Dominant bee species and floral abundance drive parasite temporal dynamics in plant-pollinator communities

Abstract

Pollinator reductions can leave communities less diverse and potentially at increased risk of infectious diseases. Species-rich plant and bee communities have high species turnover, making the study of disease dynamics challenging. To address how temporal dynamics shape parasite prevalence in plant and bee communities, we screened >5,000 bees and flowers over an entire growing season for five common bee microparasites (Nosema ceranae, Nosema bombi, Crithidia bombi, Crithidia expoeki and neogregarines). Over 110 bee species and 89 flower species were screened, revealing that 42% of bee species (12.2% individual bees) and 70% of flower species (8.7% individual flowers) had at least one parasite in or on them, respectively. Some common flowers (for example, Lychnis flos-cuculi) harboured multiple parasite species whilst others (for example, Lythrum salicaria) had few. Significant temporal variation of parasite prevalence in bees was linked to bee diversity, bee and flower abundance and community composition. Specifically, we found that bee communities had the highest prevalence late in the season, when social bees (Bombus spp. and Apis mellifera) were dominant and bee diversity was lowest. Conversely, prevalence on flowers was lowest late in the season when floral abundance was highest. Thus turnover in the bee community impacted community-wide prevalence, and turnover in the plant community impacted when parasite transmission was likely to occur at flowers. These results imply that efforts to improve bee health will benefit from the promotion of high floral numbers to reduce transmission risk, maintaining bee diversity to dilute parasites and monitoring the abundance of dominant competent hosts.

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Fig. 1: Parasite prevalence in bee and on flower genera across three old-field communities.
Fig. 2: Parasite prevalence increased throughout the season in the bee community while it decreased or remained constant in the floral community.
Fig. 3: Associations between bee community composition, diversity and parasite prevalence over time.
Fig. 4: Increase in floral abundance over time may dilute parasite prevalence on flowers.

Data availability

All raw data, including site surveys and screening results, are found on Dryad in addition to all analysis code used (https://doi.org/10.6086/D1X09V). Sequence data are also deposited in the NCBI database, with accession nos. MT212154, MT212155, MT212156, MT212157, MT212158, MT212159, MT296581, MT296582, MT296583, MT296584, MT296585, MT296586, MT302779, MT302780, MT302781, MT302782, MT302783, MT302784, MT359894MT359896, MT366919, MT387450 and MT387451.

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Acknowledgements

T. Salazar and D. Lewis assisted with fieldwork, J. Teague helped with bee dissections, M. Arduser confirmed bee identifications and J. Strange (USDA-ARS-PIRU) provided support in the development of diagnostic primers. The research group of R. Gill provided comments on the manuscript. Research reported in this publication was supported by the National Institute of General Medical Sciences of the National Institutes of Health (NIH, award no. R01GM122062). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

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P.G., Q.S.M., C.R.M. and S.H.M. conceived the study. P.G., A.A.F., Q.S.M., C.R.M. and S.H.M. contributed to study design. P.G. and A.A.F. collected the field data. P.G., K.P. and Q.S.M. conducted the molecular work. A.D.T. developed molecular primers. P.A.M. identified and pinned the bee samples collected. W.H.N., P.G., C.R.M. and S.H.M. contributed to data analysis and wrote the first draft of the manuscript. All authors contributed substantially to the final draft.

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Correspondence to Peter Graystock.

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The authors declare no competing interests. A.D.T. contributed to this article in her personal capacity. The views expressed are her own and do not necessarily represent the views of the Agricultural Research Service or the United States Government.

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Supplementary methods, Tables 1–11 and Figs. 1–10.

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Graystock, P., Ng, W.H., Parks, K. et al. Dominant bee species and floral abundance drive parasite temporal dynamics in plant-pollinator communities. Nat Ecol Evol (2020). https://doi.org/10.1038/s41559-020-1247-x

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