Different behavioral profiles between invasive and native nudibranchs: means for invasion success?

Behavior is predicted to be a primary determinant of the success of the invasion process during the early phases of colonization. Comparing invaders with sympatric native species may provide a good approach to unravel behavioral traits involved in an invasion process. In this study, we carried out an experimental simulation of the introduction and the acclimatization phase into a new environment and assessed the expression of activity, alertness, and habituation in an invasive Mediterranean population of the South African nudibranch Godiva quadricolor comparing its profiles with those of the sympatric Mediterranean native nudibranchs Cratena peregrina and Caloria quatrefagesi. Individuals of these 3 species were subjected to 3 behavioral tests: spontaneous activity, carried out in the introduction phase (immediately after sampling) and after a week of acclimatization; alert test, in which a potential threat was simulated by means of a tactile stimulus, and habituation test, in which the same alert test stimulus was repeated 5 times at 30-min intervals. The invasive G. quadricolor showed higher levels of exploration activity, thigmotaxis, alertness, and sensitization than the native species. These behavioral traits may represent pivotal drivers of the ongoing invasion process.

A robotic falcon induces similar collective escape responses in different bird species.

Patterns of collective escape of a bird flock from a predator are fascinating, but difficult to study under natural conditions because neither prey nor predator is under experimental control. We resolved this problem by using an artificial predator (RobotFalcon) resembling a peregrine falcon in morphology and behaviour. We imitated hunts by chasing flocks of corvids, gulls, starlings and lapwings with the RobotFalcon, and compared their patterns of collective escape to those when chased by a conventional drone and, in case of starlings, hunted by wild peregrine falcons. Active pursuit of flocks, rather than only flying nearby by either the RobotFalcon or the drone, made flocks collectively escape more often. The RobotFalcon elicited patterns of collective escape in flocks of all species more often than the drone. Attack altitude did not affect the frequency of collective escape. Starlings escaped collectively equally often when chased by the RobotFalcon or a wild peregrine falcon. Flocks of all species reacted most often by collective turns, second most often by compacting and third by splitting into subflocks. This study demonstrates the potential of an artificial aerial predator for studying the collective escape behaviour of free-living birds, opening exciting avenues in the empirical study of prey-predator interactions.

Evolution of personality and locomotory performance traits during a late Pleistocene island colonization in a tree frog.

Recent empirical and theoretical studies suggest that personality and locomotory performance traits linked to dispersal abilities are crucial components of the dispersal syndromes, and that they can evolve during range expansions and colonization processes. Island colonization is one of the best characterized processes in dispersal biogeography, and its implication in the evolution of phenotypic traits has been investigated over a wide range of temporal scales. However, the effect of island colonization on personality and performance traits of natural populations, and how these traits could drive island colonization, has been little explored. Noteworthy, no studies have addressed these processes in the context of late Pleistocene range expansions. Here, we investigated the contribution of island colonization triggered by postglacial range expansions to intraspecific variation in personality and locomotory performance traits. We compared boldness, exploration, jumping performance, and stickiness abilities in populations from 3 equidistant areas of the Tyrrhenian tree frog Hyla sarda, 2 from the main island (Corsica Island), and 1 from the recently colonized island of Elba. Individuals from Elba were significantly bolder than individuals from Corsica, as they emerged sooner from a shelter (P = 0.028), while individuals from Corsica showed markedly higher jumping and stickiness performance (both P < 0.001), resulting as more performing than those of Elba. We discuss these results in the context of the major microevolutionary processes at play during range expansion, including selection, spatial sorting, founder effects, and their possible interaction with local adaptation processes.

Co-migration fidelity at a stopover site increases over time in African-European migratory landbirds.

Migratory species are changing their timing of departure from wintering areas and arrival to breeding sites (i.e. migration phenology) in response to climate change to exploit maximum food availability at higher latitudes and improve their fitness. Despite the impact of changing migration phenology at population and community level, the extent to which individual and species-specific response affects associations among co-migrating species has been seldom explored. By applying temporal co-occurrence network models on 15 years of standardized bird ringing data at a spring stopover site, we show that African-European migratory landbirds tend to migrate in well-defined groups of species with high temporal overlap. Such 'co-migration fidelity' significantly increased over the years and was higher in long-distance (trans-Saharan) than in short-distance (North African) migrants. Our findings suggest non-random patterns of associations in co-migrating species, possibly related to the existence of regulatory mechanisms associated with changing climate conditions and different uses of stopover sites, ultimately influencing the global economy of migration of landbirds in the Palearctic-African migration system.

Deterrence of birds with an artificial predator, the RobotFalcon.

Collisions between birds and airplanes can damage aircrafts, resulting in delays and cancellation of flights, costing the international civil aviation industry more than 1.4 billion US dollars annually. Driving away birds is therefore crucial, but the effectiveness of current deterrence methods is limited. Live avian predators can be an effective deterrent, because potential prey will not habituate to them, but live predators cannot be controlled entirely. Thus, there is an urgent need for new deterrence methods. We developed the RobotFalcon, a device modelled after the peregrine falcon, and tested its effectiveness to deter flocks of corvids, gulls, starlings and lapwings. We compared its effectiveness with that of a drone, and of conventional methods routinely applied at a military airbase. The RobotFalcon scared away bird flocks from fields immediately, and these fields subsequently remained free of bird flocks for hours. The RobotFalcon outperformed the drone and the best conventional method at the airbase (distress calls). Importantly, there was no evidence that bird flocks habituated to the RobotFalcon over the course of the fieldwork. We conclude that the RobotFalcon is a practical and ethical solution to drive away bird flocks with all advantages of live predators but without their limitations.

Biogeographic history moulds population differentiation in ageing of oxidative status in an amphibian.

Regulation of oxidative status plays a substantial role in physiological ageing. However, we know little about age-related changes of oxidative status in wild animals, and even less about the role of population history in moulding ageing rates. We addressed these questions by means of a common garden experiment, using the Tyrrhenian tree frog Hyla sarda as the study species. This species underwent a range expansion from northern Sardinia (source) up to Corsica (newly founded) during the Late Pleistocene, and then the two populations became geographically isolated. We found that, at the beginning of the experiment, Sardinian and Corsican frogs had similar concentrations of all oxidative status markers analysed. One year later, Corsican frogs had higher oxidative stress and suffered higher mortality than Sardinian frogs. Our results suggest the intriguing scenario that population differentiation in rates of physiological ageing owing to oxidative stress might be an overlooked legacy of past biogeographic processes.

Oxidative stress inhibition by resveratrol in alcohol-dependent mice.

OBJECTIVES: Uncontrolled ingestion of alcohol has dramatic consequences on the entire organism that are also associated with the oxidation process induced by alcohol and elevate radical oxygen species. Resveratrol, a nonflavonoid phenol, shows well-documented antioxidant properties. We investigated the potential antioxidant ability of this natural compound in a mouse model of alcohol addiction. METHODS: We administered (per os) for 60 d 10 mg · kg-1 · d-1 of resveratrol in alcoholic adult male mice. Oxidative stress was evaluated by measuring serum-free oxygen radicals defense and free oxygen radical levels. Resveratrol metabolites were measured in the serum of mice that were administered with resveratrol. Finally, the effect of resveratrol on the alcohol-induced alteration of brain-derived neurotrophic factors (BDNF) in the liver was investigated. RESULTS: Prolonged consumption of resveratrol strongly counteracts serum radical oxygen species formation caused by chronic alcohol intake without effects on natural, free oxygen radical defense. The presence of resveratrol metabolites in the serum only of animals supplemented with resveratrol potentiates the evidence that the antioxidant effect observed is due to the ingestion of the natural compound. Moreover, resveratrol supplementation can counteract alcohol-induced BDNF elevation in the liver, which is the main target of organ alcohol-induced damage. CONCLUSIONS: The consumption of resveratrol through metabolite formation may play a protective role by decreasing free radical formation and modulating the BDNF involved in hepatic disruption induced by chronic alcohol consumption. Further investigation into the mechanism underlying the protective effect could reinforce the potential use of resveratrol as a dietary supplement to prevent damage associated with chronic alcohol abuse.

Variability in the "stereotyped" prey capture sequence of male cuttlefish (Sepia officinalis) could relate to personality differences.

Studies of animal personality have shown consistent between-individual variation in behaviour in many social and non-social contexts, but hunting behaviour has been overlooked. Prey capture sequences, especially in invertebrates, are supposed to be quite invariant. In cuttlefish, the attack includes three components: attention, positioning, and seizure. The previous studies indicated some variability in these components and we quantified it under the hypothesis that it could relate to personality differences. We, therefore, analysed predation sequences of adult cuttlefish to test their association with personality traits in different contexts. Nineteen subjects were first exposed to an "alert" and a "threat" test and then given a live prey, for 10 days. Predation sequences were scored for components of the attack, locomotor and postural elements, body patterns, and number of successful tentacle ejections (i.e. seizure). PCA analysis of predatory patterns identified three dimensions accounting for 53.1%, 15.9%, and 9.6% of the variance and discriminating individuals based on "speed in catching prey", "duration of attack behaviour", and "attention to prey". Predation rate, success rate, and hunting time were significantly correlated with the first, second, and third PCA factors, respectively. Significant correlations between capture patterns and responsiveness in the alert and threat tests were found, highlighting a consistency of prey capture patterns with measures of personality in other contexts. Personality may permeate even those behaviour patterns that appear relatively invariant.

Individual behavioural type and group performance in Formica fusca ants.

The link between individual and group-level behaviour may help understanding cooperation and division of labour in social animals. Despite the recent surge of studies, especially in social insects, the way individual differences translate into group performance remains debated. One hypothesis is that groups may simply differ in the average personality of their members and this would translate into inter-group differences in collective behaviour. We tested the hypothesis of a linear relationship between individual and group phenotype in the ant Formica fusca by using same-age groups of workers after measuring an individual behavioural trait. Individual exploratory activity in an open-field arena was significantly repeatable. Based on this trait, groups were composed, each consisting of 6 individuals with similar exploration tendency housed with 3 cocoons and a refuge. Individual exploratory activity was associated with the performance in cocoon recovery at the group level: groups composed of high exploratory individuals started transporting displaced cocoons significantly earlier and transported more cocoons into the refuge than groups with low exploratory workers. When in a group, more exploratory animals showed significantly more returns to the refuge than less exploratory ones and tended to transport more cocoons. These results show a direct linear link between individual and collective behaviour, suggesting that colony personality reflects the average personality of workers involved in a given task.

Dietary antioxidants, food deprivation and growth affect differently oxidative status of blood and brain in juvenile European seabass (Dicentrarchus labrax).

Compensatory growth may increase molecular oxidative damage, which may be mitigated through the intake of dietary antioxidants. However, dietary antioxidants may also reduce concentration of antioxidant enzymes, which have a key role in regulating the oxidative status. Here we investigated whether feeding on a diet rich in antioxidants (vitamin E) enables juvenile European seabass (Dicentrarchus labrax) to catch up after a period of food deprivation with negligible effects on the oxidative stress to blood and brain as compared to fish feeding on a normal diet (i.e., not enriched in antioxidants). The results show that a higher intake in antioxidants favoured compensatory growth, but this came at a cost in terms of increased oxidative damage. Increased intake of antioxidants also resulted in changes in the activity of enzymatic antioxidant defences and increased protein oxidative damage in both brain and blood. In addition, food deprivation caused increased protein oxidative damage in brain. Our findings show that the beneficial effects of dietary antioxidants on growth may be offset by hidden detrimental effects and that different early life events affect different components of oxidative status of a given tissue.

Active explorers show low learning performance in a social insect.

An intriguing question in behavioral biology is whether consistent individual differences (called animal personalities) relate to variation in cognitive performance because commonly measured personality traits may be associated with risk-reward trade-offs. Social insects, whose learning abilities have been extensively characterized, show consistent behavioral variability, both at colony and at individual level. We investigated the possible link between personality traits and learning performance in the carpenter ant Camponotus aethiops. Exploratory activity, sociability, and aggression were assessed twice in ant foragers. Behaviors differed among individuals, they were partly repeatable across time and exploratory activity correlated positively with aggression. Learning abilities were quantified by differential conditioning of the maxilla-labium extension response, a task that requires cue perception and information storage. We found that exploratory activity of individual ants significantly predicted learning performance: "active-explorers" were slower in learning the task than "inactive-explorers". The results suggest for the first time a link between a personality trait and cognitive performance in eusocial insects, and that the underlying individual variability could affect colony performance and success.

The role of habitat choice in micro-evolutionary dynamics: An experimental study on the Mediterranean killifish Aphanius fasciatus (Cyprinodontidae).

Habitat choice is defined as a nonrandom distribution of genotypes in different microhabitats. Therefore, it could exert a great impact on the genetic variance of natural populations by promoting genetic divergence, local adaptation, and may even lead to sympatric speciation. Despite this potential role in micro- and macro-evolutionary processes, there is little empirical evidence that the various genotypes within a population may differ in habitat choice-related behaviors. Here, we tested whether habitat choice may have contributed to genetic divergence within a local population of the Mediterranean killifish Aphanius fasciatus, which emerged between groups inhabiting microhabitats with different oxygen concentrations during previous field studies. In a first experiment, we studied the distribution of individuals in conditions of hypoxia and normoxia to test whether they had a different ability to shy away from a hypoxic environment; in a second experiment, we analyzed the individual behavior of fish separately in the two conditions, to verify whether they showed peculiar behavioral responses linked to a possible differential distribution. We then analyzed the six allozyme loci, whose allelic and genotypic frequencies were significantly divergent in the previous studies. In the first test, we found that the distribution of the two homozygote genotypes of the glucose-6-phosphate isomerase-1 locus (GPI-1) was significantly different between the hypoxic and the normoxic conditions. During the second test, all individuals were more active in hypoxic conditions, but the two GPI-1 homozygotes showed a significant difference in time spent performing surface breathing, which was consistent with their distribution observed in the first experiment. These results provide evidence that individual behavioral traits, related to genetic features, may lead to a nonrandom distribution of genotypes in heterogeneous although contiguous microhabitats and, consequently, that habitat choice can play a significant role in driving the micro-evolutionary dynamics of this species.

Individual differences in exploratory activity relate to cognitive judgement bias in carpenter ants.

Emotional state may influence cognitive processes such as attention and decision-making. A cognitive judgement bias is the propensity to anticipate either positive or negative consequences in response to ambiguous information. Recent work, mainly on vertebrates, showed that the response to ambiguous stimuli might change depending on an individual's affective state, which is influenced by e.g. the social and physical environment. However, the response to ambiguous stimuli could also be affected by the individual's behavioural type (personality), a question that has been under-investigated. We studied the link between individual differences in exploratory activity and the response to an ambiguous stimulus in the ant Camponotus aethiops. Exploratory behaviour, quantified with an open-field test, was variable among individuals but consistent over time within individuals. Individual ants learned to associate a spatial position to a reinforcement and another spatial position to a punishment. Once the ants had acquired this discrimination, cognitive judgement bias was tested with the stimulus in an intermediate position. Fast explorers in the open-field took significantly more time to approach the ambiguous stimulus compared to slow explorers, suggesting a negative judgement bias for fast explorers and a positive bias for slow explorers. This previously unknown link between individual difference in exploratory activity and cognitive bias in a social insect may help understanding the evolution and organization of social life.

The Tangled Evolutionary Legacies of Range Expansion and Hybridization.

Spatial sorting of dispersal-enhancing traits has been implicated in substantial directional changes in the phenotypic and genotypic makeup of populations undergoing range expansion. We explore here the evolutionary consequences of such changes when two divergent lineages come into secondary contact. We combine instances from the study of contemporary range expansions and historical hybridizations, and highlight links between dispersal, sexual, and physiological traits during the non-equilibrium conditions imposed by range expansions. We argue that a stronger research focus on processes of spatial sorting of multiple traits will improve our understanding of subsequent hybridization dynamics and their evolutionary outcomes, including genomic introgression and speciation.

Bolder Takes All? The Behavioral Dimension of Biogeography.

Animal personality can be seen as behavioral polymorphism that could play a direct and active role in driving evolutionary pathways. We argue here that consistent individual differences in key personality traits affecting dispersal and other density-dependent processes have provided substantial contributions to molding biogeographic patterns. Building upon opportunities recently opened by genomics and other novel approaches, we explore the hypothesis that Pleistocene range expansions, island colonizations, and other historical biogeographic processes could have been promoted by non-random samples of behavioral types of the founder populations. We provide context and testable hypotheses, based on case studies, that could bring new implications to our understanding of the processes shaping spatial and temporal patterns of variation in animal biodiversity.

EU guidelines for the care and welfare of an "exceptional invertebrate class" in scientific research. Commentary.

Cephalopods have been defined as "advanced invertebrates" due to the complexity of their nervous system and to their sophisticated behavioural repertoire. However, until recently, the protection and welfare of this class of invertebrates has been mostly disregarded by EU regulations on the use of laboratory animals. The inclusion of "live cephalopods" in the Directive 2010/63/EU has been prompted by new scientific knowledge on the "sentience" of animals used for experimental or other scientific purposes, a fundamental criterion to which animal species are included or not under the protective umbrella of the Directive. In this scenario, the imminent publication of the Guidelines for the care and welfare of cephalopods in research as an initiative by the CephRes-FELASA-Boyd Group is a sign of ethical progress in the consideration of animals in research, and is likely to have a significant impact on both scientific and practical aspects of research conducted with these animals.

Behavioural response of European starlings exposed to video playback of conspecific flocks: effect of social context and predator threat.

We studied the behavioural response of European starlings to a socially mediated predation event. Adult starlings were exposed to either a video of a flock attacked by a peregrine falcon or a video of a flock not under attack. We investigated whether the social condition affected the anti-predator response under the hypothesis that in such a gregarious species singletons would increase their anti-predator behaviour more than individuals in groups, to compensate for potential increased risk. The video of the flock under attack caused an increase in immobility and vigilance, more marked in singletons, both during and after the exposure. The video of the non-threatened flock caused an increase in activity levels, especially during the exposure. Furthermore, we observed a marked increase in comfort activities in singletons as well as in social interactions and vocalizations in mini-flocks. Only birds in mini-flocks vocalized, which may be explained by an audience effect, a process of social cognition mediated by the social context, and not only by the stimulus. The results are in line with previous field studies, which showed that isolated starlings are exposed to a higher risk of predation compared to individuals in flocks.

Infaunal macrobenthic community dynamics in a manipulated hyperhaline ecosystem: a long-term study.

BACKGROUND: Understanding the responses of ecological communities to human-induced perturbations is crucial for establishing conservation goals. Ecological communities are dynamic entities undergoing fluctuations due to their intrinsic characteristics as well as anthropogenic pressures varying over time. In this respect, long-term studies, based on large spatial and temporal datasets, may provide useful information in understanding patterns and processes influencing the communities' structure. Theoretical evidence suggests that a role of biodiversity is acting as a compensatory buffer against environmental variability by decreasing the temporal variance in ecosystem functioning and by raising the level of community response to perturbations through the selection of better performing species. Therefore, the spatial and temporal changes in the specialization of the community components may be used as an effective tool to monitor the effects of natural and anthropogenic alterations of the environment in dynamic systems. We examined the temporal dynamics of macroinvertebrate community structure in the hyperhaline habitat of Tarquinia Saltworks (central Italy). We aimed at: (i) investigating the relationships between the level of community specialization and the alterations of the environment across fourteen years; (ii) comparing the ability of aggregate community parameters such as the average abundance vs. species specialization in describing patterns of community composition. RESULTS: We arranged the data in three sub-sets according to three periods, each characterized by different environmental conditions. The mean abundance of sampled macroinvertebrates showed a significant change (p < 0.01) only in the community inhabiting the saltwork basin closely connected to the sea, characterized by the highest environmental variation (i.e. the coefficient of variation, CV, of the aggregate environmental variability over the study period, CVrange = 0.010 - 0.2). Here we found marine species like Modiolus adriaticus (Lamarck, 1819), Neanthes irrorata (Malmgren, 1867), and Amphiglena mediterranea (Leydig, 1851), which inhabited the saltworks during the halt period but disappeared during the subsequent eutrophication phase. Conversely, species specialization showed a significant decrease for each sampled community in the presence of habitat degradation and a recovery after ecological restoration. The widest fluctuations of specialization were recorded for the community inhabiting the saltwork basin with the highest long-term environmental variability. CONCLUSIONS: Recent advances have shown how the increased temporal and spatial variability of species' abundance within the communities may be a signal of habitat disturbance, even in the absence of an apparent decline. Such approach could also be used as a sensitive monitoring tool, able to detect whether or not communities are subjected to increasing biotic homogenization. Also, the increased functional similarity triggered by habitat degradation may impact on species at higher trophic levels, such as the waterbirds wintering in the area or using it as a stopover during migration.