Phyllis D. Coley

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.

Allocating Resources to Reproduction and DefenseNew assessments of the costs and benefits of allocation patterns in plants are relating ecological roles to resource use

M ost species of higher plants have qualitatively similar resource requirements for growth and reproduction (Chapin et al., p. 49, this issue). They differ, however, in the way they use resources to carry out three essential functions-reproduction, defense against herbivores, and growth. Each of these functions requires a complex set of resources, including carbon, nitrogen, and phosphorus, that make up the structures (leaves, stems, fruits, roots) associated with different functions. Variation in resource allocation occurs through differences in the chemical composition of structures, the relative mass of different structures or organs, and the relative numbers of different structures a plant produces. This variation occurs within individuals through time, within and among populations, and especially among species (Figure 1). Examinations of this variation cross many fields of ecology, including physiological studies of the relationship between structure and function in plants, biochemical studies of

Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense

SummaryGrowth, herbivory and defenses were studied for 41 common tree species in a lowland rainforest in Panama. Species represented a range of shade tolerance, but all individuals were measured in light gaps to control for environmental conditions and the availability of herbivores. Species growth rates and leaf lifetimes differed by almost 50-fold and were related to the degree of shade tolerance. Various measures of plant growth were significantly negatively correlated with an estimate of defense investment, and significantly positively correlated with rates of herbivory. Species with long-lived leaves had significantly higher concentrations of immobile defenses such as tannins and lignins. These data support current hypotheses that the intrinsic growth rate of a species evolutionarily determines the optimal amount and type of defense.

THE GROWTH-DEFENSE TRADE-OFF AND HABITAT SPECIALIZATION BY PLANTS IN AMAZONIAN FORESTS

Tropical forests include a diversity of habitats, which has led to specialization in plants. Near Iquitos, in the Peruvian Amazon, nutrient-rich clay forests surround nutrient-poor white-sand forests, each harboring a unique composition of habitat specialist trees. We tested the hypothesis that the combination of impoverished soils and herbivory creates strong natural selection for plant defenses in white-sand forest, while rapid growth is favored in clay forests. Recently, we reported evidence from a reciprocal-transplant experiment that manipulated the presence of herbivores and involved 20 species from six genera, including phylogenetically independent pairs of closely related white-sand and clay specialists. When protected from herbivores, clay specialists exhibited faster growth rates than white-sand specialists in both habitats. But, when unprotected, white-sand specialists outperformed clay specialists in white-sand habitat, and clay specialists outperformed white-sand specialists in clay habitat. Here we test further the hypothesis that the growth defense trade-off contributes to habitat specialization by comparing patterns of growth, herbivory, and defensive traits in these same six genera of white-sand and clay specialists. While the probability of herbivore attack did not differ between the two habitats, an artificial defoliation experiment showed that the impact of herbivory on plant mortality was significantly greater in white-sand forests. We quantified the amount of terpenes, phenolics, leaf toughness, and available foliar protein for the plants in the experiment. Different genera invested in different defensive strategies, and we found strong evidence for phylogenetic constraint in defense type. Overall, however, we found significantly higher total defense investment for white-sand specialists, relative to their clay specialist congeners. Furthermore, herbivore resistance consistently exhibited a significant trade-off against growth rate in each of the six phylogenetically independent species-pairs. These results confirm theoretical predictions that a trade-off exists between growth rate and defense investment, causing white-sand and clay specialists to evolve divergent strategies. We propose that the growth-defense trade-off is universal and provides an important mechanism by which herbivores govern plant distribution patterns across resource gradients.

Convergence in defense syndromes of young leaves in tropical rainforests

Abstract In tropical forests, the majority of damage by herbivores or pathogens occurs on young leaves, yet the patterns of damage and the factors that influence them are poorly known. By measuring damage throughout leaf development and maturation for five species in a Panamanian forest, we showed that leaf toughening, which only occurs over a few days once the leaf is fully expanded, is the main factor decreasing damage in mature leaves. Although rates of damage to young leaves are, on average, orders of magnitude greater than on mature leaves, there is significant interspecific variation in young leaf defenses and in damage rates. In a survey of 55 species of shade-tolerant plants, we found that each species only invested in a subset of the potential defensive mechanisms for young leaves. We measured rates of young leaf expansion, nitrogen content, delayed chloroplast development, synchrony of leaf production and rates of damage in the field. On a subset of 24 species, we also measured phenolic compounds, checked for the presence of saponins and alkaloids, and conducted bioassays using lepidopteran, coleopteran and orthopteran herbivores and four fungal pathogens to test for toxicity of young leaf extracts. Certain combinations of traits repeatedly co-occurred across unrelated species suggesting convergent evolution. We argue that selection has repeatedly led to tradeoffs among defenses such that species fall along an escape/defense continuum. At one extreme are species with a ‘defense’ strategy, which includes effective chemical defense, slow leaf expansion, normal greening and low rates of damage (less than 20% of the leaf area lost). At the other extreme are ‘escape’ species which have ineffective chemical defenses and, as a consequence, have high rates of leaf damage, >60% of leaf area lost during expansion. In partial compensation for ineffective chemical defense, these species have very rapid leaf expansion (doubling in area every day) which minimizes the window of vulnerability, delayed chloroplast development (white young leaves) which contain fewer resources, and synchronous leaf production to satiate herbivores. Thus, interspecific variation in young leaf damage rates is explained by differences in defense combinations along this escape/defense continuum. Because apparently beneficial traits such as effective chemical defense and rapid leaf expansion do not occur in the same species, we suggest that physiological constraints limit the defense combinations of any one species to a restricted subset of those observed. However, the defense and escape strategies do not represent different tradeoffs that have equal fitness, as species with the escape syndrome suffer much higher rates of damage. We hypothesize that the escape syndrome arose over evolutionary time among plants that failed to evolve effective secondary metabolites while herbivores succeeded in evolving adaptations to the chemistry of their host plant. Hence the defense syndrome should provide the greatest fitness, whereas the escape syndrome minimizes damage given the failure of the plant’s secondary metabolites to provide protection.

Costs and benefits of defense by tannins in a neotropical tree

SummaryThe costs and benefits of defense by tannins were investigated for a neotropical tree, Cecropia peltata L. (Moraceae). Seedlings of equal age were grown under uniform conditions in a greenhouse for 18 months. Within a plant, leaf tannin concentrations measured in different years were highly correlated. Tannin concentrations differed substantially among individuals; plants with high tannin content had lower damage levels in herbivory experiments. The effects of tannin on herbivory appeared to be dosage dependent. There was, however, a cost associated with tannin production in terms of reduced leaf production.

Possible Effects of Climate Change on Plant/Herbivore Interactions in Moist Tropical Forests

The interactions between plants and herbivores are key determinants of community structure world wide. Their role is particularly important in lowland tropical rain forests where rates of herbivory are higher, plants are better defended chemically and physically, and herbivores have specialized diets. In contrast to the temperate zone, most of the herbivory in the tropics occurs on ephemeral young leaves (>70%), which requires herbivores to have finely tuned host-finding abilities. As a consequence of these tight ecological and evolutionary linkages, the interplay between plants and herbivores in the tropics may be more susceptible to perturbations of climate change.Increases in global temperature, atmospheric CO2, and the length of the dry season are all likely to have ramifications for plant/herbivore interactions in the tropics. Here I extrapolate from our current and incomplete understanding of the mechanisms regulating plant/herbivore interactions and present a scenario for possible trends under a changing climate. Although elevated CO2 tends to enhance plant growth rates, the larger effects of increased drought stress will probably result in lower growth. In atmospheres experimentally enriched in CO2, the nutritional quality of leaves declines substantially due to a dilution of nitrogen by 10-30%. This response is buffered in plant species associated with nitrogen fixers. Elevated CO2 should also cause a slight decrease in nitrogen-based defenses (e.g., alkaloids) and a slight increase in carbon-based defenses (e.g., tannins). The most dramatic and robust predicted effect of climate change is on rates of herbivory. Lower foliar nitrogen due to CO2 fertilization of plants causes an increase in consumption per herbivore by as much as 40%, and unusually severe drought appears to cause herbivore populations to explode. In areas where elevated CO2 is combined with drying, rates of herbivory may rise 2-4 fold. The frequency of insect outbreaks is also expected to increase. Higher herbivory should further reduce plant growth rates, perhaps favoring plant species that are well-defended or fix nitrogen. The predicted increase in the number of herbivores is primarily due to relaxed pressure from predators and parasitoids. Elevated temperatures may increase herbivore developmental times, affording them partial escape from discovery by natural enemies, and drought appears to decimate parasitoid populations. The expected decline in parasitoid numbers may be due to direct effects of dry season drought or to the relative scarcity of herbivores during that period. As a consequence, the relative abundance of species will change, and overall biodiversity should decline.

The evolution of antiherbivore defenses and their contribution to species coexistence in the tropical tree genus Inga

Plants and their herbivores constitute more than half of the organisms in tropical forests. Therefore, a better understanding of the evolution of plant defenses against their herbivores may be central for our understanding of tropical biodiversity. Here, we address the evolution of antiherbivore defenses and their possible contribution to coexistence in the Neotropical tree genus Inga (Fabaceae). Inga has >300 species, has radiated recently, and is frequently one of the most diverse and abundant genera at a given site. For 37 species from Panama and Peru we characterized developmental, ant, and chemical defenses against herbivores. We found extensive variation in defenses, but little evidence of phylogenetic signal. Furthermore, in a multivariate analysis, developmental, ant, and chemical defenses varied independently (were orthogonal) and appear to have evolved independently of each other. Our results are consistent with strong selection for divergent defensive traits, presumably mediated by herbivores. In an analysis of community assembly, we found that Inga species co-occurring as neighbors are more different in antiherbivore defenses than random, suggesting that possessing a rare defense phenotype increases fitness. These results imply that interactions with herbivores may be an important axis of niche differentiation that permits the coexistence of many species of Inga within a single site. Interactions between plants and their herbivores likely play a key role in the generation and maintenance of the conspicuously high plant diversity in the tropics.

Causes and consequences of monodominance in tropical lowland forests

Tropical canopy dominance in lowland, well‐drained forests by one plant species is a long‐standing conundrum in tropical biology. Research now shows that dominance is not the result of one trait or mechanism. We suggest that the striking dominance of Gilbertiodendron dewevrei in the Ituri Forest of northeastern Congo is the result of a number of traits in adult trees that significantly modify the understory environment, making it difficult for other species to regenerate there. Adults cast deep shade that reduces light levels in the understory of the Gilbertiodendron forest to levels significantly lower than in the mixed‐species forest. Moreover, the monodominant forest has deep leaf litter that could inhibit the establishment of small‐seeded species, and the leaf litter is slow to decompose, potentially causing the low availability of nitrogen. We expect that juveniles of Gilbertiodendron may have an advantage in this environment over other species. In general, it appears that all tropical monodominant species share a similar suite of traits.

Dioecy and herbivory: the effect of growth rate on plant defense in Acer negundo

(...) Male trees had significantly faster growth rates than females. Leaf defense levels were estimated by measuring leaf characters, such as nitrogen and water content, toughness, tannins and total phenolic compounds. Female and male trees could be distinguished from one another using a discriminant function analysis based solely on leaf characters. Leaves from female trees were tougher than those from males, although no consistent differences were found between the sexes in other leaf characters. When all leaf characters were combined in a multiple regression, females were significantly better defended than males (...)