Soil Rhizosphere Food Webs, Their Stability, and Implications for Soil Processes in Ecosystems

Soil rhizosphere food webs, their stability, and implications for soil processes in ecosystems John C. Moore 1, Kevin McCann 2 and Peter C. de Ruiter 3 1Department of Biological Sciences, University of Northern Colorado, Greeley, CO 80639 USA, 2Department of Zoology, University of Guelph, Guelph, Ontario N1G 2W1 Canada, 3Department of Environmental Studies, University of Utretch, 3508 Utretch, The Netherlands Introduction As students of biology we design and are exposed to a variety of caricatures to convey complex interactions and relationships. We are all acquainted with the first caricature, what for a better term can be referred to a the fundamental equation of life: 6CO 2 + 6H 20 ↔ C 6H12 O6 + 6O 2 (1) Like Euler’s equation in mathematics, Equation 1 maps several concepts. It embodies the conservation of matter, as each side of the equation possesses different molecules but equal numbers of atoms and mass. It depicts the inter-dependence between life and death processes operating at different scales, photosynthesis and respiration, the autotroph and heterotroph, the interaction between a plant and herbivore, and the immobilization of inorganic matter into organic matter and the mineralization of organic matter to inorganic matter. If we add nitrogen to the equation a similar set of processes emerges, and the interdependence of elements in shaping rates and life processes is evident (Reiners 1986, Sterner and Elser 2001). As with carbon, nitrogen is immobilized into organic matter and mineralized into inorganic matter, but we see an added dimension of a tight coupling of the compartmentalized aboveground and belowground processes as organisms from within each realm has perfected the biogeochemical pathways to immobilize the immobilize the inorganic metabolic wastes of the other. Nowhere is this more apparent than within the rhizosphere, the region of soil influenced by the roots of plants. Students are also familiar with a set of caricatures used to depict trophic interactions. The figures include a plant an herbivore and a predator, and if the vignette is of a terrestrial systems, an arrow points below the soil surface to ‘nutrients’ and/or ‘microbes’, followed by an arrow point to plant roots. The clear emphases of these depictions is on the aboveground realm, even though the interactions occurring belowground within the rhizosphere may be as or more significant in scope, complexity and overall importance to the system. Part of the reason the aboveground system receives greater attention is purely for heuristic reasons, and soils and soil processes are given short shrift stems from the obscure nature of soil biota and processes. Mathematical models represent a third type of caricature. On the one hand, effective models are internally consistent, simple in design and assumption, and thought provoking. On the other hand, they can be devoid of the details that make them biologically interesting and lead to biologically counterintuitive results. A good example of the later being the unstable mathematical representations of mutualisms and the ubiquitous nature of what appear to be stable symbiotic mutualisms that occur within the rhizosphere that have evolved over time. The objectives of this chapter are to present an approach that incorporates the three types of caricatures described above: 1) the reciprocal transfer of nutrients that are essential for plant growth and heterotrophic life depicted in Equation 1, 2) the trophic interactions among organisms aboveground and belowground, and 3) the mathematical representations of these. We demonstrate that the rhizosphere possesses a distinct trophic structure that is important to mathematical stability, and that human activities can alter the structure that are mathematically unstable and in ways that alter key ecological process. The Rhizosphere We define the rhizosphere as plant roots and the surrounding soil that is influenced by plant roots. This definition encompasses not only the roots and region of nutrient uptake by the roots, but extends into soils by action of root products and the trophic iteractions that are affected by these products or by roots (Coleman et al. 1983, Van der Putten et al. 2001, Moore et al. 2003). This definition is more inclusive than other definitions that includes roots and the soils that adhere to them, but operationally allows for a richer discussion. Significant quantities of photosynthetic products produced by plants are diverted to roots for root growth, which provides a carbon base for the soil species. The rhizosphere is characterized by rapid and prolific root growth, the sloughing of root cells, root death, and the exudation of simple carbon compounds. The size and dynamic of the rhizosphere relative to the aboveground component of plants differs by plant species and ecosystem type. For example, in grasslands, the ratio of shoot to root (S:R) production is roughly 1:1, contrasting sharply with forests, where far more photosynthate is allocated aboveground (Jackson et al. 1996), while Arctic tundra is characterized by a rhizosphere that turns over slowly resulting in an accumulation of root materials (Shaver et al. 1990). Interestingly, the range in S:R is narrowly conserved between .1 and 5 (Farrar et al. 2003); significant when contrasted with the range in plant sizes. The reasons offered for the constancy in S:R is due to the constraints on plant imposed by limitations and invariance in C:N and C:P ratios and the selective pressure to acquire just enough of the soil-based resources to balance aboveground carbon fixation. The constancy in the S:R and the dependence on elemental ratios greatly simplifies and strengthens our ability to generalize any models that we may develop. Detailed studies of the rhizosphere reveal that a growing root can be subdivided into a continuum of zones of activity from the root tip to the crown where different microbial populations have access to a continuous flow of organic substrates derived from the root (Trofymow and Coleman 1982). The root tip represents the first and lowest root zone. It is the site of root growth and is characterized by rapidly dividing cells and secretions or exudates that lubricate the tip as it passes through the soil. The exudates and sloughed root cells provide carbon for bacteria and fungi which in turn immobilize nitrogen and phosphorous. Farther up the root is the region of nutrient exchange, characterized by root hairs and lower rates of exudation. The birth and death of root hairs stimulates additional microbial growth (Bringhurst et al. 2001). The upper zones have been characterized as the region of remineralization of nutrients by predators, the region of symbiotic mutualistic relations, and the structural region (Coleman et al. 1983). Within each of the zones there is an infusion of carbon into the rhizosphere by plants which stimulates the growth and activity of microbes (Foster 1988, Grayston et al. 1996, Bardgett et al. 1998) and their invertebrate grazers (Lussenhop and Fogel 1991, Parmelee et al. 1993). Rhizosphere food web Hunt et al. (1987) presented a model of the rhizosphere food web for the North American shortgrass steppe in Colorado based on the three descriptions of food webs proposed by Paine (1980) and on the subdivisions of activities described above: 1) the connectedness web depicts the trophic interactions among organisms, 2) the energy flow web represents the flow of nutrients among organisms, and 3) the interaction web depicts the influences of the dynamics of one group on another (Figure 1). This approach has been adopted by several research groups that have attempted to link the structure of soil food webs in relation to the decomposition of organic matter and the mineralization of nutrients (Andrén et al. 1990, Brussaard et al. 1988, Brussaard et al. 1997, de Ruiter et al. 1993a, de Ruiter et al. 1993b, Hendrix et al. 1986, Hunt et al. 1987, Moore et al. 1988). The connectedness web defines the model’s basic structure (Figure 1). The diagram simplifies the high complexity and diversity by defining the web in terms of functional groups of organisms that shared similar prey and predators, feeding modes, life history attributes and habitat preferences (Moore et al. 1988). At the base of the web are plant roots, labile (C:N ratio < 30:1) and resistant (C:N ratio > 30:1) forms of detritus, and an inorganic nitrogen source. These basal resources are utilized microbes and invertebrates, terminating with predatory mites. The energy flow web expresses food web structure in quantitative measures, i.e. population sizes (biomass) and feeding rates (Figure 1). The estimates of flow are derived indirectly using a simple food web model (Figure 1), that used estimates of population sizes, turn-over rates, consumption rates, prey preferences and energy conversion parameters (Table 1, see de Ruiter et al. 1993b; Hunt et al. 1987; O'Neill 1969). Feeding rates were estimated using the procedures presented by Hunt et al. (1987). Consumed matter is divided into a fraction that is immobilized into consumer biomass (assimilation) and a fraction that is returned to the environment as feces, orts, and unconsumed prey, and of the assimilated fraction, material that is incorporated into new biomass (production) and materials that is mineralized as inorganic material. The estimates begin with top predators with the assumptions that the amount of material required to maintain the predators steady state biomass must equal the sum of its steady state biomass and loss due to death divided by its ecological efficiency: F = (D nat B + P)/e ass eprod (2) -1 -1 where F is the feeding rate (biomass time ), Dnat is the specific death rate (time ) of the consumer, B (biomass) is the population size of the consumer, P is the death rate to predators -1 (biomass time ), and eass and eprod are the assimilation (%) and production (%) efficiencies, respectively. For a top predator the death due to predator is zero.

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