Reproduction in the vervet monkey (Cercopithecus aethiops): II. Annual menstrual patterns and seasonality

Menstrual patterns and progesterone levels were monitored for 5 years from a cohort of 28 female vervet monkeys that were individually caged indoors. Three distinct cycle types (short, normal, and prolonged) were defined according to cycle length. Mean length of the normal cycle (32.5 days) and menses duration (4.8 days) are in agreement with previous reports. Prolonged cycles (> 50 days) contributed 20% of the total, with a decreased incidence during the natural peak breeding period. Weekly progesterone measurements indicated that many prolonged cycles were associated with an extended luteal phase, while others were probably due to lack of ovulation. From these data it would appear that the vervet monkey, although not strongly seasonal, does favor a particular time of year for breeding in a colony housed indoors.     

Hematological changes in vervet monkeys (Chlorocebus aethiops) during eight months' adaptation to captivity

This study investigated fluctuations in hematological values of 50 wild-caught vervet monkeys (African green monkeys, grivets, Chlorocebus aethiops) during habituation to captivity. The monkeys were categorized into four groups according to age and sex viz adult males, adult females, juvenile males, and juvenile females. The erythrocyte values were significantly higher (P<0.05) in the adult males than in the other animals. There was an increase in most of the erythrocyte parameters studied during the monitoring period with the most significant being hemoglobin, hematocrit, and mean corpuscular volume. However, the red cell distribution widths, which were higher in adult females, declined. The total white blood cell (WBC) counts, which were higher in adult females than in the other animals, were closely correlated with granulocytes counts. The WBC levels decreased in all the animals throughout the 8 months study, indicating gradually decreasing stress, but they were relatively stable in males. The platelet counts declined significantly (P<0.05) and at 8 months post capture the counts were higher in females than in males. The juvenile female platelet counts were relatively stable during the monitoring period. The maintenance of the monkeys on an improved stable diet and in environment-controlled housing combined with progressing psycho-physiological adaptation may be important factors for the gradual improvements of the hematological values recorded. There were wide variations in these between individual animals emphasizing the need for long adaptation combined with establishment of individual baseline values before experimental studies.     

Comparative effects of interferon alpha‐2b and pegylated interferon alpha‐2b on menstrual cycles and ovarian hormones in cynomolgus monkeys

BACKGROUND : The covalent modification of interferon (IFN) α2b with monomethyoxy polyethylene glycol (PEG) reduces its clearance rate and increases its half‐life. High doses of interferon (IFN) α2b have previously been shown to affect maintenance of pregnancy in rhesus monkeys. Given the role of ovarian hormones in reproductive function and pregnancy, this study was conducted to assess the effects of PEG‐IFNα2b or IFNα2b (comparative control) on ovarian hormones and menstrual cyclicity in cynomolgus monkeys. In addition, the potential for reversibility of PEG‐IFNα2b or IFNα2b‐related observations was assessed. METHODS : Monkeys were administered 3,105 µg/m² human recombinant (hr) IFNα2b or 52, 262, or 4,239 µg/m² PEG‐hr‐IFNα2b every other day for one menstrual cycle, followed by a post‐dose period of up to two menstrual cycles. RESULTS : Monkeys administered 3,105 µg/m² hr‐IFNα2b or 52, 262, or 4,239 µg/m² PEG‐hr‐IFNα2b exhibited transient decreases in food consumption, leukocyte and erythrocyte parameters. Monkeys administered 3,105 µg/m² hr‐IFNα2b exhibited lengthened menstrual cycles that were associated with a delay in reaching peak ovarian hormone levels and lower respective peak concentrations. Similarly, monkeys administered 4,239 µg/m² PEG‐hr‐IFNα2b exhibited lengthened menstrual cycles and a delay in reaching peak ovarian hormone levels and slightly lower respective peak concentrations. Post‐dosing menstrual cycle length, estradiol and progesterone profiles exhibited evidence of recovery in both the hr‐IFNα2b and the high‐dose PEG‐hr‐IFNα2b groups. CONCLUSIONS : Administration of hr‐IFNα2b or PEG‐hr‐IFNα2b at high doses to cynomolgus monkeys resulted in similar effects on menstrual cycles, estradiol and progesterone profiles, and exhibited evidence of reversibility upon cessation of dosing. These results suggest that the previously observed high‐dose IFNα‐related effects on the maintenance of pregnancy in monkeys are likely the result of altered ovarian function. Birth Defects Res (Part B) 86:29‐39, 2009. © 2009 Wiley‐Liss, Inc.     

Contact with human facilities appears to enhance technical skills in wild vervet monkeys (Chlorocebus aethiops)

Technical abilities of primates are typically tested in the laboratory. It has been argued that close contact between animals and humans may lead to an increase in skills due to an 'enculturation' of subjects. Here, we provide evidence that exposure to human facilities may improve wild vervet monkeys' technical skills in a social learning task using the 'artificial fruit' approach. Two of our 6 study groups had access to human facilities within their territories. Only members of these 2 groups were likely to open successfully 'artificial fruit' during their first attempt. Success appeared to be independent of individual sex or the type of task. Our results highlight the possibility that human enculturation may allow captive monkeys to acquire more technical skills than their wild counterparts, and we suggest that this possibility should be tested in further field experiments.     

Vitamin A toxicity in wild-caught African green vervet monkeys (Chlorocebus aethiops) after 2 years in captivity

Primate lab diets typically contain high vitamin A concentrations when compared with human recommended intakes. In this study, we analyzed the vitamin A contents of liver and serum from 13 adult female African green vervet monkeys (Chlorocebus aethiops). These monkeys were wild-caught and held in captivity for 2 y, during which time they consumed a standard primate diet. Liver vitamin A concentration (mean +/- 1 standard deviation) was 14.6 +/- 2.3 micromol retinol/g liver; subtoxicity in humans is defined as at least 1 micromol/g liver. The serum retinol concentration (0.93 +/- 0.21 microM) was not elevated. Hypertrophy and hyperplasia of hepatic stellate cells were present which, in conjunction with elevated hepatic vitamin A concentrations, are evidence of toxicity. Although the ramifications of chronically toxic vitamin A status in experimental monkeys have not been defined, this state may influence nonhuman primate research outcomes and confound data interpretation. The validity of bone mineral research using nonhuman primates is of greatest concern, in light of the association between vitamin A toxicity and compromised bone health.     

Probable genetic origin for a large number of cataracts among captive-bred vervet monkeys (Chlorocebus aethiops)

During a period of 6 years, uni- or bilateral cataracts occurred in 55 captive-bred vervet monkeys, representing 27.6% of all offspring produced in that time. Fifty-eight percent of all cases were detectable only by ophthalmoscopy. A total of 30% of cases were offspring of wild-caught parents, 40% from first-generation captive-bred parents, 4% from second-generation captive-bred parents, and 26% from parents of which one was wild caught. Cataracts that could be observed macroscopically appeared at about 6-8 mo of age. A sample of juvenile vervet monkeys with cataracts and their parents had no antibodies against rubella virus, herpes simplex virus, or toxoplasma gondi, and all except two wild-caught breeding females had no antibodies against cytomegalovirus. Plasma vitamin D3 (25 [OH] D), calcium, phosphorus, and glucose concentrations of six cataract cases were comparable to a control group of healthy individuals. The exclusion of these extraneous factors, as well as the fact that the majority of all cases were related, was considered evidence of hereditary etiology. Males and females that had either produced offspring with cataracts or were related to individuals with cataracts were replaced. To date, 35 babies have been born, and no new cases have since occurred.     

The effect of housing and environmental enrichment on stereotyped behavior of adult vervet monkeys (Chlorocebus aethiops)

Little information is available on the response of vervet monkeys to different housing conditions or on the suitability of enrichment devices or methods for vervet monkeys. In this study, the authors evaluated the occurrence of stereotyped behavior in adult vervet monkeys under various conditions of housing and enrichment. The variables included cage size, cage level (upper or lower), enrichment with a foraging log, enrichment with an exercise cage and presence of a mate. The authors first determined the incidence of stereotyped behavior in captive-bred, singly housed adult female and male vervet monkeys. They then exposed monkeys to different housing and enrichment situations and compared the incidence of stereotyped behavior among the monkeys. The authors found that more females than males engaged in stereotyped behavior and that females, on average, engaged in such behavior for longer periods of time than males. Stereotyped behavior was most often associated with a small, single cage. The average amount of observed stereotyped activity in monkeys housed in a small cage was significantly lower when the monkeys had access to either a foraging log or an exercise cage. Stereotyped behavior was also lower in female monkeys that were housed (either with a male or without a male) in a larger cage. The least amount of abnormal behavior was associated with the largest, most complex and enriched housing situation. Males and females housed in cages on the lower level of two-level housing engaged in more stereotyped behavior than did monkeys housed in the upper level, regardless of the presence or type of enrichment provided.     

A genetic linkage map of the vervet monkey (Chlorocebus aethiops sabaeus)

The spectacular progress in genomics increasingly highlights the importance of comparative biology in biomedical research. In particular, nonhuman primates, as model systems, provide a crucial intermediate between humans and mice. The close similarities between humans and other primates are stimulating primate studies in virtually every area of biomedical research, including development, anatomy, physiology, immunology, and behavior. The vervet monkey (Chlorocebus aethiops sabaeus) is an important model for studying human diseases and complex traits, especially behavior. We have developed a vervet genetic linkage map to enable mapping complex traits in this model organism and facilitate comparative genomic analysis between vervet and other primates. Here we report construction of an initial genetic map built with about 360 human orthologous short tandem repeats (STRs) that were genotyped in 434 members of an extended vervet pedigree. The map includes 226 markers mapped in a unique order with a resolution of 9.8 Kosambi centimorgans (cM) in the vervet monkey genome, and with a total length (including all 360 markers) of 2726 cM. At least one complex and 11 simple rearrangements in marker order distinguish vervet chromosomes from human homologs. While inversions and insertions can explain a similar number of changes in marker order between vervet and rhesus homologs, mostly inversions are observed when vervet chromosome organization is compared to that in human and chimpanzee. Our results support the notion that large inversions played a less prominent role in the evolution within the group of the Old World monkeys compared to the human and chimpanzee lineages. Electronic supplementary material The online version of this article (doi: ) contains supplementary material, which is available to authorized users.     

Decreased global DNA methylation in the white blood cells of high fat diet fed vervet monkeys (Chlorocebus aethiops)

Epigenetic mechanisms are associated with the development of many chronic diseases and due to their reversible nature offer a unique window of opportunity to reverse the disease phenotype. This study investigated whether global DNA methylation correlates with dysglycemia in the vervet monkey (Chlorocebus aethiops). Diet-induced changes in DNA methylation were observed where global DNA methylation was twofold lower in monkeys fed a high fat diet (n?=?10) compared to monkeys fed a standard diet (n?=?15). An inverse correlation was observed between DNA methylation, blood glucose concentrations, bodyweight, and age, although the association was not statistically significant. Consumption of a high fat diet is associated with the development of metabolic disease; thus, these results suggest the use of global DNA methylation as a biomarker to assess the risk for metabolic disease. Moreover, this study provides further support for the use of the vervet monkey as a model system to study metabolic diseases such as type 2 diabetes. Integration of altered DNA methylation profiles into predictive models could facilitate risk stratification and enable intervention strategies to inhibit disease progression. Such interventions could include lifestyle modifications, for example, the increased consumption of functional foods with the capacity to modulate DNA methylation, thus potentially reversing the disease phenotype and preventing disease.     

Pregnancy outcome in free-ranging vervet monkeys (Cercopithecus aethiops)

A preliminary assessment of individual female differences in conception rate and fetal wastage has been determined for a population of wild vervet monkeys (Cercopithecus aethiops). One of three troops of vervet monkeys, the subjects of a long-term behavioral study, was trapped and blood was obtained for electrophoretic analysis. Pregnant females exhibited a distinctive serum aminopeptidase phenotype allowing a conclusive determination of pregnancy. Of the seven females diagnosed as pregnant, three later gave birth. Of the females that aborted, two were nulliparous and one was very old. Studies of captive animals have indicated that age and rank may affect a female's ability to carry a fetus to term. These factors, rather than the trapping procedure, may have been responsible for most of the fetal loss in the trapped troop. A comparison of all three troops for a 3-year period indicated that there were fluctuations in yearly birth success of individual females, as well as a relatively high miscarriage rate. The results of this study indicate the advantages of obtaining joint behavioral and biological data.     

Fire and home range expansion: A behavioral response to burning among savanna dwelling vervet monkeys (Chlorocebus aethiops)

The behavioral adaptations of primates to fire‐modified landscapes are of considerable interest to anthropologists because fire is fundamental to life in the African savanna—the setting in which genus Homo evolved. Here we report the behavioral responses of a savanna‐dwelling primate, vervet monkeys (Chlorocebus aethiops), to fire‐induced ecological change. Using behavioral and spatial data to characterize ranging patterns prior to and postburn and between burn and nonburn years, we show that these primates inhabiting small, spatially bound, riverine habitats take advantage of newly burned savanna landscapes. When subjects encountered controlled fires, they did not flee but instead avoided the path of the fire seemingly unbothered by its approach. After fire, the primates' home range expanded into newly burned but previously unused areas. These results contribute to understanding the response of non‐human primates to fire‐modified landscapes and can shed light on the nature and scope of opportunities and constraints posed by the emergence of fire‐affected landscapes in the past. Results also expose deficiencies in our knowledge of fire‐related behavioral responses in the primate lineage and highlight the need for further investigation of these responses as they relate to foraging opportunities, migration, resource use, and especially fire‐centric adaptations in our own genus. Am J Phys Anthropol 154:554–560, 2014. © 2014 Wiley Periodicals, Inc.     

Urinary immunoreactive estrogen and pregnanediol-3-glucuronide during the normal menstrual cycle of the female lowland gorilla (Gorilla gorilla)

Urine samples were taken daily during 22 menstrual cycles of six normal adult female gorillas. Urine was analyzed for total immunoreactive estrogens (E_t) and pregnanediol-3-glucuronide (PdG) and indexed by creatinine (Cr). An average cycle length of 32 ± 1 days (mean ± SE) with a range of 25–42 days is reported. Estrogen values range from 4 to 128 ng/mg Cr and show a midcycle peak and a midluteal rise. PdG values range from 0.01 to 2.4 μg/mg Cr and display a low, flat follicular phase followed by a luteal elevation. The follicular phase is 19.5 ± 1 days in length (range 11–30 days) and accounts for the variation in cycle length. The luteal phase is 12.3 ± 0.3 days long (range 10–14 days). In contrast to previous studies, PdG levels rise two days before the estrogen peak. The results from the present study are compared with information available on the gorilla, chimpanzee, and human. The accuracy of various alignment methods is discussed, as well as the importance of the methods presented in this study for the captive propagation of gorillas.     

Captive propagation of vervet monkeys (Cercopithecus aethiops) in harems

A small breeding colony of captive vervet monkeys (Cercopithecus aethiops), consisting of ten single male harem groups, was established in Kenya. Vervets were extremely prone to stress after capture and manipulative procedures led to high mortalities. Six weeks were required for partial habituation, after which routine handling was not too problematic. However, complete adjustment to captivity took a minimum of one year. Establishment of stable breeding groups from adult animals initially proved difficult because of fighting among females. Once harem groups stabilized, reproductive rate was high with just under 90% pregnancies and 85% livebirths annually. Births exhibited a seasonal pattern similar to that reported from wild populations in Kenya.     

Female mate choice in vervet monkeys (Cercopithecus aethiops sabaeus)

Female mate choice was examined in a captive group of vervet monkeys (Cercopithecus aethiops sabaeus). Male-female interactions were examined under both dyadic and group conditions to determine whether females mate with different males under the two conditions. Results showed that all females preferred to mate with the alpha male under both dyadic and group conditions. Alpha females, however, were more successful than subordinate females in rejecting the sexual solicitations of subordinate males. Thus female dominance status played an important role in determining the degree to which females exercised mate choice.     

The influences of sleep duration,chronotype, and nightwork on the ovarian cycle

ABSTRACT

Despite research indicating that sleep disorders influence reproductive health, the effects of sleep on reproductive hormone concentrations are poorly characterized. We prospectively followed 259 regularly menstruating women across one to two menstrual cycles (the BioCycle Study, 2005–2007), measuring fasting serum hormone concentrations up to eight times per cycle. Women provided information about daily sleep in diaries and chronotype and night/shift work on a baseline questionnaire. We evaluated percent differences in mean hormone concentrations, the magnitude of shifts in the timing and amplitude of hormone peaks, and the risk for sporadic anovulation associated with self-reported sleep patterns and night/shift work. We estimated chronotype scores – categorizing women below and above the interquartile range (IQR) as “morning” and “evening” chronotypes, respectively. For every hour increase in daily sleep duration, mean estradiol concentrations increased by 3.9% (95% confidence interval [CI] 2.0, 5.9%) and luteal phase progesterone by 9.4% (CI 4.0, 15.2%). Receiving less than 7 hours of sleep per day was associated with slightly earlier rises in peak levels for several hormones. Women reporting night/shift work (n = 77) had lower testosterone relative to women employed without night/shift work (percent difference: ?9.9%, CI ?18.4, ?0.4%). Women with morning chronotypes (n = 47) had earlier rises in estradiol during their cycles and potentially an earlier rise in luteinizing hormone. Compared to those who had intermediate chronotypes, women with evening chronotypes (n = 42) had a later luteinizing hormone peak of borderline statistical significance. A reduced risk for sporadic anovulation was suggested, but imprecise, for increasing hours of daily sleep leading up to ovulation (risk ratio 0.79, CI 0.59, 1.06), while an imprecise increased risk was observed for women with morning chronotypes (risk ratio 2.50, CI 0.93, 6.77). Sleep-related hormonal changes may not greatly alter ovarian function in healthy women, but have the potential to influence gynecologic health.