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On the natural history of neonicotinoids and bees

2014; Wiley; Volume: 28; Issue: 6 Linguagem: Inglês

10.1111/1365-2435.12319

1365-2435

James Cresswell,

Insect and Arachnid Ecology and Behavior

'Everybody knows the burly, good-natured bumblebee. Clothed in her lovely coat of fur, she is the life of the gay garden as well as of the modestly blooming wayside as she eagerly hums from flower to flower.' This is the introductory sentence to Frederick Sladen's The Humble-bee, which was published in 1912 (Sladen, 1912). The first monograph in the English language on the topic, Sladen's book described the life history of Bombus in temperate climates: how a queen emerges in spring from hibernation to initiate a colony; how her brood becomes a foraging force of workers to collect nectar and pollen from flowers; and how reproduction yields males and new queens to renew the annual cycle. Sladen's work was an enchanting foundation for a century of 'pure' ecological research into the behaviour and domestic arrangements of bumblebees giving insights into energetics (Heinrich 1979), cognition (Chittka & Thomson 2001) and kin selection (Bourke & Ratnieks 2001). Under this scrutiny, the bumblebee colony emerged as a complex and highly integrated social unit. Nevertheless, much remains undiscovered about bumblebees, particularly about colony functions. If you want to know how many of a colony's workers forage, how often and successfully, then the published data are sparse, which makes Gill and Raine's finely detailed picture reported in the current issue of Functional Ecology so instructive (Gill & Raine 2014). While Sladen made his observations in the 'favourable and pleasant' conditions of a 'humble-bee house' with colonies installed in glass-topped tables, Gill and Raine pragmatically housed 40 nest boxes in a laboratory and used RFID tags and computers to monitor the bees' foraging activity as they accessed the outside through tubes. Unlike Sladen, an Edwardian gentleman-scientist, the 21st century university ecologists Gill and Raine had an applied bent: they investigated the impact of insecticides. Sladen found bumblebee colonies at will. To discover nests, he recommended walking at the foot of a woodland bank or driving along a roadside in one's trap where 'we shall be rewarded within a few minutes' by the sight of a bee either leaving or entering her nest. But there are fewer wild bumblebees these days (Biesmeijer et al. 2006) and the causes of bumblebee declines are not fully understood. Potential culprits include parasites, disease, loss of habitat (Potts et al. 2010) and the detrimental impact of competition from honeybees (Thomson 2004). Most notoriously, agricultural pesticides are blamed and neonicotinoids are most conspicuous among the insecticides (Forster 2009; Blacquière et al. 2012). Introduced in 1994, the neonicotinoids account for about 30% of global insecticide sales (Nauen & Jeschke 2011), and their residues in the nectar and pollen of widely planted bee-attractive crops such as oilseed rape constitute a major exposure for bumblebees. In insects, they act as unregulated artificial ligands for ligand-gated ion channels of the nicotinic acetylcholine receptors (nAChRs), which disrupts the coordinated activity of the nervous system (Déglisé, Grünewald & Gauthier 2002). It is natural to assume that sublethal neurotoxicity will manifest principally as cognitive dysfunctions in individuals. In the laboratory, this dysfunction can be revealed by impaired associative learning (Decourtye et al. 2004) and in the field by impaired homing (Bortolotti et al. 2003). Gill and Raine's new study begins to unify the field of bumblebee ecotoxicology by indicating how neurotoxic effects of dietary neonicotinoids on individuals could cause the reduced reproduction of colonies in a recent high-profile report (Whitehorn et al. 2012). As an additional novelty, it has tested for a synergistic 'cocktail effect' between a neonicotinoid, imidacloprid, and another widely used insecticide, a pyrethroid, which bees could potentially experience as a mixture by foraging on differently treated crops. The experiment revealed no cocktail effect between the two insecticides, which is probably unsurprising because a synergy would already be exploited commercially were it to exist. The pyrethroid insecticide (delivered in wet matting in the nest box to simulate spray exposure) had almost no detectable impact on foraging activity, but not so the imidacloprid (delivered in the feeder syrup to simulate systemic exposure). Among control colonies, daily foraging involved one or two bees making half a dozen trips of about half an hour each to collect pollen, which was an equal mix of three types. With imidacloprid, eventually more bees foraged but an increasingly small proportion collected pollen, and its composition was dominated by a single type: Dahlia. Seemingly, the neonicotinoid affected not only individual behaviour (diet choice) but also social organisation (the deployment of the foraging force). A companion report of the same experiment (Gill, Ramos-Rodriguez & Raine 2012), showed that colonies exposed to insecticide treatments for a month contained only three quarters of the number of workers in the control group and it is straightforward to conclude that the insecticides 'impaired' foraging. As a natural historian, Sladen would doubtless be amazed by the ingenuity of Gill and Raine's RFID technology and be delighted by the new insights into the activities of bumblebee colonies, although he would be dismayed at the plight of his beloved bees. Today, however, pure curiosity is eclipsed by an explosive issue at the interface of science and policy. In 2013, the European Union controversially prohibited the use of neonicotinoids on bee-attractive crops pending 'relevant scientific developments' (Regulation No. 485/2013, Europa 2014), and whether neonicotinoids actually threaten the sustainability of bumblebees is a vortex of the debate. The interested parties (including pesticide producers and environmentalists) differentially value agricultural utility and environmental protection, which could bias their interpretation of each new scientific result (Maxim & van der Sluijs 2010). Scientists too are not immune; for example, we see the Chief Scientist of the United Kingdom's environmental protection agency (Defra) chiding the editors of Nature for publishing a correlative study (Hallmann et al. 2014) linking neonicotinoids to bird declines (https://ianlboyd.wordpress.com/2014/07/10/more-is-sometimes-less-a-response-to-the-hollman-et-al-paper/). So thorny is the issue that some scientists have explicitly attempted a 'policy-neutral' restatement of the natural science evidence concerning neonicotinoids and bees (Godfray et al. 2014). Gill and Raine discuss their results plainly, but they too have coloured their language. The imidacloprid-treated colonies that they studied altered the intensity of their pollen foraging, but could this have been a strategic response by bees to a reduced demand for protein (Kitaoka & Nieh 2009) because imidacloprid reduced the fecundity of the queen (Laycock & Cresswell 2013)? If so, individual bees returning without pollen were in no sense 'unsuccessful', even though their imidacloprid-treated colony ultimately was. Regulatory agencies will seek definitive answers in large field experiments where many bumblebee colonies will be placed in replicated sites, but a place will remain for careful natural history to understand the inevitably complex outcomes (Thompson et al. 2013) and the causes. Gill and Raine's study reminds us that bumblebees collect a mixture of pollens, perhaps because polylecty balances their dietary needs (Tasei & Aupinel 2008). By creating dilution, this detail may profoundly influence levels of dietary exposure to contaminated pollen in agricultural landscapes with wildflowers or nearby gardens. Scientists still need to understand their study organism, and Sladen's curiosity must be honoured yet.