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Bryophyte Diversity Is Related to Vascular Plant Diversity And Ecological Indicators 120 (2021) 106947 Contents lists available at ScienceDirect Ecological Indicators journal homepage: www.elsevier.com/locate/ecolind Bryophyte diversity is related to vascular plant diversity and microhabitat T under disturbance in karst caves ⁎ Hai Rena,b, ,1, Faguo Wanga,1, Wen Yea,1, Qianmei Zhanga, Taotao Hana, Yao Huanga,b, Guowei Chua, Dafeng Huic, Qinfeng Guod a CAS Engineering Laboratory for Vegetation Ecosystem Restoration on Islands and Coastal Zones, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China b University of Chinese Academy of Sciences, Beijing 100049, China c Department of Biological Sciences, Tennessee State University, Nashville, TN 37209, USA d Southern Research Station, USDA Forest Service, Asheville, NC 28804, USA ARTICLE INFO ABSTRACT Keywords: Plant diversity, habitat properties, and their relationships in karst caves remain poorly understood. We surveyed Plant diversity vascular plant and bryophyte diversities and measured the habitat characteristics in six karst caves in south Habitat heterogeneity China with different disturbance histories (one had been disturbed by poultry feeding, three had been disturbed Light and water status by tourism, and two were undisturbed). The plant diversity differences among the six caves were analyzed using Soil nutrient cluster analysis, and the relationships of plant diversity and microhabitat were assessed using canonical cor- Restoration respondence analysis. We found a total of 43 angiosperm species from 27 families, 20 lycophyte and fern species from 9 families, and 20 species of bryophytes from 13 families in the six caves. Habitat characteristics including light intensity, air relative humidity, air temperature, and soil properties varied among the caves. The plant diversity in karst caves was not rich, but the species composition was unique. The caves with high disturbance had the lowest species richness, numbers of individuals, and Shannon-Wiener diversity indices but the highest Simpson’s dominance indices. The caves with less disturbance had the highest numbers of species, numbers of individuals, and Shannon-Wiener diversity indices but the lowest Simpson’s dominance indices. The disturbed caves were often dominated by drought-tolerant, tenacious mosses (bryophytes), while the relatively un- disturbed caves contained abundant liverworts (bryophytes), which were better adapted to humid environments. Plant diversity in karst caves was closely related to habitat heterogeneity, light and water status, and nutrient availability. Tourism and poultry farming were associated with the degradation of vegetation in some karst caves. Protecting and restoring bryophytes might facilitate the settlement, growth, and succession of vascular plants in karst caves. Bryophytes can be used as indicators of overall plant diversity and restoration status in karst caves. 1. Introduction features, the ecosystems in karst regions are fragile and extremely vulnerable to human disturbance (Brandt et al., 2018). Increased Karst landscapes are widely distributed and account for nearly 15% human exploitation of natural resources and agricultural activities have of the world’s land surface. The karst regions of China cover 1.9 million resulted in vegetation loss and land degradation during the last half km2 (about 0.54 million km2 are underlain by carbonate rocks) and are century in the karst regions of China (Tong et al., 2018). Karst soils are among the largest karst regions in the world (Yuan, 1994). The average thin and have great spatial heterogeneity, and these properties affect density of karst caves is 6.4/km2 in China as a whole and is 41.8/km2 in the conservation and restoration of the plant communities that they South China (Zhang, 1986). Topographic features of karst regions in- support (Cong et al., 2017; Wang et al., 2020). The structure, function, clude caves, sinkholes, and mogotes. Because of these geological and dynamics of karst vegetation in China have been recently ⁎ Corresponding author at: CAS Engineering Laboratory for Vegetation Ecosystem Restoration on Islands and Coastal Zones, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China. E-mail addresses: [email protected], [email protected] (H. Ren), [email protected] (F. Wang), [email protected] (W. Ye), [email protected] (Q. Zhang), [email protected] (T. Han), [email protected] (Y. Huang), [email protected] (G. Chu), [email protected] (D. Hui), [email protected] (Q. Guo). 1 Contribute equally. https://doi.org/10.1016/j.ecolind.2020.106947 Received 28 February 2020; Received in revised form 13 August 2020; Accepted 8 September 2020 1470-160X/ © 2020 Elsevier Ltd. All rights reserved. H. Ren, et al. Ecological Indicators 120 (2021) 106947 investigated (Wang et al., 2011, 2020; Voloscuk et al., 2016; Zhang 2.2. Plant survey, soil sampling, and analysis et al., 2016; Cong et al., 2017; Cao et al., 2020; Tong et al., 2020). Although caves are threatened biodiversity hotspots, they receive The study involved six caves of similar size and altitude: Caves A, B, little governmental attention or appropriate management (Barr, 1964; C, and D are located in Dixiahe (the distance between them is < 2 km), Medellin et al., 2017). There is no governmental agency or non-gov- and Caves E and F are located in Shangbaichang (the distance between ernmental organization concerned with the conservation of cave eco- them is about 1 km). Shangbaichang is about 21 km away from Dixiahe. systems in China or in many other countries (Whitte, 2009). There are Caves A, B, and C were developed into tourist spots in 1988. At present, caving expeditions, but such expeditions concentrate on exploration there are 800,000 visitors every year at Cave A. Cave B was closed to rather than on the investigating cave organisms. Disturbances by tourism and subjected to natural restoration after 2000. Cave C was farming, visitors, tourism infrastructure, and changes in water flow can protected after 2010. Caves D and E were relatively undisturbed. Cave F have devastating effects on the highly adapted and range-restricted has long been used to feed poultry and is highly disturbed. The major organisms that live in caves (Whitte, 2009). Cave conservation and disturbances to caves A, B, and C included atmospheric, water, and restoration therefore require the attention of researchers and govern- noise pollution, the damage and interference on animals and plants, mental agencies (Elliott, 2006). The use of mosses as nurse plants to and the damages caused by the construction of scenic spots. The major restore endangered herbs in karst caves is one of the few studies of karst disturbances at cave F included atmosphere pollution and the con- cave restoration (Ren et al., 2010a). sumption of plants by poultry. We could not find three replicate caves Although cave vegetation and soils are important in the study of with similar size and altitude for each disturbance type in Lianzhou autogenic/primary succession, cave ecology, evolutionary biology, and City. Therefore, we did not conduct any univariate statistical compar- global change biology, they are poorly understood (Barr, 1964; Bai isons of richness and diversity values among disturbance types or lo- et al., 2020). Karst caves and their entrances have dim light with lim- cation types within the caves. ited nutrient availability, high humidity, and relatively low tempera- At each cave, we established three plots, each with an area of ture fluctuations (Northup and Lavoie, 2001). The karst cave plant 5 m × 5 m, along a transect from the entrance of the cave to deep into community is a relic of the surrounding karst forest community and is the cave; the intervals between plots (from the entrance inward) were strongly dominated by understory life forms and taxa. The vegetation at 10, 30, and 60 m. Hereafter, the plots at the entrance, at the deepest cave entrances usually has low species richness and a small number of location, and at the intermediate location are referred to as entrance individuals (Supplementary Fig. 1 and Supplementary Fig. 2). In con- plots, deep plots, and intermediate plots. A light gradient existed among trast, the plant communities in karst caves are often diverse (Monro the plots at each cave because the light exposure declined with distance et al., 2018). Bryophytes are the most common plants in karst caves from the cave entrance. Field sampling was conducted at the beginning (Mulec and Kubešová, 2010; Cong et al., 2017; Puglisi et al, 2019). of November 2018. Bryophytes may be used as indicators of plant diversity and ecosystem All plant species were identified in each plot, and the height, den- health in karst caves. The plant diversity in karst caves is closely related sity, and crown of all plant species were measured (Ren et al., 2010b). to micro-habitat properties. As noted earlier, human disturbance such Three subplots with an area of 1 m × 1 m each were established in each as tourism and agriculture can lead to habitat and vegetation de- plot; the bryophyte, lichen, and algal species and their coverage area gradation in karst caves (Belnap and Lange, 2013; Liu et al., 2019; were recorded in each subplot (Li et al., 2015; Cong et al., 2017; Wu Pakeman et al., 2019). Leaf nutrient concentrations of cave-dwelling et al., 2019). We also collected soil samples during vegetation surveys. plants often reveal convergent adaptations to cave environments (Bai Because the soils around the cave entrances
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