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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.

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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.

References

  1. Pongsiri, M. J. et al. Biodiversity loss affects global disease ecology. BioScience 59, 945–954 (2009).

    Google Scholar 

  2. Dirzo, R. et al. Defaunation in the Anthropocene. Science 345, 401–406 (2014).

    CAS  PubMed  Google Scholar 

  3. Barnosky, A. D. et al. Has the Earth’s sixth mass extinction already arrived? Nature 471, 51–57 (2011).

    CAS  PubMed  Google Scholar 

  4. Sala, O. E. et al. Accelerated modern human-induced species losses: entering the sixth mass extinction. Sci. Adv. 1, e1400253 (2000).

    Google Scholar 

  5. Anderson, P. K. et al. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol. Evol. 19, 535–544 (2004).

    PubMed  Google Scholar 

  6. Daszak, P., Cunningham, A. A. & Hyatt, A. D. Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287, 443–449 (2000).

    CAS  PubMed  Google Scholar 

  7. Johnson, P. T. J. J., de Roode, J. C. & Fenton, A. Why infectious disease research needs community ecology. Science 349, 1259504 (2015).

    PubMed  PubMed Central  Google Scholar 

  8. Goulson, D., Lye, G. C. & Darvill, B. Decline and conservation of bumble bees. Annu. Rev. Entomol. 53, 191–208 (2008).

    CAS  PubMed  Google Scholar 

  9. Williams, P. H. & Osborne, J. L. Bumblebee vulnerability and conservation world-wide. Apidologie 40, 367–387 (2009).

    Google Scholar 

  10. Goulson, D., Nicholls, E., Botias, C. & Rotheray, E. L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957 (2015).

  11. Gallai, N., Salles, J. M., Settele, J. & Vaissiere, B. E. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68, 810–821 (2009).

    Google Scholar 

  12. Paull, S. H. et al. From superspreaders to disease hotspots: linking transmission across hosts and space. Front. Ecol. Environ. 10, 75–82 (2012).

    PubMed  Google Scholar 

  13. Wood, C. L. et al. Does biodiversity protect humans against infectious disease? Ecology 95, 817–832 (2014).

    PubMed  Google Scholar 

  14. Salkeld, D. J., Padgett, K. A. & Jones, J. H. A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic. Ecol. Lett. 16, 679–686 (2013).

    PubMed  PubMed Central  Google Scholar 

  15. Wood, C. L. & Lafferty, K. D. Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trends Ecol. Evol. 28, 239–247 (2013).

    PubMed  Google Scholar 

  16. Luis, A. D., Kuenzi, A. J. & Mills, J. N. Species diversity concurrently dilutes and amplifies transmission in a zoonotic host–pathogen system through competing mechanisms. Proc. Natl Acad. Sci. USA 115, 7979–7984 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Keesing, F., Holt, R. D. & Ostfeld, R. S. Effects of species diversity on disease risk. Ecol. Lett. 9, 485–498 (2006).

    CAS  PubMed  Google Scholar 

  18. Ostfeld, R. S. & Keesing, F. Biodiversity and disease risk: the case of Lyme disease. Conserv. Biol. 14, 722–728 (2000).

    Google Scholar 

  19. Schmidt, K. A. & Ostfeld, R. S. Biodiversity and the dilution effect in disease ecology. Ecology 82, 609–619 (2001).

    Google Scholar 

  20. Woolhouse, M. E. J., Dye, C. & Etard, J. Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc. Natl Acad. Sci. USA 94, 338–342 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Graystock, P., Goulson, D. & Hughes, W. O. H. Parasites in bloom: flowers aid dispersal and transmission of pollinator parasites within and between bee species. Proc. R. Soc. B 282, 20151371 (2015).

    PubMed  PubMed Central  Google Scholar 

  22. Rigaud, T., Perrot-Minnot, M.-J. & Brown, M. J. F. Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proc. R. Soc. B 277, 3693–3702 (2010).

    PubMed  PubMed Central  Google Scholar 

  23. Adler, L. S. et al. Disease where you dine: plant species and floral traits associated with pathogen transmission in bumble bees. Ecology 99, 2535–2545 (2018).

    PubMed  Google Scholar 

  24. McFrederick, Q. S. et al. Flowers and wild megachilid bees share microbes. Microb. Ecol. 73, 188–200 (2017).

    PubMed  Google Scholar 

  25. CaraDonna, P. J. et al. Interaction rewiring and the rapid turnover of plant-pollinator networks. Ecol. Lett. 20, 385–394 (2017).

    PubMed  Google Scholar 

  26. Jones, K. E. et al. Global trends in emerging infectious diseases. Nature 451, 990–993 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Piot, N. et al. Establishment of wildflower fields in poor quality landscapes enhances micro-parasite prevalence in wild bumble bees. Oecologia 189, 149–158 (2019).

    PubMed  Google Scholar 

  28. Theodorou, P. et al. Pollination services enhanced with urbanization despite increasing pollinator parasitism. Proc. R. Soc. B 283, 21060561 (2016).

  29. Graystock, P., Goulson, D. & Hughes, W. O. H. The relationship between managed bees and the prevalence of parasites in bumblebees. PeerJ 2, e522 (2014).

    PubMed  PubMed Central  Google Scholar 

  30. Graystock, P., Blane, E. J., McFrederick, Q. S., Goulson, D. & Hughes, W. O. H. Do managed bees drive parasite spread and emergence in wild bees? Int. J. Parasitol. Parasites Wildl. 5, 64–75 (2016).

    PubMed  Google Scholar 

  31. Alger, S. A., Burnham, P. A., Boncristiani, H. F. & Brody, A. K. RNA virus spillover from managed honeybees (Apis mellifera) to wild bumblebees (Bombus spp.). PLoS ONE 14, e0217822 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Randolph, S. E. & Dobson, A. D. M. Pangloss revisited: a critique of the dilution effect and the biodiversity–buffers–disease paradigm. Parasitology 139, 847–863 (2012).

    CAS  PubMed  Google Scholar 

  33. LoGiudice, K. et al. Impact of host community on Lyme disease risk. Ecology 89, 2841–2849 (2008).

    PubMed  Google Scholar 

  34. Keesing, F. et al. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647–652 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Johnson, P. T. J., Lund, P. J., Hartson, R. B. & Yoshino, T. P. Community diversity reduces Schistosoma mansoni transmission, host pathology and human infection risk. Proc. R. Soc. B 276, 1657–1663 (2009).

    PubMed  PubMed Central  Google Scholar 

  36. Mitchell, C. E., Tilman, D. & Groth, J. V. Effects of grassland plant species diversity, abundance, and composition on foliar fungal disease. Ecology 83, 1713–1726 (2013).

    Google Scholar 

  37. Johnson, P. T. J. & Thieltges, D. W. Diversity, decoys and the dilution effect: how ecological communities affect disease risk. J. Exp. Biol. 213, 961–970 (2010).

    CAS  PubMed  Google Scholar 

  38. Becker, D. J., Streicker, D. G. & Altizer, S. Linking anthropogenic resources to wildlife–pathogen dynamics: a review and meta-analysis. Ecol. Lett. 18, 483–495 (2015).

    PubMed  PubMed Central  Google Scholar 

  39. Nunn, C. L., Thrall, P. H. & Kappeler, P. M. Shared resources and disease dynamics in spatially structured populations. Ecol. Modell. 272, 198–207 (2014).

    Google Scholar 

  40. Durrer, S. & Schmid-Hempel, P. Shared use of flowers leads to horizontal pathogen transmission. Proc. R. Soc. B 258, 299–302 (1994).

    Google Scholar 

  41. Figueroa, L. L. et al. Landscape simplification shapes pathogen prevalence in plant-pollinator networks. Ecol. Lett. https://doi.org/10.1111/ele.13521 (2020).

  42. Truitt, L. L., McArt, S. H., Vaughn, A. H. & Ellner, S. P. Trait-based modeling of multihost pathogen transmission: plant-pollinator networks. Am. Nat. 193, E149–E167 (2019).

    PubMed  PubMed Central  Google Scholar 

  43. Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. & Getz, W. M. Superspreading and the effect of individual variation on disease emergence. Nature 438, 355–359 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Daszak, P. et al. Interdisciplinary approaches to understanding disease emergence: the past, present, and future drivers of Nipah virus emergence. Proc. Natl Acad. Sci. USA 110, 3681–3688 (2013).

    CAS  PubMed  Google Scholar 

  45. Lafferty, K. D. & Gerber, L. R. Good medicine for conservation biology: the intersection of epidemiology and conservation theory. Conserv. Biol. 16, 593–604 (2002).

    Google Scholar 

  46. Cottam, E. M. et al. Integrating genetic and epidemiological data to determine transmission pathways of foot-and-mouth disease virus. Proc. R. Soc. B 275, 887–895 (2008).

    PubMed  PubMed Central  Google Scholar 

  47. Bhatt, S. et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature 526, 207–211 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Pyšek, P. & Richardson, D. M. Invasive species, environmental change and management, and health. Annu. Rev. Environ. Resour. 35, 25–55 (2010).

    Google Scholar 

  49. Malone, J. D. et al. U.S. airport entry screening in response to pandemic influenza: modeling and analysis. Travel Med. Infect. Dis. 7, 181–191 (2009).

    PubMed  PubMed Central  Google Scholar 

  50. Tatem, A. J., Rogers, D. J. & Hay, S. I. Global transport networks and infectious disease spread. Adv. Parasitol. 62, 293–343 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Nicolaides, C., Cueto-Felgueroso, L., González, M. C. & Juanes, R. A metric of influential spreading during contagion dynamics through the air transportation network. PLoS ONE 7, e40961 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Gardner, L. & Sarkar, S. A global airport-based risk model for the spread of dengue infection via the air transport network. PLoS ONE 8, e72129 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Urbanowicz, C. M., Muñiz, P. A. & McArt, S. H. Honey bees and wild bees differ in their preference for and use of introduced floral resources. Ecol. Evol. https://doi.org/10.1002/ece3.6417 (2020).

  54. Wiegand, K. M. & Eames, A. J. The Flora of the Cayuga Lake Basin, New York https://doi.org/10.5962/bhl.title.59518 (The University, 1926).

  55. Medina, B. F. & Medina, V. Central Appalachian Wildflowers (Falcon Guides, 2002).

  56. House, H. D. The Wild Flowers of New York (Univ. of New York Albany, 1918).

  57. Niering, W. A., Olmstead, N. C., Rayfield, S. & Nehring, C. National Audubon Society Field Guide to North American Wildflowers (Eastern Region) (AbeBooks, 1979).

  58. Ascher, J. S. & Pickering, J. DiscoverLife Bee Species Guide and World Checklist (Hymenoptera: Apoidea: Anthophila) (Discover Life, 2020); http://www.discoverlife.org/mp/20q?guide=Apoidea_species

  59. Gibbs, J. Revision of the metallic Lasioglossum (Dialictus) of eastern North America (Hymenoptera: Halictidae: Halictini). Zootaxa 216, 1–216 (2011).

    Google Scholar 

  60. Grixti, J. C., Wong, L. T., Cameron, S. A. & Favret, C. Decline of bumble bees (Bombus) in the North American Midwest. Biol. Conserv. 142, 75–84 (2009).

    Google Scholar 

  61. Sheffield, C. S., Ratti, C., Packer, L. & Griswold, T. Leafcutter and mason bees of the genus Megachile Latreille (Hymenoptera: Megachilidae) in Canada and Alaska. Can. J. Arthropod Identif. 18, 1–107 (2011).

    Google Scholar 

  62. Schwarz, R. S. & Evans, J. D. Single and mixed-species trypanosome and microsporidia infections elicit distinct, ephemeral cellular and humoral immune responses in honey bees. Dev. Comp. Immunol. 40, 300–310 (2013).

    CAS  PubMed  Google Scholar 

  63. Meeus, I., Brown, M. J. F., de Graaf, D. C. & Smagghe, G. Effects of invasive parasites on bumble bee declines. Conserv. Biol. 25, 662–671 (2011).

    PubMed  Google Scholar 

  64. Solter, L. F. in Microsporidia: Pathogens of Opportunity 1st edn (eds Weiss, L. M. & Becnel, J. J.) 165–194 (Wiley–Blackwell, 2014).

  65. Otti, O. & Schmid-Hempel, P. Nosema bombi: a pollinator parasite with detrimental fitness effects. J. Invertebr. Pathol. 96, 118–124 (2007).

    PubMed  Google Scholar 

  66. Graystock, P., Yates, K., Darvill, B., Goulson, D. & Hughes, W. O. H. Emerging dangers: deadly effects of an emergent parasite in a new pollinator host. J. Invertebr. Pathol. 114, 114–119 (2013).

    PubMed  Google Scholar 

  67. Fürst, M. A., McMahon, D. P., Osborne, J. L., Paxton, R. J. & Brown, M. J. F. Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506, 364–366 (2014).

    PubMed  PubMed Central  Google Scholar 

  68. Otti, O. & Schmid-Hempel, P. A field experiment on the effect of Nosema bombi in colonies of the bumblebee Bombus terrestris. Ecol. Entomol. 33, 577–582 (2008).

    Google Scholar 

  69. Higes, M., Martín-Hernández, R. & Meana, A. Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie 41, 375–392 (2010).

    Google Scholar 

  70. Li, J. et al. Diversity of Nosema associated with bumblebees (Bombus spp.) from China. Int. J. Parasitol. Parasites Wildl. 42, 49–61 (2012).

    CAS  Google Scholar 

  71. Sinpoo, C., Disayathanoowat, T., Williams, P. H. & Chantawannakul, P. Prevalence of infection by the microsporidian Nosema spp. in native bumblebees (Bombus spp.) in northern Thailand. PLoS ONE 14, e0213171 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Müller, U., McMahon, D. P. & Rolff, J. Exposure of the wild bee Osmia bicornis to the honey bee pathogen Nosema ceranae. Agric. Entomol. 21, 363–371 (2019).

    Google Scholar 

  73. Bramke, K., Müller, U., McMahon, D. P. & Rolff, J. Exposure of larvae of the solitary bee Osmia bicornis to the honey bee pathogen Nosema ceranae affects life history. Insects 10, 380 (2019).

    PubMed Central  Google Scholar 

  74. Brown, M. J. F., Schmid-Hempel, R. & Schmid-Hempel, P. Strong context-dependent virulence in a host–parasite system: reconciling genetic evidence with theory. J. Anim. Ecol. 72, 994–1002 (2003).

    Google Scholar 

  75. Yourth, C. P., Brown, M. J. F. & Schmid-Hempel, P. Effects of natal and novel Crithidia bombi (Trypanosomatidae) infections on Bombus terrestris hosts. Insectes Soc. 55, 86–90 (2008).

    Google Scholar 

  76. Brown, M. J. F., Loosli, R. & Schmid-Hempel, P. Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91, 421–427 (2000).

    Google Scholar 

  77. Gegear, R. J., Otterstatter, M. C. & Thomson, J. D. Bumble-bee foragers infected by a gut parasite have an impaired ability to utilize floral information. Proc. R. Soc. B 273, 1073–1078 (2006).

    PubMed  PubMed Central  Google Scholar 

  78. Imhoof, B. & Schmid-Hempel, P. Patterns of local adaptation of a protozoan parasite to its bumblebee host. Oikos 82, 59–65 (1998).

    Google Scholar 

  79. Dill, L. M. Costs of energy shortfall for bumble bee colonies: predation, social parasitism, and brood development. Can. Entomol. 123, 283–293 (1991).

    Google Scholar 

  80. Strobl, V., Yañez, O., Straub, L., Albrecht, M. & Neumann, P. Trypanosomatid parasites infecting managed honeybees and wild solitary bees. Int. J. Parasitol. 49, 605–613 (2019).

    PubMed  Google Scholar 

  81. Ravoet, J. et al. Differential diagnosis of the honey bee trypanosomatids Crithidia mellificae and Lotmaria passim. J. Invertebr. Pathol. 130, 21–27 (2015).

    PubMed  Google Scholar 

  82. Ngor, L. et al. Cross-infectivity of honey and bumble bee-associated parasites across three bee families. Parasitology https://doi.org/10.1017/S0031182020001018 (2020).

  83. Lipa, J. J. & Triggiani, O. Apicystis gen. nov. and Apicystis bombi (Liu, Macfarlane & Pengelly) comb. nov. (Protozoa: Neogregarinida), a cosmopolitan parasite of Bombus and Apis (Hymenoptera: Apidae). Apidologie 27, 29–34 (1996).

    Google Scholar 

  84. Graystock, P., Meeus, I., Smagghe, G., Goulson, D. & Hughes, W. O. H. The effects of single and mixed infections of Apicystis bombi and deformed wing virus in Bombus terrestris. Parasitology 143, 358–365 (2016).

    PubMed  Google Scholar 

  85. Maharramov, J. et al. Genetic variability of the neogregarine Apicystis bombi, an etiological agent of an emergent bumblebee disease. PLoS ONE 8, e81475 (2013).

    PubMed  PubMed Central  Google Scholar 

  86. Rutrecht, S. T. & Brown, M. J. F. The life-history impact and implications of multiple parasites for bumble bee queens. Int. J. Parasitol. 38, 799–808 (2008).

    PubMed  Google Scholar 

  87. Plischuk, S., Meeus, I., Smagghe, G. & Lange, C. E. Apicystis bombi (Apicomplexa: Neogregarinorida) parasitizing Apis mellifera and Bombus terrestris (Hymenoptera: Apidae) in Argentina. Environ. Microbiol. Rep. 3, 565–568 (2011).

    PubMed  Google Scholar 

  88. Tian, T., Piot, N., Meeus, I. & Smagghe, G. Infection with the multi-host micro-parasite Apicystis bombi (Apicomplexa: Neogregarinorida) decreases survival of the solitary bee Osmia bicornis. J. Invertebr. Pathol. 158, 43–45 (2018).

    PubMed  Google Scholar 

  89. Lacey, L. A. Manual of Techniques in Insect Pathology (Academic Press, 1997).

  90. Fries, I. et al. Standard methods for Nosema research. J. Apic. Res. 52, 1–28 (2013).

    Google Scholar 

  91. Mullins, J. L., Strange, J. P. & Tripodi, A. D. Why are queens broodless? Failed nest initiation not linked to parasites, mating status, or ovary development in two bumble bee species of Pyrobombus (Hymenoptera: Apidae: Bombus). J. Econ. Entomol. 113, 575–581 (2019).

  92. Schmid-Hempel, R. & Tognazzo, M. Molecular divergence defines two distinct lineages of Crithidia bombi (Trypanosomatidae), parasites of bumblebees. J. Eukaryot. Microbiol. 57, 337–345 (2010).

    CAS  PubMed  Google Scholar 

  93. Tripodi, A. D., Szalanski, A. L. & Strange, J. P. Novel multiplex PCR reveals multiple trypanosomatid species infecting North American bumble bees (Hymenoptera: Apidae: Bombus). J. Invertebr. Pathol. 153, 147–155 (2018).

    PubMed  Google Scholar 

  94. King, G. & Zeng, L. Logistic regression in rare events data. Polit. Anal. 9, 137–163 (2001).

    Google Scholar 

  95. Nelder, J. A. A reformulation of linear models. J. R. Stat. Soc. Ser. A 140, 48–77 (1977).

    Google Scholar 

  96. Venables, W. N. Exegeses on linear models. In SPLUS User’s Conference (2000); https://www.stats.ox.ac.uk/pub/MASS3/Exegeses.pdf

  97. R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2018).

  98. Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

  99. Brooks, Mollie et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R. J. 9, 378–400 (2017).

    Google Scholar 

  100. Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (Multi-level/Mixed) Regression Models. R package v.0.2.0 https://CRAN.R-project.org/package=DHARMa (2018).

  101. Signorell, A. DescTools: Tools for Descriptive Statistics https://cran.r-project.org/web/packages/DescTools/index.html (2019).

  102. Wood, S. N., Pya, N. & Säfken, B. Smoothing parameter and model selection for general smooth models. J. Am. Stat. Assoc. 111, 1548–1563 (2016).

    CAS  Google Scholar 

  103. Engels, B. XNomial: Exact Goodness-of-Fit Test for Multinomial Data with Fixed Probabilities https://cran.r-project.org/web/packages/XNomial/vignettes/XNomial.html (2015).

  104. Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biom. J. 50, 346–363 (2008).

    PubMed  Google Scholar 

  105. Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.4-3 https://www.researchgate.net/publication/323265822_vegan_Community_Ecology_Package_R_package_version_24-3_2017_accessed_2016_Jan_1 (2017).

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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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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 4, 1358–1367 (2020). https://doi.org/10.1038/s41559-020-1247-x

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