A matter of taste: the adverse effect of pollen compounds on the pre-ingestive gustatory experience of sugar solutions for honeybees

Abstract

In addition to sugars, nectar contains multiple nutrient compounds in varying concentrations, yet little is known of their effect on the reward properties of nectar and the resulting implications for insect behaviour. We examined the pre-ingestive responses of honeybees to sucrose solutions containing a mix of pollen compounds, the amino acids proline or phenylalanine, or known distasteful substances, quinine and salt. We predicted that in taste and learning assays, bees would respond positively to the presence of nutrient compounds in a sucrose solution. However, bees’ proboscis extension responses decreased when their antennae were stimulated with pollen- or amino acid-supplemented sucrose solutions. Compared to pure sucrose, bees exhibited worse acquisition when conditioned to an odour with pollen-supplemented sucrose as the unconditioned stimulus. Such learning impairment was also observed with quinine-containing sucrose solutions. Our results suggest that bees can use their antennae to detect pollen compounds in floral nectars. Depending on the type and concentrations of compounds present, this may result in nectar being perceived as distasteful by bees, making it less effective in reinforcing the learning of floral cues. Such reward devaluation might be adaptive in cases where plants benefit from regulating the frequency of bee visitation. Electronic supplementary material The online version of this article (10.1007/s00359-019-01347-z) contains supplementary material, which is available to authorized users.

Combined secondary compounds naturally found in nectars enhance honeybee cognition and survival

“…Given that it is an essential nutritional component for insects (House, 1965), its potential recognition by bees as a palatable substance would be expected. In line with this, previous studies have shown that the presence of other amino acids offered during or before training affects honeybee learning performance (Kim and Smith, 2000;Simcock et al, 2014;Nicholls et al, 2019). In addition, another study has shown that bees can identify umami taste, and has characterized a chemosensory taste receptor that responds to L-amino acids (AmGr10), among which is L-arginine (Lim et al, 2019).…”

Comparative analysis of 3 pollen sterilization methods for feeding bumble bees

“…We used adult worker bees sourced from 3 commercial B. impatiens colonies (BioBest LTD, Leamington, Ontario, Canada) and 6 treatment combinations: sterilization treatment (GI, EO, or no treatment) crossed by pollen type (wildflower pollen mix or monofloral sunflower pollen) with 10 bees/colony/treatment combination (10/colony × 3 colonies × 6 treatment combinations = 180 bees total). Differences in the nutritive quality, secondary metabolite content, and freshness of stored pollen can influence palatability and preferences by bees (Vaudo et al 2016a, Carroll et al 2017, Nicholls and de Ibarra 2017, Nicholls et al 2019). We thus included both the wildflower pollen mixture and monofloral sunflower pollen to assess whether pollen sterilization treatment differentially affected palatability of 2 distinct pollen diets.…”

Pollen, anther, stamen, and androecium mimicry

“…2006; Nicholls et al . 2019) and tarsi as well as proboscis of Eristalis hoverflies (Wacht et al . 1996, 2000).…”

“…Bees can also perceive tactile stimuli via their antennae (Gack 1981). Proline is a common amino acid present in pollenkitt (Linskens & Schrauwen 1969;Mattioli et al 2018) and thus a potential candidate for a universal chemical pollen cue that can be perceived with the antennae of bumblebees (Ruedenauer et al 2019), honeybees (Carter et al 2006;Nicholls et al 2019) and tarsi as well as proboscis of Eristalis hoverflies (Wacht et al 1996(Wacht et al , 2000. However, proline has never been found in pollen-mimicking structures (Biancucci et al 2015), reinforcing that the visual cue is predominant in the PASAM system as compared to any other chemical cue.…”

“…For example, Bougainvillea spectabilis flowers combine three stamenmimicking flowers with petal-like bracts; many Asteraceae inflorescences combine yellow and UV-absorbing disk florets mimicking an androecium and differently coloured ray florets mimicking the corolla of a single flower (Vogel 1978;Osche 1979Osche , 1983Lunau 2000Lunau , 2007. Plant-parasitic fungi are known to stimulate host plants to produce pseudoflowers presenting pseudopollen (Ngugi & Scherm 2006). PASAM structures are potentially multimodal signals including visual, olfactory, gustatory and tactile stimuli, but their chemical properties have only rarely been studied (Ruedenauer et al 2017;Wilmsen et al 2017).…”