Skip to main content
SpringerLink
Log in

Gut-Based Antioxidant Enzymes in a Polyphagous and a Graminivorous Grasshopper

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Graminivorous species of grasshoppers develop lethal lesions in their midgut epithelia when they ingest tannic acid, whereas polyphagous grass- hoppers are unaffected by ingested tannins. This study tests the hypothesis that polyphagous species are defended by higher activities of antioxidant enzymes (constitutive or inducible) in their guts than are graminivorous species. Comparisons were made between four antioxidant enzymes: superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APOX), and glutathione transferase peroxidase (GSTPX). Enzyme activities were measured in the gut lumens and midgut tissues of Melanoplus sanguinipes (polyphagous) and Aulocara ellioti (graminivorous). The results of this study do not support the hypothesis that M. sanguinipes is better defended by antioxidant enzymes than is A. ellioti, nor are these enzymes more inducible in M. sanguinipes than in A. ellioti when insects consume food containing 15% dry weight tannic acid. Instead, tannic acid consumption reduced SOD, APOX, and GSTPX activities in both species. This study reports the first evidence that SOD is secreted into the midgut lumen in insects, with activities two- to fourfold higher than those found in midgut tissues. The spatial distribution of GSTPX and APOX activities observed in both species suggests that ingested plant antioxidant enzymes may function as acquired defenses in grasshoppers. In addition, the results of this study permit the first comparison between the antioxidant enzyme defenses of Orthoptera and Lepidoptera. Most notably, grasshoppers have higher SOD activities than caterpillars, but completely lack APOX in their midgut tissues.

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

Similar content being viewed by others

REFERENCES

  • Aebi, H.1984. Catalase in vitro. Methods Enzymol. 105:121–126.

    Google Scholar 

  • Ahmad, S. and Pardini, R. S.1990. Antioxidant defense of the cabbage looper, Trichoplusia ni: Enzymatic responses to the superoxide-generating flavonoid, quercetin, and photodynamic furanocoumarin, xanthotoxin. Photochem. Photobiol. 51:305–311.

    Google Scholar 

  • Ahmad, S., Pritsos, C. A., Bowen, S. M., Kirkland, K. E., Blomquist, G. J., and Pardini, R. S.1987. Activities of enzymes that detoxify superoxide anion and related toxic oxyradicals in Trichoplusia ni. Arch. Insect Biochem. Physiol. 6:85–96.

    Google Scholar 

  • Appel, H. M. and Joern, A.1998. Gut physicochemistry of grassland grasshoppers. J. Insect Physiol. 44:693–700.

    Google Scholar 

  • Appel, H. M. and Martin, M. M.. 1990. Gut redox conditions in herbivorous lepidopteran larvae. J. Chem. Ecol.16:3277–3290.

    Google Scholar 

  • Asada, K.1984. Chloroplasts: Formation of active oxygen and its scavenging. Methods Enzymol.105:422–429.

    Google Scholar 

  • Aucoin, R. R., Philogene, B. J. R., and Arnason, J. T.1991. Antioxidant enzymes as biochemical defenses against phototoxin-induced oxidative stress in three species of herbivorous Lepidoptera. Arch. Insect. Biochem. Physiol.16:139–152.

    Google Scholar 

  • Barbehenn, R. V. and Martin, M. M.1994. Tannin sensitivity in Malacosoma disstria: Roles of the peritrophic envelope and midgut oxidation. J. Chem. Ecol. 20:1985–2001.

    Google Scholar 

  • Barbehenn, R. V., Martin, M. M., and Hagerman, A. E.1996. Reassessment of the roles of the peritrophic envelope and hydrolysis in protecting polyphagous grasshoppers from ingested hydrolyzable tannins. J. Chem. Ecol.22:1901–1919.

    Google Scholar 

  • Barbehenn, R. V., Bumgarner, S. L., Roosen, E. F., and Martin, M.M.2001. Antioxidant defenses in caterpillars: Role of the ascorbate-recycling system in the midgut lumen. J. Insect Physiol. 47:349–357.

    Google Scholar 

  • Berenbaum M.R.1991. Comparative processing of allelochemicals in the Papilionidae (Lepidoptera). Arch. Insect Biochem. Physiol.17:213–221.

    Google Scholar 

  • Bernays, E. A.1978. Tannins: An alternative viewpoint. Entomol. Exp. Appl. 24:244–253.

    Google Scholar 

  • Bernays, E. A. and Barbehenn, R. V.1987. Nutritional ecology of grass foliage-chewing insects, pp. 147–176, inF. Slansky, Jr., and J. G. Rodriguez (eds.). Nutritional Ecology of Insects, Mites, Spiders, and Related Invertebrates. Wiley, New York.

    Google Scholar 

  • Bernays, E. A. and Chamberlain, D. J.1980. A study of tolerance of ingested tannin in Schistocerca gregaria. J. Insect Physiol.26:415–420.

    Google Scholar 

  • Bernays, E. A., Chamberlain, D., and McCarthy, P.1980. The differential effects of ingested tannic acid on different species of Acridoidea. Entomol. Exp. Appl.28:158–166.

    Google Scholar 

  • Bi, J. L. and Felton G. W.1995. Foliar oxidative stress and insect herbivory: Primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J. Chem. Ecol. 21:1511–1530.

    Google Scholar 

  • Canada, A. T., Giannella, E., Nguyen, T. D., and Mason, R. P.1990. The production of reactive oxygen species by dietary flavonols. Free Radic. Biol. Med. 9:441–449.

    Google Scholar 

  • Chapman, R. F.1988. The relationship between diet and the size of the midgut caeca in grasshoppers (Insecta: Orthoptera: Acridoidea). Zool. J. Linn. Soc. 94:319–338.

    Google Scholar 

  • Dow, J. A. T.1984. Extremely high pH in biological systems: A model for carbonate transport. Am. J. Physiol. 246:R633–R635.

    Google Scholar 

  • Duffey, S. S. and Felton, G. W.1989. Plant enzymes in resistance to insects, pp. 289–313, inJ. R. Whitaker and P. E. Sonnet (eds.). Biocatalysis in Agricultural Biotechnology. ACS Symposium Series, Vol. 389. American Chemical Society, Washington, D.C.

    Google Scholar 

  • Evans, W. A. L. and Payne, D. W.1964. Carbohydrases of the alimentary tract of the desert locust, Schistocerca gregariaForsk. J. Insect Physiol.10:657–674.

    Google Scholar 

  • Felton, G. W. and Duffey, S. S.1991. Protective role of midgut catalases in lepidopteran larvae against oxidative plant defenses. J. Chem. Ecol. 17:1715–1732.

    Google Scholar 

  • Felton, G. W. and Duffey, S. S.1992. Ascorbate oxidation reduction in Helicoverpa zeaas a scavenging system against dietary oxidants. Arch. Insect Biochem. Physiol. 19:27–37.

    Google Scholar 

  • Felton, G. W. Donato, K., Del Veccio, R. J., and Duffey, S. S.1989. Activation of plant foliar oxidases by insect feeding reduces the nutritive quality of foliage for herbivores. J. Chem. Ecol. 15:2667–2694.

    Google Scholar 

  • Feng, R. and Isman, M. B.1994. Tissue distribution and developmental changes in detoxication enzyme activities in the migratiory grasshopper, Melanoplus sanguinipes(Acrididae). Pestic. Biochem. Physiol.48:48–55.

    Google Scholar 

  • Ferreira, C., Oliveira, M. C., and Terra, W. R.1990. Compartmentalization of the digestive process in Abracris flavolineatea(Orthoptera: Acrididae) adults. Insect Biochem. 20:267–274.

    Google Scholar 

  • Gant, T. W., Ramakrishna, R., Mason, R. P., and Cohen, G. M.1988. Redox cycling and sulphydryl arylation; their relative importance in the mechanism of quinone cytotoxicity to isolated hepatocytes. Chem.-Biol. Interactions65:157–173.

    Google Scholar 

  • Grisham, M.B.1992. Reactive Metabolites of Oxygen and Nitrogen in Biology and Medicine. Landes, Austin, Texas.

    Google Scholar 

  • Hanham, A. F., Dunn, B. P., and Stich, H. F.1983. Clastogenic activity of caffeic acid and its relationship to hydrogen peroxide generated during autoxidation. Mutat. Res.116:333–339.

    Google Scholar 

  • Halliwell, B. and Gutteridge, J. M. C.1999. Free Radicals in Biology and Medicine. Oxford University Press, Oxford.

    Google Scholar 

  • Imlay, J. A., Chin, S. M., and Linn, S.1988. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science240:640–642.

    Google Scholar 

  • Isely, F. B.1944. Correlation between mandibular morphology and food specificity in grasshoppers. Ann. Entomol. Soc. Am. 37:47–67.

    Google Scholar 

  • Isman, M. B., Feng, R., and Johnson, D. L.1996. Detoxicative enzyme activities in five species of field-collected melanopline grasshoppers (Orthoptera: Acrididae). Can. Entomol. 128:353–354.

    Google Scholar 

  • Lee, K.1991. Glutathione S-transferase activities in phytophagous insects: Induction and inhibition by plant phototoxins and phenols. Insect Biochem.21:353–361.

    Google Scholar 

  • Lee K. and Berenbaum M.R.1989. Action of antioxidant enzymes and cytochrome P-450 monooxygenases in the cabbage looper in response to plant phototoxins. Arch. Insect Biochem. Physiol.10:151–162.

    Google Scholar 

  • Lee, K. and Berenbaum, M. R.1990. Defense of parsnip webworm against phototoxic furanocoumarins: Role of antioxidant enzymes. J. Chem. Ecol. 16:2451–2460.

    Google Scholar 

  • Lindroth, R. L. and Peterson, S. S.1988. Effects of plant phenols on performance of southern armyworm larvae. Oecologia75:185–189.

    Google Scholar 

  • Maddrell, S. H. P. and Gardiner, B. O. C.1980. The permeability of the cuticular lining of the insect alimentary canal. J. Exp. Biol. 85:227–237.

    Google Scholar 

  • Martin, M. M.1987. Invertebrate-Microbial Interactions: Ingested Fungal Enzymes in Arthropod Biology. Comstock Publishing Associates, Ithaca, New York.

    Google Scholar 

  • Mathews, M. C., Summers, C. B., and Felton, G.W.1997. Ascorbate peroxidase:Anovel antioxidant enzyme in insects. Arch. Insect Biochem. Physiol. 34:57–68.

    Google Scholar 

  • Misra, H. P. and Fridovich, I.1972. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J. Biol. Chem. 247: 3170–3175.

    Google Scholar 

  • Munkres, K. D.1990. Purification of exocellular superoxide dismutases. Methods Enzymol. 186:249–259.

    Google Scholar 

  • Peric-Mataruga, V., Blagojevic, D., Spasic, M. B., Ivanovic, J., and Jankovic-Hladni, M.1997. Effect of the host plant on the antioxidative defence in the midgut of Lymantria disparL. caterpillars of different population origins. J. Insect Physiol. 43:101–106.

    Google Scholar 

  • Pritsos, C. A., Ahmad, S., Bowen, S. M., Elliot, A. J., Blomquist, G. J., and Pardini, R. S.1988.Antioxidant enzymes of the black swallowtail butterfly, Papilio polyxenes, and their response to the prooxidant allelochemical, quercetin. Arch. Insect Biochem. Physiol. 8:101–112.

    Google Scholar 

  • Rosen, G. M., Britigan, B. E., Halpern, H. J., and Pou, S.1999. Free Radicals: Biology and Detection by Spin Trapping. Oxford University Press, Oxford.

    Google Scholar 

  • SAS Institute. 2000. The SAS System for Windows, Version 8e. SAS Institute, Cary, North Carolina.

    Google Scholar 

  • Schultz, J. C. and Lechowicz, M. J.1986. Hostplant, larval age, and feeding behavior influence midgut pH in the gypsy moth (Lymantria dispar). Oecologia71:133–137.

    Google Scholar 

  • Steinly, B. A. and Berenbaum, M.1985. Histopathological effects of tannins on the midgut epithelium of Papilio polyxenesand Papilio glaucus. Entomol. Exp. Appl. 39:3–9.

    Google Scholar 

  • Stoscheck, C. M.1990. Increased uniformity in the response of the Coomassie blue G protein assay to different proteins. Anal. Biochem. 184:111–116.

    Google Scholar 

  • Summers, C. B. and Felton, G.W.1994. Prooxidant effects of phenolic acids on the generalist herbivore Helicoverpa zea(Lepidoptera: Noctuidae): Potential mode of action for phenolic compounds in plant anti-herbivore chemistry. Insect Biochem. Mol. Biol.24:943–953.

    Google Scholar 

  • Thiboldeaux, R. L., Lindroth, R. L., and Tracy, J. W.1998. Effects of juglone (5-hydroxy-1,4-naphthoquinone) on midgut morphology and glutathione status in Saturniid moth larvae. Comp. Biochem. Physiol. 120:481–487.

    Google Scholar 

  • Weinhold, L. C., Ahmad, S., and Pardini, R. S.1990. Insect glutathione S-transferase: A predictor of allelochemical and oxidative stress. Comp. Biochem. Physiol.95B:355–363.

    Google Scholar 

  • Zheng, J., Cho, M., Jones, A. D., and Hammock, B. D.1997. Evidence of quinone metabolites of naphthalene covalently bound to sulfur nucleophiles of proteins of murine clara cells after exposure to napthalene. Chem. Res. Toxicol. 10:1008–1014.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, Michigan, 48109-1048

    Raymond V. Barbehenn

Authors
  1. Raymond V. Barbehenn
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barbehenn, R.V. Gut-Based Antioxidant Enzymes in a Polyphagous and a Graminivorous Grasshopper. J Chem Ecol 28, 1329–1347 (2002). https://doi.org/10.1023/A:1016288201110

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1016288201110

Search

Navigation