Bees and angiosperms have shared a long and intertwined evolutionary history and their interactions have resulted in remarkable adaptations. Yet, at a time when the “pollination crisis” is of major...

The chemical ecology and evolution of bee-flower interactions: a review and perspectives'

Wholemount analysis with optic and confocal microscopy of iontophoretic ally stained (cobalt or Lucifer Yellow) bee antennal lobe interneurones led us to identify and classify four main types of olfactory responsive neurones, differing in their morphology and spatial distribution within the glomerular space and amongst the glomeruli in the whole antennal lobe. Two types of local interneurones (LIN), restricted to the antennal lobe were: (i) Homo LIN presenting an apparently similar density of arbors among all the glomeruli where they branch, the fine neurites being limited to the core of the glomeruli; (ii) Hetero LIN, also pluriglomerular, differ from the Homo LIN by a high dense neurite arborization in one particular glomerulus with fine branches invading the core and reaching the outermost part of this glomerulus. Two types of output interneurones (ON) having dendrites in the antennal lobe and axons projecting in other brain parts were: (i) Uni ON with dendrites invading the core and periphery of only one glomerulus; (ii) Pluri ON, pluriglomerular, with dendrites limited to the glomerular cores. The Uni ON axons follow the median tract and project to the mushroom bodies and lateral lobe of the protocerebrum. On the contrary, axons of Pluri ON follow several subtracts of the antenno-glomerular tract and project to various protocerebal structures or to the contralateral antennal lobe. Local interneurones and output interneurones both invade many glomeruli (1/3 to 2/3 and >50% of the total number, respectively), most being distributed in the different glomerular populations. The high complexity demonstrated in the architecture of the bee antennal lobe neurones might support the high functional complexity described elsewhere (Fonta a al., 1991; Sun et al., submitted).

Morphology and spatial distribution of bee antennal lobe interneurones responsive to odours

The honeybee Apis mellifera has been a central insect model in the study of olfactory perception and learning for more than a century, starting with pioneer work by Karl von Frisch. Research on olfaction in honeybees has greatly benefited from the advent of a range of behavioural and neurophysiological paradigms in the Lab. Here I review major findings about how the honeybee brain detects, processes, and learns odours, based on behavioural, neuroanatomical and neurophysiological approaches. I first address the behavioural study of olfactory learning, from experiments on free-flying workers visiting artificial flowers to laboratory-based conditioning protocols on restrained individuals. I explain how the study of olfactory learning has allowed understanding the discrimination and generalization ability of the honeybee olfactory system, its capacity to grant special properties to olfactory mixtures as well as to retain individual component information. Next, based on the impressive amount of anatomical and immunochemical studies of the bee brain, I detail our knowledge of olfactory pathways. I then show how functional recordings of odour-evoked activity in the brain allow following the transformation of the olfactory message from the periphery until higher-order central structures. Data from extra- and intracellular electrophysiological approaches as well as from the most recent optical imaging developments are described. Lastly, I discuss results addressing how odour representation changes as a result of experience. This impressive ensemble of behavioural, neuroanatomical and neurophysiological data available in the bee make it an attractive model for future research aiming to understand olfactory perception and learning in an integrative fashion.

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Behavioral and neurophysiological study of olfactory perception and learning in honeybees.

IntraceLlular responses to olfactory signals (three components and the combination of mixtures which they can provide) of 90 morphological identified local and output interneurones of the bee antennal lobe (the so-called Homo LIN, Hetero LIN, Pluri ON and Uni ON) were analysed and classified into eight main categories of response profiles. The different morphological types exhibit differences m (i) background activity; (ii) response patterns; and (iii) selectivity and responsiveness to pure odours and mixtures. The results demonstrate that the responses to mixtures are unpredictable from the responses to the single components. Olfactory integration includes inhibitory processes. Results of the present work considered together with those related to the morphological and spatial aspects demonstrate that the antennal lobe layer of the bee olfactory neuronal network is characterized by a complex architecture and connectivity underlying highly complex and somewhat unpredictable intracellular responses.

Odour quality processing by bee antennal lobe interneurones

In order to define the part of olfactory cues in the selective behavior of honeybees, observation on their foraging behavior was carried out on various sunflower genotypes in parallel with chemical analysis of aromatic extracts of the genotypes. Foragers show a preference for the early stages of flowering and, when they are given a choice between couples of parental lines of two commercial hybrids, Marianne and Mirasol, they are randomly distributed on Mirasol parents, but they prefer the female line of Marianne. The comparison of relative proportions of compounds among aromagrams obtained from head space trapping from the two couples of genotypes, reveals (1) a phenological stage effect for 17 compounds among 144 indexed compounds for Marianne lines and for 18 among 136 indexed compounds of Mirasol lines; most of these compounds exhibit higher relative proportions in the early flowering stages, which is related to plant attractiveness towards honeybees; (2) a sex effect for 33 compounds among 144 for Marianne lines and for 14 compounds among 136 for Mirasol lines; further semiquantitative analyses reveal a sex effect for only eight compounds of 134 for Marianne lines and 20 compounds of 250 for Mirasol lines, which represents less than 10% of the indexed compounds. These discriminatory compounds were partly identified by coupled GC-MS. Possible relations between such phenological and genotypical volatile fluctuations and forager attraction are discussed.

Sunflower volatiles involved in honeybee discrimination among genotypes and flowering stages.

A bioassay based on an olfactory conditioning method simulating the foraging situation in laboratory conditions was coupled with chemical analysis of volatile sunflower blends. Behavioural data obtained from for-agers'responses to volatile fraction point out that honeybees need to use only a limited fraction acting as a “simplified aromatic pattern” of the plant, among hundreds of compounds constituting the whole aroma. This active fraction included 27 polar compounds among which 14 were identified. Extension of such data to crop pollination and plant improvement is discussed.

Selective olfactory choices of the honeybee among sunflower aromas: A study by combined olfactory conditioning and chemical analysis.

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Selective olfactory choices of the honeybee among sunflower aromas: A study by combined olfactory conditioning and chemical analysis.