Anxiolytic-like effects of substance P fragment (SP(1-7)) in non-human primates (Callithrix penicillata)

The behavioral effects of the amino (N)-terminal fragment of substance P (SP(1-7)) on the marmoset (Callithrix penicillata) predator confrontation test of fear/anxiety were investigated. The test apparatus consisted of a figure-eight maze with three parallel arms interconnected at each extremity to a perpendicular arm. A taxidermized oncilla cat (Felis tigrina) was placed outside the maze facing one of its corners. Subjects were submitted to seven 30 min maze habituation trials (HTs), in the absence of the 'predator', and then to six 30 min treatment trials (TTs), in the presence of the 'predator', consisting of four doses of SP(1-7) (5, 50, 250 and 500 microg/kg; IP), saline and sham injection. SP(1-7) treatment reversed, in a dose-dependent way, the fear-induced avoidance behavior due to the predator's presence and increased the frequency of exploratory behaviors. Locomotor activity decreased during successive HTs, yet increased after all SP(1-7) treatments. These results indicate that systemic administration of SP(1-7) produces anxiolytic-like effects in marmosets tested in the predator confrontation model of fear/anxiety.     

Rapid habituation of scan behavior in captive marmosets following brief predator encounters

Scan behavior in 10 captive predator-naive adult black tufted-ear marmosets (Callithrix penicillata) was investigated prior, during and following brief predator encounters (taxidermized oncilla cat -- Leopardus tigrinus) versus neutral stimulus exposures (stuffed toy). For each stimulus, three 9 min home-cage trials were conducted > or = 72 h apart. Each trial was divided into three consecutive 3 min intervals: pre-exposure baseline observation, stimulus exposure, and post-exposure observation period. Post-exposure scan duration increased during the first two predator confrontations, while scan frequency increased significantly only after the first. Scan behavior remained constant within the last predator encounter, as it also did within and between the three neutral stimulus exposures. Although marmosets scanned more often and significantly longer after encountering the predator than the neutral stimulus, this response rapidly habituated by the second trial. Therefore, black tufted-ear marmosets in a familiar environment rapidly habituate to brief repeated predator encounters, possibly minimizing anti-predation costs once the degree of a potential threat has been adequately assessed.     

Visual scanning by common marmosets (Callithrix jacchus): Functional aspects and the specialrrole of adult males

The rates of visual scanning and vocalizations were studied in a group of captive marmosets (Callinthrix jacchus) after the presentation of five different stimuli (artificial flower, playback of long calls, female/male conspecific, stuffed wild cat) in order to assess the function of visual scanning. Only the presentation of a stuffed cat induced a significant response. The adult males in particular increased their scanning rate and all adult individuals decreased their rate of vocalizations. The results indicate that visual scanning in marmosets is an appropriate measure of vigilance which seems to serve the function of predator detection and avoidance. The strong response of adult males suggests that they play a special role in predator detection.     

Disturbances by dog barking increase vigilance in coots Fulica atra

Animals frequently interrupt their activity to look up and to scan their surrounding environment for potential predators (vigilance). As vigilance and other activities are often mutually exclusive, such behaviours are at the expense of feeding, sleeping or preening. Authors of many wildlife disturbance studies found that people with free-running dogs provoked the most pronounced disturbances (e.g. greater flushing distances and more birds affected). However, dogs on leash may also negatively affect wild animals, and barking dogs may lead to an increase in vigilance. In this study, I tested this hypothesis in coots (Fulica atra) using three different playback procedures: (1) dog barks, (2) conspecific coot alarm calls and (3) chaffinch song. The trials were conducted in spring and autumn 2005 at three study sites in southwestern Germany. During the dog playbacks, vigilance increased significantly from 17 to 28%. This increase in vigilance is comparable to the presence of a natural predator. As expected, vigilance also increased significantly during conspecific coot alarm calls but not during playbacks of the chaffinch song control. Two main findings result from the study: (1) coots respond to acoustic traits of dogs and may be able to acoustically recognise this predator and (2) this increase in vigilance might have implications for conservation, especially when considering buffer zones around sensitive areas.     

Differences in aerial and terrestrial visual scanning in captive black tufted-ear marmosets (Callithrix penicillata) exposed to a novel environment

Aerial and terrestrial visual scanning were investigated in captive black tufted-ear marmosets, Callithrix penicillata, exposed to a novel environment. Naive adult subjects (n=24) were individually exposed to a figure-eight maze during seven 30-min trials, 48 h apart. Habituation to the maze was observed, as indicated by the significant decrease in locomotion. The frequency of aerial scanning, however, remained elevated throughout the 7 trials, while its duration rapidly increased to high levels. Frequency and duration of terrestrial scanning persisted at constant low rates, differing significantly from aerial scanning. Males and females did not differ significantly. The different impact of aerial versus terrestrial predators could have a significant influence on vigilant behaviour in this species. Thus, visual scanning is an important and highly organized antipredation strategy in marmosets.     

Sleep quantitation in common marmoset, cotton top tamarin and squirrel monkey by non-invasive actigraphy

Sleep quantitation data on the Neotropical primate species, apart from the squirrel monkey, are still sparse. As such, we have quantitated sleep in the common marmosets (Callithrix jacchus), cotton top tamarins (Saguinus oedipus) and squirrel monkeys (Saimiri sciureus) reared in one primate facility simultaneously, by non-invasive actigraphy. The range in total sleep time/24h measured for male adult common marmosets, cotton top tamarins and squirrel monkeys were 713-793 min (n=4), 707-889 min (n=4) and 459-475 min (n=2) respectively. The range in sleep episode length /12h dark phase for marmosets, tamarins and squirrel monkeys were 21-52 min (n=3), 10-28 min (n=4) and 9-15 min (n=2) respectively. Since vigilance is a critical evolutionary adaptive feature of predator avoidance among Callitrichid monkeys and squirrel monkeys, the shorter ranges in sleep episode length recorded, even under captivity, in this study could be interpreted as probable indicators of such vigilance behavior during the rest phase. We hypothesize that the vigilance behavior when it exists during a primate's active phase should also prevail when it is at rest (sleep). This hypothesis deserves additional testing in female Callitrichid monkeys.     

Immediate, but no delayed, behavioral response to a snake model by captive black tufted-ear marmosets

Whether callitrichids are naturally capable of detecting and responding to predators - or if such skills are learned - remains a controversial issue, with results differing in terms of species, predator and encounter conditions. Therefore, the behavioral response of naïve adult captive black tufted-ear marmosets (Callithrix penicillata) was assessed before, during, 0 and 4 h after a 5-min encounter with a snake and flower model. Using a two-phase cross-over design, marmosets (n = 16) were submitted to one trial for each stimulus, divided into four 5-min intervals: pre-exposure, exposure and post-exposure observations held 0 and 4 h later. The snake exposure increased the number of gazes made towards the stimulus and the time cage-mates spent close to each other, as well as induced tsik-tsik alarm/mobbing calls, while inhibiting foraging and decreasing the time spent near the snake's location. After the snake was removed, all changes were immediately reversed. Mobbing was not observed. The flower stimulus only increased direct gazes and time spent in proximity during its presentation. All marmosets were captive-born and snake-naïve yet had recently been confronted with a cat stimulus in a previous experiment. Thus, previous experiences with snakes may be required for marmosets to fully develop appropriate immediate and long-term responses.     

Pre-retirement predator encounters alter the morning behavior of captive marmosets (Callithrix geoffroyi)

Limited data are available on the long-term effect an encounter with a predator has on its potential prey. Anecdotal reports from field research indicate that even unsuccessful attacks by predators on callitrichids have long-lasting effects. The subjects for this study were two groups of Geoffroy's marmosets (Callithrix geoffroyi) housed outside, off exhibit, at the Center for Reproduction of Endangered Species at the San Diego Wild Animal Park. Before they retired in the evening, the marmosets were observed under one of three conditions: snake model, cloth control, and no-stimulus control. Data were collected the following morning for 1 hr after the animals emerged from the sleeping box. Compared to control conditions, exposure to the snake model before retirement the previous evening was associated with significantly more vigilance checks (i.e., inspecting the area where the stimulus was last seen), and a delay in beginning to forage on the ground. These results suggest that callitrichids use recent threatening experiences to guide their vigilance behavior 12 hr after the threat is detected, and that they adjust their early morning behavior in response to potential predatory threats.     

Effect of Male Emigration on the Vigilance Behavior of Coresident Males in White-Faced Capuchins (Cebus capucinus)

I examined the vigilance behavior of male Cebus capucinus residing in four groups in Santa Rosa Park, Costa Rica. One male emigrated from each of three study groups, providing ideal experimental conditions for examining the effect of coresident males on male vigilance behavior (social and non-social). Following the predator and conspecific defense theories for the adaptive value of male vigilance behavior and the occurrence of multimale groups, I predicted that male nonsocial vigilance would increase after the emigration of a coresident male. My prediction was supported in only one of the three study groups. Males in two groups decreased their nonsocial vigilance after the emigration of a coresident male, which was probably influenced by seasonal changes and the peripherality of one group's coresident male before his emigration. The social vigilance hypothesis proposes that for species with rigid dominance hierarchies, social vigilance should increase with an increase in same sex competitors. Therefore, I predicted that male social vigilance would decrease after the emigration of a coresident male. The hypothesis is generally supported in my findings, as two of the three groups displayed a decrease in social vigilance after the emigration of a coresident male. Increased social vigilance in the third group is best explained by the change in the alpha male's social behavior after the emigration of his only coresident male.     

Individual Behavioural Strategies Associated with Predator Inspection in Minnow Shoals

When confronted with a live pike, Esox lucius, European minnows, Phoxinus phoxinus, showed individual differences in rate of predator inspection. Predator inspection behaviour, in which single individuals or small groups approached the predator, was ordinated with several other behavioural parameters using principal components analysis. Individual minnows showed one of two strategies. Fish with high inspection rates were bolder, skittered more frequently and fed more persistently than fish with low inspection rates. Fish with low inspection rates showed the opposite strategy. Individuals did not show habituation of predator inspection during trials or over the experimental period.     

Behavioural Responses of European Roe Deer to Temporal Variation in Predation Risk

In natural environments, predation risk varies over time. The risk allocation hypothesis predicts that prey is expected to adjust key anti‐predator behaviours such as vigilance to temporal variation in risk. We tested the predictions of the risk allocation hypothesis in a natural environment where both a species‐rich natural predator community and human hunters are abundant and where the differences in seasonal and circadian activity between natural and anthropogenic predators provided a unique opportunity to quantify the contributions of different predator classes to anti‐predator behaviour. Whereas natural predators were expected to show similar levels of activity throughout the seasons, hunter activity was high during the daytime during a clearly defined hunting season. According to the risk allocation hypothesis, vigilance should then be higher during the hunting season and during daytime hours than during the non‐hunting season and night‐time hours. Roe deer (Capreolus capreolus) on the edge of Bia?owie?a Primeval Forest in Eastern Poland displayed vigilance behaviour consistent with these predictions. The behavioural response of roe deer to temporarily varying predation risks emphasises the behavioural plasticity of this species and suggests that future studies of anti‐predator behaviour need to incorporate circadian variation in predation pressure as well as risk gradients of both natural and anthropogenic predators.     

Behavioral and cardiophysiological responses of common marmosets (<Emphasis Type="Italic">Callithrix jacchus</Emphasis>) to confrontations with opposite-sexed strangers

Common marmosets exhibit under captive conditions socially monogamous propensities. During confrontation with opposite-sexed stranger, in the presence of the pairmate, common marmosets often respond aggressively. However, in the absence of their mates, males actively solicit contact and even sexual interactions with strange females whereas mated females are indifferent to strange males. In the present study behavioral and cardiophysiological responses of pairmates of six established pairs of common marmosets were recorded during confrontation with an opposite-sexed stranger (1) in the presence or (2) in the absence of the familiar pairmate. Systolic and diastolic blood pressure, heart rate as well as locomotor activity were recorded telemetrically through peritoneally implanted transmitters. Behavioral responses were videotaped and in addition, urine samples from the female individuals were analyzed for their estrogen concentrations to monitor their ovarian cycles. The cardiophysiological values did not differ significantly between the two confrontation conditions. However, compared to baseline, heart rate values of both sexes and in males also blood pressure values, were significantly higher during confrontations. Hence, confrontations with an opposite-sexed conspecific clearly affect cardiophysiological parameters. Between confrontees affiliative behaviors could not been recorded but aggressive and sexual behaviors occurred.     

Bimodal temporal organization of specific vigilance behaviors in captive black tufted-ear marmosets (Callithrix penicillata)

The aerial/terrestrial scan and glance behaviors of 20 captive adult black tufted-ear marmosets (Callithrix penicillata), kept undisturbed in their own familiar social environments, were assessed at 07:00, 09:00, 11:00, 13:00 and 15:00 h, as little is known on the temporal organization of their vigilance repertoire, particularly under normal social and stress-free conditions. For each time point, four 20-min observation sessions were held. Although general high vigilance rates were observed, significantly more time was spent scanning the upper part of the home-cage, particularly during the earliest and latest hours of the day. Significantly higher terrestrial than aerial glance frequencies were also seen, yet both remained constant throughout the day. Therefore, the observed pattern not only varied significantly according to the specific vigilance behavior and time of day, but also seemed associated with eco-physiological factors, such as the search/intake of food, sleep site selection and higher risk of air-born threats.     

Behavioral and cardiophysiological responses of common marmosets (Callithrix jacchus) to social and environmental changes

Under captive conditions common marmosets (Callithrix jacchus) show socially monogamous propensities. Male and female form a social bond as characterized by signs of behavioral arousal during separation of the pairmates, high levels of affiliative interactions between pairmates and agonistic responses towards strange conspecifics. In the present study behavioral and cardiophysiological responses of mated individuals of common marmosets were recorded while the animals were in an unfamiliar environment (1) alone, (2) with the pairmate, or (3) with an opposite-sexed stranger. Pairmates of 6 established pairs were tested in 3 replicates yielding a total of 36 trials per experiment. A trial was divided into three 10-min segments (baseline; unfamiliar environment; reunion). Behavioral responses were videotaped with a remote controlled camera system installed within the cage. Systolic (SBP) and diastolic blood pressure (DBP), and heart rate (HR) as well as locomotor activity (ACT) were recorded telemtrically through peritoneally implanted transmitters. The individuals’ responses measured while in an unfamiliar environment was only reduced by the pairmate, but not by an opposite-sexed stranger. No affiliative behaviors occurred between strange conspecifics, whereas aggressive and sexual behaviors were observed. During reunion with the pairmate individuals recovered physiologically. The present study shows that an individualized pair bond exists between pairmates of common marmosets. Further, it becomes evident that establishing a social bond with the pairmate is important for maintaining physiological homeostasis.     

Reactions to Potential Predators in Captive-Born Marmosets (Callithrix penicillata)

We describe the behavioral repertoire of captive-born black tufted-eared marmosets (Callithrix penicillata) elicited by brief exposures to three potential mounted taxidermized predators (caracara hawk, Polyborus plancus; rattlesnake, Crotalus durissus; oncilla, Leopardus tigrina), and a stuffed toy. For each of the four stimuli, we submitted the subjects to a 9-min trial divided into three consecutive intervals: a 4-min pre-exposure baseline observation, a 1-min stimulus exposure, and a 4-min postexposure observation period. We positioned stimuli in front of each subject's home cage, and video-taped trials for behavioral analysis. During exposures to the potential taxidermized predators, we heard tsik-tsik vocalization and alarm behavior. After exposures, only the cat induced these reactions. All stimuli elicited observational reaction, albeit only during exposure intervals. Further comparisons between the three trial intervals indicated a decrease in the time spent in proximity to the cat during exposures, while an increase in proximity occurred when subjects were exposed to either the hawk or snake for the same period. Taken together, the behavioral responses during and after exposures to the taxidermized oncilla suggest that this stimulus is capable of inducing strong and persistent emotional reactions in Callithrix penicillata.     

A Test of the Multi-Predator Hypothesis: Rapid Loss of Antipredator Behavior after 130 years of Isolation

Many species find themselves isolated from the predators with which they evolved. Isolation often leads to the loss of costly antipredator behavior, which may have adverse consequences if the population should later come into contact with predators. An understanding of both the mechanism (i.e. the degree to which antipredator behavior depends on experience), and of the time course of loss is important to be able to predict how a population will respond to future contact. We studied ‘group‐size effects’– the way in which animals change the time they allocate to antipredator vigilance as a function of group size – and visual and acoustic predator recognition in a population of tammar wallabies (Macropus eugenii), a cat‐sized (6–10 kg) macropodid marsupial. To study group size effects we observed wallabies foraging in four populations – three with some sort of predator and a New Zealand population that was isolated from all predators for about 130 yr. To study predator recognition, we observed the response of New Zealand wallabies to the presentation of a model or taxidermic mount of mammalian predators, and to the broadcast sounds of mammalian and avian predators. We compare these predator recognition experiments with results from a previous study of Kangaroo Island (South Australia) tammars. Complete isolation from all predators for as few as 130 yr led to the loss of group size effects and a rapid breakdown in visual predator recognition abilities. Our results are consistent with a key prediction of the multi‐predator hypothesis – namely, that the isolation from all predators may lead to a rapid loss of antipredator behavior.     

Predator Avoidance of Transgenic Channel Catfish Containing Salmonid Growth Hormone Genes

Transgenic channel catfish (Ictalurus punctatus) containing salmonid growth hormone genes can grow 33% faster than normal channel catfish under aquaculture conditions. However, before transgenic catfish are released and utilized by the private sector, their genetic impact on the natural environment must be examined. Predator avoidance is one of the major fitness traits determining potential environmental risk. To determine the predator avoidance ability and growth performance of transgenic catfish in a natural habitat, various densities of transgenic and nontransgenic channel catfish were communally stocked in 0.04-ha earthen ponds without supplemental feeding. Largemouth bass (Micropterus salmoides) and green sunfish (Lepomis cyanellus) were stocked as predators. Nontransgenic fry had better predator avoidance than transgenic channel catfish when data were pooled (p < .01). When data were not pooled, nontransgenic catfish had better predator avoidance in six trials and transgenic individuals had better predator avoidance in four trials. There was no difference in predator avoidance in three trials. Overall predator avoidance was also better for nontransgenic individuals (p < .01) when the fish were evaluated as 3.5-g fingerlings, more clearly than as fry, as transgenic individuals were more vulnerable in 3 of 4 trials at this life stage. There was no significant difference in growth performance between transgenic and nontransgenic channel catfish in ponds without supplemental feeding. These findings indicate that transgenic channel catfish could be used for commercial aquaculture without affecting the natural environment. Although transgenic channel catfish may be released to nature by accident, any ecological effect would be unlikely because the increased susceptibility of transgenic channel catfish to predators would most likely decrease or eliminate the transgenic genotype. Received March 8, 1999; accepted June 3, 1999.     

Effects of acidic-astressin and ovine-CRF microinfusions into the ventral hippocampus on defensive behaviors in rats

This study investigated a possible role for ventral hippocampal corticotropin-releasing factor (CRF) in modulating both unconditioned and conditioned defensive behaviors by examining the effects of pre-training ventral hippocampal ovine-CRF (oCRF) or acidic-astressin ([Glu^11,16]Ast) microinfusions in male Long-Evans hooded rats exposed to various threat stimuli including the elevated plus-maze (EPM) (oCRF), cat odor (oCRF and [Glu^11,16]Ast) and a live cat ([Glu^11,16]Ast). Unconditioned defensive behaviors were assessed during threat exposure, while conditioned defensive behaviors were assessed in each predator context 24 h after the initial threat encounter. Pre-training infusions of the CRF₁ and CRF₂ receptor agonist oCRF significantly increased defensive behaviors during both the unconditioned and conditioned components of the cat odor test, as well as exposure to the EPM. In contrast to the behavioral effects of oCRF microinfusions, the CRF₁ and CRF₂ receptor antagonist [Glu^11,16]Ast significantly decreased defensive behaviors during exposure to cat odor, while producing no discernible effects following a second injection in the cat exposure test. During conditioned test trials, pre-training infusions of [Glu^11,16]Ast also significantly reduced defensive behaviors during re-exposure to both predator contexts. These results suggest a specific role for ventral hippocampal CRF receptors in modulating anxiety-like behaviors in several ethologically relevant animal models of defense.     

Vigilance and group size in ostriches

Wild ostriches were observed while feeding alone or in groups of up to four birds, and their vigilance (proportion of time with the head up) recorded. Individual vigilance declined as group size increased, mainly through a decrease in the frequency with which the head was raised. Males were more vigilant than females, mainly because they kept their heads up for longer. Vigilance was influenced more by the presence than by the vigilance of a companion. When a head would stay down for a long time was impossible for a predator to predict. It is concluded that grouping by ostriches when feeding results in only a slight reduction in the group's vulnerability to successful predator attack, but in a considerable decrease in individual vulnerability.     

Source Odor,Intensity, and Exposure Pattern Affect Antipredatory Responses in the Subterranean Rodent Ctenomys talarum

Predation is a strong selective force, and prey species may show specific adaptations that allow recognition, avoidance, and defense against predators. Facing a situation of predatory risk, anxiety constitutes a reaction of adaptive value, allowing to evaluate the potential risk of this encounter as well as to generate a physiological and behavioral response. Previous studies in the subterranean rodent Ctenomys talarum revealed that exposure to predator odors (urine or fur) generates an anxiety state and induces behavioral changes. However, no differences between the responses generated by both odor sources were observed, although fur odors may indicate a higher level of predatory immanence. Therefore, the aim of this study was to evaluate the behavioral and physiological responses of C. talarum to different intensities of predator odors (urine and fur) and to the repeated exposition to the same odorous stimulus. When comparing the highest behavioral effects elicited by both predatory odors on C. talarum, our study supports the assumption that fur odors are more anxiogenic than urine, while the former provoked significant changes in the distance traveled, the number of arm entries and time in transparent arms in the elevated plus maze; cat urine only caused slight changes on those behavioral parameters. Furthermore, we also found that the intensity of natural predator odor presented to tuco‐tucos has a role on the appearance of defensive behaviors, although an amount‐dependent relationship between predator odor and anxiety levels was not observed. Finally, while individuals exposed for 1 day to fur odor displayed an evident anxiety state, those exposed repeatedly for 5 consecutive days did not differ with the control group in their behavioral response, indicating a clear habituation to the predatory cue. In our intensity and habituation experiments, we did not find differences in the measured physiological parameters among control individuals, exposed to different cues intensity (urine and fur odor) and exposed only once or for 5 days to fur odor. These results provide valuable evidence that the types of predatory odor, along with the frequency of exposition, are important determinants of the appearance, strength, and extinction of defensive behaviors in the subterranean rodent C. talarum.