effect of within-field and landscape factors on insect damage in winter oilseed rape

6
Effect of within-field and landscape factors on insect damage in winter oilseed rape Johann G. Zaller * , Dietmar Moser, Thomas Drapela, Claudia Schmo ¨ger, 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. 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 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 www.elsevier.com/locate/agee Agriculture, Ecosystems and Environment 123 (2008) 233–238 * 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

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Page 1: Effect of within-field and landscape factors on insect damage in winter oilseed rape

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

Page 2: Effect of within-field and landscape factors on insect damage in winter oilseed rape

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

Page 3: Effect of within-field and landscape factors on insect damage in winter oilseed rape

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.

Page 4: Effect of within-field and landscape factors on insect damage in winter oilseed rape

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)

Page 5: Effect of within-field and landscape factors on insect damage in winter oilseed rape

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).

References

Ahman, I., 1985. Oviposition behaviour of Dasineura brassicae on a high-

versus a low-quality Brassica host. Entomol. Exp. Appl. 39, 247–253.

Alford, D.V., Nilsson, C., Ulber, B., 2003. Insect pests of oilseed rape crops.

In: Alford, D. (Ed.), Biocontrol of Oilseed Rape Insect Pests. Blackwell,

Oxford, UK, pp. 9–41.

Bartlet, E., 1996. Chemical cues to host-plant selection by insect pests of

oilseed rape. Agric. Zool. Rev. 7, 89–116.

BMLFUW (Ed.), 2006. Gruner Bericht 2006. Bundesministerium fur Land-

und Forstwirtschaft, Umwelt und Wasserwirtschaft, Vienna, Austria.

Cook, S.M., Smart, L.E., Martin, J.L., Murray, D.A., Watts, N.P., Williams,

I.H., 2006. Exploitation of host plant preferences in pest management

strategies for oilseed rape (Brassica napus). Entomol. Exp. Appl. 119,

221–229.

Debinski, D.M., Holt, R.D., 2000. A survey and overview of habitat

fragmentation experiments. Conserv. Biol. 14, 342–355.

Ferguson, A.W., Klukowski, Z., Walczak, B., Clark, S.J., Mugglestone,

M.A., Perry, J.N., Williams, I.H., 2003. Spatial distribution of pest

insects in oilseed rape: implications for integrated pest management.

Agric. Ecosyst. Environ. 95, 509–521.

Free, J.B., Williams, I.H., 1978. A survey of the damage caused to crops of

oil-seed rape (Brassica napus L.) by insect pests in south-central

England and their effect on seed yield. J. Agric. Sci. Camb. 90,

417–424.

Free, J.B., Williams, I.H., 1979. The distribution of insect pests on crops of

oil-seed rape (Brassica napus L.) and the damage they cause. J. Agric.

Sci. Camb. 92, 139–149.

Garthwaite, D.G., Thomas, M.R., Anderson, H.M., Stoddart, 2004. Arable

Crops in Great Britain 2004. Department for Environment, Food &

Rural Affairs and Scottish Executive Environment & Rural Affairs

Department, York, UK.

Gianessi, L.P., Marcelli, M.B., 2000. Pesticide Use in U.S. Crop Production:

1997. National Center for Food and Agricultural Policy, Washington,

DC, USA.

Hansen, L.M., 2003. A model for determination of the numbers of pollen

beetles (Meligethes aeneus F.) (Col., Nitidulidae) per plant in oil-seed

rape crops (Brassica napus L.) by estimating the percentage of plants

attacked by pollen beetles. J. Appl. Entomol. 127, 163–166.

Hokkanen, H.M.T., 2000. The making of a pest: recruitment of Meligethes

aeneus onto oilseed Brassicas. Entomol. Exp. Appl. 95, 141–149.

Kraus, P., Kromp, B., 2002. Parasitization rates of the oilseed rape pests

Ceutorhynchus napi, Ceutorhynchus pallidactylus (Coleoptera, Curcu-

lionidae) and Meligethes aeneus (Coleoptera, Nitidulidae) by Ichneu-

monids in several localities of eastern Austria. IOBC/WPRS Bull. 25,

117–122.

Kruess, A., 2003. Effects of landscape structure and habitat type on a plant-

herbivore-parasitoid community. Ecography 26, 283–290.

Kruess, A., Tscharntke, T., 1994. Habitat fragmentation, species loss, and

biological control. Science 264, 1581–1584.

Kruess, A., Tscharntke, T., 2000. Effects of habitat fragmentation on plant-

insect communities. In: Ekbom, B., Irwin, M.E., Robert, Y. (Eds.),

Interchanges of Insects between Agricultural and Surrounding

Page 6: Effect of within-field and landscape factors on insect damage in winter oilseed rape

J.G. Zaller et al. / Agriculture, Ecosystems and Environment 123 (2008) 233–238238

Landscapes. Kluwer Academic Publishers, Dordrecht, The Netherlands,

pp. 53–70.

Lancashire, P.D., Bleiholder, T., Van den Boom, T., Langeluddecke, P.,

Stauss, R., Weber, E., Witzenberger, A., 1991. A uniform decimal code

for growth stages of crops and weeds. Ann. Appl. Biol. 119, 561–601.

OBG, 2001. Bodenaufnahmesysteme in Osterreich. Mitteilungen der Oster-

reichischen Bodenkundlichen Gesellschaft 62, 219 pp.

Ostman, O., Ekbom, B., Bengtsson, J., 2001. Landscape heterogeneity and

farming practice influence biological control. Basic Appl. Ecol. 2,

365–371.

Rathke, G.-W., Behrens, T., Diepenbrock, W., 2006. Integrated nitrogen

management strategies to improve seed yield, oil content and nitrogen

efficiency of winter oilseed rape (Brassica napus L.): a review. Agric.

Ecosyst. Environ. 117, 80–108.

Rathke, G.W., Diepenbrock, W., 2006. Energy balance of winter oilseed

rape (Brassica napus L.) cropping as related to nitrogen supply and

preceding crop. Eur. J. Agron. 24, 35–44.

Thies, C., Steffan-Dewenter, I., Tscharntke, T., 2003. Effects of landscape

context on herbivory and parasitism at different spatial scales. Oikos

101, 18–25.

Tischendorf, L., Grez, A., Zaviezo, T., Fahrig, L., 2005. Mechanisms

affecting population density in fragmented habitat. Ecol. Soc. 10, 7

(online). URL: http://www.ecologyandsociety.org/vol10/iss1/art7/

Walters, K.F.A., Young, J.E.B., Kromp, B., Cox, P.D., 2003. Management of

oilseed rape pests. In: Alford, D. (Ed.), Biocontrol of Oilseed Rape

Insect Pests. Blackwell, Oxford, UK, pp. 43–71.

Zar, J.H., 1996. Biostatistical Analysis, 3rd ed. Prentice-Hall, Englewood

Cliffs, USA.