The ability of the green peach aphid

(Myzus persicae) to penetrate mesh crop

covers used to protect potato crops
against tomato potato psyllid (Bactericera
cockerelli)
Howard London1 ,2 , David J. Saville1 ,3 , Charles N. Merfield4 , Oluwashola Olaniyan1
and Stephen D. Wratten1
1
Bio-Protection Research Centre, Lincoln University, Lincoln, New Zealand
2
National Agricultural Research and Extension Institute, Mon Repos, East Coast Demerara, Guyana
3
Saville Statistical Consulting Limited, Lincoln, Canterbury, New Zealand
4
The BHU Future Farming Centre, Lincoln University, Lincoln, New Zealand

ABSTRACT
In Central and North America, Australia and New Zealand, potato (Solanum tubero-
sum) crops are attacked by Bactericera cockerelli, the tomato potato psyllid (TPP). ‘Mesh
crop covers’ which are used in Europe and Israel to protect crops from insect pests, have
been used experimentally in New Zealand for TPP control. While the covers have been
effective for TPP management, the green peach aphid (GPA, Myzus persicae) has been
found in large numbers under the mesh crop covers. This study investigated the ability
of the GPA to penetrate different mesh hole sizes. Experiments using four sizes (0.15
× 0.15, 0.15 × 0.35, 0.3 × 0.3 and 0.6 × 0.6 mm) were carried out under laboratory
conditions to investigate: (i) which mesh hole size provided the most effective barrier to
GPA; (ii) which morph of adult aphids (apterous or alate) and/or their progeny could
breach the mesh crop cover; (iii) would leaves touching the underside of the cover, as
opposed to having a gap between leaf and the mesh, increase the number of aphids
Submitted 15 May 2018 breaching the mesh; and (iv) could adults feed on leaves touching the cover by putting
Accepted 17 May 2020 only their heads and/or stylets through it? No adult aphids, either alate or apterous,
Published 7 August 2020 penetrated the mesh crop cover; only nymphs did this, the majority being the progeny
Corresponding author of alate adults. Nymphs of the smaller alatae aphids penetrated the three coarsest mesh
Charles N. Merfield, sizes; nymphs of the larger apterae penetrated the two coarsest sizes, but no nymphs
[email protected]
penetrated the smallest mesh size. There was no statistical difference in the number of
Academic editor aphids breaching the mesh crop cover when the leaflets touched its underside compared
Nigel Andrew
to when there was a gap between leaf and mesh crop cover. Adults did not feed through
Additional Information and the mesh crop cover, though they may have been able to sense the potato leaflet using
Declarations can be found on
page 10
visual and/or olfactory cues and produce nymphs as a result. As these covers are highly
effective for managing TPP on field potatoes, modifications of this protocol are required
DOI 10.7717/peerj.9317
to make it effective against aphids as well as TPP.
Copyright
2020 London et al.
Subjects Agricultural Science
Distributed under
Creative Commons CC-BY 4.0 Keywords Aphids, Tomato potato psyllid, Mesh crop covers, Insect nets, Insect exclusion screens

OPEN ACCESS

How to cite this article London H, Saville DJ, Merfield CN, Olaniyan O, Wratten SD. 2020. The ability of the green peach aphid (Myzus
persicae) to penetrate mesh crop covers used to protect potato crops against tomato potato psyllid (Bactericera cockerelli). PeerJ 8:e9317
http://doi.org/10.7717/peerj.9317
 INTRODUCTION
Potato (Solanum tuberosum L.) is a globally important food crop, having the fourth highest
production level of 388 million tonnes in 2017 after maize (Zea mays L.), wheat (Triticum
aestivum L.), and rice (Oryza sativa L.) (FAOSTAT, 2020). In New Zealand, potatoes
are the highest grossing vegetable, with consumers purchasing approximately NZ $119
million in 2013 (Vegetables.co.nz, 2020). However, potato production is threatened by the
tomato potato psyllid (TPP, Bactericera cockerelli (Ŝulc 1908) (Hemiptera, Triozidae)).
This phloem-feeding insect originated in North and central America and was first
identified in New Zealand in 2006 (Teulon et al., 2009) and in Western Australia in 2017
(International Plant Protection Convention, 2017). TPP feeds on plants in the Solanaceae
and Convolvulaceae families (Wallis, 1955), and can cause complete crop loss (Munyaneza,
2013; Munyaneza, 2014).
Due to the negative impacts of TPP on potatoes in New Zealand, organic farmers asked
researchers to investigate non-chemical management approaches. Biological options such
as the predatory mite Anystis baccarum L. (Geary et al., 2016) were explored, but without
commercial success. In the laboratory, the coccinellid beetle Cleobora mellyi (Mulsant 1850)
has very high consumption rates of TPP, but this remains to be confirmed in glasshouse
and field crops (O’Connell et al., 2012; Pugh, O’Connell & Wratten, 2015).
‘Mesh crop covers’ (also referred to as ‘insect nets’, ‘Agronets’, ‘insect exclusion screens’)
have been used in Europe for many years to protect a wide range of crops, but not
potatoes, from both invertebrate and vertebrate pests (Collier, 2001; Collier, 2002; Hill,
1987; Saidi et al., 2013). In New Zealand, however, such covers have only recently been
investigated experimentally. Mesh crop covers with a hole size up to 0.6 mm were completely
impermeable to TPP in laboratory tests, and were able to reduce TPP populations in field
trials to very low levels, even outperforming insecticides (Merfield, 2017; Merfield et al.,
2015a; Merfield, Hale & Hodge, 2015b; Merfield et al., 2019).
Despite the promising results obtained with mesh crop covers for control of TPP, an
unexpected result was that aphids, believed to be mostly the green peach aphid (GPA,
Myzus persicae (Sulzer, 1776) (Hemiptera: Aphididae)) appeared in large numbers under
the mesh crop covers, particularly in the 2016–17 field trials where their populations were
significantly higher than uncovered controls, even though the edges of the mesh crop
covers were dug into the soil, creating a complete seal (Merfield, 2017; Merfield et al., 2019).
Aphids can significantly affect plant growth and development, reducing yields. In
addition, GPA in particular, is a vector of many plant viruses that also cause significant
yield losses (Capinera, 2001).
The GPA is the most common and widespread aphid on potatoes in New Zealand, as
it feeds on many plant species (Stufkens & Teulon, 2001). It is also the most economically
important aphid on potatoes, both in New Zealand and worldwide, because it transmits
both potato virus Y and leaflet curl virus, which are among the most damaging of the potato
viruses (Marczewski, 2001; Saguez et al., 2013; Srinivasan et al., 2013; Woodford, 1992). The
main management tool for aphids in potatoes is insecticides. However, the GPA has

London et al. (2020), PeerJ, DOI 10.7717/peerj.9317 2/15

 developed resistance to a number of these (Bass et al., 2014; Foster, Devine & Devonshire,
2007), which means that both novel and improved non-chemical control techniques are
required.
With mesh crop covers being highly effective for TPP management on potatoes, the
major challenge is understanding how aphids are circumventing mesh crop covers. Also it
is unclear if adults can, from outside the mesh crop cover, feed on potato leaves touching
the underside of it. If so, this means aphids outside the mesh crop cover could transmit
viruses to potatoes under it. This could discourage seed-potato growers from using the
mesh crop cover as a management option for TPP because of virus transmission to tubers
intended for propagation.
With these gaps in knowledge, the present research was therefore designed to investigate
(i) if aphid stylets can penetrate mesh crop cover of different hole sizes; (ii) if there is a
difference in this respect between alate and apterous adults and/or if their progeny have the
ability to penetrate mesh crop cover as individuals; (iii) if having potato leaves touching
the mesh crop cover from below increases the number of individual aphids penetrating it,
compared to when the leaves do not touch the mesh crop cover; and (iv) if adult aphids
are capable of feeding on potato leaves through the mesh crop cover.

MATERIALS AND METHODS

GPA was sourced from a colony cultured on Brassica rapa subsp. chinensis (L.) pak choi
(cultivar: Mei Qing Choi F1) kept at Lincoln University in a controlled-temperature room.
The room was kept at 16 h day length, temperature of 23 ◦ C with a 4 ◦ C range and 60%
relative humidity. Potato plants (cv. Ilam Hardy) were grown in a glasshouse at the Lincoln
University plant nursery to provide leaflets for the laboratory experiment.
For the laboratory work, two, nine-cm diameter Petri dishes were used to create two
compartments separated by mesh crop cover; the top dish contained the aphids and the
bottom one a single potato leaflet. In the ‘control’ treatments, three aphids were placed
in the bottom dish (Fig. 1). A piece of moist tissue paper was placed in the bottom dish
to maintain humidity. Leaflets were then collected from potato plants and cotton wool
was wrapped around the petiole of the leaflet, which was inserted into an Eppendorf tube
filled with water to maintain leaflet turgidity. The tube with leaflet inserted was placed in
the lower dish with the adaxial surface facing up. The mesh crop cover was carefully glued
around the full circumference of the opening between the two dishes, because, in previous
experiments by Hodge, Bluon & Merfield (2019), aphids could locate and penetrate minimal
gaps between the mesh crop cover and hard surfaces. The two Petri dishes were then held
together with plastic food wrap. For the mesh crop cover treatments, three adult aphids
were inserted through a hole (15 mm diameter) in the top of the upper dish, after which
the hole was sealed with mesh crop cover (0.15×0.15 mm mesh) held in place by adhesive
tape.
There was a total of 24 treatments in a 4 × 2 × 3 factorial design: four mesh crop cover
hole sizes × two aphid morphs (apterous or alate) × (three leaflet/aphid positions), in a
randomised complete block, with five replicates. Eight of these treatments were controls,

London et al. (2020), PeerJ, DOI 10.7717/peerj.9317 3/15

 Figure 1 Experimental set up: (1) top Petri dish, (2) bottom Petri dish, (3) hole for aphid introduction,
(4) mesh between dishes, (5) Eppendorf tube and leaflet. For the eight ‘control’ treatments, aphids were
placed below the mesh, while for the other 16 treatments, aphids were placed above the mesh.
Full-size DOI: 10.7717/peerj.9317/fig-1

one for each of the 4 mesh crop cover hole sizes and 2 aphid morphs, in which three aphids
were placed directly on the leaflet under the mesh crop cover. The other 16 (= 4 × 2 × 2)
treatments had a mesh crop cover barrier between aphids and leaflets. The mesh crop cover
hole sizes stated by the manufacturer were 0. 15×0.15 mm, 0.15 × 0.35 mm, 0.3 × 0.3
mm and 0.6× 0.6 mm. Aphid morphs were apterous or alate, while leaflet positions were
touching or not touching the mesh crop cover barrier. The experiment ran for 72 h, at
which point the number of aphids, both adults and nymphs, on the leaflets were counted.
The experiment was conducted in a controlled temperature room as above.
To investigate whether adult aphids could feed through the mesh crop cover, all adults
in the upper dish (size 00) at 12, 24, 36 and 48 h through the opening of the top Petri
dish. Therefore, 240 individuals were touched four times each, giving a total of 960 tests of
feeding. Those that moved following probing were considered to not have been feeding,
while those that remained in the same position following probing were judged as having

London et al. (2020), PeerJ, DOI 10.7717/peerj.9317 4/15

 Table 1 Measurements of each mesh type.

Mesh size (mm)

0.15× 0.15 0.15× 0.35 0.3× 0.3 0.6× 0.6
Mean 0.14 0.13 0.15 0.32 0.37 0.23 0.52 0.52
Max. 0.16 0.15 0.18 0.37 0.53 0.31 0.57 0.55
Min. 0.12 0.10 0.12 0.30 0.27 0.17 0.45 0.47

their stylets inserted into the leaflet and therefore, to be feeding (Auclair, 1963; Giordanengo
et al., 2010).
Mesh crop covers with hole sizes 0.15 × 0.15 mm and 0.15 × 0.35 mm were supplied by
AB Ludvig Svensson (http://www.ludvigsvensson.com) as ECONET 1515 and ECONET
1535. Those measuring 0.3 × 0.3 mm and 0.6 × 0.6 mm were supplied by Crop Solutions
Ltd. (http://www.cropsolutions.co.uk) and were custom-made for an earlier field trial
(Merfield, 2017). To test the accuracy of the measurement for each mesh crop cover hole
size used in this experiment, ten random samples of each type were selected and 10 holes
of each sample were measured under a Nikon SMZ25 microscope (magnification range
0.63–15.75×). The mean, minimum and maximum mesh hole size measurements are
presented in Table 1.
All data were analysed in a randomised block analysis of variance (ANOVA) (with a
factorial treatment structure) using GenStat R
18th edition. The response variable (number
of aphids on potato leaflets) was subjected to a square-root transformation to normalise the
data before analysis. Also, the analysis was split into two ANOVAs to achieve homogeneity
of variance. (1) The eight controls (4 mesh hole-sizes ×2 aphid-morphs), which were
relatively highly variable, were analysed separately as a 4× 2 factorial with 5 blocks. (2) For
the 16 non-control treatments, six were all zeroes and hence had zero variability, so were
omitted from the analysis, leaving 10 treatments which were analysed as a (2× 2 + 1) ×2
factorial with 5 blocks.

RESULTS
For the eight control treatments, with aphids below the mesh, there were no significant
differences in nymph numbers produced by the two aphid morphs, no significant linear or
quadratic components of mesh crop cover hole size (assuming these were in the ratio 1: 2:
3: 6), nor any significant interaction components (Table 2).
In the 16 treatments with adults placed above the mesh cover, only nymphal, not adult
aphids were able to pass through the mesh. Nymphs of the smaller alate adults penetrated
the 0.15 × 0.35, 0.3 × 0.3 and 0.6 × 0.6 meshes but not the 0.15 × 0.15 mesh (Table 2).
Nymphs of the larger apterous adults penetrated the 0.3× 0.3 and 0.6× 0.6 meshes but did
not breach the 0.15× 0.15 and 0.15× 0.35 ones.
Comparing when leaflets touched or did not touch the mesh crop cover, there was no
significant difference in the number of nymphs penetrating the mesh (P = 0.612). The
interaction between aphid morph (alate and apterous) and the leaflet touching mesh crop
cover or not was also not significant (P = 0.066).

London et al. (2020), PeerJ, DOI 10.7717/peerj.9317 5/15

 √
Table 2 Mean ( ) number of aphid nymphs of apterous and alate parents breaching different mesh
sizes when leaflets were touching the mesh or not. (A) Controls were statistically analysed. (B) Treat-
ments with means in brackets indicate those that were omitted because they had zero mean and zero vari-
ance. m.e. = main effect.
Aphid Mesh Mean of square Back
morph size (mm) root of # of transformed
nymphs below mesh means
(A)
Control Apterous 0. 15×0.15 2.460 6.05
0. 15×0.35 2.202 4.85
0. 3×0.3 1.940 3.76
0. 6×0.6 2.448 5.99
Alate 0. 15×0.15 1.823 3.32
0. 15×0.35 1.673 2.80
0. 3×0.3 2.455 6.03
0. 6×0.6 1.756 3.08
LSD 5% 1.235
Significance of m.e., apterous vs alate not sig.
(B)
Leaflet not touching mesh Apterous 0.15× 0.15 (0.000) 0.00
0.15× 0.35 (0.000) 0.00
0.3× 0.3 0.483 0.23
0.6× 0.6 0.883 0.78
Alate 0.15× 0.15 (0.000) 0.00
0.15× 0.35 0.200 0.04
0.3× 0.3 0.283 0.08
0.6× 0.6 0.829 0.69
Leaflet touching mesh Apterous 0.15× 0.15 (0.000) 0.00
0.15× 0.35 (0.000) 0.00
0.3× 0.3 0.200 0.04
0.6× 0.6 0.400 0.16
Alate 0.15× 0.15 (0.000) 0.00
0.15× 0.35 0.546 0.30
0.3× 0.3 1.012 1.02
0.6× 0.6 1.029 1.06
LSD 5% 0.905

No aphids, at any time fed through the mesh crop cover, as all moved when probed with
the artist’s brush.

DISCUSSION
Mesh crop cover hole size and aphid penetration
The fact that no adult aphids penetrated the covers, differs from the result of Hodge, Bluon
& Merfield (2019) studying GPA and the melon aphid (Aphis gossypii (Glover 1877)). They
found that adult GPA did penetrate LS ECONET 1515, but no GPA adults penetrated
the larger hole LS ECONET 1,535, a result which appears inconsistent. Hodge, Bluon &

London et al. (2020), PeerJ, DOI 10.7717/peerj.9317 6/15

 Merfield (2019) did, however, find that nymphs penetrated the mesh, in agreement with
these results.
That adults did not penetrate mesh, but newly hatched nymphs did, suggesting a means
by which aphids entered all mesh covered plots in the field trial of Merfield (2017): adult
aphids that alighted on the upper surface of the mesh, produced nymphs, which are small
enough to penetrate the mesh, and once through that they can reproduce on the potato
crop. This result needs to be verified under field conditions.
The extent to which aphids penetrate mesh and for mesh to control aphids is clearly
variable. For example, Bethke, Redak & Paine (1994) who worked with adult aphids, found
GPA could not pass through a square, brass mesh with hole sizes ranging from 0.19 mm2 to
0.94 mm2 , but melon aphid could penetrate meshes larger than 0.46 mm2 . Using mosquito
nets of knitted polyester, 30 gm−2 and a mesh size of 25 holes per cm2 , untreated or treated
with deltamethrin, supported 50 cm above seedling cabbages (Brassica oleracea L.), Martin
et al. (2006) found the treated nets had significantly lower numbers of plants infested with
the mustard aphid (Lipaphis erysimi (Kaltenbach 1843)). In subsequent work, Martin et
al. (2013) used mesh with 0.9 mm diameter, treated with alphacypermethrin and two
untreated nets, one with the same hole size and the other with a smaller one of 0.4 mm, and
control without mesh, to cover pot-grown cabbages in the field with the mesh supported 30
cm above the plants. They found no cabbage aphid (Brevicoryne brassicae L.) under the 0.9
mm alphacypermethrin treated and untreated 0.4 mm mesh, but a small, yet statistically
significant greater number, under the untreated 0.9 mm mesh. In comparison, both GPA
and mustard aphids (counted together as ’green aphids’), were not present under the
treated 0.9 mm mesh but were present in much larger numbers than cabbage aphid in the
two other meshes. The untreated 0.9 mm mesh had a statistically significant population 5.8
times larger than the non-covered control while the 0.4 mm mesh had more than twice the
number of aphids than the control, although the difference was not statistically significant.
Licciardi et al. (2007), using deltamethrin-treated polyester mesh with 40 holes/cm2 , kept
50 cm above cabbages, with the mesh either removed during the day (’temporary’) or kept
permanently on the crop, found that aphids infested the untreated control immediately on
planting out the crop. The temporary mesh was infested at 20 days after planting (DAP),
and the permanent mesh at 30 DAP, but then, the aphid numbers under the permanent
screen rapidly increased to finish at approximately four times that under the temporary
mesh. In orchard trials in France and Italy using mesh covers with hole sizes of either 2.2
× 5.4 mm or 3 × 7.4 mm to control codling moth (Cydia pomonella L.), Alaphilippe et
al. (2016) found that rosy apple aphid (RAA, Dysaphis plantaginea (Passerini 1860)) and
woolly apple aphid (Eriosoma lanigerum (Hausmann, 1802)) populations increased. In
contrast, Dib, Sauphanor & Capowiez (2010) found mesh covers reduced RAA populations
and also those of their ant mutualists as well as their predators under covers also used
for codling moth control. In a comparison of nets treated and untreated with insecticides
against black bean aphids (Aphis fabae (Scopoli 1763)) on French bean (Phaseolus vulgaris
L.), Gogo et al. (2014) found both mesh types significantly reduced aphid populations
compared with the control, but did not eliminate them.

London et al. (2020), PeerJ, DOI 10.7717/peerj.9317 7/15

 In a few cases, mesh crop covers appeared to be impenetrable to aphids, or at least
can prevent aphids reaching crops, though this varies with aphid species e.g., cabbage
aphid cv. GPA (Martin et al., 2013), and could be related to size, though other factors, e.g.,
behavioural, may also have a role. However, in most cases discussed above, mesh covers
appeared only to delay aphids reaching the crops, and, in some cases, aphid populations
then rapidly built to levels much higher than those in untreated controls or insecticide
treatments. It is hypothesised that the mesh is preventing, or at least reducing the range
and number of aphid natural enemies that can reach the crop.
Aphids are also not the only insect species that can circumvent mesh. Talekar, Su &
Lin (2003) and Licciardi et al. (2007) reported that adult female moths of the armyworm
(Spodoptera littoralis (Boisduval 1833)) laid eggs on the top of a hooped screen, and the
newly hatched larvae were sufficiently small to penetrate the mesh and drop onto the
crop below. Merfield (2017) found a large number of lacewings (Micromus tasmaniae
(Walker 1860)) in plots of potatoes under mesh, following aphid outbreaks under the
mesh. Lacewing adults are much too large to penetrate mesh, and the mesh was dug into
the soil preventing entry from the edges, so it was hypothesised that the lacewings laid
eggs on the mesh, and then the neonate larvae penetrated the mesh. As aphids, lacewings
and armyworms would not be expected to lay eggs or produce nymphs in the absence of
suitable hosts, this indicates that the insects can detect their hosts through the mesh, even
when the mesh is at some distance from the crop (Licciardi et al., 2007; Talekar, Su & Lin,
2003).

Difference between the progeny of alate and apterous adults to

penetrate mesh crop cover
In the present study, nymphs produced by alate adults penetrated the 0. 15×0.35 mesh
crop cover, while those produced by apterous adults did not. This supports the findings
of (Dixon & Wratten, 1971) who found that alate aphids were smaller, and produced fewer
and smaller nymphs than did apterous aphids, which indicates that only the smallest size
mesh crop cover hole size (0. 15×0.15 mm) would be an effective barrier. For mesh crop
cover with larger hole sizes, neonate nymphs of both adult morphs can enter the mesh
crop cover, so both alate and apterous adults are potential threats to the crop. However,
apterous aphids, lacking wings, could arrive only on the outside of mesh crop cover from
other plants bordering the mesh crop cover. In the field trial of Merfield (2017) and Merfield
et al. (2019), the periphery of mesh crop cover was kept free of vegetation with residual
herbicides and tillage such that apterous aphids walking onto the mesh crop cover should
have been eliminated, yet all mesh crop cover plots were infested by aphids. It is therefore
believed, that nymphs, which infested the mesh crop cover treatments in those trials, were
produced by alate adults.

Adult aphid feeding through mesh and implications for virus

transmission
That adults were not found to feed through the mesh indicates potato viruses will not
be transmitted through mesh. However, this result is not direct evidence for lack of
transmission, as it only demonstrated a lack of feeding but not a lack of probing. GPA

London et al. (2020), PeerJ, DOI 10.7717/peerj.9317 8/15

 can also transmit viruses by probing (Radcliffe & Ragsdale, 2002). Direct testing of virus
transmission is required, using virus-infected aphids to test the rates of transmission when
mesh is present or not.

Solutions for aphids penetrating mesh crop covers

That some aphid species, and also armyworm (Licciardi et al., 2007; Talekar, Su & Lin,
2003) can circumvent mesh indicates that for some insect pests, additional control measures
will be required when using covers. Three general approaches are suggested: (i) modify
the physical properties of the mesh to prevent pests alighting or reproducing on it; (ii)
use insecticide or repellent-treated mesh covers to kill or repel alighting pests; (iii) use
supplemental biological control. For aphids on potatoes, the approach used should ideally
also ensure that virus transmission is minimised.
A range of research has altered the physical properties of mesh crop covers to both
repel and attract insects. Some of this research can be considered for field potatoes.
These alterations include: different colours (Ben-Yakir et al., 2012a), and ultra-violet light
properties (Ben-Yakir et al., 2012b), such that the mesh prevents aphids alighting.
Insecticide treated mesh crop covers have been discussed above, and, are clearly highly
effective in some situations. A further refinement of this approach has been to create
attractive areas on the mesh, e.g., yellow spots, with only the attractive areas treated with
insecticides (Ben-Yakir et al., 2014). Chemical repellants can also be used in place of biocides
(Martin et al., 2013). However, the insecticides and repellents are lost from the mesh covers
over time, so the efficacy of treated mesh covers reduces, meaning their effective lifespan
can be less than that of untreated mesh covers (Dáder et al., 2015). Treating mesh also
increases cost, and may require personnel to use protective equipment when handling and
storing the mesh covers. If a single chemical is used to treat the mesh, this is likely to create
increased pressure for evolved resistance, both against biocides, and, also repellents (Foster,
Devine & Devonshire, 2007). This could be partially mitigated through impregnating the
mesh covers with multiple insecticides with different modes of action, but, at further
increased cost.
A range of biological control approaches could be used. In the case of armyworm
(discussed above), infestations were effectively controlled using the biological control
agent (BCA) Bacillus thuringiensis (Talekar, Su & Lin, 2003). In field crops, microbial
BCAs could be applied through the mesh (Ester, Van de Zande & Frost, 1994; Merfield,
2018). Augmentative biological control using predators and parasitoids is widely used in
protected cropping, such as glasshouses. Mesh crop covers are considered to be a form of
protected cropping, in that they should prevent introduced BCAs escaping from the crop, so
existing glasshouse biocontrol solutions could be leveraged. For example, Gagnon Lupien,
Aoun & Chouinard (2014) suggested the release of the commercially available coccinellid
Adalia bipunctata (L.) to compensate for the lack of aphid natural enemies under mesh crop
covers. Other biological control agents (BCAs) that have been used to successfully manage
GPA in protected envrionments include, Aphidius matricariae, Aphidius colemani (Zamani
et al., 2007) and Micromus tasmaniae (Harcourt, 1996; Jonsson et al., 2009). Augmentative
biological control with insects could be further enhanced by the use of banker plants

London et al. (2020), PeerJ, DOI 10.7717/peerj.9317 9/15

 (which provide supplemental food for beneficial insects, which helps them maintain a
stable population) (Frank, 2010) grown under the mesh / among the potato crop; this
approach is already used for control of GPA (Andorno & López, 2014).

CONCLUSIONS
Because of commercial availability and cost, it is recommended that the 0. 6×0.6 mm
mesh crop cover be used to manage TPP on potatoes, even though this mesh can be
penetrated by GPA nymphs. Further research is required to confirm GPA nymphs’ ability
to penetrate mesh covers in the field and whether or not mesh is an effective barrier to
virus spread, both by adults and nymphs. A considerable amount of research is required
into methods to control GPA and other aphid species in mesh-covered potato crops. If
mesh crop cover is combined with additional approaches that achieve a high level of GPA
control and therefore that of potato viruses, the benefits to the potato seed industry are
likely to be considerable. Mesh crop covers have been in use across Israel and Europe since
the early 1990s and the area used in Europe is estimated at 50,000 ha, with hundreds of ha
on individual farms (Ian Campbell, Crop Solutions Ltd., personal communication). Mesh
crop covers are therefore a completely farm-proven, large-scale, technology. If an effective
means of managing aphids on potatoes under mesh crop covers can be developed, it has
the potential to be a viable option for management of TPP on potato in New Zealand and
globally.

ACKNOWLEDGEMENTS
The authors thank Brent Richards and Leona Meachen from Lincoln University plant
nursery for assisting in growing potato plants; Jenny Brookes for the supply of GPA; Brian
Kwan for technical advice; Janine Johnson for editorial assistance; Crop Solutions Ltd and
AB Ludvig Svensson for donating mesh crop cover samples.

ADDITIONAL INFORMATION AND DECLARATIONS

Funding
This work was supported by the Ministry of Foreign Affairs and Trade, New Zealand, and
the Bio-Protection Research Centre, Lincoln University, New Zealand. The funders had no
role in study design, data collection and analysis, decision to publish, or preparation of the
manuscript.

Grant Disclosures
The following grant information was disclosed by the authors:
Ministry of Foreign Affairs and Trade, New Zealand.
Bio-Protection Research Centre, Lincoln University, New Zealand.

Competing Interests
David J. Saville is employed by Saville Statistical Consulting Limited and is contracted
to the Bio-Protection Research Centre, Lincoln University, for statistical advice. Stephen

London et al. (2020), PeerJ, DOI 10.7717/peerj.9317 10/15

 D Wratten is an Academic Editor for PeerJ. The authors declare there are no competing
interests.

Author Contributions
• Howard London conceived and designed the experiments, performed the experiments,
prepared figures and/or tables, authored or reviewed drafts of the paper, and approved
the final draft.
• David J. Saville conceived and designed the experiments, analyzed the data, authored or
reviewed drafts of the paper, and approved the final draft.
• Charles N. Merfield and Stephen D. Wratten conceived and designed the experiments,
authored or reviewed drafts of the paper, and approved the final draft.
• Oluwashola Olaniyan conceived and designed the experiments, performed the
experiments, authored or reviewed drafts of the paper, and approved the final draft.

Data Availability
The following information was supplied regarding data availability:
The raw data is available as a Supplementary File.

Supplemental Information
Supplemental information for this article can be found online at http://dx.doi.org/10.7717/
peerj.9317#supplemental-information.

REFERENCES
Alaphilippe A, Capowiez Y, Severac G, Simon S, Saudreau M, Caruso S, Vergnani S.
2016. Codling moth exclusion netting: an overview of French and Italian experi-
ences. IOBC-WPRS Bulletin 112:31–35.
Andorno AV, López SN. 2014. Biological control of Myzus persicae (Hemiptera: Aphi-
didae) through banker plant system in protected crops. Biological Control 78:9–14
DOI 10.1016/j.biocontrol.2014.07.003.
Auclair JL. 1963. Aphid feeding and nutrition. Annual Review of Entomology 8:439–490
DOI 10.1146/annurev.en.08.010163.002255.
Bass C, Puinean AM, Zimmer CT, Denholm I, Field LM, Foster SP, Gutbrod O, Nauen
R, Slater R, Williamson MS. 2014. The evolution of insecticide resistance in the
peach potato aphid, Myzus persicae. Insect Biochemistry and Molecular Biology
51:41–51 DOI 10.1016/j.ibmb.2014.05.003.
Ben-Yakir D, Antignus Y, Offir Y, Shahak Y. 2012a. Colored shading nets impede
insect invasion and decrease the incidences of insect-transmitted viral dis-
eases in vegetable crops. Entomologia Experimentalis et Applicata 144:249–257
DOI 10.1111/j.1570-7458.2012.01293.x.
Ben-Yakir D, Antignus Y, Offir Y, Shahak Y. 2012b. Optical manipulations of in-
sect pests for protecting agricultural crops. Acta Horticulturae 956:609–615
DOI 10.17660/ActaHortic.2012.956.72.

London et al. (2020), PeerJ, DOI 10.7717/peerj.9317 11/15

 Ben-Yakir D, Antignus Y, Offir Y, Shahak Y. 2014. Photoselective nets and screens
can reduce insect pests and diseases in agricultural crops. Acta Horticulturae
1015:95–102 DOI 10.17660/ActaHortic.2014.1015.10.
Bethke JA, Redak RA, Paine TD. 1994. Screens deny specific pests entry to greenhouses.
California Agriculture 48:37–40 DOI 10.3733/ca.v048n03p37.
Capinera JL. 2001. Green Peach Aphid, Myzus persicae (Sulzer) (Insecta: Hemiptera:
Aphididae). In: Entomology and Nematology Department. Florida Cooperative
Extension Service, Institute of Food and Agricultural Sciences, University of Florida,
11.
Collier RH. 2001. Crop covers offer considerable opportunities for pest control. The
Vegetable Farmer 2001:18–20.
Collier RH. 2002. Using crop covers and mulches as an aid to pest control. The Vegetable
Farmer 2002:16–19.
Dáder B, Legarrea S, Moreno A, Plaza M, Carmo-Sousa M, Amor F, Viñuela E,
Fereres A. 2015. Control of insect vectors and plant viruses in protected crops
by novel pyrethroid-treated nets. Pest Management Science 71:1397–1406
DOI 10.1002/ps.3942.
Dib H, Sauphanor B, Capowiez Y. 2010. Effect of codling moth exclusion nets on the
rosy apple aphid, Dysaphis plantaginea, and its control by natural enemies. Crop
Protection 29:1502–1513 DOI 10.1016/j.cropro.2010.08.012.
Dixon AFG, Wratten SD. 1971. Laboratory studies on aggregation, size and fecundity in
the black bean aphid, Aphis fabae Scop. Bulletin of Entomological Research 61:97–111
DOI 10.1017/S0007485300057485.
Ester A, Van de Zande JC, Frost AJP. 1994. Crop covering to prevent pest damage to
field vegetables, and the feasibility of pesticide application through polyethylene nets.
In: Brighton crop protection conference: Pests and diseases -1994. Brighton: The British
Crop Protection Council, 761–766.
FAOSTAT. 2020. Available at http:// www.fao.org/ faostat/ en/ #compare (accessed on 14
January 2020).
Foster SP, Devine G, Devonshire AL. 2007. Insecticide resistance. In: Emden HF, Van
Harrington R, eds. Aphids as crop pests. Oxford: Oxford University Press, 261–286.
Frank SD. 2010. Biological control of arthropod pests using banker plant systems: past
progress and future directions. Biological Control 52:8–16
DOI 10.1016/j.biocontrol.2009.09.011.
Gagnon Lupien N, Aoun M, Chouinard G. 2014. Le contrôle des pucerons par les coc-
cinelles sous filets d’exclusion dans un verger de pommiers en régie biologique au Québec:
L’efficacité de la coccinelle Adalia bipunctata comme moyen de lutte aux pucerons sous
filet. Victoriaville, Québec, Canada: CETAB+ Le Centre d’expertise et de transfert en
agriculture biologique et de proximité. 5.
Geary IJ, Merfield CN, Hale RJ, Shaw MD, Hodge S. 2016. Predation of nymphal tomato
potato psyllid, Bactericera cockerelli (Šulc) (Hemiptera: Triozidae), by the predatory
mite, Anystis baccarum L. (Trombidiformes: Anystidae). New Zealand Entomologist
39:110–116 DOI 10.1080/00779962.2016.1218525.

London et al. (2020), PeerJ, DOI 10.7717/peerj.9317 12/15

 Giordanengo P, Brunissen L, Rusterucci C, Vincent C, Van Bel A, Dinant S, Girousse
C, Faucher M, Bonnemain J-L. 2010. Compatible plant-aphid interactions:
how aphids manipulate plant responses. Comptes Rendus Biologies 333:516–523
DOI 10.1016/j.crvi.2010.03.007q.
Gogo EO, Saidi M, Ochieng JM, Martin T, Baird V, Ngouajio M. 2014. Microclimate
modification and insect pest exclusion using agronet improve pod yield and quality
of French bean. HortScience 49:1298–1304 DOI 10.1273/HORTSCI.49.10.1298.
Harcourt N. 1996. Evaluation of the potential of the Tasmanian brown lacewing,
Micromus tasmaniae Walker [Neuroptera: Hemerobiidae], as a biocontrol agent of
aphids on glasshouse capsicums M.Sc. Lincoln University.
Hill DS. 1987. Agricultural insect pests of temperate regions and their control. Cambridge:
Cambridge University Press.
Hodge S, Bluon A, Merfield CN. 2019. Pore size requirements for mesh crop cov-
ers to protect potatoes from aphids. New Zealand Entomologist 41:66–71
DOI 10.1080/00779962.2018.1556914.
International Plant Protection Convention. 2017. Detection of Bactericera cockerelli
(Tomato-potato psyllid) in Western Australia. Available at https:// www.ippc.int/ en/
countries/ australia/ pestreports/ 2017/ 02/ detection-of-bactericera-cockerelli-tomato-
potato-psyllid-in-western-australia/ .
Jonsson M, Wratten SD, Robinson KA, Sam SA. 2009. The impact of floral resources
and omnivory on a four trophic level food web. Bulletin of Entomological Research
99:275–285 DOI 10.1017/S0007485308006275.
Licciardi S, Assogba-Komlan F, Sidick I, Chandre F, Hougard JM, Martin T. 2007. A
temporary tunnel screen as an eco-friendly method for small–scale farmers to protect
cabbage crops in Benin. International Journal of Tropical Insect Science 27:152–158
DOI 10.1017/S1742758407883184.
Marczewski S. 2001. Potato leafroll virus-assisted aphid transmission of potato spindle
tuber viroid to potato leafroll virus-resistant potato. Journal of Phytopathology
149:195–201 DOI 10.1046/j.1439-0434.2001.00600.x.
Martin T, Assogba-Komlan F, Houndete T, Hougard JM, Chandre F. 2006. Efficacy of
mosquito netting for sustainable small holders’ cabbage production in Africa. Journal
of Economic Entomology 99:450–454, 455 DOI 10.1603/0022-0493-99.2.450.
Martin T, Palix R, Kamal A, Delétré E, Bonafos R, Simon S, Ngouajio M. 2013. A
repellent net as a new technology to protect cabbage crops. Journal of Economic
Entomology 106:1699–1706 DOI 10.1603/EC13004.
Merfield CN. 2017. Mesh crop covers for non-chemical potato pest & disease control: final
results from the 2016-17 field trial of mesh vs. agrichemicals. Lincoln: The BHU Future
Farming Centre, 48.
Merfield CN. 2018. Testing the compatibility of mesh crop covers with desiccant sprays in
seed potato production. Lincoln: The BHU Future Farming Centre, 10.
Merfield CN, Geary IJ, Hale RJ, Hodge S. 2015a. Field evaluation of the effective-
ness of mesh crop covers for the protection of potatoes from tomato potato

London et al. (2020), PeerJ, DOI 10.7717/peerj.9317 13/15

 psyllid. New Zealand Journal of Crop and Horticultural Science 43:123–133
DOI 10.1080/01140671.2015.1015576.
Merfield CN, Hale RJ, Hodge S. 2015b. Pore size criteria of mesh crop covers for the
exclusion of tomato-potato psyllid (Bactericera cockerelli). New Zealand Journal of
Crop and Horticultural Science 43:53–58 DOI 10.1080/01140671.2014.949800.
Merfield CN, Winder L, Stilwell SA, Hofmann RW, Bennett JR, Wargent JJ, Hodge S.
2019. Mesh crop covers improve potato yield and inhibit tomato potato psyllid and
blight: The roles of mesh pore size and ultraviolet radiation. Annals of Applied Biology
174:223–237 DOI 10.1111/aab.12489.
Munyaneza JE. 2013. Bactericera cockerelli. EPPO Bulletin 43:202–208
DOI 10.1111/epp.12044.
Munyaneza JE. 2014. Bactericera cockerelli (tomato/potato psyllid). Available at https:
// www.cabi.org/ isc/ datasheet/ 45643 (accessed on 14 January 2020).
O’Connell DM, Wratten SD, Pugh AR, Barnes AM. 2012. ‘New species association’
biological control? Two coccinellid species and an invasive psyllid pest in New
Zealand. Biological Control 62:86–92 DOI 10.1016/j.biocontrol.2012.03.011.
Pugh AR, O’Connell DM, Wratten SD. 2015. Further evaluation of the south-
ern ladybird (Cleobora mellyi) as a biological control agent of the invasive
tomato–potato psyllid (Bactericera cockerelli). Biological Control 90:157–163
DOI 10.1016/j.biocontrol.2015.06.009.
Radcliffe EB, Ragsdale DW. 2002. Aphid-transmitted potato viruses: the importance
of understanding vector biology. American Journal of Potato Research 79:353–386
DOI 10.1007/BF02870173.
Saguez J, Giordanengo P, Vincent C, Alyokhin A. 2013. Aphids as major potato pests.
In: Alyokhin A, Vincent C, Giordanengo P, eds. Insect pests of potato. San Diego:
Academic Press, 31–63.
Saidi M, Gogo EO, Itulya FM, Martin T, Ngouajio M. 2013. Microclimate modification
using eco-friendly nets and floating row covers improves tomato (Lycopersicon
esculentum) yield and quality for small holder farmers in East Africa. Agricultural
Sciences 4:577–584 DOI 10.4236/as.2013.411078.
Srinivasan R, Cervantes FA, Alvarez JM, Alyokhin A, Vincent C, Giordanengo P. 2013.
Aphid-borne virus dynamics in the potato-weed pathosystem. In: Alyokhin A,
Vincent C, Giordanengo P, eds. Insect pests of potato. San Diego: Academic Press,
311–337.
Stufkens M, Teulon D. 2001. Aphids species on potato crops in Canterbury. New Zealand
Plant Protection 54:235–239 DOI 10.30843/nzpp.2001.54.3746.
Talekar NS, Su FC, Lin MY. 2003. How to grow safer leafy vegetables in nethouses and net
tunnels. AVRDC pub # 03-558. Shanhua; Taiwan: Asian Vegetable Research and
Development Center, 6.
Teulon DAJ, Workman PJ, Thomas KL, Nielsen M-C. 2009. Bactericera cockerelli:
incursion, dispersal and current distribution on vegetable crops in New Zealand.
New Zealand Plant Protection 62:136–144 DOI 10.30843/nzpp.2009.62.4783.

London et al. (2020), PeerJ, DOI 10.7717/peerj.9317 14/15

 Vegetables.co.nz. 2020. Top vegetables by spend: Ranking of vegetables based on
household expenditure. Available at https:// www.vegetables.co.nz/ education-and-
resources/ top-vegetables-by-spend/ (accessed on 14 January 2020).
Wallis RL. 1955. Ecological studies on the potato psyllid as a pest of potatoes. Washington:
U.S. Dept. of Agriculture.
Woodford J. 1992. Virus transmission by aphids in potato crops. Netherlands Journal of
Plant Pathology 98:47–54 DOI 10.1007/BF01974471.
Zamani AA, Talebi A, Fathipour Y, Baniameri V. 2007. Effect of temperature on life
history of Aphidius colemani and Aphidius matricariae (Hymenoptera: Braconidae),
two parasitoids of Aphis gossypii and Myzus persicae (Homoptera: Aphididae).
Environmental Entomology 36:263–271 DOI 10.1603/0046-225x-36.2.263.

London et al. (2020), PeerJ, DOI 10.7717/peerj.9317 15/15