Laterality Influences Schooling Position in Rainbowfish,Melanotaenia spp

Cerebral lateralization is a widespread trait among animals, is often manifested as side biases in behaviour (laterality) and has been suggested to provide fitness benefits. Here we examined the influence of laterality on the organisation of fish schools using rainbowfish (Melanotaenia spp) as model species. The pattern and strength of laterality for each individual was determined by examining eye preferences whilst examining their reflection in a mirror. Schools of four fish of known laterality were then created and the preferred position for each fish within the school was repeatedly observed in a flume. Fish which showed right eye preferences in the mirror test preferentially adopted a position on the left side of the school. Conversely, fish that showed left eye preferences in the mirror test or where non-lateralised preferentially adopted a position slightly to the right side of the school. However, this general pattern varied depending on the species and sex of the school. Our results strongly implicate individual laterality in the geometry of school formation.     

Lateralization of lateral displays in convict cichlids

We examine lateralization of lateral displays in convict cichlids, Amatitlania nigrofasciata, and show a population level preference for showing the right side. This enables contesting pairs of fish to align in a head-to-tail posture, facilitating other activities. We found individuals spent a shorter mean time in each left compared with each right lateral display. This lateralization could lead to contesting pairs using a convention to align in a predictable head-to-tail arrangement to facilitate the assessment of fighting ability. It has major implications for the common use of mirror images to study fish aggression, because the 'opponent' would never cooperate and would consistently show the incorrect side when the real fish shows the correct side. With the mirror, the 'normal' head-to-tail orientation cannot be achieved.     

Differences in Timidity and Escape Responses between Predator-naive and Predator-sympatric Rainbowfish Populations

Responses of rainbowfish ( Melanotaenia duboulayi ) from two populations towards a) an active and a passive predatory fish and b) a novel trawl apparatus, were compared. Predator-sympatric fish avoided the fish predators and showed stronger avoidance behaviour in response to the active predator. These fish used predator inspection excursions to rapidly assess the potential risk and their escape responses were consistently effective. In contrast the predator-naive fish ignored the passive predator but were continually drawn towards the active predator possibly due to generalized curiosity and the absence of significant negative feedback from the predator, which was restrained by a clear Perspex partition. Despite this attraction, the predator-naive fish did not display typical predator inspection behaviour and showed very poor escape performance when initially confronted by the trawl apparatus. Many of these fish, however, showed rapid improvement in their escape performance through learning. These results suggest that predator-sympatric rainbowfish have the capacity to assess the level of threat posed by a predator and predator-naive rainbowfish learn to implement appropriate escape strategies when forced to evade a threat.     

Predator attack motivation influences the inspection behaviour of European minnows

Predator inspection behaviour at different levels of attack motivation (attack status of the predator) was investigated in European minnows Phoxinus phoxinus from a population sympatric with pike Esox lucius , during controlled laboratory experiments. Shoals of minnows performed more predator inspections and formed larger inspection group sizes shortly after an attack by a pike. After inspection, minnows returned to the safety of the main shoal, regardless of predator motivation. Minnows which inspected last-before and first-after a strike by a pike modified their behaviour after inspection; they reduced feeding, increased shoaling, flicked their dorsal and pectoral fins and skittered. This behaviour signified alarm and appeared to reflect the severity of the threat posed by the predator at the time of inspection. Fish that had inspected when the pike displayed low attack motivation did not modify their behaviour after inspection to reflect alarm. Information concerning the attack motivation of the predator is probably transferred passively throughout the shoal by changed inspector behaviour and by inspection rate. These data demonstrate that: (1) minnows modified their behaviour after inspection to reflect a predator's attack motivation; and (2) minnows which inspected immediately before a strike appeared to anticipate the future attack and modified their behaviour accordingly.     

Inspection behaviour and inter-individual cooperation in juvenile qingbo: the effects of prior predator exposure and food deprivation

The predation pressure and food availability to which individuals are exposed during their life histories shape inspection behaviour in animals. In this study, we aimed to test whether such behaviours varied with prior experience (predation, starvation or both treatments) or measurement condition (with or without the presence of a predator; here, the snakehead fish, Channa argus) in the fish species Spinibarbus sinensis, known as qingbo. Unexpectedly, prior predator experience showed no significant effect on inspection behaviour as demonstrated by either the frequency or the duration of each activity outside shelter or on cooperation as demonstrated by the inter-individual distance or synchronization of speed. This may have been due to the different adjustments in behaviour among individuals (more shelter use vs. more inspection), the predator treatment used in the present study (exposure to caged predator rather than direct predation) and/or a species-specific strategy in the qingbo. The starved fish displayed shorter inspection latency, increased inspection behaviour and greater cooperation when measured without the predator; however, when measured in the presence of the predator, the starved fish showed increased inspection frequency but shorter inspection duration, possibly due to the compromise between energy needs and predation risk. Similar to those of the predation group, the fish from the double-treated group showed no difference in inspection behaviour compared to the control group under the predator-absent condition, while the high-frequency, short-duration inspection behaviours remained the same as in the starved group. These findings suggested that the adjustment of inspection behaviour and related cooperation are rather complicated according to either predator experience or food deprivation, partially due to the inter-individual differences in behavioural adjustment and/or different environmental conditions.     

Lateralization When Monitoring Predators in the Wild: A Left Eye Control in the Common Wall Lizard (Podarcis muralis)

Lateralization is the function specialization between left and right brain hemispheres. It is now ascertained in ectotherms too, where bias in eye use for different tasks, i.e., visual lateralization, is widespread. The lateral eye position on the head of ectotherm animals, in fact, allows them to observe left/right stimuli independently and allows lateralized individuals to carry out left and right perceived tasks at the same time. A recent study conducted on common wall lizards, Podarcis muralis, showed that lizards predominantly monitor a predator with the left eye while escaping. However, this work was conducted in a controlled laboratory setting owing to the difficulty of carrying out lateralization experiments under natural conditions. Nevertheless, field studies could provide important information to support what was previously found in the laboratory and demonstrate that these traits occur in nature. In this study, we conducted a field study on the antipredatory behavior of P. muralis lizards. We simulated predatory attacks on lizards in their natural environment. We found no lateralization in the measure of eye used by the lizard to monitor the predator before escaping from it, but the eye used was probably determined by the relative position of the lizard and the predator just before the attack. This first eye used did not affect escape decisions; lizards chose to escape toward the nearest refuge irrespective of whether it was located to the lizard’s left or right side. However, once they had escaped to a refuge, lizards had a left eye–mediated bias to monitor the predator when first emerging from the refuge, and this bias was likely independent of other environmental variables. Hence, these field findings support a left eye–mediated observation of the predator in P. muralis lizards, which confirms previous findings in this and other species.     

Who dares, learns: chemical inspection behaviour and acquired predator recognition in a characin fish

Individuals that dare approach predators (predator inspection behaviour) may benefit by acquiring information regarding the potential threat of predation. Although information acquisition based on visual cues has been demonstrated for fish, it is unknown whether fish will inspect predators on the basis of chemical cues or whether such inspection behaviour results in information acquisition. Here, we first ascertained whether predator inspection behaviour can be mediated by chemical cues from predators by exposing groups of predator-naive glowlight tetras (Hemigrammus erythrozonus) to the chemical cues of a potential fish predator (convict cichlid Cichlasoma nigrofasciatum) that had been fed either tetras (which possess an alarm pheromone) or swordtails (Xiphophorus helleri, which lack Ostariophysan alarm pheromones). Tetras showed a significant increase in antipredator behaviour when exposed to the tetra-diet cue, but not when exposed to the swordtail-diet cue. Chemically mediated predator inspection behaviour was also affected. Both the latency to inspect and the minimum approach distance to the predator significantly increased, and the mean number of inspectors per predator inspection visit significantly decreased when tetras were exposed to the tetra-diet versus the swordtail-diet chemical cues. We then examined a potential benefit associated with chemically mediated predator inspection behaviour. Only tetras that were initially exposed to the tetra-diet cue and that had inspected the predator acquired the visual recognition of a convict cichlid as a predation threat. Our results thus demonstrate that (1) predator inspection behaviour in the glowlight tetra can be initiated by chemical cues, (2) chemically mediated inspection behaviour is affected by the presence of alarm pheromone, and (3) inspectors benefit by acquiring the recognition of novel predators. Copyright 1999 The Association for the Study of Animal Behaviour.     

Effects of nucleus accumbens lesions in rats on spatial preference in an open field

Selective lesions placed in three different regions of the nucleus accumbens were performed to assess their effects on spatial preference in the rat. Histological verification allowed to establish three groups of lesioned animals: medial, intermediate and lateral. Sham operations involved all procedures except the passing of a current. All animals were tested once prior to operation and twice postoperatively. Sherman's directionality score (DS) was adopted. Positive values indicate right side preference and negative ones leftward bias. Statistical analysis revealed that rats used in this study showed a nonsignificant spontaneous right side preference in the open field (DS = +0.08). Medial and intermediate lesions increased the right side bias (DS = +0.37), whereas lateral lesioned animals reversed their preoperative rightward bias and showed a significant left side preference (DS = -0.48). These results suggest a participation of the nucleus accumbens in spatial preference and are considered to be due to the well known uneven distribution of the afferent and efferent fiber systems within the nucleus.     

The influence of predator presence on utilization of artificial seagrass habitats by juvenile walleye pollock,Theragra chalcogramma

Synopsis Behavioral preference for a structured habitat (artificial seagrass) by juvenile walleye pollock,Theragra chalcogramma, was tested in controlled laboratory experiments. We monitored position of fish in 2000 1 tanks with and without artificial seagrass present in one half of the tank. In addition, we exposed walleye pollock to a predator model, assessing their response when a grass plot was available or unavailable as a potential refuge. In the absence of predators, the fish avoided the artificial seagrass, displaying a preference for the open water side of the experimental tanks. In the presence of a predator model, however, juvenile walleye pollock readily entered the artificial seagrass plots. In addition, they often remained in the grass canopy in proximity to the predator instead of moving out of the grass to avoid the predator (when no grass was present they consistently moved to the opposite side of the tank from the predator). The behavioral choices exhibited in this study suggest that juvenile walleye pollock modify habitat selection in response to perceived predation risk, and recognize the structure provided by artificial seagrass as a potential refuge.     

Infection with an acanthocephalan manipulates an amphipod's reaction to a fish predator's odours

Many parasites with complex life cycles increase the chances of reaching a final host by adapting strategies to manipulate their intermediate host's appearance, condition or behaviour. The acanthocephalan parasite Pomphorhynchus laevis uses freshwater amphipods as intermediate hosts before reaching sexual maturity in predatory fish. We performed a series of choice experiments with infected and uninfected Gammarus pulex in order to distinguish between the effects of visual and olfactory predator cues on parasite-induced changes in host behaviour. When both visual and olfactory cues, as well as only olfactory cues were offered, infected and uninfected G. pulex showed significantly different preferences for the predator or the non-predator side. Uninfected individuals significantly avoided predator odours while infected individuals significantly preferred the side with predator odours. When only visual contact with a predator was allowed, infected and uninfected gammarids behaved similarly and had no significant preference. Thus, we believe we show for the first time that P. laevis increases its chance to reach a final host by olfactory-triggered manipulation of the anti-predator behaviour of its intermediate host.     

Predator model recognition and response habituation in shoaling minnows

Minnows in shoals used a spectrum of behaviours to discriminate stalking models of pike. Predator recognition was initially based on model shape and size, with identification being confirmed using information on markings gathered by minnows during predator inspection visits. Minnow behaviour indicated that shoals regarded the most realistic model as the greates threat. Conversely, habituation of the anti-predator response in repeated stalks was most evident with the least realistic model. Implications for the design of models used in predation experiments are discussed.     

Selective stimulus control in discrimination of lateral mirror images by pigeons

Four monocularly and two binocularly viewing pigeons were trained to peck a key when it displayed one stimulus (S+) but not to peck when it displayed another stimulus (S−). S+ and S− were a lateral mirror-image pair of two-coloured stimuli. When tested for transfer with the untrained eye open, two of the monocular birds pecked more during S− than S+, the other two continuing to favour S+. During generalization tests on the wavelength dimension all monocular birds pecked much more often during one S+ colour than during the other. The colour controlling pecking was that displayed on the side of the key facing the open eye during S+ presentations. Both binocular birds developed asymmetrical responses to the key, one favouring the left, the other the right side of the key. Generalization tests on the wavelength dimension showed selective control by the colour displayed on the favoured side of the key during S+ presentations. The results are interpreted as supporting the view that pigeons learn to discriminate lateral mirror images by developing asymmetrical observing responses that convert the left-right difference between the mirror images into a difference more easily discriminable.     

Lateralization in response to social stimuli in a cooperatively breeding cichlid fish

Cerebral lateralization, an evolutionarily ancient and widespread phenomenon among vertebrates, is thought to bestow cognitive advantages. The advantages of lateralization at the individual-level do not necessarily require that the entire population share the same pattern of lateralization. In fact, directional bias in lateralization may lead to behavioural predictability and enhanced predator success or prey evasion. Recent theory has suggested that population-level lateralization may be favored if individuals are better able to perform coordinated behaviours, providing a distinct advantage in cooperative contexts. Here we test whether the highly social, cooperatively breeding cichlid fish Neolamprologus pulcher shows lateralized responses to a social stimulus. We found population-level biases in males; on average male N. pulcher use their right eye/left hemisphere to view their mirror image. Individual females had a preferred hemisphere, but these preferences appeared not to be directionally aligned among females. We discuss these results in the context of coordinated social behaviour and suggest future research directions.     

Lateral position preference in grazing feral horses

Behavioural lateralisation is an effective way for animals to manage daily tasks by specialising behaviour to either side of the body. Many types of lateralisation are linked to the function of each brain hemisphere. Lateralisation of monitoring behaviour in mother–infant relationships occurs in a wide range of mammals, where infants frequently use their left eye to monitor their mother. However, few studies have focused on this type of spatial relationships among adults in daily life, such as during foraging. The present study focused on monitoring adult feral horse behaviour using quantitative analysis of spatial relationships, using drone technology. We found that horses form a localised spatial relationship with their nearest neighbour. Specifically, the nearest neighbour was located to the left rear of a target individual significantly more frequently than to the right rear. Furthermore, the nearest neighbour was less frequently located behind a target individual. We propose that this relationship is caused by a left-eye preference, because information via the left eye predominantly proceeds to the right hemisphere, which is dominant for social processing.     

How birds use their eyes: Opposite left-right specialization for the lateral and frontal visual hemifield in the domestic chick

Recent evidence has demonstrated that, in animals with laterally placed eyes, functional cerebral asymmetry is revealed by preferential use of either the left or right eye in a range of behaviors (birds: [1, 2, 3]; fish: [4, 5]; reptiles: [6, 7]). These findings pose a theoretical problem. It seems that there would be disadvantages in having a substantial degree of asymmetry in the use of the two eyes; a deficit on one side would leave the organism vulnerable to attack on that side or unable to exploit resources appearing on one side. We here report a possible solution to the problem. We have found that domestic chicks show selective use of the lateral visual field of the left eye and of the right hemifield in the binocular, frontal visual field when they peck at strangers but not at cagemates. Thus, during social recognition, there seems to be opposite and complementary left-right specialization for the lateral and frontal visual fields of the two eyes. These findings can reconcile the computational advantages associated with asymmetry of the left and right sides of the brain with the ecological demands for an animal to perceive and respond equally well to the left and right sides of its midline.     

Do competing males cooperate? Familiarity and its effect on cooperation during predator inspection in male three‐spined sticklebacks (Gasterosteus aculeatus)

We investigated the trade‐off between conflict and cooperation, using predator inspection behaviour in sticklebacks as a model system. Male three‐spined sticklebacks ( Gasterosteus aculeatus ) compete for territories during the breeding season and it has been demonstrated that the level of aggression between territorial neighbours declines with time, a phenomenon known as the dear enemy effect. In this experiment we examine whether this increase in familiarity between territorial neighbours can facilitate an increase in cooperation during predator inspection events. This was analyzed using male sticklebacks from four pond populations, two with and two without predatory rainbow trout ( Oncorhyncus mykiss ). Males were each exposed to five different treatments: (1) the presentation of a live rainbow trout when alone; (2) with a newly revealed territorial neighbour; (3) with this neighbour after two days of familiarization; (4) with another unfamiliar neighbour (termed a 'floater'); and (5) a second solitary trial (to provide controls at the start and end of the experiment). As predicted, fish from predator‐sympatric populations showed higher levels of predator inspection and lower rates of misdirected territorial aggression towards the predator throughout. However, familiarity between neighbouring males did not facilitate an increase in predator inspection behaviour. Instead, predator inspection behaviour decreased throughout treatments involving the presence of any sort of neighbouring male. Familiarity between neighbours did not influence their ability to cooperatively inspect, but only the nature of any aggressive territorial behaviours, all of which detracted equally from individual inspection effort.     

Visual lateralization in wild striped dolphins (Stenella coeruleoalba) in response to stimuli with different degrees of familiarity

Background

Apart from findings on both functional and motor asymmetries in captive aquatic mammals, only few studies have focused on lateralized behaviour of these species in the wild.

Methodology/Principal Findings

In this study we focused on lateralized visual behaviour by presenting wild striped dolphins with objects of different degrees of familiarity (fish, ball, toy). Surveys were conducted in the Gulf of Taranto, the northern Ionian Sea portion delimited by the Italian regions of Calabria, Basilicata and Apulia. After sighting striped dolphins from a research vessel, different stimuli were presented in a random order by a telescopic bar connected to the prow of the boat. The preferential use of the right/left monocular viewing during inspection of the stimuli was analysed.

Conclusion

Results clearly showed a monocular viewing preference with respect to the type of the stimulus employed. Due to the complete decussation of the optical nerves in dolphin brain our results reflected a different specialization of brain hemispheres for visual scanning processes confirming that in this species different stimuli evoked different patterns of eye use. A preferential use of the right eye (left hemisphere) during visual inspection of unfamiliar targets was observed supporting the hypothesis that, in dolphins, the organization of the functional neural structures which reflected cerebral asymmetries for visual object recognition could have been subjected to a deviation from the evolutionary line of most terrestrial vertebrates.     

Differences in the pattern of antipredator behaviour between hatchery‐reared and wild European sea bass juveniles

Shoals of hatchery‐reared and wild sea bass juveniles Dicentrarchus labrax were tested for differences in their antipredator responses towards a potential live predator, the eel Anguilla anguilla . Eight experimental shoals ( i.e . replicates), each composed of 15 individuals from the same stock of juveniles ( i.e . wild or hatchery), were video recorded for 5 min before and after predator exposure. A set of behavioural variables were measured during the pre‐stimulus and stimulus phases of each test and compared between the two groups of replicates. Results showed that in both hatchery‐reared and wild juveniles predator exposure elicited a significant increase in the mean level of shoal cohesiveness and mean shoal distance from the predator, and a significant decrease in the mean shoal distance from the bottom. Shoals of wild juveniles, however, aggregated more quickly and reached higher shoal cohesiveness within the first 20 s of the stimulus period than shoals of hatchery‐reared fish. During this period, the wild fish also reached the highest peak in shoal cohesiveness, which then decreased gradually towards the levels observed before predator exposure. Another component of the antipredator response, the predator inspection behaviour, was fully developed in both wild and hatchery fish. Wild fish, however, tended to inspect the predator at a closer distance than hatchery fish.     

Information Transfer across Fish Shoals under Predator Threat

The hypothesis that shoaling fish can obtain information about a predator's approach from changes in the behaviour of other shoal members was tested in an experiment in which receiver minnows (Phoxinus phoxinus) behind a one-way-mirror could observe the reaction of transmitter minnows threatened by the stalk of a pike (Esox lucius) model. Although the receiver minnows were out of visual contact with the pike model they decreased their foraging behaviour and started hiding when the pike model came towards the feeding patch of the transmitter fish. The presence of skittering behaviour and inspection behaviour in the transmitter but not in the receiver fish suggests that individual confirmation of the predator does play a role in determining the nature of the anti-predator response. Nevertheless there is clear evidence that receiver fish modify their own behaviour on the basis of information obtained from individuals which have seen a predator.