Harper Prize Shortlist 2019: Mauro Brum

“We are nothing if we do not deal with our roots.”

Author Mauro Brum offers an insight into his paper “Hydrological niche segregation defines forest structure and drought tolerance strategies in a seasonal Amazon forest“, which was shortlisted for the 2019 Harper Prize.  Mauro also discusses his further research and what (and who!) inspired him to pursue a career in ecology. You can see a full list of all shortlisted papers in the Harper Prize 2019 Virtual Issue.


About the paper

This paper stems from my PhD work at the University of Campinas in Brazil that was part of a wider FAPESP (São Paolo Research Foundation)-funded project entitled Understanding the Response of Photosynthetic Metabolism in Tropical Forests to Seasonal Climate Variations in cooperation with the US Department of Energy, which sought to understand the overall drought-resilience mechanisms in tropical Amazon forest and how this diverse ecosystem might respond to expected climate change. Our part of this large project was to elucidate the ecohydrological mechanisms behind photosynthetic metabolism in tropical forests to seasonal climate variations.

In the paper, we highlighted the underlying role of water availability in niche partitioning and species coexistence in our study site in the Tapajós National Forest, a highly diverse ecosystem in the Brazilian seasonal Amazon forest. We showed that differences in vertical soil water uptake by plants select for differences in drought tolerance/avoidance strategies defined by the covariance of root depth, tree size and vulnerability to xylem embolism in dominant species within a community. We also derived an equation to estimate the effective functional rooting depth, i.e. the likely maximum soil depth from which roots take up water for physiological functions. For Amazon seasonal sites, we can use a simple variable, such as DBH (diameter at breast height), to parameterize the model representation of rooting depth, which is considered a hard trait to measure.

For the first time, we presented a model that can estimate with relatively high probabilistic accuracy the effective rooting depth pattern for an entire community. We also showed that shallow-rooted plants were selected by a higher tolerance to xylem embolism formation, and they tolerate a higher decrease in water potential status during a strong drought induced by the 2015/2016 El-Niño Southern Oscillation (ENSO).

Tapajós National Forest in Brasilian seasonal eastern Amazon 2015. Left panel the flux tower from LBA project (Large Scale Atmospheric Biosphere project). Right panel the overview of forest canopy observed from 60 m height in the flux tower.

Questions stemming from the work

We suggested that differences in drought tolerance/avoidance strategies would also likely be reflected along tree ontogeny in Tapajós Forest. In my current postdoc research we are testing what we called a niche acclimation hypothesis where young trees of dominant canopy species must start out with relatively shallow roots, and during this phase of development may need a high degree of embolism resistance to survive in the dense understory environment where competition for space and water among smaller trees can be intense during dry seasons. Understory tree species, on the other hand, would present less variability in drought tolerance mechanisms along their ontogeny, since they will survive for most of the time in shallow soil with higher variability in water availability.

Also, we would expect leaf phenology of canopy trees to respond more to light availability, while the phenology of shallow-rooted smaller trees would be driven mostly by water availability. We are building on previous work by Smith et al. (2019) who started answering such questions.

About the research

We faced the normal challenges of field work in a tropical forest: the main problem was to reach the canopy trees to sample for leaves and branches. I do not know how to climb trees, so always depended on somebody else for bringing me samples from the canopy. Most canopy trees are higher than 40 m, limiting our sample size.

The 2015/2016 ENSO induced a strong unplanned drought stress during my studies, and we were able to use the natural abundance of stable isotopes of water to estimate root water uptake at that moment. The stable isotopes method is effective only when there is a gradient in water isotope ratios with depth, caused by evaporative enrichment at the soil surface. Thanks to the ENSO event we were able to get this fractioning without water from precipitation (with a different isotopic signal) diluting the soil water.

These data were key to the discoveries we made and the conclusions we drew. We were also able to measure the extreme water potential status that plants can reach during extreme events. Those ground and plant-level data are very helpful for parametrizing models that want to predict forest response and resilience to extreme events induced by periodic droughts.

Contributions to the wider field

We showed for the first time that plant diversity in a tropical Amazon ecosystem is driven by hydrological niche segregation. Silvertown et al. (1999) and Araya et al. (2010) proposed that the most dominant plant groups partition space at relatively fine scales. The distance at which competition is minimized through this partitioning can actually be estimated. Our results support these assertions, and show that seasonal Amazon trees use different strategies to partition water as a resource. These strategies reflect different means of handling drought tolerance and avoidance.

In addition, Starck et al. (2012; 2015) previously had shown that in the Tapajós seasonal Amazon forest the distributions of leaf area and light environments are strongly related to DBH distribution, as individuals optimize their productivity over the vertical gradient to create consistent relationships between canopy light environments and biomass growth. Our results further suggest that rooting depth increases with tree height, compensating for the greater evaporative demand at the top of the canopy and allowing larger trees to be photosynthetically active during the dry season. The spatial variation in light and water, what we called the eco-hydro-light niche, along vertical profiles drives niche partitioning, and forest structural and taxonomic organization within the Tapajós community.

About the author

During my undergraduate biology degree, I took part in an ecology field course in the Brazilian Cerrado, where I met Professor Dr. Rafael S. Olveira who steered me towards plant ecophysiology and has catalysed my history ever since. He has been a good adviser and thanks to him, I am where I am now.  I also had very good friends during my studies who always encouraged me to move forward.

Tumucumaque National Park in north Amazon, Amapá-Brazil, November 2019. From left to right, my advisor Professor Dr. Rafael S. Oliveira, myself in the middle, and my friend and co-author of JoE paper Dr. Paulo Bittencourt.

At the moment I’m a postdoc researcher investigating carbon cycling using multiple methods related to an NSF-funded project entitled: “Are Amazon forest trees source or sink limited? Mapping hydraulic traits to carbon allocation strategies to decipher forest function during drought”, under the supervision of Professor Dr. Scott Saleska from the Department of Ecology & Evolutionary Biology at the University of Arizona. I met him during my field works in Tapajós National Forest in Brazil, and he has since invited me to join his amazing research team.

For you understand what it means to be an ecologist today in Brazil, I’ll refer you to the editorial written by Jos Barlow for the BES Virtual Issue Ecology in Brazil. Investment in science is decreasing in Brazil, laws aimed at conserving natural landscapes are being relaxed and science denial is rife in political circles. It is not enough to be an advocate for science these days, ecologists in Brazil also need to start engaging at a political level and try to save what is left.

This paper in Journal of Ecology is very, very special to me because of its scientific importance and novelty. However, I have a special feeling for a research paper that came out of my master’s degree during which I worked on the ecophysiology of plants from Campos Rupestres, high-altitude, fire-prone grasslands with rocky outcrops occurring in Brazil. In the supplementary material of Brum et al. (2017) there are few pictures of the roots that I worked with. When I produced those materials, I had one of the most philosophical enlightenments that still drives my thoughts today, “We are nothing if we do not deal with our roots”. Since then I consider myself as a root ecophysiologist.


You can read all of the Harper Prize 2019 shortlisted papers in our Virtual Issue.


References 

Araya, Y. N., Silvertown, J., Gowing, D. J., McConway, K. J., Peter Linder, H., & Midgley, G. (2011). A fundamental, eco‐hydrological basis for niche segregation in plant communities. New Phytologist, 189(1), 253-258. https://doi.org/10.1111/j.1469-8137.2010.03475.x

Brum, M., Teodoro, G.S., Abrahão, A. et al. Coordination of rooting depth and leaf hydraulic traits defines drought-related strategies in the campos rupestres, a tropical montane biodiversity hotspot. Plant Soil 420, 467–480 (2017). https://doi.org/10.1007/s11104-017-3330-x

Silvertown, J., Dodd, M. E., Gowing, D. J., & Mountford, J. O. (1999). Hydrologically defined niches reveal a basis for species richness in plant communities. Nature, 400(6739), 61-63.

Smith, M. N., Stark, S. C., Taylor, T. C., Ferreira, M. L., de Oliveira, E., Restrepo‐Coupe, N., Chen, S. , Woodcock, T., dos Santos, D. B., Alves, L. F., Figueira, M. , de Camargo, P. B., de Oliveira, R. C., Aragão, L. E., Falk, D. A., McMahon, S. M., Huxman, T. E. and Saleska, S. R. (2019) Seasonal and drought related changes in leaf area profiles depend on height and light environment in an Amazon forest. New Phytologist, 222: 1284-1297. https://doi.org/10.1111/nph.15726

Stark, S. C., Enquist, B. J., Saleska, S. R., Leitold, V., Schietti, J., Longo, M., Alves, L. F, Camargo, P. B., Oliveira, R. C. (2015). Linking canopy leaf area and light environments with tree size distributions to explain Amazon forest demography. Ecology Letters, 18(7), 636–645. https://doi.org/10.1111/ele.12440

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