These creatures have mastered agriculture, cultivating crops and herding livestock. In the process, all parties involved have reciprocally shaped each other’s evolution.
For us humans, farming changed everything. Starting around 10,000 years ago, the domestication of plants and animals meant people could for the first time build up food surpluses. This liberated them to think about something other than subsistence. Nomadic hunter-gatherer lifestyles gave way to permanent settlements. Villages became cities. Cities gave rise to civilizations.
By any estimation, the agricultural revolution was a pivotal chapter in the human story. But look closely enough and you see we’re not the only animals that can grow our own food. In fact, ants and beetles were cultivating bumper crops of fungi 50 million years before we started farming. And just as we ‘invented’ agriculture several times in different parts of the world when we made use of plants and animals living wild around us, several non-human species have developed farming-like relationships with organisms they’ve encountered.
We raise multiple crops, whereas animals typically specialise in one.
Some cultivate crops. Others have mastered animal husbandry. Either way, all such relationships are examples of a rare form of symbiosis known as a cultivation mutualism.
In many ways, these associations resemble human agriculture. It’s important not to anthropomorphise too much, though, and there are limitations to the analogy. These days we consciously carry out sophisticated selective breeding programs to maximize crop yields or improve livestock. That’s not true of animal farmers, whose associations have been forged unwittingly by natural selection. We also raise multiple crops, whereas animals typically specialise in one.
Nevertheless, in the co-evolution of organisms in farming-like mutualisms there are similarities to the way we first domesticated plants and animals in the Neolithic. We can also see parallels in how such associations can change the biology of both parties. And as with humans, agricultural life has in some cases allowed animal farmers to rise to major ecological importance.
The fish that farms alga
Damselfish are one of the most abundant fish on coral reefs across the world, from the Caribbean to Indonesia. Some species forage on tiny crustaceans but many stake out permanent gardens among the coral to cultivate algae. “They weed out the stuff they don't want by taking a bite of it and swimming to the edge of the territory to spit it out,” says Jordan Casey, a PhD candidate at James Cook University in Queensland, Australia, who studies damselfish on the Great Barrier Reef. They also protect their algal gardens from would-be thieves. “They’re tiny fish but very aggressive,” says Casey. “They’ll attack humans.”
Exactly which type of algae damselfish prefer varies with species and location. In Mauritius, for example, the damselfish Stegastes nigricans grows a mixed bed of alga. But in the Okinawa islands off Japan, the Red Sea, and the Great Barrier Reef, S. nigricans maintains a monoculture of red algae from a family called Polysiphonia.
It seems the damselfish turned to farming red algae because they lack the enzymes needed to digest many common algal species. Polysiphonia is easy to digest. It’s also less robust than the inedible algal species it usually competes with, meaning it needs protection. So the relationship works for both parties: the damselfish gets a steady supply of food and the alga avoids competition.
What works for the damselfish might not be so good for the reef. Last year, Casey and her colleagues found that bacteria associated with black band disease are more abundant inside damselfish territories on the Great Barrier Reef than outside of their territories.
This suggests damselfish behaviour may be contributing to an increase in the disease, though Casey points out that rising temperatures have a much bigger impact.
The dancing, farming crab
Many leagues below is another marine farmer, one that ‘dances’ while it works.
In 2006, ecologist Andrew Thurber, now at Oregon State University, US, was part of a geological research cruise studying seeps on the ocean floor off Costa Rica that belch methane and hydrogen sulphide gas. To his amazement, the submersible pilot brought to the surface an unusual crab he’d spotted waving its arms among the seeps. It was a new species of yeti crab, since named Kiwa puravida.
The first yeti crab species (Kiwa hirsuta), so named for the bristles covering its claws, had been discovered earlier that year at a hydrothermal vent off Easter Island.
In 2011, Thurber and colleagues confirmed that K. puravida uses its bristly claws to raise bacteria, which capture energy from the gases released by the seeps, before grazing on them with its comb-like mouthparts. He has also demonstrated that the bacteria are the crab’s main source of food. That was important because although deep-sea vents are home to crustaceans that have similar bacteria growing on their bodies, it was not clear whether they rely on the bacteria for nourishment. “What we have with the yeti crab is a very clear-cut case of using a cultivational mutualism to get energy from the seafloor,” says Thurber.
It seems to be a behavioural adaptation to improve yield
In doing so, the yeti crabs form part of a deep-sea seep community that consumes methane and therefore keeps it from escaping into the atmosphere.
And while he’s yet to prove it, Thurber thinks that the yeti crab waves its claws back and forth to stimulate bacterial growth. With every swing of their arms, the crabs churn up water and seepage to ensure that the bacteria get fresh supplies of oxygen and hydrogen sulphide. “It seems to be a behavioural adaptation to improve yield,” says Thurber. “At least that’s the hypothesis.”
Ants that domesticate fungus
On the salt marshes along the east coast of North America, the marsh periwinkle (Littoraria irrorata) grows fungus on Spartina grass.
But by far the most impressive fungus farming takes place on land, where termites and more than 200 different species of Attine ants raise fungi for food.
Most advanced are the leafcutter ants, more than 40 different species that live in the forests of South and Central America, and southern parts of the US. They form some of the largest, most complex societies on the planet, with some colonies containing as many as 8 million ants. To sustain these vast settlements, leafcutters, which arose around 12 million years ago, have refined the fungus farming pioneered by their ancestors.
They march in convoy to cut and collect fresh green leaves. These are munched into a pulp and fertilised with ant faeces before being added to the top of the garden - a ball of mashed up leaves, the fungus Leucogaricus gonglypherous, and selected bacteria. As the fungus and microbes break down the leaves, the ants diligently tend their gardens. “It’s an elaborate and intensive process of grooming, pruning, and weeding out infected parts,” says Cameron Currie, who studies leafcutters at the University of Wisconsin-Madison in the US. In return, the fungus produces blob-like fruiting bodies packed with nutrients for the ants to eat.
Fungi may have evolved to attract ants and then ants made the transition to cultivation
In some cases, researchers have discovered, leafcutters carry symbiotic bacteria on their bodies that produce antibiotics, which they rub onto the fungus to protect it against fungal parasites.
Clearly, the ants have adapted in response to this relationship in order to be a better partner, even going as far as developing complementary mutualisms with bacteria. But it cuts both ways. “This particular fungus is only found in association with leafcutter ants, suggesting that is has become specialised,” says Currie. “It has unusually large and nutrient-rich fruiting bodies that are not present in other strains of fungi cultured by Attine ants.” In that sense, it looks like the leafcutters have domesticated the fungus.
Surprisingly, when it comes to the question of how this mutualism originated, recent research suggests the fungus initially drove it. “What we think now is that fungi may have evolved to attract ants to disperse its spores and provided nutrients in return, and then ants made the transition to cultivation,” says Currie.
Over millions of years of co-evolution, the beetles have selected the fungi best suited to their needs
This partnership has allowed leafcutters to become the dominant herbivores of New World tropical forests, shaping the ecosystem they call home.
What’s more, having perfected their methods for millions of years, it seems the leafcutter ants might teach us a thing or two. In 2013, Currie and colleagues identified novel enzymes in L. gongylopherous involved in plant degradation that could potentially be used to improve the chemical cocktails we use to convert biomass into ethanol for biofuels. Also, Currie is discovering that the leafcutters might be a rich source of much-needed new antibiotics.
Feeding weevil larvae
Fungus farming emerged only once in ants. In wood-boring beetles, it evolved independently eleven times. Today there are roughly 3,200 species of ambrosia beetles, none larger than a grain of rice, that raise fungi in chambers tunnelled out of dead trees. They’re a diverse bunch of weevils united by fungus farming, and they’re more common than you might think.
“The ambrosia beetles are largely ignored compared to Attine ants but they’re much more ubiquitous,” says Jiri Hulcr, a forest entomologist at the University of Florida in Gainsville, US. “These beetles are everywhere,” from the tropics to temperate climes.
The fungi depend on the beetles for entry into trees, where bark presents a formidable barrier. To facilitate such transport, the beetles have evolved specialised pockets on their bodies to carry the big sticky spores of fungi when they move on after exhausting their host tree. For its part, the fungus extracts nutrients from the tree tissue that the beetle could not, then presents a portion of it as nutritious morsels for beetle larvae to gobble.
They smell so good you would not believe. Some smell like ripe bananas
Each group of ambrosia beetles has one or several species of fungi it prefers to raise, but all of them produce nourishing globules not found in fungi that are not associated with beetles. Again, this is akin to what we might call domestication. “It’s like if you compare wild wheat, which is nothing but a grass, and domestic wheat, which is weird organism with huge amount of nutrients packed in seeds that can’t reproduce without our help,” says Hulcr. “Over millions of years of co-evolution, the beetles have selected the fungi best suited to their needs.”
Hulcr has grown many of them in his lab. “They smell so good you would not believe,” he says. “Some smell like ripe bananas.”
Ambrosia beetles have not received much attention from scientists. That’s changing now we’re seeing the damage they cause when transplanted from the areas where they evolved. “Sometimes naïve trees can’t cope with the fungus; they have some sort of allergic reaction and you get massive die-offs,” says Hulcr.
Take the redbay ambrosia beetle (Xyleborus glabratus), for example. Originally from southeast Asia, where it lives in dead trees, it was accidentally brought into the southeastern US, where it has moved into living redbay. It has also spread into avocado trees in some areas, raising the prospect that it could devastate Florida’s multimillion-dollar avocado industry.
Animals that herd livestock
Like humans, some animals have also turned to animal husbandry and herding. Common across Europe and some parts of North America, the black garden ant (Lasius niger), herds certain species of aphid. The little green bugs, the scourge of many a human gardener, feed on plant sap and excrete a sugary liquid called honeydew from their anuses, which the ants drink in exchange for providing protection from predators and shepherding them to leafy pastures new.
The ants often bite off the aphids’ wings to stop them flying away. In 2011 Tom Oliver and colleagues at University College London, UK, discovered that they tranquilise their flock with chemicals to slow them down and keep them from wandering off.
Sometimes, presumably when they’re hungry for protein or perhaps because they need to cull the herd, the ants eat their aphids.
But new research suggests that the Melissotarsus ants of mainland Africa and Madagascar might be the only animals other than humans to keep herds not for honeydew but for meat. These 3mm-long ants burrow out homes under the bark of trees. There they keep armoured scale insects, also known as diaspidids, which typically periodically secrete a waxy shell to protect their soft bodies. “Armoured scale insects don’t have a complete gut, so they’re incapable of producing honeydew,” says Scott Schneider, a PhD candidate at the University of Massachusetts in Amherst, US. “Actually they don’t produce much of anything. So it’s not been clear what the ants are getting from this relationship.”
As humans we like to think of ourselves as unique. We think of our cultivation of plants, for example, as a unique innovation
In the case of Melissotarsus emeryi, a species found in South Africa, the diaspidid it herds doesn’t even produce a waxy cover.
That rules out the idea that the ants are nibbling on the protective waxy coatings. The only other explanation, thought Schneider, is that armoured scales themselves serve as the food reward. It’s proven difficult to catch them in the act because the ants quickly repair any openings made to allow researchers to peer into their chambers.
Instead of spying on the ants, Schneider has measured chemical markers called isotopes in their bodies. These indicate whether the ant’s diet is primarily made up of plants or animals. He’s yet to publish the findings but Schneider says his evidence suggests that they do indeed eat armoured scales. If so, it looks like M. emeryi ants have selected armoured scale insects that don’t produce a waxy shell because it makes them easier to munch – yet another example of domestication reminiscent of how we selected for changes in wheat or corn, whose wild ancestor, teosinte, bears little resemble to corn cobs we chomp on today.
“As humans we like to think of ourselves as unique,” says Cameron Currie. “We think of our cultivation of plants, for example, as a unique innovation. But there are clear parallels [in non-human animals] in terms the origins of these relationships and how they change the biology of those involved.”