Use of water flow direction to provide spatial information in a small-scale orientation task

Experiments were designed to investigate whether three-spined sticklebacks Gasterosteus aculeatus can use direction of water flow as an orientation cue. The fish had to learn the location of a food patch in a channel where water flow direction was the only reliable indicator of the food patch position. Fish from two ponds and two rivers were trained and tested in the spatial task to determine whether river three-spined sticklebacks are more adept at using water flow as a spatial cue than fish from ponds. All fish were able to use water flow to locate the food patch but one of the two river groups was significantly faster at learning the patch location. When the task was reversed so that fish that had formerly been trained to swim downstream now had to learn to swim upstream and vice versa both river groups learned the reversed task faster than the two pond groups. In a second experiment, to investigate whether fish from ponds or rivers vary in the type of spatial cue that they prefer to use, fish from one pond and one river were given a choice between two different types of spatial cue: flow direction or visual landmarks. A test trial in which these two cues were put into conflict revealed that the river population showed a strong preference for flow direction whilst the pond population preferred to use visual landmarks.     

Influence of habitat complexity on route learning among different populations of climbing perch (Anabas testudineus Bloch, 1792)

Animals use different behavioral strategies to maximize their fitness in the natural environment. Learning and memory are critical in this context, allowing organisms to flexibly and rapidly respond to environmental changes. We studied how the physical characteristics of the native habitat influence the spatial learning capacity of Anabas testudineus belonging to four different populations collected from two streams and two ponds, in a linear maze. Stream fish were able to learn the route faster than pond fish irrespective of the presence or absence of landmarks in the maze. However, climbing perch collected from ponds learned the route faster in the maze provided with landmarks than in Plain maze. The results indicate that fish inhabiting a lotic ecosystem use egocentric cues in route learning rather than visual cues like landmarks. A local landmark may be a more reliable cue in route learning in a relatively stable habitat like a pond. In flowing aquatic systems, water flow may continually disrupt the visual landscape and thus landmarks as visual cues become unreliable. Spatial learning is thus a fine-tuned response to the complexity of the habitat and early rearing conditions may influence the spatial learning ability in fish.     

Learn and live: predator experience and feeding history determines prey behaviour and survival

Determining how prey learn the identity of predators and match their vigilance with current levels of threat is central to understanding the dynamics of predator–prey systems and the determinants of fitness. Our study explores how feeding history influences the relative importance of olfactory and visual sensory modes of learning, and how the experience gained through these sensory modes influences behaviour and survival in the field for a juvenile coral reef damselfish. We collected young fish immediately prior to their settlement to benthic habitats. In the laboratory, these predator-naïve fish were exposed to a high- or low-food ration and then conditioned to recognize the olfactory cues (odours) and/or visual cues from two common benthic predators. Fish were then allowed to settle on reefs in the field, and their behaviour and survival over 70 h were recorded. Feeding history strongly influenced their willingness to take risks in the natural environment. Conditioning in the laboratory with visual, olfactory or both cues from predators led fish in the field to display risk-averse behaviour compared with fish conditioned with sea water alone. Well-fed fish that were conditioned with visual, chemical or a combination of predator cues survived eight times better over the first 48 h on reefs than those with no experience of benthic predator cues. This experiment highlights the importance of a flexible and rapid mechanism of learning the identity of predators for survival of young fish during the critical life-history transition between pelagic and benthic habitats.     

Associative Learning of Color by Males of the Parasitoid Wasp Nasonia vitripennis (Hymenoptera: Pteromalidae)

Males of the parasitoid wasp Nasonia vitripennis showed no innate preference for blue versus yellow or for green versus brown. They learned to associate color with mates, but their ability to do so depended on the color used and the strength of the reward. Specifically, males learned to associate brown or green with a reward of many virgin females. With fewer females, fewer training periods, or mated females as the reward, males still learned a preference for green but not for brown. Males did not learn to associate color with rewards of honey or water. Previous studies of color preference and associative learning in parasitoid wasps have focused almost entirely on females. This is the first demonstration of associative learning in response to visual cues by male parasitoid wasps.     

Back to school: can antipredator behaviour in guppies be enhanced through social learning?

The ability to recognize and respond to predators often has a learned component, but few studies have examined the role of social learning in the development of antipredator behaviour. We investigated whether wild-caught juvenile guppies, Poecilia reticulata, from a low-predation river in Trinidad increase their response towards a novel predator through association with conspecifics from a high-predation river. We assigned fish to one of three treatment groups: (1) repeated exposure to a model accompanied by high-predation conspecifics; (2) repeated exposure to a model with low-predation conspecifics; (3) a control group in which focal fish interacted with high-predation fish in the absence of the model. Guppies trained with high-predation, but not low-predation, ‘demonstrators’ significantly improved their antipredator behaviour (spent more time schooling and inspected the model from further away). The guppies assigned to the control group showed no significant improvement in antipredator behaviour after the training period, suggesting that association with experienced conspecifics in the absence of the model is not sufficient to enhance the antipredator behaviour of na?ve fish. We conclude that guppies can improve their antipredator behaviour through association with more experienced conspecifics in the presence of visual cues simulating high predation risk. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.        

Microhabitat use affects goby (Gobiidae) cue choice in spatial learning task

This study investigated whether spatial learning ability and cue use of gobies (Gobiidae) from two contrasting habitats differed in a spatial task. Gobies were collected from the spatially complex rock pools and dynamic, homogenous sandy shores. Fishes were trained to locate a shelter under the simulated threat of predation and it was determined whether they used local or extra‐maze (global) and geometric cues to do so. It was hypothesized that fishes from rock pools would outperform fishes from sandy shores in their ability to relocate shelter and the two groups would differ in their cue use. It was found that rock‐pool species learnt the location of the correct shelter much faster, made fewer errors and used a combination of all available cues to locate the shelter, while sand species relied significantly more on extra‐maze and geometric cues for orientation. The results reported here support the hypothesis that fishes living in complex habitats have enhanced capacity for spatial learning and are more likely to rely on local landmarks as directional cues than fishes living in mundane habitats where local cues such as visual landmarks are unreliable.     

Amarillo Fish (Girardinichthys multiradiatus) Use Visual Landmarks to Orient in Space

Fish responsiveness to visual stimuli has been studied extensively in contexts such as female mate choice, predator inspection and schooling, yet surprisingly little work has been conducted on visual orientation in space in fish. Here we report on an experiment designed to test whether Amarillo fish can learn to find a goal within a maze more effectively in the presence of local visual landmarks than otherwise. We found that: (a) Amarillo fish can use landmarks to locate a goal, (b) there was no observed difference in the ability to use visual landmarks between two populations and (c) overall navigational performance differed between two populations of Amarillo fish: individuals from a permanently turbid eutrophic pond performed better than those from a pond with clear waters. We hypothesize that fish that inhabit clear waters possess poorer navigational capabilities than fish from turbid waters because they normally rely on goal‐oriented behaviour, which requires neither egocentric nor environmental clues to navigate. This paper adds to the literature on the links between habitat characteristics and population differences in performance.     

Landscape complexity influences route-memory formation in navigating pigeons

Observations of the flight paths of pigeons navigating from familiar locations have shown that these birds are able to learn and subsequently follow habitual routes home. It has been suggested that navigation along these routes is based on the recognition of memorized visual landmarks. Previous research has identified the effect of landmarks on flight path structure, and thus the locations of potentially salient sites. Pigeons have also been observed to be particularly attracted to strong linear features in the landscape, such as roads and rivers. However, a more general understanding of the specific characteristics of the landscape that facilitate route learning has remained out of reach. In this study, we identify landscape complexity as a key predictor of the fidelity to the habitual route, and thus conclude that pigeons form route memories most strongly in regions where the landscape complexity is neither too great nor too low. Our results imply that pigeons process their visual environment on a characteristic spatial scale while navigating and can explain the different degrees of success in reproducing route learning in different geographical locations.     

The Computational Development of Reinforcement Learning during Adolescence

Adolescence is a period of life characterised by changes in learning and decision-making. Learning and decision-making do not rely on a unitary system, but instead require the coordination of different cognitive processes that can be mathematically formalised as dissociable computational modules. Here, we aimed to trace the developmental time-course of the computational modules responsible for learning from reward or punishment, and learning from counterfactual feedback. Adolescents and adults carried out a novel reinforcement learning paradigm in which participants learned the association between cues and probabilistic outcomes, where the outcomes differed in valence (reward versus punishment) and feedback was either partial or complete (either the outcome of the chosen option only, or the outcomes of both the chosen and unchosen option, were displayed). Computational strategies changed during development: whereas adolescents’ behaviour was better explained by a basic reinforcement learning algorithm, adults’ behaviour integrated increasingly complex computational features, namely a counterfactual learning module (enabling enhanced performance in the presence of complete feedback) and a value contextualisation module (enabling symmetrical reward and punishment learning). Unlike adults, adolescent performance did not benefit from counterfactual (complete) feedback. In addition, while adults learned symmetrically from both reward and punishment, adolescents learned from reward but were less likely to learn from punishment. This tendency to rely on rewards and not to consider alternative consequences of actions might contribute to our understanding of decision-making in adolescence.     

Ocean acidification boosts larval fish development but reduces the window of opportunity for successful settlement

Locating appropriate settlement habitat is a crucial step in the life cycle of most benthic marine animals. In marine fish, this step involves the use of multiple senses, including audition, olfaction and vision. To date, most investigations of larval fish audition focus on the hearing thresholds to various frequencies of sounds without testing an ecological response to such sounds. Identifying responses to biologically relevant sounds at the development stage in which orientation is most relevant is fundamental. We tested for the existence of ontogenetic windows of reception to sounds that could act as orientation cues with a focus on vulnerability to alteration by human impacts. Here we show that larvae of a catadromous fish species (barramundi, Lates calcarifer) were attracted towards sounds from settlement habitat during a surprisingly short ontogenetic window of approximately 3 days. Yet, this auditory preference was reversed in larvae reared under end-of-century levels of elevated CO₂, such that larvae are repelled from cues of settlement habitat. These future conditions also reduced the swimming speeds and heightened the anxiety levels of barramundi. Unexpectedly, an acceleration of development and onset of metamorphosis caused by elevated CO₂ were not accompanied by the earlier onset of attraction towards habitat sounds. This mismatch between ontogenetic development and the timing of orientation behaviour may reduce the ability of larvae to locate habitat or lead to settlement in unsuitable habitats. The misinterpretation of key orientation cues can have implications for population replenishment, which are only exacerbated when ontogenetic development decouples from the specific behaviours required for location of settlement habitats.     

Learned orientation in landward swimming in the cricket Pteronemobius Lineolatus

Pteronemobius lineolatus swims landward visually guided by terrestrial and, at times, associated celestial cues.Crickets irrespective of their previous visual experience swim towards artificial black horizontal landmarks. Non shore-dwelling crickets select random directions when released, under blue sky, for the first time on water surface in the absence of landmarks. If old enough to swim larvae and adult crickets learn a compass direction, during their first swim and each new directional landward swimming, if there are conspicuous terrestrial landmarks.There is forgetting and relearning of celestial compass orientation.     

Social learning of predators in the dark: understanding the role of visual,chemical and mechanical information

The ability of prey to observe and learn to recognize potential predators from the behaviour of nearby individuals can dramatically increase survival and, not surprisingly, is widespread across animal taxa. A range of sensory modalities are available for this learning, with visual and chemical cues being well-established modes of transmission in aquatic systems. The use of other sensory cues in mediating social learning in fishes, including mechano-sensory cues, remains unexplored. Here, we examine the role of different sensory cues in social learning of predator recognition, using juvenile damselfish (Amphiprion percula). Specifically, we show that a predator-naive observer can socially learn to recognize a novel predator when paired with a predator-experienced conspecific in total darkness. Furthermore, this study demonstrates that when threatened, individuals release chemical cues (known as disturbance cues) into the water. These cues induce an anti-predator response in nearby individuals; however, they do not facilitate learnt recognition of the predator. As such, another sensory modality, probably mechano-sensory in origin, is responsible for information transfer in the dark. This study highlights the diversity of sensory cues used by coral reef fishes in a social learning context.     

Eye-specific learning of routes and “signposts” by walking honeybees

This study investigates the honeybee's ability to learn routes based on visual stimuli presented to a single eye, and to then navigate these routes using the other (naive) eye. Bees were trained to walk through a narrow tunnel carrying visual stimuli on the two walls. At the end of the tunnel the bees had to choose between two arms, one of which led to a feeder. In a first experiment, bees had to learn to choose the left arm to get a reward when the right wall carried a yellow grating, but the right arm when the left wall carried a blue grating. The bees learned this task well, indicating that stimuli encountered by different eyes could be associated with different routes. In a second experiment, bees had to turn left when the right eye saw a blue grating, but to the right when the same eye saw a yellow grating. They also learned this task well. In subsequent tests, they chose the correct arm even when these gratings were presented to the untrained eye. These results suggest that there is interocular transfer of route-specific learning with respect to visual stimuli that function as navigational “signposts”. Accepted: 18 December 1997     

Ground-nesting bees determine the location of their nest relative to a landmark by other than angular size cues

Bees and wasps acquire a visual representation of their nest's environment and use it to locate their nest when they return from foraging trips. This representation contains among other features cues to the distance of near-by landmarks. We worked with two species of ground-nesting bees, Lasioglossum malachurum (Hymenoptera: Halictidae), Dasypoda hirtipes (Hymenoptera: Melittidae) and asked which cues to landmark distance they use during homing. Bees learned to associate a single cylindrical landmark with their nest's location. We subsequently tested returning bees with landmarks of different sizes and thus introduced large discrepancies between the angular size of the landmark as seen from the nest during training and its distance from the nest. The bees' search behaviour and their choice of dummy nest entrances show that both species of ground-nesting bees consistently search for their nest at the learned distance from landmarks. The influence of the apparent size of landmarks on the bees' search and choice behaviour is comparatively weak. We suggest that the bees exploit cues derived from the apparent speed of the landmark's image at their retina for distance evaluation.     

Visual marks learned by the solitary bee Megachile rotundata for localizing its nest

We studied homing behaviour of leaf-cutter bees, Megachile rotundata, by using artificial landmarks. We evaluated their nest-searching behaviour in different test situations to elucidate the nature of the visual marks they used in this task. When we modified or removed geometrical figures surrounding the nest, the bees searched for longer, showing that they noticed the introduced changes. However, these manipulations never prevented bees from finding their nest, suggesting that other visual cues were crucial in the task. Manipulations of the edges provided by the boundaries of the device (nest block, metal sheet on which the block was mounted) strongly impaired the homing performance. The further away the edges that were left intact, the stronger was the impairment of the homing behaviour. These results suggest that bees learn the distances of the various edges from the goal and that edges have a hierarchical significance according to their distance from the nest. The most distant edges provide vague information, which suffices to guide the insect towards the next edge in the sequence, until it recognizes the final, precise location of the nest. The results support the conclusion that information on distances is acquired using cues derived from motion parallax generated by the insect's self-motion. Recognition of edge parameters such as position and orientation might be achieved by an image-matching mechanism based on dynamic processes. Thus, in the homing task, there is no clear discrepancy between the eidetic and the parametric hypotheses of spatial representation.     

Smell, learn and live: The role of chemical alarm cues in predator learning during early life history in a marine fish

The speed with which individuals can learn to identify and react appropriately to predation threats when transitioning to new life history stages and habitats will influence their survival. This study investigated the role of chemical alarm cues in both anti-predator responses and predator identification during a transitional period in a newly settled coral reef damselfish, Pomacentrus amboinensis. Individuals were tested for changes in seven behavioural traits in response to conspecific and heterospecific skin extracts. Additionally, we tested whether fish could learn to associate a previously novel chemical cue (i.e. simulated predator scent) with danger, after previously being exposed to a paired cue combining the conspecific skin extract with the novel scent. Fish exposed to conspecific skin extracts were found to significantly decreased their feeding rate whilst those exposed to heterospecific and control cues showed no change. Individuals were also able to associate a previously novel scent with danger after only a single previous exposure to the paired conspecific skin extract/novel scent cue. Our results indicate that chemical alarm cues play a large role in both threat detection and learned predator recognition during the early post-settlement period in coral reef fishes.     

Discrimination reversal learning reveals greater female behavioural flexibility in guppies

Behavioural flexibility allows an animal to adapt its behaviour in response to changes in the environment. Research conducted in primates, rodents and domestic fowl suggests greater behavioural persistence and reduced behavioural flexibility in males. We investigated sex differences in behavioural flexibility in fish by comparing male and female guppies (Poecilia reticulata) in a reversal learning task. Fish were first trained on a colour discrimination, which was learned equally rapidly by males and females. However, once the reward contingency was reversed, females were better at inhibiting the previous response and reached criterion twice as fast as males. When reward reversing was repeated, males gradually reduced the number of errors, and the two sexes had a comparable performance after four reversals. We suggest that sex differences in behavioural flexibility in guppies can be explained in terms of the different roles that males and females play in reproduction.     

Cognitive aspects of food searching behavior in free-ranging wild Common Carp

Although laboratory experiments have shown that many fishes, Goldfish (Carassius auratus) in particular, employ relatively sophisticated orientation strategies to learn the location of food in laboratory arenas, this ability has not been rigorously tested in the natural environment. In this study we documented the ability of Common Carp (Cyprinus carpio), a close relative of Goldfish, to learn the location of newly introduced food in a lake. Two experiments were conducted, the first of which determined that carp feed largely at night. The second used this information and tracked the day- and night-time locations of 34 radio-tagged carp before and then while a food reward was introduced at a specific location in the lake for 10 days. Before the introduction of the reward, carp maintained small (∼100 m × 70 m), isolated home ranges which expanded slightly at night. This movement pattern changed after the reward was added when on the fourth night six radiotagged carp visited and exploited the reward and then returned to their home areas after sunrise. This pattern persisted for the rest of the experiment with increasing numbers of carp visiting the reward each night (21 of 34 carp visited on the tenth night) and returning to their home ranges each day. The speed and precision with which wild carp learned to exploit this reward is consistent with the social learning and spatial memory skills that they and their relatives have shown in laboratory arenas. This is particularly impressive given the turbid conditions in the lake and the lack of obvious visual landmarks.     

The turn-back-and-look behaviour: bee versus robot

 Honeybees and social wasps departing from a novel food source perform stereotype flight manoeuvres, termed the turn-back-and-look behaviour (TBL). Based on results of behavioural studies, it is proposed that the image motion generated by the TBL provides the insect with information about the three-dimensional structure of the goal's surroundings, thus enabling it to select reliable landmarks that will guide it to the goal upon return. The colour, shape, and size of landmarks, on the other hand, are learned mainly during arrival at the food source. However, when bees are prevented from learning these cues on arrival, they learn them during the TBL, despite the fact that this performance does not require the use of image motion. A recently developed model shows that landmark learning can indeed be accomplished during the TBL by exploiting cues others than image motion. A mobile robot equipped with the appropriate software selects, during the TBL, reliable marks and returns to the site of departure from different locations by accomplishing image matching along a two-dimensional vector field. Received: 7 May 1999 / Accepted in revised form: 20 March 2000     

Short-range orientation in fish: How fish map space

One way in which fish can move around efficiently is to learn and remember a spatial map of their environment. This can be a relatively simple process where, for example, sequences of landmarks are learned. However, more complex spatial representations can be generated by integrating multiple pieces of information. In this review, we consider what types of information fish use to generate a spatial map; for instance, beacons (single landmarks) that signal a specific location, or learned geometric relationships between multiple landmarks that allow fish to guide their movements. Owing to the diversity of fish species and the broad range of environments that they inhabit, there is considerable diversity in the maps that they develop and the sensory systems that they use to detect spatial information. This chapter uses a series of examples to investigate the types of spatial information that fish encode, for instance, how they map three-dimensional space, how they make use of different sensory modalities, and where this information might be processed. We also highlight the versatility of short-range orientation in fish, and discuss a number of similarities between the mapping mechanisms used by fish and terrestrial vertebrates.