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PCR-Based Screening of Pathogens in Bombus terrestris Populations of Turkey

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Abstract

Purpose

Bumblebees are an important group of insects in the pollination of various vegetables, fruits, oilseeds, legumes, and the fodder crops. Compared to honeybees, they have a wider choice of hosts and a longer flight period. These bees are used especially for the pollination of plants in greenhouses and are commercially produced for this purpose. Recently, serious decreases have been occurring in bumblebee populations due to various reasons such as pathogens, and some of species are even threatened with extinction. Due to the worldwide decline in pollinator insects, determining the distribution and prevalence of bumblebee pathogens is of great importance. Therefore, this study was conducted to determine the incidence and prevalence of pathogens in Turkish bumblebee populations and how much of each pathogen was in bumblebee samples.

Methods

A total of 172 Bombus terrestris (Linnaeus,1758) samples (21 samples from commercial enterprises, 79 samples from greenhouses and 72 samples from nature) were randomly collected from 3 provinces (Antalya, Mersin and İzmir) where greenhouse cultivation is intensively carried out in Turkey. Eighty-nine of these samples were collected in the spring and eighty-three in the autumn. The presence of four pathogens (Nosema bombi, Crithidia bombi, Apicystis bombi, and Locustacarus buchneri) was investigated by PCR using universal primers.

Results

The overall prevalence of Nosema bombi, Crithidia bombi, Apicystis bombi, and Locustacarus buchneri was determined as 7.55%, 9.3%, 11.62%, and 4.65%, respectively. Co-infections (5.81%) were only detected in wild-caught (nature) samples. C. bombi and A. bombi infections were detected at higher rates in the spring samples than in the autumn samples (p < 0.05). There was no significant difference between the spring and autumn samples with respect to the presence of N. bombi and L. buchneri (p > 0.05).

Conclusion

The results obtained could be important in determining the prevalence and spread rates of the bumblebee diseases in Turkey and to determine appropriate protection measures. The information gathered should increase our knowledge about the presence of these pathogens in Turkey and could contribute to improve apiarist’s practice. More studies are needed to determine the transmission pathways of these pathogens between the populations. Also, complex pathogen interactions in bumblebee populations should be considered in the future to improve bumblebee health.

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Data Availability

All data generated or analyzed during this study are included in this published article.

References

  1. Pattemore DE (2017) Pollination. In: Thomas B, Murray BG, Murphy DJ (eds) Encyclopedia of Applied Plant Sciences, 2nd edn. Academic Press, Cambridge, pp 309–320

    Chapter  Google Scholar 

  2. Aizen MA, Arbetman MP, Chacoff NP, Chalcoff VR, Feinsinger P, Garibaldi LA, Harder LD, Morales CL, Sáez A, Vanbergen AJ (2020) Invasive bees and their impact on agriculture. In: Bohan DA, Vanbergen AJ (eds) Advances in Ecological Research, 1st edn. Academic Press, Cambridge, pp 49–92

    Google Scholar 

  3. Hoy MA (2019) Insect population ecology and molecular genetics. In: Hoy MA (ed) Insect Molecular Genetics, 4th edn. Academic Press, Cambridge, pp 515–561

    Chapter  Google Scholar 

  4. Velthuis HHW, 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

    Article  Google Scholar 

  5. Kissinger CN, Cameron SA, Thorp RW, White B, Solter LF (2011) Survey of bumble bee (Bombus) pathogens and parasites in Illinois and selected areas of northern California and southern Oregon. J Invertebr Pathol 107:220–224. https://doi.org/10.1016/j.jip.2011.04.008

    Article  PubMed  Google Scholar 

  6. Argun Karslı BA, Gürel F (2014) Identification of some important bumblebee (Bombus terrestris L.) parasites by molecular methods. Uludag Bee Journal 14:88–98

    Google Scholar 

  7. Colla SR, Otterstatter MC, Gegear RJ, Thomson JD (2006) Plight of the bumble bee: pathogen spillover from commercial to wild populations. Biol Conserv 129:461–467. https://doi.org/10.1016/j.biocon.2005.11.013

    Article  Google Scholar 

  8. Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumble bees. Annu Rev Entomol 53:191–208. https://doi.org/10.1146/annurev.ento.53.103106.093454

    Article  CAS  PubMed  Google Scholar 

  9. 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

    Article  PubMed  PubMed Central  Google Scholar 

  10. Bartolomé C, Jabal-Uriel C, Buendía-Abad M, Benito M, Ornosa C, De la Rúa P, Martín-Hernández R, Higes M, Maside X (2021) Wide diversity of parasites in Bombus terrestris (Linnaeus, 1758) revealed by a high-throughput sequencing approach. Environ Microbiol 23:478–483. https://doi.org/10.1111/1462-2920.15336

    Article  CAS  PubMed  Google Scholar 

  11. Tokarev YS, Zinatullina ZY, Ignatieva AN, Zhigileva ON, Malysh JM, Sokolova YY (2018) Detection of two Microsporidia pathogens of the European honeybee Apis mellifera (Insecta: Apidae) in Western Siberia. Acta Parasit 63:728–732. https://doi.org/10.1515/ap-2018-0086

    Article  Google Scholar 

  12. Erler S, Lommatzsch S, Lattorff HM (2012) Comparative analysis of detection limits and specificity of molecular diagnostic markers for three pathogens (Microsporidia, Nosema spp.) in the key pollinators Apis mellifera and Bombus terrestris. Parasitol Res 110:1403–1410. https://doi.org/10.1007/s00436-011-2640-9

    Article  PubMed  Google Scholar 

  13. Vavilova V, Sormacheva I, Woyciechowski M, Eremeeva N, Fet V, Strachecka A, Bayborodin SI, Blinov A (2015) Distribution and diversity of Nosema bombi (Microsporidia: Nosematidae) in the natural populations of bumblebees (Bombus spp.) from West Siberia. Parasitol Res 114:3373–3383. https://doi.org/10.1007/s00436-015-4562-4

    Article  PubMed  Google Scholar 

  14. Lannutti L, Gonzales FN, Dus Santos MJ, Florin-Christensen M, Schnittger L (2022) Molecular detection and differentiation of arthropod, fungal, protozoan, bacterial and viral pathogens of honeybees. Vet Sci 9:221–231. https://doi.org/10.3390/vetsci9050221

    Article  PubMed  PubMed Central  Google Scholar 

  15. Argun Karslı B, Gürel F (2016) Bumblebee diseases and parasites. Nevşehir J Sci Technol 5:228–235. https://doi.org/10.1710/nevbiltek.211002

    Article  Google Scholar 

  16. Eldeniz Cankaya N, Kaftanoglu O (2006) An Investigation on Some Diseases and Parasites of Bumblebee Queens (Bombus terrestris L.) in Turkey. Pak J Biol Sci 9:1282–1286. https://doi.org/10.3923/pjbs.2006.1282.1286

    Article  Google Scholar 

  17. Aytekin AM, Çağatay N, Hazır S (2002) Floral choices, parasites and microorganisms in natural populations of bumblebees (Apidae: Hymenoptera) in Ankara province. Turk J Zool 26:149–155

    Google Scholar 

  18. Sevim A, Akpınar R, Karaoğlu ŞA, Bozdeveci A, Sevim E (2022) Prevalence and phylogenetic analysis of Ascosphaera apis (Maassen ex Claussen) LS Olive & Spiltoir (1955) isolates from honeybee colonies in Turkey. Biologia. https://doi.org/10.1007/s11756-022-01114-7

    Article  Google Scholar 

  19. Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp 41:95–98

    CAS  Google Scholar 

  20. Benson DA, Karsch-Mizrachi I, Clark K, Lipman DJ, Ostell J, Sayers EW (2012) GenBank. Nucleic Acids Res 40(Database issue):D48–D53

    Article  CAS  PubMed  Google Scholar 

  21. Belsky JE, Camp AA, Lehmann DM (2020) The importance of males to bumblebee (Bombus species) nest development and colony viability. Insects 11:506–522. https://doi.org/10.3390/insects11080506

    Article  PubMed  PubMed Central  Google Scholar 

  22. Mola JM, Hemberger J, Kochanski J, Richardson LL, Pearse IS (2021) The importance of forests in bumble bee biology and conservation. Bioscience 71:1234–1248. https://doi.org/10.1093/biosci/biab121

    Article  Google Scholar 

  23. Cameron SA, Sadd BM (2020) Global trends in bumble bee health. Annu Rev Entomol 65:209–232. https://doi.org/10.1146/annurev-ento-011118-111847

    Article  CAS  PubMed  Google Scholar 

  24. Pislak Ocepek M, Toplak I, Zajc U, Bevk D (2021) The Pathogens spillover and incidence correlation in bumblebees and honeybees in Slovenia. Pathogens 10:884. https://doi.org/10.3390/pathogens10070884

    Article  PubMed  PubMed Central  Google Scholar 

  25. Bosmans L, Pozo MI, Verreth C, Crauwels S, Wilberts L, Sobhy IS, Wackers F, Jacquemyn H, Lievens B (2018) Habitat specific variation in gut microbial communities and pathogen prevalence in bumblebee queens (Bombus terrestris). PLoS ONE 13(10):e0204612. https://doi.org/10.1371/journal.pone.0204612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Felden A, Baty JW, Lester PJ (2021) Gut microbial communities and pathogens infection in New Zealand bumble bees (Bombus terrestris, Linnaeus, 1758). NZ Entomol 44:71–80. https://doi.org/10.1080/00779962.2022.2053350

    Article  Google Scholar 

  27. Trillo A, Brown MJF, Vilà M (2019) Prevalence of Nosema microsporidians in commercial bumblebees (Bombus terrestris) is not related to the intensity of their use at the landscape scale. Apidologie 50:234–242. https://doi.org/10.1007/s13592-019-00637-4

    Article  Google Scholar 

  28. Yoneda M, Furuta H, Tsuchida K, Okabe K, Goka K (2008) Commercial colonies of Bombus terrestris (Hymenoptera: Apidae) are reservoirs of the tracheal mite Locustacarus buchneri (Acari: Podapolipidae). Appl Entomol Zool 43:73–76. https://doi.org/10.1303/aez.2008.73

    Article  Google Scholar 

  29. Murray TE, Coffey MF, Kehoe E, Horgan FG (2013) Pathogen prevalence in commercially reared bumble bees and evidence of spillover in conspecific populations. Biol Conserv 159:269–276. https://doi.org/10.1016/j.biocon.2012.10.021

    Article  PubMed  PubMed Central  Google Scholar 

  30. Ignoffo CM (1992) Environmental factors affecting persistence of entomopathogens. Fla Entomol 75:516e525. https://doi.org/10.2307/3496133

    Article  Google Scholar 

  31. Shapiro Ilan DI, Bruck DJ, Lacey LA (2012) Principles of epizootiology and microbial control. In: Vega F, Kaya HK (eds) Insect Pathology, 2nd edn. Elsevier, San Diego, pp 29–72

    Chapter  Google Scholar 

  32. Yoon HJ, Kim SE, Kim YS (2002) Temperature and humidity favorable for colony development of the indoor-reared bumblebee, Bombus ignites. Appl Entomol Zool 37:419–423. https://doi.org/10.1303/aez.2002.419

    Article  Google Scholar 

  33. Couvillon MJ, Fitzpatrick G, Dornhaus A (2010) Ambient air temperature does not predict whether small or large workers forage in bumble bees (Bombus impatiens). Psyche. https://doi.org/10.1155/2010/536430

    Article  PubMed  Google Scholar 

  34. Pawlikowski T, Sparks TH, Olszewski P, Pawlikowski K, Rutokowski L, Jakubowski R (2020) Rising temperatures advance the main flight period of Bombus bumblebees in agricultural landscapes of the Central European Plain. Apidologie 51:652–663. https://doi.org/10.1007/s13592-020-00750-9

    Article  Google Scholar 

  35. Sharma HK, Kalia L, Sharma R, Thakur M, Prasad H, Devi M, Thakur P, Sharma D, Rna K (2021) Seasonal incidence, epidemiology and establishment of different pests and disease in laboratory reared Bombus haemorrhoidalis Smith. Int J Trop Insect Sci 41:2555–2564. https://doi.org/10.1007/s42690-021-00435-5

    Article  Google Scholar 

  36. Plischuk S, Martín-Hernández R, Prieto L, Lucía M, Botías C, Meana A, Abrahamovich AH, Lange C, Higes M (2009) South American native bumblebees (Hymenoptera: Apidae) infected by Nosema ceranae (Microsporidia), an emerging pathogen of honeybees (Apis mellifera). Environ Microbiol Rep 1:131–135. https://doi.org/10.1111/j.1758-2229.2009.00018.x

    Article  PubMed  Google Scholar 

  37. Schmid Hempel R, Tognazzo M (2010) Molecular divergence defines two distinct lineages of Crithidia bombi (Trypanosomatidae), parasites of bumblebees. J Eukoryat Microbiol 57:337–345. https://doi.org/10.1111/j.1550-7408.2010.00480.x

    Article  CAS  Google Scholar 

  38. Meesus 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. https://doi.org/10.1111/j.1365-2672.2009.04635.x

    Article  CAS  Google Scholar 

  39. Goka K, Okabe K, Yoneda M, Niwa S (2001) Bumblebee commercialization will cause worldwide migration of parasitic mites. Mol Ecol 10:2095–2099. https://doi.org/10.1046/j.0962-1083.2001.01323.x

    Article  CAS  PubMed  Google Scholar 

  40. Pislak Ocepek M, Toplak I, Zajc U, Bevk D (2021) The pathogens spillover and incidence correlation in bumblebees and honeybees in Slovenia. Pathogens 10(7):884. https://doi.org/10.3390/pathogens10070884

    Article  PubMed  PubMed Central  Google Scholar 

  41. Adler LS, Michaud KM, Ellner SP, McArt SH, Stevenson PC, Irwin RE (2018) Disease where you dine: Plant species and floral traits associated with pathogen transmission in bumble bees. Ecology 99:2535–2545. https://doi.org/10.1002/ecy.2503

    Article  PubMed  Google Scholar 

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Funding

This study was supported by T.C. Ministry of Agriculture and Forestry, General Directorate of Agricultural Research and Policies under the project number of TAGEM/HSGYAD/G/18/A5/P3/736.

Author information

Authors and Affiliations

  1. Department of Plant Protection, Faculty of Agriculture, Kırşehir Ahi Evran University, Kırşehir, 40100, Turkey

    Ali Sevim

  2. Honeybee Diseases Laboratory, T.C Ministry of Agriculture and Forestry, Samsun Veterinary Control Institute, Samsun, Turkey

    Rahşan Akpınar

  3. T.C Ministry of Agriculture and Forestry, Ordu Apiculture Research Institute, Ordu, Turkey

    Seyit Hasan Öztürk, Fatih Yılmaz, Ümit Kayaboynu, Hasan Ese, Ümit Karataş & Mücahit Buldağ

  4. Department of Medical Biology, Faculty of Medicine, Kırşehir Ahi Evran University, Kırşehir, 40100, Turkey

    Elif Sevim

  5. Department of Veterinary Parasitology, Faculty of Veterinary Medicine, Ondokuz Mayıs University, Samsun, Turkey

    Şinasi Umur

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  1. Ali Sevim
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  2. Rahşan Akpınar
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Contributions

AS participated in almost all parts of the study such as the study conception, design, analysis, and writing the manuscript. RA participated in PCR and sequence analysis. SHÖ, FY, ÜK, HE, ÜK, MB, and ŞU performed collection of the bee samples and DNA extraction from the samples. Elif Sevim participated in gene sequencing.

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Correspondence to Ali Sevim.

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Sevim, A., Akpınar, R., Öztürk, S.H. et al. PCR-Based Screening of Pathogens in Bombus terrestris Populations of Turkey. Acta Parasit. 69, 275–282 (2024). https://doi.org/10.1007/s11686-023-00743-5

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