Skip to main content

Advertisement

SpringerLink
Log in

A leaf-rolling weevil benefits from general saprophytic fungi in polysaccharide degradation

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

Insects, especially those feeding on leaf litter, widely form symbiosis with fungi. As dead plant tissues provide insects with poor-quality diets, which contain relatively high levels of indigestible lignin and cellulose, some saprophytic fungi may increase nutrient availability by polysaccharide degradation. Although the inherited, obligate bacterial symbionts are well documented, the non-inherited, facultative fungal symbionts are relatively overlooked. Females of the leaf-rolling weevil Heterapoderopsis bicallosicollis, a specialist of Triadica sebifera, construct leaf-rolls that serve as retreats from which larvae feed internally. We found that fungi associated with leaf-rolls were not transported by the female, but likely originated from the soil. To determine the effects of fungi on H. bicallosicollis development, fungal growth was reduced by a dry treatment. This treatment decreased adult weight and survival, and prolonged larval duration significantly. We further tested the hypothesis that fungi degrade leaf-roll polysaccharides, by a fungus inoculation experiment. Three dominant fungi (Penicillium sp., Aspergillus sp. and Cladosporium sp.) decreased the levels of soluble carbohydrate, cellulose, and lignin in inoculation experiments. Soluble carbohydrate, cellulose, and lignin of leaf-rolls all were found to decrease gradually during insect development. We conclude that these saprophytic fungi form facultative associations with H. bicallosicollis and benefit weevil nutrition by polysaccharide decomposition. Our study highlights the significance of fungal symbionts in insect nutritional ecology.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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 99(23):14887–14892

    Article  PubMed  CAS  Google Scholar 

  • Ayres MP, Wilkens RT, Ruel JJ, Lombardero MJ, Vallery E (2000) Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi. Ecology 81(8):2198–2210

    Article  Google Scholar 

  • Batra L, Batra S (1979) Termite-fungus mutualism. In: Betra L (ed) Insect-fungus symbiosis: mutualism and commensalism. Allaheld & Osmun, Montclair, pp 117–163

    Google Scholar 

  • Beaver R (1989) Insect-fungus relationships in the bark and ambrosia beetles. In: Wilding N, Collins N, Hammond P, Webber J (eds) Insect-fungus interactions. Academic Press, London, pp 121–143

    Google Scholar 

  • Bruce K, Cameron G, Harcombe P, Jubinsky G (1998) Introduction, impact on native habitats, and management of a woody invader, the Chinese tallow tree, Sapium sebiferum (L.) Roxb. Nat Areas J 17(3):255–260

    Google Scholar 

  • Damman H (1987) Leaf quality and enemy avoidance by the larvae of a pyralid moth. Ecology 68(1):88–97

    Article  Google Scholar 

  • Douglas AE (1989) Mycetocyte symbiosis in insects. Biol Rev Camb Philos Soc 64(4):409–434

    Article  PubMed  CAS  Google Scholar 

  • Douglas AE (2009) The microbial dimension in insect nutritional ecology. Funct Ecol 23(1):38–47

    Article  Google Scholar 

  • Dreywood R (1946) Qualitative test for carbohydrate material. Ind Eng Chem Anal Ed 18(8):499

    Article  CAS  Google Scholar 

  • Effland M (1977) Modified procedure to determine acid-insoluble lignin in wood and pulp. Tappi 60(10):143–144

    CAS  Google Scholar 

  • Ezeonu I, Noble J, Simmons R, Price D, Crow S, Ahearn D (1994) Effect of relative humidity on fungal colonization of fiberglass insulation. Appl Environ Microbiol 60(6):2149–2151

    PubMed  CAS  Google Scholar 

  • Gibson CM, Hunter MS (2010) Extraordinarily widespread and fantastically complex: comparative biology of endosymbiotic bacterial and fungal mutualists of insects. Ecol Lett 13(2):223–234

    Article  PubMed  Google Scholar 

  • Grassé P, Noirot C (1958) Le meule des termites champignonnistes et sa signification symbiotique. Ann Sci Nat Zool Biol Anim 20(11):113–128

    Google Scholar 

  • Grebebbikov VV, Leschen RAB (2010) External exoskeletal cavities in Coleoptera and their possible mycangial functions. Entomol Sci 13(1):81–98

    Article  Google Scholar 

  • Hättenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218

    Article  Google Scholar 

  • Heath JJ, Stireman JO III (2010) Dissecting the association between a gall midge, Asteromyia carbonifera, and its symbiotic fungus, Botryosphaeria dothidea. Entomol Exp Appl 137(1):36–49

    Article  Google Scholar 

  • Holloway B (1982) Anthribidae (Insecta: Coleoptera), vol. 3. Fauna of New Zealand Science Information Division, DSIR, Wellington, NZ

  • Hyodo F, Inoue T, Azuma J, 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(5):653–658

    Article  CAS  Google Scholar 

  • Jubinsky G, Anderson LC (1996) The invasive potential of Chinese tallow-tree (Sapium sebiferum Roxb.) in the Southeast. Castanea 61(3):226–231

    Google Scholar 

  • Kobayashi C, Fukasawa Y, Hirose D, Kato M (2008) Contribution of symbiotic mycangial fungi to larval nutrition of a leaf-rolling weevil. Evol Ecol 22(6):711–722

    Google Scholar 

  • Legalov A (2003) Taxonomy, Classification, and Phylogeny of Rhynchitids and Leaf-rolling Weevils (Coleoptera: Rhynchitidae, Attelabidae) of the World Fauna, vol. 733 + 350 (641 Mb). Novosibirsk

  • Martin M, Martin J (1978) Cellulose digestion in the midgut of the fungus-growing termite Macrotermes natalensis: the role of acquired digestive enzymes. Science 199(4336):1453–1455

    Article  PubMed  CAS  Google Scholar 

  • Martin M, Jones C, Bernays E (1991) The evolution of cellulose digestion in insects. Philos Trans R Soc Lond B Biol Sci 333(1267):281–288

    Article  Google Scholar 

  • Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190

    Article  PubMed  CAS  Google Scholar 

  • Mueller U (2002) Ant versus fungus versus mutualism: ant-cultivar conflict and the deconstruction of the attine ant-fungus symbiosis. Am Nat 160(4):67–98

    Article  Google Scholar 

  • Ohkuma M (2003) Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl Microbiol Biotechnol 61(1):1–9

    PubMed  CAS  Google Scholar 

  • Osono T (2005) Colonization and succession of fungi during decomposition of Swida controversa leaf litter. Mycologia 97(3):589–597

    Article  PubMed  Google Scholar 

  • Paine T, Raffa K, Harrington T (1997) Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Annu Rev Entomol 42(1):179–206

    Article  PubMed  CAS  Google Scholar 

  • Richard F, 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 Biochem Syst Environ Physiol 175(5):297–303

    Article  Google Scholar 

  • Rohlfs M, Kürschner L (2010) Saprophagous insect larvae, Drosophila melanogaster, profit from increased species richness in beneficial microbes. J Appl Entomol 134(8):667–671

    Google Scholar 

  • Rouland-Lefèvre C, Inoue T, Johjima T (2006) Termitomyces/termite interactions. In: König H (ed) Soil biology, Intestinal microorganisms of termites and other invertebrates, vol 6. Springer, Berlin, pp 335–350

    Chapter  Google Scholar 

  • Sakurai K (1985) An attelabid weevil (Euops splendida) cultivates fungi. J Ethol 3(2):151–156

    Article  Google Scholar 

  • Singh K (1991) An illustrated manual on identification of some seed-borne Aspergilli, Fusaria, Penicillia and their mycotoxins. Danish Government Institute of Seed Pathology for Developing Countries, Hellerup

    Google Scholar 

  • Teng N, Wang J, Chen T, Wu X, Wang Y, Lin J (2006) Elevated CO2 induces physiological, biochemical and structural changes in leaves of Arabidopsis thaliana. New Phytol 172(1):92–103

    Article  PubMed  CAS  Google Scholar 

  • Tokuda M, Maryana N, Yukawa J (2001) Leaf-rolling site preference by Cycnotrachelus roelofsi (Coleoptera: Attelabidae). Entomol Sci 4(2):229–237

    Google Scholar 

  • Updegraff D (1969) Semimicro determination of cellulose inbiological materials. Anal Biochem 32(3):420–424

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Ding J, Wheeler G, Purcell M, Zhang G (2009) Heterapoderopsis bicallosicollis (Coleoptera: Attelabidae): a potential biological control agent for Triadica sebifera. Environ Entomol 38(4):1135–1144

    Article  PubMed  Google Scholar 

  • Wang Y, Wu K, Ding J (2010) Host specificity of Euops chinesis, a potential biological control agent of Fallopia japonica, an invasive plant in Europe and North America. Biocontrol 55(4):551–559

    Article  Google Scholar 

  • Watanabe T (2002) Pictorial atlas of soil and seed fungi: Morphologies of cultured fungi and key to species. Lewis Publishers, Boca Raton

    Book  Google Scholar 

  • Watanabe H, Noda H, Tokuda G, Lo N (1998) A cellulase gene of termite origin. Nature 394(6691):330–331

    Article  PubMed  CAS  Google Scholar 

  • Zheng H, Wu Y, Ding J, Binion D, Fu W, Reardon R (2004) Invasive plants of Asian origin established in the United States and their natural enemies. US Department of Agriculture, Forest Service, Forest Health Technology Enterprise Team

Download references

Acknowledgments

We thank Shunliang Feng, Lin Wang, and Yi Wang for their field assistance. We also thank Minyan He and Wenfeng Guo for improvements of this manuscript. The project was funded by the 100 Talent Programs of the Chinese Academy of Sciences (to J. Ding) and the Florida Department of Environmental Protection (SL849 to G. Wheeler).

Author information

Authors and Affiliations

  1. Key Laboratory of Aquatic Plant and Watershed Ecology, Wuhan Botanical Garden/Institute, Chinese Academy of Science, Wuhan, 430074, Hubei, China

    Xiaoqiong Li & Jianqing Ding

  2. Graduate School of Chinese Academy of Sciences, Beijing, China

    Xiaoqiong Li

  3. Invasive Plant Research Laboratory, USDA/ARS, 3225 College Ave., Fort Lauderdale, FL, 33314, USA

    Gregory S. Wheeler

Authors
  1. Xiaoqiong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gregory S. Wheeler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jianqing Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jianqing Ding.

Additional information

Handling Editor: Guy Smagghe.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, X., Wheeler, G.S. & Ding, J. A leaf-rolling weevil benefits from general saprophytic fungi in polysaccharide degradation. Arthropod-Plant Interactions 6, 417–424 (2012). https://doi.org/10.1007/s11829-012-9194-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-012-9194-3

Keywords

Search

Navigation