Paul B. Reichardt

Diversity of structure and antiherbivore activity in condensed tannins

We characterized the structure of condensed tannins from 16 woody plant species (seven genera, six families) and determined their effects on six herbivorous insect species (four genera, two families). There were major differences in tannin structure, even between congeneric plant species. Condensed tannins differed markedly in their antiherbivore activity, averaged over these herbivores, and the herbivores differed in their sensitivity, averaged over these tannins. Furthermore, the same tannin can have different effects on different herbivores, presumably because of interactions between tannin structure and gut physiology. Results challenge the view that tannins provide an evolutionarily stable plant defense because of their uniform chemical properties. Condensed tannin can sometimes impact herbivore fitness through effects on survival and growth, but the largest effects in 45 insect–tannin combinations were less than that of many other plant metabolites at lower doses. Even at high doses, condensed tanni...

Effect of nitrogen fertilization upon the secondary chemistry and nutritional value of quaking aspen (Populus tremuloides Michx.) leaves for the large aspen tortrix (Choristoneura conflictana (Walker))

SummaryWe investigated the effects of nitrogen fertilization upon the concentrations of nitrogen, condensed tannin and phenolic glycosides of young quaking aspen (Populus tremuloides) leaves and the quality of these leaves as food for larvae of the large aspen tortrix (Choristoneura conflictana), a Lepidopteran that periodically defoliates quaking aspen growing in North America. Nitrogen fertilization resulted in decreased concentrations of condensed tannin and phenolic glycosides in aspen leaves and an increase in their nitrogen concentration and value as food for the large aspen tortrix. These results indicate that plant carbon/nutrient balance influences the quality of aspen leaves as food for the large aspen tortrix in two ways, by increasing the concentrations of positive factors (e.g. nitrogen) and decreasing the concentrations of negative factors (eg. carbon-based secondary metabolites) in leaves. Addition of purified aspen leaf condensed tannin and a methanol extract of young aspen leaves that contained condensed tannin and phenolic glycosides to artificial diets at high and low levels of dietary nitrogen supported this hypothesis. Increasing dietary nitrogen increased larval growth whereas increasing the concentrations of condensed tannin and phenolic glycosides decreased growth. Additionally, the methanol extract prevented pupation. These results indicate that future studies of woody plant/insect defoliator interactions must consider plant carbon/nutrient balance as a potentially important control over the nutritional value of foliage for insect herbivores.

Response of winter chemical defense in Alaska paper birch and green alder to manipulation of plant carbon/nutrient balance

SummaryPlant carbon/nutrient balance has been implicated as an important factor in plant defensive chemistry and palatability to herbivores. We tested this hypothesis by fertilizing juvenile growth form Alaska paper birch and green alder with N, P and N-plus-P in a balanced 2x2 factorial experiment. Additionally, we shaded unfertilized plants of both species. Fertilization with N and N-plus-P increased growth of Alaska paper birch, reduced the concentration of papyriferic acid in internodes and increased the palatability of birch twigs to snowshoe hares. Shading decreased birch growth, decreased the concentration of papyriferic acid in internodes and increased twig palatability. These results indicate that the defensive chemistry and palatability of winter-dormant juvenile Alaska paper birch are sensitive to soil fertility and shade. Conversely the defensive chemistry and palatability of green alder twigs to snowshoe hares were not significantly affected by soil fertility or shade. The greater sensitivity of Alaska paper birch defensive chemistry and palatability to snowshoe hares in comparison to green alder is in agreement with the hypothesis that early successional woody plants that are adapted to high resource availability are more plastic in their chemical responses to the physical environment than are species from less favorable environments.

Conditioned Flavor Aversion: A Mechanism for Goats to Avoid Condensed Tannins in Blackbrush

It has been hypothesized that herbivores instinctively avoid tannin-containing plant parts in response to the adverse effects of tannins on forage digestion. However, we found that goats learned to avoid condensed tannins (CTs) from blackbrush current seasons growth by associating the flavor of foods containing CTs with aversive postingestive consequences. The aversive consequences experienced by goats apparently are not related to digestion inhibition and may depend on the structure of CTs and on how CTs are bound with other cell constituents. These observations suggest several areas of inquiry related to the interaction between CTs and herbivores. A better understanding of the physiological effects of CTs and how herbivores perceive these effects is essential to our knowledge of chemically mediated interactions between plants and mammalian herbivores. With few exceptions, the effects of food flavor have not been separated from those associated with postingestive consequences, even though our data show that postingestive consequences strongly influence palatability. We also need to know how herbivores learn which plant species to eat and which to avoid while foraging in areas that contain a variety of plant species and parts with different kinds and concentrations of CTs. Condensed tannins are pervasive in nature and can defend plants from herbivory, but since many important forages contain high levels of tannins, the presence or absence of tannins per se does not reliably indicate food quality. To predict the ability of a tannin-producing plant to deter herbivores requires a full understanding of how changes in CT structure and binding affect herbivores.

Defense of winter-dormant Alaska paper birch against snowshoe hares

SummaryMature growth-phase internodes of Alaska paper birch (Betula resinifera) are preferred by the snowshoe hare (Lepus americanus) over juvenile growth-phase internodes due to the low food value of the latter. While the mature over juvenile preferencec cannot be explained by the levels of inorganic nutrients or gross chemical fractions (resins or phenols), it can be explained by the striking differences in secondary metabolites of the two growth phases. The principle compound which renders the juvenile phase internodes unpalatable is papyriferic acid, a triterpene which is a demonstrated feeding deterrent to snowshoe hares and which is present in juvenile internodes at concentrations 25 times greater than those in mature internodes.

Chemically mediated interactions between woody plants and browsing mammals.

A diverse array of secondary metabolites deters feeding by mammals on woody plants. However, not all secondary metabolites are equally deterrent and the potencies of these substances as antifeedants is related to their structures. Although the physiological reason underlying deterrence by secondary metabolites is not well understood, the available evidence indicates that toxicity is more important than digestion inhibition. Resource limitation influences the production of secondary metabolites by woody plants. Species that are adapted to unproductive habitats are more chemically defended than species that are adapted to productive habitats. Resource limitation also affects the phenotypic expression of chemical defense with nutrient stress favoring increased production of carbon-based secondary metabolites and reduced production of nitrogen-containing secondary metabolites. Light stress has the opposite effects on the production of these substances. Herbivory by mammals also affects the chemical defenses of woody plants. In some cases browsing results in increased defense and in others decreased defense. Three circumstances under which browsing by mammals can change the chemical defenses of woody plants are discussed.

Carbon/nutrient balance as a predictor of plant defense in Alaskan balsam poplar: Potential importance of metabolite turnover

SummaryThe carbon/nutrient balance hypothesis fails to correctly predict effects of fertilization and shading on concentrations of defensive metabolites in Alaskan balsam poplar (Populus balsamifera). Of six metabolites analyzed, only one responded in the predicted fashion to fertilization and one to shading. These results and those of other similar studies suggest that while the carbon/nutrient balance hypothesis may correctly predict the effects of fertilization and shading on the concentrations of metabolic “end products”, it fails for many metabolites because of the dynamics associated with their production and turnover. In metabolites that turn over, static concentration is a poor predictor of defensive investment.

Ecological implications of condensed tannin structure: A case study

Condensed tannins were isolated from bitterbnish (Purshia tridentata) and blackbrush (Coleogyne ramosissima). Structural analyses showed that both tannins were procyanidins of similar polymer length. The overall stereochemistries at C-3 and C-4, however, differed between the two tannins. These changes in stereochemistry resulted in blackbrush tannins being less preferred than bitterbrush tannins when offered to snowshoe hares (Lepus americanus). It is unlikely that differences in protein-precipitating abilities are the cause for the preference of the bitterbrush over the blackbrush tannins. Instead, we hypothesize that condensed tannins may be depolymerized and absorbed following ingestion. Differences in tannin structure can lead to different depolymerized products and rates of depolymerization, both of which may affect herbivore preferences.

Chemical model for short-term induction in quaking aspen (Populus tremuloides) foliage against herbivores

Simulated large aspen tortrix (Choristoneura conflictana) herbivory of quaking aspen (Populus tremuloides) induces significant increases in concentrations of two phenol glycosides, salicortin and tremulacin, in leaves within 24 hr. Crushing of leaf tissue, as must occur when aspen leaves are eaten by chewing insects such as the large aspen tortrix, results in conversion of salicortin and tremulacin to 6-hydroxy-2-cyclohexenone (6-HCH). Salicortin, tremulacin, 6-HCH, and its degradation product, catechol, are all toxic to the large aspen tortrix when fed on an artificial diet. These damage-induced chemical changes provide a plausible mechanism for short-term resistance induced in aspen leaves by insect herbivory.

Effects of Mineral Nutrition on Delayed Inducible Resistance in Alaska Paper Birch

In subarctic forests, birch (Betula) trees respond to severe (50-100%) manual defoliation by delayed inducible resistance (DIR). This plant response to defoliation is characterized by a decline in the nutritional quality of leaves for immature insects for several years after defoliation events, and concomitant changes in leaf chemistry that may be detrimental to insect nutrition, that is, a decline in leaf nitrogen and an increase in leaf phenols. Two explanations of delayed inducible resistance have been proposed. (1) The active defense response hypothesis claims that delayed inducible resistance is an active response to defoliation per se rather than merely a passive consequence of recovery from the stress of severe defoliation. (2) In contrast, the carbon-nutrient balance (CNB) hy- pothesis claims that delayed inducible resistance is caused by nutritional stress resulting from severe defoliation. We used two experiments to test these hypotheses. (1) In a three- way factorial field experiment we reared spear-marked black moth (Rheumaptera hastata) larvae on Alaska paper birch (B. resinifera) saplings that had experienced combinations of 100% manual defoliation and fertilization with N and P in previous years, and measured larval survival and pupal mass. In association with these measurements of larval perfor- mance, we assayed leaf condensed tannin levels and the concentrations of N and P in leaves, and correlated the results of these assays with larval performance. (2) In a laboratory experiment we tested the biological activity of condensed tannin and linalool, the major secondary metabolites of Alaska paper birch leaves, by treating leaves collected from previously undefoliated Alaska paper birch saplings with combinations of condensed tannin and linalool, and measuring the performance of spear-marked black moth larvae reared on these leaves. Our results supported predictions of the carbon-nutrient balance hypoth- esis. We found that fertilization with nitrogen, the nutrient limiting growth of Alaska paper birch in our study site, mitigated delayed inducible resistance, and that condensed tannin is likely to be the major chemical cause of delayed inducible resistance in Alaska paper birch. In our field experiment we also found that fertilization of Alaska paper birch with phosphorus, a nutrient that does not limit the growth of Alaska paper birch in our study site, affected levels of condensed tannin in leaves and the saplings defoliation history influenced this effect. Thus, future studies of the effects of mineral nutrition on secondary metabolite production by woody plants and their responses to herbivory should consider