FIGURE 6 Indicator species in different segments of Yuanjiang dry-hot valley. (A) Upper stream, transect A; (B) Middle stream, transect B; (C) Downstream, transect F; (D) Aleuritopteris squamosa indicator of transect A; (E) Sinephropteris delavayiindicator of transect B; (F) Selaginella pseudopaleiferaindicator of transect F.
4. Discussion
4.1. Variation of thermal and moisture altitudinally
The importance of altitudes in plant distribution is usually ignored. However, some studies have paid attention to altitudinal influence on vascular plants. In the tropical area, studies reveal a hump-shaped pattern with the highest diversity at mid-altitudes and then decrease toward both high and low altitudes (Hernández-Rojas et al ., 2018). The altitude where maximum fern and fern allies diversity occurs differs somehow among mountain ranges. For example, maximum diversity occurs around 1,800 m in both Costa Rica (Kluge et al ., 2006) and Mount Kinabalu, Borneo (Kessler et al ., 2001), 2,000 m in Bolivia (Salazar et al ., 2015), and 2,400 m on Mount Kilimanjaro, Tanzania (Kessler et al ., 2011). Climatically, these gradients corresponded to the upper parts of tropical gradients where richness also declined. Species were comparable between these data sets at the same mean annual temperature. In temperate regions, richness was reported to decline continuously with elevation or remains roughly constant, such as New Zealand or North America (Brock et al ., 2016). In subtropical regions, a study from the Fanjingshan of Guizhou, China revealed a strong negative correlation between altitude and species (Wang et al ., 2008).
The altitudinal transects along mountain slope were located from 360~690 m a.s.l . (table 1). The annual temperature was over 22.3 OC, and annual precipitation was less than 984 mm (Supplementary data: Table A). Species regeneration was difficult for most species. Generally, fern and fern allies were rarely discovered, in which two species were discovered in transect C, and three species were in transect E. Transect B was different from C and E. In contrast, it was rich in fern and fern allies with 22 species and 971 individuals (Supplementary data: Table B). Such a difference could be explained with topographic features. The altitude of transects C and E was around 970 m a.s.l ., where annual temperature and precipitation were 20.8 OC and 785 mm, respectively. In contrast, the altitude of transect B was around 1750 m a.s.l ., where annual temperature and precipitation were 16.8 ~ 17.3 OC and 1211 ~ 1312 mm, respectively (Supplementary data: Table A). Rainfall drained into the ravine and supports the plants inside. Water supply in transect B was better than others because there was plenty of water supply coming from the higher elevation. Relative humidity was recorded at above 90% in transect B, which was more humid than other transects (around 72%). Comparing to the drought in transects C and E, much more shrubs (Salix myrtillacea, Ilex cornuta, Buddleja officinalis, Solanum verbascifolium etc .) and trees (Phyllanthus emblica, Trema tomentosa, Grewia biloba var. parviflora, Broussonetia papyrifera etc. ) were developed. A closed canopy was composed in densely vegetates. Diversity in the closed ravine was higher than an open ravine or a ridge.
4.2. Water condition determines the distribution of fern and fern allies
The population of species acquiring high water supply had shrunk in Yuanjiang dry-hot valley for centuries (Xu, 1985). Undoubtedly, fern populations were distributed broadly in the past compared to the mosaic habitats nowadays. Water condition has traditionally been considered a decisive factor for fern and fern allies (Kluge et al ., 2006; Yang et al ., 2011). The fern and fern allies flourishment is interpreted as a reflection of environmental humidity (Yang et al ., 2011) (or an optimal combination of mild temperature and humidity (Kluge et al ., 2006). Compared to ground-living fern and fern allies, epiphytic species strongly rely on water air in the closed-canopy (Kreft et al ., 2010). In this study, ground-living fern and fern allies did not display a different water requirement. Instead, both of them performed similar positive correlations to the water condition. It turns out that 1980 individuals (98%) were growing well in humid transects, i.e., A, B, D, and F (A, D, F benifited from river flow, while transect B benifited from inner cycling precipitation), whereas 36 individuals (2%) lived in dry transects. Considering transect B, the plot at the bottom preserved 54 individuals of 3 species. It increased to 364 individuals of 19 species at the top plot, almost seven times of the bottom. Plots in low altitude were occupied mainly by worldwide species such as Pteris vittata andAdiantum malesianum . However, it was altered to uncommonly seen species when the altitude went up, where the dominant species wereSinephropteris delavayi and Phymatosorus cuspidatus . The reason was ascribed to inner cycling precipitation at high altitude.
4.3. Heterogeneous habitat and fern and fern allies distribution
Generally, to maintain plants growing and population size, fern and fern allies have to absorb more water from the circumstance surroundings, e.g., Pteris vittata, Lygodium japonicum, and Microlepia speluncae . However, other species, such as SelaginellaS delicatula , S. uncinata , Adiantum capillus-veneris , andA. malesianum , survive in a unique approach, e.g ., slender plant size and vegetative reproduction by rhizomes. Their rarity in the plots is ascribed to frequent hot and dry air and habitat deterioration such as substance rocks fragmentation and surface soil erosion. It becomes worse in recent decades and has resulted in a dramatically declined environment. Reproductive organisms, e.g., spores, gemmae, and slender rhizomes, suffer and regeneration cannot proceed under such environmental stress. Habitat determines which plants grow, while environmental factors define a habitat. According to the habitat heterogeneity hypothesis (Tuanmu & Jetz, 2015; Hamm & Drossel, 2017), the living requirement differs in species, and each species has their living requirements exclusively. Their requirements include living substances, water, temperature, and nutrition, to name a few. A complicated and diverse habitat supports more species while a unitary habitat supports less. Diversity increases in more heterogeneous habitats (Negrão et al ., 2017). For an arid ecosystem, disturbances with varying intensities and spatial scales are responsible for habitat patterns (Torimaru et al ., 2018). As regards the fern and fern allies distribution in Yunnan, China, heterogeneity was reported to be critical to the diversity of species and to be related to biogeographic zonation (Zhang et al ., 2017). In Yuanjiang dry-hot valley, Bray-Curtis index revealed that transects C and E were unitary habitats, while transects A, B, D, and F were more complicated and diverse. In the field survey, only three species were recorded in the unitary transects C and E, whereas 33 species were found in heterogeneous transects A, B, D, and F (Supplementary data: Table B). A Topographic variation on altitudinal and latitudinal gradients and divergent temperature and water condition generated a mosaic microclimate on the slopes in the valley.
4.4. Fern and fern allies indicators
Indicator species are correlated to specific environmental factors. The population sizes usually increase or decrease due to the change of one or several factors. Their presence or absence is mostly determined by an environmental factor. They are optimal to indicate the environmental evolution process regarding their diverse habitat requirements in species (Karst et al ., 2005; Yang & Grote, 2018; Yang et al ., 2019). Most fern and fern allies are strictly limited in their habitats because of their intrinsic sensitivity to environmental change. For example, Gonocormus minutus live on water due to their fragile mesophyll tissue, whileSelaginella tamariscina can resist extreme arid at Yang tribute due to its resuscitation, etc. They are considered key indicators of the environment (Silva et al ., 2018).
In this study, screened indicators fit well with the hot-dry or hot-wet environment (Table 4). Three species were worldwide distributed with broad ecological amplitude, i.e., Pteris vittata , Lygodium japonicum , and Adiantum malesianum .
However, five other species were limited in distribution and confined to narrow amplitude, i.e., Selaginella pseudopaleifera , S. jugorum , Sinephropteris delavayi , Davallia trichomanoides , and Aleuritopteris squamosa . Although growing in different river segments from upper to lower, they all occurred in relatively humid areas and disappeared in hot and dry places. Similar results revealed the indicator function in these selected genera, e.g., endemic species of genus Selaginella in Philippine are recognised as indicators of refuge in the geological past (Tan, 2013) andDavallia mariesii is used as an indicator of landforms and vegetation types (Park et al ., 2019). A. squamosa is endemic in the upper and middle segment of Yuanjiang-Red River, which strongly associates to dry-hot climate (Wu, 1981). Meanwhile, a cryptic species A. argentea , is reported as a pyrophytic species andSinephropteris is monotypic confined to karst in southwest China, northeast India, and north Burma (Pallvi et al ., 2019).
5. Conclusions
In recent years, climate change is broadly focused, while environmental disasters have occurred frequently. Significant land degradation and climate events have been reported for more than decades. Plants are considered as a serious part of environmental change. In response to such ecological crises, this research demonstrates such changes in Yuanjiang valley located in the first half part of a river shared by China and Vietnam by focusing on fern and fern allies affected by other environmental factors. From bottom to top of the mountain, precipitation increased while the temperature decreased. Fern and fern allies are positively correlated with height as a result of atmospheric conditions. Species richness increases further accompanied habitat heterogeneity in the valley. Even with no influence of human disturbance, these current appearances are not the original pattern of the areas, indicating another consequence of climate change.
Acknowledgement: This research is supported by the Research Foundation for Advanced Talents of Yibin Vocational and Technical College (No. ybzysc20bk03), the Innovation Project of the Department of Education of Guangdong Province, China (No. 2019KTSCX71), Scientific Research Platform of Yibin Vocational and Technical College (No. ybzy21kypt05), Project of Science and Technology Innovation Team (No. ybzy21cxtd-04) and Yi Minority Culture Research Center of the Key Research Base of Philosophy and Social Sciences of Sichuan Province (No. YZWH2101). The authors would like to thank Ms. Hong Anh Thi Nguyen for general assistance and also acknowledge Faculty of Environment and Resource studies, Mahidol University’s editing service for support in the improvement of this manuscript.
Data Accessibility: All sampling data are online available with https://doi.org/10.5061/dryad.k0p2ngf8h.
References
Abotsi, K. E., Bose, R., Adjossou, K., Deblauwe ,V., Rouhan, G., Segla, K. N., Atsri, K. H., & Kokou, K. (2020). Ecological drivers of pteridophyte diversity and distribution in Togo (West Africa).Ecological Indicators, 108, 105741. DOI: 10.1016/j.ecolind.2019.105741
Andersen, A. N., Del Toro, I., & Parr, C. L. (2015). Savanna ant species richness is maintained along a bioclimatic gradient of increasing latitude and decreasing rainfall in northern Australia.Journal of Biogeography, 42(12), 2313-2322. DOI: 10.1111/jbi.12599
Baselga, A. (2017). Partitioning abundance‐based multiple‐site dissimilarity into components: Balanced variation in abundance and abundance gradients. Methods in Ecology and Evolution , 8(7), 799-808.
Brock, J. M., Perry, G. L., Lee, W. G., & Burns, B. R. (2016). Tree fern ecology in New Zealand: A model for southern temperate rainforests.Forest Ecology and Management, 375, 112-126. DOI: 10.1016/j.foreco.2016.05.030
Cáceres, M., Legendre, P. (2009). Associations between species and groups of sites: Indices and statistical inference. Ecology, 90,3566–3574. DOI: 10.1890/08-1823.1
Chao, A. (1984). Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics, 11, 265-270.
Chao, A. (1987). Estimating the population size for capture-recapture data with unequal catchability. Biometrics, 43, 783-791. DOI: 10.2307/2531532
Chao, A. & Chiu, C.H. (2016) Bridging two major approaches (the variance framework and diversity decomposition) to beta diversity and related similarity and differentiation measures. Methods in Ecology and Evolution , 8, 919-928.
Chao, A., Colwell, R. K., Chiu, C. H., & Townsend, D. (2017). Seen once or more than once: Applying Good–Turing theory to estimate species richness using only unique observations and a species list.Methods in Ecology and Evolution, 8(10), 1221-1232. DOI: 10.1111/2041-210X.12768
Colwell, R.K. (2019, April 4). EstimateS: Statistical Estimation of Species Richness and Shared Species from Samples. Version 9.1. [Software]. Retrieved from http://viceroy.eeb.uconn.edu/estimates/EstimateSPages/AboutEstimateS.htm.
Diserud, O.H. & Ødegaard, F. (2007) A multiple‐site similarity measure.Biology Letters , 3, 20-22.
Dong, Y., Xiong, D., Su, Z. A., Li, J., Yang, D., Shi, L., & Liu, G. (2014). The distribution of and factors influencing the vegetation in a gully in the Dry-hot Valley of southwest China. Catena,116, 60-67. DOI: 10.1016/j.catena.2013.12.009
Girardello, M., Chapman, A., Dennis, R., Kaila, L., Borges, P. A., & Santangeli, A. (2019). Gaps in butterfly inventory data: A global analysis. Biological Conservation, 236, 289-295. DOI: 10.1016/j.biocon.2019.05.053
Giovannini, L., Laiti, L., Serafin, S., & Zardi, D. (2017). The thermally driven diurnal wind system of the Adige Valley in the Italian Alps. Quarterly Journal of the Royal Meteorological Society ,143(707), 2389-2402. DOI: 10.1002/qj.3092
GMS Operations Center. (2017). Greater Mekong Subregion Atlas of the Environment (2nd Edition). derived online: http://portal.gms-eoc.org
Hamm, M., & Drossel, B. (2017). Habitat heterogeneity hypothesis and edge effects in model metacommunities. Journal of theoretical biology, 426, 40-48. DOI: 10.1016/j.jtbi.2017.05.022
Hea, Z, Dua, J., Chena, L., Zhua, X., Lina, P., Zhao, M., Fan, S. (2018). Impacts of recent climate extremes on spring phenology in arid-mountain ecosystems in China. Agricultural and Forest Meteorology, 260-261, 31-40. DOI: 10.1016/j.agrformet.2018.05.022
Hernández-Rojas, A., Kessler, M., Krömer, T., Carvajal-Hernández, C., Weigand, A., & Kluge, J. (2018). Richness Patterns of Ferns Along an Elevational Gradient in the Sierra de Juárez, Oaxaca, Mexico: a Comparison with Central and South America. American Fern Journal ,108 (3), 76-95. DOI: 10.1640/0002-8444-108.3.76
Jina, J., Wang, Q., Wanga, J., & Otienoc D. (2019). Tracing water and energy fluxes and reflectance in an arid ecosystem using the integrated model SCOPE. Journal of Environmental Management , 231, 1082-1090. DOI: 10.1016/j.jenvman.2018.10.090
Karst, J., Gilbert, B., & Lechowicz, M. J. (2005). Fern community assembly: the roles of chance and the environment at local and intermediate scales. Ecology, 86(9), 2473-2486. DOI: 10.1890/04-1420
Kessler, M., Parris, B. S., & Kessler, E. (2001). A comparison of the tropical montane pteridophyte floras of Mount Kinabalu, Borneo, and Parque Nacional Carrasco, Bolivia. Journal of Biogeography, 28(5), 611-622. DOI: 10.1046/j.1365-2699.2001.00577.x
Kessler, M., Kluge, J., Hemp, A., & Ohlemüller, R. (2011). A global comparative analysis of elevational species richness patterns of ferns.Global Ecology and Biogeography, 20(6), 868-880. DOI: 10.1111/j.1466-8238.2011.00653.x
Kluge, J., Kessler, M., & Dunn, R. R. (2006). What drives elevational patterns of diversity? A test of geometric constraints, climate and species pool effects for pteridophytes on an elevational gradient in Costa Rica. Global Ecology and Biogeography, 15(4), 358-371. DOI: 10.1111/j.1466-822X.2006.00223.x
Kreft, H., Jetz, W., Mutke, J., & Barthlott, W. (2010). Contrasting environmental and regional effects on global pteridophyte and seed plant diversity. Ecography, 33(2), 408-419. DOI: 10.1111/j.1600-0587.2010.06434.x
Magurran, A. E. (2004). Measuring biological diversity . Blackwell, New York.
Negrão, R., Sampaio-e-Silva, T., Kortz, A. R., Magurran, A., & Matos, D. M. S. (2017). An endangered tree fern increases beta-diversity at a fine scale in the Atlantic Forest Ecosystem. Flora , 234 , 1-6. DOI: 10.1016/j.flora.2017.05.020
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., O’Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., & Wagner, H. (2011). vegan: Community Ecology Package. R Package Version 1.17-8. [Software]. Retrieved from http://CRAN.R-project.org/package=vegan.
Pallvi, S., Chander, D. H., & Bikarma, S. (2019). Four pyrophytic pteridophytes in the Chir pine forest of Kalidhar forest range in Shiwaliks of North West Himalaya in Indian Himalayan region.Environment Conservation Journal , 20 (3), 73-77. DOI: 10.36953/ECJ.2019.20310.
Park, B. J., Byeon, J. G., & Cheon, K. I. (2019). Study of Ecological Niche and Indicator Species by Landforms and Altitude of Forest Vegetation in Mt. Myeonbong. Korean Journal of Plant Resources, 32(4), 325-337. DOI: 10.7732/kjpr.2019.32.4.325.
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & the R Development Core Team. (2011) nlme: Linear and Nonlinear Mixed Effects Models. R Package Version 3.1-98. [Software]. Retrieved from http://web.mit.edu/~r/current/arch/i386_linux26/lib/R/library/nlme/html/lme.html
R Development Core Team. (2012). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Rajakaruna, H., Drake, D. A. R., T. Chan, F., & Bailey, S. A. (2016). Optimizing performance of nonparametric species richness estimators under constrained sampling. Ecology and evolution, 6(20),7311-7322. DOI: 10.1002/ece3.2463
Ricotta, C., & Podani, J. (2017). On some properties of the Bray-Curtis dissimilarity and their ecological meaning. Ecological complexity , 31, 201-205.
Roberts, D.W. (2018, November 9). Ordination and Multivariate Analysis for Ecology [Software]. Retrieved from http://ecology.msu.montana.edu/labdsv/R
Salazar, L., Homeier, J., Kessler, M., Abrahamczyk, S., Lehnert, M., Krömer, T., & Kluge, J. (2015). Diversity patterns of ferns along elevational gradients in Andean tropical forests. Plant Ecology & Diversity, 8(1), 13-24. DOI: 10.1080/17550874.2013.843036
Shapiro, S. S., & Wilk, M.B. (1965). An analysis of variance test for normality (complete samples), Biometrika, 52, 591–611. DOI: 10.2307/2333709
Silva, V. L., Mehltreter, K., & Schmitt, J. L. (2018). Ferns as potential ecological indicators of edge effects in two types of Mexican forests. Ecological Indicators, 93, 669-676.
Srivastava, P., Singh, R., Tripathi, S., Singh, H., & Raghubanshi, A. (2018). Understanding the complex interaction between soil N availability and soil C dynamics under changing climate conditions.Soil Management and Climate Change, 20, 337–348. DOI: 10.1016/B978-0-12-812128-3.00022-7
Su, Z., Xiong, D., Dong, Y., Zhang, B., Zhang, S., Zheng, X., & Fang, H. (2015). Hydraulic properties of concentrated flow of a bank gully in the dry‐hot valley region of southwest China. Earth Surface Processes and Landforms, 40(10), 1351-1363. DOI: 10.1002/esp.3724
Szewczyk, T. M., & McCain, C. M. (2019). Disentangling elevational richness: a multi‐scale hierarchical Bayesian occupancy model of Colorado ant communities. Ecography, 42(5), 977-988. DOI: 10.1111/ecog.04115
Tan, B. C. (2013). The Selaginella Flora, A Good Indicator of the Philippine Pleistocene Island Groups. Philippine Journal of Science , 142: 211-213.
Torimaru, T., Akada, S., Ishida, K., Narita, M., & Higaki, D. (2018). Species habitat associations in an old-growth beech forest community organised by landslide disturbances. Journal of Forest Research ,23(2), 98-104. DOI: 10.1080/13416979.2017.1396418
Tuanmu, M. N., & Jetz, W. (2015). A global, remote sensing‐based characterization of terrestrial habitat heterogeneity for biodiversity and ecosystem modelling. Global Ecology and Biogeography, 24(11),1329-1339. DOI: 10.1111/geb.12365
Wang, H. (2008). The Floristic composition and vertical distribution patterns of Pteridophytes in Mt. Fanjingshan Nature Reserve . Matser Dissertation, Guizhou University. (in Chinese with English abstract)
Wang, X., Zhao, L., Yan, B., Shi, L., Liu, G., & He, Y. (2016). Morphological and physiological responses ofHeteropogon contortus to drought stress in a dry-hot valley.Botanical Studies, 57, 17.
Wu S. K. (1981). A study of the genus Aleuritopteris Fée in China. Journal of Systematics and Evolution , 19 (1), 57-74.
Wu, Z. Y. (2006). Flora Yunnanica (Volumes 20, 21). Science Press, Beijing.
Xu, Z. F., Tao, G. H., Yu, P. H., & Wang, Y. L. (1985). An approach to the vegetational changes from yuanjiang dry-hot valley of yunnan in the last 500 years. Acta Botanica Yunnanica, 7(4), 403-412. (in Chinese with English abstract)
Yang, F. C., Li, D. F., & Huang, H. P. (2018). Pteridophytes of Thailand . Nanhai Publishing House, Haikou.
Yang F. C. & Grote P. J. (2018). Riverine vegetation and environments of a Late Pleistocene river terrace, Khorat Plateau, Southeast Asia.Palynology, 42 (2), 158–167. DOI: 10.1080/01916122.2017.1296044
Yang F. C., Grote P. J. & Zhang S. T. (2019). The evolution of Mun River in Southeast Asia, and its relationship with the environmental changes in the late Middle Pleistocene, based on sedimentologic and palynological evidences. Quaternary International, 519, 50–57. DOI: 10.1016/j.quaint.2019.02.010
Yang, F. C., Zhang, C. L., Wu, G., Liang, S. Y., & Zhang, X. C. (2011). Endangered pteridophytes and their distribution in Hainan Island, China.American Fern Journal , 101 (2), 105-117. DOI: 10.1640/0002-8444-101.2.105
Zhang, B., Shi, K., Liu, C. Q., Ai, N. S., Liu, G. C., & Qin, F. C. (2009). Changes of Seasonal Precipitation of Yuanmou Dry-hot Valley in Recent 50 Years Based on method of DFA. Scientia Geographica Sinica , 4.
Zhang, L. L, Xu, C. D., & Feng, J. M. (2017). Biogeographical explanation of distribution pattern of fern diversity in Yunnan province. Journal of Chuxiong Normal University, 32(3), 45-50. (in Chinese with English abstract)