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Pit vipers detect infrared radiation by means of temperature contrasts created on their pit organ membranes. Signals from pit organs integrate with visual signals in the optic tectum, leading to the conjecture that the facial pits operate as an extension of the visual system. Because similar mechanisms underlie thermal imaging technology, imagery from thermal cameras is often used to infer how pit vipers perceive their environment. However, pit organs lack a focusing mechanism, and biophysical models predict that pit organs should have poor spatial resolution compared with thermal imaging cameras. Nevertheless, behavioral studies occasionally suggest pits may have better resolution than predicted by biophysical models, indicating that processing in the central nervous system may improve imaging. To estimate the spatial resolution of the neural image informing behavior, we recorded snake responses evoked by targets moving across backgrounds composed of two contrasting temperatures with an average temperature equal to the target temperature. An unresolved background would appear uniform; thus, the target would be detectable only if the background pattern were resolved. Western rattlesnakes (Crotalus oreganus) displayed no statistically significant responses to targets presented in front of patterned backgrounds, regardless of the temperature contrasts or spatial frequencies within the background, but responded strongly to targets presented in front of homogeneous backgrounds. We found no evidence that the pit organ system can resolve spatial details subtending an angle of 9 deg or less. We discuss the implications of these results for understanding pit organ function in ecologically relevant habitats with thermal heterogeneity., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2022. Published by The Company of Biologists Ltd.)

1: Thermal refuges are widely used by animals of all taxonomic groups and are critical to survival in severe weather. 2: Human activities are reducing the availability of natural refuges; consequently, artificial refuges are used as conservation management tools, particularly for bats. 3: Published box evaluations are generally incomplete, omitting thermal physiology and relevant thermal properties. 4: Here, we compare methods for evaluating the potential utility of bat box designs for bats and present a graphical spatiotemporal method that provides more complete information. 5: For illustration, we compare the original to three modified versions of the "rocket box" style bat box. 6: Box internal temperatures and generalized thermal physiology models are combined in two suitability indices appropriate to the mother, and to pups. 7: Results revealed that daily and seasonal averages of these indices obscured important processes and showed insignificant differences among bat box design modifications. 8: In contrast, graphical analysis highlighted the presence and spatiotemporal structure of significant differences among boxes, which were most evident in sunny weather. 9: Differences among boxes were sensitive to assumptions about bat thermal physiology and behavior. 10: We found that an external water jacket mitigated temperature extremes and extended favorable temperatures into the night, which could enhance pup development while the mothers foraged. 11: Further experiments are needed to evaluate the relation between metabolic heating by box occupants and thermal conditions within bat boxes., (Copyright © 2021 Elsevier Ltd. All rights reserved.)

Sensory information drives the ecology and behaviour of animals, and some animals are able to detect environmental cues unavailable to us. For example, rattlesnakes use infrared (IR) radiation to detect warm prey at night when visual cues are reduced. Until recently these sensory worlds have been inaccessible to human observers; now technology can allow us to "eavesdrop" on these species and understand how sensory perception drives ecology and behaviour. We used thermography and computer simulations to examine how prey-background temperature contrast and areas of temperature transitions influence the angular orientation of free-ranging rattlesnakes once they have selected an ambush site. We tracked free-ranging sidewinder rattlesnakes Crotalus cerastes to their selected ambush sites and recorded 360° near-ground thermographic panoramas from the centre of the ambush site. A computer simulation then moved a simulated prey item across the panorama and computed a contrast index for all directions. Rattlesnakes did not face ambush directions that offered stronger contrast than average, but they demonstrated a striking tendency to face directions with strong thermal transitions. Background transitions likely create a readily detected, rapidly changing stimulus when a prey animal passes. Quantifications of sensory environments like this one can boost our comprehension of how sensory function impacts the ecology, behaviour, and evolution of animals.

Understanding microhabitat preferences of animals is critical for effective conservation, especially for temperate-zone bats, which receive fitness benefits from selecting optimal roost microhabitats. Artificial roost structures are increasingly being used in conservation efforts for at-risk bat species. To evaluate microhabitat differences in common artificial roost structures and determine if roost selection occurs based on structure type, we installed artificial roosts of three different styles (bat box, rocket box, and bark mimic) in six clusters. We compared size and measured temperature parameters (12 points/roost) while bats were excluded from one cluster. We simultaneously conducted census counts during the active season at five more clusters open to bats for 1-2 years. The rocket box style provided larger entrance area, surface area, and volume versus other roost types. Microclimate varied with roost design. More positions inside the bat box and rocket box stayed within critical temperature limits for bats (0-45°C)-i.e., were usable. The bark-mimic provided less usable space than the rocket box and, often, large proportions of the roost were > 45°C. The rocket box provided the widest temperature availability in a given hour (max range available 7°C) and was more stable than the bark mimic. A maternity colony of Indiana bats (Myotis sodalis) selected the rocket box style; four of five available rocket boxes became primary maternity roosts, with 2-210 bats emerging per night. Future work should aim to manipulate roost size, temperature availability, and temperature stability in isolation to identify which features drive roost microhabitat selection by bats. Comparative studies of artificial roosts account for some inherent irregularity in natural systems, allowing us to study the dynamics of roost microhabitats. We recommend season-long monitoring of microhabitat in novel artificial refuges and comparative studies of artificial and natural roosts, and urge managers to consider potential positive and negative effects when substituting artificial roosts for natural habitat., Competing Interests: The authors have declared that no competing interests exist.

The pit organ defining pit vipers (Crotalinae) contains a membrane covered with temperature receptors that detect thermal radiation from environmental surfaces. Temperature is both the environmental parameter being sensed and the mechanism by which the pit membrane detects the signal. As snakes are ectotherms, temperature also has a strong influence on neurological and locomotor responses to the signal. This study of Pacific rattlesnakes ( Crotalus oreganus ) systematically examined the effect of body, target and background temperatures on response to a moving target. We presented each snake with a moving pendulum bob regulated at a series of six temperatures against a uniform background regulated at one of three temperatures. Snake body temperatures varied from 18 to 36°C. As expected, we found stronger responses to positive contrasts (target warmer than background) than to negative contrasts, and stronger responses to greater contrasts. However, the effect of body temperature was contrary to expectations based on studies of the TRPA1 ion channel (believed to be the molecular basis for pit membrane temperature receptors) and typical thermal reaction norms for neural and motor performance. These predict (1) no response below the threshold where the TRPA1 channel opens, (2) response increasing as temperature increases, peaking near preferred body temperature, and (3) declining thereafter. Remarkably, this behavioral response decreased as body temperature increased from 18 to 36°C, with no threshold or peak in this range. We review various possible physiological mechanisms related to body temperature proposed in the literature, but find none that can satisfactorily explain this result., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2018. Published by The Company of Biologists Ltd.)

Understanding animal movement behaviour is key to furthering our knowledge on intra- and inter-specific competition, group cohesion, energy expenditure, habitat use, the spread of zoonotic diseases or species management. We used a radial basis function surface approximation subject to minimum description length constraint to uncover the state-space dynamical systems from time series data. This approximation allowed us to infer structure from a mathematical model of the movement behaviour of sheep and red deer, and the effect of density, thermal stress and vegetation type. Animal movement was recorded using GPS collars deployed in sheep and deer grazing a large experimental plot in winter and summer. Information on the thermal stress to which animals were exposed was estimated using the power consumption of mechanical heated models and meteorological records of a network of stations in the plot. Thermal stress was higher in deer than in sheep, with less differences between species in summer. Deer travelled more distance than sheep, and both species travelled more in summer than in winter; deer travel distance showed less seasonal differences than sheep. Animal movement was better predicted in deer than in sheep and in winter than in summer; both species showed a swarming behaviour in group cohesion, stronger in deer. At shorter separation distances swarming repulsion was stronger between species than within species. At longer separation distances inter-specific attraction was weaker than intra-specific; there was a positive density-dependent effect on swarming, and stronger in deer than in sheep. There was not clear evidence which species attracted or repelled the other; attraction between deer at long separation distances was stronger when the model accounted for thermal stress, but in general the dynamic movement behaviour was hardly affected by the thermal stress. Vegetation type affected intra-species interactions but had little effect on inter-species interactions. Our modelling approach is useful in interpreting animal interactions, in order to unravel complex cooperative or competitive behaviours, and to the best of our knowledge is the first modelling attempt to make predictions of multi-species animal movement under different habitat mosaics and abiotic environmental conditions.

Understanding how quickly physiological traits evolve is a topic of great interest, particularly in the context of how organisms can adapt in response to climate warming. Adjustment to novel thermal habitats may occur either through behavioural adjustments, physiological adaptation or both. Here, we test whether rates of evolution differ among physiological traits in the cybotoids, a clade of tropical Anolis lizards distributed in markedly different thermal environments on the Caribbean island of Hispaniola. We find that cold tolerance evolves considerably faster than heat tolerance, a difference that results because behavioural thermoregulation more effectively shields these organisms from selection on upper than lower temperature tolerances. Specifically, because lizards in very different environments behaviourally thermoregulate during the day to similar body temperatures, divergent selection on body temperature and heat tolerance is precluded, whereas night-time temperatures can only be partially buffered by behaviour, thereby exposing organisms to selection on cold tolerance. We discuss how exposure to selection on physiology influences divergence among tropical organisms and its implications for adaptive evolutionary response to climate warming.

Gigantic size presents both opportunities and challenges in thermoregulation. Allometric scaling relationships suggest that gigantic animals have difficulty dissipating metabolic heat. Large body size permits the maintenance of fairly constant core body temperatures in ectothermic animals by means of gigantothermy. Conversely, gigantothermy combined with endothermic metabolic rate and activity likely results in heat production rates that exceed heat loss rates. In tropical environments, it has been suggested that a substantial rate of heat storage might result in a potentially lethal rise in core body temperature in both elephants and endothermic dinosaurs. However, the behavioral choice of nocturnal activity might reduce heat storage. We sought to test the hypothesis that there is a functionally significant relationship between heat storage and locomotion in Asian elephants (Elephas maximus), and model the thermoregulatory constraints on activity in elephants and a similarly sized migratory dinosaur, Edmontosaurus. Pre- and post-exercise (N=37 trials) measurements of core body temperature and skin temperature, using thermography were made in two adult female Asian elephants at the Audubon Zoo in New Orleans, LA, USA. Over ambient air temperatures ranging from 8 to 34.5°C, when elephants exercised in full sun, ~56 to 100% of active metabolic heat production was stored in core body tissues. We estimate that during nocturnal activity, in the absence of solar radiation, between 5 and 64% of metabolic heat production would be stored in core tissues. Potentially lethal rates of heat storage in active elephants and Edmontosaurus could be behaviorally regulated by nocturnal activity.

Recent work published in the accompanying paper used a combination of 3D morphological reconstruction to define optical spread functions and heat transfer physics to study how external heat energy would reach the sensory membrane within the facial pit of pitvipers. The results from all of the species examined indicated asymmetric directional sensitivity, e.g. the pit would preferentially respond to stimuli located below and behind the snake. The present study was intended as a test of these findings through a quantitative neurophysiological analysis of directional sensitivity in the facial pit of the western diamondback rattlesnake, Crotalus atrox. An infrared emitter was positioned through a coordinate system (with varying angular orientations and distances) and the response it evoked measured through neurophysiological recordings of a trigeminal nerve branch composed of the afferents from the sensory membrane of the facial pit. Significant differences were found in the strength of the membrane's neural response to a constant stimulus presented at different orientations (relative to the facial pit opening) and over different distances. The peak sensitivity (at 12 deg above and 20 deg in front of the facial pit opening) was in good agreement with the predicted directional sensitivities based on optical spread functions and 3D topography. These findings support the hypothesis that the topography, and functional performance, of the facial pit has undergone an adaptive radiation within the pit vipers, and that differences in the behavioral ecology of the pit vipers (i.e. terrestrial versus arboreal) are reflected within the facial pits.

The pitviper facial pit is a pinhole camera-like sensory organ consisting of a flask-shaped cavity divided into two chambers by a suspended membrane. Neurophysiological studies and simplified optical models suggest that facial pits detect thermal radiation and form an image that is combined with visual input in the optic tectum to form a single multispectral image. External pit anatomy varies markedly among taxonomic groups. However, optical function depends on unknown internal anatomy. Therefore, we developed methods for relating anatomy to optical performance. To illustrate, we constructed detailed anatomical models of the internal anatomy of the facial pits of four individuals of four pitviper species using X-ray tomography sections of fresh material. We used these models to define the point spread function, i.e. the distribution of radiation from a point source over the pit membrane, for each species. We then used optical physics, heat transfer physics and computational image processing to define the thermal image formed on the pit membrane for each species. Our computed pit membrane images are consistent with behavioral observations if the sensitivity of membrane receptors equals the most sensitive (ca. 0.001°C) laboratory estimates. Vignetting (variation in optical aperture size with view angle) and differences between body and environmental temperatures can create temperature variation across the membrane that greatly exceeds image temperature contrasts, potentially impairing imaging. Spread functions plotted versus source point azimuth and elevation show distinct patterns that suggest new research directions into the relationships among the optical anatomy, ecology, behavior and sensory neurophysiology of pitvipers.

Many bird species do not make their own nests; therefore, selection of existing sites that provide adequate microclimates is critical. This is particularly true for owls in north temperate climates that often nest early in the year when inclement weather is common. Spotted owls use three main types of nest structures, each of which are structurally distinct and may provide varying levels of protection to the eggs or young. We tested the hypothesis that spotted owl nest configuration influences nest microclimate using both experimental and observational data. We used a wind tunnel to estimate the convective heat transfer coefficient (h(c)) of eggs in 25 potential nest configurations that mimicked 2 nest types (top-cavity and platform nests), at 3 different wind speeds. We then used the estimates of h(c) in a biophysical heat transfer model to estimate how long it would take unattended eggs to cool from incubation temperature (~36 °C) to physiological zero temperature (PZT; ~26 °C) under natural environmental conditions. Our results indicated that the structural configuration of nests influences the cooling time of the eggs inside those nests, and hence, influences the nest microclimate. Estimates of time to PZT ranged from 10.6 minutes to 33.3 minutes. Nest configurations that were most similar to platform nests always had the fastest egg cooling times, suggesting that platform nests were the least protective of those nests we tested. Our field data coupled with our experimental results suggested that nest choice is important for the reproductive success of owls during years of inclement weather or in regions characterized by inclement weather during the nesting season.

A renaissance in organismal biology has been sparked by recent conceptual, theoretical, methodological, and computational advances in the life sciences, along with an unprecedented interdisciplinary integration with Mathematics, Engineering, and the physical sciences. Despite a decades-long trend toward reductionist approaches to biological problems, it is increasingly recognized that whole organisms play a central role in organizing and interpreting information from across the biological spectrum. Organisms represent the nexus where sub- and supra-organismal processes meet, and it is the performance of organisms within the environment that provides the material for natural selection. Here, we identify five "grand challenges" for future research in organismal biology. It is intended that these challenges will spark further discussion in the broader community and identify future research priorities, opportunities, and directions, which will ultimately help to guide the allocation of support for and training in organismal biology.

It is commonly assumed that the facial pit of pitvipers forms relatively sharp images and can detect small differences in environmental surface temperatures. We have visualized the temperature contrast images formed on the facial pit membrane using a detailed optical and heat transfer analysis, which includes heat transfer through the air in the pit chambers as well as via thermal infrared radiation. We find the image on the membrane to be poorly focused and of very low temperature contrast. Heat flow through the air in the pit chambers severely limits sensitivity, particularly for small animals with small facial pit chambers. The aperture of the facial pit appears to be larger than is optimal for detecting small targets such as prey at 0.5 m. Angular resolution (i.e. sharpness) and image strength and contrast vary complexly with the size of the pit opening. As a result, the patterns of natural background temperatures obscure prey items and other environmental features, creating false patterns. Consequently, snakes cannot simply target the strongest signal to strike prey. To account for observed behavioral capabilities, the sensory endings on the pit membrane apparently must respond to temperature contrasts of 0.001 degrees C or less. While neural image sharpening likely enhances imaging performance, it appears important for foraging snakes to select ambush sites offering uniform backgrounds and strong thermal contrasts. As the ancestral facial pit was likely less sensitive than the current organ, objects with strong thermal signals, such as habitat features, were needed to drive the evolution of this remarkable sense.

Water birds whose young begin swimming while downy are interesting because hypothermia and mortality are associated with wetting. While wetting is known to increase heat loss, little is known about basic issues, such as the amount of heat lost to air vs water during surface swimming. To partition heat loss to air and water, we measured the body temperature, metabolism and thermal conductance of 2-3-day-old mallard ducklings (Anas platyrhynchos) swimming under different combinations of air and water temperature. Ventral down remained dry or was wetted only on the surface, and most ducklings could maintain Tb>39 degrees C for 1 h while swimming on water as cold as 5 degrees C. Ducklings were at or below thermal neutrality when swimming in water at Tw=30 degrees C even when air temperature Ta=45 degrees C. Heat loss from ducklings with dry down to air and water was partitioned by fitting data to a heat transfer model of the form M=G(Tb-Tw)+Ke(Tb-Ta). For an average 48 g duckling, thermal conductance to water increased with water temperature, G=0.0470(1+1.059 x 10(-6)Tw4)W/ degrees C-animal. Conductance to air was Ke=0.0196 W/ degrees C-animal for all air temperatures. Thus, a minimum of 70% of metabolic heat production is lost to water, and this fraction increases with increasing temperature.

Pitvipers (Viperidae: Crotalinae) possess thermal radiation receptors, the facial pits, which allow them to detect modest temperature fluctuations within their environments. It was previously thought that these organs were used solely to aid in prey acquisition, but recent findings demonstrated that western diamondback rattlesnakes (Crotalus atrox) use them to direct behavioral thermoregulation, suggesting that facial pits might be general purpose organs used to drive a suite of behaviors. To investigate this further, we conducted a phylogenetic survey of viperine thermoregulatory behavior cued by thermal radiation. We assessed this behavior in 12 pitviper species, representing key nodes in the evolution of pitvipers and a broad range of thermal environments, and a single species of true viper (Viperidae: Viperinae), a closely related subfamily of snakes that lack facial pits but possess a putative thermal radiation receptor. All pitviper species were able to rely on their facial pits to direct thermoregulatory movements, while the true viper was unable to do so. Our results suggest that thermoregulatory behavior cued by thermal radiation is a universal role of facial pits and probably represents an ancestral trait among pitvipers. Further, they establish behavioral thermoregulation as a plausible hypothesis explaining the evolutionary origin of the facial pit.

Pitvipers (Viperidae: Crotalinae) possess unique sensory organs, the facial pits, capable of sensing subtle fluctuations in thermal radiation. Prey acquisition has long been regarded as the sole function of the facial pits. However, the ability to sense thermal radiation could also direct thermoregulatory behavior by remotely sensing nearby surface temperatures. Using a series of behavioral arenas of varying spatial complexity and ecological relevance, we surveyed the ability of the western diamondback rattlesnake Crotalus atrox to direct successful thermoregulatory movements with either functional or disabled facial pits. We found that western diamondback rattlesnakes could base thermoregulatory decisions on thermal radiation cues when their pits were functional, but not when blocked. Our results indicate that the facial pit is part of a generalized sense, and suggest thermoregulation as an alternative hypothesis to prey acquisition for the origin of facial pits.

Wind is a significant factor in the thermoregulation of chicks of shorebirds on the Arctic tundra. We investigated the effect of wind at speeds typical of near-surface conditions (0.1-3 ms(-1)) on metabolic heat production, evaporative cooling and thermal conductance of 1- to 3- week-old downy scolopacid chicks (least sandpiper Calidris minutilla; short-billed dowitcher Limnodromus griseus; whimbrel Numenius phaeopus). Body mass ranged from 9 to 109 g. To accurately measure the interacting effects of air temperature and wind speed, we used two or more air temperatures between 15 degrees and 30 degrees C that produced cold stress at all wind speeds, but allowed chicks to maintain normal body temperature (approximately 39 degrees C). Thermal conductance increased by 30-50% as wind speed increased from 0.1 to 3 ms(-1). Conductance in these chicks is somewhat lower than that of 1-day-old mallard ducklings of similar mass, but higher than values reported for downy capercaillie and Xantus' murrelet chicks, as well as for adult shorebirds. Evaporative water loss was substantial and increased with mass and air temperature. We developed a standard operative temperature scale for shorebird chicks. The ratio of evaporative cooling to heat production varied with wind speed and air temperature.

Studies using mounts have an inherently nested error structure; calibration and standardization should use the appropriate procedures and statistics. One example is that individual mount differences are nested within morphological factors related to species, age, or gender; without replication, mount differences may be confused with differences due to morphology. Also, the sensitivity of mounts to orientation to wind or sun is nested within mount; without replication, inadvertent variation in mount positioning may be confused with differences among mounts. Data on heat loss from a of 1-day-old mallard duckling mount are used to illustrate orientation sensitivity.

Most duckling mortality occurs during the week following hatching and is often associated with cold, windy, wet weather and scattering of the brood. We estimated the thermoregulatory demands imposed by cold, windy weather on isolated 1-d-old mallard (Anas platyrhynchos) ducklings resting in cover. We measured O2 consumption and evaporative water loss at air temperatures from 5 degrees to 25 degrees C and wind speeds of 0.1, 0.2, 0.5, and 1.0 m/s. Metabolic heat production increased as wind increased or temperature decreased but was less sensitive to wind than that of either adult passerines or small mammals. Evaporative heat loss ranged from 5% to 17% of heat production. Evaporative heat loss and the ratio of evaporative heat loss to metabolic heat production was significantly lower in rest phase. These data were used to define a standard operative temperature (Tes) scale for night or heavy overcast conditions. An increase of wind speed from 0.1 to 1 m/s decreased Tes by 3 degrees -5 degrees C.

Studies of the spectral reflectance of the eggs of 25 species of birds from nine families disclosed uniformly high reflectance (often above 90 percent) in the near infrared. This property is associated with the presence of the eggshell pigments protoporphyrin and the bilins. These pigments allow coloration for cryptic or other purposes with minimum solar heating, a combination not possible with the melanin pigments typical of vertebrates.