Standing up to 30 metres tall, Madagascar's giant baobab trees have towered over the island for thousands of years - but as the large animals that used to spread their seeds have died out, the trees' survival is threatened. New research indicates that much smaller species have an unexpected role in helping baobabs thrive.
One of Madagascar's most photographed tourist sites is the Avenue of the Baobabs near the city of Morondava, in the west of the island, where giant, stately baobabs line a dirt road.
But the trees are endangered, partly because the megafauna that once dispersed their seeds are now extinct.
"The hypothesis in the first place was that they are orphan plants, meaning that without major seed dispersers like giant animals, their survival is challenging," says Seheno Andriantsaralaza, a researcher at the University of Antananarivo.
Baobabs like the ones growing in Morondava are known to science as Adansonia grandieri, or in Malgasy as renala. While baobabs in mainland Africa have elephants to eat and scatter their seeds, the so-called megafauna once reputed to have done that on behalf of renala baobabs - giant lemurs and giant tortoises - went extinct centuries ago.
Scientists say there's no evidence any of the large lemur species still living in Madagascar can break open the pods of renala baobabs, or chew off the chalky pulp surrounding each of the tiny brown seeds packed inside.
Caught on camera traps
To find out if the trees might be getting a helping hand from other, less charismatic Malagasy animals, a team led by Andriantsaralaza and her co-author Onja Razafindratsima conducted a four month-long study at two sites in the western Menabe region to find out which animals ate the fruit.
No animals or birds visited the baobab fruit while they were still on the tree, the team found, but when the large pods fell to the ground, native western tuft-tailed rats - small rodents with rich brown fur, elongated ears and a tuft of fur at the end of their long smooth tails - were caught on camera traps sniffing the fallen fruit and then eating the seeds.
It's still unclear if the rats can actually chew through the hard shells of the pods to reach the seeds, or simply prise open the shells of cracked fruit.
At least 40 percent of baobab pods crack open when they fall, giving "secondary dispersers" - animals without jaws strong enough to break through - an opportunity to prise out seeds.
Useful seed spreaders
As secondary dispersers the tuft-tailed rats appear to be compensating for the absence of larger, long-extinct animals, says Andriantsaralaza.
For instance, it's likely that the rats are stashing away baobab seeds beneath the soil, and occasionally forgetting about those caches. This allows the seeds to germinate far from the parent trees, where they have a higher rate of survival.
"Seed dispersal is important to ensure that the next generation [of baobabs] can colonise new sites, favourable sites, but also [so] they can avoid competition from the parent [plants]," says Andriantsaralaza.
Directly beneath the tree, where seedlings grow in clusters, the young baobab plants are also more susceptible to being eaten by grazing animals, she says.
Help from bushpigs
She and the team also found intact seeds in the dung of African bushpigs - a species of wild pig resembling a Eurasian wild boar that was introduced to Madagascar from Africa around 300 years ago.
That came as a surprise, says Andriantsaralaza.
When she did research at Anatananarivo Zoo as part of her PhD, she discovered that when captive bushpigs ate baobab fruit they crushed 100 percent of the seeds.
In the forest their chewing habits appear to be altered, though she's not sure why, and renala seeds pass through unbroken. That makes bushpigs another potential seed disperser.
When baobab seeds pass through the digestive tract of an animal they become more permeable to moisture and nutrients, and the dung in which they end up provides excellent fertilizer to boost their growth.
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Resisting deforestation
The findings are encouraging. Renala baobabs are threatened by deforestation in western Madagascar, and although there is no scientific evidence to suggest that overharvesting of their fruit to manufacture juice and cosmetics is a threat to the trees' survival, researchers like Andriantsaralaza want to mitigate against that possibility.
Up to 80 percent of renala fruits were collected by harvesters at the study sites surveyed by Andriantsaralaza and her team. She and other researchers, together with NGOs, local communities and the Malagasy government, are working to establish and enforce sustainable harvesting quotas.
"There is an urgent need for baobab conservation," she says, adding that it's important not to neglect the ecological interactions happening between the trees and nocturnal animals like the tuft-tailed rats.
"We need to conserve and protect both baobabs and their animal partners."
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