Elsa Youngsteadt

Seed odor mediates an obligate ant–plant mutualism in Amazonian rainforests

Seed dispersal mutualisms are essential for the survival of diverse plant species and communities worldwide. Among invertebrates, only ants have a major role in seed dispersal, and thousands of plant species produce seeds specialized for ant dispersal in “diffuse” multispecies interactions. An outstanding but poorly understood ant–seed mutualism occurs in the Amazonian rainforest, where arboreal ants collect seeds of several epiphyte species and cultivate them in nutrient-rich nests, forming abundant and conspicuous hanging gardens known as ant-gardens (AGs). AG ants and plants are dominant members of lowland Amazonian ecosystems, and their interaction is both specific and obligate, but the means by which ants locate, recognize, and accept their mutualist seeds while rejecting other seeds is unknown. Here we address the chemical and behavioral basis of the AG interaction. We show that workers of the AG ant Camponotus femoratus are attracted to odorants emanating from seeds of the AG plant Peperomia macrostachya, and that chemical cues also elicit seed-carrying behavior. We identify five compounds from P. macrostachya seeds that, as a blend, attract C. femoratus workers. This report of attractive odorants from ant-dispersed seeds illustrates the intimacy and complexity of the AG mutualism and begins to illuminate the chemical basis of this important and enigmatic interaction.

Do cities simulate climate change? A comparison of herbivore response to urban and global warming

Cities experience elevated temperature, CO2 , and nitrogen deposition decades ahead of the global average, such that biological response to urbanization may predict response to future climate change. This hypothesis remains untested due to a lack of complementary urban and long-term observations. Here, we examine the response of an herbivore, the scale insect Melanaspis tenebricosa, to temperature in the context of an urban heat island, a series of historical temperature fluctuations, and recent climate warming. We survey M. tenebricosa on 55 urban street trees in Raleigh, NC, 342 herbarium specimens collected in the rural southeastern United States from 1895 to 2011, and at 20 rural forest sites represented by both modern (2013) and historical samples. We relate scale insect abundance to August temperatures and find that M. tenebricosa is most common in the hottest parts of the city, on historical specimens collected during warm time periods, and in present-day rural forests compared to the same sites when they were cooler. Scale insects reached their highest densities in the city, but abundance peaked at similar temperatures in urban and historical datasets and tracked temperature on a decadal scale. Although urban habitats are highly modified, species response to a key abiotic factor, temperature, was consistent across urban and rural-forest ecosystems. Cities may be an appropriate but underused system for developing and testing hypotheses about biological effects of climate change. Future work should test the applicability of this model to other groups of organisms.

Fine-scale heterogeneity across Manhattan's urban habitat mosaic is associated with variation in ant composition and richness

Global urbanisation is rapidly expanding and most of the worlds humans now live in cities. Most ecological studies have, however, focused on protected areas. To address this issue, we tested predictions from studies of protected areas in urban ecosystems. Because most cities are heterogeneous habitat mosaics which include habitats with varying levels of chronic environmental stress, we focused on predictions from studies of less modified ecosystems about community‐wide responses to variation in chronic stress. We sampled ants across Manhattans urban habitat mosaic, at sites with varying levels of chronic environmental stress. Many predictions derived from less modified ecosystems were supported by our findings: despite being the most intensively sampled habitat, high stress urban medians had less variability in ant composition –both within and among sites – than either urban parks or urban forests, the lowest stress habitat – urban forests‐had significantly more accumulated species and a higher number of unique species than higher stress habitats, and urban parks, which have intermediate levels of chronic environmental stress, also had intermediate levels of variation in among‐site species composition, accumulated species richness, and the incidence of unique species. The most common species also differed across Manhattans urban habitat mosaic. Nevertheless, the prediction that exotic species would occur more frequently in higher stress habitats was not supported; exotic species were equally common across all habitats. These findings suggest that fine‐scale heterogeneity in the chronic stress of urban habitats may be an underappreciated, but important structuring force for urban animal communities.

Species-specific seed dispersal in an obligate ant-plant mutualism.

Throughout lowland Amazonia, arboreal ants collect seeds of specific plants and cultivate them in nutrient-rich nests, forming diverse yet obligate and species-specific symbioses called Neotropical ant-gardens (AGs). The ants depend on their symbiotic plants for nest stability, and the plants depend on AGs for substrate and nutrients. Although the AGs are limited to specific participants, it is unknown at what stage specificity arises, and seed fate pathways in AG epiphytes are undocumented. Here we examine the specificity of the ant-seed interaction by comparing the ant community observed at general food baits to ants attracted to and removing seeds of the AG plant Peperomia macrostachya. We also compare seed removal rates under treatments that excluded vertebrates, arthropods, or both. In the bait study, only three of 70 ant species collected P. macrostachya seeds, and 84% of observed seed removal by ants was attributed to the AG ant Camponotus femoratus. In the exclusion experiment, arthropod exclusion significantly reduced seed removal rates, but vertebrate exclusion did not. We provide the most extensive empirical evidence of species specificity in the AG mutualism and begin to quantify factors that affect seed fate in order to understand conditions that favor its departure from the typical diffuse model of plant-animal mutualism.

Urban warming reduces aboveground carbon storage

A substantial amount of global carbon is stored in mature trees. However, no experiments to date test how warming affects mature tree carbon storage. Using a unique, citywide, factorial experiment, we investigated how warming and insect herbivory affected physiological function and carbon sequestration (carbon stored per year) of mature trees. Urban warming increased herbivorous arthropod abundance on trees, but these herbivores had negligible effects on tree carbon sequestration. Instead, urban warming was associated with an estimated 12% loss of carbon sequestration, in part because photosynthesis was reduced at hotter sites. Ecosystem service assessments that do not consider urban conditions may overestimate urban tree carbon storage. Because urban and global warming are becoming more intense, our results suggest that urban trees will sequester even less carbon in the future.

Urbanization Increases Pathogen Pressure on Feral and Managed Honey Bees.

Given the role of infectious disease in global pollinator decline, there is a need to understand factors that shape pathogen susceptibility and transmission in bees. Here we ask how urbanization affects the immune response and pathogen load of feral and managed colonies of honey bees (Apis mellifera Linnaeus), the predominant economically important pollinator worldwide. Using quantitative real-time PCR, we measured expression of 4 immune genes and relative abundance of 10 honey bee pathogens. We also measured worker survival in a laboratory bioassay. We found that pathogen pressure on honey bees increased with urbanization and management, and the probability of worker survival declined 3-fold along our urbanization gradient. The effect of management on pathogens appears to be mediated by immunity, with feral bees expressing immune genes at nearly twice the levels of managed bees following an immune challenge. The effect of urbanization, however, was not linked with immunity; instead, urbanization may favor viability and transmission of some disease agents. Feral colonies, with lower disease burdens and stronger immune responses, may illuminate ways to improve honey bee management. The previously unexamined effects of urbanization on honey-bee disease are concerning, suggesting that urban areas may favor problematic diseases of pollinators.

Urban stress is associated with variation in microbial species composition—but not richness—in Manhattan

The biological diversity and composition of microorganisms influences both human health outcomes and ecological processes; therefore, understanding the factors that influence microbial biodiversity is key to creating healthy, functional landscapes in which to live. In general, biological diversity is predicted to be limited by habitat size, which for green areas is often reduced in cities, and by chronic disturbance (stress). These hypotheses have not previously been tested in microbial systems in direct comparison to macroorganisms. Here we analyzed bacterial, fungal and ant communities in small road medians (average area 0.0008 km2) and larger parks (average area 0.64 km2) across Manhattan (NYC). Bacterial species richness was not significantly different between medians and parks, but community composition was significantly distinct. In contrast, ant communities differed both in composition and richness with fewer ant species in medians than parks. Fungi showed no significant variation in composition or richness but had few shared taxa between habitats or sites. The diversity and composition of microbes appears less sensitive to habitat patchiness or urban stress than those of macroorganisms. Microbes and their associated ecosystem services and functions may be more resilient to the negative effects of urbanization than has been previously appreciated.

Physiological thermal limits predict differential responses of bees to urban heat-island effects

Changes in community composition are an important, but hard to predict, effect of climate change. Here, we use a wild-bee study system to test the ability of critical thermal maxima (CTmax, a measure of heat tolerance) to predict community responses to urban heat-island effects in Raleigh, NC, USA. Among 15 focal species, CTmax ranged from 44.6 to 51.3°C, and was strongly predictive of population responses to urban warming across 18 study sites (r2 = 0.44). Species with low CTmax declined the most. After phylogenetic correction, solitary species and cavity-nesting species (bumblebees) had the lowest CTmax, suggesting that these groups may be most sensitive to climate change. Community responses to urban and global warming will likely retain strong physiological signal, even after decades of warming during which time lags and interspecific interactions could modulate direct effects of temperature.

Divergent Chemical Cues Elicit Seed Collecting by Ants in an Obligate Multi-Species Mutualism in Lowland Amazonia

In lowland Amazonian rainforests, specific ants collect seeds of several plant species and cultivate them in arboreal carton nests, forming species-specific symbioses called ant-gardens (AGs). In this obligate mutualism, ants depend on the plants for nest stability and the plants depend on ant nests for substrate and nutrients. AG ants and plants are abundant, dominant members of lowland Amazonian ecosystems, but the cues ants use to recognize the seeds are poorly understood. To address the chemical basis of the ant-seed interaction, we surveyed seed chemistry in nine AG species and eight non-AG congeners. We detected seven phenolic and terpenoid volatiles common to seeds of all or most of the AG species, but a blend of the shared compounds was not attractive to the AG ant Camponotus femoratus. We also analyzed seeds of three AG species (Anthurium gracile, Codonanthe uleana, and Peperomia macrostachya) using behavior-guided fractionation. At least one chromatographic fraction of each seed extract elicited retrieval behavior in C. femoratus, but the active fractions of the three plant species differed in polarity and chemical composition, indicating that shared compounds alone did not explain seed-carrying behavior. We suggest that the various AG seed species must elicit seed-carrying with different chemical cues.

Ad hoc instrumentation methods in ecological studies produce highly biased temperature measurements

Abstract In light of global climate change, ecological studies increasingly address effects of temperature on organisms and ecosystems. To measure air temperature at biologically relevant scales in the field, ecologists often use small, portable temperature sensors. Sensors must be shielded from solar radiation to provide accurate temperature measurements, but our review of 18 years of ecological literature indicates that shielding practices vary across studies (when reported at all), and that ecologists often invent and construct ad hoc radiation shields without testing their efficacy. We performed two field experiments to examine the accuracy of temperature observations from three commonly used portable data loggers (HOBO Pro, HOBO Pendant, and iButton hygrochron) housed in manufactured Gill shields or ad hoc, custom‐fabricated shields constructed from everyday materials such as plastic cups. We installed this sensor array (five replicates of 11 sensor‐shield combinations) at weather stations located in open and forested sites. HOBO Pro sensors with Gill shields were the most accurate devices, with a mean absolute error of 0.2°C relative to weather stations at each site. Error in ad hoc shield treatments ranged from 0.8 to 3.0°C, with the largest errors at the open site. We then deployed one replicate of each sensor‐shield combination at five sites that varied in the amount of urban impervious surface cover, which presents a further shielding challenge. Bias in sensors paired with ad hoc shields increased by up to 0.7°C for every 10% increase in impervious surface. Our results indicate that, due to variable shielding practices, the ecological literature likely includes highly biased temperature data that cannot be compared directly across studies. If left unaddressed, these errors will hinder efforts to predict biological responses to climate change. We call for greater standardization in how temperature data are recorded in the field, handled in analyses, and reported in publications.