Meta-analysis measures multiple mycorrhizal benefits to plants

Plants and fungi sometimes live together in peace and harmony. Arbuscular mycorrhizal associations are associations between plant roots and fungi, in which the fungal hyphae (usually branched tubular structures) grow between root cells, penetrating some cells with a network of branches or arbuscules.  Oftentimes these are mutualistic associations with both the plants and the fungi benefiting from living together. Though plants with arbuscular mycorrhizal fungi (AMF) tend to grow better than plants without AMF, it not always clear what causes them to do so.


Kura clover, Trifolium ambiguum, grown with AMF (left) and without AMF (right). Credit: Liz Koziol.

Ecologists have traditionally viewed arbuscular mycorrhizal associations as a straightforward nutrient-carbon exchange. Fungal hyphae, with their vast surface area, pick up nutrients (such as nitrogen and phosphorus compounds) from the soil, which they deliver to the root cells in exchange for plant-produced carbon molecules.

But recently researchers have identified numerous other potential ways that the fungi help the plants, including the following: (1) promoting water uptake and transport, (2) helping to spread allelochemicals – toxic chemicals that some plants release to rid themselves of nearby competitors, (3) inducing chemical defenses against herbivores, (4) enhancing disease resistance, and (5) promoting soil aggregation or clumping, which stabilizes the soil near the roots, reduces erosion and promotes stable water flow.

Ecology Fig1

Camille Delavaux and her colleagues wondered whether these other plant benefits might actually be more important than we originally thought. Delavaux was planning to write a review paper for a 1 credit independent study, but she found so many papers on this topic that she decided to collaborate with fellow students Lauren Smith-Ramesh and Sara Kuebbing on a full-scale meta-analysis.

A meta-analysis is a systematic analysis of data collected by many other researchers. Delavaux and her colleagues used the Web of Science database to find 4410 studies on how AMF supplied plants with nutrients and 1239 studies on how AMF provided other plant benefits. That’s a lot of studies! But for the meta-analysis, the authors only used a small fraction of these studies because they set certain restrictions. For example, to be used in the meta-analysis the authors required each study to show some measure of variation for the data (such as standard deviation or standard error). In addition, the authors required each study to compare plants grown under two conditions: with AMF and without AMF.  In many studies the researchers collected soil, which they sterilized in a hot oven, and then set up a test group, which they inoculated with AMF spores or a plug of soil or root fragments that contained AMF. In addition, these studies also had a control group of plants that received only sterilized soil with no AMF added.


A collection of eight different species of AMF spores. Credit: Liz Koziol.

Delavaux and her colleagues compared how plants performed with and without an AMF. Because each study was different, one might only have been looking at the effects of AMF on nitrogen uptake performance, while a second study might consider how AMF influenced soil aggregation. Effect size (Hedges d+) compares mean performance of the AMF plant to mean performance of non-AMF plants for a particular variable (such as nitrogen uptake or soil aggregation). A positive effect size means that the AMF plant did better. Of course we need to know how much better is biologically meaningful, so for each variable the researchers calculated the 95% confidence intervals of the mean effect size. If the 95% confidence intervals were positive, then Delavaux and her colleagues could be 95% confident that there was a biologically important effect of AMF on plants for that particular measure of performance.

As expected, the researchers found a positive effect of AMF on plant nitrogen uptake. The mean effect size was 0.674 with a 95% confidence interval of 0.451- 0.912. We can interpret this to mean that we are 95% confident that the true mean effect size on nitrogen uptake is between 0.451 and 0.912. But the greatest effect of AMF on plants was on soil aggregation (mean effect size = 1.645, 95% confidence interval = 1.032 – 2.248). AMF also had significant positive effects on phosphorus uptake, water flow and disease resistance.


Mean effect size (Hedges’ d+) of AMF on different factors considered in the meta-analysis.  The horizontal error bars are the 95% confidence intervals. n = number of observations.  If the error bars do not cross zero, inoculation with AMF had a significant positive effect relative to plants without AMF.

This meta-analysis shows that AMF help plants in many different ways. Researchers knew about the AMF impact on nitrogen and phosphorus uptake, but may be surprised to learn of equally strong effects on water flow, disease resistance and soil aggregation. Consequently, AMF may be very useful for forest management, agriculture, conservation and habitat restoration. As examples, conservation biologists and forest managers may need to consider adding AMF to soils that have suffered severe burns from fires, which may kill the existing soil fungi. Or agriculturalists intent on growing a particular crop may want to inoculate the soil with a specific group of AMF spores that enhance soil aggregation and water uptake, so their crop may thrive in a habitat that might otherwise not be suitable.

More than 3/4 of land plants form associations with AMF. Consequently, any attempts to restore habitats or to maintain high levels of species diversity in existing ecosystems require understanding what types of AMF inhabit the soils, and how these AMF influence ecosystem functioning.

note: the paper that describes this research is from the journal Ecology. The reference is Delavaux, C. S., Smith-Ramesh, L. M. and Kuebbing, S. E. (2017), Beyond nutrients: a meta-analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils. Ecology, 98: 2111–2119. doi:10.1002/ecy.1892. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.

Biological control: birds vs. (insects vs. insects)

We all know that birds eat crop-destroying bugs, so we might think that farmers would welcome insectivorous birds to their fields with radiant rakes or happy hoes. But not so fast! Research by Ingo Grass and his colleagues alerts us to the reality that not all insects are created equal. Some insects eat crops, but some insects eat insects that eat crops.

Aphids are one of the worst scourges of the agricultural world. They suck the phloem sap from many plant species; this action can kill the plant directly, and also cause infections by plant pathogens and viruses. Fortunately for farmers, many animals enjoy eating aphids, including birds such as the Eurasian Tree Sparrow, Passer montanus, and insects such as ladybird beetles and hoverfly larvae.


Hoverfly larva consumes an aphid while a second aphid looks on. Credit: Beatriz Moisset.

Grass and his colleagues knew that sparrows eat both aphids and hoverflies, but they did not know how the effects of bird predation on these insects cascaded down to the oats and wheat crops grown near Gottingen, Germany. Their research tested the hypothesis that sparrows eat so many hoverflies that aphid abundance actually increases (despite also being eaten by sparrows), and oat and wheat abundance decreases (top food web in the diagram below). If so, they reasoned that removing the birds would increase hoverfly abundance, thereby decreasing aphids and increasing grain abundance (bottom food web).


Agricultural food web with (top) and without (bottom) sparrows. Arrows show consumption, with dashed arrows indicating weak effects, and solid arrows and doubled organisms indicating strong effects.

The researchers set up an experiment with 11 nest boxes strategically placed between an oat field and a wheat field. Each box was equipped with a camera, so the researchers could see what the parents fed to their nestlings. In addition, Grass and his colleagues set up eight 4 X 5 meter plastic mesh exclosures which excluded birds, but allowed insects free access. They periodically surveyed 50 plants in each exclosure and in equal-sized control plots for hoverflies and aphids over the course of the sparrow breeding season. Because these birds can have three broods, this project kept them (the sparrows and the researchers) busy from early May to late July.


The birds fed very little on the two grain fields during the first brood, but towards the end of their second brood, they turned their attention to feeding on insects from the two grain fields, and later to eating the ripening grain. One important finding is that bird predation severely reduced hoverfly abundance. By early July hoverfly abundance was about 1 per 50 shoots when birds were present, and more than 3 per 50 shoots when birds were excluded (top graph below).



How did hoverfly consumption translate to aphid abundance? As you can see from the bottom graph, by early July, aphid abundance without birds was considerably lower than aphid abundance in the presence of birds. Taken together, these findings indicate that European Tree Sparrows consume hoverflies, which ultimately leads to an increase in aphid abundance.

Grass and his colleagues conclude that insectivorous birds can interfere with natural pest control of cereal production in central Europe. When birds were experimentally excluded, aphid densities declined 24% in wheat and 26% in oat crops. European Tree Sparrows were doubly bad for the crops, as they also harvested substantial quantities of grain from these fields to feed their third brood. The researchers argue that management of biological control systems for agriculture requires a broad food-web perspective that accounts for trophic cascades, such as the interactions that occur among sparrows, hoverflies, aphids and various types of economically important grain crops.

note: the paper that describes this research is from the journal Ecology. The reference is Grass, Ingo, Katrin Lehmann, Carsten Thies, and Teja Tscharntke. 2017. Insectivorous birds disrupt biological control of cereal aphids. Ecology 98 (6): 1583-1590Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.