Thomas A. Kursar

Drought sensitivity shapes species distribution patterns in tropical forests.

Although patterns of tree species distributions along environmental gradients have been amply documented in tropical forests, mechanisms causing these patterns are seldom known. Efforts to evaluate proposed mechanisms have been hampered by a lack of comparative data on species’ reactions to relevant axes of environmental variation. Here we show that differential drought sensitivity shapes plant distributions in tropical forests at both regional and local scales. Our analyses are based on experimental field assessments of drought sensitivity of 48 species of trees and shrubs, and on their local and regional distributions within a network of 122 inventory sites spanning a rainfall gradient across the Isthmus of Panama. Our results suggest that niche differentiation with respect to soil water availability is a direct determinant of both local- and regional-scale distributions of tropical trees. Changes in soil moisture availability caused by global climate change and forest fragmentation are therefore likely to alter tropical species distributions, community composition and diversity.

Host specificity of Lepidoptera in tropical and temperate forests

For numerous taxa, species richness is much higher in tropical than in temperate zone habitats. A major challenge in community ecology and evolutionary biogeography is to reveal the mechanisms underlying these differences. For herbivorous insects, one such mechanism leading to an increased number of species in a given locale could be increased ecological specialization, resulting in a greater proportion of insect species occupying narrow niches within a community. We tested this hypothesis by comparing host specialization in larval Lepidoptera (moths and butterflies) at eight different New World forest sites ranging in latitude from 15° S to 55° N. Here we show that larval diets of tropical Lepidoptera are more specialized than those of their temperate forest counterparts: tropical species on average feed on fewer plant species, genera and families than do temperate caterpillars. This result holds true whether calculated per lepidopteran family or for a caterpillar assemblage as a whole. As a result, there is greater turnover in caterpillar species composition (greater β diversity) between tree species in tropical faunas than in temperate faunas. We suggest that greater specialization in tropical faunas is the result of differences in trophic interactions; for example, there are more distinct plant secondary chemical profiles from one tree species to the next in tropical forests than in temperate forests as well as more diverse and chronic pressures from natural enemy communities.

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.

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.

The global distribution of diet breadth in insect herbivores

Significance Dietary specialization determines an organism’s resource base as well as impacts on host or prey species. There are important basic and applied reasons to ask why some animals have narrow diets and others are more generalized, and if different regions of the Earth support more specialized interactions. We investigated site-specific host records for more than 7,500 species of insect herbivores. Although host specialists predominate, the proportion of specialists is affected by the diversity of hosts and shifts globally, supporting predictions of more exclusive tropical interactions. These results not only affect our understanding of the ecology of food webs, but also have implications for how they respond to environmental change, as well as for ecosystem management and restoration. Understanding variation in resource specialization is important for progress on issues that include coevolution, community assembly, ecosystem processes, and the latitudinal gradient of species richness. Herbivorous insects are useful models for studying resource specialization, and the interaction between plants and herbivorous insects is one of the most common and consequential ecological associations on the planet. However, uncertainty persists regarding fundamental features of herbivore diet breadth, including its relationship to latitude and plant species richness. Here, we use a global dataset to investigate host range for over 7,500 insect herbivore species covering a wide taxonomic breadth and interacting with more than 2,000 species of plants in 165 families. We ask whether relatively specialized and generalized herbivores represent a dichotomy rather than a continuum from few to many host families and species attacked and whether diet breadth changes with increasing plant species richness toward the tropics. Across geographic regions and taxonomic subsets of the data, we find that the distribution of diet breadth is fit well by a discrete, truncated Pareto power law characterized by the predominance of specialized herbivores and a long, thin tail of more generalized species. Both the taxonomic and phylogenetic distributions of diet breadth shift globally with latitude, consistent with a higher frequency of specialized insects in tropical regions. We also find that more diverse lineages of plants support assemblages of relatively more specialized herbivores and that the global distribution of plant diversity contributes to but does not fully explain the latitudinal gradient in insect herbivore specialization.

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.

Drought effects on seedling survival in a tropical moist forest

The amount and seasonality of rainfall varies strongly in the tropics, and plant species abundance, distribution and diversity are correlated with rainfall. Drought periods leading to plant stress occur not only in dry forests, but also in moist and even wet forests. We quantified experimentally the effect of drought on survival of first year seedlings of 28 co-occurring tropical woody plant species in the understory of a tropical moist forest. The seedlings were transplanted to plots and subjected to a drought and an irrigation treatment for 22 weeks during the dry season. Drought effects on mortality and wilting behavior varied greatly among species, so that relative survival in the dry treatment ranged from 0% to about 100% of that in the irrigated treatment. Drought stress was the main factor in mortality, causing about 90% (median) of the total mortality observed in the dry treatment. In almost half of the species, the difference in survival between treatments was not significant even after 22 weeks, implying that many of the species are well adapted to drought in this forest. Relative drought survival was significantly higher in species associated with dry habitats than in those associated with wet habitats, and in species with higher abundance on the dry side of the Isthmus of Panama, than in those more abundant on the wet side. These data show that differential species survival in response to drought, combined with variation in soil moisture availability, may be important for species distribution at the local and regional scale in many tropical forests.

Desiccation Tolerance of Five Tropical Seedlings in Panama. Relationship to a Field Assessment of Drought Performance

Studies of the desiccation tolerance of the seedlings of five tropical trees were made on potted plants growing in a greenhouse. Pots were watered to field capacity and then dehydrated for 3 to 9 weeks to reach various visual wilting stages, from slightly wilted to dead. Saturated root hydraulic conductance was measured with a high-pressure flowmeter, and whole-stem hydraulic conductance was measured by a vacuum chamber method. Leaf punches (5.6-mm diameter) were harvested for measurement of leaf water potential by a thermocouple psychrometer method and for measurement of fresh and dry weight. In a parallel study, the same five species were studied in a field experiment in the understory of a tropical forest, where these species frequently germinate. Control seedlings were maintained in irrigated plots during a dry season, and experimental plants were grown in similar plots with rain exclusion shelters. Every 2 to 4 weeks, the seedlings were scored for wilt state and survivorship. After a 22-week drought, the dry plots were irrigated for several weeks to verify visual symptoms of death. The field trials were used to rank drought performance of species, and the greenhouse desiccation studies were used to determine the conditions of moribund plants. Our conclusion is that the desiccation tolerance of moribund plants correlated with field assessment of drought-performance for the five species (r2 > 0.94).

Delayed greening in tropical leaves: an antiherbivore defense?

Many tropical species flush entire canopies of red, white, or light green young leaves. In these species, there is a delay of the normal greening process until after leaves have fully expanded and have begun to toughen. Delayed greening involves a delay in the input of chlorophyll, rubisco, nitrogen, and energy. Photosynthetic capacity is therefore lower than in species with normal greening. At full expansion, leaves begin to toughen quickly, and rates of herbivory drop by a factor of 4. We suggest that delayed greening has evolved as a mechanism for minimizing losses to herbivores by delaying input of valuable resources until after the leaf is fully expanded and better protected by toughness. These benefits outweigh the costs of forfeited photosynthesis in the shaded understory but not in the high light treefall gaps. This cost evaluation suggests that, in the face of herbivory, it is advantageous to have delayed greening in the shade and normal development in the sun. Data from 175 of the most common tree species on Barro Colorado Island confirm that delayed greening is extremely common in shade tolerant species and rare in gap specialists.

Nitrogen content and expansion rate of young leaves of rain forest species: implications for herbivory

We investigated variation in the nitrogen content of young leaves and the rate of leaf expansion in tropical shade tolerant species. Both these factors can influence rates of herbivory: low nitrogen content makes leaves less attractive to herbivores, while rapid expansion reduces the time that young leaves are vulnerable to herbivory. Among the 13 study species, nitrogen in young leaves (at 5% of full expansion) ranged from 20 to 71 mg/g DW. Most species had higher nitrogen in young leaves compared to mature leaves, but one species showed no change with age. The ratio of nitrogen import relative to dry weight import was low (1-4%) and dropped during expansion. The amount of nitrogen imported daily into the leaf peaked at 70-75 percent of-full expansion, though species varied in the percent of final nitrogen that was imported prior to full expansion (67%-93%). There was a significant positive correlation between nitrogen content of young leaves and the rate of leaf expansion. We suggest that the age-specific patterns of nitrogen can best be understood as a trade-off between high palatability to herbivores and escape through rapid expansion. IN MOST SPECIES, young expanding leaves are more heavily attacked by both chewing and sucking insects than are mature leaves (e.g., Feeny 1976, Raupp & Denno 1983, Lowman 1985, Crawley 1986, Lightfoot & Whitford 1987, Slansky & Rodriguez 1987). This pattern has been documented in communities as diverse as grasslands, tundra, and temperate forests, but may be most pronounced in tropical rain forests (Coley & Aide 1991). For 24 shade tolerant species studied in Panama, rates of herbivory were 25 times faster on young leaves compared to mature leaves (Coley 1983). This means that although young leaves are expanding for only 3 percent of their lifetime, almost 50 percent of the lifetime damage occurs during this period. Therefore, to fully understand the factors that regulate losses to herbivores, we must examine the characteristics of young leaves. Young leaves have a variety of characteristics that are likely to function as anti-herbivore defenses. In many species, young leaves are protected by ants associated with extrafloral nectaries (Bentley & Elias 1983, McKey 1989). Young leaves tend to be more pubescent and to contain higher concentrations of tannins and other secondary metabolites (Coley 1983, Coley & Aide 1991). Synchronous production of young leaves during times of low herbivore density may permit plants to avoid most herbivores and satiate those that are present (Feeny 1976; McKey 1979, 1989; Lieberman & Lieberman 1984; l Received 24 December 1989, revision accepted 13 November 1990. Crawley 1986; Aide 1988). Rapid expansion of individual leaves may also reduce the period of vulnerability before leaves have expanded, toughened, and become better defended against herbivores (Orians & Janzen 1974, McKey 1979, Hay et al. 1988, Aide & Londono 1989). Despite these defenses, young leaves generally have higher rates of herbivory than mature leaves. One reason may be because young leaves are less tough and easier to chew and digest. For mature leaves of tropical species, leaf toughness is quite negatively correlated with herbivory and appears to be the most effective defense (Coley 1983). However, toughness is not an option for expanding leaves because the formation of a lignified secondary cell wall is not compatible with cell division and cell expansion. Once young leaves reach full size and begin to toughen, rates of herbivory can drop precipitously (Coley 1983). Another factor which may contribute to high herbivory on young leaves is their greater nutritional value. Young leaves typically have two to four times the nitrogen content of mature leaves (Ho et al. 1984, Mattson & Scriber 1987, Coley & Aide 1991). Diets with higher nitrogen can increase herbivore fitness (Mattson & Scriber 1987). It is therefore not surprising that nitrogen content is positively correlated with food choice for both chewing and sucking insects. Any changes in the developmental patterns of young leaves that reduce the concentration of nitrogen might therefore reduce the rates of herbivory on young leaves (Moran & Hamilton 1980, Neuvonen & Haukioja 1984).