Megafauna-Dependent Plants

How did megafauna-dependent plants survive after the demise of the giant Pleistocene seed dispersers? Before hand, be warned that coextinctions are very difficult to assess and demonstrate in nature, especially for certain groups (e.g., hosts and ectoparasites). Moreover, think of the myriad possibilities for plants to stay on place even with collapsed dispersal: just haphazard seed dispersal may help; or suboptimal fruit removal and sporadic dispersal by other, less reliable frugivores; or the dispersal being taken over by efficient frugivores (e.g., scatter-hoarders) yet with limitations in some aspect of the dispersal service (e.g., loss of long-distance dispersal events); or dispersal taken over by megafauna surrogates such as livestock; or just by relying on vegetative propagation; or maybe by just being used by humans… All these situations show up eventually when one examines the natural history details of present-day “megafauna-dependent” plants. Thus, at some point it is not surprising that documented coextinctions of plants following the loss of seed dispersers are so rare, if there is any.

Seeds of fruits from megafauna-dependent plants
Seeds of fruits from megafauna-dependent plants (the label, for scale, is ca. 11 cm long). From top left to bottom right: Pouteria ucucui (Sapotaceae), Attalea (Orbygnia) phalerata (Arecaceae), Scheelea martiana (Arecaceae), Theobroma grandiflora (Malvaceae) (two images), Pouteria pariry (Sapotaceae), Licania macrophyla (Chrysobalanaceae), Parinari montana (Chrysobalanaceae), Lacunaria jemmani (Quiinaceae), Pouteria macrocarpa (Sapotaceae), Phytelephas macrocarpa (Arecaceae), Caryocar villosum (Caryocaraceae), Theobroma sp. (Malvaceae), Raphia vinifera (Arecaceae), Lecythidaceae, and Theobroma speciosa (Malvaceae). Pedro Jordano; Museum Goeldi Herbarium, Belém, Pará, Brazil.

However, even if seed dispersal has not fully collapsed, and even if coextinctions have not been extensive, the consequences have been non-trivial for the plant species that lost their megafauna frugivores: increased clumping, increased population isolation, severily-limited gene flow via seed, loss of genetic diversity, markedly reduced effective population sizes (i.e., the number of adults effectively contributing progeny), and demographic bottlenecks. Much research is still needed to fully understand which are these “cryptic” consequences of collapsed seed dispersal mutualisms, yet there are good evidences that the demographic and population genetic consequences are non-trivial.

Collevatti, R., Grattapaglia, D. & Hay, J. (2003) Evidences for multiple maternal lineages of Caryocar brasiliense populations in the Brazilian Cerrado based on the analysis of chloroplast DNA sequences and microsatellite haplotype variation. Molecular Ecology, 12, 105–115.

Malhi, Y., Doughty, C.E., Galetti, M., Smith, F.A., Svenning, J.-C. & Terborgh, J.W. (2016) Megafauna and ecosystem function from the Pleistocene to the Anthropocene. Proceedings of the National Academy of Sciences USA, 113, 838–846.

McConkey, K.R., Brockelman, W.Y., Saralamba, C. & Nathalang, A. (2015) Effectiveness of primate seed dispersers for an “oversized” fruit, Garcinia benthamii. Ecology, 96, 2737–2747.

Hall, J.A. & Walter, G.H. (2014) Relative seed and fruit toxicity of the Australian cycads Macrozamia miquelii and Cycas ophiolitica: further evidence for a megafaunal seed dispersal syndrome in cycads, and its possible antiquity. Journal of Chemical Ecology, 40, 860–868.

Hall, J.A. & Walter, G.H. (2013) Seed dispersal of the Australian cycad Macrozamia miquelii (Zamiaceae): Are cycads megafauna-dispersed “grove forming” plants? American Journal of Botany, 100, 1127–1136.

Janzen, D.H. (1981) Enterolobium cyclocarpum seed passage rate and survival in horses, Costa Rican Pleistocene seed dispersal agents. Ecology, 62, 593–601.

Text and photos: Pedro Jordano. Seedlings and dung photos: Alicia Solana. Seed photos from Museum Goeldi Herbarium, Belém, Pará, Brazil.

Seed Dispersal Anachronisms

The pequi, Caryocar brasilense, is an example of a seed dispersal anachronism. The fruits (pequi, "skin with spines" in tupi-guarani), up to 10-12 cm in diameter, have internal spines in the pulp, surrounding the seeds. Each fruit has a single or very few large seeds resulting a large fruit with a hard pericarp. Field studies of fruit removal rates have reported extremely low actual dispersal of seeds away from maternal trees, the fruits simply rotting on the ground beneath the tree canopy. Virtually no diaspores are found buried by hoarding rodents, or preyed upon by these animals. Pequi is common in central Brazilian cerrado vegetation from southern Pará to Paraná and northern Paraguay. Photos by Mauricio Mercadante CC
The pequi, Caryocar brasilense, is an example of a seed dispersal anachronism. The fruits (pequi, “skin with spines” in tupi-guarani), up to 10-12 cm in diameter, have internal spines in the pulp, surrounding the seeds. Each fruit has a single or very few large seeds resulting a large fruit with a hard pericarp. Field studies of fruit removal rates have reported extremely low actual dispersal of seeds away from maternal trees, the fruits simply rotting on the ground beneath the tree canopy. Virtually no diaspores are found buried by hoarding rodents, or preyed upon by these animals. Pequi is common in central Brazilian cerrado vegetation from southern Pará to Paraná and northern Paraguay. Photos by Mauricio Mercadante CC

In 1982, Daniel H. Janzen and Paul S. Martin advanced the hypothesis that a number of plant species we see in present-day forests shows fruits and seed dispersal adaptations not consistent with their interactions with extant frugivores. Thus, only when we consider the extensive frugviory shown by the extinct Pleistocene megafauna (horses, toxodons, gomphoteres, mastodons, macrauchenias, etc.) we can understand how these species evolved the fruit traits we see nowadays. How then, did these tree and shrub species persist in the absence of the animal mutualists they required for population persistence? The core of the hypothesis expects these anachronic dispersal systems to be best explained by interactions with extinct animals, showing impaired dispersal resulting in altered seed dispersal dynamics.
Janzen and Martin defined seed dispersal anachronisms as those dispersal syndromes with fruit traits and phenological patterns best explained by interactions with extinct animals and offered some striking examples of Neotropical fruits with anachronic traits. These ‘‘unfit’’ species share fruit traits and phenological patterns that are at least in part not expected from their interactions with the extant frugivore community, but logically explained if we consider the extinction or local absence of the main frugivores.
Key traits of megafaunal fruits include 1) overbuilt design, with large seeds protected mechanically by thick and hard endocarp and indehiscence, with nutrient-rich pulp and external similarity to fruits eaten by extant large African/Asian mammals; 2) phenological segregation of ripening times throughout the year; 3) fruits falling to the ground upon ripening; 4) fruits unattractive or not very attractive to arboreal or flying frugivores; 5) a large proportion of the fruit crop rots on the tree without being consumed; 6) frugivores include a large coterie of seed predators that might act sporadically as legitimate dispersers; 7) fallen fruits are avidly eaten by introduced horses, pigs, and cattle; and 8) natural habitats of the plant species today are alluvial bottoms on gentle slopes, usually along forest edges with grassland.
It is clear that functional dispersal for many of these species operates in present-day neotropical communities by means of diplochorous and alternative seed dispersal systems involving other agents such as scatter-hoarding rodents, tapirs, cattle, some primates and even bats, as well as haphazard (runoff) and human-mediated dispersal. However, the loss of seed dispersal by extremely large mammals may imply marked shifts in the patterns and consequences of seed dispersal for these plant species. Ongoing and future research should unveil the signals of the “ghosts of past mutualisms”.

Guimarães Jr., P.R., Galetti, M. & Jordano, P. (2008) Seed dispersal anachronisms: rethinking the fruits extinct megafauna ate. PLoS ONE, 3, e1745.
Janzen, D. & Martin, P.S. (1982) Neotropical anachronisms: the fruits the gomphotheres ate. Science, 215, 19–27.
Martin, P.S. & Klein, R.G. (1984) Quaternary Extinctions: a Prehistoric Revolution. University of Arizona Press, Tucson, AZ.

How To Make A Megafauna Fruit

Just make it big, very big. Well, it’s not just that…- yet we’ll probably agree that megafauna fruits are, in some sense, overbuilt.
If we take the two major types of fruits that extant megafauna consume (e.g., elephants, rhino, etc.), we find two distinct typoplogies. Both are extremely large-sized fruits forms. The first one is like a drupaceous mega-cherry, a large fruit with a single, or very few (i.e., up to three or four) large individual seeds; the second type is kind of a mega-tomato, a large fruit with many, really many (up to hundreds), tiny seeds. Fruits of the first type are usually 4-10 cm diameter; those of the second type are usually > 10 cm in diameter.

megafauna_functional-001
The two main typologies of (fleshy) fruits eaten by extant megafauna. We should add also the role megafauna had in dispersing seeds of herbs and grasses, as well as epizoochoric seeds like those of devil’s claw (genera Proboscidea, Martynia, and Ibicella, Martyniaceae). Illustration: Pedro Jordano. Photo: Kulpat Saralamba CC 3.0.

Why do these fruit types differ when compared to other ‘normal’ fuits? It is not simply that they are much larger. Their key characteristic is that, for a given number of seeds per fruit, they pack up seed sizes up to three orders of magnitude larger than ‘normal’ fruits. Thus, megafaunal fruits allowed plants to circumvent the trade-off between seed size and dispersal by relying on frugivores able to disperse enormous seed loads over long-distances.

Some fleshy fruited, megafaunal-dependent species illustrating size, shape, and color variation. a, Attalea speciosa, Arecaceae; b, Mouriri elliptica, Melastomataceae; c, Hymenaea stigonocarpa, Fabaceae; d, Genipa americana, Rubiaceae; e, Salacia elliptica, Celastraceae; f, Annona dioica, Annonaceae. Black reference line is 2 cm length. Photos: Pedro Jordano, Mauro Galetti and Camila Donatti (fruits).
Some fleshy fruited, megafaunal-dependent species from Brazil (Pantanal) illustrating size, shape, and color variation. a, Attalea speciosa, Arecaceae; b, Mouriri elliptica, Melastomataceae; c, Hymenaea stigonocarpa, Fabaceae; d, Genipa americana, Rubiaceae; e, Salacia elliptica, Celastraceae; f, Annona dioica, Annonaceae. Black reference line is 2 cm length. Photos: Pedro Jordano, Mauro Galetti and Camila Donatti.

In addition to these two types of megafaunal (fleshy) fruits, the extinct Pleistocene megafauna most likely also dispersed grass seeds and seeds attached to their fur (epizoochoric).

Barlow, C. (2001) Anachronistic fruits and the ghosts who haunt them. Arnoldia, 61, 14–21.
Bretting, P.K. 1986. Changes in fruit shape in Proboscidea parviflora ssp. parviflora (Martyniaceae) with domestication. Economic Botany, 40, 170-176.
Feer, F. (1995) Morphology of fruits dispersed by African forest elephants. 
African Journal of Ecology, 33, 279–284.
Guimarães Jr., P.R., Galetti, M. & Jordano, P. (2008) Seed dispersal anachronisms: rethinking the fruits extinct megafauna ate. PLoS ONE, 3, e1745.
Janzen, D. & Martin, P.S. (1982) Neotropical anachronisms: the fruits the gomphotheres ate. Science, 215, 19–27.
Janzen, D. (1984) Dispersal of small seeds by big herbivores: foliage is the fruit. American Naturalist, 123, 338–353.