title: Holistic screening of collapsing honey bee colonies in Spain: a case study.
abstract: BACKGROUND
  Here we present a holistic screening of collapsing colonies from three professional apiaries in Spain. Colonies with typical honey bee depopulation symptoms were selected for multiple possible factors to reveal the causes of collapse.
  
  
  RESULTS
  Omnipresent were Nosema ceranae and Lake Sinai Virus. Moderate prevalences were found for Black Queen Cell Virus and trypanosomatids, whereas Deformed Wing Virus, Aphid Lethal Paralysis Virus strain Brookings and neogregarines were rarely detected. Other viruses, Nosema apis, Acarapis woodi and Varroa destructor were not detected. Palinologic study of pollen demonstrated that all colonies were foraging on wild vegetation. Consequently, the pesticide residue analysis was negative for neonicotinoids. The genetic analysis of trypanosomatids GAPDH gene, showed that there is a large genetic distance between Crithidia mellificae ATCC30254, an authenticated cell strain since 1974, and the rest of the presumed C. mellificae sequences obtained in our study or published. This means that the latter group corresponds to a highly differentiated taxon that should be renamed accordingly.
  
  
  CONCLUSIONS
  The results of this study demonstrate that the drivers of colony collapse may differ between geographic regions with different environmental conditions, or with different beekeeping and agricultural practices. The role of other pathogens in colony collapse has to bee studied in future, especially trypanosomatids and neogregarines. Beside their pathological effect on honey bees, classification and taxonomy of these protozoan parasites should also be clarified.
authors.forename: Almudena
authors.initials: A
authors.lastname: Cepero
authors.forename: Jorgen
authors.initials: J
authors.lastname: Ravoet
authors.forename: Tamara
authors.initials: T
authors.lastname: Gómez-Moracho
authors.forename: José Luis
authors.initials: JL
authors.lastname: Bernal
authors.forename: Maria J
authors.initials: MJ
authors.lastname: Del Nozal
authors.forename: Carolina
authors.initials: C
authors.lastname: Bartolomé
authors.forename: Xulio
authors.initials: X
authors.lastname: Maside
authors.forename: Aránzazu
authors.initials: A
authors.lastname: Meana
authors.forename: Amelia V
authors.initials: AV
authors.lastname: González-Porto
authors.forename: Dirk C
authors.initials: DC
authors.lastname: de Graaf
authors.forename: Raquel
authors.initials: R
authors.lastname: Martín-Hernández
authors.affiliation: Bee Pathology Laboratory, Consejería de Agricultura, Gobierno de Castilla-La Mancha, Centro Apícola Regional (CAR), Marchamalo E-19180, Spain. mhiges@jccm.es.
authors.forename: Mariano
authors.initials: M
authors.lastname: Higes
mesh_terms: D000818:Animals; D056630:Beekeeping / Q000379:methods*; D001516:Bees / Q000382:microbiology / Q000469:parasitology / Q000821:virology; D056631:Colony Collapse / Q000382:microbiology / Q000469:parasitology / Q000821:virology; D017753:Ecosystem; D005247:Feeding Behavior; D006790:Host-Parasite Interactions; D054884:Host-Pathogen Interactions; D007304:Insect Viruses / Q000235:genetics / Q000302:isolation & purification / Q000472:pathogenicity*; D016818:Nosema / Q000235:genetics / Q000302:isolation & purification / Q000472:pathogenicity*; D010802:Phylogeny; D011058:Pollen; D011157:Population Dynamics; D021521:Ribotyping; D013030:Spain; D014351:Trypanosomatina / Q000235:genetics / Q000302:isolation & purification / Q000472:pathogenicity*