Glucocorticoid Metabolite Levels Research Articles

Effects of reproductive seasonality on the excretion of fecal glucocorticoid metabolites in free‐ranging Pampas Deer

AbstractUnderstanding how fecal glucocorticoid (GC) concentration is associated with reproduction in wild animals allows us to associate physiological stress with the costs of reproduction. Glucocorticoids are among the main stress‐related hormones, and their secretion is strongly associated with reproductive seasonality. Using non‐invasive methods (thereby avoiding causing stress), we used fecal GC metabolites (FGC) to test the hypothesis that the reproductive phase (mating, non‐mating, gestation, and lactation) influences stress levels of the seasonally reproductive Pampas Deer (Ozotoceros bezoarticus). Furthermore, we compared FGC between sexes and between males of different antler statuses (velvet, hard, cast). During 1 year, in the Pantanal of Brazil, we collected 621 fresh fecal samples (327 from females, 294 from males) from which we estimated FGC using enzyme immunoassay (EIA). FGC concentrations varied by reproductive phase and antler status. Agonistic and courtship interactions associated with mating (i.e., fights between males, attempts to mount females), suggest that they influence FGC concentrations most strongly in both sexes. Females also had greater FGC concentrations during lactation, suggesting that this phase and parental care are also associated with increased physiological stress. In males, the association of FGC concentrations with antler status may be, in part, associated with photoperiod and testosterone secretion, both of which can trigger reproductive and agonistic behaviors. Finally, reproductive synchrony of the sexes causes similar FGC over time and suggests that environmental factors contribute as well. We show that non‐invasive monitoring of glucocorticoid metabolites levels is an effective tool for detecting changes in the physiological stress response in Pampas Deer, suggesting that this tool will be useful for detecting changes in physiological stress caused by human disturbance, such as cattle ranching in Pantanal and similar disturbances elsewhere.

The Comparative Effect of Occupational and Musical Enrichment on Fecal Glucocorticoid Metabolite Levels in a Captive Colony of Stumptail Macaques (Macaca arctoides).

Environmental enrichment improves captive animal welfare by reducing stress-related behaviors. Previous studies in a captive colony of stumptail macaques (Macaca arctoides) reported a reduction of aggression, coprophilia, and stereotypic behaviors after an occupational enrichment program; however, the effect on stress hormones such as glucocorticoids has not been investigated yet. The goal of this study was to compare the effect of sex, age, and social rank on changes in fecal glucocorticoid metabolites (fGCM) after applying two kinds of enrichments (occupational vs. musical) in a captive colony of stumptail macaques. We collected 234 fecal samples from 25 stumptail macaques under the following conditions: (1) basal (no enrichment), (2) three weeks of occupational enrichment, and (3) three weeks of relaxing/classical music. The Generalized Estimated Equation Model showed an increase in fGCM levels after the occupational enrichment only in adult subjects (p = 0.003 compared to basal). The fGCM levels reached by the adults after the occupational enrichment was higher than that of juveniles (p = 0.002) and subadults (p = 0.02). Occupational and musical enrichment decreased fGCM levels only in middle-ranking individuals (p < 0.001 and p = 0.013, respectively). No sex differences were found. In conclusion, there were age and rank differences in individuals' physiological reactivity to the effects of environmental enrichment which need to be considered when planning enrichment programs.

Reaction to Novel Objects and Fecal Glucocorticoid Metabolite Levels in Two Species of Nocturnal Geckos.

Many reptiles are maintained in captivity and heavily traded, although welfare measures for many species are not well established and are under-researched compared to other animals. In this study, we focused on two of these species: crested geckos (Correlophus ciliatus) and leopard geckos (Eublepharis macularius). To better interpret their behavior in captivity, the individual reaction to novel objects and the fecal glucocorticoid metabolite levels were measured in an attempt to identify the potential correlation between them. Also, we explored if some characteristic of the objects (e.g., color, shape, or smell) resulted in being more attractive to some species and/or individuals. Equivalent responses to different objects were not obtained for all the geckos, the behavioral response being highly individual and context-dependent, although modulated by the species. Individuals which manipulated earlier and interacted longer with novel objects showed lower basal fecal corticosterone metabolite (FCM) levels. Differences according to the species suggested that crested geckos have significantly greater and more variable FCM levels than leopard geckos. Our results can help to understand the reaction of geckos to novelty and have the potential to serve in their welfare assessment, although more studies are needed to proper establish welfare protocols.

Identifying potential measures of stress and disturbance during a captive to wild African elephant reintegration.

There is increasing evidence of compromised welfare for elephants managed in captivity. Should such facilities eventually close, more elephants will need to be rehabilitated and reintegrated into the wild. The goal of such reintegration would be to restore any physical or psychological aspects of the elephant that may have been compromised in captivity, followed by introduction into a free-roaming system where they can interact with other elephants. However, to achieve this goal, the reintegration methods implemented need to be assessed to ensure that welfare remains the priority. The objective of this study was to test whether parameters generally associated with stress and disturbance in African elephants, respond to changes in potentially stressful environmental conditions, assessed at multiple temporal scales ranging from minutes to months. The main changes in environmental conditions that were investigated included the different phases of reintegration of a group of elephants from captivity into the wild. Stress and disturbance related parameters used for comparisons included physiological responses, namely the extent of temporal gland secretions (eTGS) and faecal glucocorticoid metabolite (fGCM) levels as well as behavioural responses, namely the display of stereotype and stress-related behaviours. Results showed that eTGS significantly increased during the initial release of the elephants compared to when in captivity. Stereotypic behaviours were only recorded during the captive phase and immediately ceased after release. Faecal GCM levels spiked in the first year after release before decreasing back to pre-reintegration levels during the third year. These findings indicate that fGCM levels, the eTGS and disturbance related behaviours all proved effective in explaining the changes in stress and disturbance experienced by elephants during the initial years after being reintegrated from captivity into the wild.

Effects of Tourist and Researcher Presence on Fecal Glucocorticoid Metabolite Levels in Wild, Habituated Sulawesi Crested Macaques (Macaca nigra).

Ecotourism managers and researchers often assume that apparently habituated primate groups no longer experience adverse consequences of prolonged exposure to tourists or researchers. We examined the effects of tourists and researchers on fecal glucocorticoid metabolite output (FGCM) in three critically endangered, wild crested macaque (Macaca nigra) groups in Tangkoko Nature Reserve, Sulawesi, Indonesia. We assayed FGCM from 456 fecal samples collected from thirty-three adults. Tourists can walk through and among macaque groups freely. Hence, we examined the possible effects of tourists both (1) in the reserve when away and not interacting with the study groups and (2) when they were present within the macaque groups. Generalized Linear Mixed Model (GLMM) analysis indicated that when tourists were present in the forest, but not directly among the macaques, FGCM levels in the macaque tourism groups were higher in months with more tourists. When tourists were among the macaque groups, some female macaques experienced rises and subsequent postexposure decreases in FGCM levels, consistent with predictions for acute stress. Male FGCM levels increased with tourist numbers within the group. Nevertheless, they were not significantly different from levels during undisturbed or postexposure conditions. FGCM responses related to researchers in groups varied by group, sex, and tourist presence. However, the temporal patterning of FGCM responses showed little evidence of chronic stress from tourism at this site.

Faecal glucocorticoid metabolite levels of intensive captive, free‐range captive and wild Tasmanian devils

AbstractCaptivity can alter the stress physiology and behaviour of an animal in both the short‐ and long‐term through repetitive exposure to novel stressors and, subsequently, may reduce the success of conservation efforts such as translocation and reintroduction. The Tasmanian devil (Sarcophilus harrisii) is threatened with extinction from a fatal facial tumour disease which has led to the establishment of an insurance meta‐population designed for future reintroductions of disease‐free devils. The meta‐population is comprised of intensive captive and free‐range captive environments; however, no study has yet examined the long‐term physiological implications of captivity on devils. We used non‐invasive faecal glucocorticoid metabolite (FGM) monitoring to determine if there were any differences in adrenal activity among intensive captive, free‐range captive and wild devils. FGM levels were not age or sex dependent, and we found that all population types had similar intra‐population variability and mean FGMs. In conclusion, both types of captive environment appear to maintain stress profiles similar to wild devils.

Diurnal fecal glucocorticoid metabolite rhythms in a cathemeral primate, the red-bellied lemur (Eulemur rubriventer), and across mammalian species.

Measuring glucocorticoids is one of the most reliable and widely used techniques to monitor stress responses, however invasive techniques to collect plasma samples may not be applicable for wild populations. Monitoring excreted glucocorticoids is an effective noninvasive technique that researchers have used increasingly over the past two decades, and it has allowed the investigation of glucocorticoids in a variety of species with a range of activity patterns. Many species exhibit predictable circadian patterns of glucocorticoid secretion in accordance with their daily activity pattern. There remains a gap in our understanding of how excreted glucocorticoid metabolites vary throughout the day and across species, despite the utility of this information when developing sampling protocols and analyzing data. We investigated circadian patterns of glucocorticoid excretion in a cathemeral primate species, Eulemur rubriventer (red-bellied lemur), in Ranomafana National Park, Madagascar. We collected fecal samples from 10 individuals throughout the day and analyzed fecal glucocorticoid levels across three time points (Early, Midday, and Late), and again across two time points (Morning and Afternoon). We also investigated whether activity pattern, sex (as a control variable), and other traits associated with gut passage rate (diet, body mass) could help predict the presence and timing of circadian patterns of fecal glucocorticoid metabolites across mammal species. We found that fecal glucocorticoid metabolite levels in E. rubriventer fluctuate throughout the day, with lowest levels in the morning and peak levels in the afternoon. None of the variables that we tested predicted whether daily fecal glucocorticoid metabolites changed significantly throughout the day, nor when levels were likely to peak, across species. We stress the importance of controlling for sampling time and reporting these results as standard practice in studies of fecal glucocorticoid metabolites.

Factors affecting captive female giraffe stress response: Male presence, small enclosure, and low temperature.

To improve animal welfare based on suitable social housing conditions, it is important to understand the factors that trigger high-stress responses. Wild giraffes live in a fission-fusion society and males and females are rarely in the same herd for a long period. The captive condition of belonging to a herd with the same individuals for months or years is uncommon in nature. To understand the effect of male presence on female stress levels, fecal glucocorticoid metabolite (fGCM) levels and social interactions in two captive female giraffes were investigated. Additionally, the effect of enclosure size and temperature on fGCM level and social interactions were examined. The results showed no significant difference in the fGCM levels of females based on male presence. The frequency of agonistic behavior by the dominant female toward the subordinate female was significantly increased when a male was present. The subordinate female was significantly less likely to approach the dominant female and showed decreased affiliative and agonistic interactions toward the dominant female when a male was present. The frequencies of agonistic interactions between females were higher in the small enclosure regardless of male presence. Low temperature triggered higher fGCM levels and increased agonistic interaction in an aged female. The findings of this study suggest that these multiple factors should be considered individually to promote the welfare of captive giraffes.

Linking glucocorticoid variations to monthly and daily behavior in a wild endangered neotropical primate.

Identifying the factors swaying physiological stress levels in wild animals can help depict how they cope with environmental and social stressors, shedding light on their feeding ecology, behavioral plasticity, and adaptability. Here, we used noninvasive methods to explore the link between glucocorticoid levels and behavior in an endangered neotropical primate facing habitat fragmentation pressure, the black lion tamarin (Leontopithecus chrysopygus). We investigated monthly and day-to-day glucocorticoid variations independently to attempt to disentangle the complex nature of the adrenocortical activity. Between May 2019 to March 2020, we followed two groups of black lion tamarins in two different areas, a continuous forest and a small fragment, and gathered behavioral data (over 95 days in total; 8.6 ± 3.9 days/month) and fecal samples (Nsamples = 468; 4.93 ± 3.5 samples/day) simultaneously. Preliminary analyses enabled us to identify circadian variations linked to the biological rhythm, which were taken into account in subsequent models. Monthly analyses revealed that black lion tamarin fecal glucocorticoid metabolite levels vary according to changes in activity budget associated with the fruit consumption, movement, and resting time of the groups. At a day-to-day level, while intergroup encounters led to increases in fecal glucocorticoid metabolite concentrations, we found that changes in food intake or activity level did not trigger physiological stress responses. These findings suggest that diet and ranging patterns, driven by food availability and distribution, influence physiological stress at a seasonal scale, while acute stressors such as interspecific competition trigger short-term stress responses. Exploring fecal glucocorticoid metabolite variations over different timescales can help uncover the predictive and reactive facets of physiological stress in wild species. Moreover, having a comprehensive understanding of the physiological state of species is a valuable conservation tool for evaluating how they cope in changing environments.

Temperament traits and glucocorticoid metabolites in tropical screech owl (Megascops choliba)

Animals constantly respond to stimuli from their surroundings, showing individual behavioral and endocrine differences upon perceived challenging and/or threatening stimuli. The temperament of 13 captive tropical screech owls (Megascops choliba) was defined by performing three challenge tests (novel space, taxidermist predator and trapping) to identify inter-individual differences and their possible relationship with the production of glucocorticoid metabolites (GCM). Feces samples of each bird were taken pre-and-post predator challenge to quantify GCM concentration by means of enzymatic immunoassay (EIA). The intensity of 13 adjectives selected to describe the owls' temperament was determined by three judges during behavioral testing. Only 3 adjectives (passive, vulnerable, and attentive) that showed strong inter-test and intra-individual correlation coefficients were considered. These adjectives were later grouped in a single dimension named “shyness”, enabling establishment of individual scores. The temperament of the owls showed correlation to post-predator challenge GCM levels (ρ = 0.79; p < 0.001). However, no significant differences were found in GCM levels before and after predator challenge. Our results both confirm that nocturnal behavior raptorial birds show positive relation between shy temper and adrenal response, and offer the non-invasive herein implemented methods for establishment of new hypotheses that will assess welfare of species kept under human care.

Between hunter and climate: the effects of hunting and environmental change on fecal glucocorticoid metabolite levels in two sympatric ungulate species in the Ruaha-Rungwa ecosystem, Tanzania.

Understanding the drivers of animal population decline is a key focus of conservation biologists. Anthropogenic activities such as hunting have long been established as potentially detrimental to a population's persistence. However, environmental perturbations such as increased temperature variability, exacerbated by climate change, can also have important effects on animal populations. Animals can respond to these challenges by adjusting both their behavior and physiology. We measured fecal glucocorticoid metabolites (FGMs) of common impala (Aepyceros melampus) and greater kudu (Tragelaphus strepsiceros), both currently in stable populations, to examine effects of hunting, forage availability, daily variability in temperature and group size on their physiological stress response. The study was conducted across two adjacent protected areas, (i) one non-hunted area (Ruaha National Park; RNP) and (ii) one area used for trophy hunting (Rungwa Game Reserve; RGR). Both impala and kudu had significantly higher FGM levels in the area that allows hunting, while FGM levels decreased with increasing forage availability and increasing daily temperature. Moreover, impala (but not kudu) had lower FGM levels with larger group sizes. Our results indicate that the management regime can significantly alter the physiological state of wild ungulate populations. We also highlight the importance of considering the combined effects of anthropogenic, environmental and social contexts when studying the stress response of wild populations. Our results emphasize the value of protected areas and continued monitoring of hunting quota in order to maintain ungulate populations that are less vulnerable to population declines.

Stress-associated metabolites vary with both season and habitat across populations of a climate sentinel species

ABSTRACT Relating physiological stress to habitat quality could refine conservation efforts. Habitat quality, which is often inferred from patch occupancy or demographic rates, might be measured in a more timely and nuanced way using metrics of physiological stress. To understand whether stress-associated hormones vary with metrics of habitat quality, we measured fecal glucocorticoid metabolite (FGM) levels in the American pika (Ochotona princeps), a small mammal with well-defined habitat (talus), which can vary in quality depending on the presence of subsurface ice features. In spring and fall 2018, we collected feces noninvasively from pika territories in taluses “with” or “without” subsurface ice to capture seasonal variation in FGM between habitat types. We used linear mixed effects models to explore the interactions among season, habitat metrics (including subsurface ice status), and subsurface temperature as predictors of FGM. We found support for interacting effects on FGM levels, which covaried with season, elevation, putative ice presence, graminoid to forb ratio, graminoid cover, and measures of acute subsurface heat exposure. However, only one subsurface temperature metric differed according to putative presence of subsurface ice. Our results contribute to the growing evidence that FGMs might be developed as a tool to assess habitat quality.

Fecal glucocorticoid analysis as a health monitoring tool for endangered African penguins (Spheniscus demersus)

African penguins (Spheniscus demersus) are an endangered species, with approximately 70,000 mature adults remaining in the wild. Population loss is linked to a combination of environmental and anthropogenic stressors. The aim of the study was to validate a commercially available enzyme immunoassay (EIA) to assess adrenal activity and measure the response to stressors in the feces of African penguins. Fecal samples (n = 609) were collected from 12 African penguins housed at Mystic Aquarium throughout their natural lifecycle, including breeding and molt, where measurable changes in fecal glucocorticoid metabolite (FGM) levels are predicted to occur. Fecal samples collected post-veterinary exam were used for biological validation. Longitudinal analysis shows a significant difference (p = <0.0001) between the average FGM levels during baseline and breeding season, 33.97 ± 1.30 ng/g and 50.21 ± 3.18 ng/g, respectively. Females displayed significantly higher FGM levels than males during both baseline (p = 0.0386; females = 38.80 ± 2.19 ng/g; males = 29.34 ± 1.37 ng/g) and breeding periods (p = 0.0175; females = 57.53 ± 4.84 ng/g; males = 42.69 ± 3.95 ng/g). Average FGM levels decreased significantly over the three-week molting period, from 85.40 ± 20.35 ng/g at week one to 20.23 ± 5.30 ng/g at week three. A seasonal difference in FGM levels was observed in both male and female fecal samples, with Fall having the highest average FGM levels, 54.38 ± 3.64 ng/g, and Summer the lowest, 30.87 ± 2.21 ng/g. General linear mixed model analysis determined that lifecycle (females) and visitor presence (males) were the two factors which best explained the variation in FGM levels observed, however neither factor was found to be significant. These results show FGM analysis can detect physiologically meaningful changes in endocrine activity in African penguins and can be used to monitor health for penguins in aquaria and in the wild, thus contributing to conservation efforts for the survival of the species.

Fecal glucocorticoid metabolite levels in captive Indian leopards (Panthera pardus fusca) housed under three different enrichment regimes.

Environmental enrichment improves the health and wellbeing of zoo animals. To test this hypothesis, we used Indian leopards (Panthera pardus fusca), one of the popular zoo animals, as a model organism to understand effects of active and passive enrichment elements on stress hormone levels of captive individuals. We included three enrichment categories, category 'A' (having both active: cage size of 1204 m3 with raised platforms and earthen flooring, and passive: controlled temperature, playback of forest sounds and sound proof glass to filter visitors' noise, enrichment elements), category 'B' (active enrichment type I, cage size of 264 m3 with air coolers), and category C (active enrichment type II, cage size of 517 m3 without air coolers) for leopards (n = 14) housed in two Indian zoos. We used a group-specific enzyme immunoassay to measure fecal glucocorticoid metabolites (fGCM) in captive leopards. For comparison, we analysed samples from free-ranging leopards, as well. fGCM levels (Mean±SEM) were 10.45±2.01 and 0.95±0.003 μg/g dry feces in captive and free-ranging leopards, respectively. Our results revealed that fGCM levels of leopards in categories B and C were significantly (P<0.05) different from each other, thus, indicating cage size (an active enrichment element) as an important factor in influencing the physiology of the sampled animals. Overall, the findings of the study will contribute towards informed policies for management of captive Indian leopards.

How individual, social, and ecological conditions influence dispersal decisions in malevervet monkeys.

Dispersal between social groups reduces the risk of inbreeding and can improve individuals'reproductive opportunities. However, this movement has costs, such as increased risk of predation and starvation, loss of allies and kin support, and increased aggression associated with entering the new group. Dispersal strategies, such as the timing of movement and decisions on whether to transfer alone or in parallel with a peer, involve different costs and benefits. We used demographic, behavioral, hormonal, and ecological data to examine the causes and consequences of 36 dispersal events from 29 male vervet monkeys (Chlorocebus pygerythrus) at Lake Nabugabo, Uganda. Adult males'secondary dispersal coincided with the conception season in females, and males improved their potential access to females by moving to groups with higher female-to-male sex ratios and/or by increasing their dominance rank. Males that dispersed with a peer had lower fecal glucocorticoid and androgen metabolite levels than lone dispersers.Subadult males were not more likely to engage in parallel dispersals compared to adult males. Dispersal was also used as a mechanism to avoid inbreeding, but changes in hormone levels did not seem to be a trigger of dispersal in our population. Our findings illustrate the complex individual strategies used during dispersal, how many factors can influence movement decisions, as well as the value of dominance and hormone analyses for understanding these strategies.

Patterns of faecal glucocorticoid metabolite levels in captive roan antelope (Hippotragus equinus) in relation to reproductive status and season

Populations of roan antelope (Hippotragus equinus) in southern Africa have experienced a drastic decline over the past few decades and this situation has led to the development of intensive breeding programmes to support conservation efforts. However, little is known about related welfare aspects, including stress-related physiological biomarkers. The present study set out to establish a non-invasive method to monitor faecal glucocorticoid metabolite (fGCM) concentrations as a measure of stress and determine fGCM concentrations in relation to male reproductive activity and female reproductive status in the roan antelope. An adrenocorticotrophic hormone challenge was performed using two adult roan antelope (one male and one female) at Lapalala Wilderness Nature Reserve, South Africa, to determine the suitability of five enzyme immunoassays (EIA) for monitoring adrenocortical function in roan antelope. An 11-oxoaetiocholanolone I EIA detecting 11,17 dioxoandrostanes performed best showing 17–20 folds increases in fGCM concentrations after 12 h-17 h post-injection. The identified EIA was then used to monitor fGCM concentrations during active and non-active reproductive periods in males (n = 3), and during periods of cyclicity, gestation, and postpartum in females (n = 10). Males showed an overall 80% increase in fGCM concentrations when reproductively active and females showed a progressively significant increase in fGCM levels throughout pregnancy, with overall fGCM concentrations being 1.5 to 2.6-fold higher than the respective fGCM concentrations during periods of postpartum and cyclicity, respectively. Furthermore, fGCM concentrations remained above baseline for up to 21 days post-partum. A correlation between ecological parameters (rainfall and temperature) and fGCM concentrations revealed elevated fGCM concentrations during the dry season for males, but not females. The non-invasive method validated in this study provides a valuable tool to quantify stress-related biomarkers in roan antelope, and findings can be used to support management decisions in conservation breeding facilities.

Seasonal Variation in Fecal Glucocorticoid Levels and Their Relationship to Reproductive Success in Captive Populations of an Endangered Parrot

Many species are threatened with extinction, and captive breeding programs are becoming more common to avoid this outcome. These programs serve to prevent extinction and produce individuals for eventual reintroduction to natural populations in historical habitat. Captive animals experience different energetic demands than those in the wild, however, and as a result may have different levels of glucocorticoid hormones. Glucocorticoids help with responses to energetically expensive and potentially stressful situations. Elevated glucocorticoid levels can also potentially alter reproduction and other key behaviors, thus complicating successful captive breeding. The Puerto Rican parrot (Amazona vittata) is a critically endangered parrot that currently exists in only two wild and two captive populations. Its recovery program provides a good platform to better understand how glucocorticoid levels may relate to reproductive success under captive conditions. We validated a corticosterone assay in this species and used non-invasive techniques of measuring fecal glucocorticoid metabolites of males and females from two captive populations (Rio Abajo and El Yunque) of Puerto Rican parrots over two consecutive breeding seasons, 2017 and 2018, and the pre-breeding season of 2018, which occurred just after Hurricane Maria struck Puerto Rico. Our results show that levels of fecal glucocorticoid metabolites of males measured during the breeding season of 2018 negatively correlated to the number of total eggs and fertile eggs laid by pairs. In contrast, there was a positive relationship of female fecal glucocorticoid metabolite levels during the pre-breeding season of 2018 with total eggs laid. In males from the Rio Abajo population, we found seasonal differences in fecal glucocorticoid metabolite levels, with higher levels during the pre-breeding season of 2018 compared to both 2017 and 2018 breeding seasons. There was no difference in the mean value of male fecal glucocorticoid metabolites between the 2017 breeding season and 2018 breeding season which started four months after Hurricane Maria struck Puerto Rico. We did find sex differences during the pre-breeding season of 2018 in birds from the Rio Abajo population. Adjustments in the care routine of both populations that could reduce circulating baseline glucocorticoids and avoid frequent, sudden elevations of glucocorticoids should be considered. These results provide a baseline for future comparison with reintroduced populations of this endangered species and other species with captive breeding programs.

How do humans impact yellow-bellied marmots? An integrative analysis

While many studies document specific human impacts on the behaviour and physiological responses of wildlife to humans, most have focused on these responses independently and over relatively short periods of time. To address this, we studied a suite of responses in yellow-bellied marmots (Marmota flaviventer) in two distinct years, 9 years apart. We first quantified the rate that vehicles, pedestrians, and bicycles passed marmot colonies, focusing on two years (2009 and 2018) to determine how, if any of these relationships changed over time. We then asked whether these disturbances were associated with marmot physiological responses including neutrophil-lymphocyte ratios (NLR), and faecal glucocorticoid metabolites levels (FGM), as well as behavioural responses including flight initiation distance (FID) and the time marmots allocated to foraging, and finally a key fitness correlate—the rate of mass gain. We found that the number of vehicles and pedestrians passing within 300 m of a marmot colony stayed relatively constant between years, while there was variation in bicycles passing by marmot colonies. Despite similar length in growing seasons, marmots at colonies that had higher disturbance gained mass more rapidly in 2018 than in 2009. By examining a suite of physiological, behavioural, and key fitness correlates, and how they changed, our findings are consistent with the hypothesis that marmots became more tolerant of human disturbances over time. This provides promise for this population in dealing with inevitable increases in eco- and nature-based tourism.

Effects of early life adversity on maternal effort and glucocorticoids in wild olive baboons

Adverse experiences during early life exert important effects on development, health, reproduction, and social bonds, with consequences often persisting across generations. A mother’s early life experiences can impact her offspring’s development through a number of pathways, such as maternal care, physiological signaling through glucocorticoids, or even intergenerational effects like epigenetic inheritance. Early life adversity in female yellow baboons (Papio cynocephalus) predicts elevated glucocorticoids, reduced sociality, shortened lifespan, and higher offspring mortality. If baboon mothers with more early life adversity, experience poorer condition and struggle to provide for their offspring, this could contribute to the persisting transgenerational effects of adversity. Here, we examined the effects of mothers’ early life adversity on their maternal effort, physiology, and offspring survivability in a population of olive baboons, Papio anubis. Mothers who experienced more adversity in their own early development exerted greater maternal effort (i.e., spent more time nursing and carrying) and had higher levels of glucocorticoid metabolites than mothers with less early life adversity. Offspring of mothers with more early life adversity had reduced survivability compared to offspring of mothers with less early life adversity. There was no evidence that high maternal social rank buffered the effects of early life adversity. Our data suggest early life experiences can have lasting consequences on maternal effort and physiology, which may function as proximate mechanisms for intergenerational effects of maternal experience. Animals exposed to early life adversity experience both immediate and lasting consequences. If early life adversity exerts developmental constraints that affect a mother’s ability to provide for her offspring, this could explain the transgenerational effects of early life adversity. In our study of wild olive baboons, we examined how a mother’s own early life adversity predicts her maternal effort (i.e., nursing and carrying time), maternal fecal glucocorticoid levels, and offspring outcomes. We found that female baboons who experienced more early life adversity had higher glucocorticoid levels during pregnancy and lactation, exerted more maternal effort, and produced offspring with higher mortality risk than females with less early life adversity. Our results suggest that female baboons with more early life adversity experience developmental constraints and struggle to invest in offspring, which likely contributes to persisting effects of early life adversity across generations.

Fecal glucocorticoids and gastrointestinal parasite infections in wild western lowland gorillas (Gorilla gorilla gorilla) involved in ecotourism

Wildlife ecotourism can offer a source of revenue which benefits local development and conservation simultaneously. However, habituation of wildlife for ecotourism can cause long-term elevation of glucocorticoid hormones, which may suppress immune function and increase an animal’s vulnerability to disease. We have previously shown that western lowland gorillas (Gorilla gorilla gorilla) undergoing habituation in Dzanga-Sangha Protected Areas, Central African Republic, have higher fecal glucocorticoid metabolite (FGCM) levels than both habituated and unhabituated gorillas. Here, we tested the relationship between FGCM levels and strongylid infections in the same gorillas. If high FGCM levels suppress the immune system, we predicted that FGCM levels will be positively associated with strongylid egg counts and that gorillas undergoing habituation will have the highest strongylid egg counts, relative to both habituated and unhabituated gorillas. We collected fecal samples over 12 months in two habituated gorilla groups, one group undergoing habituation and completely unhabituated gorillas. We established FGCM levels and fecal egg counts of Necator/Oesophagostomum spp. and Mammomonogamus sp. Controlling for seasonal variation and age-sex category in strongylid infections we found no significant relationship between FGCMs and Nectator/Oesophagostomum spp. or Mammomonogamus sp. egg counts in a within group comparison in either a habituated group or a group undergoing habituation. However, across groups, egg counts of Nectator/Oesophagostomum spp. were lowest in unhabituated animals and highest in the group undergoing habituation, matching the differences in FGCM levels among these gorilla groups. Our findings partially support the hypothesis that elevated glucocorticoids reduce a host’s ability to control the extent of parasitic infections, and show the importance of non-invasive monitoring of endocrine function and parasite infection in individuals exposed to human pressure including habituation process and ecotourism.