Our lab builds spatial models and conducts both field and laboratory experiments to understand the biotic and abiotic mechanisms underlying the distribution of wildlife and their pathogens from local to global scales, with the overarching goal of diagnosing patterns of biodiversity threats and loss. Our research interests fall at the interface of host-microbial interactions, landscape ecology, and conservation biology, and our research includes detailed mechanistic studies that can be divided into four broad areas of investigation: 1) host-microbe interactions, 2) diversity-disease relationships, 3) spatial ecology & landscape genetics, and 4) translating scientific findings to conservation. The conceptual thread tying these areas together is the understanding that the ecology of these various threats to wildlife has important implications for evolutionary processes and conservation, and thus, will be instrumental in the determination of general patterns of biodiversity persistence. A large fraction of our work has focused on tropical amphibians due to accelerated population declines and extinctions such as those observed in the Neotropics.
1) Host-microbe Interactions
We have been investigating how anthropogenic interference on both vegetation and climate impact host-microbie interactions. We have been investigating the impact of forest fragmentation and connectivity on the assembly of host microbiomes (Figure 1) (Becker et al. 2017 Proceedings of the Royal Society of London - B) and disease (Becker & Zamudio 2011 PNAS, Becker et al. 2016 Basic & Applied Ecology). Our future research in this topic will involve understanding how repeated exposure to pathogens alter community dynamics within the host skin microbiome and promote competitive microbial interactions and host responses that enrich the microbiome with anti-pathogen members. This form of acquired pathogen resistance, termed microbial memory, may facilitate host recovery and prime the host for future pathogen exposures. Anthropogenic habitat disturbance and fragmentation notoriously restrict host movement at the landscape scale, which may alter rates of pathogen exposure that are critical for establishing microbial memory prior to seasonal increases in pathogen pressure (i.e., during breeding aggregations). More specifically, different patterns of human land use, spatial connectivity and pathogen pressure could result in diverging host microbial assemblages, leading to seasonal changes in adaptive immune function (microbial memory) and disease susceptibility. Using amphibians of as a model system, we are currently planning field experiments, including bacterial culturing and challenge assays, host microbiome manipulation, and radio telemetry of individual hosts in the wild to test for mechanisms linking habitat connectivity, disease, and the microbiome independently from other components of host immunity.
Figure 1. Spatial connectivity is linked to host microbiome similarity.
Our lab recently witnessed a local outbreak of chytridiomycosis in a population of terrestrial-breeding toadlets (Figure 2a). One of our recent experimental manipulations supports the hypothesis that low-load pathogen spillover from aquatic-breeding frogs may be enough to cause rapid increases in pathogen loads, microbiome dysbiosis, and mortality in terrestrial toadlets (Figure 2b) (Becker et al. 2019, Proceedings of the Royal Society of London - B).
Figure 2. (a) Outbreak of chytridiomycosis in a population of Brachycephalus ephippium (Photo by Diego Moura) (b) spillover of chytrid fungus and opportunistic bacteria from aquatic-breeding species to terrestrial-breeding Brachycephalus pitanga
2) Diversity-disease Relationships
Habitat destruction and alteration can have profound consequences on disease, as shifts in diversity at both host and microbiome scales can alter the risk of epizootics. Our lab has worked to identify circumstances in which host species diversity promotes an increase (pathogen amplification; Becker et al. 2015 Basic & Applied Ecology) or decrease (pathogen dilution; Becker et al. 2014 Proceedings of the Royal Society B) in disease risk. More recently, our lab showed that diverse pools of pathogen genotypes could favor pathogen hybridization and give rise to strains more virulent than the parental lineages (Figure 3) (Greenspan et al. 2018 Scientific reports).
Figure 3. Hybrids of amphibian chytrid show high virulence in native hosts.
Our lab has also recently demonstrated that diversity of bacterial community in the water column of bromeliads is positively associated with opportunistic infections and disease risk in tadpoles, and that diverse communities of filter-feeding arthropods reduce opportunistic microbes and disease in amphibian hosts (Figure 4a) (Greenspan et al. 2019, Proceedings of the Royal Society of London - B), underscoring the major impacts of multiple scales of diversity on the structure and functioning of bromeliad micro-ecosystems. As a follow up, our lab has recently led a field experiment on biodiversity-ecosystem functioning simulating predicted temperature increases in bromeliads (using automated radiators) to test how global warming influences the assembly of both aquatic microorganism and arthropod communities. Results indicate that increasing temperatures enhance the risk of gut microbiome dymbiosis in vertebrates (tadpoles) associated to bromeliad micro-ecosystems (Greenspan et al. 2020, Nature Climate Change; Figure 4b).
Figure 4. Arthropod-bacteria interaction influence diversity of the aquatic host microbiome and host gut micro biome function.
3) Spatial Ecology & Landscape Genetics
We rely on landscape ecology to answer many eco-evolutionary questions. We have been interested in how landscape complementation and discontinuity between terrestrial and aquatic habitats (habitat split) affect population stability in amphibians. We have demonstrated that habitat split forces amphibians to make risky breeding migrations between suitable aquatic and terrestrial habitats in disturbed fragmented landscapes (Figure 5a) (Becker et al. 2010 Conservation Biology), and that this mechanism is capable of reducing species diversity across tropical amphibian communities (Figure 5b) (Becker et al. 2008 Science), reinforcing the need for investments in the restoration of riparian habitats and corridors linking breeding and natural upland habitats. Our lab has been involved in fine-scale spatial population genetic efforts focusing on taxa as diverse as pond-breeding salamanders, field crickets, and mayflies in the U.S., freshwater turtles in the Iberian Peninsula, and tropical frogs and snakes in the Atlantic Forest. In collaboration with the Savage Lab at University of Central Florida, we are proposing to test how landscape configuration impacts diversity and expression of MHC genes in tropical amphibians afflicted with the chytrid fungus.
Figure 5. Habitat split forces aquatic-breeding amphibians to migrate through inhospitable environments during breeding season (a), a process linked to local extinctions and declines in amphibian diversity across tropical amphibian communities (b).
Figure 6. Systematic conservation planning incorporating species life history and different patterns of habitat fragmentation produces more ecologically relevant conservation strategies (Becker et al. 2010, Diversity & Distributions). This map highlights the importance of the Mantiqueira mountains to safeguarding endemic amphibian species breeding with varying breeding requirements: flowing water (FW), still water (permanent - SP and temporary - ST) and in the forest floor (DI). We have been informing decision makers with relevant scientific information for the implementation of a new National Park along the ridges of Mantiqueira, Brazil (Becker et al. 2013, Science).
Cumulatively, our research underscores the importance of understanding interactions between environmental change and disease −two key factors at the root of the current biodiversity crisis −to curbing further extinctions and developing effective mitigation and restoration programs. Research in the Becker Lab will continue to focus on these two important forces, through spatially oriented studies, manipulative field and laboratory experiments, and demographic models that integrate ecological and evolutionary approaches to advance theoretical ecology and develop effective conservation strategies.
A specimen of Holoaden bradei, last seen in the wild in 1978 and likely extinct, sits in what was once its natural habitat: Itatiaia National Park, Rio de Janeiro / Minas Gerais, Brazil
Photo © Gui Becker
4) From Basic to Applied: Translating Scientific Findings to Conservation
The current biodiversity crisis makes it impossible for organismal biologists and wildlife disease ecologists to conduct research without considering threats to habitats, fauna and flora. The negative impacts on environmental protection and the limited budgets for science & technology in the US and many countries in Latin America motivated us to strengthen our focus on conservation science. Our lab is actively engaged in applying our research to the management of endangered and threatened species, and we attempt to make applied conservation biology available to the decision-makers that implement biodiversity conservation plans. Our lab has been leading and co-authoring research on (i) systematic conservation planning aiming to pinpoint priority areas for conservation (Figure 6) (Becker et al. 2011 Diversity & Distributions, Loyola et al. 2008 PLoS One), (ii) the impact of exotic species on the native fauna (Forti et al. 2017 PLoS One), (iii) the effect of pathogen pressure on endangerment (Projeto Dots link), and (iv) how life history affect microendemism and conservation success (Toledo et al. 2014 Biological Conservation); results that have been considered in Red List assessments.