Author: gtattersall

Unearthing energetic mysteries: exploring metabolic rates in fossorial amphibians

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The following is a guest blog by Danilo Giacometti, MSc.

Background

By living underground or in burrows, fossorial animals benefit from protection against predators and climatic buffering. This seclusion, however, may lead to increased exposure to low O2 (hypoxia) and high CO2 (hypercarbia) levels in burrows. Hypoxia and hypercarbia are well known to impact respiration and energetics in both endotherms and ectotherms. If exposure to hypoxic and hypercarbic conditions persist over the long term (i.e., across generations), natural selection should favour organisms with a blunted sensitivity to gas exchange limitations. As such, fossoriality has long been associated with energy conservation. Most of the evidence in favour of fossorial species having low energetic requirements comes from work in mammals. By studying the metabolism of rodents, McNab (1966) suggested that fossorial species had convergently evolved low metabolic rates compared to non-fossorial ones. McNab’s logic was straightforward: given an energetic stressor (i.e., hypoxia and hypercarbia), natural selection favoured a physiological adaptation (i.e., low metabolic rates) that would minimise O2 depletion and CO2 buildup.

Almost 20 years later, this hypothesis was extended to explain metabolic adaptations in squamate reptiles by Andrews & Pough (1985). Although other researchers attempted to elucidate whether fossoriality had impacted the metabolism of vertebrate ectotherms (e.g., Kamel & Gatten, 1983; Ultsh & Anderson, 1988; Withers, 1981), most studies were limited by a small number of species used in comparisons, lack of phylogenetic control, and improper consideration of body mass effects over metabolism. Perhaps the most important consideration in this context comes from Wang & Abe (1994), who called attention to the fact that the metabolism of vertebrate ectotherms is intrinsically lower than that of endotherms. Thus, a further reduction in metabolism driven solely by fossoriality would be evolutionarily unlikely given the limited energetic benefit. In this sense, the impact of fossoriality on the metabolic rates of vertebrate ectotherms has remained unclear.

What did we do?

With this in mind, we addressed whether fossorial amphibians were selected for lowered metabolic rates compared to non-fossorial and aquatic ones in a phylogenetic framework. Building from a compilation of amphibian metabolic rates found in Chapter 12 of Feder & Burggren (1992), we collated a dataset with information on metabolic rates, test temperature, body mass, latitude, lifestyle, and phylogenetic relatedness of 185 species of amphibians (Fig. 1). Details on our methodology, inclusion criteria, and analyses can be found in our manuscript.

Fig. 1. States of lifestyle (aquatic, fossorial, or non-fossorial) plotted along the tips of the phylogeny representing the relationship among the 185 species contained in our dataset. We obtained silhouettes of representatives of major amphibian families from PhyloPic’s public repository.

What did we find?

Thermal and body mass effects over metabolic rates

As expected, both test temperature and body mass explained differences in metabolism among species (Fig. 2). Metabolic rates increased with temperature; however, the thermal dependence of metabolism did not differ among lifestyles (Fig. 2A). Additionally, our results are in concert with the principle of metabolic scaling, as body mass was the primary determinant of metabolic rate variation after accounting for phylogenetic effects. In general, the larger the species, the higher its metabolic rate—once again, regardless of lifestyle (Fig. 2B). This finding fits in with the framework proposed by White et al. (2022), who argued that metabolic scaling is the outcome of optimised growth and reproduction. Considering that we found metabolism and body size to be inextricably correlated in amphibians, life history optimisation could be the mechanism behind our recovered pattern.

Fig. 2. A. Variation of predicted metabolic rates (logV̇O2) across test temperatures for the 185 species considered in this study. logV̇O2 increased with test temperature, as indicated by the red dots and their corresponding confidence limits (red bars). B. Phylogenetically controlled linear regression depicting the scaling between predicted logV̇O2 values and logBody Mass. The solid red line and grey shaded area indicate the predicted relationship between the two variables and the 95% confidence interval, respectively.

Unraveling the mysteries of fossoriality: potential roles of cutaneous breathing

Our results revealed that fossorial amphibians do not have lower metabolic rates compared to their non-fossorial and aquatic counterparts after controlling for body mass, temperature, and phylogenetic effects. We suggest that the low energetic requirements of amphibians, coupled with their efficient cutaneous and pulmonary respiration capabilities, may explain why fossoriality did not impinge on their metabolism. Preliminary work in caecilians showed that fossorial species can sustain energetic requirements solely through cutaneous breathing, suggesting increased reliance on skin breathing and enhanced control of bimodal breathing in this group (Smits & Flanagin, 1994). We suggest that further research into the blood respiratory properties and bimodal breathing capacities of fossorial versus non-fossorial amphibians should provide valuable insights into their energy-saving strategies.

Conclusion

Through a comprehensive comparative analysis, we bring to light the complex interplay of factors influencing the metabolism of amphibians. Our work emphasises the central role of body mass and temperature in determining metabolic rates and suggest the possibility that the unique respiratory physiology of amphibians may have contributed to offset the effects of fossoriality over energetics in this group. As research continues to unearth the mysteries of fossoriality, it promises to deepen our appreciation for the remarkable adaptations of these unique creatures living beneath the surface.

Our article will be freely available for eight weeks on initial publication. Read the full study here.

Citation

Giacometti, D and Tattersall, GJ. 2023. Putting the energetic‐savings hypothesis underground: fossoriality does not affect metabolic rates in amphibians. Evolutionary Ecology, In Press.

Acknowledgements

We thank Leonardo Servino for helping us obtain geographic coordinates for the species in our dataset. We also thank the two anonymous reviewers whose comments helped improve our manuscript. Research funding was provided by a Natural Sciences and Engineering Research Council of Canada Discovery Grant to GJT (RGPIN-2020-05089).

Hermit crabs going boldly into the sun

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Long time in coming, but Phil Bartel’s Honours project was just accepted for publication in Behavioural Processes! We explored the influence of temperature on boldness, a personality trait, and more specifically the repeatability of these behaviours as a function of temperature.

Hermit crab (Coenobita clypeatus) walking on sun exposed sand (Belize).

Abstract to the study:

An animal’s boldness is generally considered to be influenced by genetic and developmental factors. However, abiotic factors such as temperature have profound effects on the physiology of ectothermic animals, and thus can influence the expression and measurement of this behavioural trait. We examined the relationship between temperature and behaviour in the Caribbean hermit crab (Coenobita clypeatus) using field and lab experiments. Crabs captured in the sun were bolder than crabs captured in the shade, even when measured at a common temperature, which led to bold crabs experiencing higher microhabitat temperatures. In laboratory housed conditions, crabs demonstrated highly repeatable boldness behaviours at all temperatures, and as temperature increased, the mean behavioural latencies decreased across all individuals. Bolder crabs do not seem to rely on an innately higher thermal preference, since there was no association between boldness behaviours and thermal preference in the laboratory.  Instead, bolder crabs seem to exploit more open, riskier habitats than shyer crabs. Our results highlight the complex interplay between physiological and ecological factors influencing the behaviour of a widespread and ecologically important ectothermic animal.

Influence of capture location on boldness related behaviour in Coenobita clypeatus showing that animals captured in sunnier locations exhibited bolder behaviours when tested at a common temperature.

For quick access to the paper (50 free clicks until September 2023):

https://authors.elsevier.com/a/1hR1o1LenMUgoK

Citation

Sakich, NB, Bartel, PC, Richards, MR, and Tattersall, GJ. 2023. Hot crabs with bold choices: temperature has little impact on behavioural repeatability in Caribbean hermit crabs. Behavioural Processes, 210: 104916. https://doi.org/10.1016/j.beproc.2023.104916

Acknowledgements

This project emerged from years of running Animal Behaviour labs with 3rd year undergraduates, teaching them about animal personalities, so we wish to the numerous cohorts of Animal Behaviour students who explored hermit crab behaviours with us, and inspired the project.

Congratulations in order!

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Belatedly, congratulations to Melanie Denommé Stauder (newly married just this month as well) for being awarded an NSERC PGS-D for her PhD research in my lab. While my announcement is a little late, I was in the field when the results came in and unable to post online. Her PhD research on the “Effects of enclosure style on the behaviour and physiology of captive-bred bearded dragons (Pogona vitticeps)” is really starting to shape up with some exciting discoveries and she has brought a whole series of new insights to the lab. Every day is a positive learning experience for me!

Congratulations in order

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Congratulations to Danilo Giacometti for proving that applying for scholarships/grants can pay off. Recently he found out he was the recipient of the Roger Conant award to support his salamander thermal biology research AND a travel award to attend the upcoming SSAR in Virginia AND he most recently found out that he has been invited to attend the RIBBiTR workshop in Costa Rica to learn techniques on research into conservation in amphibians.

I do have such great students!

Toucans make do without bill heat transfer, but with a cost.

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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. 

Toco toucan (Ramphastos toco)

For a great summary of the article by Kathryn Knight, please see the Inside JEB article “Toucans’ ostentatious beaks do not expand their thermoneutral zone“.

Link

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.

Star-nosed moles have chilly stars

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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.

Gallery Images

Close-up image of the star of the star-nosed mole. © Joel Sartore/Photo Ark
Thermal image of star-nosed mole in an artificial burrow.

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

Link to the paper (50 free clicks)

Acknowledgements

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).

Data Repository

The data from the paper are shared in the following open repository: http://hdl.handle.net/10464/16980

Hummingbirds rarely use torpor when incubating eggs

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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.

Ultraviolet Sensing Behaviour in Bearded Dragons

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Exposure to ultraviolet (UV) light has both physiological benefits as well as costs. Many lepidosaur reptiles can behaviourally self-regulate their exposure to UV light in order to take advantage of the benefits of UV light while minimizing the costs. Furthermore, lepidosaur scales have been conceptualized by some as a barrier to the penetration of UV light.

In a recently published study, we (Nick Sakich, recent graduate from the lab) examine regulation of self-exposure to UV light in three different phenotypes of Bearded Dragon (Pogona vitticeps): wild type, animals exhibiting scales of reduced prominence (‘Leatherback’), and scaleless animals (‘Silkback’). These scaleless mutants have arisen in the captive reptile husbandry industry. All phenotypes were tested in a 3 chamber system, offered 3 different intensity of standard basking lamps to assess how long they spent under each UV lamp.

Silkbacks on average chose to expose themselves to lower levels of UV light irradiation than Leatherbacks or wild types did, which suggests that the ability for UV to penetration through the skin is diminished in normal scaled phenotypes.

Simultaneously, we tested their self-exposure behaviour while they were able to choose cold or warm temperatures. Bearded Dragons of all scalation phenotypes received higher UV irradiation when they were in the cold section of a UV gradient apparatus compared to when they were in the hot section of the apparatus. This either demonstrates that Bearded Dragons under higher UV irradiances choose cooler temperatures or demonstrates that Bearded Dragons at cooler temperatures choose higher UV irradiances. The relationship between chosen temperature and chosen UV light irradiance was not affected by scalation phenotype.

This study highlights external influences on the mechanism that regulates UV self-exposure behavior in lepidosaur reptiles. Scales are apparently a barrier to UV absorbance, and thus scaleless lizards need to adjust their time exposed to UV light.

One logical interpretation the temperature sensitive UV seeking behaviour shows evidence that when cold, lizards may adopt UV seeking behaviour in an attempt to bask (i.e. an attempt to warm up) as would happen in the wild when basking in the sun. In our study, the UV bulbs were fluorescent bulbs and not radiant bulbs, and thus lizards may spend preferentially more time exposed to UV as part of their natural basking behaviour.

Figures and citation are provided below:

Wildtype Bearded Dragon (juvenile)
Leatherback phenotype of bearded dragon (juvenile)
Silkback phenotype of bearded dragon (juvenile)
Ultraviolet light test chamber involve 3 separate ‘basking’ sites partitioned within a circular chamber. Bearded dragons were free to move between the partitions due to gaps underneath the vertical baffles. The floor was kept at the preferred temperature (35°C) within the red zone, and allow to fall to room temperature (22-24°C) outside of that zone. This created allowed us to track the UV preferences while lizards were selecting warm or cool temperatures.

For those wishing to see a pdf of our article, for the next 50 days, free access is available at the following link: https://www.ichthyologyandherpetology.org/ihbjbb/ovh2020134ug688044yq

Alternatively, please request access to a pdf from Researchgate.

Citation

Sakich, N and Tattersall, GJ. 2022. Regulation of exposure to ultraviolet light in bearded dragons (Pogona vitticeps) in relation to temperature and scalation phenotype. Ichthyology and Herpetology, 110: 477-488. https://doi.org/10.1643/h2020134

Thermal adaptations best explain biogeographic rules in Australian shorebirds

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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:

https://www.nature.com/articles/s41467-022-32108-3

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 Commun 13, 4727. https://doi.org/10.1038/s41467-022-32108-3