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.

Quantifying nutrient recovery efficiency and loss from compost-based urban agriculture.

The use of compost in urban agriculture offers an opportunity to increase nutrient recycling in urban ecosystems, but recent studies have shown that compost application often results in phosphorus (P) being applied far in excess of crop nutrient demand, creating the potential for P loss through leachate and runoff. Management goals such as maximizing crop yields or maximizing the mass of nutrients recycled from compost may inadvertently result in P loss, creating a potential ecosystem disservice. Here, we report the results from the first two years of an experimental study in which four different crops grown in raised-bed garden plots with high background P and organic matter received one of two types of compost (municipal compost made from urban organics waste, or manure-based compost) at two different levels (applied based on crop N or P demand), while additional treatments received synthetic N and P fertilizer or no soil amendments. Because of the low N:P ratio of compost relative to crop nutrient uptake, compost application based on crop N demand resulted in overapplication of P. Crop yield did not differ among treatments receiving compost inputs, and the mass of P recovered in crops relative to P inputs decreased for treatments with higher compost application rates. Treatments receiving compost targeted to crop N demand had P leachate rates approximately twice as high as other treatments. These results highlight tradeoffs inherent in recycling nutrients through UA, but they also show that targeted compost application rates have the capacity to maintain crop yields while minimizing nutrient loss. UA has the potential to help close the urban nutrient loop, but if UA is to be scaled up in order to maximize potential social, economic, and environmental benefits, it is especially important to carefully manage nutrients to avoid ecosystem disservices from nutrient pollution.

Measuring the Fate of Compost-Derived Phosphorus in Native Soil below Urban Gardens.

The heavy reliance on compost inputs in urban gardening provides opportunities to recycle nutrients from the urban waste stream, but also creates potential for buildup and loss of soil phosphorus (P). We previously documented P in leachate from raised-bed garden plots in which compost had been applied, but the fate of this P is not known. Here, we measured P concentrations in soils below four or six-year-old urban garden plots that were established for research. We hypothesize that the soil P concentration and depth of P penetration will increase over time after gardens are established. Soil cores were collected in five garden plots of each age and quantified for inorganic weakly exchangeable P. Inorganic weakly exchangeable P was significantly elevated in native soil below garden plots (>35 cm deep) relative to reference soil profiles, and excess P decreased with increasing depth, although differences between garden plots of different ages were not significant. Our analysis shows that excess P from compost accumulates in native soil below urban garden plots. While urban agriculture has the potential to recycle P in urban ecosystems, over-application of compost has the potential to contribute to soil and water pollution.

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.

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.

Thermal adaptation and phosphorus shape thermal performance in an assemblage of rainforest ants.

We studied the Thermal Performance Curves (TPCs) of 87 species of rainforest ants and found support for both the Thermal Adaptation and Phosphorus-Tolerance hypotheses. TPCs relate a fitness proxy (here, worker speed) to environmental temperature. Thermal Adaptation posits that thermal generalists (ants with flatter, broader TPCs) are favored in the hotter, more variable tropical canopy compared to the cooler, less variable litter below. As predicted, species nesting in the forest canopy 1) had running speeds less sensitive to temperature; 2) ran over a greater range of temperatures; and 3) ran at lower maximum speeds. Tradeoffs between tolerance and maximum performance are often invoked for constraining the evolution of thermal generalists. There was no evidence that ant species traded off thermal tolerance for maximum speed, however. Phosphorus-Tolerance is a second mechanism for generating ectotherms able to tolerate thermal extremes. It posits that ants active at high temperatures invest in P-rich machinery to buffer their metabolism against thermal extremes. Phosphorus content in ant tissue varied three-fold, and as predicted, temperature sensitivity was lower and thermal range was higher in P-rich species. Combined, we show how the vertical distribution of hot and variable vs. cooler and stable microclimates in a single forest contribute to a diversity of TPCs and suggest that a widely varying P stoichiometry among these ants may drive some of these differences.

I don't want the money, I just want your time: How moral identity overcomes the aversion to giving time to prosocial causes.

Four studies show that moral identity reduces people's aversion to giving time-particularly as the psychological costs of doing so increase. In Study 1, we demonstrate that even when the cost of time and money are held equivalent, a moral cue enhances the expected self-expressivity of giving time-especially when it is given to a moral cause. We found that a moral cue reduces time aversion even when giving time was perceived to be unpleasant (Study 2), or when the time to be given was otherwise seen to be scarce (Study 3). Study 4 builds on these studies by examining actual giving while accounting for the real costs of time. In this study, we found that the chronic salience of moral identity serves as a buffer to time aversion, specifically as giving time becomes increasingly costly. These findings are discussed in terms of the time-versus-money literature and the identity literature. We also discuss policy implications for prosocial cause initiatives. (PsycINFO Database Record

Plant species' origin predicts dominance and response to nutrient enrichment and herbivores in global grasslands.

Exotic species dominate many communities; however the functional significance of species' biogeographic origin remains highly contentious. This debate is fuelled in part by the lack of globally replicated, systematic data assessing the relationship between species provenance, function and response to perturbations. We examined the abundance of native and exotic plant species at 64 grasslands in 13 countries, and at a subset of the sites we experimentally tested native and exotic species responses to two fundamental drivers of invasion, mineral nutrient supplies and vertebrate herbivory. Exotic species are six times more likely to dominate communities than native species. Furthermore, while experimental nutrient addition increases the cover and richness of exotic species, nutrients decrease native diversity and cover. Native and exotic species also differ in their response to vertebrate consumer exclusion. These results suggest that species origin has functional significance, and that eutrophication will lead to increased exotic dominance in grasslands.

Thermal adaptation generates a diversity of thermal limits in a rainforest ant community.

The Thermal Adaptation Hypothesis posits that the warmer, aseasonal tropics generates populations with higher and narrower thermal limits. It has largely been tested among populations across latitudes. However, considerable thermal heterogeneity exists within ecosystems: across 31 trees in a Panama rainforest, surfaces exposed to sun were 8 °C warmer and varied more in temperature than surfaces in the litter below. Tiny ectotherms are confined to surfaces and are variously submerged in these superheated boundary layer environments. We quantified the surface CTmin and CTmax s (surface temperatures at which individuals grew torpid and lost motor control, respectively) of 88 ant species from this forest; they ranged in average mass from 0.01 to 57 mg. Larger ants had broader thermal tolerances. Then, for 26 of these species we again tested body CTmax s using a thermal dry bath to eliminate boundary layer effects: body size correlations observed previously disappeared. In both experiments, consistent with Thermal Adaptation, CTmax s of canopy ants averaged 3.5-5 °C higher than populations that nested in the shade of the understory. We impaled thermocouples in taxidermy mounts to further quantify the factors shaping operative temperatures for four ant species representing the top third (1-30 mg) of the size distribution. Extrapolations suggest the smallest 2/3rds of species reach thermal equilibrium in <10s. Moreover, the large ants that walk above the convective superheated surface air also showed more net heating by solar radiation, with operative temperatures up to 4 °C higher than surrounding air. The thermal environments of this Panama rainforest generate a range of CTmax subsuming 74% of those previously recorded for ant populations worldwide. The Thermal Adaptation Hypothesis can be a powerful tool in predicting diversity of thermal limits within communities. Boundary layer temperatures are likely key to predicting the future of Earth's tiny terrestrial ectotherm populations.

Metabolism and the rise of fungus cultivation by ants.

Most ant colonies are comprised of workers that cooperate to harvest resources and feed developing larvae. Around 50 million years ago (MYA), ants of the attine lineage adopted an alternative strategy, harvesting resources used as compost to produce fungal gardens. While fungus cultivation is considered a major breakthrough in ant evolution, the associated ecological consequences remain poorly understood. Here, we compare the energetics of attine colony-farms and ancestral hunter-gatherer colonies using metabolic scaling principles within a phylogenetic context. We find two major energetic transitions. First, the earliest lower-attine farmers transitioned to lower mass-specific metabolic rates while shifting significant fractions of biomass from ant tissue to fungus gardens. Second, a transition 20 MYA to specialized cultivars in the higher-attine clade was associated with increased colony metabolism (without changes in garden fungal content) and with metabolic scaling nearly identical to hypometry observed in hunter-gatherer ants, although only the hunter-gatherer slope was distinguishable from isometry. Based on these evolutionary transitions, we propose that shifting living-tissue storage from ants to fungal mutualists provided energetic storage advantages contributing to attine diversification and outline critical assumptions that, when tested, will help link metabolism, farming efficiency, and colony fitness.

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.

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.

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.

Predicting invasion in grassland ecosystems: is exotic dominance the real embarrassment of richness?

Invasions have increased the size of regional species pools, but are typically assumed to reduce native diversity. However, global-scale tests of this assumption have been elusive because of the focus on exotic species richness, rather than relative abundance. This is problematic because low invader richness can indicate invasion resistance by the native community or, alternatively, dominance by a single exotic species. Here, we used a globally replicated study to quantify relationships between exotic richness and abundance in grass-dominated ecosystems in 13 countries on six continents, ranging from salt marshes to alpine tundra. We tested effects of human land use, native community diversity, herbivore pressure, and nutrient limitation on exotic plant dominance. Despite its widespread use, exotic richness was a poor proxy for exotic dominance at low exotic richness, because sites that contained few exotic species ranged from relatively pristine (low exotic richness and cover) to almost completely exotic-dominated ones (low exotic richness but high exotic cover). Both exotic cover and richness were predicted by native plant diversity (native grass richness) and land use (distance to cultivation). Although climate was important for predicting both exotic cover and richness, climatic factors predicting cover (precipitation variability) differed from those predicting richness (maximum temperature and mean temperature in the wettest quarter). Herbivory and nutrient limitation did not predict exotic richness or cover. Exotic dominance was greatest in areas with low native grass richness at the site- or regional-scale. Although this could reflect native grass displacement, a lack of biotic resistance is a more likely explanation, given that grasses comprise the most aggressive invaders. These findings underscore the need to move beyond richness as a surrogate for the extent of invasion, because this metric confounds monodominance with invasion resistance. Monitoring species' relative abundance will more rapidly advance our understanding of invasions.

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.

Towards a general life-history model of the superorganism: predicting the survival, growth and reproduction of ant societies.

Social insect societies dominate many terrestrial ecosystems across the planet. Colony members cooperate to capture and use resources to maximize survival and reproduction. Yet, when compared with solitary organisms, we understand relatively little about the factors responsible for differences in the rates of survival, growth and reproduction among colonies. To explain these differences, we present a mathematical model that predicts these three rates for ant colonies based on the body sizes and metabolic rates of colony members. Specifically, the model predicts that smaller colonies tend to use more energy per gram of biomass, live faster and die younger. Model predictions are supported with data from whole colonies for a diversity of species, with much of the variation in colony-level life history explained based on physiological traits of individual ants. The theory and data presented here provide a first step towards a more general theory of colony life history that applies across species and environments.

A life history continuum in the males of a Neotropical ant assemblage: refuting the sperm vessel hypothesis.

Animal lifespans range from a few days to many decades, and this life history diversity is especially pronounced in ants. Queens can live for decades. Males, in contrast, are often assumed to act as ephemeral sperm delivery vessels that die after a brief mating flight-a view developed from studies of lekking species in temperate habitats. In a tropical ant assemblage, we found that males can live days to months outside the nest, a trait hypothesized to be associated with female calling, another common mating system. We combined feeding experiments with respirometry to show that lifespan can be enhanced over 3 months by feeding outside the nest. In one focal female calling species, Ectatomma ruidum, feeding enhanced male lifespan, but not sperm content. Extended lifespans outside the nest suggest stronger than expected selection on premating traits of male ants, although the ways these traits shape male mating success remain poorly understood.

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.