Interactions with soil biota shift from negative to positive when a tree species is moved outside its native range

Pinus contorta

Pinus contorta. Image by Rudi Riet, Washington, DC, United States [CC-BY-SA-2.0], via Wikimedia Commons

This week’s paper is a Rapid Report by Gundale et al which appeared in New Phytologist in late January.  It also happens to be the paper we discussed at the Hawkesbury Institute for the Environment’s student journal club this week.

This study was a really good example of a home-away growth experiment, and showed some really striking results.  Seeds from Pinus contorta trees of known provenance were collected in Sweden, and then grown in soil from their native Canadian sites and their introduced

Swedish sites to look for differences in aboveground and belowground biomass.  Sounds simple?  It would be, but they didn’t just compare fresh soils containing whatever biota could contend with the 2mm sieve.  They also used sterilised soils from both countries, sterilised soils which had been cross-inoculated with soils from the opposite country, and included a fertilisation element to make it more interesting.

So what was the take-home message?  The clue is in the title, but the short version is that it’s all about the soil biota.  Seedlings grown in Swedish soils had much higher biomass (around 43% higher) than those grown in native their native Canadian soils, despite the Swedish soils having lower pH and nutrient availability.  When seedlings were grown in sterilised soils, the soil origin had no effect on biomass.  When seedlings were grown in sterilised soil from either country, but inoculated with soil biota from Sweden, biomass was again much greater than when sterilised soils were inoculated with Canadian soil biota.  The effect of soil biota was even greater than the effect of fertiliser on biomass.

Considering these different trials together, it becomes clear that not only did the Swedish biota have a strong positive effect on P. contorta seedling biomass, but that the Canadian biota actually had a negative effect on biomass. This provides evidence that better growth in soils from outside of the native range is probably down to a combination of pathogen release and positive biotic associations.

However, this evidence also highlights the gap in this paper – analysis of the soil biota itself.  We see the effects, but what are the actual differences in the bacterial, fungal, and/or mesofaunal communities?  Are there differences in community structure? Abundances or biomass? Activity?  All of these?  It would be great to see data on this, especially regarding known pathogens or ectomycorrhizal fungi associates.  I hope/suspect there may be another paper on the way exploring some this.

Overall, this was a really nicely designed project that asked interesting questions and addressed them in a very straightforward way.  The paper itself was well written.  It flows nicely and is easy to follow and understand even on a quick reading.  The methods made no attempt to disguise the logistical issues associated with transporting soils half way around the world, and the data analysis and presentation was simple and direct with no unnecessary frills or risk of misinterpretation.  All of these are elements that we should expect of any paper, but sometimes experiments are complex and difficult to describe, methodological detail gets glossed over in an attempt to meet word counts, and data are not easy to interpret.  While it is not possible to answer all questions with a glasshouse study, or to present all data with bar graphs, it is a nice reminder of the clarity with which we should try to communicate our work.

So now that I’ve had my say, exposing my soil ecology and science communication biases, we’d love to hear what you thought about the paper.  Was there anything you would have done differently?  What do you think the next steps should be?  What did you think of the tree provenance element of the study?  It didn’t show a significant effect here, but would it be worth pursuing in other systems?  How well do you think the results of this glasshouse study represent what’s happening in the natural communities?

You can let us know your take on this either in the comments or via twitter using the hashtag #psejclub.  We’d also love to hear from you If you have a suggestion for a paper you’d like us to discuss, or if you want to write a post yourself!

Pinus contorta native range.  Image by  Elbert L. Little, Jr., of the U.S. Department of Agriculture, Forest Service, and others

Pinus contorta native range. Image by Elbert L. Little, Jr., of the U.S. Department of Agriculture, Forest Service, USGS

P. contorta range in Sweden.  Image by Philippe Rekacewicz, UNEP/GRID-Arendal

P. contorta range in Sweden. Image by Philippe Rekacewicz, UNEP/GRID-Arendal


Eutrophication weakens stabilizing effects of diversity in natural grasslands

This letter, by Yann Hautier and many others, appeared in Nature ten days ago. Its focus is grasslands, and what happens to their [above-ground] diversity when you add fertiliser. I was drawn to this paper by the simple message communicated in the title, and the universality implicit in ‘natural grasslands’. Excellent; a succinct study of the effects of excessive nutrients on the modulation ecosystem functioning by diversity – read on!

It’s immediately apparent that the strength of this work lies in the size and global reach of its dataset. The authors utilised an established network of experiments looking at the relationships between fertilization, diversity and production in grasslands: the Nutrient Network (NutNet). This allowed the authors to address their hypotheses using data collected from 41 different grasslands, spanning five continents. One of the major advantages of using sites in an established network is that methods are broadly standardised; this goes some way towards ensuring that, while the sites encompass a wide range of variation in grassland types, the data are comparable between sites. In the extended methods section, the authors describe the sensitivity analyses they performed to check that distinctive sites (subject to strong seasonality, or anthropogenic influence, for example) did not unduly influence their results.

So what did the authors measure? They chose above-ground net primary productivity (ANPP) as their response variable, which they estimated by measuring above-ground live biomass at each site. The authors also introduced two related concepts: the stability of ANPP and species asynchrony; stability of ANPP increases as species asynchrony increases and the productivity of individual species fluctuates in response to the environment at different rates. This is a neat idea: in an asynchronous community, a decline in the productivity of one species is more liekly to be compensated for by another, and so the productivity of the community as a whole is more likely to remain stable.

To arrive at their finding that the application of fertiliser weakens the stabilising effect of diversity, the authors observed that, while the temporal variation of ANPP decreased at higher diversities in the unfertilised communities, it increased at higher diversities in the fertilised communities. The increased variation in ANPP, combined with lower species asynchrony in fertilised communities, led the authors to conclude that [over]-fertilisation of grasslands can reduce the stability of their productivity. Importantly, the authors showed that the loss of diversity caused by fertilisation didn’t affect species asynchrony.

While I initially found this article difficult to get to grips with, due to the introduced concepts and number of scatterplots and lines to compare, but now that I get it, I agree with the results. One of the best aspects of this study is that it draws its conclusions from a controlled experiment, rather than observational correlations. I think the work also raises a number of further questions, which would be interesting to address using NutNet or a similar project.

  • The authors used species richness as their measure of diversity. What about functional diversity? Perhaps some groups (grasses, forbs, legumes) respond to fertilisation more than others?
  • While ANPP is certainly likely to be related to below-ground productivity, it would be interesting to see whether stability of below-ground productivity showed the same patterns in response to fertilisation. Are there other ecosystem functions that are worth measuring? What about carbon and nitrogen cycling? These functions obviously come with the caveat that they are much more difficult to measure (you can’t just see them, unlike plants), but if it was feasible, what patterns might we expect to see?
  • The amount of fertiliser applied in the study was quite high. Do we see the same results at lower concentrations?
  • There were no sites in South America – do we think this is likely to have biased the result significantly?

Now that I’ve had my say, it would be great to hear yours; did you find this paper interesting, do you think its conclusions are valid? How might you have done things differently? Do you think there are specific lessons to be learnt? Please get in touch by commenting on this post, or on Twitter or Facebook using the hashtag #psejclub. I’m looking forward to hearing from you!

#psejclub discusses: plants, fungi, competition and carbon storage

It’s nearly two weeks since Franciska wrote the first post for our journal club (#psejclub), about a paper published in Nature, entitled ‘Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage‘. Her thoughts on the paper prompted an interesting discussion, which you can catch up on here.

Keep your eyes peeled for a new #psejclub post in the next couple of days!

Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage

– added by Franciska de Vries

This paper, by Colin Averill and colleagues, came out as a Letter in Nature almost two weeks ago. It immediately excited me, as the title suggests that in this paper, the authors are revealing the mechanism through which mycorrhizal fungi increase soil carbon storage. Groundbreaking!

I started to read. What the authors did in this paper was compose a global dataset, consisting of observations of soil organic C, N, and clay content (to a depth of one meter) across a range of vegetation types and biomes. They then assigned values of mean annual temperature (MAT), mean annual precipitation (MAP), and net primary productivity (NPP) to each site, using previously published climate interpolations and satellite-based observations. Finally, they assigned a mycorrhizal status to each of the vegetation types, which could be either arbuscular (AM) or ericoid and ecto-mycorrhizal (EEM).

Mycorrhizal status of each site was assigned based on the dominant vegetation present, and knowledge of its mycorrhizal status. Understorey vegetation (in forests) was ignored, and where no vegetation data was present, they used the vegetation description. So, for example, the vegetation description “grassland” was classified as the AM, whereas “mixed coniferous forest” was classified as EEM.

This dataset was then used to explain soil C storage, using soil N and mycorrhizal status as explanatory variables, while at the same time accounting for variation in climate and other soil properties.

Using mixed effects models, the authors found that in ecosystems dominated by EEM fungi, 1.7 times more C was stored per unit N than in AM ecosystems.

For the first time, this study shows that C global cycling does not only depend on abiotic factors like temperature and moisture, but also on soil mycorrhizal status, highlighting the importance of biotic factors in addition to abiotic factors for soil C storage. This finding supports the results from a modelling study by Orwin et al. (2011), who showed that competition for organic N between EEM and decomposer fungi increases soil C storage.

Averill and colleagues conclude that ‘mycorrhizal functional traits are as important a control over decomposition and soil C storage as are soil chemical properties and the physical protection of soil organic matter’, and that ‘the identity and functional traits of soil microbes exert a control over the terrestrial C cycle’.

So, a pretty exciting paper, but does it really do what it promises? When I read the title, I expected a paper reporting on (a range of) mechanistic experiments to prove that mycorrhizal fungi drive soil C storage. But, rather than a mechanistic study, it is an observational study that uses a powerful data set and an advanced modeling approach to show that there is a relationship between mycorrhizal status and soil C storage. However strong their finding is, and although it holds across a range of ecosystems and biomes, their study does not allow for testing a hypothesis and elucidating a mechanism. As Mark Bradford elegantly says in his News and Views article about the paper: “The authors propose, in line with a previous hypothesis, that these richer carbon stores result from competition for nitrogen between EM fungi and free­living soil microorganisms that feed on organic matter” and: “Pinpointing which mechanism explains Averill and colleagues’ results will require more data and involve challenges common to all large observational data sets, including unobserved variables and spurious cor­ relations”.

I couldn’t agree more.

However powerful the data set in this paper is, there are several issues that would have to be addressed to come up with a conclusive answer of how and whether mycorrhizal fungi drive soil C storage. First of all, important soil properties that can explain both soil C content and mycorrhizal status, such as soil moisture or pH, haven’t been included in the models. Second, certain vegetation types, such as heathland, which is known to be dominated by ericoid mycorrhizal fungi, are missing. Third, the assigned mycorrhizal type might be occurring under a certain vegetation type because of the quality of the C inputs into the soil, which might itself drive soil C storage; something that the authors do acknowledge in the paper. Finally, Mark Bradford calculated, in his News and Views article, that only when the soil contains more that 3 kg N per square meter, C stores in EEM dominated systems exceeds that of AM dominated systems by 1.3 times.

But, despite these nuances that will need addressing in future studies, this is an important study that proposes an important hypothesis, namely that mycorrhizal type is of pivotal importance in driving soil C storage. By formulating this testable hypothesis and identifying a global relationship between soil biota and soil C storage, this study significantly advances the field of plant-soil interactions. It also highlights that disruptions of links between vegetation and mycorrhizal fungi, as a result of global change, might have far-reaching implications for soil C stocks and thus for the climate mitigation potential of soils.

So, I am curious what other people think about this paper! Do you agree or disagree with my views? How do you think we could go about testing the hypotheses proposed in this paper? Or is this enough evidence already? What do you think about the statistical methods used? Feel free to comment – the aim of this journal club is to stimulate discussion – through replies here, but also on Twitter. If you respond on Twitter, please use the hashtag #psejclub.


With thanks to all members of the Soil and Ecosystem Ecology group of The University of Manchester for inspiring discussions.

Full reference: Averill, C., B. L. Turner, and A. C. Finzi. 2014. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature advance online publication.