Worker thermal tolerance in the thermophilic ant Cataglyphis cursor (Hymenoptera, Formicidae)

In the thermophilic ant genus Cataglyphis, species differing in their physical caste system have developed alternative mechanisms to face extreme heat by physiological and/or behavioural adaptations. In this study, we tested whether thermal tolerance is related to worker size in the ant Cataglyphis cursor that presents intermediate worker size compared with previously studied species (size range 3.5–10 mm). Thermal tolerance at two temperatures was tested in the laboratory on colonies originating from two habitats (seaside versus vineyard), known to differ in average worker size. As expected large workers were more resistant to high temperature than small workers, but the effect of worker size on thermal resistance was less pronounced under the more extreme temperatures. The pattern of thermal tolerance was similar in the two habitat types. After controlling for worker size, worker thermal tolerance significantly varied amongst colonies, but this variation was not related to colony size. Our results suggest that a higher thermal tolerance can confer an advantage to larger workers especially during foraging and are discussed in the context of the evolution of worker size in ants.     

Evolution of hybridogenetic lineages in Cataglyphis ants

In most social Hymenoptera, a diploid egg develops into either a queen or a worker depending on environmental conditions. Hybridogenetic Cataglyphis ants display a bizarre genetic system, where queen‐worker caste determination is primarily determined by genetic factors. In hybridogenetic populations, all workers are F1 hybrids of two distinct lineages, whereas new queens are nearly always pure‐lineage individuals produced by clonal reproduction. The distribution and evolutionary history of these hybridogenetic populations have not yet been thoroughly analysed. Here, we studied the phylogeographic distribution of hybridogenetic populations in two closely related Spanish species: Cataglyphis humeya and Cataglyphis velox. Hybridogenesis has been previously documented in a locality of C. velox, but whether this system occurs elsewhere within the range of the two species was yet unknown. Queens and workers from 66 localities sampled across the range of the species were genotyped at 18 microsatellite markers to determine whether queens were produced by parthenogenesis and whether workers were hybrids of divergent lineages. Populations with F1 hybrid workers were identified by combining genetic, geographical and mating assortments data. In most populations of C. velox, workers were found to be hybrids of two divergent lineages. Workers were however produced via random mating in two marginal populations of C. velox, and in all populations studied of its sister species C. humeya. High‐throughput sequencing data were obtained to confirm inferences based on microsatellites and to characterize relationships between populations. Our results revealed a complicated history of reticulate evolution that may account for the origin of hybridogenetic lineages in Cataglyphis.     

Acclimation responses to temperature vary with vertical stratification: implications for vulnerability of soil‐dwelling species to extreme temperature events

The occurrence of summer heat waves is predicted to increase in amplitude and frequency in the near future, but the consequences of such extreme events are largely unknown, especially for belowground organisms. Soil organisms usually exhibit strong vertical stratification, resulting in more frequent exposure to extreme temperatures for surface‐dwelling species than for soil‐dwelling species. Therefore soil‐dwelling species are expected to have poor acclimation responses to cope with temperature changes. We used five species of surface‐dwelling and four species of soil‐dwelling Collembola that habituate different depths in the soil. We tested for differences in tolerance to extreme temperatures after acclimation to warm and cold conditions. We also tested for differences in acclimation of the underlying physiology by looking at changes in membrane lipid composition. Chill coma recovery time, heat knockdown time and fatty acid profiles were determined after 1 week of acclimation to either 5 or 20 °C. Our results showed that surface‐dwelling Collembola better maintained increased heat tolerance across acclimation temperatures, but no such response was found for cold tolerance. Concordantly, four of the five surface‐dwelling Collembola showed up to fourfold changes in relative abundance of fatty acids after 1 week of acclimation, whereas none of the soil‐dwelling species showed a significant adjustment in fatty acid composition. Strong physiological responses to temperature fluctuations may have become redundant in soil‐dwelling species due to the relative thermal stability of their subterranean habitat. Based on the results of the four species studied, we expect that unless soil‐dwelling species can temporarily retreat to avoid extreme temperatures, the predicted increase in heat waves under climatic change renders these soil‐dwelling species more vulnerable to extinction than species with better physiological capabilities. Being able to act under a larger thermal range is probably costly and could reduce maximum performance at the optimal temperature.     

Rain shadow effects predict population differences in thermal tolerance of leaf-cutting ant workers (Atta cephalotes)

Tests of hypotheses for the evolution of thermal physiology often rely on mean temperatures, but mounting evidence suggests geographic variation in temperature extremes is also an important predictor of species’ thermal tolerances. Although the tropics are less thermally variable than higher latitude regions, rain shadows on the leeward sides of mountains can experience greater diel and seasonal variation in temperature than windward sites. Rain shadows provide opportunities to test predictions about the relationships of extreme temperatures with thermal physiology while controlling for latitude. We tested the hypothesis that populations of leaf-cutting ants (Atta cephalotes) in leeward, montane, and windward sites in Costa Rica would differ in upper thermal tolerances (CT_max) of workers. As predicted from rain shadow effects via extreme high temperatures, the leeward rain shadow site yielded the highest mean CT_max (rain shadow site 42.1 ± 0.3°C, Montane site 38.2 ± 0.5°C, and windward site 38.2 ± 0.3°C). This suggests that high-temperature extremes in tropical rain shadow forests can select for higher thermal tolerances. CT_max increased with worker body size within sites, but CT_max increased with body size more gradually at the two lowland sites, as predicted if local high temperatures selected more strongly on the most thermally vulnerable society members (small workers). This suggests that warmer lowland climates selected for colonies with less variation in heat tolerance than cooler high elevation climates.     

Thermal tolerance of sympatric hymenopteran parasitoid species: does it match seasonal activity?

Climatic changes result in an increased in mean temperature and in a higher incidence of extreme weather events such as heat and cold waves. For ectotherms, such as insect parasitoids, the ability to remain active under extreme climatic conditions is a significant key to fitness. The body size of individuals, and in particular their surface to volume ratio, may play a role in their resistance to thermal conditions. The thermal tolerances are investigated of two closely‐related sympatric parasitoid species [Aphidius avenae Haliday and Aphidius rhopalosiphi De Stefani‐Perez (Hymenoptera: Aphidiinae)] that have a similar ecology but differ in body size and phenologies. The critical thermal limits of individuals are assessed in both sexes of each parasitoid species and the influence of surface–volume ratios on their thermal tolerances. Aphidius avenae is less resistant to low temperatures and more resistant to high temperatures than A. rhopalosiphi. The lower surface to volume ratio of A. avenae individuals may help them to remain active in summer when experiencing heat waves. However, body size is not the sole factor that plays a role in differences of thermal tolerance between species and body size may not be an adaptation to extreme temperatures but rather a by‐product of developmental regulation. Closely‐related sympatric species from the same ecological guild can have different thermal tolerances that may allow them to occur within the same habitat. The present study also highlights the importance of clearly defining how to measure critical thermal limits to determine the thermal tolerance of a species.     

Phenotypic plasticity of immune defence linked with foraging activity in the ant Cataglyphis velox

Because immune defences are costly, life-history theories predict a modulation of immune investment according to its potential benefits. Social insects provide interesting models since infection risk may vary among individuals within a colony. In particular, the foraging workers, that have to leave the nest, suffer a higher infection risk and can contaminate their nest, which may favour high immune investments. However, evolutionary theories of aging predict that foragers should reduce their immune investment when they suffer high extrinsic mortality. To test these two predictions, we investigated the levels of phenoloxidase (PO) and prophenoloxidase, two important enzymes of the insect immune system, in workers of the ant Cataglyphis velox. We found a higher PO activity in foragers than in intra-nidal workers. This could result from an adaptive upregulation of the harmful PO (an enzyme potentially leading to autoimmune reactions) only when the risk of infection and wounding is high.     

Seed size and germination response: a relationship for fire-following plant species exposed to thermal shock

Thermal shock is well known to be an important stimulus for the germination of soil-stored seeds in fire-prone plant communities. Nevertheless, while the overall germination response of different species is known to vary, the interaction between seed size and germination to a range of thermal-shock temperatures is poorly understood. This interaction may be important in regulating post-fire plant community establishment, since larger seeds are able to emerge from deeper within the soil profile than smaller seeds, and are therefore likely to be insulated against high above-ground temperatures by a deeper soil covering. In this experiment we examined how germination of eight co-occurring Western Australian fire-followers was influenced by thermal shock, and whether germination was significantly correlated with seed size. We found that small-seeded species not only showed enhanced germination at higher temperatures, but that their ability to germinate at higher temperatures was also greater than that displayed by larger-seeded species. These findings suggest that while seed size may be a useful general predictor of post-fire recruitment success, under different fire regimes the interaction between seed size, maximum seedling emergence depth, and the ability to withstand different thermal-shock temperatures is complex and may confound recent predictive models.     

A temperate pollinator with high thermal tolerance is still susceptible to heat events predicted under future climate change

1. Mutualisms may be particularly vulnerable to climate change as interacting species are likely to respond differently, which could destabilise interactions. 2. Temperate zone insects typically experience mean temperatures below their thermal optima, making them less vulnerable than tropical insects to small increases in mean temperature. However, they are likely to experience a higher frequency of extreme heat events, putting mutualism persistence in jeopardy. 3. This study investigated the potential impacts of climate change on Pleistodontes imperialis, a temperate Australian fig wasp that pollinates Port Jackson figs (Ficus rubiginosa). Wasp emergence and longevity were measured at temperatures ranging from those commonly experienced in nature (25 °C) to high values (> 40 °C) that are currently infrequent, but which are becoming more common with climate change. 4. Wasp emergence was unaffected by temperatures up to 39 °C, but it declined drastically above 39 °C. Adult longevity was unaffected by temperatures up to 30 °C, but decreased at 35 °C and above. Low humidity reduced wasp longevity across all temperatures. 5. Fitness reductions were observed at temperatures ～5 °C above the summer daily mean maximum, suggesting that P. imperialis has a high thermal tolerance, but is vulnerable to extreme heat. Figs located in the shade may provide protected microhabitats under hot conditions. 6. Tropical pollinators may be threatened by small increases in mean temperature. In contrast, it is shown here that temperate pollinators may face a different primary threat from climate change – the increasing frequency of extreme heat events – despite their higher thermal tolerances.     

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.     

Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency?

Bumblebee workers vary greatly in size, unlike workers of most other social bees. This variability has not been adequately explained. In many social insects, size variation is adaptive, with different-sized workers performing different tasks (alloethism). Here we established whether workers of the bumblebee, Bombus terrestris (L.) (Hymenoptera; Apidae), exhibit alloethism. We quantified the size of workers engaging in foraging compared to those that remain in the nest, and confirmed that it is the larger bees that tend to forage (X±SE thorax widths 4.34±0.01 mm for nest bees and 4.93±0.02 mm for foragers). We then investigated whether large bees are better suited to foraging because they are able to transport heavier loads of food back to the nest. Both pollen and nectar loads of returning foragers were measured, demonstrating that larger bees do return with a heavier mass of forage. Foraging trip times were inversely related to bee size when collecting nectar, but were unrelated to bee size for bees collecting pollen. Overall, large bees brought back more nectar per unit time than small bees, but the rate of pollen collection appeared to be unrelated to size. The smallest foragers had a nectar foraging rate close to zero, presumably explaining why foragers tend to be large. Why might larger bees be better at foraging? Various explanations are considered: larger bees are able to forage in cooler conditions, may be able to forage over larger distances, and are perhaps also less vulnerable to predation. Conversely, small workers are presumably cheaper to produce and may be more nimble at within-nest tasks. Further research is needed to assess these possibilities. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Age-dependent and task-related volume changes in the mushroom bodies of visually guided desert ants, Cataglyphis bicolor

Desert ants of the genus Cataglyphis are skillful long-distance navigators employing a variety of visual navigational tools such as skylight compasses and landmark guidance mechanisms. However, the time during which this navigational toolkit comes into play is extremely short, as the average lifetime of a Cataglyphis forager lasts for only about 6 days. Here we show, by using immunohistochemistry, confocal microscopy, and three-dimensional reconstruction software, that even during this short period of adult life, Cataglyphis exhibits a remarkable increase in the size of its mushroom bodies, especially of the visual input region, the collar, if compared to age-matched dark-reared animals. This task-related increase rides on a much smaller age-dependent increase of the size of the mushroom bodies. Due to the variation in body size exhibited by Cataglyphis workers we use allometric analyses throughout and show that small animals exhibit considerably larger task-related increases in the sizes of their mushroom bodies than larger animals do. It is as if there were an upper limit of mushroom body size required for accomplishing the ant's navigational tasks.     

Using a historic drought and high‐heat event to validate thermal exposure predictions for ground‐dwelling birds

Deviations from typical environmental conditions can provide insight into how organisms may respond to future weather extremes predicted by climate modeling. During an episodic and multimonth heat wave event (i.e., ambient temperature up to 43.4°C), we studied the thermal ecology of a ground‐dwelling bird species in Western Oklahoma, USA. Specifically, we measured black bulb temperature (T_bb) and vegetation parameters at northern bobwhite (Colinus virginianus; hereafter bobwhite) adult and brood locations as well as at stratified random points in the study area. On the hottest days (i.e., ≥39°C), adults and broods obtained thermal refuge using tall woody cover that remained on average up to 16.51°C cooler than random sites on the landscape which reached >57°C. We also found that refuge sites used by bobwhites moderated thermal conditions by more than twofold compared to stratified random sites on the landscape but that T_bb commonly exceeded thermal stress thresholds for bobwhites (39°C) for several hours of the day within thermal refuges. The serendipitous high heat conditions captured in our study represent extreme heat for our study region as well as thermal stress for our study species, and subsequently allowed us to assess ground‐dwelling bird responses to temperatures that are predicted to become more common in the future. Our findings confirm the critical importance of tall woody cover for moderating temperatures and functioning as important islands of thermal refuge for ground‐dwelling birds, especially during extreme heat. However, the potential for extreme heat loads within thermal refuges that we observed (albeit much less extreme than the landscape) indicates that the functionality of tall woody cover to mitigate heat extremes may be increasingly limited in the future, thereby reinforcing predictions that climate change represents a clear and present danger for these species.     

Generalist grasshoppers from thermally variable sites do not have higher thermal tolerance than grasshoppers from thermally stable sites - A study of five populations

Thermal tolerance allows many organisms, including insects, to withstand stressful temperatures. Thermal generalists are expected to have higher thermal tolerance than specialists, but the environmental conditions leading to the evolution of a thermal generalist life history are not fully understood. Thermal variability has been put forth as an evolutionary driver of high thermal tolerance, but rarely has this been empirically tested. We used a generalist agricultural pest grasshopper, Melanoplus differentialis, to test upper and lower thermal limits of populations that experienced different levels of thermal variability.We quantified thermal heterogeneity at five sites in a longitudinal transect in the Midwestern U.S. by examining, over a 101-year period, 1) variance in daily thermal maxima and minima; and 2) daily range. Also, as a measure of a biologically relevant thermal extreme, we depicted days per month at each site that reached a stressfully high temperature for M. differentialis. We collected individuals from these sites and tested their upper and lower thermal limits. We found that most of our metrics of thermal heterogeneity differed among sites, while all sites experienced an average of at least two stressfully high temperature events per month. We found that heavier males from these sites were able to withstand both warmer and colder temperatures than smaller males, while heavier females had no thermal advantage over lighter females. However, site of origin had no effect on thermal tolerance.Our findings indicate three things: 1) there is no clear correlation between thermal variability and thermal tolerance in the populations we studied; 2) weight affects thermal tolerance range among sites for M. differentialis males, and 3) thermal extremes may be more important than thermal variability in determining CTMax in this species.     

Effects of temperature acclimation on maximum heat production,thermal tolerance,and torpor in a marsupial

Marsupials, unlike placental mammals, are believed to be unable to increase heat production and thermal performance after cold-acclimation. It has been suggested that this may be because marsupials lack functional brown fat, a thermogenic tissue, which proliferates during cold-acclimation in many placentals. However, arid zone marsupials have to cope with unpredictable, short-term and occasionally extreme changes in environmental conditions, and thus they would benefit from an appropriate physiological response. We therefore investigated whether a sequential two to four week acclimation in Sminthopsis macroura (body mass approx. 25 g) to both cold (16 degrees C) and warm (26 degrees C) ambient temperatures affects the thermal physiology of the species. Cold-acclimated S. macroura were able to significantly increase maximum heat production (by 27%) and could maintain a constant body temperature at significantly lower effective ambient temperatures (about 9 degrees C lower) than when warm-acclimated. Moreover, metabolic rates during torpor were increased following cold-acclimation in comparison to warm-acclimation. Our study shows that, despite the lack of functional brown fat, short-term acclimation can have significant effects on thermoenergetics of marsupials. It is likely that the rapid response in S. macroura reflects an adaptation to the unpredictability of the climate in their habitat.     

Frequent colony orphaning triggers the production of replacement queens via worker thelytoky in a desert-dwelling ant

Although related, Cataglyphis floricola and Cataglyphis tartessica show very different responses to colony orphaning. In the laboratory, under queenless conditions, C. tartessica workers produced male offspring via arrhenotoky, while C. floricola workers produced female offspring, including new queens, via thelytoky. Both species have workers with active ovaries that produce trophic eggs. In the field, in the late spring, C. floricola colonies were more likely to be orphaned than were C. tartessica colonies, probably due to differences in how they performed fission, their colony foundation system. The combined action of these two features could explain the presence of thelytoky in C. floricola and its absence in C. tartessica.

     

Nest box design for a changing climate: The value of improved insulation

Mean air temperatures and the frequency, intensity and duration of extreme weather events such as heatwaves are increasing due to climate change. Nest boxes experience more variable and extreme temperatures than natural cavities, which may reduce survival and reproductive success of the species which utilize them, but little is known about the factors which drive nest box temperature profiles. We quantified the potential for retrofitted insulation on nest boxes to modify internal temperatures and to mimic the thermal characteristics of natural cavities more closely. We tested three types of materials with insulative or reflective properties which were easy to retrofit to nest boxes: 3‐cm‐thick polystyrene, pleated foil batts and reflective paint. We found that polystyrene and foil batts reduced mean nest box temperatures during the day by 0.31 ± 0.01°C and 0.17 ± 0.01°C, respectively (but up to 5.84°C and 4.02°C). The effects of all insulation types were dependent on the time of day, and only polystyrene had a significant effect at night, with a greater capacity to retain heat (mean 0.21 ± 0.01°C warmer). Contrary to expectations, reflective paint caused a small increase in temperature during the late afternoon. In our study, the temperature modulation provided by insulation was able to match or exceed that due to variation in nest location and surrounding vegetation canopy cover. Our findings show that polystyrene and foil batts may offer effective and tractable means to mitigate the effects of extreme temperatures in nest boxes and thereby help achieve temperature profiles more similar to natural cavities.     

Interaction of a small heat shock protein of the fission yeast, Schizosaccharomyces pombe, with a denatured protein at elevated temperature

We have expressed, purified, and characterized one small heat shock protein of the fission yeast Schizosaccharomyces pombe, SpHsp16.0. SpHsp16.0 was able to protect citrate synthase from thermal aggregation at 45 degrees C with high efficiency. It existed as a hexadecameric globular oligomer near the physiological growth temperature. At elevated temperatures, the oligomer dissociated into small species, probably dimers. The dissociation was completely reversible, and the original oligomer reformed immediately after the temperature dropped. Large complexes of SpHsp16.0 and denatured citrate synthase were observed by size exclusion chromatography and electron microscopy following incubation at 45 degrees C and then cooling. However, such large complexes did not elute from the size exclusion column incubated at 45 degrees C. The denatured citrate synthase protected from aggregation was trapped by a GroEL trap mutant at 45 degrees C. These results suggest that the complex of SpHsp16.0 and denatured citrate synthase at elevated temperatures is in the transient state and has a hydrophobic nature. Analyses of the interaction between SpHsp16.0 and denatured citrate synthase by fluorescence cross-correlation spectrometry have also shown that the characteristics of SpHsp16.0-denatured citrate synthase complex at the elevated temperature are different from those of the large complex obtained after the shift to lowered temperatures.     

The influence of brood size upon metabolic rate and body temperature in nestling Blue tits Parus caeruleus and House sparrows Passer domesticus

Metabolic rate and body temperature in nestling Blue tits and House sparrows were measured in broods of different size and age. Surface-volume ratio effects were found in both poikilothermic and homoiothermic Blue tits at ambients of 15°C but not at 20°C. The possibility of incipient hyperthermia amongst young nestlings maintaining sub-adult body temperatures is discussed. For the House sparrows heat retention by the nest was of greater importance than the surface-volume effect. Differences in nest structure between the two species are described and related to the thermal requirements of nestlings in large as against small broods.     

Thermal range predicts bird population resilience to extreme high temperatures

The identification of the characteristics of species that make them susceptible or resilient to climate change has been elusive because non-climatic influences may dominate short- and medium-term changes in population and distribution sizes. Here we studied the 2003 French heat wave, during which other confounding variables remained essentially unchanged, with a correlational approach. We tested the relationship between population resilience and thermal range by analysing the responses of 71 bird species to a 6-month heat wave. Species with small thermal ranges showed the sharpest decreases in population growth rate between 2003 and 2004 in locations with the highest temperature anomalies. Thermal range explained the resilience of birds to the heat wave independently of other potential predictors, although it correlated with nest location and broad habitat type used by species. The geographically deduced thermal range appears to be a reliable predictor of the resilience of these endothermic species to extreme temperatures.     

Mountain stoneflies may tolerate warming streams: Evidence from organismal physiology and gene expression

Rapid glacier recession is altering the physical conditions of headwater streams. Stream temperatures are predicted to rise and become increasingly variable, putting entire meltwater‐associated biological communities at risk of extinction. Thus, there is a pressing need to understand how thermal stress affects mountain stream insects, particularly where glaciers are likely to vanish on contemporary timescales. In this study, we measured the critical thermal maximum (CT_MAX) of stonefly nymphs representing multiple species and a range of thermal regimes in the high Rocky Mountains, USA. We then collected RNA‐sequencing data to assess how organismal thermal stress translated to the cellular level. Our focal species included the meltwater stonefly, Lednia tumana, which was recently listed under the U.S. Endangered Species Act due to climate‐induced habitat loss. For all study species, critical thermal maxima (CT_MAX > 20°C) far exceeded the stream temperatures mountain stoneflies experience (<10°C). Moreover, while evidence for a cellular stress response was present, we also observed constitutive expression of genes encoding proteins known to underlie thermal stress (i.e., heat shock proteins) even at low temperatures that reflected natural conditions. We show that high‐elevation aquatic insects may not be physiologically threatened by short‐term exposure to warm temperatures and that longer‐term physiological responses or biotic factors (e.g., competition) may better explain their extreme distributions.