Predicting Honeybee Colony Failure: Using the BEEHAVE Model to Simulate Colony Responses to Pesticides

To simulate effects of pesticides on different honeybee (Apis mellifera L.) life stages, we used the BEEHAVE model to explore how increased mortalities of larvae, in-hive workers, and foragers, as well as reduced egg-laying rate, could impact colony dynamics over multiple years. Stresses were applied for 30 days, both as multiples of the modeled control mortality and as set percentage daily mortalities to assess the sensitivity of the modeled colony both to small fluctuations in mortality and periods of low to very high daily mortality. These stresses simulate stylized exposure of the different life stages to nectar and pollen contaminated with pesticide for 30 days. Increasing adult bee mortality had a much greater impact on colony survival than mortality of bee larvae or reduction in egg laying rate. Importantly, the seasonal timing of the imposed mortality affected the magnitude of the impact at colony level. In line with the LD50, we propose a new index of “lethal imposed stress”: the LIS50 which indicates the level of stress on individuals that results in 50% colony mortality. This (or any LISx) is a comparative index for exploring the effects of different stressors at colony level in model simulations. While colony failure is not an acceptable protection goal, this index could be used to inform the setting of future regulatory protection goals.

[1]  John William Trevan,et al.  The Error of Determination of Toxicity. , 1927 .

[2]  G. DeGrandi-Hoffman,et al.  PC BEEPOP, an ecotoxicological simulation model for honey bee populations , 1991 .

[3]  G. Robinson,et al.  Regulation of honey bee division of labor by colony age demography , 1996, Behavioral Ecology and Sociobiology.

[4]  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.

[5]  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.

[6]  J. Ambrose,et al.  Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellife , 2004 .

[7]  Steven F. Railsback,et al.  Individual-based modeling and ecology , 2005 .

[8]  C. Scott-dupree,et al.  Contact and oral toxicity to honey bees (Apis mellifera) of agents registered for use for sweet corn insect control in Ontario, Canada , 2005 .

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

[10]  T. Schmickl,et al.  HoPoMo : A model of honeybee intracolonial population dynamics and resource management , 2007 .

[11]  D. Naug Nutritional stress due to habitat loss may explain recent honeybee colony collapses. , 2009 .

[12]  Q. Wang,et al.  Effects of sublethal concentrations of bifenthrin and deltamethrin on fecundity, growth, and development of the honeybee Apis mellifera ligustica , 2010, Environmental toxicology and chemistry.

[13]  J. Devillers,et al.  Ecotoxicity of neonicotinoid insecticides to bees. , 2010, Advances in experimental medicine and biology.

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

[15]  D. vanEngelsdorp,et al.  A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. , 2010, Journal of invertebrate pathology.

[16]  J. Cresswell A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees , 2011, Ecotoxicology.

[17]  Jay D. Evans,et al.  Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. , 2011, The Journal of general virology.

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

[19]  F. Nazzi,et al.  How does the mite Varroa destructor kill the honeybee Apis mellifera? Alteration of cuticular hydrcarbons and water loss in infested honeybees. , 2012, Journal of insect physiology.

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

[21]  J. Nieh,et al.  A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing , 2012, Journal of Experimental Biology.

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

[23]  S. Wilkins,et al.  Effects of solvent on the toxicity of dimethoate in a honey bee in vitro larval study. , 2013, Pest management science.

[24]  Richard J. Gill,et al.  Chronic sublethal stress causes bee colony failure , 2013, Ecology letters.

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

[26]  R. Menzel,et al.  Effect of Flumethrin on Survival and Olfactory Learning in Honeybees , 2013, PloS one.

[27]  J. Boesten,et al.  EFSA Guidance Document on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees) , 2013 .

[28]  P. Campbell,et al.  A Four-Year Field Program Investigating Long-Term Effects of Repeated Exposure of Honey Bee Colonies to Flowering Crops Treated with Thiamethoxam , 2013, PloS one.

[29]  Pernille Thorbek,et al.  REVIEW: Towards a systems approach for understanding honeybee decline: a stocktaking and synthesis of existing models , 2013, The Journal of applied ecology.

[30]  G. C. Cutler,et al.  Distributed under Creative Commons Cc-by 4.0 a Large-scale Field Study Examining Effects of Exposure to Clothianidin Seed-treated Canola on Honey Bee Colony Health, Development, and Overwintering Success , 2022 .

[31]  S. Potts,et al.  Impact of Chronic Neonicotinoid Exposure on Honeybee Colony Performance and Queen Supersedure , 2014, PloS one.

[32]  F. Ratnieks,et al.  The dose makes the poison: have “field realistic” rates of exposure of bees to neonicotinoid insecticides been overestimated in laboratory studies? , 2014 .

[33]  Angela R. McLean,et al.  A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators , 2014, Proceedings of the Royal Society B: Biological Sciences.

[34]  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.

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

[36]  Reed M. Johnson Honey bee toxicology. , 2015, Annual review of entomology.

[37]  I. Fries,et al.  Seed coating with a neonicotinoid insecticide negatively affects wild bees , 2015, Nature.

[38]  Colin Ockleford,et al.  Statement on the suitability of the BEEHAVE model for its potential use in a regulatory context and for the risk assessment of multiple stressors in honeybees at the landscape level , 2015 .

[39]  J. Pettis,et al.  Correction: Assessment of Chronic Sublethal Effects of Imidacloprid on Honey Bee Colony Health , 2017, PloS one.