View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Kyoto University Research Information Repository Leaf trait variations associated with habitat affinity of tropical Title karst tree species Geekiyanage, Nalaka; Goodale, Uromi Manage; Cao, Kunfang; Author(s) Kitajima, Kaoru Citation Ecology and Evolution (2018), 8(1): 286-295 Issue Date 2018-01 URL http://hdl.handle.net/2433/230804 © 2017 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. This is an open access article under the Right terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Type Journal Article Textversion publisher Kyoto University Received: 27 June 2017 | Revised: 3 September 2017 | Accepted: 16 September 2017 DOI: 10.1002/ece3.3611 ORIGINAL RESEARCH Leaf trait variations associated with habitat affinity of tropical karst tree species Nalaka Geekiyanage1,2,3 | Uromi Manage Goodale3,4 | Kunfang Cao3,4 | Kaoru Kitajima1,5 1Division of Forest and Biomaterial Science, Graduate School of Agriculture, Kyoto Abstract University, Kyoto, Japan Karst hills, that is, jagged topography created by dissolution of limestone and other 2 Department of Plant Science, Faculty soluble rocks, are distributed extensively in tropical forest regions, including southern of Agriculture, Rajarata University, Anuradhapura, Sri Lanka parts of China. They are characterized by a sharp mosaic of water and nutrient avail- 3Plant Ecophysiology and Evolution ability, from exposed hilltops with poor soil development to valleys with occasional Group, Guangxi Key Laboratory for Forest flooding, to which trees show species- specific distributions. Here we report the rela- Ecology and Conservation, College of Forestry, Guangxi University, Nanning, tionship of leaf functional traits to habitat preference of tropical karst trees. We de- Guangxi, China scribed leaf traits of 19 tropical tree species in a seasonal karst rainforest in Guangxi 4State Key Laboratory for Conservation and Utilization of Subtropical Agro- Province, China, 12 species in situ and 13 ex situ in a non-karst arboretum, which Bioresources, Guangxi University, Nanning, served as a common garden, with six species sampled in both. We examined how the Guangxi, China measured leaf traits differed in relation to species’ habitat affinity and evaluated trait 5Smithsonian Tropical Research Institute, Balboa, Republic of Panama consistency between natural habitats vs. the arboretum. Leaf mass per area (LMA) and optical traits (light absorption and reflectance characteristics between 400 and Correspondence Nalaka Geekiyanage and Uromi Manage 1,050 nm) showed significant associations with each other and habitats, with hilltop Goodale, Division of Forest and Biomaterial species showing high values of LMA and low values of photochemical reflectance Science, Graduate School of Agriculture, KyotoUniversity, Kyoto, Japan index (PRI). For the six species sampled in both the karst forest and the arboretum, Emails: [email protected] LMA, leaf dry matter content, stomatal density, and vein length per area showed in- and [email protected] consistent within- species variations, whereas some traits (stomatal pore index and Funding information lamina thickness) were similar between the two sites. In conclusion, trees specialized Arnold Arboretum of Harvard University, Grant/Award Number: Ashton Award for in exposed karst hilltops with little soils are characterized by thick leaves with high Student Research; Guangxi University Invited tissue density indicative of conservative resources use, and this trait syndrome could Expert Special Project; National Natural Science Foundation of China, Grant/Award potentially be sensed remotely with PRI. Number: 31660125 KEYWORDS edaphic habitats, lamina thickness, leaf mass per area, photochemical reflectance index, stomatal density, stomatal pore index, trait plasticity, vein length per area 1 | INTRODUCTION Phillips, Vargas, & Monteagudo, 2003). Many tree species exhibit strong habitat affinity to topography, elevation, and/or water and The spatial distribution patterns of tree species with respect to en- nutrient availability (Gunatilleke et al., 2006; Guo et al., 2017; Itoh vironmental heterogeneity are a central theme in tropical forest et al., 2003). Such specializations occur at various spatial scales in community ecology (Condit et al., 2000; Kitajima & Poorter, 2008; response to edaphic habitats created by the interaction of bedrock This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2017 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 286 | www.ecolevol.org Ecology and Evolution. 2018;8:286–295. GEEKIYANAGE ET AL. | 287 with geomorphic factors and climate. Karst landscapes create par- only in their natural habitats. Common garden experiments are ticularly complex habitat mosaics full of fissures, conduits, sink- useful in teasing apart whether an apparent association of certain holes, and steep terrains, because limestone is prone to dissolution. species traits with their natural habitats is due to habitat filtering of Consequently, karst forests exhibit fine- scale heterogeneity of hydro- species or plastic responses (Cordell, Goldstein, Mueller- Dombois, geology, topography, and associated water availability, to which tree Webb, & Vitousek, 1998). For tree species, an arboretum where species may specialize (Bonacci, Pipan, & Culver, 2008; Guo et al., trees were grown on a common soil and receive adequate supply of 2017; Schindler, 1982). water and nutrients may serve as a common garden in which leaf Identification of traits associated with edaphic habitat specializa- traits may be evaluated under a standardized favorable condition. tion, such as seen in tropical karst forests, may promote a mechanis- Karst forests occupy 7%–15% of the global terrestrial landmass tic understanding of the community assembly process and ecosystem (Fu et al., 2012; Hartmann et al. 2014). In an extensive karst forest functioning. Kraft and Ackerly (2010) demonstrated how leaf mass zone in southwestern China, ranging from Yunnan to Guangxi, recent per area (LMA) and leaf nitrogen concentrations are associated with studies report affinities of tree species to various topographic posi- topography in a lowland Amazonian forest in an evolutionarily con- tions (Guo et al., 2017; Zhang, Hu, Zhu, Luo, & Ni, 2010). Steep to- vergent manner. Tree species adapted to different habitat types pography and percolation of water through the bedrock accompanied within a karst landscape may exhibit trait variations reflecting adap- by nutrient leaching and soil erosion creates a gradient of water and tation to differences in supply regimes of water, nutrients, and light nutrient availability from mountain hilltops to foothills, leading to drier among these habitats. As a key axis in the leaf economic spectrum and nutrient- poor conditions in hilltops and mid- slopes compared (Wright et al., 2004), LMA values exhibit negative associations with to foothills. The karst valleys are not necessarily resource- rich habi- inherent growth rates and soil resource availability, of which environ- tats due to prolonged inundation and soil anoxia in the rainy season mental heterogeneity explains around 36% of the variation (Poorter, (Bonacci et al., 2008; Guo et al., 2017; Schindler, 1982). Among the Niinemets, Poorter, & Wright, 2009). Long leaf lifespan, which is pos- four topographical habitats we discussed above, foothills perhaps rep- itively associated with LMA, is adaptive in infertile soils as it reduces resent the most favorable in terms of water and nutrient availabilities the nutrient turnover rates (conservative ecological strategy: Westoby, for plant growth (Guo et al., 2015; Huang et al., 2014). However, po- Falster, & Moles, 2002). tential associations of leaf traits in karst tree species to their habitat Optically detectable traits (hereafter optical traits) and ana- affinities are yet to be characterized. tomical traits may exhibit functional adaptation specific to indi- Here, we report a comparative study of leaf traits among karst vidual environmental stress factors. Recent advances in visible to tree species growing in their natural habitats and in an arboretum in near- infrared range (400–1,050 nm) spectroscopy allow estimation Guangxi Province, China. We selected 19 karst tree species known to of LMA, concentrations of nitrogen and photosynthetic pigments, show habitat affinity to four topographic positions (i.e., hilltop, mid- and water content from spectral reflectance at both leaf and can- slope, foothill, and valley). Twelve were common species in Nonggang opy levels (Asner et al., 2011; Doughty, Asner, & Martin, 2010). National Nature Reserve (hereafter the karst forest), and 13 were Photochemical Reflectance Index (PRI: Gamon, Peñuelas, & Field, growing in an arboretum in Nanning, Guangxi. Of these, only six spe- 1992) in particular is significant as an indicator of the degree of cies affiliated to valley and foothill habitats were sampled at both sites. protection from excess radiation with xanthophyll cycle pigments. We measured 13 leaf traits to test the following hypotheses: (1) spe- Plant adaptations to contrasting water regimes may be reflected in cies affiliated to resource-