Skip to main content
Log in

Occurrence of bee viruses and pathogens associated with emerging infectious diseases in native and non-native bumble bees in southern Chile

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The invasion of non-native bees to new ecological territories could spread novel pathogens causing emerging infectious diseases (EIDs) in native species. We provide novel information on the prevalence, load, and co-infection network of honey bee viruses, trypanosoma, microsporidia and neogregarinorida pathogens in native Bombus dahlbomii and non-native Bombus terrestris and Bombus ruderatus. Apicystis bombi and Crithidia bombi were highly prevalent (> 78%) in three bumble bee species, with high loads of these pathogens. Nosema bombi was detected only in B. terrestris (37%) and B. ruderatus (15%). Lotmaria passim was detected in low prevalence (< 6%) and low loads in three bumble bee species. Deformed wing virus (genotype A) was detected only in B. terrestris (20%) and B. ruderatus (6%). Black queen cell virus was detected in B. terrestris (34%), B. ruderatus (22%) and B. dahlbomii (23%). Chronic bee paralysis virus, Kashmir bee virus and Acute bee paralysis virus were detected with low prevalence (7%) and titers in the three bumble bee species. The proximity of apiaries and collection sites was not a significant factor in the presence of viruses in bumble bees. The three bumble species were found to be co-infected with Apicystis bombi and C. bombi; a significant positive correlation was found between these two parasites, especially in B. terrestris. Multiple infections with N. bombi, A. bombi, C. bombi and viruses in B. terrestris and B. ruderatus were also detected. This suggests that the invasion and successful establishment of exotic bumble bees in a new area also entails the possible establishment of the pathogens that they carry, which could also be present in native bee species. This finding evidences a potential link between the population decline of B. dahlbomii and the pathogens that were detected with high levels and prevalence.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data accessibility

Real time PCR data are available in Zenodo data base. https://doi.org/10.5281/zenodo.3332941.

References

  • Abrahamovich AH, Díaz NB, Morrone JJ (2004) Distributional patterns of the neotropical and andean species of the genus Bombus (Hymenoptera: Apidae). Acta Zool Mex 20:99–117

    Article  Google Scholar 

  • Alger SA, Burnham PA, Boncristiani HF et al (2019a) RNA virus spillover from managed honeybees (Apis mellifera) to wild bumblebees (Bombus spp.). PloS One 14(6):e0217822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alger SA, Burnham PA, Brody AK (2019b) Flowers as viral hot spots: Honey bees (Apis mellifera) unevenly deposit viruses across plant species. PLoS ONE 14(9):e0221800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anido M, Branchiccela B, Castelli L et al (2015) Prevalence and distribution of honey bee pathogens in Uruguay. J Apicult Res 54:532–540

    Article  Google Scholar 

  • Arbetman MP, Meeus I, Morales CL et al (2013) Alien parasite hitchhikes to Patagonia on invasive bumblebee. Biol Invasions 15:489–494

    Article  Google Scholar 

  • Arbulo N, Antúnez K, Salvarrey S et al (2015) High prevalence and infection levels of Nosema ceranae in bumblebees Bombus atratus and Bombus bellicosus from Uruguay. J Invert Pathol 130:165–168

    Article  CAS  Google Scholar 

  • Arismendi N, Bruna A, Zapata N et al (2016a) Molecular detection of the tracheal mite Locustacarus buchneri in native and non-native bumble bees in Chile. Insectes Soc 63:629–633

    Article  Google Scholar 

  • Arismendi N, Bruna A, Zapata N et al (2016b) PCR-specific detection of recently described Lotmaria passim (Trypanosomatidae) in Chilean apiaries. J Invert Pathol 134:1–5

    Article  CAS  Google Scholar 

  • Arismendi N, Caro S, Castro MP et al (2020) Impact of mixed infections of gut parasites Lotmaria passim and Nosema ceranae on the lifespan and immune-related biomarkers in Apis mellifera. Insects 11:420

  • Blanchard P, Schurr F, Olivier V et al (2009) Phylogenetic analysis of the RNA-dependent RNA polymerase (RdRp) and a predicted structural protein (pSP) of the Chronic bee paralysis virus (CBPV) isolated from various geographic regions. Virus Res 144:334–338

    Article  CAS  PubMed  Google Scholar 

  • Brown MJF (2017) Microsporidia: an emerging threat to bumblebees? Trends Parasitol 33:754–762

    Article  CAS  PubMed  Google Scholar 

  • Brown MJF, Loosli R, Schmid-Hempel P (2000) Condition-dependent expression of virulence in a trypanosome infecting bumble bees. Oikos 91:421–427

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Castelli L, Branchiccela B, Invernizzi C et al (2019) Detection of Lotmaria passim in Africanized and European honey bees from Uruguay, Argentina and Chile. J Invert Pathol 160:95–97

    Article  Google Scholar 

  • Chester S (2008) A wildlife guide to Chile: Continental Chile, Chilean Antarctica, Easter Island, Juan Fernandez Archipelago. Princeton University Press, Princeton, pp 10–13

    Book  Google Scholar 

  • Choi YS, Lee MY, Hong IP et al (2010) Detection of honey bee virus from bumblebee (Bombus terrestris and Bombus ignitus). Korean J Apicult 25:259–266

    Google Scholar 

  • Colla SR, Otterstatter MC, Gegear RJ et al (2006) Plight of the bumble bee: pathogen spillover from commercial to wild populations. Biol Conserv 129:461–467

    Article  Google Scholar 

  • Couvillon MJ, Pearce FCR, Accleton C et al (2015) Honey bee foraging distance depends on month and forage type. Apidologie 46:61–70

    Article  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 287:443–449

    Article  CAS  PubMed  Google Scholar 

  • de Landa GF, Revainera P, Brasesco C et al (2020) Chronic bee paralysis virus (CBPV) in South American non-Apis bees. Arch Virol 165:2053–2056

    Article  CAS  Google Scholar 

  • de Miranda J, Cordoni G, Budge G (2010) The acute bee paralysis virus-Kashmir bee virus-Israeli acute paralysis virus complex. J Invert Pathol 103:S30–S47

    Article  CAS  Google Scholar 

  • Dolezal AG, Hendrix SD, Scavo NA et al (2016) Honey bee viruses in wild bees: viral prevalence, loads, and experimental inoculation. PLoS ONE 11:e0166190

  • Evans JD, Pettis JS (2005) Colony-level impacts of immune responsiveness in honey bees, Apis mellifera. Evolution 59:2270–2274

    CAS  PubMed  Google Scholar 

  • Fantham HB, Porter A (1914) The morphology, biology and economic importance of Nosema bombi, parasitic in various humble bees (Bombus spp.). Ann Tropical Med Parasitol 8:623–638

    Article  Google Scholar 

  • Fürst MA, McMahon DP, Osborne JL et al (2014) Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506:364–366

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gamboa V, Ravoet J, Brunain M et al (2015) Honey bee pathogens in Bombus atratus from Colombia: a case study. J Invert Pathol 129:36–39

    Article  Google Scholar 

  • Genersch E, Yue C, Fries I et al (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

    Article  Google Scholar 

  • Gisder S, Genersch E (2017) Viruses of commercialized insect pollinators. J Invert Pathol 147:51–59

    Article  Google Scholar 

  • Goulson D, Hughes WOH (2015) Mitigating the anthropogenic spread of bee parasites to protect wild pollinators. Biol Conserv 191:10–19

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Graystock P, Meeus I, Smagghe G et al (2016) The effects of single and mixed infections of Apicystis bombi and deformed wing virus in Bombus terrestris. Parasitology 143:358–365

    Article  PubMed  Google Scholar 

  • Huang WF, Solter LF (2013) Comparative development and tissue tropism of Nosema apis and Nosema ceranae. J Invert Pathol 113:35–41

    Article  Google Scholar 

  • Johnson RM, Evans JD, Robinson GE et al (2009) Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera). PNAS 106:14790–14795

    Article  CAS  PubMed  Google Scholar 

  • Kukielka D, Esperón F, Higes M et al (2008) A sensitive one-step real-time RT-PCR method for detection of deformed wing virus and black queen cell virus in honeybee Apis mellifera. J Virol Methods 147:275–281

    Article  CAS  PubMed  Google Scholar 

  • Lipa JJ, Triggiani O (1996) 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

    Article  Google Scholar 

  • Madjidian JA, Morales CL, Smith HG (2008) Displacement of a native by an alien bumblebee: lower pollinator efficiency overcome by overwhelmingly higher visitation frequency. Oecologia 156:835–845

    Article  PubMed  Google Scholar 

  • Manley R, Temperton B, Doyle T et al (2019) Knock-on community impacts of a novel vector: spillover of emerging DWV-B from Varroa-infested honeybees to wild bumblebees. Ecol Lett. https://doi.org/10.1111/ele.13323

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Meeus I, De Graaf DC, Jans K et al (2010) Multiplex PCR detection of slowly-evolving trypanosomatids and neogregarines in bumblebees using broad-range primers. J Appl Microbiol 109:107–115

    Article  CAS  PubMed  Google Scholar 

  • Meeus I, de Miranda JR, de Graaf DC et al (2014) Effect of oral infection with Kashmir bee virus and Israeli acute paralysis virus on bumblebee (Bombus terrestris) reproductive success. J Invert Pathol 121:64–69

    Article  Google Scholar 

  • Montalva J, Ruz L, Arroyo MTK (2008) Bombus terrestris Linnaeus (Hymenoptera: pidae). Causas y consecuencias de su introducción. Chagual 6:13–20

    Google Scholar 

  • Montalva J, Dudley L, Arroyo MK et al (2011) Geographic distribution and associated flora of native and introduced bumble bees (Bombus spp.). J Apicult Res 50:11–21

    Article  Google Scholar 

  • Morales CL, Arbetman MP, Cameron SA et al (2013) Rapid ecological replacement of a native bumble bee by invasive species. Front Ecol Environ 11:529–534

    Article  Google Scholar 

  • Morales C, Montalva J, Arbetman M et al (2016) Bombus dahlbomii. IUCN Red List Threatened Species 2016:e.T21215142A100240441. https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T21215142A100240441

    Article  Google Scholar 

  • Osborne J, Martin AP, Carreck NL et al (2008) Bumblebee flight distances in relation to the forage landscape. J Anim Ecol 77:406–415

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Peng WJ, Li J, Boncristiani H et al (2011) Host range expansion of honey bee black queen cell virus in the bumblebee, Bombus huntii. Apidologie 42:650–658

    Article  Google Scholar 

  • Plischuk S, Lange CE (2012) Sphaerularia bombi (Nematoda: Sphaerulariidae) arasitizing Bombus atratus (Hymenoptera: Apidae) in southern South America. Parasitol Res 111:947–950

    Article  PubMed  Google Scholar 

  • Plischuk S, Lange CE (2016) Bombus brasiliensis Lepeletier (Hymenoptera, Apidae) infected with Nosema ceranae (Microsporidia). Rev Brasil Entomol 60:347–351

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Plischuk S, Meeus I, Smagghe G et al (2011) Apicystis bombi (Apicomplexa: Neogregarinorida) parasitizing Apis mellifera and Bombus terrestris (Hymenoptera: Apidae) in Argentina. Environ Microbiol Reports 3:565–568

    Article  Google Scholar 

  • Plischuk S, Pocco ME, Lange CE (2013) The tracheal mite Locustacarus buchneri in South American native bumble bees (Hymenoptera: Apidae). Parasitol Int 62:505–507

    Article  PubMed  Google Scholar 

  • Plischuk S, Salvarrey S, Arbulo N et al (2017) Pathogens, parasites, and parasitoids associated with bumble bees (Bombus spp.) from Uruguay. Apidologie 48:298–310

    Article  Google Scholar 

  • Popp M, Lattorff HMG (2011) A Quantitative in vitro cultivation technique to determine cell number and growth rates in strains of Crithidia bombi (Trypanosomatidae), a parasite of bumblebees. J Eukaryot Microbiol 58:7–10

    Article  PubMed  Google Scholar 

  • Poulin R (2007) Evolutionary ecology of parasites. Chapter 8: Interactions between species and the parasite niche. 2nd edn, Princeton University Press, New Jersey, pp 188–208

  • Reynaldi FJ, Sguazza GH, Albicoro FJ et al (2013) First molecular detection of co-infection of honey bee viruses in asymptomatic Bombus atratus in South America. Brazilian J Biol 73:797–800

    Article  CAS  Google Scholar 

  • Riveros G, Arismendi N, Zapata N et al (2020) Occurrence, prevalence and viral load of deformed wing virus variants in Apis mellifera colonies in Chile. J Apicult Res 59:63–68

    Article  Google Scholar 

  • Rutrecht ST, Brown MJF (2008) The life-history impact and implications of multiple parasites for bumble bee queens. Int J Parasitol 38:799–808

    Article  PubMed  Google Scholar 

  • Ruz L (2002) Bee pollinators introduced to Chile: a review. In: Kevan P, Imperatriz F (eds) Pollinating bees the conservation link between agriculture and nature. Ministry of Environment, Brasilia, pp 155–167

    Google Scholar 

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

    Article  Google Scholar 

  • Schlüns H, Sadd BM, Schmid-Hempel P et al (2010) Infection with the trypanosome Crithidia bombi and expression of immune-related genes in the bumblebee Bombus terrestris. Dev Comp Immunol 34:705–709

    Article  PubMed  CAS  Google Scholar 

  • Schmid-Hempel R, Eckhardt M, Goulson D et al (2014) The invasion of southern South America by imported bumblebees and associated parasites. J Anim Ecol 83:823–837

    Article  PubMed  Google Scholar 

  • Schwarz RS, Bauchan GR, Murphy CA et al (2015) Characterization of two species of Trypanosomatidae from the honey bee Apis mellifera: Crithidia mellificae Langridge and McGhee, 1967 and Lotmaria passim n. gen., n. sp. J Eukaryot Microbiol 62:567–583

    Article  PubMed  Google Scholar 

  • Sguazza GH, Reynaldi FJ, Galosi CM et al (2013) Simultaneous detection of bee viruses by multiplex PCR. J Virol Methods 194:102–106

    Article  CAS  PubMed  Google Scholar 

  • Shen M, Yang X, Cox-Foster D et al (2005) The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees. Virology 342:141–149

    Article  CAS  PubMed  Google Scholar 

  • Singh R, Levitt AL, Rajotte EG et al (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith KF, Sax DF, Lafferty KD (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conserv Biol 20:1349–1357

    Article  PubMed  Google Scholar 

  • Stout JC, Morales CL (2009) Ecological impacts of invasive alien species on bees. Apidologie 40:388–409

    Article  Google Scholar 

  • Tripodi AD, Szalanski AL, Strange JP (2018) Novel multiplex PCR reveals multiple trypanosomatid species infecting North American bumble bees (Hymenoptera: Apidae: Bombus). J Invert Pathol 153:147–155

    Article  Google Scholar 

  • Tritschler M, Retschnig G, Yañez O et al (2017) Host sharing by the honey bee parasites Lotmaria passim and Nosema ceranae. Ecol Evol 7:1850–1857

    Article  PubMed  PubMed Central  Google Scholar 

  • Vargas M, Arismendi N, Riveros G et al (2017) Viral and intestinal diseases detected in Apis mellifera in Central and Southern Chile. Chilean J Agricult Res 77:243–249

    Article  Google Scholar 

  • Weinstein-Teixeira E, Chen Y-P, Message D et al (2008) Virus infections in Brazilian honey bees. J Invert Pathol 99:117–119

    Article  CAS  Google Scholar 

  • Williams ES, Yuill T, Artois M et al (2002) Emerging infectious diseases in wildlife. Rev Sci Tech Off Int Epiz 21:139–157

    Article  CAS  Google Scholar 

  • Williams PH, Cameron SA, Hines HM et al (2008) A simplified subgeneric classification of the bumblebees (genus Bombus). Apidologie 39:46–74

    Article  Google Scholar 

  • Wu Y, Dong X, Kadowaki T (2017) Characterization of the copy number and variants of Deformed Wing Virus (DWV) in the pairs of honey bee pupa and infesting Varroa destructor or Tropilaelaps mercedesae. Front Microbiol 8:1558

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was supported by Grants FONDECYT No 1171781 and FONDECYT No 11170088 from the National Commission for Scientific and Technological Research, CONICYT, Chile.

Author information

Authors and Affiliations

Authors

Contributions

NA designed new primers, carried out the field work, and led the manuscript writing. GR conducted the laboratory work and helped in the sampling collection. MV guided the research and designed the experimental work in the field. NZ, GS and CG contributed to the analysis of the results. All authors provided manuscript input, editing and collaboration in the discussions of the results.

Corresponding author

Correspondence to Marisol Vargas.

Ethics declarations

Conflict of interest

The authors declare that they do not have conflicts of interest or competing interests to disclose.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Arismendi, N., Riveros, G., Zapata, N. et al. Occurrence of bee viruses and pathogens associated with emerging infectious diseases in native and non-native bumble bees in southern Chile. Biol Invasions 23, 1175–1189 (2021). https://doi.org/10.1007/s10530-020-02428-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-020-02428-w

Keywords

Navigation