Australasian Science Magazine

Scientists could never have justified dumping more than 500,000 tonnes of methane into the ocean to study the effects of climate change on deep-sea habitats, but they didn’t have to – Deepwater Horizon did it for them.

By Shanta Barley & Jessica Meeuwig

Ecologists are treating oil spills, species invasions and other environmental calamities as natural experiments on a scale that could never be attained by normal laboratory or field studies.

Since the 1940s humans have detonated more than 2000 atomic bombs. We have cut down more than one-third of our tropical forests. We have transformed the humble chicken into an unlikely avian superstar: its bones may become the “type fossil” for future geologists studying the Anthropocene. We have effortlessly wiped out the apex predators that we once worshipped, and conferred on ourselves alarming names such as “superpredator” to underline our strange superpowers when it comes to eating other animals to extinction.

We have nevertheless failed spectacularly to anticipate how our ecological meddling has altered the planet. The 1985 discovery that ozone levels over Antarctica had halved due to our dependence on chlorofluorocarbons came as an unpleasant jolt, just as few predicted that the “wonder” pesticide DDT would ultimately cause the egg shells of birds of prey to thin and crumble.

In a new paper published in Ecosystems (http://tinyurl.com/z78ucyf) we argue that humanity will continue to receive unpleasant ecological shocks unless it begins to conduct experiments at the planetary, or at least ecosystem, scale.

But should scientists be allowed to experiment with our planet, given that we only have one? The answer is, of course, no but in many cases we are already using Earth as a guinea pig.

Massive oil spills like Deepwater Horizon and the construction of the Suez Canal have transformed our environment while commercial fisheries have acted as a form of ecological “keyhole surgery”, excising crucial species from the ocean. These large-scale, unreplicated natural experiments (LUNEs) have delivered insights of great power into cosmology, evolution and geology, yet they are relatively rare in the field of ecology and continue to meet resistance because they cannot be replicated.

Although LUNEs have only just begun to be exploited, they have had a disproportionately positive effect on conservation policy and are a crucial step in extrapolating our understanding of ecological processes from small to global scales. Without LUNEs we will struggle to solve the problems we create as we descend further into the Anthropocene.

Some Large, Unreplicated Natural Experiments

The range of the sea otter once stretched from California to Japan via the Aleutian arc, a 1900 km-long chain of islands located to the west of Alaska. Cursed with the thickest fur of any mammal, sea otters were almost wiped out by fur traders in the 1700s. This devastation fashioned an unlikely natural experiment, creating islands in the Aleutian archipelago that were empty of otters and others where the animal remained.

A landmark 1974 study published in Science (http://tinyurl.com/j2nyddk) compared these islands and found that what had become the latest winter fashion accessory was crucial for preventing ecosystem collapse – sea otters were a “keystone” species. Without otters, sea urchins had carte blanche to munch through as much kelp as they liked, causing these underwater forests to die back and robbing the harbour seals and bald eagles that relied on them of food.

One of the most famous LUNEs to date gave scientists a unique opportunity to explore the ecological role of the grey wolf, an apex predator that was re­introduced to Yellowstone National Park in 1995. In 2004 a study published in Bioscience (http://tinyurl.com/zv52yv3) reported that once-cocky elk now thought twice before venturing down to the riverbanks to gorge on willow. As a result the trees grew back, reducing erosion and altering the meander of the river itself.

Large-scale natural experiments often involve energies and timescales beyond the reach of one generation of humankind, and as a result they can reveal ecological insights that would be unattainable using direct experiments. In 2010, for example, an iceberg crashed into the Mertz Glacier, causing a 78 km piece of the latter to splinter off. The melting of the iron-rich ice led to abrupt declines in salinity and triggered massive phytoplankton blooms, simulating the effect of climate change on glaciers in a way that scientists could never have orchestrated.

In addition, this LUNE revealed that a swathe of the Southern Ocean that had been covered by a vast tongue of ice for 80 years still supported a diversity of marine life. “Despite no natural light reaching the area… nutrient-rich water has supported a proliferation of vulnerable marine life, including sea-stars the size of hubcaps,” Australian Antarctic Division Program Leader Martin Riddle reported in a press release in 2011 (http://tinyurl.com/zngkmpv).

Also out of reach for most ecologists is the ability to connect two oceans that have been separated for millions of years. Handily, the US built the 77 km-long Panama Canal between the Atlantic and Pacific Oceans in 1914. In addition to providing ships with a much-needed shortcut, this LUNE gave scientists a rare glimpse into how confrontations between previously isolated populations of fishes play out at large scales. The research, published in Proceedings of the Royal Society B Biological Sciences (http://tinyurl.com/juevbe4), showed that freshwater fish communities are not “saturated” but can easily make room for new species. Were the twin forces of competition and predation not as powerful as previously thought?

LUNEs are particularly useful when traditional experimental approaches are off the cards for ethical reasons. For instance, it would be impossible to wipe out a population of animals, yet mass mortality events are relatively common in the wild. For example, 97% of long-spined sea urchins in the Caribbean inexplicably expired in 1983 (http://tinyurl.com/honp2o8). While this event may initially have led to some high-fiving among beachgoers, it also created a tragic LUNE that transformed the legendary coral reefs of the Caribbean into barren, algae-coated rock, revealing the important role played by sea urchins in the food web.

Similarly, scientists could never have justified dumping more than 500,000 tonnes of methane into the ocean to study the effects of climate change on deep-sea habitats, but they didn’t have to – Deepwater Horizon did it for them. Researchers publishing in Science (http://tinyurl.com/jhykvs7) found that the disaster triggered an explosion in deep-water methane-eating bacteria that, 120 days later, had “mopped up” most of the pollutant. (Unfortunately, however, the bacteria also covert the methane into carbon dioxide, which can create “dead zones” by acidifying the water).

Invasive species pose a growing threat to biodiversity, with 60% of bird, mammal and reptile extinctions recently attributed to marauding predators. However, invasive species have also created important LUNEs by crippling populations of endemic species on remote islands. Whereas Guam’s only native snake, the burrowing blind snake (Rhamphotyphlops braminus), poses no threat to the island’s animals, the invasive brown tree snake (Boiga irregularis) has devastated native bird populations.

Indeed, this snake’s invasion of the island created an unusual LUNE that scientists have used to study whether birds regulate the food web through predation. Published in 2012 in PLoS ONE (http://tinyurl.com/

h2sn9by), Haldre Rogers and colleagues at The University of Washington found that loss of insect-eating birds led to an explosion in spider density. It also altered when spiders built their webs and how big the webs were.

Similarly, a LUNE generated by the invasion of Christmas Island by yellow crazy ants (Anoplolepsis gracilipes) revealed that without the island’s trademark red land crabs (Gecarcoidea natalis), the ecosystem underwent a meltdown. Plants took over, leaf litter rotted less efficiently, and honeydew-secreting scale insects high up in the canopy prospered, causing outbreaks of sooty moulds and ultimately the death of canopy trees.

The study was published in Ecology Letters in 2003 (http://tinyurl.com/zwkfzkx).

The Replication Crisis

There is no question that LUNEs will continue to play a crucial role in scientific progress, particularly as science budgets tighten and evidence mounts that experiments conducted in laboratories or mesocosms do not always “scale up”. Yet LUNEs remain a minority in the scientific literature and often face resistance from journal referees, partly because many ecologists continue to view traditional, small-scale experiments as the scientific gold standard. In contrast, LUNEs constitute a kind of Faustian bargain: in exchange for insights into how ecological processes work at large scales, replication must be sacrificed. The complex interplay of natural and anthropogenic forces that generate LUNEs cannot be fully understood by scientists, let alone recreated. How does one build a life-sized replica of the Panama Canal?

Nonetheless, there is change afoot in the scientific community. Science is in the throes of a “replication crisis” triggered by the realisation that few studies are replicated and that a disconcerting proportion of research is irreproducible.

In response to this crisis, some scientists have decided that it’s time to overhaul the role of replication. What if exact replications should no longer be treated as all-powerful “one-off” confirmations or rejections of a theory? Instead, critics argue, we should focus on testing hypotheses in the real world through “conceptual” replications in a range of contexts and using different techniques.

LUNEs fit neatly into the new approach to replication. For example, a recent Nature study (http://tinyurl.com/gnh34q2) tested hypotheses about the effect of predators on carbon storage using a range of species (sharks, bony fishes and crabs) and habitats to look for trends in response. Their novel finding was that predators may be crucial for keeping carbon in the ground and thereby prevent climate change.

Putting the sapiens in Homo sapiens

LUNEs are revolutionising the way we view our world. From developing ways to “crowdsource” civility to understanding the effect of daylight savings time on heart attack risk, childhood obesity and air quality, LUNEs have allowed scientists to test ideas that are important to social and scientific progress in real-world settings.

Why does this matter? Because history tells us that it is necessary to demonstrate that human activities have an ecosystem-wide effect before changes in policy can occur. It’s widely agreed that the global decision to ban chlorofluorocarbons was largely driven by the discovery of the Antarctic ozone hole, even though evidence from smaller-scale experiments had existed for two decades. Similarly, the debate over whether phosphorus versus nitrogen or carbon was to blame for deteriorating water quality in the lakes and rivers of the US in the 1970s was only resolved when the “father” of LUNEs, Prof David Schindler, addressed the question using an unreplicated, ecosystem-scale experiment that split a lake down the middle and observed the effects of phosphorus in one half. Shortly afterwards, Canada and several US states passed laws banning phosphorus.

Time is running out to halt and reverse the greatest ecological challenges facing the planet. Two recent studies published in eLife found that more than 50% of all chondrichthyans – the class that contains sharks and rays – are threatened or near-threatened, blowing insects, mammals and amphibian extinction rates out of the water (http://tinyurl.com/zs324gk; http://tinyurl.com/j82xc99). More than 60% of the world’s coral reefs are now under threat from fishing, urban development and sediment run-off. China alone is estimated to have lost more than 80% of its coral cover in the past 30 years.

Despite these alarming developments, policies continue to lag behind what’s needed to stave off an ecological meltdown. Many scientists believe that current carbon pledges are inadequate to prevent the Earth’s temperature rising 2°C – the tipping point for dangerous and irreversible climate change – ­by the end of the century. The speed at which glaciers are now retreating globally is “historically unprecedented”, according to a recent study in the Journal of Glaciology (http://tinyurl.com/h3n328f). For example, the ice river flowing from the Jakobshavn glacier in Greenland is now travelling at a rate of 46 m/day – twice the rate reported in 2003. Despite such revelations, policies on climate change remain inadequate and indeed US President-elect Donald Trump recently proposed a halt to all climate change research at NASA

LUNEs can play a role in galvanising the global policy changes required to not only halt but reverse these challenges. Promisingly, many politicians already seem to be aware of the power of LUNEs. “We are as humans conducting a massive science experiment with this planet,” noted current Prime Minister Malcolm Turnbull in 2010. Despite this, he concluded, we “have a deep and abiding obligation to this planet and to the generations that will come after us.”