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Below-Ground Determinants and Ecological Implications of Shrub Species' Degree of Isohydry in Subtropical Pine Plantations

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Below-Ground Determinants and Ecological Implications of Shrub Species' Degree of Isohydry in Subtropical Pine Plantations Full Paper Below-ground determinants and ecological implications of shrub species’ degree of isohydry in subtropical pine plantations Peipei Jiang1,2, Frederick C. Meinzer3 , Huimin Wang1,2, Liang Kou1,2 , Xiaoqin Dai1,2 and Xiaoli Fu1,2 1Qianyanzhou Ecological Research Station, Key Laboratory of Ecosystem Network Observation and Modelling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China; 2College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100190, China; 3USDA Forest Service, Pacific Northwest Research Station, 3200 SW Jefferson Way, Corvallis, OR 97331, USA Printed by[NationalForestServiceLib-170.144.252.182/doi/epdf/10.1 Summary Author for correspondence: The degree of plant iso/anisohydry is a popular framework for characterising species-speci- Xiaoli Fu fic drought responses. However, we know little about associations between below-ground Tel: +86 10 64889913 and above-ground hydraulic traits as well as the broader ecological implications of this frame- Email: [email protected] work. Received: 29 November 2019 For 24 understory shrub species in seasonally dry subtropical coniferous plantations, we Accepted: 16 February 2020 investigated contributions of the degree of isohydry to species’ resource economy strategies, abundance, and importance value, and quantified the hydraulic conductance (Kh) of above- New Phytologist (2020) 226: 1656–1666 ground and below-ground organs, magnitude of deep water acquisition (WAdeep), shallow doi: 10.1111/nph.16502 absorptive root traits (diameter, specific root length, tissue density), and resource-use efficien- cies (Amax, maximum photosynthesis rate; PNUE, photosynthetic nitrogen-use efficiency). Key words: deep soil water uptake, hydraulic The extreme isohydric understory species had lower wood density (a proxy for higher conductance, resource-use efficiency, growth rates) because their higher WAdeep and whole-plant Kh allowed higher Amax and shallow absorptive root, water storage. PNUE, and thus did not necessarily show lower abundance and importance values. Although 1 species’ Kh was coordinated with their water foraging capacity in shallow soil, the more 1 1/nph.16502] at[23/06/2021]. acquisitive deep roots were more crucial than shallow roots in shaping species’ extreme isohy- dric behaviour. Our results provide new insights into the mechanisms through which below-ground hydraulic traits, especially those of deep roots, determine species’ degree of isohydry and eco- nomic strategies. Introduction the concept is applied either to a single species across environ- mental gradients or different species under similar environmental Under current global change scenarios, the adaptability of differ- conditions (Ratzmann et al., 2019; Novick et al., 2019). Never- ent species to drought will determine the structure and function theless, important knowledge gaps persist conc erning the broad of plant communities (Thuiller et al., 2008; Tylianakis et al, applicability of this framework and how plant functional traits 2008; Anderegg et al., 2012). A continuum of isohydric to aniso- are integrated to yield a given degree of iso/anisohydry. hydric behaviour provides a framework for characterising whole- One knowledge gap concerns the utility of the iso/anisohydry plant, species-specific differences in the stringency of stomatal framework for understanding species-specific economic strategies control of transpiration and thus leaf water potential during and community assembly processes. Over the past decade, drought (Klein, 2014; Martınez-Vilalta et al., 2014; Meinzer research on iso/ani sohydry directed towards how well this frame- et al., 2016; Ratzmann et al., 2019). Generally, isohydric species work predict s species’ vulnerability to drought-induced mortality maintain a relatively constant midday minimum leaf water has yielded conflicting results (McDowell et al., 2008, 2011; Ψ Ψ potential ( md) despite changes in soil water potential ( S), Kumagai & Porporato, 2012; Gu et al., 2015; Martınez-Vilalta Ψ whereas md of anisohydric species covaries more strongly with & Garcia-Forner, 2017). The inconsistent results may reflect Ψ S (Meinzer et al., 2016, 2017; Hochberg et al., 2018). It is diffi- incompatible, coexisting definitions or misconceptions of iso/ cult to scale such species-specific iso/anisohydric behaviour to the anisohydry or may indicate that application of the framework ecosystem scale (Konings & Gentine, 2017), as coexisting plants should be restricted to studyi ng relationships among hydraulic can exhibit different hydraulic behaviour and degrees of isohydry strategies, and drought-induced hydraulic damage and recovery (Quero et al., 2011; Roman et al., 2015). However, the relative processes under nonle thal water stress conditions (Volaire, 2018; degree of iso/anisohydry could reflect interspecific or intraspecific Kannenberg et al., 2019). Based on the plant economic spectrum differences in the ability to adjust to different environments when theory, species with lower wood density have faster growth rates 1656 New Phytologist (2020) 226: 1656–1666 2020 The Authors www.newphytologist.com New Phytologist 2020 New Phytologist Trust New Phytologist Research 1657 and ‘fast’ resource acquisition strategies, which would dominate and less reliance on mycorrhizae, which can benefit plants coping in environments with minimal resource constraints, whereas with less predictable environments (e.g. seasonal drought) species with ‘slow’ resource acquisition strategies would eventu- through rapid root growth (Ma et al., 2018). Studies have shown ally dominate when resources are scarc e (Reich, 2014). A recent that specie s with a large shallow root biomass have greater ability global meta-analysis showed that species with higher wood den- to maintain leaf water potential in drying soil (Houssard et al., sity were less isohydric (Fu & Meinzer, 2019), leading to our first 1992; Liu et al., 20 15a), and a recent modelling exercise con- hypothesis that less isohydric species may grow slowly and even- cluded that root hydraulic properties exerted a greater influence tually dominate under conditions of lower resource availability, on whole-plant hydraulic function than branch hydraulic proper- which to our knowledge has never been tested within understory ties (McCulloh et al., 2019). Based on the preceding findings and vegetation communities where light is low. observations, our second hypothesis is that the degree of isohydry Another knowledge gap concerns the associations between of coexisting species may be partly determined by coordination Printed by[NationalForestServiceLib-170.144.252.182/doi/epdf/10.1 below-ground and above-ground hydraulic traits that determine between their ability to utilise deep and shallow soil water, and a species’ degree of iso/anisohydry. Studies have shown that root system hydraulic conductance. where species operate along the isohydric to anisohydric contin- To test the first hypothesis, we quantified the degree of iso- uum results from the integration of properties of different plant hydry for 24 understory woody shrub species with a wide range organs (Fu et al., 2019; Li et al., 2019; Mirfenderesgi et al., of wood density in subtropical coniferous plantations with a 2019). At the leaf level, more isohydric species tend to have less marked dry season (Yang et al., 2015). We then examined the Ψ negative turgor loss point ( TLP), slower kinetics of stomatal association of the degree of isohydry with species’ wood density opening and activation of photosynthesis, but higher intrinsic and abundance. To test the second hypothesis, we inve stigated water-use efficiency and are more likely to exhibit drought-in- the linkage between species’ water transport efficiency with duced leaf shedding (Meinzer et al., 2017; Fu & Meinzer, 2019; below-ground water uptake, and then examined the roles of water Li et al., 2019). At the stem level, more isohydric species tend to transport efficiency and root water uptake in determining species’ have higher hydraulic capacitance, conductivity and safety mar- degree of iso/anisohydry. gins, but lower wood density and xylem resistance to embolism (Klein, 2014; Martınez-Vilalta et al., 2014; Fu et al., 2019; Mir- Materials and Methods fenderesgi et al., 2019). Importantly, plant hydraulic properties could be inversely related across different organs. For example, Site description 1 Fu et al. (2019) found that there was a trade-off between 1 1/nph.16502] at[23/06/2021]. hydraulic storage and efficiency in the leaf, but coordination This study was conducted at the Qianyanzhou Ecological Station between hydraulic storage and efficiency in the stem along a spec- of the Chinese Academy of Sciences, located in a typical hilly trum of plant iso/anisohydry. The studies cited above have largely red-soil region of subtropical China, which is strongly influenced focused on the contributions of above-ground functional by the subtropical Eastern-Asian monsoon climate. Due to the attributes to the degree of species’ isohydry; as a res ult, little unevenly distributed rainfall, seasonal droug hts frequently occur information is known about how below-ground hydraulic from July to October in this region (Yang et al., 2015). The mean attributes shape the degree of isohydry. annual temperature and precipitation are 18.0°C and It was believed that species with deeper root systems would 1509.0 mm, respectively. The soil is an iron-rich red soil classi- have greater ability
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