Our paper “Energetic costs of bill heat exchange demonstrate contributions to thermoregulation at high temperatures in toco toucans (Ramphastos toco)” was just accepted for publication in the Journal of Experimental Biology.
This research project was from Jussara Chaves’ MSc thesis done at UNESP, Rio Claro, Brasil with Dr. Denis Andrade.
We showed that insulating the bill does not alter the width of the thermal neutral zone, suggesting the toco toucan has the capacity to compensate for the sudden reduction in heat transfer from the bill, but at higher temperatures the normal role of the bill in assisting with heat dissipation becomes more clear. Birds with insulated bills show significantly higher metabolic costs of heat dissipation. Since the primary avenues for dissipating heat at high ambient temperatures are evaporative cooling, the compensatory mechanisms involve an increased reliance on panting and gular fluttering, which are metabolically costly. These results indicate that while heat dissipation through the bill does not contribute significantly to widening of the TNZ, it may well be critically important in assisting body temperature regulation at higher temperatures extending above the upper limit of the TNZ.
Access the paper from this Link (50 free clicks) or at the JEB website.
Citation
Chaves, J.N, Tattersall, GJ, and Andrade, DV. 2023. Energetic costs of bill heat exchange demonstrate contributions to thermoregulation at high temperatures in toco toucans (Ramphastos toco).Journal of Experimental Biology, 226, jeb245268. doi:10.1242/jeb.245268.
Acknowledgements
We wish to acknowledge Guilherme Gomes and Ariovaldo Pereira da Cruz-Neto for assistance with experiments and preliminary data analysis, and Luá T. Timpone and Adriana Fuga for assistance with animal care.
Our study on star-nosed moles was recently accepted in the Journal of Experimental Biology! In it we (myself and Kevin Campbell from University of Manitoba) present on a curious observation that the fleshy, tentacled nose of the star-nosed mole does not show much evidence for elevated blood flow, even when the moles encounter warm temperatures. Indeed, the highly mechanosensitive nasal rays of the star-nosed mole thermo-conform closely with ambient temperature thereby minimizing heat loss without apparent changes in sensory performance. Because this was a non-invasive study, we have to use thermo-conformation as a proxy for blood flow, and discover that they really don’t have high blood flow to the rays!
Abstract of the study
The star-nosed mole (Condylura cristata) is renowned for its densely innervated 22 appendage star-like rostrum (‘star’) specialised for tactile sensation. As a northerly distributed insectivorous mammal exploiting aquatic and terrestrial habitats, these vascularized nasal rays are regularly exposed to cold water and thermally conductive soil, leading us to ask whether the star surface temperature, a proxy for blood flow, conforms to the local ambient temperature to conserve body heat. Alternatively, given the exquisite sensory nature of the star, we posited that the uninsulated rays may be kept warm when foraging to maintain high mechanosensory function. To test these hypotheses, we remotely monitored surface temperatures in wild-caught star-nosed moles. While the tail acted as a thermal window exhibiting clear vasoconstriction/vasodilation, the star varied passively in surface temperature, with little evidence for thermoregulatory vasomotion. This thermoconforming response may have evolved to minimize conductive heat loss to the water or wet soils when foraging.
Note: WordPress may have mangled the videos. Looking into fixing….
Bottom view of the star-nosed mole searching the ground with its star. Blink and you’ll miss it.
Bottom view of a star-nosed mole foraging on an earth worm. One of the world’s fastest eaters!
A rare video / timelapse of a star-nosed mole standing still. In this case it is grooming. This is the only time we observed the star showing any evident “body heat” warming up the star itself. Watch up to the end to see the brief vasodilation to the star before the mole walks off scene. Usually the star remains at or slightly below ambient temperature.
Backstory
This work took place in Northern Ontario in the summer 2022, as the first sabbatical project I took on board this past year. Kevin Campbell was hosting two film crews out at his field site, and invited me to “tag along” (i.e. research) with the group. My lab been interested in the inter-play between temperature and sensory functions (plus a 4th year course I teach concerns neuro-ethology and sensory ecology/physiology, so this was a fun way to explore teaching/research overlap). Best (and only) two weeks I have ever spent working in a garage/film set. Also, no trip to northern Ontario would be complete without a picture of the resident loon from the cottage.
Citation
Tattersall, GJ and Campbell, KL. 2023. Thermoconforming rays of the star-nosed mole. J Exp Biol 2023; jeb.245127. https://doi.org/10.1242/jeb.245127
We thank Josh Campbell for assistance with mole capture, and the British Broadcasting Corporation Studios Natural History Unit for accommodating this study. This research was supported by NSERC Discovery Grants to GJT (RGPIN-2020-05089) and KLC (RGPIN-2016-06562) and an NSERC Research Tools and Instrumentation Grant to GJT (NSERC RTI-2021-00278).
Our study that started in 2017 has finally been published! Congratulations to Dr. Erich Eberts, who was project lead for this project while he was finishing his undergraduate degree at Loyola Marymount University, and who stuck with the writing, analysis, and manuscript handling. It is rather apt that the study was accepted and In Press around about the same time that Dr. Eberts defended his PhD!
Here is the abstract:
Reproduction entails a trade-off between short-term energetic costs and long-term fitness benefits. This is especially apparent in small endotherms that exhibit high mass-specific metabolic rates and live in unpredictable environments. Many of these animals use torpor, substantially reducing their metabolic rate and often body temperature to cope with high energetic demands during non-foraging periods. In birds, when the incubating parent uses torpor, the lowered temperatures that thermally sensitive offspring experience could delay development or increase mortality risk. We used thermal imaging to noninvasively explore how nesting female hummingbirds sustain their own energy balance while effectively incubating their offspring. We located 67 active Allen’s hummingbird (Selasphorus sasin) nests in Los Angeles, California and recorded nightly time-lapse thermal images at 14 of these nests for 108 nights using thermal cameras. We found that nesting females usually avoided entering torpor, with one bird entering deep torpor on two nights (2% of nights), and two other birds possibly using shallow torpor on three nights (3% of nights). We also modeled nightly energetic requirements of a bird experiencing nest temperatures vs. ambient temperature and using torpor or remaining normothermic, using data from similarly-sized broad-billed hummingbirds. Overall, we suggest that the warm environment of the nest, and possibly shallow torpor, help brooding female hummingbirds reduce their own energy requirements while prioritizing the energetic demands of their offspring.
Thermal images of a normothermic hummingbird (A) and one in torpor (B). Right hand images are a 3D-rendering of the surface temperatures.Digital and thermal images of eggs and hatchling hummingbirds.
Thermal video of a Ruby-throated hummingbird feeding from a feeding station. Video captured at Brock University in 2012, and has no association with the study.
Citation
Eberts, ER, Tattersall, GJ, Auger, PJ, Curley, M, Morado, MI, Strauss, EG, Powers, DR, Camacho, NM, Tobalske, BW, and Shankar, A. 2022. Free-living Allen’s hummingbirds (Selasphorus sasin) rarely use torpor while nesting. Journal of Thermal Biology. Available online 5 December 2022, 103391. https://doi.org/10.1016/j.jtherbio.2022.103391
Acknowledgements
We thank the numerous undergraduate assistants who completed much of the nest searching, equipment maintenance, and data collection, CURes, the LMU grounds and facilities maintenance staff for assisting with the location of and access to nests. We also thank Susan Wethington for providing broad-bill hummingbird nests. We also thank Welch lab members (University of Toronto) for helpful discussions. We especially thank our crowdfunding campaign donors who participated in the Experiment.com crowd-source campaign and FLIR Systems for their support.
Bergmann’s and Allen’s rules state that endotherms should be larger and have shorter appendages in cooler climates. However, the drivers of these rules are not clear. Both rules could be explained by adaptation for improved thermoregulation, including plastic responses to temperature in early life.
Our study has just been published in Nature Communications here:
Non-thermal explanations are also plausible as climate impacts other factors that influence size and shape, including starvation risk, predation risk, and foraging ecology. In this study, we assess the potential drivers of Bergmann’s and Allen’s rules in 30 shorebird species using extensive field data (>200,000 observations). We show birds in hot, tropical northern Australia have longer bills and smaller bodies than conspecifics in temperate, southern Australia, conforming with both ecogeographical rules.
Heat map of Australia, including the sample sites where morphological data from >30 species of shorebirds were used.
This pattern is consistent across ecologically diverse species, including migratory birds that spend early life in the Arctic. Our findings best support the hypothesis that thermoregulatory adaptation to warm climates drives latitudinal patterns in shorebird size and shape.
Acknowledgements
Dr. Alexandra McQueen (Post-Doc at Deakin University) did most of the work on this manuscript. The Victorian Wader Study Group and the Australasian Water Studies Group were responsible for the 46 years worth of data collected that made this study possible. My thanks to Matt Symonds and Marcel Dekker for including me in this study, a result made possible from an Australian Research Council Discovery Grant.
Citation
McQueen A, Klaassen M, Tattersall GJ, Atkinson R, Jessop R, Hassell CJ, Christie M; Victorian Wader Study Group; Australasian Wader Studies Group, Symonds MRE. 2022. Thermal adaptation best explains Bergmann’s and Allen’s Rules across ecologically diverse shorebirds. Nat Commun13, 4727. https://doi.org/10.1038/s41467-022-32108-3
I’m happy to report on a paper from Matt Pamenter’s lab (U Ottawa) that has just been published in Nature Communications. Matt and colleagues teamed up to examine how naked mole rats show a remarkable capacity to rapidly down-regulate UCP1 levels in their brown fat. It might come as a bit of a surprise to some to hear that naked mole-rats even have functional UCP1, since they are often described as “poikilothermic” mammals, not capable of producing heat. This is actually not entirely accurate, as can be seen in thermal images of naked mole-rats (Figure 1 below from Cheng et al 2021), they have a substantial band of heat within their shoulder region, where the brown fat lies.
Figure 1. Thermogenesis ceases in acute hypoxia and body temperature drops to ambient levels.
Naked mole-rats are among the most hypoxia-tolerant mammals. During hypoxia, their body temperature (Tb) decreases via unknown mechanisms to conserve energy. In small mammals, non-shivering thermogenesis in brown adipose tissue (BAT) is critical to Tb regulation; therefore, we hypothesized that hypoxia decreases naked mole-rat BAT thermogenesis. To test this, we measure changes in Tb during normoxia and hypoxia (7% O2; 1–3 h). We report that interscapular thermogenesis is high in normoxia but ceases during hypoxia, and Tb decreases. Furthermore, in BAT from animals treated in hypoxia, UCP1 and mitochondrial complexes I-V protein expression rapidly decrease, while mitochondria undergo fission, and apoptosis and mitophagy are inhibited. Finally, UCP1 expression decreases in hypoxia in three other social African mole-rat species, but not a solitary species. These findings suggest that the ability to rapidly down-regulate thermogenesis to conserve oxygen in hypoxia may have evolved preferentially in social species.
This work was a team effort, lead by Dr. Matt Pamenter’s lab at U Ottawa and Dr. Mary-Ellen Harper (U Ottawa), and included colleagues from the University of Pretoria, and University of Shaqra, Saudi Arabia, and myself (Brock University).
Cheng, H, Rebaa, R, Malholtra, N, Lacost, B, El Hankouri, Z, Kirby, A, Bennett, NC, van Jaarsveld, B, Hart, DW, Tattersall, GJ, Harper, M-E, and Pamenter, ME. 2021. Naked mole-rat brown fat thermogenesis is diminished during hypoxia through a rapid decrease in UCP1. Nature Communications, 12: 6801.https://doi.org/10.1038/s41467-021-27170-2
I’m happy to report that our paper entitled “Staying warm is not the norm: Behavioural differences in thermoregulation in two snake species” is published in the Canadian Journal of Zoology at the following link:
Congratulations to the team in my lab for pulling this paper together.
In this study, we focus on laboratory measurements of behaviours (in two species of snakes) related to temperature regulation to highlight methodological approaches to studying thermoregulation in ectotherms.
Over the past few years, we have read a lot of papers that report on thermoregulation in ectotherms, but we have felt that critical information on whether the animals are purposely thermoregulating is missing. How do you know they are thermoregulating? Is it sufficient to simply examine their position within the thermal gradient? Perhaps the direction they orient is important to establishing their motivations? How do you know an ectotherm is thermoregulating rather than simply moving around at random? Maybe accounting for activity and exploration effects in these studies can help make a difference? These topics have been covered in a number of other papers from our laboratory (Wang et al 2019; Black and Tattersall, 2017; Black et al, 2019), but we test them here using two species of snakes with contrasting life histories, where we would expect different thermoregulatory preferences given the different microhabitats preferred in nature.
These are some of the questions we focus on in this study of the Eastern Garter Snake (Thamnophis sirtalis sirtalis) and the semi-fossorial Northern Red-bellied Snake (Storeria occipitomaculata occipitomaculata). While we do report that the semi-fossorial snakes appear to prefer cooler temperatures, please read the paper for some of the more subtle differences between these species.
Anyhow, we hope to convince fellow researchers to report on these sort of behaviours since they may likely be helpful in bolstering the case that the animal is motivated to select temperatures.
Video time lapse of a garter snake in a circular / doughnut shaped thermal gradient.Thermal gradient used in the study.
Citation
Giacometti, D., Yagi, KT, Abney, CR, Jung, MP, and Tattersall, GJ. 2021. Staying warm is not always the norm: Behavioural differences in thermoregulation of two snake species. Canadian Journal of Zoology, Accepted, Aug 25 2021.http://doi.org/10.1139/cjz-2021-0135
Many thanks to the co-authors in this study. This research was originally part of Curtis Abney’s MSc thesis, supplemented with Matthew Jung’s Honours thesis (with input and guidance from Dr. Katherine Yagi), and brought together by the fine analytical and writing skills of Danilo Giacometti.
Black, IRG, Berman, JM, Cadena, V, and Tattersall, GJ. 2019. Behavioral thermoregulation in lizards: Strategies for achieving preferred temperature. In: Behavior of Lizards: Evolutionary and Mechanistic Perspectives, Eds. Vincent Bels and Anthony Russell, CRC Press, 410 pp.
Wang, SYS, Tattersall, GJ, and Koprivnikar, J. 2019. Trematode parasite infection affects temperature selection in aquatic host snails.Physiological and Biochemical Zoology. 92(1):71-79. https://doi.org/10.1086/701236
Nick Sakich here. The first paper from my MSc has just been published in the Journal of Experimental Biology. The paper is entitled, “Bearded dragons (Pogona vitticeps) with reduced scalation lose water faster but do not have substantially different thermal preferences.”
In it, we examine both “wild-type” bearded dragons and two phenotypes unique to captivity (i.e. not found naturally): animals with scales of reduced prominence (known as “leatherbacks”) and completely scaleless animals (known as “silkbacks”). The following slideshow depicts the 3 variants:
There has long been speculation as to whether or not scales play a role in reducing evaporative water loss across the skin in reptiles. The seminal studies that most point to are by Licht and Bennett (1972) and Bennett and Licht (1975). Those authors looked at aberrant partially scaleless individual snakes found living in the wild and found that they did not have higher rates of water loss than “normal” snakes. However, these studies had some methodological issues, most notably sample sizes of only one (Licht and Bennett, 1972) and two (Bennett and Licht, 1975) partially scaleless snakes, respectively.
Furthermore, can reptiles (or lizards and snakes, at least) detect their rate of evaporative water loss and respond accordingly? If they can, animals with higher rates of evaporative water loss will perhaps choose cooler temperatures compared to animals with lower rates of evaporative water loss. The rate of evaporative water loss is partially thermally dependent, so for the animals this would be a way to compensate and bring their rate of evaporative water loss down.
In this study, we set out to test two hypotheses. First, we hypothesized that scales are indeed a barrier to evaporative water loss, and so leatherbacks and silkbacks would have higher rates of evaporative water loss than wild-types. Second, we hypothesized that, because of this increased rate of evaporative water loss, leatherbacks and silkbacks would have lower thermal preferences than wild-types.
We found support for our first hypothesis: both leatherbacks and silkbacks evaporated water faster than wild-types. It is likely that most of this occurs across the skin, rather than through changes in breathing or metabolism, given the simultaneous measurements we made of metabolism. This confirms what many who keep silkbacks as pets have long suspected. However, we didn’t find a statistically significant difference in thermal preference between the three phenotypes. This suggests that either leatherbacks and silkbacks can’t tell that they’re losing water faster than wild-types, or that they can tell, but they make a strategic decision to prioritize warmth over water.
I’d like to thank Arnold Liendo and Paula Rodriguez, Mandy Peck, and Kirk Riddle for supplying us with lizards for this study. I’d also like to thank Tom Eles and Wynne Reichheld, without whom keeping up with the nuts-and-bolts of animal acquisition and care would have been impossible.
Citation
Sakich, NB and Tattersall, GJ. 2021. Bearded dragons (Pogona vitticeps) with reduced scalation lose water faster but do not have substantially different thermal preferences.Journal of Experimental Biology.224 (12): jeb234427.
A link to the pdf of the manuscript can be found here (limited to 50 clicks). Otherwise, requests for pdfs can be made on Researchgate.
References
Licht, P. and Bennett, A. F. (1972). A scaleless snake: tests of the role of reptilian scales in water loss and heat transfer. Copeia 1972, 702-707. doi:10.2307/ 1442730
Bennett, A. F. and Licht, P. (1975). Evaporative water loss in scaleless snakes. Comp. Biochem. Physiol. A Physiol. 52, 213-215. doi:10.1016/S0300- 9629(75)80155-1
The following is a guest blog by Dr. Joshua Robertson Tabh
In my short research career, I’ve come to accept (even relish) that there are some projects that endlessly surprise; projects with shifting objectives that find you running drive-by thermal camera hand-offs along the QEW at questionable hours. The project that I’m about to describe is one of “those”. And curiously, despite the innumerable twists and turns, it just so happened to be a project with some of the most useful outcomes I’ve helped to produce. In this guest post, I’ll describe those outcomes.
But first, let’s begin in 2016. I had just begun my PhD research in avian stress physiology, and mere months before, Paul Jerem and others had released a highly intriguing protocol which suggested that the physiological stress response could be detected, and possibly quantified, in birds by simply measuring changes in body surface temperature (https://www.jove.com/t/53184/thermal-imaging-to-study-stress-non-invasively-in-unrestrained-birds). The rationale behind their protocol was that following exposure to a stressor, the sympathetic nervous system triggers vasocontriction of blood vessels at the skin (among other things), which manifests as measurable changes in skin temperature. This idea isn’t new. Rather, it likely dates back to the early 20th century or previous (e.g. Wolff and Mittelman, 1937). However, Jerem et al’s protocol was the first to show that a stress-induced change in skin temperature could be detected at the eye region in a wild bird, using infrared thermography (see Edgar et al, 2013, for a study in chickens). A clever application of thermography.
Jerem et al’s work was exciting. But a few important questions seemed to linger:
(1) how well does this stress-induced change in eye region temperature reflect circulating changes in sympathetic nervous system markers (i.e. catecholamines, like adrenaline and noradrenaline)?
So, being nagged by these questions, a team of ecophysiologists (Glenn Tattersall, Gary Burness, and Oliver Wearing), an endocrinologist (Gaby Mastromonaco), and myself sought answers.
To do so, we required an experimental approach that would allow us to measure both body surface temperature (here, at the eye region and bill) and circulating catecholamines in “stressed” and “unstressed” birds. However, measuring circulating catecholamines requires sampling blood. And since puncturing a vein with a syringe is surely sufficient to activate a physiological stress response on its own (thus rendering “unstressed” birds “stressed”) blood sampling by this standard method simply wasn’t possible. Ideally, we would fit a sample of birds with central venous catheters to permit blood sampling without capture and venipuncture. This approach could work, however, even if blood samples were to be collected effectively, catecholamines can be a pain to quantify, even for contracted labs with high-end machinery. It’s for this latter reason that we accepted the reality of leaving our first research question unanswered.
Fig. (1) Domestic pigeon being monitored during rest, before experimentation.
Nevertheless, we could persist with a simple experimental design to answer research questions (2) and (3); quite simply, thermographically image birds during rest (Fig 1) and during a stress exposure (for us, handling). To answer question (2), we would then quantify and compare the magnitude of stress-induced changes at the eye region and bill. And lastly, to answer question (3), we would aim to test the effect of head angle on our ability to detect stress-induced changes in eye region and bill temperature. In theory, a nice and clean approach.
Before I get to the answers of our remaining research questions, a small note on how we estimated head angle (for the interested reader).
Estimating Head Angle from 2D Image
Estimating the orientation of a 3D object from a 2D angle has been a concern for humans since photography was invented. Among mathematicians, this challenge has since acquired a formal name: the “perspective-n-point” (or “PnP”) problem. All solutions to the PnP problem first require knowledge of where, in a 2D plane, at least 3 points in an imaged object lay. We’ll call these points “landmarks”. Of course, more than 3 landmarks are best to improve estimation accuracy, but most agree that 3 will do for a reasonable guess. Next, rough dimensions of the imaged object in 3D space are needed. Such dimensions must be sufficient for one to estimate where the chosen landmarks may lie, relative to each other, in a theoretical 3D co-ordinate system known as the “world co-ordinate system”.
Once this information is collected, several geometrical approaches may be used to calculate how the imaged object must have moved or rotated such that the landmarks in 3D space overlap with those observed in 2D space (after adjusted for lens distortion). Interestingly, there is one industry with considerable investment in creating efficient geometrical approaches: virtual reality (or “VR”) gaming. Why? Because using VR gaming requires that the system can estimate the gamer’s 3D position at all times (with, interestingly, tiny infra-red lights implanted in the headset as landmarks). Thanks to this investment by the VR industry, studies developing and comparing the accuracy of geometrical solutions to the PnP problem are flourishing. It’s a perfect time for biologists like us to start taking a peak at them.
For our study, we chose to use to an approach called the “EPnP” that was first proposed by Lepetit and others in 2009 (https://link.springer.com/content/pdf/10.1007/s11263-008-0152-6.pdf). We chose this approach because it permits one to use >4 landmarks for positional estimation (thus reducing error) with little cost to computational time relative to traditional solutions. Other approaches have been lauded for improving accuracy (e.g. P3P with RANSAC) and we encourage others to pursue those approaches. For our study, however, we were interested in balancing accuracy and efficiency.
To execute the EPnP approach, we estimated the 2D position of up to 9 landmarks on a pigeon’s head by loading our thermographic images into ImageJ (Fig 2). Building a 3D model turned out to be much less time consuming – simply draw on morphometric measurements of domestic pigeons reported in literature. From these data, and EPnP algorthims, we were thus able to estimate both a 3D translation and 3D rotation of an imaged bird’s head, relative to a virtual model of a perpendicularly facing individual.
Fig. (2) Thermographic image of a domestic pigeon with black dots marking 6 of 9 possible landmarks. The black line at the tip of the bill indicates the estimated direction in which the pigeon is facing.
Our results?
I’ll break them down by question.
Question (1): How well does this stress-induced change in eye region temperature reflect circulating changes in sympathetic nervous system markers (i.e. catecholamines, like adrenaline and noradrenaline)?
Answer: Our results suggest that, at least in our study species, surface temperature the bill is probably a better indicator of stress physiological state. I’ll explain why by referencing what we observed from data that did not control for head position. After stress exposure, bill temperature fell significantly by ~4°C after stress exposure (handling), while eye region temperature did not significantly change (Fig 3). Rather, temporal patterns in eye region temperature appeared remarkably similar between “stressed” and “unstressed” birds. Moreover, only stress-induced changes in bill temperature showed significant inter-individual variation, suggesting that if one wishes to build a metric of “stress-responsiveness” from changes in surface temperature, doing so at the bill is likely more effective than at the eye region.
Fig. (3) Changes in eye region and bill temperature across time in both stress-exposed and control birds. Time 0 (marked with a vertical dashed line) indicated that time that flight cages were opened to permit capture and handling of birds in the stress-exposed treatment group. Dots represent averages across birds per 5 seconds of observation, and lines of best fit represent trends estimated by generalised additive mixed-effects models. Ribbons represent 95% confidence intervals around trend estimates.
Question (3): How robust and reliably detectable are stress-induced changes in body surface temperature?
Answer: It depends on where you look. After correcting for changes in head position in our birds, a significant effect of stress-exposure on eye region temperature emerged (Fig 4). This was not the case for stress-induced changes in bill temperature, which were detectable regardless of whether head position was accounted for or not. This point, we think, is particularly important for two reasons:
(1) don’t correct for changes in object position and you risk missing out on detecting biological processes, and
(2) surface temperatures of some body regions might be better indicators of your biological process of interest than others.
Fig. (4) Change in eye region temperature of stress-exposed and control pigeons after correcting for changes in head orientation. Again, time 0 (marked with a vertical dashed line) indicated that time that flight cages were opened to permit capture and handling of birds in the stress-exposed treatment group. Dots represent averages across birds per 5 seconds of observation, and lines of best fit represent trends estimated by generalised additive mixed-effects models. Ribbons represent 95% confidence intervals around trend estimates.
Take Home Message
To conclude, drawing biological inference from thermographic images is tricky. Many sources of error can get in the way of your ability to meaningfully do so, and a common one is changes in object position. As such, biologist should always remember to correct for object position when working with their surface temperature data – perhaps by using our method or another.
Tabh, Joshua KR, Burness, G, Wearing, OH, Tattersall, GJ, Mastromonaco, GF. 2021. Infra-red thermography as a technique to measure physiological stress in birds: body region and image angle matter. Physiological Reports, Accepted.https://doi.org/10.14814/phy2.14865
Acknowledgements
Dr. Joshua Robertson Tabh is a graduate of Trent University, co-supervised by Dr. Gary Burness and Dr. Gaby Mastromonaco. This research was made possible with the cooperation of the Toronto Zoo and by the watchful eye of Oliver Wearing. Since 2016, Joshua and Glenn have shared many conversations about avian physiology, imaging, and coding and Glenn invited Joshua to guest author this post after all these efforts finally reached the publication stage.
Funding for this research was provided by the Toronto Zoo Foundation, an NSERC Collaborative Research and Training Experience Program (Grant #: CREATE 481954-2016), a Howard P. Whidden grant to OHW, and an NSERC Discovery Grant to GJT (Grant # RGPIN-2014-05814).
We’re happy to share news that our paper (shareable link) was recently accepted in Methods in Ecology and Evolution! As for the nitty gritty secrets of the study, that headline was to get your attention! I’ll point out some highlights here, with some visuals to summarize the main results.
The study resulted from a visiting PhD student (Núria Montmany-Playà, @NuriaBeachy) to the lab in January 2020, immediately prior to the pandemic and lock-down. Sadly, some of the research we planned to do was not possible due to travel restrictions and embassies immediately calling back their citizens. So, this represents about the only kind of research my lab is capable of doing during a lockdown.
So, what is the paper about? Technically, it’s a methods (thus the journal choice!) and resource paper (information on empirical measurements of emissivity which I often get from colleagues) with a warning to field thermographers to “check your distance“! (Actually, Faye et al 2016 already advised this, but given various interactions I have had over the past few years, some field thermographers might not be reading all the literature – so please read Faye et al’s paper cited at the bottom of this blog).
Distance Effects
It has become increasing common in some animal thermography studies to capture the maximum temperature from a specific region of the body (often the face or the eye) and use this as an estimate of body temperature (it is not a good estimate!) or as a proxy for vasoreactivity related to stress (which it is a better indicator of, although depends on species and body part). This effect of distance was earlier studied by Faye et al (2016), although we focus on the challenges in animal thermography in the field where animals control how close you can get! Watch the video below for the effect in action, paying attention to the maximum temperature in the eye region and how it changes as this Trumpeter swan walks closer (starting from ~15 m) and closer (~2 m) to the camera:
Thermal video of a Trumpeter swan walking toward the camera. Max refers to the maximum temperature being captured (see plus sign) in the face/eye region.
Here are the results plotted over time as an animated plot:
Animation of the estimated maximum eye region temperature as the Trumpeter swan walks closer to the camera. Distance estimates are calculated based on an empirical relationship based on the camera’s focus distance estimate and vary depending on the focus and region being assessed. The major drop in temperature ~9 metres was due to a brief period of time where the image was out of focus (showing how crucial focus effects can be!!).
As the bird gets closer, the maximum temperature of the same animal rises from a low of ~25C to reach closer to a more realistic value of ~33C. This is an enormous range and cannot reasonably be based on vasoreactivity, when the physics of thermal optics can explain this. Read the paper for the explanation behind how spot size and distance effects interact to produce fairly large errors in thermography. Controlling for distance and/or being aware of its influences is important to any field application of thermography. I doubt too many people are trying to image animals at 10 m away given the low resolution of many thermal cameras, but as prices come down and people take their devices into the field, I am sure researchers will run into these situations.
We measured the technical error using a blackbody calibration source placed at different distances from the camera, and tested under different conditions. Below, Tb refers to the blackbody temperature (i.e. true temperature) and Ta refers to prevailing ambient temperature. Delta T refers to how the thermal camera estimates the same black body temperature (where 0 refers to the closest distance measurement). We tested this with different camera/lens combinations to give insight into how the devices function even under well controlled conditions, far different from most field applications. You can see below that the error in temperature can be as poor as 6C below actual temperature at 10 m distance, and these results are for measurements of an electronic calibration source.
Error (Delta T = offset in estimated temperature from true temperature) as a function of distance from a calibration source as a function of camera/lens and background radiation difference from blackbody calibration temperature, Ta – Tb).
Angle Effects
Thermal image of an Atlantic puffin taken 0.97 seconds apart after the bird changes head position. This sudden change in the angle of the bill leads to a decline in estimated surface temperature, unlikely to result from vasoreactive physiological events.
We also published some simple results on how the angle of incidence influences thermography measurements (see image above of the puffin). This is also well known by thermal imaging engineers and physicists, but not likely well appreciated by biologists, so we used a Leslie cube (see image below) and adhered various bits of biological materials to a copper surface, heated the surface up and painstakingly measured the temperature, allowing us to calculate the apparent emissivity. Objects at steep angles of incidence to the camera will have a lower emissivity, which means that the apparent radiation we measure is actually a lot of background reflected radiation, and thus is a source of possible error in field thermography.
A Leslie cube is typically made of copper or a highly conductive metal, onto which a surface paint or test material is adhered. The copper allows the material to be heated up to a constant temperature, while the angle of incidence can be adjusted and the apparent radiation (or temperature) of the surface of interest be estimated. The image above shows the same surface measured at different angles; at steeper angles the surface (dotted lines) appears cooler because it is reflecting more of the cooler room radiation back to the observer.
So the main message of the paper is to keep good records of how far your camera is from your object of study. Correcting for this effect is complex and beyond the scope of our study, although we report that the potential error of being 10 meters away from an object can be as high as 4 to 6C, with similar errors for measuring objects at angles greater than 50 degrees incidence.
Acknowledgements
Many thanks to Núria for her hard work on this project. Without her visit, we would not have done this. And we also want to thank the two reviewers for their hard but fair questions but also for listening to our response.
Lockdown science had me borrowing plant material from my parents, Clifford and Brenda Tattersall, so their help was crucial to the final acceptance of the manuscript!
Citation
Montmany-Playà, N. and Tattersall, GJ. 2021. Spot size, distance, and emissivity errors in field applications of infrared thermography. Methods in Ecology and Evolution.https://doi.org/10.1111/2041-210X.13563
A luna moth was on our window outside the department yesterday.
So, we brought it inside for a lab show and tell. Shivering up a storm….
Thorax temperature up to 32C, while the abdomen temperature was still below 20C (the lab was ~21C, and the moth had been briefly placed in a cold fridge).
Tattersall Lab (TEMP) 