Bryophyte diversity in karst sinkholes affected by different degrees of human disturbance

Run Liu, Zhaohui Zhang, Jiachen Shen, Zhihui Wang


The diversity of bryophytes in karst sinkholes has received little attention, and these habitats probably play a crucial role as refugia. In this study, bryophyte diversity affected by different levels of human disturbance in five karst sinkholes was compared. A total of 132 species of bryophytes (17 liverworts and 115 mosses) that belong to 64 genera and 30 families were recorded. The richness of the bryophytes in the natural sinkholes was significantly higher than that of the bryophytes in the sinkholes affected by tourism and used as farmland. Canonical correspondence analysis showed that soil moisture is one of the most important factors that affect the abundance of bryophyte distribution in the five sinkholes. Human activities, including agriculture, animal husbandry, and tourism development, reduce the bryophyte coverage of sinkholes and lead to soil moisture loss. Therefore, effective protection of karst sinkholes is required to maintain their original value for biodiversity conservation.


negative terrain; microhabitat; liverworts; environmental factors; artificial interference; Southwestern China

Full Text:



Bátori Z, Vojtkó A, Farkas T, Szabó A, Havadtői K, E. Vojtkó A, et al. Large- and small-scale environmental factors drive distributions of cool-adapted plants in karstic microrefugia. Ann Bot. 2017;119(2):301–309.

Raschmanová N, Miklisová D, Kováč Ľ. A unique small-scale microclimatic gradient in a temperate karst harbours exceptionally high diversity of soil Collembola. Int J Speleol. 2018;47(2):247–262.

Bátori Z, Körmöczi L, Erdös L, Zalatnai M, Csiky J. Importance of karst sinkholes in preserving relict, mountain, and wet-woodland plant species under sub-Mediterranean climate: a case study from southern Hungary. Journal of Cave and Karst Studies. 2012;74(1):127–134.

Galbreath KE, Hafner DJ, Zamudio KR. When cold is better: climate-driven elevation shifts yield complex patterns of diversification and demography in an alpine specialist (American pika, Ochotona princeps). Evolution. 2010;63(11):2848–2863.

Stewart JR, Lister AM, Barnes I, Dalén L. Refugia revisited: individualistic responses of species in space and time. Proc Biol Sci. 2010;277:661–671.

Ohlemüller R, Huntley B, Normand S, Svenning JC. Potential source and sink locations for climate-driven species range shifts in Europe since the Last Glacial Maximum. Global Ecology and Biogeography. 2012;21:152–163.

Theurillat JP, Guisan A. Potential impact of climate change on vegetation in the European Alps. Clim Change. 2001;50:77–109.

Bátori Z, Lengyel A, Maróti M, Körmöczi L, Tölgyesi C, Bíró A, et al. Microclimate–vegetation relationships in natural habitat islands: species preservation and conservation perspectives. Quarterly Journal of the Hungarian Meteorological Service. 2014;118(3):257–281.

Bátori Z, Galle R, Erdős L, Körmöczi L. Ecological conditions, flora and vegetation of a large doline in the Mecsek Mountains (south Hungary). Acta Bot Croat. 2011;70:147–155.

Lazarević P, Lazarević M, Krivošej Z, Stevanović V. On the distribution of Dracocephalum ruyschiana (Lamiaceae) in the Balkan Peninsula. Phytologia Balcanica. 2009;15:175–179.

Bátori Z, Csiky J, Farkas T, Vojtkó EA, Erdős L, Kovács D, et al. The conservation value of karst dolines for vascular plants in woodland habitats of Hungary: refugia and climate change. Int J Speleol. 2014;43(1):15–26.

Kovačič G, Barrage N. Analysis of human induced changes in a karst landscape – the filling of dolines in the Kras plateau, Slovenia. Sci Total Environ. 2013;447(1):143–151.

Valjavec MB, Zorn M, Čarni A. Bioindication of human-induced soil degradation in enclosed karst depressions (dolines) using ellenberg indicator values (classical karst, Slovenia). Sci Total Environ. 2018;640–641:117–126.

Marschall M, Proctor M. Are bryophytes shade plants? Photosynthetic light responses and proportions of chlorophyll a, chlorophyll b and total carotenoids. Ann Bot. 2004;94(4):593–603.

Liu Y, Li Z, Cao T, Glime JM. The influence of high temperature on cell damage and shoot survival rates of Plagiomnium acutum. Transactions of the British Bryological Society. 2004;26(4):265–271.

Mölder A, Schmidt M, Schönfelder E, Engel F, Schulz F. Bryophytes as indicators of ancient woodlands in Schleswig-Holstein (northern Germany). Ecol Indic. 2015;54:12–30.

Alatalo JM, Jägerbrand AK, Molau U. Testing reliability of short-term responses to predict longer-term responses of bryophytes and lichens to environmental change. Ecol Indic. 2015;58:77–85.

Frego KA. Bryophytes as potential indicators of forest integrity. For Ecol Manage. 2007;242(1):65–75.

Santos NDD, Costa DPD, Shepherd GJ, Kinoshita LS. Windborne: can liverworts be used as indicators of altitudinal gradient in the Brazilian Atlantic forest? Ecol Indic. 2014;36(36):431–440.

Robinson H, Wells J. The bryophytes of certain limestone sinks in Alpena County, Michigan. Bryologist. 1956;59(1):12–17.

Pericin C, Hürlimann H. Beobachtungen zur vertikalen Verteilung der Moosarten in der Doline Sterna-Filaria im Karstgebiet von Buje/Buie in Istrien (Kroatien). Bauhinia. 2001;15:91–96.

He W, Li P, Qian Z. Tiankeng and formation process in Zhijin cave geopark. Guizhou Science. 2011;29(3):1–7.

Gao Q. Flora Bryophytarum Sinicorum. Vol. 1. Beijing: Science Press; 1994.

Gao Q. Flora Bryophytarum Sinicorum. Vol. 2. Beijing: Science Press; 1996.

Li XJ. Flora Bryophytarum Sinicorum. Vol. 3. Beijing: Science Press; 2000.

Wu PC. Flora Bryophytarum Sinicorum. Vol. 6. Beijing: Science Press; 2002.

Wu PC, Jia Y. Flora Bryophytarum Sinicorum. Vol. 8. Beijing: Science Press; 2004.

Li XJ. Flora Bryophytarum Sinicorum. Vol. 4. Beijing: Science Press; 2004.

Hu RL, Wang YF. Flora Bryophytarum Sinicorum. Vol. 7. Beijing: Science Press; 2005.

Gao Q, Wu YH. Genera Hepaticopsida et Anthocerotopsida Sinicorum. Beijing: Science Press; 2010.

Wu PC, Jia Y. Flora Bryophytarum Sinicorum. Vol. 5. Beijing: Science Press; 2011.

Kimberling DN, Karr JR, Fore LS. Measuring human disturbance using terrestrial invertebrates in the shrub-steppe of eastern Washington (USA). Ecol Indic. 2001;1(2):63–81.

Wu ZY. The areal-types of Chinese genera of seed plants. Acta Botanica Yunnanica. 1991;4:1–139.

Roberts DW, Cooper SV. Concepts and techniques of vegetation mapping. In: Land classifications based on vegetation: applications for resource management. Ogden, UT: U.S. Department of Agriculture; 1989. p. 90–96.

Liu C, Li C, Shi M, Liang HY. Multivariate statistical analysis techniques applicated in differentiation of soil fertility. Acta Ecologica Sinica. 1996;16:444–447.

Qi YX, Luo H, Zhao TN. Simplified approach to measure canopy closure based on fish lenses. Journal of Beijing Forestry University. 2009;31(6):60–66.

Skuja A, SpuņGis V. Influence of environmental factors on the distribution of caddisfly (Trichoptera) communities in medium-sized lowland streams in Latvia. Estonian Journal of Ecology. 2010;59(3):197–215.

Bioinformatics and Evolutionary Genomics. Calculate and draw custom Venn diagrams [Internet]. 2019 [cited 2019 May 5]. Available form:

Hammer Ø, Harper DAT, Ryan PD. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica. 2001;4(1):[9 p.].

Li CY, Zhang ZH, Wu J, Li XF. Distribution pattern of liverwort community in relation to environmental factors of caves in karst tiankeng: a case study of Monkey-Ear Tiankeng of Guizou Province. Chinese Journal of Ecology. 2019;38(3):744–752.

Toure D, Ge J, Zhou J. Spatial patterns of tree species number in relationship with the local environmental variations in karst ecosystems. Applied Ecological and Environment Research. 2015;13(4):1035–1054.

Zhang Z, Gong DJ, Sun CX, Li XJ, Li WJ. Altitudinal patterns of species richness and species range size of vascular plants in Xiaolongshan Reserve of Qinling Mountain: a test of Rapoport’s rule. Chinese Journal of Applied Ecology. 2014;25(9):2477–2485.

Peng T, Zhang ZH. Study on bryoflora in Xiangzhigou karst area. Guizhou Province. Guizhou Science. 2009;27:56–62.

Zhang ZH, Chen JK. Floristic characteristics of aquatic bryophytes and their biokarst deposition types at waterfalls in central Guizhou, China. Carsologica Sinica. 2007;26(2):170–177.

Xiong YX. Bryophyte flora of Guizhou China. Guiyang: Guizhou Science and Technology Press; 2014.

Lenoir J, Gégout JC, Marquet PA, de Ruffray P, Brisse H. A significant upward shift in plant species optimum elevation during the 20th century. Science. 2008;320:1768–1771.

Thuiller W, Lavorel S, Araújo MB, Sykes MT, Prentice IC. Climate change threats to plant diversity in Europe. Proc Natl Acad Sci USA. 2005;102:8245–8250.

Jian XM, Shui Wei, Wang YA, Wang QF, Chen YP, Jiang C, et al. Species diversity and stability of grassland plant community in heavily-degraded karst tiankeng: a case study of Zhanyi tiankeng in Yunnan, China. Acta Ecologica Sinica. 2018;38(13):4704–4714.

Zhang ZH, Hu G, Zhu JD, Ni J. Stand structure, woody species richness and composition of subtropical karst forests in Maolan, South-West China. Journal of Tropical Forest Science. 2012;24(4):498–506.

Wei YW, Su YR, Chen XB, He XY. Effects of human disturbance on profile distribution of soil organic C, total N, total P and microbial biomass in karst region of northwest Guangxi. J Soil Water Conserv. 2010;24(3):164–169.

Kong XS, Qi SH, Sun Q, Huang BJ. Transport and differentiation of polycyclic aromatic hydrocarbons in air from Dashiwei karst sinkholes in Guangxi, China. Environmental Science. 2012;33(12):4212–4219.

Kong XS, Qi SH, Huang BJ, Zhang Y, Li J. Atmospheric deposition of PAHs in Dashiwei karst tiankeng group in Leye, Guangxi. Environmental Science. 2012;33(3):746–753.

Kong XS, Qi SH, Jian ZC, Huang BJ. Environmental factors on distribution of polycyclic aromatic hydrocarbons in soils from Dashiwei karst giant doline (tiankeng) in Guangxi, China. Environmental Science. 2012;33(11):3905–3915.

Sagar R, Raghubanshi AS, Singh JS. Tree species composition, dispersion and diversity along a disturbance gradient in a dry tropical forest region of India. For Ecol Manage. 2003;186(1–3):61–71.

Moritz C. Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol. 2002;51(2):238–254.

Zhu X, Tony W. Tiankeng: definition and description. Speleogenesis and Evolution of Karst Aquifers. 2006;4(1):8.