Characteristics of a group of Hubei Golden Snub-nosed Monkeys (Rhinopithecus roxellana hubeiensis) before and after major snow storms.код для вставкиСкачать
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  reported that 26% of chacma baboons (Papio ursinus) died or disappeared after a 5-month drought in the Kuiseb River canyon, Namibia. Dittus  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.  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: email@example.com 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.  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  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 , 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. REFERENCES Behie AM, Pavelka MSM. 2005. The short-term effects of a hurricane on the diet and activity of black howlers (Alouatta pigra) in Monkey River Belize. Folia Primatol 76:1–9. Dittus WPJ. 1988. Group fission among wild toque macaques as a consequence of female resource competition and environmental stress. Anim Behav 36:1626–1645. Gould L, Sussman RW, Sauther ML. 1999. 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