ECOLOGY AND BEHAVIOR
Colonization of the Biomass Energy Crop Miscanthus by the Three
Aphid Species, Aphis fabae, Myzus persicae, and Rhopalosiphum padi
Q. COULETTE,1 A. COUTY,1 P. LASUE,2 C. RAMBAUD,3
AND
A. AMELINE1,4
J. Econ. Entomol. 106(2): 683Ð689 (2013); DOI: http://dx.doi.org/10.1603/EC12147
ABSTRACT Miscanthus is a perennial C4-grass that has received much interest as a potential
biomass crop in Europe. However, little is known about the consequences of its introduction in terms
of impact on the local agroecosytem. In this context, laboratory experiments were conducted to
investigate the potential colonization of this new exotic plant species by three of the main aphid pest
species of common crops in Picardie, northern France. In host preference experiments, the two
polyphagous aphid species studied, Aphis fabae (Scop) and Myzus persicae (Sulzer), exhibited an
exclusive preference for their host plant, whereas the cereal specialist Rhopalosiphum padi (L.)
showed no preference between its host plant and miscanthus. When assessed by electrical penetration
graph technique, plant tissue probing activity by all three species always was characterized by pathway
phases including potential drops that are typically associated to the transmission of noncirculative
viruses. Phloem ingestion was observed in 5% of the polyphagous aphid individuals tested and in 20%
of the R. padi tested. Aphids kept in clip-cages on miscanthus had a low survival rate and were unable
to reproduce. These results demonstrate that miscanthus is not a suitable host for these three main
aphid pest species but could act as a potential host for some viruses transmitted in a noncirculative
manner and also in a circulative nonpropagative manner. The use of miscanthus as a barrier crop to
limit the ßow of aphid vectors and their phytoviruses is discussed.
KEY WORDS host plant suitability, Miscanthus sacchariflorus, Aphididae, electrical penetration
graph, phytovirus
The perennial C4-grasses of the genus Miscanthus originated from eastern Asia and comprise about a dozen
grass species among which Miscanthus sinensis Anderrs., Miscanthus sacchariflorus (Maxim.) Franch.,
and their triploid sterile hybrid Miscanthus x giganteus
attracted much attention as potential biomass crops
during the 1990s. These miscanthus grasses are particularly interesting because they are not only highyielding but also have a high nitrogen use efÞciency
linked to low nutritional requirements and low pesticide needs (Jorgensen 1997, Zub and BrancourtHulmel 2010, Gloyna et al. 2011, Thompson and Hoffmann 2011) in comparison to conventional crops.
Being strongly promoted by politicians and administrative bodies, miscanthus is cultivated in various European countries (United Kingdom, Germany, Denmark, the Netherlands, France) as well as in the
1 Unité EDYSAN (Ecologie et Dynamique des Systèmes Anthropisés), Laboratoire de Bio-Ecologie des Insectes Phytophages et Entomophages, Université Picardie Jules Verne, 33, rue Saint Leu,
F-80039 Amiens Cedex, France.
2 FREDON de Picardie, 19 rue Alexandre Dumas, 80096 AMIENS
Cedex 3.
3 UMR INRA 1281, Stress abiotiques et différenciation des végétaux
cultivés, Université Lille Nord de France, Lille1, Bâtiment SN2,
F-59650 Villeneuve dÕAscq Cedex, France.
4 Corresponding author: Drive. A. AMELINE, EA 4698, laboratoire
BIPE, Université Picardie Jules Verne, 33 Rue Saint Leu, FR-80000
Amiens Cedex, France (e-mail: [email protected]).
United States and Japan (Stampß et al. 2007, Gloyna et
al. 2011). In France, miscanthus has only recently been
planted (2006) for industrial purposes in addition to
experimental purposes. The introduction of such an
exotic biofuel crop may have important consequences
on the equilibrium of local agroecosystems. One nonnegligible risk is that bioenergy crops may act as reservoirs of serious pests and pathogens for other crops.
For instance, Gloyna et al. (2011) showed that miscanthus was suitable for the development of a European population of a coleopteran larva (Diabrotica
virgifera vigifera LeConte). Moreover, the barley yellow dwarf virus (family Luteoviridae, genus Luteovirus, BYDV) has been found in M. sacchariflorus and M.
sinensis grown in the United Kingdom from micropropagated plants imported from Germany (Christian
et al. 1994). In Picardie, a region located in the northern part of France, a Þeld survey of miscanthus crops
was conducted in 2011 (29 AprilÐ29 July). Yellow
water traps were placed on a pole at a height of 50 cm
above the canopy and 50 m from the border to attract
and collect insects ßying over the Þelds (according to
the protocol detailed in Marame et al. 2010). Collected
data showed that all the common aphid species occurring throughout northern France on many crop
plants were present. Among the 1,025 aphids trapped,
19.83% belonged to Myzus persicae (Sulzer) (green
peach aphid), 14.52% to Aphis fabae Scopoli (bean
0022-0493/13/0683Ð0689$04.00/0 䉷 2013 Entomological Society of America
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JOURNAL OF ECONOMIC ENTOMOLOGY
aphid), and 1.99% to Rhopalosiphum padi (L.) (bird
cherry-oat aphid) (Hemiptera: Sternorrhyncha: Aphididae) (data not shown). This result is consistent with
a previous study conducted in Herefordshire, southern England, by Semere and Slater (2007a), which
reports that Hemiptera found in miscanthus production areas were dominated by Aphididae.
M. persicae is a polyphagous species found on various families, including typical crops from Picardie,
northern France (e.g., potato, Solanum tuberosum L.;
beet, Beta vulgaris L.; and wheat, Triticum aestivum
L.). A. fabae is also polyphagous but with a predilection for beans and vetches. R. padi is a specialist and
attacks all cereals and pasture grasses (Blackman and
Eastop 2000). These aphids are major crop pests as
they cannot only cause direct damage by phloem feeding, resulting in signiÞcant impairment of plant growth
and yield, but, also, cause indirect damage by transmitting phytoviruses (Nault 1997). The spread of Phytoviruses is dependent on aphid behavior, including
locomotion and probing. Virus acquisition and inoculation depend not only on aphid interplant movement abilities (Irwin and Ruesink 1986) but also on
cell puncture occurrence within epidermal and mesophyll tissues (also called potential drops [pd]) for
viruses transmitted in a noncirculative manner (Powell et al. 1995, Martin et al. 1997) and on phloem sap
ingestion for viruses transmitted in a circulative manner (Gray and Banerjee 1999). Circulative viruses,
contrary to noncirculative viruses, are not lost after
aphid molting and invade the host hemolymph and
salivary glands. Noncirculative viruses do not cross the
gut membrane and remain attached to the aphid stylet
tips or foregut (Fereres and Moreno 2009).
The aim of this work was to study the suitability of
miscanthus as a new host plant for three aphid pest
species, M. persicae, A. fabae, and R. padi. In aphids,
host plant colonization can be divided into a behavioral sequence of several steps: 1) approach and landing on the plant; 2) leaf surface exploration and brief
testing probes to measure the suitability of the plant;
3) deep probes in plant tissues; 4) after assessment of
the phloem sap, host acceptance that leads to sustained sap ingestion and Þnally; 5) survival and reproduction (Niemeyer 1990, Powell et al. 2006).
Early steps of plant colonization were assessed by
using a dual choice bioassay to test the preferences of
each aphid species between their host plant and miscanthus. Aphid feeding behavior on miscanthus was
quantiÞed in electrical penetration graph (EPG) experiments. Finally, aphid survival and potential reproduction on miscanthus were measured using clip-cage
bioassays.
Materials and Methods
Insects. The M. persicae colony was established from
a single virginoparous female collected in 1999 in a
potato Þeld near Loos-en-Gohelle (France) and was
reared on potato plants (Solanum tuberosum ÔBintjeÕ).
Both the colonies of R. padi and A. fabae were initiated
in 2008 from a single apterous parthenogenetic female.
Vol. 106, no. 2
R. padi, provided by INRA-Le Rheu (Rennes,
France), and A. fabae, collected on eggplant (Solanum
melongena L.) in a greenhouse (Amiens, France).
They were reared respectively on wheat (Triticum
aestivum ÔMendelÕ) and on broad bean (Vicia faba L.
ÔMayaÕ). Each aphid clone was maintained on its host
plant in a ventilated Plexiglas cage in different growth
chambers under 20 ⫾ 1⬚C, 60 ⫾ 5% RH, and a photoperiod of 16:8 (L:D) h to induce parthenogenesis.
Bioassays were conducted with alate aphids either
newly emerged as young adults or that had been synchronized previously in ßight phase according to the
set-up described by Brunissen et al. (2009). All assays
were performed at 20 ⫾ 2⬚C.
Plantlets. Vitroplants of Miscanthus sacchariflorus
were obtained from nodes that were taken from
greenhouse-grown plants on shoots of 1Ð2 m in height.
For the induction stage, nodes were sterilized with
80-g/liter calcium hypochloride (60% active chlorine)
for 15 min and were then washed three times with
sterile distilled water. They then were dissected by
removing the leaves to discover the auxiliary shoots
followed by cutting 5 mm under the node and 5 mm
above the node. Aseptic explants were cultured in
petri boxes on agar-solidiÞed Murashige and Skoog
(1962) (MS) medium (mineral salts and vitamins)
with 50 mg/liter cysteine, 30 g/liter sucrose, and 5
mg/liter BAP, and adjusted to pH 5.5 before autoclaving at 115⬚C for 25 min (induction medium). The
explants were grown at 24⬚C under 16-h light per day
provided by cool-white ßuorescent lamps (40 ␮mol/
m2/s). Shoots obtained from this induction stage were
transferred to 240- by 24-mm glass tubes with transparent plastic covers for multiplication. The medium
consisted of MS salts and vitamins, 100 mg/liter myoinositol, 750 mg/liter MgCl2, 50 mg/liter cysteine-HCl,
30 g/liter sucrose, 3 mg/liter BAP, and 0.45 mg/liter
IAA (multiplication medium). Each glass tube contained 20 ml of multiplication medium supplemented
with 100 mg of perlite to support the regenerated
shoots. Every 6 wk, clusters were divided in single,
two, or three shoot-bundles and transferred to subculture. Single shoots coming from these clusters were
used for experiments. In vitro potato (Bintje) lines,
were obtained from germ fragments (2Ð3 cm) collected from a tuber, washed for 20 min with a 70 g/liter
calcium hypochloride (6% active chlorine), dried with
blotting paper, and deposited on a basal medium MS
(Murashige and Skoog 1962) supplemented with sucrose and agar for development. For micropropagation, explants were isolated on the MS medium in a
small glass vial (5 ml) placed in a sterile culture glass
tube (25 by 150 mm) in a growth chamber. Plantlets
of Vicia faba (variety Maya) and Triticum aestivum
(variety Mendel) were grown from seeds by using the
same protocol as the in vitro potato plantlets.
Plantlets were used for the experiments when they
reached ⬇8 ⫾ 1 cm height. All plantlets were grown
under 20 ⫾ 1⬚C, 60 ⫾ 5% RH, and a photoperiod of 16:8
(L:D) h.
Early Steps of Plantlet Colonization. An experiment
chamber made from Plexiglas (180 by 120 by 75 mm)
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COULETTE ET AL.: ABILITY OF APHIDS TO COLONIZE MISCANTHUS
685
and closed at one end with Þne screen mesh was
constructed, inside which plantlets (host plant versus
miscanthus) were set in small receptacles containing
water to avoid aphid plant colonization by walking
(Boquel et al. 2012).
The alate aphids, previously synchronized, were
individually placed on the ßoor of the device by using
a small paintbrush, at an equal distance from both
plantlets. Twenty-four hours after its introduction,
aphid location, on the host plant or on miscanthus, or
in the neutral zone (inner walls and ground of the
experimental chamber) was recorded. For each aphid
species, a total of 30 individuals were tested.
Aphid Feeding Behavior on Plantlets. The DCelectrical penetration graph (DC-EPG) technique
(Tjallingii 1978) was used to quantify the feeding
behavior of aphids. In each case one aphid and one
plant were connected in an electrical circuit and a gold
wire (20 ␮m in diameter, 2 cm in length) was attached
with conductive silver glue to the aphid dorsum. The
aphid then was connected to the DC-EPG ampliÞer
and carefully placed on the in vitro plantlets and a
second electrode was inserted into the soil to complete the electrical circuit. During daytime, for a period of 8 h, continuous recordings were performed.
Acquisition and analysis of the EPG waveforms were
carried out with PROBE 3.5 software (Tjallingii,
Wageningen University, The Netherlands) (Tjallingii
1988) and the EPG-Calc 4.9 software (Giordanengo
2009) was used to calculate parameters from the recorded EPG waveforms. For each aphid species, 20
replicates were performed.
Aphid Survival Bioassays. Newly emerged alate
aphids (⬍24-h old) were transferred individually onto
a leaf of a miscanthus plantlet and enclosed in a clipcage or placed onto a humidiÞed Þlter paper in a
petri-dish (5 cm in diameter) (negative control).
Aphids were monitored daily for 4 d. Dead aphids and
newly born nymphs were removed and counted each
day to calculate the mean daily percentage of surviving aphids and the mean daily fecundity. For each
treatment, 20 replicates were performed.
with a DunnÕs correction (Dunn 1964) of the alpha
threshold. The analysis was performed with the
Kruskal and WallisÕs utility, carried out by Georgin and
Gouet (2000) (http://Anastats.fr).
Aphid Survival Bioassays. At the beginning of the
experiment 20 aphids were placed individually in clipcages. Aphid survival was recorded every 24 h over a
period of 4 d (i.e., at Þve check-point dates) by calculating the ratio “number of dead aphids/20.” To
compare aphid survival on miscanthus and on moistened Þlter paper (negative control), the PearsonÕs
chi-square test of independence was performed on the
5 by 2 contingency tables obtained (Statistica version
5.5; StafSoft, Tulsa, OK). The same statistical test
(PearsonÕs chi-square test of independence) was also
used to make pairwise comparisons among the three
aphid species. To account for the problem of multiple
testing, the Benjamini and Hochberg (1995) procedure was used to control the false discovery rate and
determine adjusted P values.
Experimental Design and Statistical Analysis
Results
Early Steps of Plantlets Colonization. To measure
the preferences of the three aphid species for either
miscanthus or their host plant, the distributions of
aphids at the end of the experiment, either on their
host plant or on miscanthus, were compared with a
random distribution (1:1) using the PearsonÕs chisquare test.
Aphid Feeding Behavior on Plantlets. For each EPG
parameter, means and standard error of the means
were calculated using the data retrieved from the 20
aphids of each species tested. In addition, the number
of aphids exhibiting the corresponding behavioral
item also was counted. EPG parameters were compared between aphid species by using a KruskallÐ
Wallis one-way analysis of variance (H) followed by
nonparametric pairwise comparisons using the Siegel
and Castellan solution (Siegel and Castellan 1988)
Early Steps of Plantlets Colonization. Out of the 30
aphids individually tested, 80% of M. persicae, 67% of
A. fabae, and 56% of R. padi were found on at least one
of the two plants (miscanthus or host plant) at the end
of the experiment. The comparison of the actual distribution of the three aphid species on either plant
(host plant or miscanthus) to a random distribution
showed that M. persicae and A. fabae exhibited a
marked preference for their host plant (␹2 ⫽ 24, df ⫽
1, P ⬍ 0.001 and ␹2 ⫽ 20, df ⫽ 1, P ⬍ 0.001, respectively)
but that R. padi did not exhibit a preference between
miscanthus and its host plant (␹2 ⫽ 1.47, df ⫽ 1, P ⫽
0.23) (Fig. 1).
Aphid Feeding Behavior on Miscanthus in Vitro
Plantlets. KruskallÐWallis statistical analysis showed
that there was an aphid species effect on the following
parameters (Table 1): total duration of probing (H ⫽
Fig. 1. Aphid preference for miscanthus or its host plant.
The Þgure represents the percentage of aphids located at the
end of the 24-h dual choice bioassay on miscanthus and on
their host plant. For each aphid species (M. persicae, A. fabae,
R. padi), 30 individuals were tested. An asterisk (*) indicates
that the distribution of aphids was signiÞcantly different from
a 1:1 random distribution (P ⬍ 0.05; chi-square test).
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Table 1. Electrical penetration graph parameters (means ⴞ SEM and numbers of insects exhibiting different phases) calculated for
three aphid species during an 8-h monitoring session on miscanthus in vitro plantlets
Total duration of probing (min)
Number of insects showing probing
Mean Pathway phase (C) duration (min)
Number of insects showing Pathway phase (C)
Mean no. of potential drops
Mean phloem salivation phase (E1) duration (minutes)
Number of insects showing phloem salivation phases (E1)
Mean phloem sap ingestion (E2) duration (min)
Number of insects showing phloem sap ingestion (E2)
Total duration of phloem phases (E1 ⫹ E2) (min)
Number of insects showing phloem phases (E1 ⫹ E2)
Mean stylet derailment (F) duration (min)
Number of insects showing stylet derailment phases (F)
Mean xylem sap ingestion (G) duration (min)
Number of insects showing xylem sap ingestion phases (G)
Myzus persicae
(n ⫽ 20)
Aphis fabae
(n ⫽ 20)
Rhopalosiphum padi
(n ⫽ 20)
132.28 ⫾ 17.19b
20
2.61 ⫾ 0.36b
20
62.05 ⫾ 9.87
1.89 ⫾ 0.76a
8
10.72 ⫾ 10.72
1
4.28 ⫾ 1.93b
8
0.13 ⫾ 0.03a
20
18.12 ⫾ 5.55
19
257.28 ⫾ 25.20a
20
5.86 ⫾ 1.92a
20
86.50 ⫾ 13.54
20.37 ⫾ 12.63b
14
10.15 ⫾ 10.15
1
28.36 ⫾ 12.98a
14
0.23 ⫾ 0.12a
20
43.81 ⫾ 13.27
19
176.56 ⫾ 24.47a
20
4.87 ⫾ 0.83a
20
58.75 ⫾ 12.32
3.48 ⫾ 1.30ab
13
63.84 ⫾ 37.76
4
33.78 ⫾ 13.57a
13
0.07 ⫾ 0.01b
16
34.01 ⫾ 13.76
17
Different letters indicate signiÞcant differences between species for each parameter at P ⬍ 0.05.
12.38, P ⬍ 0.05), mean duration of a pathway phase
(H ⫽ 9.35, P ⬍ 0.05), mean duration of a phloem
salivation phase (H ⫽ 9.54, P ⬍ 0.05), and mean stylet
derailment phase (H ⫽ 12.10, P ⬍ 0.05). Multiple
comparisons showed that total probing duration was
signiÞcantly lower in M. persicae compared with the
two other species (P ⬍ 0.05). A. fabae and R. padi spent
about two times longer in realizing their pathway
phase (mean duration) than M. persicae (P ⬍ 0.05).
Within these pathway phases, the number of potential
drops was not signiÞcantly different (H ⫽ 3.25, P ⬎
0.05) between species. Only some individuals
achieved the phloem phases on miscanthus: the number of aphids attaining salivation phases (E1) ranged
between eight and 14 and the number of aphid realizing ingestion phases (E2) was extremely low (between one and four) which made statistical comparison impossible for this latter parameter. In terms of
total duration, phloem phase (E1 ⫹ E2) was signiÞcantly higher in A. fabae and R. padi compared with M.
persicae (P ⬍ 0.05). The mean duration of a salivation
phase was only signiÞcantly higher in A. fabae compared with M. persicae (P ⬍ 0.05). However, mean
duration of xylem ingestion phase was not signiÞcantly
different between aphid species. Finally, the mean
duration of stylet derailment phase was enhanced in
M. persicae and A. fabae compared with R. padi (P ⬍
0.05) (Table 1).
Aphid Performance. For each aphid species, survival on miscanthus was not signiÞcantly different
from survival on a humidiÞed Þlter paper (M. persicae:
␹2 ⫽ 3.95, dl ⫽ 4, P ⫽ 0.41; A. fabae: ␹2 ⫽ 0.90, dl ⫽ 4,
P ⫽ 0.92; R. padi: ␹2 ⫽ 3.17, dl ⫽ 4, P ⫽ 0.53) (Fig. 2).
At the end of the 4-d experiment, almost no aphid
survived, whatever the aphid species considered.
However, survival was less rapidly affected in M. persicae than in A. fabae (P ⫽ 0.001, alpha corrected by
BH ⫽ 0.012) (Fig. 2).
Reproduction on miscanthus was either null (M.
persicae) (zero nymphs recorded from the 20 aphid
tested) or anecdotic for R. padi (two nymphs re-
corded from the 20 aphids tested) and A. fabae (four
nymphs recorded from the 20 aphid tested).
Discussion
Strongly supported by the data collected in this
study, miscanthus is not a suitable host for three of the
most common aphid pests in northern France. However, some differences in the ability to colonize miscanthus appeared between the two polyphagous species and the cereal specialist species R. padi.
Miscanthus is not a suitable host plant for the three
aphid species. In dual choice tests miscanthus was
never preferred over the host plant. M. persicae and A.
fabae were not at all attracted by miscanthus from a
short distance and R. padi showed no preference.
These behaviors are likely to result from aphid responses to volatile organic compounds emitted by the
plants. M. persicae (Alla et al. 2003) and A. fabae
(Nottingham et al. 1991, Webster et al. 2008) have
been shown to be naturally attracted by volatiles emitted by their respective host plants Solanum tuberosum
and Vicia faba. R. padi was also shown to be attracted
by oat and wheat volatiles (Quiroz and Niemeyer
1998).
Probing behavior of the three aphid species on
miscanthus was altered drastically in comparison to
what is reported in previous studies when they were
tested on their host plant. Indeed, in our experiments,
aphids spent 50% or less of the recorded time in plant
tissue activity (versus at least 70% on their host plant)
and ⬍4% (versus between 20 and 64% on their host
plant) of the time realizing phloem phases (i.e., salivation and ingestion in phloem tissues) (Powell and
Hardie 2001, Slesak et al. 2001, Boquel et al. 2012). This
lack of phloem acceptance and phloem sustained ingestion shows that miscanthus is not a suitable host for
these three aphid species. Survival and above all reproduction on miscanthus were also weak, conÞrming
the nonsuitability of this plant. Huggett et al. (1999)
already showed that Miscanthus sinensis x giganteus
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COULETTE ET AL.: ABILITY OF APHIDS TO COLONIZE MISCANTHUS
Fig. 2. Survival (expressed in %) of three aphid species
(A: M. persicae, B: A. fabae, C: R. padi), on miscanthus in vitro
plantlets (black triangle) or on humidiÞed Þlter paper (negative control, black square). For each aphid species, 20 individuals were tested.
and Miscanthus sinensis were poor quality hosts for R.
padi as it was unable to complete its development on
seedlings of these two plants. They hypothesized that
it may be because of high levels of antifeedant chemicals commonly found in young grasses. For instance
Bernays and Chapman (1976) identiÞed 6-methoxybenzoxazolinone as being responsible for the lesser
fecundity of R. padi on young maize than on older
maize seedlings. In addition, it is worthy to note that,
although only few aphids ingested phloem (between
one and four individuals out of the three aphid species
tested realized an E2 phase), all tested aphids ingested
xylem and most of them exhibited stylet derailment.
This lack of phloem ingestion may be also regarded as
a fasting period resulting from antifeedant compounds
687
present in the phloem, beneÞtting in return the total
duration of xylem sap ingestion. Alate aphids in particular tend to ingest more xylem than apterous aphids
to rehydrate after their dispersal ßight (Spiller et al.
1990, Ramirez and Niemeyer 2000, Powell and Hardie
2001). Another study by Weibull (1990), comparing
the inßuence of leaf anatomy and plant storage carbohydrates on the acceptability of C3 and C4 plants to
R. padi concluded that it was the inability of this
species to penetrate the phloem tissue that rendered
C4 plants as unsuitable.
The aphid species tested cannot be considered as
miscanthus “colonizing aphids” but as “transient
aphids” (Irwin et al. 2007, Fereres and Moreno 2009)
because they do not stay and reproduce on this plant.
Thus, rather than exhibiting a reservoir status, Miscanthus can act as a potential refuge where aphids
occasionally land, rest, and hydrate on the plant. In an
epidemiological context, the feeding behavior analysis
demonstrates that all three aphid species, which
showed activity in the plant tissues and realized potential drops, are potential phytoviruses vectors. Indeed, potential drop (pd) activities are directly linked
to the transmission of viruses in a noncirculative manner (i.e., non persistent viruses) (Martin. et al. 1997).
In addition, when tested in the EPG set up, A. fabae
and M. persicae almost never ingested phloem and
when it did happen the duration of phloem ingestion
was ⬍20 min, which prevents the transmission of viruses in a circulative manner (Brault et al. 2010). R.
padi also quite rarely ingested phloem, but when it did,
phloem ingestion lasted for ⬇1 h making possible the
transmission in a circulative nonpropagative manner
of viruses such as the barley yellow dwarf virus
(BYDV). Christian et al. (1994) reported the presence
of BYDV in miscanthus Þelds grown in the United
Kingdom, and showed in laboratory experiments that
R. padi was able to inoculate at least one of the three
serotypes of BYDV tested to Miscanthus sinensis in
vitro plantlets. So, although R. padi cannot be regarded as a colonizing aphid, it may occasionally transmit viruses in a circulative nonpropagative manner.
Miscanthus could act as a barrier for aphids and
their associated phytoviruses. Several reports have
shown aphids and some of their associated viruses to
be manageable by barrier cropping (for review see
Hooks and Fereres 2006) and intercropping (for review see Lithourgidis et al. 2011). For instance, infestation of beans with black bean aphids was reduced
when beans intercropped with older and taller maize
plants (Ogenga-Latigo et al. 1993) or when intercropped with spring wheat or spring barley (Hansen
et al. 2008). The incidence of Bean Common Mosaic
Virus (family Potyviridae, genus Potyvirus, BCMV),
among other pathogens, also was reduced when beans
where grown in association with maize (Van Rheenen
et al. 1981).
Myzus persicae is a major virus vector and aphid pest
of several important crops in Picardie, northern
France. The use of the Poaceae winter wheat as a
barrier crop has proven to be an efÞcient method to
control its populations and limit the spread of Potato
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JOURNAL OF ECONOMIC ENTOMOLOGY
Virus Y (family Potyviridae, genus Potyvirus, PVY) in
potato Þelds (Difonzo et al. 1996). Poaceae may host
numerous other virus species that can be transmitted
by cereal aphids, such as R. padi, which is a vector of
luteoviruses, e.g., BYDV, and potyviruses, e.g., Maize
Dwarf Mozaic Virus (family Potyviridae, genus Potyvirus, MDMV). However, as R. padi does not stay and
reproduce on miscanthus the propagation of such phytoviruses via this aphid will be limited.
Several mechanisms can account for the efÞciency
of miscanthus as barrier crop. This plant being a tall
grass (⬎2m50), it can be easily used to form a physical
barrier preventing the alate aphid vectors access to
their host plant, as reported in various Þeld studies
(Hooks and Fereres 2006). Semere and Slater
(2007a,b) and Thompson and Hoffmann (2011) suggested that, as miscanthus harbors a low biodiversity,
large areas of this crop may also play a role of barrier
by preventing biological ßow. Moreover, miscanthus
planted as a border surrounding the crop of interest
could act as a sink for noncirculative viruses. Aphid
vectors would then lose their virulence while probing
the barrier crop, as it was suggested by Difonzo et al.
(1996).
Miscanthus planted as a barrier plant would consequently limit not only the reproduction of aphid vectors but also limit movements between crops, reducing
the risk of virus propensity, i.e., the probability of a
vector transmitting viruses under Þeld conditions (Irwin and Ruesink 1986).
Acknowledgments
This work was made possible by the Þnancial support of
Comité Nord Plant de Pomme de Terre through a scholarship
for Quentin Coulette. We thank the Conseil régional de
Picardie, D. Tagu (INRA, Rennes, France) for providing the
R. padi clones, and F. Lemoine from the Comité Nord Plants
de Pommes de Terre for providing potato in vitro plantlets
and tubers. Andrew Roots is thanked for its critical reading
of the manuscript especially concerning the English language.
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Received 10 April 2012; accepted 27 November 2012.