Variation In Learning Abilities Research Articles

Odour Learning Bees Have Longer Foraging Careers Than Non-learners in a Natural Environment

Individual animals allowed the opportunity to learn generally outperform those prevented from learning, yet, within a species the capacity for learning varies markedly. The evolutionary processes that maintain this variation in learning ability are not yet well understood. Several studies demonstrate links between fitness traits and visual learning, but the selection pressures operating on cognitive traits are likely influenced by multiple sensory modalities. In addition to vision, most animals will use a combination of hearing, olfaction (smell), gustation (taste), and touch to gain information about their environment. Some animals demonstrate individual preference for, or enhanced learning performance using certain senses in relation to particular aspects of their behaviour (e.g., foraging), whereas conspecific individuals may show different preferences. By assessing fitness traits in relation to different sensory modalities we will strengthen our understanding of factors driving observed variation in learning ability. We assessed the relationship between the olfactory learning ability of bumble bees (Bombus terrestris) and their foraging performance in their natural environment. We found that bees which failed to learn this odour-reward association had shorter foraging careers; foraging for fewer days and thus provisioning their colonies with fewer resources. This was not due to a reduced propensity to forage, but may have been due to a reduced ability to return to their colony. When comparing among only individuals that did learn, we found that the rate at which floral resources were collected was similar, regardless of how they performed in the olfactory learning task. Our results demonstrate that an ability to learn olfactory cues can have a positive impact of the foraging performance of B. terrestris in a natural environment, but echo findings of earlier studies on visual learning, which suggest that enhanced learning is not necessarily beneficial for bee foragers provisioning their colony.

No sex differences in learning in wild bumblebees

Abstract Females and males often face different sources of selection, resulting in dimorphism in morphological, physiological, and even cognitive traits. Sex differences are often studied in respect to spatial cognition, yet the different ecological roles of males and females might shape cognition in multiple ways. For example, in dietary generalist bumblebees (Bombus), the ability to learn associations is critical to female workers, who face informationally rich foraging scenarios as they collect nectar and pollen from thousands of flowers over a period of weeks to months to feed the colony. While male bumblebees likely need to learn associations as well, they only forage for themselves while searching for potential mates. It is thus less clear whether foraging males would benefit from the same associative learning performance as foraging females. In this system, as in others, cognitive performance is typically studied in lab-reared animals under captive conditions, which may not be representative of patterns in the wild. In the first test of sex and species differences in cognition using wild bumblebees, we compared the performance of Bombus vancouverensis nearcticus (formerly bifarius) and Bombus vosnesenskii of both sexes on an associative learning task at Sierra Nevada (CA) field sites. Across both species, we found that males and females did not differ in their ability to learn, although males were slower to respond to the sucrose reward. These results offer the first evidence from natural populations that male bumblebees may be equally as able to learn associations as females, supporting findings from captive colonies of commercial bees. The observed interspecific variation in learning ability opens the door to using the Bombus system to test hypotheses about comparative cognition.

Strain differences rather than species differences contribute to variation in associative learning ability in Nasonia

Insect species display a large range of inter- and intraspecific variation in learning and memory retention. Variation in associative learning ability has also been reported for three species in the parasitoid wasp genus Nasonia, most notably between Nasonia vitripennis and Nasonia giraulti, for which inbred isogenic strains have been established and studied intensively. We addressed the question how learning and memory of such isogenic strains compare to the phenotypes found in genetically diverse strains of these species. We recorded memory retention of both isogenic and genetically diverse strains of two species at 4–120 h after either olfactory or visual conditioning. Memory retention typically declined over time, but the pattern of decline differed consistently between strains. The isogenic N. vitripennis strain formed long-lasting (>5 days) memory, whereas the isogenic N. giraulti strain lost its memory after 48 h. Yet, genetically diverse strains of both species formed long-lasting memory. Memory retention patterns of strains were independent of sensory modality of the conditioned stimulus for all strains. These results show that there is variation for associative learning and memory within the two species, but not clear interspecies differences in memory retention. Without a better overview of the natural variation in learning abilities within a species, individual strains, especially isogenic strains with low genetic variability, are not necessarily representative of the species in general.

Exploring individual variation in associative learning abilities through an operant conditioning task in wild baboons.

Cognitive abilities underpin many of the behavioural decisions of animals. However, we still have very little understanding of how and why cognitive abilities vary between individuals of the same species in wild populations. In this study, we assessed the associative learning abilities of wild chacma baboons (Papio ursinus) across two troops in Namibia with a simple operant conditioning task. We evaluated the ability of individuals to correctly associate a particular colour of corn kernels with a distasteful flavour through repeated presentations of two small piles of corn dyed different colours, one of which had been treated with a non-toxic bitter substance. We also assessed whether individual variation in learning ability was associated with particular phenotypic traits (sex, social rank and neophilia) and states (age and prior vigilance). We found no evidence of learning the association either within each trial or across trials, nor any variation based on individuals' phenotypes. This appeared to be due to a high tolerance for bitter foods leading to similar acceptance of both palatable and unpalatable kernels. Earlier avoidance of the bitter kernels during pilot trials suggests this higher tolerance may have been largely driven by a drought during the experiments. Overall, our findings highlight the potential influence of current environmental challenges associated with conducting cognitive tests of animals in the wild.

Interindividual variation in learning ability in honeybees

Performance on different cognitive tasks could either be positively correlated in an individual as a measure of general intelligence or costs related to specific aspects of cognition could give rise to specialized cognitive phenotypes. Social living offers the potential for individual specialization in learning and a cooperative group can benefit from a diversity of learning phenotypes. However, there is little empirical data regarding the nature of such interindividual variation in learning abilities in honeybees, a classic model of animal cognition. We tested for the presence of variation in learning abilities in the honeybee, Apis mellifera, and whether any component of learning has an influence on wing damage, a proxy for performance and survival. Our results show considerable interindividual variation in different types of learning abilities. At the individual level, while landmark and olfactory learning abilities are negatively correlated, olfactory learning shows a positive association with maneuverability performance, a measure which in turn shows a positive influence on wing damage, a proxy for survival. We discuss our results in the context of cognitive diversity and specialization in a social group.

Testing domain general learning in an Australian lizard.

A key question in cognition is whether animals that are proficient in a specific cognitive domain (domain specific hypothesis), such as spatial learning, are also proficient in other domains (domain general hypothesis) or whether there is a trade-off. Studies testing among these hypotheses are biased towards mammals and birds. To understand constraints on the evolution of cognition more generally, we need broader taxonomic and phylogenetic coverage. We used Australian eastern water skinks (Eulamprus quoyii) with known spatial learning ability in three additional tasks: an instrumental and two discrimination tasks. Under domain specific learning we predicted that lizards that were good at spatial learning would perform less well in the discrimination tasks. Conversely, we predicted that lizards that did not meet our criterion for spatial learning would likewise perform better in discrimination tasks. Lizards with domain general learning should perform approximately equally well (or poorly) in these tasks. Lizards classified as spatial learners performed no differently to non-spatial learners in both the instrumental and discrimination learning tasks. Nevertheless, lizards were proficient in all tasks. Our results reveal two patterns: domain general learning in spatial learners and domain specific learning in non-spatial learners. We suggest that delineating learning into domain general and domain specific may be overly simplistic and we need to instead focus on individual variation in learning ability, which ultimately, is likely to play a key role in fitness. These results, in combination with previously published work on this species, suggests that this species has behavioral flexibility because they are competent across multiple cognitive domains and are capable of reversal learning.

Transgenerational loss and recovery of early learning ability in foraging predatory mites

The ability to learn is ubiquitous in animals but highly variable within and between species, populations and individuals. Diet-related circumstances, such as diet quantity and quality can influence both long-term constitutive (genetic; by selection) and short-term operational (non-genetic; by the immediate circumstances) learning performance. Here, we scrutinized the causes of loss of learning ability, following multi-generational feeding on pollen, in a line of the predatory mite Amblyseius swirskii, which was previously well able to learn prey during early life, enhancing foraging later in life. We investigated whether, and, if so, how quickly, a transgenerational diet switch to live prey restores the early learning ability of foraging predatory mites. The first experiment shows that the early learning ability was restored after switching the diet of the pollen-fed predator line to live spider mites for two generations before conducting the behavioral assay. The second experiment reveals that offspring regained their learning ability if the diet of their mothers was switched from pollen to spider mites for 3 or 10 days before offspring production. Both experiments in concert suggest transgenerational, pollen-induced operational loss of learning ability in the predatory mite A. swirskii. Maternally-transmitted nutrient deficiency and/or maternally-induced epigenetic changes are the most plausible explanations for the pollen diet-induced loss of learning ability. Our study represents a key example for maternal diet-induced variation in learning ability.

Constitutive and Operational Variation of Learning in Foraging Predatory Mites.

Learning is widely documented across animal taxa but studies stringently scrutinizing the causes of constitutive or operational variation of learning among populations and individuals are scarce. The ability to learn is genetically determined and subject to constitutive variation while the performance in learning depends on the immediate circumstances and is subject to operational variation. We assessed variation in learning ability and performance of plant-inhabiting predatory mites, Amblyseius swirskii, caused by population origin, rearing diet, and type of experience. Using an early learning foraging paradigm, we determined that homogeneous single prey environments did not select for reduced learning ability, as compared to natural prey-diverse environments, whereas a multi-generational pollen diet resulted in loss of learning, as compared to a diet of live prey. Associative learning produced stronger effects than non-associative learning but both types of experience produced persistent memory. Our study represents a key example of environmentally caused variation in learning ability and performance.

Reproductive environment affects learning performance in bumble bees

Despite a presumed fitness advantage for individuals with well-developed cognitive abilities, learning performance is usually found to be highly variable within a population. Although little is currently known about the mechanisms responsible for maintaining such variation, there is correlative evidence to suggest that learning performance may be linked to reproductive physiology in the social insects. Bumble bee colonies naturally undergo an initial co-operative phase, when only the queen reproduces, and a subsequent competition phase when all colony members compete to produce male offspring. We experimentally induced these distinct phases by manipulating the presence/absence of the queen and assessed changes in sucrose responsiveness and learning performance. We found that nest-based workers upregulated their reproductive potential in queenless colonies, and correspondingly, these bees were more responsive to sucrose than their queenright counterparts, performing better in an olfactory learning task as a result. These findings suggest that differences in ovarian development are responsible for at least some of the remarkable variation in learning performance that can be observed among very closely related members of social insect colonies. Cognitive abilities are often assumed to be inherently adaptive, so the question of why individuals vary in their learning ability has received relatively little attention. Here, we focus on reproductive status as a proximate cause of variation in learning ability in the social insects. We show that a significant proportion of the surprising variation that exists between genetically similar colony members can be explained by worker ovarian development; reproductively active workers are more sensitive to food rewards and thus learn more quickly. Learning ability may be one of a suite of correlated traits that are linked to reproductive physiology in social insects and therefore play an important role in the evolution of division of labour.

Towards systemic and individualized brain markers for learning difficulties

Towards systemic and individualized brain markers for learning difficulties

A comparison of visual and olfactory learning performance in the bumblebee Bombus terrestris

Animals use cues from a range of sensory modalities to discriminate stimuli and as predictors of reward. Whilst there is appreciable variation in the cognitive performance of animals, we know surprisingly little about the extent to which learning varies among individuals across different sensory modalities. Do individuals that are good at learning in one sensory modality also perform well in another (performance is correlated between modalities), or do individuals demonstrate specialisation in learning performance in one modality (trading-off performance between modalities)? We tested these hypotheses by examining the performance of 76 Bombus terrestris workers, from four colonies, in both an odour-and visual learning task. Olfactory learning was assessed using proboscis extension reflex (PER) conditioning and visual (colour) learning was examined using a well-established free-flying paradigm. Our results showed neither a correlation, nor a trade-off, in individual performance for learning tasks using different sensory modalities. However, there was considerable variation among workers within each colony in their performance in both learning tasks. This extent of interindividual variation in learning ability across sensory modalities could be adaptive for colonies dealing with changeable foraging conditions. There was also significant intercolony variation in final task performance level in the olfactory learning task, and both the strength and persistence of blue preference in the colour learning task. This is the first study to demonstrate variation in olfactory learning performance across multiple bumblebee colonies using PER conditioning, suggesting this is an effective paradigm for assessing associative olfactory learning performance both within and among colonies.

Foraging errors play a role in resource exploration by bumble bees (Bombus terrrestris).

If the cognitive performance of animals reflects their particular ecological requirements, how can we explain appreciable variation in learning ability amongst closely related individuals (e.g. foraging workers within a bumble bee colony)? One possibility is that apparent 'errors' in a learning task actually represent an alternative foraging strategy. In this study we investigate the potential relationship between foraging 'errors' and foraging success among bumble bee (Bombus terrestris) workers. Individual foragers were trained to choose yellow, rewarded flowers and ignore blue, unrewarded flowers. We recorded the number of errors (visits to unrewarded flowers) each bee made during training, then tested them to determine how quickly they discovered a more profitable food source (either familiar blue flowers, or novel green flowers). We found that error prone bees discovered the novel food source significantly faster than accurate bees. Furthermore, we demonstrate that the time taken to discover the novel, more profitable, food source is positively correlated with foraging success. These results suggest that foraging errors are part of an 'exploration' foraging strategy, which could be advantageous in changeable foraging environments. This could explain the observed variation in learning performance amongst foragers within social insect colonies.

NaCl Taste Thresholds in 13 Inbred Mouse Strains

Molecular mechanisms of salty taste in mammals are not completely understood. We use genetic approaches to study these mechanisms. Previously, we developed a high-throughput procedure to measure NaCl taste thresholds, which involves conditioning mice to avoid LiCl and then examining avoidance of NaCl solutions presented in 48-h 2-bottle preference tests. Using this procedure, we measured NaCl taste thresholds of mice from 13 genealogically divergent inbred stains: 129P3/J, A/J, BALB/cByJ, C3H/HeJ, C57BL/6ByJ, C57BL/6J, CBA/J, CE/J, DBA/2J, FVB/NJ, NZB/BlNJ, PWK/PhJ, and SJL/J. We found substantial strain variation in NaCl taste thresholds: mice from the A/J and 129P3/J strains had high thresholds (were less sensitive), whereas mice from the BALB/cByJ, C57BL/6J, C57BL/6ByJ, CE/J, DBA/2J, NZB/BINJ, and SJL/J had low thresholds (were more sensitive). NaCl taste thresholds measured in this study did not significantly correlate with NaCl preferences or amiloride sensitivity of chorda tympani nerve responses to NaCl determined in the same strains in other studies. To examine whether strain differences in NaCl taste thresholds could have been affected by variation in learning ability or sensitivity to toxic effects of LiCl, we used the same method to measure citric acid taste thresholds in 4 inbred strains with large differences in NaCl taste thresholds but similar acid sensitivity in preference tests (129P3/J, A/J, C57BL/6J, and DBA/2J). Citric acid taste thresholds were similar in these 4 strains. This suggests that our technique measures taste quality-specific thresholds that are likely to represent differences in peripheral taste responsiveness. The strain differences in NaCl taste sensitivity found in this study provide a basis for genetic analysis of this phenotype.

Phase-dependent associative learning in desert locusts

Phase-dependent associative learning in desert locusts

Host kairomone learning and foraging success in an egg parasitoid: a simulation model

Abstract 1. Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) is an egg parasitoid that recognises chemical residues left by its host the green stink bug Nezara viridula (L.) (Heteroptera: Pentatomidae) as kairomone signals, enabling it to find egg masses in which to lay eggs.2. Kairomones are usually present as patches deposited by N. viridula females, and recent results (Peri et al., Journal of Experimental Biology, 209, 3629–3635, 2006) indicated that females of T. basalis are able to learn the features of their foraging environment and to adjust accordingly the amount of time spent on the patches of kairomones they are visiting, depending on whether or not host eggs are found.3. In order to assess the impact of this learning ability, a Monte Carlo, spatially explicit and individual‐based simulation model was built to quantify the foraging efficiency of T. basalis females in environments with different levels of host abundance and distribution. In all cases, the present study compared the foraging efficiency of simulated T. basalis females having the ability to learn with those lacking this ability.4. Learning females always visited a higher number of kairomone patches and attacked a higher number of hosts than non‐learning females, especially when there was a high density of kairomone patches in the environment.5. Learning ability globally appears to allow the maintenance of efficient foraging success, especially when there is a low probability for the kairomone patches to contain discoverable hosts.6. The increase in foraging efficiency for learning females appears to depend on the characteristics of the habitat in which they are foraging. Results thus suggest that significant variation in learning ability is likely to occur in natural wasp populations facing different environments with different host spatial distributions.

A relation between maze performance and increased ethanol intake in Long–Evans rats

In addition to the neurochemical and genetic basis of high ethanol consumption, there has been renewed interest in studying the role of behavioral variables and their relation to ethanol consumption. The present study was designed to assess whether a relation exists between a behavioral variable such as maze learning ability and ethanol consumption. Sixty, male, Long–Evans rats, exposed to food and water ad libitum, were given a daily trial in a complex, 16-arm T-maze for 19 consecutive days. The number of errors and time to complete the maze were monitored. Individual maze variable scores were transformed and then combined to allot each animal with an index of overall maze performance, with a smaller maze index score denoting good performance. After completion of maze testing, animals were given alternate-day, free-choice presentations of water and ascending doses of ethanol solutions (2%–10%), followed by a 10-day maintenance period with 10% ethanol. Animals were subsequently separated into two groups of high and low drinkers to examine any relation between differential ethanol intake and maze performance. A significant negative correlation between maze index and ethanol intake for the high drinkers group indicated that a smaller maze index was related to increased ethanol intake. No significant correlation was obtained for the low drinkers group. These results seem to indicate that individual variation in learning ability seems to be related to increased ethanol intake. Thus, innate learning processes may be a relevant trait when one attempts to understand the behaviors related to ethanol intake and preference.

THE LEARNING ABILITIES OF BIRDS.

THE LEARNING ABILITIES OF BIRDS.