Sublethal acetamiprid doses negatively affect the lifespans and foraging behaviors of honey bee (Apis mellifera L.) workers
Graphical abstract
Introduction
Honey bee (Apis mellifera L.) as an important pollinator not only provides nutritious bee products for its efficient foraging capability, but also plays a vital role in agricultural production and in maintaining ecological balance (Klein et al., 2006). However, a large number of scientific investigations have reported the heavy losses of bee colonies across the world (Potts et al., 2010; Santos et al., 2014; Antúnez et al., 2016). A sharp decline of honey bees seriously restricts the development of bee industry and may cause plant pollination crisis (Clermont et al., 2015). In recent years, a variety of factors linked to declined bees, such as parasitic mites, pathogens, pesticides, habitat loss, poor nutrition and magnetic field (Naug, 2009; Ferrari, 2014; Goulson et al., 2015; Sánchez-Bayo et al., 2016; Abbo et al., 2016; Steinhauer et al., 2018), have been studied to determine causes of colony losses. Moreover, interactions between various factors may generate synergies on honey bee populations (Goulson et al., 2015; Chambers et al., 2019).
To date, although exact causes of bee declines is complex and incomprehensible, the widespread use of pesticides is widely considered to be a major factor (Sánchez-Bayo et al., 2016). Pesticides have been applied broadly in agriculture for pest control, and bees are susceptible to be poisoned (Thompson et al., 2010). Previous studies found that bees treated with insecticides can impair the lifespan, colony growth, and foraging behavior of honeybees (Thompson et al., 2005; Yang et al., 2008; Tan et al., 2014; Shi et al., 2019a). Remarkably, the acute toxicity of insecticides to honey bees is well identified usually through determining the LD50 or LC50 values under laboratory conditions (Iwasa et al., 2004; Laurino et al., 2011; Jacob et al., 2019a). Nevertheless, bees in many cases are exposed to sublethal doses of insecticides. Numerous studies have reported the potential threats of sublethal insecticides doses to honey bees, such as affecting the development of bee larvae and queen bees (Wang et al., 2017; Wu-Smart and Spivak, 2016), causing metabolic disorders and abnormal foraging behaviors of honey bees (Schneider et al., 2011; Cook, 2019; Stanley et al., 2016). Therefore, it is of greater practical significance to assess the effect of sublethal doses of insecticides on honey bees.
Among the various insecticides, including organophosphates, neonicotinoids, pyrethroids, and carbamates, the neonicotinoids are the most widely used insecticides around the world (Lin et al., 2014). Because compared with other insecticides, neonicotinoids have higher selectivity for insects versus mammals (Tomizawa and Casida, 2004). Neonicotinoids can act on insect nicotinic acetylcholine receptors (nAChRs) and interfere with the conduction of its nervous system, then cause the insect to die for paralysis (Bicker, 1999). Unfortunately, pollinators as the nontarget insects like targets have been chronically suffered from the deleterious effects of neonicotinoids, especially for bee species. Furthermore, bee genomes code significantly deficient detoxifying enzymes compared with other insect genomes (Claudianos et al., 2006; Johnson et al., 2010). Therefore, neonicotinoids at sublethal doses can seriously affect the survival, foraging activity and olfactory memory (Hassani et al., 2008; Schneider et al., 2011; Abdel–Kader et al., 2017; Shi et al., 2019a).
Recently, three highly toxic neonicotinoids were banned since 2013 (Godfray et al., 2014), while acetamiprid is currently the mainly one available neonicotinoid in EU for its low acute toxicity on bees (Iwasa et al., 2004; Yang et al., 2019). However, the chronic sublethal effects of acetamiprid on honey bees should not be ignored since high acetamiprid residue levels in pollen and beeswax have been frequently detected (Mullin et al., 2010; Jabot et al., 2015). Acetamiprid is a primary member of neonicotinoid insecticides with broad-spectrum characteristic and widely used in the tea, vegetables, fruit trees, flowers and other plants for pest control (Zhou et al., 2006). Meanwhile, bees are frequently exposed to pesticide residues by collecting nectar and pollen from flowering plants which are treated with pesticides. Most strikingly, beehives in many cases are placed near blooming crops for improving the collection efficiency and subsequently much honey profit. Therefore, sprayed pesticides will easily enter the beehive with the form of fog. All individuals especially for younger bees in the colony are inevitably contact the pesticides. Sublethal doses of acetamiprid negatively influence the cognition and long-term memory of honey bees (Hassani et al., 2008; Aliouane et al., 2010). Moreover, when acetamiprid residue in queen cells is over 100 μg/kg, it will generate negative effects on queen rearing (Shi et al., 2019b). A recent research found nearly half pesticides in combination with acetamiprid acted synergistic effects on honey bees (Wang et al., 2020). However, there is still data gap for the risk assessment of chronic toxicity about acetamiprid to honey bees (EFSA, 2016), especially for effects of acetamiprid on foraging behavior of honey bees have rarely been previously investigated, though adverse effects of imidacloprid or other neonicotinoid compounds on the foraging behavior of worker honey bees were frequently reported (Yang et al., 2008; Schneider et al., 2011; Tan et al., 2014). For this reason, the present study in detail assessed how sublethal doses of acetamiprid affect the foraging performance of A. mellifera workers, which containing individual bees performed their first foraging flights, rotating day-off status and the number of foraging flights. Furthermore, the lifespan of worker bees exposed to acetamiprid was also examined. The above indicators were achieved with the help of radio frequency identification (RFID) system. RFID system can be used to systematically study the biological characteristics of social bees and dynamically monitor the target bees at the entrance of the hive as bees come and go (He et al., 2013; Henry et al., 2015).
Former studies proposed and used the newly emerged bees for comparative physiological, developmental, and host-pathogen studies (Erban et al., 2016, Erban et al., 2019a). In this study, the lifespan and foraging behavior of newly emerged worker bees from emergence to death were documented with acetamiprid exposure in natural swarm conditions using RFID system. In addition, this is the first study to investigate whether exposed to acetamiprid of worker bees can change the rotating day-off status in the foragers. Honey bees from the same colony exists a rotation day-off system which is similar to humans (Moore et al., 1989; Klein and Seeley, 2011), proper day-off rotation is helpful to improve work efficiency, but excessive day-off rotation is a kind of go-slow phenomenon. Here, we speculate that the foraging behaviors involving first foraging flights, rotating day-off status and the number of foraging flights would be affected by exposure to acetamiprid.
Section snippets
Insects
Experimental honey bee (Apis mellifera L.) colonies were reared at the Honeybee Research Institute, Jiangxi Agricultural University, Nanchang, China (28.46° N, 115.49° E). Selected bee colonies were strong and healthy colonies that were not threatened by parasitic mites or other parasites and had no prior exposure to pesticides. All experimental work was conducted from May to July of 2019.
Radio frequency identification setup
Two empty hives (standard Langstroth hive) were selected to setup the radio frequency identification
Precocious foraging activity of worker bees induced by acetamiprid
The age at onset of foraging in the 2 μg/bee group was significantly lower than those in the 0.5 μg/bee group and 0 μg/bee group (P (0,2) = 0.002); P (0.5, 2) = 0.001), respectively, while there was no significant difference between 1 μg/bee group and 2 μg/bee group (P > 0.05) (Fig. 1, Table 1). Remarkably, the age at onset of foraging showed no significant difference among 0 μg/bee group, 0.5 μg/bee group and 1 μg/bee group (F2,317 = 1.341, df = 2, P > 0.05). Honey bee workers exposed to
Discussion
All experimental data were well documented in swarm conditions using RFID technology, the survival and foraging behavior of honey bee individuals exposed to sublethal acetamiprid doses were monitored throughout their life. As much research verified the high toxicity of the nitro-substituted compounds mainly including imidacloprid, thiamethoxam and clothianidin on honey bees or other bee species, while lower acute toxicity of cyano-substituted neonicotinoids such as acetamiprid (Tome´ et al.,
Conclusions
Exposure to 2 μg/bee acetamiprid significantly affected the first foraging flights, influenced rotating day-off status, reduced average foraging trips, and shortened lifespans of A. mellifera L. worker bees. This work may provide a new perspective into the neonicotinoids that accelerate the colony failure. However, there are several limitations of this study. For instance, the effect of acetamiprid on food collection ability of bees is also worth investigating.
Author contribution statement
In this work, J Shi carried out the laboratory work and wrote the manuscript. X Wu conceived this research and designed experiments. H Yang, L Yu, Y Liu and W Yan contribute to the laboratory work. X Wu, J Shi, C Liao and M Jin performed the experimental analysis and participated in the revisions of this manuscript. All authors read and approved the final manuscript.
CRediT authorship contribution statement
Jingliang Shi: Methodology, Formal analysis, Investigation, Writing - original draft, Visualization. Heyan Yang: Investigation, Methodology. Longtao Yu: Investigation. Chunhua Liao: Methodology, Formal analysis. Yao Liu: Investigation. Mengjie Jin: Investigation. Weiyu Yan: Conceptualization, Resources, Funding acquisition. Xiao Bo Wu: Conceptualization, Methodology, Resources, Funding acquisition, Project administration.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
The authors would like to thank the National Natural Science Foundation of China (31760714), the Outstanding Young Talent Program of Jiangxi Province (20162BCB23029) and the Major Discipline Academic and Technical Leaders Training Program of Jiangxi Province (20194BCJ22007).
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