Ginkgo

Ginkgoes and dodos are my two favorite icons of “ghost” mutualistic interactions. So, I had the two last posts on megafauna and extinct interactions dedicated to them.

There are only five living groups of seed plants, and ginkgo is one of them; just a single species. Ginkgoes (Ginkgo biloba, Ginkgoaceae) have fleshy “fruits” and their “seeds” were dispersed by animals including, most probably, from dinosaurs to Pleistocene megafauna, and to extant frugivores nowadays. The reason is that the ginkgo has survived on Earth for a really extended period of time, with the earliest fossils of ginkgo-like plants dated more than 200 million years ago. Among the many ginkgo-like tree species, only Ginkgo biloba has survived (up to five Ginkgo species are known as fossils).

gbiloba

Living ginkgo very nearly went extinct, in fact, as of two million years ago, existing in only a small area in eastern China, the Tian Mu Shan mountains in Guizhou Province. Ginkgoes have then survived just by human intervention, with an assisted dissemination for cultivation starting at least 1200 yr ago by Buddhist monks, and introduced to Europe just by 1730-1750.

captura-de-pantalla-2016-12-30-a-las-5-51-41-pm
From Engelbert Kaempfer in his Amoenitates, 1712: the first illustration of ginkgo by a Western botanist.

Most likely a combination of extreme dispersal limitation due to lack of efficient seed dispersers combined with large-scale climate shifts and habitat modification contributed to their nearly extinction in the wild. Contrary to other tree species, retractions to small refugia populations failed to recover the original range, especially in North America and Europe. As with other megafauna-dependent species, it resprouts vigorously from buds buried in its underground parts, and human use certainly rescued the ginkgoes, probably because of their nutritous “nut”. In Peter Crane’s words: “It is irrepressible; its capacity for self-preservation has helped it survive through millions of generations.”

We know very little about how seed dispersal works in living ginkgo. The fleshy “fruit” is really the mature, fertilized ovule with a a three-layered integument: a fleshy outer sarcotesta, a stony inner sclerotesta, and a thin endotesta. Its smelly, large seeds (20-30 mm x 16-24 mm) are one of its most well-known and distinctive features: the seed’s soft outer layer starts to break down after a few days on the ground and produces butyric acid, CH3(CH2)2COOH giving it the “interesting” odor. Germination improves after the fleshy seed coat has been removed by passing through the gut of an animal or being teared-off. In one of the potentially wild ginkgo populations in China it is documented that the seeds are eaten by a wild cat, and in Japan they are eaten by badgers. Yet, there were very few seedlings in this population, located in 1989 by Del Tredici, despite good fruiting. People harvested the nuts, which are very nutritious, as well as Pallas’s squirrels (Callosciurus erythraeus), which also may act as good dispersers by scatter-hoarding the seeds.

Yet who were the seed dispersers that mediated the range expansion of ginkgoes over continents and islands (Japan) before human-mediated propagation? As in other megafauna-dependent plants, most likely a combination of dispersal agents, including large and medium-sized mammals and, well before that, dinosaurs. As with other extant large-‘seeded’ Coniferopsida like Cephalotaxus and Torreya with very large seeds, scatter-hoarding animals like the extinct multituberculates (i.e., the ‘rodents’ of the Mesozoic; g. Ptilodus) would have played a role in active seed dispersal of ginkgoes by scatter-hoarding the seeds.

We can see ginkgoes as survivors with a long history of mutualistic interactions involving a diverse array of animals, whose actual diversity we can only speculate about, then replaced by extensive human use.

  • van Beek, T.A. (2003) Ginkgo biloba. CRC Press, NY.
  • Crane, P. (2013). Ginkgo. The tree that time forgot. Yale University Press, New Haven.
  • del Tredici, P. (1989) Ginkgos and multituberculates: evolutionary interactions in the Tertiary. Bio Systems, 22, 327–339.

Text: Pedro Jordano with excerpts from Del Tredici (1989) and Crane (2013). Illustrations: WikiMedia.

Megafauna in Madagascar

pleistocene_madagascar_final_by_wsnyder-d7f6uwm

A scene in Madagascar in the late Pleistocene. From left to right: elephant bird (Aepyornis maximus), Malagasy giant rat (Hypogeomys antimena), melanistic giant fossa (Cryptoprocta spelea), monkey lemur (Archaeolemur), streaked tenrec (Hemicentetes), and koala lemur (Megaladapis).

Madagascar had a highly diversified megafauna, as also occurred in other islands, quickly becoming defaunated because of human action and habitat destruction, starting very recently, ca. 2000 yr BP. For example, the Spiny Thicket Ecoregion (STE) of SW Madagascar was home to numerous giant lemurs and other megafauna, including pygmy hippopotamuses, giant tortoises, elephant birds, and large euplerid carnivores.

Island frugivore faunas are much more phylogenetically diverse than continental ones; their frugivore assemblages are known as disharmonic because a given plant species may depend on distinct sorts of animal seed dispersers (e.g., lizards, birds, mammals) quite distinct in evolutionary history and likely not being complementary in their ecological functions. For example, only one-third of the lemur species which earlier occupied the spiny thicket ecoregion survive today. The extinct lemurs occupied a wide range of niches, often distinct from those filled by non-primates. Many of the now-extinct lemurs regularly exploited habitats that were drier than the gallery forests in which the remaining lemurs of this ecoregion are most often protected and studied. Recent evidence using stable isotope biogeochemistry has shown that most extinct lemurs fed predominantly on C3 plants and some were likely the main dispersers of the large seeds of native C3 trees; others included CAM and/or C4 plants in their diets.
While the negative effects on seed dispersal of Pleistocene megafauna extinction in continental areas were probably buffered by complementary dispersers (e.g., scatter-hoarders, domestic megafauna, human use), island assemblages had not this option. Thus, if we seek instances of actual co-extinction of co-dependent frugivores and their food plants we may probably have to resort to islands, especially oceanic islands, or extreme habitats (e.g., deserts) where the mutualistic partners are highly disharmonic.

  • Crowley, B.E., Godfrey, L.R. & Irwin, M.T. (2011) A glance to the past: subfossils, stable isotopes, seed dispersal, and lemur species loss in Southern Madagascar. American Journal of Primatology, 73, 25–37.
  • Grubb, P.J. (2003) Interpreting some outstanding features of the flora and vegetation of Madagascar. Perspectives in Plant Ecology Evolution and Systematics, 6, 125–146.
  • Jungers, W.L., Demes, B. & Godfrey, L.R. (2007) How big were the “‘giant’” extinct lemurs of madagascar? J. G. Fleagle, C. C. Gilbert (eds.), Elwyn Simons: A Search for Origins. Springer, pp: 1–18.
  • Shapcott, A., Rakotoarinivo, M., Smith, R.J., Lysakova, G., Fay, M.F. & Dransfield, J. (2007) Can we bring Madagascar’s critically endangered palms back from the brink? Genetics, ecology and conservation of the critically endangered palm Beccariophoenix madagascariensis. Botanical Journal of the Linnean Society, 154, 589–608.

Text: Pedro Jordano; excerpts fromCrowley et al. 2011.
Illustration: William Snyder @deviantart.com (Pleistocene Madagascar).

It takes guts to disperse seeds: the amazing physiologies of megafauna

Megafauna can be divided in two large groups in terms of food digestion: foregut and hindgut fermenters, depending on where in the digestive tract the ingesta is digested. Foregut fermenters include ruminants, pseudoruminants (i.e., hippo, camelids), just the hoatzin among birds, and the colobine monkeys, sloths, and some marsupials and rodents- all them have complex, multipart stomachs. Hindgut fermenters are monogastric herbivores.

The very large megafauna are largely non-ruminants and may have either foregut or hindgut fermentation of food, with this having very important consequences for seed treatment. While the largest extant non-ruminant foregut fermenter is the hippopothamus, the largest terrestrial animals nowadays are hindgut fermenters, with the exception of large bovids: elephants, rhinos, equids, tapirs.

Interestingly, the digestive tract of elephants is surprisingly short compared to other herbivorous mammals. Typical retention times of ingesta in elephants are below 50h; with Asian elephants achieving higher digestion coefficients on comparable diets, and having longer ingesta mean retention times, than their African counterparts. This is probably associated to the fact that intestine lengths of Asian elephants (~30m) nearly double those of African elephants (~15m) for a given body mass.

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The diversity of digestive systems among several types of mammal hindgut fermenters. a, peccary; b, pig; c, zebra; d, tapir; e, African elephant; f, Asian elephant; g, rhino.

Tapirs, in the order Perissodactyla, are the closest extant relatives to equids and rhinoceroses, thus their digestive tract reportedly resembles that of horses. They both have a large caecum and proximal colon as fermentation chambers. In both the horse and the rhinoceros, the caecum and colon have approximately the same width. In contrast, the tapir also has a large caecum, but the rest of the large intestine—in particular, the ventral proximal colon— is less voluminous. The caecum of the tapir is its most voluminous gastro-intestinal section, suggesting that during the evolutionary history of tapirs, and in contrast to other extant perissodactyls, the caecum was the major fermentation site in the digestive tract.


The caecum of rhinos, horses, and probably also tapirs may retain seeds for many days (kind of a side-storage of indigestible food), being suddenly evacuated in pulses. The browsing black rhinoceros (Diceros bicornis) has both shorter small and large intestines than the grazing rhinoceroses (Ceratotherium simum, Rhinoceros unicornis).

Peccaries in contrast, are foregut fermenters, with a digestive tract characterised by an elaborate forestomach. Peccaries have a small relative stomach volume compared to other foregut fermenters, which implies a comparatively lower fermentative capacity and thus forage digestibility. The forestomach could enable peccaries to deal, in conjunction with their large parotis glands, with certain plant toxins (e.g. oxalic acid).

This fascinating diversity of digestive strategies and food processing has undoubtely emerged from coevolved interactions with plants, either as antagonistic herbivores or mutualistic seed dispersers. Plants were benefited by megafauna evolving very large body sizes (especially among monogastric hindgut fermenters), yet with relatively short retention times that did not damage seeds, even with a lengthy digestion process; however, with more limitations to detoxify plant toxins compared to ruminants. Many of the extremely large extinct megafauna (e.g., Indricotherium, reaching up to 15000 kg body mass) were most likely hindgut fermenters with browsing habits and extensive use of fruit food. Ruminants, on the other hand, have been likely limited in their evolution to smaller body sizes (up to 1200 kg in some bovids, 2700 kg in hippos). All the very large ruminants (bovids, buffalo, zebu), but not the smaller ones (e.g., antelopes) lack the ability to reabsorb water in the colon and depend on the availability of drinking water.

The combinations of digestive characteristics of monogastric hindgut fermenters supports their key ecologial functions for seed dispersal: 1) ample diversity of plant food species dispersed; 2) extremely large number of seeds dispersed due to huge gut capacities; 3) long seed dispersal distances due to long retention times with a distinct role of caeca; and 4) gentle treatment to seeds during mastication and digestion, favouring adequate germination potential of dispersed seeds in most instances.

Photos: Kulpat Saralamba, Kim McKonkey, Mauro Galetti, Carlos R Brocardo, WikiCommons.

  • Clauss, M. & Hummel, J. (2005) The digestive performance of mammalian herbivores: why big may not be that much better. Mammal Review, 35, 174–187.
  • Clauss, M., Steinmetz, H., Eulenberger, U., Ossent, P., Zingg, R., Hummel, J. & Hatt, J.M. (2006) Observations on the length of the intestinal tract of African Loxodonta africana (Blumenbach 1797) and Asian elephants Elephas maximus (Linné 1735). European Journal of Wildlife Research, 53, 68–72.
  • Clauss M, Steuer P, Müller DWH, Codron D, Hummel J (2013) Herbivory and body size: allometries of diet quality and gastrointestinal physiology, and implications for herbivore ecology and dinosaur gigantism. PLoS One 8:e68714
  • Hagen, K., Müller, D.W.H., Wibbelt, G., Ochs, A., Hatt, J.-M. & Clauss, M. (2014) The macroscopic intestinal anatomy of a lowland tapir (Tapirus terrestris). European Journal of Wildlife Research, 61, 171–176.
  • Müller, D.W.H., Codron, D., Meloro, C., Munn, A., Schwarm, A., HUMMEL, J. & Clauss, M. (2013) Assessing the Jarman–Bell Principle: Scaling of intake, digestibility, retention time and gut fill with body mass in mammalian herbivores. Comparative Biochemistry and Physiology, Part A, 164, 129–140.
  • Schwarm, A., Ortmann, S., Rietschel, W., Kühne, R., Wibbelt, G. & Clauss, M. (2009) Function, size and form of the gastrointestinal tract of the collared Pecari tajacu (Linnaeus 1758) and white-lipped peccary Tayassu pecari (Link 1795). European Journal of Wildlife Research, 56, 569–576.

The Gardeners of the Forest

Elephants are the major gardeners of the rainforest. Weighing around 4000 kg, they are more than twice as large as the next biggest sympatric animal species (the one-horned rhinoceros) and four times as large as the third-place finisher (the gaur, Bos gaurus). Current taxonomy recognizes two extant species of elephant, the African elephant (Loxodonta africana), with forest and savannah subspecies, and the Asian elephant (Elephas maximus). They disperse massive amounts of seeds in conditions adequate for germination and establishment of tree seedlings, with estimates ranging between 300-2000 seeds/km2/day depending on elephant species and habitat. Recent studies indicate that seeds taken from elephant dung germinated as well or better than seeds from bovid dung or directly from fruit. Elephants were calculated to move seeds up to 10 times as far as domestic bovids. When elephants are missing, there are no ecological counterparts to compensate their absence.


The video from the Elephant Reintroduction Foundation nicely cartoons the type of mechanistic models that help us to estimate the ecological functions derived from mutualistic interactions between these megafrugivores and plants.
An empirical probability model estimated that the loss of elephants would result in reductions of about 66%, 42%, and 26% in the number of successfully dispersed seeds of key species such as Dillenia indica (chalta), Careya arborea (kumbhi), and Artocarpus chaplasha (lator), without compensation. In compensation scenarios, other frugivores could ameliorate reductions in dispersal, making them as low as 6% if species such as gaur (Bos gaurus) persist. Thus the importance of elephants as seed dispersers is amplified by the population reductions of other large disperser species throughout tropical Asia. The African and Asian elephants are the exclusive or near-exclusive disperser of a considerable number of plant species. The loss of forest elephants (and other large-bodied dispersers) may lead to a wave of recruitment failure among animal-dispersed tree species, and favor regeneration of the species-poor abiotically dispersed guild of trees.

– Beaune, D., Fruth, B., Bollache, L., Hohmann, G. & Bretagnolle, F. (2013). Doom of the elephant-dependent trees in a Congo tropical forest. Forest Ecology and Management, 295, 109–117.
– Blake, S., Deem, S.L., Mossimbo, E., Maisels, F. & Walsh, P. (2009) Forest elephants: tree planters of the Congo. Biotropica, 41, 459–468.
– Campos-Arceiz, A., & Blake, S. (2011). Megagardeners of the forest – the role of elephants in seed dispersal. Acta Oecologica, 37, 542-553.
– Sekar, N., Lee, C.L. & Sukumar, R. (2015). In the elephant’s seed shadow: the prospects of domestic bovids as replacement dispersers of three tropical Asian trees. Ecology, 96, 2093–2105.
– Sukumar, R. (2003). The living elephants: evolutionary ecology, behavior, and conservation. New York: Oxford Univ. Press.

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.

Megafauna fruits and seeds photos updated


I’m in the process of moving photo repositories to iCloud and have my previous photos of megafauna fruits and seeds moved to this gallery. You can access the photos here.

These photos were taken in the herbarium of Museu Goeldi (Belém, Pará, Brazil) in 2002. They include many of the species we discuss in our paper in PLoS One on megafauna fruits.

Megafauna manuscript accepted!

New paper in PLoS One

We now have our manuscript on seed dispersal by extinct megafauna accepted in PLoS One. It should come to the light by the 5th March.
Guimarães Jr, P., Galetti, M. and Jordano, P. 2008. Seed dispersal anachronisms: rethinking the fruits extinct megafauna ate. PLoS ONE.