🏆Eminent Ecologist 2022: Hans Cornelissen (part 2)

The Journal of Ecology Editors are delighted to honour Hans Cornelissen as our Eminent Ecologist award winner for 2022!

In recognition of his work, we asked Hans to put together a virtual issue of some of his favourite contributions to the journal. Hans has also written this blog series related to the virtual issue, linking the main research themes throughout his career, and including highlights and anecdotes from his student years to his current life as a professor of ecology. Han’s full blog series can be found here: Part 1 | Part 2👇 | Part 3

In my first blog related to the virtual issue showcasing a selection of my papers in Journal of Ecology, I got so carried away while writing that I had to press the pause button to keep you, reader, on board. In part 1, I wrote about (1) the comparative (trait) ecology of living plants, and (2) the extension to fates and (decomposition) rates in the afterlife of these plants and their parts. I hope you are feeling refreshed after this pause to read about two related topics that have been close to my heart for quite some time: (3) Trait evolution and carbon and nutrient cycling; and in my next blog (4) Cryptogam ecology.

(3) TRAIT EVOLUTION AND CARBON AND NUTRIENT CYCLING

In my oldest papers in this journal (Cornelissen 1996; Cornelissen et al. 1996, both in the virtual issue) I mentioned taxonomic relatedness analysis (or “phylogenetic correction”), which became very popular in the 1990-ies (see blogs by Mark Westoby and Michelle Leishman in this journal). Initially several colleagues and I at UCPE in Sheffield (see blog part 1) saw it as a negative thing that we had to demonstrate, through phylogenetic analyses, that the patterns in traits and processes among species that we wanted to publish were also valid beyond the specific flora we focused on. For instance, could we prove that the patterns were not driven by very specific evolutionary groups that might not occur in certain other floras?  We joked about the “phylogenetic thought police” making our lives difficult and rejecting our papers. But in hindsight they did me a great favour; while doing these analyses, I actually found that there was much added value from putting our findings in an evolutionary context. I began to see, for instance, that certain contrasts in trait values or trait relationships can be traced back to very early evolutionary divergences, as shown convincingly by a team of evolution-minded trait enthusiasts with Will Cornwell and Amy Zanne as driving forces. I can recommend their work on “functional distinctiveness of major plant lineages” whole-heartedly (Cornwell et al. 2014 in this journal). For instance, the generally slow decomposition rates of gymnosperms (“conifers”) compared to angiosperms (flowering plants) (Cornwell et al. 2008; Pietsch et al. 2014)  seem to be traceable to a very early trait divergence in the Mesozoic (Scheffer & Berendse 2009). In contrast, great trait divergence can also be seen at the tips of the phylogenetic tree, for instance at the level of species within genera  (e.g. Donovan et al. 2014 in this journal for sunflowers, Helianthus). Across 48 species of the same genus,  Artemisia, Xuejun Yang and colleagues (at the Institute of Botany in Beijing) found that even very plastic traits such as tissue carbon, nitrogen and phosphorus content, and their stoichiometry (ratios of C:N:P) also have a strong species-specific, i.e. genetic component, which is evident across major soil and climate gradients across China  (Yang et al. 2015, virtual issue). With the same group of young scientists (headed by Zhenying Huang) we found similar evolutionary patterns for biomass allocation among leaves, stems and roots, i.e. species-specific allocation across the genus Artemisia  in spite of major variation in soil and climate (Liu et al. 2021 in this journal).

Evolution and decomposition

Actually, the “functional distinctiveness” paper and Lisa Donovan’s sunflower paper were contributions to a BES-supported symposium at the ESA in Montreal (2013) and subsequently a special issue of Journal of Ecology, which Will and I organized fueled by enthusiasm for the “Tree of Life of biogeochemical cycling” (Cornelissen & Cornwell 2014).  Another contribution was driven forward by young scientist friends including, again, Guofang Liu, Xu Pan and Xuehua Ye  (supervised by Kunfang Cao, Ming Dong, Zhenying Huang, Will Cornwell and myself). This study took us  back to the end of the Cretaceous era, i.e. around the time of the enormous meteorite impact that likely wiped out the dinosaurs. This event seemed to have somehow facilitated the switch from domination of the Earth’s vegetation by gymnosperms and “basal“ angiosperms such as Magnoliids to the modern angiosperms, which benefitted from some major evolutionary innovations, e.g. in reproductive traits and in leaf vein architecture (and associated water and sugar transport). We asked the question whether the evolutionary changes in leaf anatomy had had, and are still having, consequences for the decomposability of the leaves. We hypothesized that the more resource-efficient, “cheaper” leaves of modern angiosperms (including eudicots) would turn into litter that would break down faster in the soil litter layer than the litter of basal angiosperms. As mentioned for another study in blog part 1 (Liu et al. 2015, virtual issue), we took advantage of the tropical botanical garden of Xishuangbanna in S. China (photo 1a), which had a great and well labelled collection of wide-ranging basal and modern angiosperms (photo 1b). It’s so nice to collect litter without having to worry about which species each leaf belongs to. Also here, we used the “common garden” litterbed approach, i.e. the same semi-natural litter environment to compare the decomposability of multiple species (in litterbags) simultaneously (photo 1c). Indeed, as hypothesized, we found that basal angiosperms generally decomposed more slowly than modern angiosperms, even when comparing only trees with trees (Liu et al. 2014, virtual issue). These findings help us to reconstruct the role of forest composition in biogeochemical cycling both in the past and in the present. Partly the same team, with key contributions by young scientists Xu Pan and Weiwei Zhao (who later became my PhD student), we looked at what type of evolutionary model leaf litter decomposability has followed over very long time scales. Based on a litterbed experiment in Beijing, with litterbag samples of wide-ranging Chinese species, we showed that litter decomposability follows the “Ornstein-Uhlenbeck model”, meaning that trade-offs in the underlying resource economics traits have strongly constrained the divergence of decomposability through time as compared with a “Brownian model” without such constraints (Pan et al. 2014). Very recently, we put litter decomposition in an evolutionary context by looking at the various ways by which co-evolution has left a legacy for decomposition (Cornelissen et al. 2022). The six of us had a lot of fun in the process leading up to this paper, brainstorming about all these different ways, from the plant-herbivore arms race, root mutualisms (mycorrhiza, N-fixing), various types of co-evolution between invertebrates and fungi (e.g. termites cultivating decomposing fungi in their mounds) and the more recent co-evolution of plants and people through agriculture (Cornwell & Cornelissen 2013; García-Palacios et al. 2013; Milla et al. 2018). Wonderful to think about evolutionary feedbacks of plants traits and human traits (e.g. our brain power) through agriculture, and how these feedbacks have affected the decomposition rates of crop plants as compared to their wild relatives.

Photos 1: Experiment testing for differences in leaf litter decomposition rates between “primitive” (basal) and modern flowering plants. (a) Xishuangbanna Tropical Botanical Garden, S China, where the litter was collected and incubated; (b) leaf litter collections before going into litterbags; (c) litterbed in which litterbags of all species were laid out simultaneously below the surface for comparing litter mass losses

Different angles and offshoots

Photo 2: The silicon content of grasses is linked to resistance against chronic wind stress across China. The picture shows an old field during secondary forest succession on Mt. Jinyun in SW China. In the foreground the widespread grass Cylindrica imperata and in the background a bamboo, i.e. a woody grass.

The discussions and papers leading towards and arising from the special issue, and discussions around it, have directly and indirectly got me involved in several exciting off-shoots and lateral extensions about evolution, traits and biogeochemical cycling. For instance, with Yaobin Song and other bright young scientists under the wings of Ming Dong at Hangzhou Normal University, we investigated silicon concentrations of leaf tissues of many evolutionary groups, collecting leaves of almost 300 vascular plant species from 27 sites all over China. The main focus of this work was on testing our hypothesis that silicium oxide  (“sand”) might be involved in mechanically protecting leaf tissues from chronic wind stress. One aspect of this was the strong phylogenetic signal along the Tree of Life of leaf Si (Song et al. 2020). For instance, horsetails have extremely high concentrations and one species (scouring horsetail, Equisetum hyemale) has been used traditionally as “sandpaper”, for instance to sand ships before painting them in the Netherlands. Also monocot families like grasses (Poaceae; see photo 2) and sedges (Cyperaceae) tend to be Si “accumulators”, i.e. they take it up more silicon than strictly needed for physiological functions. Based on our findings, we argue it’s no coincidence that, within these two families, species with higher leaf Si concentrations occur in relatively windy sites throughout China (Song et al. 2020). We found that even within grass species, like common reed (Phragmites australis), populations from windier sites had higher Si concentrations. It would be great to see new studies that test more directly, i.e. experimentally (in wind tunnels?), whether “sand-proofing” leaves against wind damage can develop (genetically or phenotypically) on short time scales besides long evolutionary scales as seen among higher plant taxa…. and to what extent the wind protection and much debated anti-herbivore defence functions of silicon in leaves (Strömberg et al. 2016) are evolutionarily linked; and whether one is a useful evolutionary consequence of the other.

Also in other environmental and trait contexts we find that zooming in on phylogenetic relations can be very revealing to understand how adaptive plant traits are linked to environmental variation in stress. An example is clonality (vegetative expansion, e.g. belowground via rhizomes, aboveground via stolons). In a study of clonal behaviour across taxa all over China, we found that clear linkages between the degree of clonality and climatic stress existed within many of the plant taxa involved, while these relationships disappeared when all taxa were pooled (Ye et al. 2016). In a conceptual paper, we showed how, in general, phylogenetic relationships might help us to predict changes in ecosystem functions and services, via plant traits, from changes in species composition (Diaz et al. 2013).

Evolution and other aspects of carbon cycling

Let’s go back to carbon cycling again, which has been so tightly linked to the climate from past to present. This important cycle is determined by plant photosynthesis and growth on one side (C gain) and carbon losses on the other side, mostly through decomposition (see above) and…. fire!  Understanding how different plant species contribute to these gains and losses is important for predicting the consequences of changing vegetation composition for the carbon budget of different ecosystems; from the past into the future. On the carbon uptake and growth side, there have been many studies about how different plants respond to the increasing CO2 concentration in the atmosphere since the Industrial Revolution, mainly as a consequence of our life style. However, in the past, for instance during the Ice Ages, there were long periods with very low CO2 concentrations, down to less than half of what plants experience now. Andries Temme (then PhD student) and long-term research friend Jinchun Liu, together with Will Cornwell, Rien Aerts and I, wondered what type of plants might have adapted relatively strongly to growth in a very low CO2 atmosphere, and whether such evolutionary responses might have made them less pre-adapted to growth at high CO2 of the future. We were lucky to be allowed to use the walk-in climate chambers at Utrecht University, not far from our place, where CO2 concentrations of the air could be set at around 160-180 ppm (carbon starvation representative of glacial periods), at ambient (roughly present-day) CO2 (400-450 ppm) and at “future” very high CO2 (750 ppm). Andries and Jinchun grew wide-ranging species in these chambers and measured their ecophysiological and morphological traits and relative growth rates. Working with the plants was quite a challenge, as breathing out into a low CO2 chamber would raise the CO2 level to ambient levels very quickly. The solution was to wear a face mask allowing us to breathe into a big plastic bin liner, which had to be emptied outside the chamber once full. The pictures from this work could invite intriguing response on social media if taken out of context (see photos 3) 😊. This work showed how plants make thinner (“carbon-cheaper”) leaves when carbon-starved like in the Ice Ages; and of course how they cannot grow as fast as they do at ambient or future high CO2. Moreover, when faced with both low CO2 and low water availability, as must have been common in some periods during the Ice Ages, the plants struggled even more to maintain a positive carbon balance for growth. In other words: they were very “hungry and thirsty” (Temme et al. 2019). We also found that fast growing species suffered more from low CO2 than slow growers. Even so, they still remained fast growers compared to slow growing species. So the winners seem to have always been winners in spite of finding the Ice Ages rather stressful (Temme et al. 2015).

Photos 3: Experimental study on plant species’ responses to past low, present intermediate and (predicted) future high CO2. (a) Jinchun Liu breathing into a plastic bag to prevent the CO2 concentration from increasing during work in a low-CO2 chamber at Utrecht University. (b) Plants of Hemisteptia lyrata grown at high (left) , ambient (middle) and low CO2 (right).
Photos 4: Experimental burn in the fire lab, FLARE at Vrije Universiteit Amsterdam. (a) pine litter fuel bed being weighed and prepared for (b) an experimental burn.

The low CO2 work took us quite some time back into the past, but this was a brief blip when compared to the evolution of conifers (gymnosperms), which already dominated the Earth’s vegetation when big dinosaurs still marched around – and tried to eat their foliated branches. Many conifers, for instance pines, tend to live in places where wildfire is an important process for the ecosystem and for releasing carbon back to the atmosphere as CO2. In turn, wildfires depend on the quantity and quality of the plant material. For instance, conifer species differ in the traits of their leaves and foliated twigs and, thereby, in the traits of the litter they drop onto the forest floor. Based on previous literature and observations, we hypothesized that the size and shape of the litter (“size and shape spectrum”, see blog part 1) would determine the flammability of the litter layer, where larger leaves with complex shape would create less dense, airy “fuel beds”, with plenty oxygen flowing through for the wildfire to spread. So we compared the flammability of many species across the Tree of Life as driven by their leaf size and shape in order to learn about their potential role in litter layer (and ecosystem) flammability, from now all the way back to the Jurassic with its predominant araucarias, cycad palms and ginkgos. How to test such a hypothesis? Well, one important aspect was to collect fresh (undecomposed) litter from many different evolutionary groups of conifers. Here, again, we made good use of different botanical gardens and, since we did this work in the temperate Netherlands, in tropical greenhouses. To test for difference in flammability, we did (and still do) experimental burns in the Fire Laboratory Amsterdam for Research in Ecology (FLARE). This is a big name for what is simply a fire-proof converted fume-hood in a lab where climatic conditions and air-flow can be controlled (photos 4). Here we fill a steel mesh basket with a standard volume of litter and set fire to it and then measure different things that tell us about flammability of the litter, e.g. rate of fire spread, temperatures above the litter and percentage of litter mass loss. For the conifer project, with Will Cornwell, Weiwei Zhao and Richard van Logtestijn, we could confirm that large, more shaped litter particles gave more flammable litter layers, as in several other studies (e.g. Schwilk and Caprio 2011 in this journal; Grootemaat et al. 2017). Interestingly, in our study this pattern was mostly due to one evolutionary group of conifers. While litter layers of most conifers burned really well, we saw within the pine family (Pinaceae) that pines (Pinus) themselves burned well, because the long needles in pairs or threesomes stacked very loosely, giving very well ventilated litter layers. In contrast, Pinaceae genera which dropped individual small needles, like larch (Larix), spruce (Picea) and fir (Abies, Pseudotsuga), produced very dense litter layers, with poor oxygen supply, in which the fire never got going or extinguished rapidly (Cornwell et al. 2015; Zhao et al. 2016). We can use these findings to study the role of different conifer groups in fire regimes not only in the present, but also “back-predict” their role in fire regimes and carbon cycling in the distant past. It’s fun to think of giant sauropods in the Jurassic using their long necks to access the foliage of some tall conifer trees in an araucaria forest, but ending up using their big feet to extinguish a fire starting in the litter layer…

What’s next?

By now I despair of myself for again using up more journal blog space than intended when I started. As for the first blog, I feel that I should pause here for now. In part 3, I will finally talk about my passion for the ecology of mosses, liverworts and lichens, the little ones that often get forgotten by plant ecologists but are super important for several ecosystem functions and services. This will also be the link to a lot of work we do especially in polar regions up north and down south, where these cryptogams are particularly important, and how they relate to climate warming. I will also provide a link back to evolution, by telling about how good or bad mosses, liverworts and lichens are at recycling their nutrients (Lang et al. 2014). But now, just for fun, I’d like to finish part 2 by sharing two pictures, both from tropical forest areas, about a further relationship between evolution and litter (photos 5). They show how some animals can hide from their predators by pretending to be leaf litter. See you again for part 3!

Photos 5: Evolution and litter: animals pretending to be leaf litter (mimicry). (a) butterflies in the collection in the museum at Xishuangbanna Tropical Botanical Garden, China; (b) frog in the tropical rain forest in Saba, Borneo (during fieldwork with the British SAFE project about ecological consequences of forest fragmentation).

Hans was interviewed by Executive Editor Richard Bardgett, about his motivations and career to date, how he sees the field of functional traits developing in the future, and what advice he’d give to ECRs interested in plant ecology:

References

Berendse, F. & Scheffer, M. (2009) The angiosperm radiation revisited, an ecological explanation for Darwin’s ‘abominable mystery’. Journal of Ecology, 12, 865–872.

Cornelissen, J.H.C., Cornwell, W.K. (2014). The Tree of Life in ecosystems: evolution of plant effects on carbon and nutrient cycling. Journal of Ecology, 102, 269-274. 

Cornelissen, J.H.C., Cornwell, W.K., Freschet, G.T., Weedon, J.T., Berg, M.P. & Zanne, A.E. (2022) Co-evolutionary legacies on plant decomposition. Trends in Ecology and Evolution, doi: 10.1016/j.tree.2022.07.008.

Cornwell, W.K. & Cornelissen, J.H.C. (2013) A broader perspective on plant domestication and nutrient and carbon cycling. New Phytologist, 198, 331-333.

Cornwell, W.K., Westoby, M., Falster, D.S., FitzJohn, R.G., O’Meara, B.C., et al. (2014) Functional distinctiveness of major plant lineages. Journal of Ecology 102 , 345-356.

Cornwell, W.K., Elvira, A., van Kempen, L., van Logtestijn, R.S.P., Aptroot, A. & Cornelissen, J.H.C. (2015) Flammability across the gymnosperm phylogeny: the importance of litter particle size. New Phytologist, 206, 672-681.

Diaz, S., A. Purvis, A., Cornelissen, J.H.C., Mace, G.M.,  Donoghue, M.J. et al. (2013) Functional traits, the phylogeny of function, and ecosystem service vulnerability. Ecology and Evolution, 3, 2958-2975.

Donovan, L.A., Mason, C.M., Bowsher, A.W., Goolsby, E.W. & Isibashi, C.D.A. (2014) Ecological and evolutionary lability of plant traits affecting carbon and nutrient cycling. Journal of Ecology, 102, 302–314.

García-Palacios, P., Milla, R., Delgado-Baquerizo, M., Martín-Robles, N., Alvaro-Sánchez, M. & Wall, D.H. (2013) Side-effects of plant domestication: ecosystem impacts of changes in litter quality. New Phytologist, 198, 504–513.

Grootemaat, S., Wright, I.J., van Bodegom, P.M. & Cornelissen, J.H.C. (2017) Scaling up flammability from individual leaves to fuel beds. Oikos, 126, 1428-1438.

Lang, S.I., Aerts, R.,  van Logtestijn, R.S.P., Schweikert, W., Klahn, T. et al. (2014)Mapping nutrient resorption efficiencies of subarctic cryptogams and seed plants onto the Tree of Life. Ecology and Evolution, 4, 2217-2227.

Liu, R., Yang, X.J., Gao, R.R., Hou, X.J., L.P. Huo, L.P. et al. (2021). Allometry rather than abiotic drivers explains biomass allocation among leaves, stems and roots of Artemisia across a large environmental gradient in China. Journal of Ecology, 109, 2026-1040.

Milla, R., Bastida, J.M., Turcotte, M.M.,  Jones, G., Violle, C. et al. (2018) Phylogenetic patterns and phenotypic profiles of the species of plants and mammals farmed for food. Nature Ecology and Evolution 11, 1808-1817.

Pan, X., Cornelissen, J.H.C., Zhao, W.W., Liu, G.F., Hu, Y.K. et al. (2014) Experimental evidence that the Ornstein-Uhlenbeck model best describes the evolution of leaf litter decomposability. Ecology and Evolution, 4, 3339-3349.

Schwilk, D.W. & Caprio, A.C. (2011) Scaling from leaf traits to fire behaviour: community composition predicts fire severity in a temperate forest. Journal of Ecology, 99, 970–980.

Song, Y.B., Hu, Y.K., Pan, X., Liu, G.F.,  Xiong, W., Dong, M.& Cornelissen, J.H.C. (2020). Association of leaf silicon content with chronic wind exposure across and within herbaceous plant species. Global Ecology and Biogeography,  29, ‏711-721.

Strömberg, C.A.E., Di Stilio, V.S. & Song, Z. (2016). Functions of phytoliths in vascular plants: An evolutionary perspective. Functional Ecology, 30, 1286–1297.

Temme, A.A., Liu, J.C., Cornwell, W.K., Cornelissen, J.H.C. & Aerts, R. (2015) Winners always win: growth of a wide range of plant species from low to future high CO2. Ecology and Evolution, 5, 4949-4961.

Temme, A.A., Liu, J.C., Cornwell, W.K., Aerts, R. & Cornelissen, J.H.C. (2019) Hungry and thirsty: Effects of CO2 and limited water availability on plant performance. Flora, 254, 188-193.

Ye, D., Liu, G.F., Song, Y.B., Cornwell, W.K., Dong, M. & Cornelissen, J.H.C. (2016) Strong but diverging clonality – climate relationships of different plant clades explain weak overall pattern across China. Scientific Reports, 6, article 26850.

Zhao, WW, Cornwell, W.K., van Pomeren, M., R.S.P. van Logtestijn, R.S.P. & Cornelissen, J.H.C. (2016) Species mixture effects on flammability across plant phylogeny: the importance of litter particle size and the special role for non-Pinus Pinaceae. Ecology and Evolution,6, 8223-8234.

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