Bezooijen, J., van

Boff, M.I.C.

Sabelis, M.W.

Smits, P.H.

Sommen, A.T.C., van der

Tol, R.W.H.M., van

English

Name not available

Plants protect their roots by alerting the enemies of grubs

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Type article
Title Plants protect their roots by alerting the enemies of grubs
Author(s) R.W.H.M. van Tol, A.T.C. van der Sommen, M.I.C. Boff, J. van Bezooijen,
M.W. Sabelis, P.H. Smits
Faculty FNWI: Institute for Biodiversity and Ecosystem Dynamics (IBED), FNWI:
Institute for Biodiversity and Ecosystem Dynamics (IBED)
Year 2001
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  http://hdl.handle.net/11245/1.183852
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I D E A
Plants protect their roots by alerting
the enemies of grubs
Rob W.H.M. van Tol,1 Anton
T.C. van der Sommen,2 Mari
I.C. Boff,3,4 Jan van Bezooijen,2
Maurice W. Sabelis5 and
Peter H. Smits3
1Applied Plant Research,
Nursery Stock Research Unit,
P.O. Box 118, 2770 AC Boskoop,
The Netherlands
E-mail:
r.w.h.m.van.tol@ppo.dlo.nl
2Wageningen-UR, Department
of Nematology, P.O. Box 8123,
6700 ES Wageningen,
The Netherlands
3Plant Research International,
P.O. Box 16, 6700 AA
Wageningen, The Netherlands
4Current address: Universidade
do Estado de Santa Catarina –
Centro de Cieˆncias
Agroveterina´rias, Av. Luis de
Camo~es, 2090, 88520-000, Lages,
Santa Catarina, Brazil
5Institute for Biodiversity and
Ecosystem Dynamics, P.O. Box
94084, 1090 GB Amsterdam,
The Netherlands
Abstract
Plant roots in the soil are under attack from many soil organisms. Although many
ecologists are aware of the presence and importance of natural enemies in the soil that
protect the plants from herbivores, the existence and nature of tritrophic interactions are
poorly understood. So far, attention has focused on how plants protect their above-
ground parts against herbivorous arthropods, either directly or indirectly (i.e. by getting
help from the herbivore’s enemies). This article is the first in showing that indirect plant
defences also operate underground. We show that the roots of a coniferous plant (Thuja
occidentalis) release chemicals upon attack by weevil larvae (Otiorhynchus sulcatus) and that
these chemicals thereby attract parasitic nematodes (Heterorhabditis megidis).
Keywords
Synomones, semiochemicals, roots, herbivory, entomopathogenic nematodes, vine weevil,
Otiorhynchus sulcatus, Heterorhabditis megidis, Thuja occidentalis.
Ecology Letters (2001) 4: 292–294
Plants protect themselves against insect herbivores, either
directly, e.g. using toxins, or indirectly by promoting the
effectiveness of the herbivore’s enemies. Indirect plant
defences may help explain why insect herbivores are
generally predator-controlled and therefore why ‘‘the World
is green’’ (Sabelis et al. 1999). The evidence for this mode
of defence comes from studies on above-ground plant
parts (stems and leaves) providing shelter, food or SOS-
signals to the herbivore’s enemies (Dicke et al. 1990;
Turlings et al. 1995; Takabayashi & Dicke 1996; Sabelis
et al. 1999). However, roots are a vital, yet vulnerable part
of the plant and the role of soil-dwelling natural enemies in
suppressing populations of root-feeding insects in natural
ecosystems has been shown (Strong et al. 1996, 1999).
Thus, one may wonder whether plants actively protect their
roots by attracting these natural enemies. We tested this
hypothesis by studying the interaction between conifer
roots (Thuja occidentalis), root-feeding vine weevil larvae
(Otiorhynchus sulcatus) and entomopathogenic nematodes
(Heterorhabditis megidis). Olfactometry revealed that roots
damaged by weevil larvae release exudates that attract
parasitic nematodes. These chemicals therefore function as
an SOS, signalling the presence of herbivores to their
natural enemies.
Little is known of the searching behaviour of entomo-
pathogenic nematodes in the soil, let alone the role of
chemical communication. Entomopathogenic nematodes
are known to be attracted to undamaged plant roots (Bird &
Bird 1986; Choo et al. 1989; Lei et al. 1992; Wang & Gaugler
1998), to their insect hosts (Schmidt & All 1978; Gaugler
et al. 1980; Lei et al. 1992; Lewis et al. 1993) and the
associated cues (e.g. CO2 and faeces) (Schmidt & All 1978;
Ecology Letters, (2001) 4: 292–294
Ó2001 Blackwell Science Ltd/CNRS
Gaugler et al. 1980; Grewal et al. 1993; Lewis et al. 1993), but
only one study (Wang & Gaugler 1998) suggests that cues
from intact and wounded grass roots influence host finding
ability of the nematodes. The possibility that plant roots
release SOS signals upon being eaten by insects has been
largely ignored, even though there is a wealth of evidence
for such herbivore-induced signals from leaves (Dicke et al.
1990; Turlings et al. 1995; Takabayashi & Dicke 1996;
Sabelis et al. 1999). We hypothesized that this is also
possible in the soil environment where plant roots are under
insect attack and would be able to maintain their function by
the aid of the herbivore’s natural enemies.
To test the olfactory behaviour of the nematodes we used
a Y-shaped tube, comprising five short tubes (two per arm –
7 cm long, 3.5 cm diam. – and one at the base – 5.5 cm
long, 4.5 cm diam.), each filled with silver-sand (moisture
content 10% w/w) and closed using nylon gauze to isolate
insects and roots, yet allow nematodes to pass through (Boff
et al. 2001). The short tube on top of each Y-arm was
disconnected and incubated for four days with one of the
following odour-emitting objects in silver-sand: six weevil
larvae, undamaged, mechanically damaged (cutting 10% of
root tips) or weevil-damaged (with or without six larvae)
roots of one intact thuja plant with its above-ground parts
sealed off from the tube. After incubation, the tube parts
were connected again on top of the Y-arms and the Y-tube
was positioned vertically, arms up, by clamping it to a stand
in a climate room (15 °C; L : D  16 : 8 h). One day
thereafter, nematodes (900 in 0.5 mL tap water) were
released in a pipette inserted up the middle of the base tube,
i.e. 16 cm from the top of the Y tube. One day later, their
numbers in either arm were counted after sand-extraction
with an independently estimated 90–95% efficiency (Boff
et al. 2001). Each experiment was replicated at least four
times with fresh odour sources, fresh sand and new batches
of nematodes. For the choice tests between weevil-damaged
and mechanically damaged or undamaged thuja roots, we
first rinsed the roots with tap water, placed them in water
for one day and finally replanted the thujas in fresh silver-
sand in the Y-tubes. Thus, odours from insects and their
faeces are absent during these tests and the observed
response of the nematodes must be attributed to odours
released from the plant.
We found that nematodes were more attracted to weevil
larvae alone and to undamaged Thuja roots alone when clean
air was the alternative, and that they were more attracted to
weevil-infested roots than to larvae alone or roots alone
(Table 1). The nematodes also moved to odours from
weevil-damaged roots, freed of weevil larvae prior to the
experiment, instead of to odours from undamaged or
mechanically damaged roots (Table 1).
The attractive plant odour probably does not travel by air
to the nematode’s sensory organs. GC-MS analysis of
volatile chemicals (using Tenax-TA adsorbents-tubes and a
thermodesorption cold trap unit) did not reveal differences
between treatments. It is probably that the chemicals
released from the plant enter the water in the silver sand
and diffuse into the Y-tube. There, the response of the
parasitic nematodes becomes manifest in a matter of hours
after release, as shown by independent olfactometer
experiments (three replicates per time treatment). A
proportion of the nematodes had entered the Thuja Y-arm
within 2 h but, even after 6 h, none of them had reached the
top tube with the control source, whereas many were already
in the top tube with the odour source under investigation.
(e.g. in the case of odour from undamaged thuja roots
against clean air: 5% after 2 h, 6% after 4 h, 8% after 6 h). It
can therefore be safely concluded that the nematodes are
attracted to the odour source, rather than arrested after
random movement.
These results demonstrate herbivory-induced release of
SOS-signals from plant roots attracting the entomopatho-
Table 1 Olfactory response of entomopathogenic nematodes
% Nematodes
Odour source (+) Odour source ()) to (+)# Results
Control Control 50.7 49, 54, 46, 54, 54, 53, 50, 53
Vine weevil larvae Control 72.5* 63, 73, 82, 67, 91, 66
Thuja roots Control 88.7* 90, 87, 84, 99, 69, 87, 91
Thuja roots + vine weevil larvae Vine weevil larvae 80.6* 78, 87, 80, 80, 81, 80
Thuja roots + vine weevil larvae Thuja roots 82.6* 94, 74, 78, 75, 81, 85
Weevil-damaged Thuja roots Mechanically-damaged Thuja roots 79.7* 71, 80, 84, 82
Weevil-damaged Thuja roots Undamaged Thuja roots 73.1* 73, 68, 82, 74
Regression analysis was performed on logit transformed data with the Genstat 5 computer program. Values followed by an asterisk (*)
indicate statistically significant preferences for a particular odour at the 5% level.
#Percentage nematodes to (+) are predicted values from the regression analysis and are thus not presenting the exact average values of the
range results shown in the table.
Protection of plant roots 293
Ó2001 Blackwell Science Ltd/CNRS
genic nematodes in the direction of the odour source.
Whether the attractants released in response to weevil
damage are de novo synthesized, produced in larger amounts
or in different relative amounts needs further study. Short-
range attraction to fluids exuded from plant roots has been
shown earlier (Bird & Bird 1986; Choo et al. 1989; Lei et al.
1992), but long-range attraction by means of SOS signalling
of plants is an entirely new result. This method of host
habitat location will be vital to the searching nematode
larvae because they are exclusively designed to search, not to
feed, they have limited energy reserves and experience host
scarcity in the soil. A mutualistic interaction between plants
and entomopathogens in the soil is therefore to be expected
and this may well provide new insight into how plants
protect their roots against grubs and how biological control
of soil pests may be achieved (Elliot et al. 2000).
A C K N O W L E D G E M E N T S
This work is supported by the Dutch programme
LNV-DWK 338 for insect pest control.
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B I O S K E T C H
Rob van Tol studies plant–weevil–parasite interactions in the
soil and the implications for pest control strategies in different
agricultural systems. He is currently working on the identifi-
cation of attractants of the vine weevil and development of a
monitoring system for this pest in ornamentals.
Editor, M. Hochberg
Manuscript received 29 November 2000
First decision made 13 December 2000
Second decision made 6 February 2001
Manuscript accepted 28 March 2001
294 R.W.H.M. van Tol et al.
Ó2001 Blackwell Science Ltd/CNRS


Plants protect their roots by alerting the enemies of grubs

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