Experimental and Applied Acarology

, Volume 75, Issue 1, pp 41–53 | Cite as

The responses of cucumber plants subjected to different salinity or fertilizer concentrations and reproductive success of Tetranychus urticae mites on these plants

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Abstract

The plant stress hypothesis posits that a herbivore’s reproductive success increases when it feeds on stressed plants, while the plant vigor hypothesis predicts that a herbivore preferentially feeds on more vigorous plants. We examined these opposing hypotheses by growing spider mites (Tetranychus urticae) on the leaves of stressed and healthy (vigorous) cucumber plants. Host plants were grown under controlled conditions at low, moderate, and high concentrations of NaCl (to induce salinity stress), at low, moderate, and high fertilizer concentrations (to support growth), and without these additions (control). The effects of these treatments were evaluated by measuring fresh and dry plant biomass, carotenoid and chlorophyll content, antioxidant enzyme activity, and concentrations of PO43−, K+, and Na+ in plant tissues. The addition of low concentrations of fertilizer increased dry mass, protein, and carotenoid content relative to controls, suggesting a beneficial effect on plants. The highest NaCl treatment (2560 mg L−1) resulted in increased Na+ and protein content relative to control plants, as well as reduced PO43−, K+, and chlorophyll levels and reduced catalase and ascorbate peroxidase enzyme activity levels. Analysis of life table data of T. urticae mites raised on leaves from the aforementioned plant groups showed the intrinsic rate of increase (r) for mites was 0.167 day−1 in control specimens, 0.125 day−1 for mites reared on plants treated with a moderate concentration of fertilizer (10 mL L−1), and was highest (0.241 day−1) on plants grown under moderate salinity conditions (1920 mg L−1 NaCl). Reproductive success of T. urticae did not differ on plants watered with a moderate concentration of NaCl or a high concentration of fertilizer. The moderately-stressed plants formed a favorable environment for the development and reproduction of spider mites, supporting the plant stress hypothesis.

Keywords

Fertilizer NaCl Salinity Plant vigor Stress Intrinsic rate of increase 

Notes

Acknowledgements

We would like to thank three anonymous referees for their helpful suggestions and comments on a previous version of our manuscript. This work was financially supported by the office of research affairs of the University of Maragheh.

Supplementary material

10493_2018_246_MOESM1_ESM.docx (22 kb)
Supplementary material 1 (DOCX 22 kb)

References

  1. Aebi H (1984) Catalase in vitro. Method Enzymol 105:121–126CrossRefGoogle Scholar
  2. Arnon DL (1949) A copper enzyme is isolated chloroplast polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15CrossRefPubMedPubMedCentralGoogle Scholar
  3. Aucejo-Romero S, Gómez-Cadenas A, Jacas-Miret JA (2004) Effects of NaCl-stressed citrus plants on life-history parameters of Tetranychus urticae (Acari: Tetranychidae). Exp Appl Acarol 33(1–2):55–67CrossRefPubMedGoogle Scholar
  4. Azevedo Neto AD, Tarquinio Prisco J, Enéas-Filho J, de Lacerda CF, Vieira Silva J, Alves da Costa PH, Gomes-Filho E (2004) Effects of salt stress on plant growth, stomatal response and solute accumulation of different maize genotypes. Braz J Plant Physiol 16(1):31–38CrossRefGoogle Scholar
  5. Bartley GE, Scolnik PA (1995) Plant carotenoids: pigments for photoprotection, visual attraction, and human health. Plant Cell 7:1027–1038CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  7. Chance B, Maehly AC (1955) Assay of catalase and peroxidase. Method Enzymol 2:764–775CrossRefGoogle Scholar
  8. Chao WS, Gu YQ, Pautot V, Bray EA, Walling LL (1999) Leucine aminopeptidase RNAs, proteins, and activities increase in response to water deficit, salinity, and the wound signals systemin, methyl jasmonate, and abscisic acid. Plant Physiol 120:979–992CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chau A, Heinz KM (2006) Manipulating fertilization: a management tactic against Frankliniella occidentalis on potted chrysanthemum. Entomol Exp Appl 120(3):201–209CrossRefGoogle Scholar
  10. Chi H (1988) Life-table analysis incorporating both sexes and variable development rates among individuals. Environ Entomol 17(1):26–34CrossRefGoogle Scholar
  11. Chi H (2013) TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. http://140.120.197.173/Ecology/Download/TWOSEX-MSChart.rar. Accessed March 2016
  12. Cornelissen T, Wilson Fernandes G, Vasconcellos-Neto J (2008) Size does matter: variation in herbivory between and within plants and the plant vigor hypothesis. Oikos 117(8):1121–1130CrossRefGoogle Scholar
  13. Demmig-Adams B, Adams WW (2002) Antioxidants in photosynthesis and human nutrition. Science 298(5601):2149–2153CrossRefPubMedGoogle Scholar
  14. Dordas C (2009) Role of nutrients in controlling plant diseases in sustainable agriculture. In: Lichtfouse E, Navarrete M, Debaeke P, Véronique S, Alberola C (eds) Sustainable agriculture. Springer, Dordrecht, pp 443–460CrossRefGoogle Scholar
  15. Foust CM (2010) Seeking generalities in salt stress effects on herbivores: a multi-species approach. UNF Theses and Dissertations. Paper 377Google Scholar
  16. Galway KE, Duncan RP, Syrett P, Emberson RM, Sheppard AW (2004) Insect performance and host-plant stress: a review from a biological control perspective. In: Proceedings of XI international symposium on biological control of weeds, pp 394–399Google Scholar
  17. Gfeller A, Baerenfaller K, Loscos J, Chételat A, Baginsky S, Farmer EE (2011) Jasmonate controls polypeptide patterning in undamaged tissue in wounded Arabidopsis leaves. Plant Physiol 156(4):1797–1807CrossRefPubMedPubMedCentralGoogle Scholar
  18. Ghosh N, Adak MK, Ghosh PD, Gupta S, Gupta DS, Mandal C (2011) Differential responses of two rice varieties to salt stress. Plant Biotechnol Rep 5(1):89–103CrossRefGoogle Scholar
  19. Gill SS, Tajrishi M, Madan M, Tuteja N (2013) A DESD-box helicase functions in salinity stress tolerance by improving photosynthesis and antioxidant machinery in rice (Oryza sativa L. cv. PB1). Plant Mol Biol 82(1–2):1–22CrossRefPubMedGoogle Scholar
  20. Gossett DR, Millhollon EP, Lucas MC (1994) Antioxidant response to NaCl stress in salt tolerant and salt sensitive cultivars of cotton. Crop Sci 34:706–714CrossRefGoogle Scholar
  21. Huang YB, Chi H (2013) Life tables of Bactrocera cucurbitae (Diptera: Tephritidae): with an invalidation of the jackknife technique. J Appl Entomol 137:327–339CrossRefGoogle Scholar
  22. Inbar M, Doostdar H, Mayer RT (2001) Suitability of stressed and vigorous plants to various insect herbivores. Oikos 94(2):228–235CrossRefGoogle Scholar
  23. Jeppson LR, Keifer HH, Baker EW (1975) Mites injurious to economic plants. University of California Press, BerkeleyGoogle Scholar
  24. Jesiotr LJ, Suski ZW, Badowska-Czubik T (1979) Food quality influences on a spider mite population. In: Rodriguez JG (ed) Recent advances in acarology, vol I. Academic Press, New York, pp 189–196CrossRefGoogle Scholar
  25. Kachout SS, Hamza KJ, Bouraoui NK, Leclerc JC, Ouerghi Z (2013) Salt-induced changes in antioxidative enzyme activities in shoot tissues of two Artiplex varieties. Not Bot Horti Agrobo 41(1):115–121CrossRefGoogle Scholar
  26. Kapoor K, Srivastava A (2010) Assessment of salinity tolerance of Vinga mungo var. Pu-19 using ex vitro and in vitro methods. Asian. J Biotechnol 2(2):73–85Google Scholar
  27. Kawasaki S, Borchert C, Deyholos M et al (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13(4):889–905CrossRefPubMedPubMedCentralGoogle Scholar
  28. Koricheva J, Larsson S, Haukioja E (1998) Insect performance on experimentally stressed woody plants: a meta-analysis. Annu Rev Entomol 43(1):195–216CrossRefPubMedGoogle Scholar
  29. Larsson S (1989) Stressful times for the plant stress: insect performance hypothesis. Oikos 56(2):277–283CrossRefGoogle Scholar
  30. Li W, Zhao F, Fang W et al (2015) Identification of early salt stress responsive proteins in seedling roots of upland cotton (Gossypium hirsutum L.) employing iTRAQ-based proteomic technique. Front. Plant Sci 6:732Google Scholar
  31. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 148:350–382CrossRefGoogle Scholar
  32. Maleknia B, Fathipour Y, Soufbaf M (2016) How greenhouse cucumber cultivars affect population growth and two-sex life table parameters of Tetranychus urticae (Acari: Tetranychidae). Int J Acarol 42(2):70–78CrossRefGoogle Scholar
  33. Marcelis LFM, Hooijdonk JV (1999) Effect of salinity on growth, water use and nutrient use in radish (Raphanus sativus L.). Plant Soil 215(1):57–64CrossRefGoogle Scholar
  34. Margalith PZ (1999) Production of ketocarotenoids by microalgae. Appl Microbiol Biotechnol 51:431–438CrossRefPubMedGoogle Scholar
  35. Martel J (1998) Plant-mediated effects of soil salinity on a gall-inducing caterpillar Epiblema scudderiana (Lepidoptera: Tortrieidae) and the influence of feeding guild. Eur J Entomol 95:545–557Google Scholar
  36. Matsukawa T, Asai T, Kajiyama S (2017) Metabolic changes during defense responses against wound stresses in Citrus plants. In: Dr. Gill H (ed) Citrus pathology. InTech.  https://doi.org/10.5772/66159
  37. Migeon A, Nouguier E, Dorkeld F (2011) Spider Mites Web: a comprehensive database for the Tetranychidae. In: Trends in Acarology. Springer, pp 557–560Google Scholar
  38. Moore KP (1992) Determination of phosphorus in plant tissue by colorimetry. In: Plank CO (eds) Plant analysis reference procedures for the southern region of the United States. SCSB # 368, pp 27–29Google Scholar
  39. Motahari M, Kheradmand K, Roustaee AM, Talebi AA (2014) Study of cucumber plant nutrition effect by different levels of potassium on biological parameters and life table of Tetranychus urticae Koch (Acari, Tetranychidae). J Entomol Res 6(1):81–95 (in Persian) Google Scholar
  40. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–668CrossRefPubMedGoogle Scholar
  41. Nakano Y, Asada K (1987) Purification of peroxidase in spinach chloroplasts: its inactivation in ascorbate-depleted medium and re-activation by monoedhydroascorbate radical. Plant Cell Physiol 28:131–140Google Scholar
  42. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60(3):324–349CrossRefPubMedGoogle Scholar
  43. Parida AK, Das AB, Mohanty P (2004) Defense potentials to NaCl in a mangrove, Bruguiera parviflora: differential changes of isoforms of some antioxidative enzymes. J Plant Physiol 161:531–542CrossRefPubMedGoogle Scholar
  44. Petchey OL, McPhearson PT, Casey TM, Morin PJ (1999) Environmental warming alters food-web structure and ecosystem function. Nature 402:69–72CrossRefGoogle Scholar
  45. Preszler RW, Price PW (1995) A test of plant-vigor, plant-stress, and plant-genotype effects on leaf-miner oviposition and performance. Oikos 74:485–492CrossRefGoogle Scholar
  46. Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251CrossRefGoogle Scholar
  47. Ramanjulu S, Kaiser W, Dietz KJ (1999) Salt and drought stress differentially affect the accumulation of extracellular proteins in barley. Z Naturforsch C Biosci 54(5–6):337–347Google Scholar
  48. Ranganayakulu GS, Veeranagamallaiah G, Sudhakar C (2013) Effect of salt stress on osmolyte accumulation in two groundnut cultivars (Arachis hypogaea L.) with contrasting salt tolerance. Afr J Plant Sci 7(12):586–592CrossRefGoogle Scholar
  49. Rasool S, Hameed A, Azooz MM, Rehman M, Siddiqi TO, Ahmad P (2013) Salt stress: causes, types and responses of plants. In: Ahmad P, Azooz MM, Prasad MNV (eds) Ecophysiology and responses of plants under stress. Springer, New York, pp 1–24Google Scholar
  50. Robinson MF, Véry A-A, Sanders D, Mansfield TA (1997) How can stomata contribute to salt tolerance? Ann Bot 80:387–393CrossRefGoogle Scholar
  51. Rogers CE, McCarty JP (2000) Climate change and ecosystems of the Mid-Atlantic Region. Clim Res 14(3):235–244CrossRefGoogle Scholar
  52. Sarfraz RM, Dosdall LM, Keddie AB (2009) Bottom-up effects of host plant nutritional quality on Plutella xylostella (Lepidoptera: Plutellidae) and top-down effects of herbivore attack on plant compensatory ability. Eur J Entomol 106(4):583–594CrossRefGoogle Scholar
  53. Schile L, Mopper S (2006) The deleterious effects of salinity stress on leafminers and their freshwater host. Ecol Entomol 31(4):345–351CrossRefGoogle Scholar
  54. Scholz SS, Reichelt M, Mekonnen DW, Ludewig F, Mithöfer A (2015) Insect herbivory-elicited GABA accumulation in plants is a wound-induced, direct, systemic, and jasmonate-independent defense response. Front Plant Sci 6:1128CrossRefPubMedPubMedCentralGoogle Scholar
  55. Scholz SS, Malabarba J, Reichelt M, Heyer M, Ludewig F, Mithöfer A (2017) Evidence for GABA-induced systemic GABA accumulation in Arabidopsis upon wounding. Front Plant Sci 8:388CrossRefPubMedPubMedCentralGoogle Scholar
  56. Sharma BL, Pande YD (1986) A study of relationship between the population of Tetranychus neocalendonicus Andre (Acarina, Tetranychidae) and external characteristics of cucurbit leaves and their NPK contents. J Adv Zool 7(1):42–45Google Scholar
  57. Shiqing S, Shirong G, Qingmao S, Zhigang Z (2006) Physiological effects of exogenous salicylic acid on cucumber seedlings under the salt stress. Acta Hortic Sin 33(1):68–72Google Scholar
  58. Sultana N, Ikeda T, Itoh R (1999) Effect of NaCl salinity on photosynthesis and dry matter accumulation in developing rice grains. Environ Exp Bot 42(3):211–220CrossRefGoogle Scholar
  59. Suski ZW, Badowska T (1975) Effect of the host plant nutrition on the population of the two spotted spider mite, Tetranychus urticae Koch (Acarina, Tetranychidae). Ekol Pol 23:185–209Google Scholar
  60. Tiwari JK, Munshi AD, Kumar R, Pandey RN, Arora A, Bhat JS, Sureja AK (2010) Effect of salt stress on cucumber: Na+–K+ ratio, osmolyte concentration, phenols and chlorophyll content. Acta Physiol Plant 32(1):103–114CrossRefGoogle Scholar
  61. Tort N, Turkyilmaz B (2004) A physiological investigation on the mechanisms of salinity tolerance in some barley culture forms. JFS 27:1–16Google Scholar
  62. Tuteja N, Sahoo RK, Garg B, Tuteja R (2013) OsSUV3 dual helicase functions in salinity stress tolerance by maintaining photosynthesis and antioxidant machinery in rice (Oryza sativa L. cv. IR64). Plant J 76(1):115–127PubMedGoogle Scholar
  63. Walls R, Appel H, Cipollini M, Schultz J (2005) Fertility, root reserves and the cost of inducible defenses in the perennial plant Solanum carolinense. J Chem Ecol 31(10):2263–2288CrossRefPubMedGoogle Scholar
  64. White TCR (1969) An index to measure weather-induced stress of trees associated with outbreaks of psyllids in Australia. Ecology 50:905–909CrossRefGoogle Scholar
  65. White TCR (1978) The importance of a relative shortage of food in animal ecology. Oecologia 33(1):71–86CrossRefPubMedGoogle Scholar
  66. White TCR (1984) The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia 63(1):90–105CrossRefPubMedGoogle Scholar
  67. Ximénez-Embún MG, Ortego F, Castañera P (2016) Drought-stressed tomato plants trigger bottom–up effects on the invasive Tetranychus evansi. PLoS ONE 11(1):e0145275CrossRefPubMedPubMedCentralGoogle Scholar
  68. Yokoi S, Bressan RA, Hasegawa PM (2002) Salt stress tolerance of plants. JIRCAS Work Rep 23(01):25–33Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Samira Khodayari
    • 1
  • Fatemeh Abedini
    • 2
  • David Renault
    • 3
    • 4
  1. 1.Department of Plant Protection, Faculty of AgricultureUniversity of MaraghehMaraghehIran
  2. 2.Department of Horticultural Sciences, Faculty of AgricultureUniversity of MaraghehMaraghehIran
  3. 3.UMR CNRS 6553 EcoBioUniversity of Rennes 1Rennes CedexFrance
  4. 4.Institut Universitaire de FranceParis Cedex 05France

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