Death of the bee hive: understanding the failure of an insect society.

Since 2007 honey bee colony failure rates overwinter have averaged about 30% across much of North America. In addition, cases of extremely rapid colony failure have been reported, which has been termed colony collapse disorder. Both phenomena result from an increase in the frequency and intensity of chronic diseases and environmental stressors. Colonies are often challenged by multiple stressors, which can interact: for example, pesticides can enhance disease transmission in colonies. Colonies may be particularly vulnerable to sublethal effects of pathogens and pesticides since colony functions are compromised whether a stressor kills workers, or causes them to fail at foraging. Modelling provides a way to understand the processes of colony failure by relating impacts of stressors to colony-level functions.

[1]  M. Winston,et al.  The influence of wax deprivation on temporal polyethism in honey bee (Apis mellifera L.) colonies , 1988 .

[2]  Andrew B. Barron,et al.  Assessment of flight activity and homing ability in Asian and European honey bee species, Apis cerana and Apis mellifera, measured with radio frequency tags , 2012, Apidologie.

[3]  S. Soubeyrand,et al.  Flight behavior and pheromone changes associated to Nosema ceranae infection of honey bee workers (Apis mellifera) in field conditions. , 2013, Journal of invertebrate pathology.

[4]  M. Winston,et al.  The influence of pollen storage area and Varroa jacobsoni Oudemans parasitism on temporal caste structure in honey bees (Apis mellifera L.) , 2000, Insectes Sociaux.

[5]  G. Robinson,et al.  Effects of colony food shortage on behavioral development in honey bees , 1998, Behavioral Ecology and Sociobiology.

[6]  Dennis vanEngelsdorp,et al.  Idiopathic brood disease syndrome and queen events as precursors of colony mortality in migratory beekeeping operations in the eastern United States. , 2013, Preventive veterinary medicine.

[7]  S. Williamson,et al.  Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees , 2013, Journal of Experimental Biology.

[8]  Jay D. Evans,et al.  Israeli Acute Paralysis Virus: Epidemiology, Pathogenesis and Implications for Honey Bee Health , 2014, PLoS pathogens.

[9]  S. Su,et al.  Viral Infection Affects Sucrose Responsiveness and Homing Ability of Forager Honey Bees, Apis mellifera L. , 2013, PloS one.

[10]  Richard J. Gill,et al.  Combined pesticide exposure severely affects individual- and colony-level traits in bees , 2012, Nature.

[11]  J. Adamczyk,et al.  Monitoring for Resistance to Organophosphorus and Pyrethroid Insecticides in Varroa Mite Populations , 2010, Journal of economic entomology.

[12]  Worker-worker inhibition of honey bee behavioural development independent of queen and brood , 2004, Insectes Sociaux.

[13]  J. Tautz,et al.  Automatic life-long monitoring of individual insect behaviour now possible. , 2003, Zoology.

[14]  Geraldine A. Wright,et al.  Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees , 2013, Nature Communications.

[15]  Lars Chittka,et al.  Colony nutritional status modulates worker responses to foraging recruitment pheromone in the bumblebee Bombus terrestris , 2008, Behavioral Ecology and Sociobiology.

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

[17]  Andrew B. Barron,et al.  Modelling Food and Population Dynamics in Honey Bee Colonies , 2013, PloS one.

[18]  C. Lu,et al.  Sub-lethal exposure to neonicotinoids impaired honey bees winterization before proceeding to colony collapse disorder , 2014 .

[19]  C. Grozinger,et al.  Chronic parasitization by Nosema microsporidia causes global expression changes in core nutritional, metabolic and behavioral pathways in honey bee workers (Apis mellifera) , 2013, BMC Genomics.

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

[21]  J. Frazier,et al.  Genomic analysis of the interaction between pesticide exposure and nutrition in honey bees (Apis mellifera). , 2014, Journal of insect physiology.

[22]  Thomas D. Seeley,et al.  Adaptive significance of the age polyethism schedule in honeybee colonies , 1982, Behavioral Ecology and Sociobiology.

[23]  C. Menzie,et al.  A Causal Analysis of Observed Declines in Managed Honey Bees (Apis mellifera) , 2013, Human and ecological risk assessment : HERA.

[24]  W. Meikle,et al.  Application of continuous monitoring of honeybee colonies , 2014, Apidologie.

[25]  Z. Huang,et al.  Physiological and Behavioral Changes in Honey Bees (Apis mellifera) Induced by Nosema ceranae Infection , 2013, PloS one.

[26]  F. Nazzi,et al.  Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees , 2013, Proceedings of the National Academy of Sciences.

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

[28]  D. vanEngelsdorp,et al.  A survey of honey bee colony losses in the United States, fall 2008 to spring 2009 , 2010 .

[29]  Peter Neumann,et al.  Colony Collapse Disorder in context , 2010, BioEssays : news and reviews in molecular, cellular and developmental biology.

[30]  James T. Wilkes,et al.  A national survey of managed honey bee 2011–12 winter colony losses in the United States: results from the Bee Informed Partnership , 2013 .

[31]  M. Woyciechowski,et al.  Life expectancy and onset of foraging in the honeybee (Apis mellifera) , 2009, Insectes Sociaux.

[32]  P. J. Kennedy,et al.  BEEHAVE: a systems model of honeybee colony dynamics and foraging to explore multifactorial causes of colony failure , 2014, The Journal of applied ecology.

[33]  J. Pettis,et al.  Assessment of Chronic Sublethal Effects of Imidacloprid on Honey Bee Colony Health , 2015, PloS one.

[34]  G. Robinson,et al.  Social inhibition and the regulation of temporal polyethism in honey bees. , 2001, Journal of theoretical biology.

[35]  Jay D. Evans,et al.  Colony Collapse Disorder: A Descriptive Study , 2009, PloS one.

[36]  Geoffrey R. Williams,et al.  Infra-Population and -Community Dynamics of the Parasites Nosema apis and Nosema ceranae, and Consequences for Honey Bee (Apis mellifera) Hosts , 2014, PloS one.

[37]  Clint J. Perry,et al.  Rapid behavioral maturation accelerates failure of stressed honey bee colonies , 2015, Proceedings of the National Academy of Sciences.

[38]  J. Tautz,et al.  RFID Tracking of Sublethal Effects of Two Neonicotinoid Insecticides on the Foraging Behavior of Apis mellifera , 2012, PloS one.

[39]  Axel Decourtye,et al.  The sublethal effects of pesticides on beneficial arthropods. , 2007, Annual review of entomology.

[40]  Andrew B. Barron,et al.  Dynamic modelling of honey bee (Apis mellifera) colony growth and failure , 2013 .

[41]  A. Barron,et al.  A Quantitative Model of Honey Bee Colony Population Dynamics , 2011, PloS one.

[42]  Peter Neumann,et al.  Predictive Markers of Honey Bee Colony Collapse , 2012, PloS one.

[43]  Mickaël Henry,et al.  A Common Pesticide Decreases Foraging Success and Survival in Honey Bees , 2012, Science.

[44]  T. Schmickl,et al.  Cannibalism and early capping: strategy of honeybee colonies in times of experimental pollen shortages , 2001, Journal of Comparative Physiology A.

[45]  J. Fewell,et al.  Models of division of labor in social insects. , 2001, Annual review of entomology.

[46]  Gene E. Robinson,et al.  Regulation of honey bee age polyethism by juvenile hormone , 1987, Behavioral Ecology and Sociobiology.

[47]  L. Wahl,et al.  Effects of Infection on Honey Bee Population Dynamics: A Model , 2014, PloS one.

[48]  Gene E. Robinson,et al.  Worker nutrition and division of labour in honeybees , 2005, Animal Behaviour.

[49]  J. Osborne,et al.  So Near and Yet So Far: Harmonic Radar Reveals Reduced Homing Ability of Nosema Infected Honeybees , 2014, PloS one.

[50]  Takashi Matsumoto,et al.  Reduction in homing flights in the honey bee Apis mellifera after a sublethal dose of neonicotinoid insecticides , 2013 .

[51]  C. Pirk,et al.  Nutrition affects survival in African honeybees exposed to interacting stressors , 2014 .

[52]  Elinor M. Lichtenberg,et al.  Crop Pollination Exposes Honey Bees to Pesticides Which Alters Their Susceptibility to the Gut Pathogen Nosema ceranae , 2013, PloS one.

[53]  Francis L. W. Ratnieks,et al.  Clarity on Honey Bee Collapse? , 2010, Science.

[54]  Gene E Robinson,et al.  Regulation of behavioral maturation by a primer pheromone produced by adult worker honey bees. , 2004, Proceedings of the National Academy of Sciences of the United States of America.