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Stoichiometric Relations in an Ant-Treehopper Mutualism

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Stoichiometric Relations in an Ant-Treehopper Mutualism Ecology Letters, (2004) 7: 1024–1028 doi: 10.1111/j.1461-0248.2004.00667.x IDEAS AND PERSPECTIVES Stoichiometric relations in an ant-treehopper mutualism Abstract Adam D. Kay,1* Sara E. Scott,2 Carbon : nitrogen : phosphorus (C : N : P) stoichiometry can underlie physiological John D. Schade3,4 and and life history characteristics that shape ecological interactions. Despite its potential Sarah E. Hobbie1 importance, there is much to learn about the causes and consequences of stoichiometric 1 Department of Ecology, variation in terrestrial consumers. Here we show that treehoppers (Publilia modesta) Evolution and Behavior, tended by ants (Formica obscuripes) contained lower N concentrations than treehoppers on University of Minnesota, 100 plants from which ants were excluded. Ant presence also affected nutrient concentra- Ecology Building, 1987 Upper tions in host plants: on plants with ants, leaves contained uniformly low concentrations Buford Circle, St Paul, MN of N; on plants without ants, N concentrations were low only in the few leaves fed upon 55108, USA 2Department of Biology, by treehoppers at the time of collection. We suggest treehopper feeding reduces leaf College of St Benedict, St nutrient levels and ants positively affect treehopper abundance, producing a top–down Joseph, MN, USA effect on plant quality. Determining the causes of these stoichiometric changes should 3School of Life Sciences, Arizona help elucidate factors guiding the dynamics of conditional mutualisms between ants and State University, Tempe, AZ, homopterans. USA 4Department of Integrative Keywords Biology, University of California, Ants, conditional, membracid, mutualism, nitrogen, phosphorus, Publilia, Solidago, Berkeley, CA, USA stoichiometry, treehoppers. *Correspondence: E-mail: [email protected] Ecology Letters (2004) 7: 1024–1028 Here, we investigate how ant attendance affects the size INTRODUCTION of aggregations of the treehopper, Publilia modesta, and the Outcomes of conditional mutualisms often depend on carbon : nitrogen : phosphorus (C : N : P) stoichiometry varying ecological factors (Bronstein 1994, 2001; Herre et al. of P. modesta individuals. Stoichiometry can underlie traits 1999). Such conditionality is thought to be widespread in that affect how organisms interact with their environment ant-homopteran mutualisms (Cushman & Addicott 1991), in (Sterner & Elser 2002): one example is the causal which homopterans produce excretions (ÔhoneydewÕ) col- relationship between P concentration and growth rate. lected by ants, and ants provide protection or other services. Although this relationship is taxonomically widespread Ant attendance can positively affect the size of a homop- (Elser et al. 2003), little is known about patterns, causes, teran aggregation (number of individuals on a host plant) or consequences of stoichiometric variation in most depending on several factors including ant abundance terrestrial consumers. (Cushman & Whitham 1991; Morales 2000) and natural Ant attendance could affect treehopper stoichiometry by at enemy levels (Bristow 1984). Ant attendance can also least two mechanisms. First, ant presence could lead to an influence characteristics of individual homopterans such as increase in P in treehoppers if ant protection creates growth rate (Bristow 1984; Stadler & Dixon 1998) by conditions for rapid growth, and growth rate in treehoppers inducing changes in feeding behaviour (Banks & Nixon is tied to body P concentration. When tended by ants, some 1958) and the quantity or quality of honeydew that homopterans increase feeding rates (Banks & Nixon 1958) homopterans produce (Yao & Akimoto 2001). Discovering and may grow faster (El-Ziady 1960; Bristow 1984; Flatt & these individual-level effects, and determining their causes Weisser 2000); however, nothing is known about how such and consequences, may elucidate mechanisms underlying changes are related to homopteran stoichiometry. Second, ant the distribution and strength of ant-homopteran associa- attendance could decrease N and P concentrations in tions. treehoppers if treehoppers produce more nutrient-rich Ó2004 Blackwell Publishing Ltd/CNRS Ants affect treehopper stoichiometry 1025 honeydew when ants are present. Ants can induce changes in We used repeated-measures ANOVA to determine whether the production rate or sugar composition of honeydew ant presence affected treehopper aggregation size. To (Fischer & Shingleton 2001), but little is known about how control for initial differences in aggregation sizes, the ants affect honeydew N and P concentrations. However, repeated measure was treehoppers on a plant divided by N-rich honeydew may help treehoppers attract ants because the maximum number of treehoppers on that plant during many ants are particularly responsive to amino acid levels in the experiment. These proportions were arcsine trans- honeydew-like substances (Kay 2002). In this study, we show formed for analysis. We used nested ANOVAs to compare that ant presence decreases the concentration of N, but not of leaf and treehopper chemistry (with plants nested within ant C or P, in treehoppers. We also show that ant presence is treatment). associated with an overall reduction in leaf N concentrations, which we argue results from treehopper feeding. RESULTS Treehopper aggregation sizes were largest in the initial METHODS survey (mean ± SE for all plants ¼ 178.5 ± 31.9) and We conducted field work at Cedar Creek (Anoka County), declined thereafter. Over the course of the experiment, MN, USA. Publilia modesta feeds on a variety of plants, but aggregation size decreased more on plants without ants than was found only on Solidago gigantea at our study site. Eggs are on control plants (Fig. 1; time · treatment interaction: laid on host plants early in the growing season and emerging F6,36 ¼ 3.26, P ¼ 0.012; final means: plants without nymphs apparently rarely leave their natal plant before ants ¼ 36.8 ± 15.8, control plants ¼ 150.3 ± 16.1). In the becoming adults (Morales 2000). Throughout the western final survey, the percentage of leaves with treehoppers was United States, P. modesta has only a single generation per year significantly lower on plants without ants than on control (Kopp & Yonke 1973). Nymphs in our study fed primarily plants (28 ± 10% vs. 89 ± 2%; v2 ¼ 5.33, d.f. ¼ 1, P ¼ by piercing leaves (rarely through stems). 0.021), but the number of treehoppers on those leaves did On 23 July 2003, we chose eight S. gigantea ramets not differ between groups (9.1 ± 4.0 vs. 6.8 ± 0.4; t-test (hereafter ¼ plants) that had large numbers of P. modesta with unequal variances: t ¼ 0.55, d.f. ¼ 3, P ¼ 0.61). We tended by ants. We haphazardly divided plants into an never observed adult treehoppers on our plants during the experimental and a control group (n ¼ 4). We removed all experiment. ants from experimental plants, and applied sticky trap Treehoppers had significantly higher N concentrations on (Tanglefoot) to the base of stems to prevent ants from plants without ants than on control plants; treehopper C and P returning. We clipped a small amount of mostly senesced concentrations did not differ between groups (Fig. 2). vegetation that provided ants with access to experimental Differences in N concentration between groups were not plants; similar amounts of vegetation were removed around explained by body mass differences. Although dry mass was control plants. We counted treehoppers on each plant after weakly (negatively) correlated with N concentration (log–log initiating the experiment and every 3–4 days thereafter for relationship; r2 ¼ 0.34, d.f. ¼ 31, P ¼ 0.056), treehopper 24 days. After 24 days, we separately collected each leaf (and any treehoppers on the leaf) from each plant. 140 With ants We conducted tissue analyses on samples dried at 60 °C 120 No ants for 48 h. We analysed subsamples of ground leaves and 100 whole treehoppers for carbon and nitrogen concentrations 80 using a Perkin–Elmer 2400 CHN analyser (Perkin–Elmer, Wellesley, MA, USA), and phosphorus concentration using 60 Treehoppers persulfate digestion and ascorbate–molybdate colorimetry. 40 We estimated soluble protein concentration in treehoppers 20 using the direct Lowry procedure (Sigma, St Louis, MO, (% of highest number counted) 0 USA), which involves colorimetry on a sample combined 0 3 6 9 1215182124 with an alkaline cupric tartrate reagent. In the phosphorus Day and soluble protein assays, treehoppers were gently crushed Figure 1 Abundance of Publilia modesta treehoppers over a 24-day with a Teflon-coated rod to expose tissues to reagents. In period as a function of the presence or absence of ants. To each assay, we analysed 3–5 haphazardly selected treehop- facilitate visual assessment of treatment differences, numbers of pers from each plant. We also analysed from each plant treehoppers for each plant were transformed to the percentage of three leaves with and three leaves without treehoppers on the highest number of treehoppers counted on that plant: data them at the time of our final census; we used all leaves in a points are the mean (± 1 SE) of those percentages for all plants in category when fewer than three existed. a treatment. Ó2004 Blackwell Publishing Ltd/CNRS 1026 A. D. Kay et al. 10 Leaves with treehoppers F = 17.22, P = 0.009 1,6 Leaves without treehoppers 9 3 b 8 2 a a a 7 1 Treehopper N (% dry mass) Leaf N (% dry mass) 6 0 60 F1,6 = 0.89, P = 0.389 0.4 a 55 a 0.3 a a 50 0.2 45 0.1 Treehopper C (% dry mass) Leaf P (% dry mass) 40 0.0 1.2 F = 0.08, P = 0.783 1,6 20 a 1.1 a a 15 b 1.0 10 0.9 5 Leaf N : P (molar ratio) Treehopper P (% dry mass) 0 0.8 With ants No ants With ants No ants Treatment Treatment Figure 2 Mean (± 1 SE) N, C and P concentrations in the tissue of Figure 3 Mean (± 1 SE) N concentration (% of dry mass), treehopper nymphs after a 24-day period in the presence or P concentration (% of dry mass), and N : P molar ratio in leaves of absence of ants.
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