What makes an urban bird?

This blog post is provided by Jenny Ouyang and tells the #StoryBehindthePaper for the paper “Changes in the rearing environment cause reorganization of molecular networks associated with DNA methylation”, which was recently published in Journal of Animal Ecology. In their paper they explore the impact of urbanisation on DNA methylation in young birds.

Urbanization is one of the most prevailing forms of habitat change, causing biodiversity loss through local extinction processes. Urban expansion is expected to impact a quarter of all endangered species in the next decade. Nevertheless, individuals vary in their response to these drastic changes, with some unable to occupy these new habitats while others persist and thrive.

This difference in the ability to adapt has promoted the study of phenotypic traits that allow individuals to inhabit urban areas. A key trait that can facilitate adaptation is the degree at which animals respond to stressors. This stress response, which includes elevation of baseline circulating concentrations of glucocorticoids, has a heritable component and exhibits individual variation. Epigenetic mechanisms can alter organism function without changes in the DNA sequence, representing a possible mechanism for the observed response to urban stressors.

Female house wren at an urban site (Caughlin Ranch) with a caterpillar ready to feed its offspring in the nest box. Photo credit: Michael Dale

In a recent paper in the Journal of Animal Ecology, we explored the contribution of DNA methylation towards observed urban phenotypes. When house wren parents bred in nestboxes across a network of urban and rural field sites, we moved their offspring across and within sites to disentangle the contribution of genetic and plastic mechanisms to the glucocorticoid phenotype. This type of experiment is an inter- and intra-environmental cross-foster to analyze the contribution of DNA methylation to early-life phenotypic variation.

Young house wrens were moved within and among urban and rural sites to investigate the contribution

We observed age-related patterns in offspring methylation, indicating developmental effects of the rearing environment. We further discovered different networks of genes were important at hatching compared to fledging. For example, we found several genes involved in auditory response and learning networks were differentially methylated across experimental treatments. Analyses showed that cellular respiration genes were differentially expressed at hatching and behavioral and metabolism genes were differentially expressed at fledgling. Lastly, hyper-methylation of a single gene (CNTNAP2) is associated with decreased glucocorticoid levels and the rearing environment. Urban house wrens appear to be hypermethylated during hatching compared to their rural counterparts. As offspring aged, wrens that stayed in the same environment increased methylation frequencies but wrens that moved between environments did not show a similar increase. These age and environment-related changes in methylation frequencies suggest that the urban phenotype is a result of both genetic and environmental factors.

Adult house wren at a rural riparian habitat. Photo credit: Chris Halsch.

Our findings are suggestive that DNA methylation can shape the physiological phenotype and is empirical evidence for a mechanism by which individuals thrive in changing environments. Together, this work provides an unprecedented empirical system that we have leveraged to explore the influence of both genetics and environment on DNA methylation. DNA methylation may be a mechanism by which individuals adjust to novel environments during their lifespan. Understanding the genetic and environmental basis of local adaptation is important in predicting species’ responses to an urbanizing world.

Author bio

Jenny Ouyang – I am an integrative physiologist at the University of Nevada, Reno. I am interested in how animals physiologically adapt to changing environmental conditions.

Read the paper

Read the full paper here: von Holdt, B. M., Kartzinel, R. Y., van Oers, K., Verhoeven, K. J. F., & Ouyang, J. Q. (2023). Changes in the rearing environment cause reorganization of molecular networks associated with DNA methylation. Journal of Animal Ecology, 00, 1– 17. https://doi.org/10.1111/1365-2656.13878

Beyond simple habituation: Anthropogenic habitats influence the escape behavior of spur-winged lapwings in response to both human and non-human threats

This blog post is provided by Bar-Ziv Michael, Sofer Aran, Gorovoy Adel and Spiegel Orr and tells the #StoryBehindthePaper for the paper “Beyond simple habituation: Anthropogenic habitats influence the escape behavior of spur-winged lapwings in response to both human and non-human threats“, which was recently published in Journal of Animal Ecology. In their paper they use a unique “Jack-Truck” to simulate a jackal predator, and explore how lapwings respond to novel predators and humans.

לחצו כאן בשביל הבלוג בשפה העברית

Spur-winged lapwings (Vanellus spinosus) are monogamous birds that tend to stay with their partner all year round. During the breeding season they guard their nest and chicks with intimidating calls, attacking everything that get close with sharp spurs located on their wings. This species is considered to be one of the most common waders in Israel, and can be found in a variety of habitats, including natural habitats, as well as dense cities. This fact is quite surprising, considering that wader populations are declining worldwide due to the fact that they nest on the ground. Natural habitats across the world are being destroyed to make way for human needs, which in turn negatively affect a large number of species that cannot cope with the changes. Lapwings, on the other hand, not only represent a growing population, but they are also found to be able to nest and raise their chicks into adulthood in parks and even next to highways.

A couple of Spur-winged lapwings (Vanellus spinosus) in a built-up area. Lapwings occupy various settlements in the Harod Valley (north-east of Israel), and we explored how living in these habitats affects their escape behavior (Photo: Avichai Ran)

While some lapwings prefer to live next to human settlements, not all of them do. Most of the lapwings stay in more natural areas with fewer encounters with humans. Wild animals that live in proximity to humans usually present a bolder set of behaviors, which differ from populations of the same species that live in a more natural habitat. Those bolder responses can be a result of fear reduction toward humans (in other words, habituation to an urban environments), or alternatively present a larger effect that the urban environment creates (for example individuals with bolder personality reside in more urban settings).

A spur-winged lapwing in the town of Beit-She’an, keeping calm in face of passing pedestrians. Habituation to humans may affect their escape behavior and flight initiation distance (FID). (Photo: Avichai Ran)

A simple and well-known method to test boldness in field conditions is testing the animal’s flight initiation distance behaviour (or FID). Generally, animals that escape too early from an approaching threat will not be able to fully exploit their environment, while on the other hand those that are escaping too late might be at risk of getting caught by a predator. The behaviours animals present after their initial escapes are important as well, because more lethal predators may require a faster reaction, fleeing further away and finding a place to hide. Different predators also require different escape strategies, and while with one type of threat it is worthwhile escaping fast and far, in others it can be a burden. Those strategies can also differ between habitat types, for example, in urban settings individuals that are too scared and will flee from every person passing by, won’t be able to exploit this habitat properly and might prefer to forage in other areas.

A golden jackal (Canis aureus), one of the main predators for lapwings and their nests in the natural and agricultural habitats. We simulated an approaching jackal to generalize lapwings’ response beyond habituation to humans. (Photo: Michael Bar-Ziv)

In a recent paper in the Journal of Animal Ecology, we tested the escape behaviour of spur-winged lapwings. More specifically, we first looked at their flight initiation distance, their mode of escaping (by foot or flight), and finally what distance they fled. We tested those behaviors between three habitat types (human-dominated, water ponds, and fields), and compared them to two kinds of approaching predators (a human and a jackal). While humans are abundant in urban settings, jackals tend to be found in natural environments. Jackals also prey on lapwing nests, chicks, and potentially also on the adults. To mimic an approaching jackal, we used a taxidermy of a young jackal mounted on top of a camouflaged, off-road remotely controlled vehicle (named “Jack-Truck”). To find lapwings in the different environments, we searched for them while driving. We choose this strategy because lapwings tend to be less alert to driving vehicles, which made it easy to notice them without disturbing them. Once a lapwing was spotted, they were approached by a human, or a jackal and the escape sequences mentioned above were recorded.

Assembling the “Jack-Truck”, a jackal model used to simulate an approaching jackal. We used this Jack-Truck to determine if lapwings within settlements are merely more habituated to humans, or whether they are generally bolder in face of an approaching predator (Photo: Assaf Uzan).

The purpose of this experiment was to understand 1) if individuals found in urban setting show a general bolder response to approaching threats when compared to other habitats? And 2) if so, does this bolder response derive from simple habituation to humans, or does it represent a larger phenomenon (such as human settlements attracting generally bolder individuals)? If lapwings showed a stronger reaction to the jackal compared to a human in human-dominated environments it might hint towards habituation, because they were more afraid of a novel predator. On the other hand, having the same reaction to both predator types might suggest a deeper effect those habitats have over these animals.

Examining our first question, we found that lapwings from human-dominated habitats were bolder in most of the sequences of the escaping behavior. First, as expected, they presented a shorter FID when approached. Secondly, even after escaping they still presented bolder behaviors by fleeing to a shorter distance and more likely to escape by running (rather than flying). Interestingly, when considering our second question, we found that lapwings tested in human-dominant habitats presented a bolder respond to both a human as well as a jackal approaching. Those results show that lapwings not only present a bolder behavior in human settlements, but more importantly, it shows that habituation to humans cannot be the only explanation for the bolder response.

A group of spur-winged lapwings gathering near a construction site next to the town of Beit-She’an (Photo: Michael Bar-Ziv)

Those results can give us a hint of the effects human disturbance have on animals. Our paper shows that some individuals can become accustomed to human settlements, but it has a cost. To do so, they will need to reduce their fear response. This can be a dangerous strategy, because while most people will not try to harm them, once a more lethal predator approaches them, it could be more difficult for them to avoid this situation. In a fast-changing world that is becoming more urbanized, findings like these are essential for understanding the impact human-development has on wildlife populations and communities, even in species that at a first glance appear more resilient to those changes.

Read the paper

Read the full paper here: Bar-Ziv, M., Sofer, A., Gorovoy, A., & Spiegel, O. (2022). Beyond simple habituation: Anthropogenic habitats influence the escape behaviour of spur-winged lapwings in response to both human and non-human threats. Journal of Animal Ecology, 00, 1– 13. https://doi.org/10.1111/1365-2656.13858

Studying Abroad With A Bahamian Coastal Fish

This blog post tells the #StoryBehindThePaper from the perspective of one author, Matt Jenkins, for the article “Natural and anthropogenic sources of habitat variation influence exploration behaviour, stress response and brain morphology in a coastal fish” by Matt Jenkins, Jack Cummings, Alex Cabe, Kaj Hulthén, Nils Peterson, and Brian Langerhans, which was recently published in the Journal of Animal Ecology.
Matt Jenkins and incoming waves at Red Bays, Andros Island, The Bahamas (Photo credit: Alex Cabe).

As the human population continuously grows and cities become more common throughout the landscape, it is becoming increasingly important to study the effects of urban phenomena on the organisms inhabiting these modified environments. Human-induced habitat change has repeatedly caused behavioral and evolutionary trait shifts in organisms that persist in the Anthropocene, but we are still in the early days of understanding the causes and consequences of these shifts.

My part in this study began during the spring of my junior year at NC State University. With the fortunate experiences of already participating in several urban ecological studies as an undergrad, I discovered my passion for studying urbanized ecosystems. I was searching for ways to gain more experience in this field when I happened to notice a flyer one day as I was walking to class. Something on a bulletin board caught my attention: a research-centered study abroad trip to Andros Island in The Bahamas, led by Drs. Brian Langerhans and Nils Peterson. Based on the information provided on the flyer, it seemed the program involved group projects where students designed and carried out their own research project on the island with the goal of publishing their findings. Taking courses and conducting research all while staying on an island paradise? I couldn’t apply fast enough and had my application submitted that evening. A few weeks later I received an email from the study abroad office letting me know that I had been selected to attend.

The end of May quickly arrived, and it was time to depart for Andros. This would be my first time both flying alone and internationally. All went smoothly, and everyone on the course met in Nassau, The Bahamas to board the small propeller plane to Andros.

We soon had our first course lecture of the trip preparing us for what to expect during our time on Andros. After an amazing first week exploring the island, learning research techniques, eating local cuisine, and snorkeling along the barrier reef, my group got to work finalizing our project design, writing a research proposal, and presenting our plans to our classmates and professors. With my “teammates” Alex Cabe and John Cummings (co-authors), we decided to examine how ecosystem fragmentation and habitat complexity might affect the exploration behavior, stress response, and brain morphology of Gambusia hubbsi, the Bahamas mosquitofish, that reside in tidal creeks. During the 1960s and 70s, roads were constructed throughout the island, resulting in the fragmentation of some of these creeks, cutting off native species from the ocean and resulting in strong ecological change. Bahamas mosquitofish is a resilient species that has persisted in these altered environments and are abundant in many bodies of water on the island, making them a good model for testing adaptive shifts resulting from habitat change.

Our first day of field work was one of the biggest wake-up calls I have ever experienced. When one thinks of The Bahamas, your first thought is probably of white sandy beaches, fancy resorts, and crystal clear water, and while parts of the island certainly do look like that, it was not the case where we were on Day 1. Our first field site greeted us with temperatures in the high 90s, jagged rocks everywhere, the relentless biting of “doctor flies,” and a ubiquitous plant called poison wood (which you can tell by the name, was not a fun time). But with positive attitudes and hard work our team quickly got into a routine and our field work got smoother and smoother. It was actually the harsh field conditions that really brought us closer together and gave us some hilarious stories, like finding an abandoned bar to set up our behavioral assays beside an unfragmented tidal creek, and having plenty of interesting interactions with local people.

Our hard work paid off: after collecting and examining 356 mosquitofish from 7 tidal creeks (4 unfragmented and 3 fragmented), we found that not only has natural variation in habitat complexity resulted in several phenotypic shifts that point to intriguing future directions, but perhaps more surprising was that human-caused habitat modification has inadvertently led to changes in how a native animal interacts with and responds to its environment: Bahamas mosquitofish in fragmented tidal creeks showed greater exploratory behavior, a stronger stress response, and a smaller telencephalon (part of the brain most responsible for fear-related learning and spatial memory). All of these changes may represent adaptive shifts in response to the reduced predation pressure and tidal dynamics caused by fragmentation.

So, an undergraduate study-abroad experience led to this study in Journal of Animal Ecology, but it also solidified my passion for conducting urban ecological research and my desire to pursue this work in graduate school and eventually become a professor in this field. In the spring of 2019, I was fortunate enough to begin my Masters research with Dr. Langerhans where I am currently examining another major effect of human activities on native animals: artificial light at night. The findings of this study taught me that human actions can alter diverse types of animal traits in a relatively short time frame, and we need to better understand both how predictable these shifts might be and what sorts of ecological and evolutionary consequences result from the trait changes.

Read the paper

Read the full paper here: Jenkins, M.R., Cummings, J.M., Cabe, A.R., Hulthén, K., Peterson, M.N. and Langerhans, R.B. (2021), Natural and anthropogenic sources of habitat variation influence exploration behaviour, stress response, and brain morphology in a coastal fish. J Anim Ecol. Accepted Author Manuscript. https://doi.org/10.1111/1365-2656.13557

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.


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.


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.

Camera site

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.


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.


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


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