Declining dung imperils custard apples

For a tropical custard apple tree species, bigger is definitely better, as new research reveals that smaller herbivores such as deer and gibbons are no match for elephants when it comes to dispersing its seeds.

It’s a very efficient evolutionary strategy – except when the big animals start to disappear.

Custard apples are known as megafaunal fruit. Species producing large fruits trade off the benefit of having many small seed dispersers such as birds or monkeys, in order to attract large herbivores such as elephants.

Elephants and other megafauna have extensive home ranges, and may visit a tree only occasionally, but when they do, they consume huge quantities of its fruit. Then they carry the seeds across long distances, inside their digestive tract, before depositing them in large piles of dung.

The population size of the trees, thus, is critically dependent on that of its dispersers. Since the late Pleistocene, around 11,000 years ago, megafaunal extinctions have left plant species that rely on them stranded – dependent on much less efficient smaller animals to do the work.

In tropical Thailand, the forest custard apple tree (Platymitra macrocarpa) bears large fruit with classic megafaunal fruit characteristics: dull brown in colour, a long fruiting period, and large numbers falling to the forest floor after ripening. The fruit is eaten by a diverse assemblage of mammals – including squirrels, gibbons, deer, bears and the Asian elephant (Elephas maximus).  These species feed on the fruit in very different ways according to their size and physiology, so Kim McConkey of the National Institute of Advanced Studies in Bangalore, India, and colleagues from BIOTEC, Thailand, decided to assess the relative contribution of each to the seed dispersal of P. macrocarpa.

The researchers were curious whether the seed dispersal role of megafauna such as the elephant could be easily taken on by the smaller animals in the forest, should extinction of the elephant occur.

At the study site, Khai Yai National Park, there is one species mega-herbivore: the Asian elephant, (Elephas maximus) weighing at 3500 kilograms. There are also three large herbivores: sambar deer, (Rusa unicolour, 180 kilograms), the Asiatic black bear (Ursus thibetanu, 109 kilograms), and the sun bear (Helarctos malayanus, 53 kilograms). All consume fruit and thus disperse seeds.

The study also looks at medium-sized frugivores, including white-handed gibbons (Hylobates lar), coming in at just six kilograms.

McConkey and fellow researchers used a combination of techniques to assess the seed dispersal effectiveness of each of these species. Camera-trapping recorded footage of animals foraging in trees and on the ground, and fruits were examined for characteristic feeding signs that identified which animal had handled them.  Transects under the canopy and further away from the trees were searched for seedlings.

The research, published in the journal PLOS One, reveals that elephants are clearly the most effective seed dispersers of P. macrocarpa. Elephants visited the trees on few occasions and consumed a mere 3% of the fruit, yet they were responsible for 37% of the seeds that produced viable seedlings.  The sambar dear foraged on the trees often, consumed 23% of the fruit but were responsible for only 17% of viable results.

Is the effectiveness of the elephant dung pile because it constitutes a warm fertile nursery of sorts for the custard apple seeds? Only partly, it turns out. In an interesting twist which illustrates the complexity of forest ecosystems, the fate of the seedlings is also tied to the behaviour of two species of beetle.

The sambar deer spit out the seeds after ingesting the fruit, and most of them are then eaten by a species of Bruchid beetle, genus unknown.  Seeds deposited in elephant poo are often buried by dung beetles, thus providing protection from the seed-eating Bruchid. The study reveals that such burial is vital for seedling survival.

The two bear species were rare visitors to the fruiting trees. They also produce faecal piles that may provide a measure of protection from the beetles, but the researchers found it difficult to locate them.

Gibbons consume large quantities of fruit and are effective seed dispersers – but the seeds are scattered and not protected by dung, so very few become seedlings.

The low numbers of P. macrocarpa and seedlings across the study site, as well as the high proportion of fruit that goes undispersed, suggests that the custard apple is already suffering from a dearth of megaherbivore skills.

Until recent times, the Javan and Sumatran rhinoceros were also present in the forests. Very little is known about forest rhinoceros and their ecology, but the paper suggests that the species would have eaten the fruit and deposited the seeds in faeces, ready for the industrious dung beetle to come the rescue.

The fate of this particular custard apple tree species is uncertain.

“If less vulnerable large herbivores such as deer are unable to replicate the seed dispersal role of threatened mega-herbivores such as elephants, megafaunal fruit could suffer range contractions, affecting forest community composition and potentially forest carbon stocks,” McConkey says.

Indeed, even with a small population of elephants still persisting in Thailand’s tropical forests, McConkey says the situation for P. macrocarpa is akin to the fate of megafaunal fruit trees in South America, dubbed ‘neotropical anachronisms’, which have long lost their primary seed dispersers – elephant-like creatures known as gomphotheres, extinct horses, and ground sloths.