Spatial heterogeneity of microscopically detected Nosema spp. infection in honeybees: Climate-associated patterns in the Eastern Black Sea Region of Türkiye

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Nosemosis has emerged as the predominant microsporidian infection of honeybees (Apis mellifera L.) in many regions, including Türkiye, yet the climatic drivers of its epidemiology remain insufficiently quantified. This study assessed the effects of temperature and relative humidity on nosemosis prevalence across seven provinces in the climatically diverse Eastern Black Sea region. A dataset of 2688 colony-level observations was analyzed using generalized linear models, mixed-effects models, beta regression, generalized additive models, and spatial autocorrelation. Both temperature and humidity were consistently significant predictors (p < .001). Quadratic temperature terms and nonlinear GAM smooths were consistent with a thermal performance pattern, with infection peaking at intermediate ranges. Humidity exerted threshold-like effects, with disproportionately higher prevalence at upper quantiles. Province-level random effects accounted for ∼18% of variance, underscoring spatial heterogeneity, while elevation was not significant once climatic variables were included. Exploratory spatial analysis (Global Moran's I = −0.476, p = 0.043) tentatively suggested dispersion rather than clustering; however, given the very small number of spatial units (n = 7), this result should be regarded as hypothesis-generating only. The beta mixed-effects model achieved moderate predictive accuracy under cross-validation (RMSE ≈ 0.109). Collectively, these findings indicate that nosemosis prevalence in the region is strongly associated with climatic variability, exhibits nonlinear and threshold-like responses, and shows pronounced spatial heterogeneity. We emphasize that these are statistical associations and that unmeasured factors (e.g., colony strength, nutrition, pesticide exposure, management practices, and co-infections) likely contribute to the unexplained variance. By integrating hierarchical, nonlinear, and spatial approaches, this study establishes a climate-associated epidemiological assessment of nosemosis risk in A. mellifera and highlights the importance of localized climatic suitability under ongoing climate change.

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dc.contributor.authorTosun, Onur
dc.contributor.authorBekircan, Çağrı
dc.contributor.authorKurnaz, Muammer
dc.date.accessioned2026-10-22T10:21:34.017107354Z
dc.date.available2026-10-22T10:21:34.017107354Z
dc.date.issued2026
dc.description.abstractNosemosis has emerged as the predominant microsporidian infection of honeybees (Apis mellifera L.) in many regions, including Türkiye, yet the climatic drivers of its epidemiology remain insufficiently quantified. This study assessed the effects of temperature and relative humidity on nosemosis prevalence across seven provinces in the climatically diverse Eastern Black Sea region. A dataset of 2688 colony-level observations was analyzed using generalized linear models, mixed-effects models, beta regression, generalized additive models, and spatial autocorrelation. Both temperature and humidity were consistently significant predictors (p < .001). Quadratic temperature terms and nonlinear GAM smooths were consistent with a thermal performance pattern, with infection peaking at intermediate ranges. Humidity exerted threshold-like effects, with disproportionately higher prevalence at upper quantiles. Province-level random effects accounted for ∼18% of variance, underscoring spatial heterogeneity, while elevation was not significant once climatic variables were included. Exploratory spatial analysis (Global Moran's I = −0.476, p = 0.043) tentatively suggested dispersion rather than clustering; however, given the very small number of spatial units (n = 7), this result should be regarded as hypothesis-generating only. The beta mixed-effects model achieved moderate predictive accuracy under cross-validation (RMSE ≈ 0.109). Collectively, these findings indicate that nosemosis prevalence in the region is strongly associated with climatic variability, exhibits nonlinear and threshold-like responses, and shows pronounced spatial heterogeneity. We emphasize that these are statistical associations and that unmeasured factors (e.g., colony strength, nutrition, pesticide exposure, management practices, and co-infections) likely contribute to the unexplained variance. By integrating hierarchical, nonlinear, and spatial approaches, this study establishes a climate-associated epidemiological assessment of nosemosis risk in A. mellifera and highlights the importance of localized climatic suitability under ongoing climate change.
dc.description.sponsorshipTurkish State Meteorological Service
dc.description.sponsorshipseven Eastern Black Sea provinces
dc.identifier.articlenumber110835
dc.identifier.doi10.1016/j.vetpar.2026.110835
dc.identifier.eissn1873-2550
dc.identifier.issn0304-4017
dc.identifier.pmid42349250
dc.identifier.scopus2-s2.0-105042708761
dc.identifier.startpage110835
dc.identifier.urihttps://rdlopen.rawdatalibrary.net/r/gumushane/13605
dc.identifier.volume346
dc.identifier.wosWOS:001812251000001
dc.language.isoen
dc.publisherElsevier B.V.
dc.relation.ispartofVeterinary Parasitology
dc.rightsinfo:eu-repo/semantics/closedAccess
dc.subjectApis mellifera
dc.subjectClimate change
dc.subjectHumidity
dc.subjectSpatial heterogeneity
dc.subjectTemperature
dc.subject.classificationParasitology
dc.subject.classificationVeterinary Sciences
dc.subject.otherAnimals
dc.subject.otherBees
dc.subject.otherClimate
dc.subject.otherHumidity
dc.subject.otherNosema
dc.subject.otherPrevalence
dc.subject.otherTemperature
dc.subject.otherTurkey
dc.subject.otherApis mellifera
dc.subject.otherArticle
dc.subject.otherautocorrelation
dc.subject.otherBlack Sea
dc.subject.otherclimate change
dc.subject.othercross validation
dc.subject.otherhoneybee
dc.subject.othernonhuman
dc.subject.othernosemosis
dc.subject.otherrelative humidity
dc.subject.otherspatial analysis
dc.subject.otherTurkey (republic)
dc.subject.otheranimal
dc.subject.otherbee
dc.subject.otherepidemiology
dc.subject.otherisolation and purification
dc.subject.othermicrobiology
dc.subject.otherparasitology
dc.subject.otherphysiology
dc.subject.otherturkey (bird)
dc.titleSpatial heterogeneity of microscopically detected Nosema spp. infection in honeybees: Climate-associated patterns in the Eastern Black Sea Region of Türkiye
dc.typeArticle
rdl.citation.openalex0
rdl.citation.scopus0
rdl.citation.wos0
rdl.departmentGümüşhane University, Kelkit Sema Doğan Vocational School of Health Services, Department of Medical Services and Techniques, Gümüşhane, Turkiye
rdl.oa.statusclosed
rdl.scopus.quartileQ1
rdl.sdgSDG02
rdl.source.indexSCOPUS
rdl.source.indexWOS
rdl.source.indexPUBMED
rdl.wos.indexScience Citation Index Expanded (SCI-EXPANDED)