{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T01:46:17Z","timestamp":1790732777457,"version":"4.1.0"},"reference-count":81,"publisher":"Public Library of Science (PLoS)","issue":"5","license":[{"start":{"date-parts":[[2021,5,20]],"date-time":"2021-05-20T00:00:00Z","timestamp":1621468800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/publicdomain\/zero\/1.0\/"}],"funder":[{"DOI":"10.13039\/100007637","name":"Departamento Administrativo de Ciencia, Tecnolog\u00eda e Innovaci\u00f3n","doi-asserted-by":"publisher","award":["202010018161"],"award-info":[{"award-number":["202010018161"]}],"id":[{"id":"10.13039\/100007637","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>\n                    The global spread of the ectoparasitic mite\n                    <jats:italic>Varroa destructor<\/jats:italic>\n                    has promoted the spread and virulence of highly infectious honey bee viruses. This phenomenon is considered the leading cause for the increased number of colony losses experienced by the mite-susceptible European honey bee populations in the Northern hemisphere. Most of the honey bee populations in Central and South America are Africanized honey bees (AHBs), which are considered more resistant to\n                    <jats:italic>Varroa<\/jats:italic>\n                    compared to European honey bees. However, the relationship between\n                    <jats:italic>Varroa<\/jats:italic>\n                    levels and the spread of honey bee viruses in AHBs remains unknown. In this study, we determined\n                    <jats:italic>Varroa<\/jats:italic>\n                    prevalence and infestation levels as well as the prevalence of seven major honey bee viruses in AHBs from three regions of Colombia. We found that although\n                    <jats:italic>Varroa<\/jats:italic>\n                    exhibited high prevalence (92%), its infestation levels were low (4.5%) considering that these populations never received acaricide treatments. We also detected four viruses in the three regions analyzed, but all colonies were asymptomatic, and virus prevalence was considerably lower than those found in other countries with higher rates of mite-associated colony loss (DWV 19.88%, BQCV 17.39%, SBV 23.4%, ABPV 10.56%). Our findings indicate that AHBs possess a natural resistance to\n                    <jats:italic>Varroa<\/jats:italic>\n                    that does not prevent the spread of this parasite among their population, but restrains mite population growth and suppresses the prevalence and pathogenicity of mite-associated viruses.\n                  <\/jats:p>","DOI":"10.1371\/journal.pone.0244906","type":"journal-article","created":{"date-parts":[[2021,5,20]],"date-time":"2021-05-20T13:55:35Z","timestamp":1621518935000},"page":"e0244906","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":26,"title":["Africanized honey bees in Colombia exhibit high prevalence but low level of infestation of Varroa mites and low prevalence of pathogenic viruses"],"prefix":"10.1371","volume":"16","author":[{"given":"V\u00edctor Manuel","family":"Tibat\u00e1","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andr\u00e9s","family":"Sanchez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9258-2073","authenticated-orcid":true,"given":"Evan","family":"Palmer-Young","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Howard","family":"Junca","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0385-0126","authenticated-orcid":true,"given":"Victor Manuel","family":"Solarte","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shayne","family":"Madella","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fernando","family":"Ariza","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Judith","family":"Figueroa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2582-5397","authenticated-orcid":true,"given":"Miguel","family":"Corona","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,5,20]]},"reference":[{"key":"pone.0244906.ref001","first-page":"21","volume-title":"Yearbook of the Association of Pacific Coast Geographers","author":"R Kent","year":"1988"},{"key":"pone.0244906.ref002","volume-title":"Africanized honey bees in the Americas","author":"D Caron","year":"2001"},{"key":"pone.0244906.ref003","first-page":"211","article-title":"Introduction of african honey bees in Brazil","volume":"3","author":"W Kerr","year":"1957","journal-title":"Brasil Apicola"},{"issue":"3","key":"pone.0244906.ref004","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1016\/j.pt.2004.01.001","article-title":"Africanized honeybees have unique tolerance to Varroa mites","volume":"20","author":"S Martin","year":"2004","journal-title":"Trends Parasitol"},{"key":"pone.0244906.ref005","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1051\/apido:19960204","article-title":"Susceptibility of European and Africanized honeybees (Apis mellifera L.) and their hybrids to Varroa jacobsoni Oud","volume":"27","author":"E Guzman-Novoa","year":"1996","journal-title":"Apidologie"},{"key":"pone.0244906.ref006","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1051\/apido:19990206","article-title":"Honey bee (Apis mellifera L.) tolerance to Varroa jacobsoni Oud. in South America","volume":"30","author":"P Rosenkranz","year":"1999","journal-title":"Apidology"},{"issue":"1","key":"pone.0244906.ref007","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3896\/IBRA.1.49.1.01","article-title":"Honey bee colony losses","volume":"49","author":"P Neumann","year":"2010","journal-title":"J Apic Res"},{"issue":"4","key":"pone.0244906.ref008","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1051\/apido\/2009076","article-title":"Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada","volume":"41","author":"E Guzm\u00e1n-Novoa","year":"2010","journal-title":"Apidologie"},{"issue":"6086","key":"pone.0244906.ref009","doi-asserted-by":"crossref","first-page":"1304","DOI":"10.1126\/science.1220941","article-title":"Global honey bee viral landscape altered by a parasitic mite","volume":"336","author":"S Martin","year":"2012","journal-title":"Science"},{"key":"pone.0244906.ref010","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1006\/jipa.1998.4807","article-title":"The transmission of deformed wing virus between honeybees (Apis mellifera L) by the ectoparasitic mite Varroa jacobsoni Oud","volume":"73","author":"P Bowen-Walker","year":"1999","journal-title":"J Invertebr Pathol"},{"key":"pone.0244906.ref011","doi-asserted-by":"crossref","first-page":"2425","DOI":"10.3390\/v3122425","article-title":"Dynamics of persistent and acute deformed wing virus infections in honey bees, Apis mellifera","volume":"3","author":"G Di 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Traynor","year":"2016","journal-title":"Apidologie"},{"issue":"10","key":"pone.0244906.ref015","doi-asserted-by":"crossref","first-page":"2885","DOI":"10.3390\/v7102885","article-title":"Special Issue: Honey Bee Viruses","volume":"7","author":"S Gisder","year":"2015","journal-title":"Viruses"},{"key":"pone.0244906.ref016","doi-asserted-by":"crossref","first-page":"606","DOI":"10.1128\/AEM.72.1.606-611.2006","article-title":"Prevalence and transmission of honey bee viruses","volume":"72","author":"Y Chen","year":"2006","journal-title":"Appli Environ Microbiol"},{"issue":"8","key":"pone.0244906.ref017","doi-asserted-by":"crossref","first-page":"e43562","DOI":"10.1371\/journal.pone.0043562","article-title":"Pathogen webs in collapsing honey bee colonies","volume":"7","author":"R Cornman","year":"2012","journal-title":"PLoS One"},{"issue":"8","key":"pone.0244906.ref018","doi-asserted-by":"crossref","first-page":"e1005757","DOI":"10.1371\/journal.ppat.1005757","article-title":"The Buzz 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Pathol"},{"key":"pone.0244906.ref039","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1051\/apido:19910303","article-title":"The effects of climate and bee race on Varroa jacobsoni Oud infestations in Brazil","volume":"22","author":"G Moretto","year":"1991","journal-title":"Apidologie"},{"key":"pone.0244906.ref040","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1051\/apido:19990207","article-title":"Susceptibility of European and Africanized honey bees (Apis mellifera L.) to Varroa jacobsoni Oud. in Mexico","volume":"30","author":"E Guzman-Novoa","year":"1999","journal-title":"Apidologie"},{"key":"pone.0244906.ref041","doi-asserted-by":"crossref","first-page":"7282","DOI":"10.4238\/2014.February.21.10","article-title":"Africanized honey bees (Apis mellifera) have low infestation levels of the mite Varroa destructor in different ecological regions in Mexico","volume":"13","author":"C Medina-Flores","year":"2014","journal-title":"Genet Mol Res"},{"issue":"4","key":"pone.0244906.ref042","first-page":"381","article-title":"Producci\u00f3n de miel de colonias de abejas (Apis mellifera L.) tratadas y no tratadas con fluvalinato contra Varroa jacobsoni Oudemans en Valle de Bravo, Estado de Mexico","volume":"31","author":"M Arechavaleta-Velasco","year":"2000","journal-title":"Vet M\u00e9x"},{"key":"pone.0244906.ref043","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1080\/00218839.2017.1409065","article-title":"Determination of the Africanized mitotypes in populations of honey bees (Apis mellifera L.) of Colombia","volume":"57","author":"V Tibata","year":"2017","journal-title":"J Apic Res"},{"key":"pone.0244906.ref044","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/j.jip.2014.12.004","article-title":"Differential responses of Africanized and European honey bees (Apis mellifera) to viral replication following mechanical transmission or Varroa destructor parasitism","volume":"126","author":"M Hamiduzzaman","year":"2015","journal-title":"J Invertebr Pathol"},{"issue":"6","key":"pone.0244906.ref045","doi-asserted-by":"crossref","first-page":"835","DOI":"10.1007\/s13592-016-0445-7","article-title":"Honeybee health in South America","volume":"47","author":"M Maggi","year":"2016","journal-title":"Apidologie"},{"key":"pone.0244906.ref046","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1002\/joc.5786","article-title":"Global bimodal precipitation seasonality: A systematic overview","volume":"39","author":"W Knoben","year":"2019","journal-title":"Int J Climatol"},{"key":"pone.0244906.ref047","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1051\/apido:19820308","article-title":"A comparative analysis of shaking solutions for the detection of Varroa jacobsoni on adult honeybees","volume":"13","author":"D De Jong","year":"1982","journal-title":"Apidologie"},{"issue":"1","key":"pone.0244906.ref048","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1128\/AEM.71.1.436-441.2005","article-title":"Quantitative real-time reverse transcription-PCR analysis of deformed wing virus infection in the honeybee (Apis mellifera L.)","volume":"71","author":"Y Chen","year":"2005","journal-title":"Appl Environ Microbiol"},{"issue":"12","key":"pone.0244906.ref049","doi-asserted-by":"crossref","first-page":"7185","DOI":"10.1128\/AEM.70.12.7185-7191.2004","article-title":"Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France","volume":"70","author":"D Tentcheva","year":"2004","journal-title":"Appl Environ Microbiol"},{"issue":"2","key":"pone.0244906.ref050","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/j.jviromet.2007.09.008","article-title":"A sensitive one-step real-time RT-PCR method for detection of deformed wing virus and black queen cell virus in honeybee Apis mellifera","volume":"147","author":"D Kukielka","year":"2008","journal-title":"J Virol Methods"},{"issue":"2","key":"pone.0244906.ref051","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1016\/j.jviromet.2009.06.014","article-title":"One-step real-time quantitative PCR assays for the detection and field study of Sacbrood honeybee and Acute bee paralysis viruses","volume":"161","author":"D Kukielka","year":"2009","journal-title":"J Virol Methods"},{"issue":"3","key":"pone.0244906.ref052","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1051\/apido:2002020","article-title":"Molecular diagnosis of chronic bee paralysis virus infection","volume":"33","author":"M Ribi\u00e8re","year":"2002","journal-title":"Apidologie"},{"issue":"2","key":"pone.0244906.ref053","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1016\/j.virol.2006.11.038","article-title":"Reciprocal sequence exchange between non-retro viruses and hosts leading to the appearance of new host phenotypes","volume":"362","author":"E Maori","year":"2007","journal-title":"Virology"},{"issue":"3","key":"pone.0244906.ref054","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1080\/00218839.1995.11100900","article-title":"Molecular diagnosis of Kashmir bee virus infection","volume":"34","author":"D Stoltz","year":"1995","journal-title":"J Apic Res"},{"issue":"2","key":"pone.0244906.ref055","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1016\/j.jip.2005.08.005","article-title":"Detection of multiple viruses in queens of the honey bee Apis mellifera L","volume":"90","author":"Y Chen","year":"2005","journal-title":"J Invertebr Pathol"},{"key":"pone.0244906.ref056","volume-title":"An {R} Companion to Applied Regression","author":"J Fox","year":"2011","edition":"2"},{"key":"pone.0244906.ref057","article-title":"Agricolae: Statistical Procedures for Agricultural Research","author":"F de Mendiburu","year":"2016","journal-title":"R package version 1.2\u20134"},{"key":"pone.0244906.ref058","volume-title":"RStudio: Integrated Development for R","author":"RStudio Team","year":"2016"},{"issue":"1","key":"pone.0244906.ref059","doi-asserted-by":"crossref","first-page":"47","DOI":"10.4206\/agrosur.2007.v35n1-17","article-title":"Sanidad ap\u00edcola en Chile, situaci\u00f3n de las principales enfermedades","volume":"35","author":"M Neira","year":"2007","journal-title":"Agro Sur"},{"issue":"1","key":"pone.0244906.ref060","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1590\/S1415-47572003000100008","article-title":"Genetic structure of honeybee populations from southern Brazil and Uruguay","volume":"26","author":"N Diniz","year":"2003","journal-title":"Genet Mol Biol"},{"key":"pone.0244906.ref061","first-page":"474","article-title":"Effect of ambient temperature and humidity conditions on the efficacy of organic treatments against Varroa destructor in differ- ent climatic zones of Chile","volume":"A 3","author":"P Aldea","year":"2013","journal-title":"J Agric Sci Technol"},{"key":"pone.0244906.ref062","doi-asserted-by":"crossref","first-page":"752","DOI":"10.1007\/s13592-014-0293-2","article-title":"Genetic changes in Apis mellifera after 40 years of Africanization","volume":"45","author":"B Branchiccela","year":"2014","journal-title":"Apidologie"},{"issue":"2","key":"pone.0244906.ref063","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1038\/sj.hdy.6800988","article-title":"Asymmetric introgression of African genes in honeybee populations (Apis mellifera L.) in Central Mexico. Heredity","volume":"99","author":"F Kraus","year":"2007","journal-title":"Heredity"},{"issue":"181","key":"pone.0244906.ref064","first-page":"15","article-title":"Situaci\u00f3n sanitaria de las abejas mel\u00edferas en Uruguay","volume":"47","author":"CA Invernizzi","year":"2011","journal-title":"Veterinaria"},{"issue":"17","key":"pone.0244906.ref065","first-page":"243","article-title":"Varroosis in honey bees in different environmental and regional conditions of Jalisco, Mexico","volume":"6","author":"J Tapia-Gonzalez","year":"2019","journal-title":"Ecosist Recur Agropec"},{"issue":"1","key":"pone.0244906.ref066","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1093\/jisesa\/iew029","article-title":"Varroa destructor (Mesostigmata: Varroidae) Parasitism and Climate Differentially Influence the Prevalence, Levels, and Overt Infections of Deformed Wing Virus in Honey Bees (Hymenoptera: Apidae)","volume":"16","author":"R Anguiano-Baez","year":"2016","journal-title":"J Insect 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Res"},{"issue":"6273","key":"pone.0244906.ref070","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1126\/science.aac9976","article-title":"Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites","volume":"351","author":"L Wilfert","year":"2016","journal-title":"Science"},{"key":"pone.0244906.ref071","first-page":"11","volume-title":"Honey Bee Pest, Predators, & Diseases","author":"B Ball","year":"1997"},{"key":"pone.0244906.ref072","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1099\/0022-1317-37-1-175","article-title":"Two more small RNA viruses from honey bees and further observations on sacbrood and acute bee-paralysis viruses","volume":"37","author":"L Bailey","year":"1977","journal-title":"J Gen Virol"},{"key":"pone.0244906.ref073","first-page":"292","article-title":"Pathogen and queen bees","volume":"94","author":"D Anderson","year":"1993","journal-title":"Australasian Beekeeper"},{"key":"pone.0244906.ref074","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1080\/0005772X.1982.11097891","article-title":"Viruses of honeybees","volume":"63","author":"L Bailey","year":"1982","journal-title":"Bee World"},{"key":"pone.0244906.ref075","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1111\/j.1744-7348.1988.tb03300.x","article-title":"The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni","volume":"113","author":"B Ball","year":"1988","journal-title":"Ann Appl Biol"},{"key":"pone.0244906.ref076","first-page":"241","volume-title":"Present Status of Varroatosis in Europe and Progress in the Varroa Mite Control","author":"B Ball","year":"1989"},{"issue":"6","key":"pone.0244906.ref077","doi-asserted-by":"crossref","first-page":"e0129956","DOI":"10.1371\/journal.pone.0129956","article-title":"Overwintering Is Associated with Reduced Expression of Immune Genes and Higher Susceptibility to Virus Infection in Honey Bees","volume":"10","author":"N Steinmann","year":"2015","journal-title":"PLoS One"},{"key":"pone.0244906.ref078","first-page":"73","article-title":"Varroa jacobsoni in South Africa","volume":"69","author":"M Allsopp","year":"1997","journal-title":"S Afr Bee J"},{"issue":"4","key":"pone.0244906.ref079","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1099\/jgv.0.000757","article-title":"ICTV Virus Taxonomy Profile: Iflaviridae","volume":"98","author":"S Valles","year":"2017","journal-title":"J Gen Virol"},{"issue":"1","key":"pone.0244906.ref080","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1099\/vir.0.025965-0","article-title":"Recombinants between Deformed wing virus and Varroa destructor virus-1 may prevail in Varroa destructor-infested honeybee colonies","volume":"92","author":"J Moore","year":"2011","journal-title":"J Gen 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