By their own devices: invasive Argentine ants have shifted diet without clear aid from symbiotic microbes.

The functions and compositions of symbiotic bacterial communities often correlate with host ecology. Yet cause-effect relationships and the order of symbiont vs. host change remain unclear in the face of ancient symbioses and conserved host ecology. Several groups of ants exemplify this challenge, as their low-nitrogen diets and specialized symbioses appear conserved and ancient. To address whether nitrogen-provisioning symbionts might be important in the early stages of ant trophic shifts, we studied bacteria from the Argentine ant, Linepithema humile - an invasive species that has transitioned towards greater consumption of sugar-rich, nitrogen-poor foods in parts of its introduced range. Bacteria were present at low densities in most L. humile workers, and among those yielding quality 16S rRNA amplicon sequencing data, we found just three symbionts to be common and dominant. Two, a Lactobacillus and an Acetobacteraceae species, were shared between native and introduced populations. The other, a Rickettsia, was found only in two introduced supercolonies. Across an eight-year period of trophic reduction in one introduced population, we found no change in symbionts, arguing against a relationship between natural dietary change and microbiome composition. Overall, our findings thus argue against major changes in symbiotic bacteria in association with the invasion and trophic shift of L. humile. In addition, genome content from close relatives of the identified symbionts suggests that just one can synthesize most essential amino acids; this bacterium was only modestly abundant in introduced populations, providing little support for a major role of nitrogen-provisioning symbioses in Argentine ant's dietary shift.

Increased grassland arthropod production with mammalian herbivory and eutrophication: a test of mediation pathways.

Increases in nutrient availability and alterations to mammalian herbivore communities are a hallmark of the Anthropocene, with consequences for the primary producer communities in many ecosystems. While progress has advanced understanding of plant community responses to these perturbations, the consequences for energy flow to higher trophic levels in the form of secondary production are less well understood. We quantified arthropod biomass after manipulating soil nutrient availability and wild mammalian herbivory, using identical methods across 13 temperate grasslands. Of experimental increases in nitrogen, phosphorus, and potassium, only treatments including nitrogen resulted in significantly increased arthropod biomass. Wild mammalian herbivore removal had a marginal, negative effect on arthropod biomass, with no interaction with nutrient availability. Path analysis including all sites implicated nutrient content of the primary producers as a driver of increased arthropod mean size, which we confirmed using 10 sites for which we had foliar nutrient data. Plant biomass and physical structure mediated the increase in arthropod abundance, while the nitrogen treatments accounted for additional variation not explained by our measured plant variables. The mean size of arthropod individuals was 2.5 times more influential on the plot-level total arthropod biomass than was the number of individuals. The eutrophication of grasslands through human activity, especially nitrogen deposition, thus may contribute to higher production of arthropod consumers through increases in nutrient availability across trophic levels.

A carbohydrate-rich diet increases social immunity in ants.

Increased potential for disease transmission among nest-mates means living in groups has inherent costs. This increased potential is predicted to select for disease resistance mechanisms that are enhanced by cooperative exchanges among group members, a phenomenon known as social immunity. One potential mediator of social immunity is diet nutritional balance because traits underlying immunity can require different nutritional mixtures. Here, we show how dietary protein-carbohydrate balance affects social immunity in ants. When challenged with a parasitic fungus Metarhizium anisopliae, workers reared on a high-carbohydrate diet survived approximately 2.8× longer in worker groups than in solitary conditions, whereas workers reared on an isocaloric, high-protein diet survived only approximately 1.3× longer in worker groups versus solitary conditions. Nutrition had little effect on social grooming, a potential mechanism for social immunity. However, experimentally blocking metapleural glands, which secrete antibiotics, completely eliminated effects of social grouping and nutrition on immunity, suggesting a causal role for secretion exchange. A carbohydrate-rich diet also reduced worker mortality rates when whole colonies were challenged with Metarhizium. These results provide a novel mechanism by which carbohydrate exploitation could contribute to the ecological dominance of ants and other social groups.

Integrating remote international experience and community engagement into course-based animal behavior research.

Human-centered, active-learning approaches can help students develop core competencies in biology and other STEM fields, including the ability to conduct research, use quantitative reasoning, communicate across disciplinary boundaries, and connect science education to pressing social and environmental challenges. Promising approaches for incorporating active learning into biology courses include the use of course-based research, community engagement, and international experiences. Disruption to higher education due to the COVID-19 pandemic made each of these approaches more challenging or impossible to execute. Here, we describe a scalable course-based undergraduate research experience (CURE) for an animal behavior course that integrates research and community engagement in a remote international experience. Students in courses at two U.S. universities worked with community partners to analyze the behavior of African goats grazing near informal settlements in Western Cape, South Africa. Partners established a relationship with goat herders, and then created 2-min videos of individual goats that differed in criteria (goat sex and time of day) specified by students. Students worked in small groups to choose dependent variables, and then compared goat behavior across criteria using a factorial design. In postcourse surveys, students from both universities indicated overall enthusiasm for the experience. In general, students indicated that the laboratory provided them with "somewhat more" of a research-based experience compared with biology laboratories they had taken of similar length, and "somewhat more" to "much more" of a community-engagement and international experience. Educational benefits were complemented by the fact that international educational partners facing economic hardship due to the pandemic received payment for services. Future iterations of the CURE can focus on goat behavior differences across ecological conditions to help herders increase production in the face of continued environmental and social challenges. More generally, applying the structure of this CURE could facilitate mutually beneficial collaborations with residents of under-resourced areas around the world.

Potential for urban agriculture to support accessible and impactful undergraduate biology education.

Active learning in STEM education is essential for engaging the diverse pool of scholars needed to address pressing environmental and social challenges. However, active learning formats are difficult to scale and their incorporation into STEM teaching at U.S. universities varies widely. Here, we argue that urban agriculture as a theme can significantly increase active learning in undergraduate biology education by facilitating outdoor fieldwork and community-engaged education. We begin by reviewing benefits of field courses and community engagement activities for undergraduate biology and discuss constraints to their broader implementation. We then describe how urban agriculture can connect biology concepts to pressing global changes, provide field research opportunities, and connect students to communities. Next, we assess the extent to which urban agriculture and related themes have already been incorporated into biology-related programs in the United States using a review of major programs, reports on how campus gardens are used, and case studies from five higher education institutions (HEIs) engaging with this issue. We found that while field experiences are fairly common in major biology programs, community engagement opportunities are rare, and urban agriculture is almost nonexistent in course descriptions. We also found that many U.S. HEIs have campus gardens, but evidence suggests that they are rarely used in biology courses. Finally, case studies of five HEIs highlight innovative programming but also significant opportunities for further implementation. Together, our results suggest that urban agriculture is rarely incorporated into undergraduate biology in the United States, but there are significant prospects for doing so. We end with recommendations for integrating urban agriculture into undergraduate biology, including the development of campus gardens, research programs, community engagement partnerships, and collaborative networks. If done with care, this integration could help students make community contributions within required coursework, and help instructors feel a greater sense of accomplishment in an era of uncertainty.

How urbanization affects sexual communication.

Urbanization is rapidly altering landscapes worldwide, changing environmental conditions, and creating novel selection pressures for many organisms. Local environmental conditions affect the expression and evolution of sexual signals and mating behaviors; changes in such traits have important evolutionary consequences because of their effect on reproduction. In this review, we synthesize research investigating how sexual communication is affected by the environmental changes associated with urbanization-including pollution from noise, light, and heavy metals, habitat fragmentation, impervious surfaces, urban heat islands, and changes in resources and predation. Urbanization often has negative effects on sexual communication through signal masking, altering condition-dependent signal expression, and weakening female preferences. Though there are documented instances of seemingly adaptive shifts in trait expression, the ultimate impact on fitness is rarely tested. The field of urban evolution is still relatively young, and most work has tested whether differences occur in response to various aspects of urbanization. There is limited information available about whether these responses represent phenotypic plasticity or genetic changes, and the extent to which observed shifts in sexual communication affect reproductive fitness. Our understanding of how sexual selection operates in novel, urbanized environments would be bolstered by more studies that perform common garden studies and reciprocal transplants, and that simultaneously evaluate multiple environmental factors to tease out causal drivers of observed phenotypic shifts. Urbanization provides a unique testing ground for evolutionary biologists to study the interplay between ecology and sexual selection, and we suggest that more researchers take advantage of these natural experiments. Furthermore, understanding how sexual communication and mating systems differ between cities and rural areas can offer insights on how to mitigate negative, and accentuate positive, consequences of urban expansion on the biota, and provide new opportunities to underscore the relevance of evolutionary biology in the Anthropocene.

Nutrition and interference competition have interactive effects on the behavior and performance of Argentine ants.

Food availability often influences competitive outcomes through effects on consumer growth. Although it has received less attention, food availability may also affect competition through nutritional effects on behavior. One hypothesis linking nutrition and competition in ants posits that increased access to carbohydrates favors greater investment in worker traits that underlie behavioral dominance. We tested this hypothesis by varying dietary protein:carbohydrate (P:C) ratios and levels of interspecific interference for Argentine ants (Linepithema humile), a widespread invasive species. As predicted, colonies facing interference increased patrolling more when reared on low P:C diets; this result is the first demonstration of an interactive effect of nutrition and interference on ant colonies. Several results suggest that this dietary effect on patrolling was due primarily to changes in colony size rather than worker behavior. Colonies on lower P:C diets had lower worker mortality and larger final colony sizes. Diet had little effect on per capita patrolling, and worker behavior in performance assays depended more on previous exposure to interference than on diet. Our findings indicate that dietary P:C ratios can influence Argentine ant performance in a competitive environment and suggest a mechanism by which monopolization of carbohydrate-rich resources can help invasive ants displace native ant competitors.

Long-term burning interacts with herbivory to slow decomposition.

Fires can generate spatial variation in trophic interactions such as insect herbivory. If trophic interactions mediated by fire influence nutrient cycling, they could feed back on the more immediate consequences of fire on nutrient dynamics. Here we consider herbivore-induced effects on oak litter quality and decomposition within a long-term manipulation of fire frequency in central Minnesota, USA. We focused on bur oak (Quercus macrocarpa) trees, which are common across the fire frequency gradient and are often heavily infested with either lace bugs (Corythuca arcuata) or aphids (Hoplochaithropsus quercicola). We used targeted exclusion to test for herbivore-specific effects on litter chemistry and subsequent decomposition rates. Lace bug exclusion led to lower lignin concentrations in litterfall and subsequently accelerated decomposition. In contrast, aphid exclusion had no effect on litterfall chemistry or on decomposition rate, despite heavy infestation levels. Effects of lace bug herbivory on litterfall chemistry and decomposition were similar in burned and unburned areas. However, lace bug herbivory was much more common in burned than in unburned areas, whereas aphid herbivory was more common in unburned areas. These results suggest that frequent fires promote oak-herbivore interactions that decelerate decomposition. This effect should amplify other influences of fire that slow nitrogen cycling.

Linking nutrition and behavioural dominance: carbohydrate scarcity limits aggression and activity in Argentine ants.

Predicting the outcome of competitive interactions is a fundamental goal in ecology. Ecological stoichiometry, which relates nutrient balance to ecological processes, provides a framework for identifying mechanistic links among macronutrient availability, nutritional physiology and competitive performance. Because carbohydrates serve as a principal metabolic fuel, carbohydrate scarcity may impinge upon behaviours affecting competitive dominance (e.g. aggression, activity) to a greater extent than deficiencies of protein or other nutrients used preferentially for growth. Here, we tested this prediction with a diet manipulation study involving laboratory colonies of Argentine ants (Linepithema humile), a widespread and aggressive invasive species. The availability of both sucrose and insect prey influenced brood production and worker survival after three months. However, colonies became less aggressive and less active only when deprived of sucrose (but not prey). Scarcity of sucrose (but not prey) was also associated with reduced fat mass in individual workers. These data provide the first experimental support that carbohydrate scarcity compromises aggression and activity in ants, and illustrate, in principle, how access to carbohydrate-rich resources (e.g. plant exudates, hemipteran honeydew) might influence behavioural investments that contribute to competitive performance. Such investments might be especially important for invasive ants, given their aggressiveness and tendency to interact with honeydew-producing Hemiptera.

Response to phosphorus limitation varies among lake populations of the freshwater snail Potamopyrgus antipodarum.

Local adaptation--typically recognized as higher values of fitness-related traits for native vs. non-native individuals when measured in the native environment--is common in natural populations because of pervasive spatial variation in the intensity and type of natural selection. Although local adaptation has been primarily studied in the context of biotic interactions, widespread variation in abiotic characteristics of environments suggests that local adaptation in response to abiotic factors should also be common. Potamopyrgus antipodarum, a freshwater New Zealand snail that is an important model system for invasion biology and the maintenance of sexual reproduction, exhibits local adaptation to parasites and rate of water flow. As an initial step to determining whether P. antipodarum are also locally adapted to phosphorus availability, we examined whether populations differ in their responses to phosphorus limitation. We found that field-collected juvenile P. antipodarum grew at a lower rate and reached an important size threshold more slowly when fed a relatively low vs. a relatively high-phosphorus diet. We also detected significant across-population variation in individual growth rate. A marginally significant population-by-dietary phosphorus interaction along with a two-fold difference across populations in the extent of suppression of growth by low phosphorus suggests that populations of P. antipodarum may differ in their response to phosphorus limitation. Local adaptation may explain this variation, with the implication that snails from lakes with relatively low phosphorus availability should be less severely affected by phosphorus limitation than snails from lakes with higher phosphorus availability.

Sensitivity to phosphorus limitation increases with ploidy level in a New Zealand snail.

Evolutionary and ecological factors that explain natural variation in ploidy level remain poorly understood. One intriguing possibility is that nutrient costs associated with higher per-cell nucleic acid content could differentially influence the fitness of different ploidy levels. Here, we test this hypothesis by determining whether access to phosphorus (P), a main component of nucleic acids, differentially affects growth rate in asexual freshwater snails (Potamopyrgus antipodarum) that differ in ploidy. As expected if larger genomes generate higher dietary P requirements, tetraploid P. antipodarum experienced a more than twofold greater reduction in growth rate in low-P versus high-P conditions relative to triploids. Mirroring these results, tetraploid P. antipodarum also had a significant reduction in body P content under low P relative to high P, whereas triploid body P content was unaffected. Taken together, these results set the stage for the possibility that P availability could influence the distribution and relative frequency of P. antipodarum of different ploidy levels. These findings could be applicable to many other animal taxa featuring ploidy-level variation, which includes many mixed sexual/asexual taxa.

Correlated biogeographic variation of magnesium across trophic levels in a terrestrial food chain.

Using samples from eastern China (c. 25 - 41° N and 99 - 123° E) and from a common garden experiment, we investigate how Mg concentration varies with climate across multiple trophic levels. In soils, plant tissue (Oriental oak leaves and acorns), and a specialist acorn predator (the weevil Curculio davidi), Mg concentration increased significantly with different slopes from south to north, and generally decreased with both mean annual temperature (MAT) and precipitation (MAP). In addition, soil, leaf, acorn and weevil Mg showed different strengths of association and sensitivity with climatic factors, suggesting that distinct mechanisms may drive patterns of Mg variation at different trophic levels. Our findings provide a first step toward determining whether anticipated changes in temperature and precipitation due to climate change will have important consequences for the bioavailability and distribution of Mg in food chain.

Productivity is a poor predictor of plant species richness.

For more than 30 years, the relationship between net primary productivity and species richness has generated intense debate in ecology about the processes regulating local diversity. The original view, which is still widely accepted, holds that the relationship is hump-shaped, with richness first rising and then declining with increasing productivity. Although recent meta-analyses questioned the generality of hump-shaped patterns, these syntheses have been criticized for failing to account for methodological differences among studies. We addressed such concerns by conducting standardized sampling in 48 herbaceous-dominated plant communities on five continents. We found no clear relationship between productivity and fine-scale (meters(-2)) richness within sites, within regions, or across the globe. Ecologists should focus on fresh, mechanistic approaches to understanding the multivariate links between productivity and richness.

Stoichiometric response of nitrogen-fixing and non-fixing dicots to manipulations of CO2, nitrogen, and diversity.

Human activities have resulted in increased nitrogen deposition and atmospheric CO(2) concentrations in the biosphere, potentially causing significant changes in many ecological processes. In addition to these ongoing perturbations of the abiotic environment, human-induced losses of biodiversity are also of major concern and may interact in important ways with biogeochemical perturbations to affect ecosystem structure and function. We have evaluated the effects of these perturbations on plant biomass stoichiometric composition (C:N:P ratios) within the framework of the BioCON experimental setup (biodiversity, CO(2), N) conducted at the Cedar Creek Natural History Area, Minnesota. Here we present data for five plant species: Solidago rigida, Achillea millefolium, Amorpha canescens, Lespedeza capitata, and Lupinus perennis. We found significantly higher C:N and C:P ratios under elevated CO(2) treatments, but species responded idiosyncratically to the treatment. Nitrogen addition decreased C:N ratios, but this response was greater in the ambient CO(2) treatments than under elevated CO(2). Higher plant species diversity generally lowered both C:N and C:P ratios. Importantly, increased diversity also led to a more modest increase in the C:N ratio with elevated CO(2) levels. In addition, legumes exhibited lower C:N and higher C:P and N:P ratios than non-legumes, highlighting the effect of physiological characteristics defining plant functional types. These data suggest that atmospheric CO(2) levels, N availability, and plant species diversity interact to affect both aboveground and belowground processes by altering plant elemental composition.