Ecological Implications of Organic Mulches in Arboriculture: A Mechanistic Pathway Connecting the Use of Organic Mulches with Tree Chemical Defenses

Effect of Organic Mulches on resource Availability

Organic mulches can affect the soil availability of two important resources for plants: water and N. Benefits of mulches to soil water content have been associated with the physical properties of mulches to buffer soil temperature (Mbagwu 1991; Bussiere and Cellier 1994). During days with high temperatures, a mulch layer protects soil surface from direct solar radiation. As a consequence, soil temperature remains cooler than air temperature and less water evaporates from the soil. Iles and Dosmann (1999) reported that 2–10 cm (0.79–4 in) of organic mulches (pine bark, pine wood, and hard wood chips) were more effective in reducing soil surface temperature [by ~2°C (3.6°F)] and increasing soil gravimetric water content [by ~0.2 g kg⁻¹ (3.2x10⁻³oz lb⁻¹)] compared to inorganic mulches (pea gravel, lava rock, river rock and crushed red bricks) or bare soil. Furthermore, Appleton et al. (1990) found that, during summer days, when soil covered with fabric or plastic film to protect them from weed establishment were also mulched, soil temperature was lower and water content was higher than nonmulched soils independently of the weed control treatment. Although the influence of mulching on soil water content is frequently associated with reduction in soil temperature, De Vleeschauwer et al. (1980) showed that mulching can also improve water content by enhancing biological activity of soil macrofauna (e.g., earthworms) that increases soil porosity.

Despite the numerous studies reporting positive benefits of organic mulches on soil water content, other studies have also reported negative or no effect of mulching on plant water availability (Watson and Kupkowski 1991; Erhart and Hartl 2003, Gilman and Grabosky 2004, Cook et al. 2006). These contradictory results reflect the variability in application methods and mulch material. For example, Gilman and Grabosky (2004) reported that hydric stress on balled-and-burlapped oak trees increased proportionally to mulch depth, after two weeks of planting. This study shows that under conditions of low precipitation and/or low irrigation rate, mulch can intercept significant amounts of water, reducing soil water-recharging rates (Gilman and Grabosky 2004). Depending on the environmental conditions, this negative effect of mulch on soil water content could be aggravated by applying mulch layer thicker than recommended by the International Society of Arboriculture [5–10 cm (2–4 in)] (ISA 2004) and by using mulching substrates with high water holding capacity, such as farmyard manure compost (Cook et al. 2006).

Organic mulches also influence the availability of N in the soil. In general, organic matter increases soil labile N through leaching and decomposition (Lambers et al. 1998; Aerts and Chapin 2000). During decomposition, decaying plant material is broken down and incorporated in the soil as particulate organic matter (POM). Nitrogen is released from POM as soluble organic N. Then, soil microorganisms may mineralize the dissolved organic N to ammonia (NH₄⁺), which may be further oxidized to nitrate (NO₃⁻). Ammonia and nitrate are considered the main sources of N used by plants in most ecosystems (Chapin 1995; Aerts and Chapin 2000). In non- or infrequently-fertilized systems, decomposition of plant material provides more than 90% of N supplied to plants (Lambers et al. 1998). For example, in Sitka spruce (Picea sitchensis) stands, system productivity of second rotation increased when branches and leaves from previous harvest episodes were left on site (Proe et al. 1996). The improvement in tree growth was attributed to the contribution of decomposing tree residues to the soil nutrient pool. The contribution was estimated to meet uptake requirements of second rotations for up to nine years (Proe et al. 1996).

Decomposition rate of decaying organic matter is highly controlled by environmental conditions, soil microbial activity and the organic matter chemical composition (Vitousek et al. 1994). Regarding organic matter chemical composition, studies have shown negative relationships between decomposition rates and the proportions of lignin:N and phenols:N ratios in decaying organic matter (Melillo et al. 1982; Vitousek et al. 1982; Northup et al. 1995; Aerts and De Caluwe 1997). Furthermore, the proportion of C:N in the organic matter has been found to be the most consistent predictor of organic matter decomposition rate (Seneviratne 2000). Specifically, plant residues with high percentages of N (> 2%), such as composted organic materials, show linear relationships with the amount of N released to the soil during decomposition (Seneviratne 2000). This pattern though, was better explained by the C:N proportion in the organic matter, rather than total N.

As in decaying organic matter, decomposition rate of organic mulches is also influenced by the substrate C:N ratio. Lloyd et al. (2002) compared the effect of two mulches made out of shredded wood pallets (C:N > 100:1) and composted yard-waste (C:N < 20:1) on soil N dynamics. They found that mulched soils with yard-waste compost had higher levels of total N, labile N and mineralization rate compared to sites mulched with shredded wood pallets. In the same study, microbial organisms immobilized up to 83% of the total pool of N in the soils after mulching with shredded wood pallets. These results support the study of Sønsteby et al. (2004) where the amount of both ammonia and nitrate, were lower on mulched soil with bark chips (C:N ~135:1) compared to nonmulched soils.

The association between organic matter C:N ratio and the amount of N released during decomposition can be explained using a metabolic approach. Overall, soil microorganisms require one atom of N for the consumption of a substrate containing 20 atoms of C (Davet 2004). During decomposition of organic matter with C:N ratio higher than 20, microorganisms have to supplement their N demand by absorbing N from the soil solution (i.e., immobilization), which in many cases results in competition with surrounding plants. In contrast, when the organic matter C:N ratio is lower than 20, excess N is excreted by the soil microorganisms in the form of inorganic N (i.e. mineralization) becoming available for the plants (Lambers et al. 1998; Davet 2004). This proportion of C to N can vary between 20 and 35 depending on the soil microbial community (Smith 1982).

Besides mulch chemical composition, soil conditions can also influence decomposition rates and consequently soil N availability. Microbial biomass and activity are sensitive to changes of soil pH, temperature, moisture and aeration (Davet 2004). However, the responses to change in these variables fluctuate among decomposer community. For example, fungi are able to develop and reproduce in a pH range of 3.5 to 8.5 while most bacteria cannot survive at a pH lower than 6.5 (Davet 2004). In addition, extremes in temperature and soil moisture reduce decomposition rates of organic matter because they decrease metabolic activities of microorganisms (Swift and Anderson 1989; Barrett and Burke 2000).

Extant nutrients in the soil may also affect mulch decomposition by providing nutrients needed by microbes during decomposition (Torn et al. 2005). However, some contrasting results have been reported between studies comparing organic matter decomposition rates in fertilized and nonfertilized soil. Torn et al. (2005) and Hobbie (2005) reported positive and significant correlation between litter decomposition rate and soil nitrogen availability in nonfertilized soil. This correlation however, was not detected when soil at the same study site was N-fertilized. Three potential explanation for these conflicting patterns are: (1) decomposition process was not N limited (Torn et al. 2005), (2) decomposition was more limited by poor C quality (e.g., high lignin content) than by N availability (Hobbie 2000), and (3) there was an inhibitory effect of supplied N on microbial synthesis of lignolytic enzymes (Hobbie and Vitousek 2000; Torn et al. 2005). More studies are needed to understand what is causing the inconsistent effects of soil N content on mulch decomposition between fertilized and nonfertilized soils.

In agro-forestry systems, mulching with blends of organic residue with contrasting C:N ratios is recommended as an alternative to enhance soil N content without adding fertilizer. Some advantages of this practice include: reduction of leaching losses, prolongation of nutrient availability and synchronization of nutrient release with plant demands (Myers et al. 1994; Fortuna et al. 2003). Schwendener et al. (2005) studied the effect of mixing high-C:N cacao litter with low-C:N leguminous litter on decomposition and soil N dynamics in a cacao agro-forest system. In this study, legume leaves decomposed faster than cacao leaves without affecting the decomposition rate of cacao leaves during the time of the experiment (96 days). In addition, total soil N and microbial activity increased proportional to the amount of legume litter in the mulch mixture. These results suggest that N availability of mulched soils with high C:N substrates (> 20) can be improved by adding low C:N (< 20) organic material to the mulch.

Resource Acquisition

Changes of soil water and N availability by mulching can have a direct effect on the amount of C and N acquired by plants. Several studies have documented that acquisition of N by plants is directly related to the abundance of inorganic N in the soil (Min et al. 1999; Aerts and Chapin 2000). As mentioned before, most plants incorporate the majority of N in the inorganic forms (NH₄⁺ and NO₃⁻). Higher concentrations of NH₄⁺ and NO₃⁻ in the soil can trigger the synthesis of nitrate reductase and glutamine synthase in plants (Oaks 1994). These enzymes are indispensable for the assimilation of NO₃⁻ and NH₄⁺, respectively.

A close relationship between N acquisition and C acquisition has been well documented (Field and Mooney 1986). In forest systems, net primary productivity (NPP) of individual trees and entire forest stands are positively correlated with soil N availability (Oren et al. 1985; Aerts 1989; Aerts and Decaluwe 1989; Sampson et al. 2006). The enhancement in productivity occurs mostly because of the increase in total foliar mass. At stand level and when levels of available soil N increase, plants allocate more resources to leaf production (Millard and Proe 1991). In this way, trees can optimize the acquired N for C assimilation (Field 1983). Although NPP can also be enhanced by an increase in leaf photosynthetic ratio (Farquhar 1978; Shadchina and Beloivan 1993), studies with woody plants of different taxa have reported no significant effect of N-fertilization on specific leaf photosynthetic ratio (Laitinen et al. 2000; Merilo et al. 2006).

Depending on the soil type, low soil water recharging rate promoted by thick layers of organic mulches can also limit C acquisition. Levels of C assimilation are determined by the amount of CO₂ entering the leaves through the stomatal aperture. Two dominant factors controlling stomatal conductance among plant species are: (1) the availability of water in the soil and (2) the particular water use efficiency of each species (Marshall and Zhang 1994; Korol et al. 1999). Chapin (1991) proposed a physiological mechanism to explain how water stress can affect stomatal conductance. Under water stress conditions, the biosynthesis of abscisic acid in the roots is transferred to the leaves. This phytohormone is responsible for decreasing the stomatal aperture and reducing the water loss. Consequently, both transpiration and C uptake rates are constrained.

Resource Allocation

In terms of resource allocation, the model (Figure 1) has a particular focus on a plant’s ability to allocate photosynthate between growth and production of secondary compounds. Evidence in the literature suggests that manipulation of nutrient dynamics in the soil can influence patterns of photosynthate allocation between growth and the production of secondary compounds (Herms and Mattson 1992; McKinnon and Quiring 1998; Glynn et al. 2003). For example, Wilkens et al. (1996) found that dry mass of tomato plant was positively correlated to the amount of fertilizer applied. However, the foliar concentration of two phenolics (rutin and chlorogenic acid) showed a parabolic relationship, with the highest concentrations of each at intermediate levels of fertilization. This pattern has been associated with plant defense hypotheses such as the Growth-Differentiation Balance (GDB) hypothesis because, in many cases, secondary compounds serve as natural defenses against pathogens and insect herbivores. Loomis (1953) and Herms and Mattson (1992) described the physiological mechanisms associated with the patterns of C allocation between growth and secondary compounds under different levels of resource availability. They contend that: (i) the assimilation of photosynthate to biomass and the synthesis of secondary metabolites are negatively correlated because both are dependent upon the same C pool of photosynthates. That (ii) under conditions of high resource availability, plant photosynthates are preferentially allocated to biomass accumulation. Finally, (iii) any condition slowing biomass accumulation more than C acquisition through photosynthesis (e.g., moderated levels of water or N availability) will increase the pool of photosynthates available for the synthesis of secondary compounds.

Alternatively, during the 1980s, a number of studies suggested that forest stands with “vigorous” trees (i.e., trees with high growing rates) are more resistant to herbivory (Larsson et al. 1983; Mitchell et al. 1983; Christiansen et al. 1987) and pathogen outbreaks (Matson and Waring 1984; Oren et al. 1985; Waring et al. 1987). This hypothesis was based on studies that examined mountain pine beetle outbreaks (Dendroctonus ponderosae). In these studies, stand wood production per unit of leaf area increased after thinning and fertilizing. Contrary to the GDB hypothesis, Waring and Pitman (1985) proposed that trees prioritize photosynthate allocation as follows: new foliage > new roots > storage > diameter growth > chemical defenses. Under this assumption, trees growing under dense canopy are more susceptible to herbivores because they receive lower levels of photosynthetic active radiation and overall produce less photosynthate. Therefore, the amount of photosynthate available for synthesis of chemical defenses become limited and trees become more susceptible to herbivores. Waring and Pitman (1985) and Waring et al. (1992) recommended stand fertilization and thinning as pest control management strategies.

Because of forest fertilization studies, fertilization has been adopted in urban landscapes as a managements practice to improve pest resistance properties on urban trees (see Herms 2002). This recommendation, clearly contradicts Lorio’s (1986) point of view of a physiological trade-off between photosynthate allocation to growth or to synthesis of chemical defenses. Lorio (1986) used the GDB hypothesis to explain how the synthesis of oleoresin [principle defensive chemicals against bark beetles (Ruel et al. 1998)] can be reduced during periods of rapid growth, creating an opportunity for bark beetle attack. Lorio’s proposition was supported by studies using a variety of botanical taxa (Bryant et al. 1987, Bryant et al. 1988, Hunter and Shultz 1995, Villalba et al. 2002). These studies showed that nutrient enhancement delayed long-term induced chemical defenses and improved the palatability of foliage to herbivores.