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.

The Cryptic Extinctions

McConkey, K.R. & O’Farrill, G. (2016) Loss of seed dispersal before the loss of seed dispersers. Biological Conservation, 201, 38–49.

Cryptic function loss is a loss in the function of a species that is hidden by its continued presence in the ecosystem; the species may still be present and showing up in a biodiversity inventory, yet its functional ecological role has disappeared. 
The authors reviewed the evidence for cryptic function loss to be widespread among seed disperser populations that persist under disturbed conditions. The results overwhelming support for the seed dispersal effectiveness of animals to be negatively impacted by all forms of disturbance (population decline, changes in community assemblages, habitat change, and climate change). However, seed dispersal was positively affected in some examples, particularly when extirpation of an interacting frugivore or predator enhanced fruit consumption. 

A group of gaurs (Bos gaurus) (also known as Indian bison); a species listed as vulnerable on the IUCN Red List since 1986. The population decline in parts of the species’ range is likely to be well over 70% during the last three generations. Photo: Kulpat Saralamba.

Behavioral changes are usually the first adaptation of an animal to disturbance and are likely to be a common trigger for function loss without species loss, resulting in the animal no longer performing a function carried out previously. Substantial decrease in population density or demography of an animal species can also trigger cryptic function loss; for example, when specialization occurs among individuals within a single population and a non-random subset of individuals is particularly vulnerable to a disturbance. Finally, cryptic function loss can occur through phenotypic adaptation of an animal species, when the physical alteration enhances survival but is not matched by interacting species.
Given the ample generalization shown by many seed dispersal systems, we are far from understanding the consequences of functional losses due to population density collapses of frugivore species triggered by disturbances. In Dan Janzen’s words, this is the most pervasive kind of extinction, the extinction of interactions.

See also:
– Jarić, I., 2015. Complexity and insidiousness of cryptic function loss mechanisms. Trends in Ecology and Evolution 30, 371–372.
– Valiente-Banuet, A., Aizen, M.A., Alcántara, J.M., Arroyo, J., Cocucci, A., Galetti, M., García, M.B., García, D., Gomez, J.M., Jordano, P., Medel, R., Navarro, L., Obeso, J.R., Oviedo, R., Ramírez, N., Rey, P.J., Traveset, A., Verdú, M., Zamora, R., 2015. Beyond species loss: the extinction of ecological interactions in a changing world. Functional Ecology 29, 299–307.

Text: Excerpts from McConkey, K.R. & O’Farrill, G. 2016; and Pedro Jordano. Photo: Kulpat Saralamba.

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.

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.

Just published the third edition of SEEDS

The 3rd edition of the book, originally edited by Michael Fenner, “Seeds: the ecology of regeneration in natural plant communities” is just published (ISBN 978-1-78064-183-6). It has been edited by R.S. Gallagher, and you can find in it a revised and updated version of my chapter on “Fruits and frugivory”. 

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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.

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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.


Muriquis (Brachyteles arachnoides) are the largest neotropical primates and the largest mammal endemic to Brazil, reaching more than 12 kg (Reis et al., 2006). They are endemic to the SE Brazil.

Previously recorded as different subspecies, muriquis are currently recognized as two distinct species, the northern muriqui B. hypoxanthus and southern muriqui B. arachnoides (Rylands et al., 1997). Aguirre (1971) estimated that before the arrival of Europeans there were about 400,000 muriquis in the Atlantic rainforest, distributed from southern Bahia to northern Paraná, and in 1971 there were no more than 3,000 individuals. Currently the northern muriqui occurs in southern Bahia, Espirito Santo and Minas Gerais and the southern muriqui occurs in southern Rio de Janeiro, São Paulo and northern Paraná (Melo and Dias 2005, Hirsch et al., 2006).

The muriquis live in groups of more than 30 individuals present social fission-fusion system where the group is divided into independent sub-groups of variable size. When in pristine areas they have a higher home ranges, ca. 1000ha, within daily displacements more than 5 km. I was fortunate enough to watch a group of 10-11 muriquis in Intervales, relatively close to the Carmo base. They were 3 males, 2-3 juveniles and 3 females, two of them carrying babies. Some of the individuals were feeding on the catkins of Cecropia glazeouvi. I approached them on a very steep slope and observed them for ca. 30 min. They were moving slowly among the canopies of the trees but with an extraordinary agility, always helping themselves with the tail. After a period close to me they moved quickly uphill.

Muriquis are herbivores, adapted to the handling, chewing and digestion of leaves or fleshy fruits, and they also consume flowers, seeds and bamboo (Strier 1991; Talebi et al., 2005). In relation to frugivory, muriquis have lower consumption of fruits (21% to 33%) in semi-deciduous Atalantic forest (Strier 1991, Martins 2006, 2008), but more intense consumption (35% to 71%) in ombrophilous Atlantic rain forests (Petroni 1993, 2000, Carvalho et al ., 2004; Talebi et al., 2005).

My friend Rafael Bueno did his master project (finished in 2010) on this species and tapirs [Frugivoria e efetividade de dispersão de sementes dos últimos grandes frugívoros da Mata Atlântica: a anta (Tapirus terrestris) e o muriqui (Brachyteles arachnoides)]. He did a great job showing the relevance of these frugivores for the dynamics of the Atlantic forest. Many tree species (at least 28 species) critically depend on their service for seed dispersal. Rafael recorded daily movements of muriqui groups ranging between 0.5 and 5.4 km. He estimated that on average, individual muriquis may disperse ca. 11,000 seeds/year. These amazing data show how relevant plant-animal mutualistic interactions are for the maintenance of tropical forests.