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.

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.

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.

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.

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.

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.

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.

Abundance of introduced species at home predicts abundance away in herbaceous communities.

Many ecosystems worldwide are dominated by introduced plant species, leading to loss of biodiversity and ecosystem function. A common but rarely tested assumption is that these plants are more abundant in introduced vs. native communities, because ecological or evolutionary-based shifts in populations underlie invasion success. Here, data for 26 herbaceous species at 39 sites, within eight countries, revealed that species abundances were similar at native (home) and introduced (away) sites - grass species were generally abundant home and away, while forbs were low in abundance, but more abundant at home. Sites with six or more of these species had similar community abundance hierarchies, suggesting that suites of introduced species are assembling similarly on different continents. Overall, we found that substantial changes to populations are not necessarily a pre-condition for invasion success and that increases in species abundance are unusual. Instead, abundance at home predicts abundance away, a potentially useful additional criterion for biosecurity programmes.

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.

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.

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.

First recorded mating flight of the hypogeic ant, Acropyga epedana, with its obligate mutualist mealybug, Rhizoecus colombiensis.

On 26-July, 2005 a mating aggregation of Acropyga epedana Snelling (Hymenoptera: Formicidae) was observed in the Chiricahua Mountains in south-eastern Arizona. This is the first record of a mating flight of A. epedana, the only nearctic member of this pantropical genus. Mating behavior was observed, newly mated queens were collected, and a complete colony was excavated. New information is reported on the natural history and mating behavior of the species. The identity of a mealybug mutualist, Rhizoecus colombiensis (Homoptera: Rhizoecinae) is confirmed. Reproductive females participating in flights all carried mealybugs between their mandibles, indicating a vertical transfer of mealybugs with their ant hosts. No captured foundresses survived long in captivity, most likely due to the death of their mealybugs. The colony excavated had a single queen, though polygyny is common in the genus. Nearly all workers within the nest were heavily parasitized by mites, although males or gynes were not parasitized. These natural history observations are discussed with regard to this poorly understood mutualistic relationship between Acropyga ants and their mealybug partners.

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