Impact of Chronic Neonicotinoid Exposure on Honeybee Colony Performance and Queen Supersedure

Abstract

BackgroundHoneybees provide economically and ecologically vital pollination services to crops and wild plants. During the last decade elevated colony losses have been documented in Europe and North America. Despite growing consensus on the involvement of multiple causal factors, the underlying interactions impacting on honeybee health and colony failure are not fully resolved. Parasites and pathogens are among the main candidates, but sublethal exposure to widespread agricultural pesticides may also affect bees.Methodology/Principal FindingsTo investigate effects of sublethal dietary neonicotinoid exposure on honeybee colony performance, a fully crossed experimental design was implemented using 24 colonies, including sister-queens from two different strains, and experimental in-hive pollen feeding with or without environmentally relevant concentrations of thiamethoxam and clothianidin. Honeybee colonies chronically exposed to both neonicotinoids over two brood cycles exhibited decreased performance in the short-term resulting in declining numbers of adult bees (−28%) and brood (−13%), as well as a reduction in honey production (−29%) and pollen collections (−19%), but colonies recovered in the medium-term and overwintered successfully. However, significantly decelerated growth of neonicotinoid-exposed colonies during the following spring was associated with queen failure, revealing previously undocumented long-term impacts of neonicotinoids: queen supersedure was observed for 60% of the neonicotinoid-exposed colonies within a one year period, but not for control colonies. Linked to this, neonicotinoid exposure was significantly associated with a reduced propensity to swarm during the next spring. Both short-term and long-term effects of neonicotinoids on colony performance were significantly influenced by the honeybees’ genetic background.Conclusions/SignificanceSublethal neonicotinoid exposure did not provoke increased winter losses. Yet, significant detrimental short and long-term impacts on colony performance and queen fate suggest that neonicotinoids may contribute to colony weakening in a complex manner. Further, we highlight the importance of the genetic basis of neonicotinoid susceptibility in honeybees which can vary substantially.

Sperm parameters of honeybee drones exposed to imidacloprid

“…The latter indicated a reduced viability of spermatozoa stored in the spermathecae of honeybee queens exposed to IMD. Moreover, recent findings of Sandrock et al (2014b) who reported 60 % queen supersedure in colonies exposed to two neonicotinoids, thiamethoxam, and clothianidin also suggest long-term effects of neonicotinoids on the quality of spermatozoa inside queen reproductive systems.…”

An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 2: impacts on organisms and ecosystems

“…Semi-field studies Sandrock et al (2014b) used a fully crossed experimental design (sister queens, in-hive pollen feeding) to test effects of clothianidin (2 ppb in pollen) and thiamethoxam (5 ppb in pollen) administered during two brood cycles on colony performance and queen supercedure. They found that the number of bees and brood rearing decreased and queen supercedure increased in treated colonies.…”

Conclusion on the peer review of the pesticide risk assessment for bees for the active substance imidacloprid considering all uses other than seed treatments and granules

“…A number of literature papers were provided to EFSA (Aufauvre et al, 2014;Bekele at al., 2015;Betti et al, 2014;Gisder and Genersch, 2015;Goblirsch et al, 2013;Graystock et al, 2014;Khoury et al, 2013;Natsopoulou et al, 2015;Naug, 2014;Perry at al., 2014;Simeunovic et al, 2014;Wolf et al, 2014;Sandrock at al., 2014;Pettis at al., 2012) regarding this issue. Data were also available in the systematic review report (Fryday et al, 2015) indicating the potential for synergistic effects between neonicotinoid pesticide active substances and honeybee disease.…”