AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 61:103-110(1983) Consequences of First Pregnancy in Rhesus Monkeys MARK E . WILSON, MARGARET L. WALKER, AND THOMAS P. GORDON Yerkes Regional Primate Research Center of Emory University, Atlanta, Georgia 30322 KEY WORDS Pregnancy, Reproductive Outcome, Parity, Rhesus Monkey ABSTRACT Female primates have been thought to be reproductively disadvantaged during their early reproductive years. In order to assess the effects of first pregnancy on a female’s subsequent reproductive activity, the breeding records of female rhesus monkeys (Macaca mulatta) living in provisioned, outdoorhoused, social groups were examined with respect t o age of sexual maturity. Of the 78 colony-born females contributing to the analysis, 20.5% had their first parturition a t 36 months of age. The majority of females, 73.1%,had first parturition a t 48 months; 6.4%did so at 5 years of age. Ofthe early-maturing females, 75% were from high-ranking matriarchies. But high social rank did not guarantee early first parturition, as 55.6% of the females from high-ranking matriarchies had first birth at 48 months. An examination of outcomes of successive pregnancies revealed that both early- and typical-maturing females experienced a significant decline in live births, owing to a significant increase in sterile years, for the reproductive year following a successful first parturition. This decline was even more pronounced for early-maturing females. The frequency of birth tragedies remained constant throughout the second and succeeding pregnancies. Thus, the capacity to conceive was reduced for some females in the reproductive year following their first pregnancy. Those females that did conceive in the year following a successful first pregnancy had a significantly longer interbirth interval between their first and second parturitions than between subsequent parturitions. Sex of offspring at first parturition did not influence reproductive outcome in the following year. The nutritional costs of lactation associated with a successful first pregnancy may preclude or delay ovulation the following year, and this effect may be greater for young females that are still in a growth phase at first pregnancy. Although these early-maturing females had proportionally fewer live births during their second reproductive year, they were equal to their age-mates when compared on the basis of offspring produced by a female at any given age. In addition, since early-maturing females have offspring entering the breeding pool a full year earlier, they may not necessarily be reproductively disadvantaged. The attainment of sexual maturity in female their first parturition at 4 years of age, some rhesus monkeys, or primates in general, re- begin reproductive activity 1 year earlier, comquires that they must have gained both a phys- pleting their first pregnancy by 3 years of age iological and behavioral capacity for successful (Drickamer, 1974). The relative costs of the reproduction. Females must have the ability advancement in sexual maturity for these feto withstand the nutritional demands of preg- males may be greater, thus possibly affecting nancy and lactation and must be behaviorally their subsequent reproductive activity. Alresponsive to the growing infant during the though studies of nonhuman primates have inlong period of maternal dependence characteristic of primate species. Although female rheReceived October 25, 1982; accepted January 6, 1983 sus monkeys (Macaca mulatta) typically have h~ 1983 ALAN R. LISS, INC 104 M.E. WILSON, M.L. WALKER, AND T.P. GORDON dicated that females may experience more stillborns and neonatal deaths a t their first pregnancy than multiparous females (Wilson et al., 1978; Hird et al., 19751, a significant number of females are nonetheless successful at first parturition (Wilson et al., 1978). Few studies have examined the consequences of a successful first pregnancy on future reproductive outcome regardless of the age a t maturity. Previous work has suggested that primiparous, nonhuman primate females may be more protective of their infants than multiparous females (Mitchell et al., 1966; Seay, 1966). A recent analysis of baboon mothers indicates that females that spend a large proportion of time in contact with their infants have a longer interbirth interval than less restrictive mothers (Altmann et al., 19781, thus suggesting that the behavior of the primiparous mother may influence her interbirth interval. It is not known if this protective behavior of primiparous females is reflected in more nursing by the infant, but work with humans has indicated that prolonged lactation does indeed delay the resumption of ovulation following parturition (Knodel, 1977). Furthermore, an analysis of the seasonally breeding bonnet macaque (Macaca radiata) suggests that the second pregnancy is more likely to be successful if primiparous females skip the year following their first pregnancy (Small and Rodman, 1981). It is not known whether a failure to ovulate and conceive or a birth tragedy differentially contributes to this apparent reproductive deficit for bonnet macaques in the year following a successful first pregnancy. In order to assess the effects of the first pregnancy on a female’s subsequent reproductive success, the breeding record of female rhesus monkeys living in provisioned, outdoor-housed social groups was examined with respect t o age at sexual maturity. Since rhesus monkeys in this environment are seasonal breeders (Gordon, 1981), as they are in the wild (Neville, 19681, a failure to reproduce can be costly for a female, since conception is only possible for less than 6 months out of the year. The present analysis, thus, compared the outcome of subsequent reproductive years following a successful first pregnancy for early maturing females and their age-mates. METHODS Reproductive data were derived from the breeding records of female rhesus monkeys a t the Yerkes Regional Primate Research Center Field Station. For the present analysis, data were used from the 78 colony-born females that had produced their first offspring by 1981. All subjects were members of large social groups containing multiple adult males, adult females, and immature animals. Animal housing and maintenance have been described previously (Bernstein and Gordon, 1977). The outcome of each reproductive year for every female was classified into three mutually exclusive categories: 1) sterile year-no indication of pregnancy; 2) birth tragedy-abortion, stillborn, or neonatal death; and 3) success-the offspring surviving a t least until the next pregnancy. The incidence of sterile years may be inflated since in this environment we could not distinguish between a female that was not impregnated and one that was impregnated but experienced an abortion early in gestation. Tabulations of specific outcomes were made for both the first and second reproductive years, as well as third and successive years combined. Five females did not contribute data to the second reproductive year. Four were housed with vasectomized males and were thus not impregnated, and the fifth female died. The birth season for this colony is restricted to the spring months with a median parturition date occurring consistently year to year during early May (Bernstein and Gordon, 1977). Parturition dates were compared across successive pregnancies by assigning the date of parturition the value of the number of calendar days that had accumulated in that year (Jan. 1 = 1, Feb. 1 = 32, March 1 = 60, etc.). Since the rhesus colony has been maintained primarily for biobehavioral research (Bernstein and Gordon, 19771, relative dominance ranks for each of the animals within each of the groups were known. For this analysis, each animal was categorized as high-, middle-, or low-ranking according to her relative standing among animals in her group (Bernstein, 1970). Data were expressed in terms of percent outcome of the total number of reproductions possible. Frequencies of outcomes were analyzed by chi-square tests, with specific comparisons evaluated by the partitioning technique described previously (Bresnahan and Shapiro, 1966). W h q e appropriate, grouped data were expressed X i. SE. Differences in parturition dates were evaluated with ANOVA or t-tests. All statistical tests having a P < 0.05 were considered significant. RESULTS Of the 78 females contributing data, 20.5% (n = 16) had their first parturition at approx- 105 CONSEQUENCES OF FIRST PREGNANCY * * 100 :145) 2* ,g 80 m 1261 70 60 % 50 40 30 :20 m 0. 10 0 1 2 3 Total R e p r o d u c t i v e Year Fig. 1. Percentage of live births between early-maturing females (stippled bar) and typical-maturing females (open bar) across reproductive years. Numbers in parentheses in- dicate the number of female years contributing to each year. Asterisks indicate a significant difference between group comparisons (P < 0.05). imately 3 years of age (36.6 +- 0.3 mos). The majority of females, 73.1% (n = 57), gave birth 12 mos later (47.4 +- 0.2 mos) with 6.4% (n = 5) delaying first parturition until 5 years of age (59.4 -+ 0.3 mos).Data from these two groups have been combined for analysis. Thus, comparisons were made between early-maturing females (first parturition at 36 mos) and typical-maturing females (first parturition at 48 or 60 mos). With respect to the date of first parturition, the early-maturing females gave birth significantly later during the birth season (day 141.3 ? 4.9) compared to their agemates (day 123.3 i 3.4; ts3= - 2.45, P < 0.05). Of the 16 females that exhibited first parturition at 36 months of age, a significant percentage were from high-ranking matriarchies. Seventy-five percent were born to high-ranking mothers compared t o middle- (18.7%) and low-ranking mothers (6.3%; xy = 12.23, P < 0.05). At first parturition, 12 of these females held the same relative rank they had at birth. Of the remaining four, two females that had had high-ranking mothers at birth and two that had had middle-ranking mothers at birth had fallen in rank by first parturition. Of the 62 females that did not have an early first parturition, 24.9% (n = 15)had mothers that were high-ranking. Among the female infants born to high-ranking females (n = 271, 44.4% (n = 12) subsequently had an early first parturition and 55.6% (n = 15) did not. Thus, first parturition at 36 mos of age is significantly related to high social rank, but high social rank does not necessarily guarantee early first parturition. Furthermore, the 16 early-maturing females in the present analysis have produced a total of nine females that have, to date, reached breeding age (3 years). Of these nine, 22.2% (n = 2) have themselves been early maturers. Successful pregnancies An examination of the outcomes of successive pregnancies revealed that, in terms of percentage of total reproductive years, females that had their first birth at 3 years of age had significantly fewer live births than did females that had had their first parturition at 4 or 5 years of age (Fig. 1;x = 8.89, P < 0.05). This difference was due to early-maturing females' having significantly fewer live births during the year following their first parturition ("year 2") than their age mates (xf = 6.42, P < 0.051, since there was no difference in the rate of live births between the two groups at their first pregnancy (xf = 1.13, P > 0.05) or in all pregnancies following their second year (x? = 2.63, P > 0.05). In addition to these between-group differences, both early- and typical-maturing females experienced a significant reduction in the percentage of live births during their second year compared to their first (early: x? = 12.04, P < 0.05; typical: x: = 9.98, P < 0.05). It thus appears that some aspect of first pregnancy has a deleterious effect on the capacity of females to have a successful birth the fol- 106 M.E. WILSON, M.L. WALKER, AND T.P. GORDON lowing year, and that this effect is even more pronounced for early-maturing females that had their first parturition at 3 years of age. Although early-maturing females had significantly fewer live births in the year following their first parturition, a further analysis revealed that, in the long run, early-maturing females produce as many offspring as their agemates. A comparison of mean number of offspring produced by age of the female indicated that there was no difference in the number of successful pregnancies between early- and typical-maturing females (Table 1; te = 0.37, P > 0.05). Thus, when the analysis of total reproductive success is based on female age and not total reproductive years, early-maturing females are as successful as typical-maturing females. TABLE 1. T h e mean I ? SE) number of surviving offspring are listed as a function of the age of the mother at the 1982 birth season, or her age at her last birth before her death (data are shown for both early- and t.ypica1maturing females) Female age (years) Early X 4 1.0 SE 0 n 4 Typical 1.0 SE 0 n 4 x 5 6 2.0 0 2 1.8 0.4 9 2.3 0.6 3 2.0 0.7 1 3 7 8 3.3 5 0.6 0 3 1 3.3 4.4 1.0 0.8 1 2 7 9 6 0 1 5.2 1.1 5 10' 11 12 3.0 0 0 1 6.0 6.3 0.7 2.1 5 3 8.0 0 1 7.8 1.5 4 - 'Since no"ear1y"fernales were 10 years ofage at the 1982 birth season, this age group was not mcluded in the analysis reproductive failures (sterile years and birth tragedies) to live births (68.8% vs 31.2%, n = 16) than all succeeding years (22.5% vs 77.5%, Reproductive outcome n = 40; x? = 16.7, P < 0.05).A similar pattern The factors that contribute to a reduced per- is shown by typical-maturing females, with a centage of live births at the second reproduc- significantly larger ratio of reproductive failtive year appear to be similar for early-ma- ures t o live births at the second year (33.3% turing and typical-maturing females. The vs 66.7%, n = 57) than in subsequent years percentage of sterile years following their first (12.4%vs87.6%,n= 145;xf= 12.10,P<0.05). parturition was significantly greater for early- Thus, independent of the age at maturity, fematuring females than for their age-mates (Fig. males tend to experience significantly more re2; xf = 4.04, P < 0.05). There was no signifi- productive failures in the year following first cant difference in the percentage of confirmed pregnancy than in later years. The outcome of first parturition appeared t o pregnancies during this second year, which resulted in a birth tragedy (abortion, stillborn, have a significant effect on the second reproor neonatal death; x: = 2.58; P > 0.05). It ductive year for both early- and typical-maappears, therefore, that the greater reduction turing females (Fig. 3). For those that expein the percentage of live births for early-ma- rienced a birth tragedy at their first pregnancy, turing females at their second pregnancy is a and thus did not lactate, all (100%) were imgreater failure to conceive. With successive pregnated during their second reproductive years, both groups of females showed a signif- year, with 66.7% of these early-maturing feicant decline in the frequency of nonpregnant males having a live birth at the second year years (Fig. 2; early: xf = 8.23, P < 0.05; typical: and 75.0% of the typical females having a live x: = 11.98, P < 0.05) but not in the occurrence birth at the second year. In contrast, those earlyof birth tragedies (early: xf = 3.34, P > 0.05; maturing females that had a successful first typical: x: = 2.75, P > 0.05). Thus, the per- pregnancy, and thus lactated for some interval, centage of birth tragedies remains somewhat had significantly fewer confirmed pregnancies constant for the second and succeeding preg- at year 2 than typical females (x? = 5.78, P < nancies. In contrast, the capacity to conceive 0.05).That is, following a successful pregnancy appears to be greatly reduced following the first at year 1, a higher percentage of early females pregnancy, and this is even more pronounced were not impregnated at year 2 compared t o for females that have their first parturition 1 the age-mates. There was no difference in the year earlier than their age-mates. percentage of live births or birth tragedies in Assuming that the occurrence of a birth year 2 following a successful pregnancy at year tragedy also represents a reproductive deficit 1 for early- and typical-maturing females (xf on the part of the female, combining the in- = 2.44, P > 0.05). cidence of sterile years and birth tragedies also Parturition dates reveals a parity effect for both early- and typical-maturing females. For early-maturing feFemales that had their first offspring surmales, the second reproductive year is char- vive through the next breeding season had a acterized by a significantly larger ratio of significantly longer interbirth interval be- CONSEQUENCES OF FIRST PREGNANCY 100 i earJy n = typical n = # early n = l typical n=4 90 * ff 80 r ; 70 ” : a z’oso 5 40 u 107 30 U L 20 2. 10 0 llhird Second REPRODUCTiVE Fig. 2. Percentage of each birth outcome between earlymaturing females (stippled bar) and typical-maturing females (open bar) for the second and successive ( 3 3rd) re- YEAR productive years. Asterisks indicate a significant betweengroup comparison. 0 ) . 0 c Pregnant Not Pregnant Yr. 2 Yr.2 Birth Tragedy Yr. 1 ! Live Birth Vr. 1 Fig. 3. Percentage of females not pregnant (open bar) or pregnant (live births stippled bar; birth tragedy hatched bar) a t their second reproductive year as a function of their birth outcome the previous year between early- and typicalmaturing females. Numbers in parentheses indicate number of females in each category. tween their first and second parturitions than between subsequent successful parturitions. Of the 78 females, 27 met the criteria for this analysis, having a successful first pregnancy followed by a live birth in year 2 and subsequent successful pregnancies. Of these 27, only two were early-maturing females so data from both groups of females were combined for analysis. Following a successful first pregnancy, the interbirth interval at year 2 was 379.5 ( 4.3) days compared to an interbirth interval between the third and successive successful pregnancies of 356.1 ( i 3.2) days (tZ6= 3.39, P < 0.05). To determine if the date of first * M.E. WILSON, M.L. WALKER, AND T.P. GORDON 108 T A B L E 2. T h e relationship between sex o f offspring a t first parturition and birth outcome the following year is listed for both early- and typical-maturing females. A l s o shown is the mean f t SE ) interbirth interual for those females who gave birth in year 2 Birth outcome in year 1 Birth yr 2 Sex of first offspring Early (n = 13) Typical ( n = 51) Total 4 in = 64) Interbirth interval yr 1 to yr 2 (days) 6 P 1 20 46.7% 376.1 3 21 53.36 363.2 No birth yr 2 P 6 6 6 63.2% - 3 4 36.86 - parturition was related to a pregnancy the following year, the parturition date at first pregnancy for both early- (day 145.0 ? 9.7, n = 4) and typical-maturing females (day 124.8 & 3.7, n = 41) that were not impregnated at year 2 was compared to the first parturition date for females that were impregnated at year 2 (early: day 153.6 7.0, n = 9; typical: day 127.0 2 7.4, n = 10). As stated earlier, early-maturing females as a group had a significantly later first parturition. With respect to reproductive outcome at year 2, there was no difference in the date of first parturition for those that were impregnated at year 2 and those that were not (F1,60< 1.0, P > 0.05) even when age at maturity was taken into account (interaction term: F1,60 < 1.0, P > 0.05). Sex of the surviving offspring at first parturition was also examined to determine if this affected reproductive outcome the followingyear (Table 2). Comparing sex of first offspring and successful birth outcome the following year for both early- and typical-maturing females combined revealed that sex of first offspring was not related to birth outcome in year 2 (x: = 1.45, P > 0.05). Furthermore, an analysis of the interbirth interval for the females that gave birth in year 2 indicated that this interval was similar for females that produced a male at year 1 and for females that produced a female ( t 4 5 = 1.66, P > 0.05). * DISCUSSION The present analysis demonstrates that first parturition for rhesus monkeys has an effect on future reproductive capacity, specifically during the second reproductive year. A reduced reproductive performance in the second year was evident following a successful first pregnancy for all females, but was even more pronounced for those females that had first par- turition at 3 years of age-a full year earlier than their age-mates. A higher rate of sterile years was associated with this reduced reproductive efficiency during the second year, which was even greater for the early-maturing females. Both the early- and typical-maturing females that experienced a birth tragedy at first pregnancy delivered a live birth the following year. Thus, a successful first pregnancy appears to have deleterious consequences that are manifested in a reduction of capacity of females to conceive the following year. Furthermore, when the incidence of sterile years and birth tragedies were combined, the rate of reproductive failures in the year following first pregnancy compared to later years was even more dramatic for both early-and typical-maturing females. The reduction in pregnancy rate in the year following a successful first parturition could be the result of either a failure t o ovulate or a failure to conceive following an ovulation. Since a successful parturition is followed by an interval of lactation that may extend into the next breeding season, it may be that the reduction in pregnancy rate at the second year, which again is more pronounced for the earlymaturing females, may be due t o the effects of the lactational period following first pregnancy. There is evidence from studies on human females that prolonged lactation does delay the next ovulation (Knodel, 1977; Van Ginneken, 1977). Since rhesus monkeys are seasonal breeders, a failure to conceive during one mating season imposes a 12-month interval to subsequent ovulation. Following a successful first parturition, some females may lactate through the next breeding season, thus precluding ovulation for another year. Females in the present analysis that had a successful first parturition and that produced a live infant the next year did indeed have a longer interbirth interval for this period than following later, successful pregnancies. Since female rhesus monkeys tend to skip the next reproductive year if they give birth late in the previous birth season (Wilson et al., 19781, it could be that the reduced pregnancy rate during the second reproductive year was due to a late parturition date a t first pregnancy. However, since there was no difference in parturition dates at first pregnancy between those females that were impregnated at year 2 and those that were not, this hypothesis was not supported. Rather, these data suggest that the lactational period followingfirst parturition may be longer than for later years, thus accounting CONSEQUENCES OF FIRST PREGNANCY for the later parturition date at second pregnancy for the females that do give birth or a failure to conceive for the remaining females. Several factors may influence the duration of the lactational interval. Although a previous study had suggested that rhesus females having a male offspring would have a shorter interbirth interval (Simpson et al., 19811, no relationship between sex of the first offspring and the interval to the next pregnancy or the pregnancy rate in the next reproductive year was observed in the present analysis. Rather than sex of the offspring, some characteristic of the mother likely has a major effect on the lactational interval. If primiparous mothers are indeed more protective or restrictive of their infants (Mitchell e t al., 1966; Seay, 19661, they may allow their infants to nurse longer. The ovulation-delaying effect of suckling may not be nursing per se, but a critical pattern of nursing, in terms of frequency and duration (Konner and Worthman, 1980; Bongaarts, 1980). Primiparous mothers may allow their infants to suckle in this pattern longer than multiparous mothers, thus delaying ovulation. Nutritional status of the mother may also influence the interval between the first and second parturition. A decrease in body weight and corresponding percent body fat has long been implicated in producing an anovulatory condition in females (Frisch, 1977). The influence of nutritional status on the duration of postpartum anovulation is not clearly understood, with some studies reporting that dietary differences are important (Chavez and Martinez, 1973; Frisch and MacArthur, 19791, whereas others report a trivial effect of diet on the lactation-induced anovulatory interval (Huffman et al., 1978). A more likely explanation is that nutritional status acts synergistically with the lactational pattern to influence the interbirth interval (Underwood, 1981; Knodel, 1977). Fully adult female rhesus monkeys typically show a weight loss from parturition through early lactation followed by a weight gain prior to the next ovulation (Van Wagenen and Catchpole, 1956). Since rhesus females do not complete growth until 2-3 years after the age of first pregnancy (Watts and Gavan, 19821, it is possible that primiparous females, particularly early-maturing females, cannot support an ovulation or pregnancy the second year. The demands of the lactational period following first pregnancy, coupled with the female’s own requirements for the completion of growth, may delay ovulation until the third year or result in a failure to maintain 109 pregnancy during the second year. Early-maturing females have been found to be heavier at puberty (defined by menarche) than latematuring females (Wilen and Naftolin, 1976). The effects of first pregnancy may be greater on early-maturing females, since this event occurs earlier in their growth phase. Typical-maturing females may gain the capacity to reproduce during the nonbreeding months following menarche; but given the seasonal control of ovulation, conception is not possible for several more months. This additional time would allow these females to achieve more growth prior to first ovulation and thus be more prepared to meet the demands of the ensuing pregnancy and lactation. Of the early-maturing females in the present analysis, significantly more were from highranking matriarchies. Not all females born into high-ranking matriarchies had an early first parturition-approximately half did and half did not. A previous report of early-maturing rhesus females indicated that early-maturing females were heavier at birth than their agemates (Van Wagenen and Catchpole, 1956). Assuming that high-dominance rank allows animals priority to food resources (Bernstein, 19701, high-ranking females may produce, on the average, heavier infants. Although no data are currently available on neonate weight as a function of the mother’s dominance rank, highranking females tend to be heavier (Small, 19811, and heavier females produce heavier offspring (Riopelle et al., 1976).Although birth weight is likely a critical variable in determining whether a female will mature early, it is obvious that a healthy developmental period may also be important. Although early-maturing females had significantly fewer live births per total reproductive years, they were as reproductively successful as typical-maturing females when compared on the basis of offspring produced by specific ages. Furthermore, the earlier reproductive start for early-maturing female allows them to have their offspring enter the breeding pool a full year earlier than the offspring of their age-mates. Thus, these early-maturing females may not necessarily show reduced fecundity, despite the increased reproductive failures during their second reproductive year. Since these early maturers tend to be from higher-ranking matriarchies, an early first pregnancy may be another mechanism by which high-ranking animals gain a reproductive advantage over their lower-ranking conspecifics (Drickamer, 1974; Wilson et al., 1978; Sade et 110 M.E. WILSON, M.L. WALKER, AND T.P. GORDON al., 1977). 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