The Landscape of Fear - Research Update

February 13, 2017
By Justine Atkins, PhD Student, Princeton University
What happens to prey when there are no predators? This was the question on my mind when I arrived in Gorongosa National Park (GNP) to start my first field season last August. As a first-time visitor to Africa, I could not have asked for a more beautiful or special introduction to savanna ecosystems. But, there was one part of this uniqueness that I found especially interesting – the missing predators. 
Gorongosa’s wildlife populations declined sharply during and shortly after Mozambique’s long and brutal civil war. The lion population is still just a fraction of its previous size, and none of the other apex predators (like hyenas, leopards, and wild dogs) have come back yet. With a predator community that is still struggling to recover, how might prey populations in GNP differ from those in other African savannas where there are more of these large carnivores? I expected there to be less predation-related deaths, but as a long-time student of animal behavior, I was more interested in the effects of predator absence on the behavioral decisions of prey. 
In ecology, the behavioral impact of predators on prey is referred to as the ‘landscape of fear’. For small antelope like the bushbucks in Gorongosa, living in a landscape of fear means that you have to hide from predators or only forage at times when you know predators aren’t out hunting. You may also choose to live in areas where there are simply fewer predators, or where predators have less of an advantage. For example, if your main predator is a lion, which hunts by stalking and ambushing prey in open areas, then you may choose to avoid such areas. In doing so, you reduce your chances of being killed, but this comes at a cost: for bushbucks, they may miss out on eating the more nutritious plants that only grow in these areas. In this way, fear-driven interactions not only impact prey species but can also cause ‘snowball’ effects further down the food chain. 
A striking example of this phenomenon occurred after wolves were re-introduced in Yellowstone National Park. Elk began avoiding aspen thickets to evade wolves, resulting in a cascading effect: aspen stand sizes increased, beavers returned to places where they had previously had too few trees to eat, and beaver dam activity altered the landscape by raising the water table and flooding new areas.
If the presence of predators can have such a large impact on herbivore behavior and the environment, then it’s possible the absence of predators could have an equally significant effect on the GNP community. With all of this in mind, I set out to conduct an experiment to test whether the low predator numbers in GNP have turned the ‘landscape of fear’ into one of ‘fearlessness’ for one particular species, the small forest antelope, bushbuck (Tragelaphus scriptus). 
Veterinarian Louis Van Wyk helps stabilize a bushbuck as she wakes up and walks away after being collared - Photograph courtesy of Jen Guyton
Testing for ‘fear’ in animals involves trying to scare prey species using artificial scents and sounds to simulate the presence of predators. In Gorongosa, I wanted to see how bushbuck reacted to simulated presence of their main predators – big cats such as lions and leopards. Luckily for me, there is a commercially available, non-toxic, nitrogen-based fertilizer called ‘Silent Roar’ which consists of fertilizer pellets soaked in lion dung and was created for gardeners who want to scare the neighbor’s cat away from their flowerbeds. Carnivore urine was a little trickier, but thanks to some cunning research, we know that animals that eat meat produce a chemical called 2-phenylethylamine in their urine. This chemical elicits an innate fear response in prey species. Using standard large mammal capture-and-release techniques, we placed GPS collars on 12 bushbucks around GNP. We then placed the artificial carnivore scat (Silent Roar) and urine (diluted 2-phenylethylamine to mimic the concentration found in real carnivore urine) in particular locations within the home range of each bushbuck, and then played recordings of leopard calls from hidden speakers. Now, we’re analyzing the GPS data from the bushbuck collars to see if any of the antelope were scared into avoiding the areas where we placed the “predator” cues. 
The equipment set up for our ‘landscape of fear’ experiments: (a) We wanted to try and make our simulated predator calls sounds as realistic as possible, so we used a high-quality PA speaker (shown here) that was then camouflaged; (b) Small pellets of “Silent Roar”, which was used to simulate lion scat – they don’t look a lot like lion poop but they sure smelled like it!
Early results show that my scare tactics were successful, and we now have several other predator simulation experiments with more species planned for 2017. Understanding predator-prey interactions is especially important for Gorongosa because they may affect the ongoing restoration process and current predator re-introduction initiatives. From our ‘fear experiments’ in GNP, we may also be able to help managers in other systems understand, and potentially predict, prey species responses to predator return or removal. I’ll be writing more as the results come in. Stay tuned!
Top photograph - The capture-and-release process: This photo was taken just before we were about to release this female bushbuck after placing a GPS collar on her. The bushbucks are captured using anesthetic darts: once the anesthesia has taken effect, we use the blindfold to ensure the animal stays calm while we attach the collar and take measurements on their condition. We are also able to check the pregnancy status of females using a portable ultrasound machine. Once it’s time to release the bushbuck, we are able to reverse the anesthetic with a small IV injection and allow the animal to carry on its way.