the effects of pesticides on species of non-target heteroptera inhabiting cereal fields in southern...

Pestic. Sci. 1997, 51, 39È48

The Effects of Pesticides on Species of Non-targetHeteroptera Inhabiting Cereal Fields in SouthernEnglandStephen J. Moreby,*1 Nicolas W. Sotherton1 & Paul C. Jepson2

1 The Game Conservancy Trust, Burgate Manor, Fordingbridge, Hampshire, SP6 1EF, UK2 Department of Entomology, Oregon State University, Cordley Hall, Corvallis 973321, Oregon, USA

(Received 1 March 1996 ; revised version received 22 April 1997 ; accepted 16 May 1997)

Abstract : The e†ects of pesticides on beneÐcial predatory arthropods have beenwidely studied ; this paper however deals with their e†ects on Heteroptera, animportant beneÐcial insect group and food source for farmland birds. Fieldtrials were used to evaluate pesticide e†ects under realistic conditions of applica-tion on a commercial arable farm and compared with previously publishedlaboratory Ðndings. Fungicides were found to produce very low levels of mortal-ity, not signiÐcantly di†erent from control treatments. Aphicides varied in theirimpact, producing non-signiÐcant to highly signiÐcant mortality levels. The likelyecological impact of pesticides on various heteropteran groups found within theÐeld and Ðeld boundary is discussed.

Pestic Sci., 51, 39È48, 1997No. of Figures : 7. No. of Tables : 3. No. of Refs : 41

Key words : pesticides, Heteroptera, beneÐcial arthropods, farmland birds, Ðeldedge

1 INTRODUCTION

Treatments for aphid pests (Hemiptera : Homoptera)constitute the major market for insecticides in the UK.Side-e†ects against non-target species of beneÐcialHemiptera, including plant bugs (Hemiptera :Heteroptera), are a potentially undesirable consequenceof aphicide use. Owing to their importance as biologicalcontrol agents in glasshouses and orchards, manystudies have assessed the impact of insecticides onimportant beneÐcial, non-target hemipteran species,including generalist predators of the genus Anthocoris(Heteroptera : Cimicidae).1h7 Within cereal crops, thelow densities of Anthocoris spp. and other species ofpredatory Heteroptera have probably contributed totheir exclusion from the numerous investigations ofinsecticide side-e†ects on beneÐcial arthropods incereals.

* To whom correspondence should be addressed.

Non-pest phytophagous species of Heteroptera mayalso be present within cereal Ðelds. Some species ofMiridae can occur in high densities, and the mostcommon of these in southern England is Calocoris nor-vegicus (Gmelin).8,9 The e†ects of pesticides on thisspecies have not previously been quantiÐed because ithas not been regarded as either a pest of arable crops ora beneÐcial invertebrate. However, Heteroptera are con-sidered to be an important component of the so-called“chick food insectsÏ10 and are to be found in the diet ofmany bird species of arable land such as Perdix perdixL.,11h13 Alectoris rufa L.,11 Phasianus colchicus L.,14Corvus monedula L.,15 Parus major L.16 and Pyrrhoco-rax pyrrhocorax L.17 The deÐnition of “beneÐcialÏ nowextends to species of importance in the feeding ecologyof farmland vertebrates such as farmland birds.18

Herbicides are normally applied before Heteropteradisperse into the Ðeld from their overwintering sites inthe vegetation of Ðeld boundaries.9 However, numerousfungicides and insecticides may be used during the

391997 SCI. Pestic. Sci. 0031-613X/97/$17.50. Printed in Great Britain(

40 Stephen J. Moreby, Nicolas W . Sotherton, Paul C. Jepson

period when C. norvegicus nymphs and other hetero-pteran species are present in the Ðeld itself, especiallywhen chemicals are applied late in the season. An initiallaboratory screening of a wide range of pesticides fortheir direct, short-term toxicity against C. norvegicusnymphs found fungicides to exhibit only low toxicity,while insecticides could be divided into two groups,with high and low toxic e†ects respectively.19 From thisprocedure, a number of insecticides and fungicides wereselected for further Ðeld studies in which the routes ofexposure to the chemical would more closely representthose experienced by Heteroptera under Ðeld condi-tions. This paper presents the Ðndings of these Ðeldexperiments.

2 MATERIALS AND METHODS

2.1 Fungicides

Three fungicides commonly used in disease control pro-grammes in UK cereal crops, tridemorph, propiconazo-le and prochloraz were tested with a water control(Table 1). The treatments were applied to 12 plots ofwinter wheat, cv. Galahad, (6 m wide] 75 m long)within the Ðeld headland on a commercial arable farmon the Hampshire/Dorset border in southern England.All the cereal headland plots had the same aspect, gra-dient and soil type, and ran consecutively adjacent tothe Ðeld boundary which was formed by a mixed thornhedgerow. The experimental plots were placed in theÐrst 6 m of cereal between the crop edge and the tram-lines running parallel to the Ðeld edge. This part of theheadland was selected as it is a preferred feeding site ofpartridge chicks foraging for insects11 and has beenshown to contain relatively high densities of Hetero-ptera compared to Ðeld areas 50 m away from theboundary.20

Each chemical application was replicated three times

and treatments were allocated to the 12 headland plotsin a random sequence (Fig. 1). No bu†er plots were pos-sible between the treated plots as this would not haveallowed all treatments to have had a similar boundarytype and aspect. The treatments were applied with aself-propelled Chafer Tramliner SP sprayer, Ðtted with a24-m spray boom and 72 cone-jet nozzles (Chafer No. 3(red)). Operating pressure was 1É7 bar and the chemicalswere applied at conventional Ðeld rates in water at 200litre ha~1, achieved with a 10 km h~1 forward speed.Insect samples were collected using a Dietrick vacuuminsect sampler21 on three dates, two post- (]5 (22 June1989) and ]15 (3 July 1989) days after treatment) andone pre-spray ([3 days (14 June 1989)). On each date,samples were taken from two positions, at the Ðeld edgewithin the wild Ñora next to the base of the hedge and3 m into the cereal headland. Five suction samples of0É5 m2, each comprising Ðve 0É1 m2 sub-samples, werecollected at each site along a transect parallel to theÐeld edge within the middle 25 m of each plot, thereforeallowing a bu†er strip within the treatment plots of50 m between adjacent sampling areas. Heteropterawere sorted into four groups ; Calocoris norvegicus,predatory species (Nabis spp., Anthocoris spp.), grass-feeding Stenodemini (L eptopterna dolabrata (L.), Notos-tira elongata (Geo†roy), Stenodema spp.) and otherHeteroptera, comprising all species not already cate-gorised in the other three groups (see Table 3). All fourgroups were also combined to form a Ðfth group, totalHeteroptera.

2.2 Insecticides

The experimental design used to quantify the extent ofthe activity of four insecticides against non-target Het-eroptera was similar to that in the fungicide experimentbut was conducted over three Ðelds of winter wheat, cv.Avalon, on the same farm. In each Ðeld the treatments

TABLE 1Details of Active Ingredients and Doses of Products used in the Field Experi-

ments.a

Product g AI litre~1 Formulation type

FungicidesTridemorph “BardewÏ 750 ECPropiconazole “TiltÏ 250-EC 250 ECProchloraz “SportakÏ 400 EC

InsecticidesPhosalone “ZoloneÏ 350 ECDemeton-S-methyl “MetasystoxÏ-55 580 ECDimethoate “RogorÏ E 400 ECPirimicarb “AphoxÏ 500 SG

a All diluted in water at 200 litre ha~1.

E†ects of pesticides on non-target Heteroptera in cereals 41

Fig. 1. Position and aspect of fungicide-treated plots on the study farm, Hampshire, 1989. CO \ Control ; PC \ Prochloraz ;PP\ Propiconazole ; TR\ Tridemorph.

were applied to 6 m wide] 100 m long lengths ofcereal in the outer headland, which again ran consecu-tively adjacent to hedgerows. All Ðelds had similar soiltypes and gradient. Four insecticide treatments, phosa-lone, pirimicarb, demeton-S-methyl and dimethoate,and a water control were used (Table 1) and were repli-cated three times in each Ðeld (Fig. 2). The treatmentswere allocated to 15 headland plots per Ðeld in arandom sequence and were applied with a tractor-mounted sprayer at conventional Ðeld rates (Table 1) inwater at 200 litre ha~1. Suction samples were collectedon two dates, pre-application ([2 days (29 June 1987))and post-spray (]7 days (8 June 1987)), at 3 m into thecereal outer headland. Five suction samples of 0É5 m2each containing Ðve 0É1 m2 sub-samples were collectedat each site, the samples being taken at random along atransect 3 m from the crop edge. While, again, no bu†erareas were possible between plots, the samples were col-lected within the middle 50 m of each plot, allowing a50 m treated bu†er strip between adjacent-samplingareas. The collected Heteroptera were sorted foranalysis as described above.

2.3 Statistical analysis

From the fungicide Ðeld trial, mean numbers of each

heteropteran group were calculated for each plot oneach sampling date and these were then transformed(log (n ] 1)) to stabilise the variance.22 Before analysis,pre-treatment transformed data were subtracted frompost-treatment ones to adjust for initial conditions. Thedi†erences were analysed by a split-plot analysis ofvariance (ANOVA) with 3 & 8 degrees of freedom fortreatment, 3 & 8 degrees of freedom for treatment]distance within plot interaction and 1 & 8 degrees offreedom for distance within plot. The analysis wascarried out using Genstat 5.23 If no signiÐcant treat-ment] distance interaction occurred, the ANOVA wasused to compare di†erences between pre-treatmentand post-treatment (]5 days) and pre-treatment andpost-treatment (]15 days) at 0 m and 3 m together. Ifan interaction was found, distances were treated separa-tely. If signiÐcant di†erences between treatmentsoccurred, ones between pairs of treatments were testedusing Students Least SigniÐcant Di†erence (LSD)(P[ 0É05).

For the insecticide trial, mean numbers of each het-eropteran group were calculated from the plots andthese were then transformed (log (n ] 1)) as above.Before analysis, pre-treatment transformed data weresubtracted from post-treatment ones to adjust for initialconditions. A two-way ANOVA by Ðeld and treatmentwas carried out on these plot di†erences ; if signiÐcant


Fig. 2. Position and aspect of insecticide-treated plots on the study farm, Hampshire, 1987. CO \ Control ; PI \ Pirimicarb ;PH\ Phosalone ; ME\ Metasystox ; DI \ Dimethoate.

Ðeld] treatment interactions occurred, the individualÐelds were reanalysed separately using a one-wayANOVA with 4 & 10 degrees of freedom, otherwise thee†ect of treatment was assessed on 4 & 30 degrees offreedom. As above, pairwise di†erences between treat-ments were examined by LSD only if the overall test fortreatment di†erences was signiÐcant.

Analysis was carried out on the Ðve heteropterangroups, Calocoris norvegicus, predatory species, Steno-demini, other Heteroptera and total Heteroptera.

3 RESULTS

3.1 Fungicides

In the two-way ANOVA, no signiÐcant treatment ]distance interactions were detected, therefore the twodistances were not separated in analysis for treatmentdi†erences. No signiÐcant treatment di†erences weredetected in the post-treatment (]5 days) minus pre-treatment or the post-treatment (]15 days) minus pre-


treatment data between any of the chemicals or betweenthe control for any of the heteropteran groups studied(Fig. 3).

Only one group, the “other HeteropteraÏ, exhibited asigniÐcant between-habitat di†erence, being morenumerous at the Ðeld edge (0 m) compared to the cropedge (3 m). The groups of predatory Heteroptera andthe Stenodemini also exhibited a similar but non-signiÐcant habitat preference. C. norvegicus, the overalldominant species, strongly favoured the cereal habitatcompared to the non-crop Ðeld edge ; however this dif-

ference was non-signiÐcant (Table 2 ; Fig. 4). While therewere few signiÐcant di†erences between habitats, all the26 heteropteran species found occurred in the Ðeldboundary, with 12 out of these 26 species being foundonly in this habitat, the remaining 14 species alsooccurring at 3 m in the crop (Table 3).

3.2 Insecticides

No signiÐcant Ðeld ] treatment interactions were found

Fig. 3. Mean di†erences between pre-treatment and post-treatment (]5 & ]15 days) sampling of Heteroptera (^S.E.) per 0É5 m2from within the combined distances (0 m & 3 m) in a Ðeld of winter wheat sampled in the replicated fungicide experiment (d.f. 3 &8) collected in June on the study farm in southern England. Di†erences between treatments at the P[ 0É05 signiÐcance level are

signiÐed by a di†erent letter, no signiÐcant di†erences between any treatments are signiÐed by ns.

Fig. 4. Mean di†erences between pre-treatment and post-treatment (]5 & ]15 days) sampling of Heteroptera (^S.E.) per 0É5 m2and between the two distances 0 m and 3 m in a Ðeld of winter wheat sampled in the replicated fungicide experiment (d.f. 1 & 8)

collected in June on the study farm in southern England. (P[ 0É05 \ *, P[ 0É01 \ **, P[ 0É001 \ ***, no signiÐcance\ ns).


TABLE 2Mean Numbers of Heteroptera (^S.E.) per 0É5 m2 Sampled from the Boundary (0 m) and within the Cereal Headland (3 m) in the

Field of Winter Wheat used for the Replicated Fungicide Experiment on the Three Sampling Dates

Pre-treatment ([3 days) Post-treatment (]5 days) Post-treatment (]15 days)

0 m 3 m 0 m 3 m 0 m 3 m

Calocoris norvegicus 2É43 (^0É75) 19É10 (^6É50) 2É33 (^0É83) 15É93 (^5É04) 1É19 (^0É42) 7É67 (^2É67)Predators 2É83 (^0É45) 1É63 (^0É89) 5É45 (^1É71) 2É50 (^1É34) 3É25 (^1É44) 5É04 (^2É68)Stenodemini 2É88 (^1É93) 0É25 (^0É12) 2É05 (^0É81) 0É36 (^0É17) 5É55 (^2É99) 0É74 (^0É26)Other Heteroptera 34É41 (^7É08) 0É51 (^0É18) 23É66 (^6É61) 0É88 (^0É24) 14É84 (^3É72) 2É04 (^0É34)Total Heteroptera 42É81 (8É99) 21É51 (^6É09) 33É81 (^5É41) 19É72 (^3É93) 24É74 (^3É97) 15É61 (^4É03)

for the groups Calocoris norvegicus, predatory Hetero-ptera or total Heteroptera, but signiÐcant interactionswere found between Ðelds for two groups, Stenodeminiand other Heteroptera. As a result each Ðeld was con-sidered separately for these two groups.

Calocoris norvegicus was numerically the dominantheteropteran in the headlands of all three cereal Ðelds.While all mean plot densities decreased post-treatment,the reductions were signiÐcantly greater in both the

TABLE 3Presence (]) or Absence ([) of Species of Heteroptera found

at the Field Edge (0 m) and at 3 m into the Field

0 m 3 m

Calocoris norvegicus (Gmelin) ] ]Predators Nabis ferus L. ] ]

Anthocoris nemorum L. ] ]Stenodemini L eptopterna dolabrata (Fallen) ] ]

Notostira elongata (Geo†roy) ] ]Stenodema spp. ] [

Other species found at 0 m onlyScolopostethus spp. ] [T aphropeltus contractus (Herrich-Schae†er) ] [Amblytylus nasutus (Kirschbaum) ] [Dicyphus spp. ] [Heterotoma merioptera (Scopoli) ] [L iocoris tripustulatus (Fabricius) ] [L ygus pabulinus L. ] [L ygus rugulipennis (L) Poppius ] [Piesma maculata Costa ] [Cyllecoris histionicus (L.) ] [Sehirus bicolor (L.) ] [

Other species found at 0 m and 3 mCalocoris sexguttatus (Fabricius) ] ]Himacerus mirmicoides (Costa) ] ]Orthonotus ruÐfrons (Fallen) ] ]Plagiognathus arbustorum (Fabricius) ] ]Capsus ater (L.) ] ]Pithanus maerkeli (Herrich-Schae†er) ] ]Deraecoris ruber (L.) ] ]Psallus spp. ] ]Palomena prasina L. ] ]

demeton-S-methyl and the dimethoate plots comparedto the phosalone- and pirimicarb-treated plots (Fig. 5).There was no signiÐcant di†erence between any treat-ment and the control.

There were no signiÐcant di†erences in numbers ofpredatory Heteroptera between any treatments (Fig. 5).While numbers were very low in all plots, a smallincrease did occur in many plots after treatment.

For the group total Heteroptera, as with C. nor-vegicus, greater reductions in numbers occurred aftertreatment in both the demeton-S-methyl and thedimethoate plots compared to the phosalone- andpirimicarb-treated plots, but with only the pirimicarbplots exhibiting a signiÐcant reduction. Again there wasno signiÐcant di†erence between the control and theother treatments. These results were caused by the largenumerical dominance of C. norvegicus over all the otherheteropteran groups (Fig. 5).

Treatment e†ects on the Stenodemini were comparedon an individual Ðeld basis (Fig. 6). In Field 1, numbersincreased slightly within the control, phosalone- andpirimicarb-treated plots after treatment and decreasedin both the demeton-S-methyl and dimethoate plots, thedi†erences between the former three and latter twotreatments being signiÐcant. In Fields 2 and 3 no signiÐ-cant di†erences between plot means were detected.

The group “other HeteropteraÏ, also exhibited signiÐ-cant Ðeld] treatment interactions (Fig. 7). Plot meanswere generally low in all treatments and as a result nosigniÐcant di†erences were found in Fields 2 and 3. InField 1, all plots exhibited small non-signiÐcant meanchanges, with the exception of the pirimicarb-treatedones, in which mean numbers signiÐcantly increasedafter treatment compared to all others.

4 DISCUSSION

This study, in particular the insecticide trial, encoun-tered problems common to many large-scale Ðeld trialswith replicated plots. The advantage of having similarboundary vegetation had to be o†set against having toplace the plots on two or more sides of a Ðeld, resulting


(a) (b) (c)Fig. 5. Mean di†erences between pre-treatment and post-treatment sampling of heteropteran groups (^S.E.) per 0É5 m2 fromwithin the combined headlands of the three winter wheat Ðelds sampled in the replicated insecticide experiment (d.f. 4 & 30)collected in June on the study farm in southern England. Di†erences between treatments at the P[ 0É05 signiÐcance level are

signiÐed by a di†erent letter.

in a possible e†ect of aspect on faunal diversity, eitherdirectly due to temperature or indirectly due to di†er-ences in the Ñora. Bu†er plots between the treatmentplots would have been ideal, but the need to have large

plots to reduce the possible risk of heteropteran move-ment between sampling sites was an important con-sideration. Collecting samples from the centre of eachtreatment plot and thus allowing a treatment bu†er

(a) (b) (c)Fig. 6. Mean di†erences between pre-treatment and post-treatment sampling of the heteropteran group, Stenodemini (^S.E.) per0.5 m2 from within the individual headlands of the three winter wheat Ðelds sampled in the replicated insecticide experiment (d.f. 4& 10) collected in June on the study farm in southern England. Di†erences between treatments at the P[ 0É05 signiÐcance level

are signiÐed by a di†erent letter.

(a) (b) (c)Fig. 7. Mean di†erences between pre-treatment and post-treatment sampling of the group “other heteropteraÏ (^S.E.) per 0É5 m2from within the individual headlands of the three winter wheat Ðelds sampled in the replicated insecticide experiment (d.f. 4 & 10)collected in June on the study farm in southern England. Di†erences between treatments at the P[ 0É05 signiÐcance level are

signiÐed by a di†erent letter.


should have minimised movement from adjoining treat-ments.

The results from these Ðeld trials conÐrmed thosefound in laboratory screening trials for the e†ects ofpesticides on C. norvegicus nymphs19 and also quanti-Ðed the Ðeld e†ects of fungicides and insecticides on agreater range of non-target Heteroptera. When appliedat Ðeld dose-rates to cereal Ðeld-dwelling Heteroptera,the three commonly used fungicides caused no signiÐ-cant reductions in numbers. No heteropteran speciesare recorded as being obligate mycetophages, thereforeindirect e†ects via depletion of fungal food resourceswould not be expected.

While these results showed that many fungicides willhave no signiÐcant e†ect on heteropteran populations,speciÐc formulations have been shown to have insecti-cidal properties that signiÐcantly reduce populations ofbeneÐcial arthropods in cereal Ðelds. For example theorganophosphate fungicide pyrazophos possesses sig-niÐcant insecticidal properties to a range of non-targetspecies.24h29 Sub-lethal doses of fungicides have alsobeen shown to a†ect some invertebrates.30

However, as important as this study may be inexamining the impacts of fungicide use, it is perhapsalso important in showing the potential diversity withinthis heteropteran group. All heteropteran species foundoccurred in the Ðeld boundary and 12 out of these 26species were found only in this non-cropped habitat.While 14 out of the 26 species were found 3 m into thecereal crop (Table 3), C. norvegicus, the numericallydominant species in both habitats, was the only speciesto feed on the cereal itself with 85% of the sampledpopulation occurring within the crop (Table 2, Fig. 4).

Insecticides are regularly used in cereal Ðelds at atime when C. norvegicus and many other heteropteranspecies are active within the crop. The di†ering levels ofmortality found between insecticide treatments in thisstudy and many others4h7,18h22, 24h36 indicate that thechoice of active ingredient could have an importantimpact on the abundance of Heteroptera and thus theiravailability as food for farmland birds.

In both the laboratory19 and this Ðeld study (Figs 5,6 & 7), the use of the two chemicals phosalone and piri-micarb resulted in only small non-signiÐcant changes innumber of C. norvegicus and other Heteroptera,whereas the use of demeton-S-methyl and dimethoatecaused larger and often signiÐcant short-termreductions. High levels of mortality have also beenrecorded in the IOBC/WPRS, “Joint Pesticide TestingProgrammesÏ4h7 when dimethoate was tested againstAnthocoris spp. using the recommended Ðeld rate.Similar results have been found for other non-targetspecies eaten by young birds, including Carabidae andLycosidae when treated with aphicides applied at therecommended dose rates approved for summer use inthe UK.31 Pirimicarb was not toxic, with very low mor-tality levels being found in laboratory and Ðeld tests

among both carabids and lycosids. However dimethoatewas found to be very toxic to the carabid Pterostichusmelanarius (Illiger), resulting in high levels of mortality,and it caused varying levels of mortality to spiders.Dimethoate has also been found to reduce densities ofmost non-target arthropod groups in cereals32 and tohave a considerable impact on densities of sawÑylarvae33,34 (Symphyta : Tenthredinidae), another impor-tant Galliform chick-food group.10

While the laboratory studies only examined mortal-ity following contact, any estimates of impact in theÐeld were likely to be as a result of exposure followingdirect contact during spraying and by contact withspray residues on vegetation surfaces. Dimethoate hasbeen found to be toxic to carabids, resulting in varyinglevels of mortality for at least six to nine days on cerealfoliage and soil,35 and spray deposits from bothdemeton-S-methyl and dimethoate on winter wheat Ñagleaves remained signiÐcantly toxic to beneÐcialinvertebrates for four to seven days.36 Some compoundssuch as dimethoate are also known to have systemicproperties which may have contributed to the highlevels of mortality observed, especially among sap-feeding Heteroptera.

No species occurred only within the crop itself, butsome chemicals could potentially have a detrimentalimpact on populations of certain species such as theheteropteran predators which occurred in low numbersin both habitats (Table 2). SigniÐcant long-termreductions of species such as C. norvegicus, which haspopulations of both nymphs and adults found predomi-nantly within the crop during the summer rather thanin the Ðeld boundary, are also likely (Table 2 & Fig. 4).Like many other heteropteran species, C. norvegicus isunivoltine and the nymphal population of this species isfound mainly concentrated within the headland zonewithin the Ðrst 6 m from the Ðeld boundary.37 The lowmobility of nymphs suggests that large reductions indensities following treatment with insecticides could notreadily be replaced by dispersal from surroundingunsprayed areas and could a†ect population levels overlarge temporal and spatial scales.

Within the Ðeld some reductions in non-targetarthropod densities following pesticide applications willbe inevitable. However, this study shows the importanceof correct spraying procedures to avoid pesticide driftinto the boundaries where heteropteran diversity wasgreatest (Tables 2 & 3; Fig. 4) and the potential value ofkeeping insecticides out of a headland zone (at least 6 mwide), which has been shown to act as a bu†er againstany potential drift into the Ðeld edge.38h41

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the effects of pesticides on species of non-target heteroptera inhabiting cereal fields in southern...

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