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.

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.

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.

F1_large
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).

Rey Jaime I Award, Environmental Sciences


 

I’m very honored with being awarded the Rey Jaime I Award in Environmental Sciences this year. I was surprised with the decision of the jury during my stay in Brazil during this year’s Ciência Sem Fronteiras stay. It was great to have many, many messages with support and congratulations from many colleagues. My sincere thanks to all them!

I’m very happy with the award, as it aids supporting conservation efforts in the natural areas where I do my field work: Cazorla, Doñana, Alcornocales, Islas Canarias.

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.

PRSB 1

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.