Red oak responses to nitrogen addition depend on herbivory type, tree family, and site

Abstract

Elevated atmospheric N deposition is predicted to increase plant growth and C storage in N-limited systems, but this assumes that no mitigating ecological factors are influenced by N deposition. Many herbivores are also N-limited and so increased herbivore damage in response to N deposition may moderate, or even eliminate, gains in plant growth under elevated N. Thus the response of herbivores to N deposition could influence the onset and magnitude of N saturation resulting in expedited decreases in C storage. Since tree susceptibility to herbivores is partially under genetic control and will be influenced by site characteristics, we tested whether the interaction between N deposition, tree growth, and herbivore damage depends on tree genetic variation in susceptibility to herbivores at different locations. By monitoring 12 half-sib families of northern red oak (Quercus rubra) saplings at two common garden sites in south-central Pennsylvania, we found that herbivores were pervasive at both sites, resulting in 13% chewing damage, 16% galling damage and 28% browsing damage. N addition significantly affected browsing damage (8% overall increase) and chewing damage (19% overall increase) but did not affect galling damage. However, this effect was strongly dependent on the Q. rubra family and location, both of which influenced oak susceptibility to herbivore damage independent of N additions. Greater browsing damage on trees under N addition caused reductions in relative height growth, and this effect also depended on tree family and location. Our result suggests that herbivory, mediated by tree genetic lineage and site-specific conditions, may represent an important component of C sinks and N saturation under elevated N deposition.

Introduction

Many regions of the world now receive elevated inputs of nitrogen (N) as human populations increase consumption of fertilizer and fuel (Vitousek et al., 1997, Gruber and Galloway, 2008, Schlesinger, 2009). Forests of the world receive currently up to 60 kg ha⁻¹ year⁻¹ of anthropogenic N deposition, depending on proximity to sources and elevation, and such N inputs are predicted to continue and increase (Fenn et al., 1998, Van Egmond et al., 2002, Galloway et al., 2004). Since many temperate forests are generally N-limited, increased N availability has been predicted to enhance forest growth and C storage (Hyvonen et al., 2008). However, over time some ecosystems may exceed their ability to retain N, which could lead to subsequent reductions in net primary production and ecosystem function (Zaccherio and Finzi, 2007, de Schrijver et al., 2008, de Vries et al., 2008, Bedison and McNeil, 2009) and there is growing concern that prolonged increases may cause long-term forest decline (Aber et al., 1989, Reich et al., 1997).

The onset and degree of nitrogen saturation is difficult to predict and most studies have focused on the role of abiotic factors like temperature, moisture, and other limiting nutrients and kinds of pollutants (Aber et al., 1993, Davis et al., 2008, Hyvonen et al., 2008, Bedison and McNeil, 2009). As a result, we know little about potentially mitigating biotic factors like pests which can slow or eliminate forest growth and lower the threshold value of N deposition at which ecosystem C storage saturates.

Like many trees, herbivores are often N-limited. However, depending on environmental factors, herbivore feeding may increase, decrease, or be unaffected by increased foliar N. If herbivores consume greater amounts of high N foliage, the response of herbivores to N deposition may moderate, or even eliminate, gains in plant growth under elevated N (e.g., Ayres, 1993, Ritchie et al., 1998, Throop and Lerdau, 2004) and herbivores could lower the threshold value of N deposition at which ecosystem C storage saturates, resulting in expedited decreases in C storage. Herbivores are both consumers of primary production and resources for other trophic levels. They have complex impacts on ecosystems (Schmitz, 2009) and their response to elevated N deposition is relatively unknown (Tylianakis et al., 2008, Zehnder and Hunter, 2008). However, three lines of evidence suggest that increased N deposition may indirectly decrease the growth of plants by increasing herbivore attack. First, herbivore damage commonly decreases plant growth and fitness and sometimes does so at even low levels of damage (Crawley, 1985, Hochwender et al., 2004). Second, the intensity of herbivory usually correlates with plant chemistry (Schultz, 1988, Berenbaum, 1995); in general, herbivore damage tends to be more severe on plant tissues with relatively higher levels of N and lower levels of defensive compounds (Berenbaum and Zangerl, 1998, Abrahamson et al., 2003). Third, N fertilization or increases in N deposition can cause changes in plant chemistry favorable to herbivores (Bryant et al., 1987, Forkner and Hunter, 2000). As a result, plants are likely to become more susceptible to herbivores in response to increased N input (e.g., Bryant et al., 1987, Hunter and Schultz, 1995) and experience greater herbivore damage.

Three additional ecological factors may influence the indirect effects of increased N deposition on plant growth: plant genetic variation, herbivore identity and abundance, and geographic location. Plant genetic variation influences plant susceptibility to herbivory (Maddox and Cappuccino, 1986, Fritz, 1992, Orians and Fritz, 1996, Rossi and Stiling, 1998, Mutikainen et al., 2000) and plant defense (Wainhouse et al., 2000) in responses to N addition. This information is especially important to forest management strategies because identifying and preserving plant genotypes that become more resistant to herbivores and productive under increased N deposition may facilitate the potential for sustainable C sequestration management strategies. Similarly, the abundance and identity of herbivores has a large effect on the effects of herbivory on plant growth (Marquis, 1990, Orians and Fritz, 1996, Mutikainen et al., 2000, Forkner and Hunter, 2000). Since herbivores feeding in a similar way on the same plant parts are more likely to respond similarly to changes in plant quality, feeding guilds have commonly been used to group diverse species assemblages of herbivores in studies that evaluate their interactions with plants (Fritz, 1992). Last, site-specific conditions such as soil chemistry or herbivore community structure may also exert an influence on the rates of herbivory and responses to N deposition (Marquis, 1990).

To evaluate whether elevated N can increase herbivory to influence tree growth in a temperate natural forest, we examined the short-term impacts of N addition on height growth and susceptibility to three kinds of herbivory for 12 half-sib families of northern red oak (Quercus rubra L.) saplings at two locations (Michaux and Tuscarora) in Pennsylvania. Quercus is a dominant genus in many forests worldwide with importance to C sequestration and ecosystem function (Catovsky and Bazzaz, 2000), with well-established genetic and environmental basis for morphology and leaf chemistry that influence herbivore susceptibility (Schultz and Baldwin, 1982, Byington et al., 1994, Stowe et al., 1994, Eliason and Potter, 2000). Specifically, we determined (1) how N addition affects the susceptibility of Q. rubra to herbivores, (2) whether increased herbivore damage decreases growth of Q. rubra, and (3) how the impact of N addition to herbivore susceptibility and plant height growth varies with tree family and geographically separated locations.