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Fig. 4.7. Categorization of bilateral symmetry by honeybees, (a) Example of a succession of triads used to train honeybees to symmetry. The three stimuli differed in shape among triads, but each triad consisted of one symmetrical, rewarding stimulus (+) and two asymmetrical non-rewarding stimuli (-) presented simultaneously. Training with each triad was interspersed with multiple-choice tests, (b) Symmetrical and asymmetrical novel test stimuli were presented; none had rewards, (c) Choice frequency for the trained feature in bees trained for symmetry (black circles) and for asymmetry (empty circles). 0.5 means random choice between the two categories of novel stimuli. From test 7 onwards, bees transferred the information appropriately to the novel stimuli, thus demonstrating a capacity to detect, learn, and abstract symmetry or asymmetry as an independent visual pattern feature (modified from Giurfa etal. 1996a).
the field. Since the bees did not show a particular bias towards symmetry or asymmetry at the beginning of the training procedure (see Fig. 4.7c, tests 1-6), it must be concluded that the formation of categories ("symmetry" and "asymmetry") observed from test 7 on was a result of the training procedure used in those experiments.
Horridge (1996), again training bees to bilaterally symmetrical stimuli, used large patterns presented in the Y-maze set-up at a distance of 27 cm from the decision point. Thus, unlike the experiments of Giurfa et al. (1996a), Horridge's experiments tested symmetry detection at a farther range. In different training experiments, the rewarding patterns had either a vertical or horizontal plane of symmetry. Bees learned the orientation of the symmetry axis in either case. They discriminated the learned orientation from other orientations even when the test patterns were novel to them. Thus, bees generalize the orientation of the axis of symmetry much the same way in which they generalize the orientation of visible contrasting edges (Srinivasan 1994), although the symmetry axis does not constitute a visible edge between two contrasting areas.
Thus, in the case of symmetry perception, there are no fundamental differences between performance at a close range and that at a further range. The only condition that must be met is that the bee sees the whole pattern; the symmetry of large patterns is perceived at a larger distance than is the symmetry of small patterns. Lehrer (1999) proposed that radial symmetry (but not bilateral symmetry) might also be recognized in large patterns viewed at a close distance, on the basis of the presence of a number of neighboring radiating pattern elements.
Experience-based flexibility of behavior and cognitive capacities
Pattern recognition in the bee is based on several capacities, the use of which depends on the experimental procedures. Forming a template requires constant spatial relations between eyes and patterns. This condition is met only when a fixation point is available to the bee, and when the distribution of areas contained in the rewarding pattern is kept constant throughout the training. In natural flowers, a fixation point is usually provided by the site of reward in the center of the flower.
Bees can, however, learn to extract a particular cue and use it in the discrimination task, even when they are presented with novel patterns, as seen in several examples above. Using artificial stimuli, there are two ways that bees can be made to generalize a particular cue. One is to train bees using two patterns, one rewarding and one not, that differ from each other only in the one parameter to be learned. In this type of experiment, bees learn to "pay attention" to the parameter in which the two patterns differ. Selective attention is a capacity than can be considered cognitive, at least to some extent (Goldstone 1998). In the present review, some examples of this capacity are the detection of presence or absence of a colored disc against a contrasting background, the discrimination between two colored stimuli that differ in amount of green contrast, and the discrimination between a horizontal and a vertical axis in patterns that do not differ in symmetry.
A second method is to train bees to a set of training patterns, all rewarding, that have one parameter in common but are randomized with respect to all other parameters. This procedure prevents the forming of an association between any of the variable features and the reward, leaving the animal with only one useful cue, namely the one that is preserved in all of the training stimuli. A measure of the animal's capacity to learn that particular cue is the degree to which the animal generalizes it to novel stimuli. This methodology has been traditionally used in testing the cognitive abilities of some vertebrates (Harlow 1949). The first experiments of this type with honeybees were performed by Lehrer et al. (1988) to study distance estimation by size-independent cues. Two other examples cited above are the generalization of orientation (Hateren et al. 1990) and of symmetry (Giurfa et al. 1996a). It is particularly this type of performance that reveals a cognitive capacity, because it involves some type of "categorization" (Pearce 1994). Categorization is defined as the capacity to discriminate on the basis of a feature common to all members of a set of stimuli, and to generalize that feature to novel stimuli. These requirements are met in the experiments on range discrimination (Lehrer et al. 1988), on the use of pattern orientation (Hateren et al. 1990), and on symmetry perception (Giurfa et al. 1996a) by honeybees.
The flexibility evinced by honeybees in visual tasks reviewed in this chapter is clearly adaptive. In natural conditions, the appearance of a particular flower species that the bee has visited on a previous foraging trip may change slightly from one visit to the next. For instance, the color may differ slightly among individuals of the same species. Pattern parameters and the spatial orientation of flowers may vary, even within the same plant, depending on genetic and environmental factors. Further, not all bilaterally symmetrical flowers are vertically oriented; the axis of symmetry may be subjected to changes in spatial alignment. Behavioral flexibility thus allows the insect to cope with a changing environment in which visual cues display a certain degree of variability.
Still, bees do use particular parameters more efficiently than others, even in the absence of previous experience and even despite experimental manipulations. For example, pattern disruption is more effective than shape, symmetrical patterns are more attractive than asymmetrical patterns, black shapes on a white background are more effective than white shapes on a black background, and color is at any time a more effective signal than any spatial parameter (Menzel 1985; Gould & Gould 1988). Thus, some innate, genetically fixed behavioral programs must be involved in the bee's choice behavior. Such programs help the bees discover natural flowers even on their very first foraging trips.
In tasks involving color and spatial vision, innate preferences may be weakened through training, but no training procedure can cause them to disappear completely. Bees can be trained to asymmetrical patterns, although they are better at symmetrical ones (Giurfa et al. 1996a); they can be trained to low frequencies at short distances, although they prefer high frequencies (Lehrer 1997); they can learn a horizontal axis of symmetry, although they prefer a vertical one (Horridge 1996); and, they can even be trained to a white shape on a black background, although they prefer black shapes on a white background (Wehner 1972). However, in these cases, learning is slow, and the frequencies of correct choices seldom reach the high value that they do in training experiments that support the bee's innate tendencies. From the ecological point of view, this makes sense: natural flowers display exactly those parameters that bees tend to prefer (Giurfa et al. 1995b; Lehrer et al. 1995; M0ller 1995; M0ller & Eriksson 1995; Neal et al. 1998).
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