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DOI 10.1007/s00442-017-3862-z
Received: 31 October 2016 / Accepted: 31 March 2017 / Published online: 5 April 2017
© Springer-Verlag Berlin Heidelberg 2017
Abstract Because water is essential to life, organisms the abilities of roots to perceive and respond correctly to
have evolved a wide range of strategies to cope with water the surrounding soundscape. These findings highlight the
limitations, including actively searching for their preferred urgent need to better understand the ecological role of
moisture levels to avoid dehydration. Plants use moisture sound and the consequences of acoustic pollution for plant
gradients to direct their roots through the soil once a water as well as animal populations.
source is detected, but how they first detect the source is
unknown. We used the model plant Pisum sativum to inves- Keywords Foraging behavior · Hydrotropism · Moisture
tigate the mechanism by which roots sense and locate sensing · Bioacoustics · Directional root growth
water. We found that roots were able to locate a water
source by sensing the vibrations generated by water mov-
ing inside pipes, even in the absence of substrate moisture. Introduction
When both moisture and acoustic cues were available, roots
preferentially used moisture in the soil over acoustic vibra- All living organisms have basic needs and can only sur-
tions, suggesting that acoustic gradients enable roots to vive in environments where vital resources are available
broadly detect a water source at a distance, while moisture for those needs to be met. Water is one of those essential
gradients help them to reach their target more accurately. resources and its availability plays a critical role in terres-
Our results also showed that the presence of noise affected trial ecosystems where it strongly influences abundance,
spatial distribution and species interactions of a wide range
of plant and animal groups (Hawkins et al. 2003; McCluney
Communicated by Hermann Heilmeier. and Sabo 2009; McCluney et al. 2012; Ledger et al. 2013).
Because water is often limited and can be unevenly distrib-
Electronic supplementary material The online version of this uted across time and space, both animals and plants have
article (doi:10.1007/s00442-017-3862-z) contains supplementary
material, which is available to authorized users.
evolved a number of morphological and physiological traits
as well as behavioral strategies to cope with water scarcity
* Monica Gagliano and avoid dehydration. Ultimately when faced with water
monica.gagliano@uwa.edu.au scarcity, both animals and plants have two main options:
1 water-saving or water-seeking.
Centre for Evolutionary Biology, School of Animal Biology,
University of Western Australia, Crawley, WA 6009, Several animals and plants have evolved to cope with
Australia water scarcity through their impressive physiological
2
Australian Institute of Marine Science, Crawley, WA 6009, capacity to save previously acquired water (e.g., cam-
Australia els, Bekele et al. 2013; cacti, Niklas 1997). Taken to an
3
Oceans Institute, University of Western Australia, Crawley, extreme, bryophytes like the so-called ‘resurrection plants’
WA, Australia can remain in a dried state for years and then, rehydrate
4
School of Plant Biology, University of Western Australia, and return to a fully functional state within 48 h of rain
Crawley, WA 6009, Australia (Scott 2000). These and many other morphological and
13
152 Oecologia (2017) 184:151–160
physiological adaptations are clearly useful water-saving emanating from water moving through the soil or flowing
or desiccation-tolerance mechanisms; in general, however, through natural channels or human-made structures such
the most common strategy to economize on water involves as underground pipelines used in water supply networks
changes in behavior. By reducing rates of mobility during and sewer systems. As a matter of fact, the invasion of
the hottest hours of the day, animals are able to minimize sewer pipes by tree roots is an all too common and costly
water loss. In plants, changes in the orientation of leaves issue in municipalities around the world (United States
(i.e., paraheliotropism) to avoid light and reduce leaf tem- Environmental Protection Agency 1999; Östberg et al.
perature can also substantially increase water use efficiency 2012; Xie et al. 2014), yet no research has been directed
(Bielenberg et al. 2003). towards better understanding plant hydrotropic behavior
Despite the incredible water-saving abilities displayed in the context of bioacoustics. Whether acoustic cues are
by many species, the majority of animals and plants are really contributing to root orientation towards a water
not physiologically well-equipped to survive long periods source available in the soil remains to be seen, however.
of drought without searching for new water sources. Con- Therefore, in this study, we used a custom-designed
sequently, they have evolved water-seeking behaviors to Y-maze (cf. Fig. 1) to investigate how roots locate a water
deal with and actively search for more suitable (wetter) source, by experimentally testing how the behavior of
environments (animals, McCluney and Sabo 2009; plants, roots responds to different acoustic cues. The study con-
Kiss 2007; Cassab et al. 2013). To actively search and find sisted of a series of test scenarios (TS) where roots effec-
water, both plants and animals must rely on information of tively ‘chose’ between different treatments applied to
various kinds to make the most efficient directional deci- the ends of the Y-maze. Specifically, we experimentally
sions. Animals are known to use an array of multisensory investigated how roots choose the direction that correctly
orientation systems, which may include visual, auditory, leads them to water by testing their response to the sound
olfactory, magnetic, hygrotactic, anemotactic, polarotactic of water moving inside a pipe (Experiment 1) and then
and other cues (Bernáth et al. 2004; Russell et al. 2014). using playback experiments to test whether roots respond
Plants are also known to be exquisitely sensitive to a wide to sound recordings of water (Experiment 2). We also
range of environmental cues including geomagnetic fields used recordings to determine whether roots were able to
and moisture gradients, which they use to direct their roots discriminate between water and other sounds when these
through the soil once a water source is detected (Hart co-occur (Experiment 3).
1990). However, how plants sense and are able to move in
the direction of water in the absence of a moisture gradient
still need to be elucidated.
Investigations addressing this fundamental question on
the water-seeking abilities of roots have been extremely
limited (Cassab et al. 2013). The main reason for this
paucity is that hydrotropism is considered a “weak”
tropism relative to other tropisms such as phototropism
and gravitropism (for example, experiments have been
performed in space in order to mitigate the overwhelm-
ing effects of gravity and gravitropism; Wolverton and
Kiss 2009; Kiss et al. 2012). Nevertheless, this paucity is
perplexing given that this behavior is critical to the way
plants acquire water and hence survive. Here, we tack-
led this issue by examining the water-finding ability of
roots of pea seedlings (Pisum sativum), a model species
that has previously been used for assessing root hydro-
tropic response to moisture gradients (Jaffe et al. 1985).
Recent work has found that the roots of corn seedlings
are able to detect sound waves or vibrations and selec-
tively use them for orientation (Gagliano et al. 2012a). As
sound travels readily and far in dense environments such
as soil, a plant’s ability to detect vibrations may represent
Fig. 1 Schematic representation of the custom-designed experimen-
a very efficient, yet hitherto unexplored, way of captur- tal Y-maze, made of a PVC pipe filled with soil and attached to two
ing information from distant sound sources for orienta- tightly fitting small black plastic pots and two transparent rectangular
tion towards water. For example, roots may detect noise plastic trays at each lower end. Not to scale
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Oecologia (2017) 184:151–160 153
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154 Oecologia (2017) 184:151–160
Table 1 Treatments applied in each test scenario, together with the expected direction of each potential hypothesized effect in each scenario: acting towards (1) or against (−1) root growth in
Water contact Water presence Sound Water sound White noise Equipment presence Equipment on
When an effect is acting on both sides equally, such as equipment in TS8 and TS9, it is assumed to have no net influence towards or against root growth in the A treatment direction (0)
0
0
1
1
1
0
1
0
0
0
0
1
1
1
1
1
0
0
−1
0
0
0
1
0
0
0
0
1
1
0
0
0
1
1
1
0
1
1
1
0
0
1
0
1
Hypothesized effects
−1
1
1
0
0
0
0
0
0
sound (ZERO Hz) were played back using a small MP3 player and
speaker. Not to scale. a and b were assigned to left or right side at
random for each maze
Water (WTR)
Treatment B
Nothing
Nothing
Nothing
Nothing
Nothing
Nothing
PLAYING)
Treatment A
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Oecologia (2017) 184:151–160 155
Data analysis
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156 Oecologia (2017) 184:151–160
the model. All analyses were conducted in the R software where the sound of water was located (Fig. 4). In TS4
environment. For the sake of reproducibility, the R script where seedlings were exposed to computer-generated white
used for analysis is provided in the online supplementary noise, the observed frequency of seedlings directing their
material. root away from the sound source increased to 8/10 (Fig. 4).
The avoidance behavior observed in TS3 and TS4 was
further intensified in TS5 (Fig. 4). In this scenario, 9/10
seedlings directed their roots away from the location of
Results
the sound equipment that, albeit being turned on and play-
ing, broadcasted no actual sound. In TS6, when the sound
Experiment 1: root directional growth towards the
equipment was turned on but not playing [NOT PLAY-
sound of water
ING], 6/10 seedlings grew away from the equipment
(Fig. 4).
In the baseline TS1, an actual water gradient was produced
by the presence of 100 ml of water contained in the trans-
Experiment 3: root responses to co‑occurring sounds
parent plastic tray at the base of one side of the maze (see
Table 1; Fig. 2a). In this scenario, 8 out of 10 (8/10) seed-
In TS7, where both moisture and acoustic gradients were
lings directed their root to the side of the maze where the
available, 2/10 seedlings directed their roots towards the
water source was located (Fig. 4). Seedlings in the TS2
WTR-REC treatment side of the maze, 50% less than in
were equally successful (8/10) at locating the water source
TS3 where the recorded sound of water was the only treat-
even though these seedlings had no direct access to water
ment applied (Fig. 4). The number of seedlings that grew
but only to the live sound of water running inside a sealed
to the WTR side where the water was physically present
pipe (Fig. 4). The presence of circulating water in the pipe
in TS7 (8/10) was the same as observed in the TS1 sce-
had no effect on soil temperature (see Electronic Supple-
nario where the WTR was the only treatment applied. In
mentary Material for detailed results on temperature).
the TS8 scenario where WTR-REC and NOISE treatments
were co-occurring, the number of seedlings that directed
Experiment 2: root responses to recordings of natural their roots towards the side of the maze with the NOISE
and artificial sounds (6/10) was threefold more than in the TS4 scenario where
the NOISE treatment was applied alone (Fig. 4). However,
In TS3 where seedlings were played back the recorded the number of seedlings growing toward the WTR-REC
sound of running water, 6/10 of seedlings directed their in this TS8 scenario (4/10) was the same as that observed
roots away from, rather than towards, the side of the maze in the TS3 scenario where the WTR-REC was the only
Fig. 4 Number of seedlings
that directed their roots towards
the treatment side A of the
maze (white bars) across all test
scenarios (TS1–TS9; defined in
Table 1). The grey bars indicate
seedlings that did not choose
the treatment side. The red dot-
ted lines are intended to visually
distinguish the scenario specifi-
cally tested in each experiment.
See also Table S1 (color figure
online)
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Oecologia (2017) 184:151–160 157
treatment applied (Fig. 4). And lastly, in the TS9 scenario Table 2 The final simplified model explaining the observed results
where WTR-REC and ZERO Hz treatments were applied at in terms of various effects potentially interacting in the different test
scenarios, showing for each effect (term retained in the simplified
the same time, the proportion of seedlings growing towards final model), the estimated value for the model coefficient, the asso-
the WTR-REC (7/9) was almost twice that observed in TS3 ciated p value, and the associated estimated probability that the root
(4/10) when the treatment was applied alone (Fig. 4). The would grow towards the side of the maze where only that effect is
proportion of seedlings growing toward the ZERO Hz in acting, versus a side where no effect is acting
this scenario (2/9) was also greater than that observed in Final simplified model
the TS5 scenario (1/9) where the ZERO Hz was the only Effect/model term Coefficient estimate p value Probability
treatment applied (Fig. 4). estimate
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158 Oecologia (2017) 184:151–160
playback experiments likely affected seedlings’ responses of loud white noise can interfere with an individual’s abili-
to the test acoustic cues by interfering magnetically. Expo- ties to receive, respond and dispatch acoustic cues and sig-
sure of pea seedlings to very low magnetic fields is known nals. For example, Montgomerie and Weatherhead (1997)
to affect the ultrastructure of root cells by disrupting met- showed that foraging success of American robins was
abolic systems such as C a2+ homeostasis (Belyavskaya reduced when auditory cues were masked by white noise.
2001). Therefore, it is possible that the seedlings sensed Bats and squirrels are also affected by white noise and
the magnetic output of our sound equipment as an envi- allocate little foraging time to these environments (Schaub
ronmental condition to be avoided by moving away from et al. 2008). If plant’s abilities to perceive and respond to
its source, even when another sought after cue (e.g., sound the surrounding soundscape are also affected by noise, as
of water) is delivered by the same source. This finding is our findings suggest, what are the ecological ramifications
interesting because it demonstrates that seedlings have the of acoustic pollution on their natural communities? While
ability of “parsing” their sensory world into its components the urgent need to understand the consequences of altered
of different types and hence, resolve the influx of informa- acoustics on animal populations has been increasingly rec-
tion by prioritizing cues that support the overall most ben- ognized (Francis and Barber 2013), our findings clearly
eficial growth decision. indicate that the scope of our understanding on the matter
When the strong repulsive effect on root growth associ- needs to be extended to include plants.
ated with the presence of the operating sound equipment A better understanding of the acoustic ecology of plants
was experimentally standardized as in part of Experiment can also offer insights into new innovative practical appli-
3 (i.e., where individual peas were exposed to the magnetic cations. For example, our study clearly demonstrated that
disturbance from both sides of the maze) and accounted for plants are able to use sound to locate water inside sealed
in the integrated statistical model, there was some indica- pipes. We propose that some kind of adaptation to other
tion that the attractive effect of the recorded sound of water ubiquitous disturbances like those described in Gagli-
was stronger than that of white noise. This would agree ano et al. 2012b (i.e., the resonant acoustic-free oscilla-
with previous studies, which have demonstrated that plants tions known as the Earth’s “hum”) and Appel and Cocroft
respond to vibrations in a selective way (Gagliano et al. 2014 (i.e., feeding sounds of herbivores) which also act
2012a; Appel and Cocroft 2014). By showing that Arabi- via vibrations may have been the key to the root behavior
dopsis plants were able to discriminate between the vibra- described here. From an evolutionary perspective, the abil-
tions caused by insect feeding and those caused by wind or ity to respond to vibrations of various kinds including, for
insect song, for example, Appel and Cocroft (2014) dem- example, those produced by a running stream would have
onstrated that the ability of plants to detect and selectively been highly relevant to a broad range of species and ben-
respond to vibrations has an ecological function. In nature, eficial to their survival. We suggest that plants already had
this selectivity in regards to sounds or vibrations could the ability to use information of vibrational origin by the
explain how trees are able to detect different water sources time humans started building their first underground pipes,
and discriminate between them based on their longer-term which archeological evidence dates to the Minoan civili-
availability. For example, streamside trees like scrub oaks zation of Crete during the Bronze Age from 3650 to 1400
and box elders are known to preferentially tap into deeper BC (Wald 2016). Accordingly, plants have had millennia
soil layers for a more reliable source of water rather than to evolve this ability of responding to environmental vibra-
the shallow streams, which are more ephemeral (Dawson tions, including the sound of water moving through pipes.
and Ehleringer 1991). This could explain why roots are particularly good at find-
In our study, the difference between the sound of water ing and invading sewer pipe systems, even when their pipe-
and white noise was not great enough to be significant, lines are otherwise sealed and intact. Far from being trivial,
which may be because the ability of seedlings to grow in root invasion of sewer pipes has severe economic, environ-
the direction that leads to water by using the sound of water mental and social consequences and is a major problem
as a cue was contingent on the surrounding soundscape. for urban areas around the world. From 2006 to 2013, the
In both cited studies above (Gagliano et al. 2012a; Appel Water Corporation in Western Australia spent over AU$ 18
and Cocroft 2014), plants were exposed to a single cue at million on sewer pipe blockage repair, of which more than
any given time, thus eliminating the possibility for acoustic 65% were due to roots intrusion (Xie et al. 2014). In Ger-
interference. In this study, however, seedlings in Experi- many, the costs of root removal and associated pipe repairs
ment 3 were subjected to two acoustic cues at once. It is are estimated at EUR 28.4 million per year (Östberg et al.
possible that the ability of seedlings to detect the recorded 2012). And boasting one of the largest and most complex
sound of water was reduced because the cue was obscured wastewater systems in the world approaching 7000 km of
by the white noise (i.e., masking effect). Experimental stud- sewer lines, the city of Los Angeles in the year 1997 spent
ies in animal systems have demonstrated that the presence about US$ 5000 per km to remove roots from its pipes
13
Oecologia (2017) 184:151–160 159
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Heilmeier and two anonymous reviewers for valuable comments on London
the manuscript. This work was supported by Research Fellowships Hawkins BA et al (2003) Energy, water, and broad-scale geographic
from the University of Western Australia and the Australian Research patterns of species richness. Ecology 84:3105–3117
Council (ARC grant n. DE130100018) to MG*. Jaffe MJ, Takahashi H, Biro RL (1985) A pea mutant for the study of
hydrotropism in roots. Science 230:445–447
Author contribution statement MG* conceived and designed the Kiss JZ (2007) Where’s the water? Hydrotropism in plants. Proc Natl
experiments. MG* and MG performed the experiments and collected Acad Sci USA 104:4247–4248. doi:10.1073/pnas.0700846104
data MG*, MD and MR analyzed and interpreted the data. MG* and Kiss JZ, Millar KDL, Edelmann RE (2012) Phototropism of Arabi-
MR drafted the paper. All authors edited and critically revised the dopsis thaliana in microgravity and fractional gravity on the
final version, and approved its publication. international space station. Planta 236:635–645. doi:10.1007/
s00425-012-1633-y
Compliance with ethical standards Ledger ME, Brown LE, Edwards KE, Milner AM, Woodward G
(2013) Drought alters the structure and functioning of complex
Conflict of interest The authors declare no competing interests. food webs. Nature Clim Change 3:223–227
Maffei ME (2015) Magnetic field effects on plant growth, devel-
opment, and evolution. Front Plant Sci 5:445. doi:10.3389/
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