Impact of chronic neonicotinoid exposure on honeybee colony performance and queen supersedure

Abstract

Background: Honeybees 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 findings: To 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/significance: Sublethal 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.

Figure 1. Dynamics of honeybee colony performance.

Data of all three endpoints number of adult bees (A), eggs and larvae (B) and pupae (C) for the different pollen feeding treatments (black  =  control; red  =  neonicotinoids) and honeybee strains (circles  =  strain A; crosses  =  strain B). The data were obtained at four successive colony assessment dates (X-axis subpanels within figures) performed before (Spring 2011) and directly after the 1.5 months of experimental pollen feeding (Summer 2011), 3.5 months after the treatment (Autumn 2011) and one year later (Spring 2012). Estimated numbers on the Y-axes are truncated for adult bees and pupae for better overview.

Figure 2. Pollen collections.

Mean (±SD) fresh weights of pollen collections for control (black) and neonicotinoid-exposed (white) colonies over the course of the treatment period (pollen-trap contents were weighed in 2-2–3 days intervals throughout the study).