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Consequences of first pregnancy in rhesus monkeys.

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Consequences of First Pregnancy in Rhesus Monkeys
Yerkes Regional Primate Research Center of Emory University, Atlanta,
Georgia 30322
Pregnancy, Reproductive Outcome, Parity, Rhesus
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
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.
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.
Of the 78 females contributing data, 20.5%
(n = 16) had their first parturition at approx-
,g 80
% 50
2 3
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-
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)
SE 0
SE 0
1 3
3.3 5
0.6 0
3.3 4.4
1.0 0.8
1 2 7
6.0 6.3
0.7 2.1
'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-
i earJy n =
typical n = #
early n = l
5 40
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-
productive years. Asterisks indicate a significant betweengroup comparison.
Not Pregnant
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
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
Early (n = 13)
Typical ( n = 51)
Total 4 in = 64)
Interbirth interval
yr 1 to yr 2
No birth yr 2
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).
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
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
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
al., 1977). Nevertheless, the consequences of a
successful first pregnancy have immediate effects on the reproductive physiology of the female. The immediate physiological impact of
successful first pregnancy can be observed in
all females, but may be more dramatic in those
females that begin reproductive activity a t a
younger age.
We thank D. Chikazawa and J. Wilson for
their technical assistance, and L. Wright for
her editorial assistance. This project was supported by NIH grants RR-00165 and HD-16305,
and NSF grant BNS-13248.
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pregnancy, monkey, first, rhesus, consequences
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