Habituation to low-risk predators improves body condition in lizards

Habituation to nonlethal predation stimuli may provide benefits for animals living in areas with frequent encounters with low-risk predators. On the other hand, individuals can be very consistent in their antipredator responses, with shy individuals showing greater degree of responsiveness than bold individuals. However, the link between habituation or boldness and individual benefits has not been thoroughly investigated. We established whether and how two behavioral components associated with antipredator responses (habituation and boldness, and their interaction) would influence body condition, which is a parameter related to fitness. We conducted an outdoor semi-natural experiment with Iberian wall lizards (Podarcis hispanica). Individual boldness was consistent across contexts, but we did not find any effect of boldness or the interaction between boldness and habituation on body condition. However, those individuals that habituated more readily to a frequent predatory stimulus were able to increase their body condition more relative to lizards that habituated less. This finding highlights the importance of individual differences in behavioral plasticity, which could influence traits related to fitness. Habituation can provide benefits for individuals exposed to low-risk predators; however, individuals more prone to habituation could also experience mortality costs by wrongly habituating to a dangerous predator.     

The roles of competition and environmental heterogeneity in the maintenance of behavioral variation and covariation

Many models of selection predict that populations will lose variation in traits that affect fitness. Nonetheless, phenotypic variation is commonly observed in natural populations. We tested the influences of competition and spatial heterogeneity on behavioral variation within and among populations of Merriam's kangaroo rats (Dipodomys merriami) and tested for the differential expression of trait correlations. We found that populations of D. merriami exhibited more aggression at sites with more competition. Contrary to theoretical predictions and empirical results in other systems, the sites with the greatest spatial heterogeneity and highest levels of competition did not exhibit the most behavioral variation among individuals. However, the greatest within-individual behavioral variability in boldness (response to cues of predator presence) was exhibited where spatial heterogeneity was highest. Aggression and boldness of D. merriami were highly repeatable, that is, individuals behaved in a consistent manner over time, and the two behaviors were also highly correlated. Interestingly, the strength of this correlation was greatest where the competitive community was least diverse. These findings add to increasing evidence that natural populations of animals exhibit patterns of behavioral covariance, or personality structure, and suggest that competitive variation may act to erode personality structure.     

Boldness is influenced by sublethal interactions with predators and is associated with successful harem infiltration in Madagascar hissing cockroaches

One of the contemporary challenges of the behavioral syndromes literature is to identify how individual variation in behavior is determined, and whether this variation impacts ecological success. Although variation in experience is an obvious potential driver of intraspecific behavioral variation, predicting the impact of experience on suites of correlated behavioral traits is less intuitive. Specifically, if experience impacts traits that shape individuals' success in multiple contexts (e.g., foraging and anti-predator behavior), then experience could generate cross-contextual performance trade-offs associated with behavioral spillover. In the present study, we explore how sublethal experience with predators impacts various aspects of male behavioral tendencies in the Madagascar hissing cockroach, Gromphadorhina portentosa. First, we found that males' activity level and boldness were correlated together in the form of a behavioral syndrome. Second, we found that repeated sublethal interactions with predators shifted male boldness but not activity level, thus suggesting that the syndrome's constituent traits can respond to experience at least semi-independently. Third, we discovered that although predator exposure only influenced boldness, we found that boldness was highly correlated with males' ability to obtain rewarding positions in the harems of rival males. Taken together, our data suggest (but do not yet confirm) that although sublethal exposure to predators influences only a narrow subset of male's behavioral tendencies, these effects could still have nonintuitive consequences for males' success in functionally dissimilar ecological contexts (i.e., social and sexual encounters).     

Is boldness affected by group composition in young-of-the-year perch (Perca fluviatilis)?

In young-of-the-year perch (Perca fluviatilis), individuals within groups differed in the degree of boldness, estimated by habitat utilisation and feeding activity in visual contact with a potential predator. We looked at changes in individual behaviour in connection with change of group composition. During the first period, perch were randomly assigned to groups, and time spent in open habitat versus in vegetation and number of prey attacks were registered. The perch were then categorised into personality types (shy, bold, intermediate) according to their behaviour. During the second period, fish were observed when sorted into new groups, each containing only one personality type. Shy individuals showed the largest changes in behaviour, and increased both the time spent in the open and the number of prey attacks when placed into the new groups. Feeding activity in shy fish during the second period was affected by group composition during the first period. After regrouping, bold individuals decreased their time in the open, whereas intermediate individuals did not change behaviour. Time in the open habitat was, to some extent, influenced by the behaviour of the other members of the group, but number of prey attacks was not. The behaviour of fish of the different personality types we have defined in this study seemed to be based on innate traits, but also modified by the influence of other group members and by habituation to the environment.Communicated by J.Krause     

Bold minnows consistently approach danger in the field and lab in response to either chemical or visual indicators of predation risk

A behavioral syndrome is a suite of behaviors correlated across multiple social contexts. In this study, boldness in the face of predation risk was assessed twice in fish across two different sensory modalities in both the field and lab to ascertain the biological relevance and complexity of this attribute. Individual fathead minnows were captured from a natural field population using traps that either contained chemical alarm cues (conspecific skin extract) or control (well water) and their responses to the presence of predator behind a glass partition assessed in the laboratory. Although fewer fish were captured in alarm cue-labeled traps, these bold fish performed longer predator inspections than shy fish captured in control traps. Thus, a shy/bold behavioral syndrome was expressed consistently across field and lab settings in response to both chemical and visual indicators of danger. Shy and bold individuals did not differ in sex, body length, secondary sexual characteristics, or parasite load but were of more robust physical condition.     

Are behavioral syndromes invariant? Spatiotemporal variation in shy/bold behavior in squid

Behavioral syndromes are correlated suites of behavior, analogous to human personality traits. Most work to date has been taken from limited “snapshots” in space and time, with the implicit assumption that a behavioral syndrome is an invariant property, fixed by evolutionary constraints or adaptations. However, directional selection on two mechanistically independent traits (selective covariance) could also result in correlated behaviors. Previously, we have shown that shy/bold behavior in Southern dumpling squid (Euprymna tasmanica) across predator encounter and feeding risk contexts is genetically and phenotypically uncoupled, and hence potentially free to vary independently. Here, we collected data on shy/bold behaviors from two independent wild populations of squid in two different years to test whether behavioral correlations across these same two functional contexts vary through time and space. We detected significant influences of population, sex, and body size on the expression of boldness in squid within each functional context, and this was coupled with significant differences in relative population density and adult sex ratio. Despite these changes in behavior and demographic parameters, we found that correlations between boldness scores across the two functional contexts were largely absent in both wild populations of squid in both years. Our work suggests that some animal groups may be largely characterized by context-specific behavioral expression. A theoretical framework which conceptualizes behavioral syndromes resulting from context-specific behavioral rules may be needed to fully understand why behaviors are sometimes correlated, and why sometimes they are not.     

Evaluating animal personalities: do observer assessments and experimental tests measure the same thing?

The animal personality literature uses three approaches to assess personality. However, two of these methods, personality ratings and experimentation, have been little compared in captivity and never compared in the wild. We assessed the boldness of wild chacma baboons Papio ursinus using both ratings and experimental methods. Boldness was experimentally assessed when individuals were presented with a novel food item during natural foraging. The boldness of the same individuals was rated on a five-point scale by experienced observers. The ratings and experimental assessments of boldness were found to correlate positively and in a linear fashion. When considered categorically the two approaches showed variable agreement depending on the number of categories assigned and the cut-off criteria adopted. We suggest that the variation between approaches arises because each method captures different aspects of personality; ratings consider personality in absolute terms (using predefined criteria) and multiple contexts, while experimental assessments consider personality in relative terms (using experimental scores relative to the population average) and in limited contexts. We encourage animal personality researchers to consider adopting both methodologies in future studies. We also propose that future studies restrict their analyses to continuous data, since the greatest comparability between methods was found with these data. However, if individuals must be categorised, we suggest that researchers either (a) analyse only those individuals categorised as bold or shy by both ratings and experimental approaches or, if these methods cannot be employed simultaneously, (b) do not use approach-specific criteria but choose a cut-off that can be compared by both approaches.     

The role of ecological context and predation risk-stimuli in revealing the true picture about the genetic basis of boldness evolution in fish

To showcase the importance of genotype × environment interactions and the presence of predation risk in the experimental assessment of boldness in fish, we investigated boldness in terms of feeding behavior and refuge use in two genetically different populations of juvenile carp (Cyprinus carpio) in two replicated experimental conditions in ponds and laboratory tanks. The populations were expected to exhibit genetic differences in boldness due to differential evolutionary adaptation to low-predation-risk pond aquaculture conditions. Boldness was measured in variants of open-field trials with and without implementation of additional predation risk-stimuli by angling on feeding spots. Without explicit implementation of risk, genotypes adapted to low-risk environments, i.e., domesticated mirror carp behaved consistently bolder than their less domesticated scaled conspecifics in the pond environment, but not in the laboratory environment. When we implemented artificial risk-stimuli by angling on previously safe feeding spots, boldness differences among genotypes also emerged in the laboratory environment, indicating strong genotype × environment effects on boldness behavior of carp. The expected genetic basis of boldness differences among genotypes was clearly supported in the pond environment, while the laboratory study revealed these patterns only under inclusion of explicit risk-stimuli. Our study thus underscores that boldness may involve both a basal component that is expressed independently of obvious predation risk (e.g., in open fields) and a component revealed in relation to explicit predation risk, and both dimensions may respond differently in behavioral tests.     

Nymphal density, behavioral development, and life history in a field cricket

Population density regulates the strength of intraspecific competition and may thereby be reflected in life-history variables, such as development time, growth rate, or investment in immune defense. However, population density may also affect the fitness payoffs of different behaviors and consequently shape the development of personality. Here we studied if population density during nymphal development (one, four, or ten individuals raised together) affects the level of boldness, measured as the latency time to recover from freezing and emerge from a shelter, aggressiveness towards conspecifics or their correlation at the adult stage in the field crickets, Gryllus integer. In addition, we tested if individuals invest more resources in immune function or speed up their development in response to a high conspecifics density during ontogeny. Nymphal density did not affect adult boldness or aggressiveness towards conspecific males per se, but these variables showed a negative association, i.e., indicated an unconventional behavioral syndrome in the highest density treatment. Supporting the effectiveness of density treatments in inducing plastic responses, individuals reached maturity sooner and invested more resources in immune function in the highest nymphal density group compared to groups consisting of one or four individuals. Our results suggest that population density may play an important role in shaping both the realized life history and development of behavioral syndromes.     

Balancing the response to predation—the effects of shoal size,predation risk and habituation on behaviour of juvenile perch

Group size, predation risk and habituation are key drivers of behaviour and evolution in gregarious prey animals. However, the extent to which they interact in shaping behaviour is only partially understood. We analyzed their combined effects on boldness and vigilance behaviour in juvenile perch (Perca fluviatilis) by observing individuals in groups of one, two, three and five faced with four different levels of predation risk in a repeated measures design. The perch showed an asymptotic increase in boldness with increasing group size and the highest per capita vigilance in groups of two. With increasing predation risk, individuals reduced boldness and intensified vigilance. The interaction between group size and predation risk influenced vigilance but not boldness. In this context, individuals in groups of two elevated their vigilance compared to individuals in larger groups only when at higher risk of predation. Further, as only group size, they significantly reduced vigilance at the highest level of risk. With increasing habituation, solitary individuals became considerably bolder. Also, predation risk affected boldness only in the more habituated situation. Hence, repeated measures may be essential to correctly interpret certain relationships in behaviour. Our results suggest that perch may adjust boldness behaviour to group size and predation risk independently. This is rather unexpected since in theory, natural selection would strongly favour an interactive adjustment. Finally, vigilance might be particularly effective in groups of two due to the intense monitoring and detailed response to changing levels of risk.     

Look before you leap - individual variation in social vigilance shapes socio-spatial group properties in an agent-based model

Next to predator detection, primate vigilance also serves to keep track of relevant conspecifics. The degree of vigilance towards group members often reflects the dominance rank of an individual: subordinates pay attention to dominants. Although it has been suggested that subordinates' vigilance may result in spatial centrality of dominants, this has not been addressed in either empirical or modeling studies. Using agent-based models, we determined how social vigilance affects socio-spatial properties of primate groups. A basic model without social vigilance, where individuals avoid potential aggressors (avoidance model), was contrasted with two models that each additionally included a different type of social vigilance: a) monitoring a specific potential aggressor to remain informed on its whereabouts (monitoring model) or b) scanning the whole group to detect potential aggressors (scanning model). Adding monitoring or scanning behavior to the avoidance model reinforced spatial centrality of dominants, a pattern often observed in primates, and resulted in more spread out groups. Moreover, variation in scanning tendency alone was already sufficient to generate spatial centrality of dominants: frequently scanning subordinates could move further away from the group center than dominants, before losing sight of group members. In the monitoring model, two mechanisms caused decreased encounter frequencies among subordinates: a) increased inter-individual distances, and b) frequent monitoring of central dominants. In the scanning model, encounters among subordinates decreased due to increased inter-individual distances. This agent-based model study provides a clear indication that individual variation in social vigilance may be an important structuring feature of primate social groups.     

Consequences of stage-structured predators: cannibalism, behavioral effects, and trophic cascades

Cannibalistic and asymmetrical behavioral interactions between stages are common within stage-structured predator populations. Such direct interactions between predator stages can result in density- and trait-mediated indirect interactions between a predator and its prey. A set of structured predator-prey models is used to explore how such indirect interactions affect the dynamics and structure of communities. Analyses of the separate and combined effects of stage-structured cannibalism and behavior-mediated avoidance of cannibals under different ecological scenarios show that both cannibalism and behavioral avoidance of cannibalism can result in short- and long-term positive indirect connections between predator stages and the prey, including "apparent mutualism." These positive interactions alter the strength of trophic cascades such that the system's dynamics are determined by the interaction between bottom-up and top-down effects. Contrary to the expectation of simpler models, enrichment increases both predator and prey abundance in systems with cannibalism or behavioral avoidance of cannibalism. The effect of behavioral avoidance of cannibalism, however, depends on how strongly it affects the maturation rate of the predator. Behavioral interactions between predator stages reduce the short-term positive effect of cannibalism on the prey density, but can enhance its positive long-term effects. Both interaction types reduce the destabilizing effect of enrichment. These results suggest that inconsistencies between data and simple models can be resolved by accounting for stage-structured interactions within and among species.     

Behavioural trait assortment in a social network: patterns and implications

The social fine structure of a population plays a central role in ecological and evolutionary processes. Whilst many studies have investigated how morphological traits such as size affect social structure of populations, comparatively little is known about the influence of behaviours such as boldness and shyness. Using information on social interactions in a wild population of Trinidadian guppies (Poecilia reticulata), we construct a social network. For each individual in the network, we quantify its behavioural phenotype using two measures of boldness, predator inspection tendency, a repeatable and reliably measured behaviour well studied in the context of co-operation, and shoaling tendency. We observe striking heterogeneity in contact patterns, with strong ties being positively assorted and weak ties negatively assorted by our measured behavioural traits. Moreover, shy fish had more network connections than bold fish and these were on average stronger. In other words, social fine structure is strongly influenced by behavioural trait. We assert that such structure will have implications for the outcome of selection on behavioural traits and we speculate that the observed positive assortment may act as an amplifier of selection contributing to the maintenance of co-operation during predator inspection.     

Variation along the shy–bold continuum in extremophile fishes (<Emphasis Type="BoldItalic">Poecilia mexicana</Emphasis>, <Emphasis Type="BoldItalic">Poecilia sulphuraria</Emphasis>)

One potential trade-off that bold individuals face is between increased predation risks and gains in resources. Individuals experiencing high predation and hungry individuals (or individuals with low body condition) are predicted to show increased boldness. We examined one behavioral trait previously reported to be associated with boldness (the time individual fish needed to emerge from shelter) in various populations of mollies (Poecilia spp.). Our study system included several southern Mexican surface streams with high piscine predation and high food availability, sulfidic surface streams with high avian predation, in which the inhabiting fish show reduced body condition, and a sulfidic cave, where predation and body condition are low. Our comparison revealed very short times to emerge from the start box in populations from non-sulfidic streams. In sulfidic habitats (whether surface or cave), it took individual Poecilia mexicana considerably longer to emerge from the start box, and the same difference was also found in an independent comparison between P. mexicana and the closely related, highly sulfide-adapted Poecilia sulphuraria. Fish reared under common garden conditions (in the absence of predators and hydrogen sulfide) showed intermediate boldness scores to the extremes observed in the field. Our data thus indicate that (a) boldness is shaped by environmental conditions/experiential effects, but is not heritable, (b) predation affects boldness in the predicted direction, but (c) low body condition leads to reduced boldness. Extremophile Poecilia spp. spend most of their time surfacing to survive under sulfidic and hypoxic conditions, which exposes them to increased levels of predations, but the fish forage on the bottom. Hence, in this system, increased boldness does not increase foraging success. We argue that energy limitation favors reducing energetically costly behaviors, and exploring novel environments may be just one of them.     

Structure of the social network and its influence on transmission dynamics in a honeybee colony

Infectious processes in a social group are driven by a network of contacts that is generally structured by the organization arising from behavioral and spatial heterogeneities within the group. Although theoretical models of transmission dynamics have placed an overwhelming emphasis on the importance of understanding the network structure in a social group, empirical data regarding such contact structures are rare. In this paper, I analyze the network structure and the correlated transmission dynamics within a honeybee colony as determined by food transfer interactions and the changes produced in it by an experimental manipulation. The study demonstrates that widespread transmission in the colony is correlated to a lower clustering coefficient and higher robustness of the social network. I also show that the social network in the colony is determined by the spatial distribution of various age classes, and the resulting organizational structure provides some amount of immunity to the young individuals. The results of this study demonstrates how, using the honeybee colony as a model system, concepts in network theory can be combined with those in behavioral ecology to gain a better understanding of social transmission processes, especially those related to disease dynamics.     

Behavioral variation shows heritability in juvenile brown trout Salmo trutta

Animal personalities (sometimes referred also as coping styles) and their fitness consequences are currently among the most intensively explored subjects in behavioral ecology. To estimate the evolvability and adaptability of individually consistent behavioral variation, there is a crucial need to quantify the genetics underlying personality. Here, we experimentally studied the repeatability of various individual behaviors and then estimated heritability of formed boldness, exploration, and aggression components in juvenile brown trout Salmo trutta in standardized laboratory environment. Principal component analysis indicated that individually recorded behaviors were described by two personality axes: the first reflecting boldness, exploration, and aggression and the second tendency to freeze. These personality components, as well as the originally recorded behaviors, were statistically significantly repeatable over time. The latter PC, but not the first one, was statistically significantly heritable, though at low level (h ²?=?0.142?±?0.096). These results suggest that additive genetic variation underlies phenotypically consistent behavioral patterns, proposing that any selection acting on behavior, stress tolerance, or correlated traits has a potential to induce evolution in fish personality.     

Do brain parasites alter host personality? — Experimental study in minnows

Despite that the existence of animal personalities is widely recognized, no consensus has been reached on the relative importance of different ecological factors behind their expression. Recently, it has been suggested that parasites may have a crucial role in shaping animal personalities, but only a very few studies have experimentally tested the idea. We infected Eurasian minnows (Phoxinus phoxinus) with the brain-encysted trematode parasite, Diplostomum phoxini, and studied whether infection could modify the personality of their hosts. Our results show that D. phoxini infection did not affect the mean levels of boldness, activity or exploration, but infected minnows showed higher repeatability in boldness and activity, and reduced repeatability in exploration. We also found that D. phoxini may be able to break the associations (behavioral syndromes) between behavioral traits, but that this effect may be dependent on parasite intensity. Furthermore, the effect of D. phoxini infection on personality of the hosts was found to be nonlinearly dependent on infection intensity. Taken together, our results suggest that D. phoxini parasites may shape the personality of their hosts, but that behavioral consequences of ecologically relevant infection levels may be rather subtle and easily remain undetected if only the mean trait expressions are compared.     

Chick-a-dee call variation in the context of “flying” avian predator stimuli: a field study of Carolina chickadees (<Emphasis Type="Italic">Poecile carolinensis</Emphasis>)

Chick-a-dee calls function in social organization in Poecile (chickadee) species. Recent field and aviary studies have found that variation in chick-a-dee calls relates to the type or proximity of avian predator, or level of threat. Earlier studies on calls in the context of predator stimuli have typically used stationary and perched predator models. For chickadees and other small songbirds, more frequently detected and more dangerous avian predatory stimuli are flying predators. In the present study, we tested whether simulated flying avian predator and control models influenced chick-a-dee calling behavior of wild Carolina chickadees, Poecile carolinensis. At 20 independent field sites, chickadee subjects were presented with wooden models that were painted to resemble either a predatory sharp-shinned hawk (Accipiter striatus) or a blue jay (Cyanocitta cristata) and that were made to “fly” down a zip line near a feeding station chickadees were using. The note composition of chick-a-dee calls was affected by both the flight of stimuli and type of model. Call variation in this flying predator context suggests interesting similarities and differences with experimental findings with congeners. Finally, increased production of certain notes to the flying of both model types provides support for a “Better Safe than Sorry” strategy. When costs of alarm calling are low but costs of discriminating potentially serious threats may be extremely high, individuals should err on the side of caution, and alarm call to any potentially threatening stimulus.     

Ontogeny of feeding behavior and cranial morphology in the whitespotted bambooshark <Emphasis Type="Italic">Chiloscyllium plagiosum</Emphasis>

Morphological and behavioral development of the feeding apparatus over early ontogeny can profoundly affect the ability of an organism to obtain nourishment, ultimately impacting survival. The interplay between morphology and behavior over the first year of life was studied in the whitespotted bambooshark Chiloscyllium plagiosum (Bennett 1830) beginning in March of 2002 using high-speed videography and dissection. Externally measured variables describing cranial growth, and jaw weight, scaled at or near isometry while jaw and hyoid musculature, especially the coracohyoideus, demonstrated considerable hypertrophication. The difference between the volume of the buccal cavity when open and closed scaled with substantial positive allometry while the time to reach maximum jaw and hyoid abduction exhibited weak allometry, resulting in the capacity for more rapid and greater volumetric intake during feeding. In addition, the relative forward motion of the predator during a strike decreased over ontogeny and the feeding modality became more suction-dominated. Kinematic variables exhibited little variability and the primary aspect of food capture that was modulated in response to food type was the forward motion of the predator. An increase in capture success was noted for live, elusive shrimp over ontogeny indicating that morphological and behavioral changes have direct consequences for prey acquisition. Conservation of head shape coupled with a narrow behavioral repertoire is hypothesized to increase prey capture success in the wild over ontogeny as individuals become more proficient in the execution of a single, low-variability, suction-dominated capture behavior.     

Network position: a key component in the characterization of social personality types

In recent years, animal social interactions have received much attention in terms of personality research (e.g. aggressive or cooperative interactions). However, other components of social behaviour such as those describing the intensity, frequency, directedness and individual repeatability of interactions in animal groups have largely been neglected. Network analysis offers a valuable opportunity to characterize individual consistency of traits in labile social groups and therein provide novel insights to personality research in ways previously not possible using traditional techniques. Should individual network positions be consistently different between individuals under changing conditions, they might reflect expressions of an individual's personality. Here, we discuss a conceptual framework for using network analyses to infer the presence of individual differences and present a statistical test based on randomization techniques for testing the consistency of network positions in individuals. The statistical tools presented are useful because if particular individuals consistently occupy key positions in social networks, then this is also likely to have consequences for their fitness as well as for that of others in the population. These consequences may be particularly significant since individual network position has been shown to be important for the transmission of diseases, socially learnt information and genetic material between individuals and populations.