ALCANCE

Phenolic compounds have many roles in plant biology, including UV protection, herbivore and pathogen defence, and contribution to plant colouration. They are defined by the presence of at least one aromatic ring bearing one (phenol) or more (polyphenols) hydroxyl substitu-tions. Polyphenols are often divided into two groups: (1) low molecular weight compounds, such as simple phenols, phenolic acids, and flavonoids; and (2) oligomers and polymers of relatively high molecular weight, such as tannins. Low molecular weight phenolics occur univer-sally in higher plants, whereas higher molecular weight compounds are most abundant in woody plants, and often absent in herbaceous plants.

Total polyphenol concentration in plants varies from 1 to 25% of total green leaf dry mass. They enter the soil via two pathways: (1) as leachates from stem, leaf, and root material; and (2) within leaf, stem, and root litter. While little is known on the relative importance of these routes, it is generally assumed that significantly more polyphenols enter soil via decomposing litter than through leachates. For example, in sugar maple (Acer saccharum) stands some 23 kg ha^1an^1of soluble polyphenols were leached from the canopy, whereas 196 kg ha^1an^1entered the soil via plant litter (MacClaugherty 1983). On entering the soil, soluble polyphenols are faced with a variety of fates: they may be degraded and mineralized by heterotrophic microbes; they can be transformed into insoluble and recalcitrant humic substances; they might be adsorbed to clay minerals or form chelates with Fe and Al ions; or they might remain dissolved, and be leached out of the soil and into waterways as dissolved organic material. Insoluble polyphenols enter the soil as litter, and this is usually the main form of polyphenol that enters soil. These are slowly decomposed by microbes, contributing to the soluble polyphenol fraction.

Some fauna can digest polyphenols in their guts (e.g. earthworms), thereby enhancing their breakdown or mixing them with minerals to form organo-mineral complexes.

Leake and Read (1989) showed that mycelium biomass of an ericoid mycorrhiza was reduced by a mixture of common phenolic acids, but was increased by host-derived polyphenols from shoot extracts. All these studies on below-ground effects of polyphenols, however, were done under laboratory conditions, so the relevance of these effects at the ecosystem scale is uncertain.

There is a growing body of literature that suggests that species-specific pro-duction of polyphenols could have marked effects on soil properties at the ecosystem scale, ultimately affecting competitive interactions of plants in natural ecosystems. For example, Schimel et al. (1998) showed in Alaskan taiga forest stands that polyphenols produced by balsam poplar (Populus balsamifera) inhibited N fixation by alder (Alnus tenuifolia) and increased microbial immobilization of N, which was suggested as the cause for a decline in growth of alder with increasing dominance of poplar (Fig. 4.6).

These findings suggest that plant polyphenols produced by poplar are a control on soil nutrient dynamics and species interactions in these forest systems. Another example is that of Northup et al. (1995) who studied the effects of polyphenols released from Bishop pine litter (Pinus muricata) on soil nutrient availability. These authors found that high levels of polyphenols released from pine litter inhibited N mineralization, but increased the release of DON from pine litter (Fig. 4.7). On the basis of this finding, these

60 Acetylene reduction activity (µmol C2H2g–1 nodule h–1)

Fig. 4.6 Changes in N2fixing activity, measured as acetylene reduction activity of nodules, and general growth conditions of alder (Alnus tenuifolia) along a successional sequence of Alaskan taiga forest. N2fixing activity and growth of alder declined with increasing dom-inance of poplar, which was attributed to a negative effect of polyphenols (PA) produced by poplar on alder, as observed in the laboratory (see insert graph). (Redrawn from Hättenschwiler and Vitousek 2000, using data from Schimel et al. 1998)

authors suggested that plants living in N-limited ecosystems, such as Bishop pine, might actually benefit from increasing the DON : mineral N ratio in that it could lead to reduced N loss, owing to reduced leaching of inorganic N, and to a short-cutting of the microbial mineralization step by allowing increased uptake of organic N. As such, it was hypothesized that high polyphenol production by certain plants on infertile soils might represent an adaptive attribute to regulate the fate of N and to influence the plants competitive advantage for uptake of organic N.

There is also emerging evidence that plant phenolics have an important role in soil N cycling and plant competition in alpine ecosystems. Bowman et al.

(2004) studied a potential soil feedback involving the slow-growing alpine herb Acomastylis rossi—that produces litter that is extremely rich in phenolics—and its co-dominant in fertile meadows, the fast-growing, N-demanding grass Deschampsia caespitosa (Fig. 4.8). In a microcosm study, they found that phenolic compounds in litter of Acomastylis enhanced microbial activity in soil—since they acted as a C source for soil microbes—

leading to net N immobilization, which reduced soil N availability. They also found that Acomastylis litter reduced the growth of, and uptake of N by, Deschampsia relative to when it was grown with its own litter. Coupled with the finding that rates of N mineralization in the field were 10-fold lower in soils dominated by Acomastylis relative to those dominated by Deschampsia (Stelzer and Bowman 1998), these findings were taken to suggest that Acomastylis litter has the potential to influence soil N availability in a way that facilitates its persistence in alpine meadows. In other words, since

0.4 0.2

0.4

N release (g kg–1 total litter N d–1) 0.6

0

0.8 1.2

Tannic acid (g kg^–1)

1.6 2.0

Fig. 4.7 Release of N as either inorganic N (●) or DON (■) from Bishop pine litter (Pinus muricata) as a function of the concentration of total phenolics in litter (tannic acid equivalents) during a three-week laboratory incubation study. Data show that high levels of polyphenols released from pine litter inhibit N mineralization, but increase the release of DON from pine litter. (Redrawn from Hättenschwiler and Vitousek 2000, using data from Northup et al. 1995)

Acomastylis can tolerate lower N availability due to its slow growth and con-servative N use, it gains a competitive advantage over its faster-growing, N-demanding neighbour, Deschampsia, which is negatively affected by a reduction in resource supply. Overall, these findings—and those of other studies discussed above—indicate that plant-produced polyphenols can be important factors determining plant competitive interactions through their effect on soil microbial activity and nutrient cycling.

4.2.4 Theoretical framework for explaining plant species effects on soils

Attempts have been made to provide a theoretical framework for explain-ing how individual plant species affect soil food webs and decomposition processes, on the basis of plant ecophysiological traits (Wardle 2002, 2005).

It is well established among plant ecologists that plant species adapted to particular habitat conditions have different sets of ecophysiological traits (e.g. Grime 1979; Chapin 1980), and it is becoming clear that these sets of traits can also determine soil biological properties, especially the rate of decomposition of litters produced by particular species (Grime et al. 1996;

Cornelissen and Thompson 1997; Wardle et al. 1998; Cornelissen et al.

1999). For example, comparative studies have shown that leaf traits such as

Fig. 4.8 Fertile, wet meadow site at Niwott Ridge Long Term Ecological Research (LTER) site, Colorado Rocky Mountains, USA. In these communities, a soil feedback operates invol-ving the slow-growing alpine herb Acomastylis rossi—that produces litter that is extremely rich in phenolics—and its co-dominant in fertile meadows, the fast-growing, N-demanding grass Deschampsia caespitosa. (Image by William Bowman.)

palatability of foliage and its decomposability are positively related, in that palatable plant species generally produce litter that is of a higher quality for decomposers than do unpalatable species (Grime et al. 1996). Similar com-parative studies show that traits such as plant growth rate, size, and longevity (Wardle et al. 1998), leaf tissue strength (Cornelissen and Thompson 1997; Cornelissen et al. 1999), and nutrient use efficiency (Aerts 1997) are strong determinants of litter decomposition rate in soil (Box 4.2).