Rex G. Cates

The Role of Carbon-Based Plant Secondary Metabolites in Decomposition in Terrestrial Ecosystems

Litter decomposition in terrestrial habitats is affected by many factors, including temperature, moisture, and nutrient and organic composition of litter. Among organic components, lignin is the primary controlling factor of decomposition rates of surface litter during the later phase of decomposition in most habitats and during the initial phase in warm, moist habitats (i.e., those with a high actual evapotranspiration, AET). In habitats with moderate AETs, we suggest that the decreased control by lignin over annual decomposition rates of surface litter is due, at least in part, to a significant periodic or seasonal influence of other carbonbased plant secondary metabolites over rates in the initial phase of decomposition. The influence of other secondary metabolites over decomposition rates should be a function of other correlates of AET: the phytochemical composition of the community and the persistence of various secondary metabolites in litter. As AET decreases from the highest extreme, we expect more, but perhaps short-term seasonal, influence of monomeric phenolics and tannins. In warm, dry environments with still-lower AETs, we expect some control by terpenes. On an annual basis, the relative influence of components other than lignin should therefore increase with decreasing AET, and the influence of lignin content alone on decomposition rates of surface litter should be reduced proportionately. Effects of these various classes of compounds should exhibit different temporal patterns in litter and soil. Complexity is added to this model by the multifarious effects of stress on the production of specific secondary metabolites, the changes that occur in secondary-metabolite composition during senescence of tissues, and the differential effects of specific secondary metabolites on decomposition.

Influence of balsam poplar tannin fractions on carbon and nitrogen dynamics in Alaskan taiga floodplain soils

The feedbacks between plant and soil processes play an important role in driving forest succession. One poorly understood feedback mechanism is the interaction between plant secondary chemicals and soil microbes. In the Alaskan taiga, changes in nutrient cycling caused by balsam poplar (Populus balsamifera) secondary chemicals may affect the transition from alder (Alnus tenuifolia) to balsam poplar on river floodplains. We examined the effects of four poplar condensed tannin fractions on N cycling in alder and poplar soils. Tannins were added to forest floor samples from both poplar and alder sites. Samples were incubated for 1 month in the laboratory with soil respiration rates measured over the course of the incubation. At the end of the incubation we measured both net and gross nitrogen mineralization and nitrification, microbial biomass C and N, and the activity of various exoenzymes. In all soils, tannin additions reduced N availability, however, the mechanisms differed depending on the molecular weight of the tannin and the native soil microbial community. Low molecular weight tannin fractions served as a labile C source in poplar Oi, poplar Oe, and alder Oe horizons but were toxic to microbes in alder Oi. High molecular weight tannin fractions appeared to act primarily by binding extracellular substrates and thus limiting C and N mineralization, with the strongest effects observed in the alder soils.

The role of balsam poplar secondary chemicals in controlling soil nutrient dynamics through succession in the Alaskan taiga.

The vegetation mosaic of the Alaskan taiga is produced by patterns of disturbance coupled to well-defined successional patterns. In primary succession on river floodplains, one of the critical transitions in succession is that from thinleaf alder (Alnus tenuifolia) to balsam poplar (Populus balsamifera). This is the shift from a N2-fixing shrub to a deciduous tree. Through this transition there are major changes in N cycling including a decrease in N2-fixation, mineralization, and nitrification. Most models of plant effects on soil processes assume that these changes are caused by shifts in litter quality and C/N ratio. This paper reviews several studies examining the effects of balsam poplar secondary chemicals on soil nutrient cycling. Balsam poplar tannins inhibited both N2-fixation in alder, and decomposition and N-mineralization in alder soils. Other poplar compounds, including low-molecular-weight phenolics, were microbial substrates and increased microbial growth and immobilization, thereby reducing net soil N availability. Thus, substantial changes in soil N cycling through succession appear to have been mediated by balsam poplar secondary chemicals.

Responses of the western spruce budworm to varying levels of nitrogen and terpenes

SummaryAn agar diet study using western spruce budworm populations from Idaho and New Mexico was carried out to determine the effects of varying concentrations of nitrogen, beta-pinene, and bornyl acetate on larval growth and survival. Increased availability of nitrogen resulted in increased larval growth rate and survival to the adult stage. Larval growth rates from the Idaho population were higher on the high-nitrogen diet than were growth rates from the New Mexico population. The high level of beta-pinene improved larval growth at the high-nitrogen concentration. Bornyl acetate significantly reduced larval growth at both the low and high levels of nitrogen although the effect was greatest with the high-nitrogen diet. High bornyl acetate concentrations also significantly reduced survival to the adult stage. At high-nitrogen levels, a high concentration of bornyl acetate reduced larval growth rates and adult survival to a level similar to that occurring at the low nitrogen and low bornyl acetate concentrations.

Arthropod dynamics on sagebrush (Artemisia tridentata): effects of plant chemistry and avian predation

We conducted a field experiment to assess interrelationships between leaf- tissue secondary chemistry, avian predation, and the abundance and diversity of arthropods occurring on sagebrush (Artemisia tridentata) in central Oregon. Arthropods were removed from individual shrubs, some of which were then caged to exclude birds. Secondary chem- istry and arthropods were sampled at intervals up to 56 wk following the defaunation/ caging treatment. Recovery rates differed among arthropod taxa and functional groups. Several sap- sucking homopterans and hemipterans reached control levels within 2-4 wk of the treat- ment, whereas abundances ofparasitoids and predators recovered to match control numbers only 6 wk after defaunation. Abundances of several herbivorous leaf-chewing taxa (pri- marily lepidopteran larvae) remained significantly depressed even 56 wk after the treatment. Fungivores (oribatid mites) reached greater abundances on defaunated than on control shrubs by the end of the experiment. There were also significant changes in the concen- trations or frequency of occurrence of several chemical compounds following the defauna- tion treatment. Several hydrocarbons, sesquiterpenes, and monoterpenes that were present in most shrubs exhibited sharply reduced concentrations in leaf tissues within 4 wk of the treatment, whereas some alcohols and ketones (linalool, borneol, thujone), which occurred at relatively low frequencies among control plants, increased dramatically in their fre- quencies of occurrence following arthropod removal. Both changes persisted for the du- ration of the experiment. We found several significant associations between the abundance or occurrence of arthropod taxa or groups and concentrations or frequencies of secondary compounds, but these were most prevalent among the leaf-chewing lepidopterans. We suggest that the shrubs responded to the removal of herbivorous, leaf-chewing arthropods by altering chemical allocation patterns; the changes in chemistry persisted for over a year because recolonization of the defaunated plants by these herbivores was slow. Effects of the caging treatment were much less obvious. The recovery of the diversity of arthropods known to constitute prey for birds in this system was slower on shrubs

Flowering in males and females of a Utah willow, Salix regida and effects on growth, tannins, phenolic glycosides and sugars.

We manipulated resource allocation to reproduction in male and female Salix rigida by removing reproductive buds before expansion, and female flowers before fruit initiation. We documented a significant difference between fruiting and flowering females. Fruiting females produced smaller shoots, fewer reproductive buds and had lower concentrations of salicortin and tannins than females in the flower-removal treatment. No effect of treatment on growth and secondary metabolites was detected among males. Female controls produced less shoot biomass and fewer reproductive buds than male controls (...)

The Role of Mixtures and Variation in the Production of Terpenoids in Conifer-Insect-Pathogen Interactions

The regulation of natural populations was debated intensively during the 1950s and 1960s, and continues to be an important topic of investigation. Although several treatises on this subject could be cited, one of the most important to the area of plant-herbivore-pathogen interactions was published by Hairston, Smith, and Slobodkin.1 In this stimulating paper the authors put forward three tenants, the third of which states that “Herbivores are seldom food-limited, appear most often to be predator-limited, and therefore are not likely to compete for common resources.” Contributing to this conclusion is the disparity between plants and herbivores in mobility, generation times, and the ability of insects and pathogens to adapt to host trees. Generation times of the myriad of insect herbivores that use woody plants are short, and the insects are highly mobile and depend upon host plants for most life processes.2 Alternatively, woody perennials are long-lived, immobile, and seemingly at the mercy of their natural enemies. This explicit yet sweeping scenario provided a major impetus toward investigations that have led to our current knowledge of plant-herbivore-pathogen interactions at the population, community, and ecosystem levels. Five years later a seminal paper by Ehrlich and Raven3 enhanced the field of plant-herbivore interactions and chemical ecology with a provocative discussion of the coevolution between butterflies and host plants. Now the field has advanced to investigations at the tritrophic level; and the linking thread among tritrophic interactions is to a large extent the natural products produced by plants.4

Foliage constituents of douglas fir (Pseudotsuga menziesii (Mirb.) Franco (Pinaceae)): Their seasonal variation and potential role in douglas fir resistance and silviculture management.

Seasonal changes in the production of primary nutrients (soluble carbohydrates) and secondary metabolites (terpenes, monomeric phenolics, and tannins) in the current needle tissue of Douglas fir were investigated. All four classes of compounds showed significant seasonal changes in concentration during foliage development. Most terpenes increased significantly in concentration from June 11 to August 3, and then showed declining concentrations to September 20. The most dramatic and significant seasonal increases occurred inα-pinene, camphene, and bornyl acetate concentrations. The monomeric phenolics chlorogenic acid, taxifolin glucoside, quercetin galactoside, and those unknown phenolics showed an overall trend of declining in concentration from June 11 through September 20. However, considerable variation between sampling dates in the concentration of these phenolics was noted. Tannin concentration decreased significantly from June 11 to July 9, and then increased in concentration to the September 20 sampling date. Fructose, galactose, glucose, and sucrose tended to decrease from June 11 to September 20. However, significant variation between sampling dates was evident in these compounds as well. Galactose was the major compound in the soluble carbohydrate fraction, amounting to almost 80% of the total concentration throughout the growing season. These data suggest that if phenolics and tannins function as defenses, they would only affect second- and possibly third-instar budworm larvae during the time that these instars mine the buds. Camphene,α-pinene, and bornyl acetate increased in concentration throughout the growing season and may be effective deterrents to the budworm. Both bornyl acetate and camphene have been shown in field and laboratory studies to increase larval mortality and adversely affect budworm larval growth. Carbohydrates generally act as nutrients that enhance herbivore growth. However, in a previous study, galactose was found to cause reduced budworm larval growth and increased larval mortality.

Effects of terpenes and phenolic and flavonoid glycosides from Douglas fir on western spruce budworm larval growth, pupal weight, and adult weight

Monoterpenes, sesquiterpenes, and phenolic and flavonoid glycosides typical of the current years foliage of Douglas fir (Pseudotsuga menziesii) were bioassayed using agar diets to determine the effect of these compounds on natural and colony populations of western spruce budworm (Choristoneura occidentalis). Several terpenes adversely affected budworm larval growth, supporting previous field and laboratory studies. However, larvae collected from a population in southeastern Idaho were significantly more tolerant of the monoterpenes than those from a Montana population. For the Montana population, agar diet studies showed that camphene, myrcene, terpinolene, bornyl acetate, and tricyclene adversely affected larval growth rate and pupal weight. For the Idaho population, agar diet studies showed that only terpinolene and bornyl acetate adversely affected larval growth and pupal weights. For both populations bornyl acetate was the most toxic, and this compound in addition to other monoterpenes represent defensive mechanisms in the current years growth of Douglas fir. Sesquiterpene and phenolic-flavonoid glycoside fractions extracted from Douglas fir current years growth also were bioassayed using agar diets. The sesquiterpene fraction showed a significant negative effect on budworm larval growth, but phenolics and flavonoid glycosides had no effect. Sesquiterpenes, in combination with tricyclene, camphene, myrcene, limonene, terpinolene, and the acetate fraction appear to represent an effective mixture of defensive compounds against the budworm.

Role of Douglas fir (Pseudotsuga menziesii) carbohydrates in resistance to budworm (Choristoneura occidentalis)

The current years growth of Douglas fir contains galactose, unusual in that this carbohydrate makes up 78.7% of the total carbohydrate fraction. An agar diet study was undertaken to determine the effects of galactose, other carbohydrates, and terpenes on western spruce budworm larval mortality, growth rate, and adult biomas production. All concentrations of the carbohydrates and terpenes tested, as well as other mineral elements not tested, were typical of the current years foliage of Douglas fir. In experiment I, the diet containing 5.61% total carbohydrate did not significantly affect larval mortality when compared to the control diet. However, diets containing 9.45% and 15% total carbohydrate concentrations significantly increased larval mortality 64% and 96.1%, respectively, when compared to the control. Also in experiment I, terpenes alone (78.9% morality) and terpenes in combination with 9.45% and 15% total carbohydrates significantly increased larval mortality (97.2% and 100%, respectively) when compared to mortality on the control diet (44%). To determine which carbohydrate was causing the adverse effect, 6% glucose, 6% fructose, and 6% galactose were placed individually and in combination with terpenes in diets in experiment II. The 6% galactose diet significantly increased larval mortality and reduced growth rate when compared to the control, glucose, and fructose diets. Glucose resulted in 16% less larval mortality, significantly enhanced female larval growth rate and pupal weight, but did not affect male larval growth rate and pupal weight, when compared to the control. Fructose resulted in a significant decrease in larval mortality and a general trend of enhanced female and male larval growth rate and pupal weight. Larval mortality on terpenes alone was not significantly different from the control, but terpenes with 6% galactose increased larval mortality and decreased female and male growth rate and pupal weight significantly when compared to glucose-terpene and fructose-terpene diets. No significant interactions were found between carbohydrates and terpenes in either experiment.