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The Borneo Hills Diet: A radical plan for carnivores
The Borneo Hills diet Instead of catching insects, a few carnivorous plants have resorted to hunting a rather more unusual prey. Stephanie Pain reveals all
MYN / Joris van Alphen/naturepl
H
IGH in the misty mountains of Borneo, death awaits the unsuspecting wanderer. This is the lair of the most awesome of the pitcher plants, with fearsome traps and a reputation to match. The pitcher plants of south-east Asia are famed for their carnivorous habits. These merciless killers lure insects to the top of their traps with sweet nectar, where many lose their grip on the ultra-slippery rim and fall into the fluid-filled trap. As the victims desperately try to climb out, they discover too late that this is no ordinary fluid – it is filled with invisible stretchy fibres, and the more an insect struggles, the more entangled it becomes. Sooner or later the trapped animals drown, and digestive enzymes in the fluid accelerate the breakdown of their rotting corpses. Only then does the plant gets its reward: nitrogen, a key nutrient that is in short supply in the places where these killers lurk. Small insects, particularly ants, are the usual prey of the 120 or so species of Nepenthes plants. But the island of Borneo is home to several spectacular species with unusually shaped giant pitchers. The largest, Nepenthes rajah, has jug-like pitchers so big they can hold several litres of fluid, and its appetite is legendary. In the century-anda-half since its discovery, there have been sporadic reports of it catching rats. So has the “king” of carnivorous plants really evolved to catch small mammals? After staking out the giant pitchers and mounting 24-hour surveillance, ecologists have discovered that the truth is even stranger than this. It turns out that N. rajah and at least three other pitcher plants in Borneo have indeed evolved to lure small mammals into their traps – but not to kill them… One of the first to suspect that some pitcher plants do things differently was Charles >
Nepenthes lowii has a strange but fruitful relationship with a mammal 1 February 2014 | NewScientist | 43
Safe haven
oozing from the lid. With a few wipes of a muscular tongue, the lids are clean and the tree shrews scamper off unharmed. It is all over in seconds. So N. lowii does not prey on shrews. But it does not go unrewarded: the footage revealed that the tree shrews sometimes pooped in the pitcher. Clarke had noted on his earlier expedition that the pitchers contained few insects but a lot of droppings. The video evidence suggested that this is no accident: N. lowii not only looks like a toilet – it is a toilet for tree shrews.
The pitcher plant Nepenthes hemsleyana has evolved to provide a safe roosting place for woolly bats
N. hemsleyana
BAT
Closely related species
An unusual relationship
LONGER PITCHER
“The orientation of the lid forces the tree shrew to position its rear end over the pitcher’s mouth while feeding,” says Moran. “That increases the chances of faeces being captured if the animal defecates while it’s on the pitcher.” It also means that any droppings left sticking to the walls of the pitcher are flushed to the bottom when it rains. With tree shrews weighing around 150 grams, this also explains why the pitchers are more robust than those of insect catchers. “If they weren’t reinforced they’d probably snap off,” says Moran. To the ecologists it seemed they had discovered an unusual and mutually beneficial relationship between a plant and a vertebrate. The pitcher plants provide tree shrews with a meal rich in carbohydrates in exchange for the occasional nitrogen-rich dropping. The clinching evidence came from an analysis of the source of the nitrogen in the plants. It showed that between 60 and 100 per cent of it came from shrew
THICK “GIRDLE” LOWER FLUID LEVEL 5cm
44 | NewScientist | 1 February 2014
the veggie option
Ch’ien Lee/Minden Pictures
Clarke of Monash University Malaysia. During an expedition to Mount Pagon in north-west Borneo in the 1990s, he took a close look at one of the weird giant pitcher plants, called N. lowii (pictured on page 45). He noticed that its pitchers lack the slippery rim and smooth inner walls that help trap insects. N. lowii is odd in other ways too: the rim is unusually narrow and the mouth unusually broad, while the leafy lid that normally keeps out rain is angled up and away from the opening. And while other pitchers secrete nectar from glands around the rim, this plant oozed much larger quantities of thicker, buttery nectar from the underside of its lid. Finally, the whole structure – both the pitcher and the tendril it dangles from – is reinforced with woody lignin. All this suggests that this plant has evolved to attract something larger and heavier than insects to its pitchers. “Growing pitchers is costly for a plant, so if the pitcher is much bigger than required you have to ask why,” says Jonathan Moran of Royal Roads University in Canada. Could its prey be a nectar-sipping bird? Or a sweet-toothed mammal? In 2008, Clarke, Moran and colleagues found the answer in the cloud forest of Gunung Mulu in another part of Borneo. Keeping watch on N. lowii pitchers they found only one vertebrate visited them: the mountain tree shrew, Tupaia montana. Intrigued, Ulrike Bauer, a member of the team from the University of Cambridge, set up cameras. Her footage revealed how tree shrews leap onto the pitcher’s narrow rim and grip it with their hind feet before stretching up, across the yawning chasm to reach the nectar
droppings (Biological Letters, vol 5, p 632). Poo might seem the perfect fertiliser for a plant, but in fact mammal faeces are not as rich in nitrogen as ants are. So why would a pitcher evolve to capture faeces rather than insects? For a mountain plant there is good reason to seek alternative supplies of nitrogen: the density of ants and other insects diminishes with increasing altitude. Tree shrew droppings are also richer in nitrogen than those of most mammals, because they have short guts that do not extract all the nutrients from their food. Plus the speedy throughput means tree shrews make frequent deposits. The strategy definitely works. The team’s analysis of leaf tissue showed that N. lowii has a higher nitrogen content than insect-eating pitcher plants growing in the same habitat. With the shortage of insects at altitude, it seemed likely other Nepenthes growing on mountains might have adopted a similar strategy. Sure enough, two more large species have been found to exploit the tree shrew’s productive bowels. N. macrophylla, a close relative of N. lowii that grows on Mount Trusmadi, and N. rajah – the notorious “rat-catcher” of Mount Kinabalu – catch both insects and droppings. Although these two plants hedge their bets with a dual-fuel policy, all three “toilet pitchers” share a unique set of features to ensure visiting tree shrews pay up after they’ve finished eating. All have large mouths and a large concave lid poised at about 90° from the pitcher’s rim. The arrangement means tree shrews must approach the lid face on. Most crucially, the distance between the front of the pitcher and the farthest point on
Poo-eating pitcher plants aren’t alone in adopting a radically different diet (main story). One species is turning vegetarian. Nepenthes ampullaria grows in lowland forests rather than the open habitats more typical of pitcher plants. It forms dense carpets of pitchers on the ground (left). These pitchers are unusually broad-mouthed, lack the normal insect-trapping features and have vestigial lids that grow away from the mouth instead of sheltering it. The clusters of pitchers present a sea of gaping mouths – and with good reason. Under the forest canopy, a constant supply of nitrogen rains down in the form of falling leaves and other plant debris. These pitchers have evolved to intercept this nitrogen bonanza before it reaches the ground and becomes available to other plants. Leaf litter isn’t the richest source of nitrogen but it is reliable and this species gets a third of its nitrogen this way.
the curve of the lid precisely matches the head-and-body length of an adult tree shrew, Clarke and colleagues reported in 2010. Reaching to get the last drops of nectar, tree shrews cannot help but position themselves with their rear ends over the bowl. So far, so neat, but N. rajah (pictured right) had another surprise in store. When Clarke returned to Mount Kinabalu in 2010 to learn more about tree shrew toilet habits, the team discovered more than one sort of dropping in the pot. The tree shrews’ were dark and malodorous. The others were paler and less smelly. No matter how long the ecologists watched during the day, the only visitors they saw were tree shrews. Perhaps the mystery mammal only appeared after dark? To find out, the team left cameras running through the night and finally unmasked the second
Yes, the tree shrew is doing what you think it is on N. raja
visitor: it was the summit rat, Rattus baluensis. The rat, much the same size as a tree shrew, is also a prolific pooper (PLoS ONE, vol 6, e21114). This could explain the reports of N. rajah eating rats. “The stories stem from clumsy rats or tree shrews that lost their footing when feeding and slipped in,” says Moran. And the discoveries keep on coming. Down in the lowland peat forests of Brunei, another pitcher plant has adapted its traps to collect faeces, but has gone about it in a very different way. Instead of luring animals with nectar, N. hemsleyana provides them with accommodation. Once ensconced, the lodgers, tiny bats, have a habit of pooing on their bedroom floor. When Ulmar Grafe at the University of Brunei Darussalam first found a Hardwicke’s woolly bat inside the pitcher of an N. hemsleyana he thought it was a one-off. But then Grafe read that these pitchers trap far fewer insects than those of other species. Grafe and his students began to patrol more than 400 of these pitchers each day and, over seven weeks of monitoring, they found that one in five pitchers played host to at least one bat. Some contained two bats, a mother and young. Analysis of leaf tissue showed that around 34 per cent of the plants’ nitrogen content came from woolly-bat droppings. Here was another unusual partnership. The team discovered that some woolly bats also roost in another species of pitcher, but because there is not enough space for them above the fluid, they roost only in dead or dying pitchers whose fluid has drained out. These plants therefore get no benefit. A few other animals, from mosquito larvae
Ch’ien Lee/Minden Pictures
”Growing pitchers is costly, so if they are bigger than required to catch insects you have to ask why”
and tadpoles to spiders and ants, have taken to living inside pitchers, but most appear to be uninvited guests. The pitchers of N. hemsleyana, by contrast, have evolved to accommodate bats in comfort and safety in exchange for regular dollops of dung (see diagram, page 44). The pitchers are longer and have a much lower fluid level than those of closely related species, providing ample room for two bats stacked one above the other. The walls also have a “girdle” of thick tissue that allows bats to wedge themselves in the pitcher a safe distance above the fluid. “Bats only use pitchers of the right dimensions,” Grafe notes. Rather than being shaped to trap and kill, then, these pitchers protect their lodgers. And the living pitchers of N. hemsleyana provide healthier homes than empty pitchers. The temperature is more stable, and cooler during the hottest part of the day. The fluid also keeps the air humid, helping to prevent dehydration in its minuscule lodgers. Not only do the bats prefer N. hemsleyana, Grafe’s team reported last year, but those that roost only in its
pitchers are bigger and in better shape than those roosting in other pitchers. Why, though, would a plant that grows where insects are plentiful go to such lengths to acquire nitrogen from another source? Although there is less pressure pushing lowland species to exploit alternative nitrogen sources, it clearly happens occasionally (see “The veggie option”, left). Nitrogen may be more easily assimilated from faeces, suggests Grafe, plus the plants don’t need to produce as much nectar to attract insects. Whatever the reasons, in the past few years it has become clear that a few pitcher plants have branched out from preying on insects, tweaking their traps to exploit other sources of essential nutrients. A lot of new species are being discovered and some have unusual shapes, says Moran. “Are there other weird nutrient strategies out there awaiting discovery? I suspect that Nepenthes may still have a few surprises in store for us.” n Stephanie Pain is a consultant for New Scientist 1 February 2014 | NewScientist | 45
MYN / Joris van Alphen/naturepl
H
IGH in the misty mountains of Borneo, death awaits the unsuspecting wanderer. This is the lair of the most awesome of the pitcher plants, with fearsome traps and a reputation to match. The pitcher plants of south-east Asia are famed for their carnivorous habits. These merciless killers lure insects to the top of their traps with sweet nectar, where many lose their grip on the ultra-slippery rim and fall into the fluid-filled trap. As the victims desperately try to climb out, they discover too late that this is no ordinary fluid – it is filled with invisible stretchy fibres, and the more an insect struggles, the more entangled it becomes. Sooner or later the trapped animals drown, and digestive enzymes in the fluid accelerate the breakdown of their rotting corpses. Only then does the plant gets its reward: nitrogen, a key nutrient that is in short supply in the places where these killers lurk. Small insects, particularly ants, are the usual prey of the 120 or so species of Nepenthes plants. But the island of Borneo is home to several spectacular species with unusually shaped giant pitchers. The largest, Nepenthes rajah, has jug-like pitchers so big they can hold several litres of fluid, and its appetite is legendary. In the century-anda-half since its discovery, there have been sporadic reports of it catching rats. So has the “king” of carnivorous plants really evolved to catch small mammals? After staking out the giant pitchers and mounting 24-hour surveillance, ecologists have discovered that the truth is even stranger than this. It turns out that N. rajah and at least three other pitcher plants in Borneo have indeed evolved to lure small mammals into their traps – but not to kill them… One of the first to suspect that some pitcher plants do things differently was Charles >
Nepenthes lowii has a strange but fruitful relationship with a mammal 1 February 2014 | NewScientist | 43
Safe haven
oozing from the lid. With a few wipes of a muscular tongue, the lids are clean and the tree shrews scamper off unharmed. It is all over in seconds. So N. lowii does not prey on shrews. But it does not go unrewarded: the footage revealed that the tree shrews sometimes pooped in the pitcher. Clarke had noted on his earlier expedition that the pitchers contained few insects but a lot of droppings. The video evidence suggested that this is no accident: N. lowii not only looks like a toilet – it is a toilet for tree shrews.
The pitcher plant Nepenthes hemsleyana has evolved to provide a safe roosting place for woolly bats
N. hemsleyana
BAT
Closely related species
An unusual relationship
LONGER PITCHER
“The orientation of the lid forces the tree shrew to position its rear end over the pitcher’s mouth while feeding,” says Moran. “That increases the chances of faeces being captured if the animal defecates while it’s on the pitcher.” It also means that any droppings left sticking to the walls of the pitcher are flushed to the bottom when it rains. With tree shrews weighing around 150 grams, this also explains why the pitchers are more robust than those of insect catchers. “If they weren’t reinforced they’d probably snap off,” says Moran. To the ecologists it seemed they had discovered an unusual and mutually beneficial relationship between a plant and a vertebrate. The pitcher plants provide tree shrews with a meal rich in carbohydrates in exchange for the occasional nitrogen-rich dropping. The clinching evidence came from an analysis of the source of the nitrogen in the plants. It showed that between 60 and 100 per cent of it came from shrew
THICK “GIRDLE” LOWER FLUID LEVEL 5cm
44 | NewScientist | 1 February 2014
the veggie option
Ch’ien Lee/Minden Pictures
Clarke of Monash University Malaysia. During an expedition to Mount Pagon in north-west Borneo in the 1990s, he took a close look at one of the weird giant pitcher plants, called N. lowii (pictured on page 45). He noticed that its pitchers lack the slippery rim and smooth inner walls that help trap insects. N. lowii is odd in other ways too: the rim is unusually narrow and the mouth unusually broad, while the leafy lid that normally keeps out rain is angled up and away from the opening. And while other pitchers secrete nectar from glands around the rim, this plant oozed much larger quantities of thicker, buttery nectar from the underside of its lid. Finally, the whole structure – both the pitcher and the tendril it dangles from – is reinforced with woody lignin. All this suggests that this plant has evolved to attract something larger and heavier than insects to its pitchers. “Growing pitchers is costly for a plant, so if the pitcher is much bigger than required you have to ask why,” says Jonathan Moran of Royal Roads University in Canada. Could its prey be a nectar-sipping bird? Or a sweet-toothed mammal? In 2008, Clarke, Moran and colleagues found the answer in the cloud forest of Gunung Mulu in another part of Borneo. Keeping watch on N. lowii pitchers they found only one vertebrate visited them: the mountain tree shrew, Tupaia montana. Intrigued, Ulrike Bauer, a member of the team from the University of Cambridge, set up cameras. Her footage revealed how tree shrews leap onto the pitcher’s narrow rim and grip it with their hind feet before stretching up, across the yawning chasm to reach the nectar
droppings (Biological Letters, vol 5, p 632). Poo might seem the perfect fertiliser for a plant, but in fact mammal faeces are not as rich in nitrogen as ants are. So why would a pitcher evolve to capture faeces rather than insects? For a mountain plant there is good reason to seek alternative supplies of nitrogen: the density of ants and other insects diminishes with increasing altitude. Tree shrew droppings are also richer in nitrogen than those of most mammals, because they have short guts that do not extract all the nutrients from their food. Plus the speedy throughput means tree shrews make frequent deposits. The strategy definitely works. The team’s analysis of leaf tissue showed that N. lowii has a higher nitrogen content than insect-eating pitcher plants growing in the same habitat. With the shortage of insects at altitude, it seemed likely other Nepenthes growing on mountains might have adopted a similar strategy. Sure enough, two more large species have been found to exploit the tree shrew’s productive bowels. N. macrophylla, a close relative of N. lowii that grows on Mount Trusmadi, and N. rajah – the notorious “rat-catcher” of Mount Kinabalu – catch both insects and droppings. Although these two plants hedge their bets with a dual-fuel policy, all three “toilet pitchers” share a unique set of features to ensure visiting tree shrews pay up after they’ve finished eating. All have large mouths and a large concave lid poised at about 90° from the pitcher’s rim. The arrangement means tree shrews must approach the lid face on. Most crucially, the distance between the front of the pitcher and the farthest point on
Poo-eating pitcher plants aren’t alone in adopting a radically different diet (main story). One species is turning vegetarian. Nepenthes ampullaria grows in lowland forests rather than the open habitats more typical of pitcher plants. It forms dense carpets of pitchers on the ground (left). These pitchers are unusually broad-mouthed, lack the normal insect-trapping features and have vestigial lids that grow away from the mouth instead of sheltering it. The clusters of pitchers present a sea of gaping mouths – and with good reason. Under the forest canopy, a constant supply of nitrogen rains down in the form of falling leaves and other plant debris. These pitchers have evolved to intercept this nitrogen bonanza before it reaches the ground and becomes available to other plants. Leaf litter isn’t the richest source of nitrogen but it is reliable and this species gets a third of its nitrogen this way.
the curve of the lid precisely matches the head-and-body length of an adult tree shrew, Clarke and colleagues reported in 2010. Reaching to get the last drops of nectar, tree shrews cannot help but position themselves with their rear ends over the bowl. So far, so neat, but N. rajah (pictured right) had another surprise in store. When Clarke returned to Mount Kinabalu in 2010 to learn more about tree shrew toilet habits, the team discovered more than one sort of dropping in the pot. The tree shrews’ were dark and malodorous. The others were paler and less smelly. No matter how long the ecologists watched during the day, the only visitors they saw were tree shrews. Perhaps the mystery mammal only appeared after dark? To find out, the team left cameras running through the night and finally unmasked the second
Yes, the tree shrew is doing what you think it is on N. raja
visitor: it was the summit rat, Rattus baluensis. The rat, much the same size as a tree shrew, is also a prolific pooper (PLoS ONE, vol 6, e21114). This could explain the reports of N. rajah eating rats. “The stories stem from clumsy rats or tree shrews that lost their footing when feeding and slipped in,” says Moran. And the discoveries keep on coming. Down in the lowland peat forests of Brunei, another pitcher plant has adapted its traps to collect faeces, but has gone about it in a very different way. Instead of luring animals with nectar, N. hemsleyana provides them with accommodation. Once ensconced, the lodgers, tiny bats, have a habit of pooing on their bedroom floor. When Ulmar Grafe at the University of Brunei Darussalam first found a Hardwicke’s woolly bat inside the pitcher of an N. hemsleyana he thought it was a one-off. But then Grafe read that these pitchers trap far fewer insects than those of other species. Grafe and his students began to patrol more than 400 of these pitchers each day and, over seven weeks of monitoring, they found that one in five pitchers played host to at least one bat. Some contained two bats, a mother and young. Analysis of leaf tissue showed that around 34 per cent of the plants’ nitrogen content came from woolly-bat droppings. Here was another unusual partnership. The team discovered that some woolly bats also roost in another species of pitcher, but because there is not enough space for them above the fluid, they roost only in dead or dying pitchers whose fluid has drained out. These plants therefore get no benefit. A few other animals, from mosquito larvae
Ch’ien Lee/Minden Pictures
”Growing pitchers is costly, so if they are bigger than required to catch insects you have to ask why”
and tadpoles to spiders and ants, have taken to living inside pitchers, but most appear to be uninvited guests. The pitchers of N. hemsleyana, by contrast, have evolved to accommodate bats in comfort and safety in exchange for regular dollops of dung (see diagram, page 44). The pitchers are longer and have a much lower fluid level than those of closely related species, providing ample room for two bats stacked one above the other. The walls also have a “girdle” of thick tissue that allows bats to wedge themselves in the pitcher a safe distance above the fluid. “Bats only use pitchers of the right dimensions,” Grafe notes. Rather than being shaped to trap and kill, then, these pitchers protect their lodgers. And the living pitchers of N. hemsleyana provide healthier homes than empty pitchers. The temperature is more stable, and cooler during the hottest part of the day. The fluid also keeps the air humid, helping to prevent dehydration in its minuscule lodgers. Not only do the bats prefer N. hemsleyana, Grafe’s team reported last year, but those that roost only in its
pitchers are bigger and in better shape than those roosting in other pitchers. Why, though, would a plant that grows where insects are plentiful go to such lengths to acquire nitrogen from another source? Although there is less pressure pushing lowland species to exploit alternative nitrogen sources, it clearly happens occasionally (see “The veggie option”, left). Nitrogen may be more easily assimilated from faeces, suggests Grafe, plus the plants don’t need to produce as much nectar to attract insects. Whatever the reasons, in the past few years it has become clear that a few pitcher plants have branched out from preying on insects, tweaking their traps to exploit other sources of essential nutrients. A lot of new species are being discovered and some have unusual shapes, says Moran. “Are there other weird nutrient strategies out there awaiting discovery? I suspect that Nepenthes may still have a few surprises in store for us.” n Stephanie Pain is a consultant for New Scientist 1 February 2014 | NewScientist | 45