ORIGINAL RESEARCH published: 23 July 2015 doi: 10.3389/fpls.2015.00511 Functional traits variation explains the distribution of Aextoxicon punctatum (Aextoxicaceae) in pronounced moisture gradients within fog-dependent forest fragments Edited by: Judy Simon, Beatriz Salgado-Negret1,2*, Rafaella Canessa2, Fernando Valladares3,JuanJ.Armesto2,4 University of Konstanz, Germany and Fernanda Pérez2,4* Reviewed by: Martin Karl-Friedrich Bader, 1 Instituto Humboldt, Bogotá, Colombia, 2 Departamento de Ecología, Pontificia Universidad Católica de Chile, Santiago, New Zealand Forest Research Chile, 3 LINCGlobal, Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Cientificas, Madrid, Spain, Institute (Scion), New Zealand 4 Instituto de Ecología y Biodiversidad, Santiago, Chile Ignacio García-González, Universidade de Santiago de Compostela, Spain Climate change and fragmentation are major threats to world forests. Understanding *Correspondence: how functional traits related to drought tolerance change across small-scale, Beatriz Salgado-Negret, pronounced moisture gradients in fragmented forests is important to predict species’ Instituto Humboldt, Calle 28A #15-09, responses to these threats. In the case of Aextoxicon punctatum, a dominant canopy Bogotá, Colombia [email protected]; tree in fog-dependent rain forest patches in semiarid Chile, we explored how the Fernanda Pérez, magnitude, variability and correlation patterns of leaf and xylem vessel traits and Departamento de Ecología, Pontificia Universidad Católica de Chile, hydraulic conductivity varied across soil moisture (SM) gradients established within and Alameda 340, Santiago, Chile among forest patches of different size, which are associated with differences in tree [email protected] establishment and mortality patterns. Leaf traits varied across soil-moisture gradients Specialty section: produced by fog interception. Trees growing at drier leeward edges showed higher This article was submitted to leaf mass per area, trichome and stomatal density than trees from the wetter core Functional Plant Ecology, a section of the journal and windward zones. In contrast, xylem vessel traits (vessels diameter and density) Frontiers in Plant Science did not vary producing loss of hydraulic conductivity at drier leeward edges. We also Received: 14 March 2015 detected higher levels of phenotypic integration and variability at leeward edges. The Accepted: 25 June 2015 ability of A. punctatum to modify leaf traits in response to differences in SM availability Published: 23 July 2015 established over short distances (<500 m) facilitates its persistence in contrasting Citation: Salgado-Negret B, Canessa R, microhabitats within forest patches. However, xylem anatomy showed limited plasticity, Valladares F, Armesto JJ and Pérez F which increases cavitation risk at leeward edges. Greater patch fragmentation, together (2015) Functional traits variation explains the distribution of Aextoxicon with fluctuations in irradiance and SM in small patches, could result in higher risk of punctatum (Aextoxicaceae) drought-related tree mortality, with profound impacts on hydrological balances at the in pronounced moisture gradients ecosystem scale. within fog-dependent forest fragments. Front. Plant Sci. 6:511. Keywords: climate change, fog-dependent forest, fragmentation, hydraulic traits, intraspecific phenotypic doi: 10.3389/fpls.2015.00511 variability, leaf traits, moisture gradient, phenotypic integration Frontiers in Plant Science | www.frontiersin.org 1 July 2015 | Volume 6 | Article 511 Salgado-Negret et al. Functional traits variation of Aextoxicon punctatum Introduction South American endemic Aextoxicon punctatum Ruiz and Pav, belonging to the monotypic and isolated family Aextoxicaceae. Reductions in precipitation expected under climate change and This species is broadly distributed in temperate rain forests of increasing forest fragmentation are major threats to temperate western South America. In Fray Jorge, it occurs in forest patches forests worldwide (Breshears et al., 2005; Echeverría et al., 2006; of all sizes and throughout the soil moisture (SM) gradient Choat et al., 2012). Particularly sensitive are forests located in the produced by fog influx from windward to leeward edges (del- boundary with drier formations, where drought intensification Val et al., 2006). Moreover, population genetic studies suggest may be fundamentally important for the persistence of forest that gene flow via seed dispersal across neighboring patches in communities (Pockman and Sperry, 2000; Engelbrecht et al., this patchy landscape has been highly significant (Fst < 0.05) 2007; Choat et al., 2012; Salgado-Negret et al., 2013). As during recent history (Nuñez-Ávila et al., 2013). Patterns of tree a consequence, improved understanding of functional trait radial growth and regeneration dynamics of A. punctatum in this variation in relation to drought tolerance becomes critical for forest have shown constant growth and continuous regeneration modeling and predicting tree species responses to future climate for 200 years, despite a declining trend in rainfall during the change (Anderegg et al., 2013). last century. This suggests that this species can survive extreme Variation in functional traits can derive from phenotypic temporal fluctuations in water availability (Gutiérrez et al., 2008). plasticity, genetic variation, developmental instability, and direct Understanding the ability of A. punctatum to withstand spatial effects of stress on plant performance, or a combination of these and temporal fluctuations in water availability requires improved mechanisms (Valladares et al., 2007; Matesanz et al., 2010; Gianoli knowledge of the mechanisms involved in drought tolerance and and Valladares, 2012). In recent years, interest in drought- vulnerability to the combined effects of increased water shortage resistance trait variation at the intraspecific level has increased and forest fragmentation. (Choat et al., 2007; Cornwell and Ackerly, 2009; Figueroa et al., Plants often respond to water deficit by modifying leaf traits 2010; Fajardo and Piper, 2011), because of its relevance to and decreasing transpirational water losses through reductions understanding plant species responses to drought stress and the in stomatal size and density, greater trichome density (TM; Fahn, maintenance of biodiversity (Violle et al., 2012). Studies have 1986; Baldini et al., 1997), and enhanced leaf mass per unit area often focused on species distributions across broad geographic (LMA; Niinemets, 2001; Poorter et al., 2009). Large number of ranges and stress conditions (Choat et al., 2007; Figueroa et al., short and narrow vessels per unit area are also adaptive under 2010; Fajardo and Piper, 2011; Vasey et al., 2012; Jacobsen and arid conditions and reduces the chances of hydraulic embolism Pratt, 2013). However, intraspecific variation of functional plant (Pockman and Sperry, 2000; Carlquist, 2001; Hacke et al., 2001; traits across pronounced environmental gradients at small spatial Jacobsen et al., 2007; Markesteijn et al., 2011a,b). The above-cited scales can also provide clues to identifying species responses studies have generally focused on changes in mean trait values, to key environmental factors, such as water availability, and while changes in trait variability [measured by the coefficient their interactions with wide spread global change threats such as of variation (CV)] have received less attention (Violle et al., fragmentation (Matesanz et al., 2009). 2012). Likewise, comparative studies across moisture gradients In semiarid regions, ecosystems that depend on coastal fogs for have often ignored the phenotypic or morphological integration water supply (del-Val et al., 2006; Hildebrandt and Eltahir, 2006; (Nicotra et al., 2007), which refers to coordinated variation Katata et al., 2010; Vasey et al., 2012) represent an interesting case of morphological traits (Cheverud et al., 1989; Murren, 2002; with respect to acute moisture gradients. In such ecosystems, fog Pigliucci, 2003; Pigliucci and Preston, 2004) and it can result from interception by vegetation is the primary or even the only source different processes (Klingenberg, 2014) including pleiotropy or of moisture during prolonged dry periods (Dawson, 1998; del-Val coordinated gene expression, functional relation among traits et al., 2006; Ewing et al., 2009). Fog influx creates pronounced or development factors. Trait correlations among individuals asymmetries between windward to leeward edges of forest within a population or species are generally used to characterize patches (Weathers et al., 2000; del-Val et al., 2006; Ewing et al., integration patterns (static integration sensu Klingenberg, 2014), 2009; Stanton et al., 2013), as well as among different-size patches but variation among related species or across ontogenetic stages with contrasting edge effects. Fragmentation enhances sensitivity has also been considered. Correlations between leaf (Wright et al., to current and future changes in fog water supply (Hildebrandt 2004)andhydraulictraits(Chave et al., 2009; Zanne et al., and Eltahir, 2006; Gutiérrez et al., 2008; Johnstone and Dawson, 2010) have been documented by several recent studies (Brodribb 2010). Changes in fog frequency and intensity are predicted to and Feild, 2000; Brodribb et al., 2002; Santiago et al., 2004; occur in these areas due to changes in sea-surface temperature Wright et al., 2006; Meinzer et al., 2008; Baraloto et al., 2010).