Consequences of leaf biochemical characters for citrus leafminer, Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) along the microclimatic gradient of citrus plants


  • Muhammad Arshad University of Sargodha, Pakistan Current: Ankara University, Turkey


citrus orchard, insect-plant interaction, infestation, Phyllocnistis citrella, plant canopy


The leaf traits and microclimate in different positions of a host plant often influence the host choice and performance of herbivore insects. In the present study, we determined the relation of leaf biochemical characters with the infestation of citrus leafminer (CLM), Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) on six citrus cultivars; Meyer Lime (lemon × mandarin hybrid), Kinnow, and Feutrell’s early (Citrus mandarins), Fairchild (C. tangerines), Succari and Musambi (C. sinensis). We also hypothesized that the CLM damage increase from lower to upper canopy of the plant. Highest level of infestation was observed on the upper canopy of citrus plants followed by a middle and lower canopy in case of all citrus cultivars. The CLM damage also varied between six citrus cultivars with the highest level of 24.24% for Meyer Lime and 21.42% for Kinnow cultivars and the least affected cultivar by CLM feeding was Musambi with 09.31% infestation. Among the leaf traits, nitrogen and moisture content showed significant and positive relation with CLM infestation in all citrus cultivars. Total mineral in leaves did not show the significant (P > 0.05) relation with CLM damage in all citrus cultivars. Crude protein showed the significant relation with CLM only in case of Meyer Lime cultivar. Our finding suggests that moisture level and nitrogen content in the leaves are important factors to enhance the activity of CLM and this interaction can impact the growth and productivity of citrus plants


Bentz, J. & Townsend, A.M. (2001) Leaf element content and utilization of maple and elm as hosts by the potato leafhopper (Homoptera: Cicadellidae). Environmental Entomology 30: 533–539.

Bi, J.L., Ballmer, G.R., Hendrix, D.L., Henneberry, T.J. & Toscano, N.C. (2001) Effect of cotton nitrogen fertilization on Bemisia argentifolii populations and honeydew production. Entomologia Experimentalis et Applicata 99: 25–36.

Cárdenas, A.M. & Gallardo, P. (2012) The effect of temperature on the preimaginal development of the Jewel beetle Coraebus florentinus (Coleoptera: Buprestidae). European Journal of Entomology 109: 21–28.

Cárdenas, R.E., Valencia, R., Kraft, N.J.B., Argoti, A. & Dangles, O. (2014) Plant traits predict inter- and intraspecific variation in susceptibility to herbivory in a hyperdiverse Neotropical rain forest tree community. Journal of Ecology 102: 939–952.

Connor, E.F. & Taverner, M.P. (1997) The evolution and the adaptive significance of the leaf-mining habit. Oikos 79: 6–25.

Douglas, A.E. (2006) Phloem-sap feeding by animals: problems and solutions. Journal of Experimental Biology 57: 747–754.

Fortin, M. & Mauffette, Y. (2002) The suitability of leaves from different canopy layers for a generalist herbivore (Lepidoptera: Lasiocampidae) foraging on sugar maple. Canadian Journal of Forest Research 32: 379–389.

Fürstenberg-Hägg, J., Zagrobelny, M. & Bak, S. (2013) Plant defense against insect herbivores. International Journal of Molecular Sciences 14: 10242–10297.

Gottwald, T.R., Graham, J.H. & Schubert, T.S. (1997) An epidemiological analysis of the spread of citrus canker in urban Miami, Florida, and synergistic interaction with the Asian citrus leafminer. Fruits 52: 383–390.

Gurevitch, J., Scheiner, S.M. & Fox, G.A. (2006) The Ecology of Plants (2nd ed.) Sunderland, MA: Sinauer Associates Inc.

Hartley, S.E. & Jones, C.G. (1997) Plant chemistry and herbivory, or why is the world green? In: Plant Ecology, edited by M. Crawley, Blackwell Science, Oxford, London. Pp. 284–324.

Heppner, J.B. (1993) Citrus leafminer, Phyllocnistis citrella, in Florida. Tropical Lepidoptera Research 4: 49–64.

Huberty, A.F. & Denno, R.F. (2006) Consequences of nitrogen and phosphorus limitation for the performance of two plant hoppers with divergent life-history strategies. Oecologia 149: 444–455.

Jesus, Jr.W.C., Belasque, Jr.J., Amorim, L., Christiano, R.S.C., Parra, J.R.P., et al. (2006) Injuries caused by citrus leafminer (Phyllocnistis citrella) exacerbate citrus canker (Xanthomonas axonopodispv. citri) infections. Fitopatologia Brasileira 31: 277–283.

Joern, A., Provin, T. & Behmer, S.T. (2012) Not just the usual suspects: insect herbivore populations and communities are associated with multiple plant nutrients. Ecology 93: 1002–1015.

Larbat, R., Paris, C., Le Bot, J. & Adamowicz, S. (2014) Phenolic characterization and variability in leaves, stems and roots of Micro-Tom and patio tomatoes, in response to nitrogen limitation. Plant Science 224: 62–73.

Leather, S.R. (2018) Factors affecting fecundity, fertility, oviposition, and larviposition in insects, In: Insect Reproduction, CRC Pres, Boca Raton. Pp. 143–174.

Linhart, Y.B., Mooney, K.A. Snyder, M.A. & Swoboda-Colberg, N. (2001) Phloem chemistry: effects of genotype and environment and implications for nutritional ecology. International Journal of Plant Science 162: 1009–1016.

Loader, C. & Damman, H. (1991) Nitrogen content of food plants and vulnerability of Pierisrapae to natural enemies. Ecology 72: 1586–1590.

Loaiza, V., Jonas, J.L. & Joern, A. (2011) Grasshoppers (Orthoptera: Acrididae) select vegetation patches in local-scale responses to foliar nitrogen but not phosphorus in native grassland. Insect Science 18: 533–540.

Mafi, S.A. & Ohbayashi, N. (2004) Seasonal prevalence of the citrus leaf miner Phyllocnistis citrella Stainton and its parasitiods in controlled and uncontrolled citrus groves in Ehime Prefecture, Japan. Applied Entomology and Zoology 39: 597–601.

Mahmood, R., Rehman, A. & Ahmad, M. (2014) Prospects of biological control of citrus insect pests in Pakistan. Journal of Agricultural Research 52: 229–244.

Maoela, M.A., Roets, F., Shayne, J.M. & Esler, K.J. (2016) Restoration of invaded cape floristic region riparian systems leads to a recovery in foliage-active arthropod alpha- and beta-diversity. Journal of Insect Conservation 20: 85–97.

Mustafa, I., Aslam, M., Arshad, M., Muhammad, S., Ullah, M.I., et al. (2014) Association of citrus leaf miner Phyllocnistis citrella (Lepidoptera: Gracillariidae: Phyllocnistinae) with leaf biochemical factors (Ca+ 2 K+ and Mg+ 2) in Kinnow leaves of district Sargodha Punjab Pakistan. Pakistan Journal of Zoology 46: 953–958.

Prestidge, R.A. (1982) Instar duration, adult consumption, oviposition and nitrogen utilization efficiencies of leafhoppers feeding on different quality food (Auchenorrhyncha: Homoptera). Ecological Entomology 7: 91–101.

Ranganna, S. (1977) Manual of analysis of fruit and vegetable products. Center for Food Technology Research Institute Mysore Tata McGraw Hill Publ. Co. Ltd., New Delhi.

Richardson, M.L., Westbrook, C.J., Hall, D.G., Stover, E., Duan, Y.P., et al. (2011) Abundance of citrus leafminer larvae on citrus and citrus-related germplasm. HortScience 46: 1260–1264.

Roslin, T., Gripenberg, S., Salminen, J.P., Karonen, M., O'hara, R.B., et al. (2006) Seeing the trees for the leaves–oaks as mosaics for a host‐specific moth. Oikos 113: 106–120.

Rowe, W.J. & Potter, D.A. (1996) Vertical stratification of feeding by Japanese beetles within linden tree canopies: selective foraging or height per se? Oecologia 108: 459–466.

Sétamou, M., Simpson, C.R., Alabi, O.J., Nelson, S.D., Telagamsetty, S., et al. (2016) Quality matters: Influences of citrus flush physicochemical characteristics on population dynamics of the Asian citrus psyllid (Hemiptera: Liviidae). PlosOne 11: e0168997. http://doi:10.1371/journal.pone.0168997

Shobana, K., Murugan, K. & Kumar, A.N. (2010) Influence of host plants on feeding, growth and reproduction of Papilio polytes (The common mormon). Journal of Insect Physiology 56: 1065–1070.

Smith, C.M. & Boyko, E.V. (2007) The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomologia Experimentalis et Applicata 122: 1–16.

Stiegel, S., Entling, M.H. & Mantilla-Contreras, J. (2017) Reading the Leaves’ Palm: Leaf traits and herbivory along the microclimatic gradient of forest layers. PlosOne 12: e0169741

Trier, T.M. & Mattson, W.J. (1997) Needle mining by the spruce budworm provides sustenance in the midst of privation. Oikos 79: 241–246.

Trigo, J.R., Pareja, M. & Massuda, K.F. (2012) O papel das substâncias químicasnas interações entre plantas e insetos herbívoros, In Ecologia das Interações Planta-animais: umaabordagemecológico-evolutiva, edited by K. Del-Claro, and H. M. Torezan-Silingardi, 69–88. Technical Books, Rio de Janeiro.

Tsai, J.H. & Wang, J.J. (2001) Effects of host plants on biology and life table parameters of Aphis spiraecola (Homoptera :Aphididae). Environmental Entomology 30: 44–50.

Winkleman, G.R., Amin, R., Rice, W.A. & Tahir, M.B. (1986) Methods: Manual Soils Laboratory,Barani Agriculture Research and Development Project, 30–33. PARC, Islamabad (Pakistan).

Zarasvanda, A.A., Allahyarib, H. & Fattah-Hosseini, S. (2013) Effect of nitrogen fertilization on biology, life table parameters and population abundance of greenbug; Schizaphis graminum (Rondani) (Hemiptera: Aphididae). Archives of Phytopathology and Plant Protection 46: 882–889.

Zia, K., Ashfaq, M., Arif, M.J. & Sahi, S.T. (2011) Effect of physico-morphic characters on population of whitefly Bemisia tabaci in transgenic cotton. Pakistan Journal of Agricultural Sciences, 48: 63–69.