The influence of habitat stability on landmark use during spatial learning in the three-spined stickleback

The capacity to learn enables animals to match their phenotypic response to a changing environment on the basis of experience but learning is likely to incur costs such as the cost of making mistakes or the energetic cost of processing information. Little is known about how animals optimize the use of learned behaviour within their natural environments such that potential costs are minimized. We investigated whether the use of local landmarks in learning orientation routes by the three-spined stickleback, Gasterosteus aculeatus, varied in response to the visual stability of their natural habitats. Sticklebacks collected from five fast-flowing rivers and five ponds were trained to locate a hidden reward in a T-maze. Locating the reward required the fish to learn a body-centred algorithmic behaviour (turn left or right) or to follow plant landmarks. Probe trials, in which these cues conflicted, revealed which spatial cue the fish was using. Pond fish appeared to rely more than river fish on visual landmarks, which is consistent with the suggestion that even within a species, learned behaviour is fine-tuned in response to local environmental conditions. Landmarks may be reliable indicators of location only in stable pond habitats. In rivers, turbulence and flow may continually disrupt the visual landscape such that river fish may benefit from learning orientation routes only if learning is constrained so that unreliable visual cues are ignored. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Prenatal learning in an Australian songbird: habituation and individual discrimination in superb fairy-wren embryos

Embryos were traditionally considered to possess limited learning abilities because of the immaturity of their developing brains. By contrast, neonates from diverse species show behaviours dependent on prior embryonic experience. Stimulus discrimination is a key component of learning and has been shown by a handful of studies in non-human embryos. Superb fairy-wren embryos (Malurus cyaneus) learn a vocal password that has been taught to them by the attending female during incubation. The fairy-wren embryos use the learned element as their begging call after hatching to solicit more parental feeding. In this study, we test whether superb fairy-wren embryos have the capacity to discriminate between acoustical stimuli and whether they show non-associative learning. We measured embryonic heart rate response using a habituation/dishabituation paradigm with eggs sourced from nests in the wild. Fairy-wren embryos lowered their heart rate in response to the broadcasts of conspecific versus heterospecific calls, and in response to the calls of novel conspecific individuals. Thus, fairy-wrens join humans as vocal-learning species with known prenatal learning and individual discrimination.     

High stimulus specificity characterizes anti-predator habituation under natural conditions

Habituation is one of the most fundamental learning processes that allow animals to adapt to dynamic environments. It is ubiquitous and often thought of as a simple form of non-associative learning. Very little is known, though, about the rules that govern habituation and their significance under natural conditions. Questions about how animals incorporate habituation into their daily behaviour and how they can assure only to habituate to non-relevant stimuli are still unanswered. Animals under threat of predation should be particularly selective about which stimuli they habituate to, since ignoring a real threat could be fatal. In this study, we tested the response of fiddler crabs, Uca vomeris, to repeatedly approaching dummy predators to find out whether these animals habituate to potential predators and to test the selectivity of the habituation process. The crabs habituated to model predators, even though they were confronted with real predators during the same habituation process. They showed remarkable selectivity towards the stimulus: a simple change in the approach distance of the stimulus led to a recovery in their responses. The results strongly indicate that in the context of predator avoidance, habituation under natural conditions is highly selective and a stimulus is not defined just by its current sensory signature, but also its spatio-temporal history.     

A natural genetic polymorphism affects retroactive interference in Drosophila melanogaster

As environments change, animals update their internal representations of the external world. New information about the environment is learned and retained whereas outdated information is disregarded or forgotten. Retroactive interference (RI) occurs when the retrieval of previously learned information is less available owing to the acquisition of recently acquired information. Even though RI is thought to be a major cause of forgetting, its functional significance is still under debate. We find that natural allelic variants of the Drosophila melanogaster foraging gene known to affect rover and sitter behaviour differ in RI. More specifically, rovers who were previously shown to experience greater environmental heterogeneity while foraging display RI whereas sitters do not. Rover responses are biased towards more recent learning events. These results provide an ecological context to investigate the function of forgetting via RI and a suitable genetic model organism to address the evolutionary relevance of cognitive tasks.     

Foraging Ecology Predicts Learning Performance in Insectivorous Bats

Bats are unusual among mammals in showing great ecological diversity even among closely related species and are thus well suited for studies of adaptation to the ecological background. Here we investigate whether behavioral flexibility and simple- and complex-rule learning performance can be predicted by foraging ecology. We predict faster learning and higher flexibility in animals hunting in more complex, variable environments than in animals hunting in more simple, stable environments. To test this hypothesis, we studied three closely related insectivorous European bat species of the genus Myotis that belong to three different functional groups based on foraging habitats: M. capaccinii, an open water forager, M. myotis, a passive listening gleaner, and M. emarginatus, a clutter specialist. We predicted that M. capaccinii would show the least flexibility and slowest learning reflecting its relatively unstructured foraging habitat and the stereotypy of its natural foraging behavior, while the other two species would show greater flexibility and more rapid learning reflecting the complexity of their natural foraging tasks. We used a purposefully unnatural and thus species-fair crawling maze to test simple- and complex-rule learning, flexibility and re-learning performance. We found that M. capaccinii learned a simple rule as fast as the other species, but was slower in complex rule learning and was less flexible in response to changes in reward location. We found no differences in re-learning ability among species. Our results corroborate the hypothesis that animals’ cognitive skills reflect the demands of their ecological niche.     

Honeybees can discriminate between Monet and Picasso paintings

Honeybees (Apis mellifera) have remarkable visual learning and discrimination abilities that extend beyond learning simple colours, shapes or patterns. They can discriminate landscape scenes, types of flowers, and even human faces. This suggests that in spite of their small brain, honeybees have a highly developed capacity for processing complex visual information, comparable in many respects to vertebrates. Here, we investigated whether this capacity extends to complex images that humans distinguish on the basis of artistic style: Impressionist paintings by Monet and Cubist paintings by Picasso. We show that honeybees learned to simultaneously discriminate between five different Monet and Picasso paintings, and that they do not rely on luminance, colour, or spatial frequency information for discrimination. When presented with novel paintings of the same style, the bees even demonstrated some ability to generalize. This suggests that honeybees are able to discriminate Monet paintings from Picasso ones by extracting and learning the characteristic visual information inherent in each painting style. Our study further suggests that discrimination of artistic styles is not a higher cognitive function that is unique to humans, but simply due to the capacity of animals—from insects to humans—to extract and categorize the visual characteristics of complex images.     

Social learning of fear and safety is determined by the demonstrator's racial group

Social learning offers an efficient route through which humans and other animals learn about potential dangers in the environment. Such learning inherently relies on the transmission of social information and should imply selectivity in what to learn from whom. Here, we conducted two observational learning experiments to assess how humans learn about danger and safety from members (‘demonstrators'') of an other social group than their own. We show that both fear and safety learning from a racial in-group demonstrator was more potent than learning from a racial out-group demonstrator.     

Early Olfactory Environment Influences Social Behaviour in Adult Octodon degus

We evaluated the extent to which manipulation of early olfactory environment can influence social behaviours in the South American Hystricognath rodent Octodon degus. The early olfactory environment of newborn degus was manipulated by scenting all litter members with eucalyptol during the first month of life. The social behaviour of sexually mature animals (5–7 months old) towards conspecifics was then assessed using a y-maze to compare the response of control (naïve) and treated animals to two different olfactory configurations (experiment 1): (i) a non-familiarized conspecific impregnated with eucalyptol (eucalyptol arm) presented against (ii) a non-familiarized unscented conspecific (control arm). In addition, in dyadic encounters, we assessed the behaviour of control and eucalyptol treated animals towards a non-familiarized conspecific scented with eucalyptol (experiment 2). We found that control subjects explored and spent significantly less time in the eucalyptol arm, indicating neophobic behaviours towards the artificially scented conspecific. Treated subjects explored and spent similar time in both arms of the maze, showing the same interest for both olfactory stimuli presented. During dyadic encounters in experiment 2, an interaction effect between early experience and sex was observed. Control males escaped and avoided their scented partner more frequently than eucalyptol treated male subjects and than females. Both groups did not differ in the exploration of their scented partners, suggesting that avoidance within agonistic context does not relate to neophobic behaviours. Our results suggest that the exposure to eucalyptol during early ontogeny decreases evasive behaviours within an agonistic context as a result of olfactory learning. Altogether, these results indicate that olfactory cues learned in early ontogeny can influence olfactory-guided behaviours in adult degus.     

Task Specialization and Odor Effects on Proboscis Extension Conditioning in Bumblebees (Bombus huntii)

Workers in a social insect colony have distinct experiences that may affect their performance in a learning task. In this study using free-foraging and flight-cage bumblebee Bombus huntii colonies, the strength of olfactory proboscis extension conditioning (PEC) was affected by a bee’s task specialization as a nurse or forager and the stimulus odor. Nurses (n?=?26) learned to respond to the odors 1-hexanol and lavender, but foragers (n?=?25) had inhibited conditioning to both odors. More nurses (73 %) than foragers (48 %) had at least one conditioned response (CR), and nurses displayed significantly more CRs than foragers. As expected, a pseudoconditioned control group (n?=?9) showed very few CRs. Among bees that were given a second day of trials, nurses—but not foragers—showed modest improvement. Such strong inhibition of PEC has not been described in honeybee or bumblebee foragers. The stimulus odor also affected conditioning strength in nurses. Lavender, a familiar odor, elicited earlier and more CRs than 1-hexanol. We propose that learning floral odors in the context of foraging may inhibit PEC in bumblebee foragers, whereas exposure to odors in the honey stores may prime subsequent learning in nurses.     

Drosophila rely on learning while foraging under semi‐natural conditions

Learning is predicted to affect manifold ecological and evolutionary processes, but the extent to which animals rely on learning in nature remains poorly known, especially for short‐lived non‐social invertebrates. This is in particular the case for Drosophila, a favourite laboratory system to study molecular mechanisms of learning. Here we tested whether Drosophila melanogaster use learned information to choose food while free‐flying in a large greenhouse emulating the natural environment. In a series of experiments flies were first given an opportunity to learn which of two food odours was associated with good versus unpalatable taste; subsequently, their preference for the two odours was assessed with olfactory traps set up in the greenhouse. Flies that had experienced palatable apple‐flavoured food and unpalatable orange‐flavoured food were more likely to be attracted to the odour of apple than flies with the opposite experience. This was true both when the flies first learned in the laboratory and were then released and recaptured in the greenhouse, and when the learning occurred under free‐flying conditions in the greenhouse. Furthermore, flies retained the memory of their experience while exploring the greenhouse overnight in the absence of focal odours, pointing to the involvement of consolidated memory. These results support the notion that even small, short lived insects which are not central‐place foragers make use of learned cues in their natural environments.     

Self-imposed food deprivation and wheel-running activity in field-trapped Norway rats as a function of environmental change,time in captivity and age at capture

The tendency of juvenile and adult field-trapped Norway rats (Rattus norvegicus) to exhibit self-induced food deprivation in response to changes in their living environment was studied after different periods of residency in the laboratory environment. Self-imposed food deprivation resulting from the forced occupation of a novel environment (activity wheels) was greater for those animals tested immediately upon capture and after 25 weeks in captivity than for rats in captivity for 4 weeks. The deprivation response of juveniles was less than for adults immediately following capture but after 25 weeks in captivity the responses of the two age groups were similar. Deprivation responses following reintroduction to the home cage environment diminished over time in captivity. Wheel-running by adults was greatest immediately following capture whereas juveniles continued to show relatively high levels of wheel-running at 4 weeks in captivity. The results are discussed in terms of habituation to the laboratory environment and time-dependent changes in response to novelty.     

Signaling via the FLP-14/FRPR-19 neuropeptide pathway sustains nociceptive response to repeated noxious stimuli in C. elegans

In order to thrive in constantly changing environments, animals must adaptively respond to threatening events. Noxious stimuli are not only processed according to their absolute intensity, but also to their context. Adaptation processes can cause animals to habituate at different rates and degrees in response to permanent or repeated stimuli. Here, we used a forward genetic approach in Caenorhabditis elegans to identify a neuropeptidergic pathway, essential to prevent fast habituation and maintain robust withdrawal responses to repeated noxious stimuli. This pathway involves the FRPR-19A and FRPR-19B G-protein coupled receptor isoforms produced from the frpr-19 gene by alternative splicing. Loss or overexpression of each or both isoforms can impair withdrawal responses caused by the optogenetic activation of the polymodal FLP nociceptor neuron. Furthermore, we identified FLP-8 and FLP-14 as FRPR-19 ligands in vitro. flp-14, but not flp-8, was essential to promote withdrawal response and is part of the same genetic pathway as frpr-19 in vivo. Expression and cell-specific rescue analyses suggest that FRPR-19 acts both in the FLP nociceptive neurons and downstream interneurons, whereas FLP-14 acts from interneurons. Importantly, genetic impairment of the FLP-14/FRPR-19 pathway accelerated the habituation to repeated FLP-specific optogenetic activation, as well as to repeated noxious heat and harsh touch stimuli. Collectively, our data suggest that well-adjusted neuromodulation via the FLP-14/FRPR-19 pathway contributes to promote nociceptive signals in C. elegans and counteracts habituation processes that otherwise tend to rapidly reduce aversive responses to repeated noxious stimuli.     

Habituation of medaka (Oryzias latipes) demonstrated by open-field testing

Habituation to novel environments is frequently studied to analyze cognitive phenotypes in animals, and an open-field test is generally conducted to investigate the changes that occur in animals during habituation. The test has not been used in behavioral studies of medaka (Oryzias latipes), which is recently being used in behavioral research. Therefore, we examined the open-field behavior of medaka on the basis of temporal changes in 2 conventional indexes of locomotion and position. The findings of our study clearly showed that medaka changed its behavior through multiple temporal phases as it became more familiar with new surroundings; this finding is consistent with those of other ethological studies in animals. During repeated open-field testing on 2 consecutive days, we observed that horizontal locomotion on the second day was less than that on the first day, which suggested that habituation is retained in fish for days. This temporal habituation was critically affected by water factors or visual cues of the tank, thereby suggesting that fish have spatial memory of their surroundings. Thus, the data from this study will afford useful fundamental information for behavioral phenotyping of medaka and for elucidating cognitive phenotypes in animals.     

The adaptive significance of avian mobbing. III. Cultural transmission of enemy recognition in blackbirds: Cross-species tutoring and properties of learning

Taped conspecific and alien species mobbing calls suffice to transmit enemy recognition of a conditioned object CS to European blackbirds (Turdus merula), though their reinforcing effect is probably less than that of a real blackbird mobber. Blackbirds habituated to the CS learn to mob it in the latter case without impairment, but fail completely if taped conspecific mobbing calls serve as the reinforcer. Mobbing performance of the learner during learning peaks significantly later with a weak CS than with a strong CS. A general mobbing motivation, as measured by mobbing performance over many episodes, is typical for each individual: i.e. responses correlate intra-individually over a wide range of different compound stimuli. A more specific motivation accompanying enemy stimulus learning weakens these inter-response relationships and enhances performance of the learned response; the learned response correlates more strongly with the response during learning than with any other preceding response. This suggests that a specific motivation during engram formation has reinforcing properties. As revealed by multiple regression analysis, all three mobbing elements scored exert their learning-enhancing effect by a strictly intra-element facilitation.     

The Influence of Learning on Host Plant Preference in a Significant Phytopathogen Vector,Diaphorina citri

Although specialist herbivorous insects are guided by innate responses to host plant cues, host plant preference may be influenced by experience and is not dictated by instinct alone. The effect of learning on host plant preference was examined in the Asian citrus psyllid, Diaphorina citri; vector of the causal agent of citrus greening disease or huanglongbing. We investigated: a) whether development on specific host plant species influenced host plant preference in mature D. citri; and b) the extent of associative learning in D. citri in the form of simple and compound conditioning. Learning was measured by cue selection in a 2-choice behavioral assay and compared to naïve controls. Our results showed that learned responses in D. citri are complex and diverse. The developmental host plant species influenced adult host plant preference, with female psyllids preferring the species on which they were reared. However, such preferences were subject to change with the introduction of an alternative host plant within 24–48 hrs, indicating a large degree of experience-dependent response plasticity. Additionally, learning occurred for multiple sensory modalities where novel olfactory and visual environmental cues were associated with the host plant. However, males and females displayed differing discriminatory abilities. In compound conditioning tasks, males exhibited recognition of a compound stimulus alone while females were capable of learning the individual components. These findings suggest D. citri are dynamic animals that demonstrate host plant preference based on developmental and adult experience and can learn to recognize olfactory and visual host plant stimuli in ways that may be sex specific. These experience-based associations are likely used by adults to locate and select suitable host plants for feeding and reproduction and may suggest the need for more tailored lures and traps, which reflect region-specific cultivars or predominate Rutaceae in the area being monitored.     

Food Neophobia and Social Learning Opportunities in Great Apes

Finding food resources and maintaining a balanced diet are major concerns for all animals. A compromise between neophobia and neophilia is hypothesised to enable animals to enlarge their diet while limiting the risk of poisoning. However, little is known about how primates respond to novel food items and whether their use is socially transmitted. By comparing how four different species of great apes respond to novel food items, we investigated how differences in physiology (digestive tract size and microbial content), habitats (predictability of food availability), and social systems (group size and composition) affect their response toward novelty. We presented two familiar foods, one novel fruit, four novel aromatic plants from herbal medicine, and kaolin to captive chimpanzees (Pan troglodytes), western gorillas (Gorilla gorilla), Bornean orangutans (Pongo pygmaeus) and Sumatran orangutans (Pongo abelii). We recorded smelling, approach-taste delays, ingestion, interindividual observations, and food transfers with continuous sampling. We found that behaviors differed between the apes: chimpanzees were the most cautious species and observed their conspecifics handling the items more frequently than the other apes. Close observations and food transfers were extremely rare in gorillas in comparison to orangutans and chimpanzees. We suggest that a low neophobia level reflects an adaptive response to digestive physiological features in gorillas and to unpredictable food availability in orangutans. Social interactions appeared to be predominant in chimpanzees and in both orangutan species to overcome food neophobia. They reflect higher social tolerance and more opportunities for social learning and cultural transmission in a feeding context.     

植食性昆虫的学习行为

学习是指因经历不同而导致的行为变化。在植食性昆虫中,学习主要包含习惯性反应、厌恶性学习、联系性学习、敏感性反应和嗜好性诱导等类型。昆虫在幼虫和成虫期都具有学习能力,但幼虫期食料和取食经历不会对成虫行为产生直接影响。昆虫学习行为的表现受其本身食性、寄主刺激物的类别及寄主植物时空分布动态等因子的影响。学习能力有助于植食性昆虫应对复杂多变的植物环境,提高对寄主植物的利用效率,有利于其生存繁衍。对害虫学习行为的了解可为栖境调控、行为调控等害虫治理方法提供重要     

Colour biases in learned foraging preferences in Trinidadian guppies

Learning allows animals to adaptively adjust their behaviour in response to variable but predictable environments. Stable aspects of the environment may result in evolved or developmental biases in the systems impacting learning, allowing for improved learning performance according to local ecological conditions. Guppies (Poecilia reticulata), like many animals, show striking colour preferences in foraging and mating contexts and guppy artificial selection experiments have found that the form and progress of evolved responses to coloured stimuli differ depending on stimulus colour. Blue colouration is thought to typically be a relatively unimportant food cue in guppies. This raises the possibility that learned foraging associations with blue objects are formed less readily than with other colours. Here, guppies were rewarded for foraging at green or blue objects in two experiments. Guppies readily foraged from these objects, but learning performance differed with rewarded object colour. With equal amounts of training, the preference for green objects became stronger than the preference for blue objects. These differences in performance were not attributable to differences in initial preferences or to foraging more on one colour during training. These findings suggest that associative pairings within a single sensory modality that do not have a historic relevancy can be more difficult for animals to learn even when there is no clear initial bias present.