Lianas increase lightning-caused disturbance severity in a tropical forest.

Lightning is an important agent of plant mortality and disturbance in forests. Lightning-caused disturbance is highly variable in terms of its area of effect and disturbance severity (i.e. tree damage and death), but we do not know how this variation is influenced by forest structure and plant composition. We used a novel lightning detection system to quantify how lianas influenced the severity and spatial extent (i.e. area) of lightning disturbance using 78 lightning strikes in central Panama. The local density of lianas (measured as liana basal area) was positively associated with the number of trees killed and damaged by lightning, and patterns of plant damage indicated that this occurred because lianas facilitated more electrical connections from large to small trees. Liana presence, however, did not increase the area of the disturbance. Thus, lianas increased the severity of lightning disturbance by facilitating damage to additional trees without influencing the footprint of the disturbance. These findings indicate that lianas spread electricity to damage and kill understory trees that otherwise would survive a strike. As liana abundance increases in tropical forests, their negative effects on tree survival with respect to the severity of lightning-related tree damage and death are likely to increase.

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.

Lightning is a major cause of large tree mortality in a lowland neotropical forest.

The mortality rates of large trees are critical to determining carbon stocks in tropical forests, but the mechanisms of tropical tree mortality remain poorly understood. Lightning strikes thousands of tropical trees every day, but is commonly assumed to be a minor agent of tree mortality in most tropical forests. We use the first systematic quantification of lightning-caused mortality to show that lightning is a major cause of death for the largest trees in an old-growth lowland forest in Panama. A novel lightning strike location system together with field surveys of strike sites revealed that, on average, each strike directly kills 3.5 trees (> 10 cm diameter) and damages 11.4 more. Given lightning frequency data from the Earth Networks Total Lightning Network and historical total tree mortality rates for this site, we conclude that lightning accounts for 40.5% of the mortality of large trees (> 60 cm diameter) in the short term and probably contributes to an additional 9.0% of large tree deaths over the long term. Any changes in cloud-to-ground lightning frequency due to climatic change will alter tree mortality rates; projected 25-50% increases in lightning frequency would increase large tree mortality rates in this forest by 9-18%. The results of this study indicate that lightning plays a critical and previously underestimated role in tropical forest dynamics and carbon cycling.

Pantropical geography of lightning-caused disturbance and its implications for tropical forests.

Lightning is a major agent of disturbance, but its ecological effects in the tropics are unquantified. Here we used ground and satellite sensors to quantify the geography of lightning strikes in terrestrial tropical ecosystems, and to evaluate whether spatial variation in lightning frequency is associated with variation in tropical forest structure and dynamics. Between 2013 and 2018, tropical terrestrial ecosystems received an average of 100.4 million lightning strikes per year, and the frequency of strikes was spatially autocorrelated at local-to-continental scales. Lightning strikes were more frequent in forests, savannas, and urban areas than in grasslands, shrublands, and croplands. Higher lightning frequency was positively associated with woody biomass turnover and negatively associated with aboveground biomass and the density of large trees (trees/ha) in forests across Africa, Asia, and the Americas. Extrapolating from the only tropical forest study that comprehensively assessed tree damage and mortality from lightning strikes, we estimate that lightning directly damages c. 832 million trees in tropical forests annually, of which c. 194 million die. The similarly high lightning frequency in tropical savannas suggests that lightning also influences savanna tree mortality rates and ecosystem processes. These patterns indicate that lightning-caused disturbance plays a major and largely unappreciated role in pantropical ecosystem dynamics and global carbon cycling.

Adhesive performance of tropical arboreal ants varies with substrate temperature.

The surface temperature of tree branches in the tropical rainforest canopy can reach up to 55°C. Ants and other small cursorial organisms must maintain adequate attachment in this extreme microenvironment to forage effectively and avoid falling. Ant adhesion depends on liquid secretions that should become less viscous at high temperatures, causing ants to slip. However, tropical arboreal ants have high thermal tolerance and actively forage on hot canopy surfaces, suggesting that these ants can maintain adhesion on hot substrates. We measured tarsal pad shear adhesion of 580 workers (representing 11 species and four subfamilies) of tropical arboreal ants at temperatures spanning the range observed in the field (23-55°C). Adhesive performance among species showed three general trends: (1) a linear decrease with increasing temperature, (2) a non-linear relationship with peak adhesive performance at ca. 30-40°C, and (3) no relationship with temperature. The mechanism responsible for these large interspecific differences remains to be determined, but likely reflects variation in the composition of the secreted adhesive fluid. Understanding such differences will reveal the diverse ways that ants cope with highly variable, and often unpredictable, thermal conditions in the forest canopy.

Thermal constraints on foraging of tropical canopy ants.

Small cursorial ectotherms risk overheating when foraging in the tropical forest canopy, where the surfaces of unshaded tree branches commonly exceed 50 °C. We quantified the heating and subsequent cooling rates of 11 common canopy ant species from Panama and tested the hypothesis that ant workers stop foraging at temperatures consistent with the prevention of overheating. We created hot experimental "sunflecks" on existing foraging trails of four ant species from different clades and spanning a broad range of body size, heating rate, and critical thermal maxima (CTmax). Different ant species exhibited very different heating rates in the lab, and these differences did not follow trends predicted by body size alone. Experiments with ant models showed that heating rates are strongly affected by color in addition to body size. Foraging workers of all species showed strong responses to heating and consistently abandoned focal sites between 36 and 44 °C. Atta colombica and Azteca trigona workers resumed foraging shortly after heat was removed, but Cephalotes atratus and Dolichoderus bispinosus workers continued to avoid the heated patch even after >5 min of cooling. Large foraging ants (C. atratus) responded slowly to developing thermal extremes, whereas small ants (A. trigona) evacuated sunflecks relatively quickly, and at lower estimated body temperatures than when revisiting previously heated patches. The results of this study provide the first field-based insight into how foraging ants respond behaviorally to the heterogeneous thermal landscape of the tropical forest canopy.

Out on a limb: Thermal microenvironments in the tropical forest canopy and their relevance to ants.

Small, cursorial ectotherms like ants often are immersed in the superheated air layers that develop millimeters above exposed, insolated surfaces (i.e., the thermal boundary layer). We quantified the thermal microenvironments around tree branches in the tropical rainforest canopy, and explored the effects of substrate color on the internal body temperature and species composition of arboreal ants. Branch temperatures during the day (09:00-16:00) were hottest (often > 50°C) and most variable on the upper surface, while the lowest and least variable temperatures occurred on the underside. Temperatures on black substrates declined with increasing distance above the surface in both the field and the laboratory. By contrast, a micro-scale temperature inversion occurred above white substrates. Wind events (ca. 2ms-1) eliminated these patterns. Internal temperatures of bodies of Cephalotes atratus workers experimentally heated in the laboratory were 6°C warmer on white vs. black substrates, and 6°C cooler than ambient in windy conditions. The composition of ant species foraging at baits differed between black-painted and unpainted tree branches, with a tendency for smaller ants to avoid the significantly hotter black surfaces. Collectively, these outcomes show that ants traversing canopy branches experience very heterogeneous thermal microenvironments that are partly influenced in predictable ways by branch surface coloration and breezy conditions.

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.

The descent of ant: field-measured performance of gliding ants.

Gliding ants avoid predatory attacks and potentially mortal consequences of dislodgement from rainforest canopy substrates by directing their aerial descent towards nearby tree trunks. The ecologically relevant measure of performance for gliding ants is the ratio of net horizontal to vertical distance traveled over the course of a gliding trajectory, or glide index. To study variation in glide index, we measured three-dimensional trajectories of Cephalotes atratus ants gliding in natural rainforest habitats. We determined that righting phase duration, glide angle, and path directness all significantly influence variation in glide index. Unsuccessful landing attempts result in the ant bouncing off its target and being forced to make a second landing attempt. Our results indicate that ants are not passive gliders and that they exert active control over the aerodynamic forces they experience during their descent, despite their apparent lack of specialized control surfaces.

Variation in thermal tolerance of North American ants.

Changing climates are predicted to alter the distribution of thermal niches. Small ectotherms such as ants may be particularly vulnerable to heat injury and death. We quantified the critical thermal maxima of 92 ant colonies representing 14 common temperate ant species. The mean CTmax for all measured ants was 47.8 °C (±0.27; range=40.2-51.2 °C), and within-colony variation was lower than among-colony variation. Critical thermal maxima differed among species and were negatively correlated with body size. Results of this study illustrate the importance of accounting for mass, among and within colony variation, and interspecific differences in diel activity patterns, which are often neglected in studies of ant thermal physiology.

First case reports of Ignatzschineria (Schineria) indica associated with myiasis.

We report three cases of infection due to the Gram-negative rod Ignatzschineria (Schineria) indica involving bacteremia and the urinary tract. Two cases were clearly associated with maggot infestation, and the third could conceivably have had unrecognized maggot infestation of the urinary tract. We believe these cases to be the first I. indica infections reported in association with maggot infestation and myiasis.

Sodium shortage as a constraint on the carbon cycle in an inland tropical rainforest.

Sodium (Na) is uncommon in plants but essential to the metabolism of plant consumers, both decomposers and herbivores. One consequence, previously unexplored, is that as Na supplies decrease (e.g., from coastal to inland forests), ecosystem carbon should accumulate as detritus. Here, we show that adding NaCl solution to the leaf litter of an inland Amazon forest enhanced mass loss by 41%, decreased lignin concentrations by 7%, and enhanced decomposition of pure cellulose by up to 50%, compared with stream water alone. These effects emerged after 13-18 days. Termites, a common decomposer, increased 7-fold on +NaCl plots, suggesting an agent for the litter loss. Ants, a common predator, increased 2-fold, suggesting that NaCl effects cascade upward through the food web. Sodium, not chloride, was likely the driver of these patterns for two reasons: two compounds of Na (NaCl and NaPO(4)) resulted in equivalent cellulose loss, and ants in choice experiments underused Cl (as KCl, MgCl(2), and CaCl(2)) relative to NaCl and three other Na compounds (NaNO(3), Na(3)PO(4), and Na(2)SO(4)). We provide experimental evidence that Na shortage slows the carbon cycle. Because 80% of global landmass lies >100 km inland, carbon stocks and consumer activity may frequently be regulated via Na limitation.

Variation in Larval Thermal Tolerance of Three Saproxylic Beetle Species.

Temperature is a key abiotic condition that limits the distributions of organisms, and forest insects are particularly sensitive to thermal extremes. Whereas winged adult insects generally are able to escape unfavorable temperatures, other less-vagile insects (e.g., larvae) must withstand local microclimatic conditions to survive. Here, we measured the thermal tolerance of the larvae of three saproxylic beetle species that are common inhabitants of coarse woody debris (CWD) in temperate forests of eastern North America: Lucanus elaphus Fabricius (Lucanidae), Dendroides canadensis Latreille (Pyrochroidae), and Odontotaenius disjunctus Illiger (Passalidae). We determined how their critical thermal maxima (CTmax) vary with body size (mass), and measured the thermal profiles of CWD representing the range of microhabitats occupied by these species. Average CTmax differed among the three species and increased with mass intraspecifically. However, mass was not a good predictor of thermal tolerance among species. Temperature ramp rate and time in captivity also influenced larval CTmax, but only for D. canadensis and L. elaphus respectively. Heating profiles within relatively dry CWD sometimes exceeded the CTmax of the beetle larvae, and deeper portions of CWD were generally cooler. Interspecific differences in CTmax were not fully explained by microhabitat association, but the results suggest that the distribution of some species within a forest can be affected by local thermal extremes. Understanding the responses of saproxylic beetle larvae to warming habitats will help predict shifts in community structure and ecosystem functioning in light of climate change and increasing habitat fragmentation.

Tropical tree species differ in damage and mortality from lightning.

Lightning is an important agent of mortality for large tropical trees with implications for tree demography and forest carbon budgets. We evaluated interspecific differences in susceptibility to lightning damage using a unique dataset of systematically located lightning strikes in central Panama. We measured differences in mortality among trees damaged by lightning and related those to damage frequency and tree functional traits. Eighteen of 30 focal species had lightning mortality rates that deviated from null expectations. Several species showed little damage and three species had no mortality from lightning, whereas palms were especially likely to die from strikes. Species that were most likely to be struck also showed the highest survival. Interspecific differences in tree tolerance to lightning suggest that lightning-caused mortality shapes compositional dynamics over time and space. Shifts in lightning frequency due to climatic change are likely to alter species composition and carbon cycling in tropical forests.

Directed aerial descent in canopy ants.

Numerous non-flying arboreal vertebrates use controlled descent (either parachuting or gliding sensu stricto) to avoid predation or to locate resources, and directional control during a jump or fall is thought to be an important stage in the evolution of flight. Here we show that workers of the neotropical ant Cephalotes atratus L. (Hymenoptera: Formicidae) use directed aerial descent to return to their home tree trunk with >80% success during a fall. Videotaped falls reveal that C. atratus workers descend abdomen-first through steep glide trajectories at relatively high velocities; a field experiment shows that falling ants use visual cues to locate tree trunks before they hit the forest floor. Smaller workers of C. atratus, and smaller species of Cephalotes more generally, regain contact with their associated tree trunk over shorter vertical distances than do larger workers. Surveys of common arboreal ants suggest that directed descent occurs in most species of the tribe Cephalotini and arboreal Pseudomyrmecinae, but not in arboreal ponerimorphs or Dolichoderinae. This is the first study to document the mechanics and ecological relevance of this form of locomotion in the Earth's most diverse lineage, the insects.

On the biogeography of salt limitation: a study of ant communities.

Sodium is an essential nutrient whose deposition in rainfall decreases with distance inland. The herbivores and microbial decomposers that feed on sodium-poor vegetation should be particularly constrained along gradients of decreasing sodium. We studied the use of sucrose and NaCl baits in 17 New World ant communities located 4-2757 km inland. Sodium use was higher in genera and subfamilies characterized as omnivores/herbivores compared with those classified as carnivores and was lower in communities embedded in forest litter than in those embedded in abundant vegetation. Sodium use was increased in ant communities further inland, as was preference for the baits with the highest sodium concentration. Sucrose use, a measure of ant activity, peaked in communities 10-100 km inland. We suggest that the geography of ant activity is shaped by sodium toxicity near the shore and by sodium deficit farther inland. Given the importance of ants in terrestrial ecosystems, changing patterns of rainfall with global change may ramify through inland food webs.

The contributions of lightning to biomass turnover, gap formation and plant mortality in a tropical forest.

Lightning is a common source of disturbance, but its ecological effects in tropical forests are largely undescribed. Here we quantify the contributions of lightning strikes to forest turnover and plant mortality in a lowland Panamanian forest using a real-time lightning monitoring system. We examined 2,195 lightning-damaged trees distributed among 93 different strikes. None exhibited scars or fires. On average, each strike disturbed 451 m2 (95% CI: 365-545 m2 ), created a canopy gap of 304 m2 (95% CI 198-454 m2 ), and caused 7.36 Mg of woody biomass turnover (CI: 5.36-9.65 Mg). Cumulatively, we estimate that lightning strikes in this forest create canopy gaps equaling 0.39% of forest canopy area, representing 20.1% of annual gap area formation, and are responsible for 16.1% of total woody biomass turnover. Trees, lianas, herbaceous climbers and epiphytes were killed by lightning at rates 8-29 times greater than their baseline mortality rates in undamaged control sites. The likelihood of lightning-caused death was higher for trees, lianas, and herbaceous climbers than for epiphytes, and high liana mortality suggests that lightning is an important driver of liana turnover. These results indicate that lightning influences gap dynamics, plant community composition and carbon storage capacity in some tropical forests.

Aerial manoeuvrability in wingless gliding ants (Cephalotes atratus).

In contrast to the patagial membranes of gliding vertebrates, the aerodynamic surfaces used by falling wingless ants to direct their aerial descent are unknown. We conducted ablation experiments to assess the relative contributions of the hindlegs, midlegs and gaster to gliding success in workers of the Neotropical arboreal ant Cephalotes atratus (Hymenoptera: Formicidae). Removal of hindlegs significantly reduced the success rate of directed aerial descent as well as the glide index for successful flights. Removal of the gaster alone did not significantly alter performance relative to controls. Equilibrium glide angles during successful targeting to vertical columns were statistically equivalent between control ants and ants with either the gaster or the hindlegs removed. High-speed video recordings suggested possible use of bilaterally asymmetric motions of the hindlegs to effect body rotations about the vertical axis during targeting manoeuvre. Overall, the control of gliding flight was remarkably robust to dramatic anatomical perturbations, suggesting effective control mechanisms in the face of adverse initial conditions (e.g. falling upside down), variable targeting decisions and turbulent wind gusts during flight.