Taste Perception in Honey Bees

Chem. Senses 36: 675–692, 2011 doi:10.1093/chemse/bjr040 Advance Access publication May 26, 2011 Taste Perception in Honey Bees Maria Gabriela de Brito Sanchez1,2 1 Université Paul Sabatier, Centre de Recherches sur la Cognition Animale, 118 route de Narbonne, F-31062 Toulouse Cedex 9, France and 2CNRS, Centre de Recherches sur la Cognition Animale, 118 route de Narbonne, F-31062 Toulouse Cedex 9, France Correspondence to be sent to: Maria Gabriela de Brito Sanchez, Research center on Animal Cognition, CNRS, University Paul Sabatier, 118 route de Narbonne, 31062 Toulouse Cedex 9, France. e-mail: Accepted April 1, 2011 Abstract Taste is crucial for honeybees for choosing profitable food sources, resins, water sources, and for nestmate recognition. Peripheral taste detection occurs within cuticular hairs, the chaetic and basiconic sensilla, which host gustatory receptor cells and, usually a mechanoreceptor cell. Gustatory sensilla are mostly located on the distal segment of the antennae, on the mouthparts, and on the tarsi of the forelegs. These sensilla respond with varying sensitivity to sugars, salts, and possibly amino acids, proteins, and water. So far, no responses of receptor cells to bitter substances were found although inhibitory effects of these substances on sucrose receptor cells could be recorded. When bees are free to express avoidance behaviors, they reject highly concentrated bitter and saline solutions. However, such avoidance disappears when bees are immobilized in the laboratory. In this case, they ingest these solutions, even if they suffer afterward a malaise-like state or even die from such ingestion. Central processing of taste occurs mainly in the subesophageal ganglion, but the nature of this processing remains unknown. We suggest that coding tastants in terms of their hedonic value, thus classifying them in terms of their palatability, is a basic strategy that a central processing of taste should achieve for survival. Key words: central processing of taste, gustation, gustatory receptors, honeybee, insect, peripheral taste detection, subesophageal ganglion, taste Introduction Since the pioneer work of von Frisch (1967), the honeybee Apis mellifera has emerged as an important insect model for the study of problems as diverse as perception, learning, memory, communication, navigation, and social organization. Although the processing of olfactory and visual information by honey bees has been intensively studied in the last decades in the context of their interaction with flowers (vision: Menzel and Backhaus 1991; Giurfa and Menzel 1997; Wakakuwa et al. 2005; olfaction: Galizia and Menzel 2000; Deisig et al. 2002, 2006; Guerrieri et al. 2005), less is known about the processing of gustatory stimuli by honey bees. Taste, the sense that distinguishes between chemical compounds and the sensations they produce based on contact with chemoreceptors, allows discriminating edible from nonedible items and is, therefore, crucial for survival. Here I will review fundamental aspects of the biology of taste of the honeybee, indicating thereby what is known and what requires further investigations. I will focus on ‘‘taste’’ in a natural context in the life of a honeybee and highlight characteristics of taste receptor cells and the peripheral processing of taste via the main gustatory appendages. I will afterward present newer characterizations of gustatory molecular receptors present in gustatory cells using a comparative approach and discuss whether or not honey bees possess a limited taste perception. This question will be analyzed through a special focus on the perception of substances that taste bitter to humans (henceforth bitter substances). Finally, I will analyze the central processing of taste using again a comparative approach. The conclusion will underline open questions that need to be answered to achieve a better understanding of the taste biology of the honeybee. Honey bee taste in a natural context Gustatory stimuli play a fundamental role in a honeybee’s life. In a foraging context, honeybee foragers collect nectar and pollen, which respectively provide carbohydrates and proteins that are necessary for survival. Nectar presents not only different types of sugars such as sucrose, glucose, and/or fructose but also organic acids, lipids, minerals, vitamins, and aromatic compounds, even if these substances constitute a low ª The Author 2011. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: 676 M.G. de Brito Sanchez percentage of nectar contents (Harborne 1994). Pollen contains proteins but also lipids, mineral salts, albumin, zvitamins, amino acids, growth regulator factors, folic acid, and enzymes among others (Harborne 1994). Furthermore, besides foraging for nectar and pollen, bees collect water, and in this context, they respond to salts. Additionally, bees collect resin for elaborating propolis and should then taste several compounds such as prenylated and nonprenylated phenylpropanoids, terpenoids, and anthracene derivatives, which have been identified in the resin loads transported in the corbiculae of the posterior legs (Weinstein Texeira et al. 2005). Finally, bees chew and process wax with their mouthparts and, thus, may taste and react to the chemicals contained in it. Taste stimuli may play further vital roles in the life of honeybees. Although the examples provided above refer essentially to adult bees that engage in different foraging activities outside the hive, younger bees within the hive may also use their gustatory senses for different purposes. Besides olfaction, taste may allow intracolonial recognition within the dark world of a hive. It has been repeatedly shown that cuticular hydrocarbons confer a chemical signature allowing nestmate recognition (e.g., Châline et al. 2005; Dani et al. 2005). So far, it is not clear whether such recognition occurs via olfactory or gustatory input. In the fruit fly Drosophila melanogaster, olfactory and gustatory inputs are involved in sensing cuticular hydrocarbons (Ferveur 2005). Cuticular hydrocarbons are usually high-molecular weight compounds so that airborne detection may not be the primary detection channel; contact chemoreceptors may be involved and gustatory detection may be the privileged channel for nestmate recognition. A tight interaction between wax comb and cuticular hydrocarbons has been shown (Breed et al. 1988) so that both may constitute a continuous medium for any hydrocarbon-soluble substances used by honeybees in nestmate recognition. Peripheral processing of taste Searching for the gustatory receptors In the honeybee, the antennae, mouthparts, and distal segments of the forelegs constitute the main chemosensory organs (Goodman 2003; see Figure 1a). On these appendages, gustatory but also hygro, thermo, mechanosensory, and olfactory receptor cells are located within specialized cuticular structures called sensilla. (...truncated)