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.

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.

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.

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.

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.

Adhesion and Running Speed of a Tropical Arboreal Ant (Cephalotes atratus) on Rough, Narrow, and Inclined Substrates.

Arboreal ants must navigate variably sized and inclined linear structures across a range of substrate roughness when foraging tens of meters above the ground. To achieve this, arboreal ants use specialized adhesive pads and claws to maintain effective attachment to canopy substrates. Here, we explored the effect of substrate structure, including small and large-scale substrate roughness, substrate diameter, and substrate orientation (inclination), on adhesion and running speed of workers of one common, intermediately-sized, arboreal ant species. Normal (orthogonal) and shear (parallel) adhesive performance varied on sandpaper and natural leaf substrates, particularly at small size scales, but running speed on these substrates remained relatively constant. Running speed also varied minimally when running up and down inclined substrates, except when the substrate was positioned completely vertical. On vertical surfaces, ants ran significantly faster down than up. Ant running speed was slower on relatively narrow substrates. The results of this study show that variation in the physical properties of tree surfaces differentially affects arboreal ant adhesive and locomotor performance. Specifically, locomotor performance was much more robust to surface roughness than was adhesive performance. The results provide a basis for understanding how performance correlates of functional morphology contribute to determining local ant distributions and foraging decisions in the tropical rainforest canopy.

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.

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.

Connectivity explains local ant community structure in a Neotropical forest canopy: a large-scale experimental approach.

Understanding how habitat structure and resource availability affect local species distributions is a key goal of community ecology. Where habitats occur as a mosaic, variation in connectivity among patches influences both local species richness and composition, and connectivity is a key conservation concern in fragmented landscapes. Similarly, availability of limiting resources frequently determines species coexistence or exclusion. For primarily cursorial arthropods like ants, gaps between neighboring trees are a significant barrier to movement through the forest canopy. Competition for limited resources such as nest sites also promotes antagonistic interactions. Lianas (woody vines) connect normally isolated neighboring tree crowns and often have hollow stems inhabited by ants. We used two large-scale liana-removal experiments to determine how connectivity and nest site availability provided by lianas affect arboreal ant species richness, species composition, and ß-diversity in a lowland tropical forest in Panama. Removing lianas from a tree crown reduced ant species richness up to 35%, and disproportionately affected species that require large foraging areas. Adding artificial connectivity to trees mitigated the effects of liana removal. Ant colonization of artificial nests was higher (73% occupied) in trees without lianas vs. trees with lianas (28% occupied). However, artificial nests typically were colonized by existing polydomous, resident ant species. As a result, nest addition did not affect ant community structure. Collectively, these results indicate that lianas are important to the maintenance of arboreal ant diversity specifically by providing connectivity among neighboring tree crowns. Anticipated increases in liana abundance in this forest could increase the local (tree-level) species richness of arboreal ants, with a compositional bias toward elevating the density of broad-ranging specialist predators.

Adhesion and running speed of a tropical arboreal ant (Cephalotes atratus) on wet substrates.

In the tropical forest canopy, wingless worker ants must cling to and run along diverse vegetative surfaces with little protection from sun, wind and rain. Ants rely in part on their tiny adhesive tarsal pads to maintain sufficient contact with substrates to prevent falls under these varied conditions. Here, we examined the effects of substrate wettability and surface water on the tarsal pad adhesive performance of a common tropical arboreal ant. Ant adhesion was consistently higher on an intermediately wetting substrate (static water contact angle ca 90°) when resisting both perpendicular (normal) force and parallel (shear) force. Normal adhesion was maintained on intermediately wetting and hydrophobic substrates following the addition of rain-mimicking water droplets, whereas shear adhesion declined on all substrate types tested after wetting. Ant running speed was slower on wet substrates. On wood substrates, normal and shear adhesion declined with increasing wetness from dry, to misted, to water-soaked. These differences probably contributed to lower ant running speed on wet wood. The results of this study provide the first quantitative assessment of tropical arboreal ant adhesive performance under substrate conditions that are commonly encountered in the rainforest canopy.

Jumping and the aerial behavior of aquatic mayfly larvae (Myobaetis ellenae, Baetidae).

Mayfly larvae generally are aquatic, but some madicolous taxa (i.e., living in thin water films) crawl over rocks within streams and waterfalls. When startled, these larvae can break the water film, jump, and enter an aerial phase of locomotion. Because mayfly larvae have been suggested as potential exemplars for the origin of insect wings as tracheal gills, and furthermore represent the most basal extant lineage of pterygotes, we analyzed jumping behavior and free-fall trajectories for one such species of mayfly (Myobaetis ellenae, Baetidae) in Costa Rica. Jumping was commonplace in this taxon, but was undirected and was characterized by body spinning at high angular velocities. No aerodynamic role for the tracheal gills was evident. By contrast, jumping by a sympatric species of bristletail (Meinertellus sp., Archaeognatha) consistently resulted in head-first and stable body postures during aerial translation. Although capable of intermittently jumping into the air, the mayfly larvae could neither control nor target their aerial behavior. By contrast, a stable body posture during jumps in adult bristletails, together with the demonstrated capacity for directed aerial descent in arboreal representatives of this order, support ancestrally terrestrial origins for insect flight within the behavioral context of either jumping or falling from heights.

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.

Effects of lightning on trees: A predictive model based on in situ electrical resistivity.

The effects of lightning on trees range from catastrophic death to the absence of observable damage. Such differences may be predictable among tree species, and more generally among plant life history strategies and growth forms. We used field-collected electrical resistivity data in temperate and tropical forests to model how the distribution of power from a lightning discharge varies with tree size and identity, and with the presence of lianas. Estimated heating density (heat generated per volume of tree tissue) and maximum power (maximum rate of heating) from a standardized lightning discharge differed 300% among tree species. Tree size and morphology also were important; the heating density of a hypothetical 10 m tall Alseis blackiana was 49 times greater than for a 30 m tall conspecific, and 127 times greater than for a 30 m tall Dipteryx panamensis. Lianas may protect trees from lightning by conducting electric current; estimated heating and maximum power were reduced by 60% (±7.1%) for trees with one liana and by 87% (±4.0%) for trees with three lianas. This study provides the first quantitative mechanism describing how differences among trees can influence lightning-tree interactions, and how lianas can serve as natural lightning rods for trees.

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.

Quantification and identification of lightning damage in tropical forests.

Accurate estimates of tree mortality are essential for the development of mechanistic forest dynamics models, and for estimating carbon storage and cycling. However, identifying agents of tree mortality is difficult and imprecise. Although lightning kills thousands of trees each year and is an important agent of mortality in some forests, the frequency and distribution of lightning-caused tree death remain unknown for most forests. Moreover, because all evidence regarding the effects of lightning on trees is necessarily anecdotal and post hoc, rigorous tests of hypotheses regarding the ecological effects of lightning are impossible. We developed a combined electronic sensor/camera-based system for the location and characterization of lightning strikes to the forest canopy in near real time and tested the system in the forest of Barro Colorado Island, Panama. Cameras mounted on towers provided continuous video recordings of the forest canopy that were analyzed to determine the locations of lightning strikes. We used a preliminary version of this system to record and locate 18 lightning strikes to the forest over a 3-year period. Data from field surveys of known lightning strike locations (obtained from the camera system) enabled us to develop a protocol for reliable, ground-based identification of suspected lightning damage to tropical trees. In all cases, lightning damage was relatively inconspicuous; it would have been overlooked by ground-based observers having no knowledge of the event. We identified three types of evidence that can be used to consistently identify lightning strike damage in tropical forests: (1) localized and directionally biased branch mortality associated with flashover among tree and sapling crowns, (2) mortality of lianas or saplings near lianas, and (3) scorched or wilting epiphytic and hemiepiphytic plants. The longitudinal trunk scars that are typical of lightning-damaged temperate trees were never observed in this study. Given the prevalence of communications towers worldwide, the lightning detection system described here could be implemented in diverse forest types. Data from multiple systems would provide an outstanding opportunity for comparative research on the ecological effects of lightning. Such comparative data are increasingly important given expected increases in lightning frequency with climatic change.

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.

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.

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.