It was probably the trip of a lifetime. In 2012, biologists on an expedition to East Timor in southeast Asia spotted a brahminy blind snake wriggling out of somewhere quite unexpected: the rear end of a common Asian toad.
Mark O'Shea from the University of Wolverhampton in the UK and his colleagues witnessed the unusual event by chance after finding the pair under a rock. It is the first account of prey surviving digestion by a toad and of an animal as big as a blind snake emerging from a digestive tract alive.
"It's quite surprising that a vertebrate, which has lungs, was able to survive," says O'Shea.
Larvae and small marine invertebrates can pass through some predators unharmed. But larger prey items are likely to be chewed to death as soon as they enter an animal's jaws. Even if they somehow dodge this fate, travelling down the predator's throat in one piece can be a tight squeeze.
And there are bigger problems ahead. Most prey would not be able to survive exposure to the harsh gastric acids that break down tissue in a predator's stomach. Coping with the lack of available oxygen deep in the digestive system is another challenge.
For prey swallowed by a toad or a bird, however, chances of survival might be a little higher. These animals often push food to the back of their throat before swallowing it, which may boost the odds of safe entry into the digestive system.
This almost certainly helps explain how an incredibly toxic amphibian – the rough-skinned newt – can survive being swallowed by a frog. Once it enters the frog's stomach, the newt's toxins kill the frog before its digestive juices can really get to work. Then the newt simply has to crawl back up the dead frog's throat and out of its mouth.
Almost certainly the biggest problem the blind snake had to deal with was a prolonged lack of oxygen
But the brahminy blind snake did not kill its host – and it took a much longer path, through the gut, to exit the toad.
The snake may be better equipped for the journey than most species. With a long, slender body just a few millimetres wide, it effortlessly burrows through tiny holes and crevices in its environment. Passing through the narrow confines of a toad's digestive tract should not be too much of a challenge in principle.
O'Shea thinks the snake crawled through the toad's gut instead of simply being carried through by muscle contractions that move food along.
One factor that might have made that journey easier is the toad's earlier dining habits. It may not have eaten much in the hours before it swallowed the snake, meaning the path through its gut might have been clear. If so, the trip would have been a quicker one, reducing the snake's exposure to digestive acids.
But its skin was probably the biggest lifesaver. The closely-knit, overlapping scales that help blind snakes move on land would likely block gastric juices, preventing them from reaching delicate tissues and organs. The scales of other snakes come apart slightly when they move, so would not have the same protective effect.
Almost certainly the biggest problem the blind snake had to deal with was a prolonged lack of oxygen. As an underground dweller and due to its small size, it needs less air to survive than many animals. But still, there is a limit to how little it can tolerate. "Theoretically, the time it takes to get through the gut would determine if it lives or dies," says O'Shea.
Snails can endure the short digestive time without being fully exposed to the digestive juice
The researchers do not know how long it took the snake to journey through the toad's gut. But although they watched it wriggle out alive, it died about five hours later.
No post-mortem examination was carried out, but the researchers think the snake probably died from complications due to a lack of oxygen. "We couldn't think of anything else that would have killed it," says O'Shea.
Snails may be better gastric travellers than blind snakes, since they can survive on less oxygen.
In an experiment published in 2011, Shinichiro Wada from Tohoku University in Japan and colleagues fed tiny land snails, Tornatellides boeningi, to Japanese white-eye birds to see whether they could pass through their digestive system intact. About 15% survived the journey, which took between 20 and 120 minutes, proving for the first time that land snails can survive digestion. "Snails can endure the short digestive time without being fully exposed to the digestive juice," says Wada.
The snails' resistance is likely due to their shell, which provides them with natural armour. But Wada and his colleagues found that size was also key to survival. The shells of the species they examined, roughly 2.5mm wide, were recovered from bird faeces intact whereas those of larger species were usually broken into pieces. They think the snails may also produce mucus as additional protection from the acidic environment, but that idea still needs to be tested.
Larger snails seem to occasionally survive ingestion too, though. Jasna Simonova from Charles University in Prague, Czech Republic found that land snails with shells up to 17mm in diameter sometimes emerged alive from a variety of bird species. These much larger shells were left undamaged by digestion.
Mussels can pass through common sea anemones and avoid being digested if their shells are sealed shut
Another unexpected gut voyager is a species of nematode worm called Caenorhabditis elegans. Hinrich Schulenburg from the University of Kiel in Germany and his team found nematodes in the intestines of slugs collected in northern Germany. Later they were surprised to find the worms alive in the slugs' faeces.
"They seem to be taken up orally which is unusual because slugs have a grinder organ that should destroy them," says Schulenburg. "And we don't know how they survive the acidic conditions." Other types of nematodes have been found inside slugs and earthworms, but they are parasitic and usually enter through a puncture in the gut.
The team was also surprised to find that it was not just juvenile nematodes that survived the journey: adults did as well. Larvae have a tough outer layer to protect them during development, so are usually able to withstand harsher conditions than their fully formed elders. "It's still completely a puzzle," says Schulenburg. The nematodes seemed to survive the journey quite frequently although they never remained in the slug for longer than a day.
Gut travelling is rare on land but it seems to be more common in aquatic environments. Casper van Leeuwen from the Utrecht University in the Netherlands and colleagues found that some adult aquatic snails were still alive after passing through mallards. Females of a species of seed shrimp can also survive in the gut of white sucker fish, while mussels can pass through common sea anemones and avoid being digested if their shells are sealed shut.
Van Leeuwen and his team speculate that traits conducive to life in wet environments may help invertebrates stay alive in the moist internal world of the gut. Survival may also be aided by digestive systems that favour high prey intake over digestive efficiency, like those of some birds. Food passes through these animals faster, and some of it might emerge unprocessed.
Since trips through digestive systems seem to be reasonably common, it is possible that they have left their mark on some animal populations. They could be an important form of transport for less mobile species, enabling them to colonise locations far away.
These results strongly suggest that the land snails can be dispersed by predatory birds
This seems to be the case with the snails that Wada and his team observed. They were collected from Hahajima, one of the Ogasawara Islands in Japan. Their pattern of distribution on the surrounding islands seemed to make sense only for an animal with wings.
And evidence of gene transfer between geographically distant snail populations could also be explained by gut transport. Wada's team found that areas with a high density of Japanese white-eye birds, the species in which the snails were able to survive, also contained more genetically diverse snails.
"These results strongly suggest that the land snails can be dispersed by predatory birds," says Wada. Furthermore, they witnessed one snail give birth after emerging from a bird's rear end, implying that the migration of just one snail is enough to start a new population.
Schulenburg suspects that nematode worms could be hitching a ride in slug guts, too. They are already known to cling on to the legs of woodlice to move from one place to another. Another possibility is that the slug's gut itself is appealing to the worms: they may be targeting its gut bacteria as a source of food. "It's also possible that they wait until the slug dies to feed on bacteria that live on the carcass," says Schulenburg.
One of the first cases of an insect using internal transport was documented in 2014 by Jan-Jakob Laux from the University of Hamburg in Germany and his team. They suspect that the eggs of an aquatic leaf beetle, Macroplea mutica, are being dispersed by mallard ducks since they can emerge from their digestive system intact. The insects' wide distribution across the Palearctic region has long been a mystery since they are not very mobile.
In the case of the blind snake, however, its voyage was probably an accident. O'Shea thinks the toad mistook it for an earthworm, one of its typical prey. "I'm certain the toad didn't know it was swallowing a vertebrate," he says. "It thought it was a shiny worm."
I think it's more likely they were brought up by accident through the gut of an owl
Other types of toads are known to hunt blind snakes, but they never escape alive once eaten. However, blind snakes may use the gut of another animal as a mode of transport: the owl.
There have been several reports of the snakes turning up in owls' nests. How they get there is unclear. Some researchers suggest that they climb up trees to feed on invertebrates living in nest detritus. According to another theory, the owls carry them to the nest as food for their fledglings.
Although O'Shea doesn't doubt their climbing ability, blind snakes would have to locate the nest first or be ending up there by chance. And an owl would be hard-pressed to feed a blind snake to its young: the snakes curl up in knots when touched and would probably wriggle quickly deep into a nest when dropped.
"I think it's more likely they were brought up by accident through the gut of an owl," says O'Shea. Like toads, owls often gulp back prey without chewing it.
If predators are unknowingly ingesting living animals, are there any implications for their health? Intestinal parasites, for example, often enter an animal with food and water and then take up residence in the gut. Schulenburg thinks that the nematode worm species – C. elegans – that he found in the intestines of slug could in fact be a parasite. "It would be exciting if it was," he says. "I think it's possible."
Some nematode species are true parasites, whereas others can switch between free-living and parasitic lifestyles. C. elegans is assumed to be non-parasitic – evidence that it can be parasitic could provide insight into the ways animals evolve into parasites.
The toad just appeared to be embarrassed
"It would be an exciting system to study adaptations and molecular mechanisms that allow organisms to become parasites and what kinds of traits are required to sometimes live as a parasite and sometimes not," says Schulenburg. As one of the simplest animals with a nervous system, C. elegans is already a model organism frequently used in research.
Wada also thinks that parasitism could be involved in the interaction between land snails and birds. He found parasitic flatworms living off many of the land snails he studied and thinks that birds could be their final host. Perhaps the flatworms are sneakily using the snails as a sort of Trojan Horse to gain access to the duck's intestines. "I am currently studying the relationship," says Wada.
However, gastric travellers may not just be exploiting predators for their own good: they could have a positive impact on them as well. Schulenburg thinks that by feeding on the bacteria inside slug guts, C. elegans nematodes could influence the microbial community in a positive way. "Some bacteria-feeding organisms help improve diversity within the microbiome," he says.
The brahminy blind snake, however, probably had little impact on the toad that ate it, beyond the strange feeling of having an animal move through its stomach and intestines. "The toad just appeared to be embarrassed," says O'Shea. After all, it had a snake sticking out of its bottom.