Quantitative assessment of intrinsic noise for visually guided behaviour in zebrafish

Supported by Royal Society of London (University Research Fellowship), Medical Research Council (New Investigator Research Grant) and CNRS.

Differences in expenditure and amounts of fresh foods, fruits & vegetables and fish purchased in urban and rural Scotland

Peer reviewed

Differences in expenditure and amounts of fresh foods, fruits & vegetables and fish purchased in urban and rural Scotland

Peer reviewed

Seawater carbonate chemistry and brown dottyback (Pseudochromis fuscus) movement and feeding behaviour during experiments, 2011

Changes in olfactory-mediated behaviour caused by elevated CO2 levels in the ocean could affect recruitment to reef fish populations because larval fish become more vulnerable to predation. However, it is currently unclear how elevated CO2 will impact the other key part of the predator-prey interaction - the predators. We investigated the effects of elevated CO2 and reduced pH on olfactory preferences, activity levels and feeding behaviour of a common coral reef meso-predator, the brown dottyback (Pseudochromis fuscus). Predators were exposed to either current-day CO2 levels or one of two elevated CO2 levels (~600 µatm or ~950 µatm) that may occur by 2100 according to climate change predictions. Exposure to elevated CO2 and reduced pH caused a shift from preference to avoidance of the smell of injured prey, with CO2treated predators spending approximately 20% less time in a water stream containing prey odour compared with controls. Furthermore, activity levels of fish was higher in the high CO2 treatment and feeding activity was lower for fish in the mid CO2treatment; indicating that future conditions may potentially reduce the ability of the fish to respond rapidly to fluctuations in food availability. Elevated activity levels of predators in the high CO2 treatment, however, may compensate for reduced olfactory ability, as greater movement facilitated visual detection of food. Our findings show that, at least for the species tested to date, both parties in the predator-prey relationship may be affected by ocean acidification. Although impairment of olfactory-mediated behaviour of predators might reduce the risk of predation for larval fishes, the magnitude of the observed effects of elevated CO2 acidification appear to be more dramatic for prey compared to predators. Thus, it is unlikely that the altered behaviour of predators is sufficient to fully compensate for the effects of ocean acidification on prey mortality.

Integrated Monitoring of Mola mola Behaviour in Space and Time

Over the last decade, ocean sunfish movements have been monitored worldwide using various satellite tracking methods. This study reports the near-real time monitoring of fine-scale (< 10 m) behaviour of sunfish. The study was conducted in southern Portugal in May 2014 and involved satellite tags and underwater and surface robotic vehicles to measure both the movements and the contextual environment of the fish. A total of four individuals were tracked using custom-made GPS satellite tags providing geolocation estimates of fine-scale resolution. These accurate positions further informed sunfish areas of restricted search (ARS), which were directly correlated to steep thermal frontal zones. Simultaneously, and for two different occasions, an Autonomous Underwater Vehicle (AUV) video-recorded the path of the tracked fish and detected buoyant particles in the water column. Importantly, the densities of these particles were also directly correlated to steep thermal gradients. Thus, both sunfish foraging behaviour (ARS) and possibly prey densities, were found to be influenced by analogous environmental conditions. In addition, the dynamic structure of the water transited by the tracked individuals was described by a Lagrangian modelling approach. The model informed the distribution of zooplankton in the region, both horizontally and in the water column, and the resultant simulated densities positively correlated with sunfish ARS behaviour estimator (rs = 0.184, p<0.001). The model also revealed that tracked fish opportunistically displace with respect to subsurface current flow. Thus, we show how physical forcing and current structure provide a rationale for a predator’s fine-scale behaviour observed over a two weeks in May 2014.

Integrated Monitoring of Mola mola Behaviour in Space and Time

Over the last decade, ocean sunfish movements have been monitored worldwide using various satellite tracking methods. This study reports the near-real time monitoring of fine-scale (< 10 m) behaviour of sunfish. The study was conducted in southern Portugal in May 2014 and involved satellite tags and underwater and surface robotic vehicles to measure both the movements and the contextual environment of the fish. A total of four individuals were tracked using custom-made GPS satellite tags providing geolocation estimates of fine-scale resolution. These accurate positions further informed sunfish areas of restricted search (ARS), which were directly correlated to steep thermal frontal zones. Simultaneously, and for two different occasions, an Autonomous Underwater Vehicle (AUV) video-recorded the path of the tracked fish and detected buoyant particles in the water column. Importantly, the densities of these particles were also directly correlated to steep thermal gradients. Thus, both sunfish foraging behaviour (ARS) and possibly prey densities, were found to be influenced by analogous environmental conditions. In addition, the dynamic structure of the water transited by the tracked individuals was described by a Lagrangian modelling approach. The model informed the distribution of zooplankton in the region, both horizontally and in the water column, and the resultant simulated densities positively correlated with sunfish ARS behaviour estimator (rs = 0.184, p<0.001). The model also revealed that tracked fish opportunistically displace with respect to subsurface current flow. Thus, we show how physical forcing and current structure provide a rationale for a predator’s fine-scale behaviour observed over a two weeks in May 2014.

To breathe or fight? Siamese fighting fish differ when facing a real opponent or mirror image.

Displays are a feature of animal contest behaviour and have been interpreted as a means of gathering information on opponent fighting ability, as well as signalling aggressive motivation. In fish, contest displays often include frontal and lateral elements, which in the latter involves contestants showing their flanks to an opponent. Previous work in a range of fish species has demonstrated population-level lateralization of these displays, preferentially showing one side to their opponent. Mirrors are commonly used in place of a real opponent to study aggression in fish, yet they may disrupt the normal pattern of display behaviour. Here, using Siamese fighting fish, Betta splendens, we compare the aggressive behaviour of males to a mirror image and real opponent behind a transparent barrier. As this species is a facultative air-breather, we also quantify surface breathing, providing insights into underlying fight motivation. Consistent with previous work, we found evidence of population-level
lateralization, with a bias to present the left side and use the left eye when facing a real opponent. Contrary to expectations, there were no differences in the aggressive displays to a mirror and real opponent, with positive correlations between the behaviour in the two scenarios. However, there were important differences in surface breathing, which was more frequent and of longer duration in the mirror treatment. The reasons for these differences are discussed in relation to the repertoire of contest behaviour and motivation when facing a real opponent.

Plasticity varies with boldness in a weakly-electric fish

The expression of animal personality is indicated by patterns of consistency in  individual behaviour. Often, the differences exhibited between individuals are consistent across situations. However, between some situations, this can be biased by variable levels of individual plasticity. The interaction between individual plasticity and animal personality can be illustrated by examining situation-sensitive personality traits such as boldness (i.e. risk-taking and exploration tendency). For the weakly electric fish Gnathonemus petersii, light condition is a major factor influencing behaviour. Adapted to navigate in low-light conditions, this species chooses to be more active in dark environments where risk from visual predators is lower. However, G. petersii also exhibit individual differences in their degree of behavioural change from light to dark. The present study, therefore, aims to  examine if an increase of motivation to explore in the safety of the dark, not only affects mean levels of boldness, but also the variation between individuals, as a result of differences  in individual plasticity.  Results: Boldness was consistent between a novel-object and a novel-environment situation in bright light. However, no consistency in boldness was noted between a bright (risky) and a  dark (safe) novel environment. Furthermore, there was a negative association between boldness and the degree of change across novel environments, with shier individuals  exhibiting greater behavioural plasticity.  Conclusions: This study highlights that individual plasticity can vary with personality. In  addition, the effect of light suggests that variation in boldness is situation specific. Finally,  there appears to be a trade-off between personality and individual plasticity with shy but  plastic individuals minimizing costs when perceiving risk and bold but stable individuals  consistently maximizing rewards, which can be maladaptive.

To breathe or fight? Siamese fighting fish differ when facing a real opponent or mirror image

Displays are a feature of animal contest behaviour and have been interpreted as a means of gathering information on opponent fighting ability, as well as signalling aggressive motivation. In fish, contest displays often include frontal and lateral elements, which in the latter involves contestants showing their flanks to an opponent. Previous work in a range of fish species has demonstrated population-level lateralization of these displays, preferentially showing one side to their opponent. Mirrors are commonly used in place of a real opponent to study aggression in fish, yet they may disrupt the normal pattern of display behaviour. Here, using Siamese fighting fish, Betta splendens, we compare the aggressive behaviour of males to a mirror image and real opponent behind a transparent barrier. As this species is a facultative air-breather, we also quantify surface breathing, providing insights into underlying fight motivation. Consistent with previous work, we found evidence of population-level lateralization, with a bias to present the left side and use the left eye when facing a real opponent. Contrary to expectations, there were no differences in the aggressive displays to a mirror and real opponent, with positive correlations between the behaviour in the two scenarios. However, there were important differences in surface breathing, which was more frequent and of longer duration in the mirror treatment. The reasons for these differences are discussed in relation to the repertoire of contest behaviour and motivation when facing a real opponent.

Foraging behaviour, swimming performance and malformations of early stages of commercially important fishes under ocean acidification and warming

Early life stages of many marine organisms are being challenged by climate change, but little is known about their capacity to tolerate future ocean conditions. Here we investigated a comprehensive set of biological responses of larvae of two commercially important teleost fishes, Sparus aurata (gilthead seabream) and Argyrosomus regius (meagre), after exposure to future predictions of ocean warming (+4 °C) and acidification (ΔpH= 0.5). The combined effect of warming and hypercapnia elicited a decrease in the hatching success (by 26.4 and 14.3 % for S. aurata and A. regius, respectively) and larval survival (by half) in both species. The length for newly-hatched larvae was not significantly affected, but a significant effect of hypercapnia was found on larval growth. However, while S. aurata growth was reduced (24.8–36.4 % lower), A. regius growth slightly increased (3.2–12.9 % higher) under such condition. Under acidification, larvae of both species spent less time swimming, and displayed reduced attack and capture rates of prey. The impact of warming on these behavioural traits was opposite but less evident. While not studied in A. regius, the incidence of body malformations in S. aurata larvae increased significantly (more than tripled) under warmer and hypercapnic conditions. These morphological impairments and behavioural changes are expected to affect larval performance and recruitment success, and further influence the abundance of fish stocks and the population structure of these commercially important fish species. However, given the pace of ocean climate change, it is important not to forget that species may have the opportunity to acclimate and adapt.

Vocal differentiation parallels development of auditory saccular sensitivity in a highly soniferous fish

Vocal differentiation is widely documented in birds and mammals but has been poorly investigated in other vertebrates, including fish, which represent the oldest extant vertebrate group. Neural circuitry controlling vocal behaviour is thought to have evolved from conserved brain areas that originated in fish, making this taxon key to understanding the evolution and development of the vertebrate vocal-auditory systems. This study examines ontogenetic changes in the vocal repertoire and whether vocal differentiation parallels auditory development in the Lusitanian toadfish Halobatrachus didactylus (Batrachoididae). This species exhibits a complex acoustic repertoire and is vocally active during early development. Vocalisations were recorded during social interactions for four size groups (fry: <2 cm; small juveniles: 2-4 cm; large juveniles: 5-7 cm; adults >25 cm, standard length). Auditory sensitivity of juveniles and adults was determined based on evoked potentials recorded from the inner ear saccule in response to pure tones of 75-945 Hz. We show an ontogenetic increment in the vocal repertoire from simple broadband-pulsed 'grunts' that later differentiate into four distinct vocalisations, including low-frequency amplitude-modulated 'boatwhistles'. Whereas fry emitted mostly single grunts, large juveniles exhibited vocalisations similar to the adult vocal repertoire. Saccular sensitivity revealed a three-fold enhancement at most frequencies tested from small to large juveniles; however, large juveniles were similar in sensitivity to adults. We provide the first clear evidence of ontogenetic vocal differentiation in fish, as previously described for higher vertebrates. Our results suggest a parallel development between the vocal motor pathway and the peripheral auditory system for acoustic social communication in fish.

Home sweet home: evidence for nest-fidelity in the rocky intertidal fish, the shanny Lipophrys pholis

The ability to be faithful to a particular area or site was analysed in the shanny Lipophrys pholis. Using passive integrated transponders, adults from a population of L. pholis at Cabo Raso, Portugal, were followed over a period of 3 years. The findings showed that site fidelity is a consistent behaviour during the breeding season with specific breeding males being found only in particular sectors within the area, and in specific nests throughout the years. The fact that, in general, L. pholis individuals were absent from the study area during the non-breeding season and breeding males were recorded returning to the same nests and sectors for consecutive breeding seasons suggests that they have developed excellent homing abilities. Translocation data corroborate this idea showing that breeding males successfully returned to their nests after a displacement of >100 m. Altogether, these findings highlight the relevance of life-history traits (e.g. nesting) in the conditioning of site fidelity and homing for this species of rocky intertidal fish, and more importantly, provide evidence for the need of a well-developed navigational system.

Feeding ecology and life-history strategy of nesting males in a fish with long parental care, Lusitanian toadfish (Halobatrachus didactylus, Batrachoididae)

The Lusitanian toadfish, Halobatrachus didactylus, like other batrachoidids, is a benthic fish species with nesting behaviour during the breeding season. During this prolonged period it engages in mating activities and remains in the nest providing parental care. It is not known whether males feed while providing parental care but it is likely that their limited mobility may restrict their diet and influence their fitness. As a consequence, egg cannibalism could occur as a life-history strategy. The aim of the present study is to ascertain the feeding behaviour of nesting males, in comparison to mature non-nesting males, and to identify potential life-history traits related to egg cannibalism. Nest-holders were sampled from artificial nests placed in an intertidal area of the Tagus estuary, only exposed during spring low tides. The diet of nest-holders was compared with that of non-nesting mature males from the same area, captured by otter trawl. The present study demonstrates that despite their constrained mobility nest-holders feed during the breeding season, although in a more opportunistic fashion than non-nesting males. Nest-holders showed a generalist feeding behaviour, with a more heterogeneous diet. Egg cannibalism was not related to male condition, paternity or brood size but showed a higher incidence early in the season when water temperatures were lower. The results suggest a possible seasonal trade-off strategy between care and energy recovery, triggered by environmental factors, where under unfavourable conditions to sustain viable eggs the male may recover energy by eating eggs, thus benefiting future reproductive success, later in the season.

At odds with the group: Changes in lateralization and escape performance reveal conformity and conflict in fish schools

Many vertebrates are known to show behavioural lateralization, whereby they differentially use one side of their body or either of their bilateral organs or limbs. Behavioural lateralization often manifests in a turning bias in fishes, with some individuals showing a left bias and others a right bias. Such biases could be the source of considerable conflict in fish schools given that there may be considerable social pressure to conform to the group to maintain effective group evasion. Here, we show that predation pressure is a major determinant of the degree of lateralization, both in a relative and absolute sense, in yellow-and-blueback fusiliers (Caesio teres), a schooling fish common on coral reefs. Wild-caught fish showed a bias for right turning. When predation pressure was experimentally elevated or relaxed, the strength of lateralization changed. Higher predation pressure resulted in an increase in the strength of lateralization. Individuals that exhibited the same turning bias as the majority of individuals in their group had improved escape performance compared with individuals that were at odds with the group. Moreover, individuals that were right-biased had improved escape performance, compared with left-biased ones. Plasticity in lateralization might be an important evolutionary consequence of the way gregarious species respond to predators owing to the probable costs associated with this behaviour.

Salmonid behaviour under winter conditions

Winter conditions are believed to play an important role in the population dynamics of northern temperate stream fish, challenging the ability of fish to physiologically and behaviourally adapt. Climate change is predicted to increase both mean temperature and temperature fluctuations, especially during winter, leading to dynamic environmental conditions in terms of river ice production and flow. Therefore, knowledge about the winter ecology of stream fish is important for predicting and mitigating anthropogenic impacts on fish production in boreal streams. Stream salmonids are relatively active throughout winter, and behavioural responses to different winter conditions may be critical for survival. Yet, relatively little is known about overwintering behaviour of salmonids, particularly in streams with ice. In this doctoral thesis, I report the results from experimental field and laboratory studies on the behavioural ecology of juvenile salmonids under winter conditions. My results from the field show that salmonids grow more and use a broader range of habitats in the presence of surface ice than in its absence. Results from the laboratory experiments show that the presence of surface ice increases food intake rates, reduces stress and affects social interactions. These laboratory results may explain the positive effects of ice cover on growth that was found in the field experiment. Moreover, I show that drift-feeding ability is reduced at low temperatures, and that nocturnal drift foraging under winter conditions has a low efficiency.