Thermal adaptations best explain biogeographic rules in Australian shorebirds

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

Case of the shrinking salamanders

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!

Fish get the “rotten egg gas” chills.

At long last, resulting from herculean efforts of a number of former students, our paper is published. Out today in Royal Society Open Science, our paper entitled: “Hydrogen sulfide exposure reduces thermal set point in zebrafish” represents the efforts of two honours students (JC Shaw and CD Dobell) and the writing and analytical skills of a great PDF and colleague (DA Skandalis).

Here is a link to the study and full citation:

Skandalis DA, Dobell CD, Shaw JC, Tattersall GJ. 2020 Hydrogen sulfide exposure reduces thermal set point in zebrafish. R. Soc. Open Sci. 7: 200416.

https://royalsocietypublishing.org/doi/10.1098/rsos.200416

We tested whether dissolved H2S in the water will alter thermal preference. Previously, work in mice has suggested that mice could be induced to adopt a “hibernation-like” state, although there was some doubt (in the literature) as to whether H2S signalled a change in thermoregulatory state or simply acted as a metabolic inhibitor. By testing this in zebrafish, we could test formally whether they prefer cooler temperatures with H2S exposure, and they did. Not only did they choose to cool down, but they continued to make thermoregulatory decisions, swimming back and forth between cool and warmer water, suggesting they are still making thermoregulatory decisions and not simply caught in the cold water. So…yeah, complicated. H2S might induce a behavioural anapyrexia (a lowered thermal set-point). We discuss the potential environmental and neurophysiological context in the paper for those interested. The rotten egg reference is to the smell of H2S gas.

To conduct this study, we used a system built by Brock University’s Technical Services and employed in our research lab that allows us to track fish in a two chamber thermal shuttle box:

Schematic of the Shuttle Box System (see Figure S1 in the paper).

This setup allows us to heat and cool a tank and track the fish’s choices over time. Here is a thermal image depicting an earlier version of the shuttle box (correcting the spill over of warm-water in the centre can be corrected using baffles and a circular chamber system, but I haven’t taken a new picture with the thermal camera during the pandemic lockdown):

There was some considerable interest in developing H2S as a therapeutic to put mammals and/or tissues/organs into a suspended state. It is intriguing that animals like zebrafish that can behaviourally regulate body temperature continue to do so under this exposure. Anaprexic stategies are commonly seen in ectotherms and perhaps by hijacking an innate signalling system, H2S evokes this response.

Bridgeman now the Master

When he left the lab to write up his thesis, he was but the learner…now, HE is the Master.

Congratulations, Justin Bridgeman for a successful defence! Justin’s thesis earlier today was on “Behavioural thermoregulation and escape behaviour in the round goby”.

Thanks to the selfless efforts of the committee members (Dr. Gaynor Spencer, Dr. Liette Vasseur, and Dr. Patricia Wright), external examiner (Dr. Dennis Higgs, U Windsor), and committee chair (Dr. Cheryl McCormick).

Thank to all the lab mates for supporting Justin and welcoming him back for his brief visit.

All the best in the future Justin! We look forward to the manuscripts…and for a place to crash when we visit you in Halifax! 😉

Shape Shifting Birds – PhD Opportunity

Please consider applying for this PhD Opportunity in Australia to work with my colleague, Dr Matthew Symonds on Shape-Shifting Birds.

This research forms part of an ARC Discovery Project (PI: Symonds; CI: Klassen & Tattersall) whose goal is to determine whether changes in body shape are an evolutionary response to climate change. Endothermic animals (such as birds) have a range of adaptations for dealing with the temperatures they experience. One such adaptation is body shape: birds in warmer climates tend to have large extremities (bills and legs), increasing their surface area and enabling loss of excess heat. Adaptations to climate (and hence climate change) can occur quickly, and there is evidence of significant increases in bird extremities in recent years – a novel potential consequence of climate change. Whether this represents an evolutionary response to climate change is unknown, nor do we know what characteristics make specific bird species liable to respond to climate change in this way, or what the likely consequences of such responses are.

The student will undertake an extensive comparative analysis of Australian birds, designed to identify a) which bird species are showing changes in body shape (bill and leg morphology); b) what ecological (life- history, behaviour, habitat) factors determine such responses; c) whether these changes relate to fitness/survival and d) whether such changes are linked to long-term populations trends in Australian birds.

The project will involve extensive work in Australian museum collections, measuring bird morphology using traditional and modern (3D-scanning) techniques. There is also a strong analytical component, involving use of long-term field data on Australian bird species as well as phylogenetic comparative analysis of large-scale ecological data sets for Australian birds.

Please send an application letter, together with your CV, to Dr Matthew Symonds (matthew.symonds@deakin.edu.au).

Further information can be found in our review papers:

Symonds, MRE and Tattersall, GJ. 2010. Geographical variation in bill size across bird species provides evidence for Allen’s rule.American Naturalist. 176: 188-197.

Tattersall, GJ, Arnaout, B, and Symonds, MRE.  2017.  The evolution of the avian bill as a thermoregulatory organ. Biological Reviews 92: 1630-1656. doi:10.1111/brv.12299