J. Asia-Pacific Entomol. 8(2): 175-183 (2005)www.entomology.or.kr

ECOLOGY AND BEHAVIOR

Interaction of English Grain Aphid, Sifobionavenae(F.) and Their Natural Enemiesto an Agro-forestry Environment

Naeem Muhammad', Steve Compton', L.D. Incoll', Waseem Akram* and Jong-Jin Lee

Faculty of Biological Resources Science, Chonbuk National University, Chonju 561-756 KoreaI Department of Entomology, University of Arid Agriculture, Rawalpindi, Pakistan

2Department of Biology, University of Leeds, Leeds, England

Abstract The agro-forestry landscape can influencethe distribution of wheat-feeding aphids and theirnatural enemies. Aphid population densities weresignificantly higher in the arable control areas com­pared to the arable alleys. The ratio of alate toapterous adults indicated that relatively higher num­bers of alates were found in the control areas. Theapterous S. avenae adults and nymphs combinedwere found to constitute approximately 97 % and98 % of the total from the arable alleys and arablecontrol areas respectively. Parasitism rates (the pro­portion of aphids that were mummified) were12.80% and 7.60% in the arable alleys and controlareas respectively. In contrast, the numbers of mum­mies per aphids were found to be lower in the arablecontrols. The small-scale variation in the distance ofplants from the tree rows did not significantly in­fluence insect abundance.

Key words agroforestry environment, natural enem­ies, Sitobion avenae

Introduction

Wheat (Triticum spp.), belonging to the Poaceaefamily, is one of the most important cereal crops.It is a staple food ofmankind (Langer and Hill, 1991),and also used for livestock feed and the manufactu­ring of industrial products. The English Grain Aphid,Sitobion avenae (F.) is potentially the most importantpest of cereal crops in Yorkshire, England. It is amonoecious and generally holocyclic species, but hasa tendency to produce anholocyclic over wintering

·Corresponding author.E-mail: apwaseemI8@yahoo.comTel: +82-63-270-2528

(Received April 13, 2004; Accepted March II, 2005)

individuals (Leather, 1993). Its virginoparae over wi­nter on wheat, barley and various grasses in SouthernEngland (Hand, 1982; Dean, 1974a). It can rapidlyincrease in numbers during the few weeks betweenthe onset of wheat flowering and the 'milky-ripe'stage. It feeds mainly on the leaves and ears, causingdamage not only by sucking nutrients from the plant,but also by transmitting viral diseases (Blackman,1974), although only mild strains of barley yellowdwarf virus (BYDV) are transmitted by the Englishgrain aphid (ADAS, 1982).

The environmental factors, temperature, rainfall andnatural enemies all influence the population dynamicsof aphids on crop plants (Dean, 1974a; Potts andVickerman, 1974; Jones, 1979). The cereal aphids areattacked by a wide range of both parasitoids and pre­dators (Naeem et al., 2002). Among the most impor­tant of these are aphidophagous hoverflies (Diptera:Syrphidae), whose larvae are voracious predators ofaphids (Rotheray, 1983). Syrphids have diverse lifecycles and phenologies, with some preferring thespring aphid peak on trees and others the early summerpeak in aphid populations on herbs. A single syrphidlarva can consume large numbers of aphids in a shortperiod of time and they have been shown to beimportant in the control of aphid numbers in fieldcrops (Chambers et al., 1986). In cereals, Episyrphusbalteatus (DeGeer) is the commonest species in Eur­ope, and its time ofemergence and population increaseare associated with the peak of abundance in aphidpopulations.

Parasitoids sometimes heavily infest cereal aphids(Stary, 1966) and are considered to be particularlyimportant at the beginning of aphid population cyclesbecause they appear earlier than predators (Laska,1984). Parasitoids are themselves attacked by a rangeofhyperparasitoids. Dean (1974a) noted that Aphidiusspp. seemed to be particularly prone to attack by thehyperparasitoid Asaphes vulgaris Walker when theyparasitised S. avenae.

176 J. Asia-Pacific Entomol. Vol. 8 (2005)

Hawthorn hedge with some shrub specie"

Block 2

/N control j

~--------~ connol J

~---------~

Copse(mostly pine and beech)

Block 3

Road

-"1*1'1"control. 4 __

~-=--=--=-J ===

Meteorological station

L~L==::"====~.~ Hawthornhedge

Fig. 1. Layout of the experimental site at the Leeds University Farm at Bramham innorthern England. The experimental site consists of the four agroforestry, four forestrycontrols and four arable controls areas. Tree species in the rows and forestry controls:A, ash; C,cherry; H, hazel; S, sycamore.

The degree of crop diversity within agro-ecosys­terns can strongly influence the abundance of paras­itoid and predator species (Powell, 1983). A silvoa­rable agroforestry system has a much higher structuraland floristic diversity than conventional arable land(Naeem et al., 1994). The tree rows also act as wind­breaks, creating a sheltered environment and thusenhancing the landing and accumulation of insects(Naeem et aI., 1997; Lewis, 1969; Lewis and Stephe­nson, 1966; Lewis and Dibley, 1970). The activityof natural enemies, and levels of parasitism in pestpopulations are often increased in systems whichemploy intercropping or mixed cropping, in compari­son to the more usual system of monocultures (Altieriet al., 1978; Risch, 1979; Altieri and Todd, 1981).These increases in levels of natural enemies have beenattributed to the plentiful supply of nectar and hone­ydew resulting from the increased availability of wildflowers. Haslett (1989) found that adults of E. bal­teatus hoverflies feed both on woodland flowers, andthose associated with field margins. It has been obse­rved that E. balteatus preferentially visits certain flo­wers associated with field margins (Cowgill et al.,1993).

The research described here on the interactionbetween wheat-feeding aphids, their natural enemiesand an agroforestry landscape had the following obje­ctives:

1. Determination of the responses of wheat-feedingaphids and their natural enemies to an agroforestrylandscape, and investigate whether these insects

respond differently to agroforestry treatments.2. To determine if small-scale variations in distance

from trees influences the densities of both aphidsand their natural enemies.

Materials and Methods

The fieldwork was carried out at the Leeds UniversityFarm at Bramham in northern England. In 1987 asilvoarable agroforestry system was established at thesite, consisting of four replicate blocks each conta­ining an agroforestry area, a forestry control area, andan adjacent arable control area (Fig. 1) (detail in Penget al., 1993; Naeem and Compton, 2000). Both thearable alleys and arable control areas in the silvoarableagroforestry system were sown with a wheat crop(Triticum sp. cv. Rialto) on October 6, 2001 and subse­quently harvested between August 8 and 11, 2002.

Sampling methods

Every week between May-August 2002, aphid num­bers were counted on the wheat and the samples weretaken within the second, third and fourth arable alleysand arable control areas of blocks 1-3. In addition,during the period of peak population densities, samp­les were also taken in the 1st and 5th arable alleys,and arable control areas of all four blocks (1-4), withcounts made per ear rather than per plant.

Responses of English grain aphid 177

Table 1. Composition (%) of the aphid forms in the arablealleys (borders, quarters and middle alleys) and the arablecontrol areas of the wheat crop

(Table 1). A total of 14,505 aphids were counted onthe marked plants, ofwhich 8,398 were from the arablealleys (border, quarter and middle alleys) and 6,107from the arable control areas. Over 99 % of the totalnumber of aphids collected were S. avenae, both inthe arable alleys and arable control areas, theremainder were S. graminum. Adult apterae and nym­phs of S. avenae were collected more frequently thanalates, with totals of 8,129 and 5,884 (apterae andnymphs pooled) in the arable alleys and arable controlareas respectively. From the ear surveys, a total of3,046 aphids were recorded, of which 1,471 aphidswere in the arable control areas and 1,575 in the arablealleys (first and fifth arable alleys). The apterous S.avenae adults and nymphs combined were found toconstitute approximately 97 % and 98 % of the totalfrom the arable alleys and arable control areas resp­ectively.

Whole plant samples

A total of 108 plants were selected at randomly andmarked at the start of the sampling period. Theseplants were visually examined at weekly intervals forthe presence of aphids and their natural enemies bet­ween May and August. The sampling dates were May9, 16 and 25, June 2, 6, 13, 20 and 28, July 7, 13,20 and 26 and August 2. A total of 27 plants weremarked in each of the three replicate agroforestryplots, giving a total of 81 plants, comprising 384 ste­ms, with an additional 27 plants (132 stems) markedin the control areas.

Agroforestry Blocks 1-3Alley 2 alley border (( X 3 samples)

quarter alley (( X 3 samples)middle alley (( X 3 samples)

Alley 3 as aboveAlley 4 as above

Control Plots 1-3 (( X 9 samples)

Counting of the aphids and their natural enemiesbegan at the time of immigration to the crop andcontinued at weekly intervals until the collapse of thepopulations.

Collection from individual ears

Apbidspeciesand morpbs

S, aVellae (alates)(apterousadults)

(nympbs)S. graminum

ArablealleysAlleyborders Quarteralleys(n = 3,588) (n = 2.286)

3.23 3321438 143982,02 82,100,36 0,17

Middlealleys(n = 2,524)

237143883,240,00

Control areas(n = 6,107)

3,6012.5783,770,04

To obtain counts of individual .ears' , samples weretaken on a •per ear basis' in the 1st arable alley (betw­een the forest area and first tree row) and 5th arablealley (between the 4th tree row and the windbreak),and arable control areas of blocks 1-4. These ears wereexamined in week 27 (July 10), when aphid densitieshad just begun to decline. A total of 144 ears wereselected at random.

Agroforestry Plots 1-4Alley 1 alley border (( X 6 ears)

middle alley (( X 6 ears)Alley 5 as above

Control Plots 1-4 (( X 12 ears)

Results

The insects present on winter wheat

Aphid numbers

S. avenae was the dominant species in both the arablealleys and arable control areas of all three blocks

Aphid mummies

A total of 249 mummified aphids were counted, ofwhich 48 mummies were in the arable control areasand 201 in the arable alleys. From the ear surveys,a total of 30 mummified aphids were counted. Therewere 16, 12 and 2 in the first and fifth arable alleys,and arable control areas, respectively. Overall, thepercentage of parasitism (the proportion of aphids thatwere mummified) was 10.20%, estimated by includingalate and apterous adult aphids.

Aphid predators

Few aphid predators were observed on the markedwheat plants. A total of 34 individuals, comprising27 coccinellids (17 larvae and 10 adults), one lacewingadult, three syrphid larvae and three syrphid pupaewere recorded. Adult ladybirds comprised three 7-spotladybirds (Coccinella 7-punctata), and seven 14-spotladybirds (Propylea 14-punctata). In addition, 20 pos­sibly predatory red mites were recorded, of whichfourteen red mites were from the arable alleys andsix from the arable control areas. A total of elevenfungal-attacked aphids were also counted, of whichfour were from the control areas and seven from thearable alleys.

arable control areas than in the arable alleys (Fig. 2-4).The numbers of S. graminum were very low and nosignificant effects were present both in the treatmentand treatments within blocks (F[I,1349j = 0.11, P = 0.742and F[4,1349j = 1.82, P = 0.12 respectively).

The numbers of S. avenae observed in the surveysof individual's ears were greater in the arable controlareas, compared to the arable alleys. These effectswere generally significant, when tested with nestedANOYA' s between the arable alleys (first and fifth

178 J. Asia-Pacific Entomol. Vol. 8 (2005)

Insect phenologies

The population densities of S. avenae were monitoredweekly between May and August 2002. The aphidswere first observed on the crop during week 20(mid-May), and reached their maximum by week 27(early July). This peak was consistent among alates,apterous adults and nymphs, in both the arable alleysand arable control areas (Figs. 2-4). After the popu­lation peak, there was a sharp decline in numbers withpopulations disappearing by the end of July. Alates,apterous adults and nymphs showed very similartrends in the three sections of the arable alleys exa­mined (border, quarter and middle alleys) and thearable control areas (Fig. 5), with population sizesall peaking at the same time except in the quarter alleyswhere alates peaked in week 28 (mid July). The smallnumbers ofS. graminum observed in the samples wereonly present during May.

The first mummified aphids were detected at theend of May in the arable alleys and the first weekof June in the control areas. The highest densities ofmummies were observed in July, when aphid popula­tions were at their maximum: Likewise' the highestnumbers of coccinellids and syrphid predators werealso recorded in July.

Comparisons between the densities of inse­cts in the arable alleys and arable controls

12

10

8

6

4

2

all blocks --0-· arable alleys

control areas

I

Based on whole plant surveys, the numbers of S.avenae (all morphs) were significantly greater in the

Fig. 3. Numbers of apterous S. avenae adults (Mean/plant ± 1 standard error) in relation to agroforestrytreatment, based on visual surveys.

all blocks3.0

--0- arable alleys-<>- control area~

80

all blocks -0- arable alleys~~o.--- control areas

2.5

2.0

~E 1.5E.z.

1.0

0.5

0.0i i i i i i i i

18 20 22 24 26 28 30 32weeki i

May June July August

60

20

o

T

i i i i i i i i

18 20 22 24 26 28 30 32week

i i i

May June July August

Fig. 2. Numbers of alate S. avenae (Mean/plant± I standard error) in relation to agroforestry tre­atment, based on visual surveys.

Fig. 4. Numbers of S. avenae nymph (Mean/plant± I standard error) in relation to agroforestry tre­atment, based on visual surveys.

Responses of English grain aphid 179

arable alleys) and arable control areas, and for treat­ment effects within blocks. Alates were the exception,with no differences between densities in the first andfifth alleys.

The ratio of apterous to alate S. avenae tended tobe greater in the arable alleys than the arable controls.However, this effect was inconsistent and not signif­icant between treatments and treatments within blocks(F[I,83] = 1.07, P = 0.30 and F[4,83j = 1.07, P = 0.92respectively).

Parasitism rates (the proportion of aphids that weremummified) were 12.80% and 7.60% in the arablealleys and control areas respectively. Significant eff­ects were found between treatment (F[I,593j = 6.09, P< 0.01) and treatments within blocks (F[4,593j = 2.65,P < 0.03). An analysis of the mummified aphids(emerged, intact and empty) was tested with nestedANaYA's between treatment and within blocks.More mummified aphids were found in the arablealleys than in the arable control areas, despite thesmaller number of aphids present there. Effects weresignificant between treatments within blocks only(F[4,1403] = 6.83, P < 0.001).

ers of S. avenae were not significantly different betw­een the three sections of the arable alleys althoughtreatments within blocks were significantly different.Apterous adult to alate ratios varied inconsistentlywithin different sections of the arable alleys, and nosignificant effects were observed (F[2,62] = 0.32, P =

0.72).The percentage parasitism was marginally greater

in the alley borders than the quarter alleys and middlealleys, (16.09%, 11.23% and 10.67% respectively),although no significant effects were found within thetreatments (F[2,416] = 1.93, P = 0.14).

Significant differences of mummified aphids wereonly observed between the treatments within blocks.Comparison between the three sections of the arablealleys revealed that greater numbers were recordedin the alley borders than either the quarter or middlealleys.

The distribution of aphid numbers betweenarable alleys (tst and 5th) within the sameblocks

Comparisons of the densities of insects wit­hin the three sections of the arable alleys(border, quarter and middle alleys)

The mean densities of S. avenae (all morphs) werealmost always higher in block I throughout all threesections of the arable alleys (alley borders, quarteralleys and middle alleys) (Fig. 5). Overall, the numb-

The densities of S. avenae differed significantlybetween blocks in the first arable alleys (nearest tothe forest areas), but there were no significantdifferences between blocks in the 5th arable alleys(furthest away from the forest areas) (Fig. 6). Thepopulation densities ofS. avenae were greater in thefifth than the first arable alleys, except for block 3,and treatment effects within blocks were significant(F[6,95j = 2.17, P < 0.05), but no significant differences

AugustJuly

i • I

June

Fig. 6. Comparison between the mean temperat­ures in the close field meterological station ofblock I and at the main outstation in an open fie­ld in 1995.

12

I I I I I I j I , I I

23 24 25 26 27 28 29 30 31 32 33

week

-0-- Meterological station in dose field

'" Meterological station in open field

-2 18~

tF 16

E!!

20

22

14

o amblealleysD controlareas

T

aJlblocks

16

14

12

10.BE

8:Z6

4

2

0alates apterae nymphs

Fig. 5. Numbers of S. avenae (Mean/plant ± Istandard error) in the arable alleys and arable co­ntrol areas, based on visual observations.

180 J. Asia-Pacific Entomol. Vol. 8 (2005)

were found between treatments (F[I,9s] = 0.22, P =0.64).

Discussion

The research focused on the study of the populationdynamics of wheat-feeding aphids and their naturalenemies in an agro forestry landscape. S. avenae wasthe only aphid species found in abundance, both inthe arable alleys and the arable agro forestry controlareas, and it was found that these habitat differencesstrongly influenced population densities of this aphid.

The distribution pattern ofS. avenae was influencedby the agro forestry treatments. Results based on plantsurveys showed significantly higher aphid densitiesin the arable control areas than in the arable alleys.

A micro-meteorological station was located in the3rd arable alley of block 1, and the main meteoro­logical station, which was situated between the 2ndand 3rd agro forestry blocks (Fig. 1). The presenceof trees in an agro forestry system has direct effectson temperature, wind speed and atmospheric moisture(Peng et al., 1992). The effects of climatic conditions(particularly temperature and wind) are critical toaphid outbreaks (Barbosa and Schultz, 1987). The dif­ference in the pattern of aphid distribution within theagro forestry treatments could therefore result frommicroclimatic variations between the arable alleys andthe control areas. Dean (1974a) observed that aphiddevelopment rate and reproduction increases with thetemperature, within the range of 10-20°C, and theincreased aphid population densities recorded in thehot year 1976 were in direct response to the highertemperatures observed in that year (Carter et al., 1980).The oviposition rate of Toxoptera graminurn Rondincreases with increasing temperature to a maximumof approximately25°C (Romoser and Stoffolano, 1994).The observed increase in both the rate of reproductionand development for S. avenae agrees very well withthe literature. The lower abundance of aphids in thearable alleys is therefore probably attributable, at leastin part to a relatively lower temperature.

Wind movement differences may be just as imp­ortant. Several studies have already suggested thatwind movement affects the settling rate, landing, anddistribution of both alate aphids, and other insects(Hagen, 1962; Lewis and Stephenson, 1966; Lewis,1967; Dean and Luuring, 1970; Lewis and Dibley,1970; Kennedy and Thomas, 1974; Willard, 1974;Moran et al., 1982). Small flying insects are distributedalmost randomly by air currents away from the imm­ediate vicinity of vegetation (Lewis and Taylor, 1967),and mean wind speeds at the crop level over periodsof days or weeks influence the patterns of aphid

distribution in the air and on the crops in the vicinityof windbreaks (Lewis and Stephenson, 1966). Thedispersal of flying aphids is influenced by air mov­ements around the barriers and along the edges ofthe crops (Johnson, 1950; Taylor and Johnson, 1954).The distribution patterns of airborne insects within thesheltered crops and in the air rely mainly on boththe height and permeability of windbreaks, and theirorientation to prevailing winds (Lewis, 1967, 1969,1970; Lewis and Dibley, 1970; Lewis and Smith,1969; Lewis and Stephenson, 1966 and Smith andLewis, 1972). Taylor (1974) defined the 'insect boun­dary layer' as the layer ofair in which airborne insectsare able to control their movement, comparative tothe ground, when wind speed is less than air speed(Pedgely, 1982). Duelli (1980) and Lewis (1967)supported the concept of the insect boundary layer,and this provided a basis for classifying the migratoryflights of aphids (Taylor and Palmer, 1972). Thedistribution patterns of airborne insects may beinfluenced by the wind speed, permeability of thewindbreak, turbulence and vegetation composition(Pasek, 1988). The wind speed in the sheltered fieldis influenced by windbreaks, tree rows and trees inthe forestry control plots. Higher wind speed was reco­rded by the main (open field) meteorological stationthan the micro-meteorological station (close field) inthe agro forestry area, even though the height of theanemometer of the micro-meteorological station washigher (Naeem, 1996). Wind speed increases with hei­ght more or less logarithmically (Pedgley, 1982). Pass­ing through the vegetation thus decreased wind speed.A slight difference in wind direction data recordedby the two meteorological stations (Naeem, 1996). Sothe putative higher landing rate of alate aphids obse­rved in the arable controls compared to the arablealleys may be attributed to higher wind speeds.

From the meteorological results, therefore, twopossible influences on aphid landing pattern areapparent. Firstly, wind speed differences may havecaused a higher settling rate of the alate aphids inthe arable control areas than the arable alleys, sincethe presence of trees reduces the wind speed in thearable alleys resulting in a decrease in amount of air'sampled' by the crop and therefore a reduction inthe setting rate of the alate aphids (Fig. 6). Secondly,the presence of trees may not only slow down windspeeds but may also act as a physical barrier, whichfacilitates the landing of alate aphids between thearable alleys. Strong (1984) has observed that smallinsects, like aphids, are particularly affected in thisway. Both could act in combination with the recordedtemperature effects.

It was also observed the natural enemies; especiallyparasitoids may reduce the aphid population densitiesin the alleys, although there were few significant

Responses of English grain aphid 181

all blocks

12 12

.s 10 .2 10

e e~ 8

Q)

8~'il 'il.s .sgj 6 e 6a ~

~ 4 ~ 4

2 2

0 i I i i i 0 i i

26 28 30 32 34 26 28week

~ quarter alleys~controlareas

all blocks

12

.910

~...~ 8'il0....g; 6til....~ 4

2

0 i i26 28

~-middle alleys-control areas

all blocks

12

.9 10

eQ)

8~'il0....~ 6til~ 4

2

0 i i26 28

'"-~- arable alleys-control areas

Fig. 7. Apterous adults: alates ratios of S. avenae in the arable alleys and arable control areas, based on plant surveys.

differences in the arable alleys or arable control areas.The parasitism rates were 2.39% and 0.78% andpredation rates were 0.27% and 0.09% in the arablealleys and in the arable control areas respectively, sothese effects were relatively small.

Analyses of individual ears showed significantlyhigher densities of aphids in the fifth arable alleyscompared to the first arable alleys in blocks 1 and2. In contrast, parasitism rates were 2.5%, 1.68%, and0.15% in the first and fifth arable alleys, and thecontrol areas respectively. This could be due to thelocation of the first arable alley, which lies between

the forest control areas and the first tree row. Becausethe forest control areas consist of abundant trees, thismay provide more favourable conditions for naturalenemies, resulting in higher rates of parasitism. Thelower parasitism observed in the arable control areasmay therefore also reflect the scarcity of trees.

Overall the results showed that a silvoarable agroforestry landscape can have a major role in thedistribution of these crop pests. The combined prese­nce of the tree rows, forest control plots and thewindbreaks therefore contributed to reducing aphidnumbers.

182 J. Asia-Pacific Entomol. Vol. 8 (2005)

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