Introduction

Nowadays, global biodiversity loss is well known and biodiversity conservation is closely relevant to human well-being (LI et al., 2011; MA et al., 2012; XU et al., 2012; WU et al., 2013; DENNIS et al., 2017). With urbanization and the development of tourism, the ecological environment has been destroyed, and habitats have become fragmented, which threatens the environments where butterflies and other animals live (VU, 2009; HARSH et al., 2015; MEI et al., 2015). Butterflies occupy an important position in ecosystems due to their pollinator status and their environmental indicator status (ROBBINS et al., 1997; ALURI et al., 2002; GHAZOUL, 2002; WANG et al., 2008; KHANDOKAR et al., 2013). Butterflies can respond quickly to changes in climate, humidity, temperature, light and some other factors and may act as representatives for less well-monitored insect groups (PARMESAN et al., 1999; FANG et al., 2010; MIHINDUKULASOORIYA et al., 2014; DENNIS et al., 2017). Moreover, butterfly indicator can monitor changes and assess the biodiversity status of environment (DENNIS et al., 2017). In addition, positive relationships have been reported between butterfly diversity and plant diversity (THOMAS & MALORIE, 1985; LEPS & SPITZER, 1990). Contemporarily, the existence and diversity of butterflies are facing threats from vegetation damage, habitat degradation, habitat fragmentation and human interference (KHANDOKAR et al., 2013; HARSH et al., 2015).

Simian Mountain is a nature reserve of the forest ecosystem type and contains a well-preserved belt of subtropical, evergreen, primary, broad-leaved forest. Naturally, it is an excellent habitat for insects due to its abundant and diverse vegetation, moderate climate and plentiful rainfall (LU et al., 2009; YANG, 2009; HE & DU, 2013). However, it is also a tourist area and summer resort because of its beautiful scenery and cool summer, which will certainly have influence on the habitats and diversity of insects. So far, only a few studies on the species diversity or fauna of insects have been reported in Simian Mountain (CHEN et al., 1994; LI et al., 2004; HE et al., 2013).

This study was conducted to reveal and compare the composition and diversity of butterflies in different habitats, and to reveal the influence of ecological environment and human interference on butterfly diversity in Simian Mountain. The results would provide original data for biodiversity assessment and be constructive to conservation of butterfly diversity.

Materials and methods

STUDY AREA AND SAMPLING SITES

The field survey was conducted in different habitats in Simian Mountain Natural Reserve (28.251~28.391 N, 106.221~106.251 E) in Jiangjin District, Chongqing, China.

The five fixed-distance belt transects, i.e., sampling sites, selected for the field survey were chosen mainly based on their vegetation, altitude and intensity of human interference and so on. Each permanent belt transect measures two kilometres long and five metres wide (POLLARD, 1977). The five belt transects were abbreviated as Sample I, Sample II, Sample III, Sample IV and Sample V, respectively, in this paper.

MATERIALS

The butterflies in this study were observed or collected from the five belt transects in Simian Mountain, and some photos were taken during the survey. Specimens were deposited in the College of Plant Protection, Southwest University, Chongqing, China (SWUCPP).

SURVEY METHODS

Monthly field surveys were conducted from April to September in the five belt transects during 2016 to 2018. The intervals between two monthly observations were 20-30 days. The butterfly observations were carried out between 9:00 and 12:00 am or between 14:30 and 17:30 pm on sunny or cloudy days with temperatures above 17~25ºC and a wind speed below 2 m/s.

Butterfly species and their populations were observed and recorded along the belt transects within a five-metre-wide area and five metres above and five metres to the front of recorder (POLLARD, 1977; RAMESH & HUSSAIN, 2010; LEVANONI et al., 2011; MAYUR et al., 2013; NIDUP et al., 2014). In general, the survey of each belt transect was finished within 1.5~2.0 hours by the observers keeping their walking speed slow and uniform. Necessary stops were made to examine and identify the species closely and to take photos. A few individuals that could not be identified accurately in the field were captured and brought to the laboratory for identification. When the butterfly population was too large to be measured exactly, the number of butterflies had to be estimated, and usually photos or videos were taken at the same time for a more accurate estimate. In addition, the habitat data for each survey, such as the date, time, temperature, humidity, weather conditions and environmental status, were recorded for further statistical analysis.

BUTTERFLY IDENTIFICATION

Identification of butterfly species mainly followed CHOU (1994, 1998), WU (2001, 2010), WANG & FAN (2002), LANG (2012, 2017), YUAN et al. (2015), WU & XU (2017) and so on. The classification system of butterflies mainly followed CHOU (1994) and LANG (2012) in this study.

DATA ANALYSIS

The indices used in the butterfly diversity analysis are as follows. 1. Shannon-Wiener index (H´): H´=∑ PilnPi; 2. Pielou evenness index (J): J=H´/lnS; 3. Relative abundance (Ra): Ra=Ni/N×100%; 4. Margalef index (R): R=(S-1)/lnN.

Results and Analysis

A total of 3004 individuals of 151 species belonging to 82 genera in 6 families were recorded in our survey, and two subfamilies (Heliconiinae, Libytheinae), 22 genera and 67 species of them were recorded from Simian Mountain for the first time. Celastrina argiolus (Linnaeus, 1758), recorded in all belt transects and with 646 recorded individuals and a relative abundance (Ra) of 21.50%, was the dominant species in Simian Mountain. It was closely followed by Pieris canidia (Sparrman, 1768) with 473 individuals and a relative abundance of 15.75%, and the relative abundance of remaining species were not more than 5.13%. A total of 48 species, such as Papilio machaon Linnaeus, 1758, P. polytes Linnaeus, 1758 and Gonepteryx maxima Butler, 1885, etc., had only one individual observed in the three years, were very rare in this area (see the Appendix).

Among the 6 families, Nymphalidae had 35 genera and 81 species recorded in the survey. It had the highest species richness (R), followed by Hesperiidae, Nymphalidae (Satyrinae), Lycaenidae, Papilionidae, Riodinidae, Pieridae, Nymphalidae (Morphinae, Amathusiini) and Nymphalidae (Danainae) and had the highest species diversity (H´(S)), followed by Hesperiidae, Nymphalidae (Satyrinae), Papilionidae, Riodinidae, Pieridae, Lycaenidae, Nymphalidae (Morphinae, Amathusiini) and Nymphalidae (Danainae). Lycaenidae had the highest genus diversity (H´(G)), followed by Hesperiidae, Nymphalidae (Nymphalinae), Nymphalidae (Satyrinae), Pieridae, Riodinidae, Papilionidae and Nymphalidae (Morphinae, Amathusiini). The species richness, species diversity, genus diversity of Nymphalidae (Heliconiinae, Acraeini) and Nymphalidae (Libytheinae) were all the least. In addition, the genus diversity of Nymphalidae (Danainae) was also the least. The results showed that Nymphalidae was the dominant group and that its community composition was more stable than that of the other families in Simian Mountain (Table 1).

In terms of butterflies in different habitats, the family diversity (H´(F)) in Sample I was the highest, followed by that in Samples II, III, IV, V; the genus diversity (H´(G)) in Sample II was the highest, followed by that in Samples III, I, V and IV; the species diversity (H´(S)) and the evenness index (J) in Sample V were the highest, followed by that in Samples I, III, II and IV; and the species richness (R) in Sample V was the highest, followed by that in Samples III, I, II, and IV. It can be concluded that most metrics of butterfly diversity were the least in Sample IV, including the genus

diversity, species diversity, evenness index and species richness (Table 2). It could be concluded that the butterfly diversity were higher in those habitats with better ecological environment, while the highest diversity of butterfly was not in the habitat with the most intact ecological environment, and strong human interference could significantly decrease the diversity of butterfly.

Discussion

In our survey, 67 species of butterflies were recorded for the first time in Simian Mountain and 68 species recorded by LI & HOU (2004) were not found in our survey. It is possible that the fauna investigation by Li and Hou was not comprehensive and some habitats suitable for some butterflies were not included in our sampling sites; of course, other reasons might also exist. In summary, the diversity of butterfly in this area is rich.

This study showed that Nymphalidae had the highest species diversity and species richness among the 6 families, and Acraeini and Libytheinae had the least in Simian Mountain. This result was also found in other studies (MAJUMDER et al., 2013; QURESHI, 2014; HARSH et al., 2015; SHANG et al., 2017). It could be attributed to the following factors. First, Nymphalidae is the most speciose group of butterflies (NIDUP et al., 2014), while Acraeini and Libytheinae are small groups. Second, members of Nymphalidae are able to inhabit different habitats for resources owing to their polyphagous nature and their stronger ability to fly (ESWARAN & PRAMOD, 2005; KRISHNAKUMAR et al., 2008; RAUT & PENDHARKAR, 2010; SARKAR et al., 2011; HARSH et al., 2015; WIDHIONO, 2015). In addition, they can avoid shade and dense vegetation but frequent openings in all vegetation types, including clearings in evergreen forest (MALI et al., 2014).

Overall, the ecological environment of Simian Mountain is suitable for the existence of butterflies. Species diversity is closely associated with their habitats, for example, butterfly diversity can reflect the diversity of host plants in the habitat (NIDUP et al., 2014; HARSH et al., 2015). In other words, an abundance of diverse vegetation generally supports high butterfly diversity. And other factors in habitats, such as light and human activities, can also influence species diversity. These were demonstrated in our survey. Among the five belt transects, the species diversity of butterfly in Sample V was the highest, closely followed by that in Sample I. It showed that Sample I in which ecological environment was relatively intact had not the highest butterfly diversity. And it indicated that not only an abundance of diverse vegetation but also a wide field of vision with sufficient light, a feature of Sample V, was important factor for a higher species diversity of butterfly. Moreover, intermediate human interference in Sample V might be helpful for species diversity which accorded with the intermediate disturbance hypothesis (CONNELL, 1978; HU et al., 2010). In addition, the diversity of butterfly in Sample IV was the least because of its less and simpler vegetation and strong human interference. This result implied that the ecological environment might have been destroyed or the vegetation had become simple probably if the diversity and populations of butterflies were distinctly decreased in the habitats under normal climatic conditions. Therefore, an effective way to protect the diversity of butterflies is to protect the environment in which they live.

At present, the main threat to butterfly diversity in Simian Mountain is the influence of tourism development. Therefore, measures such as controlling the number of tourists and vehicles and stopping additional construction in the Natural Reserve must be taken to decrease human interference and protect the habitats of butterflies. Of course, continued monitoring of butterfly diversity is highly advocated for biodiversity assessment and conservation.

Acknowledgments

Our sincere appreciation was presented to the Forestry Resources Administration Bureau of Simian Mountain, Chongqing, China, for their support and assistance in the field survey and to the other members of the Lepidoptera Laboratory of Southwest University for their efforts in the field survey. This study is funded by the Biodiversity Conservation Program of the Ministry of Ecology and Environment, China (SDZXWJZ01007-2016), by Chongqing Research Program of Basic Research and Frontier Technology (cstc2018jcyjAX0544) and by the National Natural Science Foundation of China (31772500).

BIBLIOGRAPHY

ALURI, J. S. R. & RAO, S. P., 2002.– Psychophily and evolutionary considerations of Cadaba fruticosa L. (Capparaceae).– Journal of the Bombay Natural History Society, 99(1): 59-63.

CHEN, B., LAN, J. H. & ZHANG, J., 1994.– Fauna analysis and vertical distribution of Scarabaeoidea in Simian Mountain, Sichuan.– Journal of Southwest China Normal University (Natural Science), 19(3): 298-304.

CHOU, I., 1994.– Monograph of Chinese butterflies: 854 pp. Henan Science and Technology Publishing house, Zhengzhou.

CHOU, I., 1998.– Classification and identification of Chinese butterflies: 349 pp. Henan Science and Technology Publishing house, Zhengzhou.

CONNELL, J. H., 1978.– Diversity in tropical rain forests and coral reefs.– Science, 199(4335): 1302-1310.

DENNIS, E. B., MORGAN, B. J. T., ROY, D. B. & BRERETON, T. M., 2017.– Urban indicators for UK butterflies.– Ecological Indicators, 76: 184-193.

ESWARAN, R. & PRAMOD, P., 2005.– Structure of butterfly community of Anaikatty hills, Western Ghats.– Zoos Print Journal, 20(8): 1939-1942.

FANG, L. J. & GUAN, J. L., 2010.– Progress in the studies of butterflies in response to global climate change.– Journal of Environmental Entomology, 32(3): 399-406.

GHAZOUL, J., 2002.– Impact of logging on the richness and diversity of forest butterflies in a tropical dry forest in Thailand.– Biodiversity and Conservation, 11(3): 521-541.

HARSH, S., JENA, J., SHARMA, T. & SARKAR, P. K., 2015.– Diversity of butterflies and their habitat association in four different habitat types in Kanha-Pench corridor, Madhya Pradesh, India.– International Journal of Advanced Research, 3(1): 779-785.

HE, G. Q. & DU, X. C., 2013.– Study on species diversity and fauna of Spilomelinae from Simian Mountian Nature Reserve in Chongqing.– Journal of Southwest University (Natural Science Edition), 35(9): 43-48.

HU, B. B., LI, H. H. & LIANG, Z. P., 2010.– Diversity and fauna of butterflies in Baxian Mountain State Nature Reserves.– Acta Ecologica Sinica, 30(12): 3226-3238.

KHANDOKAR, F., RASHID, M., DAS, D. K. & HOSSAIN, M., 2013.– Species diversity and abundance of butterflies in the Lawachara National Park, Bangladesh.– Jahangirnagar University Journal of Biological Science, 2(2): 121-127.

KRISHNAKUMAR, N., KUMARAGURU, A., THIYAGESAN, K. & ASOKAN, S., 2008.– Diversity of papilonid butterflies in the Indira Gandhi Wildlife Sanctuary, Western Ghats, Southern India.– Tigerpaper, 35(1): 1-8.

LANG, S. Y., 2012.– The Nymphalidae of China (Lepidoptera, Rhopalocera). Part I: 454 pp. Tshikolovets Publications, Pardubice.

LANG, S. Y., 2017.– The Nymphalidae of China (Lepidoptera, Rhopalocera). Part II: 200 pp. Tshikolovets Publications, Pardubice.

LEPS, J. & SPITZER, K., 1990.– Ecological determinants of butterfly communities (Lepidoptera, Papilionoidea) in the Tam Dao Mountains, Vietnam.– Acta Entomologica Bohemoslovaca, 87(3): 182-194.

LEVANONI, O., LEVIN, N., PEER, G., TURBÉ, A. & KARK, S., 2011.– Can we predict butterfly diversity along an elevation gradient from space?.– Ecography, 34(3): 372-383.

LI, S. H. & HOU, J., 2004.– Studie on butterfly fauna in the Simian Mountain in Chongqing Muncipality.– Journal of Southwest Agricultural University (Natural Science), 26(4): 405-408.

LI, Y. L., ZHEN, S. W. & GONG, G. T., 2011.– Progress in biodiversity research.– Journal of Sichuan Forestry Science and Technology, 32(4): 12-19.

LU, W. L., ZHANG, H. J., WANG, W., WANG, B. & ZHANG, R., 2009.– Studies on biodiversity in five different deposition model plantations in Chongqing Simian Mountain.– Acta Botanica Boreal-Occidentalia Sinica, 29(1): 160-166.

MA, J. Z., RONG, K. & CHEN, K., 2012.– Research and practice on biodiversity in situ conservation in China: progress and prospect.– Biodiversity Science, 20(5): 551-558.

MAJUMDER, J., LODH, R. & AGARWALA, B. K., 2013.– Butterfly species richness and diversity in the Trishna Wildlife Sanctuary in South Asia.– Journal Insect Science, 13(79): 1-13.

MALI, M., KHOKHARIYA, B. P. & DABGAR, Y. B., 2014.– Biotic interrelationship of plants and butterflies in surrounding of Gandhinagar, Gujarat.– International Journal of Scientific Research, 3(4): 420-422.

MAYUR, A. M., HATTAPPA, S., MAHADEVAMURTHY, M. & CHAKRAVARTHY, A. K., 2013.– The impact of newly established Bangalore international airport on local biodiversity.– Global Journal of Biology Agriculture & Health Sciences, 2(2): 49-53.

MEI, J., RAN, H. & YANG, T. Y., 2015.– Species diversity of butterflies in Fanjing Mountain National Nature Reserve of Guizhou.– Chinese Journal of Ecology, 34(2): 504-509.

MIHINDUKULASOORIYA, M. W. D. M., RANAWANA, K. B. & MAJER, J. D., 2014.– Comparison of butterfly diversity in natural and regenerating forest in a biodiversity conservation site at Maragamuwa, Sri Lanka.– Journal of Biodiversity and Environmental Sciences, 5: 387-391.

NIDUP, T., DORJI, T. & TSHERING, U., 2014.– Taxon diversity of butterflies in different habitat types in Royal Manas National Park.– Journal of Entomology and Zoology Studies, 2(6): 292-298.

PARMESAN, C., RYRHOLM, N. & STEFANESCU, C., 1999.– Poleward shifts in geographical ranges of butterfly species associated with regional warming.– Nature, 399(6736): 579-583.

PIELOU, E. C., 1966.– The measurement of diversity in different types of biological collections.– Journal of Theoretical Biology, 13(1): 131-144.

POLLARD, E., 1977.– A method for assessing changes in the abundance of butterflies.– Biological Conservation, 12(2): 115-134.

QURESHI, A. A., 2014.– Diversity of butterflies (Lepidoptera: Papilionoidea and Hesperoidea) of Dachigam National Park, Jammu and Kashmir, India.– Journal of Threatened Taxa, 6(1): 5389-5392.

RAMESH, T. & HUSSAIN, K. J., 2010.– Patterns of diversity, abundance and habitat associations of butterfly communities in heterogeneous landscapes of the department of atomic energy (DAE) campus at Kalpakkam, South India.– Biodiversity Conservation, 2(4): 75-85.

RAUT, N. B. & PENDHARKAR, A., 2010.– Butterfly (Rhopalocera) fauna of Maharashtra Nature Park, Mumbai, Maharashtra, India.– Check List, 6(1): 22-25.

ROBBINS, R. K., OPLER, P., REAKAKUDLA, A. M. L., WILSON, D. E. & WILSON, E. O., 1997.– Butterfly diversity and preliminary comparison with bird and mammal diversity.– Joseph Henty Press, Biodiversity, 2: 69-82.

SARKAR, V. K., DAS, D. S., BALAKRISHNAN, V. C. & KUNTE, K., 2011.– Validation of the reported occurrence of Tajuria maculata, the Spotted Royal butterfly (Lepidoptera: Lycaenidae), in the Western Ghats, southwestern India, on the basis of two new records.– Journal of Threatened Taxa, 3(3): 1629-1632.

SHANG, S. Q., ZHANG, H. Y. & TIAN, F. B., 2017.– Diversity of butterfly fauna in Xinglong Mountain National Nature Reserve of Gansu Province.– Pratacultural Science, 34(6): 1314-1322.

THOMAS, C. D. & MALORIE, H. C., 1985.– Rarity, Species richness and conservation: Butterflies of the Atlas Mountains in Morocco.– Biological Conservation, 33: 95-117.

VU, L. V., 2009.– Diversity and similarity of butterfly communities in five different habitat types at Tam Dao National Park, Vietnam.– Journal of Zoology, 277(1): 15-22.

WANG, M. & FAN, Y. L., 2002.– Butterflies Fauna Sinica: Lycaenidae: 440 pp. Henan Science and Technology Publishing house, Zhengzhou.

WANG, Y. P., WU, H. & XU, H. C., 2008.– Butterfly diversity and evaluation offoresteco-system health in important ecological areas of Zhejiang Province.– Acta Ecologica Sinica, 28(11): 5259-5269.

WIDHIONO, I., 2015.– Diversity of butterflies in four different forest types in Mount Slamet, Central Java, Indonesia.– Biodiversitas Journal of Biological Diversity, 16(2): 196-204.

WU, C. S., 2001.– Fauna Sinica Insecta. Lepidoptera Papilionidae, 25: 367 pp. Science Press, Beijing.

WU, C. S., 2010.– Fauna Sinica Insecta. Lepidoptera Pieridae, 53: 416 pp. Science Press, Beijing.

WU, C. S. & XU, Y. F., 2017.– Butterflies of China, 1-4: 2036 pp. The Straits Publishing House, Fujian.

WU, J. Y., XUE, D. Y. & ZHAO, F. W., 2013.– Progress of the study on investigation and conservation of biodiversity in China.– Journal of Ecology and Rural Environment, 29(2): 146-151.

XU, H. G., DING, H. & WU, J., 2012.– Interpretation of the 2020 global biodiversity targets and its assessment indicators.– Journal of Ecology and Rural Environment, 28(1): 1-9.

YANG, F., 2009.– Studies on Amphibian diversity in the Simian Mountains of Chongqing.– Sichuan Journal of Zoology, 28(4): 611-613.

YUAN, F., YUAN, X. Q. & XUAN, G. X., 2015.– Fauna Sinica Insecta. Lepidoptera Hesperiidae, 55: 754 pp. Science Press, Beijing.

Author notes

*Autor para la correspondencia / Corresponding author. E-mail: duxicui@hotmail.com