Estuaries and Coasts (2012) 35:475–485 DOI 10.1007/s12237-011-9458-7

Effects of an Omnivorous Katydid, Salinity, and Nutrients on a Planthopper-Spartina Food Web

Juan M. Jiménez & Kazimierz Więski & Laurie B. Marczak & Chuan-Kai Ho & Steven C. Pennings

Received: 25 May 2011 /Revised: 19 October 2011 /Accepted: 22 October 2011 /Published online: 21 December 2011 # Coastal and Estuarine Research Federation 2011

Abstract Top–down and bottom–up effects interact to contrast, top–down control by Orchelimum of Prokelisia was structure communities, especially in salt marshes, which independent of bottom–up conditions. Orchelimum grew contain strong gradients in bottom–up drivers such as best on a diet containing both Spartina and Prokelisia,andin salinity and nutrients. How omnivorous consumers respond contrast to a sympatric omnivorous crab, did not shift to an to variation in prey availability and plant quality is poorly animal-based diet when prey were present, suggesting that it understood. We used a mesocosm experiment to examine is constrained to consume a mixed diet. These results suggest how salinity, nutrients, an omnivore (the katydid Orchelimum that the trophic effects of omnivores depend on omnivore fidicinium) and an herbivore (the planthopper Prokelisia behavior, dietary constraints, and ability to suppress lower spp.) interacted to structure a simplified salt marsh food web trophic levels, and that omnivorous katydids may play a based on the marsh grass Spartina alterniflora. Bottom–up previously unrecognized role in salt marsh food webs. effects were strong, with both salinity and nutrients decreasing leaf C/N and increasing Prokelisia abundance. Keywords Top–down and bottom–up interactions . Top–down effects on plants were also strong, with both the Orchelimum fidicinium . Omnivory. Prokelisia spp. . herbivore and the omnivore affecting S. alterniflora traits Salt marsh . Spartina alterniflora and growth, especially when nutrients or salt were added. In

Introduction

Electronic supplementary material The online version of this article (doi:10.1007/s12237-011-9458-7) contains supplementary material, Herbivores play a central role in community structure because which is available to authorized users. they both support higher trophic levels and regulate plant community structure and biomass; however, understanding J. M. Jiménez : K. Więski : L. B. Marczak : C.-K. Ho : S. C. Pennings (*) what regulates herbivore abundance is complicated. Department of Biology and Biochemistry, University of Houston, Herbivore densities can be affected by top–down forcing Houston, TX 77204-5001, USA from predators (Oksanen et al. 1981), side-to-side forces e-mail: [email protected] from competitors (Moon and Stiling 2002)andbottom–up Present Address: forcingbyplants(HunterandPrice1992). Because these L. B. Marczak potential drivers can interact in many ways, the study of Department of Ecosystem and Conservation Sciences, herbivore population dynamics is a challenging task College of Forestry and Conservation, University of Montana, (Power 1992;Strong1992). Missoula, MT 59812, USA In salt marshes, the strong abiotic gradients that occur Present Address: across the marsh in flooding and salinity, and the variation C.-K. Ho in nutrient input that different estuaries receive from natural Institute of Ecology and Evolutionary Biology, or anthropogenic sources, can all be important bottom–up National Taiwan University 1, Sec. 4, Roosevelt Rd., factors regulating plant biomass and performance (Pennings Taipei 106 Taiwan, Republic of China and Bertness 2001). A number of studies have examined 476 Estuaries and Coasts (2012) 35:475–485 how top–down and bottom–up forces interact to regulate indirectly increasing plant size by eating herbivores, leading the abundance of herbivores in salt marshes (Bertness et al. to weak net effects. Moreover, we hypothesized that both 2008; Sala et al. 2008). In particular, top–down control of nutrient addition and salinity stress would reduce top–down planthopper herbivores on Borrichia shrubs in Florida control of Prokelisia spp. by O. fidicinium by decreasing the saltmarshes is decreased by abiotic stress and increased by C/N ratio of plants (making plants a more attractive alternate eutrophication (Moon and Stiling 2000, 2002, 2004). diet for O. fidicinium) and increasing Prokelisia spp. Similarly, top–down control of planthopper herbivores on abundance (leading to herbivore escape from control by O. Spartina alterniflora grasses in New Jersey saltmarshes is fidicinium). Third, we compared our results with those of a mediated by interactions between nutrients and spider similar study by Ho and Pennings (2008)ofanomnivorous abundance, with Prokelisia spp. able to achieve very high crab feeding on aphids and a salt marsh shrub to test the densities when plant nutrition is high and predators rare, hypothesis that these two omnivores would have similar conditions typical of tall-form S. alterniflora plants along effects on trophic structure. creek edges (Denno et al. 2002, 2003, 2005; Wimp et al. 2010). These studies and others have laid a foundation for Methods understanding how top–down and bottom–up factors interact to structure communities. These studies, however, S. alterniflora (hereafter, Spartina) is the most common salt examined food webs where the top consumers were marsh plant on the Atlantic and Gulf coasts of the USA, obligate predators and parasitoids, feeding solely on dominating lower and middle marsh elevations (Pennings herbivores. Both intraguild predators and true omnivores, and Bertness 2001). Spartina stands are exposed to wide however, are common in natural communities in general gradients of nutrient availability, flooding, and salinity. (Polis and Strong 1996) and in salt marshes in particular These gradients are partly responsible for the occurrence of (Buck et al. 2003; Ho and Pennings 2008; Wason and different height forms of S. alterniflora (Pennings and Pennings 2008). A few studies have examined the trophic Bertness 2001), with shorter plants (10–40 cm in height) effects of intraguild predators, finding that intraguild occupying higher marsh elevations than taller plants (1–2m predators often interfere with each other, weakening trophic in height), which have a higher nitrogen content and cascades (Finke and Denno 2004, Matsumura et al. 2004). dominate lower marsh elevations. At a given elevation, Less is known about the trophic effects of true omnivores, plants exposed to high salinities may respond by increasing which feed on both animals and plants (Eubanks 2005). production of nitrogen-based compounds to reduce osmotic Because true omnivores feed on both plants and animals, stress (Morris 1984), potentially increasing plant quality for they might respond to bottom–up changes in plant quality herbivores. by shifting their diet to include more or less plant material. The most common herbivores of Spartina are the As a result, their trophic impacts might differ considerably delphacid planthoppers P. marginata Van Duzee and P. from those of strict predators (Bruno and O’Connor 2005; dolus Wilson (Denno et al. 1987). P. marginata and P. Long et al. 2011), limiting our ability to construct dolus (hereafter, Prokelisia) are multivoltine, with a nomothetic theories of ecosystem structure. summer generation time of 5–6 weeks (Denno et al. 1985; In this paper, we examine how salinity and nutrient Stiling et al. 1991). They are phloem sap-feeders that can supply interact with the abundance of Orchelimum fidicinium reach densities of up to 1,000 adults and 100,000 nymphs/m2 Rehn and Hebard, an omnivorous katydid, to regulate the (Denno et al. 1987). abundance of Prokelisia spp. (Prokelisia marginata Van ThemostcommontrueomnivoreintheSpartina Duzee and Prokelisia dolus Wilson)herbivoresfeedingon zone of salt marshes on the southeastern coast of the the salt marsh grass S. alterniflora Loisel in Georgia salt United States is the tettigoniid katydid O. fidicinium marshes (Electronic Supplementary Material). We tested (hereafter, Orchelimum)(Smalley1960; Wason and Pennings three groups of hypotheses. First, we hypothesized that 2008). Although historically regarded as an herbivore (Teal nutrient addition would directly increase Prokelisia spp. 1962), Orchelimum, like most tettigoniids, is omnivorous, herbivore populations by increasing plant nitrogen content. and readily eats small arthropods. For example, individual Similarly, because S. alterniflora uses nitrogenous com- Orchelimum ate 7.8 Prokelisia planthoppers individuals per pounds for osmoregulation, we hypothesized that salinity day (SE, 1.4; n=10) when housed in 1-L jars for 48 h in the stress would also increase plant nitrogen content and laboratory (Wason and Pennings, personal observations) and Prokelisia spp. populations. Second, because O. fidicinium grew to adulthood when fed a diet consisting only of is omnivorous, eating both plants and herbivores, we Prokelisia (see “Results”). Orchelimum is univoltine, with hypothesized that it would have opposing effects on plant adult densities reaching 9.6 individuals/m2 (Smalley 1960; size, directly reducing plant size by eating plants, and Stiling et al. 1991). Estuaries and Coasts (2012) 35:475–485 477

Experimental work was done in mesocosms on Sapelo analyze variation in Orchelimum damage, and did not Island, GA (81.2699° W, 31.3929° N). Two hundred consider final leaf number a useful indicator of plant size. Spartina plants (~120 cm tall) were collected from the We calculated plant growth as the difference between initial Dean Creek salt marsh at the southern end of the island in and final plant height. As indicators of leaf quality, we late June, 2005, and potted in 3.5-L plastic pots in 50:50 measured chlorophyll content using an optical meter potting soil/sand. After 20 days, 112 healthy plants were (Opti-Sciences CCM-200 chlorophyll meter) and leaf haphazardly assigned to four combinations of nutrients toughness using a penetrometer (model 516, Chatillon (ambient and fertilized) and salinity (low and high) and N.Y.) at the end of the experiment. Leaf chlorophyll content acclimated for 7 weeks. Nutrient and salinity treatments was negatively correlated with leaf C/N ratio (n=80, r=0.61, were initiated with low doses (5 g) of nitrogen-based P<0.0001), based on a subset of leaves collected at the end fertilizer (20:10:5 N/P/K fertilizer pellets, Forestry Suppliers) of the experiment (Perkin-Elmer 2400 CHN analyzer). and low salinity concentrations (10). Nutrient additions and Because we fixed Orchelimum density at one individual salinity levels were progressively increased every two weeks per cage, replacing individuals that died, we did not examine to final levels of 21 g of fertilizer per month and a salinity of bottom–up effects on Orchelimum. 25. These nutrient and salinity combinations were not Data were analyzed with four-way ANOVA using JMP. designed to mimic particular field situations, but rather to Nutrients, salinity, herbivore addition, and omnivore addi- affect plant traits sufficiently to test the hypothesis that tion were treated as fixed effects. C/N, chlorophyll content bottom–up conditions would alter top–down control. Both and Prokelisia abundance were log-transformed to improve treatments were sufficient to affect plant traits and herbivore normality and homoscedasticity. For clarity, we show only abundances (see “Results”). Plants were watered daily with significant effects in the figures (i.e., data are presented fresh or saline water and allowed to drain fully. pooled across non-significant terms). The omnivore (present/absent) and herbivore (present/ To examine multivariate relationships among the absent) treatments were combined in a factorial design with response variables, and to examine the generality of the nutrient and salinity treatments, for a total of 16 our results, we used structural equation modeling (SEM) treatment combinations (2 omnivore×2 herbivore×2 to compare a subset of our treatments (omitting the nutrient×2 salinity), with seven replicates each. Arthropods nutrient and salt addition treatment combinations) with were enclosed on a single Spartina plant in a 1.4-m high cage parallel treatments in a similar study of top–down made of fine cloth mesh. The cloth reduced PAR (photosyn- control by the omnivorous crab Armases cinereum of thetically available radiation) levels inside cages to ~70% of aphids and a salt marsh shrub (Ho and Pennings 2008). SEM ambient. Mesocosms were located outdoors under a plastic is a multivariate technique that allows one to examine the roof that sheltered them from direct rain but exposed them to strength of direct and indirect effects between causally ambient temperature and humidity conditions. Mesocosms related variables (Grace 2006). SEM is superior to ANOVA representing different treatment combinations were inter- for some analyses because it can consider variables (e.g., spersed to prevent any location effects. Prokelisia and herbivore damage to leaves) as both response variables and Orchelimum were collected from marshes around Sapelo simultaneously as drivers of other response variables. SEM Island. Treatments including Orchelimum contained a single starts with a construction of a path diagram based on a priori katydid; plants were checked daily and katydids that died known relationships in the system studied. In the next step, were replaced. Treatments including Prokelisia were initiated the parameters of the SEM model are estimated by scanning with 30 nymphs and supplemented weekly with 40 adults to the matrix of covariances from the source data over the represent immigrants (Denno et al. 1985). Examination of a hypothesized model. Finally, based on the estimated model subset of the Prokelisia individuals suggested that we parameters, a predicted matrix of covariances is calculated stocked 80% P. marginata and 20% P. dolus. anditsfitiscomparedwiththeobservedmatrix.As Once arthropods were stocked, the experiment ran for with multiple regression, the “best” SEM model can one month (26 August to 27 September 2005). At the end include some marginally-significant terms. Parameters of the experiment, we counted all the arthropods present on wereestimatedwithAMOS7.0usingthemaximum the plants. We measured several plant traits at the beginning likelihood method, and model fit was tested by the and end of the experiment. As indicators of plant size and likelihood chi-square value. herbivory, we measured plant height, leaf width, and the To determine the importance of an omnivorous diet to number of healthy and damaged leaves, scoring damage growth of Orchelimum,weconductedalaboratorygrowth from both Prokelisa (visible as yellow spots against the experiment. We collected 32 Orchelimum nymphs in early normal dark green leaves) and Orchelimum (visible as July of 2010 from the field at Sapelo Island. Individuals were missing leaf material). Because Orchelimum damaged every measured (live mass) and haphazardly assigned to four diet leaf of the Spartina plants when present, we could not treatments (n=8 reps/treatment): live Spartina (S), live 478 Estuaries and Coasts (2012) 35:475–485

Spartina and Prokelisia (SP), dead Spartina (D), and dead and Orchelimum on plants, especially when nutrients or salt Spartina plus Prokelisia (P). Orchelimum offered only dead were added and (3) strong top–down effects of Orchelimum Spartina did not feed and died within 10 days; therefore, this on Prokelisia. Comparison of these results with a parallel treatment was not considered further, and we considered the study of a crab-aphid-shrub food web indicated (4) that dead Spartina plus Prokelisia treatment to essentially be a katydids and crabs have different effects as top omnivores. Prokelisia only treatment (with the dead Spartina providing Finally, growth studies indicated (5) that Orchelimum grows a perch). Individual Orchelimum were housed in 1 L glass best on a mixed diet containing both plant and animal prey. jars, stocked with a single ~50-cm Spartina leaf that was Below, we present these results in this order. either live or dead, as appropriate. A small amount of fresh water was added daily to each replicate to maintain humidity. Bottom–up effects Both nutrient addition and salinity had The experiment was run indoors at ~25°C and a photoperiod strong bottom–up effects on Spartina and Prokelisia of 14:10. For treatments containing Prokelisia,additional (Table 1). Nutrient addition increased Spartina leaf Prokelisia adults and nymphs were added every 2 days. Live chlorophyll (Fig. 1a) and reduced leaf C/N ratios and dead Spartina leaves were also replaced every 2 days. (Fig. 1b). Nutrient addition decreased leaf toughness, but All diets were ad libitum, with food available in excess of only when Orchelimum was present (Fig. 1c). Either salt what Orchelimum consumed. Orchelimum were weighed or nutrient addition alone increased Prokelisia abundance weekly for five weeks. by ~75 % (Fig. 1d) and decreased leaf C/N by 17–36% (Fig. 1e); however, when both salt and nutrients were added in combination, leaf C/N did not decrease much Results further, and Prokelisia abundance did not increase further (significant salinity x nutrient interactions, Table 1). In the mesocosm experiment, we found (1) strong bottom– Finally, nutrient addition moderately decreased the num- up effects of nutrients and salt that affected both plants and ber of leaves damaged by Prokelisia (Fig. 1f). Across all Prokelisia, (2) strong top–down effects from both Prokelisia treatments with Prokelisia, the number of leaves damaged

Table 1 Summary of ANOVA results for the effects of salinity stress and their interactions on C/N ratio, chlorophyll content, leaf (low or high), nutrient availability (ambient or addition), herbivore toughness, plant growth, leaf width, Prokelisia abundance, and treatment (present or absent), omnivore treatment (present or absent) Prokelisia damage

Source P

C/N Chlorophyll Leaf Plant Leaf Prokelisia Prokelisia ratio content toughness growth width abundance damage

Salinity (S) 0.04 0.20 0.99 0.13 0.008 0.21 0.22 Nutrients (N) <0.0001 <0.0001 0.045 0.57 0.81 0.04 0.02 S*N 0.02 0.10 0.51 0.65 0.67 0.01 0.47 Herbivore (H) 0.14 0.005 0.001 0.59 0.37 NT NT S*H 0.09 0.18 0.78 0.46 0.14 NT NT N*H 0.04 0.01 0.14 0.52 0.81 NT NT S*N*H 0.76 0.69 0.48 0.02 0.017 NT NT Omnivore (O) 0.03 0.89 0.37 <0.0001 0.96 0.005 0.002 S*O 0.88 0.80 0.33 0.18 0.08 0.71 0.92 N*O 0.15 0.46 0.047 0.04 0.60 0.83 0.64 S*N*O 0.03 0.09 0.43 0.61 0.006 0.87 0.61 H*O 0.78 0.16 0.45 0.52 0.96 NT NT S*H*O 0.14 0.87 0.89 0.55 0.74 NT NT N*H*O 0.61 0.64 0.58 0.07 0.017 NT NT S*N*H*O 0.40 0.99 0.07 0.69 0.668 NT NT Initial number of leaves NS NS NS NT NT NS 0.008

Full ANOVA results are presented in digital Electronic Supplementary Material. Initial number of leaves was initially included as a covariate in tests where appropriate but dropped if not significant Significant p-values (<0.05) are indicated with italics NT not tested, NS not significant (and dropped from model) Estuaries and Coasts (2012) 35:475–485 479

Fig. 1 Bottom–up effects of nutrients and salinity, and interactions with presence of herbivorous Prokelisia planthoppers and omnivorous Orchelimum katydids, on plant a chlorophyll content, b C/N ratio, and c leaf toughness (in Newtons); interactive effects of nutrient and salinity on d Prokelisia abundance and e plant C/N ratio; bottom–up effects of nutrient addition on f the number of leaves damaged by Prokelisia; and g relationship between the number of leaves damaged by Prokelisia and leaf chlorophyll content (y=−0.5x+0.19, n=56, R2=0.16, P=0.002). H+ herbivore present, H− herbivore absent, O+ omnivore present, O− omnivore absent, S+ salt added, So no salt added; black bars, no nutrient addition (No); white bar: nutrient addition (N+). ANOVA statistics are reported in Table 1 and Electronic Supplementary Material. Data are means+1 SE

by Prokelisia decreased with increasing chlorophyll content (Fig. 1a) and increased C/N ratio when nutrients content (Fig. 1g), suggesting that Prokelisia needed to were added (Fig. 1b, significant nutrient x herbivore feed less extensively on nutrient-rich plants. There was no interactions, Table 1). Prokelisia reduced plant growth, interaction between salinity and nutrients for chlorophyll especially when nutrients and salt were both added content, leaf toughness or Prokelisia damage (Table 1). (Fig. 2b; salinity×nutrients×herbivore interaction, Table 1). Changes in leaf width depended on three way interactions Top–down Effects on Plants Prokelisia and Orchelimum between salt, nutrients, herbivores, and omnivores: leaf both had strong top–down effects on plants, and Orchelimum width decreased in all treatments when salt was added; also had a strong top–down effect on Prokelisia (next however, in the no salt treatment, leaf width increased paragraph); however, only the top–down effects on plants when either omnivores or herbivores were present and were mediated by bottom–up conditions (Table 1). Prokelisia nutrients were added (significant salinity×nutrients× reduced leaf toughness (Fig. 2a), and reduced chlorophyll omnivore and salinity×nutrients×herbivore interactions, 480 Estuaries and Coasts (2012) 35:475–485

– Fig. 2 Top down effects of No N+ herbivorous Prokelisia planthoppers and omnivorous 15 Orchelimum katydids and A C interactions with nutrients and 40 C:N Ratio salinity, on a leaf toughness (in 10 Newtons); b plant growth; c plant C/N ratio and d plant 20 growth. H+ herbivore present, 5 H− herbivore absent, O+ omnivore present, O− omnivore toughness (N)Leaf absent, S+ salt added, So no salt 0 0 added; black bars, no nutrient H- H+ O- O+ O- O+ addition (No); white bar, nutrient addition (N+). ANOVA So S+ statistics are reported in Table 1 and Electronic Supplementary

Material. Data are means+1 SE B D 15 Plant growth (cm) 15

10 10

5 5 Plant growth (cm) growth Plant

0 0 H- H+ H- H+ O- O+ So S+

Table 1). Orchelimum increased leaf toughness in unfertilized Pennings 2008)andOrchelimum indicated important treatments (Fig. 1c) and interacted with nutrients and salt to differences in the way that these two omnivores structure affect leaf C/N ratios: fertilization decreased all C/N ratios, their communities. SEM analysis of the mesocosm exper- but the largest fertilization effect occurred when Orchelimum was absent and salt was not added (Fig. 2c; significant 500 salinity×nutrient×omnivore interaction, Table 1). Addition- ally, Orchelimum reduced plant growth (change in height), 400 but did so most effectively when nutrients were added (Fig. 2d; significant nutrients×omnivore interaction, 300

Table 1). Nutrient addition had different effects on leaf (#) abundance 200 width depending on the presence of Orchelimum and Prokelisia: leaf width increased with nutrients in the presence 100 of Orchelimum, but decreased when both Orchelimum and Prokelisia 0 Prokelisia were present (significant nutrient×omnivore× herbivore interaction, Table 1). 12 10 Top–down Effects on Herbivores Orchelimum reduced 8

Prokelisia abundance by ~50% (Fig. 3a) and thereby damage indirectly reduced the number of leaves damaged by 6

Prokelisia by 25% (Fig. 3b). Top–down control of Prokelisia (#of leaves) 4

populations and the trophic cascade on the number of leaves Prokelisia 2 – damaged by Prokelisia were strong regardless of bottom up 0 – – conditions (no significant bottom up×top down interactions O- O+ for Prokelisia abundance or damage, Table 1). Fig. 3 Top–down effects from omnivorous Orchelimum katydids on a Relationships Among Response Variables and Comparison herbivorous Prokelisia planthoppers and b the number of leaves damaged by Prokelisia. O+ omnivore present, O− omnivore absent. with Omnivorous Crabs SEM analysis of parallel food web ANOVA statistics are reported in Table 1 and Electronic Supplemen- experiments with an omnivorous salt marsh crab (Ho and tary Material. Data are means+1 SE Estuaries and Coasts (2012) 35:475–485 481 iment in Ho and Pennings (2008) indicated that the not affect plant growth, although Prokelisia damage omnivorous crab Armases negatively affected aphids, reduced leaf width; this difference between the ANOVA negatively affected growth of the Iva shrub, and indirectly and SEM results occurred because the top–down effects of increased Iva leaf area through its negative effect on aphids Prokelisia on plant growth were strongest when salt and (Fig. 4a). Aphids had a significant top–down effect only on nutrients were added, but these treatments were not Iva leaf area; however, the best SEM model retained non- included in the SEM analysis because we used only significant top–down effects of aphids on leaf number and treatment combinations that were parallel to those used by plant growth, suggesting that these effects were likely also Ho and Pennings (2008). important. SEM analysis of the no nutrient, no salt treatments in the Spartina mesocosm experiment (this Benefits of Mixed Diets In the laboratory, Orchelimum fed a paper) indicated that Orchelimum had stronger direct effects mixed diet of both Spartina and Prokelisia attained a body on plants and weaker effects on herbivores than did mass 25% greater than individuals fed either diet alone Armases. Orchelimum reduced Spartina leaf width and (Fig. 5). Only 2 of 24 individuals died during the experiment growth (change in height), negatively (but weakly) affected (both from the Spartina-only diet; these were not included Prokelisia numbers and indirectly increased leaf width by in calculations of final mass), and all but one of the reducing damage from Prokelisia (Fig. 4b). Prokelisia did survivors had molted into the final instar after 5 weeks.

Fig. 4 SEM path diagrams for a interactions in the experimental Iva food web from Ho and Pennings (2008)(p=0.13, Chi-square/df=1.58) and b a subset of the experimental Spartina food web (this paper) (p=0.49, Chi-square/df=0.96). Path coefficients represent standardized values showing relative effects of variables upon each other; solid lines indicate statistically significant paths; dashed lines indicate non-significant paths retained to improve overall model fit. Arrow width is proportional to path coefficient strength; one-headed arrows depict causal relationships; two-headed arrows depict correlations 482 Estuaries and Coasts (2012) 35:475–485

0.25 a with a salt marsh shrub, found that intermediate levels of b b 0.20 chronic salinity stress stimulated a planthopper herbivore (Pissonotus quadripustulatus,Homoptera:Delphacidae)but 0.15 that high levels of chronic salinity had negative effects. Given that we did not examine extremely high salinity levels 0.10 (Spartina occurs in soils with porewater salinities of >60), it is possible that negative effects of salinity on herbivores 0.05 would have prevailed at higher salinities. Orchelimum body mass (g) 0.00 Because both nutrients and salinity decreased plant C/N SPSP ratio and increased Prokelisia abundance, one might have expected that their combination would affect plant C/N and Fig. 5 Body mass of O. fidicinium after 5 weeks of feeding on Spartina (S), Prokelisia and Spartina (PS), and Prokelisia (P). Data planthopper abundance even further, but this did not occur. are means+1 SE. ANCOVA with initial mass as the covariate, F(2, Moon and Stiling (2000) and Stiling and Moon (2005) 17)=7.18, p<0.01 obtained a similar result for P. quadripustulatus feeding on the shrub Borrichia. Although the mechanism underlying Discussion this result was not explored in any of these cases, the fact that nitrogen and salinity have less than additive effects on We correctly predicted (hypothesis 1) that nutrients and salt herbivores is important, because it means that the effects of would increase the nitrogen content of Spartina and benefit nitrogen addition on herbivores cannot be predicted without herbivorous planthoppers. In contrast, we largely failed also considering the salinity regime experienced by the (hypothesis 2) to predict the effects of the omnivorous plants. katydid on the planthopper-Spartina food web, illustrating Because both nutrients and salinity decreased plant C/N the difficulty in predicting the effects of omnivores on food ratio and increased Prokelisia densities, one might expect to web structure and processes. The comparison of the find increased suppression of plant growth in these treat- omnivorous katydid and omnivorous crab (hypothesis 3) ments. This did happen, but only when both nutrients and suggested that variation in diet flexibility may mediate food salt were added. Previous studies with the salt marsh shrub web effects of omnivores. Borrichia frutescens (Moon and Stiling 2002, 2004; Stiling and Moon 2005) and with Spartina (Denno et al. 2002; Hypothesis 1: Effects of Nutrients and Salt on Plants Sala et al. 2008) also found positive effects of nutrients on and Herbivores the top–down effect of herbivores on plants. Similarly, some studies have found increased effects of herbivores on We hypothesized that nutrient and salt additions would salt-stressed S. alterniflora (Silliman et al. 2005). Why we directly increase Prokelisia herbivore populations by only found increased top–down effects when both nutrients increasing plant quality. This hypothesis was supported. and salt were added is not clear, but the general pattern of Nitrogen addition increased leaf chlorophyll content, the results is consistent with these previous studies. decreased leaf C/N and toughness, and increased the abundance of Prokelisia. This result was consistent with Hypothesis 2: Effects of Orchelimum on Plants previous studies that have found that fertilizing Spartina and Herbivores plants in the field decreases C/N ratio and increases Prokelisia abundance (Gratton and Denno 2003; McFarlin Our hypotheses about top–down effects from Orchelimum et al. 2008). were not as often correct. Because Orchelimum is omniv- Similarly, salinity addition decreased leaf C/N and orous, eating both plants and herbivores, we hypothesized increased Prokelisia abundance. This result was also that it would have both direct negative and indirect positive consistent with previous studies that have found that higher effects on plants, leading to weak net effects. In contrast to salinities decrease Spartina C/N ratio (Moon et al. 2000; our expectations, Orchelimum strongly suppressed plant Moon and Stiling 2000, 2004). Salt marsh plants are known growth (determined as change in height). The SEM analysis to increase production of nitrogen-based compounds to confirmed that Orchelimum did have an indirect positive reduce osmotic stress when growing in high-salinity soils effect on Spartina by reducing Prokelisia abundance, which (Morris 1984). Given that the high-salinity treatment in our in turn reduced the number of leaves damaged by experiment (25) was well within the levels that Spartina can Prokelisia. However, although Prokelisia affected leaf tolerate (Richards et al. 2005), it is likely that our “high”- chlorophyll content, width, and toughness, it did not affect salinity treatment was only a moderate stress that did not plant growth, and thus the beneficial effect of Orchelimum highly stress the plants. Moon and Stiling (2005), working on Spartina (reduced leaf damage from Prokelisia) did not Estuaries and Coasts (2012) 35:475–485 483 translate into a growth benefit, and its direct negative et al. 2002; Moon and Stiling 2002, 2004). One mechanism effects were far stronger than its indirect positive ones that might have reduced the importance of interactions (Fig. 4). As a result, Orchelimum had strong net negative between top–down and bottom–up factors at the herbivore effects on plants, not weak net effects. In general, it has level in this experiment is that the mesocosm cages proven easier to demonstrate trophic cascades that affect prevented immigration and emigration of arthropods. In herbivore damage to plants than to demonstrate cascades particular, migration of Prokelisia from low to high-quality that affect plant growth (Schmitz et al. 2000). Other studies plants is known to mediate the strength of top–down have demonstrated negative effects of Prokelisia on interactions in the field (Denno et al. 2003, 2005). It is Spartina growth (Denno et al. 2002; Finke and Denno likely that Orchelimum also moves across the marsh to 2004); however, and it is likely that we would have found follow high-quality plants or abundant prey, with similar such an effect had the experiment continued longer than effects, but this has not been documented. one month. We further hypothesized that both nutrient addition and Hypothesis 3: Different Omnivores have Similar Trophic salinity stress would reduce top–down control of Prokelisia Effects by Orchelimum by decreasing the C/N ratio of plants (making plants a more attractive alternate diet for Orche- Finally, we compared our results with those of a similar limum) and increasing Prokelisia abundance (leading to study by Ho and Pennings (2008) of an omnivorous crab herbivore escape from control by Orchelimum). Only some feeding on aphids and a salt marsh shrub to test the aspects of this hypothesis were supported. As discussed hypothesis that these two omnivores would have similar above, nutrient and salt addition did decrease plant C/N effects on trophic structure. This hypothesis was rejected, ratios and did increase Prokelisia abundances; however, the with Orchelimum having strongest effects on plants top–down effect of Orchelimum on Prokelisia was not whereas the crab had similar effects on plants and affected by nutrient or salinity additions (Table 1). The top– herbivores (Fig. 4). One benefit of an omnivorous diet is down effect of Orchelimum on plants, however, strongly that the consumer can potentially switch between various increased in the fertilized treatment, and in this way the food types depending on their availability and quality. effects of Orchelimum paralleled those of herbivores. Thus, the omnivorous crab A. cinereum consumed fewer A number of studies have shown that predators (mostly Iva frutescens leaves when aphids were present as an spiders) can exert strong top–down control on Prokelisia alternative, preferred food source (Ho and Pennings 2008). populations (Denno et al. 2003, 2005; Finke and Denno We expected Orchelimum to switch in the same way from 2004). The role of Orchelimum and related katydids as top– feeding on Spartina when Prokelisia were absent to feeding down consumers in salt marshes, however, has been mostly on Prokelisia when it was present. Contrary to this overlooked since the foundational work of Teal (1962) expectation, Orchelimum always heavily damaged plant and Smalley (1960) mis-identified these species as strict leaves, and suppressed Spartina growth whether or not herbivores. Based on the premise that Orchelimum was a Prokelisia was present. strict herbivore, subsequent experimental work that Whether omnivory should in general strengthen or detected decreases in Prokelisia when Orchelimum was weaken trophic cascades is unclear (Polis and Strong present attributed the results to competition (Stiling et al 1996; Eubanks 2005). The answer likely depends in part 1991). We observed, however, that Orchelimum vigorously on the omnivore’s feeding preferences for plant versus hunts and consumes Prokelisia,thatProkelisia actively animal prey, and on the strength of its negative effects on hides from Orchelimum behind Spartina leaves, and we different trophic levels. In our study, Orchelimum sup- documented that Orchelimum benefits from including both pressed both Prokelisia and Spartina, but the direct animal and plant material in its diet (Fig. 5). Several negative effects on Spartina dominated the food web species of Orchelimum and related katydids in the genus (Fig. 4). Conversely, the omnivorous crab Armases Conocephalus occur in North American salt marshes preferred to eat aphids, and switched foods to essentially (Wason and Pennings 2008). All are likely omnivorous act as a predator whenever aphids were present, producing (Goeriz Pearson et al. 2011). We suggest that these a trophic cascade that benefitted Iva plants (Ho and katydids may play a previously overlooked role in Pennings 2008). This difference is reflected in the stronger mediating the densities of small arthropods in salt marsh direct link from omnivore to herbivore in the SEM food webs, and that these effects merit additional study. analysis of the Iva food web versus the Spartina food Previous studies looking for interactions between nutrient web. The different food web effects of these two or salt addition and predator pressure on salt marsh herbivores omnivores are a function of their dietary flexibility: found that nutrient additions can strengthen top–down forces Armases grows as well on a diet of animal prey as on a on herbivores, while salinity stress can weaken them (Denno mixed diet (Buck et al. 2003)andsocanreadilyswitchto 484 Estuaries and Coasts (2012) 35:475–485 an animal-only diet when animal preys are abundant. In References contrast, Orchelimum grows best on a mixed diet (Fig. 5) and therefore is less flexible in its feeding behavior. In other Bertness, M.D., C. Crain, C. Holdredge, and N. Sala. 2008. words, whereas plants and herbivores may be somewhat Eutrophication and consumer control of New England salt marsh substitutable foods (Van-Rijn and Sabelis 2005)forArmases, primary productivity. Conservation Biology 22: 131–139. ’ they are complimentary for Orchelimum, meaning that both Bruno, J.F., and M.I. 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