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The fitness of the cotton mealybug Phenacoccus solenopsis (Tinsley) is reduced after feeding on virus-infected Hibiscus rosa-sinensis

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Abstract

The cotton mealybug Phenacoccus solenopsis (Tinsley) and Cotton leaf curl Multan virus (CLCuMV), serious threats to economic crops and garden plants, have invaded southern China and widely infected Hibiscus rosa-sinensis. Whether an inter-species connection has facilitated the invasion process is unclear. In this study the interaction between P. solenopsis and H. rosa-sinensis infected with CLCuMV was investigated in the laboratory. We observed that 1st and 2nd instar nymphs of P. solenopsis preferred to feed on healthy H. rosa-sinensis leaves, whereas 3rd instar nymphs and female adults had no preference between healthy and virus-infected H. rosa-sinensis leaves. The developmental time of each P. solenopsis developmental stage increased significantly after feeding on infected H. rosa-sinensis leaves (p < 0.05). In particular, the development time for 2nd instar female and male nymphs and 3rd instar female nymphs increased by approximately twofold. The generation time of female mealybugs increased from 25.84 d on healthy H. rosa-sinensis to 32.12 d when feeding on CLCuMV-infected H. rosa-sinensis, and the survival rate decreased from 71.04 % on healthy H. rosa-sinensis to 5.80 % on infected plants. Nymph survival was most affected by feeding on infected plants. Additionally, the fecundity of female mealybugs feeding on infected H. rosa-sinensis decreased by 47.8 %. Thus, feeding on CLCuMV-infected H. rosa-sinensis significantly decreased the biological fitness and invading and colonizing abilities of P. solenopsis.

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References

  • Akhtar KP, Hussain M, Khan AI (2004) Influence of plant age, whitefly population and cultivar resistance on infection of cotton plants by cotton leaf curl virus (CLCuV) in Pakistan. Field Crop Res 86:15–21

    Article  Google Scholar 

  • Akintola A, Ande A (2008) First record of Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) on Hibiscus rosa-sinensis in Nigeria. Agric J 3:1–3

    Google Scholar 

  • Belliure B, Janssen A, Maris PC, Peters D, Sabelis MW (2005) Herbivore arthropods benefit from vectoring plant viruses. Ecol Lett 8:70–79

    Article  Google Scholar 

  • Blua MJ, Perring TM, Madore MA (1994) Plant virus-induced changes in aphid population development and temporal fluctuations in plant nutrients. J Chem Ecol 20:691–707

    Article  CAS  PubMed  Google Scholar 

  • Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trend Ecol Evol 18:119–125

    Article  Google Scholar 

  • Cory JS, Hoover K (2006) Plant-mediated effects in insect–pathogen interactions. Trend Ecol Evol 21:278–286

    Article  Google Scholar 

  • Culver JN, Padmanabhan MS (2007) Virus-induced disease: altering host physiology one interaction at a time. Ann Rev Phytopathol 45:221–243

    Article  CAS  Google Scholar 

  • DeAngelis JD, Sether DM, Rossignol PA (1993) Survival, development, and reproduction in western flower thrips (Thysanoptera: Thripidae) exposed to impatiens necrotic spot virus. Environ Entomol 22:1308–1312

    Article  Google Scholar 

  • Dutt U (2007) Mealybug infestation in Punjab: Bt. cotton falls flat. Countercurrents.org. http://www.countercurrents. org/dutt210807.htm. Accessed 24 Nov 2015

  • Eleftherianos I, Revenis C (2011) Role and importance of phenoloxidase in insect hemostasis. J Innate Immun 3:28–33

    Article  CAS  PubMed  Google Scholar 

  • Enayati AA, Ranson H, Hemingway J (2005) Insect glutathione transferases and insecticide resistance. Insect Mol Biol 14:3–8

    Article  CAS  PubMed  Google Scholar 

  • Fereres A, Lister RM, Araya JE, Foster JE (1989) Development and reproduction of the English grain aphid (Homoptera: Aphididae) on wheat cultivars infected with Barley yellow dwarf virus. Environ Entomol 18:388–393

    Article  Google Scholar 

  • Fuchs TW, Stewart JW, Minzenmayer R, Rose M (1991) 1st record of Phenacoccus solenopsis Tinsley in cultivated cotton in the United States. Southwest Entomol 16:215–221

    Google Scholar 

  • Gao W (2014) Proteomic analysis of molecular mechanism in cotton defense response to Verticillium dahlia and functional characterization of HDTF1. Dissertation, Huangzhou Agricultural University

  • Ghule SR, Barkhade UP, Moharil MP, Ugale TB (2010) Role of detoxifying enzymes in host plant resistance to cotton mealybugs (Phenococcus solenopsis Tinsley). Asian J Bio Sci 5:219–222

    Google Scholar 

  • He ZF, Dong D, Li SF, She XM, Luo FF (2010) Threat of cotton leaf curl Multan virus to China cotton production. Plant Protect 36:147–149

    CAS  Google Scholar 

  • Hodgson C, Abbas G, JalalArif M (2008) Phenacoccus solenopsis Tinsley (Sternorrhyncha: Coccoidea: Pseudococcidae), an invasive mealybug damaging cotton in Pakistan and India, with a discussion on seasonal morphological variation. Zootaxa 1913:1–35

    Google Scholar 

  • Jiu M, Zhou XP, Tong L (2007) Vector-virus mutualism accelerates population increase of an invasive whitefly. PLoS One 2:e182

    Article  PubMed  PubMed Central  Google Scholar 

  • Kirthi N, Priyadarshini CGP, Sharma P (2004) Genetic variability of begomoviruses associated with cotton leaf curl disease originating from India. Arch Virol 149:2047–2057

    CAS  PubMed  Google Scholar 

  • Lohaus G, Heldt HW, Osmond CB (2000) Infection with phloem limited abutilon mosaic virus causes localized carbohydrate accumulation in leaves of abutilon striatum: relationships to symptom development and effects on chlorophyll fluorescence quenching during photosynthetic induction. Plant Biol 2:161–167

    Article  CAS  Google Scholar 

  • Mao MJ, He ZF, Yu H, Li HP (2008) Molecular characterization of cotton leaf curl multan virus and its satellite DNA that infects Hibiscus rosa-sinensis. Chin J Virol 24:64–68

    CAS  Google Scholar 

  • Maris PC, Joosten NN, Goldbach RW, Peters P (2004) Tomato spotted wilt virus improves host suitability for its vector Frankliniella occidentalis. Phytopathology 94:706–711

    Article  CAS  PubMed  Google Scholar 

  • Mayer CJ, Vilcinskas A, Gross J (2008) Pathogen-induced release of plant allomone manipulates vector insect behavior. J Chem Ecol 34:1518–1522

    Article  CAS  PubMed  Google Scholar 

  • Moore BD, Andrew RL, Külheim C, Foley WJ (2014) Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytol 201:733–750

    Article  PubMed  Google Scholar 

  • Morse JG, Hoddle MS (2006) Invasion biology of thrips. Ann Rev Entomol 51:67–89

    Article  CAS  Google Scholar 

  • Muniz M (2000) Host suitability of two biotypes of Bemisia tabaci on some common weeds. Entomol Exp Appl 95:63–70

    Article  Google Scholar 

  • Nogia VK, Singh V, Meghwal RR (2014) Effect of cotton leaf virus infected plants on the biology of the whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae): vector-virus mutualism. Phytoparasitica 42:619–625

    Article  Google Scholar 

  • Qin JD (2003) Describing how herbivorous insects select their foodplants. Bul Biology 38:1–3

    Google Scholar 

  • Qing L, Zhou XP (2005) Advances of research on cotton leaf curl disease. Acta Phytopathologica Sin 35:193–200

    Google Scholar 

  • Quiroz C, Lister RM, Araya JE, Foster JE (1991) Effect of symptom variants derived from the NY-MAV isolate of barley yellow dwarf virus on the life cycle of the English grain aphid (Homoptera: Aphididae) and on yield components in wheat and oats. J Econ Entomol 84:1920–1925

    Article  Google Scholar 

  • Rao YY, Shen LL, Zhu SF, Yan J, Huang GS (2011) The economic losses of cotton caused by leaf curl virus in China. Plant Quar 25:12–16

    Google Scholar 

  • Shalitin D, Wolf S (2000) Cucumber mosaic virus infection affects sugar transport in melon plants. Plant Pathol 123:597–604

    CAS  Google Scholar 

  • Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32

    Article  Google Scholar 

  • Stout MJ, Thaler JS, Thomma BPHJ (2006) Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Ann Rev Entomol 51:663–689

    Article  CAS  Google Scholar 

  • Stumpf CF, Kennedy GG (2007) Effects of tomato spotted wilt virus isolates, host plants, and temperature on survival, size, and development time of Frankliniella occidentalis. Entomol Exp Appl 123:139–147

    Article  Google Scholar 

  • Sun F, Lu YY (2011) A new invasive mealybug, Phenacoccus solenopsis, could cause serious damage to cotton plants. Chin Cotton 38:19–20

    Google Scholar 

  • Tang Y, Lu YY (2013) Species identification of viruses causing hibiscus yellow leaf curl disease in Guangdong region. Guangdong Agr Sci 40:85–87

    Google Scholar 

  • van Molken T, de Caluwe H, Hordijk CA, Leon-Reyes A, Snoeren TA, van Dam NM, Stuefer JF (2012) Virus infection decreases the attractiveness of white clover plants for a non-vectoring herbivore. Oecologia 170:433–444

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang J (2012) The nutrition-related mechanisms underlying TYLCCNV-MEAM 1 whitefly-tobacco plant interactions. Dissertation, Zhejiang University

  • Wang L, Yang XZ (2010) The biological character, damage and management of solenopsis mealybug, Phenacoccus solenopsis Tinsley. J Environ Entomol 32:561–564

    Google Scholar 

  • Wang YP, Wu SA, Zhang RZ (2009) Pest risk analysis of a new invasive pest, Phenacoccus solenopsis, to China. Chin J Appl Entomol 46:101–106

    Google Scholar 

  • Wang ZH, Shi BC, Kang ZJ, Zhu L, Jin GH, Wei SJ, Gong YJ (2014) The sensitivity of different larval instars of the beet armyworm Spodoptera exigua to insecticides and correlation with enzyme activity. Chin J Appl Entomol 51:185–193

    CAS  Google Scholar 

  • Werner BJ, Mowry TM, Bosque-Perez NA, Ding H, Eigenbrode SD (2009) Changes in green peach aphid responses to potato leafroll virus-induced volatiles emitted during disease progression. Chem Ecol 38:1429–1438

    CAS  Google Scholar 

  • Wu SA, Zhang RZ (2009) A new invasive pest, Phenacoccus solenopsis, threatening seriously to cotton production. Chin J Appl Entomol 46:159–162

    Google Scholar 

  • Zhao XN (2012) Biological, physiological and biochemical changes in different varieties of cotton in response to the mealybug Phenacoccus solenopsis Tinsley (Hemiptera: Pseudoccidae) damage. Dissertation, China Jiliang University

  • Zhou AM, Lu YY, Zeng L, Xu YJ, Liang GW (2012) Does mutualism drive the invasion facilitation between two alien species? The case of Solenopsis invicta and Phenacoccus solenopsis. PLoS One 7:e41856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The National Natural Science Foundation of China (31171855) supported this work.

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    Authors and Affiliations

    1. College of Agriculture, South China Agricultural University, 483 Wushan Road, Guangzhou, 510642, People’s Republic of China

      Yuan TANG, Lei WANG & Yongyue LU

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    1. Yuan TANG
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    2. Lei WANG
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    3. Yongyue LU
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    Correspondence to Yongyue LU.

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    Handling Editor: Heikki Hokkanen.

    Yuan Tang and Lei Wang have contributed equally to this work.

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    TANG, Y., WANG, L. & LU, Y. The fitness of the cotton mealybug Phenacoccus solenopsis (Tinsley) is reduced after feeding on virus-infected Hibiscus rosa-sinensis . Arthropod-Plant Interactions 10, 455–462 (2016). https://doi.org/10.1007/s11829-016-9448-6

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