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Acoustic Emissions to Measure Drought-Induced Cavitation in Plants


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Acoustic emissions are frequently used in material sciences and engineering applications for structural health monitoring. It is known that plants also emit acoustic emissions, and their application in plant sciences is rapidly increasing, especially to investigate drought-induced plant stress. Vulnerability to drought-induced cavitation is a key trait of plant water relations, and contains valuable information about how plants may cope with drought stress. There is, however, no consensus in literature about how this is best measured. Here, we discuss detection of acoustic emissions as a measure for drought-induced cavitation. Past research and the current state of the art are reviewed. We also discuss how the acoustic emission technique can help solve some of the main issues regarding quantification of the degree of cavitation, and how it can contribute to our knowledge about plant behavior during drought stress. So far, crossbreeding in the field of material sciences proved very successful, and we therefore recommend continuing in this direction in future research.
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Acoustic Emissions to Measure Drought-Induced
Cavitation in Plants
Linus De Roo *,† , Lidewei L. Vergeynst , Niels J.F. De Baerdemaeker and Kathy Steppe
Laboratory of Plant Ecology, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience
Engineering, Ghent University, Coupure links 653, 9000 Gent, Belgium; (L.L.V.); (N.J.F.D.B.); (K.S.)
*Correspondence:; Tel.: +32-9-264-6115
These authors contributed equally to this work.
Academic Editor: Dimitrios G. Aggelis
Received: 30 December 2015; Accepted: 27 January 2016; Published: 3 March 2016
Acoustic emissions are frequently used in material sciences and engineering applications
for structural health monitoring. It is known that plants also emit acoustic emissions, and their
application in plant sciences is rapidly increasing, especially to investigate drought-induced plant
stress. Vulnerability to drought-induced cavitation is a key trait of plant water relations, and contains
valuable information about how plants may cope with drought stress. There is, however, no consensus
in literature about how this is best measured. Here, we discuss detection of acoustic emissions as a
measure for drought-induced cavitation. Past research and the current state of the art are reviewed.
We also discuss how the acoustic emission technique can help solve some of the main issues regarding
quantification of the degree of cavitation, and how it can contribute to our knowledge about plant
behavior during drought stress. So far, crossbreeding in the field of material sciences proved very
successful, and we therefore recommend continuing in this direction in future research.
Keywords: cavitation; embolism; acoustic emission detection; vulnerability curve; drought
1. Introduction
Stress in materials or structures is often accompanied by the built up of mechanical pressures,
which, upon release, lead to elastic wave propagation away from the stressed zone [
]. These waves are
called acoustic emissions. Today, the acoustic emission technique is widely applied for material testing
and structural health monitoring on engineering materials such as concrete [
], metal alloys [
] and
fiber composite materials [
]. However, the oldest reported scientifically planned acoustic emission
experiment avant la lettre was performed on wood in 1933 by Fuyuhiko Kishinouye [
], long before
the term acoustic emission (AE) was introduced by Schofield in 1961 [
]. In 1966, Milburn and Johnson
used a similar measurement set-up as Kishinouye to detect for the first time AE signals in plants,
when they were subjected to dehydration.
Nowadays, drought associated with global warming gains increasing interest. How plants cope
with drought stress is a topic of an intense debate [
] and urges the need for a good measure
of drought stress. In this paper, the relevant literature contributing to the development of the AE
technique is reviewed in order to propose it as a promising method to measure drought-induced
cavitation in plants.
Before starting, we want to point out the different use of the concept stress between physicists
and plant scientists. As described by Lichtenthaler [
] and according to physics, stress in plants
means the state of a plant under the condition of a force applied. The response of the plant to this
stress is called strain as long as no damage occurs. This distinction is not often made in plant sciences,
where stress and strain are mostly used interchangeably, but which can be confusing in other research
Appl. Sci. 2016,6, 71; doi:10.3390/app6030071
Appl. Sci. 2016,6, 71 2 of 15
fields. Therefore, in what follows, we will use both physically defined terms as an attempt to also
introduce this stress concept in plant sciences.
2. The Importance of Water
On a daily basis, plants extract water from the soil via the roots from where it is transported in
the stem towards the leaves, where it eventually transpires into the atmosphere [
]. This seemingly
wasteful process is vital for plant survival. Water is the transport medium that carries nutrients
from the soil towards the plant organs and distributes generated carbohydrates throughout the plant.
The evaporation of water in the stomata of leaves provides a cooling function, which is necessary to
prevent overheating of leaves during sunny days. The water in living cells also provides a crucial
role in the firmness and elasticity of soft tissues. The positive pressure that is exerted on the cell
walls, called turgor pressure, is essential for growth (through cell growth and cell division) and fulfills
the role of backbone in non-woody tissues such as leaves and petioles. Only a minor fraction of the
transported water (<1%) is used to make new plant material through photosynthesis [
]. Given
this multitude of functions, it is hence no wonder that water shortage is one of the main causes of
plant mortality [21,22].
Water is transported in the xylem tissue of the plant following a gradient in water potential. Xylem
is a porous structure of dead cells containing a network of parallel conduits, interconnected by pits [
The xylem conduits operate under negative pressure, or tension. According to the cohesion-tension
theory [
], the origin of this tension is the evaporation of water in the stomatal region. When the
stomata in the leaves are open, water is transpired due to the difference in water vapour pressure
between the atmosphere and the substomatal cavity. As water evaporates into the air spaces in the
leaf, water menisci in the small capillaries (nanometer scale) in adjacent cell walls are retracted and
capillary forces (due to strong adhesion) pull the menisci back towards the surface. The network of
many small capillaries in the cell wall acts thus as a wick for water rise [
]. Thanks to the strong
cohesion between water molecules, the tension is transmitted downwards and water can be drawn
towards the leaves. The tension in the xylem conduits may increase enormously when faced with a
dry soil or with a great transpirational demand that exceeds the rate of water supply from the roots or
from internal water reserves. This involves a risk of gas bubbles entering the conduits, which may
expand and quickly fill the whole conduit. The water released from the conduits during this process
may contribute to the transpiration stream, but on the other hand, the water conducting system will be
locally interrupted. Because adjacent conduits are interconnected via pits in the conduit walls, the sap
may circumvent the embolized conduit. However, when too many conduits are embolized, this will
impair plant functioning. The formation of air emboli that block sap flow in xylem conduits is currently
of high interest because it is one of the key processes leading to plant mortality during drought [
The phenomenon is called cavitation, which is the mechanical breakage of the continuous xylem water
column and occurs when the tensile strength of the column is exceeded [
]. According to the current
knowledge, the main cause of cavitation is the failure of a pit in the conduit wall to prevent gas from
entering the conduit at strong tension [
], known as the air-seeding hypothesis [
]. Recently, Schenk
et al. [
] postulated that nanobubbles are snapped off during air-seeding. These nanobubbles are
stabilized by surfactants and may exist in plant sap under tension. They may eventually result in an
embolism when the size of the nanobubble exceeds a critical threshold due to increasing tension or
when many nanobubbles coalesce.
A plant’s vulnerability to cavitation is often used as a key feature of its drought resistance [
and has been defined by plotting the percentage loss of hydraulic conductivity (PLC, %) against
decreasing xylem water potential (
, MPa), which results in a vulnerability curve (VC) (Figure 1) [
The xylem water potential at 50% PLC (P50) is the most common parameter to describe a species
“drought resistance”. The cumulative number of AE, originating from cavitation events, are a good
estimate for conductivity loss [
] and thus has the potential to be used as an indirect and
non-destructive method to construct VCs and to determine drought resistance of plants.
Appl. Sci. 2016,6, 71 3 of 15
Figure 1.
Typical vulnerability curve with P12, P50 and P88 representing the xylem water potential at
which, respectively, 12%, 50% and 88% of xylem hydraulic conductivity is lost, adapted from Domec
and Gartner [30] and Fichot et al. [36].
Because of prevailing tensions in plants, xylem is under a metastable state [
], which makes
it a difficult object to study. A small intrusion in the tissue will cause the formation of emboli in the
conduits, hereby influencing the very mechanism that is about to be studied. Therefore, the current
destructive methods are under intense debate [
], triggered as well by recent evidence for possible
artefacts in these techniques [
]. The use of the non-destructive AE technique has therefore gained
renewed interest in plant sciences [
]. In particular, the question about how plants cope with
drought stress in a changing climate, and which mechanisms are underlying drought resistance are
gaining increased importance [
]. Application of AE in plant research can help with answering
these fundamental questions to increase our knowledge on drought tolerance of plants and their ability
to recover from and adapt to predicted future droughts.
3. Acoustic Emission (AE) Application to Measure Drought-Induced Cavitation: From Past
to Present
As stated in the introduction, Milburn and Johnson [
] recorded sounds in plants when they
were subjected to dehydration. They detected audible vibrations (<20 kHz) in petioles of dehydrating
leaves of diverse plant species by fixing the petiole on a phonograph pick-up needle (Figure 2). Because
measurements were often disturbed by environmental noise, the step was made towards AE detection
in the ultrasonic frequency range (>20 kHz) by Tyree and Dixon [
]. This has facilitated various
experiments because the problematic ambient noise in the audible range could be electronically filtered.
Based on similar sound production by the rupture of plant sap under tension in glass tubes [
it was hypothesized that the rupture of sap in plant conduits produced the observed sounds during
drying. Although extensive circumstantial evidence was provided to support this hypothesis [
it was realized that sounds may be produced by other mechanisms too. Sounds were observed during
drying of plant tissues that do not contain conduits [
], during re-watering [
], and also during
freezing [
] and thawing [
]. The AE technique is also applied to monitor internal cracking of
wood during drying [
] and soaking [
]. Moreover, Gagliano et al. [
] speculated that plants may
actively produce sounds for short-distance communication. AE detection is thus an interesting tool,
applicable in a wide range of domains. Further scope of this review is, however, on its application in
the detection of drought-induced cavitation in plants.
Appl. Sci. 2016,6, 71 4 of 15
Figure 2.
Picture of the vibration detector used by Milburn and Johnson [
] to detect drying-induced
sounds in leaf petioles.
During dehydration of fresh plant material, AE signal detection was found to be a valid
method to measure cavitation in woody branches [
], leaves [
], herbaceous stems [
] and sap
wood sections [
], while others found a poor correspondence between hydraulic and acoustic
measurements [
]. Especially in angiosperm species, the continued AE activity after loss of
most of the hydraulic conductivity was a great cause of concern [
]. Other processes than
cavitation in sap-conducting elements that could cause extra AE signals during drought stress have
been suggested by various authors: cavitation of fibers, wood tracheids or ray cells [
mechanical strains [
], and microscopic failure [
]. Moreover, the actual mechanism that
causes cavitation-related AE signals is not exactly known. Different processes have also been suggested:
vibration of the conduit wall after sudden pressure release due to cavitation [
], oscillation of
hydrogen bounds in water after pressure release [
], conversion from liquid water to vapour during
cavitation of the water [
], pit membrane rupture [
], torus aspiration (in gymnosperms [
the entry of a gas bubble through a pore in the pit membrane [
], and subsequent bubble
oscillation [
]. Moreover, as the number of detected cavitation related AE signals may be larger
than the number of cavitated conduits [
], different AE-inducing processes might be involved
during cavitation.
Attempts have been made to use signal features in order to get more insights into the underlying
processes. Ritman and Milburn [
] suggested that vessel length has an influence on the cut-off
frequency of the detected signals. They suggested that cavitation in long vessels produced broadband
signals with frequencies down to 500 Hz, whereas cavitation in fibers and wood tracheids only
produced higher frequencies (>100 kHz). Tyree and Sperry [
] observed that, when detecting AE
signals in the frequency range 50–1000 kHz, the frequency spectra changed towards higher frequencies
when the degree of cavitation increased in Thuja,Pinus, and Acer stems. However, they stayed
indecisive about the possible origin of the signals. Based on the waveforms, Laschimke et al. [
distinguished two types of AE signals in dehydrating leaves of Ulmus glabra: the abrupt disruption
of the water column and an oscillating source that was related to the vibration of gas bubbles during
sap flow. It was also found that AE energy is a function of conduit size and xylem tension [
] and
Rosner et al. [
] found that this parameter might be a better measure for hydraulic conductivity loss
than AE counts.
Although further research is necessary to develop reliable methods for AE data interpretation,
this technique has a high potential for continuous long-term cavitation monitoring in the field [
Already in 1983, Tyree and Dixon [
] (page 1099) were looking forward to the scientific progress that
could be realized with the AE method:
Appl. Sci. 2016,6, 71 5 of 15
“If it can be proved that most ultrasonic AE are a result of cavitation events, then we will have a
powerful diagnostic tool that may give us new insight into the water relations of trees and other plants.”
However, Quarles [
], who was especially interested in AE detection of fractures in wood,
realized that deeper insights in the AE method would be essential for successful implementation:
“For successful implementation, it will be essential to understand how the propagating acoustic
wave changes as a function of factors such as distance and propagating direction between the acoustic
source and the receiving transducer.”
During the past couple of decades, rapid developments in microelectronics have resulted in great
advances in the AE technique. Currently, high performance acquisition systems are available that are
able to record and store waveforms from multiple channels at high sample frequencies [
]. Despite
the large amount of research concerning AE application to measure drought-induced cavitation, the full
potential of these state of the art measurement systems has not been used so far. In what follows,
current state-of-the-art and applications of AE in cavitation research will be illustrated as well as future
opportunities. These deliver important findings that contribute to the development of a powerful
diagnostic AE-tool for online and non-destructive measurement of cavitation.
4. Current State-of-the-Art and Application of AE in Plant Sciences
4.1. Endpoint Selection
Due to the many different AE sources acting during plant dehydration, AE activity can be detected
long after most of the hydraulic conductivity is lost [
]. This makes it difficult to determine the
endpoint (i.e., 100% PLC) of the VC, which physiologically corresponds with complete cavitation
of the xylem vessels and, thus, the full breakdown of the plants hydraulic pathway. As a possible
solution, many studies make use of arbitrary methods. In addition, they focus more on gymnosperms,
because gymnosperms have a more uniform and plain anatomy, and, thus, a more straightforward
AE pattern compared to angiosperms [
]. Wolkerstorfer, Rosner et al. [
] filtered AE measured on
dehydrating Pinus by drawing a straight line “by eye” through the point cloud of amplitude versus
time. If no clear groups can be distinguished in the point cloud, they suggest using other AE features
such as cumulative amplitude or energy until plausible VCs can be constructed. However, one has
to be cautious when using this method, because the filtering has a strong effect on the estimated
vulnerability. Other arbitrary methods include setting the endpoint at a water potential value that
equals (i) the endpoint taken from parallel testing with another method [
]; (ii) a value taken from
literature; or (iii) the turgor loss point of the leaves [78,79].
Vergeynst et al. [
] developed a more mathematical approach to determine the VC endpoint.
Given that PLC should by definition be linked to cumulative AE, and that, according to
Aggelis et al. [
], a specific AE-inducing mechanism results in an AE activity, Vergeynst et al. [
recommended determining the VC endpoint by the end of the AE activity peak, which mathematically
corresponds to the local maximum of the third derivative of the curve of cumulative AE versus time
(Figure 3).
Although the AE activity may continue after the selected endpoint (Figure 3), the obtained P50
values (
2.30 to
2.73 MPa) corresponded well with values found in literature for grapevine (
2.17 to
2.97 MPa; [
]), from which was concluded that the endpoint was accurate, and that the remaining
AE activity was related to other sources than cavitation. Strong evidence for their approach was given
by validation with X-ray micro-computed tomography (
CT), which showed quite similar patterns for
both visually and acoustically detected cavitation [31] (Figure 4).
Appl. Sci. 2016,6, 71 6 of 15
branch 1
5 10
10 10
15 10
20 10
25 10
cum AE
(# signals)
branch 2
Time of deh
branch 3
Figure 3.
Vergeynst et al. [
] calculated the point of 100% loss of hydraulic conductivity (P100) as the
endpoint of the acoustic emission (AE) activity (first derivative of the curve of cumulative AE) peak,
where the third derivative of the curve of cumulative AE signals in time reached a local maximum
(indicated by the vertical dashed line and the “*” symbol). The black line shows the curve of cumulative
AE. Results of measurements on three different grapevine branches are shown.
branch 1
5 10
10 10
15 10
20 10
25 10
cum AE
(# signals)
branch 2
Time of deh
branch 3
Figure 4.
) Cumulative AE (cum AE, grey symbols, left y-axis) detected by four different AE sensors
(1–4) showed a pattern similar to the number of cavitated vessels (black symbols, right y-axis) counted
CT images when plotted against relative radial diameter shrinkage (
d/d), which is a measure
for decreasing xylem water potential. The
CT cross-sections of the grapevine branch are shown for
the beginning (
) and end (
) of the dehydration experiment and at the breakpoint between Phases I
and II (
). The grey zone in (
) delimits the 99.7% confidence interval around the mean cumulative
AE curve [33].
The difficulty in determining the endpoint of VCs based on AEs has also been addressed by
Nolf et al. [
]. To tackle this problem, these authors hypothesized that the highest acoustic activity
Appl. Sci. 2016,6, 71 7 of 15
should occur near the steepest part of the VC, which is the inflection point, reflecting P50. They obtained
good similarity when comparing their method with hydraulic measurements of 16 species. The major
drawback of this approach is that the VC has to have a perfect sigmoidal S-shape. Any deviation from
this ideal curve might cause the steepest part to deviate from the targeted P50 value.
4.2. AE Feature Extraction
A major challenge in using AEs as an indirect measure for cavitation is determination of the source
of the detected signal [
]. The AE signal is shaped by the followed path from source to sensor, which
makes signal interpretation not straightforward because of the wood’s anisotropic characteristics [
These include differences in sound propagation in the three wood directions, wood density, xylem
water content and wood anatomy [
]. Previous AE application in cavitation research mainly focused
on the cumulative AE signal because of the assumption that the majority of the signals correspond to a
loss in hydraulic conductivity [
]. Given the many different AE sources during dehydration,
this assumption is, however, not always valid [
]. Extraction of the AE signals caused by cavitation
is therefore necessary. A method that has already proven its success is extraction of the signals based
on corresponding wave features. In industrial lumber drying, for example, the amplitude and energy
of AE signals were used to pinpointing wood checking [8892].
Rosner et al. [
] measured AEs on juvenile and mature wood samples, taken from living Picea abies
trees, with a broadband sensor in the frequency range 100–1000 kHz. After extraction of the waveform
features amplitude, rise time, rise angle and absolute energy (Figure 5), cumulative AE energy
appeared to be a good measure for PLC and, thus, for VC development. This was confirmed in
other studies on leaves of P. ponderosa,P. nigra,C. chrysophylla and P. japonica [
], and on P. abies
wood samples [
]. Mayr and Rosner [
] found a correlation between tracheid lumen area and
mean AE energy in P. abies wood samples using a 150 kHz resonant sensor, which responds most
strongly to acoustic waves in the 50–200 kHz frequency range. A comparison between samples with
different early-latewood distribution revealed that the mean energy of AEs during wood drying
increased in earlywood but decreased in samples containing more latewood. This was attributed to the
homogeneous structure of earlywood and its larger tracheid diameters, causing AE energy to increase
with increasing xylem tension. More resistant latewood tracheids, which cavitate at a more negative
xylem tension, emitted lower energy because of their smaller diameters and more heterogeneous
structure [
]. Ponomarenko et al. [
] found a similar relationship, confirming that AE energy is
linked to mechanical elastic energy, which is released during cavitation in conifer tracheids. Whereas
AE feature extraction to determine cavitation-related AE has been successfully applied in conifers,
it remains a challenge for the more heterogeneous angiosperms [31,34].
0 800 kHz
Frequency spectrum
0 50 s
rise time
rise angle
Figure 5.
) Frequency features peak frequency (PF), weighted peak frequency (WPF), frequency
centroid (FC) and four partial powers (PP) were used for the automated clustering algorithm;
and (
) Waveform features rise time, amplitude and rise angle describe the shape of the AE signal [
Appl. Sci. 2016,6, 71 8 of 15
Vergeynst et al. [
] proposed clustering to determine cavitation-related AE in angiosperms.
By using state-of-the-art techniques from material sciences, finite element modelling and an automated
clustering algorithm [
], in combination with broadband point-contact sensors, they were able
to extract the AE that originated from cavitation during dehydration of grapevine branches. The flat
frequency response of these sensors in a wide frequency range (20–1000 kHz) allows differentiation
between different AE sources. Instead of relating waveform features of AE signals with cavitation,
Vergeynst et al. [
] recommended to use the frequency features of AE signals. Following Sause and
Horn [
], they extracted from the frequency spectrum, peak frequency (PF), frequency centroid (FC),
weighted PF (WPF, geometric mean of PF and FC) and the partial powers of the following frequency
ranges: 0–100 kHz, 100–200 kHz, 200–400 kHz and 400–800 kHz (Figure 5). The signals that typified
the cavitation phase were characterized by a high intensity at 100–200 kHz. Another signal type, with
high intensity in the range 400–800 kHz, was strongly related with branch shrinkage, and probably
originated from micro-fractures, which are small fissures in the stretched cell wall or pith membrane
due to an initial volume change. Finally, a low-frequency signal type (high intensity below 100 kHz)
was identified that was attributed to macro-fractures or free drainage of water through the porous
wood medium. This clustering approach to identify cavitation-related AE signals is a great advance,
and may lead to the development of a powerful tool to also investigate cavitation in plants in their
native environment. AE sources, such as micro- and macro-fractures, will no longer disturb cavitation
measurements but may provide additional information on, for instance, use of elastic water reserves
or mechanical strains.
It has often been assumed that one AE signal represents cavitation of a single water column [
However, except from the observed one-to-one relationship by Tyree and Dixon [
] and Lewis [
on small sapwood samples of two gymnosperm species, the number of AE signals has been either
lower [
] or higher [
] than the number of cavitating conduits in further experiments.
In measurements on grapevines, the number of cavitation-related AE signals exceeded the number
of vessels in the branch by one or two size orders [
]. Moreover, the amplitude distribution with
maximum signal density near the detection threshold of 28 dB
suggested that a considerable part of
the signals could not be detected because their amplitude fell below the detection threshold, and thus
probably even more AE signals are produced during xylem cavitation [
]. The use of less sensitive
measurement systems, or higher detection threshold settings, might explain cases where less AE
signals than cavitated conduits were observed.
One reason for the higher number of signals observed by Vergeynst et al. [
] could be overlapped
between adjacent cluster types, so that part of the cavitation-related signal type possibly originated
from other co-occurring AE sources, such as micro-fractures or water drainage. This overlap might be
caused by different attenuation of the AE signals dependent on their frequency. The effect of attenuation
was also observed during a freeze-thaw experiment, where it decreased in frozen samples [
A second hypothesis is that the cavitation process generates many AE signals. According to the
nanobubble theory of Schenk et al. [
], many nanobubbles may be formed and exist in the xylem
before they coalesce and form an embolism. Coalescence of these nanobubbles and subsequent bubble
collapse may result in much more AE signals than cavitated conduits. Alternatively, fissures in the
stretched pith membrane or rearrangements of the cell wall layers due to pressure redistribution after
cavitation may cause many AE signals per cavitated conduit. Further research and more detailed
modelling of the actual micro-mechanical processes at the AE source, such as bubble formation and
coalescence, may hopefully throw light on cavitation-related AE sources and, accordingly, on the
processes behind emboli formation.
4.3. In Vivo Measurements
Dealing with drought stress is a dynamic process and the resistance of a plant against drought
depends on both physiological and anatomical characteristics [
]. To obtain a good understanding of
a plant’s behavior during drought stress,
in vivo
measurements on plants are necessary. Conventional
Appl. Sci. 2016,6, 71 9 of 15
methods to determine a plants’ vulnerability to cavitation are destructive, and their results are recently
under intense debate because several artefacts are reported to play a role [
]. In addition,
these methods are labor-intensive, which hampers their applicability in the field. The call for
non-destructive methods is therefore now more urgent than ever [
]. Cochard et al. [
] recently
CT as the standard technique to measure hydraulic vulnerability, but this method is
not suitable for field applications. Today, the AE technique is used in a destructive way and, thus,
subject to similar artefacts as the conventional methods, but in contrast to these established methods,
the AE technique has the potential to measure non-destructively, enabling automated and continuous
measurements of cavitation in the field. Because of the difficult signal interpretation of AEs, only a few
studies have focused on the possibility of
in vivo
measurements of cavitation on actively growing trees
with acoustic sensors. Field measurements on P. sylvestris with a 150 kHz resonant sensor during the
growing season showed good relationships between AE activity and stem diameter variation [
] or
sap flow [
]. In addition, such continuous measurements will provide valuable information on
plant behavior during drought and, more specifically, contribute to the debated process of cavitation
recovery [36,108111].
When using the AE technique on living plants in lab or field conditions, Vergeynst et al. [
] use a
broadband point-contact sensor (20–1000 kHz) with flat frequency response in order to differentiate
between the different AE sources. Based on preliminary analysis and clustering, a minimum set of
signal frequency features may be selected (weighted peak frequency, frequency centroid and partial
powers) that enable discrimination between different AE sources. However, when it is sufficiently
demonstrated that the resonant sensor shows good results, its use might be preferred in further
practical applications because of the more straightforward data processing and interpretation. A second
point of attention for
in vivo
measurements is the particular nature of cavitation detection. Contrary
to the hydraulic method and visualization methods, the AE technique measures changes in the
degree of embolism rather than the degree of embolism itself. This principle should be kept in
mind when preparing and interpreting AE measurements of cavitation. If the initial state of xylem
embolism is known, cumulative AE measurements might result in the degree of embolism if cavitation
has not been repaired in the measurement period. This will require a reference number of AE
signals at 100% embolism, which may be obtained in a VC or at the end of a drought experiment.
Combination of broadband AE measurements with other non-destructive measurements of sap flow,
water potential, water content and xylem/phloem shrinkage [
] may yield the largest insight into
plant water dynamics during drought. A better knowledge of these dynamics is crucial to feed
mechanistic plant and climate models and will help with guiding mitigation of climate change impacts
on plants in natural and agricultural communities [112].
5. Conclusions and Future Perspectives
How plants cope with drought in a changing climate is an active area of research, but a lot of
questions remain unanswered. Mechanisms and strategies that underlie plant survival and mortality
during drought are the subject of an intense debate [
]. The main drivers of this discussion are,
however, the used methods instead of the actual mechanisms that occur in plants [
Development of a universal technique to measure cavitation, and vulnerability to it, will be essential
to bring the debate to a next level, which will change the focus towards physiology behind drought
resistance. In this review, we showed that revival in the use of AEs for detection of plants’ vulnerability
to drought is very promising. It might become a powerful non-destructive, readily automated and
online method. Although great advances were recently made in dealing with the main criticisms of
the technique, such as being indirect and endpoint selection difficulties, further research is needed.
The behavior of AEs in plant material has to be studied, and questions regarding wave propagation
through wood, the behavior of dehydrating wood, and the mechanisms behind cavitation need to
be answered in order to fundamentally link AEs and cavitation events. In order to achieve this,
we recommend:
Appl. Sci. 2016,6, 71 10 of 15
A combination of cavitation measurements with AE broadband sensors and
CT in a broad range
of plant species: interpretation of the acoustic signals in combination with visuals will govern the
largest insights in the mechanisms underlying cavitation.
Feature extraction from the AE signals: this will allow a comprehensive analysis of the AE sources,
and will deliver valuable information on cavitation and other AE producing processes that occur
in drought-stressed plants.
Detailed study of wave propagation and attenuation in plants, both in dehydrating and in
frozen samples.
Investigation of the effects of debarking prior to acoustic measurements: as the bark can be an
additional AE source, this might influence the captured signals.
Further validation of the use of broadband point-contact AE sensors in the field of plant hydraulics
versus the 150 kHz resonance AE sensor.
Development of an in situ AE measurement protocol for living plants, and its translation to
drought sensitivity.
To conclude, the use of AEs in plant sciences to measure cavitation is promising and is gaining
increasing interest. As implementation of some of the state-of-the-art techniques from material sciences
already pushed frontiers in cavitation research, we believe that cross-fertilization between these
different scientific domains will also be beneficial for both in the future.
The authors thank the Research Foundation—Flanders (FWO) for funding (research program
G.0941.15N granted to Kathy Steppe, and PhD Fellowship granted to Lidewei L. Vergeynst).
Author Contributions:
Lidewei L. Vergeynst, Linus De Roo and Niels J. F. De Baerdemaeker reviewed the
literature. Kathy Steppe supervised the work. Linus De Roo wrote most of the manuscript with the input of
Lidewei L. Vergeynst, and all authors contributed by discussing and reviewing drafts and the final version of the
manuscript. Linus De Roo and Lidewei L. Vergeynst contributed equally to the manuscript.
Conflicts of Interest: The authors declare no conflict of interest.
Ernst, R.; Zwimpfer, F.; Dual, J. One sensor acoustic emission localization in plates. Ultrasonics
64, 139–150. [CrossRef] [PubMed]
Robeyst, N.; Grosse, C.U.; de Belie, N. Measuring the change in ultrasonic p-wave energy transmitted in
fresh mortar with additives to monitor the setting. Cem. Concrete Res. 2009,39, 868–875. [CrossRef]
Ohtsu, M. History and fundamentals. In Acoustic Emission Testing; Springer: Heidelberg, Germany, 2008;
pp. 11–18.
Ohtsu, M. Fundamentals and applications. In Acoustic Emission and Related Non-Destructive Evaluation
Techniques in the Fracture Mechanics of Concrete; Woodhead Publishing: Cambridge, UK, 2015; Volume 1,
pp. 11–18.
Jayakumar, T.; Mukhopadhyay, C.K.; Venugopal, S.; Mannan, S.L.; Raj, B. A review of the application of
acoustic emission techniques for monitoring forming and grinding processes. J. Mater. Process. Technol.
159, 48–61. [CrossRef]
Hamstad, M.A. Thirty years of advances and some remaining challenges in the application of acoustic
emission to composite materials. In Acoustic Emission beyond the Millennium; Kishi, T., Ohtsu, M.,
Yuyama, S., Eds.; Elsevier: Oxford, UK, 2000; pp. 77–91.
7. Drouillard, T.F. Anecdotal history of acoustic emission from wood. J. Acoust. Emiss. 1990,9, 155–176.
Kishinouye, F. An experiment on the progression of fracture (a preliminary report). J. Acoust. Emiss.
9, 177–180.
Anderegg, W.R.; Berry, J.A.; Smith, D.D.; Sperry, J.S.; Anderegg, L.D.; Field, C.B. The roles of hydraulic and
carbon stress in a widespread climate-induced forest die-off. Proc. Natl. Acad. Sci. USA
,109, 233–237.
[CrossRef] [PubMed]
Appl. Sci. 2016,6, 71 11 of 15
Allen, C.D.; Macalady, A.K.; Chenchouni, H.; Bachelet, D.; McDowell, N.; Vennetier, M.; Kitzberger, T.;
Rigling, A.; Breshears, D.D.; Hogg, E.T. A global overview of drought and heat-induced tree mortality
reveals emerging climate change risks for forests. For. Ecol. Manag. 2010,259, 660–684. [CrossRef]
Anderegg, W.R.L.; Flint, A.; Huang, C.-Y.; Flint, L.; Berry, J.A.; Davis, F.W.; Sperry, J.S.; Field, C.B. Tree
mortality predicted from drought-induced vascular damage. Nat. Geosci. 2015,8, 367–371. [CrossRef]
McDowell, N.G.; Ryan, M.G.; Zeppel, M.J.; Tissue, D.T. Feature: Improving our knowledge of
drought-induced forest mortality through experiments, observations, and modeling. New Phytol.
200, 289–293. [CrossRef] [PubMed]
Martínez-Vilalta, J.; Lloret, F.; Breshears, D.D. Drought-induced forest decline: Causes, scope and
implications. Biol. Lett. 2012,8, 689–691. [CrossRef] [PubMed]
Zeppel, M.J.; Anderegg, W.R.; Adams, H.D. Forest mortality due to drought: Latest insights, evidence
and unresolved questions on physiological pathways and consequences of tree death. New Phytol.
197, 372–374. [CrossRef] [PubMed]
Doughty, C.E.; Metcalfe, D.; Girardin, C.; Amézquita, F.F.; Cabrera, D.G.; Huasco, W.H.; Silva-Espejo, J.;
Araujo-Murakami, A.; da Costa, M.; Rocha, W. Drought impact on forest carbon dynamics and fluxes in
amazonia. Nature 2015,519, 78–82. [CrossRef] [PubMed]
Hartmann, H.; Adams, H.D.; Anderegg, W.R.; Jansen, S.; Zeppel, M.J. Research frontiers in drought-induced
tree mortality: Crossing scales and disciplines. New Phytol. 2015,205, 965–969. [CrossRef] [PubMed]
Lichtenthaler, H.K. Vegetation stress: An introduction to the stress concept in plants. J. Plant Physiol.
148, 4–14. [CrossRef]
18. Dixon, H.H. Transpiration and the Ascent of Sap in Plants; Macmillan and Co.: London, UK, 1914.
19. Kozlowski, T.T.; Pallardy, S.G. Growth Control in Woody Plants; Elsevier: San Diego, CA, USA, 1997.
Steppe, K.; Sterck, F.; Deslauriers, A. Diel growth dynamics in tree stems: Linking anatomy and
ecophysiology. Trends Plant Sci. 2015,20, 335–343. [CrossRef] [PubMed]
Sevanto, S.; McDowell, N.G.; Dickman, L.T.; Pangle, R.; Pockman, W.T. How do trees die? A test of the
hydraulic failure and carbon starvation hypotheses. Plant Cell Environ.
,37, 153–161. [CrossRef]
22. McDowell, N.; Pockman, W.T.; Allen, C.D.; Breshears, D.D.; Cobb, N.; Kolb, T.; Plaut, J.; Sperry, J.; West, A.;
Williams, D.G. Mechanisms of plant survival and mortality during drought: Why do some plants survive
while others succumb to drought? New Phytol. 2008,178, 719–739. [CrossRef] [PubMed]
Ponomarenko, A.; Vincent, O.; Pietriga, A.; Cochard, H.; Badel, E.; Marmottant, P. Ultrasonic emissions reveal
individual cavitation bubbles in water-stressed wood. J. R. Soc. Interface 2014,11. [CrossRef] [PubMed]
24. Nobel, P.S. Physicochemical and Environmental Plant Physiology; Academic Press: San Diego, CA, USA, 1999.
25. Jackson, G.; Grace, J. Cavitation and water transport in trees. Endeavour 1994,18, 50–54. [CrossRef]
Rockwell, F.E.; Wheeler, J.K.; Holbrook, N.M. Cavitation and its discontents: Opportunities for resolving
current controversies. Plant Physiol. 2014,164, 1649–1660. [CrossRef] [PubMed]
Zimmermann, M. Xylem structure and the ascent of sap. Xylem Structure and the Ascent of Sap; Springer-Verlag:
Berlin, Germany, 1983.
Schenk, H.J.; Steppe, K.; Jansen, S. Nanobubbles: A new paradigm for air-seeding in xylem. Trends Plant Sci.
2015,20, 199–205. [CrossRef] [PubMed]
Choat, B.; Jansen, S.; Brodribb, T.J.; Cochard, H.; Delzon, S.; Bhaskar, R.; Bucci, S.J.; Feild, T.S.; Gleason, S.M.;
Hacke, U.G.; et al. Global convergence in the vulnerability of forests to drought. Nature
,491, 752–755.
[CrossRef] [PubMed]
Domec, J.-C.; Gartner, B.L. Cavitation and water storage capacity in bole xylem segments of mature and
young douglas-fir trees. Trees 2001,15, 204–214. [CrossRef]
Rosner, S. A new type of vulnerability curve: Is there truth in vine? Tree Physiol.
,35, 410–414. [CrossRef]
Cochard, H.; Badel, E.; Herbette, S.; Delzon, S.; Choat, B.; Jansen, S. Methods for measuring plant vulnerability
to cavitation: A critical review. J. Exp. Bot. 2013,64, 4779–4791. [CrossRef] [PubMed]
Vergeynst, L.L.; Dierick, M.; Bogaerts, J.A.; Cnudde, V.; Steppe, K. Cavitation: A blessing in disguise? New
method to establish vulnerability curves and assess hydraulic capacitance of woody tissues. Tree Physiol.
2015,35, 400–409. [CrossRef] [PubMed]
Appl. Sci. 2016,6, 71 12 of 15
Mayr, S.; Rosner, S. Cavitation in dehydrating xylem of picea abies: Energy properties of ultrasonic emissions
reflect tracheid dimensions. Tree Physiol. 2011,31, 59–67. [CrossRef] [PubMed]
Gullo, M.L.; Salleo, S. Different vulnerabilities of Quercus ilex L. To freeze-and summer drought-induced
xylem embolism: An ecological interpretation. Plant Cell Environ. 1993,16, 511–519. [CrossRef]
Fichot, R.; Brignolas, F.; Cochard, H.; Ceulemans, R. Vulnerability to drought-induced cavitation in poplars:
Synthesis and future opportunities. Plant Cell Environ. 2015,38, 1233–1251. [CrossRef] [PubMed]
37. Dixon, H.H.; Joly, J. On the ascent of sap. Philos. Trans. R. Soc. Lond. B 1895. [CrossRef]
Steudle, E. The cohesion-tension mechanism and the acquisition of water by plant roots. Annu. Rev. Plant Biol.
2001,52, 847–875. [CrossRef] [PubMed]
Jansen, S.; Schuldt, B.; Choat, B. Current controversies and challenges in applying plant hydraulic techniques.
New Phytol. 2015,205, 961–964. [CrossRef]
Wheeler, J.K.; Huggett, B.A.; Tofte, A.N.; Rockwell, F.E.; Holbrook, N.M. Cutting xylem under tension
or supersaturated with gas can generate plc and the appearance of rapid recovery from embolism.
Plant Cell Environ. 2013,36, 1938–1949. [CrossRef] [PubMed]
Cochard, H.; Delzon, S.; Badel, E. X-ray microtomography (micro-CT): A reference technology for
high-resolution quantification of xylem embolism in trees. Plant Cell Environ.
,38, 201–206. [CrossRef]
Milburn, J.; Johnson, R. The conduction of sap: II. Detection of vibrations produced by sap cavitation in
ricinus xylem. Planta 1966,69, 43–52. [CrossRef] [PubMed]
Tyree, M.T.; Dixon, M.A. Cavitation events in Thuja occidentalis L.? Utrasonic acoustic emissions from the
sapwood can be measured. Plant Physiol. 1983,72, 1094–1099. [CrossRef] [PubMed]
Temperley, H.; Chambers, L.G. The behaviour of water under hydrostatic tension: I. Proc. Phys. Soc.
58, 420. [CrossRef]
Milburn, J.A. Cavitation in Ricinus by acoustic detection: Induction in excised leaves by various factors.
Planta 1973,110, 253–265. [CrossRef] [PubMed]
Tyree, M.T.; Dixon, M.A.; Thompson, R.G. Ultrasonic acoustic emissions from the sapwood of
Thuja occidentalis measured inside a pressure bomb. Plant Physiol.
,74, 1046–1049. [CrossRef] [PubMed]
Tyree, M.T.; Dixon, M.A.; Tyree, E.L.; Johnson, R. Ultrasonic acoustic emissions from the sapwood of cedar
and hemlock an examination of three hypotheses regarding cavitations. Plant Physiol.
,75, 988–992.
[CrossRef] [PubMed]
Milburn, J.A. Cavitation studies on whole ricinus plants by acoustic detection. Planta
,112, 333–342.
[CrossRef] [PubMed]
Kikuta, S.B. Ultrasound acoustic emissions from bark samples differing in anatomical characteristics. Phyton
2003,43, 161–178.
Raschi, A.; Mugnozza, G.S.; Surace, R.; Valentini, R.; Vazzana, C. The use of ultrasound technique to monitor
freezing and thawing of water in plants. Agric. Ecosyst. Environ. 1989,27, 411–418. [CrossRef]
Mayr, S.; Sperry, J.S. Freeze-thaw-induced embolism in pinus contorta: Centrifuge experiments validate the
“thaw-expansion hypothesis” but conflict with ultrasonic emission data. New Phytol.
,185, 1016–1024.
[CrossRef] [PubMed]
Charrier, G.; Charra-Vaskou, K.; Kasuga, J.; Cochard, H.; Mayr, S.; Ameglio, T. Freeze-thaw stress: Effects
of temperature on hydraulic conductivity and ultrasonic activity in ten woody angiosperms. Plant Physiol.
2014,164, 992–998. [CrossRef] [PubMed]
Moli ´nski, W.; Raczkowski, J.; Poliszko, S.; Ranachowski, Z. Mechanism of acoustic emission in wood soaked
in water. Holzforschung 1991,45, 13–17. [CrossRef]
Rosner, S. Characteristics of acoustic emissions from dehydrat-ing wood related to shrinkage processes.
J. Acoustic Emission 2007,25, 149–157.
Gagliano, M.; Mancuso, S.; Robert, D. Towards understanding plant bioacoustics. Trends Plant Sci.
17, 323–325. [CrossRef] [PubMed]
Kikuta, S.; Gullo, M.; Nardini, A.; Richter, H.; Salleo, S. Ultrasound acoustic emissions from dehydrating
leaves of deciduous and evergreen trees. Plant Cell Environ. 1997,20, 1381–1390. [CrossRef]
Hacke, U.G.; Sperry, J.S.; Pittermann, J. Drought experience and cavitation resistance in six shrubs from the
great basin, utah. Basic Appl. Ecol. 2000,1, 31–41. [CrossRef]
Appl. Sci. 2016,6, 71 13 of 15
Sperry, J.S.; Tyree, M.T.; Donnelly, J.R. Vulnerability of xylem to embolism in a mangrove vs. an inland
species of rhizophoraceae. Physiol. Plant. 1988,74, 276–283. [CrossRef]
Cochard, H.; Tyree, M.T. Xylem dysfunction in quercus: Vessel sizes, tyloses, cavitation and seasonal changes
in embolism. Tree Physiol. 1990,6, 393–407. [CrossRef] [PubMed]
Tyree, M.; Sperry, J. Characterization and propagation of acoustic emission signals in woody plants: Towards
an improved acoustic emission counter. Plant Cell Environ. 1989,12, 371–382. [CrossRef]
Ritman, K.; Milburn, J. Acoustic emissions from plants: Ultrasonic and audible compared. J. Exp. Bot.
39, 1237–1248. [CrossRef]
Kasuga, J.; Charrier, G.; Uemura, M.; Améglio, T. Characteristics of ultrasonic acoustic emissions from walnut
branches during freeze-thaw-induced embolism formation. J. Exp. Bot.
,66, 1965–1975. [CrossRef]
Rosner, S.; Konnerth, J.; Plank, B.; Salaberger, D.; Hansmann, C. Radial shrinkage and ultrasound acoustic
emissions of fresh versus pre-dried norway spruce sapwood. Trees 2010,24, 931–940. [CrossRef] [PubMed]
Wolkerstorfer, S.V.; Rosner, S.; Hietz, P. An improved method and data analysis for ultrasound acoustic
emissions and xylem vulnerability in conifer wood. Physiol. Plant
,146, 184–191. [CrossRef] [PubMed]
Rosner, S. Waveform features of acoustic emission provide information about reversible and irreversible
processes during spruce sapwood drying. BioResources 2012,7, 1253–1263.
Rosner, S.; Klein, A.; Wimmer, R.; Karlsson, B. Extraction of features from ultrasound acoustic emissions:
A tool to assess the hydraulic vulnerability of norway spruce trunkwood? New Phytol.
,171, 105–116.
[CrossRef] [PubMed]
Mayr, S.; Schmid, P.; Laur, J.; Rosner, S.; Charra-Vaskou, K.; Dämon, B.; Hacke, U.G. Uptake of water via
branches helps timberline conifers refill embolized xylem in late winter. Plant Physiol.
,164, 1731–1740.
[CrossRef] [PubMed]
Laschimke, R.; Burger, M.; Vallen, H. Acoustic emission analysis and experiments with physical model
systems reveal a peculiar nature of the xylem tension. J. Plant Physiol.
,163, 996–1007. [CrossRef]
Tyree, M.T.; Fiscus, E.L.; Wullschleger, S.; Dixon, M. Detection of xylem cavitation in corn under field
conditions. Plant Physiol. 1986,82, 597–599. [CrossRef] [PubMed]
Ikeda, T.; Ohtsu, M. Detection of xylem cavitation in field-grown pine trees using the acoustic emission
technique. Ecol. Res. 1992,7, 391–395. [CrossRef]
Jackson, G.; Grace, J. Field measurements of xylem cavitation: Are acoustic emissions useful? J. Exp. Bot.
1996,47, 1643–1650. [CrossRef]
Perks, M.P.; Irvine, J.; Grace, J. Xylem acoustic signals from mature pinus sylvestris during an extended
drought. Ann. For. Sci. 2004,61, 1–8. [CrossRef]
Hölttä, T.; Vesala, T.; Nikinmaa, E.; Perämäki, M.; Siivola, E.; Mencuccini, M. Field measurements of ultrasonic
acoustic emissions and stem diameter variations. New insight into the relationship between xylem tensions
and embolism. Tree Physiol. 2005,25, 237–243. [CrossRef] [PubMed]
Quarles, S.L.; Association, W.D.K.; Association, W.D.K. Acoustic Emission Generated during Drying.
In Proceedings of the 41st Western Dry Kiln Association Meeting, Corvallis, OR, USA, 1990; p. 53.
Michlmayr, G.; Cohen, D.; Or, D. Sources and characteristics of acoustic emissions from mechanically stressed
geologic granular media—A review. Earth Sci. Rev. 2012,112, 97–114. [CrossRef]
Tyree, M.T.; Sperry, J.S. Vulnerability of xylem to cavitation and embolism. Annu. Rev. Plant Biol.
40, 19–36. [CrossRef]
Hacke, U.; Sauter, J. Xylem dysfunction during winter and recovery of hydraulic conductivity in
diffuse-porous and ring-porous trees. Oecologia 1996,105, 435–439. [CrossRef]
Nardini, A.; Tyree, M.T.; Salleo, S. Xylem cavitation in the leaf of prunus laurocerasusand its impact on leaf
hydraulics. Plant Physiol. 2001,125, 1700–1709. [CrossRef] [PubMed]
Salleo, S.; Gullo, L.; Raimondo, F.; Nardini, A. Vulnerability to cavitation of leaf minor veins: Any impact on
leaf gas exchange? Plant Cell Environ. 2001,24, 851–859. [CrossRef]
Vergeynst, L.L.; Sause, M.G.R.; Steppe, K. Clustering reveals cavitation-related acoustic emission signals
from dehydrating branches. Tree Physiol. 2016. in press.
Appl. Sci. 2016,6, 71 14 of 15
Aggelis, D.; Matikas, T.; Shiotani, T. Advanced acoustic techniques for health monitoring of concrete
structures. In The Song’s Handbook of Concrete Durability; Kim, S.H., Ann, K.Y., Eds.; Middleton Publishing Inc:
Middleton, WI, USA, 2010; pp. 331–378.
Choat, B.; Drayton, W.M.; Brodersen, C.; Matthews, M.A.; Shackel, K.A.; Wada, H.; Mcelrone, A.J.
Measurement of vulnerability to water stress-induced cavitation in grapevine: A comparison of four
techniques applied to a long-vesseled species. Plant Cell Environ.
,33, 1502–1512. [CrossRef] [PubMed]
Brodersen, C.R.; McElrone, A.J.; Choat, B.; Lee, E.F.; Shackel, K.A.; Matthews, M.A.
In vivo
visualizations of
drought-induced embolism spread in vitis vinifera. Plant Physiol.
,161, 1820–1829. [CrossRef] [PubMed]
Nolf, M.; Beikircher, B.; Rosner, S.; Nolf, A.; Mayr, S. Xylem cavitation resistance can be estimated based on
time-dependent rate of acoustic emissions. New Phytol. 2015,208, 625–632. [CrossRef] [PubMed]
Vergeynst, L.L.; Sause, M.G.; Hamstad, M.A.; Steppe, K. Deciphering acoustic emission signals in drought
stressed branches: The missing link between source and sensor. Front. Plant Sci.
,6. [CrossRef] [PubMed]
Lo, G.M.; Salleo, S. Three different methods for measuring xylem cavitation and embolism: A comparison.
Ann. Bot. 1991,67, 417–424.
Cochard, H. Vulnerability of several conifers to air embolism. Tree Physiol.
,11, 73–83. [CrossRef]
Niemz, P.; Emmler, R.; Pridöhl, E.; Fröhlich, J.; Lühmann, A. Vergleichende untersuchungen zur Anwendung
von piezoelektrischen und Schallemissionssignalen bei der trocknung von Holz. Holz als Roh und Werkstoff
1994,52, 162–168. [CrossRef]
Lee, S.-H.; Quarles, S.; Schniewind, A. Wood fracture, acoustic emission, and the drying process part 2.
Acoustic emission pattern recognition analysis. Wood Sci. Technol. 1996,30, 283–292. [CrossRef]
Beall, F. Overview of the use of ultrasonic technologies in research on wood properties. Wood Sci. Technol.
2002,36, 197–212. [CrossRef]
Kawamoto, S.; Williams, R.S. Acoustic Emission and Acousto-Ultrasonic Techniques for Wood and Wood-Based
Composites: A Review; US Department of Agriculture: Madison, WI, USA, 2002.
Beall, F.C.; Breiner, T.A.; Wang, J. Closed-loop control of lumber drying based on acoustic emission peak
amplitude. For. Prod. J. 2005,55, 167–174.
Johnson, D.M.; Meinzer, F.C.; Woodruff, D.R.; McCulloh, K.A. Leaf xylem embolism, detected acoustically
and by cryo-sem, corresponds to decreases in leaf hydraulic conductance in four evergreen species.
Plant Cell Environ. 2009,32, 828–836. [CrossRef] [PubMed]
Rosner, S.; Karlsson, B.; Konnerth, J.; Hansmann, C. Shrinkage processes in standard-size norway spruce
wood specimens with different vulnerability to cavitation. Tree Physiol.
,29, 1419–1431. [CrossRef]
Sause, M.G.R.; Gribov, A.; Unwin, A.R.; Horn, S. Pattern recognition approach to identify natural clusters of
acoustic emission signals. Pattern Recognit. Lett. 2012,33, 17–23. [CrossRef]
Zelenyak, A.M.; Hamstad, M.A.; Sause, M.G. Modeling of acoustic emission signal propagation in
waveguides. Sensors 2015,15, 11805–11822. [CrossRef] [PubMed]
Sause, M.; Horn, S. Simulation of acoustic emission in planar carbon fiber reinforced plastic specimens.
J. Nondestruct. Eval. 2010,29, 123–142. [CrossRef]
Haacs, R.; Blank, R.W. Acoustic emission from drought-stressed red pine (Pinus resinosa). J. Acoust. Emiss.
1990,9, 181–187.
Lewis, A.M. Two Mechanisms for the Initiation of Embolism in Tracheary Elements and Other Dead Plant Cells
under Water Stress; Harvard University: Cambridge, MA, USA, 1987.
Sandford, A.; Grace, J. The measurement and interpretation of ultrasound from woody stems. J. Exp. Bot.
1985,36, 298–311. [CrossRef]
Ritman, K.; Milburn, J. Monitoring of ultrasonic and audible emissions from plants with or without vessels.
J. Exp. Bot. 1991,42, 123–130. [CrossRef]
Kikuta, S.; Lo Gullo, M.; Kartusch, B.; Rosner, S.; Richter, H. Ultrasound Acoustic Emissions
from Conifer Sapwood Sections: Relationship between Number of Events Detected and Number of
Tracheids. In Proceedings of the IAWA International Symposium on Wood Sciences, Montpellier, France,
24–29 October 2004; p. 29.
Vergeynst, L.L. Investigation and Application of the Acoustic Emission Technique to Measure Drought-Induced
Cavitation in Woody Plants; Ghent University: Ghent, Belgium, 2015.
Appl. Sci. 2016,6, 71 15 of 15
Charrier, G.; Pramsohler, M.; Charra-Vaskou, K.; Saudreau, M.; Ameglio, T.; Neuner, G.; Mayr, S. Ultrasonic
emissions during ice nucleation and propagation in plant xylem. New Phytol.
,207, 570–578. [CrossRef]
Torres-Ruiz, J.M.; Jansen, S.; Choat, B.; McElrone, A.J.; Cochard, H.; Brodribb, T.J.; Badel, E.; Burlett, R.;
Bouche, P.S.; Brodersen, C.R.; et al. Direct X-ray microtomography observation confirms the induction of
embolism upon xylem cutting under tension. Plant Physiol. 2015,167, 40–43. [CrossRef] [PubMed]
Zweifel, R.; Zeugin, F. Ultrasonic acoustic emissions in drought-stressed trees—More than signals from
cavitation? New Phytol. 2008,179, 1070–1079. [CrossRef] [PubMed]
Steppe, K.; Zeugin, F.; Zweifel, R. Low-decibel ultrasonic acoustic emissions are temperature-induced and
probably have no biotic origin. New Phytol. 2009,183, 928–931. [CrossRef] [PubMed]
Brodersen, C.R.; McElrone, A.J. Maintenance of xylem network transport capacity: A review of embolism
repair in vascular plants. Front. Plant Sci. 2013,4. [CrossRef] [PubMed]
Zwieniecki, M.A.; Holbrook, N.M. Confronting maxwell
s demon: Biophysics of xylem embolism repair.
Trends Plant Sci. 2009,14, 530–534. [CrossRef] [PubMed]
McCulloh, K.A.; Meinzer, F.C. Further evidence that some plants can lose and regain hydraulic function
daily. Tree Physiol. 2015,35, 691–693. [CrossRef] [PubMed]
Meinzer, F.C.; McCulloh, K.A. Xylem recovery from drought-induced embolism: Where is the hydraulic
point of no return? Tree Physiol. 2013,33, 331–334. [CrossRef] [PubMed]
Zwieniecki, M.A.; Secchi, F. Threats to xylem hydraulic function of trees under “new climate normal”
conditions. Plant Cell Environ. 2015,38, 1713–1724. [CrossRef] [PubMed]
McElrone, A.; Brodersen, C.; Alsina, M.; Drayton, W.; Matthews, M.; Shackel, K.; Wada, H.; Zufferey, V.;
Choat, B. Centrifuge technique consistently overestimates vulnerability to water stress-induced cavitation
in grapevines as confirmed with high-resolution computed tomography. New Phytol.
,196, 661–665.
[CrossRef] [PubMed]
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... Seasonal changes in the response to freezing temperature has been related to the process of cold acclimation of living cells (Charrier et al., 2014a;Charrier et al., 2021b). In dehydrating branches from grapevine, three clusters of events have been characterized: high, middle and low-frequency events (Vergeynst et al., 2016). High frequency signals were assumed to be generated by capillary action of water and fast contraction of the bark, while low frequency signals were generated by micro-fractures (Vergeynst et al., 2016). ...
... In dehydrating branches from grapevine, three clusters of events have been characterized: high, middle and low-frequency events (Vergeynst et al., 2016). High frequency signals were assumed to be generated by capillary action of water and fast contraction of the bark, while low frequency signals were generated by micro-fractures (Vergeynst et al., 2016). Mid-frequency signals seem linked to hydraulic failure and likely generated by cavitation events. ...
... During the second phase AE 2 , since the shrinkage goes on and the branch becomes completely dry, other events than cavitation are likely to generate acoustic events such as cracks (De Roo et al., 2016) or cell wall shrinkage (Čunderlik et al., 1996). The relation with cellular damages is not straightforward although frost-induced cellular damages have been shown to induce acoustic events (Kasuga et al., 2015). ...
Acoustic emission analysis is promising to investigate the physiological events leading to drought-induced injuries and mortality. However, their nature and source are not fully understood making this technique difficult to use as a direct measure of the loss of xylem hydraulic conductance. Acoustic emissions were recorded during severe dehydration in lavender plants (Lavandula angustifolia) and compared to the dynamics of embolism development and cell damages. The timing and characteristics of acoustic signals from two independent recording systems were compared by principal component analysis. Changes in water potential, branch diameter, loss of hydraulic conductance and cellular damages were also measured to quantify drought-induced damages. Two distinct phases of acoustic emissions were observed during dehydration: the first one associated with a rapid loss of diameter and a significant increase in loss of xylem conductance (90%) and the second one with slower diameter changes and a significant increase in cellular damages. Based on Principal Component Analysis, a developed algorithm discriminated hydraulic-related acoustic signals from other sources, proposing a reconstruction of hydraulic vulnerability curves. Cellular damages preceded by hydraulic failure seem to lead to a lack of recovery. The second acoustic phase would allow to detect plant mortality.
... Anticipating and mitigating these climatic risks therefore requires a precise characterization of the exposure to the different climatic stresses (intensity, frequency, type), of the spatial and temporal vulnerability to these stresses, as well as the quantification of damage in situ e.g. at the edges of species distribution [2]. Although these types of damages are physically and physiologically different, including cellular, hydraulic or mechanical failure, they share the characteristic of generating ultrasonic acoustic emissions [3]. The detection of acoustic emissions is therefore a preferred technique for monitoring damage under highly constrained environmental conditions, while being minimally invasive. ...
... In different contexts, several sources of acoustic emissions have been identified during water stress and linked to cavitation events (formation of air bubbles in the sap under high tension) within the conducting tissues. Once the tension in the cell walls is released by the cavitation event, an elastic longitudinal waves propagates within a fluid medium (usually the cell walls), resulting in acoustic emission [3]. Acoustic emissions were recorded for the first time in plants in the audible range (below 20 kHz) during dehydration of Ricinus communis petioles [4]. ...
... Anticipating and mitigating these climatic risks therefore requires a precise characterization of the exposure to the different climatic stresses (intensity, frequency, type), of the spatial and temporal vulnerability to these stresses, as well as the quantification of damage in situ e.g. at the edges of species distribution [2]. Although these types of damages are physically and physiologically different, including cellular, hydraulic or mechanical failure, they share the characteristic of generating ultrasonic acoustic emissions [3]. The detection of acoustic emissions is therefore a preferred technique for monitoring damage under highly constrained environmental conditions, while being minimally invasive. ...
... In different contexts, several sources of acoustic emissions have been identified during water stress and linked to cavitation events (formation of air bubbles in the sap under high tension) within the conducting tissues. Once the tension in the cell walls is released by the cavitation event, an elastic longitudinal waves propagates within a fluid medium (usually the cell walls), resulting in acoustic emission [3]. Acoustic emissions were recorded for the first time in plants in the audible range (below 20 kHz) during dehydration of Ricinus communis petioles [4]. ...
... In parallel, xylem anatomical traits, vulnerability to drought-induced vessel embolism formation, and hydraulic capacitance were determined by means of the bench dehydration method. For this, simultaneous measurements of W xylem , embolism-related acoustic emissions (AEs; Nolf et al., 2015;De Roo et al., 2016; see methodological considerations below) and stem volumetric water content (VWC; Vergeynst et al., 2015a) were carried out. ...
The timing of abiotic stress elicitors on wood formation largely affects xylem traits that determine xylem efficiency and vulnerability. Nonetheless, seasonal variability of elevated CO2 (eCO2) effects on tree functioning under drought remains largely unknown. To address this knowledge-gap, one-year-old aspen (Populus tremula L.) trees were grown under ambient (±445 ppm) and elevated (±700 ppm) CO2 and exposed to an early (spring/summer 2019) or late (summer/autumn 2018) season drought event. Stomatal conductance and stem shrinkage were monitored in vivo as xylem water potential decreased. Additional trees were harvested for characterization of wood anatomical traits and to determine vulnerability and desorption curves via bench dehydration. The abundance of narrow vessels decreased under eCO2 only during the early season. At this time, xylem vulnerability to embolism formation and hydraulic capacitance during severe drought increased under eCO2. Contrastingly, stomatal closure was delayed during the late season, while hydraulic vulnerability and capacitance remained unaffected under eCO2. Independently of the CO2 treatment, elastic and inelastic water pools depleted simultaneously after 50% of complete stomatal closure. Our results suggest that the effect of eCO2 on drought physiology and wood traits are small and variable during the growing season and question a sequential capacitive water release from elastic and inelastic pools as drought proceeds.
... 18 Past research and the current state of the art about detection of acoustic emissions as a measure for drought-induced cavitation have been reviewed by De Roo et al. and what arises from this review is that vibrations have always been recorded by means of connection of the recording device directly to the plant; thus we cannot reveal the extent to which these vibrations could be sensed at a distance from the plant. 19 The possibility that plants emit airborne sounds had slightly been explored until an investigation by Khait and colleagues came to light in 2019: plants emit ultrasounds ranging between 20 and 150 kHz when exposed to drought and stress from cutting. The scientists found that tobacco (Nicotiana tabacum) and tomato (Solanum lycopersicum) plants, when stressed, produce remotely detectable ultrasonic sounds that could potentially be heard by other organisms (they could be detected from a distance ranging between 3-5 m by mammals and insects). ...
In a very recent book called Sensory Biology of Plants, published by renowned publisher Springer Nature, the authors stated that the scientific literature gathered so far regarding knowledge around the field of Plant Acoustics allows us to divert the focus from the question “whether plants perceive sound” toward the questions “how and why they are doing it” Some phenomena are well known: roots perceive the sound of flowing water and display a sound-mediated growth toward the water source, while the buzz pollination process allows plants to minimize the pollen lost and maximize which is collected by true pollinators. But plants are far more perceptive and responsive to their environment than we generally consider them to be, and they are communicating far more information than we realize if we only took all their signals (VOCs, sound, exudates, etc.) into a greater picture. Could Volatile Organic Compounds (VOCs) be involved in mediating more responses than we imagine? VOC synthesis and release is known to be elicited also by electrical signals caused by mechanical stimuli, touching and wounding being among these, serving as info-chemicals in the communication between plants (“eavesdropping”), and within the organs of the same plant, in order for it to get synchronized with its surroundings. This paper is an overview of the discoveries around plant perception with a focus on the link between mechanical stimuli, as sound vibrations are, and changes in plant physiology leading to VOC emission.
... To overcome this issue, some studies have attempted to link structure and function via the calibration of relatively rapid and integrative assessments of wood technological properties. These include wood density (Dalla-Salda et al., 2011), ultrasonic waves (De Roo et al., 2016), and Fourier transform infrared spectroscopy (Tsuchikawa and Kobori, 2015;Savi et al., 2019). However, all of these approaches fail to include variable wood cell structure in their analysis, as it is very difficult to link hydraulic characteristics to specific wood structural elements, such as annual rings or single conduits (but see e.g. ...
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Xylem hydraulic properties determine the ability of plants to efficiently and safely provide water to their leaves. These properties are key to understanding plant responses to environmental conditions and to evaluating their fate under a rapidly changing climate. However, their assessment is hindered by the challenges of quantifying basic hydraulic components such as bordered pits and tracheids. Here we use isometric scaling between tracheids and pits morphology to merge partial hydraulic models of tracheid’s component to upscale properties at the tree-ring level in conifers trees. Our new model output is first cross-validated with literature and then applied to cell anatomical measurements from Larix sibirica tree-rings formed under harsh conditions in southern Siberia to quantify the intra- and inter-annual variability in hydraulic properties. The model provides a means of assessing how different-sized tracheid’s components contribute to the hydraulic properties of the ring. Up-scaled results indicate that natural inter- and intra-ring anatomical variations have a substantial impact on the tree’s hydraulic properties. Our model facilitates the assessment of important xylem functional attributes because it only requires the more accessible measures of cross-sectional tracheid size. This approach, if applied to dated tree-rings, provides a novel way to investigate xylem structure-function relations across time and environmental conditions.
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Selection of high-yielding traits in cereal plants led to a continuous increase in productivity. However, less effort was made to select on adaptive traits, favorable in adverse and harsh environments. Under current climate change conditions and the knowledge that cereals are staple foods for people worldwide, it is highly important to shift focus to the selection of traits related to drought tolerance, and to evaluate new tools for efficient selection. Here, we explore the possibility to use vulnerability to drought-induced xylem embolism of wheat cultivars Excalibur and Hartog (Triticum aestivum L.), rye cultivar Duiker Max (Secale cereale L.), and triticale cultivars Dublet and US2014 (x Triticosecale Wittmack) as a proxy for their drought tolerance. Multiple techniques were combined to underpin this hypothesis. During bench-top dehydration experiments, acoustic emissions (AEs) produced by formation of air emboli were detected, and hydraulic capacitances quantified. By only looking at the AE50 values, one would classify wheat cultivar Excalibur as most tolerant and triticale cultivar Dublet as most vulnerable to drought-induced xylem embolism, though Dublet had significantly higher hydraulic capacitances, which are essential in terms of internal water storage to temporarily buffer or delay water shortage. In addition, xylem anatomical traits revealed that both cultivars have a contrasting trade-off between hydraulic safety and efficiency. This paper emphasizes the importance of including a cultivar’s hydraulic capacitance when evaluating its drought response and vulnerability to drought-induced xylem embolism, instead of relying on the AE50 as the one parameter.
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The formation of air emboli in the xylem during drought is one of the key processes leading to plant mortality due to loss in hydraulic conductivity, and strongly fuels the interest in quantifying vulnerability to cavitation. The acoustic emission (AE) technique can be used to measure hydraulic conductivity losses and construct vulnerability curves. For years, it has been believed that all the AE signals are produced by the formation of gas emboli in the xylem sap under tension. More recent experiments, however, demonstrate that gas emboli formation cannot explain all the signals detected during drought, suggesting that different sources of AE exist. This complicates the use of the AE technique to measure emboli formation in plants. We therefore analysed AE waveforms measured on branches of grapevine (Vitis viniferaL. 'Chardonnay') during bench dehydration with broadband sensors, and applied an automated clustering algorithm in order to find natural clusters of AE signals. We used AE features and AE activity patterns during consecutive dehydration phases to identify the different AE sources. Based on the frequency spectrum of the signals, we distinguished three different types of AE signals, of which the frequency cluster with high 100-200 kHz frequency content was strongly correlated with cavitation. Our results indicate that cavitation-related AE signals can be filtered from other AE sources, which presents a promising avenue into quantifying xylem embolism in plants in laboratory and field conditions.
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When drought occurs in plants, acoustic emission (AE) signals can be detected, but the actual causes of these signals are still unknown. By analyzing the waveforms of the measured signals, it should, however, be possible to trace the characteristics of the AE source and get information about the underlying physiological processes. A problem encountered during this analysis is that the waveform changes significantly from source to sensor and lack of knowledge on wave propagation impedes research progress made in this field. We used finite element modeling and the well-known pencil lead break source to investigate wave propagation in a branch. A cylindrical rod of polyvinyl chloride was first used to identify the theoretical propagation modes. Two wave propagation modes could be distinguished and we used the finite element model to interpret their behavior in terms of source position for both the PVC rod and a wooden rod. Both wave propagation modes were also identified in drying-induced signals from woody branches, and we used the obtained insights to provide recommendations for further AE research in plant science.
The new edition of Physicochemical and Environmental Plant Physiology uses elementary chemistry, physics, and mathematics to explain and develop key concepts in plant physiology. In fundamental ways, all physiological processes that occur in cells, tissues, organs, and organisms obey such relations. Topics include diffusion, membranes, water relations, ion transport, photochemistry, bioenergetics of energy conversion, photosynthesis, environmental influences on plant temperature, and gas exchange for leaves and whole plants. This new edition maintains the unparalleled commitment to clear presentation and improves upon the user friendliness of the previous versions. * All illustrations have been redrawn, many in two-color * New material includes: 14 new figures, 100 new references, 20 new equations and considerable new and revised text * Extensive cross-referencing with a simpler system for chapter sections and subsections * Easy-to-use format including major equations being presented at the beginning of each chapter, and calculations presented outside of the chapter text. Physicochemical and Environmental Plant Physiology, 3rd edition, establishes a new standard of excellence in the teaching and quantitative understanding of plant physiology.
After preliminary drying runs to establish the experimental procedure and acoustic emission (AE) parameters, several runs were made to determine a method of using feedback to control the drying process. The basis for using AE in drying control is that it directly measures stress development that leads to checking. In past studies, the approach has been to rely on changes in AE event rates to accelerate or decelerate the drying process. One of the major difficulties in using AE has been the very limited area from which AE could be sensed. The approach in this study, which has been previously reported, is the use of a metal sticker inserted into the load of lumber that acts as an accumulator of AE during the drying process without affecting airflow. Because of the multiple board contact, the AE is much greater in numbers than direct contact with a single transducer and more reflective of the response of the load. This paper reports on a new method of using automatic feedback control from a ratio of peak amplitudes to more accurately reflect the development of checking. Three runs were made with a difficult to dry hardwood (tanoak), of which the first two were made with conventional sample board controlled schedules to establish the AE control strategy. The final run was made solely under AE control, with the end result of a reduction in drying time to the fiber saturation point of about 40 percent with degrade no greater than the conventional runs.
Many theories have been formed to account for the ascent of sap in high trees, when root pressure is not acting. All have been found, on careful examination, unsatisfactory. Our attention was particularly directed to the problem as we were together in Bonn, in the Summer of 1893, when Professor E. Strasburger was kind enough to show us some of his experiments on the question, and since then we have, at intervals, occupied ourselves with some considerations as to the cause of the ascent of liquids in trees. It was not, however, till late last Spring that we had leisure to enter definitely on the research. We wish to acknowledge the kindness of Professor E. Perceval Wright in giving us the benefit of his advice on all occasions, and also the advantage we derived from Professor G. F. FitzGerald’s suggestive ideas.
The development of NDT (non-destructive testing) techniques used for the inspection of concrete structures is currently in high demand, because many existing structures have become aged and deteriorated in service. In order to formulate predictions on their stability and to estimate their safety, it is necessary to identify damage signals and to determine their causes. In this regard, the development and establishment of innovative and highly advanced non-destructive methods are required. Acoustic Emission (AE) and related NDE (non-destructive evaluation) techniques have been extensively used to determine crack detection and damage evaluation in concrete. With the move towards a more sustainable society, and the need to extend the long-term service life of infrastructure and aging and disastrous damage due to recent earthquakes, Acoustic Emission (AE) and Related Non-destructive Evaluation (NDE) Techniques in the Fracture Mechanics of Concrete: Fundamentals and Applications is a critical reference source for civil engineers, contractors working in construction and materials scientists working both in industry and academia.
Acoustic emissions are elastic waves accompanying damage processes and are therefore used for monitoring the health state of structures. Most of the traditional acoustic emission techniques use a trilateration approach requiring at least three sensors on a 2D domain in order to localize sources of acoustic emission events. In this paper, we present a new approach which requires only a single sensor to identify and localize the source of acoustic emissions in a finite plate. The method proposed makes use of the time reversal principle and the dispersive nature of the flexural wave mode in a suitable frequency band. The signal shape of the transverse velocity response contains information about the propagated paths of the incoming elastic waves. This information is made accessible by a numerical time reversal simulation. The effect of dispersion is reversed and the original shape of the flexural wave is restored at the origin of the acoustic emission. The time reversal process is analyzed first for an infinite Mindlin plate, then by a 3D FEM simulation which in combination results in a novel acoustic emission localization process. The process is experimentally verified for different aluminum plates for artificially generated acoustic emissions (Hsu-Nielsen source). Good and reliable localization was achieved for a homogeneous quadratic aluminum plate with only one measurement.