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Data from: Habitat quality influences pollinator pathogen prevalence through both habitat–disease and biodiversity–disease pathways

Citation

Fearon, Michelle; Wood, Chelsea; Tibbetts, Elizabeth (2022), Data from: Habitat quality influences pollinator pathogen prevalence through both habitat–disease and biodiversity–disease pathways, Dryad, Dataset, https://doi.org/10.5061/dryad.mkkwh710c

Abstract

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 this as the ‘habitat–disease relationship’) 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 landcover types were directly associated with increased viral prevalence, while 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, as prevalence of sacbrood virus was not 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.

Methods

We collected pollinator community species richness and abundance data by sampling pollinators from each community with hand nets and pan traps. At each collection site, we measured the density of flowers and species richness of flowering plants (including native and non-native plants) to assess local habitat quality along the same transects that pollinators were collected from. To assess landscape habitat quality for pollinators, we used the USDA cropland data layer to quantify the proportion of natural area (including forest, wetland, and grassland) and the landscape richness (the number of different landcover types) within a 1000 m radius of each collection site. Landowner permission was given for pollinator collection at each site. 

A subset of Apis melliferaBombus impatiensLasioglossum spp. and Eucera pruinosa was tested for the presence of deformed wing virus (DWV), black queen cell virus (BQCV), and sacbrood virus (SBV). Viral data was recorded as binary presence or absence of each virus for each individual tested. Each bee in the study was tested for all three viruses.

We used a path model to test the relative effects of habitat quality characteristics and pollinator community characteristics on patterns of viral prevalence. The path model allows us to rigorously disentangle the effects of habitat characteristics on patterns of pathogen prevalence through the newly proposed habitat–disease relationship and the well-established biodiversity–disease relationship.

Usage Notes

Summary of field and virus prevalence data
Field collected data examining the relative impact of local- and landscape-level habitat quality characteristics and pollinator community diversity and abundance on viral prevalence in a natural multihost-multipathogen system. This data uses pollinator communities sampled from winter squash farms along a landscape gradient from low to high proportion natural area and vary substantially in pollinator diversity and abundance to evaluate patterns of deformed wing virus (DWV), black queen cell virus (BQCV), and sacbrood virus (SBV) prevalence within four focal host species: Apis melliferaBombus impatiensLasioglossum spp., and Eucera pruinosa. A subset of the four host species collected from each site was used to test for the presence or absence of DWV, BQCV, and SBV using RT-PCR with virus-specific primers.
Virus_Positive_Community+Habitat_Covariates_1Mar2022.csv
README_for_Fearon,Wood,Tibbetts_Ecology.txt

R script for path models 
The code used to run the main and species-specific path analyses presented in the manuscript. This code produces the information presented in Figures 1–4, and all tables in Appendix S2 and Appendix S3.
BeeVirusHabitat+CommunityPathModels_29Sept2022.R

Calculations of relative strength of direct, indirect, and total effects from the main path model (Figure 4)
These calculations were done in Microsoft Excel based on the significant scale standardized coefficients produced from the main path model (Figure 4).
Fig 4_indirect and total effect calculations from main path model.xlsx

Original pollinator community data and compilation and analysis of the prevalence of the viral negative strand in each host species, indicative of active viral replication and infection, from the bee specimen used in this study can be found in Data from: Pollinator community species richness dilutes prevalence of multiple viruses within multiple host species (https://doi.org/10.5061/dryad.zpc866t7g).

Funding

National Science Foundation, Award: IOS-1557564

National Science Foundation, Award: OCE-1829509

Dow Chemical Company

North American Pollinator Protection Campaign

The Garden Club of America

Alfred P. Sloan Foundation

University of Washington Innovation Award

University of Washington Royalty Research Fund

Pollinator Partnership

Horace H. Rackham School of Graduate Studies, University of Michigan