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Reproductive Parameters of Wild Rhinopithecus bieti

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Animal life activities are rhythmic and affected by seasonal periodicity. Based on 9 years of observations, we estimated the reproductive parameters of a wild, but provisioned Yunnan snub-nosed monkey (Rhinopithecus bieti) group at Xiangguqing in Baimaxueshan National Nature Reserve, Yunnan Province, China. We observed 84 infants (43 males and 41 females) from 41 females between 2010 and 2018. We found the birth sex ratio was 1:1, the female age at first birth was 6.13 years and infant mortality was about 15.5%. Nine years of data showed that the maximum birth season lasted 126 days, and the average length per year was 98.57 ± 18.71 days. R. bieti,characterized by strictly seasonal reproduction, started giving birth on February 1, and this ended on June 7, with a peak reached from March 4 to March 11 (10th week). The mean birth date was March 20 (79.21 ± 29.54 days), and the median birth date was March 11 (71st day). The mean interbirth interval (IBI) was approximately 2 years, and the IBIs among females whose infants had survived for 1 year were found to be significantly longer than those found in females who lost their infant within 1 year. Comparing the reproduction parameters among Asian and African colobines, we concluded that Asian and African colobines tend to have an IBI of 2 years or more, females tend to give birth at the age of 5-6 years, Rhinopithecus species had a strict seasonal reproductive pattern concentrated in February to April. Seasonal changes in food resources and climatic factors may be the main reasons for the variation in reproductive parameters in intraspecific and interspecific comparisons of Asian and African colobines.
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Original Research Article
Folia Primatol
DOI: 10.1159/000503246
Reproductive Parameters of Wild
Rhinopithecus bieti
Wancai Xia a, b Baoping Ren c Hong Zhou b, d Hao Feng d
Xinming He e Ali Krzton f Jie Hu b, d Majda Aouititen a
Xiaofeng Luan a Dayong Li b, d
a School of Nature Conservation, Beijing Forestry University, Beijing, China; b Institute of
Rare Animals and Plants, China West Normal University, Nanchong, China; c Key Laboratory
of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy
of Sciences, Beijing, China; d Key Laboratory of Southwest China Wildlife Resources
Conservation (Ministry of Education), China West Normal University, Nanchong, China;
e Baimaxueshan Natural Nature Reserve, Diqing, China; f RBD Library, Auburn University,
Auburn, AL, USA
Keywords
Yunnan snub-nosed monkey · Interbirth interval · Sex ratio · Infant mortality · Age
at first parturition · Seasonal birth
Abstract
Animal life activities are rhythmic and affected by seasonal periodicity. Based on 9
years of observations, we estimated the reproductive parameters of a wild, but provi-
sioned Yunnan snub-nosed monkey (Rhinopithecus bieti) group at Xiangguqing in
Baimaxueshan National Nature Reserve, Yunnan Province, China. We observed 84 in-
fants (43 males and 41 females) from 41 females between 2010 and 2018. We found the
birth sex ratio was 1: 1, the female age at first birth was 6.13 years and infant mortality
was about 15.5%. Nine years of data showed that the maximum birth season lasted 126
days, and the average length per year was 98.57 ± 18.71 days. R. bieti, characterized by
strictly seasonal reproduction, started giving birth on February 1, and this ended on
June 7, with a peak reached from March 4 to March 11 (10th week). The mean birth date
was March 20 (79.21 ± 29.54 days), and the median birth date was March 11 (71st day).
The mean interbirth interval (IBI) was approximately 2 years, and the IBIs among females
whose infants had survived for 1 year were found to be significantly longer than those
found in females who lost their infant within 1 year. Comparing the reproduction param-
eters among Asian and African colobines, we concluded that Asian and African colo-
Received: March 20, 2019
Accepted: July 30, 2019
Published online: November 13, 2019
Xiaofeng Luan
School of Nature Conservation
Beijing Forestry University
Beijing 100083 (China)
E-Mail luanxiaofeng @ bjfu.edu.cn
Dayong Li
Institute of Rare Animals and Plants
China West Normal University
Nanchong, Sichuan 637009 (China)
E-Mail 980119lsc @ 163.com
© 2019 S. Karger AG, Basel
www.karger.com/fpr
E-Mail karger@karger.com
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DOI: 10.1159/000503246
bines tend to have an IBI of 2 years or more, females tend to give birth at the age of 5–6
years, Rhinopithecus species had a strict seasonal reproductive pattern concentrated in
February to April. Seasonal changes in food resources and climatic factors may be the
main reasons for the variation in reproductive parameters in intraspecific and interspe-
cific comparisons of Asian and African colobines. © 2019 S. Karger AG, Basel
Introduction
Understanding reproductive parameters is critical for evaluating the conserva-
tion status of primate populations [Dunbar, 1988]. For example, knowing reproduc-
tive parameters can allow scientists to evaluate population growth, analyze popula-
tion dynamics, and predict future population trends; they are useful for in situ and ex
situ management of wildlife populations [Zhang et al., 2015]. They are also necessary
to examine metapopulation dynamics, such as determining the reproductive output
of source populations and estimating the minimum viable population size [Smith and
McDougal, 1991]. Age at first parturition, interbirth interval (IBI) and infant mortal-
ity are critical factors influencing the effectiveness of animal breeding [Fedigan and
Griffin, 1996]. To obtain data on reproductive parameters, it is necessary to continu-
ously record the reproductive histories of known individuals for several years, which
is extremely difficult for wild primates [Jin et al., 2009]. Long-term reproductive data
for colobine species are particularly scarce [Newton and Dunbar, 1994; Kirkpatrick,
2007]. Most Asian and African colobines are not strictly seasonal breeders, but rath-
er have distinct birth peaks during the year, with IBIs of approximately 2 years (Table
1) [Jin et al., 2009]. In contrast, infant mortality and age at first parturition are vari-
able among Asian and African colobines [Jin et al., 2009] (Table 1).
Bias in birth sex ratio has been a highly debated topic in mammalian research,
especially in primates [Bercovitch, 2002]. Recent empirical and theoretical work has
suggested that, under certain circumstances, females adjust the sex ratio of their prog-
eny [Qi et al., 2008]. The sex allocation theory predicts that in some species, females
in good condition (i.e., superior nutrition and health, and low stress) will tend to pro-
duce more sons than daughters [Fisher, 1930; Trivers and Willard, 1973]. Such female
reproductive flexibility results in diverse sex-biased birth patterns that act to balance
fitness benefits and maternal investment [Clutton-Brock et al., 1984; McFarland,
1987; Robinson, 1988; Di Bitetti and Janson, 2001].
Animals’ daily activities are rhythmic and affected by seasonal periodicity. Envi-
ronmental variables such as food supply and climatic factors (e.g., ambient tempera-
ture, precipitation and photoperiod, and variation in energy balance) are the ultimate
causes of seasonal breeding in all mammals and the proximate cause in many [Hern-
don, 1983; Crockett and Rudran, 1987a, b; Bronson, 1989; Gevaerts, 1992; Brockman
and van Schaik, 2005; Bronson, 2009; Xiang and Sayers, 2009; Tecot, 2010; Huang et
al., 2012; Li et al., 2014a]. Relying on external cues such as photoperiod and internal
cues such as food abundance, Brockman and van Schaik [2005] proposed two sea-
sonal birth modes – income breeders (give birth before the food peak) and capital
breeders (give birth at the end of the food peak). Seasonally breeding species usually
inhabit higher latitudes, where food availability and abiotic factors vary as local envi-
ronments change [Herndon, 1983]. Facing cyclical and hence predictable conditions,
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Reproductive Parameters of R. bieti
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DOI: 10.1159/000503246
Table 1. Reproduction parameters of African and Asian colobines
Species Site Birth season/
birth peak
Age at first
parturition,
years
IBI,
months
Infant
mortality
Birth
sex ratio
(F:M)
Reference
Colobus guereza Kibale 25.2 Struhsaker and
Leland, 1987
Colobus polykomos Tiwai 24 Dasilva, 1989
Procolobus badius Kibale Apr to Jun
and Nov
(peak)
25.5 Struhsaker and
Leland, 1987
Procolobus verus Tiwai Nov? to Feb?
(peak)
Struhsaker and
Leland, 1987
Presbytis thomasi Ketambe 5.4 22 1:1 Wich et al., 2007
Semnopithecus
entellus
Abu 25.4 Hrdy, 1974, 1977
Dharwar Nov to May
(peak)
Sugiyama, 1966,
1967
Jodhpur Mar (peak) 3.5 16.7 Sommer et al.,
1992
Kaukori Apr to May Dolhinow, 1972
Kanha Dec to May 40% Newton, 1987
Orcha weak 24 Dolhinow, 1972
Semnopithecus
schistaceus
Melemchi Feb to Apr 20–24 Bishop, 1979
Ramnagar Jan to Jun 6.7 28.8 Borries et al., 1999,
2001
Trachypithecus
pileatus
Arunachal
Pradesh
Dec to Apr 23.3 Solanki et al., 2007
Madhupur Dec to Apr 24 Stanford, 1993
Trachypithecus
vetulus
Polonnaruwa May to Aug
(peak)
23 Rudran, 1973
Horton Plains no 16.5 Rudran, 1973
Trachypithecus johnii Nilgiri district May to Jun 21 Poirier, 1970
Trachypithecus
phayrei
Phu Khieo Dec to Apr
(peak)
21.3–24.5 Borries et al., 2008
Trachypithecus
leucocephalus
Chongzuo Nov to Mar
(peak)
5–6 23.2 15.80% Jin et al., 2009
Pygathrix nemaeus Hin Namno Jun to Sep Phiapalath et al.,
2011
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animals tend to align reproduction with periods of relatively abundant resources and
suitable climate, improving offspring survival and reducing the risk of maternal death
[Crockett and Rudran, 1987a; Goldizen et al., 1988; Di Bitetti et al., 2000; Schoech and
Hahn, 2008]. This strategy can allow greater energy storage prior to gestation or min-
imize nutritional stress during lactation [Huang et al., 2012]. Since animals do not
always have enough energy to maintain both reproductive capacity and their own
metabolic needs, seasonal breeding maximizes individual fitness by synchronizing
energetically demanding periods of the breeding cycle with the season of greatest food
availability [Lancaster and Lee, 1965; Di Bitetti et al., 2000; Brockman and van Schaik,
2005; Tecot, 2010].
The endangered Yunnan snub-nosed monkey (Rhinopithecus bieti) lives in the
eastern Himalayan highlands, bounded by the upper Yangtze River and Mekong Riv-
ers [Long et al., 1994; Xiao et al., 2003; Li et al., 2010; Huang et al., 2012]. R. bieti is
characterized by a multilevel society [Kirkpatrick et al., 1998; Kirkpatrick and Grue-
ter, 2010; Ren et al., 2012], that is composed of 5–41 breeding units (one-male units,
OMUs) and 1 or more all-male units (AMUs) [Grueter and Zinner, 2004; Ren et al.,
2012; Grueter, 2013]. In R. bieti, females transfer between OMUs, and male offspring
also emigrate from their natal unit before sexual maturity [Kirkpatrick, 2007]. More
than two decades of studies on wild and captive groups have characterized the repro-
ductive behavior of R. bieti. With regard to seasonal birth patterns in captive groups,
Species Site Birth season/
birth peak
Age at first
parturition,
years
IBI,
months
Infant
mortality
Birth
sex ratio
(F:M)
Reference
Rhinopithecus bieti Wuyapiya Mar/Apr 36 55–60% Kirkpatrick et al.,
1998
Captive Dec to Jun 5 20.5 30% 1:4.4 Cui et al., 2006
Xiaochangdu Feb to Mar Xiang and Sayers,
2009
Mt Lasha Feb to Apr 24 Huang et al., 2012;
Li et al., 2014a
Xiangguqing Feb to Apr 5–6 24 15.50% 1:1 our research
Rhinopithecus
roxellana
Qinling Mar to May 5–6 21.9 22.40% 1:1.71 Qi et al., 2008
Captive Mar to Jun 18–20 Ren et al., 2003;
Zhang et al., 2000
Rhinopithecus brelichi Captive Mar to Apr 8.6 38.2 Yang et al., 2009
Simias concolor Pungut Sep to Oct
(peak)
Erb et al., 2012
Nasalis larvatus Kinabatangan/
Sukai
weak Boonratana, 1994
Tab le 1 (continued)
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Ji et al. [1998] reported that R. bieti living at the Kunming Zoo gave birth from Janu-
ary to June. Subsequently, Cui et al. [2006] reported a birth period from December to
June, with a birth peak observed from March to May, based on a 10-year study at the
Kunming Institute of Zoology and the Kunming Zoo. In wild groups, however, Kirk-
patrick et al. [1998] reported a birth season of March to April for R. bieti at Wuyapi-
ya. Xiang and Sayers [2009] found tightly synchronized births in their study popula-
tion as well, with newborns observed from February to March. Huang et al. [2012]
and Li et al. [2014a] suggested that wild R. bieti typically give birth from February to
April.
In this article, we present data on births recorded during systematic censuses of
known wild R. bieti groups over 9 consecutive years at Xiangguqing, Baimaxueshan
National Nature Reserve. We aimed to obtain accurate reproductive parameters of R.
bieti in Xiangguqing, including (i) birth sex ratio and infant mortality, (ii) birth tim-
ing and length of the breeding season and (iii) the IBI of adult females. We also com-
pare these reproductive parameters to those calculated for other Asian and African
colobines, then describe the differences among colobines and discuss the proximate
factors.
Materials and Methods
Study Areas and Species
Xiangguqing is located in the southernmost region of Baimaxueshan National Nature Re-
serve, Yunnan Province, China (99°22 E, 27°37 N). The site is approximately 10 km long and 9
km wide, about 90 km² in total area [Li et al., 2014a; Xia et al., 2016]. Xiangguqing contains mul-
tiple habitat types including mixed coniferous and deciduous broad-leaf forest, subalpine fir for-
est, montane sclerophyll oak forest, subtropical evergreen broad-leaf forest, and pine forest. The
study group inhabits subtropical evergreen broad-leaf forest, mixed deciduous broad-leaf and
conifer forest, and pine forest ranging from 2,600 to 3,200 m in altitude [Xia et al., 2016]. In 2008,
staff at Baimaxueshan successfully split a small group of 95 individuals away from a larger wild
group, forming a wild-living provisioned group at Xiangguqing [Ren et al., 2012], including 1
AMU with approximately 30 males and 8 OMUs [Li et al., 2013]. The staff fed a small amount of
food to them to habituate the monkeys to the researchers. Reserve management has occasionally
released individuals from this provisioned group into the wild [Zhu et al., 2016]. From 2010 to
2018, data on a total of 20 OMUs and 1 AMU were collected, from 45 to 93 individuals. Each year,
the study group consisted of 5–10 OMUs and 1 AMU. The demographic data recorded each July
are shown in Table 2.
Data Collection and Statistical Analyses
We recorded birth data in this group of R. bieti over a period of 9 years as part of long-term
population monitoring efforts. Rangers provisioned the study group twice daily (around 9: 00 and
17: 00) in one of several 30 m by 30 m areas located in nearby forest patches where the group
naturally ranges and feeds. The monkeys generally used the same provisioning site for 2–3 con-
secutive days, then moved to another part of their range [Zhu et al., 2016]. When feeding every
day, we counted the number of individuals in each unit, identified them and recorded birth data.
Birth data included the date of birth along with the sex of the newborn and the name of its moth-
er. We monitored the infant’s condition, and in the case of death, we recorded the date of death.
Circular statistics were used to test birth seasonality [Batschelet, 1981; Zar, 1999; Huang et
al., 2012; Li et al., 2014b]. We transformed birth dates into the degrees of a circle (360° = 1 year),
then calculated mean vector length r to determine whether the birth data were evenly distributed
throughout the year. The length of r indicates how observations are spread across the annual
cycle. When r = 1, all births occur on the same day of year, and when r = 0, the births are evenly
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Table 2. The demographic data for July of each year in the one-male units (OMUs) and all-male unit (AMU)
(2010–2018)
2010 2013 2016
OMU AM AF J I OMU AM AF J I OMU AM AF J I
DGZ 1 2 3 2 DGZ 1 3 3 1 DGZ 1 2 2 1
YDH 1 4 2 3 HL 1 4 2 XS 1 4 1
DB 1 4 2 1 DB 1 5 1 HL 1 4 1 4
SB 1 2 3 1 LHG 1 2 1 DB 1 1 1
HLG 1 4 3 HC 1 2 LHG 1 1 1 1
XW 1 4 4 3 PG 1 3 2 DS 1 1 1 1
HC 1 4 3 2 AMU 4 7 HD 1 6 3
GS 1 3 LB 1 1 3 1
AMU 7 12 AMU 1 4
2011 2014 2017
OMU AM AF J I OMU AM AF J I OMU AM AF J I
DGZ 1 4 3 DGZ 1 5 5 DGZ 1 2 3 1
YDH 1 4 5 1 HL 1 5 3 XS 1 4 3
BL 1 3 4 DB 1 3 1 2 HL 1 2 2
SB 1 3 1 LHG 1 1 1 1 DB 1 1 1
LHG 1 4 3 2 DS 1 4 1 LHG 1 1 2
XW 1 2 4 AMU 3 5 DS 1 1 2
HC 1 4 5 2 HD 1 6 3 4
PG 1 2 3 LB 1 1 2
HD 1 3 6 ML 1 1 2
AMU 8 8 JG 1 1 2
AMU 2 4
2012 2015 2018
OMU AM AF J I OMU AM AF J I OMU AM AF J I
DGZ 1 6 2 2 DGZ 1 4 5 2 DGZ 1 2 3 1
YDH 1 4 4 2 HL 1 4 3 XS 1 5 3 2
BL 1 2 1 1 DB 1 2 1 HL 1 2 2 2
DZ 1 4 3 LHG 1 2 1 DB 1 1 1
LHG 1 5 3 1 DS 1 1 1 LHG 1 1 1 1
XW 1 3 3 HD 1 7 1 HD 1 6 7 2
HC 1 7 4 2 LB 1 1 1 LB 1 2 1 1
PG 1 3 2 AMU 3 2 ML 1 3 1
AMU 4 6 CG 1 1 1
JG 1 2 1 1
AMU 2 4
AM, adult male; AF, adult female; J, juvenile; I, infant; other abbreviations are codes for resident males
(i.e., for OMUs).
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distributed across the 12 months [Batschelet, 1981]. We used the Kolmogorov-Smirnov test to
compare the difference in IBI between females whose infants died before the age of 1 year and
those whose infants survived for more than 1 year. All data are presented as means ± SD. The
binominal test was used to detect differences in birth sex ratio. As miscarriages are difficult to
observe in the wild, only pregnancies leading to births, including stillbirths, were used for analy-
sis [Qi et al., 2008]. All data were analyzed in SPSS 19.0. Statistical tests were two-tailed, with p <
0.05 taken as the threshold for significance:
22
11
cos sin
nn
i i ii
ii
f a fa
r
nn
 
 
 
 
 

==
,
where n is the mean of birth dates, and ai is the angle conversion value of day i.
Results
Sex Ratio and Infant Mortality
During the study period, 41 R. bieti females gave birth to 84 infants (43 males
and 41 females). The number of males and females born did not significantly differ,
so we could not reject the null hypothesis that the birth sex ratio was 1: 1 (51.19 vs.
48.81%, binomial test, p = 0.913). Among those 84 infants, 13 died in their first year
(Fig.1), a 15.5% mortality rate.
IBIs and Age at First Parturition
On the basis of 43 birth records from 27 continuously fertile mothers, the mean
IBI of the monkeys was 719.7 ± 239.7 days (mean ± SD, n = 43, range 293–1,502 days).
These IBIs were divided into two categories. The IBI of females whose infants sur-
vived for at least 1 year (category A) was 760.5 ± 226.1 days (mean ± SD, n = 36, range
399–1,502 days), whereas the IBI of females who lost their infants within the first year
(category B) was 510.1 ± 206.6 days (mean ± SD, n = 7, range 293–740 days). The IBI
of category A was significantly longer than that of category B (Kolmogorov-Smirnov
test: Z = 1.381, p = 0.023) (Fig.1, 2).
Subadult females left their natal unit and began breeding behavior as early as 3–4
years of age, but they did not conceive until they were 5 years of age. The age at first
parturition was known for 15 primiparous females, and the mean age was 6.13 years
(range: 5–9 years). Of the 15 primiparous females, 4 females first gave birth at the age
of 5, 8 females at 6, 1 female at 7, 1 female at 8, and 1 female at 9 (Fig.1).
Seasonal Birth and Length of the Reproduction Period
Circular statistical tests of periodicity in birth showed that r > 0.8, and as births
only occurred between February and June (Fig.3), we conclude that reproduction in
R. bieti is strictly seasonal. From 2010 to 2018, monkeys began giving birth on the
32nd day of the year (February 1) and finished on the 157th day (June 7), with a peak
between March 4 and March 11 (the 10th week of the year). The mean birth date was
March 20 (mean ± SD, 79.21 ± 29.54, n = 84), and the median birth date was March
11 (the 71th day). Out of 84 births for which the date of birth was confirmed, 73 births
(86.9%) occurred from February to April. Detailed information for each year is shown
in Figures 1 and 4 and Table 3.
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Fig. 1. The birth events during the 9 years from 2010 to 2018. Capital letters in parentheses are
codes for the infants’ fathers; a different code after a slash represents a replacement male which
sired new infant(s). B: birth of infant, F and M in parentheses are sexes of the infants. C: The fe-
male reached maturity. 1First birth; , replacement of the original resident male by a new male;
dInfant dead during first year; , adult female dead, , emigrated from this troop; , immigrated
to this troop.
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Seven years of observational data indicated a breeding season of 126 days, with
mean length per year of 98.57 ± 18.71 days (mean ± SD, n = 7; because only 1 infant
was born in 2013 and just 2 were born in 2015, we excluded these years as outliers)
(Table 3). Based on Brockman and van Schaik [2005], who proposed two seasonal
birth modes, R. bieti belongs to the income breeders.
Comparing the Reproduction Parameters among Asian and African Colobines
Limited previously published data suggest that most Asian and African colo-
bines are not strictly seasonal breeders. In contrast, members of the genus Rhinopithe-
cus have a strictly seasonal reproduction pattern, mainly concentrated from February
to April of each year (with some variation between populations and species: see Table
1). Age at first parturition is relatively uniform among the Asian and African colo-
bines except for captive Guizhou snub-nosed monkeys (Rhinopithecus brelichi: 8.6
years) and the gray langur (Semnopithecus entellus) in Jodhpur (3.5 years); all other
species first give birth around the age of 5–6 years (Table 1). The mean IBI of Asian
and African colobines taken together is approximately 2 years except for R. bieti at
Wuyapiya and captive R. brelichi (Table 1).
Discussion and Conclusion
Even Birth Sex Ratio and Lower Infant Mortality in R. bieti
Females in good condition tend to produce more sons than daughters in polyg-
ynous species [Fisher, 1930; Trivers and Willard, 1973]. However, we found a new-
born sex ratio close to 1: 1 at Xiangguqing from 2010 to 2018, with no significant bias
toward male infants, and the proportion of males in our study was smaller than that
found in captive R. bieti [Cui et al., 2006] and wild R. roxellana [Qi et al., 2008]. Wild
members of the genus Macaca seldom produce a biased sex ratio at birth, while ma-
caques living in captivity often do [Zhao and Deng, 1988]. Unlike captive popula-
1,500
1,250
1,000
750
500
250
Category A
IBI, days
Category B
*
Fig. 2. Difference in interbirth
interval (IBI) for females
whose infants survived within
the first year (category A) and
IBI for females whose infants
died within the first year (cat-
egory B). *p < 0.05.
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Dec Jan
Nov Feb
Oct Mar
Sep Apr
Aug
r = 0.97 Jul Jun
May
1.00
0.75
0.50
0.25
0
2010
Dec Jan
Nov Feb
Oct Mar
Sep Apr
Aug
r = 0.91 Jul Jun
May
2011
Dec Jan
Nov Feb
Oct Mar
Sep Apr
Aug
r = 0.91 Jul Jun
May
2012
Dec Jan
Nov Feb
Oct Mar
Sep Apr
Aug
r = 1 Jul Jun
May
1.00
0.75
0.50
0.25
0
2013
Dec Jan
Nov Feb
Oct Mar
Sep Apr
Aug
r = 0.95 Jul Jun
May
2014
Dec Jan
Nov Feb
Oct Mar
Sep Apr
Aug
r = 0.99 Jul Jun
May
2015
Dec Jan
Nov Feb
Oct Mar
Sep Apr
Aug
r = 0.80 Jul Jun
May
1.00
0.75
0.50
0.25
0
2016
Dec Jan
Nov Feb
Oct Mar
Sep Apr
Aug
r = 0.89 Jul
Proportion of births during month
Jun
May
2017
Dec Jan
Nov Feb
Oct Mar
Sep Apr
Aug
r = 0.83 Jul Jun
May
2018
0 0.25 0.50 0.75 1.00
Fig. 3. Circular histograms showing the proportion of births in each month from 2010 to 2018.
Note that the radial axis is the proportion of births during the month transformed to exaggerate
differences in the lower end of the scale. The red lines show the mean vector (r).
Color version available online
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tions, wild populations lack consistent access to high-quality food, shelter from ex-
treme climates and protection from predators [Berman, 1988; Aureli et al., 1990;
Koyama et al., 1992; Nevison et al., 1996]. Harsh conditions in the wild may eliminate
the advantage of a male-biased sex ratio at birth.
Infant mortality of R. bieti was 15.5% in this study, lower than that observed in
another wild population at Wuyapiya [55–60%, Kirkpatrick et al., 1998] and a captive
population [30%, Cui et al., 2006]. It was also lower than that found in other colobine
species, such as Semnopithecus entellus at Ramnagar [50%, Borries, 1997], Kanha
[40%, Newton, 1987], R. roxellana [22.4%, Qi et al., 2007] and Trachypithecus leuco-
Table 3. Reproductive parameters of R. bieti at four study areas
Site LAL AMSL,
m
Year Begin End Length,
days
Mn Md Nnb Nm Nf IM IBI,
days
BSR Data
algorithm
Reference
Xiaochang-
du (wild)
29°15 N,
98°37 E
3,500–
4,250
2005 Feb 4 Mar 14 38 58±
6.5
54 37 I/F estima-
tion
Xiang and
Sayers, 2009
Xiang-gu-
qing (provi-
sioned)
27°38 N,
99°21 E
2,600–
3,200
2010 Feb 10 Jun 3 114 67±
27.19
63 14 5 9 15.5% 722.6±
236.9
1:1 accurate
data
our research
2011 Feb 4 May 11 97 76±
24.84
72 862
2012 Feb 19 May 30 102 83±
25.66
76 17 8 9
2013 Mar 20 177 77 101
2014 Feb 2 Apr 4 62 61±
19.79
62 826
2015 Mar 8 Mar 9 266±
0.71
66 220
2016 Feb 4 May 27 114 82±
37.95
72 13 7 6
2017 Feb 24 May 23 89 88±
27.75
77 972
2018 Feb 16 Jun 7 112 90±
36.25
85 12 6 6
Mt.
Lasha
(wild)
26°20 N,
99°15 E
2,900–
3,600
2009 Feb 21 Apr 3 42 84±
11.58
79 11 I/F
estimation
Huang et al.,
2012;
Li et al.,
2014
2010 Feb 15 Apr 4 49 81±
19.48
89 16
2011 Feb 19 Apr 12 53 82±
17.23
75 13
2012 Feb 17 Apr 6 50 86±
17.27
86 15
2013 Feb 20 Apr 8 48 82±
16.9
77 13
Kunming
Zoo (captive)
25°03 N,
102°42 E
1,891 1991–
2003
Dec Jun ~210 107±
43
27 22 530% 624±
150
1:4.4 accurate
data
Cui et al.,
2006
LAL, latitude and longitude; AMSL, above mean sea level; Begin, End, Length indicate dates of beginning and end of the birth season and its length, respectively; Mn,
mean birth date (mean ± SD); Md, median birth date; Nnb, number of newborns; Nm, number of males; Nf, number of females; Im, infant mortality; IBI, interbirth interval;
BSR, birth sex ratio (female:male); I/F, infant-to-female ratio.
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DOI: 10.1159/000503246
cephalus [15.8%, Jin et al., 2009]. The climate and available food during the birth peak
(February to April) are not ideal for wild R. bieti, but many can find young leaves to
eat during this period [Li et al., 2011]. Jin et al. [2009] speculate that low infant mor-
tality may result from a prolonged lactation period. We hypothesize that infant mor-
tality is a function of lactation period [Jin et al., 2009], infanticide [Ren at al., 2011]
and the rate of inexperienced females giving birth, but this requires further testing. A
low infant mortality can also be a consequence of the additional food available [War-
ren et al., 2011], and our result was consistent with the hypothesis that the infant
mortality rate of the provisioned group is lower than that of the wild R. bieti group at
Wuyapiya.
Consistent Mean IBIs in Asian and African Colobines and the Proximate Cause
of IBI Length
Previously published data show that the mean IBI across all the Asian and Afri-
can colobines is approximately 2 years. In primates, prolonged lactation inhibits ovu-
lation and thus prevents pregnancy [Nadler et al., 1981; Frawley et al., 1983; Ziegler
et al., 1990]. Maternal infertility during lactation and the mother’s own nutritional
status determine birth interval length [Clutton-Brock et al., 1984; McFarland, 1987;
Robinson, 1988; Di Bitetti and Janson, 2001]. We found the mean IBI for R. bieti at
Xiangguqing was approximately 2 years, similar to that found in other wild popula-
tions of this species [Xiang and Sayers, 2009; Huang et al., 2012; Li et al., 2014a, b], in
R. roxellana [Qi et al., 2008] and in species such as M. fuscata, M. mulatta [Takahata
et al., 1998] and M. cyclopis [Hsu et al., 2001].
In the wild, food is scarce, and infants are highly dependent on their mothers for
nutrition in their first year of life [Li et al., 2005]. Wild colobines mainly feed on low-
quality food, which barely meets the nutritional requirements of both a newborn and
a female preparing for pregnancy. In these cases, the mother preferentially directs
0
2
3
4
6
8
10
12
14
16
18
Newborns, n
4 5 6 7 8 9 10 11 12 13 14
Weeks of the year
15 16 17 18 19 20 21 22 23 24 25 26
Md Mn
Fig. 4. Birth distribution from 2010 to 2018. Md, median; Mn, mean.
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Reproductive Parameters of R. bieti
13
Folia Primatol
DOI: 10.1159/000503246
energy towards the infant’s growth until it is weaned. Only then will the female begin
to build physiological reserves for her next pregnancy. This explains why the mean
IBI of females who lose their infants within the first year of birth is significantly short-
er than that of females whose infants survive. Similar results were reported for captive
R. bieti in Kunming [Cui et al., 2006] and in R. roxellana [Qi et al., 2008].
Environmental Conditions and Seasonal Reproduction
Brockman and van Schaik [2005] characterize most southeast Asian primates as
capital breeders showing moderate birth seasonality. According to this analysis (Ta-
ble 1), members of the genus Rhinopithecus are strictly seasonal breeders, concentrat-
ing their births from February to May of each year. Seasonal breeding in primates is
related to seasonal variations in climate and the availability of food [Brockman and
van Schaik, 2005; Qi et al., 2008; Jin et al., 2009; Xiang and Sayers, 2009; Huang et al.,
2012; Erb et al., 2012; Li et al., 2014a, b]. Rhinopithecus spp. live at higher altitudes
and latitudes than most other colobines, where temporal patchiness in food availabil-
ity and changes in climate are more pronounced over the course of a year [Newton
and Dunbar, 1994; Li et al., 2000]. The pattern of seasonal reproduction for high-
latitude species is more apparent than in low-latitude species [Di Bitetti and Janson,
2000], and this may be the proximate cause of seasonality in the births of snub-nosed
monkeys as opposed to other colobines.
There are also different reproduction parameters in different geographic popula-
tions of the same species (as in Rhinopithecus and Semnopithecus; Table 1). In addi-
tion to the environmental factors mentioned above, other reasons for the differences
in reproductive patterns between the populations of R. bieti include whether they are
wild, provisioned or captive, and how these parameters are calculated. Acquisition
and allocation of nutrients are considered the limiting factors controlling the timing
of reproduction [Di Bitetti and Janson, 2000; Brockman and van Schaik, 2005; Bron-
son, 2009]. Synchronizing energy-demanding periods of the breeding cycle with the
season having the greatest food availability or quality promotes offspring survival
[Lancaster and Lee, 1965; Di Bitetti et al., 2000; Brockman and van Schaik, 2005;
Tecot, 2010]. Therefore food supplementation, especially in periods of nutritional
stress, will likely improve the body condition of R. bieti, thus affecting their reproduc-
tion. Our results show an actual breeding season longer than what would be estimat-
ed using the infant-to-female ratio (a method of inferring reproductive parameters
by the change in the ratio of infants to females) in wild R. bieti [Xiang and Sayers,
2009; Huang et al., 2012; Li et al., 2014a, b]. Due to the limitations of field observa-
tions, including distance and poor weather conditions, the value of the infant-to-fe-
male ratio fluctuates greatly, sometimes yielding estimates that deviate substantially
from observed birth patterns and underestimate the length of the birth season [Wang
et al., 2012].
In conclusion, we present the first detailed analysis of the reproductive param-
eters of R. bieti in its natural habitat, demonstrating that R. bieti has strictly seasonal
reproduction. Females typically gave birth for the first time at 6.13 years old, the birth
sex ratio was 1: 1, 15.5% of infants died within their first year, and IBIs were approxi-
mately 2 years. Comparing the reproduction parameters among Asian and African
colobines, we concluded that the colobines generally have an IBI of 2 years or more,
with females also giving birth for the first time at the age of 5–6 years. Compared with
other colobines, snub-nosed monkeys’ reproduction is more strictly seasonal, with
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DOI: 10.1159/000503246
References
Aureli F, Schino G, Cordischi C, Cozzolino R, Scucchi S, van Schaik CP (1990). Social factors affect sec-
ondary sex ratio in captive Japanese macaques. Folia Primatologica 55: 176–180.
Batschelet E (1981). Circular Statistics in Biology. London, Academic Press.
Bercovitch FB (2002). Sex-biased parental investment in primates. International Journal of Primatology
23: 905–921.
Berman CM (1988). Maternal condition and offspring sex ratio in a group of free-ranging rhesus mon-
keys: an eleven-year study. American Naturalist 131: 307–328.
Bishop NH (1979). Himalayan langurs: temperate colobines. Journal of Human Evolution 8: 251–281.
Boonratana R (1994). The Ecology and Behaviour of the Proboscis Monkey (Nasalis larvatus) in the Lower
Kinabatangan, Sabah. PhD dissertation, Mahidol University.
Borries C (1997). Infanticide in seasonally breeding multimale groups of Hanuman langurs (Presbytis en-
tellus) in Ramnagar (South Nepal). Behavioral Ecology and Sociobiology 41: 139–150.
Borries C, Koenig A, Winkler P (2001). Variation of life history traits and mating patterns in female langur
monkeys (Semnopithecus entellus). Behavioral Ecology and Sociobiology 50: 391–402.
births concentrated between February and April. Seasonal changes in food resources
and climatic factors most likely drive the variation in reproductive parameters
throughout the Asian and African colobines.
Acknowledgment
We are grateful to our field assistants Tai Zhong, Jianhua Yu, Jinming Yu and Lizhong Yu.
We thank Baimaxueshan National Nature Reserve for our work permit.
Statement of Ethics
The authors have no ethical conflicts to disclose.
Disclosure Statement
The authors have no conflicts of interest to declare.
Funding Sources
Financial support was provided by the project of the National Key Programme of Research
and Development, Ministry of Science and Technology (No. 2016YFC0503200), NSFC (No.
31470461), Sichuan Youth Science and Technology Foundation (No. 2015JQ0024) and the Ap-
plied Basic Research Program of Sichuan Province (No. 2017JY0325).
Author Contributions
Wancai Xia and Dayong Li wrote the manuscript; Wancai Xia, Hong Zhou, Hao Feng and
Xinming He collected field data; Xiaofeng Luan, Baoping Ren, Ali Krzton and Majda Aouititen
revised the manuscript.
Downloaded by:
Sichuan University
202.115.54.187 - 11/14/2019 7:51:58 AM
Reproductive Parameters of R. bieti
15
Folia Primatol
DOI: 10.1159/000503246
Borries C, Larney E, Lu A, Ossi K, Koenig A (2008). Costs of group size: lower developmental and repro-
ductive rates in larger groups of leaf monkeys. Behavioral Ecology 19: 1186–1191.
Borries C, Launhardt K, Epplen C, Epplen JT, Winkler P (1999). Males as infant protectors in Hanuman
langurs (Presbytis entellus) living in multimale groups – defense pattern, paternity and sexual behav-
iour. Behavioral Ecology and Sociobiology 46: 350–356.
Brockman DK, van Schaik CP (2005). Seasonality and reproductive function. In Seasonality in Primates:
Studies of Living and Extinct Human and Non-human Primates (Brockman DK, van Schaik CP,
eds.), pp 269–306. Cambridge, Cambridge University Press.
Bronson FH (1989). Mammalian Reproductive Biology. Chicago, University of Chicago Press.
Bronson FH (2009). Climate change and seasonal reproduction in mammals. Philosophical Transactions
of the Royal Society of London B Biological Sciences 364: 3331–3340.
Clutton-Brock TH, Albon SD, Guinness FE (1984). Maternal dominance, breeding success and birth sex
ratios in red deer. Nature 308: 358–360.
Crockett CM, Rudran R (1987a). Red howler monkey birth data. I. Seasonal variation. American Journal
of Primatology 13: 347–368.
Crockett CM, Rudran R (1987b). Red howler monkey birth data. II. Inter annual, habitat, and sex com-
parisons. American Journal of Primatology 13: 369–384.
Cui LW, Sheng AH, He SC, Xiao W (2006). Birth seasonality and inter-birth interval of captive Rhino-
pithecus bieti. American Journal of Primatology 68: 457–463.
Dasilva GL (1989). The Ecology of the Western Black and White Colobus (Colobus polykomos Zimmerman
1780) on a Riverine Island in Southeastern Sierra Leone. PhD thesis, University of Oxford.
Di Bitetti MS, Janson CH (2000). When will the stork arrive? Patterns of birth seasonality in neotropical
primates. American Journal of Primatology 50: 109–130.
Di Bitetti MS, Janson CH (2001). Reproductive socioecology of tufted capuchins (Cebus apella nigritus)
in northeastern Argentina. International Journal of Primatology 22: 127–142.
Di Bitetti MS, Vidal EML, Baldovino MC, Benesovsky V (2000). Sleeping site preference in tufted capu-
chin monkeys (Cebus apella nigritus). American Journal of Primatology 50: 257–274.
Dunbar RIM (1988). Primate Social Systems. London, Croom Helm.
Dolhinow PJ (1972). The North Indian langur. In Primate Patterns (Dolhinow PJ, ed.), pp 181–238. New
York: Holt, Rinehart & Winston.
Erb WM, Borries C, Lestari NS, Hodges JK (2012). Annual variation in ecology and reproduction of wild
simakobu (Simias concolor). International Journal of Primatology 33: 1406–1419.
Fedigan LM, Griffin L (1996). Determinants of reproductive seasonality in the Arashiyama West Japanese
macaques. In Evolution and Ecology of Macaque Societies (Fa JE, Lindburg DG, eds.), pp 369–388.
Cambridge, Cambridge University Press.
Fisher RA (1930). The Genetical Theory of Natural Selection. New York, Dover Publications.
Frawley LS, Mulchahey JJ, Neill JD (1983). Nursing induces a biphasic release of prolactin in rhesus mon-
keys. Endocrinology 112: 558–561.
Gevaerts H (1992). Birth seasons of Cercopithecus, Cercocebus and Colobus in Zaire. Folia Primatologica
59: 105–113.
Goldizen AW, Terborgh J, Corejo F, Porras DT, Evans R (1988). Seasonal food shortage, weight loss, and
the timing of births in saddleback tamarins (Saguinus fuscicollis). Animal Ecology 57: 893–901.
Grueter CC (2013). The Biology of Snub-Nosed Monkeys, Douc Langurs, Proboscis Monkeys, and Simako-
bus. New York, Nova Biomedical.
Grueter CC, Zinner D (2004). Nested societies, convergent adaptations of baboons and snub nosed mon-
keys. Primate Report 70: 1–98.
Herndon JG (1983). Seasonal breeding in rhesus monkeys: influence of the behavioral environment.
American Journal of Primatology 5: 197–204.
Hrdy SB (1974). Male-male competition and infanticide among the langurs (Presbytis entellus) of Abu,
Rajasthan. Folia Primatologica 22: 19–58.
Hrdy SB (1977). The Langurs of Abu: Female and Male Strategies of Reproduction. Cambridge, Harvard
University Press.
Hsu MJ, Agoramoorthy G, Lin JF (2001). Birth seasonality and interbirth intervals in free ranging Formo-
san macaques, Macaca cyclopis, at Mt. Longevity, Taiwan. Primates 42: 15–25.
Huang ZP, Cui LW, Scott MB, Wang SJ, Xiao W (2012). Seasonality of reproduction of wild black-and-
white snub-nosed monkeys (Rhinopithecus bieti) at Mt. Lasha, Yunnan, China. Primates 53: 237–
245.
Ji WZ, Zou RJ, Shang EY, Zhou HW, Yang SC, Tian BP (1998). Maintenance and breeding of Yunnan
snub-nosed monkeys (Rhinopithecus bieti) in captivity. In The Natural History of the Doucs and
Snub-Nosed Monkeys (Jablonski NG, ed.), pp 323–335. Singapore, World Scientific.
Jin T, Wang DZ, Zhao Q, Yin LJ, Pan WS (2009). Reproductive parameters of wild Trachypithecus leuco-
cephalus: seasonality, infant mortality and interbirth interval. American Journal of Primatology 71:
558–566.
Downloaded by:
Sichuan University
202.115.54.187 - 11/14/2019 7:51:58 AM
Folia Primatol
16 Xia/Ren/Zhou/Feng/He/Krzton/Hu/Aouititen/
Luan/Li
DOI: 10.1159/000503246
Kirkpatrick RC (2007). The Asian colobines: diversity among leaf-eating monkeys. In Primates in Perspec-
tive (Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK, eds.), pp 186–200. New York,
Oxford University Press.
Kirkpatrick RC, Grueter CC (2010). Snub-nosed monkeys: multilevel societies across varied environ-
ments. Evolutionary Anthropology 19: 98–113.
Kirkpatrick RC, Long YC, Zhong T, Xiao L (1998). Social organization and range use in the Yunnan snub-
nosed monkey Rhinopithecus bieti. International Journal of Primatology 19: 13–51.
Koyama N, Takahata Y, Huffman MA, Norikoshi K, Suzuki H (1992). Reproductive parameters of female
Japanese macaques: thirty years data from the Arashiyama troops, Japan. Primates 33: 33–47.
Lancaster JB, Lee RB (1965). The annual reproductive cycle in monkeys and apes. In Primate Behavior
(Devore I, ed.), pp 486–513. New York, Holt, Rinehart & Winston.
Li BG, Chen C, Ji WH, Ren BP (2000). Seasonal home range changes of the Sichuan snub-nosed monkey
(Rhinopithecus roxellana) in the Qinling Mountains of China. Folia Primatologica 71: 375–386.
Li DY, Ren BP, Li BG, Li M (2010). Range expansion as a response to increasing group size in the Yunnan
snub-nosed monkey. Folia Primatologica 81: 315–329.
Li DY, Ren BP, He XM, Hu G, Li BG, Li M (2011). Diet of Rhinopithecus bieti at Xiangguqing in Baimax-
ueshan National Nature Reserve (in Chinese). Acta Theriologica Sinica 31: 338–346.
Li JF, He YC, Huang ZP, Wang SJ, Xiang ZF, Zhao JJ (2014a). Birth seasonality and pattern in black-and-
white snub-nosed monkeys (Rhinopithecus bieti) at Mt. Lasha, Yunnan. Zoological Research 35:
474–484.
Li TF, Ren BP, Li DY, Zhu PF, Li M (2013). Mothering style and infant behavioral development in Yun-
nan snub-nosed monkeys (Rhinopithecus bieti) in China. International Journal of Primatology 34:
681–695.
Li YH, Li BG, Tan LC (2005). Behavioral development of individuals within one-year-old individuals of
Sichuan snub-nosed monkeys Rhinopithecus roxellana in the Qinling Mountains. Acta Zoologica
Sinica 51: 953–960.
Li YH, Li DY, Ren BP, Hu J, Li BG, Krzton A, Li M (2014b). Differences in the activity budgets of Yunnan
snub-nosed monkeys (Rhinopithecus bieti) by age-sex class at Xiangguqing in Baimaxueshan Nature
Reserve, China. Folia Primatologica 85: 335–342.
Long YC, Kirkpatrick RC, Zhong T, Xiao L (1994). Report on the distribution, population, and ecology of
the Yunnan snub-nosed monkey (Rhinopithecus bieti). Primates 35: 241–250.
McFarland SM (1987). Sex ratio and maternal rank in wild spider monkeys: when daughters disperse. Be-
havioral Ecology and Sociobiology 20: 421–425.
Nadler RD, Graham CE, Collins DC, Kling OR (1981). Postpartum amenorrhea and behavior of apes. In
Reproductive Biology of the Great Apes (Graham CE, ed.), pp 69–81. London, Academic Press.
Nevison CM, Rayment FDG, Simpson MJA (1996). Birth sex ratios and maternal social rank in a captive
colony of rhesus monkeys (Macaca mulatta). American Journal of Primatology 39: 123–138.
Newton PN (1987). The social organization of forest Hanuman langurs (Presbytis entellus). International
Journal of Primatology 8: 199–232.
Newton PN, Dunbar RIM (1994). Colobine monkey society. In Colobine Monkeys: Their Ecology, Behav-
iour and Evolution (Davies AG, Oates JF, eds.), pp 311–346. Cambridge, Cambridge University
Press.
Phiapalath P, Borries C, Suwanwaree P (2011). Seasonality of group size, feeding, and breeding in wild
red-shanked douc langurs (Lao PDR). American Journal of Primatology 73: 1134–1144.
Poirier FE (1970). The Nilgiri langur (Presbytis johnii) of South India. In Primate Behavior: Developments
in Field and Laboratory Research (Rosenblum RA, ed.), pp 251–383. New York, Academic Press.
Qi XG, Li BG, Ji WH (2008). Reproductive parameters of wild female Rhinopithecus roxellana. American
Journal of Primatology 70: 311–319.
Ren BP, Li DY, Garber PA, Li M (2012). Fission-fusion behavior in Yunnan snub-nosed monkeys (Rhi-
nopithecus bieti) in Yunnan, China. International Journal of Primatology 33: 1096–1109.
Ren BP, Li DY, He XM, Qiu J, Li M (2011). Female resistance to invading males increases infanticide in
langurs. PLoS One 6: e18971.
Ren BP, Zhang SY, Xia SZ, Li QF, Liang B, Lu MQ (2003). Annual reproductive behavior of Rhinopithecus
roxellana. International Journal of Primatology 24: 575–589.
Robinson JG (1988). Demography and group structure in wedge-capped capuchin monkeys, Cebus oliva-
ceus. Behaviour 104: 202–232.
Rudran R (1973). The reproductive cycles of two subspecies of purple-faced langurs (Presbytis senex) with
relation to environmental factors. Folia Primatologica 19: 41–60.
Schoech SJ, Hahn TP (2008). Retracted article: Latitude affects degree of advancement in laying by birds
in response to food supplementation: a meta-analysis. Oecologia 157: 369–376.
Smith JLD, McDougal C (1991). The contribution of variance in lifetime reproduction to effective popu-
lation size in tigers. Conservation Biology 5: 484–490.
Downloaded by:
Sichuan University
202.115.54.187 - 11/14/2019 7:51:58 AM
Reproductive Parameters of R. bieti
17
Folia Primatol
DOI: 10.1159/000503246
Solanki GS, Kumar A, Sharma BK (2007). Reproductive strategies of Trachypithecus pileatus in Arunachal
Pradesh, India. International Journal of Primatology 28: 1075–1083.
Sommer V, Srivastava A, Borries C (1992). Cycles, sexuality, and conception in free-ranging langurs (Pres-
bytis entellus). American Journal of Primatology 28: 1–27.
Stanford CB (1993). The capped langur in Bangladesh: behavior ecology and reproductive tactics. Inter-
national Journal of Primatology 14: 511–512.
Struhsaker TT, Leland L (1987). Colobines: infanticide by adult males. In Primate Societies (Smuts B,
Wrangham RW, Cheney DL, Struhsaker TT, Seyfarth RM, eds.), pp 83–97. Chicago, University of
Chicago Press.
Sugiyama Y (1966). An artificial social change in a hanuman langur troop (Presbytis entellus). Primates 7:
41–72.
Sugiyama Y (1967). Social organization of hanuman langurs. In Social Communication among Primates
(Altmann S, eds.), pp 221–236. Chicago, University of Chicago Press.
Takahata Y, Suzuki S, Agetsuma N, Okayasu N, Sugiura H, Takahashi H, Yamagiwa J, Izawa K, Furuichi
T, Hill DA, Maruhashi T, Saito C, Saito S, Sprague DS (1998). Reproduction of wild Japanese ma-
caque females of Yakushima and Kinkazan Islands: a preliminary report. Primates 39: 339–349.
Tecot SR (2010). It’s all in the timing: birth seasonality and infant survival in Eulemur rubriventer. Inter-
national Journal Primatology 31: 715–735.
Trivers R, Willard D (1973). Natural selection of parental ability to vary the sex ratio of offspring. Science
179: 90–92.
Wang SJ, Huang ZP, He YC, He XD, Li DH, Sun J, Cui LW, Xiao W (2012). Mating behavior and birth
seasonality of black-and-white snub-nosed monkeys (Rhinopithecus bieti) at Mt. Lasha (in Chinese).
Zoological Research 33: 241–248.
Warren Y, Higham JP, Maclarnon AM, Ross C (2011). Crop-raiding and commensalism in olive baboons:
the costs and benefits of living with humans. In Primates of Gashaka II (Sommer V, Ross C, eds.),
pp 359–384. New York, Springer.
Wich SA, Steenbeek R, Sterck EHM, Korstjens AH, Willems EP, van Schaik CP (2007). Demography and
life history of Thomas langurs (Presbytis thomasi). American Journal of Primatology 69: 641–651.
Xia WC, Ren BP, Li YH, Hu J, He XM, Krzton A, Li M, Li DY (2016). Behavioural responses of Yunnan
snub-nosed monkeys (Rhinopithecus bieti) to tourists in a provisioned monkey group in Baimaxue-
shan Nature Reserve. Folia Primatologica 87: 349–360.
Xiang ZF, Sayers K (2009). Seasonality of mating and birth in wild black-and-white snub-nosed monkeys
(Rhinopithecus bieti) at Xiaochangdu, Tibet. Primates 50: 50–55.
Xiao W, Ding W, Cui LW, Zhou RL, Zhao QK (2003). Habitat degradation of Rhinopithecus bieti in Yun-
nan, China. International Journal of Primatology 24: 389–398.
Yang MY, Sun DY, Zinner D, Roos C (2009). Reproductive parameters in Guizhou snub-nosed monkeys
(Rhinopithecus brelichi). American Journal of Primatology 71: 266–270.
Zar JH (1999). Biostatistical Analysis, 4th ed. Upper Saddle River, Prentice Hall.
Zhang FH, Wu SB, Yang L, Zhang L, Sun RY, Li SS (2015). Reproductive parameters of the Sunda pango-
lin, Manis javanica. Folia Zoologica 64: 129–135.
Zhang SY, Liang B, Wang LX (2000). Seasonality of matings and births in captive Sichuan golden monkeys
(Rhinopithecus roxellana). American Journal of Primatology 51: 265–269.
Zhao QK, Deng ZY (1988). Macaca thibetana at Mt. Emei, China. II. Birth seasonality. American Journal
of Primatology 16: 261–268.
Zhu PF, Ren BP, Garber PA, Xia F, Grueter CC, Li M (2016). Aiming low: a resident male’s rank predicts
takeover success by challenging males in Yunnan snub-nosed monkeys. American Journal of Prima-
tology 78: 974–982.
Ziegler TE, Widowski TM, Larson ML, Snowdon CT (1990). Nursing does affect the duration of the post-
partum to ovulation interval in cotton-top tamarins (Saguinus oedipus). Journal of Reproduction and
Fertility 90: 563–570.
Downloaded by:
Sichuan University
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... They live in polygynous one-male units (OMUs) or 'harems' that are part of a larger multilevel society [29,53]. They are characterized by strictly seasonal reproduction and a mean interbirth interval of approximately 2 years [54]. Harem holders possess nearly exclusive mating rights over all females in the harem. ...
... From March 2010 to December 2020, a total of 26 OMUs and 1 AMU (182 individuals) were recorded in the research group. Each year, the research group consisted of 5-10 OMUs and 1 AMU, ranging from 45 to 72 individuals [54]. ...
... There may be several reasons for this finding. First, female Yunnan snub-nosed monkeys give birth every two years on average [54], thus reducing reproductive competition during years when they take a reproductive time out. Second, Yunnan snubnosed monkey harems are composed mostly of related females [29], and nepotistic cooperation such as allocare and allonursing may promote successful reproduction. ...
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Simple Summary: The size of primate 'harems' varies considerably, both inter-and intra-specifically. Previous studies have shown that females prefer high-quality males and that high-quality males are superior in inter-male competition, leading to them having a larger harem size. Based on eleven years of observations of Yunnan snub-nosed monkeys (Rhinopithecus bieti), we documented longitudinal stability in the distribution of harem sizes between 2010 and 2020. These demographic properties are the outcome of male and female social investment decisions that affect their reproductive performance and success. Male reproductive success was positively related to harem size, while constraints on individual social benefits and social investments limited harem size. Our findings advance our understanding of the socioecological determinants of harem size variation in polygynous primates. Abstract: We used long-term data on the variation in harem size in Yunnan snub-nosed monkeys to research the effects of harem size on reproductive success and the ratio of grooming received to given (RGRG). The results suggest that harem holders derive reproductive benefits commensurate with harem size, whereas the females' reproductive success is unaffected by harem size. Males of larger harems groomed less and had higher RGRG than males of smaller harems. In the case of females, grooming given increased, and RGRG decreased with an increase in harem size. The males' reproductive success seems to be a driver of harem size maximization. From the females' perspective, dwindling social benefits appear to set the upper limit for harem enlargement. We also showed that males of monogamous units ('single-female harems') invested more into grooming their female, presumably to prevent unit disintegration and loss of mating privileges.
... Since the end of 2009, all individuals have been identified (Xia et al. 2020b). From 2010 to 2018, a total of 22 OMUs and 1 AMU (158 individuals, including 83 males and 75 females) were recorded in the focal group (Xia et al. 2020c). Each year, the focal group consisted of 5-10 OMUs and 1 AMU, ranging from 45 to 93 individuals (Xia et al. 2020c). ...
... From 2010 to 2018, a total of 22 OMUs and 1 AMU (158 individuals, including 83 males and 75 females) were recorded in the focal group (Xia et al. 2020c). Each year, the focal group consisted of 5-10 OMUs and 1 AMU, ranging from 45 to 93 individuals (Xia et al. 2020c). ...
... In 2008 and 2009, not all individuals could be reliably identified, so data from those two years was only used to calculate the age of known individuals. The age of unknown individuals was assessed by body color, body size, and the thinning of white hairs on the back (Xia et al. 2020c). Accurate and detailed dispersal data was recorded over nine years (2010.1.1-2018.12.31) for this group as part of long-term population monitoring. ...
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Sex-biased dispersal is common in group-living animals. Due to differences in local demographic and environmental factors, sex-biased dispersal presents many irregular patterns. In this study, a habituated, individually-identified Yunnan snub-nosed monkey Rhinopithecus bieti group was observed over 9 years; 192 dispersal events, including 97 male dispersal events (25 natal dispersal, 72 secondary dispersal) and 95 female dispersal events (34 natal dispersal, 61 secondary dispersal) were observed. Males and females showed different dispersal paths, dispersal ages and dispersal patterns. Females had two dispersal paths, while males had four paths. In terms of age of dispersal, the male age of natal dispersal was younger than for females. Males prefer single dispersal, while females prefer parallel dispersal. Our study indicates that the dispersal pattern of R. bieti should be classified as a bisexual dispersal pattern. The differences in dispersal path, average age at dispersal, and dispersal path pattern indicate that Yunnan snub-nosed monkeys may still retain a loose matrilineal social system.
... Phylogeny has a strong effect on age at first reproduction and IBI (Borries et al. 2011;Shelmidine et al. 2009). For example, Asian colobine species give birth for the first time normally at 5-6 yr, with an IBI of 24 mo (Qi et al. 2008;Xia et al. 2019). In contrast, female great apes usually begin to breed at 10-15 yr, with an IBI of ca. ...
... Moreover, primiparous mothers may harm their offspring through inappropriate nursing or infant abandonment, resulting in a higher rate of offspring mortality compared to multiparous mothers, as observed in mountain gorillas (Gorilla beringei: Robbins et al. 2006). In addition, infant loss may accelerate reproduction, resulting in shorter IBI (Cui et al. 2006;Hodgkiss et al. 2010;Qi et al. 2008;Xia et al. 2019). ...
... We used χ 2 tests to determine if the sex ratio of newborns deviated from 1:1. Because infant loss shortens the IBI (Cui et al. 2006;Hodgkiss et al. 2010;Xia et al. 2019), we excluded any IBI for females whose infants had died within 18 mo (1.5 yr) from comparative analyses of IBI. For yellow-cheeked gibbons, we excluded 7 IBIs because the sex of the offspring was unidentified. ...
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Reproductive and life-history characteristics, such as age at first reproduction, interbirth interval (IBI), sex ratio of newborns, and infant mortality, are crucial for assessing the population dynamics and survival of threatened species. There are no longitudinal data on the life histories of the threatened northern white-cheeked gibbons (Nomascus leucogenys) and yellow-cheeked gibbons (Nomascus gabriellae). Here, we examine the reproductive parameters of these species in 19 Chinese zoos. Some of these captive individuals may be hybrids of N. leucogenys × N. gabriellae, but it is not possible to distinguish these hybrids from the parent species based on morphological characteristics. Thus, in this study we identified individuals to species level from the zoos’ archives. Based on breeding records, 46 infants were born to 14 female northern white-cheeked gibbons from 2000 to 2019 and 89 infants to 29 female yellow-cheeked gibbons from 1995 to 2018. The mean age at first reproduction was 10.1 ± SD 2.4 yr for northern white-cheeked gibbons and 10.0 ± SD 3.1 yr for yellow-cheeked gibbons. The mean IBI was 32.8 ± SD 11.7 mo for northern white-cheeked gibbons and 27.2 ± SD 14.8 mo for yellow-cheeked gibbons. There was no significant effect of parity on IBI in northern white-cheeked gibbons, but primiparous mothers had a significantly longer IBI than multiparous mothers in yellow-cheeked gibbons. There was no significant difference in infant mortality between primiparous and multiparous mothers for either species. The sex ratio of newborns did not deviate significantly from 1:1 for either species. Infant mortality was 13% for northern white-cheeked gibbons and 12% for yellow-cheeked gibbons. Infant death reduced the IBI by 19 mo in northern white-cheeked gibbons and 10 mo in yellow-cheeked gibbons. Our data suggest that the intrinsic reproduction rate is very low in these gibbons and that wild populations may continue to decline without suitable conservation intervention.
... It is made available under a The copyright holder for this preprint this version posted August 11, 2020. . https://doi.org/10.1101/2020 The present study corroborates the hominoid slowdown hypothesis (Goodman, 1985;Li and Tanimura, 1987;Steiper et al., 2004) as the paths of the families Hominidae and Hylobatidae are fairly short relative to other groups of the Primates, which is more evident resolving the phylogeny by the ME method (Fig. 3). ...
... kg) than it is in H. s. sapiens (57.2 kg) (Kappelman, 1996) and accordingly P. troglodytes gives first birth ~1.1 years earlier than H. s. sapiens ( Fig. 3 The copyright holder for this preprint this version posted August 11, 2020. . https://doi.org/10.1101/2020 This all suggests that the relatively small-bodied members of the human lineage have probably reached sexual maturity faster than living humans, which confirms inferences from the branch lengths. ...
... The copyright holder for this preprint this version posted August 11, 2020. . https://doi.org/10.1101/2020 . CC-BY-NC 4.0 International license (which was not certified by peer review) is the author/funder. ...
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mtDNA-based phylogenetic trees of the order Primates were constructed by the minimum evolution (ME) and maximum likelihood (ML) methods. Branch lengths were compared with the mean female age at first birth in the taxa studied. Higher reproductive age in females triggers a lower number of generations through time and, on average, at the molecular level smaller evolutionary distances between related taxa. However, this relationship is significant when the phylogeny is resolved by the ME method rather than the ML method. Reliability of the minimum evolution approach is discussed. In contrast to most studies, the ME tree recovers Tarsius bancanus (Tarsiiformes) as a member of the Strepsirrhini, which phylogeny is supported by a strong branch length−reproductive age relationship and which is proposed as a novel heuristic method to test phylogeny. However, branches of certain taxa on the constructed phylogenetic tree show anomalous lengths relative to the mean female age at first birth, such as e.g. the human branch. As estimated in this paper, early members of the human lineage have likely reproduced at higher rates than modern humans, some forms possibly giving first birth at the mean age of 10−12 years, which is more comparable to the mean age at first birth in extant gorillas than to that typical of living humans and chimpanzees. Probable early reproduction in human ancestors is also supported by the comparably more evolved mitochondrial DNA in Denisovans than in modern humans, and by a smaller body mass in most fossil hominins, which often triggers fast maturation in primates.
... We found that, compared with resident males, AMU bachelors were more active participants in mating with females. Bachelors responded more when solicited by females, and they initiated more matings during part of the reproductive season (Xia et al. 2019). Black-and-white snub-nosed monkeys display birth seasonality both in captivity and in the field (Cui and Xiao 2004;Xia et al. 2019). ...
... Bachelors responded more when solicited by females, and they initiated more matings during part of the reproductive season (Xia et al. 2019). Black-and-white snub-nosed monkeys display birth seasonality both in captivity and in the field (Cui and Xiao 2004;Xia et al. 2019). In the harshest known habitat of this species, the Xiaochangdu troop mates mostly between July and October (Xiang and Sayers 2009). ...
... A follow-up study on the same band indicated that intra-unit matings are concentrated between July and December . Similarly, in the present study, most sneak matings between AMU bachelors and females occurred between September and January (Fig. 1), part of the reproductive season of the focal band (Xia et al. 2019). We infer that AMU males might fertilize females on at least some of these occasions. ...
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Snub-nosed monkeys exhibit a rare multilevel social system composed of several one-male units (OMU) and at least one all-male unit (AMU). The AMU comprises males who are blocked from access to females by resident males in the OMUs, and how these satellite males achieve reproductive success is still unclear. To investigate their reproductive strategies, we focused on the AMU in a band of provisioned black-and-white snub-nosed monkeys (Rhinopithecus bieti) in Yunnan, China. Behaviors that AMU males use to gain access to females (i.e. immigration, male takeover, and sexual interaction with females) were recorded and compared with resident OMU males to explore how AMU bachelors achieve reproductive success when they are denied stable access to females. We found that in response to solicitation from females, adult and sub-adult members of the AMU responded more actively than resident males, and the bachelors actively initiated mating with females when the latter's resident male was temporarily absent. These mating opportunities mostly coincided with the peak mating season in OMUs, and probably allowed bachelors to sire some offspring. We also found that for some AMU adults, taking over an OMU is the main strategy used to gain stable access to females, and these males repeatedly migrate between bands. AMU members therefore show multiple strategies that allow them to gain some degree of reproductive success.
Chapter
The golden snub‐nosed monkey, or golden monkey, inhabits the eastern Yangtze River. The black‐and‐white snub‐nosed monkey or Yunnan snub‐nosed monkey survives between the upper reaches of the Yangtze River and the Upper Mekong River. The bones, brains and other body parts of black‐and‐white snub‐nosed monkeys were then used to prepare medicinal remedies, which amounted to several dozen animals per year in the late 1970s and early 1980s. A spatial modeling of the ecological network of black‐and‐white snub‐nosed monkeys was then carried out in order to evaluate the degree of connectivity of its habitats and the impact of different development scenarios. Ecotourism responds to a demand for interaction with nature, while developing biodiversity conservation programs and increasing financial and educational benefits for local communities.
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Ecotourism is increasing worldwide for financial, educational and social purposes. Organized viewing of wildlife, especially at feeding sites where wildlife is “ready-to-view”, increases the opportunities for tourists to observe animals in the wild. However, feeding sites might retain only a subsample of wild populations. We thus hypothesized that such human intervention could induce population subdivisions and alter random mating by artificially creating small groups. The endangered Yunnan snub-nosed monkey (Rhinopithecus bieti) is an emblematic example reflecting the contradictions between conservation and ecotourism. In Gehuaqing/Xiangguqing (Yunnan, China), some individuals are maintained at feeding sites, while the rest of the monkey subpopulation wanders in a large surrounding area. Using faecal sampling and molecular analyses, we showed that this subpopulation is genetically structured into two moderately differentiated subgroups. The fed subgroup exhibited lower genetic diversity and higher relatedness than the rest of the subpopulation. Simulation model results indicated that a single translocation probably would not restore genetic diversity in fed individuals. Thus, feeding sites implementation and associated management practices might rapidly induce founder effects. We discuss the possibilities of conciliating ecotourism and the conservation of endangered animal species from this viewpoint.
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The appearance of tourists brings about behavioural changes in some primates. Primate behavioural responses to human activities can reflect their survival strategy. Little is known about how the behaviour of Rhinopithecus bieti changes in the presence of tourists. Here we provide the first detailed description of interactions between a provisioned group of R. bieti and tourists at Xiangguqing in Baimaxueshan Nature Reserve from July 2012 to June 2013. We found that R. bieti had different response rates to the 5 most common human actions (shout, photograph, offer food, clap, and wave). Results indicated that R. bieti expresses 10 behavioural reactions (threat, escape, vigilance, warning, panic, alliance, attack, foraging, approach, and staring) to tourists' actions. On the whole, most of the monkeys' responses were unfriendly or hostile; a small number were neutral and affiliative. Behavioural responses were also significantly different among the different age/sex classes. Immature individuals engaged in more affiliative behaviours than adult individuals, and adult males tended towards more hostile behaviours. The behaviour of R. bieti towards tourists showed both tension and adaptability. Scientific management of provisioned monkey groups and strict regulation of tourist behaviour is needed in order to protect the animals from the negative effects of tourism-related disturbance.
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Theory suggests that it may be advantageous to females to bias the sex ratio among their offspring if investment in one sex yields a higher fitness return [1]. Two specific models have been used to explain rank-related variation in the secondary sex ratios of females among gregarious non-human primates. The first, due to Trivers and Willard [2], assumes that under certain conditions in species with a polygynous mating system extra investment in males is most effective [3]. The second (the Local Resource Competition model), due to Clark [4] and extended by Silk [5], assumes that extra investment is required to produce successful daughters if females are the resident sex. Both models assume that females differ in their ability to invest and that this depends on their social position.
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In many primate species that form one-male breeding units (OMUs), the threat of a takeover by a bachelor male represents a major challenge to group stability and individual reproductive success. In the case of snub-nosed monkeys, which live in large multilevel or modular societies (MLS) comprising several OMUs that travel, feed and rest together and as well as one or more all male units (AMUs), the process by which rival males challenge resident OMU males for access to females is poorly understood. From September 2012 to October 2013, we recorded 48 cases in which rival males visited an OMU in a MLS of Yunnan snub-nosed monkeys (Rhinopithecus bieti) inhabiting the Baimaxueshan National Nature Reserve, Yunnan Province, China. In 40 cases, rival males engaged in mild agonistic interactions (approaching, staring, teeth-baring and chasing) but failed to take over the group; we counted these visits as failed takeovers, recognizing that they may nevertheless allow rival males to assess the competitive ability of residents. During eight successful takeovers, however, there was severe physical aggression between challenging and resident males, with serious injuries to participants. We found that neither the number of adult and subadult females in an OMU, the number of non-pregnant, non-lactating adult females in an OMU, nor the rank of a resident male relative to other resident males in the MLS predicted which OMU a challenging male targeted for takeover. However, a resident male's rank significantly predicted whether takeover attempts were successful. Specifically, challenging males were more successful in displacing a lower-ranking resident male than a higher-ranking male. Given that a Yunnan snub-nosed monkey MLS may contain as many as 40 resident and 36 bachelor males, continued research is required to determine the set of factors that enable resident males to maintain high social rank and successfully defend their harems. Am. J. Primatol. © 2016 Wiley Periodicals, Inc.
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Compares the seasonal timing of births in the Arashiyama Macaca fuscata population in Japan (35°00′N) during 15-yr to that of a descendant population in Texas (28°05′N) over a subsequent 15-yr period. Reproductive seasonality in this group relies primarily on an endogenous circannual clock that has become emancipated from the traditionally examined climatological cues, but which may be affected by the social environment and by other proximate cues that have yet not been identified.
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Within the Colobinae, the genera Rhinopithecus (snub-nosed monkeys), Pygathrix (douc langurs) and Nasalis (proboscis monkeys and simakobus) are informally grouped as the odd-nosed monkeys. While these genera comprise an eclectic mix featuring remarkable natural histories, this ecologically diverse group previously received little attention from the scientific community. In the last decade, however, a plethora of new and exciting research has occurred on these understudied colobines. In this book, we present a summary and synthesis of this new knowledge, looking to compare across taxa and scientific disciplines and generate in-depth discussion of what odd-nosed monkeys can tell us about the unity and diversity of the primates as a whole. This review follows the central themes of primatology and covers topics as diverse as taxonomy and phylogeny, functional morphology, spatial and dietary ecology, activity patterns, social organization, life histories and ends with an overview of the conservation status of these enthralling and endangered primates.
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The observations of Sunda pangolin reproductive parameters in this paper were based on the wild-caught animals and those that had spent time in captive environments, however, when analyzing the results, we did not consider differences in terms of breeding habits between the two. Still, this research has led to an increase in knowledge of the breeding habits of the Sunda pangolin. Our results suggest that there is no breeding season or season of parturition for the Sunda pangolin, which breeds all year round. We estimated the gestation period in this species to be around six months. Sexual maturity occurred at one year old or as early as six-seven months old in some individuals, and requires further investigation. Each Sunda pangolin in this study gave birth to one offspring at a time. The sex ratio at birth was 0.875:1 (♀:♂) (n = 15); and the weaning age was estimated at four months with a weight of 1.19 ± 0.50 kg (n = 3), which concurs with recent research. Findings in this study will contribute to future analyses of population dynamics, species conservation, and both in situ and ex situ management of the Sunda pangolin. Despite this contribution, further studies are needed on the reproductive parameters of Sunda pangolin.
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(1) Annual birth peaks in the breeding of several primate species are thought to correlate with seasonal changes in food availability, yet no study published to date has both correlated birth seasonality with food availability, and shown that the physical conditions of individuals decline during annual periods of food scarcity. (2) We document the following observations in a population of saddle-back tamarins (Saguinus fuscicollis Spix; Callitrichidae) at the Cocha Cashu Biological Station in Peru's Manu National Park. (3) The availability of both fruits and insects was substantially lower during the annual 4-month dry season (May-September) than at other times of the year. (4) Individual tamarins lost an average of 5% of their weight over this period. (5) Three-quarters of twenty-two S. fuscicollis births at this site occurred between November and February, and none occurred between mid-March and mid-August. (6) We suggest that tamarin births at Cocha Cashu are timed such that lactation and weaning occur when food is abundant, because during the period of low food availability, there would be insufficient food to meet the demands of lactation and to serve as easily obtainable weaning foods. In this sort of seasonal environment, tamarins appear to be constrained, by the seasonality of their food supply, from breeding as frequently as they do in captivity.