Nitrogen utilization pattern and degradation capability of some plant secondary metabolites by Agelastica alni L. (Coleoptera: Chrysomelidae)

An oligophagous leaf beetle, Agelastica alni (L., 1758) (Coleoptera: Chrysomelidae), often occurs in outbreak densities and utilizes both alders and willows in Europe. It was reported on alder and hazel in Turkey and its outbreaks on alder occur almost every year in the middle and eastern Black Sea regions of the country where hazel plantations cover huge areas. Nitrogen utilization, and degradation of some plant secondary metabolites by A. alni larvae fed with leaves of alder (Alnus glutinosa (L.) Gaertn. ssp. glutinosa), babylon willow (Salix babylonica L.) and hazel (Corylus avellana L.) with varying nutritional status were investigated. Larvae of this species were fed leaves of these plants that had been fertilized (NPK) and not been fertilized. Larval nitrogen utilization was determined to calculate the nitrogen utilization efficiency (NUE). The effects of some secondary metabolites of leaves of the plants on the digestion efficiency of A. alni larvae were tested. It was determined that A. alni larvae balanced its nitrogen utilization to some degree, despite the increase of nitrogen content of the leaves. Although the nitrogen content changed from 2,97% to 4,33 in hazel, from 2,47 % to 3,68 in babylon willow, from 4,27 % to 5,34 in young alder, from 4,04 % to 4,66 in older alder, the efficiency of nitrogen utilization of larvae changed from 16,54% to 12,77, from 11,92 % to 13,86, 22,72 % to 24,53, and 21,09 % to 23,71, respectively. In addition, the correlation between the changed N content of the treated leaves and the nitrogen utilization of the larvae that fed on them was negative (except from the larvae fed on unfertilized leaves of C. avellana) in all plants and treatments. The statistical analysis indicated that the approximate digestibility (AD) of the larvae was not affected by these secondary compounds (r2< 0.7, P < 0.05). On the other hand, the degradation ratio of proanthocyanidin (condensed tannin) and total phenolics by A. alni larvae was determined as 33- 81%. These results lead to the interpretation that metabolites had no measurable effects on A. alni larvae, or alternatively, the larvae utilized regulatory mechanisms to overcome the undesirable effects of these compounds. This study also indicated that larvae of A. alni have developed nitrogen homeostasis, which may involves a decrease of predation risk.

Kaynakça

Barone, J. A., 1998, Host-specificity of folivorous insects in a moist tropical forest. Journal of Animal Ecology, 67: 400–409.

Bate-Smith, E. C., 1975, Phytochemistry of proanthocyanidins. Phytochemistry, 14: 1107-1113.

Bate-Smith, E. C., 1977, Astringent tannins of Acer species, Phytochemistry, 16: 2331-2336.

Baur, R., Rank, N. E., 1996, Influence of quality and natural enemies on the life history of the alder leaf beetles Agelastica alni and Linaeidae aenea. In: Jolivet P.H.A., Cox, M. (Eds.). Chrysomelidae Biology. Vol. 2: Ecological Studies. SPB Academic Publishing, Amsterdam, 173-194.

Bernays, E. A., Chamberlain, D. J., Woodhead, S., 1983, Phenols as nutrient for a phytophagous insect Anacridium melanorhodon. Journal of Insect Physiology, 29: 535-539.

Bernays, E. A, Graham M., 1988, On the evolution of host specificity in phytophagous arthropods. Ecology, 69: 886-892.

Bernays, E. A., Chapman, R. F., 1994, Host-Plant Selection by Phytophagous Insects. Chapman & Hall, New York.

Bilgener, M., 1988, Chemical component of howler monkeys (Aloutta papillata) food choise and kinetics of tannin binding with natural polymers. PhD Dissertation, Boston University.

Çanakçıoğlu, H., Mol, T., 1998, Orman Entomolojisi -Zararlı ve Yararlı Böcekler. İ. Ü. Orman Fakültesi Yayınları, No. 451, İstanbul, 541.

Fox, L. R., Macauley, B. J., 1977, Insect grazing on Eucalyptus in response to variation in leaf tannins and nitrogen. Oecologia (Berlin), 29: 145-162.

Gross, J., Hilker, M., 1994/1995, Chemoecological studies of the exocrine glandular larval secretions of two chrysomelid species (Coleoptera): Phaedon cochleariae and Chrysomela lapponica. Chemoecology, 5/6, 3/4:185-189.

Harborne, J. B., 1977, Introduction to Ecological Biochemistry. Academic Press. London. 243 pp.

Harborne, J. B., 1994, Phenolics in natural products. Their chemistry and biological significance. In: Mann, J., Davidson, R. S.,. Hobbs, J. B., Banthorpe, D. V., Harborne J. B., Longman, Harlow, 362-388.

Ikonen, A., Tahvanainen, J., Roininen, H., 2001, Cholorogenic acid as an antiherbivore defence of willows aganist leaf beetles. Entomolia Experimentalis et Applicata, 99: 47-54.

Jaenike, J., 1990, Host specialization in phytophagous insects. Annual Review of Ecological Systems, 21: 243-273.

Kagata, H., Ohgushi, T., 2006, Nitrogen homeostasis in a willow leaf beetle, Plagiodera versicolora, is independent of host plant quality. Entomologia Experimentalis et Applicata, 118: 105-110.

Kelly, M. T., Curry, J. P., 1991, The influence of phenolic compounds on the suitability of three Salix species as hosts fort he willow beetle Phratora vulgatissima. Entomologia Experimentalis et Applicata, 61: 25-32.

Koch, K., 1992, Die Kafer Mitteleuropas. Ökologie, Band 3E, Goecke & Evers, Krefeld. 389 pp.

Kolehmainen, J., Roininen, H., Julkunen-Tiitto, R., Tahvananien, J., 1994, Importance of phenolic glucosides in host selection of shoot galling sawfly, Euura amerinae, on Salix pentandra. Journal of Chemical Ecology, 20: 2455-2466.

Kraft, S. K., Denno R. F., 1982, Feeding responses of adapted and nonadapted insects to the defensive properties of Baccharis halimfolia. Oecologia, 52: 156-163.

Kreslavsky, A. G., Mikheev, A. V., Solomatin, V. M., Gritzenko, V. V., 1981, Genetic exchange and isolating mechanisms in sympatric races of Lochmaea capreae (Coleoptera, Chrysomelidae). Zoolicheskii Zhurnal, 60: 62-68.

Lee, K. P., Behmer, S. T., Simpson, S., Raubenheimer, D., 2002, A geometric analysis of nutrient regulation in the generalist caterpillar Spodoptera littoralis (Boisduval). Journal of Insect Physiology, 48, 655-665.

Lee, K. P., Raubenheimer, D., Simpson, S. J., 2004, The effects of nutritional imbalance on compensatory feeding for cellulose-mediated dietary dilution in a generalist caterpillar. Physiological Entomology, 29: 108-117.

Lempa, K., Agrawal, A. A,, Salminen, J. P,, Turunen, T., Ossipov, V., Ossipova, S., Haukioja, E., Pihlaja, K., 2004, Rapid herbivore changes in mountain birch phenolics and nutritive compounds and their effects on performance of the major defoliator Epirrita autumnata. Journal of Chemical Ecology, 30: 303-321.

Lindroth, R. L,, Scriber, J. M., Hsia, M. T. S., 1988, Chemical ecology of the tiger swallowtail: Mediation of host use by phenolic glycosides. Ecology, 69: 814-822.

Loomis, W. D., 1974, Overcoming problems of phonemics and quinines in the isolation of plant enzymes and organelles. Methods in Enzymology, 31: 528-544.

Matsuda, K., Matsuo, H., 1985, A flavonoid, luteolin-7-glucoside, as well as salicin and populin, stimulating the feeding of leaf beetles attacking Salicaceous plants. Applied Entomology and Zoology, 20: 305-313.

Matsudo, K., Senbo, S., 1986, Chlorogenic acid as a feeding deterrent for the Salicaceae-feeding leaf beetle, Lochmaeae capreae cribrata (Coleoptera: Chrysomelidae) and other species of leaf beetles. Applied Entomology and Zoology, 21: 411-416.

Mattson, W. J. Jr., 1980, Herbivory in relation to plant nitrogen content. Annual Review of Ecology and Systematics, 11: 119-161.

Mole, S., Waterman, P. G., 1987, Tannic acid and proteolytic enzyme inhibition or substrate deprivation. Phtyochemistry, 26: 99-102.

Morrison, I. M., 1972, A semi-micro method for the determination of lignin and its use in predicting digestibility of forage crops. Journal of the Science of Food and Agriculture, 23: 455-463.

Ohmart, C. P., Stewart, L. G., Thomas, J. R., 1985, Effects of food quality, particularly nitrogen concentrations, of Eucalyptus blakelyi foliage on the growth of Paropsis atomaria larvae (Coleoptera: Chrysomelidae). Oecologia, 65: 543-549.

Orians, C. M., Huang, C. H., Wild, A., Dorfman, K. A, Zee, P., Dao, M. T. T., Fritz, R. S., 1997, Willow hybridization differentially affects preferences and performance of herbivorous beetles. Entomologia Experimentalis et Applicata, 83: 285-294.

Price, P. W., Bouton, C. E., Gross, P., Mc. Pheron, B. A., Thompson, J. N., Weis, A. E., 1980, Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecological Systems, 11: 41-65.

Rank, N. E., 1992, Host plant preference based on salicylate chemistry in willow leaf beetle (Chrysomela aeneicollis). Oecologia, 90: 95-101.

Roininen, H., Price, P. W., Julkunen-Tiitto, R., Tahvanainen, J., Ikonen, A., 1999, Oviposition stimulant for a gall-inducing sawfly, Euura lasiolepis, on willow is a phenolic glucoside, Journal of Chemical Ecology. 25: 943-953.

Scriber, J. M., 1977, Limiting effects of low leaf-water content on the nitrogen utilization, energy budget, and larval growth of Hyalophora cecropia (Lepidoptera: Saturniidae). Oecologia, 28: 269-287.

Scriber, J. M., Slansky, F. Jr,. 1981, The nutritional ecology of immature insects. Annual. Review of Entomology, 26: 183-211.

Scriber, J. M., 1984, Larval food plant utilization by the world Papilionidae (Lepidoptera): Latitudinal gradients reappraised. Tokurana (Acta Rhopalocerologica), 6-7: 1-16.

Simpson, S. J., Raubenheimer, D., 2001, The geometric analysis of nutrient-allelochemical interactions: a case study using locusts. Ecology, 82: 422-439.

Slansky, F. Jr.,1993, Nutritional ecology: the fundamental quest for nutrients. In: Stamp, N.E., Casey, T.M. (eds.). Caterpillars: Ecological and Evolutionary Constraints on Foraging. Chapman and Hall, New York, 29-91.

Slansky, F., Feeny, P., 1977, Stabilization of the rate of nitrogen accumulation by larvae of the cabbage butterfly on wild and cultivated food plants. Ecological Monographs, 47: 207-228.

Slansky, F. Jr., Scriber J. M., 1985, Food consumption and utilization. In: Kerkut, G.A., Gilbert, L.I. (Eds.). Comprehensive Insect Physiology, Biochemistry and Pharmacology. Vol. 4, Pergamon, Oxford, 87-163.

Slansky, F. Jr., Wheeler, G. S., 1989, Compensatory increases in food consumption and utilization efficiencies by velvetbean caterpillars mitigate impact of diluted diets on growth. Entomologia Experimentalis et Applicata, 51(2): 175-187.

Smiley, J., 1978, Plant chemistry and the evolution of host specificity: New evidence from Heliconius and Passiflora. Science, 201: 745-747.

Soetens, Ph., Pasteels, J. M., 1994, Synergistic effect of secondary compounds and nutrients in the host plant choice of a salicaceous-feeding leaf beetle: Phratora vitellinae (Coleoptera: Chrysomelidae). Mededelingen -Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen Universiteit Gent. 59/2b: 685-689.

Swain, T., Hillis, W. E., 1959, The phenolic constituents of Prums domestica, Journal of the Science of Food and Agriculture, 10: 63-68.

Symons, F. B., Beccaloni, G. W., 1999, Phylogenetic indices for measuring the diet breadths of phytophagous insects. Oecologia, 119: 427–434.

Tabashnik, B. E., 1982, Responses of pest and non-pest Colias butterfly larvae to intraspecific variation in leaf nitrogen and water content. Oecologia, 55: 389-394.

Takechi, M., Tanaka, Y., 1987, Binding of 1,2,3,4,6-pentagalloyl glucoseto proteins, lipids, lipids, nucleic acids and sugars. Phytochemistry, 26: 94-97.

Tischler, W., 1977, Kontinuität, Des Biosystems Erle (Alnus) Erlenblattkäfer (Agelastica alni). Zeitschfirt fuer Angewandte Zoologie, 64: 69 -92.

Waldbauer, G. P., 1968, The Consumption and Utilization of Food by Insect. Advances in Insect Physiology, 5: 229-289.

Waterman, P. G., Mole, S., 1994, Analysis of Plant Phenolic Metabolites. Blackwell Scientific Publications, Oxford. viii, 238 p.

Wheeler, G. S., Halpern, M. D., 1999, Compensatory responses of Samea multiplicalis larvae when fed leaves of different fertilization levels of the aquatic weed Pistia stratiotes. Entomologia Experimentalis et Applicata, 92: 205–216.

White, T. C. R., 1993, Nitrogen and the Abundance of Animals. The Inadequate Environment. Springer- Verlag, Berlin. 425 pp.

Zamora, R., Hódar, J. A., Gómez, J. M., 1999, Plant-herbivore interaction: beyond a binary vision. In: Pugnaire, F. I., Valladares, F. (Eds.). Handbook of Functional Plant Ecology Marcel Dekker Inc., New York, 677-718.

Kaynak Göster