Editorial “Developing a cartography of fear“
IN JANUARY 1995, grey wolves returned to Yellowstone National Park, almost 70 years after they had been exterminated by an overenthusiastic predator-control programme. Over the next two winters, 31 animals captured in Canada were released into the park, fitted with radio collars so that rangers could track their whereabouts. But not all eyes were on the wolves; John Laundre was more interested in their main prey, elk. The large deer had run amok in the wolf-free decades, causing serious damage to the park’s trees. He wanted to know how they would fare now that their old nemesis was back.
By the second year, the answer was obvious. In the parts of Yellowstone that the wolves hadn’t yet reached, female elk grazed peacefully while their calves gambolled around them. “It was a scene out of a Disney film,” says Laundre, an ecologist at the State University of New York at Oswego. But in areas the wolves had colonised, things were very different. The calves were pinned to the sides of their ever-wary mothers. “It was like looking at two different countries, one at war and one at peace,” he says.
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For Laundre, it was a light-bulb moment. He realised that wolves don’t just kill elk, they also change the deer’s behaviour without even lifting a claw. Their mere presence – perhaps their scent on the wind and tracks in the dirt – creates a perpetual state of apprehension in their prey. Seen through the eyes of an elk, the physical terrain is overlaid with a mental map of risk, complete with “mountains” where the odds of being eaten are high and they must be constantly vigilant, and “valleys” of relative safety where they can lower their guard. To describe this psychological environment, Laundre coined the term “landscape of fear”.
“In the eyes of an elk, the physical terrain is overlaid with a mental map of risk – a landscape of fear”
The concept seems simple but it subverts the dominant view in ecology – that predators only affect their prey by killing them. It also challenges the belief that most animals feel fear only in short bursts, like the sharp panic of a chase, while long-term psychological stress is something that only humans and other primates experience. With such emotions pushed aside, traditional ecological models have reduced predators and prey to little more than rolling marbles. “If one bumped into another, the second ball was dead,” says Laundre. The idea of adding psychology to the mix, especially a seemingly anthropomorphic emotion like fear, was anathema.
But times are changing. Ecologists are studying landscapes of fear in animals as diverse as wolves and elk, sharks and dugongs, spiders and grasshoppers. Time and again it has emerged that the greatest effect predators have upon their prey is not through slaughter, but intimidation. They can influence how successfully their potential victims feed, breed and raise their young, all without a single kill. And it doesn’t end there: these effects trickle through entire ecosystems, shaping the make-up of the local flora and even influencing the flow of nutrients through the soil. The implications are huge. Through the landscape of fear, predators can unwittingly remodel the physical landscape – just by being scary.
Laundre wasn’t the first to recognise the role of fear in ecology. Since the 1970s, studies had shown that predators can force prey to mount costly defences, such as moving into poorer habitats and being so relentlessly vigilant that they do not have the time to eat enough. But most of these experiments were small in scale and duration, and few looked at the lasting consequences of the choices made by prey. It was the advent of big, long-term studies in natural settings that addressed these failings and brought the importance of fear into sharp relief.
“The Yellowstone example is the first one that really smacked us in the face,” says Laundre. Before the wolves were reintroduced, ecologists correctly predicted how big their populations would become and how many elk they would kill. However, they greatly underestimated the effect on elk numbers. “They really just assumed that wolves would impact the elk by eating them,” says Scott Creel from Montana State University in Bozeman, whose findings in another corner of Yellowstone showed how wrong that idea was.
Creel’s studies between 2002 and 2006 revealed that when wolves were around, elk more than doubled the time they spent on watch. They also moved away from the grassy fields they prefer into wooded areas that offer more protection but less food. These changes slashed the amount of energy they were getting by around a quarter – with dire consequences. When Creel saw a dramatic decline in calf numbers, he knew the wolves were not directly responsible because they rarely kill young elk. Measuring levels of progesterone – a hormone that spikes during pregnancy – in stool samples from 1500 female elk, he found that they were far lower in areas where wolves lived. Many elk were in such poor condition they didn’t have enough energy to reproduce ().
Today the population stands at just over 6000, down from 19,000 in the elk’s wolf-free heyday. Its downfall has been Yellowstone’s gain. In 2010, William Ripple from Oregon State University in Corvallis reported that since the wolves’ comeback, trees including aspen, willow and cottonwoods have bounced back. More saplings survive, now that intimidated elk are less likely to nibble their lower branches, and the older trees have doubled or even tripled in height (). Taller trees provide more wood for beavers, whose populations have increased from just one colony in 1996 to a dozen in 2009 (see charts). By damming rivers they in turn create ideal habitats for birds, amphibians, fish and more, so their presence is likely to alter the face of Yellowstone even further.
These sorts of knock-on effects, known as trophic cascades, are a familiar part of ecology but, again, they have traditionally been understood as a direct consequence of predation. Could the landscape of fear really affect entire food webs simply by changing the behaviour of prey? Doubters argue that some other factor, such as climate change, might explain the changing face of Yellowstone. But evidence that fear can shape ecosystems is mounting. In Western Australia’s Shark Bay, for example, the lush seagrass meadows that grow in shallow waters probably wouldn’t exist if it weren’t for the presence of predators. In the absence of tiger sharks, dugongs graze them, digging for nutritious roots with their muscular lips. But between September and May, when sharks are around, the dugongs retreat to deeper waters, and when they do venture to the meadow’s edge to feed they keep their heads up and take only the topmost leaves (). The mere presence of sharks not only changes the distribution of dugongs in the bay, it also prevents them from decimating the seagrass ecosystem.
Such examples from nature have been enough to persuade some of the importance of fear in ecology, but to convince the sceptics experiments were needed. In particular, scientists needed to devise clever ways of exposing animals to the threat of predators, while completely removing the chances of a kill. Liana Zanette from the University of Western Ontario in Canada has been doing just that. Through painstaking surveys, she first documented everything that attacked song sparrow chicks at her study site in the Gulf Islands off the western coast of Canada. She then introduced countermeasures to protect the nests: electric fences to keep out raccoons, and wire nets to keep crows, ravens and owls at bay while allowing safe passage to the smaller sparrow parents. Having ensured that the fledglings would not be killed, Zanette bathed half the sparrows in sounds of danger, by playing recordings of predators from nearby speakers.
The results, published in 2011, were astonishing. Sparrows that regularly heard predator sounds raised 40 per cent fewer chicks each year than those that heard the noises of harmless animals. They laid fewer eggs. Those that were laid were lighter and more frequently failed to hatch, partly because the skittish mothers spent less time incubating them. And the chicks that did hatch were more likely to die of starvation, because their fearful parents brought less food to the nest (). “It was the first study to unambiguously show that fear can affect populations,” says Zanette.
“Sparrows that regularly heard predator sounds raised 40 per cent fewer chicks each year”
Last year, Dror Hawlena and Oswald Schmitz from Yale University showed that the effects of fear can cascade further. They raised grasshoppers in large outdoor cages and released spiders into half of them. The arachnids could not kill because Hawlena had glued their mouthparts shut, but the grasshoppers didn’t know that. In the spiders’ presence, the metabolic rate of stressed individuals shot up by 40 per cent, increasing their need for energy. The team found the grasshoppers paid this debt by changing their diet, eating more carbohydrate-rich goldenrod plants and fewer protein-rich grasses. Protein is important for growth and reproduction but with the looming possibility of predation, the grasshoppers downplayed these future needs in favour of a quick energy fix. This altered menu changed the chemical composition of their bodies, increasing the ratio of carbon to nitrogen by 4 per cent – a small difference but an important one. When dead grasshoppers were buried together with dead plants in pots of soil, the fearful, carbon-rich animals made inferior fertiliser ().
“It’s a really important study,” says Creel. Without doing a thing, the spiders were changing natural cycles of nutrients in the soil. If the same applies in other environments, predators could shape the way nutrients travel across the entire landscape.
Although ecologists have long appreciated that species on different tiers of a food web influence each other, these fear-centric studies show that connections are far more intricate than they suspected. In the orthodox view, the survival of prey animals depends both on not being eaten by animals further up the food chain, and on consuming resources down the chain. If elk or sparrows raise fewer young, the orthodox explanations are that predators eat them, or that food supplies are low. But add fear to the mix and things become more complex. Just having predators in the area changes the behaviour of prey, with big impacts on their survival and reproduction. Likewise, the standard explanation for why herbivores do not overgraze their food supply is that predators keep their numbers in check. The alternative, brought to you by the landscape of fear, is that the presence of predators simply keeps prey away from certain areas, creating refuges where vegetation thrives. “Why is the world green? It’s because of fear,” says Laundre. “This has the potential to really change our world view of how ecology works.”
The landscape of fear is not just a lens for seeing the natural world – it can also be a tool for conserving it. For a start, conservationists can visualise the landscape by watching the reactions of prey, and use it to deduce the whereabouts of predators, even the most elusive ones.
Snow leopards, for example, are extremely hard to find in the wild. So Joel Brown at the University of Illinois at Chicago didn’t bother – he simply looked for the reactions of their prey. Blue sheep and the Himalayan tahr are not only conspicuous and easily tracked, but are much better at spotting snow leopards than any ecologist. When they do so, they gather in larger groups and spend more time looking around than grazing. By watching these reactions, Brown’s team could measure the density of snow leopards, which they later confirmed by finding droppings and paw prints. “We became the first snow leopard project whose goal was to see no snow leopards,” he says.
Lines of escape
Conservationists could use similar techniques to map the rise and fall of populations of predators. Alternatively, they could study endangered prey species, which is what Burt Kotler at the Ben-Gurion University of the Negev has done in Israel’s Ein Avdat National Park. There Nubian ibex roam through the desert canyons seemingly habituated to tourists – but Kostler found otherwise. On weekends, when most tourists visit the park, the ibex left far more food behind in their feeding trays than on quieter weekdays (). By measuring this simple indicator of risk perception, Kotler was able to map the ibex’s landscape of fear, revealing, for example, that they are particularly spooked by the appearance of tourists on slopes above them, cutting off their lines of escape.
Studies like this could help ecologists make better decisions about safeguarding vulnerable animals and planning reintroduction efforts. Thinking about the landscape of fear might, for example, assist conservation groups trying to return bighorn sheep to parts of the south-western US. In the bighorn’s former range, vegetation has grown significantly and now easily conceals stalking predators. “They bring the sheep in, and mountain lions kill them, to the point where they think they need to control the lions,” says Laundre. He suspects that simply trimming the shrubs along corridors connecting mountain ridges would make a big difference, allowing the sheep to let down their guard and move freely.
Landscapes of fear may be psychological, but for prey they are as real as their physical counterparts. “Every step an animal takes out there happens in a changing risk environment,” says Brown. “That topography exists in the mind of the animal.” This realisation has big implications for how we understand ecology. Indeed, Laundre believes the future of conservation lies in managing these metaphysical landscapes – keeping just the right levels of risky and safe habitats to maintain stable populations of both predator and prey. “This could be one of the most valuable tools we have in conservation ecology,” he says.
This article appeared in print under the headline “Scared to death”
