Leaf litter and other plant debris are broken down in the soil by fungi and microbes, which decompose the organic matter into molecules which they can use.  We know that all living matter is connected through complex ecosystem interactions.  Changes in predator populations affect the prey populations which may then cause changes to the plants they eat.  Changes in plant populations would alter the amount of decomposition of leaf litter, the soil microbes and the amount of carbon dioxide released by the microbes.  This interconnection between predator and soil decomposition is not unexpected and seems fairly logical.  However, as reported by Hawlena et al. in Science last week, there is another way in which predators can affect the belowground communities.

Fear changes molecular composition of prey
When predators are present in an ecosystem, the prey are afraid and stressed out.  The stress actually causes a slight change in the ratio of carbon to nitrogen (C:N) in the bodies of the prey.  This has been reported before, but let’s try to understand why this would happen.  There are two very important types of molecules that affect the C:N ratio.
1) Sugars/carbohydrates: sugars are our main source of food and energy.  They are made of carbon, oxygen and hydrogen, but not nitrogen.  
 2) Proteins: proteins have many functions in the cell, but are usually not used as a direct source of energy. Proteins are made up of amino acids, each of which has at least one nitrogen atom.
Therefore, the amount of carbon is most affected by concentrations of sugars and the amount of nitrogen is most affected by the presence of proteins.
When prey are afraid and on guard against attack, they consume more carbs, because that’s the best source of energy.  They make less protein, because that process takes up precious energy that is needed to escape predators.  They also breakdown their remaining proteins into glucose to fuel the cells.  In other words, the prey increase their ratio of sugar to protein, which means they will have an increased C:N ratio.
When the prey with altered C:N content die in the soil, will this affect the soil microbes’ ability to decompose other materials?
Scare the grasshoppers, harm the soil
The authors set out to test this question in various settings.  They did an experiment in the field and did a number of others in a pseudo field/lab setting, so they could control the variables.  They raised grasshoppers in the field with or without the risk of spider predation.  The spiders scared the grasshoppers (understandably) and raised the grasshopper C:N ratio by just 4%.  The spiders couldn’t actually kill the grasshoppers because their mouths had been glued shut, so the authors sacrificed the scared grasshoppers and the controls and took them back to the lab.  They added the grasshoppers to large natural soil samples to let them decompose.  Both types of grasshoppers decomposed at roughly the same rates (measured by the amount of CO2 released by the soil microbes). 
The authors then added grass litter to the soils which had previously broken down the grasshoppers.  Remember there was only a 4% change in C:N ratio of the scared grasshoppers.  This small change caused a threefold decrease in decomposition of the plant material!  Small changes to the amount of carbon and nitrogen that is entering the soil can have a major impact on how well the soil breaks down plant litter.  Wow!
It’s the protein
The nitrogen content in the soil is very important to the functioning of decomposers.  Nitrogen is used by the microbes to produce enzymes that catalyze the degradation of complex carbohydrates (found in high concentrations in plants).  Therefore, the high C:N ratio in the scared grasshoppers is most likely hurting the soil microbes by offering less nitrogen.  To test this idea, Hawlena et al. created “artificial grasshoppers”, basically a mass of chitin (the shell of insects), carbohydrates and proteins.  They could change the ratio of carbon to nitrogen and specifically the amount of protein.  The more protein they added to the artificial grasshopper, the more the grass was broken down later on and CO2 emitted.  In other words, the microbes need nitrogen from the proteins of the dead herbivores in order to decompose the plant litter.  Even a small change in nitrogen content can throw everything way out of whack.
A grasshopper in the presence of predators (like the spider) will make less proteins.  When the grasshopper dies, less nitrogen (from protein) will enter the soil ecosystem.  The decomposers will not be able to make key enzymes necessary to break down plants, so the levels of decomposition will drop.
So a predator in an ecosystem can have effects all the way down to the way the tiny microbes in the soil decompose organic matter.

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