Do predators create healthier prey populations?

This blog post is provided by Ellen E. Brandell and tells the #StoryBehindThePaper for the paper “Examination of the interaction between age-specific predation and chronic disease in the Greater Yellowstone Ecosystem”, which was recently published in the Journal of Animal Ecology.
Photo credit: Yellowstone Wolf Project, National Park Service

The debate about if and how predators kill their prey to result in “healthier” prey populations has been ongoing for the past three decades, but current wildlife disease issues have shone an even brighter light on it. Chronic wasting disease (CWD) is a fatal infection of deer species (deer, elk, moose) that is spreading geographically and increasing in prevalence across North America. CWD has no cure and animals are infectious long before they show symptoms or die – this is what makes it so hard for wildlife agencies to control. Some claim that the best solution for controlling CWD already exists in nature: predators. They claim that predators, like gray wolves and cougars, have heightened senses that allow them to detect and kill infected animals, thereby removing infection and preventing transmission in prey populations. This is supported by studies demonstrating that predators, especially predators that chase down their prey, select for the easiest individuals to kill, which are often the very young, very old, sick, or injured. However, other studies have shown that the “cleansing effect” of predators is modulated by other factors like prey behavior; for example, the presence of predators may cause prey to group together for protection, and within groups, high contact rates can lead to more disease transmission than would occur if there were no or fewer predators.

Age is a defining feature of both prey selection by predators and infectious disease patterns. In the case of chronic wasting disease, middle-aged deer tend to have higher prevalence than other ages because the young have not been exposed yet and the old have already succumbed to the disease. Similarly, predation has an age signature; many predators prefer to kill very young prey because they are highly vulnerable. For this reason, we suspected that the ability of predators to remove infected prey and thereby create healthier prey populations depends on the extent to which both predation and disease occur in the same ages.

The Yellowstone Ecosystem is an exciting area to study this because there is a rich predator community and CWD has just started to infect elk and deer, so there is much to be learnt about how predators, prey, and disease interact here. However, CWD is a very slow disease and it will be many years to decades before we can measure the impacts in the field. In the interim, we used data collected from predator studies in Yellowstone to develop a model of potential scenarios. More specifically, we built a mathematical model based on CWD, predators (wolves, cougars), and prey (elk, mule deer) in the Yellowstone Ecosystem to examine predator-prey-disease relationships. Our model, although based on this system, was generic and meant to explore the relationship between age-specific predation and disease. We built in realistic ecological components including prey age and sex, increasing CWD transmission rates as the infection progressed, a predator population that fluctuated with prey abundance, and predator selection of prey based on their age and infection severity. This work is now published in the Journal of Animal Ecology

Wolves hunting an elk calf in Yellowstone National Park. (Photo credit: Yellowstone Wolf Project, National Park Service)

Results from our model suggest that predators can reduce CWD prevalence in a prey population under realistic conditions. Predators are more effective at removing CWD when they select for prey ages with the most infections, which in this case is younger adults. However, this comes at a cost because younger adults are also responsible for population growth via reproduction and high survival rates when uninfected. Typically, wolves prefer to kill juvenile or old prey and cougars prefer juvenile prey – therefore, these predators must switch their preferred prey age class to effectively remove CWD. This could happen if CWD makes deer and elk more vulnerable to predation, which has been observed in certain settings. We demonstrate that prey selection by age and infection severity is very important when considering predator-prey-disease relationships, and predator cleansing effects can be complex. The utility of models like this is a deeper understanding of complex ecological relationships, but models require simplifying certain processes as well and should be interpreted with some caution.

Our objective was to better understand the interaction between disease and predation that is characterized by prey age. Our work does not show that predators will reduce disease burdens in prey populations for all types of infectious diseases. And in fact, there are many areas where CWD-infected deer and elk coexist with cougars, coyotes, and black bears. However, wolves and CWD-infected prey are just starting to overlap in the Yellowstone Ecosystem, Great Lakes region, and soon in Colorado. Our model demonstrates the possibility of predator cleansing effects, yet whether or not wolves will actually have a detectable effect on CWD in these areas will likely take decades of data collection to determine. For example, the rate at which predators select infected individuals compared to healthy individuals is a key element that requires many years of data collection to estimate. Protected areas like national parks will be critical to study because wolves and other predators occur at relatively higher densities than managed lands, and our results show that at least moderate predator abundance and kill rates are required to reduce disease prevalence in prey. Given more data and stronger estimates for our model, we can move towards predicting predator-prey-disease outcomes rather than identifying a range of potential scenarios.

Read the paper

Read the full paper here: Brandell, E.E., Cross, P.C., Smith, D.W., Rogers, W., Galloway, N.L., MacNulty, D., Stahler, D.R., Treanor, J. and Hudson, P.J. (2022), Examination of the interaction between age-specific predation and chronic disease in the Greater Yellowstone Ecosystem. J Anim Ecol. Accepted Author Manuscript. https://doi.org/10.1111/1365-2656.13661

Catching the parasite: three-spined sticklebacks eat trematode free-living stages

This blog post is provided by Ana Born-Torrijos and Miroslava Soldánová and tells the #StoryBehindThePaper for their article “Cercarial behaviour alters the consumer functional response of three-spined sticklebacks“, which was recently published in Journal of Animal Ecology.
Trematode free-living stages emerging from their snail host Radix balthica. Credit: Miroslava Soldánová.

When we see a small fish swimming about in a lake, we might assume they are searching for something to eat, perhaps some copepods, cladocerans or ostracods. What rarely springs to mind is that these small fish may in fact be feeding on parasites. Trematode parasites have free-living infectious stages called cercariae that swim in the water to infect their next hosts. During this brief life span of approximately 24-72 hours, these cercariae are vulnerable to predation from non-host predators, who simply regard them as an abundant, energy rich prey resource similar to zooplankton. Furthermore, some predators have the ability to act as biocontrol agents of parasite-induced diseases, which are particularly important in a context of future climate change scenarios.

How do we study parasite consumption by a fish predator?

Trematode infections often have a patchy distribution in their first intermediate snail hosts, from which the free-living cercariae are released. This causes the density of trematode cercariae to naturally vary within and among lake habitats. Consumer functional responses (hereafter ‘FRs’) describe the relationship between the consumption rate of a predator and the density of its prey, and are useful tool for understanding how predator-prey dynamics may change as prey densities vary.

Sampling of the first intermediate snail host Radix balthica, from which the free-living cercariae are released. Credit: Rune Knudsen.

Three main FR types are often used to describe predator-prey dynamics: Type I – when a predator consumes a constant proportion of the available prey; Type II – when the proportion of prey consumed decreases as the density of the prey increases; Type III – when the proportion of prey consumed initially increases, then decreases with increasing prey density. The main difference between Type II and Type III FRs is the proportion of prey that are consumed when the density of prey is low. Predators displaying a Type II FR are able to consume a high proportion of prey even when only few prey are present, which may have destabilising effects on prey populations.

The three types of functional responses to describe the relationships between prey density and prey consumption.
Functional responses in different predator-prey combinations

Our study investigated how the widely distributed freshwater fish, three-spined sticklebacks Gasterosteus aculeatus, consumed cercariae of two trematodes (Trichobilharzia, Plagiorchis) commonly found in lakes throughout Europe.

The beautiful study area, sub-Arctic lake Takvatn in Norway. Credit: Rachel Parterson.

Our FR experiments allowed three-spined sticklebacks to consume cercariae at a range of naturally occurring densities. We also considered how ecologically relevant factors may alter consumption rates, using (i) three-spined sticklebacks with different degrees of cestode parasitic infection, and (ii) two temperatures (6, 13ºC) representative of warmer and colder months in our sub-Arctic lake study system. Do not hesitate to check out our full paper if you are interested in the effects caused by predator’s infection status and water temperature. Three-spined sticklebacks displayed different FR types towards each trematode genera: Type II for Plagiorchis spp. and Type III for Trichobilharzia, with an overall higher consumption on Trichobilharzia.

A. Plagiorchis cercariae swimming in the water after emerging from their first intermediate snail host Radix balthica. B. Plagiorchis cercaria under the microscope (̴ 480 µm). Credit: Miroslava Soldánová.
A. Trichobilharzia cercariae swimming in the water after emerging from their first intermediate snail host Radix balthica. B. Trichobilharzia cercaria under the microscope (̴ 940 µm). Credit: Miroslava Soldánová.

Why do fish consume two tiny cercariae in a different manner?

            Imagine you are a fish searching for prey; you would be probably attracted to bigger and vigorous prey, right? Trichobilharzia is twice as big as Plagiorchis, and furthermore, they swim in dense clouds in a “rest-swim-rest” motion that could facilitate their predation. In contrast, Plagiorchis may go unnoticed by pelagic fish since this parasite swims continuously and slowly in benthic habitats. At the same time, this behaviour might make Plagiorchis cercariae easier to prey on when present at low densities, determining a Type II response, while Trichobilharzia may be more difficult to catch when swimming isolated from a cercariae cloud. The different swimming patterns have likely evolved to facilitate transmission to the next host, which are benthic invertebrates for Plagiorchis and birds for Trichobilharzia. It is then the traits inherent to parasite transmission and dispersal that likely determine the FR of three-spined sticklebacks towards these cercariae.

Video showing a three-spined stickleback actively consuming trematode free-living swimming cercarial stages during a functional response experimental trial.
Three-spined sticklebacks’ predatory impact on cercarial prey

Cercariae consumption by three-spined sticklebacks may have major impacts on trematode population dynamics, especially considering the wide distribution and high population densities three-spined sticklebacks can attain. This is where FRs become crucial in understanding the potential impact of a fish predator on parasite populations, by determining the rate at which parasites are consumed depending on their density in the environment. FRs could thus help to evaluate potential biocontrol agents to modulate problematic trematode infections. Although our study demonstrated that three-spined sticklebacks showed a Type III response to Trichobilharzia prey, the identification of a fish species displaying the destabilising effects of Type II responses would be highly beneficial in the suppression of this parasite, which is the main causative agent of human cercarial dermatitis (swimmer’s itch) in Europe. The right fish-trematode combination that might help reduce parasites of medical and veterinary importance is thus waiting to be discovered!

So, next time you see some small fish swimming about in your local lake, just imagine all the parasites that they are happily eating!

Ana Born Torrijos is a Postdoctoral Researcher at the Institute of Parasitology from the Biology Centre of the Czech Academy of Sciences (BC CAS). She is deeply interested in behavioral ecology of parasites, ecological parasitology and parasite transmission strategies. Her research includes in vivo and in vitro experiments in a parasitological and food ecology framework. Currently she leads a project focused on the infection and transmission strategies of a trematode present in marine aquaculture, involving transcriptomic and proteomic data to elucidate the physiological basis of infection-associated changes in host behaviour. You can follow Ana on Twitter @BornTorrijos. Researchgate: https://www.researchgate.net/profile/Ana_Born-Torrijos.

Miroslava Soldánová, Ph.D. is a freshwater ecologist with a broad interest in the role of digenean trematodes in aquatic ecosystems, their interactions with ecological communities, effects on food web dynamics and importance in the ecosystem structure and functioning. Miroslava’s research also focuses on elucidating ecological and environmental processes forming trematode populations and communities in freshwater molluscs at spatial and temporal scales in various freshwater ecosystems, uncovering hidden trematode diversity, and studying life-cycles, transmission strategies and use of trematode communities as indicators of environmental conditions and ecosystem stability.

Read the paper

Read the full paper here: Born‐Torrijos, A, Paterson, RA, van Beest, GS, et al. Cercarial behaviour alters the consumer functional response of three‐spined sticklebacks. J Anim Ecol. 2021; 00: 1– 11. https://doi.org/10.1111/1365-2656.13427

Urbanization alters predator‐avoidance behaviours

Urbanisation is changing the natural landscape at a global scale. This obviously alters habitat structures, but what is the influence on predator-prey dynamics? A recent paper in the Journal of Animal Ecology studied two urban prey species to examine whether urbanisation changed their predator-avoidance behaviour. Lead author Dr Travis Gallo, an Urban Wildlife Postdoctoral Researcher at the Urban Wildlife Institute, Lincoln Park Zoo, tells us more. 

It’s easy to recognize that urban environments are quite different from the rural or natural landscapes ecologists have historically studied. Thus, urban ecologist have long stated that traditional ecological principles should be adjusted or fine-tuned to better fit urban ecosystems. For example, continuously maintained landscapes in cities stabilize primary productivity and reduce the ‘dynamic’ part of the well-studied principles of top-down and bottom-up trophic dynamics. Along those same lines, we became interested in the role that cities and their unique characteristics play in predator-prey dynamics.

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A coyote out in the open in Chicago (Photo: Julie Fuller)

In a study recently published in the Journal of Animal Ecology, we explored predator-avoidance behaviors of two common mammal species – eastern cottontail (Sylvilagus floridanus) and white-tailed deer (Odocoileus virginianus) in the highly urbanized landscape of Chicago, IL USA. Contrary to what one might expect, we found that coyotes (Canis latrans) – a natural predator – had little influence on predator-avoidance behaviors of either species in the more urbanized areas of Chicago.

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White-tailed deer doe and fawn (Photo: Urban Wildlife Institute)

But first let’s step back and offer a little context. Typically, the presence of a predator influences the distribution and behavior of prey species. One might expect that prey, if able, would first and foremost avoid habitat patches that contain predators. But our expectations for this outcome were derived from more natural systems — so how might this relationship change in a city? Habitat patches in urban environments are typically spaced far apart and embedded in a matrix of houses, businesses, and roads. The roads and buildings between habitat patches could restrict an animal’s ability to move between them. As a result, it may be all the more difficult for prey to ‘pack up and move’ if they so happen to encounter a predator. Therefore, we predicted that urban prey might be forced to occupy the same habitat patches as predators. If this were the case, we predicted that prey would change their daily activity schedules or increase their vigilance to avoid interactions with predators. But again, human development and human activity in and around an urban habitat patch might alter a species ability to perform such predator-avoidance behaviors.

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Remotely-triggered wildlife cameras around Chicago allowed a sneak peek into predator-prey dynamics of local wildlife (Photo: Urban Wildlife Institute)

Using photos collected from over 100 remotely triggered wildlife cameras placed across the greater Chicago region, we first assessed whether deer and cottontails were more likely to occupy the same habitat patches as coyotes – or were they avoiding them across the landscape? Additionally, we used the time of day each picture was taken to explore whether deer and cottontails changed their daily activity patterns when coyotes were present within a habitat patch. And finally, in each picture of deer and cottontail we identified whether the individual animal had their head up in a vigilance posture or down in foraging posture, and used that information to assess whether the presence of coyotes increased their rate of vigilance.

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An eastern cottontail displaying vigilance (Photo: Urban Wildlife Institute)

 

Contrary to our prediction – that prey species would likely be constrained to the same habitat patch as coyotes – we found no evidence of spatial aggregation, nor did we find any evidence of spatial avoidance. Both deer and cottontails were spatially distributed independent of where coyotes were present. Additionally, we found that neither species changed their daily activity schedules when coyotes were present. Our most interesting finding was that cottontails had their highest rates of vigilance when coyotes were absent from the most urban sites. Even when coyotes had a low probability of being at a site, cottontails were still on their toes! In Chicago, these highly urban habitat patches (e.g., city parks, golf courses, cemeteries) are often visited by people and in many cases people with their pets (sometimes untethered). While these urban green spaces may provide a refuge from coyote (i.e. a human-shield effect), they likely come with tradeoffs in the form of increased interactions with humans and their pets. As a result, their vigilance rates are high in urban areas even when coyotes are not around. Conversely, as sites became less urban we began to see a shift back to expected vigilance behaviors, and rabbits were more vigilant when coyotes were present in the less urban areas.

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Cemetaries are highly-urban habitat patches, regularly visited by people (Photo: Urban Wildlife Institute)

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As well as people, wildlife also come across pets (Photo: Urban Wildlife Institute)

These results indicate that urban ecosystems are still fear driven systems, but perhaps, the fear inducing agents are now anthropogenic in nature. Traditionally we think of predator-prey dynamics in the context of two interactions – predators and prey. But in urban ecosystems we must begin to think of it as a three-player game – predators, prey, and people. Thus, we should begin to explicitly consider people in our ecological equations – especially in urban ecosystems. Doing so will improve our predictions, advance our understanding of urban ecology, and increase our ability to conserve biodiversity on an urbanizing planet.

More Info:

Gallo et al. (2019) Urbanization alters predator‐avoidance behaviours. Journal of Animal Ecology. https://doi.org/10.1111/1365-2656.12967

A high cost of infidelity for swift parrots

A recent paper published in the Journal of Animal Ecology has found that a chronic shortage of females in a critically endangered parrot species has led to love triangles, sneaky sex on the side, increased fighting between males, and fewer babies.  Here to tell us more are three of the authors: Rob Heinsohn, George Olah, and Dejan Stojanovic.

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Swift parrot at nest hollow (Photo: D Stojanovic).

Most birds are at least socially monogamous, although paired individuals in many species often seek various benefits from extra-pair sex. The ratio of males to females plays a large role in determining the mating system, and even large, long-lived bird species can change to mate sharing when males outnumber females. Parrots are considered to be mostly monogamous but occasionally mate in different configurations when there is a scarcity of mating opportunities. In a recent paper in the Journal of Animal Ecology we outlined a revealing case of a parrot species that appears to have adopted high rates of extra-pair sex after the sex ratio became strongly male-biased due to unnatural causes. We found that mating in trios came at a cost to both individuals and the population.

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Swift parrot feeding from blue gum flowers (Photo: D Stojanovic).

In 2014 we reported that an introduced predator, the sugar glider (Petaurus breviceps), kills large numbers of breeding female swift parrots (Lathamus discolor) in their nest hollows. These small marsupials can access the hollows high in old Eucalyptus trees and kill the female while she is incubating her eggs. Sugar gliders were introduced accidentally to Tasmania in the 19th century but have proliferated in recent times as forests become more disturbed and fragmented. Swift parrots are nomadic and gain a limited reprieve from this introduced predator in occasional years when their food, nectar from flowering Eucalyptus trees, becomes available on predator free islands. On average though, over 50% of adult female swift parrots die each year from sugar gliders leading to a population in freefall with a projected decrease of over 90% in 16 years.

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Sugar glider entering swift parrot nest hollow (Photo: D Stojanovic)

Male swift parrots now outnumber females almost three to one. We became aware that at many nests an extra unpaired male would hang around and harass the resident female and sometimes engage in courtship feeding with her. The resident males were constantly chasing these interlopers out of the territory. When we examined the mating system using molecular techniques, we found that over half of the nests had babies with more than one father. In other words the resident females were engaging in sneaky sex with the extra males. We think it must have been in the females’ best interests to mate with other males just to get them off their backs.

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Swift parrots killed by sugar gliders in nest (Photo: D Stojanovic).

Our analysis showed that mate sharing was not beneficial for anyone in the ménage à trois. The overall number of fledglings produced fell when the sex ratio was more male-biased, and shared paternity went up. Female reproduction went down a little but males suffered greater individual losses whenever mate sharing occurred. It is not surprising that males fight so hard to protect their mates, but it seems they lose precious time and energy constantly chasing the intruders away and may be unable to feed the nestlings as much.

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Female with three large nestlings (Photo: D Stojanovic).

Alongside individual losses the overall population takes a direct hit from lower reproductive success. We used population modelling to isolate the impact of lower reproduction due to mating in trios. Although most of the projected 90% population decline was directly attributable to sugar gliders killing nesting females, the impact of lower breeding success from shared mating reduced the population by about five per cent.

Our study is important because it teases apart how individuals in populations may be affected differently by introduced predators – especially how the loss of so many females can change the balance of the sexes, as well as the whole mating and social system. Swift parrots are not the only species where the fabric of society is threatened by too few females. This process is happening in other birds, reptiles, and even humans in some parts of the world.

Our team is looking for innovative ways to limit the impact of sugar gliders on swift parrots. Our first success was to improve the habitat for swift parrots on small islands off Tasmania where sugar gliders do not occur by providing over 500 nest sites including nest boxes and artificially cut hollows. Our other strategy has been to invent a new type of predator-proof nest box for when food availability leads to the swift parrots breeding in predator infested habitat on mainland Tasmania. We now use a light sensitive door that effectively locks the breeding female safely inside the nest box at night, and opens at first light to let her out in the morning. Our ‘possum-keeper-outerer’ or PKO holds great promise if we can get enough females to use nest boxes instead of natural hollows.

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Sugar glider thwarted by automatic door on a swift parrot nest box (Photo: D Stojanovic).

The myriad impacts of an introduced predator are just one side of the equation in saving swift parrots from extinction. The other side is a continuing loss of their blue and black gum forest habitat due to industrial scale logging and other processes. Swift parrots are migratory and every year, upon their return to Tasmania, they look for the right combination of ephemerally flowering eucalypts close to old growth forest with enough tree hollows. Habitat has been so reduced that in some years they fail to find enough opportunities to breed. Solving the sugar glider problem will not save swift parrots from extinction if habitat continues to be lost.

More Info:

Stojanovic, D., Webb, M., Alderman, R., Porfirio, L., & Heinsohn, R. (2014). Discovery of a novel predator reveals extreme but highly variable mortality for an endangered bird. Diversity and Distributions, 20, 1200–1207. https://doi.org/10.1111/ddi.12214

Heinsohn, R., Webb, M., Lacy, R., Terauds, A., Alderman, R., & Stojanovic, D. (2015). A severe predator-induced population decline predicted for endangered, migratory swift parrots (Lathamus discolor). Biological Conservation, 186, 75–82. https://doi.org/10.1016/j. biocon.2015.03.006

Heinsohn R, Olah G, Webb M, Peakall R, Stojanovic D. (2018). Sex ratio bias and shared paternity reduce individual fitness and population viability in a critically endangered parrotJournal of Animal Ecologyhttps://doi.org/10.1111/1365-2656.12922

Stojanovic, D., Cook, H. C. L., Sato, C., Alves, F., Harris, G., McKernan, A., & Heinsohn, R. (2018). Pre-Emptive action as a measure for conserving nomadic species. The Journal of Wildlife Management, https://doi.org/10.1002/jwmg.21575

Stojanovic, D., Eyles, S., Cook, H., Alves, F., Webb, M., & Heinsohn, R. (2018) Photosensitive automated doors to exclude nocturnal predators from nest boxes. Animal Conservation DOI: 10.1111/acv.12471

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).

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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.

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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.

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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.

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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.

Go Big or Go Home: Pitcher plant hosts and their crab spider tenants

The carnivorous traps of Nepenthes pitcher plants are sometimes inhabited by a species of crab spider which ambushes insects as they arrive at traps. Recently published work by Weng Ngai Lam and Hugh Tan showed that this apparent thievery is actually beneficial to the plants — but only when crab spiders attack big prey with high nutrient contents.

Pitcher plants are carnivorous plants that trap and digest insect prey to supplement their nutrient requirements. But some specialized animals are able to exploit their traps and make a living out of these modified leaf structures. One such animal is the pitcher crab spider (Thomisus nepenthiphilus), which lives in pitchers of the slender pitcher plant (Nepenthes gracilis). This crab spider spends its whole life in pitchers, building its nests on pitcher walls, and diving into its fluids to hide whenever it senses danger from without.

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A female pitcher crab spider (Thomisus nepenthiphilus) guarding her nest in a dissected upper pitcher of the slender pitcher plant (Nepenthes gracilis). (Photo: Weng Ngai Lam)

Pitchers secrete nectar around their lids and lips (also known as ‘peristomes’), and visiting insects often slip into their fluids while feeding on this nectar. Slender pitcher plants trap lots of ants this way, but only succeed in trapping flying insect prey occasionally. In an earlier, experimental study, we had shown that the pitcher crab spider ambushes flesh flies as these are feeding at pitchers, and subsequently drops prey carcasses into pitcher fluids after feeding on them. Fortunately, flesh fly carcasses still contain some nutrients after being consumed by crab spiders, and pitchers can benefit from this residual nitrogen. Thus, pitchers which are not inhabited by crab spiders catch fewer prey, but get more out of each, while those which are inhabited ‘catch’ more, but get less out of each.

pitchercrabspider_wengngailam

A pitcher crab spider waits motionlessly for prey at the mouth of a pitcher. (Photo: Weng Ngai Lam.)

In our recently published article in the Journal of Animal Ecology, we examined the natural prey spectra of pitchers which were inhabited or uninhabited by crab spiders, and identified a few prey taxa which were ‘trapped’ in higher numbers in crab spider-inhabited ones. We then measured the nutrient contents of these prey and estimated the nutritional benefit that pitchers would obtain from crab spiders’ consumption of them.

We found that crab spiders increased the prey capture rates of multiple different prey taxa, including mosquitoes, scuttle flies, flesh flies, cockroaches, bean bugs, and even other spiders. Unsurprisingly, small prey were trapped in greater abundances, both by pitchers alone, and by crab spiders inhabiting them, while large prey were only trapped occasionally. However, crab spiders’ contributions to pitchers were much higher through large prey like bean bugs and cockroaches than they were through small prey like mosquitoes and scuttle flies.

pitcherspiderprey_wengngailam

A crab spider with a freshly-killed flesh fly. (Photo: Weng Ngai Lam.)

Reviewing the literature on nutritional mutualisms, we classified this interaction as a ‘resource conversion’ mutualism—an interspecific interaction in which one species (in this case the crab spider) converts a resource from a poorly-accessible state (flying prey which pitchers seldom trap) to a more accessible one (prey carcasses deposited straight into pitcher fluids) for its partner (the pitcher plant), often in exchange for a non-resource benefit such as protection or domicile. Our study confirms the existence of mutualism between the slender pitcher plant and the pitcher crab spider. But it also shows that this relationship, like many other resource conversion mutualisms, can have both beneficial or harmful net effects on the host species, depending on the quality (in this case prey nutrient content) of the resource being converted. It seems, from the perspective of the pitcher plant, that crab spider tenants should either go big or go home.

More Info:

Lim, R.J.Y, Lam, W.N., and Tan, H.T.W. (2018) Novel pitcher plant–spider mutualism is dependent upon environmental resource abundance. Oecologia.

Lam, W.N., and Tan, H.T.W. (2018) The crab spider–pitcher plant relationship is a nutritional mutualism that is dependent on prey resource quality. Journal of Animal Ecology.

 

Understanding what’s driving Arctic skua declines in Scotland

Dr Allan Perkins is a Senior Conservation Scientist at the RSPB Centre for Conservation Science. Here, he describes some of the challenges faced by Arctic skuas and his paper assessing ‘bottom-up’ processes, which was recently published in JAE.

Arctic skuas are spectacular birds, pirates among our seabird communities. Having spent the winter, off Namibia and South Africa, they return each spring to nest on the coastal heaths and clifftops of northern and western Scotland.

Arctic Skua adult

Arctic skua adult (pale-phase)

They are a kleptoparasite. This means they steal most of their food from other birds – involving aerial chases with aerobatic twists and turns until their victim drops its food. In UK waters, smaller seabirds such as terns, kittiwakes and auks act as the skuas’ main ‘hosts’, and most skuas nest close these species’ breeding colonies.

Their actual food is small fish, especially sandeels, and skuas exploit the ability of other seabirds to catch these below the sea’s surface.

Scotland lies at the southern edge of the Arctic skua’s global breeding range, with Shetland and Orkney their stronghold, but with other colonies in Sutherland, Caithness, and the Hebrides as far south as Jura.

The last national seabird census (Seabird 2000) recorded 2136 Apparently Occupied Territories (AOTs), compared with 3388 AOTs in the previous 1985–88 census. Since Seabird 2000, numbers have continued declining, and Arctic skuas now on the Red list of Birds of Conservation Concern, with breeding records now sought by the Rare Breeding Birds Panel.

The Study

We wanted to assess the relative impacts on breeding Arctic skuas of ‘bottom-up’ pressures caused by food shortage, and ‘top-down’ pressures from predation. Findings from the study have just been published in the Journal of Animal Ecology.

Using regional and national datasets, notably the Seabird 2000 census and the UK Seabird Monitoring Programme (SMP), we collated data on Arctic skuas and five other species for 1992–2015 from colonies throughout Orkney and Shetland, and also Handa island in northwest Scotland.

These included four major species exploited by Arctic skuas – kittiwake, guillemot, puffin and Arctic tern – whose population size and breeding success we used as an index of food availability around Arctic skua colonies.

Arctic terns

Arctic terns are one of four seabird ‘hosts’ that Arctic skuas in Scotland frequently kleptoparasitise (steal food from).

For predation pressure, our measure was the local density of great skuas (or bonxies). These are another pirate of the seas, and a large, powerful predator weighing in at around 1.2–1.6 Kg compared with just 0.3–0.6 Kg for the Arctic skua.

Although not as agile as Arctic skuas, great skuas also steal food from other seabirds. However, they also frequently kill and eat the seabirds themselves, including chicks, fledglings and sometimes even the adult Arctic skuas.

Great skuas also scavenge bird and animal carcasses as well as waste fish discarded from trawlers – utilising a variety of food resources has helped increase their population size in Scotland.

In the 1985–88 census, 7645 AOTs were recorded, but this increased to 9635 AOTs in the Seabird 2000 census, including colonising new breeding areas in western Scotland and Ireland. Although in many ways this is regarded as a conservation success story (our islands hold around 57% of the global population), several studies during the 1990s and 2000s revealed that great skuas were negatively impacting other seabirds at some colonies.

Adult Great Skua

Adult Great Skua

We used digital mapping and statistical models to quantify changes in population size and breeding success of Arctic skuas, their hosts, and great skuas. We also used it to determine the relative effects of host breeding success and great skua density on Arctic skua breeding success and population trends.

We compared these trends and effects between different types of Arctic skua colony, categorised by the local abundance of cliff-nesting hosts (i.e. kittiwakes, guillemots and puffins).

What did the study find?

Between 1992 and 2015, Arctic skuas declined by 81%, and their average breeding success fell sharply, from around 0.9 chicks per pair in the early 1990s to 0.3 chicks per pair by the 2010s.

It seems clear that reduced breeding success is driving the population decline of Arctic skuas, and the two were strongly correlated, although large fluctuations between consecutive years at some sites suggested other factors at play. These may include variation in adult survival, or large scale non-breeding in years with exceptionally poor food availability.

Amongst the hosts, average Arctic tern, kittiwake and puffin colony sizes declined by approximately 90% each, and guillemots by 42%. We should stress that although indicative of the severity of declines, these figures are not derived from complete censuses of the entire populations in Orkney and Shetland and should not be used in that context – ie they are from regularly monitored colonies that hold only a proportion of the whole population.

Breeding success of hosts also declined significantly, indicative of large-scale drivers of food shortage in most years since 2000, linked to climate change. A large body of research points to increasing sea temperatures and oceanographic changes making the waters around Orkney and Shetland less hospitable for sandeels.

Unsurprisingly, Arctic skuas fledged more chicks in years when their hosts had good breeding success – i.e. in years when sandeels were abundant.

Arctic skua chick

Arctic skua chick

However, their population trends and breeding success were negatively associated with great skua density, and variation between colony types suggested that Arctic skuas were most sensitive to top-down predation pressures at colonies where great skuas had increased the most. Great skuas had increased by a colony average of 75%, but this masked substantial variation. The largest colonies showed declines while other sites had been colonised, such that overall great skua numbers had remained stable.

It seems that great skuas have to some extent redistributed themselves within Orkney and Shetland, with populations declining at the super-colonies of Hoy and Foula, but increasing rapidly on other islands including those with relatively small cliff-nesting seabird colonies (hundreds to low thousands of birds) such as Mousa, Fetlar, Rousay and Papa Westray.

These islands also saw some of the largest declines in Arctic skuas, and it would appear that great skuas here are adding top-down pressures onto a species that is already facing significant bottom-up pressures due to lack of food. At very large seabird colonies such as Fair Isle, Hermaness and Handa, great skuas have also increased, but Arctic skuas at these types of colonies appear to be more sensitive to bottom-up pressures (lack of food) than to predation pressure from great skuas.

How can you help?

Check back next week for our follow-up blog post, containing details on how you can help future projects by participating in seabird monitoring!

More Info:

Perkins, A. et al. (2018) Combined bottom‐up and top‐down pressures drive catastrophic population declines of Arctic skuas in ScotlandJournal of Animal Ecology87: 1573–1586. https://doi.org/10.1111/1365-2656.12890

 

Understanding ecosystem function (and each other)

Proponents of interdisciplinary work can range from grant reviewers to department chairs, but what goes into this type of collaboration? Alva Curtsdotter (ecologist) and Amanda Laubmeier (mathematician) talk about the process behind their recent paper on dynamic food web modelling.

Alva: There has for some time now been an increasing interest in using dynamic food web models in ecosystem function research. These mathematical models describe species’ feeding interactions and how, as a result of these interactions, species’ abundances develop over time. The idea is that these models could help us understand ecosystem functions and services that include predator-prey interactions, such as biological pest control. The research team I was in had already applied these models to small predator-prey assemblages in the lab, and a next logical step would be to try the same for a real-world ecosystem. From a previous project, we had data on the food web structure and species abundances of arthropod prey and predators in barley fields. We decided to test whether we could use a food web model, assuming body size dependent consumption rates, to replicate the observed abundances of an herbivorous pest, the bird cherry-oat aphid (Rhopalosiphum padi). Essentially, we were asking whether such a general model could describe abundances observed in a specific ecosystem — or if the real world was simply too complex for such approaches.

RHOPAL~1

The focal prey species: the bird cherry-oat aphid (Rhopalosiphum padi). Photo by Adam Sisson (Wikimedia commons).

Amanda: This is where I came in. Our group works with real-world data, and we’re often interested in how that data lines up with mathematical descriptions of the world (data-fitting). There’s a great theoretical framework for answering this kind of question, and plenty of related mathematical tools. It’s an exciting area to work in, because the world is a lot messier than mathematics. For example, we could clearly see aphids dying off in this data set, but there wasn’t information to include in our analysis about what was causing it. There’s a lot going on in this system, so figuring out what actually mattered for the aphid population was neat.

DSC_5083

Ladybugs were one of the three main predator groups. Here, the seven-spotted ladybug (Coccinella septempunctata). Photo by Mattias Jonsson.

Alva: Unlike Amanda, this was my first time fitting a mathematical (not statistical!) model to real-world data. I knew it would be challenging but, still, I had not expected how much work it would be just to get the data in shape! For example, in the field we have to use different sampling techniques for different organisms, and not all of these methods are well suited to estimate population densities. But to use that data for the model-fitting, we needed to convert it into population density (individuals per unit area) so that we had a standardized common currency for the abundances.

Amanda: Another challenging aspect of this project was that we all came from different backgrounds. We had differing opinions about the power of mathematical descriptions of physical systems (Alva being more of an optimist in this area than myself), and random bits of terminology wouldn’t translate across disciplines. I remember a meeting where I needed to know which species interact in order to solve the equations for aphid abundances. But our collaborators didn’t think of this information as part of the model at all, so we managed to talk around one another for hours!

DSC_5276

Spiders were one of the three main predator groups. Here, a wolf spider (Lycosidae). Photo by Mattias Jonsson.

Alva: Looking back on it, these initial communication challenges make me laugh. It’s almost hard to understand now, what was so difficult then! We are certainly still learning – a lot – from each other, but at least the communication barrier is not quite as ridiculous as it once was.

Amanda: And, despite all that, we did manage to fit the model and get some neat results.

Alva: Oh yes! I was pleasantly surprised by how much of the aphid abundance variation the model could capture. Especially considering how simple the model is and how many environmental factors there are that can influence a species’ abundance. But to me, one of the major advantages of working with a model that describes ecological mechanisms, and not just their outcome, was that we could go beyond model fit! For example, we could look into consumption rates of our predators in the model, both to evaluate model performance and as a way to to gain insight into ecosystem function.

aphidClumpCoccinellaByChloe_Brightened20Contrast20Colder

The seven-spotted ladybug (Coccinella septempunctata) consuming black bean aphids (Aphis fabae). The aphids used in the study were bird cherry-oat aphids, but the authors assure the reader that the ladybug’s table manners are about the same regardless of aphid species. Photo by Chloë Raderschall.

Amanda: Mathematically, the project gave rise to pretty interesting ideas as well! A lot of the time, it’s easy enough to fit a model to data. The thing we wonder about is whether the description we have is meaningful or unique. An aspect of this is “parameter identifiability,” where we check if the effects of different components of the mathematical model can be disentangled from one another. There’s so much you could investigate there. Thankfully, working with our ecological collaborators helped us focus our analysis on answering meaningful questions (without going down too many rabbit holes).

Harpalus rufipes

Ground beetles were one of the three main predator groups. Here, a Strawberry seed beetle (Harpalus rufipes). Photo by Mattias Jonsson.

Alva: Yes, and I think this really highlights the benefits of interdisciplinary work; it can improve your research questions as well as your methods, and can really open you up to new concepts and perspectives. I used to consider a good model to be one that has good predictive ability and is based on an accurate description of the underlying processes. But what good is a model if it’s formulated so that its components aren’t identifiable? This is certainly something that I will be thinking more about in choosing and developing models in the future.

Amanda: As fruitful as this research has been for all of us, I do think a challenge has been finding the right format for communicating our work. I remember we first wrote it up as a methods paper, but the journal rejected us, pretty much saying, “This isn’t a methods paper.” The rejection was, in itself, useful; it helped us translate our results in a more meaningful way. Going to conferences and talking with peers also helped us figure that out. I’m happy we’ve found a good place for this manuscript, but it certainly took some trial and error.

Alva: But the funny thing is that wherever we have presented this project, people get excited about it. Partly it’s because we have some unanswered questions, like “What is causing those darn aphids to crash mid-season?” — people really go into mystery-solving mode with that one! But mostly I think people get excited because we show that a general model can actually describe a lot of the natural abundance variation in a specific system (in the field!), without including a lot of system-specific information! And I think that the key to success is the trait-based approach to modeling. Without it this type of modelling wouldn’t be feasible, nor do I think it’d be successful. So I’m glad the paper is getting published now, so that people can read it and (hopefully) be as excited about it as we are. I also hope people will read it and go, “Oh, that’s cool but I could do it so much better!” — and then do so. I would love to see more of this kind of work.

More info:

Curtsdotter, A., Banks, H.T., Banks, J.E., Jonsson, M., Jonsson, T., Laubmeier, A.N., Traugott, M., and Bommarco, R. (2018) Ecosystem function in predator‐prey food webs ‐ confronting dynamic models with empirical data. Journal of Animal Ecology. DOI: 10.1111/1365-2656.12892

Banks, H.T., Banks, J.E., Bommarco, R., Curtsdotter, A., Jonsson, T., Laubmeier, A.N. (2017) Parameter estimation for an allometric food web model. International Journal of Pure and Applied Mathematics 114: 143-160.

I Set Out To Track Birds, but Ended Up Tracking Predators

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).

But sometimes, you don’t end up tracking exactly what you expect… This was the case for Dylan Smith, an undergrad at Kansas State University doing research on grassland songbirds. However, not to be discouraged by this surprising result, Dylan is currently looking for a Master’s program.

I was looking for a baby bird, a Dickcissel that recently left the nest (fledged). So why am I holding a snake? Because that little lump in the snake’s belly is the bird that I was looking for. Thanks to the radio transmitter I attached to the bird, I can still locate it, even from the inside of a snake’s belly. I can follow the snake long enough to retrieve the transmitter after the snake is – ahem – “finished” with it. Now that I have retrieved it, I can clean it off very, very thoroughly and reuse it on another bird later.

Fig 1 - Dylan Smith

There’s a bird in this snake!

Even though I set out to look for young Dickcissels, I ended up spending a lot of time trying to find predators. Here’s another example: I tracked a fledgeling to a hole in the ground. I’d found a few birds that were underground before (which I can tell by the way the dirt messes with the signal, plus the fact that the strongest signal points to bare ground), but I never before found an actual hole. Because of this, I didn’t actually know what was taking these birds underground (Snake? Small mammal? Badger??). I decided to take advantage of this by placing one of the nest cameras we were using for another project at the entrance, to try and see what came out. Unfortunately, I never managed to find out, since the predator must have been scared off by the camera and used a different entrance.

Fig 2 - Dylan Smith.jpg

Camera set up on a burrow to try and figure out what ate one of my birds

I didn’t set out to track predators. For an REU (Research Experience for Undergraduates) project in Dr. Alice Boyle’s lab, I was trying to track Dickcissel fledgelings, to determine how they moved after leaving the nest, and to study their survival. Another researcher, Sarah Winnicki, was studying baby birds while they were in the nest, to see how Brown-headed Cowbird brood parasitism affected the hosts’ growth. Brood parasitism is a reproductive strategy in which, rather than making their own nest and caring for their own young, female cowbirds lay their eggs in the nests of other species (including Dickcissels) and force the host species to care for their young. Although this would seem like cowbirds are placing a burden on the hosts, and cowbirds have strong impacts on nest success in other systems, there isn’t much evidence that parasitism affects the chances of a nest fledging at least one young in our system. But does cowbird parasitism affect the birds after they leave the nest?

Fig 3 - Dylan Smith

One of my fledgelings perched in a plant. I didn’t even know they did that this young!

The plan was to obtain ten radio transmitters, which emit a beep ever couple seconds that can be heard using a receiver and antenna and attach these to Dickcissel nestlings before they leave the nest. I would attach half of the transmitters to birds from nests with cowbird parasitism, and half from nests without parasitism, to compare between the two. Then I could relocate them daily to see where they move and how long they survive. I would go back to each spot the next day and measure the habitat the bird was choosing. After two weeks, I would recapture the bird and remove the transmitter, both to save the bird from the hassle of carrying it around, and to allow me to reuse it a second time. This would allow me to track a total of twenty birds, ten with and ten without parasitism.

Fig 4 - Dylan Smith

Fledgeling with a brand new transmitter (the antenna sticking out of the back)

The challenging part of this study wasn’t really the actual tracking of the birds – that part is easy. Just wave an antenna around and find the spot where the beeping is loudest. The hard part is finding the birds in the first place. I needed to locate Dickcissel nests, and then I needed the babies in those nests to make it to fledging. Dickcissel nest success is naturally pretty low, so this is a bigger roadblock than it might seem. Few nests make it to hatching, and out of those that do, few of those make it to fledge age. And even if they do manage to fledge, the first four days out of the nest are the riskiest of all. Previous studies found that 70-90% of Dickcissel fledgelings don’t make it past four days. As for my study, a full half of my birds were eaten within a day of leaving the nest.

Fig 5 - Dylan Smith

Here I am tracking one of my fledgelings with an antenna. I always liked how cool this part looks.

If a bird made it the full planned tracking period of two weeks, then I needed to try to recapture the bird to remove the transmitter (since it was sized to fit on a recent fledgeling, not an adult). This proved much more difficult than I’d imagined it would be. The usual method to catch a specific bird involves setting up a net in its territory and playing a territorial song, to make the bird think there was an intruder. The bird would then fly over to investigate – right into the net. However, fledgelings don’t defend territories of their own, so this technique wouldn’t work. The only strategy we had was to track the bird to a patch of shrubs, set up several nets around the shrubs, then wade through bushes higher than my head to try and scare the bird into a net. We tried for several hours several days in a row, with no luck. We did capture it eventually, and I’ve never felt so accomplished in my life. I measured as many things as I could think to measure, and I let it go, feeling a little bit of pride that “my” bird had made it.

Release

“I measured as many things as I could think to measure, and I let it go, feeling a little bit of pride that ‘my’ bird had made it.”

Unfortunately, this was the only bird that made it. Out of the twenty birds I was planning on tracking, I only ended up with six. This was largely due to a severe drought on Konza this summer, which reduced the number of nesting attempts later on in the season (the time of season when Dickcissels normally do most of their nesting). I did see several juvenile Dickcissels being fed by parents, which means there were definitely many nests that we simply weren’t able to find in time. If I were to conduct a similar study again in the future, I would make a stronger effort to find nests early in the season, rather than expecting to find plenty later on.

Fig 6 - Dylan Smith

This was the only fledgeling that made it to two weeks after leaving the nest.

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