Object detection by honeybees: Why do they land on edges?

Behavioural experiments using a variety of experimental situations (Figs. 1, 3, 6, 7, 9) were conducted to investigate the visual cues which bees use in the task of object-ground discrimination. The bees' flight and landing behaviour was video-filmed throughout the experiments. The evaluation of the video data shows that bees trained to find a randomly textured figure raised above a similarly textured ground land mainly on the boundaries of the figure, facing its inner surface (Fig. 2a, b). Bees can also be trained to find a hole, i.e. a low texture viewed through a window cut in a raised texture, but these bees are not attracted to the edges of the hole (Fig. 5a, b). Bees trained to a single edge between a low and a raised random texture land at the edge mainly facing the raised side (Table 1). Bees approaching the edge from the high side cross the edge in most cases without landing on it (Table 1). Bees trained to an edge between 2 striped patterns, one raised above the other, again land on the edge facing the raised pattern, regardless of whether the stripes on the 2 patterns run parallel or perpendicular to each other or to the edge (Fig. 8). In this case, the bees acquire range information by flying in oblique directions with respect to the orientation of the stripes (Fig. 10). All of the results suggest that the edge elicits landings when the bee perceives a local increase in the speed of image motion, signalling an abrupt decrease in range. This is corroborated by the results of further experiments in which artificial motion was used to simulate range differences between the two sides of an edge (Table 2). We conclude that image speed is a powerful cue in range discrimination as well as object detection. Dedicated to G. Adrian Horridge on the occasion of his retirement     

Why do bees turn back and look?

The timing of learning of colour and shape of the food source, as well as of near-by landmarks, was examined exploiting a behaviour described recently, the Turn Back and Look behaviour (TBL): Bees departing from a novel food source after feeding turn around to view it at a short distance (Figs. 2, 3) before departing for the hive. They repeat this behaviour on several successive visits, termed the TBL phase (Fig. 5). To examine the function of the TBL, I trained individual bees in 4 different modes. In the first 3 they could view a food source or a landmark of a particular colour or shape during (i) arrival as well as departure, (ii) only arrival, and (iii) only departure; in the final mode (iv) the bees viewed one colour (or shape) on arrival, and another on departure. At the end of the TBL phase, the bees were tested by offering them a choice between the visual stimulus to which they were trained (modes i–iii) and a different (novel) one, or between the stimulus viewed on arrival and that viewed on departure (mode iv). The test results show that learning after feeding (while performing the TBL), i.e. backward conditioning, occurs regardless of whether the colour (Fig. 6, Fig. 10a) or shape (Fig. 7) of the food source, or the colour (Fig. 10b), shape (Fig. 11), and position (Fig. 12) of a near-by landmark is considered. Bees trained in mode (iv) preferred the stimulus learned on arrival over that learned on departure in almost all cases. However, a stimulus viewed exclusively on departure (mode iii) was often learned as well as when it was viewed exclusively on arrival (mode ii) (Figs. 10a, 11, 12), or both on arrival and departure (mode i) (Fig. 6). The finding that the timing of learning can be manipulated suggests that it is not based on hard wired predispositions to learn particular visual cues on arrival, and others on departure.     

Generalization in visual recognition by the honeybee (Apis mellifera) : A review and explanation

During a century of studies on honeybee vision, generalization was the word for the acceptance of an unfamiliar pattern in the place of the training pattern, or the ability to learn a common factor in a group of related patterns. The ideas that bees generalize one pattern for another, detect similarity and differences, or form categories, were derived from the use of the same terms in the human cognitive sciences. Recent work now reveals a mechanistic explanation for bees. Small groups of ommatidia converge upon feature detectors that respond selectively to certain parameters that are in the pattern: modulation in the receptors, edge orientations, or to areas of black or colour. Within each local region of the eye the responses of each type of feature detector are summed to form a cue. The cues are therefore not in the pattern, but are local totals in the bee. Each cue has a quality, a quantity and a position on the eye, like a neuron response. This summation of edge detector responses destroys the local pattern based on edge orientation but preserves a coarse, sparse and simplified version of the panorama. In order of preference, the cues are: local receptor modulation, positions of well-separated black areas, a small black spot, colour and positions of the centres of each cue, radial edges, the averaged edge orientation and tangential edges. A pattern is always accepted by a trained bee that detects the expected cues in the expected places and no unexpected cues. The actual patterns are irrelevant. Therefore we have an explanation of generalization that is based on experimental testing of trained bees, not by analogy with other animals.Historically, generalization appeared when the training patterns were regularly interchanged to make the bees examine them. This strategy forced the bees to ignore parameters outside the training pattern, so that learning was restricted to one local eye region. This in turn limited the memory to one cue of each type, so that recognition was ambiguous because the cues were insufficient to distinguish all patterns. On the other hand, bees trained on very large targets, or by landing on the pattern, learned cues in several eye regions, and were able to recognize the coarse configural layout.     

Bee-pollination inHibbertia fasciculata (Dilleniaceae)

In direct contrast to mostHibbertia spp., the flowers ofH. fasciculata R. Br. ex D. C. bear only a single whorl of stamens and these stamens are arranged separately (not in typical bundles). The short filaments are appressed to the three carpels so that the inflated, porose and introrsive anthers form a centralized cluster obscuring the three ovaries. The three slender styles emerge at right angles from between the filaments. These styles curve upward and the stigmas form the three points of a triangle; each stigma is approximately one millimeter outside the centralized cluster of anthers. The flowers are nectarless and bear a bright yellow corolla. A pungent and unpleasant fragrance appears to be concentrated within the pollenkitt. When native bees attempt to forage for the pollen, within the cluster of anthers, the ventrally deposited loads of pollen, on the bees' abdomens, contact the outer triangle of stigmas. The major pollinators ofH. fasciculata are female bees in the polylectic genera,Lasioglossum (subgenusChilalictus, Halictidae) andLeioproctus (Colletidae). These bees carry an average of more than two pollen taxa when they are caught foraging onH. fasciculata. 78% of the 47 bees, captured onH. fasciculata carried the pollen from at least one sympatric taxon bearing nectariferous flowers (e.g., genera in theMyrtaceae, Compositae, andEpacridaceae). The pollination biology ofH. fasciculata is assessed in relation to the known radiation of bee-pollinated flowers in the genusHibbertia, and within theDilleniaceae s. l.     

Uniformity of Leaf Shelter Construction by Larvae of Epargyreus clarus (Hesperiidae), the Silver-Spotted Skipper

Larvae of the silver-spotted skipper, Epargyreus clarus (Hesperiidae), construct shelters from leaves of their leguminous host plants, making four distinct shelter types that change predictably over larval ontogeny. Shelters built by first-instar larvae are located on the apical half of the leaflet and are almost invariant in size, shape, and orientation, suggesting a stereotypical process of shelter location and construction. We have determined that the regularity of these shelters results from a prescribed pattern of larval movements and behaviors, in which larvae use their body length as a ruler and employ silk not only as a building material but also as a template to guide the location of cuts in the leaf. Though lepidopteran larvae lack the sensitive antennae, long jointed appendages, and other measurement devices used by structure-building bees, wasps, and caddis flies, they can nonetheless use simple tools and behavioral patterns to produce characteristic and regular shelters.     

A Change in Orientation: Recognition of Rotated Patterns by Bumble Bees

In three experiments, bumble bees were trained to discriminate between a reinforcing pattern (S+) and a nonreinforcing one (S–) which differed only in the configuration of four artificial petals. They were subsequently tested for recognition of the S+ rotated by 90° (S + 90). Experiment 1 used petals of four colors, and the other experiments used four symbols. The symbols either remained unchanged when the whole pattern was rotated (e.g., + in Experiment 2) or changed appearance (e.g., < in Experiment 3). The bees failed to recognize the S + 90 in the first two experiments, but in Experiment 3, the choice proportion for S + 90 in the presence of a New pattern was significantly higher than chance. Bumble bees can recognize a rotated pattern, possibly by using mental rotation, provided that a cue as to the extent of the pattern transformation is given.     

Light-inducedtrans-cis isomerization of retinal by a protein from honeybee retina

Summary Two retinal-binding proteins (RBP-A and RBP-B) isolated from the honeybee retina were further purified by ion-exchange chromatography. Whereas RBP-A seems to be denatured by this procedure, RBP-B remains intact with respect to its photochemical characteristics (Fig. 3a). Analysis of the geometric isomers of retinal bound to RBP-B by high performance liquid chromatography demonstrated that all-trans retinal was the chromophore of the non-irradiated RBP-B. Irradiation converted RBP-B (_max 440 nm) into a photoproduct (_max 370 nm) the chromophore of which was 11-cis retinal, i.e., light isomerized all-trans retinal almost exclusively to the 11-cis form (Fig. 3b). Irradiation of a solution of RBP-B in the presence of excess all-trans retinal also led to the formation of 11-cis retinal indicating that RBP catalyzes the photoisomerization of all-trans retinal. The physiological significance of RBP-B is discussed with respect to the renewal of rhodopsin.Abbreviations RBP retinal-binding protein - HPLC high performance liquid chromatography     

Floral constancy in bumble bees: handling efficiency or perceptual conditioning?

Individual bees often prefer flowers of the same species that they are already foraging on, and other individual bees prefer other flowers. This floral constancy has classically been explained as a learned behavior by which bees avoid wasting time switching between handling techniques. Choice trails were given to Bombus vagans workers that were freely foraging in mixed and pure fields of Trifolium pratense, T. repens, Viccia cracca, and Prunella vulgaris. Contrary to expectation, (1) bees showed if anything a stronger preference for their flower type in pure fields where they lacked experience than in a mixed field where they had had the opportunity to learn, (2) there was greater constancy in a mixed field of the two morphologically similar Trifolium species than in a mixed field of the morphologically disparate T. pratense and P. vulgaris, and (3) bees were more willing to switch between flowers of distinct morphologies when the colors were similar than between flowers of distinct colors when the morphologies were similar. We suggest that constancy is due to some form of perceptual conditioning whereby individual bees become temporarily sensitized to one or a few floral cues.     

An owl's eye: Schematic optics and visual performance inStrix aluco L.

Summary The schematic eye ofStrix aluco, a nocturnal owl species, is described. A comparative and ecological context is used to examine the relationships between optical parameters of the eye and its light gathering and resolving powers. It is concluded that the essentially nocturnal feature of the owl eye does not lie in either its light gathering power or the sensitivity of individual rod receptors. Differences in visual performance at low light levels between the owl and the diurnal pigeon appear to be attributable to differences in the retinal neural integration mechanisms of the two species. However, it is hypothesised that the neural mechanisms which mediate the extraction of spatial information from the retinal image throughout the nocturnal luminance range, can function in the owl eye only because of its absolutely large sized retinal image. Thus the primarily nocturnal feature of the owl eye is its absolutely large posterior nodal distance, retinal image brightness is maximised only as a secondary feature.Abbreviation PND posterior nodal distance     

The menotactic orientation of the prosobranch mollusc Littorina littorea

The menotactic orientation of the prosobranch mollusc Littorina littorea to a one stripe pattern (Fig. 2) has been investigated under open-loop and closed-loop conditions. Results: 1) Under open-loop conditions the animals try to compensate for an angular deviation of the pattern from the menotactic angular position by turning movements of, on the average, constant angular velocity (Fig. 4). 2) The angular velocity depends on this deviation according to the -characteristic (Fig. 5). The orientation behaviour under closed-loop conditions can be directly derived from the -characteristic. Within experimental limits the snail does not show an optomotor response. 3) To patterns of wedge-shaped intensity distribution the snails orientate at a small angle relative to the edge of the pattern (Fig. 3). The orientation angle of the animals to this pattern is much less variable than the orientation angle to a single light source. The orientation behaviour shows that the intensity gradient of the pattern is important for the orientation of the animal. 4) A normally distributed noise process is superimposed on the average orientation direction. The variance of this noise process is the same for the orientation under open-loop and under closed-loop conditions (Fig. 7). In both cases the power spectrum of the noise process contains pronounced maxima at equally spaced frequencies (Fig. 8).     

Allometric relations,metabolism and heart conductance in clusters of honey bees at cool temperatures

Summary Clusters of honey bees,Apis mellifera carnica, showed a clear dependence of oxygen consumption and heat conductance on bee cluster mass (between 5 g and 1.2 kg) when exposed to a cold temperature (2°C) overnight. As the bee cluster mass was increased, total cluster metabolism increased. Mass-specific oxygen consumption, , decreased with increasing mass following the relation: = 22.69BW ^−0.479 (Fig. 1). Larger clusters of bees had lower heat conductance (i.e., better insulation) than the smaller groups (Fig. 4). The mechanisms of adaptation and adjustment to cold temperature in bee clusters are discussed and compared with those of mammals and birds.     

What the honeybee sees: a review of the recognition system of Apis mellifera

Abstract. For many years, two opposing theories have dominated our ideas of what honeybees see. The earliest proposal based on training experiments was that bees detected only simple attributes or features, irrespective of the actual pattern. The features demonstrated experimentally before 1940 were the disruption of the pattern (related to spatial frequency), the area of black or colour, the length of edge, and the angle of orientation of a bar or grating. Cues discovered recently are the range, and radial and tangential edges, and symmetry, relative to the fixation point, which is usually the reward hole. This theory could not explain why recognition failed when the pattern was moved. In the second theory, proposed in 1969, the bee detected the retinotopic directions of black or coloured areas, and estimated the areas of overlap and nonoverlap on each test pattern with the corresponding positions in the training pattern. This proposal explained the progressive loss of recognition as a test pattern was moved or reduced in size, but required that the bees saw and remembered the layout of every learned pattern and calculated the mismatch with each test image. Even so, the same measure of the mismatch was given by many test patterns and could not detect a pattern uniquely. Moreover, this theory could not explain the abundant evidence of simple feature detectors. Recent work has shown that bees learn one or more of a limited number of simple cues. A newly discovered cue is the position, mainly in the vertical direction, of the common centre (centroid) of black areas combined together. Significantly, however, the trained bees look for the cues mentioned above only in the range of places where they had occurred during the training. These two observations made possible a synthesis of both theories. There is no experimental evidence that the bees detect or re-assemble the layout of patterns in space; instead, they look for a cue in the expected place. With an array of detectors of the known cues, together with their directions, this mechanism would enable bees to recognize each familiar place from the coincidences of cues in different directions around the head.     

Elementary pattern discrimination (behavioural experiments with the fly Musca domestica)

This paper investigates the problem of spontaneous pattern discrimination by the visual system of the fly. The indicator for discrimination and attractivity of a pattern is the yaw torque of a test fly. It is shown that the pattern discrimination process may be treated as a special (degenerate) case of figureground discrimination which has been described in detail in earlier publications. Decisive for the discrimination process is the fact that pattern discrimination by the fly is mediated by motion detectors which respond not only a pattern velocity but also to structural properties of pattern contrast. This is demonstrated by the transition from the existing twodimensional array of motion detectors to a continuous detector field which enabled us to calculate instantaneous detector responses to instationary pattern motion. The new approach, together with the special theory for figure-ground discrimination, is then applied to predict spontaneous discriminations of onedimensional periodic patterns. It is shown that predictions and experimental results are in good agreement. The second set of discrimination experiments deals with two dimensional dot patterns for which a quantitative theory is not yet available. However, it is shown that the attractivity of a dot pattern crucially depends on both the orientation and the direction of motion relative to the fly's eyes. If the contrast of a moving dot elicits an event in a motion detector which through the detector's time constant leads to an interference with an event received by a preceeding dot, the attractivity of the dot pattern is diminished. In the discussion relations are drawn between the concepts of pattern discrimination in honey bees and the theoretical aspects of discrimination put forward in this paper. It is briefly discussed why a two-dimensional motion detector theory might become the key for an understanding of pattern categories like figural intensity and figural quality.     

Flower-feeding specialization in wild bee and wasp communities in seasonal neotropical habitats

Summary Flower visitation records were obtained for 192 species of bees and 138 species of wasps in three neotropical habitats. Four indices of feeding specialization were calculated for common species, and similar patterns were observed using each index. Variation in specialization could be attributed to several factors: the habitat and season in which species were found, the degree of sociality of species, and whether species were bees or wasps. Important differences among habitats and seasons were the number of coexisting consumer species and the species richness and phenology of resource plants. Differences in average consumer specialization among habitats and seasons may have been the result of differences in competitive pressures and to a lesser extent, differences in the flowering strategies of local plants. Eusocial bees and wasps were much more generalized in feeding than solitary species, and bees were more generalized than wasps. Bees in these neotropical communities were much less specialized than their north temperate counterparts. This pattern is reflected by the near absence of species that feed at only one or two plant species in Guanacaste, as compared to a very high frequency of these extreme specialist species in north temperate areas. Temperate zone species of bees have less even visitation rates to their resources than tropical bees. Consequently, temperate zone bees are more specialized in both the variety of plant species visited and the dominance of visitation to each set of resource plants. Several hypotheses are examined as possible explanations for this apparent qualitative difference in community structure between neotropical and temperate communities.     

EEG analysis gives model of neuronal template-matching mechanism for sensory search with olfactory bulb

The spatial pattern of EEG activity at the surface of the olfactory bulb tends to be invariant with respect to input and to change to a new pattern whenever an animal is trained to expect or search for a particular odor. It is postulated here that the spatial EEG pattern is dependent on a neural template for that odor that is formed during training. This hypothesis is expressed in the form of a model consisting of an array of interconnected elements (1x10 or 6x6). Each element represents 2 excitatory and 2 inhibitory subsets of neurons with 3 types of internal feedback: negative, mutually excitatory, and mutually inhibitory. The elements are interconnected only by mutual excitation and mutual inhibition. Each neural subset is represented by a nonlinear differential equation; the connections are represented by modifiable coupling coefficients. With appropriate values of the time, coupling, and gain coefficients, and with input that is modelled on olfactory input, the set of 40 or 144 equations gives output that simulates the time and space patterns of the EEG.In the naive state the coefficients are uniform. A template is formed by giving input to selected elements, cross-correlating the outputs, and weighting the mutually excitatory coupling coefficient between each pair of elements by the corresponding correlation coefficient. When a template has been formed, input to nontemplate elements is treated as noise. Optionally a matched filter is made to simulate habituation by reducing the synaptic gain coefficients of those excitatory subsets that receive the noise. The model is tested by giving input to nontemplate elements and to none, part or all of the template elements.There are two outputs of the model. One is the spatial pattern V _j of the root mean square (rms) amplitudes of the individual outputs v(j,t) of the elements. The other output is the rms amplitude E _rms of the ensemble average E(t) over v(j, t).The results show that V _j depends on the template and is relatively insensitive to input, whether or not input is given to template elements. However, E _rms increases in proportion to the number of hits on the template. If the number of elements receiving noise does not exceed the number of elements in a template, or if the noise is matched with a habituation filter, then E _rms rises above the noise level for a hit on any one or more template elements irrespective of location or combination. V _j conforms to the performance of the surface EEG. E _rms is not yet accessible to physiological measurement.Supported by a grant MH 06686 from the National Institute of Mental Health and by a Research Professorship from the Miller Institute, Berkeley.     

Transplantation of a time-signal in honeybees

Summary It has been possible — by transplantation of brain tissue (i.e. mushroom-bodies) — to perform an interindividual transfer of a learned time-signal in honeybees. The information of the donor bees becomes determinative for the temporal activity pattern of the recipients about 3 to 4 days following transplantation.As seen from histological investigations done in parallel, the donor tissue is treated as a xenograft by the recipient's organism including disintegration and encapsulation processes. These observations give evidence for a humoral transfer of information.The results are discussed from the point of view of the analysis of the mechanism of time reception.Dedicated to Prof. Dr. H. Autrum on the occasion of his 70th birthdaySupported by the Akademie der Wissenschaften und der Literatur zu Mainz, the Stiftung Volkswagenwerk and the Deutsche ForschungsgemeinschaftAll observations done were individual per hand registrations. We want to give thanks to all people in the department who helped us to do the experiments.     

Neural expectation: cerebellar and retinal analogs of cells fired by learnable or unlearned pattern classes

Neural networks are introduced which can be taught by classical or instrumental conditioning to fire in response to arbitrary learned classes of patterns. The filters of output cells are biased by presetting cells whose activation prepares the output cell to expect prescribed patterns. For example, an animal that learns to expect food in response to a lever press becomes frustrated if food does not follow the lever press. It's expectations are thereby modified, since frustration is negatively reinforcing. A neural analog with aspects of cerebellar circuitry is noted, including diffuse mossy fiber inputs feeding parallel fibers that end in Purkinje cell dendrites, climbing fiber inputs ending in Purkinje cell dendrites and giving off collaterals to nuclear cells, and inhibitory Purkinje cell outputs to nuclear cells. The networks are motivated by studying mechanisms of pattern discrimination that require no learning. The latter often use two successive layers of inhibition, analogous to horizontal and amacrine cell layers in vertebrate retinas. Cells exhibiting hue (in)constancy, brightness (in)constancy, or movement detection properties are included. These results are relevant to Land's retinex theory and to the existence of opponent- and nonopponent-type cell responses in retinal cells. Some adaptation mechanisms, and arousal mechanisms for crispening the pattern weights that can fire a given cell, are noted.Supported in part by the Alfred P. Sloan Foundation and the Office of Naval Research (N00014-67-A-0204-0051).