Toxicity and sublethal effects of two plant allelochemicals on the demographical traits of cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae)

Autoři: Kangsheng Ma aff001;  Qiuling Tang aff001;  Pingzhuo Liang aff001;  Jin Xia aff001;  Baizhong Zhang aff002;  Xiwu Gao aff001
Působiště autorů: Department of Entomology, China Agricultural University, Beijing, China aff001;  College of Resources and Environment, Henan Institute of Science and Technology, Xinxiang, China aff002
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0221646


Plant allelochemicals are a group of secondary metabolites produced by plants to defend against herbivore. The mortality of two plant allelochemicals (tannic acid and gossypol) on the cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae), were investigated using feeding assays and the sublethal effects were evaluated using the age-stage, two-sex life table approach. Tannic acid and gossypol have deleterious effects on A. gossypii, and as the concentrations increased, the mortality of cotton aphid increased. The life history traits of A. gossypii including the developmental duration of each nymph stage, the longevity, oviposition days, total preadult survival rate and adult pre-oviposition period were not significantly affected by sublethal concentration of tannic acid (20 mg/L) and gossypol (50 mg/L), while the population parameters (r, λ and R0) were significantly affected by these two plant allelochemicals. Furthermore, tannic acid can increase the pre-adult duration time and TPOP but reduce the fecundity of A. gossypii significantly compared to the control and gossypol treatment groups. These results are helpful for comprehensively understanding the effects of plant allelochemicals on A. gossypii.

Klíčová slova:

Aphids – Cotton – Diet – Fecundity – Herbivory – Insect pests – Nymphs – Plant-herbivore interactions


1. Després L, David JP, Gallet C. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol. 2007; 22(6): 298–307. doi: 10.1016/j.tree.2007.02.010 17324485

2. Li XC, Berenbaum MR, Schuler MA. Plant allelochemicals differentially regulate Helicoverpa zea cytochrome P450 genes. Insect Mol Biol. 2002; 11(4): 343–351. doi: 10.1046/j.1365-2583.2002.00341.x 12144700

3. Nishida R. Chemical ecology of insect-plant interactions: ecological significance of plant secondary metabolites. Biosci Biotech Bioch. 2014; 78(1): 1–13.

4. Golawska S, Sprawka I, Lukasik I, Golawski A. Are naringenin and quercetin useful chemicals in pest-management strategies? J Pest Sci. 2014; 87: 173–180.

5. Selin-Rani S, Senthil-Nathan S, Thanigaivel A, Vasantha-Srinivasan P, Edwin ES, Ponsankar A, et al. Toxicity and physiological effect of quercetin on generalist herbivore, Spodoptera litura Fab. and a non-target earthworm Eisenia fetida Savigny. Chemosphere. 2016; 165: 257–267. doi: 10.1016/j.chemosphere.2016.08.136 27657818

6. Stipanovic RD, Lopez JD Jr., Dowd MK, Puckhaber LS, Duke SE. Effect of racemic and (+)- and (-)-gossypol on the survival and development of Helicoverpa zea larvae. J Chem Ecol. 2006; 32(5): 959–968. doi: 10.1007/s10886-006-9052-9 16739016

7. Wang Q, Eneji AE, Kong X, Wang K, Dong H. Salt stress effects on secondary metabolites of cotton in relation to gene expression responsible for aphid development. PLoS One. 2015; 10(6): e0129541. doi: 10.1371/journal.pone.0129541 26061875

8. Simmonds MS, Stevenson PC. Effects of isoflavonoids from Cicer on larvae of Heliocoverpa armigera. J Chem Ecol. 2001; 27(5): 965–977. doi: 10.1023/a:1010339104206 11471948

9. Zhang L, Lu Y, Xiang M, Shang QL, Gao XW. The retardant effect of 2-tridecanone, mediated by cytochrome P450, on the development of cotton bollworm, Helicoverpa armigera. BMC Genomics. 2016; 17(1): 954. doi: 10.1186/s12864-016-3277-y 27875986

10. Klocke JA, Chan BG. Effects of cotton condensed tannin on feeding and digestion in the cotton pest, Heliothis zea. J Insect Physiol. 1982; 28: 911–915.

11. Krempl C, Heidel-Fischer HM, Jimenez-Aleman GH, Reichelt M, Menezes RC, Boland W, et al. Gossypol toxicity and detoxification in Helicoverpa armigera and Heliothis virescens. Insect Biochem Mol Biol. 2016; 78: 69–77. doi: 10.1016/j.ibmb.2016.09.003 27687846

12. Du L, Ge F, Zhu S, Parajulee MN. Effect of cotton cultivar on development and reproduction of Aphis gossypii (Homoptera: Aphididae) and its predator Propylaea japonica (Coleoptera: Coccinellidae). J Econ Entomol. 2004; 97: 1278–1283. doi: 10.1093/jee/97.4.1278 15384338

13. Guo JY, Wu G, Wan FH. Effects of high-gossypol cotton on the development and reproduction of Bemisia tabaci (Hemiptera: Aleyrodidae) MEAM1 cryptic species. J Econ Entomol. 2013; 106(3): 1379–1385. doi: 10.1603/ec12401 23865205

14. Celorio-Mancera MdlP, Ahn SJ, Vogel H, Heckel DG. Transcriptional responses underlying the hormetic and detrimental effects of the plant secondary metabolite gossypol on the generalist herbivore Helicoverpa armigera. BMC Genomics. 2011; 12: 575. doi: 10.1186/1471-2164-12-575 22111916

15. Peng TF, Pan YO, Gao XW, Xi JH, Zhang L, Yang C, et al. Cytochrome P450 CYP6DA2 regulated by cap 'n'collar isoform C (CncC) is associated with gossypol tolerance in Aphis gossypii Glover. Insect Mol Biol. 2016; 25(4): 450–459. doi: 10.1111/imb.12230 27005728

16. Karowe DN. Differential effect of tannic acid on two tree-feeding Lepidoptera: implications for theories of plant anti-herbivore chemistry. Oecologia. 1989; 80: 507–512. doi: 10.1007/BF00380074 28312836

17. War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, et al. Mechanisms of plant defense against insect herbivores. Plant Signal Behav. 2012; 7(10): 1306–1320. doi: 10.4161/psb.21663 22895106

18. Blackman RL, Eastop VF. Aphids on the world's crops: An identification guide. John Wiley and Sons, NY. 1984.

19. Qu YY, Xiao D, Li J, Chen Z, Biondi A, Desneux N, et al. Sublethal and hormesis effects of imidacloprid on the soybean aphid Aphis glycines. Ecotoxicology. 2015; 24(3): 479–487. doi: 10.1007/s10646-014-1396-2 25492586

20. 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

21. Stark JD, Banks JE. Population-level effects of pesticides and other toxicants on arthropods. Annu Rev Entomol. 2003; 48: 505–519. doi: 10.1146/annurev.ento.48.091801.112621 12221038

22. Akca I, Ayvaz T, Yazici E, Smith CL, Chi H. Demography and population projection of Aphis fabae (Hemiptera: Aphididae): with additional comments on life table research criteria. J Econ Entomol. 2015; 108(4): 1466–1478. doi: 10.1093/jee/tov187 26470285

23. Chi H, Getz WM. Mass rearing and harvesting based on an age-stage, wwo-sex life table: a potato tuberworm (Lepidoptera: Gelechiidae) case study. Environ Entomol. 1988; 17(1): 18–25.

24. Tang QL, Xiang M, Hu HM, An CJ, Gao XW. Evaluation of sublethal effects of sulfoxaflor on the green peach aphid (Hemiptera: Aphididae) using life table parameters. J Econ Entomol. 2015; 108(6): 2720–2728. doi: 10.1093/jee/tov221 26470367

25. Xiao D, Zhao J, Guo X, Chen H, Qu M, Zhai W, et al. Sublethal effects of imidacloprid on the predatory seven-spot ladybird beetle Coccinella septempunctata. Ecotoxicology. 2016; 25(10): 1782–1793. doi: 10.1007/s10646-016-1721-z 27670666

26. Zhang P, Liu F, Mu W, Wang Q, Li H, Chen C. Life table study of the effects of sublethal concentrations of thiamethoxam on Bradysia odoriphaga Yang and Zhang. Pestic Biochem Physiol. 2014; 111: 31–37. doi: 10.1016/j.pestbp.2014.04.003 24861931

27. Ma KS, Li F, Liang PZ, Chen XW, Liu Y, Gao XW. Identification and validation of reference genes for the normalization of gene expression data in qRT-PCR analysis in Aphis gossypii (Hemiptera: Aphididae). J Insect Sci. 2016; 16(1): 1–9.

28. Ma KS, Li F, Liang PZ, Chen XW, Liu Y, Tang QL, et al. RNA interference of Dicer-1 and Argonaute-1 increasing the sensitivity of Aphis gossypii Glover (Hemiptera: Aphididae) to plant allelochemical. Pestic Biochem Physiol. 2017; 138: 71–75. doi: 10.1016/j.pestbp.2017.03.003 28456307

29. Chi H. Life-table analysis incorporating both sexes and variable development rates among individuals. Environ Entomol. 1988; 17(1): 26–34.

30. Chi H, Liu H. Two new methods for the study of insect population ecology. Bull Inst Zool Academia Sinica. 1985; 24(2): 225–240.

31. Chi H. TWOSEX-MS Chart: A computer program for the age-stage, two-sex life table analysis. (accessed 30 June 2018).

32. Efron B, Tibshirani RJ. An introduction to the bootstrap. J Great Lakes Res. 1993; 20(1): 1–6.

33. Huang HW, Chi H, Smith CL. Linking demography and consumption of Henosepilachna vigintioctopunctata (Coleoptera: Coccinellidae) fed on Solanum photeinocarpum (Solanales: Solanaceae): with a new method to project the uncertainty of population growth and consumption. J Econ Entomol. 2018; 111(1): 1–9. doi: 10.1093/jee/tox330 29281063

34. Huang YB, Chi H. Life tables of Bactrocera cucurbitae (Diptera: Tephritidae): with an invalidation of the jackknife technique. J Appl Entomol. 2013; 137(5): 327–339.

35. Stipanovic RD, López JD, Dowd MK, Puckhaber LS, Duke SE. Effect of racemic, (+)- and (−)-gossypol on survival and development of Heliothis virescens larvae. Environ Entomol. 2008; 37(5): 1081–1085. doi: 10.1603/0046-225X(2008)37[1081:EORAGO]2.0.CO;2 19036185

36. Martemyanov VV, Bakhvalov SA, Dubovskiy IM, Glupov VV, Salakhutdinov NF, Tolstikov GA. Effect of tannic acid on the development and resistance of the gypsy moth Lymantria dispar L. to viral infection. Dokl Biochem Biophys. 2006; 409(1): 219–222.

37. Ma GM, Shi XY, Kang ZJ, Gao XW. The influence of Tetranychus cinnabarinus-induced plant defense responses on Aphis gossypii development. J Integr Agr. 2018; 17(1): 164–172.

38. Barbehenn RV, Peter Constabel C. Tannins in plant-herbivore interactions. Phytochemistry. 2011; 72(13): 1551–1565. doi: 10.1016/j.phytochem.2011.01.040 21354580

39. Aerts RJ, Barry TN, McNabb WC. Polyphenols and agriculture: beneficial effects of proanthocyanidins in forages. Agr Ecosyst Environ. 1999; 72: 1–12.

40. Yousaf HK, Shan TS, Chen XW, Ma KS, Shi XY, Desneux N, et al. Impact of the secondary plant metabolite Cucurbitacin B on the demographical traits of the melon aphid, Aphis gossypii. Scientific reports. 2018;8(1):16473. doi: 10.1038/s41598-018-34821-w 30405179

41. Ma KS, Li F, Liu Y, Liang PZ, Chen XW, Gao XW. Identification of microRNAs and their response to the stress of plant allelochemicals in Aphis gossypii (Hemiptera: Aphididae). BMC Mol Biol. 2017; 18(1): 5. doi: 10.1186/s12867-017-0080-5 28202045

42. Wu KM, Guo YY. The evolution of cotton pest management practices in China. Annu Rev Entomol. 2005; 50: 31–52. doi: 10.1146/annurev.ento.50.071803.130349 15355239

43. Ma KS, Tang QL, Zhang BZ, Liang PZ, Wang BM, Gao XW. Overexpression of multiple cytochrome P450 genes associated with sulfoxaflor resistance in Aphis gossypii Glover. Pestic Biochem Physiol. 2019; 157: 204–210. doi: 10.1016/j.pestbp.2019.03.021 31153470

44. Chen XW, Tie MY, Chen AQ, Ma KS, Li F, Liang PZ, et al. Pyrethroid resistance associated with M918 L mutation and detoxifying metabolism in Aphis gossypii from Bt cotton growing regions of China. Pest Manag Sci. 2017; 73(11): 2353–2359. doi: 10.1002/ps.4622 28544677

45. Sun LJ, Zhou XG, Zhang J, Gao XW. Polymorphisms in a carboxylesterase gene between organophosphate-resistant and -susceptible Aphis gossypii (Homoptera: Aphididae). J Econ Entomol. 2005; 98(4): 1325–1332. doi: 10.1603/0022-0493-98.4.1325 16156587

46. Wang KY, Liu TX, Yu CH, Jiang XY, Yi MQ. Resistance of Aphis gossypii (Homoptera: Aphididae) to fenvalerate and imidacloprid and activities of detoxification enzymes on cotton and cucumber. J Econ Entomol. 2002; 95(2): 407–413. doi: 10.1603/0022-0493-95.2.407 12020021

47. Zheng BZ, Gao XW, Wang ZG, Liang TT, Cao BJ, Gao H. Resistant mechanism of organophosphorous and carbamate insecticides in Aphis gossypii Glov. Acta Phytophylacica Sinica. 1989; 16(2): 131–138.

48. Zheng BZ, Gao XW, Wang ZG, Cao BJ. Preliminary studies of pyrethroid resistance in melon-cotton aphid (Aphis gossypii Glov.) in Beijing suburbs and northern region of Hebei Province. Acta Phytophylacica Sinica. 1988; 15(1): 55–61.

49. Desneux N, Barta RJ, Hoelmer KA, Hopper KR, Heimpel GE. Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia. 2009; 160(2): 387–398. doi: 10.1007/s00442-009-1289-x 19219460

50. 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. 2006; 35(5): 1342–1349.

51. Shrestha RB, Parajulee MN. Potential cotton aphid, Aphis gossypii, population suppression by arthropod predators in upland cotton. Insect Sci. 2013; 20(6): 778–788. doi: 10.1111/j.1744-7917.2012.01583.x 23956125

52. Madadi H, Mohajeri Parizi E, Allahyari H, Enkegaard A. Assessment of the biological control capability of Hippodamia variegata (Col.: Coccinellidae) using functional response experiments. J Pest Sci. 2011; 84(4): 447–455.

53. Ebadollahi A, Davari M, Razmjou J, Naseri B. Separate and combined effects of Mentha piperata and Mentha pulegium essential oils and a pathogenic fungus Lecanicillium muscarium against Aphis gossypii (Hemiptera: Aphididae). J Econ Entomol. 2017; 110(3): 1025–1030. doi: 10.1093/jee/tox065 28334238

54. Wang D, Xie N, Yi S, Liu C, Jiang H, Ma Z, et al. Bioassay-guided isolation of potent aphicidal Erythrina alkaloids against Aphis gossypii from the seed of Erythrina crista-galli L. Pest Manag Sci. 2018; 74(1): 210–218. doi: 10.1002/ps.4698 28799721

55. Chaieb I, Zarrad K, Sellam R, Tayeb W, Hammouda AB, Laarif A, et al. Chemical composition and aphicidal potential of Citrus aurantium peel essential oils. Entomol Gen. 2017; 37(1): 63–75.

56. Roh HS, Kim J, Shin E-S, Lee DW, Choo HY, Park CG. Bioactivity of sandalwood oil (Santalum austrocaledonicum) and its main components against the cotton aphid, Aphis gossypii. J Pest Sci. 2014; 88(3): 621–627.

57. Boissot N, Schoeny A, Vanlerberghe-Masutti F. Vat, an amazing gene conferring resistance to aphids and viruses they carry: from molecular structure to field effects. Front Plant Sci. 2016; 7: 1420. doi: 10.3389/fpls.2016.01420 27725823

58. Garzo E, Soria C, Gomez-Guillamon ML, Fereres A. Feeding behavior of Aphis gossypii on resistant accessions of different melon genotypes (Cucumis melo). Phytoparasitica. 2002; 30(2): 129–140.

Článek vyšel v časopise


2019 Číslo 11