Plant Pathology (2017) 66, 325–335 Doi: 10.1111/ppa.

12561

New aphid vectors and efficiency of transmission of Potato

virus A and strains of Potato virus Y in the UK

A. Fox*, L. E. Collins, R. Macarthur, L. F. Blackburn and P. Northing

Fera, Sand Hutton, York YO41 1LZ, UK

The aphid-transmitted viruses Potato virus Y (PVY) and Potato virus A (PVA) commonly affect seed potatoes in the UK.
The transmission efficiency for aphid species is used to calculate a potential transmission risk and is expressed as a rela-
tive efficiency factor (REF). These REFs have not previously been calculated for UK strains of viruses or aphid clones.
Using a previously published method, REFs have been calculated for the aphid species and viruses commonly occurring
in UK potatoes. The efficiency of transmission of Myzus persicae is nominally set to a REF of 1 and REFs for other spe-
cies are calculated relative to this. These data represent the first set of REFs calculated for PVA transmission. Macrosi-
phum euphorbiae (REF 0.91) was almost as efficient as M. persicae at PVA transmission. The data were further analysed
to compare transmission rates of PVY and PVA using a binomial (logit) generalized mixed model to take into account
the potential influence of variation in virus titre between leaves. This approach found that there is little variation between
the efficiency of transmission between clones of each aphid species or between strains within a virus species. This is a first
report that Aphis fabae, Metopolophium dirhodum, Sitobion avenae, Acyrthosiphon pisum and Cavariella aegopodii have
the ability to vector PVA. This study also represents a first report that C. aegopodii has the ability to vector PVY and
confirms the potential of S. avenae, A. fabae, M. euphorbiae and Rhopalosiphum padi as important PVY vectors.

Keywords: aphid, transmission, vector, virus

PVY infection range from 15% to 30% for PVYN (Van

Introduction
Potatoes (Solanum tuberosum) are a globally important
food crop. The potato industry in the UK produces 5.6
million tonnes of potatoes per year, including almost
17 000 ha of certified seed potatoes (AHDB, 2015).
Excessive virus levels in seed potato crops are the major
reason for seed crops being downgraded or failed within
the England and Wales Seed Potato Certification
Scheme (Fera, 2013). The most commonly intercepted
viruses in UK growing crop inspections are the non-
persistent, aphid-transmitted, mosaic-inducing viruses:
strains of Potato virus Y (PVY, genus Potyvirus, family
Potyviridae) and Potato virus A (PVA, genus Potyvirus,
family Potyviridae). PVY strains are known to have a
global distribution (Singh et al., 2008), and whilst PVA
is also thought to have a global distribution, with occa-
sional exceptions (Pickup et al., 2009; Were et al.,
2013), specific surveillance for this virus is rarely
reported. The effects of these viruses in the plant range
from symptomless infections through to severe mosaics,
although the former may be a consequence of subtle
symptom development during the season of infection.
Severity of symptoms is also dependent upon virus strain
and the cultivar affected. Assessments of yield loss from
*E-mail: adrian.fox@fera.co.uk
Published online 1 July 2016
der Zaag, 1987) to as high as 70% for mixed infections
with Potato leaf roll virus (Beemster & De Bokx, 1987).
Other studies suggest a more linear relationship between
percentage PVY content and percentage yield loss in a field
situation (Nolte et al., 2004). PVY strains may also lead
to the development of potato tuber necrotic ring disease in
susceptible cultivars (LeRomancer & Kerlan, 1994). Addi-
tionally, infections with PVY strains, PVA and Potato
virus V have been associated with an increase in growth
cracking of tubers (Carnegie & McCreath, 2010).
Mechanical transmission of PVY, such as transmission
on knives through cutting infected tubers or on farm
machinery, has been shown to be of no practical signifi-
cance in the epidemiology of this virus (Sturz et al.,
2000; Coutts & Jones, 2015). Natural spread of PVY
can, therefore, be attributed to aphids. There are differ-
ences in the ability of each aphid species to retain and
transmit nonpersistent viruses (Van Hoof, 1980). Previ-
ous studies have demonstrated that at least 25 aphid spe-
cies are capable of vectoring PVY, with Myzus persicae
(the peach–potato aphid) recognized as the most efficient
vector (Harrington et al., 1986; De Bokx & Piron, 1990;
Basky & Alm asi, 2005; Verbeek et al., 2010; Boquel
et al., 2011; Mello et al., 2011). However, as the
methodology for quantifying transmission differed in
each study, the relative efficiency factors (REFs) gener-
ated are not directly comparable. Although M. persicae
is recognized as being the most efficient transmitter of
PVY, in some countries this species is of low relative

ª 2016 British Society for Plant Pathology 325

326 A. Fox et al.
abundance compared to other aphid species (Sigvald,
1990; Pickup et al., 2010). The importance of migrating
and transitory aphids in epidemics of PVY has long been
recognized: Broadbent (1948) reported that noncoloniz-
ing transitory aphids may play a role in the transmission
of nonpersistent aphid-transmitted potato viruses. In
some countries, noncolonizing (non-potato) aphids are
recognized as having a major role in driving PVY and
PVA transmission (Sigvald, 1987; Pickup et al., 2009,
2010; Steinger et al., 2015). Laboratory studies have
tended to use apterae (non-winged aphids; Basky &
Almasi, 2005; Verbeek et al., 2010; Boquel et al., 2011;
Mello et al., 2011). However, there have also been lim-
ited studies on the transmission rates by alate (winged)
aphids that have been live-trapped (Harrington et al.,
1986; De Bokx & Piron, 1990), but these findings are
inevitably skewed by the populations caught during the
study. Due to the practical difficulties of working with
the alate form, laboratory-based studies on these forms
have focused on a single aphid species (Boiteau et al.,
1998). Although individual studies do not give complete
lists of vectors or PVY strains, collated data have been
used to formulate a comprehensive list of PVY REFs
where M. persicae is given a nominal value of 1, and the
transmission efficiency of all other species can be calcu-
lated relative to that figure (Sigvald, 1986; De Bokx &
Piron, 1990). A composite list of these REFs has
subsequently been used as part of aphid monitoring
programmes for virus risk management in the Fera/
AHDB-Potatoes Aphid Monitoring Programme (Nor-
thing et al., 2004). Verbeek et al. (2010) investigated
recently emerged strains of PVY in the Netherlands, such
as PVYNTN, using a standardized method. This study
observed variability amongst different clones of the same
aphid and with different strains of PVY in the same
clone. Other investigations into the relative ability of
aphids to transmit a range of potyviruses by different
clones of an aphid species have shown that within the
species Aphis gossipyii, a 3.5-fold difference in propen-
sity to transmit between the most and least efficient
clones was observed (Lupoli et al., 1992).
For PVA, there are only limited data on the ability of
different aphid species to vector the virus. There are cur-
rently only seven aphid species reported as vectors: Aphis
frangulae, Aphis nasturtii, Brachycaudus helichrysi,
Macrosiphum euphorbiae, M. persicae, Neomyzus cir-
cumflexum and Rhopalosiphum padi (Loughnane, 1933;
Edwards, 1963; Brunt et al., 1996; Radcliffe & Rags-
dale, 2002). Loughnane (1933) also reported that Aula-
corthum solani (the glasshouse potato aphid) failed to
transmit PVA. These reports simply give a confirmation
of the ability to transmit the virus with no attempt to
quantify the efficiency of each species.
The work reported here was carried out between 2010
and 2012. The objectives of the work reported were: (i)
to ascertain which of the aphid species commonly found
in yellow water traps (YWTs) in seed potato fields are
capable of transmitting PVA, (ii) to ascertain the REFs
for transmission of PVA by confirmed vectors, (iii) to
ascertain or revisit the REFs for transmission of PVY
strains using UK-collected aphids and UK-collected virus
isolates, including a M. persicae control (clone Mp2) that
was the same M. persicae clone used by Verbeek et al.
(2010) to allow for comparison of results, and (iv) to
compare transmission rates of PVY and PVA using a
binomial (logit) generalized mixed model. The output of
the model is presented in comparison with the results
obtained by comparing transmission rates with the
M. persicae internal control (Mp2). This was done to
allow for the potential influence of variation in virus titre
between leaves, because this was found by Verbeek et al.
(2010) to be a factor that influenced virus transmission
results using the same experimental method.
Materials and methods
Virus isolates
The virus isolates used in this study were obtained from the
virus-infected potato collection held at SASA, Edinburgh, UK
(DV field plots) kindly donated by Dr Christophe Lacomme.
The source of PVYO and PVYN were tubers of the cultivar
Maris Piper (DV71 and DV69, respectively). Nadine (DV 76)
was used as the source of PVYNTN. Desiree (DV 28) was used
as a source for PVA. Field isolates used in this study were used
in field studies and characterized at SASA as part of the same
AHDB-potato funded study (data not presented). Potato plants
were grown from infected daughter tubers in a glasshouse at
18–22 °C, ambient humidity, 20 h light: 4 h dark (L20:D4; with
supplemental lighting). Virus infection was confirmed using
ELISA (as described below) prior to transmission work being
carried out.
Aphid collection and rearing
Where possible, aphids were collected from the wild in the UK
(listed in Table 1 as ‘UK wild’). Each species was collected at
least three times from separate locations, with the aim of pro-
ducing three distinct clonal cultures for each species. However,
not all of the clones survived. Where wild-caught aphids could
not be used, aphid cultures that were already held at Fera were
used (listed as ‘Fera culture’). Where these were not available,
cultures were generously provided by Richard Harrington,
Rothamsted Research, UK (Rothamsted culture) and Brian Fen-
ton, The James Hutton Institute, UK (JHI culture). Additionally,
a M. persicae control culture was kindly provided by Martin
Verbeek at PRI, Netherlands. In each case a clonal culture was
initiated from a single aphid. These were isolated onto a range
of hosts as detailed in Table 1 and grown in aphid-proof cages
in the glasshouse at 18–22 °C, ambient humidity, L20:D4 (with
supplemental lighting). Aphid populations were allowed to
increase on their respective culture hosts until they were of suffi-
cient abundance to allow further experimental work.
Determination of relative efficiency factors
The method used for determination of the REFs was adapted
from Verbeek et al. (2010). For each virus isolate, 50 aphids of
the control M. persicae (Mp2) and 200 aphids of the aphid
clone being tested were collected, i.e. 50 aphids for each of the
viruses being studied. Apteres were used for all species except
Plant Pathology (2017) 66, 325–335
 New vectors of PVA and PVY in the UK 327

Table 1 Origins of each aphid species clone and the host plants on using the double antibody sandwich enzyme-linked immunosor-
which they were reared bent assay (DAS-ELISA) method (Clark & Adams, 1977). Five
millilitres of leaf extraction buffer (0.01 M phosphate-buffered
Aphid species Clone Origin Host plant for culture saline (PBS, pH 7.4) containing 0.05% Tween-20, 2%
Acyrthosiphon 1 Rothamsted Vicia faba
polyvinylpyrrolidone (PVP) MW 40 000 (Sigma)) was added to
pisum culture
the bag and the leaflets were ground using a Homex 6 homoge-
2 Fera culture V. faba
nizer (BIOREBA AG). A further 5 mL leaf extraction buffer was
3 UK wild V. faba
added to the bag after sample disruption/homogenization.
Aphis fabae 1, 2, 3 UK wild V. faba
One hundred microlitres of the homogenized sample was
Brevicoryne 1, 2 UK wild Brassica oleracea var.
added in duplicate to the wells of microtitre plates that had been
brassicae capitata f. alba
precoated with PVA-, PVYO- and PVYN-monoclonal antibodies
Cavariella 1, 2 UK wild Anthriscus cerefolium
(SASA, Edinburgh, UK) at 1 lL mL 1. As no specific antisera
aegopodii
were available for confirmation of PVYNTN, the presence of this
Drepanosiphum A UK wild Acer pseudoplatanus
virus was also checked using PVYN antisera. Leaf samples from
platanoidis
positive and negative control material were also added to each
Hyperomyzus D UK wild Sonchus arvensis
plate. Negative controls were like-for-like, i.e. potato plant sam-
lactucae
ples were assessed against an uninfected potato control. Follow-
Macrosiphum me1, JHI culture Solanum melongena
ing an overnight incubation at 4 °C, plates were washed with
euphorbiae me3,
0.1 M PBS containing 0.5% Tween-20. A PVA-, PVYO- and
me4
PVYN-specific alkaline phosphatase conjugate was added to each
Metopolophium A, B, C UK wild Triticum aestivum
well at 0.25 lL mL 1 and plates were incubated for a further
dirhodum
2 h at 37 °C. Plates were then washed three times with 0.1 M
Microlophium 1, 2 UK wild Urtica dioica
PBS containing 0.5% Tween-20 prior to the addition of sub-
carnosum
strate. One hundred microlitres of p-nitrophenyl phosphate sub-
Myzus persicae B Rothamsted Brassica napus
strate (1 mg mL 1) was then added to each well, and plates
culture
were incubated at room temperature for 1 h to allow colour
D JHI culture Solanum melongena
development.
E JHI culture Brassica rapa var.
Plates were read using a microplate reader (ThermoFisher) at
pekinensis
405 nm. Samples were deemed to be positive when the mean
Mp2 NL culture B. rapa var. pekinensis
absorbance values were greater than three-fold that of the nega-
Rhopalosiphum 1 Fera culture T. aestivum
tive controls.
padi 2, 3 UK wild T. aestivum
Sitobion avenae 11, N, E UK wild T. aestivum
Calculation of relative efficiency factors
The percentage of plants infected with each virus isolate by
transmission with M. persicae clone Mp2 was calculated across
Drepanosiphum platanoidis for which this was not possible. three replicates of 50 plants.
Aphids were starved in batches of 50 for 2 h in 140 mm diame- The REF of each aphid clone was calculated according to Ver-
ter glass Petri dishes. One compound leaf was collected from beek et al. (2010): REF (clone) = No. infected plants (clone)/
each virus-infected potato plant. Two leaflets were taken from a No. infected plants (Mp2).
compound leaf for transmission experiments; the rest of the leaf The REF for M. persicae as a species was calculated as the
was kept for virus testing to confirm the infection status of the average of four M. persicae clones (Mp2, B, D, E) for each of
leaf. Fifty M. persicae were allowed to feed on one leaflet and the virus isolates used. This average was subsequently used as a
50 of the test species were fed on the other leaflet for an acquisi- correction factor to set the REF to 1 for the species M. persicae
tion access period of 2.5 min. Each aphid was transferred onto for each of the virus isolates: REFcorr. (clone) = REF (clone)/
an individual Physalis floridana or Nicotiana hesperis plant Correction factor.
(cotyledon stage), depending on the virus, and covered with a For the three PVY strains and for PVA, the overall REF for
plastic tube (30 mm diameter 9 110 mm) to prevent it from each aphid species was calculated from the average of the cor-
escaping. Due to its highly characteristic symptom expression rected REFs determined for the available clones of each species.
upon infection with viruses, P. floridana was used for tests for
transmission of PVYO, PVYN and PVYNTN, and similarly N.
Binomial (logit) generalized mixed model for
hesperis was used for tests for transmission of PVA. The tubes
were removed after 24 h and the aphids killed by spraying the
transmission of PVY strains
plants with Bug Clear Ultra (0.05 g L 1 acetamiprid; Scotts This method was applied to the data for PVY transmission.
Company (UK) Ltd), following the manufacturer’s instructions. There was insufficient data to apply it to PVA transmission
The plants were grown on in a plant growth room (20 °C, 60% because tests were only carried out with one strain of the virus.
RH, L16:D8) and visually inspected for virus symptoms 14 days A binomial (logit) generalized mixed model was fitted to the
after the aphids were killed. Any plants exhibiting symptoms of results. The size of the effects of aphid species and virus species
virus infection were counted. were estimated for those aphid species in which some transmis-
sion was observed. Variation was estimated between clones
within aphid species, between leaves treated with the same virus
Confirmation of source plant infection by ELISA strains, and between strains of the same virus. Upper limits for
To confirm infection status of virus source plants, leaf samples relative transmission rates for these aphids were estimated by
from individual potato plants were tested for potato viruses simulation to find the average infection rate that gives a 5%

Plant Pathology (2017) 66, 325–335

328
probability of observing zero transmission by 50 aphids each on
the number of leaves for the aphid species used in the study.
Results
Determination of relative efficiency factors –
transmission of virus strains by M. persicae Mp2
Observed symptoms of PVA infection in N. hesperis
were stunting, mosaic, leaf curling, thickened and brittle
leaves, and necrosis (Fig. 1). Observed symptoms of
infection with PVY strains in P. floridana were veinal
chlorosis, stunting, mosaic, crinkle, leaf curling and
necrosis (Fig. 2). The reaction of P. floridana was consis-
tent across all PVY strains tested.
The average percentage transmission by M. persicae
Mp2 was calculated across three replicates of 50 plants
for each virus isolate. The results are shown in Table 2
together with the results of tests for each clone of each
species with each virus strain. The average REF for all
four M. persicae clones tested was used as the correction
factor to relate the REFs of the other aphid species to M.
persicae. The corrected REFs are given in brackets in
Table 2.
Figure 1 PVA-infected Nicotiana hesperis showing growth retardation
and chlorotic mosaic. Photograph taken 14 days post-inoculation.
[Colour figure can be viewed at wileyonlinelibrary.com].
Figure 2 PVYN-infected Physalis floridana showing veinal chlorosis,
growth retardation and distortion. Photograph taken 14 days post-
inoculation. [Colour figure can be viewed at wileyonlinelibrary.com].
A. Fox et al.
There was variation in the observed transmission rate
of the clones within a species for the same virus isolate.
Myzus persicae clone E transmitted to fewer plants for
all virus isolates tested except PVYNTN. Acyrthosiphon
pisum clone 1 did not transmit PVYN although the other
two clones tested did. Only one of the three A. pisum
clones tested transmitted PVA. Only one of the three A.
fabae clones tested transmitted PVYO and two of the
three transmitted PVYNTN. Similarly, only one of three
clones of Metopolophium euphorbiae transmitted PVYO
and two of the three clones transmitted PVYN and
PVYNTN. Macrosiphum euphorbiae me3 did not transmit
any of the PVY isolates but transmitted PVA to a greater
number of plants than other clones of this species. Two
of the three Metopolophium dirhodum clones transmit-
ted PVYN and only one clone, C, transmitted PVYNTN
and PVA. Only one of the three R. padi clones transmit-
ted PVA. Two of the three Sitobion avenae clones trans-
mitted PVA and one of these clones, E, transmitted
PVYNTN at a lower rate than the other two clones of the
same species.
There was considerable variation between aphid species
in their ability to transmit the different virus species/strains
(Table 2). Four species (Brevicoryne brassicae, Drepanosi-
phum platanoidis, Hyperomyzus lactucae and Microlo-
phium carnosum) did not transmit any of the virus isolates
tested. All of the virus isolates were transmitted by M. per-
sicae. PVYO was transmitted variably: with high efficiency
by A. pisum and M. euphorbiae (one clone only); with
moderate efficiency by Cavariella aegopodii, R. padi and
S. avenae; and with poor efficiency by A. fabae. PVYN was
transmitted variably: with high efficiency by two clones of
M. dirhodum; and with moderate efficiency by A. pisum,
C. aegopodii, M. euphorbiae, R. padi and S. avenae. PVY
NTN
was transmitted variably: with good efficiency by R.
padi; with moderate efficiency by A. pisum, C. aegopodii
and S. avenae; with poor efficiency by A. fabae and M.
dirhodum; and with very variable efficiency by M. euphor-
biae. PVA was transmitted with good efficiency by
M. euphorbiae and S. avenae; with moderate efficiency by
one A. pisum clone, A. fabae and C. aegopodii; and with
poor efficiency by M. dirhodum and R. padi.
For the three PVY strains and PVA, the overall REF for
each aphid species was calculated from the average of the
corrected REFs determined for the available clones of
each species (Table 3). Acyrthosiphon pisum had a very
high REF for PVYO, higher than that of any other species
including M. persicae. Aphis fabae and M. euphorbiae
had much higher REFs for PVA than for any of the PVY
strains tested. Metopolophium dirhodum and S. avenae
were more efficient vectors of PVYN than of the other two
PVY strains or PVA. Rhopalosiphum padi had much
higher REFs for all of the PVY strains tested than for
PVA. Cavariella aegopodii was consistently moderately or
highly efficient at transmitting all of the PVY and PVA
isolates tested. This species had not previously been
reported to be a vector of potyviruses in potatoes.
Data presented in Figure 3 are a comparison of the
estimated mean transmission efficiencies for PVY strains
Plant Pathology (2017) 66, 325–335
 New vectors of PVA and PVY in the UK 329

Table 2 Relative efficiency factors (REFs) of

REFs per Potato virus Y (PVY) or Potato virus A
aphid clones tested. REFs are calculated
(PVA) isolate
relative to the transmission rate of the
Myzus persicae Mp2 control Aphid species Clone PVYO PVYN PVYNTN PVA
a
Myzus persicae Mp2 (control) 1.00 (47%) 1.00 (36%) 1.00 (35%) 1.00 (23%)
B 1.18 0.88 1.08 1.00
D 0.96 0.71 0.62 1.38
E 0.65 0.14 1.05 0.29
Correction factor 0.95 0.68 0.94 0.92
(average M.
persicae)b
Acyrthosiphon 1 1.06 (1.12)c 0.00 (0.00) 0.07 (0.07) 0.00 (0.00)
pisum 2 1.24 (1.31) 0.25 (0.37) 0.88 (0.94) 0.50 (0.54)
3 0.77 (0.81) 0.33 (0.49) 0.43 (0.46) 0.00 (0.00)
Aphis fabae 1 0.17 (0.18) 0.00 (0.00) 0.25 (0.27) 0.60 (0.65)
2 0.00 (0.00) 0.00 (0.00) 0.00 (0.00) 0.56 (0.61)
3 0.00 (0.00) 0.00 (0.00) 0.11 (0.12) 0.09 (0.10)
Brevicoryne 1 0.00 (0.00) 0.00 (0.00) 0.00 (0.00) 0.00 (0.00)
brassicae 2 0.00 (0.00) 0.00 (0.00) 0.00 (0.00) 0.00 (0.00)
Cavariella 1 0.46 (0.48) 0.43 (0.63) 1.39 (1.48) 0.63 (0.68)
aegopodii 2 1.00 (1.05) 0.24 (0.35) 0.41 (0.44) 0.35 (0.38)
Drepanosiphum A 0.00 (0.00) 0.00 (0.00) 0.00 (0.00) 0.00 (0.00)
platanoidis
Hyperomyzus D 0.00 (0.00) 0.00 (0.00) 0.00 (0.00) 0.00 (0.00)
lactucae
Macrosiphum me1 0.00 (0.00) 0.68 (1.00) 0.93 (0.99) 0.77 (0.84)
euphorbiae me3 0.00 (0.00) 0.00 (0.00) 0.00 (0.00) 1.13 (1.23)
me4 0.86 (0.91) 0.66 (0.97) 0.14 (0.15) 0.60 (0.65)
Metopolophium A 0.00 (0.00) 0.83 (1.22) 0.00 (0.00) 0.00 (0.00)
dirhodum B 0.00 (0.00) 0.95 (1.40) 0.00 (0.00) 0.00 (0.00)
C 0.00 (0.00) 0.00 (0.00) 0.21 (0.22) 0.07 (0.08)
Microlophium 1 0.00 (0.00) 0.00 (0.00) 0.00 (0.00) 0.00 (0.00)
carnosum 2 0.00 (0.00) 0.00 (0.00) 0.00 (0.00) 0.00 (0.00)
Rhopalosiphum 1 0.89 (0.94) 0.58 (0.85) 0.93 (0.99) 0.00 (0.00)
padi 2 0.69 (0.73) 0.24 (0.35) 1.17 (1.24) 0.00 (0.00)
3 0.62 (0.65) 0.35 (0.51) 0.57 (0.61) 0.05 (0.05)
Sitobion avenae 11 0.22 (0.23) 0.74 (1.09) 0.44 (0.47) 0.00 (0.00)
N 0.53 (0.56) 1.21 (1.78) 0.61 (0.95) 0.47 (0.51)
E 0.20 (0.21) 0.29 (0.43) 0.05 (0.05) 1.20 (1.30)

a
M. persicae clone Mp2 acted as an internal control in all experiments and the REF of this
clone was set to 1.00 as a reference. The percentage of infected test plants is indicated in
parentheses.
b
Average REF for M. persicae was calculated from REFs of clones Mp2, B, D and E. This
average is used as the correction factor for the REFs of other aphid species to set the REF
of the species M. persicae to 1.00.
c
REF calculated from transmission experiment compared with M. persicae clone Mp2 [REF
(clone)], in parentheses: REF corrected for the species M. persicae (divided by correction
factor) [REFcorr.(clone)].

from this study compared to previously published REFs
and those currently used in the aphid monitoring
schemes in support of the UK seed potato industry.
Cavariella aegopodii is confirmed for the first time as a
vector of PVY and from these data it seems to be a very
efficient vector. The grain aphids R. padi and S. avenae
appear to have REFs markedly higher than those arising
from other studies.
There are a few species where there is a marked differ-
ence in ability to transmit the different viruses. From
these data M. euphorbiae, a moderately efficient vector
of PVY, appears to be almost as efficient at transmitting
PVA as M. persicae. Aphis fabae has traditionally been
considered to be a low efficiency vector of PVY, a con-
clusion supported by the findings of this study; however,
it is a moderately efficient vector of PVA. Conversely,
M. dirhodum and R. padi, both moderately efficient
vectors of PVY, appear to be relatively inefficient as
transmitters of PVA.
In comparison with REFs for PVYN and PVYNTN
determined by Verbeek et al. (2010) and earlier stud-
ies, the REFs determined in this study were generally

Plant Pathology (2017) 66, 325–335

330 A. Fox et al.

Table 3 Average relative efficiency factors

Average REF per Potato virus Y (PVY) or Potato virus A (PVA) strain [REF
(REFs) of aphid clones tested in
(species, PVY or PVA strain)]
comparison to Verbeek et al. (2010) for
PVYN PVYNTN PVYNTN PVYN and PVYNTN, and Boquel et al. (2011)
PVYO PVYN (Verbeek PVYNTN (Verbeek (Boquel PVA for PVYNTN
this this et al., this et al., et al., this
Aphid species study study 2010)b study 2010)c 2011) study

Myzus 1.00 1.00 1.00 1.00 1.00 1.00 1.00

persicaea
Acyrthosiphon 1.08 0.29 0.08 0.49 0.07 0.08 0.18
pisum
Aphis fabae 0.06 0.00 0.03 0.13 0.04 0.00 0.45
Brevicoryne 0.00 0.00 0.00 0.00 0.00 0.04 0.00
brassicae
Cavariella 0.77 0.49 0.00 0.96 0.00 n.t. 0.53
aegopodii
Drepanosiphum 0.00 0.00 n.t.d 0.00 n.t. n.t. 0.00
platanoidis
Hyperomyzus 0.00 0.00 0.00 0.00 0.00 n.t. 0.00
lactucae
Macrosiphum 0.30 0.66 0.00 0.38 0.00 0.32 0.91
euphorbiae
Metopolophium 0.00 0.87 0.02 0.07 0.00 n.t. 0.03
dirhodum
Microlophium 0.00 0.00 n.t. 0.00 n.t. n.t. 0.00
carnosum
Rhopalosiphum 0.77 0.57 0.00 0.95 0.01 0.00 0.02
padi
Sitobion avenae 0.33 1.10 0.00 0.49 0.00 0.20 0.60

a
REF of M. persicae is set to 1.00.
b
Average of results for all clones for one isolate.
c
Average of results for all clones and three isolates.
d
n.t., not tested.

150
Relative transmission (%)

100

50 Figure 3 Estimated mean transmission

efficiency with 95% confidence intervals
generated in this study compared to
● ●
previous data covering a broad range of PVY
●
0 ● ● strains and the current UK PVY REFs. Where
data points are omitted from the graph these
A. pisum

A. fabae

B. brassicae

C. aegopodii

D. platanoidis

H. lactucae

M. carnosum

M. dirhodum

M. euphorbiae

R. padi

S. avenae

species were not tested in that specific

study. ● 1980s from Verbeek et al. (2010);
▲ De Bokx & Piron (1990); ■ average of
PVYN and PVYNTN strains, Verbeek et al.
(2010); + UK PVY, Northing et al. (2004); □
Aphid this study.

higher. The most notable differences are S. avenae, found that S. avenae, M. euphorbiae and C. aegopodii
M. dirhodum, M. euphorbiae, C. aegopodii, R. padi and did not transmit PVYN and PVYNTN whereas this study
A. pisum (Table 3). Specifically, Verbeek et al. (2010) found that they were moderately efficient vectors;

Plant Pathology (2017) 66, 325–335

 New vectors of PVA and PVY in the UK 331

Verbeek et al. (2010) also found that M. dirhodum, R. for most species. There are some species that stand out
padi and A. pisum were poor vectors whereas these data as having the most potential as vectors of PVY in addi-
demonstrate that these species were moderately good tion to M. persicae, i.e. R. padi, A. pisum, S. avenae, C.
vectors of PVYN and PVYNTN. aegopodii and M. euphorbiae. For PVA, the species with
most potential as vectors are M. persicae, M. euphorbiae,
C. aegopodii, S. avenae and A. fabae.
Binomial (logit) generalized mixed model for
transmission of PVY strains
Discussion
Variation between leaves was estimated to be the cause
of nearly all of the variation in results; a single strain of Any method for determining relative virus transmission
each of these viruses and a single clone of each of these efficiencies is always limited by the numbers of aphid
aphid species could be expected to be representative of individuals, the number of clones of aphid, and the par-
the populations of aphid clones and virus strains. The ticular strains of virus used. A further limitation of the
variation caused by introducing an unknown random method used for this study is that it cannot be assumed
clone of a known aphid species and an unknown random that transmission from a potato plant to one of the
strain of a known virus was estimated to result in an indicator plant species used equates to transmission
increase in the total standard deviation of less than 5% between potato plants (Harrington & Gibson, 1989).
(Table 4). However, this method does allow for an assessment as
The current approach to estimating transmissibility is to whether particular aphid species are capable of trans-
to estimate a rate of transmission of a vector species rela- mitting PVY or PVA. Further work would be required
tive to the rate of transmission by M. persicae on a vec- to assess the specific risks posed to potato crops in the
tor-by-vector basis. Following that approach with field.
separate mixed models for PVY and PVA gives estimated The modelling approach to comparing virus transmis-
transmission rates. These are shown expressed on the sion efficiency between aphid species, clones within spe-
proportion scale in Table 5. They are expressed relative cies and virus strains has not been previously applied to
to M. persicae (Mp2) in Table 6. These data show that this type of study. The modelling work undertaken on
there are broad 95% confidence intervals in transmission the transmission of the PVY strains took into account
efficiency for most of the species tested. For both viruses, the effects of population variation. This contrasted
the ranges in transmission efficiency overlap significantly with the approach of calculating REFs in that a range of
variation was produced for each virus–aphid combina-
tion rather than a single calculated point. There was very
Table 4 Estimates of the size of variation little variation in virus transmission efficiency between
aphid clones within species or between virus strains
Between group standard
within a species. Taking into account variability in the
deviation (logit scale)
virus titre of the leaves, the aphid and virus populations
Group PVY PVA may explain some of the differences in the ability of dif-
Leaf 1.490 1.077 ferent species to transmit viruses. Where aphid species
Strain (within virus) 0.0031 NA
Clone (within aphid) 0.4596 0.0002
Table 6 Estimated mean aphid transmission rate for PVY and PVA
relative to Myzus persicae Mp2 Control. Rates presented as lower and
upper 95% confidence intervals (CI)
Table 5 Estimated mean aphid transmission rate for PVY and PVA
presented as lower and upper 95% confidence intervals (CI) % Aphids (test % Aphids (test
species)⁄% species)⁄%
% Aphids: PVY % Aphids: PVA Aphids (M. Aphids (M.
Aphid species (95% CI) (95% CI) persicae): PVY persicae): PVA
Aphid species (95% CI) (95% CI)
M. persicae (ref) 12.2 48.0 14.9 26.3
A. fabae 0.5 3.6 4.1 13.0 A. fabae 1.0 14.2 18.6 54.5
A. pisum 7.3 23.2 0.6 4.9 A. pisum 14.6 128.5 2.4 19.6
B. brassicae 0 0.7 0 1.4 B. brassicae 0 3.2 0 5.6
C. aegopodii 7.4 27.6 3.5 15.4 C. aegopodii 15.4 156.0 15.7 67.6
D. platanoidis 0 2.4 0 12.1 D. platanoidis 0 5.9 0 56.6
H. lactucae 0 2.4 0 12.1 H. lactucae 0 5.9 0 56.6
M. carnosum 0 0.7 0 3.8 M. carnosum 0 2.9 0 16.4
M. dirhodum 0.1 1.6 0.03 1.7 M. dirhodum 0.3 5.9 0.1 6.8
M. euphorbiae 4.3 13.2 8.5 23.7 M. euphorbiae 8.1 66.4 41.4 129.3
M. persicae (test) 11.7 32.6 18.1 39.4 M. persicae (test) 24.1 207.4 97.3 236.8
R. padi 6.8 21.4 0.04 2.2 R. padi 13.4 115.9 0.2 8.9
S. avenae 4.7 15.9 5.6 15.3 S. avenae 9.1 79.8 26.4 64.9

Plant Pathology (2017) 66, 325–335

332 A. Fox et al.
have been previously unreported as virus vectors, this
may also explain differences in their transmission effi-
ciency between different studies.
These data represent a first report of relative efficiency
factors for PVA. The study is also the first demonstration
that A. fabae, A. pisum, C. aegopodii, M. dirhodum and
S. avenae have the ability to vector PVA. There were dif-
ferences in transmission efficiency between species and
sometimes between clones: M. euphorbiae was a high
efficiency PVA vector; S. avenae, A. fabae and C. aego-
podii were moderate; and A. pisum, M. dirhodum and
R. padi were low efficiency vectors.
This is also the first time C. aegopodii has been
reported as being a vector of PVY. Sitobion avenae
appears to be a far more efficient PVY vector than
reported by previous studies. This moderate efficiency of
transmission, combined with the propensity for these
species towards large population migrations (Hille Ris
Lambers, 1938; Llewellyn et al., 2003) may mean that
they have a more significant role in potato virus epi-
demics than previously thought.
The reasons for differences between this and previous
studies are unclear but there are possible explanations.
It is possible that the transmission ability of the Mp2
clone changed between studies. However, given that the
percentage of plants infected with PVYN by the control
clone during this study (36%) was identical to that
found by Verbeek et al. (2010) and the percentage
infection rates with PVYNTN were within 2% of each
other, this is unlikely. The most probable explanation,
given the results of the modelling approach used here,
is that there was a much smaller difference between the
studies than it first appears because most of the varia-
tion in transmission efficiency was due to the variation
in virus titre of the leaf used to infect the aphids. This
is in agreement with Verbeek et al. (2010) who found
that there was no significant difference in transmission
efficiency between virus strains when the same M. persi-
cae clone was used as the vector. There were also some
similarities and some differences between these results
and those of Boquel et al. (2011). In addition to the
differences in virus leaf titre, the differences in method-
ology and numbers of clones tested probably also con-
tributed to the differences in observed transmission
efficiency.
The variety of methods used previously to determine
transmission efficiency probably contributes to the differ-
ences in REFs attributed to each species. For example,
De Bokx & Piron (1990) and Piron (1986) used wild-
trapped rather than laboratory-cultured aphids and used
relatively low numbers of aphids. Boquel et al. (2011)
used a single clone of each aphid and tested transmission
between in vitro potato plantlets rather than between
potato and an indicator plant. Lupoli et al. (1992) found
that differences in transmission efficiency between clones
of Aphis gossypii were not as great as they first
appeared: as the numbers of replicates tested increased,
the differences between clones decreased. Although not
directly comparable by species, this supports the analysis
here that factors other than aphid clone have a greater
effect on the measured transmission efficiency than the
effect of the clone itself.
Cavariella aegopodii, a species not previously shown
to be a vector of potato-affecting potyviruses, was mod-
erately to highly efficient at transmitting all of the virus
isolates. Van Harten (1983) found that for six of the
years between 1970 and 1979, transmission on PVY
using bait plants coincided with M. persicae flight. How-
ever, for two years transmission occurred before the start
of M. persicae flight. It is hypothesized that this was due
to transmission by C. aegopodii, which is generally
found in YWTs earlier than M. persicae in the UK.
Varying transmission efficiencies for R. padi and PVY
have been recorded by different authors. Ryden (1979)
found that this species was a good vector of PVYO; how-
ever, Kostiw (1979) found that it was not. Van Hoof
(1980) found that R. padi was a poor vector of PVYN,
Boquel et al. (2011) found that it did not transmit
PVYNTN and Kurppa (1983) found that it did not trans-
mit PVY at all. There was variation in transmission effi-
ciency for each of the PVY strains tested during this
study but the variation was relatively small. The most
notable variation was that only one of the three clones
tested transmitted PVA. Again, when variation in leaf
virus titre is taken into account and the variation around
the mean transmission efficiency is calculated, it is unsur-
prising that results differed between studies.
There is also variation in previous studies as to the
ability of S. avenae to transmit PVYN. This study found
this species to be a better PVYN vector than did authors
of previous studies (although a variety of methods were
used): Van Hoof (1980) and Katis & Gibson (1985)
found that S. avenae did not transmit PVYN whereas
Piron (1986) and Harrington & Gibson (1989) found
that it was a PVYN vector, albeit a poor one.
The possible reasons for the differences in transmission
efficiency between clones are explored in detail by Ver-
beek et al. (2010). These include interactions between
the surface proteins of the aphid’s stylet, virus helper
component protein and the virus particle’s coat protein.
Of each of three clones of each species tested by Verbeek
et al. (2010), not all were able to transmit each virus
strain tested. Testing of additional clones and simultane-
ous exploration of the virus–helper protein–stylet protein
interactions would help elucidate the effects of interac-
tions at a molecular level on virus transmission in the
field. Host plant choice and acceptance by aphids is a
complex process (Powell et al., 2006) and no doubt con-
tributes to variation in REFs between species (Boquel
et al., 2011).
The use of the binomial (logit) generalized mixed
model as an alternative method of data analysis high-
lighted the variation in the leaves used in the experiments
as the major source of variation. In future, using the
maximum practicable number of leaves may be the best
way to reduce the uncertainty associated with the esti-
mates of the rate of transmission in these kinds of exper-
iments. The variation caused by introducing an unknown
Plant Pathology (2017) 66, 325–335
 New vectors of PVA and PVY in the UK 333

random clone of a known aphid species and an unknown comparable with the results of the calculation of REFs
random strain of a known virus is estimated to result that were carried out separately for individual virus
in an increase in the total standard deviation of less strains. However, it is possible to make a comparison
than 5%. based on the relative transmission efficiency of each
The estimated average transmission rates and esti- aphid species for each of the strains of PVY tested. When
mated average transmission rates relative to M. persicae this is done, the order of magnitude of transmission is
are shown in Figure 4. For transmission of PVA, this comparable between the two methods of analysis. In
analysis is in agreement with the calculated REF values order of combined REFs for all strains, C. aegopodii, A.
in that the order of species in terms of their efficiency to pisum, R. padi and S. avenae are the most efficient vec-
transmit this virus is the same. It also confirms the tors for each of the PVY strains, followed by M. euphor-
magnitude of efficiency of transmission compared with biae, then A. fabae and finally M. dirhodum.
M. persicae. This analysis further highlights the potential No transmission was observed by B. brassicae, D. pla-
of M. euphorbiae and M. persicae as extremely efficient tanoidis, H. lactucae and M. carnosum for any of the
vectors of PVA. It is interesting that, of all the aphid PVY strains tested or for PVA. Upper limits for relative
species tested, these are also the only two potato-coloniz- transmission rates for these aphids were estimated by
ing species. The potential of C. aegopodii, S. avenae and simulation to find the average infection rate that gives a
B. brassicae as important vectors of PVA was also 5% probability of observing zero transmission by 50
confirmed. aphids each on the number of leaves for the aphid spe-
For PVY, the data for all of the strains were analysed cies used in the study. Of these four species, the model
together, therefore the results are not directly predicts a higher upper 95% confidence interval for

60 (a)
Estimated average relative transimission (%)

50

40

30

20

10

0
B.brassicae
M.carnosum

M.dirhodum

D.platanoidis

H.lactucae

S.avenae

R.padi
A.fabae

M.euphorbiae

A.pisum

C.aegopodii

M.persicae(test)

M.persicae(reft)
Aphid species

160 (b)
Estimated average relative transimission (%)

140

120

100

80

60

40

20
Figure 4 (a) Estimated average transmission
rates from binomial (logit) generalized mixed 0
M.euphorbiae
M.carnosum

D.platanoidis
M.dirhodum
B.brassicae

C.aegopodii
H.lactucae

S.avenae

A.pisum
A.fabae

R.padi

model (95% confidence intervals). (b)

Estimated average transmission rates relative
to Myzus persicae from binomial (logit)
generalized mixed model (95% confidence
intervals). Grey bars PVY, black bars PVA. Aphid species

Plant Pathology (2017) 66, 325–335

334 A. Fox et al.
transmission by both D. platanoidis and H. lactucae than
by B. brassicae and M. carnosum with both PVY and
PVA. This is due to greater uncertainty due to fewer
available data points, because only one clone was tested
for each of these species compared with at least two
clones for the other species.
Following this study, further work is required in a num-
ber of areas: first, to assess the transmission risk, particu-
larly for PVA but also for some aphid species and PVY.
This should include an assessment of transmission both
between potato plants in the glasshouse under controlled
conditions and in seed potato crops in the field. An assess-
ment of clonal variation in transmission efficiency under
field conditions should be made to ascertain the variability
in risk to the crop from clonal variation under field condi-
tions. Secondly, to assess whether genetic analysis of virus
binding sites on the stylet can be used to predict the vector
efficiency of aphid species and whether this does account
for any of the variability in transmission efficiency
between species. Finally, to test the hypothesis that mature
plant resistance affects virus transmission efficiency (po-
tentially by changing secondary plant compounds affect-
ing feeding behaviour), how this is affected by potato
variety and aphid species and clone. Further investigation
in these areas will assist the development of decision sup-
port tools for growers and agronomists that incorporate
realistic estimates of virus transmission risk and provide
more accurate information for the development of virus
transmission risk forecasting tools.
Acknowledgements
This work was carried out with funding from the AHDB
Potato Council under project R428. The authors would
like to acknowledge the work of Samantha Bennett for
her assistance in ELISA testing leaf samples from this
study; Danny Skelton, Andrew Shaw and Richard Natt
for growing plants; Michelle Powell for assistance with
transmission experiments; and John Magson for cultur-
ing the aphids.
References
AHDB, 2015. GB Potatoes Market Intelligence Data 2014–15. [http://
www.potato.org.uk/sites/default/files/publication_upload/GB%
20Potatoes%20Market%20Intelligence%202014-15_0.pdf]. Accessed
26 May 2016.
Basky Z, Alm asi A, 2005. Differences in aphid transmissibility and
translocation between PVYN and PVYO isolates. Journal of Pest
Science 78, 67–75.
Beemster A, De Bokx J, 1987. Survey of properties and symptoms. In: de
Bokx JA, van der Want JPH, eds. Viruses of Potatoes and Seed-Potato
Production. Wageningen, Netherlands: Pudoc, 84–113.
Boiteau G, Singh M, Singh RP, Tai GCC, Turner TR, 1998. Rate of spread
of PVYn by alate Myzus persicae (Sulzer) from infected to healthy plants
under laboratory conditions. Potato Research 41, 335–44.
Boquel S, Ameline A, Giordanengo P, 2011. Assessing aphids potato
virus Y-transmission efficiency: a new approach. Journal of Virological
Methods 178, 63–7.
Broadbent L, 1948. Aphids migration and the efficiency of the trapping
method. Annals of Applied Biology 35, 379–94.
Brunt AA, Crabtree K, Dallwitz M, Gibbs A, Watson L, 1996. Viruses of
Plants. Descriptions and Lists From the VIDE Database. Wallingford,
UK: CAB International.
Carnegie S, McCreath M, 2010. Mosaic virus symptoms in potato crops
and the occurrence of growth cracking in tubers. Potato Research 53,
17–24.
Clark MF, Adams A, 1977. Characteristics of the microplate method of
enzyme-linked immunosorbent assay for the detection of plant viruses.
Journal of General Virology 34, 475–83.
Coutts B, Jones R, 2015. Potato virus Y: contact transmission, stability,
inactivation, and infection sources. Plant Disease 99, 387–94.
De Bokx JA, Piron PGM, 1990. Relative efficiency of a number of aphid
species in the transmission of Potato virus YN in the Netherlands.
Netherlands Journal of Plant Pathology 96, 237–46.
Edwards A, 1963. A non-colonizing aphid vector of potato virus
diseases. Nature 200, 1233–4.
Fera, 2013. England and Wales Seed Potato Classification Scheme – 2013
season review. [http://webarchive.nationalarchives.gov.uk/
20140904082245/http://
www.fera.defra.gov.uk/plants/plantHealth/documents/ewSPCSStats
2013.pdf]. Accessed 26 May 2016.
Harrington R, Gibson R, 1989. Transmission of potato virus Y by
aphids trapped in potato crops in southern England. Potato Research
32, 167–74.
Harrington R, Katis N, Gibson R, 1986. Field assessment of the relative
importance of different aphid species in the transmission of potato
virus Y. Potato Research 29, 67–76.
Hille Ris Lambers D, 1938. Contributions to a Monograph of the
Aphididae of Europe. I–V. Leiden, Netherlands: Temminckia.
Katis N, Gibson R, 1985. Transmission of potato virus Y by cereal
aphids. Potato Research 28, 65–70.
Kostiw M, 1979. Transmission of potato virus Y by Rhopalosiphum padi
L. Potato Research 22, 237–8.
Kurppa A, 1983. Potato viruses in Finland and their identification.
Journal of the Scientific Agricultural Society of Finland 55, 189–301.
LeRomancer M, Kerlan C, 1994. Biological characterisation of various
geographical isolates of potato virus Y inducing superficial necrosis on
potato tubers. Plant Pathology 43, 138–44.
Llewellyn K, Loxdale H, Harrington R, Brookes C, Clark S, Sunnucks P,
2003. Migration and genetic structure of the grain aphid (Sitobion
avenae) in Britain related to climate and clonal fluctuation as revealed
using microsatellites. Molecular Ecology 12, 21–34.
Loughnane JB, 1933. Insect transmission of virus A of potatoes. Nature
131, 838–9.
Lupoli R, Labonne G, Yvon M, 1992. Variability in the transmission
efficiency of potyviruses by different clones of Aphis gossypii.
Entomologia Experimentalis et Applicata 65, 291–300.
Mello AFS, Olarte RA, Gray SM, Perry KL, 2011. Transmission
efficiency of Potato virus Y strains PVYo and PVYN-Wi by five aphid
species. Plant Disease 95, 1279–83.
Nolte P, Whitworth J, Thornton MK, McIntosh CS, 2004. Effect of
seedborne Potato virus Y on performance of Russet Burbank, Russet
Norkotah, and Shepody potato. Plant Disease 88, 248–52.
Northing P, Walters K, Barker I, King L, 2004. Crop specific virus risk
assessment: a cost effective management tool for the seed potato
growing industry. In: Heilbronn T, ed. Proceedings of Crop Protection
in Northern Britain, Dundee, UK, 2004. Peterborough, UK: The
Association for Crop Protection in Great Britain, 297–302.
Pickup J, Davie K, Fox A, Highet F, Holmes R, Dale F, 2009.
Epidemiology of viruses in Scottish seed potatoes. Aspects of Applied
Biology 94, 5–10.
Pickup J, Fox A, Holmes R, Highet F, Davie K, Lacomme C, 2010.
Potato viruses PVA and PVY – do they have the same aphid
vectors? In: Heilbronn T, ed. Proceedings of Crop Protection in
Northern Britain 2010, Dundee, UK, 2010. Peterborough, UK: The
Association for Crop Protection in Northern Britain, 219–24. [http://
www.sipr.ac.uk/CPNB/Index_and_Proceedings_2010.pdf]. Accessed 26
May 2016.
Plant Pathology (2017) 66, 325–335
 New vectors of PVA and PVY in the UK
Piron P, 1986. New aphid vectors of potato virus YN. Netherlands
Journal of Plant Pathology 92, 223–9.
Powell G, Tosh CR, Hardie J, 2006. Host plant selection by aphids:
behavioral, evolutionary, and applied perspectives. Annual Review of
Entomology 51, 309–30.
Radcliffe EB, Ragsdale DW, 2002. Aphid-transmitted potato viruses: the
importance of understanding vector biology. American Journal of
Potato Research 79, 353–86.
Ryden K, 1979. Havrebladulsen, Rhopalosiphum padi, kan sprida
potativirus Y. Vaxtskyddsnotiser 43, 51–3.
Sigvald R, 1986. Forecasting the incidence of potato virus Y(0). In:
McLean GD, Garrett RG, Ruesink WG, eds. Plant Virus Epidemics:
Monitoring, Modelling and Predicting Outbreaks. Sydney, Australia:
Academic Press, 419–41.
Sigvald R, 1987. Aphid migration and the importance of some aphid
species as vectors of potato virus Yo (PVYo) in Sweden. Potato
Research 30, 267–83.
Sigvald R, 1990. Aphids on potato foliage in Sweden and their
importance as vectors of Potato virus Y0. Acta Agriculturae
Scandinavica 40, 53–8.
Singh RP, Valkonen JP, Gray SM et al., 2008. Discussion paper. The
naming of Potato virus Y strains infecting potato. Archives of Virology
153, 1–13.
Plant Pathology (2017) 66, 325–335
335
Steinger T, Goy G, Gilliand H, Hebeisen T, Derron J, 2015. Forecasting
virus disease in seed potatoes using flight activity data of aphid
vectors. Annals of Applied Biology 166, 410–9.
Sturz A, Stewart J, McRae K, Diamond J, Lu X, Singh R,
2000. Assessment of the importance of seed cutting, in-
season cultivation, and the passage of row equipment in the spread
of PVY in potatoes. Canadian Journal of Plant Pathology 22,
166–73.
Van der Zaag D, 1987. Yield reduction in relation to virus infection.
In: de Bokx JA, van der Want JPH, eds. Viruses of Potatoes and
Seed-Potato Production. Wageningen, Netherlands: Pudoc,
149–50.
Van Harten A, 1983. The relation between aphid flights and the spread
of potato virus YN (PVYN) in the Netherlands. Potato Research 26,
1–15.
Van Hoof H, 1980. Aphid vectors of potato virus YN. European Journal
of Plant Pathology 86, 159–62.
Verbeek M, Piron PGM, Dullemans AM, Cuperus C, van der Vlugt
RAA, 2010. Determination of aphid transmission efficiencies for N,
NTN and Wilga strains of Potato virus Y. Annals of Applied Biology
156, 39–49.
Were H, Kabira J, Kinyua Z et al., 2013. Occurrence and distribution of
potato pests and diseases in Kenya. Potato Research 56, 325–42.