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Feeding Biology and Nutritional Physiology of Psylloidea(Insecta:Hemiptera):Implications in Host-Plant Relations


Affiliations
1 Charles Sturt University & Graham Centre for Agricultural Innovation, PO Box 833, Orange, NSW 2800, Australia
 

About 3500 species represent the Psylloidea across the world. Many Psylloidea live on a wide range of agriculturally and horticulturally important plants and some of them also act as vectors of plant pathogens. Generally they show a arrow host-plant range and feed on plant sap. Endosymbiotic bacteria are shown to be associated with some of them, enabling them to live on a nutritionally imbalanced plant diet. During feeding, the Psylloidea induce changes in plant tissues. Salivary enzymes such as pectinases enable them to mobilize primary metabolites rapidly to feeding sites from uninfested parts. Specific proteins (64 and 58 kDa) occur in the saliva of free-living Psylloidea (e.g. Aphalaridae) as well as in host-plant phloem. These insects live either freely or by constructing lerps or by inducing galls. Variations in guilds and feeding behaviour determine the nutritional ecology and physiology of the Psylloidea. Varying nutrient levels in leaves regulate populations of the gregariously feeding Psylloidea. The lerp-constructing Psylloidea utilize more of sugar-based nutrients, while the group feeding Psylloidea induce more intense changes in amino-acid, fatty-acid, and mineral levels in host plants. High C and low N ratios in leaves influence psylloid growth rates negatively. For instance, the gall-inducing Psylloidea achieve only two generations a year. High levels of the sterol (440.3 molecular weight) and ergosterol and low levels of complex lipids in young leaves of E. macrorhyncha appear to regulate the specificity of the gall-inducing species of Glycaspis (Synglycaspis) (Aphalaridae). About 100 plants are indicated as hosts of Indian Psylloidea. Curiously no lerp-forming psylloid is known in India.

Keywords

Auchenorrhyncha, Feeding Behaviour, Heteroptera, Nutritional Requirements, Primary Metabolites, Sternorrhyncha.
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  • Burckhardt, D. and Ouvrard, D., A revised classification of the jumping plant-lice, Zootaxa, 2012, 3509, 1–34.

  • Hodkinson, I. D., Life cycle variation and adaptation in jumping plant lice (Insecta: Hemiptera: Psylloidea): a global synthesis. J. Nat. Hist., 2009, 43, 65–179.

  • Balakrishna, P. and Raman, A., Cecidogenesis of leaf galls of Strychnos nux-vomica (Loganiaceae) induced by the jumping plant louse species Diaphorina truncata (Homoptera: Psylloidea: Psyllidae). Entomol. Gener., 1992, 17, 285–295.

  • Raman, A., Cecidogenesis of leaf galls on Syzygium cumini (L.) Skeels (Myrtaceae) induced by Trioza jambolanae Crawford (Homoptera: Psylloidea), J. Nat. Hist., 1991, 25, 653–663.

  • Hollis, D., Australian Psylloidea: Jumping Plantlice and Lerp Insects, The Australian Biological Resource Study, CSIRO, Canberra, 2004, p. 216.

  • Ramakrishna, T. V., List of Psyllidae recorded from India and Ceylon. Rec. Ind. Mus., 1924, 26, 621–625.

  • Mathur, R. N., Psyllidae of the Indian Subcontinent, Indian Council of Agricultural Research, New Delhi, 1975, p. 260.

  • Kandasamy, C., Taxonomy of South Indian psyllids, Rec. Zool. Surv. India, 1986, 84, 1–110.

  • Mani, M. S., Plant Galls of India, Macmillan India, New Delhi, 1973, 1st edn.

  • Mani, M. S., Plant Galls of India, Science Publishers, New Hampshire, 2000, 2nd edn.

  • Burckhardt, D., Ouvrard, D., Queiroz, D., and Percy, D., Psyllid host-plants (Hemiptera: Psylloidea): resolving a semantic problem, Fla. Entomol., 2014, 97, 242–246.

  • Hodkinson, I. D., The psyllids (Homoptera: Psylloidea) of the Austro-Oriental, Pacific, and Hawaiian zoogeographical realms: an annotated check list. J. Nat. Hist., 1983, 17, 341–377.

  • Hodkinson, I. D., The psyllids (Homoptera: Psylloidea) of the Oriental zoogeographical region: an annotated check list. J. Nat. Hist., 1986, 20, 299–357.

  • Burckhardt, D., Jumping plant lice (Homoptera: Psylloidea) of the temperate Neotropical region. Part 1. Psyllidae (Subfamilies Aphalarinae, Rhinocolinae, and Aphalaridinae). Zool. J. Linn. Soc., 1987, 89, 299–392.

  • Burckhardt, D., Jumping plant lice (Homoptera: Psylloidea) of the temperate Neotropical region. Part 2. Psyllidae (Subfamilies Diaphorininae, Acizziinae, Ciriacreminae, and Psyllinae). Zool. J. Linn. Soc., 1987, 90, 145–205.

  • Burckhardt, D., Notes on the Indo-Australian plant louse genus Cecidopsylla (Homoptera, Psylloidea) with descriptions of two new species, Phytophaga, 1991, 3, 73–86.

  • Burckhardt, D., Biology, ecology, and evolution of gall-inducing psyllids (Hemiptera: Psylloidea). In Biology, Ecology, and Evolution of Gall-inducing Arthropods (eds Raman, A., Schaefer, C. W. and Withers, T. M.), Science Publishers, Inc., Enfield, New Hampshire, 2005, pp. 143–157.

  • Singh, G., Mango shoot gall: its causal organism and control measures. In Gleanings in Entomology (eds Ramamurthy, V. V. et al.), Indian Agricultural Research Institute, New Delhi, 2003, pp. 56–77.

  • Kumar, S., Prasad, L. and Khan, H. R., Observations on the biology of tendu leaf gall forming insect Trioza obsoleta Buckton (Homoptera: Psyllidae) and a control strategy. J. Trop. Forest, 1989, 5, 304–311.

  • Negi, D. S. and Bisht, R. S., On the biology of psyllid Pauropsylla depressa Crawford (Homoptera: Psyllidae), Uttar Prad. J.. Zool., 1989, 9, 253–257.

  • Dhiman, S. C. and Singh, S., Biology of Trioza hirsuta Crawford (Homoptera: Psyllidae), a pest of Terminalia tomentosa W. & A., Ind. For., 2004, 130, 680–690.

  • Raman, A., Singh, R. N. and Maryanska-Nadachowska, A., Biology and karyology of a cecidogenous psylloid, Trioza fletcheri minor (Homoptera: Psylloidea) and morphogenesis of galls on the leaves of Terminalia tomentosa and T. arjuna (Combretaceae), Insect Matsum. (NS), 1997, 53, 117–134.

  • Raman, A., On the cecidogenesis and nutritive tissues of the leaf galls of Garuga pinnata Roxburgh (Burseraceae) induced by Phacopteron lentiginosum Buckton (Pauropsyllinae: Psyllidae: Homoptera), Phytophaga, 1987, 1, 141–159.

  • Albert, S., Padhar, A., Gandhi, D. and Nityanand, P., Morphological, anatomical and biochemical studies on the foliar galls of Alstonia scholaris (Apocynaceae), Rev. Bras. Bot., 2011, 34, 343–358.

  • Shivankar, V. J. and Rao, C. N., Psyllids and their management. Pest Manag. Hort. Ecosys., 2010, 16, 1–4.

  • Singh, G., Field resistance in mango varieties against shoot gall, Acta Horticult. (ISHS), 2000, 509, 759–764.

  • Burckhardt, D., Psylloid pests of temperate and subtropical crop and ornamental plants (Hemiptera, Psylloidea): a review. Entomol. (Trends Agric. Sci.), 1994, 2, 173–186.

  • Munyaneza, J. E., Psyllids as vectors of emerging bacterial diseases of annual crops. Sthwest. Entomol., 2010, 35, 471–477.

  • Mathur, R. N., On the biology of the Psyllidae. Ind. For. Rec., 1935, 1, 35–70.

  • Sokhi, J. and Kapil, R. N., Morphogenetic changes induced by Trioza in flowers of Terminalia arjuna – I. Androecium, Phytomorph., 1984, 34, 117–128.

  • Sokhi, J. and Kapil, R. N., Morphogenetic changes induced by Trioza in flowers of Terminalia arjuna – II. Gynoecium, Phytomorph., 1985, 35, 69–82.

  • Capinera, J. L., Green peach aphid, Myzus persicae (Sulzer) (Insecta: Hemiptera: Aphididae). In Encyclopedia of Entomology (ed. Capinera, J. L.), Springer, Dordrecht, The Netherlands, 2008, pp. 1727–1730.

  • Sharma, A., Raman, A., Taylor, G. and Fletcher, M., Nymphal development and lerp construction of Glycaspis sp. (Hemiptera: Psylloidea) on Eucalyptus sideroxylon (Myrtaceae) in central-west New South Wales, Australia, Arthr. Struct. Dev., 2013, 42, 551– 564.

  • Sharma, A., Raman, A., Taylor, G. S., Fletcher, M. J. and Nicol, H., Development, feeding and oviposition behaviour of Ctenarytaina eucalypti (Maskell) (Hemiptera: Psylloidea: Aphalaridae) on Eucalyptus globulus (Myrtaceae) in the central tablelands of New South Wales, Aust. Entomol., 2014, 54, 117–136.

  • Sharma, A., Raman, A., Taylor, G. S., Fletcher, M. J. and Nicol, H., Feeding and oviposition behaviour of a gall-inducing species of Glycaspis (Synglycaspis) (Hemiptera: Psylloidea: Aphalaridae) and development of galls on the leaves of Eucalyptus macrorhyncha (Myrtaceae) in central western New South Wales, Australia, Eur. J. Entomol., 2015, 112, 75–90.

  • Rohfritsch, O., Trâces de succion de deux Chermisidae: Chermes abietes L. et Chermes strobilobius Kalt. dans les bourgeons de Picea excelsa L., Marcellia, 1976, 39, 69–84.

  • Raman, A., Gall induction by hemipteroid insects, J. Plant Int., 2012, 7, 29–44.

  • Sopow, S. L., Shorthouse, J. D., Strong, W. and Quiring, D. T., 2003. Evidence for long-distance, chemical gall induction by an insect. Ecol. Lett., 2003, 6, 102–105.

  • Sharma, A., Khan, A. K., Subrahmanyam, S., Raman, A., Taylor, G. S. and Fletcher, M. J., Salivary proteins of plant-feeding hemipteroids – implication in phytophagy. Bull. Entomol. Res., 2013, 104, 117–136.

  • Oliveira, D. C., Isaias, R. M. S., Moreira, A. S. F. P., Magalhães, T. A. and Lemos-Filho, J. P., Is the oxidative stress caused by Aspidosperma sp. galls capable of altering leaf photosynthesis? Plant Sci., 2011, 180, 489–495.

  • Hori, K., Possible causes of diseases symptoms resulting from the phytophagous Heteroptera. In Heteroptera of Economic Importance (eds Schaefer, C. W. and Panizzi, A. R.), CRC Press, Boca Raton, 2000, pp. 11–35.

  • Miles, P. W., Aphid saliva. Biol. Rev., 1999, 74, 41–85.

  • Sharma, A., Madhavan, S., Raman, A., Taylor, G. and Fletcher, M., Salivary gland structure of Ctenarytaina eucalypti (Hemiptera: Aphalaridae) and interaction of salivary proteins with Eucalyptus globulus. Pol. J. Entomol., 2014, 84, 21–32.

  • Douglas, A. E., Phloem-sap feeding by animals: problems and solutions, J. Exp. Bot., 2006, 57, 747–754.

  • Fromont, C., Riegler, M., Cook, J. M. and Olson, J., Phylogeographic analyses of bacterial endosymbionts in fig homotomids (Hemiptera: Psylloidea) reveal codiversification of both primary and secondary endosymbionts, FEMS Microbiol. Ecol., 2016, 92, https://doi.org/10.1093/femsec/fiw205.

  • Subandiyah, S., Nikoh, N., Tsuyumu, S., Somowiyarjo, S. and Fukatsu, T., Complex endosymbiotic microbiota of the citrus psyllid Diaphorina citri (Homoptera: Psylloidea). Zool. Sci., 2000, 17, 983–989.

  • Zchori-Fein, E., Lahav, T. and Freilich, S., Variations in the identity and complexity of endosymbiont combinations in whitefly hosts, Front. Microbiol., 2014, 5, 1–8.

  • Agrios, G., Plant Pathology, Academic Press, Massachusetts, 2004, 5th edn, p. 952.

  • Mensah, R. K. and Madden, J. L., Feeding behaviour and pest status of Ctenarytaina thysanura Ferris and Klyver (Hemiptera: Psyllidae) on Boronia megastigma Nees in Tasmania. J. Aust. Entomol. Soc., 1992, 31, 71–78.

  • White, T. C. R., The nymphal stage of Cardiaspina densitexta (Homoptera, Psyllidae) on leaves of Eucalyptus fasciculosa, Aust. J. Zool., 1970, 18, 273–293.

  • Mani, T. and Raman, A., Biochemical changes in relation to growth in two leaf gall systems induced by Trioza jambolanae and Microceropsylla longispiculata (Homoptera: Psylloidea), Phytophaga, 1994, 6, 59–64.

  • Watanabe, M. et al., Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis, Plant Physiol., 2013, 162, 1290–1310.

  • Williams, M., Robertson, E. J., Leech, R. M. and Harwood, J. L., Lipid metabolism in leaves from young wheat (Triticum aestivum cv. Hereward) plants grown at two carbon dioxide levels. J. Exp. Bot., 1998, 49, 511–520.

  • Coviella, C. E., Stipanovic, R. D. and Trumble, J. T., Plant allocation to defensive compounds: interactions between elevated CO2 and nitrogen in transgenic cotton plants, J. Exp. Bot., 2002, 53, 323–331.

  • Sharma, A., Allen, J., Madhavan, S., Raman, A., Taylor, G. and Fletcher, M., How do free-living, lerp-forming, and gall-inducing Aphalaridae (Hemiptera: Psylloidea) affect the nutritional quality of Eucalyptus leaves? Ann. Entomol. Soc. Am., 2015, doi:10.1093/aesa/sav094.

  • Raman, A., Morphogenesis of insect-induced plant galls: facts and questions, Flora, 2011, 206, 517–533.

  • Schultz, J. C., Appel, H. M., Ferrieri, A. P. and Arnold, T. M., Flexible resource allocation during plant defense responses. Front.Plant Sci., 2013, 4, 324; doi:10.3389/fpls.2013.00324.

  • Crawford, S. A. and Wilkens, S., Ultrastructural aspects of damage to leaves of Eucalyptus camaldulensis by the psyllid Cardiaspina retator, Micron, 1996, 27, 359–366.

  • Moore, B. D., Wallis, I. R., Wood, J. T. and Foley, W. J., Foliar nutrition, site quality, and temperature influence foliar chemistry of tallowwood (Eucalyptus microcorys). Ecol. Monogr., 2004, 74, 553–568.

  • Schoonhoven, L. M., van Loon, J. J. A. and Dicke, M., Insect – Plant Biology, Oxford University Press, New York, 2005, p. 421.

  • Fontellas, T. M. L. and Zucoloto, F. S., Effect of sucrose ingestion on the performance of wild Anastrepha obliqua (Macquart) females (Diptera: Tephritidae), Neotrop. Entomol., 2003, 32, 209–216.

  • Sempruch, C., Michalk, A., Leszczyński, B. and Chrzanowski, G., Effect of Sitobion avenae (Fabricius, 1775) feeding on the free amino acid content within selected parts of Triticale plants, Aphids and Other Hemipterous Insects, 2011, 17, 137–144.

  • Dubey, N. K. et al., Comparative transcriptome analysis of Gossypium hirsutum L. in response to sap sucking insects: aphid and whitefly, BMC Genomics, 2013, doi:10.1186/1471-2164-14-241.

  • Behmer, S. T. and Nes, W. D., Insect sterol nutrition and physiology: a global overview. Adv. Insect. Physiol., 2003, 31, 1–72.

  • Bashan, M., The distribution in lipids classes of fatty acids biosynthesized by the black cricket Melanogryllus desertus Pall. (Orthoptera: Gryllidae). Turk. Entomol. Derg., 1998, 22, 93–99.

  • Kanobe, C., In Fatty Acid Changes in Soybean (Glycine max) Under Soybean Aphid (Aphis glycines) Infestation and their Implications on Plant Defense Against Insects, Iowa State University, Ames, 2012, p. 135.

  • Silva, A. D. A. E., Varanda, E. M. and Primavesi, A. C., Effect of the inherent variation in the mineral concentration of alfalfa cultivars on aphid populations. Bragantia, 2005, 64, 233–239.

  • Mahadeva, A. and Nagaveni, V., Evaluation of nutritional quality in spiralling whitefly (Aleurodicus dispersus Russell) infested mulberry (Morus sp.) foliage. Int. J. Environ. Sci., 2012, 3, 1065– 1071.

  • Ouvrard, D., Chalise, P. and Percy, D. M., Host-plant leaps versus host-plant shuffle: a global survey reveals contrasting patterns in an oligophagous insect group (Hemiptera, Psylloidea), Syst. Biodivers., 13, 434–454.

  • Douglas, A. E., The microbial dimension in insect nutritional ecology. Funct. Ecol., 2009, 23, 38–47.

  • Brooker, M. I. H., A new classification of the genus Eucalyptus L’Hér (Myrtaceae). Aust. Syst. Bot., 2000, 13, 79–148.

  • Woodhams, M., Steane, D. A., Jones, R. C., Nicolle, D., Moulton, V. and Holland, B. R., Novel distances for dollo data. Syst. Biol., 2013, 62, 62–77.

  • Sharma, A., Allen, J., Madhavan, S., Raman, A., Taylor, G. and Fletcher, M., Complex lipids and sterols in the leaves of three species of Eucalyptus (Myrtaceae) hosting three species of Aphalaridae (Hemiptera: Psylloidea): do they have a role in regulating host fidelity? Ann. Entomol. Soc. Am., 2016, doi:http://dx. doi.org/10.1093/aesa/saw059.

  • Behmer, S. T, Grebenok, R. J. and Douglas, A. E., Plant sterols and host plant suitability for a phloem feeding insect, Funct. Ecol., 2011, 25, 484–491.

  • Jing, X. F., Vogel, H., Grebenok, R. J., Zhu-Salzman, K. and Behmer, S. T., Dietary sterols/steroids and the generalist caterpillar Helicoverpa zea: physiology, biochemistry and midgut gene expression. Insect Biochem. Mol. Biol., 2012, 42, 835–845.

  • Kaloshian, I. and Walling, L. L., Hemipterans as plant pathogens, Ann. Rev. Phytopathol., 2005, 43, 491–521.

  • Rajadurai, S., Mani, T., Balakrishna, P. and Raman, A., On the digestive enzymes and soluble proteins of the nymphal salivary glands of Trioza jambolanae Crawford (Triozinae: Psyllidae: Homoptera), the gall maker of the leaves of Syzygium cumini (L.) Skeels (Myrtaceae), Phytophaga, 1990, 3, 47–53.

  • Brodbeck, B. V., Andersen, P. C., Oden, S. and Mizell, R. F. III, Preference-performance linkage of the xylem feeding leafhopper, Homalodisca vitripennis (Hemiptera Cicadellidae), 2007, Environ. Entomol., 36, 1512–1522.

  • Offor, E., The nutritional requirements of phytophagous insects: why do some insects feed on plants, 2010; http://dx.doi.org/ 10.2139/ssrn.1535274; accessed on 25 October 2016.

  • Laudonia, S. and Garonna, A. P., The red gum lerp psyllid, Glycaspis brimblecombei, a new exotic pest of Eucalyptus camaldulensis in Italy. B. Insectol., 2010, 63, 233–236.


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  • Feeding Biology and Nutritional Physiology of Psylloidea(Insecta:Hemiptera):Implications in Host-Plant Relations

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Authors

Anamika Sharma
Charles Sturt University & Graham Centre for Agricultural Innovation, PO Box 833, Orange, NSW 2800, Australia
Anantanarayanan Raman
Charles Sturt University & Graham Centre for Agricultural Innovation, PO Box 833, Orange, NSW 2800, Australia

Abstract


About 3500 species represent the Psylloidea across the world. Many Psylloidea live on a wide range of agriculturally and horticulturally important plants and some of them also act as vectors of plant pathogens. Generally they show a arrow host-plant range and feed on plant sap. Endosymbiotic bacteria are shown to be associated with some of them, enabling them to live on a nutritionally imbalanced plant diet. During feeding, the Psylloidea induce changes in plant tissues. Salivary enzymes such as pectinases enable them to mobilize primary metabolites rapidly to feeding sites from uninfested parts. Specific proteins (64 and 58 kDa) occur in the saliva of free-living Psylloidea (e.g. Aphalaridae) as well as in host-plant phloem. These insects live either freely or by constructing lerps or by inducing galls. Variations in guilds and feeding behaviour determine the nutritional ecology and physiology of the Psylloidea. Varying nutrient levels in leaves regulate populations of the gregariously feeding Psylloidea. The lerp-constructing Psylloidea utilize more of sugar-based nutrients, while the group feeding Psylloidea induce more intense changes in amino-acid, fatty-acid, and mineral levels in host plants. High C and low N ratios in leaves influence psylloid growth rates negatively. For instance, the gall-inducing Psylloidea achieve only two generations a year. High levels of the sterol (440.3 molecular weight) and ergosterol and low levels of complex lipids in young leaves of E. macrorhyncha appear to regulate the specificity of the gall-inducing species of Glycaspis (Synglycaspis) (Aphalaridae). About 100 plants are indicated as hosts of Indian Psylloidea. Curiously no lerp-forming psylloid is known in India.

Keywords


Auchenorrhyncha, Feeding Behaviour, Heteroptera, Nutritional Requirements, Primary Metabolites, Sternorrhyncha.

References





DOI: https://doi.org/10.18520/cs%2Fv113%2Fi08%2F1543-1552