Influence of human activities on the historical and current distribution of Sichuan snub-nosed monkeys in the Qinling Mountains, China.

Original Article Received: April 11, 2014 Accepted after revision: September 16, 2014 Published online: January 21, 2015

Folia Primatol 2014;85:343–357 DOI: 10.1159/000368398

Influence of Human Activities on the Historical and Current Distribution of Sichuan Snub-Nosed Monkeys in the Qinling Mountains, China Chengliang Wang a Xiaowei Wang a Xiaoguang Qi b Songtao Guo b Haitao Zhao a Wei Wei b Baoguo Li a, b

a

Shaanxi Institute of Zoology, and b College of Life Sciences, Northwest University, Xi’an, China

Key Words Rhinopithecus roxellana · Distribution changes · Human activities · Conservation · Qinling Mountains

Abstract Due to their rich animal diversity and the presence of rare and endemic species, the Qinling Mountains are listed as a significant global biodiversity area. The Sichuan snubnosed monkey (Rhinopithecus roxellana) has been distributed in this area since the Middle Pleistocene. Due to the gradual encroachment of humans into their habitat, both the distribution range and population sizes of R. roxellana have significantly decreased. Based on literature research as well as field and questionnaires, we investigated the influence of human activities on R. roxellana distribution in the Qinling Mountains. Human activity within the habitat of R. roxellana began in the Stone and Bronze Ages, though initially it had no significant influence on its populations. When China entered the Iron Age, however, different historical and social periods had a considerable impact on R. roxellana distribution. Although national and provincial level governments introduced strict protection policies with the establishment of the People’s Republic of China in 1949, human activities continued to influence R. roxellana distribution. Since the launch of the Natural Forest Protection Project across the Qinling Mountains in 1999, the quality of R. roxellana habitat has shown marked improvement. This research will help promote the survival and conservation of the Sichuan snub-nosed monkey in the Qinling Mountains. © 2015 S. Karger AG, Basel

© 2015 S. Karger AG, Basel 0015–5713/15/0856–0343$39.50/0 E-Mail [email protected] www.karger.com/fpr

Baoguo Li College of Life Sciences Northwest University North Taibai Road No. 229 Xi’an, Shaanxi Province 710069 (China) E-Mail baoguoli @ nwu.edu.cn

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Xiaowei Wang Shaanxi Institute of Zoology Xingqing Road, No. 88 Xi’an, Shaanxi Province 710032 (China) E-Mail [email protected]

Introduction

The Qinling Mountains are an important east-west mountain range in the centre of China, running across Gansu, Shaanxi, He’nan and Hubei provinces. The average altitude is 2000 m above sea level, and the highest peak is Taibai Mountain at 3,767.12 m [Xie, 2012]. The Qinling Mountains are not only the watershed between the Yangtze and Yellow rivers, but are also the climatic boundary between subtropical and temperate regions. This mountain range forms the convergence zone of the Palaearctic and Oriental realms as well as the convergence zone of the Huabei, Meng’xin, Qing’zang, Huazhong and Xi’nan fauna [Tian et al., 2003]. Many northern and southern animal species are found in the Qinling Mountains, including relic fauna such as the Sichuan snub-nosed monkey (Rhinopithecus roxellana) and the giant panda (Ailuropoda melanoleuca). Due to its rich animal diversity and the presence of rare and endemic species, the Qinling Mountains have been listed as a significant global biodiversity area and have been the focus of many studies on endangered animal conservation, e.g. the crested ibis (Nipponia nippon) [Li et al., 1996], giant panda (A. melanoleuca) [Feng et al., 2006], golden takin (Budorcas taxicolor) [Zeng et al., 2002] or the Sichuan snub-nosed monkey (R. roxellana) [Guo et al., 2008]. Chinese snub-nosed monkeys are all placed in the genus Rhinopithecus and are distributed in very limited areas within China [Napier and Napier, 1967]. Four Rhinopithecus species are endemic to China, including the Sichuan or Golden (R. roxellana), Yunnan or Black (R. bieti), Guizhou or Grey (R. brelichi) and newly found Myanmar or Burmese (R. strykeri) snub-nosed monkeys [Geissmann et al., 2010]. Though limited to isolated regions, they form a graded geographical array from R. brelichi in subtropical evergreen and deciduous broad-leaf forests at less than 1,000 m elevation to R. bieti in temperate, coniferous forests at elevations as high as 3,000– 4,500 m, where annual average temperatures hover near freezing [Pan and Yong, 1989; Boonratana and Le, 1998]. R. roxellana falls within the geographical gradation between R. brelichi and R. bieti, inhabiting temperate forests in mountainous highlands that range from 1,400 to 3,300 m in elevation [Li et al., 2002; Qi et al., 2009]. Extant populations occur in 3 isolated areas in Sichuan, Shaanxi, Gansu and Hubei provinces. The Sichuan populations are distributed in the Qionglaishan, Mingshan, Daxianling and Xiaoxianling Mountain ranges; the Hubei populations are distributed in the Shennongjia Mountain range, and the Qinling populations are distributed in the Qinling Mountains in Shaanxi and Gansu [Chen et al., 1989; Hu et al., 1989; Li et al., 2000]. Due to their geographical isolation, the Qinling populations possess unique characteristics. These populations not only occupy the northernmost range (33°53′ N) of all snub-nosed monkey species [Li et al., 2002; Qi et al., 2009], but the contraction of their habitat appears to be synchronized with the expansion of human activity. Thus, studies on the influence of human activity on R. roxellana distribution in the Qinling Mountains can help establish a scientific strategy to ensure its survival and conservation. R. roxellana has lived in the Qinling Mountains since the Middle Pleistocene [Pan and Jablonski, 1987; Jablonski and Pan, 1988; Jablonski, 1993], at which time its populations prospered. With the arrival of people, however, competition for forest resources between humans and R. roxellana began, and this remains a significant influence on R. roxellana survival today. Despite this, detailed research on the influence of human activity on the distribution of R. roxellana during Chinese human history


Wang /Wang /Qi /Guo /Zhao /Wei /Li


344

Table 1. Sichuan snub-nosed monkey historical records in the Qinling Mountains Province

City

Fossil location

Geographic distribution location historical distribution

Shaanxi

Xi’an Baoji

Xixiang, Foping, Lueyang, Liuba, Zhenba, Chenggu, Nanzheng, Yangxian, Ningqiang, Mianxian Ankang, Ziyang, Langao, Xunyang, Zhenping, Pingli, Shiquan, Hanyin

Ankang

Gansu

current distribution

Lantian Chanan, Huxian, Zhouzhi, Early Pleistocene Ningshan, Foping (109°15′ E, 33°55′ N) Baoji, Qishan, Fengxiang, Longxian, Linyou, Fufeng, Qianyang, Meixian

Hanzhong

Tianshui Dingxi

Tianshui, Gangu, Qingshui, Qin’an, Lixian, Liangdang, Huixian Minxian, Dangchang

Longnan Gannan

Wudu, Chengxian, Kangxian, Wenxian, Zhouqu

Hubei

Shiyan

Quyuan river, Fangxian, Zhushan Yunxian Early Pleistocene (111°15′ E, 31°55′ N)

He’nan

Luoyang

Badu Mt., Xi’nan Early Pleistocene (112°05′ E, 34°30′ N)

Reference

Zhouzhi Taibai

Yangxian, Foping Ningshan

Kangxian, Wudu, Wenxian Fangxian

Xi’an governmental record, 1779 Shanglinfu, 130 BC Zhouzhi country record, 1925 Fengxiang governmental record, 1521 Qishan country record, 1591 Ming Dynasty record, 1418 Hanzhong governmental record, 1544 Hanzhong governmental record, 1656 Fengxiang governmental record, 1710 Lueyang country record, 1552 Xixiang country record, 1828 Hannan governmental record, 1814 Xing’an state record, 1695 Xunyang country record, 1731 Xing’an state record, 1788 Qinzhou state record, 1764 Fuqiang country record, 1775 Minzhou state record, 1720 Ganshu governmental record, 1908 Ganshu governmental record, 1736 Wujiebei record, 1808 New Kangxian record, 1936 Wenxian country Digest, 1947 Zhushan county record, 1865 Hubei governmental record, 1921

in the Qinling Mountains has not yet been conducted. Understanding the events associated with current distribution, especially the relationships between R. roxellana, its natural environments and human activities, is important for its continued survival and conservation. Accordingly, we investigated historical records on R. roxellana distribution during Chinese human history in the Qinling Mountains to clarify why populations have diminished so markedly and to analyse the relationships between the reduction and the factors that caused it. Methods We conducted extensive literature and historical record research from libraries and official government archives concerning the fauna and flora of Gansu, Shaanxi, Hubei and He’nan provinces in China. In addition to social, political and environmental changes, we investigated the fauna and flora at specific times and regions in documents maintained and archived by local and state governments (table 1). We also carried out field surveys in Gansu, Shaanxi, Hubei and He’nan covering both historical and current distribution areas of R. roxellana populations in the Qinling Mountains. We confirmed whether monkeys were still found in these areas and explored the factors that affected their survival or extinction.


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Distribution Changes of R. roxellana

Fig. 1. Historical distribution changes in R. roxellana populations in the Qinling Mountains from

the Pleistocene to 2013. Fossil locations were obtained from Gu and Jablonski [1989], Gu and Hu [1991] and Pan [1995]. Historical records were obtained from libraries and official government archives.

We also conducted surveys within the Qinling Mountains, interviewing local farmers, government officers and forestry workers who have lived or worked long within R. roxellana habitat areas. The overall aim of this research was to clarify the historical distribution of R. roxellana and how it has been impacted by human activities.

Results

Comprehensive research (table 1) evidence from fossil records in Liantian county (109°15′ E, 33°55′ N) in Shaanxi, Yunxian county (111°15′ E, 31°55′ N) in Hubei, and Xin’an county (112°05′ E, 34°30′ N) in He’nan revealed that Rhinopithecus has lived in the Qinling Mountains since the Early Pleistocene and was distributed widely across the whole range. Some 2,000 years ago, however, humans began to gradually develop and utilize the natural resources of the Qinling Mountains, resulting in a remarkable reduction in R. roxellana populations, firstly in He’nan and Hubei, and, by the late eighteenth century, from their habitats in Gansu and Shaanxi (fig. 1). The disappearance of R. roxellana populations across He’nan, Hubei, Gansu and Shaanxi was not only a reduction in area, but also in altitudinal distribution (fig. 2). Initial disappearance began in low coteau and hilly land in the eastern Qinling Mountains in He’nan and Hubei at altitudes of less than 1,200 m, followed by the high mountains in western Gansu at altitudes of more than 3,000 m. Finally, distribution became restricted to mountains in the middle Qinling Mountains’ range in Shaanxi at altitudes between 1,200 and 3,500 m.




346

3,000

Altitude (m)

2,500

2,000

Population mainly vanished secondly Wenxian Wudu Kangxian Taibai

Ningshan Zhouzhi Foping Fangxian Meixian Yangxian

1,500

1,000

Extant populations in the Qinling Mountains

500

Population mainly vanished first

Distribution location

Fig. 2. Average altitude distribution changes in the Qinling Mountains where R. roxellana occurred during Chinese human history.

Results from our field surveys also indicated significant changes in the distribution boundaries of R. roxellana (fig. 1). Historically (table 1) the highest northern boundary latitude (east to west) was Xi’an (108°54′ E, 34°12′ N), Linyou (107°48′ E, 34°36′ N), Qianyang (107°6′ E, 34°36′ N), Longxian (106°48′ E, 34°54′ N), Qingshui (106°6′ E, 34°42′ N), Qin’an (105°36′ E, 34°48′ N), Gangu (105°18′ E, 34°42′ N), Wushan (104°48′ E, 34°42′ N) and Minxian (104° E, 34°24′ N). Currently, however, the highest latitude boundary (east to west, isolated habitat in Shaanxi and Gansu) is Zhouzhi (107°12′ E, 34°6′ N) and Taibai (107°18′ E, 34°24′ N) in Shaanxi, and Kangxian (105°30′ E, 33°24′ E) and Wudu (104°54′ E, 33°24′ N) in Gansu. Comparison between the historical and current northernmost boundary for R. roxellana in the Qinling Mountains shows that its distribution in Shaanxi has extended southwards by 48′ from Longxian to Taibai, while in Gansu, its distribution has extended southwards by 1°24′ from Wudu to Qin’an, 1°18′ from Wushan to Wudu, and 1°24′ from Qin’an to Kangxian. Overall, the northern distribution boundaries have shown obvious movement southwards. Historically, the eastern distribution boundary of R. roxellana was Xin’an (112°8′ E, 34°43′ N) in He’nan and Yunxian (110°48′ E, 32°50′ N) and Yunxixian (110°24′ E, 32°59′ N) in Hubei. Currently, the eastern distribution boundary is Fangxian (110°42′ E, 32° N), Shennongjia (110°36′ E, 31°42′ N), Xingshan (110°42′ E, 31°12′ N) and Badong (110°18′ E, 31° N) in Hubei, with populations now extinct in He’nan. Comparison between the historical and current easternmost boundary for




R. roxellana in the Qinling Mountains shows that its distribution has retreated westwards from 6′ to 1°26′ in the eastern part of the Qinling Mountains (fig. 1). Thus, the eastern distribution boundaries of R. roxellana have shown significant movement westwards. Results from our questionnaires showed that the distribution of R. roxellana changed from large areas of continuous habitat to small, separate, patchy areas of habitat. From historical records, the distribution area previously consisted of large and contiguous habitat across the middle of Shaanxi to the south-eastern areas of Gansu. Firstly, the populations in western Gansu and eastern Shaanxi decreased. Secondly, R. roxellana habitat became fragmented due to human activities. Thirdly, populations located in western Gansu and eastern Shaanxi became locally extinct. Finally, the once large habitat in Shaanxi and Gansu split into smaller, narrower areas, forming 2 isolated island habitats. Discussion

Current extant R. roxellana populations occur in only 3 isolated regions in China. Because the Sichuan and Shennongjia populations are found outside the Qinling Mountains’ range, they were excluded from this study. In the Qinling Mountains, the main R. roxellana habitat areas are located upstream of the Weihe, Jialingjiang and Hanshui rivers. This district is the most northern R. roxellana distribution and formed a large area of contiguous distribution. Fossil and literature records indicate that R. roxellana populations were once distributed in 46 locations, 30 of which were found in Shaanxi and 16 in Gansu [Quan and Xie, 2002]. At present, this district is divided into 2 isolated areas, with R. roxellana populations distributed in 8 locations, 5 of which are located in Shaanxi and 3 in Gansu [Quan and Xie, 2002]. Comparison between historical and current R. roxellana distribution in the Qinling Mountains shows that 83% of distribution locations have disappeared, with 54% disappearing in Shaanxi and 29% in Gansu (table 1; fig. 1). Presently, the number of R. roxellana individuals in the Qinling Mountains is approximately 4,000–5,000. In Shaanxi, the population is distributed in Zhouzhi, Taibai, Foping, Ningshaan and Yangxian in the middle of the Qinling Mountains’ range, accounting for about 3,800–4,000 individuals in 39 groups [Li et al., 2002]. In Gansu, the population is mainly distributed in areas adjacent to the Sichuan Province, including Wenxian, Kangxian and Wuduon, accounting for about 800–1,000 individuals in 8 groups [Zhang, 1995]. Our field study revealed that both R. roxellana habitats in the Qinling Mountains occur mainly in subtropical and temperate forests, with monkeys foraging in the deciduous broad-leaf forests and the mixed coniferous and deciduous broad-leaf forests at elevations ranging from 1,400 to 3,300 m [Li et al., 2000]. The distribution of R. roxellana in the Qinling Mountains can be traced from the late Quaternary (table 1) in the Middle Pleistocene and Holocene deposits [Zhao and Li, 1981; Han, 1982; Wang et al., 1982; Ma and Tang, 1992; Jablonski and Peng, 1993; Pan, 1995; Jablonski, 1998a]. Although 2 fossil species, one from Xin’an in He’nan (R. tingianus) and the other from Lantian in Shaanxi and from Yunxian in Hubei (R. lantianensis), have been found as early as the Middle Pleistocene, these 2 species bear similarities to all modern species of Rhinopithecus but cannot be conclusively associated as an ancestor of R. roxellana. Although these fossils cannot be identified to spe-




348

cies level, they suggest that Rhinopithecus species were more extensively dispersed in the Early and Middle Pleistocene than they are today [Pan and Jablonski, 1987; Jablonski and Pan, 1988; Jablonski 1993; Jablonski, 1998a, b; Pan and Oxnard, 2001]. According to literature records, most R. roxellana populations have disappeared in the east and north-west Qinling Mountains during Chinese human civilization history, and current populations survive in only 2 isolated regions in Gansu and Shaanxi. This distribution scenario and local extinctions are likely related to human activities and social events in Chinese history. Influences on Rhinopithecus Distribution Changes before Human Activity (Early and Middle Pleistocene) Palaeontologists have found a relationship between climate change and evolution, suggesting that biological evolution is the result of or caused by climate change [Quan and Xie, 2002]. In the Early Pleistocene, 2 warm climate periods and 2 cool climate periods occurred. The warmer climates dated from 2.4 to 2 million years ago and 1.8 to 1 million years ago. The colder climates dated from 2 to 1.8 million years ago and 0.9 to 0.7 million years ago [Quan and Xie, 2002]. During the same periods, R. lantianensis and R. tingianus, both ancestors of modern Rhinopithecus, were more extensively distributed in the Qinling Mountains [Pan and Jablonski, 1987; Jablonski and Pan, 1988; Jablonski, 1998a, b; Pan and Oxnard, 2001]. At the end of the last cool period, the global climate had cooled and the flora and fauna had changed dramatically, resulting in the loss of forest habitats, habitat fragmentation and a decline in the distribution and density of Rhinopithecus populations [Jablonski, 1992; Li et al., 2003]. Changes in R. roxellana Distribution during the Stone Age (Late Pleistocene to 4,000 Years Ago) The oldest evidence of R. roxellana is a Middle Pleistocene cranium from He’nan [Jablonski, 1993], which coincides with the Stone Age of human civilization. During the Stone Age, the vegetation in the Qinling Mountains was predominantly undisturbed by human activity. In Neolithic Yangshao ash pits in Longgang temple, Shaanxi (approx. 4,000 years ago), a large number of forest animals, such as wild boar, bison, small deer and musk deer, have been discovered, adding to other animal fossils that existed at the same time in the Qinling Mountains. During the Stone Age, animals in the Qinling Mountains enjoyed a high-quality environment and forest coverage reached 70–80% [Wang and Yan, 2011]. Throughout this period, R. roxellana was distributed widely across high-quality habitat in the Qinling Mountains. Although humans lived in this area and manufactured rough tools for hunting at this time, archaeological examination of ash pits of these primitive settlements has rarely found R. roxellana bones [Liang, 2002]. The paucity of evidence in relation to human hunting and consumption is likely related to the arboreal nature of R. roxellana and the difficulties associated with its capture. Consequently, during the Stone Age, R. roxellana continued to thrive in high-quality Qinling Mountains’ habitats, without human factors impacting on their distribution. Changes in R. roxellana Distribution during the Bronze Age (Approx. 3,000 Years Ago) From 2100 BC to 221 BC, China entered the Bronze Age and feudal rule, which lasted more than 1,800 years and consisted of the Xia, Shang and Zhou Dynasties. The




Table 2. Plank road construction status in the Qin and Han Dynasties

Road name

Time of completion

Connects

Length, Reference km

Ziwu road

316 BC

Xi’an + Hanzhong

500

Shimen song, Eastern Han Dynasty

Tangluo road

244 BC

Xi’an + Hanzhong

240

Sanguo Dynasty record

Baoxie road

221 BC

Xi’an + Hanzhong

470

Huayang state record

Chencang road

206 BC

Xi’an + Hanzhong

600

Liuba county record

Bronze Age in China saw an increase in social and economic development, and Chinese agriculture moved from slash-and-burn cultivation to intensive agriculture [Liang, 2002]. Due to bronze ware production (firing materials) and agricultural-land requirements, flatland forest areas were very scarce at the end of this period, though remote mountainous areas were still uninhabited by people and high forest coverage was maintained. Consequently, natural conditions remained relatively unaffected and high-quality habitat persisted. Changes in R. roxellana Distribution during the Iron Age (Approx. 2,000 Years Ago) From the Qin Dynasty (221 BC), China entered the Iron Age. The invention of iron tools not only accelerated productive development and the changing social landscape, but also enhanced human ability to develop, manipulate and change the natural environment. The gradual movement of human populations into the Qinling Mountains and the introduction of iron tools impacted on the distribution area of R. roxellana greatly. Plank Road Construction in the Qin and Han Dynasties The development and use of iron allowed for significant expansion of human activities within the Qinling Mountains, including construction of the famous Qinling plank road [Zhou, 1993]. The plank road was built along cliffs and was overlaid by high quality woods such as pine and beech. The Qinling plank road was the main form of transportation in the area and was finally completed in the Western Han Dynasty (206 BC to 8 AD), with maintenance continuing in the following dynasties. Although this transportation system accelerated social exchange among Shaanxi, Hubei and Sichuan, the ecological impact in relation to forest destruction was substantial (table 2). Construction of the plank road consumed fuel wood for the fire and cold water shock techniques used to break huge rocks, as well as timber construction material for the vast number of columns and planks required. Because the plank road crossed through R. roxellana habitat and destroyed vegetation along the road, the once continuous habitat became divided and the impact of this human transportation thoroughfare increased with use. Royal Palace Construction in the Sui and Tang Dynasties During the middle of the Iron Age (221 BC to 709 AD), Shaanxi was the political centre of China, and 13 dynastic capitals were established in the city of




350

1,400

Present

Human population size (n × 106)

1,200 1,000 800 600 400

Qing Dynasty

200 0

Western Han Dynasty Jin Dynasty Eastern Han Dynasty

0

Tang Dynasty

Song Dynasty

Yuan Dynasty

Sui Dynasty

500

Ming Dynasty

1000 Year

1500

2000

Fig. 3. Changes in the size of the human population in China since the Western Han Dynasty.

Chang’an (now Xi’an). As a symbol of royal power, each Chinese emperor constructed palaces of his own, especially in the Han, Sui and Tang Dynasties. During the Tang Dynasty, Chang’an was not only unprecedented in ancient China, but was also the largest city in the world at that time. It was 2.4 times larger than Chang’an during the Han Dynasty, 1.7 times larger than Dadu (now Beijing) during the Yuan Dynasty, and 1.9 times larger than Nanjing in the Ming Dynasty. With the expanding scale of city construction, wood consumption also increased rapidly. Initially, the wood came from Nanshan located on the northern slopes of the Qinling Mountains; however, by the end of the Tang Dynasty, tens of thousands of people were sent to the southern slopes to continue logging for construction timber. Thus, the R. roxellana habitat experienced a significant impact and deterioration, with low altitude habitat disappearing and high altitude habitat declining significantly. Human Populations in the Qinling Mountains in the Song, Ming and Qing Dynasties During the early and middle Iron Age (before the Song Dynasty, 960 AD), R. roxellana habitat suffered a significant impact from human activities, although this impact was indirect. By the late Iron Age, however, humans began to compete di-




rectly with monkeys within their habitat for living space. During the early Song Dynasty (960 AD to 1127 AD), the human population density within the Qinling Mountains was low (

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