William J. Mattson

The dilemma of plants: To grow or defend.

Physiological and ecological constraints play key roles in the evolution of plant growth patterns, especially in relation to defenses against herbivores. Phenotypic and life history theories are unified within the growth-differentiation balance (GDB) framework, forming an integrated system of theories explaining and predicting patterns of plant defense and competitive interactions in ecological and evolutionary time. Plant activity at the cellular level can be classified as growth (cell division and enlargement) of differentiation (chemical and morphological changes leading to cell maturation and specialization). The GDB hypothesis of plant defense is premised upon a physiological trade-off between growth and differentiation processes. The trade-off between growth and defense exists because secondary metabolism and structural reinforcement are physiologically constrained in dividing and enlarging cells, and because they divert resources from the production of new leaf area. Hence the dilemma of plants: They must grow fast enough to complete, yet maintain the defenses necessary to survive in the presence of pathogens and hervivores. The physiological trade-off between growth and differentiation processes interacts with herbivory and plant-plant competition to manifest itself as a genetic trade-off between growth and defense in the evolution of plant life history strategies. Evolutionary theories of plant defense are reviewed. We also extend a standard growth rate model by separating its ecological and evolutionary components,and formalizing the role of competition in the evolution of plant defense. We conclude with a conceptual model of the evolution of plant defense in which plant physioligical trade-offs interact with the abiotic environment, competition and herbivory.

The Role of Drought in Outbreaks of Plant-eating Insects

Substantial evidence indicates that drought stress promotes outbreaks of plant-eating (phytophagous) fungi and insects. Observations and experiments show that colonization success and pervalence of such fungi as root and stalk rots, stem cankers, and sometimes wilts and foliar diseases are much higher on water-stressed plants than on normal plants (Schoeneweiss 1986). The evidence associating insects and drought is more circumstantial, consisting largely of observations that outbreaks around the world of such insects as bark beetles and leaf feeders (see Table 1) are typically preceded by unusually warm, dry weather. There is also a consistent, positive correlation between insect oubreaks and dry, nutrient-poor sites (Mattson and Haack 1987).

Invasion of North American Forests by European Phytophagous Insects Legacy of the European crucible

Over the last 500 years, nearly 2000 insects and 2000 weedy plants have invaded North America (Kim and McPheron 1993, Sailer 1983, Stuckey and Barkley 1993). Many of these inadvertent immigrants have become serious agricultural or forest pests (Liebhold et al. 1995, Wilson and Graham 1983). Kim and McPheron (1993) calculated that 40% of the major North American insect pests are of exotic origin even though as a group exotic insects constitute just 2% of the insect fauna. For example, Haack and Mattson (1993) discovered that alien, tree-feeding sawflies in North America are more prone to cause outbreaks than are the equivalent native species. Questions about managing these introduced insect species and concern about continued importation of new ones are timely because of the past severe and everspreading impacts of introduced insect pests on North American forest ecosystems (Campbell and Schlarbaum 1994, Liebhold et al. 1995). We have only begun to comprehend the manifold, often insidious effects of alien invaders on the

Defensive Strategies of Woody Plants Against Different Insect-Feeding Guilds in Relation to Plant Ecological Strategies and Intimacy of Association with Insects

A major question confronting scientists who want to exploit plant resistance in the management of a particular insect or pathogen pest is whether the plant in question has any exploitable resistance, and if so, what are the likely resistance mechanisms (Harris 1980, 1982). This question is not trivial because its answer affects the entire research approach--how to search for resistance. To this end, we offer here, a framework for classifying defensive strategies by certain classes of plants against various feeding guilds of herbivores.

Few immigrant phytophagous insects on woody plants in Europe: legacy of the European crucible?

Exotic phytophagous insects are invading forest ecosystems worldwide. So far, 109 invasive insects on woody plants, 57 from North American (NA), and 52 from Asia (A) have established populations in European forests. Four orders account for about 84% of the immigrants: Homoptera 39%, Lepidoptera 13%, Coleoptera 19%, and Hymenoptera 13%. The majority of these invasive species (63% of NA and 77% of A) live on deciduous trees, of which 36% have been introduced from NA and Asia. The remaining insect species (37% NA and 25% A) live on various conifers, of which 53% have also been introduced. Most (57%) of the NA insects feeding on coniferous plants live upon their introduced, native host plants. These data suggest that many NA immigrant phytophagous species in Europe have been successful in establishing permanent populations because their native hosts preceded or accompanied them into Europe and/or were asexually reproducing species. We propose that fewer invasive phytophagous insects have become established in European compared to North American woodlands because of the unique legacy of the European Pleistocene/Holocene crucible (i.e. endless cycles of populations contracting into highly disparate, dispersed metapopulation refugia and eventually expanding out of them) on European species and ecosystems that caused highly diminished heterogeneity. This translates to fewer and less penetrable tri-trophic niches in Europe due to fewer and less available host plants, but greater zootic resistance per niche derived from more competition-hardened competitors and possibly natural enemies. Moreover, many European species are probably superior invasion specialists because the crucible favored traits that are conducive to success in highly subdivided, and extinction-prone metapopulations: asexual reproduction, polyploidy, and other traits especially conducive to persistence under stress, and explosive growth/spread under amelioration.

Considering the nutritional ecology of the spruce budworm in its management

To successfully manage spruce budworm (Choristoneura fumiferana (Clemens)) populations, we need more knowledge about the insects nutritional ecology. Here we address this issue by considering variations in host suitability for the budworm due to tree species, age, nutrient levels, defensive compounds, inducible defenses, and stress. Tree age has minor effects on foliar nutritional quality. Nitrogen levels (as an index of protein) in the diet appear to be the most significant factor affecting performance both in the field and laboratory. Tannins/phenolics, and supraoptimal levels of calcium in host foliage may interfere with the bioavailability of some minerals such as iron. Monoterpenes can be toxic at very high levels but otherwise seem to have minor negative effects on budworm performance. There is little evidence of short-term inducible defenses in fir foliage. Likewise, there is little evidence that drought stress makes fir trees more nutritionally favorable for spruce budworm. However, drought-induced flowering may be very important to larval survival. Neither is there evidence for substantial variation among trees in their inherent susceptibility to budworm. We hypothesize that variations in host-plant quality are less important in regulating budworm dynamics than other factors, such as the physical environment and natural enemies. However, spruce-budworm/host-plant phenological synchrony and host flowering status may be very important variables that deserve more research. Management of budworm will require more detailed knowledge about the entire complex of community factors that contribute to the increased likelihood of outbreak development.

Plant growth and defense

In their review of the growth-differentiation balance hypothesis (GDBH), Lerdau et al.1 misrepresent the general model of plant defense outlined in our review*. They fault the model as a ‘source-driven GDBH model’ which ‘predicts allocation of carbon to terpenes based on resources’ rather than a ‘demand-side model’, which ‘str&sses how allocation varies in response to phenological or herbivory demands’. This IS not the case. In fact, our model is very highly ‘demand-side’, with explicit emphasis on the adaptive evolution of phenotypic plasticity m, and interspeclfic patterns of, growth and secondary metabolism. Herbivores create the demand for defense, and competitors create the demand for growth. Lerdau et al. failed to distinguish between the original concept of growth-differentiation balance proposed by Loomis3 and our integration of these constraints with optimal defense theory. Loomis predicts trade-offs between growth and secondary metabohsm because (1) ontogenetlc constraints limit secondary metabolism in developing cells, and (2) resource demands of growth limit secondary metabolism at the whole-plant level. While the success of a parficular resource allocation strategy IS environmentally dependent, our model assumes explicitly that ‘the importance of herbivory can vary within an environment independently of resource availability’. There are no Inherent constraints that limit secondary metabolism in resource-rich environments as there are on growth in resourcelimited environments. But many studies show plants to increase their growth in response to resource enrichment. We argue this to be adaptive, the result of strong demand for growth created by competitors that would otherwise usurp the plant’s resources. It is only because plants grow that secondary metabolism IS constrained. Chemical defense diverts resources from growth, thus any benefit derived from Increased secondary metabohsm must exceed this opportunity cost. Induced resistance IS a defensive adaptation with a particularly high benefit:cost ratio. We review the (scant) evidence that GDB constraints apply to induced. as well as constitutive, secondary metabolism. Lerdau et ai. argue that analysis of seasonal patterns of growth and secondary metabolism within an individual is ideal for testing the GDEH, and the frequent observation that expanding leaves have both the highest growvl rates and the highest concentrations of secondary metabolites IS Inconsistent with the GDBH. We disagree. Secondary metabolism by mature cells withln Immature leaves is not mconslstent with constraints on secondary metabolism in immature cells. We review some of the developmental ‘tricks’ plants use to overcome this constraint. Furthermore, such phenological correlations Ignore the opportunity cost of secondary metabolism resulting from resource trade-offs at the whole-plant level. While high concentrations

Physical effects of weather events on the abundance and diversity of insects in North American forests

We summarize the effects of major weather events such as ice storms, wind storms, and flooding on the abundance and diversity of terrestrial forest insects and their allies. This synthesis indicates that weather events influence both spatial and temporal patterns of forests and insect communities in North American landscapes. The Atlantic and Pacific oceanic sides of the continent are relatively more susceptible to ice and wind storms, respectively. There have been more studies and reports on the responses of forest insects to wind storms, and on economically important subcortical insects than on gall-forming, foliage-feeding, fungal-feeding, litter-dwelling, pollinating, parasitizing, predaceous, root-feeding, and sap-feeding insects. Weather events positively affect populations of subcortical insect species, and impact their colonization patterns and dynamics. Species belonging to genera such as Dendroctonus (Scolytidae) and Monochamus (Cerambycidae) may sometimes cause economic damage by colonizing res...

The Spruce Budworm in Eastern North America

The spruce budworm, Choristoneura fumiferana (Clemens), (Lepidoptera: Tortricidae) was first described from specimens collected in Virginia,17 but this native insect occurs primarily in the northern boreal forest from Newfoundland west to the McKenzie River near 66°N.53 The most extensive and destructive outbreaks have occurred in the maritime provinces (New Brunswick, Nova Scotia, Newfoundland), Quebec, Ontario, Maine, and the Great Lakes states. This defoliator feeds primarily on the new growth of balsam fir (Abies balsamea), red spruce (Picea rubens), white spruce (Picea glauca), and black spruce (Picea mariana). Sometimes it feeds on other conifers, such as eastern larch (Larix lancina), eastern hemlock (Tsuga canadensis), Engelmann spruce (Picea engelmannii), subalpine fir (Abies lasiocarpa), and eastern white pine (Pinus strobus).28,47

Symposium on Agroacoustics: Ultrasonic Acoustical Emissions from Sapwood of Eastern White Pine, Northern Red Oak, Red Maple, and Paper Birch: Implications for Bark- and Wood-Feeding Insects

Ultrasonic acoustical emissions (AEs) were recorded from trunk samples of eastern white pine, Pinus strobus L., northern red oak, Quercus rubra L., paper birch, Betula papyrifera Marsh., and red maple, Acer rubrum L., that were cut in winter (February) and allowed to dry indoors. Emission rates were determined for waxed and unwaxed samples at weekly intervals throughout the drying period. Waveform parameters determined for each AE were duration, counts (oscillations above threshold), rise time, amplitude, energy, and average frequency (counts/duration). For all tree species, AE rates from unwaxed samples first increased and then decreased during drying, and they were several times greater than rates for waxed samples. For white pine, mean duration, counts, rise time, amplitude, and energy decreased over time while average frequency increased. Such patterns were often lacking among the three hardwood species. Average waveform parameters differed among species; AEs from white pine were strongest while those from red oak were weakest. Implications for bark- and wood-boring insects are discussed.