|

Received: 24 May 2021    Accepted: 28 September 2021

DOI: 10.1111/1365-2435.13945

REVIEW

Opportunities, challenges and pitfalls in characterizing plant

water-­use strategies

Steven A. Kannenberg1  | Jessica S. Guo2,3  | Kimberly A. Novick4  |

William R. L. Anderegg1  | Xue Feng5,6  | Daniel Kennedy7  |
Alexandra G. Konings8  | Jordi Martínez-­Vilalta9,10  | Ashley M. Matheny11

1
School of Biological Sciences, University of
Utah, Salt Lake City, UT, USA Abstract
2
Department of Geology and Geophysics, 1. Classifying the diverse ways that plants respond to hydrologic stress into gener-
University of Utah, Salt Lake City, UT, USA
alizable ‘water-­use strategies’ has long been an eco-­physiological research goal.
3
Arizona Experiment Station, College of
Agriculture and Life Sciences, University of
While many schemes for describing water-­use strategies have proven to be quite
Arizona, Tucson, AZ, USA useful, they are also associated with uncertainties regarding their theoretical basis
4
O’Neill School of Public and Environmental and their connection to plant carbon and water relations. In this review, we discuss
Affairs, Indiana University, Bloomington,
IN, USA the factors that shape plant water stress responses and assess the approaches
5
Department of Civil, Environmental, and used to classify a plant's water-­use strategy, paying particular attention to the
Geo-­Engineering, University of Minnesota,
popular but controversial concept of a continuum from isohydry to anisohydry.
Minneapolis, MN, USA
6
Saint Anthony Falls Laboratory, University 2. A generalizable and predictive framework for assessing plant water-­use strategies
of Minnesota, Minneapolis, MN, USA has been historically elusive, yet recent advances in plant physiology and hydrau-
7
National Center for Atmospheric Research,
lics provide the field with a way past these obstacles. Specifically, we promote the
Boulder, CO, USA
8
Department of Earth System Science,
idea that many metrics that quantify water-­use strategies are highly dynamic and
Stanford University, Stanford, CA, USA emergent from the interaction between plant traits and environmental conditions,
9
CREAF, Bellaterra (Cerdanyola del Vallès), and that this complexity has historically hindered the development of a generaliz-
Catalonia, Spain 10Universitat Autònoma de
Barcelona, Bellaterra (Cerdanyola del Vallès), able water-­use strategy framework.
Catalonia, Spain 3. This idea is explored using a plant hydraulics model to identify: (a) distinct tem-
11
Department of Geological Sciences,
poral phases in plant hydraulic regulation during drought that underpin dynamic
Jackson School of Geosciences, University
of Texas, Austin, TX, USA water-­use responses, and (b) how variation in both traits and environmental forc-
ings can significantly alter common metrics used to characterize plant water-­use
Correspondence
Steven A. Kannenberg strategies. This modelling exercise can bridge the divide between various concep-
Email: s.kannenberg@utah.edu
tualizations of water-­use strategies and provide targeted hypotheses to advance
Funding information the understanding and quantification of plant water status regulation across spa-
National Institute of Food and Agriculture,
tial and temporal scales.
Grant/Award Number: 2018-­67019-­27850;
National Aeronautics and Space 4. Finally, we describe research frontiers that are necessary to improve the predic-
Administration, Grant/Award Number:
tive capacity of the plant water-­use strategy concept, including further investiga-
80NSSC18K0715; David and Lucille Packard
Foundation; Biological and Environmental tion into the below-­ground determinants of plant water relations, targeted data
Research, Grant/Award Number: DE-­
collection efforts and the potential to scale these concepts from individuals to
SC0020116 and DE-­SC0022052; U.S.
Forest Service, Grant/Award Number: EM whole regions.
19-­05; Division of Environmental Biology,
Grant/Award Number: 1714972, 1753845,
1802880, 1942133, 2003017 and 2045610;
Division of Earth Sciences, Grant/Award

|
24     © 2021 British Ecological Society wileyonlinelibrary.com/journal/fec Functional Ecology. 2022;36:24–37.
KANNENBERG et al.
Number: 2046768; Spanish Ministry of
KEYWORDS
Science, Grant/Award Number: CGL2017-­
89149-­C2-­1-­R drought, isohydry, plant hydraulics, water potential, water-­use strategy
Handling Editor: Katherine McCulloh
1 |  I NTRO D U C TI O N
Plant water transport regulation underlies many aspects of physi-
ological ecology and serves as a central linkage between the water
and carbon cycles (Mencuccini et al., 2019). Over the years, numer-
ous efforts have been made to characterize the water-­use dynamics
of different plant species and understand the consequences of in-
terspecific variability in water use for plant health and physiology. At
their conception, these frameworks were viewed as broad notions
characterizing life-­history strategies such as ‘conservative versus
profligate’, ‘tolerant versus avoidant’ or ‘water savers versus spend-
ers’ (Jones, 1980; Ludlow, 1989; Noy-­Meir, 1973).
Theoretical and mathematical advances in stomatal optimization
(Katul et al., 2010; Medlyn et al., 2011) and plant hydraulics models
(Anderegg, Wolf, et  al.,  2018; Novick, Ficklin, et  al.,  2016; Sperry
et al., 2017) provide the foundation for a more quantitative perspec-
tive on plant water-­use strategies linked to directly measurable water
fluxes and potentials. The ‘isohydry–­anisohydry’ framework, which
classifies plant species based on the sensitivity of water potential
as water availability declines, is an especially popular approach for
describing a water-­use strategy (Hochberg et al., 2017; Jones, 1998;
Tardieu & Simonneau,  1998). Other common approaches focus on
the degree of ‘risk’ a plant's hydraulic system faces during drought,
which depends both on intrinsic traits related to embolism resis-
tance and the stringency of stomatal regulation. Indeed, most of
the approaches to quantify a plant's water-­use strategy are based
on common hydraulic traits or the sensitivity of response variables
to fluctuations in water limitation. The water-­use strategy concept
has also been extended to assess the physiological consequences of
drought for plant carbon and water relations, with occasional suc-
cess (e.g. Kannenberg et al., 2019; McCulloh et al., 2019; McDowell
et al., 2008; Meinzer et al., 2017). As attempts to characterize broad
water-­use strategies grew, so did efforts to develop quantitative
and generalizable ‘metrics’ that are representative of these strate-
gies and can capture relevant physiological processes to plant water
stress.
Despite recent advances, major uncertainties remain regarding
the key axes of variation in water-­use strategies (Feng et al., 2018). In
particular, a common criticism is that many water-­use metrics do not
account for environmental forcings and interactions. Specifically,
the average slope of the relationship between leaf water potential
and soil water potential or the water potential at half the maximum
stomatal conductance are among the most popular metrics for clas-
sifying the degree of isohydry and are often interpreted as a trait.
However, within sites and species, these metrics vary as a function
of environmental drivers like temperature and humidity. Likewise,
there may be intraspecific variability in water-­use strategies due
Functional Ecology |
      25
to macro-­scale couplings between soil moisture and atmospheric
drivers, or as a function of site-­to-­site differences in rooting depth
caused by subsurface variability (i.e. bedrock depth, rock fraction,
soil texture). While such plant–­environment interactions have
formed the backbone of modern plant hydraulics research (Sperry
& Love, 2015; Tyree & Sperry, 1989), it is only recently that their
importance has been tackled specifically within the context of a
water-­use strategy. Spatial and temporal variation in a metric that
is often interpreted as an intrinsic strategy is confusing and unde-
sirable towards the goal of distilling the complexity of plant water
use into a few key generalizable axes of variation. These uncer-
tainties have resulted in calls to revisit water-­use strategy frame-
works (Martínez-­V ilalta & Garcia-­Forner,  2017) or abandon them
altogether (Hochberg et al., 2017). Given these issues, the pressing
questions moving forward are:
1. What are the advantages and disadvantages of various metrics
used to quantify plant water-­use strategies?
2. What is the predictive power of these current metrics?
3. What are the information gaps that need to be addressed to move
the concept of generalizable plant water use strategies forward?
This review will seek to answer these questions by integrating
cross-­disciplinary work on plant water-­use strategies from theory,
physiology, modelling and remote sensing. Throughout, we identify
how the plant water-­use strategy concept needs to draw on exist-
ing physiological and hydraulic research to consider the interactions
between plant traits, environmental conditions and physiological
responses. These interactions, along with limited consideration for
below-­ground processes, are reasons why a generalized view of
plant water-­use strategies has been so elusive. Finally, we present a
modelling exercise that provides novel insights regarding the physio-
logical and environmental factors that give rise to a plant's water-­use
strategy, and highlight the approaches and data sources that will be
necessary to move the concept forward.
2 | A N O RG A N IZ I N G FR A M E WO R K
FO R TH E PL A NT WATE R- ­U S E S TR ATEG Y
CO N C E P T
Historically, ‘plant water-­use strategy’ has been used as a general
conceptual term to characterize plant water use or the regulation
of water status, and thus simplify the enormous variability in plant
responses to variations in hydrometeorological conditions. This
concept has served multiple purposes, such as: (a) delineate eco-­
physiological or life-­history trade-­offs between individuals and
26       |
Functional Ecology KANNENBERG et al.

species, (b) provide a predictive framework regarding the conse-
quences of water stress and (c) shed light into the traits, processes
and parameterization schemes that need to be included in vegeta-
tion and land–­atmosphere exchange models.
We propose a framework and terminology that differentiates
the common approaches for characterizing water-­use strategies
(Figure  1). Our framework is based on the recognition that many
factors interact to determine a plant's water-­use strategy across a
range of spatio-­temporal scales. Climate and site factors are long-­
term controls on plant water use dynamics, as they determine the
vegetation functional types and life-­history strategies that can exist
in a given environment. These functional relationships shape the
distribution of plant traits that are possible, and this distribution is
further altered by phenotypic plasticity and adaptive processes. It
is common to infer a plant's water-­use strategy using combinations
of traits, which we call a ‘trait syndrome’ approach. Trait syndrome
approaches largely rely on empirical measurements, but can also be
derived from water status observations via inverse modelling. Trait
syndrome metrics are based in plant physiological theory and should
describe relatively durable properties of a plant's water use strategy,
but are also limited in that the number of relevant traits is potentially
large and our understanding of their coordination is limited.
Other approaches to quantify water-­use strategies rely on various
measured response processes, which we refer to as ‘response-­based’
approaches. These metrics traditionally leverage measurements of
transpiration, stomatal conductance or water potential. However,
these observations are heavily influenced by their specific meteo-
rological context, as short-­term variability in environmental forcings
imposes direct and indirect effects on water status. For example, the
direct effect of increased vapour pressure deficit (VPD), with all else
held constant, would be a roughly proportional increase in transpira-
tion. Increasing VPD is likewise usually associated with reduced sto-
matal conductance, which would indirectly mitigate such increases
in transpiration. Response-­based metrics integrate the influence of
plant traits, physiological responses and short-­term environmental
forcings. They are thus a more accurate quantification of a plant's
water-­use strategy at a given place and time, but are less likely to be
consistent across broader spatio-­temporal scales.
Recent approaches strive for a more generalizable approach
by standardizing response-­based metrics for various environmen-
tal forcings and carefully considering the interplay between plant
traits, meteorological conditions and physiological responses. These
approaches could, in principle, be used to identify relatively stable
water-­use strategies. We discuss these promising advances in later
sections.
Our framework illustrates the broadness of the water-­use strat-
egy concept, which has been used interchangeably to describe reg-
ulation of both water flow and water status (i.e. water potential).
Combining these interlinked, yet distinct, aspects of plant water
relations under the plant water-­use strategy framework presents a
conceptual challenge. For example, a plant that ceases to use water
is not necessarily water stressed. In addition to characterizing trait
syndrome versus response-­based approaches, we propose that fu-
ture research on plant water-­use strategies differentiates between
water flow and water status regulation. Although these two as-
pects are linked and have been frequently used interchangeably in
the literature, they are not equivalent (Martínez-­Vilalta & Garcia-­
Forner, 2017). Here, we will focus on the characterization of water
potential regulation due to a recent focus in the literature, its con-
nections to the growing field of plant hydraulics and its utility as an
integrator of various aspects of plant physiology. Moreover, mea-
surements of water potential are common and new data sources pro-
vide an avenue to scale water potential measurements across space
and time (Konings et  al.,  2019). The increasing frequency at which
plant hydraulic schemes are being incorporated into large-­scale veg-
etation models (e.g. Eller et  al.,  2020; Kennedy et  al.,  2019; Sabot

Fast
Meteorology Plant physiological Response-based
VPD responses Quantifies variation in
Light Conductance physiological responses over time
Plant–
Temperature environment Water potential
Water availability interactions Transpiration

WATER-USE STRATEGY
Water flow Water status Drought
Abiotic factors Biotic factors regulation regulation responses
Water saver/spender Degree of isohydry
Temporal variability

Conservative/profligate Avoidant/tolerant

Pedo-climate Plant traits

MAT, MAP Plasticity and P50
Seasonality adaptation Root structure Trait syndrome
Lithology Allometry Quantifies coordination of traits
Edaphology Stomatal anatomy that result in functional groups
Topography
Slow

F I G U R E 1   Conceptualization of the factors that shape a plant's water-­use strategy that highlights the common ways that plant water-­use
strategies are quantified
KANNENBERG et al.
et al., 2020) also foreshadows the utility of linking plant water poten-
tial regulation to broad-­scale carbon and water cycling.
3 |  Q UA NTI F Y I N G PL A NT WATE R- ­U S E
S TR ATEG I E S
The distinction between trait syndrome and response-­based ap-
proaches to quantifying water-­use strategies (Figure  1) is a chal-
lenge for the plant water-­use strategy concept: how can we best
condense the complexity of plant physiological responses to water
stress into a quantitative metric of hydraulic regulation, and what
is the utility of such frameworks? This fundamental question has
resulted in a variety of approaches towards characterizing water-­
use strategies (see Feng et  al.,  2019 for a detailed comparison of
water-­use strategy metrics). Here, we provide a brief overview of
the strengths and weaknesses of trait syndrome and response-­
based approaches.
3.1 | ‘Trait syndrome’ metrics
Trait syndrome metrics rely on common plant hydraulic traits such
as P50 (the water potential at which 50% of hydraulic conductivity
is lost), the water potential at stomatal closure or the water poten-
tial at turgor loss (e.g. Brodribb & McAdam,  2013; Mirfenderesgi
et al., 2016; Pivovaroff et al., 2018; Skelton et al., 2015). The wide
availability of plant trait information contained in trait databases
such as TRY (Kattge et  al.,  2020) facilitates the quantification of
these metrics across a variety of species. Moreover, a large litera-
ture surrounding the coordination of hydraulic traits suggests the
existence of fundamental trade-­offs between carbon gain and water
loss—­implying that basic axes of variation in plant water use can be
captured by these traits (Reich,  2014). Trait syndrome approaches
are conceptually appealing relative to response-­based approaches
since, by being treated as independent from climatic and hydromete-
orological conditions, they are generally easier to interpret.
However, trait interactions are often complex and multidimen-
sional (Mursinna et al., 2018, Rosas et al., 2019), which would suggest
that plant water-­use strategies may sometimes not be fully captured
by a few univariate traits. Unfortunately, many efforts to create
metrics of plant water use rely on one or two commonly measured
traits. Furthermore, these metrics are commonly constructed using
species-­level means from trait databases, an approach that does not
account for intraspecific trait variation (Figure 2a; Anderegg, 2015;
Anderegg, Konings, et  al.,  2018; Rosas et al., 2019). Intraspecific
variability can be especially problematic for generalizing species'
responses when traits are measured under controlled contexts on
young plants (i.e. in a greenhouse or growth chamber) and applied to-
wards understanding the drought responses of mature individuals in
the field. Trait means from a database likely inadequately represent
the complex realities of plant water use, especially when such means
obscure important spatio-­temporal and intraspecific variability.
Functional Ecology |
      27
Plant traits can vary in space and time depending on hydrologi-
cal conditions. For example, some traits such as minimum leaf water
potential (which is implicitly calculated over the measured period)
and turgor loss point can fluctuate substantially in response to soil
and atmospheric dryness (Bartlett et  al.,  2014). Water-­use metrics
such as hydraulic safety margin that depend upon minimum leaf
water potential are thus challenging to interpret (Martínez-­Vilalta
et al., 2021). These variations are rarely accounted for because trait
databases often do not report sufficient metadata regarding the
environmental context during which these more dynamic variables
were collected; for example, was a particular minimum leaf water
potential observation collected during a normal growing season, or
one characterized by a severe drought event? Thus, approaches that
are actually response-­based can be mischaracterized as trait syn-
drome approaches and are unlikely to be generalizable across cli-
matic contexts.
3.2 | ‘Response-­based’ metrics
Response-­based metrics seek to quantify changes in stomatal con-
ductance, transpiration, hydraulic conductivity or water potential
during a specified dry-­down period or across a range of natural vari-
ation in water availability (e.g. Fisher et al., 2006; Franks et al., 2007;
Klein, 2014; Martínez-­Vilalta et al., 2014; Meinzer et al., 2016). The
benefit of these approaches is that they are based around the in-
tegrated physiological changes observed during water stress, thus
circumventing many of the issues pertaining to the uncertain link-
ages between traits and physiological responses. These metrics can
be quantified without explicit linkages to the mechanistic causes of
variation in plant water-­use strategies.
Response-­based approaches are not without limitations, as
these metrics are often derived from leaf water potential, which is
most commonly measured non-­continuously via destructive sam-
pling. Such sparse measurements are not well-­suited for comparison
across species, functional groups or large spatial scales. The lack of
temporal and spatial uniformity of these data exposes these metrics
to bias introduced by variation in environmental drivers at scales not
captured by the intermittent sampling (e.g. diurnal variation in VPD,
Novick et al., 2019). Thus, these metrics may be calculated using a
small sample of data that are not representative of the complete dis-
tribution (e.g. Figure 2b), which obscures possible associations with
environmental drivers and limits comparability between metrics
from different climatic contexts. Finally, many of these metrics (even
if standardized by various environmental drivers) may be sensitive
to and influenced by the conditions in which they were measured,
which may limit their generality.
3.3 | Consistency across metrics
Unfortunately, there is a lack of consistency across metrics in
the relative ranking of a species' water-­use strategy, even when
28       |
Functional Ecology KANNENBERG et al.

(a)
0.8 Juniperus osteosperma
Pinus ponderosa
0.6 Populus tremuloides
Kernel density

Pseudotsuga menziesii

0.4

0.2

0.0
−7 −6 −5 −4 −3 −2 −1
P50 (MPa)
(b)
Jan Feb Mar Apr May Jun
125 Automated 8
100 Manual
6
75
4
Count (automated)

50

Count (manual)
25 2
0 0
Jul Aug Sep Oct Nov Dec
125 8
100 6
75
50 4
25 2
0 0
−9 −6 −3 0 −9 −6 −3 0 −9 −6 −3 0 −9 −6 −3 0 −9 −6 −3 0 −9 −6 −3 0
Ψpd (MPa)

F I G U R E 2   An illustration of the methodological pitfalls of using trait syndrome approaches (i.e. intraspecific variability) versus response-­
based approaches (i.e. non-­representative data). (a) Kernel density estimate plot of stem P50 values for four tree species common to the
western United States and (b) histograms showing the frequency of predawn water potential observations for Larrea tridentata from
automated stem psychrometers (n = 2,324, orange) versus manual measurements via pressure chamber (n = 144, grey). Note the double axes
in Figure 2b. Data for panel (a) come from the XFT database (Choat et al., 2012) after dropping outliers (>2 standard deviations from the
mean P50). Data for panel (b) are from the study by Guo et al. (2020)

measurements are made in a standardized fashion (Li et  al.,  2019;
Martínez-­Vilalta & Garcia-­Forner, 2017). This finding likely reflects
that these different metrics are not conceptually consistent and cap-
ture different aspects of plant physiology (Figure  1). For example,
metrics that rely on xylem traits to characterize the risk of hydraulic
failure are likely to be relatively consistent over time within an in-
dividual (but see Hacke et al., 2001)—­though they do not consider
other central aspects of drought responses such as root structure
and subsurface features. In contrast, flow-­based metrics (using
measures of sap flow, transpiration or stomatal conductance) are
better suited to capture such contextual differences, though some-
times stomatal conductance fails to capture water loss through the
cuticle, which can be considerable in plants experiencing extreme
drought (Machado et al., 2020). While it is perhaps unsurprising that
different water-­use strategy metrics reflect different dimensions of
plant physiology, it does raise significant questions regarding the
utility of these metrics—­how can the field come to consistent con-
clusions regarding a plant's water use if our metrics capture funda-
mentally different processes?
4 | C H A LLE N G E S I N CO N C E P T UA LIZ I N G
PL A NT WATE R- ­U S E S TR ATEG I E S
As it currently stands, we lack a consistent and generalizable view of
plant water-­use strategies, which is striking given how much focus
has been devoted to the topic in recent decades. This is partially
due to methodological issues inherent with the data sources we use
to construct metrics of plant water use. These include the afore-
mentioned issues regarding intraspecific trait variability, variability
in plant physiological responses caused by fluctuating environmen-
tal conditions and conflating trait syndromes with response-­based
KANNENBERG et al.
approaches. However, much of the problem is linked to conceptual
challenges that obscure a generalizable plant water-­use strategy
framework. In the following sections, we highlight recent progress
that illustrates how the assumptions inherent in many popular plant
water use frameworks can fail under certain conditions. We then
leverage these studies to identify research frontiers that will be nec-
essary towards developing theoretically robust and predictive met-
rics of plant water use.
4.1 | Can we define relatively stable water-­use
strategies?
We propose that a core limitation inherent in common plant water-­
use metrics is a lack of proper consideration of dynamic responses to
environmental variability. In practice, these metrics are usually con-
structed to treat plant water-­use dynamics as species-­specific strat-
egies that remain static throughout space and time. However, given
that intraspecific and temporal variability in both plant traits and
physiological responses has been common knowledge for decades,
describing relatively stable water-­use strategies remains a challenge.
The idea that there is significant plasticity in plant water-­use strat-
egy metrics is gaining empirical support. For example, a recent study
found high temporal variability in Larrea tridentata water potential
regulation (Guo et al., 2020). This desert shrub experienced highly
dynamic hydrologic conditions throughout the year and altered its
water status regulation accordingly—­from highly anisohydric be-
haviour during the wet season to more isohydric behaviour as the
ecosystem dried. Significant spatial and temporal plasticity has also
been found in Quercus douglasii water potential regulation and was
attributed to variability in climatic, topographic and edaphic condi-
tions (Feng et al., 2019).
The effect of VPD variation on water-­use strategies requires
particular consideration. Novick et al. (2019) found that short-­term
changes in VPD alters the apparent sensitivity of water potential
independently of stomatal behaviour. Understanding the effects
of atmospheric aridity on the stringency of plant water potential
regulation in particular is especially important in the face of climate
change, as increases in VPD may outpace phenotypic plasticity in
some plant traits, causing shifts in plant water-­use strategy metrics
independent of physiological acclimation or demographic turnover.
The importance of atmospheric demand in modulating water poten-
tial regulation has resulted in the development of new metrics that
explicitly allow a plant's degree of iso-­anisohydry to vary with VPD
(Mrad et al., 2019; Novick et al., 2019). These models are an essen-
tial step forward in recognizing the plasticity in how plants regulate
water potential and could provide a roadmap for more holistic and
standardized water-­use strategy metrics.
There is an emerging consensus that the dynamic interactions
between plant traits and the environment affect commonly used
water-­use strategy metrics (Feng et al., 2018; Hochberg et al., 2017).
If the goal of these metrics is to provide a generalizable glimpse into
Functional Ecology |
      29
the physiological processes underlying plant drought responses,
this variability in water-­use metrics is a major impediment. While
such variability can provide novel insights regarding drought eco-­
physiology, spatio-­temporal consistency and low intraspecific
variability are necessary to apply these metrics at broad scales
and integrate them into vegetation models (Matheny, Fiorella,
et al., 2017). Experimental and observational approaches that quan-
tify the mechanisms behind variability in plant water-­use metrics
are a necessary step towards this aim, as are modelling approaches
where multidimensional trait variability can be explored in detail and
environmental conditions can be standardized (Feng et al., 2018).
4.2 | Looking below-­ground
Our knowledge of plant–­e nvironment interactions is often shaped
by the tools we have available (Körner, 2021). Accordingly, our un-
derstanding of plant water use (and plant eco-­p hysiology in gen-
eral) is heavily centred on above-­ground tissues and processes.
This limitation is particularly striking considering that the highly
dynamic below-­ground environment plays a crucial role in medi-
ating plant water stress responses (Brunner et  al.,  2015; Phillips
et al., 2016). Indeed, plant water-­use strategies can shift within a
species due to variation in rooting depth, root hydraulics and soil
biotic interactions (Jiang et al., 2020; Kannenberg & Phillips, 2017;
Matheny, Mirfenderesgi, et  al.,  2017). Inferences regarding plant
water sourcing and below-­ground behaviour are often limited
by current model representations that treat the rhizosphere as a
one-­dimensional profile, with no lateral interaction or competition
(Warren et  al.,  2014). However, root structure and interactions
have been shown to alter the spatio-­temporal evolution of both
soil moisture and plant water sourcing (Agee et al., 2021; Couvreur
et  al.,  2012; Guswa,  2012). In addition, edaphic and lithological
factors at a site often constrain the overall amount of water avail-
able to plants and can either ameliorate or exacerbate the cli-
matic stress imposed on plants (Hahm et  al.,  2019; McLaughlin
et  al.,  2020). Variation in nutrient availability also affects im-
portant plant hydraulic traits (Oliveira et  al.,  2018), which could
serve as another source of spatio-­temporal variability in plant
water-­use strategies (Gessler et  al.,  2016). Hydraulic disconnec-
tion between soil and roots due to xylem embolism, root shrinkage
or fine root mortality is also underexplored and could alter the
apparent plant water-­use strategy during and following drought
(Jackson et  al.,  2000). However, the degree to which root physi-
ology, below-­ground biotic interactions, hydrology and edaphic/
lithological factors intersect with the concept of plant water-­use
strategies is highly underexplored and an area ripe for future in-
vestigation. Cross-­s cale advances in measuring below-­ground
plant hydraulics and soil moisture, in conjunction with more fre-
quent and widespread measurements of water potential (see ‘Data
needs’ and ‘Scaling from leaves to ecosystems’ sections below),
provide a promising avenue forward in this regard.
 |
30      
Functional Ecology
4.3 | Can we predict the physiological
consequences of drought?
A powerful application of the plant water-­use strategy concept
lies not just in describing the dynamics of water transport and
regulation during drought, but in understanding the downstream
physiological consequences of this behaviour. The ramifications
of various water-­use strategies have been most extensively re-
searched in the context of the isohydry–­anisohydry framework
(McDowell,  2011; McDowell et  al.,  2008). Specifically, isohydric
species were hypothesized to experience carbon limitation due to
stomatal closure, which if lengthy enough, can result in a detri-
mental depletion of stored sugars and starches. In contrast, an-
isohydric plants were predicted to be prone to hydraulic damage,
since their propensity towards open stomata can lead to damag-
ing drops in water potential during severe drought and thus ap-
proach thresholds for significant embolism formation. However, in
the past few years, evidence has accumulated that obfuscates the
direct link between leaf-­level behaviour and carbon–­water rela-
tions (Martínez-­V ilalta & Garcia-­Forner, 2017). While some studies
have observed a link between anisohydric behaviour and hydraulic
risk (e.g. Kannenberg et al., 2019; Pivovaroff et al., 2018), others
have found that relatively isohydric species can also experience
significant xylem embolism during drought (Duan et  al.,  2015;
Gaylord et  al.,  2015). Likewise, drought-­induced depletion of
stored carbon in isohydric trees is infrequently observed (Duan
et  al.,  2015; Gruber et  al.,  2012; Kannenberg & Phillips,  2020;
Weber et  al.,  2019). The rarity of carbon depletion in isohydric
species likely reflects the complex interplay between water status,
carbon assimilation, active carbon allocation and sink limitation
during periods of water stress (Dietze et  al.,  2014; Hoch,  2015;
Körner, 2003, 2015).
Resolution of these issues is currently an area of active research.
However, most of the aforementioned studies take a qualitative
approach towards defining a plant's water-­use strategy and rarely
consider environmental context, and thus a definitive link from
water-­use strategies to physiological outcomes has yet to be es-
tablished. Studies that pair quantitative metrics of plant water use
with measurements of hydraulic damage and carbon dynamics (e.g.
Gattmann et al., 2021), in both experimental and observational con-
texts, are key steps forward to demonstrate if water-­use strategies
can be used to understand the consequences of drought, including
susceptibility to mortality.
5 |  Q UA NTI F Y I N G WATE R U S E
S TR ATEG I E S I N A M O D E LLI N G
FR A M E WO R K
Thus far, we have identified: (a) issues with traditional metrics
of water-­u se strategies that arise from a failure to consider their
spatio-­t emporal variability, and (b) uncertainties regarding the
traits and processes (especially below-­g round) that underpin
KANNENBERG et al.
these water-­u se strategies. Here, we use a modelling approach to
demonstrate these concerns, focusing on the popular isohydric-
ity framework. We employed a ‘gain-­r isk’ plant hydraulics model
(Sperry et al., 2017) to quantify the benefit of stomatal opening
for carbon gain relative to the associated risk of hydraulic dam-
age. This model is driven by a set of common plant traits (see
Supporting Information for model details, traits, validation and
parameterization) and accurately predicts leaf water potential,
gas exchange and hydraulic damage across a wide range of en-
vironmental conditions (Love et al., 2019; Venturas et al., 2018).
Using hourly meteorological data from 2019, along with a mix
of in situ measured plant traits and literature values (Table S1),
we applied this model in a near-­m onodominant stand of Pinus
ponderosa located in Big Cottonwood Canyon, Salt Lake City,
UT (40°38′37.1″N, 111°38′17.4″W). P. ponderosa was chosen
since it is an important and widespread species in the western
United States, it has been demonstrated that our model accu-
rately predicts its water status during drought events (Venturas
et  al.,  2020), and it is known to have a water-­u se strategy that
is representative of many other widespread species (Martínez-­
Vilalta et  al.,  2014). To quantify variation in water-­u se strat-
egy, we also conducted a sensitivity analysis by varying traits
associated with water acquisition and loss. These trait values
were based on previously obtained values for other conifers
(see Supporting Information). Using modelled leaf water poten-
tials, we quantified this species’ water status regulation during
the growing season from 1 May to 30 September 2019. Here,
we used a common metric of isohydricity (σ) as a case study
(Martínez-­V ilalta et al., 2014), which represents the slope of the
linear relationship between midday (12 p.m.–­3 p.m.) and predawn
(2 a.m.–­5 a.m.) leaf water potentials. We took the additional step
of excluding data where predawn water potential was greater
than −0.5 MPa prior to calculating σ, in order to isolate periods
where stomata exert some control on midday water potential
(Meinzer et al., 2016).
5.1 | Temporal variability in the stringency of water
potential regulation
The model demonstrated significant temporal variability in the
stringency of plant water potential regulation. P. ponderosa was
more anisohydric early in the growing season when precipita-
tion was plentiful, shifted to more isohydric behaviour as water
deficits developed, then returned to anisohydry as late summer
precipitation increased water availability (Figure  3a). This oc-
curred because the nature of the relationship between predawn
and midday water potential was not linear, which is a primary
assumption inherent in many water-­u se strategy metrics that are
based on water potential (Figure  3b). A nonlinear relationship
between predawn and midday water potential was recently con-
ceptualized by Wu et al. (2020) and Knipfer et al. (2020), where
during wet periods (‘Phase 1’ in Figure 3b) there is little stomatal
KANNENBERG et al.       31
Functional Ecology |
F I G U R E 3   Temporal variability in the 2.0 (a) 0.0 (b) VPD (kPa)
metric of iso-­anisohydry (σ) binned across 3
Precipitation (mm)
months during the growing season (a), and σ

Midday water potential (MPa)

1,500 2

simulations of predawn and midday water 1.5 −0.5 1

Precipitation (mm)
potential (b)

1,000 −1.0

σ
1.0
Phase 1

−1.5
500
0.5 Phase 2

−2.0 Phase 3

May Jun Jul Aug Sep −2.0 −1.5 −1.0 −0.5 0.0
Month Predawn water potential (MPa)

F I G U R E 4   Variability in our metric (a) (b) (c)

of iso-­anisohydry (σ) due to variation
in hydraulic traits, morphological traits
1.0 1.0 1.0
and meteorological conditions, including
rooting depth (panel a), vapour pressure
σ

deficit (‘VPD’, panel b), the water potential

at which 50% of xylem conductivity is lost 0.5 0.5 0.5
(‘P50’, panel c), stand basal area (‘Ba:Ga’,
panel d), maximum sapwood-­specific
hydraulic conductivity (‘Kmax’, panel e) 1 2 3 4 −20 −10 0 10 20 2 4 6
Rooting depth (m) VPD (% deviation) P50 (−MPa)
and leaf area per unit basal area (‘La:Ba’,
(d) (e) (f)
panel f). The horizontal dashed red line
represents σ during a realistic model run
where measured traits (along with a few 1.0 1.0 1.0
literature values) were used (Table S1)
σ

0.5 0.5 0.5

40 80 120 100 200 300 500 1,000 1,500 2,000

Ba:Ga ( m2/ha) Kmax ( kg hr−1 MPa−1 m−2) La:Ba ( m2 /m2)

control over midday water potentials, which then transitions into
tight stomatal control over water potential during moderate dry
downs (‘Phase 2’). If conditions become dry enough, a ‘Phase 3’
is entered that is associated with the leaf turgor loss point and
declines in hydraulic conductivity (Knipfer et  al.,  2020). In ad-
dition to loss of leaf hydraulic function, the steeper declines in
water potential that characterize this phase could also be due
to transpirative cooling in some species (Aparecido et al., 2020).
However, it is important to note that this ‘Phase 3’ is not com-
mon in the literature nor ubiquitous in the model runs analysed
below (Wu et  al.,  2020), as a fairly severe hot drought is nec-
essary to cause conductivity declines or increased transpira-
tive cooling. Importantly, we saw significant deviations from the
‘Phase 2’ trend due to short-­t erm decreases in VPD. This result
supports the notion that plants respond rapidly to fluctuations
in both soil water availability and atmospheric aridity (Novick,
Miniat, et  al.,  2016; Sulman et  al.,  2017); and that a water-­u se
strategy metric that considers only the relationship between leaf
and soil water potential, without explicitly accounting for atmos-
pheric water demand, will give an incomplete representation of
the overall drought response.
5.2 | Implications for common plant water-­use
strategy metrics
The existence of the three-­phase water potential curve has impor-
tant ramifications for quantifying plant hydraulic regulation, as the
relationship between midday and predawn water potential forms
the backbone of the most common response-­based metrics, specifi-
cally σ (Martínez-­Vilalta et al., 2014) and the ‘hydroscape’ (Meinzer
et al., 2016). The model simulations in the previous section showed
that the environmental context during which water potential meas-
urements are taken is likely to impact estimates of the stringency
of water potential regulation. Specifically, we found that short-­term
fluctuations in VPD have the potential to significantly alter σ, as
does the range of predawn water potentials during which measure-
ments are taken. For example, during a period of moderate water
stress, predawn water potentials likely fluctuate between Phase 1
and Phase 2, resulting in a shallower slope between predawn and
midday leaf water potential than in a more severe drought where a
Phase 3 is present. Short-­term decreases in VPD similarly affected
the magnitude of this slope. Thus, measurements conducted in con-
ditions that do not capture a strong enough atmospheric and soil
 |
32      
Functional Ecology
dry down (such as during a moderate drought or an experimental
drought in a greenhouse) may misrepresent the stringency of water
potential regulation. Species-­level estimates of σ should therefore
be computed using a wide soil (or predawn) water potential gradi-
ent that covers the variety of conditions experienced by the species
in the field. Further investigation of the shape of this curve across
space, time and species will be necessary to advance the conceptual
basis of response-­based metrics. To further elucidate the nuances in
plant water-­use strategies, we suggest an expansion of water poten-
tial observations from pressure chambers and stem psychrometers,
which we discuss in more detail below.
5.3 | Trait variation gives rise to plasticity in plant
water use regulation
While our modelling exercise found significant temporal variability
in σ due to fluctuations in environmental conditions, we also found
shifts in σ can occur due to variation in traits associated with water
acquisition or loss. Some of these relationships were quite intuitive.
For example, we found that synthetically increasing rooting depth
(Figure 4a) allowed greater access to deep water and groundwater
sources, allowing the trees to avoid severe drought stress and thus
remain in the more isohydric Phase 2. Likewise, increasing VPD made
P. ponderosa more anisohydric by driving leaf-­level water loss and the
associated drops in midday water potential (Figure  4b). Increasing
the tree's resistance to embolism (P50) also resulted in more aniso-
hydric behaviour since P. ponderosa could tolerate lower water po-
tentials without detrimental consequences to their hydraulic system
(Figure  4c). However, this increase in anisohydry did not continue
past P50 = −3.5 MPa, likely due to the increased embolism resistance
allowing for greater plant water uptake and depletion of existing
water pools (Martin-­StPaul et al., 2017). We also found that increas-
ing parameters associated with water uptake and demand, such as
stand basal area, maximum hydraulic conductivity per unit sapwood
and leaf area per basal area, made trees more anisohydric, up to a
point (Figure 4d–­f ). However, at more extreme values of these traits,
there was a slight transition towards more isohydric behaviour, likely
because drought stress increased to the point of hydraulic damage,
which limited further drops in midday water potential. Many of the
traits that significantly increased σ pertained to enhanced water use
or demand, causing trees to deplete soil water and experience more
extreme drought stress (De Cáceres et al., 2021). Thus, the interac-
tions between hydraulic traits, environmental variability and water
resources dictated this P. ponderosa stand's water use regulation.
This modelling exploration demonstrated the importance of al-
lometric factors (including maximum sapwood-­specific hydraulic
conductivity, which is primarily controlled by xylem and leaf area)
in dictating a plant's water-­use strategy. In fact, σ was altered more
by allometric variability than by P50 or VPD, which are variables that
are more commonly thought to exert control over a plant's water-­use
strategy. These results also highlight significant equifinality regard-
ing many plant water-­use metrics. There are likely numerous trait
KANNENBERG et al.
and environment combinations that give rise to the same water-­use
strategy (however it is defined), despite the fact that those unique
sets of interactions likely have different ramifications for processes
such as carbon allocation, hydraulic damage and mortality. Further
efforts to constrain these allometric factors are necessary to reduce
the risk of equifinality, though measurements of rooting depth and
leaf area in particular are challenging. While it is a significant meth-
odological difficulty, pairing estimates of above-­ and below-­ground
allometry with plant water potential dynamics will help reduce the
number of unknown trait interactions that shape a plant's water-­use
strategy.
We note that this model, though parameterized mostly with ob-
servational data and driven with observed meteorological forcings,
may not represent the precise interplay between traits, environmen-
tal conditions and water use. Specifically, traits frequently covary
in situ (Mursinna et al., 2018; Rosas et al., 2019) and thus a shift on
one trait without corresponding shifts in other associated traits may
be unlikely. However, our results provide a starting point to predict
temporal, spatial and intraspecific variation in water-­use strategy
metrics, which can be tested with other tree-­level and ecosystem-­
level vegetation models and used to guide fieldwork efforts to char-
acterize the exact nature of these relationships. Importantly, these
modelling approaches can also be used to make predictions across
space and time when we lack field measurements of physiological
response variables.
6 | DATA N E E DS
Despite the uncertainties linked to water-­use strategy classification
highlighted above, there has undeniably been substantial progress
in recent decades linking plant traits and environmental conditions
to plant hydraulic processes. Water potential measurements form
the backbone of much of this research—­they are a necessary com-
ponent of most popular water-­use metrics and are also commonly
used to validate the output of plant hydraulics models. Leaf water
potential measurements are generally easy to make (if canopy access
is possible) and are extremely common. These data, however, are
rarely available to other researchers in a standardized and central-
ized format, and metadata that provide insight regarding the context
of these measurements are not frequently available, despite their
importance (e.g. Figure  2b). Metadata on plant traits, weather and
site factors are a vital step towards contextualizing our quantifica-
tions of plant water-­use strategies. Especially important is recording
the environmental conditions contemporaneous with the measured
water potentials, which would help elucidate when water potential
measurements were made across the three phases of drought we
have identified (i.e. Figure 3b).
It is notable that there is currently no network of water potential
measurements across space and time, especially when viewed in the
light of the numerous existing networks that generate and aggre-
gate observations of ecosystem-­scale carbon and water fluxes and
associated atmospheric drivers (e.g. AmeriFlux, FLUXNET, NEON),
KANNENBERG et al.
and tree census surveys and tree-­ring networks that provide critical
information on growth and mortality (e.g. standardized forest in-
ventories, ITRB). Until very recently, the field also lacked networked
observations of transpiration. The recently created SAPFLUXNET
dataset (Poyatos et al., 2021), which aggregates previously collected
observations of sap flow and meteorological variables, fills an im-
portant gap in this respect. However, SAPFLUXNET is a bottom-­up
network relying on voluntary contributions of previously collected
sap flux observations, in contrast with numerous centralized and
continuously updated efforts to continuously collect ecosystem-­
scale carbon and water fluxes.
One promising way to increase the quantity of water poten-
tial data is through the use of stem psychrometers, which semi-­
continuously measure plant water potential (e.g. Figure 2b) at hourly
time-­scales. Notably, this matches the time-­scale of variability of at-
mospheric drivers such as VPD and matches the frequency at which
eddy covariance or sap flux observations are reported. Unfortunately,
this methodology is limited to non-­resinous woody plants, and thus
the development of new instruments (e.g. Jain et al., 2021), hydraulic
models and/or remote sensing approaches will be needed to infer
water potential dynamics across all vascular plant species. When
paired with other data on water fluxes from eddy covariance towers
or models, expanded water potential datasets will be invaluable for
quantifying variability in plant water use, and for benchmarking and
testing plant hydraulic modelling schemes. New networks focused
on bottom-­up efforts to aggregate water potential data contributed
by site-­level teams, or more top-­down and centralized efforts to sys-
tematically deploy psychrometers (and sap flux) in flux tower foot-
prints, would both represent a major step forward to answer critical
questions in plant eco-­physiology and hydraulics.
7 |  S C A LI N G FRO M LE AV E S TO
ECOS YS TE M S
The majority of studies on plant water-­use strategies have focused
on quantifying and predicting the responses of individual plants or
species to water stress. However, in an era of global ecology, there
is a pressing need to use eco-­physiological theories and quantitative
approaches to inform our understanding of carbon and water cycles
at large spatial scales. Thus, broadening the plant water-­use strategy
concept will serve as a step for improving the predictive capacity
of remote sensing observations, flux measurements and models.
Furthermore, by quantifying plant water use at ecosystem scales, it
may be possible to incorporate the significant spatio-­temporal vari-
ation inherent in individual plant water use into broad-­scale metrics
that could provide a tractable way to predict ecosystem carbon and
water cycles during drought. Moreover, these approaches could set
the stage for new types of water use strategy metrics that account
for the influences of climate and site factors (Figure 1).
Recent work has taken advantage of the sensitivity of remotely
sensed microwave observations to vegetation water content, which
can in turn be linked to leaf water potential (Holtzman et al., 2021;
Functional Ecology |
      33
Konings et al., 2019). This approach enables the estimation of plant
water-­use strategies at canopy scales (Konings & Gentine, 2017; Liu
et al., 2021) and has been linked to site-­level functional traits and
drought responses in eddy covariance data (Anderegg, Konings,
et  al.,  2018). Nevertheless, future work is needed to better char-
acterize the uncertainties of these methods and to account for
cross-­biome variation in how these data are interpreted. A recent
study used a remotely sensed metric of isohydricity to show that
plant water use was quite temporally variable, though the nature
of this plasticity differed based on site aridity. For example, mesic
ecosystems became more anisohydric during dry years, while xeric
ecosystems became more isohydric (Wu et al., 2020). These types of
approaches show great promise for elucidating the spatial and tem-
poral patterns that drive variation in water-­use strategies.
While this field is still developing, these approaches could pro-
vide a powerful way to scale the individual responses of plants
up to inform our understanding of whole ecosystem functioning
during periods of water stress, and understand which ecosystems
are most sensitive to fluctuations in soil moisture and atmospheric
aridity—­processes that are necessary steps towards improving our
capacity to predict the impacts of climate change on terrestrial
carbon and water cycling. However, the success of these broader
scale approaches is partially contingent upon robust and generaliz-
able frameworks of water use and regulation at the individual scale.
Improvements in our conceptualization and quantification of plant
water-­use strategies can form the basis of these broader efforts to
characterize carbon and water fluxes.
8 | CO N C LU S I O N
As the plant water-­use strategy concept transitioned from binary
and qualitative to continuous and quantitative, there was great hope
that this framework could be used as a ‘trait integrator’ of numer-
ous plant physiological processes and thus improve predictions of
the consequences of drought. However, recent evidence has in-
troduced much uncertainty regarding the theoretical basis of plant
water-­use strategy metrics and their practical applicability. To move
this concept forward, we need to draw on recent plant hydraulics
research (Venturas et  al.,  2017) to recognize that plant water use
is controlled by a wide variety of factors and is variable at different
temporal scales due to shifting environmental forcings, allometric
variability and the nonlinearity of water potential dynamics during
drought. Our modelling approach is one such effort towards linking
plant traits with dynamic responses and bridging the gap between
response-­based and trait syndrome conceptions of water use strate-
gies. Further theoretical, observational and empirical methods will
be able to inform a new generation of water-­use strategy metrics
that capture the relevant phases of drought for understanding hy-
draulic damage, carbon dynamics and mortality. To facilitate these
studies, we require water potential datasets of greater quantity and
quality to pair with flux measurements, model output and remote
sensing approaches. By advancing these aims, we can move towards
 |
34      
Functional Ecology
a physiologically relevant understanding of plant water-­use regula-
tion that scales from individuals to ecosystems to the biosphere.
AC K N OW L E D G E M E N T S
The authors extend a special thanks to Martin Venturas for assis-
tance with modelling efforts, Richard Fiorella and Avery Driscoll for
help with field measurements and Emma Sayer for reaching out to
us about the possibility of writing a review. S.A.K. was supported
by the NSF DEB grant 1753845, the USDA Forest Service Forest
Health Protection Evaluation Monitoring program grant #19-­05
and the DOE Environmental System Science program grant #DOE
DE-­SC0022052. A.M.M. was supported by the DOE TES grant DE-­
SC0020116 and the NSF EAR CAREER award #2046768. A.G.K. was
supported by NASA Terrestrial Ecology 80NSSC18K0715 under the
New Investigator program and by the NSF DEB grant 1942133. X.F.
was supported by the NSF DEB grant 2045610. J.M.-­V. was supported
by the Spanish Ministry of Science through grant CGL2017-­89149-­
C2-­1-­R and benefited from an ICREA Academia award. W.R.L.A.
was supported by the David and Lucille Packard Foundation, NSF
DEB grants 1714972, 1802880 and 2003017, and USDA National
Institute of Food and Agriculture, Agricultural and Food Research
Initiative Competitive Programme, Ecosystem Services and Agro-­
Ecosystem Management, grant 2018-­67019-­27850.
C O N FL I C T O F I N T E R E S T
The authors declare no conflict of interest.
AU T H O R S ' C O N T R I B U T I O N S
This review originated as an organized oral session at the Ecological
Society of America meeting in 2020, titled ‘Plant water use strate-
gies in a changing world: Theory, physiology, and implications for
ecosystem function’. All authors were involved in outlining and con-
ceptualizing the review. S.A.K. and J.S.G. contributed the data and
created the figures. S.A.K. led the initial writing efforts with signifi-
cant assistance from J.S.G., K.A.N. and W.R.L.A. All authors were
involved in subsequent feedback and writing and gave final approval
for publication.
DATA AVA I L A B I L I T Y S TAT E M E N T
Data are available via Dryad at https://doi.org/10.5061/dryad.zcrjd​
fnd1 (Kannenberg, 2021).
ORCID
Steven A. Kannenberg  https://orcid.org/0000-0002-4097-9140
Jessica S. Guo  https://orcid.org/0000-0002-9566-9182
Kimberly A. Novick  https://orcid.org/0000-0002-8431-0879
William R. L. Anderegg  https://orcid.org/0000-0001-6551-3331
Xue Feng  https://orcid.org/0000-0003-1381-3118
Daniel Kennedy  https://orcid.org/0000-0001-9494-3509
Alexandra G. Konings  https://orcid.org/0000-0002-2810-1722
Jordi Martínez-­Vilalta  https://orcid.org/0000-0002-2332-7298
Ashley M. Matheny  https://orcid.org/0000-0002-9532-7131
KANNENBERG et al.
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S U P P O R T I N G I N FO R M AT I O N
Additional supporting information may be found in the online ver-
sion of the article at the publisher’s website.
How to cite this article: Kannenberg, S. A., Guo, J. S., Novick,
K. A., Anderegg, W. R. L., Feng, X., Kennedy, D., Konings, A. G.,
Martínez-­Vilalta, J., & Matheny, A. M. (2022). Opportunities,
challenges and pitfalls in characterizing plant water-­use
strategies. Functional Ecology, 36, 24–­37. https://doi.
org/10.1111/1365-­2435.13945