Inhibitory control and memory in the search process for a modified problem in grey squirrels, Sciurus carolinensis.

Inhibiting learned behaviours when they become unproductive and searching for an alternative solution to solve a familiar but different problem are two indicators of flexibility in problem solving. A wide range of animals show these tendencies spontaneously, but what kind of search process is at play behind their problem-solving success? Here, we investigated how Eastern grey squirrels, Sciurus carolinensis, solved a modified mechanical problem that required them to abandon their preferred and learned solution and search for alternative solutions to retrieve out-of-reach food rewards. Squirrels could solve the problem by engaging in either an exhaustive search (i.e., using trial-and-error to access the reward) or a 'backup' solution search (i.e., recalling a previously successful but non-preferred solution). We found that all squirrels successfully solved the modified problem on their first trial and showed solving durations comparable to their last experience of using their preferred solution. Their success and high efficiency could be explained by their high level of inhibitory control as the squirrels did not persistently emit the learned and preferred, but now ineffective, pushing behaviour. Although the squirrels had minimal experience in using the alternative (non-preferred) successful solution, they used it directly or after one or two failed attempts to achieve success. Thus, the squirrels were using the 'backup' solution search process. Such a process is likely a form of generalisation which involves retrieving related information of an experienced problem and applying previous successful experience during problem solving. Overall, our results provide information regarding the search process underlying the flexibility observable in problem-solving success.

Bees associate colour cues with differences in pollen rewards.

In contrast to the wealth of knowledge concerning sucrose-rewarded learning, the question of whether bees learn when they collect pollen from flowers has been little addressed. The nutritional value of pollen varies considerably between species, and it may be that bees learn the features of flowers that produce pollen best suited to the dietary requirements of their larvae. It is still unknown, however, whether a non-ingestive reward pathway for pollen learning exists, and how foraging bees sense differences between pollen types. Here we adopt a novel experimental approach testing the learning ability of bees with pollen rewards. Bumblebees were reared under controlled laboratory conditions. To establish which pollen rewards are distinguishable, individual bees were given the choice of collecting two types of pollen, diluted to varying degrees with indigestible α-cellulose. Bees preferentially collected a particular pollen type, but this was not always the most concentrated sample. Preferences were influenced by the degree of similarity between samples and also by the period of exposure, with bees more readily collecting samples of lower pollen concentration after five trials. When trained differentially, bees were able to associate an initially less-preferred contextual colour with the more concentrated sample, whilst their pollen preferences did not change. Successful learning of contextual cues seems to maintain pollen foraging preferences over repeated exposures, suggesting that fast learning of floral cues may preclude continuous sampling and evaluation of alternative reward sources, leading to constancy in pollen foraging.

Head movements and the optic flow generated during the learning flights of bumblebees.

Insects inform themselves about the 3D structure of their surroundings through motion parallax. During flight, they often simplify this task by minimising rotational image movement. Coordinated head and body movements generate rapid shifts of gaze separated by periods of almost zero rotational movement, during which the distance of objects from the insect can be estimated through pure translational optic flow. This saccadic strategy is less appropriate for assessing the distance between objects. Bees and wasps face this problem when learning the position of their nest-hole relative to objects close to it. They acquire the necessary information during specialised flights performed on leaving the nest. Here, we show that the bumblebee's saccadic strategy differs from other reported cases. In the fixations between saccades, a bumblebee's head continues to turn slowly, generating rotational flow. At specific points in learning flights these imperfect fixations generate a form of 'pivoting parallax', which is centred on the nest and enhances the visibility of features near the nest. Bumblebees may thus utilize an alternative form of motion parallax to that delivered by the standard 'saccade and fixate' strategy in which residual rotational flow plays a role in assessing the distances of objects from a focal point of interest.

Bumblebee calligraphy: the design and control of flight motifs in the learning and return flights of Bombus terrestris.

Many wasps and bees learn the position of their nest relative to nearby visual features during elaborate 'learning' flights that they perform on leaving the nest. Return flights to the nest are thought to be patterned so that insects can reach their nest by matching their current view to views of their surroundings stored during learning flights. To understand how ground-nesting bumblebees might implement such a matching process, we have video-recorded the bees' learning and return flights and analysed the similarities and differences between the principal motifs of their flights. Loops that take bees away from and bring them back towards the nest are common during learning flights and less so in return flights. Zigzags are more prominent on return flights. Both motifs tend to be nest based. Bees often both fly towards and face the nest in the middle of loops and at the turns of zigzags. Before and after flight direction and body orientation are aligned, the two diverge from each other so that the nest is held within the bees' fronto-lateral visual field while flight direction relative to the nest can fluctuate more widely. These and other parallels between loops and zigzags suggest that they are stable variations of an underlying pattern, which enable bees to store and reacquire similar nest-focused views during learning and return flights.

Coordinating compass-based and nest-based flight directions during bumblebee learning and return flights.

Bumblebees tend to face their nest over a limited range of compass directions when learning the nest's location on departure and finding it on their approach after foraging. They thus obtain similar views of the nest and its surroundings on their learning and return flights. How do bees coordinate their flights relative to nest-based and compass-based reference frames to get such similar views? We show, first, that learning and return flights contain straight segments that are directed along particular compass bearings, which are independent of the orientation of a bee's body. Bees are thus free within limits to adjust their viewing direction relative to the nest, without disturbing flight direction. Second, we examine the coordination of nest-based and compass-based control during likely information gathering segments of these flights: loops during learning flights and zigzags on return flights. We find that bees tend to start a loop or zigzag when flying within a restricted range of compass directions and to fly towards the nest and face it after a fixed change in compass direction, without continuous interactions between their nest-based and compass-based directions of flight. A preferred trajectory of compass-based flight over the course of a motif, combined with the tendency of the bees to keep their body oriented towards the nest automatically narrows the range of compass directions over which bees view the nest. Additionally, the absence of interactions between the two reference frames allows loops and zigzags to have a stereotyped form that can generate informative visual feedback.

Do wood ants learn sequences of visual stimuli?

The visually guided foraging routes of some formicine ants are individually stereotyped, suggesting the importance of visual learning in maintaining these routes. We ask here whether the wood ant Formica rufa learns a sequence of visual features encountered at different stages along a route, as reported for honeybees. We trained ants in several simple mazes to follow two alternative routes. Along each two-stage route, the ants first encountered one of two priming stimuli. The identity of the priming stimulus determined which of two choice stimuli was rewarded in the second stage of the route. As stimuli we used ultraviolet and yellow/green light panels, and two black-and-white patterns. Did ants learn to pair each colour with the appropriate black-and-white pattern? Ants learnt readily to discriminate between the two coloured stimuli or between the two black-and-white patterns. They could also pair coloured and black-and-white patterns, provided that the two were presented simultaneously. The ants' behaviour with sequential stimuli varied according to whether the priming stimulus was a coloured stimulus or a black-and-white pattern. When the priming stimulus was coloured, ants seemed to learn the two sequences, but tests showed that their success was probably caused by the after-effects of colour adaptation. With a black-and-white priming stimulus and a coloured second stage stimulus, robust sequential learning could not be demonstrated, although under certain experimental conditions a tiny proportion of ants did acquire the sequence. Thus, ants perform conditional discriminations reliably when priming and choice stimuli are simultaneous, but they usually fail when the stimuli are sequential.

Preferred viewing directions of bumblebees (Bombus terrestris L.) when learning and approaching their nest site.

Many bees and wasps learn about the immediate surroundings of their nest during learning flights, in which they look back towards the nest and acquire visual information that guides their subsequent returns. Visual guidance to the nest is simplified by the insects' tendency to adopt similar viewing directions during learning and return flights. To understand better the factors determining the particular viewing directions that insects choose, we have recorded the learning and return flights of a ground-nesting bumblebee in two visual environments--an enclosed garden with a partly open view between north and west, and a flat roof with a more open panorama. In both places, bees left and returned to an inconspicuous nest hole in the centre of a tabletop, with the hole marked by one or more nearby cylinders. In all experiments, bees adopted similar preferred orientations on their learning and return flights. Bees faced predominantly either north or south, suggesting the existence of two attractors. The bees' selection between attractors seems to be influenced both by the distribution of light, as determined by the shape of the skyline, and by the direction of wind. In the partly enclosed garden with little or no wind, bees tended to face north throughout the day, i.e. towards the pole in the brighter half of their surroundings. When white curtains, which distributed skylight more evenly, were placed around the table, bees faced both north and south. The bees on the roof tended to face south or north when the wind came from a wide arc of directions from the south or north, respectively. We suggest that bees switch facing orientation between north and south as a compromise between maintaining a single viewing direction for efficient view-based navigation and responding to the distribution of light for the easier detection of landmarks seen against the ground or to the direction of the wind for exploiting olfactory cues.

What can be learnt from analysing insect orientation flights using probabilistic SLAM?

In this paper, we provide an analysis of orientation flights in bumblebees, employing a novel technique based on simultaneous localisation and mapping (SLAM) a probabilistic approach from autonomous robotics. We use SLAM to determine what bumblebees might learn about the locations of objects in the world through the arcing behaviours that are typical of these flights. Our results indicate that while the bees are clearly influenced by the presence of a conspicuous landmark, there is little evidence that they structure their flights to specifically learn about the position of the landmark.

Pollen Elicits Proboscis Extension but Does not Reinforce PER Learning in Honeybees.

The function of pollen as a reward for foraging bees is little understood, though there is evidence to suggest that it can reinforce associations with visual and olfactory floral cues. Foraging bees do not feed on pollen, thus one could argue that it cannot serve as an appetitive reinforcer in the same way as sucrose. However, ingestion is not a critical parameter for sucrose reinforcement, since olfactory proboscis extension (PER) learning can be conditioned through antennal stimulation only. During pollen collection, the antennae and mouthparts come into contact with pollen, thus it is possible that pollen reinforces associative learning through similar gustatory pathways as sucrose. Here pollen was presented as the unconditioned stimulus (US), either in its natural state or in a 30% pollen-water solution, and was found to elicit proboscis extension following antennal stimulation. Control groups were exposed to either sucrose or a clean sponge as the US, or an unpaired presentation of the conditioned stimulus (CS) and pollen US. Despite steady levels of responding to the US, bees did not learn to associate a neutral odour with the delivery of a pollen reward, thus whilst pollen has a proboscis extension releasing function, it does not reinforce olfactory PER learning.

Artificial light pollution: are shifting spectral signatures changing the balance of species interactions?

Technological developments in municipal lighting are altering the spectral characteristics of artificially lit habitats. Little is yet known of the biological consequences of such changes, although a variety of animal behaviours are dependent on detecting the spectral signature of light reflected from objects. Using previously published wavelengths of peak visual pigment absorbance, we compared how four alternative street lamp technologies affect the visual abilities of 213 species of arachnid, insect, bird, reptile and mammal by producing different wavelength ranges of light to which they are visually sensitive. The proportion of the visually detectable region of the light spectrum emitted by each lamp was compared to provide an indication of how different technologies are likely to facilitate visually guided behaviours such as detecting objects in the environment. Compared to narrow spectrum lamps, broad spectrum technologies enable animals to detect objects that reflect light over more of the spectrum to which they are sensitive and, importantly, create greater disparities in this ability between major taxonomic groups. The introduction of broad spectrum street lamps could therefore alter the balance of species interactions in the artificially lit environment.

Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid).

Currently, there is concern about declining bee populations and the sustainability of pollination services. One potential threat to bees is the unintended impact of systemic insecticides, which are ingested by bees in the nectar and pollen from flowers of treated crops. To establish whether imidacloprid, a systemic neonicotinoid and insect neurotoxin, harms individual bees when ingested at environmentally realistic levels, we exposed adult worker bumble bees, Bombus terrestris L. (Hymenoptera: Apidae), and honey bees, Apis mellifera L. (Hymenoptera: Apidae), to dietary imidacloprid in feeder syrup at dosages between 0.08 and 125µg l(-1). Honey bees showed no response to dietary imidacloprid on any variable that we measured (feeding, locomotion and longevity). In contrast, bumble bees progressively developed over time a dose-dependent reduction in feeding rate with declines of 10-30% in the environmentally relevant range of up to 10µg l(-1), but neither their locomotory activity nor longevity varied with diet. To explain their differential sensitivity, we speculate that honey bees are better pre-adapted than bumble bees to feed on nectars containing synthetic alkaloids, such as imidacloprid, by virtue of their ancestral adaptation to tropical nectars in which natural alkaloids are prevalent. We emphasise that our study does not suggest that honey bee colonies are invulnerable to dietary imidacloprid under field conditions, but our findings do raise new concern about the impact of agricultural neonicotinoids on wild bumble bee populations.

Adaptation of microglomerular complexes in the honeybee mushroom body lip to manipulations of behavioral maturation and sensory experience.

Worker honeybees proceed through a sequence of tasks, passing from hive and guard duties to foraging activities. The underlying neuronal changes accompanying and possibly mediating these behavioral transitions are not well understood. We studied changes in the microglomerular organization of the mushroom bodies, a brain region involved in sensory integration, learning, and memory, during adult maturation. We visualized the MB lips' microglomerular organization by applying double labeling of presynaptic projection neuron boutons and postsynaptic Kenyon cell spines, which form microglomerular complexes. Their number and density, as well as the bouton volume, were measured using 3D-based techniques. Our results show that the number of microglomerular complexes and the bouton volumes increased during maturation, independent of environmental conditions. In contrast, manipulations of behavior and sensory experience caused a decrease in the number of microglomerular complexes, but an increase in bouton volume. This may indicate an outgrowth of synaptic connections within the MB lips during honeybee maturation. Moreover, manipulations of behavioral and sensory experience led to adaptive changes, which indicate that the microglomerular organization of the MB lips is not static and determined by maturation, but rather that their organization is plastic, enabling the brain to retain its synaptic efficacy.