The cup of a pitcher plant looks simple. But it is a deadly trap.

Pitcher plants lure insects with sweet-smelling nectar. When the insects arrive to feast, they slide into the pitcher’s deadly pool.

The liquid inside the pitcher is like the plant version of a stomach, brimming with digestive juices that can break down hundreds of insects at a time.

While most devour insects, some have more specialised tastes

Darwin coined this taste for animals the “carnivorous syndrome”. It evolved numerous times in plants, and always for the same reason. When plants ended up in soil that lacked nitrogen, a key ingredient plants need to make proteins and DNA, the plants developed a taste for nitrogen-rich flesh.

But recent studies are revealing there is much more to these huge meat-eating plants, which can grow stems up to six metres long, flowers that are one metre tall, traps more than 40 centimetres deep, and can hold two litres of flesh-digesting liquid.

While most devour insects, some have more specialised tastes. Others collaborate in odd ways with animals, which use them as a place to stay. A few have even harnessed the power of bacteria to better digest and consume the flesh of their victims.

 

Most pitcher plants devour insects, and evolution has shaped the three parts of a pitcher to each perform a precise task that ensures an insect’s demise.

At the top of the pitcher is a lid called an operculum. The lid keeps out rainwater that would otherwise dilute the digestive juices.

The slippery rim of the pitcher is known as the peristome.

The pitcher species Nepenthes rajah of Borneo is large enough to drown a rat

“It has lots of grooves, and a microstructure that makes it so insects can not attach to it that well,” explains Dr Tanya Renner who studied pitcher plants for her PhD, and will continue to explore them as a professor at San Diego State University, beginning August of 2015. She is currently a post-doctoral student at the University of Arizona.

The rim is very ‘wettable’, she adds. In other words, “when water touches it, it makes it very slippery.”

Once an insect slips into the pitcher pool, the inside of the pitcher is extremely waxy. “It’s like ice-skating on a leaf surface,” she says, and the bugs can’t get any traction to crawl out.

Even flying insects rarely escape. If a bug doesn’t drown immediately, the sugars and digestive juices give the liquid a tackiness that makes flying with wet wings very difficult.

The training of the shrew

But one tropical pitcher plant species, Nepenthes lowii, tends to be curiously lacking in insects.

Instead, this plant’s pitchers fill with faeces from a much larger prey: Tupaia montana, the montane tree shrew.

To see if the pitcher plants had developed a mutually beneficial relationship with the shrew, in 2009 a team of scientists led by Dr Jonathan Moran of Royal Roads University in Canada, travelled to the montane cloud forest of Malaysia where N. lowii grows.

An individual plant of N. lowii has two types of pitchers: terrestrial pitchers along the ground, and aerial pitchers held in the air.

Tree shrews perch on the pitcher and lick sugary juice from its rim

By remotely videotaping these plants during the day, the team confirmed that only the terrestrial pitchers catch insects. Videos showed the aerial pitchers are visited by the tree shrew, which eats nectar the plant produces on its rim.

While the tree shrew feeds, it often defecates into the pitcher. The faeces is very nitrogen-rich, and would be extremely useful to the plant.

To determine if the plants were able to incorporate nitrogen from the tree shrew droppings, the scientists conducted a stable-isotope analysis on the pitcher’s leaves, a technique that tracks the origin of an element. The team concluded that N. lowii plants with aerial pitchers derive 57-100% of their nitrogen from this shrew poo.

This study revealed the first known mutualism between a carnivorous plant and a mammal. The discovery sparked a sudden scientific interest in the giant plants that eat meat.

For example, the pitcher species Nepenthes rajah of Borneo is large enough to drown a rat.

Just like the inside of a newborn baby, each nubile pitcher begins its life completely free of microbes

That sparked speculation that some plants actually killed and ate the flesh of mammals.

In 2011, a different band of scientists from Germany and Malaysia headed to Borneo to monitor this giant pitcher plant.

Like the previous study, the scientists filmed pitcher plants to reveal who visited them. But instead of only filming nighttime visitors, this group split their recording time between day and night.

They found that, during the day, tree shrews perch on the pitcher and lick sugary juice from the pitcher rim, then defecate directly into it.

After the sun sets, the nocturnal rat Rattus baluensis feeds in the same way, trading sweet juice for nitrogen-rich faeces. The same pitcher plant species forms multiple symbioses with mammals, separated only by the time of day.

During the course of the two-month study, only one mammal actually drowned in a pitcher plant. The pitcher plants probably aren’t intending to kill rodents, though creepily enough, despite the presence of the rat corpse, other animals still sought nectar and used the pitcher lavatory.

But the rat cadaver could have deterred a different creature: bats.

The bat cave

A few scientists had glimpsed bats sleeping in tropical pitcher plants over the years.

But until the tree shrew studies were published, most scientists assumed the bats were simply freeloaders, exploiting the pitchers as free motels when they failed to reach their permanent roost by sunrise.

It took a bat-loving science duo, doctoral students Caroline and Michael Schöner, to show that the bats are actually loyal, paying customers.

The plants are really benefiting from the bats

The duo travelled to the lowland forests of Borneo in search of the pitcher plant Nepenthes hemsleyana. This species had been observed hosting woolly bats (Kerivoula hardwickii hardwickii), and a few clues hinted the plants had evolved to entice bat tenants.

N. hemsleyana is up to seven times worse at catching insects than its close cousin, N. rafflesiana and N. hemsleyana pitchers are up to four times longer, too. This increased length would allow a lanky bat to fit much more comfortably.

Once the Schöners knew which pitcher types to look for, the bats were easy to find. In just six weeks, the team found 32 different woolly bats roosting in pitchers. The woolly bat is the only bat species they found roosting in pitchers.

Michael and Caroline then placed trackers on 17 of the bats, to quantify how much the bats use the pitcher plants as daytime roosts.

What they found was surprising: the woolly bats exclusively use N. hemsleyana pitchers as daytime roosts. Though the forest holds many other bat-motel options, such as furled leaves or hollow trees, to the woolly bat, pitcher plants are home.

The bats are good homemakers, too. “Stable isotope analysis showed the plants are really benefiting from the bats,” Caroline says. N. hemsleyana reaps about a third of the nitrogen in its leaves from woolly bat faeces. The study was published in Biology Letters.

This type of mutualism is very rare.

When plants and animals usually collaborate, the plants provide food in exchange for services. Plants might supply nutritious nectar or fruit, for example, and in return animals visit the plants to feed, distributing pollen or seeds when they leave.

With pitcher plants, the roles are reversed: the plant receives nutritious nitrogen, and the animal receives services such as protection from predators and weather.

Caroline and Michael Schöner are supervised by Dr Gerald Kerth of the University of Greifswald in Germany and Dr T Ulmar Grafe from the University of Brunei in Darussalam. Together, the group is working to better understand this exceptional mutualism.

The team launched a second monitoring experiment that was much longer, and explored more field sites across Borneo. This research revealed the bats also sometimes roost in a second Nepenthes species, N. bicalcarata.

After a plant senses an insect in its pitcher it produces enzymes

Bats have their reasons for preferring to roost in N. hemsleyana, the team discovered. N. hemsleyana pitchers create a better microclimate for the bats, keeping a more stable and higher humidity than pitchers of N. bicaclarata.

“The bats have a huge wing membrane,” notes Caroline, and it is through this membrane that bats lose a lot of their water. A pitcher roost that maintains a higher humidity can be a huge plus to a bat battling dehydration.

Unhealthy bats can also suffer from ectoparasites.

Bats that only roosted in N. hemsleyana were completely free of parasites, unlike bats that spent time in N. bicalcarata, the other pitcher species. Unlike N. bicalcarata, N. hemsleyana pitchers have a slippery waxy zone on their inner surface, which makes it difficult for parasites to lay eggs on the pitcher walls.

Bats that preferred to roost in N. hemsleyana were in better overall condition, being larger, heavier, and free of parasites.

So, why do bats bother with N. bicalcarata at all?

This inferior pitcher roost is simply more common and a tired bat can’t always be a choosy bat.

Other factors influence bat decision-making, too, such as the pitcher’s distance from the ground, or exposure to rain and sunlight and the Schöners discovered then when possible, the bats did demonstrate a loyalty for resettling in different N. hemsleyana pitchers.

The second study was published in the journal Oecologia, and more publications are soon to follow.

Chemical warfare

In order to digest the insects they trap, pitcher plants have to be talented chemists. They produce proteins called enzymes to break down their insect prey.

“Insects are like little tanks,” explains Dr Renner.

The armour-like exoskeleton of an insect is made out of a very sturdy protein called chitin. Chitin has a complicated structure immune to most general enzymes.

After a plant senses an insect in its pitcher it first produces enzymes called chitinases. Only these enzymes can cut a chink in the insect’s chitin armour.

Once the armour has been compromised, the plant launches a second wave of enzymes. These mostly fall into three categories: proteases that break down proteins, lipases that reduce fat, and esterases that attack a range of other compounds.

The plant enzymes are highly specific, which led Dr Renner to wonder how the plants acquired such advanced weaponry.

“The majority of them look really similar to enzymes that plants use in defence,” says Dr Renner. “Non-carnivorous plants have to protect themselves against all sorts of things.”

Plants often must defend themselves against disease-causing fungi such as moulds. The fungi possess sturdy cell walls with a familiar key ingredient: chitin.

Both fungi and insects use chitin as part of their armour against chemical weapons.

Dr Renner’s research, published in the journal Molecular Biology and Evolution, shows the early ancestors of pitcher plants co-opted common defence proteins that kill fungi, to be able to digest insect exoskeletons.

A microbial army

But some pitcher species appear to enlist microbes to manufacture enzymes for them.

Leonora Bittleston is a PhD student at Harvard University in the US, studying both Nepenthes pitcher plants in Borneo, and an unrelated pitcher plant genus Sarracenia that grows in Harvard Forest, Massachusetts.

Just like the inside of a newborn baby, each nubile pitcher begins its life completely free of microbes. As the pitcher opens, resilient bacteria, fungi, protozoa, and even aquatic insects drift into the pitcher fluid, making a living in the dangerous fluid.

And much like the microbes that live inside the human gut, the tiny critters inside the pitcher fluid help the host absorb additional nutrients from their food.

The Sarracenia pitcher plants that grow in Harvard Forest may rely exclusively on microbial mutualists to digest their insect prey. In short, they get bacteria to dissolve the flesh of their victims rather than doing it themselves.

“So far there is no evidence that Sarracenia make their own chitinases,” Leonora explains. Fungal yeast and bacteria do make chitinases, however, and Leonora’s research suggests those are the microbes that have the largest effect on Sarracenia health.

Leonora is one of the first researchers to study the tiny communities that assemble inside pitcher plants. Her first pitcher plant study describes the methods she developed to compare communities inside the pitcher fluid, and is being published in Austral Ecology.

Even as tropical pitcher plant habitats are being destroyed at record rates, scientists and explorers are discovering new pitcher plant species in Borneo and the Philippines.

“Especially in the mountainous areas, I think there are several species not yet discovered, and what they do… nobody knows,” says Caroline Schöner.