Biogeochemical flows, especially those of nitrogen (N) and phosphorous (P), are being greatly affected by anthropic activity, affecting ecosystems worldwide (Steffen et al., 2015). While N is a limiting nutrient for plants in most environments, human-driven increases in its availability is leading to biodiversity losses and changes in ecosystem functioning (Bobbink et al., 2010). Yet, most studies that evaluate the impacts of ongoing terrestrial eutrophication tend to focus on community-level patterns of primary producers (Bobbink et al., 2010; Stevens et al., 2018), while only a few studies investigate the inter-specific variability of such effects and the propagation of these impacts to higher trophic levels (but see Chen et al., 2010; Pöyry et al., 2017; Stevens et al., 2018; David et al., 2019). Such gap of knowledge is particularly accentuated in tropical regions and can limit our ability to predict the impacts of global changes and plan adequate management actions.
Tropical ecosystems, such as the Cerrado, have ancient geological formations with advanced soil weathering processes, limiting the development and productivity of its vegetation by the low availability of nutrients in the soil, mainly N and P (oligotrophic soils, Bustamante et al., 2006; Haridasan, 2008). Many species in these environments have specific and energetically costly strategies that increase access to soil nutrients (e.g., root structures like root dimorphism, resorption of nutrients before leaf senescence and symbioses with microorganisms; Haridasan, 2008; Oliveira et al., 2015). These strategies require a substantial investment and can result in less investment of plants in above-ground growth (Hoffmann & Franco, 2003; Lambers et al., 2020). Hence, in a scenario of increased nutrient availability, the negative impacts on plants above-ground growth may be more accentuated in these oligotrophic and highly biodiverse tropical ecosystems (e.g., Lambers et al., 2020). Change in plant quality induced by increased N availability is more pronounced in soils co-limited by N and P. Indeed, increased N availability tends to increase P limitation both in plants and their consumers (Vogels et al., 2023). Understanding the diversity of responses of plant trees in oligotrophic soils (e.g., Cerrado) to changes in nutrient soil levels is essential to better predict impacts of global environmental changes and to define adequate conservation and restoration practices.
Effects of increased N availability can vary between plant species depending on their nutritional requirements. In a scenario of increased nutrient availability, plant species adapted to N rich soils (nitrophilous) can better take advantage of such increase than species that are adapted to oligotrophic soils (nitrophobous) (Bobbink et al., 2010; Stevens et al., 2018). Such, N-driven changes in plant species composition (i.e., abundance, richness, evenness) will hence affect the availability of resources for primary consumers, such as abundance of leaves (Throop & Lerdau, 2004; Stevens et al., 2018). Another important pathway through which eutrophication can affect plant consumers is through changes in the nutritional quality of plant resources. Plant species naturally differ in their primary (e.g., protein and carbohydrate; Wilson et al., 2019) and secondary (e.g., alkaloids; Kessler & Kalske, 2018) compound content, and such variability is known to influence primary consumers performance and fitness (Throop & Lerdau, 2004; Nijssen et al., 2017; Stevens et al., 2018). The concentration of such compounds in leaves is affected by changes in soil N availability, especially when P is not a factor limiting N fixation (Throop & Lerdau, 2004, Vitousek et al., 2010), changing how herbivores perceive the quality of the plant as a food resource. Indeed, several amino acids necessary for herbivore growth and reproduction are solely obtained through diet (i.e., are essential amino acids), thus, an increase in N soil levels can change the quality and palatability of plants as a food resource (Throop & Lerdau, 2004; Li et al., 2016; Stevens et al., 2018). Furthermore, increasing N supply, can also significantly decrease concentrations of secondary C-based compounds (e.g., polyphenolics and phenolics), which act as herbivory defenses, reducing plant resistance to herbivory (Chen & Ni, 2011; Sun et al., 2020). Consequently, such N-driven effects are likely to make the plant more susceptible to herbivory (Throop & Lerdau, 2004; Li et al., 2016; Stevens et al., 2018).
The effects of changes of soil N content in plants and herbivores can also propagate to higher trophic levels, e.g., changing the susceptibility of herbivorous insects to their natural enemies (i.e., predators, parasitoids, and pathogens; Throop & Lerdau, 2004) or changing the production of plant’s volatile defense compounds that act as foraging signals for natural enemies (Chen & Ni, 2011). However, there is still little information on how changes in soil nutrient levels propagate from plants to herbivores and predators, particularly in tropical ecosystems.
In this work, we used a controlled fertilization experiment to investigate the impacts of soil nutrient changes on plant resource, herbivory, and predation in six tree species that naturally occur in the Cerrado biome, but also occurring in other biomes with richer soils. Since the experimental plants were not exposed to competition with other plants, we expected that, moderated N increases would lead to a positive effect on plant aerial biomass, these effects being more accentuated when P is not a limiting factor (expectation 1). We also expected herbivores to prefer plants grown in soils with moderate levels of N added than plants grown in low levels of N, these effects cascading to herbivore natural enemies (expectation 2). On the other hand, above certain thresholds of N and P levels, the plant may suffer a nutritional imbalance or start to invest more in toxic compounds (Throop & Lerdau, 2004; Chen et al., 2010), reducing the herbivores and their natural enemies (expectation 3).