Projects
Dimensions US-São Paulo: animal biases in fruit selection and seed dispersal as drivers of biotic filters in the assembly of successional forests and their carbon capture potential
(2021 - present)
Tropical forests play a major role in regulating the earth's climate through their effects on water cycles and their immense capacity to sequester and store atmospheric carbon. Because of their global preeminence and the threats they face, understanding the mechanisms governing community assembly, biodiversity, resilience, and emergent ecosystem functions of tropical forests is urgent. Frugivory and Seed Dispersal (FSD) are overlooked mutualistic processes involving communities of fruit-eating vertebrates (frugivores) and fleshy-fruited plants that dominate tropical forests. In fact, the vast majority of Neotropical trees depend on frugivores, most commonly birds, to disperse their seeds. This places FSD interactions as a central process directly affecting the assembly and resilience of tropical forests in the face of widespread forest disturbance and destruction. But large gaps persist in our understanding of tropical forests since FSD processes have not been seriously considered by core ecological theories. Gaps are also due to the absence of large manipulative field experiments that explore community assembly and functionality in the tropics.
This project will provide a novel and rigorous experimental test to integrate multiple theories and mechanisms to advance understanding of tropical forest assembly, biodiversity patterns, and ecosystem functions. This project builds around three Aims that link phylogenetic, genetic, and functional aspects of biodiversity in the context of the role of FSD interactions on community assembly patterns of early-successional tropical forests, as follows:
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With an experimental design that strategically incorporates functional plant traits and phylogenetic relationships as fixed-effects, the project test functional relationships between FSD processes and phylogeny in affecting community assembly (aim 1).
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The project then examines how the interaction of FSD processes with the functional-phylogenetic traits of pioneer plant species affect the genetic diversity of the plant colonizer species that follow, and in turn, how patterns of genetic diversity lead to differences in plant survival, growth, and community assembly (aim 2).
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The project ultimately explores how the biotic filtering interactions of FSD processes and the functional and phylogenetic trait diversity of successional communities influence, or are influenced by, soil microbiomes and the nutrient pools and carbon transformation processes they control (aim 3).
This project will advance fundamental knowledge by exploring ecological mechanisms and outcomes across disparate scales of biological organization rarely brought together in a single experimental framework. From trophic and seed-dispersal processes linking vertebrates and plants, to soil microbial communities and their role in mediating biogeochemical cycling of essential elements in ecosystems.
Principal Investigators: Marco Pizo (UNESP), Tomás Carlo (Pennsylvania State University)
Co-PIs: Marina Côrtes, James Marden (Penn State), Francisco Dini-Andreote (Penn State)
Collaborators and researchers: Paulo Camargo (Penn State), Pedro Brancalion (ESALQ)
Funding: FAPESP Research Grant # 2021/02943-6
Dimensions of biodiversity in assembling forest nuclei
Dimensions of biodiversity in assembling forest nuclei
ReSeeD: The contribution of animal-plant interactions to biodiversity and ecosystem restoration of the Atlantic forest
(2019 - present)
Across the world old-growth forests are rapidly diminishing due to anthropogenic forest conversion. Simultaneously, forest recovery in human-modified landscapes has led to an increase of secondary forests, which may have the potential to mitigate loss of biodiversity and provide important
ecosystem services. Human impacts regulate both tree and animal abundances, but in a different way, so that in restored fragments novel communities (in terms of plant-animal interactions) are likely to
develop. Important landscape characteristics such as surrounding land-use and surrounding native forest cover are likely to greatly affect the composition and functioning of these novel communities, by altering the influx of frugivorous animals, tree seeds and genotypes from neighboring forests. This project addresses the complex interactions between plants and animals that enable ecosystem functioning and the provisioning of ecosystem services including carbon sequestration.
We will quantify to what extent landscape connectivity affects restoration outcomes in terms of functional plant-frugivore relationships and cascading effects on carbon storage, population-level tree recruitment and genetic diversity and biodiversity conservation value in novel communities in the São Paulo Atlantic forest region. Based on our findings, we will identify priority areas within the Atlantic forest region that are most suitable for natural regeneration, and develop restoration guidelines to promote plant-frugivore interactions that enhance biodiversity and carbon sequestration where needed.
Students: Robert Timmers (Utrecht University); Willian Simioni (UNESP, Rio Claro), Carina Motta (UNESP), Guilherme Canassa (UNESP), André Martínez (Unicamp)
Collaborators: PI abroad Merel Soons (Utrecht University, The Netherlands), Marco Pizo (UNESP, Rio Claro), Mathias Pires (UNICAMP, Campinas), Marijke van Kuijk (Utrecht University), Jaboury Ghazoul (Utrecht University).
Funding: FAPESP Research Grant # 2018/19011-6
Spatial distribution and genetics of a pioneer animal dispersed tree
(2017 - 2021)
Tropical landscapes have been undergoing an increase in secondary forests. This is due to the pervasive degradation of old-growth forests and because abandoned lands are going through natural and human-induced restoration. Pioneer plants play an important ecological role in forest succession and are frequently dominant elements in these dynamic anthropogenic landscapes. Population establishment and diversity, however, depend on plants capacity to spread and recruit in often barren environments. Our goal is to evaluate how the wind pollinated and animal seed dispersed pioneer tree Cecropia hololeuca respond to landscape composition and configuration in a human-dominated Atlantic forest region. Using microsatellite markers we assessed the genetic diversity and differentiation within and between populations to infer evolutionary potential and gene flow across the region. Urban cover interspersed between populations was the main landscape feature impacting genetic differentiation, suggesting that urbanization impairs pollen and seed-mediated gene flow even of highly dispersed plants.
Also, knowing that Cecropia hololeuca is very abundant but patchily distributed in the region, we ask: what bioclimatic, anthropogenic and natural landscape features determine the spatial distribution of these widely dispersed plants? We rely on a thorough mapping of Cecropia individuals using satellite imagery, which is possible due to the silvery aspect of the upper surface of the leaf lamina.
Students: Renata Gonçalves
Collaborators: Dr. Rosane Collevatti (UFG, Goiânia), Dr. Milton Ribeiro (UNESP, Rio Claro).
Sampled landscapes, elevation gradient and landcape genetics analyses of Cecropia hololeuca
Gene dispersal of Euterpe edulis, from patches to landscapes
(2013 - present)
Seed and gene dispersal by animals is a non-random process that depends on the frugivore assemblage and how the individual dispersers interact with the environment. Therefore, disentangling the relative importance of multiple factors ranging from population characteristics, microhabitat and landscape features on seed and gene dispersal processes is important to understand how populations persist in human modified environments.
In this project, we aim at understanding how gene dispersal via movement of seeds is generated at local scale depending on microhabitat characteristics, as well as along a fragmentation and defaunation gradient in the Atlantic forest.
The study system comprises the juçara palm Euterpe edulis and its avian dispersers. Euterpe edulis is a paramount food source for several animal species, eaten by more than 20 mammals and 50 species of birds. The abundance of the palm varies immensely across its distribution mainly because of the large scale, uncontrolled, harvesting of the heart of palm, which led to the drastic reduction and local extinction of this palm in many remnants of the Atlantic Rainforest. Likewise, most of the large fruit-eating birds (toucans, toucanets and bellbirds) are functionally extinct from most of the small remnants and heavily defaunated reserves. The ecological roles provided by the different frugivore assemblages across the fragmentation gradient will most likely generate a spatial and genetic signature with unknown consequences for the long term persistence of the palm populations in highly impacted areas.
The main studies involved in this project are:
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Influence of frugivory and landscape structure on the genetic composition of dispersed seeds: we employ microsatellite markers to characterize maternal progeny in deposition sites and conduct maternity analyses to assign dispersed seeds to neighboring palms. In a multiscale approach, we aim at quantifying the direct and indirect contribution of microhabitat characteristics, plant density, avian frugivory, forest cover and other land use types on the genetic diversity of dispersed seeds.
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Relative contribution of different bird species to frugivory, seed and gene dispersal: we conduct maternity analyses on seeds endocarp and DNA barcoding on animal tissue left on dispersed seeds to connect individual propagules to both the maternal plant and avian seed disperser. For that, we are working on a permanent 1 ha plot located in an Atlantic Rainforest reserve. We expect to characterize the seed dispersal kernel for the palm population and disentangle the specific influence of each bird species. Ultimately, we will assess if patterns generated by different species or functional groups (large vs. small-body birds) are redundant or complementary in space.
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Mating system and pollination: we use seeds collected directly from palm trees to conduct progeny analyses and characterize rates of outcrossing and self-fertilization. Our goal is to compare these parameters across fragmented and protected forests to better understand the role of pollination on maintaining genetic diversity in fragments of the Atlantic forest.
Students: Lilian Kinukawa, Marília Souza, Mariana Winter, Giovane Böerner, Karen Fernandes.
Collaborators: Dr. Carolina da Silva Carvalho (Instituto Técnológico Vale, Belém), Dr. Mauro Galetti (UNESP Rio Claro), Dr. Pedro Jordano (Estación Biológica de Doñana, CSIC), Dr. Cristina García (Rede de Investigação em Biodiversidade e Biologia Evolutiva), Dr. Milton Ribeiro (UNESP Rio Claro).
Funding: CNPq Universal Program # 434115/2018-5
Spatial pattern and gene dispersal of Heliconia acuminata
(2007 - 2012)
Understanding how plants are spatially and genetically distributed in the environment can be a challenging task given the difficulty to characterize ecological processes, such as gene flow, and to disentangle the relative importance of multiple factors underlying the generation of distinct patterns. In this project we studied different populations of the understory plant Heliconia acuminata distributed across 1-ha fragments and continuous forest sites in the Biological Dynamics of Forest Fragments Project (BDFFP), an experimentally fragmented landscape in central Amazonia.
We characterized a set of ten microsatellite markers developed for Heliconia acuminata to first evaluate gene flow, which is one of the main processes influencing genetic structure and spatial patterns of plants, and second to assess the potential influence of endogenous (e.g., seed dispersal) and environmental factors on spatial patterns of plants and genetic relatedness distribution. We first combined genetic and ecological data in a comprehensive Bayesian model to estimate parentage to more fully characterize the contribution of pollen and seed dispersal to H. acuminata gene flow. Second, we used a flexible statistical methodology to model marked point patterns and evaluate whether local spatial genetic structure was associated with spatial distribution of plants. In turn, we evaluated whether the spatial distribution of plants was associated with microhabitat characteristics (soil, light) and biotic interactions.
Collaborators: Dr. María Uriarte (advisor, Columbia University), Dr. Emilio Bruna (University of Florida), Dr. John Kress (Smithsonian Institution), Dr. Maristerra Lemes and Dr. Rogério Gribel (Instituto Nacional de Pesquisas da Amazônia), Dr. Peter Smouse (Rutgers University), Dr. Janine Illian (University of Saint Andrews).
Frugivory of Euterpe edulis
(2002 - 2006)
The interaction between frugivores and fruits is the first step in the process of seed dispersal and recruitment of animal dispersed plants. Identifying the relative importance of multiple frugivores to seed dispersal of plants, as well as quantifying the extent to which microhabitat characteristics and intrinsic plant traits influence fruit selection by animals, are some of the main questions comprising studies of frugivory and seed dispersal.
In this project, we evaluated the variation in frugivory of the juçara palm Euterpe edulis at the microhabitat and habitat scale, along an elevation gradient of the Atlantic Rainforest in the State Park of Ilha do Cardoso (SP, Brazil). Euterpe edulis is a key species in the Atlantic Rainforest, its fruits are massively consumed by a broad range of mammals and birds. The species is naturally abundant in well preserved forests. Forest fragmentation, habitat loss and intense over exploitation of the palm heart have, however, led to the reduction and local extinction of this palm species in many forest remnants. Unveiling the primary processes involved in the recruitment of such an emblematic species can help us better understand the effect of the interplay of different agents and factors on the recruitment of plants in natural and human impacted environments.
Collaborators: Dr. Mauro Galetti (advisor, UNESP Rio Claro), Dr. Pedro Jordano (Estación Biológica de Doñana, CSIC), Dr. Rodrigo de Castro (Instituto Federal de Rondônia).