Toxins induce ‘malaise’ behaviour in the honeybee (Apis mellifera)

Abstract

To avoid poisoning and death when toxins are ingested, the body responds with a suite of physiological detoxification mechanisms accompanied by behaviours that in mammals often include vomiting, nausea, and lethargy. Few studies have characterised whether insects exhibit characteristic ‘malaise-like’ behaviours in response to intoxication. Here, we used the honeybee to investigate how intoxication produced by injection or ingestion with three toxins with different pharmacological modes of action quinine, amygdalin, and lithium chloride affected behaviour. We found that toxin-induced changes in behaviour were best characterised by more time spent grooming. Bees also had difficulty performing the righting reflex and exhibited specific toxin-induced behaviours such as abdomen dragging and curling up. The expression of these behaviours also depended on whether a toxin had been injected or ingested. When toxins were ingested, they were least 10 times less concentrated in the haemolymph than in the ingested food, suggesting that their absorption through the gut is strongly regulated. Our data show that bees exhibit changes in behaviour that are characteristic of ‘malaise’ and suggest that physiological signalling of toxicosis is accomplished by multiple post-ingestive pathways in animals.Electronic supplementary materialThe online version of this article (doi:10.1007/s00359-014-0932-0) contains supplementary material, which is available to authorized users.

Bumble bee parasite strains vary in resistance to phytochemicals

“…Bumble bees are generalist pollinators that consume nectar and pollen from a wide range of plant species11. Both nectar51 and pollen14 contain diverse compound mixtures, to which C. bombi in the gut lumen would be directly exposed52, particularly in the proximal parts of the gut, before phytochemicals are absorbed or metabolized by hosts or commensalists. Study of the mechanisms by which C. bombi withstands such high phytochemical concentrations could offer insight into the evolution of chemical resistance in medically important trypanosomes.…”

“…Thymol is used prophylactically to combat Varroa mite infestations65, and inhibited Nosema infection in A. mellifera 19 and Crithidia infection in B. impatiens 22. Although it is possible that nectar thymol is absorbed or metabolized by bees or their gut commensalists, or diluted through combination with nectar of other species, phytochemicals are detectable in the lumen post-ingestion52, and even very low nectar concentrations (0.2 ppm) can reduce C. bombi infection intensity in B. impatiens 22. Because individual bumble bees generally forage from only one or several floral species66, consumption of medicinally relevant amounts of thymol would seem plausible in the wild.…”

A Novel Behavioral Assay to Investigate Gustatory Responses of Individual, Freely-moving Bumble Bees (<em>Bombus terrestris</em>)

“…Together, these results suggest that quinine is perceived by the gustatory receptor cells on the mouthparts of the bumble bee, as already previously identified in the honey bee 9 . Quinine is a toxin for insects that induces malaise-like behavior in the honey bee 10 and knockdown in the malaria mosquito (Anopheles gambiae) 23 . This assay could well lead to the identification of some deterrent and potentially toxic compounds that are perceived by the taste receptor cells on the mouthparts in the bumble bees.…”

“…This assay of food consumption described by Tiedeken et al 7 revealed that bees can detect bitter compounds in solutions. However, this assay was unable to distinguish taste from post-ingestive processes such as malaise that could also affect feeding behavior over this time interval [8][9][10] .…”

Spontaneous honeybee behaviour is altered by persistent organic pollutants

“…Factor analysis was performed on the frequency data using the principal components method of factor extraction with a Varimax rotation (Hurst et al 2014). The generated factor scores were analysed using a multivariate analysis of variance (MANOVA) with Factor as the variable and chemical and day of exposure as fixed factors, with post hoc comparisons.…”