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Milk secretion in pregnancy among free-ranging Japanese macaques.

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American Journal of Primatology 30169-174 (1993)
Milk Secretion in Pregnancy Among Free-Ranging
Japanese Macaques
ICHIROU TANAKA', SHIN-ICHI HAYAMA', AND HIDE0 NIG12
'Department of Anthropology, Faculty of Science, The University of Tokyo; 'Division of
Wild Animal Medicine, Nippon Veterinary and Animal Science University, Musashino,
Tokyo, Japan
Milking under anesthesia in pregnant free-ranging Japanese macaques
(Macaca fuscata) directly revealed lactation in gestation at Jigokudani
Monkey Park, the Shiga Heights, Nagano Prefecture, Japan, from 12 to 14
February 1992. Multiparae secreted milk at 76-97 days of estimated fertilization age when the birth intervals t o the next offspring were 2 years.
The observation of sucking behavior from February 1991 to March 1992
indicated that concurrent suckling by these multiparae terminated approximately 70 days before the next parturition after the growth of fetuses
had accelerated and the embryos survived the crisis of abortion. Thus,
Japanese macaque mothers appear to hedge maternal investment with
concurrent lactation against possible miscarriage. Two nulliparous pregnant females secreted milk 3 months before the first parturition although
they had no suckers. The first preparation of lactation appears to require
the duration of longer than 3 months in nulliparae although worked mammary glands appear to be able to resume within 1month in multiparae.
0 1993 Wiley-Liss, Inc.
Key words: Japanese macaque, duration of lactation, pregnancy, parity,
suckling behavior
INTRODUCTION
Most Old World primates usually give birth to single young, which develop
slowly and have a long period of breast-feeding [review in Hearn, 19841. The
pattern of changes in suckling behavior, however, had not been determined in
primates [Hearn, 19841.Although Hearn [19841conjectured that rhesus macaques
mothers ceased to suckle their infant before entering the next pregnancy, the
observation of suckling behaviour in free-ranging Japanese macaques suggested
lactation in pregnancy [Tanaka, 19921.We investigated lactation in gestation with
milking under anesthesia and estimated the duration of lactation.
METHODS
We temporarily (for 2 or 3 h) captured free-ranging Japanese macaques
(Macaca fuscata) in Jigokudani Monkey Park, the Shiga Heights, Nagano Prefec-
Received for publication J u n e 9, 1992;revision accepted February 9,1993.
Address reprint requests to Dr. Ichirou Tanaka, Department of Anthropology, Faculty of Science, The
University of Tokyo, Hongo 7-3-1,
Bunkyo-ku, Tokyo, 113 Japan.
0 1993 Wiley-Liss, Inc.
170 / Tanaka et al.
ture, Japan, from 12 to 14 February 1992. There is a distinct mating season in
autumn from November to early December and a distinct birth season in spring
from late April to June. After the injection of two anesthetics (xylazine hydrochloride and ketamine hydrochloride) intramuscularly, we diagnosed pregnancy with
ultrasonography. Then we wrung the nipples of pregnant female macaques. As
soon as milk seeped, we stopped squeezing breasts to minimize the influence of
milking on sucking infants. Therefore we did not use oxytocin. After diagnosis and
milking, we injected intravenously the antagonist (tolazoline hydrochloride) of the
former anesthetic into macaques to recover from anesthesia quickly. We had no
sooner released captured monkeys than they awoke. None of the anesthetics or the
antagonist affects fetal development.
The suckling behavior of a free-ranging troop of Japanese macaques was studied in Jigokudani Monkey Park from February 1991 to March 1992. The monkeys
can be observed within a distance of 30 cm at closest approach. Using the focalanimal sampling (continuous recording) method [Martin & Bateson, 19861 for
mother-infant dyads, we recorded when the infant began to suck its mother’s
nipple and when it stopped. Based on the local rate of sucking (the number of sucks
per second), we discriminated nutritive sucking (sucking with milk flow) from
non-nutritive sucking (sucking without milk flow) because nutritive sucking occurred a t a constant low local rate; non-nutritive sucking occurred a t a n increasing
and high local rate [Tanaka, 19921. To measure the local rate of sucking, we used
8 mm video cameras (SONY CCD-TR75 and CCD-TR705). During the video playback of suckling, we calculated local rates and distinguished nutritive sucking
from non-nutritive sucking.
In Japanese macaques, in the second phase of suckling (after infants were 7
months old), suckling occurred cyclically with the mean cycle length of 2 h, 2 min,
and 58.5 seconds (mean 5 SEM = 7,378.5 481.2 seconds, N = 36), whereas the
estimated standard deviation is 2,807.0 seconds. A cycle length is defined as the
time from a n increase in sucking rate (the end of nutritive sucking) to a n increase
in sucking rate in the next sucking bout [Tanaka, 19921, because infants sucked
milk that had been secreted by and stored in mammary glands. We analyzed only
the temporal lengths in which the previous nutritive sucking bout, the interval
from the previous bout to the bout, and the nutritive sucking bout were observed
continuously. We excluded from analysis those observations where we could not
distinguish the local rate of sucking because the mother tightly embraced and hid
her infant. Because our records of suckling cycle length were complete data, survival analysis [Nelson, 19821 estimated that the 99 percentile of the cycle length
distribution was 3 h , 51 min, and 48 seconds (13,908 seconds). If no nutritive
sucking of a n infant to its mother is observed during 5 h of continuous focal
sampling which includes a t least two normal suckling cycles, suckling was considered finished. As the criterion of suckling cessation, we used not 4 h (just beyond
the 99 percentile) but 5 h because, in the different phase (the first phase), there was
a n outlier whose cycle length was 4 h, 29 min, and 39 seconds [see Tanaka, 19921
in which a n infant continued whimpering 3 h after the previous nutritive sucking
bout. This frustration behavior also suggested that the duration of more than 3 h
was abnormally long for the suckling cycle. We continually observed the target
mother-infant dyad from birth for at least continuous 5 h. We defined the duration
of suckling a s the age of the target infant between the last observation with
nutritive sucking and the first observation without nutritive sucking.
As to the technical terms, we used lactation in physiological phenomena based
on milk secretion and suckling in behavioral phenomena based on the observation
of nutritive sucking by infants.
*
Macaque Lactation in Gestation / 171
TABLE I. Milking Under Anesthesia in Pregnant Japanese Macaques
Mother
Name
Toimu
Mesumu
Taiko
Mekako
Tachiyo
Narumi
Kerimi
Tomano
Ringokamikiri
Dokuga
Mesuguro
Tobira
Knife
Nadeshiko
Momiji
Meakan
Tarai
Age
(years) Parity
5
5
6
6
7
8
8
10
11
11
11
12
12
13
13
15
12
0
0
1
1
1
1
2
3
3
3
3
4
4
4
4
5
3
Milk
secretion
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
No
Embryo
Interbirth
interval
(years)"
Days before
parturition
2
2
2
2
2
2
2
2
2
2
2
2
2
2
3
88
103
78
88
85
92
81
79
93
97
81
88
76
87
93
77
73
Estimated fertilization
age (days)b
85
70
95
85
88
81
92
94
80
76
92
85
97
86
80
96
100
"Interbirth interval (years) is a period from the parturition of the suckling infant (except Tarai) to the parturition of the embryo. In Tarai, interbirth interval is a period from the parturition of the previous infant to that
of the embryo.
bEstimated fertilization age (days) is calculated by taking away days before parturition from 173 because the
mean gestation length is 173 2 1.8 (SEM) days among Japanese macaques [Nigi, 19761.
RESULTS
In 16 pregnant female Japanese macaques milk secretion was revealed directly in milking under anesthesia (Table I). Two nulliparous pregnant females
(named Toimu and Mesumu) secreted milk (70 and 85 days after estimated fertilization) 3 months before the first parturition. Multiparous lactation lasted until
approximately 100 days into gestation: milk secretion was documented in 14 females examined 70-97 days after estimated fertilization but was not present in
one female examined 100 days after fertilization (Table I). In multiparae, interbirth intervals to the subsequent offspring (the fetuses) varied our results: when
interbirth intervals from suckers to fetuses were 2 years, pregnant mothers (N =
14) secreted milk, and when an interbirth interval was 3 years, a pregnant mother
(N = 1)did not secrete milk.
A month after milking, Dokuga, one of the milking subjects, suckled her 658day-old infant on March 13, 1992, 68 days before the next parturition, and no
suckling was observed during 5 h and 20 min of continuous focal sampling on
March 19, 1992, 62 days before parturition. A pregnant mother named Namako
suckled her 640-day-old infant on February 15, 1991, 110 days before the next
parturition, and termination of suckling was confirmed on April 6, 1991, 60 days
before parturition.
DISCUSSION
Milking under anesthesia revealed lactation in gestation in 16 Japanese
macaque females. Fourteen multiparae had embryos and suckled their infants
simultaneously. Two nulliparae secreted milk although they had no sucker. Milk
172 / Tanaka et al.
secretion in pregnancy appears to differ between multiparous and nulliparous
mothers, because multiparous suckling behaviour ceased at late gestation when
the interbirth intervals were 2 years. Moreover, a pregnant multipara did not
secrete milk a t the 100 days of estimated fertilization age when the interbirth
interval was 3 years. Two multiparous mothers ceased suckling just before conception when the birth intervals were 3 years [Tanaka, 19921. Thus, in multiparae
with 2-year-old infants lactation appears to terminate before gestation. Even if
multiparous suckling (the second phase with a low level of milk energy output)
lasted until parturition when the next offspring was born in the following year, the
other phase of suckling (the third phase with a high level of milk energy output)
occurred a month before parturition [Tanaka, 19923. These cessations of suckling
behavior show that multiparous lactation in gestation appears to be the extension
of suckling for the previous offspring; nulliparous lactation in gestation appears to
be the expansion of preparation for the first neonates.
Milk secretion in two nulliparous females indicated that nulliparae prepared
for lactation at least 3 months before parturition although multiparae prepared for
lactation only a month before parturition because of the timing of the third phase
of lactation in Japanese macaques [Tanaka, 19921. Thus, the first preparation of
milk secretion appears to need longer duration than the next. Once mammary
glands worked, lacation might resume only within a month.
Milking under anesthesia in pregnant free-ranging Japanese macaques indicates that lactation lasted until approximately 100 days into gestation when the
next offspring was born after 2 years. Besides the above two cases of cessation of
suckling (60 and 62 days before parturition), two terminations of suckling were
confirmed a t 77 and 82 days before parturition when the next offspring was born
after 2 years [Tanaka, 19921. Suckling, hence, ceased a t approximately 110 days
after estimated fertilization (see Table I). The data from different subjects and the
rough estimates of fertilization age appear to overlap the duration of lactation and
the termination of suckling behavior. Further study of hormones and continuous
milking on the same subject is required.
In rhesus macaques whose gestation length (168 days) is approximately equal
to that of Japanese macaques (173 days), the growth of fetuses accelerates at 70
days of gestation [van Wagnen et al., 19651. From 90-100 days to 155-160 days of
gestation, the rhesus fetal growth curve follows a n almost linear curve where fetal
weight change is approximately 5.7 glday [van Wagenen et al., 19651. Assuming
that prenatal growth in Japanese macaques follows a similar pattern, this suggests that lactation ceases when fetuses begin to grow linearly after organogenesis
(embryonic period). Human mothers tend to abort embryos in organogenetic period
[Hoshi, 19881. Boklage [19901 estimated that in human beings 73% of natural
single conceptions do not survive to 6 weeks of gestation. In baboons, which are
similar to humans in many important aspects of early reproductive biology, 60% of
embryos were aborted spontaneously in early pregnancy [Kuehl et al., 19921. In
Japanese macaques abortion peaks 1 month after conception [Goto, personal communication] although Japanese macaques are seasonal breeders, differing from
baboons, which are non-seasonal breeders. Thus, after fetuses survive the crisis of
miscarriage, macaque mothers appear to cease suckling yearlings. If mothers
abort, mothers can increase survivability of the previous offspring in compensation
for miscarriage with concurrent lactation. This suggests that Japanese macaques
hedge maternal investment in yearlings and embryos with lactation in pregnancy.
This coexistence of lactation and gestation is also seen in humans [the Kalahari desert San: Konner, 1977; rural Guatemalans: Klein et al., 19771. Jones
[ 19881 reported rural Indonesian women who experienced resumption of menses
Macaque Lactation in Gestation / 173
while breast-feeding. Ellison [ 19901 suggested that in human beings ovarian responsiveness has evolved to optimize the probability of a successful reproductive
outcome in any individual instance of reproductive effort based on long-term energy balance. In rodents, simultaneous gestation and lactation of two litters may
be a n adaptation to ecological constraints [Gilbert, 19843: rodents (voles and lemmings), whose breeding season is seasonally restricted and whose conception-toweaning interval is short relative to the breeding season, tend to overlap litters to
increase fecundity with reduced interlitter spacing.
In Japanese macaques, when the next offspring is born after a n interval of 1
year, suckling lasts until the subsequent parturition; when the next offspring is
born after a n interval of 2 years, suckling continues into the early part of the next
pregnancy; when the next offspring is born after a n interval of 3 years, suckling
ceases before gestation [Tanaka, 19923. This concurs with milking data in multiparae (Table I). Therefore, the duration of lactation may be related to the ages of
the previous offspring. In toque macaques, age-specific mortality peaked from
birth to 1 year old, and secondly from 1year old to 2 years old [Dittus, 19791. This
is consistent with Japanese macaques in Jigokudani Monkey Park [Tokida, personal communication]. When the interbirth interval to the subsequent offspring is
1year, mothers who desert suckling might tend to lose the previous infant, because
infants less than a year old do not get milk like orphans. Mothers, hence, continue
lactation until parturition. Because yearling orphans had better chances of surviving than newborn orphans in free-ranging Japanese macaques [Hasegawa &
Hiraiwa, 19801, yearlings appear to need less maternal care. Therefore, mothers
cease suckling 2 months before parturition. The rhesus prenatal growth curve [van
Wagenen et al., 19651 shows a small cost of embryos on mothers in early pregnancy. This small expense may enable mothers to continue investment in the
previous offspring and to increase its chance of survival. However, if the burden of
fetuses on mothers increases after the growth of fetuses accelerates, mothers stop
suckling yearlings. Since 2-year-old orphans are much more likely to survive than
l-year-old orphans, lactation ceases before gestation when the next offspring is
born after a n interval of more than 2 years.
CONCLUSIONS
1. When the interbirth intervals to the subsequent offspring were 2 years,
pregnant Japanese macaque multiparae (N = 14) secreted milk a t 76-97 days of
estimated fertilization age.
2 . When the next offspring was born after 2 years, suckling lasted until approximately 100 days into gestation when the growth of fetuses accelerated.
3. Nulliparous pregnant females (N = 2) could secret milk 3 months before
the first parturition.
ACKNOWLEDGMENTS
We thank Mr. Sougo Hara for permission to study a t Jigokudani Monkey Park;
Mr. Eishi Tokida, Mr. Haruo Takefushi, Mr. Shigenori Nishizawa, Mr. Toshio
Hagiwara, and the other staff of Jigokudani Monkey Park for their assistance; and
Dr. Kenichi Aoki, Professor Toshisada Nishida, Dr. Yukio Takahata, and anonymous reviewers for their valuable advice. This study was supported in part by a
grant in aid from the Japanese Ministry of Education, Science, and Culture.
174 / Tanaka et al.
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