Spatio-temporal variations in wheat aphid populations and their natural enemies in four agro-ecological zones of Pakistan


Authors: Muhammad Faheem aff001;  Shafqat Saeed aff003;  Asif Sajjad aff004;  Su Wang aff005;  Abid Ali aff006
Authors place of work: Department of Entomology, Faculty of Agricultural Sciences and Technology, Bahauddin Zakariya University, Multan, Pakistan aff001;  CABI South East Asia, MARDI, Serdang, Selangor, Malaysia aff002;  Department of Entomology, Faculty of Agriculture & Environmental Sciences, Muhammad Nawaz Shareef University of Agriculture, Multan, Pakistan aff003;  Department of Entomology, University College of Agriculture and Environmental Sciences, The Islamia University of Bahawalpur, Bahawalpur, Pakistan aff004;  Institute of Plant and Environment Protection, Beijing Academy of Agricultural and Forestry Sciences, Beijing, PR China aff005;  Department of Entomology, Faculty of Agriculture, University of Agriculture, Faisalabad, Pakistan aff006
Published in the journal: PLoS ONE 14(9)
Category: Research Article
doi: 10.1371/journal.pone.0222635

Summary

Aphids are major pests of wheat crop in Pakistan inflicting considerable economic losses. A better knowledge of landscape scale spatial distribution of aphids and their natural enemies could be used to improve integrated pest management programs. Therefore, the present study aimed to document spatio-temporal variations in populations of wheat aphids and their natural enemies in Pakistan. The 2-year survey study was carried out at ten experimental farms located in five districts of four contrasted agro-ecological zones of eastern Pakistan (Punjab area) i.e. District Chakwal in arid zone, Gujranwala in rice-cropped zone, Faisalabad in central mixed-cropped zone, and Khanewal and Multan in cotton-cropped zone. The dominant aphid species i.e. Schizaphis graminum, Rhopalosiphum padi, R. maidis and Sitobion avenae varied significantly among the five districts surveyed. The population of S. graminum was observed more abundant in arid, R. padi in rice, S. avenae in aird and rice, and R. maidis in cotton-I zones. Aphids ended their population dynamics on 25th March in central mixed-cropped zone and 12th April in other three zones. Various species of natural enemies, mainly Coccinella septumpunctata, C. undecimpunctata, Menochilus sexmaculata, Chrysoperla carnea, Syrphidae and parasitoid mummies were inconsistently observed in four agro-ecological zones. The population of C. septumpunctata, was observed more abundant in rice zone, C. undecimpunctata and C. carnea in cotton-I and arid zones, M. sexmaculata in cotton-I and II zones, Syrphidae in cotton-I zone and parasitoid mummies in rice and arid zones. There were no clear relationships between aphid and the natural enemy populations. The present study may serve as a baseline regarding distribution of wheat aphids and their natural enemies and the results provided insights for further studies on the potential top-down (natural enemies) versus bottom-up (fertilization and irrigation regimes) forces in management of wheat aphids in eastern Pakistan.

Keywords:

Cereal crops – Cotton – Population dynamics – Rice – Seasons – Wheat – Aphids – Pakistan

Introduction

Wheat (Triticum aestivum L.) is Pakistan’s staple diet and accounts for 10 percent of value added in agriculture and contributes over two percent to the country’s GDP [1]. It has been cultivated on over nine million ha with production of 26.3 million tons of grains with an average yield of 2,893 kg per ha in 2017–18 [2]. The average wheat yield is even lower than the neighbouring countries like India and Bangladesh i.e. 2,962 kg per ha and 4357 kg per ha, respectively [1]. Several factors are responsible for the low yield of wheat in Pakistan like varieties [3], sowing time [4], improper inputs as water and fertilizers [5], weeds [6] rainfall and insect pests. Among insect pest, wheat aphids are gradually attaining regular pest status in Pakistan [7]. Aphids reduce yield by direct damages i.e. sap sucking from plant parts, yellowing and reduced grain size [8, 9], and indirect damages through transmitting plant virus [10, 11]. The direct wheat yield losses may reach up to 35–40% and indirect losses up to 20–80% due to aphids [12].

Several species of aphids have been reported from various agro-ecological zones of Pakistan. Rhopalosiphum padi, Sitobion avenae and Schizaphis graminum have been reported from Khayber Pakhtun Khaw (KPK) province while, Macrosiphum miscanthi, Sipha mydis and Sipha elegans from northern hilly areas (temperate climate) [1315]. In addition to S. graminum and M. miscanthi, Aphis maidis has been recorded from the plains of the Punjab [16, 17]. Punjab province has been divided into eleven agro-ecological zones on the basis of climates supporting particular cropping patterns [18]. The population dynamic pattern of aphids varies in different agro-ecological zones of Pakistan due to variation in climatic conditions. They appeared and departed earlier in the warmer areas and later in the colder areas [15]. Population fluctuations have also been recorded among consecutive years within a location [15, 1921]. Multiple factors affect spatial distribution of aphids including climatic conditions and some biotic factors such as quality of host plants, dispersal efficacy of aphids and natural enemies [22, 23].

The infestation of cereal aphids can be reduced by applying various biological, cultural and chemical control strategies [24]. Pesticides are being used against aphids on wheat, known to have negative effects on key beneficial arthropods [25, 26], including natural enemies of aphids e.g. affect the oviposition behaviour and functional response of parasitosis i.e. Aphidius ervi, Diaeretiella rapae, A. matricariae, Aphytis melinus, Lysiphlebus fabarum [2731], besides promoting selection of resistances in pest populations [32, 33]. Knowledge of spatial distribution of aphids at the field scale can be used to create or improve pest monitoring procedures and adjust pesticide application programs, as well as to effectively plan augmentative releases of biological control agents [3436]. Temporal distribution of sucking insect pests and their natural enemies in different crops have been studied worldwide [3742]. However, in Pakistan, there is few information on spatial and temporal variations in natural enemies of wheat aphids, notably with special reference to their potential top-down effect, their present status and distribution patterns.

Therefore, there is need to conduct a study to investigate tempo-spatial variations in populations and seasonal dynamics of various aphid species and their natural enemies across the four agro-ecological zones in eastern Pakistan. These findings could serve as a baseline for using natural enemies in optimized integrated aphid management strategies in plain areas of the Pakistan.

Materials and methods

Study area

The study was conducted at ten experimental farms without use of pesticides in four agro-ecological zones of Punjab, Pakistan during two consecutive wheat growing seasons in 2010 and 2011 (Fig 1). The agro-ecological zones, i.e., cotton zone, central mixed zone, rice zone and arid zone [18] are established on the basis of average annual rainfall i.e. 156, 446, 800 and 900 mm, respectively [43]. District Khanewal and Bahawalpur were selected from cotton zone (we regarded Khanewal as cotton zone I and Bahawalpur as cotton zone II), Faisalabad from central mixed zone, Gujranwala from rice zone and Chakwal from arid zone. In each district, two experimental plots (2 ha for each) were selected with minimum 10 km buffer from each other having wheat crops and other vegetation (Table 1, Fig 1). To overcome the marginal effects, each study plot was surrounded by wheat fields by at least 1 ha. Commonly grown wheat variety ‘Sahar’ was planted in two 2-ha plots at each agro-ecological zone through drill sowing method at the sowing rate of 125 kg/ha from October 15th to 31st in both growing seasons (2010–2011). All agronomic practices were done according to local recommendations.

The map of experimental plots in five districts of Punjab province of Pakistan.
Fig. 1. The map of experimental plots in five districts of Punjab province of Pakistan.
Tab. 1. Detail for the distribution and selection of experimental plots in four different ecological zones during 2010 and 2011 in Punjab province of Pakistan.
Detail for the distribution and selection of experimental plots in four different ecological zones during 2010 and 2011 in Punjab province of Pakistan.

Sampling

Weekly visual observations of aphids and their natural enemies were started from 8th February to 12th April during both the seasons. Three hundred and forty eight sampling points were selected in each of 2-ha plot in zigzag fashion on each observation day and completed within a week from all ten locations. On each sampling point, three consecutive tillers of a wheat plant were randomly selected and visually observed for counting species of aphids (Schizaphis graminum, Rhopalosiphum padi, Rhopalosiphum maidis and Sitobion avenae) and their natural enemies (Coccinella septumpunctata, C. undecimpunctata, Menochilus sexmaculata, Chrysoperla carnea, syrphidae and parasitoid mummies). Aphid species were morphologically identified using the identification keys developed by the University of Idaho [44]. Only the visually identifiable mummies e.g. having change in colour and swollen were counted, while already hatched mummies were excluded from the counts. In the case of heavy infestation of aphids, tillers were clipped and put in paper bags, which were then preserved in ice chest boxes for later counting in the laboratory [45].

Statistical analyses

Prior to analysis, data were checked for their conformance to the normal distribution using Kolmogrov-Simirnov normality test. Per tiller populations of aphids and natural enemies among the five locations were compared per species (or group of species) using Kruskal-Wallis tests. The means of ranks were compared using Dunn’s post hoc test. To compare the difference in the means of population of aphids and natural enemies between the two years, T-test (two tailed, paired sample) was applied. The relationship between natural enemy and aphid density was tested using linear regression analysis. The data of all aphids and natural enemies species were pooled to compare the relative proportion of natural enemies and aphids in four agro-ecological zones during 2010 and 2011. XLSTAT computer software was used for all analysis [46].

Results

Population dynamics of aphids

In 2010 season, the population of all four aphid species did not differ significantly among the five districts (S. graminum: KW = 3.27, P = 0.51, d.f. = 4; R. padi: KW = 2.97, P = 0.56, d.f. = 4; R. maidis: KW = 3.92, P = 0.42, d.f. = 4; S. avenae: KW = 1.55, P = 0.82, d.f. = 4) (Table 2). All the aphid species were present from 18th February to 4th March. The peak activity period of aphids lasted from 11th to 18th March. During this period, the aphid species, S. graminum and R. padi were the most abundant in arid zone while R. maidis and S. avenae in cotton zone II and cotton zone I, respectively (Fig 2).

Seasonal fluctuation of different aphid species in four ecological zones of Punjab, Pakistan during 2010 and 2011.
Fig. 2. Seasonal fluctuation of different aphid species in four ecological zones of Punjab, Pakistan during 2010 and 2011.
(a) Schizaphis graminum, (b) Rhopalosiphum padi, (c) R. maidis and (d) Sitobion avenae. Error bars show ± standard error of means.
Tab. 2. Means of ranks of population of aphids and their natural enemies as computed by Dunn’s post hoc test at alpha 0.05.
Means of ranks of population of aphids and their natural enemies as computed by Dunn’s post hoc test at alpha 0.05.

In 2011 season, except for S. avenae, the population of S. graminum, R. padi and R. maidis varied significantly (KW = 17.81, P<0.001, d.f. = 4; KW = 16.68, P<0.001, d.f. = 4; KW = 11.12, P = 0.03, d.f. = 4; respectively) among the five districts (Table 2). All aphid species started their activity from 15th February. Peak abundance of all aphid species was recorded from 8th to 22nd March followed by a sharp or gradual decline until 12th April (Fig 2). The abundance of the species varied greatly among different zones during peak activity period (8th to 22nd March). Schizaphis graminum and R. padi were the most abundant at arid and rice zones, respectively. Rhopalosiphum maidis was the most abundant at cotton zone II whereas it was the least abundant on 22nd March during 2011. Sitobion avenae was the most abundant at cotton zone I on the 22nd March (Fig 2).

Population dynamics of natural enemies

In 2010 season, the population of syrphids and mummies varied significantly (KW = 22.12, P<0.001, d.f. = 4; KW = 11.54, P = 0.02, d.f. = 4, respectively) among the five districts of four agro-ecological zones. The Dunn’s post hoc test showed the maximum mean of ranks for Syrphidae in cotton zone I and the minimum for arid zone. In the case of mummies, the maximum mean of ranks was recorded for rice zone and the minimum for cotton zone II (Table 2). Population dynamics of all the natural enemies started to increase from the 11th March and attained peak from 18th March to 1st April (Fig 3A–3F).

Seasonal fluctuation of different natural enemies in four ecological zones of Punjab, Pakistan during 2010 and 2011.
Fig. 3. Seasonal fluctuation of different natural enemies in four ecological zones of Punjab, Pakistan during 2010 and 2011.
(a) Coccinella septumpunctata, (b) C. undecimpunctata, (c) Menochilus sexmaculata. (d) Chrysoperla carnea, (e) Syrphidae and (f) Mummies. Error bars show ± standard error of means.

In 2011 season, except for C. septumpunctata (KW = 13.79, P = 0.01, d.f. = 4), all the other five natural enemies did not differ significantly among the five districts (all P>0.05, d.f. = 4). The Dunn’s post hoc test showed the maximum mean of ranks of C. septumpunctata in rice zone and the minimum in the mixed zone (Table 2). The three types of natural enemies, C. septumpunctata, syrphid and mummies peaked from 29th March to 5th April. Coccinella undecimpunctata and M. sexmaculata abundance were relatively low during the season (Fig 3A–3F).

Overall seasonal comparison of aphids revealed that S. graminum and R. maidis were more abundant in 2010 than those in 2011(T = 2.81, P = 0.006, d.f. = 93 and T = 2.13, P = 0.036, d.f. = 93, respectively). There was no significant relationship between populations of the aphids and their natural enemies in both seasons (linear regressions: both P>0.05). The relative proportion between cumulative aphids and natural enemies population in five zones showed that the highest relative proportion of natural enemies to aphids was observed in rice and arid zones during 2010, and rice and mix zones during 2011. The natural enemies were relatively more abundant during 2010 than 2011 (Fig 4).

Relative proportion of cumulative aphids and natural enemies species in four ecological zones of Punjab, Pakistan during 2010 and 2011.
Fig. 4. Relative proportion of cumulative aphids and natural enemies species in four ecological zones of Punjab, Pakistan during 2010 and 2011.
Diagonal line area = Aphids, Diamond grid area = Natural enemies.

Discussion

The populations of aphid species did not differ significantly among the five districts in season 2010 except for S. avenae, which differed significantly in season 2011. Spatial variation of aphids and other insect pest species is predicted by climatic conditions and some biotic factors such as dispersal efficiency, host plants genotype identity and natural enemies [22, 23, 47]. The migration is another factor which may affect aphid populations while temperature is a dominant factor affecting aphid migration phonologies [48]. Understanding spatial variability of aphids in wheat agro-ecosystems using certain models can potentially facilitate site specific application of pesticides, decreasing the amount and cost of pesticides, environmental pollution and pesticide exposure to farmers while increasing the biological control agents [49]. A recent preliminary study suggests that forecasting of aphid epidemics can be more reliable within the radius of only 10 km [50]. However, landscape scale studies can create or improve pest monitoring procedure and pesticide application programs at regional level [36].

Sitobion avenae was the most abundant in arid and rice zones whereas R. padi in rice zone. On the other hand, population densities of R. maidis were the most abundant in cotton zone I. The distribution patterns of wheat aphid species have not been reported so far in Punjab province of Pakistan. It is known that abiotic factors such as temperature, rainfall, fertilization and irrigation are crucial for regulating arthropod populations [5158]. Both the arid and rice zones of Punjab are relatively colder with high altitude and rainfall while cotton zone is relatively warmer with low altitude and rainfall. The mean monthly temperatures of arid, rice and cotton zone are 20°C, 25°C and 30°C, respectively while annual rainfall is 40, 20 and 10 inches, respectively [59].

In present study, the peak activity period of all the aphid species lasted from 11th to 18th March in 2010 while from 8th to 22nd March in 2011 followed by a sharp or gradual decline until 12th April. Khan (2005) [15] reported seasonal trends of wheat aphids from Khayber Pakhtun Khaw (KPK) province i.e. aphids appear and depart earlier in warmer districts and vice versa. However, we did not see any remarkable difference in aphids’ dynamics among the warmer and colder districts of Punjab in this study. This might be due to overall colder climate of KPK compared to the districts of Punjab. Mühlenberg and Stadler (2005) [60] reported similar findings that the warmer and drier conditions at the low altitude site resulted in earlier aphid multiplication in spring compared with high altitude site, where aphid population got their peak few weeks later.

Seasonal dynamics of aphids followed almost similar pattern in both growing seasons (2010 and 2011), i.e. the population started to grow from the 15th February, peaked during last fortnight of March followed by a sharp or gradual decline until the 12th April. Seasonal dynamic pattern of aphids varied across latitude as several previous studies have documented slightly different trends in Multan and Peshawar districts. Aslam et al. (2004) [16] reported that in Multan population appeared on the 3rd week of January and increased exponentially and peaked on the 3rd week of March followed by a sudden decline after the 4th week of March until the 1stweek of April. Similarly, Khattak et al (2007) [19] reported from Peshawar that population of aphids started to build up from the 2nd week of January and attained its peak on the first two weeks of March. Another study from Peshawar suggested that aphid population started to increase in the last week of December, remained low populations in January and peaked in the 1st week of March [20].

Population dynamics of natural enemies attained their peak from the 18th March to 1st April in 2010 while 29th March to 5th April in 2011. Similar findings have been reported by Saleem et al. (2009) [20] from Peshawar documenting the peak population density of coccinellids in 4th week of March, syrphids in the 3rd week of March, chrysopids in the 2nd week of April and parasitoids in the 3rd week of March. The fluctuation of natural enemies was more abrupt than aphids in 2010 season compared to 2011 season. The populations of Syrphidae and mummies varied significantly among the five districts in season 2010 while only C. septumpunctata varies significantly in season 2011. Syrphid flies are efficient predators of aphids and exponentially decrease their population [61, 62]. The relationship between predators and prey densities has been a central theme in ecological theories [63, 64]. In agricultural system, predator-prey interactions play a key role in suppressing herbivore prey (often regarded as pests), which is suggested to be examined aiming to reduce crop damage and increase crop yield [40, 6569]. Ideally, predators should respond numerically by aggregating attacks with high prey densities for an effective biological control or switch among different prey species pending on their relative abundance [7073]. However, such an ideal scenario has rarely been supported by empirical data. In present study we found no correlation between the population of aphids and natural enemies in both years. Several factors may explain such discrepancies including differences in spatial scale at which observations are made [74], behavioral differences among species, varying habitat features (i.e. shelters and nesting sites), availability & distribution of alternate prey [23, 37, 75], and genotypic diversity that can influence the effects of spatial processes on the plant-herbivore interactions [47]. These factors are also important with view point of aphids forecasting as they determine the reinvasion pattern in the following season [76].

The present study for the first time established a baseline data on distribution and seasonal population dynamics of wheat aphids and their natural enemies in four agro-ecological zones in eastern Pakistan. Further research is warranted to examine (i) the top-down vs. bottom-up forces in wheat agro-ecosystems in order to develop sustainable IPM, and (ii) side effects of commonly used insecticides on the behavior and physiology of those potential natural enemies.


Zdroje

1. Pakissan. Spotlight on Pakistan’s wheat economy. Pakissan.com. 2017. Available from: http://www.pakissan.com/2017/08/02/spotlight-on-pakistans-wheat-economy/amp

2. Asmat R. Pakistan grain and feed update. USDA Global Agriculture Information Network. 2018; Report No. PK1823.

3. Khan AM, Khan AA, Afzal M, Iqbal MS. Wheat crop yield losses caused by the aphids infestation. J Biofertil Biopestici. 2012; 3:122. doi: 10.4172/2155-6202.1000122

4. Aheer GM, Haq I, Ulfat M, Ahmad KJ, Ali A. Effects of sowing dates on aphids and grain yield in wheat. J Agric Res. 1993; 31: 75–79.

5. Kibe AM, Singh S, Kalrac N. Water-nitrogen relationships for wheat growth and productivity in late sown conditions. Agric Water Manage. 2006; 84: 221–228.

6. Memon RA, Bhatti GR, Khalid S, Mallah A, Ahmed S. Illustrated weed flora of wheat crop of Khairpur District, Sindh. Pak J Bot. 2013; 45: 39–47.

7. Aheer GM, Ali A, Munir M. Abiotic factors effect on population fluctuation of alate aphids in wheat.–J Agric Res. 2008; 46: 367–371.

8. Angood BA, Stewart RK. Effect of cereal aphid infestation on grain yield and percentage protein of barley, wheat and oats in Southwestern Quebec.–Can Entomol. 1980; 112: 681–686.

9. Hullé M, Chaubet B, Turpeau E, Simon JC. Encyclop’Aphid: a website on aphids and their natural enemies. Entomol Gen. 2019. doi: 10.1127/entomologia/2019/0867

10. Gair R, Jenkins JEE, Lester E. Cereal pests and diseases.–Farming Press Ltd., UK, 1983; pp. 54–80.

11. Fiebig M, Poehling HM. Host-plant selection and population dynamics of the grain aphid Sitobion avenae (F.) on wheat infected with Barley Yellow Dwarf Virus.–Bull.IOBC/WPRS.1998; 21: 51–62.

12. Aslam M, Razaq M, Akhter W, Faheem M, Ahmad F. Effect of sowing date of wheat on aphid (Schizaphis graminum RONDANI) population. Pak Entomol. 2005; 27: 79–82.

13. Khan SM, Maqbool R. Varietal performance of wheat (Triticum aestivum) against wheat aphid (Macrosiphum miscanthi) and its chemical control with different doses of insecticides.–Asian J Plant Sci. 2002; 1: 205–207.

14. Mahmood R, Poswal MA, Shehzad A. Distribution, host range and seasonal abundance of Sipha sp. (Homoptera: Aphididae) and their natural enemies in Pakistan.–Pak J Biol Sci. 2002; 5: 47–50.

15. Khan SA. Studies on aphid distribution pattern and their natural enemies in wheat and maize crop. PhD thesis.–Department of Plant Protection, Agricultural University Peshawar-Pakistan. 2005; pp 179.

16. Aslam M, Razaq M, Ahmad F, Faheem M, Akhter W. Population of aphid (Schizaphis graminum R.) on different varieties/lines of wheat (Triticum aestivum L.). Int J Agric Bio. 2004; l6: 974–977.

17. Inayat TP, Rana SA, Rana N, Ruby T, Sadique MJI, Abbas MN. Predation rate in selected coccinellid (coleoptera) predators on some major aphids and coccinellids (Hemipteran) pests. Int J Agric Biol. 2011;13: 427–430.

18. PARC. Agro-ecological regions of Pakistan. Pakistan Agriculture Research Council, Islamabad. 1980.

19. Khattak MK, Riazuddin, Anayatullah N. Population dynamics of aphids (Aphididae: Homoptera) on different wheat cultivars and response of cultivars to aphids in respect of yield and yield related parameters. Pak J Zool. 2007; 39:109–115.

20. Saleem S, Ullah F, Ashfaque M. Population dynamics and natural enemies of aphids on winter wheat in Peshawar, Pakistan. Pak J Zool. 2009; 41: 505–513.

21. Zeb Q, Badshah H, Ali H, Shah RA, Rehman M. Population of aphids on different varieties/lines of wheat and their effect on yield and thousands grain weight. Sarhad J Agric. 2011; 27: 443–450.

22. Mann JA, Tatchel GM, Dupuch MJ, Harrington R, Clark SJ, Mccartney HA. Movement of apterous Sitobion avenae (Homoptera: Aphididae) in response to leaf disturbances caused by wind and rain. Annals Appl Biol. 1995; 125:417–427.

23. Elliott NC, Kieckhefer RW. Response by coccinellids to spatial variation in cereal aphid density. Popul Ecol. 2000; 42: 81–90.

24. Brewer MJ, Elliott NC. Biological control of cereal aphids in North America and mediating effects of host plant and habitat manipulations. Ann Rev Entomol. 2004; 49: 219–242.

25. Desneux N, Decourtye A, Delpuech JM. The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol. 2007; 52: 81–106. doi: 10.1146/annurev.ento.52.110405.091440 16842032

26. Decourtye A, Henry M, Desneux N. Overhaul pesticide testing on bees. Nature, 2013; 497:188.

27. Desneux N, Pham-Delègue MH, Kaiser L. Effects of sublethal and lethal doses of lambda-cyhalothrin on oviposition experience and host searching behaviour of a parasitic wasp, Aphidius ervi. Pest Manag Sci. 2004; 60: 381–89. doi: 10.1002/ps.822 15119601

28. Desneux N, Wajnberg E, Fauvergue X, Privet S, Kaiser L. Sublethal effects of a neurotoxic insecticide on the oviposition behaviour and the patch-time allocation in two aphid parasitoids, Diaeretiella rapae and Aphidius matricariae. Entomol Exp Appl. 2004; 112:227–235.

29. Biondi A, Campolo O, Desneux N, Siscaro G, Palmeri V, Zappalà L. Life stage-dependent susceptibility of Aphytis melinus DeBach (Hymenoptera: Aphelinidae) to two pesticides commonly used in citrus orchards. Chemosphere, 2015; 128:142–147. doi: 10.1016/j.chemosphere.2015.01.034 25698292

30. Jam NA, Saber M. Sublethal effects of imidacloprid and pymetrozine on the functional response of the aphid parasitoid, Lysiphlebus fabarum. Entomol Gen. 2018; 38:173–190.

31. Mohammed AAH, Desneux N, Fan YJ, Han P, Ali A, Song DL, Gao XW. Impact of imidacloprid and natural enemies on cereal aphids: Integration or ecosystem service disruption? Entomol Gen. 2018; 37:47–61.

32. Liang P, Tian YA, Biondi A, Desneux N, Gao XW. Short-term and transgenerational effects of the neonicotinoid nitenpyram on susceptibility to insecticides in two whitefly species. Ecotoxicology. 2012; 21:1889–1898. doi: 10.1007/s10646-012-0922-3 22661314

33. Liu XL, Tang QL, Li YD, Mateus RC, Liang P, Gao XW. Widespread resistance of the aphid Myzus persicae to pirimicarb across China, and insights on ace2 mutation frequency in this species. Entomol Gen. 2017; 36:285–299.

34. Weisz R, Fleischer S. Site-specific integrated pest management for high value crops: some units for map generation using the Colorado potato beetle (Coleoptera: Chrysomelidae) as a model system. J Econ Entomol. 1995; 88: 1069–1080. doi: 10.1093/jee/88.5.1069 7593891

35. Winder L, Perry JN, Holland JM. The spatial and temporal distribution of the grain aphid, Sitobion avenae in winter wheat. Entomol Exp Appl. 1999; 93: 277–290.

36. Young CL, Wright MG. Seasonal and spatial distribution of banana aphid, Pentalonia nigronervosa (Hemiptera: Aphididae), in banana plantations on Oahu. In: Proc Hawaiian Entomol Soc.– 2005; 37: 73–80.

37. Desneux N, O’Neil RJ, Yoo HJS. Suppression of population growth of the soybean aphid, Aphis glycines Matsumura, by predators: the identification of a key predator and the effects of prey dispersion, predator abundance, and temperature. Environ Entomol.– 2006a; 35: 1342–1349.

38. Desneux N, Rabasse JM, Ballanger Y, Kaiser L. Parasitism of canola aphids in France in autumn. J Pest Sci. 2006b; 79: 95–102.

39. Jankovic M, Plecas M, Sandic D, Popovic A, Petrovic A, Petrovic-Obradovic O, et al. Functional role of different habitat types at local and landscape scales for aphids and their natural enemies. J Pest Sci. 2017; 90: 261–273.

40. Han P, Niu CY, Desneux N. Identification of top-down forces regulating cotton aphid population growth in transgenic Bt cotton in central China. PloS One. 2014a; 9: e102980. doi: 10.1371/journal.pone.0102980 25170907

41. Jaworski CC, Xiao D, Xu QX, Ramirez-Romero R, Guo XJ, Wang S, et al. Varying the spatial arrangement of synthetic herbivore-induced plant volatiles and companion plants to improve conservation biological control. J Appl Ecol. 2019; 56: 1176–1188.

42. Yang F, Xu L, Wu YK, Wang Q, Yao ZW, Zikic V, et al. Species composition and seasonal dynamics of aphid parasitoids and hyperparasitoids in wheat fields in northern China. Sci Rep. 2017; 7: 13989. doi: 10.1038/s41598-017-14441-6 29070808

43. FAO. Fertilizer use by crop in Pakistan, Land and Plant Nutrition Management Service, Land and Water Development Division. Food and Agriculture Organization of the United Nations, Rome. 2004.

44. Stoltz RL, Baird CR, Sandvol LE, Homan HW. Identification keys for insect pests in Pacific Northwest field crops. University of Idaho. 1999. (http://www.cals.uidaho.edu/edcomm/keys/plates/plates_contents.htm). Accessed on 10 Nov 2009.

45. Klueken AM, Hau B, Koepke I, Poehling HM. Comparison of techniques to survey populations of cereal aphids (Homoptera: Aphididae) in winter cereals during autumn and spring with special consideration of sample size. J Plant Dis Prot. 2008; 115: 279–287.

46. XLSTAT. XLSTAT Software.–Addinsoft. 2008. http://xlstat.com/en/download. Accessed on 20 Aug 2010.

47. Genung MA, Crutsinger GM, Bailey JK, Schweitzer JA, Sanders NJ. Aphid and ladybird beetle abundance depend on the interaction of spatial effects and genotypic diversity. Oecologia. 2012; 168(1):167–74. doi: 10.1007/s00442-011-2080-3 21805301

48. Zhou X, Harrington R, Woiwod IP, Perrey JN, Bale JS, Clark SJ. Effects of temperature on aphid phenology. Global Change Biol. 1995; 1: 303–313.

49. Merrill SC, Holtzer TO, Peairs FB, Lester PJ. Modeling spatial variation of Russian wheat aphid overwintering population densities in Colorado winter wheat. J. Econ. Entomol. 2009; 102(2): 533–541. doi: 10.1603/029.102.0210 19449632

50. Damgaard C, Bruus M, Joergen AA. The effect of spatial variation for predicting aphid epidemics. BiorRxiv. 2018. doi: org/10.1101/367953

51. Frampton GK, Van Den Brink PJ, Gould PJL. Effects of spring drought and irrigation on farmland arthropods in southern Britain. J App Ecol. 2000; 37: 865–883.

52. Ovadia O, Schmitz OJ. Weather variation and trophic interaction strength: sorting the signal from the noise. Oecologia. 2004; 140: 398–406. doi: 10.1007/s00442-004-1604-5 15179581

53. Han P, Lavoir AV, Le Bot J, Amiens-Desneux E, Desneux N. Nitrogen and water availability to tomato plants triggers bottom-up effects on the leafminer Tuta absoluta. Sci Rep. 2014b; 4: 4455. doi: 10.1038/srep04455 24675796

54. Han P, Dong Y, Lavoir AV, Adamowicz S, Bearez P, Wajnberg E et al. Effect of plant nitrogen and water status on the foraging behavior and fitness of an omnivorous arthropod. Eco Evol. 2015a; 5: 5468–5477.

55. Han P, Bearez P, Adamowicz S, Lavoir AV, Desneux N. Nitrogen and water limitations in tomato plants trigger negative bottom-up effects on the omnivorous predator Macrolophus pygmaeus. J Pest Sci. 2015b; 88: 685–691. doi: 10.1007/s10340-015-0662-2

56. Gao GZ, Feng LK, Perkins LE, Sharma S, Lu ZZ. Effect of the frequency and magnitude of extreme temperature on the life history traits of the large cotton aphid, Acyrthosiphon gossypii (Hemiptera: Aphididae): implications for their population dynamics under global warming. Entomol Gen. 2018; 37:103–113

57. Horgan FG, Vu Q, Bernal CC, Ramal AF, Villegas JM, Almazan MLP. Population development of rice black bug, Scotinophara latiuscula (Breddin), under varying nitrogen in a field experiment. Entomol Gen. 2018; 37:19–33.

58. Nguyen LTH, Monticelli LS, Desneux N, Metay-Merrien C, Amiens-Desneux E, Lavoir AV. Bottom-up effect of water stress on the aphid parasitoid Aphidius ervi. Entomol Gen. 2018; 38:15–27.

59. Khan SU, Hassan M, Khan FK, Bari A. Climate classification of Pakistan. Balwois Conference: Republic of Macedonia. 2010; 1–47.

60. Muhlenberg E, Stadler B. Effects of altitude on aphid-mediated processes in the canopy of Norway spruce. Agric For Entomol. 2005; 7: 133–143.

61. Amiri-Jami AR, Sadeghi-Namaghi H. Responses of Episyrphus balteatus DeGeer (Diptera: Syrphidae) in relation to prey density and predator size. J Asia-Pacific Entomol. 2014; 17(3), 207–211.

62. Kafle K. Management of Mustard Aphid Lipaphis erysimi (Kalt.) (Homoptera: Aphididae). Int J App Sci Biotech. 2015; 3(3), 537–540.

63. Krebs CJ. Ecology: The experimental analysis of distribution and abundance. 6th edn. Benjamin Cummings, San Francisco, 2009; pp 655.

64. Begon MC, Townsend R, Harper JL. Ecology from Individuals to Ecosystems.– 4th edn. Malden, Blackwell Publishing, London. 2006; pp 281.

65. Symondson WOC, Sunderland KD, Hgrenstone M. Can generalist predators be effective biocontrol agents? Annu Rev Entomol. 2002; 47: 561–594. doi: 10.1146/annurev.ento.47.091201.145240 11729085

66. Ostman O, Ekborm B, Bengtsson J. Yield increase attributable to aphid predation by ground-living polyphagous natural enemies in spring barley in Sweden. Ecol Econ. 2003; 45: 149–158.

67. Lu Y, Wu K, Jiang Y, Guo Y, Desneux N. Widespread adoption of Bt-cotton and insecticide decrease promotes biocontrol services. Nature. 2012; 487: 362–365. doi: 10.1038/nature11153 22722864

68. Ali A, Desneux N, Lu Y, Liu B, Wu K. Characterization of the natural enemy community attacking cotton aphid in the Bt cotton ecosystem in Northern China. Sci Rep. 2016; 6: 24273; doi: 10.1038/srep24273 27075171

69. Ali A, Desneux N, Lu YH, Wu KM. Key aphid natural enemies showing positive effects on wheat yield through biocontrol services in northern China. Agrics Ecosyst Environ. 2018; 266:1–9.

70. Holt RD, Lawton JH. The ecological consequences of shared natural enemies.–Annu Rev Ecol Syst. 1994; 25: 495–520.

71. Murdoch WW, Briggs CJK. Theory of biological control: recent developments. Ecology. 1996; 77: 2001–2013.

72. Jaworski CC, Bompard A, Genies L, Amiens-Desneux E, Desneux N. Preference and prey switching in a generalist predator attacking local and invasive alien pests. PloSOne. 2013; 8(12): p.e82231.

73. Jaworski CC, Chailleux A, Bearez P, Desneux N. Apparent competition between major pests reduces pest population densities on tomato crop, but not yield loss. J Pest Sci. 2015; 88: 793–803.

74. Ray C, Hastings A. Density dependence: are we searching at the wrong spatial scale? J Anim Ecol. 1996; 65:556–566.

75. van Baalen M, Krivan V, van Rijn PCJ, Sabelis MW. Alternative food, switching predators, and the persistence of predator-prey systems. Am Nat. 2001; 157: 512–524. doi: 10.1086/319933 18707259

76. Mazzi D, Dorn S. Movement of insect pests in agricultural landscapes. Ann Appl Biol. 2012; 160: 97–113.


Článek vyšel v časopise

PLOS One


2019 Číslo 9

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Krvácení v důsledku portální hypertenze při jaterní cirhóze – od pohledu záchranné služby až po závěrečný hepato-gastroenterologický pohled
nový kurz
Autoři: PhDr. Petr Jaššo, MBA, MUDr. Hynek Fiala, Ph.D., prof. MUDr. Radan Brůha, CSc., MUDr. Tomáš Fejfar, Ph.D., MUDr. David Astapenko, Ph.D., prof. MUDr. Vladimír Černý, Ph.D.

Rozšíření možností lokální terapie atopické dermatitidy v ordinaci praktického lékaře či alergologa
Autoři: MUDr. Nina Benáková, Ph.D.

Léčba bolesti v ordinaci praktického lékaře
Autoři: MUDr. PhDr. Zdeňka Nováková, Ph.D.

Revmatoidní artritida: včas a k cíli
Autoři: MUDr. Heřman Mann

Jistoty a nástrahy antikoagulační léčby aneb kardiolog - neurolog - farmakolog - nefrolog - právník diskutují
Autoři: doc. MUDr. Štěpán Havránek, Ph.D., prof. MUDr. Roman Herzig, Ph.D., doc. MUDr. Karel Urbánek, Ph.D., prim. MUDr. Jan Vachek, MUDr. et Mgr. Jolana Těšínová, Ph.D.

Všechny kurzy
Kurzy Doporučená témata