Madagascar's orphans of extinction
Researchers in Comparative Seed Biology, Wolfgang Stuppy and Aurélie Albert-Daviaud, explain how some Madagascan plants are living on 'borrowed time' following the extinction of their seed dispersers.
The island of Madagascar is one of the world's top biodiversity hotspots. Its landmass separated from continental Africa 160 million years ago, and from India 88 million years ago, well before the demise of the dinosaurs. Due to its long geographical isolation it has become home to a unique fauna and flora. Over 80% of the island's plants and animals are endemic, which means they are found nowhere else on Earth.
The riddle of the rotting fruit
Madagascar is, in many ways, a unique place. One peculiar aspect of its biodiversity is that, compared to other tropical areas, it has relatively few fruit-eating (and therefore seed-dispersing) animals. Among all animals worldwide, birds are by far the most important dispersers of seeds. However, Madagascar is poor in frugivorous (fruit-eating) birds. In fact, there are only five bird species on the island which can be considered bona fide dispersers rather than granivores (seed-eaters). This dispersal-ecological gap is filled by lemurs, Madagascar's unique primates. Of the c.100 extant lemur species, 21 are frugivores and therefore ‘good’ seed dispersers.
Many of Madagascar's endemic plant species produce fleshy fruits which are obviously animal-dispersed but their seeds are too large to fit the gape of any living animal. As a result, these fruits find no 'takers' and simply drop to the ground in large numbers where they rot.
Madagascar’s lost megafauna
The only logical explanation for the apparently paradoxical existence of fleshy fruits with no dispersers is that they are adapted to larger animals that no longer exist.
Indeed, over the last 2,000 years, the island of Madagascar has lost 48 unique species of large-bodied animals. Among them were aardvark-like insectivores (Plesiorycteropus madagascariensis), giant lemurs, pygmy hippopotamuses, giant tortoises and, probably the most famous of all, around eight species of gigantic ratites (Aepyornithidae), the so-called elephant birds (Aepyornis spp., Mullerornis spp.).
The last historical sighting of an elephant bird was in the 17th century. Since their extinction, the role of the largest seed dispersers has passed from the elephant birds (450kg) to the radiated tortoise (10kg) (Hansen & Galetti, 2009).
The most important seed dispersers among Madagascar’s extinct animals were undoubtedly the giant lemurs; there were 17 species, all significantly larger than any extant lemur species. It is likely that more than half of these giant lemurs had a diet of fruits or a mixed diet of fruits and leaves. Therefore, they are extremely likely to have acted as seed dispersers.
As a result of the disappearance of these large-bodied animals, large-seeded plants that relied on them have now lost their dispersers. The fruits have become ‘anachronistic’, a concept first suggested by Janzen & Martin (1982). The plants themselves have become 'orphans' of extinction and this means that they will most likely face the same fate as their animal partners.
Why is seed dispersal so important?
Seed dispersal is a key process in plant communities that allows seeds to escape direct competition with both their parent plants and their siblings. Seed dispersal reduces density-dependent mortality of seeds and seedlings, and it allows population growth as well as gene flow between populations.
Non-dispersal or impaired dispersal leads to reduced geographic ranges and restricted gene flow between populations. The result is diminished genetic diversity within populations which ultimately reduces individual fitness. Although it is a slow process, it has been demonstrated that the loss of animal seed dispersers considerably increases the risk of extinction for plants with animal-dispersed fruits or seeds.
Finding Madagascar’s orphans of extinction
Several Malagasy plants with fleshy fruits and excessively large seeds have long been suspected to be anachronistic. Their seeds are simply too large to be swallowed by any extant disperser.
Among these plants are the famous baobabs (Adansonia spp., Malvaceae), several palm species (Borassus madagascariensis, Hyphaene coriacea, Orania longisquama and Satranala decussilvae) and two species of the genus Dilobeia (Proteaceae) (Baum, 1995; Dransfield & Beentje, 1995; Godfrey et al., 2008). However, these are just the most obvious cases; there are many more waiting to be identified.
Because Madagascar’s orphans of extinction potentially share the same fate as their lost animal partners, we have started a research project which aims to identify, study and conserve species whose fruits have become anachronistic.
Size does matter
The simplest way to initially identify suspected dispersal anachronisms is via the size of the seeds. If the seeds of an obviously animal-dispersed fruit are too large to be swallowed by any extant disperser, they are very likely to be anachronistic.
In a recently published paper (Federman, et al. 2016) the authors calculated the absolute maximum seed sizes that extinct and extant lemurs could/can swallow based on the relationship between body mass and maximum ingestible food size. They found that among extant lemurs, the black-and-white ruffed lemur (Varecia variegata) and the red ruffed lemur (Varecia rubra) are the two species that can swallow the largest seeds, limited to a diameter of up to 26 mm. However, among the extinct giant lemurs, the largest disperser, Palaeopropithecus ingens (a sloth lemur), could probably swallow seeds of up to 70 mm in diameter (e.g. Borassus madagascariensis) – nearly three times larger.
The logical conclusion is that any plant species in Madagascar that has animal dispersed fruits with seeds larger than 26 mm in diameter is now anachronistic.
What this means for conservation
Extreme dispersal anachronisms, i.e. cases where no extant animal species is capable of swallowing (and therefore dispersing) the seeds, are the most compelling cases. However, anachronism is not simply a binary concept. Lesser dispersal inefficiencies also qualify as anachronisms. For example, the black-and-white ruffed lemur and the red ruffed lemur are the only extant species able to facilitate the dispersal of many large-seeded species which were undoubtedly also part of the diet of the extinct giant lemurs. However, both species are currently critically endangered and are irreplaceable in their seed dispersal function. If they also perish, yet more of Madagascar’s unique plant species will face an uncertain future.
Identifying and studying Madagascar’s orphans of extinction is an important and urgent task. Species that have lost most if not all their animal dispersers are on borrowed time. The results of our research will hopefully inform and improve conservation strategies and policies, which should lead to a more secure future of Madagascar’s diverse forests.
Acknowledgements
We would like to thank our Kew colleagues Gwilym Lewis, Bill Baker, Stuart Cable and Wolf Eiserhardt for their collaboration, and our Kew MSc student Sarah Perillo for her work on anachronisms in Madagascan palms. We also thank the team of the Kew Madagascar Conservation Centre (KMCC) for their invaluable collaboration, in particular Hélène Ralimanana, Franck Rakotonasolo, Guy Onjalalaina, Romer Rabarijaona and Tatamo Andrianantenaina. Without their input, ranging from obtaining permits to organising field work and their excellent plant identification skills, this project would not be possible.
This project is part-funded by the Joseph Jones and Daisy and Graham Rattenbury Charitable Trust.
References
Baum, D. (1995). A systematic revision of Adansonia (Bombacaceae). Annals of the Missouri Botanical Garden 82: 440-470.
Dransfield, J. & Beentje, H. (1995). The Palms of Madagascar. Kew: Royal Botanic Gardens, Kew and International Palm Society.
Federman, S., Dornburg, A., Daly, D.C., Downie, A., Perry, G.H., Yoder, A.D., Sargis, E.J., Richard, A.F., Donoghue, M.J. & Baden, A.L. (2016). Implications of lemuriform extinctions for the Malagasy flora. Proceedings of the National Academy of Sciences Early Edition. Available online.
Godfrey, L.R., Jungers, W.L., Schwartz, G.T., & Irwin, M.T. (2008). Ghosts and orphans. In: Elwyn Simons: a search for origins, ed. J.G. Fleagle &C.C. Gilbert, pp 361-395. Springer, United States. Available online.
Hansen, D.M. & Galetti, M. (2009). The forgotten megafauna. Science 324: 42-43. Available online.
Janzen, D.H. & Martin, P.S. (1982). Neotropical anachronisms: the fruits the gomphotheres ate. Science 215: 19-27. Available online
