Directory UMM :Data Elmu:jurnal:A:Agriculture, Ecosystems and Environment:Vol83.Issue1-2.Jan2001:

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Biotypic differences in Russian wheat aphid (Diuraphis noxia)

between South African and Hungarian agro-ecosystems

Zsuzsa Basky

a,∗

_{, Keith. R. Hopper}

b

_{, Jorrie Jordaan}

c

_{, Tanya Saayman}

d a_{Plant Protection Institute, Hungarian Academy of Sciences, P.O.Box 102, Budapest 1525, Hungary} b_{Beneficial Insects Introduction Research Unit, ARS-USDA, University of Delaware, Newark, DE, USA}

c_{Sensaco Cooperative Ltd., P.O.Box 556, Bethlehem 9700, South Africa}

d_{Agricultural Research Council, Plant Protection Research Institute, Private Bag X134, Pretoria 0001, South Africa}

Received 31 December 1999; received in revised form 18 July 2000; accepted 1 August 2000

Abstract

The effect of Russian wheat aphid Diuraphis noxia (Mordvilko) from South Africa and Hungary was measured on suscepti-ble and resistant South African wheat cultivars and a susceptisuscepti-ble Hungarian barley cultivar. For the three cultivars (‘SST 333’, ‘Betta’, and ‘Isis’) tested in both countries, Hungarian D. noxia reduced plant weight and leaf area more than South African D. noxia and this difference increased over time. Hungarian D. noxia reduced plant weight and leaf area of the resistant wheat SST 333 more than the susceptible wheat Betta. Hungarian D. noxia also reduced plant weight of the resistant wheat ‘PI 262660’ more than the susceptible wheat Betta (although the opposite was true for leaf area). In Hungary the resistant SST 333 and PI 262660 showed similar severe symptoms of yellowing and leaf rolling as susceptible Betta. In addition, Hungarian D. noxia caused visible water imbalance in resistant wheats SST 333 and PI 262660. The differences in damage did not result from higher growth rate of Hungarian D. noxia colonies because aphid numbers did not differ consistently between countries or match the differences in damage. Differences between Hungarian and South African D. noxia suggest genetic differences between these populations. These results support the idea that resistant plant germplasm has geographical limits because of variation in agro-ecosystems. © 2001 Elsevier Science B.V. All rights reserved.

Keywords: Russian wheat aphid; Diuraphis noxia; Plant weight; Leaf area; Biotypic variation; South Africa; Hungary

1. Introduction

The Russian wheat aphid, Diuraphis noxia (Mord-vilko) (Homoptera: Aphidaidae), was first recorded as a pest of cereals by Mokrzhetsky (1901). It has not subsequently been a persistent pest in Eurasia, its area of origin, although short-lived outbreaks have been re-ported (e.g. Grossheim, 1914; Tuatay and Remaudiere, 1964; Dyadechko and Ruban, 1975; Fernandez et al.,

∗_{Corresponding author. Tel.:}₊_{36-1-3-769-555/618;}

fax:+36-1-3-769-729.

E-mail address: [email protected] (Z. Basky).

1992). D. noxia was first detected in Hungary in 1989 by Basky and Eastop (1991), but it has not become a pest. However, after its discovery in South Africa in 1978 and in the US in 1986, D. noxia became a major pest of cereals in these countries (Du Toit and Wal-ters, 1984; Brooks et al., 1994). Intensive resistance breeding programs were undertaken in South Africa and the United States to reduce D. noxia damage (Du Toit, 1989; Webster et al., 1987; Webster, 1990; Miller et al., 1994). Biotypic variation can affect the success of such breeding programs (for review see Diehl and Bush, 1984). Puterka et al. (1992) showed variation in damage to resistant wheat cultivars among eight

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D. noxia collections from several regions throughout the world, suggesting that biotypic variation may ex-ist in D. noxia. In this paper, results of experiments on differences in plant development as a result of at-tack by South African and Hungarian D. noxia are re-ported. Because of the risk of introducing potentially damaging biotypes into South Africa and Hungary, D. noxia could not be transferred between the two coun-tries. Therefore, the effects of infestation by locally collected D. noxia in South Africa and in Hungary were compared. Plant weight and leaf area of South African wheat cultivars considered susceptible and re-sistant to D. noxia and a Hungarian barley cultivar considered susceptible to D. noxia were studied.

2. Materials and methods

2.1. Sources of aphids

In South Africa, D. noxia viviparous apterae and nymphs were collected at the beginning of November from wheat at Zadoks growth stage 65–69 (anthe-sis half finished to anthe(anthe-sis complete) (Tottman and Broad, 1987) in the main South African wheat grow-ing area near Bethlehem, Orange Free State. Before the experiments, the aphids were reared for 10 gener-ations on seedlings of wheat cultivar ‘Betta’ at 20◦C and photoperiod ∼14:10 (L:D) h at 5000–15,000 lx at the Sensaco Cooperative Breeding Station. In Hungary, D. noxia fundatrices were collected in the middle of April from wheat at growth stage 30–35 (stem elongation) near Szolnok, which is at the centre of the main wheat growing area in Hungary. Before the experiments, the aphids were reared for 10 gen-erations on wheat cultivar ‘Bezostaja’ at 20◦C and photoperiod 14:10 (L:D) h at 7500–8500 lx.

2.2. Treatments

To test differences between the effects of South African and Hungarian D. noxia, experiments were done in both countries with the South African win-ter wheat cultivars Betta (susceptible to D. noxia) and ‘SST 333’ (resistant to D. noxia) (Du Toit, 1989) and the Hungarian spring barley cultivar ‘Isis’ (suscepti-ble to D. noxia). Because feeding by Hungarian D. noxia caused leaf rolling and streaks in the resistant SST 333, an additional experiment was done in

Hun-gary to compare the effects of Hungarian D. noxia on Betta, SST 333, and another D. noxia-resistant wheat line ‘PI 262660’. PI 262660, in which resistance is from a single dominant gene Dn2 (Du Toit, 1989), is the source of resistance in SST 333.

In each experiment, 16 seeds were sown in each of eight pots (17 cm diameter in Bethlehem (South Africa) and 15 cm in Budapest) for each cultivar. Af-ter emergence, seedlings were thinned to 12 seedlings per pot. Six days after plant emergence (i.e. at growth stage 11), the plants in half the pots were infested with one D. noxia apterae (7 days old) per plant. In South Africa, experimentation was undertaken in a temperature-controlled greenhouse at 20–14◦C (day–night) with a photoperiod of ∼14:10 (L:D) h at 5000–15,000 lx. Plants were placed in cages, with glass fronts and sides and with fine mesh screens covering the top and the back of the cages. Infested and uninfested plants were in separate cages. The plants were irrigated by an automated system with 40 ml water per pot three times per day giving a total of 120 ml per day. In Hungary, the plants were kept in a greenhouse at 24–13◦C (day–night) with a pho-toperiod of ∼14:10 (L:D) h at 5000–15,000 lx. The plants were watered twice per day with 60–70 ml wa-ter giving a total of 120–140 ml per day. In Hungary, infested and uninfested pots were covered with 20 cm high transparent cages. Ventilation holes and cage tops were covered with fine-mesh organza.

2.3. Measurements

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2.4. Data analyses

Because of potential interaction among plants within pots, infested pots were considered the smallest experimental units; the four plants sampled from each pot on each date were sub-samples. Therefore, values of plant weight, leaf area, and number of aphids were averaged across the four plants sampled from a pot on a given date. Because the goal of this research was to compare the effect of Hungarian and South African D. noxia on each cultivar, the differences between infested and uninfested pots were used as dependent variables. This allowed correction for differences in growing environment between countries independent of differences in aphid population. Thus for plant weight and leaf area, the observed value of infested pots was substracted from the mean value of unin-fested pots for each combination of country, cultivar, and sample day. Because the same pots were sampled across dates, repeated-measure analysis of variance was used to test the effects of country, sample day, and their interactions on the difference in plant weight and the difference in leaf area between infested and uninfested pots of each cultivar. Repeated measure analysis of variance was also used to test the effects of country, sample day, and their interaction on number of aphids per plant for each cultivar. The means were compared between countries for each sample day us-ing Bonferroni’s adjustment of comparison-wise error rate to maintain experiment-wise error rate at 0.05 (Milliken and Johnson, 1992). For comparison among cultivars in Hungary, repeated-measure analysis of variance was used to test the effects of cultivar, sample day, and their interactions on the difference in plant weight and the difference in leaf area between infested and uninfested pots of each cultivar. All analyses were done with SAS statistical software (SAS, 1992).

3. Results

3.1. Plant weight

For all three cultivars tested in both countries, Hun-garian D. noxia reduced plant weight more than South African D. noxia (Fig. 1; Table 1(a)). The difference in plant weight between uninfested and infested pots increased with the time aphids were on the plants.

Fig. 1. Difference in plant weight between uninfested plants and plants infested with D. noxia for resistant (SST 333) and suscep-tible (Betta, Isis) cultivars in Hungary and South Africa.

The differences between countries also increased over time, as is revealed by significant interactions between country and sample day. The difference in reduction of plant weight between countries was less for Isis than for Betta and SST 333, which showed similar differ-ences in plant weight between countries (Figs. 1–3, error bars are±2S.E.; asterisks indicate sample days on which the means for Hungary and South Africa differed significantly using the Bonferroni correction to control experiment-wise error rate).

3.2. Leaf area

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Table 1

Analysis of variance for the effect of country, sample day, and their interaction on the difference in (a) plant weight and (b) leaf area between plants infested with D. noxia and uninfested plants

Plant cultivar Factor df F P

(a) D. noxia effect on plant weight

Betta (wheat) Country 1, 8 35.74 0.0003 Sample day 2, 16 179.11 0.0001 Country×

sample day

2, 16 194.24 0.0001

SST 333 (wheat) Country 1, 8 41.07 0.0002 Sample day 2, 16 58.84 0.0001 Country×

sample day

2, 16 28.71 0.0001

Isis (barley) Country 1, 8 90.95 0.0001 Sample day 2, 16 241.60 0.0001 Country×

sample day

2, 16 9.61 0.002

(b) D. noxia effect on leaf area

sample day

2, 16 422.47 0.0001

sample day

2, 16 688.23 0.0001

sample day

2, 16 3075.81 0.0001

both countries, Hungarian D. noxia reduced leaf area more than South African D. noxia (Fig. 2; Table 1(b)). The difference in plant weight between uninfested and infested pots increased with the time aphids were on the plants. The differences between countries also in-creased over time, as is revealed by significant interac-tions between country and sample day. Furthermore, the difference in reduction of leaf area between coun-tries was less for Isis than for Betta and SST 333, where the differences between countries were similar.

3.3. Aphid numbers

For all three cultivars tested in both countries, aphid numbers increased over time (Fig. 3; Table 2). However, aphid numbers did not differ consistently

between countries. Aphid numbers on SST 333 were significantly higher in Hungary than in South Africa. However, country and sample day interacted, and aphid numbers only differed significantly 7 days af-ter infestation, with no significant difference by 14 days. On the other hand, aphid numbers on Betta were significantly lower in Hungary than in South Africa. Again country and sample day interacted, and for this cultivar, aphid numbers did differ 14 days after infestation. Aphid numbers on Isis did not differ significantly between countries, nor did country and sample day interact in their effect on aphid numbers for this cultivar.

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Fig. 3. Number of D. noxia per plant on resistant (SST 333) and susceptible (Betta, Isis) cultivars in Hungary and South Africa.

Table 2

Analysis of variance for effect of country, sample day, and their interaction on the number of D. noxia per plant

Plant cultivar Factor df F P

sample day

2, 16 11.53 0.0008

sample day

2, 16 3.03 0.08

sample day

2, 16 1.22 0.32

3.4. Resistant versus susceptible cultivars

SST 333 and PI 262660, cultivars previously found resistant to South African D. noxia (Du Toit, 1989), and Isis and Betta previously found susceptible to South African D. noxia, showed mixed responses to infestation with Hungarian D. noxia (Fig. 4; Table 3). By day 14, the ranking for difference in plant weight between uninfested and infested plants was Isis > SST 333=PI 262660 >Betta (Fig. 4, Table 4). On the other hand, the ranking for difference in leaf area between uninfested and infested plants was SST 333> Betta> Isis> PI 262660. Aphid number increased

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Table 3

Analysis of variance for effect of cultivar, sample day, and their interaction on the difference in plant weight and leaf area between plants infested with D. noxia and uninfested plants and on the number of aphids per plant in Hungary

Dependent variable Factor df F P

Plant weight (g) Cultivar 3, 16 25.23 0.0001

Sample day 2, 32 1083.25 0.0001

Cultivar×sample day 6, 32 25.26 0.0001

Leaf area (mm2₎ _Cultivar _{3, 16} _356.25 _0.0001

Sample day 2, 32 2493.15 0.0001

Number of aphids Cultivar 3, 16 8.86 0.0010

Sample day 2, 32 10.01 0.0004

Table 4

Bonferonni-corrected comparisons of least-squares means among cultivars for each sample day days after, for the difference in plant weight and leaf area between plants infested with Diuraphis noxia and uninfested plants and for the number of aphids per plant in Hungarya

Sample day Cultivar Difference in plant weight Difference in leaf area Aphid number

Betta Isis PI 262660 Betta Isis PI 262660 Betta Isis PI 262660

7 Isis 1.000 – – 0.002 – – 1.000 – –

PI 262660 1.000 1.000 – 0.002 1.000 – 1.000 1.000 –

SST 333 1.000 1.000 1.000 1.000 0.004 0.002 1.000 1.000 0.002

10 Isis 0.130 – – 0.002 – – 1.000 – –

PI 262660 0.180 1.000 – 0.002 1.000 – 0.180 1.000 –

SST 333 1.000 0.002 0.005 0.310 0.002 0.002 1.000 0.970 0.020

14 Isis 0.002 – – 0.002 – – 0.620 – –

PI 262660 0.002 0.002 – 0.002 0.002 – 0.030 1.000 –

SST 333 0.002 0.002 0.360 0.002 0.002 0.002 1.000 0.160 0.007

a _{P (probability of observed difference in means if true difference)}₌_0.

with sample day and varied among cultivars, but there was no interaction between cultivar and sample day (Fig. 4, Table 3). By day 14, SST 333 had more aphids per plant than PI 262660 and Betta, but there were no other significant differences among cultivars in aphid numbers.

4. Discussion

The differences between Hungarian and South African D. noxia in their effects on plant weight and leaf area suggest genetic differences in D. noxia between countries. The differences in damage did not result from higher growth rate of Hungarian

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Bush et al. (1989) and Scott et al. (1990), who found that reduction in plant weight can occur in a line even though a visual damage rating indicates a high level of resistance.

That damage by D. noxia was sometimes not signif-icant a week after infestation may be because one adult and its progeny were insufficient to cause detectable damage. Webster et al. (1987) suggested that an ini-tial infestation of at least 10 D. noxia per seedling was required for evaluation of resistance. The authors van der Westhuizen and Botha (1993) found that D. noxia infestation induced quantitative differences between the polypeptide profiles of resistant and susceptible wheat leaves. Aphid infestation induces accumulation of specific proteins in the intercellular fluid of resis-tant cultivars only (Nagel et al., 1994), but produc-tion of these proteins requires sufficient aphid numbers (A.J. van der Westhuizen, personal communication, 1995).

In Hungary, visible water imbalance occurred 10 and 14 days after infestation. Miller et al. (1994) re-ported that symptoms of susceptibility to D. noxia in barley indicated alterations to the water status of the leaf, with infested susceptible barley taking up less water than uninfested plants. Burd and Burton (1992) pointed out that “the prevention of unfolding of new leaves and reduction of leaf size caused by Russian wheat aphid feeding apparently results from the reduc-tion of leaf turgor below the threshold for elongareduc-tion and cell wall extensibility”. Burd et al. (1993) found significantly lower leaf turgor for infested susceptible triticale ‘Beagle 82’ and susceptible wheat ‘TAM W 101’ and resistant wheat ‘PI 372129’ compared with the uninfested control. The leaf turgor of D. noxia infested resistant triticale cultivars ‘Okay R’ and ‘PI 386148’ did not differ from the uninfested control. Water imbalance in most cases has been found in sus-ceptible plant cultivars (Burd et al., 1993). In contrast, the present study showed loss of turgor only in re-sistant cultivars. The occurrence of water imbalance, together with characteristic leaf rolling and yellow streaking on cultivars which are resistant to South African D. noxia suggests biotypic differences in D. noxia between South Africa and Hungary. These data support the idea that resistant plant germplasm has ge-ographical limits because of gege-ographical variation in pest species (Puterka et al., 1992). This means that, in an aggressive breeding program, resistance should be

identified against collections of pests from throughout the region of crop production. Furthermore, stacking genes for resistance in a cultivar should prove a more durable strategy in the long run.

Acknowledgements

The authors thank Léan van der Westhuizen (Uni-versity of Orange Free State, Department of En-tomology) for suggestions on experimental design, Willie Maree (Sensaco Cooperative Ltd.) for provid-ing research facilities, the Cereal Research Institute, Szeged, Hungary for supplying germplasm, and Árpád Szentesi and Ferenc Kádár (Plant Protection Institute of Hungarian Academy of Sciences) for suggestions on statistical analyses. This research was funded by Sensaco Cooperative Ltd.

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