effect of within-field and landscape factors on insect damage in winter oilseed rape
TRANSCRIPT
Effect of within-field and landscape factors on insect damage
in winter oilseed rape
Johann G. Zaller *, Dietmar Moser, Thomas Drapela, Claudia Schmoger, Thomas Frank
Department of Integrative Biology and Biodiversity Research, Institute of Zoology, University of Natural Resources and Applied Life Sciences Vienna,
Gregor Mendel Strasse 33, A-1180 Vienna, Austria
Received 30 January 2007; received in revised form 11 July 2007; accepted 16 July 2007
Available online 23 August 2007
Abstract
It was investigated whether damage on winter oilseed rape (Brassica napus) caused by three major pests (rape and cabbage stem weevil,
pollen beetle, brassica pod midge) was affected by within-field (soil quality, nitrogen fertilization level, plant development, stand density) and
landscape factors (percentage B. napus area, isolation of B. napus fields, number of B. napus fields, average distance between study field and
surrounding B. napus fields—all within a radius of 2000 m around the study fields). Damage and within-field/landscape relationships were
analyzed on 29 landscape sectors using stepwise multiple regression analyses. Damage caused by stem weevil larvae was assessed by
measuring the length of damaged stem pith on dissected B. napus stems, pollen beetle damage was assessed on top racemes by calculating the
percentage of podless peduncles, damage by pod midge larvae was calculated as the percentage of yellow and prematurely split pods in the top
racemes. Stem weevil and pollen beetle damage was significantly positively correlated with respective pest abundances, however no such
relationship could be observed for pod midge. Oilseed rape yield was for all three damage measures significantly negatively related to the
degree of damage. Multiple regression analyses revealed that pollen beetle and pod midge damage was negatively related to B. napus area in
the surrounding landscape, while stem weevil damage showed a positive relationship with soil quality, plant development and stand density.
The results indicated that pollen beetle and pod midge damage was mainly influenced by the amount of host plants in the landscape while stem
weevil damage seemed to be more affected by within-field characteristics that might have altered the nutritional quality of the oilseed rape
crop and/or the stand microclimate.
# 2007 Elsevier B.V. All rights reserved.
www.elsevier.com/locate/agee
Agriculture, Ecosystems and Environment 123 (2008) 233–238
Keywords: Brassica napus; Ceutorhynchus napi; Ceutorhynchus pallidactylus; Dasineura brassicae; Herbivory; Meligethes aeneus; Winter oilseed rape
1. Introduction
The importance of oilseed rape (Brassica napus L.) as a
source for industrial and nutritional oil has been increasing
worldwide and in some countries an increasing acreage is
accompanied by a dramatic disproportionate increase of
pesticide applications. For instance, in the USA, the
harvested oilseed rape area increased fivefold from 1992
to 1997 (from 53,000 ha to 283,080 ha; FAOSTAT, http://
faostat.fao.org) while pesticide use in B. napus during this
time increased more than 60-fold (from 2703 to 171,261 kg
* Corresponding author. Tel.: +43 1 47654 3205; fax: +43 1 47654 3203.
E-mail address: [email protected] (J.G. Zaller).
0167-8809/$ – see front matter # 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.agee.2007.07.002
active ingredients year�1; Gianessi and Marcelli, 2000). For
most of Europe, comparable data are lacking, however, data
from the UK show a similar trend (50% increase in B. napus
area versus 70% increased amount of insecticides applied;
Garthwaite et al., 2004). In Europe the most important insect
pests in B. napus are the cabbage stem flea beetle (Psylliodes
chrysocephala L., Chrysomelidae), the pollen beetle
(Meligethes aeneus F., Nitidulidae), the cabbage seed
weevil (Ceutorhynchus assimilis Payk., Curculionidae),
the rape stem weevil (C. napi Gyll.), the cabbage stem
weevil (C. pallidactylus Marsh.) and the brassica pod midge
(Dasineura brassicae Winn., Cecidomyiidae) (Alford et al.,
2003). Although oilseed rape crop has been shown to
compensate considerably after insect damage (Free and
J.G. Zaller et al. / Agriculture, Ecosystems and Environment 123 (2008) 233–238234
Williams, 1978, 1979), yield losses up to 80% have been
reported when insecticide spraying was ceased (Hansen,
2003).
Agroecological studies on crop–pest interactions have
usually focused on the impact of either within-field or
landscape factors on a single species (Thies et al., 2003) but
only rarely included both factors in a multi-species setting
(Ostman et al., 2001). In the current study it was investigated
how damage on winter oilseed rape caused by pollen beetle,
cabbage and rape stem weevil and pod midge is related to
within-field and B. napus-specific landscape factors in the
surroundings (radius 2000 m). These pest species were
considered because they were the most abundant in the study
region and differ in their overwintering strategies, genera-
tion cycles and mobility. Additionally, they affect different
parts of the crop in different developmental stages: (i) stem
weevils lay eggs in leaf petioles or midribs of B. napus
plants, hatched larvae tunnel in the stems; (ii) adult pollen
beetles feed on pollen and damage any of the flowering
structures particularly during the green to yellow bud stages
resulting in podless peduncles; and (iii) brassica pod midges
lay eggs into pods where the hatched larvae feed on the inner
wall of the pod and cause the pods to split prematurely
(Alford et al., 2003).
The specific objective of this study was to determine
whether species-specific damage on B. napus was affected
by within-field characteristics and/or the amount and
distribution of B. napus in the surrounding landscape.
Based on the results, it was also the intention to identify
possible consequences for field and landscape management.
Table 1
Within-field and landscape variables of the 29 study fields
Range
Minimum Maximum Average
Within-field
Soil index (0–100) 29 59 42
Amount of N (kg ha�1) 45 143 125
Plant development (% of
maximum height)
70 88 79
Stand density (no. plants m�2) 27 77 57
Landscape level (within 2000 m from each study field)
Brassica napus area (%) 0.6 8.1 4.9
Isolation of B. napus fields 9763 58,406 24,896
Number B. napus fields 7 50 31
Mean distance to B. napus fields (m) 872 1,509 1,240
For more details on the variables see Section 2.
2. Materials and methods
The study region (area about 240 km2) was located in the
topographically relatively flat region of Lower Austria,
about 40 km east of Vienna (arable land ranging from 130 m
to 250 m a.s.l.; coordinates of the centre of the study area:
168570E, 488040N). During the study period from April to
July 2005 the average temperature was 16.9 8C; the rainfall
during this period amounted to 336 mm (average tempera-
ture and rainfall in these months between 1990 and 2004 was
16.0 8C and 230 mm, respectively; weather data were
provided from the meteorological station Bruck/Leitha
located about 16 km to the west of the study region). The
region mainly consisted of farmland on chernozem soils
cropped according to integrated pest management guidelines
(main crops: wheat, maize, barley, winter oilseed rape,
sunflower, sugar beet, poppy seed). Farmland was inter-
spersed with semi-natural non-crop areas such as fallows,
hedges and forest remnants. In this region, 29 winter B.
napus fields were randomly selected to assess pest damage.
Landscape variables included B. napus area, number of
B. napus fields, isolation of B. napus fields and the average
distance between the study field and other B. napus fields.
These were calculated within a radius of 2000 m around
each of the study fields using the software packages
ArcGis 9.1 and ArcView GIS 3.3 (ESRI Redlands, CA,
USA) (Table 1). Field surveys using real-colour ortho-
photos (minimum resolution 0.25 m) were conducted in
2005 to assess the current spatial distribution of B. napus
fields. Isolation of B. napus fields in the landscape was
calculated by applying a negative exponential weighting
function based on the distances of neighboring B. napus
fields to the study field using the formula: isolation oilseed
rapei = �P
(e�distance � oilseed rape areaj)/Se�distance (i.e.
the lower the value the higher the isolation; Kruess, 2003).
Within-field variables included plant development, stand
density, soil index and nitrogen fertilization level. Plant
development was assessed at one sampling date (growth
stages GS 77–80; Lancashire et al., 1991) on 30 random B.
napus plants per field and was calculated as the height
relative to maximum height at B. napus harvest. Oilseed
rape stand density was assessed by counting the number of
stems within two 1 m2 frames per field. Soil index and
nitrogen fertilization was obtained by a questionnaire
among the participating farmers (Table 1). Soil index is an
integrative measure of soil quality that encompasses soil
type, humus content, soil depth, texture, density, structure,
lime content, gleying and soil congregation (OBG, 2001)
and generally specifies the natural yield capacity of a field in
relation to the highest yielding capacity of the country (0:
soil with lowest yield capacity, 100: soil with highest yield
capacity).
Oilseed rape (cv. Californium) was sown by the
participating farmers on the 29 fields between 20 August
and 14 September 2004. Oilseed rape fields were fertilized
(125 � 4 kg N ha�1 a�1; mean � 1 standard error) and
treated with herbicides (0.81 � 0.03 l ha�1 Metazachlor)
and insecticides (9.65 � 0.44 ml ha�1 a�1 Alphacyperme-
thrin) until December 2004. From January 2005, 1 ha was
excluded from pesticide applications at the head of these B.
napus fields and used for sampling crop plants for this study.
A buffering zone of at least 10 m to the next sprayed B.
napus field was kept. The preceding crop was winter barley
J.G. Zaller et al. / Agriculture, Ecosystems and Environment 123 (2008) 233–238 235
for 18 fields, winter wheat for 10 fields and poppy seed for
one field.
Yield data for 25 of 29 fields were provided by
participating farmers after harvest in the third week of
June 2005.
Damage caused by stem weevil larvae was assessed in late
April 2005 (GS 64–67) after removing 25 randomly chosen B.
napus plants from the central area of each of the 29 study
fields; stems were dissected and stem length with visible signs
of herbivory (i.e. brownish pith due to excrements of weevil
larvae) measured as a percentage of the overall stem length.
Damage on B. napus stems mainly stemmed from the two
stem weevils (C. pallidactylus and C. napi) where C.
pallidactylus larvae comprised more than 80% of the stem
weevil abundance in the region. Damage caused by adult
pollen beetles usually leads to podless peduncles and was
quantified in late May 2005 (GS 77–79) on top racemes of 25
randomly chosen plants in the central area of the 29 fields;
percentage of podless peduncles in relation to total number of
pods was calculated. In the study region two pollen beetle
species were present: M. aeneus was the predominant one and
M. viridescens could be observed only sporadically (Kraus
and Kromp, 2002). Generally, pod loss could potentially result
from pollen beetle damage, pod midge damage or nutrient
deficiencies. However, since pod midge damage usually
leaves much larger peduncles than pollen beetle damage, it
was possible to clearly determine what species caused the
damage. In order to avoid nutrient deficiencies causing pod
loss, participating farmers were required to fertilize the study
fields similarly to other B. napus fields (Table 1). Damage
from brassica pod midge larvae (D. brassicae) was assessed
by counting the premature, yellow and splitted pods on 25
randomly chosen top racemes from the central area of each
study field in late May 2005 (GS 76–80). Abundances of stem
weevil larvae were assessed at GS 64–67, of pollen beetle
adults at GS 64–65 and brassica pod midge at GS 76–79. For
better comparison, insect numbers per m2 were calculated by
multiplying pest abundances per plant with the average field-
specific crop density.
Pearson correlation analyses were used to test inter-
dependencies between within-field and landscape variables
and relationships between pest abundances and damage
Fig. 1. Relations between winter oilseed rape yield and species-
measures. In order to assess the influence of within-field and
landscape variables on pest damage stepwise multiple
regression analyses were conducted. Response variables
were tested for normality using Shapiro–Wilk W-statistic
and log-transformed when necessary to meet criteria for
statistical analyses (Zar, 1996). All statistical analyses were
performed using SPSS (vers. 12.0.1 for Windows, SPSS Inc.,
Chicago, IL, USA).
3. Results
Investigated within-field and landscape factors varied
considerably among the studied B. napus fields (Table 1).
Abundances of stem weevil larvae varied between 2 m�2
and 118 m�2, of pollen beetle adults in top racemes between
34 m�2 and 1798 m�2 and of brassica pod midge larvae in
top racemes between 14 m�2 and 490 m�2. There was no
relation between the preceding crop and total pest
abundances (r2 = 0.179, P = 0.354; logistic regression
analysis). Within-field variables were uncorrelated to each
other (data not shown), of the landscape variables only B.
napus area was significantly positively correlated with
number of B. napus fields (r = 0.621, P < 0.001) and B.
napus isolation (r = 0.568, P = 0.001). B. napus area and
number of B. napus fields were significantly negatively
correlated with soil index (r = �0.650, P < 0.001 and
r = �0.733, P < 0.001, respectively); no other correlations
between within-field and landscape variables were found.
Stem length damaged was positively related to log number
of stem weevil larvae stem�1 (r = 0.685, P < 0.001),
however unrelated to pollen beetle or pod midge abundance.
Percentage podless peduncles was positively related to log
pollen beetle adults raceme�1 (r = 0.838, P < 0.001),
however unrelated to stem weevil or pod midge abundance.
Percentage premature pods was significantly positively
related to log pollen beetle adults raceme�1 (r = 0.792,
P < 0.001), however unrelated to stem weevil or pod midge
abundance. Damage caused by stem weevil larvae was
significantly positively correlated with damage of pollen
beetles (r = 0.545, P = 0.002) but not with that of pod midge
(r = 0.233, P = 0.223); damage by pollen beetle and pod
specific damage measures in 29 winter oilseed rape fields.
J.G. Zaller et al. / Agriculture, Ecosystems and Environment 123 (2008) 233–238236
Table 2
Results of stepwise multiple regression analyses relating pest damage in B. napus to within-field (soil index, nitrogen fertilization level, stand density, plant
development) and landscape factors (B. napus area, number of B. napus fields, isolation of B. napus fields, mean distance study field to other B. napus fields)
Response variable Explanatory variable Beta t P
% Stem length damaged Model adjusted r2 = 0.473
Soil index 0.446 3.078 0.005
Plant development 0.334 2.424 0.023
Stand density 0.310 2.149 0.042
% Podless peduncles Model adjusted r2 = 0.520
B. napus area �0.733 �5.599 <0.001
% Premature pods Model adjusted r2 = 0.433
B. napus area �0.673 �4.730 <0.001
Only variables with P < 0.05 were included in the final model (n = 29).
Fig. 2. Relations between species-specific damage measures in 29 winter oilseed rape fields and best-explaining within-field and landscape variables revealed
through multiple regression analyses.
midge was significantly correlated with each other
(r = 0.792, P < 0.001). Oilseed rape yield was significantly
negatively related to stem length damaged (r = 0.388,
P = 0.046), podless peduncles (r = 0.596, P = 0.001) and
premature pods (r = 0.743, P < 0.001; Fig. 1).
Multiple regression analyses showed that a significant
proportion of variation for pollen beetle and pod midge
damage was accounted for by a negative relationship with B.
napus area as the single explanatory variable (Table 2,
Fig. 2); other within-field and landscape variables tested did
not account for significant amounts of variability. In the
multiple regression analysis, stem weevil damage was
significantly positively related to the within-field variables
soil quality, plant development and stand density (Table 2,
Fig. 2), while other within-field and landscape variables did
not explain significant amounts of variability (data not
shown).
4. Discussion
Generally, pod loss could potentially also be caused by
nutritional deficiencies (Rathke and Diepenbrock, 2006),
however the lack of a relationship with nitrogen fertilization
demonstrated that the applied fertilizer levels were sufficient
to avoid effects on pod development. However, because the
number of pod midge larvae in pods can vary from <10 to
>100 (Ahman, 1985) it is likely that even small variations in
pod midge oviposition behaviour between crop plants (e.g.
due to differences in crop quality and/or microclimatic
conditions) could result in different damage levels (Ferguson
et al., 2003). Hence, the randomized sampling design for
assessing pod midge abundance and damage might not have
been sensitive enough to document this relationship. The
relationship between premature pods and pollen beetle
abundance was surprising because pollen beetle damage
usually precludes the development of pods leaving only
podless stalks on the racemes. Nevertheless, a comparison of
the relationships between B. napus yield and damage among
the three pest species suggested that the number of yellow
and premature pods was a relevant parameter that indeed
reflected pest damage.
4.1. Within-field versus landscape characteristics
Multiple regression analysis for the three species revealed
that stem weevils were mainly affected by within-field
parameters while pollen beetles and pod midges were
responsive to B. napus area in the landscape. For stem
weevils, it is unlikely that within-field characteristics would
have directly affected damage because these species invaded
the study fields from non-crop overwintering sites. However,
soil quality, B. napus development and stand density may
have affected stem weevil damage indirectly via (i)
J.G. Zaller et al. / Agriculture, Ecosystems and Environment 123 (2008) 233–238 237
influencing the nutritional quality of B. napus plants, e.g.
through the production of glucosinolates (Bartlet, 1996); (ii)
altering the odour intensity of B. napus plants and thereby
changing the attractiveness for this pest species (Cook et al.,
2006); and (iii) altering the B. napus canopy microclimate
and thus influencing the searching efficiency of pest species
(Walters et al., 2003).
Pollen beetle and pod midge damage was best explained
by a negative relationship to B. napus area in the landscape
indicating that damage was higher in landscapes where less
B. napus area was available and vice versa. An analogous
concentration effect has been reported for other insect
species in fragmentation studies (Debinski and Holt, 2000;
Tischendorf et al., 2005), the current study is the first one
suggesting this relationship for B. napus pests. In contrast to
the current study, Thies et al. (2003) found no relationship
between pollen beetle damage and B. napus area in the
landscape. An explanation for this discrepancy could be the
fundamentally different methodological approaches used:
potted B. napus plants distributed in the landscape were used
in the former study while field-grown plants were
investigated in the current study.
Assuming that the distribution of pest damage would
reflect the foraging range and dispersal ability of the studied
pest species (Kruess and Tscharntke, 1994, 2000) it was
surprising to see that variables characterizing the distribution
of B. napus fields in the landscape (e.g. distance between B.
napus fields) were unrelated to pest damage in the
multivariate analysis. Generally, B. napus pest damage also
reflects the B. napus area of the preceding year that enabled
the buildup of a landscape pest pool available in the current
year (Hokkanen, 2000). Due to subsidies from agri-
environmental programmes aimed to promote both B. napus
and the extensification of farmland in the region, B. napus area
remained stable during the last years (BMLFUW, 2006).
4.2. Management implications
From a farmer’s perspective all three pest species seem to
be important because damages of all three showed negative
impacts on yields. These results suggest that stem weevil
damage and yield loss would be reduced if B. napus was
cropped on fields with below-average soil quality combined
with lower stand density and delayed crop development.
Since it was shown that pollen beetle and pod midge damage
was higher when less B. napus area was available, dramatic
fluctuations in B. napus area between years should be
avoided. Thus, crop rotation schemes already in place to
reduce carry-over of oilseed rape pests and diseases (Rathke
et al., 2006) could be expanded by a landscape perspective.
Acknowledgements
We are grateful to the farmers for participating, to the
regional governments of Lower Austria and Burgenland for
providing maps and aerial photographs of the project area.
Help by Norbert Schuller and Erhard Tesarik in the field and
laboratory is gratefully acknowledged. We also thank the
staff at the University Research Farm Gross-Enzersdorf for
their help during post harvesting activities. Two anonymous
referees gave valuable comments on an earlier draft of the
manuscript. J.G.Z., D.M. and T.D. are grateful to the
Austrian Science Fund for supporting this research (grant
no. P16972).
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