Biologia 69/11: 1625—1630, 2014
Section Zoology
DOI: 10.2478/s11756-014-0452-y
Potential effects of climate change on the Chinese Bulbul
(Pycnontus sinensis) in China
Longying Wen1,2* , Huigen He3, Yong Wang4, Jimmy Gorimar5 & Mark Liu6*
1
College of Life Sciences, Leshan Normal University, Leshan 614004, Sichuan, China; e-mail: lywen02@126.com
Key Laboratory of Colleges and Universities in Sichuan Province for Protecting Endangered Birds in the Southwest Mountains, Leshan, 614004, Sichuan, China
3
Chongqing Climate Center, Chongqing 401147, China
4
Department of Biological and Environmental Sciences, Alabama A&M University, Normal, AL 35762, USA
5
Faculty of English, Leshan Normal University, Leshan 614004, Sichuan, China
6
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA; e-mail:
markliu@fas.harvard.edu
2
Abstract: The Chinese Bulbul (Pycnontus sinensis) has an extensive distribution throughout southern China. Investigators
have reported that the species has expanded its distribution range northward since 1995. We performed a literature review
and analysis to examine the relationships between the range expansion of the species and the changes of climate and
habitat. We found that the northward range expansion was associated with the increased temperature and human created
habitat. We believe that the combination of the increased temperature and the ability to utilize human created habitat
while maintaining genetic diversity resulted in the population increase and range expansion of the species. We suggest that
increased temperature and human disturbance could lead to evolutionary and distributional changes of some species such
as the Chinese Bulbul, therefore possibly making these species indicators of climate change.
Key words: climate change; human activity; Chinese Bulbul; north range expansion; evolution
Introduction
The topic of climate change is not without controversy (Davidson & Janssens 2006; Hulme 2010). Understanding the effect of climate change on bird populations is undoubtedly important for our knowledge
of avian species evolution or extinction and maintaining biodiversity (Wang et al. 2012). One of the direct
impacts of climate change, particularly the change of
ambient temperature, is the temporal and spatial shifts
in food abundance and suitable habitat. For examples,
the great tit Parus major L., 1758 and the pied flycatcher Ficedula hypoleuca (Pallas, 1774) have showed
population declines because of changes in food availability during their breeding season (Both & Visser
2001). Climate change has also affected birds in other
aspects such as migration timing (Butler 2003; MurphyKlassen et al. 2005; MacMynowski et al. 2007), migration route (Fiedler 2003; Newton 2008), the occurrence
and spread of invasive avian species (Reino et al. 2009),
and other life-history features (Parmesan & Yohe 2003;
Rosenzweig et al. 2008) such as the breeding season
(Crick & Sparks 1999; Dunn & Winkler 1999). However,
these changes are complicated by concurrent alterations
caused by human activities such as the modification of
* Corresponding author
c 2014 Institute of Zoology, Slovak Academy of Sciences
land-use and land-cover patterns at local, regional, and
global landscape scales (Tryjanowski & Sparks 2001;
Rosenzweig et al. 2008). Many studies about the effect
of climate change on birds have focused on the shift
or expansion of species distribution range (Pounds et
al. 1999; Walther et al. 2002; Hitch & Leberg 2007;
La & Thompson 2007; Peh 2007; Brommer & Møller
2010; Robinet & Roques 2010). It is generally agreed
that climate changes affect bird species distributions
because species-specific physiological tolerance to temperature, precipitation, and other environmental variations (Woodward 1987; Hoffman & Parsons 1997). The
impact of climate change depends on the evolutionary
history and endogenous control mechanisms of the birds
(Knudsen et al. 2011). Some bird species are more sensitive to climatic change and can respond quickly to environmental changes (Møller et al. 2004). The Chinese
Bulbul Pycnontus sinensis (Gmelin, 1789) is a common
species of East Asia and widely distributed in southern China. The species is often associated with humanaltered habitats such as urban parks, forest belts, and
rural agricultural areas. Studies have reported recent
expansion of this species to previously uninhabited regions in northern China (Song et al. 2013; Xing et al.
2013). This northward expansion is consistent to what
L. Wen et al.
1626
Fig. 1. Distribution of Chinese Bulbul (Pycnonotus sinensis), grey area presenting provinces before range expansion, and 1, 2, 3, 4,
5, and 6 are new distribution locations: Zhengzhou (Henan Province), Rongcheng (Shandong Province), Qingyang (Gansu Province),
Beijing City, Dalian (Liaoning Province), and Xining (Qinghai Province), respectively.
Fig. 2. Annual mean temperature of Zhengzhou (Henan Province), Rongcheng (Shandong Province), Qingyang (Gansu Province),
Beijing City, Dalian (Liaoning Province), and Xining (Qinghai Province) during the period of 1951–2008.
has been reported in other bird species, supposedly in
response to climate change (Thomas & Lennon 1999;
Walther 2004). In addition to climatic change, other
researchers have reported that the range expansion of
some bird species could be due to the direct and indirect effects of human activities such as those related to
urbanization (Burger 1981; Jean-Marc 2006). We evaluated the data of Chinese Bulbul’s recent northward
expansion from literature, climate changes, and urbanization of the newly inhabited areas to explore the potential relationship between the northward range ex-
pansion of Chinese Bulbul and changes in climatic and
human activities.
Methods
We compiled the data from the studies that reported the
northward range expansion of the Chinese Bulbul in China
(Fig. 1). We obtained climatic data from the National Climate Center of China and data of human population growth
and the area of urban parks and gardens from the National
Bureau of Statistics of China for the new distribution loca-
Climate change and Chinese Bulbul distribution
1627
Table 1. Differences of the average temperature ( ◦C) and precipitation (mm) in Zhengzhou, Rongcheng, Qingyang, Beijing, Dalian,
and Xining between the period of 1951–1994 and that of 1995–2008. The differences were tested with two independent sample t-test.
Time classification
Annual
Spring
Summer
Autumn
Winter
Temperature
Precipitation
Temperature
Precipitation
Temperature
Precipitation
Temperature
Precipitation
Temperature
Precipitation
Zhengzhou
Rongcheng
Qingyang
Beijing
Dalian
Xining
1.01**
–1.48
1.56**
–0.36
0.18
48.77
0.91**
–16.50
1.40**
–8.78
1.02**
9.48
0.89**
12.79
0.21
8.08
1.28**
–12.21
1.70**
0.82
1.40**
–57.18
1.78**
–27.62
1.02**
–12.96
1.19**
–10.89
1.60**
–5.71
1.30**
–159.03
1.44**
6.82
0.96**
–171.59
1.13**
6.83
1.69**
–1.09
1.11**
–80.92
1.37**
8.18
0.87**
–54.74
0.82**
–22.02
1.39**
–12.34
0.00
54.25**
0.14
12.91
–0.01
31.20**
–0.27
10.56
0.13
3.04
Explanations: ** The difference is significant at the 0.01 level (2-tailed); * The difference is significant at the 0.05 level (2-tailed).
Fig. 3. The human population changes from 1954 to 2010 in Henan, Shandong, Gansu, Liaoning, and Qinghai provinces and Beijing
City.
tions of the Chinese Bulbul (Fig. 2). Because the Chinese
Bulbul was found to expand northward beginning in 1995
(Zhang et al. 2008), we used 1995 as the dividing year for
the period spanning from 1951 to 2008. We compared the
average temperature and precipitation between the period
from 1951 to 1994 and that from 1995 to 2008. The differences were tested with two independent sample t-test with
P < 0.05 as the significant level. Statistical analyses were
performed with SPSS16 (SPASS Inc., Chicago, IL USA).
Results
Northern range expansion of Chinese Bulbul
The Chinese Bulbul was first reported northward range
expansion in Zhengzhou, Henan Province of China
in 1995 (Zhang et al. 2008). Later it was found in
Qingyang, Gansu Province (Han & Zhou 2005); Beijing
(Zhang et al. 2003); Rongcheng, Shandong Province
(Yan 2003); Xingtai, Hebei Province (Wu & Wu 2005);
Dalian, Liaoning Province (Wang et al. 2005); Xining, Qinghai Province (Li et al. 2006); and Yinchuan,
Ningxia Huizu Autonomous Region (Du & Ma 2011).
The most recent report (Li et al. 2013) suggested
that the distribution was further expanded north to
Shenyang, Liaoning Province, at the latitude of 41◦ 42
(Fig. 1).
Changes in temperature and precipitation
The increasing trend in annual mean temperature appeared in Zhengzhou, Rongcheng, Qingyang, Beijing,
Dalian, and Xining from 1951 to 2008 (Fig. 2). Except
for Xining, the temperature was significantly higher
during the period of 1995–2008 than that of 1951–1994
for all areas where Chinese Bulbul newly occurred. The
temperature increased about two degrees Celsius in the
northern regions during both winter and spring seasons
(both P < 0.01). The precipitation was not different
between the two periods at these locations (Table 1).
Changes in human population and urban green areas
The human population increased during the period of
1954–2010 in all locations where the Chinese Bulbul
expanded its range to with an exception of Qinghai
Province. The largest population occurred in Henan
1628
L. Wen et al.
Fig. 4. The change of total areas of parks, gardens and green spaces (hectares) from 1999 to 2011 in Henan, Shandong, Gansu, Liaoning,
and Qinghai provinces and Beijing City.
and Shandong provinces of all years examined (Fig. 3).
Increased human population created extensive
metropolitan areas which lead to an increase in the
number of urban parks, gardens, and other urban green
spaces.
The trends of the change in the total green areas
were similar to that of human population growth. The
total areas of parks increased in all areas from 1999 to
2011. While the rate increase was the lowest at Qinghai Province, it was the highest at Shandong Province
(Fig. 4).
Discussion
This study suggested an association between the northern range expansion of the Chinese Bulbul and increasing temperature in mainland China. Climatic change
is often associated with the rising temperature during
winter and spring (McCarthy et al. 2001), which was
also the case in this study. Warmer temperature may
function as an ecological release for some species, and
allow these species to expand into areas where they were
not able to inhabit previously due to lower temperature
and lack of suitable resources such as food for survive or
breeding (Thomas & Lennon 1999; Walther et al. 2002;
Brommer 2004; Gao 2006; Gong 2007; Luo et al. 2006;
Parmesan 2006; Hitch & Leberg 2007; La & Thompson 2007; Stephen et al. 2011). The Chinese Bulbul’s
northward range expansion could be such an example
related to the climatic change. The northern expansion of the Chinese Bulbul could have an impact on the
surrounding habitat because of its dietary preferences.
Bulbuls are known to feed on the seeds of the Southern
China Yew (Taxus chinensis var. mairei), which could
lead to a northward expansion of the Yew and other
plant species: an indirect impact to the native ecosystems of climate change. On the other side, the native
species that cannot adapt to the new climate conditions or shift their geographical distribution may be at
risk of extinction when climate changes (Huntley et al.
2006; Thomas et al. 2004). The Chinese Bulbuls’ northward expansion is consistent with the paradigm that
geographically-widely distributed species have lower extinction probability compared to those with limited distribution range.
Climate change has been related to the events from
anthropogenic disturbances (Milly et al. 2005; Root et
al. 2005; Wu et al. 2005), and the change may advance
the time of leaf-out, flower blooming, and seed reproduction of plants (Rosenzweig et al. 2008). Food availability is often a limited factor for the range expansion
of animals. Our study showed that the urban green
area was increased with the increase of human population (Figs 3 and 4). The Bulbul, feeding primarily on
seeds, flowers, fruits, leaf buds and insects, benefited
most likely from the increase of both the temperature
and food resources at urban green areas associated with
the growth of human population in northern China,
which resulted in the northward range expansion of the
species.
Generally, there are lower levels of genetic diversities in frontier or pioneer populations because of
small population size or in-breeding among closely related individuals (Xie & Zhang 2006). However, genetic diversity has been found not be low in the newly
expanding populations of the Chinese Bulbul (Song
et al. 2013), which suggested the pioneer population
of the Bulbul still retains an innate evolutionary potential. It was reported that there are large variations in the song patterns of pioneer populations of
the Chinese Bulbul in the northern China than that
in the southern China (Xing et al. 2013). Individuals of the same species in different habitats with
large song variations could lead to breeding isolation
(Bermúdez-Cuamatzin et al. 2011), which may be one
of the mechanisms that the Chinese Bulbul has been
able to use to maintain its genetic diversity. The Chinese Bulbul could be a good model species for investigating the microevolution of spreading population.
Climate change and Chinese Bulbul distribution
Conclusion
The Chinese Bulbuls’ northward expansion was correlated with the temperature increase and habitat change
related to the human growth, which might provide suitable habitat with rich food resources for this species.
Behavioral characteristics of the species such as song
and vocal traits may be some of the mechanisms of the
species maintaining genetic diversity and evolutional
adaptation to the environment.
Acknowledgements
We thank the two anonymous reviewers and Mr. Andrew Cantrell who provided valuable inputs for significantly
improving the manuscript. This work was supported by
Natural Science Foundation of China (No.31372171), Department of Applied Basic Research of Sichuan Province
(2013JY0073), and Introduction to the Talent Research
Project (No.Z1064).
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Received October 29, 2013
Accepted September 20, 2014