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Influence of Cultivar on Aphids (Hemiptera: Aphididae) and Associated Natural Enemies in Pakistani Wheat Ecosystems




Influence of Cultivar on Aphids (Hemiptera: Aphididae) and Associated Natural Enemies in Pakistani Wheat Ecosystems

Qamar Zeb1*, Silvia I. Rondon2, Hayat Badshah,1 and Arsalan Khan1

1Agricultural Research Institute, Tarnab, Peshawar, Khyber Pakhtunkhwa, Pakistan.

2Oregon State University, Department of Crops and Soil Science, Hermiston Agricultural Research and Extension Center, Hermiston, OR USA 97838


The objective of this study was to determine the influence of cultivar on aphids and their natural enemies in wheat (Triticum aestivum L.). Thus, twenty Pakistani wheat cultivars were grown at the Agricultural Research Institute in Tarnab-Peshawar, Pakistan during the winter (‘rabi’ in local language) season. Plots were arranged in a randomized complete block design with three replicates per treatment/cultivar. Population of aphids, and numbers of parasitoids and predators were recorded at weekly intervals. Rhopalosiphum padi Linnaeus, Schizaphis graminum Rondani, and Sitobion avenae Fabricius were the predominant aphid species (Homoptera: Aphididae). Two species of parasitoids Aphidius ervi L. and Aphidius colemani Viereck were recorded. Coccinella septempunctata L. (Coleoptera: Coccinellidae), Chryoperla carnea Stephens (Neuroptera: Chrysomelidae), and several species of Hover flies (Diptera: Syrphidae) were the most common predators. In general, aphids were reported in all wheat cultivars. Cultivar Saleem-2000 presented the highest number of aphids per tiller (9.1), while Gomal-2008 presented the lowest (1.9). Based on aphid presence per tiller, no cultivar was found to be Susceptible or Highly Susceptible, but 1 cultivar was found to be Moderate Susceptible, 8 Moderate Resistant, 9 Resistant, and 2 Immune. Rate of parasitism and predation increased when aphid density increased. In general, wheat cultivar influenced aphid population pressure, and indirectly influenced the natural population of parasitoids and predators.

Article Information

Received 09 October 2018

Revised 12 July 2019

Accepted 27 August 2019

Available online 17 January 2020

Authors’ Contribution

QZ designed, conducted the research and recorded the data. HB, RAS helped in data compilation. AK helped in data analysis. SIR helped in manuscript preparation and editing.

Key words

Wheat, Aphids, Parasitoids, Predators, Wheat Aphids, Resistance, Ecosystems, Control


* Corresponding author:

0030-9923/2020/0002-0503 $ 9.00/0

Copyright 2020 Zoological Society of Pakistan


Wheat, Triticum aestivum Linnaeus (Poales: Family Poaceae), is a major staple food crop worldwide. In Pakistan, wheat is grown as an annual crop and is an important nutritional source in the Pakistani diet (Naz and Akmal, 2016). Wheat contributes about 96% of the total value of the country’s agricultural sector, which represents 1.9% of the total Pakistani economy (Pakistan Economic Survey, 2017). In the 2016-17 growing season, wheat was sown on 9,052 thousand hectares, producing 26 million tons with an average yield of 2,845 kg ha-1 (Pakistan Economic Survey, 2017). Depending on the region, there are two main crop-growing seasons in Pakistan. During winter or ‘rabi’ (1), in local language, crops like wheat, barley (Hordeum vulgare L.), chick pea (Cicer arietinum L.), and lentils (Lens culinaris Medikus) are grown from Oct to Dec, and harvested during Mar to May; summer or ‘kharif’ (2), were maize (Zea mays L.), rice (Oryza sativa L.), sorghum (Sorghum bicolor Moench), and millet (Panicum spp.) are sown from Mar to Jul, and harvested around late Sept (Hatam, 1994). Both field seasons allow the presence of green crops that serve as host to many pest species.

Several arthropod species reduce wheat productivity in Pakistan. Species of aphids are present in wheat, and cause direct or indirect damage, by feeding or vectoring plant pathogens, respectively (Chapin et al., 2001; Steffey and Gray, 2012). Aphid infestations have considerably affected productivity and profitability by reducing shoot growth, lowering chlorophyll concentrations, and overall root growth (Reidell and Kieckefer, 1995). Different aphid species like Rhopalosiphum maidis Fitch, R. padi L., Schizaphis graminum Rondoni, Sitobion avenae Fabricius, Sipha maydis Passerini, Macrosiphum avenae Fabricius, Aphis nerii Boyer de Fonscolombe, Myzus persicae Sulzer, Brevicoryne brassicae L., Macrosiphum granarium Kirby, and R. rufiabdominalis Sasaki prevail on wheat in Pakistan (Hamid, 1983; Leather et al., 1989; Irshad, 2001; Mushtaq et al., 2013). In the Peshawar valley of the Khyber Pakhtunkhwa province, S. graminum, R. padi, and S. avenae are dominant species (Hashmi et al., 1983; Hachett et al., 1987; Ali et al., 2015).

In Pakistan, aphids have mostly been controlled by insecticide application (Irshad, 2001). However, we recognize that excessive pesticide use may cause pest-resurgence, insect resistance, and disturb the natural balance of pest and natural enemies; they can also create human health problems and environmental pollution (Zacharia, 2011). In addition, chemical control can cause adverse effects on non-target organisms such as birds, fish, and other aquatic life; insecticides can also reduce the number of pollinators and adversely affect the soil microorganism composition that are involved in nutrient recycling (Iyaniwura, 1991; Baskar et al., 2017). Due to recent outbreaks of aphids in Pakistan, producers have heavily relied on the use of pesticides (Punjab Agriculture Research Board, 2011; Wains et al., 2014). Until recently, aphids were not a threat to wheat and populations were under control potentially by natural enemies (Hamid, 1983). Several botanical insecticides derived from oils coming from leaf and seeds have been used to control aphids in Pakistan (Iqbal et al., 2011). A few examples include neem Azadirachta indica Juss, sweet orange Citrus sinensis Osbeck, balsam pear Momordica dioica Roxb.ex Willd, wild garlic Allium vineale L., chili pepper Capsicum frutescens L., Moringa oleifera Lam, and tobacco Nicotiana tabacum L. Neonicotinoid insecticides have been widely used in the region including several formulations such as thiamethoxam 25GW, imidacloprid 20% EC, and acetamiprid 20SP (Iqbal et al., 2011; Zeb et al., 2016; Shah et al., 2017).

Host plant resistance along with natural enemies and cultural control provide an effective, environmentally friendly, and economical aphid control strategy. The premise is the alteration of pest behavior on insect host selection, oviposition and feeding, reduce insect survival and development, and recovery from injury (Smith, 1989). The general thought is that the use of plants with resistance traits will help reduce insecticide applications, and aid in the increase of biological control activity (Sharma and Ortiz, 2002). Certain host genotypes are known to affect performance of herbivores and community structure including predators and parasitoids (Kennedy, 2003; Schadler et al., 2010). For instance, quack grass, Elytrigia repens L., affects the interaction of R. padi, the parasitoid wasp Aphidius colemani Viereck, and the predatory lacewing Chrysoperla carnea Stephens (Schadler et al., 2010). Schadler et al. (2010) reported that the number of R. padi offspring’s, and presence of its parasitoids differed considerably when exposed to different plant genotypes and the behavior was related to the nutritional contribution of each plant type which influence natural enemies’ preference. Effects of any particular plant defense trait on parasitoids and predators depends on the specific attributes of the plant trait, and the detail of the physical, biochemical, and behavioral interaction between natural enemies, its host (prey), and the plant (Kennedy, 2003). Givovich and Niemeyer (1995) and Eleftherianos et al. (2006) indicated that the presence of chemical compounds such as phenolics and hydroxamic acids, are involved in wheat plants resistance against R. padi and S. avenae. More specifically, aphids feeding caused reduction in the percentage of epicuticular wax, dry weight, sugar, amino acid level and slows the uptake of minerals like P, K, Ca, Mg, and Fe. In cabbage, ascorbic acid, proline, phenol peroxidases, oxidases, and minerals like Ca and K play a role against aphids (Khattab, 2007). α-Tomatine, an alkaloid in tomato plants, is indirectly toxic to endoparasite of lepidopterous pest in tomatoes, since parasitoids acquire the alkaloid while parasitizing the pest who previously fed on the alkaloid (Campbell and Duffy, 1979). Leaf pubescence also could be one of the resistance factors against various wheat aphid species (Gholami et al., 2013); for example, wheat cultivars with high trichome density reduced D. noxia incidence (Bahlmann et al., 2003). Similarly, ecological aspects can be affected; such as the searching ability of Encarsia formosa Gahan, a parasitoid of whiteflies, whose numbers increase three-fold on hairless cucumber compared to hairy varieties (Van Emden, 1986). The searching and walking speed of Trichogramma exiguum L., egg parasitoids of Heliothis zea Boddie, are influenced by differences in leaf structure, particularly trichome form and density (Keller, 1987).

Because screening and identification of resistant germplasm are fundamental for long-term sustainable production, the impact of several Pakistani wheat cultivars on aphid species populations and their associated natural enemies’ populations was studied in the Peshawar valley of the Khyber Pakhtunkhwa province in Pakistan. Natural enemies were included in our study since their impact in our region is under study (Adisu et al., 2002).



The experiment was conducted at the Agricultural Research Institute (ARI) Tarnab-Peshawar in Pakistan (34.0040o N, 71.6970o E). Twenty wheat cultivars (n=20) were planted in a randomized complete block with three replicates per treatment/cultivar (Table I). Each plot was 2.5 m wide × 2 m in length with a buffer area of 1 m between plots. Approximately 56.3 g of seed per variety per plot was sown by using a locally made hand manual single line seed drill hoe. Standard 30-cm row spacing, and general local agronomic practices were followed. Fertilizers at the rate of 120 kg of N, and 90 kg of P ha-1, came from urea and diammonium phosphate (DAP). Half of the N, and full dose of K were applied at soil preparation, while the


Table I. Parentage and pedigree of wheat varieties used on this experiment.

















F12-71/COC/CNO 79












JUP/ALD'S'//KLT'S'/3/VEE'S'/6/BEZ //TOB/8156/4/ON/3/6*TH/KF//6*LEE/KF/5































PB 222138-3A-0A-0A-231A-0A




Source of origin of the used wheat varieties is CIMMYT/ICARDA; This information was obtained from the Cereal Crop Research Institute (CCRI), Pirsabak, Nowshera-Kyber Pakhtunkhwa.


remaining half N was applied with first irrigation 3-wks after sowing (Inamullah et al., 2011).

Sampling aphids and natural enemies

After seed germination until crop maturity, 9 tillers per plot were regularly inspected at weekly interval, and number of aphid species (alate and apterous), aphid mummies, and predators per tiller were counted. Aphids were collected from wheat plants using a fine camel hairbrush; samples were placed in vials in 80% ethyl alcohol, and transported to the laboratory for identification. Permanent slides of a sub-sample of the aphids collected were prepared in Hoyer’s medium (Manya, 1987). Aphids were identified using morphological characteristics according to Blackman and Eastop (1984, 2000) and Manya (1987) identification keys. Percent parasitism was calculated by the following formula: [No. mummified aphid/ (No. mummified aphid + No. non-mummified aphid)]×100 (Shahid et al., 2012). For the identification of the parasitoids, a sub-sample of mummies collected were placed in petri dishes (10 cm × 1.5 cm) in the laboratory at a temperature of 20 ± 50C, 50-65% relative humidity, and a photoperiod of 16:8 h D: L until hatching. Adult parasitoids were identified using Tobias (1995) identification keys. Also, most common predators groups were identified.

Rating host plant resistance

Aphid data were classified in groups and analyzed as early-season (last week of Nov to Jan), mid-season (Feb to mid-Mar), and late-season populations (mid-Mar to first week of Apr). Aphids’ parasitism was recorded weekly and data were analyzed per season as described above. This procedure of classification of data into group was adopted from Ronquim et al. (2004), Muhammad et al. (2013) and Wains et al. (2014). The following modifications were made: Immunity (I), 1-2 aphid tiller-1; Resistance (R), 3-4 aphid tiller-1; Moderately Resistant (MR), 5-6 aphid tiller-1; Tolerant (T), 7-8 aphid tiller-1; Moderately Susceptible


Table II. Mean number of aphids per tiller per variety during early, mid and late season in Agriculture Research Institute, Tarnab-Peshawar, Pakistan.

Wheat cultviars

Early (Nov to Jan)

Mid (Feb to mid-Mar)

Late (Mid-Mar to first week of Apr)

Seasonal mean



7.80 a

13.00 a

5.51 a




4.00 b

9.36 cd

4.54 b




4.16 b

10.20 b

2.51 e



4.00 b

10.42 b

2.30 efgh



4.06 b

9.40 c

2.31 efgh



3.41 c

8.92 cd

2.31 efgh



3.28 cd

9.12 cd

2.0 gh

4.93 bcde


2.93 d

8.72 de

3.04 cd



3.27 cd

8.21 ef

1.24 j



2.23 e

7.64 f

4.30 b




2.01 ef

7.97 f

2.93 d



3.00 cd

6.48 gh

1.33 j



1.59 fg

7.69 f

3.41 c



1.65 fg

6.90 g

2.02 fgh



1.61 fg

6.96 g

1.59 ij



1.65 fg

6.06 h

2.40 ef



1.42 gh

5.23 i

1.30 j



1.13 h

5.02 i

2.29 efgh



0.64 i

5.04 i

2.36 fg




0.57 i

3.97 j

1.92 hi



Within columns, means followed by the same letters are not significantly different at 0.05 % level of significance. Rating scale: Immunity (I), 1-2 aphid tiller-1; Resistance (R), 3-4 aphid tiller-1; Moderately Resistant (MR), 5-6 aphid tiller-1; Tolerant (T), 7-8 aphid tiller-1; Moderately Susceptible (MS), 9-10 aphid tiller-1; Susceptible (S), 11-15 aphid tiller-1 ; and Highly Susceptible (HS), 16-20 aphid tiller-1.

(MS), 9-10 aphid tiller-1; Susceptible (S), 11-15 aphid tiller-1; and Highly Susceptible (HS), 16-20 aphid tiller-1 (Table II).


Data analysis

Data were analyzed with analysis of variance using Statistix 8.1 (Analytical Software, 2005) for multiple comparisons; LSD-test was used for separation of means at α=0.05. Standard errors of means of aphids (all aphids pooled together, and main aphid species individually; Table III) aphid parasitoids (Table IV), and predators (Table V) were calculated following previous parameters reported by Zeb et al. (2011). Correlation (r) between aphid density and rate of parasitism per variety and aphid density and number of predator per variety were determined using statistical software (Table VI).



As shown in Table II, the mean number of aphids per tiller per cultivar differ early, mid, and late-season. Overall, statistically significant differences of the entire season mean were observed (F=517.49; df=19; P ˃0.0000). The highest mean number of aphids per tiller was recorded on Saleem-2000 (9.1 aphids/tiller), while the lowest was found on Gomal-2008 (1.9), followed by Pisabak-2004 (2.4), Pisabak-2005 (2.6), and Hashim-2008 (2.6). Early (F=396.56; df=19; P ˃0.0000), mid (F=93.86; df=19; P ˃0.0000), and late (F=68.79; df=19; P ˃0.0000) season, the cultivar Saleem-2000 presented the highest number of aphids/tiller (Table II) classifying this variety as moderately susceptible (MS). In addition, no cultivar was found to be susceptible or highly susceptible, but 1 cultivar was found to be moderate susceptible, 8 moderate resistant, 9 resistant, and 2 immune.

Differences were observed when most common aphid species were analyzed separately (Table III). Close to 67% of aphids collected were R. padi, 16%, S. graminum, 15% S. avenae, and less than 2% ‘other aphids’. Consistently, cultivar Saleem-2000 presented the highest number of R. padi (F=28.77, df=19, 319; P ˃0.0000), S. graminum (F=2.74, df=19; P ˃ 0.0003), and S. avenae (F=23.41, df=19; P ˃0.0000) per tiller.


Table III. Number of aphids (Mean±SE) per tiller per cultivar in Agricultural Research Institute, Tarnab, Peshawar, Pakistan.

Wheat cultivars

R. padi

S. graminum

S. avenae


8.12 ± 0.78 a

2.02 ± 0.32 a

1.64 ± 0.12 a


5.39 ± 0.73 b

0.64 ± 0.23 fg

1.89 ± 0.12 a


5.22 ± 0.73 bc

1.20 ± 0.46 bcdefg

0.66 ± 0.17 bcd


5.01 ± 0.71 bcd

1.55 ± 0.41 abcd

0.26 ± 0.07 fgh


4.35 ± 0.77 de

1.63 ± 0.44 abc

0.89 ± 0.99 b


4.17 ± 0.76 ef

1.13 ± 0.4 bcdefg

0.30 ± 0.03 efg


4.39 ± 0.76 cde

0.95 ± 0.29 defg

0.74 ± 0.18 bc


3.75 ± 0.73 efg

1.32 ± 0.35 bcde

0.74 ± 0.13 bc


4.24 ± 0.71 de

0.59 ± 0.28 g

0.57 ± 0.18 cde


3.40 ± 0.78 fgh

1.25 ± 0.35 bcdefg

0.67 ± 0.11 bcd


3.16 ± 0.72 ghi

1.28 ± 0.36 bcdef

1.64 ± 0.09 a


2.99 ± 0.51 ghi

1.08 ± 0.29 cdefg

0.10 ± 0.05 g


3.05 ± 0.76 ghi

1.38 ± 0.45 abcde

0.13 ± 0.06 g


2.33 ± 0.71 ijk

1.31 ± 0.4 bcde

0.37 ± 0.12 defg


2.12 ± 0.57 jkl

1.74 ± 0.4 ab

0.09 ± 0.07 g


2.78 ± 0.59 hij

0.83 ± 0.28 efg

0.10 ± 0.06 g


2.08 ± 0.49 jkl

0.78 ± 0.44 efg

0.50 ± 0.09 cdef


1.64 ± 0.36 kl

1.41 ± 0.46 abcde

0.31 ± 0.09 efg


1.92 ± 0.6 kl

0.80 ± 0.28 efg

0.20 ± 0.07 fg


1.39 ± 0.4 l

1.06 ± 0.26 cdefg

0.22 ± 0.07 fg


Within columns, means followed by the same letters are not significantly different at 0.05 % level of significance.


Aphidius ervi and A. colemani were the most common parasitoids. Early in the season (F=2.92; df=19; P ˃0.0001), the mean rate of parasitism was close to zero (Table IV); however, as season progressed, parasitism gradually increased (mid-season F=5.38; df=19; P ˃0.0001; late season, F=28.37; df=19; P ˃0.0001). The highest seasonal mean rate of parasitism was recorded on Pirsabak-2005 (20) followed by Siran-2010 (20), and Gomal-2008 (19) (Table IV).

Coccinella septempunctata L (Coleoptera: Coccinellidae) (F=11.32, df= 19, P= 0.000), Chrysoperla carnea Stephens (Neuroptera: Chrysopidae) (F=4.07; df=19; P= 0.001, and several species of Hover flies (F=2.44, df=19, P=0.0095) were the dominant predators (Table V). Total predator population (all predators combined) per tiller-1 was significantly higher (F= 7.03, df= 19, P=0.0000) on Attahabib-2010 followed by Pirsabak-2005 (Table V). Lower mean predators’ population was recorded on Siran-2010 and Auqab-2000.


Table IV. Mean rate of parasitism per tiller per variety during early, mid and late season in Agricultural Research Institute, Tarnab, Peshawar, Pakistan.



Early (Nov to Jan)

Mid(Feb to mid-Mar)

Late (mid-Mar to first week of Apr)

Seasonal mean


2.96 a

15.46 b

46.98 cde

20.21 ± 7.49 a


0.00 f

9.82 d

56.53 a

20.2 ± 10.87 a


0.00 f

16.30 a

45.15 de

19.04 ± 8.19 a


0.80 d

11.75 c

50.50 bc

18.34 ± 8.53 ab


0.00 f

6.19 gh

51.40 b

16.53 ± 9.55 abc


0.00 f

4.16 j

48.39 bcd

15.35 ± 1.57 abcd


0.00 f

9.67 d

43.80 e

15.14 ± 7.26 abcd


0.00 f

5.23 i

39.76 f

13.45 ± 8.44 abcde


1.54 b

7.62 e

29.80 gh

11.54 ± 5.35 bcde


0.57 e

4.90 i

31.33 g

10.99 ± 5.82 cde


1.10 c

6.05 gh

29.05 gh

10.84 ± 4.97 cde


0.00 f

4.93 i

27.93 ghi

10.17 ± 6.02 cde


053 e

6.75 f

26.76 hij

10.09 ± 4.52 cde


0.00 f

4.12 j

30.65 g

10.08 ± 6.11 cde


1.1 c

6.25 fgh

25.32 ij

10.04 ± 4.52 cde


0.56 e

6.40 fg

25.11 ij

9.89 ± 4.47 cde


0.00 f

6.58 fg

26.50 hij

9.20 ± 4.48 cde


0.00 f

5.24 i

24.33 ij

8.62 ± 4.46 de


0.00 f

3.40 k

23.41 j

8.13 ± 4.71 e


0.00 f

5.85 h

16.87 k

6.61 ± 2.54 e


Within columns, means followed by the same letters are not significantly different at 0.05 % level of significance.


Table VI shows a correlation between aphid density and rate of parasitism and between aphid density and number of predators per tiller on each variety. Varieties such as Saleem-2000 that consistently showed the highest number of aphids per tiller was negative correlated to rate of parasitism but positive correlated to predator density. The only significant correlations were observed between aphids per tiller and predators present in cultivars Gomal-2008 and Pirsabak-2008.


Table V. Number of predators (Mean±SE) per tiller per variety in Agricultural Research Institute, Tarnab, Peshawar, Pakistan.

Wheat cultivars

Coccinellid beetles

Green lace wing

Syrphid flies

Total predators population


0.25 ± 0.09 a

0.37 ± 0.03 a

0.05 ± 0.01 cd

0.44 ± 0.15 a


0.28 ± 0.09 a

0.13 ± 0.03 cdefgh

0.12 ± 0.02 ab

0.40 ± 0.10 ab


0.19 ± 0.5 b

0.32 ± 0.04 ab

0.10 ± 0.01 bcd

0.36± 0.12 abc


0.17 ± 0.02 b

0.25 ± 0.03 abcd

0.14 ± 0.03 ab

0.36 ± 0.08 abc


0.10 ± 0.02 cdefg

0.27 ± 0.02 abc

0.22 ± 0.05 a

0.34 ± 0.10 abcd


0.15 ± 0.02 bcd

0.24 ± 0.02 abcde

0.13 ± 0.01 bc

0.32 ± 0.06 abcd


0.16 ± 0.06 bc

0.22 ± 0.17 bcdef

0.07 ± 0.04 bcd

0.29 ± 0.06 bcde


0.14 ± 0.04 bcde

0.15 ± 0.04 cdefgh

0.09 ± 0.03 bc

0.26 ± 0.07 cdef


0.08 ± 0.02 fghi

0.20 ± 0.03 bcdefg

0.12 ± 0..03bc

0.23 ± 0.03 defg


0.11 ± 0.04 cdef

0.12 ± 0.03 fgh

0.04 ± 0.02 cd

0.19 ± 0.05 efgh


0.08 ± 0.01 fgh

0.10 ± 0.00 fgh

0.09 ± 0.04 bc

0.18 ± 0.05 efgh


0.10 ± 0.01 defg

0.07 ± 0.02 gh

0.09 ± 0.05 bc

0.17 ± 0.05 fgh


0.10 ± 0.03 defg

0.11 ± 0.03 efgh

0.04 ± 0.02 cd

0.17 ± 0.05 fgh


0.08 ± 0.01 fgh

0.03 ± 0.02 h

0.12 ± 0.06 bc

0.16 ± 0.03 fgh


0.03 ± 0.01 hi

0.13 ± 0.03 cdefgh

0.10 ± 0.01 bc

0.14 ± 0.05 gh


0.10 ± 0.02 defg

0.02 ± 0.02 h

0.06 ± 0.03 bcd

0.13 ± 0.11 gh


0.08 ± 0.03 def

0.12 ± 0.04 defgh

0.00 ± 0.00 d

0.13± 0.02 gh


0.05 ± 0.01 ghi

0.07 ± 0.04 gh

0.06 ± 0.00 bcd

0.11 ± 0.06 gh


0.05 ± 0.01 ghi

0.08 ± 0.02 fgh

0.06 ± 0.02 bcd

0.12 ± 0.05 gh


0.02 ± 0.01 i

0.12 ± 0.04 defgh

0.00.05±0.04 cd

0.10 ± 0.03 h


Within columns, means followed by the same letters are not significantly different at 0.05 % level of significance.



Aphids are present in all wheat Pakistani cultivars early, mid, and late season. Following a modification of Ronquim et al., 2004, Muhammad et al. (2013) and Wains et al. (2014) ranking scales, the cultivar Saleem-2000 was found Moderately Susceptible; 8 cultivars including Tatara-97, Zam-2004, FakhreSarhad-99, Barsat-2010, KT-2000, Dera-98, Attahabib-2010, and Daman-98 were found Moderately Resistant; 9 cultivars, including Bakhtawar-92, Khyber-87, Sehar-2006, Pirsabak-2008, Bathoor-2008, Siran-2010, and Uqab-2000 were categorized Resistant; while Pirsabak-2004 and Gomal-2008 showed immune response (Table II). This ranking scale, based on the number of aphids per tiller, is widely used. For instance, Muhammad et al. (2013) conducted field experiments to study the population dynamics of wheat aphids on 16 wheat cultivars where Sehar-2006, which was also included in our study, was the least ‘preferred’ cultivar considered “Immune”, based on mean number of aphids per tiller; in our study this cultivar performed somewhere in the middle classifying as “Resistant”. Khan and Gul (2012) reported the screening of 20 wheat cultivars where 4 of those, CT-0492, CT-07043, WL-01869 and NIFA V-16, were highly infested or “Susceptible” (11 aphids per tiller) while others such Bathoor-2008 (8 aphids per tiller) was found to be “Tolerant”. Wains et al. (2010) tested 12 wheat lines including Shafaq-2006, Sehar-2006, FSD-08 and Lasani-2008 classified as “Resistant”. Akhtar et al. (2009) studied Inqilab-91, Chakwal-97, MH-97, Margalla-99, Chenab-2000, Iqbal-2000, Saleem-2000 and Wafaq-2001 concluding that Saleem-2000 and Iqbal-2000 were “Susceptible” varieties to wheat aphids. Iqbal et al. (2008) screened 28 wheat varieties/lines finding that Iqbal-2000 (8 aphids per tiller) was “Susceptible” while the advance line V00147 was “Resistant” (3 aphids per tiller). Other varieties such as Suliman-96, RT-5, Khaniwal, K2-L, Takbeer, Nowshera-96, Pirsabak-85, Blue Silver, KRL-1.4, Ghaznawi-98, Bakhtawar-92, Kim, Fakhr-e-Sarhad, Dera-98, Saleem-2000, ICARDA, SARC-3, RT-10, Tatara-97, KT-2000 and Inqilab have been continuously tested (Akhtar and Mujahid, 2006; Khan et al., 2007a). Some of these cultivars, varieties or lines are common in local commercial production (Pakistani Economic Survey, 2017).


Table VI. Correlation of aphid density and its predators and percent parasitism per tiller per variety.

Wheat cultivars

Correlation coefficient (r) between aphid density and predator

Correlation coefficient (r) between aphid density and parasitism

Pirsabak 2005



Atta habib 2010



Zam 2004



Bathoor 2008



Barsat 2010



Seher 2006



Saleem 2000



Dera 98



FakhreSarhad 99



Tatara 97



Daman 98



Auqab 2000



Pirsabak 2004



Khyber 87



Bakhtawar 92



Hashim 2008



Gomal 2008



KT 2000



Pirsabak 2008



Siren 2010




*Significant (P≤ 0.05)


The parental and pedigree of each cultivar tested are present in Table I showing the indirect linkage of some cultivars; some cultivars are coming from long standing breeding programs mainly disease resistant oriented. It was not part of this study to evaluate the morphological or chemical characteristics of each cultivar tested that could help us understand why aphids choose one cultivar versus another one. Plant morphological characteristic such as growth habit, plant height, leaf color and growth stage of various wheat genotypes could affect the aphid seasonal dynamic (Markova and Tomchev, 2013). It was part of our study to determine presence of aphids in given cultivars to be able to determine action control methods. Based on our study, alate aphids can start colonizing as soon as plants emerged (personal observation). Previously, Ali et al. (2011, 2015), and Aheer et al. (2006) reported similar results. Ronquim et al., 2004 indicated that population differences based on number of individuals occurring on the host plant is one way to verify host resistance to insects. It is known that the seasonal distribution of aphids depends upon the climatic condition of the region, host plant quality, natural enemies and agricultural practices (Brewer and Elliot, 2004).

Although unknown how many species of aphids are present in Pakistani wheat fields, it is not surprising to find R. padi as the predominant specie; S. graminum, and S. avenae were also predominant in wheat fields (Table III). Gianoli (2000) and Honek et al. (2006) previously reported the three species aforementioned as the main species found in wheat fields. In our study, R. padi was found to colonize the leaves (1-2 leaf stage) and stems early in the season, while S. graminum infestation occurred at the 5-6 leaf stage mainly on leaves but later on spikes; S. avenae appeared late in the season but only present on spikes suggesting some sort of species displacement or specialization which was not evaluated on this study.

Insect-parasitoid-predator interactions are important when evaluating susceptibility or resistance of cultivars/varieties/lines. For instance, in our study the cultivars characterized as “Immune” based on the number of aphids per tiller such as Pirsabak-2004 and Gomal-2008 (Table II) presented one of the lowest (Pirsabak-2004) and highest (Gomal-2008) parasitism rate (Table IV); in contrast one of the highest (Pirsabak-2004), and lowest (Gomal-2008) predator rate (Table V) suggesting a more complex relationship. In an early study by Schuster and Starks (1975), this complexity was demonstrated studying the preference of Lysiphlebus testaceipes L. for greenbug in small grain. Similarly, Biswas and Singh (1998) indicated that host plant resistance and bio-control should be further study in well control settings. In our study, A. ervi and A. cloemani were identified as the main two parasitoids. In other studies, Adisu et al. (2002) reported A. colemani, A. rhopalosiphi and A. uzbekistanicus in Germany; Chambers et al. (1982) and Charlet et al. (2002) reported L. testaceipes, Aphilinus mali, and A. avenaphis in North Dakota, USA; Khan et al. (2007b) also reported A. ervi and A. colemani in Pakistan, while Ali et al. (2015) reported Diaeretiella rapae. In our study, parasitism rates started low, however, as season progressed, the mean rate of parasitism increased (Table IV). This observation is is similar to the one noted by Tomanovic et al. (2008).



A good degree of resistance was observed in varieties, Gomal-2008, Hashim-2008, Pisabak-2004 and Pirsabak-2005 against whet aphid. Furthermore, these varieties shown high compatibility for natural parasitism. Pirsabak-2005 was the only variety among the tested wheat varieties which provided easy access to parasitoids and predators for parasitism or consumed his prey (aphid). The susceptible variety Saleem-2000 in spite of having more aphid shown less compatible for bio-control agents. It is further suggested that resistance mechanism of these varieties should be studies to explore the physiochemical and physiological base of resistance. This information will provide a baseline data to breeder to develop high yielding wheat varieties with adaptation to different agro ecological condition and compatible with biological control agents.



This study was completed with financial help of the Higher Education Commission, Islamabad Pakistan under a PhD fellowship. Authors thank Drs. J. Crosslin, USDA-ARS and A. Rashed, University of Idaho for editorial comments.


Statement of conflict of interest

The authors stated no conflicts of interest.



Adisu, B., Stary, P., Freier, B. and Buttner, C., 2002. Aphidius colemani Viereck (Hymenoptera: Braconidae: Aphidiinae) detected in cereal fields in Germany. Anz. Schädlingsk., 75:89-94.

Aheer, G.M., Munir, M. and Ali, M., 2006. Screening of wheat varieties against aphid in ecological condition of district Mandi Bahauddin. J. agric. Res., 44: 55-59.

Akhtar, N. and Mujahid, M.Y., 2006. Patterns of resistance to Schizaphis graminum (Rondani) among rain fed National Uniform wheat varieties. Pakistan J. Zool., 38: 153-157.

Akhtar, I.H., Naeem, M. Javed, H. and Aziz, M.A., 2009. Could host plant resistance affect on cereal aphid (Aphididae: Homoptera) population on wheat crop. Int. J. Agric. Vet. Med. Sci., 3: 31-42.

Ali, I., Khan, B.S. Sagher, M. and Ali, A., 2011. Determination of varietal resistance for and losses by aphids in wheat cultivars. Pak. Entomol., 33: 157-160.

Ali, S., Khalid, S., Ali, S., Akhtar, K., Khan, M.S., Ali, A., Samad, A., Hussain, S., Fahad, S. and Khan. F., 2015. Preferential influence of wheat genotypes on the distribution pattern and population dynamics of cereal aphid and their natural enemies in Peshawar valley. Pakistan J. Zool., 47: 223-233.

Analytical Software Statistix Version 8.1. 2005. User manual. Analytical software, Tallahassee. Florida. pp. 88.

Bahlmann, L., Govender, P. and Botha, A., 2003. Leaf epicuticular wax ultrastructure and trichome presence on Russian wheat aphid (Diuraphis noxia) resistant and susceptible leaves. Afr. Entomol., 11: 59-64.

Baskar, K., Sudha, V. and Jayakumar, M., 2017. Effect of pesticides on pollinators. Ecol. Environ. Sci., 2: 00052

Biswas, S. and Singh, R., 1998. Interaction between host plant resistance and the bio control of a cereal aphid: A laboratory study. Biol. Agric. Horticul., 16: 25-36.

Blackman, R.L. and Eastop, V.F., 1984. Aphid on the world’s crops. An identification and information guide (1st Edition) New York, John Wiley and Sons Ltd, Chicheste, pp. 466.

Blackman, R.L. and Eastop, V.F., 2000. Aphid on the world’s crop. An identification and information guide (2nd Edition) John Wiley Ltd, Uk, pp. 414.

Brewer, M.J. and Elliott, N.C., 2004. Biological control of cereal aphid in North America and mediating effects of host plant and habitat manipulations. Annu. Rev. Ent., 49: 103-111.

Campbell, B.C. and Duffy, S.S., 1979. Tomatine and parasitic wasps-potential incompatibility of plant antibiosis with biological control. Science, 205: 700-702.

Chambers, R.J. and Sunderland, K.D., 1982. A survey of cereal aphid and their natural enemies in winter wheat in 1980. Annls. appl. Biol., 101: 175-178.

Chapin, J.W., Thomas, J.S. Gray, S.M. Smith, D.M. and Halbert, S.E., 2001. Seasonal abundance of aphid (Homoptera: Aphididae) in wheat and their role as barley yellow dwarf virus vectors in the South Carolina coastal plain. J. econ. Ent., 94: 410-421.

Charlet, L.D., Olson, D. and Glogoza, P.A., 2002. Biological control of insect and weed pests in North Dakota agriculture. North Dakota State University, extension service, Fargo: North Dakota., 58105: 4-10.

Eleftherianos, I., Vamvatsikos, P., Ward, D. and Gravanis, F., 2006. Changes in the levels of plant total phenols and free amino acids induced by two cereal aphids and effects on aphid fecundity. J. appl. Ent., 130: 15-19.

Gianoli, E., 2000. Competition in cereal aphid (Homoptera: Aphididae) on wheat plants. Environ. Ent., 29: 213-219.

Givovich A. and Niemeyer, H.M., 1995. Comparison of the effect of hydroxamic acids from wheat on five species of cereal aphids. Ent. Exp. Appl. 74: 115-119.

Gholami, M.S., Hosseini, M. and Modarres, A.M., 2013. Does leaf pubescence of wheat affect host selection and life table parameters of Sipha maydis (Passirini) (Hemiptera: Aphididae. Crop Prot., 2: 81-92.

Hachett, A.H., Starks, K.J. and Webster, J.A., 1987. Insect and mites pest of wheat. Wheat and wheat improvement (ed. E.G. Heyne), Madison, Wisconsin. pp. 625-675.

Hashmi, A.A., Hussain, M.M. and Ulfat, M., 1983. Insect pest complex of wheat crop. Pakistan J. Zool., 15: 169-176

Hamid, S., 1983. Natural balance of graminicolous aphids in Pakistan. Survey of populations. Agronomie, 3: 665-673.

Hatam, M., 1994. Classification of field crops. In: Crop production (eds. S. Nazire, E. Bashire and B. Robout). National Book Foundation. Islamabad. pp. 14-24.

Honek, A., Jarosik, V. and Dixon. A.F.G., 2006. Comparing growth patterns among field populations of cereal aphid revels factors limiting their maximum abundance. Bull. entomol. Res., 96: 269-277.

Inamullah, F., Khan, U. and Khalil, I.H., 2011. Environmental effect on wheat penology and yields. Sarhad J. Agric., 27: 395-402.

Iqbal, M., Kahloon, M., Nawaz, M. and Javaid, M., 2011. Effectiveness of some botanical extracts on wheat aphids. J. Anim. Pl. Sci., 21: 114-115.

Iqbal, J., Ashfaq, M. and Ali, A., 2008. Screening of wheat varieties/advance lines against aphid. Pak. Entomol., 30: 77-81.

Irshad, M., 2001. Aphids and their biological control in Pakistan. Pak. J. biol. Sci., 4: 537-541.

Iyaniwura, T.T., 1991. Non-target and environmental hazards of pesticides. Rev. environ. Hlth., 9: 161-176.

Keller, M.A., 1987. Influence of leaf surfaces on movements by the hymenopterus parasitoid Trichogramma exiguum. Ent. Exp. Appl., 43: 55-59.

Kennedy, G.G., 2003. Tomato pests’ parasitoids and predators tritrophic interactions involving the genus Lycopersicon. Annu. Rev. Ent., 48: 51-72.

Khan, S.A., Naseer, H. Ullah, F. and. Hayat, Y., 2007a. Screening of wheat genotypes for resistance against cereal aphid. Sarhad J. Agric., 23: 427-434.

Khan, S.A., Ullah, F., Hussain, N., Sattar, S. and Hayat, Y., 2007b. Natural enemies of cereal aphid in North West Frontier Province (NWFP) of Pakistan. Sarhad J. Agric., 23: 435-439.

Khattab, H., 2007. The defense mechanism of cabbage plant against phloem-sucking aphid (Brevicoryne brassicae L.). Aust. J. Basic appl. Sci., 1: 56-62.

Khan, M. and Gul, S., 2012. Screening of twenty wheat genotypes for resistance against aphid. Annual report, NIFA (Nuclear Institute for food and agriculture, Tarnab, Peshawar). Available at

Leather, S.R., Walters, K.F.A. and Dixon, A.F.G., 1989. Factors determining the pest status of the bird cherry-oat aphid, Rhopalosiphum padi (L.) (Hemiptera: Aphididae), in Europe: a study and review. Bull. entomol. Res., 79: 345-360.

Manya, B.S., 1987. Information and identification of Diuraphis noxia (Homoptera: Aphididae) and other aphid species colonizing leaves of wheat and barley in United States. J. econ Ent., 80: 696-704.

Markova, L. and. Tomchev, N., 2013. Seasonal dynamics of cereal aphid and predators on various wheat genotypes (Triticum aestivum L.) 1st Global virtual conference; April 8-12: 669-673: Agriculture. available at (Web page:

Muhammad, W., Nasir, M. Abbas, S.K. Irshad, M. Abbas, M.W. Nawaz, A. and Atta-ur-Rehman., 2013. Resistance pattern against (Diuraphis noxia) in different wheat varieties/line at district Layyah. Acad. J. Ent., 6: 116-120.

Mushtaq S., Rana, S.A., Khan, H.A. and Ashfaq, M., 2013. Diversity and abundance of family aphididae from selected crops of Faisalabad, Pakistan. Pak. J. agric. Sci., 50: 103-109.

Naz, G. and Akmal, M., 2016. Yield and yield contributing traits of wheat varieties as affected by nitrogen rates. Sarhad J. Agric., 32(3): 212-217.

Pakistan Economic Survey., 2017. Government of Pakistan, ministry of finance.

Punjab Agriculture Research Board Bull., 2011. Wheat aphid is a serious threat which require proactive measures along with multi-pronged strategy to protect the staple food grain. Punjab Agriculture Research Board. (http://

Reidell, W.E. and Kieckhefer, R.W., 1995. Feeding damage effect of three aphid species on wheat root growth. J. Pl. Nutr. 18: 1881-1891.

Ronquim, J.C., Pacheco, J.M. and Ronquim, C.C., 2004. Occurrence and Parasitism of Aphid (Hemiptera: Aphididae) on varieties of Irrigated Oat (Avena spp.) in São Carlos, Brazil. Braz. Arch. Biol. Technol., 47: 163-169.

Schuster, D.J. and Starks, K.J., 1975. Preference of Lysiphlebus testaceipes for greenbug resistant and susceptible small grain species. Environ. Ent., 4: 887-888.

Schadler, M., Brandle, R. and Kempel, A., 2010. Host plant genotype determines bottom-up effects in an aphid-parasitoid-predator system. Ent. Exp. Appl., 135: 162–169.

Shahid, S., Zia, A., Naeem, M. and Naz. F., 2012. Bionomics of aphid and their parasitoid in selected wheat varieties grown under homologous ecological conditions. Pakistan J. Zool., 44: 1423-1430.

Sharma, H. and Ortiz. R., 2002. Host plant resistance to insects: an eco-friendly approach for pest management and environment conservation. J. environ. Biol., 23: 111-136.

Shah, F.M., Razaq, M., Ali, A., Han, P. and Chen. J., 2017. Comparative role of neem seed extract, moringa leaf extract and imidacloprid in the management of wheat aphids in relation to yield losses in Pakistan. PLoS One, 12: e0184639.

Smith, C.M., 1989. Plant resistance to insects. A fundamental approach. John Wiley and Sons Ltd. New York, USA, pp. 286.

Steffey, K. and Gray, M., 2012. Managing insect pests. Illinois agronomy handbook. pp. 179 (http:/

Tobias, S., 1995. Hymenoptera, Keys to the insect of the european part of USSR (eds. G.S. Medvedev). American Publishing Co pvt Ltd., New Dehli. pp. 507.

Tomanovic, Z., Kalallieratos, N.G., Stary, P., Petrovic-Obradovic, G., Athanassiou, O.C. and Stanisavljevic, L.Z., 2008. Cereal aphid (Hemiptera-Aphidoidea) in serbia: Seasonal dynamics and natural enemies. Eur. J. Ent., 105:495-501.

Van Emden H.F., 1986. The interactions of plant resistance and natural enemies: effects on populations of sucking insects. In: Interactions of plant resistance and parasitoids and predators of insects (eds. D.J. Boethel and R.D. Eikenbary). Ellis Horwood, Chichester. pp. 224.

Wains M.S., Jamil, M.W., Ali, M.A., Hussain, M. and Anwar, J., 2014. Germplasm screening and incorporation of aphid resistance in bread wheat (Triticum aestivium L.). J. Anim. Pl. Sci., 23: 919-925.

Wains M.S., Ali, M.A., Hussain, M., Anwar, J., Zulkifal, M. and Sabir, W., 2010. Aphid dynamics in relation to meteorological factors and various management practices in bread wheat. J. Pl. Prot. Res., 50: 385-392.

Zacharia, J.T., 2011. Ecological effects of pesticides, pesticides in the modern world - risks and benefits. (ed. M. Stoytcheva). In Tech, Available at

Zeb, Q., Badshah, H., Ali, H., Shah, R.A. and Rehman, M., 2011. Population of aphid on different varieties/lines of wheat and their effect on yield and thousands grain weight. Sarhad J. Agric., 27: 443-450.

Zeb, Q., Naeem, M., Khan, S.A. and Ahmad. S., 2016. Effect of insecticides on the population of aphids, natural enemies and yield components of wheat. Pakistan J. Zool., 48: 1839-1848.

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