Tree Physiology Advance Access published February 24, 2015
Tree Physiology 00, 1–13 doi:10.1093/treephys/tpv001
Research paper
Environmental controls in the water use patterns of a tropical cloud forest tree species, Drimys brasiliensis (Winteraceae) Cleiton B. Eller1, Stephen S.O. Burgess2 and Rafael S. Oliveira1,2,3 1Department of Plant Biology, Institute of Biology, University of Campinas – UNICAMP, CP6109, Campinas, SP, Brazil; 2School of Plant Biology, The University of Western Australia – UWA, Perth, WA 6009, Australia; 3Corresponding author ([email protected])
Received January 30, 2014; accepted January 4, 2015; handling Editor Kathy Steppe
Trees from tropical montane cloud forest (TMCF) display very dynamic patterns of water use. They are capable of downwards water transport towards the soil during leaf-wetting events, likely a consequence of foliar water uptake (FWU), as well as high rates of night-time transpiration (Enight) during drier nights. These two processes might represent important sources of water losses and gains to the plant, but little is known about the environmental factors controlling these water fluxes. We evaluated how contrasting atmospheric and soil water conditions control diurnal, nocturnal and seasonal dynamics of sap flow in Drimys brasiliensis (Miers), a common Neotropical cloud forest species. We monitored the seasonal variation of soil water content, micrometeorological conditions and sap flow of D. brasiliensis trees in the field during wet and dry seasons. We also conducted a greenhouse experiment exposing D. brasiliensis saplings under contrasting soil water conditions to deuterium-labelled fog water. We found that during the night D. brasiliensis possesses heightened stomatal sensitivity to soil drought and vapour pressure deficit, which reduces night-time water loss. Leaf-wetting events had a strong suppressive effect on tree transpiration (E). Foliar water uptake increased in magnitude with drier soil and during longer leaf-wetting events. The difference between diurnal and nocturnal stomatal behaviour in D. brasiliensis could be attributed to an optimization of carbon gain when leaves are dry, as well as minimization of nocturnal water loss. The leaf-wetting events on the other hand seem important to D. brasiliensis water balance, especially during soil droughts, both by suppressing tree transpiration (E) and as a small additional water supply through FWU. Our results suggest that decreases in leaf-wetting events in TMCF might increase D. brasiliensis water loss and decrease its water gains, which could compromise its ecophysiological performance and survival during dry periods. Keywords: crown conductance, drought, fog, foliar water uptake, night-time transpiration, sap flow, stable isotopes, stomatal sensitivity, tropical montane cloud forest.
Introduction Water movement in plants is mostly a passive process driven by water potential gradients throughout the soil–plant–atmosphere continuum (SPAC). Recent evidence has suggested that water movement in plants is not necessarily a unidirectional process (see Goldsmith 2013). Water can flow from tree crowns to roots during leaf-wetting events (Burgess and Dawson 2004, Oliveira et al. 2005a, Nadezhdina et al. 2010, Eller et al. 2013, Goldsmith et al. 2013), or between roots in soil compartments with different moisture content (Burgess et al. 2001a, Oliveira
et al. 2005b, Burgess and Bleby 2006). The multidirectional movement of water in the SPAC might improve plant water balance during drought (Dawson 1993, Querejeta et al. 2007, Bauerle et al. 2008, Eller et al. 2013), affect plant–plant interactions (Dawson 1993, Ludwig et al. 2003, Warren et al. 2008) and even influence larger scale water fluxes and ecosystem-level processes (Ryel et al. 2002, Lee et al. 2005). Night-time transpiration (Enight) is another important aspect of plant water relations that has received considerable attention in recent years. This phenomenon has been observed in several
© The Author 2015. Published by Oxford University Press. All rights reserved. For Permissions, please email: [email protected]
2 Eller et al. plant species from contrasting ecosystems (Daley and Phillips 2006, Dawson et al. 2007, Scholz et al. 2007, Rosado et al. 2012) but the environmental and physiological mechanisms controlling Enight remain unclear. Daytime and night-time stomatal conductance (gs) are both controlled by soil water availability (Dawson et al. 2007, Zeppel et al. 2010) and atmospheric vapour pressure deficit (VPD; Zeppel et al. 2010, Rosado et al. 2012), but recent studies suggest that diurnal and nocturnal gs are under different genetic controls (Caird et al. 2007, Christman et al. 2009) and might respond differently to environmental drivers (Oren et al. 2001, Sellin and Lubenets 2010, Ogle et al. 2012). Trees from tropical montane cloud forests (TMCF) are good study models to understand the high dynamicity of water movement in plants because of the wide variety of environmental conditions to which this vegetation is often exposed. These conditions include frequent leaf-wetting events (Bruijnzeel et al. 2011), high VPDs and potential evapotranspiration during clear days (Rosado et al. 2010) and strongly seasonal rainfall patterns (Jarvis and Mulligan 2011). Recent studies have shown that TMCF trees are able to move water towards their roots during leaf-wetting events due to foliar water uptake (FWU; Eller et al. 2013) and transpire substantially at night (Rosado et al. 2012, Gotsch et al. 2014). Given the important hydrological role of TMCF (Bruijnzeel et al. 2011), it is crucial to understand how TMCF tree water use responds to different environmental conditions in order to predict the response of these ecosystems to climatic changes that could affect tropical montane regions, such as reduced cloud immersion and increased atmospheric evaporative demand (Still et al. 1999). In our study, we quantified the relative importance of Enight and FWU to whole-tree water balance of Drimys brasiliensis (Miers), a dominant TMCF tree species. We expected these processes to comprise a significant part of D. brasiliensis water balance. We also investigated the main environmental conditions controlling D. brasiliensis water use and how the effect of these environmental controls changes between different periods of the diel cycle (day vs night). We hypothesized that VPD would be the main driver of D. brasiliensis transpiration (E). Leaf wetness (LW) and lower soil water content (SWC) should inhibit E by different mechanisms: LW should impede gas exchange due to the formation of a water film on leaves (Smith and McClean 1989, Brewer and Smith 1997, Oliveira et al. 2014a), while lower SWC should decrease D. brasiliensis gs. Foliar water uptake should be mostly affected by LW and SWC, as these variables should represent the water potential gradients driving this process (Oliveira et al. 2014a). We expected to find differences between nocturnal and diurnal processes, especially E as we expect it to depend more on gs than does FWU. To address these questions we monitored seasonal variations in SWC, VPD and LW, and then we used these environmental data to explain the daily sap flow patterns of TMCF trees in
Tree Physiology Volume 00, 2015
the field. We also conducted a deuterium-labelling experiment in a greenhouse to confirm some of the water use patterns found in the field.
Materials and methods Site description Field observations were conducted from March to November of 2011 in a TMCF stand located in Campos do Jordão, SP, Brazil (22°69′S 45°52′W; elevation: ∼2000 m). The climate at the site is characterized by a mean annual rainfall of 1590 ± 98 mm year−1 (mean ± SE; from 2000 to 2010; National Institute of Metereology, INMET), with a distinct dry season in the middle of the year in which
Tree Physiology 00, 1–13 doi:10.1093/treephys/tpv001
Research paper
Environmental controls in the water use patterns of a tropical cloud forest tree species, Drimys brasiliensis (Winteraceae) Cleiton B. Eller1, Stephen S.O. Burgess2 and Rafael S. Oliveira1,2,3 1Department of Plant Biology, Institute of Biology, University of Campinas – UNICAMP, CP6109, Campinas, SP, Brazil; 2School of Plant Biology, The University of Western Australia – UWA, Perth, WA 6009, Australia; 3Corresponding author ([email protected])
Received January 30, 2014; accepted January 4, 2015; handling Editor Kathy Steppe
Trees from tropical montane cloud forest (TMCF) display very dynamic patterns of water use. They are capable of downwards water transport towards the soil during leaf-wetting events, likely a consequence of foliar water uptake (FWU), as well as high rates of night-time transpiration (Enight) during drier nights. These two processes might represent important sources of water losses and gains to the plant, but little is known about the environmental factors controlling these water fluxes. We evaluated how contrasting atmospheric and soil water conditions control diurnal, nocturnal and seasonal dynamics of sap flow in Drimys brasiliensis (Miers), a common Neotropical cloud forest species. We monitored the seasonal variation of soil water content, micrometeorological conditions and sap flow of D. brasiliensis trees in the field during wet and dry seasons. We also conducted a greenhouse experiment exposing D. brasiliensis saplings under contrasting soil water conditions to deuterium-labelled fog water. We found that during the night D. brasiliensis possesses heightened stomatal sensitivity to soil drought and vapour pressure deficit, which reduces night-time water loss. Leaf-wetting events had a strong suppressive effect on tree transpiration (E). Foliar water uptake increased in magnitude with drier soil and during longer leaf-wetting events. The difference between diurnal and nocturnal stomatal behaviour in D. brasiliensis could be attributed to an optimization of carbon gain when leaves are dry, as well as minimization of nocturnal water loss. The leaf-wetting events on the other hand seem important to D. brasiliensis water balance, especially during soil droughts, both by suppressing tree transpiration (E) and as a small additional water supply through FWU. Our results suggest that decreases in leaf-wetting events in TMCF might increase D. brasiliensis water loss and decrease its water gains, which could compromise its ecophysiological performance and survival during dry periods. Keywords: crown conductance, drought, fog, foliar water uptake, night-time transpiration, sap flow, stable isotopes, stomatal sensitivity, tropical montane cloud forest.
Introduction Water movement in plants is mostly a passive process driven by water potential gradients throughout the soil–plant–atmosphere continuum (SPAC). Recent evidence has suggested that water movement in plants is not necessarily a unidirectional process (see Goldsmith 2013). Water can flow from tree crowns to roots during leaf-wetting events (Burgess and Dawson 2004, Oliveira et al. 2005a, Nadezhdina et al. 2010, Eller et al. 2013, Goldsmith et al. 2013), or between roots in soil compartments with different moisture content (Burgess et al. 2001a, Oliveira
et al. 2005b, Burgess and Bleby 2006). The multidirectional movement of water in the SPAC might improve plant water balance during drought (Dawson 1993, Querejeta et al. 2007, Bauerle et al. 2008, Eller et al. 2013), affect plant–plant interactions (Dawson 1993, Ludwig et al. 2003, Warren et al. 2008) and even influence larger scale water fluxes and ecosystem-level processes (Ryel et al. 2002, Lee et al. 2005). Night-time transpiration (Enight) is another important aspect of plant water relations that has received considerable attention in recent years. This phenomenon has been observed in several
© The Author 2015. Published by Oxford University Press. All rights reserved. For Permissions, please email: [email protected]
2 Eller et al. plant species from contrasting ecosystems (Daley and Phillips 2006, Dawson et al. 2007, Scholz et al. 2007, Rosado et al. 2012) but the environmental and physiological mechanisms controlling Enight remain unclear. Daytime and night-time stomatal conductance (gs) are both controlled by soil water availability (Dawson et al. 2007, Zeppel et al. 2010) and atmospheric vapour pressure deficit (VPD; Zeppel et al. 2010, Rosado et al. 2012), but recent studies suggest that diurnal and nocturnal gs are under different genetic controls (Caird et al. 2007, Christman et al. 2009) and might respond differently to environmental drivers (Oren et al. 2001, Sellin and Lubenets 2010, Ogle et al. 2012). Trees from tropical montane cloud forests (TMCF) are good study models to understand the high dynamicity of water movement in plants because of the wide variety of environmental conditions to which this vegetation is often exposed. These conditions include frequent leaf-wetting events (Bruijnzeel et al. 2011), high VPDs and potential evapotranspiration during clear days (Rosado et al. 2010) and strongly seasonal rainfall patterns (Jarvis and Mulligan 2011). Recent studies have shown that TMCF trees are able to move water towards their roots during leaf-wetting events due to foliar water uptake (FWU; Eller et al. 2013) and transpire substantially at night (Rosado et al. 2012, Gotsch et al. 2014). Given the important hydrological role of TMCF (Bruijnzeel et al. 2011), it is crucial to understand how TMCF tree water use responds to different environmental conditions in order to predict the response of these ecosystems to climatic changes that could affect tropical montane regions, such as reduced cloud immersion and increased atmospheric evaporative demand (Still et al. 1999). In our study, we quantified the relative importance of Enight and FWU to whole-tree water balance of Drimys brasiliensis (Miers), a dominant TMCF tree species. We expected these processes to comprise a significant part of D. brasiliensis water balance. We also investigated the main environmental conditions controlling D. brasiliensis water use and how the effect of these environmental controls changes between different periods of the diel cycle (day vs night). We hypothesized that VPD would be the main driver of D. brasiliensis transpiration (E). Leaf wetness (LW) and lower soil water content (SWC) should inhibit E by different mechanisms: LW should impede gas exchange due to the formation of a water film on leaves (Smith and McClean 1989, Brewer and Smith 1997, Oliveira et al. 2014a), while lower SWC should decrease D. brasiliensis gs. Foliar water uptake should be mostly affected by LW and SWC, as these variables should represent the water potential gradients driving this process (Oliveira et al. 2014a). We expected to find differences between nocturnal and diurnal processes, especially E as we expect it to depend more on gs than does FWU. To address these questions we monitored seasonal variations in SWC, VPD and LW, and then we used these environmental data to explain the daily sap flow patterns of TMCF trees in
Tree Physiology Volume 00, 2015
the field. We also conducted a deuterium-labelling experiment in a greenhouse to confirm some of the water use patterns found in the field.
Materials and methods Site description Field observations were conducted from March to November of 2011 in a TMCF stand located in Campos do Jordão, SP, Brazil (22°69′S 45°52′W; elevation: ∼2000 m). The climate at the site is characterized by a mean annual rainfall of 1590 ± 98 mm year−1 (mean ± SE; from 2000 to 2010; National Institute of Metereology, INMET), with a distinct dry season in the middle of the year in which
