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.

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.

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Curso “Frugivoria e dispersão de sementes”, 2016


Frugivory and Seed Dispersal Course (Portuguese/Spanish) – 7-11 March 2016

Registrations: 4 Créditos – 01 a 12/02/2016.

@UNESP_PG_EcoBio with @mauro_galetti @pedro_jordano.

Part of the Programa de Pós-Graduação em Ecologia e Biodiversidade. UNESP, Rio Claro.

Fotos: Marina Cortes, Guto Balieiro, Lindolfo Souto, Pedro Jordano.

How do furgivorous birds build-up their fruit meals?

This is the third part of a trilogy of papers dedicated to understanding the evolution of fruit colors and visual signals evolved by plants to attract animal mutualists. The paper is now available online at the Proceedings of the Royal Society, Biology website.

Theory predicts that trade among mutualists requires high reliability. Here, we show that moderate reliability already allows mutualists to optimize their rewards. The colours of Mediterranean fleshy-fruits indicate lipid rewards (but not other nutrients) to avian seed dispersers on regional and local scales. On the regional scale, fruits with high lipid content were significantly darker and less chromatic than congeners with lower lipid content.

Sylvia atricapillaSylvia borin

On the local scale, two warbler species (Sylvia atricapilla and Sylvia borin, above) selected fruit colours that were less chromatic, and thereby maximized their intake of lipids—a critical resource during migration and wintering.


Figure. The trade of resources characterizing mutualistic interactions leads to multiple, repeated interactions among individual producers and consumers. For example, birds use visual information to decide which fruits to consume. Two individual birds combine different fruit species in their meals during a short feeding bout (t0 − t1), along their foraging sequence, in which they visited different fruiting plants. M1–M4 indicate the composition of four meals, i.e. the number of fruits consumed and their species identity, different fruits with different colours. We analyzed the combination of colors in field-sampled fruit meals in relation to the nutrient composition and food “reward” obtained by the birds. Birds used markedly non-random combinations of colors in their meals, indicating a significant choice of fruit meals maximizing energy intake.

In a passage and wintering area in SW Spain where I intensively studied these birds, the two warbler species consistently selected fruit color combinations that were significantly less chromatic, evidencing the use of color as a cue of nutrient rewards during short feeding bouts. Being extremely dependent on fleshy fruits during migration and wintering, these warblers use a very diverse set of fruit species to build-up reserves required for long-distance flights (garden warbler) or winter survival (blackcap).

It is amazing how selective were these birds in their choice of fruits. Even in a short feeding bout blackcaps can ingest up to seven different fruit species. I used analyses of fecal pellets, identifying not only seeds, but also fruit skins in the remains using a microscope, which enabled me to identify the number of different fruit species consumed during a short feeding bout. The fruit meals thus combine a varied assortment of flavors, pulp types, etc. The warblers have a very short gut passage time (16 moon on average- and up to 40 min), so that a sample of faecal material indicates the previous choices of fruits made by the bird, immediately before capture. I used mist-netted birds that were released after capture.

Warblers need to maintain a high throughput of fruits when relying on fruit food because fleshy fruits are a quite “diluted” type of food: not only they are rich in water, quite succulent, but they also have indigestible seeds that occupy very valuable space within the bird’s gut. The birds need to process all this stuff very rapidly in order to get enough “reward”. In turn this is good for the plant because the seeds are readily dispersed away from the mother plant. This is a mutualistic interaction driven by the visual cues used by the birds.

Our results indicate that mutualisms require only that any association between the quality and sensory aspects of signallers is learned through multiple, repeated interactions. Because these conditions are often fulfilled, also in social communication systems, we contend that selection on reliability is less intense than hitherto assumed. This may contribute to explaining the extraordinary diversity of signals, including that of plant reproductive displays.

Our study on functional extinction of frugivores, published in Science

Our new paper “Functional Extinction of Birds Drives Rapid Evolutionary Changes in Seed Size”, just published in this week issue of Science.

Mauro Galetti, Roger Guevara, Marina C. Côrtes, Rodrigo Fadini, Sandro Von Matter, Abraão B. Leite, Fábio Labecca, Thiago Ribeiro, Carolina S. Carvalho, Rosane G. Collevatti, Mathias M. Pires, Paulo R. Guimarães Jr., Pedro H. Brancalion, Milton C. Ribeiro, and Pedro Jordano. 2013. Functional Extinction of Birds Drives Rapid Evolutionary Changes in Seed Size. Science 340: 1086-1090.
DOI: 10.1126/science.1233774.

Palmito collage large

Photos, from top left, descending, to right:

1. Selenidera maculisrotris (male) handling a palmito seed.
2. Palmito fruits with beak marks, dropped beneath the palm, and regurgitated seeds.
3. Turdus flavipes trying to swallow a palmito fruit.
4. Ramphastos vitellinus (subsp. vitellinus) handling a fruit.
5. Selinedera maculirostris (male) picking a fruit.
6. Palmito seedling just after germination (note the seed still attached).
7. Palmito juçara, Euterpe edulis (Arecaceae).
8. Aburria (Pipile) jacutinga.
9. Baillonius (Pteroglossus) bailloni handling a fruit.
10. Turdus amaurochalinus (young), picking a fruit.
11. View of the ompbrphilous atlantic rainfrorest (Mata Atlántica) understory in Carlos Botelho park.
12. Penelope obscura.
13. Pyroderus scutatus, swallowing a fruit.
Photos by: Edson Endrigo, Pedro Jordano, Mauro Galetti, Marina Cortes, Guto Balieiro, and Lindolfo Souto.

The selective extinction of large frugivorous birds is associated with the rapid evolutionary reduction of seed size in a keystone palm.

Local extinctions have cascading effects on ecosystem functions, yet little is known about the potential for the rapid evolutionary change of species in human-modified scenarios. We show that the functional extinction of large-gape seed dispersers in the Brazilian Atlantic forest is associated with the consistent reduction of seed size of a keystone palm species. Among 22 palm populations, areas deprived of large avian frugivores for several decades present smaller seeds than non-defaunated forests, with negative consequences for palm regeneration. Coalescence and phenotypic selection models indicate that seed size reduction most likely occurred within the last 100 years, associated with human-driven fragmentation. The fast-paced defaunation of large vertebrates is most likely causing unprecedented changes in the evolutionary trajectories and community composition of tropical forests.

When we talk about biodiversity we normally refer to the number of species found in a given area. But these species have ecological functions that are essential to the functioning of ecosystems. The loss of a species also entails the loss of the ecological role it plays in the ecosystem, and this kind of extinction happens much unnoticed. We have documented the effect of functional extinction of large fruit-eating birds on an important plant trait – seed size – of a key plant species of the Atlantic Rainforest in Brazil, one of the biodiversity “hot-spots” on the planet. Our study is a natural experiment that takes advantage of the presence of fragmented areas of forest that have remained so since the early 1800s, when the development of crops such as coffee and sugar cane triggered the extensive deforestation of the Atlantic rainforest. Only 12% of the original forest persists, and over 80% of what remains are fragments are too small to maintain large animals. Our results show that the loss of large fruit-eating birds such as toucans leads to the size reduction of the seeds of a palm tree, which is a key species in these Atlantic forests. These evolutionary changes in fruit and seed size have occurred only in defaunated forests, where only small frugivorous birds persist. These small birds only successfully disperse smaller seeds.

PressReleaseImage 002

We studied 22 populations of this palm tree along the SE coast of Brazil. In the defaunated areas, which persist as fragments from several decades ago, the seed sizes are consistently smaller than in well-preserved forests, and this has negative consequences for regeneration. The smaller seed size in defaunated areas is not explained by other environmental or geographic variables. Fast natural selection: Small birds such as thrushes cannot swallow and disperse large seeds. Large birds, such as aracaris and toucans, play an important role in dispersing seeds of plants, especially of large seeds. In rainforests without toucans large seeds tend to disappear over time because undispersed seeds are attacked by seed predators. Small seeds are more vulnerable to desiccation and cannot withstand projected climate change.

We have combined a number of techniques including field work, genetic analyses, evolutionary models and statistical analyses. We collected ground data on a large number of palm trees in 22 populations, by collecting fruits, observing the avian frugivore assemblage and conducting germination experiments. We have also used DNA genetic markers to employ quantitative genetic models to estimate the intensity of selection on seed traits and coalescence theoretical models to infer the time of isolation of populations. Finally, we statistically analyzed the effect of different types of data, including climatic and environmental information, on seed size variation. 

Our work provides one of the few existing evidence that evolutionary change in natural populations can happen very fast as a direct result of changes induced by human action. The extinction of large vertebrates is happening all over the world and the implication is poorly known. These large bodied species maintain mutualistic interactions with plants: while flesh-fruited plants offer fruits as food sources, frugivores disperse their seeds. Such ecological process ensures natural regeneration of the forest. Unfortunately, the effect we document in our work is probably not an isolated case. The constant extirpation of large vertebrate in natural habitats is very likely causing unprecedented changes in evolutionary trajectories of many tropical species.

Habitat loss and species extinction is causing drastic changes in the composition and structure of ecosystems. This involves the loss of key ecosystem functions that can determine evolutionary changes much faster than we anticipated. Our work highlights the importance of identifying these key functions to quickly diagnose functional collapse of ecosystems.

Lizards, endemic island plants and extinctions

Seed dispersal by lizards is an insular phenomenon. In the Canary Islands, many fleshy-fruited plants depend on lizards for their successful dispersal and recruitment. We are now working in a project directed by Alfredo Valido to analyze the movement ecology of Canarian endemic Gallotia lizards and its consequences for plant dispersal and recruitment. We study the reproductive ecology of orijama plants Neochamaelea pulverulenta, an endemic Cneoraceae in the islands, whose seeds are exclusively dispersed by the lizards. We combine studies of fine- and medium-scale genetic structure with data and models of foraging movements of the lizards, monitoring with radio-tracking methods. So far the results are superb, and we now have detailed data on movement patterns of Gallotia galloti in Teno Bajo (Tenerife)- our main study site- and G. stehlini (in the photo) in Barranco de Veneguera (Gran Canaria). We have also seeds samples from two 1.2 ha plots in the two sites as well as leaf samples from >2000 plants to assess seed dispersal patterns with genetic methods, similar to those that we’ve been using with Prunus mahaleb and Frangula alnus. We are interested in assessing the potential effects of previous extinctions of other giant lizard species (e.g., G. goliath) that were very good dispersers of orijama. These were up to 1.3 m long and able to disperse even the largest fruits and seeds of orijama, which now remain undispersed on the plants; only the smaller fruits and seeds remain dispersed by the extant smaller lizards.