Patterns of urinary cortisol levels during ontogeny appear population specific rather than species specific in wild chimpanzees and bonobos.

Compared with most mammals, postnatal development in great apes is protracted, presenting both an extended period of phenotypic plasticity to environmental conditions and the potential for sustained mother-offspring and/or sibling conflict over resources. Comparisons of cortisol levels during ontogeny can reveal physiological plasticity to species or population specific socioecological factors and in turn how these factors might ameliorate or exaggerate mother-offspring and sibling conflict. Here, we examine developmental patterns of cortisol levels in two wild chimpanzee populations (Budongo and Taï), with two and three communities each, and one wild bonobo population (LuiKotale), with two communities. Both species have similar juvenile life histories. Nonetheless, we predicted that key differences in socioecological factors, such as feeding competition, would lead to interspecific variation in mother-offspring and sibling conflict and thus variation in ontogenetic cortisol patterns. We measured urinary cortisol levels in 1394 samples collected from 37 bonobos and 100 chimpanzees aged up to 12 years. The significant differences in age-related variation in cortisol levels appeared population specific rather than species specific. Both bonobos and Taï chimpanzees had comparatively stable and gradually increasing cortisol levels throughout development; Budongo chimpanzees experienced declining cortisol levels before increases in later ontogeny. These age-related population differences in cortisol patterns were not explained by mother-offspring or sibling conflict specifically; instead, the comparatively stable cortisol patterns of bonobos and Taï chimpanzees likely reflect a consistency in experience of competition and the social environment compared with Budongo chimpanzees, where mothers may adopt more variable strategies related to infanticide risk and resource availability. The clear population-level differences within chimpanzees highlight potential intraspecific flexibility in developmental processes in apes, suggesting the flexibility and diversity in rearing strategies seen in humans may have a deep evolutionary history.

Oxytocin reactivity during intergroup conflict in wild chimpanzees.

Intergroup conflict is evident throughout the history of our species, ubiquitous across human societies, and considered crucial for the evolution of humans' large-scale cooperative nature. Like humans, chimpanzee societies exhibit intragroup coordination and coalitionary support during violent intergroup conflicts. In both species, cooperation among group members is essential for individuals to gain access to benefits from engaging in intergroup conflict. Studies suggest that a contributive mechanism regulating in-group cooperation during intergroup conflicts in humans involves the neuropeptide hormone oxytocin, known to influence trust, coordination, and social cognition, although evidence from natural settings is lacking. Here, applying a noninvasive method, we investigate oxytocinergic system involvement during natural intergroup conflicts in wild chimpanzees. We found that chimpanzees of both sexes had significantly higher urinary oxytocin levels immediately before and during intergroup conflict compared with controls. Also, elevated hormone levels were linked with greater cohesion during intergroup conflicts, rather than with the level of potential threat posed by rival groups, intragroup affiliative social interactions, or coordinated behavior alone. Thus, the oxytocinergic system, potentially engendering cohesion and cooperation when facing an out-group threat, may not be uniquely human but rather a mechanism with evolutionary roots shared by our last common ancestor with chimpanzees, likely expediting fitness gains during intergroup conflict.

Urinary oxytocin levels in relation to post-conflict affiliations in wild male chimpanzees (Pan troglodytes verus).

Many animals living in social groups have evolved behaviors to resolve conflicts between group members, behaviors thought crucial for maintaining stable group life. Several hypotheses, based mainly on observational data, aim to explain how post-conflict (PC) affiliations, such as reconciliation and consolation, resolve conflicts by restoring relationships and/or alleviating anxiety. To examine a potential endocrinological mechanism of PC affiliations, we used an experimental-like procedure to investigate whether the oxytocinergic system is activated during naturally observed reconciliations, receiving bystander PC affiliations and aggressions not followed by PC affiliations in wild male chimpanzees. We compared urinary oxytocin (uOT) levels after reconciliations, receiving bystander PC affiliations or aggressions without affiliations with two control conditions: affiliations without previous aggression and after time periods without social interactions. We furthermore tested the 'valuable relationship' hypothesis of reconciliation, as well as the influence of relationship quality between individuals engaged in each of the three behavioral conditions involving aggression on uOT levels. We found that the probability to reconcile a conflict increased with increasing relationship quality between opponents, thus our results support the 'valuable relationship' hypothesis. However, relationship quality did not influence uOT levels, while behavioral condition had a significant effect on uOT levels. uOT levels after reconciliations, receiving bystander PC affiliations and affiliations not related to conflicts were higher than after aggressions alone and time periods without social interactions. Overall, our results indicate that the oxytocinergic system is activated during affiliative interactions, whether occurring as reconciliation, bystander PC affiliation or affiliation alone. We conclude that the oxytocinergic system, in addition to building and maintaining social relationships, also takes part in repairing them.

An assessment of the efficacy of camera traps for studying demographic composition and variation in chimpanzees (Pan troglodytes).

Demographic factors can strongly influence patterns of behavioral variation in animal societies. Traditionally, these factors are measured using longitudinal observation of habituated social groups, particularly in social animals like primates. Alternatively, noninvasive biomonitoring methods such as camera trapping can allow researchers to assess species occupancy, estimate population abundance, and study rare behaviors. However, measures of fine-scale demographic variation, such as those related to age and sex structure or subgrouping patterns, pose a greater challenge. Here, we compare demographic data collected from a community of habituated chimpanzees (Pan troglodytes verus) in the Taï Forest using two methods: camera trap videos and observational data from long-term records. By matching data on party size, seasonal variation in party size, measures of demographic composition, and changes over the study period from both sources, we compared the accuracy of camera trap records and long-term data to assess whether camera trap data could be used to assess such variables in populations of unhabituated chimpanzees. When compared to observational data, camera trap data tended to underestimate measures of party size, but revealed similar patterns of seasonal variation as well as similar community demographic composition (age/sex proportions) and dynamics (particularly emigration and deaths) during the study period. Our findings highlight the potential and limitations of camera trap surveys for estimating fine-scale demographic composition and variation in primates. Continuing development of field and statistical methods will further improve the usability of camera traps for demographic studies.

Does Stochastic and Modulated Wind Turbine Infrasound Affect Human Mental Performance Compared to Steady Signals without Modulation? Results of a Pilot Study.

Wind turbines (WT) are a specific type of noise source, with unique characteristics, such as amplitude modulation (AM) and tonality, infrasonic and low frequency (LF) components. The present study investigates the influence of wind turbine infrasound and low frequency noise (LFN) on human well-being. In the between-subjects study design, 129 students performed a cognitive test evaluating attention and filled out questionnaires in three various exposure conditions, including background noise, synthesized LFN (reference noise) and registered WT infrasound (stimulus). No significant differences in test results or in the number of reported post-exposure feelings and ailments in various exposure conditions were found when analyzing them in males and females, separately. However, a significant association between pre-exposure well-being and reported post-exposure complaints was noted and explained by in-depth statistical analysis.

Shared community effects and the non-genetic maternal environment shape cortisol levels in wild chimpanzees.

Mechanisms of inheritance remain poorly defined for many fitness-mediating traits, especially in long-lived animals with protracted development. Using 6,123 urinary samples from 170 wild chimpanzees, we examined the contributions of genetics, non-genetic maternal effects, and shared community effects on variation in cortisol levels, an established predictor of survival in long-lived primates. Despite evidence for consistent individual variation in cortisol levels across years, between-group effects were more influential and made an overwhelming contribution to variation in this trait. Focusing on within-group variation, non-genetic maternal effects accounted for 8% of the individual differences in average cortisol levels, significantly more than that attributable to genetic factors, which was indistinguishable from zero. These maternal effects are consistent with a primary role of a shared environment in shaping physiology. For chimpanzees, and perhaps other species with long life histories, community and maternal effects appear more relevant than genetic inheritance in shaping key physiological traits.

LC-MS analysis of androgen metabolites in serum and urine from east African chimpanzees (Pan troglodytes schweinfurthii).

Testosterone regulates a wide variety of behavioral and physiological traits in male vertebrates. It influences reproductive and aggressive behaviors and is used as a marker of gonadal activity. While testosterone is the primary biologically active male gonadal steroid in the blood, it is metabolized into a variety of related steroids when excreted via urine and feces. To monitor endocrinological profiles studies on wild-living animals primarily rely on non-invasively collected samples such as urine or feces. Since a number of androgen metabolites that are found in high concentrations in these matrices do not stem exclusively from gonadal production, but are also produced by the adrenal cortex, the metabolism and excretion pattern of testosterone and its characteristic metabolites have to be investigated. Here, we compare the levels of 11 androgens and their metabolites in serum and urine (after hydrolytic/solvolytic cleavage of conjugates) from female, and intact and castrated male chimpanzees to investigate whether they were of testicular or adrenal origin. For serum, significant differences in concentrations were found only for native testosterone. For urine, testosterone concentrations showed the largest differences between intact and castrated males, and intact males and females, while no differences were seen between females and castrated males. Epitestosterone levels revealed the same pattern. These differences in urinary concentrations could also be seen for 5α-androstane-3α,17ß-diol (androstanediol), and less clearly for 5α-dihydrotestosterone (5α-DHT), etiocholanolone, and androsterone. In urine of males, significant correlations were found between the levels of testosterone and 5α-androstane-3α,17ß-diol, as well as between testosterone and epitestosterone. Therefore, the clearest urinary markers of gonadal activity in male chimpanzees seems to be testosterone itself.

Androgen and androgen metabolite levels in serum and urine of East African chimpanzees (Pan troglodytes schweinfurthii): comparison of EIA and LC-MS analyses.

The primary male androgen testosterone (T) is often used as an endocrinological marker to investigate androgen-behaviour interactions in males. In chimpanzees and bonobos, studies investigating the relationship between T levels and dominance rank or aggressive behaviour have revealed contradictory results. The immunoassays used in these studies were originally developed for the measurement of steroids in serum. Their application to non-invasively collected samples, however, can lead to methodological problems due to cross-reacting metabolites, which might occur in urine or faeces but not in blood. The overall aim of this study, therefore, is to clarify whether a T enzyme immunoassay (EIA) is an applicable method to monitor testicular function in adult male chimpanzees. To estimate the impact of cross-reacting androgens on the used T EIA, we compared the results of an EIA measurement with a set of androgen metabolite levels measured by LC-MS. In urine from male chimpanzees, cross-reactivities appear to exist mainly with T and its exclusive metabolites, 5α-dihydrotestosterone (5α-DHT) and 5α-androstanediol (androstanediol). Both urinary and serum T levels of male chimpanzees were significantly higher than female T levels when measured with the T EIA, indicating a reliable measurement of testicular androgens and their exclusive metabolites with the used EIA. In urine from female chimpanzees, the comparison between LC-MS and T EIA results indicated a higher impact of cross-reactions with adrenal androgen metabolites. Therefore, the investigation of urinary T levels in female chimpanzees with a T EIA seems to be problematic. Overall our results show that a T EIA can be a reliable method to monitor testicular function in male chimpanzee urine and that LC-MS is a valuable tool for the validation of immunoassays.

Early maternal loss leads to short- but not long-term effects on diurnal cortisol slopes in wild chimpanzees.

The biological embedding model (BEM) suggests that fitness costs of maternal loss arise when early-life experience embeds long-term alterations to hypothalamic-pituitary-adrenal (HPA) axis activity. Alternatively, the adaptive calibration model (ACM) regards physiological changes during ontogeny as short-term adaptations. Both models have been tested in humans but rarely in wild, long-lived animals. We assessed whether, as in humans, maternal loss had short- and long-term impacts on orphan wild chimpanzee urinary cortisol levels and diurnal urinary cortisol slopes, both indicative of HPA axis functioning. Immature chimpanzees recently orphaned and/or orphaned early in life had diurnal cortisol slopes reflecting heightened activation of the HPA axis. However, these effects appeared short-term, with no consistent differences between orphan and non-orphan cortisol profiles in mature males, suggesting stronger support for the ACM than the BEM in wild chimpanzees. Compensatory mechanisms, such as adoption, may buffer against certain physiological effects of maternal loss in this species.

Long-term repeatability in social behaviour suggests stable social phenotypes in wild chimpanzees.

Consistent individual differences in social phenotypes have been observed in many animal species. Changes in demographics, dominance hierarchies or ecological factors, such as food availability or disease prevalence, are expected to influence decision-making processes regarding social interactions. Therefore, it should be expected that individuals show flexibility rather than stability in social behaviour over time to maximize the fitness benefits of social living. Understanding the processes that create and maintain social phenotypes requires data encompassing a range of socioecological settings and variation in intrinsic state or life-history stage or strategy. Using observational data spanning up to 19 years for some individuals, we demonstrate that multiple types of social behaviour are repeatable over the long term in wild chimpanzees, a long-lived species with complex fission-fusion societies. We controlled for temporal, ecological and demographic changes, limiting pseudo-repeatability. We conclude that chimpanzees living in natural ecological settings have relatively stable long-term social phenotypes over years that may be independent of life-history or reproductive strategies. Our results add to the growing body of the literature suggesting consistent individual differences in social tendencies are more likely the rule rather than the exception in group-living animals.

Group dominance increases territory size and reduces neighbour pressure in wild chimpanzees.

Territorial social species, including humans, compete between groups over key resources. This between-group competition has evolutionary implications on adaptations like in-group cooperation even with non-kin. An emergent property of between-group competition is group dominance. Mechanisms of group dominance in wild animal populations are difficult to study, as they require long-term data on several groups within a population. Here, using long-term data on four neighbouring groups of wild western chimpanzees, we test the hypothesis that group dominance impacts the costs and benefits of between-group competition, measured by territory size and the pressure exerted by neighbouring groups. Larger groups had larger territories and suffered less neighbour pressure compared with smaller groups. Within-group increase in the number of males led to territory increase, suggesting the role of males in territory acquisition. However, variation in territory sizes and neighbour pressure was better explained by group size. This suggests that the bisexually-bonded social system of western chimpanzees, where females participate in territorial behaviour, confers a competitive advantage to larger groups and that group dominance acts through group size in this population. Considering variation in social systems offers new insights on how group dominance acts in territorial species and its evolutionary implications on within-group cooperation.

Between-Group Competition Impacts Reproductive Success in Wild Chimpanzees.

Between-group competition in social animals appears to be a prominent selective pressure shaping the evolution of territoriality and cooperation [1-4]. Evidence for an effect of between-group competition on fitness in territorial species, however, is mostly lacking because of difficulty in measuring between-group competition and its long-term impact [5]. Between-group competition corresponds to a complex set of interactions between neighboring groups, and its intensity seems to depend on the competitive abilities of each interacting group [6, 7]. We tested whether the competitive ability of groups and the pressure exerted by neighboring groups affected the reproductive success of wild female chimpanzees (Pan troglodytes verus). Using long-term data on four neighboring groups in the Taï National Park, Côte d'Ivoire, collected over the course of 54 observation years, we measured the competitive ability of habituated groups using the number of mature males and the pressure exerted by non-habituated neighbors with an index of neighbor pressure that combined the frequency of neighboring encounters and related spatial information. Importantly, we found that experiencing low neighbor pressure provides fitness benefits through increased offspring survival and shorter inter-birth intervals. Also, many males in a group are associated with shorter inter-birth intervals. We conclude that high between-group competition hampers fast reproduction and offspring survival when exposure is during the prenatal period. Our findings suggest that having many males in a group results in fitness benefits and that between-group competition should be considered as a potential selective pressure that shaped key social adaptations in the hominoid lineage.

Urinary Cortisol Increases During a Respiratory Outbreak in Wild Chimpanzees.

In mammals, the excretion of cortisol can provide energy toward restoring homeostasis and is a major component of the stress response. However, chronically elevated cortisol levels also have suppressive effects on immune function. As mounting an immune response is energetically costly, sick individuals may conserve energy by exhibiting certain sickness behaviors, such as declining activity levels. Due to the complex interplay between immune function and sickness behaviors, endocrinological correlates have received growing attention in the medical community, but so far, this subject was investigated rarely. Furthermore, given the complexities of studying illnesses and immunity in natural settings, correlates of sickness behaviors have yet to be studied in non-human primates in the wild. Methods: We measured urinary cortisol levels using liquid chromatography-mass spectrometry in a group of wild habituated chimpanzees in Taï National Park, Côte d'Ivoire, before, during, and after a respiratory disease outbreak (main causative pathogen: human respiratory syncytial virus A, with coinfections of Streptococcus pneumoniae). Changes in cortisol levels were then related to urinary neopterin levels, a biomarker of immune system activation. Results: Urinary cortisol levels were found to be more than 10-fold higher during the outbreak in comparison with levels before and after the outbreak period. Increasing cortisol levels were also associated with increasing neopterin levels. Interestingly, rather atypical patterns in a diurnal decline of cortisol levels were found during infection periods, such that levels remained raised throughout the day. Conclusion: In conclusion, cortisol increase was related to cellular immune response. Our results suggest that cortisol is a mediator of infectious disease pathogenicity through its impact on the immune system and that wild chimpanzees may be facing energetic stress when sick. By monitoring immune challenges in wild-living animals, our study demonstrates that immune defenses have costs and that these costs are context-specific.

Reward of labor coordination and hunting success in wild chimpanzees.

Cooperative hunting and meat sharing are hypothesized as fundamental to human life history adaptations and biological success. Wild chimpanzees also hunt in groups, and despite the potential of inferring ancestral hominid adaptations, it remains unclear whether chimpanzee hunting is a cooperative act. Here we show support for cooperative acquisition in wild chimpanzees since hunters are more likely to receive meat than bystanders, independent of begging effort. Engagement in prey searches and higher hunt participation independently increase hunting success, suggesting that coordination may improve motivation in joint tasks. We also find higher levels of urinary oxytocin after hunts and prey searches compared with controls. We conclude that chimpanzee hunting is cooperative, likely facilitated by behavioral and neuroendocrine mechanisms of coordination and reward. If group hunting has shaped humans' life history traits, perhaps similar pressures acted upon life history patterns in the last common ancestor of human and chimpanzee.

Flexible decision-making in grooming partner choice in sooty mangabeys and chimpanzees.

Living in permanent social groups forces animals to make decisions about when, how and with whom to interact, requiring decisions to be made that integrate multiple sources of information. Changing social environments can influence this decision-making process by constraining choice or altering the likelihood of a positive outcome. Here, we conceptualized grooming as a choice situation where an individual chooses one of a number of potential partners. Studying two wild populations of sympatric primate species, sooty mangabeys (Cercocebus atys atys) and western chimpanzees (Pan troglodytes verus), we tested what properties of potential partners influenced grooming decisions, including their relative value based on available alternatives and the social relationships of potential partners with bystanders who could observe the outcome of the decision. Across 1529 decision events, multiple partner attributes (e.g. dominance ranks, social relationship quality, reproductive state, partner sex) influenced choice. Individuals preferred to initiate grooming with partners of similar global rank, but this effect was driven by a bias towards partners with a high rank compared to other locally available options. Individuals also avoided grooming partners who had strong social relationships with at least one bystander. Results indicated flexible decision-making in grooming interactions in both species, based on a partner's value given the local social environment. Viewing partner choice as a value-based decision-making process allows researchers to compare how different species solve similar social problems.

Bystanders intervene to impede grooming in Western chimpanzees and sooty mangabeys.

Grooming interactions benefit groomers, but may have negative consequences for bystanders. Grooming limits bystanders' grooming access and ensuing alliances could threaten the bystander's hierarchy rank or their previous investment in the groomers. To gain a competitive advantage, bystanders could intervene into a grooming bout to increase their own grooming access or to prevent the negative impact of others' grooming. We tested the impact of dominance rank and social relationships on grooming intervention likelihood and outcome in two sympatric primate species, Western chimpanzees (Pan troglodytes verus) and sooty mangabeys (Cercocebus atys atys). In both species, rather than increasing their own access to preferred partners, bystanders intervened mainly when an alliance between groomers could have a negative impact on them: when the lower-ranking groomer was close to the bystander in rank, when either groomer was an affiliation partner whose services they could lose, or the groomers were not yet strongly affiliated with each other. Thus, bystanders in both species appear to monitor grooming interactions and intervene based on their own dominance rank and social relationships, as well as triadic awareness of the relationship between groomers. While the motivation to intervene did not differ between species, mangabeys appeared to be more constrained by dominance rank than chimpanzees.

Polish Translation and Validation of the Tinnitus Handicap Inventory and the Tinnitus Functional Index.

Objective: The need for validated measures enabling clinicians to classify tinnitus patients according to the severity of tinnitus and screen the progress of therapies in our country led us to translate into Polish and to validate two tinnitus questionnaires, namely the Tinnitus Handicap Inventory (THI) and the Tinnitus Functional Index (TFI). Design: The original English versions of the questionnaires were translated into Polish and translated back to English by three independent translators. These versions were then finalized by the authors into a Polish THI (THI-Pl) and a Polish TFI (TFI-Pl). Participants from three laryngological centers in Poland anonymously answered the THI-Pl (N = 98) and the TFI-Pl (N = 108) in addition to the Polish versions of the Center for Epidemiologic Studies Depression Scale as a measure of self-perceived level of depression, and the Satisfaction With Life Scale to assess self-perceived quality of life. Both were used to determine discriminant validity. Two Visual Analog Scales were used to measure tinnitus annoyance and tinnitus loudness in order to determine convergent validity. Results: Similar to the original version of the THI, the THI-Pl showed a high internal consistency (Cronbach's α = 0.93). The exploratory factor analysis revealed that the questionnaire has a three-factorial structure that does not correspond to the original division for functional, catastrophic, and emotional subscales. Convergent and discriminant validities were confirmed. The TFI-Pl showed high internal consistency (Cronbach's α = 0.96) with the reliability ranging from 0.82 to 0.95 for its different subscales. Factor analysis confirmed an eight-factorial structure with factors assigning all items to appropriate subscales reported in the original version of the questionnaire. Discriminant and convergent validities were also confirmed for the TFI-Pl. Conclusion: We translated and validated the Polish versions of the THI and the TFI to make them suitable for clinical use in Poland.

Audio-visual interactions in environment assessment.

The aim of the study was to examine how visual and audio information influences audio-visual environment assessment. Original audio-visual recordings were made at seven different places in the city of Poznan. Participants of the psychophysical experiments were asked to rate, on a numerical standardized scale, the degree of comfort they would feel if they were in such an environment. The assessments of audio-visual comfort were carried out in a laboratory in four different conditions: (a) audio samples only, (b) original audio-visual samples, (c) video samples only, and (d) mixed audio-visual samples. The general results of this experiment showed a significant difference between the investigated conditions, but not for all the investigated samples. There was a significant improvement in comfort assessment when visual information was added (in only three out of 7 cases), when conditions (a) and (b) were compared. On the other hand, the results show that the comfort assessment of audio-visual samples could be changed by manipulating the audio rather than the video part of the audio-visual sample. Finally, it seems, that people could differentiate audio-visual representations of a given place in the environment based rather of on the sound sources' compositions than on the sound level. Object identification is responsible for both landscape and soundscape grouping.

Polish version of standardized noise reaction questions for community noise surveys.

OBJECTIVES: This article presents the Polish version of two standardized noise reaction questions for community noise surveys. An internationally comparable noise reaction measure for social surveys was published by Fields et al. as a result of work performed by the Community Response to Noise Team of the International Commission on the Biological Effects of Noise. This measure consists of two recommended noise reaction questions: a 5-point verbal scale question and a 0-10-point numeric scale question. METHODS: The Polish words for a 5-point noise annoyance verbal scale were selected by respondents from a group of 21 potential adverbs following the method described by Fields et al. The same standardized empirical study protocol was used to select annoyance scale words (a 5-point verbal scale question) for the nine different languages. RESULTS: The following words for a 5-point noise annoyance scale were obtained: not at all, a little, rather, substantially, extremely annoying. CONCLUSIONS: The Polish version of the scale described in this paper has international counterparts. It means that our data expand the world database on human reactions to noise in different communities and become more comparable with the data from other countries.