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 CT_min and CT_maxs (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 CT_maxs using a thermal dry bath to eliminate boundary layer effects: body size correlations observed previously disappeared. In both experiments, consistent with Thermal Adaptation, CT_maxs 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 CT_max 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.     

Lower thermal tolerance in nocturnal than in diurnal ants: a challenge for nocturnal ectotherms facing global warming

1. The thermal adaptation hypothesis proposes that because thermoregulation involves a high metabolic cost, thermal limits of organisms must be locally adapted to temperatures experienced in their environments. There is evidence that tolerance to high temperatures decreases in insects inhabiting colder habitats and microclimates. However, it is not clear if thermal limits of ectotherms with contrasting temporal regimes, such as diurnal and nocturnal insects, are also adapted to temperatures associated with their circadian activities. 2. This study explores differences in heat tolerance among diurnal and nocturnal ant species in four ecosystems in Mexico: tropical montane, tropical rainforest, subtropical dry forests, and high‐elevation semi‐desert. 3. The critical thermal maximum (CT_max), i.e. the temperature at which ants lost motor control, was estimated for diurnal and nocturnal species. CT_max for 19 diurnal and 12 nocturnal ant species distributed among 45 populations was also estimated. 4. Semi‐desert and subtropical dry forest ants displayed higher tolerances to high temperatures than did ants in tropical rainforest. The lowest tolerance to high temperatures was recorded in tropical montane forest ants. In general, among all habitats, the CT_max of nocturnal ants was lower than that of diurnal ants. 5. An increase in nocturnal temperatures, combined with lower tolerance to high temperatures, may represent a substantial challenge for nocturnal ectotherms in a warming world.     

Body size and microclimate use in Neotropical granivorous ants

The stability of tropical microclimates has left microclimate use by tropical species little unexplored. At La Selva Costa Rica, I related foraging activity at seed baits to humidity in two forests types. I recorded 38 and 35 ant species at seed baits in closed and open canopy forest. The microclimate 5 cm above the forest floor in the younger, Open Forest was warmer, drier, more variable, and more sensitive to current weather than in the older Closed Forest. Ant species within both forests foraged at different Vapor Pressure Deficits (kPa), a measure of the drying power of the air. VPD use was not confounded with diel activity patterns. Body size explained 46% of the variance in mean VPD use among ant species. Small ant species tended to forage in moist microclimates; large species tended to be microclimate generalists. Larger species were also more active in the drier Open Forest. Foraging activity by these assemblages varies 4-fold, and peaks close to the mean VPD for each habitat. The behavior of these assemblages suggest that 1) small ant species at La Selva potentially compete with the entire range of ant body sizes, whereas large ants forage when and where small ants are inactive; and 2) seeds dispersed to the forest floor at dawn will be consumed or further dispersed by a larger suite of ants species than those falling in the heat of the tropical afternoon.     

The distribution of vascular epiphytes over gradients of light and humidity in north‐east Australian rainforest

Microclimatic conditions have a strong influence on the distribution of vascular epiphytes, among which orchids often occur in sunnier and more drought‐prone situations than ferns. However, very few studies have looked at the distribution of ferns and orchids in Australian tropical rainforests. By using transmitted light measurements at the locations of individual epiphytes and vapour pressure deficit from the canopy and base of host trees, we were able to determine the patterns of light and humidity in the rainforest environment, and the responses of ferns and orchids to variation in the physical environments. We surveyed five sites, ranging from 800 to 1180 m in elevation in the lower montane rainforests of north‐east Australia. Data loggers recorded the vapour pressure deficit (VPD) at the forest floor and canopy of each site. Light was correlated with height within the host tree and VPD differed significantly over position in the host tree and elevation. There was a strong partitioning of taxonomic groups over the light and VPD gradients. Orchids occurred in environments that had higher mean light levels and mean daily maximum VPD (27% and 0.43 kPa, respectively) than ferns (21% and 0.28 kPa). There was also strong microclimatic partitioning of species within taxonomic groups, suggesting that microclimatic factors play an important role in the realized niche spaces of epiphytes within the tropical Australian rainforest. Thus, the tested ecological generalizations made on tropical rainforest epiphytes apply in Australia.     

Within-tree distribution of nest sites and foraging areas of ants on canopy trees in a tropical rainforest in Borneo

It has been argued that canopy trees in tropical rainforests harbor species-rich ant assemblages; however, how ants partition the space on trees has not been adequately elucidated. Therefore, we investigated within-tree distributions of nest sites and foraging areas of individual ant colonies on canopy trees in a tropical lowland rainforest in Southeast Asia. The species diversity and colony abundance of ants were both significantly greater in crowns than on trunks. The concentration of ant species and colonies in the tree crown seemed to be associated with greater variation in nest cavity type in the crown, compared to the trunk. For ants nesting on canopy trees, the numbers of colonies and species were both higher for ants foraging only during the daytime than for those foraging at night. Similarly, for ants foraging on canopy trees, both values were higher for ants foraging only during the daytime than for those foraging at night. For most ant colonies nesting on canopy trees, foraging areas were limited to nearby nests and within the same type of microhabitat (within-tree position). All ants foraging on canopy trees in the daytime nested on canopy trees, whereas some ants foraging on the canopy trees at night nested on the ground. These results suggest that spatial partitioning by ant assemblages on canopy trees in tropical rainforests is affected by microenvironmental heterogeneity generated by three-dimensional structures (e.g., trees, epiphytes, lianas, and aerial soils) in the crowns of canopy trees. Furthermore, ant diversity appears to be enriched by both temporal (diel) and fine-scale spatial partitioning of foraging activity.     

Effects of selective logging on the arboreal ants of a Bornean rainforest

We examined the effect of selective logging and corresponding forest canopy loss on arboreal ant diversity in a tropical rainforest. Arboreal ants were collected from an unlogged forest plot and from forest plots selectively logged 14 years and 24 years earlier in Danum Valley, Sabah, Malaysia, using a canopy fogging method. Selective logging was associated with a significant decrease in canopy cover and an increase in understory vegetation density relative to unlogged forest. Our study showed that selective logging in primary forest might not dramatically decrease total species number and overall abundance of arboreal ants; however, it may influence the species composition and dominance structure of the ant community, accompanied by an increase in abundance of shrub‐layer species and trophobiotic species. In view of the results of this study, management techniques that minimize logging impact on understory vegetation structure are likely to help maintain the conservation value of logged forests for arboreal ants. Our results also suggest that accurate assessment of the impacts on biodiversity should not be based only on measurement of species number and overall abundance, but also on analysis of species composition and community structure.     

Effects of an Epiphytic Orchid on Arboreal Ant Community Structure in Panama

Epiphytes are conspicuous structural elements of tropical forest canopies. Individual tree crowns in lowland forests may support more than 30 ant species, yet we know little about the effects of epiphytes on ant diversity. We examined the composition of arboreal ant communities on Annona glabra trees and their interactions with the epiphytic orchid Caularthron bilamellatum in Panama. We surveyed the ants on 73 trees (45 with C. bilamellatum and 28 lacking epiphytes) and recorded their nest sites and behavioral dominance at baits. We found a total of 49 ant species (in 20 genera), ranging 1–9 species per tree. Trees with C. bilamellatum had higher average (±SD) ant species richness (4.2±2.28) than trees without epiphytes (2.7±1.21). Hollow pseudobulbs (PBs) of C. bilamellatum were used as nest sites by 32 ant species, but only 43 percent of suitable PBs were occupied. Ant species richness increased with PB abundance in trees, but nest sites did not appear to be a limiting resource on A. glabra. We detected no close association between ants and the orchid. We conclude that higher ant species richness in the presence of the orchid is due to bottom‐up effects, especially the year‐round supply of extrafloral nectar. The structure of ant communities on A. glabra partly reflects interference competition among behaviorally dominant species and stochastic factors, as observed in other forests.     

Canopy Openness Enhances Diversity of Ant–Plant Interactions in the Brazilian Amazon Rain Forest

In closed‐canopy tropical forest understory, light availability is a significant determinant of habitat diversity because canopy structure is highly variable in most tropical forests. Consequently, variation in canopy cover affects the composition and distribution of plant species via creating variable light environments. Nevertheless, little is known about how variation in canopy openness structures patterns of plant–animal interactions. Because of the great diversity and dominance of ants in tropical environments, we used ant–plant interactions as a focal network to evaluate how variation in canopy cover influences patterns of plant–insect interactions in the Brazilian Amazon rain forest. We observed that small increases in canopy openness are associated with increased diversity of ant–plant interactions in our study area, and this change is independent of plant or ant species richness. Additionally, we found smaller niche overlap for both ants and plants associated with greater canopy openness. We hypothesize that enhanced light availability increases the breadth of ant foraging sources because variation in light availability gives rise to plant resources of different quality and amounts. Moreover, greater light availability promotes vegetative growth in plants, creating ant foraging ‘bridges’ between plants. In sum, our results highlight the importance of environmental heterogeneity as a determinant of ant–plant interaction diversity in tropical environments.     

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 (CT_max). 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.     

Day vs. night predation on artificial caterpillars in primary rainforest habitats – an experimental approach

The influence of natural enemies has led to the evolution of various predator avoidance strategies in herbivorous insects. Many caterpillars are exclusively active at night and rest during the day. It is widely assumed that nocturnal activity in caterpillars reduces their risk of falling prey to their natural enemies. To test this hypothesis, we compared predation pressure between day and night in tree‐fall gaps and closed‐canopy forest sites in an Amazonian primary lowland rainforest. Artificial clay caterpillars, showing camouflaged colouration (green), were exposed as potential prey to a natural predator community. Attacks were significantly more frequent during daytime and were reduced by about a quarter at night in tree‐fall gaps, and by a third in closed‐canopy forest sites. This supports the idea of time‐dependent activity in caterpillars as an antipredatory adaptation. Further, independent of the time of day, predation pressure on caterpillars was significantly higher in tree‐fall gaps compared to closed‐canopy forest habitats. Nearly all predation events were caused by arthropods, whereas birds played a negligible role. Across both habitat types and time scales, ants acted as major predator group, emphasising their important role in population control of herbivorous insects in lowland rainforest ecosystems. This is the first experimental study using artificial caterpillars to examine whether time‐scheduling of exposition might influence predation risk amongst undefended, solitary, free‐living lepidopteran larvae.     

Photosynthetic responses to vapour pressure deficit in temperate and tropical evergreen rainforest trees of Australia

Rainforests occur in high precipitation areas of eastern Australia, along a gradient in seasonality of precipitation, ranging from a summer dry season in the temperate south to a winter dry season in the tropical north. The response of net photosynthesis to increasing vapour pressure deficit (VPD) was measured in a range of Australian rainforest trees from different latitudes to investigate possible differences in their response to atmospheric drought. Plants were grown in glasshouses under ambient or low VPD to determine the effect of growth VPD on the photosynthetic response. Temperate species, which experience low summer precipitation, were found to maintain maximum net photosynthesis over the measurement range of VPD (0.5–1.9 kPa). In contrast, the tropical species from climates with high summer precipitation showed large reductions in net photosynthesis with increasing VPD. Temperate species showed higher intrinsic water-use efficiencies under low VPD than the tropical species, whereas their efficiencies were similar under high VPD. Growing plants under a low VPD had little effect on either the photosynthetic response to VPD or the intrinsic water-use efficiency of the species. These different responses of gas exchange to VPD shown by the tropical and temperate rainforest species may reflect different strategies to maximise productivity in their respective climates.     

Desiccation Tolerance and Global Change: Implications for Tropical Bryophytes in Lowland Forests

Global change puts an increasing pressure on tropical forests and their inherent diversity by the risk of longer droughts and drier microclimatic conditions within the forest. How organisms will respond is uncertain, especially for organisms highly depending on their microclimatic environment such as bryophytes. An adequate tolerance to desiccation is important to face these changes, however, little is known for tropical bryophytes. We investigated for the first time the desiccation tolerance of epiphytic bryophytes from contrasting microsites at the tropical lowland forest in French Guiana. Using chlorophyll‐fluorescence (F_v/F_m) as an indicator of recovery, we tested: (1) desiccation tolerance for short (3 d) and long (9 d) desiccation events; (2) different desiccation intensities; and (3) recovery by rehydration with water vapor. Species from the canopy were well adapted to desiccation events. Thirteen of 18 species maintained more than 75 percent of their photosynthetic capacity after recovery at the strongest desiccation treatment of 9 d at 43 percent relative humidity (RH). In contrast, species from the understory were sensitive and withstood desiccation only at humid conditions of 75 percent RH and higher. The photosystem of the studied bryophytes was reactivated efficiently in equilibration with water vapor only—a yet neglected phenomenon in bryology. A novel introduced desiccation tolerance index allows global comparison of desiccation tolerances and highlights the sensitivity of understory species. Our results suggest that decreasing humidity caused by climate change and forest degradation could be a concerning threat for understory species.     

Testing associational resistance against pine weevils mediated by Lasius ants attending conifer seedlings

Natural enemies attracted to plants may provide those plants with protection against herbivores but may also protect neighbouring plants, that is through associational resistance. Ant attendance may be an important mechanism for the occurrence of such effects because ants can reduce the damage caused by a wide variety of herbivorous insects. Ants have been shown, in a previous field experiment, to decrease the damage caused by the pine weevil, Hylobius abietis (L.) (Coleoptera: Curculionidae), a pest species that causes high seedling mortality in forest regeneration areas. In this study, we specifically tested whether seedlings planted close to ant‐attended seedlings experience associational resistance. We did this under laboratory conditions using the ant species Lasius niger (L.) (Hymenoptera: Formicidae). The feeding damage by pine weevils was significantly reduced on seedlings attended by ants. The neighbouring seedlings, however, did not experience associational resistance. Nevertheless, some associational effects were observed as the number of weevils recorded on both ant‐attended and neighbouring seedlings was significantly lower compared with ant‐excluded seedlings.     

Novel interactions of non-pollinating ants with pollinators and fruit consumers in a tropical forest

The tropical ants Ectatomma ruidum and E. tuberculatum (Formicidae) regularly patrol leaves, flowers, and fruits of the understory shrub, Psychotria limonensis (Rubiaceae), on Barro Colorado Island, Panama. Ant and pollinator exclusion experiments elucidated both positive and negative effects of ant attendance on plant reproductive success, including pollination, fruit set, fruit loss, and fruit removal. Ants did not pollinate flowers but did contribute to higher pollination success, probably by increasing the relocation frequency of winged pollinators and thus the rate of flower visitation. Ants also prevented fruit loss to herbivorous insects which were common during the early stages of fruit development. Thus, ant attendance strongly improved both pollination and fruit set whereby plants with ants set more fruit per flower and also lost fewer fruits during fruit maturation. In contrast, ants had a negative effect on the removal of ripe fruits by avian frugivores. Thus, ant attendance has a non-trivial influence on plant reproduction, this interaction being beneficial at some stages of the plant reproductive cycle and carrying costs at another stage. A tight ecological or co-evolved relationship between these Ectatomma spp. and P. limonensis is unlikely given that ant attendance of plants is detrimental to fruit removal. Received: 18 May 1998 / Accepted: 1 March 1999     

Spatial Variation in Army Ant Swarm Raiding and its Potential Effect on Biodiversity

Invertebrate communities of the tropical rain forest floor are highly diverse, characterized by patchy species distribution patterns and high variation in species density. Spatial variation in the foraging activity of swarm raiding army ants, prime invertebrate predators in tropical rain forests, is discussed as a mechanism contributing to these patterns, but highly resolved long‐term data on army ant raiding on the local and landscape scale are hitherto lacking. In this study, 196 positions in 11 study sites in a tropical rain forest in western Kenya were continuously monitored over ~4 mo for the occurrence of swarm raids of army ants. Using population simulation analyses, the consequences of army ant raiding for prey communities were assessed. We found an unexpectedly high variation in raid rates at the study site and landscape scale. The weekly chance of communities to become raided by army ants was on average 0.11, but ranged from 0 to 0.50 among the 196 positions. Simulating population developments of two Lotka–Volterra species—showing slight trade‐offs between competitive strength and resistance to army ant raids—in the real raiding landscapes showed that the observed spatial variation in raid rates may produce high prey diversity at larger spatial scales (due to high β‐diversity) and strong variation in species density. Our results indicate that high spatial variation in army ant swarm raiding is a mechanism capable of generating patchy species distribution patterns and maintaining the high biodiversity of invertebrate communities of the tropical rain forest floor.     

Abiotic mediation of a mutualism drives herbivore abundance

Species abundance is typically determined by the abiotic environment, but the extent to which such effects occur through the mediation of biotic interactions, including mutualisms, is unknown. We explored how light environment (open meadow vs. shaded understory) mediates the abundance and ant tending of the aphid Aphis helianthi feeding on the herb Ligusticum porteri. Yearly surveys consistently found aphids to be more than 17‐fold more abundant on open meadow plants than on shaded understory plants. Manipulations demonstrated that this abundance pattern was not due to the direct effects of light environment on aphid performance, or indirectly through host plant quality or the effects of predators. Instead, open meadows had higher ant abundance and per capita rates of aphid tending and, accordingly, ants increased aphid population growth in meadow but not understory environments. The abiotic environment thus drives the abundance of this herbivore exclusively through the mediation of a protection mutualism.     

Collapse of an ant–scale mutualism in a rainforest on Christmas Island

Positive interactions play a widespread role in facilitating biological invasions. Here we use a landscape–scale ant exclusion experiment to show that widespread invasion of tropical rainforest by honeydew-producing scale insects on Christmas Island (Indian Ocean) has been facilitated by positive interactions with the invasive ant Anoplolepis gracilipes . Toxic bait was used to exclude A. gracilipes from large (9–35 ha) forest patches. Within 11 weeks, ant activity on the ground and on trunks had been reduced by 98–100%, while activity on control plots remained unchanged. The exclusion of ants caused a 100% decline in the density of scale insects in the canopies of three rainforest trees in 12 months ( Inocarpus fagifer , Syzygium nervosum and Barringtonia racemosa ), but on B. racemosa densities of scale insects also declined in control plots, resulting in no effect of ant exclusion on this species. This study demonstrates the role of positive interactions in facilitating biological invasions, and supports recent models calling for greater recognition of the role of positive interactions in structuring ecological communities.     

Strategic Management of an Invasive Ant‐scale Mutualism Enables Recovery of a Threatened Tropical Tree Species

Mutualisms between invasive ants and honeydew‐producing insects can have widespread negative effects on natural ecosystems. This is becoming an increasingly serious problem worldwide, causing certain ecosystems to change radically. Management of these abundant and influential mutualistic species is essential if the host ecosystem is to recover to its former non‐invaded status. This negative effect is particularly prevalent on some tropical islands, including Cousine Island, Seychelles. On this island, the invasive ant Pheidole megacephala has caused serious indirect damage to the threatened native Pisonia grandis trees via a mutualism with an invasive scale insect, Pulvinaria urbicola. We aimed to suppress the ant, thereby decoupling the mutualism and enabling recovery of the Pisonia trees. We treated all areas where ant pressure was high with a selective formicidal bait, which was deployed in custom‐made bait stations designed to avoid risk of treatment to endemic fauna. In the treated area, ant foraging activity was reduced by 93 percent and was followed by a 100 percent reduction in scale insect density. Abundance of endemic herbivorous insects and herbivorous activity increased significantly, however, after the decline in mutualistic species densities. Despite the native herbivore increase, there was considerable overall improvement in Pisonia shoot condition and an observed increase in foliage density. Our results demonstrate the benefit of strategic management of highly mutualistic alien species to the native Pisonia trees. It also supports the idea that area‐wide suppression is a feasible alternative to eradication for achieving positive conservation management at the level of the forest ecosystem.     

Midday depression of photosynthesis in <Emphasis Type="Italic">Enkleia malaccensis</Emphasis>, a woody climber in a tropical rainforest

We measured the diurnal changes in net photosynthetic rate (P _N) and stomatal conductance (g _s) of the leaves of a liana, Enkleia malaccensis Griff. (Thymelaeaceae), at the canopy level in the lowland tropical rainforest at Pasoh, Peninsular Malaysia. The measurements were made from a canopy walkway system, 30 m from the ground for 3 d in March 2003. P _N increased with increasing photosynthetically active radiation (PAR) before noon, though P _N was not enhanced by the strong radiation hit in the afternoon. Plotting g _s at saturating PAR (>0.5 mmol m⁻² s⁻¹) against the vapour pressure deficit (VPD) failed to reveal a significant correlation between VPD and g _s, and g _s became very low at VPD >2.5 kPa. The relationship between P _N and g _s was fitted on the same regression line irrespective of measuring day, indicating that this relationship was not influenced by either VPD or leaf temperature (T _L). Therefore, in the liana E. malaccensis, an increase in VPD leads to partial stomatal closure and, subsequently, reductions in P _N and the midday depression of P _N of this plant.