The brilliant multimedia team from the Eberly College of Science at Penn State came to visit our lab a few weeks ago, and took some wonderful pictures. Here’s David and I taking some limb measurements from an adult female. Limb length has been shown to be a trait that is altered by exposure to fire ants over multiple generations – lizards that come from areas that have a relatively long history of fire ant invasion (like our sites in Alabama) have longer hind limbs, possibly to facilitate the twitching behaviour that helps to flick ants off (paper here)! Measuring limb length is therefore an important part of our data collection repertoire.
All photos were taken by Carley LaVelle, Eberly College of Science.
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.
If you’ve missed me, it’s because I’ve been superbly busy with this summer’s field season in Alabama! It’s been a boom season: we caught females in April/May, they laid fast and furious at Penn State over June, and since the beginning of July I’ve been back at the Solon Dixon Forestry Education Center hatching out the babies, and putting them into experimental enclosures. I will write a full report at the end of the season (currently coming to a close), but for now, a reminder that you can read more regular updates using the #ALlizards2017 hashtag or via my profile on Twitter.
In case you haven’t noticed, it’s been an unusually mild winter in most parts of the United States. How mild? Well, for the first time in 146 years, Chicago had no snow in January and February (38 years longer than they went without a World Series win, not that anyone was counting) – and in Miami, temperatures never once dropped below 50˚F, a first in recorded history (and they’ve been keeping records there for 121 years). Although the north west saw record cold, far more weather stations (8% in fact) recorded the HOTTEST winter on record.
To put this in perspective, the record for “warmest winter” in the Lower 48 states was held by – you guessed it, the winter immediately before this one (2015/16). And this is part of an upward trend in winter temperatures, not just a 2-year fluke:
Looking at the top graphic, the south east region of the US (where I conduct my research on eastern fence lizards) was particularly warm this winter. This area is an important hotspot for reptile and amphibian diversity, and as I’ve been working on reptiles in particular, these interesting (and worrying) trends have had me thinking about how warm winters might affect reptiles.
Reptiles are ectotherms, meaning they depend on external sources of body heat, and have limited ability to physiologically control their own body temperatures. Maintaining an optimal body temperature is therefore very environmentally-dependent in these species. This is thought to make them particularly vulnerable to the effects of climate change.
Elegant work done by Barry Sinervo and colleagues (published in Science) suggests that increased global temperatures will lead to a reduction in reptilian diversity because as temperatures increase, reptiles are limited by their upper temperature limits. Every reptile (and animal generally) has a “critical thermal maximum/minimum” – these are the upper and lower temperatures beyond which physiological processes will cease and they will die. So, if it’s hotter, reptiles can spend less time being active and foraging, and have to spend more time resting in the shade to avoid reaching critical thermal max. This will have effects on their body condition, ability to reproduce, and ultimately, on population growth, leading to increased likelihood of extinction.
So it’s pretty obvious how warmer SUMMERS could impact reptiles, by pushing them more frequently to their critical thermal maximum, and forcing them to adjust their behaviours to avoid this. But, what about warmer WINTERS?
My hunch was that warmer winters probably interfere with regular over-wintering behaviours in reptiles. But when I started to dig into this topic I found that what a “regular” over-wintering behaviour is in a reptile is highly variable, even within species. Some species, like rattlesnakes (see pic), go into hibernation much like a bear or a small mammal – though when they do this, and for how long, is highly dependent on their latitude. To generalise, reptiles at least “power down” for the winter months when food is relatively scarce: they lower their metabolism to conserve energy, and may burrow underground or move into crevices, which is why they’re usually hard to spot during this period.
I work on the eastern fence lizard, Sceloporus undulatus, which is a widely-distributed species, occuring from Mississippi to southern Pennsylvania. We don’t know much about over-wintering behaviour, but we do know that they come out when it’s warm, even if that’s in the middle of winter:
Although they are likely to display variation in over-wintering behaviour given their huge latitudinal range, seeing them out and about this early in central Arkansas is definitely unusual.
But – should we be worried to see little Scelops out in late January or February? Are warm days at this time of year going to do them any harm? Temperature increases during the winter are surely likely to fall well between critical thermal min & max, and if anything, should result in temperatures that are closer to each species optimum (the smaller range of temperatures that ectotherms will seek to achieve, at which physiological processes, such as digestion, are optimised). So, do warmer winters matter?
The short answer is yes, it probably does, and it’s probably not great news for reptiles like the fence lizard.
There are a couple of reasons why. First, becoming active in winter requires upregulation of the animal’s metabolic rate, which has been lowered for the winter period. Our metabolism, amongst other things, is the suite of processes that convert food/fuel to usable energy to allow us to be active. Metabolic rate is highly sensitive to temperature in reptiles, so as it gets warmer, they start burning through their energy stores. Remember, there’s a reason that reptiles go into a state of reduced metabolism during winter: there’s less food around! Especially for those that rely on hibernating mammals, but also those that need to eat lots of insects that are less plentiful when it’s cooler, like lizards. So, becoming active and increasing your metabolism is probably a bad thing when it’s going to burn up your stored energy, and there’s limited potential for you to recoup it by finding lots of food.
A number of studies have found that milder over-wintering temperatures result in decreased body condition come Spring-time, and higher levels of physiological stress, as a result of this increase in metabolism. For example, painted turtles that experience just a 5˚C increase in winter temperatures use almost twice as much energy (Muir et al. 2013); and aspic vipers had reduced Spring body condition after being kept at 14˚C instead of 6˚C (Brischoux et al. 2016).
There’s another reason that “milder” temperatures are likely to be bad news for reptiles (and other animals too): they may be high enough to promote activity, but still low enough to result in impaired digestion, performance etc. Remember the optimal range of temperatures that maximise physiological performance? For Sceloporus lizards, that range centres around 30˚C. So, they have to reach this temperature, or close to it, to be able to digest food properly. In other words – mild temperatures of, say, 16-22˚C may be enough to fire up the engine, but not get it working efficiently, which can lead to problems like this:
@kirstyjean@AlongsideWild Winter heat spikes cause issues for alligators- resume feeding, gets cold again, temps 2 low to digest food->die
As well as digestion, other aspects of physiological “performance” may suffer at low-mild temperatures, such as sprint speed. As you can see in this figure, endurance (minutes on a treadmill) and especially sprint speed (centimetres moved per second) in Sceloporus lizards (both things that are likely to be important in escaping a predator, or trying to catch a food item) are maximised above 26˚C, and reduced below 20˚C.
So, to sum up my non-expert forays into thermal biology of reptiles and answer my initial question: yes, increased temperatures during the winter period most likely do matter. To summarise:
mild temperatures are likely to bring reptiles out of torpor
this necessitates/is accompanied by an increase in metabolic rate, which uses stored energy
furthermore, food availability is likely to be lower at this time
and their digestion/other physiological processes are impaired at these temperatures
with the result that they are in lower body condition when the Spring finally rolls around.I’ve really enjoyed diving into the thermal ecology literature out of interest to know how the warm winter we’ve been experiencing will affect my study species. But this is outside my realm of expertise! So, if you’re interested in this topic, here are some great Twitter accounts to follow for people who know far more about this than me:
Muir et al. 2013. Journal of Thermal Biology. Energy use and management of energy reserves in hatchling turtles (Chrysemys picta) exposed to variable winter conditions. http://www.sciencedirect.com/science/article/pii/S0306456513000557