Influence of keeping conditions of behavior and stress in captive apes

Im Lauf der vergangenen Jahrzehnte hat sich die Einstellung des Menschen gegenüber der Haltung exotischer Tiere dahingehend gewandelt, dass diese nicht mehr nur dem Wohlbefinden des Menschen dienen sollen. Vielmehr steht heute das Wohlbefinden der Tiere in einem für sie adäquaten Haltungssystem im Vordergrund. Die Bewertung von Haltungssystemen und die Beurteilung des Wohlbefindens der Tiere spielen eine immer bedeutungsvollere Rolle. Die Tiere im Zoo sollen sich möglichst natürlich verhalten. Um Verhaltensauffälligkeiten entgegenzuwirken, wird in den meisten Zoos eine Tierbeschäftigung durchgeführt. Um das Wohlbefinden der Tiere beurteilen zu können sind reine Verhaltensbeobachtungen unter Umständen nicht ausreichend und endokrine Aspekte können diese vervollständigen. Die vorliegende Studie behandelt den Einfluss der Haltungsbedingungen und der Beschäftigung auf das Verhalten von drei Menschenaffenarten. Zur Unterstützung der Verhaltensdaten wurden Speichelproben gesammelt und hinsichtlich ihrer Cortisolkonzentration ausgewertet. Ziel der Studie war es, Verhaltensänderungen nach einem Transfer von einem alten in ein neues Gehege, oder nach dem Einbringen von Beschäftigungen, im Zoo Frankfurt, zu dokumentieren und mithilfe der Speichelproben bewerten zu können. Für die Speichelproben wurde in dieser Untersuchung eine chemische und eine biologische Validierung für die Analyse von Cortisol und Cortison im Speichel der drei gehaltenen Menschenaffenarten ermöglicht. Daten wurden von den drei im Zoo Frankfurt gehaltenen Menschenaffenarten gesammelt und mit dem bisherigen Wissenstand von Freiland- und Zoo-Publikationen abgeglichen. Der Beobachtungszeitraum wurde in Phasen aufgeteilt. Es wurden die Verhaltensweisen und Cortisolkonzentrationen im alten Menschenaffenhaus, mit der Zeit vor dem Umzug, dem Umzug selbst und im neunen Menschenaffenhaus verglichen. Hinzu kam ein Vergleich von einem Zeitraum mit und ohne Beschäftigung im alten Menschenaffenhaus. Bei den Gorillas wurde als fünfter Zeitraum die Integration eines Schwarzrückens in die bestehende Gorilla-Gruppe, aufgenommen. Die Verhaltensweisen aller drei Menschenaffenarten unterschieden sich in den gebildeten Phasen. In Verbindung mit dem Umzug konnte eine engere Gruppenbindung bei den Gorillas und Bonobos nachgewiesen werden, bei den Gorillas war dies außerdem bei der Integration des jungen Männchens beobachtet worden. Des Weiteren förderte das neue Gehege bei allen drei Arten das Erkundungsverhalten. Auf das Spielverhalten wirkten sich sowohl der Umzug bei allen drei Arten wie auch die Integration des Schwarzrückens bei den Gorillas negativ aus. Für die Orang-Utan Gruppe konnten die meisten positiven Verhaltensänderungen dokumentiert werden. Das neue Gehege bot ein größeres Raumangebot und vor allem auch eine auf die Höhe ausgelegte Kletterstruktur. Außerdem konnten die Orang-Utans den unmittelbaren Kontakt mit Artgenossen vermeiden, was zu einer Reduktion von Auseinandersetzungen führte. Bei der Gorilla-Gruppe führte der Umzug, das Verscheiden des Silberrückens und die Integration eines neuen Männchens zu einer stetigen Veränderung. In diesem Kontext konnte auch eine ungewöhnliche hohe Aktivität bei den Gorillas nachgewiesen werden. Ein weiterer Aspekt der Studie hatte sich auf die Beschäftigung der drei Menschenaffenarten konzentriert. Alle drei getesteten Beschäftigungsvarianten waren von den Menschenaffen angenommen worden. Dabei konnten inter- als auch intraartliche Präferenzen festgestellt werden. Ein Ergebnis war, dass neben besonders großen Futtermitteln auch kleinere Nahrungsmittel in den Beschäftigungen anzubieten waren, um den Anreiz über einen längeren Zeitraum konstant zu halten. Im Zusammenhang mit der Beschäftigungsvariante Kistensystem konnte bei allen drei Arten der Einsatz von Werkzeugen nachgewiesen werden. Ein dritter Aspekt wurde durch die Messung von Cortisol und Cortison im Speichel der drei Menschenaffenarten gebildet. Die Ergebnisse zeigten, dass es artspezifische Unterschiede gab. Auch führten unterschiedliche Stressparameter bei den Tieren zu erhöhten Cortisolkonzentrationen. Bei allen drei Arten wurde ein circadianer Rhythmus für das immunreaktive Cortisol im Speichel nachgewiesen. Die gemessenen Cortisolkonzentrationen gingen mit aufgezeichneten Stressverhaltensweisen einher, und konnten daher zur Bewertung der Stresssituation der untersuchten Menschenaffen herangezogen werden. Außerdem wurde ebenfalls bei allen drei Arten eine deutlich höhere Menge von Cortison als Cortisol im Speichel gefunden, wie auch eine Korrelation der beiden Hormone. Die Ergebnisse dieser Arbeit zeigen, wie unterschiedlich die drei Menschenaffenarten auf Veränderungen in ihrer unmittelbaren Umwelt reagieren. Die Studie könnte Impulse liefern, welche Gehegestrukturen von Vorteil für die Tiere sind und welche Besonderheiten bedacht werden sollten. Die Sammlung von Speichelproben kann nicht auf Untersuchungen im Feld übertragen werden, jedoch können Einblicke in das Wohlbefinden der Tiere gewonnen werden.In the last decades the keeping of exotic animals had changed. Zoological parks were initially built to suit human needs. Focus nowadays is on the welfare and the keeping conditions of animals. The evaluation of welfare and keeping becomes more and more important. Animals should behave as naturally as possible, but in zoos a lot of animal times is spent in routines. Environmental enrichment can be used to prevent routines and abnormal behavior and to improve welfare. To measure the welfare of the animal collecting behavioral data is often not enough and endocrine measurements can be used to complement them. The main aspects of this study were to find out, if keeping conditions and enrichment influenced the daily- and social behavior of western lowland gorillas, Sumatran orangutans and bonobos. To support the behavioral data, saliva samples were collected and analyzed for immunoreactive Cortisol concentration. Behaviour and saliva samples were collected in different but enriched environments: the new and the old great ape house Frankfurt Zoo. Furthermore, a chemical as well as a biological validation for cortisol and cortisone in the saliva of these three apes species was conducted. Behavioral data as well as saliva were sampled in three ape species and examined in the light of the existing literature whether on captive groups or from wild animals. The observation time was divided in four parts for orangutans and bonobos, and in five parts for the gorillas. Behavioral data and saliva samples were sampled at the old great ape house, without enrichment and then with enriched condition, during the transfer and in the new great ape house. For the gorilla-group a fifth phase was established during the integration of a blackback male after the death of a silverback in the existing group. The results of this study suggest that the behavior of all three species was influenced by the four holding conditions. An increase of group cohesion was found in gorillas and bonobos during and after the transfer. Also a strong group cohesion was documented for the gorillas during the integration of the new male. Moreover an increase in the exploration behavior was observed in the new environment for all three species. Also in all three species the play behavior decreased for a short period of time after the transfer. In gorillas the same decrease in play behavior was seen after the integration of the blackback male. The most changes in positive behavior were observed in the Sumatran orangutan group. In the new environment more space was available and a high climbing structure was provided. In the new enclosure, orangutans were less often on the ground as seen in wild animals. They avoided close contact with other group members, and a decrease in aggression behavior was observed. The behavior of the gorilla group was unstable, due to the transfer, the dead of the silverback and the integration of the new male. During this time the activity of all gorillas increased. Another aspect of this study was the environmental enrichment. All three enrichments were used in every species. Inter- and intraspecific differences were found. Most often it depended on the age of the animal. One important result for a longer use of the enrichment was that beside from the main food pieces small food pieces should also be provided. The bonobos preferred the tennis balls and the gorillas the box puzzle feeder (K1). For orangutans no preference was found but they exhibited more diversity in the way they used enrichments. For all three species the box puzzle feeder provoked tool use abilities. The third aspect was the measurement of cortisol and cortisone in the saliva of the three species. A chemical as well as a biological validation was conducted. The results of the hormones showed species-specific differences. Also different stress responses to events were found. In all three species a circadian rhythm was detected. Furthermore, the cortisol concentration correlated with the behavioral data. In all species a higher amount of cortisone than cortisol was found in saliva. And there was a correlation between cortisone and cortisol’s concentrations. The study showed how the environment could influence the behavior of great apes in keeping conditions. The results could be used as advice for enclosure structure or enrichment options. The saliva measurement may not be used directly in field studies but remains complementary to understand and improve the welfare of zoo kept animals

Nasal temperature drop in response to a playback of conspecific fights in chimpanzees : a thermo-imaging study

This study was conducted in part under the first author's postdoc program; the Japan Society for Promotion of Science (JSPS) for study abroad. FK and SH respectively received JSPS KAKENHI Grant Number 26885040 and 26245069. This study was also in part funded by JSPS MEXT KAKENHI Grant Number 24000001, JSPS-LGP-U04, JSPS core-to-core type A CCSN, and MEXT-PRI-Human Evolution.Emotion is one of the central topics in animal studies and is likely to attract attention substantially in the coming years. Recent studies have developed a thermo-imaging technique to measure the facial skin temperature in the studies of emotion in humans and macaques. Here we established the procedures and techniques needed to apply the same technique to great apes. We conducted two experiments respectively in the two established research facilities in Germany and Japan. Total twelve chimpanzees were tested in three conditions in which they were presented respectively with the playback sounds (Exp. 1) or the videos (Exp. 2) of fighting conspecifics, control sounds/videos (allospecific display call: Exp. 1; resting conspecifics: Exp. 2), and no sound/image. Behavioral, hormonal (salivary cortisol) and heart-rate responses were simultaneously recorded. The nasal temperature of chimpanzees linearly dropped up to 1.5. °C in 2. min, and recovered to the baseline in 2. min, in the experimental but not control conditions. We found the related changes in excitement behavior and heart-rate variability, but not in salivary cortisol, indicating that overall responses were involved with the activities of sympathetic nervous system but not with the measureable activities of the hypothalamus-pituitary-adrenal (HPA) axis. The influence of general activity (walking, eating) was not negligible but controllable in experiments. We propose several techniques to control those confounding factors. Overall, thermo-imaging is a promising technique that should be added to the traditional physiological and behavioral measures in primatology and comparative psychology.PostprintPeer reviewe

2. Izbor iz vojne ostavine Svetozara Borojevića od Bojne; 2.1.7. Razdoblje između Četvrte i Šeste bitke na Soči (sredina prosinca 1915. do početka kolovoza 1916.)

Ecological immunology proposes that the optimal immune defence, and the costs coming with it, vary across environments. In environments with higher pathogen load, the immune system should experience greater challenges and, therefore, investment in maintaining it should be higher. The biomarker neopterin allows monitoring of innate immune responses, and is therefore an ideal tool to investigate the effects of ecological variables on the immune system. Here, we compared urinary neopterin levels of apparently healthy chimpanzees without acute symptoms of sickness across two environments: in captivity (22 zoos) and in the wild (two populations)

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.Publisher PDFPeer reviewe

The Steady State Great Ape? Long Term Isotopic Records Reveal the Effects of Season, Social Rank and Reproductive Status on Bonobo Feeding Behavior

Dietary ecology of extant great apes is known to respond to environmental conditions such as climate and food availability, but also to vary depending on social status and life history characteristics. Bonobos (Pan paniscus) live under comparatively steady ecological conditions in the evergreen rainforests of the Congo Basin. Bonobos are an ideal species for investigating influences of sociodemographic and physiological factors, such as female reproductive status, on diet. We investigate the long term dietary pattern in wild but fully habituated bonobos by stable isotope analysis in hair and integrating a variety of long-term sociodemographic information obtained through observations. We analyzed carbon and nitrogen stable isotopes in 432 hair sections obtained from 101 non-invasively collected hair samples. These samples represented the dietary behavior of 23 adult bonobos from 2008 through 2010. By including isotope and crude protein data from plants we could establish an isotope baseline and interpret the results of several general linear mixed models using the predictors climate, sex, social rank, reproductive state of females, adult age and age of infants. We found that low canopy foliage is a useful isotopic tracer for tropical rainforest settings, and consumption of terrestrial herbs best explains the temporal isotope patterns we found in carbon isotope values of bonobo hair. Only the diet of male bonobos was affected by social rank, with lower nitrogen isotope values in low-ranking young males. Female isotope values mainly differed between different stages of reproduction (cycling, pregnancy, lactation). These isotopic differences appear to be related to changes in dietary preference during pregnancy (high protein diet) and lactation (high energy diet), which allow to compensate for different nutritional needs during maternal investment

Salivary cortisol reaction norms in zoo-housed great apes : diurnal slopes and intercepts as indicators of stress response quality

SIMPLE SUMMARY: Changes in cortisol fluctuations are used for stress monitoring. Methodologically, this is straight forward, because sample collection is simple and analytical methods advanced, but since cortisol is primarily a hormone that facilitates energy allocation, the interpretation of these measures is often complex. Acute elevations in cortisol levels are not per se bad, but may constitute an adaptive coping mechanism. Likewise, low cortisol levels do not always indicate the absence of a stressor. To distinguish between stress response qualities, a more fine-grained analyses of cortisol fluctuations is warranted. Cortisol excretion follows a diurnal pattern with high levels in the morning, decreasing throughout the day. Two regression coefficients describe this curve: the intercept (the constant with which levels change throughout the day) and the slope (curve steepness and direction). We assessed salivary cortisol intercepts and slopes in zoo-housed apes on routine days, enrichment days, and in the new ape house. While cortisol excretion increased on enrichment days, the daily decline of cortisol levels was not affected. The move to the new house seemingly was a major stressor as cortisol levels increased slightly and the circadian cortisol decrease was impaired. The combination of intercept and slope measures can differentiate between stress responses, thereby constituting a useful tool for stress monitoring. ABSTRACT: Monitoring changes in cortisol levels is a widespread tool for measuring individuals’ stress responses. However, an acute increase in cortisol levels does not necessarily denote an individual in distress, as increases in cortisol can be elicited by all factors that signal the need to mobilize energy. Nor are low levels of cortisol indicative for a relaxed, healthy individual. Therefore, a more fine-grained description of cortisol patterns is warranted in order to distinguish between cortisol fluctuations associated with different stress response qualities. In most species, cortisol shows a distinct diurnal pattern. Using a reaction norm approach, cortisol levels across the day can be described by the two regression coefficients: the intercept and the slope of the curve. We measured immunoreactive salivary cortisol in three zoo-housed ape species under three conditions (routine days, enrichment days, and after the move to a new house). We examined salivary cortisol intercepts (SCI) and salivary cortisol slopes (SCS) of the diurnal curves. SCI and SCS were independent from each other. SCI was highest on enrichment days and lowest on routine days. SCS was steep on routine days and blunted after the move. Only SCI was species-specific. Our study provides evidence that combining SCI and SCS measures allows us to differentiate between types of stress responses, thereby constituting a useful tool for welfare assessment

Urinary neopterin levels increase and predict survival during a respiratory outbreak in wild chimpanzees (Taï National Park, Côte d’Ivoire)

Monitoring immune system activation of wild animals has garnered increasing interest within the field of ecological immunology, leading to an urgent need for non-invasive biomarkers measuring these changes. Urinary neopterin, a marker of the cell-mediated immune response, is validated as an immune-related biomarker in captive and laboratory animals. However, wild animals naturally host higher and chronic pathogen loads. Therefore, detection and quantification of additional infections via neopterin might not be possible against the background of a chronically challenged immune system. To assess the suitability of urinary neopterin in wild animals, we measured neopterin corrected for specific gravity with an enzyme immunoassay in 185 samples collected before, during and after a respiratory disease outbreak in 28 individuals from a group of wild chimpanzees (Taï National Park, Côte d’Ivoire). Urinary neopterin levels were significantly higher during periods when individuals showed respiratory symptoms versus before and after the outbreak. Furthermore, urinary neopterin levels were significantly higher in individuals that died, with higher levels already apparent before the outbreak, suggesting individuals may have an already activated immune system. Measuring urinary neopterin levels, with other biomarkers of energetic condition, stress challenges, and reproduction will contribute towards a deeper understanding of life-history trade-offs in wild animals.Peer Reviewe

Plasma testosterone and androstenedione levels follow the same sex-specific patterns in the two Pan species

In most animals, males are considered more aggressive, in terms of frequency and intensity of aggressive behaviors, than their female peers. However, in several species this widespread male-biased aggression pattern is either extenuated, absent, or even sex-reversed. Studies investigating potential neuro-physiological mechanisms driving the selection for female aggression in these species have revealed an important, but not exclusive role of androgens in the expression of the observed sex-specific behavioral patterns. Two very closely related mammalian species that markedly differ in the expression and degree of sex-specific aggression are the two Pan species, where the chimpanzee societies are male-dominated while in bonobos sex-biased aggression patterns are alleviated. Using liquid chromatography–mass spectrometry (LC-MS) methods, we measured levels of plasma testosterone and androstenedione levels in male and female zoo-housed bonobos (N = 21; 12 females, 9 males) and chimpanzees (N = 41; 27 females, 14 males). Our results show comparable absolute and relative intersexual patterns of blood androgen levels in both species of Pan. Plasma testosterone levels were higher in males (bonobos: females: average 0.53 ± 0.30 ng/mL; males 6.70 ± 2.93 ng/mL; chimpanzees: females: average 0.40 ± 0.23 ng/mL; males 5.84 ± 3.63 ng/mL) and plasma androstenedione levels were higher in females of either species (bonobos: females: average 1.83 ± 0.87 ng/mL; males 1.13 ± 0.44 ng/mL; chimpanzees: females: average 1.84 ± 0.92 ng/mL; males 1.22 ± 0.55 ng/mL). The latter result speaks against a role of androstenedione in the mediation of heightened female aggression, as had been suggested based on studies in other mammal species where females are dominant and show high levels of female aggressivenes