in

Effects of planted pollinator habitat on pathogen prevalence and interspecific detection between bee species

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

    PubMed 
    Article 

    Google Scholar 

  • Sorensen, A., Van Beest, F. M. & Brook, R. K. Impacts of wildlife baiting and supplemental feeding on infectious disease transmission risk: A synthesis of knowledge. Prev. Vet. Med. 113, 356–363 (2014).

    PubMed 
    Article 

    Google Scholar 

  • Gortázar, C., Acevedo, P., Ruíz-Fons, F. & Vicente, J. Disease risks and overabundance of game species. Eur. J. Wildl. Res. 52, 81–87 (2006).

    Article 

    Google Scholar 

  • Brittingham, M. C. & Temple, S. A. Avian disease and winter bird feeding. Passeng. Pigeon 50, (1998).

  • Franz, M., Kramer-Schadt, S., Greenwood, A. D. & Courtiol, A. Sickness-induced lethargy can increase host contact rates and pathogen spread in water-limited landscapes. Funct. Ecol. 32, 2194–2204 (2018).

    Article 

    Google Scholar 

  • Galbraith, J. A., Stanley, M. C., Jones, D. N. & Beggs, J. R. Experimental feeding regime influences urban bird disease dynamics. J. Avian Biol. 48, 700–713 (2017).

    Article 

    Google Scholar 

  • Moyers, S. C., Adelman, J. S., Farine, D. R., Thomason, C. A. & Hawley, D. M. Feeder density enhances house finch disease transmission in experimental epidemics. Philos. Trans. R. Soc. B Biol. Sci. 373(1745), 20170090 (2018).

    Article 
    CAS 

    Google Scholar 

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

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Mathiasson, M. E. & Rehan, S. M. Status changes in the wild bees of north-eastern North America over 125 years revealed through museum specimens. Insect Conserv. Divers. 12, 278–288 (2019).

    Google Scholar 

  • Vanbergen, A. J. & Initiative, I. P. Threats to an ecosystem service: pressures on pollinators. Front. Ecol. Env. 11, 251–259 (2013).

    Article 

    Google Scholar 

  • Buhk, C. et al. Flower strip networks offer promising long term effects on pollinator species richness in intensively cultivated agricultural areas. BMC Ecol. 18(1), 1–13 (2018).

    Article 

    Google Scholar 

  • Morandin, L. A. & Kremen, C. Hedgerow restoration promotes pollinator populations and exports native bees to adjacent fields. Ecol. Appl. 23, 829–839 (2013).

    PubMed 
    Article 

    Google Scholar 

  • Williams, N. M. et al. Native wildflower plantings support wild bee abundance and diversity in agricultural landscapes across the United States. Ecol. Appl. 25, 2119–2131 (2015).

    PubMed 
    Article 

    Google Scholar 

  • Graystock, P. et al. Dominant bee species and floral abundance drive parasite temporal dynamics in plant-pollinator communities. Nat. Ecol. Evol. 4, 1358–1367 (2020).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 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 
    Article 

    Google Scholar 

  • Alger, S. A., Burnham, P. A. & Brody, A. K. Flowers as viral hot spots: Honey bees (Apis mellifera) unevenly deposit viruses across plant species. PLoS ONE 14(9), e0221800 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • McNeil, D. J. et al. Bumble bees in landscapes with abundant floral resources have lower pathogen loads. Sci. Rep. 10, 1–12 (2020).

    Article 
    CAS 

    Google Scholar 

  • Daughenbaugh, K. F. et al. Metatranscriptome analysis of sympatric bee species identifies bee virus variants and a new virus, andrena-associated bee virus-1. Viruses 13, 291 (2021).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Alger, S. A., Alexander Burnham, P., 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 
    Article 

    Google Scholar 

  • Ravoet, J. et al. Widespread occurrence of honey bee pathogens in solitary bees. J. Invertebr. Pathol. 122, 55–58 (2014).

    PubMed 
    Article 

    Google Scholar 

  • Hayes, S. E., Tuiwawa, M., Stevens, M. I. & Schwarz, M. P. A recipe for weed disaster in islands: A super-generalist native pollinator aided by a ‘Parlourmaid’ plant welcome new arrivals in Fiji. Biol. Invasions 21, 1643–1655 (2019).

    Article 

    Google Scholar 

  • Levenson, H. & Tarpy, D. R. Pollinator community response to planted pollinator habitat in agroecosystems over time. Authorea https://doi.org/10.22541/au.164191433.37143936/v1 (2022).

    Article 

    Google Scholar 

  • 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 
    Article 

    Google Scholar 

  • Genersch, E., Yue, C., Fries, I. & De Miranda, J. R. Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. J. Invertebr. Pathol. 91, 61–63 (2006).

    PubMed 
    Article 

    Google Scholar 

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

    Article 

    Google Scholar 

  • 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 
    Article 

    Google Scholar 

  • Gisder, S. et al. Rapid gastrointestinal passage may protect Bombus terrestris from becoming a true host for Nosema ceranae. Appl. Environ. Microbiol. 86(12), e00629-20 (2020).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Tehel, A., Streicher, T., Tragust, S. & Paxton, R. J. Experimental infection of bumblebees with honeybee-associated viruses: No direct fitness costs but potential future threats to novel wild bee hosts. R. Soc. Open Sci. 7(7), 200480 (2020).

    ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Reynaldi, F. J., Sguazza, G. H., Albicoro, F. J., Pecoraro, M. R. & Galosi, C. M. First molecular detection of co-infection of honey bee viruses in asymptomatic Bombus atratus in South America. Braz. J. Biol. 73, 797–800 (2013).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Schoonvaere, K. et al. Unbiased RNA shotgun metagenomics in social and solitary wild bees detects associations with eukaryote parasites and new viruses. PLoS ONE 11(12), e0168456 (2016).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Melathopoulos, A. et al. Viruses of managed alfalfa leafcutting bees (Megachille rotundata Fabricus) and honey bees (Apis mellifera L.) in Western Canada: Incidence, impacts, and prospects of cross-species viral transmission. J. Invertebr. Pathol. 146, 24–30 (2017).

    PubMed 
    Article 

    Google Scholar 

  • Schoonvaere, K., Smagghe, G., Francis, F. & de Graaf, D. C. Study of the metatranscriptome of eight social and solitary wild bee species reveals novel viruses and bee parasites. Front. Microbiol. 9, 177 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Payne, A. N., Shepherd, T. F. & Rangel, J. The detection of honey bee (Apis mellifera)-associated viruses in ants. Sci. Rep. 10(1), 1–8 (2020).

    Article 
    CAS 

    Google Scholar 

  • Dalmon, A. et al. Possible spillover of pathogens between bee communities foraging on the same floral resource. Insects 12(2), 122 (2021).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Kojima, Y. et al. Infestation of Japanese native honey bees by tracheal mite and virus from non-native European honey Bees in Japan. Microb. Ecol. 62, 895–906 (2011).

    PubMed 
    Article 

    Google Scholar 

  • Graystock, P. et al. The Trojan hives: Pollinator pathogens, imported and distributed in bumblebee colonies. J. Appl. Ecol. 50, 1207–1215 (2013).

    Article 

    Google Scholar 

  • Plischuk, S. et al. South American native bumblebees (Hymenoptera: Apidae) infected by Nosema ceranae (Microsporidia), an emerging pathogen of honeybees (Apis mellifera). Environ. Microbiol. Rep. 1, 131–135 (2009).

    PubMed 
    Article 

    Google Scholar 

  • Evison, S. E. et al. Pervasiveness of parasites in pollinators. PLoS ONE 7(1), e30641 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 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 
    Article 

    Google Scholar 

  • Graystock, P., Goulson, D. & Hughes, W. O. Parasites in bloom: Flowers aid dispersal and transmission of pollinator parasites within and between bee species. Proc. R. Soc. B Biol. Sci. 282(1813), 20151371 (2015).

    Article 

    Google Scholar 

  • 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 
    Article 

    Google Scholar 

  • Singh, R. et al. RNA viruses in hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS ONE 5(12), e14357 (2010).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Peng, W. et al. Host range expansion of honey bee Black Queen Cell Virus in the bumble bee, Bombus huntii. Apidologie 42, 650–658 (2011).

    Article 

    Google Scholar 

  • Levitt, A. L. et al. Cross-species transmission of honey bee viruses in associated arthropods. Virus Res. 176, 232–240 (2013).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 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).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Gamboa, V. et al. Bee pathogens found in Bombus atratus from Colombia: A case study. J. Invertebr. Pathol. 129, 36–39 (2015).

    PubMed 
    Article 

    Google Scholar 

  • Radzevičiūtė, R. et al. Replication of honey bee-associated RNA viruses across multiple bee species in apple orchards of Georgia, Germany and Kyrgyzstan. J. Invertebr. Pathol. 146, 14–23 (2017).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Murray, E. A. et al. Viral transmission in honey bees and native bees, supported by a global black queen cell virus phylogeny. Environ. Microbiol. 21, 972–983 (2019).

    PubMed 
    Article 

    Google Scholar 

  • Dobelmann, J., Felden, A. & Lester, P. J. Genetic strain diversity of multi-host RNA viruses that infect a wide range of pollinators and associates is shaped by geographic origins. Viruses 12, 13–15 (2020).

    Article 
    CAS 

    Google Scholar 

  • Olgun, T., Everhart, S. E., Anderson, T. & Wu-Smart, J. Comparative analysis of viruses in four bee species collected from agricultural, urban, and natural landscapes. PLoS ONE 15(6), e0234431 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Fearon, M. L. & Tibbetts, E. A. Pollinator community species richness dilutes prevalence of multiple viruses within multiple host species. Ecology 102(5), e03305 (2021).

    PubMed 
    Article 

    Google Scholar 

  • Sokół, R., Michalczyk, M. & Michołap, P. Preliminary studies on the occurrence of honeybee pathogens in the national bumblebee population. Ann. Parasitol. 64, 385–390 (2018).

    PubMed 

    Google Scholar 

  • Bravi, M. E. et al. Wild bumble bees (Hymenoptera: Apidae: Bombini) as a potential reservoir for bee pathogens in northeastern Argentina. J. Apic. Res. 58, 710–713 (2019).

    Article 

    Google Scholar 

  • Mazzei, M. et al. Detection of replicative Kashmir Bee Virus and Black Queen Cell Virus in Asian hornet Vespa velutina (Lepelieter 1836) in Italy. Sci. Rep. 9, 1–9 (2019).

    CAS 
    Article 

    Google Scholar 

  • Li, J. et al. Cross-species infection of deformed wing virus poses a new threat to pollinator conservation. J. Econ. Entomol. 104, 732–739 (2011).

    PubMed 
    Article 

    Google Scholar 

  • Sachman-Ruiz, B., Narváez-Padilla, V. & Reynaud, E. Commercial Bombus impatiens as reservoirs of emerging infectious diseases in central México. Biol. Invasions 17, 2043–2053 (2015).

    Article 

    Google Scholar 

  • Jones, L. J., Ford, R. P., Schilder, R. J. & López-Uribe, M. M. Honey bee viruses are highly prevalent but at low intensities in wild pollinators of cucurbit agroecosystems. J. Invertebr. Pathol. 185, 107667 (2021).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Dolezal, A. G. et al. Honey bee viruses in wild bees: Viral prevalence, loads, and experimental inoculation. PLoS ONE 11(11), e0166190 (2016).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Mazzei, M. et al. First detection of replicative deformed wing virus (DWV) in Vespa velutina nigrithorax. Bull. Insectology 71, 211–216 (2018).

    Google Scholar 

  • Plischuk, S. et al. Parasites and pathogens associated with native bumble bees (Hymenoptera: Apidae: Bombus spp.) from highlands in Bolivia and Peru. Stud. Neotrop. Fauna Environ. Stud. https://doi.org/10.1080/01650521.2020.1743551 (2020).

    Article 

    Google Scholar 

  • McMahon, D. P. et al. A sting in the spit: Widespread cross-infection of multiple RNA viruses across wild and managed bees. J. Anim. Ecol. 84, 615–624 (2015).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Bailes, E. J. et al. First detection of bee viruses in hoverfly (syrphid) pollinators. Biol. Lett. 14(2), 20180001 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Pritchard, Z. A. et al. Do viruses from managed honey bees (Hymenoptera: Apidae) endanger wild bees in native prairies?. Environ. Entomol. 50, 455–466 (2021).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Danforth, B. N., Mitchell, P. L. & Packer, L. Mitochondrial DNA differentiation between two cryptic Halictus (Hymenoptera: Halictidae) species. Ann. Entomol. Soc. Am. 91, 387–391 (1998).

    CAS 
    Article 

    Google Scholar 

  • Grozinger, C. M. & Flenniken, M. L. Bee viruses: Ecology, pathogenicity, and impacts. Annu. Rev. Entomol. 64, 205–226 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Antúnez, K. et al. Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environ. Microbiol. 11, 2284–2290 (2009).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Cameron, S. A. et al. Patterns of widespread decline in North American bumble bees. PNAS 108, 662–667 (2011).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Leite, G. M., Magan, N. & Medina, A. Comparison of different bead-beating RNA extraction strategies: An optimized method for filamentous fungi. J. Microbiol. Methods 88, 413–418 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Simms, D., Cizdziel, P. & Chomczynski, P. TRIzol: A new reagent for optimal single-step isolation of RNA. Focus (Madison) 15, 99–102 (1993).

    Google Scholar 

  • Vandesompele, J. et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3(7), 1–12 (2002).

    Article 

    Google Scholar 

  • Mwalili, S. M., Lesaffre, E. & Declerck, D. The zero-inflated negative binomial regression model with correction for misclassification: An example in caries research. Stat. Methods Med. Res. 17, 123–139 (2008).

    MathSciNet 
    PubMed 
    MATH 
    Article 

    Google Scholar 

  • R Core Team. R: Language and Environment for Statistical Computing. R Foundation for Statistical Computer (2018). Available at: https://www.r-project.org/.

  • Jackman, S. et al. Package ‘pscl’. (2020).

  • Canty, A. & Ripley, B. Package ‘boot’. (2021).

  • Figueroa, L. L. et al. Landscape simplification shapes pathogen prevalence in plant-pollinator networks. Ecol. Lett. 23, 1212–1222 (2020).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • National Heritage Program. Species/Community Search. National Heritage Program: Natural and Cultural Resources (2021). Available at: https://ncnhp.org/data/speciescommunity-search.

  • Hatfield, R. et al. IUCN Assessments for North American Bombus spp. (2014).

  • Sersic, A. N., Masco, M. & Noy-Meir, I. Natural hybridization between species of Calceolaria with different pollination syndromes in southern Patagonia, Argentina. Plant Syst. Evol. 230, 111–124 (2001).

    Article 

    Google Scholar 

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

    PubMed 
    Article 

    Google Scholar 

  • Crabbe, J. C., Wahlsten, D. & Dudek, B. C. Genetics of mouse behavior: Interactions with laboratory environment. Science 284(5420), 1670–1672 (1999).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Wahlsten, D. et al. Different data from different labs: Lessons from studies of gene-environment interaction. J. Nuerobiol. 54, 283–311 (2003).

    Article 

    Google Scholar 

  • Brownie, J. et al. The elimination of primer-dimer accumulation in PCR. Nucleic Acids Res. 25(16), 3235–3241 (1997).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Boncristiani, H. F. et al. In vitro infection of pupae with israeli acute paralysis virus suggests disturbance of transcriptional homeostasis in honey bees (Apis mellifera). PLoS ONE 8(9), e73429 (2013).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 


  • Source: Ecology - nature.com

    Unravelling seasonal trends in coastal marine heatwave metrics across global biogeographical realms

    MIT Climate “Plug-In” highlights first year of progress on MIT’s climate plan