Taking a shortcut: what mechanisms do fish use?

Path integration is a powerful navigational mechanism whereby individuals continuously update their distance and angular vector of movement to calculate their position in relation to their departure location, allowing them to return along the most direct route even across unfamiliar terrain. While path integration has been investigated in several terrestrial animals, it has never been demonstrated in aquatic vertebrates, where movement occurs through volumetric space and sensory cues available for navigation are likely to differ substantially from those in terrestrial environments. By performing displacement experiments with Lamprologus ocellatus, we show evidence consistent with fish using path integration to navigate alongside other mechanisms (allothetic place cues and route recapitulation). These results indicate that the use of path integration is likely to be deeply rooted within the vertebrate phylogeny irrespective of the environment, and suggests that fish may possess a spatial encoding system that parallels that of mammals.

Distance estimation in the goldfish (Carassius auratus).

Neurophysiological advances have given us exciting insights into the systems responsible for spatial mapping in mammals. However, we are still lacking information on the evolution of these systems and whether the underlying mechanisms identified are universal across phyla, or specific to the species studied. Here we address these questions by exploring whether a species that is evolutionarily distant from mammals can perform a task central to mammalian spatial mapping-distance estimation. We developed a behavioural paradigm allowing us to test whether goldfish (Carassius auratus) can estimate distance and explored the behavioural mechanisms that underpin this ability. Fish were trained to swim a set distance within a narrow tank covered with a striped pattern. After changing the background pattern, we found that goldfish use the spatial frequency of their visual environment to estimate distance, doubling the spatial frequency of the background pattern resulted in a large overestimation of the swimming distance. We present robust evidence that goldfish can accurately estimate distance and show that they use local optic flow to do so. These results provide a compelling basis to use goldfish as a model system to interrogate the evolution of the mechanisms that underpin spatial cognition, from brain to behaviour.

High turbidity levels alter coral reef fish movement in a foraging task.

Sensory systems allow animals to detect and respond to stimuli in their environment and underlie all behaviour. However, human induced pollution is increasingly interfering with the functioning of these systems. Increased suspended sediment, or turbidity, in aquatic habitats reduces the reactive distance to visual signals and may therefore alter movement behaviour. Using a foraging task in which fish (Rhinecanthus aculeatus) had to find six food sites in an aquarium, we tested the impact of high turbidity (40-68 NTU; 154 mg/L) on foraging efficiency using a detailed and novel analysis of individual movements. High turbidity led to a significant decrease in task efficacy as fish took longer to begin searching and find food, and they travelled further whilst searching. Trajectory analyses revealed that routes were less efficient and that fish in high turbidity conditions were more likely to cover the same ground and search at a slower speed. These results were observed despite the experimental protocol allowing for the use of alternate sensory systems (e.g. olfaction, lateral line). Given that movement underlies fundamental behaviours including foraging, mating, and predator avoidance, a reduction in movement efficiency is likely to have a significant impact on the health and population dynamics of visually-guided fish species.

Archerfish vision: Visual challenges faced by a predator with a unique hunting technique.

Archerfish are well-known for their ballistic hunting behaviour, in which they shoot down aerial prey with a well-aimed jet of water. This unique hunting strategy poses several challenges for visual systems. Archerfish face significant distortion to the appearance of targets due to refraction at the air/water interface, they search for prey against a complex background of foliage, they change prey targeting behaviour as conditions change, and they must make high speed decisions to avoid competition. By studying how archerfish have overcome these challenges, we have been able to understand more about fundamental problems faced by visual systems and the mechanisms used to solve them. In some cases, such as when searching for targets, the visual capabilities of archerfish are functionally similar to those of humans, despite significant differences in neuroanatomy. In other cases, the particular challenge faced by archerfish magnifies fundamental problems generally faced by visual systems, such as recognizing objects given strong viewpoint dependent changes to appearance. The efficiency of archerfish retrieving fallen prey to avoid kleptoparasitism, demonstrates that their visual processing excels in both speed and accuracy. In this review, we attempt to provide an overview of the many facets of visually driven behaviour of archerfish, and how they have been studied. In addition to their hunting technique, archerfish are ideal for visual processing experiments as they can be quickly trained to perform a range of non-ecologically relevant tasks. Their behavioural flexibility moreover, introduces the opportunity to study how experience-dependence and choice affects visual processing.

Comparison of functional and anatomical estimations of visual acuity in two species of coral reef fish.

The high-contrast, complex patterns typical of many reef fish serve several purposes, including providing disruptive camouflage and a basis for vision-based communication. In trying to understand the role of a specific pattern, it is important to first assess the extent to which an observer can resolve the pattern, itself determined, at least in part, by the observer's visual acuity. Here, we studied the visual acuity of two species of reef fish - Pomacentrus amboinensis and Pseudochromis fuscus - using both anatomical and behavioural estimates. The two species share a common habitat but are members of different trophic levels (predator versus herbivore/omnivore) and perform different visual tasks. On the basis of the anatomical study, we estimated visual acuity to lie between 4.1 and 4.6 cycles deg-1 for P. amboinensis and 3.2 and 3.6 cycles deg-1 for P. fuscus Behavioural acuity estimates were considerably lower, ranging between 1.29 and 1.36 cycles deg-1 for P. amboinensis and 1.61 and 1.71 cycles deg-1 for P. fuscus Our results show that two species from the same habitat have only moderately divergent visual capabilities, despite differences in their general life histories. The difference between anatomical and behavioural estimates is an important finding as the majority of our current knowledge on the resolution capabilities of reef fish comes from anatomical measurements. Our findings suggest that anatomical estimates may represent the highest potential acuity of fish but are not indicative of actual performance, and that there is unlikely to be a simple scaling factor to link the two measures across all fish species.

Discrimination of human faces by archerfish (Toxotes chatareus).

Two rival theories of how humans recognize faces exist: (i) recognition is innate, relying on specialized neocortical circuitry, and (ii) recognition is a learned expertise, relying on general object recognition pathways. Here, we explore whether animals without a neocortex, can learn to recognize human faces. Human facial recognition has previously been demonstrated for birds, however they are now known to possess neocortex-like structures. Also, with much of the work done in domesticated pigeons, one cannot rule out the possibility that they have developed adaptations for human face recognition. Fish do not appear to possess neocortex-like cells, and given their lack of direct exposure to humans, are unlikely to have evolved any specialized capabilities for human facial recognition. Using a two-alternative forced-choice procedure, we show that archerfish (Toxotes chatareus) can learn to discriminate a large number of human face images (Experiment 1, 44 faces), even after controlling for colour, head-shape and brightness (Experiment 2, 18 faces). This study not only demonstrates that archerfish have impressive pattern discrimination abilities, but also provides evidence that a vertebrate lacking a neocortex and without an evolutionary prerogative to discriminate human faces, can nonetheless do so to a high degree of accuracy.

Same/Different Abstract Concept Learning by Archerfish (Toxotes chatareus).

While several phylogenetically diverse species have proved capable of learning abstract concepts, previous attempts to teach fish have been unsuccessful. In this report, the ability of archerfish (Toxotes chatareus) to learn the concepts of sameness and difference using a simultaneous two-item discrimination task was tested. Six archerfish were trained to either select a pair of same or different stimuli which were presented simultaneously. Training consisted of a 2-phase approach. Training phase 1: the symbols in the same and different pair did not change, thereby allowing the fish to solve the test through direct association. The fish were trained consecutively with four different sets of stimuli to familiarize them with the general procedure before moving on to the next training phase. Training phase 2: six different symbols were used to form the same or different pairs. After acquisition, same/different concept learning was tested by presenting fish with six novel stimuli (transfer test). Five fish successfully completed the first training phase. Only one individual passed the second training phase, however, transfer performance was consistent with chance. This individual was given further training using 60 training exemplars but the individual was unable to reach the training criterion. We hypothesize that archerfish are able to solve a limited version of the same/different test by learning the response to each possible stimulus configuration or by developing a series of relatively simple choice contingencies. We conclude that the simultaneous two-item discrimination task we describe cannot be successfully used to test the concepts of same and different in archerfish. In addition, despite considerable effort training archerfish using several tests and training methods, there is still no evidence that fish can learn an abstract concept-based test.

Concept learning and the use of three common psychophysical paradigms in the archerfish (Toxotes chatareus).

Archerfish are well known for their specialized hunting technique of spitting water at prey located above the water line. This unique ability has made them a popular focus of study as researchers try to understand the mechanisms involved in targeting and spitting. In more recent years, archerfish have also become an increasingly popular model for studying visual discrimination and learning in general. Until now, only the alternative forced-choice (AFC) task has been used with archerfish, however, they may be capable of learning other classical discrimination tasks. As well as providing alternative, and potentially more efficient, means for testing their visual capabilities, these other tasks may also provide deeper insight into the extent to which an organism with no cortex can grasp the concepts underlying these tasks. In this paper, we consider both the matched-to-sample (MTS) and the odd-one-out (OOO) tasks as they require the subject to learn relatively sophisticated concepts rather than a straight, stimulus-reward relationship, of the kind underlying AFC tasks. A variety of line drawings displayed on a monitor were used as stimuli. We first determined if archerfish could complete the MTS and OOO test and then evaluated their ability to be retrained to new stimuli using a 4-AFC test. We found that archerfish were unable to learn the MTS and had only a limited capacity for learning the OOO task. We conclude that the MTS and OOO are impractical as paradigms for behavioral experiments with archerfish. However, the archerfish could rapidly learn to complete an AFC test and select the conditioned stimulus with a high degree of accuracy when faced with four stimuli, making this a powerful test for behavioral studies testing visual discrimination. In addition, the fish were able to learn the concept of oddity under particular training circumstances. This paper adds to the growing evidence that animals without a cortex are capable of learning some higher order concepts.

Colour vision and response bias in a coral reef fish.

Animals use coloured signals for a variety of communication purposes, including to attract potential mates, recognize individuals, defend territories and warn predators of secondary defences (aposematism). To understand the mechanisms that drive the evolution and design of such visual signals, it is important to understand the visual systems and potential response biases of signal receivers. Here, we provide raw data on the spectral capabilities of a coral reef fish, the Picasso triggerfish Rhinecanthus aculeatus, which is potentially trichromatic with three cone sensitivities of 413 nm (single cone), 480 nm (double cone, medium sensitivity) and 528 nm (double cone, long sensitivity), and a rod sensitivity of 498 nm. The ocular media have a 50% transmission cut off at 405 nm. Behavioural experiments confirmed colour vision over their spectral range; triggerfish were significantly more likely to choose coloured stimuli over grey distractors, irrespective of luminance. We then examined whether response biases existed towards coloured and patterned stimuli to provide insight into how visual signals - in particular, aposematic colouration - may evolve. Triggerfish showed a preferential foraging response bias to red and green stimuli, in contrast to blue and yellow, irrespective of pattern. There was no response bias to patterned over monochromatic non-patterned stimuli. A foraging response bias towards red in fish differs from that of avian predators, who often avoid red food items. Red is frequently associated with warning colouration in terrestrial environments (ladybirds, snakes, frogs), whilst blue is used in aquatic environments (blue-ringed octopus, nudibranchs); whether the design of warning (aposematic) displays is a cause or consequence of response biases is unclear.