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.

1 Pollinating insects provide crucial and economically important ecosystem services to crops and wild plants, but pollinators, particularly bees, are globally declining as a result of various driving factors, including the prevalent use of pesticides for crop protection. Sublethal pesticide exposure negatively impacts numerous pollinator lifehistory traits, but its influence on reproductive success remains largely unknown. Such information is pivotal, however, to our understanding of the long-term effects on population dynamics. 2 We investigated the influence of field-realistic trace residues of the routinely used neonicotinoid insecticides thiamethoxam and clothianidin in nectar substitutes on the entire life-time fitness performance of the red mason bee Osmia bicornis. 3 We show that chronic, dietary neonicotinoid exposure has severe detrimental effects on solitary bee reproductive output. Neonicotinoids did not affect adult bee mortality; however, monitoring of fully controlled experimental populations revealed that sublethal exposure resulted in almost 50% reduced total offspring production and a significantly male-biased offspring sex ratio. 4 Our data add to the accumulating evidence indicating that sublethal neonicotinoid effects on non-Apis pollinators are expressed most strongly in a rather complex, fitness-related context. Consequently, to fully mitigate long-term impacts on pollinator population dynamics, present pesticide risk assessments need to be expanded to include whole life-cycle fitness estimates, as demonstrated in the present study using O. bicornis as a model.

Monitoring is an integral part of species conservation. Monitoring programs must take imperfect detection of species into account in order to be reliable. Theory suggests that detection probability may be determined by population size but this relationship has not yet been assessed empirically. Population size is particularly important because it may induce heterogeneity in detection probability and thereby cause bias in estimates of biodiversity. We used a site occupancy model to analyse data from a volunteer-based amphibian monitoring program to assess how well different variables explain variation in detection probability. An index to population size best explained detection probabilities for four out of six species (to avoid circular reasoning, we used the count of individuals at a previous site visit as an index to current population size). The relationship between the population index and detection probability was positive. Commonly used weather variables best explained detection probabilities for two out of six species. Estimates of site occupancy probabilities differed depending on whether the population index was or was not used to model detection probability. The relationship between the population index and detectability has implications for the design of monitoring and species conservation. Most importantly, because many small populations are likely to be overlooked, monitoring programs should be designed in such a way that small populations are not overlooked. The results also imply that methods cannot be standardized in such a way that detection probabilities are constant. As we have shown here, one can easily account for variation in population size in the analysis of data from long-term monitoring programs by using counts of individuals from surveys at the same site in previous years. Accounting for variation in population size is important because it can affect the results of long-term monitoring programs and ultimately the conservation of imperiled species.