Amy M. Savage

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.

Stable isotopes reveal links between human food inputs and urban ant diets

The amount of energy consumed within an average city block is an order of magnitude higher than that consumed in any other ecosystem over a similar area. This is driven by human food inputs, but the consequence of these resources for urban animal populations is poorly understood. We investigated the role of human foods in ant diets across an urbanization gradient in Manhattan using carbon and nitrogen stable isotopes. We found that some—but not all—ant species living in Manhattans most urbanized habitats had δ13C signatures associated with processed human foods. In particular, pavement ants (Tetramorium sp. E) had increased levels of δ13C similar to δ13C levels in human fast foods. The magnitude of this effect was positively correlated with urbanization. By contrast, we detected no differences in δ15N, suggesting Tetramorium feeds at the same trophic level despite shifting to human foods. This pattern persisted across the broader ant community; species in traffic islands used human resources more than park species. Our results demonstrate that the degree urban ants exploit human resources changes across the city and among species, and this variation could play a key role in community structure and ecosystem processes where human and animal food webs intersect.

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.

Timing of Prescribed Burns Affects Abundance and Composition of Arthropods in the Texas Hill Country

Abstract Prior research has demonstrated that fire can be an important structuring force for plant communities in prairies and grasslands. However, investigations of land-management techniques, such as prescribed fire, often overlook responses of local fauna, particularly the arthropods. In this study, we examined a previously unappreciated, although potentially important, component of fire ecology by asking, does the timing of prescribed burns alter community structure of arthropods? At a site in the Texas Hill Country, we used sweep-net sampling to collected arthropods from experimental plots that had been treated with a summer-burn or winter-burn regime. Summer-burn plots supported >170% more individual arthropods than winter burns. Although overall diversity of arthropods did not significantly differ between treatments, there were significantly more carnivorous arthropods and marginally more herbivorous arthropods after fire in summer relative to fire in winter. Effects of timing were particularly strong for Cicadellidae (leaf hoppers) and Tetragnathidae (long-jawed spiders). Our results demonstrate that timing of prescribed fire can substantially alter composition of resident communities of arthropods. Furthermore, these data highlight the importance of examining composition of the community, in addition to diversity indices, when assessing response of arthropods to land-management techniques.

Diversity and evolution of the primate skin microbiome

Skin microbes play a role in human body odour, health and disease. Compared with gut microbes, we know little about the changes in the composition of skin microbes in response to evolutionary changes in hosts, or more recent behavioural and cultural changes in humans. No studies have used sequence-based approaches to consider the skin microbe communities of gorillas and chimpanzees, for example. Comparison of the microbial associates of non-human primates with those of humans offers unique insights into both the ancient and modern features of our skin-associated microbes. Here we describe the microbes found on the skin of humans, chimpanzees, gorillas, rhesus macaques and baboons. We focus on the bacterial and archaeal residents in the axilla using high-throughput sequencing of the 16S rRNA gene. We find that human skin microbial communities are unique relative to those of other primates, in terms of both their diversity and their composition. These differences appear to reflect both ancient shifts during millions of years of primate evolution and more recent changes due to modern hygiene.

Non-additive benefit or cost? Disentangling the indirect effects that occur when plants bearing extrafloral nectaries and honeydew-producing insects share exotic ant mutualists

BACKGROUND AND AIMS In complex communities, organisms often form mutualisms with multiple different partners simultaneously. Non-additive effects may emerge among species linked by these positive interactions. Ants commonly participate in mutualisms with both honeydew-producing insects (HPI) and their extrafloral nectary (EFN)-bearing host plants. Consequently, HPI and EFN-bearing plants may experience non-additive benefits or costs when these groups co-occur. The outcomes of these interactions are likely to be influenced by variation in preferences among ants for honeydew vs. nectar. In this study, a test was made for non-additive effects on HPI and EFN-bearing plants resulting from sharing exotic ant guards. Preferences of the dominant exotic ant species for nectar vs. honeydew resources were also examined. METHODS Ant access, HPI and nectar availability were manipulated on the EFN-bearing shrub, Morinda citrifolia, and ant and HPI abundances, herbivory and plant growth were assessed. Ant-tending behaviours toward HPI across an experimental gradient of nectar availability were also tracked in order to investigate mechanisms underlying ant responses. KEY RESULTS The dominant ant species, Anoplolepis gracilipes, differed from less invasive ants in response to multiple mutualists, with reductions in plot-wide abundances when nectar was reduced, but no response to HPI reduction. Conversely, at sites where A. gracilipes was absent or rare, abundances of less invasive ants increased when nectar was reduced, but declined when HPI were reduced. Non-additive benefits were found at sites dominated by A. gracilipes, but only for M. citrifolia plants. Responses of HPI at these sites supported predictions of the non-additive cost model. Interestingly, the opposite non-additive patterns emerged at sites dominated by other ants. CONCLUSIONS It was demonstrated that strong non-additive benefits and costs can both occur when a plant and herbivore share mutualist partners. These findings suggest that broadening the community context of mutualism studies can reveal important non-additive effects and increase understanding of the dynamics of species interactions.

Geographic variation in a facultative mutualism: consequences for local arthropod composition and diversity

Geographic variation in the outcome of interspecific interactions may influence not only the evolutionary trajectories of species but also the structure of local communities. We investigated this community consequence of geographic variation for a facultative mutualism between ants and wild cotton (Gossypium thurberi). Ants consume wild cotton extrafloral nectar and can protect plants from herbivores. We chose three sites that differed in interaction outcome, including a mutualism (ants provided the greatest benefits to plant fitness and responded to manipulations of extrafloral nectar), a potential commensalism (ants increased plant fitness but were unresponsive to extrafloral nectar), and a neutral interaction (ants neither affected plant fitness nor responded to extrafloral nectar). At all sites, we manipulated ants and extrafloral nectar in a factorial design and monitored the abundance, diversity, and composition of other arthropods occurring on wild cotton plants. We predicted that the effects of ants and extrafloral nectar on arthropods would be largest in the location with the mutualism and weakest where the interaction was neutral. A non-metric multidimensional scaling analysis revealed that the presence of ants altered arthropod composition, but only at the two sites in which ants increased plant fitness. At the site with the mutualism, ants also suppressed detritivore/scavenger abundance and increased aphids. The presence of extrafloral nectar increased arthropod abundance where mutual benefits were the strongest, whereas both arthropod abundance and morphospecies richness declined with extrafloral nectar availability at the site with the weakest ant–plant interaction. Some responses were geographically invariable: total arthropod richness and evenness declined by approximately 20% on plants with ants, and extrafloral nectar reduced carnivore abundance when ants were excluded from plants. These results demonstrate that a facultative ant–plant mutualism can alter the composition of arthropod assemblages on plants and that these community-level consequences vary across the landscape.

The effect of habitual and experimental antiperspirant and deodorant product use on the armpit microbiome

An ever expanding body of research investigates the human microbiome in general and the skin microbiome in particular. Microbiomes vary greatly from individual to individual. Understanding the factors that account for this variation, however, has proven challenging, with many studies able to account statistically for just a small proportion of the inter-individual variation in the abundance, species richness or composition of bacteria. The human armpit has long been noted to host a high biomass bacterial community, and recent studies have highlighted substantial inter-individual variation in armpit bacteria, even relative to variation among individuals for other body habitats. One obvious potential explanation for this variation has to do with the use of personal hygiene products, particularly deodorants and antiperspirants. Here we experimentally manipulate product use to examine the abundance, species richness, and composition of bacterial communities that recolonize the armpits of people with different product use habits. In doing so, we find that when deodorant and antiperspirant use were stopped, culturable bacterial density increased and approached that found on individuals who regularly do not use any product. In addition, when antiperspirants were subsequently applied, bacterial density dramatically declined. These culture-based results are in line with sequence-based comparisons of the effects of long-term product use on bacterial species richness and composition. Sequence-based analyses suggested that individuals who habitually use antiperspirant tended to have a greater richness of bacterial OTUs in their armpits than those who use deodorant. In addition, individuals who used antiperspirants or deodorants long-term, but who stopped using product for two or more days as part of this study, had armpit communities dominated by Staphylococcaceae, whereas those of individuals in our study who habitually used no products were dominated by Corynebacterium. Collectively these results suggest a strong effect of product use on the bacterial composition of armpits. Although stopping the use of deodorant and antiperspirant similarly favors presence of Staphylococcaceae over Corynebacterium, their differential modes of action exert strikingly different effects on the richness of other bacteria living in armpit communities.

Ecologists, educators, and writers collaborate with the public to assess backyard diversity in The School of Ants Project

Citizen science can generate data that would not exist otherwise while increasing public scientific literacy. However, the quality and use of citizen science data have been criticized in the recent ecological literature. We need an approach that advances eco-evolutionary understanding, achieves education goals and incorporates public participation into as many aspects of the scientific process as possible. We collaborated with public participants to make new discoveries about the distribution and ecology of ants while informing the next studies that participants and scientists might perform together. We implemented the School of Ants (SoA) program in which participants sample ants that are identified by taxonomic experts. Using a comprehensive framework that meets the needs of multiple agents, we also developed outreach materials about ant biology, collaborated with educators to incorporate SoA into classroom science, and launched an international SoA module in Italy. In the first 17 months, SoA volunteers collected ants at 500 unique sites across the USA-including all 50 states and Washington, D.C. To address concerns about the validity of citizen scientist-derived data, we conducted a ground truthing trial that confirmed that trained and untrained volunteers were equally effective at collecting ants. Data from SoA samples indicate that ant diversity varies across wide geographic scales and that there can be high levels of native ant diversity where people live. SoA volunteers collected 7 exotic and 107 native ant species. Although exotic ants were common, ants native to North America occurred in ∼70% of all sites. Many of the ants common in backyards were species that tend to be very poorly studied. For example, citizen scientists documented a range extension of more than 2000 miles for the Asian Needle Ant, Pachycondyla chinensis. Using SoA data as a starting point, we collaborated with a science writer to produce a free, interactive iBook about the common ants in North America; the book included distribution maps such as that for P. chinensis informed by participant collections. Moving forward, we plan to leverage this existing framework to address more complex ecological and evolutionary questions in partnership with our public participants.

Trait-mediated indirect interactions in invasions: unique behavioral responses of an invasive ant to plant nectar

Exotic species often form beneficial, facultative associations with indigenous species. However, we still have a limited understanding of the influences that these positive associations may have on the dynamics and impacts of species invasions. Highly invasive species may respond differently than less invasive species to resources that are exchanged in mutualisms, leading to trait-mediated indirect interactions between native species via invaders that may reshape native communities. In this study, we tested the hypothesis that the highly invasive ant species, Anoplolepis gracilipes, exhibits stronger trait changes in response to increasing levels of nectar than co-occurring, less invasive ant species. Across two islands in the Samoan Archipelago, we located multiple sites dominated by A. gracilipes and multiple sites dominated by other, less invasive species. At each site, we manipulated nectar levels on a common extrafloral nectary-bearing shrub and assessed short-term changes in ant worker recruitment and aggression. We found that the recruitment response of the highly invasive ant species A. gracilipes was not unique: other dominant ant species also increased recruitment in response to increasing nectar levels. However, A. gracilipes did show unique changes in aggressive behaviors: as nectar levels increased, the proportion of prey discovered, attacked and removed by A. gracilipes workers and the speed at which they performed these aggressive behaviors all increased strongly. Other ant species showed no such responses. In addition, fewer subordinate ants persisted on plants at sites invaded by A. gracilipes. Finally, plot-level, simultaneous manipulations of ant access to the plants and nectar availability demonstrated that Morinda citrifolia-ant mutualisms influenced the β-diversity of local arthropod communities differently when A. gracilipes dominated local ant assemblages. These results suggest that mutualisms between invasive ants and native plants can modify interactions between invaders and co-occurring arthropods, possibly leading to more negative consequences for native communities. They also underscore the importance of incorporating both positive species interactions and indirect pathways into our studies of both community ecology and invasion biology.