Chasing interactions

Ecological interactions are the wireframe of biodiversity. No single species on Earth lives without interacting with other species. Thus, biodiversity is more than just species: interactions among them are the architecture that supports ecosystems. It’s the Web of Life.

Just in the same way we sample individuals of free living species to estimate the diversity of a particular area or ecosystem, we can sample interactions. In this way we can assess the full complexity of ecosystem structure.

Our paper on defaunation effects on carbon storage in tropical forests

Plant-animal mutualisms for seed dispersal are key to preserve tropical forests and many other ecosystems (e.g., Mediterranean forests). These interactions may go extinct, and pervasively affect the forests in many aspects. One of them is a substantial loss of carbon storage capacity, simply as a result of collapsed recruitment of large-seeded trees.

Our study shows that the extinction of large animals has negative impacts on climate change.

Bello C., Galetti M., Pizo M.A., Magnago L.F.S., Ferreira Rocha M., Lima R.A.F., Peres C.A., Ovaskainen O., and Jordano P. 2015. Defaunation affects carbon storage in tropical forests. Science Advances, 1(11): e1501105. doi: 10.1126/sciadv.1501105


Defaunation, the severe decline of animal populations from natural ecosystems, is a process faced by tropical forests that can go unnoticed. Several large birds and mammals are threatened by hunting and human persecution. However, the loss of animals can bring about large unforeseen impacts. The extinction of large mammals implies the loss of functions that maintain diversity and ecosystem services on which humans depend.

Our recent study published in the journal Science Advances was conducted by Brazilian researchers from the Universidade Estadual Paulista (São Paulo State University) in Rio Claro, in collaboration with researchers from Spain, England, and Finland, and demonstrated that the loss of large frugivores negatively affects the capacity of tropical forests to stock carbon and, therefore, their potential to counter climate change.

The big frugivores, such as large primates, the tapir, the toucans, among other large animals, are the only ones able to effectively disperse plants that have large seeds. Usually, the trees that have large seeds are big trees with dense wood that store more carbon.

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Figure. Large frugivores and large-seeded trees of the Atlantic Forest. Mauro Galetti author of the photos a, d, and e. Pedro Jordano author of photos b, c, and f.

When we lose large frugivores we are losing dispersal and recruitment functions of large seeded trees and therefore, the composition of tropical forests changes. The result is a new forest dominated by smaller trees with milder woods which stock less carbon.

Our study showed that when large-seeded trees are removed from the forest and are replaced by trees with smaller seeds, the carbon stock potential of the forest decreases. This is a net result of the seed dispersal and recruitment collapse that entails the large frugivores extinction.

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Replacement process of tree species composition in tropical forests when they lose large dispersers. Forests with large trees and hardwood (initial community) are replaced by forests with smaller trees with mild wood (final community).

This is the result of the loss of crucial interactions that support the Web of Life in tropical forests. Not only we are facing the loss of charismatic animals, but we are facing the loss of interactions that maintain the proper functioning and key ecosystem services such as carbon storage. To date, tropical forest degradation has been entirely defined by REDD+ programs in terms of structural forms of human disturbance such as timber extraction and wildfires. Yet, even an apparently intact but otherwise defaunated forest should be considered as degraded because the insidious carbon erosion processes we highlight in this paper are already well underway.

Our study alerts current REDD+ programs that seek to counteract climate change by storing carbon in tropical forests, about the importance of considering the animals and their functionality as a fundamental part of the maintenance of carbon stocks. The effectiveness of these programs will be improved if the preservation of ecological processes that sustain the ecosystem service of carbon storage over time is guaranteed.

The study also included Marco A. Pizo (UNESP), Otso Ovaskainen (University of Helsinki), Renato Lima (USP), Luiz Fernando S. Magnago (Federal University of Lavras) and Mariana Rocha Ferreira (Federal University of Viçosa).

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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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.

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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.

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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 new book, Mutualistic networks, just published by Princeton University Press

Book cover
Book cover

We have just published our book “Mutualistic Networks“, the no. 53 issue in the series Monographs in Population Biology of Princeton University Press.

Mutualistic interactions among plants and animals have played a paramount role in shaping biodiversity. Yet the majority of studies on mutualistic interactions have involved only a few species, as opposed to broader mutual connections between communities of organisms. Our book comprehensively explores this burgeoning field. Integrating different approaches, from the statistical description of network structures to the development of new analytical frameworks, we describe the architecture of these mutualistic networks and show their importance for the robustness of biodiversity and the coevolutionary process.

Making a case for why we should care about mutualisms and their complex networks, we offer a new perspective on the study and synthesis of this growing area for ecologists and evolutionary biologists.

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.

Components of pollination effectiveness and their consequences in insular pollinator assemblages

Our paper “Quantity and quality components of effectiveness in insular pollinator assemblages” online in Oecologia. Thanks Cande and Alfredo. This is a field study of the pollination of Isoplexis canariensis by birds and lizards in the Canary Islands, a part of Cande Rodríguez PhD project.

Ecologically isolated habitats (e.g., oceanic islands) favor the appearance of small assemblages of pollinators, generally characterized by highly contrasted life modes (e.g., birds, lizards), and opportunistic nectar-feeding behavior. Different life modes should promote a low functional equivalence among pollinators, while opportunistic nectar feeding would lead to reduced and unpredictable pollination effectiveness (PE) compared to more specialized nectarivores.

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Dissecting the quantity (QNC) and quality (QLC) components of PE, we studied the opportunistic bird–lizard pollinator assemblage of Isoplexis canariensis from the Canary Islands to experimentally evaluate these potential characteristics. Birds and lizards showed different positions in the PE landscape, highlighting their low functional equivalence. Birds were more efficient than lizards due to higher visitation frequency (QNC). Adult lizards differed from juveniles in effecting a higher production of viable seeds (QLC). The disparate life modes of birds and lizards resulted in ample intra- and inter-specific PE variance. The main sources of PE variance were visitation frequency (both lizards and birds), number of flowers probed (lizards) and proportion of viable seeds resulting from a single visit (birds).

The non-coincident locations of birds and lizards on the PE landscape indicate potential constraints for effectiveness. Variations in pollinator abundance can result in major effectiveness shifts only if QLC is relatively high, while changes in QLC would increase PE substantially only at high QNC. The low functional equivalence of impoverished, highly contrasted pollinator assemblages may be an early diagnostic signal for pollinator extinction potentially driving the collapse of mutualistic services.