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Stem and leaf hydraulic properties are finely coordinated in three tropical rainforest tree species
Abstract
Coordination of stem and leaf hydraulic traits allows terrestrial plants to maintain safe water status under limited water supply. Tropical rainforests, one of the world's most productive biomes, are vulnerable to drought and potentially threatened by increased aridity due to global climate change. However, the relationship of stem and leaf traits within the plant hydraulic continuum remains understudied, particularly in tropical species. We studied within-plant hydraulic coordination between stems and leaves in three tropical lowland rainforest tree species by analyses of hydraulic vulnerability (hydraulic methods and ultrasonic emission (UE) analysis), pressure-volume relations and in situ predawn and midday water potentials (Ψ). We found finely coordinated stem and leaf hydraulic features, with a strategy of sacrificing leaves in favour of stems. Fifty percent of hydraulic conductivity (P50 ) was lost at -2.1 to -3.1 MPa in stems and -1.7 to -2.2 MPa in leaves. UE analysis corresponded to hydraulic measurements. Safety margins (leaf P50 - stem P50 ) were very narrow at -0.4 to -1.4 MPa. Pressure-volume analysis and in situ Ψ indicated safe water status in stems but risk of hydraulic failure in leaves. Our study shows that stem and leaf hydraulics were finely tuned to avoid embolism formation in the xylem.
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Supplementary resources (2)
Data
October 2015
Data
October 2015
... Si la fermeture stomatique seule entraîne un arrêt temporaire des échanges gazeux, l'embolie des feuilles entraînerait, elle, une perte de fonction a priori irréversible à l'échelle de la feuille en l'absence de 'refilling' sous tension. Plusieurs études ont mis en évidence que la fermeture stomatique survient avant et protège la feuille contre la propagation de l'embolie (Hochberg et al., 2017 ;Li et al., 2019 ;Trueba et al., 2019 ;Creek et al., 2020), mais cela ne semble pas toujours être le cas (Nolf et al., 2015). De plus, les espèces avec une plus forte résistance à l'embolie des feuilles ont des potentiels de fermeture stomatique plus négatifs , et il semblerait que ces deux traits peuvent montrer une réponse plastique au cours de la saison sèche en s'ajustant de concert (Sorek et al., 2020). ...
... L'embolie des feuilles aurait pour effet de réduire la demande évapotranspirative et de retarder la propagation de l'embolie dans les organes pérennes. Il existe de nombreux exemples de segmentation de vulnérabilité hydraulique positive (Hao et al., 2008 ;Chen et al., 2009 ;Johnson et al., 2011Johnson et al., , 2016Bucci et al., 2012 ;Nolf et al., 2015 ;Charrier et al., 2016 ;Hochberg et al., 2016 ;Rodriguez-Dominguez et al., 2018 ;Skelton et al., 2018 ;Losso et al., 2019 ;Smith-Martin et al., 2020). ...
... Cependant, une absence de segmentation (Chen et al., 2009 ;Nolf et al., 2015 ;Skelton et al., 2017a ;Klepsch et al., 2018 ;Skelton et al., 2018 ;Losso et al., 2019 ;Li et al., 2020 ;Smith-Martin et al., 2020) voire une segmentation négative ont aussi été rapportées (Fig. 25 ...
Les forêts tropicales humides jouent un rôle clé dans les cycles biogéochimiques à l’échelle globale. Les évènements de sécheresse saisonniers entrainent des modifications dans le fonctionnement de ces forêts. L’augmentation de la fréquence et de l’intensité des évènements de sécheresse de forte intensité à l’échelle de l’Amazonie entraine déjà un changement dans la composition des communautés d’arbres, mais notre capacité à prédire leur réponse future dépend en partie de nos connaissances des mécanismes physiologiques leur permettant de résister à la sécheresse. Cette thèse explore la diversité interspécifique des mécanismes de résistance à la sécheresse des arbres en forêt tropicale humide de Guyane et vise à améliorer les connaissances actuelles. Elle montre que les espèces d’arbres de canopée en forêt naturelle peuvent avoir une grande résistance à l’embolie des tiges et qu’une majorité des espèces ont un grand niveau de sureté hydraulique en saison sèche, avec une grande variabilité interspécifique. Cependant, pour la majorité d’entre eux, une diminution de la disponibilité en eau du sol entraine une diminution de leur densité de flux de sève en saison sèche, et une partie de cette sensibilité peut être expliquée par des mécanismes physiologiques liés à des stratégies de résistance à la sécheresse. Les mécanismes physiologiques sous-jacents à ces stratégies varient fortement entre espèces pour de jeunes arbres. Certaines bénéficient d’une fermeture stomatique précoce et d’une faible conductance minimum, alors que d’autres ont une plus grande résistance à l’embolie des tiges et un plus fort degré de segmentation de vulnérabilité, parfois associés à une grande tolérance à l’embolie des tiges. Lors d’une sécheresse de forte intensité, nous avons observé une forte réduction des teneurs en carbohydrates, ce qui souligne l’interdépendance entre le fonctionnement hydraulique et carboné des espèces. Cependant, le principal processus physiologique causant la mort semble être la défaillance hydraulique. Cette forte variabilité interspécifique amène à postuler que les populations d’arbres de forêt tropicale humide pourraient répondre de manière contrastée à une intensification des épisodes de sécheresse, ce qui pourrait avoir des conséquences sur la composition des communautés d’arbres en Guyane.
... Dysoxylum, Elaeocarpus and Syzygium sayeri (Nolf et al., 2015). We reanalysed these data using the Loess regression for consistency within the current study and included them in our analysis. ...
... We also included previously reported Ψ TLP values from Dysoxylum, Elaeocarpus and Syzygium sayeri (Nolf et al., 2015) and ...
... Therefore, in this study, we tailored field visits to each site and its unique climate and weather patterns, targeting the month of greatest water limitation and evaporative demand. For the few tree species we measured that have appeared in other field studies, we have captured similar or more negative water potential values (Apgaua et al., 2015;Blake, 1977;Gleason et al., 2012;Nolf et al., 2015;Sinclair, 1980). However, water potential is strongly influenced by species specific biotic factors and localityspecific abiotic factors, such as climate, soil depth and water holding capacity, -meaning water potentials will vary across a species' range. ...
Globally, forests are facing an increasing risk of mass tree mortality events associated with extreme droughts and higher temperatures. Hydraulic dysfunction is considered a key mechanism of drought triggered dieback. By leveraging the climate breadth of the Australian landscape and a national network of research sites (Terrestrial Ecosystem Research Network), we conducted a continental‐scale study of physiology and hydraulic traits of 33 native tree species from contrasting environments to disentangle the complexities of plant response to drought across communities.
We found strong relationships between key plant hydraulic traits and site aridity. Leaf turgor loss point and xylem embolism resistance were correlated with minimum water potential experienced by each species. Across the dataset, there was a strong coordination between hydraulic traits, including those linked to hydraulic safety, stomatal regulation, and the cost of caron investment into woody tissue.
These results illustrate that aridity has acted as a strong selective pressure, shaping hydraulic traits of tree species across the Australian landscape. Hydraulic safety margins were constrained across sites, with species from wetter sites tending to have smaller safety margin compared with species at driest sites, suggesting trees are operating close to their hydraulic thresholds and forest biomes across the spectrum may be susceptible to shifts in climate that result in the intensification of drought.
... With the development of new methods for measuring stem resistance to embolism, leaf vein resistance to embolism, and the loss of leaf conductance, the vulnerability segmentation hypothesis has gained a large interest since the 2000's, maybe in disfavour of the hydraulic segmentation hypothesis. The vulnerability segmentation is now rather a consensus than a hypothesis, since it has been repeatedly shown (Hao et al. 2008;Johnson et al. 2011;Bucci et al. 2012;Nolf et al. 2015;Johnson et al. 2016;Hochberg et al. 2016;Losso et al. 2019). The leaf-stem segmentation degree varies across species, with various studies suggesting segmented species, unsegmented species, and even species negatively segmented (i.e. ...
... Most of studies investigating the vulnerability segmentation were based on measurements of the total leaf conductance, integrating both the xylem pathway and the outside-xylem pathway (Hao et al. 2008;Johnson et al. 2011;Bucci et al. 2012;Nolf et al. 2015;Johnson et al. 2016;, whereas the stem is mainly made of a xylem pathway. On the one hand, the loss of leaf conductance with water stress does not tell anything on the level of embolism of the vein xylem. ...
... Our results confirmed that some species can exhibit vulnerability segmentation, whereas others are not. This is in agreement with past studies showing species positively segmented (Hao et al. 2008;Johnson et al. 2011Johnson et al. , 2016Bucci et al. 2012;Nolf et al. 2015;Hochberg et al. 2016;Losso et al. 2019), negatively segmented , or unsegmented Nolf et al. 2015;Losso et al. 2019). Moreover, our study covered the strongest variation in vulnerability segmentation in one experiment, with a range of 4 MPa (between -1 and 3 MPa). ...
Les traits hydrauliques sont reliés aux fonctions fondamentales du transport de l’eau dans la plante et de la résistance à la sécheresse, déterminant l’écologie, l’évolution, et les processus en lien avec le changement climatique pour les plantes. Cependant, ces traits restent que peu documentés pour les forêts tropicales humides, empêchant de mieux comprendre l’écologie des arbres tropicaux et le futur des forêts tropicales. À partir d’une approche générale s’intéressant à la structure (morphologie et anatomie) et au fonctionnement (physiologie) de la pousse feuillée au sein des arbres, cette thèse analyse la structure et le fonctionnement de la pousse feuillée des arbres, notamment dans la perspective de la résistance à la sécheresse. Cette thèse s’appuie sur un jeu de données général qui concerne 42 espèces d’arbres de canopée échantillonnées en forêt tropicale humide de Guyane, et qui illustre une large gamme de tailles de feuilles. Un second jeu de données, destiné à mieux comprendre les sources de variabilité intraspécifique, porte de l’espèce pionnière Cecropia obtusa Trécul (Urticaceae). Une première partie de la thèse vise à comprendre la coordination entre la feuille et la tige pour une large gamme de dimension foliaire, en analysant les changements morpho-anatomiques et fonctionnels soulignant la relation entre dimensions de la feuille et dimensions de la tige à l’échelle interspécifique. Ce cadre est aussi appliqué à l’échelle intraspécifique pour le modèle C. obtusa pour la relation pétiole-limbe. Comprendre les changements liés aux dimensions de la feuille permet ainsi d’investir correctement les effets ontogénétiques et saisonniers sur les traits foliaires vasculaires et hydrauliques pour C. obtusa. La seconde partie vise à mieux comprendre les mécanismes de résistance à la sécheresse de la pousse feuillée. En retenant 25 espèces, les déterminants anatomiques de la résistance à l’embolie par sécheresse des tiges et sont étudiés. Les différentes propriétés et mécanismes déjà connus pour des plantes tempérées sont abordés conjointement afin de conforter ou non leur existence et comprendre leurs contributions relatives. La segmentation de vulnérabilité (c.-a.d. la différenciation de résistance à l’embolie) à l’interface tige-feuille est également étudiée pour 20 espèces. Sa coordination avec la segmentation hydraulique (c.-à-d. différenciation de résistance hydraulique), qui est dérivée des études anatomiques réalisées dans la première partie, est étudiée. Je montre ainsi (i) un large spectre de variation pour la segmentation de vulnérabilité entre espèces, (ii) une relation positive avec la segmentation hydraulique, suggérant qu’il y a des espèces promouvant à la fois la segmentation hydraulique et la segmentation de vulnérabilité pour découpler le fonctionnement la feuille de la tige du point de vue hydraulique, et (iii) que la segmentation de vulnérabilité a un impact important sur le temps de dessiccation théorique de la pousse feuillée, confirmant que la segmentation de vulnérabilité est un mécanisme de résistance à la sécheresse. Dans une dernière partie, je teste le pouvoir prédictif des différents traits hydrauliques étudiés sur la distribution hydro-topographique des espèces, ainsi que l’impact du stress hydrique sur la croissance des arbres, à une échelle locale. Dans la Discussion générale, je discute de la signification fonctionnelle de la surface de la feuille et des traits de résistance à la sécheresse en forêt tropicale humide, ainsi que la relation potentielle entre la surface de la feuille et la résistance à la sécheresse.
... With the development of new methods for measuring xylem resistance to embolism in stems and leaves, and the loss of leaf conductance, the vulnerability segmentation hypothesis has gained renewed interest since the 2000s. Positive segmentation (leaf less resistant to the loss of conductance than stem) has been shown frequently (Hao et al., 2008;Chen et al., 2009;Johnson et al., 2011Johnson et al., , 2016Bucci et al., 2012;Nolf et al., 2015;Charrier et al., 2016;Hochberg et al., 2016;Rodriguez-Dominguez et al., 2018;Skelton et al., 2018;Losso et al., 2019). However, there are also records of negative segmentation (leaf more resistant to the loss of conductance than stem; Klepsch et al., 2018), or the absence of segmentation (leaf and stem equally resistant to the loss of conductance; Chen et al., 2009;Nolf et al., 2015;Skelton et al., 2017Skelton et al., , 2018Klepsch et al., 2018;Losso et al., 2019). ...
... Positive segmentation (leaf less resistant to the loss of conductance than stem) has been shown frequently (Hao et al., 2008;Chen et al., 2009;Johnson et al., 2011Johnson et al., , 2016Bucci et al., 2012;Nolf et al., 2015;Charrier et al., 2016;Hochberg et al., 2016;Rodriguez-Dominguez et al., 2018;Skelton et al., 2018;Losso et al., 2019). However, there are also records of negative segmentation (leaf more resistant to the loss of conductance than stem; Klepsch et al., 2018), or the absence of segmentation (leaf and stem equally resistant to the loss of conductance; Chen et al., 2009;Nolf et al., 2015;Skelton et al., 2017Skelton et al., , 2018Klepsch et al., 2018;Losso et al., 2019). A recent meta-analysis suggests that the degree of vulnerability segmentation is correlated with biome aridity (Zhu et al., 2016), with a larger positive segmentation degree found in dry regions. ...
... Most studies investigating the vulnerability segmentation hypothesis were based on measurements of the whole leaf conductance, integrating both the xylem pathway and the outsidexylem pathway (Hao et al., 2008;Chen et al., 2009Chen et al., , 2010Johnson et al., 2011Johnson et al., , 2016Bucci et al., 2012;Nolf et al., 2015;Scoffoni et al., 2017b), whereas water transport in the stem relies on xylem only. But owing to long-standing methodological concerns, differences between leaf and stem xylem in embolism resistance have only recently been investigated (Charrier et al., 2016;Hochberg et al., 2016;Skelton et al., 2017Skelton et al., , 2018Klepsch et al., 2018;Rodriguez-Dominguez et al., 2018), and not yet on a broad set of species. ...
Hydraulic segmentation at the stem–leaf transition predicts higher hydraulic resistance in leaves than in stems. Vulnerability segmentation, however, predicts lower embolism resistance in leaves. Both mechanisms should theoretically favour runaway embolism in leaves to preserve expensive organs such as stems, and should be tested for any potential coordination.
We investigated the theoretical leaf‐specific conductivity based on an anatomical approach to quantify the degree of hydraulic segmentation across 21 tropical rainforest tree species. Xylem resistance to embolism in stems (flow‐centrifugation technique) and leaves (optical visualization method) was quantified to assess vulnerability segmentation.
We found a pervasive hydraulic segmentation across species, but with a strong variability in the degree of segmentation. Despite a clear continuum in the degree of vulnerability segmentation, eight species showed a positive vulnerability segmentation (leaves less resistant to embolism than stems), whereas the remaining species studied exhibited a negative or no vulnerability segmentation.
The degree of vulnerability segmentation was positively related to the degree of hydraulic segmentation, such that segmented species promote both mechanisms to hydraulically decouple leaf xylem from stem xylem. To what extent hydraulic and vulnerability segmentation determine drought resistance requires further integration of the leaf–stem transition at the whole‐plant level, including both xylem and outer xylem tissue.
... Moreover, species identity was shown to be the main driver of variation in π tlp , with, respectively, low and negligible intraspecific and seasonal variability (Maréchaux et al. 2016). At present, the few studies providing a combined investigation of Ψ 50 and π tlp for tropical rainforest species concern only a limited number of species and have yielded contradictory conclusions Nolf et al. 2015;Bartlett et al. 2016;Martin-StPaul et al. 2017;Powell et al. 2017). Likewise, the absence of a general consensus on the magnitude of Ψ 50 and the risk of hydraulic failure in hyper-diverse ecosystems such as tropical rainforests highlights the need for more research, in particular for large canopy-trees, which are at higher risk of drought-induced mortality during extreme climatic events (Bennett et al. 2015). ...
... Considerable interspecific variability in branch xylem vulnerability to embolism In this study, our sampling of 25 tropical rainforest canopy-tree species showed a four-fold range of magnitude in branch xylem vulnerability to embolism (Fig. 1, Table 1). This range encompasses 72% of the previously observed angiosperm variation in Ψ 50 at the global scale (Choat et al. 2012) and expands the range of known branch xylem vulnerability to embolism for tropical forest Angiosperm tree species (Choat et al. 2012;Nolf et al. 2015;Rowland et al. 2015;Christoffersen et al. 2016;Powell et al. 2017;Santiago et al. 2018). The limited importance of confounding factors (e.g., genetics, ontogeny, competition, habitat) indicates that the observed interspecific variability was mostly related to the species' intrinsic functional characteristics. ...
... The limited importance of confounding factors (e.g., genetics, ontogeny, competition, habitat) indicates that the observed interspecific variability was mostly related to the species' intrinsic functional characteristics. Mean community branch Ψ 50 (− 3.93 ± 0.31 MPa; Fig. 1 and Table 1) was much more negative than the worldwide mean for tropical rainforests; it was also more negative than the mean values published to date for terra firme canopy-tree species (− 2.31 ± 0.20 MPa; Sperry et al. 1988;Machado and Tyree 1994;Tyree et al. 1998;Choat et al. 2007;Sperry et al. 2007;Meinzer et al. 2008;Nolf et al. 2015;Rowland et al. 2015;Powell et al. 2017;Santiago et al. 2018) and was comparable to values found for drier biomes (Fig. 1). Our results therefore clearly contrast with the global and inter-biome pattern of interspecific variation in branch embolism resistance, where total precipitation is thought to be the main driver (Maherali et al. 2004;Choat et al. 2012). ...
Key message
Abundant Neotropical canopy-tree species are more resistant to drought-induced branch embolism than what is currently admitted. Large hydraulic safety margins protect them from hydraulic failure under actual drought conditions.
Context
Xylem vulnerability to embolism, which is associated to survival under extreme drought conditions, is being increasingly studied in the tropics, but data on the risk of hydraulic failure for lowland Neotropical rainforest canopy-tree species, thought to be highly vulnerable, are lacking.
Aims
The purpose of this study was to gain more knowledge on species drought-resistance characteristics in branches and leaves and the risk of hydraulic failure of abundant rainforest canopy-tree species during the dry season.
Methods
We first assessed the range of branch xylem vulnerability to embolism using the flow-centrifuge technique on 1-m-long sun-exposed branches and evaluated hydraulic safety margins with leaf turgor loss point and midday water potential during normal- and severe-intensity dry seasons for a large set of Amazonian rainforest canopy-tree species.
Results
Tree species exhibited a broad range of embolism resistance, with the pressure threshold inducing 50% loss of branch hydraulic conductivity varying from − 1.86 to − 7.63 MPa. Conversely, we found low variability in leaf turgor loss point and dry season midday leaf water potential, and mostly large, positive hydraulic safety margins.
Conclusions
Rainforest canopy-tree species growing under elevated mean annual precipitation can have high resistance to embolism and are more resistant than what was previously thought. Thanks to early leaf turgor loss and high embolism resistance, most species have a low risk of hydraulic failure and are well able to withstand normal and even severe dry seasons.
... For each rehydration experiment, leaves were connected to the hydraulic apparatus within 2 s and K leaf was calculated from the flow rate recorded within the first 4-6 s following leaf connection to the flow meter. These initial flow rates were assumed to be influenced predominantly by the hydraulic resistance of the xylem pathway, and thus we considered the decline in K leaf to be driven primarily by the formation and spread of xylem embolism (see Nolf et al., 2015;Skelton et al., 2015Skelton et al., , 2017aBrodribb et al., 2016a, b). However, we acknowledge that the decline in K leaf can also be influenced by measurement light intensity, which has been shown to affect hydraulic processes in leaf tissues beyond the xylem (Guyot et al., 2012;Trifilo et al., 2016). ...
... This suggests that a similar level of coordination between xylem reinforcement and embolism resistance may be present in leaves. Although we cannot preclude the possibility that cell collapse occurs in angiosperm leaves under tension (see Zhang et al., 2016), the weight of recent evidence suggests that leaf hydraulic decline during severe drought is caused by xylem embolism (Johnson et al., 2009;Nolf et al., 2015;Brodribb et al., 2016a, b;Scoffoni et al., 2017b;Skelton et al., 2017a). Thus, we suggest xylem reinforcement in leaves has evolved to provide a degree of safety from vessel collapse under tension, while embolism spread via air-seeding could potentially relate to the size and structure of pores in pit membranes (Jansen et al., 2009), nucleation from hydrophobic surfaces (Tyree et al., 1994) or, as hypothesized recently, conduit/fluid properties that influence the expansion of nanobubbles (Schenk et al., 2015). ...
... Indeed, we note that our estimate of maximum K leaf and thus P50 leaf for each species may be underestimated on the basis that our rehydration measurements were conducted under low light and thus did not allow for the influence of outside xylem processes in driving the response of K leaf during drought (Scoffoni et al., 2008(Scoffoni et al., , 2017a. However, our approach of measuring K leaf under low light is consistent with the approach of other studies that have shown strong correspondence between the decline in K leaf during drought, measured using the rehydration technique (Brodribb and Cochard, 2009), and the accumulation of xylem embolisms detected acoustically (Nolf et al., 2015) and visually via a recently developed optical technique (Brodribb et al., 2016a, b) and X-ray micro-computed tomography (Skelton et al., 2017a). Furthermore, in contrast to the evaporative flux technique (Sack et al., 2002) and the timed rehydration kinetics technique (Brodribb and Holbrook, 2003), we calculated K leaf from the initial flow rate into the leaf through the petiole, which is more likely to be influenced by within-xylem rather than outside-xylem processes. ...
Background and aims:
The structural properties of leaf venation and xylem anatomy strongly influence leaf hydraulics, including the ability of leaves to maintain hydraulic function during drought. Here we examined the strength of the links between different leaf venation traits and leaf hydraulic vulnerability to drought (expressed as P50leaf by rehydration kinetics) in a diverse group of 26 woody angiosperm species, representing a wide range of leaf vulnerabilities, from four low-nutrient sites with contrasting rainfall across eastern Australia.
Methods:
For each species we measured key aspects of leaf venation design, xylem anatomy and leaf morphology. We also assessed for the first time the scaling relationships between hydraulically weighted vessel wall thickness (th) and lumen breadth (bh) across vein orders and habitats.
Key results:
Across species, variation in P50leaf was strongly correlated with the ratio of vessel wall thickness (th) to lumen breadth (bh) [(t/b)h; an index of conduit reinforcement] at each leaf vein order. Concomitantly, the scaling relationship between th and bh was similar across vein orders, with a log-log slope less than 1 indicating greater xylem reinforcement in smaller vessels. In contrast, P50leaf was not related to th and bh individually, to major vein density (Dvmajor) or to leaf size. Principal components analysis revealed two largely orthogonal trait groupings linked to variation in leaf size and drought tolerance.
Conclusions:
Our results indicate that xylem conduit reinforcement occurs throughout leaf venation, and remains closely linked to leaf drought tolerance irrespective of leaf size.
... Although several studies using morphological traits have found that relationships between leaf and stems traits are weak or nonexistent (Baraloto et al., 2010;Fortunel et al., 2012;Silva et al., 2017), most studies of physiological processes have indeed found relationships between leaf and stem traits (Ishida et al., 2008;Meinzer et al., 2008;Pivovaroff et al., 2014;Nolf et al., 2015). Within organs, some traits are expected to be coordinated given their role in resource acquisition, use, and conservation. ...
... We also found negative relationships between WD and both K h and SLA. These results are consistent with studies that show a functional link between leaves and nonphotosynthetic stems (Ishida et al., 2008;Meinzer et al., 2008;Pivovaroff et al., 2014;Nolf et al., 2015;De Guzman et al., 2017), indicating that such links hold in leaves and photosynthetic stems as well. Despite high precipitation seasonality in our site, few changes in trait values were related to seasonal drought, and these traits were mainly traits involved with water movement. ...
METHODS: We studied photosynthetic, hydraulic, morphometric (specific leaf area [SLA], wood density [WD]), and biochemical (C and N isotopes) traits in leaves and photosynthetic stems of 12 plant species from a sarcocaulescent scrub in the southern Baja California Peninsula, Mexico, in wet and dry seasons.
RESULTS: Leaves and stems had similar mean photosynthetic capacity, as evaluated by chlorophyll fluorescence traits, indicating similar investment in leaf and stem photosynthesis. We did not find a relationship between stem hydraulic conductivity and leaf or stem photosynthetic traits. However, we found resource allocation trade-offs, between WD and both stem hydraulic conductivity and SLA. Leaf and stem photosynthetic traits did not change with season, but specific stem area was one of the few traits that changed the most between seasons—it increased during the dry season by as much as 154% indicating substantial water storage.
CONCLUSIONS: Our results indicate the same proportional investment in photosynthetic capacity and dry matter in both leaves and photosynthetic stems across all 12 species. We identified multiple strategies at this seasonal site, with species ranging from high WD, low SLA, low hydraulic conductivity, and high specific bark area on one end of the spectrum and opposite traits on the other end.
... Using Ψ tlp as a proxy for leaf water potential at stomatal closure can provide a rapid way to quantify stomatal regulation strategy (Martin-StPaul et al., 2017;Ziegler et al., 2019). (3) HSM can be calculated as the difference between water potentials at 50% loss of leaf hydraulic conductance and that at 50% loss of branch hydraulic conductivity, which is also termed as vulnerability segmentation (HSM segmentation ; Tyree et al., 1993;Bucci et al., 2013;Nolf et al., 2015). Unlike HSM leaf that is strongly influenced by environmental water conditions (water potential), HSM segmentation seems to be more inherent and static for a plant species. ...
... The stomatal safety margin (HSM stomatal ) was calculated as follows: HSM stomatal = Ψ tlp − P50 branch . The difference between water potential causing 50% loss of hydraulic conductance in leaves and branches was also a way to define hydraulic safety margin and calculated as HSM segmentation = P50 leaf -P50 branch (Bucci et al., 2013;Nolf et al., 2015). ...
... Compound leaf form with multiple leaf laminas growing on one rachis apparently can result in a potentially more efficient hydraulic system at the whole-shoot level, which has likely contributed to relatively high photosynthetic capacity and growth rates in tree species with compound leaves (Royer and Wilf 2006). The significantly higher K shoot found in CL species compared with SL species is a result of substantially higher hydraulic conductance in all the three major components (stem, rachis and leaflet) of the branch (see Table S1 and Figure S2 available as Supplementary Data at Tree Physiology Online), indicating strong functional coordination in xylem water transport among different parts of the hydraulic system (Pivovaroff et al. 2014, Nolf et al. 2015. The significantly higher average K stem of the CL species is associated with overall larger vessel diameters in their stem xylem (see Figure S1 available as Supplementary Data at Tree Physiology Online), since the theoretical hydraulic conductivity of a vessel increase exponentially with its diameter (Tyree and Zimmermann 2002). ...
... It is likely that species with larger leaves need more efficient water supply to support their potentially higher transpiration rate per leaf area Cao 2009, Pivovaroff et al. 2014). In turn, species with larger xylem conduits and higher hydraulic efficiency can better compensate for leaf water loss due to higher transpiration resulting in favorable water status provided that water is readily available (Meinzer 2002, 2003, Nolf et al. 2015. Moreover, wider conduits would allow trees to achieve higher hydraulic efficiency with relatively low-cost wood and hence contribute to the maximization in allocation to organs for resource acquisition and carbon assimilation (Zhu et al. 2013). ...
Characterizing differences in key functional traits between simple-leaved (SL) and compound-leaved (CL) tree species can contribute to a better understanding of the adaptive significance of compound leaf form. In particular, this information may provide a mechanistic explanation to the long-proposed fast-growth hypothesis of CL tree species. Here, using five SL and five CL tree species co-occurring in a typical temperate forest of Northeast China, we tested whether higher hydraulic efficiency underlies potentially high photosynthetic capacity in CL species. We found that the CL species had significantly higher hydraulic conductance at the whole-branch level than the SL species (0.52 ± 0.13 vs 0.15 ± 0.04 × 10 −4 kg m −2 s −1 Pa −1 , P = 0.029). No significant difference in net photosynthetic rate (14.7 ± 2.43 vs 12.5 ± 2.05 μmol m −2 s −1 , P = 0.511) was detected between these two groups, but this was largely due to the existence of one outlier species in each of the two functional groups. Scrutinization of the intragroup variations in functional traits revealed that distinctions of the two outlier species in wood type (ring-vs diffuse-porous) from their respective functional groups have likely contributed to their aberrant physiological performances. The potentially high photosynthetic capacity of CL species seems to require ring-porous wood to achieve high hydraulic efficiency. Due to its limitation on leaf photosynthetic capacity, diffuse-porous wood with lower hydraulic conductivity largely precludes its combination with the 'throw-away' strategy (i.e., annually replacing the stem-like rachises) of compound-leaved tree species, which intrinsically requires high carbon assimilation rate to compensate for their extra carbon losses. Our results for the first time show clear differentiation in hydraulic architecture and CO 2 assimilation between sympatric SL and CL species, which contributes to the probing of the underlying mechanism responsible for the potential fast growth of trees with compound leaves.
... Maherali, Pockman & Jackson, 2004;Choat et al. 2012;Scoffoni, McKown, Rawls & Sack, 2012) few studies have evaluated the simultaneous coordination of different portions of hydraulic pathway (e.g. Bucci et al., 2012Bucci et al., , 2013Nolf et al., 2015;Li, Chen, Chen & Shi, 2016;Skelton et al., 2018). ...
... Although total annual precipitation is homogenous in the study area, there are edaphic differences such that the two species with highest K Leaf and k s are more abundant in lowland sites with relatively wetter soils (Ramirez, San Martín & San Martín, 1996). Both K Leaf and k s were strongly and positively coordinated across species, similar to relationships found in others studies Nolf et al., 2015). ...
The hydraulic coordination along the water transport pathway helps trees provide adequate water supply to the canopy ensuring that water deficits are minimized and that stomata remain open for CO2 uptake. We evaluated the stem and leaf hydraulic coordination and the linkages between hydraulic traits and the timing of diurnal depression of photosynthesis across seven evergreen tree species in the southern Andes. There was a positive correlation between stem hydraulic conductivity (ks) and leaf hydraulic conductance (KLeaf) across species. All species had similar maximum photosynthetic rates (Amax). The species with higher ks and KLeaf attained Amax in the morning while the species with lower ks and KLeaf exhibited their Amax in the early afternoon concurrently with turgor loss. These latter species had very negative leaf water potentials, but far from the pressure at which the 88% of leaf hydraulic conductance is lost. Our results suggest that diurnal gas exchange dynamics may be determined by leaf hydraulic vulnerability such that a species more vulnerable to drought restrict water loss and carbon assimilation earlier than species less vulnerable. However, under stronger drought, species with earlier CO2 uptake depression may increase the risk of hydraulic failure as their safety margins are relatively narrow. Stem and leaf hydraulic traits were positively correlated across temperate evergreen tree species. While all species had similar maximum photosynthesis rates, the diurnal depression occurred earlier in species with higher hydraulic efficiency and leaves more vulnerable to drought than in the species less efficient but more resistance to loss of leaf hydraulic conductance.
... Stem hydraulic vulnerability (VC stem ) was determined from three branches, each from a separate tree unaffected by dieback using the bench-top dehydration method, as described elsewhere (Nolf et al. 2015). From these same branches, we also measured leaf hydraulic vulnerability using the timed rehydration kinetics method (Brodribb and Holbrook 2003). ...
... In our study species, leaves were more hydraulically vulnerable than stems, which is consistent with a number of recent studies in support of hydraulic vulnerability segmentation (Pivovaroff et al. 2014, Nolf et al. 2015, Zhang et al. 2017; but see Villagra et al. 2013, Zhu et al. 2016). Although we did not measure leaf water potentials in situ, at the peak of water stress during the 2017 winter-spring drought, we speculate that dieback-affected trees of E. piperita most likely reached minimum water potentials between −2 and −4 MPa, which corresponds to the levels of embolism observed across individual branchlets, in association with stem vulnerability ( Figure 5). ...
Manipulative experiments have suggested that embolism-induced hydraulic impairment underpins widespread tree mortality during extreme drought, yet in situ evidence is rare. One month after drought-induced leaf and branch dieback was observed in field populations of Eucalyptus piperita Sm. in the Blue Mountains (Australia), we measured the level of native stem embolism and characterized the extent of leaf death in co-occurring dieback and healthy (non-dieback) trees. We found that canopy dieback-affected trees showed significantly higher levels of native embolism (26%) in tertiary order branchlets than healthy trees (11%). Furthermore, there was a significant positive correlation (R2 = 0.51) between the level of leaf death and the level of native embolism recorded in branchlets from dieback-affected trees. This retrospective study suggests that hydraulic failure was the primary mechanism of leaf and branch dieback in response to a natural drought event in the field. It also suggests that post-drought embolism refilling is minimal or absent in this species of eucalypt.
... Also, deep root and dense root system together with stomatal closure and leaf area reduction enhanced in maximizing water uptake which improve plant water status especially by turgor maintenance and important for maintaining physiological activity in extended drought stress [35,50]. Moisture deficit tolerant coffee genotypes showed narrow conducting xylem, high wood density (D w ) and fiber wall thickness [1,49] which increase water use efficiency, control hydraulic conductance and lessening water leaf potential tension [51]. Drought stress tolerant genotypes stay green under sever soil water deficit due to their deep root and water saving ability [52]. ...
... Leaves and roots represent the primary regions of resistance to the flow of water within a plant: in both cases due to the necessary flow path outside the xylem where very large frictional costs are incurred as water moves between and into the living cells (Tyree & Cheung, 1977;Frensch & Steudle, 1989;Steudle & Peterson, 1998;Wolfe et al., 2023). Leaves play an essential role in photosynthesis and transpiration and have commonly been observed to cavitate earlier than stems during drought (Choat et al., 2005;Brodribb & Cochard, 2009;Nolf et al., 2015;Charrier et al., 2016;Zhu et al., 2016;Scoffoni & Sack, 2017;Skelton et al., 2019;Mantova et al., 2023), although exceptions exist (Klepsch et al., 2018;Levionnois et al., 2020;Guan et al., 2022). Consequently, a large body of work has carefully examined leaf hydraulic traits such as the vessel size and xylem vulnerability to cavitation to understand the loss of hydraulic function within leaves and across canopies (Scoffoni et al., 2017b;Blackman et al., 2018;Cardoso et al., 2020;Johnson et al., 2022). ...
The propagation of xylem embolism throughout the root systems of drought‐affected plants remains largely unknown, despite this process being comparatively well characterized in aboveground tissues.
We used optical and X‐ray imaging to capture xylem embolism propagation across the intact root systems of bread wheat ( Triticum aestivum L. ‘Krichauff’) plants subjected to drying. Patterns in vulnerability to xylem cavitation were examined to investigate whether vulnerability may vary based on root size and placement across the entire root system.
Individual plants exhibited similar mean whole root system vulnerabilities to xylem cavitation but showed enormous 6 MPa variation within their component roots ( c . 50 roots per plant). Xylem cavitation typically initiated in the smallest, peripheral parts of the root system and moved inwards and upwards towards the root collar last, although this trend was highly variable.
This pattern of xylem embolism spread likely results in the sacrifice of replaceable small roots while preserving function in larger, more costly central roots. A distinct pattern of embolism‐spread belowground has implications for how we understand the impact of drought in the root system as a critical interface between plant and soil.
... The hydraulic vulnerability segmentation hypothesis uses patterns of tissue preservation and sacrifice to consider the carbon investment and cost of losing tissues under drought (Tyree and Ewers, 1991;Tsuda and Tyree, 1997;Choat et al., 2005;Hochberg et al., 2016). The theory suggests more long-lived non-redundant structures such as stems that require large carbon investments should be more resistant to embolism and persist longer under water stress than short-lived distal tissues such as leaves (Cochard et al., 1992;Zimmermann, 2013;Pivovaroff et al., 2014;Nolf et al., 2015;Charrier et al., 2016, Johnson et al., 2016. This theory was developed to examine the variation in vulnerability between leaves and stems but may be applied more broadly across whole plants. ...
Background and aims:
Many annual grasses exhibit drought avoiding life cycles where rapid reproduction must be completed before soil water is exhausted. This strategy would seem to require a hydraulic system capable of sustaining reproduction at all costs to the rest of the plant, yet little is known about the whole-plant structure of hydraulic vulnerability in grasses.
Methods:
We examine vulnerability to water-stress induced xylem cavitation in roots, flag leaves, basal and apical regions of peduncles of wheat (Triticum aestivum var Krichauff) to understand the staged failure of xylem function in severe drought. The functionality of segmented vulnerabilities is tested by conducting rehydration experiments after acute dehydration.
Key results:
We show the water supply to peduncles is more drought resistant than in leaves due to greater xylem cavitation resistance, ensuring a pathway of water can be maintained from the roots to the reproductive tissues even after severe water deficit. Differential rehydration of peduncles compared to leaves following drought confirmed the functionality of xylem supply from roots to seed after water stress sufficient to completely cavitate flag leaf vessels.
Conclusions:
These results demonstrate that a proportion of the hydraulic pathway between roots and seeds remains functional under extreme dehydration, suggesting that vulnerability traits in this key grass species reflect its reproductive strategy.
... Branches were immediately transported to the laboratory, with the cut end being maintained under water and placed in darkness for rehydration. During rehydration, Ψ L was measured periodically to assess the water status of the branch, assuming equilibrium in water potential across organs for non-transpiring samples (Nolf et al., 2015;Rodriguez-Dominguez et al., 2022). Branches were considered well-rehydrated when Ψ L ≥ − 0.5 MPa. ...
Irrigation is essential for sustaining the productivity of plantation forests in arid, semi-arid, and seasonal drought regions. Current irrigation management is commonly scheduled based on time or soil water status, which often fails to capture plant physiological demand. Here we report on the variation of traits related to plant water use for 7-year-old Populus tomentosa plantations under different irrigation treatments in North China during two growth seasons with contrasting environmental dryness. Plant hydraulics were assessed by stomatal regulation strategy as well as hydraulic traits conferring water transport efficiency and safety, including branch hydraulic conductivity (Ks), thresholds for xylem embolism (Px) and percentage loss of leaf rehydration capacity (PLRC), leaf water potential at turgor loss point (Ψtlp) as well as hydraulic capacitance before and after turgor loss (Cbulk-pre and Cbulk-post respectively). Our results showed that both seasonal increases in rainfall and irrigation could modify stomatal regulation strategy, resulting in a more anisohydric stomatal behavior, but through different underlying mechanisms. Specifically, seasonal variation in stomatal regulation was primarily manipulated by the daily fluctuation of leaf water potential, Ψtlp, and possibly the water supply-demand relationship. At the same time, we speculated that irrigation-dependent alternation was presumably associated with shifted belowground traits. Seasonal variation in hydraulic traits was found for Ks and Ψtlp, with trees in the dry season displaying higher Ks and less negative Ψtlp regardless of irrigation, while other traits governing hydraulic functioning were essentially invariable across seasons or irrigation treatments. Tree growth rate was lower in the wet season and was independent of irrigation, which was likely explained by the occurrence of hydraulic impairment due to less stringent stomatal control. Overall, our results suggest that limited precipitation and high atmospheric vapor pressure deficit in the dry season would not compromise tree growth because of the tighter stomatal control, while hydraulic dysfunction could occur in the wet season due to excessive water use strategy, subsequently perhaps contributing to the reduction in growth rate. The findings of this study underscore the usefulness of physiological traits in guiding irrigation management and advocate reconsidering plantation water management strategy based on reliable indicators.
... Such reductions in water-delivering capacity can at least partially be responsible for the reduced productivity of species Zhu et al., 2018). Consistently, it has been found at the global scale that species of varying environments function with relatively small hydraulic safety margins to balance the need to maximize photosynthetic carbon assimilation and guarantee hydraulic integrity (Choat et al., 2012;Nolf et al., 2015). growing' strategy along a fast-slow economics spectrum (Brouillette et al., 2014). ...
Xylem hydraulic characteristics govern plant water transport, affecting both drought resistance and photosynthetic gas exchange. Therefore, they play critical roles in determining the adaptation of different species to environments with various water regimes. Here, we tested the hypothesis that variation in xylem traits associated with a trade-off between hydraulic efficiency and safety against drought-induced embolism contributes to niche differentiation of tree species along a sharp water availability gradient on the slope of a unique river valley located in a semi-humid area. We found that tree species showed clear niche differentiation with decreasing water availability from the bottom towards the top of the valley. Tree species occupying different positions, in terms of vertical distribution distance from the bottom of the valley, showed a strong trade-off between xylem water transport efficiency and safety, as evidenced by variations in xylem structural traits at both the tissue and pit levels. This optimised their xylem hydraulics in their respective water regimes. Thus, the trade-off between hydraulic efficiency and safety contributes to clear niche differentiation and, thereby, to the coexistence of tree species in the valley with heterogeneous water availability. This article is protected by copyright. All rights reserved.
... In the plant-water transport system, the pressure gradient generated by transpiration in leaves enables water from the soil to move to the canopy under tension (Tyree and Zimmermann, 2002). During plant dehydration, increased xylem tension increases the risk of embolism (cavitation) in xylem conduits, which likely restricts water transport (Nolf et al., 2015). The plant hydraulic system is also tightly linked to water and metabolism of carbon (Christoffersen et al., 2016;Eller et al., 2018), such that plants might adjust their hydraulic traits to achieve an optimal carbon-water balance under changing environmental conditions. ...
Plant growth, photosynthesis, and hydraulics are affected by heavy metals but also by elevated atmospheric CO2 concentration (e[CO2]) and nitrogen (N) deposition. However, few studies have investigated the response of woody species to the combined effects of these three factors. We conducted an open-top chamber experiment with two common subtropical trees (Acacia auriculiformis and Syzygium hainanense) to explore the effects of cadmium (Cd)-contamination, e[CO2], and N addition on plant eco-physiological traits. We found that the growth of A. auriculiformis was insensitive to the treatments, indicating that it is a Cd-tolerant and useful afforestation species. For S. hainanense, in contrast, e[CO2] and/or N addition offset the detrimental effects of Cd addition by greatly increasing plant biomass and reducing the leaf Cd concentration. We then found that e[CO2] and/or N addition offset the detrimental Cd effects on S. hainanense biomass by increasing its photosynthetic rate, its N concentration, and the efficiency of its stem water transport network. These offsetting effects of e[CO2] and/or N addition, however, came at the expense of reduced xylem hydraulic safety resulting from wider vessels, thinner vessel walls, and therefore weaker vessel reinforcement. Our study suggests that, given future increases in global CO2 concentration and N deposition, the growth of Cd-tolerant tree species (like A. auriculiformis) will be probably stable while the growth of Cd-sensitive tree species (like S. hainanense) might be enhanced despite reduced hydraulic safety. This also suggests that both species will be useful for afforestation of Cd-contaminated soils given future global change scenarios.
... Due to differences in experimental conditions and settings, these studies could not be directly compared to the results from this study. Nonetheless, measured values of Ψ md from this study were within the ranges of those observed in Neotropics 21,26,34,35 , Australasia 36,37 , and Indomalaya [38][39][40] . For xylem vulnerability, results from this study were within similar ranges of those from Neotropics 26,34 and Indomalaya 38,40 , but were lower than those shown in the other studies in Table S1. ...
Large-scale abandoned agricultural areas in Southeast Asia resulted in patches of forests of multiple successions and characteristics, challenging the study of their responses to environmental changes, especially under climatic water stress. Here, we investigated seasonal variation in leaf water status and drought tolerance of dominant tree species in three multi-aged tropical forests, ranging from 5 to > 200 years old, with contrasting soil moisture in Thailand. Seasonal variation in leaf water status differed among the forests with trees in young and intermediate sites demonstrating larger differences between seasons than the old-growth forest. Although vulnerability to embolism curves revealed that trees in old-growth forest were potentially more sensitive to declining leaf water status than others, they were predicted to lose < 5% of their hydraulic capacity as opposed to 13% for the trees in the younger sites. Our results suggest that the responses to water stress of tree species in different forest ages greatly vary with a tendency of trees in younger sites to be more resilience than those in older sites. Such information would benefit the selection of tree species that could adapt well to specific environments, thus improving the strategies for managing forests of different ages under a warmer future.
... The high limitation on the plant carbon assimilation capacity under soil water deficient conditions has been a major reason for plant growth and crop productivity reduction (Hussain et al., 2021;Nolf et al., 2015). It is widely accepted that there are two ways in which water stress affects the photosynthesis of plants: one is the stomatal limitations, such as closing the stoma and lowering the stomatal conductance (Daryanto, Wang & Jacinthe, 2017;Talbi et al., 2020); the other is non-stomatal limitations, such as photosynthetic phosphorylation (Du et al., 2021), regeneration of ribulose-1,5-bisphosphate (RuBP) (Song et al., 2016a), activation of Rubisco and the synthesis of ATP (Ashraf & Harris, 2013;Hu et al., 2020). ...
Background
As a fundamental metabolism, leaf photosynthesis not only provides necessary energy for plant survival and growth but also plays an important role in global carbon fixation. However, photosynthesis is highly susceptible to environmental stresses and can be significantly influenced by future climate change.
Methods
In this study, we examined the photosynthetic responses of Phragmites australis ( P . australis ) to three precipitation treatments (control, decreased 30%, and increased 30%) under two thermal regimes (ambient temperature and +4 °C) in environment-controlled chambers.
Results
Our results showed that the net CO 2 assimilation rate ( P n ), maximal rate of Rubisco ( V cmax ), maximal rate of ribulose-bisphosphate (RuBP) regeneration ( J max ) and chlorophyll (Chl) content were enhanced under increased precipitation condition, but were declined drastically under the condition of water deficit. The increased precipitation had no significant effect on malondialdehyde (MDA) content ( p > 0.05), but water deficit drastically enhanced the MDA content by 10.1%. Meanwhile, a high temperature inhibited the positive effects of increased precipitation, aggravated the adverse effects of drought. The combination of high temperature and water deficit had more detrimental effect on P . australis than a single factor. Moreover, non-stomatal limitation caused by precipitation change played a major role in determining carbon assimilation rate. Under ambient temperature, Chl content had close relationship with P n (R ² = 0.86, p < 0.01). Under high temperature, P n was ralated to MDA content (R ² = 0.81, p < 0.01). High temperature disrupted the balance between V cmax and J max (the ratio of J max to V cmax decreased from 1.88 to 1.12) which resulted in a negative effect on the photosynthesis of P . australis . Furthermore, by the analysis of Chl fluorescence, we found that the xanthophyll cycle-mediated thermal dissipation played a major role in PSII photoprotection, resulting in no significant change on actual PSII quantum yield ( Φ PSII ) under both changing precipitation and high temperature conditions.
Conclusions
Our results highlight the significant role of precipitation change in regulating the photosynthetic performance of P . australis under elevated temperature conditions, which may exacerbate the drought-induced primary productivity reduction of P . australis under future climate scenarios.
... Two indirect techniques were used to construct the vulnerability curves at branch and leaf level, namely, the AV method and OV method. Both of them have been validated several times using other methods (see e.g., Nolf et al., 2015b;De Baerdemaeker et al., 2019b;Steppe et al., 2022 for the AV method and Skelton and Diaz, 2020 for the OV method), so it was decided not to repeat this validation in this study. The AV method was, for example, validated by Vergeynst et al. (2015) comparing the AV results with simultaneously acquired X-ray micro-computed tomography (µCT) images. ...
Lianas are a key growth form in tropical forests. They are believed to be strong competitors for water, thanks to their presumed efficient vascular systems. However, despite being a large polyphyletic group, they are currently often considered as a functionally homogeneous entity. In this study, we challenged this assumption by estimating the variability in hydraulic traits of two common, co-occurring liana species in a water-limited environment, namely, a seasonally dry tropical forest in Costa Rica. We measured vulnerability to embolism at the leaf and branch levels using two different methods (optical and acoustic vulnerability) and found that both species had very different hydraulic properties. Compared to reported P 50 values in literature, we found two extreme P 50 values: a low value for Bignonia diversifolia (−4.30 ± 0.54 MPa at the leaf level; −7.42 ± 0.54 MPa at the branch level) and a high value for Cissus microcarpa (−1.07 ± 0.14 at the leaf level; −1.20 ± 0.05 MPa at the branch level). Furthermore, B. diversifolia had a higher apparent modulus of elasticity in the radial direction (556.6 ± 401.0 MPa) and a variable midday water potential. On the other hand, C. microcarpa had a low apparent modulus of elasticity in the radial direction (37.8 ± 26.3 MPa) and a high branch water content, which enabled the species to keep its water potential stable during the dehydration experiments and during a drought period in the field. This mechanism may enable this species to coexist with species that are more resistant to drought-induced embolisms such as B. diversifolia . Although only two species were studied, considerable overlap was found between the range of hydraulic properties of trees growing in the same location and trees and lianas growing in two forests in Panama. These findings demonstrate that lianas cannot be considered as a homogeneous group and call for further research into the intra-growth form diversity of liana properties.
... Some parameters even returned to pre-drought levels Phillips et al., 2010). Plants can maintain a relative dynamic balance under changing inter-annual fluctuations by developing adaptive strategies such as stomatal behavior (McDowell et al., 2008), osmotic regulation (Binks et al., 2016), hydraulic system regulation (Rita et al., 2015;Tomasella et al., 2018), deciduous behavior (Mendivelso et al., 2014), non-structural carbon buffering (O'Brien et al., 2014), utilization of deeper soil water (Bréda et al., 2006;Brunner et al., 2015) and hydraulic segmentation (Nolf et al., 2015). These strategies enable plants to survive under a certain degree of drought stress and restore when the environment recovers to an ideal state. ...
Studies on the effects of drought on tropical rainforests have revealed their sensitivity on multiple levels, for example, decreased photosynthetic capacity and increased mortality. However, studies on the impact of occasional drought on the rainforests are not enough as they tend to recover from such droughts within a few years. In the present study, the Xishuangbanna rainforest, located at the northern edge of Asia, witnessed extensive damage after six years of a field drought treatment (30 m × 30 m plot; ∼35% through-fall reduction): the plant carbon pool decreased at the rate of 13.71 T ha−1 yr−1 (amount to 23% loss of plant carbon in the 10th year compared to the 7th), although soil carbon accumulated at the rate of 2.68 T ha−1 yr−1. The radial growth rate of the surviving tagged trees was not constrained by drought. Additionally, drought reduced the number of seedlings per unit area by 61% compared to the control plot. The residual analysis indicates that the net ecosystem carbon exchange (NEE) of eddy covariance (EC) flux site was insensitive to soil drought on annual scale, while regression analyses showed that photosynthetic light response parameters were inhibited by drought on decalal scale. The results of both drought experiment and flux data analysis showed that the impact of drought on the rainforest will be highly apparent on long-term scale. In order to predict the fate of forests more accurately in response to prolonged drought, it is worth reassessing the long-term drought sensitivity of forest ecosystems.
... Nevertheless, this response did not reduce the overall hydraulic safety margin (MPa) in drought-acclimated plants due to the relatively large increase (in MPa) in stem embolism resistance. We may have also expected to see a similar coordinated response between leaf and stem vulnerability to embolism in water-limited plants, considering their fine-tuned coordination in many species (Pivovaroff et al. 2014a, Nolf et al. 2015, Creek et al. 2018, Levionnois et al. 2020. However, the difference in leaf vulnerability between treatments was non-significant and had very little effect on THF (data not shown). ...
The capacity of trees to tolerate and survive increasing drought conditions in situ will depend in part on their ability to acclimate (via phenotypic plasticity) key hydraulic and morphological traits that increase drought tolerance and delay the onset of drought-induced hydraulic failure. However, the effect of water deficit acclimation in key traits that determine time to hydraulic failure (THF) during extreme drought remains largely untested.
We measured key hydraulic and morphological traits in saplings of a hybrid poplar grown under well-watered and water-limited conditions. The time for plants to dry-down to critical levels of water stress (90% loss of stem hydraulic conductance), as well as the relative contribution of drought acclimation in each trait to THF, was simulated using a soil–plant hydraulic model (SurEau).
Compared to controls, water-limited plants exhibited significantly lower stem hydraulic vulnerability (P50stem), stomatal conductance (gs) and total canopy leaf area (LA). Taken together, adjustments in these and other traits resulted in longer modeled THF in Water-limited (~160 hours) compared to Well-watered plants (~50 hours), representing an increase of more than 200%. Sensitivity analysis revealed that adjustment in P50stem and LA contributed the most to longer THF in Water-limited plants.
We observed a high degree of trait plasticity in poplar saplings in response to water-deficit growth conditions, with decreases in stem hydraulic vulnerability and leaf area playing a key role in delaying the onset of hydraulic failure during a simulated drought event. These findings suggest that understanding the capacity of plants to acclimate to antecedent growth conditions will enable better predictions of plant survivorship during future drought.
... Hydraulic vulnerability segmentation may be especially helpful to basal angiosperms, whose survival during protracted drought may depend on reducing the evaporative leaf area and isolating roots from drying soils while preserving the hydraulic integrity of less-redundant stems. Recent studies have suggested that the level of vulnerability segmentation exhibited by different plant species is influenced by climate, with strong segmentation detected in species from semiarid, temperate, and seasonally dry environments (Martinez-Vilalta et al., 2002, Pivovaroff et al., 2014, Johnson et al., 2016, Wolfe et al., 2016, Zhu et al., 2016, whereas weak and/or absent segmentation is detected in species from more mesic environments (Villagra et al., 2013;Nolf et al., 2015;Zhu et al., 2016) and herbs (Skelton et al., 2017). A case in point, M. insignis, a species whose xylem vessels possess scalariform perforation plates, showed weak hydraulic vulnerability segmentation, which explains its high vulnerability to drought. ...
Basal angiosperms have relatively primitive hydraulic systems and may be vulnerable to drought. The coordination in hydraulic function between leaf, stem and root of a plant during and after a drought is not well understood. Here, we examined the interaction between gas exchange and hydraulic function in the leaves, stems, and intact root systems of potted-seedlings of three evergreen basal angiosperm tree-species exposed to a cycle of severe water stress and subsequent rewatering. In all three species, stomatal closure occurred at water potentials before 50% loss of stem hydraulic conductivity, because their leaves and roots were more vulnerable to drought than the stems. Manglietia insignis that has scalariform perforatiom plates was more vulnerable to drought than the other two species that have simple porforation plates. During rewatering, water potentials of D. chinensis and C. camphora were recovered after 10 days, their gas exchange were gradually recovered and reached to pre-drought levels after 3 weeks, whereas, the recovery of hydraulic function in their leaves, stems and roots lagged behind but also reached pre-drought levels after 3 weeks. Manglietia insignis displayed poor recovery in both gas exchange and hydraulic function and a high mortality. Our results reveal that drought-induced severe embolism can be recovered even in seedlings of basal angiosperms depending on species if a drought does not persist long, and earlier recovery in xylem water potential and gas exchange than hydraulic function.
... This suggests that effective stem xylem transport could mediate leaf acquisitive traits, e.g. SLA (Santiago et al. 2004, Zhang and Cao 2009, Zhu and Cao 2009, Nolf et al. 2015. ...
The scandent shrub plant form is a variant of liana that has upright and self-supporting stems when young but later becomes a climber. We aimed to explore the associations of stem and leaf traits among sympatric lianas, scandent shrubs and trees, and the effects of growth form and leaf habit on variation in stem or leaf traits. We measured 16 functional traits related to stem xylem anatomy, leaf morphology and nutrient stoichiometry in eight liana, eight scandent shrub and 21 tree species co-occurring in a subalpine cold temperate forest at an elevation of 2,600-3,200 m in Southwest China. Overall, lianas, scandent shrubs and trees were ordered along a fast-slow continuum of stem and leaf functional traits, with some traits overlapping. We found a consistent pattern of lianas > scandent shrubs > trees for hydraulically weighted vessel diameter, maximum vessel diameter and theoretical hydraulic conductivity. Vessel density and sapwood density showed a pattern of lianas = scandent shrubs < trees, and lianas < scandent shrubs = trees, respectively. Lianas had significantly higher specific leaf area and lower carbon concentration than co-occurring trees, with scandent shrubs showing intermediate values that overlapped with lianas and trees. The differentiation among lianas, scandent shrubs and trees was mainly explained by variation in stem traits. Additionally, deciduous lianas were positioned at the fast end of the trait spectrum, and evergreen trees at the slow end of the spectrum. Our results showed for the first time clear differentiation in stem and leaf traits among sympatric liana, scandent shrub and tree species in a subalpine cold temperate forest. This work will contribute to understanding the mechanisms responsible for variation in ecological strategies of different growth forms of woody plants.
... For example, genotypes with high K root-r also had high k stem-sw and K shoot-l . This suggests that hydraulics traits of a given organ could be proportionally scaled by the hydraulic traits of another plant organ or whole plant (Sack et al., 2003, Pratt et al., 2010Nolf et al., 2015;Rodríguez-Gamir et al., 2019). This would explain why many studies have related hydraulic conductance traits at organ level to tree growth rates Fan et al., 2012) or gas exchange parameters (Brodribb and Feild, 2000;Aasamaa and Sõber 2001;Clearwater and Meinzer, 2001;Sack et al., 2003;Brodribb et al., 2005). ...
Stem growth reflects genetic and phenotypic differences within a tree species. The plant hydraulic system regulates the carbon economy, and therefore variations in growth and wood density. A whole-organism perspective, by partitioning the hydraulic system, is crucial for understanding the physical and physiological processes that co-ordinately mediate plant growth. The aim of this study was to determine whether the relationships and trade-offs between (1) hydraulic traits and their relative contribution to whole-plant hydraulic system, (2) plant water transport, (3) CO2 assimilation, (4) plant growth and (5) wood density are revealed at inter-clonal level within a variable population of ten Pinus radiata (D. Don) clones for these characters. We demonstrated strong coordination between several plant organs regarding their hydraulic efficiency. Hydraulic efficiency, gas exchange and plant growth were intimately linked. Small reductions in stem wood density were related to large increase in sapwood hydraulic efficiency, and thus with plant growth. However, stem growth rate was negatively related with wood density. We discuss insights explaining the relationships and trade-offs of plant traits examined in this study, which provide better understanding of the existing coordination, likely genetic-dependent, between biophysical structure of wood, plant growth, hydraulic partitioning and physiological plant functions in P. radiata.
... Narrow or negative HSM leaf indicates a high risk of leaf hydraulic failure under drought [10,17]. The vulnerability segmentation hypothesis suggests that leaves are more vulnerable to cavitation than stems, and early decline in leaf hydraulic conductance could prevent water loss and protect the main stems from hydraulic dysfunction [15,[18][19][20]. Indeed, species with narrower HSM leaf values tend to have stronger leaf-to-stem vulnerability segmentation [20,21]. ...
Leaf hydraulic conductance and the vulnerability to water deficits have profound effects on plant distribution and mortality. In this study, we compiled a leaf hydraulic trait dataset with 311 species-at-site combinations from biomes worldwide. These traits included maximum leaf hydraulic conductance ( K leaf ), water potential at 50% loss of K leaf (P50 leaf ), and minimum leaf water potential ( Ψ min ). Leaf hydraulic safety margin (HSM leaf ) was calculated as the difference between Ψ min and P50 leaf . Our results indicated that 70% of the studied species had a narrow HSM leaf (less than 1 MPa), which was consistent with the global pattern of stem hydraulic safety margin. There was a positive relationship between HSM leaf and aridity index (the ratio of mean annual precipitation to potential evapotranspiration), as species from humid sites tended to have larger HSM leaf . We found a significant relationship between K leaf and P50 leaf across global angiosperm woody species and within each of the different plant groups. This global analysis of leaf hydraulic traits improves our understanding of plant hydraulic response to environmental change.
... Cavitation in the leaf, petiole, or midrib has been suggested as a mechanism to provide segmentation of the plant; isolating embolism to the more distal organs and thus reducing whole-plant water loss (Zimmermann, 1983;Pivovaroff et al., 2014;Nolf et al., 2015;Charrier et al., 2016;Johnson et al., 2016). Whereas cavitation in the petiole is likely to lead to loss of the entire leaf, embolism in the higher order veins could leave part of the venation system of leaves intact and functioning. ...
Vascular networks in plant leaves must provide for the safe and efficient transport of water, nutrients, and energy; however, the conditions whereby these networks lose and regain conductive capacity are still poorly understood. We measured the loss and recovery of leaf hydraulic conductance (Kleaf) in a tropical monocotyledon (Bambusa vulgaris) and dicotyledon species (Bauhinia blakeana) using Rehydration Kinetics Method (RKM) as well as a recently developed optical method. We found that both species lost ca 88% of their maximal Kleaf (measured by RKM) before any embolization was detected in their conductive elements (via optical observation). This suggests that the majority of loss in Kleaf, as measured with RKM, was associated with resistances other than embolization. Furthermore, embolism in B. vulgaris, a species known to generate root pressure, was reversed when rehydrated under positive pressure (120 kPa), but not under atmospheric pressure. In contrast, embolism was not reversed in B. blakeana under either elevated or atmospheric pressure. However, reductions in Kleaf that was not associated with embolization was recovered by this species when rehydrated under atmospheric conditions, whereas B. vulgaris did not exhibit any recovery under the same conditions. We suggest that root pressure is an adaptive mechanism allowing for the reversal of embolism and the recovery of extraxylary conductance. The absence of embolism reversal in B. blakeana suggests that embolization may be permanent without neutral or positive xylem pressure, but that the recovery of extraxylary conductance can be regained routinely in this species in the absence of root pressure.
... Experimental studies testing the segmentation and vulnerability segmentation hypotheses have produced inconsistent results, which could in part arise from methodological discrepancies when the cause of hydraulic decline of different organs is examined. Much of the previously published literature measuring hydraulics characteristics of different organs indicates that leaves and petioles are generally more vulnerable to embolism than stems, thus providing evidence in support of the vulnerability segmentation hypothesis (Tyree et al. 1993;Choat et al. 2005;Pivovaroff et al. 2014;Nolf et al. 2015;Johnson et al. 2016). However, vulnerability curves used for these comparisons have been generated using a wide range of techniques and this causes some complications for interpretation Trifilo et al. 2014;Torres-Ruiz et al. 2015a, b). ...
Context
Hydraulic failure and disconnection of distal organs during protracted drought stress is thought to protect large branches or trunks by reducing water loss and restricting the spread of embolism. Hydraulic segmentation and preferential sacrifice of distal organs such as leaves can be driven by two mechanisms: more negative water potentials at the terminal section of the hydraulic pathway and/or by higher vulnerability to xylem embolism of distal organs. Although vulnerability segmentation has been reported in the literature, the generality of this phenomenon is unclear, in part due to the methodological limitations related to direct measurement of xylem vulnerability to embolism in intact plants.
Aims
The objective of this study was to evaluate vulnerability segmentation between petioles and stems using non-invasive micro computed tomography (microCT).
Methods
Vulnerability to embolism was measured in leaf petioles and subtending stems of four woody species (Betula pendula R., Liriodendron tulipifera L., Populus tremula L. and Olea europaea L.) with contrasting drought tolerances. In addition, previously published vulnerability data for petioles and stems were compiled from the literature to investigate the commonality of hydraulic segmentation across a wide range of woody species, with the vulnerability curve methodology distinguished.
Results
Using non-invasive imaging on intact plants, we found no evidence of hydraulic segmentation between petioles and stems of four angiosperm tree species, regardless of mechanism. Moreover, the literature dataset indicated that little or no difference in vulnerability to embolism is present between petioles and stems when vulnerability curves were constructed using methods specifically measuring the dynamics of xylem tissue during dehydration (e.g. optical visualization, MicroCT).
Conclusion
Our results suggest that vulnerability segmentation between stems and distal organs (petioles and leaves) is limited when only xylem tissue is considered. Large differences in vulnerability between stems and leaves are likely to be driven by extra-xylary components, rather than xylem embolism.
... However, hydraulic functions may be more integrated through plant organs than carbon economy. Indeed, several studies reported a coordination of hydraulic traits across plant organs in some tropical forest sites (Li et al., 2018;Meinzer, Johnson, Lachenbruch, McCulloh, & Woodruff, 2009;Meinzer et al., 2008;Nolf et al., 2015) and in global syntheses (Bartlett, Klein, Jansen, Choat, & Sack, 2016). Other hydraulic traits than π tlp are ...
Human activities modify the disturbance regimes of tropical forests. Since tropical forests host high biological diversity, understanding the role of biodiversity in ecosystem recovery pathways and the underlying ecological mechanisms is crucial to predict the fate of tropical ecosystems. Studies relying on regularly censused forest plots, rarely include disturbed forests, are not long enough to assess long‐term forest dynamics and often lack repeatability.
We used an individual‐based model of tropical forest growth to assess the effect of species and functional diversity on long‐term ecosystem recovery from disturbance. We manipulated the number of species and functional assemblages across a large number of simulations and simulated different levels of disturbance. To investigate the ecological mechanisms that underlie the effect of biodiversity on forest functioning along recovery pathways, we partitioned the net effect of biodiversity on ecosystem properties into complementarity and selection effects over time.
We found that functional diversity improved tropical forest resilience after a disturbance. The complementarity effect dominated soon after the disturbance but was progressively surpassed by a selection effect as more competitive species dominated the forest community. This pattern increased with the intensity of the disturbance.
Synthesis . We found that the mechanisms through which biodiversity influences forest functioning depend on the ecosystem state, shifting from a dominant complementarity effect in recently disturbed systems to a selection effect in systems disturbed a long time ago. Our results thus suggest that the time since the last disturbance is a key to understanding biodiversity–ecosystem functioning relationships in tropical forests and can help reconcile previous contrasting results obtained with snapshots of ecosystem state in empirical studies.
... However, hydraulic functions may be more integrated through plant organs than carbon economy. Indeed, several studies reported a coordination of hydraulic traits across plant organs in some tropical forest sites (Li et al., 2018;Meinzer, Johnson, Lachenbruch, McCulloh, & Woodruff, 2009;Meinzer et al., 2008;Nolf et al., 2015) and in global syntheses (Bartlett, Klein, Jansen, Choat, & Sack, 2016). Other hydraulic traits than π tlp are ...
Plants are enormously diverse in their traits and ecological adaptation, even within given ecosystems, such as tropical rainforests. Accounting for this diversity in vegetation models poses serious challenges. Global plant functional trait databases have highlighted general trait correlations across species that have considerably advanced this research program. However, it remains unclear whether trait correlations found globally hold within communities, and whether they extend to drought tolerance traits.
For 134 individual plants spanning a range of sizes and life forms (tree, liana, understorey species) within an Amazonian forest, we measured leaf drought tolerance (leaf water potential at turgor loss point, π tlp ), together with 17 leaf traits related to various functions, including leaf economics traits and nutrient composition (leaf mass per area, LMA; and concentrations of C, N, P, K, Ca and Mg per leaf mass and area), leaf area, water‐use efficiency (carbon isotope ratio), and time‐integrated stomatal conductance and carbon assimilation rate per leaf mass and area. We tested trait coordination and the ability to estimate π tlp from the other traits through model selection. Performance and transferability of the best predictive model were assessed through cross‐validation.
Here π tlp was positively correlated with leaf area, and with N, P and K concentrations per leaf mass, but not with LMA or any other studied trait. Five axes were needed to account for >80% of trait variation, but only three of them explained more variance than expected at random. The best model explained only 30% of the variation in π tlp , and out‐sample predictive performance was variable across life forms or canopy strata, suggesting a limited transferability of the model.
Synthesis . We found a weak correlation among leaf drought tolerance and other leaf traits within a forest community. We conclude that higher trait dimensionality than assumed under the leaf economics spectrum may operate among leaves within plant communities, with important implications for species coexistence and responses to changing environmental conditions, and also for the representation of community diversity in vegetation models.
... f ψ leaf = 0) when Ψ leaf is lower than −2MPa, while field observations showed that the stomata were still open and that leaves were photosynthesizing, even when Ψ leaf < −2MPa. The difference in water potential between leaf and stem is quite difficult to quantify in nature, as it varies largely with tree-species, growth environment and plant traits (Christoffersen et al., 2016;Nolf et al., 2015). Thus, including Ψ leaf in the g s models should be done by considering a more comprehensive quantification of the entire soil-plantatmosphere continuum (e.g. ...
Stomata regulate CO2 uptake for photosynthesis and water loss through transpiration. The approaches used to represent stomatal conductance (gs) in models vary. In particular, current understanding of drivers of the variation in a key parameter in those models, the slope parameter (i.e. a measure of intrinsic plant water‐use‐efficiency), is still limited, particularly in the tropics. Here we collected diurnal measurements of leaf gas exchange and leaf water potential (Ψleaf), and a suite of plant traits from the upper canopy of 15 tropical trees in two contrasting Panamanian forests throughout the dry season of the 2016 El Niño. The plant traits included wood density, leaf‐mass‐per‐area (LMA), leaf carboxylation capacity (Vc,max), leaf water content, the degree of isohydry, and predawn Ψleaf. We first investigated how the choice of four commonly used leaf‐level gs models with and without the inclusion of Ψleaf as an additional predictor variable influence the ability to predict gs, and then explored the abiotic (i.e. month, site‐month interaction) and biotic (i.e. tree‐species‐specific characteristics) drivers of slope parameter variation. Our results show that the inclusion of Ψleaf did not improve model performance and that the models that represent the response of gs to vapor pressure deficit performed better than corresponding models that respond to relative humidity. Within each gs model, we found large variation in the slope parameter, and this variation was attributable to the biotic driver, rather than abiotic drivers. We further investigated potential relationships between the slope parameter and the six available plant traits mentioned above, and found that only one trait, LMA, had a significant correlation with the slope parameter (R2=0.66, n=15), highlighting a potential path towards improved model parameterization. This study advances understanding of gs dynamics over seasonal drought, and identifies a practical, trait‐based approach to improve modeling of carbon and water exchange in tropical forests. This article is protected by copyright. All rights reserved.
... The significant correlation between stomatal density and G sref at t ¼ 0.6 was consistent with the study in Eucalytpus globulus, indicating higher g s observed in those trees with higher stomatal density in more favorable environments ). This result indicated that stem and leaf hydraulics are finely tuned to avoid embolism in the xylem (Locosselli and Ceccantini, 2012;M endez-Alonzo et al., 2012;Nolf et al., 2015). The co-ordination between wood density and stomatal morphology could potentially also be explained by the tradeoff between "efficiency" and "safety." ...
Transpiration through stomata in tree canopies plays an important role in terrestrial water cycles. However, the empirical relationship between leaf stomata anatomy and canopy stomatal conductance (Gs) is surprisingly rare, thereby the underlying biological mechanisms of terrestrial water flux are not well elucidated. To gain further insight into these mechanisms, we reanalyzed the dataset of Gs previously reported by Gao et al. (2015) using a quantile regression model. The results indicated that the reference Gs (Gsref, Gs at 1 kPa) was negatively correlated with wood density at each quantile, which confirmed previous data; however, Gsref was significantly correlated with stomatal density at the 0.6 quantile, i.e., 450 stomata mm−2. This highlighted the potential of using stomatal density as a trait to predict canopy water flux. A conceptual model of co-determinants of xylem and stomatal morphology suggests that these traits and their coordination may play a critical role in determining tree growth, physiological homeostatic response to environmental variables, water use efficiency, and drought resistance. Keywords: Gsref, Quantile regression, Stomatal density, Water flux, Wood density
... Trees cope with drought stress either through drought avoidance mechanisms that maintain tree water status by preventing water loss or increasing water delivery to leaves, or through tolerance mechanisms which help trees to function under low tissue water potentials when drought levels become too severe [9,10]. Stomatal closure prevents water loss, but also reduces CO 2 assimilation and negatively affects photosynthesis, ultimately affecting tree growth [11][12][13]. Drought tolerance mechanisms, on the other hand, could lead to tree death if stomata remain open for too long. ...
A population of eight open pollinated families of Pinus contorta was selected from sites varying in precipitation regimes and elevation to examine the possible role of aquaporins in adaptation to different moisture conditions. Five Pinus contorta aquaporins encoding PiconPIP2;1, PiconPIP2;2, PiconPIP2;3, PiconPIP1;2, and PiconTIP1;1 were cloned and detailed structural analyses were conducted to provide essential information that can explain their biological and molecular function. All five PiconAQPs contained hydrophilic aromatic/arginine selective filters to facilitate the transport of water. Transcript abundance patterns of PiconAQPs varied significantly across the P. contorta families under varying soil moisture conditions. The transcript abundance of five PiconPIPs remained unchanged under control and water-stress conditions in two families that originated from the sites with lower precipitation levels. These two families also displayed a different adaptive strategy of photosynthesis to cope with drought stress, which was manifested by reduced sensitivity in photosynthesis (maintaining the same rate) while exhibiting a reduction in stomatal conductance. In general, root:shoot ratios were not affected by drought stress, but some variation was observed between families. The results showed variability in drought coping mechanisms, including the expression of aquaporin genes and plant biomass allocation among eight families of Pinus contorta.
... Drought is a predominant environmental stress factor which is known to affect the physiological responses of terrestrial plants, by inhibiting carbon assimilation and which in turn affects the plant growth as well as yield of terrestrial plants (Nolf et al., 2015). Rapid increases in fossil fuel consumption, deforestation and industrialization contribute towards significant variations in global average air temperature and precipitation patterns, which are predicted to influence the frequency and severity of drought events in many regions of the world, particularly in mediterranean and subtropical climates (Martorell et al., 2014). ...
... Traditionally it has been suggested that leaves may function like fuses in the hydraulic circuit, embolizing early to protect more costly upstream tissues such as stems ( Zimmermann 1983;Nardini and Salleo 2000). This idea has generally been supported by studies of leaf vulnerabil- ity in woody plants ( Choat et al. 2005;Hao et al. 2007;Nolf et al. 2015), but not in herbs ( Skelton et al. 2017). Questions about the timing of leaf cavitation, and in particular the possibility of recovery or repair of K leaf after water stress, remains hotly debated. ...
In most terrestrial ecosystems, water availability is the principal governor of primary productivity. Vascular plants can only sustain high rates of photosynthetic activity by transporting enormous quantities of water from reserves in the soil to the sites of gas exchange in leaves to prevent desiccation of photosynthetic tissues. This demand for water requires plants to invest in a vascular system that begins as a simple pipe system in roots and branches and terminates in a sophisticated network of veins in the leaf. This chapter will examine the tight linkage between photosynthesis and the efficiency of water transport in leaves, explaining how plants use a non-living network of xylem to deliver water under high tension to evaporating cells. We explore how plants achieve high efficiency in water delivery by developing an intricately branched system of leaf veins as a means of piping water close to the stomatal layer, and how evolution has shaped the venation of higher plant species as densely reticulated networks.
... Appendix S4) reflect maximum conductance and that realized conductance can be limited by other factors (Tyree and Ewers, 1991). Nonetheless, this interpretation is consistent with the idea that hydraulic safety is a fundamental requirement for sound functional design in a system relying on a passive water transport system vulnerable to cavitation and foliar dehydration Sack and Holbrook, 2006;Markesteijn et al., 2011;Bucci et al., 2013;Liu et al., 2015;Nolf et al., 2015). ...
... Regulation of water use is often considered to be primarily domi- nated by interactions between xylem architecture and stomatal behav- ior ( McDowell et al., 2008). In many cases, vascular structure and stomatal response strategies may covary to optimize water use and offset risks associated with traits along the other axis (Manzoni, 2014;Manzoni, Vico, Katul, Palmroth, & Porporato, 2014;Nolf et al., 2015). However, several counterexamples exist. ...
... Water scarcity can produce xylem tension to surpass critical thresholds in trees, leading to embolism formation and the consequent blocking of the xylem water transport (Tyree and Sperry, 1989;Tyree and Zimmermann, 2002). This impairment may cause reductions in primary productivity and in more extreme cases tree mortality (Hartmann et al., 2013b;Nolf et al., 2015). The sensitivity of stem xylem to water stress can be measured using the vulnerability curve, which reveals the decline in hydraulic conductivity as water potential decreases. ...
... In relation to recovery strategies, growth of new xylem tissue would be expected to incur a significantly higher carbon cost compared with embolism repair. This paradigm is consistent with recent work showing the plants generally close stomata at water potentials above those causing any significant embolism (Nolf et al. 2015, Martin-StPaul et al. 2017, Li et al. 2018. ...
Drought stress can result in significant impairment of the plant hydraulic system via blockage of xylem conduits by gas emboli. Recovery after drought stress is an essential component of plant survival but is still a poorly understood process. In this study, we examined the capacity of woody species from two genera (Eucalyptus and Quercus) to refill embolized xylem vessels during a cycle of drought and recovery. Observations were made on intact plants of Eucalyptus calmudulensis, E. grandis, E. saligna and Quercus palustris using X-ray microtomography. We found no evidence of an effective xylem refilling mechanism in any of the plant species. Despite rehydration and recovery of plant water potential to near pre-drought levels, embolized vessels were not refilled up to 72 h after rewatering. In E. saligna, water droplets accumulated in previously air-filled vessels for a very small percentage of vessels. However, no instances of complete refilling that would restore embolized vessels to hydraulic function were observed. Our observations suggest that rapid refilling of embolized vessels after drought may not be a wide spread mechanism in woody plants and that embolism formed during drought represents long term cost to the plant hydraulic system.
... Our finding that the leaf-level hydraulic trait, π tlp , influences whole-plant functioning is in line with a body of evidence of hydraulic coordination among the different plant organs (Meinzer et al., 2008;Nolf et al., 2015). Measurement of π tlp is much easier than other drought tolerance traits in tropical forests. ...
Water availability is a key determinant of forest ecosystem function and tree species distributions. While droughts are increasing in frequency in many ecosystems, including in the tropics, plant responses to water supply vary with species and drought intensity and are therefore difficult to model. Based on physiological first principles, we hypothesized that trees with a lower turgor loss point ( π tlp ), that is, a more negative leaf water potential at wilting, would maintain water transport for longer into a dry season.
We measured sapflux density of 22 mature trees of 10 species during a dry season in an Amazonian rainforest, quantified sapflux decline as soil water content decreased and tested its relationship to tree π tlp , size and leaf predawn and midday water potentials measured after the onset of the dry season.
The measured trees varied strongly in the response of water use to the seasonal drought, with sapflux at the end of the dry season ranging from 37 to 117% (on average 83 ± 5 %) of that at the beginning of the dry season. The decline of water transport as soil dried was correlated with tree π tlp (Spearman’s ρ ≥ 0.63), but not with tree size or predawn and midday water potentials. Thus, trees with more drought‐tolerant leaves better maintained water transport during the seasonal drought.
Our study provides an explicit correlation between a trait, measurable at the leaf level, and whole‐plant performance under drying conditions. Physiological traits such as π tlp can be used to assess and model higher scale processes in response to drying conditions.
A plain language summary is available for this article.
... Based on the observation that community-mean WD tends to increase during forest succession, previous work has attempted to estimate WD from ALS-derived metrics such as TCH, but with mixed results (Asner & Mascaro 2014;Jucker et al. 2018). Here, we take a different approach which assumes that because leaf and stem traits are generally coordinated in trees (M endez-Alonzo et al. 2012;Nolf et al. 2015;Zeballos et al. 2017; although see Baraloto et al. 2010), we can use hyperspectral imagerywhich has been shown to reliably capture leaf properties (e.g. Asner et al. 2015) to also estimate WD. ...
Topography is a key driver of tropical forest structure and composition, as it constrains local nutrient and hydraulic conditions within which trees grow. Yet we do not fully understand how changes in forest physiognomy driven by topography impact other emergent properties of forests, such as their aboveground carbon density (ACD). Working in Borneo – at a site where 70-m- tall forests in alluvial valleys rapidly transition to stunted heath forests on nutrient-depleted dip-slopes – we combined field data with airborne laser scanning and hyperspectral imaging to characterize how topography shapes the vertical structure, wood density, diversity and ACD of nearly 15 km 2 of old-growth forest. We found that subtle differences in elevation – which control soil chemistry and hydrology – profoundly influenced the structure, composition and diversity of the canopy. Capturing these processes was critical to explaining landscape-scale heterogeneity in ACD, highlighting how emerging remote sensing technologies can provide new insights into longstanding ecological questions.
... Secondly, it is important to recognize that the hydraulic safety margin may differ when measured with reference to either leaf or stem vulnerability. This occurs because leaves tend to be more vulnerable (Pivovaroff et al. 2014, Nolf et al. 2015 to drought-induced hydraulic dysfunction than stems (but see Skelton et al. 2017), but the degree to which that occurs will depend on the strength of the vulnerability segmentation. In the current study, the relationship between low TLP and narrow leaf hydraulic safety is significant only in seasonally dry forests, which are likely to contain species with strong vulnerability segmentation, as noted by the authors. ...
... Based on the observation that community-mean WD tends to increase during forest succession, previous work has attempted to estimate WD from ALS-derived metrics such as TCH, but with mixed results (Asner & Mascaro 2014;Jucker et al. 2018). Here, we take a different approach which assumes that because leaf and stem traits are generally coordinated in trees (M endez-Alonzo et al. 2012;Nolf et al. 2015;Zeballos et al. 2017; although see Baraloto et al. 2010), we can use hyperspectral imagerywhich has been shown to reliably capture leaf properties (e.g. Asner et al. 2015) to also estimate WD. ...
Topography is a key driver of tropical forest structure and composition, as it constrains local nutrient and hydraulic conditions within which trees grow. Yet, we do not fully understand how changes in forest physiognomy driven by topography impact other emergent properties of forests, such as their aboveground carbon density (ACD). Working in Borneo – at a site where 70‐m‐tall forests in alluvial valleys rapidly transition to stunted heath forests on nutrient‐depleted dip slopes – we combined field data with airborne laser scanning and hyperspectral imaging to characterise how topography shapes the vertical structure, wood density, diversity and ACD of nearly 15 km2 of old‐growth forest. We found that subtle differences in elevation – which control soil chemistry and hydrology – profoundly influenced the structure, composition and diversity of the canopy. Capturing these processes was critical to explaining landscape‐scale heterogeneity in ACD, highlighting how emerging remote sensing technologies can provide new insights into long‐standing ecological questions.
Observations show vulnerability segmentation between stems and leaves is highly variable within and between environments. While a number of species exhibit conventional vulnerability segmentation (stem P 50 < ${P}_{50}\lt $ leaf P 50 ${P}_{50}$ ), others exhibit no vulnerability segmentation and others reverse vulnerability segmentation (stem P 50 > ${P}_{50}\gt $ leaf P 50 ${P}_{50}$ ). We developed a hydraulic model to test hypotheses about vulnerability segmentation and how it interacts with other traits to impact plant conductance. We do this using a series of experiments across a broad parameter space and with a case study of two species with contrasting vulnerability segmentation patterns: Quercus douglasii and Populus trichocarpa. We found that while conventional vulnerability segmentation helps to preserve conductance in stem tissues, reverse vulnerability segmentation can better maintain conductance across the combined stem-leaf hydraulic pathway, particularly when plants have more vulnerable P 50 ${P}_{50}$ s and have hydraulic segmentation with greater resistance in the leaves. These findings show that the impacts of vulnerability segmentation are dependent upon other plant traits, notably hydraulic segmentation, a finding that could assist in the interpretation of variable observations of vulnerability segmentation. Further study is needed to examine how vulnerability segmentation impacts transpiration rates and recovery from water stress.
Considerable evidences highlight the occurrence of increasing widespread tree mortality as a result of global climate change-associated droughts. However, knowledge about the mechanisms underlying divergent strategies of various tree species to adapt to drought has remained remarkably insufficient. Leaf stomatal regulation and embolism resistance of stem xylem serves as two important strategies for tree species to prevent hydraulic failure and carbon starvation, as comprising interconnected physiological mechanisms underlying drought-induced tree mortality. Hence, the physiological and anatomical determinants of leaf stomatal regulation and stems xylem embolism resistance are evaluated and discussed. In addition, root properties related to drought tolerance are also reviewed. Species with greater investment in leaves and stems tend to maintain stomatal opening and resist stem embolism under drought conditions. The coordination between stomatal regulation and stem embolism resistance are summarized and discussed. Previous studies showed that hydraulic safety margin (HSM, the difference between minimum water potential and that causing xylem dysfunction) is a significant predictor of tree species mortality under drought conditions. Compared with HSM, stomatal safety margin (the difference between water potential at stomatal closure and that causing xylem dysfunction) more directly merge stomatal regulation strategies with xylem hydraulic strategies, illustrating a comprehensive framework to characterize plant response to drought. A combination of plant traits reflecting species’ response and adaptation to drought should be established in the future, and we propose four specific urgent issues as future research priorities.
Accurately predicting global drought-induced tree mortality remains a major challenge facing plant science and ecology. Stem hydraulic safety margin (HSM, the difference between water potential at the minimum value and the value that causes xylem vulnerability to embolism) performs as one of the best hydraulic traits in predicting global drought-induced tree mortality, however, HSM is time-consuming and very difficult to measure. We proposed to use leaf turgor loss point (TLP, the water potential at which leaves start to wilt) as a proxy for HSM because HSM may be highly correlated to TLP, as both of them are tightly linked with water potential changes after stomatal closure. Since TLP is more easy and rapid to measure than HSM, if we find strong HSM-TLP relationships at the global scale, TLP can be used in predicting global drought-induced tree mortality. However, no study has quantified the relationships between HSM and TLP at the global scale. Here we draw together published data on HSM and TLP for 1,773 species from 370 sites worldwide to check whether HSM and TLP are highly associated. We found that HSMs and TLPs are merely highly related in tropical forests, thus TLP can be a reliable surrogate of HSM to predict drought-induced tree mortality in tropical forest. Here we are certainly not advocating for the use of TLP instead of HSM to predict drought-induced tree mortality in tropical forests, but simply for predicting drought-induced tree mortality in tropical forests in supplementary of HSM in the future.
The hydraulic vulnerability segmentation (HVS) hypothesis implies the existence of differences in embolism resistance between plant organs along the xylem pathway and has been suggested as an adaptation allowing the differential preservation of more resource-rich tissues during drought stress. Compound leaves in trees are considered a low-cost means of increasing leaf area and may thus be expected to show evidence of strong HVS, given the tendency of compound-leaved tree species to shed their leaf units during drought. However, the existence and role of HVS in compound-leaved tree species during drought remain uncertain. We used an optical visualization technique to estimate embolism occurrence in stems, petioles, and leaflets of shoots in two compound-leaved tree species, Manchurian ash (Fraxinus mandshurica) and Manchurian walnut (Juglans mandshurica). We found higher (less negative) water potentials corresponding to 50% loss of conductivity (P50) in leaflets and petioles than in stems in both species. Overall, we observed a consistent pattern of stem > petiole > leaflet in terms of xylem resistance to embolism and hydraulic safety margins (i.e., the difference between mid-day water potential and P50). The coordinated variation in embolism vulnerability between organs suggests that during drought conditions, trees benefit from early embolism and subsequent shedding of more expendable organs such as leaflets and petioles, as this provides a degree of protection to the integrity of the hydraulic system of the more carbon costly stems. Our results highlight the importance of HVS as an adaptive mechanism of compound-leaved trees to withstand drought stress.
The plant hydraulic network faces several challenges under drought stress. Hydraulic conductivity is one of the major indicators of the hydraulic network's response to drought stress. Here, we review our current understanding of the factors directly affecting hydraulic conductivity and the methods used to measure it.
Plants are always suffering periods of soil water deficit and sustained soil salinity during their life cycle. Unraveling the mechanisms underpinning the responses of plants, especially the photosynthesis, to drought, salinity, and co-occurring stresses is critical for both the protection of natural vegetation and the stabilization of crop production. To better understand the downregulation of photosynthetic capability induced by soil salinity and drought, gas exchange parameters, leaf pigment contents, and chlorophyll (Chl) a fluorescence transients were analyzed in leaves of Hybrid Pennisetum. Our results showed that long-term moderate salinity, short-term drought, and the combination of these stressors decreased leaf pigment content by 11.4–31.5% and net photosynthetic rate (Pn) by 14.6–67.6% compared to those in untreated plants. The reduction of Pn in Hybrid Pennisetum under long-term salinity stress mainly occurred by stomatal limitation, whereas non-stomatal limitation played a dominant role under short-term drought stress. The changes in Chl a fluorescence kinetics (especially the appearance of the L-band and K-band) in both stress treatments showed that salinity and drought stress damaged the structural stability of photosystem II (PSII) and disturbed the equilibrium between the electrons at the acceptor and donor sides of PSII. Furthermore, although the negative effect of drought stress on leaf photosynthesis was much greater than that of salinity stress, moderate salt stress alleviated the negative effect of drought stress on the photosynthetic performance of Hybrid Pennisetum after long acclimation times.
The ability to resist hydraulic dysfunction in leaves, stems and roots strongly influences whether plants survive and recover from drought. However, the coordination of hydraulic function among different organs within species and their links to gas exchange during drought and recovery remains understudied. Here we examine the interaction between gas exchange and hydraulic function in the leaves, stems and roots of three semi‐arid evergreen species exposed to a cycle of severe water stress (associated with substantial cavitation) and recovery. In all species, stomatal closure occurred at water potentials well before 50% loss of stem hydraulic conductance, while in two species leaves and/or roots were more vulnerable than stems. Following soil rewetting, leaf‐level photosynthesis (Anet) returned to pre‐stress levels within 2‐4 weeks, whereas stomatal conductance and canopy transpiration were slower to recover. The recovery of Anet was decoupled from the recovery of leaf, stem and root hydraulics, which remained impaired throughout the recovery period. Our results suggest that in addition to high embolism resistance, early stomatal closure and hydraulic vulnerability segmentation confers drought tolerance in these arid zone species. The lack of substantial embolism refilling within all major organs suggests that vulnerability of the vascular system to drought‐induced dysfunction is a defining trait for predicting post‐drought recovery. Early stomatal closure and hydraulic vulnerability segmentation rather than embolism refilling confers drought tolerance and enables recovery in three arid zone Australian species after drought.
Significance
A major determinant of plant species distribution on Earth is a specific tolerance to soil drying, yet there are currently no functional or anatomical characteristics that can predict species’ requirement for rainfall. This study examines the systems responsible for controlling water delivery and water loss in the leaves of conifers and finds functional evidence of how conifers have evolved in drying climates over the course of the last 150 million years. Two “strategies” for conserving water during water stress emerged. One group relied on the plant hormone abscisic acid to maintain stomata closed during sustained drought, and another, more derived group allowed leaves to dehydrate and resisted damage by producing a water transport system capable of functioning under the extreme tension that develops in water-stressed plants.
Under drought conditions, the xylem of trees that conducts ascending sap produces ultrasonic emissions whose exact origin is not clear. We introduce a new method to record simultaneously both acoustic events and optical observation of the xylem conduits within slices of wood that were embedded in a transparent material setting a hydric stress. In this article, we resolved the rapid development of all cavitation bubbles and demonstrated that each ultrasound emission was linked to the nucleation of one single bubble, whose acoustic energy is an increasing function of the size of the conduit where nucleation occurred and also of the hydric stress. We modelled these observations by the fact that water columns in conduits store elastic energy and release it into acoustic waves when they are broken by cavitation bubbles. Water columns are thus elastic, and not rigid, 'wires of water' set under tension by hydric stresses. Cavitation bubbles are at the origin of an embolism, whose development was followed in our experiments. Such an embolism of sap circulation can result in a fatal condition for living trees. These findings provide new insights for the non-destructive monitoring of embolisms within trees, and suggest a new approach to study porous media under hydric stress.
Leaf shrinkage with dehydration has attracted attention for over 100 years, especially as it becomes visibly extreme during drought. However, little has been known of its correlation with physiology. Computer simulations of the leaf hydraulic system showed that a reduction of hydraulic conductance of the mesophyll pathways outside the xylem would cause a strong decline of leaf hydraulic conductance (Kleaf). For 14 diverse species, we tested the hypothesis that shrinkage during dehydration (i.e., in whole leaf, cell and airspace thickness, and in leaf area) is associated with reduction in Kleaf at declining leaf water potentials (Ψleaf). We tested hypotheses for the linkage of leaf shrinkage with structural and physiological water relations parameters including modulus of elasticity (ε) and osmotic pressures at full turgor (πo) and turgor loss point (TLP) and cuticular conductance. Species originating from moist habitats showed substantial shrinkage during dehydration before reaching TLP in contrast with species originating from dry habitats. Across species, the decline of Kleaf with mild dehydration (i.e., the initial slope of the Kleaf versus Ψleaf curve) correlated with the decline of leaf thickness (the slope of the leaf thickness versus Ψleaf curve), as expected based on predictions from computer simulations. Leaf thickness shrinkage before TLP correlated negatively with ε and positively with πo, as did leaf area shrinkage between full turgor and oven-desiccation. These findings point to a role for leaf shrinkage in hydraulic decline during mild dehydration, with potential impacts on drought adaptation for cells and leaves, influencing plant ecological distributions.
A regional atmospheric model with 60-km resolution is asynchronously coupled with a potential vegetation model to study the implications of twenty-first-century climate change for the tropical and subtropical climate and vegetation of South America. The coupled model produces an accurate simulation of the present day climate and vegetation. Future climate is simulated by increasing atmospheric CO2 levels to 757 ppmv and imposing lateral and surface boundary conditions derived from a GCM simulation for 2081–2100 from the Canadian Climate Center GCM.
The coupled regional model simulation projects a 70% reduction in the extent of the Amazon rain forest by the end of the twenty-first century and a large eastward expansion of the caatinga vegetation that is prominent in the Nordeste region of Brazil today. These changes in vegetation are related to reductions in annual mean rainfall and a modification of the seasonal cycle that are associated with a weakening of tropical circulation systems.
Xylem cavitation resistance has profound implications for plant physiology and ecology. This process is characterized by a 'vulnerability curve' (VC) showing the variation of the percentage of cavitation as a function of xylem pressure potential. The shape of this VC varies from 'sigmoidal' to 'exponential'. This review provides a panorama of the techniques that have been used to generate such a curve. The techniques differ by (i) the way cavitation is induced (e.g. bench dehydration, centrifugation, or air injection), and (ii) the way cavitation is measured (e.g. percentage loss of conductivity (PLC) or acoustic emission), and a nomenclature is proposed based on these two methods. A survey of the literature of more than 1200 VCs was used to draw statistics on the usage of these methods and on their reliability and validity. Four methods accounted for more than 96% of all curves produced so far: bench dehydration-PLC, centrifugation-PLC, pressure sleeve-PLC, and Cavitron. How the shape of VCs varies across techniques and species xylem anatomy was also analysed. Strikingly, it was found that the vast majority of curves obtained with the reference bench dehydration-PLC method are 'sigmoidal'. 'Exponential' curves were more typical of the three other methods and were remarkably frequent for species having large xylem conduits (ring-porous), leading to a substantial overestimation of the vulnerability of cavitation for this functional group. We suspect that 'exponential' curves may reflect an open-vessel artefact and call for more precautions with the usage of the pressure sleeve and centrifugation techniques.
The pressure-bomb technique as developed by Scholander and colleagues is reviewed. A theoretical analysis of the equilibrium
water-relations of individual cells of a twig is derived taking due account of the fact that each cell has a unique solute
concentration, fluid volume, shape, and unique mechanical constraint by virtue of its cell-wall structure and attachment to
nearest neighbours. These equations combine to give a complete description of the whole twig in response to mechanical (air
pressure) stress. Our theoretical analysis suggests that the ‘pressure-volume curve’ can be related quantitatively to meaningful
bulk parameters of water relations: viz. the total osmolar content of the symplast Ns, the original volume of the symplast Vo, the volume expressed from the symplast Ve, the gas-pressure of the bomb P, and the volume-averaged turgor pressure (the sum of the products of the relative volume and turgor pressure of each cell).
An empirical relation for the volume-averaged turgor pressure of twigs is found which fits all species examined; it also fits
the turgor pressure relation for single (Nitella) cells.
We determined adjustments in physiology and morphology that allow Neotropical savanna trees from central Brazil (Cerrado) to avoid water deficits and to maintain a nearly constant internal water balance despite seasonal changes in precipitation and air saturation deficit (D). Precipitation in the study area is highly seasonal with about five nearly rainless months during which D is two fold higher compared to wet season values. As a consequence of the seasonal fluctuations in rainfall and D, soil water potential changes substantially in the upper 100 cm of soil, but remains nearly constant below 2 m depth. Hydraulic architecture and water relations traits of Cerrado trees adjusted during the dry season to prevent increasing water deficits and insure homeostasis in minimum leaf water potential ψL and in total daily water loss per plant (isohydry). The isohydric behavior of Cerrado trees was the result of a decrease in total leaf surface area per tree, a strong stomatal control of evaporative losses, an increase in leaf-specific hydraulic conductivity and leaf hydraulic conductance and an increase in the amount of water withdrawn from internal stem storage, during the dry season. Water transport efficiency increased in the same proportion in leaves and terminal stems during the dry season. All of these seasonal adjustments were important for maintaining ψL above critical thresholds, which reduces the rate of embolism formation in stems and help to avoid turgor loss in leaf tissues still during the dry season. These adjustments allow the stems of most Cerrado woody species to operate far from the point of catastrophic dysfunction for cavitation, while leaves operate close to it and experience embolism on a daily basis, especially during the dry season.
Hydraulic architecture was studied in shrub species differing in rooting depth in a cold desert in Southern Argentina. All species exhibited strong hydraulic segmentation between leaves, stems and roots with leaves being the most vulnerable part of the hydraulic pathway. Two types of safety margins describing the degree of conservation of the hydraulic integrity were used: the difference between minimum stem or leaf water potential (Ψ) and the Ψ at which stem or leaf hydraulic function was reduced by 50% (Ψ - Ψ50 ), and the difference between leaf and stem Ψ50 . Leaf Ψ50 - stem Ψ50 increased with decreasing rooting depth. Large diurnal decreases in root specific hydraulic conductivity suggested high root vulnerability to embolism across all species. Although stem Ψ50 became more negative with decreasing species-specific Ψsoil and minimum stem Ψ, leaf Ψ50 was independent of Ψ and minimum leaf Ψ. Species with embolism-resistant stems also had higher maximum stem hydraulic conductivity. Safety margins for stems were > 2.1 MPa, whereas those for leaves were negative or only slightly positive. Leaves acted as safety valves to protect the integrity of the upstream hydraulic pathway, whereas embolism in lateral roots may help to decouple portions of the plant from the impact of drier soil layers.
Long distance water transport through plant xylem is vulnerable to hydraulic dysfunction during periods of increased tension on the xylem sap, often coinciding with drought. While the effects of local and systemic embolism on plant water transport and physiology are well documented, the spatial patterns of embolism formation and spread are not well understood. Using a recently developed non-destructive diagnostic imaging tool, high resolution X-ray computed tomography (HRCT), we documented the dynamics of drought-induced embolism in grapevine (Vitis vinifera) plants in vivo, producing the first three dimensional, high resolution, time-lapse observations of embolism spread. Embolisms formed first in the vessels surrounding the pith at stem water potentials of approximately -1.2 MPa in drought experiments. As stem water potential decreased, embolisms spread radially toward the epidermis within sectored vessel groupings via intervessel connections and conductive xylem relays, and infrequently (16 of 629 total connections) through lateral connections into adjacent vessel sectors. Theoretical loss of conductivity calculated from the HRCT images showed good agreement with previously published nuclear magnetic resonance imaging and hydraulic conductivity experiments also using V. vinifera. Overall, these data support a growing body of evidence that xylem organization is critically important to the isolation of drought-induced embolism spread, and confirm that air seeding through the pit membranes is the principle mechanism of embolism spread.
Shifts in rainfall patterns and increasing temperatures associated with climate change are likely to cause widespread forest decline in regions where droughts are predicted to increase in duration and severity. One primary cause of productivity loss and plant mortality during drought is hydraulic failure. Drought stress creates trapped gas emboli in the water transport system, which reduces the ability of plants to supply water to leaves for photosynthetic gas exchange and can ultimately result in desiccation and mortality. At present we lack a clear picture of how thresholds to hydraulic failure vary across a broad range of species and environments, despite many individual experiments. Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely consequences of climate change for forest biomes. We show that 70% of 226 forest species from 81 sites worldwide operate with narrow (<1 megapascal) hydraulic safety margins against injurious levels of drought stress and therefore potentially face long-term reductions in productivity and survival if temperature and aridity increase as predicted for many regions across the globe. Safety margins are largely independent of mean annual precipitation, showing that there is global convergence in the vulnerability of forests to drought, with all forest biomes equally vulnerable to hydraulic failure regardless of their current rainfall environment. These findings provide insight into why drought-induced forest decline is occurring not only in arid regions but also in wet forests not normally considered at drought risk.
For the past 25 years NIH Image and ImageJ software have been pioneers as open tools for the
analysis of scientific images. We discuss the origins, challenges and solutions of these two programs,
and how their history can serve to advise and inform other software projects.
Abstract Hydraulic conductivity of the xylem is computed as the quotient of mass flow rate and pressure gradient. Measurements on excised plant stems can be difficult to interpret because of time-dependent reductions in flow rate, and because of variable degrees of embolism. Using Acer saccharum Marsh. stems, we found that certain perfusing solutions including dilute fixatives (e.g. 0.05% formaldehyde) and acids with pH below 3 (e.g. 10 mol m−3 oxalic) prevent long-term decline in conductivity. Xylem embolism can be quantified by expressing the initial conductivity as a percentage of the maximum obtained after flow-impeding air emboli have been removed by repeated high-pressure (175 kPa) flushes. Correlation between microbial contamination and declining conductivity suggests that long-term (> 4h) declines are caused by microbial growth within the vessels. Unpredictable trends in short-term (< 4h) measurements may be caused by movements of air emboli in vessels and/or participate matter.
Hydraulic traits were studied for six Nothofagus species from South America (Argentina and Chile), and for three of these species two populations were studied. The main goal was to determine if properties of the water conductive pathway in stems and leaves are functionally coordinated and to assess if leaves are more vulnerable to cavitation than stems, consistent with the theory of hydraulic segmentation along the vascular system of trees in ecosystems subject to seasonal drought. Vulnerability to cavitation, hydraulic conductivity of stems and leaves, leaf water potential, wood density and leaf water relations were examined. Large variations in vulnerability to cavitation of stems and leaves were observed across populations and species, but leaves were consistently more vulnerable than stems. Water potential at 50% loss of maximum hydraulic efficiency (P(50)) ranged from -0.94 to -2.44 MPa in leaves and from -2.6 to -5.3 MPa in stems across species and populations. Populations in the driest sites had sapwood and leaves more vulnerable to cavitation than those grown in the wettest sites. Stronger diurnal down-regulation in leaf hydraulic conductance compared with stem hydraulic conductivity apparently has the function to slow down potential water loss in stems and protect stem hydraulics from cavitation. Species-specific differences in wood density and leaf hydraulic conductance (K(Leaf)) were observed. Both traits were functionally related: species with higher wood density had lower K(Leaf). Other stem and leaf hydraulic traits were functionally coordinated, resulting in Nothofagus species with an efficient delivery of water to the leaves. The integrity of the more expensive woody portion of the water transport pathway can thus be maintained at the expense of the replaceable portion (leaves) of the stem-leaf continuum under prolonged drought. Compensatory adjustments between hydraulic traits may help to decrease the rate of embolism formation in the trees more vulnerable to cavitation.
Species distribution models predict a wholesale redistribution of trees in the next century, yet migratory responses necessary to spatially track climates far exceed maximum post-glacial rates. The extent to which populations will adapt will depend upon phenotypic variation, strength of selection, fecundity, interspecific competition, and biotic interactions. Populations of temperate and boreal trees show moderate to strong clines in phenology and growth along temperature gradients, indicating substantial local adaptation. Traits involved in local adaptation appear to be the product of small effects of many genes, and the resulting genotypic redundancy combined with high fecundity may facilitate rapid local adaptation despite high gene flow. Gene flow with preadapted alleles from warmer climates may promote adaptation and migration at the leading edge, while populations at the rear will likely face extirpation. Widespread species with large populations and high fecundity are likely to persist and adapt, but will likely suffer adaptational lag for a few generations. As all tree species will be suffering lags, interspecific competition may weaken, facilitating persistence under suboptimal conditions. Species with small populations, fragmented ranges, low fecundity, or suffering declines due to introduced insects or diseases should be candidates for facilitated migration.
Vegetation structure, floristics and distance from a seed source influence dispersal of seeds to revegetated sites. This study investigates the effects of distance from a seed source on dispersal of seeds to three restored rainforest sites (all approximately 10 years old) on the Atherton Tablelands, North Queensland. The three sites were located at varying distances from the nearest seed source, one being adjacent to a rainforest reserve and two being surrounded by pasture and isolated from the nearest rainforest by distances of 600 m and 2 km. Floristics and vegetation structure (LAI, lateral cover at ground level, stem density and groundcover) were similar between sites, suggesting that the three sites would be equally suitable for use by seed-dispersing fauna. Differences in propagule dispersal to the three sites were therefore likely attributable to distance from seed source rather than vegetation structure. Over the decade since establishment a far higher number of native species—dispersed by flying fauna, ground-dwelling mammals, wind and varied dispersal agents—had been recruited (in higher densities) to the adjacent site than to either of the isolated sites. The two isolated sites had far higher levels of exotic recruits (characteristic of early successional stages) than did the adjacent site, owing to the proximity of these sites to pasture containing exotic grasses and forbs. A very small number of recruited species were extremely abundant at each site, while the majority of new species were rare, this pattern being particularly pronounced at the distant sites. Owing to isolation from a seed source, recruitment of species typical of intermediate and late-successional stages is occurring far more slowly at both isolated sites compared with the adjacent site. Recovery of these distant sites to self-sustaining mature rainforest may not occur without human mediated seed dispersal. Mammal-dispersed species in particular are unlikely to reach these sites unless contributed by humans. Recovery of tropical rainforest systems is likely to occur more quickly and be more successful if restoration is concentrated around the perimeter of existing rainforest rather than in isolated patches.
Diel variation in specific hydraulic conductivity (ks) was recorded in petioles of two savanna tree species, Schefflera macrocarpa and Caryocar brasiliense, from central Brazil. These two species have compound leaves with long petioles (10–30 cm). In both species, petiole ks decreased sharply with increasing transpiration rates and declining leaf water potentials (YL) during the morning. Petiole ks increased during the afternoon while the plants were still transpiring and the water in the non-embolized vessels was still under tension. Dye experiments confirmed that in both species diel variation in ks was associated with embolism formation and repair. When transpiration was prevented in individual leaves, their petiole ks and water potential remained close to their maximum values during the day. When minimum daily YL on selected branches was experimentally lowered by 0.2–0.6 MPa, the rate of ks recovery during the afternoon was slower in comparison with control branches. Several field manipulations were performed to identify potential mechanisms involved in the refilling of embolized petiole vessels. Removal of the cortex or longitudinal incisions in the cortex prevented afternoon recovery of ks and refilling of embolized vessels. When distilled water was added to petiole surfaces that had been abraded to partially remove the cuticle, ks increased sharply during the morning and early afternoon. Evidence of starch to sugar conversion in the starch sheath cells surrounding the vascular bundles of the petioles was observed during periods of rapid transpiration when the abundance of starch granules in the starch sheath cells surrounding the vascular bundles decreased. Consistent with this, petiole sugar content was highest in the early afternoon. The most parsimonious explanation of the field observations and the experimental results was that an increase in osmotically active solutes in cells outside the vascular bundles at around midday leads to water uptake by these cells. However, the concurrent increase in tissue volume is partially constrained by the cortex, resulting in a transient pressure imbalance that may drive radial water movement in the direction of the embolized vessels, thereby refilling them and restoring water flow. This study thus presents evidence that embolism formation and repair are two distinct phenomena controlled by different variables. The degree of embolism is a function of tension, and the rate of refilling a function of internal pressure imbalances.
Forest Trees of Australia is the essential reference for observing, identifying and obtaining information on the native trees in this country. It describes and illustrates over 300 of our most important indigenous trees, which have been carefully selected for their environmental significance, their importance to the timber industry, or their prominence in our landscape. This new and thoroughly revised edition has been fully updated throughout and includes treatments of 72 additional species. New maps and photographs show us a wonderfully diverse range of forests, from mangrove swamps, tropical regions and deserts, to alpine areas and majestic stands of temperate forests. A colour section illustrates some of the major forest types of Australia and bark from a diverse range of species. Forest Trees of Australia is an unsurpassed guide to identification for horticulturists, botanists, foresters, students, farmers, environmentalists and all those who are interested in our native trees.