Seedlings planted for Brazilian forest restoration are not representative of tropical tree biodiversity

A collaborative research project involving MBG’s Center for Conservation and Sustainable Development, the Tropical Silviculture Lab at the University of São Paulo, and the PARTNERS research coordination network highlights important differences between the native tree flora of the Brazilian Atlantic Forest and the species that are widely planted for ecological restoration projects.

The Brazilian Atlantic Forest is a global biodiversity hotspot. This designation denotes two things. First, the Atlantic Forest is exceptionally and uniquely biodiverse. Second, the biodiversity of the Atlantic Forest is exceptionally threatened. This once-vast biome historically stretched from northern Argentina to Brazil’s eastern tip in Rio Grande do Norte, but it is now reduced to about 12% of its original size, and most of what remains exists as small, isolated fragments.

During the past decade, a major, multilateral effort has been undertaken to staunch biodiversity loss by doubling the size of the Atlantic Forest through ecological restoration. The Atlantic Forest Restoration Pact is composed of more than 270 private companies, governments, NGOs, and research organizations. It aims to restore 15 million hectares of Atlantic Forest by 2050.

The Atlantic Forest biome: a global biodiversity hotspot and the site of the most ambitious tropical forest restoration project on the planet. Map imagery from NASA via Wikimedia Commons.

Atlantic Forest restoration projects are characteristically thorough and well-documented. For example, they often include high diversity plantings more than 80 tree species. Yet until recently there had never been a systematic study to evaluate how well these restoration plantings represented the Atlantic Forest biodiversity they aimed to protect.

Dr. Pedro Brancalion is a professor at the University of São Paulo’s agricultural school in Piracicaba, Brazil, where he co-directs the Tropical Silviculture Lab. Five years ago, he approached me at a meeting of the Society for Ecological Restoration in Madison, Wisconsin, and over a beer he told me about a dataset that he thought could shed light on the how well Atlantic Forest restoration projects were conserving tree biodiversity. The dataset consisted of seedling donation records from the NGO SOS Mata Atlântica. Between 2002 and 2015, the NGO donated more than 14 million tree seedlings to 961 restoration projects. By comparing the species composition in these records to tree species living in mature forests, we could see what elements of biodiversity might be missing and how this could be affecting carbon stocking – an important factor in mitigating global climate change.

Even in high diversity plantings, many of the most threatened tree species were not included.

Last month, Pedro and our collaborative team published a paper in Conservation Letters describing our results. We found that restoration projects in the Atlantic Forest biome had included 416 tree species out of the >2,500 tree species known from mature and old-growth forest fragments. This is an impressive figure, but the team discovered that it reflects a highly biased subsample of the Atlantic Forest tree flora. The most under-represented species were those with large seeds that are dispersed by animals. Animal-dispersed trees make up as much as 89% of tree species in some parts of the Atlantic Forest and include some of the most threatened species.

The reason that large-seeded, animal-dispersed species are being used less often was probably related to the cost and challenges of collecting and growing seeds. Large-seeded, animal-dispersed trees are more expensive to purchase from nurseries than small-seeded or wind-dispersed species. Because they are energetically expensive to produce and are contained within large fruits, trees tend to produce large seeds in relatively low quantities, with just one or a few seeds per fruit. They are generally found in remote forest areas, and seed collectors have to compete for them with seed-eating animals, like peccaries and agoutis. Once large seeds are collected, they also take up considerably more space in storage and production facilities.

In our analysis of animal-dispersed tree species, seed diameter explained 87% of the variance in seed price. Large seeds like those of Caryocar brasiliense were much more expensive than small ones, like Ficus guaranitica. Grid size: 1 mm. Photos reproduced from C. N. Souza Junior & P. H. S. Brancalion (2016).

The absence of large-seeded, animal-dispersed tree species in restoration plantings has important implications for biodiversity conservation. First, fewer large-seeded trees means less food for large birds, some of which eat mainly large fruits. Second, these species are sometimes overharvested for timber and have difficulty recolonizing forests from which they have been removed. So the fact that large-seeded, animal-dispersed trees are under-represented in restoration projects means that even if the ambitious restoration goals of the Atlantic Forest Restoration Pact are met, the increase in forest cover may not improve dispersal between fragmented populations of the most vulnerable species.

Large-seeded tree species also tend to store carbon more densely than small-seeded species. This tendency is related to large-seeded species growing slowly in the shady understory of the Atlantic Forest and their gradual formation of dense wood, which is rich in carbon. We simulated potential carbon stocking in restored forests and compared it to mature forests, and our results showed that under-representation of large-seeded, animal-dispersed trees could cause a 2.8-10.6% reduction in carbon storage. Based on the current price of carbon, this loss could represent $17-63 USD per hectare in lost carbon credits.

Many Atlantic Forest restoration projects are quite isolated. A large seed would have a hard time reaching sites like this forest in a sugarcane matrix. Photo by Pedro Brancalion.

Reduced capacity for biodiversity conservation and carbon stocking sounds like bad news, and indeed it is not ideal. However, restoration ecology moves forward by identifying problems and seeking scientifically-based solutions to overcome them. Knowing that large-seeded, animal-dispersed trees are under-represented in restoration plantings means that we can turn our attention to innovative solutions.

For example, new policies could help bridge the gap between Brazil’s exceptional tree biodiversity and the relative paucity of species being used for ecological restoration. One way this could happen would be for the Brazilian government to subsidize the cost of producing large-seeded, animal-dispersed tree seedlings. This could be done through financial incentives or potentially by opening some forest reserves for seed harvesting, to make it easier for collectors to acquire these species. Facilitating uptake by reducing costs would be a carrot. A stick could be to legally mandate some representation of these species in future restoration plantings.

Market solutions may also exist. Based on our calculations, adding more large-seeded, animal-dispersed species to restoration plantings would increase carbon storage and carbon credits, offsetting the cost of the expensive seedlings and creating a net gain of $3-32 USD per hectare.

Banner image: Sterculia striata (Malvaceae). Photo by Mauricio Mercadante. CC BY-NC-SA 2.0.

Drivers of epiphyte recovery in secondary forests in southeastern Brazil

Alex Fernando Mendes is an undergraduate researcher in the Tropical Silviculture Lab at the University of São Paulo, Brazil. He describes his thesis project, undertaken in dozens of forest fragments in the endangered Atlantic Forest biome. Currently, Alex is analyzing his data as a visiting researcher in the Center for Conservation and Sustainable Development.

Historically, intensive agriculture in the Brazilian Atlantic Forest has caused large-scale deforestation of this biome. However, new legal requirements, land exhaustion, and the shifting priorities of farmers have recently allowed forests to regenerate on some formerly farmed lands. Given the unique nature of the Atlantic Forest, its high species endemism, and its potential for providing ecosystem services, the Tropical Silviculture Lab (LASTROP) at the University of São Paulo, coordinated by Prof. Pedro Brancalion and its partners, initiated a project in 2014 to better understand the structure and composition of these new forests.

However, forests aren’t made solely of trees. Among the plant components of a forest, there are others life forms such as epiphytes, lianas, and herbs that contribute to biodiversity and provide food, water, and shelter for many animal species. Epiphytes are plants that use other plants as support. Due to their sensitivity to environmental changes, epiphytes can be used as bioindicators. Therefore, we asked how these plants are doing in these young regenerating forests. And what landscape and local attributes facilitate or hinder their recolonization?

Epiphyte species found in second-growth forests of the Atlantic Forest – A) Philodendron bipinnatifidum Schott; B) Lepismium houlletianum (Lem.) Barthlott.; C) Ionopsis utricularioides (Sw.) Lindl.; D) Catasetum fimbriatum (E. Morren) Lindl. & Paxton; E) Aechmea bromeliifolia (Rudge) Baker; F) Billbergia sp.

 

To try to answer these questions, we are studying the epiphyte communities in 40 second-growth forests (i.e., forests that were once completely cut down). We are considering three landscape drivers (distance from watercourses, distance from forest edge and forest cover in a 1-km buffer around the remnant) and four local drivers (previous land use, forest age, liana abundance, and tree basal area). We expect that forests close to watercourses would provide the moisture required by epiphytes. We expect to find more epiphytes further from the forest edge since forest cover in more conserved forests may limit their establishment. Since our forests regenerated from abandoned eucalyptus plantation and pastures, we want to check if the non-native eucalyptus could act as a filter preventing epiphytes recolonization. We also expect that older forests and forests with more basal area could house more epiphytes than young forests. Finally, field observations made us wonder if lianas could compete with epiphytes by occupying the same niche.

Of the more than 6,000 phorophytes (trees that could support epiphytes) sampled in these 40 forests we found 398 epiphytes belonging to 21 morphospecies distributed in 4 families (Araceae – 1 species, Bromeliaceae – 14 species, Cactaceae – 5 species, Orchidaceae – 5 species). Only three species, Tillandsia pohliana, Tillandsia tricholepis, and Ionopsis utricularioides, represented more than half (59.5%) of all epiphytes found in second-growth forests. The genus Tillandsia was expected to be abundant in these young forests, since these are disturbance-adapted species that can even be found growing on power lines in cities.

Epiphytes of the genus Tillandsia (Bromeliaceae) are often found in extreme microenvironments in urban areas (Photos by A. Mendes, 2017).

Our analysis is in progress, but our preliminary observations suggest that forests closer to watercourses and closer to forest edge are more likely to have epiphyte recolonization than forests far from edge and watercourses. Forests regenerated on pastures have more epiphytes than those on abandoned eucalyptus plantation. Our dataset will soon be upgraded with new forest types: conserved and disturbed old-growth forests, and mixed tree plantings for forest restoration, totaling approximately 70 forests with epiphyte samples.

With this research, we hope to find out the local and landscape factors that contribute to epiphyte recolonization in second-growth forests. In practice, this will allow us to locate sites with limited potential for spontaneous colonization of this life form to take actions that promote colonization and establishment, such as introducing individuals. Finally, by identifying epiphytes species that are more sensitive to disturbance, we can focus our reintroduction interventions.

Small, remnant forests are surrounded by cattle pastures in southern Brazil.

Note: The image of Philodendron bipinnatifidum featured at the top of this post was taken by David Stang. 

Epiphyte restoration in Brazil’s Atlantic Forest

CCSD restoration ecologist and PARTNERS member Leighton Reid spent 10 days collaborating with scientists and students in the Tropical Silviculture Lab (LASTROP) at the University of São Paulo. Epiphytes were a central theme of the visit.

Vascular epiphytes are plants that live non-parasitically on other plants. Readers from the tropics will be quite familiar with some epiphytes, like the ubiquitous Tillandsia of Neotropical powerlines, but temperate zoners will have seen many epiphytes as well, at the florist, the botanical garden, and the mall. These plants are incredibly diverse; by one estimate, epiphytes make up 9% of all vascular plants worldwide. But epiphytes also face serious challenges in today’s world. Habitat loss and overharvesting threaten some epiphyte species with extinction. Many epiphytes also have a hard time recolonizing new habitat in regenerating forests, but new studies on epiphyte restoration could help.

I spent the past 10 days in the State of São Paulo learning about epiphyte ecology, conservation, and restoration from students and scientists at the University of São Paulo’s College of Agriculture (Escola Superior de Agricultura Luiz de Queiroz). This part of Brazil was once covered in semideciduous tropical and subtropical forests, which hosted about 150 vascular epiphyte species. Today, only ~15% of the forest remains, but there is a large effort underway to restore 15 million hectares (nearly 58,000 square miles) of it by 2050.

ESALQ maintains shade house with more than 3,000 orchids, including (A) Cattleya loddigesii, (B) C. forbesii, and (C) Arpophyllum giganteum.

Frederico Domene is a doctoral student studying epiphyte reintroduction in restored Atlantic Forest. Like his advisor, Pedro Brancalion, Fred’s interest in epiphyte restoration stems from a passion for orchids. He grows a variety of them at his house in Piracicaba, preferring true species over horticultural varieties.

Fred picked me up in his black pickup, “mamangava”, and took me on a tour of several tree plantations where he has been developing methods for reestablishing populations of epiphytic orchids, bromeliads, cacti, and aroids. Fred’s basic procedure involves collecting epiphyte seeds (or purchasing small plants, in the case of orchids), growing them out in a nursery, and then attaching them to trees using twine or plastic. He started his work in 2010 and has been monitoring his plants, and reintroducing new plants, every year since. He uses a ladder to put the orchids up high, out of easy reach for would-be poachers.

Atlantic Forest restoration plantations. Left: 60-year old plantation along the Rio Piracicaba near Rio Claro. Right: 12-year old plantation at the Anhembi Forest Science Experimental Station. The older restoration site had considerably more naturally recolonizing epiphytes than the younger site.

Late August is mid-winter in São Paulo, and while it doesn’t get particularly cold, it is quite dry. The restoration plantations were crunchy with desiccated leaves and twigs. These are harsh conditions for epiphytes, which do not have the luxury of soil to buffer to their roots from the sunlight and dry air. Some of Fred’s epiphytes have withered and died, especially during a 100-year drought in 2012. But others are thriving, thanks to special adaptations, such as the velamen of orchid roots, which wicks up rainwater when it drips down the tree trunk during storms. Many individuals have started fruiting and flowering, a good sign for the future viability of these reintroduced populations.

Epiphyte reintroductions in restoration plantations. (A) A reintroduced festoon of bromeliads, orchids, and cacti. (B) A fruit-bearing orchid (Cattleya forbesii), six years after reintroduction. (C) This reintroduced cactus (Epiphyllum phyllanthus) seemed to grow better in tree forks than on vertical stems, as did an aroid, (D) Philodendron bipinnatifidum. (E) Two tiny cacti have germinated in this direct seeding experiment, using seeds enrobed in paper discs. (F) Even where epiphytes have dessicated and died, experimental infrastructure continues to enhance epiphyte development; here a small bromeliad (Tillandsia recurvata) uses a piece of natural twine as a foothold.

To identify the key challenges for epiphyte restoration, it is also important to study epiphyte recolonization in naturally regenerating forests. Alex Mendes, an undergraduate researcher at ESALQ, is doing just that. On an unseasonably rainy morning, Alex, Fred, and I visited three regenerating forests near the sugar town of Rio Claro. We ducked under barbed wire fences and wandered through low, dense vegetation where Alex is systematically searching for vascular epiphytes. Two forests had rather few epiphytes – mostly generalist bromeliads – but one forest had a high density of orchids, which happened to be flowering spectacularly on the day we visited. Based on historical aerial photos, Alex knows that these three forests are at least 20 years old. They are part of a network of 75 sites that he will ultimately search for epiphytes. By the end of his undergraduate program, Alex hopes to be able to predict where epiphyte communities will regenerate on their own, and where they will need more assistance.

This secondary forest near Rio Claro might have felt like your average overgrown Psidium guajava patch had it not been  decorated with dozens of Ionopsis sp. orchids.

These are early days for learning about epiphyte restoration, and there is still a lot of work to be done. The projects that I visited in Brazil are making headway, complementing our research in Costa Rica. It remains to be seen under what circumstances epiphyte reintroductions will be most successful. Perhaps an even more important issue will be convincing funding agencies and land managers to think beyond trees.

Fred Domene and Alex Mendes are making strides in the ecology of epiphyte reintroductions and community assembly. Here, they pose with a reintroduced bromeliad (Billbergia zebrina) at Anhembi experimental station.