Journal of Ecology 2013, 101, 1169–1182
doi: 10.1111/1365-2745.12137
Importance of local vs. geographic variation in salt
marsh plant quality for arthropod herbivore
communities
Laurie B. Marczak1,2*†, Kazimierz Wiez ski1, Robert F. Denno2 and Steven C. Pennings1
1
Department of Biology and Biochemistry, University of Houston, Houston, TX 77204, USA; and 2Department of
Entomology, University of Maryland, College Park, MD 20742, USA
Summary
1. An important recent advance in food web ecology has been the application of theory regarding
spatial gradients to studies of the factors that affect animal population dynamics. Building on extensive studies of the Spartina alterniflora food web at the local scale, we hypothesized that geographic
variation in S. alterniflora quality is an important bottom-up control on food web structure and that
geographic variation in S. alterniflora quality would interact with the presence of predators and top
omnivores to mediate herbivore densities.
2. We employed a four-factor fully crossed experiment in which we (i) collected plants from highand low-latitude locations and grew them in a common garden and varied (ii) plant fertilization status (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 is
local variation in plant quality – induced in our experiment by fertilization and demonstrated
repeatedly as a consequence of marsh elevation.
4. Top-down effects were generally weak and in those cases where predators did exert a significant
suppressing 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 measurable
effects of this variation on herbivores, geographic-scale variation in plant quality was overwhelmed
by local conditions in our experiments.
6. Synthesis. We suggest that a first-order understanding of variation across large latitudinal ranges in
the Spartina alterniflora arthropod food web must begin with local variation in plant quality, which
provides strong bottom-up forcing to herbivore populations. A second-order understanding of the
arthropod food web should consider the role of predation in controlling herbivores feeding on lowquality plants. Finally, while latitudinal variation in plant quality probably explains some variation in
herbivore densities, it is probably more of a response to herbivore pressure than a driver of the herbivore dynamics. Although extrapolating from local to geographic scales presents multiple challenges, it
is 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 been
the application of theory regarding spatial gradients to studies of the factors that affect animal population dynamics
*Correspondence author. E-mail: [email protected]
† Present address: Department of Ecosystem and Conservation Sciences, The University of Montana - Missoula, MO 59812, USA.
(McGeoch & Price 2005; Post 2005). Historically, ecologists debated the importance of top-down (Hairston, Smith
& Slobodkin 1960) and bottom-up (Ehrlich & Birch 1967)
factors in regulating herbivore populations, but most ecologists now agree that these factors interact, sometimes in
complex ways, to influence population dynamics (Hunter &
Price 1992). With this new, nuanced perspective, ecologists
are now asking how variation in abiotic factors and community composition across landscapes affects the relative
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society
1170 L. B. Marczak et al.
importance of top-down and bottom-up forces (Walker &
Jones 2001; Denno, Lewis & Gratton 2005). Most of this
work has focused on local and regional scales, with few
studies at large geographic (= continental) scales that span
large gradients in climate, oceanographic drivers or soil
type (but see Blanchette et al. 2008; Marczak et al. 2011;
McCall & Pennings 2012). As a result, we currently have
a poor understanding of the extent to which factors mediating variation in community structure at local scales also
matter at geographic scales. Thus, an important task for
ecologists is to expand our studies of local landscapes to
the geographic scale in order to better understand
geographic variation in community structure.
Salt marshes on the Atlantic Coast of the United States are
ideal systems for comparing local and geographic variations
in community structure. Atlantic Coast salt marshes consist of
relatively simple communities of plants and animals that are
broadly similar in composition across a large range of latitude
and climate from Central Florida through to Maine (Pennings,
Siska & Bertness 2001). In particular, lower elevations of
marshes throughout this geographic range are dominated by a
single plant species, salt marsh cordgrass, Spartina alterniflora (Bertness 2007), with its associated herbivores (Denno
et al. 1987; Pennings et al. 2009). This apparent simplicity,
however, conceals considerable variation at both local and
geographic spatial scales.
At the local scale, S. alterniflora plants close to creekbanks
are larger, richer in nitrogen, lower in phenolics and more
palatable to herbivores than the plants from the high marsh
(Ornes & Kaplan 1989; Goranson, Ho & Pennings 2004;
Denno, Lewis & Gratton 2005). Within local marshes, planthoppers migrate seasonally to creekbanks, departing as winter
conditions make this habitat unsuitable (Denno 1983).
Mesopredators (spiders) also migrate from high-marsh to
low-marsh habitats seasonally (Finke & Denno 2006). As a
consequence of this variation in plant quality and predator
distribution, top-down and bottom-up forces on herbivores
vary 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 palatable to herbivores than conspecific plants from the same habitats at low latitudes (Pennings, Siska & Bertness 2001; Siska
et al. 2002; Salgado & Pennings 2005). Planthopper herbivores show little variation in density with latitude, but herbivorous snails are more abundant at low latitudes (Pennings
et al. 2009). Spiders are present at all latitudes, but top omnivores (katydids) are most abundant at low latitudes (Pennings
et al. 2009). The consequences of geographic variation in
plant quality and predator distribution for herbivore populations are poorly understood (but see Marczak et al. 2011;
McCall & Pennings 2012).
An additional complication in understanding the geographic variation of arthropod community structure is that
the trophic impacts of omnivores are ambiguous. Omnivores
may sustain their population levels when prey are scarce by
eating plants (Dayton 1984; Eubanks & Denno 2000),
resulting in increased predation pressure on herbivores when
herbivores are present. Alternately, omnivores may become
satiated faster by eating at multiple trophic levels, reducing
their per capita consumption of any particular prey (Eubanks
& Denno 2000). Omnivory may thus either enhance or attenuate top-down effects (Denno et al. 2002; Ho & Pennings
2008), and variation in the abundance of omnivores or the
strength of their interactions may be important factors in
determining the structure of food webs across large latitudinal gradients.
In sum, we have a reasonable understanding of how topdown and bottom-up forces interact to explain variation in
herbivore densities over small elevational gradients (creekbank vs. mid-marsh) within single marshes. In contrast,
although we know that plant quality and predator/omnivore
densities vary geographically, we have little understanding of
how these factors interact to mediate geographic variation in
herbivore densities. Previous work suggests that enhanced
plant nutrient status may allow herbivores to escape from
predator control either through nutritional benefits leading to
rapid population growth (Denno et al. 2002) or because predator search times are increased on plants with higher biomass
(Olmstead et al. 1997). Here, we compare the importance of
local vs. geographic controls on arthropod communities, using
Spartina alterniflora and associated arthropods as a model
system. To explore how local and geographic variation in
plant quality and food web composition might affect Spartina
herbivore dynamics, we conducted a mesocosm study that
varied (i) plant provenance (plant quality derived from the latitudinal gradient), (ii) fertilization status (mimicking plant
quality differences due to marsh elevation), and the presence
of (iii) mesopredators (the spider Pardosa littoralis) and (iv)
omnivores (the katydid Orchelimum fidicinium). To further
understand the results of this mesocosm experiment and
extrapolate to more complicated food webs in the field, we
conducted predation trials in the laboratory to determine the
rates at which different species from the Spartina food web
feed on each other (a subset of the most abundant taxa from
field collections: four spiders, a beetle and Orchelimum adults
as predators and three additional prey species). Building on
extensive studies of the S. alterniflora food web at the local
scale that have shown a strong bottom-up effect of local variation in plant quality (Denno et al. 2002, 2003; Denno, Lewis
& Gratton 2005), we hypothesized that geographic variation
in S. alterniflora quality was also an important bottom-up
control on food web structure and that local and geographic
variation in S. alterniflora quality would interact with the
presence of predators and top omnivores to strongly mediate
herbivore densities.
Materials and methods
THE SPARTINA FOOD WEB
On the Atlantic Coast of North America, salt marshes dominated by
Spartina alterniflora (henceforth Spartina) range from peninsular
Florida 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
Local vs. geographic variation in plant quality 1171
2001). Spartina plants from high latitudes (RI to ME, 41–43°) are
more nutritious (% N) and tender than conspecific plants from low
latitudes (GA to FL, 30–31°) (Salgado & Pennings 2005; McCall &
Pennings 2012). Moreover, the concentration of phenolics in Spartina
is 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 the
laboratory using a variety of herbivores demonstrated that both polar
extracts (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 are
known to be more nutritious, softer, less defended and more palatable
than 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 & Deuser
1978). Tall-form plants close to creekbanks are larger, richer in
nitrogen (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 in
phenolics and more palatable to herbivores than plants from the high
marsh (Ornes & Kaplan 1989; Goranson, Ho & Pennings 2004;
Denno, Lewis & Gratton 2005). Nitrogen is more available to plants
at creekbanks than in the high marsh (Mendelssohn & Morris 2000),
and fertilization experiments have demonstrated that the nutritional
status of tall Spartina (TS) and short Spartina (SS) generally
accounts for the majority of the phenotypic differences between the
height forms (Valiela, Teal & Deuser 1978). Consequently, fertilization is a common experimental practice used to mimic variation
between tall- and short-form plants in greenhouse experiments
(Denno et al. 2002).
By far, the most common herbivores of Spartina are the delphacid
planthoppers Prokelisia marginata and P. dolus (Denno et al. 2002).
Prokelisia marginata and P. dolus (hereafter, Prokelisia) are multivoltine, with a summer generation time of 5–6 weeks (Stiling &
Rossi 1997). They are phloem sap-feeders that can reach densities
exceeding several thousand adults per m2 with nymphal densities
greater than 10 000 per m2 (Denno 1983). A number of invertebrate
predators are common in Spartina stands, including spiders and
coccinellid beetles. The hunting spiders Hogna modesta (hereafter
Hogna) and Pardosa littoralis (hereafter, Pardosa) are particularly
common and are known to suppress planthopper populations (Denno
et al. 2004) except when planthoppers experience ‘outbreaks’ on
high-nitrogen host plants (Denno et al. 2004; Huberty & Denno
2006). In our mesocosm experiment, we used Pardosa as a wellstudied representative of the Spartina predator community that is
abundant across the entire latitudinal range of our study; other predators were included in predation trials to help us generalize the experimental results across the Spartina community. The most common
true omnivore in the Spartina zone of south-eastern salt marshes is
the tettigoniid katydid Orchelimum fidicinium (hereafter, Orchelimum) (Pennings et al. 2009). Although historically regarded as an
herbivore (Teal 1962), Orchelimum, like most tettigoniids, is omnivorous and readily eats small arthropods (Jimenez et al. 2012).
Orchelimum is univoltine, with adult densities reaching 9.6 individuals per m2 (Stiling, Brodbeck & Strong 1991). At high latitudes,
Orchelimum is replaced by the smaller tettigoniid Conocephalus
spartinae (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 drivers
of herbivore density by varying four factors in a fully crossed design:
(i) plant provenance (constitutive plant quality derived from the latitudinal gradient), (ii) fertilization (causing plant quality differences to
mimic those related to marsh elevation), and the presence of a dominant species of both (iii) mesopredator (the spider Pardosa littoralis)
and (iv) omnivore (the katydid Orchelimum fidicinium). We collected
Spartina from five high-latitude sites and five low-latitude sites
(Table 1) and established mesocosms with two levels each of fertilizer level (fertilized and unfertilized), mesopredator density (0 or 3)
and omnivore density (0 or 1). These treatments were crossed in a
full factorial design for a total of 80 mesocosms with five replicates
per treatment where each replicate contained field-collected plants
from a single site of the appropriate latitude (site was thus nested
within latitude). Each mesocosm was stocked with 25 herbivores
(Prokelisia). Initial Prokelisia, spider and katydid densities were
selected to represent average densities that occur naturally on the
marsh (Denno et al. 1996; Ho & Pennings 2008).
Plants (short-form plants from the marsh platform) were collected
from field locations between 18 and 22 May 2009 and established in
mesocosm containers (each mesocosm consisting of four Spartina
stems 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 outdoor
greenhouse with a roof to block rain but no walls, thereby keeping
plants at close to ambient temperature and humidity, at the University
of Georgia Marine Institute on Sapelo Island GA (31°27′ N; 81°16′
W). Beginning on June 2 of 2009, mesocosms assigned to the fertilizer treatment received 9.5 g of fertilizer (Ultra Vigoro Plant Food, 125-7, Madison, Wisconsin, USA) every week for 4 weeks prior to the
beginning of the experiment and every second week after the experiment had begun. On 19 June 2009, after plants had acclimated to
greenhouse 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 damage to leaves, chlorophyll content measured with an OPTI-Sciences
CCM-200 chlorophyll metre) and placed 5 g of (dry weight) dead
Spartina stems and leaves at the base of each plant to provide habitat
structure for spiders. Each mesocosm was fitted with a mesh cage
consisting of lightweight fabric supported by bamboo stakes. The
mesh cages reduced incident light by c. 18%. Although this design
placed plants from high and low latitudes in a common garden, differences in the palatability of high- vs. low-latitude Spartina plants persisted for more than a year and five clonal generations in a previous
common garden experiment, we saw no evidence for local feeding
preferences 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
Great Neck
100 Acres
Rumstick Cove
Cottrell Marsh
Baruch
Ace Basin
Eulonia
Airport/Dean Creek
Amelia
MA
MA
RI
RI
CT
SC
SC
GA
GA
FL
42.44
42.42
41.46
41.43
41.20
33.22
32.33
31.54
31.23
30.40
High
High
High
High
High
Low
Low
Low
Low
Low
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1169–1182
1172 L. B. Marczak et al.
and differences observed in the common garden were sufficient to
explain differences in palatability observed in freshly collected field
plants (Salgado & Pennings 2005). Thus, we expect that the ‘latitudinal signal’ of plant quality was fully maintained in this common garden experiment.
On 21 June 2009, we field-collected spiders (Pardosa littoralis)
and katydids (Orchelimum sp.) in Georgia and held them in the laboratory. On 22–23 June 2009, we collected Prokelisia from the field in
Georgia and placed 25 individuals in each mesocosm. We allowed
the Prokelisia to disperse within each mesocosm and added spiders
(Pardosa) the following day. Katydids (Orchelimum) were introduced
4 h after the addition of spiders. Once mesocosms were fully stocked
according to the treatment (26 June 2009), we positioned each mesocosm haphazardly across the greenhouse. A limited number of variables (number of Prokelisia, Orchelimum and Pardosa) were
measured 2 weeks into the experiment to assess the potential for outbreak dynamics; variables relating to plant quality could not be determined because of the risk of escape by arthropods. Mesocosms were
broken down and resampled after 6 weeks (12 August 2009) once it
became apparent that herbivores were reproducing rapidly in some
treatments and consuming entire plants.
We used mixed-model nested ANOVAS to assess the effect of treatments for individual response variables where site was nested within
latitude (random) and latitude, fertilizer, spider density and katydid
density were fully crossed fixed factors. Relative growth rate of plants
was calculated as the natural log +1 of the final number of green
leaves minus the natural log +1 of the initial number of green leaves,
divided by the duration (days) of the experiment. Katydid relative
growth rates were calculated analogously as the natural log of final
mass minus the natural log of initial mass, divided by the duration
(days) of time in the experiment. Growth rates could not be similarly
calculated for spiders because we were unable to mark individuals; a
group estimate of change in biomass was hindered by low survival
rates (many zeros). Accordingly, we used survival as our variable of
interest for spiders. We estimated initial plant biomass allometrically
based on the height of all shoots (cm) in each plant mesocosm at the
start of the experiment; final plant biomass was determined by clipping, drying and weighing all the above-ground live biomass (g).
Leaves from each of these plants were lyophilized and analysed for
total nitrogen content at the University of Georgia Chemical Analysis
Laboratory, Athens, Georgia, USA. We used log (v + 1) and square
root transformations where necessary to improve the normality and
heterogeneity of variances. Where data were unbalanced, we
employed Satterthwaite’s approximation (as recommended by Quinn
& Keough 2002) that results in fractional denominator degrees of
freedom.
A potential weakness of the ANOVA approach is that it does not
account for the fact that some variables (e.g. herbivore numbers, plant
traits) are both responding to and simultaneously driving other variables. Thus, we also analysed results of the mesocosm experiment
using structural equation modelling (SEM) that allows a variable to
be simultaneously influenced by other variables and cause variation in
a dependent variable (Grace 2006). We were particularly interested in
using SEM to test the hypotheses that there would be an interaction
between fertilization and top-down effects, that any effect of fertilization on Prokelisia would be mediated through increased plant biomass and N content and that fertilization would decrease damage to
plants by increasing plant biomass (a dilution effect). Building an
SEM model consists of several consecutive steps. It starts with a priori identification of the causal relationships between the interplaying
variables, followed by the estimation of the path parameters
performed by screening the matrix of covariances over the hypothetical model. Finally, model fit is determined by comparing the predicted matrix of covariances with that from the original data.
Parameters of the model were estimated using AMOS 7.0 (Amos
Development Corporation, Mount Pleasant, South Carolina, USA)
with the maximum likelihood method, and the model fit was tested
by the likelihood chi-square value.
PREDATION TRIALS
To broaden our understanding of the trophic interactions and to determine the rates at which different species within the Spartina food
web feed on each other, we conducted cannibalistic trials and predation trials in the laboratory including animals not used in our experimental food web but which were numerically dominant in the field at
the time of the experiment. Trials for cannibalism included Orchelimum adults that were enclosed with 5th instar Orchelimum juveniles
(last instar before maturation). The Orchelimum adults were 24% larger (tibia or body length) than the juveniles. Predation trials included
six predators (four spiders, a beetle and Orchelimum adults), as well
as the mirid bug Trigonotylus sp. and the lygaeid bug Ischnodemus
badius as potential prey. Trials were conducted in June and July of
2009 and 2010. Animals were collected from the field by hand,
sweep net or vacuum sampler. Replicates of the different treatments
were run as individuals of different species became available, and the
number of replicates varied among species combinations due to the
availability of animals (n = 27 for Orchelimum adults on Prokelisia
and n = 3–15 for all other trials; refer to Fig. 7 for details). Upon collecting, animals were acclimated for 24 h to laboratory conditions
and to standardize levels of hunger for field caught animals. Individual trials were run for up to 24 h in 850-mL glass jars at a constant
room temperature of 25 °C and photoperiod (14 : 8 day : night).
Each jar was stocked with a 15 cm long Spartina leaf that served as
a substrate for the animals. In each case, consumers were allowed to
feed ad libitum and were used only once. Since the containers we
used were of small volume, we assume that the predator–prey
encounter rates were so high that predation rates were not limited by
the number of prey offered, but only by the ability and motivation of
predators to subdue and consume prey. This motivation, however,
may have been occasionally modified by nonpredatory mortality of
prey that occurred after 8 h of the trial (all trials with the soft-bodied
mirid Trigonotylus and some with Prokelisia). Some trials were
stopped at 8 h if predators were depleting prey or if prey appeared
stressed in the jars. Consumption rates for longer assays were prorated by duration and all data reported as number consumed in 8 h.
Results from 2009 and 2010 were broadly consistent across years and
across Prokelisia size categories, but distinct among different
predator–prey combinations; we therefore pooled data among years
and across different sizes of Prokelisia prey to increase sample sizes.
We conducted one-way ANOVAs for different predator–prey combinations within each of three prey groupings (Prokelisia, Orchelimum,
mixed trials) with predator–prey combination treated as a fixed factor.
Results
INITIAL PLANT QUALITY
At the start
greater total
more green
higher levels
of the experiment, fertilized plants had 8.8%
biomass (F1,56 = 45.19, P < 0.0001), 22.5%
leaves (F1,56 = 47.22, P < 0.0001) and 58%
of chlorophyll (F1,56 = 24.24, P < 0.0001) than
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1169–1182
Local vs. geographic variation in plant quality 1173
unfertilized plants. In contrast, there were no initial differences 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 Spartina
leaves at the end of the experiment by 50–100%
(F1,45.2 = 130.81, P < 0.0001) over unfertilized plants. The
resulting differences in N content (control 1%; fertilized
1.8%) are within the range of those observed between shortand tall-form Spartina alterniflora in South Atlantic salt
marshes (refer to data from Ornes & Kaplan 1989 summarized under Materials and methods in this report). Fertilized
plants had a lower percentage of damage to individual leaves
(Fig. 1a) than unfertilized plants; the proportion of green
leaves that were damaged followed the same patterns and statistical significance (Table 2). Fertilized plants also exhibited
greater overall plant biomass (Fig. 1b) than unfertilized
plants. Low-latitude plants had greater biomass (Fig. 1b and
Table 2) than high-latitude plants. At the end of the experiment, plants from high-latitude sources were 22.4% higher in
Proportion of leaf area damaged
by omnivore
(a)
1
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
P = 0.023
P < 0.0001
Low high
latitude
0 +
fertilized
P = 0.02
P < 0.0001
0 +
+
mesopredator omnivore
foliar nitrogen than those from the low-latitude sources. The
presence of katydids in mesocosms reduced final plant biomass (Fig. 1b and Table 2). We recorded the lowest plant
growth rates (negative RGR) in unfertilized plants from high
latitudes in mesocosms containing katydids; in contrast, the
growth of plants from low latitudes was enhanced by fertilizer
application, but not consistently affected by omnivore presence (Fig. 2 and Table 2). There were no important main
effects of spider presence on any plant variables (Table 2).
High-latitude plants lacking either consumer had depressed
nitrogen contents relative to plants with spiders (latitude 9 mesopredator 9 omnivore interaction, Table 2). This
effect was particularly striking for fertilized plants, but only
at
high
latitudes
(latitude 9 fertilized 9 mesopredator 9 omnivore, Table 2). We suspect that this effect was
due to herbivore feeding depressing plant nitrogen content
(Denno et al. 2000), especially on the relatively smaller highlatitude plants, but did not investigate this further.
HERBIVORE RESPONSES
After 2 weeks, Prokelisia populations were elevated on highlatitude plants (P = 0.003) and tended to be suppressed
(P = 0.097) by spiders (Fig. 3a). At this time, Prokelisia populations were suppressed in the presence of spiders only on
unfertilized plants; on fertilized plants, Prokelisia attained
similar populations regardless of spider predation pressure
(Fig. 3b). These basic patterns continued to the end of the
experiment (Table 3), but levels of statistical significance varied. At the end of the experiment, Prokelisia populations did
not differ between high- and low-latitude plants, were
enhanced several-fold by fertilizer and were reduced by omnivores but not by spiders (Fig. 4c). The impacts of both omnivores and spiders depended on whether or not plants were
fertilized: both consumers tended to suppress Prokelisia only
on unfertilized plants Fig. 4a,b), although this pattern was
only significant for omnivores. Over all treatment combinations, Prokelisia population density was positively related to
leaf nitrogen content (Fig. 5a).
Total plant biomass (g)
(b) 40
35
P = 0.012
30
25
20
15
10
5
0
Low high
latitude
0 +
fertilized
0 +
0 +
mesopredator omnivore
Fig 1. Mesocosm experiment. Main effects for models without significant interactions. (a) Mean area (as a proportion) of individual leaves
showing Orchelimum damage (F1,22.6 = 27.19, P < 0.0001). (b) Total
above-ground plant biomass (fertilized: F1,56 = 142.8, P < 0.0001;
latitude: F1,8 = 8.43, P = 0.02). All data are back-transformed
lsmeans and 95% confidence intervals.
PREDATOR AND OMNIVORE RESPONSES
Spider survival to the end of the experiment was unrelated to
any treatment variables (Table 3). The growth rate of katydids
was positive for fertilized plants but negative across all unfertilized plants (Table 3). Over all treatment combinations, the
growth rate of katydids was positively related to leaf nitrogen
content with a transition from negative to positive growth at
leaf nitrogen contents of around 1.5% (Fig. 5b). Neither
source latitude of plants nor the presence of spiders affected
katydid growth rates (Table 3).
SEM ANALYSIS
Overall, the SEM analysis supported our initial prediction and
general finding from ANOVA that fertilization (or local nutrient
status) was a strong mediating factor on top-down effects in
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1169–1182
Den d.f.
8
56
56
56
56
56
56
56
56
56
56
56
56
56
56
Source of variation
Latitude
Fertilizer
Mesopredator
Omnivore
Lat 9 fert
Lat 9 meso
Lat 9 om
Fert 9 meso
Fert 9 om
Meso 9 om
Lat 9 fert 9 meso
Lat 9 fert 9 om
Lat 9 meso 9 om
Fert 9 meso 9 om
Lat 9 fert 9 meso 9 om
8.43
142.83
0.08
6.77
0.49
1.23
0.06
0.61
0.01
2.17
1.15
1.12
1.25
1.98
0.43
F
Plant biomass
Den d.f.
9.0
45.2
45.2
45.5
45.2
45.2
45.5
48.3
48.2
46.3
48.3
48.2
46.3
45.5
45.5
P
0.02
< 0.0001
0.79
0.012
0.49
0.27
0.81
0.44
0.93
0.15
0.29
0.30
0.27
0.17
0.52
6.81
130.32
4.84
1.57
0.01
1.82
5.24
7.09
0.01
3.71
1.10
2.42
9.45
1.92
6.77
F
Percent foliar N
0.028
< 0.0001
0.03
0.22
0.98
0.18
0.027
0.011
0.91
0.06
0.30
0.13
0.0035
0.17
0.013
P
8
56
56
56
56
56
56
56
56
56
56
56
56
56
56
Den d.f.
23.28
16.97
4.36
1.80
1.38
7.34
0.54
<0.01
3.15
4.73
1.51
6.74
2.48
1.64
0.19
F
RGR green leaves
0.0013
< 0.0001
0.041
0.19
0.25
0.0089
0.47
0.95
0.08
0.034
0.22
0.012
0.12
0.21
0.67
P
7.4
53.6
53.6
53.6
53.6
53.6
53.6
53.6
53.6
53.6
53.6
53.6
53.6
53.6
53.6
Den d.f.
1.25
15.76
0.23
0.26
2.04
1.25
0.20
0.88
3.25
1.33
0.02
0.18
<0.01
0.05
1.15
F
0.30
0.0002
0.63
0.61
0.16
0.27
0.65
0.35
0.08
0.25
0.90
0.68
0.97
0.83
0.29
P
Green leaves (proportion)
2.24
33.88
1.35
2.75
0.14
0.18
0.05
22.9
22.9
22.9
22.9
F
7.7
22.9
22.9
Den d.f.
0.84
0.68
0.11
0.71
0.18
< 0.0001
0.26
P
Damaged leaves (proportion)
22.6
22.6
22.6
22.6
7.2
22.6
22.6
Den d.f.
0.11
0.90
0.98
0.09
8.22
27.19
1.92
F
0.74
0.35
0.33
0.77
0.023
< 0.0001
0.18
P
Percent damage to leaves
Table 2. Mesocosm experiment. Results from nested mixed-model ANOVAS for the following variables: plant biomass, percent foliar nitrogen, relative growth rate (RGR) of green leaves, the proportion of leaves that were green, the proportion of leaves that were damaged and the percentage of damage to individual leaves. Since measures of plant damage were scored as the proportion or percent of omnivore damage, estimations could only be made for mesocosm combinations which included omnivores – absent estimations are indicated by blank cells. We used
log (v + 1) and square root transformations where necessary 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 of freedom for all effects = 1). All models included a random
site effect (nested within latitude). Effects that are statistically significant at <0.05 are highlighted in bold – no post hoc corrections for multiple tests have been employed
1174 L. B. Marczak et al.
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1169–1182
Local vs. geographic variation in plant quality 1175
0.05
0.04
a
RGR green leaves
0.03
0.02
ab
ab
ab
ab
0.01
abc
bc
0
–0.01
–0.02
–0.03
c
–0.04
Fig 2. Mesocosm experiment. Interactive
effects of latitude, omnivore and fertilizer for
relative growth rate (RGR) of green leaves
(lat 9 fert 9 om, F1,56 = 6.74, P = 0.012).
–O
–O
+O
+O
–F
–O
+O
Low latitude
(b) After 2 weeks
After 2 weeks
50
P = 0.003
Fertilized x Mesopredator
P = 0.027
P = 0.097
a
40
45
40
a
35
35
30
30
25
25
a
20
20
15
15
10
10
b
5
0
Low
High
+O
+F
High latitude
50
45
–O
–F
+F
–M
+M
5
0
–M
+M
–F
–M
Abundance of Prokelisia (individuals/plant)
Abundance of Prokelisia (individuals/plant)
(a)
–0.05
+M
+F
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 represent
high latitude and mesopredator presence, respectively. (b) Significant interaction of fertilizer and mesopredator presence (fertilized 9 mesopredator, F1,53.2 = 5.2, P = 0.027). Data are back-transformed lsmeans and 95% confidence intervals.
the Spartina mesocosms. As we initially predicted, SEM analysis showed that the effect of fertilization on Prokelisia was
in large part mediated through an increase in plant biomass
(Fig. 6a,b); larger plants simply represented greater food
availability for herbivores. We do not believe that this rules
out a direct effect for nitrogen content as shown in Fig. 5,
because the SEM considered high- and low-latitude plants
separately and so had less power and a reduced range of N
content within each analysis, but it emphasizes that plant
nutrition affects both size and N content and that both can
affect herbivore populations. We also predicted that fertilized
plants would experience lower levels of damage essentially
via a dilution effect attributable to an overall increase in plant
biomass. In our experiment, fertilized plants did experience
less omnivore damage – a result confirmed by both ANOVA
(Fig 1b) and SEM analyses. The SEM also supports the
hypothesis that this was due to omnivore effects being diluted
among the greatly increased biomass of plants, particularly at
low latitudes (Fig. 6b). At the same time, an increase in Prokelisia densities reduced omnivore leaf damage in both highand low-latitude plants, probably by providing an alternative
food for Orchelimum.
PREDATION TRIALS
All five predators tested (three spiders, a beetle and Orchelimum adults) ate Prokelisia, but the spider Hogna ate 3–4
times more Prokelisia than the other predator species (Tukey–
Kramer HSD P < 0.05, Fig. 7a). Both Hogna and Pardosa
spiders ate fifth-instar Orchelimum, but did so at very low
rates, and Marpissa and a salticid spider ate no Orchelimum
(Fig. 7b). Adult Orchelimum did not feed on fifth-instar conspecifics (Fig. 7b). Other arthropod herbivores (Ischnodemus,
Trigonotylus) common in the Spartina community were consumed at moderate rates in predation trials by at least one
potential consumer, and Marpissa spiders were vulnerable to
intraguild predation from the larger Hogna spiders (Fig. 7c).
Discussion
It is now generally agreed that top-down and bottom-up forces
interact to affect populations of herbivores (Gruner 2004;
Stiling & Moon 2005; Bertness et al. 2007; Sala, Bertness &
Silliman 2008). In our mesocosm experiment, bottom-up
sources of variation in plant quality determined food web
structure. This effect, however, was strong at the local scale
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1169–1182
1176 L. B. Marczak et al.
Table 3. Mesocosm experiment. Results from nested mixed-model ANOVAS for the following variables: total abundance of Prokelisia
nymphs, Prokelisia adults, all Prokelisia combined, the relative growth rate (RGR) of grasshoppers and proportion of spiders surviving. Estimations of grasshopper RGR and spider survival could only be made for mesocosm combinations which contained
these animals – absent estimations are indicated by blanks cells. We used log (v + 1) and square root transformations where necessary 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 of
freedom for all effects = 1). All models included a random site effect (nested within latitude). Effects that are statistically significant at <0.05 are highlighted in bold – no post hoc correction for multiple tests has been employed
Prokelisia nymphs
Prokelisia adults
All Prokelisia (log)
RGR grasshoppers
Spider survival
Source of
variation
Den
d.f.
F
P
Den
d.f.
F
P
Den
d.f.
F
P
Den
d.f.
F
P
Den
d.f.
F
P
Latitude
Fertilizer
Mesopredator
Omnivore
Lat 9 fert
Lat 9 meso
Lat 9 om
Fert 9 meso
Fert 9 om
Meso 9 om
Lat 9 fert
9 meso
Lat 9 fert
9 om
Lat 9 meso
9 om
Fert 9 meso
9 om
Lat 9 fert
9 meso 9 om
8
56
56
56
56
56
56
56
56
56
56
0.37
18.26
0.00
5.66
2.11
5.34
2.45
3.09
4.01
0.34
2.29
0.56
< 0.0001
0.96
0.0208
0.15
0.025
0.12
0.084
0.050
0.56
0.14
8
56
56
56
56
56
56
56
56
56
56
2.34
25.14
0.25
3.40
0.34
1.06
1.45
3.43
4.69
0.73
0.57
0.16
< 0.0001
0.62
0.071
0.56
0.31
0.23
0.069
0.035
0.40
0.45
8
56
56
56
56
56
56
56
56
56
56
1.73
25.69
0.45
5.47
1.75
2.07
1.19
3.49
5.43
1.05
1.17
0.22
< 0.0001
0.504
0.023
0.19
0.16
0.28
0.067
0.024
0.31
0.28
2.6
17.1
20.3
0.19
18.33
0.71
0.70
0.0005
0.409
7.7
41.7
0.12
2.20
0.73
0.15
17.1
20.3
0.01
0.01
41.2
41.7
0.00
1.15
0.99
0.29
41.2
0.00
0.97
16.4
1.00
41.7
0.25
56
0.03
0.86
56
2.13
0.15
56
1.12
0.30
56
0.03
0.86
56
0.24
0.63
56
0.32
0.57
56
0.11
0.74
56
0.08
0.78
56
0.11
0.74
56
0.05
0.82
56
1.44
0.24
56
0.55
0.46
but weak at the latitudinal scale. Top-down effects on consumers were driven by the omnivorous katydid in our study rather
than the strictly carnivorous spider. In those cases where predators 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 set
the stage on which herbivorous insects and their enemies
interact’ (Denno, McClure & Ott 1995; Denno et al. 2002).
LOCAL, NOT GEOGRAPHIC, SOURCES OF BOTTOM-UP
CONTROL
Our mesocosm experiment indicated that the Spartina food
web is strongly structured by local variation in plant quality – a
result supported by recent field experiment that noted increases
in multiple functional groups in response to in-situ fertilization
in both high- and low-latitude Spartina marshes (McCall &
Pennings 2012). In our more-controlled greenhouse experiment, fertilized plants (mimicking variation in plant quality and
form across the local elevation gradient) were consistently larger and supported more herbivores, but showed less damage
(due to dilution of herbivore damage and increased numbers of
alternate prey for omnivores) than unfertilized plants. This
result is consistent with a number of studies that have documented that herbivores prefer and perform better on higherquality plants from the creekbank vs. the mid-marsh and that
0.98
0.94
.
0.33
0.62
16.4
0.63
0.44
41.7
1.81
0.19
this result also tracks the variation in plant quality and height
noted 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 highlatitude plants, this effect was no longer apparent by the end
of the experiment. Because latitudinal variation in plant quality is maintained for an extended period of time when plants
are grown in a common garden (Salgado & Pennings 2005),
we do not believe that the latitudinal plant quality signal was
artificially weak in our experiment. While the effects of
latitude were not as dramatic as that of fertilizer addition,
low-latitude plants were consistently larger, but lower in
nitrogen, at the end of the experiment. Although high-latitude
plants are higher in nitrogen, lower in phenolics and more
palatable than low-latitude plants (Pennings, Siska & Bertness
2001; Siska et al. 2002; Salgado & Pennings 2005), and
although these differences are sufficient to cause geographic
variation in herbivore body size (Ho, Pennings & Carefoot
2010), they were nevertheless overwhelmed in our experiments by fertilizer-induced nutritional status and food web
composition. These findings are similar to those in our
previous work with the high-marsh shrub Iva frutescens
(Marczak et al. 2011), where we found that latitudinal variation in plant quality had much smaller effects on herbivore
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1169–1182
Abundance of Prokelisia (individuals/plant)
Local vs. geographic variation in plant quality 1177
400
(a)
(b)
Fertilized x mesopredator
P = 0.067
350
Fertilized x omnivore
P = 0.024
a
300
a
250
200
150
a
100
50
b
0
–M
+M
–M
–F
+M
–O
+F
+O
–O
–F
+O
+F
Fig 4. Mesocosm experiment. Abundance of
Prokelisia in mesocosms at the end of the
experiment. (a) Interaction of fertilizer and
mesopredator presence. (b) Interaction of
fertilizer and omnivore presence. (c) Main
effects. Data are back-transformed lsmeans
and 95% confidence intervals.
Abundance of Prokelisia (individuals/plant)
(c)
300
P = 0.023
P < 0.0001
250
200
150
100
50
0
Low
populations than latitudinal variation in top consumers and
competition.
We anticipated interactions between top-down effects and
the nutrient status of Spartina in our mesocosms, and we subsequently observed that local (fertilized) differences in the
nutritional status of Spartina modified the effects of both katydids and spiders on herbivore populations. Predators were
able to suppress herbivores only on unfertilized plants, possibly because herbivores were concentrated on these smaller
plants and had lower reproductive rates. At the same time,
damage from omnivore populations was greatest on plants
that did not receive fertilizer, again probably because omnivores were concentrated on smaller, unfertilized plants and
had fewer insect prey as an alternative to feeding on plants.
Control of consumers by local variation in plant quality is
consistent with some previous work on the Spartina food
web. For example, Denno et al. (2002) found that enhancing
the nutrition of host plants did not strengthen top-down
effects on Prokelisia despite field-based evidence that predator densities were also elevated on higher-quality plants.
Instead, predators more effectively suppressed Prokelisia populations on poor-quality host plants (Denno et al. 2002). In
contrast, when Prokelisia are feeding on high-quality plants
(in the case of the present experiment, fertilized plants), they
escape from effective predator control. Denno (2002) has previously argued that this result is the key to understanding the
seasonal migration of Prokelisia populations from the high to
the low marsh in high-latitude locations where high-quality
High
–F
+F
–M
+M
–O
+O
plants are only available seasonally in the low marsh due to
severe winter freezes.
Similarly, Bertness et al. (2007) demonstrated that mixed
insect communities had little effect on Spartina productivity
in relatively low-nutrient marshes in Rhode Island (US), while
increasing levels of eutrophication triggered outbreaks or
aggregations that led to herbivore control of marsh productivity in eutrophic marshes. Nitrogen-rich Spartina are characteristic of low-marsh habitats (Denno 1983; Ornes & Kaplan
1989) 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 high
nitrogen content of low elevation Spartina plants encourages
mass colonization, enhances both survival and fecundity, and
promotes rapid population expansion of Prokelisia planthoppers (Olmstead et al. 1997), and that nitrogen enhancement
results in a greater abundance of herbivores, predators and
parasitoids across a large range of latitude (McCall &
Pennings 2012). Our mesocosm experiment also demonstrated
these outbreak conditions on fertilized plants. In contrast, latitudinal variation in plant quality did not affect Prokelisia populations, omnivore growth rates or the effect of predators on
herbivore populations.
WEAKER TOP-DOWN EFFECTS
Since the early studies by Teal (1962), salt marsh ecosystems
have been considered systems under strong bottom-up control,
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1169–1182
Density of Prokelisia (number/g plant biomass)
1178 L. B. Marczak et al.
1200
(a)
(a)
1000
800
600
400
200
0
0
0.5
1
1.5
2
Percent foliar nitrogen
2.5
3
(b)
Relative growth rate of katydids
0.01
(b)
0.005
0
–0.005
–0.01
–0.015
–0.02
–0.025
0
0.5
1
1.5
Percent foliar nitrogen
2
2.5
Fig 5. Mesocosm experiment. (a) Relationship between percent foliar
N and Prokelisia density (R2 = 0.16, P < 0.0001,). (b) Relationship
between percent foliar N and RGR of Orchelimum (R2 = 0.27,
P = 0.022).
with primary productivity patterns being largely driven by
physical conditions and nutrient availability. More recent
work has championed top-down regulation of productivity in
salt marshes by herbivores (snails: Silliman & Bertness 2002;
insects: Finke & Denno 2004; geese: Kuijper & Bakker 2005;
crabs: Altieri et al. 2012). Control of herbivore populations
meanwhile appears to be regulated by a combination of bottom-up and top-down factors. In our mesocosm experiment,
while both katydids and spiders successfully suppressed Prokelisia populations, these consumer effects were consistently
modified by bottom-up conditions and consumer effects did
not cascade to benefit plants.
The effects of plant architecture on predator capture efficiencies have been noted in salt marsh and other systems
(Landis, Wratten & Gurr 2000). It is possible that in our
experiment, predator suppression of herbivores on low-nitrogen plants was due to the differences in physical structure
and size of fertilized and control plants that altered the foraging efficiency of invertebrate predators. In particular, predator
foraging success is likely to have been higher on smaller,
unfertilized plants. Alternately, suppression of Prokelisia populations on unfertilized plants by katydids and spiders
Fig 6. Mesocosm experiment. SEM model of the experimental Spartina food web imitating (a) high latitudes and (b) low latitudes. The
model is consistent with the data (P = 0.70, chi-square d.f. = 0.78).
Path coefficients describe standardized values showing relative effects
of variables upon each other. Arrow width is proportional to the
strength of the path coefficient; one headed arrows represent causal relationships; nonsignificant relationships are marked with a dotted line.
(Fig. 4a,b) might have occurred because Prokelisia populations were reproducing poorly and individuals were less able
to escape predators due to feeding on a nutritionally poor
food source.
WEAK OR ABSENT TROPHIC CASCADES
In our mesocosm study, Orchelimum reduced Prokelisia
abundance; however, this did not cascade to indirectly benefit
plants, probably because Orchelimum also negatively affected
plants by directly consuming them. Control of herbivore
abundance by spiders was generally weak (statistically discernible at the experiment mid-point but not evident at its
conclusion), and this effect was not strong enough to cascade
to positively affect plant growth or other characteristics.
While Orchelimum are capable of consuming substantial
quantities of Prokelisia planthoppers (Fig. 7), they appear to
have relatively inflexible diets that require them to also consume plant material (Jimenez et al. 2012), and they may
continue to eat high-quality plant tissue even when invertebrate prey are also available. Several studies have suggested
(Denno & Fagan 2003; Matsumura et al. 2004) that even a
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1169–1182
Local vs. geographic variation in plant quality 1179
(a) 10
# Prokelisia consumed/8 h
9
Prey = Prokelisia
4
8
7
6
5
4
3
3
2
7
4
Pardosa
Marpissa
27
1
0
Hogna
coccinellid
(b)
# Orchelimum consumed/8 h
0.14
Prey = fifth-instar Orchelimum
0.12
0.1
15
0.08
11
0.06
0.04
0.02
0
(c)
4
4
Hogna
Pardosa
Marpissa
2
# Prey consumed/8 h
Orchelimum
adults
Prey = mixed trials
1.6
6
1.4
5
1.2
1
11
Salticid sp
1.8
Fig 7. Predation trials. Predator success over
8 h with (a) Prokelisia or (b) fifth-instar
Orchelimum as the prey item and (c) in
addition predator–prey pairings using other
intermediate-sized arthropods common in the
Spartina community as prey items. Numerals
indicate sample size in each trial.
Orchelimum
adults
10
0.8
0.6
0.4
0.2
9
0
Prey = Ischnodemus badius
Hogna
Marpissa
small addition of protein in the diet of omnivores can result
in large improvements in nutrition and growth. Jimenez et al.
(2012) found that Orchelimum grew better on a mixed diet
including both prey and plant material than on either single
diet alone. We found that Orchelimum exhibited greater relative growth rates on plants with greater foliar nitrogen
(Fig. 5b). This could have been because Orchelimum performed better when eating plants with higher nitrogen content, or because Orchelimum were able to eat more prey on
fertilized plants because Prokelisia were more abundant. In
either case, both results are consistent with the idea that
Orchelimum is severely limited by N availability on a diet of
low-N Spartina. At the same time, Orchelimum grew better
on a mixed diet than on a diet of pure animal prey (Jimenez
et al. 2012), indicating that while plants and herbivores may
be somewhat substitutable foods (Van-Rijn & Sabelis 2005)
for other marsh omnivores (Armases crabs, Ho & Pennings
Prey = Marpissa sp.
Hogna
Prey = Trigonotylus sp.
Orchelimum adults
2008), they are complementary for Orchelimum. Whether
omnivory acts to strengthen or weaken trophic cascades (Polis
& Strong 1996; Eubanks & Styrsky 2005) may thus depend
on how readily an omnivore can switch food sources. This
may be particularly true in the case of true omnivores (those
that consume both plant and animal tissue) where a preference for plant over animal tissue will serve to cancel cascading effects of consuming herbivorous prey.
EXTRAPOLATING TO THE MORE DIVERSE COMMUNITY
IN THE FIELD
Our mesocosm experiments necessarily utilized a limited
number of species. Although these were selected because they
were among the more common taxa in the field, this still
raises the question of whether the results can safely be extrapolated to the more diverse field community. The predation
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1169–1182
1180 L. B. Marczak et al.
trials suggest that they can, albeit with an important caveat.
First, all the moderately sized arthropod herbivores that we
tested (Prokelisia, Ischnodemus and Trigonotylus) were readily eaten by common predators. Second, with the exception of
a salticid spider that we did not identify to species, all the
predators that we tested (three other spiders, a beetle and
Orchelimum) readily consumed at least one of the herbivore
species tested. Thus, although the precise predation rates in
any particular setting would depend on the densities of the
different taxa and the differences in vulnerability of particular
herbivores to particular predators, the predator–prey interactions in this community appear to be relatively generalized.
As a result, the various less-common herbivore species are
likely to be affected by predators and top omnivores in much
the same way that Prokelisia was affected.
The major caveat with extending our results to the more
diverse field community is that the multiplicity of predatory
taxa in the field (e.g. at least six common spiders and another
six or more rare species, Wimp et al. 2010; authors personal
observations) greatly increases the potential for intraguild predation between predators. Depending on variation in predator
density, and on the extent to which various predators interfere
with vs. facilitate each other, our mesocosm results may imprecisely estimate predation rates in the field (Schmitz, Beckerman
& O’Brien 1997; Finke & Denno 2004). No doubt the details
of the trophic ecology of each of the predators differs somewhat. Nevertheless, because almost all the consumers tested
(with the exception of one spider) readily ate the common
arthropod herbivores, it is most likely that the relatively diverse
predator assemblage found in the field has a negative effect on
Prokelisia populations that is broadly consistent with the mesocosm results based on the single common predator Pardosa. In
sum, although there is much to be learned about how herbivore
and predator diversity affects the functioning of the Spartina
arthropod community, we are confident that our mesocosm
experiments, despite being stocked with only a few species,
provide a robust first-order approximation of how the more
diverse field community functions.
Fully understanding geographic variation in the Spartina
food web will need to consider the full suite of herbivores
including snails (Silliman & Zieman 2001), crabs (Altieri
et al. 2012) and vertebrates (Buchsbaum, Valiela & Swain
1984). A complete consideration of these herbivores, and their
interactions with insect herbivores, awaits further study; however, we speculate that the principles that we have outlined
here for insect herbivores also apply to these other herbivores.
For example, herbivorous Sesarma crabs are most abundant
near high-quality, tall-form Spartina plants (Teal 1958), and
per capita snail effects on Spartina are greatest on tall-form
plants (Silliman & Bertness 2002). Snails experience the
strongest top-down control from predators on high-quality
creekside instead of low-quality platform plants, but this is
simply because their predators are of marine rather than terrestrial origin (Silliman & Bertness 2002). Snail herbivory is
most important at low latitudes due to a turnover in the most
common 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 and
geographic variation in herbivore abundance may be the same
factors that affect insect herbivores: local variation in plant
quality and geographic variation in species composition. This
suggests that we are close to a conceptual unification of the
factors mediating the distribution and abundance of salt marsh
herbivores at both local and geographic scales.
COMPARING LOCAL AND GEOGRAPHIC PATTERNS
Taken as a whole, our results suggest that the single most
important factor mediating Prokelisia densities is local variation in plant quality between short- and tall-form plants. Predation pressure can be important, but only on low-quality
plants, because herbivores escape from predator control on
high-quality plants. Similarly, although plants demonstrably
vary in quality across latitude, and this has measurable effects
on herbivore performance (Ho, Pennings & Carefoot 2010),
the effects of latitudinal variation on herbivore abundance
tend 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 colder
winters at high latitudes are the most likely reasons why high
latitudes are characterized by a reduced number of generations
in multivoltine species such as Prokelisia (Friedenberg et al.
2008), a reduced body size of some univoltine species such as
Orchelimum (Wason & Pennings 2008; Ho, Pennings & Carefoot 2010) and a reduced density of some other members of the
food web (Pennings et al. 2009; McCall & Pennings 2012).
In sum, we argue that a first-order understanding of variation in the Spartina arthropod food web at geographic scales
consists of two variables: geographic variation in climate,
which mediates the density and body size of different members of the food web in ways that are not yet well studied;
and local variation in plant quality, which provides strong
bottom-up forcing to herbivore populations. A second-order
understanding of the arthropod food web needs to also consider predation, which is most effective at controlling herbivores feeding on low-quality plants (Denno, Lewis & Gratton
2005). Finally, latitudinal variation in plant quality probably
explains 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 constructive
commentary. This work is a contribution of the Georgia Coastal Ecosystem
Long-Term Ecological Research programme and contribution number 1030
from the University of Georgia Marine Institute.
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Received 25 January 2013; accepted 13 June 2013
Handling Editor: Martin Heil
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1169–1182