A missing key to our understanding of forest carbon dynamics. A commentary on: ‘High nitrogen resorption efficiency of forest mosses’

Cold-climate forests have a crucial role in the global carbon cycle as they currently act as an increasing carbon sink for global emissions of CO₂ (Ciais et al., 2019). In these forests, bryophytes often contribute a major part of the ‘non-tree’ living biomass. In a paper published in this issue of Annals of Botany, Liu et al. (2020) suggest that even though mosses account for only a minor proportion of the forest biomass and carbon uptake, they may have a decisive influence on ecosystem carbon and nitrogen dynamics.

Moss productivity in old-growth closed canopy forest has been estimated to be in the same range as for the field-layer vegetation, i.e. 0.2–0.8 Gt C ha⁻¹ year⁻¹ (Turetsky, 2003). The annual gross carbon uptake by mosses in a full-grown forest may thus equal ~3 % of that by the trees (Palmroth et al., 2019). However, in cold-climate forests plant growth is mainly limited by the supply of plant-available nitrogen, and ecosystem carbon sequestration is closely related to the internal turnover of nitrogen. Liu et al. in this issue corroborate previous research showing mosses’ high capacity to retain and internally turn over assimilated nitrogen, but in addition, and perhaps more surprisingly, they also demonstrate that mosses may leach a significant proportion of their nitrogen from their living tissues. Consequently, the work by Liu et al. highlights that in order to fully understand how the carbon sink in the world’s cold-climate forests will develop under climate change, we need to put more emphasis on elucidating how mosses influence the forests’ carbon and nitrogen assimilation and turnover.

In an elegant experiment in situ, Liu et al. demonstrate that two species of moss, Actinothuidium hookeri and Hylocomium splendens, resorbed between 50 and 60 % of the nitrogen from their senescing tissues and allocated it to new tissue growth. Together these mosses accounted for more than 60 % of the ground cover in a high-altitude coniferous forest of the Tibetan Plateau. The authors traced ¹⁵N-labelled nitrogen applied to the mosses over three consecutive years to enable the careful quantification of the mosses’ pools and fluxes of nitrogen. Similarly high, or even higher, nitrogen resorption from senescing tissues has been reported for mosses elsewhere in cold-climate forests, e.g. boreal forests. Generally, bryophytes are very efficient in both assimilating and reallocating nitrogen. Their high cation exchange and water-holding capacities lead to assimilation of nitrogen from associated nitrogen-fixing cyanobacteria, precipitation and forest canopy throughfall (e.g. Turetsky, 2003). The nitrogen made available to bryophytes by these pathways generally comes in very low concentrations, and under such circumstances nitrogen retention by bryophyte carpets can be close to 100 %. Due to bryophytes’ high nitrogen retention capacity and their efficient internal recycling, it is often assumed that nitrogen losses to soils underlying ground-dwelling bryophytes or to surrounding vegetation of epiphytic bryophytes are generally very minor.

Fluctuating weather conditions may, however, interfere with mosses’ high nitrogen retention efficiency. Mosses are poikilohydrous, which means that when their environment dries they desiccate until their cellular water content is in equilibrium with the surrounding air. Cellular integrity is often compromised during this process, and when re-wetted, damaged cell membranes will leach intracellular contents like carbohydrates, amino acids and ionic compounds. Hence, the interesting observation of Liu et al. that nitrogen leached from live moss tissue indicates that environmental fluctuations in their study system caused their two study species, A. hookeri and H. splendens, to lose as much as 23 and 33 %, respectively, of their live tissue nitrogen via leaching.

The result of Liu et al. suggesting nitrogen leaching from live bryophyte tissue in situ challenges the idea that mosses have the capacity to more or less monopolize nitrogen atmospherically deposited into an ecosystem, and that nitrogen is mainly released from moss tissues during litter decomposition. Although the physiological mechanisms underlying potential nitrogen leaching from live moss tissues have been well known for a long time, re-assimilation of leached nitrogen has been assumed to prevent that nitrogen being lost from living mosses. However, recently Slate et al. (2019) demonstrated in a laboratory experiment on eight moss species that desiccated–rehydrated mosses lost between 2 and 31 times more carbon in an experimental throughfall event than mosses that were continuously hydrated. In addition, all the desiccated–hydrated mosses lost some nitrogen, in contrast to the continuously hydrated ones, which lost none (Slate et al., 2019). Large interspecific variations occurred (Slate et al., 2019), which calls for similar studies in situ investigating the effects of site-specific environmental fluctuations on adherent moss species.

The moss species used in the study by Liu et al. are both so-called leafy mosses: H. splendens is ubiquitous in the circumboreal region, while A. hookeri is more specific for the high-altitude regions of eastern Asia. Both species represent the same ecosystem functions in cold-climate forests and this selection of study species contributes to the generalizability of the results. It is widely acknowledged that an improved understanding of the processes involved in organic carbon storage in forest soils is needed to appreciate the full potential of the terrestrial carbon sink (e.g. Ciais et al., 2019). The role of mosses in ecosystem carbon and nitrogen turnover has been targeted in many studies, but similarly careful quantifications of pools and fluxes like those done by Liu et al. are still rare. Andrieux et al. (2018) designates the dominance of mosses as an important driver of carbon accumulation in organic soil. These authors attribute to mosses a key role in forming a functional bridge between the climate and the soil’s carbon accumulation (Andrieux et al., 2018), i.e. mosses that thrive in forest understorey environments with a relatively stable, humid and cool climate contribute to slowing litter decomposition and the subsequent release of carbon and nitrogen. With the changing climate, the cold-climate forests may be subjected to more frequent extreme environmental fluctuations, e.g. longer and stronger heat waves in summer and prolonged periods of freeze–thaw cycles in autumn and winter. Hence, the role of mosses in forest ecosystems may change, as leaching of nitrogen and carbon compounds from living tissues may increasingly occur. Compounds leached from mosses during desiccation–rehydration and freeze–thaw events have the potential to affect soil carbon transformations (e.g. Slate et al., 2019), and may thus have direct effects on forests’ carbon accumulation. Further studies like the one by Liu et al. in this issue will be needed to enable a better understanding of the role mosses may play in forests’ carbon balance in a changing climate.