First data on the prevalence and distribution of pathogens in bumblebees (Bombus terrestris and Bombus pascuorum) from Spain

  1. Clara Jabal-Uriel 1
  2. Raquel Martín-Hernández 1
  3. Concepcion Ornosa 2
  4. Mariano Higes 1
  5. Eduardo Berriatua 3
  6. Pilar De la Rua 3
  1. 1 Consejería de Agricultura de la Junta de Comunidades de Castilla-La Mancha, España
  2. 2 Universidad Complutense de Madrid, España
  3. 3 Universidad de Murcia, España
Revista:
Spanish journal of agricultural research

ISSN: 1695-971X 2171-9292

Año de publicación: 2017

Volumen: 15

Número: 1

Tipo: Artículo

DOI: 10.5424/SJAR/2017151-9998 DIALNET GOOGLE SCHOLAR lock_openDialnet editor

Otras publicaciones en: Spanish journal of agricultural research

Objetivos de desarrollo sostenible

Resumen

Bumblebees provide pollination services not only to wildflowers but also to economically important crops. In the context of the global decline of pollinators, there is an increasing interest in determining the pathogen diversity of bumblebee species. In this work, wild bumblebees of the species Bombus terrestris and Bombus pascuorum from northern and southern Spain were molecularly screened to detect and estimate prevalence of pathogens. One third of bumblebees were infected: while viruses only infected B. pascuorum, B. terrestris was infected by Apicystis bombi, Crithidia bombi and Nosema bombi. Ecological differences between host species might affect the success of the pathogens biological cycle and consequently infection prevalence. Furthermore, sex of the bumblebees (workers or males), sampling area (north or south) and altitude were important predictors of pathogen prevalence. Understanding how these factors affect pathogens distribution is essential for future conservation of bumblebee wild populations.

Referencias bibliográficas

  • Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, Solter LF, Griswold TL, 2011. Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci USA 108: 662-667. https://doi.org/10.1073/pnas.1014743108
  • Chantawannakul P, Ward L, Boonham N, Brown M, 2006. A scientific note on the detection of honeybee viruses using real-time PCR (TaqMan) in Varroa mites collected from a Thai honeybee (Apis mellifera) apiary. J Invert Pathol 91: 69-73. https://doi.org/10.1016/j.jip.2005.11.001
  • Fantham HB, Porter A, 1914. The morphology, biology and economic importance of Nosema bombi, N. sp., parasitic in various humble bees (Bombus spp.). Ann Trop Med Parasitol 8: 623-638. https://doi.org/10.1080/00034983.1914.11687667
  • Francis RM, Kryger P, 2012. Single assay detection of Acute Bee Paralysis Virus, Kashmir Bee Virus and Israeli Acute Paralysis Virus. J Apic Science 56: 137-146. https://doi.org/10.2478/v10289-012-0014-x
  • Gallot-Lavallée M, Schmid-Hempel R, Vandame R, Vergara CH, Schmid-Hempel P, 2016. Large scale patterns of abundance and distribution of parasites in Mexican bumblebees. J Invert Pathol 133: 73-82. https://doi.org/10.1016/j.jip.2015.12.004
  • Gamboa V, Ravoet J, Brunain M, Smagghe G, Meeus I, Figueroa J, Ria-o D. de Graaf DC, 2015. Bee pathogens found in Bombus atratus from Colombia: A case study. J Invert Pathol 129: 36-39. https://doi.org/10.1016/j.jip.2015.05.013
  • Genersch E, Yue C, Fries I, de Miranda JR, 2006. Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. J Invert Pathol 91: 61-63. https://doi.org/10.1016/j.jip.2005.10.002
  • Goulson D, 2010. Bumblebees: behaviour, ecology, and conservation. Oxford University Press, Oxford, UK. https://doi.org/10.1017/cbo9780511778230.025
  • Goulson D, Whitehorn P, Fowley M, 2012. Influence of urbanisation on the prevalence of protozoan parasites of bumblebees. Ecol Entomol 37: 83-89. https://doi.org/10.1111/j.1365-2311.2011.01334.x
  • Goulson D, Nicholls E, Botías C, Rotheray EL, 2015. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347(6229): 1255957. https://doi.org/10.1126/science.1255957
  • Graystock P, Yates K, Darvill B, Goulson D, Hughes WHO, 2013. Emerging dangers: deadly effects of an emergent parasite in a new pollinator host. J Invert Pathol 114: 114-119. https://doi.org/10.1016/j.jip.2013.06.005
  • Graystock P, Goulson D, Hughes WHO, 2014. The relationship between managed bees and the prevalence of parasites in bumblebees. PeerJ 2: e522. https://doi.org/10.7717/peerj.522
  • Graystock P, Goulson D, Hughes WHO, 2015. Parasites in bloom: flowers aid dispersal and transmission of pollinator parasites within and between bee species. Proc R Soc B 282: 20151371. https://doi.org/10.1098/rspb.2015.1371
  • Martín-Hernández R, Meana A, Prieto L, Martínez-Salvador A, Garrido-Bailón E, Higes M 2007. Outcome of colonization of Apis mellifera by Nosema ceranae. Appl Environ Microbiol 73: 6331-6338. https://doi.org/10.1128/AEM.00270-07
  • Meeus I, de Graaf DC, Jans K, Smagghe G, 2010. Multiplex PCR detection of slowly-evolving trypanosomatids and neogregarines in bumblebees using broad-range primers. J Appl Microbiol 109: 107-115.
  • Meeus I, Brown MJF, de Graaf DC, Smagghe G 2011. Effects of invasive parasites in bumble bee declines. Conserv Biol 25: 662-671. https://doi.org/10.1111/j.1523-1739.2011.01707.x
  • Murray TE, Fitzpatrick U, Brown MJF, Paxton RJ, 2008. Cryptic species diversity in a widespread bumble bee complex revealed using mitochondrial DNA RFLPs. Conserv Genet 9: 653-666. https://doi.org/10.1007/s10592-007-9394-z
  • Ninyerola M, Pons X, Roure JM, 2007. Objective air temperature mapping for the Iberian Peninsula using spatial interpolation and GIS. Int J Climatol 27: 1231-1242. https://doi.org/10.1002/joc.1462
  • Ornosa C, 1996. Una nota de atención sobre la introducción artificial de subespecies foráneas de abejorros polinizadores en la Península Ibérica (Hymenoptera, Apidae, Bombinae). Bol Soc Esp Entomol 20: 259-260.
  • Ornosa C, Ortiz-Sánchez FJ, 2004. Hymenoptera: Apoidea I. In: Fauna Ibérica, vol. 23. Ramos MA et al. (eds.) Museo Nacional de Ciencias Naturales, CSIC. Madrid. 556 pp.
  • Ortiz-Sánchez FJ, 1992. Introducción de Bombus terrestris terrestris (Linneaus, 1758) en el sur de España para la polinización de cultivos de invernadero (Hymenoptera, Apidae). Bol Soc Esp Entomol 16: 247-248.
  • Ploquin EF, Herrera JM, Obeso JR, 2013. Bumblebee community homogenization after uphill shifts in montane areas of northern Spain. Oecologia 173: 1649-1660. https://doi.org/10.1007/s00442-013-2731-7
  • Potts SG, Imperatriz-Fonseca V, Ngo HT, Aizen MA, Biesmeijer JC, Breeze TD, Dicks LV, Garibaldi LA, Hill R, Steele J, Vanbergen AJ (2016) Safeguarding pollinators and their values to human well-being. Nature 540: 220–229. https://doi.org/10.1038/nature20588
  • Rasmont P, Franzén M, Lecocq T, Harpke A, Roberts SPM, Biesmeijer K, Castro L, Cederberg B, Dvorák L, Fitzpatrick Ú, et al., 2015. Climatic risk and distribution atlas of European bumblebees. Biorisk 10 (Spec Issue), 246 pp.
  • Ravoet J, Maharramov J, Meeus I, De Smet L, Wenseleers T, Smagghe G, De Graaf DC, 2013. Comprehensive bee pathogen screening in Belgium reveals Crithidia mellificae as a new contributory factor to winter mortality. PLoS One 8(8): e72443. https://doi.org/10.1371/journal.pone.0072443
  • Scriven JJ, Woodall LC, Goulson D, 2013. Nondestructive DNA sampling from bumblebee faeces. Mol Ecol Res 13 (2): 225-229. https://doi.org/10.1111/1755-0998.12036
  • Singh R, Levitt AL, Rajotte EG, Holmes EC, Ostiguy N, vanEngelsdorp D, Lipkin WI, dePamphilis CW, Toth AL, Cox-Foster DL, 2010. RNA viruses in hymenopteran pollinators: Evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS ONE 5: e14357. https://doi.org/10.1371/journal.pone.0014357
  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725-2729. https://doi.org/10.1093/molbev/mst197
  • Velthuis HHW, van Doorn A, 2006. A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37: 421-451. https://doi.org/10.1051/apido:2006019
  • Whitehorn PR, Tinsle, MC, Brown MJF, Darvill B, Goulson D, 2011. Genetic diversity, parasite prevalence and immunity in wild bumblebees. Proc R Soc Lond 278: 1195-1202. https://doi.org/10.1098/rspb.2010.1550
  • Williams PH, Osborne JL, 2009. Bumblebee vulnerability and conservation world-wide. Apidologie 40: 367-387. https://doi.org/10.1051/apido/2009025