Around the world right now, thousands of animals are about to die. The game is up for untold numbers of deep-sea fish, mountain-dwelling hares, subterranean earthworms and high-flying songbirds. They are all seconds away from becoming dinner for predators like lions, eagles and sharks.
But when did this carnage begin? Have predators stalked the Earth since the origin of life itself? Or was our primordial planet once a Garden of Eden where species lived in peaceful co-existence?
The truth is, no one actually knows for sure. But evolutionary biologists have learned enough about the history of life on Earth to begin the hunt for the first predator. Their work suggests it was about as far removed in appearance from today's killers as it's possible to imagine.
Before we pick up the trail, it might help to spell out what a predator is. According to most biologists, predation must involve the death of one living thing at the hands (or teeth, or claws) of another, which has to gain some nutritional benefit from the kill. A lion is a predator because it kills and eats a gazelle, but the gazelle is not a predator, because it doesn't have to kill the grasses it eats.
Predators can kill without inflicting physical injury
What sort of traces would the first predator have left behind? We often think of predators using jaws and sharp teeth to rip chunks out of their prey, so maybe we should look for the oldest jaws and teeth. In fact, just last year, we learned that modern vertebrate jaws date back 420 million years and that teeth appeared 500 million years ago.
But predators can kill without inflicting physical injury. Think of the predatory pitcher plants that trap, drown and devour insects. So if predators don't need teeth and jaws, they might have appeared long before the 500-million-year mark.
It turns out they really did. Palaeontologists have collected fossils of predators that existed tens of millions of years before teeth evolved. These predators date right back to the first abundant animal life, about 540 million years ago.
They are known collectively as the anomalocaridids, a name that translates as "abnormal shrimp". It's well chosen: the anomalocaridids were odd-looking marine animals that to our eyes seem to have been cobbled together from bits of various different species. They grew up to 2 m (6ft) in length, and had good eyes and a pair of dextrous graspers near their mouth. They may have lacked teeth and jaws but they were undoubtedly terrors of the seas they occupied.
"Anomalocaridids are the earliest 'mega-predator'," says Lindsey Leighton at the University of Alberta in Edmonton, Canada.
Originally palaeontologists thought a hunting anomalocaridid would have used the formidable ring of plates around its mouth to crush its prey. But disappointingly, an analysis a few years ago suggested that these plates were too weak to crush anything. The anomalocaridids may actually have used their mouths to suck up soft worms from the muddy ocean floor.
To crush or to suck?
But were these worm-sucking anomalocaridids the original predators? In July 2014, we learned something new that helps answer the question. An exceptionally well-preserved fossil revealed that, for all their sophisticated appearance, anomalocaridids had simple brains. What's more, other well-preserved fossils from the same time period show that the animals living alongside the anomalocaridids - including some that the predators might have eaten - had relatively complex brains in comparison.
This actually fits with what we know about today's predators, says Nicholas Strausfeld at the University of Arizona in Tucson, who helped describe the anomalocaridid brain. "There are many extant examples of what can be considered small-brained species preying on others that have larger brains," he says. This shows that predatory behaviour can occur in relatively simple species: the kind that existed before the anomalocaridids evolved.
"We subconsciously tend to think of predators as advanced, probably because we envision them at the top of the food web," says Leighton. But predatory behaviour may be among the first feeding strategies to appear in ecosystems. "Actually, herbivory [plant-eating] tends to show up much later."
In fact, there is evidence that predators existed before the anomalocaridids. Animals first began to grow hard shells and exoskeletons about 550 million years ago. Some of the fossils of these earliest exoskeletons are punctured with circular holes about 0.4 mm across. These are almost certainly marks left by predators that bored through the tough armour to feast on the soft tissue hidden within.
The borings are all similar in shape, which suggests they were made by a single predatory species. We don't yet know what it looked like. But the borings it made are currently the earliest good evidence for relatively large predators, says Leighton. That makes the mystery species responsible a much better candidate for the title of first predator than the anomalocaridids.
The Ediacarans escaped the attention of predators, simply because there weren't any
A look at slightly older rocks and fossils strengthens the case. Between about 575 and 540 million years ago the world was occupied by a peculiar collection of organisms that have been labelled the Ediacaran biota. The Ediacaran organisms were large – some were over 1 m (3 ft) long – soft-bodied, and mostly incapable of movement. They should have been torn to shreds by predators, but they weren't.
In the 1980s, Mark McMenamin at Mount Holyoke College in South Hadley, Massachusetts suggested that the Ediacarans escaped the attention of predators simply because there weren't any – or at least, none large enough to pose any real threat. These ecosystems may have been peaceful live-and-let-live worlds in which each Ediacaran used photosynthesis to meet its own energy needs. McMenamin dubbed his idea "the Garden of Ediacara".
In the 30 years since, geologists have found little evidence that large predators were active during the Ediacaran period. That suggests McMenamin's ideas may be correct. If they are, we have identified the point in geological time – about 550 million years ago – when large predators first appeared.
But not all predators are large. The world of microbes is teeming with tiny killers. They might be too small to inflict damage on something the size of an Ediacaran, but these predators can still wreak havoc at the microscopic scale - and they were doing so long before the Ediacarans evolved.
A decade ago, Susannah Porter at the University of California Santa Barbara and her colleagues discovered tiny fossilised amoebae in 740-million-year-old rocks near the bottom of the Grand Canyon. The amoebae had developed tough skeletons, just like big animals did 550 million years ago did when large predators appeared.
It seems that at least some of the amoebae grew their skeletons for a similar, defensive reason. Several of the fossils carried semi-circular borings about 20 micrometres wide. These were probably the marks left by some unidentified predatory microbe that punctured the tough skeletons to feed on the nutrients within, rather like vampire amoebae do today.
Teeny tiny miniature predators
In the same way that the borings in the 550-million-year-old animals are the earliest strong evidence we have that big predators had evolved, the borings in the 740-million-year-old microfossils are the earliest good evidence of tiny predators.
But they probably don't signify the moment when predatory behaviour first evolved. More likely they show us when micro-predators began to attack complex microbes, like amoebae, that could evolve hard skeletons in response. Simpler microbes, like bacteria, might have been attacked by micro-predators much earlier in Earth's history, but without ever evolving a defence strategy that can be easily identified in the fossil record.
In other words, micro-predation probably predates these 740-million-year-old fossils. So we will need a different way to study it.
One approach is to look at the predatory strategies that microbes use today. The most well-known is called engulfment: a relatively large microbe swims up to a smaller cell and swallows it whole. Look at these microbial engulfers, though, and a pattern soon emerges. They are almost all "eukaryotes", the group that includes big organisms like animals and plants, as well as microbes like the amoebae. Engulfers seem to be absent from the other great branch of the tree of life, the prokaryotes, which include all the bacteria.
Some prokaryotes force their way into larger cells
No one knows for sure when the eukaryotes first evolved, but the general consensus is that they came after the prokaryotes, around 2 billion years ago. So perhaps engulfment, and predation, began with those first eukaryotes. This would imply that the earlier, prokaryotic-only world was a predator-free zone.
That seems to fit with what we know about living prokaryotes. "There are no real prokaryote predators today," says David Penny at Massey University in Palmerston North, New Zealand.
Or are there? It's true that prokaryotes seem to be incapable of engulfment, says Edouard Jurkevitch at the Hebrew University of Jerusalem in Rehovot, Israel. But they can use other strategies to prey on cells in their environment. Some prokaryotes force their way into larger cells and digest them from the inside, says Jurkevitch. Others latch onto the side of cells and consume them from the outside. Some even team up with other prokaryotes to form hunting packs that can target entire microbial colonies.
The general consensus is that prokaryotes first appeared about 3.5 billion years ago. Perhaps some of them were predatory. "The roots of predation (and parasitism) may be very ancient," says Jurkevitch.
Penny's research backs this conclusion. A few years ago, he decided to test whether life could have enjoyed a peaceful Garden of Eden-style existence before eukaryotes appeared. He ran computer simulations to see how the first populations of cells would have evolved 3.5 billion years ago, assuming they obeyed a few fundamental biological principles. His results suggest that predation is too good a strategy not to evolve rapidly, although predators will usually be heavily outnumbered by organisms that make their own energy.
We don't know what the very first life was like
"It did seem that predation was an inevitable outcome of the principles," says Penny. "Predation appeared within a thousand or so generations."
Penny's theoretical work, and Jurkevitch's observations of prokaryotes today, suggest that there were predators on Earth 3.5 billion years ago, very soon after prokaryotic cells first appeared. So have we finally identified the very first killers? After all, before prokaryotes appeared there was no cellular life at all. We don't know what the very first life was like, but it may have been a loose collection of complex organic chemicals floating in solution. These probably included nucleic acids similar to DNA, such as RNA.
Remarkably, though, some researchers think predators might have lurked even in this pre-cellular world of chemical replicators.
About 15 years ago Thomas Cavalier-Smith at the University of Oxford suggested that these nucleic acid communities were a kind of simple ecosystem. Today, some nucleic acids act as catalysts that break up other molecules. Cavalier-Smith reasoned that they probably existed in the pre-cellular communities too. Some of them would have latched onto other nucleic acids and broken them apart, effectively attacking and destroying them to fuel their own growth and replication. In other words, these molecules would have behaved as predators.
Armen Mulkidjanian at the University of Osnabrück in Germany, who studies the origins of life, says the idea is reasonable. It's more common for researchers to call this behaviour parasitic, he says. "But parasitic behaviour, generally, should include predatory behaviour."
The biggest hurdle of all is to picture the predators in the primordial soup
If Cavalier-Smith is right, then these catalytic nucleic acids really were the very first predators. Go back to the time before they existed and there was no life of any sort, so by definition there can have been no predators.
From our position as large animals, it's easy to lose perspective on life's history on Earth. Think predators and the first thing that springs to mind might well be a pride of lions or a pack of wolves. It's a big mental leap from these modern killers to the worm-sucking anomalocaridids and the enigmatic predators that patiently drilled their way through defensive armour over half a billion years ago.
But even that leap is easy compared to the jump we have to make to recognise predators among prokaryotes. And the biggest hurdle of all is to picture the predators in the primordial soup that existed before cellular life. If they existed, they might not have looked particularly fierce, but those killer molecules are hugely significant. They suggest that from its very inception, life has been troubled by predators intent on causing death.