вход по аккаунту


Energetic consequences of seasonal breeding in female Japanese macaques (Macaca fuscata).

код для вставкиСкачать
Energetic Consequences of Seasonal Breeding in
Female Japanese Macaques (Macaca fuscata)
Cécile Garcia,1* Michael A. Huffman,2 Keiko Shimizu,3 and John R. Speakman4
Laboratoire de Dynamique de l’Evolution Humaine, CNRS UPR 2147, 44 rue de l’Amiral Mouchez,
75014 Paris, France
Department of Ecology and Social Behavior, Primate Research Institute, Kyoto University, Inuyama, Japan
Department of Zoology, Faculty of Science, Okayama University of Science, Japan
Aberdeen Centre for Energy Regulation and Obesity (ACERO), Institute of Biological and Environmental Science,
University of Aberdeen, UK
deuterium method; nutritional status; body composition; reproductive costs
Japanese macaques inhabit a relatively
cold environment and females of this species could have
developed strategies of energy economy to face the sometimes-harsh seasonal conditions of temperate climates,
as well as reproductive costs, and thus regulate their
energy balance. Here, we explore the relationship
between nutritional status, body composition, seasonality, and reproductive status using isotope-labeled water,
anthropometric measurements, and leptin assays from
14 captive female Japanese macaques. Our results indicated that body mass provided the best predictor of fatfree mass and fat mass. These females varied in
estimated percent body fat between 8 and 25% (18% on
average at the beginning of the mating season and 13%
during the birth season). Higher body mass and body fat
content were observed at the beginning of the mating
How energetics influence female reproductive function
in primates remains the subject of considerable debate
as to mechanisms and controls. Several studies in
humans and non-human primates have shown that inadequate caloric intake, strenuous physical activity, and
short-term negative energy balance may induce reproductive dysfunction and decreased fertility (Dewey, 1998;
Loucks and Thuma, 2003; Schneider, 2004; De Souza et
al., 2007; Williams et al., 2007). Although there is large
consensus that nutritional status is a key factor influencing female fitness, accurate monitoring of energetic condition and body composition in wild or semi-free ranging
primates remains a significant methodological challenge,
so that relatively little attention has focused on the energetic stresses of mating activity and lactation, specifically in seasonally reproducing species. These two reproductive activities are considered to entail more energy
costs than pregnancy (Lee, 1996; Key and Ross, 1999),
and include the energy expanded on intra-sexual competition for mates and parental care in addition to the
daily energy expenditure. Whereas lactation length may
be used as a proxy for energy costs of parental care, it is
nevertheless difficult to assess the energy costs of intrasexual competition directly; and other costs associated
with intra- or inter-sexual conflicts, such as risk of
injury, are not easily translated into energetic terms.
Primates and many other mammalian species living in
seasonal environments exhibit a variety of physiological
and behavioral characteristics that enable them to cope
with temporal fluctuations in climate and energy availC 2011
season, which supports the hypothesis that individual
females need to attain a sufficient physical condition to
cover energy costs associated with mating activity, and
to survive under severe ecological conditions in winter
with high thermoregulatory costs. We found a relationship between conception rates and energetic condition or
body fat, with females that conceived during one mating
season being fatter after the end of their previous mating season. Together, these results suggest that, even in
captive settings with constant food availability, seasonal
breeding entails relatively high energy costs, and that
females with higher energy status could invest more in
reproductive activities and could afford to reproduce
more rapidly. Am J Phys Anthropol 146:161–170, 2011.
C 2011
Wiley-Liss, Inc.
ability. Therefore, energy balance and adiposity are not
maintained at a constant set point but rather vary with
season and also with reproductive status. This is exacerbated in seasonally breeding animals, especially for
females, which are characterized by annual changes in
body mass and adiposity (Rousseau et al., 2003). In the
seasonal environment, primates accumulate and subsequently loose energy stores in a yearly body mass gain–
loss cycle (Mori, 1979; Richard et al., 2000; Kurita et al.,
2002; Hamada et al., 2003; Pusey et al., 2005) and most
of the increase/decrease in mass seems due to an
increase/decrease in fat reserves. During periods of food
scarcity, endogenous lipids are the main source of energy
utilized and proteins are spared. Studies on protein or
Grant sponsors: Ministry of Foreign Affairs, France; Japan
Society for the Promotion of Science; Institutional Research
*Correspondence to: Dr. Cécile Garcia, Laboratoire de dynamique
de l’évolution humaine, CNRS UPR 2147, 44 rue de l’Amiral Mouchez, 75014 Paris, France.
Received 1 July 2010; accepted 18 April 2011
DOI 10.1002/ajpa.21553
Published online 8 August 2011 in Wiley Online Library
fat sparing were mainly conducted on rodent species or
heterothermic primates (Giroud et al., 2010), but few
data are available in homeotherms and primates inhabiting highly seasonal environments. Seasonal breeding is
one potential factor in the timing of energy saving mechanisms among cercopithecoids. If breeding seasonality
evolved in response to predictable seasonal energy shortfalls, females may be selected to develop efficient fat deposition mechanisms to help them get through harsh seasonal conditions and offset the increased metabolic
requirements of reproductive effort.
Japanese macaques (Macaca fuscata) show marked
seasonal changes in body mass in response to the predictable cycle of food allocation (Kurita et al., 2002;
Hamada et al., 2003). They inhabit an environment
characterized by an extreme seasonality in terms of both
temperature and precipitation variation, and they are
found at the most northerly extent of any primate’s
range. They are widely distributed in Japan and are seasonal breeders, mating from late autumn to early winter,
and give birth from spring to early summer (Kawai,
1969). This species form multi-male/multi-female social
groups in which females mate promiscuously throughout
the mating season and mate when they are not ovulating, but with some selectivity (Huffman, 1991; Inoue and
Takenaka, 2008). Competition between males, female
mate choice (Huffman, 1992; Soltis et al., 1997a, 1997b),
male sexual coercion of females and alternative male
mating strategies (sneak copulations) are all suggested
to be important determinants of mating and reproductive success in this species (Soltis et al., 2001). Male
aggression against females both constrains female mate
choice and imposes costs on females so that coercive
aggression could increase male copulation rates through
at least two mechanisms: by overcoming female resistance (direct coercion), and/or by limiting female promiscuity (mate guarding). Several types of sexual coercion
have been identified (Smuts and Smuts, 1993; CluttonBrock and Parker, 1995; van Schaik et al., 2004): forced
copulation (violent restraint resulting in immediate mating), harassment (repeated attempts to copulate inducing eventual female submission), intimidation (physical
punishment of female refusals to mate increasing the
likelihood of submission and matings in the future) and
mate guarding (aggression at females to prevent them
from mating with other males), all of them imposing
energy costs on females. Forced copulation is not known
to occur in Japanese macaques, but harassment, intimidation, and mate guarding may occur, especially in captivity where there is less availability for sneak copulations and fewer areas to avoid male aggression (Soltis et
al., 1997a, 2001). These constraining behaviors impose
energy costs on females, in terms of energy spent to
escape from males and in terms of increased physiological stress (Muller et al., 2007). Moreover, in this species
living in relatively cold habitats, the problem of energy
sparing could be crucial. Under such ecological pressures, it should be very advantageous to accumulate fat
reserves, which can be used during temporary energy
imbalance and weight loss within a restricted breeding
season. Compared to primate species living in more tropical climates, this species could be characterized by specific behavioral and physiological adaptations and unique
fat-depositing mechanisms which have evolved to cope
with cold weather. Japanese macaques are therefore a
good model for understanding seasonal variation in fat
deposition, and the link between energetic condition and
American Journal of Physical Anthropology
Knowing the changes in body composition that accompany seasonal fluctuations in body mass is essential to
further understand the nature and the limits of the
strategy of energy economy used by female Japanese
macaques to face predicted/unpredicted food shortage
and reproductive costs, and thus regulate their energy
balance. The present study extends previous observations (Garcia et al., 2009b, 2010) of the relationship
among female nutritional status, reproductive outcome,
and social parameters in the Japanese macaque by
investigating body composition changes during two successive seasons with labeled-water technique, which is
the most precise method to establish body composition.
We specifically hypothesized that this species would use
fat-sparing strategies to adjust energy expenditure to
the behavioral and reproductive requirements of a given
season. We therefore predict that body composition and
body fat accumulation will depend on seasonality with
females accumulating fat reserves in autumn to sustain
the costs of mating activity, prepare for pregnancy, and/
or to survive under severe ecological conditions in winter. Moreover, based on previous studies showing that
dominance status may affect energetic condition
(Whitten, 1983; Smuts and Nicolson, 1989; Altmann,
1998; Gerald, 2002; Koenig, 2002; Altmann and Alberts,
2005), with low-ranking females having higher rates of
interruption during feeding bouts and higher energy expenditure, we predict that these disadvantages will
result in worse body condition for low-ranking females
compared to high-ranking ones.
Animals, housing, and diet
The subjects of this study were 14 captive female Japanese macaques (14.8 6 6.3 years of age, range 5 5–24
years) living in an outdoor corral enclosure (960 m2 with
climbing structures) at the Primate Research Institute of
Kyoto University, Inuyama, Japan. All subjects were
part of a longitudinal study of nutritional and stress
effects on reproductive outcome. In this troop, females
mate mainly between October and February, and give
birth between April and August. This cross-sectional
research was conducted at the beginning of the 2006–
2007 mating season (October 2006) and during the following birth season (May 2007). We selected all the
adult multiparous females in this group for that year
(excluding one very old female), and excluded subadult
or nulliparous females in order to avoid confounding factors due to maternal experience and maturational age.
In October 2006, the group was composed of 52 individuals consisting of 7 adult and 9 subadult males, 17 adult,
and 9 subadult females and their immature offspring (10
infants younger than 1-year-old: 7 females and 3 males).
All animals had free access to water except during the
experimental period. During the study, food was provided once daily and the individuals were fed vegetables
(sweet potatoes) and standard primate pellets.
Experimental protocol
As per the guidelines of the Primate Research Institute, all monkeys underwent yearly health assessment,
with all individuals being trapped for tattooing of
infants, tetanus inoculations, morphometrics, and collection of biological samples from all individuals. We conducted the deuterium experiment and morphometric
measurements during this health assessment in October
2006. Upon recapture, in May 2007, the same experiment was done using the same methodology. The same
investigator (CG) was responsible for all anthropometric
measurements to minimize inter-observer error.
Deuterium experiment. The females were anesthetized
with ketamine (10 mg kg21 by intramuscular injection), a
widely accepted dissociative anesthetic used in studies
requiring transient animal tranquillization. An initial 3
ml blood sample was taken at the cubital vein (for background enrichment, i.e., the natural enrichment of 2H).
Immediately after, about 0.1 g kg21 2H2O 99.9% (Wako
Pure Chemical Industries, Japan) was injected subcutaneously in the scapular region. The average quantity
injected was 0.102 g kg21 body weight (60.008, N 5 14).
After injection, the females were kept in separate cages
until the next blood sampling. Previous investigations in
macaque species indicated that the injected stable isotope
should be nearly equilibrated within 1 h of administration and fully equilibrated within 2 h (Macaca nemestrina, Kodama, 1970; Macaca mulatta: Walker et al.,
1984). Blood samples (1 ml) were therefore obtained after
an interval of 2 h. During the experimental period, the
females had no access to food or water. Upon completion
of the measurements, they were released back into their
social group as soon as any effects of the anesthesia had
worn off. Blood samples were flame-sealed into capillary
tubes immediately after collection and stored at 48C until
analysis at the Aberdeen Centre for Energy Regulation
and Obesity (Aberdeen University, Scotland). Capillaries
were vacuum-distilled (Nagy, 1983), and water from the
resulting distillate was used to produce H2 (methods in
Speakman and Król, 2005). The isotope ratios 2H/1H
were analyzed using gas source isotope ratio mass spectrometry (Optima, Micromass IRMS, Manchester, UK)
with isotopically characterized cylinder gases of H2 (CP
grade gases; BOC Ltd) in the reference channel. These
cylinder gases were characterized relative to the isotopic
standards mean ocean water (SMOW) and standard light
arctic precipitate (SLAP) (de Wit et al., 1980) supplied by
the International Atomic Energy Agency (IAEA, Vienna,
Austria). In each batch of samples for analysis, we ran
our own laboratory standards to ensure day-to-day variation in performance of the analyzer was not a significant
factor. All isotope enrichments were measured in d/ml
relative to the working standards and then converted to
ppm using the established ratios for these reference
materials. Total body water (TBW) was calculated from
the deuterium dilution space as follows:
TBW (kg) = 1,000 (Alpha D 3mass injected) =Dr D
with Alpha D = 0.899 and
Dr D ¼ðð2 H=1 HÞt2 ð2 H=1 HÞt0 Þ=eðkd 3tÞ
where t 5 times and kd 5 disappearance rate of the
The 2H2O dilution space typically overestimates by
about 4% the total body water as determined by carcass
analysis (Sheng and Huggins, 1979) while H218O dilution
space is equivalent to total body water (Lifson et al.,
1955) and provides values similar to those obtained by
direct evaluation for various species (Nagy and Costa,
1980). In the present experiment, total body water was
calculated from 2H dilution space after correction by the
factor 1.04 (Speakman et al., 1993; Speakman, 1997,
1998). Fat-free mass (FFM) was derived from TBW
assuming a hydratation coefficient of 73.2% (Pace and
Rathburn, 1945; Walker et al., 1984; Power et al., 2001;
Garcia et al., 2004). Total body fat (TBF in kg) was then
calculated from the difference between body mass and
fat-free mass.
Body measurements. A complete description of the anthropometric measurements can be found in Garcia et
al. (2010). In brief, we monitored body mass, body
length, arm and calf circumferences, and skinfold thickness at three different sites (abdominal, supra-iliac, subscapular). By summing the skinfold thickness at those
three sites, we therefore calculated the total skinfold
thickness (TS) for each individual (Hamada et al., 2003).
Female physical condition was assessed as the relationship between: 1) body mass (BM) and length using the
Quetelet Index (QI) (Bowman and Lee, 1995; Garcia et
al., 2004) defined as follows: QI 5 (BM in kg)/(crownrump length in m)2. Quetelet index approximates condition in the same way as does body mass index or BMI
(Norgan, 1987; Garcia et al., 2009a). 2) Body mass and
anterior trunk length (ATL) using the physical index
(PI) defined by Hamada et al. (1996): PI 5 1.05 3 (BM
in kg)/(ATL in mm)2.3 3 107.
Hormonal assays. We performed blood sampling and
hormonal assays in October 2006 and May 2007, as
described previously (Garcia et al., 2010). Samples were
analyzed for concentrations of leptin, having been shown
to be an indicator of nutritional status and body condition. Briefly, the leptin radioimmunoassay (Linco
Research, St. Charles, MO) had a sensitivity of 0.5 ng
ml21 with intra-assay and inter-assay coefficients of variation \10%. Hormonal analysis revealed that 2 of the
14 females were pregnant in May 2007. Leptin values
from these two pregnant females were subsequently
excluded from the analysis because of higher values compared to those from non-pregnant females.
Behavioral observations. The study subjects were part
of a longitudinal study on the determinants of reproductive success. Behavioral observations on mating activity
were conducted daily by a single observer (CG) over a
period of 15 months from the start of the 2006 mating
season (October) through December 2007. We determined if conception occurred during the first mating season (2006–2007), and the day of conception was assessed
using fecal hormone analysis (for more details, see Garcia et al., 2009b). We confirmed pregnancy by palpation
during the physical exam and by ultrasound scan during
the second experiment in May 2007. We also classified
the females as lactating or non-lactating by the presence
or absence of milk and the duration of lactation in individual females was estimated by infant ages (range 5
66–158 days in October 2006). Of 14 females available in
the group in October 2006 (9 lactating and 5 non-lactating), 2 females conceived during the 2006–2007 mating
season and gave birth to a surviving offspring. Before
the beginning of the next mating season (2007–2008),
three females were excluded from the initial sample
because of death or illness. Among the 11 females
remaining in the social group (2 lactating and 9 non-lactating), 7 females conceived during the 2007–2008 mating season and the date of conception was calculated by
subtracting 176 days of mean gestation length (Fujita et
al., 2004) from the birth date reported in the long-term
database of the Primate Research Institute.
American Journal of Physical Anthropology
TABLE 1. Body composition estimated by deuterium dilution
space at the beginning of the mating season (period 1) and
during birth season (period 2) in female Japanese macaques
Period 1 (N 5 14)
Total body water (kg)
Water content (%)
Total body fat (kg)
Body fat (%)
Fat-free mass (kg)
Fat-free mass (%)
Period 2 (N 5 10)
We also monitored female dominance rank using ad
libitum observations of the outcome of agonistic and
approach–avoidance interactions, following methods
used by Garcia et al. (2006). There was no rank reversal
between subject individuals through the study period.
Female rank was expressed as the proportion of females
dominated providing a relative rank ranging between 0
(low-ranking) and 1 (high-ranking).
Statistical analysis
Data are presented as means and standard deviations.
However, due to the small sample size (N 5 14), normal
distribution of variables with equal variances cannot be
always assumed. Where data were not normal, we used
non-parametric Mann-Whitney U tests and Wilcoxon
matched-pairs signed-ranks tests in comparisons
between groups of females and Spearman’s rank correlation coefficients for correlations. Throughout the analysis, the sample size of analyzed data varied to a small
extent due to experimental limitations. When data were
missing for any individual female, she would be excluded
from relevant analyses, although she might contribute to
other analyses where data were available. Thus sample
sizes vary in the different statistical tests. Of 14 females
available in the group at the beginning of the study, four
females had to be excluded during the second deuterium
experiment in May due to illness or experimental problems with deuterium injection. All statistical tests were
conducted with SPSS 15.0 for Windows and used twotailed probabilities with a significance level of 0.05.
Ethical considerations
All manipulations and treatments of the subjects followed Primate Research Institute animal handling
guidelines to minimize pain and distress. The small sample used here was intentional as the use of the absolute
minimum numbers of primates in any experimental procedure is the international norm. Furthermore, in the
context of the broader study, we aimed to maintain normal social and sexual behavior, and to minimize
any physiological stress associated with capture and
Relations among measures of body composition
Mean values for body composition are presented in
Table 1. The Pearson’s correlations of the individual
morphometric measures and leptin with FFM and TBF
measured by isotopic method are presented in Table 2.
We found a strong positive relationship between TBF at
the beginning of the mating season and BM, and none of
the other anthropometric measurements correlated more
American Journal of Physical Anthropology
TABLE 2. Univariate correlation matrix of body composition to
morphometric measurements, nutritional indexes, and leptin levels at the beginning of the mating season (period 1) and during
the birth season (period 2) in female Japanese macaques
Fat-free mass (kg)
Total body fat (kg)
Period 1
Period 2
Period 1
Period 2
Body mass
Crown-rump length
Arm circumference
Calf circumference
Abdominal skinfold
Suprailiac skinfold
Subscapular skinfold
Total skinfold
Quetelet Index
Physical Index
* P \ 0.05, **P \ 0.01, ***P \ 0.001 (italics 0.05\ P \ 0.1).
highly with TBF than did BM. Concerning FFM at either the beginning of the mating season or the birth season, BM was also the single best predictor. Stepwise
multiple regressions analyses were used to determine
whether combinations of the morphometric measurements could provide greater accuracy in the prediction of
TBF and FFM. Table 3 presents the amount of variance
explained and the best regression formulae for predicting lean and fat mass in this sample. We found in particular that the ability to predict TBF during the birth season was increased by combining morphometric variables,
with TBF being best predicted by BM and total skinfolds. The predicted vs. observed fat mass or fat-free
mass values showed overall mean differences of less
than 3%, which suggests that morphometric variables
were appropriate for predicting fat mass and fat-free
Energetic condition dynamics
Despite a lack of difference in the leptin levels
between the beginning of the mating season and the
birth season (Wilcoxon test: Z 5 20.51, NS), there were,
nevertheless, body mass differences with female Japanese macaques losing on average 0.65 kg between the
two seasons (beginning of the mating season: 9.03 6
1.03 kg, range 5 7.80–10.90 kg, N 5 10; birth season:
8.38 6 1.07 kg, range 5 7.30–10.10 kg, N 5 10; Z 5
22.81, P 5 0.005), i.e., about 7% of their body mass
(range 5 0.98–19.78%). On the one hand, fat-free mass
remained unchanged between the two seasons (7.31 6
0.54 kg vs. 7.29 6 0.78 kg; Z 5 20.18, NS, N 5 10). On
the other hand, total body fat and percent body fat were
different between the two seasons (beginning: TBF: 1.72
6 0.55 kg, range 5 1.11–2.72 kg, percent body fat:
18.70% 6 4.08%, range 5 13.55–24.94%, N 5 10; birth
season: TBF: 1.09 6 0.42 kg, range 5 0.63–1.59 kg, percent body fat: 12.67% 6 3.99%, range 5 8.49–19.23%, N
5 10; Z 5 22.80, P 5 0.005), with females being significantly leaner during the birth season. Because of
the small sample size, the observed percent body fat
differences between the two seasons were absent when
considering non-lactating females only, but were still
significant for lactating females (Z 5 22.53, P 5 0.012),
with the mean differences reported in non-lactating
females being comparable to those in lactating ones
(6.87% 6 3.10%, N 5 2 vs. 5.81% 6 2.80%, N 5 8). On
TABLE 3. Regression formulae for total body fat (TBF) and fat-free mass (FFM) in female Japanese macaques
0.476 3 (BM) 2 2.554
0.193 3 (BM) 1 0.135 3 (TS) 2 1.717
0.524 3 (BM) 1 2.554
0.685 3 (BM) 1 1.551
BM, body mass; TS, total skinfold; SEE, standard error of estimate.
Beginning of the mating season. b Birth season.
TABLE 4. Linear, quadratic, and cubic curve fit statistics for fat
mass and fat-free mass at the beginning of the mating
season with age
Fat mass
Linear 0.362 0.460 0.023 b 5 20.053
Quadratic 0.372 0.477 0.077 b 5 20.107
c 5 0.002
0.466 0.461 0.087 b 5 0.477
c 5 20.043
d 5 0.001
0.427 0.476 0.011 b 5 20.063
Quadratic 0.452 0.486 0.036 b 5 0.028
c 5 20.003
0.649 0.408 0.012 b 5 0.949
c 5 20.074
d 5 0.002
SEE 5 standard error of estimate.
Fig. 1. Linear regression of total body fat at the beginning
of the mating season against age in 14 female Japanese
average, females lost 32.53% (612.93) of their body fat
between the two seasons (range 5 10.35–53.97%), and
there was no difference between lactating and nonlactating females (Mann-Whitney test: U 5 5.00, NS,
N 5 10). Among lactating females, there was a trend for
an effect of lactation stage on body fat loss between the
two seasons, with females in mid-lactation (i.e., with
infants aged between 3 and 5 months) at the beginning
of the mating season losing a larger proportion of fat
than females in late lactation (with infants above
the age of 5 months) at the beginning of the mating season (35.70% 6 12.67% vs. 14.13% 6 5.34%, U 5 0.00,
P 5 0.064).
To examine inter-individual variation in body condition with age, we fitted curves for BM, FFM, and TBF
against age in years for all females using a curve-fit process. We used polynomials least-squares fitting and compared linear, quadratic, and cubic regressions. There
was a negative linear relationship between BM at the
beginning of the mating season and age (r 5 20.656,
P 5 0.011, N 5 14). A linear negative association was
also observed between age and TBF at the beginning of
the mating season (r 5 20.602, P 5 0.023, Fig. 1 and
Table 4) and we found a third-order polynomial relationship between FFM measured at the beginning of the
mating season and age (r2 5 0.649, P 5 0.012, Fig. 2
and Table 4). We reported a trend for a relationship
between age and leptin levels at the beginning of the
mating season (see Garcia et al., 2010). There was no
significant association between age and any of the body
composition measurements (BM, FFM, and TBF) or lep-
Fig. 2. Third-order polynomial regression of fat-free mass at
the beginning of the mating season against age in 14 female
Japanese macaques.
tin levels during the birth season, i.e., when females
were lighter and leaner. Nevertheless, we found a cubic
relationship between age and %BF loss between the two
seasons (r2 5 0.755, P 5 0.029).
We found an inverse correlation between rank and
%BF at the beginning of the mating season (rs 5
20.534, P 5 0.049, N 5 14), with a tendency for a relationship between rank and BM (rs 5 20.504, P 5 0.066,
N 5 14). There was no relationship between rank and
leptin levels and there was no correlation between delta
mass (i.e., the difference between BM at the beginning of
the mating season and BM during the birth season) or
delta fat mass and rank (rs 5 20.455 and rs 5 20.248
American Journal of Physical Anthropology
Body composition in female Japanese macaques
and comparison with other primates
Fig. 3. Quetelet index during the birth season 2007 for
females who conceived (N 5 7) during the following mating season (2007–2008), compared to those that did not conceive (N 5
4). Plot shows median (bar), interquartile range (box), and highest and lowest values (whiskers).
respectively, NS). There was a slight trend for an effect
of rank on relative mass loss (100 3 (BM1 - BM2)/BM1)
between the two seasons with low-ranking females tending to lose proportionally more mass than high-ranking
ones (rs 5 20.503, P 5 0.09, N 5 12).
Nutritional status and reproduction
Despite a difference in subscapular skinfolds between
lactating (4.83 6 0.61 mm) and non-lactating females
(4.00 6 0.61 mm) at the beginning of the mating season
(U 5 7.00, P 5 0.035, N 5 14), there was, nevertheless,
no effect of lactation status on %BF at either the
beginning of the mating season or during the birth season (U 5 13.00, N 5 14, NS and U 5 8.00, N 5 10, NS).
Neither baby age nor baby sex was associated with TBF
or FFM. Of 14 females available in the group in 2006, 3
females were excluded as dead or ill during the 2007–
2008 mating season. Among the 11 females remaining in
the social group at the beginning of the 2007–2008 mating season, we found that females who conceived during
this mating season (N 5 7) had a larger Quetelet Index
(Fig. 3; U 5 1.00, P 5 0.014) and higher TBF during the
previous birth season than did females who did not conceive (U 5 0.00, P 5 0.040). We also found that females
with higher TBF at the beginning of the previous
mating season (2006–2007) were more likely to conceive
during the next mating season (P 5 0.072, N 5 11). Predictors of conception status for the 2007–2008 mating
season were also analyzed by entering morphometric
measures into a logistic regression along with fertility in
the previous year as statistical control. When birth in
2007 and Quetelet Index (during birth season 2007)
were entered in the model together (v2 5 8.36, P 5
0.004), Quetelet Index was still significant (P 5 0.022)
but birth status in the previous year was not a significant predictor. Moreover, percent body fat in May 2007
was not a good predictor of birth date within the following birth season (rs 5 0.071, NS).
American Journal of Physical Anthropology
The purpose of our study was not only to examine the
relations among reproduction and energetic status in a
sample of captive female Japanese macaques but also to
provide a comparative study of the relations among various body composition techniques. The estimation of
nutritional status in primates has generally been
inferred from morphometrics (Bercovitch, 1987; Campbell and Gerald, 2004) and specifically from measurements of body mass. However, body mass may not necessarily be the best estimator of body fat, since age, sex,
reproductive state, muscle mass, and bone density can
all affect the relationship between mass and fat levels
and thereby reduce the accuracy of body fat estimates.
Various other methods are also used to assess the
nutritional status of captive and wild animals such as
carcass analysis (Lewis et al., 1986; Rutenberg et al.,
1987; Zihlman and McFarland, 2000), dual energy X-ray
absorptiometry (DEXA) (Hamada et al., 2003; Takahashi
et al., 2006), total body electroconductivity (TOBEC)
(Power et al., 2001), blood sampling to assess insulin,
leptin, or cholesterol levels (Chen et al., 2002; Kemnitz
et al., 2002; Muehlenbein et al., 2005; Takahashi et al.,
2006; Whitten and Turner, 2008; Garcia et al., 2010),
and urine sampling to measure ketones or C-peptide
(Knott, 1998; Sherry and Ellison, 2007; Deschner et al.,
2008). Determination of nutritional status and energy
balance can also be monitored by using the labeled-water
technique (Altmann et al., 1993; Garcia et al., 2004;
Blanc et al., 2005; Schmid and Speakman, 2009; Simmen
et al., 2010). The main advantage of this isotope-based
method over alternative techniques is that it permits the
study of subjects living unrestricted in their natural
environment. However, a reliance on blood samples as
the source of body water in which to measure the concentrations of the isotopes used in the technique, 2H and
O, has restricted application of this method to captive
animals or animals easy to catch.
Our comparative study of nutritional status in
Japanese macaques involved use of three techniques:
anthropometry, blood sampling to assess leptin levels,
and labeled-water dilution. This is the first study presenting body composition data using the stable isotope
method in the Japanese macaque. Leptin correlated very
poorly with total body fat measured with isotopic method
but anthropometric measurements, such as body mass
and skinfold thickness, could provide valid estimates of
total body fat, as suggested in previous studies using
DEXA (Colman et al., 1999; Hamada et al., 2003; Takahashi et al., 2006). Given the results obtained with the
deuterium technique, the anthropometric measurements,
even though less precise, remain a valid method for estimating body condition because it provides an easy, inexpensive, and non-invasive way of doing serial evaluations of body composition changes.
These female Japanese macaques varied in estimated
percent body fat from 8.5 to 24.9% (18% on average at
the beginning of the mating season and about 13% during the birth season). If we consider our findings in light
of the available literature for cercopithecoid primates
and with respect to similarities and differences with
humans, percent body fat of our captive females was
well within the range found in several groups of primates previously studied (18.3% for multiparous female
rhesus macaques (Walker et al., 1984); 1.9% for
wild-feeding baboons and 23.2% for garbage-feeding
baboons (Altmann et al., 1993); 16.9% for captive
baboons (Rutenberg et al., 1987); 20% in captive
baboons (Comuzzie et al., 2003)), and none of our animals were obese (obesity defined as [27% body fat:
Hamada et al., 2003). Our results were also in the range,
though lower than those observed in humans (Heymsfield et al., 2005: mean percent body fat of 27.6% in a
Reference Caucasian Woman). It seems that non-human
primates can become as fat as humans under environmental circumstances of low physical activity and abundant food supply, which are associated with provisioning
and captivity and are similar to those of affluent societies (Altmann et al., 1993; Dufour and Sauther, 2002).
While sparse, data from non-human primates seem to
suggest that fat deposition in humans is only slightly
greater than in non-human primates (Dufour and
Sauther, 2002) and this supports the view that an abundance of body fat is an evolutionarily derived condition
for modern humans and that lower levels of body fat
may have been the norm during most of human evolution. However, it remains to be demonstrated whether
the characteristic fat deposition in humans is a unique
trait, shared with other primate species but manifested
to a greater extent, i.e., a difference of evolutionary relevance between human and non-human primates, or
whether it is a more recent result of certain cultural
changes such as food storage and agriculture. Moreover,
even if data on percent body fat in captive female primates overlap considerably those reported in human
females, the anatomical distribution of body fat in different regions or compartments of the body (i.e., subcutaneous adipose tissue vs. abdominal visceral adipose tissue)
may differ between human and non-human primates
and further studies on that topic may help determine if
the relatively large fat reserves accumulated by humans
can be considered a distinctive feature of the species.
Rank and age effects on body composition
Given that dominance rank is often presumed to confer
priority of access to resources (Whitten, 1983; Altmann,
1998; Gerald, 2002; Koenig, 2002), we hypothesized that
dominant females would exhibit greater fat reserves that
subordinate ones. Contrary to this prediction, we found
that there was an inverse relationship between social
rank and body fatness, but that low-ranking females
tended to lose proportionally more mass between the two
seasons. Energy cost of lactation and infant growth rates
may underlie at least some of the variation in body condition with rank. The conversion of maternal nutrients or
body reserves to milk may differ between dominant and
subordinate females. There could be differential postnatal
maternal expenditure in terms of milk input or gross
energy transfer, or even different extraction and conversion of maternal resources by infants of high and lowranking females. Then, there could be complex deterministic processes involved in the relationship between rank
and body condition. Further investigation of the role of
dominance rank and social stress is therefore warranted
and a close hormonal monitoring of social stress is currently underway to assess exposure to chronic stress and
its relationship to body condition.
According to previous studies (Glassman and Coelho,
1987; Rutenberg et al., 1987; Campbell and Gerald,
2004), body mass and body fat declined as a function of
age. However, our investigation was cross-sectional, and
our sample did not contain enough older individuals for
complete analysis of this relation. Therefore, these
results should be viewed with these methodological limitations in mind and further studies are needed to determine if our current findings can be generalized to other
populations of Japanese macaques, especially in the
wild. Whether such relationships between age and body
condition translate into differences in reproductive performance between young and old females, and whether
older females do not have enough fat reserves to cover
the energetic costs of reproduction, still warrant further
Seasonality in nutritional status
We have reported a large seasonal fluctuation in body
mass and fat levels. These results are in agreement with
previous studies in Verreaux’s sifaka (Richard et al.,
2000), brown mouse lemurs and ring-tailed lemurs
(Randrianambinina et al., 2003; Simmen et al., 2010),
showing that body mass fluctuated with the seasons and
that individuals needed to attain a sufficient physical
condition prior to the long dry season. According to our
hypothesis, there was an impact of seasonal breeding on
body condition with females gaining weight and accumulating energy reserves in fall to prepare for mating activity and the next conception, and/or to survive under
severe conditions in winter with high thermoregulatory
costs (Nakagawa, 1997; Muroyama et al., 2006). As suggested by Hamada et al. (2003), it seems that body fat
accumulation and loss depend on a physiological mechanism based on a fixed circannual cyclicity. Japanese macaques may have been selected to respond to body composition changes over the course of the mating and breeding season.
These results confirmed that even in captive individuals with constant food, nutritional status was markedly
influenced by season. Seasonal changes in nutritional
status thus may not necessarily be related to seasonal
fluctuations in energy and protein intake from natural
foods but may also be influenced by differences in energy
expenditure and energy balance caused by seasonal
changes in resource allocation strategies, activity budgets, and thermoregulation (Nagy and Milton, 1979; Agetsuma, 2000). There is an increase in energy expenditure
for thermoregulation in winter, with energy expenditure
of Japanese macaques at 58C being 2.5 times more important than that at 298C (Nakayama et al., 1971). If
this increase is not counterbalanced by an increase in
energy intakes, it may lead to a temporary negative
energy balance associated with a depleted condition and
potential consequences for reproductive success and survival. Moreover, Bercovitch (1997) has shown that activity budgets differed between the seasons in captive male
rhesus macaques, with feeding time plunging from 17 to
8% of the day between the non-mating and mating
season. These changes occurred despite the availability
of a constant quantity of monkey chow throughout the
year. Therefore, feeding strategies may have direct
repercussions on nutritional status, with time and
energy devoted to mating probably corresponding to
reduced time spent feeding.
Most of the decrease in mass between the two seasons
was due to a decrease in fat reserves, suggesting that
females spared fat-free mass, i.e., protein mass, and
relied on fatty acids for energy over the course of the
American Journal of Physical Anthropology
mating season. Endogenous lipid reserve constituted the
primary source of energy used and the relatively high
fat mass level in fall seemed to be sufficient to cover
energy costs. Therefore fat-free mass was not used to
meet energy needs and maintain a stable energy balance, indicating that there was no protein oxidation in
lean females.
for their technical assistance in handling and nursing the
animals during the experimental period. They further
thank S. Hayakawa, S. Higaki, T. Kunieda, C.A.D. Nahallage, and K. Takumi for assistance in anthropometric
measurements and blood sampling. They thank Y. Hamada for allowing using his anthropometric equipment. The
comments of two anonymous reviewers and editors also
greatly improved an earlier draft of this article.
Energetics and reproductive effort
Reproductive status of a female is another factor
potentially influencing body condition, as the energy
costs of carrying and suckling an infant add to the costs
of maintenance. In this study, lactating females had
larger subscapular skinfolds than did non-lactating ones
suggesting that fatter, better condition females are those
who could afford the demands of lactation and reproduce
more rapidly (Johnson and Kapsalis, 1995; Campbell
and Gerald, 2004). However, we were unable to document any differences in body fat between lactating and
non-lactating females. We cannot completely rule out the
possibility that the small sample size and the corollary
lack of power may have obscured the relationship
between body fatness and lactation status. However,
females in mid-lactation tended to lose a larger proportion of fat between the two seasons than females in late
lactation suggesting that this period of peak lactation
and maximum infant growth rate represents the highest
energetic costs to the mother (Oftedal, 1984; Lee, 1987).
The energy invested in lactation determines infant
growth rates and may determine in part the delay
between reproductive events (Garcia et al., 2009a), with
a trade-off between investment in current and future
Our results suggested that not only did the reproductive status of the female influence her body condition but
also that condition played a role in reproductive success
and fecundity. Physiological modulation of reproductive
outcome in females starts with mechanisms that adjust
the probability of conception in response to maternal
energy availability. We found that differences in conception rates were associated with differences in body fat
and body condition, suggesting that females with a
higher energy status were those who could afford to
reproduce more rapidly. These results are in agreement
with previous studies showing that in sifakas, female
body mass at the outset of the mating season strongly
influenced the probability to give birth to an infant that
survived the dry season and weaning (Richard et al.,
2000; Lewis and Kappeler, 2005). This suggests that
female condition influences competence and quality of
ovarian cycles, with individual variation in condition
and energy balance appearing to play a significant role
in reproductive potential (Garcia et al., 2006). Although
energy is not the only limiting resource to be considered
in optimizing reproductive effort, it is certainly the principal one for primates as for other organisms (Ellison,
2003). However, due to the small sample size, we
were unable to document any effect of body fat on infant
birth dates the following year, and thus infant survival
and further studies are therefore required to clarify
this issue.
The authors thank the staff of the Center for Human
Evolution Modeling Research, especially the veterinarians,
American Journal of Physical Anthropology
Agetsuma N. 2000. Influence of temperature on energy intake
and food selection by macaques. Int J Primatol 21:103–111.
Altmann J, Alberts SC. 2005. Growth rates in a wild primate
population: ecological influences and maternal effects. Behav
Ecol Sociobiol 57:490–501.
Altmann J, Schoeller D, Altmann SA, Muruthi P, Sapolsky RM.
1993. Body size and fatness of free-living baboons reflect food
availability and activity levels. Am J Primatol 30:149–161.
Altmann SA. 1998. Foraging for survival: yearling baboons in
Africa. Chicago: University of Chicago Press.
Banks WA, Phillips-Conroy JE, Jolly CJ, Morley JE. 2001.
Serum leptin levels in wild and captive populations of
baboons (Papio): implications for the ancestral role of leptin. J
Clin Endocrinol Metab 86:4315–4320.
Bercovitch FB. 1987. Female weight and reproductive condition
in a population of olive baboons (Papio anubis). Am J Primatol 12:189–195.
Bercovitch FB. 1997. Reproductive strategies of rhesus macaques. Primates 38:247–263.
Blanc S, Colman R, Kemnitz J, Weindruch R, Baum S, Ramsey
J, Schoeller D. 2005. Assessment of nutritional status in rhesus monkeys: comparison of dual-energy X-ray absorptiometry
and stable isotope dilution. J Med Primatol 34:130–138.
Bowman JE, Lee PC. 1995. Growth and threshold weaning
weights among captive rhesus macaques. Am J Phys Anthropol 96:159–175.
Campbell BC, Gerald MS. 2004. Body composition, age and fertility among free-ranging female rhesus macaques (Macaca
mulatta). J Med Primatol 33:70–77.
Chen Y, Ono F, Yoshida T, Yoshikawa Y. 2002. Relationship
between body weight and hematological and serum biochemical parameters in female cynomolgus monkeys (Macaca fascicularis). Exp Anim 51:125–131.
Clutton-Brock TH, Parker GA. 1995. Sexual coercion in animal
societies. Anim Behav 49:1345–1365.
Colman RJ, Hudson JC, Barden HS, Kemnitz JW. 1999. A comparison of dual-energy X-ray absorptiometry and somatometrics for determining body fat in rhesus macaques. Obes Res
Comuzzie AG, Cole SA, Martin L, Carey KD, Mahaney MC,
Blangero J, VandeBerg JL. 2003. The baboon as a nonhuman
primate model for the study of the genetics of obesity. Obes
Res 11:75–80.
De Souza MJ, Lee DK, VanHeest JL, Scheid JL, West SL, Williams NI. 2007. Severity of energy-related menstrual disturbances increases in proportion to indices of energy conservation in exercising women. Fertil Steril 88:971–975.
De Wit JC, van der Straaten CM, Mook WG. 1980. Determination of the absolute isotopic ratio of V-SMOW and SLAP.
Geostand Newslett 4:33–36.
Deschner T, Kratzsch J, Hohmann G. 2008. Urinary C-peptide
as a method for monitoring body mass changes in captive
bonobos (Pan paniscus). Horm Behav 54:620–626.
Dewey KG. 1998. Effects of maternal caloric restriction and
exercise during lactation. J Nutr 128:386S–389S.
Dufour DL, Sauther ML. 2002. Comparative and evolutionary
dimensions of the energetics of human pregnancy and lactation. Am J Hum Biol 14:584–602.
Ellison PT. 2003. Energetics and reproductive effort. Am J Hum
Biol 15:342–351.
Fujita S, Sugiura H, Mitsunaga F, Shimizu K. 2004. Hormone
profiles and reproductive characteristics in wild female
Japanese macaques (Macaca fuscata). Am J Primatol 64:367–
Garcia C, Huffman M, Shimizu K. 2010. Seasonal and reproductive variation in body condition in captive female Japanese
macaques (Macaca fuscata). Am J Primatol 72:277–286.
Garcia C, Lee PC, Rosetta L. 2006. Dominance and reproductive
rates in captive female olive baboons, Papio anubis. Am J
Phys Anthropol 131:64–72.
Garcia C, Lee PC, Rosetta L. 2009a. Growth in colony living
anubis baboon infants and its relationship with maternal activity budgets and reproductive status. Am J Phys Anthropol
Garcia C, Rosetta L, Ancel A, Lee PC, Caloin M. 2004. Kinetics
of stable isotope and body composition in olive baboons (Papio
anubis) estimated by deuterium dilution space: a pilot study.
J Med Primatol 33:146–151.
Garcia C, Shimizu K, Huffman M. 2009b. Relationship between
sexual interactions and the timing of the fertile phase in captive female Japanese macaques (Macaca fuscata). Am J Primatol 71:868–879.
Gerald MS. 2002. Social status correlates inversely with feedingpriority amongst pairs of unfamiliar adult male vervet monkeys (Cercopithecus aethiops sabaeus). Primates 43:127–132.
Giroud S, Perret M, Stein P, Goudable J, Aujard F, Gilbert C,
Robin JP, Le Maho Y, Zahariev A, Blanc S, Momken I. 2010.
The grey mouse lemur uses season-dependent fat or protein
sparing strategies to face chronic food restriction. PloS ONE
Glassman DM, Coelho AM. 1987. Principal components analysis
of physical growth in savannah baboons. Am J Phys Anthropol 72:59–66.
Hamada Y, Hayakawa S, Suzuki J, Watanabe K, Ohkura S.
2003. Seasonal variation in the body fat of Japanese macaques Macaca fuscata. Mamm Stud 28:79–88.
Hamada Y, Watanabe T, Iwamoto M. 1996. Morphological variation among local populations of the Japanese macaque
(Macaca fuscata). In: Shotake T, Wada K, editors. Variations
in the Asian macaques. Tokyo: Tokai University Press. p 97–
Heymsfield SB, Lohman TG, Wang Z, Going SB. 2005. Human
body composition. Champaign, IL: Human Kinetics.
Huffman MA. 1991. Mate selection and partner preferences in
female Japanese macaques. In: Fedigan LM, Asquith PJ, editors.
The monkeys of Arashiyama: thirty-five years of
research in Japan and the West. Albany, NY: State University
of New York Press. p 101–122.
Huffman MA. 1992. Influences of female partner preference on
potential reproductive outcome in Japanese macaques. Folia
Primatol 59:77–88.
Inoue E, Takenaka O. 2008. The effect of male tenure and
female mate choice on paternity in free-ranging Japanese
macaques. Am J Primatol 70:62–68.
Johnson RL, Kapsalis E. 1995. Determinants of postnatal
weight in infant rhesus monkeys: implications for the study of
inter-individual differences in neonatal growth. Am J Phys
Anthropol 98:343–353.
Kawai M. 1969. Ecology of Japanese Monkeys. Tokyo: KawadeShobo-Shinsha.
Kemnitz JW, Sapolsky RM, Altmann J, Muruthi P, Mott GE,
Stefanick ML. 2002. Effects of food availability on serum insulin and lipid concentrations in free-ranging baboons. Am J
Primatol 57:13–19.
Key C, Ross C. 1999. Sex differences in energy expenditure in
non-human primates. Proc R Soc Lond B 266:2479–2485.
Kodama AM. 1970. Total body water of the pigtailed macaque,
Macaca nemestrina. J Appl Physiol 29:260–262.
Knott CD. 1998. Changes in orangutan caloric intake, energy
balance, and ketones in response to fluctuating fruit availability. Int J Primatol 19:1061–1079.
Koenig A. 2002. Competition for resources and its behavioral
consequences among female primates. Int J Primatol 23:759–
Kurita H, Shimomura T, Fujita T. 2002. Temporal variation in
Japanese macaque bodily mass. Int J Primatol 23:411–428.
Lee PC. 1987. Nutrition, fertility and maternal investment in
primates. J Zool Lond 213:409–422.
Lee PC. 1996. The meanings of weaning: growth, lactation, and
life history. Evol Anthropol 5:87–98.
Lewis DS, Bertrand HA, Masoro EJ. 1986. Total body water-tolean body mass ratio in baboons (Papio sp.) of varying adiposity. J Appl Physiol 61:1234–1236.
Lewis RJ, Kappeler PM. 2005. Seasonality, body condition, and
timing of reproduction in Propithecus verreauxi verreauxi in
the Kirindy forest. Am J Primatol 67:347–364.
Lifson N, Gordon GB, McClintock R. 1955. Measurement of
total carbon dioxide production by means of D2O18. J Appl
Physiol 7:704–710.
Loucks AB, Thuma JR. 2003. Luteinizing hormone pulsatility is
disrupted at a threshold of energy availability in regularly
menstruating women. J Clin Endocrinol Metab 88:297–311.
Mori A. 1979. Analysis of population changes by measurement
of body weight in the Koshima Troop of Japanese monkeys.
Primates 20:371–391.
Muehlenbein MP, Campbell BC, Richards RJ, Watss DP, Svec F,
Falkenstein KP, Murchison MA, Myers L. 2005. Leptin, adiposity, and testosterone in captive male macaques. Am J Phys
Anthropol 127:335–341.
Muller MN, Kahlenberg SM, Emery Thompson M, Wrangham
R. 2007. Male coercion and the costs of promiscuous mating
for female chimpanzees. Proc R Soc B 274:1009–1014.
Muroyama Y, Kanamori H, Kitahara E. 2006. Seasonal variation and sex differences in the nutritional status in two local
populations of wild Japanese macaques. Primates 47:355–364.
Nagy KA. 1983. Doubly-labelled water: a guide to its use. Los
Angeles: UCLA Publications.
Nagy KA, Costa DP. 1980. Water flux in animals: analysis of
potential errors in the tritiated water method. Am J Physiol
Nagy KA, Milton K. 1979. Energy metabolism and food consumption by wild howler monkeys (Alouatta palliata). Ecology
Nakagawa N. 1997. Determinants of the dramatic seasonal
changes in the intake of energy and protein by Japanese
monkeys in a cool temperate forest. Am J Primatol 41:268–
Nakayama T, Hori T, Nagasaka T, Tokura H, Tadaki E. 1971.
Thermal and metabolic responses in the Japanese monkey at
temperatures of 5–388C. J Appl Physiol 31:332–337.
Norgan NE. 1987. Human body composition and fat distribution. Euro/Nut report 8. The Hague: CIP-gegevens Koninklijke Bibliotheek.
Oftedal OT. 1984. Milk composition, milk yield and energy output at peak lactation: a comparative review. Symp Zool Soc
Lond 51:33–85.
Pace N, Rathburn EN. 1945. Studies on body composition III:
The body water and chemically combined nitrogen content in
relation to fat content. J Biol Chem 158:685–691.
Power RA, Power ML, Layne DG, Jaquish CE, Oftedal OT, Tardif SD. 2001. Relations among measures of body composition,
age, and sex in the common marmoset monkey (Callithrix jacchus). Comp Med 51:218–223.
Pusey AE, Oehlert GW, Williams JM, Goodall J. 2005. Influence
of ecological and social factors on body mass of wild chimpanzees. Int J Primatol 26:3–31.
Randrianambinina B, Rakotondravony D, Radespiel U, Zimmermann E. 2003. Seasonal changes in general activity, body
mass and reproduction of two small nocturnal primates: a
comparison of the golden brown mouse lemur (Microcebus
ravelobensis) in northwestern Madagascar and the brown
mouse lemur (Microcebus rufus) in eastern Madagascar. Primates 44:321–331.
Richard AF, Dewar RE, Schwartz M, Ratsirarson J. 2000. Mass
change, environmental variability and female fertility in wild
Propithecus verreauxi. J Hum Evol 39:381–391.
Rousseau K, Atcha Z, Loudon SI. 2003. Leptin and seasonal
mammals. J Neuroendocrinol 15:409–414.
American Journal of Physical Anthropology
Rutenberg GW, Coelho AM, Lewis DS, Dee Carey K, McGill HC.
1987. Body composition in baboons: evaluating a morphometric method. Am J Primatol 12:275–285.
Schmid J, Speakman JR. 2009. Torpor and energetic consequences in free-ranging grey mouse lemurs (Microcebus murinus):
a comparison of dry and wet forests. Naturwissenschaften
Schneider JE. 2004. Energy balance and reproduction. Physiol
Behav 81:289–317.
Sheng HP, Huggins RA. 1979. A review of body composition
studies with emphasis on total body water and fat. Am J Clin
Nutr 32:630–647.
Sherry DS, Ellison PT. 2007. Potential applications of urinary
C-peptide of insulin for comparative energetics research. Am
J Phys Anthropol 133:771–778.
Simmen B, Bayart F, Rasamimanana H, Zahariev A, Blanc S,
Pasquet P. 2010. Total energy expenditure and body composition in two free-living sympatric lemurs. PLoS One 5:e9860.
Smuts B, Nicolson N. 1989. Reproduction in wild female olive
baboons. Am J Primatol 19:229–246.
Smuts B, Smuts RW. 1993. Male aggression and sexual coercion
of females in nonhuman primates and other mammals:
evidence and theoretical implications. Adv Stud Behav
Soltis J, Mitsunaga F, Shimizu K, Yanagihara Y, Nozaki M.
1997a. Sexual selection in Japanese macaques I: female mate
choice or male sexual coercion? Anim Behav 54:725–736.
Soltis J, Mitsunaga F, Shimizu K, Nozaki M, Yanagihara Y,
Domingo-Roura X, Takenaka O. 1997b. Sexual selection in
Japanese macaques II: female mate choice and male-male
competition. Anim Behav 54:737–746.
Soltis J, Thomsen R, Osamu T. 2001. The interaction of male
and female reproductive strategies and paternity in wild
Japanese macaques, Macaca fuscata. Anim Behav 62:485–
American Journal of Physical Anthropology
Speakman JR. 1997. Doubly labelled water: theory and practice.
London: Chapman and Hall.
Speakman JR. 1998. The history and theory of the doubly
labelled water technique. Am J Clin Nutr 68:932S–938S.
Speakman JR, Król E. 2005. Comparison of different approaches
for the calculation of energy expenditure using doubly labeled
water in a small animal. Physiol Biochem Zool 78:650–667.
Speakman JR, Nair KS, Goran MI. 1993. Revised equations for
calculating CO2 production from doubly labelled water in
humans. Am J Physiol 264:E912–E917.
Takahashi T, Higashino A, Takagi K, Kamanaka Y, Abe M, Morimoto M, Kang KH, Goto S, Suzuki J, Hamada Y, Kageyama
T. 2006. Characterization of obesity in Japanese monkeys
(Macaca fuscata) in a pedigreed colony. J Med Primatol
van Schaik CP, Pradhan GR, van Noordwijk MA. 2004. Mating
conflict in primates: infanticide, sexual harassment and
female sexuality. In: Kappeler P, van Schaik CP, editors.
Sexual selection in primates: new and comparative perspectives. Cambridge, UK: Cambridge University Press. p 131–
Walker ML, Schwartz SM, Wilson ME, Musey PI. 1984. Estimation of body fat in female rhesus monkeys. Am J Phys Anthropol 63:323–329.
Whitten PL. 1983. Diet and dominance among female vervet
monkeys (Cercopithecus aethiops). Am J Primatol 5:139–159.
Whitten PL, Turner TR. 2008. Ecological and reproductive
variance in serum leptin in wild vervet monkeys. Am J Phys
Anthropol 137:441–448.
Williams NI, Berga SL, Cameron JL. 2007. Synergism between
psychosocial and metabolic stressors: impact on reproductive
function in cynomolgus monkeys. Am J Physiol Endocrinol
Metab 293:E270–E276.
Zihlman AL, McFarland RK. 2000. Body mass in lowland gorillas: a quantitative analysis. Am J Phys Anthropol 113:61–78.
Без категории
Размер файла
213 Кб
breeding, japanese, macaque, fuscata, energetic, female, macaca, consequences, seasonal
Пожаловаться на содержимое документа