Efects of Usnic, Barbatic and Fumarprotocetraric acids on Survival of Nasutitermes corniger (Isoptera: Termitidae: Nasutitermitinae)
DOI:
https://doi.org/10.13102/sociobiology.v65i1.1840Keywords:
Cladoniaceae, lichen substances, arboreal termite, termiticidal activityAbstract
Lichens (Algal-Fungal association) synthesize unique chemical substances with different biological activities. Three pure lichen compounds were assayed to evaluate their potential insecticidal activity against the termite Nasutitermes corniger on Petri dishes. Usnic, fumarprotocetraric and barbatic acids were isolated and purified from the lichens Cladonia substellata, C. verticillaris and Cladia aggregata, respectively, using thin-layer and high-performance liquid chromatography for attesting their purity. Nuclear proton magnetic resonance and infrared spectrophotometry was used for their chemical characterization. After exposure, mortality of termites (workers and soldiers) was determined during 11 days period. The termiticidal effect was influenced by the exposure time and the type of member colony. The results showed that lichen substances, tested at 5, 7 and 10 mg mL-1, have a termiticidal activity (~100%) on worker termites after 8th days of treatment, in comparison with controls. However, no significant effect on soldiers was found. These findings indicate that usnic, fumarprotocetraric and barbatic acids are potential compounds for use in the control of this urban pest.Downloads
References
Ahti, T., Stenroos, S., Filho, L.X. (1993). The lichen family Cladoniaceae in Paraiba, Pernambuco and Sergipe, Northeast Brazil. Tropical Bryology 7: 55-70. doi: http://dx.doi.org/10.11646/bde.7.1.6
Asahina, Y. & Shibata, S. (1954). Chemistry of lichen substances. Tokyo: Japan Society for the Promotion of Science.
Asplund, J., Solhaug, K.A., Gauslaa, Y. (2009). Fungal depsidones – an inducible or constitutive defense against herbivores in the lichen Lobaria pulmonaria? Basic Applied Ecolology 10: 273–278. doi: 10.1016/j.baae.2008.04.003
Balaji, P., Malarvannan, S.E., Hariharan, G.N. (2007). Efficacy of Rocella montagnei extracts on Helicoverpa armigera. Journal of Entomology 4: 248-252. doi: 10.3923/je.2007.248.252
Breznak, J.A. (1982). Intestinal microbiota of termites and other xylophagous insects. Annual Review of Microbiology 36: 323–343. doi: 10.1146/annurev.mi.36.100182.001543
Breznak, J.A. & Brune, A. (1994). Role of microorganisms in the digestion of lignocellulose by termites. Annual Review of Entomology 39: 453–487. doi: 10.1146/annurev.en.39.010194.002321
Cetin, H., Tufan-Cetin, O., Turk, A.O., Tay, T., Candan, M., Yanikoglu, A., Sumbul, H. (2008). Insecticidal activity of major lichen compounds (-) – and (+) -usnic acid, against the larvae of house mosquito, Culex pipiens L. Parasitology Research 102: 1277-1279. doi: 10.1007/s00436-008-0905-8.
Culberson, C.F.J. (1972). Improved conditions and new data the identification of lichen products by a standardized thin layer chromatographic method. Journal of Chromatography 72: 133-135.
Díaz, E.M., Sánchez-Elordi, E., Santiago, R., Vicente, C., Legaz, M.E. (2016). Algal-Fungal Mutualism: Cell Recognition and Maintenance of the Symbiotic Status of Lichens. Journal of Veterinary Medicine and Research 3: 1052-1057.
Eisenreich, W., Knispe, L.N., Beck, A. (2011). Advanced methods for the study of the chemistry and the metabolism of lichens. Phytochemistry Reviews 10: 445–456.
Emmerich, R., Giez, I., Lange, O.L., Proksch, P. (1993). Toxicity and antifeedant activity of lichen compounds against the polyphagous herbivorous insect Spodoptera littoralis. Phytochemical 33:1389-1394. doi: https://doi.org/10.1016/0031-9422(93)85097-B
Emsen, B., Yildirim, E., Aslan, A. (2015). Insecticidal Activities of Extracts of Three Lichen Species on Sitophilus granarius (L.) (Coleoptera: Curculionidae). Plant Protection Sciences 51: 155–161. doi: 10.17221/101/2014-PPS
Giez, I., Lange, O.L., Proksch, P. (1994). Growth retarding activity of lichen substances against the polyphagous herbivorous insect Spodoptera littoralis. Biochemical Systematics and Ecology 22: 113-120. doi: 10.1016/0305-1978(94)90001-9
Gudjnsdottir, G.A. & Ingolfsdottir, K. (1997). Quantitative determination of protolichesterinic- and fumarprotocetraric acids in Cetraria islandica by highperformance liquid chromatography. Journal of Chromatography A 757: 303-306. doi: 10.1016/S0021-9673(96)00670-X
Howell, G.M.E., Newton, E.M., Williams-Wynn, D.D. (2003). Molecular structural studies of lichen substances II: atranorin, gyrophoric acid, fumarprotocetraric acid, acid rhizocarpic, calycin, pulvinic dilactone and usnic acid. Journal of Molecular Structure 651: 27-37. doi: 10.1016/S0022-2860(02)00626-9
Ivanova, D. & Invanov, D. (2009). Ethnobotanical use of lichens: lichens for food review. Scripta Scientifica Medica 41: 11-16. doi: http://dx.doi.org/10.14748/ssm.v41i1.456.
Kang, H.Y., Matsushima, N., Sameshima, K., Takamura, N., 1990. Termite resistance tests of hardwoods of Kochi growth. The strong termiticidal activity of kagonoki (Litsea coreana Léveillé). Mokuzai Gakkaishi= Journal of the Japan Wood Research Society 36: 78-84.
Korb, J. (2007). Termites. Current Biology 17: 995–999. doi: http://dx.doi.org/10.1016/j.cub.2007.10.033
Lawrey, J.D. (1980). Correlations between lichen secondary chemistry and grazing activity by Pallifera varia. Bryologist 23: 128-134.
Lawrey, J.D. (1987). Nutritional ecology of lichen/moss arthropods. In: F.J.R. Slansky & J.G. Rodriguez (Eds.), Nutritional ecology insects, mites, spiders and related invertebrates. New York: John Wiley and Sons.
Legaz, M.E. & Vicente C. (1983). Endogenous inactivators of arginase, arginine decarboxylase and agmatine amidinohydrolase in Evernia prusnastri thallus. Plant Physiology 71: 300-302.
Lucarini, R., Tozatti, M.G, Salloum, A.O, Crotti, A.E.M, Silva, M.L.A, Gimenez, V.M.M, Groppo, M, Januário, A.H, Martins, C.H.G, Cunha, W.R. (2012). Antimycobacterial activity of Usnea steineri and its major constituent (+)-usnic acid. African Journal of Biotechnology 11: 4636-4639. doi: 10.5897/AJB11.3551
Martins, M.C.B., Lima, M.J.G., Silva, F.P., Azevedo-Ximenes, E., Silva, N.H., Pereira, E.C. (2010). Cladia aggregata (lichen) from Brazilian Northeast: Chemical characterization and antimicrobial activity. Brazilian Archives of Biology and Tecnology 53: 115–122. doi: http://dx.doi.org/10.1590/S1516-89132010000100015
Milano, S.E. & Fontes, L. R. (2002). Termite pests and their control in urban Brazil. Sociobiology 40: 163–177.
Nimis, P.L. & Skert, N. (2006). Lichen and selective grazing by the coleopteran Lasioderma serricorne. Environmental and Experimental Botany 55: 175-182. doi: 10.1016/j.envexpbot.2004.10.011
Neeraj, V. & Behera, B.C. (2011). Bactericidal activity of some lichen secondary compounds of Cladonia ochrochlora, Parmotrema nilghrrensis, Parmotrema sanctiangelii. International Journal of Drug development and Research 3: 222-232.
Odabasoglu, F., Cakir, A., Suleyman, H., Aslan, A., Bayir, Y., Halici, M., Kazaz, C. (2006). Gastroprotective and antioxidant effects of usnic acid on indomethacin-indiced gastric ulcer in rats. Journal of Ethnopharmacology 103: 59-65. doi: 10.1016/j.jep.2005.06.043
de Paz, G., Raggio, J., Gómez-Serranillos, M.P., Palomino, O.M, González-Burgos, E., Carretero, M.E., Crespo, A. (2010). HPLC isolation of antioxidant constituents from Xanthoparmelia spp. Journal of Pharmaceutical and Biomedical Analysis 53: 165–171. doi: 10.1016/j.jpba.2010.04.013
Pejin, B., Iodice, C., Bogdanovic, G., Kojić, V., Tešević, V. (2013). Stictic acid inhibits cell growth of human colon adenocarcinoma HT-29 cells. Arabian Journal of Chemistry 10:1240–1242. https://doi.org/10.1016/j.arabjc.2013.03.003
Pöykkö, H., Baĉkor, M., Bencúrová, E., Molcanová, V., Hyvärinen, M. (2010). Host use of a specialist lichen-feeder: dealing with lichen secondary metabolites. Oecologia 164: 423-430. doi: 10.1007/s00442-010-1682-5
Reutimann, P. & Scheidegger, C. (1987). Importance of lichen secondary products in food choice of two oribatid mites (acari) in an alpine meadow ecosystem. Journal of Chemical Ecology 13: 363-369. doi: 10.1007/BF01025896
Rundel, P.W. (1978). The ecological role of secondary lichen substances. Biochemical Systematics and Ecology 6: 157-170. doi: 10.1016/0305-1978(78)90002-9
Sahip, K., Kularate, S., Kumar, S., Karunarate, V. (2008). Effect of (+)-usnic acid on the shot-hole
borer (Xyleborus fornicatus Eichh.) of tea. Journal of the National Science Foundation of Sri Lanka 36: 335-336. doi:10.4038/jnsfsr.v36i4.274
Santana, A.L.B.D., Maranhão, C.A., Santos, J.C., Cunha, F.M., Conceição, G.M., Bieber, L.W., Nascimento, M.S. (2010). Antitermitic activity of extractives from three Brazilian hardwoods against Nasutitermes corniger. International Biode-terioration and Biodegradation 64: 7-12. doi: 10.1016/j.ibiod.2009.07.009
Scheffrahn, R.H., Krecek, J., Szalanski, A.L., Austin, J.W. (2005). Synonomy of neotropical arboreal termites Nasutitermes corniger and N. costalis (Isoptera: Termitidae: Nasutitermitinae), with evidence from morphology, genetics, and biogeography. Annals of the Entomological Society of America 98: 273-281. doi: 0013- 8746/05/0273-0281804.00/0
Silva, M.D.C., Sá, R.A., Napoleão, T.H., Gomes, F.S., Santos, N.D.L., Albuquerque, A.C., Xavier, H.S., Paiva, P.M.G., Correia, M.T.S., Coelho, L.C.B.B. (2009). Purified Cladonia verticillaris lichen lectin: Insecticidal activity on Nasutitermes corniger (Isoptera: Termitidae). International Biodeterioration and Biodegradation 63: 334-340. doi: 10.1016/j.ibiod.2008.11.002
Sipman, H.J.M. & Aptroot, A. (2001). Where are the missing lichens? Mycological Research 105: 1433-1439. doi: https://doi.org/10.1017/S0953756201004932
Solhaug, K.A., Lind, M., Nybakken, L., Gauslaa, Y. (2009). Possible functional roles of cortical depsides and medullary depsidonas in the foliose lichen Hypogymnia phydodes. Flora 204: 40-48. doi: 10.1016/j.flora.2007.12.002
Verma, M., Sharma, S., Prasad, R. (2009). Biological Alternatives for termite control: a review. International Biodeterioration and Biodegradation 63: 959-972. doi: 10.1016/j.ibiod.2009.05.009
Yamaoka, I. (1996). Symbiosis in termites. Diversity in time and space. New York: Plenum Press.
Yildirim E., Emsen, B., Aslan, A., Bulak, Y., Ercisli, S. (2012). Insecticidal activity of lichens against the maize weevil, Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae). Egyptian Journal of Biological Pest Control 22: 151-156.
Zhou, X., Wheeler, M.M., Oi, F.M., Scharf, M.E. (2008). Inhibition of termite cellulases by carbohydrate-based cellulase inhibitors: evidence from in vitro biochemistry and in vivo feeding studies. Pesticide Biochemistry and Physiology 90: 31–41. doi: 10.1016/j.pestbp.2007.07.011
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