queen cell virus and deformed wing virus) via increased pollinator species richness, providing evidence for a habitat-mediated dilution effect on viral prevalence. Biodiversity-disease relationships varied across viruses, with the prevalence of sacbrood virus not being associated with any habitat quality or pollinator community metrics. Across all viruses and hosts, habitat-disease and biodiversity-disease paths had effects of similar magnitude on viral prevalence. Therefore, habitat quality is a key driver of variation in pathogen prevalence among communities via both direct habitat-disease and indirect biodiversity-disease pathways, though the specific patterns varied among different viruses and host species. Critically, habitat-disease relationships could either contribute to or obscure dilution effects in natural systems depending on the relative strength and direction of the habitat-disease and biodiversity-disease pathways in that host-pathogen system. Therefore, habitat may be an important driver in the complex interactions between hosts and pathogens.

Honeybee visitation to shared flowers increases Vairimorpha ceranae prevalence in bumblebees.

Vairimorpha (=Nosema) ceranae is a widespread pollinator parasite that commonly infects honeybees and wild pollinators, including bumblebees. Honeybees are highly competent V. ceranae hosts and previous work in experimental flight cages suggests V. ceranae can be transmitted during visitation to shared flowers. However, the relationship between floral visitation in the natural environment and the prevalence of V. ceranae among multiple bee species has not been explored. Here, we analyzed the number and duration of pollinator visits to particular components of squash flowers-including the petals, stamen, and nectary-at six farms in southeastern Michigan, USA. We also determined the prevalence of V. ceranae in honeybees and bumblebees at each site. Our results showed that more honeybee flower contacts and longer duration of contacts with pollen and nectar were linked with greater V. ceranae prevalence in bumblebees. Honeybee visitation patterns appear to have a disproportionately large impact on V. ceranae prevalence in bumblebees even though honeybees are not the most frequent flower visitors. Floral visitation by squash bees or other pollinators was not linked with V. ceranae prevalence in bumblebees. Further, V. ceranae prevalence in honeybees was unaffected by floral visitation behaviors by any pollinator species. These results suggest that honeybee visitation behaviors on shared floral resources may be an important contributor to increased V. ceranae spillover to bumblebees in the field. Understanding how V. ceranae prevalence is influenced by pollinator behavior in the shared floral landscape is critical for reducing parasite spillover into declining wild bee populations.

Pollinator community species richness dilutes prevalence of multiple viruses within multiple host species.

Most pathogens are embedded in complex communities composed of multiple interacting hosts, but we are still learning how community-level factors, such as host diversity, abundance, and composition, contribute to pathogen spread for many host-pathogen systems. Evaluating relationships among multiple pathogens and hosts may clarify whether particular host or pathogen traits consistently drive links between community factors and pathogen prevalence. Pollinators are a good system to test how community composition influences pathogen spread because pollinator communities are extremely variable and contain several multi-host pathogens transmitted on shared floral resources. We conducted a field survey of four pollinator species to test the prevalence of three RNA viruses (deformed wing virus, black queen cell virus, and sacbrood virus) among pollinator communities with variable species richness, abundance, and composition. All three viruses showed a similar pattern of prevalence among hosts. Apis mellifera and Bombus impatiens had significantly higher viral prevalence than Lasioglossum spp. and Eucera pruinosa. In each species, lower virus prevalence was most strongly linked with greater pollinator community species richness. In contrast, pollinator abundance, species-specific pollinator abundance, and community composition were not associated with virus prevalence. Our results support a consistent dilution effect for multiple viruses and host species. Pollinators in species-rich communities had lower viral prevalence than pollinators from species-poor communities, when accounting for differences in pollinator abundance. Species-rich communities likely had lower viral prevalence because species-rich communities contained more native bee species likely to be poor viral hosts than species-poor communities, and all communities contained the highly competent hosts A. mellifera and B. impatiens. Interestingly, the strength of the dilution effect was not consistent among hosts. Instead, host species with low viral prevalence exhibited weaker dilution effects compared to hosts with high viral prevalence. Therefore, host species susceptibility and competence for each virus may contribute to variation in the strength of dilution effects. This study expands biodiversity-disease studies to the pollinator-virus system, finding consistent evidence of the dilution effect among multiple similar pathogens that infect "replicate" host communities.