Aging in the musculoskeletal system of rhesus monkeys: III. Bone loss

It is well established that aging of the human skeleton includes the loss of bone mass or density, but little comparative information on age-related osteopenia in other primates is available. In order to determine whether bone loss occurs in normally locomoting nonhuman primates, radiographs of 139 rhesus monkey skeletons from the Cayo Santiago collection were examined, and measures of percent cortical bone (PCT) at the midshaft of second metacarpals, humeri, and femora were calculated. An age-related osteopenia was observed in the metacarpal of adult female macaques, although much individual variation was present. This variability could not be explained by reproductive history (number of offspring), matrilineal affiliation, or degree of osteoarthrosis. However, in a subsample of 15 animals, females who had given birth in the three months prior to death showed lower PCTs than those who had not conceived in the previous mating season. In adult males, PCT did not vary significantly with age, but males that weighed less and those with no/little osteoarthrosis showed lower PCTs than heavier or more arthritic animals, respectively. The multifactorial nature of the variation in PCT observed here suggests that similar processes of bone behavior are involved in the skeletal aging of both humans and rhesus monkeys.     

Percentage ash content of nonhuman primate long limb bones

Trotter and Hixon ('76) and Vose and Roach ('72) presented conflicting data about percentage ash content of the long limb bones of M. mulatta and M. nemestrina. The suggestion of Trotter and Hixon ('76) that this discrepancy was due to methods of preparing the bone prior to ashing, rather than to species differences, was tested using data collected by Gong ('72) on the volumetric composition of nonhuman primate bone. Masses of the various chemical fractions of bone reported by Gong ('72) were used to compute ash content as a percentage of total dry weight and ash content as a percentage of fat-free dry weight. Good agreement was found between ash content as a percentage of total dry weight and the data of Vose and Roach ('72); good agreement was also found between ash content as a percentage of fat-free dry weight and the data of Trotter and Hixon ('76). This suggests that the data of Vose and Roach ('72) conflict with those of Trotter and Hixon ('76) because Vose and Roach ('72) failed to defat the bones prior to ashing. No actual species differences exist in the ash content of bones of M. mulatta and M. nemestrina. The data of Trotter and Hixon ('76) are most likely a more adequate reflection of both the magnitude and the regional similarity of ash content in nonhuman primate bone.     

Primigravidity,body weight,and costs of rearing first offspring in rhesus macaques

Body size is associated with menarche and ovarian function, but the relationship to first conception is rarely examined. We conducted a longitudinal investigation of rhesus macaques, Macaca mulatta, to determine the effect of differences in body weight on both the age at first conception and survivorship of first progeny. Young females who became pregnant weighed significantly more than peers who remained barren, with weight changes for females who successfully raised offspring no different than those for females who did not produce offspring. Infant mortality among primiparae was not significantly greater than that among multiparae, although nearly twice as high. First-born males tended to have lower survivorship than first-born female offspring. We suggest that reproductive costs encountered by primiparous females are more likely to be modulated by immature neuroendocrine function than by inexperience, small body size, or infant suckling patterns. We conclude that body size influences probability of first conception, socioendocrine factors mediate the likelihood of infant survival, and primiparous production of male progeny seems to exert a greater reproductive cost than does production of female progeny. Am. J. Primatol. 46:135–144, 1998. © 1998 Wiley-Liss, Inc.     

现生太行山猕猴与猕猴化石骨指数的比较

为探讨现生太行山猕猴与猕猴化石骨指数的差异,对太行山猕猴与广西崇左早更新世猕猴化石的肢间指数(Intermembral index,IM)、臂指数(Brachial index,BI)、股指数(Crural index,CI)和股骨粗壮指数(Robusticity index,RI)等指数进行比较。结果表明,猕猴化石IM值(96)高于太行山猕猴,BI值(94.5)和CI值(88.5)均低于太行山猕猴,推测该猕猴化石在早更新世时期可能地栖生活,适合于陆地四足行走,同时也验证了太行山猕猴主要为半树栖生活。结合对猕猴化石伴生哺乳动物习性的分析,推测广西崇左早更新世的气候温暖潮湿并有一定的水域,植被以森林和灌木为主,有局部的草地或草坡,其自然环境非常适宜高等灵长类生息繁衍。     

猕猴(Macaca mulatta)主动脉弓的分支类型

随着心血管系统研究的进展和猿猴在医学中的广泛应用,猴主动脉弓分支的情况引起人们的重视。虽然张胜泉等（1974）对猕猴的心脏冠状动脉的解剖学作过调查,但有关主动脉弓分支的资料很少。为此,我们进行了本题研究,以供参考。     

Urinary cyclic AMP excretion is increased in Macaca fascicularis and Macaca mulatta compared to humans

Changes in parathyroid hormone and its second messenger cyclic AMP have been implicated in the pathogenesis of osteoporosis. Nonhuman primate models have been useful in the study of osteoporosis, but the physiology of mineral metabolism in certain species is different than in humans. We investigated parameters of mineral metabolism in 15 normal adult female cynomolgus and 14 normal adult female rhesus monkeys. In both species, urinary cyclic AMP was increased compared with humans, and the nephrogenous cyclic AMP in the cynomolgus monkeys was also elevated. Despite this, there was no evidence for hyperparathyroidism in either species as evaluated by serum or plasma phosphorus and midregion-specific and/or aminoterminal-specific immunoreactive parathyroid hormone. Given the increasing use of nonhuman primates in the study of osteoporosis, understanding basic changes in mineral metabolism is important before pathologic effects of bone loss can be understood.     

Growth of the maxillary complex in the rhesus monkey (Macaca mulatta)

The growth of the maxillary complex of 36 rhesus monkeys (Macaca mulatta) was analyzed quantitatively and qualitatively during four defined stages of postnatal development (i.e., infant, juvenile, adolescent, young adult). At each stage, growth was observed during a 24 week period. Since some animals were observed during two successive stages of development, 47 periods of growth were studied. The incremental growth data were collected by superimposing serial cephalograms on cranial base implants and on maxillary implants. The largest increments of growth were observed in the infant animals and were successively less during the other periods studied. The horizontal growth component was more prominent than the vertical component in all age groups. The contribution of sutural growth to the vertical displacement of the maxilla was greater posteriorly, leading to a rotation of the maxillary complex during growth. The occlusal relationship was maintained by selective bone remodeling in conjunction with dentitional migration.     

Behavioral responses of unrelated rhesus monkey females paired for the purpose of environmental enrichment

An attempt was made to socialize unrelated and unfamiliar adult rhesus monkey females that had lived in single cages for more than one year. Partners first were given the opportunity for noncontact familiarization in partitioned double cages. They were then transferred into an ordinary double cage. Clear-cut rank relationships were evident within the first 90 minutes of pair formation in 94% (17/18) of dyads tested. Only 28% (5/18) of pairs resorted to fighting (in no case with infliction of serious injury), while 50% (9/18) engaged in social grooming or hugging during this initial phase of pair formation. Eighty-three percent (15/18) of pairs were compatible, with none of the partners showing signs of depression and none inflicting serious injury on the other. Seventeen percent (3/18) of pairs were incompatible (two cases of depression, one serious tail injury) and were separated. It was concluded that the barren environment of singly caged rhesus monkey females can be enriched with little risk by carefully making them compatible companions.     

Wounding patterns in three species of captive macaques

The incidence of wounding in captive groups of rhesus (Macaca mulatta), pigtail (M. nemestrina), and stumptail (M. arctoides) macaques was studied for 21 months. Groups were monitored daily for evidence of wounding. Wounded animals were captured, treated by veterinary staff, and returned following recovery. Records were kept on the age, sex, and species of the recipient, along with the type and location of wound. In each species of macaque, adult males incurred the highest frequency of wounds and multiple wounds of any age-sex class. This contrasted with previously reported behavioral data indicating low frequencies of aggression received by adult males, especially contact aggression and bites. These discrepancies indicate wounding frequencies do not necessarily correspond with behavioral measures of aggression. Inhibition of aggression directed toward infants and the selective avoidance of bites directed to vital body regions were presented as possible mechanisms that modify intragroup aggression. Increased wounding in the birth season under captive conditions suggests that the pattern of increased wounding reported during the breeding season under freeranging conditions may reflect xenophobic responses to immigrating males, rather than direct male-male competition for estrous females.     

Atresia of the dominant ovarian follicle in rhesus monkeys is detected within 24 hours of estradiol treatment

Following treatment with estradiol-17β (E₂) on day 6 of the menstrual cycle, degenerative alterations in the microenvironment of the dominant follicle (DF) (follicular fluid [FF], granulosa cells [GC], and oocyte) are readily apparent on day 10, or 96 h after E₂ administration. The present study was designed to determine how early such changes could be detected and which indices of atresia were observed first. The DF was identified during laparoscopy on day 5 or 6 of the cycle, and four capsules containing crystalline E₂ were inserted s.c. for 24 h. Contents of the DF were aspirated at 24, 48, and 72 h following initiation of E₂ treatment. General size and appearance of the DF did not change distinctly with E₂ treatment; however, by 48 h FF viscosity was increased markedly. GC viability was not altered with treatment. FF concentrations of estrogen (E) were dramatically reduced at 24 h. These differences were maintained at 48 h and at 72 h. E accumulation by cultured GC was significantly reduced by > eightfold. There appeared a similar trend for reduced progesterone (P) in FF and decreased P production by GC in vitro. These results demonstrate that degenerative alterations in the DF indicative of atresia can be detected as early as 24 h after initiation of E₂ treatment; the index of atresia appearing earliest is a reduction in FF concentrations of E, and the first morphological changes in the DF can be observed 24 h later. This study indicates that biochemical alterations precede morphologic changes with E₂-induced atresia, and should allow us to begin to determine the earliest events and putative initiation sites of atresia.     

Delayed dispersal and elevated monoaminergic activity in free-ranging rhesus monkeys

Male rhesus monkeys typically disperse from their groups of birth when they are between 3 and 5 years of age. Some males, however, delay dispersal from their natal groups until after they are 5 years old. The current study evaluated central monoaminergic neurotransmitter activity as a potential correlate of such “delayed” dispersal among 54 randomly selected adolescent and adult male rhesus monkeys (Macaca mulatta) captured on Cayo Santiago during an annual trapping season. Specifically, cerebrospinal fluid (CSF) concentrations of 5-hydroxyindoleacetic acid (5-HIAA, a serotonin metabolite), 3-methoxy-4-hydroxyphenylglycol (MHPG, a norepinephrine metabolite), and homovanillic acid (HVA, a dopamine metabolite) were compared in monkeys 60 months of age or more that had either dispersed (n = 33) or were still in their natal groups (n = 5). The monkeys still in their natal groups had higher CSF concentrations of both 5-HIAA and HVA (but not MHPG) than did the animals that had emigrated (Ps < 0.05). Subsequent analysis indicated that only 5-HIAA independently differentiated dispersing monkeys from delayed dispensers. Of monkeys less than 60 months of age (n = 16), only two had dispersed from their natal groups; in this age class, there were no significant differences between dispersing and natal individuals in any CSF monoaminergic metabolite (all Ps = NS). Finally, there was no difference in the CSF 5-HIAA concentrations of the five delayed dispersers and those of younger animals (P = NS), suggesting a failure to experience the frequently reported adolescent decline in serotonergic activity. In contrast, the CSF 5-HIAA concentrations of the dispersing animals were lower than those of the younger animals (P < 0.05), consistent with either an agerelated decline or an effect of dispersal per se. © 1995 Wiley-Liss, Inc.     

Behavioral responses of unrelated adult male rhesus monkeys familiarized and paired for the purpose of environmental enrichment

An attempt was made to pair ten unrelated, adult male rhesus monkeys that had been kept in single cages for several years. Potential companions were first given the opportunity to establish clear-cut rank relationships (unidirectional fear-grinning and/or withdrawing) during a 5-day period of noncontact familiarization. Only then were they paired in a different double cage. Rank relationships were confirmed within the first 6 minutes after pairing without the occurrence of any biting and fighting. A total of four physical aggressions (slapping) were observed in all five dyads during 5 hours of observations on the first 5 days after pairing. It was concluded that the establishment of clear-cut rank relationships prior to pairing was instrumental in this extremely low incidence of aggression.     

Dietary Myoinositol Results in Lower Urine Glucose and in Lower Postprandial Plasma Glucose in Obese Insulin Resistant Rhesus Monkeys.

In a previous study, D-chiroinositol added to a meal (0.5 g/kg) resulted in significantly lower postprandial plasma glucose concentrations without an increase in insulin concentrations in obese insulin-resistant monkeys. The present report describes the effects of another isomer of inositol, myoinositol, on postprandial plasma glucose and insulin concentrations and on urine glucose concentrations in 6 similarly insulin-resistant monkeys. The three 5 day study periods included a control period (liquid diet ad libitum) and 2 experimental periods (liquid diet ad libitum with either 1.5 g/kg/day myoinositol or D-chiroinositol added). Twenty-four hour urine samples were collected during each 5 day period. On the sixth day of each period the monkeys were anesthetized 110 min after completing either the control meal (15 ml/kg) or the experimental meals (1.5 g/kg myoinositol or D-chiroinositol) and plasma samples were obtained at 120, 150,180, 210, 240, 270 and 300 min. The plasma glucose concentration was lower after the meal with myoinositol compared to the control meal at 120, 150 and 180 min (p's<0.05). The plasma insulin concentration was lower after the meal with myoinositol compared to the control meal at 150 and 180 min (p's<0.05). In addition, 24 hour urine glucose concentrations were lower during the myoinositol diet compared to the control diet (p<0.001). The plasma glucose concentration was lower after the meal with D-chiroinositol compared to the control meal at 150, 240, 270 and 300 min (p's≥0.05). In obese insulin-resistant monkeys, myoinositol added to the diet lowers urine glucose concentrations and both myoinositol and D-chiroinositol added to a meal lower postprandial plasma glucose concentrations without increasing postprandial insulin concentrations. Therefore, myoinositol, like D-chiroinositol, may be a useful agent for reducing meal-induced hyperglycemia without inducing hyperinsulinemia in insulin-resistant subjects.     

一种改进的阴茎电刺激采精法和猕猴藏酋猴及熊猴的采精及其精液特征的初步研究

本文报道了一种改进的阴茎电刺激采精法,用脱脂棉和铝箔作为电极,以避免直接用金属电极可能对阴茎的损伤,并运用这一方法对猕猴（Ｍａｃａｃａｍｕｌａｔｔａ）、藏酋猴（Ｍ．ｔｈｉｂｅｔａｎａ）和熊猴（Ｍ．ａｓｓａｍｅｎｓｉｓ）进行了电刺激采精及其精液特征研究。电刺激采精模式为连续刺激和间断刺激方式。在采精过程中没有发生阴茎损伤。对初次接受电刺激采精的动物以间断刺激模式效果较好。猕猴、藏酋猴和熊猴的射精体积分别为２．０±０．１、６．３±１．１和３．２±０．６ｍｌ;液化体积分别为０．７±０．６、２．１±０．４和１．７±０．３ｍｌ;精子浓度分别为１２．６±１．２×１０~８、４５．６±５．６×１０~８和１１．５±０．９×１０~８／ｍｌ。３种动物精液的液化率分别为：猕猴３６．２±０．９％,藏酋猴３４．０±１．４％;熊猴５１．８±１．２％。３种动物的精子总数与射精体积和凝块体积没有相关性（ｒ~２＝０．０７９;０．０１６;０．０９４和ｒ~２＝０．０６４;０．０２０;０．０７２）。上述结果表明：１）改进的阴茎电刺激采精法适用于猕猴,特别是阴茎表面较为粗糙的藏酋猴和熊猴;２）藏酋猴的射精体积和精子总数是迄今已报道的非人灵长类中最大的,可能