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The Effects of Long-Term Nitrogen Loading on Grassland Insect Communities

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The Effects of Long-Term Nitrogen Loading on Grassland Insect Communities Oecologia (2000) 124:73–84 © Springer-Verlag 2000 Nick M. Haddad · John Haarstad · David Tilman The effects of long-term nitrogen loading on grassland insect communities Received: 18 May 1999 / Accepted: 5 January 2000 Abstract Just as long-term nitrogen loading of grass- plant communities, insect species richness, abundance, lands decreases plant species richness and increases and composition were impacted by nitrogen addition. plant biomass, we have found that nitrogen loading de- This study demonstrates that long-term nitrogen loading creases insect species richness and increases insect abun- affects the entire food chain, simplifying both plant and dances. We sampled 54 plots that had been maintained at insect communities. various rates of nitrogen addition for 14 years. Total in- sect species richness and effective insect diversity, as Key words Insect communities · Productivity · well as herbivore and predator species richness, were Diversity · Abundance · Nitrogen loading significantly, negatively related to the rate of nitrogen addition. However, there was variation in trophic re- sponses to nitrogen. Detritivore species richness in- Introduction creased as nitrogen addition increased, and parasitoids showed no response. Insect abundances, measured as the Humans have greatly altered the global nitrogen cycle, number of insects and insect biovolume (an estimate of increasing the rate and magnitude of nitrogen deposition biomass), were significantly, positively related to the rate (Vitousek et al. 1997). Among its many environmental of nitrogen addition, as were the abundances of herbi- consequences, long-term nitrogen loading decreases vores and detritivores. Parasitoid abundance was nega- plant species richness, increases standing crop biomass, tively related to the rate of nitrogen addition. Changes in and shifts plant composition to a few dominant species the insect community were correlated with changes in (Bakelaar and Odum 1978; Tilman 1987, 1988; Aerts the plant community. As rates of nitrogen addition in- and Berendse 1988; Inouye and Tilman 1988, 1995; creased, plant species richness decreased, plant produc- Huenneke et al. 1990; Pysek and Leps 1991). Such plant tivity and plant tissue nitrogen increased, and plant com- community responses to nitrogen loading may impact position shifted from C4 to C3 grass species. Along this the rest of the food chain, but there are few studies of gradient, total insect species richness and effective insect the consequences of long-term nutrient loading on terres- diversity were most strongly, positively correlated with trial trophic structure. Responses of terrestrial food plant species richness. Insect biovolume was negatively chains to nutrient loading may be similar to responses of correlated with plant species richness. Responses of indi- aquatic food chains, where phosphorus loading increases vidual herbivores varied along the nitrogen gradient, but algal productivity and shifts algal, zooplankton, insect, numbers of 13 of the 18 most abundant herbivores were and fish community composition (Mundie et al. 1991; positively correlated with their host plant biomass. Al- Lathrop and Carpenter 1992; Peterson et al. 1993; Perrin though insect communities did not respond as strongly as and Richardson 1997; Carpenter et al. 1998). Here, we test the hypothesis that long-term nitrogen N.M. Haddad · J. Haarstad · D. Tilman loading impacts insect communities much as it impacts Department of Ecology, Evolution, and Behavior, plant communities, causing lower insect species richness, 1987 Upper Buford Circle, University of Minnesota, higher insect abundances (both numbers of insects and St. Paul, MN 55108, USA biomass), and shifts in insect species composition. Be- Present address: cause inputs of limiting nutrients simultaneously affect N. Haddad, Department of Zoology, Box 7617, plant species richness, plant productivity, plant composi- North Carolina State University, Raleigh, NC 27695-7617, USA, tion, and plant tissue quality, separating their independent e-mail: [email protected], effects on insect communities can be difficult (Siemann Tel.: +1-919-5154588, Fax: +1-919-5155327 1998). In some cases, attributes of insect communities re- 74 spond similarly to changes in plant species richness, plant To better understand insect responses to long-term nu- productivity, plant composition, and plant tissue quality trient addition, we evaluated the diversity and abundance along nitrogen gradients. For example, high nitrogen in- of insects along a nitrogen addition gradient that had put should increase insect abundances because these in- been experimentally maintained for 14 years (Tilman crease as plant species richness decreases, as plant pro- 1987, 1988, 1996). We analyzed the responses of insect ductivity increases, and as plant composition shifts to a species richness and abundance (both the number of in- few dominant plant species with high tissue quality sects and biovolume, an approximation of biomass) to (Pimentel 1961; Tahvanainen and Root 1972; Root 1973; the rate of nitrogen input, which was the direct experi- Hurd and Wolf 1974; Vince et al. 1981; Strauss 1987; mental manipulation. In addition, to gain insights into Sedlacek et al. 1988; Andow 1991; Siemann 1998). Nu- the factors that might have contributed to insect respons- merous studies have shown that nitrogen fertilization in- es to nitrogen addition, we used multiple regressions to creases tissue quality for many insect species by increas- try to identify the influences of plant species richness, ing plant tissue nitrogen, soluble nitrogen, and amino acid plant productivity, plant composition, and plant tissue ni- concentrations, and fertilized plants can then support trogen on insect communities. Clearly, such analyses are larger insect population sizes (e.g., McNeill and South- not as definitive as analyses based solely on manipulated wood 1978; Mattson 1980; Scriber and Slansky 1981; variables, but they might provide insights into responses Scriber 1984; Strong et al. 1984; Nordin et al. 1998). of the insect community. We controlled for spatial effects The effects of nitrogen addition on insect diversity are on local diversity that might result from the small size more complicated because changes in the plant commu- and proximity of our experimental plots. Because nutri- nity may have opposing effects on insect species rich- ent addition may alter trophic interactions between in- ness. When nitrogen input is high, the resulting lower sects (Siemann 1998), we also controlled for the effects plant species richness should decrease insect species of trophic interactions on species richness and abun- richness because the diversity of resources for insect dance at each trophic level. specialists is lower (Murdoch et al. 1972; Nagel 1979; Siemann et al. 1998; Knops et al. 1999). But nitrogen in- puts should also increase plant productivity, which Methods should increase the availability of insect resources and increase the number of insect individuals and possibly Nitrogen addition experiment the number of insect species (Hurd et al. 1971; Hurd and Wolf 1974; Kirchner 1977; Vince et al. 1981; but see The experiment was conducted at Cedar Creek Natural History Area, which is located in Isanti and Anoka Counties in east-central Prestidge 1982; Sedlacek et al. 1988; Siemann 1998). In Minnesota, in field C described in Tilman (1987, 1988). The field addition, fertilized plants with higher tissue quality was abandoned from agriculture in 1935. Beginning in 1982, the should be resources for a greater number of generalist field was fenced above- and belowground to exclude non-insect herbivore species and individuals (Mattson 1980; herbivores and divided into 54 4×4 m plots, each separated from Prestidge and McNeill 1983a; Strauss 1987; Nordin et al. adjacent plots by 1 m on each side and by aluminum flashing bur- ied to a depth of 25 cm. The completely randomized design in- 1998). Thus, the effects of nutrient addition on insect cluded nine treatments – six replicates each of a control (no nutri- communities are potentially complex and interrelated. ents added), and eight treatments that received a mixture of P, K, –2 Results of previous studies along experimental nitrogen Ca, Mg, S, and trace metals (achieved by adding 10 g·m P2O5 –2 –2 –2 gradients illustrate difficulties in predicting insect commu- and K2O, 15 g·m MgSO4, 20 g·m CaCO3, and 0.0625 ml·m trace metals), and nitrogen in amounts of 0.0, 1.0, 2.0, 3.4, 5.4, nity responses to nitrogen loading. In these studies, data 9.5, 17.0, or 27.2 g·m–2·year–1. were collected 1–2 years after nitrogen manipulations (Hurd et al. 1971; Hurd and Wolf 1974; Kirchner 1977; Sedlacek et al. 1988; Siemann 1998). Each reported that Plant community responses higher nitrogen input increased insect species richness. Detailed descriptions of plant species richness, plant productivity, These results are consistent with the prediction that nitro- plant composition, and plant community stability in these plots are gen input increases plant productivity and tissue quality, presented in Tilman (1987, 1988, 1993, 1996), Inouye and Tilman which increases insect species richness, but contrast with (1988, 1995), and Tilman and Downing (1994). Vegetation in low- the prediction that nutrient addition decreases plant spe- nitrogen plots was composed of perennial bunch grasses, primarily Schizachyrium scoparium, and forbs, including Artemisia ludo- cies richness, which would then decrease insect species
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