ABSTRACT
Leaf water potential is a good indicator of tree species responses to
rainfall seasonality, allowing to better understand water stress effects
on vegetation. We investigated daily and seasonal patterns on leaf water
potentials of 21 dominant species in three distinct vegetation types
from the Cerrado-Amazonia transition to assess how they respond to
seasonal changes in water availability. We found that the variation on
leaf water potential (Ψl) across species was higher in
the dry compared to the rainy season, for all vegetation types. Typical
cerrado and cerradão species showed similar patterns, with higher
Ψl regulation under higher VPD and lower variation in
predawn Ψl (ΔΨpd), indicating root
access to soil water even during intense drought. In contrast, seasonal
forest species showed lower regulation under lower VPD effects in both
seasons, and higher ΔΨpd, indicating lower access to
deep water in the soil. These differences revealed two main groups of
species: higher Ψl regulators with a strategy isohydric
occurring in both typical cerrado (savanna) and cerradão (woodland), and
lower Ψl regulators with anisohydric strategy, occurring
in seasonal forest. Our results suggest that seasonal tropical forest
species will become very vulnerable to predicted increases on drought
severity in the region.
Keywords: savanna, Neotropics, tropical forest, isohydric,
anisohydric, seasonality, plant hydraulics, vapour pressure deficit,
climate change, plant traits.
Introduction
In the tropics, species distribution occurs along gradients of water
availability, affected by their resistance to drought (Aguirre‐Gutiérrez
et al., 2019). Thus, a marked seasonality, with well-defined periods of
drought and rain, will favour plants with traits and ecological
strategies that enhance survival under such circumstances (Franco,
Rossatto, Silva, & Ferreira, 2014). Hence, plants occurring in highly
seasonal habitats will display specialized mechanisms for water
acquisition, maintenance and use, to guarantee a continuous flow, with
strategies that allow homeostasis in hydraulic functioning (Oliveira et
al., 2014).
The most common explanation of how hydraulic functioning occurs in
plants is the unidirectional movement (i.e., the continuous
soil-plant-atmosphere), where water flow occurs from less to more
negative water potentials, establishing a difference of potentials
through a pressure gradient (Oliveira et al., 2014). The leaf water
potential (Ψl) reflects the tension in which the xylem
transports water, and it is a crucial variable to check the water status
of the plant at a given time, being influenced by leaf transpiration
processes, which is determined by the atmospheric evaporative demand
(Oliveira, Dawson, Burgess, & Nepstad, 2005; Palhares, Franco, &
Zaidan, 2010) and by the water availability in the soil (Jones, 1998).
If there are severe changes in these mechanisms, such as limited water
availability and high evaporative demand, hydraulic failure (i.e.,
cavitation of the xylem vessels) can occur interrupting water transport,
and eventually could lead to the plant death (McDowell, 2011). Thus, a
higher vapour pressure deficit (VPD) during the dry season expose plants
to more stressful conditions (Prado, Wenhui, Cardoza Rojas, & Souza,
2004), which require effective mechanisms to avoid excessive water loss
and regulate plant water transport, which reflect mainly on stomatal
regulation process (Martínez‐Vilalta, Poyatos, Aguadé, Retana, &
Mencuccini, 2014). Water availability in the soil directly influences
this control; roots access water in the soil, and their hydraulic
conductivity will be a function of the daily transpiration of the plant
(Meinzer et al., 1999). Based on the mechanism of transpiration
regulation over time, there is a continuum of variation between two
extreme strategies: isohydric species that adjust their stomatal opening
to avoid significant drops on Ψl, and anisohydric
species with lower stomatal control and higher daily and annual
variation in the Ψl (Jones, 1998; Martínez‐Vilalta &
Garcia‐Forner, 2017; Tardieu & Simonneau, 1998).
Theory suggests that Ψl at predawn reflects the water
potential of the soil (Tardieu & Simonneau, 1998) and therefore, its
variation during different periods of the year can be used as an
estimate (proxy) of root depth, i.e., the range of water acquired by
roots (Brum, Teodoro, Abrahão, & Oliveira, 2017; Scholz, Bucci, Arias,
Meinzer, & Goldstein, 2012). Thus, plants with shallow roots may show
more negative values of Ψl in the dry season as the dry
season, while plants with deep roots would maintain less negative
Ψl values (Scholz et al., 2012).
The Cerrado-Amazonia transition, the world’s largest savanna-forest
transition, has a strongly seasonal climate, with a wide variety of
vegetation types, ranging from savannas (e.g., typical cerrado and rocky
cerrado), characterized by open environments with high temperature and
solar radiation, to closed-canopy environments (e.g., cerradão, gallery
forest and semi-deciduous seasonal forest), with higher moisture and the
presence of Amazonian species (Marimon, Lima, Duarte, Chieregatto, &
Ratter, 2006; Marimon et al., 2014). Some studies suggested that, in
Brazilian savannas (Cerrado), water availability in the soil is not a
limiting factor (Franco & Lüttge, 2002) but the higher VPD imposes a
strong limitation on transpiration (Franco & Lüttge, 2002; Meinzer et
al., 1999). Some authors suggest that, although several woody species
from Cerrado have deep roots and can access the water table throughout
the year (Bucci et al., 2008; Oliveira et al., 2005), the simple access
to underground water reserves does not ensure they extract enough water
to compensate for the high evaporative demand during prolonged droughts
(Franco, Matsubara, & Orthen, 2007). On the other hand, in forests
formations, stomata tend to show high sensitivity with the increase in
the atmospheric evaporative demand (Cunningham, 2004). However, forest
plants have other hydraulic mechanisms to deal with high VPD, through
continuous water absorption in the soil (Juárez, Hodnett, Fu, Goulden,
& Von Randow, 2007; Oliveira et al., 2005). Still, we do not have
enough information on how Ψl regulation occurs in trees
along the Cerrado-Amazonia transition.
Hence, savanna and forest formations of the Cerrado-Amazonia transition
provide a good opportunity to investigate how species from different
vegetation types respond to limiting access to water. These species are
under the influence of pronounced climate seasonality, high
temperatures, and marked variations in humidity, which can trigger a
water deficit gradient during the year (Marimon et al., 2020; Peixoto et
al., 2018). In this highly seasonal region, where the rainy and dry
seasons are well defined (INMET, 2018), Ψl regulation
may be a distinct trait reflecting ecological strategies from species in
different vegetation types. Based on the premise that physiological
activity of the root system and leaf stomatal control depend on the
balance between the atmospheric evaporative demand and the water
availability in the soil (Oliveira et al., 2014; Oliveira et al., 2005;
Palhares et al., 2010), we set out to test the following hypotheses: (i)
Different vegetation types will show distinct patterns of
Ψl regulation, which will depend on daily and seasonal
VPD. Thus, we expect savanna environments (typical cerrado), which occur
under higher variation in temperature, air humidity, and, consequently,
VPD (Prado et al., 2004), species will be more isohydric, as a strategy
to prevent water loss. In contrast, in forest environments, species will
be anisohydric with higher tolerance to environmental changes; (ii)
typical cerrado will show more and forest will show less interspecific
variation in Ψl regulation. In addition, we expect that,
in all vegetation types, Ψl variations will be
associated with the minimum Ψl and the variation of
predawn Ψl (root proxy; ΔΨpd).
Material and methods
Study area
The studied areas are located in southern Amazonia, in the transition
between Cerrado and Amazonia biomes, state of Mato Grosso, Nova
Xavantina municipality (Fig. 1). The climate is Aw, according to the
Köppen’s classification (Kottek, Grieser, Beck, Rudolf, & Rubel, 2006),
with well-defined wet (October to March) and dry seasons (April to
September), annual rainfall around 1500 mm, and average annual
temperature of 25 ºC (Marimon et al., 2020). Between 2000 and 2017,
according to data provided by the National Institute of Meteorology
(conventional station of Nova Xavantina), the average annual rainfall
was 1364 mm, with a minimum of 957.1 mm (2007) and the maximum of 1858
mm (2006). The average annual temperature recorded in this period was
26.3 ºC, with the lowest average annual temperature recorded in 2003 and
2007 (18 ºC) and the highest in 2007 (34.5 ºC). Between 1997 and 2019
this region also presented a general trend of markedly increasing
temperature and declining precipitation, with more negative maximum
cumulative water deficits (MCWD) values (Marimon et al., 2020).
Despite the relatively small spatial scale (25 km), there is a huge
difference in vegetation types in the study area, with distinct species
composition and vegetation structure comprising typical savanna and
forest formations (Marimon et al., 2014). We assessed three vegetation
types: savanna (typical cerrado - STC), transitional community (cerradão
- SCF) and forest (semi-deciduous seasonal forest - SSF). According to
Ribeiro and Walter (1998), the typical cerrado is a cerradostricto sensu subtype with predominantly arboreal-shrubby
vegetation, 20 to 50% of tree cover, and tree heights between 3 and 6
m. The cerradão is characterized by mostly continuous canopy with
xeromorphic aspects, being considered an ecotonal community (Ratter,
Richards, Argent, & Gifford, 1973), with species (e.g., Hirtella
glandulosa and Emmotum nitens ) that characterize the transition
between forests and savannas on the southern Amazonian border (Marimon
et al., 2006). At last, the semi-deciduous seasonal forest (hereafter
forest) is characterized by tall and closed canopy vegetation and
well-defined vertical strata (Askew, Moffatt, Montgomery, & Searl,
1970; Marimon et al., 2006). The typical cerrado and cerradão show
Red-Yellow Latosols, dystrophic, acidic, and alic soils (Marimon-Junior
& Haridasan, 2005), and the semi-deciduous seasonal forest shows
Plintosols (Marimon et al., 2014).
Typical cerrado and cerradão occur in the Bacaba Municipal Park (14°41’
S; 52°20’ W), and the forest is located at Vera Cruz Farm (14º49’27.1”
S; 52º10’2.9” W) 25 km away from the other two (Fig. 1). We carried out
the study in 1-ha permanent plots subdivided into 25 subplots (20 x 20 m
each), which comprise the PELD/CNPq project (Transição
Cerrado-Amazônia: bases ecológicas e socioambientais para a
conservação , Proc. # 403725/2012-7 and 441244/2016-5), which are also
part of the Amazon Network of Forest Inventories (RAINFOR; typical
cerrado: NXV-01; cerradão: NXV-02 and forest: VCR-02).
To assess the hydraulic traits we selected the seven most representative
species in each area, which showed the largest basal area contribution
in the community, comprising a total of 21 species. In the typical
cerrado, we choose adult trees with at least 5 cm in diameter at breast
height (DBH), and in cerradão and forest, we selected trees with ≥10 cm
of DBH.
Measurements of leaf water potential
(Ψl)
In August 2016 (peak of the dry season) and January, February and March
2017 (rainy season), we measured the Ψl in two leaves of
five individuals from each species, using a pressure chamber (PMS
Instruments Co., Albany, USA; model: 1505D- EXP; Scholander, Bradstreet,
Hemmingsen, and Hammel (1965)). Measurements were taken at four
different times during the day: predawn (0400-0600), early-morning
(0700-0900), late-morning (1000-1130), and at midday (1200-1400 hours)
in all vegetation types. We selected healthy and mature leaves, exposed
to the sun. We also measured the temperature and relative humidity with
a portable weather station (Kestrel 3500) in the vicinity of trees and
where the leaves were collected. With these data, we calculated the
Vapour Pressure Deficit (VPD) in each vegetation type (Abtew & Melesse,
2013).
We determined the relationship between predawn (Ψpd),
and midday (Ψmd) leaf water potential, for all species
and vegetation types, to access Ψl regulation. We used
the linear model proposed by (Martínez‐Vilalta et al., 2014),
Ψmd = Δ + * Ψs, where
Ψs is the soil water potential, which we considered to
be similar to Ψpd (Tardieu & Simonneau, 1998);
represents the slope angle and is a measure of the transpiration
sensitivity to changes in water availability. For each species, we
analysed this relationship using the model Ψmd~ Ψpd + (Ψpd |
individuals).
Individuals of each species were included as random and fixed effects in
the model to estimate the values of slopes () and intercepts (Λ) of the
specific relationships between Ψmd and
Ψpd for each species. We measured each set of
individuals of a given species under the same environmental conditions.
Next, we classified species as strict isohydric if the value and its
confidence interval (CI; defined as ± 1) included zero ( = 0), strict
anisohydric if the CI of included 1 ( = 1), partially isohydric if CI
did not include 0 and 1 (0 < <1), and extreme
anisohydric if CI did not include 1 ( > 1)
(Martínez‐Vilalta et al., 2014). For each species and communities, we
also inferred the control of water potential through
ΔΨmd, which is the difference between the minimum
Ψl at midday in the rainy season and the minimum
Ψl in the dry season (Martínez‐Vilalta & Garcia‐Forner,
2017). We also used the variation in Ψpd (root proxy;
ΔΨpd), calculated by the difference between
Ψpd in the rainy season and dry season, to estimate the
root depth of species in relation to the water availability in the soil
(Scholz et al., 2012). For this latter step, we used the modular values
of the deltas.
Data analysis
We analysed leaf water potential regulation at two levels: species and
vegetation types. We adopted the terminology of maximum water potential
value (Ψmax) for the least negative potentials and the
minimum water potential value (Ψmin) for the most
negative potentials of the day. We performed all analyses in the R 4.0.1
environment (R Core Team 2020) and considered p-value<0.05.
We tested whether the dependent variable Ψl varied
between species and among the four different periods of the day assessed
in each season (dry and rainy). We also investigated whether
Ψl and other hydraulic traits (Ψmin,
ΔΨpd, and ΔΨmd) varied among the
vegetation types (typical cerrado, cerradão, and semi-deciduous seasonal
forest) in different seasons (dry and rainy). For the analyses, we used
Kruskal-Wallis non-parametric test, followed by the Dunn test as apost-hoc analysis, since data did not follow normality
assumptions for parametric tests. We used plyr , dunn.test ,
and FSA packages (Dunn, 1964; Wickham, 2011). The weighted
average for each attribute (Ψmin, ΔΨpd,
ΔΨmd and ) in the vegetation types was calculated
through weight the relative dominance in the basal area of the species,
i.e., we used the relative dominance - proportion basal area specific of
the species by the sum of the basal areas of all species in the
community (Shepherd, 2010). We used the weights , quantreg ,
and Hmisc packages (R Core Team 2020).
We calculated and compared the coefficient of variance of the
Ψl and other traits (, Ψmin,
ΔΨpd, and ΔΨmd) between vegetation types
in the dry and rainy seasons. We applied the Mood test (non-parametric
data) to compare the Ψl variance between vegetation
types and used F-test, from the stats package (R Core Team 2020),
for other attributes. We applied a linear regression analysis to relate
the Ψl values of species to the vapour pressure deficit
(VPD) in each vegetation type in both seasons. We also compared linear
regression curves for the bi-variate relationship of Ψland VPD between different vegetation types (Standardised Major
Axis - SMA), using the smatr package (Warton, Duursma, Falster,
& Taskinen, 2012), for log10 transformed variables.
Results
Effect of seasonality on
Ψl
We found a broad variation in Ψl among species and
vegetation types (Table 1). The Ψmin varied from -2.8
MPa (Qualea parvilfora ) to -0.9 MPa (Eriotheca gracilipes )
in the dry season. In contrast, Ψmax varied from -0.24
MPa (Guapira graciliflora ) to -0.1 MPa (Eriotheca
gracilipes ), in the rainy season. Regarding communities, on average,
forest vegetation showed the lowest values, both for
Ψmax (-0.3 MPa, rainy season) and Ψmin(-2.8 MPa, dry season).
The Ψl of the 21 species varied according to the dry
(Q2 = 179.1, df = 19, p <0.001) and
rainy seasons (Q2 = 39.2, df = 19, p<0.001) and also among the different times of the day (dry
season: Q2 = 82.3, df = 3, p <0.001;
rainy season: Q2 = 250.7, df = 3, p<0.001). In the dry season, we recorded a significant
interspecific difference in Ψl values for all vegetation
types (typical cerrado: Q2 = 51.7, df = 6, p<0.001; cerradão: Q2 = 56.4, df = 6,p <0.001; and forest: Q2 = 3.5, df =
6, p <0.001). On the other hand, in the rainy season,
only cerradão species differed from each other in relation to
Ψl (Q2 = 14.15, df: 6; p =
0.02).
In both dry and rainy seasons, Ψl values of the typical
cerrado and cerradão species were similar and differed from the forest
(p <0.05 for all tests, Fig. 2). In the dry season, the
forest species showed the lowest mean values of Ψl at
all times of the day, with a continuous decrease from predawn to midday
(Figs. 2, 3). In contrast, in the rainy season, Ψlvalues in the forest species remained higher compared to those of other
vegetation types (Fig. 2; forest and typical cerrado - dry season: Z =
4.48; p = 0.00 and rainy season: Z = -3.94; p = 0.00; and
forest and cerradão - dry season: Z = 1.97; p = 0.00 and rainy
season: Z = 3.89; p = 0.00). Regarding the Ψlvariability, we noticed that vegetation types were more similar in the
dry season, whereas, in the rainy season, we recorded a higher
variability for the typical cerrado and cerradão (Table 2).
We observed a distinct regulation of Ψl in the forest
species compared to other vegetation types, and species from cerradão
and typical cerrado had relatively similar hydraulic strategies (Table 2
and Figs. 2, 3). The Ψmin also differed among vegetation
types (Q2 = 11.42; df: 2, p = 0.003) and the
lowest values were recorded for the forest species. A similar pattern
was recorded for the ΔΨpd, which also differed among
vegetation types (Q2 = 16.92, df = 2, p<0.001). Considering ΔΨpd as an estimate of
root depth (proxy), we found that forest species showed higher
ΔΨpd than those in the typical cerrado
(Q2 = 3.35; p = 0.00) and cerradão
(Q2 = 3.72; p = 0.00) according to the Dunn
test (Fig. 3).
Regulation of
Ψl
We observed that 47% of the species are partially isohydric, and 43%
are extreme anisohydric (Fig. 4). Eriotheca gracilipes was the
only strict isohydric species (10%), which showed the same pattern in
both typical cerrado and cerradão. When we separated by vegetation
types, we observed that 57% of typical cerrado and cerradão species are
partially isohydric, whereas most forest species are extreme anisohydric
(71%). We also found that all deciduous species are partially
isohydric, while evergreen and brevideciduous species vary among
vegetation types (Table 1). The forest species, Cheiloclinium
cognatum , and the cerrado and cerradão species, Eriotheca
gracilipes , represent the extremes in Ψl regulation
(Fig. 4).
The ΔΨmd differed in all vegetation types
(Q2 = 26.26; p <0.001), being the
forest with less regulation (Table 3). Therefore, almost all species in
the forest showed the same pattern of Ψl regulation for
and ΔΨmd, as well as the highest variation values,
indicating a lower control of water use and lower variability in the
ΔΨmd.
The cerradão species showed higher coefficients of variance in all
traits (, Ψmin, and ΔΨmd), except for
ΔΨpd, that was higher in the typical cerrado. However,
there were no statistical differences in the coefficients of variation
between all vegetation types (Tables 3 and S1).
Effect of the vapor pressure deficit (VPD)
on the leaf water potential
(Ψl)
The VPD differed among vegetation types but was higher in the dry season
in all areas (Tables 4 and S2), with a significant negative correlation
between VPD and Ψl (Fig. 5). The forest showed the
lowest Ψl values and the lowest VPD amplitude in both
seasons (Fig. 5 and Table 6).
In the dry season, typical cerrado VPD was 20% higher than that
recorded in the cerradão, and approximately 30% higher than that of the
forest (VPDtypical cerrado >
VPDcerradão > VPDforest),
which confirms that species are subject to a higher atmospheric water
demand during this season in the savanna vegetation (Table 4). We also
observed a direct relationship between the decrease in
Ψl and the increase in VPD; the cerradão showed
environmental variations more similar to typical cerrado than to forest,
which showed the lowest Ψl in the dry season (Fig. 5 and
S2).
Discussion
Our results showed different strategies for water use and access among
species and vegetation types in the Brazilian Cerrado-Amazonia
transition. We observed differences between the hydraulic functioning of
forest species in relation to typical cerrado and cerradão species,
which tended to show stronger leaf water potential regulation (isohydric
strategy) than forest species (anisohydric strategy). We also found that
cerradão, the transitional community, which is considered to be
floristically closer to forests than savannas (Morandi et al., 2016),
showed hydraulic traits and environmental conditions more similar to the
savanna (typical cerrado) than forest.
Hydraulic functioning
We found that different intensities in water deficit across vegetation
types determines different community-level patterns in the strategies of
water use and access. We expected that main difference in hydraulic
traits would occur between species from more contrasting vegetation
types, typical cerrado and semi-deciduous seasonal forest, and that
species from cerradão, which in our study area represents transitional
vegetation between cerrado and forest, since ther are no marked
differences in soil fertility (Marimon-Junior & Haridasan, 2005),would
show intermediate strategies of water use. However, contrary to our
expectations, we found that hydraulic traits of the cerradão species
were generally more similar to typical cerrado than to semi-deciduous
seasonal forest. We also observed that cerradão species showed a higher
amplitude of variation for all hydraulic traits assessed, which reflects
a great diversity of strategies within the species that comprise this
transitional vegetation (Marimon et al., 2006; Marimon et al., 2014;
Ratter, Ribeiro, & Bridgewater, 1997; Ratter et al., 1973).
Regarding community-level hydraulic traits, we suggest that typical
cerrado in our study area is already in successional stage of
thickening, turning to a dense cerrado (Morandi et al., 2016; Ribeiro &
Walter, 1998). Both typical cerrado and cerradão are geographically
close (900 m), showing similar soil parameters, topography
(Marimon-Junior & Haridasan, 2005) and VPD, which reinforces the
similar hydraulic functioning we reported here. Topography and soil
physical characteristics are key factors in the plants hydraulic
patterns as they are related to the level of groundwater and humidity
regime that can affect plant water relations water absorption from the
soil (Villalobos‐Vega et al., 2014).
We could separate species into two very distinct groups: the first,
composed of species from the typical cerrado and cerradão, with
strategies of higher water potential regulation, and the second,
composed of species from the forest, with lower water potential
regulation. The typical cerrado and cerradão species, most of which
characterized as partially isohydric, are exposed to higher VPD and also
better regulate and have higher Ψl values. Besides, the
lower variation in the Ψpd (values did not decrease much
in the dry season) suggests that typical cerrado and cerradão species
are growing with access to water in the soil (Palhares et al., 2010).
In addition, the stronger regulation of Ψl recorded for
typical cerrado and cerradão species, which are subject to high
atmospheric evaporative demand (VPD), may be related to more efficient
regulation of stomatal opening, especially in response to changes in
VPD, resulting in higher water use efficiency (Franco & Lüttge, 2002).
In such conditions, deeper roots are critical to maintain water balance
of Cerrado ecosystems (Oliveira et al., 2005), despite involving higher
maintenance costs or strict control of plant water balance (Franco et
al., 2005). For example, species such as Eriotheca gracilipesshowed little seasonal variation in leaf water potential, suggesting
access to deep water sources through root investment. Indeed, (Durigan,
Melo, & Brewer, 2012) showed that this particular species invests in a
main root, with approximately 2.5 m in length, without many fine roots.
Forest species showed a lower regulation of Ψl, with
higher drop in Ψl and higher ΔΨpd, which
might indicate shallower roots and less access to the water in the soil.
Thus, these species might have higher transpiration rates, probably due
to low stomatal control, both in dry and rainy seasons, which might help
explaining the observed steep decrease in Ψl in this
study, thus having a more acquisitive strategy in terms of carbon gain
and less conservativism on safety strategies. These strategies might
also indicate a mechanism for maintaining leaf temperature and reducing
the negative effect of VPD (Tardieu & Simonneau, 1998). Regarding water
availability in the soil, even though root depth estimates were
considered shallow and with limited access to deep soil layers, they
might compensate it through a more efficient water absorption capacity
(Butler et al., 2013). According to these authors, the water absorption
by surface root area increases with tree diameter in species that
occurred in our study areas. They showed that typical cerrado species
showed lower values of the root area absorption index (0.03
m2 m-2) than cerradão (0.07
m2 m-2) and forest (0.11
m2 m-2), which showed higher
efficiency in the absorption capacity by surface root area.
Thus, forest species showed a less conservative stomatal regulation
behaviour (anisohydric), characterized by open stomata and higher
photosynthetic rates for long periods, even with a decrease in
Ψl (Sade, Gebremedhin, & Moshelion, 2012). Therefore,
we believe that the lowest VPD values recorded in the forest provide a
mild to moderate environment under abiotic stress that directly
influences plants and their capacity in the face of climate seasonality
(Sade et al., 2012).
Interspecific variability in hydraulic
functioning
The differences in Ψl among species suggest a
substantial interspecific variation in hydraulic functioning regulation
of the different vegetation types. Species-level variations in hydraulic
traits depend on the access to water in the soil and atmospheric
evaporative demand, which are the main environmental drivers that
influence plant hydraulic functioning, regulating gas exchange (Buckley
& Mott, 2013). Thus, within the same vegetation type, we found species
displaying different strategies; cerradão species with higher
(Eriotheca gracilipes ) or lower (Tapirira guianensis )
regulation of leaf water potential; typical cerrado species with an
estimate of high (Euplassa inaequalis ) or limited (Guapira
graciliflora ) access to deeper layers of the soil; and forest species
with support of higher (Chaetocarpus echinocarpus ,Ephedranthus parviflorus ) or lower (Brosimum pubescens )
tension in which the xylem transports water.
These different hydraulic strategies also seem to involve other
structural characteristics (e.g., anatomical and morphological; Sperry,
Meinzer, and McCulloh (2008)). In this case, the variability of
morpho-functional traits in plant communities, at a local and global
scale, provides evidence that species efficiently share resources (Brum
et al., 2017; Meinzer et al., 1999). Thus, the variation in water
availability is a dimension of the species niche, which represents a
complex resource condition intrinsically connected to the availability
of other resources (Araya et al., 2011). Our results also indicated that
the differences in hydraulic functioning among species characterize
responses that depend on climate seasonality, since all evaluated
vegetation types are subject to similar seasonality effects, especially
in the dry season, when the greatest VPD amplitude occurs. In this case,
plant and environment water availability and the dynamics of
soil-plant-atmosphere interaction affect the species responses to biotic
and abiotic stress (Sade et al., 2012).
Although we have recorded different water use and acquisition
strategies, forest species displayed a similar pattern for most
hydraulic traits, showing lower Ψl values in both dry
and rainy seasons. This strategy allows plants to function in a more
negative Ψl range and regulate it according to the VPD,
that is, a typically anisohydric strategy (McDowell et al., 2008). On
the other hand, typical cerrado and cerradão species showed more
variability in hydraulic traits, which are in agreement with theoretical
models that predict that a limitation of water resources in arid or
savanna environments would select different strategies for water use and
conservation (Meinzer et al., 1999). Hence, these different hydraulic
strategies may favor a higher species and functional diversity,
especially where strong environmental filters are more evident, such is
the case in the typical cerrado and cerradão (Neyret et al., 2016).
Hydraulic traits among vegetation types in the face of
climate
change
Hydraulic characteristics may reflect the evolutionary history of
species that shape their performance over the years under the influence
of environmental conditions (Reich & Cornelissen, 2014), which was
evidenced in the present study through different responses given by
savanna and forest species. Hence, in case extreme drought events become
more intense and frequent in this zone of ecological tension/stress on
the southern Amazonia, as predicted (Marimon et al., 2014; Rifai et al.,
2018), with deregulation in the mechanism of water demand and supply in
the environment (increase in VPD and decrease in soil moisture), more
resistant species and vegetation types, as well as species more
vulnerable to drought events, can emerge (McDowell, 2011). In any case,
we know that savanna vegetation is mainly composed by species with
higher Ψl regulation that preserve water transport and
help preventing hydraulic failures (e.g., Guapira graciliflora ),
even at the expense of reduction in the carbon balance and a possible
overheating caused by photosynthetic damage (McDowell et al., 2008). On
the other hand, forest species showed lower regulation of
Ψl (e.g., Cheiloclinium cognatum ) and might be
susceptible to hydraulic failures (McDowell, 2011; McDowell et al.,
2008), especially in extreme drought situations, although hydraulic
failaure will also depend on their resistance to xylem embolism. Thus,
this may be an opportunistic and risky behaviour that under conditions
of minimal or moderate stress can be beneficial. Still, it may be
disadvantageous under intense or prolonged stress conditions (Sade et
al., 2012).
Having high or low hydraulic regulation can bring severe implications
for plants. Some studies have shown that, in isohydric species, xylem
vessels embolism is more frequent, since the Ψlmin is
close to P50 (i.e., Ψl value in which the stem hydraulic
conductivity is reduced by half), with a small safety margin (McDowell,
2011). On the other hand, these authors also noted that anisohydric
species have higher safety margins because they maintain xylem tension
above the water potential values that usually cause embolism. In this
case, the safety margin can be an important characteristic with great
interespecific variation. Safety margin variability at the community
level might be favoured by natural selection in environments with
seasonal water restriction, since the duration and intensity of the dry
seasons provide different responses in the functioning of plant
hydraulics and carbon assimilation (McDowell et al., 2008).
Conclusion
The hydraulic functioning of the species within the three studied
vegetation types differed in response to the marked climate seasonality
of the region. Species from the typical cerrado and cerradão showed
relatively similar hydraulic strategies, with higher Ψlregulation under more intense VPD effects. On the other hand, forest
species showed lower Ψl regulation, suggesting less
access to deep water, and under lower effects of VPD. These
characteristics allowed us to propose two different species groups: one
with higher regulation and isohydric behavior (typical cerrado and
cerradão species) and the other with lower regulation and anisohydric
behavior (semi-deciduous seasonal forest species), both under current
climate conditions.
In case drought events become more intense and frequent in this region,
forest species, which have lower hydraulic regulation, may be more
vulnerable. However, to better understand drought resistance conditions
of species we need to consider more drought-resistance traits, such as
the critical xylem water potential and hydraulic safety margins, both
integrated with the regulation attributes of Ψl. Our
study described key hydraulic traits and how they vary throughout the
year for the major vegetation types that occur in the transition of the
two largest South American biomes. It also advanced the knowledge of the
hydraulic functioning patterns of this unique and vulnerable region, to
better understand species and community-level hydraulic responses in a
future scenario of more frequent and more extreme drought events.