Above‐ and belowground insect herbivory modifies the response of a grassland plant community to nitrogen eutrophication

Abstract

Understanding the role that species interactions play in determining the rate and direction of ecosystem change due to nitrogen (N) eutrophication is important for predicting the consequences of global change. Insects might play a major role in this context. They consume substantial amounts of plant biomass and can alter competitive interactions among plants, indirectly shaping plant community composition. Nitrogen eutrophication affects plant communities globally, but there is limited experimental evidence of how insect herbivory modifies plant community response to raised N levels. Even less is known about the roles of above- and belowground herbivory in shaping plant communities, and how the interaction between the two might modify a plant community's response to N eutrophication. We conducted a 3-yr field experiment where grassland plant communities were subjected to above- and belowground insect herbivory with and without N addition, in a full-factorial design. We found that herbivory modified plant community responses to N addition. Aboveground herbivory decreased aboveground plant community biomass by 21%, but only at elevated N. When combined, above- and belowground herbivory had a stronger negative effect on plant community biomass at ambient N (11% decrease) than at elevated N (4% decrease). In addition, herbivory shifted the functional composition of the plant community, and the magnitude of the shifts depended on the N level. The N and herbivory treatments synergistically conferred a competitive advantage to forbs, which benefited when both herbivory types were present at elevated N. Evenness among the plant species groups increased when aboveground herbivory was present, but N addition attenuated this increase. Our results demonstrate that a deeper understanding of how plant-herbivore interactions above and below ground shape the composition of a plant community is crucial for making reliable predictions about the ecological consequences of global change.

Effects of Soil Organisms on Aboveground Plant-Insect Interactions in the Field: Patterns, Mechanisms and the Role of Methodology

“…In field studies, plant-mediated effects of coleopteran root herbivores on aboveground chewing herbivores can be neutral (Hunt-Joshi et al, 2004;Barber et al, 2015;Borgström et al, 2017), positive (Wurst et al, 2008), or negative (White and Andow, 2006;Wurst et al, 2008;Megías and Müller, 2010, see Figure 2D, Supplementary Table 4). Interestingly, on ribwort plantain, Plantago lanceolata that were exposed to belowground herbivory by Agriotes spp., aboveground herbivory levels were three times lower on a high-iridoid glycoside (secondary defense metabolites in Plantago) producing lineage, compared to controls without root herbivores.…”

Above‐ and belowground insect herbivores mediate the impact of nitrogen eutrophication on the soil food web in a grassland ecosystem

“…of Agricultural Sciences,PO Box 7044, Uppsala, Sweden. Borgström et al 2017), thereby influencing nutrient turnover (Belovsky and Slade 2000). In addition, through their influence on induced plant defences, foliar-and root-feeding insects may also impact each other's performance in different ways (Masters et al 1993, Johnson et al 2012, as well as the performance and abundances of other functionally important invertebrates, such as those that play a part in determining nutrient turnover rates (De Deyn et al 2007).…”

“…When herbivory effects propagate to such central players in the soil food web, it may have important implications for functioning of the whole ecosystem. The impact of herbivory on a plant community, and consequently on the whole ecosystem, is in turn often dependent on abiotic factors, such as nutrient availability (Olff and Ritchie 1998, Von Euler et al 2014, Borgström et al 2017. Here, we investigated how insect herbivory alters the functional composition of the soil nematode community in the context of nitrogen (N) eutrophication, a major global change driver (Bobbink et al 2010, Stevens et al 2010.…”

“…Combined above and belowground insect herbivory can cause non-additive shifts in the composition of the plant community (van Ruijven et al 2005, Borgström et al 2017, making the response of the nematode community hard to predict. In a previous study, aboveground herbivory from grasshoppers reduced the total aboveground plant biomass as a result of a reduction in the biomass of grasses and an increase in the biomass of forbs, but only in the presence of belowground herbivory (Borgström et al 2017). Since increased plant biomass often confers increased bacterial biomass (Bardgett et al 1999, Broughton andGross 2000), one would expect an increase in plant biomass to result in an increase in the abundance of bacterial-feeding nematodes.…”

“…Nitrogen eutrophication can dramatically alter the composition of plant communities, most often by reducing the number of plant species (Cleland and Harpole 2010). In addition, the impacts of the interplay between above-and belowground herbivory on the plant community can become more pronounced at elevated N. For example, the effect of belowground insect herbivory turned from neutral at ambient N to amplifying the effect of aboveground herbivory and reinforcing the advantage of forbs over grasses at elevated N (Borgström et al 2017). Consequently, such knock-on effects on soil nematodes might also be more pronounced at elevated N. Besides being affected by N induced changes of the plant community, soil nematode communities can also show complex direct responses to changes in soil N levels; N addition can reduce generic richness of nematodes (Ruan et al 2013, Song et al 2016), but also decreased N input can reduce the abundance and diversity of root-feeding nematodes (Verschoor et al 2001, Ruan et al 2013).…”