Occurrence of parasites and pathogens in honey bee colonies used in a European genotype-environment interactions experiment

Summary Diseases are known to be one of the major contributors to colony losses. Within a Europe-wide experiment on genotype—environment interactions, an initial 621 colonies were set up and maintained from 2009 to 2012. The colonies were monitored to investigate the occurrence and levels of key pathogens. These included the mite Varroa destructor (mites per 10 g bees), Nosema spp. (spore loads and species determination), and viruses (presence/absence of acute bee paralysis virus (ABPV) and deformed wing virus (DWV)). Data from 2010 to the spring of 2011 are analysed in relation to the parameters: genotype, environment, and origin (local vs. non-local) of the colonies in the experiment. The relative importance of different pathogens as indicators of colony death within the experiment is compared. In addition, pathogen occurrence rates across the geographic locations are described.

[1]  Louise Taylor,et al.  OIE Terrestrial Manual , 2014 .

[2]  P. Kryger,et al.  A selective sweep in a microsporidian parasite Nosema-tolerant honeybee population, Apis mellifera. , 2014, Animal genetics.

[3]  P. Kryger,et al.  The influence of genetic origin and its interaction with environmental effects on the survival of Apis mellifera L. colonies in Europe , 2014 .

[4]  P. Kryger,et al.  The genetic origin of honey bee colonies used in the COLOSS Genotype-Environment Interactions Experiment: a comparison of methods , 2014 .

[5]  P. Kryger,et al.  Swarming, defensive and hygienic behaviour in honey bee colonies of different genetic origin in a pan-European experiment , 2014 .

[6]  P. Kryger,et al.  Effect of genotype and environment on parasite and pathogen levels in one apiary—a case study , 2014 .

[7]  M. Lodesani,et al.  Impact of control strategies for Varroa destructor on colony survival and health in northern and central regions of Italy , 2014 .

[8]  P. Kryger,et al.  Population dynamics of European honey bee genotypes under different environmental conditions , 2014 .

[9]  P. Hendrikx,et al.  Demographics of the European Apicultural Industry , 2013, PloS one.

[10]  T. Wenseleers,et al.  Comprehensive Bee Pathogen Screening in Belgium Reveals Crithidia mellificae as a New Contributory Factor to Winter Mortality , 2013, PloS one.

[11]  E. Genersch,et al.  Molecular differentiation of Nosema apis and Nosema ceranae based on species-specific sequence differences in a protein coding gene. , 2013, Journal of invertebrate pathology.

[12]  P. Kryger,et al.  Varroa-Virus Interaction in Collapsing Honey Bee Colonies , 2013, PloS one.

[13]  D. vanEngelsdorp,et al.  Population-genomic variation within RNA viruses of the Western honey bee, Apis mellifera, inferred from deep sequencing , 2013, BMC Genomics.

[14]  P. Kryger,et al.  Patterns of viral infection in honey bee queens , 2013, The Journal of general virology.

[15]  I. Fries,et al.  Temporal study of Nosema spp. in a cold climate. , 2013, Environmental microbiology reports.

[16]  Geoffrey R. Williams,et al.  Standard methods for Nosema research , 2013 .

[17]  J. V. D. van der Steen,et al.  Standard methods for virus research in Apis mellifera , 2013 .

[18]  P. Neumann,et al.  The COLOSS BEEBOOK Volume II, Standard methods for Apis mellifera pest and pathogen research: Introduction , 2013 .

[19]  James D. Ellis,et al.  Standard methods for varroa research , 2013 .

[20]  M. Higes,et al.  Low prevalence of honeybee viruses in Spain during 2006 and 2007. , 2012, Research in veterinary science.

[21]  F. Puerta,et al.  Asymptomatic presence of Nosema spp. in Spanish commercial apiaries. , 2012, Journal of invertebrate pathology.

[22]  D. vanEngelsdorp,et al.  Pathogen Webs in Collapsing Honey Bee Colonies , 2012, PloS one.

[23]  P. Kryger,et al.  A Europe-Wide Experiment for Assessing the Impact of Genotype-Environment Interactions on the Vitality and Performance of Honey Bee Colonies: Experimental Design and Trait Evaluation , 2012 .

[24]  Sam P. Brown,et al.  Synergistic Parasite-Pathogen Interactions Mediated by Host Immunity Can Drive the Collapse of Honeybee Colonies , 2012, PLoS pathogens.

[25]  P. Kryger,et al.  Single Assay Detection of Acute Bee Paralysis Virus, Kashmir Bee Virus and Israeli Acute Paralysis Virus , 2012 .

[26]  P. Neumann,et al.  Dead or Alive: Deformed Wing Virus and Varroa destructor Reduce the Life Span of Winter Honeybees , 2011, Applied and Environmental Microbiology.

[27]  R. Büchler,et al.  Breeding for resistance to Varroa destructor in Europe , 2010, Apidologie.

[28]  W. Ritter,et al.  Varroa mites and honey bee health: can Varroa explain part of the colony losses? , 2010, Apidologie.

[29]  T. Rinderer,et al.  Breeding for resistance to Varroa destructor in North America , 2010, Apidologie.

[30]  E. Genersch,et al.  The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies , 2010, Apidologie.

[31]  E. Genersch,et al.  Emerging and re-emerging viruses of the honey bee (Apis mellifera L.) , 2010, Veterinary research.

[32]  E. Genersch,et al.  Five-Year Cohort Study of Nosema spp. in Germany: Does Climate Shape Virulence and Assertiveness of Nosema ceranae? , 2010, Applied and Environmental Microbiology.

[33]  A. Imdorf,et al.  Virus infections and winter losses of honey bee colonies (Apis mellifera) , 2010 .

[34]  S. Martin,et al.  Honey bee colony collapse and changes in viral prevalence associated with Varroa destructor , 2010 .

[35]  R. Paxton.  Does infection by Nosema ceranae cause “Colony Collapse Disorder” in honey bees (Apis mellifera)? , 2010 .

[36]  N. Carreck,et al.  Honey bee colony losses , 2010 .

[37]  P. Kryger,et al.  Factors involved in the recent increase in colony losses in Denmark , 2010 .

[38]  D. Schroeder,et al.  Deformed Wing Virus Implicated in Overwintering Honeybee Colony Losses , 2009, Applied and Environmental Microbiology.

[39]  A. B. Jensen,et al.  Differential susceptibility across honey bee colonies in larval chalkbrood resistance , 2009, Apidologie.

[40]  P. García-Palencia,et al.  Honeybee colony collapse due to Nosema ceranae in professional apiaries. , 2009, Environmental microbiology reports.

[41]  Jeffrey W. Harris.  Effect of Brood Type on Varroa-Sensitive Hygiene by Worker Honey Bees (Hymenoptera: Apidae) , 2008 .

[42]  J. Jiménez,et al.  How natural infection by Nosema ceranae causes honeybee colony collapse. , 2008, Environmental microbiology.

[43]  R. Currie,et al.  The ability of high- and low-grooming lines of honey bees to remove the parasitic mite Varroa destructor is affected by environmental conditions , 2008 .

[44]  E. Genersch,et al.  Varroosis – the Ongoing Crisis in Bee Keeping , 2008, Journal für Verbraucherschutz und Lebensmittelsicherheit.

[45]  J. Rousselle,et al.  Honey bee colonies that have survived Varroa destructor , 2007, Apidologie.

[46]  Jay D. Evans,et al.  A Metagenomic Survey of Microbes in Honey Bee Colony Collapse Disorder , 2007, Science.

[47]  M. Bergoin,et al.  Viral load estimation in asymptomatic honey bee colonies using the quantitative RT-PCR technique , 2007, Apidologie.

[48]  I. Fries,et al.  Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. , 2007, Journal of invertebrate pathology.

[49]  J. Todd,et al.  Incidence and molecular characterization of viruses found in dying New Zealand honey bee (Apis mellifera) colonies infested with Varroa destructor , 2007, Apidologie.

[50]  I. Fries,et al.  Infection of drone larvae (Apis mellifera) with American foulbrood , 2007, Apidologie.

[51]  D. Cox-Foster,et al.  Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge , 2006, Parasitology.

[52]  I. Fries,et al.  Survival of mite infested (Varroa destructor) honey bee (Apis mellifera) colonies in a Nordic climate , 2006 .

[53]  S. Fuchs,et al.  Parasitic Varroa destructor mites influence flight duration and homing ability of infested Apis mellifera foragers , 2006 .

[54]  E. Genersch,et al.  Detection of viral sequences in semen of honeybees (Apis mellifera): evidence for vertical transmission of viruses through drones. , 2006, Journal of invertebrate pathology.

[55]  Raquel Martín,et al.  Nosema ceranae, a new microsporidian parasite in honeybees in Europe. , 2006, Journal of invertebrate pathology.

[56]  R. Currie,et al.  Timing acaricide treatments to prevent Varroa destructor (Acari: Varroidae) from causing economic damage to honey bee colonies , 2006, The Canadian Entomologist.

[57]  Y. P. Chen,et al.  Prevalence and Transmission of Honeybee Viruses , 2006, Applied and Environmental Microbiology.

[58]  E. Genersch,et al.  RT-PCR analysis of Deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor). , 2005, The Journal of general virology.

[59]  L. Cui,et al.  Intricate transmission routes and interactions between picorna-like viruses (Kashmir bee virus and sacbrood virus) with the honeybee host and the parasitic varroa mite. , 2005, The Journal of general virology.

[60]  Xiaolong Yang,et al.  Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[61]  S. Fuchs,et al.  Distribution of Varroa destructor between swarms and colonies , 2005 .

[62]  Jeffrey W. Harris,et al.  Suppressed mite reproduction explained by the behaviour of adult bees , 2005 .

[63]  J. Ellis,et al.  The worldwide health status of honey bees , 2005 .

[64]  M. Bergoin,et al.  Prevalence and Seasonal Variations of Six Bee Viruses in Apis mellifera L. and Varroa destructor Mite Populations in France , 2004, Applied and Environmental Microbiology.

[65]  Yan Zhao,et al.  Multiple virus infections in the honey bee and genome divergence of honey bee viruses. , 2004, Journal of invertebrate pathology.

[66]  G. Amdam,et al.  Altered Physiology in Worker Honey Bees (Hymenoptera: Apidae) Infested with the Mite Varroa destructor (Acari: Varroidae): A Factor in Colony Loss During Overwintering? , 2004, Journal of economic entomology.

[67]  I. Fries,et al.  Swarming in honey bees (Apis mellifera) and Varroa destructor population development in Sweden. , 2003 .

[68]  Pedro Duay,et al.  Decreased flight performance and sperm production in drones of the honey bee (Apis mellifera) slightly infested by Varroa destructor mites during pupal development. , 2002, Genetics and molecular research : GMR.

[69]  J. Strange,et al.  Optimum Timing of Miticide Applications for Control of Varroa destructor (Acari: Varroidae) in Apis mellifera (Hymenoptera: Apidae) in Washington State, USA , 2001, Journal of economic entomology.

[70]  S. Martin.  The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach , 2001 .

[71]  B. Oldroyd,et al.  Coevolution while you wait: Varroa jacobsoni, a new parasite of western honeybees. , 1999, Trends in ecology & evolution.

[72]  R. E. Page,et al.  Effect of Varroa jacobsoni (Mesostigmata: Varroidae) on Feral Apis mellifera (Hymenoptera: Apidae) in California , 1995 .

[73]  A. Alippi,et al.  The mite Varroa jacobsoni does not transmit American foulbrood from infected to healthy colonies , 1995, Experimental & Applied Acarology.

[74]  B. Ball,et al.  The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni , 1988 .

[75]  J. Perry,et al.  Association of viruses with two protozoal pathogens of the honey bee , 1983 .

[76]  Per Kragh Andersen,et al.  Testing Goodness of Fit of Cox's Regression and Life Model , 1982 .

[77]  L. Bailey.  Honey Bee Pathology , 1981 .

[78]  L. Bailey,et al.  Two More Small RNA Viruses from Honey Bees and Further Observations on Sacbrood and Acute Bee-Paralysis Viruses , 1977 .

[79]  O. W. Park.  Testing for Resistance to American Foulbrood in Honeybees , 1937 .

[80]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[81]  R. Sokół,et al.  Nosemosis in honey bees , 2014 .

[82]  D. Engelsdorp,et al.  Colony collapse disorder. , 2014 .

[83]  K. M. Cobb,et al.  Global Honey Bee Viral Landscape Altered by a Parasitic Mite , 2012 .

[84]  T. Seeley.  Honey bees of the Arnot Forest: a population of feral colonies persisting with Varroa destructor in the northeastern United States , 2011, Apidologie.

[85]  G. Budge,et al.  The Acute bee paralysis virus-Kashmir bee virus-Israeli acute paralysis virus complex. , 2010, Journal of invertebrate pathology.

[86]  P. Rosenkranz,et al.  Biology and control of Varroa destructor. , 2010, Journal of invertebrate pathology.

[87]  E. Genersch,et al.  Deformed wing virus. , 2010, Journal of invertebrate pathology.

[88]  M. Hagensee,et al.  Development and Validation of a HPV-32 Specific PCR Assay , 2009, Virology Journal.

[89]  A. Gajda,et al.  The investigation of bee virus infections in Poland. , 2009 .

[90]  J. Fazakerley.  Emerging and re-emerging viruses , 2009 .

[91]  D. Sumpter,et al.  The dynamics of virus epidemics in Varroa -infested honey bee colonies , 2004 .

[92]  S. Nordström.  Distribution of deformed wing virus within honey bee (Apis mellifera) brood cells infested with the ectoparasitic mite Varroa destructor , 2004, Experimental & Applied Acarology.

[93]  K. Bienefeld,et al.  Survival test without treatment against varroatosis: the island project in Croatia , 2002 .

[94]  Gunn,et al.  The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite varroa jacobsoni Oud , 1999, Journal of invertebrate pathology.

[95]  S.,et al.  Economic threshold for Varroa jacobsoni Oud. in the southeastern USA , 1999 .

[96]  I. Fries,et al.  Virus infections in Nordic honey bee colonies with no, low or severe Varroa jacobsoni infestations , 1999 .

[97]  L. Bailey,et al.  2 – THE HONEY BEE , 1991 .

[98]  R. Cavalloro.  Present status of varroatosis in Europe and progress in the varroa mite control. Proceedings of a meeting of the EC-Experts' Group, Udine, Italy, 28 to 30 November, 1988. , 1989 .

[99]  I. Fries.  INFECTIVITY AND MULTIPLICATION OF NOSEMA APIS Z. IN THE VENTRICULUS OF THE HONEY BEE , 1988 .

[100]  P. Schneider,et al.  EINFLUSS DER PARASITIERUNG DURCH DIE MILBE VARROA JACOBSONI OUD. AUF DAS SCHLUPFGEWICHT, DIE GEWICHTSENTWICKLUNG, DIE ENTWICKLUNG DER HYPOPHARYNXDRÜSEN UND DIE LEBENSDAUER VON APIS MELLIFERA L. , 1987 .

[101]  R. Campbell,et al.  In a Cold Climate , 1984 .

[102]  B. Ball.  association of Varroa jacobsoni with virus diseases of honey bees , 1983 .

[103]  R. Morse,et al.  Mite Pests of Honey Bees , 1982 .

[104]  D. Cox.  Regression Models and Life-Tables , 1972 .

[105]  D.,et al.  Regression Models and Life-Tables , 2022 .