Field Notes: Risky Business

Humans are everywhere! In fact, it is likely that there is not a single place on earth’s surface that humans have not touched. Because of this, all animals face human interaction to some degree, but little is known about how we may be changing their behavior (think actions), morphology (think body and bones) and physiology (think hormones). This topic has always interested me. When I first started field research in 2016 as an assistant researcher for a long-term study on the California ground squirrel (Otospermophilus beecheyi) in Briones Regional Park (Contra Costa County, CA), I noticed that squirrels who lived in areas of higher human activity were different from those living in areas of lower human activity. They would allow humans to approach closer, they appeared to be more social with each other (think greeting and playing — very similar to how puppies greet and play), and they seemed to be hanging out above ground rather than in their underground burrows more often. What was even cooler was these noticeable differences occurred at a very small spatial scale – in fact, there were differences in behavior between squirrels living a couple hundred meters from each other as opposed to miles! This could mean that even animals living very close to each other could behave different depending on what is occurring in their immediate surrounding environment. This sparked so many questions in my young scientist brain like: Did some squirrels actively choose to live near humans? Was there a benefit? Thus, I have focused my research on exploring how human presence in natural environments impact behavior of wildlife, particularly focusing on how humans’ impact risk-taking behaviors in prey species (behaviors like allowing predators to get close or eating in a scary place).


Figure 1. California ground squirrels (Otospermophilus beecheyi) gathering around a burrow. PC: Dr. Jennifer E. Smith, Mills College

For my interests, I have continued to study the California ground squirrel, which are semi-fossorial mammals, meaning they live both above- and below-ground (Fig. 1)[1]. Many people view ground squirrels as pests because their underground homes, also knowns as burrows, have been blamed for many things from ruining gardens to damaging the structural integrity of buildings. However, what many people do not realize is that these squirrels play an important role in our ecosystem. Not only are they a main prey source for multiple predators (including coyotes, birds of prey and rattlesnakes, Fig. 2 & 3), they also are ecosystem engineers, which means they provide habitat for other species who rely on their burrows for refuge, including the endangered burrowing owl (Athene cunicularia hypugaea, [3]).


Figure 2. Ground squirrel, named Pi, faces off against a rattlesnake. PC: Dr. Jennifer E. Smith, Mills College

Figure 3. Two ground squirrels, Capital_K and Alpha, face off against a rattlesnake using tactics such as tail-flagging to distract the snake and alarm calling to warn others of the nearby predator. PC: Dr. Jennifer E. Smith

My team and I (aka. Team Squirrel, Fig. 4) set out to discover whether squirrels were fearful of humans and if they viewed them as a potential threat. Our experiment explored where ground squirrels perceive risk (or areas that squirrels viewed as “scary”) in their environment and other factors that might contribute to that perception. For example, did squirrels avoid certain areas that may give them an idea of where a predator would be (like hiding in a bush). We strategically set out plastic plates mixed with millet, a seed naturally found in the environment (birds also love it!), and sand (Fig. 5). Think of it like a food puzzle similar to what we give our dogs and cats – squirrels had to dig through the sand to find millet seeds. We set out 100 plates prior to squirrels emerging from their burrows at the beginning of the day (around 8am) and allowed them to sift through and eat at the plates for 4 hours. We then collected the plates, sieved the millet from the sand, and looked at how much millet they were able to find and eat. This provided us with something known as giving up density (GUD) which is almost exactly what it sounds like and is a useful tool to explore perceived risk by animals across a landscape based on how much food animals will eat. Theoretically an animal will eat less food if perceived risk is high and vice versa [1]. This allowed us to explore the factors surrounding plates with a lot of food left to try and understand what made that area riskier, or “scary”, to squirrels than areas where they ate more food from the plates. We could then map out squirrels “landscape of fear” (where they felt safe vs. where they were fearful).


Figure 4. Team Squirrel poses on a hike after a morning of observations at Briones Regional Park, Contra Costa County, CA. PC: Haifa Algabri, Mills College

In 2019, we found from our GUD that squirrels preferred to eat in areas of higher human activity. This means that squirrels actually felt safer around humans, but why? It may be that squirrels living in areas of higher human activity do not encounter predators often, which may be because humans are scaring predators away. Thus, if humans are around that means there are fewer predators and a very safe space to eat. We also found squirrels had particular habitat features that made them feel safer and eat more. This included being near burrows and in areas of low vegetation. Both of these factors are likely preferred in order to lower their chance of being predated upon. In lower vegetation, squirrels are able to see their surroundings better and any potential nearby predators. If they are able to spot a predator, then being nearby a burrow provides an easy escape in case the predator decides to pursue them.


Figure 5. Ground squirrel, Peep, foraging at experimental giving-up density plate filled with millet mixed with sand. PC: Chelsea Ortiz-Jimenez, UCD

These findings were super exciting to Team Squirrel, and we really wanted to continue this experiment across years to see if squirrels maintained the same preferences for safety from year to year. However, a few months prior to our 2020 field season, COVID-19 lead to the country declaring a “stay at home” order to keep citizens healthy. Briones Regional Park’s trails remained open, but gatherings within the park were restricted. This caused a huge shift in human activity within our study site. Luckily, we were still able to conduct research and take advantage of the natural human activity shift presented within our field site.

In 2020, we reran the experiment and found a significant change in the landscape of fear; however, there was not a significant change in squirrels overall safety preferences. Squirrels still preferred to eat in areas of higher human activity, closer to their burrows and in low vegetation, but because the shift of human presence occurred within the site, we saw a shift occur with the landscape of fear! Squirrels’ safety areas moved to where humans were most active – which was now closer to trails and very different from the previous year.

We’re finding humans really do have an impact on wildlife behavior and not necessarily in a negative way. At our field site, squirrels are not fed by humans nor do they benefit greatly from human foods. It is likely that humans rather provide this population of ground squirrels a safe refuge from predators who may be avoiding places and times when humans are present. I plan to continue this research exploring how humans are impacting predator-prey relationships and other trade-offs squirrels may be facing when living in areas of high human activity because I just can’t keep away from these cool ground squirrels!

Chelsea Ortiz-Jimenez is a 3rd year PhD candidate in the Animal Behavior Graduate Group at UC Davis in Dr. Andy Sih’s lab, co-advised by Dr. Jennifer E. Smith at Mills College. She has been working on the ground squirrel system since 2016, which has inspired her research interest exploring the impacts of human presence on wildlife behavior.

References:

[1] Brown, J. S. (1988). Patch use as an indicator of habitat preference, predation risk, and competition. Behavioral ecology and sociobiology, 22(1), 37-47

[2] Smith, J. E., Long, D. J., Russell, I. D., Newcomb, K. L., & Muñoz, V. D. (2016). Otospermophilus beecheyi (Rodentia: Sciuridae). Mammalian Species, 48(939), 91-108.

[3] Swaisgood, R. R., Montagne, J. P., Lenihan, C. M., Wisinski, C. L., Nordstrom, L. A., & Shier, D. M. (2019). Capturing pests and releasing ecosystem engineers: translocation of common but diminished species to re‐establish ecological roles. Animal Conservation, 22(6), 600-610.

Main Image Credit: Wade Tregaskis

[Edited by Josie Hubbard and Maggie Creamer]

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