Species Traits, Landscape Quality and Floral Resource Overlap with Honeybees Determine Virus Transmission in Plant-pollinator Networks

Overview

Journal Nat Ecol Evol

Publisher Springer Nature

Specialty Biology

Date 2024 Oct 4

PMID 39367259

Authors

Corina Maurer

Alexandria Schauer

Orlando Yanez

Peter Neumann

Anna Gajda

Robert J Paxton

Loic Pellissier

Oliver Schweiger

Hajnalka Szentgyorgyi

Adam J Vanbergen

Matthias Albrecht

Affiliations

Soon will be listed here.

Abstract

Emerging infectious diseases pose a threat to pollinators. Virus transmission among pollinators via flowers may be reinforced by anthropogenic land-use change and concomitant alteration of plant-pollinator interactions. Here, we examine how species' traits and roles in flower-visitation networks and landscape-scale factors drive key honeybee viruses-black queen cell virus (BQCV) and deformed wing virus-in 19 wild bee and hoverfly species, across 12 landscapes varying in pollinator-friendly (flower-rich) habitat. Viral loads were on average more than ten times higher in managed honeybees than in wild pollinators. Viral loads in wild pollinators were higher when floral resource use overlapped with honeybees, suggesting these as reservoir hosts, and increased with pollinator abundance and viral loads in honeybees. Viral prevalence decreased with the amount of pollinator-friendly habitat in a landscape, which was partly driven by reduced floral resource overlap with honeybees. Black queen cell virus loads decreased with a wild pollinator's centrality in the network and the proportion of visited dish-shaped flowers. Our findings highlight the complex interplay of resource overlap with honeybees, species traits and roles in flower-visitation networks and flower-rich pollinator habitat shaping virus transmission.

Citing Articles

Species traits, landscape quality and floral resource overlap with honeybees determine virus transmission in plant-pollinator networks.

Maurer C, Schauer A, Yanez O, Neumann P, Gajda A, Paxton R Nat Ecol Evol. 2024; 8(12):2239-2251.

PMID: 39367259 PMC: 11618065. DOI: 10.1038/s41559-024-02555-w.

References

Manley R, Boots M, Wilfert L . Condition-dependent virulence of slow bee paralysis virus in Bombus terrestris: are the impacts of honeybee viruses in wild pollinators underestimated?. Oecologia. 2017; 184(2):305-315. PMC: 5487845. DOI: 10.1007/s00442-017-3851-2. View

Bustin S, Benes V, Garson J, Hellemans J, Huggett J, Kubista M . The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009; 55(4):611-22. DOI: 10.1373/clinchem.2008.112797. View

Schmidt S, Schmid-Egger C, Moriniere J, Haszprunar G, Hebert P . DNA barcoding largely supports 250 years of classical taxonomy: identifications for Central European bees (Hymenoptera, Apoidea partim). Mol Ecol Resour. 2015; 15(4):985-1000. DOI: 10.1111/1755-0998.12363. View

Alaux C, Allier F, Decourtye A, Odoux J, Tamic T, Chabirand M . A 'Landscape physiology' approach for assessing bee health highlights the benefits of floral landscape enrichment and semi-natural habitats. Sci Rep. 2017; 7:40568. PMC: 5234012. DOI: 10.1038/srep40568. View

Maurer C, Schauer A, Yanez O, Neumann P, Gajda A, Paxton R . Species traits, landscape quality and floral resource overlap with honeybees determine virus transmission in plant-pollinator networks. Nat Ecol Evol. 2024; 8(12):2239-2251. PMC: 11618065. DOI: 10.1038/s41559-024-02555-w. View

Gisder S, Genersch E . Viruses of commercialized insect pollinators. J Invertebr Pathol. 2016; 147:51-59. DOI: 10.1016/j.jip.2016.07.010. View

Fearon M, Wood C, Tibbetts E . Habitat quality influences pollinator pathogen prevalence through both habitat-disease and biodiversity-disease pathways. Ecology. 2022; 104(2):e3933. PMC: 10078577. DOI: 10.1002/ecy.3933. View

Ruiz-Villalba A, Ruijter J, van den Hoff M . Use and Misuse of C in qPCR Data Analysis and Reporting. Life (Basel). 2021; 11(6). PMC: 8229287. DOI: 10.3390/life11060496. View

Bluthgen N, Menzel F, Bluthgen N . Measuring specialization in species interaction networks. BMC Ecol. 2006; 6:9. PMC: 1570337. DOI: 10.1186/1472-6785-6-9. View

10.

Bosco L, Yanez O, Schauer A, Maurer C, Cushman S, Arlettaz R . Landscape structure affects temporal dynamics in the bumble bee virome: Landscape heterogeneity supports colony resilience. Sci Total Environ. 2024; 946:174280. DOI: 10.1016/j.scitotenv.2024.174280. View

11.

Tehel A, Streicher T, Tragust S, Paxton R . 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. 2020; 7(7):200480. PMC: 7428241. DOI: 10.1098/rsos.200480. View

12.

McNeil D, McCormick E, Heimann A, Kammerer M, Douglas M, Goslee S . Bumble bees in landscapes with abundant floral resources have lower pathogen loads. Sci Rep. 2020; 10(1):22306. PMC: 7749142. DOI: 10.1038/s41598-020-78119-2. View

13.

Figueroa L, Grab H, Ng W, Myers C, Graystock P, McFrederick Q . Landscape simplification shapes pathogen prevalence in plant-pollinator networks. Ecol Lett. 2020; 23(8):1212-1222. PMC: 7340580. DOI: 10.1111/ele.13521. View

14.

Casanelles-Abella J, Frey D, Muller S, Aleixo C, Orti M, Deguines N . A dataset of the flowering plants (Angiospermae) in urban green areas in five European cities. Data Brief. 2021; 37:107243. PMC: 8258796. DOI: 10.1016/j.dib.2021.107243. View

15.

Fearon M, Tibbetts E . Pollinator community species richness dilutes prevalence of multiple viruses within multiple host species. Ecology. 2021; 102(5):e03305. DOI: 10.1002/ecy.3305. View

16.

Jones L, Ford R, Schilder R, Lopez-Uribe M . Honey bee viruses are highly prevalent but at low intensities in wild pollinators of cucurbit agroecosystems. J Invertebr Pathol. 2021; 185:107667. DOI: 10.1016/j.jip.2021.107667. View

17.

Greenleaf S, Williams N, Winfree R, Kremen C . Bee foraging ranges and their relationship to body size. Oecologia. 2007; 153(3):589-96. DOI: 10.1007/s00442-007-0752-9. View

18.

Doublet V, Oddie M, Mondet F, Forsgren E, Dahle B, Furuseth-Hansen E . Shift in virus composition in honeybees () following worldwide invasion by the parasitic mite and virus vector . R Soc Open Sci. 2024; 11(1):231529. PMC: 10776227. DOI: 10.1098/rsos.231529. View

19.

Casanelles-Abella J, Fontana S, Fournier B, Frey D, Moretti M . Low resource availability drives feeding niche partitioning between wild bees and honeybees in a European city. Ecol Appl. 2022; 33(1):e2727. PMC: 10077915. DOI: 10.1002/eap.2727. View

20.

Civitello D, Cohen J, Fatima H, Halstead N, Liriano J, McMahon T . Biodiversity inhibits parasites: Broad evidence for the dilution effect. Proc Natl Acad Sci U S A. 2015; 112(28):8667-71. PMC: 4507196. DOI: 10.1073/pnas.1506279112. View