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1.  Testosterone related to age and life-history stages in male baboons and geladas 
Hormones and behavior  2009;56(4):472-480.
Despite significant advances in our knowledge of how testosterone mediates life-history trade-offs, this research has primarily focused on seasonal species. We know comparatively little about the relationship between testosterone and life-history stages for non-seasonally breeding species. Here we examine testosterone profiles across the lifespan of males from three non-seasonally breeding primates: yellow baboons (Papio cynocephalus or P. hamadryas cynocephalus), chacma baboons (Papio ursinus or P. h. ursinus), and geladas (Theropithecus gelada). First, we predict that testosterone profiles will track the reproductive profiles of each taxon across their respective breeding years. Second, we evaluate age-related changes in testosterone to determine whether several life-history transitions are associated with these changes. Subjects include males (>2.5 years) from wild populations of each taxon from whom we had fecal samples for hormone determination. Although testosterone profiles across species were broadly similar, considerable variability was found in the timing of two major changes: (1) the attainment of adult levels of testosterone, and (2) the decline in testosterone after the period of maximum production. Attainment of adult testosterone levels was delayed by one year in chacmas compared with yellows and geladas. With respect to the decline in testosterone, geladas and chacmas exhibited a significant drop after three years of maximum production, while yellows declined so gradually that no significant annual drop was ever detected. For both yellows and chacmas, increases in testosterone production preceded elevations in social dominance rank. We discuss these differences in the context of ecological and behavioral differences exhibited by these taxa.
PMCID: PMC3630238  PMID: 19712676
androgen; fecal steroid; hormone; life-history; maturation; method validation
2.  Relationship between Social Rank and Cortisol and Testosterone concentrations in Male Cynomolgus Monkeys (Macaca fascicularis) 
Journal of neuroendocrinology  2009;21(1):68-76.
In nonhuman primate social groups, biological differences related to social status have proven useful in investigating mechanisms of sensitivity to various disease states. Physiological and neurobiological differences between dominant and subordinate monkeys have been interpreted in the context of chronic social stress. The present experiments were designed to investigate the relationships between basal cortisol and testosterone concentrations and the establishment and maintenance of the social hierarchy in male cynomolgus monkeys. Cortisol concentrations were measured at baseline and following suppression with dexamethasone (DEX) and subsequent administration of ACTH while monkeys were individually housed (n=20) and after 3 months of social housing (n=4/group), by which time dominance hierarchies had stabilised. Cortisol was also measured during the initial three days of social housing. Neither pre-social housing hormone concentrations nor HPA axis sensitivity predicted eventual social rank. During initial social housing, cortisol concentrations were significantly higher in monkeys that eventually became subordinate; this effect dissipated within three days. During the 12 weeks of social housing, aggressive and submissive behaviours were observed consistently, forming the basis for assignment of social ranks. At this time, basal testosterone and cortisol concentrations were significantly higher in dominant monkeys and, following dexamethasone suppression, cortisol release in response to a challenge injection of ACTH was significantly greater in subordinates. These results indicate that basal cortisol and testosterone concentrations and HPA axis function are state variables that differentially reflect position in the dominance hierarchy, rather than trait variables that predict future social status.
PMCID: PMC2709846  PMID: 19094095
cortisol; dexamethasone suppression; dominance hierarchy; testosterone; nonhuman primates
3.  The endocrinology of male rhesus macaque social and reproductive status: a test of the challenge and social stress hypotheses 
Social status primarily determines male mammalian reproductive success, and hypotheses on the endocrinology of dominance have stimulated unprecedented investigation of its costs and benefits. Under the challenge hypothesis, male testosterone levels rise according to competitive need, while the social stress hypothesis predicts glucocorticoid (GC) rises in high ranking individuals during social unrest. Periods of social instability in group-living primates, primarily in baboons, provide evidence for both hypotheses, but data on social instability in seasonally-breeding species with marked social despotism but lower reproductive skew are lacking. We tested these hypotheses in seasonally-breeding rhesus macaques on Cayo Santiago, Puerto Rico. We documented male fecal GC and androgen levels over a 10 month period in relation to rank, age, natal status and group tenure length, including during a socially unstable period in which coalitions of lower-ranked males attacked higher-ranked males. Androgen but not GC levels rose during the mating season; older males had lower birth season levels but underwent a greater inter-season rise than younger males. Neither endocrine measure was related to rank except during social instability, when higher ranked individuals had higher and more variable levels of both. High ranking male targets had the highest GC levels of all males when targeted, and also had high and variable GC and androgen levels across the instability period. Our results provide evidence for both the challenge and social stress hypotheses.
PMCID: PMC3950204  PMID: 24634561
challenge hypothesis; social stress; male-male competition; social status; dominance
4.  Androgen and glucocorticoid levels reflect seasonally occurring social challenges in male redfronted lemurs (Eulemur fulvus rufus) 
Intense reproductive competition and social instability are assumed to increase concentrations of glucocorticoids and androgens in vertebrates, as a means of coping with these challenges. In seasonally breeding redfronted lemurs (Eulemur fulvus rufus), the mating and the birth season and the associated increased male competition are predicted to pose such reproductive challenges. In this paper, we investigate seasonal variation in hormone excretion in male redfronted lemurs, and examine whether this variation is associated with social or ecological factors. Although dominance status has been shown to affect individual stress levels across many taxa, we predicted no rank-related differences in glucocorticoids for redfronted lemurs because relatively equal costs are associated with both high and low rank positions (based on patterns of rank acquisition/maintenance and threats toward subordinates). Over a 14-month period, we collected behavioral data (1843 focal hours) and 617 fecal samples from 13 redfronted lemur males in Kirindy Forest/Madagascar. We found no general rank-related pattern of testosterone or glucocorticoid excretion in this species. Both hormones were excreted at significantly higher levels during the mating and the birth season, despite social stability during both periods. The elevated mating season levels may be explained by increased within-group reproductive competition during this time and are in line with previous studies of other seasonally reproducing primates. For the birth season increase, we propose that the predictable risk of infanticide in this highly seasonal species affects male gonadal and adrenal endocrine activity. We evaluate alternative social and ecological factors influencing the production of both hormone classes and conclude based on our preliminary investigations that none of them can account for the observed pattern.
PMCID: PMC2755774  PMID: 19816530
Glucocorticoids; Androgens; Eulemur fulvus rufus; Sexual competition; Seasonality; Stress
5.  Nodular Worm Infection in Wild Chimpanzees in Western Uganda: A Risk for Human Health? 
This study focused on Oeosophagostomum sp., and more especially on O. bifurcum, as a parasite that can be lethal to humans and is widespread among humans and monkeys in endemic regions, but has not yet been documented in apes. Its epidemiology and the role played by non-human primates in its transmission are still poorly understood. O. stephanostomum was the only species diagnosed so far in chimpanzees. Until recently, O. bifurcum was assumed to have a high zoonotic potential, but recent findings tend to demonstrate that O. bifurcum of non-human primates and humans might be genetically distinct. As the closest relative to human beings, and a species living in spatial proximity to humans in the field site studied, Pan troglodytes is thus an interesting host to investigate. Recently, a role for chimpanzees in the emergence of HIV and malaria in humans has been documented. In the framework of our long-term health monitoring of wild chimpanzees from Kibale National Park in Western Uganda, we analysed 311 samples of faeces. Coproscopy revealed that high-ranking males are more infected than other individuals. These chimpanzees are also the more frequent crop-raiders. Results from PCR assays conducted on larvae and dried faeces also revealed that O. stephanostomum as well as O. bifurcum are infecting chimpanzees, both species co-existing in the same individuals. Because contacts between humans and great apes are increasing with ecotourism and forest fragmentation in areas of high population density, this paper emphasizes that the presence of potential zoonotic parasites should be viewed as a major concern for public health. Investigations of the parasite status of people living around the park or working inside as well as sympatric non-human primates should be planned, and further research might reveal this as a promising aspect of efforts to reinforce measures against crop-raiding.
Author Summary
The disease caused by the nodular worm Oesophagostomum bifurcum can be lethal in humans and is thus of major human health significance in certain African regions. There are still gaps in the understanding of the epidemiology of the disease, including the role of non-human primates as reservoirs of the infection. We recently conducted a survey in a community of wild chimpanzees (Pan troglodytes schweinfurthii) in Kibale National Park, Western Uganda. O. stephanostomum is so far the only species previously found in chimpanzees. A total of 311 stool samples was examined and revealed that high-ranking males are more infected than other individuals. These chimpanzees are also the more frequent crop-raiders. Moreover, we reported for the first time molecular evidence for O. bifurcum in addition to O. stephanostomum in chimpanzees. Our results raise public health concerns for a neglected infection in regions where spatial proximity between great apes and humans are increasing because of forest fragmentation.
PMCID: PMC2838776  PMID: 20300510
6.  Dominance and queen succession in captive colonies of the eusocial naked mole-rat, Heterocephalus glaber. 
Naked mole-rat colonies exhibit a high reproductive skew, breeding being typically restricted to one female (the 'queen') and one to three males. Other colony members are reproductively suppressed, although this suppression can be reversed following the removal or death of the queen. We examined dominance and queen succession within captive colonies to investigate the relationship between urinary testosterone and cortisol, dominance rank and reproductive status; and to determine if behavioural and/or physiological parameters can be used as predictors of queen succession. Social structure was characterized by a linear dominance hierarchy before and after queen removal. Prior to queen removal, dominance rank was negatively correlated with body weight and urinary testosterone and cortisol titres in males and females. Queen removal results in social instability and aggression between high ranking individuals. Dominance rank appears to be a good predictor of reproductive status: queens are the highest ranking colony females and are succeeded by the next highest ranking females. The intense dominance-related aggression that accompanies reproductive succession in naked mole-rats provides empirical support for optimal skew theory.
PMCID: PMC1688532  PMID: 9263466
7.  Second to fourth digit ratio, testosterone and perceived male dominance. 
Previous studies have shown that male faces with extreme features associated with testosterone are perceived as dominant and masculine. Women have been reported to prefer more masculinized male faces as they may consider testosterone markers to be an 'honest' indication of good health, and such considerations may underlie their aesthetic preferences. However, pronounced testosterone facial markers are also associated with dominance, and several negative personality traits. This suggests that female aesthetic preferences may be an adaptive compromise between positive attributes associated with higher than average testosterone, and negative attributes associated with more extreme masculinization. This current study attempts to clarify the role of hormone markers in female perceptions of dominance, masculinity and attractiveness, in male facial images. Recent evidence suggests that the relative length of the 2nd to 4th finger (2D : 4D ratio) is a pointer to prenatal testosterone levels and may thus serve as a window to the prenatal hormonal environment. We measured 2D : 4D in a sample of male college students and took salivary samples to analyse circulating levels of testosterone. Women rated facial images of these males for dominance, masculinity and attractiveness. Our results show that male 2D : 4D was significantly negatively related to perceived dominance and masculinity but not attractiveness. Circulating testosterone levels were not related to dominance, masculinity or attractiveness. These findings suggest that: (i) high prenatal levels of testosterone serve to 'organize' male facial features to subsequently reflect dominance and masculine characteristics presumably activated during puberty; and (ii) attractiveness is not directly related to testosterone levels. We conclude that facial dominance and masculinity reflect a male's perceived status rather than his physical attraction to women.
PMCID: PMC1691489  PMID: 14561281
8.  Hormonal and behavioural correlates of male dominance and reproductive status in captive colonies of the naked mole-rat, Heterocephalus glaber. 
Naked mole-rat colonies are societies with a high reproductive skew, breeding being restricted to one dominant female (the 'queen') and 1-3 males. Other colony members of both sexes are reproductively suppressed. Experimental removal of breeding males allowed us to investigate the relationship between urinary testosterone and cortisol, dominance rank, and male reproductive status. Dominance rank was strongly correlated with body weight, age, and urinary testosterone titres in males. No relationship between urinary cortisol levels and male reproductive status or dominance was found. Breeding males were among the highest-ranking, heaviest and oldest males in their respective colonies, and were succeeded by other high-ranking, large, old colony males. In contrast to females, no evidence of competition over breeding status was observed among males. Male-male agonism was low both before and after removal of breeders and mate guarding was not observed. The lower reproductive skew for males compared with female skew or queen control over male reproduction may explain why males compete less strongly than females over breeding status after removal of same-sexed breeders.
PMCID: PMC1689228  PMID: 9721687
9.  Age-independent increases in male salivary testosterone during horticultural activity among Tsimane forager-farmers 
Testosterone plays an important role in mediating male reproductive trade-offs in many vertebrate species, augmenting muscle and influencing behavior necessary for male-male competition and mating-effort. Among humans, testosterone may also play a key role in facilitating male provisioning of offspring as muscular and neuromuscular performance are deeply influenced by acute changes in testosterone. This study examines acute changes in salivary testosterone among 63 Tsimane men ranging in age from 16–80 (mean 38.2) years during one-hour bouts of tree-chopping while clearing horticultural plots. The Tsimane forager-horticulturalists living in the Bolivian Amazon experience high energy expenditure associated with food production, have high levels of parasites and pathogens, and display significantly lower baseline salivary testosterone than age-matched US males. Mixed-effects models controlling for BMI and time of specimen collection reveal increased salivary testosterone (p<0.001) equivalent to a 48.6% rise, after one hour of tree chopping. Age had no effect on baseline (p=0.656) or change in testosterone (p=0.530); self-reported illness did not modify testosterone change (p=0.488). A comparison of these results to the relative change in testosterone during a competitive soccer tournament in the same population reveals larger relative changes in testosterone following resource production (tree chopping), compared to competition (soccer). These findings highlight the importance of moving beyond a unidimensional focus on changes in testosterone and male-male aggression to investigate the importance of testosterone-behavior interactions across additional male fitness-related activities. Acutely increased testosterone during muscularly intensive horticultural food production may facilitate male productivity and provisioning.
PMCID: PMC3810999  PMID: 24187482
Challenge hypothesis; testosterone; Tsimane; resource production; competition; physical activity
10.  Winning Isn't Everything: Mood and Testosterone Regulate the Cortisol Response in Competition 
PLoS ONE  2013;8(1):e52582.
Dominance contests are recurrent and widespread causes of stress among mammals. Studies of activation of the stress axis in social defeat – as reflected in levels of adrenal glucocorticoid, cortisol – have generated scattered and sometimes contradictory results, suggesting that biopsychological individual differences might play an important mediating role, at least in humans. In the context of a larger study of the regulation of endocrine responses to competition, we evaluated the notion that mood states, such as self-assurance and hostility, may influence cortisol reactivity to dominance cues via an interplay with baseline testosterone, considered as a potential marker of individual differences in dominance. Seventy healthy male university students (mean age 20.02, range 18–26) provided saliva samples before and after competing for fifteen minutes on a rigged computer task. After a winner was determined, all participants were assessed on their mood states through a standardized psychometric instrument (PANAS-X). Among winners of a rigged videogame competition, we found a significant interaction between testosterone and self-assurance in relation to post-competition cortisol. Specifically, self-assurance was associated with lower post-competition cortisol in subjects with high baseline testosterone levels, but no such relationship was observed in subjects with lower baseline testosterone levels. In losers of the competition no interaction effect between basal testosterone and hostility was observed. However, in this subgroup a significant negative relationship between basal testosterone and post-competition cortisol was evident. Overall, these findings provide initial support for the novel hypothesis that biological motivational predispositions (i.e. basal testosterone) and state (i.e. mood changes) may interact in regulating the hypothalamic-pituitary-adrenal axis activation after a social contest.
PMCID: PMC3541278  PMID: 23326343
11.  Testosterone and Aggressive Behavior in Man 
Atavistic residues of aggressive behavior prevailing in animal life, determined by testosterone, remain attenuated in man and suppressed through familial and social inhibitions. However, it still manifests itself in various intensities and forms from; thoughts, anger, verbal aggressiveness, competition, dominance behavior, to physical violence. Testosterone plays a significant role in the arousal of these behavioral manifestations in the brain centers involved in aggression and on the development of the muscular system that enables their realization. There is evidence that testosterone levels are higher in individuals with aggressive behavior, such as prisoners who have committed violent crimes. Several field studies have also shown that testosterone levels increase during the aggressive phases of sports games. In more sensitive laboratory paradigms, it has been observed that participant’s testosterone rises in the winners of; competitions, dominance trials or in confrontations with factitious opponents. Aggressive behavior arises in the brain through interplay between subcortical structures in the amygdala and the hypothalamus in which emotions are born and the prefrontal cognitive centers where emotions are perceived and controlled. The action of testosterone on the brain begins in the embryonic stage. Earlier in development at the DNA level, the number of CAG repeats in the androgen receptor gene seems to play a role in the expression of aggressive behavior. Neuroimaging techniques in adult males have shown that testosterone activates the amygdala enhancing its emotional activity and its resistance to prefrontal restraining control. This effect is opposed by the action of cortisol which facilitates prefrontal area cognitive control on impulsive tendencies aroused in the subcortical structures. The degree of impulsivity is regulated by serotonin inhibiting receptors, and with the intervention of this neurotransmitter the major agents of the neuroendocrine influence on the brain process of aggression forms a triad. Testosterone activates the subcortical areas of the brain to produce aggression, while cortisol and serotonin act antagonistically with testosterone to reduce its effects.
PMCID: PMC3693622  PMID: 23843821
Testosterone; Cortisol; Serotonin; Aggressiveness
12.  Social status, immune response and parasitism in males: a meta-analysis 
In male vertebrates, two conflicting paradigms—the energetic costs of high dominance rank and the chronic stress of low rank—have been proposed to explain patterns of immune function and parasitism. To date, neither paradigm has provided a complete explanation for status-related differences in male health. Here, we applied meta-analyses to test for correlations between male social status, immune responses and parasitism. We used an ecoimmunological framework, which proposes that males should re-allocate investment in different immune components depending on the costs of dominance or subordination. Spanning 297 analyses, from 77 studies on several vertebrate taxa, we found that most immune responses were similar between subordinate and dominant males, and neither dominant nor subordinate males consistently invested in predictable immune components. However, subordinate males displayed significantly lower delayed-type hypersensitivity and higher levels of some inflammatory cytokines than dominant males, while dominant males exhibited relatively lower immunoglobulin responses than subordinate males. Despite few differences in immunity, dominant males exhibited consistently higher parasitism than subordinate males, including protozoan blood parasites, ectoparasites and gastrointestinal helminths. We discuss our results in the context of the costs of dominance and subordination and advocate future work that measures both parasitism and immune responses in wild systems.
PMCID: PMC4410375  PMID: 25870395
social status; dominance rank; life-history trade-offs; immune function; parasitism
13.  Monkeys in the Middle: Parasite Transmission through the Social Network of a Wild Primate 
PLoS ONE  2012;7(12):e51144.
In wildlife populations, group-living is thought to increase the probability of parasite transmission because contact rates increase at high host densities. Physical contact, such as social grooming, is an important component of group structure, but it can also increase the risk of exposure to infection for individuals because it provides a mechanism for transmission of potentially pathogenic organisms. Living in groups can also create variation in susceptibility to infection among individuals because circulating levels of immunosuppressive hormones like glucocorticoids often depend on an individual’s position within the group’s social structure. Yet, little is known about the relative roles of socially mediated exposure versus susceptibility in parasite transmission among free-living animal groups. To address this issue, we investigate the relationship between host dominance hierarchy and nematode parasite transmission among females in a wild group of Japanese macaques (Macaca fuscata yakui). We use social network analysis to describe each individual female’s position within the grooming network in relation to dominance rank and relative levels of infection. Our results suggest that the number of directly-transmitted parasite species infecting each female, and the relative amount of transmission stages that one of these species sheds in faeces, both increase with dominance rank. Female centrality within the network, which shows positive associations with dominance hierarchy, is also positively associated with infection by certain parasite species, suggesting that the measured rank-bias in transmission may reflect variation in exposure rather than susceptibility. This is supported by the lack of a clear relationship between rank and faecal cortisol, as an indicator of stress, in a subset of these females. Thus, socially mediated exposure appears to be important for direct transmission of nematode parasites, lending support to the idea that a classical fitness trade-off inherent to living in groups can exist.
PMCID: PMC3515516  PMID: 23227246
Coalitionary aggression occurs when at least two individuals jointly direct aggression at one or more conspecific targets. Scientists have long argued that this common form of cooperation has positive fitness consequences. Nevertheless, despite evidence that social bond strength (which is thought to promote coalition formation) is correlated with fitness in primates, cetaceans, and ungulates, few studies have directly examined whether coalitionary aggression improves reproductive success. We tested the hypothesis that among free-ranging chimpanzees (Pan troglodytes schweinfurthii), participation in coalitionary aggression increases reproductive output. Using 14 years of genetic and behavioral data from Gombe National Park, Tanzania, we found that coalitionary aggression increased a male’s chances of A) siring offspring, compared to other males of similar dominance rank, and B) ascending in rank, a correlate of future reproductive output. Because male chimpanzees form coalitions with many others within a complex network, we used social network analysis to identify the types of connections correlated with these fitness benefits. The beneficiaries of coalitionary aggression were males with the highest ‘betweenness’ – that is, those who tended to have coalition partners who themselves did not form coalitions with each other. This suggests that beyond simply recognizing third-party relationships, chimpanzees may use this knowledge to choose coalition partners. If so, this is a significant step forward in our knowledge of the adaptive value of social intelligence. Regardless of mechanism, however, this is the first evidence of genetic benefits of coalitionary aggression in this species, and therefore has important implications for understanding the evolution of cooperation.
PMCID: PMC3582680  PMID: 23459197
coalition; chimpanzee; social network analysis; cooperation; paternity; dominance rank; social bonds
15.  Rank effects on social stress in lactating chimpanzees 
Hormones and behavior  2010;58(3):440-449.
Given the deleterious consequences associated with chronic stress, individual differences in stress susceptibility can have important fitness implications. These differences may be explained in part by dominance status because high rank is typically associated with decreased aggression and improved nutrition. Here, we examined the relationship between dominance and social stress in lactating chimpanzees, Pan troglodytes schweinfurthii, at Gombe National Park, Tanzania. We did so by pairing daily demographic and behavioural data with faecal glucocorticoid metabolite (FGM) concentrations collected over 37 months. While there was no main effect of rank, interesting differences emerged by adult subgroup size and adult sex ratio (males/females). We found that differences in FGM concentrations between high- and low-ranking females were most pronounced as adult subgroup size and sex ratio increased. Low-ranking females had higher FGM concentrations in larger subgroups and in subgroups biased towards adult males; we observed no comparable change in FGM concentrations amongst high-ranking females. Because low-ranking females were the recipient of significantly more male aggression relative to females of high rank, these patterns may be driven by psychosocial stress in low-ranking females. There was no significant change in diet quality across subgroup sizes; this finding suggests that nutritional stressors were not driving differences in female FGM concentrations. Being susceptible to social stress has important fitness implications as it may constrain low-ranking females from ‘choosing’ optimal subgroups to take advantage of food resources and/or for the socialization of their offspring.
PMCID: PMC3951729  PMID: 20546741
chimpanzee; Gombe National Park; lactation; Pan troglodytes schweinfurthii; rank status; stress
16.  Rank effects on social stress in lactating chimpanzees 
Animal behaviour  2014;87:195-202.
Given the deleterious consequences associated with chronic stress, individual differences in stress susceptibility can have important fitness implications. These differences may be explained in part by dominance status because high rank is typically associated with decreased aggression and improved nutrition. Here, we examined the relationship between dominance and social stress in lactating chimpanzees, Pan troglodytes schweinfurthii, at Gombe National Park, Tanzania. We did so by pairing daily demographic and behavioural data with faecal glucocorticoid metabolite (FGM) concentrations collected over 37 months. While there was no main effect of rank, interesting differences emerged by adult subgroup size and adult sex ratio (males/females). We found that differences in FGM concentrations between high- and low-ranking females were most pronounced as adult subgroup size and sex ratio increased. Low-ranking females had higher FGM concentrations in larger subgroups and in subgroups biased towards adult males; we observed no comparable change in FGM concentrations amongst high-ranking females. Because low-ranking females were the recipient of significantly more male aggression relative to females of high rank, these patterns may be driven by psychosocial stress in low-ranking females. There was no significant change in diet quality across subgroup sizes; this finding suggests that nutritional stressors were not driving differences in female FGM concentrations. Being susceptible to social stress has important fitness implications as it may constrain low-ranking females from ‘choosing’ optimal subgroups to take advantage of food resources and/or for the socialization of their offspring.
PMCID: PMC4004704  PMID: 24791015
chimpanzee; Gombe National Park; lactation; Pan troglodytes schweinfurthii; rank status; stress
17.  Suitable Habitats for Endangered Frugivorous Mammals: Small-Scale Comparison, Regeneration Forest and Chimpanzee Density in Kibale National Park, Uganda 
PLoS ONE  2014;9(7):e102177.
Landscape patterns and chimpanzee (Pan troglodytes schweinfurthii) densities in Kibale National Park show important variation among communities that are geographically close to one another (from 1.5 to 5.1 chimpanzees/km2). Anthropogenic activities inside the park (past logging activities, current encroachment) and outside its limits (food and cash crops) may impact the amount and distribution of food resources for chimpanzees (frugivorous species) and their spatial distribution within the park. Spatial and temporal patterns of fruit availability were recorded over 18 months at Sebitoli (a site of intermediate chimpanzee density and higher anthropic pressure) with the aim of understanding the factors explaining chimpanzee density there, in comparison to results from two other sites, also in Kibale: Kanyawara (low chimpanzee density) and Ngogo (high density, and furthest from Sebitoli). Because of the post-logging regenerating status of the forest in Sebitoli and Kanyawara, smaller basal area (BA) of fruiting trees most widely consumed by the chimpanzees in Kanyawara and Sebitoli was expected compared to Ngogo (not logged commercially). Due to the distance between sites, spatial and temporal fruit abundance in Sebitoli was expected to be more similar to Kanyawara than to Ngogo. While species functional classes consumed by Sebitoli chimpanzees (foods eaten during periods of high or low fruit abundance) differ from the two other sites, Sebitoli is very similar to Kanyawara in terms of land-cover and consumed species. Among feeding trees, Ficus species are particularly important resources for chimpanzees at Sebitoli, where their basal area is higher than at Kanywara or Ngogo. Ficus species provided a relatively consistent supply of food for chimpanzees throughout the year, and we suggest that this could help to explain the unusually high density of chimpanzees in such a disturbed site.
PMCID: PMC4102508  PMID: 25033459
18.  Social Opportunity Rapidly Regulates Expression of CRF and CRF Receptors in the Brain during Social Ascent of a Teleost Fish, Astatotilapia burtoni 
PLoS ONE  2014;9(5):e96632.
In social animals, hierarchical rank governs food availability, territorial rights and breeding access. Rank order can change rapidly and typically depends on dynamic aggressive interactions. Since the neuromodulator corticotrophin releasing factor (CRF) integrates internal and external cues to regulate the hypothalamic-pituitary adrenal (HPA) axis, we analyzed the CRF system during social encounters related to status. We used a particularly suitable animal model, African cichlid fish, Astatotilapia burtoni, whose social status regulates reproduction. When presented with an opportunity to rise in rank, subordinate A. burtoni males rapidly change coloration, behavior, and their physiology to support a new role as dominant, reproductively active fish. Although changes in gonadotropin-releasing hormone (GnRH1), the key reproductive molecular actor, have been analyzed during social ascent, little is known about the roles of CRF and the HPA axis during transitions. Experimentally enabling males to ascend in social rank, we measured changes in plasma cortisol and the CRF system in specific brain regions 15 minutes after onset of social ascent. Plasma cortisol levels in ascending fish were lower than subordinate conspecifics, but similar to levels in dominant animals. In the preoptic area (POA), where GnRH1 cells are located, and in the pituitary gland, CRF and CRF1 receptor mRNA levels are rapidly down regulated in ascending males compared to subordinates. In the Vc/Vl, a forebrain region where CRF cell bodies are located, mRNA coding for both CRFR1 and CRFR2 receptors is lower in ascending fish compared to stable subordinate conspecifics. The rapid time course of these changes (within minutes) suggests that the CRF system is involved in the physiological changes associated with shifts in social status. Since CRF typically has inhibitory effects on the neuroendocrine reproductive axis in vertebrates, this attenuation of CRF activity may allow rapid activation of the reproductive axis and facilitate the transition to dominance.
PMCID: PMC4019471  PMID: 24824619
19.  Efficacy of Handwashing with Soap and Nail Clipping on Intestinal Parasitic Infections in School-Aged Children: A Factorial Cluster Randomized Controlled Trial 
PLoS Medicine  2015;12(6):e1001837.
Intestinal parasitic infections are highly endemic among school-aged children in resource-limited settings. To lower their impact, preventive measures should be implemented that are sustainable with available resources. The aim of this study was to assess the impact of handwashing with soap and nail clipping on the prevention of intestinal parasite reinfections.
Methods and Findings
In this trial, 367 parasite-negative school-aged children (aged 6–15 y) were randomly assigned to receive both, one or the other, or neither of the interventions in a 2 × 2 factorial design. Assignment sequence was concealed. After 6 mo of follow-up, stool samples were examined using direct, concentration, and Kato-Katz methods. Hemoglobin levels were determined using a HemoCue spectrometer. The primary study outcomes were prevalence of intestinal parasite reinfection and infection intensity. The secondary outcome was anemia prevalence. Analysis was by intention to treat. Main effects were adjusted for sex, age, drinking water source, latrine use, pre-treatment parasites, handwashing with soap and nail clipping at baseline, and the other factor in the additive model. Fourteen percent (95% CI: 9% to 19%) of the children in the handwashing with soap intervention group were reinfected versus 29% (95% CI: 22% to 36%) in the groups with no handwashing with soap (adjusted odds ratio [AOR] 0.32, 95% CI: 0.17 to 0.62). Similarly, 17% (95% CI: 12% to 22%) of the children in the nail clipping intervention group were reinfected versus 26% (95% CI: 20% to 32%) in the groups with no nail clipping (AOR 0.51, 95% CI: 0.27 to 0.95). Likewise, following the intervention, 13% (95% CI: 8% to 18%) of the children in the handwashing group were anemic versus 23% (95% CI: 17% to 29%) in the groups with no handwashing with soap (AOR 0.39, 95% CI: 0.20 to 0.78). The prevalence of anemia did not differ significantly between children in the nail clipping group and those in the groups with no nail clipping (AOR 0.53, 95% CI: 0.27 to 1.04). The intensive follow-up and monitoring during this study made it such that the assessment of the observed intervention benefits was under rather ideal circumstances, and hence the study could possibly overestimate the effects when compared to usual conditions.
Handwashing with soap at key times and weekly nail clipping significantly decreased intestinal parasite reinfection rates. Furthermore, the handwashing intervention significantly reduced anemia prevalence in children. The next essential step should be implementing pragmatic studies and developing more effective approaches to promote and implement handwashing with soap and nail clipping at larger scales.
In a factorial cluster randomized controlled trial, Mahmud Abdulkader Mahmud and colleagues examine the efficacy of handwashing with soap and nail clipping on intestinal parasitic infections in school-aged children.
Editors' Summary
Intestinal parasitic infections are common human infections, particularly in resource-limited countries, where personal hygiene and access to clean water and sanitation (disposal of human feces and urine) is often poor. Worldwide, more than a billion people are infected with soil-transmitted helminths—roundworms, tapeworms, and other parasitic worms that live in the human intestine (gut). And millions of people are infected with protozoan (single-celled) intestinal parasites that cause diseases such as amebiasis and giardiasis. Both helminths and protozoan parasites are mainly spread by the fecal-oral route. Infected individuals excrete helminth eggs and protozoan parasites in their feces, and in regions where people regularly defecate in the open, the soil and water supplies become contaminated with parasites. People then ingest the parasites by eating raw, unwashed vegetables, by not washing their hands after handling contaminated soil, or by drinking contaminated water. Mild infections with helminths rarely have symptoms, but severe infections can cause abdominal pain, diarrhea, and malnutrition. Protozoan parasites also cause diarrhea. Importantly, among children, who are particularly susceptible to parasitic infections, intestinal parasite infections may slow growth, affect school performance, and cause anemia.
Why Was This Study Done?
Intestinal worm and protozoan infections can be treated with anthelmintic drugs and antibiotics, respectively. However, reinfection is often rapid, and, particularly in resource-limited countries, additional preventative measures are needed that do not rely on drugs (parasites can become drug-resistant) and that are sustainable with available resources. Given that intestinal parasitic infections usually spread through the fecal-oral route, the promotion of handwashing with soap and regular fingernail clipping might be one way to reduce intestinal parasite infection rates in low-income settings. Handwashing prevents other types of infection, and both unwashed hands and dirty, untrimmed nails are associated with high rates of parasite infection. Here, the researchers investigate whether handwashing with soap and nail clipping reduce intestinal reinfection rates by undertaking a factorial cluster randomized controlled trial (a study that compares outcomes in groups of people chosen at random to receive different combinations of two or more interventions) among school-aged children in northern Ethiopia.
What Did the Researchers Do and Find?
The researchers assigned 367 parasite-negative school-aged children to receive a handwashing intervention, a nail clipping intervention, both interventions, or neither intervention for six months. For the handwashing intervention, fieldworkers visited each intervention household weekly, provided soap, encouraged all the household members to wash their hands with water and soap at key times, such as before meals and after defecation, and checked on the household’s use of soap. For the nail clipping intervention, the fieldworkers clipped the nails of children in the intervention households every week. After six months, parasite reinfection (primary outcome) and anemia (secondary outcome) in the participants were assessed by examining stool samples for parasites and by measuring hemoglobin levels, respectively. After adjustment for factors likely to affect reinfection such as latrine use and drinking water source, 14% of the children in the handwashing with soap groups (handwashing alone and handwashing plus nail clipping) were reinfected with parasites compared to 29% of the children in the no handwashing groups (nail clipping only or neither intervention). Similarly, 17% of the children in the nail clipping groups were reinfected compared to 26% in the no nail clipping groups. Finally, handwashing (but not nail clipping) significantly reduced the rate of anemia among the children.
What Do These Findings Mean?
These findings show that handwashing with soap at key times decreased intestinal parasite reinfection rates by 68% and that weekly nail clipping reduced reinfection rates by 49% among school-aged Ethiopian children. Thus, these findings support the promotion of proper handwashing and weekly nail clipping as a public health measure to reduce parasite reinfection rates in resource-limited regions. However, although both interventions were “efficacious” under trial conditions that included intensive monitoring and follow-up, handwashing and nail clipping may not be “effective” interventions. That is, they may not work as well under real-life conditions. Moreover, because long-established personal hygiene and sanitation practices may be hard to change, large-scale implementation of these interventions might be expensive. The researchers call, therefore, for pragmatic studies to be undertaken to investigate the performance of these interventions under real-life conditions and for the development of effective approaches for widespread promotion of handwashing with soap and nail clipping.
Additional Information
This list of resources contains links that can be accessed when viewing the PDF on a device or via the online version of the article at The US Centers for Disease Control and Prevention provides basic information about protozoan parasites and helminths; its Alphabetical Index of Parasitic Diseases provides more information about roundworms, tapeworms, giardiasis, amebiasis, and other intestinal parasites/parasitic infections; it also provides information about handwashing and about handwashing as a family activityThe World Health Organization provides detailed information about intestinal worms, including a description of its current control strategyPARA-SITE is a multimedia resource provided by the Australian Society of Parasitology that provides detailed information about the biology of intestinal and other parasitesKidsHealth, a site provided by the US-based non-profit Nemours Foundation, provides information for parents, kids, and teenagers about several intestinal parasites and about the importance of handwashing for parents, kids, and teenagers (in English and Spanish)
PMCID: PMC4461173  PMID: 26057703
20.  Associations between salivary testosterone and cortisol levels and neonatal health and growth outcomes 
Early human development  2012;88(10):789-795.
Male vulnerability in health and growth outcomes has often been reported in very low birth weight (VLBW) preterm neonates. On the basis of gender-difference theories, possible associations were explored between the levels of postnatal salivary testosterone/cortisol and the outcomes of neonatal health/growth.
This study used an exploratory and comparative research design. One-hundred-one mother–VLBW preterm neonate pairs were recruited from the neonatal intensive care unit (NICU) of a tertiary medical center in the Southeastern, US. Demographic information, health and growth variables of neonates, and pregnancy and labor variables of mothers were obtained from the medical record reviews and interviews of mothers. Saliva samples from each pair were collected between 9 and 60 days of age. The levels of testosterone and cortisol were determined by using an enzyme immunoassay methodology.
Linear regression analysis showed that neonatal health problems were positively associated with the levels of postnatal salivary testosterone and cortisol, while growth delays were positively associated with the levels of postnatal salivary testosterone after adjusting for the characteristics of neonates and mothers and day of saliva sampling. The salivary levels of testosterone and cortisol were higher in neonates than in mothers. A positive correlation between the levels of testosterone and cortisol was found in neonates and in mothers.
The level of postnatal salivary testosterone is a more reliable marker in assessing neonatal health and growth outcomes compared to salivary cortisol. Further research on both testosterone and cortisol measurements at various stages during the neonatal period may elucidate further these associations.
PMCID: PMC3601806  PMID: 22633533
Salivary testosterone; Salivary cortisol; Neonatal health and growth
21.  Demographic and Ecological Effects on Patterns of Parasitism in Eastern Chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania 
From January 2006 to January 2008, we collected 1,045 fecal samples from 90 individually-recognized, free-ranging, eastern chimpanzees (Pan troglodytes schweinfurthii) inhabiting Gombe National Park, Tanzania to determine how patterns of parasitism are affected by demographic and ecological covariates. Seventeen parasite species were recovered, including eight nematodes (Oesophagostomum sp., Necator sp., Probstmayria gombensis, Strongyloides fulleborni, Ascaris sp., Trichuris sp., Abbreviata caucasica, and an unidentified strongyle), 1 cestode (Bertiella sp.), 1 trematode (Dicrocoeliidae), and 7 protozoa (Entamoeba coli, Entamoeba histolytica/dispar, Iodamoeba bütschlii, Troglodytella abrassarti, Troglocorys cava, Balantidium coli, and an unidentified protozoa). Significant differences were observed in interannual infection prevalence and parasite richness between 2006 and 2007. Intercommunity comparisons demonstrated higher prevalence of parasites for the Mitumba compared with Kasekela chimpanzee community. Prevalence of several parasites was strongly correlated with monthly rainfall patterns for both 2006 and 2007. Subadult chimpanzees had lower prevalence for most parasite species compared with adults in both years and also yielded a lower average parasite species richness. No significant differences were observed between males and females in prevalence in 2006. However, in 2007 the prevalence of S. fulleborni and I. bütschlii were higher in males than in females. Parasite prevalence and richness were substantially higher in this multiyear study compared with previous short-term studies of the gastrointestinal parasites of Gombe chimpanzees. This coupled with the significant interannual and interseasonal variation, demonstrated in this study, emphasizes the importance of multiyear monitoring with adequate sample size to effectively determine patterns of parasitism in wild primate populations.
PMCID: PMC4048996  PMID: 20623606
apes; gastrointestinal parasites; health; noninvasive analyses; zoonoses
22.  Cortisol and testosterone increase financial risk taking and may destabilize markets 
Scientific Reports  2015;5:11206.
It is widely known that financial markets can become dangerously unstable, yet it is unclear why. Recent research has highlighted the possibility that endogenous hormones, in particular testosterone and cortisol, may critically influence traders’ financial decision making. Here we show that cortisol, a hormone that modulates the response to physical or psychological stress, predicts instability in financial markets. Specifically, we recorded salivary levels of cortisol and testosterone in people participating in an experimental asset market (N = 142) and found that individual and aggregate levels of endogenous cortisol predict subsequent risk-taking and price instability. We then administered either cortisol (single oral dose of 100 mg hydrocortisone, N = 34) or testosterone (three doses of 10 g transdermal 1% testosterone gel over 48 hours, N = 41) to young males before they played an asset trading game. We found that both cortisol and testosterone shifted investment towards riskier assets. Cortisol appears to affect risk preferences directly, whereas testosterone operates by inducing increased optimism about future price changes. Our results suggest that changes in both cortisol and testosterone could play a destabilizing role in financial markets through increased risk taking behaviour, acting via different behavioural pathways.
PMCID: PMC4489095  PMID: 26135946
23.  Foci of Endemic Simian Immunodeficiency Virus Infection in Wild-Living Eastern Chimpanzees (Pan troglodytes schweinfurthii) 
Journal of Virology  2003;77(13):7545-7562.
Simian immunodeficiency virus of chimpanzees (SIVcpz) is the immediate precursor to human immunodeficiency virus type 1 (HIV-1), yet remarkably, the distribution and prevalence of SIVcpz in wild ape populations are unknown. Studies of SIVcpz infection rates in wild chimpanzees are complicated by the species' endangered status and by its geographic location in remote areas of sub-Saharan Africa. We have developed sensitive and specific urine and fecal tests for SIVcpz antibody and virion RNA (vRNA) detection and describe herein the first comprehensive prevalence study of SIVcpz infection in five wild Pan troglodytes schweinfurthii communities in east Africa. In Kibale National Park in Uganda, 31 (of 52) members of the Kanyawara community and 39 (of ∼145) members of the Ngogo community were studied; none were found to be positive for SIVcpz infection. In Gombe National Park in Tanzania, 15 (of 20) members of the Mitumba community, 51 (of 55) members of the Kasekela community, and at least 10 (of ∼20) members of the Kalande community were studied. Seven individuals were SIVcpz antibody and/or vRNA positive, and two others had indeterminate antibody results. Based on assay sensitivities and the numbers and types of specimens analyzed, we estimated the prevalence of SIVcpz infection to be 17% in Mitumba (95% confidence interval, 10 to 40%), 5% in Kasekela (95% confidence interval, 4 to 7%), and 30% in Kalande (95% confidence interval, 15 to 60%). For Gombe as a whole, the SIVcpz prevalence was estimated to be 13% (95% confidence interval, 7 to 25%). SIVcpz infection was confirmed in five chimpanzees by PCR amplification of partial pol and gp41/nef sequences which revealed a diverse group of viruses that formed a monophyletic lineage within the SIVcpzPts radiation. Although none of the 70 Kibale chimpanzees tested SIVcpz positive, we estimated the likelihood that a 10% or higher prevalence existed but went undetected because of sampling and assay limitations; this possibility was ruled out with 95% certainty. These results indicate that SIVcpz is unevenly distributed among P. t. schweinfurthii in east Africa, with foci or “hot spots” of SIVcpz endemicity in some communities and rare or absent infection in others. This situation contrasts with that for smaller monkey species, in which infection rates by related SIVs are generally much higher and more uniform among different groups and populations. The basis for the wide variability in SIVcpz infection rates in east African apes and the important question of SIVcpz prevalence in west central African chimpanzees (Pan troglodytes troglodytes) remain to be elucidated.
PMCID: PMC164799  PMID: 12805455
24.  Pubertal testosterone programs context-appropriate agonistic behavior and associated neural activation patterns in male Syrian hamsters 
Physiology & behavior  2013;0:1-7.
Pubertal testosterone programs the level of aggressive behavior displayed by male Syrian hamsters during resident-intruder interactions. To further explore the pubertal programming of adult male agonistic behaviors, the current study investigated the formation, stability, and maintenance of dominant-subordinate relationships in males that either did (T@P) or did not (NoT@P) experience testicular hormones during adolescent development. NoT@P males were gonadectomized prepubertally and T@P males were gonadectomized in adulthood. Four weeks after gonadectomy, all males received testosterone-replacement. Two weeks later, two males of the same hormonal history were given a 60 min introductory trial in a neutral arena, followed immediately and again 24 h later by three 5-min trials. During the introductory trial, each male was deemed dominant, subordinate, or no-status. Brains were collected 1 h after the last trial and sections were stained for Fos-immunoreactivity. Dominant T@P males flank marked more frequently than subordinate and no-status T@P males; this difference was not found in NoT@P males. NoT@P males showed an increase in the number of offensive postures the day after the first series of tests, whereas T@P males did not. Dominant T@P males had significantly more Fos expression than no-status T@P males in anterior cingulate cortex; this relationship was not observed in NoT@P males. Additionally, dominant T@P males had higher Fos expression than dominant NoT@P males in lateral septum. Thus, pubertal testosterone does not organize the formation or stability of male-male relationships, but does program the behavioral strategies used to maintain these relationships over time and the neural correlates of status.
PMCID: PMC3654525  PMID: 23419537
puberty; testosterone; fos; agonistic behavior; cingulate cortex; lateral septum
25.  Testosterone is associated with cooperation during intergroup competition by enhancing parochial altruism 
The steroid hormone testosterone is widely associated with negative behavioral effects, such as aggression or dominance. However, recent studies applying economic exchange tasks revealed conflicting results. While some point to a prosocial effect of testosterone by increasing altruistic behavior, others report that testosterone promotes antisocial tendencies. Taking into account additional factors such as parochial altruism (i.e., ingroup favoritism and outgroup hostility) might help to explain this contradiction. First evidence for a link between testosterone and parochial altruism comes from recently reported data of male soccer fans playing the ultimatum game. In this study high levels of endogenous testosterone predicted increased altruistic punishment during outgroup interactions and at the same time heightened ingroup generosity. Here, we report findings of another experimental task, the prisoner's dilemma, applied in the same context to examine the role of testosterone on parochial tendencies in terms of cooperation. In this task, 50 male soccer fans were asked to decide whether or not they wanted to cooperate with partners marked as either fans of the subject's own favorite team (ingroup) or fans of other teams (outgroups). Our results show that high testosterone levels were associated with increased ingroup cooperation during intergroup competition. In addition, subjects displaying a high degree of parochialism during intergroup competition had significantly higher levels of testosterone than subjects who did not differentiate much between the different groups. In sum, the present data demonstrate that the behavioral effects of testosterone are not limited to aggressive and selfish tendencies but may imply prosocial aspects depending on the context. By this means, our results support the previously reported findings on testosterone-dependent intergroup bias and indicate that this social hormone might be an important factor driving parochial altruism.
PMCID: PMC4464174  PMID: 26124701
testosterone; intergroup conflict; prisoner's dilemma; altruistic behavior; competition

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