Time-place learning in individually reared angelfish, but not in pearl cichlid

Time-place learning based on food association was investigated in the cichlids angelfish (Pterophyllum scalare) and pearl cichlid (Geophagus brasiliensis) reared in isolation, therefore eliminating social influence on foraging. During a 30-day period, food was placed in one side of the aquarium (containing three compartments) in the morning and in the opposite side in the afternoon. Learning was inferred by the number of correct side choices of all fish in each day of test (15th and 30th). During the test day fish were not fed. The angelfish learned to switch sides at the correct day period in order to get food, suggesting this species has time-place learning ability when individually reared. On the other hand, the same was not observed for pearl cichlid.     

The presence of the dam affects the efficiency of gentling and feeding on the early establishment of the stockperson-lamb relationship

This experiment investigates how the maternal presence influences the effect of additional human contact in early age on the reaction of lambs to their stockperson. Forty twin-born lambs were involved in this experiment during their first 4 days of life. Ten pairs of twins were reared artificially from 12h of age. One of each litter (AF, n=10) received 6.5+/-0.7 sessions of 30min of separation from the twin (with a wire fence) with 5min of gentling and feeding (suckling from a bottle and from a bucket fitted with a rubber teat). The other twin was not treated. Ten pairs of twins were reared with their dam and received 6.6+/-0.7 sessions of treatment. One twin (MAF, n=10) received the same treatment as AF. The other twin (M, n=10) was separated for 30min from the dam and had no human contact. From the age of 70+/-7h, lambs were tested in a social isolation test (alone for 1min, with the familiar stockman for 2min, alone again for 1min), in a Preference test (2min) between an unfamiliar maternal ewe and the familiar stockman, and, for the AF lambs only, in a Preference test (2min) between their familiar and an unfamiliar stockman. Eight AF lambs learned to suck on their own from the bucket of milk by the end of the experiment compared to only one MAF (P<0.001). AF lambs approached the human more (P<0.01), vocalised less (P<0.01) and walked less (P<0.01) during the social isolation test than animals reared with their mother (M and MAF). AF did not show any preference between the stockman and the unfamiliar maternal ewe while M and MAF lambs chose the ewe (P<0.05). AF lambs discriminated the familiar from an unfamiliar stockman only if they had learned to suck from the bucket during the treatment. Nevertheless MAF lambs vocalised less than M (P<0.05) in the presence of the stockman during the social isolation test, indicating a possible reduction of isolation distress. These results show that artificially reared lambs are preferentially motivated to interact with a familiar human after only a few days of contact. Moreover, they highlight the difficulty in using a feeding reward to improve the human-lamb relationship when lambs are reared permanently with their dams. However, the results suggest that early gentling improves the human-animal relationship whatever the maternal environment.     

Attraction to and learning from social cues in fruitfly larvae

We examined the use of social information in fruitfly larvae, which represent an ideal model system owing to their robust learning abilities, small number of neurons and well-studied neurogenetics. Focal larvae showed attraction to the distinct odour emanating from food occupied by other larvae. In controlled learning experiments, focal larvae preferred novel odours previously paired with food occupied by other larvae over novel odours previously paired with unoccupied food. When we gave groups of larvae a choice between food patches differing in quality, more larvae aggregated on the higher-quality food, suggesting that attraction to and learning about cues associated with other larvae can be beneficial. Furthermore, larvae were more likely to find the best available food patch in trials when that food patch was occupied by other larvae than in trials when that food patch was unoccupied. Our data suggest, however, that the benefits from joining others may be at least partially offset by the fitness costs of increased competition, because larvae reared in isolation did as well as or better than larvae reared in groups on three key fitness parameters: developmental rate, survival rate and adult dry body mass. Our work establishes fruitfly larvae as a highly tractable model species for further research on the mechanisms that modulate behaviour and learning in a social context.     

Effects of Degree and Timing of Social Housing on Reversal Learning and Response to Novel Objects in Dairy Calves

Rodents and primates deprived of early social contact exhibit deficits in learning and behavioural flexibility. They often also exhibit apparent signs of elevated anxiety, although the relationship between these effects has not been studied. To investigate whether dairy calves are similarly affected, we first compared calves housed in standard individual pens (n = 7) to those housed in a dynamic group with access to their mothers (n = 8). All calves learned to approach the correct stimulus in a visual discrimination task. Only one individually housed calf was able to re-learn the task when the stimuli were reversed, compared to all but one calf from the group. A second experiment investigated whether this effect might be explained by anxiety in individually housed animals interfering with their learning, and tested varying degrees of social contact in addition to the complex group: pair housing beginning early (approximately 6 days old) and late (6 weeks old). Again, fewer individually reared calves learned the reversal task (2 of 10 or 20%) compared to early paired and grouped calves (16 of 21 or 76% of calves). Late paired calves had intermediate success. Individually housed calves were slower to touch novel objects, but the magnitude of the fear response did not correlate with reversal performance. We conclude that individually housed calves have learning deficits, but these deficits were not likely associated with increased anxiety.     

Endocrine effects of social stimuli on maturing queens of the dampwood termite Zootermopsis angusticollis

Abstract.  The reproductive physiology of social insects is often highly responsive to social stimuli from nestmates, but the mechanisms underlying this sensitivity are usually poorly understood. The effect of varied social conditions on the endocrinology and ovarian maturation in maturing female primary reproductives of the dampwood termite Zootermopsis angusticollis Hagen is studied to better understand their developmental responses to conspecifics. Newly dealate queens are paired with a reproductive male, with another maturing female, or are allowed to mature in isolation. Developmental responses are tracked by monitoring rates of juvenile hormone (JH) production by corpora allata in vitro , haemolymph ecdysteroids titres and ovarian development after 5, 10, 15 and 30 days of maturation. Significant declines in rates of JH production rates are observed by days 5, 10 and 30, respectively, for females paired with males, left to mature in isolation or paired with a female. Ecdysteroid titres increase by day 5 and stay elevated in females nesting with males. By contrast, for CA from females that are isolated or paired with another female, the titres decline and stay low until at least day 15, but increase significantly by day 30. These hormonal differences correspond to differential rates of physiological maturation, with more rapid ovarian development occurring in females paired with a male, than in those nesting alone or with another female. The results suggest that JH and ecdysteroids modulate the ovarian response of alates to stimuli from nestmates during this period of maturation, and that JH and ecdysteroid titres may be regulated independently during this period of development.     

A few days of social separation affects yearling horses' response to emotional reactivity tests and enhances learning performance

Learning performance is influenced by emotional reactivity, low reactivity being generally beneficial. Previous experiments show that emotional reactivity can be modified after a period of social isolation. We hypothesized that eleven days of isolation would affect yearlings' emotional reactivity and improve their learning abilities. Twenty-five yearlings were divided into two groups: 12 were continuously isolated for 11 days (isolated) and 13 stayed together (control). During the period of isolation, all yearlings underwent two learning tasks: a habituation procedure in which a novel object was presented for 120 s every day, either when the horse was alone (isolated) or with conspecifics (control); an instrumental learning task in which the yearling had to walk forwards or backwards to obtain a food reward. At the end of the isolation period, animals performed tests to assess aspects of emotional reactivity: reactivity to novelty, to humans, to social separation, to suddenness and to sensory stimuli. Results showed that isolated yearlings habituated more to the novel object than controls and performed better in the instrumental task. Moreover, they were less reactive to novelty, to social separation and to suddenness than controls. Overall, these data suggest that the better performance of isolated yearlings could be explained by a decrease in their emotional reactivity. This article is part of a Special Issue entitled: insert SI title.     

Effect of isolation and conspecific presence in a novel environment on corticosterone concentrations in a social avian species, the zebra finch (Taeniopygia guttata)

Zebra finches are a highly social and monogamous avian species. In the present study, we sought to determine the effect of social isolation (separation from the flock) in a novel environment with and without a conspecific present on the adrenocortical activity of paired and unpaired individuals of this species. With regard to paired birds, we hypothesized that the presence of the mate during isolation from the group would act as a social buffer against the stressful effects of isolation. We observed that 10 but not 30 minutes of social isolation resulted in elevated concentrations of corticosterone in unpaired and paired male zebra finches in comparison to baseline concentrations of corticosterone. Furthermore, the presence of a mate during isolation in a novel environment did not have a buffering effect against increases in corticosterone concentrations. Additionally, to compare concentrations of corticosterone in response to isolation (in a novel environment) to a previously well-established stressor, we subjected groups of birds to restraint. We observed that 10 or 30 minutes of restraint led to significantly higher concentrations of corticosterone as compared to baseline. Finally, to rule out the possibility that merely handling a bird would result in significantly elevated concentrations of corticosterone as compared to baseline samples, we measured corticosterone concentrations 10 or 30 minutes after handling involving capture and release only. Our results suggest that handling alone might have contributed to the elevation of corticosterone in birds exposed to 10 minutes but not 30 minutes of restraint. Handling by itself did not account, however, for the elevated corticosterone in birds socially isolated for 10 minutes.     

Increased Drinking following Social Isolation Rearing: Implications for Polydipsia Associated with Schizophrenia

Primary polydipsia, excessive drinking without known medical cause, is especially associated with a diagnosis of schizophrenia. We used animal models of schizophrenia-like symptoms to examine the effects on schedule-induced polydipsia: post-weaning social isolation rearing, subchronic MK-801 treatment (an NMDA-receptor antagonist) or the two combined. Male, Sprague-Dawley rats reared in groups or in isolation beginning at postnatal day 21 were further divided to receive subchronic MK-801 (0.5 mg/kg twice daily) or saline for 7 days beginning on postnatal day 62. Following a 4-day withdrawal period, all groups were trained on a schedule-induced polydipsia paradigm. Under food-restriction, animals reared in isolation and receiving food pellets at 1-min intervals developed significantly more drinking behavior than those reared with others. The addition of subchronic MK-801 treatment did not significantly augment the amount of water consumed. These findings suggest a predisposition to polydipsia is a schizophrenia-like behavioral effect of post-weaning social isolation.     

Critical and sensitive periods for reversing the effects of mechanosensory deprivation on behavior, nervous system, and development in Caenorhabditis elegans

In these studies the nematode Caenorhabditis elegans was used as a model to investigate ways to reverse the effects of mechanosensory deprivation on behavior and development. Rose et al. (J Neurosci 2005; 25:7159-7168) showed that worms reared in isolation responded significantly less to a mechanical tap stimulus, were significantly smaller, and expressed significantly lower levels of a postsynaptic glutamate receptor subunit on the command interneurons of the tap response circuit and a presynaptic vesicle marker in the tap sensory neurons compared with worms raised in groups. Here, brief mechanical stimulation at any time throughout development reversed the effects of isolation on the response to tap and on postsynaptic glutamate receptor expression on the command interneurons, suggesting there is no critical period for these measures. In contrast to the high level of plasticity in glutamate receptor subunit expression on the interneurons, low levels of stimulation only rescued vesicle expression in the tap sensory neurons early in development and progressively higher levels of stimulation were required as the worm developed, suggesting a sensitive period immediately after hatching, followed by a period of decreasing plasticity. Stimulation during the first three stages of larval development, but not later, rescued the effects of isolation on worm length, suggesting there is a critical period for this measure that ends in the third larval stage. These results indicate that different effects of early isolation required different amounts and/or timing of stimulation to be reversed.     

Effect of age,behaviour and social environment on honey bee brain plasticity

We examined the effects of behaviour, age and social environment on mushroom body volume in adult bees. The mushroom bodies are regions of the central brain important for sensory integration and learning. Their volume was influenced by behaviour throughout life: always larger in forager bees than age-matched nurse bees, even in old bees up to 93 days of age as adults. Mushroom body development was influenced by the social environment in the first 8 days of adult life, with different environments having markedly different effects on mushroom body size. Compared to hive-reared bees, isolation slowed mushroom body growth, but bees reared in isolation confined with a single dead bee showed a dramatic increase in mushroom body volume comparable to that seen in active foragers. Despite their precocious mushroom body development, these bees did not show improved performance in an olfactory learning test. Since simple environmental manipulations can both accelerate and delay mushroom body growth in young bees, and since mushroom body volume is sensitive to behaviour throughout life, the honey bee has great potential as a model for exploring the interactions between environment, behaviour and brain structure.     

The weight of the clan: Even in insects, social isolation can induce a behavioural syndrome

Social isolation has dramatic consequences on the development of individuals of many vertebrate species, and it induces a set of behavioural disturbances rending them unable to process environmental as well as social stimuli appropriately. We hypothesized that isolation syndrome is a ubiquitous trait of social life that can be observed in a wide array of species, including invertebrates. Here we report that gregarious cockroaches (Blattella germanica) reared in isolation showed (i) stronger exploration-avoidance, (ii) reduced foraging activity, (iii) reduced willingness to interact socially, and (iv) reduced ability to assess mating partner quality than conspecifics reared in groups. We demonstrate the occurrence of a behavioural syndrome induced by social isolation, similar to syndromes described in vertebrates, revealing the importance of social interactions and group-living in this non-eusocial insect species. We suggest that investigating social isolation effects on individual development should provide interesting results to assess social cohesion of species and thus constitute an additional tool for comparative studies focusing on the evolution of social life.     

Social influences on nymphal development in the cockroach, Diploptera punctata

Solitary male nymphs of the cockroach Diploptera punctata (Eschscholtz) (Blattaria: Blaberidae) took significantly longer to reach adulthood than males paired with either a male or female nymph or grouped with four other male nymphs since birth. When isolated throughout nymphal development, 15.8% of males passed through 3 stadia before adult eclosion, and the remainder went through 4 stadia. In contrast, 61.3% of paired males became adults in 3 stadia. Males need not, however, be isolated or paired for the entire nymphal period to express isolated or paired patterns of development. About 60% of males paired in just the first stadium or its initial 9 days became adults in 3 stadia, and only 20.4% of males isolated in the first stadium and the first 3 days of the second reached adulthood within 3 stadia. Although the first stadium was a critical period in which social condition determined the course of future development, analyses of covariance showed that isolated males gained less weight than paired ones, not only in the first stadium, but in the second as well. Moreover, the degree of growth of a male in the second stadium, measured as either weight gain or relative growth rate, did not depend on the male's social condition in the first stadium, because isolated second-instar males grew less than paired ones, even when both sets of insects had been paired in the first stadium. Female nymphal development, unlike that of males, was not greatly affected by social factors.     

Sweetened ethanol drinking during social isolation: enhanced intake,resistance to genetic heterogeneity and the emergence of a distinctive drinking pattern in adolescent mice

With its ease of availability during adolescence, sweetened ethanol (‘alcopops’) is consumed within many contexts. We asked here whether genetically based differences in social motivation are associated with how the adolescent social environment impacts voluntary ethanol intake. Mice with previously described differences in sociability (BALB/cJ, C57BL/6J, FVB/NJ and MSM/MsJ strains) were weaned into isolation or same‐sex pairs (postnatal day, PD, 21), and then given continuous access to two fluids on PDs 34–45: one containing water and the other containing an ascending series of saccharin‐sweetened ethanol (3–6–10%). Prior to the introduction of ethanol (PDs 30–33), increased water and food intake was detected in some of the isolation‐reared groups, and controls indicated that isolated mice also consumed more ‘saccharin‐only’ solution. Voluntary drinking of ‘ethanol‐only’ was also higher in a subset of the isolated groups on PDs 46–49. However, sweetened ethanol intake was increased in all isolated strain × sex combinations irrespective of genotype. Surprisingly, blood ethanol concentration (BEC) was not different between these isolate and socially housed groups 4 h into the dark phase. Using lickometer‐based measures of intake in FVB mice, we identified that a predominance of increased drinking during isolation transpired outside of the typical circadian consumption peak, occurring ≈8.5 h into the dark phase, with an associated difference in BEC. These findings collectively indicate that isolate housing leads to increased consumption of rewarding substances in adolescent mice independent of their genotype, and that for ethanol this may be because of when individuals drink during the circadian cycle.     

Peer separation in infant chimpanzees,a pilot study

Seven nursery reared chimpanzees (Pan troglodytes), 7.5 to 10.5 months of age, were studied to determine the effects of a short period of separation from their peers on behavior and heart rate. The chimpanzees were separated from their mothers at birth, and reared in the nursery in a group living environment. The experiment encompassed a 13-day period, including 4 days of normative baseline, 5 days during which three of the infants were separated and housed in isolation while the other four controls remained together, and 4 days in which all of the animals were reunited. Six quantified behavioral observations and five heart rate measurements were obtained daily. Following separation, the isolated infants were behaviorally agitated, and exhibited increases in vocalizations, rocking and self-clasp behaviors, as well as changes in facial expression including cry face, whimper face and pout face. Time spent locomoting decreased in all seven animals during the separation period. Agitated behavior in the separated and isolated infants alternated with stationary withdrawn behavior. Individual differences were prominent. Heart rate was notable by the generally poorly developed circadian rhythmicity throughout the 13 day period; significant HR changes did not appear otherwise associated with separation. Day three of separation appeared to represent a point of transition with stereotyped motor behaviors developing in the three isolated infants and in one control infant.     

The effects of rearing method on social behaviors of mentored,captive‐reared juvenile California condors

Puppet‐reared and parent‐reared captive‐bred California condor (Gymnogyps californianus) juveniles were studied before their release into the wild. Behavioral data were collected during social interactions within two cohorts of juveniles (N = 11) and their adult mentors (N = 5). The purposes of this study were to (1) document the social behaviors of mentored juvenile California condors, and (2) compare social behaviors for two different rearing methods (puppet‐reared versus parent‐reared) during two phases of the mentoring process (San Diego Wild Animal Park versus release sites). Of the 17 behaviors examined by 2 × 2 analyses of variance (ANOVAs), two significant interactions between the rearing method and mentoring phase were found: pulls feathers and feeds alone. For both behaviors, parent‐reared condors engaged in these activities more often at the zoo and less often at the release pens than did the puppet‐reared condors. The main effect of rearing was also significant for two behaviors: near others, and receives contact aggression from other. Parent‐reared birds were more likely to be near another bird and receive contact aggression, regardless of mentoring phase, than puppet‐reared birds. The effect size for 16 of the 17 behaviors was greater for the rearing method than for mentoring phase. Rearing method differences may persist long‐term, as parent‐reared adult mentors were significantly more aggressive than puppet‐reared adult mentors. Dominance relations were examined for both cohorts, with the first cohort exhibiting a strong linear relationship (h′ = 0.86, P = 0.018), whereas the second cohort exhibited a moderate but non‐significant linear hierarchy (h′ = 0.63, P = 0.21). The rearing method had no effect on dominance among the juveniles, but adults were probably dominant to juveniles (P = 0.052; the difference was nearly significant). Although social behaviors between the two rearing groups were similar in most respects, this study is the first to document measurable differences between puppet‐ and parent‐reared captive‐bred California condor juveniles. Zoo Biol 27:1–18, 2008. © 2007 Wiley‐Liss, Inc.     

Effects of social influence on neonatal approach responses of Gallus chicks

Although most laboratory studies of imprinting rear and test subjects individually, in the natural setting birds are imprinted in groups. In order to approximate and evaluate naturally occuring conditions, the present study compared the approach responses of chicks reared and trained alone to those reared and trained in pairs to an audio-visual imprinting stimulus. The responses of both groups were virtually identical during the presence of the imprinting stimulus. However, under conditions of experimental extinction, the paired trained birds (now tested alone) were more resistant to extinction than their isolated counterparts, thus suggesting that birds with prior social experience are more strongly imprinted than has been previously reported.     

Social learning and mother's behavior in manipulative tasks in infant marmosets

High levels of social tolerance are considered to promote social learning, as they allow direct observation of a manipulating conspecific and facilitate scrounging. Owing to tolerance toward infants, infancy is thought to be especially suited for learning socially transmitted behaviors. Despite this, few studies have investigated social learning of infants, particularly in manipulative tasks where observation might be most helpful. Here, we investigated (1) the influence of social learning on task acquisition in infant marmosets, and (2) whether the mother augments her behavior in a way that may enhance social learning by her infants. We tested infant and juvenile marmosets in four different complex foraging‐related tasks, featuring large living insects (two tasks) or artificially embedded prey (two tasks). Each individual observed the mother solving two of the tasks and served as a control in the other two tasks. Observers manipulated more and succeeded sooner than control animals, suggesting that observing the mother promoted learning either directly or by decreasing neophobia. Moreover, the data suggest that learning in 11–15 week‐old infants might be promoted actively by the mother. She solved the tasks, consumed less food, and consumed it later than when foraging with older offspring or alone. Furthermore, the results indicate the possible importance of the third and fourth month of infancy as the crucial ontogenetic period for social learning in marmosets, corroborating recent observations of free‐living common marmosets. Am. J. Primatol. 71:503–509, 2009. © 2009 Wiley‐Liss, Inc.     

Isolation and characterization of avian influenza viruses, including highly pathogenic H5N1, from poultry in live bird markets in Hanoi, Vietnam, in 2001

Since 1997, outbreaks of highly pathogenic (HP) H5N1 and circulation of H9N2 viruses among domestic poultry in Asia have posed a threat to public health. To better understand the extent of transmission of avian influenza viruses (AIV) to humans in Asia, we conducted a cross-sectional virologic study in live bird markets (LBM) in Hanoi, Vietnam, in October 2001. Specimens from 189 birds and 18 environmental samples were collected at 10 LBM. Four influenza A viruses of the H4N6 (n = 1), H5N2 (n = 1), and H9N3 (n = 2) subtypes were isolated from healthy ducks for an isolation frequency of over 30% from this species. Two H5N1 viruses were isolated from healthy geese. The hemagglutinin (HA) genes of these H5N1 viruses possessed multiple basic amino acid motifs at the cleavage site, were HP for experimentally infected chickens, and were thus characterized as HP AIV. These HA genes shared high amino acid identities with genes of other H5N1 viruses isolated in Asia during this period, but they were genetically distinct from those of H5N1 viruses isolated from poultry and humans in Vietnam during the early 2004 outbreaks. These viruses were not highly virulent for experimentally infected ducks, mice, or ferrets. These results establish that HP H5N1 viruses with properties similar to viruses isolated in Hong Kong and mainland China circulated in Vietnam as early as 2001, suggest a common source for H5N1 viruses circulating in these Asian countries, and provide a framework to better understand the recent widespread emergence of HP H5N1 viruses in Asia.     

Artificially generated cultural variation between two groups of captive monkeys, Colobus guereza kikuyuensis

The majority of studies of social learning in primates have tested subjects in isolation and investigated the effects of learning over very short periods of time. We aimed to test for social learning in two social groups of colobus monkeys, Colobus guereza kikuyuensis. Subjects were shown video footage of familiar monkeys either pushing or pulling a plastic flap to obtain a food reward, while they were given simultaneous access to the same apparatus. Action frequencies showed a significant difference between the two groups, with the pull group performing a higher proportion of pulls to pushes, compared with the push group. Copying persisted even in later sessions during which the demonstration footage was not being shown. We conclude that we successfully generated two contrasting behavioural traditions in these groups of monkeys. We do not know how long this contrast in behaviour would have persisted had we been able to continue testing for an even longer period of time, but further studies using similar designs and even longer test periods would have the power to confirm whether stable behavioural variation can be sustained between groups of monkeys, supported by social transmission.     

Early social isolation alters behavioral and physiological responses to an endotoxin challenge in piglets

Psychosocial stress in the form of maternal deprivation and social isolation during early postnatal life induces persistent alterations in behavioral and physiological mechanisms of adaptation. One consequence may be an increased susceptibility to diseases in later life. Therefore, the aim of the present study was to investigate in domestic piglets the effects of a repeated social isolation (2 h daily from day 3 to day 11 of age) on behavioral, endocrine and immune responses to an endotoxin challenge with lipopolysaccharide (LPS) 1 day or 45 days after the isolation period. Peripheral LPS administration caused serious sickness behavior (somnolence, shivering, vomiting) and provoked profound increases in circulating tumor necrosis factor-α (TNF-α), ACTH and cortisol concentrations. The prior social isolation treatment enhanced signs of sickness and impaired suckling behavior. Early isolated piglets responded to LPS by an increase of shivering on day 12 and by increased vomiting on day 56 compared to controls. Further, there were considerable delays and reductions of time isolated piglets spent suckling on day 12. The repeated isolation stressor diminished TNF-α increases after LPS, whereas stress hormone levels were not significantly affected by isolation treatment. Finally, stronger relationships between signs of sickness and physiological measures were revealed in early isolated piglets. The duration of somnolence in isolated piglets was related to changes of cortisol and TNF-α concentrations, and the highest impact on duration of shivering was found for changes in cortisol and corticosteroid binding globulin levels. The present results suggest a sustained adaptive sensitization of coping with infection by social stress experience during early development in piglets.