Evolutionary Ecology

, Volume 22, Issue 6, pp 711–722

Contribution of symbiotic mycangial fungi to larval nutrition of a leaf-rolling weevil

  • Chisato Kobayashi
  • Yu Fukasawa
  • Dai Hirose
  • Makoto Kato
Original Paper

Abstract

Some phytophagous insects have been known to inoculate certain fungi on plant substrates. In many cases of such insect–fungi relationships it has been considered that fungi contribute to insects by decomposing lignin or polysaccharides, and that the insects feed on the decomposition products or fungi themselves. Females of the leaf-rolling weevil in the genus Euops (Attelabidae) store spores of symbiotic fungi in the mycangia and inoculate them on leaf rolls. To determine the effect of mycangial fungi on larval nutrition in E. lespedezae, the nutritional value was compared between leaves with and without mycangial fungi. Two Penicillium species were isolated from the mycangia. These mycangial fungi showed little effect on the decomposition of lignin and polysaccharides, and showed little effect on enhancement of soluble sugars within leaves. Thus, the mutualism between Euops and its mycangial fungi contrasts with the mainly nutritional mutualisms between wood-infesting insects (termites, bark/ambrosia beetles, and wood wasps) and lignin/polysaccharide-decomposing fungi.

Keywords

Euops lespedezae Insect–fungus symbiosis Larval development Nutritional enhancement Penicillium 

References

  1. Aanen DK, Eggleton P, Rouland-Lefèvre C, Guldberg-Frøslev T, Rosendahl S, Boomsma JJ (2002) The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc Natl Acad Sci USA 23:14887–14892CrossRefGoogle Scholar
  2. Abe T, Higashi M (1991) Cellulose centered perspective on terrestrial community structure. Oikos 60:127–133CrossRefGoogle Scholar
  3. Abril AB, Bucher EH (2002) Evidence that the fungus cultured by leaf-cutting ants does not metabolize cellulose. Ecol Lett 5:325–328CrossRefGoogle Scholar
  4. Bacci M Jr, Anversa MM, Pagnocca FC (1995) Cellulose degradation by Leucocoprinus gongylophorus, the fungus cultured by the leaf-cutting ant Atta sexdens rubropilosa. Antonie von Leeuwenhoek 67:385–386CrossRefGoogle Scholar
  5. Barras SJ, Hodges JD (1969) Carbohydrates in inner bark of Pinus taeda as affected by Dendroctonus frontalis and associated microorganisms. Can Entomol 101:489–493CrossRefGoogle Scholar
  6. Batra LR (1979) Insect–fungus symbiosis. Allenheld & Osmun, Montclair, NJGoogle Scholar
  7. Batra LR, Batra SWT (1979) Termite–fungus mutualism. In: Batra LR (ed) Insect–fungus symbiosis. Allenheld & Osmun, Montclair, NJ, pp 77–116Google Scholar
  8. Bridges JR (1983) Mycangial fungi of Dendroctonous frontalis (Coleoptera: Scolytidae) and their relationship to beetle population trends. Environ Entomol 12:858–861Google Scholar
  9. Bridges JR, Perry TJ (1985) Effects of mycangial fungi on gallery construction and distribution of bluestain in southern pine beetle-infested pine bolts. J Entomol Sci 20(2):271–275Google Scholar
  10. D’Ettorre P, Mora P, Dibangou V, Rouland C, Errard C (2002) The role of the symbiotic fungus in the digestive metabolism of two species of fungus-growing ants. J Comp Physiol B 172:169–176PubMedCrossRefGoogle Scholar
  11. Domsch KH, Gams W, Anderson T-H (1993) Compendium of soil fungi, vol 1. IHW-Verlag, EchingGoogle Scholar
  12. Evans HC (1989) Mycopathogens of insects of epigeal and aerial habitats. In: Wilding N, Collins NM, Hammond PM, Webber JF (eds) Insect–fungus interactions. Academic Press, London, pp 205–238Google Scholar
  13. Gardes M, Bruns TD (1993) ITS primer with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rust. Mol Ecol 21:113–118CrossRefGoogle Scholar
  14. Haack RA, Slansky F Jr (1987) Nutritional ecology of wood-feeding Coleoptera, Lepidoptera, and Hymenoptera. In: Slansky F Jr, Rodriguez JG (eds) Nutritional ecology of insects, mites, spiders, and related invertebrates. Wiley, New York, pp 449–486Google Scholar
  15. Hochuli DF (1996) The ecology of plant/insect interactions: implications of digestive strategy for feeding by phytophagous insects. Oikos 75:133–141CrossRefGoogle Scholar
  16. Hölldbler B, Wilson EO (1990) The ants. Belknap, CambridgeGoogle Scholar
  17. Hyodo F, Inoue T, Azuma J-I, Tayasu I, Abe T (2000) Role of the mutualistic fungus in lignin degradation in the fungus-growing termite Macrotermes gilvus (Isoptera; Macrotermitinae). Soil Biol Biochem 32:653–658CrossRefGoogle Scholar
  18. Iwamoto S, Tokumasu S, Suyama Y, Kakishima M (2002) Molecular phylogeny of four selected species of the strictly anamorphic genus Thysanophora using nuclear ribosomal DNA sequences. Mycoscience 43:169–180CrossRefGoogle Scholar
  19. Kendrick B (2000) The fifth kingdom, 3rd edn. Focus Publishing, USAGoogle Scholar
  20. Kukor JJ, Martin MM (1983) Acquisition of digestive enzymes by siricid woodwasps from their fungal symbiont. Science 220:1161–1163PubMedCrossRefGoogle Scholar
  21. Lee KE, Wood TG (1971) Termites and soil. Academic Press, LondonGoogle Scholar
  22. Littledyke M, Cherrett JM (1976) Direct ingestion of plant sap from cut leaves by the leaf-cutting ants Atta cephalotes (L.) and Acromyrmex octospinosus (Reich) (Formicidae, Attini). Bull Entomol Res 66:205–217CrossRefGoogle Scholar
  23. Madden JL (1988) Sirex in Australasia. In: Berryman AA (ed) Dynamics of forest insect populations: patterns, causes, implications. Plenum, New York, pp 407–429Google Scholar
  24. Martin MM (1991) The evolution of cellulose digestion in insects. Philos Trans R Soc Lond B 333:281–288CrossRefGoogle Scholar
  25. Martin MM, Martin JS (1978) Cellulose digestion in the midgut of the fungus-growing termite Macrotermes natalensis: the role of acquired digestive enzymes. Science 199:1453–1455PubMedCrossRefGoogle Scholar
  26. Martin MM, Weber NA (1969) The cellulose-utilizing capability of the fungus cultured by the Attine ant Atta colombica tonsipes. Ann Entomol Soc Am 62:1386–1387PubMedGoogle Scholar
  27. Martin T, Oliveira L, Garcia P (2005) Larval mortality factors of Spodoptera littoralis in the Azores. BioControl 50:761–770CrossRefGoogle Scholar
  28. Maynard AL, Loosli BS, Harold FH, Warner RG (1979) Animal nutrition. McGrow-Hill Book Company, New YorkGoogle Scholar
  29. Miura K, Kudo M (1970) An agar-medium for aquatic hyphomycetes. Trans Mycol Soc Jpn 11:116–118 (in Japanese)Google Scholar
  30. Morgan FD (1968) Bionomics of siricidae. Annu Rev Entomol 13:239–256CrossRefGoogle Scholar
  31. O’Donnell K (1993) Fusarium and its near relatives. In: Reynolds DR, Taylor JW (eds) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Wallingford, pp 225–233Google Scholar
  32. Osono T (2002) Phyllosphere fungi on leaf litter of Fagus crenata: occurrence, colonization, and succession. Can J Bot 80:460–469CrossRefGoogle Scholar
  33. Paine TD, Raffa KF, Harrington TC (1997) Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Annu Rev Entomol 42:179–206PubMedCrossRefGoogle Scholar
  34. Peterson SW (2000) Phylogenetic analysis of Penicillium species based on ITS and lsu-rDNA nucleotide sequences. In: Samson RA, Pitt JI (eds) Integration of modern taxonomic methods for Penicillium and Aspergillus classification. Hardwood, Amsterdam, pp 163–178Google Scholar
  35. Quinlan RJ, Cherrett JM (1979) The role of fungus in the diet of the leaf-cutting ant. Ecol Entomol 4:151–160CrossRefGoogle Scholar
  36. Richard F-J, Mora P, Errard C, Rouland C (2005) Digestive capacities of leaf-cutting ants and the contribution of their fungal cultivar to the degradation of plant material. J Comp Physiol B 175:297–303PubMedCrossRefGoogle Scholar
  37. Riedel A (2002) Taxonomy, phylogeny, and zoogeography of the weevil genus Euops (Insecta: Coleoptera: Curcurionoidea) in the Papuan region. PhD thesis, Ludwig Maximilians University, MunichGoogle Scholar
  38. Rohlfs M, Obmann B, Peterson R (2005) Competition with filamentous fungi and its implication for a gregarious lifestyle in insects living on ephemeral resources. Ecol Entomol 30:556–563CrossRefGoogle Scholar
  39. Sakurai K (1985) An attelabid weevil (Euops splendida) cultivates fungi. J Ethol 3:151–156CrossRefGoogle Scholar
  40. Sawada Y, Morimoto K (1986) The mycetangia and the mode of the fungus transmission in the weevil genus Euops (Coleoptera: Attelabidae). Sci Bull Fac Agr Kyusyu Univ 40(4):197–205 (in Japanese with English summary) Google Scholar
  41. Schoonhoven LM, Jermy T, van Loon JJA (1997) Insect–plant biology. Chapman & Hall, LondonGoogle Scholar
  42. Silva A, Bacci M Jr, Siqueira CG, Bueno OC, Pagnocca FC, Hebling MJA (2003) Survival of Atta sexdens workers on different food sources. J Insect Physiol 49:307–313PubMedCrossRefGoogle Scholar
  43. Siqueira CG, Bacci M Jr, Pagnocca FC, Bueno OC, Hebling MJA (1998) Metabolism of plant polysaccharides by Leucoagaricus gongylophorus, the symbiotic fungun of the leaf-cutting ant Atta sexdens L. Appl Environ Microb 64:4820–4822Google Scholar
  44. Suzuki K, Uehara C (1997) Cradle structure and formation process in the subfamilies Apoderinae and Attelabinae (Coleoptera, Attelabidae) from Japan. Bull Hoshizaki Green Found 1:99–204Google Scholar
  45. Takabe N (2004) Host use of Euops splendidus and dynamics of its mutualistic fungi through development of the beetle. Master’s thesis, Nagoya University (in Japanese)Google Scholar
  46. Talmadge KW, Keegstra K, Bauer WD, Albersheim P (1973) The structure of plant cell wall. Plant Physiol 51:158–173PubMedCrossRefGoogle Scholar
  47. Watanabe H, Noda H, Tokuda G, Lo N (1998) A cellulase gene of termite origin. Nature 394:330–331PubMedCrossRefGoogle Scholar
  48. Wheeler Q, Blackwell M (1984) Fungus–insect relationships. Columbia University Press, New YorkGoogle Scholar
  49. Wilding N, Collins NM, Hammond PM, Webber JF (1989) Insect–fungus interactions. Academic Press, LondonGoogle Scholar
  50. Yamaji K, Fukushi Y, Hashidoko Y, Yoshida T, Tahara S (1999) Characterization of antifungal metabolites produced by Penicillium species isolated from seeds of Picea glehnii. J Chem Ecol 25:1643–1645CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Chisato Kobayashi
    • 1
  • Yu Fukasawa
    • 2
  • Dai Hirose
    • 3
  • Makoto Kato
    • 1
  1. 1.Graduate School of Human and Environmental StudiesKyoto UniversityKyotoJapan
  2. 2.Laboratory of Forest Ecology, Graduate School of AgricultureKyoto UniversityKyotoJapan
  3. 3.Sugadaira Montane Research CenterUniversity of TsukubaSanadaJapan

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