F
ood webs attempt to describe trophic relationships between organisms. An organism’s position within a particular food web is defined by its ‘function’ (e.g. whether it is a predator, a herbivore or a decomposer). Although the functional roles of aboveground organisms are usu-ally either known or can easily be estab-lished by observation or experimental manipulation, it has been exceptionally difficult to assign functional roles to belowground soil organisms. This is not only because of the habitat in which they live but also because soil organisms are phenomenally diverse, small in size, taxo-nomically challenging and practically diffi-cult to extract from their habitat sub-strate. Our ability to construct detailed soil food webs has therefore been limited and the determination of feeding guilds in soil environments has often reflected a taxonomic, rather than a functional, basis. As well as providing useful insights for the development of contemporary food-web theory1, a precise definition and appreciation of the feeding interac-tions between organisms is essential for a full understanding of ecosystem pro-cesses, such as nutrient cycling. Because approximately 90% of aboveground net primary production is decomposed below-ground2, the role of soil biota in these processes is unquestionable. However, we know little about how these organ-isms interact in food webs. Two new studies3,4 now provide the most ad-vanced attempts, to date, to disentangle the complex structure of soil food webs.Stable isotopes
In marine systems, natural stable isotope abundance techniques have been suc-cessfully applied to define the functional role of organisms5,6. In these studies, the naturally occurring stable isotopes of carbon (12C and 13C) and nitrogen (14N and 15N) are used in concert with the fact that all biochemical reactions discrimi-nate against the heavier isotope of a par-ticular element (a process called fraction-ation). The concentration of the heavier isotope tends to be enhanced in both plant and animal tissues.
In trophic interactions, as one organ-ism feeds on another organorgan-ism, the con-sumer tends to be isotopically ‘heavier’ than its food source. Various studies7,8 have attempted to quantify the difference in isotope concentration between trophic levels. For example, nitrogen (N) gives a characteristic difference of 3.4‰ be-tween any two trophic levels (Box 1).
Although stable isotopes have been used successfully in single species–substrate feeding studies8,9 of soil biota, they have never been applied to entire commu-nities. Independently, both Ponsard and Arditi3, and Scheu and Falca4have now used the natural abundance of N-stable isotopes (14N and 15N) to characterize the trophic relationships that exist between soil organisms in different deciduous for-est ecosystems (13C was also used as an additional source of information in one of the studies3).
Trophic interactions
In measuring the natural abundance of
d15N of consumers and their potential food sources at a community level, both studies make important advances on earlier soil food-web work. For the first time, ecologists have been able to identify the functional role of soil organisms within food webs in habitats where direct observations are difficult if not impos-sible. Particularly noteworthy is that both studies show similar results despite their differing objectives and methodologies.
At both the French and German forest sites, bulk animal 15N measurements were taken from different soil depths and from the litter (food source) layer. For all soil organisms, the expected clear-cut
grouping of species with similar d15N ratios into trophic levels, separated by the characteristic 3.4‰ difference previ-ously found in marine food webs, did not occur. Instead, a gradual change was observed throughout the entire commu-nity. Moreover, Scheu and Falca4found that this gradual change was not restricted to the community as a whole but was repeated even within taxa previ-ously thought to feed on a similar diet. For example, Collembola, which were initially thought to be predominantly fungal feed-ers, had d15N values (21.33‰) similar to
those of known secondary decomposers at the site (21.66‰). This immediately
questions the ‘one-taxonomic-group–one-diet’ hypothesis, which is frequently applied in soil food-web ecology1,10,11. These gradual changes in d15N values indicate a relatively high proportion of links between basal and top species within soil food webs12, and support the view of Pimm and Lawton, and DeAngelis that omnivory is common across all taxonomic groups in decomposer food webs13,14.
A distinct, and significant, difference between trophic levels could only be extracted from the data if the organisms were assigned a priorito groups of either predators or decomposers on the basis of traditional trophic classification3. Within the two a prioridefined groups, the variance of d15N values was small enough to identify each as a separate homo-geneous functional group. The mean
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You are what you eat…or are you?
Box 1. The use of stable isotopes in food-web studies
The unit of stable isotope measures:at levels of natural abundance, stable isotopes are meas-ured using an isotope ratio mass spectrometer (IRMS). This instrument measures the ratio between the heavy and the light isotopes. Because differences between absolute isotope values are usually small and subject to natural fluctuations, isotope ratios are conveniently compared relative to a standard. The deviation (d) of the ratio (R) from the standard is expressed per thousand
(‘per mil’or ‰):
15N in food webs:animal tissues are typically more enriched in both the heavy isotopes of
nitro-gen (15N) and carbon (13C) than their food source16. This effect is more pronounced in nitrogen (N)
and leads to increases in d15N of approximately 3.4‰ per trophic level5. Thus, ‘you are what you
eat (or more correctly assimilate) plus a few per mil’16. 13C is not as good a trophic level indicator
(d13C is approximately plus 1‰) but is often used as an additional source of information in the
interpretation of 15N values.
Bulk measures and compound-specific analysis: because of their small size, intact animals (bulk measures) are often measured rather than dissected parts. However, there are drawbacks in this approach17. For example, some juvenile soil insects have a different diet or a different feeding
behaviour from that which they exhibit as adults. Because the chitin exoskeleton of adult insects, which will be part of any bulk measure, is composed from substances assimilated during their juvenile stages, 15N:14N ratios might not always reflect the true trophic level of the adults. In
addi-tion, many soil animals consume considerably more than they assimilate. Removing gut contents to leave only tissues containing assimilated N is often practically impossible.
A more accurate approach would be to use the isotope ratio measurements of single chemical compounds. These compounds might be extracted macromolecules of known synthesis, such as chitin (for arthropods other than insects), DNA or phospholipid fatty acids (PLFAs). The more complex the synthesis of the macromolecules, the more likely these substances are to reflect the true trophic status of an organism within a food web. Although currently available [e.g. Py-GC-C-IRMS/MS (Ref. 18)], these methods have rarely been used.
decomposer d15N value differed from the litter layer and the mean predator d15N value differed from that of the decom-poser value by 3.4‰. These isotopic values can be taken to reflect a trophic relation between predators and de-composers, and also between decom-posers and their food source. As far as we are aware, this is the first quantita-tive (albeit relaquantita-tively simple and descrip-tive) attempt to classify the trophic structure in soil systems using isotope values derived from nonexperimental studies. This finding can also be taken as support of earlier direct observations suggesting that soil food webs consist of two15, rather than four or five, trophic levels10. However, a note of caution: although a major initial advance in the use of stable isotopes in soil interac-tions, the use of a priori classifications does have its drawbacks. Not only is there a possibility that wrong conclu-sions might be drawn about the true trophic structure of a community, but also this approach defeats the main objective of stable isotope methodology: to enable the definition of an organism’s functional role a posteriori.
Ecosystem processes
As well as providing exciting evidence elucidating the structure of soil food webs, these two studies also provide information on how soil organisms affect, and even alter, nutrient cycling. At both study sites decomposer organisms showed an average d15N enrichment from the litter of approximately 3.4‰. This suggests that litter might be their food source. Scheu and Falca4 found that decomposers collected from deeper layers possessed d15N values that were more similar to the d15N values (1 3.4‰)
of the top litter layer than to those (1 3.4‰) of the soil layers they were
extracted from. This finding can be inter-preted in one of two ways. Organisms liv-ing in deeper soil layers either feed exclu-sively on the top litter layer but have relatively high mobility and dispersal capabilities or they feed selectively in the deeper soil layers on compounds that are isotopically similar to those found in the top litter layer.
Individual species variation
Both studies also found that neither the litter layer nor its components were isotopically homogeneous. In analysing the biota, a few individual species classified a priori as primary de-composers did not show the expected ~3.4‰ shift in d15N. In fact, isotopically they were virtually equal to (Lumbricus
terrestris 22.82‰), or even below
(Glomeris marginata25.37‰), the mean
litter values (23.68‰)4. This suggests that a few specialized species within each trophic guild feed on totally differ-ent resources to all the other member species.
Some invertebrate predator species in both studies showed values for N that were well above the expected 3.4‰ shift, even when compared with the highest
d15N values found in their potential prey. This might have been due to either intraguild predation among predators3or to a mixed diet consisting of both pri-mary and secondary decomposers, with a preference for secondary (often more enriched in d15N than primary) over pri-mary decomposers4.
Regardless of the mechanism, the data provide further evidence that omnivory is common in soil food webs. If this is the case, then it would suggest that there is little specialization among soil animals and consequently there exists a high degree of functional redun-dancy in soil food webs. In addition, it would appear that soil communities con-tain a few trophic specialists that poten-tially play a key role in nutrient cycling and other ecosystem processes.
These two studies are rich in novel and valuable information that will not only help future researchers to design properly manipulated experiments, but also contributes substantially to the development of new modelling ap-proaches that take into account the fact that taxonomic groups rarely reflect trophic guilds. Combined with manipu-lated food-web experiments there is no doubt that isotopic techniques will enhance not only our understanding of the structure and function of soil food webs, but also the role organisms play within these ecosystems.
Acknowledgements
We thank M. Bradford, N. Tïen, W. Voigt and M. Bonkowski for ‘enriching’earlier versions of this article.
Till Eggers T. Hefin Jones
NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berkshire, UK SL5 7PY ([email protected]; [email protected])
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