Response of the lichen-eating moth Cleorodes lichenaria larvae to varying amounts of usnic acid in the lichens
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Abstract
Lichens are characterized by a great variety of secondary metabolites. The function of these substances remains partly unknown. In this study, we propose that some of these metabolites may expel insect herbivores. To test this hypothesis, we reared larvae of the lichenivorous moth Cleorodes lichenaria on three selected lichens, Cladonia arbuscula subsp. mitis, Usnea hirta, and Usnea dasypoga. In experimental setup, the secondary metabolite usnic acid was removed from the lichens with acetone prior to feeding, whereas a control was left untreated. On all three lichens, removal of usnic acid from the lichens using acetone significantly prolonged survival of larvae and increased their viability. Larvae reared on control lichens contained significantly more usnic acid than those reared on treated lichens, both in their biomass and their faeces. These results support the hypothesis that usnic acid serves as a repellent against insect feeding, besides its well established functions of UV protection and antimicrobial properties.
Keywords
Herbivory Insect feeding Moths Repellent Usnic acidNotes
Acknowledgments
This work was financially supported by Slovak Grant Agency (VEGA 1/1238/12). Thanks are expressed to Ass. Prof. Mag. Dr. Ingeborg Lang (Core Facility Cell Imaging and Ultrastructure Research, University of Vienna) for critical reading and reviewing this manuscript.
References
- Asplund J, Wardle DA (2013) The impact of secondary compounds and functional characteristics on lichen palatability and decomposition. J Ecol 101:689–700CrossRefGoogle Scholar
- Asplund J, Bokhorst S, Kardol P, Wardle DA (2015) Removal of secondary compounds increases invertebrate abundance in lichens. Fungal Ecol 18:18–25CrossRefGoogle Scholar
- Bačkor M, Klemová K, Bačkorová M, Ivanova V (2010) Comparison of the phytotoxic effect of usnic acid on cultures of free-living alga Scenedesmus quadricauda and aposymbiotically grown lichen photobiont Trebouxia erici. J Chem Ecol 36:405–411CrossRefPubMedGoogle Scholar
- Blewitt MR, Cooper-Driver GA (1990) The effects of lichen extracts on feeding by gypsy moth (Lymantria dispar). Bryologist 93:220–221CrossRefGoogle Scholar
- Culberson CF, Culberson WL, Johnson A (1977) Second supplement to chemical and botanical guide to lichen products. The American Bryological and Lichenological Society, Missouri Botanical Garden, St. LouisGoogle Scholar
- Emmerich R, Giez I, Lange OL, Proksch P (1993) Toxicity and antifeedant activity of lichen compounds against the polyphagous herbivorous insect Spodoptera littoralis. Phytochemistry 33(6):1389–1394. doi: 10.1016/0031-9422(93)85097-B CrossRefGoogle Scholar
- Fahselt D (1994) Secondary biochemistry of lichens. Symbiosis 16:117–165Google Scholar
- Feige GB, Lumbsch HT, Huneck S, Elix JA (1993) The identification of lichen substances by a standardized high-performance liquid chromatographic method. J Chromatogr 646:417–427CrossRefGoogle Scholar
- Gauslaa Y (2005) Lichen palatability depends on investments in herbivore defence. Oecologia 143(1):94–105CrossRefPubMedGoogle Scholar
- Gerson U, Seaward MRD (1977) Lichen-invertebrate associations. In: Seaward MRD (ed) Lichen ecology. Academic Press, London, pp 69–119Google Scholar
- Giez I, Lange OL, Proksch P (1994) Growth retarding activity of lichen substances against the polyphagous herbivorous insect Spodoptera littoralis. Biochem Syst Ecol 22:113–120CrossRefGoogle Scholar
- Hauck M, Huneck S (2007) Lichen substances affect metal absorption in Hypogymnia physodes. J Chem Ecol 33:219–223CrossRefPubMedGoogle Scholar
- Hauck M, Willenbruch K, Leuschner C (2009) Lichen substances prevent lichens from nutrient deficiency. J Chem Ecol 35:71–73CrossRefPubMedGoogle Scholar
- Hawksworth DL, Kirk PM, Sutton BC, Pegler DN (1995) Ainsworth and Bisby’s dictionary of the fungi, 8th edn. CAB International, Wallingford, p 616Google Scholar
- Hyvärinen M, Crittenden PD (2000) 33P translocation in the thallus of the mat forming lichen Cladonia portentosa. New Phytol 145:281–288CrossRefGoogle Scholar
- Ingólfsdóttir K (2002) Usnic acid. Phytochemistry 61(7):729–736CrossRefPubMedGoogle Scholar
- Larson DW (1987) The absorption and relase of water by lichens. In: Peveling E (ed) Progress and problems in lichenology in the eighties. Bibliotheca Lichenologica 25, J. Cramer, Berlin-Stuttgart, pp 351–360Google Scholar
- Lawrey JD (1983) Lichen herbivore preference: a test of two hypotheses. Am J Bot 70:1188–1194CrossRefGoogle Scholar
- Lawrey JD (1986) Biological role of lichen substances. Bryologist 89:111–122CrossRefGoogle Scholar
- Orange A, James PW, White FJ (2001) Microchemical methods for the identification of lichens. British Lichen Society, LondonGoogle Scholar
- Pöykkö H (2005) Host range of Lichenivorous Moths with special reference to nutritional quality and chemical defence in lichens. Ph.D. dissertation, Oulu University pressGoogle Scholar
- Pöykkö H (2006) Females and larvae of a geometrid moth Clerodes lichenaria prefer a lichen host that assures shortest larval period. Environ Entomol 35:1669–1676CrossRefGoogle Scholar
- Pöykkö H (2011a) Host growth form underlies enemy-free space for lichen-feeding moth larvae. J Anim Ecol 80:1324–2329CrossRefPubMedGoogle Scholar
- Pöykkö H (2011b) Enemy-free space and the host range of a lichenivorous moth: a field experiment. Oikos 120:564–569CrossRefGoogle Scholar
- Pöykkö H, Tammaru T (2010) Countergradient versus cogradient variation in growth and diapause in a lichen-feeding moth, Eilema depressum (Lepidoptera: Arctiidae). J Evol Biol 23(6):1278–1285CrossRefPubMedGoogle Scholar
- Pöykkö H, Hyvärinen M, Bačkor M (2005) Removal of lichen secondary metabolites affects food choice and survival of lichenivorous moth larvae. Ecology 86(10):2623–2632CrossRefGoogle Scholar
- Pöykkö H, Bačkor M, Bencúrová E, Mocanová V, Bačkorová M, Hyvärinen M (2010) Host use of a specialist lichen-feeder: dealing with lichen secondary metabolites. Oecologia 164(2):423–430CrossRefPubMedGoogle Scholar
- Reutimann P, Scheidegger C (1987) Importance of lichen secondary products in food choice of two oribatid mites (Acari) in an alpine meadow ecosystem. J Chem Ecol 13:363–369CrossRefPubMedGoogle Scholar
- Slansky F (1979) Effect of the lichen chemicals atranorin and vulpinic acid upon feeding and growth of larvae of the yellow—striped armyworm, Spodoptera ornithogalli. Environ Entomol 8:865–868CrossRefGoogle Scholar
- Solhaug KA, Gauslaa Y (1996) Protective role of parietin against high light in the lichen Xanthoria parietina. Oecologia 108:412–418CrossRefGoogle Scholar
- Solhaug KA, Gauslaa Y (2004) Photosynthates stimulate the UV-B induced fungal anthraquinone synthesis in the UV-B induced fungal anthraquinone synthesis in the foliose lichen Xanthoria parietina. Plant Cell Environ 27:167–176CrossRefGoogle Scholar
- Solhaug KA, Lind M, Nybakken L, Gauslaa Y (2009) Possible functional roles of cortical depsides and medullary depsidones in the foliose lichen Hypogymnia physodes. Flora 204:40–48CrossRefGoogle Scholar
- Stahl GE (1904) Die Schutzmittel der Flechten gegen Tierfrass. In: Festschrift zum sibenzigsten Geburstage von Ernst Haeckel. Fischer, Jena, pp 357–375Google Scholar
- Stephenson NL, Rundel PW (1979) Quantitative variation and the ecological role of vulpinic acid and atranorin in the thallus Letharia vulpina (Lichenes). Biochem Syst Ecol 7:263–267CrossRefGoogle Scholar
- Zukal H (1895) Morphologische und biologische Untersuchungen über die Flechten II. Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften. Mathematisch-Naturwissenschaftliche Classe 104:1303–1395Google Scholar