Maternal corticosterone increases embryonic heart rate at elevated temperatures

New paper out in Biology Letters (1)! This study, led by collaborator Dustin Owen, shows that increasing maternal levels of glucocorticoids (CORT) during gestation alters embryonic heart rates. At higher temperatures (>26˚C), embryonic heart rate in offspring of CORT-treated mothers was elevated compared to the heart rate of offspring in eggs laid by control treatment mothers. At lower temperatures, there was no difference in heart rate between embryos from the two groups. This is important and interesting, because lizard embryo development is closely tied to temperature – at temps below 26˚C, embryos are in maintenance mode only – above these temps, embryos start to develop! Increased heart rates at these higher temperatures could mean that embryos born to stressed mothers develop faster and hatch sooner (2), allowing them to escape this vulnerable life history stage in a potentially stressful environment.

Congratulations, Dustin!

Paper available here.

1) Owen, D., Sheriff, M.J., Heppner, J., Gerke, H., Ensminger, D.C., MacLeod, K.J.,Langkilde, T. Maternal corticosterone increases thermal sensitivity of heart rate in lizard embryos. Biology Letters, 15: 20180718.

2) Du W-G, Radder RS, Sun B, Shine R. 2009. Determinants of incubation period: do reptilian embryos hatch after a fixed total number of heart beats? J. Exp. Biol. 212, 1302-1306. (doi:10.1242/jeb.027425)

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Highlights from Hobart!

The main empirical part of my current research project will take me far from my current, chilly homes in Sweden/Vancouver – in fact, far from pretty much anything! I’ll be investigating patterns of maternal stress effects in a social lizard that’s found in the southernmost part of Australia – Tasmania. I took a trip there in October/November of last year to test out some lab protocols, and to set up a similar stress experiment that will run for the next couple of months, and which will give us an idea of what to expect when I return later this year.

Great news for me – Hobart, where the University of Tasmania is based, is an amazing city, and my research collaborators there – Geoff While and associated researchers in the BEER group (Behavioural and Evolutionary Ecology Research) are a fantastic, supportive team and awesome fun to be around. I had a blast learning how to catch Egernia lizards (unlike Sceloporus, which we catch with mini nooses, Egernia are caught by baiting a line with mealworms!), and familiarising myself with the lab set up.

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My lab work aimed to test the efficacy of the “stress” dose regime that worked so well in my previous fence lizard studies. If anything, it seemed to work even better in the smooth-scaled Egernia – so happily, very few tweaks will be needed when I return. As was the case in my previous work, this “stress” regime mimics the short-term spike in hormones that naturally occur when a lizard, or really any species, gets a fright – for example, as a result of a predator encounter. I’m very happy that this protocol works here too, because it means no injections (as would be associated with a hormone implant), and no pain!

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After an acclimatisation period in the lab, my preggo lizard ladies were transferred to outdoor enclosures to soak up that Australian sun and gestate in as natural conditions as possible. They’ll continue in this experiment until they give birth, at which point they’ll come back indoors with their offspring, and we’ll measure morphological and behavioural traits.

I had a fantastic time in Hobart, and am so looking forward to returning later this year!

P.S. Follow me on Twitter and check out the field season hashtag #Tazards2018 for more!

P.P.S.

Of course my time in Tassie brought many wonderful wildlife/herpetological encounters – some calmer than others…

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Tree selection is linked to locomotor performance and associated noise production in fence lizards

New paper in Journal of Zoology! The substrates on which animals spend their time can affect how they look, move, and sound. We found fence lizards more frequently on deciduous trees, on which they sprint faster and produce less noise relative to coniferous trees, which may affect their ability to catch prey or evade detection by predators. Noisiness and performance have received less attention in the context of substrate preferences than visual camouflage, but our results suggest they may also be important in determining the surfaces on which lizards prefer to be. (Check out the paper: Tree selection is linked to locomotor performance and associated noise production in a lizard.)

In the summer of 2016 I began a large-scale experiment investigating the effects of maternal stress on offspring characteristics in the eastern fence lizard, Sceloporus undulatus. My primary mission for the first part of that summer was simple: catch as many lizards as possible in the longleaf pine forests of southern Alabama. When you spend most of your day pursuing a small prey species, you quickly start to think like a predator. In what areas are you most likely to find them? At what times? On what surfaces? The cumulative years of experience of my fieldwork team (colleagues from the Langkilde lab) suggested that fence lizards were mostly found where there was a mix of hardwood deciduous trees and pines, and that they preferred the deciduous trees, like oaks and hickory, to the famous pines of the region. The longer I spent looking for lizards, the more I noticed that this observation held true. I didn’t put much thought into why until one day when I followed a lizard into a small stand of pine trees. I momentarily lost sight of the lizard, until I heard a loud scrabbling from a few metres away – there was the lizard, scuttling up a pine tree on the smooth, dry flakes of its bark. If the noise of the lizard’s claws moving on the pine bark alerted me so easily to its presence, I thought, perhaps the same was true for its real predators! Also – perhaps that noise was indication that this type of bark, with fewer crenulations and ridges on which to grip, was more difficult for the lizard to run on. Together, could these provide a reason that fence lizards seem to avoid pine trees despite their prevalence?

My colleagues and I decided to test this in the field. First, we quantified whether our anecdotal hunch that lizards prefer deciduous trees to conifers (pines) was really true by conducting thorough searches for fence lizards throughout our field sites, and noting the tree type we found them on, as well as the availability of trees in that area. This allowed us to test whether lizards were “choosing” deciduous trees in areas where they could also choose pines, as opposed to just being found in areas with only deciduous trees. As we expected, we found that even when availability of coniferous:deciduous trees was more or less 1:1, lizards were overwhelmingly found on deciduous trees, not pines.

Next, we tested our hypotheses that tree type changes how noisy lizards are when they move, and how quickly they are able to move. We did this by releasing wild lizards on either coniferous or deciduous trees, and then recording them as we stimulated them to run upwards on the tree by gently tickling their back legs. We then analysed these recordings and found, as we predicted, that the noise of lizards running (the sound level they produced when running compared to the background noise when they were still) was significantly higher when they were running on the smooth, flakier bark of coniferous trees. We also found that the sprint speed they attained on coniferous trees was lower than on deciduous trees. In other words: they are noisy and slow on pine bark compared to the bark of trees like oaks and hickorys.

Studies investigating where animals spend their time (either in terms of broader habitat preference, or more localised use of substrates) has often focused on coloration, and the camouflage it may or may not afford. Our study shows that other aspects of camouflage, such as acoustic camouflage, may also be important. It’s also important to consider how substrate affects performance, like sprinting speed: once you’re spotted by a predator, the speed at which you’re able to escape may be just as important as trying to remain hidden in the first place.

This was one of my favourite studies to be involved in, for a number of reasons! First, I love that we were able to find ways to test hypotheses based on a very simple natural history observation. Understanding the natural history of an organism is crucial for developing new ideas – and the “why does this happen?” questions are the bedrock of behavioural ecology. Second, this study was an opportunity to bring together friends and start new collaborations! Langkilde lab alum Nicole Freidenfelds brought her great knowledge and understanding of herpetofauna and natural history; local friends in Alabama helped me to identify tree species; I knew of Gavin’s prowess in acoustic analysis through Twitter, and asked him to help with this aspect of the project; and Tracy and I had a blast exploring these ideas with them!

Survival and reproductive costs of repeated acute glucocorticoid elevations – new paper in GCE

Click the below to go straight to the paper:Screen Shot 2018-10-25 at 16.27.46.png

During a visit to Harrisburg Academy’s 1st-4th graders, I asked the students if they had ever experienced “stress”. A dozen hands shot up. “I’m stressed all the time!” said one 1st grader. “When my sister comes in my room when I don’t want her to, that stresses me out,” said another. Although a 7 year old’s understanding of “stress” may differ to mine – or anyone else’s! – it was clear from this very switched-on young focus group that the concept of “stress” is ubiquitous.

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“Stress” as a response to encounters we don’t want or things we don’t like may be an anthropomorphic term, but in its broadest sense it is a concept that we can extend to non-human vertebrates too. When we experience a “stressor”, from speaking in public to a near-miss accident as we cross the road, our brain triggers a hormone response resulting in the production of a glucocorticoid hormone, cortisol. The function of this hormone product is to mobilise the body’s fight or flight response – generating the immediate production of glucose, for example, and suppressing processes that don’t need energy in that moment of danger, such as reproduction and immune function. This same pathway is similarly triggered in most other vertebrates by encounters with ecological stressors, such as coming across a predator while foraging, or being in an aggressive altercation with a fellow group member, though the hormone produced may differ (rodents and primates generally also produce cortisol; other vertebrates may produce corticosterone).

Screen Shot 2018-10-26 at 14.38.34.pngSo, if an organism in the wild is stressed as regularly as a first grader, we can assume that they are experiencing regular spikes of glucocorticoid hormones. While these elevations facilitate the response necessary for escape from predators and moving out of danger and are therefore likely to be selected for by evolution, studies have shown that elevated glucocorticoid levels can also have negative effects – for example, elevated glucocorticoid levels are associated with reduced immune function (McCormick et al. 2014), and lowered body condition (De Vos et al. 1995; Klein, 2015). However, few studies have investigated whether regular short-term increases in glucocorticoids (i.e. as would be expected if an animal was frightened by a predator cue, or got into a fight every day) lead to any reductions in “fitness” – an animal’s ability to pass on its genes through surviving to be able to reproduce.

We set out to test this in the eastern fence lizard which, as I’ve written about before, is likely to be frequently “stressed” given the frequency of its interactions with predators, including invasive fire ants across the lower half of its range. We were interested in the effects of frequently elevated glucocorticoids on two parameters: adult survival, and their reproductive success, which we measured as the proportion of the eggs they laid that actually hatched live babies.

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Fence lizard receiving a dose of glucocorticoid hormone

To do this, we brought gravid female lizards from the field in Alabama into the lab at Penn State, and treated them with a low-dose glucocorticoid hormone between capture and laying to mimic a daily short-term spike such as they would experience if they were encountering a predator in the wild. We then monitored their survival over the next weeks, and the success of the eggs that they laid after treatment.

 

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Newly hatched eastern fence lizard

We found that frequent, low-level elevations of glucocorticoid hormone (corticosterone) led to reduced female survival, AND reduced egg hatching success (fewer eggs successfully hatched of those that were laid). Interestingly, we also found that the effect of corticosterone elevations were greater in 2016 compared to 2015. Two years do not a pattern make – but one potential cause for this greater effect could be that the winter between 2015 and 2016 was significantly warmer than that between 2014 and 2015 – I’ve written more about why warmer winters could be bad for reptiles here.

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So, why does this matter? Well, going back to our “stressed” 1st graders for a moment – if low level stress is really so ubiquitous, then our results suggest that we may be underestimating its effects on individuals and populations. For example, we have a good understanding of the effects of direct predation on animal populations – predators kill prey animals, resulting in fewer prey animals. But perhaps the “stress” of encountering predators could also lead to reduced survival and reproduction, even in instances where prey animals escape and live to fight (or flight) another day. As animals are exposed to human-induced environmental change, they will face increasing and novel stressors, such as invasive species and climatic warming – considering the effects of the physiological outcomes of these stressors is therefore useful going forward in understanding how they will actually affect individuals and communities.

Maternal stress effects on offspring in eastern fence lizards – new paper in JAE

The consequences of exposure to environmental stressors in animals is of increasing interest given the changing world we live in. Our recent paper published in the Journal of Animal Ecology explores the consequences of stress-relevant hormones for mothers and their offspring. In other words: if a mother is stressed, does this influence her offspring? And how?

This paper is part of a large-scale study that I was involved in – this part of that project was led by PhD student David Ensminger. In this study, we found that if levels of the hormone corticosterone (which increases in response to stress) were frequently elevated during gestation, this changed the behaviour of the mother, the characteristics of her eggs, and the physiology and behaviour of her offspring, even though they themselves were never exposed to a stressor. This goes a long way to helping us understand the long-term and cross-generational effects of stress-exposure.

Read more in David’s new paper, and featured blogpost on the Journal of Animal Ecology blog!Ensminger Maternal Stress Graphical  Abstract V2.jpg

 

Update – some art!

There will soon be a bunch of freshly-accepted papers to write about… but in the meantime, I’ve been maintaining my work-life balance by indulging one of my oldest passions – art! My Mum was an art teacher before she retired, and working on creative projects has been something I’ve done to relax for as long as I can remember.

Nowadays, there’s nothing I love more than combining my love for art with my love for science and the natural world!

I designed and made these lino prints with my friend Beth Reinke in mind. Beth studies painted turtles (Chrysemys picta) at her long-term field site in Wisconsin, where she’s collected data on morphology and colour from 1000+ turtles! They’re the most widespread native turtle in North America – keep an eye out for these beautiful reptiles next time you’re near some slow-moving fresh water.

Lino printing (a descendent of traditional wood block printing that became popular through artists like Matisse and Picasso in the early 1900s) is my current favourite way to relax and be creative in my downtime. I started with a basic turtle-shaped stamp, and then carved down to provide the layers of gold and black that you see – what’s cool about this method (and what makes each print unique!) is that by adding detail to the lino stamp, you are also destroying it – so, these can’t be recreated. ART, PEOPLE 😄

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I’m working on some more natural history-based ideas, and taking lots of inspiration from the study species of my friends. Got any ideas? What do you do to relax in your downtime? Let me know!