Mother trees, altruistic fungi, and the perils of plant personification.

There are growing doubts about the true role of the common mycorrhizal networks (CMN or wood wide web) connecting the roots of trees in forests. We question the claims of a substantial carbon transfer from 'mother trees' to their offspring and nearby seedlings through the CMN. Recent reviews show that evidence for the 'mother tree concept' is inconclusive or absent. The origin of this concept seems to stem from a desire to humanize plant life but can lead to misunderstandings and false interpretations and may eventually harm rather than help the commendable cause of preserving forests. Two recent books serve as examples: The Hidden Life of Trees and Finding the Mother Tree.

Re-examining the evidence for the mother tree hypothesis - resource sharing among trees via ectomycorrhizal networks.

Seminal scientific papers positing that mycorrhizal fungal networks can distribute carbon (C) among plants have stimulated a popular narrative that overstory trees, or 'mother trees', support the growth of seedlings in this way. This narrative has far-reaching implications for our understanding of forest ecology and has been controversial in the scientific community. We review the current understanding of ectomycorrhizal C metabolism and observations on forest regeneration that make the mother tree narrative debatable. We then re-examine data and conclusions from publications that underlie the mother tree hypothesis. Isotopic labeling methods are uniquely suited for studying element fluxes through ecosystems, but the complexity of mycorrhizal symbiosis, low detection limits, and small carbon discrimination in biological processes can cause researchers to make important inferences based on miniscule shifts in isotopic abundance, which can be misleading. We conclude that evidence of a significant net C transfer via common mycorrhizal networks that benefits the recipients is still lacking. Furthermore, a role for fungi as a C pipeline between trees is difficult to reconcile with any adaptive advantages for the fungi. Finally, the hypothesis is neither supported by boreal forest regeneration patterns nor consistent with the understanding of physiological mechanisms controlling mycorrhizal symbiosis.

Tree water uptake enhances nitrogen acquisition in a fertilized boreal forest - but not under nitrogen-poor conditions.

Understanding how plant water uptake interacts with acquisition of soil nitrogen (N) and other nutrients is fundamental for predicting plant responses to a changing environment, but it is an area where models disagree. We present a novel isotopic labelling approach which reveals spatial patterns of water and N uptake, and their interaction, by trees. The stable isotopes 15 N and 2 H were applied to a small area of the forest floor in stands with high and low soil N availability. Uptake by surrounding trees was measured. The sensitivity of N acquisition to water uptake was quantified by statistical modelling. Trees in the high-N stand acquired twice as much 15 N as in the low-N stand and around half of their N uptake was dependent on water uptake (2 H enrichment). By contrast, in the low-N stand there was no positive effect of water uptake on N uptake. We conclude that tree N acquisition was only marginally dependent on water flux toward the root surface under low-N conditions whereas under high-N conditions, the water-associated N uptake was substantial. The results suggest a fundamental shift in N acquisition strategy under high-N conditions.

The mycorrhizal tragedy of the commons.

Trees receive growth-limiting nitrogen from their ectomycorrhizal symbionts, but supplying the fungi with carbon can also cause nitrogen immobilization, which hampers tree growth. We present results from field and greenhouse experiments combined with mathematical modelling, showing that these are not conflicting outcomes. Mycorrhizal networks connect multiple trees, and we modulated C provision by strangling subsets of Pinus sylvestris trees, assuming that carbon supply to fungi was reduced proportionally to the strangled fraction. We conclude that trees gain additional nitrogen at the expense of their neighbours by supplying more carbon to the fungi. But this additional carbon supply aggravates nitrogen limitation via immobilization of the shared fungal biomass. We illustrate the evolutionary underpinnings of this situation by drawing on the analogous tragedy of the commons, where the shared mycorrhizal network is the commons, and explain how rising atmospheric CO2 may lead to greater nitrogen immobilization in the future.

Stem Compression: A Means to Reversibly Reduce Phloem Transport in Tree Stems.

Stem compression reduces or terminates the phloem-mediated transport of carbohydrates and other solutes in tree stems, without causing permanent damage to phloem functioning (Henriksson et al. Tree Physiol. 35:1075-1085, 2015). This has been tested on two species of pine trees, with diameters ranging from 3 to 26 cm in a forest in northern Sweden (Henriksson et al. Tree Physiol. 35:1075-1085, 2015) and in Harvard Forest, USA. Halting the phloem transport of trees in a forest is useful for studying tree physiological processes related to, or dependent on, phloem-transported compounds as well as downstream processes, in particular interactions with soil microbes. Phloem compression can be deployed in the lab and field on single trees, subsets, or over larger areas, depending on what is relevant for a particular research question.

Improved in vivo measurement of alternative oxidase respiration in field-collected pine roots.

Cellular respiration via the alternative oxidase pathway (AOP) leads to a considerable loss in efficiency. Compared to the cytochrome pathway (COP), AOP produces 0-50% as much ATP per carbon (C) respired. Relative partitioning between the pathways can be measured in vivo based on their differing isotopic discriminations against 18 O in O2 . Starting from published methods, we have refined and tested a new protocol to improve measurement precision and efficiency. The refinements detect an effect of tissue water content (P < 0.0001), which we have removed, and yield precise discrimination endpoints in the presence of pathway-specific respiratory inhibitors [CN- and salicylhydroxamic acid (SHAM)], which improves estimates of AOP/COP partitioning. Fresh roots of Pinus sylvestris were sealed in vials with a CO2 trap. The air was replaced to ensure identical starting conditions. Headspace air was repeatedly sampled and isotopically analyzed using isotope-ratio mass spectrometry. The method allows high-precision measurement of the discrimination against 18 O in O2 because of repeated measurements of the same incubation vial. COP and AOP respiration discriminated against 18 O by 15.1 ± 0.3‰ and 23.8 ± 0.4‰, respectively. AOP contributed to root respiration by 23 ± 0.2% of the total in an unfertilized stand. In a second, nitrogen-fertilized, stand AOP contribution was only 14 ± 0.2% of the total. These results suggest the improved method can be used to assess the relative importance of COP and AOP activities in ecosystems, potentially yielding information on the role of each pathway for the carbon use efficiency of organisms.

Stem compression reversibly reduces phloem transport in Pinus sylvestris trees.

Manipulating tree belowground carbon (C) transport enables investigation of the ecological and physiological roles of tree roots and their associated mycorrhizal fungi, as well as a range of other soil organisms and processes. Girdling remains the most reliable method for manipulating this flux and it has been used in numerous studies. However, girdling is destructive and irreversible. Belowground C transport is mediated by phloem tissue, pressurized through the high osmotic potential resulting from its high content of soluble sugars. We speculated that phloem transport may be reversibly blocked through the application of an external pressure on tree stems. Thus, we here introduce a technique based on compression of the phloem, which interrupts belowground flow of assimilates, but allows trees to recover when the external pressure is removed. Metal clamps were wrapped around the stems and tightened to achieve a pressure theoretically sufficient to collapse the phloem tissue, thereby aiming to block transport. The compression's performance was tested in two field experiments: a (13)C canopy labelling study conducted on small Scots pine (Pinus sylvestris L.) trees [2-3 m tall, 3-7 cm diameter at breast height (DBH)] and a larger study involving mature pines (∼15 m tall, 15-25 cm DBH) where stem respiration, phloem and root carbohydrate contents, and soil CO2 efflux were measured. The compression's effectiveness was demonstrated by the successful blockage of (13)C transport. Stem compression doubled stem respiration above treatment, reduced soil CO2 efflux by 34% and reduced phloem sucrose content by 50% compared with control trees. Stem respiration and soil CO2 efflux returned to normal within 3 weeks after pressure release, and (13)C labelling revealed recovery of phloem function the following year. Thus, we show that belowground phloem C transport can be reduced by compression, and we also demonstrate that trees recover after treatment, resuming C transport in the phloem.