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👇
A journey back in time…
Finally, after much blogging about vascular plants, their traits and associated ecosystem processes, we are getting to the small and beautiful: bryophytes and lichens! Although there must have been thousands of ecological studies on cryptogams by now, they still undoubtedly represent only a tiny fraction of all plant ecology studies. I was lucky to be introduced to them already by some infectiously passionate lecturers (Rob Gradstein, Fred Daniëls) when I was still a master student. They even made me choose cryptogam themes for my thesis projects in spite of my strong passion for birds. It started with fieldwork in the Belgian Ardennes, where Gea Karssemeijer and I did a phytosociological study on the succession of cryptogam communities on decaying spruce tree stumps. I remember we used a sharp metal pin that we dropped from a certain height and recorded the penetration depth as a measure of decay stage. It worked really well to understand the succession of cryptogam communities as a consequence of wood decay. After some extra effort the thesis became my first international publication (Cornelissen & Karssemeijer 1987), but I am hesitant to share it with you as our academic and English writing was still rather – let’s say – underdeveloped.
Then, out of the blue one day, Hans ter Steege (total stranger then, long-term friend now) phoned me to ask whether I wanted to join him on an MSc project about the vertical distribution of rainforest epiphytes in Guyana, South America. He was interested in tropical orchids and bromeliads and he had heard that I was interested in mosses, liverworts and lichens. The plan was to climb big trees together and map the epiphytic vegetation, where Hans 1 would identify the vascular plants and Hans 2 the cryptogams. I had never considered tropical epiphytes before and never been on an airplane, but my attitude towards exciting adventures was, already then: say yes first, think about the problems afterwards. I could write three blogs just about this project, but will control myself. It was a great adventure and we did things I (and my university) would now never allow my own students to do. We used bow and arrow and speleo gear to climb up to 35 meters high into trees to map the epiphytic plant communities in the different vertical zones (Photos 1). We collected specimens for identification and deposition in the Utrecht University herbarium later and took measurements of relative light exposure, bark texture and other variables in the different height zones of the host trees. To reach the highest, narrow branches and twigs we sawed out a large branch at the base and lowered it down to the forest floor. I had gradually overcome my vertigo while practicing climbing techniques, but falling out of the first tree we sampled for real didn’t help with that. After a week with my foot up, I limped (in some pain) through the rainforest for months in order for us to complete our target set of trees. Back in The Netherlands it turned out that a piece of bone the size of a dice was still floating round in my foot and the surgeon took it out. Life experience doesn’t always come easily. Much time and sweat went into plant identification upon return – there were few keys available for some of the plant and lichen groups, so we often had to find actual specimens in the herbarium for comparison. But the reward was great, as we published two papers from this study that turned out to be picked up by other epiphyte enthusiasts; one of which was on the cryptogam communities (Cornelissen and ter Steege 1989). Thinking about it now, this study was perhaps my first encounter with plant traits and plant functional types, as we classified our mosses, liverworts and lichens according to growth form. There were some amazing ones amongst them, for instance leafy bryophytes like the liverwort Symbiezidium transversale, which grew horizontally on the bark of vertical trunks. Their stems had leaves on both sides, with the leaves pointing up being small and closely attached to the bark and the leaves on the opposite side being twice the size and stretching out horizontally. What great adaptation to intercept precious water along a vertical surface!
From equator to pole; cryptogams and climate warming
My activities on mosses, liverworts and lichens went into a prolonged state of dormancy through my PhD work in China and my postdoc years at UCPE in Sheffield, UK (see blogs 1 and 2). But when UCPE ceased to exist, I was lucky to move to a postdoc position in the Sheffield Centre for Arctic Ecology of Terry Callaghan (and John Lee, Malcolm Press) at Sheffield University. This move turned out to become a dream come true. As a student I had hiked in the arctic tundra of northern Sweden and seen Abisko Research Station in the distance. My friend and I had discussed how wonderful it would be to work as a biologist in a beautiful place like that, surrounded by snow-topped mountains, tundra and lakes. And now by some amazing turn of luck I found myself going to Abisko and Svalbard to study the responses of arctic vegetation to climate warming. This work was part of a larger EU project (BASIS) on climate impact scenarios of the Barents Region. The project had an important socio-economic dimension and so it was logical to put particular focus on lichens as the staple food for reindeer; and the Saami people in northern Scandia strongly depend on reindeer for their livelihood. So I decided to study how arctic lichens could respond to climate warming. The hypothesis was that indirect responses might be important, i.e. that in more vegetated tundra at lower latitude and altitude, warming-induced growth and expansion of vascular plants, especially shrubs, would reduce the growth of lichens via shading. In climatically very harsh regions, i.e. in the High Arctic (e.g. Svalbard) or high up in the mountains in the Subarctic, any expansion of vascular plants would still not be enough to outcompete the lichens. Since two years of postdoc position would not be enough to collect enough data in the field myself, I collected data from the literature or via contacting researchers directly for their datasets. By then, several studies had reported biomass or cover by vascular plants and lichens in field experiments with treatments mimicking climate warming (see below for an example) or warming-induced faster nutrient mineralization and availability. I also collected literature data from natural gradients where biomass or cover of vascular plants and lichens had both been recorded. The patterns turned out to be really consistent and to support the hypothesis: that lichens struggle where vascular plants become more abundant, for instance because of climate warming (Cornelissen et al. 2001, virtual issue). When, subsequently, more data became available from experimental field warming studies, this finding (warming-induced “shrubification” at the expense of lichens) was confirmed more robustly across the cold parts of the globe (Elmendorf et al. 2012; Lang et al. 2012).
When I moved to my current place, at Vrije Universiteit Amsterdam, back in 2000, I continued both the arctic research line and pursued my interest in traits as well as in cryptogams. And these three came together there. With (then) PhD students Ellen Dorrepaal, Simone Lang, Frida Keuper and Eva Krab, and postdocs Nadia Soudzilovskaia, Tanya Elumeeva and Pascale Michel, we worked both on the climate responses and functional trait ecology of cryptogams; and the linkages between them. Rien Aerts, Ellen Dorrepaal, Richard van Logtestijn and I, in collaboration with Abisko Research Station, set up a field warming experiment in a Sphagnum peat bog in Abisko, N Sweden. This work was not only to look at Sphagnum responses to climate warming but also to contribute to knowledge of climate responses to Sphagnum, because much of the world’s organic carbon is currently (still…) locked up in Sphagnum peatlands worldwide. But how to keep this carbon locked up in the face of melting permafrost and other threats? Using the then already established “open top chambers” (OTC), we went for a factorial design that would disentangle the separate and combined warming effects on ecosystem functions and biodiversity in winter, spring and summer (Photos 2). Because our site was exposed and windy, the OTCs (which were moved on and off between seasons depending on the treatment) not only raised the air temperature in spring and summer, but also “warmed” the soil in winter by trapping the snow that blew in over the OTC sides, thereby insulating the soil from the cold winter air. I have always loved working in this experiment, both because of the science and the fantastic scenery, with views over the big glacial lake Torneträsk and mountains all around and Red-throated Divers calling loudly on their frequent foraging flights to connect mountains and lake. We found that the dominant peatmoss, Sphagnum fuscum, did what ecosystem engineers are supposed to do: orchestrate the entire ecosystem. We measured it growing faster and producing more new biomass in response to experimental warming. Thereby it “bogged down” the vascular plants, which had a hard time climbing up towards the light again (Dorrepaal et al. 2006; Keuper et al. 2011). At the same time, Sphagnum provided suitable habitat to a community of several tiny special liverworts (Lang et al. 2009a in this journal). This special role of Sphagnum peatmosses in driving both vascular and cryptogam communities also came out strongly when Simone Lang studied them not only in warming experiments but also across large natural climatic gradients in northern Sweden and Norway; (Lang et al. 2009a; see Photo 3).
Cryptogam traits and ecosystem functions
Parallel to this global change work we started to measure bryophytes and lichens for functional traits that we thought might underpin their important roles in biogeochemical cycling (Cornelissen et al. 2007). These studies often involved collecting monospecific turfs of wide-ranging species, measuring some of their morphological or chemical traits and subjecting them to experimental tests. These test quantified, for instance, species differences and species interactions with regard to their water economy and thereby in ecosystem water retention capacity (Elumeeva et al. 2011; Michel et al. 2012 in this journal); their capacity (or not…) to acidify their environment via their organic acids (Soudzilovskaia et al. 2010; see Photo 4); to modulate the germination of vascular plants (Soudzilovskaia et al. 2011); to insulate soil temperatures and thereby freeze-thaw cycles (Soudzilovskaia et al. 2013); and to host nitrogen fixing cyanobacteria, thereby helping to bring new nitrogen into rather infertile tundra (Gavazov et al. 2010). All of these examples relate to the important roles of cryptogam species composition in the functioning of arctic ecosystems.
Currently we (with Stef Bokhorst, Pete Convey, Seringe Huisman, Emma Ciric, Ingeborg Klarenberg) are extending this research line to the Antarctic, where we study, for instance, the role of different lichen species in rock weathering (by exuding organic acids) and the role of different moss and lichen species and their traits in carbon capture via photosynthesis (Photo 5) and in their host function to invertebrate communities (e.g. mites, springtails and tardigrades). Among all those polar studies, the one I want to highlight as having been the most fun is the experiment in which we literally “turned peatlands upside down”. With (then) PhD student Eva Krab we studied the vertical stratification of different springtail (Collembola) species in arctic peat bogs and especially to find out whether they basically had a favourite depth along the gradient of temperature and moisture from the surface to deeper layers, whether they went for a certain Sphagnum quality (“traits”) from fresh on top to partly decomposed deeper down; or both (Krab et al. 2010; photos 6). It was a wild idea that started as a joke: “let’s turn peat cores upside down”. That’s exactly what we did: drilling out deep peat cores and putting half back as they were and the other half upside down in the hole they came from. We also some disturbance controls without any action. What started as a joke revealed some amazing patterns also relating to the traits of the springtails. We identified “movers” as species that were sensitive to the abiotic gradient from top to bottom and had to move back to where they came from. Pigmented species with eyes, adapted to life close to the light at the surface, moved back up while white, blind species moved back down when confronted with conditions close to the surface. Other species qualified as “stayers”; they were happy where they ended up in the upside-down core as long as they still had the same quality of peat to live in and feed on. I have found out that this fun experimental design has since also been adopted in ecological experiments in other parts of Europe. Having fun is an important ingredient of doing novel science. 😊
Like for vascular plants, we have been intrigued not only by cryptogam functions during their lifetime, but also in their afterlife. As announced in the previous blog, (then) PhD student Simone Lang studied one of the key processes during the transition from green leaves to litter: nutrient resorption into other plant parts by way of recycling these precious resources. We asked the question how efficient different evolutionary groups on the Tree of Life were at resorbing their nitrogen and phosphorus. Answering this question took us to the subarctic tundra of North Sweden, where we collected both fresh tissues and litter of wide-ranging species of vascular plant, bryophyte and lichen. It was a particular challenge to collect senesced tissues of bryophytes and lichens, as it was often hard to distinguish between living and dead tissues. What wasn’t known in the literature was that bryophytes and lichens do actually resorb nutrients during senescence, even though they lack vascular tissues to aid them with that. Mosses and lichens had low, liverworts intermediate and, as expected, vascular plants intermediate to high resorption efficiency (Lang et al. 2014). But this was only a first shot at cryptogam nutrient resorption; much work needs to be done in other biomes to test for the robustness of the evolutionary patterns found. And the same can be said about comparing the decomposability of different cryptogams. Here we adopted the “common garden” litter-bed approach (see first blog) but with adjustments for hosting cryptogam litter in a relevant environment. As for the resorption work, one of the main challenges was to find or “create” actual litter, as mosses and lichens are good at many things but not good at dying a natural death. Anyway, we found enormous variation between evolutionary groups, for instance liverworts and mosses being generally slow to decompose compared to vascular plant litter with Sphagnum species always coming out as the slowest of all (Lang et al. 2009b, virtual issue; Dorrepaal et al. 2005 in this journal). But there were also huge differences in decomposition rate among species within mosses, within liverworts and within lichens (Lang et al. 2009b, virtual issue). As for vascular plants, such findings have important implications for the formation and maintenance of large-scale carbon stocks as dependent on vegetation composition. Much work to be done on this not only in tundra but also in other biomes in the world.
I’d like to finish this blog by saying that cryptogams, being the little ones, have not been seen as inferior to vascular plants everywhere in the world. I have very fond memories of the fantastic “moss gardens” around old temples in Japan (Photo 7). Fortunately, these fantastic and important creatures do sometimes get the love and attention they so much deserve.
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:
Cornelissen, J.H.C. & Karssemeijer, G.J. (1987). Bryophyte vegetation on spruce stumps in the Hautes-Fagnes, Belgium, with special reference to wood decay. Phytocoenologia, 15, 485-504.
Cornelissen, J.H.C. & ter Steege, H. (1989) Distribution and ecology of epiphytic bryophytes and lichens in dry evergreen forest of Guyana. Journal of Tropical Ecology, 5, 131-150.
Cornelissen, J.H.C., Lang, S.I., Soudzilovskaia, N.A. & During, H.J. (2007) Comparative cryptogam ecology: a review of bryophyte and lichen traits that drive biogeochemistry. Annals of Botany, 99, 987-1001.
Dorrepaal, E., Cornelissen, J.H.C., Aerts, Wallén, B. & van Logtestijn, R.S.P. (2005) Are growth forms consistent predictors of leaf litter quality and decomposability across peatlands along a latitudinal gradient? Journal of Ecology, 93, 817-828.
Dorrepaal, E., Cornelissen, J.H.C., Aerts, R. & van Logtestijn, R.S.P. (2006) Sphagnum modifies climate change impacts on sub-arctic vascular bog plants. Functional Ecology, 20, 31-41.
Elmendorf, S.C., Henry, G.H.R., Hollister, R.D., Björk, R.G., Bjorkman, A.J. et al. (2012) Global assessment of experimental climate warming on tundra vegetation: Heterogeneity over space and time. Ecology Letters, 15, 164-175.
Elumeeva E.G., Soudzilovskaia, N.A., During, H.J. & Cornelissen, J.H.C. (2011) The importance of shoot adaptation versus aggregation for the water balance of subarctic bryophytes. Journal of Vegetation Science, 122, 152-164.
Gavazov, K.S., Soudzilovskaia, N.A., van Logtestijn, R.S.P., Braster, M. & Cornelissen, J.H.C. (2010) Isotopic analysis of cyanobacterial nitrogen fixation associated with subarctic lichen and bryophyte species. Plant and Soil, 3331-2, 507-517.
Keuper F., Dorrepaal, E., van Bodegom, P.M., Aerts, R., van Logtestijn, R.S.P., Callaghan, T.V. & Cornelissen, J.H.C. (2011) A Race for Space? How Sphagnum fuscum stabilizes vegetation composition during long-term climate manipulations. Global Change Biology, 17, 2162-2171.
Krab, E.J., H. Oorsprong, M.P. Berg & J.H.C. Cornelissen 2010. Turning northern peatlands upside-down: disentangling microclimate and substrate quality effects on vertical distribution of Collembola. Functional Ecology 24: 1362–1369.
Lang S.I., Cornelissen, J.H.C., Hölzer, A., ter Braak, C.J.F., Ahrens, M. et al. (2009) Determinants of cryptogam composition and diversity in Sphagnum-dominated peatlands: the importance of temporal, spatial and functional scales. Journal of Ecology, 97, 299-310.
Lang S.I., Cornelissen J.H.C., Shaver G.R., Ahrens M., Callaghan, T.V. et al. (2012) Arctic warming on two continents has consistent negative effects on lichen diversity and mixed effects on bryophyte diversity. Global Change Biology, 18, 1096–1107.
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.
Michel, P., Lee, W.G., During, H.J. & Cornelissen, J.H.C. (2012) Species traits and their non-additive interactions control the water economy of bryophyte cushions. Journal of Ecology, 100, 222-231.
Soudzilovskaia, N.A., van Bodegom, P.M. & Cornelissen, J.H.C. 2013.Dominant bryophyte control over high-latitude soil temperature fluctuations predicted by heat transfer traits, field moisture regime and laws of thermal insulation. Functional Ecology, 27, 1442-1454.
Soudzilovskaia, N.A., Braae, B., Douma, J., Grau, O., Milbau, A. et al. (2011) How do bryophytes govern generative recruitment of vascular plants? New Phytologist, 190, 1019-1031.
Soudzilovskaia N.A., Cornelissen, J.H.C., During, H.J., van Logtestijn, R.S.P., Lang, S.I. & R. Aerts (2010) Similar cation exchange capacities among bryophytespecies refute a presumed mechanism of peatland acidification. Ecology, 91, 2716-2726.