Tropical ant community responses to experimental soil warming.

Climate change is one of the primary agents of the global decline in insect abundance. Because of their narrow thermal ranges, tropical ectotherms are predicted to be most threatened by global warming, yet tests of this prediction are often confounded by other anthropogenic disturbances. We used a tropical forest soil warming experiment to directly test the effect of temperature increase on litter-dwelling ants. Two years of continuous warming led to a change in ant community between warming and control plots. Specifically, six ant genera were recorded only on warming plots, and one genus only on control plots. Wasmannia auropuctata, a species often invasive elsewhere but native to this forest, was more abundant in warmed plots. Ant recruitment at baits was best predicted by soil surface temperature and ant heat tolerance. These results suggest that heat tolerance is useful for predicting changes in daily foraging activity, which is directly tied to colony fitness. We show that a 2-year increase in temperature (of 2-4°C) can have a profound effect on the most abundant insects, potentially favouring species with invasive traits and moderate heat tolerances.

Behavioral response to heat stress of twig-nesting canopy ants.

Tropical forests experience a relatively stable climate, but are not thermally uniform. The tropical forest canopy is hotter and thermally more variable than the understory. Heat stress in the canopy is expected to increase with global warming, potentially threatening its inhabitants. Here, we assess the impact of heating on the most abundant tropical canopy arthropods-ants. While foragers can escape hot branches, brood and workers inside twig nests might be unable to avoid heat stress. We examined nest choice and absconding behavior-nest evacuation in response to heat stress-of four common twig-nesting ant genera. We found that genera nesting almost exclusively in the canopy occupy smaller cavities compared to Camponotus and Crematogaster that nest across all forest strata. Crematogaster ants absconded at the lowest temperatures in heating experiments with both natural and artificial nests. Cephalotes workers were overall less likely to abscond from their nests. This is the first test of behavioral thermoregulation in tropical forest canopy ants, and it highlights different strategies and sensitivities to heat stress. Behavioral avoidance is the first line of defense against heat stress and will be crucial for small ectotherms facing increasing regional and local temperatures.

Increased acclimation ability accompanies a thermal niche shift of a recent invasion.

Globalization is removing dispersal barriers for the establishment of invasive species and enabling their spread to novel climates. New thermal environments in the invaded range will be particularly challenging for ectotherms, as their metabolism directly depends on environmental temperature. However, we know little about the role climatic niche shifts play in the invasion process, and the underlining physiological mechanisms. We tested if a thermal niche shift accompanies an invasion, and if native and introduced populations differ in their ability to acclimate thermal limits. We used an alien ant species-Tapinoma magnum-which recently started to spread across Europe. Using occurrence data and accompanying climatic variables, we measured the amount of overlap between thermal niches in the native and invaded range. We then experimentally tested the acclimation ability in native and introduced populations by incubating T. magnum at 18, 25 and 30°C. We measured upper and lower critical thermal limits after 7 and 21 days. We found that T. magnum occupies a distinct thermal niche in its introduced range, which is on average 3.5°C colder than its native range. Critical thermal minimum did not differ between populations from the two ranges when colonies were maintained at 25 or 30°C, but did differ after colony acclimation at a lower temperature. We found twofold greater acclimation ability of introduced populations to lower temperatures, after prolonged incubation at 18°C. Increased acclimation ability of lower thermal limits could explain the expansion of the realized thermal niche in the invaded range, and likely contributed to the spread of this species to cooler climates. Such thermal plasticity could be an important, yet so far understudied, factor underlying the expansion of invasive insects into novel climates.

Biogeochemistry and forest composition shape nesting patterns of a dominant canopy ant.

Humans are increasing nutrient deposition across the globe, and we know little about how these changes influence consumer populations in tropical rainforests. We used a long-term fertilization experiment conducted in a Panamanian forest to explore how nutrient availability and tree traits affect abundance of a higher-level consumer. We added nitrogen, phosphorus and potassium in a factorial design for 18 years. Given that phosphorus often limits ecosystem processes in lowland tropical forests, and added nitrogen reduces insect abundance in our experiment, we first hypothesized that phosphorus addition would increase nest density and nest size of Azteca chartifex ants while nitrogen addition would have the opposite effects. We found 48% lower nest density in the canopy of nitrogen addition plots relative to plots that did not receive nitrogen. Phosphorus addition did not affect nest density or size. These nutrient effects were not diminished by the selectivity of host trees. In general, larger trees held more nests, despite their low frequencies across the forest, while some abundant species (e.g., palms) were rarely used. We further predicted higher nest frequency on trees with extrafloral nectaries, because this ant fuels its large colonies with extrafloral nectar. Despite the non-random distribution of A. chartifex nests, across tree species and nutrient treatments, trees with extrafloral nectaries did not host more nests. Our study suggests that areas of a tropical lowland forest which are not oversaturated with nitrogen, and contain large trees, have higher nest density. This could enable A. chartifex in similar areas to outcompete other ants due to high abundance.

Plant responses to fertilization experiments in lowland, species-rich, tropical forests.

We present a meta-analysis of plant responses to fertilization experiments conducted in lowland, species-rich, tropical forests. We also update a key result and present the first species-level analyses of tree growth rates for a 15-yr factorial nitrogen (N), phosphorus (P), and potassium (K) experiment conducted in central Panama. The update concerns community-level tree growth rates, which responded significantly to the addition of N and K together after 10 yr of fertilization but not after 15 yr. Our experimental soils are infertile for the region, and species whose regional distributions are strongly associated with low soil P availability dominate the local tree flora. Under these circumstances, we expect muted responses to fertilization, and we predicted species associated with low-P soils would respond most slowly. The data did not support this prediction, species-level tree growth responses to P addition were unrelated to species-level soil P associations. The meta-analysis demonstrated that nutrient limitation is widespread in lowland tropical forests and evaluated two directional hypotheses concerning plant responses to N addition and to P addition. The meta-analysis supported the hypothesis that tree (or biomass) growth rate responses to fertilization are weaker in old growth forests and stronger in secondary forests, where rapid biomass accumulation provides a nutrient sink. The meta-analysis found no support for the long-standing hypothesis that plant responses are stronger for P addition and weaker for N addition. We do not advocate discarding the latter hypothesis. There are only 14 fertilization experiments from lowland, species-rich, tropical forests, 13 of the 14 experiments added nutrients for five or fewer years, and responses vary widely among experiments. Potential fertilization responses should be muted when the species present are well adapted to nutrient-poor soils, as is the case in our experiment, and when pest pressure increases with fertilization, as it does in our experiment. The statistical power and especially the duration of fertilization experiments conducted in old growth, tropical forests might be insufficient to detect the slow, modest growth responses that are to be expected.

Biogeochemistry drives diversity in the prokaryotes, fungi, and invertebrates of a Panama forest.

Humans are both fertilizing the world and depleting its soils, decreasing the diversity of aquatic ecosystems and terrestrial plants in the process. We know less about how nutrients shape the abundance and diversity of the prokaryotes, fungi, and invertebrates of Earth's soils. Here we explore this question in the soils of a Panama forest subject to a 13-yr fertilization with factorial combinations of nitrogen (N), phosphorus (P), and potassium (K) and a separate micronutrient cocktail. We contrast three hypotheses linking biogeochemistry to abundance and diversity. Consistent with the Stress Hypothesis, adding N suppressed the abundance of invertebrates and the richness of all three groups of organisms by ca. 1 SD or more below controls. Nitrogen addition plots were 0.8 pH units more acidic with 18% more exchangeable aluminum, which is toxic to both prokaryotes and eukaryotes. These stress effects were frequently reversed, however, when N was added with P (for prokaryotes and invertebrates) and with added K (for fungi). Consistent with the Abundance Hypothesis, adding P generally increased prokaryote and invertebrate diversity, and adding K enhanced invertebrate diversity. Also consistent with the Abundance Hypothesis, increases in invertebrate abundance generated increases in richness. We found little evidence for the Competition Hypothesis: that single nutrients suppressed diversity by favoring a subset of high nutrient specialists, and that nutrient combinations suppressed diversity even more. Instead, combinations of nutrients, and especially the cation/micronutrient treatment, yielded the largest increases in richness in the two eukaryote groups. In sum, changes in soil biogeochemistry revealed a diversity of responses among the three dominant soil groups, positive synergies among nutrients, and-in contrast with terrestrial plants-the frequent enhancement of soil biodiversity.

Insects in temperate urban parks face stronger selection pressure from the cold than the heat.

Urban areas experience higher temperatures compared to rural areas and as such, are increasingly considered places of acclimatization and adaptation to warming. Small ectotherms, such as insects, whose body temperature rises with habitat temperature, are directly affected by temperature changes. Thus, warming could have a profound effect on insect behavior and physiology. To test if the urban heat island effect drives higher thermal tolerance and activity changes, we used globally distributed and abundant insects-ants. We measured the heat and cold tolerance of 14 ant species distributed across urban and peri-urban areas. As thermal traits are often correlated with ant foraging, we measured foraging activity during three consecutive years across eight sites. Contrary to our prediction, ants exposed to the urban heat island effect did not have a higher heat tolerance than peri-urban ants. Instead, cold tolerance varied across habitats, with ants from the cooler, peri-urban habitats being able to tolerate lower temperatures. We recorded the same pattern of invariant heat and higher cold tolerance for ants in the canopy, compared to ground nesting ants. Ant activity was almost 10 times higher in urban sites and best predicted by cold, not heat tolerance. These unexpected results suggest that we need to rethink predictions about urban heat islands increasing insect heat tolerance in urban habitats, as cold tolerance might be a more plastic or adaptable trait, particularly in the temperate zone.

Temperature influences desiccation resistance of bumble bees.

Ongoing climate change has increased temperatures and the frequency of droughts in many parts of the world, potentially intensifying the desiccation risk for insects. Because resisting desiccation becomes more difficult at higher temperatures and lower humidity, avoiding water loss is a key challenge facing terrestrial insects. However, few studies have examined the interactive effects of temperature and environmental humidity on desiccation resistance in insects. Such studies on bees (Hymenoptera: Apoidea: Anthophila) are especially rare, despite their ecological and economic importance. Here, we crossed temperature (20, 25, and 30 °C) with humidity (<5, 50, >95 % RH) manipulations and measured time to mortality, water loss rates, and the water content at mortality of bumble bees (Bombus impatiens). We found that both higher temperature and lower humidity increased water loss rates, while warmer temperatures reduced survival time and lower humidity decreased water content at mortality. Additionally, we observed large intraspecific variation in water balance traits between colonies, and larger individuals survived longer and could tolerate more water loss before mortality. This study raises important questions about the mechanisms underpinning water loss in bumble bees and suggests that frequent access to nectar may be especially important for bumble bees' water balance and survival in a warming and drying climate.

Seasonal plasticity of thermal tolerance in ants.

Analyses of heat tolerance in insects often suggest that this trait is relatively invariant, leading to the use of fixed thermal maxima in models predicting future distribution of species in a warming world. Seasonal environments expose populations to a wide annual temperature variation. To evaluate the simplifying assumption of invariant thermal maxima, we quantified heat tolerance of 26 ant species across three seasons that vary two-fold in mean temperature. Our ultimate goal was to test the hypothesis that heat tolerance tracks monthly temperature. Ant foragers tested at the end of the summer, in September, had higher average critical thermal maximum (CTmax ) compared to those in March and December. Four out of five seasonal generalists, species actively foraging in all three focal months, had, on average, 6°C higher CTmax in September. The invasive fire ant, Solenopsis invicta, was among the thermally plastic species, but the native thermal specialists still maintained higher CTmax than S. invicta. Our study shows that heat tolerance can be plastic, and this should be considered when examining species-level adaptations. Moreover, the plasticity of thermal traits, while potentially costly, may also generate a competitive advantage over species with fixed traits and promote resilience to climate change.

Species energy and Thermal Performance Theory predict 20-yr changes in ant community abundance and richness.

In an era of rapid climate change, and with it concern over insect declines, we used two theories to predict 20-yr changes in 34 North American ant communities. The ecosystems, from deserts to hardwood forests, were first surveyed in the 1990s. When resurveyed in 2016-2017, they averaged 1°C warmer with 200 g C·m-2 ·yr-1 higher plant productivity. Ant colony abundance changed from -49% to +61%. Consistent with Thermal Performance Theory, colony abundance increased with temperature increases < 1°C, then decreased as a site's mean monthly temperature change increased up to +2.4°C. Consistent with Species Energy Theory, (1) ant abundance tracked changes in a measure of energy availability (net aboveground productivity, g C·m-2 ·yr-1 ) and (2) increases in colony abundance drove increases in local plot- and transect-level species richness but not that of Chao 2, an estimate of the size of the species pool. Even after accounting for these drivers, local species richness was still higher ~20 yr after the original surveys, likely due to the increased activity of ant workers. These results suggest community changes are predictable using theory from geographical ecology, and that warming can first enhance but may ultimately decrease the abundance of this important insect taxon.

Nutrition modifies critical thermal maximum of a dominant canopy ant.

While adaptive responses to climate gradients are increasingly documented, little is known about how individuals alter their upper thermal tolerances. Long-term increases in dietary carbohydrates can elevate upper thermal tolerances in insects. We explored how the nutritional state of a Neotropical canopy ant governs its CTmax - the temperature at which individuals lose muscle control. We predicted that Azteca chartifex workers recently fed a carbohydrate-rich diet, such as honeydew and extrafloral nectar, would use that energy to increase their CTmax. Moreover, if a carbohydrate-rich diet increases CTmax, then we predicted that ants from colonies with high CTmaxs feed at a lower trophic level, and thus have a higher carbon:nitrogen ratio. We used A. chartifex colonies from a long-term fertilization experiment where phosphorus addition increased A. chartifex foraging activity with respect to controls. As foraging activity can be governed by resource availability, we first measured CTmax of field collected colonies. In freshly collected field colonies, CTmax was 2°C higher in control plots. This difference disappeared when ants were provided with only water for 10h. Ants were then provided with a 10% sucrose solution ad lib which increased CTmax by 5°C. We thus support the hypothesis that enhanced carbohydrate nutrition enables higher thermal tolerance, but this does not appear to be linked to colony trophic status, higher carbon:nitrogen ratios, or higher total body phosphorus. This short-term thermal plasticity linked to carbohydrate nutrition demonstrates the importance of ant diet in shaping their physiological traits. It is especially relevant to ant species that maintain high abundance by feeding on plant exudates. In a rapidly warming world, carbohydrate availability and use may represent a new element for predicting population and community responses of herbivorous insects.

Desiccation resistance in tropical insects: causes and mechanisms underlying variability in a Panama ant community.

Desiccation resistance, the ability of an organism to reduce water loss, is an essential trait in arid habitats. Drought frequency in tropical regions is predicted to increase with climate change, and small ectotherms are often under a strong desiccation risk. We tested hypotheses regarding the underexplored desiccation potential of tropical insects. We measured desiccation resistance in 82 ant species from a Panama rainforest by recording the time ants can survive desiccation stress. Species' desiccation resistance ranged from 0.7 h to 97.9 h. We tested the desiccation adaptation hypothesis, which predicts higher desiccation resistance in habitats with higher vapor pressure deficit (VPD) - the drying power of the air. In a Panama rainforest, canopy microclimates averaged a VPD of 0.43 kPa, compared to a VPD of 0.05 kPa in the understory. Canopy ants averaged desiccation resistances 2.8 times higher than the understory ants. We tested a number of mechanisms to account for desiccation resistance. Smaller insects should desiccate faster given their higher surface area to volume ratio. Desiccation resistance increased with ant mass, and canopy ants averaged 16% heavier than the understory ants. A second way to increase desiccation resistance is to carry more water. Water content was on average 2.5% higher in canopy ants, but total water content was not a good predictor of ant desiccation resistance or critical thermal maximum (CT max), a measure of an ant's thermal tolerance. In canopy ants, desiccation resistance and CT max were inversely related, suggesting a tradeoff, while the two were positively correlated in understory ants. This is the first community level test of desiccation adaptation hypothesis in tropical insects. Tropical forests do contain desiccation-resistant species, and while we cannot predict those simply based on their body size, high levels of desiccation resistance are always associated with the tropical canopy.