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.
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)
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.
“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).
So, 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.
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.
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.
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.
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.
The direct effects that predators have on prey are obvious – predators kill and consume the prey they catch, and that prey individual’s chances to reproduce and pass on its genes are then over. Through these direct effects, predators have substantial effects on prey species demography and evolution. But for every prey animal a predator catches and kills, there are many that escape and live – perhaps they managed to outrun the predator, or simply hid successfully and managed to evade detection. What might be the long-term effects of these highly stressful encounters with predators? And could the stress of predator encounters provide an alternate, indirect route to prey mortality?
These were questions I set out to answer in my newly published article, “Fear and lethality in snowshoe hares: the deadly effects of non-consumptive predation risk”. This study is a good example of finding interesting results when you look at old data in a new way: Michael collected these data as part of his PhD thesis, in an experiment designed to test maternal predator exposure effects on reproductive output in snowshoe hares. As part of this experiment, which he conducted under the supervision of our co-authors Rudy Boonstra and Charley Krebs, captured pregnant wild snowshoe hares were exposed every other day to a predator that was not able to catch them (a trained dog), a treatment which stopped as soon as the hares gave birth. When I joined Michael’s lab as a postdoc to work on a project investigating maternal stress effects on offspring in lizards, we started to think about potential effects of this kind of predator exposure on adult mortality through the likely physiological stress it causes, and together revisited this data and developed new questions to test using it.
In this article we show that simply being exposed to a predator every other day resulted in death for six of the twenty experimental female hares, while hares in the control group (that were not exposed to a predator) suffered no mortalities at all. Even more interesting, when the surviving fourteen females that were exposed to the dog gave birth, their offspring were less likely to survive until weaning (when they stop suckling from their mother at around 4 weeks of age) than the offspring of females in the control group.
To sum up, predator exposure of pregnant adult females reduced their own survival, but also the survival of their offspring, which were never themselves exposed to predators. So, encounters with predators affected survival even when the predator could not kill the prey, and these effects passed on to the next generation too. The effect on group size was striking: the control group all reproduced successfully, and grew from 11 adults to a final group size of 30 adults and offspring. Meanwhile, the predator-exposed group, which was almost twice as large to begin with, dwindled from 20 adult females, to a final group size of 16 adults and offspring.
Our results suggest that just the perception of predation risk can lead to increased mortality – and that while the direct effects of predation are obvious, we should also be thinking about the less obvious indirect effects that predators can have on their prey.