Lecture 16. The Role of Soil Animals in Decomposition
And nightly, meadow-fairies, look you sing,
Like to the Garter’s compass, in a ring:
The expressure that it bears, green let it be,
More fertile-fresh than all the field to see.
--Merry Wives of Windsor, V, v
-attention so far has been on fungi and bacteria -- the main agents of decomposition
-but what about the soil animals? How do they figure in this?
-soil systems are about the most complex environments known:
“Up to 1000 species alone in a well developed temperate woodland soil (of which several hundreds will
be mites and Collembola), at densities >1-2 million/m2”
“There are approximately 45,000 described mite species world-wide, two-thirds of which are found in
soil. But described species of mites are estimated to represent only 5% of total mite diversity.”
(Behan-Pelletier and Newton, 1999, BioScience 49: 149-153)
**-most of these organisms feed on detritus or the microbes growing on it
-so some effect on the decomposition process is to be expected.
** we are still trying to figure out exactly how soil animals influence decomposition
-generally, soil animals here refers to soil mesofauna;
-except for nematodes, the role of microfauna in soil processes are very poorly known
-a few animals, notably earthworms and termites, have dramatic effects on decomposition,
-because of the large volume of material that they consume.
-more difficult question is the significance of the microarthropods
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Field Studies on Animals
-our best evidence of soil mesofauna effects come from field studies
-using litterbags, there are two simple ways to study animal effects in the field:
-first is to put out litterbags in the usual way, in pairs
-to one set of bags, add a repellent or a toxin, usually naphthalene, to get rid of animals
-compare mass loss between control and treatment bags (assuming toxin does not affect microbes!)
-or, make litter bags of different mesh sizes, so as to exclude animals, especially earthworms
-difficult to build litterbags that exclude the microfauna
** these experiments often show that soil fauna change both the rate of decomposition
(mass loss) and rate of nutrient release
-by using different mesh sizes, we can confirm that large organisms like earthworms have
a dramatic effect of mass loss
-trouble is, hard to tell if lost material is truly decomposed or just dragged out of the litterbag
**substantial effects of microarthropods on litter decomposition have also been demonstrated
-see figures on next page (very old: sorry for the poor quality)
-but effect is not always positive;
-sometimes decomposition slows down in the presence of animals
-we have also made abundant use of microcosms
-excellent example of the microcosm approach is work of Heikki Setälä in Finland
(Setälä et al. 1988, 1990a, 1990b etc., all in Ecology)
-he set up complicated microcosms of birch litter or needles over humus from a coniferous forest floor
-with and without various kinds of soil animals
-many replicates monitored under natural conditions (summer and winter) for up to two years.
**his work emphatically shows a stimulatory effect of soil micro-animals on litter decomposition rates
-CO2 evolution increased up to 32%
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-in later experiments, Setälä included a birch seedling in each microcosm
** adding animals to the microcosms sharply increased the growth rate of the birch tree
-and nutrient contents of tissues (N and P in leaves by 3× and 1.5×)
-presumably, more rapid decomposition released nutrients for trees roots to absorb
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-also changed root:shoot ratio toward more shoots,
-again because less extensive root network necessary
**-but again the situation is complicated
-in most complex microcosms, fauna accelerated litter decay, but inhibited respiration in the humus
-and results were strongly influenced by composition of the animal community.
-adding fungivores and detritivores (who also eat microbes) stimulated decomposition and tree growth
-adding top predators made no difference, even though they reduced populations of the above groups
[therefore little evidence of trophic cascades]
-also, it didn’t matter which species, or how many species (1 to 5), were added in each trophic group
-suggesting a great deal of functional redundancy in soil animals
-with the exception of one enchytraid worm, that seemed to be essential
-a more recent study refutes this result, suggests that animals become important at larger scale
-we have come to see soil animals as regulators of decomposition rates
-how are they doing this? A number of possibilities:
Animals as Litter Consumers
-simplest proposition is that animals consume detritus directly. (that is, act as primary consumers)
-soon becomes obvious that this is not the case
-table below shows mineral standing crops in different organism groups
-more or less typical data
-of course, throughput, not standing crop, is what really matters
-a rough calculation shows that for animals like these to be significant in energy flow in the litter system,
-they would have to consume their own weight ~1000 times per year, or roughly 3 times d-1
-and much more for element cycling
** usual case is for direct invertebrate consumption of litter to account for <5% of total mass loss
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So how do animals accelerate decomposition?
-variety of evidence suggests secondary effects may be important
-that is, effect of animals on the decomposer microbes may affect their decomposition ability
Mechanisms of Animal Effects
-it has been postulated, back in the 60s and 70s, that animals might enhance decomposition rates by
interacting with the microbial community,
-and thereby changing microbial metabolic rates
-postulated mechanisms:
1. Comminution
-popularly known as “shredding”
-many litter-feeding invertebrates chop and crush and shred the litter as they feed
(here we are speaking just of shredding, not chewing and digestion -- see below)
Effect: reduces particle size and increases surface area for colonization.
In one study, 180 mm2 of pine needles became ~1.8 m2 after animal feeding,
-an increase of 1000 times. [Mignolet ‘72]
-this change in surface area may be important for bacteria that cannot penetrtate (and some fungi)
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2. Passage through the gut
This has three categories of effect
(A) physical disruption
(B) digestion and chemical changes
(C) innoculation
A. Physical disruption results from chewing and is therefore connected to particle size reduction
-as whole leaves are chewed up, access provided to cells, tissues, protected by structure of the leaf
-e.g., breaks cuticle, breaks structural fibres, opens cells, opens lignin to let bugs get at cellulose
B. Digestion of leaf litter is generally very incomplete (no cellulase enzymes)
-animals digest mostly the fungi and bacteria (less) growing on the surface
-a great deal of the digestive capacity of most animals is derived from gut symbionts,
-either bacteria or actinomycetes (in earthworms)
-termites are the classic example (gut contains a protozoan which contains a bacterium)
-but there may be significant “softening” of the ingested material -- and lower C/N ratio
-may also be altered pH or addition of gut secretions
C. passage through the guts of insects (and other organisms) tends to disrupt filamentous fungal growth
-but enhances bacterial growth
-feaces of shredders may support 5-10 times the bacterial population of the ingested litter
-guts provide an incubator of bacterial populations to continually colonize ingested material
3. Dispersal of Propagules
-passage through the gut is important for bacteria, but largely excludes fungi or actinomycetes
** Nevertheless, many studies have demonstrated spore transport in or on mites, springtails
-and most other soil organisms studied
**transport by animals appears to be a major route of dispersal for fungi in soil
the Table below shows typical results from these studies
-note high prevalance of spore-carrying animals in each group
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-recall that soil fungi are prolific spore-formers, especially Deuteromycota,
-so spores are everywhere
-many are sticky, adapted to clinging to animals like weed seeds
-there may or may not be preferential spore transport
-depending on the animal’s feeding preferences and the characteristics of the fungus.
But does this matter to decomposition?
Hassell et al. (1986): in a microcosm, transport of spores by a collembolan accelerates decomposition
of sterilized aspen leaves (see figure below)
-because the collembolan innoculates the leaf
** But, when the experiment was repeated with non-sterile leaves, already colonized,
-collembolan made no difference
-presumably because there were lots of spores from many species there already
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4. Selective Feeding: Growth Stimulation and Altered Succession
-theory runs like this:
-as microbial growth proceeds, the growth curve begins to taper off
-from depletion of space, carbon sources, nutrients, or from accumulation of waste products
-theoretically, if animals eat and recycle old hyphae, they would stimulate fungal growth
-and cause faster decomposition
-this theory was tested by a number of researchers back in the early 1980s
-stimulation by removal of old hyphae did occur,
-but only when the animal population was in the right range.
-too many or too few inhibited fungal growth
**a very tight analogy here with grazer effects on vegetation
-also possible that selective feeding by fungivorous animals alters the competitive balance among fungi
-and thereby alters the fungal community composition
**some animals are known to be very selective of which fungi they feed on
Results here too have been both ways:
-McLean et al. (1996), grew oribatid mites and collembola on pine needles in the laboratory, and found
they “did not affect fungal species richness, diversity, dominance, or per cent frequency of occurrance of
29 fungal taxa, including taxa known to be preferred and avoided by the animals.”
-that seems pretty definitive
-on the other hand, look at decomposition of Sitka spruce needles in England (Newell 1984a, b)
-system dominated by two basidiomycot fungi, a fast-growing Marasmius and a slow-growing Mycena
-and a fungal feeding collembolan, which preferentially eats the fast-growing Marasmius
-add the collembolan to the litter, it shifts balance from Marasmius to Mycena
-rate of needle litter decomposition slows down
(in another system, with different fungi, the effect could go the other way)
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-appears that effect of animals on decomposition rates not due to changes in fungal community structure,
-but rather to shifts in competitive balance between community members
-at another level, animal feeding may alter competition between fungi and bacteria
-in culture experiments, bacterial growth is increased by animal feeding on fungi,
-probably because the bacteria snap up all the released nutrients
Variation with climate?
-from Heneghan et al. 1999. Ecology 80(6): 1873-1882.
-they did a field study on decomposition of oak leaves in tropical sites (Costa Rica, Puerto Rico)
-compared with a temperate site (North Carolina)
-used litterbags treated with naphthalene
-very little effect of microarthropods in North Carolina
-but a strong effect in the tropics
** they argue: faunal effects should be more pronounced in the tropics, where climate is more stable,
-therefore more opportunity for faunal-microbe interactions to become more intense
-they suggest fauna should become less important farther north as climate becomes more variable
Conclusion: Fauna influence the rate of decomposition in complex ways, largely through
secondary interactions with the microbial community.
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