Thermoregulatory Strategies Research Articles

Formal comment on: Myhrvold (2016) Dinosaur metabolism and the allometry of maximum growth rate. PLoS ONE; 11(11): e0163205.

In his 2016 paper, Myhrvold criticized ours from 2014 on maximum growth rates (Gmax, maximum gain in body mass observed within a time unit throughout an individual’s ontogeny) and thermoregulation strategies (ectothermy, endothermy) of 17 dinosaurs. In our paper, we showed that Gmax values of similar-sized extant ectothermic and endothermic vertebrates overlap. This strongly questions a correct assignment of a thermoregulation strategy to a dinosaur only based on its Gmax and (adult) body mass (M). Contrary, Gmax separated similar-sized extant reptiles and birds (Sauropsida) and Gmax values of our studied dinosaurs were similar to those seen in extant similar-sized (if necessary scaled-up) fast growing ectothermic reptiles. Myhrvold examined two hypotheses (H1 and H2) regarding our study. However, we did neither infer dinosaurian thermoregulation strategies from group-wide averages (H1) nor were our results based on that Gmax and metabolic rate (MR) are related (H2). In order to assess whether single dinosaurian Gmax values fit to those of extant endotherms (birds) or of ectotherms (reptiles), we already used a method suggested by Myhrvold to avoid H1, and we only discussed pros and cons of a relation between Gmax and MR and did not apply it (H2). We appreciate Myhrvold’s efforts in eliminating the correlation between Gmax and M in order to statistically improve vertebrate scaling regressions on maximum gain in body mass. However, we show here that his mass-specific maximum growth rate (kC) replacing Gmax (= MkC) does not model the expected higher mass gain in larger than in smaller species for any set of species. We also comment on, why we considered extant reptiles and birds as reference models for extinct dinosaurs and why we used phylogenetically-informed regression analysis throughout our study. Finally, we question several arguments given in Myhrvold in order to support his results.

The evolution of eccrine sweat glands in human and nonhuman primates

Sweating is an unusual thermoregulatory strategy for most mammals, yet is critical for humans. This trait is commonly hypothesized to result from human ancestors moving from a forest to a warmer and drier open environment. As soft tissue traits do not typically fossilize, this idea has been difficult to test. Therefore, we used a comparative approach to examine 15 eccrine gland traits from 35 primate species. For each trait we measured phylogenetic signal, tested three evolutionary models to explain trait variation, and used phylogenetic models to examine how traits varied in response to climate variables. Phylogenetic signal in traits varied substantially, with the two traits exhibiting the highest values being gland distribution on the body and percent eccrine vs. apocrine glands on the body. Variation in most traits was best explained by an Ornstein-Uhlenbeck model suggesting the importance of natural selection. Two traits were strongly predicted by climate. First, species with high eccrine gland glycogen content were associated with habitats exhibiting warm temperatures and low rainfall. Second, species with increased capillarization were associated with high temperature. Glycogen is a primary energy substrate powering sweat production and sodium reabsorption in the eccrine gland, and increased capillarization permits greater oxygen, glucose and electrolyte delivery. Thus, our results are evidence of natural selection for increased sweating capacity in primate species with body surface eccrine glands living in hot and dry climates. We suggest that selection for increased glycogen content and capillarization may have been part of initial increases in hominin thermoregulatory sweating capacity.

Effects of Contingency versus Constraints on the Body-Mass Scaling of Metabolic Rate

I illustrate the effects of both contingency and constraints on the body-mass scaling of metabolic rate by analyzing the significantly different influences of ambient temperature (Ta) on metabolic scaling in ectothermic versus endothermic animals. Interspecific comparisons show that increasing Ta results in decreasing metabolic scaling slopes in ectotherms, but increasing slopes in endotherms, a pattern uniquely predicted by the metabolic-level boundaries hypothesis, as amended to include effects of the scaling of thermal conductance in endotherms outside their thermoneutral zone. No other published theoretical model explicitly predicts this striking variation in metabolic scaling, which I explain in terms of contingent effects of Ta and thermoregulatory strategy in the context of physical and geometric constraints related to the scaling of surface area, volume, and heat flow across surfaces. My analysis shows that theoretical models focused on an ideal 3/4-power law, as explained by a single universally applicable mechanism, are clearly inadequate for explaining the diversity and environmental sensitivity of metabolic scaling. An important challenge is to develop a theory of metabolic scaling that recognizes the contingent effects of multiple mechanisms that are modulated by several extrinsic and intrinsic factors within specified constraints.

Geographical and experimental contexts modulate the effect of warming on top-down control: a meta-analysis.

Ecologists have extensively investigated the effect of warming on consumer-resource interactions, with experiments revealing that warming can strengthen, weaken or have no net effect on top-down control of resources. These experiments have inspired a body of theoretical work to explain the variation in the effect of warming on top-down control. However, there has been no quantitative attempt to reconcile theory with outcomes from empirical studies. To address the gap between theory and experiment, we performed a meta-analysis to examine the combined effect of experimental warming and top-down control on resource biomass and determined potential sources of variation across experiments. We show that differences in experimental outcomes are related to systematic variation in the geographical distribution of studies. Specifically, warming strengthened top-down control when experiments were conducted in colder regions, but had the opposite effect in warmer regions. Furthermore, we found that differences in the thermoregulation strategy of the consumer and openness of experimental arenas to dispersal can contribute to some deviation from the overall geographical pattern. These results reconcile empirical findings and support the expectation of geographical variation in the response of consumer-resource interactions to warming.

The dark side of Lepidoptera: Colour lightness of geometrid moths decreases with increasing latitude

AbstractAimThe observed decrease in insect colour lightness with increasing latitude has been explained in earlier macroecological studies by the increased solar absorption of dark coloration, which allows extended periods of activity. However, melanin‐based dark coloration also protects against pathogens and ultraviolet radiation, which select for dark coloration at low latitudes where these selection pressures intensify. In nocturnal insects, the relative importance of these protective functions of dark coloration is expected to surpass thermoregulatory functions, as nocturnal species cannot benefit from extended periods of activity during the daytime. Hence, we expected that diurnal and nocturnal insects show contrasting geographical patterns of colour lightness. We tested these predictions using geometrid moths, which comprise both diurnal and nocturnal species.LocationWestern Palearctic.Time periodContemporary.Major taxa studiedGeometridae (Lepidoptera).MethodsWe used digital image analysis to assess the colour lightness of 637 species, compiled their distribution across 3,777 grid cells of 50 km × 50 km and calculated the assemblage‐based average colour lightness. We used multiple regressions, autoregressive error models and randomizations to test for relationships between colour lightness and environmental variables associated with the thermal environment, putative pathogen pressure and ultraviolet radiation.ResultsWe found a clear decrease in colour lightness of assemblages of both diurnal and nocturnal moth species with increasing latitude. In every model, solar radiation was the most important predictor of colour lightness; that is, colour lightness consistently increased with increasing solar radiation.Main conclusionsThese results indicate that the thermal environment is the most influential climatic driver of insect colour lightness—independent of thermoregulatory strategy and nocturnal or diurnal activity. This challenges the view that extended periods of activity are the main selection pressure for geographical variation in insect colour lightness. Consequently, the relationship between insect colour lightness and the thermal environment might be more general than previously thought.

The influence of thermal inputs on brain regulation of exercise: An evolutionary perspective.

The relationship between performance, heat load and the ability to withstand serious thermal insult is a key factor in understanding how endurance is regulated. The capacity to withstand high thermal loads is not unique to humans and is typical to all mammals. Thermoregulation is an evolutionary adaptation which is species specific and should be regarded as a survival strategy rather than purely a physiological response. The fact that mammals have selected ~37°C as a set point could be a key factor in understanding our endurance capabilities and strategy. Endurance presents a significant challenge to bodily homeostasis while our thermoregulatory strategy is able to cope exquisitely under the most unfavorable conditions. The ability of the CNS to regulate this strategy is key in athletic performance since the thermoregulatory center is located within the brain and receives input from multiple systems and deploys effector responses as needed. This chapter will discuss the evolution of thermoregulation in humans and propose that the brain is more than sufficiently capable of maintaining thermal-homeostasis because of its evolutionary path. As such, this is connected to our ability to modulate efferent drive during heat strain and in so doing provides us with the capability to pace during endurance events in the heat.

Behavioural responses of naked mole rats to acute hypoxia and anoxia.

Naked mole rats (NMRs) are among the most hypoxia-tolerant mammals. Other species respond to hypoxia by either escaping the hypoxic environment or drastically decreasing behavioural activity and body temperature (Tb) to conserve energy. However, NMRs rarely leave their underground burrows, which are putatively hypoxic and thermally stable near the NMRs' preferred Tb Therefore, we asked whether NMRs are able to employ behavioural and thermoregulatory strategies in response to hypoxia despite their need to remain active and the minimal thermal scope in their burrows. We exposed NMRs to progressively deeper levels of hypoxia (from 21 to 0% O2) while measuring their behaviour and Tb Behavioural activity decreased 40-60% in hypoxia and Tb decreased slightly in moderate hypoxia (5-9%) and then further with deeper hypoxia (3% O2). However, even at 3% O2 NMRs remained somewhat active and warm, and continued to explore their environment. Remarkably, NMRs were active for greater than 90 s in acute anoxia and Tb and metabolic rate decreased rapidly. We conclude that NMRs are adapted to remain awake and functional even at the extremes of their hypoxia-tolerance. This adaptation likely reflects variable and challenging levels of environmental hypoxia in the natural habitat of this species.

Sociality Affects REM Sleep Episode Duration Under Controlled Laboratory Conditions in the Rock Hyrax, Procavia capensis.

The rock hyrax, Procavia capensis, is a highly social, diurnal mammal. In the current study several physiologically measurable parameters of sleep, as well as the accompanying behavior, were recorded continuously from five rock hyraxes, for 72 h under solitary (experimental animal alone in the recording chamber), and social conditions (experimental animal with 1 or 2 additional, non-implanted animals in the recording chamber). The results revealed no significant differences between solitary and social conditions for total sleep times, number of episodes, episode duration or slow wave activity (SWA) for all states examined. The only significant difference observed between social and solitary conditions was the average duration of rapid eye movement (REM) sleep episodes. REM sleep episode duration was on average 20 s and 40 s longer under social conditions daily and during the dark period, respectively. It is hypothesized that the increase in REM sleep episode duration under social conditions could possibly be attributed to improved thermoregulation strategies, however considering the limited sample size and design of the current study further investigations are needed to confirm this finding. Whether the conclusions and the observations made in this study can be generalized to all naturally socially sleeping mammals remains an open question.

Hibernators on Madagascar

AbstractIn our latitudes, we are familiar with mammals who spend the less hospitable season of the year in dens, but it has come as some surprise to discover that dwarf lemurs in the tropics do the same. New studies show that thanks to their special thermoregulation strategies, they can adapt even more flexibly to the climate, habitats and sleeping sites.

Thermal adaptation in North American cicadas (Hemiptera: Cicadidae)

We determine and summarize the thermal responses for 118 species and subspecies of North American cicadas representing more than 50 years of fieldwork and experimentation. We investigate the role that habitat and behavior have on the thermal adaptation of the North American cicadas. There are general patterns of increasing thermal responses in warmer floristic provinces and increasing maximum potential temperature within a habitat. Altitude shows an inverse relationship with thermal responses. Comparison of thermal responses of species emerging early or late in the season within the same habitat show increases in the thermal responses along with the increasing environmental temperatures late in the summer. However, behavior, specifically the use of endothermy as a thermoregulatory strategy, can influence the values determined in a particular habitat. Subspecies generally do not differ in their thermal tolerances and thermal tolerances are consistent within a species over distances of more than 7600km.

It Takes Time to Be Cool: On the Relationship between Hyperthermia and Body Cooling in a Migrating Seaduck.

The large amount of energy expended during flapping flight is associated with heat generated through the increased work of the flight muscles. This increased muscle work rate can manifest itself in core body temperature (Tb) increase of 1–2°C in birds during flight. Therefore, episodic body cooling may be mandatory in migratory birds. To elucidate the thermoregulatory strategy of a short-distance migrant, common eiders (Somateria mollissima), we implanted data loggers in the body cavity of wild birds for 1 year, and report information on Tb during their entire migration for 19 individuals. We show that the mean body temperature during flight (TbMean) in the eiders was associated with rises in Tb ranging from 0.2 to 1.5°C, largely depending on flight duration. To understand how eiders are dealing with hyperthermia during migration, we first compare, at a daily scale, how Tb differs during migration using a before-after approach. Only a slight difference was found (0.05°C) between the after (40.30°C), the before (40.41°C) and the migration (40.36°C) periods, indicating that hyperthermia during flight had minimal impact at this time scale. Analyses at the scale of a flight cycle (flight plus stops on the water), however, clearly shows that eiders were closely regulating Tb during migration, as the relationship between the storage of heat during flight was highly correlated (slope = 1) with the level of heat dumping during stops, at both inter-individual and intra-individual levels. Because Tb at the start of a flight (TbStart) was significantly and positively related to Tb at the end of a flight (TbEnd), and the maximal attained Tb during a flight (TbMax), we conclude that in absence of sufficient body cooling during stopovers, eiders are likely to become increasingly hyperthermic during migration. Finally, we quantified the time spent cooling down during migration to be 36% of their daily (24 h) time budget, and conclude that behavioral body cooling in relation to hyperthermia represents an important time cost.

Oxygen isotopes suggest elevated thermometabolism within multiple Permo-Triassic therapsid clades.

The only true living endothermic vertebrates are birds and mammals, which produce and regulate their internal temperature quite independently from their surroundings. For mammal ancestors, anatomical clues suggest that endothermy originated during the Permian or Triassic. Here we investigate the origin of mammalian thermoregulation by analysing apatite stable oxygen isotope compositions (δ18Op) of some of their Permo-Triassic therapsid relatives. Comparing of the δ18Op values of therapsid bone and tooth apatites to those of co-existing non-therapsid tetrapods, demonstrates different body temperatures and thermoregulatory strategies. It is proposed that cynodonts and dicynodonts independently acquired constant elevated thermometabolism, respectively within the Eucynodontia and Lystrosauridae + Kannemeyeriiformes clades. We conclude that mammalian endothermy originated in the Epicynodontia during the middle-late Permian. Major global climatic and environmental fluctuations were the most likely selective pressures on the success of such elevated thermometabolism.

Ambient temperature and humidity modulate the behavioural thermoregulation of a small arboreal mammal (Callicebus bernhardi)

Maintaining a constant body temperature is critical to the proper functioning of metabolic reactions. Behavioural thermoregulation strategies may minimize the cost of energetic balance when an animal is outside its thermoneutral zone. We investigated whether ambient temperature and relative air humidity influence the use of behavioural strategies by a group of Prince Bernhard's titi monkeys (Callicebus bernhardi) living in a forest fragment. We monitored a social group composed of four individuals (an adult couple and two juveniles) for 1010h from March to September 2015. We used the instantaneous scan sampling method to record the body posture, the microhabitat, and the occurrence of huddling with group mate(s) when animals were resting. We recorded ambient temperature and relative humidity in the shade every 10min with a data logger hanging at a height of approximately 5m. Daytime temperature ranged from 18.5°C to 38.5°C and relative humidity ranged from 21% to 97%. Titi monkeys avoided sunny places at higher temperatures, especially above 31°C. Minimum night temperature did not influence the choice of resting microhabitats during the first hour after sunrise. Sitting was the major resting posture during the day (62%). Titi monkeys increased the use of heat-dissipating postures at ambient temperatures >27°C. In addition, an increase in relative humidity increased the use of these postures at 26°C, 27°C, 29°C and 33°C, but caused a decrease at 24°C. On the other hand, the ambient temperature did not influence the occurrence of huddling. We conclude that microhabitat choice and postural behaviour are important for titi monkeys to prevent overheating and suggest that these behavioural adjustments might also be critical for other tropical arboreal mammals.

The evolution of gigantism in active marine predators

A novel hypothesis to better understand the evolution of gigantism in active marine predators and the diversity of body sizes, feeding strategies and thermophysiologies of extinct and living aquatic vertebrates is proposed. Recent works suggest that some aspects of animal energetics can act as constraining factors for body size. Given that mass-specific metabolic rate decreases with body mass, the body size of active predators should be limited by the high metabolic demand of this feeding strategy. In this context, we propose that shifts towards higher metabolic levels can enable the same activity and feeding strategy to be maintained at bigger body sizes, offering a satisfactory explanation for the evolution of gigantism in active predators, including a vast quantity of fossil taxa. Therefore, assessing the metabolic ceilings of living aquatic vertebrates and the thermoregulatory strategies of certain key extinct groups is now crucial to define the energetic limits of predation and provide quantitative support for this model.

Huddling is more important than rest site selection for thermoregulation in southern bamboo lemurs

Resting site selection can have important effects on the behaviour and fitness of organisms. The maintenance of optimal body temperatures (Tb) when faced with environmental variables has often been attributed to either specific microhabitat rest site characteristics or to behavioural strategies. Among many small group-living endotherms, social thermoregulation (i.e. huddling) is utilized as an energy conservation mechanism at low ambient temperatures (Ta), thus decreasing the metabolic cost of maintaining Tb. Although unusual among primates, lemurs maintain a low metabolic rate and exhibit a diversity of thermoregulatory strategies; however, objective Tb measurements have thus far been limited to small-bodied lemurs (e.g. Cheirogaleids). As such, we sought to determine whether a medium-sized lemur model, the southern bamboo lemur, Hapalemur meridionalis, would maintain thermoregulation through microhabitat rest site selection, huddling behaviour, or potentially both strategies. Within a degraded littoral forest fragment in southeast Madagascar, we conducted full-day focal observations on three groups of H. meridionalis between January and December 2013. Adult individuals were collared with data-loggers that collected instantaneous skin temperature Tsk (°C). We calculated the mean Tsk of the focal individual during each resting bout, and the proportional rate of huddling between the focal individual and conspecifics. In addition, we recorded all resting sites utilized for at least 15 min and collected standard tree characteristics. We fitted linear mixed-effects models to determine the thermoregulatory combined effect of specific resting site characteristics, huddling behaviour and environmental variables on Tsk. Our results showed that lemurs selected tree sites with larger diameter at breast height; however, huddling was most predictive of increasing Tsk whereas resting site characteristics were not included in the best-fit model. It is possible that microhabitat rest site selection is not significant in a degraded forest as the potential environmental buffering is limited; thus, thermoregulatory mechanisms are probably best served by behavioural strategies, i.e. social huddling.

Avian torpor or alternative thermoregulatory strategies for overwintering?

It is unclear whether torpor really is uncommon amongst passerine birds. We therefore examined body temperature and thermoregulatory strategies of an Austral passerine, the white-browed babbler (Pomatostomus superciliosus), which has characteristics related to a high probability of torpor use; it is a sedentary, insectivorous, cooperative breeding species, which we studied during winter in a temperate habitat. Wild, free-living babblers maintained normothermy overnight, even at sub-zero ambient temperatures, with a mean minimum body temperature of 38.5±0.04°C that was independent of minimum black bulb temperature. Physiological variables measured in the laboratory revealed that babblers had a low basal metabolic rate and evaporative water loss, but their body temperature and thermal conductance were typical of those of other birds and they had a typical endothermic response to low ambient temperature. Huddling yielded significant energy savings at low temperatures and a roost nest created a microclimate that buffered against low temperatures. Low basal energy requirements, communal roosting and the insulation of a roost nest confer sufficient energetic benefits, allowing babblers to meet energy requirements without resorting to heterothermia, even in their depauperate, low-productivity landscape, suggesting that passerine birds use alternatives to torpor to balance their energy budgets when possible.

Thermoregulation in the Andean lizard Anolis heterodermus (Squamata: Dactyloidae) at high elevation in the Eastern Cordillera of Colombia.

ABSTRACT Low thermal quality environments, such extreme latitudes or high elevation regions, are highly expensive for reptiles in terms of thermoregulation. Thus, physiological adaptations or behavioral adjustments to live in these habitats have evolved in some species. Anolis heterodermus (Duméril, 1851) is an anole lizard that lives at high elevations in the Andes region. In this paper, we attempted to elucidate the thermoregulation strategy of a population of this species from the eastern cordillera of Colombia during wet and dry seasons. We measured body temperatures (Tb), operative temperatures (Te) and preferred temperatures (Tpref). Based on these data, we obtained accuracy ( b ), environmental thermal quality ( e ) and efficiency of thermoregulation (E) indexes. There were no significant differences of Tb or b between seasons, sexes, ages, and for Tpref between sexes or ages, but we found differences in Te and e between seasons. The indexes suggested high thermoregulatory accuracy, low thermal environment quality and indicated that A. heterodermus was an active thermoregulator in both seasons. Broad ranges of Tb and the species association with microhabitats with high solar radiation suggest eurythermy and heliothermy. Anolis heterodermus lives in a low thermal quality habitat, using exposed perches, which seems the most efficient thermal microhabitats. We concluded that A. heterodermus performed behavioral adjustment for compensating seasonal variation in the environmental thermal costs.

Cardiac autonomic innervation of the western pygmy possum (Cercatetus concinnus) and golden bandicoot (Isoodon auratus)

Evidence for a functional ventricular parasympathetic innervation of the mammalian heart between and within taxa remains controversial. We have previously proposed that the presence of a functional parasympathetic innervation of the ventricle was indicative of heterothermy, and is essential for maintaining ventricular stability at low body temperature. However, it is possible that the presence of such an innervation is also representative of the primitive mammalian state. In this study, we aimed to determine whether a functional parasympathetic innervation of the ventricle, that is capable of actively reducing the force of contraction, is present across metatherian mammals. Using in vitro isolated cardiac preparations, we examined evidence for a functional ventricular parasympathetic innervation of the ventricle in two species of metatherian mammal, one heterotherm (Western pygmy possum; Cercatetus concinnus) and one homeotherm (Golden bandicoot; Isoodon auratus), from different families to complement existing data from a heterothermic dasyurid. Both C. concinnus and I. auratus had a potent biphasic response to transmural electrical stimulation in both atrial and ventricular preparations. Both the decrease and increase in the force of contraction in response to stimulation were almost entirely blocked by the cholinergic and adrenergic antagonists, atropine and propranolol, respectively. These observations provide clear evidence for a parasympathetic innervation of the ventricle that is capable of directly influencing the force of contraction across metatherian mammals with different thermoregulatory strategies. While this innervation may facilitate heterothermy, this suggests that the presence of such an innervation pattern is indicative of the primitive mammalian state.

Daily Thermal Fluctuations Experienced by Pupae via Rhythmic Nursing Behavior Increase Numbers of Mushroom Body Microglomeruli in the Adult Ant Brain.

Social insects control brood development by using different thermoregulatory strategies. Camponotus mus ants expose their brood to daily temperature fluctuations by translocating them inside the nest following a circadian rhythm of thermal preferences. At the middle of the photophase brood is moved to locations at 30.8°C; 8 h later, during the night, the brood is transferred back to locations at 27.5°C. We investigated whether daily thermal fluctuations experienced by developing pupae affect the neuroarchitecture in the adult brain, in particular in sensory input regions of the mushroom bodies (MB calyces). The complexity of synaptic microcircuits was estimated by quantifying MB-calyx volumes together with densities of presynaptic boutons of microglomeruli (MG) in the olfactory lip and visual collar regions. We compared young adult workers that were reared either under controlled daily thermal fluctuations of different amplitudes, or at different constant temperatures. Thermal regimes significantly affected the large (non-dense) olfactory lip region of the adult MB calyx, while changes in the dense lip and the visual collar were less evident. Thermal fluctuations mimicking the amplitudes of natural temperature fluctuations via circadian rhythmic translocation of pupae by nurses (amplitude 3.3°C) lead to higher numbers of MG in the MB calyces compared to those in pupae reared at smaller or larger thermal amplitudes (0.0, 1.5, 9.6°C), or at constant temperatures (25.4, 35.0°C). We conclude that rhythmic control of brood temperature by nursing ants optimizes brain development by increasing MG densities and numbers in specific brain areas. Resulting differences in synaptic microcircuits are expected to affect sensory processing and learning abilities in adult ants, and may also promote interindividual behavioral variability within colonies.

Small bees overheat in sunlit flowers: do they make cooling flights?

1. Although thermoregulation by large bees in cool climates has been well studied, less is known about the very different thermoregulatory strategies of small bees, especially those subjected to heat stress.2. Studies were carried out on small (< 20 mg fresh weight), dark‐coloured, solitary bees (mostly halictids and hylaeine colletids) experiencing an extreme radiative heat load, enhanced by the high‐altitude location and by reflection of incident radiation by the high‐albedo petals of the flowers of Potentilla lancinata.3. When foraging in the flowers, such bees experienced peak operative temperatures exceeding 44 °C. In these conditions, males largely stopped foraging but females continued, usually limiting their flower visits to a few seconds and making frequent short flights. These flights would cool the bees down, because bees suspended in air were cooler than bees in sunlit flowers, and convective cooling during flight would further enhance the cooling effect of departure from the flower.4. As far as is known, cooling flights in small bees have not been proposed before, providing a new avenue for exploration of bee thermoregulatory strategies.