Rice-Straw Mulch Reduces the Green Peach Aphid, Myzus persicae (Hemiptera: Aphididae) Populations on Kale, Brassica oleracea var. acephala (Brassicaceae) Plants

Abstract

Organic mulches, like peel and rice-straw, besides other materials affect the UV and temperature, which cause a reduction in the aphid arrival. The aim was to evaluate the effect of covering the soil with straw on the populations of the green peach aphid, Myzus persicae on the kale, Brassica oleracea var. acephala plants. The first experiment evaluated the direct effect of the rice-straw mulch and the second its indirect effect on aphid immigration, testing the plant characteristics that could lead to the landing preference of this insect. The third experiment evaluated the direct effect of the mulch on the aphid population. In the second and third experiments, four plants, each in a 14 L polyethylene pot with holes at the bottom, were used in areas with and without soil mulching. These pots were changed between areas, after seven days, to evaluate the effects of this change on the arrival of the winged aphids to the plants. Each plant was covered with anti-aphid gauze and inoculated with one winged M. persicae. Winged and apterous adults of this insect were counted per plant after 15 days. The temperature increased in the mulched plots to a maximum of 21-36°C and to 18-32°C in the plots with or without soil covering, respectively. Plant growth reduced the numbers of the winged aphids landing before and after they were moved to the bare soil plots. The nutrient content was similar in plants in both the mulched and no mulched plots. The population growth of M. persicae was higher in the control than in the mulched plots. This was partially due to temperatures close to 30°C in these plots and changes in the plant physiology. The soil mulching with rice-straw decreased the M. persicae landing, increased the plot temperatures and improved the vegetative growth of the kale plants.

Full text

Rice-Straw Mulch Reduces the Green Peach Aphid,
Myzus
persicae
(Hemiptera: Aphididae) Populations on Kale,
Brassica oleracea
var.
acephala
(Brassicaceae) Plants
Reinildes Silva-Filho
1
, Ricardo Henrique Silva Santos
2
, Wagner de Souza Tavares
2
, Germano Lea
˜o
Demolin Leite
3
, Carlos Frederico Wilcken
4
, Jose
´Eduardo Serra
˜o
5
, Jose
´Cola Zanuncio
1
*
1Departamento de Biologia Animal, Universidade Federal de Vic¸osa, Vic¸osa, Brazil, 2Departamento de Fitotecnia, Universidade Federal de Vic¸osa, Vic¸osa, Brazil,
3Instituto de Cie
ˆncias Agra
´rias, Universidade Federal de Minas Gerais, Montes Claros, Brazil, 4Departamento de Protec¸a
˜o Vegetal, Universidade Estadual Paulista, UNESP,
campus of Botucatu, Botucatu, Brazil, 5Departamento de Biologia Geral, Universidade Federal de Vic¸osa, Vic¸osa, Brazil
Abstract
Organic mulches, like peel and rice-straw, besides other materials affect the UV and temperature, which cause a reduction in
the aphid arrival. The aim was to evaluate the effect of covering the soil with straw on the populations of the green peach
aphid, Myzus persicae on the kale, Brassica oleracea var. acephala plants. The first experiment evaluated the direct effect of
the rice-straw mulch and the second its indirect effect on aphid immigration, testing the plant characteristics that could lead
to the landing preference of this insect. The third experiment evaluated the direct effect of the mulch on the aphid
population. In the second and third experiments, four plants, each in a 14 L polyethylene pot with holes at the bottom, were
used in areas with and without soil mulching. These pots were changed between areas, after seven days, to evaluate the
effects of this change on the arrival of the winged aphids to the plants. Each plant was covered with anti-aphid gauze and
inoculated with one winged M. persicae. Winged and apterous adults of this insect were counted per plant after 15 days.
The temperature increased in the mulched plots to a maximum of 21–36uC and to 18–32uC in the plots with or without soil
covering, respectively. Plant growth reduced the numbers of the winged aphids landing before and after they were moved
to the bare soil plots. The nutrient content was similar in plants in both the mulched and no mulched plots. The population
growth of M. persicae was higher in the control than in the mulched plots. This was partially due to temperatures close to
30uC in these plots and changes in the plant physiology. The soil mulching with rice-straw decreased the M. persicae
landing, increased the plot temperatures and improved the vegetative growth of the kale plants.
Citation: Silva-Filho R, Santos RHS, Tavares WdS, Leite GLD, Wilcken CF, et al. (2014) Rice-Straw Mulch Reduces the Green Peach Aphid, Myzus persicae
(Hemiptera: Aphididae) Populations on Kale, Brassica oleracea var. acephala (Brassicaceae) Plants. PLoS ONE 9(4): e94174. doi:10.1371/journal.pone.0094174
Editor: Martin Heil, Centro de Investigacio
´n y de Estudios Avanzados, Mexico
Received December 28, 2013; Accepted March 12, 2014; Published April 8, 2014
Copyright: ß2014 Silva-Filho et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Funding was received from the Conselho Nacional de Desenvolvimento Cientı
´fico e Tecnolo
´gico (CNPq), Coordenac¸a
˜o de Aperfeic¸oamento de Pessoal
de Nı
´vel Superior (CAPES) and Fundac¸a
˜o de Amparo a
`Pesquisa do Estado de Minas Gerais (FAPEMIG). The funders had no role in study design, data collection and
analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: zanuncio@ufv.br
Introduction
The chemical control of pests on the Brassica spp. L.
(Brassicaceae) plants increased the production costs and environ-
ment contamination [1,2]. However, reflective mulches, including
rice-straw, Oryza sativa L. (Poaceae) is a suitable alternative to
reduce it [3–5]. Mulch with synthetic materials and rice peels or
rice-straw can reduce the aphid infestation [3,6,7]. The organic
and synthetic mulches can repel the winged aphid due to theirs
color, heat reflection and increase in the UV and air temperature
near to the mulch, although synthetic ones are more reflective
[3,8].
The peel and rice-straw reflect UV, which reduced the virus
transmitted by the cabbage aphid, Brevicoryne brassicae L., 1758
(Hemiptera: Aphididae) to potato, Solanum tuberosum L. (Solanace-
ae) and kale, Brassica oleracea var. acephala (Brassicaceae) plants
[4,9]. This covering is more significant than the synthetic ones, as
it is more economical and does not require removal [10–12],
improves the soil by incorporating organic material and does not
contaminate the environment [13–15]. Mulch can also directly
affect the aphid immigration and their populations indirectly by
changes in the plant physiology which could lead to the lower
landing preference and population growth of these insects [16–18].
The green peach aphid, Myzus persicae Sulzer, 1776 (Hemiptera:
Aphididae) is one of the most important agricultural pests in the
world, which reduces the yield production in more than 40
different plant families [19,20]. This peach aphid is an efficient
vector of more than 100 plant viruses [21,22] and resistant to the
major insecticides being used [23,24].
This work studied the effects of the rice-straw mulch on the M.
persicae populations on kale plants, to test the following hypotheses:
(a) the mulch reduces the aphid landing on the kale plants; (b) this
effect is due to the higher air temperature in the plant
environment, (c) plant nutrient content changes, and (d) the
factors that increase aphid population.
PLOS ONE | www.plosone.org 1 April 2014 | Volume 9 | Issue 4 | e94174

Materials and Methods
The Direct Effect of the Mulch on Aphid Immigration
This experiment evaluates the direct effect of the rice-straw
mulch on the M. persicae immigration to the kale plants in the field
at the ‘‘Universidade Federal de Vic¸osa (UFV)’’ in Vic¸osa, Brazil.
The kale clone cultivar (B. oleraceae var. acephala) was obtained from
the germplasm bank of the UFV and the rice-straw mulch from
the agro-ecological sector of the UFV. The experiment was
conducted with five randomized blocks and two treatments (with
or without the mulch). Each plot had 16 plants spaced at
0.80 m60.80 m and 1.20 m apart.
The kale seedlings were then transplanted and the plants were
thinned on October 16 and 17, 2012 leaving them with five leaves
each. A total of 2.5 L of chicken manure and 200 g of 4-14-8 NPK
were applied per hole during the transplantation of the kale plants
and they were daily sprinkler-watered over the next 15 days.
Winged and apterous aphids were removed from the kale leaves
and 1.056 Kg of dry matter.m
–2
of rice-straw per hectare was
placed on the soil. The winged aphids landing on the four central
plants per plot were counted and removed daily at 5:00 P.M.
between October 18 and November 1, 2012. The four central
plants were chosen to avoid edge effects on the lateral ones. The
daily maximum temperature was recorded with a max-min
thermometer in the center of the plots at plant canopy height,
opposed to direct sunlight. The maximum temperature was
recorded because it was positively correlated to the aphid flying
period [25,26].
The data were evaluated by covariance analysis, with Poisson
error and x2 of Pearson to correct over dispersion, following F test
at 5% probability. The average winged M. persicae which landed on
the four kale plants per plot were obtained over 15 days. The
maximum average temperature was the first exploratory variable
(x
1
), the mulched and no mulched treatments, the second one (x
2
),
and the mean number of the winged aphids the response one (y)
on plots sampled. ‘‘Sistema para Ana´lises Estatı
´sticas e Gene´ticas
(SAEG)’’ version 9.1 [27] (Supplier: UFV) was the software used
for data analysis.
The Indirect Effect of the Mulch on Aphid Immigration
The second experiment evaluated the indirect effect of the
mulch on aphid immigration to test if the effect on the nutrient
content of the kale plants was correlated with the aphid landing.
These plants were cultivated in pots in bare soil or in mulch plots
and their positions were changed after seven days. The change in
the positions of the pots was made after the evaluations: those in
the plots with soil covering were transferred to plots without
covering and vice-versa. Counting and removal of the winged
aphids continued for more seven days. The lower degree of
immigration of this insect to the bare soil plots after changing the
pots positions would imply that the plants carried over some
characteristics from the previous environment. The kale seedlings
were transplanted on April 30, 2013 to 14 L polyethylene pots
with soil fertilized with 50 g of NPK (formulation 4-14-8) and 2.0
L of chicken manure which was chosen due to its richness in
nutrients and availability [28]. Poultry manure may have some
additional effects on aphid population along with effects of rice-
straw mulch such as increase plant vigor and water retention [29].
All the aphids were eliminated and the pots were placed into holes
at ground level in the field on May 30, 2013. The plot location and
design, leaf thinning, sampling, aphid removal, rice-straw layer
and irrigation were conducted similar to the first experiment.
The aphids were counted from May 30 to June 5, 2012
(‘beginning’ period) and from June 6 to June 12, 2012 (latter
period) after the pots had their positions changed. Two leaves were
taken from a kale plant per plot in June 5, 2012 to determine their
macronutrient content. The material sampled was washed with
deionized water, dried until constant weight, grounded and the
NO
3
–
,NH
4
+
, P, K, Ca, Mg and S content were determined based
on the dry matter [30,31].
Data were evaluated by multiple regression analysis, with
Poisson error, and x2 Pearson to correct over dispersion followed
by the F test at 5% probability. The average daily number of
winged M. persicae on the plants per plot was obtained during the
seven day period. The exploratory variables were x
1
=NO
3
–
,
x
2
=NH
4
+
,x
3
=P, x
4
=K, x
5
= Ca, x
6
= Mg, x
7
= S and
x
8
= mulch treatments and the mean number of winged aphids
was the result (y) on the plots sampled. The nutrient content of the
kale plants on the mulched and bare soils was compared with the
analysis of variance (p#0.05).
The Effect of Mulch on the Aphid Population Growth
One winged M. persicae was inoculated per kale leaf to evaluate
the mulch effect on the growth of the aphid colony. These leaves
were covered with anti-aphid gauze to prevent the inoculated
aphids from flying out, other aphids from landing and to avoid
predation. The aphids were inoculated on June 12, 2012 and all
the nymphs and winged adults of M. persicae were counted on June
27, 2012. This experiment had five replications, and the plot
design and plant manipulation were similar to the second
experiment.
The data were evaluated using the variance analysis with Poison
error and F test at 5% probability. The treatments (with or without
mulch) were considered the exploratory variable (x
1
) and the
number of nymphs and adult winged aphids were the response
variables (y).
No specific permits are required for the plantation of kale and
rearing M. persicae in Brazil. The field and laboratory studies did
not involve endangered or protected species.
Figure 1. Number of winged green peach aphid,
Myzus persicae
(Hemiptera: Aphididae) landed on kale,
Brassica oleracea
var.
acephala
(Brassicaceae) plants as related to maximum temper-
ature in the plots, with F
1,9
= 39.03, p#0.008, r
2
= 0.60. Each dot
corresponds to the mean number of aphids per plant in 10 plots with a
Poisson error and x2 of Pearson to correct over dispersion, followed F
test at 5% probability.
doi:10.1371/journal.pone.0094174.g001
Rice-Straw Mulch Reduces Aphid on Kale
PLOS ONE | www.plosone.org 2 April 2014 | Volume 9 | Issue 4 | e94174

Results
The number of winged M. persicae was lower on the kale plants
of the mulched plots than on those in the bare soil (F = 39.03;
d.f. = 1.8; p#0.008), 83 and 327 individuals, respectively, during
the monitoring period. The mulch reduced the number of the
winged M. persicae on the kale plants during the 15-day period
(Fig. 1) and increased the maximum temperature at canopy height
(Fig. 2). The maximum temperature ranged between 21–36uC and
18–32uC on the mulched and no mulched plots, respectively,
which implies that these factors had reduced the arrival of the
winged aphids.
As in the first experiment, the mulch decreased the M. persicae
immigration (F = 26.52; d.f. = 1.7; p#0.0001). The number of
individuals of this aphid was 1 and 61 and 520 and 351, at the
beginning and after the change in the positions of the pots, in the
mulched and no mulched plots, respectively. The number of
aphids which landed was higher in the no mulched plants moved
to the mulched plots (F = 26.52; d.f. = 1.7; p#0.0001), compared
with the ‘beginning’ period. On the other hand, plants from the
mulched plots had a lower number of winged aphids when moved
to the no mulched plots (Fig. 3). The macronutrient content of the
kale leaves was similar in the mulched and no mulched plots (p$
0.05), with means of: NO
3
–
= 1.30 dag.Kg
–1
,NH
4
+
= 1.36
dag.Kg
–1
, Ca = 1.88 dag.Kg
–1
, S = 0.10 dag.Kg
–1
, K = 2.41
dag.Kg
–1
, Mg = 0.43 dag.Kg
–1
, and P = 0.46 dag.Kg
–1
. The
nutrient content boron no relation to the number of aphids on
the kale plants (p$0.05).
The mulch reduced the population growth of M. persicae with a
lesser number of nymphs, adults (F = 35.62; d.f. = 1.8; p#0.0001)
and winged individuals (F = 8.12; d.f = 1.8; p#0.03) in the
mulched plots 15 days after the inoculation with the winged
insect (Fig. 4). In all, 31 adults and nymphs and 1 winged
individual were found per colony of M. persicae 15 days after the
inoculation, with a temperature of 33.8uC in the mulched plots.
This value was 318 adults and nymphs and 3 winged adults per
colony over the same 15 days in the no mulched plots which had a
temperature of 28.9uC.
Discussion
The temperature increasing in the plots by the mulch may
explain the reduced number of arriving winged M. persicae on the
kale plants as reported for the lower populations of Aphis sp.
(Hemiptera: Aphididae), Myzus sp. and silverleaf whitefly, Bemisia
argentifolii Bellows & Perring, 1994 (Hemiptera: Aleyrodidae) on
watermelon, Citrullus lanatus (Thunb.) Matsum. & Nakai (Cucurbi-
taceae) and corn, Zea mays L. (Poaceae) with the polyethylene
mulch which was attributed to raising the soil temperature and
plant growth besides light reflectance [32–34]. This confirms that
the mulch can decrease the aphid immigration due to the
temperature increase with a negative impact on the aphid
populations by slowing down the development and reducing the
fecundity [19,33]. Mulch obtained from a crop of sunn hemp,
Crotalaria juncea L. (Fabaceae) or weeds (original weed cover) acts as
physical barrier to lesser cornstalk borer, Elasmopalpus lignosellus
Zeller, 1848 (Lepidoptera: Pyralidae) around host plants of bush
bean, Phaseolus vulgaris L. (Fabaceae) in Florida, USA [35]. High
temperatures can be harmful to the developing embryos and thus,
reduce the population growth in subsequent generations [36,37].
The indirect effect of the mulch on the M. persicae immigration
to the kale plants may have induced this aphid to move to the no
mulched plots. This result suggests that the differences in the plant
physiology in each environment were maintained for at least seven
days. On the other hand, the effectiveness of these characteristics
(higher plants and better leaf development) to repel the winged
aphids is lower than the mulch effect. Mulching can improve the
physical and chemical properties of the soil and favors plant
growth [38,39]. The maintenance of adequate soil conditions is
important to assure satisfactory crop growth and high yields [8,40]
with a good impact on the insect pests [41,42]. Plants cultivated on
the mulched plots were more vigorous and with higher biomass
which could allow more effective defense mechanisms. This
probably includes the production of semiochemicals which repel
the aphids, thus resulting in lower M. persicae populations
[4,43,44]. This is due to the humidity maintenance, higher soil
temperature, better weed control and mineral nutrient increase in
the plants in the mulched plots [45,46]. The use of cover crops and
mulches are convenient non-chemical methods for managing some
insect pests and weeds. The numbers of Cicadellidae (Hemiptera),
Figure 2. Maximum temperature in the plots with kale,
Brassica
oleracea
var.
acephala
(Brassicaceae) plants on mulched and no
mulched plots (average of 15 days) with Poisson error and x2
of Pearson to correct over dispersion followed by an F test at
5% probability.
doi:10.1371/journal.pone.0094174.g002
Figure 3. Mean number of winged green peach aphid,
Myzus
persicae
(Hemiptera: Aphididae) landed on kale,
Brassica
oleracea
var.
acephala
(Brassicaceae) plants on mulched and
no mulched plots (hatched bars) at the beginning (days 1–7)
and after vase position was changed (days 8–14). Poisson error
and x2 of Pearson to correct over dispersion followed by an F test at 5%
probability.
doi:10.1371/journal.pone.0094174.g003
Rice-Straw Mulch Reduces Aphid on Kale
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Formicidae (Hymenoptera), Orthoptera, and small-bodied plant-
feeders (aphids, Aphidoidea; thrips, Thysanoptera, and whiteflies,
Aleyrodidae; Hemiptera) were higher in control (no mulched) or
cowpea, Vigna unguiculata (L.) Walp. (Fabaceae) plots than several of
the other mulch treatment plots (sunn hemp mulch; sorghum-
sudangrass mulch, Sorghum 6drummondii (Nees ex. Steud.) Millsp. &
Chase (Poaceae), and pine bark nuggets, Pinus sp., Pinaceae) in
Florida, USA, possibly because weed levels were higher in control
and cowpea plots [47]. Fire ants, Solenopsis spp. (Hymenoptera:
Formicidae) were more abundant where there was mulched cover
and are important predators of weed seed and pest insects in killed
cover crop plots and that cover crop mulches in summer pepper
(Capsicum annuum L. cv. ‘Camelot’, Solanaceae) and fall collard
(Brassica oleracea L. cv. ‘Champion’, Brassicaceae) production are
potentially viable alternatives to black plastic mulch and soil
fumigation in South Carolina, USA [48].
The indirect effect of the mulch on M. persicae immigration was
not related to the macronutrient content of the kale leaves and no
negative relationship between the aphid landing and expected K
content of the plant was found. Nutrients make these plant tissues
more resistant and with thicker cellular walls which could affect
the feeding preference and increase the resistance to the insects
[49,50]. The UV radiation could increase the tannin accumulation
in the lumen and the phenols in the epidermal cells. These factors
make the epidermal cells thicker, although with a smaller
mesophyll area, suggesting that more carbon is allocated as a
protective mechanism with the lower photosynthetic rate [51].
This indicates that the occurrence of these factors and the reduced
number of winged aphids on the plants grown or maintained in
the mulched plots may be caused by an indirect effect of the UV
light reflectance [4,52]. The inorganic mulch reflects the short-
wave UV light [53], which confuses and repel the incoming
winged aphids, thus reducing their incidence on the plants [11].
Although the impact of the short-wave light to repel the whiteflies
was not conclusive, these insects may respond similarly to those of
the winged M. persicae approaching the reflective (Al) surfaces [54].
The mulch can influence the concentrations of the carbohydrates
and soluble sugars in the kale plants [55], which may have reduced
the number of aphids probably due the production of semio-
chemicals.
The reduction in the M. persicae population by the mulch helps
to explain the effect of light reflectance. This parameter was not
evaluated. However, the UV was responsible as seen by the lesser
number of aphids landing on the kale plants [56] and the
temperature increased in the cantaloupe, Cucumis melo var.
cantalupensis Naudin (Cucurbitaceae) and tulip, Tulipa sp. (Liliaceae)
plants on the mulched soil [54]. Temperatures between 25–30uC
increased the population growth of the cotton aphid, Aphis gossypii
Glover, 1887; the turnip aphid, Lipaphis erysimi Kaltenbach, 1843
(Hemiptera: Aphididae) and the M. persicae on the cotton,
Gossypium hirsutum L. (Malvaceae) and citrus, Citrus sp. (Rutaceae)
[57,58], but temperatures above 30uC reduced their populations
[59]. This shows that the higher temperatures in the mulched
plots, probably, may have reduced the population growth of M.
persicae during the 15-day period. Besides, the temperature
influences the synthesis of the acyclic polyol (mannitol), common
in most animals, but registered only for a few insects [60]. The
healthy polyols also protect the proteins against denaturation at
high temperatures [61]. The aphids may adapt to the high
temperatures by accumulating the polyhydric alcohols in their
hemolymph, as observed for mannitol in the greenflies (Hemip-
tera: Aphidoidea) [62]. The synthesis of these compounds is
stimulated by high temperatures. They are not excreted by the
aphids; they accumulate in the hemolymph and thus act as a
thermo protective mechanism [62]. However, the aphids may not
synthesize the mannitol due to the high energy expense and for
this reason show a preference for plants with lower temperatures.
The rice-straw mulch decreased the number of winged aphids
landing on the kale plants and the growth of this insect colony,
which concurs with the lower aphid populations and the reduced
Figure 4. Number of winged adults+nymphs of green peach aphid,
Myzus persicae
(Hemiptera: Aphididae) on kale,
Brassica oleracea
var.
acephala
(Brassicaceae) leaves on mulch and no mulched plots after 15 days of infestation. Poisson error and x2 of Pearson to
correct over dispersion followed by an F test at 5% probability.
doi:10.1371/journal.pone.0094174.g004
Rice-Straw Mulch Reduces Aphid on Kale
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incidence of the aphid-borne viruses on the wheat, Triticum aestivum
L. (Poaceae) and rice plants on mulched soil [4,63,64]. The
incidence of the Cucumber mosaic virus (CMV) Cucumovirus (Bromo-
viridae) on the narrow-leafed lupins, Lupinus angustifolius L.
(Fabaceae) and the Bean yellow mosaic virus (BYMV) Potyvirus
(Potyviridae) on cereal straw was lower than in the bare soil in
Australia. This was explained by the lower occurrence of the virus
with a decreasing incidence of the winged aphids landing [65].
The increasing UV reflectance of the backgrounds decreased Aphis
spp. and M. persicae landing on the B. brassica plants with a negative
correlation of this parameter with the aphid numbers [11]. Straw
mulch, therefore, reduced the populations and the numbers of this
aphid on the green traps want confirms results obtained in potato
[66] and faba beans, Vicia faba L. (Fabaceae) [67].
Conclusions
The lower number of winged M. persicae landing and the better
vegetative development of the kale plants may be explained by the
higher temperature in the mulched plots, as well as to the
physiological changes of the kale plants. Besides, the soil covering
may reduce the winged M. persicae to find the kale plants. The
strategy using rice-straw mulch presents a potential to be used in
integrated aphid management in the kale plantations.
Acknowledgments
Global Edico Services of India edited and proofread this manuscript.
Author Contributions
Conceived and designed the experiments: RS-F RHSS GLDL JES JCZ.
Performed the experiments: RS-F WST CFW. Analyzed the data: RS-F
RHSS GLDL. Contributed reagents/materials/analysis tools: RS-F RHSS
GLDL JES JCZ. Wrote the paper: RS-F RHSS WST GLDL CFW JES
JCZ.
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