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

1Institute of Zoology, The Chinese Academy of Sciences, Chaoyang, Beijing, China2Departments of Anthropology and Biological Sciences, University of Southern California, Los Angeles, California3Management 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 worstsnow storms in nearly five decades hit portions of southern and central China between January 10 andFebruary 6, 2008, presenting a unique opportunity to observe their immediate effects on a previouslystudied group of Hubei Golden Snub-nosed Monkeys (Rhinopithecus roxellana hubeiensis) in temperateforests in Shennongjia Nature Reserve, Hubei Province, China. We recorded social and demographiccharacteristics of the group before and after the snow storms. The average group size decreased from270 individuals before the storms to 197 individuals after the storms, a reduction of 27.2%. Adultfemales (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-termpotential 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 primatepopulation demography and social group structure.Several cases of mass mortality and populationdecline due to disasters have been reported inprimates. For example, Hamilton [1985] reportedthat 26% of chacma baboons (Papio ursinus) died ordisappeared after a 5-month drought in the KuisebRiver canyon, Namibia. Dittus [1988] found thata population of toque macaques (Macaca sinica)decreased in size by 15% as a result of a severedrought in Polonnaruwa, Sri Lanka. Pavelka et al.[2007] noted that a population of black howlers(Alouatta pigra) declined by 88% during the 3.5 yearsafter Hurricane Iris hit the Monkey River watershedin southern Belize. Natural disasters can changegroup structure and mating opportunities by reduc-ing the ratio of adult males to adult females, andreduce opportunities for population growth if adultfemales or immatures experience high rates ofmortality or periods of subfertility [Pavelka et al.,2007]. Natural disasters also can affect vegetationstructure, food supply, diet and activity [Behie &Pavelka, 2005], resulting in fissioning of establishedsocial groups [Dittus, 1988]. A clear understanding ofthese effects has important implications for wildlifeconservation strategies [Pavelka et al., 2007].

Sichuan snub-nosed monkeys (Rhinopithecusroxellana) occur in highly seasonal temperate-mixedforests in mountainous regions of the Chineseprovinces of Hubei, Shaanxi, Gansu and Sichuan[Wang et al., 1998], where snow cover lasts for 4months of the year. This species experiences thelongest winters and lowest average temperatures(about �141C) of any non-human primate in theworld [Happel & Cheek, 1986]. The monkeys live inlarge groups, composed of a number of one-male units[Ren et al., 2000], and mating usually occurs betweenAugust and October, producing infants from March toJune. Their main food source is lichen [Li, 2006],which makes up 90% of their feeding time during thewinter. Other items in the diet include leaves, fruitsand seeds, flowers, buds, bark and herbs. R. roxellana

Published online 5 March 2009 in Wiley InterScience (www.interscience.wiley.com).

DOI 10.1002/ajp.20674

Received 22 August 2008; revised 4 February 2009; revisionaccepted 4 February 2009

Contract grant sponsor: ‘‘973’’ program; Contract grant number:2007CB411600; Contract grant sponsor: National Science Foun-dation; Contract grant number: 30670354.

�Correspondence to: Yiming Li, Institute of Zoology, TheChinese Academy of Sciences, Datun Road, Chaoyang, Beijing100101, China. E-mail: liym@ioz.ac.cn

rr 2009 Wiley-Liss, Inc.

is classified into three subspecies: the Moupin GoldenSnub-nosed Monkey (R. roxellana roxellana), theHubei Golden Snub-nosed Monkey (R. roxellanahubeiensis), and the Qinling Golden Snub-nosedMonkey (R. roxellana qinlingensis) [Groves, 2001;Wang et al., 1998]. R. roxellana hubeiensis is found inShennongjia Nature Reserve and in other areas inHubei Province. This is the most endangered of thethree subspecies, with only about 1,000 monkeys leftin the wild [Wang et al., 1998].

The worst snow storms in the last five decades hitlarge portions of southern and central China betweenJanuary 10 and February 6, 2008 [Stone, 2008], pre-senting a unique opportunity to observe their imme-diate effects on a previously studied group of HubeiGolden Snub-nosed Monkeys in Shennongjia NatureReserve. In this study, we investigated the effects ofthese storms on the group. Our aims were (1) tocompare the group size and its social structure beforeand after the storms and (2) to determine the numberand demographic distribution of monkey deaths.

METHODS

Study Area

This study was conducted in the Qianjiapingarea of Shennongjia Nature Reserve (311220–311370Nand 1101030–1101340E), Hubei Province [for detailedinformation, see Li, 2006, 2007]. The area has arugged topography with an elevational range of1,500–2,600 m. The vegetation comprises temperatedeciduous broadleaf coniferous forest, which is amosaic of primary forest, young forest (secondaryforest), shrub forest and grassland. At an elevation of1,700 m, the average temperature is 17.81C in Julyand –2.751C in January. The annual precipitation isapproximately 1,800 mm. Winter and spring snowstorms occur approximately every 3 years. Accordingto Dalongtan Weather Station, located at 2,170 min the reserve, the snowfall during the storms ofJanuary 2008 was 30% higher, the average dailytemperature was 21C lower, and the number of dayswhen it snowed and was misty doubled, comparedwith other years. The trees remained covered withsnow and rime throughout the storms (28 days).

Data Collection

The behavioral ecology of a group of R. roxellanahubeiensis in the Qianjiaping area has been studiedsince 1999 [Li, 2006, 2007]. The semi-habituatedgroup had been observed for a total of 43 monthsbefore this study, including 7 months in spring,14 months in summer, 14 months in autumn and8 months in winter. We were able to identify somemonkeys based on anatomical features, such as lostears or permanent scars or spots, allowing us toensure that we observed the same group before andafter the storms. We were able to approach to within

20–30 m of the group, and observed it every day fromNovember 2007 to January 24, 2008 before thestorms, and from March 26 to the end of April afterthe storms. The deciduous trees were leafless duringthese periods when the monkeys were censused. We(Li and two field assistants) censused the group inareas where there were no coniferous trees, while itrested at midday, so the animals could be clearlyseen. We divided the area occupied by the groupinto two or three parts. To avoid counting thesame individual twice, each researcher censused themonkeys in one part. We counted every member ofthe group that we could see with the naked eye orusing binoculars. We censused the group four times(November 11, November 22, December 14, 2007, andJanuary 1, 2008) before the storms and four timesafter the storms (April 20, April 24, April 27 and April28, 2008). We calculated the average group size beforeand after the storms. We classified each individualaccording to age and sex as either adult female, adultmale, juvenile or infant [Li, 2007]. When a deadmonkey was encountered, we recorded information onits age and sex, and the location, elevation, type offorest and habitat where it was found.

Data Analysis

We compared differences in group size, thenumber of monkeys in each age/sex class, the ratiosof adult males to adult females, adults to immatures,and adult females to immatures before and after thestorms, using the Wilcoxon signed rank test. Weanalyzed differences in mortality among age/sexclasses using the w2 test.

The research conducted in this article adheredto the legal requirements of China, where theresearch was conducted. Permission was obtainedfrom the Management Bureau of ShennongjiaNature Reserve.

RESULTS

The average group size of the monkeys before thestorms was 270713 individuals (Table I). After thestorms, the group size was 203712 individuals. Thisnumber included six infants born in April. The groupsize therefore decreased from 270 individuals before thestorms to 197 individuals after the storms (Wilcoxonsigned rank test, z 5 2.521, n 5 4, P 5 0.012), a reduc-tion of 27.2%. The number of monkeys in each of theage/sex classes was reduced (z 5 2.521, P 5 0.012 foreach age/sex class). The mortality of adult males was15.7%, adult females 30.1%, juveniles 38.1% and infants55.4%. The mortality of females, juveniles and infantswas 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 forjuveniles; w2 5 16.214, Po0.001 for infants). Further-more, the mortality of infants was higher than that ofadult females (w2 5 4.807, P 5 0.028).

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The ratios of adult males to adult females, adultsto immatures and adult females to immatures variedbefore and after the storms (Table I), but thesedifferences were not significant (Wilcoxon signedrank test, z 5 1.416, n 5 4, P 5 0.144 for adult malesto 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 November2007 and January 2008, but by the end of April 2008,12 dead monkeys had been found in the region. Thecauses and time of death for these individuals couldnot be identified. Seven of the dead monkeys wereadults and five were juveniles. Only two (one adultmale and one juvenile female) could be sexed, asthe other carcasses had been dismembered by the timewe encountered them. All of the dead monkeys werefound in young forest, shrub forest and grasslandbetween elevations of 1,748 and 2,129 m.

Only four dead monkeys had been found in theregion during the previous 8-year study period(1999–2007), during which we used a similar samplingregime to observe the monkeys. One dead monkeywas found in summer 1999, one in December 2001(killed by falling from an icy slope), and two inDecember 2002 (one killed by a predator).

DISCUSSION

This study reports the first evidence of massmortality in R. roxellana hubeiensis because of theworst storms to hit this region of China in fivedecades. Frequent and heavy snows and rime ice,along with extremely low temperatures, may havebeen responsible for the mass deaths of the monkeys.The snow and rime covered most of the monkeys’ foodresources (lichens, buds and bark) during the storms,reducing food availability and increasing the cost offoraging. Thus, some monkeys may have died becausethey were malnourished and unable to produceenough heat to endure the low temperatures.

Infant and juvenile mortality are reported to bemarkedly higher than those of adults during times ofenvironmental stress, such as droughts, cyclones andhurricanes [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 ifthey are weakened by malnourishment, and thus maybecome 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 duringa 2-year drought was related to reproductive state.They found that the majority of females werelactating at the time of death. Hamilton [1985]suggested that adult male chacma baboon (P. ursinus)were better able to survive food shortages than adultfemales during a 5-month drought, because they wereable to outcompete the females for access to limitedfood resources. Reproductive state and competitiveability may both have contributed to the higherfemale mortality in the Qianjiaping area. Duringthe storms, some females were pregnant or nursinginfants, which might have made them more vulner-able to the snow storms. For example, before thestorms 21 females in the group were nursing infantsand after the storm only 10 females were nursinginfants. Moreover in general, adult males spend moretime searching for food than other age/sex classes[2007], and this may have been an advantage to themduring this period of food scarcity.

Although the size of this group had increasedbetween 1999 (109 individuals) and 2007, the snowstorms resulted in an immediate reduction in groupsize. In addition, greater storm-related mortality inadult females, juveniles and infants reduced thegroup’s potential for growth. Mass mortality ofmonkeys because of this series of storms also wasreported in other groups in the reserve (unpublisheddata). These observations suggest that snow stormsmay be a threat to the small population of R. roxellanahubeiensis. Six new infants were born in April, afterthe storms, indicating that not all pregnant femaleswere severely affected. The snow storms led toextensive forest damage in southern and centralChina, including Hubei Province [Stone, 2008]. Thismay have modified vegetation structure and affectfood availability for the monkeys over the next severalyears. Further research is needed to determine thelong-term effects of snow storms on Hubei GoldenSnub-nosed monkeys.

TABLE I. Changes in Group Demography and Group Size in Rhinopithecus roxellana hubeiensis in theShennongjia Nature Reserve Before and after Major Snowstorms

Characteristics Before snow storms After snow storms Change (average %)

Group size (individuals) 270712.5 196.5712.2 �27.2Adult males (individuals) 114.878.9 96.878.1 �15.7Adult females (individuals) 90.8713.6 63.579.5 �30.1Juveniles (individuals) 43.375.9 26.874.9 �38.1Infants (individuals) 21.374.8 9.572.4 �55.4Sex ratio (AM:AF) 1:0.79 1:0.66 7.8Age ratio (adult:immature) 1:0.31 1:0.23 6.5Age ratio (adult female:immature) 1:0.71 1:0.57 8.9

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ACKNOWLEDGMENTS

The research conducted in this paper adhered tothe legal requirements of China, where the researchwas conducted. Permission was obtained fromthe Management Bureau of Shennongjia NatureReserve.

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