#Amphibian

Supercool Survival Strategies of Blue-Spotted Salamanders

/ gtattersall

In the cold, temperate forests, long before spring fully arrives, blue-spotted salamanders (Ambystoma laterale) are already on the move. These small amphibians begin migrating to their breeding ponds while snow still blankets the ground and ice lingers on and in the soil. This is a risky strategy for a species that can’t survive freezing. Our recent Natural History note, spearheaded by Dr. Danilo Giacometti and published in the Canadian Journal of Zoology, documents this remarkable early migration and presents new thermal imaging evidence that blue-spotted salamanders achieve this while at sub-zero body temperatures.

Blue-spotted salamander (Ambystoma laterale), navigating the forest floor (Photo by D. Giacometti©)

For amphibians like blue-spotted salamanders, freezing is typically fatal. Ice crystals rupture cells, leading to irreversible damage. Unlike some frogs that survive being partially frozen thanks to natural antifreezes like glucose, blue-spotted salamanders are known to be freeze-intolerant. 

But in spring 2022 in Algonquin Park, during a brief window of opportunity we observed salamanders actively migrating, even while walking across or sheltering beside ice. Using high-resolution thermal imaging, we measured their skin temperatures (a reliable proxy for body temperature in such small animals) and found several individuals with body temperatures as low as –3.6°C, which is well below their known freezing point. Our findings suggest that blue-spotted salamanders may rely on supercooling, where their body fluids remain liquid even below freezing. This strategy has been shown in lab studies to be possible down to about –1.5°C, but our field data suggest some individuals may supercool even further, albeit briefly. 

One of the most surprising observations was that several salamanders were in direct contact with ice, a known trigger for freezing of fluids that are supercooled. Despite this, they were active and moving, raising fascinating questions about how they might avoid nucleation (the start of ice formation) in natural settings or if they can manage short-term freeze/thaw during their migration.

Thermal images of blue spotted salamanders migrating at sub-zero temperatures. Temperatures reflect variation in microhabitats encountered by animals during movement, and these observed skin temperatures fall below the known freezing points and minimum supercooling points for Ambystoma laterale.

Why would salamanders take such a risk by migrating so early? There may be several evolutionary advantages. By arriving at breeding ponds early before other species, they reduce competition and potentially avoid predators. Early breeding also gives their offspring more time to grow before winter returns.

Our study opens new questions about the limits of amphibian cold tolerance and the role of behavior and microhabitat selection. More research is needed to understand whether these salamanders truly remain supercooled for long periods or whether they occasionally freeze and recover, a possibility hinted at but not yet proven in this species.

For now, our thermal images offer a rare glimpse into the early spring lives of blue-spotted salamanders and reveal that there’s still much to learn about how animals survive the cold.

You can access our open data and images here: https://doi.org/10.5683/SP3/FZJBQH and the paper at the following doi:

Citation

Giacometti, D, Moldowan, P, and Tattersall, GJ. 2025.  Sub-zero body temperatures during early spring migration in blue-spotted salamanders (Ambystoma laterale). Canadian Journal of Zoology, https://doi.org/10.1139/cjz-2025-0045

Postscript: An Editor’s Lament

The journey that this very brief natural history note took to reach publication was unnecessarily arduous. We originally submitted this study to Canadian Field Naturalist in August 2022.  In that initial submission, we heard back after 16 months from the editor that the manuscript had been peer reviewed (3 reviewers) and with straightforward revisions; we supplied revisions within 30 days in January 2024. Then all went quiet with the journal for months. We reached out on numerous occasions to the editors in 2024 about whether the manuscript was still being handled, whether we would hear a decision, and received responses that indicated that editing it was not a high priority.

So, after 2.5 years sitting with Canadian Field Naturalist, we withdrew the manuscript (Spring 2025) and submitted it to CJZ where I am pleased to note that the manuscript underwent a normal peer review process. 

As an editor (the average turnaround time for 1st submit Major/Minor decision papers I handle is 51 days – this includes the time to find reviewers), I was saddened at how CFN handled the initial manuscript. There were extenuating circumstances in that the associate editor handling the initial submission passed away, but we were assured by the editorial team that the manuscript would not get ‘lost’ in the re-shuffle. 

As a society journal, it deserves support, but 2.5 years to handle a short manuscript does not set a good example for early career researchers; this is almost a lifetime for a graduate student. 

I understand that editors need to make difficult decisions and in the course of those duties often reject studies (for fit or for other reasons). But timely decision making is just as important or more so for early career researchers. All the academic editors I know are full-time employed with academic and research jobs, but I have never heard any of them indicate or hint to an author that their submission is not a priority. If the work is not appropriate for the journal, the most humane decision is to reject it in a timely manner.

Anyhow, I am pleased with the Canadian Journal of Zoology’s handling of the manuscript.  It was professional and straightforward and now we can move on from this experience.

I do think that we need to support natural history style studies/observations, so I can only hope that by sharing this, those that read this may push for change at journals that could use the support.

Hydro Hackers: How Salamanders Outsmart “the Drying”

/ gtattersall

For amphibians, water is everything. Their thin skin makes them especially vulnerable to drying out, so staying hydrated is not just about comfort—it is about survival. But how do amphibians manage their hydration state in the face of different temperatures and fluctuating humidity? 

Our recent study on spotted salamanders (Ambystoma maculatum) provides some new insights into this question. We exposed salamanders to two temperatures—17°C and 22°C—within a humidity gradient (Fig 1) to understand how salamanders behaved when given the choice to move toward more or less humid conditions under contrasting thermal conditions.

Figure 1. Schematic of the humidity gradient, showing how salamanders can freely move throughout a circular environment to select from low to high humidity.

We found that salamanders consistently selected localities in the gradient that maintained a constant vapour pressure deficit (VPD), which is the key variable driving evaporative water loss (Figure 2).  VPD reflects a more physiologically relevant metric for the “drying power” of air. Since they behaviourally regulate a constant VPD regardless of temperature, this provides support for a humidistat (i.e., that they regulate their water loss).

Figure 2. Summary of the selected VPD and selected RH for spotted salamanders tested at 17 and 22C.

Virtually, what this means is that salamanders prefer higher relative humidity (RH) at 22°C than at 17°C to offset the increased drying power of the air at warmer temperatures. This suggests that salamanders are not just responding to RH or temperature independently. Instead, they are tuning into the combined effects that actually influence water loss.

Additionally, salamanders that selected higher VPDs (i.e., dryer conditions) lost more water, and body size also mattered, as larger individuals lost more water than smaller ones even after accounting for temperature. This highlights a trade-off between body size, humidity preference, and the risk of dehydration. 

Temperature also played an important role in rehydration. Salamanders rehydrated faster at 22°C than at 17°C, suggesting that warmer conditions may boost water uptake—perhaps because of increased skin permeability at warmer temperatures, or from active processes that promote water uptake.

One of the most intriguing findings was the idea that salamanders might be able to sense how much water they are losing. We propose that local evaporative cooling of the skin—especially on the parts exposed to air—could serve as a sensory cue. If the dorsal skin is cooler than the ventral skin (which stays in contact with the moist substrate), that temperature difference might help the salamanders detect and respond to evaporative demand.

Overall, our study shows that rather than being passive victims of their environment, salamanders actively choose conditions that help them stay hydrated. Their behaviour is not random—it is a targeted response to complex environmental pressures.

One take home from this is that we can’t only measure relative humidity as an environmental predictor for microhabitat selection in salamanders and other ectotherms, but we need to incorporate the biophysical aspects of water loss. Hopefully this isn’t too scary!

Here’s Spotty! – All drought and no rain make salamanders insane.

For more information, please access the study here: https://doi.org/10.1242/jeb.250297 and the Inside JEB write-up here: https://doi.org/10.1242/jeb.250813

Citation

Giacometti, D and Tattersall, GJ. 2025. Behavioural evidence of a humidistat: a temperature-compensating mechanism of hydroregulation in spotted salamanders. Journal of Experimental Biology, 250297 https://doi.org/10.1242/jeb.250297

Blog Author: Danilo Giacometti

Digging into physiology: how salamanders balance energy and water between seasons

/ gtattersall

Ectotherms from highly seasonal habitats often exhibit remarkable physiological plasticity, which allows them to balanceand adjust energy and water budgets in the face of fluctuating climatic conditions. Yet, fossorial (i.e., underground-dwelling) ectotherms are thought to experience attenuated climatic variability underground, raising the question: do fossorial ectotherms also display seasonal adjustments in key physiological functions?

In our recent publication, we investigated how seasonal acclimation (spring vs. autumn) affected energy expenditure and water loss in the spotted salamander. By measuring standard metabolic rates (SMR) and rates of evaporative water loss (EWL), we aimed to disentangle acute (i.e., exposure to test temperatures) from prolonged (i.e., seasonal acclimation) effects.

The effect of temperature over log-transformed rates of carbon dioxide (logV̇CO2) and water vapour production (logV̇H2O) in Ambystoma maculatum between the autumn and spring.

We found that increases in temperature led to increases in both SMR and EWL, demonstrating that fossorial salamanders also experience acute physiological costs when warmed. Salamanders had lower SMR in the spring, which may be beneficial in the context of overwintering emergence and breeding. In contrast, sustaining higher SMR in the autumn may allow salamanders to forage aboveground to replenish energy stores in preparation for the winter. EWL was stable between seasons, suggesting that salamanders may be more reliant on behavioural instead of physiological adjustments to manage water loss throughout the year. Together, our findings challenge the assumption that fossorial ectotherms are largely insulated from environmental fluctuations by virtue of living underground.

For more detailed information, you can access the full study here: https://doi.org/10.1007/s00442-025-05711-6

Citation

Giacometti, D, and Tattersall, GJ. 2025. Seasonal plasticity in the thermal sensitivity of metabolism but not water loss in a fossorial ectotherm. Oecologia. 207: 67. https://doi.org/10.1007/s00442-025-05711-6

Unearthing energetic mysteries: exploring metabolic rates in fossorial amphibians

/ gtattersall

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).

Case of the shrinking salamanders

/ gtattersall

Congratulations to Patrick Moldowan for our publication in Global Change Biology on “Climate associated decline of body condition in a fossorial salamander”.

Abstract of the study below:

Temperate ectotherms have responded to recent environmental change, likely due to the direct and indirect effects of temperature on key life cycle events. Yet, a substantial number of ectotherms are fossorial, spending the vast majority of their lives in subterranean microhabitats that are assumed to be buffered against environmental change.

Here, we examine whether seasonal climatic conditions influence body condition (a measure of general health and vigor), reproductive output, and breeding phenology in a northern population of fossorial salamander (Spotted Salamander, Ambystoma maculatum). We found that breeding body condition declined over a 12-year monitoring period (2008–2019) with warmer summer and autumn temperatures at least partly responsible for the observed decline in body condition.

Our findings are consistent with the hypothesis that elevated metabolism drives the negative associa- tion between temperature and condition. Population-level reproduction, assessed via egg mass counts, showed high interannual variation and was weakly influenced by autumn temperatures. Salamander breeding phenology was strongly correlated with lake ice melt but showed no long-term temporal trend (1986–2019).

Climatic warming in the region, which has been and is forecasted to be strongest in the summer and autumn, is predicted to lead to a 5%–27% decline in salamander body condition under realistic near-future climate scenarios. Although the subterranean environment offers a thermal buffer, the observed decline in condition and relatively strong effect of summer temperature on body condition suggest that fossorial salamanders are sensitive to the effects of a warming climate.

Given the diversity of fossorial taxa, heightened attention to the vulnerability of subterranean microhabitat refugia and their inhabitants is warranted amid global climatic change.

This study resulted from the PhD research of Patrick Moldowan, working with Dr. Njal Rollinson (U of Toronto) and myself. The research emanated from a long-term monitoring project called BLISS (https://tattersalllab.com/bliss/) that was initiated at various times in the past, with an objective to monitor mole salamanders (Spotted Salamanders, Ambystoma maculatum) in a pristine environment, for potential changes over time in population, phenology, reproductive output, and morphology.

I first met the Bat Lake salamanders in 1993, being introduced to the field site by a generous Dr. James Bogart who trusted me enough to leave me alone for 4 months to conduct research on an NSERC USRA project. I really want to thank Jim for sending me to this place where the field site captured the imagination, was a retreat from the urban life, and a crash course in wildlife ecology.

Here is a link to the paper http://doi.org/10.1111/gcb.15766 or request access from researchgate. 

Citation

Moldowan, PD, Tattersall, GJ, and Rollinson, N. 2021. “Climate associated decline of body condition in a fossorial salamander”. Global Change Biology. http://doi.org/10.1111/gcb.15766 

Acknowledgements

Many thanks to all the folks at the Algonquin Wildlife Research Station for support over the years and to all the Salamanderers who took part in BLISS: DL LeGros, SP Boyle, O Butty, JWD Connoy, D Crawford, EA Francis, G H-Y Gao, N Hrynko, JA Leivesley, DI Mullin, S Paiva, D Ravenhearst, C Rouleau, M Terebiznik, H Vleck, L Warma, SJ Kell and T Wynia. There are so many others who have helped out over the years, and we hope we have acknowledged all their assistance in the paper acknowledgements!