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This paper examined the association between grip type, hand use, and fingerprint patterns in a sample of captive chimpanzees. Grip type for simple reaching was assessed for the left and right hand and classified as thumb-index, middle-index, or single-digit responses. Fingerprint patterns were characterized as whorls, loops, or arches on each finger. The results indicated that chimpanzees exhibit significantly more thumb-index responses for the right compared to the left hand. In addition, thumb-index responses were more prevalent for subjects that had a whorl compared to a loop or arch on their thumb. The results suggest that fingerprint patterns are associated with individual differences in grasping type in chimpanzees as well as some variation in hand use.

In 1997, we began to assess the genetic variability and the potential conservation risk of the increasing human impact on the howling monkeys of Ometepe Island in southern Nicaragua. We captured and collected blood from 29 howling monkeys (Alouatta palliata) at two geographically separated localities in a single area (San Ramon) on Ometepe Island, Nicaragua, during two field seasons. We also collected blood from a community of 10 Alouatta pigra in the Scotland Half Moon region in Belize. We extracted DNA from the blood and analyzed 12 microsatellite loci. The number of alleles per locus (allele variability) is less for most (but not all) loci in the Ometepe versus the Belize sample and less than earlier published reports of mixed geographic samples from Central America. The results are noteworthy in that both the Ometepe Island sample and the Belize sample possess greater allelic heterozygosity for most loci than reported in other Central American howling monkey populations. The Ometepe and Belize groups also demonstrated differences in allele frequencies at each geographic location. There appeared to be adequate gene flow in both locations despite extensive fragmentation due to agriculture and other human land usage.

Perineal swelling during pregnancy in captive common chimpanzees (Pan troglodytes) was studied to examine if the swelling pattern is consistent with known fluctuations in estrogens and progesterone and to test associations between reduced swelling and pathological outcome. Analyses of swelling during 107 pregnancies with a variety of outcomes revealed that a majority of swelling patterns fit an endocrinological model closely, but that a small minority (6.6%) from low parity mothers had exaggerated and extended swelling, suggesting an altered sensitivity of the swelling to steroids. Disregarding this extreme minority, swelling was found to be significantly reduced from that of normal outcome pregnancies for sub-groups with varying degrees of maternal incompetence, neonatal fatality, and stillbirth. This reduction was most marked for pregnancies in nursery-reared mothers. Given the validity of the correspondence between swelling patterns and steroid concentrations, lower estrogen concentrations are implicated in the etiology of the puerperal pathologies seen. That steroid hormone concentrations during pregnancy may influence maternal behavior in apes provides a clue to the etiology of post-partum depression in women.

Size and form of the external penis, or pars libera, was documented for 17 living orangutans ( Pongo pygmaeus ) of varying age. The pars libera was much longer than previously represented in comparative analyses, and most were filiform (as in Pan ), but form and color was variable: 1) a partially or completely demarcated glans-like structure (as in Gorilla ) was present in a few subjects; 2) epidermal specializations of the pars distalis had either a hinge-like or flap-like form and might be homologous to the keratinized spines seen in other species; 3) the pars libera was not a uniform pink in all cases as the pars medialis often was black or purple. Comparisons of the length of the pars libera relative to size of females across the great apes and humans ( Homo ) reveals that the pars libera of Pan is much longer than that of Homo which is longer than but similar to that of Pongo , which is much longer than that of Gorilla . Relative to size of males, however, Homo have pars libera that are twice as long as those of Pongo . Similarities and differences in penile structure between Pongo , which has a non-gregarious (dispersed) mating system, and Pan (with a multimale system) may be understood in relation to the form of the female genitalia; this is consistent with the notion that sexual selection by female choice may be an ultimate cause of sexual characteristics of hominoids. Hypotheses about causation, however, require scrutiny with a more complete dataset from living subjects.

We investigated the sexual behavior of 13 chimpanzees (Pan troglodytes) in 2 types of pair test in order to clarify the interaction of social variables with female hormonal state. The frequency of copulation in tests in which the partners were freely accessible to each other was related to the male's dominance over the female; copulation was less frequent and was related to social compatibility in tests in which the female controlled access. Copulation was related to female hormonal state in both types of test. The results demonstrate (a) an association between female hormonal state and sexual activity of chimpanzees, (b) the influence of social relationships on sexual interactions, and (c) the importance of focusing on female sexual behavior before copulation, rather than copulation per se, in research on sexual arousability of female primates.

Behavioral and physiological effects of a combined oral contraceptive (OC) were studied in chimpanzees for comparative purposes related to (i) the ambiguity surrounding the effects of OCs on the sexuality of humans, (ii) the close biological relationship between chimpanzees and humans, especially with respect to endogenous sex hormones and sexual behavior, and (iii) the relatively greater behavioral sensitivity of the chimpanzee to changes in sex hormone levels such as those that accompany the use of OCs. Two different types of pair tests and detailed behavioral assessments were used to differentiate the hormonal effects of female behavior from social effects imposed by the male. Anogenital swelling and copulation were reduced during OC cycles, but the effect of the OC on copulation was directly related to the social and sexual relationship of the pair during natural cycles. The more compatible and more frequently copulating pairs in the natural cycles continued to copulate during the OC cycles, albeit at reduced rates, whereas the less compatible and less frequently copulating pairs ceased copulating altogether when the female received the OC. There was no independent effect of the OC on ejaculation per se. Both male and female sexual initiative were reduced in the OC cycles, but female responsiveness to male sexual solicitations and direct copulatory attempts were not affected. Data indicate that despite generally adverse effects of the OC on certain physiological and behavioral dimensions of sexuality, social factors ultimately determined the degree of response to the OC. The research on the chimpanzee serves two purposes relevant to women who use OCs: (i) it identifies three specific areas affected adversely by OCs (female genital tissues, sexual proceptivity, and sexual attractivity) and (ii) it suggests that the individuals who are most vulnerable to such effects of OCs are those with unusually high sensitivity to hormones and those with relatively low sexual activity or preexisting problems in sexual adjustment.

The relationship between sex hormone concentrations and female genital swelling during the menstrual cycle in the monogamous gibbon was comparable with that of polygamous female primates, such as the chimpanzee, which live in multimale groups and have larger swellings. The data, therefore, support the hypothesis proposed by C. R. Carpenter more than 50 years ago, that the gibbon's genital swelling, like that of other female primates, reflects basic physiological processes associated with progress of the menstrual cycle. Genital swelling increased during the follicular phase with increasing concentrations of oestradiol and oestrone glucuronide, reached maximal swelling in association with the mid-cycle peaks in the oestrogens and LH and began detumescence with the initial increases in progesterone during the luteal phase. The data also suggest that the menstrual cycle of the gibbon is shorter than previously reported, since cycles of 19–22 days exhibited hormone patterns that are consistent with ovulation. The genital swelling of the female gibbon is a useful marker for monitoring progress of the menstrual cycle and the presumptive time of ovulation. Journal of Endocrinology (1993) 136, 447–455

Few data are available for assessing the relative testicle size of orang-utans, Pongo pygmaeus, so measures were obtained for 31 individuals of varying age. It was shown that the volume of the testicles, calculated from in situ measures of testicle length and breadth, closely approximates testicle weight when multiplied by the specific gravity of solid tissue. Growth curves for body weight and data published for wild specimens were evaluated to obtain the weight most characteristic of male Pongo, and the ratio of testicle weight to body weight was calculated. The mean ratio for individuals with fully adult stature is 0.034, similar to but smaller than that of humans at about 0.050, and larger than the ratios reported for 5 gorillas at 0.013. The testicles mature faster than the body, however, so the mean ratio for young adult orang-utans is about 0.056 and resembles the ratio for humans more closely than the full adults. The differences between the ratios for a monogamous gibbon species, orang-utans, and humans is accounted for when testicle size relative to the weight of the female is considered. This is consistent with a sperm dilution effect produced by variation in the size of the female reproductive tract. The small relative testicle size of the gorilla is anomalous and requires verification as does the application of female size to scale the testicles. © 1993 Wiley-Liss, Inc.

Cyclical changes in the vulvae of five adult lar gibbons (Hylobates [H.] lar) were studied and compared with those of eight lowland gorillas. The results reveal that the gibbons have relatively conspicuous and specialized sexual swellings that alter shape and appearance during the ovarian cycle. At maximum extent, the genital swellings of gorillas are relatively and absolutely smaller than those of gibbons, and lack the distinctive coloration seen in the genital swellings of the smaller apes. We conclude that the female gibbon's sexual swelling is a far more conspicuous and effective signal of estrus status than that of the gorilla, and that this is not explicable in terms of allometry. Previous investigators have pointed to one-male mating systems, monogamous pair-bonding, or an arboreal habitat as reasons that some primates should have less conspicuous signals of estrus than others. Our findings for the gibbon are the reverse of these predictions, and indicate that sexual selection other than by intermale competition for estrous females is implicated in the ultimate causation of the gibbon's swelling. The adaptive value and significance of the female gibbon's sexual signals remain unclear, however.

Genetic mechanisms have been proposed to explain the pervasive representation of right-handedness in humans, whereas random, nongenetic factors have been posited to explain the lack of population-level right-handedness in nonhuman primates. We report evidence that hand preferences in chimpanzees are heritable, even among related individuals raised in different environments. Furthermore, we report that the degree of heritability is modified by factors associated with developmental instability, notably, offspring parity. The data are interpreted to reconcile both genetic models for handedness and hypotheses suggesting that developmental instability influences variation in handedness.

This paper examines the relationship between parity, pregnancy outcome, and handedness in a sample of captive chimpanzees (Pan troglodytes). The relation between parity, maternal age and positive or negative pregnancy outcome was assessed from life history data for 536 chimpanzees housed at the Yerkes Regional Primate Research Center. The incidences of negative pregnancy outcome (notably spontaneous abortions and stillbirths) were significantly higher in parities of 8 or higher compared to all other parities. In a sub-sample of 165 chimpanzees, the relation between parity, maternal age and handedness was assessed to determine whether left handedness may serve as a marker of prenatal pathology. These analyses indicated that left-handedness was more prevalent in 1st and 8 or higher parities compared to parities between 2 and 7, respectively. Possible prenatal hormonal and periparturitional factors are discussed as possible mechanisms for the observed findings.

Approximately 85% to 90% of humans report themselves as being right-handed (Annett, 1985; Porac & Coren, 1981). Explaining the pervasive degree of right-handedness in the human species has fostered considerable theoretical debate and empirical investigation. Genetic, biological, and environmental models have been proposed to explain this population-level right-handedness, each with varying amounts of empirical support (Annett, 1999; Collins, 1985; Corballis, 1997; Laland, Kumm, Van Horn, & Feldman, 1995; Previc, 1991; Provins, 1997; Trevarthen, 1996). Equally important are theoretical models proposed to explain the occurrences of left-handedness or non-right-handedness in human populations. That genetic factors may play a role is supported by the observation that approximately 70% of individuals born to two left-handed parents are right-handed, which is significantly lower than the proportion of fight-handed individuals born to two right-handed parents (McGee & Cozad, 1980; McManus & Bryden, 1992). Genetic explanations account for only part of the variance, however, leaving error or other factors to explain the remaining variability. Rather than emphasize genetic factors, others have suggested that both pre- and postnatal environmental factors play a role in determining non-right-handedness. Such factors include but are not limited to birth season, birth order, maternal age, and prenatal hormones. In these models, right-handedness is perceived as being the normative path of development, and therefore non-right-handedness reflects a deviation from normal development that is due to pathological factors (see Satz, Soper, & Orsini, 1988). Of specific interest to this study are the reports focusing on the effect of birth order on hand preference in humans. Bakan and colleagues (Bakan, 1971; Bakan, Dibb, & Reed, 1973) first reported and theorized about the relationship between birth order and hand preference in humans. Bakan (1971) reported that there was a higher percentage of left-handedness in first- and latter-born offspring (defined as more than 4 birth orders) and postulated that the effects were due to birth trauma experienced by offspring born to primiparous or older women. Bakan (1971) proposed that birth trauma is more likely in women who are giving birth for the first time or for older women who present a higher risk group for prenatal insult. Researchers who have attempted to replicate Bakan's early reports have come up with equivocal results, with most of the discrepancies between studies centering on the issue of sampling procedures (Annett & Ockwell, 1980; Badian, 1983; Bakan, 1977, 1978; Coren & Porac, 1980; Dellatolas, Curt, & Lellouch, 1991; Hicks, Evans, & Pellegrini, 1978; McKeever, Suter, & Rich, 1995; Nachshon & Denno, 1986; Perelle & Ehrman, 1994; Schwartz, 1977; Searleman, Porac, & Coren, 1989; Tan & Nettleton, 1980). Specifically, there are significant relationships between socioeconomic status (SES), rate of pregnancy, and birth complications that are likely due to factors associated with maternal lifestyle (such as nutritional habits, medical care, etc.). For example, less well-off individuals typically have more offspring, poorer prenatal care, poorer nutritional habits, and more birth complications compared with well-off individuals (Birch & Gussow, 1970). According to Bakan (1977), it is critical to have equal representation of subjects from various SES backgrounds to control for these extraneous variables, which he argues has not been the case in studies in which his findings were not replicated (e.g., Hubbard, 1971; Schwartz, 1977). The purpose of this study was to examine the effect of birth order on hand preference in a sample of captive chimpanzees. Theoretically, the effect of birth order on hand preference in captive chimpanzees (as well as other primates) is of interest because the hypothesized SES confounding variables debated in the literature on humans would not be potential confounds in a sample of captive chimpanzees (or other primates) where the environment and access to resources are more uniform. In other words, the methodological issue of whether there was adequate sampling of subjects to control for SES variables would never be considered in a sample of nonhuman primates. Presumably, any significant effect of birth order on hand preference would be solely due to biological factors associated with parity or maternal age or both. Pragmatically, chimpanzees offer a good model for testing the effect of birth order on hand preference because they are biologically and genetically very similar to humans, but there is no socioeconomic variation in a captive colony. Additionally, chimpanzees have been reported to exhibit population-level right-handedness, and therefore non-right-handedness can be viewed as reflecting deviation from a species-typical norm (Hopkins, 1996; but see McGrew & Marchant, 1997). Finally, chimpanzees have a relatively long gestation period (approximately 230 days), exhibit stages of prenatal development comparable to humans, display periparturitional behaviors that resemble many of those observed in humans (Nissen & Yerkes, 1943), and exhibit a wide range of similar puerperal pathologies (Dahl, 1999).

Assisted reproduction with great apes will be considered here as facilitated reproduction in order to include the experimental and clinical approaches related to fertility evaluation (including correction of infertility) and optimization of natural fertilization as well as the more invasive methods of reproduction enhancement associated with artificial insemination (AI), in vitro fertilization (IVF), gamete storage, and surgical intervention. Those techniques are only now becoming effectively applied to the great apes. In addition, the existing data pertaining to early termination of pregnancy, obstetrical intervention, and neonatal and infant mortality can provide valuable guidance regarding the development of strategies for assisted reproduction. Such strategies are, therefore, to be directed to initiation of pregnancy, maintenance of pregnancy, reduction of neonatal loss, provision of means for “normal” postnatal development, and arrangement for social conditions conducive to subsequent natural breeding and rearing of offspring.

A combined oral contraceptive consisting of ethinyl estradiol (EE2) in three dosages (50, 100, and 400 micrograms) and norethindrone (0.5 mg) was given to female chimpanzees to determine the effect on endogenous sex hormone levels and anogenital swelling. Serum levels of EE2 increased with increasing dosages of EE2, estradiol decreased, and luteinizing hormone, progesterone and testosterone were maintained at approximately midfollicular phase levels. Urinary levels of EE2 glucuronide increased with the increasing dosages of EE2, whereas estrone and pregnanediol glucuronide were essentially undetectable. The cyclic increase in female anogenital swelling was abolished when the norethindrone was combined with 50 micrograms of EE2 and relatively constant and low levels of swelling were recorded. Relatively constant but successively higher levels of swelling were recorded when the norethindrone was combined with the higher dosages of EE2. These effects of oral contraceptives on female genital tissues are relevant to our laboratory studies of sexual behavior in chimpanzees given oral contraceptives and could also have implications for women taking oral contraceptives.

The external genitalia of one perimenarcheal and five adult female white handed-gibbons (Hylobates (H.) lar) were examined to clarify their gross anatomy. It was found that the vulval structures were complex and exhibited inter-individual variation in arrangement. This complexity appears to result from an ontogenetic process by which the tissues of the vaginal rim (the labia minora) bud-off and extrude extensions toward the vagina immediately prior and subsequent to menarche. Two of these lobular structures surround the urethral meatus and constitute a urethral eminence. The tissues of the vulva, excluding the clitoris with associated prepuce and frenulum and vestigial labia majora, undergo cycles of tumescence and detumescence during intermenstrual intervals. The complex form of the external genitalia and the presence of a swelling cycle are unusual for a monogamous species, are contrary to current applications of sexual selection theory, and raise questions about the significance of mate choice in hominoid evolution.

Females of both species of chimpanzee, Pan troglodytes and P. paniscus, exhibit conspicuous anogenital sex swellings that are useful external markers for assessing ovarian cyclicity. A new, quantitative method for describing these swelling cycles was refined during laboratory studies of four P. paniscus and nine P. troglodytes and was used to analyze variability in swelling patterns. Clear-cut anatomical changes of the perineum were found to have both interindividual and interspecific reliability. The swollen phase of the cycle was defined as the period when the medial surfaces of the labia minora are pressed against each other so the aperture leading to the vagina appears as a slit (labial occlusion). When defined with this precision, comparisons within and between the species revealed two types of cycle for both species; swollen phases of P. paniscus were about 24 or 39 days in duration, on average, whereas those of P. troglodytes were about 14 or 18 days. Urine samples from the P. troglodytes were collected and analyzed for luteinizing hormone (LH) (34 cycles), estrone glucuronide (E1G), and pregnanediol-3-glucuronide (PdG) (18 cycles). When the two types of cycle were separated in analysis, it was found that the day when labial occlusion occurred served as a predictor of the preovulatory LH peak in the cycles with a long swollen phase. Levels of E1G correlated closely with swelling scores in multiparous females regardless of phase lengths, suggesting that the new swelling scores are a reliable indicator of E1G excretion in multipara. Cycles with long swollen phases had relatively high levels of PdG during the luteal phase, whereas cycles with short swollen phases had relatively low levels of PdG and a shorter luteal phase. The marker of labial occlusion and the duration of the preswollen phase defined by the marker appear to be potentially useful in studies of reproduction in Pan, for monitoring female fertility, and in artificial insemination procedures. If it is confirmed that swelling pattern predicts progesterone levels during the luteal phase, it would make interventions possible in the case of low levels so that a potential pregnancy could be maintained to term.

The perineal swelling cycle and intermenstrual interval of pygmy chimpanzees ( Pan paniscus ) have not been well documented, and it is not clear that cither characteristic differs from those of common chimpanzees ( P. troglodytes ). Consequently, adult females in a breeding colony of P. paniscus were monitored for menses over four and one-half years, and the perineal swelling cycles were detailed for half that period. To test the hypothesis that there are no differences between the species of Pan in reproductive cyclicity of captive females, the results were compared with data collected from 22 captive P. troglodytes over an eight-year period by W. C. Young and R. M. Yerkes. The average duration of the intermenstrual interval of 49 days ( n =23; S.E.=2·9) for adult P. paniscus differed from an average of 34–36 days for adult P. troglodytes , but was similar to the 50-day interval of adolescent P. troglodytes . The pattern of the swelling cycle was different from any cycles exhibited by adult or adolescent P. troglodytes ; following the first sign of detumescence, the swelling retained significant tumescence for an average of 12 days. By altering slightly the definitions of each swelling phase, the durations of the phases subsequent to abrupt detumescence were found to resemble either the adult or the adolescent postswelling phases of P. troglodytes . Adult female P. paniscus exhibit marked swelling for approximately 75% of the intermenstrual interval in comparison to about 50% or less of the intervals exhibited by P. troglodytes . It follows that female P. paniscus are sexually attractive to males for a greater portion of the time, which may contribute to the differences in social organization reported for the two species in the wild. Aspects of the similarity in cyclicity between adult P. paniscus and adolescent P. troglodytes are congruous with interspecific morphometric analyses and the comparative anatomy of the female external genitalia, suggesting that some characteristics of P. paniscus may be neotenous with respect to P. troglodytes but not all distinctions can be accounted for by neoteny alone. The structural resemblance between the sexual swelling of female chimpanzees and the buttocks of human females suggests that female Australopithecinae may have been continuously attractive to males.

It is proposed that differences in fertility between naturally living great apes (Pongidae, Primates) and captive individuals are caused, in part, by an absence of naturalistic features in captive habitats. One component of probable importance in the natural habitat of pongids is temporal complexity. This is indicated by description of climate fluctuations over the pongid geographic range. In this paper the introduction of temporal complexity to captive habitats is proposed as an important modification that should contribute substantially to improved fertility of the captive great ape, in addition to greater utilization by researchers. Improvements of this sort are not economically feasible, however, if traditional building designs are utilized. Adoption of an enlightened perspective using appropriate, alternative technologies is a requirement for cost effective improvements. A first priority in such an approach is a revision of attitudes toward appropriate designs, and a collaboration between agencies responsible for establishing building costs and those for setting maintenance costs.

Tattersall, Ian. The Primates of Madagascar. New York: Columbia University Press, 1982. xiv + 382 pp. including photographs, maps, references, index. $40.00 cloth.

The external genitalia of four adult female pygmy chimpanzees (Pan paniscus) were examined during a 2-year period. It was found that the labia majora are retained in adults of this species and that, when tumescent, the labia minora effectively relocate the frenulum and clitoris so that they point anteriorly between the thighs. When detumescent, the configuration of the labia minora and clitoris resembles that of immature common chimpanzees (P. troglodytes). It is suggested that the simple, structural relocation of the clitoris from the normal condition noted in adult P. troglodytes makes possible the homosexual, intergenital rubbing observed in P. paniscus, when ventroventral juxtaposition of the individuals permits eye-to-eye contact. In addition, this change probably increases sexual stimulation of the female during heterosexual, ventroventral copulations. The possibility of intense, face-to-face sexual interactions has been achieved by P. paniscus without the evolution of bipedalism and the consequent reorientation of the genitalia seen in Homo sapiens.