Condensed tannins, attine ants, and the performance of a symbiotic fungus

Abstract

Field experiments indicate that the foliar concentration of condensed tannin affects the selection of leaf material ofInga oerstediana Benth., a tropical legume tree, by leaf cutter ants. In one study an increase in tannin concentration was correlated with a decrease in the acceptability of leaves to leaf-cutter ants, except at low tannin concentrations. Protein concentration was not correlated with acceptability nor was the ratio of protein to tannin. Results from a second study suggest that when the concentration of tannin was low the ants appear to select leaves on the basis of nutrient availability. Laboratory assays with the ants indicated that quebracho tannin, a commercially available condensed tannin, inhibits foraging ants. Again, at lower concentrations, quebracho tannin appeared to have little affect on the ants. The fungus the ants cultivate is a wood-rotting Basidiomycete that produces enzymes, such as polyphenol oxidase (PPO), that are capable of inactivating tannins. The activity of these PPOs may explain why leaf-cutter ants are undeterred by low concentrations of condensed tannins. I hypothesized that PPO activity would be absent from fungal cultures without tannin and that only high concentrations of tannin would inhibit the fungus. Cultures with and without tannin showed similar PPO activity. Thus PPO activity is constitutive. In fact, as fungal biomass increased, so did PPO activity. As hypothesized, only high concentrations of quebracho tannin inhibited PPO activity and fungal growth. However, it is not clear whether the ants can discriminate between concentrations that do and do not inhibit the fungus.

Soil bulk density effects on soil microbial populations and enzyme activities during the growth of maize (Zea mays L.) planted in large pots under field exposure

“…Urease, protease, and phosphatase (alkaline, pH 9.0 and acid, pH 5.0) were determined according to the methods described by Tabatabai (1982). Catalase activity was measured according to Roberge (1978), and polyphenol oxidase according to Nichols-Orians (1991). Controls were performed for all enzyme assays by the addition of substrate after incubation but prior to the analysis of the product (Dick et al 1988).…”

Diversity of Structure and Antiherbivore Activity in Condensed Tannins

“…The average effect of five different condensed tannins on Calligrapha verrucosa seemed to be greater than that on either of the two Chrysomela species (Tables 4-5). Laboratory rats appear to be more resistant to the effects of tannins than other rodents, mule deer appear more resistant than some other ruminants, and a browsing marsupial is more resistant than a grazing marsupial (Robbins et al 1987b, 1991, McArthur and Sanson 1993b. Insects that feed on graminoids or herbaceous dicots (both typically low in tannin; Mole 1993) may be more susceptible to tannins than are other insects (Berenbaum 1980, Bernays et al 1980, Schultz 1989.…”

“…The formation of tannin-protein complexes could be limited by high gut pH (Berenbaum 1980, Felton andDuffey 1991), surfactants (Martin and Martin 1984, De Veau and Schultz 1992, Tugwell and Branch 1992, high concentrations of cations (Martin et al 1985), and gut redox potential (Appel and Martin 1990). The enzyme polyphenol oxidase (PPO) can inactivate tannins (Nichols-Orions 1991). In some insects, the peritrophic membrane acts as an ultrafilter for tannins Chamberlain 1980, Barbehenn andMartin 1992).…”

Laccase detoxification mediates the nutritional alliance between leaf-cutting ants and fungus-garden symbionts

“…Phytophagous fungi interacting with plant-feeding Hemiptera have been shown to neutralize phenolic plant defenses with polyphenol oxidases (20), and leaf-cutting ant cultivars are known to produce phenol-oxidizing enzymes (21,22) of the laccase subgroup of polyphenoloxidases (benzendiol oxygen oxidoreductase; synonyms: urishiol oxidase, p-diphenol oxidase, EC 1.10.3.2) (23). It was also shown experimentally that high concentrations of phenolic compounds discourage leaf cutting by Atta foragers and inhibit the growth of their L. gongylophorus gardens (21, 22), making it a reasonable conjecture that rapid and efficient phenol detoxification has been an important enabling factor for leafcutting ants to become dominant terrestrial herbivores in Central and South America.…”