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Effects of agricultural intensification on
ability of natural enemies to control
aphids
Zi-Hua Zhao
1
, Cang Hui
2,3
, Da-Han He
4
& Bai-Lian Li
5,6
1
Department of Entomology, College of Agriculture and Biotechnology, China Agricultura l University. Beijing 100193, P. R. China,
2
Centre for Invasion Biology, Department of Mathematical Sciences, Stellenbosch University, Matieland 7602, South Africa,
3
Mathematical and Physical Biosciences, African Institute for Mathematical Sciences, Muizenberg 7945, South Africa,
4
College of
Agronomy, Ningxia University, Yinchuan 750021, China,
5
Ecological Complexity and Modeling Laboratory, Department of
Botany and Plant Sciences, University of California, Riverside, CA 92521-0124, USA,
6
USDA-China MOST Joint Research Center
for AgroEcology and Sustainability, University of California, Riverside, CA 92521, USA.
Agricultural intensification through increasing fertilization input and cropland expansion has caused rapid
loss of semi-natural habitats and the subsequent loss of natural enemies of agricultural pests. It is however
extremely difficult to disentangle the effects of agricultural intensification on arthropod communities at
multiple spatial scales. Based on a two-year study of seventeen 1500 m-radius sites, we analyzed the relative
importance of nitrogen input and cropland expansion on cereal aphids and their natural enemies. Both the
input of nitrogen fertilizer and cropland expansion benefited cereal aphids more than primary parasitoids
and leaf-dwelling predators, while suppressing ground-dwelling predators, leading to an disturbance of the
interspecific relationship. The responses of natural enemies to cropland expansion were asymmetric and
species-specific, with an increase of primary parasitism but a decline of predator/pest ratio with the
increasing nitrogen input. As such, agricultural intensification (increasing nitrogen fertilizer and cropland
expansion) can destabilize the interspecific relationship and lead to biodiversity loss. To this end,
sustainable pest management needs to balance the benefit and cost of agricultural intensification and restore
biocontrol service through proliferating the role of natural enemies at multiple scales.
In agroecosystem, arthropods provide important ecosystem services due to their abundance and diversity; such
service can be sustained and even enhanced by conserving semi-natural and natural habitats within agricul-
tural landscapes
1,2
. This is because many arthropod species are very mobile and need to cross multiple habitats,
including both crop and semi-natural habitats, for food and refuge
3,4
. Indeed, heterogeneous landscapes with a
high proportion of semi-natural habitats can sustain a high diversity of aphid natural enemies including specia-
lists and generalists, a prerequisite for effective biocontrol
5,6
. As such, the provision of arthropod ecosystem
service in croplands is sensitive to resource availability in surrounding semi-natural habitats
7
.
Agricultural intensification, through increasing fertilization input within fields and cropland expansion at
landscape scales, is considered a key driver of biodiversity loss and the decline of ecosystem services
8
. To this end,
habitat management which optimizes the effect of agricultural landscape structure on the efficacy of biological
control of agricultural pests has become a new paradigm for sustainable pest management
7,9
. At the field scale,
agrochemical inputs can have great impacts on arthropod communities through changing plant nutrition,
resulting in a rapid biodiversity loss in agroecosystems
10–12
. Increasing fertilizer input within fields affects insects
differently due to the asymmetric responses of different species to changing host nutrition. Phytophagous insects,
which have a relatively rapid developmental rate in high-nutrition plants, are more sensitive to changes in host
nutrition than their natural enemies
13
. Changes in plant nitrogen availability could trigger a bottom-up effect on
insect survival and the interaction between insect herbivores and pathogenic fungi
14,15
. At the landscape scale,
cropland expansion (increasing the proportion of cropland in agricultural landscapes) has been shown to
negatively affect biocontrol efficacy by disproportionally harming the natural enemies of agricultural pests
16,17
.
The effects of landscape structure on pest populations can vary with spatial scale; that is, habitat management
should be prioritized at a specific spatial scale
7,18,19
. The negative effect of agricultural intensification on biocontrol
often peaks at a specific spatial scale
20
. As such, habitat management is proven here to be most effective at the
optimal spatial scale while making little contribution at other spatial scales
21
. Moreover, the response of arthro-
OPEN
SUBJECT AREAS:
AGROECOLOGY
ZOOLOGY
Received
11 November 2014
Accepted
31 December 2014
Published
26 January 2015
Correspondence and
requests for materials
should be addressed to
Z.-H.Z. (zhzhao@cau.
edu.cn)
SCIENTIFIC REPORTS | 5 : 8024 | DOI: 10.1038/srep08024 1
pods to landscape structures could also be scale dependent due to
species-specific dispersal ability. For species with strong dispersal
ability (e.g. flying predators such as hover flies, lady beetles, and
lacewings), habitat management should target large spatial scales,
while improving local habitat quality can enhance the activity of
species with weak dispersal ability (e.g. walking predators such as
spiders and Carabid beetles). For example, the species diversity and
abundance of ground-dwelling arthropods could increase after
planting grass strips every 200 m, supplying alterative food resources
and refuge for these natural enemies
9,22
. These grass strips can act as
banker plants which release the natural enemy when pest popula-
tions increase in crop fields and conserve them after harvest
23
. Some
field experiments have examined the effects of landscape complexity
on predation and parasitism at either the field or landscape scales, but
to date studies have not examined both scales concurrently
24
.
Higher levels of ecosystem service provision are sometimes
achieved through interactions of species from different functional
groups
25
, making assessing the effects of agricultural intensification
rather challenging. Many arthropod species belong to different func-
tional modules in the insect community of wheat fields (e.g. cereal
aphid, predator, and parasitic wasp), forming complicated food
webs
11
. Therefore, landscape modification differentially benefits
some species over others, complicating the biocontrol of cereal
aphids by their natural enemies
26,27
. To date, most research has been
conducted for specific insect modules at one particular scale,
emphasizing the need for experiments at multiple scales and target-
ing multiple functional modules
11
.
Here, we conducted a field experiment of collecting cereal aphids
and their natural enemies of different functional modules in
Northwest China to elucidate the effects of agricultural intensifica-
tion at both field and landscape scales. Based on empirical evidence
and existing hypotheses in the literature, we specifically addressed
two research questions: i) whether the effects of agricultural intensi-
fication on population and community structures differ at the field
and landscape scale; ii) the potential mechanism behind the scale
dependence of the effects of agricultural intensification (increasing
fertilizer input and cropland expansion) on agricultural arthropods.
Results
Effect of nitrogen fertilizer.In the experiment, the amount of
nitrogen fertilizer ranged from 115.8 kg/ha to 170.6 kg/ha while
the proportion of cropland ranged from 63.73% to 90.25% (see
supplementary Table S1). In total, we collected 24,672 individuals
including 19,723 cereal aphids, 3,679 primary parasitoids, 843 leaf-
ground predators, and 427 ground-dwelling predators.
All selected species (two species in each functional group) were
significantly affected by the increasing input of nitrogen fertilizer
within the sampled fields (Figure 1, see supplementary Table S2).
Specifically, the increasing input of nitrogen fertilizer led to the
increase of the population densities of cereal aphids, their primary
parasitoids, and leaf-dwelling predators. The correlation coefficient
between population density and nitrogen input ranged from 0.3365
(Syrphus nitens) to 0.8653 (Aphidius gifuensis), showing different
sensitivity to applying nitrogen fertilizer within the field (e.g. a pos-
itive correlation for primary parasitoids, in contrast to a negative
correlation for ground-dwelling predators; Figure 1, see supplement-
ary Table S2). The abundance of cereal aphids increased more rapidly
than their natural enemies in response to the increasing input of
nitrogen fertilizer, followed by the primary parasitoids (Figure 1,
see supplementary Table S2), indicating a weakening effect of bio-
control service from applying nitrogen fertilizer within the field in
agroecosystems.
Effect of cropland expansion.At the population level, agricultural
intensification (AI) caused by increasing proportion of cropland has
a positive effect on the abundance of cereal aphids at all spatial scales
except when measured at the broadest scale (1500 m; Figure 2, see
supplementary Table S3). The correlation coefficients between the
proportion of cropland and the population densities of the two aphid
species (Sitobion avenae and Schizaphis graminum) peaked at the
scales of 800 m and 200 m, respectively. Furthermore, the
correlation coefficients for primary parasitoids and leaf-dwelling
predators were positive, which peaked at the scales of 200 m and
500 m. In contrast, the correlation coefficients became negative for
ground-dwelling predators (see supplementary Table S3). Overall, at
broad scales increasing proportion of cropland had a positive effect
on cereal aphids, leaf-dwelling predators and primary parasitoids but
had a negative effect on ground-dwelling predators (Figure 2, see
supplementary Table S3). Moreover, the response of cereal aphids
and their natural enemies to cropland expansion was species specific.
The parasitic wasps were more sensitive than cereal aphids to
cropland expansion across multiple scales, while even species
within the same module (e.g. the two leaf-dwelling predators, H.
variegata and S. nitens) responded differently (Figure 2, see
supplementary Table S3).
Impact on biocontrol and diversity.At the community level, the
increasing input of nitrogen fertilizer significantly enhanced the
primary parasitism in wheat field (F
1,101
56.31, P50.013,
Figure 3A) but negatively affected the predator/pest ratio (Leaf-
dwelling predator: F
1,101
54.29, P50.041; Ground-dwelling
predator: F
1,101
58.11, P50.005, Figure 3B, C). The increasing
input of nitrogen fertilizer was also detrimental to the species
diversity of natural enemies in the wheat field (F
1,101
57.72, P5
0.006, Figure 3D).
Moreover, we selected the scale of 500 m to examine the effects of
the proportion of cropland on predation and parasitism, showing an
insignificant effect on primary parasitism (F
1,101
52.36, P50.127,
Figure 4A) but a negative effect on the predator/pest ratio (Leaf-
dwelling predators: F
1,101
55.58, P50.020; Ground-dwelling pre-
dators: F
1,101
56.97, P50.010, Figure 4B, C) and a negative effect on
the species diversity of natural enemies (F
1,101
56.61, P50.012,
Figure 4D).
Discussion
Differential responses to agricultural intensification.Our results
show that the input of nitrogen fertilizer facilitates the cereal aphid
populations. Surprisingly, increasing nitrogen input did not suppress
the activity of parasitic wasps; rather, it slightly increased the
parasitism of cereal aphids, contrasting the result from Lohaus
et al. (2013) that the parasitism of cereal aphids showed no
difference between conventional and organic wheat fields
28
.
However, the density of cereal aphids still increased with the input
of nitrogen fertilizer due perhaps to the rapid development of cereal
aphids in high-nitrogen wheat fields
29
. As such, cereal aphids were
not controlled by the high parasitism driven by the high nitrogen
input. Other possible reasons include that species at the higher
trophic level (hyperparasitoids) may also gain benefits from
nitrogen input and pose a top-down interference to the interaction
between cereal aphids and their primary parasitoids
27,30
. These
results suggest that several modules (parasitoids, leaf- and ground-
dwelling predators) can have strong complementary effects on the
biological control of cereal aphids in wheat fields
6,11,31
.
Landscape simplification (i.e. a high percentage of arable lands in
agricultural landscapes or homogeneous landscape structure) can
have a negative effect on biological control of cereal aphids
32,33
.
Here, the correlation between the percentage of arable lands in the
agricultural landscape and parasitism decreased as the spatial scale
increases, suggesting that parasitic wasps might respond to changes
in landscape structure at small spatial scales
28
. Additionally, agricul-
tural intensification can facilitate the population growth of cereal
aphids due to the abrupt decline of natural enemy/pest ratio
34
. The
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SCIENTIFIC REPORTS | 5 : 8024 | DOI: 10.1038/srep08024 2
abundance of ground-dwelling predators decreased significantly
with increasing proportion of cropland at all spatial scales, suggesting
that a homogenous landscape cannot stabilize the population density
of natural enemies due to the importance of semi-natural habitats to
the recruitment of natural enemies
17,35,36
. Therefore, agricultural
intensification, including increasing fertilizer input within fields
and cropland expansion at the landscape scale, can disturb the inter-
specific relationship of arthropod community in wheat fields, which
may have a negative effect on biocontrol of cereal aphids.
Strong evidence shows that species within a same functional mod-
ule can respond differently to changes in landscape structure
37,38
. For
example, ladybirds and parasitic wasps differ greatly in their dis-
persal ability and thus respond differently to changes in landscape
composition across spatial scales
39
. Wheat crop is attacked by mul-
tiple pest species which are then attacked by multiple natural enemies
that perceive/use the mosaic landscape differently at different spatial
scales
40
. Based on our results, the spatial range for analyzing the effect
of landscape structures on insect communities varied depending on
the particular functional groups
11
.
Potential mechanism of differential responses.In agroecosystems,
agricultural intensification is the most important driver for changing
the land cover and soil structure
6,23
. In particular, nitrogen deposition
in China’s agroecosystem has increased by about 60% in the past
three decades
45
, causing great disturbance to the food web of
arthropods. On the one hand, although increasing nitrogen
fertilizers has directly proliferated crop nutrition and yield, it also
accelerates the development rate of herbivorous insects and their
natural enemies to a different extent, with the outbreak of pests
causing serious damage to crops. Two hypotheses have been
proposed so far to explain the effect of increasing nitrogen
fertilizer input on insect performance, namely the plant vigor
hypothesis and nitrogen limitation hypothesis
15
. These hypotheses
argue that the nitrogen content in plants is an important limiting
factor which dictates the developmental rate, breeding, behavior, and
fecundity of insect herbivores. Contrast to their natural enemies,
these insect pests could benefit more from increasing nitrogen
fertilizer input due to the direct improvement of both food
quantity and quality.
On the other hand, cropland expansion further provides more
resources and habitats for insect pests (resource concentration hypo-
thesis), while the decline of semi-natural habitats from the expansion
eliminates alternative preys and refuges of natural enemies
41,42
.
Moreover, landscape simplification could cause the rearrangement
of habitat patches and reallocation of plant resources. These changes
could further affect the population dispersion and host searching.
The asymmetric responses of cereal aphids and their natural enemies
to cropland expansion could therefore cause the shifts observed in
community structure, leading to biocontrol loss under agricultural
intensification
30
.
Conclusion.Global environmental changes have been occurring at
multiple spatial scales and are an important driver of changes in
biodiversity composition and population dynamics. Increasing
nitrogen input can facilitate the population of parasitic wasps
while suppressing the activity of ground-dwelling predators
43
, all
greatly effecting the community structure of natural enemies
within fields. Cropland expansion in agricultural landscapes can
Figure 1
|
The effects of input of nitrogen fertilizer on cereal aphids and their natural enemies in wheat fields ((A) cereal aphids: solid circular indicates
Sitobion avenae
(Fabricius), hollow circular indictes
Schizaphis graminum
(Rondani); (B) parasitic wasps: solid circular indicates
Aphidius avenae
Haliday, hollow circular indicates
Aphidius gifuensis
Ashmaed; (C) leaf-ground predators: solid circular indicates
Hippodamia variegata
(Goeze),
hollow circular indicates
Syrphus nitens
Zetterstedt; (D) ground-dwelling predators: solid circular indicates
Pardosa astrigena
L. Koch hollow circular
indicates
Chlaeniu spallipes
Geb).
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SCIENTIFIC REPORTS | 5 : 8024 | DOI: 10.1038/srep08024 3
also shift the natural enemy community, causing the loss of
biocontrol service and the outbreak of cereal aphids at landscape
scale. Therefore, agricultural intensification at both the field and
landscape scales can disturb the food web structure of arthropods
and destabilize the interaction between cereal aphids and their
natural enemies
21,35
. Habitat management for sustainable pest
management should be conducted at multiple spatial scales
including the field and landscape scales
46,47
.
The marked changes of different species modules in response to
agricultural intensification suggest that studies on isolated modules
could be misleading, and that quantitative food web metrics need to
be considered in future research
37,44
. Future studies should compare
functional groups or interspecific relationship of all species in land-
scapes with different levels of complexity in patch arrangement and
spatial structure in order to distinguish between the intraguild effects
of different biocontrol agents working at different spatial scales
7,28,48
.
Methods
The study area.This experiment was conducted near the city of Yinchuan, Ningxia
Hui Autonomous Region of Northwest China. This agricultural region (Yinchuan
plateau, 1100–1200 m a.s.l) has a temperate continental climate and a long history of
crop culture. The area has an average 3,000 h p.a. of sunshine and an annual mean
temperature of 13.1uC. The type of soil is Chernozem, a typical type of the region. The
area has experienced drastic land use changes from natural habitats to arable land,
forming a gradient of landscape simplification through agricultural intensification in
the past decades. The landscape mosaic consists of different habitat patches including
crops, fallow land, grasslands, and woodlands. Agricultural management within crop
fields has led to a gradual change of soil chemical composistion through frequent use
of nitrogen fertilizer for sustaining high crop yields. These changes could have
affected the distribution and composition of arthropod communities in wheat fields
at both local and regional scales.
Seventeen agricultural sites (see supplementary Table S1) were selected along a
gradient of landscape simplification in a radius of 1500 m among sites, from intensive
agricultural sites with a high percentage of arable land (maximum value 583.26%) to
sites with a low percentage of arable land (minimum value 555.82%). Semi-natural
habitats in these sites, including woodlands and fallow land, remained unchanged
during the experiment period from 2010 to 2011
49
. The nearest neighbor distances of
these sites ranges from 3000 m to 5600 m.
The experimental region had an old planting history (.30 years) of wheat crop.
Three wheat fields in the center of 1500 m radius were selected in each site. To
simplify the experiment design, we chose the wheat fields with the same wheat variety
and soil type. This has been shown to be an appropriate method for studying the effect
Figure 2
|
Effect of spatial scales on the Pearson correlation between the
proportion of cropland and the abundance of cereal aphids and their
natural enemy in agricultural landscapes (cereal aphids (individuals/100
straws): solid circular indicates
S. avenae
, hollow circular indicates
S.
graminum
; primary parasitoids (individuals/100 straws): solid triangle
indicates
A. avenae
, hollow triangle indicates
A. gifuensis
;leaf-ground
predators (individuals/100 nets): solid square indicates
H. variegata
, hollow
square indictes
S. nitens
; ground-dwelling predators (individuals/traps):
solid rhomb indicates
P. astrigena
, hollow rhomb indicates
C. spallipes
).
Figure 3
|
The effects of nitrogen fertilizer input on parasitism, predator/pest ratio, and species diversity in wheat fields ((A) primary parasitism; (B)
predator/pest ratio for leaf-ground predators; (C) predator/pest ratio for ground-dwelling predators; (D) species diversity).
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SCIENTIFIC REPORTS | 5 : 8024 | DOI: 10.1038/srep08024 4
of landscape structure on arthropod communities
7,17,50
. Wheat density was kept to
about 400–450 plants per m
2
, and the irrigation was kept nearly the same across all
studied wheat fields, each year from March to June.
Insect sampling.Two dominant pests, Sitobion avenae (Fabricius) and Schizaphis
graminum (Rondani), and their primary parasitoids, leaf- and ground-dwelling
predators were investigated in the field experiment. As the primary parasitoids spend
their whole larval stage in the mummies of cereal aphids, they can be investigated at
the same time. In each field, five randomly-selected points were used to sample cereal
aphids and their primary parasitoids by visual inspection and hand collection
49
.In
each point, 100 wheat tillers were selected for investigation (5 minutes for cereal aphid
and 15 minutes for primary parasitoids). All fields were sampled within a two-day
period (for diminishing potential stochasticity); three times per year (14
th
–15
th
,19
th
–
20
th
, and 24
th
–25
th
of May -when the population of cereal aphids peaks). All cereal
aphids and their natural enemies were collected before pesticide application (30
th
May–5
th
July) to ignore the effect of pesticides on the experiment. All aphid mummies
were taken back to the laboratory and reared in the gelatin capsules for 30 days. The
hatched adults of primary parasitoids were collected and conserved in 90% ethyl
alcohol.
The ground-dwelling predators (e.g. Carabid beetles and spiders) are important
natural enemies of aphids
51
. We used pitfall traps for collecting ground-dwelling
predators at the same five randomly-selected points. In each pitfall trap (6.5 cm in
diameter and 11 cm high), 60 mL mixture of vinegar, sugar, propylene glycol and
water at a ratio of 25151520 were filled in a 0.2-L plastic cup. An odorless detergent
(0.3%) was added into the trap to break the surface tension of the mixture. Ground-
dwelling predators were collected 3 times from 10
th
to 25
th
of May in each year. In
every time, the trap was open for five days. Population density of ground-dwelling
predators was calculated in individuals per 5 traps.
The same five randomly-selected points were also used to collect leaf-dwelling
predators (coccinellids, syrphids and lacewings); we used a sweep net (200 meshes)
for this purpose at the same period of pitfall trapping
51
. We sampled 10 times (nets)
per point by sweeping and thus 50 times (nets) per wheat field. The leaf-dwelling
predators collected in the sweeping were transferred into finger shaped bottles, with
80% ethyl alcohol added into each bottle to preserve the samples. Population density
of leaf-dwelling predators was calculated in individuals per 10 nets. All adult primary
parasitoids, ground- and leaf-dwelling predators were identified to species according
to their morphological and taxonomic characteristics.
Field and landscape survey.Within each field scale, landowners were surveyed by
questionnaires and data was collected regarding type of the fertilizer, insecticide, and
yield. These three variables were obtained through two questions: 1) What is the
amount of fertilizer applied per hectare and its composition? 2) What is the average
yield in sampled wheat fields? Because nitrogen fertilizer is the main limiting resource
for wheat growing and breeding, we calculated the amount of nitrogen fertilizer
applied based on the answers to question 1.
At the landscape scale, geostatistic methods were used for collecting information
on agricultural intensification. Specifically, the spatial arrangement of habitat com-
position in each landscape was derived from the Cropland Data Layer, with a 30-m
resolution, obtained from the Chinese Academy of Sciences. All landscape metrics
were computed using the Patch Analyst extension of FRAGSTATS (ArcGIS 9.3,
2008). For further analysis, proportion of cropland (PC) was indicated by the per-
centage of arable lands in the selected site:
PC%~AREAarable habit at
AREAtotal area
|100%,
where AREA
arable habitat
and AREA
total area
are the area sizes of arable habitats and
total area in each landscape. The PC was obtained at six spatial scales from 200 to
1500 m based on the buffer circle method in agricultural landscape.
Statistical analysis.The abundance (Individuals per 5 traps for ground-dwelling
predators; per 10 sweeps for leaf-dwelling predators; per 100 wheat tillers for primary
parasitoids) were estimated for further analyses. At the population level, two
dominant species (primary parasitoids: Aphidius avenae and Aphidius gifuensis; leaf-
dwelling predators: Hippodamia variegata and Syrphus nitens; ground-dwelling
predators: Pardosa astrigena and Chlaeniu spallipes) were selected for the analysis in
each module containing natural enemies. To prevent the interference of temporal
trends in the analysis, we detrended population density by regressing population
density against year before calculating standard deviation of detrended population
density
52,53
. The detrended data was used for examining the relationship between
agricultural intensification and insect communities at the six spatial scales. At the
community level, Simpson’s diversity (D~1{Pi(Ni=N)2) was used to calculate
species diversity of natural enemies according to population density.
At the field scale the Pearson correlation was used to examine the relationship
between fertilizer input and the abundance of cereal aphids and their natural enemies.
As the amount of nitrogen fertilizer is strongly correlated with grain yield (covar-
iance), it was removed from the analysis. At the landscape scale, the Pearson cor-
relation was also used to examine the relationship between proportion of cropland
(PC) and the abundance of cereal aphids and their natural enemies at multiple spatial
scales.
To analyze the joint effects of nitrogen input within the field and the proportion of
cropland at the landscape level on the distribution of cereal aphids and their natural
Figure 4
|
The effects of the proportion of cropland at the 500 m scale on parasitism, predator/pest ratio, and species diversity in wheat fields ((A)
primary parasitism; (B) predator/pest ratio for leaf-ground predators; (C) predator/pest ratio for ground-dwelling predators; (D) species diversity).
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SCIENTIFIC REPORTS | 5 : 8024 | DOI: 10.1038/srep08024 5
enemies, we applied a linear mixed-effect model (LMM) with the restricted maximum
likelihood method
54
. Species were lumped together into three modules (aphids,
predators and parasitoids) for calculating the predator/prey ratio and primary
parasitism in wheat fields. Nitrogen fertilizer input and the proportion of cropland
were considered as fixed factors, and the landscape site and year as random factors.
Wald tests were used to examine the significant level of fixed effects and twofold
interactions between them. A backward stepwise procedure was used to examine the
contribution of fixed factors and interactions; the fixed factors with P ,0.05 were left
in the full model. Response factors were log-transformed to meet the Gaussian dis-
tribution requirement. Furthermore, the polynomial effects of landscape structure
were tested by adding the fixed factors, (nitrogen input)
2
and (the proportion of
cropland)
2
, to the model. As none of these factors had noticeable additional explan-
atory power, we considered the relationships between landscape structure and log-
transformed insect population density to be linear. R was used for conducting the
statistical analysis (lme4, packages, R Development Core Team 2005). Sigma Plot 12.5
was used for drawing the graphs.
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Acknowledgments
We are grateful to Ying Wang, Jia Hang, Ting-Ting Zhang, Ying-shu Zhao, Xiao hu Li, Chun
Lu for field assistance and to Beverley Laniewski for English editing. Financial sup port came
www.nature.com/scientificreports
SCIENTIFIC REPORTS | 5 : 8024 | DOI: 10.1038/srep08024 6
from the State Key Program of National Natural Science of China (No. 31400349). CH is
supported by the National Research Foundation of South Africa (grants 76912, 81825 and
89967). BL is partially supported by the University of California Agricultural Experiment
Station.
Author contributions
Z.Z. and D.H. designed and conducted the field experiments. Z.Z. conducted the data
analysis. Z.Z., H.C. and B.L. wrote the main manuscript text. All authors reviewed the
manuscript.
Additional information
Supplementary information accompanies this paper at http://www.nature.com/
scientificreports
Competing financial interests: The authors declare no competing financial interests.
How to cite this article: Zhao, Z.-H., Hui, C., He, D.-H. & Li, B.-L. Effects of agricultural
intensification on ability of natural enemies to control aphids. Sci. Rep. 5, 8024;
DOI:10.1038/srep08024 (2015).
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