John P. Bryant

Resource Availability and Plant Antiherbivore Defense

The degree of herbivory and the effectiveness of defense varies widely among plant species. Resource availability in the environment is proposed as the major determinant of both the amount and type of plant defense. When resource are limited, plants with inherently slow growth are favored over those with fast growth rates; slow rates in turn favor large investments in antiherbivore defenses. Leaf lifetime, also determined by resource availability, affects the relative advantages of defenses with different turnover rates. Relative limitation of different resources also constrains the types of defenses. The proposals are compared with other theories on the evolution of plant defenses.

Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory

The evolutionary response of plants to herbivory is constrained by the availability of resources in the environment. Woody plants adapted to low-resource environments have intrinsically slow growth rates that limit their capacity to grow rapidly beyond the reach of most browsing mammals. Their low capacity to acquire resources limits their potential for compensatory growth which would otherwise enable them to replace tissue destroyed by browsing. Plants adapted to low-resource environments have responded to browsing by evolving strong constitutive defenses with relatively low ontogenetic plasticity. Because nutrients are often more limiting than light in boreal forests, slowly growing boreal forest trees utilize carbon-based rather than nitrogen-based defenses. More rapidly growing shade-intolerant trees that are adapted to growth in high-resource environments are selected for competitive ability and can grow rapidly beyond the range of most browsing mammals. Moreover, these plants have the carbon and nutrient reserves necessary to replace tissue lost to browsing through compensatory growth. However, because browsing of juvenile plants reduces vertical growth and thus competitive ability, these plants are selected for resistance to browsing during the juvenile growth phase. Consequently, early successional boreal forest trees have responded to browsing by evolving strong defenses during juvenility only. Because severe pruning causes woody plants to revert to a juvenile form, resistance of woody plants to hares increases after severe hare browsing as occurs during hare population outbreaks. This increase in browsing resistance may play a significant role in boreal forest plant-hare interactions. Unlike woody plants, graminoids retain large reserves of carbon and nutrients below ground in both low-resource and high-resource environments and can respond to severe grazing through compensatory growth. These fundamental differences between the response of woody plants and graminoids to vertebrate herbivory suggest that the dynamics of browsing systems and grazing systems are qualitatively different.

Effects of Severe Defoliation on the Long-Term Resistance to Insect Attack and on Leaf Chemistry in Six Woody Species of the Southern African Savanna

Severe defoliation as occurs in insect outbreaks can alter the chemistry and food value of woody-plant leaves for insects for several years after defoliation ceases. Two hypotheses, the active-defense hypothesis (AD) and the hypothesis of a carbon/nutrient balance (CNB), attempt to explain the mechanism of such responses to defoliation. We tested these hypotheses by studying the responses to severe defoliation by six southern African savanna woody species. Manual defoliation of the three fast-growing deciduous species we studied (Grewia flavescens, Acacia tortilis, Dichrostachys cinerea) resulted in increased resistance to insect attack in the next year. Concomitantly, nitrogen (N) and phosphorus (P) concentrations in leaves decreased and leaf total phenol and condensed tannin concentrations increased. The three slowly growing species that we studied (Burkea africana, Ochna pulchra, Euclea natalensis) responded differently to manual defoliation. In the year following defoliation, leaf resistance to insect attack declined, concentrations of total phenols and condensed tannin in leaves decreased, and concentrations of N and P increased. These opposite responses are consistent with the expectations of CNB rather than AD. We also found that defoliation of B. africana by caterpillars of one of its major defoliators, the saturniid moth Cirina forda, resulted in a greater loss of resistance than did manual defoliation of B. africana. This result further suggests that the AD does not apply to B. africana. We conclude that inherently slow growth constrains the long-term responses of woody plants to severe defoliation. Most of our results indicate that the CNB is a useful working model of woody-plant responses to defoliation. However, CNBs current emphasis on evergreenness as a control over the way slowly growing woody species respond to severe defoliation cannot explain our results. Thus, we suggest that a low photosynthetic capacity is also an important control over these responses.

Phytochemical deterrence of snowshoe hare browsing by adventitious shoots of four alaskan trees.

After snowshoe hares have severely browsed deciduous trees and shrubs, these woody plants produce adventitious shoots that are extremely unpalatable to them. The adventitious shoots of four common boreal forest trees contain significantly higher concentrations of terpene and phenolic resins than the mature-growth-form twigs of the same species. These resins are experimentally shown to be repellent to snowshoe hares and appear to explain the avoidance of adventitious shoots by hares. The production of adventitious shoots after intense hare browsing and the avoidance of these shoots by hares may play an important role in the 10-year hare cycle.

Regrowth and Palatability of Acacia Shoots Following Pruning by African Savanna Browsers

Stands of two species of African Acacia were monitored for 1 yr in a natural savanna ecosystem, to compare shoot regrowth and leaf chemistry in lightly browsed and heavily browsed trees. Where ungulates concentrated at a seasonal waterhole, A. nigrescens was more severely browsed than the thornier and finer leafed A. tortilis. Shoot regrowth in heavily browsed A. nigrescens more than compensated for herbivory, as net annual shoot extension was not significantly different from that in lightly browsed trees. Foliage of heavily browsed A. nigrescens was higher in nutrients and lower in condensed tannins than foliage of lightly browsed trees. We propose that severe pruning by browsing ungulates reduces intershoot competition for nutrients, promoting rapid shoot regrowth. Carbohydrate de- mands of rapid regrowth reduce carbon-based secondary metabolite synthesis. This results in patches of highly palatable browse that attract further browsing, generating a browsing- regrowth feedback loop. Such patches may be considered analogous to grazing lawns.

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.

Foliage acceptability to browsing ruminants in relation to seasonal changes in the leaf chemistry of woody plants in a South African savanna

SummaryWe investigated seasonal changes in food selection by hand-reared kudus and impalas in savanna vegetation in northern Transvaal, South Africa. The acceptability of the leaves of woody plants to these animals was compared with leaf concentrations of nutrients, fibre components and old leaf phenophases. No consistently significant correlation was found between acceptability and any single chemical factor. Based on an a priori palatability classification, discriminant function analysis separated relatively palatable species from unpalatable species in terms of a linear combination of protein and condensed tannin concentrations. The high acceptability of certain otherwise unpalatable species during the new leaf phenophase was related to elevation of protein levels relative to condensed tannin contents. Species were added to the diet during the dry season approximately in the order of their relative protein-condensed tannin difference.