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Characteristics of a group of Hubei Golden Snub-nosed Monkeys (Rhinopithecus roxellana hubeiensis) before and after major snow storms.

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American Journal of Primatology 71:523–526 (2009)
BRIEF REPORT
Characteristics of a Group of Hubei Golden Snub-Nosed Monkeys
(Rhinopithecus roxellana hubeiensis) Before and After Major Snow Storms
YIMING LI1, XUECONG LIU1,2, MINGYAO LIAO3, JINGYUAN YANG3, AND CRAIG B. STANFORD2
1
Institute of Zoology, The Chinese Academy of Sciences, Chaoyang, Beijing, China
2
Departments of Anthropology and Biological Sciences, University of Southern California, Los Angeles, California
3
Management Bureau of Shennongjia Nature Reserve, Shennongjia Forestry Region, Hubei, China
Natural disasters can negatively affect primate population demography and social group structure.
A clear understanding of these effects has important implications for wildlife conservation. The worst
snow storms in nearly five decades hit portions of southern and central China between January 10 and
February 6, 2008, presenting a unique opportunity to observe their immediate effects on a previously
studied group of Hubei Golden Snub-nosed Monkeys (Rhinopithecus roxellana hubeiensis) in temperate
forests in Shennongjia Nature Reserve, Hubei Province, China. We recorded social and demographic
characteristics of the group before and after the snow storms. The average group size decreased from
270 individuals before the storms to 197 individuals after the storms, a reduction of 27.2%. Adult
females (30.1%), juveniles (38.1%) and infants (55.4%) suffered higher mortality than did adult males
(15.7%). Despite age and sex-based differences in mortality, the ratios of adult males to adult females,
adults to immatures and adult females to immatures remained similar before and after the storms.
However, higher mortality among females, juveniles and infants may reduce the group’s long-term
potential for growth. Am. J. Primatol. 71:523–526, 2009.
r 2009 Wiley-Liss, Inc.
Key words: snow storms; Rhinopithecus roxellana hubeiensis; mass mortality; group structure;
conservation
INTRODUCTION
Natural disasters can negatively affect primate
population demography and social group structure.
Several cases of mass mortality and population
decline due to disasters have been reported in
primates. For example, Hamilton [1985] reported
that 26% of chacma baboons (Papio ursinus) died or
disappeared after a 5-month drought in the Kuiseb
River canyon, Namibia. Dittus [1988] found that
a population of toque macaques (Macaca sinica)
decreased in size by 15% as a result of a severe
drought in Polonnaruwa, Sri Lanka. Pavelka et al.
[2007] noted that a population of black howlers
(Alouatta pigra) declined by 88% during the 3.5 years
after Hurricane Iris hit the Monkey River watershed
in southern Belize. Natural disasters can change
group structure and mating opportunities by reducing the ratio of adult males to adult females, and
reduce opportunities for population growth if adult
females or immatures experience high rates of
mortality or periods of subfertility [Pavelka et al.,
2007]. Natural disasters also can affect vegetation
structure, food supply, diet and activity [Behie &
Pavelka, 2005], resulting in fissioning of established
social groups [Dittus, 1988]. A clear understanding of
these effects has important implications for wildlife
conservation strategies [Pavelka et al., 2007].
r 2009 Wiley-Liss, Inc.
Sichuan snub-nosed monkeys (Rhinopithecus
roxellana) occur in highly seasonal temperate-mixed
forests in mountainous regions of the Chinese
provinces of Hubei, Shaanxi, Gansu and Sichuan
[Wang et al., 1998], where snow cover lasts for 4
months of the year. This species experiences the
longest winters and lowest average temperatures
(about 141C) of any non-human primate in the
world [Happel & Cheek, 1986]. The monkeys live in
large groups, composed of a number of one-male units
[Ren et al., 2000], and mating usually occurs between
August and October, producing infants from March to
June. Their main food source is lichen [Li, 2006],
which makes up 90% of their feeding time during the
winter. Other items in the diet include leaves, fruits
and seeds, flowers, buds, bark and herbs. R. roxellana
Contract grant sponsor: ‘‘973’’ program; Contract grant number:
2007CB411600; Contract grant sponsor: National Science Foundation; Contract grant number: 30670354.
Correspondence to: Yiming Li, Institute of Zoology, The
Chinese Academy of Sciences, Datun Road, Chaoyang, Beijing
100101, China. E-mail: liym@ioz.ac.cn
Received 22 August 2008; revised 4 February 2009; revision
accepted 4 February 2009
DOI 10.1002/ajp.20674
Published online 5 March 2009 in Wiley InterScience (www.
interscience.wiley.com).
524 / Li et al.
is classified into three subspecies: the Moupin Golden
Snub-nosed Monkey (R. roxellana roxellana), the
Hubei Golden Snub-nosed Monkey (R. roxellana
hubeiensis), and the Qinling Golden Snub-nosed
Monkey (R. roxellana qinlingensis) [Groves, 2001;
Wang et al., 1998]. R. roxellana hubeiensis is found in
Shennongjia Nature Reserve and in other areas in
Hubei Province. This is the most endangered of the
three subspecies, with only about 1,000 monkeys left
in the wild [Wang et al., 1998].
The worst snow storms in the last five decades hit
large portions of southern and central China between
January 10 and February 6, 2008 [Stone, 2008], presenting a unique opportunity to observe their immediate effects on a previously studied group of Hubei
Golden Snub-nosed Monkeys in Shennongjia Nature
Reserve. In this study, we investigated the effects of
these storms on the group. Our aims were (1) to
compare the group size and its social structure before
and after the storms and (2) to determine the number
and demographic distribution of monkey deaths.
METHODS
20–30 m of the group, and observed it every day from
November 2007 to January 24, 2008 before the
storms, and from March 26 to the end of April after
the storms. The deciduous trees were leafless during
these periods when the monkeys were censused. We
(Li and two field assistants) censused the group in
areas where there were no coniferous trees, while it
rested at midday, so the animals could be clearly
seen. We divided the area occupied by the group
into two or three parts. To avoid counting the
same individual twice, each researcher censused the
monkeys in one part. We counted every member of
the group that we could see with the naked eye or
using binoculars. We censused the group four times
(November 11, November 22, December 14, 2007, and
January 1, 2008) before the storms and four times
after the storms (April 20, April 24, April 27 and April
28, 2008). We calculated the average group size before
and after the storms. We classified each individual
according to age and sex as either adult female, adult
male, juvenile or infant [Li, 2007]. When a dead
monkey was encountered, we recorded information on
its age and sex, and the location, elevation, type of
forest and habitat where it was found.
Study Area
This study was conducted in the Qianjiaping
area of Shennongjia Nature Reserve (311220 –311370 N
and 1101030 –1101340 E), Hubei Province [for detailed
information, see Li, 2006, 2007]. The area has a
rugged topography with an elevational range of
1,500–2,600 m. The vegetation comprises temperate
deciduous broadleaf coniferous forest, which is a
mosaic of primary forest, young forest (secondary
forest), shrub forest and grassland. At an elevation of
1,700 m, the average temperature is 17.81C in July
and –2.751C in January. The annual precipitation is
approximately 1,800 mm. Winter and spring snow
storms occur approximately every 3 years. According
to Dalongtan Weather Station, located at 2,170 m
in the reserve, the snowfall during the storms of
January 2008 was 30% higher, the average daily
temperature was 21C lower, and the number of days
when it snowed and was misty doubled, compared
with other years. The trees remained covered with
snow and rime throughout the storms (28 days).
Data Collection
The behavioral ecology of a group of R. roxellana
hubeiensis in the Qianjiaping area has been studied
since 1999 [Li, 2006, 2007]. The semi-habituated
group had been observed for a total of 43 months
before this study, including 7 months in spring,
14 months in summer, 14 months in autumn and
8 months in winter. We were able to identify some
monkeys based on anatomical features, such as lost
ears or permanent scars or spots, allowing us to
ensure that we observed the same group before and
after the storms. We were able to approach to within
Am. J. Primatol.
Data Analysis
We compared differences in group size, the
number of monkeys in each age/sex class, the ratios
of adult males to adult females, adults to immatures,
and adult females to immatures before and after the
storms, using the Wilcoxon signed rank test. We
analyzed differences in mortality among age/sex
classes using the w2 test.
The research conducted in this article adhered
to the legal requirements of China, where the
research was conducted. Permission was obtained
from the Management Bureau of Shennongjia
Nature Reserve.
RESULTS
The average group size of the monkeys before the
storms was 270713 individuals (Table I). After the
storms, the group size was 203712 individuals. This
number included six infants born in April. The group
size therefore decreased from 270 individuals before the
storms to 197 individuals after the storms (Wilcoxon
signed rank test, z 5 2.521, n 5 4, P 5 0.012), a reduction of 27.2%. The number of monkeys in each of the
age/sex classes was reduced (z 5 2.521, P 5 0.012 for
each age/sex class). The mortality of adult males was
15.7%, adult females 30.1%, juveniles 38.1% and infants
55.4%. The mortality of females, juveniles and infants
was higher than that of adult males (w2 5 5.819,
df 5 1, P 5 0.016 for females; w2 5 9.731, P 5 0.002 for
juveniles; w2 5 16.214, Po0.001 for infants). Furthermore, the mortality of infants was higher than that of
adult females (w2 5 4.807, P 5 0.028).
The Effects of Snow Storms on Hubei Golden Snub-Nosed Monkeys / 525
TABLE I. Changes in Group Demography and Group Size in Rhinopithecus roxellana hubeiensis in the
Shennongjia Nature Reserve Before and after Major Snowstorms
Characteristics
Group size (individuals)
Adult males (individuals)
Adult females (individuals)
Juveniles (individuals)
Infants (individuals)
Sex ratio (AM:AF)
Age ratio (adult:immature)
Age ratio (adult female:immature)
Before snow storms
After snow storms
Change (average %)
270712.5
114.878.9
90.8713.6
43.375.9
21.374.8
1:0.79
1:0.31
1:0.71
196.5712.2
96.878.1
63.579.5
26.874.9
9.572.4
1:0.66
1:0.23
1:0.57
27.2
15.7
30.1
38.1
55.4
7.8
6.5
8.9
The ratios of adult males to adult females, adults
to immatures and adult females to immatures varied
before and after the storms (Table I), but these
differences were not significant (Wilcoxon signed
rank test, z 5 1.416, n 5 4, P 5 0.144 for adult males
to adult females and adults to immatures; z 5 1.059,
P 5 0.273 for adult females to immatures).
No monkey deaths were noted between November
2007 and January 2008, but by the end of April 2008,
12 dead monkeys had been found in the region. The
causes and time of death for these individuals could
not be identified. Seven of the dead monkeys were
adults and five were juveniles. Only two (one adult
male and one juvenile female) could be sexed, as
the other carcasses had been dismembered by the time
we encountered them. All of the dead monkeys were
found in young forest, shrub forest and grassland
between elevations of 1,748 and 2,129 m.
Only four dead monkeys had been found in the
region during the previous 8-year study period
(1999–2007), during which we used a similar sampling
regime to observe the monkeys. One dead monkey
was found in summer 1999, one in December 2001
(killed by falling from an icy slope), and two in
December 2002 (one killed by a predator).
DISCUSSION
This study reports the first evidence of mass
mortality in R. roxellana hubeiensis because of the
worst storms to hit this region of China in five
decades. Frequent and heavy snows and rime ice,
along with extremely low temperatures, may have
been responsible for the mass deaths of the monkeys.
The snow and rime covered most of the monkeys’ food
resources (lichens, buds and bark) during the storms,
reducing food availability and increasing the cost of
foraging. Thus, some monkeys may have died because
they were malnourished and unable to produce
enough heat to endure the low temperatures.
Infant and juvenile mortality are reported to be
markedly higher than those of adults during times of
environmental stress, such as droughts, cyclones and
hurricanes [Dittus, 1988; Gould et al., 1999; Hamilton,
1985; Pavelka et al., 2007]. Weaned infants and young
juveniles may not be able to keep up with the group if
they are weakened by malnourishment, and thus may
become relatively easy targets for predators [Janson &
van Schaik, 1993].
In a study on Lemur catta, Gould et al. [1999]
reported that the mortality (20.8%) of females during
a 2-year drought was related to reproductive state.
They found that the majority of females were
lactating at the time of death. Hamilton [1985]
suggested that adult male chacma baboon (P. ursinus)
were better able to survive food shortages than adult
females during a 5-month drought, because they were
able to outcompete the females for access to limited
food resources. Reproductive state and competitive
ability may both have contributed to the higher
female mortality in the Qianjiaping area. During
the storms, some females were pregnant or nursing
infants, which might have made them more vulnerable to the snow storms. For example, before the
storms 21 females in the group were nursing infants
and after the storm only 10 females were nursing
infants. Moreover in general, adult males spend more
time searching for food than other age/sex classes
[2007], and this may have been an advantage to them
during this period of food scarcity.
Although the size of this group had increased
between 1999 (109 individuals) and 2007, the snow
storms resulted in an immediate reduction in group
size. In addition, greater storm-related mortality in
adult females, juveniles and infants reduced the
group’s potential for growth. Mass mortality of
monkeys because of this series of storms also was
reported in other groups in the reserve (unpublished
data). These observations suggest that snow storms
may be a threat to the small population of R. roxellana
hubeiensis. Six new infants were born in April, after
the storms, indicating that not all pregnant females
were severely affected. The snow storms led to
extensive forest damage in southern and central
China, including Hubei Province [Stone, 2008]. This
may have modified vegetation structure and affect
food availability for the monkeys over the next several
years. Further research is needed to determine the
long-term effects of snow storms on Hubei Golden
Snub-nosed monkeys.
Am. J. Primatol.
526 / Li et al.
ACKNOWLEDGMENTS
The research conducted in this paper adhered to
the legal requirements of China, where the research
was conducted. Permission was obtained from
the Management Bureau of Shennongjia Nature
Reserve.
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