Alliance of ecologists and physiologists to study the effect of size and food quantity on muscle metabolism in the European sardine Sardina pilchardus

This blog post is provided by Elisa Thoral, Claire Saraux and Loïc Teulier and tells the #StoryBehindThePaper for the paper ‘Changes in foraging mode caused by a decline in prey size have major bioenergetic consequences for a small pelagic fish’, which was recently published in the Journal of Animal Ecology. Elisa Thoral (PhD student) and Loïc Teulier (her thesis co-director), are from the University of Lyon in France. Claire Saraux is a Researcher from the CNRS in France.

The effect of global warming on individual body size has been a topic of high interest in marine ecology recently, especially with the now well documented shrinking of fish. A decrease in fish size of key species can have strong deleterious consequences both in terms of ecosystem functioning and economy and resource management. The European sardine Sardina pilchardus has been a source of worry in the western Mediterranean Sea over the past 10 years: its size and body condition have been declining, and the oldest individuals have disappeared from the Gulf of Lions. Individual hypotheses including the possible effects of migration, overfishing, epizootic diseases, or increased predation have all been refuted in explaining this phenomenon. Scientists are now taking a new approach, looking at what sardines eat, to test if “bottom up” effects could be responsible for the decline in sardine condition.

It is by combining their expertise across fields, that a physiologist, Loïc Teulier, and a quantitative ecologist, Claire Saraux, at the time Senior Lecturer at the University of Lyon (UMR LEHNA) and Researcher at Ifremer (UMR MARBEC), Sète, respectively, tackled this question. Both researchers belonged to structures with a common interest: water and the species which live in it, but with very different perspectives. While one measured the metabolism of fish from the cell to the whole organism, the other had a vision that extends from the individual to the population and ecosystem. To bridge the gap between these two scales, they collaborated through the supervision of Elisa Thoral, a Masters student. Loïc and Elisa went to Palavas-Les-Flots, on the shores of the Mediterranean Sea, in February 2017 to join Claire Saraux and her colleagues from the Ifremer experimental station.

Accompanied by their high-precision Oxygraphs Oroboros®, they first adapted their usual protocols to measure mitochondrial respiration in Gilthead Sea bream and European sardine muscles. Strong from this first success, an idea was born in the scientists’ minds. What if the physiologists from Lyon, took part in the large-scale study that started a few months ago to study the mechanisms through which food size and quantity might affect sardines? While sardine prey size had been suggested to decrease in the wild based on stomach contents, the mechanisms underlying the effects of prey size on sardine condition and energetics remained entirely new questions. Sardines are known to use two different feeding modes according to the size of their prey: they will directly capture the largest prey, but use filtration for the smallest prey. Could this be the reason for the important demographic changes observed in the Gulf of Lions’ sardines? Their hypothesis was that filtering small prey would result in higher energy costs than hunting large prey, as it would require a longer swimming time to assimilate the same amount of energy. Thanks to resourceful zootechnicians, the Ifremer team was able to capture wild sardines, bring them back to the experimental station and maintain them in captivity.

In June 2017, the Lyon team of physiologists and ecophysiologists came back to Palavas-Les-Flots for a few weeks, surrounded by their ecologist colleagues from Ifremer, to measure mitochondrial respiration and energy production within the muscle of sardines fed for 7 months under four different treatments (two different food quantities and two different food sizes). This alliance made it possible to have a robust analysis of the data, but also to look at the relationship between purely physiological measurements, such as basal mitochondrial respiration, and more integrative measures more often used by ecologists such as body condition index.

The results were convincing: while caloric restriction appeared to have effects at the individual level, with marked effects on body condition in particular, particle size had consequences at both individual and mitochondrial levels. Indeed, a smaller particle size led to a decrease in body condition, regardless of the amount of food delivered, and also led to a decrease in mitochondrial fluxes, but with an improved coupling between oxygen consumption and energy production in the form of ATP. Yet, this is when things got complicated. How to reconcile the larger perspective from the ecologists with the detailed mechanistic approach of the physiologists in a paper? After months of writing, proofreading, corrections and animated discussions, the article saw the light of day, to the great pleasure of all co-authors, proving that it was possible to understand each other, despite very different fields of study, and to learn from each other to produce an eco-physiology paper. By linking both ecological questions and rather physiological answers, this paper showed that the filtration of small particles represents an energetic challenge compared to the capture of larger particles, which may support the bottom-up effect hypothesis that could be linked to climate changes consequences.

Read the paper

Read the full paper here: Thoral, E., Queiros, Q., Roussel, D., Dutto, G., Gasset, E., McKenzie, D. J., Romestaing, C., Fromentin, J.-M., Saraux, C., & Teulier, L. (2021). Changes in foraging mode caused by a decline in prey size have major bioenergetic consequences for a small pelagic fish Journal of Animal Ecology, 00, 1– 13.

A Colourful Distribution

Skinks come in a variety of colours and patterns. But why and how are these colour polymorphisms maintained? Genevieve Matthews, a PhD student at Monash University, has been studying skinks for four years. Her research examines the maintenance of genetic variation in the form of colour pattern polymorphism in the delicate skink, and the costs associated with sexual conflict. Here, Genevieve summarises her recent publication in the Journal of Animal Ecology that studied avian predation intensity as a driver of colour polymorphism.

Lizards are one of the most diverse groups across the animal kingdom – and nowhere more diverse than in Australia. There are more than 6,500 species of lizards currently recognised across the world and over 800 native to Australia. Adapted to an incredible range of habitats and ecosystems from deserts to rainforests, lizards are a useful group to study, and more than half of those in Australia are skinks (Scincidae).


A plain-back skink (Photo: Genevieve Matthews)

The Liopholis skink genus contains 11 species, including both alpine and desert-adapted skinks. Across various habitats, distributions and levels of conservation interest, the Liopholis species belong to a colourful genus. Some species sport leopard-pattern spots on their sides, some have a patterned back, some with both, some with a general all-over pattern and some with no pattern at all. Around half of the Liopholis species have multiple wardrobes; more than one of these colour pattern types, or morphs, is represented within a single species. In White’s skink, Liopholis whitii, three different morphs can be found: patterned sides and back, plain back with patterned sides, and patternless.


A patterned skink (Photo: Genevieve Matthews)

Colour pattern polymorphisms like this are not uncommon in general, nor in reptiles, but it’s the distribution of colour morphs in White’s skink that makes it particularly interesting. Along eastern Australia, the colour morphs of White’s skink change in frequency according to latitude. The rare patternless morph, strangely, is present in one small cluster at a low to mid-range latitude of the total species distribution. On the other hand, northern populations consist of around 80% patterned variants, which increases gradually southward until populations in Tasmania are composed of only patterned individuals. But why?

Polymorphisms can represent alternate strategies for a species to deal with a selection pressure. That is, different morphs may go about dealing with the same environment in two different ways, both of which are at least partially or temporarily successful, even though it’s usually a difficult business to find one successful strategy. This depends entirely on the current available genetic variation and the state of the environment and its selection pressures at the time.

Without considering genetic inheritance, we expect that the adaptive significance of the White’s skink morphs is highly relevant when explaining their latitudinal distribution. In other words, each colour pattern morph should provide some benefit to the individual based on its latitude. Selection differs from population to population, so morph frequency variation between populations is not unexpected. But such a strong spatial gradient begs a more involved explanation.

Among ectotherms, we naturally predict that climate-related temperature should interact with a species’ thermal limits to produce a large effect on its distribution. We hypothesised that Liopholis whitii morphs might have different thermal physiologies that explain why they are distributed in such a smooth latitudinal cline. Though hotly contested, there is evidence to suggest that melanistic ectotherms have faster heating rates than lighter-coloured ones. The dorsal patterned Liopholis whitii have dark spots and stripes that may allow them to maximise the intake of heat in cooler southern populations, relative to the plain-back populated northern locations.

The stunning Girraween National Park in south-east Queensland harbours both plain-back and patterned skinks, perfect for collecting and testing the thermal physiology of both. Over six weeks, I and several field assistants caught some of each morph, representing both males and females. As we caught them, we assessed their microhabitat for its thermal properties and its structure, as well as its reflectance composition, or background colours. Skinks that were collected underwent tests for their sprint speed, heating and cooling rate and their own colour properties were measured with a spectrometer, before being released back to their burrows.


Morphology measurements taken in the field (Photo: Genevieve Matthews)

Despite the beautiful surrounds, and the pleasure of handling such a gorgeous species, field collection wasn’t without its downsides. One notable catching attempt ended with a juvenile brown snake in my armpit. Data collection ultimately successful without mishap, what we found was surprising: there was very little difference between the thermal physiology of patterned and plain-back morphs, and only subtle differences in their use of microhabitat. More interesting, however, was the choice of background colour among morphs. By using models of bird visual systems, we could determine how well avian predators could distinguish each morph against the microhabitat it selected. In general, both morphs were discriminable to birds against their background, but to differing degrees. For the most common bird eye type and illumination, plain-back morphs were more conspicuous than patterned morphs.

This prompted a further question: how was predation intensity related to morph frequency across latitude? I collected information from the literature about all potential predators of White’s skink, and how likely they might be to consume the species, to produce a potential predation intensity score across latitude. I further included information about temperature and rainfall and constructed a series of models to see which factors best explained the distribution of colour pattern morphs. The best model suggested that bird predation intensity alone explained the gradient in morph frequency. Paradoxically, the morph most conspicuous to birds (plain-back) occurs where bird predation is highest.


A White’s skink peeking out of its burrow in Girraween National Park (Photo: Genevieve Matthews)

By looking solely at a single population along this latitudinal cline, we only have one snapshot in space and time with which to compare the broad scale patterns of predation intensity. It is very likely that conspicuousness and background matching interact with behaviour, gene flow, more complex thermal physiology, or other forces of selection to produce the observed patterns. Nonetheless, predation plays a key role in the smooth frequency cline of this species, contrary to our expectations. By combining local and distribution-wide data on a single polymorphic species, we know that colour pattern morphs are important in predator avoidance, however complex the relationship may be across and within populations.

More Info:

Matthews, G., Goulet, C. T., Delhey, K., Atkins, Z. S., While, G. M., Gardner, M. G., & Chapple, D. G. (2018). Avian predation intensity as a driver of clinal variation in colour morph frequency. Journal of Animal Ecology87(6), 1667-1684.

Ecophysiological feedbacks under climate change

Variability in heat tolerance among populations modifies the climate-driven periods of diurnal activity expected for ectotherm species. This phenomenon is illustrated for Iberian lizards in a paper recently published in the Journal of Animal Ecology. Lead author Dr Salvador Herrando-Pérez is a generalist ecologist with expertise in community ecology, demography, ecophysiology and palaeoecology, and currently undertaking his second postdoc. Here, he explains the approach used in this paper for assessing to what extent such plasticity shapes metrics of climate impact.

Iberia is a wonderful natural laboratory, with a complex blend of flat/hilly, open/woody and coastal/continental terrain, swept by climatic gradients of temperature and moisture. In 2013, I launched a BES-supported project about the thermal ecology of Iberian lizards and managed to drive over much of the Iberian Peninsula in fairly little time. Not being a reptile specialist myself, I was confronted by the consistent observation that lizard populations occupied very different habitats across the known distribution of each of the ~ 25 known Iberian species belonging to the family Lacertidae.

For instance, the common wall lizard (Podarcis muralis) likes water, rocks and mountains, but you can find this pencil-long reptile at the top of a summit, along the slopes or riversides of shallow and deep ravines, on little stones barely surfacing above peatland grasslands, or among the bricks of buildings. These animals must experience different local climates conditional on where they live, and adapt their thermal physiology accordingly.

Fig 1 Common Wall Lizard - Credit Salvador Herrando-Perez

Common wall lizard (Podarcis muralis, male) and three localities where the species is abundant in Spain, left to right including Valdesquí/Madrid (Central System), Peñagolosa/Castellón (Iberian System) and El Portalet/Huesca (The Pyrenees). (Photo: Salvador Herrando-Pérez)

Having then started a postdoc in Miguel Araújo’s lab — a world-class site for global change ecology and ‘big’ biodiversity patterns — I reviewed a sizeable body of literature looking into large-scale gradients of thermal tolerance. Most of those papers had collated (mostly) one estimate of tolerance from each of tens to thousands of species, then mapped them against regional and global metrics of climate change through sophisticated mathematical frameworks. But these studies rarely accounted for population-level thermal tolerance.

At the time and in parallel with my project, the lab had just gathered a team of ecologists to do, to our knowledge, one of the largest one-off surveys of thermal tolerances in a group of closely related vertebrate ectotherms from a single biogeographic region in just two consecutive spring-summer seasons. This massive effort finally garnered upper and lower thermal limits (the highest and coldest temperatures an organism can withstand prior to death, also known as CTmax and CTmin, respectively) of 59 populations from 15 different species of lizards. We know that thermal traits are spatially and temporarily plastic — so much so for ectotherms (lizards in particular), whose body temperature relies heavily on air temperatures. So, we had the ideal data to assess to what extent such plasticity could shape our metrics of climate impact.

Fig 2 Fieldwork - Credit Gomes and Gomez-Lobo

Field work at two of the Spanish sampling localities*: Doñana National Park/Huelva (left) and Plataforma/Ávila (right). Admittedly, to an external observer, the view of an ecologist aiming at noosing a lizard must look weird, imagine a guy avidly staring at an uninteresting point in a tai chi posture while slowly manoeuvring a fishing rod in dry terrain. * Pics show Camila Monasterio and Wouter Beukema (left) and Salvador Herrando-Pérez. Our paper is also co-authored by project leader Miguel Araújo, and (by alphabetical order) Josabel Belliure, Steven Chown, Paco Ferri, Verónica Gomes and David Vieites. (Photos: Verónica Gomes [left] and Gloria Gómez-Lobo [right]).

No sooner thought than done. The collation of the dataset involved driving over 25,000 km for lizard sampling, allocating 200 hours to thermal assays, and 500 hours to lizard caring including terraria cleaning, and daily watering and life-prey feeding for each of 304 male lizards. We then statistically analysed the data in two steps with a focus on heat tolerance alone.

First, we found strong statistical support that single populations could not represent the heat tolerance of a full species, with (median) differences between populations of up to 3 °C. Such intraspecific variation nears the range of heat tolerance found across all of our study species! (median CTmax = 41.3 to 45.6 ºC).

Second, we fed our population estimates of heat tolerance into a biophysical model encapsulating how an organism exchanges heat with the environment. We used this model to quantify the annual total of diurnal hours a species would be expected to be inactive (air temperature > CTmax) per unit of occupied area (25 km2). The rationale of our analyses was to mimic the widespread practice of choosing one population for a given species (see above), run our biophysical model to get an estimate of species-level restriction time, then repeat the same approach for each population sampled for that species.

We found that restriction times varied from 43 to 188 hours (median = 83 hours) depending on which population represented a species. For an average day with seven hours of sunlight, those discrepancies would imply intraspecific discrepancies in restriction time of 7 to 27 days (median = 11 days), and > 20 days for six of our study species. This is ecologically relevant because, during restriction times, lizards would be unable to feed or reproduce (unless accessing benign microhabitats not controlled for in our analysis). The take-home message pops up concisely in the title of our article: ‘Intraspecific variation in lizard heat tolerance alters estimates of climate impact’.

Fig 3 Graphical abstract - Credit Salvador Herrando-Perez

Graphical Abstract: Heat tolerance (=CTmax, left plot) and annual restriction times for 15 lizard species from the Iberian Peninsula. Boxes represent variability among populations (2 to 5 sampled per species). In the middle, a male of Schreiber’s green lizard (Lacerta schreiberi, Iberian endemism), and below* several Spanish localities where this reptile is abundant. The species likes riparian shrubs close to mountain ranges and slopes, and is the most heavily restricted by climate in our species set – annual restriction times vary from 596 to 715 hours per 25 km2 depending on which population-level CTmax is selected as the species trait (median CTmax = 40.5 to 42 .9 °C among four study populations). * Localities (left to right): Candelario/Salamanca, Castro de Cepeda/León and La Hiruela/Madrid. (Photos: Salvador Herrando-Pérez)

In discussing our results, we were cautious about not falling into the straw-man fallacy that past macroecological studies using one thermal-trait estimate per species get it wrong. Far from that. Previous research has revealed relevant patterns and posed critical hypotheses advancing the fields of macroecology and macrophysiology.

For example, many tropical species seem to live closer to their limits of heat tolerance and might be more sensitive to climate change than temperate species. Or heat tolerance appears to be less variable than cold tolerance, supporting the notion that the former might possess less scope to evolve in a warming scenario. Although we still lack a clear understanding of the evolutionary and adaptive drivers of such variation, our overarching argument is that controlling for intraspecific variation in thermal tolerance should improve our predictions of climate impacts on biodiversity.

Ecologists and physiologists have managed to gather information about the thermal ecology of just above 2000 species, but in most cases those species have been investigated at a single location each. Expanding taxonomic coverage is indeed a worthy effort to have a global picture of ecophysiological feedbacks under climate change – for planet Earth is teeming with at least several million species. Nonetheless, to address climate impacts in a comprehensively biological manner, future work should also endeavour to sample, map and model clines of thermal tolerance in the entire distribution of single species.

Salvador would like to acknowledge the assistance of Corey Bradshaw in revising the content of this blog article.

More Info:

Chown, S.L. and Gaston, K.J. (2016) Macrophysiology – progress and prospects. Functional Ecology, 30, 330-344.

Herrando‐Pérez, S. , Ferri‐Yáñez, F. , Monasterio, C. , Beukema, W. , Gomes, V., Belliure, J. , Chown, S. L., Vieites, D. R. and Araújo, M. B. (2018), Intraspecific variation in lizard heat tolerance alters estimates of climate impact. Journal of Animal Ecology, Accepted Author Manuscript. doi:10.1111/1365-2656.12914

Valladares, F., Matesanz, S., Guilhaumon, F., Araújo, M.B., Balaguer, L., Benito-Garzón, M., Cornwell, W., Gianoli, E., van Kleunen, M., Naya, D.E., Nicotra, A.B., Poorter, H. and Zavala, M.A. (2014) The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecology Letters, 17, 1351-1364.

Stopovers for sickly songbirds

The understanding of the interplay of movement, behaviour and physiology that biologging offers has applied relevance for a range of fields, including evolutionary ecology, wildlife conservation and behavioural ecology. In recognition of this, the Journal of Animal Ecology has an upcoming Special Feature on Biologging  (submissions due 20th September).

This blog posts is written to accompany a recent publication in the Journal of Animal Ecology. Lead-author Dr Arne Hegemann is a Researcher at the Department of Biology at Lund University in Sweden. An eco-physiologist studying the interplay between physiology and ecology, Arne is interested in how immune function influences life-history decisions in general and migration in particular. 

If we humans get sick, e.g. catch a cold or have the flu, we don’t like, or can’t, go for a run or do any other sports. But what do birds do when they get sick during migration?


To answer this question, we caught small songbirds during their autumn migration in southern Sweden. We took a blood sample and attached a tiny (0.3 g) radio-transmitter to each bird. In half of all birds, we stimulated the immune system with a mimicked bacterial infection. Afterwards we released all birds, and an automated radio-telemetry system was constantly registering the presence of each bird.

We showed that those birds that received a mimicked infection stayed longer before they continued with their migration than the un-challenged birds. Hence, if birds are sick during migration, they take a rest and don’t do a migratory flight, just as we humans don’t go for a run when we are sick. Interestingly though, individuals of those species that fly all the way to Africa to winter south of the Sahara, just stayed one extra day, while individuals of those species that only migrate to Western Europe stayed for two extra days.

This suggests that birds, which need to fly to Africa are under bigger pressure to continue migration and to ensure an early arrival in Africa. Reasons may include that their main food (insects) decreases rapidly in autumn. The telemetry data furthermore showed that the birds don’t simply sit still when being “sick”, but they don’t fly around as much as the other birds. Finally, the condition of their immune system before the simulated infection had an influence on how long they stayed. As better the immune system as smaller the effect.

Taken together, our study shows that the immune system and the effect of a possible infection can have important consequences for the migration of small birds. This knowledge will help us understand the timing and behaviour of migration, especially under the threats of climate change when pathogens may spread.

More info:

Hegemann, A., Alcalde Abril, P., Sjöberg, S., Muheim, R., Alerstam, T., Nilsson, J. Å., and Hasselquist, D. (2018). A mimicked bacterial infection prolongs stopover duration in songbirds–but more pronounced in short‐than long‐distance migrants. Journal of Animal Ecology.


Stressed-Out Squirrels

A recently-published paper in the Journal of Animal Ecology has discovered that the grey squirrel (one of the most impacting alien invasive species in Europe) causes an increase in chronic stress in the native red squirrel. Lead author Dr Francesca Santicchia is a research fellow at the University of Insubria in Italy. She had studied the relationships among parasites, physiological stress, and personality in grey squirrel / red squirrel interactions. In this blog post, she tells us more about her recent paper.

Our native red squirrels (Sciurus vulgaris) are threatened with extinction in large parts of the UK and Ireland and in areas in Northern Italy colonised by introduced invasive grey squirrels (Sciurus carolinensis). The replacement of native red by alien grey squirrels, a North America tree squirrel species, is a paradigm of the negative impacts induced by biological invasions on native ecosystems. It is based on two mechanisms of competition: food exploitation competition with grey squirrels strongly reducing the availability of tree seeds for red squirrels leading to a progressive reduction in the fitness of red squirrels; and disease-mediated competition where the grey squirrels acts as healthy reservoir for a shared pathogen, the squirrelpox virus, that causes high mortality in the native species.


Red squirrel (Photo: Ambrogio Molinari)

This was best of our knowledge on the red-grey squirrel paradigm before we demonstrated that invasive grey squirrels also cause an increase in chronic stress in native Eurasian red squirrels. In collaboration with teams from Austria and the US, we used a non-invasive technique to demonstrate that the occurrence of alien grey squirrels increases chronic stress of red squirrels living in the same forests.

grey squirrel_creditFrancescaSanticchia

Invasive grey squirrels compete for food with the native red squirrels, as well as transmitting the squirrelpox virus (Photo: Francesca Santicchia)

Mammals produce extra amounts of glucocorticoid hormones when trying to cope with harmful environmental stressors. However, when elevated glucocorticoid concentrations persist over longer periods of time, they often have negative effects on an animal’s fitness. Since these stress hormones are metabolized in the gut and excreted into the faeces, their concentration in faecal pellets – taken from red squirrels when they are captured for routine population dynamics studies – can be quantified as a stress parameter without the need of taking blood samples. When these concentrations of glucocorticoid metabolites excreted in faeces (FGM) are significantly higher than normal levels, they indicate an increase in chronic stress, a situation with potential devastating effects on the animal.

red squirrel_trapping_credit_FrancescaSanticchia

Faecal pellets were collected from captured red squirrels, allowing the team to measure the presence of stress hormones (Photo: Francesca Santicchia)

We predicted that since, for red squirrels, the ‘natural’ situation is being the only diurnal arboreal mammal in our woods, grey squirrels colonizing these habitats will act as a true environmental stressor. We tested this in three ways.

First, we compared FGM concentrations in individual red squirrels co-occurring with grey squirrels (red-grey sites), with FGM concentrations of squirrels in sites not colonised by the invasive species (red-only sites). Second, we monitored changes in FGM concentrations of red squirrels in two study sites that were colonised by the invader during our study (measuring FGM concentrations before and after colonisation). Thirdly, and finally, we removed grey squirrels in red-grey sites over a period of six months, and concomitantly monitoring changes in FGM concentrations in native red squirrels.

We found that native red squirrels in sites where they co-occurred with invasive grey squirrels had glucocorticoid concentrations that were three times higher than those in sites without the invasive species. Furthermore, in those woodlands colonised by grey squirrels, stress hormones in the local red squirrels increased after colonisation by the alien species. When we experimentally reduced the abundance of the invasive grey squirrels, the concentration of faecal glucocorticoid metabolites in co-occurring red squirrels decreased significantly between pre- and post-removal periods.

red squirrel handling_creditFrancesca Santicchia

Red squirrel populations could face extinction, partly due to increased physiological stress and food competition with greys (Photo: Francesca Santicchia)

This study shows that the invasive grey squirrel acts as a stressor which significantly increases physiological stress in the native red squirrel. This is a subtle form of interspecific competition, which may exacerbate the effects of food competition. In fact, both a lower food intake and chronic stress can produce a reduction in body growth and reduce reproduction among the red squirrels that are forced to share their habitat with the invaders. Ultimately, smaller size, lower fertility, and reduced recruitment of juvenile red squirrels will lead to the extinction of a population in few years’ time.

More info:

Santicchia et al. (2018) Stress in biological invasions: introduced invasive grey squirrels increase physiological stress in native Eurasian red squirrels. Journal of Animal Ecology, 87(5): 1342-1352.

Gurnell et al. (2004) Alien species and interspecific competition: effects of introduced eastern grey squirrels on red squirrel population dynamics. Journal of Animal Ecology, 73(1): 26-35.

Effects of a maternal stress hormone across life stages

Anthropogenic disturbance is a growing threat, and the physiological consequences of exposure to such stressors is gaining increasing attention. A recent paper published in the Journal of Animal Ecology explores the consequences of stress-relevant hormones for mothers and their offspring. David Ensminger, lead author of the study, is finishing up his PhD with Dr. Tracy Langkilde, taking an integrative approach to examining the role stress-relevant hormones play in allowing an animal to respond to environmental perturbations. Dr. Tracy Langkilde is a Professor and the Head of the Department of Biology at Penn State University, and examines the mechanisms and consequences of population-level responses to global environmental change.

Maternal Stress Lizards 1

A gravid female fence lizard, Sceloporus undulatus, basking on a perch in the sun. You can see the outline of eggs near her back leg.

Many animals (including humans) are frequently exposed to stressors. Responses range from behavioral adjustments to escape from or mitigate the stressor, to alterations in the body’s hormonal profile in order to cope with the stressor. One common response is for animals to increase concentrations of “stress” hormones – cortisol in humans and many mammals, and corticosterone in reptiles and birds (hereafter referred to as CORT). In addition to the direct effect of CORT, laboratory experiments on rodents have shown that CORT can have effects that transmit from mothers to their offspring. However, few studies have looked at this phenomenon in wild organisms.

Maternal Stress Lizards 2

We capture lizards from the field using a loop of fishing line at the end of a fishing pole. We slip the loop over their bodies and gently pull them off their perch. These lizards rely on camouflage to avoid being seen by predators, so they generally sit really still while we do this.  We get lots of strange looks for walking along country roads far from water with fishing rods.

In our recent paper published in the Journal of Animal Ecology, we looked at how elevated CORT in gravid (pregnant) females can affect not only the female herself, but also the eggs she produces and the offspring that hatch out of those eggs. To do this, we collected gravid female fence lizards from the field in southern Alabama. Once back at the lab, we applied CORT to the females’ backs every night, while they were asleep, until they laid their eggs. CORT is commercially available and easily soaks into their skin when mixed with sesame oil, much like moisturizer, causing an elevation in their blood CORT concentrations that mimic the CORT response to natural stressors such as being attacked by fire ants and getting overheated. We applied just sesame oil only to half of the lizards to control for any effect of the oil or our presence.

Maternal Stress Lizards 3

Applying CORT to a female lizard’s back. You can see a drop of the CORT and oil solution hanging off the pipette tip. This was done at night, but the picture was taken during day for ease of visualization.

We tested for effects on the mothers by recording their behavior and taking blood samples to measure blood glucose. We measured the shape of the eggs once they were laid and tested a subsample for hormone and nutrients in the yolk, then incubated the rest of the eggs. Once the hatchlings emerged from the eggs, we took their morphological measurements, recorded their behavior, and took a blood sample for hormone measurements.

Maternal Stress Lizards 4.jpg

A baby fence lizard emerging from its egg. The mother lays a clutch of eggs in a sandy nest and leaves them untended. The hatchlings emerge totally self-sufficient and weigh about 0.4 grams.

We found that this increase in CORT in the mothers while gravid was enough to affect them, their eggs, and their offspring. CORT-treated mothers altered their behavior in ways that may help protect them from predators, including spending less time up on their basking perches where they would be more visible to predators. They also had increased blood glucose 3 days after laying which may give them greater short-term energy reserves. The eggs that the CORT-treated mothers laid were the same size but the makeup of their yolk differed compared to those laid by control mothers: CORT-treated mothers laid eggs that had more CORT and less protein in their yolks. However, offspring that hatched from eggs of CORT-treated mothers were longer from head to tail-tip than those from control mothers. This increase in size was only by 3%, but this could be enough to give them a head-start in the world; similar increases in body length have been shown to increase survival of hatchlings of this and other lizard species. Offspring of CORT-treated mothers had lower levels of CORT in their blood, which may buffer them when they encounter future stressors. They also exhibited increased antipredator-associated behaviors including spending more time hiding and being less likely to break their crypsis (camouflage) when provoked. This could help them avoid and survive predator encounters.

Maternal Stress Lizards 5

Hatchling lizards are especially vulnerable to predation. They blend into their perches and freeze in response to approaching predators (this one recruited a jumping spider to sit on its head).

Few previous studies have looked at multiple traits (such as behavior, physiology, and morphology) across different life stages (adult, egg, hatchling), providing only a snapshot of how CORT can alter animals. With this study, we were able to look at transgenerational effects of CORT, from the mother’s behavior and her allocation of hormones and nutrients to her eggs, to effects on behavior, size, and hormones of the resulting offspring. Doing so allowed us to shine a little more light on how CORT alters offspring and potential mechanisms for those changes. The changes we saw could impact the offspring’s ability to survive in the face of stressors such as predators. Stress (CORT) during pregnancy is typically seen as negative, but if these maternal CORT-effects better adapt offspring to a high-stress environment, it could provide evidence that maternal CORT can match offspring to their future environment.

More Info:

Ensminger, D. C., Langkilde, T. , Owen, D. A., MacLeod, K. J. and Sheriff, M. J. (2018), Maternal stress alters the phenotype of the mother, her eggs, and her offspring in a wild caught lizard. Journal of Animal Ecology. DOI: 10.1111/1365-2656.12891

Volume 85:6 a slideshow


Male Montagu’s Harrier Edwin on the hunt for grasshoppers near Djilas, Senegal. Ellinor Schlaich et al.

Issue 85:6 is now online and for the first time we have two In Focus papers in the issue as we no longer want to limit ourselves to championing only one great paper!

The First is by Pedro Jardano and takes a look at the paper by Sazatornil et al. on morphological matches and the assembly of mutualistic hawkmoth–plant networks. The second is by Shawn Wilder and Punidan Jeyasingh and they review the paper by Zhang et al. on how warming and predation risk shape stoichiometry.

To make the most of all the great photos from our authors we have included a slideshow of the best images.

Read the full November 2016 issue here.

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