Protection Mutualisms and the Community: Geographic Variation in an Ant-Plant Symbiosis and the Consequences for Herbivores

Protection mutualisms mediate trophic interactions in many systems, but their effects on the surrounding community are rarely studied. Ant-plant symbioses are classic examples of protection mutualisms: myrmecophytic plants provide nesting space and food for symbiotic ants in exchange for ant defense. Ant defense should thus reduce the abundance of herbivores, but studies of ant-plant symbioses usually measure damage to the plant without quantifying the herbivores themselves. In this study, we investigated whether geographic variation in the quality of ant defense in a symbiotic mutualism between Cordia alliodora trees and Azteca ants was associated with the abundance and species richness of plant herbivore communities. In three tropical-dry-forest sites in Middle America, we found that the density of Azteca ants within trees was negatively associated with the levels of leaf herbivory. At sites where ants were effective tree defenders, tree herbivores were less abundant and herbivore assemblages on trees exhibited lower species richness than at a site where ants were poor defenders. In addition, in a site where ants reduced herbivory, herbivore communities were less abundant and diverse in the presence of ants than in their absence, where as in a site where ants did not reduce herbivory, there were no differences in herbivore abundance or richness between trees with or without ants. We conclude that geographic variation in the quality of ant defense drives variation in myrmecophytic-plant herbivore communities. Moreover, ant-plant protection mutualisms should have important but rarely considered effects on herbivore population dynamics and food-plant specialization

Orthogonal fitness benefits of nitrogen and ants for nitrogen‐limited plants in the presence of herbivores

Predictable effects of resource availability on plant growth‐defense strategies provide a unifying theme in theories of direct anti‐herbivore defense, but it is less clear how resource availability modulates plant indirect defense. Ant‐plant‐hemipteran interactions produce mutualistic trophic cascades when hemipteran‐tending ants reduce total herbivory, and these interactions are a key component of plant indirect defense in most terrestrial ecosystems. Here we conducted an experiment to test how ant‐plant‐hemipteran interactions depend on nitrogen (N) availability by manipulating the presence of ants and aphids under different N fertilization treatments. Ants increased plant flowering success by decreasing the densities of herbivores, and the effects of ants on folivores were positively related to the density of aphids. Unexpectedly, N fertilization produced no changes in plant N concentrations. Plants grown in higher N grew and flowered more, but aphid honeydew chemistry stayed the same, and neither the density of aphids nor the rate of ant attraction per aphid changed with N addition. The positive effects of ants and N addition on plant fitness were thus independent of one another. We conclude that N was the plant’s limiting nutrient and propose that addition of the limiting nutrient is unlikely to alter the strength of mutualistic trophic cascades.Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/139927/1/ecy2013_am.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/139927/2/ecy2013-sup-0002-AppendixS2.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/139927/3/ecy2013-sup-0003-AppendixS3.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/139927/4/ecy2013-sup-0001-AppendixS1.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/139927/5/ecy2013-sup-0006-AppendixS6.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/139927/6/ecy2013.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/139927/7/ecy2013-sup-0007-AppendixS7.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/139927/8/ecy2013-sup-0004-AppendixS4.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/139927/9/ecy2013-sup-0005-AppendixS5.pd

Plant‐derived differences in the composition of aphid honeydew and their effects on colonies of aphid‐tending ants

In plant–ant–hemipteran interactions, ants visit plants to consume the honeydew produced by phloem‐feeding hemipterans. If genetically based differences in plant phloem chemistry change the chemical composition of hemipteran honeydew, then the plant's genetic constitution could have indirect effects on ants via the hemipterans. If such effects change ant behavior, they could feed back to affect the plant itself. We compared the chemical composition of honeydews produced by Aphis nerii aphid clones on two milkweed congeners, Asclepias curassavica and Asclepias incarnata , and we measured the responses of experimental Linepithema humile ant colonies to these honeydews. The compositions of secondary metabolites, sugars, and amino acids differed significantly in the honeydews from the two plant species. Ant colonies feeding on honeydew derived from A. incarnata recruited in higher numbers to artificial diet, maintained higher queen and worker dry weight, and sustained marginally more workers than ants feeding on honeydew derived from A. curassavica . Ants feeding on honeydew from A. incarnata were also more exploratory in behavioral assays than ants feeding from A. curassavica . Despite performing better when feeding on the A. incarnata honeydew, ant workers marginally preferred honeydew from A. curassavica to honeydew from A. incarnata when given a choice. Our results demonstrate that plant congeners can exert strong indirect effects on ant colonies by means of plant‐species‐specific differences in aphid honeydew chemistry. Moreover, these effects changed ant behavior and thus could feed back to affect plant performance in the field. The role of indirect effects in trait evolution remains poorly understood. We show that plant chemical traits indirectly affect ant colony fitness and behavior via direct interactions with aphids. These plant‐derived effects on ant behavior could feed back to affect plant fitness in the field.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/109587/1/ece31277.pd

Water Stress Strengthens Mutualism Among Ants, Trees, and Scale Insects

Abiotic environmental variables strongly affect the outcomes of species interactions. For example, mutualistic interactions between species are often stronger when resources are limited. The effect might be indirect: water stress on plants can lead to carbon stress, which could alter carbon-mediated plant mutualisms. In mutualistic ant–plant symbioses, plants host ant colonies that defend them against herbivores. Here we show that the partners\u27 investments in a widespread ant–plant symbiosis increase with water stress across 26 sites along a Mesoamerican precipitation gradient. At lower precipitation levels, Cordia alliodora trees invest more carbon in Azteca ants via phloem-feeding scale insects that provide the ants with sugars, and the ants provide better defense of the carbon-producing leaves. Under water stress, the trees have smaller carbon pools. A model of the carbon trade-offs for the mutualistic partners shows that the observed strategies can arise from the carbon costs of rare but extreme events of herbivory in the rainy season. Thus, water limitation, together with the risk of herbivory, increases the strength of a carbon-based mutualism

Changes in tree community structure in defaunated forests are not driven only by dispersal limitation

Bushmeat hunting has reduced population sizes of large frugivorous vertebrates throughout the tropics, thereby reducing the dispersal of seeds. This is believed to affect tree population dynamics, and therefore community composition, because the seed dispersal of large-seeded trees depends upon large-bodied vertebrates.We report on a long-running study of the effect of defaunation on a tropical tree community. In three censuses over 11 years, we compared sapling recruitment between a hunted and a nonhunted site, which are nearby and comparable to one another, to determine the extent to which species composition has changed through time following defaunation. We expected to find a reduced abundance of tree species that rely on large frugivores for dispersal at the hunted site and altered community structure as a consequence.Although community composition at the hunted site diverged from that at the nonhunted site, the changes were independent of dispersal syndrome, with no trend toward a decline in species that are dispersed by large, hunted vertebrates. Moreover, the loss of large-bodied dispersers did not generate the changes in tree community composition that we hypothesized. Some species presumed to rely on large-bodied frugivores for dispersal are effectively recruiting despite the absence of their dispersers.Synthesis: The presumption that forests depleted of large-bodied dispersers will experience rapid, directional compositional change is not fully supported by our results. Altered species composition in the sapling layer at the hunted site, however, indicates that defaunation may be connected with changes to the tree community, but that the nature of these changes is not unidirectional as previously assumed. It remains difficult to predict how defaunation will affect tree community composition without a deeper understanding of the driving mechanisms at play

Changes in tree community structure in defaunated forests are not driven only by dispersal limitation

1. Bushmeat hunting has reduced population sizes of large frugivorous vertebrates throughout the tropics, thereby reducing the dispersal of seeds. This is believed to affect tree population dynamics, and therefore community composition, because the seed dispersal of large‐seeded trees depends upon large‐bodied vertebrates. 2. We report on a long‐running study of the effect of defaunation on a tropical tree community. In three censuses over 11 years, we compared sapling recruitment between a hunted and a nonhunted site, which are nearby and comparable to one another, to determine the extent to which species composition has changed through time following defaunation. We expected to find a reduced abundance of tree species that rely on large frugivores for dispersal at the hunted site and altered community structure as a consequence. 3. Although community composition at the hunted site diverged from that at the nonhunted site, the changes were independent of dispersal syndrome, with no trend toward a decline in species that are dispersed by large, hunted vertebrates. Moreover, the loss of large‐bodied dispersers did not generate the changes in tree community composition that we hypothesized. Some species presumed to rely on large‐bodied frugivores for dispersal are effectively recruiting despite the absence of their dispersers. 4. Synthesis: The presumption that forests depleted of large‐bodied dispersers will experience rapid, directional compositional change is not fully supported by our results. Altered species composition in the sapling layer at the hunted site, however, indicates that defaunation may be connected with changes to the tree community, but that the nature of these changes is not unidirectional as previously assumed. It remains difficult to predict how defaunation will affect tree community composition without a deeper understanding of the driving mechanisms at play

Integrating plant carbon dynamics with mutualism ecology

Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/138937/1/nph13679.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/138937/2/nph13679_am.pd

Tree recruitment in an empty forest

To assess how the decimation of large vertebrates by hunting alters recruitment processes in a tropical forest, we compared the sapling cohorts of two structurally and compositionally similar forests in the Rio Manu floodplain in southeastern Peru. Large vertebrates were severely depleted at one site, Boca Manu (BM), whereas the other, Cocha Cashu Biological Station (CC), supported an intact fauna. At both sites we sampled small (1 m tall, ,1 cm dbh) and large (1 cm and ,10 cm dbh) saplings in the central portion of 4-ha plots within which all trees 10 cm dbh were mapped and identified. This design ensured that all conspecific adults within at least 50 m (BM) or 55 m (CC) of any sapling would have known locations. We used the Janzen-Connell model to make five predictions about the sapling cohorts at BM with respect to CC: (1) reduced overall sapling recruitment, (2) increased recruitment of species dispersed by abiotic means, (3) altered relative abundances of species, (4) prominence of large-seeded species among those showing depressed recruitment, and (5) little or no tendency for saplings to cluster closer to adults at BM. Our results affirmed each of these predictions. Interpreted at face value, the evidence suggests that few species are demographically stable at BM and that up to 28% are increasing and 72% decreasing. Loss of dispersal function allows species dispersed abiotically and by small birds and mammals to substitute for those dispersed by large birds and mammals. Although we regard these conclusions as preliminary, over the long run, the observed type of directional change in tree composition is likely to result in biodiversity loss and negative feedbacks on both the animal and plant communities. Our results suggest that the best, and perhaps only, way to prevent compositional change and probable loss of diversity in tropical tree communities is to prohibit hunting

A protein interaction map for cell polarity development

Many genes required for cell polarity development in budding yeast have been identified and arranged into a functional hierarchy. Core elements of the hierarchy are widely conserved, underlying cell polarity development in diverse eukaryotes. To enumerate more fully the protein–protein interactions that mediate cell polarity development, and to uncover novel mechanisms that coordinate the numerous events involved, we carried out a large-scale two-hybrid experiment. 68 Gal4 DNA binding domain fusions of yeast proteins associated with the actin cytoskeleton, septins, the secretory apparatus, and Rho-type GTPases were used to screen an array of yeast transformants that express ∼90% of the predicted Saccharomyces cerevisiae open reading frames as Gal4 activation domain fusions. 191 protein–protein interactions were detected, of which 128 had not been described previously. 44 interactions implicated 20 previously uncharacterized proteins in cell polarity development. Further insights into possible roles of 13 of these proteins were revealed by their multiple two-hybrid interactions and by subcellular localization. Included in the interaction network were associations of Cdc42 and Rho1 pathways with proteins involved in exocytosis, septin organization, actin assembly, microtubule organization, autophagy, cytokinesis, and cell wall synthesis. Other interactions suggested direct connections between Rho1- and Cdc42-regulated pathways; the secretory apparatus and regulators of polarity establishment; actin assembly and the morphogenesis checkpoint; and the exocytic and endocytic machinery. In total, a network of interactions that provide an integrated response of signaling proteins, the cytoskeleton, and organelles to the spatial cues that direct polarity development was revealed

Intraspecific Geographic Variation of Fragrances Acquired by Orchid Bees in Native and Introduced Populations

Male orchid bees collect volatiles, from both floral and non-floral sources, that they expose as pheromone analogues (perfumes) during courtship display. The chemical profile of these perfumes, which includes terpenes and aromatic compounds, is both species-specific and divergent among closely related lineages. Thus, fragrance composition is thought to play an important role in prezygotic reproductive isolation in euglossine bees. However, because orchid bees acquire fragrances entirely from exogenous sources, the chemical composition of male perfumes is prone to variation due to environmental heterogeneity across habitats. We used Gas Chromatography/Mass Spectrometry (GC/MS) to characterize the perfumes of 114 individuals of the green orchid bee (Euglossa aff. viridissima) sampled from five native populations in Mesoamerica and two naturalized populations in the southeastern United States. We recorded a total of 292 fragrance compounds from hind-leg extracts, and found that overall perfume composition was different for each population. We detected a pronounced chemical dissimilarity between native (Mesoamerica) and naturalized (U.S.) populations that was driven both by proportional differences of common compounds as well as the presence of a few chemicals unique to each population group. Despite these differences, our data also revealed remarkable qualitative consistency in the presence of several major fragrance compounds across distant populations from dissimilar habitats. In addition, we demonstrate that naturalized bees are attracted to and collect large quantities of triclopyr 2-butoxyethyl ester, the active ingredient of several commercially available herbicides. By comparing incidence values and consistency indices across populations, we identify putative functional compounds that may play an important role in courtship signaling in this species of orchid bee