Gut pH, redox conditions and oxygen levels in an aquatic caterpillar: Potential effects on the fate of ingested tannins

Journal of Insect Physiology

Volumn 54, Issue 2, 2008, Pages 462-471

  Gross, Elisabeth M ^a   Brune, Andreas ^b   Walenciak, Oliver ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

Author keywords

Chemical defence; Freshwater plant herbivore interaction; Gut redox conditions; Hydrolysable tannin

Indexed keywords

OXYGEN; TANNIN DERIVATIVE;

AQUATIC PLANT; BIOCHEMICAL OXYGEN DEMAND; CATERPILLAR; DIGESTIVE SYSTEM; MOTH; OXYGEN; PH; PLANT-HERBIVORE INTERACTION; REDOX CONDITIONS; TANNIN;

ANIMAL; ARTICLE; CHEMISTRY; ECOSYSTEM; FEEDING BEHAVIOR; GASTROINTESTINAL TRACT; METABOLISM; MOTH; OXIDATION REDUCTION REACTION; PH; PHYSIOLOGY; POTAMOGETONACEAE; SAXIFRAGACEAE;

ANIMALS; ECOSYSTEM; FEEDING BEHAVIOR; GASTROINTESTINAL TRACT; HYDROGEN-ION CONCENTRATION; MOTHS; OXIDATION-REDUCTION; OXYGEN; POTAMOGETONACEAE; SAXIFRAGACEAE; TANNINS;

ACENTRIA EPHEMERELLA; LEPIDOPTERA; MYRIOPHYLLUM SPICATUM; POTAMOGETON PERFOLIATUS; PYRALIDAE;

EID: 38749100170     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2007.11.005     Document Type: Article

References (54)

1. Appel H.M. Phenolics in ecological interactions: the importance of oxidation. Journal of Chemical Ecology 19 (1993) 1521-1552
2. Appel H.M., and Maines L.W. The influence of host-plant on gut conditions of gypsy moth (Lymantria dispar) caterpillars. Journal of Insect Physiology 41 (1995) 241-246
3. Appel H.M., and Martin M.M. Gut redox conditions in herbivorous lepidopteran larvae. Journal of Chemical Ecology 16 (1990) 3277-3290
4. Barbehenn R.V. Roles of peritrophic membranes in protecting herbivorous insects from ingested plant allelochemicals. Archives of Insect Biochemistry and Physiology 47 (2001) 86-99
5. Barbehenn R.V., and Martin M.M. The protective role of the peritrophic membrane in the tannin-tolerant larvae of Orgyia leucostigma (Lepidoptera). Journal of Insect Physiology 38 (1992) 973-980
6. Barbehenn R.V., and Martin M.M. Tannin sensitivity in larvae on Malacosoma disstria (Lepidoptera): roles of the peritrophic envelope and midgut oxidation. Journal of Chemical Ecology 20 (1994) 1985-2001
7. Barbehenn R.V., Poopat U., and Spencer B. Semiquinone and ascorbyl radicals in the gut fluids of caterpillars measured with EPR spectrometry. Insect Biochemistry and Molecular Biology 33 (2003) 125-130
8. Barbehenn R.V., Walker A.C., and Uddin F. Antioxidants in the midgut fluids of a tannin-tolerant and a tannin-sensitive caterpillar: effects of seasonal changes in tree leaves. Journal of Chemical Ecology 29 (2003) 1099-1116
9. Barbehenn R., Dodick T., Poopat U., and Spencer B. Fenton-type reactions and iron concentrations in the midgut fluids of tree-feeding caterpillars. Archives of Insect Biochemistry and Physiology 60 (2005) 32-43
10. Barbehenn R.V., Jones C.P., Hagerman A.E., Karonen M., and Salminen J.-P. Ellagitannins have greater oxidative activities than condensed tannins and galloyl glucoses at high pH: potential impact on caterpillars. Journal of Chemical Ecology 32 (2006) 2253-2267
11. Berenbaum M. Adaptive significance of midgut pH in larval Lepidoptera. American Naturalist 115 (1980) 138-146
12. Bernays E.A. Tannins: an alternative viewpoint. Entomologia Experimentalis Et Applicata 24 (1978) 244-253
13. Bi J.L., and Felton G.W. Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. Journal of Chemical Ecology 21 (1995) 1511-1530
14. Brune A., Emerson D., and Breznak J.A. The termite gut microflora as an oxygen sink: microelectrode determination of oxygen and pH gradients in guts of lower and higher termites. Applied and Environmental Microbiology 61 (1995) 2681-2687
15. Choi C., Bareiss C., Walenciak O., and Gross E.M. Impact of polyphenols on the growth of the aquatic herbivore Acentria ephemerella (Lepidoptera: Pyralidae). Journal of Chemical Ecology 28 (2002) 2223-2235
16. De Veau E.J.I., and Schultz J.C. Reassessment of interaction between gut detergents and tannins in Lepidoptera and significance for gypsy moth larvae. Journal of Chemical Ecology 18 (1992) 1437-1453
17. Dow J.A. pH gradients in lepidopteran midgut. Journal of Experimental Biology 172 (1992) 355-375
18. Ebert A., and Brune A. Hydrogen concentration profiles at the oxic-anoxic interface: a microsensor study of the hindgut of the wood-feeding lower termite Reticulitermes flavipes (Kollar). Applied and Environmental Microbiology 63 (1997) 4039-4046
19. Felton G.W., Donato K., Del Vecchio R.J.D., and Duffey S.S. Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. Journal of Chemical Ecology 15 (1989) 2667-2694
20. Gaevskaya, N.S., 1969. The Role of Higher Aquatic Plants in the Nutrition of the Animals of Freshwater Basins (Muller, D.G.M., Trans.; Mann, K.H., Ed.). National Lending Library of Science and Technology, Yorkshire, UK.
21. Gringorten J.L., Crawford D.N., and Harvey W.R. High pH in the ectoperitrophic space of the larval lepidopteran midgut. Journal of Experimental Biology 183 (1993) 353-359
22. Gross E.M., Meyer H., and Schilling G. Release and ecological impact of algicidal hydrolysable polyphenols in Myriophyllum spicatum. Phytochemistry 41 (1996) 133-138
23. Gross E.M., Johnson R.L., and Hairston Jr. N.G. Experimental evidence for changes in submersed macrophyte species composition caused by the herbivore Acentria ephemerella (Lepidoptera). Oecologia 127 (2001) 105-114
24. Gross E.M., Feldbaum C., and Choi C. High abundance of herbivorous Lepidoptera larvae (Acentria ephemerella Denis & Schiffermüller) on submersed macrophytes in Lake Constance (Germany). Archiv fuer Hydrobiologie 155 (2002) 1-21
25. Henn M. The changes of polyphenols as a result of the passage through the gut of the gypsy moth Lymantria dispar (Lep., Lymantriidae): influence on the growth of the larvae. Journal of Applied Entomology 123 (1999) 391-395
26. Henn M. Intestinal modifications of oak leaf tannins by Lymantria dispar L. (Lep., Lymantriidae) and possible effect on larval development. Journal of Applied Entomology 123 (1999) 261-264
27. Isman M.B., and Duffey S.S. Toxicity of tomato phenolic compounds to the fruitworm, Heliothis zea. Entomologia Experimentalis Et Applicata 31 (1982) 370-376
28. Isman M.B., and Duffey S.S. Pharmacokinetics of chlorogenic acid and rutin in larvae of Heliothis zea. Journal of Insect Physiology 29 (1983) 295-300
29. Jeffries M. Evidence of induced plant defenses in a pondweed. Freshwater Biology 23 (1990) 265-270
30. Johnson K.S. Plant phenolics behave as radical scavengers in the context of insect (Manduca sexta) hemolymph and midgut fluid. Journal of Agricultural and Food Chemistry 53 (2005) 10120-10126
31. Johnson K.S., and Barbehenn R.V. Oxygen levels in the gut lumens of herbivorous insects. Journal of Insect Physiology 46 (2000) 897-903
32. Johnson K.S., and Felton G.W. Physiological and dietary influences on midgut redox conditions in generalist lepidopteran larvae. Journal of Insect Physiology 42 (1996) 191-198
33. Johnson K.S., and Felton G.W. Potential influence of midgut pH and redox potential on protein utilization in insect herbivores. Archives of Insect Biochemistry and Physiology 32 (1996) 85-105
34. Johnson R.L., Gross E.M., and Hairston Jr. N.G. Decline of the invasive submersed macrophyte Myriophyllum spicatum (Haloragaceae) associated with herbivory by larvae of Acentria ephemerella (Lepidoptera). Aquatic Ecology 31 (1998) 273-282
35. Krishnan N., and Kodrik D. Antioxidant enzymes in Spodoptera littoralis (Boisduval): are they enhanced to protect gut tissues during oxidative stress?. Journal of Insect Physiology 52 (2006) 11-20
36. Leu E., Krieger-Liszkay A., Goussias C., and Gross E.M. Polyphenolic allelochemicals from the aquatic angiosperm Myriophyllum spicatum L. inhibit photosystem II. Plant Physiology 130 (2002) 2011-2018
37. Lindroth R.L., and Peterson S.S. Effects of plant polyphenols on performance of southern armyworm larvae. Oecologia 75 (1988) 185-189
38. Lindsay W.L. Chemical Equilibria in Soils (1979), Wiley, New York, USA pp. 23-30
39. Lodge D.M. Herbivory on fresh-water macrophytes. Aquatic Botany 41 (1991) 195-224
40. Müller N., Hempel M., Philipp B., and Gross E.M. Degradation of gallic acid and hydrolysable polyphenols is constitutively activated in the freshwater plant-associated bacterium Matsuebacter sp. FB25. Aquatic Microbial Ecology 47 (2007) 83-90
41. Newman R.M. Herbivory and detritivory on fresh-water macrophytes by invertebrates: a review. Journal of the North American Benthological Society 10 (1991) 89-114
42. Newman R.M., Kerfoot W.C., and Hanscom Z.I. Watercress allelochemical defends high-nitrogen foliage against consumption: effects on freshwater invertebrate herbivores. Ecology 77 (1996) 2312-2323
43. Prusak A.C., O'Neal J., and Kubanek J. Prevalence of chemical defenses among freshwater plants. Journal of Chemical Ecology 31 (2005) 1145-1160
44. Revsbech N.P. An oxygen microsensor with a guard cathode. Limnology and Oceanography 34 (1989) 474-478
45. Ruuhola T., Tikkanen O.-P., and Tahvanainen J. Differences in host use efficiency of larvae of a generalist moth, Operophtera brumata on three chemically divergent Salix species. Journal of Chemical Ecology 27 (2001) 1595-1615
46. Salminen J.-P., and Lempa K. Effects of hydrolysable tannins on a herbivorous insect: fate of individual tannins in insect digestive tract. Chemoecology 12 (2002) 203-211
47. Schultz J.C., and Lechowicz M.J. Host plant, larval age, and feeding behavior influence midgut pH in the gypsy moth (Lymantria dispar). Oecologia 71 (1986) 133-137
48. Skibbe U., Christeller J.T., Callaghan P.T., Eccles C.D., and Laing W.A. Visualization of pH gradients in the larval midgut of Spodoptera litura using P-31-NMR microscopy. Journal of Insect Physiology 42 (1996) 777-790
49. Smolders A.J.P., Vergeer L.H.T., van der Velde G., and Roelofs J.G.M. Phenolic contents of submerged, emergent and floating leaves of aquatic and semi-aquatic macrophyte species: why do they differ?. Oikos 91 (2000) 307-310
50. Steinly B.A., and Berenbaum M. Histopathological effects of tannins on the midgut epithelium of Papilio polyxenes and Papilio glaucus. Entomologia Experimentalis Et Applicata 39 (1985) 3-9
51. Summers C.B., and Felton G.W. 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 Biochemistry and Molecular Biology 24 (1994) 943-953
52. Summers C.B., and Felton G.W. Peritrophic envelope as a functional antioxidant. Archives of Insect Biochemistry and Physiology 32 (1996) 131-142
53. Walenciak O., Zwisler W., and Gross E.M. Influence of Myriophyllum spicatum-derived tannins on gut microbiota of its herbivore Acentria ephemerella. Journal of Chemical Ecology 28 (2002) 2045-2056
54. Zimmer M. The fate and effects of ingested hydrolyzable tannins in Porcellio scaber. Journal of Chemical Ecology 25 (1999) 611-628