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Predators shape ecosystems more by fear than killing

Contrary to what researchers had expected, snails flourished when there were more of their predators, mud crabs, around. Image credit: Creative Commons/ Pseudopanax

A ground-breaking study has caused a dramatic rethink of the process by which predators control ecosystems, and it’s turning classic ecology on its head.

In the gleaming salt marshes of Georgia’s Sapelo Island, US, Dr John Griffin was unleashing terror. An ecologist, he had emptied an army of mud crabs into the sediment to see what would happen to their prey.

Dr Griffin, a lecturer at Swansea University in the UK, had his eye on the little marsh periwinkles. These snails like to feast on the leaves of the green and precious cordgrass that dominates the marshes. Mud crabs ought to gobble up myriads of snails — and give the grasses a reprieve.

The Issue

Human activity is causing species to go extinct at between 1 000 and 10 000 times the natural extinction rate, according to the World Wide Fund For Nature (WWF).

That's because by polluting rivers, cutting down forests and covering huge tracts of land in tarmac and concrete, humans are using 25 % more resources than the planet can sustain, the WWF believes.

The loss of an entire species is a tragedy in itself, but it can also have far-reaching consequences on an ecosystem, such as reducing the availability of food and fresh water for other species, including humans.

It is classic ecology you may have been taught at school: predator eats prey, prey eats plants, so more predators mean more plants. What happened, though, did not fit the models: the snails actually flourished under the assault of the mud crabs — and the vivid green of the marshes became dotted with circles of dead grass.

The result of the experiment was unexpected, and the explanation is profound. It challenges assumptions about how species respond to each other and it may mean that we have underestimated their ability to cope with changes in the environment.

Dr Griffin’s work, conducted with Brian Silliman, a marine ecologist at Duke University in the United States, is part of a broader swathe of research that is uncovering previously unknown ways in which ecosystems respond to change.

This field is showing that ‘ecological communities may be far more resilient to environmental changes and damages than previously thought’, said Professor Oswald Schmitz, a population ecologist at Yale University in the US, whose pioneering studies in the field inspired Dr Griffin.

‘It has caused some ecologists even to question the likelihood of the portended extinction crisis,’ adds Prof. Schmitz, referring to warnings that human activity is causing a sixth mass extinction. Other scientists, however, including Dr Griffin, think that the worldwide march of habitat destruction is enough to overwhelm this new-found resilience.

Dr Griffin, who is funded through the EU’s Marie Skłodowska-Curie actions, explains what happened in the marsh. To escape the mud crabs, some snails crept upwards, away from the lower stems and the mud where they spent a lot of time eating nutritious algae, and into the giddy heights of the leaves, where they feasted in safety. The extra leaf consumption damaged the plants  — and hence the withering grass.

Knock-on effects

Viewing snails as docile prey, fixed and identical in their responses, means you don’t spot tactics such as these. Instead, says Dr Griffin, we can view prey as more in charge of their destiny. They respond to trouble in a variety of ways, finding new spaces and new foods. The knock-on effects can cascade through the system and even affect the nutrients in the soil, he says.

Dr Griffin then travelled to Tibet where, in an Alpine meadow, he and ecologists Chuan Zhao and Shucun Sun from the Chengdu Institute of Biology in China, uncovered a similar story.

In the meadows, flanked by snowy mountains and dotted with brilliantly coloured flowers in the spring, earthworms tunnel through the soil, leaving a healthy environment for grass roots. Predacious beetles eat the earthworms, so theory would predict that releasing more beetles onto the soil would diminish the number of earthworms and weaken the grass.

In fact, the grass thrived because the earthworms burrowed deeper, where the plants benefited even more from their aerating activities.

‘It advocates for a precautionary approach for biodiversity conservation.’

Dr John Griffin, Swansea University, UK

Theorists predicted in the 1990s that the ways in which organisms change their behaviour may shape ecosystems more powerfully than previously thought. But scientists in the field have been slower to accept the role of these interactions, known as Trait-Mediated Indirect Interactions (TMIIs).

Much of TMII research has shown that delicate changes in behaviour can enable prey to shift geographically, seeking out new and safer habitats, with knock-on effects. Dr Griffin has added the unexpected discovery that they don’t necessarily have to undertake dangerous treks into new territory — they can move upwards or downwards instead, and that shimmying up stalks or squeezing deeper into the ground can cause a complete reversal of their normal effects on plants. 

Now, he plans to use his grant to explore marine ecosystems and to search for European examples.

If prey are more flexible than we thought, the converse of this is that predators exert much more complicated effects in ecosystems.

Until now, it was thought that they were one-trick acts: gobbling prey, keeping the numbers down. They do keep the numbers down but the amount they actually consume is often too small to account for it.

‘It’s actually exceptional for a predator to control a population by eating it,’ says Prof. Schmitz.


Predators have other tools, of which terror may be the most potent. Terror drives prey into less nutritious areas, and reduces fertility through stress.

There’s a beautiful example from Yellowstone National Park in Wyoming, US, where grey wolves were introduced in 1995. Wolves hunt elk, but elk populations have now diminished far below the number that could be accounted for by what wolves consume.

Viewed from the TMII perspective, scientists can see that wolves have dramatically changed the elk world. Elk have shifted to less accessible parts of the park, adopted a new diet and had fewer babies — and these changes are altering the park’s ecosystem.

Fear of being eaten, rather than being eaten itself, is shaping the environment.

Since our greatest planetary threat is said by many experts to be the loss of biodiversity, what perspective do TMIIs give us?

Ecologists are divided. Some point out that, if a predator goes extinct, the consequences may ripple far beyond what it used to eat.

Over-fishing is removing top predators from our oceans and they may have been influencing the food web in unknown ways — perhaps through the chemicals they secreted, or even the sounds they made.

‘It advocates for a precautionary approach for biodiversity conservation,’ says Dr Griffin. ‘The deletion of species can have strong unpredictable effects.’

TMIIs make it harder to predict what will happen, adds Dr Rebecca Morris, a community ecologist at Oxford University who did not participate in the study. ‘They add another route by which extinctions can cascade through a system, but … the only generalisation we can make at present is that the consequences of species loss may have far wider ramifications than we can predict.’

In some cases, she adds, TMIIs ‘may well increase the stability of ecological systems’.

For Prof. Schmitz at Yale, this is a vital point. ‘The ultimate message for conservation is that it gives much hope that species can keep pace with human-caused environmental change, to the extent that humans do not push species beyond their genetic capacities to change.’

But his optimism comes with a proviso: if you are trying to conserve a species, you have to see them as individuals as well. You don’t know which ones possess the key characteristics for surviving change so you have to conserve a range of traits and therefore individuals. You can’t just protect a typical representative.

‘It’s akin to having a diverse portfolio of stocks or bonds,’ he says.

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