What is the speed of link between aboveground and belowground processes?
Carbon (C) sequestration in terrestrial ecosystems partially counteracts anthropogenic CO2 emission and thus mitigates global climate change and its effects on the environment and on human societies (IPCC, 2007). Carbon stored in the biomass of vegetation and in the organic matter of soils contributes to the sequestration potential of terrestrial biomes. These plant and soil pools vary in their absolute and relative contributions, depending on climate zone, vegetation type and management (e.g. Malhi et al., 1999). Therefore, a core research objective of ecosystem science is to understand the controls of C flow between plant and soil pools, that is, the coupling between aboveground and belowground systems.
Vegetation is increasingly viewed as the central driver of ecosystem C dynamics (Högberg & Read, 2006) and is important for the C-sequestration potential of terrestrial ecosystems (Trumbore, 2006). From a long-term perspective, the role of vegetation is evident because aboveground and belowground litter from vegetation is the original source of soil organic matter (SOM), thus contributing to C accumulation in soil. However, vegetation also determines short-term biogeochemical processes belowground. For example, recent photo-assimilates transported belowground can contribute > 60% of the C in soil respiration (Bhupinderpal-Singh et al., 2003; Taneva et al., 2006) and labile plant-derived C strongly affects SOM formation and turnover via soil priming (Kuzyakov et al., 2000; Sulzman et al., 2005). The fate of recent assimilates is therefore the subject of many recent and ongoing studies because their fate is key in describing the degree to which plant-assimilatory and soil-respiratory processes are coupled.
The role of the phloem
The recent assimilates that feed root respiration and are transferred from the roots to the rhizosphere are transported basipetally via the phloem (Carbone et al., 2007; Gessler et al., 2007; Högberg et al., 2008). Currently, C flow through the phloem is a major point of uncertainty in deciphering the patterns of plant–soil C coupling and identifying the underlying physiological mechanisms. However, the phloem is notoriously difficult to study in situ and this is why the paper of Mencuccini & Hölttä (2010) is important. They advance towards a mechanistic understanding of phloem as a ‘bottleneck’ to C flow belowground by providing evidence that specific phloem properties (path length, specific conductivity and turgor pressure differences) and transport velocities are crucial in explaining the linkage between canopy photosynthesis and soil respiration.
In their paper, Mencuccini & Hölttä discuss the speed of the link between photosynthesis and respiration by soil or ecosystems. They take a meta-analytical approach by applying models to data analysed for speed of link by various research groups using different methods (isotopic or canopy/soil flux-based approaches). One of their central hypotheses in the paper is that pressure–concentration waves (Thompson & Holbrook, 2004) – and not the transport and supply of newly assimilated carbohydrates to the roots and the rhizosphere – describe the speed of the link between photosynthesis and soil respiration. A pressure wave is ‘the displacement required to distribute local disturbances in turgor and solute concentration over long distances’ (Thompson, 2006). The pressure wave fronts are assumed to move several orders of magnitude faster than the phloem solution, resulting in a signal that is rapidly transferred through the phloem. The pressure wave fronts are also thought to control membrane solute exchange throughout the translocation pathway. Such a mechanism would make phloem turgor status a source of information about changes in the aboveground plant system that is conveyed to the roots. Consequently, one of the primary conclusions reached by Mencuccini & Hölttä is ‘that isotopic approaches are not well suited to document whether changes in photosynthesis of tall trees can rapidly affect soil respiration’ because they mainly trace the fate of molecules and do not account for pressure–concentration waves.
Uncertainties and potential errors
However, the conclusion that isotopic approaches are ill-suited for documenting the coupling between photosynthesis and soil respiration is provocative. There are many recent publications applying isotope pulse-labelling approaches to characterize the coupling between assimilation and belowground processes (Carbone & Trumbore, 2007; Carbone et al., 2007; Högberg et al., 2008; Bahn et al., 2009; Plain et al., 2009; Rühr et al., 2009) and to quantify the transport speed of labelled recent photosynthates to the belowground system. Consequently, controversy has developed regarding which method(s) or approach(es) is (are) most suited for assessing this coupling (Bahn et al., 2010; Kuzyakov & Gavrichkova, 2010). Furthermore, the evidence favouring pressure–concentration waves as central mechanisms to couple these processes is not as straightforward as discussed by Mencuccini & Hölttä in the main text of their paper. One major limitation is the very low number of studies for the flux-based estimates of transfer times (n = 12) included in the meta-analysis, only seven of which include vegetation taller than 2 m – only above this height do the differences in time lags become apparent between the different (flux-based vs isotopic) approaches (Fig. 1 in Mencuccini & Hölttä, 2010). These flux-based estimates are, however, the main argument to support the pressure–concentration wave hypothesis. If the additional flux-based estimates of time lags shown in the review article of Kuzyakov & Gavrichkova (2010) were included in the analysis by Mencuccini & Hölttä, then differences between the two approaches (flux-based vs isotopic) would probably be diminished. With the larger set of studies compiled in their review, Kuzyakov & Gavrichkova (2010) could consequently not detect significant differences in time lags between pulse labelling, natural abundance isotope and CO2 flux approaches (see table 2 in Kuzyakov & Gavrichkova, 2010) and concluded that ‘pulse labeling is the most advantageous approach’.
Another limitation of the study by Mencuccini & Hölttä that is explicitly addressed by the authors in the supplementary material – but not in the paper itself – is the large potential for artefacts in correlation approaches. The main source of error might be that assimilation and respiration co-vary with similar environmental variables so that causal relationships between the two are hard to disentangle. The authors cite Stoy et al. (2007) in their review, and this article is, in fact, a very good example of how one needs to be cautious when aiming to derive mechanisms of respiration from correlative information. In their paper, Stoy et al. (2007) report time lags of 1 and 3 d between assumed environmental drivers and soil respiration in a deciduous hardwood forest and in a pine plantation. These lags were, however, fully independent from photosynthesis and from phloem transport processes because they also occurred in the deciduous forest during the leafless period.
In addition, soil respiration is certainly known to be not only dependent on substrate delivery, and thus on the coupling to assimilation, but also on environmental drivers such as temperature and desiccation stress affecting root and microbial activities (Davidson et al., 2006), the latter being largely neglected by Mencuccini & Hölttä.
Speed of link vs degree of coupling
While Mencuccini & Hölttä advocate against isotopic approaches to reveal the speed of the link between photosynthesis and respiration, another recent review of the photosynthesis–respiration time lag arrives at contrary conclusions and states that isotope techniques are the best approach (Kuzyakov & Gavrichkova, 2010). The apparent discrepancy between the conclusions of Mencuccini & Hölttä and those of Kuzyakov & Gavrichkova is partially a semantic issue, but one that is highly relevant to the interpretation of the data: what actually is meant by ‘speed of link’?
We posit that researchers are interested in the aforementioned short-term effects of recent assimilates on belowground biogeochemistry, in which case the time of arrival of C molecules belowground conveys highly important information. The time that it takes a C molecule to pass through the plant can indicate the status of plant storage pools (Högberg et al., 2001), the impact of drought on biological activity (Rühr et al., 2009) and the plant nutrient status (Lattanzi et al., 2005). Clearly, the time-lag between the fixation of a C molecule during photosynthesis and its respiration belowground contains real information about plant physiology and C use as well as the degree to which plant and soil are coupled.
By contrast, the mechanisms behind pressure–concentration waves and their impact on respiration are not as clear. The increase of soil respiration as a result of the arrival of a pressure wave is particularly difficult to explain when the amount of sugar released by the phloem does not increase because the newly fixed assimilates travel much more slowly than the wave and thus have not reached the soil system. Therefore, it remains unclear what the substrate for respiration actually is in the conceptual framework of pressure–concentration wave-induced respiration. It is further postulated that the pressure increase in the release phloem is tied to an increase in water efflux from the sieve tubes. This water is assumed to be pushed into the soil along with soluble organics already present in the roots (Kuzyakov & Gavrichkova, 2010). This might well result in a short-lived increase in respiration, and this increase in respiration might indeed contain information about the photosynthetic status of the plant. However, there is a lack of empirical data that support pressure–concentration waves as a consistent mechanism behind the coupling of photosynthesis and respiration. Thus, while pressure–concentration waves as a means of signal transfer along the sieve tubes remain valid, the presentation of these waves as a pivotal mechanism behind the coupling of photosynthesis and respiration is highly speculative, and at best premature. The future challenge lies in collecting field and laboratory data to determine the eco-physiological meaning of such waves.
The work by Mencuccini & Hölttä has advanced our understanding of the role of phloem as the ‘bottleneck’ to C flow belowground. Furthermore, they have brought to the forefront the potentially important role of pressure–concentration waves in the coupling of photosynthesis and respiration, which raises important questions about their evolutionary and physiological relevance. However, we think that their conclusion on the suitability of isotopic vs flux-based approaches is not sufficiently supported by the data currently available and thus is invalid at this stage. Clever experiments need to be designed to test the hypothesis of pressure waves vs the allocation of assimilated molecules feeding soil respiration. We also emphasize that a physiological and biogeochemical basis is needed to characterize the time that passes between photosynthesis and respiration – the ‘speed of link’– so that we understand the degree of coupling between aboveground and belowground processes as well as their response to environmental stress.