Vol. 11(29), pp. 2630-2639, 21 July, 2016
Article Number: 637C69059568
Author(s) retain the copyright of this article
African Journal of Agricultural
Full Length Research Paper
Companion plants associated with kale increase the
abundance and species richness of the natural-enemies
of Lipaphis erysimi (Kaltenbach) (Hemiptera:
Valkíria Fabiana D.A. Silva1*, Luís Cláudio Paterno Silveira2, Alexandre dos Santos3, Adriano
Jorge Nunes dos Santos3 and Vitor Barrile Tomazella4
1Department of Agronomy, Federal University of Lavras-UFLA/DAG, Lavras, MG, Brazil.
2Department of Entomology, Federal University of Lavras -UFLA/DEN, Lavras, MG, Brazil.
3Department of Forest Engineering, Federal Institute of Mato Grosso, Cáceres, MT, Brazil.
4Laboratory of Entomology, Embrapa Milho e Sorgo, Sete Lagoas, MG, Brazil.
Received 25 February, 2016; Accepted 2 June, 2016
The effects of intercropping of Brassicaceae with coriander (Coriandrum sativum), dill (Anethum
graveolens), African marigold (Tagetes erecta) and calendula (Calendula officinalis) on the abundance,
species richness and diversity of predators and parasitoids of Lipaphis erysimi have been assessed.
The numbers of aphids, parasitized aphids and natural enemies were determined during two
consecutive phases. The first period comprised the vegetative phase of companion plants up to the
onset of flowering and the development of kale up to the start of harvesting, while the second period
encompassed the late flowering of companion plants up to senescence and the complete harvesting
phase of kale. The establishment of L. erysimi and its natural enemies during the first period was
enhanced by the climatic conditions and the additional nutritional resources offered by companion
plants. Over the complete 13 week period, the abundance of natural enemies in kale intercropped with
African marigold, calendula, coriander and dill increased by factors of 3.1, 2.1, 2.0 and 1.6, respectively,
compared with the kale monoculture, while species richness increased by 1.8-fold in kale/African
marigold intercrop and by a factor of 2.7 in the other treatments. The predominant predators were
Syrphidae larvae and Hippodamia convergens whereas the predominant parasitoid was Diaeretiella
rapae. The diversity of natural enemies was similar in all crops owing to the high proportion of syrphids
in relation to the other groups of insects. The improved resources offered by companion plants can be
exploited in the conservative biological control of insect pests.
Key words: Conservation biological control, natural enemies, insect seasonality, Hemiptera, Aphididae,
Asteraceae, Apiaceae, Lipaphis erysimi, abundance, richness, Syrphidae, ladybird, kale
Increasing plant diversity within an agriculture-dominated
landscape can bestow a setting approximating to that of
the natural environment. Diversification may also serve to
increase the abundance of beneficial insects by providing
increased floral resources, alternative prey and hosts, and
additional sites for hibernation, mating and oviposition
for natural enemies of crop pests (Alignier et al., 2014).
Implementation of an organic production system
coupled with diversification represents an alternative
strategy to the use of insecticides for regulating insect
communities. Indeed, the expansion and intensification of
monoculture farming has been considered one of the
main factors responsible for loss of arthropod diversity
around the globe (Altieri, 2009; Welch and Harwood,
2014). While the selection of appropriate companion
plants for successful management of agricultural
landscapes is important, relatively few studies have
focused on the influence of habitat on the relationship
between insect pests and their natural enemies (Chaplin-
Kramer and Kremen, 2012).
Kale (Brassica oleracea L. var. acephala D. C.) is one
of the most popular vegetables in Brazil, and is of
considerable economic importance, especially to small-
scale farmers, so we use this plant as a model, however
Lipaphis erysimi (Kaltenbach, 1843) (Hemiptera:
Aphididae) being one of the most important pests of
brassicas on the world. Kale and other species of
brassicas crops throughout the world are constantly
plagued by L. erysimi, a specialist brassica aphid that not
only attacks the terminal portions of stems and
inflorescences, causing curling and yellowing of the plant,
but also acts as a vector for phytopathogenic viruses
(Blande et al., 2008).
A number of reports are available concerning the
impact of diversification on the population dynamics of
insect communities associated with brassica crops
(Hooks and Johnson, 2003). It is known that the
intercropping of food crops with flowering species of the
families Asteraceae and Apiaceae can enhance the
efficiency of pest predators by increasing their longevity,
fecundity, colonization and permanence in the cropping
system (Walton and Isaacs, 2011).
Members of the Asteraceae have been shown to
maintain the biodiversity of predators and parasitoids
when employed as a companion crop in onion fields
(Silveira et al., 2009). Regarding the Apiaceae, aromatic
species attract numerous insects that forage for pollen
and nectar, while the floral architecture provides shelter
for prey and/or preferential or alternative hosts. The
bright yellow color of the flowers and the nutritional value
of the pollen are highly attractive to ladybirds and wasps,
while the floral architecture is compatible with the head
morphology and foraging behavior of the coccinellids
(Patt et al., 1997; Walton and Isaacs, 2011).
Considering the beneficial effects that companion
flowering species may have in the suppression of crop
pests, we propose that intercropping kale with species of
Silva et al. 2631
Apiaceae or Asteraceae in an organic culture system
would increase the attraction and permanence of natural
enemies of the aphid L. erysimi. In order to test this
hypothesis, we evaluated the effect of intercropping kale
with African marigold, calendula, coriander or dill on the
abundance, species richness and diversity of aphid
predators and parasitoids.
MATERIALS AND METHODS
The experiment was carried out between March and June 2012 at
the organic crops research station of the Universidade Federal de
Lavras (UFLA) (21°14’43” S; 44°59’59” W; 930 m altitude). The fully
randomized block design consisted of five treatments, with five
replications each, and involved 25 plots (4 x 1.7 m) comprising kale
monoculture (control) and kale intercropped with African marigold,
calendula, coriander or dill. Seeds of kale and the companion plants
were germinated in a greenhouse in separate polystyrene trays
(200 cells per tray) containing commercial Plantmax® substrate
(Eucatex Agro, Paulínia, SP, Brazil), and transplanted to the
experimental plots 30 days after germination. The soil in the plots
was analyzed prior to experimentation and found to contain 11.05
mg dm-3 of P, 84 mg dm-3 of K, 3.30 cmolc dm-3 of Ca2+ and 1.00
cmolc dm-3 of Mg2+.
In each of the plots, kale was arranged in five rows with three
plants each (15 plants/plot) spaced 1.0 m between rows and 0.8 m
between plants. Companion plants were arranged between the
rows of kale, with each of the four rows containing four plants (16
plants/plot) spaced 0.4 m from one another. The applicable plot
was considered to be the three central rows containing nine kale
plants. Plots within a block were separated by 1.5 m weed-free
aisles, and blocks were separated by pathways (1.0 m wide). The
soil was covered with plastic mulch to suppress weeds that could
interfere with the results and to conserve humidity, and the plants
were irrigated daily by sprinkler irrigation aspersion. Meteorological
data (monthly mean temperature and relative humidity and monthly
accumulated rainfall) were collected at the weather station at the
UFLA determined throughout the experimental period.
Determination of the numbers of aphids, parasitized aphids and
natural enemies present in the kale crops commenced 20 days
after transplanting seedlings to plots. Sampling was performed
weekly in the morning over a period of 13 weeks until senescence
of the companion plants. In order to facilitate evaluation of the
fluctuating populations of insects, the sampling period was divided
in two stages. The first period (P1) extended from 26th March to the
7th May and covered the vegetative stage of the companion plants
up to full flowering, and the development of the kale up to the start
of harvesting. During this period, six observations were performed,
one at the end of March, four in April and one at the beginning of
May. The second period (P2) extended from 17th May to 22nd
June, and covered the late flowering of companion plants up to their
*Corresponding author. E-mail:firstname.lastname@example.org.
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2632 Afr. J. Agric. Res.
senescence and the complete harvesting phase of the kale. During
this period, seven observations were carried out, four in May and
three in June.
Since collection and counting procedures at each sampling were
carried out on the same plants, the predators and parasitoids had to
be removed before counting the aphids and collecting the
parasitized aphids (mummies) in order to avoid dispersion of the
natural enemies. Predators and parasitoids of L. erysimi were
collected from three randomly selected plants in each plot (75
plants/week) using a manual aspirator and brush on each whole
plant for 5 min. The insects were subsequently transported to the
laboratory for counting and identification. Adult insects were placed
in acrylic flasks containing 70% ethanol, while immature insects
were transferred to Petri dishes containing L. erysimi-infested kale
leaves and incubated at 241°C and 7010% relative humidity
under a 12 h photoperiod until they matured into adults. Taxonomic
classification of insect predators was carried out with the aid of
specific dichotomous identification keys.
The numbers of aphids present on leaves from plants that had
been previously sampled for the presence of natural enemies were
determined with the aid of a manual counter. In order to ensure
consistency of sampling, leaves were classified as:
Apical – young leaf not fully expanded
Median – adult and fully expanded leaf; and
Basal - senescent leaf with visible yellowing.
One leaf of each type was selected randomly from each plant prior
to visualization of aphids on the abaxial side. After counting,
mummies were collected from the same leaves.
Analyses were performed using R software (R Development Core
Team 2014) with the level of statistical significance set at 5%. The
effects of sampling period (P1 and P2) and treatments (explanatory
variables) on the numbers of predators, parasitoids, aphids and
mummies (response variables) were evaluated by analysis of
variance (ANOVA) and regression analysis using generalized linear
models with Poisson distribution errors and chi-square test (p<0.05)
(Buckley et al., 2003; Crawley, 2005).
Subsequently, non-significant qualitative terms for kale
monoculture (control) and kale intercropped with African marigold,
calendula, coriander or dill factors were compared by contrasts, in
order to establish similarities between treatments in the full model.
The ecological parameters (n, S and H’) were calculated using
PAST software version 2.04 (Hammer et al., 2001), tested for
homogeneity of variance, and analyzed by ANOVA and Kruskal-
The true number of species or species richness (S) in relation to the
observed number of species (S0) was established using the
Jackknife estimator. The Shannon-Wiener diversity index (H´; range
0 - 5) was used to characterize diversity since it combines species
richness and abundance.
Influence of sampling time and treatments on the
population of aphids and natural enemies
The study periods P1 and P2 showed significant effects
on the population of L. erysimi over time (χ2 = 54215.0; P
< 0.00001), with the highest incidence of aphids being
observed during P1 (Figure 1). Moreover, the incidence
of L. erysimi was significantly lower (χ2= 73.52705; P <
0.00001) in the treatment pair kale monoculture x kale/dill
compared with the pair kale/coriander x kale/calendula
(Figure 1). The kale/African marigold intercrop resulted in
a lower incidence of aphids in comparison with others
treatments (153.74; p < 0.00001), and the highest
incidence was observed during P1 coinciding with the
period in which the population of predators was lower
In contrast, the study periods did not exhibit significant
influence on the population of parasitoids (χ2= 7.5815; P
= 0.10817) or the occurrence of mummies (χ2 = 2.7910; P
= 0.09479) over time. Comparison of treatment pairs
revealed that the incidence of predators was significantly
higher (χ2 = 24.09329; p < 0.00001) in the treatment pair
kale monoculture x kale/dill compared with the pair
kale/coriander x kale/calendula (Figure 2). However, the
kale/African marigold intercrop resulted in a higher
incidence of predators in comparison with the other two
treatment pairs (χ2 = 94.71723; P < 0.00001).
Considering the two sampling periods together, the
incidence of parasitoids was not significantly influenced
by the treatments (χ2= 7.5815; P = 0.1082), although the
numbers of parasitized aphids were affected significantly
(χ2 = 23.8320; P < 0.00001). The number of parasitized
aphids was highest in the kale/African marigold intercrop
followed by the kale/calendula intercrop (Figure 3).
Influence of climatic conditions on the aphid
The mean temperature during P1 (March and April) was
around 21°C, and the mean rainfall was approximately 39
mm with 75% relative humidity. During P2, average
temperatures decreased to 17°C (May) and 18°C (June),
and precipitation increased to 42 mm (May) and 95 mm
(June) with 84% relative humidity. As shown in Figure 4,
the percentage of aphids diminished markedly from P1 to
P2 as the temperature decreased, and the humidity
Evaluation of the ecological parameters
The abundances of various groups of natural enemies of
aphids observed in kale crops during the period of March
to June, 2012 are presented in Table 1. Larvae of
aphidophagous Syrphidae (Diptera) were predominant in
all treatments, particularly in the kale monoculture where
the richness of species was markedly lower than in all
other treatments and hoverflies accounted for 62.1% of
all specimens collected. Hippodamia convergens
Silva et al. 2633
Figure 1. Mean numbers of L. erysimi aphids observed in kale crops during the
sampling periods from 26 March to 7 May (P1) and from 17 May to 22 June (P2) 2012.
Figure 2. Mean numbers of predators observed in kale crops during
the sampling periods from 26 March to 7 May (P1) and from 17 May
to 22 June (P2) 2012.
2634 Afr. J. Agric. Res.
Figure 2. Mean numbers of predators observed in kale crops during the sampling
periods from 26 March to 7 May (P1) and from 17 May to 22 June (P2) 2012.
(Guérin-Méneville, 1842) was also observed in all
treatments, but the frequency was considerably higher in
the kale/African marigold intercrop where the convergent
lady beetle accounted for 21.1% of all natural enemies
Parasitoid wasps accounted for around 10% of the
natural enemies of aphids identified in the kale crops and
included Diaeretiella rapae (McIntosh, 1855), which was
present in all crop treatments and accounted for 89.6% of
all parasitoids collected, Aphidius colemani (Viereck,
1912) (8.62%) and Praon volucre (Haliday, 1833)
(1.72%) (Table 1). The highest abundance of D. rapae
was observed in the kale/dill intercrop with 18 individuals
Regarding the overall abundance (n) of natural
enemies, significantly more beneficial insects were
observed in the kale/African marigold, then Kale/
Calendula intercrop in comparison with the other
treatments (Table 2). Species richness (S) in the kale
monoculture was considerably lower in comparison with
those of the intercrops, but no statistically significant
between-treatment differences were observed in the
Shannon-Wiener diversity index (H’).
Factors that are intrinsic to the host plant, especially
those related to nutritional quality, influence the
colonization and performance of phytophagous insects.
For example, the reproductive rate of aphids is associated
positively with the amounts of nitrogen in the plant
(Zarghami et al., 2010) and these, along with the levels of
proteins and carbohydrates, vary as the plant matures
(Staley et al., 2011). In the present study, the colonization
of kale plants by L. erysimi was markedly higher in P1
than in P2 (Figure 1), a finding that probably reflects the
greater concentrations of soluble nitrogen translocated
through the phloem in the young leaves of P1 compared
with the old leaves of P2. According to Agarwal and Datta
(1999), young leaves of mustard greens (Brassica
juncea) are of superior nutritional quality in comparison
with older leaves and, therefore, support the highest rates
of fecundity and survival of L.
Silva et al. 2635
Figure 4. Variation in L. erysimi aphid population, rainfall, temperature and
relative humidity during the whole sampling period of March to June 2012.
In the present study, the highest density of natural
enemies of L. erysimi, particularly predators, was
maximal in P1, the period during which the companion
plants attained full bloom and the aphid population was at
its highest level. During the flowering stage, members of
the Apiaceae and Asteraceae are very attractive to the
natural enemies of aphids, and the favorable dietary
conditions serve to enhance the longevity, fecundity and
preying capacity of beneficial insects (Walton and Isaacs,
2011) and, as a consequence, the aphid population tends
Evaluation of the influence of treatments on the
populations of aphids and their natural enemies during
the crop cycle revealed that the kale/African marigold and
Kale/Calendula intercrop attracted more predators than
the other intercrop and also exhibited the lowest
incidence of aphids (Figure 1). This is a promising result
2636 Afr. J. Agric. Res.
Table 1. Abundance (n) of natural enemies of L. erysimi observed in kale monoculture and kale intercropped with companion plants during the whole sampling
period of March to June 2012.
Kale intercropped with companion plants
Silva et al. 2637
Table 2. Abundance (n), species richness (S) and Shannon-Wiener diversity index (H’) of
natural enemies of L. erysimi observed in kale monoculture and kale intercropped with
companion plants during the whole sampling period of March to June 2012.
1 Mean values of n bearing the same superscript letter are not significantly different (Tukey test; P >
0.02); 2 Mean values of H’ are not significantly different (Kruskal-Wallis test; P > 0.05).
considering that the counting of natural enemies was
performed on the kale plants themselves where predatory
action against the aphids was more likely to occur.
Silveira et al. (2009) demonstrated that African marigolds
offer conditions that favor the maintenance of natural
enemies of onion pests. Climatic conditions have been
shown to influence the density of L. erysimi (Bapuji Rao
et al., 2013).
Landin and Wennergren (1987) studied the intrinsic
rate of increase of L. erysimi under different temperatures
and concluded that the highest growth rate occurred
around 25°C, while Bakhetia and Sidhu (1983)
established that temperatures within the range 20 to 30°C
favored the development and reproduction of the aphid.
In the present study, the mean temperature of 21°C
recorded during P1 probably contributed to the high
incidence of aphids observed on kale crops during the
first study period. Increased precipitation, which is
considered to be a natural mortality factor of L. erysimi
(Dogra et al., 2001), coupled with the reduced
temperatures (17 to 18°C) registered during P2 were
partly responsible for the increased aphid mortality
observed during second study period. In contrast, relative
humidity varied little between P1 and P2 (75 and 84%,
respectively), and these levels were within the 75 to 85%
range cited by Kulat et al. (1997) as favorable for the
presence of L. erysimi in the field.
It is concluded, therefore, that relative humidity alone
was not a factor in determining the variation in population
size of the aphids during the kale cropping cycle.
Meteorological data gathered during the crop cycle are
also important since climatic conditions may constitute a
decisive factor in determining the timing of absence or
peak infestations of aphids in the field (Chattopadhyay et
In the present study, predators predominated over
parasitoids throughout the crop cycle. According Venzon
et al. (2013) predators can benefit not only from the floral
resources of the companion plants but also from the that
allowed them to survive longer in the field, a factor that is
particularly important when pest density is low. Most of
the sampled predators were generalists or
zoophytophagous (that is, spiders, syrphids, ladybird
beetles and thrips) and were prevalent from the start of
the culture period until the senescence of the companion
plants. The main advantage of generalist predators is
their ability to colonize an agro-ecosystem before the
arrival of the primary pests and to remain in the field
throughout the crop cycle by feeding on alternative prey
(Aguiar-Menezes, 2003; Amaral et al., 2013).
Nevertheless, the results indicate that the density of
predators accompanied changes in the phenology of the
plants but that S was greater than S0, most likely because
the experiment was field-based and predators constantly
appeared from the surrounding areas.
The three species of parasitoids observed were host-
specific and all belonged to the Aphidiinae subfamily of
parasitic wasps (Starý et al., 2007). This specificity
explains the decrease in parasitoid density during P2,
which occurred because of the decline in the L. erysimi
population within this period (Figure 4). The results
obtained herein indicate that the relative abundance and
species richness of the natural enemies of L. erysimi vary
according to the phenology (vegetative, flowering and
senescence phases) of the companion plants, thus
confirming previous reports relating to species of the
families Asteraceae and Apiaceae (Silveira et al., 2009;
Resende et al., 2012). In general, insect populations
change over time according to the availability of food
resources, microclimate and shelter offered by the host
plants, and these elements clearly favored the continuous
richness and addition of species during the present study.
In the present study, although the highest number of
specimens of natural enemies was collected in the
kale/African marigold intercrop (n = 174), species
diversity was similar in all treatments as shown by the H’
values (Table 2). This result was due to the high number
of coccinellids, particularly H. convergens, which were
present in all intercrops but mainly in the kale/African
marigold treatment. A study conducted by Medeiros et al.
(2010) demonstrated that the most common pollen grains
found in populations of H. convergens within and around
2638 Afr. J. Agric. Res.
horticultural areas derived from members of the
Asteraceae, thereby showing the importance of pollen as
a food resource for these beneficial insects in a
conservative biological control program. In contrast to the
intercrop treatments, the kale monoculture presented a
low S value with only 69 specimens collected, a finding
that may be explained by the absence of extra food
resources and the predominance of Syrphidae larvae
Although the other treatments also presented a
preponderance of these larvae, there was greater
homogeneity in the overall distribution of natural enemies
compared with the kale monoculture. Syrphidae larvae
were observed during the entire experimental period and
their permanence in the kale monoculture and intercrops
was favored by the constant presence of L. erysimi. The
predator-prey dependency between aphidophagous
Syrphidae and aphids observed in this study is also
noteworthy. Tenhumberg and Poehling (1992)
demonstrated that syrphids are sensitive to reduction in
the aphid population, and examples of predator-prey
dependency have been described involving larvae of
Aphidoletes sp. and L. erysimi in cabbage crops (Silva et
al., 2011). It is possible to infer that the permanence of
syrphids in the present study depended on the presence
of L. erysimi, since the density of these predators was
associated with the density of aphids in the kale crops.
Clearly, predator-prey interactions must be taken into
account during the evaluation of the abundance of insect
groups in field cultures, while the understanding of this
relationship is very important for devising biological
The attraction of syrphids towards Apiaceae plants has
been widely investigated, and floral structure is
considered to be one of the key factors. The morphology
of flowers of the Apiaceae is compatible with the short
mouthparts of adult Syrphidae hoverflies, thus facilitating
access to nectar and pollen (Morales and Köhler, 2008).
Flowers of the Asteraceae, including marigold species,
are also attractive to syrphids, as verified by Robertson
(1929), who reported that 25% of the 257 species of this
family serve as hosts for hoverflies, and by Sajjad and
Saeed (2010) who established that the Asteraceae is
one of the families most visited by Syrphidae.
In the present study, D. rapae was the most abundant
of the three species of parasitoids and was present in all
treatments, especially in the kale/dill intercrop. The
exposed nectaries of dill flowers emit odors that attract
adult parasitoid species and the floral architecture
facilitates their feeding behavior (Patt et al., 1997). The
results of the present study indicate that the factors
influencing the dynamics of multitrophic interactions
present in an agro-ecosystem should be considered
when assessing the population patterns of the pests and
their natural enemies. However, the influence of climatic
factors and the structure of the local landscape on the
dynamics of arthropod populations require further
elucidation in order to establish plant associations that
would confer extra benefits to the main crop through the
response of herbivores and their natural enemies.
The results presented herein revealed that establishment
of L. erysimi and its natural enemies in kale crops were
influenced by the climatic conditions and nutritional
resources of the host plant. The abundance of natural
enemies in kale intercropped with African marigold,
calendula, coriander and dill increased by factors of 3.1,
2.1, 2.0 and 1.6, respectively, in comparison with the kale
monoculture, while species richness increased 1.8-fold in
kale/African marigold intercrop and by a factor of 2.7 in
the other three intercrops. The data presented in this
study support the original hypothesis that intercropping
kale with Apiaceae or Asteraceae species in an organic
culture system increases the attraction and permanence
of the natural enemies of L. erysimi by virtue of the
improved resources offered to these beneficial insects.
Moreover, the information collected will be used to
forecast the period when kale crops in the study area are
more susceptible to the attack of pests, and to make
suitable management decisions to reduce pest
populations in a planned manner, that is, by configuring
the kale crop and companion plants in such a way that
natural enemies are attracted during the critical phase.
Conflict of Interests
The authors have not declared any conflict of interests.
The authors wish to thank Universidade Federal de
Lavras and Conselho Nacional de Desenvolvimento
Científico e Tecnológico (CNPq) for financial support to
the study and scholarship awarded to one of us (VFS).
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