The forest or the trees: preference for global over local image processing is reversed by prior experience in honeybees

Traditional models of insect vision have assumed that insects are only capable of low-level analysis of local cues and are incapable of global, holistic perception. However, recent studies on honeybee (Apis mellifera) vision have refuted this view by showing that this insect also processes complex visual information by using spatial configurations or relational rules. In the light of these findings, we asked whether bees prioritize global configurations or local cues by setting these two levels of image analysis in competition. We trained individual free-flying honeybees to discriminate hierarchical visual stimuli within a Y-maze and tested bees with novel stimuli in which local and/or global cues were manipulated. We demonstrate that even when local information is accessible, bees prefer global information, thus relying mainly on the object''s spatial configuration rather than on elemental, local information. This preference can be reversed if bees are pre-trained to discriminate isolated local cues. In this case, bees prefer the hierarchical stimuli with the local elements previously primed even if they build an incorrect global configuration. Pre-training with local cues induces a generic attentional bias towards any local elements as local information is prioritized in the test, even if the local cues used in the test are different from the pre-trained ones. Our results thus underline the plasticity of visual processing in insects and provide new insights for the comparative analysis of visual recognition in humans and animals.     

Mapping Sleeping Bees within Their Nest: Spatial and Temporal Analysis of Worker Honey Bee Sleep

Patterns of behavior within societies have long been visualized and interpreted using maps. Mapping the occurrence of sleep across individuals within a society could offer clues as to functional aspects of sleep. In spite of this, a detailed spatial analysis of sleep has never been conducted on an invertebrate society. We introduce the concept of mapping sleep across an insect society, and provide an empirical example, mapping sleep patterns within colonies of European honey bees (Apis mellifera L.). Honey bees face variables such as temperature and position of resources within their colony''s nest that may impact their sleep. We mapped sleep behavior and temperature of worker bees and produced maps of their nest''s comb contents as the colony grew and contents changed. By following marked bees, we discovered that individuals slept in many locations, but bees of different worker castes slept in different areas of the nest relative to position of the brood and surrounding temperature. Older worker bees generally slept outside cells, closer to the perimeter of the nest, in colder regions, and away from uncapped brood. Younger worker bees generally slept inside cells and closer to the center of the nest, and spent more time asleep than awake when surrounded by uncapped brood. The average surface temperature of sleeping foragers was lower than the surface temperature of their surroundings, offering a possible indicator of sleep for this caste. We propose mechanisms that could generate caste-dependent sleep patterns and discuss functional significance of these patterns.     

The preferences of the honeybee (Apis mellifera) for different visual cues during the learning process

By working with very simple images, a number of different visual cues used by the honeybee have been described over the past decades. In most of the work, the bees had no control over the choice of the images, and it was not clear whether they learned the rewarded pattern or the difference between two images. Preferences were known to exist when untrained bees selected one pattern from a variety of them, but because the preferences of the bees were ignored, it was not possible to understand how natural images displaying several cues were detected. The preferences were also essential to make a computer model of the visual system. Therefore experiments were devised to show the order of preference for the known cues in the training situation. Freely flying bees were trained to discriminate between a rewarded target with one pattern on the left side and a different one on the right, versus a white or neutral target. This arrangement gave the bees a choice of what to learn. Tests showed that in some cases they learned two or three cues simultaneously; in other cases the bees learned one, or they preferred to avoid the unrewarded target. By testing with different combinations of patterns, it was possible to put the cues into an order of preference. Of the known cues, loosely or tightly attached to eye coordinates, a black or blue spot was the most preferred, followed by strong modulation caused by edges, the orientation of parallel bars, six equally spaced spokes, a clean white target, and then a square cross and a ring. A patch of blue colour was preferred to yellow.     

Nonelemental visual learning in honeybees

Free-flying honeybees, Apis mellifera, learn visual stimuli in the appetitive context of food search. Visual compound stimuli are relevant in nautre as bees learn flower images that consist of many visual elements. We studied whether elemental associations between each visual element and the reinforcement (elemental approach) are enough to explain the solving of visual discrimination problems that raise ambiguity at the elemental level. We asked whether bees could solve three different visual discriminations: (1) positive patterning (A−, B−, AB+); (2) negative patterning (A+, B+, AB−); and (3) biconditional discrimination (AB+, CD+, AC−, BD−). In experiments 1 and 2 bees had to discriminate a yellow-violet chequerboard from the yellow or the violet squares alone. In experiment 3, four different gratings combining one colour (yellow or violet) with one orientation (vertical or horizontal) had to be discriminated. In all three problems binary compounds were trained in such a way that each element appeared equally often as rewarded and nonrewarded. Bees could solve the three discrimination problems. They always chose the reinforced stimulus despite ambiguity at the level of the elements. For solving positive patterning, elemental processing could be used. For negative patterning and biconditional discrimination, nonelemental processing strategies (unique-cue or configural approach) are necessary to account for these results. Although we cannot decide between a configural and a unique-cue interpretation, we can clearly reject purely elemental processing in these cases. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Fearful symmetry? Intra-individual comparisons of asymmetry in cryptic vs. signalling colour patterns in butterflies

The signalling role of asymmetry has attracted considerable recent interest among evolutionary biologists. Although it has been studied primarily within the context of sexual selection, symmetry of signals may play a role also in inter-specific communication, such as predator–prey interactions. Both theory and experimental evidence suggest that asymmetry may impair the efficacy of visual warning signals used to deter potential predators, but increase the protective value of non-signalling, cryptic colour patterns used to decrease the risk of detection. Here we tested the prediction from this hypothesis by means of intra-individual comparisons of asymmetry in colour pattern elements in three species of moths (Arctia caja (L.), Noctua orbona (L.), Smerinthus ocellata (L.)) that possess cryptic fore wing patterns and signalling hind wing patterns. Mean asymmetries constituted 4.3% (range 2.1–7.0%) of trait size for colour pattern elements, whereas individual asymmetry levels reached as high as 26%. Asymmetry tended to be somewhat larger in cryptic patterns on fore wings than in signalling patterns on hind wings in five of six comparisons, but in only one case was the difference statistically significant. In addition, pattern elements were somewhat more asymmetric on fore wings also in Saturnia pavonia (L.), which possesses identical signalling eyespots on both fore and hind wings. The relatively low levels of asymmetry also in cryptic patterns imply either that selection does not favour increased asymmetry in cryptic patterns, or that the evolution of pronounced asymmetry is developmentally or genetically constrained.     

The 185/333 gene family is a rapidly diversifying host-defense gene cluster in the purple sea urchin Strongylocentrotus purpuratus

The genome of the purple sea urchin contains numerous large gene families with putative immunological functions. One gene family, known as 185/333, is characterized by extraordinary molecular diversity resulting from single nucleotide polymorphisms and the presence or the absence of 27 large blocks of sequences known as elements. The mosaic composition of elements, known as element patterns, that is present within the members of this gene family is encoded entirely in the second of two exons. Many of the elements correspond to one of six types of repeats that are present throughout the genes. The sequence diversity and variation in element patterns led us to investigate the evolution of the 185/333 gene family. The work presented here suggests that the element patterns are the result of both recombination and duplication and/or deletion of intragenic repeats. Each element is composed of a limited number of similar but distinct sequences, and their distribution among the 185/333 genes suggests frequent recombination within this gene family. Phylogenetic analyses of five 185/333 elements and two regions of the intron were performed using two tests: incongruence length difference and incongruence permutation. Results indicated that each pair of sequence segments was incongruent, suggesting that recombination occurs frequently along the length of the genes, including both the intron and the second exon, and that recombination is not restricted to intact elements. Paradoxically, the high level of similarity among the elements indicated that the 185/333 genes appear to be the result of a recent diversification. These results add to the growing body of evidence suggesting that invertebrate immune systems are not simple and static, but are dynamic and highly complex, and may employ group-specific mechanisms for diversification.     

The generalization of directional visual stimuli in the honey bee, Apis mellifera

In transfer tests the ability of bees to generalize visual stimuli was tested by using differently inclined stripes and stripe patterns offered on a vertical screen. After having been trained to single stripes or equidistant stripe patterns, which were orientated by α₊ = 45° to the horizontal, the bees had to discriminate between the training direction α₊ and the competition direction α_c = 135° by means of special stripe configurations. These transfer patterns were obtained by varying different stimulus parameters of the original training stripes, for example by (1) reversing contrast between a stripe and the surrounding visual field, (2) changing the ratio of length/width and by this the dimensions of the stripe, and (3) inserting white intervals into the black stripes. In all three test series the bees succeeded in detecting the α₊-direction along a broad range of stimulus variations. As the bees in the transfer tests positively responded to patterns, which on the other side were significantly discriminated from the training pattern (control tests), the information about the direction of the visual cue had been transferred to a new pattern configuration never seen by the bees during the training situation.     

Spontaneous number representation in semi-free-ranging rhesus monkeys

Previous research has shown that animals possess considerable numerical abilities. However, this work was based on experiments involving extensive training, a small number of captive subjects and relatively artificial testing procedures. We present the results of experiments on over 200 semi-free-ranging rhesus monkeys using a task which involves no training and mimics a natural foraging problem. The subjects observed two experimenters place pieces of apple, one at a time, into each of two opaque containers. The experimenters then walked away so that the subjects could approach. The monkeys chose the container with the greater number of apple slices when the comparisons were one versus two, two versus three, three versus four and three versus five slices. They failed at four versus five, four versus six, four versus eight and three versus eight slices. Controls established that it was the representation of number which underlay their successful choices rather than the amount of time spent placing apple pieces into the box or the volume of apple placed in the box. The failures at values greater than three slices stand in striking contrast to other animal studies where training was involved and in which far superior numerical abilities were demonstrated. The range of success achieved by rhesus monkeys in this spontaneous-number task matches the range achieved by human infants and corresponds to the range encoded in the syntax of natural languages.     

Nocturnal Homing: Learning Walks in a Wandering Spider?

Homing by the nocturnal Namib Desert spider Leucorchestris arenicola (Araneae: Sparassidae) is comparable to homing in diurnal bees, wasps and ants in terms of path length and layout. The spiders'' homing is based on vision but their basic navigational strategy is unclear. Diurnal homing insects use memorised views of their home in snapshot matching strategies. The insects learn the visual scenery identifying their nest location during learning flights (e.g. bees and wasps) or walks (ants). These learning flights and walks are stereotyped movement patterns clearly different from other movement behaviours. If the visual homing of L. arenicola is also based on an image matching strategy they are likely to exhibit learning walks similar to diurnal insects. To explore this possibility we recorded departures of spiders from a new burrow in an unfamiliar area with infrared cameras and analysed their paths using computer tracking techniques. We found that L. arenicola performs distinct stereotyped movement patterns during the first part of their departures in an unfamiliar area and that they seem to learn the appearance of their home during these movement patterns. We conclude that the spiders perform learning walks and this strongly suggests that L. arenicola uses a visual memory of the burrow location when homing.     

Effects of Rhododendron removal and prescribed fire on bees and plants in the southern Appalachians

Rhododendron maximum is an evergreen shrub native to the Appalachian Mountains of North America that has expanded in recent decades due to past disturbances and land management. The purpose of this study was to explore how bees and plants were affected by the experimental removal of R. maximum followed by a prescribed fire in one watershed compared to a neighboring reference watershed. Bees and plants were sampled for three years in both watersheds. Comparisons were based on the rarefaction and extrapolation sampling curves of Hill numbers as well as multivariate methods to assess effects on community composition. Bee richness, Shannon''s diversity, and Simpson''s diversity did not differ between watersheds in the year after removal but were all significantly higher in the removal watershed in year two, following the prescribed fire. Bee Shannon''s diversity and Simpson''s diversity, but not richness, remained significantly higher in the removal watershed in the third year. Similar but weaker patterns were observed for plants. Comparisons of community composition found significant differences for bees in the second and third year and significant differences for plants in all three years. For both groups, significant indicator taxa were mostly associated with the removal watershed. Because bees appeared to respond more strongly to the prescribed fire than to the removal of R. maximum and these benefits weakened considerably one year after the fire, clearing R. maximum does not appear to dramatically improve pollinator habitat in the southern Appalachians. This conclusion is underscored by the fact that about one quarter of the bee species in our study area were observed visiting R. maximum flowers. The creation of open areas with wildflowers may be a better way to benefit bees in this region judging from the high diversity of bees captured in the small roadside clearings in this study.     

Chromatic and achromatic stimulus discrimination of long wavelength (red) visual stimuli by the honeybee Apis mellifera

It has long been assumed that bees cannot see red. However, bees visit red flowers, and the visual spectral sensitivity of bees extends into wavelengths to provide sensitivity to such flowers. We thus investigated whether bees can discriminate stimuli reflecting wavelengths above 560 nm, i.e., which appear orange and red to a human observer. Flowers do not reflect monochromatic (single wavelength) light; specifically orange and red flowers have reflectance patterns which are step functions, we thus used colored stimuli with such reflectance patterns. We first conditioned honey bees Apis mellifera to detect six stimuli reflecting light mostly above 560 nm and found that bees learned to detect only stimuli which were perceptually very different from a bee achromatic background. In a second experiment we conditioned bees to discriminate stimuli from a salient, negative (un-rewarded) yellow stimulus. In subsequent unrewarded tests we presented the bees with the trained situation and with five other tests in which the trained stimulus was presented against a novel one. We found that bees learned to discriminate the positive from the negative stimulus, and could unambiguously discriminate eight out of fifteen stimulus pairs. The performance of bees was positively correlated with differences between the trained and the novel stimulus in the receptor contrast for the long-wavelength bee photoreceptor and in the color distance (calculated using two models of the honeybee colors space). We found that the differential conditioning resulted in a concurrent inhibitory conditioning of the negative stimulus, which might have improved discrimination of stimuli which are perceptually similar. These results show that bees can detect long wavelength stimuli which appear reddish to a human observer. The mechanisms underlying discrimination of these stimuli are discussed. Handling Editor: Lars Chittka.     

Influence of Unrewarded Stimuli on the Classification of Visual Patterns by Honey Bees

Bees were trained to discriminate visual patterns in five experiments. The rewarded pattern (S+), was a 50-mm black disc in all experiments; the unrewarded pattern (S–) was varied. Subsequently bees were given a choice between different stimuli in order to discover what bees learnt about five attributes of the training stimuli. The attributes tested were size, contrast, color, ‘compactness’ vs. ‘dissectedness’ (tests with ring-patterns), and presence or absence of acute points (tests with discs, squares, triangles and stars). The significance of these attributes varied with the particular unrewarded pattern (S–) used in training (Figs. 1, 2). This is interpreted as a modification of the bee's selective attention to certain features during training. The results also indicate a difference in the salience of attributes. Differences in size or outline (presence of acute points) only influenced the bee's preference after a training that specifically required this distinction, while differences in contrast, colour and dissectedness were also significant when the training stimuli did not differ in that respect.     

Places and patterns — a study of context learning in honeybees

To investigate the priming of memories by contextual cues, bees were trained to negotiate two mazes in different places 25?m apart. In the first maze, bees flew leftwards when the inner wall of the maze was covered with 45° stripes or rightwards when the inner wall was coloured yellow. In the second maze, bees flew rightwards on viewing 135° diagonal stripes or leftwards on viewing blue. The trajectories evoked by 45° or 135° stripes were similar in both mazes. However, vertical stripes were treated like 45° stripes in maze 1 and like 135° stripes in maze 2. Contextual cues prime the response to stripes that are oriented in the training condition for that site so influencing responses to stripes in closely neighbouring orientations. What objects in a bee's surroundings determine its sense of place? Bees were trained to different visual patterns at two sites 40?m apart (A+ versus A– at site A, and E+ versus E– at site E). A+ was preferred over A– and E+ was preferred over E– at both training sites. A preference for A+ over E+ exhibited at site A dropped gradually with distance to suggest that spatial context includes both close and distant objects.     

Folk knowledge of invertebrates in Central Europe - folk taxonomy,nomenclature, medicinal and other uses,folklore, and nature conservation

Background

There is scarce information about European folk knowledge of wild invertebrate fauna. We have documented such folk knowledge in three regions, in Romania, Slovakia and Croatia. We provide a list of folk taxa, and discuss folk biological classification and nomenclature, salient features, uses, related proverbs and sayings, and conservation.

Methods

We collected data among Hungarian-speaking people practising small-scale, traditional agriculture. We studied “all” invertebrate species (species groups) potentially occurring in the vicinity of the settlements. We used photos, held semi-structured interviews, and conducted picture sorting.

Results

We documented 208 invertebrate folk taxa. Many species were known which have, to our knowledge, no economic significance. 36 % of the species were known to at least half of the informants. Knowledge reliability was high, although informants were sometimes prone to exaggeration. 93 % of folk taxa had their own individual names, and 90 % of the taxa were embedded in the folk taxonomy.Twenty four species were of direct use to humans (4 medicinal, 5 consumed, 11 as bait, 2 as playthings). Completely new was the discovery that the honey stomachs of black-coloured carpenter bees (Xylocopa violacea, X. valga) were consumed. 30 taxa were associated with a proverb or used for weather forecasting, or predicting harvests. Conscious ideas about conserving invertebrates only occurred with a few taxa, but informants would generally refrain from harming firebugs (Pyrrhocoris apterus), field crickets (Gryllus campestris) and most butterflies. We did not find any mythical creatures among invertebrate folk taxa. Almost every invertebrate species was regarded as basically harmful. Where possible, they were destroyed or at least regarded as worth eradicating. However, we could find no evidence to suggest any invertebrate species had suffered population loss as a result of conscious destruction. Sometimes knowledge pertaining to the taxa could have more general relevance, and be regarded as folk wisdom concerning the functioning of nature as a whole.

Conclusions

The high number of known invertebrate folk taxa suggests that it would be worth conducting further investigations in other areas of Europe.

     

Multisensory integration of colors and scents: insights from bees and flowers

Karl von Frisch’s studies of bees’ color vision and chemical senses opened a window into the perceptual world of a species other than our own. A century of subsequent research on bees’ visual and olfactory systems has developed along two productive but independent trajectories, leaving the questions of how and why bees use these two senses in concert largely unexplored. Given current interest in multimodal communication and recently discovered interplay between olfaction and vision in humans and Drosophila, understanding multisensory integration in bees is an opportunity to advance knowledge across fields. Using a classic ethological framework, we formulate proximate and ultimate perspectives on bees’ use of multisensory stimuli. We discuss interactions between scent and color in the context of bee cognition and perception, focusing on mechanistic and functional approaches, and we highlight opportunities to further explore the development and evolution of multisensory integration. We argue that although the visual and olfactory worlds of bees are perhaps the best-studied of any non-human species, research focusing on the interactions between these two sensory modalities is vitally needed.     

Numerical Abstraction in Young Domestic Chicks (Gallus gallus)

In a variety of circumstances animals can represent numerical values per se, although it is unclear how salient numbers are relative to non-numerical properties. The question is then: are numbers intrinsically distinguished or are they processed as a last resort only when no other properties differentiate stimuli? The last resort hypothesis is supported by findings pertaining to animal studies characterized by extensive training procedures. Animals may, nevertheless, spontaneously and routinely discriminate numerical attributes in their natural habitat, but data available on spontaneous numerical competence usually emerge from studies not disentangling numerical from quantitative cues. In the study being outlined here, we tested animals'' discrimination of a large number of elements utilizing a paradigm that did not require any training procedures. During rearing, newborn chicks were presented with two stimuli, each characterized by a different number of heterogeneous (for colour, size and shape) elements and food was found in proximity of one of the two stimuli. At testing 3 day-old chicks were presented with stimuli depicting novel elements (for colour, size and shape) representing either the numerosity associated or not associated with food. The chicks approached the number associated with food in the 5vs.10 and 10vs.20 comparisons both when quantitative cues were unavailable (stimuli were of random sizes) or being controlled. The findings emerging from the study support the hypothesis that numbers are salient information promptly processed even by very young animals.     

Nest preference and ecology of cavity-nesting bees (Hymenoptera: Apoidea) in Punjab,Pakistan

Among bees, 85 % are solitary species, most of them are ground-nester and some are cavity-nesting and construct their nests in pre-existing cavities. This work was conducted to evaluate the substrate preference and nest architecture (acceptance, occupation percentage, seasonality and parasitism) of cavity-nesting bees in different substrates. Trap nests offered comprised five different materials (drilled cavities in wood, bamboo, cardboard tubes, plastic soda straws, and mud blocks). These were installed in four districts for two years. The nesting cavities of five different diameters (6, 8, 10, 12 and 14 mm) were provided in each nesting material with an average length of 180 ± 9.92 mm. In all the materials, 5400 nesting cavities were offered, out of which 628 were colonized by bees from two families (Megachilidae and Apidae) and six species (Megachile cephalotes, M. lanata, M. bicolor, Xylocopa basalis, X. fenestrata and Ceratina smaragdula), including one parasitic bee (Euaspis carbonaria). The bee species differed significantly in occupying five nesting materials. The most preferred diameters were 8 mm and 10 mm, with 52.20% and 29.45% of colonization, respectively. Nesting was done throughout the year except in winter. This study will serve as a baseline for future studies and conservation programs of cavity-nesting bees in Pakistan.     

Discrimination of coloured patterns by honeybees through chromatic and achromatic cues

We investigated pattern discrimination by worker honeybees, Apis mellifera, focusing on the roles of spectral cues and the angular size of patterns. Free-flying bees were trained to discriminate concentric patterns in a Y-maze. The rewarded pattern could be composed of either a cyan and a yellow colour, which presented both different chromatic and achromatic L-receptor contrast, or an orange and a blue colour, which presented different chromatic cues, but the same L-receptor contrast. The non-rewarded alternative was either a single-coloured disc with the colour of the central disc or the surrounding ring of the pattern, a checkerboard pattern with non-resolvable squares, the reversed pattern, or the elements of the training pattern (disc or ring alone). Bees resolved and learned both colour elements in the rewarded patterns and their spatial properties. When the patterns subtended large visual angles, this discrimination used chromatic cues only. Patterns with yellow or orange central discs were generalised toward the yellow and orange colours, respectively. When the patterns subtended a visual angle close to the detection limit and L-receptor contrast was mediating discrimination, pattern perception was reduced: bees perceived only the pattern element with higher contrast.     

Observations on the big bang flowering of Miconia minutiflora (Melastomataceae)

Trees ofMiconia minutiflora produced abundant flowers for only one to three days during mid-April 1983 in the vicinity of Saül, French Guiana. They attracted large numbers of at least 14 species of bees that collected nectar or pollen or both. Nectar production is uncommon in the Melastomataceae and not previously reported forMiconia. Peak bee activity at the trees was in the morning and by afternoon most visits were limited to those bees in search of remnant pollen, especially species ofTrigona. As has been shown for other neotropical plants, heavy rains may trigger flowering in this species. It is suggested that the flowering system ofM. minutiflora promotes outcrossing because of interactions among the numerous species of bees visiting the trees and because of inter-individual variation in nectar and pollen availability. Therefore, bees may fly to other trees instead of becoming satiated with nectar or pollen from a single tree.