Ethological Aspects of Stress in a Model Lizard, Anolis carolinensis

Research on the stress response in reptiles can provide a usefulcomparative perspective for understanding how the constituentelements of the response can be put into service of diversebehavioral adaptations. A summary of the neural and endocrinecauses and consequences of specific behavioral patterns seenin the small diurnal lizard, Anolis carolinensis, has provideda model for the exploration of the dynamics of autonomic andneurohormonal contributions to adaptive behavior. In this species,changes in body color provide indices of the flux of circulatingstress-relevant hormones, and are seen in situations from spontaneousexploration through agonistic behavior. Furthermore, captiveadult males spontaneously and consistently manifest social dominancerelationships that provide many of the elements of a stress-mediatedadaptive behavioral patterns. These patterns include suppressedreproduction and long-term coping apparently based more on stress-mediatedchanges in motivation than acquired changes in behavior.     

Risk-taking behavior predicts aggression and mating success in a fiddler crab

Evidence is growing that an individual's propensity to takerisks in the presence of a predator is correlated to behaviorsthat can affect individual fitness. We examined whether risk-takingbehavior predicts aggression, surface activity levels, and matingsuccess in male fiddler crabs, Uca mjoebergi. Risk-taking behaviorwas highly consistent among individuals, remained stable overtime, and was unrelated to male size. We found that males thattook greater risks in the presence of a potential predator alsobehaved more aggressively when searching for a new territory.In addition, bold males exhibited higher surface activity levelsand spent more time courting females compared with their shycounterparts. Although risk-taking behavior was independentof other sexually selected traits, it accurately predicted malemating success in U. mjoebergi. We suggest nonsexually selectedtraits, such as risk taking, may represent important behavioralpredictors of success in other species.     

Speed of exploration and risk-taking behavior are linked to corticosterone titres in zebra finches

The existence of consistent individual differences in behavioral strategies ("personalities" or coping styles) has been reported in several animal species. Recent work in great tits has shown that such traits are heritable and exhibit significant genetic variation. Free-living birds respond to environmental stresses by up-regulating corticosterone production. Behavior during mild stress can occur in accordance to two types of coping styles, i.e. active and passive. Using artificially selected lines of zebra finches that vary in the amount of corticosterone produced in response to a manual restraint stressor we ran three "personality" experiments. We show that birds in the different corticosterone lines differ in their exploratory and risk-taking behaviors. There was an increase in exploratory behavior as corticosterone titre increased but only in the low corticosterone line. Birds in high corticosterone line showed greater risk-taking behavior than birds in the other lines. Thus, in general, higher levels of circulating corticosterone following a mild stress result in greater exploratory behavior and greater risk taking. This study shows that lines of animals selected for endocrine hormonal responses differ in their "coping" styles or "personalities".     

Behavioral Syndromes in Stable Social Groups: An Artifact of External Constraints?

Individuals of many species differ consistently in their behavioral reactions toward different stimuli, such as predators, rivals, and potential mates. These typical reactions, described as ‘behavioral syndromes’ or ‘personalities,’ appear to be heritable and therefore subject to selection. We studied behavioral syndromes in 36 male fowl living in 12 social groups and found that individuals behaved consistently over time. Furthermore, responses to different contexts (anti‐predator, foraging, and territorial) were inter‐correlated, suggesting that males exhibited comparable behavioral traits in these functionally distinct situations. We subsequently isolated the same roosters and conducted tests in a ‘virtual environment,’ using high‐resolution digital video sequences to simulate the anti‐predator, foraging, and territorial contexts that they had experienced outdoors. Under these controlled conditions, repeatability persisted but individual responses to the three classes of stimuli failed to predict one another. These were instead context‐specific. In particular, production of each type of vocal signal was independent, implying that calls in the repertoire are controlled by distinct mechanisms. Our results show that extrinsic factors, such as social position, can be responsible for the appearance of traits that could readily be mistaken for the product of endogenous characters.     

Sex-specific differences in reindeer calf behavior and predation vulnerability

According to reproductive strategy theory, males in polygamousbreeding systems should invest in morphological or behavioralfeatures that increase reproductive success. When the earlydevelopment of such traits conflicts with predator protection,we expect that male calves will exhibit risk-taking behavior,such as high activity level and increasing distance from mother,to a greater extent than female calves. We investigated sexdifferences in mother–calf distance, calf activity levels,and calf mortality in a semi-domesticated reindeer (Rangifertarandus) population. The results show that male calves strayfarther away from their mothers, exhibit a higher level of locomotivebehavior in terms of play and walking, and are more vulnerableto predation than are female calves. Although mother–calfdistance increased over time in 1- to 6-month-old calves, noevidence was apparent for an increase in sex difference in mother–calfdistance over this period. The results suggest a trade-off betweenpredation vulnerability and investments in behavioral traitsthought to be important for future reproductive success andsuggest that these sex-related differences in behavior are apparentas early as 6 months of age.     

Brain Structural Correlates of Risk-Taking Behavior and Effects of Peer Influence in Adolescents

Adolescents are characterized by impulsive risky behavior, particularly in the presence of peers. We discriminated high and low risk-taking male adolescents aged 18–19 years by assessing their propensity for risky behavior and vulnerability to peer influence with personality tests, and compared structural differences in gray and white matter of the brain with voxel-based morphometry (VBM) and diffusion tensor imaging (DTI), respectively. We also compared the brain structures according to the participants'' actual risk-taking behavior in a simulated driving task with two different social conditions making up a peer competition situation. There was a discrepancy between the self-reported personality test results and risky driving behavior (running through an intersection with traffic lights turning yellow, chancing a collision with another vehicle). Comparison between high and low risk-taking adolescents according to personality test results revealed no significant difference in gray matter volume and white matter integrity. However, comparison according to actual risk-taking behavior during task performance revealed significantly higher white matter integrity in the high risk-taking group, suggesting that increased risky behavior during adolescence is not necessarily attributed to the immature brain as conventional wisdom says.     

The evolution of sexually dimorphic earwig forceps: social interactions among adults of the toothed earwig, Vostox apicedentatus

Earwigs (Insecta, Dermaptera) are characterized by uniquelyelaborated cerci, commonly called forceps, the function of whichremains unclear. We studied intrasexual and intersexual interactionsin the laboratory to examine the context and pattern of forcepsuse in the toothed earwig. Vostox apictdenlatus (Caudell). Interactionsbetween pairs of earwigs were recorded in four social situations:(1) two males, (2) two males plus a virgin female, (3) two females,and (4) one male and one female. Forceps were used as both weaponsand display structures by males and females in all of thesesocial contexts. During pairwise male-male interactions, onemale clearly dominated the other male. Dominant males were moreactive and more likely to use their forceps in intrasexual interactionsthan were subordinate males. In interactions where there weretwo males and one female present, the male that dominated male-maleinteractions was able to maintain exclusive access to the female.There was no indication of active female choice during or aftercourtship. During intersexual interactions, only males usedtheir forceps during courtship. The behavioral repertoire involvingforceps was greater for males than for females, especially inintrasexual contests. There was no clear outcome of intrasexualinteractions among females. These results suggest that forcepsfunction mainly as weapons in male-male interactions and mayhave evolved, at least in part, as a result of sexual selection.Further research is required to test for female mate choiceand to separate the various mechanisms of sexual selection ifmate choice exists. Comparative studies are needed to determineif sexual selection was the original evolutionary mechanismleading to the development of these unusual structures or ifsexual selection is relegated to a secondary effect, leadingto the elaboration and sexualdimorphism of these structuresin selected groups of earwigs.     

Experimental induction of social instability during early breeding does not alter testosterone levels in male black redstarts,a socially monogamous songbird

Testosterone plays an important role in territorial behavior of many male vertebrates and the Challenge Hypothesis has been suggested to explain differences in testosterone concentrations between males. For socially monogamous birds, the challenge hypothesis predicts that testosterone should increase during male–male interactions. To test this, simulated territorial intrusion (STI) experiments have been conducted, but only about a third of all bird species investigated so far show the expected increase in testosterone. Previous studies have shown that male black redstarts (Phoenicurus ochruros) do not increase testosterone during STIs or short-term male–male challenges. The aim of this study was to evaluate whether black redstarts modulate testosterone in an experimentally induced longer-term unstable social situation. We created social instability by removing males from their territories and compared the behavior and testosterone concentrations of replacement males and neighbors with those of control areas. Testosterone levels did not differ among replacement males, neighbors and control males. Injections with GnRH resulted in elevation of testosterone in all groups, suggesting that all males were capable of increasing testosterone. We found no difference in the behavioral response to STIs between control and replacement males. Furthermore, there was no difference in testosterone levels between replacement males that had expanded their territory and new-coming males. In combination with prior work these data suggest that testosterone is not modulated by male–male interactions in black redstarts and that testosterone plays only a minor role in territorial behavior. We suggest that territorial behavior in species that are territorial throughout most of their annual life-cycle may be decoupled from testosterone.     

Male mating strategies under predation risk: do females call the shots?

Many authors have reported that, under elevated risk of predation,male guppies (Poecilia reticulata) alter their behavior fromcourtship to forced copulation (gonopodial thrusts not precededby sigmoid displays). This shift is presumed to benefit thebrightly colored male, whose intense courting activity mightotherwise increase his risk of detection and attack by predators.However, there is some evidence that females engaged in reproductiveactivity with males may be even more vulnerable to predatorsthan the males themselves, which suggests an alternative hypothesis:females in high-risk situations are less receptive to male courtship,and this leads males to change their behavior. We tested thishypothesis by providing either males and females separately,or both sexes concurrently, with information about elevatedpredation risk from a cichlid (Crenicichla sp.). We found thatwhen only females were provided with information about increased risk,males performed fewer courtship displays and fewer thrusts.They did not perform more forced copulations in any treatmentgroup. Nonetheless, our results suggest that the female's perceptionof predation risk can be at least as important as the male'sin changing male mating behavior.     

Pairing success of male Gammarus lacustris infected by two acanthocephalans: a comparative study

The costs of parasitism to host reproduction can be best assessedusing field studies to determine overall mating success andexperimental studies to examine how parasites may affect matingbehavior. We compared the influence of two parasites, Polymorphusparadoxus and P. marilis (Acanthocephala), on the pairing successof their intermediate host (Gammarus lacustris, Crustacea) inboth the field and laboratory. Parasitism significantly loweredthe pairing success of male gammarids. In the field, P. paradoxus-infectedmales paired significantly less often than P. marilis-infectedor uninfected males. Those infected by P. marilis were alsofound in precopula significandy less often than uninfected ones.In the laboratory, the pairing success of males infected byeither parasite was significantly reduced in both competitiveand noncompetitive situations. As in the field studies, thepairing success of P. paradoxus-infected males was significantlylower than that of P. marilis-infected and uninfected males.Polymorphus marilis-infected males were also outcompeted byuninfected individuals, however, their pairing success improvedwhen alone with a female (noncompetitive experiments). We relatethe differential influence of the two parasites on the pairingsuccess of male gammarids to their effects on the physiologyand behavior of G. lacustris.     

Personality of Wild Male Crested Macaques (Macaca nigra)

Animal personalities, i.e. consistent differences in behavior across time and/or context, have received increased attention of behavioral biologists over the last years. Recent research shows that personalities represent traits on which natural and sexual selection work and which can have substantial fitness consequences. The aim of this study is to establish the personality structure of crested macaque (Macaca nigra) males as foundation for future studies on its adaptive value. We collected behavioral data through focal animal sampling and additionally conducted two sets of playback experiments. Results of a factor analysis on the behavioral data revealed a four factor structure with components we labeled Anxiety, Sociability, Connectedness and Aggressiveness. Results from the experiments revealed an additional and independent Boldness factor but the absence of Neophilia. Overall, this structure resembles other macaque and animal species with the exception of Connectedness, which might be a consequence of the species'' tolerant social style. Our results thus not only form the basis for future studies on the adaptive value of personality in crested macaques but also contribute an important data point for investigating the evolution of personality structure from a comparative perspective by refining, for example, which personality factors characterized the last common ancestor of hominids and macaques.     

Laboratory Research on Behavioral Interactions as Generators of Population Phenomena in Rodents

Many population phenomena are driven by the behavior of individualanimals. The effects of behavior on differential reproductionvary with the mating system and with ecological factors; understandingof the complex interactions requires both laboratory and fieldresearch. Ecologically-relevant laboratory research should bedesigned using generalizable behavioral patterns with animalsof appropriate species, meaningful genotypes, and known earlyexperience that are studied in carefully-designed situations.Three exemplars of research of potential relevance to populationphenomena are discussed. Studies of dominance and differentialreproduction in deer mice in seminatural enclosures suggestthat dominant males make disproportionately large contributionsto gene pools and that dominance may be heritable. Laboratorystudies of reproductive function in individuals bearing differentalleles, determined electrophoretically, appear relevant topopulation processes reported correlated with changes in genefrequencies at these loci. Patterns of mate choice in two speciesof Microtus may be important in generating their contrastingmating systems in the field. Well-designed laboratory researchcan help reveal behavioral processes critical to populationphenomena.     

The baby effect and young male syndrome: social influences on cooperative risk-taking in women and men

Parental investment theory predicts differences in risk-taking for females and males as a consequence of reproductive context, with females attempting to reduce risks in relation to their own offspring (here called the baby effect) and males taking more risks in competition with one another (young male syndrome). The experiment we report tests these predictions in a cooperative context by introducing the Social Balloon Analogue Risk Task—the Balloon Analogue Risk Task modified to include a social partner (adult male, adult female, or baby)—along with a commitment device in which participants choose among several possible social partners, with whom they will share their earnings. Results were consistent with the predictions of parental investment theory. Females did not change their levels of risk-taking when paired with adult males or females, but showed a strong reduction in risk when paired with babies. Consistent with previous research, males were strongly inclined to take more risks when paired with another male of the same age, but males showed no change in risk-taking when paired with a female of the same age or a child. The current work provides the first experimental evidence of gender differences in cooperative social risk-taking, as well as the first experimental evidence of a mediator of female risk-taking, i.e., babies.     

Caribbean damselfish with varying territory quality: correlated behaviors but not a syndrome

The behavioral syndrome hypothesis suggests that individualanimals within a population behave differently due to specificbehavioral types, and these should be consistent across behaviorsor in different contexts. In contrast, for animals that livewithin an environment in which territory quality can changeover time, natural selection should have favored behavioralflexibility and modulation of the cost of defense in relationto territory quality. This would require assessment of the territoryfollowed by displays of appropriate types and intensities ofbehavior. We examined the territorial behavior of male beaugregorydamselfish (Stegastes leucostictus) by enhancing territory qualityusing artificial breeding sites and comparing their behaviorto males on lower quality natural sites. When male fish weredefending high-quality artificial territories, they had higherlevels of aggression toward male conspecifics and courtshiptoward females than when on low-quality natural territories.We also found that aggression and courtship behaviors were correlatedon natural sites but not on artificial sites. Behaviors werenot correlated within individuals when males switched from naturalto artificial territories or from artificial to natural territories.These results indicate that males assess their current territoriesand adjust behaviors accordingly and that courtship and aggressivebehaviors are not linked within a permanent behavioral syndrome.     

Individual behaviour in firebugs (Pyrrhocoris apterus)

The concept of animal personalities has recently become of major interest as researchers began to wonder why animals within a given population show consistent behaviour across situations and contexts, what led to the evolution of such behavioural inflexibility and what mechanisms might underlie the phenomenon. A recent model explains individual differences in a population as the result of trade-off between present and future reproduction. We tested this model on the two wing morphs, i.e. short-winged (brachypterous) and long-winged (macropterous) specimens of the firebug (Pyrrhocoris apterus). Since it has been already demonstrated that the two wing morphs differ in their life-history strategies, this species is an ideal subject to test whether the specimens with different life-history strategies have different personalities as well. The results show that individuals behave consistently over time and across contexts, meaning observed bugs do have personalities. We also have found that in females, the two wing morphs have different personalities supporting the theoretical predictions, i.e. winged ones, which are supposed to have lower future reproductive value, are braver and more exploratory. We found no difference between the morphs in males. Differences in reproductive investment might explain this discrepancy between the sexes.     

Comparative paternal and infanticidal behavior of sympatric white-footed mice (Peromyscus leucopus noveboracensis) and deermice (P. maniculatus nubiterrae)

We studied parental and infanticidal behavior in the field andlaboratory in two ecologically equivalent and sympatric congeners,white-footed mice, Peromyscus leucopus noveboracensis, and deermice,P. maniculatus nubiterrae. Despite their close phylogeneticrelationship and ecological similarity, various aspects of parentaland nesting behavior of the two species were significantly different.P. maniculatus males were more paternal than were P. leucopusmales in that they retrieved pups, nested with pregnant femalesand females with newborn pups, and formed longer associationswith females than did P. leucopus males. Thus, P. m. nubiterraeexhibited more pair-bonding (monogamous) characteristics thandid either P. leucopus or P. m. bairdi, as reported in otherstudies. The behavioral differences may represent the differentevolutionary history of the three subspecies. Infanticidal behavior,however, was similar in both species. Dispersing and unmatedmales killed strange pups placed in experimental test chambersin the field, whereas mated males did not kill pups within theirown home ranges. Resident females of both species were moreinfanticidal than were males, killing pups in 90% of the trials.The results support the sexual selection and resource competitionhypotheses for male and female infanticide, respectively. [BehavEcol 1991; 2: 38-45]     

Social Information Embedded in Vocalizations Induces Neurogenomic and Behavioral Responses

Social cues facilitate relationships within communities. Zebra finches form long-term stable mate pairs and produce offspring within a multi-family, multi-generational community that can include hundreds of birds. Males use song to communicate in this complex environment. Males sing as part of their courtship display but also abundantly throughout each day, suggesting a role for their vocal signature outside of a reproductive context. One advantage of a vocal social cue is that it can be exchanged when birds are out of visual contact, as regularly occurs in a zebra finch community. Previous works have demonstrated that females hearing song are affected by their social relationship to the bird singing it, and the immediate social context. Here, we probed the question of whether or not the song itself carried social information, as would be expected from the situations when males sing outside of view of the female. We quantified behavioral and neurogenomic responses to two songs we predicted would have distinct “attractive” qualities in adult females housed in either mixed sex or female-only social communities. Our results show that only mixed sex-housed females show distinctive behavioral and neurogenomic responses to attractive songs. These data are consistent with the idea that the acoustic properties of song carry social information, and that the current social situation modulates the neural and behavioral responses to these signals.     

Zebra finches are bolder in an asocial, rather than social, context

Despite an expanding interest in animal personalities, the influence of social interactions and sex differences on individual differences in behaviour remains poorly understood. Using the social zebra finch (Taeniopygia guttata), we tested for behavioural differences in exploration of a novel environment and objects, between individuals of both sexes in relation to a social context; the presence of three male companions, three female companions or no companion birds. We predicted that the presence of conspecific companions should result in focal birds reacting to novelty by exploring more extensively because the companion birds contribute to anti-predator vigilance behaviour and because social isolation often causes behavioural inhibition in social species. We found that exploratory behaviour of focal individuals was significantly reduced in the presence of conspecific companions, irrespective of the companion's sex. Moreover, we found a weak trend towards females being more exploratory than males, irrespective of the social context. These results demonstrate the importance of considering the social context in animal personality studies and of exploring sex differences in personalities.     

A Neuroethological Study of Display Behavior in the Lizard Anolis Carolinensis (Reptilia, Lacertilia, Iguanidae)

A behavior inventory and ethogram for display behavior, an atlasof the principal forebrain nuclei and fiber tracts, and microtechniquesfor stereotaxic surgery were developed in conjunction with astudy of forebrain involvement in the display behavior of Anoliscarolinensis In a behavior inventory of 100 units consistingof states and events, forty-seven were observed exclusivelyor frequently in social situations. An analysis of the effectsof forebrain lesions on two stereotyped displays indicated involvementof the striatal area of the basal forebrain in species-typical"challenge" displays that are characteristic of territorialencounters between adult conspecifics. "Assertive" displaysassociated with elevated behavioral arousal were not significantlyaffected Lesions confined to the dorsal ventricular ridge resultedin no significant deficits in either display type.     

Functional relationships between genotypes and environments in behavior. Effects of different kinds of early social experience on interstrain fighting in male mice

Comparisons are made of the interstrain fighting behavior of adult male mice from two inbred strains (ST-albino; CBA-black-agouti), raised in one of three postweaning social situations: 1) isolated from other males, 2) reared with males of the same strains, or 3) reared with males of the opposite strain. Using the fighting behavior of isolated males as a baseline, it is found that each type of early social experience affects the fighting behavior of the males from each of the two inbred strains differently, indicating that the functional relationships between genotype and environment studied in these experiments are nonadditive. The importance of these results in describing the norm of reaction of a behavioral phenotype and in extrapolating data from one experiment to another is discussed.