One moment Stefano Mammola is standing in a mossy forest overlooking northern Italy’s Po plain. The next, he has vanished through a hole little wider than his body, into the forest floor. With less grace, I clamber after him, landing in a pit 2 metres below. A tunnel ahead is the gateway to a 3-kilometre-long cave network. As I falter, Mammola, a cave biologist at the Water Research Institute in Verbania, Italy, encourages me with tales of an exotic spider living deep inside. It has cocoon silk that can stretch to more than seven times its length without breaking – outstanding even by arachnid standards.
Superstrong silk is just one of the ways life has adapted to Earth’s most extensive and unexplored terrestrial ecosystem: the caves, fissures and tiny gaps beneath its crust. Scientists have spent the past few decades exploring these remote locations and cataloguing and probing the creatures within. Now they are raising the alarm.
Until recently, it was assumed that this subterranean life would sit out climate change relatively unaffected, in cool seclusion. But new research has shot down this belief. Warmth, drought, seasonal change and rising seas are all reaching into underground refuges, leaving their occupants uniquely stranded. Yet our ignorance of these fantastical creatures is vast. Mammola is so concerned that he has coordinated a project aiming to map the entire subterranean ecosystem of Europe, reveal what biodiversity is present and figure out where to prioritise conservation efforts. This weird and wonderful world is worth saving not just for its own sake, but also because it is crucial to human survival.
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Caves are defined, a bit anthropocentrically, as . Combined with smaller voids, they make up (there is also a submarine ecosystem beneath the ocean crust). Limestone karst, sandstone and cooled lava are richest in perforations, but most of the ground beneath us contains habitats at between a metre and 2000 metres depth. “We are only on the surface of a cheese that’s full of small holes,” says at the Federal University of Lavras, Brazil.
Crawling, swimming and wriggling through these mostly pitch dark and often wet labyrinths are an of spiders, millipedes, crustaceans, insects, bats, worms, snails and fish, plus bacteria, fungi and protists. Most remain undiscovered and undiscoverable. “What we can explore are the caves, but the habitat is much, much bigger than that,” says . Some of its inhabitants, known as troglobites, can only survive underground. Others – cave-roosting bats, for example – are trogloxenes, living underground for a portion of their lives. Then there are troglophiles, including most salamanders, which are happy living both inside and outside caves.
In the past few decades, this world has opened up to scientists. Spectacular discoveries in Europe include those in Movile cave, Romania, where an entire food web was found living without light, complete with giant microbial mats, leeches, woodlice, a water scorpion and a snail. In Brazil, discoveries began to escalate more recently, says Ferreira. Brazilian scientists have formally described around 300 troglobites, but 1000 or so more await examination in freezers and cupboards.
Even well-known species can hold surprises. Mammola often encounters a spider called Pimoa rupicola. Despite being very common, until recently no one had noticed that it is, . One of these sports a spike protruding at right angles from the tip of its pedipalp (the spider equivalent of a penis), part of a lock and key mechanism that ensures it mates only with its own kind.
The spiders he and I are hunting are equally strange. But, as I slide down loose rocks under a slab of slimy granite, my claustrophobia is growing. Mammola, sensing I will never reach the depth required to encounter our quarry, shimmies ahead, disengages one from its web and returns. The bewildered-looking creature, Troglohyphantes lanai, has tiny scars where its eyes should be and improbably long legs, which may have evolved to accommodate the many sensory hairs it deploys to detect air currents, humidity and various chemicals – or perhaps just to elevate it above the water.
For cave-dwelling species, such remarkable features are the norm. Waiting in darkness for a scrap of biomass to drift in from outside has led to some extraordinary adaptations. Many species have lost characteristics that are indispensable above ground, including eyes and pigmentation. In temperate caves, cuticles, the external layer crucial on the surface to lock in precious moisture, have thinned. Changes aren’t just skin deep. Cave creatures live slowly to save on calories. Mammola tells me the story of “Katrina”, a spider inhabiting a well-studied cave that remained motionless on her web for a year, waiting for a fly to blunder in from outside. Reproduction can be similarly leisured. One cave spider mates every 19 years, – measly compared with the hundreds produced by many of its overground counterparts. Slow metabolism can also mean a long life. The olm, a colourless, eyeless salamander, can live for a century.
Then there is the trick of swapping genitals. In 1997, Ferreira discovered a new genus of cave-dwelling insects, Neotrogla, but it was another 17 years before a colleague, Charles Lienhard at the Natural History Museum of Geneva, Switzerland, noticed that the females have a penis – known as a gynosome – and the males a vagina-like chamber. The female protrudes and retracts her gynosome, dipping it deeply into the male vagina to suck up his voluminous semen. She does this regardless of her fertility, says Ferreira. “It seems that the males are more efficient at gathering food and then their sperm becomes not only useful for fertilising eggs, but also a nutritious and important drink [for females].”
Subterranean life furnishes us with more than mystery, however. It is a treasure chest of genetic information. The isolation and relative simplicity of communities provide a natural laboratory . Troglobites can even give insights into human health. For example, identifying the genes responsible for their eye degeneration has helped scientists , which causes loss of vision.
Critically, this underworld also provides services to the world above. Some . that more than half the world’s population relies on groundwater for consumption and agriculture, and 50 per cent of surface ecosystems also depend on groundwater. The subterranean world acts like a giant utility system below us, says Mammola, a backstairs operation that stores, cleanses and transports water and plays a role in the carbon and nitrogen cycles.
, also at the Water Research Institute, dives into flooded caves to study these processes. He tells me about one such cave system under the Yucatán peninsula in Mexico, 1600 kilometres of which have been mapped. To reach this realm, he treks through the jungle to an unobtrusive hole in the ground and slips into its murky water. “As we dive down, the visibility becomes spectacularly clear,” he says. These caves were thought to be “aquatic deserts” because the bedrock above them filters out everything except water. But that water turns out to contain dissolved organic matter from the forest, including the greenhouse gas methane, and this provides food for microbes, . , sequesters carbon and purges excessive nutrients such as nitrogen – then it seeps clean water into the ocean, a service previously thought to be the preserve of rivers. Without the life underground, says Brankovits, coastal waters would be at greater risk of severe degradation and much more methane would bubble into the atmosphere. “It really matters,” he says.
Discoveries like this are making scientists increasingly alarmed at the rate of disappearance of the subterranean world – from destruction by mining, tunnelling and groundwater extraction, and as a knock-on effect of deforestation. Now there is the added realisation that global warming poses another challenge. “What I find fascinating is that people had been saying climate change will not be relevant underground,” says Mammola.
Two decades ago, Mammola was among the first to predict that cave temperatures rise in concert with those outside, but with a 20-year time lag. The finding, based on computer modelling, was hard to confirm due to a lack of temperature data, but in 2018 it was . Since then, researchers led by at the University of Lisbon, Portugal, have looked at caves in multiple locations and found that temperatures within each vary very little, but .
Can’t stand the heat
Recently, Mammola returned to 30 caves whose temperature he had measured a decade ago to repeat the experiment. He found an average increase of 0.5°C. He fears instrumental error and plans to take further measurements, but, if accurate, the finding could be a big deal for troglobites. “If you are adapted to stable conditions and have been living for generations in the same constant temperature, you probably do not have a lot of physiological mechanisms to cope with change,” says Reboleira.
Mammola and his colleagues have on eyeless, long-legged spiders of the genus Troglohyphantes. “Most of the species will really retract their distributions and even go locally extinct,” he says. Experiments in the lab revealed that a rise of between . Other fauna may be more resilient, though. Reboleira is about to publish work showing that various cave-adapted animals die at 6°C above their average living temperature. And in other experiments, blind and wingless cave beetles endemic to the Iberian peninsula . But their cells were stressed and damaged. “So maybe in the long term there will be other consequences that we don’t know of,” says at the University of Murcia, Spain, one of the researchers.
Cave dwellers might, of course, find a solution. “You need to hope that they will have the capacity for local adaptation in their DNA,” says Mammola. One possibility is that the genes that would allow them to adjust to changes in temperature are merely switched off, rather than lost – something Mammola is planning to study. Another possibility is that the heat-stressed creatures will retreat deeper into their underground network (although food gets scarcer the deeper you go).
Controversial human intervention
A further possibility is that humans could intervene. In Pennsylvania, conservationists drilled new entrances into old mines and railroad tunnels where bats roost to encourage upwards air flow, allowing heat to escape. Interfering in this way has been controversial, but it , successfully slowing the growth of white nose fungus, which has of three North American bat species.
Troglobites might also be relocated. Entire cave communities have been transplanted twice already, in Brazil and the US, to escape destruction from mining, says Mammola. Conservationists can offer temporary sanctuary, too. In Slovenia, when heavy rains wash olms into the open, scientists rehabilitate them in and reintroduce them to caves within their species range.
Such measures may seem drastic, but cave biologists warn that we ignore the vertical dimension of climate change at our peril. Late last year, they because they make up a “keystone ecosystem… an essential component of planetary health”. Governments drawing up biodiversity plans have mostly ignored the underworld, they say. As a result, only 7 per cent of subterranean ecosystems globally are in protected areas.
This is where Mammola’s mapping project comes in. The project, funded with €1.7 million from the European Biodiversity Project Biodiversa+, aims to of the entire continent. At the Water Research Institute, shows me how DarCo is taking shape. With the click of a mouse, spots rain down on a map of Europe on his computer screen. This is the data being collected about which subterranean species have been found and where. He feeds it into a model that extrapolates to predict species distributions across undocumented regions. This is done using information on geology, precipitation and the extent to which the presence of one species predicts or excludes the presence of another. The next step, says Bellvert, is to apply sometimes ruthless reasoning about the feasibility of protecting each area. Places where extreme temperature rises are predicted or mining projects are planned may not be worth the effort – and it isn’t always worth saving a place whose species differ little from another, already conserved region.
The results, the DarCo scientists hope, will be used to inform regional and global conservation commitments, in particular the network of protected areas in the European Union and the bloc’s Biodiversity Strategy for 2030, which seeks to create protected zones for 30 per cent of its land and sea territories by the end of the decade. So far, only two-thirds of protected areas has been decided. The team wants to influence the remaining choices.
Protect and defend
Protection can’t prevent temperature rise, acknowledges Mammola. But it can reduce other environmental pressures that may drive a species over the edge. It can also shine a spotlight onto a long-ignored part of nature. Take Barrocal cave in Portugal’s Algarve region. A , the local municipality bought the land above it in 2021 and is working with scientists to create a legal framework to protect the cave and its inhabitants and build a long-term monitoring station. “These are local initiatives, but that’s also part of how you get to major things,” says Reboleira, who is leading the project.
Persuading people to conserve something critically important but full of unknowns makes for hard work, says Mammola. But there is no time to wait. “It means accepting the predominantly undefined nature [of the underworld],” he says. “It implies, quite literally, operating in the dark.”
Aisling Irwin is a freelance journalist based in Oxfordshire, UK
