Abstract
Acarapisosis is a disease of the adult honey bee Apis mellifera L., caused by the tracheal mite Acarapis woodi (Rennie), that affects the prothoracic tracheas of worker honey bees. Although it is not usually considered a real problem for honey bee colonies in southern Europe (mainly Spain and Greece), where the majority of professional beekeepers are located in Europe, recent works have reported the constant presence of this mite in this area, making it a potential cofactor for colony losses. In this study, we developed a specific PCR diagnostic tool that improves the techniques used so far and allowed us to confirm the presence of this parasite in Spain, urging the need to monitor its prevalence and implications in the health of the colonies. Indeed, in a total of 635 apiaries analysed, the prevalence of A. woodi in 2010 was 8.3 and 4 % in 2011. The mite is present in bee colonies over time and should not be underestimated as a possible cofactor in the collapse of bee colonies. Additionally, some positive samples were cloned so a genetic analysis on the diversity within A. woodi isolates was also approached. This allowed us to identify different genetic variants within an isolate, even when they were present at low frequencies. And this genetic analysis revealed the existence of a different clade of Acarapis sequences that could represent a new species or subspecies, although more research is required to verify the identity of this novel lineage at genetic and morphological level.
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References
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Massachusetts
Chauzat MP, Cauquil L, Roy L et al (2013) Demographics of the European apicultural industry. PLoS One 8:e79018. doi:10.1371/journal.pone.0079018
Downey DL, Winston ML (2001) Honey bee colony mortality and productivity with single and dual infestations of parasitic mite species. Apidologie 32:567–575. doi:10.1051/apido:2001144
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. doi:10.1093/nar/gkh340
Evans JD, Pettis JS, Smith IB (2007) A diagnostic genetic test for the honey bee tracheal mite, Acarapis woodi. J Apic Res 46:195–197. doi:10.3896/IBRA.1.46.3.11
Fichter BL (1988) ELISA detection of Acarapis woodi. In: Needham GR, Page RE Jr, Delfinado-Baker M, Bowman CE (eds) Africanized honey bees and bee mites. Ellis Horwood, Chichester, pp 526–529
Fries I (2010) Nosema ceranae in European honey bees (Apis mellifera). J Invertebr Pathol 103(Suppl):S73–S79. doi:10.1016/j.jip.2009.06.017
Garrido-Bailón E (2012) Repercusión potencial en la cabaña apícola española de agentes nosógenos detectados en colonias de Apis mellifera iberiensis. 273pp. PhD thesis
Garrido-Bailón E, Bartolomé C, Prieto L et al (2012) The prevalence of Acarapis woodi in Spanish honey bee (Apis mellifera) colonies. Exp Parasitol 132:530–536. doi:10.1016/j.exppara.2012.08.018
Grant GA, Nelson DL, Olsen PE, Rice WA (1993) The “Elisa” detection of tracheal mites in whole honey bee samples. Am Bee J 133:652–655
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Higes M, Martín-Hernández R, Martínez-Salvador A et al (2010a) A preliminary study of the epidemiological factors related to honey bee colony loss in Spain. Environ Microbiol Rep 2:243–250. doi:10.1111/j.1758-2229.2009.00099.x
Higes M, Martín-Hernández R, Meana A (2010b) Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie 41:375–392. doi:10.1051/apido/2010019
Higes M, Meana A, Bartolomé C et al (2013) Nosema ceranae (Microsporidia), a controversial 21st century honey bee pathogen. Environ Microbiol Rep 5:17–29. doi:10.1111/1758-2229.12024
Kojima Y, Toki T, Morimoto T et al (2011a) Infestation of Japanese native honey bees by tracheal mite and virus from non-native European honey bees in Japan. Microb Ecol 62:895–906. doi:10.1007/s00248-011-9947-z
Kojima Y, Yoshiyama M, Kimura K, Kadowaki T (2011b) PCR-based detection of a tracheal mite of the honey bee Acarapis woodi. J Invertebr Pathol 108:135–137. doi:10.1016/j.jip.2011.07.009
Martín-Hernández R, Botías C, Garrido-Bailón E et al (2012) Microsporidia infecting Apis mellifera: coexistence or competition. Is Nosema ceranae replacing Nosema apis? Environ Microbiol 14:2127–2138. doi:10.1111/j.1462-2920.2011.02645.x
Mutanen M, Hausmann A, Hebert PDN et al (2012) Allopatry as a Gordian knot for taxonomists: patterns of DNA barcode divergence in arctic-alpine Lepidoptera. PLoS One. doi:10.1371/journal.pone.0047214
Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426
Office International des Épizooties, OIE (2008) Manual of standards for diagnostic test and vaccines for terrestrial animals. Chapter 2.2.1. Acarapisosis of honey bees. OIE—World Organisation for Animal Health http://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.02.01_ACARAPISOSIS.pdf Accessed 10 October 2014
Ragsdale D, Furgala B (1987) A serological approach to the detection of Acarapis woodi parasitism in honey bees using an enzyme-linked immunosorbent assay. Apidologie 18:1–10. doi:10.1051/apido:19870101
Ragsdale D, Kjer KM (1989) Diagnosis of tracheal mite (Acarapis woodi Rennie) parasitism of honey bees using a monoclonal based enzyme-linked immunosorbent assay. Am Bee J 129:550–553
Tamura K, Peterson D, Peterson N et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121
Yang B, Peng G, Li T, Kadowaki T (2013) Molecular and phylogenetic characterization of honey bee viruses, Nosema microsporidia, protozoan parasites, and parasitic mites in China. Ecol Evol 3(2):298–311
Acknowledgments
The authors wish to thank the Spanish Beekeepers’ Association for supplying the samples and Dr McMullan and Dr Villa for the control parasitized honey bee samples. R. Martín-Hernández is on contract to the Parque Científico y Tecnológico de Albacete. This study was supported by funding from the Gobierno Castilla-La Mancha (Consejería de Agricultura), INIA-FEDER funds (RTA2005-152 and RTA 2008-00020-C02-01) and MAGRAMA-FEAGA funds (Programa Nacional Apícola 2013–14). We would like to thank Virginia Albendea, María Gajero, Carmen Uceta and Teresa Corrales for their technical support.
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None of the authors have any financial or personal relationships that could inappropriately influence or bias the content of the paper.
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Cepero, A., Martín-Hernández, R., Prieto, L. et al. Is Acarapis woodi a single species? A new PCR protocol to evaluate its prevalence. Parasitol Res 114, 651–658 (2015). https://doi.org/10.1007/s00436-014-4229-6
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DOI: https://doi.org/10.1007/s00436-014-4229-6