ANIMAL BEHAVIOUR, 2001, 62, 485–494
doi:10.1006/anbe.2001.1774, available online at http://www.idealibrary.com on
The interaction of male and female reproductive strategies and
paternity in wild Japanese macaques, Macaca fuscata
JOSEPH SOLTIS*, RUTH THOMSEN† & OSAMU TAKENAKA‡
*Department of Ecology and Social Behavior, Primate Research Institute, Kyoto University
†Department of Zoology, University of Munich
‡Department of Cellular and Molecular Biology, Primate Research Institute, Kyoto University
(Received 28 August 2000; initial acceptance 25 October 2000;
final acceptance 1 March 2001; MS. number: A8867)
Japanese macaques reside in large, mixed-sex social groups in which various reproductive strategies of
both sexes operate simultaneously. This report represents the first study combining behavioural and
genetic data to examine the interaction of male and female reproductive strategies in primates (N=15
adult males, N=15 adult females, Yakushima Island, Japan). During one mating season, socially dominant
males monopolized most female matings. Furthermore, the six offspring sired by troop males were more
likely sired by higher-ranking males than lower-ranking males. Nontroop males sired three additional
offspring in the troop. Lower-ranking troop males avoided direct competition with higher-ranking males
by engaging in sneak copulations with females outside of the presence of other males. Also, females
expressed mate choice behaviour towards multiple males of various dominance ranks. Thus, the female
strategy of attempting to mate with multiple males conflicted with the mate-guarding strategy of
high-ranking males. Despite some female mate choice for mid- and low-ranking males and alternative
male mating tactics by subordinate males, high-ranking males were able to monopolize most, but not all,
within-troop mating and paternity. This result was due in part to the low number of females mating at
the same time. The mean number of females displaying mating behaviour per day was 2.42 (range 1–5),
and higher-ranking males more successfully monopolized females on days when fewer females were
mating. The number of females mating simultaneously influences the outcome of reproductive conflicts
between the sexes.

correlated with mating success (Cowlishaw & Dunbar
1991; Bercovitch 1992a, b; Dunbar & Cowlishaw 1992).
Recently, analysis of DNA or immediate gene products
has allowed for more accurate assessment of paternity.
Similarly, male dominance rank and number of offspring sired are usually positively correlated, with various
levels of statistical significance (e.g. nonwild: Smith 1981,
1993; Inoue et al. 1990, 1993; Paul & Kuester 1996; Soltis
et al. 1997b; wild: Melnick 1987; Pope 1990; Ohsawa
et al. 1993; de Ruiter et al. 1994), but rarely negatively
correlated (e.g. nonwild: Shively & Smith 1985).
Male dominance rank does not explain all of the
variance in male mating and reproductive success, however. Additional sources of variation in male reproductive success include alternative male mating tactics
(Rubenstein 1980) and female mate choice (Small 1993;
Andersson 1994). In primates, for example, there is evidence that low-ranking and nongroup males use alternative tactics such as sneak copulations to obtain matings
(e.g. Dunbar 1984; Ohsawa et al. 1993; Berard et al. 1994;
Manson 1996).
Animals living in mixed-sex social groups, such as many
primates (Dixson 1998), pose a challenge for those studying sexual selection because of the simultaneous operation
of many reproductive strategies, such as competition
among males, female mate choice, alternative tactics by
subordinate males and male sexual coercion of females.
Competition among males for access to females is
common in animals (e.g. Le Boeuf & Peterson 1969;
Clutton-Brock et al. 1982). Among primates, the relationship between male dominance rank and reproductive
success is not as straightforward as in other animals (Ellis
1993). Nevertheless, male dominance rank is usually
positively correlated with mating success, with various
levels of statistical significance, but rarely negatively
Correspondence: J. Soltis, National Institutes of Health, Laboratory of
Comparative Ethology, NIH Animal Center, Box 529, Poolesville, MD
20837, U.S.A. (email: soltisj@mail.nih.gov). R. Thomsen is at the
Department of Zoology, LM-University of Munich, Luisenstrasse 14,
80333, Munich, Germany. Osamu Takenaka is at the Department of
Cellular and Molecular Biology, Primate Research Institute, Kyoto
University, Aichi 484-0081, Japan.
0003–3472/01/090485+10 $35.00/0
2001 The Association for the Study of Animal Behaviour
485

2001 The Association for the Study of Animal Behaviour
486
ANIMAL BEHAVIOUR, 62, 3
The study of female mate choice in primates has been
problematic. Validated measures of female mate choice
are only sometimes used (e.g. Manson 1992), distinguishing between behavioural mate choice and underlying
preference remains difficult (Soltis 1999), and in only a
few species is there evidence for the criteria by which
females choose males (e.g. squirrel monkey, Saimiri
oerstedi: Boinski 1987; brown capuchin monkey, Cebus
apella: Janson 1984; vervet monkey, Cercopithecus
aethiops: Keddy 1986; Japanese macaques, Macaca fuscata:
Soltis et al. 1999; orang-utan, Pongo pygmaeus: van Schaik
& van Hooff 1996). In addition, females can re-enforce
the male dominance hierarchy by choosing dominant
males (e.g. Cox & Le Boeuf 1977), or act in opposition to
the male dominance hierarchy by choosing males of
other ranks (e.g. Davies 1992; Manson 1992). When male
and female strategies are in conflict, there may be sexual
coercion (Smuts & Smuts 1993).
Japanese macaques live in bisexual social groups with
female philopatry and male dispersal (Pusey & Packer
1987). Direct male–male competition, alternative male
mating tactics, female mate choice and male sexual coercion of females are all important in this species. Male
dominance rank explains some, but not all, of the variation in male reproductive success. Reported correlations
between male dominance rank and (1) mating success
and (2) number of offspring sired range from nonsignificant correlations to significant, positive correlations (e.g.
mating only: Enomoto 1974; Eaton 1978; Takahata 1982;
Perloe 1992; number of offspring: Inoue et al. 1991, 1993;
Soltis et al. 1997b).
There is evidence that subordinate Japanese macaque
males use sneak copulations as an alternative mating
tactic. Nontroop males often invade social groups and
mate with resident females (Sprague 1991). Also, in a
captive study, low-ranking fathers were less likely to be
observed mating with mothers during the ovulatory
period than high-ranking fathers (Soltis et al. 1997b).
Female mate choice has also been considered important
in Japanese macaques. For example, Huffman (1987,
1991) has shown that females can easily reject male
mount attempts, and that dominant males are usually
unsuccessful at breaking up mounting series involving
females and low-ranking males. Furthermore, Soltis et al.
(1997b) showed that female mate choice is a stronger
predictor than male–male competition of both mating
success and number of offspring sired.
Nevertheless, male sexual coercion of females also may
be important in Japanese macaques. Male aggression
towards females increases in the mating season, and is
correlated with high mating frequency (e.g. Enomoto
1981). In addition, male–female aggression may keep
females from leaving males once mounting series have
begun (Soltis 1999). One study, however, showed that
most male–female aggression was a side effect of overall
male aggression during the mating season (Soltis et al.
1997a).
This paper comprises the first study combining genetic
and behavioural data to answer questions concerning
sexual selection in wild, nonprovisioned Japanese
macaques. We address the following specific questions.
Table 1. Composition of the Nina-A Troop at the beginning of the
1997 mating season
Males
Females
Total
15
10
3
28
15
7
2
24
30
17
5
52
Adult* (≥4 years)
Juvenile (1–3 years)
Infant (0 years)
Total
*Adult=potentially sexually mature (Takahata et al. 1998).
(1) What is the relationship between male dominance
rank and male mating and paternity of offspring? (2) Do
subordinate males use alternative mating tactics? (3) How
does female mate choice predict male mating and
paternity of offspring? (4) How do conflicting male and
female strategies interact to produce mating and reproductive outcomes? We compare these results with our
previous work on captive Japanese macaques using
similar methodology.
METHODS
Study Subjects and Site
This study was conducted on the Nina-A troop of
Japanese macaques residing in a broad-leaf evergreen
forest on Yakushima Island, Japan, (30N, 131E;
Maruhashi 1980, 1982). The Nina-A troop consisted of 52
individuals at the beginning of the study (Table 1).
Subject animals included all adult males (N=15) and adult
females that displayed copulatory behaviour (N=10 nonlactating and N=2 lactating females). All adults could
be individually identified by sex, size, facial markings,
injuries and scars. In addition, eight of 15 adult males
could be identified by unique facial tattoos. The mating
season begins in September and can last until February
(Maruhashi 1982; personal observations). Troop males
are those that were present within the troop at the
beginning of the mating season. No males permanently
transferred out of or into the Nina-A troop during the
study period. Intergroup encounters occurred when one
or more nontroop macaques and Nina-A members were
observed simultaneously.
Behavioural Data Collection
This study represents part of a larger research project in
which J.S. and R.T. monitored the Nina-A troop from July
1997 to June 1999. J.S. collected the core behavioural data
reported here during the 1997 mating season peak from
27 September to 11 December. Focal samples were conducted on females that displayed copulatory behaviour
on the day of or previous to observations (at least
2 mounts, an ejaculatory mount, or copulatory plug
observed). J.S. attempted to locate the troop at dawn, and
when found, began focal observations on the first such
female encountered. Social and sexual behaviours were
recorded (see Soltis 1999). Japanese macaques are series
mounters (Tokuda 1961), and in this paper mating or
SOLTIS ET AL.: REPRODUCTIVE STRATEGIES IN MACAQUES
ejaculation refer to terminal, ejaculatory mounts. We
defined a ‘sneak copulation’ as a mounting series culminating in ejaculation in which no other adult male was
observed from the first mount in the series to the final
ejaculatory mount. Focal samples were continued until
the female was lost for more than 5 min. Focal samples
under 20 min were not analysed. When a focal female
was lost, a new focal sample was begun on the next
female encountered who met the criteria for observations
(even if it was the same female). A total of 198.72 h of
focal observations were completed (meanSD=16.56
14.87 h/female). The mean focal sample length was
90.99 min (range 20–520 min).
Prior to and during the mating season, J.S. recorded a
total of 509 male submissive behaviours (cower, facial
grimace, flee) ad libitum. A matrix was formed with losers
on one axis and winners on the other. There was a rank
reversal between the alpha and beta males midway
through the mating season observations. These males
were assigned the average of those two ranks combined.
The third- through the fifth-ranking males had unstable
relationships throughout the season, with bidirectional
submission shown among all three males. These three
males were each assigned the average of the three ranks
combined. Finally, the three lowest-ranking males did
not express submission to one another. These three males
were assigned the average of the three lowest ranks
combined. In the analyses that follow, male dominance
rank is expressed as the fraction of other males outranked.
‘High-’, ‘middle-’, and ‘low-’ ranking males are the top,
middle, and bottom five males, respectively.
We also arranged males into an attractiveness hierarchy
(‘attractivity rank’) based on female mate choice behaviour directed towards them during female focal samples
(Halliday 1983). We used the female Hinde’s index
(Hinde & Atkinson 1970) as an assay of female mate
choice. The Hinde’s index measures responsibility for
proximity maintenance within dyads, and is calculated as
the proportion of female approaches within the dyad
minus the proportion of females leaves within the dyad
(we used 1-m leaves and approaches). The index ranges
from 1 (where the male is responsible for proximity) to
+1 (where the female is responsible for proximity). Only
dyads for which there were a total of at least 10 summed
approaches and leaves were scored a Hinde’s index
(N=79). Twelve males were ranked according to their
mean female Hinde’s index. Three males low in dominance rank were excluded because they had only one
measurable female Hinde’s index. Males to whom females
maintain proximity most have high Hinde’s indices,
while males to whom females maintain proximity the
least have low Hinde’s indices.
We used the female Hinde’s index as an assay of female
mate choice because our previous work shows that this
measure is a powerful predictor of both mating and
reproductive success in this species (Soltis et al. 1997a, b;
Soltis 1999). Even though the female Hinde’s index was
negatively correlated with dominance rank, it was a more
powerful predictor of mating, ovulatory mating and
number of offspring sired than was male dominance
rank. Also, female initiation and/or maintenance of
proximity are associated with mating in other primate
species (rhesus monkey, Macaca mulatta: Wallen et al.
1984; Manson 1992; Savanna baboon, Papio cynocephalus:
Bercovitch 1991).
DNA Sample Collection and Analysis
J.S. and R.T. used noninvasive sampling techniques to
collect DNA from mothers (N=10), infants born in 1998
(N=10) and potential sires in the troop (N=15). Ejaculate
(from masturbation or that issuing from the penis after
mating) was collected from 11 males, blood samples
collected by previous researchers were used for three
males, and a urine sample was collected from the final
male. Urine and/or faecal samples were collected from all
10 mothers and for 9 of 10 infants. Muscle tissue was
extracted from one infant whose body was recovered after
an infanticidal attack (Soltis et al. 2000).
Faecal, urine and ejaculate samples were collected
immediately after they were left behind by identified
individuals (Hayakawa & Takenaka 1999). A cotton swab
was used to scrape the outer surface of faecal samples, and
collected faeces was inserted into a tube with 2 ml EDTA
and 99.5% ethanol (to 10 ml). Urine samples were
collected with plastic pipettes and inserted into tubes
with 99.5% ethanol (twice the volume of urine). The
coagulated portions of ejaculates were collected with
wooden sticks and inserted into tubes with 99.5% ethanol
(to 10 ml). All samples were refrigerated at the Kyoto
University Yakushima Field Station until DNA extraction
at the Primate Research Institute of Kyoto University.
J.S. and O.T. extracted DNA from samples using standard phenol-chloroform procedures, extracts were maintained at 4 C until polymerase chain reaction (PCR), and
amplified DNA was subject to polyacrylamide gel electrophoresis and visualized after silver staining (Inoue &
Takenaka 1993; Takenaka et al. 1993; Soltis et al. 1997b;
Domingo-Roura 1997; Hayakawa & Takenaka 1999). To
relieve amplification inhibition for faecal and urine
samples, we included 0.02 l of T4 gene 32 protein per
tube (Kreader 1996), and amplified each sample three
separate times using variable amounts of template DNA
(0.1, 0.5 and 1.0 l).
We used nine primers known to be polymorphic in
Yakushima macaques (S. Hayakawa, unpublished data).
One primer was designed specifically for Japanese
macaques (MFGT 21; Domingo-Roura et al. 1997) and
eight others originally designed for humans (D1S 550,
D1S 533, D5S 820, D5S 1457, D5S 1470, D6S 493, D6S 501
and D14S 255; Morin et al. 1997; Nurnberg et al. 1998).
PCR products from noninvasive samples such as faeces
and urine can sometimes result in false genotyping, such
as allelic drop-out and amplification of nontarget DNA
(Taberlet et al. 1999). Methods for overcoming false
genotyping include collecting fresh samples combined
with good preservation methods, and using trinucleotide
or tetranucleotide microstellites (Taberlet et al. 1999).
Samples were always collected immediately after released
from the animal and were preserved in ethanol and
refrigerated at the end of the day. In addition, seven of
nine primers (78%) were tetranucleotide repeats, while
487
488
ANIMAL BEHAVIOUR, 62, 3
Table 2. Paternity exclusion analysis for nine mother–infant pairs and 15 males of the Nina-A troop
Mother–Infant
pair
HOT–HRS
TAM–TMK
NOR–NRK
YAM–YMS
WAK–WRB
HAM–HCM
SKO–SKE
NAM–NMZ
YKO–YGI
Number of
group males
excluded
Number
of loci
Number of males
not excluded
(compatible)
14
14
14
14
14
14
15
15
15
2–5
2–4
2–4
2–4
2–4
2–4
2–4
2–4
1–4
1
1
1
1
1
1
0
0
0
only two of nine (22%) were dinucleotide repeats
(Domingo-Roura et al. 1997; Morin et al. 1997; Nurnberg
et al. 1998).
The most conservative way to overcome these problems
is to repeat each DNA amplification (PCR) independently
many times for each locus, the so-called ‘multiple-tubes
approach’ (e.g. Navidi et al. 1992). But this method is
extremely time-consuming and requires large amounts of
DNA (Taberlet et al. 1999). We could not follow this most
conservative method because of time constraints and the
small volume of unreplaceable template DNA from some
subjects (small sample amounts combined with high
mortality on Yakushima). We did attempt to remove the
potential effects of allelic drop-out by excluding all
homozygotes derived from noninvasive samples from the
data set. The only change in the results was that there
were no extra group paternities, so the estimate of the
extragroup paternity provided here should be viewed
with caution. Associations between independent variables and paternity, on the other hand, were essentially
the same with the more conservative approach. Finally,
using identical procedures in our laboratory, faecal- and
urine-derived PCR products have been cross-validated
with blood-derived PCR products from the same
individuals (Hayakawa & Takenaka 1999).
Paternity Determination
After bands for most individuals were visualized for a
particular primer, the PCR products from the mother, her
offspring and each potential male were run on lanes
adjacent to one another (Soltis et al. 1997b). By comparing the mother and offspring genotypes, the paternal
genotype was deduced. If the male did not possess the
paternal allele(s), he was excluded. If all males in the
group were excluded, we considered a nontroop male to
have sired the offspring. We considered a male the likely
father if (1) the other 14 males in the troop were all
excluded, and (2) the male was compatible with the
paternal genotype at all examined loci (e.g. Borries et al.
1999). Paternity inclusion probability for likely fathers
could not be calculated because allele frequencies are not
known on Yakushima Island (Chakraborty et al. 1988).
Number
of loci
7
7
7
7
8
8
Ten infants were born in 1998. In nine cases, paternity
was resolved according to the above rules (Table 2).
Nonfathers were excluded at one to five loci, and likely
fathers possessed genotypes compatible with offspring
genotypes at seven to eight loci. Paternity could not be
resolved for one infant who disappeared, because of the
small amount of template DNA that was recovered and a
low rate of amplification.
Statistical Analyses
We used nonparametric statistical tests throughout (SPSS 10.0; two-tailed alpha=0.05). We calculated
Wilcoxon matched-pairs signed-ranks tests and partial
correlation coefficients according to Conover (1980), and
determined for the latter the probability values using a
standard table minus one degree of freedom.
RESULTS
Male Reproductive Strategy and Paternity
Nontroop males sired three of nine offspring (33%) for
whom paternity could be resolved (Table 2). Twenty-one
encounters with neighbouring troops were observed during the study, but only one female was observed to mate
with nontroop males. She was a lactating female who
mated with two nontroop males during one intergroup
encounter, but she did not give birth the following year.
Within the troop, however, dominant males were able
to monopolize female mating and paternity. We observed
139 ejaculations by 15 troop males during female focal
samples. The number of observed matings was correlated
with male dominance rank (Spearman’s rank correlation:
rS =0.700, N=15 males, P=0.004; Fig. 1). The number of
offspring sired within the troop (6 of 9 offspring, 67%;
Table 2) was also positively correlated with male dominance rank (rS =0.587, N=15 males, P=0.021; Fig. 1).
Results were similar after removing males below 7 years of
age (mating: rS =0.595, N=13 males, P=0.032; infants
sired: rS =0.551, N=13 males, P=0.051).
Sires were almost never observed mating with the
mother during the estimated time of conception, however. We estimated conception periods by counting back
SOLTIS ET AL.: REPRODUCTIVE STRATEGIES IN MACAQUES
10
Number of mating males/male rank
60
50
40
30
20
0.071
0.071
0.071
0.214
0.286
0.357
0.500
0.429
0.571
0.643
0.786
0.786
0.786
0
0.965
10
0.965
Number of ejaculations/offspring
70
Male dominance rank
Figure 1. Relationship between male dominance rank and the
number of observed ejaculations ( ) and the number of offspring
sired ( ). The highest-ranking male sired two offspring, and four
other males sired one offspring each.
from birth the average gestation length1 SD from
observed birthdays (1737 days; Nigi 1976; Thomsen &
Soltis 2000). Nontroop males sired three offspring, but
mothers of these offspring were not observed to mate
with nontroop males at any time. Of three mothers
whose offspring were sired by troop males, one was
observed to mate with the sire during the time of her
conception period, one was observed to mate with the
sire at times other than the conception period, and one
was never observed to mate with the sire. In the last three
cases, such analyses could not be performed, either
because exact birthdays were not known (two cases), or
there were no mating season behavioural data for the
mother (the case of one lactating female who gave birth).
Dominant males could often monopolize females
because there were not usually very many females
displaying mating behaviour simultaneously. The
meanSD number of females displaying mating behaviour per day was 2.421.177 (range 1–5). For comparison, in an earlier captive study of Japanese macaques in
which males did not monopolize females (N=8 males,
N=21 females; Soltis et al. 1997a, b), the meanSD
number of females displaying mating behaviour per day
was 3.591.606 (range 1–8; Mann–Whitney U test:
U=1109.50, N1 =45 days, N2 =85 days, P<0.001). In fact, in
this study, 21 of the alpha male’s 61 observed ejaculations
(34%; Fig. 1) occurred with one female during an 8-day
stretch in which she was either the only female mating or
was one of two females mating. During that period, the
alpha male secured 84% (21/25) of her matings, although
this did not coincide with her conception period, and he
did not sire her offspring.
We further tested the priority of access model by
calculating, for each observation day, the number of
females in the group displaying copulatory behaviour (see
Methods), the number of males observed mating during
focal samples and the average rank of mating males. The
number of males observed mating increased, but not
8
6
4
2
0
N = 11 11
1.00
7 7
15 15
5 5
2.00
3.00
4.00
Number of copulating females
1 1
5.00
Figure 2. For days on which there were one to five females
displaying copulatory behaviour in the group, the mean±SE number
of males that mated with focal females ( ), and the mean±SE
dominance rank of males that mated with focal females ( ).
Dominance rank is expressed as the fraction of other males outranked multiplied by 10. Number of observation days (N) on
which one to five females were displaying copulatory behaviour is
indicated.
significantly, with the number of females displaying
copulatory behaviour (SPSS 10.0 Jonckheere-Terpstra test:
JT=336, N=39 days, P=0.099; Fig. 2), but the average
dominance rank of males observed mating did decrease
significantly with the number of females displaying
mating behaviour (JT=190, N=39 days, P=0.029; Fig. 2).
This result shows that the larger the number of available
females, the greater the mating opportunity for males of
various dominance ranks.
Females and males were often observed to run from the
central part of the troop and engage in sneak copulations
(see Methods) outside of the presence of other troop
members. Lower-ranking males were most likely to
engage in such sneak copulations (rS = 0.783, N=15
males, P=0.001; Fig. 3).
Female Reproductive Strategy and Paternity
The meanSD number of 15 males with whom 12
females were observed to mate during focal samples was
5.172.855 (range 1–10 males). Although the number of
observation hours per female was correlated with the
number of observed mating partners (rS =0.883, N=12
females, P<0.001), it was not correlated with the mean
rank of females’ mating partners (rS = 0.399, N=12
females, P=0.199), or with the mean female Hinde’s
index across males (rS = 0.238, N=12 females, P=0.457).
Female Hinde’s indices ranged from 0.692 to +0.909.
The mean Hinde’s index for each female, calculated
across males, ranged from 0 to +0.533, and the grand
mean across all female means was +0.208.
We ordered males into an attractiveness hierarchy
based on the Hinde’s index. For each female, we calculated the mean Hinde’s index across males, and males
489
ANIMAL BEHAVIOUR, 62, 3
did not differ (T=1.423, N=11 females, P=0.182; Table 3).
Group males for whom there was a measurable Hinde’s
index sired only four infants. A male of high attractivity
sired one offspring, and males of low attractivity sired
three (Table 3).
100
80
% Sneak copulations
490
60
The Interaction of Male and Female Strategies
40
20
0
0.965 0.786 0.786 0.571 0.429 0.286 0.071 0.071
0.965 0.786 0.643 0.500 0.357 0.214 0.071
Male dominance rank
Figure 3. The relationship between male dominance rank and
the percentage of the total observed matings that were sneak
copulations.
high in attractivity were those with Hinde’s indices above
the female’s mean, and males low in attractivity were
those with Hinde’s indices below the female’s mean.
Female mate choice had only a minimal effect on male
mating and no measurable effect on paternity. Males of
high attractivity were more likely to become mates than
males of low attractivity (Wilcoxon matched-pairs signed
ranks test: T= 2.018, N=11 females, P=0.044; Table 3).
The absolute number of matings received, however, did
not differ between males of high and low attractivity
(T= 0.474, N=11 females, P=0.636; Table 3). This is
because some females mated many times with a few
high-ranking males that were low in attractivity. The
dominance rank of males of high and low attractivity also
To compare the effects of male dominance rank with
the effects of female mate choice, we ordered males into
an attractiveness hierarchy based the their mean female
Hinde’s indices (see Methods). Males varied in their
attractivity to females, but no male was universally high
or low in attractivity across all females. The percentage of
troop females to whom males were high in attractivity
(definition above) ranged from 25% to 71% (median=
50%). Across males, the mean female Hinde’s index
ranged from 0.123 to +0.352 with an overall mean of
+0.198. As in the female-centred analysis above, male
attractivity rank was not significantly correlated with the
number of matings (rS = 0.304, N=12 males, P=0.337) or
number of offspring sired (rS = 0.064, N=12 males,
P=0.844).
Male attractivity and male dominance rank were negatively but nonsignificantly correlated (rS = 0.444, N=12
males, P=0.148). That is, females expressed mate choice
behaviour to males of various dominance ranks (also see
Table 3). We conducted partial correlation analyses to
control for the effects of the opposing variables (Table 4).
When controlling for the effects of male attractivity rank,
the correlations between dominance and mating/number
of offspring were stronger. Similarly, when controlling for
the effects of male dominance rank, the correlations
between attractivity rank and mating/number of offspring also were stronger. In fact, when the effects of
male–male competition were removed, the correlation
Table 3. Males of high and low attractivity to females and reproductive success
% Males mated
High*
Females†
V
F§
D**
S**
T
G**
L
Z
C
W
N
Mean
75‡
67
50
80
75
50
100
67
50
75
100
71.73
Low
67
0
50
33
0
0
100
75
86
57
33
45.55
Mean number of matings
Mean dominance rank
High
Low
High
Low
1
1.67
0.5
2.2
2
0.5
1.5
1
0.5
2.25
1.33
1
0
0.5
1.33
0
0
3.5
1.25
5.43
2.14
1
0.706
0.726
0.608
0.534
0.724
0.679
0.876
0.828
0.554
0.357
0.607
0.679
0.965
0.876
0.703
0.733
0.571
0.768
0.693
0.694
0.755
0.679
1.314
1.468
0.654
0.738
*For each female, males with a Hinde’s index above the female’s mean across all males were high in attractivity,
while those males with a Hinde’s index below the female’s mean were low in attractivity.
†One female who had a Hinde’s index for only one male was excluded.
‡Bold indicates that the sire of the female’s offspring was either high or low in attractivity.
§The sire of this female’s offspring had no Hinde’s index.
**The sires of these females’ offspring were nontroop males.
SOLTIS ET AL.: REPRODUCTIVE STRATEGIES IN MACAQUES
Table 4. Simple and partial Spearman’s correlation coefficients
Variables
Dominance and mating
Dominance and offspring
Attractivity and mating
Attractivity and offspring
Simple
correlation
Partial
correlation†
0.700**
0.587*
0.304
−0.064
0.978**
0.625*
0.961**
0.271
†Attractivity rank was partialled out for dominance rank and mating/
offspring, and dominance rank was partialled out for attractivity
rank and mating/offspring.
*P<0.05; **P<0.01.
between female mate choice and mating was statistically
significant (Table 4).
DISCUSSION
Male–Male Competition
Nontroop males sired one-third of the offspring born,
although this could be an overestimate (see Methods). In
only one of 21 intergroup encounters, however, were
there observations of a female (who did not give birth)
mating with nontroop males. The Nina-A troop was the
largest in the area, and other troops usually avoided it.
This may have required Nina-A females to mate with
nontroop males away from the troop, where observation
was particularly unlikely. On the other hand, this result is
consistent with previous observations on Yakushima
Island, in which mating by nontroop males is extensive
(Sprague 1991). Generally, this result adds to a body of
evidence that indicates the social group per se is not
necessarily predictive of paternity (e.g. Birkhead et al.
1995; Lubjuhn et al. 1999).
Within the troop, however, dominant males were able
to monopolize female mating and paternity, thus supporting the priority of access model (Altmann 1962).
Only high- and mid-ranking males sired offspring, and
the two males that held the alpha position sired 50%
(3/6) of within-troop paternity (Fig. 1). More importantly,
within- and between-population tests show that the
number of females mating simultaneously is associated
with the strength of the correlation between male dominance rank and male mating and offspring produced.
First, male dominance rank was not correlated with
number of offspring sired in a previous captive study
where many females mated simultaneously (Soltis et al.
1997b), but was positively correlated with the number of
offspring sired in this wild study where fewer females
mated simultaneously. Second, in this study, on days
when there were more females displaying copulatory
behaviour, the average dominance rank of mating males
decreased. Taken together, these data provide strong
evidence that male–male competition does influence
mating and reproductive outcome, but that female
mating or ovulatory synchrony can have a strong effect
on dominant males’ ability to monopolize mating and
paternity (Paul 1997).
In a previous review of primates (Cowlishaw & Dunbar
1991), however, the number of adult group females did
not affect the relationship between male dominance rank
and mating. This is probably due to the fact that the total
number of adult females in a group is a poor measure of
the number that actually display mating behaviour at any
given time (Emlen & Oring 1977).
Alternative Mating Tactics and Female Mate
Choice
Male dominance rank does not explain all the variation
in mating and reproductive success, however. First, like
other animals (e.g. Gross 1982), male Japanese macaques
engage in alternative mating tactics to avoid direct competition with higher-ranking males. In this study, there
was a near-linear negative relationship between male
dominance rank and the proportion of sneak copulations. Monopolizing females or pursuing sneak ejaculations is probably part of a single conditional strategy,
which changes based on relative dominance rank. In this
case, such alternative tactics were partially successful.
Two mid-ranking males that obtained 63 and 75% of
their copulations from sneak copulations (Fig. 3) each
sired one offspring, but no low-ranking males did so
(Fig. 1).
Second, female mate choice can also dilute the effects
of dominance rank. We used a measure of responsibility
for proximity maintenance (the female Hinde’s index) as
an assay of female mate choice, but found that it did not
predict the number of male matings or the number of
offspring sired. This is in sharp contrast to our previous
work in Japanese macaques, in which the same measure
of female mate choice was a strong predictor of mating
and number of offspring sired (Soltis et al. 1997b). Again,
we believe one reason for this contrast is that in the
captive group more females mated simultaneously,
allowing more mating opportunities for females and
lower-ranking males.
The Interaction of Male and Female Strategies
In this study, male ‘attractivity rank’ was negatively
(but not significantly) correlated with male dominance
rank. Therefore, when controlling for the effects of the
opposing variable, associations with mating and number
of offspring became stronger. In particular, when controlling for the effects of male dominance rank, attractivity
and mating became significantly correlated. We interpret
these results to mean that females preferred males of
many dominance ranks but were monopolized by dominant males, who mostly prevented females from mating
with mid- and low-ranking animals. In the absence
of male–male competition, therefore, the influence of
female mate choice would have been stronger. Likewise,
in the absence of female mate choice, the influence of
male–male competition would have been stronger (Table
4; see Soltis et al. 1997b for a similar result).
Although the partial correlation between attractivity
rank and mating was significant, the partial correlation
between attractivity and number of offspring was not
(Table 4). That is, even when controlling for the effects of
491
492
ANIMAL BEHAVIOUR, 62, 3
dominance rank, female mate choice did not predict
which males sired offspring. We suspect that female mate
choice at ovulation is different from mate choice over the
course of the entire mating season, and that we may have
missed ovulatory mate choice behaviour due to limited
observations. We could not determine the time of ovulation for these study subjects, but in our previous captive
work, ovulatory periods were determined based on hormonal profiles. In that study, females directed mate
choice behaviour towards multiple males throughout the
season, but chose specific males (those who displayed
most frequently) during ovulatory periods (Soltis et al.
1999). Thus, females may choose at ovulation, but mate
with multiple males throughout the rest of the mating
season. We believe that females may benefit from mating
with multiple males by decreasing the probability of
infant harassment or infanticide (Hrdy 1979). In this
study, troop males physically attacked infants eight times
more often (including one infanticide) when they had
not mated with the mother previously (Soltis et al. 2000).
Males may have used coercion and mate guarding to
prevent females from mating with multiple males, however (Smuts & Smuts 1993). In this data set, male aggression was not significantly correlated with frequency of
mating (Soltis 1999). On the other hand, 43% of dyads
were often characterized in part by high-ranking males
successfully monopolizing females. Specifically, male–
female aggression, female approach to the male, male
grooming the female and prolonged mount series
co-occurred within these dyads (Soltis 1999). Male aggression preceded female approaches to the male, indicating
that these males may have coerced the females to remain
with them. Male grooming of the female and prolonged
mount series also may be mate-guarding tactics (Soltis
1999; Manson 1996). Thus, high-ranking male strategies
may have prevailed over those of females in part because
of successful mate guarding and coercion. Females were
often seen attempting to escape from dominant males
with whom they were mating, but only 16 of 139
ejaculations (12%) were with low-ranking males (Fig. 1).
Again, this contrasts with an earlier study, in which
female strategies prevailed over those of males, and male
coercion was considered minimal (Soltis et al. 1997a, b).
could be nontroop males with similar genotypes. We
consider this unlikely because genotypes of likely fathers
were consistent with those of their presumed infants at
seven to eight loci. Nevertheless, when paternity inclusion is possible, more confidence can be put into the
results. More paternity studies in the wild would be
especially welcome in any case, to avoid the temptation
to generalize from this single case from one mating
season.
Third, there are other mechanisms of sexual selection
that we have not considered, such as female–female
competition and sperm competition. Female–female
aggression was very rare, although it was sometimes
observed in mating contexts. Presently, we are examining
aspects of sperm competition and the function of masturbation in these Yakushima macaques, in part to determine whether middle- and low-ranking males increase
sperm quality through masturbation to make up for the
low quantity of matings.
We make the following conclusions concerning
Japanese macaques. (1) Males follow a conditional mating
strategy that is dependent on relative rank. At one end
of the continuum, high-ranking males primarily guard
females and exclude other males, thus avoiding sperm
competition, and at the other end, low-ranking males
opportunistically engage in sneak copulations, thus
increasing sperm competition. (2) Throughout the entire
mating season, females attempt to mate with many males
of various dominance ranks. Previous work shows that
this benefits females by reducing the probability of infant
harassment and infanticide (Soltis et al. 2000). During
ovulation, on the other hand, females may choose particular males, perhaps those who display most frequently
(Soltis et al. 1999). (3) The strategies of females (mating
with multiple males) and high-ranking males (monopolizing females) are often in conflict with one another. In
this study, male strategies prevailed, while in an earlier
study, female strategies prevailed (Soltis et al. 1997a, b).
The winning sex is determined, in part, by the number of
females mating and/or ovulating simultaneously.
Future Directions and Conclusions
We are indebted to Drs Yukimaru Sugiyama and Juichi
Yamagiwa, who supported this research and made local
arrangements on Yakushima Island. J.S. is especially
indebted to Sachiko Hayakawa, who provided critical
assistance in the DNA analysis by kindly furnishing
advice on primer polymorphism and PCR protocols and
to Linda Vigilant for advice on interpretation of DNA
results. Carola Borries, Joseph Manson and two anonymous referees provided excellent advice on earlier drafts.
J.S. was supported financially by the U.S.A. National
Science Foundation, the Japan Society for the Promotion
of Science, and Grants-in-Aid for Scientific Research,
Ministry of Science, Culture and Education, Japan. R.T.
was supported by a grant from the German Academic
Exchange Service (DAAD). The research presented here
was evaluated and approved by the Animal Behavior
Society’s Animal Care Committee on 23 May 2001.
Several problems with this study point the way towards
a better understanding of sexual selection in Japanese
macaques and other species. First, we cannot be certain
that the female Hinde’s index, or any other behaviour
recorded in social groups, is a good measure of underlying
female preferences. Only with experimental manipulation can we determine such preferences. Mate choice
can be viewed as preferences expressed in a field of
constraints, such as male mate guarding, which may
inhibit preferences. Future research on mate preferences
in primates will benefit from the experimental approach
(e.g. Bischoff et al. 1985; Keddy 1986).
Second, paternity inclusion was not performed because
the allele frequencies on Yakushima are not known. Thus,
‘likely fathers’ may not be actual fathers. The real fathers
Acknowledgments
SOLTIS ET AL.: REPRODUCTIVE STRATEGIES IN MACAQUES
References
Altmann, S. J. 1962. A field study of the sociobiology of the rhesus
monkey, Macaca mulatta. Annals of the New York Academy of
Sciences, 102, 338–435.
Andersson, M. 1994. Sexual Selection. Princeton, New Jersey:
Princeton University Press.
Bercovitch, F. B. 1991. Mate selection, consortship formation, and
reproductive tactics in adult female savanna baboons. Primates,
32, 437–452.
Bercovitch, F. B. 1992a. Re-examining the relationship between
rank and reproductive success in male primates. Animal Behaviour,
44, 1168–1170.
Bercovitch, F. B. 1992b. Dominance rank, reproductive success and
reproductive tactics in male primates: a reply to Dunbar and
Cowlishaw. Animal Behaviour, 44, 1174–1175.
Berard, J. D., Nurnberg, P., Epplen, J. T. & Schmidtke, J. 1994.
Alternative reproductive tactics and reproductive success in male
rhesus macaques. Behaviour, 129, 177–201.
Birkhead, T. R., Fletcher, F., Pellatt, E. J. & Staples, A. 1995.
Ejaculate quality and the success of extra-pair copulations in the
zebra finch. Nature, 377, 422–423.
Bischoff, R. J., Gould, J. L. & Rubenstein, D. I. 1985. Tail size and
female choice in the guppy (Poecilia reticulata). Behavioral Ecology
and Sociobiology, 17, 253–255.
Boinski, S. 1987. Mating patterns in squirrel monkeys (Saimiri
oerstedi): implications for seasonal sexual dimorphism. Behavioral
Ecology and Sociobiology, 21, 13–21.
Borries, C., Launhardt, K., Epplen, C., Epplen, J. T. & Winkler, P.
1999. DNA analyses support the hypothesis that infanticide is
adaptive in langur monkeys. Proceedings of the Royal Society of
London, Series B, 266, 901–904.
Chakraborty, R., Meagher, T. R. & Smouse, P. E. 1988. Parentage
analysis with genetic markers in natural populations. I. The
expected proportion of offspring with unambiguous paternity.
Genetics, 118, 527–536.
Clutton-Brock, T. H., Guinness, F. E. & Albon, S. D. 1982. Red
Deer: Behavior and Ecology of Two Sexes. Chicago: University of
Chicago Press.
Conover, W. J. 1980. Practical Nonparametric Statistics. 2nd edn.
New York: J. Wiley.
Cowlishaw, G. & Dunbar, R. I. M. 1991. Dominance rank and
mating success in male primates. Animal Behaviour, 41, 1045–
1056.
Cox, C. R. & Le Boeuf, B. J. 1977. Female incitation of male
competition: a mechanism in sexual selection. American Naturalist,
111, 317–355.
Davies, N. B. 1992. Dunnock Behaviour and Social Evolution. Oxford:
Oxford University Press.
Dixson, A. F. 1998. Primate Sexuality. Comparative Studies of the
Prosimians, Monkeys, Apes, and Human Beings. Oxford: Oxford
University Press.
Domingo-Roura, X. 1997. The analysis of hypervariable DNA
regions for the study of the ecology and genetic structure
of wild mamalian populations. Applications to conservation
biology. Ph.D. thesis, Universitat Autonoma de Barcelona,
Spain.
Domingo-Roura, X., Lopez-Giraldez, T., Shinohara, M. &
Takenaka, O. 1997. Hypervariable microsatellite loci in the
Japanese macaque (Macaca fuscata) conserved in related species.
American Journal of Primatology, 43, 357–360.
Dunbar, R. I. M. 1984. Reproductive Decisions: an Economic Analysis
of Gelada Baboon Strategies. Princeton, New Jersey: Princeton
University Press.
Dunbar, R. I. M. & Cowlishaw, G. 1992. Mating success in male
primates: dominance rank, sperm competition and alternative
strategies. Animal Behaviour, 44, 1171–1173.
Eaton, G. G. 1978. Longitudinal studies of sexual behavior of the
Oregon troop of Japanese macaques. In: Sex and Behavior (Ed. by
T. E. McGill, D. A. Dewsbury & B. D. Sachs), pp. 35–59. New York:
Plenum.
Emlen, S. T. & Oring, L. W. 1977. Ecology, sexual selection, and the
evolution of mating systems. Science, 197, 215–223.
Ellis, L. 1993. Dominance and reproductive success among nonhuman animals: a cross-species comparison. Ethology and
Sociobiology, 16, 257–333.
Enomoto, T. 1974. The sexual behaviour of Japanese monkeys.
Journal of Human Evolution, 3, 351–372.
Enomoto, T. 1981. Male aggression and the sexual behaviour of
Japanese monkeys. Primates, 22, 15–23.
Gross, M. R. 1982. Sneakers, satellites, and parentals: polymorphic
mating strategies in North American sunfishes. Zeitschrift für
Tierpsychologie, 60, 1–26.
Halliday, T. R. 1983. The study of mate choice. In: Mate Choice (Ed.
by P. Bateson), pp. 3–32. Cambridge: Cambridge University Press.
Hayakawa, S. & Takenaka, O. 1999. Urine as another source for
template DNA in polymerase chain reaction (PCR). American
Journal of Primatology, 48, 299–304.
Hinde, R. A. & Atkinson, S. 1970. Assessing the roles of social
partners in maintaining mutual proximity as exemplified by
mother–infant relations in rhesus monkeys. Animal Behaviour, 18,
169–176.
Huffman, M. A. 1987. Consort intrusion and female mate
choice in Japanese macaques (Macaca fuscata). Ethology, 75,
221–234.
Huffman, M. A. 1991. Mate selection and partner preferences in
female Japanese macaques. In: The Monkeys of Arashiyama: Thirtyfive years of Research in Japan and the West (Ed. by L. M. Fedigan
& P. J. Asquith), pp. 101–122. Albany: State University of New
York Press.
Hrdy, S. B. 1979. Infanticide among animals: a review, classification,
and examination of the implications for the reproductive
strategies of females. Ethology and Sociobiology, 1, 13–40.
Inoue, M. & Takenaka, O. 1993. Japanese macaque microsatellite
PCR primers for paternity testing. Primates, 34, 37–45.
Inoue, M., Takenaka, A., Tanaka, S., Kominami, R. & Takenaka, O.
1990. Paternity discrimination in a Japanese macaque group by
DNA fingerprinting. Primates, 31, 563–570.
Inoue, M., Mitsunaga, F., Ohsawa, H., Takenaka, A., Sugiyama,
Y., Gaspard, S. A. & Takenaka, O. 1991. Male mating behaviour
and paternity discrimination by DNA fingerprinting in a Japanese
macaque group. Folia Primatologica, 56, 202–210.
Inoue, M., Mitsunaga, F., Nozaki, M., Ohsawa, H., Takenaka, A.,
Sugiyama, Y., Shimizu, K. & Takenaka, O. 1993. Male dominance and reproductive success in an enclosed group of Japanese
macaques: with special reference to post-conception mating.
Primates, 34, 503–511.
Janson, C. H. 1984. Female choice and mating system of the brown
capuchin monkey Cebus apella (Primates: Cebidae). Zeitschrift für
Tierpsychologie, 65, 177–200.
Keddy, A. C. 1986. Female mate choice in vervet monkeys
(Cercopithecus aethiops). American Journal of Primatology, 10, 125–
143.
Kreader, C. A. 1996. Relief of amplification inhibition in PCR with
bovine serum albumin or T4 gene 32 protein. Applied and
Environmental Microbiology, 62, 1102–1106.
Le Boeuf, B. J. & Peterson, R. S. 1969. Social status and mating
activity in elephant seals. Science, 163, 91–93.
Lubjuhn, T., Strohbach, S., Brun, J., Gerken, T. & Epplen, J. T.
1999. Extra-pair paternity in great tits (Parus major): a long term
study. Behaviour, 136, 1157–1172.
Manson, J. 1992. Measuring female mate choice in Cayo Santiago
rhesus macaques. Animal Behaviour, 44, 405–416.
493
494
ANIMAL BEHAVIOUR, 62, 3
Manson, J. 1996. Male dominance and mount series duration in
Cayo Santiago rhesus macaques. Animal Behaviour, 51, 1219–
1231.
Maruhashi, T. 1980. Feeding behavior and diet of the Japanese
monkey (Macaca fuscata yakui) on Yakushima Island, Japan.
Primates, 21, 141–160.
Maruhashi, T. 1982. An ecological study of troop fissions of
Japanese monkeys (Macaca fuscata yakui) on Yakushima Island,
Japan. Primates, 23, 317–337.
Melnick, D. J. 1987. The genetic consequences of primate social
organization: a review of macaques, baboons and vervet
monkeys. Genetica, 73, 117–135.
Morin, P. A., Streetharan, K. & Smith, D. G. 1997. Simple
sequence repeat (SSR) polymorphisms for colony management
and population genetics in rhesus macaques (Macaca mulatta).
American Journal of Primatology, 42, 199–213.
Navidi, W., Arnheim, N. & Waterman, M. S. 1992. A multipletubes approach for accurate genotyping of very small DNA
samples by using PCR: statistical considerations. American Journal
of Human Genetics, 50, 347–359.
Nigi, H. 1976. Some aspects related to conception of the Japanese
monkey (Macaca fuscata). Primates, 17, 81–87.
Nurnberg, P., Sauermann, M., Kayser, M., Lanfer, C., Manz, E.,
Widdug, A., Berard, J., Bercovitch, F. B., Kessler, M., Schmidke,
J. & Krawczak, M. 1998. Paternity assessment in rhesus macaques
(Macaca mulatta): multilocus DNA fingerprinting and PCR marker
typing. American Journal of Primatology, 44, 1–18.
Ohsawa, H., Inoue, M. & Takenaka, O. 1993. Mating strategy and
reproductive success of male patas monkeys (Erythrocebus patas).
Primates, 34, 533–544.
Paul, A. 1997. Breeding seasonality affects the association between
dominance and reproductive success in non-human male
primates. Folia Primatologica, 68, 344–349.
Paul, A. & Kuester, J. 1996. Differential reproduction in male and
female Barbary macaques. In: Evolution and Ecology of Macaque
Societies (Ed. by J. E. Fa & D. G. Lindburg), pp. 293–317.
Cambridge: Cambridge University Press.
Pope, T. R. 1990. The reproductive consequences of male cooperation in the red howler monkey: paternity exclusion in
multi-male and single-male troops using genetic markers. Behavioral Ecology and Sociobiology, 27, 439–446.
Perloe, S. I. 1992. Male mating competition, female choice, and
dominance in a free ranging group of Japanese macaques.
Primates, 33, 289–304.
Pusey, A. E. & Packer, C. 1987. Dispersal and philopatry. In: Primate
Societies (Ed. by B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W.
Wrangham & T. T. Struhsaker), pp. 250–266. Chicago: University
of Chicago Press.
Rubenstein, D. 1980. On the evolution of alternative mating
strategies. In: Limits to Action: the Allocation of Individual Behavior
(Ed. by J. E. R. Staddon), pp. 65–100. New York: Academic Press.
de Ruiter, J. R., van Hooff, J. A. R. A. M. & Scheffrahn, W. 1994.
Social and genetic aspects of paternity in wild long tailed
macaques (Macaca fascicularis). Behaviour, 129, 203–224.
van Schaik, C. P. & van Hooff, J. A. R. A. M. 1996. Toward an
understanding of the orangutan’s social system. In: Great Ape
Societies (Ed. by W. C. McGrew, L. F. Marchant & T. Nishida),
pp. 3–15. Cambridge: Cambridge University Press.
Shively, C. & Smith, D. G. 1985. Social status and reproductive success of male Macaca fascicularis. American Journal of
Primatology, 9, 129–135.
Small, M. 1993. Female Choices. Ithaca, New York: Cornell University
Press.
Smith, D. G. 1981. The association between rank and reproductive
success of male rhesus monkeys. American Journal of Primatology,
1, 83–90.
Smith, D. G. 1993. A 15-year study of the association between
dominance rank and reproductive success of male rhesus
macaques. Primates, 34, 471–480.
Smuts, B. & Smuts, R. 1993. Male aggression and sexual coercion
of females in nonhuman primates and other mammals: evidence
and theoretical implications. Advances in the Study of Behavior, 22,
737–746.
Soltis, J. 1999. Measuring male–female relationships during the
mating season in wild Japanese macaques (Macaca fuscata yakui).
Primates, 40, 453–467.
Soltis, J., Mitsunaga, F., Shimizu, K., Yanagihara, Y. & Nozaki, M.
1997a. Sexual selection in Japanese macaques I: female
mate choice or male sexual coercion? Animal Behaviour, 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. Animal Behaviour, 54, 737–746.
Soltis, J., Mitsunaga, F., Shimizu, K., Yanagihara, Y. & Nozaki, M.
1999. Female mating strategy in an enclosed group of Japanese
macaques. American Journal of Primatology, 47, 263–278.
Soltis, J., Thomsen, R., Matsubayashi, K. & Takenaka, O. 2000.
Male infanticide by resident males and female counter-strategies
in wild Japanese macaques (Macaca fuscata). Behavioral Ecology
and Sociobiology, 48, 195–202.
Sprague, D. S. 1991. Mating by nontroop males among the
Japanese macaques of Yakushima Island. Folia Primatologica, 57,
156–158.
Taberlet, P., Waits, L. P. & Luikart, G. 1999. Noninvasive genetic
sampling: look before you leap. Trends in Ecology and Evolution,
14, 323–327.
Takahata, Y. 1982. The socio-sexual behaviour of Japanese
monkeys. Zeitschrift für Tierpsychologie, 59, 89–108.
Takahata, Y., Suzuki, S., Agetsuma, N., Okayasu, N., Sugiura, H.,
Takahashi, H., Yamagiwa, J., Izawa, K., Furuichi, T., Hill, D. A.,
Maruhashi, T., Saito, C., Sato, S. & Sprague, D. S. 1998.
Reproduction of wild Japanese macaque females of Yakushima
and Kinkazan islands: a preliminary report. Primates, 39, 339–349.
Takenaka, O., Takasaki, H., Kawamoto, S., Arakawa, M. &
Takenaka, A. 1993. Polymorphic microsatellite DNA amplification
customized for chimpanzee paternity testing. Primates, 34, 27–35.
Thomsen, R. & Soltis, J. 2000. Socioecological context of parturition in wild Japanese macaques (Macaca fuscata) on Yakushima
Island. International Journal of Primatology, 21, 685–696.
Tokuda, K. 1961. A study of the sexual behavior in the Japanese
monkey troop. Primates, 3, 1–40.
Wallen, K., Winston, L., Gaventa, S., Davis-DaSilva, M. & Collins,
D. C. 1984. Periovulatory changes in female sexual behaviour
and patterns of ovarian sterioid secretion in group-living rhesus
monkeys. Hormones and Behavior, 18, 431–450.