Thursday, November 21, 2024

🏆Eminent Ecologist 2024: Fernando T. Maestre (part III: biocrust ecology)

Ecology🏆Eminent Ecologist 2024: Fernando T. Maestre (part III: biocrust ecology)


The Journal of Ecology Editors are delighted to announce that Fernando Maestre is our Eminent Ecologist award winner for 2024!

In recognition of his work, we asked Fernando to put together a virtual issue of some of his favourite contributions to the journal. Fernando has also written this blog series, and was interviewed by Richard Bardgett about about how he started his career in ecology, how he uses his work to inform decision making, and the advice he’d give to someone about to embark on a career in ecology. Fernando’s full blog series can be found here: Part 1 | Part 2 | Part 3 👇 | Part 4 (coming soon) | Part 5 (coming soon)


Part III. Setting up a new lab and working with your favorite organisms

Over my career I had the chance of starting a new lab three times so far in two different countries (Rey Juan Carlos University [URJC] in 2005, University of Alicante [UA] in 2019, and King Abdullah University of Science and Technology [KAUST] in 2024). Like virtually all Principal Investigators (PIs), I was never trained about how to start, manage, and run a research group and all of a sudden I transitioned from being a postdoc to being a new PI with teaching, training, and administrative duties, and with the need and pressure to bring in external funding to launch my lab and research program. Setting up a new lab has always been a mixture of excitement, uncertainty, and hard work, and provided me with the opportunity to think about and reshape/refocus my objectives as a scientist. Two things were very clear to me when setting up my first lab at URJC: i) I wanted to focus my research program on drylands, and ii) creating a collaborative environment would be a top priority for me as a PI.

Figure 1. The Dryland Ecology and Global Change Lab at some points in time. From upper to lower and left to right: 2008, 2012, 2017, and 2022.

Getting to work back in the field after my postdoc at the time was easy given the amount of very interesting and relatively well-preserved drylands that can be found in central Spain and the prevalence there of biocrusts, one of my favorite communities. Biocrusts, communities that result “from an intimate association between soil particles and differing proportions of photoautotrophic (e.g. cyanobacteria, algae, lichens, bryophytes) and heterotrophic (e.g. bacteria, fungi, archaea) organisms, which live within, or immediately on top of, the uppermost millimetres of soil” (Weber et al. 2022) already sparked my interest as a biology undergraduate and PhD student (Maestre 2003, Maestre & Cortina. 2002, Maestre et al. 2002, 2005), as they were also abundant in Sax, my hometown, and PhD study sites. When I started my PhD there were very few colleagues studying their ecology in Spain, despite the fact their taxonomy and physiology were quite well known thanks to the work of lichenologists and bryologists such as Ana Crespo, Eva Barreno and Leopoldo García-Sancho. Internationally, biocrusts were often seen by many colleagues at the time as something of marginal interest (compared to plant communities) and thus more a “niche” than a “mainstream” topic for ecologists and soil scientists. Inspired by the work of giants like Jayne Belnap in the USA and David Eldridge in Australia, who later became a very good friend a long-term collaborator, I certainly wanted to contribute to change by making the study of biocrust ecology a key research topic within my new lab, and by using biocrusts as model organisms to explore questions of general interest.

Figure 2. Biocrusts have always intrigued me and not only are key determinants of the structure and functioning of drylands but are also a wonderful model community to work with. Plus, they are beautiful and very photogenic!

Our biocrust research program was launched thanks to the support of the British Ecological Society (BES), which awarded me with an Early Career Project Grant in 2006 to conduct experimental work using biocrusts, and to the dedication of my students like Andrea Castillo-Monroy, who arrived soon after the establishment of the lab and focused her PhD research on these organisms. This BES grant funded the work that led to the fifth article of this virtual issue (Maestre et al. 2012). Here we report results from two microcosm experiments using model biological soil crust communities dominated by lichens to evaluate the joint effects and relative importance of changes in species composition, spatial pattern, evenness, and richness on soil functions and multifunctionality. We found that the probability of sustaining multiple ecosystem functions increased with species richness, but this effect was largely modulated by attributes such as species evenness, composition and spatial pattern. We worked very hard in these experiments, which were seen as crazy by some colleagues at the time (we had to cut over 20000 1 cm x 1 cm lichen squares to set up the microsoms!), but this project was lots of fun and also allowed me to start working on the concept of multifunctionality, which has also been a prevalent focus of our research since then.

Figure 3. Setting up and harvesting the experiment presented in Maestre et al. (2012), one of these crazy experiments that you only do when you are young.

Our work with biocrusts also involved conducting observational studies along experimental gradients, which we did for the sixth article of this virtual issue (Bowker et al. 2010). This work was led by Matthew Bowker, who was the first postdoc I mentored. I had been following Matt´s articles with great interest and was very pleased (and surprised!) when he asked if there was a possibility to join my new lab in Spain. I remember telling him “Matt, it’s usually Spanish PhDs that go to the USA for a postdoc, not the other way around!” But he wanted to work with us, and this was possible thanks to a competitive “Juan de la Cierva” fellowship that he obtained from the Spanish Ministry of Science in 2007. I cannot be more grateful to Matt for joining my lab, as he was not only fundamental to launching our biocrusts research program, but he taught me a lot (to be honest I do not know who mentored who!), did wonderful research that led to multiple articles (Matt is one of the best writers I had the chance to work with), and did a fantastic job mentoring and collaborating with other students and lab members, thus contributing to creating a healthy and collaborative atmosphere in the lab. Plus, we became close friends and long-term collaborators, a friendship that lasts until today. But coming back to the paper, for this study we conducted the first regional-scale test of the Stress-gradient hypothesis using biocrusts dominated by mosses and lichens. In doing so, we examined the intensity of facilitative or competitive interactions at the level of the community and among species pairs along an aridity gradient. Our results suggested that negative species interactions are prevalent in this study system and much more common than expected by chance, and that abiotic stress associated with aridity was positively related to and explained 6–56% of the variance in indicators of facilitation or competition. We also found that the relationship between competition and species richness, usually negatively affected by competition, was positively related to richness at low abiotic stress, and negatively related to richness at high abiotic stress.

Figure 4. With Cristina Escolar, Matthew Bowker, and Richard Bardgett during Richard´s visit to the Aranjuez Experimental Station.

A major highlight of my years at URJC was the setup of the Aranjuez Experimental Station, a beautiful research site located very close to the historic city of Aranjuez where we carried out an important part of our biocrust research over the years. Another highlight was the setup of a manipulative field experiment focused on the understanding of biocrusts as modulators of ecosystem responses to climate change in 2008, an experiment that is still running today (against all odds!). This experiment was set up thanks to the support (again!) of the BES, who awarded me a project to support the PhD of Cristina Escolar and that allowed setting up and maintaining this experiment for the first years. Cristina did a fantastic job during her PhD, was fundamental (together with all lab technicians that have worked over the years in this experiment, in particular Victoria Ochoa, Beatriz Gozalo, and Sergio Asensio) to make this experiment the success that it has been, and helped a lot to create a collaborative atmosphere, always with a smile on her face and ready to help her lab mates. More than 15 articles have been published from this ongoing experiment, which has also supported the PhDs of multiple students in the lab (in addition to Cristina, Ángela Lafuente and Concha Cano-Díaz, and Selina Baldauf conducted parts of their PhDs in this experiment), and I would like to highlight here two articles from this experiment that have been published in Journal of Ecology.

In the seventh article of this virtual issue (Delgado-Baquerizo et al. 2014), we evaluated how warming, rainfall exclusion, and biocrust cover affect soil N availability and its resistance to climate change. We found that warming and/or rainfall exclusion treatments enhanced N availability and promoted the dominance of inorganic over organic N four years after the beginning of the experiment, and that biocrusts promoted the resistance of soil N availability to simulated climate change. The results of this work indicate that biocrusts can play an important role slowing down the impacts of warming and rainfall reduction on the N cycle, highlighting its key role as regulators of ecosystem responses to climate change in drylands. This article was part of the PhD of Manuel Delgado-Baquerizo, an amazing scientist (and wonderful person!) who since the first days we started to interact surprised me with his working capacity, ability to generate new ideas, capacity to deal with complex problems, and challenge the existing status quo to move science forward. I have been incredibly fortunate to have had the chance of seeing his growth since his early days as a graduate student and to count him among my friends and long-term collaborators.

Figure 5. Our long-term climate change experiment at the Aranjuez Experimental Station (and the replicates of the experiment established in Sax and Sorbas) has been a major highlight of the work we have done over the years. Running it for 16 years has been possible thanks to the dedicated work of multiple lab students, postdoctoral researchers, technicians, and visiting scientists over the years (the list is too large to mention without risking missing anyone, so many thanks to everyone involved in this experiment!).

In the next article of this virtual issue (Baldauf et al. 2020) we used a mechanistic model to explore the long-term impacts of climate change in biocrust communities, to address the mechanisms underlying the observed decline in biocrust cover with warming in our experiment (Ladrón de Guevara et al. 2018). I always wanted to use models to do things such as those we did in this article, but was unable to do it because of my lack of expertise in the use of mechanistic models. This changed when we initiated a very enjoyable collaboration with the group of Prof. Britta Tietjen from Freie Universität Berlin and Selina Baldauf got excited about doing her PhD research with biocrusts. Selina did a fantastic job parameterizing from scratch a mechanistic model for the key biocrust species Diploschistes diacapsis, something that took a substantial amount of time and that was frustrating at times (particularly when everything seems to be right with the model, but it did not deliver trustable results). After lots of work to fine-tune the model, it reproduced observed experimental findings, and revealed that negative warming effects on lichen cover were largely caused by the associated decrease in relative humidity and non-rainfall water inputs, which are major water sources for biocrust-forming lichens. This study highlights the value of process-based modelling to disentangle the effects and interactions of major climate change drivers acting simultaneously and in isolation, something that it is difficult to do using field experiments alone, and the power of combining field experiments with modelling to be able to deliver long-term forecasts and to gain a more comprehensive understanding of the mechanisms behind experimental results. 

Contributing to the development of the field of biocrust ecology, to increase awareness about the ecological roles and importance of these key communities, and to inspire additional research both in Spain and beyond with these organisms has been without any doubt one of the highlights of my career so far. And publishing our biocrust research in Journal of Ecology has been fundamental for doing so. The articles highlighted in this post are also important for me because they showcase biocrusts as a great model system for studying multiple ecological questions of great interest and relevance within ecology and global change biology. They also illustrate how biocrusts can be used to test broad ecological theories, provide novel insights on heavily studied topics such as species coexistence, and show the potential and value of these organisms to set up complex experiments (it is very difficult to warm up a forest or to experimentally manipulate the spatial pattern and diversity of a shrubland, tasks that while not easy are doable with biocrusts!). And above all I have really enjoyed working with awesome organisms I love, interacting with fellow biocrust lovers (the collaborative atmosphere of the global biocrust research community is quite unique and enjoyable) and making a lot of friends and colleagues along the way. Working with small organisms can lead to large and amazing things!

Fernando T. Maestre, King Abdullah University of Science and Technology.

Literature cited

Baldauf, S., Porada, P., Raggio, J., Maestre, F. T., & Tietjen, B. (2021). Relative humidity predominantly determines long-term biocrust-forming lichen cover in drylands under climate change. Journal of Ecology, 109, 1370–1385.

Bowker, M. A., Soliveres, S., & Maestre, F. T. (2010). Competition increases with abiotic stress and regulates the diversity of biological soil crusts. Journal of Ecology, 98, 551–560.

Delgado-Baquerizo, M., Maestre, F. T., Escolar, C., Gallardo, A., Ochoa, V., Gozalo, B., & Prado-Comesaña, A. (2014). Direct and indirect impacts of climate change on microbial and biocrust communities alter the resistance of the N cycle in a semiarid grassland. Journal of Ecology, 102, 1592–1605.

Ladrón de Guevara, M., Gozalo, B., Raggio, J., Lafuente, A., Prieto, M., & Maestre, F. T. (2018). Warming reduces the cover, richness and evenness of lichen-dominated biocrusts but promotes moss growth: Insights from an 8 yr experiment. New Phytologist, 220, 811–823.

Maestre, F. T. (2003). Small-scale spatial patterns of two soil lichens in semi-arid Mediterranean steppe. The Lichenologist, 35, 71–81.

Maestre, F. T., Castillo-Monroy, A. P., Bowker, M. A., & Ochoa-Hueso, R. (2012). Species richness effects on ecosystem multifunctionality depend on evenness, composition and spatial pattern. Journal of Ecology, 100, 317–330.

Maestre, F. T., & Cortina, J. (2002). Spatial patterns of surface soil properties and vegetation in a Mediterranean semi-arid steppe. Plant and Soil, 241, 279–291.

Maestre, F. T., Escudero, A., Martinez, I., Guerrero, C., & Rubio, A. (2005). Does spatial pattern matter to ecosystem functioning? Insights from biological soil crusts. Functional Ecology, 19, 566–573.

Maestre, F. T., Huesca, M., Zaady, E., Bautista, S., & Cortina, J. (2002). Infiltration, penetration resistance and microphytic crust composition in contrasted microsites within a Mediterranean semi-arid steppe. Soil Biology and Biochemistry, 34, 895–898.

Weber, B., Belnap, J., Büdel, B., Antoninka, A. J., Barger, N. N., Chaudhary, V. B., Darrouzet-Nardi, A., Eldridge, D. J., Faist, A. M., Ferrenberg, S., Havrilla, C. A., Huber-Sannwald, E., Malam Issa, O., Maestre, F. T., Reed, S. C., Rodriguez-Caballero, E., Tucker, C., Young, K. E., Zhang, Y., … Bowker, M. A. (2022). What is a biocrust? A refined, contemporary definition for a broadening research community. Biological Reviews, 97, 1768–1785.



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