Pit viper thermography: the pit organ used by crotaline snakes to detect thermal contrast has poor spatial resolution.

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.

Methods for assessing artificial thermal refuges: Spatiotemporal analysis more informative than averages.

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.

Infrared-sensing snakes select ambush orientation based on thermal backgrounds.

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.

In artificial roost comparison, bats show preference for rocket box style.

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.

Cooler snakes respond more strongly to infrared stimuli, but we have no idea why.

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.

Evolutionary stasis and lability in thermal physiology in a group of tropical lizards.

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.

Potential influences of climate and nest structure on spotted owl reproductive success: a biophysical approach.

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.

Analytical methods for the geometric optics of thermal vision illustrated with four species of pitvipers.

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.

Directional sensitivity in the thermal response of the facial pit in western diamondback rattlesnakes (Crotalus atrox).

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.

Grand challenges in organismal biology.

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.

The imaging properties and sensitivity of the facial pits of pitvipers as determined by optical and heat-transfer analysis.

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.

Partitioning heat loss from mallard ducklings swimming on the air-water interface.

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.

Heat in evolution's kitchen: evolutionary perspectives on the functions and origin of the facial pit of pitvipers (Viperidae: Crotalinae).

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.

Thermoregulation is the pits: use of thermal radiation for retreat site selection by rattlesnakes.

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.

Metabolic response to wind of downy chicks of Arctic-breeding shorebirds (Scolopacidae).

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.