"The Botanical Ghosts of Evolution"
by Connie Barlow

a contribution in Forest Canopies
edited by Bruce Rinker and Meg Lowman, 2004


Many plants, especially those in or beneath a dense and therefore wind-restricted canopy, depend on mobile animals not only for transferring pollen but also for dispersing seeds. We are achingly familiar with the consequences for plants when bird, bat, or insect pollinators dwindle or become extinct. But what about the loss of seed dispersal partners?

Vanishing pollinators is an anthropogenic phenomenon that is happening on our watch (see Buchmann and Nabhan 1995). So, too, with vanishing dispersal partners, but with this distinction: The loss of seed carriers began long before humans learned to till the soil (Barlow 2000). Modern humans are culpable, of course, but so were our distant ancestors — and in a very big way.

Insects and small vertebrates can evolve into superb carriers of pollen, but it takes a much larger creature to swallow and defecate very large seeds in a viable condition. Elephants, rhinos, and other "megafauna" are thus the primary agents of seed dispersal for many plants that produce large fleshy fruits or nutritious, indehiscent pods. Dispersal troubles began for many plants when large mammals were sent into extinction by spear-toting humans entering landscapes in which the inhabitants had not co-evolved with projectiles.

This happened in Australia some 60,000 years ago when the first humans arrived, and in North and South America just 13,000 years ago when the Clovis culture of mammoth hunters crossed the Bering land bridge (Martin 1990). Thanks to the longevity of many trees, a capacity to reproduce clonally from roots, and the fact that the human invaders fancied fruit, there are plants alive today whose fruits are markedly anachronistic.

Consider the avocado, Persea americana, native to South America. Wild stock of avocado (now rare) from which our plumped-up varieties were bred had only a thin layer of oily flesh to attract dispersers, but the seed was about the same size. Except for the rare jaguar, no animal native to South America today will swallow and defecate the seed of avocado. But there was no shortage of dispersers 15,000 years ago, when the Americas were home to elephantine gomphotheres, rhinolike toxodons, and lumbering ground sloths.

Tropical and semi-tropical species of family Annonaceae (cherimoya, soursop, pawpaw) that are native to the Western Hemisphere are also anachronistic. Omnivores (notably, bears) are capable dispersers, but these plants have lost their herbivore partners, especially the "hindgut fermenters" whose microbial symbionts are located far enough down the line that fruit sugars do not interfere with acid-intolerant microbes.

Avocado, annona fruits, and some large-podded legumes (such as Kentucky coffee tree, Gymnocladus, in North America) are all suited for shady environments of the forest understory. Their large seeds contain energy stores sufficient for young plants to establish beneath a mature canopy. But those that would swallow such seeds, enticed by the surrounding pulp, are now gone.

Some small trees of forest-edge and savanna environments, such as honey locust (Gleditsia sp.) of both Americas and osage orange (Maclura pomifera) of North America, also bear anachronistic fruit-and widely spaced anachronistic thorns. The centimeter-long seeds within the sweet pods of honey locust are so well adapted to withstand the grinding teeth of their extinct dispersal partners that they now must be scarred by knife or acid in order to sprout.

Five hundred years ago, when Spanish invaders returned the horse to its continent of origin, they unknowingly restored a key dispersal partner for osage orange, a close relative of Asian breadfruit. A deep time understanding of the range of osage orange in the late Cenozoic suggests that it truly is native to much of North America even though early botanists noted that its "natural" range entailed only a bit of eastern Texas and Arkansas. Apparently, once-prolific osage orange was heading toward extinction for lack of dispersers. The return of the horse, along with the tree's appeal as an ornamental, reversed this downward evolutionary trend (Barlow 2001).

An awareness of lost dispersal partners is vital, therefore, not only for determining the extent of native range but also for managing plant diversity with a look toward intact forest canopy.

References

Barlow, C. (2000). "The Ghosts of Evolution: Nonsensical Fruit, Missing Partners, and Other Ecological Anachronisms." Basic Books, New York.

Barlow, C. (2001). Anachronistic fruits and the ghosts who haunt them. Arnoldia 61(2), 14-21.

Buchmann, S.L. and Nabhan, G.P. (1995). "The Forgotten Pollinators." Island Press, Washington, DC.

Martin, P.S. (1990). 40,000 years of extinctions on the 'Planet of Doom.' Palaeogeography, Palaeoclimatology, Palaeoecology 82, 182-201.

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