Reproductive maturation in a sample of captive male baboons

Though baboons have been considered an appropriate non-human primate model for studying human reproductive and endocrine development. the overall similarity of reproductive maturation between the two species is unclear. This paper examines the role of testicular and adrenal hormones for pubertal changes in a cross-sectional sample of 21 captive male savanna baboons. Morphometric and hormonal indices demonstrate changes in size and gonadal function, but not adrenal function, during pubertal maturation among baboons. Results also indicate that gonadal, but not adrenal, androgens are related to morphometric variables. We conclude that savanna baboons do not make an appropriate evolutionary model of human pubertal maturation.     

A comparison of sex steroid hormone excretion and metabolism by psittacine species

The metabolism, excretory rates, and excretory patterns of carbon 14 (¹⁴C) radiolabeled estradiol (E₂) and testosterone (T) were studied in female budgerigars (Melopsittacus undulatus) and orange‐winged Amazon parrots (Amazona amazonica). Radiolabeled E₂ and T were injected intramuscularly into six budgerigars and two orange‐winged Amazon parrots. Serial fecal/urine samples were collected for 168 h post‐radiolabel injection. Peak radiolabeled E₂ excretion was observed at 4 h post‐injection, and by 24 h, 93.3 ± 6.3 and 65.9% (range, 59.1–72.7%) of the injected radiolabel was recovered in the fecal/urine matter of budgerigars and orange‐winged Amazon parrots, respectively. Similarly, peak radiolabeled T excretion was observed at 4 h post‐injection with 92.7± 3.6 and 66.2% (range, 57.5–75.2%) of the injected radiolabel recovered in the fecal/urine matter by 24 h in the budgerigars and orange‐winged Amazon parrots, respectively. High‐performance liquid chromatography (HPLC) analysis of the fecal/urine material revealed that both parrot species excreted >80% of the radiolabel in the form of complex steroid conjugates. Immunoreactive E₂ and T metabolites were detected using estrone (E₁) and C‐21/C‐19 conjugate enzyme immunoassays, respectively. Hydrolysis of the E₂ metabolites and HPLC analysis of the ether extracts revealed that E₂ and E₁ were the major steroid moieties. Hydrolysis of the T metabolites and HPLC analysis of the ether extracts revealed two and three major unconjugated peaks for the budgerigars and the orange‐winged Amazon parrots, respectively. Zoo Biol 18:247–260, 1999. © 1999 Wiley‐Liss, Inc.     

Fatal intragroup kidnapping in yellow baboons

The fatal kidnapping of a 5-day-old baboon (Papio cynocephalus) in Amboseli National Park, Kenya, is described. Although pulling and rough handling of primate infants by nonmothers are frequently observed, records of fatal intragroup kidnappings are rare. In the instance described here, the mother, a healthy, primiparous female, did not retrieve the infant from the kidnapper, a higher-ranking juvenile female of the same group, until he died 3 days later, presumably from starvation or dehydration. This incident is compared with other fatal intragroup kidnappings in nonhuman primates and related to adaptive interpretations.     

Information content of female copulation calls in yellow baboons.

In a wide variety of animal species, females produce vocalizations just before, during, or immediately after copulation. Observational and experimental evidence indicates that these copulation calls are sexually selected traits, functioning to promote competition between males for access to the calling female. In this paper, we present an acoustic analysis of variation in the form of copulation calls of female yellow baboons, Papio cynocephalus cynocephalus. In particular, we examine whether information about three factors-the calling female's reproductive state, the occurrence or absence of ejaculation, and the dominance rank of the mating male-is encoded in call structure and hence is potentially available to male receivers attending to the signal. Although several features of copulation calls were correlated with each of these factors, when all three were included in multiple regressions only reproductive state and rank of the mating male had independent effects on call form. These findings indicate that female copulation calls in this species signal information about the proximity to ovulation of the calling female and also the relative competitive strength of her mating partner.     

Correlates of agonistic and competitive interactions in pregnant baboons

Maternal condition during pregnancy is known to influence fetal viability. Recently, primatologists have suggested that certain characteristics of the fetus may influence maternal condition as well. For example, among captive pigtailed macaques (Macaca nemestrina) mothers of female infants may be at greater risk of injury during their pregnancies than mothers of male infants. Analysis of the rates of aggression, submission, competition, and wounding among free-ranging pregnant baboons (Papio cynocephalus) in Amboseli National Park generally fail to support these findings, but several other factors such as maternal dominance rank, environmental conditions during pregnancy, maternal parity, and fetal age correlate with aggression, submission, competition, and injuries sustained by pregnant female baboons.     

Seasonal Changes of Reproductive Behavior and Fecal Steroid Concentrations in Père David's Deer

From July 1997 to September 1997 and from March 1998 to July 1998, we studied reproductive behaviors of Père David's deer in Dafeng, China. During the field behavioral observations, we collected fresh voided fecal samples from the Père David's stags and hinds periodically and kept those samples under −20°C until laboratory analysis. We analyzed the fecal testosterone, estradiol, and progesterone concentrations in those samples using radioimmunoassay. During this study, we also recorded 17 types of male reproductive behaviors and nine types of female reproductive behaviors. Reproductive behaviors and the fecal steroid concentrations showed overt seasonal fluctuations. There were statistically significant correlations between some male reproductive behaviors, such as anogenital sniffing, urine sniffing, urine spraying, wallowing, bellowing, antler adorning, Antler swags mud, chasing, herding hinds, chin resting, mounting and copulating, with the fecal testosterone concentrations. These results suggested that seasonal reproductive behaviors in stags are strongly associated with circulating testosterone. We also found that some female reproductive behaviors fluctuate corresponding with changes in fecal estrogen concentrations. Although there was no direct evidence to confirm the correlations between female reproductive behaviors and fecal estrogen in our experiment, we could not rule out that reproductive activities of hinds were largely related to ovarian estrogen secretion, and estrogen is necessary for inducing female reproductive behaviors.     

Life-history correlates of steroid concentrations in wild peripartum baboons

Steroid concentrations during late pregnancy and early lactation may be affected by both a female's reproductive history and her current condition, and may in turn predict subsequent life-history events, such as offspring survival. This study investigated these relationships in a wild primate population through the use of fecal steroid analysis in repeated sampling of peripartum baboons (Papio cynocephalus). Fecal samples were collected from 32 females in five groups within the Amboseli basin during 8 weeks prior to parturition and 13 weeks postpartum. From December 1999 through February 2002, 176 fecal samples were collected from individuals representing 39 peripartum periods. Fecal concentrations of progestins (fP), estrogen metabolites (fE), glucocorticoids (fGC), and testosterone metabolites (fT) were measured by radioimmunoassay. Steroid concentrations declined from late pregnancy to lactation, and the decline was greatest and most precipitous for fE and fP. Primiparous females had significantly higher mean fE concentrations in each of the last 2 months of pregnancy compared to multiparous females. Among multiparous females, fE and fT were significantly higher during late pregnancy in females carrying a male fetus compared to those carrying a female fetus. During early lactation, high fT in young mothers predicted subsequent infant death during the first year of life. These findings illustrate the potential power of repeated fecal-steroid sampling to elucidate mechanisms of life-history variability in natural populations. They also document significant differences in hormone profiles among subgroups, and highlight that such normative subgroup information is essential for interpreting individual variability in hormone-behavior associations.     

A cytogenetic survey of 110 baboons (Papio cynocephalus)

A cytogenetic investigation of 110 adult baboons (Papio cynocephalus) captured in Kenya and sacrificed at the Institut Pasteur, Paris, showed the absence of anomalies, numerical or structural bearing on nonheterochromatic material; a polymorphism of the AgNOR-positive secondary constriction of chromosome 5 in 12% of the animals; a polymorphism of a secondary constriction of chromosome 7 in 2% of the animals; a fragile site of chromosome 6 in one animal. We believe that our data show that cytogenetic observations in present day primates probably reflect their chromosomal evolution.     

Age and individual foraging behavior predict tooth wear in Amboseli baboons

Teeth represent an essential component of the foraging apparatus for any mammal, and tooth wear can have significant implications for survival and reproduction. This study focuses on tooth wear in wild baboons in Amboseli, southern Kenya. We obtained mandibular and maxillary tooth impressions from 95 baboons and analyzed digital images of replicas made from these impressions. We measured tooth wear as the percent dentine exposure (PDE, the percent of the occlusal surface on which dentine was exposed), and we examined the relationship of PDE to age, behavior, and life history variables. We found that PDE increased significantly with age for both sexes in all three molar types. In females, we also tested the hypotheses that long‐term patterns of feeding behavior, social dominance rank, and one measure of maternal investment (the cumulative number of months that a female had dependent infants during her lifetime) would predict tooth wear when we controlled for age. The hypothesis that feeding behavior predicted tooth wear was supported. The percent of feeding time spent consuming grass corms predicted PDE when controlling for age. However, PDE was not associated with social dominance rank or maternal investment. Am J Phys Anthropol, 2010. © 2010 Wiley‐Liss, Inc.     

Scratching,dominance, tension,and displacement in male baboons

This paper reports a study designed to test the hypothesis that a relationship exists among dominance rank, tension, and scratch behaviors in anubis baboons (Papio cynocephalus anubis). Our study was conducted on two groups of male baboons, each containing eight unrelated individuals who were approximately 6 years of age and who shared common rearing histories. Focal animal sampling was used to collect behavioral data. Hand scratching, foot scratching, avoid, tension, allogrooming, autogrooming, and manipulation were measured as acts performed per hour of sampling. Dominance matrices were constructed based on net difference of avoid behavior performed and received (adjusted for time sampled). Individual status ranks were grouped into two status classes, high and low. Analysis of variance models demonstrated significant differences in the performance rate of scratching behaviors by dominance rank class, as well as differences in scratching performance by tension class. Individuals in the high status class had significantly higher rates of total scratching, hand scratching, foot scratching, and tension behavior performance than their counterparts in the low status class. No significant difference was found between status classes or tension classes for performance rate of allogrooming, autogrooming, or manipulation behavior. The frequency of scratching and general level of activity were not significantly correlated. The results are interpreted to indicate the possibility that scratching may function as a displacement behavior, which subjectively appears to communicate heightened frustration, anxiety, or arousal.     

Excretion and metabolic fate of radiolabeled estradiol and testosterone in the cockatiel (Nymphicus hollandicus)

The metabolism and time courses for clearance of radiolabeled estradiol and testosterone were studied in the female cockatiel (Nymphicus hollandicus) using a simple technique of solubilizing dried fecal/urine matter in an aqueous solution. Carbon ¹⁴ radiolabeled estradiol and testosterone were injected intramuscularly and the urine and fecal matter collected for the pursuant 168 hr. The predominant radiolabel peak was found associated with the aqueous residue of the ether extracted aliquot for both hormones. High-performance liquid chromatographic (HPLC) separation of solubilized fecal/urine material collected during the first sampling interval (0–4 hr after injection) demonstrated that the majority of the excreted radiolabel was in the form of conjugated steroid metabolites in both the estradiol and testosterone injected birds. Subsequent hydrolysis of the aqueous residue of the ether extracted aliquots and HPLC characterized the estrogen and testosterone metabolites as being estrone/estradiol and a variety of androgen based moieties, respectively. By 24 hr postinjection, 79.4 and 79.1% of the original radiolabel was recovered in birds injected with estradiol and testosterone, respectively. These findings demonstrate that steroid hormone excretion in the cockatiel is a rapid and efficient process that is 79% complete by 24 hr and that the primary excretion products are conjugated metabolites. This study also supports the concept that fecal/urine collection is a practical and efficient method of monitoring sex steroid excretion and provides additional evidence that simple solubilization of fecal matter is a sufficient and efficient method for processing feces for subsequent metabolite measurements. Zoo Biol 16:505–518, 1997. © 1997 Wiley-Liss, Inc.     

Fecal analysis of ovarian cycles in female black-handed spider monkeys (Ateles geoffroyi)

An enzyme immunoassay (EIA) was applied to characterize the reproductive endocrinology of adult female black-handed spider monkeys (Ateles geoffroyi). Analysis of paired urine and fecal samples, collected from two females housed at San Diego Zoo, confirmed that the EIAs employed provided quantitative measurements of ovarian sex steroid hormones. Fecal metabolite levels were significantly correlated with those in urine, confirming that feces are a valid source of steroid metabolites in this species. The excretion of these metabolites in feces lagged urinary excretion by 1-2 days. The ovarian cycle profiles of the two captive females and five free-ranging females are comparable, with an average length of approximately 20-23 days. Cyclical bleeding, as previously reported, was observed in one of the two captive females. Pregnancy was detected in four free-ranging females, and early fetal loss for one female was indicated by hormonal data.     

Steroid metabolism and validation of noninvasive endocrine monitoring in the African wild dog (Lycaon pictus)

The purpose of this study was to validate noninvasive endocrine monitoring techniques for African wild dogs (Lycaon pictus) and to establish physiological validity of these methods by evaluating longitudinal reproductive-endocrine profiles in captive individuals. To determine the primary excretory by-products of ovarian steroid metabolism, [¹⁴C]-progesterone and [³H]-estradiol were co-administered to a female and all excreta were collected for 80 hr postinjection. Radiolabel excretion peaked ≤ 18 hr postinfusion, and progesterone and estradiol metabolites were excreted in almost equivalent proportions in urine (39.7 and 41.1%, respectively) and feces (60.3 and 58.9%, respectively). Most of the urinary metabolites were conjugated (estradiol, 94.3 ± 0.3%; progesterone, 90.4 ± 0.5%), so that immunoassays for pregnanediol-3α-glucuronide (PdG) and estrogen conjugates (EC) were effective for assessing steroid metabolites. Two immunoreactive estrogens (estradiol and estrone) and at least one immunoreactive progesterone metabolite (3α-hydroxy-5α, pregnan-20-one) were detected in feces. Urine and fecal samples were collected (1–3 times per week) for 1.5 yr from one adult female and two adult males to assess longitudinal steroid metabolite excretion. Overall correlation of urinary PdG to matched, same-day fecal progesterone metabolites immunoreactivity was 0.38 (n = 71, P < 0.05). Similarly, urinary EC was correlated (P < 0.05) with same-day fecal estrogen immunoreactivity (r = 0.49, n = 71). During pregnancy and nonpregnant cycles, copulation occurred at the time of peak (or declining) estrogen metabolites and increasing progesterone metabolites concentrations. Estrus duration was 6–9 days and gestation lasted 69 days with parturition occurring coincident with a drop in progesterone metabolites. Males exhibited seasonal trends in fecal testosterone excretion with maximal concentrations from July to September coincident with peak mating activity. Although these limited longitudinal hormone profiles should be interpreted cautiously, noninvasive gonadal steroid monitoring suggests that: (1) both female and male wild dogs may exhibit reproductive seasonality in North America, (2) females are monoestrous, and (3) peak testicular activity occurs between August and October coincident with mating behavior. From a conservation perspective, noninvasive endocrine monitoring techniques should be useful for augmenting captive breeding programs, as well as for developing an improved understanding of the physiological mechanisms underlying reproductive suppression in response to social and ecological pressures. Zoo Biol 16:533–548, 1997. © 1997 Wiley-Liss, Inc.     

Movement patterns of yellow baboons (Papio cynocephalus): Sex differences in juvenile development toward adult patterns

Age-sex differences in the sociospatial positioning of progressing baboon troops have been postulated as an important, protective aspect of baboon adaptation to a terrestrial existence. The protection theory is an ultimate hypothesis which can be disproven by showing that the postulated age-sex positioning fails to occur. Alternatively, confidence in the protection theory can be increased if the postulated positioning persists across several troops despite significant opportunities for variation, and if progression order is shown to be linked to biological phenomena such as sex differences in physical maturation. Data from 73 individually identified, free-ranging juveniles of both sexes were compared with previous findings. Small juveniles of several troops were more centrally located than large juveniles. Large juveniles males were more toward the front than were large juvenile females. As male walking infants and juveniles aged, a change in positioning (i.e., location) occurred: males were located increasingly toward the front of progressions. Comparable data from females suggest that the adult female pattern had begun to form among large juveniles. Data are consistent with an ultimate protection theory.     

Movement patterns of yellow baboons (Papio cynocephalus): Central positioning of walking infants

According to DeVore and Washburn's protection theory of the spatial organization of moving baboon troops, walking infants, which are among the most vulnerable and least self-sufficient of all troop members, should tend to occupy the troop's center. The protection theory is an ultimate hypothesis from which persistently recurring behavior is expected. Two troops living in Mikumi National Park, Tanzania, were compared with troops studied at other locations. Walking infants tended to occupy the center of their troop and to be underrepresented primarily in the frontal portion of progressions and secondarily in the rear. The lead position of progressions was analyzed using 82 walking infants, 11 troops, three locations, two species, and three studies involving eight or more observers employing somewhat different procedures at the different study sites. Despite so many opportunities for variation, 1,317 observations from these 11 troops did not produce a single instance in which a walking infant led the troop and very few in which one was in the frontal twelfth.     

Gm and Inv studies on baboons, Papio cynocephalus: analysis of serum samples from Kenya, Ethiopia and South Africa.

Serum samples from 526 baboons (Papio cynocephalus) from 10 troops from the Laikipia district of northern Kenya, from 60 baboons from two troops from the Awash National Park, central Ethiopia, and from 127 baboons from South Africa were tested for Gm and Inv allotypes. Four of the 10 troops from Kenya formed a western cluster and six formed an eastern cluster. The clusters were separated by approximately 10 miles. The samples were tested for Gm (1, 2, 3, 5, 6, 11, 13, 14, 15, 16, 17, 21, 24) and for Inv (1, 2, 3). All samples were negative for Gm (2, 6, 14, 16, 24). All from Kenya and Ethiopia were negative for Inv (2), and all were positive for Gm (11, 17) and for Inv (3). The south African samples differed from the others in that 10 were negative for Gm (11) and four were positive for Inv (2). Taking all animals into account, polymorphism was present for Gm (1, 3, 5, 11, 13, 15, 21) and for Inv (1, 2). No two Kenya troops had the same array of phenotypes or of haplotypes, but the four western troops were more similar to each other than to the six eastern troops. Three haplotypes were present in the eastern troops that were not present in the western troops and five were present in the western troops that were not present in the eastern troops. Five haplotypes appeared in at least some troops of each cluster of troops. The samples from each of the two troops from Ethiopia show the same three phenotypes but with significantly different frequencies. It is suggested that the variation in haplotype frequencies observed among the 10 troops from Kenya is the result of a founder effect deriving largely from fission of a large troop into two smaller troops. The data show that speculations about the evolutionary origin of the allotypes are premature. For most species, too few animals have been tested and except for those in this study their origins are not known. Finally, the samples have been from too restricted an area.     

Development of a field‐friendly technique for fecal steroid extraction and storage using the African wild dog (Lycaon pictus)

Hormonal analysis provides information about wildlife populations, but is difficult to conduct in the field. Our goal was to develop a rapid and effective field method for fecal steroid analysis by comparing: (1) three extraction methods (laboratory (LAB), homogenize (HO) and handshake (HS)) and (2) two storage methods (solid‐phase extraction (SPE) tubes vs. plastic tubes (PT)). Samples (n=23) from captive African wild dogs (Lycaon pictus) were thoroughly mixed, three aliquots of each were weighed (～0.5 g) and 5 ml of 90% ethanol was added. For LAB, samples were agitated (mixer setting 60; 30 min), centrifuged (1,500 rpm; 20 min) and poured into glass tubes. Or aliquots were HO (1 min) or HS (1 min) and poured through filter paper into glass tubes. Samples were split, analyzed for corticosterone (C) and testosterone (T) metabolites using enzyme immunoassays or stored in SPE or PT. Samples were stored (room temperature) for 30, 60 or 180 days, reconstituted in buffer and analyzed. Mean C and T recoveries of HO were greater (P=0.03) than HS compared with LAB, which was similar to HO (P>0.05). After 30 days <21% of C and T was recovered from SPE, but ～100% of each was recovered from HO‐PT and HS‐PT. Similarly, after 60 and 180 days, ～100% of C and T was recovered from HO‐PT and HS‐PT. Results demonstrated that, for C and T, HO was more comparable (P<0.001) to LAB than HS and PT storage was more efficient than SPE (P<0.001). Zoo Biol 29:289–302, 2010. © 2009 Wiley‐Liss, Inc.     

Demography of Amboseli baboons, 1963–1983

Repeated censuses of a population of yellow baboons (Papio cynocephalus) in Amboseli National Park, Kenya, revealed a decrease from over 2,500 animals in 1963–1964 to 123 individuals in 1979, or from a density of about 73 to 1.8 baboons per km² over a 15-year period. Median group size decreased from 43 in 1964 to 27 in 1979. The largest and smallest groups declined the most; groups near the median have maintained fairly stable size and age distributions. The population seemed to have stabilized by 1983 at approximately 150 animals in six groups (median group size 28; density 2.2/km²). Although baboon population and group size appeared to be stable during 1963–1964, the age distribution and demographic parameters (age-specific mortality and natality for one social group) during that year indicate that the population decline had already started. The rate of population decline was greatest in the 1964–1969 period and remained appreciable during the next 5 years. The decline of the baboon population was paralleled by that of other Amboseli savannah woodland mammalian species and took place during a period of very high mortality of fever trees (Acacia xanthophloea) and extensive invasion of the area by halophytes, a transition brought on by rising ground water and consequent elevation of the soil salinity zone. In this and several other primate populations, mortality of infants and juveniles appears to be the demographic variable most sensitive to environmental change.     

Carbonic anhydrase isoenzymes in nine troops of Kenya baboons, Papio cynocephalus (Linnaeus 1766)

The distributions of alleles at the carbonic anhydrase I (CA I = CA B) and carbonic anhydrase II (CA II = CA C) loci in nine troops of Papio cynocephalus were determined. Two alleles were found at the CA I locus, and three at the CA II locus; the frequencies were: CA I^a = 0.856; CA I^b = 0.144; CA II^a = 0.784; CA II^b = 0.209; CA II^c = 0.007. Results of tests for Hardy-Weinberg equilibrium, homogeneity tests, and calculations of migration rates were used in support of the interpretation that migration and genetic drift may affect the distribution of alleles at the CA I locus and that selection is the process responsible for the distribution of alleles at the CA II locus.