importance of local vs. geographic variation in salt marsh plant quality for arthropod herbivore

Importance of local vs. geographic variation in saltmarsh plant quality for arthropod herbivorecommunitiesLaurie B. Marczak1,2*†, Kazimierz Wiezski1, Robert F. Denno2 and Steven C. Pennings1

1Department of Biology and Biochemistry, University of Houston, Houston, TX 77204, USA; and 2Department ofEntomology, University of Maryland, College Park, MD 20742, USA

Summary

1. An important recent advance in food web ecology has been the application of theory regardingspatial gradients to studies of the factors that affect animal population dynamics. Building on exten-sive studies of the Spartina alterniflora food web at the local scale, we hypothesized that geographicvariation in S. alterniflora quality is an important bottom-up control on food web structure and thatgeographic variation in S. alterniflora quality would interact with the presence of predators and topomnivores to mediate herbivore densities.2. We employed a four-factor fully crossed experiment in which we (i) collected plants from high-and low-latitude locations and grew them in a common garden and varied (ii) plant fertilization sta-tus (mimicking the plant quality differences due to marsh elevation), (iii) mesopredator density and(iv) omnivore density.3. Our results suggest that the single most important factor mediating insect herbivore densities islocal variation in plant quality – induced in our experiment by fertilization and demonstratedrepeatedly as a consequence of marsh elevation.4. Top-down effects were generally weak and in those cases where predators did exert a significantsuppressing effect on herbivores, that impact was itself mediated by host-plant characteristics.5. Finally, despite observed variation in plant quality with latitude, and the separately measurableeffects of this variation on herbivores, geographic-scale variation in plant quality was overwhelmedby local conditions in our experiments.6. Synthesis. We suggest that a first-order understanding of variation across large latitudinal ranges inthe Spartina alterniflora arthropod food web must begin with local variation in plant quality, whichprovides strong bottom-up forcing to herbivore populations. A second-order understanding of thearthropod food web should consider the role of predation in controlling herbivores feeding on low-quality plants. Finally, while latitudinal variation in plant quality probably explains some variation inherbivore densities, it is probably more of a response to herbivore pressure than a driver of the herbi-vore dynamics. Although extrapolating from local to geographic scales presents multiple challenges, itis an essential task in order for us to develop an understanding that is general rather than site-specific.

Key-words: latitudinal gradient, plant–herbivore interactions, salt marsh, Spartina alterniflora,top-down vs. bottom-up

Introduction

An important recent advance in food web ecology has beenthe application of theory regarding spatial gradients to stud-ies of the factors that affect animal population dynamics

(McGeoch & Price 2005; Post 2005). Historically, ecolo-gists debated the importance of top-down (Hairston, Smith& Slobodkin 1960) and bottom-up (Ehrlich & Birch 1967)factors in regulating herbivore populations, but most ecolo-gists now agree that these factors interact, sometimes incomplex ways, to influence population dynamics (Hunter &Price 1992). With this new, nuanced perspective, ecologistsare now asking how variation in abiotic factors and com-munity composition across landscapes affects the relative

*Correspondence author. E-mail: [email protected]† Present address: Department of Ecosystem and Conservation Sci-ences, The University of Montana - Missoula, MO 59812, USA.

© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society

Journal of Ecology 2013, 101, 1169–1182 doi: 10.1111/1365-2745.12137

importance of top-down and bottom-up forces (Walker &Jones 2001; Denno, Lewis & Gratton 2005). Most of thiswork has focused on local and regional scales, with fewstudies at large geographic (= continental) scales that spanlarge gradients in climate, oceanographic drivers or soiltype (but see Blanchette et al. 2008; Marczak et al. 2011;McCall & Pennings 2012). As a result, we currently havea poor understanding of the extent to which factors mediat-ing variation in community structure at local scales alsomatter at geographic scales. Thus, an important task forecologists is to expand our studies of local landscapes tothe geographic scale in order to better understandgeographic variation in community structure.Salt marshes on the Atlantic Coast of the United States are

ideal systems for comparing local and geographic variationsin community structure. Atlantic Coast salt marshes consist ofrelatively simple communities of plants and animals that arebroadly similar in composition across a large range of latitudeand climate from Central Florida through to Maine (Pennings,Siska & Bertness 2001). In particular, lower elevations ofmarshes throughout this geographic range are dominated by asingle plant species, salt marsh cordgrass, Spartina alternifl-ora (Bertness 2007), with its associated herbivores (Dennoet al. 1987; Pennings et al. 2009). This apparent simplicity,however, conceals considerable variation at both local andgeographic spatial scales.At the local scale, S. alterniflora plants close to creekbanks

are larger, richer in nitrogen, lower in phenolics and morepalatable to herbivores than the plants from the high marsh(Ornes & Kaplan 1989; Goranson, Ho & Pennings 2004;Denno, Lewis & Gratton 2005). Within local marshes, plant-hoppers migrate seasonally to creekbanks, departing as winterconditions make this habitat unsuitable (Denno 1983).Mesopredators (spiders) also migrate from high-marsh tolow-marsh habitats seasonally (Finke & Denno 2006). As aconsequence of this variation in plant quality and predatordistribution, top-down and bottom-up forces on herbivoresvary both seasonally and across the marsh landscape (Denno,Lewis & Gratton 2005).At the geographic scale, plants from high latitudes are

again richer in nitrogen, lower in phenolics and more palat-able to herbivores than conspecific plants from the same habi-tats at low latitudes (Pennings, Siska & Bertness 2001; Siskaet al. 2002; Salgado & Pennings 2005). Planthopper herbi-vores show little variation in density with latitude, but herbiv-orous snails are more abundant at low latitudes (Penningset al. 2009). Spiders are present at all latitudes, but top omni-vores (katydids) are most abundant at low latitudes (Penningset al. 2009). The consequences of geographic variation inplant quality and predator distribution for herbivore popula-tions are poorly understood (but see Marczak et al. 2011;McCall & Pennings 2012).An additional complication in understanding the geo-

graphic variation of arthropod community structure is thatthe trophic impacts of omnivores are ambiguous. Omnivoresmay sustain their population levels when prey are scarce byeating plants (Dayton 1984; Eubanks & Denno 2000),

resulting in increased predation pressure on herbivores whenherbivores are present. Alternately, omnivores may becomesatiated faster by eating at multiple trophic levels, reducingtheir per capita consumption of any particular prey (Eubanks& Denno 2000). Omnivory may thus either enhance or atten-uate top-down effects (Denno et al. 2002; Ho & Pennings2008), and variation in the abundance of omnivores or thestrength of their interactions may be important factors indetermining the structure of food webs across large latitudi-nal gradients.In sum, we have a reasonable understanding of how top-

down and bottom-up forces interact to explain variation inherbivore densities over small elevational gradients (creek-bank vs. mid-marsh) within single marshes. In contrast,although we know that plant quality and predator/omnivoredensities vary geographically, we have little understanding ofhow these factors interact to mediate geographic variation inherbivore densities. Previous work suggests that enhancedplant nutrient status may allow herbivores to escape frompredator control either through nutritional benefits leading torapid population growth (Denno et al. 2002) or because pred-ator search times are increased on plants with higher biomass(Olmstead et al. 1997). Here, we compare the importance oflocal vs. geographic controls on arthropod communities, usingSpartina alterniflora and associated arthropods as a modelsystem. To explore how local and geographic variation inplant quality and food web composition might affect Spartinaherbivore dynamics, we conducted a mesocosm study thatvaried (i) plant provenance (plant quality derived from the lat-itudinal gradient), (ii) fertilization status (mimicking plantquality differences due to marsh elevation), and the presenceof (iii) mesopredators (the spider Pardosa littoralis) and (iv)omnivores (the katydid Orchelimum fidicinium). To furtherunderstand the results of this mesocosm experiment andextrapolate to more complicated food webs in the field, weconducted predation trials in the laboratory to determine therates at which different species from the Spartina food webfeed on each other (a subset of the most abundant taxa fromfield collections: four spiders, a beetle and Orchelimum adultsas predators and three additional prey species). Building onextensive studies of the S. alterniflora food web at the localscale that have shown a strong bottom-up effect of local vari-ation in plant quality (Denno et al. 2002, 2003; Denno, Lewis& Gratton 2005), we hypothesized that geographic variationin S. alterniflora quality was also an important bottom-upcontrol on food web structure and that local and geographicvariation in S. alterniflora quality would interact with thepresence of predators and top omnivores to strongly mediateherbivore densities.

Materials and methods

THE SPARTINA FOOD WEB

On the Atlantic Coast of North America, salt marshes dominated bySpartina alterniflora (henceforth Spartina) range from peninsularFlorida to Canada (Denno et al. 1996; Pennings, Siska & Bertness

© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1169–1182

1170 L. B. Marczak et al.

2001). Spartina plants from high latitudes (RI to ME, 41–43°) aremore nutritious (% N) and tender than conspecific plants from lowlatitudes (GA to FL, 30–31°) (Salgado & Pennings 2005; McCall &Pennings 2012). Moreover, the concentration of phenolics in Spartinais lower in plants from high (2.45 � 0.13% dry mass) vs. low(3.16 � 0.10%) latitudes (Siska et al. 2002). Preference tests in thelaboratory using a variety of herbivores demonstrated that both polarextracts (polar extracts containing allelochemicals in artificial diet)and live leaf tissue from high-latitude Spartina are far more palatable(more diet or leaf area consumed) than their low-latitude counterparts(Pennings, Siska & Bertness 2001; Siska et al. 2002; Salgado &Pennings 2005). In sum, high-latitude plants in these marshes areknown to be more nutritious, softer, less defended and more palatablethan low-latitude plants.

Spartina also varies in quality within individual salt marshes.Spartina grows across an elevational range of c. 0.5–2.0 m (McKee& Patrick 1988) within a single marsh. Tall-form Spartina plants(about 1.5 m tall) occur along estuarine creeks while the short form(about 0.5 m) occurs in high-marsh habitats (Valiela, Teal & Deuser1978). Tall-form plants close to creekbanks are larger, richer innitrogen (tall-form shoot tissue, 1.0–1.69%N; short-form shoot tissue,0.8–1.53%N; data summarized in Ornes & Kaplan 1989), lower inphenolics and more palatable to herbivores than plants from the highmarsh (Ornes & Kaplan 1989; Goranson, Ho & Pennings 2004;Denno, Lewis & Gratton 2005). Nitrogen is more available to plantsat creekbanks than in the high marsh (Mendelssohn & Morris 2000),and fertilization experiments have demonstrated that the nutritionalstatus of tall Spartina (TS) and short Spartina (SS) generallyaccounts for the majority of the phenotypic differences between theheight forms (Valiela, Teal & Deuser 1978). Consequently, fertiliza-tion is a common experimental practice used to mimic variationbetween tall- and short-form plants in greenhouse experiments(Denno et al. 2002).

By far, the most common herbivores of Spartina are the delphacidplanthoppers Prokelisia marginata and P. dolus (Denno et al. 2002).Prokelisia marginata and P. dolus (hereafter, Prokelisia) are multi-voltine, with a summer generation time of 5–6 weeks (Stiling &Rossi 1997). They are phloem sap-feeders that can reach densitiesexceeding several thousand adults per m2 with nymphal densitiesgreater than 10 000 per m2 (Denno 1983). A number of invertebratepredators are common in Spartina stands, including spiders andcoccinellid beetles. The hunting spiders Hogna modesta (hereafterHogna) and Pardosa littoralis (hereafter, Pardosa) are particularlycommon and are known to suppress planthopper populations (Dennoet al. 2004) except when planthoppers experience ‘outbreaks’ onhigh-nitrogen host plants (Denno et al. 2004; Huberty & Denno2006). In our mesocosm experiment, we used Pardosa as a well-studied representative of the Spartina predator community that isabundant across the entire latitudinal range of our study; other preda-tors were included in predation trials to help us generalize the exper-imental results across the Spartina community. The most commontrue omnivore in the Spartina zone of south-eastern salt marshes isthe tettigoniid katydid Orchelimum fidicinium (hereafter, Orcheli-mum) (Pennings et al. 2009). Although historically regarded as anherbivore (Teal 1962), Orchelimum, like most tettigoniids, is omniv-orous and readily eats small arthropods (Jim�enez et al. 2012).Orchelimum is univoltine, with adult densities reaching 9.6 individu-als per m2 (Stiling, Brodbeck & Strong 1991). At high latitudes,Orchelimum is replaced by the smaller tettigoniid Conocephalusspartinae (hereafter, Conocephalus) (Wason & Pennings 2008),which is also omnivorous (Bertness, Wise & Ellison 1987; Bertness& Shumway 1992; Goeriz Pearson et al. 2011).

MESOCOSM EXPERIMENT

The mesocosm study addressed putative local and geographic driversof herbivore density by varying four factors in a fully crossed design:(i) plant provenance (constitutive plant quality derived from the latitu-dinal gradient), (ii) fertilization (causing plant quality differences tomimic those related to marsh elevation), and the presence of a domi-nant species of both (iii) mesopredator (the spider Pardosa littoralis)and (iv) omnivore (the katydid Orchelimum fidicinium). We collectedSpartina from five high-latitude sites and five low-latitude sites(Table 1) and established mesocosms with two levels each of fertil-izer level (fertilized and unfertilized), mesopredator density (0 or 3)and omnivore density (0 or 1). These treatments were crossed in afull factorial design for a total of 80 mesocosms with five replicatesper treatment where each replicate contained field-collected plantsfrom a single site of the appropriate latitude (site was thus nestedwithin latitude). Each mesocosm was stocked with 25 herbivores(Prokelisia). Initial Prokelisia, spider and katydid densities wereselected to represent average densities that occur naturally on themarsh (Denno et al. 1996; Ho & Pennings 2008).

Plants (short-form plants from the marsh platform) were collectedfrom field locations between 18 and 22 May 2009 and established inmesocosm containers (each mesocosm consisting of four Spartinastems from a single collection site in a single 30-cm diameter pot;soil was a 1 : 1 mixture of sand and potting soil) in an outdoorgreenhouse with a roof to block rain but no walls, thereby keepingplants at close to ambient temperature and humidity, at the Universityof Georgia Marine Institute on Sapelo Island GA (31°27′ N; 81°16′W). Beginning on June 2 of 2009, mesocosms assigned to the fertil-izer treatment received 9.5 g of fertilizer (Ultra Vigoro Plant Food, 12-5-7, Madison, Wisconsin, USA) every week for 4 weeks prior to thebeginning of the experiment and every second week after the experi-ment had begun. On 19 June 2009, after plants had acclimated togreenhouse conditions and responded to initial fertilizer treatments,we took preliminary measurements of all plants (number of green,yellow [naturally senescing] and damaged leaves, mean percent dam-age to leaves, chlorophyll content measured with an OPTI-SciencesCCM-200 chlorophyll metre) and placed 5 g of (dry weight) deadSpartina stems and leaves at the base of each plant to provide habitatstructure for spiders. Each mesocosm was fitted with a mesh cageconsisting of lightweight fabric supported by bamboo stakes. Themesh cages reduced incident light by c. 18%. Although this designplaced plants from high and low latitudes in a common garden, differ-ences in the palatability of high- vs. low-latitude Spartina plants per-sisted for more than a year and five clonal generations in a previouscommon garden experiment, we saw no evidence for local feedingpreferences among herbivores (Pennings, Siska & Bertness 2001),

Table 1. Sources of Spartina alterniflora plants used in mesocosms:site names and locations

Site name State Decimal latitude Latitude category

Nelson Island MA 42.44 HighGreat Neck MA 42.42 High100 Acres RI 41.46 HighRumstick Cove RI 41.43 HighCottrell Marsh CT 41.20 HighBaruch SC 33.22 LowAce Basin SC 32.33 LowEulonia GA 31.54 LowAirport/Dean Creek GA 31.23 LowAmelia FL 30.40 Low


Local vs. geographic variation in plant quality 1171

and differences observed in the common garden were sufficient toexplain differences in palatability observed in freshly collected fieldplants (Salgado & Pennings 2005). Thus, we expect that the ‘latitudi-nal signal’ of plant quality was fully maintained in this common gar-den experiment.

On 21 June 2009, we field-collected spiders (Pardosa littoralis)and katydids (Orchelimum sp.) in Georgia and held them in the labo-ratory. On 22–23 June 2009, we collected Prokelisia from the field inGeorgia and placed 25 individuals in each mesocosm. We allowedthe Prokelisia to disperse within each mesocosm and added spiders(Pardosa) the following day. Katydids (Orchelimum) were introduced4 h after the addition of spiders. Once mesocosms were fully stockedaccording to the treatment (26 June 2009), we positioned each meso-cosm haphazardly across the greenhouse. A limited number of vari-ables (number of Prokelisia, Orchelimum and Pardosa) weremeasured 2 weeks into the experiment to assess the potential for out-break dynamics; variables relating to plant quality could not be deter-mined because of the risk of escape by arthropods. Mesocosms werebroken down and resampled after 6 weeks (12 August 2009) once itbecame apparent that herbivores were reproducing rapidly in sometreatments and consuming entire plants.

We used mixed-model nested ANOVAS to assess the effect of treat-ments for individual response variables where site was nested withinlatitude (random) and latitude, fertilizer, spider density and katydiddensity were fully crossed fixed factors. Relative growth rate of plantswas calculated as the natural log +1 of the final number of greenleaves minus the natural log +1 of the initial number of green leaves,divided by the duration (days) of the experiment. Katydid relativegrowth rates were calculated analogously as the natural log of finalmass minus the natural log of initial mass, divided by the duration(days) of time in the experiment. Growth rates could not be similarlycalculated for spiders because we were unable to mark individuals; agroup estimate of change in biomass was hindered by low survivalrates (many zeros). Accordingly, we used survival as our variable ofinterest for spiders. We estimated initial plant biomass allometricallybased on the height of all shoots (cm) in each plant mesocosm at thestart of the experiment; final plant biomass was determined by clip-ping, drying and weighing all the above-ground live biomass (g).Leaves from each of these plants were lyophilized and analysed fortotal nitrogen content at the University of Georgia Chemical AnalysisLaboratory, Athens, Georgia, USA. We used log (v + 1) and squareroot transformations where necessary to improve the normality andheterogeneity of variances. Where data were unbalanced, weemployed Satterthwaite’s approximation (as recommended by Quinn& Keough 2002) that results in fractional denominator degrees offreedom.

A potential weakness of the ANOVA approach is that it does notaccount for the fact that some variables (e.g. herbivore numbers, planttraits) are both responding to and simultaneously driving other vari-ables. Thus, we also analysed results of the mesocosm experimentusing structural equation modelling (SEM) that allows a variable tobe simultaneously influenced by other variables and cause variation ina dependent variable (Grace 2006). We were particularly interested inusing SEM to test the hypotheses that there would be an interactionbetween fertilization and top-down effects, that any effect of fertiliza-tion on Prokelisia would be mediated through increased plant bio-mass and N content and that fertilization would decrease damage toplants by increasing plant biomass (a dilution effect). Building anSEM model consists of several consecutive steps. It starts with a pri-ori identification of the causal relationships between the interplayingvariables, followed by the estimation of the path parameters

performed by screening the matrix of covariances over the hypotheti-cal model. Finally, model fit is determined by comparing the pre-dicted matrix of covariances with that from the original data.Parameters of the model were estimated using AMOS 7.0 (AmosDevelopment Corporation, Mount Pleasant, South Carolina, USA)with the maximum likelihood method, and the model fit was testedby the likelihood chi-square value.

PREDATION TRIALS

To broaden our understanding of the trophic interactions and to deter-mine the rates at which different species within the Spartina foodweb feed on each other, we conducted cannibalistic trials and preda-tion trials in the laboratory including animals not used in our experi-mental food web but which were numerically dominant in the field atthe time of the experiment. Trials for cannibalism included Orcheli-mum adults that were enclosed with 5th instar Orchelimum juveniles(last instar before maturation). The Orchelimum adults were 24% lar-ger (tibia or body length) than the juveniles. Predation trials includedsix predators (four spiders, a beetle and Orchelimum adults), as wellas the mirid bug Trigonotylus sp. and the lygaeid bug Ischnodemusbadius as potential prey. Trials were conducted in June and July of2009 and 2010. Animals were collected from the field by hand,sweep net or vacuum sampler. Replicates of the different treatmentswere run as individuals of different species became available, and thenumber of replicates varied among species combinations due to theavailability of animals (n = 27 for Orchelimum adults on Prokelisiaand n = 3–15 for all other trials; refer to Fig. 7 for details). Upon col-lecting, animals were acclimated for 24 h to laboratory conditionsand to standardize levels of hunger for field caught animals. Individ-ual trials were run for up to 24 h in 850-mL glass jars at a constantroom temperature of 25 °C and photoperiod (14 : 8 day : night).Each jar was stocked with a 15 cm long Spartina leaf that served asa substrate for the animals. In each case, consumers were allowed tofeed ad libitum and were used only once. Since the containers weused were of small volume, we assume that the predator–preyencounter rates were so high that predation rates were not limited bythe number of prey offered, but only by the ability and motivation ofpredators to subdue and consume prey. This motivation, however,may have been occasionally modified by nonpredatory mortality ofprey that occurred after 8 h of the trial (all trials with the soft-bodiedmirid Trigonotylus and some with Prokelisia). Some trials werestopped at 8 h if predators were depleting prey or if prey appearedstressed in the jars. Consumption rates for longer assays were pro-rated by duration and all data reported as number consumed in 8 h.Results from 2009 and 2010 were broadly consistent across years andacross Prokelisia size categories, but distinct among differentpredator–prey combinations; we therefore pooled data among yearsand across different sizes of Prokelisia prey to increase sample sizes.We conducted one-way ANOVAs for different predator–prey combina-tions within each of three prey groupings (Prokelisia, Orchelimum,mixed trials) with predator–prey combination treated as a fixed factor.

Results

IN IT IAL PLANT QUALITY

At the start of the experiment, fertilized plants had 8.8%greater total biomass (F1,56 = 45.19, P < 0.0001), 22.5%more green leaves (F1,56 = 47.22, P < 0.0001) and 58%higher levels of chlorophyll (F1,56 = 24.24, P < 0.0001) than



unfertilized plants. In contrast, there were no initial differ-ences by latitude of plant origin in plant biomass(F1,56 = 0.10, P = 0.76), chlorophyll content (F1,56 = 0.35,P = 0.57), number of green leaves (F1,56 = 0.27, P = 0.27)or plant damage (mean percent damage, F1,56 = 1.0,P = 0.32).

PLANT RESPONSES

Fertilization increased the percent foliar nitrogen in Spartinaleaves at the end of the experiment by 50–100%(F1,45.2 = 130.81, P < 0.0001) over unfertilized plants. Theresulting differences in N content (control 1%; fertilized1.8%) are within the range of those observed between short-and tall-form Spartina alterniflora in South Atlantic saltmarshes (refer to data from Ornes & Kaplan 1989 summa-rized under Materials and methods in this report). Fertilizedplants had a lower percentage of damage to individual leaves(Fig. 1a) than unfertilized plants; the proportion of greenleaves that were damaged followed the same patterns and sta-tistical significance (Table 2). Fertilized plants also exhibitedgreater overall plant biomass (Fig. 1b) than unfertilizedplants. Low-latitude plants had greater biomass (Fig. 1b andTable 2) than high-latitude plants. At the end of the experi-ment, plants from high-latitude sources were 22.4% higher in

foliar nitrogen than those from the low-latitude sources. Thepresence of katydids in mesocosms reduced final plant bio-mass (Fig. 1b and Table 2). We recorded the lowest plantgrowth rates (negative RGR) in unfertilized plants from highlatitudes in mesocosms containing katydids; in contrast, thegrowth of plants from low latitudes was enhanced by fertilizerapplication, but not consistently affected by omnivore pres-ence (Fig. 2 and Table 2). There were no important maineffects of spider presence on any plant variables (Table 2).High-latitude plants lacking either consumer had depressednitrogen contents relative to plants with spiders (lati-tude 9 mesopredator 9 omnivore interaction, Table 2). Thiseffect was particularly striking for fertilized plants, but onlyat high latitudes (latitude 9 fertilized 9 mesopreda-tor 9 omnivore, Table 2). We suspect that this effect wasdue to herbivore feeding depressing plant nitrogen content(Denno et al. 2000), especially on the relatively smaller high-latitude plants, but did not investigate this further.

HERBIVORE RESPONSES

After 2 weeks, Prokelisia populations were elevated on high-latitude plants (P = 0.003) and tended to be suppressed(P = 0.097) by spiders (Fig. 3a). At this time, Prokelisia pop-ulations were suppressed in the presence of spiders only onunfertilized plants; on fertilized plants, Prokelisia attainedsimilar populations regardless of spider predation pressure(Fig. 3b). These basic patterns continued to the end of theexperiment (Table 3), but levels of statistical significance var-ied. At the end of the experiment, Prokelisia populations didnot differ between high- and low-latitude plants, wereenhanced several-fold by fertilizer and were reduced by omni-vores but not by spiders (Fig. 4c). The impacts of both omni-vores and spiders depended on whether or not plants werefertilized: both consumers tended to suppress Prokelisia onlyon unfertilized plants Fig. 4a,b), although this pattern wasonly significant for omnivores. Over all treatment combina-tions, Prokelisia population density was positively related toleaf nitrogen content (Fig. 5a).

PREDATOR AND OMNIVORE RESPONSES

Spider survival to the end of the experiment was unrelated toany treatment variables (Table 3). The growth rate of katydidswas positive for fertilized plants but negative across all unfer-tilized plants (Table 3). Over all treatment combinations, thegrowth rate of katydids was positively related to leaf nitrogencontent with a transition from negative to positive growth atleaf nitrogen contents of around 1.5% (Fig. 5b). Neithersource latitude of plants nor the presence of spiders affectedkatydid growth rates (Table 3).

SEM ANALYSIS

Overall, the SEM analysis supported our initial prediction andgeneral finding from ANOVA that fertilization (or local nutrientstatus) was a strong mediating factor on top-down effects in

latitude

P = 0.023

P = 0.02

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Tab

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Mesocosm

experiment.Resultsfrom

nested

mixed-m

odel

ANOVASforthefollo

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ass,percentfoliarnitrog

en,relativegrow

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(RGR)of

greenleaves,the

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that

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theprop

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andthepercentage

ofdamageto

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ince

measuresof

plantdamagewerescored

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ations

couldon

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combinatio

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includ

edom

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estim

ations

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eused

log(v

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where

necessaryto

improv

eno

rmality

andho

mog

eneity

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data

wereun

balanced,weused

Satterthw

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imation,

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inlatitud

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Source

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ass

PercentfoliarN

RGRgreenleaves

Green

leaves

(propo

rtion)

Dam

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leaves

(propo

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leaves

Den

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FP

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Latitu

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8.43

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9.0

6.81

0.028

823

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0.0013

7.4

1.25

0.30

7.7

2.24

0.18

7.2

8.22

0.023

Fertilizer

56142.83

<0.0001

45.2

130.32

<0.0001

5616

.97

<0.0001

53.6

15.76

0.0002

22.9

33.88

<0.0001

22.6

27.19

<0.0001

Mesop

redator

560.08

0.79

45.2

4.84

0.03

564.36

0.041

53.6

0.23

0.63

22.9

1.35

0.26

22.6

1.92

0.18

Omnivore

566.77

0.012

45.5

1.57

0.22

561.80

0.19

53.6

0.26

0.61

Lat

9fert

560.49

0.49

45.2

0.01

0.98

561.38

0.25

53.6

2.04

0.16

22.9

2.75

0.11

22.6

0.98

0.33

Lat

9meso

561.23

0.27

45.2

1.82

0.18

567.34

0.0089

53.6

1.25

0.27

22.9

0.14

0.71

22.6

0.09

0.77

Lat

9om

560.06

0.81

45.5

5.24

0.027

560.54

0.47

53.6

0.20

0.65

Fert9

meso

560.61

0.44

48.3

7.09

0.011

56<0.01

0.95

53.6

0.88

0.35

22.9

0.18

0.68

22.6

0.90

0.35

Fert9

om56

0.01

0.93

48.2

0.01

0.91

563.15

0.08

53.6

3.25

0.08

Meso9

om56

2.17

0.15

46.3

3.71

0.06

564.73

0.034

53.6

1.33

0.25

Lat

9fert9

meso

561.15

0.29

48.3

1.10

0.30

561.51

0.22

53.6

0.02

0.90

22.9

0.05

0.84

22.6

0.11

0.74

Lat

9fert9

om56

1.12

0.30

48.2

2.42

0.13

566.74

0.012

53.6

0.18

0.68

Lat

9meso9

om56

1.25

0.27

46.3

9.45

0.0035

562.48

0.12

53.6

<0.01

0.97

Fert9

meso9

om56

1.98

0.17

45.5

1.92

0.17

561.64

0.21

53.6

0.05

0.83

Lat

9fert9

meso9

om56

0.43

0.52

45.5

6.77

0.013

560.19

0.67

53.6

1.15

0.29



the Spartina mesocosms. As we initially predicted, SEM anal-ysis showed that the effect of fertilization on Prokelisia wasin large part mediated through an increase in plant biomass(Fig. 6a,b); larger plants simply represented greater foodavailability for herbivores. We do not believe that this rulesout a direct effect for nitrogen content as shown in Fig. 5,because the SEM considered high- and low-latitude plantsseparately and so had less power and a reduced range of Ncontent within each analysis, but it emphasizes that plantnutrition affects both size and N content and that both canaffect herbivore populations. We also predicted that fertilizedplants would experience lower levels of damage essentiallyvia a dilution effect attributable to an overall increase in plantbiomass. In our experiment, fertilized plants did experienceless omnivore damage – a result confirmed by both ANOVA

(Fig 1b) and SEM analyses. The SEM also supports thehypothesis that this was due to omnivore effects being dilutedamong the greatly increased biomass of plants, particularly atlow latitudes (Fig. 6b). At the same time, an increase in Prok-elisia densities reduced omnivore leaf damage in both high-and low-latitude plants, probably by providing an alternativefood for Orchelimum.

PREDATION TRIALS

All five predators tested (three spiders, a beetle and Orcheli-mum adults) ate Prokelisia, but the spider Hogna ate 3–4times more Prokelisia than the other predator species (Tukey–Kramer HSD P < 0.05, Fig. 7a). Both Hogna and Pardosaspiders ate fifth-instar Orchelimum, but did so at very lowrates, and Marpissa and a salticid spider ate no Orchelimum(Fig. 7b). Adult Orchelimum did not feed on fifth-instar con-specifics (Fig. 7b). Other arthropod herbivores (Ischnodemus,Trigonotylus) common in the Spartina community were con-sumed at moderate rates in predation trials by at least onepotential consumer, and Marpissa spiders were vulnerable tointraguild predation from the larger Hogna spiders (Fig. 7c).

Discussion

It is now generally agreed that top-down and bottom-up forcesinteract to affect populations of herbivores (Gruner 2004;Stiling & Moon 2005; Bertness et al. 2007; Sala, Bertness &Silliman 2008). In our mesocosm experiment, bottom-upsources of variation in plant quality determined food webstructure. This effect, however, was strong at the local scale

–0.05

–0.04

–0.03

–0.02

–0.01

0

0.01

0.02

0.03

0.04

0.05

RG

R g

reen

leav

es

High latitudeLow latitude

– O + O– O + O– O + O– O + O– F + F– F + F

a

abcbc

c

abab

abab

Fig 2. Mesocosm experiment. Interactiveeffects of latitude, omnivore and fertilizer forrelative growth rate (RGR) of green leaves(lat 9 fert 9 om, F1,56 = 6.74, P = 0.012).

0

5

10

15

20

25

30

35

40

45 P = 0.003 P = 0.097 P = 0.027

50

Abu

ndan

ce o

f Pro

kelis

ia (

indi

vidu

als/

plan

t)

0

5

10

15

20

25

30

35

40

45

50

Abundance of P

rokelisia (individuals/plant)

Fertilized x Mesopredator

a

a

a

b

(a) (b)

– M + MLow High – M + M – M + M

– F + F

After 2 weeks After 2 weeks

Fig 3. Mesocosm experiment. Abundance of Prokelisia after 2 weeks in experimental mesocosms. (a) Main effects of latitude (F1,9.2 = 15.24)and mesopredator presence (F1,53.23 = 2.84). Open bars represent low latitude and mesopredator absence, respectively, while closed bars representhigh latitude and mesopredator presence, respectively. (b) Significant interaction of fertilizer and mesopredator presence (fertilized 9 mesopreda-tor, F1,53.2 = 5.2, P = 0.027). Data are back-transformed lsmeans and 95% confidence intervals.



but weak at the latitudinal scale. Top-down effects on consum-ers were driven by the omnivorous katydid in our study ratherthan the strictly carnivorous spider. In those cases where pre-dators did exert a significant suppressing effect on herbivores,that impact was itself mediated by host-plant characteristics.Thus, in this case, we agree with the paradigm that ‘plants setthe stage on which herbivorous insects and their enemiesinteract’ (Denno, McClure & Ott 1995; Denno et al. 2002).

LOCAL, NOT GEOGRAPHIC, SOURCES OF BOTTOM-UP

CONTROL

Our mesocosm experiment indicated that the Spartina foodweb is strongly structured by local variation in plant quality – aresult supported by recent field experiment that noted increasesin multiple functional groups in response to in-situ fertilizationin both high- and low-latitude Spartina marshes (McCall &Pennings 2012). In our more-controlled greenhouse experi-ment, fertilized plants (mimicking variation in plant quality andform across the local elevation gradient) were consistently lar-ger and supported more herbivores, but showed less damage(due to dilution of herbivore damage and increased numbers ofalternate prey for omnivores) than unfertilized plants. Thisresult is consistent with a number of studies that have docu-mented that herbivores prefer and perform better on higher-quality plants from the creekbank vs. the mid-marsh and that

this result also tracks the variation in plant quality and heightnoted with field-collected plants (Denno et al. 2002; Goranson,Ho & Pennings 2004; Wimp et al. 2010).In contrast, latitudinal variation in plant quality produced

only weak or transient effects on herbivore populations.While Prokelisia populations were initially elevated on high-latitude plants, this effect was no longer apparent by the endof the experiment. Because latitudinal variation in plant qual-ity is maintained for an extended period of time when plantsare grown in a common garden (Salgado & Pennings 2005),we do not believe that the latitudinal plant quality signal wasartificially weak in our experiment. While the effects oflatitude were not as dramatic as that of fertilizer addition,low-latitude plants were consistently larger, but lower innitrogen, at the end of the experiment. Although high-latitudeplants are higher in nitrogen, lower in phenolics and morepalatable than low-latitude plants (Pennings, Siska & Bertness2001; Siska et al. 2002; Salgado & Pennings 2005), andalthough these differences are sufficient to cause geographicvariation in herbivore body size (Ho, Pennings & Carefoot2010), they were nevertheless overwhelmed in our experi-ments by fertilizer-induced nutritional status and food webcomposition. These findings are similar to those in ourprevious work with the high-marsh shrub Iva frutescens(Marczak et al. 2011), where we found that latitudinal varia-tion in plant quality had much smaller effects on herbivore

Table 3. Mesocosm experiment. Results from nested mixed-model ANOVAS for the following variables: total abundance of Prokelisianymphs, Prokelisia adults, all Prokelisia combined, the relative growth rate (RGR) of grasshoppers and proportion of spiders sur-viving. Estimations of grasshopper RGR and spider survival could only be made for mesocosm combinations which containedthese animals – absent estimations are indicated by blanks cells. We used log (v + 1) and square root transformations where nec-essary to improve normality and homogeneity of variances. Where data were unbalanced, we used Satterthwaite’s approximation,which results in fractional denominator degrees of freedom. Den d.f. = denominator degrees of freedom (numerator degrees offreedom for all effects = 1). All models included a random site effect (nested within latitude). Effects that are statistically signifi-cant at <0.05 are highlighted in bold – no post hoc correction for multiple tests has been employed

Source ofvariation

Prokelisia nymphs Prokelisia adults All Prokelisia (log) RGR grasshoppers Spider survival

Dend.f. F P

Dend.f. F P

Dend.f. F P

Dend.f. F P

Dend.f. F P

Latitude 8 0.37 0.56 8 2.34 0.16 8 1.73 0.22 2.6 0.19 0.70 7.7 0.12 0.73Fertilizer 56 18.26 < 0.0001 56 25.14 < 0.0001 56 25.69 < 0.0001 17.1 18.33 0.0005 41.7 2.20 0.15Mesopredator 56 0.00 0.96 56 0.25 0.62 56 0.45 0.504 20.3 0.71 0.409Omnivore 56 5.66 0.0208 56 3.40 0.071 56 5.47 0.023 41.2 0.00 0.99Lat 9 fert 56 2.11 0.15 56 0.34 0.56 56 1.75 0.19 17.1 0.01 0.98 41.7 1.15 0.29Lat 9 meso 56 5.34 0.025 56 1.06 0.31 56 2.07 0.16 20.3 0.01 0.94Lat 9 om 56 2.45 0.12 56 1.45 0.23 56 1.19 0.28 . 41.2 0.00 0.97Fert 9 meso 56 3.09 0.084 56 3.43 0.069 56 3.49 0.067 16.4 1.00 0.33Fert 9 om 56 4.01 0.050 56 4.69 0.035 56 5.43 0.024 41.7 0.25Meso 9 om 56 0.34 0.56 56 0.73 0.40 56 1.05 0.31 0.62Lat 9 fert9 meso

56 2.29 0.14 56 0.57 0.45 56 1.17 0.28 16.4 0.63 0.44

Lat 9 fert9 om

56 0.03 0.86 56 2.13 0.15 56 1.12 0.30 41.7 1.81 0.19

Lat 9 meso9 om

56 0.03 0.86 56 0.24 0.63 56 0.32 0.57

Fert 9 meso9 om

56 0.11 0.74 56 0.08 0.78 56 0.11 0.74

Lat 9 fert9 meso 9 om

56 0.05 0.82 56 1.44 0.24 56 0.55 0.46



populations than latitudinal variation in top consumers andcompetition.We anticipated interactions between top-down effects and

the nutrient status of Spartina in our mesocosms, and we sub-sequently observed that local (fertilized) differences in thenutritional status of Spartina modified the effects of both ka-tydids and spiders on herbivore populations. Predators wereable to suppress herbivores only on unfertilized plants, possi-bly because herbivores were concentrated on these smallerplants and had lower reproductive rates. At the same time,damage from omnivore populations was greatest on plantsthat did not receive fertilizer, again probably because omni-vores were concentrated on smaller, unfertilized plants andhad fewer insect prey as an alternative to feeding on plants.Control of consumers by local variation in plant quality isconsistent with some previous work on the Spartina foodweb. For example, Denno et al. (2002) found that enhancingthe nutrition of host plants did not strengthen top-downeffects on Prokelisia despite field-based evidence that preda-tor densities were also elevated on higher-quality plants.Instead, predators more effectively suppressed Prokelisia pop-ulations on poor-quality host plants (Denno et al. 2002). Incontrast, when Prokelisia are feeding on high-quality plants(in the case of the present experiment, fertilized plants), theyescape from effective predator control. Denno (2002) has pre-viously argued that this result is the key to understanding theseasonal migration of Prokelisia populations from the high tothe low marsh in high-latitude locations where high-quality

plants are only available seasonally in the low marsh due tosevere winter freezes.Similarly, Bertness et al. (2007) demonstrated that mixed

insect communities had little effect on Spartina productivityin relatively low-nutrient marshes in Rhode Island (US), whileincreasing levels of eutrophication triggered outbreaks oraggregations that led to herbivore control of marsh productiv-ity in eutrophic marshes. Nitrogen-rich Spartina are character-istic of low-marsh habitats (Denno 1983; Ornes & Kaplan1989) and herbivores are thought to be generally N-limited(White 1983; Huberty & Denno 2006), as we also found(Fig. 5a,b). Field studies have demonstrated that the highnitrogen content of low elevation Spartina plants encouragesmass colonization, enhances both survival and fecundity, andpromotes rapid population expansion of Prokelisia planthop-pers (Olmstead et al. 1997), and that nitrogen enhancementresults in a greater abundance of herbivores, predators andparasitoids across a large range of latitude (McCall &Pennings 2012). Our mesocosm experiment also demonstratedthese outbreak conditions on fertilized plants. In contrast, lati-tudinal variation in plant quality did not affect Prokelisia pop-ulations, omnivore growth rates or the effect of predators onherbivore populations.

WEAKER TOP-DOWN EFFECTS

Since the early studies by Teal (1962), salt marsh ecosystemshave been considered systems under strong bottom-up control,

0

50

100

150

200

250

300

350

400

P = 0.067

Abu

ndan

ce o

f Pro

kelis

ia (

indi

vidu

als/

plan

t)

Fertilized x mesopredator Fertilized x omnivore

(a) (b)

0

50

100

150

200

250

300

Abu

ndan

ce o

f Pro

kelis

ia (

indi

vidu

als/

plan

t)(c)

a

a a

b

– O + O– M + M– F + FLow High

– F + F – F + F

– M + M – M + M – O + O – O + O

P = 0.024

P < 0.0001 P = 0.023

Fig 4. Mesocosm experiment. Abundance ofProkelisia in mesocosms at the end of theexperiment. (a) Interaction of fertilizer andmesopredator presence. (b) Interaction offertilizer and omnivore presence. (c) Maineffects. Data are back-transformed lsmeansand 95% confidence intervals.



with primary productivity patterns being largely driven byphysical conditions and nutrient availability. More recentwork has championed top-down regulation of productivity insalt marshes by herbivores (snails: Silliman & Bertness 2002;insects: Finke & Denno 2004; geese: Kuijper & Bakker 2005;crabs: Altieri et al. 2012). Control of herbivore populationsmeanwhile appears to be regulated by a combination of bot-tom-up and top-down factors. In our mesocosm experiment,while both katydids and spiders successfully suppressed Prok-elisia populations, these consumer effects were consistentlymodified by bottom-up conditions and consumer effects didnot cascade to benefit plants.The effects of plant architecture on predator capture effi-

ciencies have been noted in salt marsh and other systems(Landis, Wratten & Gurr 2000). It is possible that in ourexperiment, predator suppression of herbivores on low-nitro-gen plants was due to the differences in physical structureand size of fertilized and control plants that altered the forag-ing efficiency of invertebrate predators. In particular, predatorforaging success is likely to have been higher on smaller,unfertilized plants. Alternately, suppression of Prokelisia pop-ulations on unfertilized plants by katydids and spiders

(Fig. 4a,b) might have occurred because Prokelisia popula-tions were reproducing poorly and individuals were less ableto escape predators due to feeding on a nutritionally poorfood source.

WEAK OR ABSENT TROPHIC CASCADES

In our mesocosm study, Orchelimum reduced Prokelisiaabundance; however, this did not cascade to indirectly benefitplants, probably because Orchelimum also negatively affectedplants by directly consuming them. Control of herbivoreabundance by spiders was generally weak (statistically dis-cernible at the experiment mid-point but not evident at itsconclusion), and this effect was not strong enough to cascadeto positively affect plant growth or other characteristics.While Orchelimum are capable of consuming substantial

quantities of Prokelisia planthoppers (Fig. 7), they appear tohave relatively inflexible diets that require them to also con-sume plant material (Jim�enez et al. 2012), and they maycontinue to eat high-quality plant tissue even when inverte-brate prey are also available. Several studies have suggested(Denno & Fagan 2003; Matsumura et al. 2004) that even a

0

200

400

600

800

1000

1200

0 0.5 1 1.5 2 2.5 3

Den

sity

of P

roke

lisia

(nu

mbe

r/g

plan

t bio

mas

s)

Percent foliar nitrogen

–0.025

–0.02

–0.015

–0.01

–0.005

0

0.005

0.01

0 0.5 1 1.5 2 2.5

Rel

ativ

e gr

owth

rat

e of

kat

ydid

s

Percent foliar nitrogen

(a)

(b)

Fig 5. Mesocosm experiment. (a) Relationship between percent foliarN and Prokelisia density (R2 = 0.16, P < 0.0001,). (b) Relationshipbetween percent foliar N and RGR of Orchelimum (R2 = 0.27,P = 0.022).

(a)

(b)

Fig 6. Mesocosm experiment. SEM model of the experimental Sparti-na food web imitating (a) high latitudes and (b) low latitudes. Themodel is consistent with the data (P = 0.70, chi-square d.f. = 0.78).Path coefficients describe standardized values showing relative effectsof variables upon each other. Arrow width is proportional to thestrength of the path coefficient; one headed arrows represent causal rela-tionships; nonsignificant relationships are marked with a dotted line.



small addition of protein in the diet of omnivores can resultin large improvements in nutrition and growth. Jim�enez et al.(2012) found that Orchelimum grew better on a mixed dietincluding both prey and plant material than on either singlediet alone. We found that Orchelimum exhibited greater rela-tive growth rates on plants with greater foliar nitrogen(Fig. 5b). This could have been because Orchelimum per-formed better when eating plants with higher nitrogen con-tent, or because Orchelimum were able to eat more prey onfertilized plants because Prokelisia were more abundant. Ineither case, both results are consistent with the idea thatOrchelimum is severely limited by N availability on a diet oflow-N Spartina. At the same time, Orchelimum grew betteron a mixed diet than on a diet of pure animal prey (Jim�enezet al. 2012), indicating that while plants and herbivores maybe somewhat substitutable foods (Van-Rijn & Sabelis 2005)for other marsh omnivores (Armases crabs, Ho & Pennings

2008), they are complementary for Orchelimum. Whetheromnivory acts to strengthen or weaken trophic cascades (Polis& Strong 1996; Eubanks & Styrsky 2005) may thus dependon how readily an omnivore can switch food sources. Thismay be particularly true in the case of true omnivores (thosethat consume both plant and animal tissue) where a prefer-ence for plant over animal tissue will serve to cancel cascad-ing effects of consuming herbivorous prey.

EXTRAPOLATING TO THE MORE DIVERSE COMMUNITY

IN THE F IELD

Our mesocosm experiments necessarily utilized a limitednumber of species. Although these were selected because theywere among the more common taxa in the field, this stillraises the question of whether the results can safely be extrap-olated to the more diverse field community. The predation

0

1

2

3

4

5

6

7

8

9

10

# P

roke

lisia

con

sum

ed/8

h

Prey = Prokelisia(a)

Hogna Pardosa Marpissa coccinellid Orchelimumadults

Hogna Pardosa Marpissa Salticid sp Orchelimumadults

0

0.02

0.04

0.06

0.08

0.1

0.12

0.14

# O

rche

limum

con

sum

ed/8

h

Prey = fifth-instar Orchelimum

(b)

Hogna Marpissa Hogna Orchelimum adults

0

0.2

0.4

0.6

0.8

1

1.2

1.4

1.6

1.8

2

# P

rey

cons

umed

/8 h

Prey = Ischnodemus badius Prey = Marpissa sp. Prey = Trigonotylus sp.

(c)Prey = mixed trials

273

47

4

15

11

4 4 11

10

9

5

6

Fig 7. Predation trials. Predator success over8 h with (a) Prokelisia or (b) fifth-instarOrchelimum as the prey item and (c) inaddition predator–prey pairings using otherintermediate-sized arthropods common in theSpartina community as prey items. Numeralsindicate sample size in each trial.



trials suggest that they can, albeit with an important caveat.First, all the moderately sized arthropod herbivores that wetested (Prokelisia, Ischnodemus and Trigonotylus) were read-ily eaten by common predators. Second, with the exception ofa salticid spider that we did not identify to species, all thepredators that we tested (three other spiders, a beetle andOrchelimum) readily consumed at least one of the herbivorespecies tested. Thus, although the precise predation rates inany particular setting would depend on the densities of thedifferent taxa and the differences in vulnerability of particularherbivores to particular predators, the predator–prey interac-tions in this community appear to be relatively generalized.As a result, the various less-common herbivore species arelikely to be affected by predators and top omnivores in muchthe same way that Prokelisia was affected.The major caveat with extending our results to the more

diverse field community is that the multiplicity of predatorytaxa in the field (e.g. at least six common spiders and anothersix or more rare species, Wimp et al. 2010; authors personalobservations) greatly increases the potential for intraguild pre-dation between predators. Depending on variation in predatordensity, and on the extent to which various predators interferewith vs. facilitate each other, our mesocosm results may impre-cisely estimate predation rates in the field (Schmitz, Beckerman& O’Brien 1997; Finke & Denno 2004). No doubt the detailsof the trophic ecology of each of the predators differs some-what. Nevertheless, because almost all the consumers tested(with the exception of one spider) readily ate the commonarthropod herbivores, it is most likely that the relatively diversepredator assemblage found in the field has a negative effect onProkelisia populations that is broadly consistent with the meso-cosm results based on the single common predator Pardosa. Insum, although there is much to be learned about how herbivoreand predator diversity affects the functioning of the Spartinaarthropod community, we are confident that our mesocosmexperiments, despite being stocked with only a few species,provide a robust first-order approximation of how the morediverse field community functions.Fully understanding geographic variation in the Spartina

food web will need to consider the full suite of herbivoresincluding snails (Silliman & Zieman 2001), crabs (Altieriet al. 2012) and vertebrates (Buchsbaum, Valiela & Swain1984). A complete consideration of these herbivores, and theirinteractions with insect herbivores, awaits further study; how-ever, we speculate that the principles that we have outlinedhere for insect herbivores also apply to these other herbivores.For example, herbivorous Sesarma crabs are most abundantnear high-quality, tall-form Spartina plants (Teal 1958), andper capita snail effects on Spartina are greatest on tall-formplants (Silliman & Bertness 2002). Snails experience thestrongest top-down control from predators on high-qualitycreekside instead of low-quality platform plants, but this issimply because their predators are of marine rather than ter-restrial origin (Silliman & Bertness 2002). Snail herbivory ismost important at low latitudes due to a turnover in the mostcommon taxa across latitude (Pennings & Silliman 2005),paralleling the many salt marsh insect herbivores that are

more abundant at low latitudes (Pennings et al. 2009). Thus,for snails and crabs, the primary factors controlling local andgeographic variation in herbivore abundance may be the samefactors that affect insect herbivores: local variation in plantquality and geographic variation in species composition. Thissuggests that we are close to a conceptual unification of thefactors mediating the distribution and abundance of salt marshherbivores at both local and geographic scales.

COMPARING LOCAL AND GEOGRAPHIC PATTERNS

Taken as a whole, our results suggest that the single mostimportant factor mediating Prokelisia densities is local varia-tion in plant quality between short- and tall-form plants. Pre-dation pressure can be important, but only on low-qualityplants, because herbivores escape from predator control onhigh-quality plants. Similarly, although plants demonstrablyvary in quality across latitude, and this has measurable effectson herbivore performance (Ho, Pennings & Carefoot 2010),the effects of latitudinal variation on herbivore abundancetend to be overwhelmed by other factors.Our experiments did not address factors extrinsic to the food

web such as climate, but the short growing season and colderwinters at high latitudes are the most likely reasons why highlatitudes are characterized by a reduced number of generationsin multivoltine species such as Prokelisia (Friedenberg et al.2008), a reduced body size of some univoltine species such asOrchelimum (Wason & Pennings 2008; Ho, Pennings & Care-foot 2010) and a reduced density of some other members of thefood web (Pennings et al. 2009; McCall & Pennings 2012).In sum, we argue that a first-order understanding of varia-

tion in the Spartina arthropod food web at geographic scalesconsists of two variables: geographic variation in climate,which mediates the density and body size of different mem-bers of the food web in ways that are not yet well studied;and local variation in plant quality, which provides strongbottom-up forcing to herbivore populations. A second-orderunderstanding of the arthropod food web needs to also con-sider predation, which is most effective at controlling herbi-vores feeding on low-quality plants (Denno, Lewis & Gratton2005). Finally, latitudinal variation in plant quality probablyexplains some variation in herbivore densities and body size,but is probably more of a response to herbivore pressure(Pennings et al. 2009) than a driver of it.

Acknowledgements

We thank the National Science Foundation (DEB-0296160, DEB-0638813,OCE06-20959) for funding and two anonymous reviewers for their constructivecommentary. This work is a contribution of the Georgia Coastal EcosystemLong-Term Ecological Research programme and contribution number 1030from the University of Georgia Marine Institute.

References

Altieri, A.H., Bertness, M., Coverdale, T.C., Herrmann, N.C. & Angelini, C.(2012) A trophic cascade triggers collapse of a salt-marsh ecosystem withintensive recreational fishing. Ecology, 93, 1402–1410.



Bertness, M. (2007) Atlantic Shorelines: Natural History and Ecology. Prince-ton University Press, Princeton, New Jersey.

Bertness, M. & Shumway, S.W. (1992) Salt stress limitation of seedling recruit-ment in a salt marsh plant community. Oecologia, 92, 490–497.

Bertness, M.D., Wise, C. & Ellison, A.M. (1987) Consumer pressure and seedset in a salt marsh perennial plant community. Oecologia, 71, 190–200.

Bertness, M., Crain, C.M., Holdredge, C. & Sala, N.M. (2007) Eutrophicationand consumer control of New England salt marsh primary productivity. Con-servation Biology, 22, 131–139.

Blanchette, C., Miner, C., Raimondi, P., Lohse, C., Heady, K. & Broitman, B.(2008) Biogeographical patterns of rocky intertidal communities along thePacific coast of North America. Journal of Biogeography, 35, 1593–1607.

Buchsbaum, R., Valiela, I. & Swain, T. (1984) The role of phenolic-compoundsand other plant constituents in feeding by Canada Geese in a coastal marsh.Oecologia, 63, 343–349.

Dayton, P. (1984) Properties structuring some marine communities: are theygeneral? Ecological Communities: Conceptual Issues and the Evidence (ed.D.S.D. Strong, L. Abele & A. Thistle), pp. 181–197. Princeton UniversityPress, Princeton, New Jersey.

Denno, R.F. (1983) Tracking variable host plants in space and time. VariablePlants and Herbivores in Natural and Managed Systems (eds R.F. Denno &M.S. McClure), pp. 291–341. Academic Press, New York.

Denno, R.F. & Fagan, W.F. (2003) Might nitrogen limitation promote omni-vory among carnivorous arthropods? Ecology, 84, 2522–2531.

Denno, R.F., Lewis, D. & Gratton, C. (2005) Spatial variation in the relativestrength of top-down and bottom-up forces: causes and consequences forphytophagous insect populations. Annales Zoologici Fennici, 42, 295–311.

Denno, R.F., McClure, M.S. & Ott, J.R. (1995) Interspecific interactions inphytophagous insects - competition reexamined and resurrected. AnnualReview of Entomology, 40, 297–331.

Denno, R.F., Schauff, M.E., Wilson, S.W. & Olmstead, K.L. (1987) Practicaldiagnosis and natural-history of 2 sibling salt marsh-inhabiting planthoppersin the Genus Prokelisia (Homoptera, Delphacidae). Proceedings of the Ento-mological Society of Washington, 89, 687–700.

Denno, R.F., Roderick, G.K., Peterson, M.A., Huberty, A.F., Dobel, H.,Eubanks, M.D., Losey, J.E. & Langellotto, G.A. (1996) Habitat persistenceunderlies the intraspecific dispersal strategies of planthoppers. EcologicalMonographs, 66, 389–408.

Denno, R.F., Peterson, M.A., Gratton, C., Cheng, J.A., Langellotto, G.A.,Huberty, A.F. & Finke, D.L. (2000) Feeding-induced changes in plant qual-ity mediate interspecific competition between sap-feeding herbivores. Ecol-ogy, 81, 1814–1827.

Denno, R.F., Gratton, C., Peterson, M.A., Langellotto, G.A., Finke, D.L. &Huberty, A.F. (2002) Bottom-up forces mediate natural-enemy impact in aphytophagous insect community. Ecology, 83, 1443–1458.

Denno, R.F., Gratton, C., Dobel, H. & Finke, D.L. (2003) Predation risk affectsrelative strength of top-down and bottom-up impacts on insect herbivores.Ecology, 84, 1032–1044.

Denno, R.F., Mitter, M.S., Langellotto, G.A., Gratton, C. & Finke, D.L. (2004)Interactions between a hunting spider and a web-builder: consequences of in-traguild predation and cannibalism for prey suppression. Ecological Entomol-ogy, 29, 566–577.

Ehrlich, P.R. & Birch, L.C. (1967) Balance of nature and population control.American Naturalist, 101, 97–107.

Eubanks, M.D. & Denno, R.F. (2000) Host plants mediate omnivore-herbivoreinteractions and influence prey suppression. Ecology, 81, 936–947.

Eubanks, M.D. & Styrsky, J.D. (2005) Effects of plant feeding on the performanceof omnivorous “predators”. Plant-Provided Food and Herbivore-CarnivoreInteractions (eds F.L. Wackers, P.C. Van-Rijn & J. Bruin), pp. 148–177. Cam-bridge University Press, Cambridge.

Finke, D.L. & Denno, R.F. (2004) Predator diversity dampens trophic cascades.Nature, 429, 407–410.

Finke, D.L. & Denno, R.F. (2006) Spatial refuge from intraguild predation:implications for prey suppression and trophic cascades. Oecologia, 149, 265–275.

Friedenberg, N.A., Sarkar, S., Kouchoukos, N., Billings, R.F. & Ayres, M.P.(2008) Temperature extremes, density dependence and southern pine beetle(Coleoptera: Curculionidae) population dynamics in east texas. Environmen-tal Entomology, 37, 650–659.

Goeriz Pearson, R.E., Behmer, S.T., Gruner, D.S. & Denno, R.F. (2011)Effects of diet quality on performance and nutrient regulation in an omnivo-rous katydid. Ecological Entomology, 36, 471–479.

Goranson, C.E., Ho, C.K. & Pennings, S.C. (2004) Environmental gradientsand herbivore feeding preferences in coastal salt marshes. Oecologia, 140,591–600.

Grace, J.B. (2006) Structural Equation Modelling and Natural Systems. Cam-bridge University Press, Cambridge.

Gruner, D.S. (2004) Attenuation of top-down and bottom-up forces in a com-plex terrestrial community. Ecology, 85, 3010–3022.

Hairston, N.G., Smith, F.E. & Slobodkin, L.B. (1960) Community structure,population control, and competition. American Naturalist, 94, 421–425.

Ho, C.K. & Pennings, S.C. (2008) Consequences of omnivory for trophic inter-actions on a salt marsh shrub. Ecology, 89, 1714–1722.

Ho, C.K., Pennings, S.C. & Carefoot, T.H. (2010) Is diet quality an over-looked mechanisms for Bergmann’s Rule? The American Naturalist, 175,269–276.

Huberty, A.F. & Denno, R.F. (2006) Consequences of nitrogen and phosphoruslimitation for the performance of two planthoppers with divergent life-historystrategies. Oecologia, 149, 444–455.

Hunter, M.D. & Price, P.W. (1992) Playing chutes and ladders - heterogeneityand the relative roles of bottom-up and top-down forces in natural communi-ties. Ecology, 73, 724–732.

Jim�enez, J., Wiezski, K., Marczak, L.B., Ho, C.K. & Pennings, S.C. (2012)Effects of an omnivorous Katydid, salinity, and nutrients on a planthopper-Spartina food web. Estuaries and Coasts, 35, 475–485.

Kuijper, D.P.J. & Bakker, J.P. (2005) Top-down control of small herbivoreson salt-marsh vegetation along a productivity gradient. Ecology, 86, 914–923.

Landis, D.A., Wratten, S.D. & Gurr, G.M. (2000) Habitat management to con-serve natural enemies of arthropod pests in agriculture. Annual Review ofEntomology, 42, 175–210.

Marczak, L.B., Ho, C.K., Wieski, K., Vu, H., Denno, R.F. & Pennings, S.C.(2011) Latitudinal variation in top-down and bottom-up control of a saltmarsh food web. Ecology, 92, 276–281.

Matsumura, M., Trafelet-Smith, G.M., Gratton, C., Finke, D.L., Fagan, W.F. &Denno, R.F. (2004) Does intraguild predation enhance predator performance?A stoichiometric perspective. Ecology, 85, 2601–2615.

McCall, B.D. & Pennings, S.C. (2012) Geographic variation in salt marshstructure and function. Oecologia, 170, 777–787.

McGeoch, M.A. & Price, P.W. (2005) Scale-dependent mechanisms in the pop-ulation dynamics of an insect herbivore. Oecologia, 144, 278–288.

McKee, K.L. & Patrick, W.H. Jr (1988) The relationship of smooth Cordgrass(Spartina alterniflora) to tidal datums: a review. Estuaries, 11(3), 143–151.

Mendelssohn, I.A. & Morris, J.T. (2000) Eco-physiological controls on the pro-ductivity of Spartina alterniflora Loisel. Concepts and Controversies in TidalMarsh Ecology (ed. M.P.W.a.D.A. Kreeger), pp. 59–80. Kluwer AcademicPublishers, Dordrecht.

Olmstead, K.L., Denno, R.F., Morton, T.C. & Romeo, J.T. (1997) Influence ofProkelisia planthoppers on the amino acid composition and growth of Sparti-na alterniflora. Journal of Chemical Ecology, 23, 303–321.

Ornes, W.H. & Kaplan, D.I. (1989) Macronutrient status of tall and short forms ofSpartina alterniflora in a South Carolina salt marsh. Marine Ecology-ProgressSeries, 55, 63–72.

Pennings, S.C. & Silliman, B.R. (2005) Linking biogeography and communityecology: latitudinal variation in plant-herbivore interaction strength. Ecology,86, 2310–2319.

Pennings, S.C., Siska, E.L. & Bertness, M.D. (2001) Latitudinal differences inplant palatability in Atlantic coast salt marshes. Ecology, 82, 1344–1359.

Pennings, S.C., Ho, C.K., Salgado, C.S., Wiezski, K., Dave, N., Kunza, A.E. &Wason, E.L. (2009) Latitudinal variation in herbivore pressure in AtlanticCoast salt marshes. Ecology, 90, 183–195.

Polis, G.A. & Strong, D.R. (1996) Food web complexity and communitydynamics. The American Naturalist, 147, 813–846.

Post, E. (2005) Large-scale spatial gradients in herbivore population dynamics.Ecology, 86, 2320–2328.

Quinn, G.P. & Keough, M.J. (2002) Experimental Design and Data Analysisfor Biologists. Cambridge University Press, Cambridge.

Sala, N.M., Bertness, M.D. & Silliman, B.R. (2008) The dynamics of bottom-up and top-down control in a New England salt marsh. Oikos, 117, 1050–1056.

Salgado, C.S. & Pennings, S.C. (2005) Latitudinal variation in palatability ofsalt-marsh plants: are differences constitutive? Ecology, 86, 1571–1579.

Schmitz, O.J., Beckerman, A.P. & O’Brien, K.M. (1997) Behaviourally medi-ated trophic cascades: effects of predation risk on food web interactions.Ecology, 78, 1388–1399.

Silliman, B.R. & Bertness, M.D. (2002) A trophic cascade regulates salt marshprimary production. Proceedings of the National Academy of Sciences, 99,105000–110505.



Silliman, B.R. & Zieman, J.C. (2001) Top-down control of Spartina alternifl-ora production by periwinkle grazing in a Virginia salt marsh. Ecology, 82,2830–2845.

Siska, E.L., Pennings, S.C., Buck, T.L. & Hanisak, M.D. (2002) Latitudinalvariation in palatability of salt-marsh plants: which traits are responsible?Ecology, 83, 3369–3381.

Stiling, P., Brodbeck, B.V. & Strong, D.R. (1991) Population increases ofplanthoppers on fertilized salt-marsh cord grass may be prevented by grass-hopper feeding. Florida Entomologist, 74, 88–97.

Stiling, P. & Moon, D. (2005) Are trophodynamic models worth their salt? Top-down and bottom-up effects along a salinity gradient. Ecology, 86, 1730–1736.

Stiling, P. & Rossi, A.M. (1997) Experimental manipulations of top-down andbottom-up factors in a tri-trophic system. Ecology, 78, 1602–1606.

Teal, J.M. (1958) Distribution of fiddler crabs in Georgia salt marshes. Ecology,39, 185–193.

Teal, J.M. (1962) Energy flow in the salt marsh ecosystem of Georgia. Ecol-ogy, 43, 614–624.

Valiela, I., Teal, J.M. & Deuser, W.G. (1978) The nature of growth forms in thesalt marsh grass Spartina alterniflora. The American Naturalist, 112, 461–470.

Van-Rijn, P.C. & Sabelis, M.W. (2005) Impact of plant-provided food on her-bivore-carnivore dynamics. Plant-Provided Food for Carnivorous Insects: AProtective Mutualism and its Applications (eds P.C. Van-Rijn, F.L. Wackers,T.K. Wilkinson & S.D. Wratten), pp. 223–266. Cambridge University Press,Cambridge.

Walker, M. & Jones, T.H. (2001) Relative roles of top-down and bottom-upforces in terrestrial tritrophic plant-insect herbivore-natural enemy systems.Oikos, 93, 177–187.

Wason, E.L. & Pennings, S.C. (2008) Grasshopper (Orthoptera: Tettigoniidae)species composition and size across latitude in Atlantic Coast salt marshes.Estuaries and Coasts, 31, 335–343.

White, T.C.R. (1983) The Inadequate Environment: Nitrogen and the Abun-dance of Animals. Springer-Verlag, Berlin.

Wimp, G.M., Murphy, S.M., Finke, D.L., Huberty, A.F. & Denno, R.F. (2010)Increased primary production shifts the structure and composition of a terres-trial arthropod community. Ecology, 91, 3303–3311.

Received 25 January 2013; accepted 13 June 2013Handling Editor: Martin Heil



importance of local vs. geographic variation in salt marsh plant quality for arthropod herbivore

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