Jerome J. Howard

Global patterns of leaf mechanical properties

Leaf mechanical properties strongly influence leaf lifespan, plant-herbivore interactions, litter decomposition and nutrient cycling, but global patterns in their interspecific variation and underlying mechanisms remain poorly understood. We synthesize data across the three major measurement methods, permitting the first global analyses of leaf mechanics and associated traits, for 2819 species from 90 sites worldwide. Key measures of leaf mechanical resistance varied c. 500-800-fold among species. Contrary to a long-standing hypothesis, tropical leaves were not mechanically more resistant than temperate leaves. Leaf mechanical resistance was modestly related to rainfall and local light environment. By partitioning leaf mechanical resistance into three different components we discovered that toughness per density contributed a surprisingly large fraction to variation in mechanical resistance, larger than the fractions contributed by lamina thickness and tissue density. Higher toughness per density was associated with long leaf lifespan especially in forest understory. Seldom appreciated in the past, toughness per density is a key factor in leaf mechanical resistance, which itself influences plant-animal interactions and ecosystem functions across the globe.

Leafcutting and Diet Selection: Relative Influence of Leaf Chemistry and Physical Features

The effects of leaf toughness, trichome characteristics, nutrient and water availability, and secondary chemistry on diet selection by the leafcutting ant Atta cephalotes were determined using individuals of 49 woody plant species from a tropical deciduous forest in Costa Rica. The palatability of plants was measured by presenting whole leaves to leafcutting ant foragers on trails and counting the number of pieces cut from leaves. The effectiveness of physical barriers to leaf cutting was evaluated by measuring the speed with which ants were able to cut leaves of varying toughness, trichome densities, and trichome lengths. Plant secondary chemistry was highly correlated with the relative palatability of leaves, while palatability was only marginally correlated with trichome characteristics and plant nutritional quality and was uncorrelated with leaf toughness and water content. Highly palatable leaves generally contained hydrolyzable tannins, while most unpalatable leaves possessed nonpolar extracts found to deter leaf cutting in laboratory bioassays. Within the subset of highly palatable plants, leaf protein content was positively correlated with the number of pieces cut, indicating that secondary chemistry and nutrient availability interact to determine palatability. Decreases in plant palatability over time paralleled decreases in protein content. Ant size was the most important variable determining the rate at which ants cut leaves. Trichome characteristics were uncorrelated with the rate at which leaves were cut, while leaf toughness explained a small amount of the variance in cutting rate. The results suggest that leaf toughness and trichome characteristics within the ranges encountered by leafcutting ants in this tropical deciduous forest do not generally deter attack by ants. Instead, the results are consistent with the idea that leafcutting ants use a combination of plant secondary chemistry and nutrient availability to evaluate the quality of leaves.

Leafcutting Ant Diet Selection: The Role of Nutrients, Water, and Secondary Chemistry

The relationship of plant secondary chemistry, water content, and nutrient content to the palatability of leaves to the leafcutting ant Atta cephalotes was determined in a study of individuals from 50 woody plant species in tropical dry forest of Costa Rica. The study took place during the yearly period of maximum leaf harvest, in the early rainy season. The palatability of plants was determined by presenting leaf disks to ants on active foraging trails of three ant colonies. The distribution of several classes of polar secondary compounds in leaf samples was determined using chemical spot tests, and that of ant—deterrent nonpolar compounds using laboratory bioassays of plant nonpolar extracts. Nitrogen, energy, and water availability in leaves were assessed using quantitative analyses. Plants of high relative palatability generally lacked deterrent nonpolar extracts but did contain hydrolyzable tannins; the opposite was true for plants of low palatability. Little or no relationship was found to exist between plant palatability and measures of leaf nitrogen, energy content, and moisture content, or the presence of alkaloids and condensed tannins in leaves. No statistically significant interactions among leaf characteristics were found. The number of leaf disks harvested by ant colonies decreased during the study period. This decrease was unrelated to nutrient and moisture availability in leaves, but may be related to changes in secondary chemistry over the course of the season. Although plants were not equally palatable to all colonies tested, there was no evidence that colony—to—colony differences in plant preferences were related to the plant characteristic studied. Overall, the results suggest that plant secondary chemistry is the best predictor of plant species utilization by leafcutting ants.

Chemical Leaf Repellency to an Attine Ant: Seasonal Distribution Among Potential Host Plant Species

The chemical repellency of leaves to the leaf-cutting, fungus-growing ant Atta cephalotes was surveyed for 42 plant species randomly selected from the dry forest of Santa Rosa National Park, Guanacaste, Costa Rica. The sample represents about one-sixth of the potential host plant species available to the ants in the secondary, semideciduous forest at Santa Rosa. Repellencies of leaf extracts were measured by bioassay. A laboratory colony of A. cephalotes collected from Santa Rosa was used. Three-quarters of the species exhibited significantly repellent nonpolar (lipid-soluble) extractables (e.g., terpenoids, steroids, and waxes), and half of the species exhibited repellent polar extractables (e.g., phenols, flavonoids, and glycosides). The occurrence of significant extractable repellents, partic- ularly in the lipid-soluble fraction, correlated closely with species that were avoided in leaf-preference tests and with seasonal patterns of host-plant selection by ant colonies in the Santa Rosa forest. There were no clear correlations of repellency with plant growth form or with evergreen vs. deciduous habit. Further chemical isolation of ant-repellent substances from a number of avoided species revealed that most of the repellent compounds are terpenoids, some of which have already been shown to be highly toxic to the ants fungus and to many other fungi as well. A dramatic decline in the amount of extractable repellent occurred in almost all plant species in the latter half of the wet season, 1-2 mo before the dry season began. Because this decline was prevalent in evergreen as well as deciduous species, we tentatively concluded that the ant-repellent substances in the leaves are mainly the result of selection in plants for fungal resistance, which incidentally confers resistance to attack by leaf-cutting ants. We suggest that the decline in the amount of repellent substance is due to a reduction in the synthesis of antifungal secondary compounds in the dry season, when the risk of fungal attack is low.

Global optimization from suboptimal parts: foraging sensu lato by leaf-cutting ants

Central-place foraging theory has been unable to explain the load selection behavior of leaf-cutting ants (Atta spp., Attini: Formicidae). We suggest that this is due to incomplete consideration of the sequence of behaviors involved in resource acquisition by these ants. Unlike most central-place foragers, leaf-cutting ants do not return to their nests with food. Instead, the leaf fragments they gather must be processed within the nest to convert them to substrate for fungal gardens. We have shown previously that leaf fragment size affects the rate of distribution and processing of leaf tissue inside laboratory nests of Atta colombica. Including these tasks in the calculation of foraging rate may help explain load selection and other features of central-place foraging by Atta colonies. Here we develop a mathematical model of the complete sequence of external and internal tasks that lead to addition of substrate to fungal gardens. Using realistic parameter values, the leaf fragment sizes predicted to maximize a colonys rate of foraging in this broad sense correspond well with the mean fragment sizes actually collected by Atta colonies in the field. The optimal fragment size for global performance in the model is below the size that would maximize the delivery rate by above-ground foragers. The globally optimal size also fails to maximize the rate of either fragment distribution or fragment processing within the nest. Our results show how maximum collective performance of an ensemble of linked tasks may require behavior that would appear suboptimal in a piecemeal analysis of tasks.

Integrating microsatellite and pedigree analyses to facilitate the captive management of the endangered Mississippi sandhill crane (Grus canadensis pulla)

The minimization of kinship in captive populations is usually achieved through the use of pedigree information. However, pedigree knowledge alone is not sufficient if pedigree information is missing, questionable, or when the founders of the captive population are related to one another. If this is the case, higher levels of inbreeding and lower levels of genetic diversity may be present in a captive population than those calculated by pedigree analyses alone. In this study, the genetic status of the critically endangered Mississippi sandhill crane (MSC) (Grus canadensis pulla) was analyzed using studbook data from the U.S. Fish and Wildlife Service managed captive breeding program as well as microsatellite DNA data. These analyses provided information on shared founder genotypes, allowing for refined analysis of genetic variation in the population, and the development of a new DNA-based studbook pedigree that will assist in the genetic management of the MSC population.

Optimality in a partitioned task performed by social insects

Biologists have long been aware that adaptations should not be analysed in isolation from the function of the whole organism. Here, we address the equivalent issue at the scale of a social insect colony: the optimality of component behaviours in a partitioned sequence of tasks. In colonies of Atta colombica, a leaf-cutting ant, harvested leaf tissue is passed from foragers to nest workers that distribute, clean, shred and implant the tissue in fungal gardens. In four laboratory colonies of A. colombica, we found that the highest colony-wide rate of leaf tissue processing in the nest was achieved when leaf fragment sizes were suboptimal for individual delivery rate by foragers. Leaf-cutting ant colonies appear to compromise the efficiency of collecting leaf tissue in order to increase their ability to handle the material when it arrives in the nest. Such compromise reinforces the idea that behavioural adaptations, like adaptations in general, must be considered within the context of the larger entity of which they are a part.

Isolation and characterization of 14 polymorphic microsatellite DNA loci for the endangered Whooping Crane (Grus americana) and their applicability to other crane species

Fourteen microsatellite DNA loci were isolated from the endangered Whooping Crane (Grus americana) and genetic variability assessed from 45 captive reared individuals. Allele numbers detected at each locus ranged from 2 to 6, the highest seen for this species. Mean observed heterozygosity varied from 0.04 to 0.79. These markers were then successfully amplified for two non-migratory populations of Sandhill Crane [Florida (Grus canadensis pratensis) and Missisippi (Grus canadensis pulla)], underscoring their utility for the conservation of threatened crane species.