Functional Anatomy and Adaptation of Male Gorillas (Gorilla gorilla gorilla) With Comparison to Male Orangutans (Pongo pygmaeus)

Great apes diversified during the Miocene in Old World forests. Two lineages, gorillas in Africa and orangutans in Asia, have sexual dimorphisms of super‐sized males, though they presumably diverged from a smaller common ancestor. We test the hypothesis that they increased in body mass independently and convergently, and that their many postcranial differences reflect locomotor differences. Whole body dissections of five adult male gorillas and four adult male orangutans allowed quantification of body mass distribution to limb segments, of body composition (muscle, bone, skin, and fat relative to total body mass), and of muscle distribution and proportions. Results demonstrate that gorilla forelimb anatomy accommodates shoulder joint mobility for vertical climbing and reaching while maintaining joint stability during quadrupedal locomotion. The heavily muscled hind limbs are equipped for propulsion and weight‐bearing over relatively stable substrates on the forest floor. In contrast, orangutan forelimb length, muscle mass, and joint construction are modified for strength and mobility in climbing, bridging, and traveling over flexible supports through the forest canopy. Muscles of hip, knee, and ankle joints provide rotational and prehensile strength essential for moving on unstable and discontinuous branches. We conclude that anatomical similarities are due to common ancestry and that differences in postcranial anatomy reflect powerful selection for divergent locomotor adaptations. These data further support the evolutionary conclusion that gorillas fall with chimpanzees and humans as part of the African hominoid radiation; orangutans are a specialized outlier. Anat Rec, 2011. © 2011 Wiley‐Liss, Inc.     

Effects of hand-rearing on the behavioral development of infant and juvenile gorillas (Gorilla g. gorilla)

Nineteen hand-reared and seven mother-reared infant and juvenile gorillas were observed for a period of 3 years. Almost all hand-reared individuals developed stereotyped behaviors during the first months. In most cases these behaviors disappeared in the first or second year. Social behaviors, solitary play, nest building and grooming developed at about the same age in hand-reared and mother-reared infants. Hand-reared immatures showed significantly more solitary play, more aggression and less social play than mother-reared ones, especially when raised in pairs. When young gorillas were kept in groups, the frequencies of these behaviors came nearer to those of mother-reared immatures. No significant differences were noted in social play. When introduced to conspecifics, hand-reared infants sometimes reacted with indiscriminant aggression. Gorillas should thus preferably be reared in peer groups and be introduced to adults not later than one year of age.     

Effects of prenatal alcohol exposure on social competence: Asymmetry in play partner preference among heterogeneous triads of male and female rats

Social behavior deficits associated with prenatal alcohol exposure (PAE) are frequently described in terms of impaired social competence, which can be defined as the effectiveness in social interaction and the ability to employ social skills successfully within different interpersonal contexts. Play behavior—which peaks during adolescence—is critical for developing social competence, as well as for motor, cognitive, and emotional development. Studies of play behavior typically utilize protocols where animals interact in dyads. However, less is understood about how the social environment may shape PAE-related social behavior deficits, particularly in more complex social contexts. Here, we assess play partner preference utilizing a novel approach in which adolescent male and female animals interact within same-sex triads comprised of animals from mixed prenatal treatments to determine how play partner identity and social group composition interact to shape behavior. When triads included one PAE animal and two control animals (i.e., control animals had the option to play either with a fellow control or a PAE playmate), we observed play target asymmetry whereby controls preferentially played with fellow controls. Notably, these results were consistent for triads of both males and females, with subtle differences in frequency of initiations versus reciprocations. We found no play target asymmetry, however, when triads included two PAE animals and one control animal or different configurations of control and pair-fed animals. Taken together, play target asymmetry resulting from ineffective social interactions, including a failure to engage with, respond to, and/or solicit play from control play partners appropriately, suggests that PAE negatively impacts the development of social competence.     

The development of "roughness" in the play fighting of rats: a Laban Movement Analysis perspective

With increasing age, rats, when play fighting, become rougher. In part, this change can be accounted for by the increasing likelihood of using adult-typical fighting tactics. However, even when using the same tactics, adults appear rougher than juveniles in their play. In this study, videotaped sequences of play fighting in rats from the juvenile (30 days) to the post-pubertal (70 days) period were analyzed using Laban Movement Analysis (LMA). Movement qualities called Effort Factors in LMA captured the character of some of this change. Juveniles tended to use Indulging Efforts, whereas older rats tended to use Condensing Efforts. The latter are related to performing movements that are more controlled. This greater level of control was also evident in the way older rats maintained postural support during play fights. When standing over supine partners, juveniles are more likely to stand on the partner with all four paws, reducing their postural stability, and hence ability to control their partner's movements. Older rats are more likely to place their hind paws on the ground, thus providing a firmer anchor for movements with their upper bodies and forepaws. These age-related changes in behavior were found for both males and females. The findings lend support to a growing body of evidence that play fighting in the juvenile phase of rats is not just a more frequently occurring version of that present in adults, but rather, has unique organizational properties.     

Hyperkeratotic mange caused by Sarcoptes scabiei (Acariformes: Sarcoptidae) in juvenile human-habituated mountain gorillas (Gorilla gorilla beringei)

To facilitate ecotourism and behavioral research, free-ranging mountain gorillas (Gorilla gorilla beringei) have been habituated to humans. During routine health monitoring, five juvenile gorillas were observed with active crusted dermatitis and alopecia. Papular and vesicular lesions and crusts with papular eruption and oozing were numerous and disseminated over the body of one gorilla with a confirmed infestation of scabies. In this gorilla, the hyperkeratotic crusts were loose and thick with a flaky and scaly appearance. Histologically, the epidermis was thickened, displayed hyperkeratosis and was infiltrated with lymphocytes and neutrophils. Examination of skin scraping yielded a positive identification of adults and eggs of Sarcoptes scabiei mites. The gorillas were treated with ivermectin, 200 mg kg(-1). As S. scabiei mites can cross-infect various mammalian species causing self-limiting dermatitis, these ectoparasites can be propagated in the habitats shared by gorillas, people, and livestock, and therefore they represent an anthropozoonotic threat.     

Cryptosporidium parvum Genotype 2 infections in free-ranging mountain gorillas (Gorilla gorilla beringei) of the Bwindi Impenetrable National Park, Uganda

For behavioral research and due to growing ecotourism, some populations of free-ranging mountain gorillas (Gorilla gorilla beringei) have become habituated to humans. Molecular analysis of two Cryptosporidium sp. oocyst isolates originating from two human-habituated gorilla groups and two oocyst isolates from non-habituated gorillas yielded positive identification of C. parvum Genotype 2 (G2; i.e., "cattle", "animal-adapted", or "zoonotic"). As G2 is cross-transmissible between humans and animals, C. parvum infections can be propagated in the habitats of human-habituated, free-ranging gorillas through both zoonotic and anthroponotic transmission cycles.     

Unusual feeding behavior in wild great apes, a window to understand origins of self-medication in humans: role of sociality and physiology on learning process

Certain toxic plants are beneficial for health if small amounts are ingested infrequently and in a specific context of illness. Among our closest living relatives, chimpanzees are found to consume plants with pharmacological properties. Providing insight on the origins of human self-medication, this study investigates the role social systems and physiology (namely gut specialization) play on learning mechanisms involved in the consumption of unusual and potentially bioactive foods by two great ape species. We collected data from a community of 41-44 wild chimpanzees in Uganda (11 months, 2008), and a group of 11-13 wild western gorillas in Central African Republic (10 months, 2008-2009). During feeding, we recorded food consumed, its availability, and social interactions (including observers watching conspecifics and the observers' subsequent activity). Unusual food consumption in chimpanzees was twice higher than in gorillas. Additionally chimpanzees relied more on social information with vertical knowledge transmission on unusual foods by continually acquiring information during their life through mostly observing the fittest (pre-senescent) adults. In contrast, in gorillas observational learning primarily occurred between related immatures, showing instead the importance of horizontal knowledge transmission. As chimpanzees' guts are physiologically less specialized than gorillas (more capable of detoxifying harmful compounds), unusual-food consumption may be more risky for chimpanzees and linked to reasons other than nutrition (like self-medication). Our results show that differences in sociality and physiology between the two species may influence mechanisms that discriminate between plants for nutrition and plants with potential therapeutic dietary components. We conclude that self-medication may have appeared in our ancestors in association with high social tolerance and lack of herbivorous gut specialization.     

The influence of natural variations in maternal care on play fighting in the rat

Naturally occurring variations in maternal care in the rat influence the sensitivity of offspring to stress in adulthood. The offspring of mothers that show lower levels of pup licking/grooming (i.e., low-LG mothers) demonstrate enhanced responses to stress and increased anxiety compared to those of high-LG mothers. Low-LG offspring are also more sensitive to the influence of environmental enrichment than high-LG offspring. This study examined play fighting in the juvenile offspring of high-LG and low-LG dams in a multiple-play partners housing environment. Male offspring from low-LG dams demonstrated a significantly higher frequency of pouncing, pinning and aggressive social grooming than did high-LG males and high-LG and low-LG females. Consistent with earlier reports, male pups engaged in more play fighting than did females and maternal care was associated with differences in play fighting but only in males. Lower levels of stimulation in the form of LG from the dam during perinatal development may thus increase sensitivity for the stimulating effects of play behavior in periadolescence, in part explaining the increased solicitation of play fighting through increased pouncing in the male offspring of the low-LG mothers. These findings identify a possible influence of variations in maternal care on play fighting and suggest that maternal care in the perinatal period influence social interactions during periadolescence.     

The prejuvenile onset of play fighting in laboratory rats (Rattus norvegicus)

Play fighting in rats is most frequent in the juvenile phase (30–40 days), and then wanes following puberty. During the juvenile phase, the most commonly used defensive tactic to block access to the nape (i.e., the play target) is to rotate around the longitudinal axis to supine. From this position of lying on its back, the defender uses its limbs to hold off the attacking pup. With the onset of puberty males, but not females, switch to more adultlike patterns of defense. The adultlike pattern involves partially rotating around the longitudinal axis of the body, but retaining ground contact with the hindpaws. In this position, the defender is able to rear to a defensive upright posture, or can slam into the partner with its hip. In this study, the manner of onset of play fighting and its components was investigated by daily videotaped observations of six litters of Long Evans hooded rats, starting at 15 or 16 days and ending at 30 days postnatally. The predominant form of social interaction in the midteens was allogrooming, but by 20 days, playful attacks to the nape were the most common form of contact. Allogrooming was most often directed to the head, not the nape. With respect to playful defense, the more adultlike tactics matured first, with all tactics present in the repertoire by 20 days. The fully juvenile pattern of defense did not mature until 25–30 days with both males and females exhibiting the same developmental pattern. These data lead to several conclusions. First, play fighting is a separate category of behavior from the outset, and does not emerge from allogrooming. Second, the adultlike defense patterns do not emerge gradually from the juvenile ones at puberty, but rather, all are present in the repertoire from infancy; and third, both males and females have the same pattern of onset of play fighting. These conclusions are discussed with respect to the possible functions of juvenile play fighting. © 1997 John Wiley & Sons, Inc. Dev Psychobiol 31: 193–205, 1997     

Metacognition in schizophrenia: the relationship of mastery to coping, insight, self-esteem, social anxiety, and various facets of neurocognition

OBJECTIVES. Deficits in metacognition, or the ability to think about thinking, are common in schizophrenia and associated with functional impairment. Unknown are what elements of function are affected by what aspects of metacognition. DESIGN. This study explored whether participants with differing capacities for Mastery, a domain of metacognition that reflects the ability to use knowledge about mental states to respond to psychological challenges, had difficulties in different elements of daily function. METHODS. Participants were 98 adults with schizophrenia or schizoaffective disorder in a non-acute phase, classified into three groups on the basis of ratings of their capacity for metacognitive Mastery using the Metacognitive Assessment Scale: low Mastery (those unable to plausibly represent psychological challenges), Intermediate Mastery (those able to plausibly represent psychological problems but cope primarily through passive measures or avoidance), and high Mastery (those able to cope with plausible problems through cognitive means). Participants completed assessments of coping preference, insight, self-esteem, and anxiety. RESULTS. Multivariate Analysis of Variance (MANOVA) and Analysis of Variance (ANOVA) revealed that the high-Mastery group had a greater preference for coping with stressors by thinking and talking about them, and greater insight than all other groups, and higher levels of feeling accepted by peers than the intermediate-Mastery group. The intermediate-Mastery group reported higher levels of resignation when facing stressors and more social phobia than the other two groups. These findings of Mastery group differences in self-esteem and anxiety persisted when neurocognition was controlled for in an Analysis of Covariance (ANCOVA). CONCLUSIONS. Mastery appears linked to coping preference, insight, self-esteem, and anxiety in a generally non-linear manner.     

The effects of stress on play and home cage behaviors in adolescent male rats

One prominent feature of adolescence is the high frequency of social behaviors, such as play. Engaging in these behaviors appears necessary for proper socio‐emotional development as social isolation during adolescence typically leads to behavioral dysfunctions in adulthood. The present experiments examined the effects of stress on social and nonsocial behaviors in group housed adolescent male rats. We found that acute restraint stress led to a complete inhibition of play (e.g., nape contacts and pins) and reduced social investigations in pre‐ (28 days), mid‐ (35 days), and late‐adolescent (42 and 49 days) animals. A follow‐up study, however, found that restraint‐induced suppression of play and social investigations was transient such that experimental animals engage in these behaviors at levels similar to those of controls 1 hr after termination of the stressor. We also found that exposure to repeated restraint stress throughout adolescence led to a decrease in social investigations, while leaving play largely unaffected. Interestingly, in all of the experiments, nonsocial behaviors (e.g., eating, drinking, grooming) were unaffected by restraint, suggesting these effects of stress are specific to social behaviors. Together, these data indicate that both acute and repeated stress significantly affect social behaviors during adolescence. © 2009 Wiley Periodicals, Inc. Dev Psychobiol 52: 62–70, 2010     

Remitted depression studies as tests of the cognitive vulnerability hypotheses of depression onset: a critique and conceptual analysis

Investigations of cognitive patterns among individuals who have recovered from a depressive episode (i.e., remitted depressives) have figured importantly in evaluations of the validity of the vulnerability hypotheses of the cognitive theories of depression. However, we suggest that remitted depression studies as typically conducted and interpreted are inadequate tests of the cognitive vulnerability hypotheses of depression onset for four reasons: (1) remitted depression studies are based on the erroneous assumption that cognitive vulnerability should be an immutable trait; (2) remitted depression studies use a logically "backward" participant selection strategy in which participants are selected on the basis of the "dependent" variable (depression) and then compared on the "independent" variable (cognitive vulnerability), which is likely to result in heterogeneity of cognitive vulnerability among both the remitted depressed as well as the nondepressed groups given the causal relations specified in the cognitive theories of depression; (3) many remitted depression studies have ignored the possible activating role of stress in the cognitive vulnerability-stress theories, particularly Beck's theory, and thus, may attempt to assess cognitive vulnerability at a time when it is not operative (i.e., priming hypothesis); and (4) remitted depression studies inappropriately use postmorbid participants to test causal hypotheses, and therefore, are ambiguous about whether negative cognitive styles observed in remitted depressed persons are vulnerabilities as opposed to consequences of depression (i.e., scar hypothesis). As a remedy, we advocate the use of a theory-guided behavioral high-risk strategy to more adequately test the cognitive vulnerability hypotheses of depression onset.     

The aging brain: the cognitive reserve hypothesis and hominid evolution.

Compared to other primates, humans live a long time and have large brains. Recent theories of the evolution of human life history stages (grandmother hypothesis, intergenerational transfer of information) lend credence to the notion that selection for increased life span and menopause has occurred in hominid evolution, despite the reduction in the force of natural selection operating on older, especially post-reproductive, individuals. Theories that posit the importance (in an inclusive fitness sense) of the survival of older individuals require them to maintain a reasonably high level of cognitive function (e.g., memory, communication). Patterns of brain aging and factors associated with healthy brain aging should be relevant to this issue. Recent neuroimaging research suggests that, in healthy aging, human brain volume (gray and white matter) is well-maintained until at least 60 years of age; cognitive function also shows only nonsignificant declines at this age. The maintenance of brain volume and cognitive performance is consistent with the idea of a significant post- or late-reproductive life history stage. A clinical model, "the cognitive reserve hypothesis," proposes that both increased brain volume and enhanced cognitive ability may contribute to healthy brain aging, reducing the likelihood of developing dementia. Selection for increased brain size and increased cognitive ability in hominid evolution may therefore have been important in selection for increased lifespan in the context of intergenerational social support networks.     

Social perception in synaesthesia for colour

Synaesthesia is a rare phenomenon in which stimulation in one modality (e.g., audition) evokes a secondary percept not associated with the first (e.g., colour). Prior work has suggested links between synaesthesia and other neurodevelopmental conditions that are linked to altered social perception abilities. With this in mind, here we sought to examine social perception abilities in grapheme–colour synaesthesia (where achromatic graphemes evoke colour experiences) by examining facial identity and facial emotion perception in synaesthetes and controls. Our results indicate that individuals who experience grapheme–colour synaesthesia outperformed controls on tasks involving fine visual discrimination of facial identity and emotion, but not on tasks involving holistic face processing. These findings are discussed in the context of broader perceptual and cognitive traits previously associated with synaesthesia for colour, with the suggestion that performance benefits shown by grapheme–colour synaesthetes may be related to domain-general visual discrimination biases observed in this group.     

Modification of juvenile play and other social behaviour in the rat by neonatal progestins: further studies

The effects of altering neonatal levels of progestins on the later development of social play behaviour was studied. Progestin levels were raised in experiment one by administering injections of either progesterone or medroxyprogesterone acetate. This indicated that exposure to either hormone led to reduced levels of social play in juvenile rats of both sexes, confirming earlier reports of lowered levels of play following medroxyprogesterone obtained via maternal milk. In Experiment 2, endogenous progestin levels were lowered by administration of the antiserum to progesterone. The prediction that this should result in raised levels of juvenile play was supported for males, but not for females. Females in Experiment 2 by contrast showed a decrease in play. Possible reasons for this sex difference in response to progesterone antiserum are discussed.     

Ontogenetic interaction between social relationships and defensive burying behavior in the rat

The present experiments clarify sexual and social relationship factors related to the development of defensive burying behavior in rats. Rats were raised in isolation, or in a variety of pairs differing in sex, age or familiarity during the juvenile and post-juvenile period. In Experiment 1, decreased burying behavior was found in both male and female rats during the juvenile stage when they were reared in isolation, or with an adult female, or for males reared with a same-age female. In Experiment 2, female rats isolated during the juvenile stage who were reared after the juvenile stage with a same-sex, non-isolated rat, showed as much burying behavior as rats reared with a littermate; this was not found for male rats. When both male and female rats isolated during the juvenile stage were reared with each other after isolation, they maintained reduced burying behavior in adulthood. These sex differences in the effect of different social groupings are likely due to the differences in social relationships during the juvenile and after puberty, when social dominance relationships emerge in male rats. In Experiment 3, the effects of social dominance relationships on burying behavior were investigated in male rats. Subordination increased the freezing tendency as a passive defense, while social tension accompanied with rearing with an adult male produced decreased burying behavior as a proactive defense. These findings suggest that affiliative relationships involving playful contacts activate and maintain burying behavior, but familiarity is not a significant factor, while dominance relationships modulate the patterns of burying behavior.     

Morphine administration selectively facilitates social play in common marmosets

Common marmosets (Callithrix jacchus) form extended families, and several cohorts of young may reside together. Play is shown extensively among the offspring. We hypothesized that opiate activity modulates social play, and predicted that administration of morphine (0.5 mg/kg) would facilitate social play, whereas pretreatment with naloxone (0.5 mg/kg) would block morphine's effects. Morphine administration was associated with significantly increased social play, and the effect of morphine was attributable to the focal subject, since play initiated by others was unaffected by treatment. Non-social categories of play, such as object manipulation and locomotor play, and affiliative behaviors, such as time spent huddled, were unaffected by treatment. Twittering and play face, behaviors used by young during play, also increased after morphine administration. Pretreatment with naloxone blocked morphine's effects. Total activity was significantly increased by morphine administration. We conclude that social play is specifically facilitated by opiate activation, whereas other categories of play behavior and social behavior were unaffected by morphine. Thus, social play represents a distinct category of social behavior in juvenile common marmosets with regulatory processes that are unique from other types of social behavior.     

Brain maturational processes and delayed onset in schizophrenia.

The central feature of schizophrenia is its onset in adolescence. Although this clinical observation is consistent with the view that schizophrenia may be a neurodevelopmental disorder, debate has focused on when the proposed brain maturational deviations may begin and what might be the nature of such defective development. Conflicting models of this illness (e.g., the early and late neurodevelopmental models) have been proposed. In this paper, we will first review concepts from basic developmental neurobiology pertinent to these issues; we then summarize aspects of the neurobiology of schizophrenia that have a particular bearing on the adolescent onset of this illness. We propose that the schizophrenic syndrome may result from early brain adversity and late maturational processes of brain development interacting with adverse humoral, biochemical, and psychosocial factors during adolescence and early adulthood. The onset of schizophrenia in adolescence may be related to the "plasticity switch" secondary to the peripubertal brain maturational changes, perhaps involving an alteration in glutamate receptor function. This loss of plasticity could result in social and nonsocial cognitive deficits that are central to the pathophysiology of schizophrenia; the vulnerable person may therefore utilize prepubertal processing styles that are insufficient to the adaptive and "gistful" abstraction requirements of adult cognition. Schizophrenia onset might occur in the context of psychosocial developmental challenges to a delayed social cognitive capacity among neurodevelopmentally compromised individuals. We review therapeutic implications as well as testable predictions generated by this model, and discuss research strategies that might further our understanding of the brain maturational abnormalities in schizophrenia.     

Social competence in young children with inflicted traumatic brain injury

As infants develop skills that allow for increasing independence in social and cognitive domains, they acquire the ability to identify goals, sequence behaviors to carry out goals, and to flexibly use strategies for attaining goals in both social and independent play contexts. Little is known about how brain injury in young children may disrupt the precursors to such executive processes. In this study, we examined social and cognitive competence in 25 infants ages 3 to 23 months who sustained moderate to severe traumatic brain injury (TBI) secondary to physical abuse and in 22 healthy community comparison children. Children with TBI were evaluated an average of 1.6 months after the injury. A toy-centered activity with the examiner was used to capture joint attention and social behavior and an exploratory toy play situation was used to measure independent goal-directed play. The inflicted TBI group showed significant reduction in both social and cognitive domains relative to the comparison group. Canonical correlation analyses disclosed that inflicted TBI was associated with reduction in (a) initiation of social interactions, (b) responsiveness to interactions initiated by the examiner, (c) positive affect, and (d) compliance. The groups performed comparably on indexes of gestural and verbal communication and for the occurrence of negative affect. Joint attention was an area of vulnerability for the TBI group in both social initiation and response contexts. Although general cognitive and motor scores were lower in the inflicted TBI group, the complexity of independent toy play did not differ across groups. Early brain injury causes significant disruption in behaviors regulating initiation and responsiveness in social contexts. Longitudinal follow-up will characterize the long-term consequences of early disruption in joint attention and other behaviors on the development of social and cognitive precursors to executive processes.     

Simian retroviruses in African apes

It is now well established that simian immunodeficiency viruses (SIVs) from chimpanzees (SIVcpz) and gorillas (SIVgor) from west Central Africa are at the origin of HIV-1/AIDS. Apes are also infected with other retroviruses, notably simian T-cell lymphotropic viruses (STLVs) and simian foamy viruses (SFVs), that can be transmitted to humans. We discuss the actual knowledge on SIV, STLV and SFV infections in chimpanzees, gorillas, and bonobos. We especially elaborate on how the recent development of non-invasive methods has allowed us to identify the reservoirs of the HIV-1 ancestors in chimpanzees and gorillas, and increased our knowledge of the natural history of SIV infections in chimpanzees. Multiple cross-species events with retroviruses from apes to humans have occurred, but only one transmission of SIVcpz from chimpanzees in south-eastern Cameroon spread worldwide, and is responsible for the actual HIV pandemic. Frequent SFV transmissions have been recently reported, but no human-to-human transmission has been documented yet. Because humans are still in contact with apes, identification of pathogens in wild ape populations can signal which pathogens may be cause risk for humans, and allow the development of serological and molecular assays with which to detect transmissions to humans. Finally, non-invasive sampling also allows the study of the impact of retroviruses and other pathogens on the health and survival of endangered species such as chimpanzees, gorillas, and bonobos.