Anogenital swelling in pregnant chimpanzees of Gombe National Park

American Journal of Primatology 31:89-98 (1993)

RESEARCH ARTICLES

Anogenital Swelling in Pregnant Chimpanzees of Gombe National Park

JANETTE WALLIS'.' AND JANE GOODALL' 'Gombe Stream Research Centre, Kigoma, Tanzania, East Africa; 'Department of Obstetrics and Gynecology, University of Oklahoma College of Medicine, Oklahoma City

Previous studies show that anogenital swelling patterns of pregnant chimpanzees in captivity are correlated with the female's age during pregnancy and are associated with changes in social behavior. The purpose of the present study was to investigate whether the anogenital swelling patterns of free-ranging pregnant chimpanzees resemble those reported for captive chimpanzees. We reviewed the records of 47 pregnancies experienced by 20 female chimpanzees living in Gombe National Park from 1975 to 1992. Percentage scores for swelling during each trimester and for the overall occurrence of various levels of swelling were obtained by dividing the frequency by the total number of days the subject was observed (i.e., 28 days of swelling/l65 days observation = 17.2% anogenital swelling for that pregnancy). Subjects exhibited anogenital swelling an average of 25.1% of the days observed during pregnancy, yet reached maximum only 9.4% of the time. Anogenital swelling occurred less frequently as pregnancy progressed, averaging 40.8, 27.3, and 2.7% in the first, second, and third trimesters, respectively. As seen in captive chimpanzees, young pregnant females at Gombe showed anogenital swelling more often than did older ones (r = -.65, P < .0001). These findings are consistent with reports of behavior associated with anogenital swelling (e.g., intercommunity transfer of young females exhibiting anogenital swelling). 0 1993 Wiley-Liss, Inc.

Key words: anogenital swelling, estrous swelling, genital swelling, pregnancy, female transfer, chimpanzee, Pun troglodytes

INTRODUCTION During their 36 day menstrual cycles, female chimpanzees (Pan troglodytes)

exhibit cyclical fluctuations in swelling of the anogenital skin. The period of anogenital swelling, particularly when maximal, is associated with both female- and male-initiated sexual behavior [Yerkes & Elder, 1936; Yerkes, 1939; van Lawick- Goodall, 1969; Lemmon & Allen, 1978; Nishida, 1979; Tutin & McGinnis, 1981; Wallis, 1982, 1992al. Pregnant female chimpanzees also display irregular anogenital swelling, especially during the early months of gestation [Yerkes & Elder,

Received for publication June 17, 1992; revision accepted March 4, 1993.

Address reprint requests to Janette Wallis, Ph.D., Department of Obstetrics and Gynecology, University of Oklahoma College of Medicine, P.O. Box 26901, Oklahoma City, Oklahoma, 73190.

0 1993 Wiley-Liss, Inc.

90 / Wallis and Goodall

1936; Clark & Birch, 1948; van Lawick-Goodall, 1968; Wallis, 1982; Wallis & Lemmon, 19861.

The hormonal mechanism involved in anogenital swelling during pregnancy is unclear. During regular menstrual cycles, the follicular phase is marked by an increase in swelling as estrogen levels rise and progesterone concentration remains low. In the luteal phase, a reversal of the relationship between estrogens and progesterone results in the detumescence of anogenital skin [Fish et al., 1941; Clark & Birch, 1948; Graham, 19811. During pregnancy, however, there are high concentrations of both estrogen and progesterone [Reyes et al., 1975; Faiman et al., 19811. Although i t was previously suggested that a certain ratio between these steroids may be responsible for regulating anogenital swelling in chimpanzee gestation, more recent evidence indicates the absolute level of progesterone appears to be most relevant [chimpanzees: Nadler et al., 1985; rhesus monkeys: Wilson et al., 19821.

Wallis and Lemmon [19861 investigated the incidence of anogenital swelling in captive pregnant chimpanzees. A review of the records of 16 females, through 40 pregnancies, showed that anogenital swelling occurred more often in young chimpanzees than in older ones. The study also revealed that captive pregnant chimpanzees differed significantly from cycling females in some behavioral interactions with males. The difference in behavior was evident only when the females were exhibiting anogenital swelling.

One behavioral category in which pregnant and cycling females did not differ was sexual interaction; as in menstrual cycles, anogenital swelling during chimpanzee pregnancy was associated with sexual activity [Wallis & Lemmon, 19861. These results were similar to previously published data for chimpanzee populations both in the wild [van Lawick-Goodall, 1969; Nishida, 1979; Tutin & McGin- nis, 19811 and in captivity [Tinklepaugh, 1933; Yerkes, 1939; Lemmon & Allen, 1978; Wallis, 19821.

The purpose of this study was to investigate the anogenital swelling patterns during pregnancy of the free-ranging chimpanzees of Gombe National Park and determine whether these patterns were similar to those found in the earlier study of captive chimpanzees [Wallis & Lemmon, 19861.

METHODS Study of pregnancy and pattern of anogenital swelling from the observations

of free-ranging chimpanzees is difficult. Although observations are made daily at Gombe National Park, each animal is not seen every day, resulting in missing data points. Pregnant females, in particular, frequently travel alone or in small parties, often not interacting with the days’ focal subject.

The data collected at Gombe National Park, from 1975 through 1992, yielded 47 pregnancies of well-habituated chimpanzees. Early miscarriages were omitted from this study. Therefore, these 47 pregnancies ended in live birth or a recognized near term stillbirth.

Two types of records were used for these analyses: the A records-the census of individuals visiting the feeding station, often biased toward lone travel-and B records-which involve all day observation of a focal animal, often biased toward group travel. Combined, these records provide information on all sightings of chimpanzees and note each female’s anogenital swelling status.

Using specific criteria for selection, we calculated an estimate of gestation duration and, separately, analyzed the swelling patterns of pregnant chimpanzees of Gombe.

Anogenital Swelling in Chimpanzee Pregnancy I 91

Gremlin, age 12

CONCEPTION Full Swelling

Partial

None A September, 1981 October November

A December January. 1982 February

BIRTH

/ March April May

Fig. 1. This figure represents the pattern of anogenital swelling in a nonfertile menstrual cycle, a fertile cycle, and the 231 day pregnancy of a 12-year-old free-ranging chimpanzee. Date of conception was estimated to be the last day of maximal swelling in the last “normal” cycle. Note the irregular occurrence of swelling throughout the early stages of pregnancy.

Pregnancy Duration Estimate Analysis In the pregnancy duration estimate analysis, no pregnancies were included in

which the first record of an infant gave an estimate of more than three days of age-that is, if an infant was first seen more than three days after the mother was last seen (still pregnant). In addition, when a retrospective review was made for the estimated time of conception, if the female was not seen for several days (one week or more), then that pregnancy was excluded from the duration estimate. For simplicity, the last day of maximal anogenital swelling occurring during the last normal swelling cycle (the suspected fertile cycle) was considered the day of conception [see Graham, 19821. A normal swelling cycle was characterized by a gradual increase in tumescence of the anogenital area, maintenance of full swelling for several days, then a gradual decrease in tumescence. Non-normal cycles are characterized by erratic swelling patterns (see Fig. 1). All stillbirths were omitted as there was no possibility of determining whether death was due to prematurity (shortened gestation) or some other cause. Because pregnancies followed by mul- tiple births are generally shorter than average [humans: Jones et al., 1990; captive chimpanzees: Wallis, unpublished data], we did not include the one twin birth for gestation duration analysis.

Swelling Pattern Analysis For the swelling pattern analysis, we included all pregnancies for which the

female was observed on at least 30% of the days during pregnancy (regardless of whether the exact date of birth was known). Stillbirths were included, if they fit

92 I Wallis and Goodall

the 30% criterion. The 30% observation time was distributed almost evenly throughout pregnancy.

At Gombe, the anogenital swelling level of a female chimpanzee is recorded on each day she is observed. Data are collected by two trained field assistants con- ducting the B record and one trained field assistant collecting the A record. For this analysis, the swelling level listed by at least two of these three observers was used each day. Notations for swelling are: 0 = no swelling; 1 = maximal swelling; 1/4, 1/2, 3/4 = estimated fractions of partial swelling levels. However, for the present analysis, all fractions were combined into a partial swelling category. In this way, the data are easily replicated and reliable (i.e., no swelling, full swelling, and anything in between).

The percentage scores for swelling during each trimester and for the overall occurrence of various levels of swelling were obtained by dividing the frequency of each event by the number of days the subject was observed. For example, 28 days of swelling/l65 days of observation = 17.2% anogenital swelling for that pregnancy.

A Pearson’s correlation analysis was used to determine the correlation between presence of swelling and maternal age. The exact age of many of the subjects is unknown. Subjects that were already present during the early years of data collection, which started in 1960, were assigned birth year estimates by Goodall long ago. The present study includes some females that were juveniles during those early years. Age estimates for immigrant females are made as they join the community. Because females tend to transfer during late adolescence or early adulthood, the age estimates are considered accurate to within 3 years. Age estimates are determined through assessment of the animals’ size, physical appear- ance (e.g., face and hair color; condition of dentition, skin, and genitalia), and behavior. Age estimates for this study ranged from 10 to 35 years.

During the study period, 1975-1992, the chimpanzee population at Gombe varied greatly. Normal changes caused by female transfer and natural death were complicated by the occurrence of two pneumonia epidemics which killed several reproductively active individuals in the Kasakela community. Consequently, very few subjects were represented more than twice in the present analysis. However, one female (Fifi) chose not to transfer, staying in the Kasakela community where she enjoyed great reproductive success. Five of her six pregnancies occurred during the study period and were treated in a separate analysis to determine the correlation between presence of anogenital swelling and maternal age.

Comparison of Free-Ranging and Captive Chimpanzees For certain measures in the analyses described above, a general linear model

and a Student’s t test were used to compare these results to data collected from study of captive chimpanzees [Wallis & Lemmon, 19861.

RESULTS Pregnancy Duration

There were 16 pregnancies used for the duration estimate ranging from 203- 234 days and averaging 224.3 days (SD = 8.9). Because this figure is only an estimate, we only report it here rather than compare it to the estimate from captive studies (mean = 231.5 2 14.9 [Wallis & Lemmon, 19861).

Swelling Patterns Thirty pregnancies were determined to fit the set criterion for inclusion in the

study; the females were observed on at least 30% of the days during pregnancy.

Anogenital Swelling in Chimpanzee Pregnancy / 93

TABLE I. Anogenital Swelling During Chimpanzee Pregnancy

Fetal gender

Female Male Total (n = 9) (n = 21) (n = 30)

Anogenital swelling (% of time) No swelling 74.2 75.1 74.8 Partial swelling 13.9 16.4 15.7 Maximal swelling 11.8 8.3 9.4

Incidence (%) of swelling in 1st trimester 37.7 42.2 40.8 2nd trimester 28.9 26.6 27.3 3rd trimester 4.0 2.2 2.7

There were nine female and nineteen male fetuses, with no difference in maternal age between the two classes (female: 23.7 yrs 5 3.8; male: 22.3 yrs ? 7.4; t = .55, n.s.). Table I presents the mean values determined from the analysis of swelling patterns. Gombe females exhibited anogenital swelling an average of 25.1% of the days observed during pregnancy, yet reached maximum only 9.4% of the time.

Anogenital swelling (partial and maximal) occurred less frequently as pregnancy progressed, averaging 40.8, 27.3, and 2.7% in the first, second, and third trimesters, respectively (Table I). A comparison according to fetal gender revealed no significant difference for any of these measures of swelling.

The incidence of anogenital swelling during gestation was negatively correlated with maternal age; young pregnant females a t Gombe showed anogenital swelling more often than did older ones (r = -.64, P < .0001). When analyzed by trimester, the negative relationship between anogenital swelling in pregnancy and maternal age was significant in the first and second trimesters only (see Table 11). Figure 2 illustrates the relationship between the percent of time anogenital swelling was present and maternal age (circles).

The one subject (Fifi) that contributed five pregnancies to the data set showed the same trend of negative correlation between anogenital swelling during pregnancy and maternal age (r = -.87, P < .05). Her data points are depicted as filled circles in Figure 2.

Comparison of Free-Ranging and Captive Chimpanzees Some differences were noted when results from this study were compared to

those from captive chimpanzees [Wallis & Lemmon, 19861. In the study of captive chimpanzees, some level of anogenital swelling was present much more frequently during pregnancy (captive: 41.1%; wild: 25.1%; t = 2.84, P < .006>. However, the incidence of reaching maximal swelling was not significantly different (captive, 8.7%; wild, 9.4%, t = -.29, ns.).

Swelling continued later into pregnancy in the captive group than in the wild. The second trimester value of 27.3% for wild chimpanzees was significantly lower than the value of 47.9% for the captive subjects (F = 8.17, P < .006). Similarly, third trimester values of 2.7% and 22.6% for the wild and captive groups, respectively, differed significantly (F = 11.43, P < .001).

Anogenital swelling in pregnancy was correlated with age in both the wild and captive groups and, in fact, the difference in swelling between the groups was partly attributable to an age difference as seen in a general linear model analysis controlling for age (F = 14.71, P < .0003). Analysis by offspring gender indicated


TABLE 11. Correlation (r) Between Mother's Age During Pregnancy and Incidence of Anogenital Swelling

Swelling (n = 9) (n = 21) (n = 30)

No swelling + .57 f .71*** + .64****

Female fetus Male fetus Total

Partial swelling - .47 -.67** - 63**** Maximal swelling -.61 - .43* -.42** 1st trimester - .66* - 79**** - 76**** 2nd trimester - .46 -.53* -.51** 3rd trimester -.14 - .03 - .04

*P < .05. **P i ,001. ***P < ,005. ****P i ,0001.

Percent

l o o r +

80;+* 60 + + 9 + + O -k

6 11 16 21 26 31 36 Age (yrs)

Fig. 2. The negative relationship between percent of time anogenital swelling was present during pregnancy and maternal age: o and dashed line = data from free-ranging chimpanzees; + and solid line = data from captive chimpanzees [from Wallis and Lemmon, 19861. Filled circles represent one free-ranging subject contrib- uting five pregnancies to the data set. See text for details.

that the significant relationship was present only when the mother was carrying a male fetus in both the captive and wild populations (Table 11).

Figure 2 combines the present data from free-ranging subjects with the labo- ratory results from Wallis and Lemmon [1986], highlighting the age difference between the two populations and illustrating the inverse relationship between maternal age and anogenital swelling during pregnancy for both groups.

DISCUSSION For this study we reviewed the records of free-ranging chimpanzees to deter-

mine whether the incidence of anogenital swelling during pregnancy showed a similar pattern to that seen in captive chimpanzees. The primary difference seen between the two populations was the higher incidence of swelling in the captive


group. Ease in making daily observations in captivity may result in more frequent recording of anogenital swellings. However, recent data indicate that pregnant females at Gombe tend to travel in larger groups on days when they exhibit anogenital swelling [Wallis & Matama, unpublished data], which increases the likelihood that they would appear in the B record observations (used in this analysis).

There was a large difference in age of the two groups (wild = 22.8 years: captive = 13.6 years: F = 45.28, P < .0001), as chimpanzees mature much earlier in captivity. Because gestation-related swelling is negatively correlated with maternal age, we would expect the disparity in overall swelling incidence.

Another difference between the two populations was the tendency for anogenital swelling to continue later in pregnancy in the captive chimpanzees compared to those living in the wild. Several factors which may affect anogenital swelling differ between the two populations. Seasonal changes in diet and rainfall which affect wild chimpanzees are not experienced by most captive animals. In this comparison, the captive population was continually housed with the same cagemates (female and male) throughout the study, whereas pregnant chimpanzees at Gombe tend to travel on their own or with dependent offspring (i.e., not always in the company of other adults). Previous research indicates an influence of social contact on chimpanzee reproductive cyclicity [Wallis, 1985, 1992bl as well as seasonal influence on timing of anogenital swelling in the wild [Wallis, 1992b, 19931. Any or all of these factors may play a role in determining the pattern of anogenital swelling during chimpanzee pregnancy.

Significance of Anogenital Swelling During Chimpanzee Pregnancy Because the basic results obtained in this study were similar to those obtained

from study of the captive animals, to a large extent a discussion of the mechanisms involved in gestation-related swelling remains the same as those mentioned in the previous study. Therefore, much of the following is based on a discussion first put forward by Wallis and Lemmon [1986].

In this study, pregnant chimpanzees exhibited some degree of anogenital swelling on an average of 25.1% of gestation days, but displayed maximal swelling for an average of only 9.4% of the time. As noted by Wallis and Lemmon [1986] although this is a small percentage, it may be important over the course of a female chimpanzee’s life. A wild female chimpanzee is reproductively active for an estimated 26-32 years [Tutin, 19801. During that time, she may have an estimated seven pregnancies, resulting in as many as five viable offspring [Tutin, 19801. The median number of births in Tutin’s analysis was three, with two offspring surviv- ing to reproductive age. Similar results were obtained from the Mahale Mountains data, where a median of two offspring per female survived to adolescence [Nishida et al., 19901.

During the time of adolescent infertility, from menarche to the first conception, a female chimpanzee experiences an average of 19 cycles with an average of 4.5 cycles between successive conceptions [Tutin, 19801. With an estimated seven pregnancies, therefore, a female chimpanzee may exhibit approximately 46 nonpregnant cycles in a lifetime. Tutin estimated that a female chimpanzee is maxi- mally tumescent for only 3.8%, or 414 days, of about 30 years of reproductive life. Therefore, what appears as a small percentage of anogenital swelling found in this study of pregnant chimpanzees in fact adds a sizable increase in the frequency of maximal swelling exhibited in the life of a female chimpanzee (7 pregnancies x 9.4% of 224.3 days’ gestation = 147.6 days). In other words, more than 25% of the total incidence of maximal anogenital swelling occurs when the female is preg-


nant, emphasizing the importance of the phenomenon of gestation-related anogenital swelling.

Wallis and Lemmon [ 19861 proposed three selective advantages for anogenital swelling in pregnancy:

1. Anogenital swelling during regular menstrual cycles increases social status in the community, which may lead to the benefits of group security, increased social grooming, and acquisition of shared food. Any benefits gained by cycling females may also benefit pregnant females exhibiting anogenital swelling.

2. Anogenital swelling increases a pregnant female’s sexual attractivity, thus establishing a recent sexual history with males of the community. This may serve to decrease the likelihood of infanticide by males and increase male protection toward the female and her offspring.

3. Anogenital swelling acts as a passport for safe intergroup transfer, thus permitting an increase in genetic diversity by allowing free movement between natal and neighboring communities for both nonpregnant and pregnant females.

The behavioral data supporting these suggestions have been published else- where [see Pusey, 1980; Tutin, 1980; Goodall, 1986; Wallis & Lemmon, 19861. The present study did not include behavioral data, but did confirm one factor significant to the third proposed advantage, that is, the relationship between gestation- related anogenital swelling and maternal age.

Unlike males, female chimpanzees may transfer from their natal community. Female transfer occurs more often at Mahale than at Gombe [Goodall, 1986; Nishida et al., 19901. Although the causative factors involved in female transfer are not well understood, females are reported to transfer successfully only when exhibiting anogenital swelling [Kawanaka & Nishida, 1974; Pusey, 19791. In fact, detumescent females attempting to enter a group may be attacked, often fatally [Goodall et al., 1979; Nishida & Hiraiwa-Hasegawa, 19851. Moreover, it is usually the young females that transfer and some chimpanzees have been known to transfer while pregnant (with an anogenital swelling) [Pusey, 1980; Goodall, 1983; Nishida et al., 19851. The data in this study, indicating that young pregnant females exhibit a higher frequency of swelling during pregnancy, replicate the results from the study of captive chimpanzees [Wallis & Lemmon, 19861 and sug- gest that the presence of swelling and ability for transfer may have a physiological component facilitating selection for young female transfer.

CONCLUSIONS

1. The incidence of anogenital swelling during pregnancy in chimpanzees de- creased as gestation progressed.

2. Anogenital swelling during chimpanzee pregnancy was negatively correlated with maternal age, consistent with these previously published observations from the field: anogenital swelling facilitates safe intergroup transfer of females; females may transfer while pregnant; it is the young females that are most often observed to transfer.

ACKNOWLEDGMENTS This is an updated version of a paper presented for the American Society of

Primatologists, Davis, CA, 1990. The study was supported by NSF grant BNS 8908572.

We thank the field assistants of Gombe Stream Research Centre and the per- sonnel of Tanzania National Parks. We especially wish to acknowledge the hard


work of our friends and colleagues, Daudi Mussa Gilagiza and Msafiri Katoto. This paper is dedicated to their memory.

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Anogenital swelling in pregnant chimpanzees of Gombe National Park