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Published in final edited form as: Gen Comp Endocrinol. 2020 Dec 7;302:113692. doi: 10.1016/j.ygcen.2020.113692

Hair cortisol in captive corral-housed baboons

Corrine K Lutz a, Jerrold S Meyer b, Melinda A Novak b
PMCID: PMC8098999  NIHMSID: NIHMS1677882  PMID: 33301757

Abstract

Hair cortisol concentrations (HCCs) are measures of long-term hypothalamic-pituitary-adrenocortical (HPA) activity and can be used as indicators of chronic stress. However, intrinsic factors such as an animal’s age and sex can also have an impact on resulting HCCs. Although baboons are commonly studied in captivity, little is known about baseline HCC in this population. Here we measured HCC in two same-sex groups of captive olive (Papio hamadryas anubis) baboons and olive/yellow baboon (Papio hamadryas cynocephalus) crosses housed in large outdoor corrals, and we assessed the impact of age and sex on HCC as major variables of interest. Hair was gently shaved from the back of the neck when the animals were sedated for routine physicals. Subjects were divided into three age categories: juvenile (2–4 years), adult (9–12 years), and senior (13–19 years). The “senior” category contained only males. Results confirm an effect of sex and age on HCCs. Females had higher levels of hair cortisol than males, and juveniles had higher levels than adults. There was also a significant sex x age interaction. There were no sex differences in HCCs in juveniles, but there was a greater decline in HCCs in adult males than in adult females. Within males, there was a significant difference in levels of hair cortisol across the three age categories. Juveniles had higher levels than did adults and seniors, but adults and seniors were not significantly different from one another. These results provide baseline measures of hair cortisol in captive baboons and demonstrate effects of sex and age on HCCs.

Keywords: cortisol, hair, baboon, sex, age

1. Introduction

The hypothalamic-pituitary-adrenocortical (HPA) axis is a central component of the body’s physiological response to stress (Meyer and Hamel, 2014; Novak et al., 2013; O’Connor et al., 2000). One outcome of HPA axis activation is an increased production of cortisol (O’Connor et al., 2000). Cortisol is a glucocorticoid hormone that mobilizes energy stores, aids delivery of blood to the muscles and brain, and increases the body’s response to infection in response to stress (Heimburge et al., 2019; O’Connor et al., 2000; Russell and Lightman, 2019). Because cortisol production can be associated with stressful situations, it is often used as a physiological measure of stress in studies of social, biological, or environmental conditions (Carnegie et al., 2011; Crockett et al., 1993; Friant et al., 2016; Linden et al., 2019; Pearson et al., 2015; Pirovino et al., 2011; Price et al., 2019; Rangel-Negrin et al., 2009). Chronic exposure to stress and elevated cortisol concentrations can become maladaptive and result in a number of disease states (Russell and Lightman, 2019). Therefore, cortisol concentrations can also be used as a biomarker for an animal’s health and wellbeing (Fardi et al., 2018; Heimburge et al., 2019; Jacobson et al., 2017; Novak et al., 2013; Schrock et al., 2019).

For measurement, cortisol can be extracted from a number of body fluids and excreta, including blood, saliva, urine, and feces (Anestis et al., 2006; Lutz et al., 2000; Novak et al., 2013); however, the timing of the sample collection with respect to the stressor differs across samples. For example, cortisol measurements obtained from blood and saliva are considered “point” samples, which can be affected within minutes by experiences immediately prior to the sampling, such as food intake, restraint, or a planned stressor, as well as by circadian rhythm (Fourie and Bernstein, 2011; Kirschbaum and Hellhammer, 2000; Meyer and Novak, 2012; Novak et al., 2013). Cortisol measurements obtained from urine or feces reflect longer-term HPA activity ranging from hours to days, but the levels are still sensitive to circadian rhythm as well as recent environmental disturbances (Fourie and Bernstein, 2011; Meyer and Novak, 2012; Novak et al., 2013; Rimbach et al., 2013). Whether the time course of these samples is in minutes, hours, or even a few days, repeated measures need to be collected when establishing basal hormone levels or when studying long-term effects of a stimulus on HPA axis activity (Davenport et al., 2006; Fourie and Bernstein, 2011). In contrast, hair is a substance that can be utilized to measure long-term cortisol levels and the effects of chronic stress on cortisol output (Davenport et al., 2006; Fourie and Bernstein, 2011; Heimburge et al., 2019; Novak et al., 2013). The period of cortisol accumulation depends on hair growth rate. In humans and rhesus macaques, the average growth rate (scalp and body hair respectively) is approximately 1 cm/month (Lebeau et al., 2011; Dolnick, 1969). Growth rates in other species of nonhuman primates estimated by Fourie and colleagues (2016) varied from 0.7 to 3.5 cm/month; however, the sample sizes were very small, ranging from 1 to 3, and therefore these findings need to be replicated. In the same study, full hair regrowth was estimated to require approximately 3 to 7 months, depending on the species (Fourie et al., 2016).

Although hair can be utilized to measure chronic levels of cortisol, hair cortisol levels can vary with an animal’s sex or age. In studies of rhesus macaques (Macaca mulatta), vervets (Chlorocebus aethiops sabaeus), and baboons (Papio spp.), females were reported to have higher levels of hair cortisol than were males, but this was dependent on facility (Lutz et al., 2016), age (Laudenslager et al., 2012), and species (Fourie et al., 2016). Studies have also reported no sex difference in hair cortisol in capuchins (Cebus [Sapajus] apella), marmosets (Callithrix jacchus), and lemurs (Lemur catta; Fardi et al., 2018; Phillips et al., 2018; Schrock et al., 2019) as well as higher levels of hair cortisol concentrations in male rhesus macaques (Linden et al., 2019) and chimpanzees (Pan troglodytes; Jacobson et al., 2017; Yamanashi et al., 2016). As with sex, age can also have an impact on hair cortisol levels. In rhesus macaques, newborn infants had significantly higher levels of hair cortisol than did their postpartum mothers (Grant et al., 2017; Kapoor et al., 2014). Newborn hair cortisol values were associated with the rise in maternal cortisol during pregnancy, reflecting an accumulation of cortisol in fetal hair during gestation (Grant et al., 2017). Cortisol levels gradually decrease from birth through the early juvenile stages, after which the levels of cortisol stabilize with adults typically having lower hair cortisol levels than younger individuals (Fourie and Bernstein, 2011; Fourie et al., 2016; Grant et al., 2017; Laudenslager et al., 2012; Linden et al., 2019). Such changes in cortisol concentrations with age may be due to life history milestones, or more generally, ontogenetic patterns of adrenocortical function (Fourie et al., 2016). Hair cortisol levels were shown to remain consistent in studies focusing on juveniles and adults (Novak et al., 2014; Schrock et al., 2019; Yamanashi et al., 2013), while cortisol levels increased from adulthood to old age (Erwin et al., 2004; Fourie et al., 2015; Sapolsky and Altmann, 1991).

The baboon (Papio hamadryas sp.) is an important model in biomedical research due to the number of physical, genetic, and physiological traits that it shares with humans. Because of these similarities to humans, baboons are utilized in a wide range of biomedical research areas including nutrition, reproduction, genetics, cardiac disease, drug abuse, xenotransplantation, infectious disease, and epilepsy (Bauer, 2015; Gurung et al., 2018; Ozwara et al., 2003; Szabo et al., 2009; VandeBerg et al. 2009; Warfel et al., 2014). The baboon is also a key primate model for the genetic study of complex diseases, including cardiovascular disease, obesity, and hypertension (see Cox et al. 2013 for a review). Although hair cortisol has been routinely collected from macaque monkeys (Davenport et al., 2006; Dettmer et al., 2012; Feng et al., 2011; Grant et al., 2017; Hamel et al., 2017; Linden et al., 2019; Lutz et al., 2016; 2019; Novak et al., 2014), few investigators have assessed hair cortisol levels in baboons (Fourie et al., 2015, 2016; Fourie and Bernstein, 2011), and these studies were conducted either on male baboons in the wild (Fourie et al., 2015) or on small samples of both wild and captive baboons (Fourie and Bernstein, 2011; Fourie et al., 2016). Therefore, the purpose of this study is to add to the current data by assessing levels of hair cortisol in a large colony of captive baboons consisting of both males and females. This will allow for further investigation of hair cortisol levels of baboons in captivity as well as the impact of sex and age on those values.

2. Materials and Methods

2.1. Animals and Housing

The subjects were 209 baboons (142 males, 67 females) consisting mainly of the subspecies olive baboon (Papio hamadryas anubis) and olive/yellow baboon (Papio hamadryas cynocephalus) crosses. They ranged in age from 2.9 to 18.6 years (M = 8.1 years). Because ages were not evenly distributed, they were divided into categories: juvenile (2–4 years), adult (9–12 years), and senior (13–19 years). The “senior” group contained only males (Table 1). The animals were group-housed outdoors in two 6-acre corrals. Males and females were housed separately to prevent breeding. The corrals contained culverts and platforms for shelter and climbing opportunities. Attached to each of the corrals was a smaller holding pen that could be covered and heated in colder weather. The animals were fed Purina® 5LEO monkey chow twice daily, a grain mix twice a week, and fruit 3–4 times per week. The facility is accredited by AAALAC International and the animals were maintained in accordance with the Guide for the Care and Use of Laboratory Animals (Institute for Laboratory Animal Research, 2011). The research was approved by the Institutional Animal Care and Use Committee and complied with the laws and regulations of the United States Animal Welfare Act.

Table 1.

Number of subjects in each age/sex category

Juvenile Adult Senior Total
Male 55 34 53 142
Female 44 23 0 67
Total 99 57 53 209
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2.2. Sampling and Assay Procedures

Hair sampling took place while the baboons were sedated for a routine physical exam which took place September 2014. During the physical, hair was gently shaved from the back of the neck, wrapped in aluminum foil packets and stored in a −80°C freezer until shipment to the University of Massachusetts-Amherst for processing. Hair was assayed for cortisol according to the procedures described in Davenport et al. [2006]. In summary, the samples were first washed with isopropanol to remove any external contaminants and then dried. The dried hair samples were then ground into a powder with a Retsch ball mill, and methanol was added to each sample to extract the steroids. After the extraction, the samples were centrifuged and dried. The dried extracts were reconstituted with assay diluent, spin-filtered to remove any residual particulate matter, and analyzed with a commercially available EIA kit designed for assessing cortisol in saliva (Salimetrics; Carlsbad, CA). The mean intra-assay coefficient of variance (CV) for the cortisol assay was 2.5%, and the inter-assay CV was 5.8%.

2.3. Data Analyses

Four cortisol values obtained from two juvenile females, one juvenile male, and one senior male were outliers (greater than three SD above the mean). These values were winsorized to three SD over the mean. The winsorized values were used in subsequent analyses. An Analysis of Variance (ANOVA) was first conducted to identify differences in cortisol level within the sex and two age (juvenile, adult) categories. A second ANOVA was conducted to identify age differences (juvenile, adult, senior) in the males. Because there were no females in the “senior” age category, the category “senior” was dropped from the first analysis and the category “female” was dropped from the second analysis.

3. Results

The overall cortisol levels for all of the subjects averaged 60.48 pg/mg (range 21.4–256.3 pg/mg; Table 2). There were significant sex and age differences in the adult and juvenile cortisol levels. Results from the first ANOVA showed that females had higher levels of hair cortisol than males (F(1) = 7.582, p < 0.01) and juveniles had higher hair cortisol levels than adults (F(1) = 24.584, p < 0.001). There was also a significant sex x age interaction (F(1) = 5.800, p < 0.05). Adult females had higher hair cortisol levels than adult males, but this sex difference was not evident in juveniles (Figure 1). Results from the second ANOVA showed a significant age effect in males (F(2) = 25.235, p < 0.001). A post-hoc Tukey test demonstrated that juvenile males had higher cortisol levels than either adult (p < 0.001) or senior (p < 0.001) males. There was no significant difference between adult and senior males.

Table 2.

Cortisol levels in pg/mg for each age/sex category (Mean ± SE)

Juvenile Adult Senior
Male 72.74 ± 3.54 40.25 ± 4.51 46.03 ± 4.46
Female 74.33 ± 3.96 62.99 ± 5.48 N/A
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Figure 1.

Figure 1.

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Sex x Age interaction in hair cortisol levels

4. Discussion

The results from this study provide baseline HCCs in outdoor corral-housed baboons and demonstrate the presence of sex- and age-related differences in this measure. Overall, females had higher cortisol levels than did males, but this sex difference was most pronounced in the adult population. Indeed, male baboons showed a greater decline in HCC with age than females. Previous studies have reported a female-biased sex difference in hair cortisol, but this effect has not been consistently observed (Fourie et al., 2016, Laudenslager et al., 2012; Lutz et al., 2016). Although one possible cause of higher levels of hair cortisol in females is pregnancy (Lutz et al., 2019), the adult females in the present study were housed in a same-sex group and none were pregnant at the time of sampling. Other possible causes may include greater reactivity in females (Crockett et al., 1993), sex-specific life history differences (Vandeleest et al., 2019), or simply a genetic or physiological difference between the sexes (Fourie et al., 2016). As hair cortisol is thought to reflect accumulation of hormone from the “free” fraction in the bloodstream (Meyer and Novak, 2012), it is also possible that there is a sex difference in corticosteroid binding globulin (CBG) in baboons. However, this explanation remains speculative since to our knowledge there is no published information on sex differences in baboon CBG. The relationship between sex and hair cortisol levels requires further investigation.

Age differences were also noted in the present study; juvenile baboons had higher hair cortisol levels than did the adults. This result reflects that of many (Fourie and Bernstein, 2011; Fourie et al., 2016; Grant et al., 2017; Laudenslager et al., 2012; Linden et al., 2019), but not all (Schrock et al., 2019) studies in which levels of hair cortisol were observed to decline with age during early development in nonhuman primates. In rhesus and pigtailed macaques, infants had significantly higher levels of hair cortisol than did their mothers, which may reflect fetal exposure as the hair was first growing (Grant et al., 2017; Kapoor et al., 2014). The levels of hair cortisol then declined as the infant aged, reaching adult levels by approximately 6 months of age in the pigtailed macaques (Grant et al., 2017). Other studies involving rhesus macaques, vervet monkeys, and several other primate species reported declines in hair cortisol concentrations occurring later in development, at approximately 1.5 to 2 years of age (Dettmer et al., 2014; Fourie and Bernstein, 2011; Laudenslager et al., 2012). The youngest age group in the present study was older than two years (2–4 years), but the animals still had significantly higher levels of hair cortisol in comparison to the adults. The high levels of hair cortisol in this age category could possibly be due to species differences or differences in colony management (Dettmer et al., 2014). Researchers have also reported an increase in hair cortisol from adulthood into old age (Erwin et al., 2004; Fourie et al., 2015; Sapolsky and Altmann, 1991). In the present study, there was a slight increase in HCCs from the adult to senior male age groups, but it was not statistically significant. This result may be due in part to the limited age range of the older subjects. Baboons can live into their twenties in the wild (Strum, 1991) and well over 25 years in captivity (Dick et al., 2014), but the upper age limit in the present study was 19 years. Although these baboons were aged (older than adult), they were not what would be considered geriatric (Dick et al., 2014).

The hair cortisol values from the current population averaged approximately 65 pg/mg, which is within the range of values from other Old World primates (rhesus and pigtailed macaques) previously reported by our laboratory using the same hair processing and analytical methods (Davenport et al., 2006; Dettmer et al., 2012; 2014; Grant et al., 2017; Hamel et al., 2017; Lutz et al., 2016; 2019; Novak et al., 2014). However, these levels are notably different from previous findings on baboon hair cortisol levels which were reported to be 10- to over 500-times greater (Fourie and Bernstein, 2011; Fourie et al., 2015; 2016). Although it is difficult to account for such large differences, there are methodological factors that can impact HCCs, several of which are discussed below. First, the body location from which the hair is sampled can affect the hair cortisol values (Yamanashi et al., 2013). For example, in yellow baboons, hair collected from the thigh had higher cortisol levels than hair collected from the base of the tail, but there were no differences in comparison to the shoulder (Fourie et al., 2016). In the present study, all of the hair samples were collected from the base of the neck. Although this location varies slightly from previous baboon studies that collected hair from the inter-scapular region or back (Fourie et al., 2015; 2016), this difference is unlikely to account for large discrepancies in hair cortisol levels. A second factor is method of incubation. The present study conducted the extraction at room temperature, while previous studies utilized a hot water bath that was reported to increase cortisol extraction by as much as 1.5 times (Fourie and Bernstein, 2011; Fourie et al., 2016). The third factor is sample preparation before extraction. Our first rhesus monkey study (Davenport et al., 2006) reported over a 3-fold increase in measured cortisol in powdered hair compared to hair minced with a scissors. The present study utilized a ball mill to grind the hair while Fourie and Bernstein (2011) and Fourie et al., (2015, 2016) utilized hair that was minced with scissors. However, this procedural difference would predict hair cortisol values occurring in the opposite direction of what is reported here. Lastly, differences in apparent cortisol levels produced by different EIA kits likely contributed to the discrepant HCCs between previous studies and the current one. The data in the present paper were obtained using the Salimetrics EIA kit, whereas the data reported in the previous papers by Fourie and coworkers used either a kit from ALPCO (Fourie and Bernstein, 2011; Fourie et al., 2016) or an assay based on a non-commercial antibody (Fourie et al., 2015). A comparison of average reported human hair cortisol levels from the ALPCO versus the Salimetrics kit found approximately 1.5-fold higher levels from the ALPCO kit (Albar et al., 2013). It remains difficult to account for the large difference in baboon hair cortisol observed here compared to previous reports; however, the factors described above along with possible species and subspecies differences in the respective subject populations alert readers to the importance of considering multiple sources of variation when comparing HCCs between studies.

5. Conclusions

Hair cortisol is an efficient measure of chronic stress in nonhuman primates; however, many of the studies previously designed to ascertain the factors that influence this variable were performed in macaque monkeys (Davenport et al., 2006; Dettmer et al., 2012; Feng et al., 2011; Grant et al., 2017; Hamel et al., 2017; Linden et al., 2019; Lutz et al., 2016; 2019; Novak et al., 2014). The present results extend previously reported data regarding age- and sex-related differences in hair cortisol in captive baboons. Comparing these results to the findings obtained from other nonhuman primate species as well as humans, can help researchers develop a better understanding of species similarities and differences in HPA axis activity and has the potential to open up avenues of both improved welfare assessment and research possibilities.

Highlights.

  • The overall hair cortisol concentrations (HCC) in captive baboons averaged 60.48 pg/mg (range 21.4–256.3 pg/mg)

  • Female baboons had higher levels of HCC than did male baboons.

  • Juveniles had higher HCC levels than did adults.

  • Males showed a greater decline in HCC with age than did females.

Acknowledgements

The authors would like to thank Brittany Peterson for her assistance with hair collection, Kendra Rosenberg for performing the cortisol assays, and Dr. Lisa Chiodo (University of Massachusetts) for statistical consultation. This study was supported by National Institutes of Health grant number 2P51OD011133 to Texas Biomedical Research Institute and grant number R24 OD011180 to Melinda Novak at the University of Massachusetts.

Footnotes

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