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Microbial links and element flows in nested detrital food-webs

Posted on: Wednesday, 3 September 2003, 06:00 CDT

Summary

Microbial links are obligate in any food chain in soil, because detritivorous animals derive essential amino acids and other resources from microorganisms. To degrade recalcitrant substrates such as cellulose, soil animals do not produce their own cellulase, but they use cellulases derived from gut microorganisms. We argue that in detrital food-webs, carbon (energy) is usually not a limiting factor. Other elements, for example nitrogen and phosphorus, are present in ratios (relative to carbon) which are lower in the food than in the animal itself, and are more likely to be limiting. This implies that we need to consider the dynamic stoichiometry of N, P and C in the food-web and we cannot assume a fixed ratio between the three elements. In addition, detrital food- webs consist of communities at three different scales. The bacteria- algae-Protozoa compartment is nested inside the fungi- microarthropod compartment and this is in turn is contained within the earthworm-rhizosphere compartment. Animals of the higher levels consume communities of the lower levels as a whole. Present approaches for the structure of detrital food-webs do not take this nested structure into account. Our hierarchical concept of food-web structure may explain why soil pollutants that are not directly toxic to animals, may still affect the functioning of soil animals, either through deterioration of their food resources or through effects on internal food-chains.

Key words: Food-web, microorganisms, nitrogen, nutrient cycling, nutrition, phosphorus, soil invertebrates, stoichiometry

Introduction

The fluxes of elements through detrital food-webs are usually considered as being tightly connected to the fluxes of energy and carbon (Hunt et al. 1987; Berg et al. 2001). This view is based on the hypothesis that energy is the main factor limiting the productivity of soil organisms. The energy-based approach to food- webs is derived from the trophic system developed by Lindeman (1942). For several generations of ecologists the energy budget was the most important concept in analysing community metabolism (see, e.g. Petrusewicz & Macfadyen 1970). When applied to ecotoxicology, the biomass pyramid was an important concept explaining the accumulation of non-regulated elements and xenobiotics in food chains (Ramade 1977). We believe, however, that the trophic system based on biomass and energy turnover is not the only way to view detrital food-webs.

Experimental manipulation of carbon, nitrogen and phosphorus in forest soil has demonstrated that both microorganisms and macrofauna respond to specific combinations of nutrients (Scheu & Schaefer 1998). In microcosm experiments the respiration of cellulose by microorganisms was limited by N and stimulated by mesofauna- mediated N mobilization (Scheu & Schulz 1994). These and other observations suggest that the flows of elements such as nitrogen and phosphorus affect the flux of carbon and that there is no fixed relationship between the carbon flux and those of other elements. Nitrogen and phosphorus may be considered as the main limiting factors that determine the pathways of other nutrients as well as toxicants in a food chain (Krivolutskii & Pokarzhevskii 1988; Krivolutskii 1994; Pokarzhevskii & Van Straalen 1996).

In aquatic food-web studies, the differential nutrient requirements of the various trophic groups have been recognized already for some time (Cummins 1974) and the consequences for food- web dynamics are analysed with reference to ecological stoichiometry (Elser & Urabe 1999). If the stoichiometric ratios between elements vary from one trophic group to another, this implies that the elements are cycled with different efficiencies between the trophic levels. For example, the N:P ratio of excreta from grazers may be different from the N:P ratio of their food (algae) (Elser & Urabe 1999). In a similar way Van Straalen (1987) showed that trace elements that accumulate during the life of an organism have a higher turnover in the population than the biomass in which they are contained.

Table 1. Contents of some major constituents in tissues of selected groups of terrestrial organisms (% of dry mass), according to Tomme (1964), Alexandrova (1980) and Pokarzhevskii (1985, 1996a)

Differential stoichiometry of nutrient turnover can still be accomodated by a conventional food-web approach by using fixed ratios between the transfer efficiencies of the different elements. However, such fixed ratios will only be valid as long as the concentrations of nutrients are in constant proportion to each other. As soon as the rate-limiting nutrient increases in concentration, another element may become limiting and the ratios between element transfer efficiencies will change. Such situations cannot be accomodated by the present food-web approaches of Hunt et al. (1987), De Ruiter et al. (1993) and Berg et al. (2001) because these authors all use fixed tissue concentrations of nutrients and standard conversion functions from the literature.

In this paper we review the various approaches to detrital food- webs. We aim at developing a new conceptual scheme which emphasizes the nested structure of soil food-webs, the effects of nitrogen and phosphorus as limiting factors for the productivity of detritivorous animals, and the importance of microorganisms as critical links in soil food-webs. We also want to point out some implications of our approach for studies of soil ecotoxicology.

Chemical composition of soil animals and their food

It is a well-known fact that the composition of the tissues of plants and animals differ markedly in the levels of proteins, carbohydrates and lipids (Table 1). It is evident that in comparison with plant tissues, animal bodies contain more proteins and lipids, and less carbohydrates, which are abundant in plant tissues as starch and cellulose. Hence animals consuming wood, leaves and needles must have effective mechanisms to direct carbon obtained from cellulose degradation into the synthesis of proteins. On the other hand, the caloric contents of soil animals are not very different from their food; the values fluctuate within relatively narrow limits (15-20 kJ g^sup -1^) when comparing different taxonomic groups (Table 2). From this simple observation, already recognized for many years, one may draw the conclusion that for all organisms, from Protozoa to vertebrates, the energy content of the food alone cannot be a limiting factor. Data on the nutrient contents of plants and animals (Table 3) support this conclusion; nitrogen and phosphorus concentrations in animal tissues are much higher than in plant materials and especially in litter. The ratios between C, N, P and S (Redfield's numbers) indicate a significant shortage of nitrogen and phosphorus when the food of herbivores and detritivores is compared to their own body composition. The contents of essential amino acids in soil animal tissues are also one order of magnitude higher than in their food (Table 4), however, the concentrations of elements and essential amino acids in microorganisms and in soil animal tissues are close to each other.

Without specific mechanisms, the differences between soil animals and their food might lead to a deficiency. To satisfy the nutritional requirements of detritivores, they have to take up nitrogen and phosporus at a rate significantly greater than carbon. This is even more important for essential compounds that have a short half-life in the organism. This is illustrated in Fig. 1, which shows annual turnover rates (flow divided by amount in biomass) for a variety of essential elements and compounds. Mobile elements such as potassium, sodium and manganese have very high turnover rates, both in detritivores and in herbivores. The fact that turnover rates of biological constituents differ by more than one order of magnitude implies that each element moves through the food-web at its own pace, determined by the nutritional requirements of the organism.

Table 2. Caloric content of different living organisms (after Pokarzhevskii 1996a, from different authors)

Table 3. Contents of C, N, P and S in different soils and in soil organisms (in % of dry mass. The data are averages for a group. For comparison the Redfield numbers (mass ratios) are also given. Data compiled from Pokarzhevskii (1985)

Conceptual scheme of a detrital food chain

Two main conceptual schemes of soil food-webs have been proposed. The first approach suggests that energy fluxes are the main limiting and regulating factors in soil community processes and that flows of nutrients are tied to the energy flux (Ingham et al. 1986; Hunt et al. 1987). The same energetics approach lays at the base of the food- web schemes of more recent studies (e.g. De Ruiter et al. 1993; Coleman & Crossley 1996; Berg et al. 2001). In these models functional groups (in the sense of Moore et al. 1988) are defined as collections of species with a similar trophic position and similar energy metabolism. In most cases bacteria, fungi, protozoans, micro- and mesofauna are discerned as separate groups. Large detritivores such as isopods, millipedes and earthworms, and large predators, such as spiders, carabid beetles and centipedes, are often not included. Combining consumption rates and energetic parameters of soil biota De Ruiter et al. (1995) and Moore & De Ruiter (\1997) examined food-web parameters such as interaction strength between prey and predator. Prey-predator interactions can be described well on this basis, because the amounts of proteins and other compounds in the predator are similar to its food. That is why Van Wensem (1997) pointed out that the energy-based food-web models satisfactorily describe soil community structures. Polis (1994), however, criticized the approach for its inadequacy in field situations and discrepancy between estimated and real interaction strengths. However, both Polis (1994) and DeAngelis (1992) considered resources in the sense of biomass and developed models based on the dynamics of carbon.

Table 4. Contents of essential amino acids in soil animals and their food (averages are given for a group, expressed in mg per g of dry mass (after Pokarzhevskii et al. 1989, 1997). Lys = lysine, His = histidine, Arg = arginine, Thr = threonine, Val = valine, Met = methionine, lle = isoleucine, Phe = phenylalanine, Tyr = Tyrosine. Tr = trace, nd = not detected

Fig. 1. Annual turnover of essential compounds and elements through detritivores (a) and herbivore populations (b) in forest- steppe ecosystems (after Krivolutskii & Pokarzhevskii 1988). 1 - nitrogen, 2 - proteins, 3 - non-essential aminoacids, 4 - lysine, 5 - histidine; 6 - arginine, 7 - threonine, 8 - valine, 9 - methionine, 10 - isoleucine, 11 - leucine, 12 - phenylalanine, 13 - phosphorus, 14 - sulfur, 15 - potassium, 16 - calcium, 17 - sodium, 18 - magnesium, 19 - manganese, 20 - molybdenum, 21 - copper, 22 - zinc

The second approach considers flows of energy and nutrients in the food-webs as separate from each other; it specifically considers nitrogen and phosphorus as the main factors limiting productivity of the organisms in detrital food-webs (Krivolutskii & Pokarzhevskii 1988; Pokarzhevskii & Van Straalen 1996). This approach was developed during studies of nutrient cycling in chernozem soil ecosystems (Pokarzhevskii & Krivolutzkii 1997). We call it the "nutrient balance" approach, to express that for every trophic group in a food-web there should be a balance (stoichiometric ratio) between all the nutrient elements it requires and that productivity is limited by the element which is in the shortest supply (Pokarzhevskii et al. 1998). The "nutrient balance" approach pays special attention to the role of microorganisms as an obligatory link at the base of any food chain (Fig. 2). Microorganisms are considered "primary providers", which supply the organisms higher in the food-chain with essential compounds. It is assumed that all detritivorous animals depend not only on detritus but also on microbial productivity, and use microbial cells as sources of nitrogen and phosphorus, whereas energy (carbohydrates) can be assimilated directly from plant tissues transformed by microorganisms.

Fig. 2. A general scheme of energy and nutrient flows through food-chains (after Pokarzhevskii et al. 2000). The figure illustrates that the flows of carbon and energy are different from those of macro- and microelements. The thickness of the arrows indicates the volume of the flows

Internal food chains

The classification of organisms as herbivores, carnivores, or detritivores does not take into account that most of them actually rely on microorganisms as sources of protein. Soil animals such as termites, earthworms and scarabaeid larvae, like ruminants, obtain essential amino acids from microorganisms in their gut and this was also suggested for diplopods (Byzov et al. 1993). Rabbits, rodents and ruminants depend so much on the protein of their gut microorganisms, that the microbial-host interaction received a specific name, "internal food chains" (Naumova 1981). This term may well be expanded to all animals that use gut microorganisms as a source of essential compounds. Coprophagy, a well-known phenomenon in herbivorous mammals, is another mechanism to acquire extra proteins derived from microorganisms. Coprophagy is recognized as being essential for nutrient acquisition in larger soil invertebrates such as diplopods, earthworms and woodlice (McBrayer & Reichle 1971; Pobozsny 1981; Hassall & Rushton 1982; Bouche et al. 1983; Ferriere & Bouche 1985; Gunnarsson 1987). The mycetomes of cockroaches, aphids and sarcoptiform mites, and the endosymbionts of isopods and molluscs may all be considered as internal food chains, because the animals digest microorganisms or use their exudates (Daly et al. 1978; Felbeck et al. 1983; Houk 1987; Barnes et al. 1988; Krivolutskii 1995; Zimmer & Topp 1998a,b).

The importance of microbivory

Consumption of fungi and bacteria is not limited to micro and mesofauna. Xylophages such as cerambycid larvae feed on wood but do not digest the wood directly; they either use a specialized gut microflora or feed on fungi developing in wood bores and insect faeces. The "fungal gardens" of termites and leaf cutting ants are classical examples of mycophagy. The importance of fungi as a resource of proteins and vitamins of insects has been recognized already some decades ago (Martin 1979). Indirect observations, such as the increase of earthworm production observed after addition of yeast to compost (Byzov et al. 1995) indicate that mycophagy or bacterivory is also important for larger invertebrates. Similar observations were made for fresh-water molluscs (Fenchel & Jorgensen 1977). Shortages in microbial and plant proteins can be compensated by cannibalism and predation, as was recognized in woodlice (Edney et al. 1974) and earthworms (Lavelle 1983). In long-term experiments with woodlice, a protein source is added to leaf-litter, to support growth and reproduction (Donker 1992). Similarly, fish food can be added to enchytraeid forage (Rombke & Moltmann 1995). Cannibalism in natural populations should be considered as one of the most common mechanisms to compensate for protein shortages under high population densities, e.g. isopods will become cannibalistic when fed inadequately (Donker 1992). These experiences derived from feeding experiments are supported by observations in rhizotrons, which show that many animals considered as detritivores occasionally feed on carrion and carcasses of other animals (Gunn & Cherrett 1993).

Lack of endogenous cellulase in animals

Microbial links in soil food-webs may explain why efforts to find animal cellulases were unsuccessful or controversial. There is no convincing report of the production of C^sub 1^ cellulase by soil invertebrates, although beta-glucanases (C^sub x^ cellulase) and cellobiase of animal origin have been found. All data on C^sub 1^ cellulase production by soil animals were obtained in studies where microbial activity (especially activity of symbionts) had not been excluded. A classical example of C^sub 1^ cellulase in gnotobiotic Ctenolepisma lineata (Lasker & Giese 1956) was not confirmed later because the ^sup 14^C-labelled cellulose food source used in the experiment contained ^sup 14^C starch (Martin 1991). Zhang et al. (1993) and Lattaud et al. (1997) showed that the cellulase present in the gut of earthworms was of microbial origin. Skambracks and Topp (1998) observed an increase of cellulolytic activity in the gut of earthworms, but not in the number of cellulolytic microorganisms. Symbiotic bacteria are responsible for cellulase production in isopods (Zimmer & Topp 1998a), although the possibility that a significant part of the cellulase derives from bacteria that were already in the ingested food was not excluded (Zimmer & Topp 1998b). Also the cellulase of molluscs (Prosser 1973) may originally derive from symbiotic bacteria (Felbeck et al. 1983). Overall, it appears to be unnecessary for animals to produce C^sub 1^ cellulase since intestinal microorganisms, supplying them with proteins, produce this enzyme to degrade cellulose as a carbon source. Only symbiotic Protozoa in termite guts, possibly produce C^sub 1^ cellulase (Prosser 1973; Schmidt-Nielsen 1979).

The nested structure of soil communities

The nutrient balance approach places microorganisms at a crucial position in between plants, litter and humus on the one hand, and animals on the other (Fig. 2). The microbial link explains why essential elements such as nitrogen can be concentrated in the food- web. An additional aspect of the microbial link is that microorganisms are much smaller than soil invertebrates. Detritivores do not feed on specific microbes, but consume organic material including the microbial community and the microfauna growing on it. Therefore, the soil food-web has a nested structure, with the microbial community being nested inside the communities of larger detritivores (Pokarzhevskii 1996b, Fig. 3). Microbial communities occupy the pore water and water films on soil surfaces. They are dominated by bacteria, algae and Protozoa, but also include microscopic multicellular organisms such as nematodes, tardigrades and rotifers. In these communities Protozoa are not only predators of bacteria and prey of nematodes and mites, but also predators of multicellular organisms such as nematodes (Yeates & Foissner 1995). The bacteria-algae-Protozoa compartment is nested inside a fungi- microarthropod compartment and this is in turn is contained within an earthworm-rhizosphere compartment. Animals of the higher levels consume communities of the lower levels as a whole (Fig. 3).

Fig. 3. A conceptual scheme illustrating the nested structure of detrital food-webs (after Pokarzhevskii et al. 1998). A distinction is made between bacteria-algae-Protozoa communities (left), fungi- microarthropod communities (right) and earthworm-plant communities (top). Communities of the higher levels consume communities of the lower levels as a whole (indicated by arrows)

That representatives from fungi-microarthropod communities consume bacteria-algae-Protozoa communities is evident from many observations. Many fungal species are capable ofbacteriolysis. They use bacterial nitrogen, vitamines and growth factors produced by bacteria (Aho et al. 1974; Blanchette & Shaw 1978; Fermor & Wood 1981). Predatory fungi feed on Protozoa and nematodes (Alexander 1977), mites feed on bacteria (Krivolutskii 1995), springtails graze algae, enchytraeids consume bacteria with soil organic matter and fungi. Oribatid and gamasid mites and springtails feed on Protozoa, tardigrades, nematodes (Hyvonen & Persson 1996).

Thus, in a detrital food-web, we have to introduce a nested element. Similar ideas have developed by other researchers that studied invertebrate feeding or soil nutrient turnover (Heal & Dighton 1985; Barnes et al. 1988; Price 1988; Wardle 1995), but these authors did not explicitly recognize the nested aspect as a crucial food-web characteristic.

The main consequence of our "nutrient balance" approach to food- webs is that effects of toxicants on microorganisms can have important secondary effects on other organisms, because all animals depend on microorganisms for their supply of proteins. Various groups of animal microbivores disappeared after application of bactericides and fungicides, although these compounds were not directly toxic to them (Santos & Whitford 1981, Santos et al. 1981). Sterile detritus was "toxic" for aquatic isopods, which died after feeding for several days, whereas animals fed non-sterile detritus or fungi isolated from it survived (Rossi & Fano 1979). Heavy metal contamination of soil can lead to similar indirect effects in animal communities (Bengtsson & Rundgren 1982). Through effects on fungi, metals may redirect the competitive relations between springtail species (Tranvik & Eijsackers 1989).

Conclusions

We believe that detrital food-webs need to incorporate three elements which are not recognized in present-day food web models; (1) the differential fluxes of elements, especially the uncoupling of nitrogen and phosphorus from the carbon flux; (2) the inclusion of microbial links, not only at the base of the food-web, but also as "internal food-chains" in detritivores; (3) a nested structure, in which small-scale communities are eaten as a whole by communities at a larger scale. These three aspects are crucial to understand the nutritional ecology of soil communities and the impact of toxicants.

Acknowledgements. This work was financially supported by a grant from the Netherlands Organization for Scientific Research NWO (grant No 047-002-009), the Russian Foundation for Basic Research (grant No 99-04-48577), and the Russian Federal Programme "Integration" (grant M0226). We thank Prof. Dmitry Krivolutsky, Prof. Alexei Panov, Dr. Ruslan Butovsky, Dr. Jorg Rombke, Dr. Alexei Tiunov and Dr. Alexei Uvarov for valuable discussions and comments. The paper was presented as an oral communication at the II (XII) All-Russian Meeting on Soil Zoology (Moscow, 1999).

Pedobiologia 47, 213-224, 2003

(C) Urban & Fischer Verlag

http://www.urbanfischer.de/journals/pedo

0031-4056/03/47/03-213 $15.00/0

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Andrei D. Pokarzhevskii1*, Nico M. van Straalen2, Dmitrii P. Zaboev3 and Andrei S. Zaitsev4

1 Institute of Ecology and Evolution of the Russian Academy of Sciences, Leninsky Prospekt 33, 119071 Moscow, Russian Federation

2 Vrije Universiteit, Institute of Ecological Science, Faculty of Earth and Life Sciences, De Boelelaan 1085 1081 HV Amsterdam, The Netherlands

3 Institute of Biology, Komi Scientific Center, Ural Branch of The Russian Academy of Sciences, 167000 Syktyvkar, Kommunisticheskaya ul. 28, Russian Federation

4 Department of Biogeography, Geography Faculty of Moscow State University, 119899 Moscow, Vorob'evy Gory, Russian Federation

Submitted March 15, 2002 [middot] Accepted August 31, 2002

*E-mail corresponding author: apokarzh@online.ru

Copyright Urban & Fischer Verlag 2003

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