latitudinal variation in herbivore pressure in atlantic

Ecology, 90(1), 2009, pp. 183–195� 2009 by the Ecological Society of America

Latitudinal variation in herbivore pressurein Atlantic Coast salt marshes

STEVEN C. PENNINGS,1 CHUAN-KAI HO, CRISTIANO S. SALGADO,2 KAZIMIERZ WIESKI, NILAM DAVE,3 AMY E. KUNZA,4

AND ELIZABETH L. WASON5

Department of Biology and Biochemistry, University of Houston, Texas 77204 USA

Abstract. Despite long-standing interest in latitudinal variation in ecological patterns andprocesses, there is to date weak and conflicting evidence that herbivore pressure varies withlatitude. We used three approaches to examine latitudinal variation in herbivore pressure inAtlantic Coast salt marshes, focusing on five abundant plant taxa: the grass Spartinaalterniflora, the congeneric rushes Juncus gerardii and J. roemerianus, the forb Solidagosempervirens, and the shrubs Iva frutescens and Baccharis halimifolia. Herbivore countsindicated that chewing and gall-making herbivores were typically �10 times more abundant atlow-latitude sites than at high-latitude sites, but sucking herbivores did not show a clearpattern. For two herbivore taxa (snails and tettigoniid grasshoppers), correctly interpretinglatitudinal patterns required an understanding of the feeding ecology of the species, becausethe species common at high latitudes did not feed heavily on plant leaves whereas the relatedspecies common at low latitudes did. Damage to plants from chewing herbivores was 2–10times greater at low-latitude sites than at high-latitude sites. Damage to transplanted‘‘phytometer’’ plants was 100 times greater for plants transplanted to low- than to high-latitude sites, and two to three times greater for plants originating from high- vs. low-latitudesites. Taken together, these results provide compelling evidence that pressure from chewingand gall-making herbivores is greater at low vs. high latitudes in Atlantic Coast salt marshes.Sucking herbivores do not show this pattern and deserve greater study. Selective pressure dueto greater herbivore damage at low latitudes is likely to partially explain documented patternsof low plant palatability to chewing herbivores and greater plant defenses at low latitudes, butother factors may also play a role in mediating these geographic patterns.

Key words: biogeography; common-garden experiment; herbivore pressure; latitudinal variation; plant–herbivore interactions; salt marsh; top-down effects.

INTRODUCTION

Interactions among species are not the same every-

where. Many species are widely distributed, but inter-

actions among species occur at local sites (Menge 2003).

At each individual site, interactions between organisms

are mediated by local abiotic conditions and the

composition of the local community, creating selective

pressures that differ from those experienced by conspe-

cifics at other sites (Dunson and Travis 1991, Sotka and

Hay 2002, Toju and Sota 2006). As a result of site-to-site

differences in both ecological context and local adapta-

tion, the nature of interactions between species is likely

to vary geographically (Thompson 1988, Travis 1996,

Callaway et al. 2002, Sotka et al. 2003). If so,

understanding the nature of this geographic variation

will be essential to developing a general theory of species

interactions (Thompson 1994, 2005).

One way that interactions among species might vary

geographically is across latitude. It is well-established

that both primary productivity and species richness vary

across latitude (Hawkins et al. 2003, Hillebrand 2004,

Novotny et al. 2006), and it is reasonable to expect that

variation in these factors would create variation in

ecological interactions. In particular, ecologists have

long been interested in the idea that competition,

predation, and herbivory might all increase in intensity

from high to low latitudes (Dobzhansky 1950, Mac-

Arthur 1972, Pennings and Silliman 2005). A variety of

evidence supports these hypotheses (Vermeij 1978, Coley

and Aide 1991, Stachowicz and Hay 2000), but rigorous

studies are difficult, especially for plant–herbivore

interactions, because taxonomic turnover and large

geographic distances create obstacles to rigorous exper-

imental designs (Pennings et al. 2001). In the case of

plant–herbivore interactions, a number of studies

Manuscript received 1 February 2008; revised 29 April 2008;accepted 14 May 2008. Corresponding Editor: J. F. Bruno.

1 E-mail: [email protected] Present address: StatoilHydro, Department of Health,

Safety and Environment, Praia de Botafogo, 300—Eighthfloor, Rio de Janeiro 22250-040 Brazil.

3 Present address: 300 NC 54 Apartment C5, Carrboro,North Carolina 27510 USA.

4 Present address: Tolunay-Wong Engineers, Inc., 10710 S.Sam Houston Parkway West, Houston, Texas 77031 USA.

5 Present address: 1300 Kraus Natural Science Building,University of Michigan, 830 North University, Ann Arbor,Michigan 48109-1048 USA.

183

support the hypothesis that these interactions are more

intense at lower latitudes (Coley and Aide 1991, Bolser

and Hay 1996), but exceptions also exist (Bryant et al.

1994, Andrew and Hughes 2005), and many early studies

suffered from limitations in design (reviewed in Pennings

et al. 2001).

One of the most comprehensive studies of latitudinal

variation in plant–herbivore interactions comes from

salt marshes along the Atlantic Coast of the United

States, where similar plant communities extend from

central Florida through Maine. For 10 species of plants

(the majority of the community), individuals from low

latitudes were less palatable to 13 species of herbivores

than were conspecifics from high latitudes (Pennings et

al. 2001). Differences in palatability were constitutive in

three plant species studied in detail (Salgado and

Pennings 2005), and were linked to differences in plant

nitrogen content, toughness, and chemical defenses in

eight of nine species studied (Siska et al. 2002).

Herbivore pressure has been compared across latitude

for one plant species, and was greater at low than at high

latitudes (Pennings and Silliman 2005). If this result was

general, it would imply that herbivore pressure may

have contributed to the different selective environments

that produced plants with different traits at low vs. high

latitudes. Less extensive studies with six plant taxa in

European salt marshes documented similar patterns:

plants located at low-latitude sites often experienced

greater herbivore pressure and, perhaps as a result, were

less palatable than high-latitude conspecifics or conge-

ners (Pennings et al. 2007).

As found in these salt marsh studies, it is common to

find geographic variation in plant traits (Reich and

Oleksyn 2004), and in particular in traits such as plant

chemistry that may affect palatability to herbivores

(Levin 1976, Levin and York 1978, Coley and Aide

1991). An open question, however, is: what are the

selective forces that drive this variation in plant traits?

One possibility is that plant traits are responding to

latitudinal variation in aspects of the abiotic environ-

ment, such as temperature, humidity, nutrient availabil-

ity, and growing-season length (Reich and Oleksyn

2004, Wright et al. 2004). In this case, latitudinal

variation in plant traits might affect herbivores but not

be caused by herbivores. Here, we consider the alternate

possibility (i.e., that latitudinal variation in plant traits is

driven by latitudinal variation in herbivore pressure).

Early workers considered herbivory to be relatively

unimportant in salt marshes (Teal 1962), but more

recent studies have shown that salt marsh herbivores

have the potential to exert strong top-down control on

plant productivity and composition (Kerbes et al. 1990,

Bortolus and Iribarne 1999, Silliman and Zieman 2001,

Rand 2003, Silliman and Bortolus 2003).

There are a number of ways that one could test the

hypothesis that herbivore pressure is greater at low vs.

high latitudes. One obvious approach would be to

compare herbivore densities at multiple sites across

latitude, but doing this is quite labor intensive and, to

the best of our knowledge, has not been done except forpreliminary work by our group (Pennings and Silliman

2005). A somewhat easier approach would be to comparevisible damage to leaves across latitude (Coley and Aide

1991). This approach might be inaccurate if someherbivores completely consume leaves, if leaf longevitydiffers among sites, or if leaves from different regions

differ in palatability. All of these concerns are likely toapply, especially when plant taxa turn over across

latitude; nevertheless, studies that have used thisapproach generally (Coley and Aide 1991, Pennings

and Silliman 2005, Pennings et al. 2007), but not always(Andrew and Hughes 2005), report greater herbivory at

lower latitudes. A third approach would be to compareherbivory levels on ‘‘phytometers’’ (e.g., standard plants

placed at multiple sites; Hay 1984). This approachovercomes a number of the limitations involved in

measuring herbivory on local vegetation because plantspecies, palatability, and leaf age can be standardized,

but is more labor intensive and, to the best of ourknowledge, has not been done. Finally, a fourth

approach would be to conduct herbivore manipulationexperiments across latitude. This method is the mostlabor intensive of all, but has the advantage that it

directly measures herbivore impacts on plant biomass.For example, snail manipulations at low-latitude salt

marshes strongly affected biomass of the salt marsh grassSpartina alterniflora, but similar manipulations at high

latitudes had no effect (Pennings and Silliman 2005).In this paper, we employ a combination of the first

three methods to test the hypotheses that (1) herbivoresare more abundant, and (2) do more damage to plants in

low- vs. high-latitude salt marshes. Although thesemethods do not measure natural selection per se,

documenting a strong geographic gradient in herbivorywould lend support to the hypothesis that geographic

variation in herbivory selects for geographic variation inplant traits.

METHODS

Study sites and species

We worked at 39 study sites ranging from northern

Florida to southern Maine (Appendix A). Most of thesesites were associated with National Estuarine Research

Reserve or Long-Term Ecological Research programs.For the purposes of this paper we grouped sites into

high-latitude (Connecticut, Rhode Island, Maine, NewHampshire, Maine; N ¼ 15) and low-latitude (Florida,

Georgia, South Carolina, North Carolina; N ¼ 24)categories, with the central Atlantic region omitted.

High-latitude sites were at 41–448 N; low latitude siteswere at 31–368 N. This was done to facilitate comparison

with our previous work (Pennings et al. 2001, Siska et al.2002, Salgado and Pennings 2005) that has focused oncomparing high- and low-latitude regions, because the

transplant experiments used high- and low-latitude sitesas geographic replicates, and to minimize the logistical

STEVEN C. PENNINGS ET AL.184 Ecology, Vol. 90, No. 1

challenges of the work. Limited sampling at central

Atlantic sites, however, has found intermediate values

for almost all variables reported here (S. C. Pennings,

unpublished data).

We sampled five plant taxa (Duncan and Duncan

1987) that included the most widespread and abundant

plants in Atlantic Coast salt marshes (Table 1). These

were: (1) the grass Spartina alterniflora, which domi-

nates low marsh elevations; (2) the rushes Juncus

gerardii and J. roemerianus, which dominate middle

marsh elevations at high- and low-latitude sites,

respectively; (3) the forb Solidago sempervirens, which

occurs as scattered individuals in the high marsh and at

the terrestrial border of the marsh; and (4) the shrubs

Iva frutescens and Baccharis halimifolia, which dominate

the terrestrial border of the marsh. In every case except

the two Juncus congeners, we made intraspecific

comparisons across latitude. Not every plant taxa was

abundant enough to sample at every site; therefore,

replication varies among species. For each taxon, we

sampled the most important associated herbivore

species (Table 1). Our sampling focused on the chewing

feeding guild, which was dominated by beetles, grass-

hoppers, crabs, and snails, but we also sampled the most

common representatives from the sucking and gall-

making guilds. We did not sample stem borers,

herbivorous birds and mammals, or belowground

herbivores, because doing so would have required

destructive or logistically complicated methods beyond

the scope of this study. We did not sample leaf miners

because these were not generally abundant at our sites.

Latitudinal sampling

Spartina alterniflora dominates lower marsh eleva-

tions and occurs as taller plants along creek banks and

shorter plants on the marsh platform. We sampled the

shorter plants on the marsh platform on four dates

(June, July, August, September) in 2002 and three (June,

July, August) in 2003. Sampling locations (transects,

quadrats, and plants) were located haphazardly within

the S. alterniflora zone on the marsh platform, with the

goal of sampling a fairly large area of each site (i.e.,

subject to the physical constraints of the site, sampling

locations were spread out over a large area). A similar

process was used to place sampling locations in the other

vegetation types. Tettigoniid grasshoppers were visually

counted by walking 2 3 10 m transects while disturbing

vegetation with a PVC pipe. Collections indicated that

tettigoniids at high-latitude sites were mostly (97%)

Conocephalus species, which eat relatively little leaf

material, and at low-latitude sites were mostly (87%)

Orchelimum fidicinium, which readily eats leaves (Wason

and Pennings 2008). Although visual transects overlook

some grasshoppers, it is unlikely that there was

systematic bias between geographic regions because the

plant and grasshopper species studied were similar or

identical at all sites. This was also true for the other

vegetation types in which we conducted visual transects

for grasshoppers, with the exception of the two species

of Juncus. In the case of Juncus spp., the low-latitude

species was taller, which would have made it harder to

observe grasshoppers, leading to a conservative test of

the hypothesis that grasshoppers would be more

abundant at low latitudes. The snails Littoraria irrorata,

TABLE 1. Plant and herbivore species.

Zone Plant species Latitude Herbivore species sampled

Low marsh Spartina alterniflora(Poaceae), smoothcordgrass

high and low Orthoptera: Tettigoniidae. Concephalus spartinae,Orchelimum fidicinium

Gastropoda. Littoraria irrorata, Melampus bidentatusHomoptera: Dephacidae. Prokelisia marginata,

Prokelisia dolusMiddle marsh Juncus gerardi (Juncaceae),

black grasshigh Orthoptera: Acrididae. Paroxya clavuliger

Orthoptera: Tettigoniidae. Concephalusspartinae, Conocephalus spp., Orchelimum concinnum

J. roemerianus (Juncaceae),needle rush

low Gastropoda. Littoraria irrorata, Melampus bidentatusDecapoda: Grapsidae. Armases cinereum

High marsh andterrestrial border

Solidago sempervirens(Asteraceae), seasidegoldenrod

high and low Orthoptera: Acrididae. Paroxya clavuliger, Melanoplusbivittatus

Coleoptera: Chrysomelidae. Erynephala maritimaHemiptera: Aphididae. Uroleucon pieloui

Marsh terrestrialborder

Iva frutescens (Asteraceae),marsh elder

high and low Orthoptera: Acrididae. Paroxya clavuliger,Hesperotettix floridensis, Melanoplus spp.

Coleoptera: Chrysomelidae. Ophraellanotulata, Paria aterrima

Decapoda: Grapsidae. Armases cinereumHemiptera: Aphididae. Uroleucon ambrosiaeDiptera: Cecidomyiidae. Asphondylia sp.Chelicerata: Acarina. Eriophyid mites

Marsh terrestrialborder

Baccharis halimifolia(Asteraceae), silverling orgroundsel tree.

high and low Coleoptera: Chrysomelidae. Trirhabda baccharidisOrthoptera: Acrididae. Various spp.

Notes: Plant taxonomy is based on Duncan and Duncan (1987). Plants are listed in order of elevation from low to high marsh.Photographs of selected species are available in Appendix B.

January 2009 185LATITUDE AND HERBIVORE PRESSURE

which at high densities can damage S. alterniflora leaves

by producing linear patterns of damage termed ‘‘radu-

lations’’ (Silliman and Zieman 2001, Silliman and

Bertness 2002, Silliman et al. 2005), and Melampus

bidentatus, which does not damage S. alterniflora leaves

(Pennings and Silliman 2005), were sampled in 0.25 3

0.25 m quadrats. The planthoppers Prokelisia marginata

and P. dolus were counted on S. alterniflora stems, which

were measured so that planthopper density could be

standardized by plant height. The two Prokelisia species

that attack S. alterniflora cannot be readily distinguished

in the field (Denno et al. 1987) and so were pooled.

Chewing damage was estimated visually and radulations

were measured on two leaves per plant, and values were

averaged to give single estimates per plant. Leaves of S.

alterniflora and other plant species were selected

haphazardly subject to the constraint that they be fully

expanded but not senescing. We scored radulations

liberally as any linear damage parallel to the leaf axis;

this may have included some damage caused by physical

processes or by species other than Littoraria. Each count

or measurement was replicated six to eight times per site,

and averaged over replicates and then over dates to yield

a single value for each measurement per site (i.e., sites

were the unit of replication in all analyses). For this and

other plant species, data were compared among regions

using two-sample t tests or (for cases with highly

unequal variances or non-normal distributions) with

Wilcoxon rank sum tests. A small subset of the Spartina

data (July and August 2002 grasshopper counts and

chewing damage, and selected snail counts) was

combined with other data in a previous study (Pennings

and Silliman 2005).

Juncus gerardii and J. roemerianus dominate middle

marsh elevations at high- and low-latitude sites, respec-

tively. We sampled Juncus spp. on four dates (June, July,

August, September) in 2002 and two (June, July) in

2003. Acridid and tettigoniid grasshoppers were visually

counted by walking 2 3 10 m transects while disturbing

vegetation with a PVC pipe. We did not collect

extensively enough in the Juncus zones to rigorously

quantify the proportional abundance of different grass-

hopper species. The snails Littoraria irrorata and

Melampus bidentatus were sampled in 0.25 3 0.25 m

quadrats. The omnivorous crab Armases cinereum was

counted in 2 3 2 m quadrats. Chewing damage on two

leaves per transect was measured as the length of any

grazing scars on the narrow leaves, standardized as a

percentage of leaf length, and values averaged. Each

count or measurement was replicated 6–8 times per site,


a single value for each measurement per site.

Solidago sempervirens occurs as scattered individuals

throughout the high marsh and terrestrial border of the

marsh (see Plate 1). We sampled Solidago on four dates

(June, July, August, September) in 2002, two (June,

July) in 2003, and three (June, July, August) in 2004.

Acridid grasshoppers, beetles, and aphids were counted

by searching entire individual plants. The length and

width of two leaves was measured, and leaf area

estimated as an ellipse. Herbivore counts were stan-

dardized by leaf area of the plant (estimated as the

number of leaves times the average leaf area). Chewing

damage was estimated visually on two leaves per plant

and values averaged to give single estimates per plant.

Each count or measurement was replicated six to eight

times per site, and averaged over replicates and then

over dates to yield a single value for each measurement

per site. Because individual Solidago plants were fairly

small, herbivore counts were more variable than similar

counts on the other plant species.

Iva frutescens occurs at the terrestrial border of the

marsh. At high-latitude sites it forms a shrub zone; at

low-latitude sites it occurs as scattered individuals within

a shrub zone dominated by Borrichia frutescens. We

sampled Iva on four dates (June, July, August,

September) in 2002, two (June, July) in 2003, and two

(June, July) in 2005. We measured the height, width, and

depth of individual plants and searched them visually

for acridid grasshoppers, herbivorous beetles, and

aphids. Herbivore counts were standardized by plant

volume (estimated as an ellipsoid). We also searched

plants for terminal galls caused by Asphondylia sp. gall

midges (Rossi et al. 2006), standardizing gall counts by

plant surface area (estimated as the surface of an

ellipsoid). Acridid grasshoppers were also visually

counted by walking 2 3 10 m transects through the

shrub zone while disturbing vegetation with a PVC pipe.

At high-latitude sites, most of the shrubs in the transect

were Iva frutescens, but at low-latitude sites the transects

included a mixture of Iva frutescens and Borrichia

frutescens. The omnivorous crab Armases cinereum was

counted in 2 3 2 m quadrats beneath the shrubs.

Chewing damage and percent cover of leaf galls was

estimated visually on three leaves per plant and values

averaged to give single estimates per plant. Each count

or measurement was replicated six to eight times per site,


a single value for each measurement per site.

Baccharis halimifolia occurs as scattered individuals at

the terrestrial border of the marsh, at slightly higher

elevations than Iva. We sampled Baccharis on two dates

(June, July) in 2003. We measured the height, width, and

depth of individual plants and searched them visually

for Trirhabda beetles and acridid grasshoppers. Herbi-

vore counts were standardized by plant volume (esti-

mated as an ellipsoid). Chewing damage was estimated

visually on three leaves per plant and values averaged to

give single estimates per plant. Each count or measure-

ment was replicated six to eight times per site, and

averaged over replicates and then over dates to yield a

single value for each measurement per site.

Transplant experiments

The sampling described in the previous section might

be criticized on the grounds that we know that low-


latitude plants are less palatable than high-latitude

conspecifics (Pennings et al. 2001, Siska et al. 2002,

Salgado and Pennings 2005); therefore, the sampling

might underestimate geographic differences in potential

herbivore pressure. An alternative approach would be to

measure herbivore damage to ‘‘standard’’ plants. We did

this for three species, Spartina alterniflora, Solidago

sempervirens, and Iva frutescens, by reciprocally trans-

planting individual plants between high- and low-

latitude sites.

Spartina alterniflora plants were collected by digging

ramets from five high- and five low-latitude sites and

acclimating them in 4-L pots for about seven weeks.

Within a site, individual ramets were collected at least 1

m apart to make it likely that we collected different

genotypes (Richards et al. 2004). Solidago sempervirens

plants were collected by digging individuals from four

high- and four low-latitude sites and acclimating them in

4-L pots for 1–2 weeks. Because this species has very

limited clonal growth, collecting individuals .1 m apart

ensured that we collected different genotypes. Iva

frutescens were germinated from seed or collected as

seedlings from seven high- and seven low-latitude sites

and grown in the greenhouse in 4-L pots for 1 yr. Based

on previous work with Spartina and Distichlis, we

expected high- and low-latitude plants to maintain

distinct phenotypes in a common garden (Salgado and

Pennings 2005), and this was in fact what occurred (see

Results). The first time that we did this experiment

(Solidago), we potted plants in soil from the collection

location. We later decided that it would be better to

standardize the soil, and so for the other two plants

(Spartina, Iva) we switched to a 50:50 mixture of

commercial potting soil and sand that was identical for

plants from all sites. The nature of the soil used did not

appear to affect the results, which were similar for all

three plant species.

Potted plants were placed in the field in blocks (one

plant from each origin site) within their normal eleva-

tional range at five (Spartina), four (Solidago), or six

(Iva) sites within each geographic region (the particular

sites used are indicated in Appendix A). Pots were sunk

into the marsh surface so that the soil within the pot was

level with that outside. Holes in the bottom of the pot

allowed water exchange with adjacent soils. Two fully

expanded but not senescent leaves with little or no initial

damage on each plant were tagged and all herbivore

damage scored when plants were outplanted and again

when they were retrieved, ;30 days later. Leaves that

were missing when plants were retrieved were dropped

from the analysis. Because the number of days that the

plants were exposed varied slightly, from 27 to 28

(Spartina), from 30 to 33 (Solidago), and from 28 to 31

(Iva), we standardized all accumulated damage to a 30-d

exposure period. Transplant experiments were conduct-

ed during seasons with high herbivore abundance for

each plant species: late July to late August of 2003 for

Spartina (N¼ 158), mid-July to mid-August of 2002 for

Solidago (N ¼ 152), and mid-June to mid-July of 2005

for Iva (N¼ 166).

For statistical purposes, origin 3 destination site

combinations were treated as the unit of replication. We

first averaged the new damage over both leaves on

individual plants, and then averaged over any plants

from the same origin site that had been transplanted at

the same destination site. This yielded 4–7 unique origin

3 destination site combinations for each of the four

combinations of origin region 3 destination region per

species. Data were log-transformed and analyzed with

two-way ANOVA, with origin region and destination

region as the main factors.

RESULTS

Herbivore counts and leaf damage

Overall, chewing herbivores and gall makers were

more abundant at low than at high latitudes, but sucking

herbivores did not show a clear latitudinal pattern.

Chewing herbivore damage was greater at low than at

high latitudes. We describe these patterns for each of the

plant species in turn.

Spartina alterniflora.—Overall densities of tettigoniid

grasshoppers did not differ between high- and low-

latitude sites (Fig. 1A); however, the tettigoniid com-

munity shifted from dominance by Conocephalus sparti-

nae (which does little damage to Spartina leaves) at high

latitudes to dominance by Orchelimum fidicinium (which

PLATE 1. Selected plant and herbivore species. Left to right: Solidago sempervirens, Eriophyid mite galls on leaf of Ivafrutescens, Hesperotettix floridensis, Trirhabda baccharidis. All photographs are by S. Pennings. A color plate showing these andmore of the species studied is available in digital Appendix B.


readily damages leaves) at low latitudes (Wason and

Pennings 2008). If the density estimates shown in Fig.

1A are adjusted to reflect the relative contribution to the

tettigoniid community of Orchelimum at high-latitude

(3%) and low-latitude (87%) sites (Wason and Pennings

2008), Orchelimum is 50-fold more abundant at low than

at high latitudes (high latitudes, 0.002 6 0.0008

individuals/m2 [mean 6 SD]; low latitudes, 0.11 6

0.037 individuals/m2; P ¼ 0.0001). The snail Littoraria

was absent at high latitudes and common at low

latitudes (Fig. 1B). The snail Melampus showed a

nonsignificant trend towards being more abundant at

high latitudes (Fig. 1C), but this snail does not do much

damage to living angiosperms (Pennings and Silliman

2005). The sucking leafhoppers Prokelisia did not differ

in abundance between high and low latitudes (Fig. 1D).

Damage to Spartina leaves from all chewing herbivores

was three times greater at low than at high latitudes

(Fig. 1E). Radulation damage was greater at low than at

high latitudes (Fig. 1F).

Juncus spp.—Densities of acridid grasshoppers did

not differ significantly between high- and low-latitude

sites, but tended to be higher at low latitudes (Fig. 2A).

As with Spartina, overall densities of tettigoniid

grasshoppers did not differ between high- and low-

latitude sites (Fig. 2B); however, the tettigoniid com-

munity shifted from dominance by Conocephalus sparti-

nae (which does little damage to Juncus leaves) at high

latitudes to dominance by Orchelimum concinnum

(which readily damages leaves) at low latitudes (E. L.

Wason and S. C. Pennings, personal observations). This

shift in species dominance, however, has not been

quantified. The snail Littoraria was absent at high

latitudes and common at low latitudes (Fig. 2C). The

snail Melampus showed a nonsignificant trend toward

being more abundant at high latitudes (Fig. 2D), but this

snail does not do much damage to living angiosperms

(Pennings and Silliman 2005). The omnivorous crab

Armases was absent at high latitudes and present at

moderate densities at low latitudes (Fig. 2E). Damage to

Juncus leaves from all chewing herbivores was two times

greater at low than at high latitudes (Fig. 2F).

Solidago sempervirens.—Density estimates of Solidago

herbivores were more variable than estimates of the

herbivores on other plant species because they were

based on smaller sampling units (individual Solidago

plants). For this reason, we detected no significant

differences in herbivore densities between high and low

latitudes; however, the trends for chewing herbivores

were similar to those found on other plants: both acridid

grasshoppers and beetles tended to be more abundant at

low latitudes (Fig. 3A, B). In contrast, sucking herbi-

vores (aphids) tended to be more abundant at high

latitudes (Fig. 3C). Damage to Solidago leaves from all

chewing herbivores was four times greater at low than at

high latitudes (Fig. 3D).

Iva frutescens.—Acridid grasshoppers were 50 times

more abundant at low than at high latitudes, whether

counted on individual shrubs (Fig. 4A) or on transects

through the shrub zone (Fig. 4B). Beetles (Ophraella and

FIG. 1. Latitudinal variation (mean þ SE) in herbivore densities and damage per leaf to Spartina alterniflora: (A) tettigoniidgrasshoppers; (B) the snail Littoraria irrorata; (C) the snail Melampus bidentatus (note that this species does little damage toSpartina); (D) Prokelisia planthoppers; (E) chewing damage to leaves; (F) radulation damage to leaves. High-latitude sites rangedfrom 418 to 448 N; low-latitude sites ranged from 318 to 368 N. Sample sizes (N¼ number of sites) are given first for the species athigh latitude and then for the species at low latitude.


Paria) were 20 times more abundant at low than at high

latitudes (Fig. 4C). The omnivorous crab Armases was

absent at high latitudes and present at moderate

densities at low latitudes (Fig. 4D). In contrast, sucking

herbivores (aphids) did not differ in abundance between

high and low latitudes (Fig. 4E). Terminal galls (Fig. 4F)

and leaf galls (Fig. 4G) were almost absent at high

latitudes and common at low latitudes. Damage to Iva

leaves from all chewing herbivores was 10 times greater

at low than at high latitudes (Fig. 4H).

Baccharis halimifolia.—Trirhabda beetles were 100

times more abundant at low than at high latitudes (Fig.

5A). Acridid grasshoppers were 10 times more abundant

at low than at high latitudes (Fig. 5B). Damage to

Baccharis leaves from all chewing herbivores was 10

times greater at low than at high latitudes (Fig. 5C).

Transplant experiments

Transplant experiments conducted with Spartina,

Solidago, and Iva all showed the same general patterns,

although the statistical details differed among plant

species (Fig. 6). First, plants transplanted to low-latitude

sites experienced two orders of magnitude more

herbivore damage than plants transplanted to high-

latitude sites (Fig. 6, ‘‘destination’’ effects). Second,

plants originating from high-latitude sites experienced

two to three times more herbivore damage than plants

originating from low-latitude sites (Fig. 6, ‘‘origin’’

effects; significant for Spartina and Iva; marginally

significant for Solidago). Finally, because the origin

effect was strong at low latitudes and weak at high

latitudes (where little herbivore damage occurred), there

was a significant origin 3 destination effect for Iva (Fig.

6C).

DISCUSSION

Past research in Atlantic Coast salt marshes has

documented strong latitudinal gradients in plant traits

and palatability, with low-latitude plants less palatable

to herbivores than high-latitude conspecifics. Data

presented in this paper suggest that herbivores may be

one cause of this pattern. Herbivores were more

abundant, and did more damage to plants, at low- vs.

high-latitude sites. The results, however, varied with

herbivore feeding guild, suggesting that future studies

would benefit from explicit comparisons of herbivores

from different feeding guilds.

Our results indicated that five groups of chewing

herbivores (i.e., acridid and tettigoniid grasshoppers,

beetles, snails, and a crab) were typically �10 times more

abundant at low- than at high-latitude sites. Although

these patterns were not statistically significant in every

case, there were no cases in which chewing herbivores

were most abundant at high latitudes. This geographic

pattern was not immediately apparent for two taxa,

tettigoniid grasshoppers and herbivorous snails, due to

geographic turnover in species with different feeding

behaviors. In both cases, the species that were most

abundant at high latitudes (Conocephalus spp. grass-

hoppers and Melampus bidentatus snails) do relatively

little damage to living angiosperm leaves, whereas the

species present at low latitudes (Orchelimum fidicinium

FIG. 2. Latitudinal variation (meanþSE) in herbivore densities and chewing damage per leaf to Juncus gerardii (high latitudes,solid bars) and J. roemerianus (low latitudes, open bars): (A) acridid grasshoppers; (B) tettigoniid grasshoppers; (C) the snailLittoraria irrorata; (D) the snail Melampus bidentatus (note that this species does little damage to Spartina); (E) the crab Armasescinereum; (F) chewing damage to leaves. Sample sizes are as described in Fig. 1.


grasshoppers and Littoraria irrorata snails) both readily

feed on living plant tissue (Silliman and Ziemann 2001,

Silliman and Bertness 2002, Silliman et al. 2005, Wason

and Pennings 2008). In the case of the snails, experi-

mental manipulations in the field indicated that Littora-

ria at densities as low as 50/m2 had negative effects on

biomass of the grass Spartina alterniflora at low-latitude

sites, but that Melampus at densities as high as 3000/m2

had no detectable effect on S. alterniflora biomass at

high-latitude sites (Pennings and Silliman 2005). In these

cases, simply counting consumers without a knowledge

of consumer feeding behavior would have led to

mistakes in interpreting the geographic patterns. The

two galling herbivores studied, a cecidomyiid fly and an

eriophyid mite (both found on Iva) were also far more

abundant at low- than at high-latitude sites.

In parallel to the pattern of increased abundance of

chewing herbivores at low latitude, chewing damage to

leaves was two to 10 times greater at low- than at high-

latitude sites. This result strongly supports the hypoth-

esis that herbivore pressure could be an important

selective force contributing to the observed pattern of

increased plant defenses and reduced plant palatability

at low- vs. high-latitude sites (Pennings et al. 2001, Siska

et al. 2002). As will be discussed, this does not rule out

other factors also contributing to latitudinal patterns in

plant palatability.

In striking contrast to chewing and galling herbivores,

sucking herbivores (Prokelisia spp. planthoppers and

two species of aphids) did not significantly differ in

abundance across latitude, and both aphid species

showed trends towards being more abundant at high

latitudes. Similarly, J. Hines (unpublished data) found

that sucking herbivores on Spartina alterniflora either

did not differ in abundance across latitude or increased

in abundance at high latitudes. We did not collect data

on damage from sucking herbivores, but it was likely

proportional to herbivore density. The four sucking

herbivores that we studied are smaller than the chewing

herbivores discussed previously, and all are multivoltine

(Denno 1977, Dixon 1985), whereas the chewing

herbivores, with one or two bivoltine exceptions (e.g.,

Ophraella beetles and possibly Paria beetles; Wilcox

1957, Futuyma 1990), have annual or longer life cycles

(Blake 1931, Abele 1992). For this reason, we speculate

that populations of chewing herbivores are limited at

high latitudes by the relatively short growing season and

by harsh physical conditions during the winter (Dob-

zhansky 1950). In contrast, because sucking herbivores

have multiple generations per year, we speculate that

their populations are better able to recover from winter

losses, and therefore may show a more equitable

distribution across latitude. In addition, we speculate

that latitudinal variation in top-down control from

predators may affect relatively large and relatively small

arthropods differently (Denno et al. 2002, 2003),

contributing to different latitudinal patterns in abun-

dance of these two groups. Past studies on latitudinal

variation in plant quality in the Atlantic Coast salt

marsh system did not include sucking herbivores

(Pennings et al. 2001). In salt marshes, however, plant

nitrogen content tends to increase and defensive

chemistry and toughness to decrease towards high

latitudes (Siska et al. 2002); therefore, it is also possible

that high-latitude plants would support faster popula-

tion growth of sucking herbivores during summer

months (C.-K. Ho, unpublished data). We doubt that

our results with the sucking herbivores reflect idiosyn-

cratic behavior of marsh species, because aphids in

FIG. 3. Latitudinal variation (mean þ SE) in herbivoredensities and chewing damage per leaf to Solidago sempervirens:(A) acridid grasshoppers; (B) beetles; (C) aphids; (D) chewingdamage to leaves. Sample sizes are as described in Fig. 1.


general decrease in abundance and diversity toward the

tropics, although the explanation for this pattern is not

well understood (Dixon 1998). Regardless of the

mechanisms explaining latitudinal patterns in abun-

dance of sucking herbivores, the fact that they are not

most abundant at low latitudes suggests that the pattern

of geographic variation in selection on plant traits

imposed by herbivores may vary among herbivore

feeding guilds. To the extent that chewing and sucking

herbivores select for different plant traits, there may be

strong selection for traits that deter chewing herbivores

at low latitudes, but little geographic variation in

selection for traits that deter sucking herbivores.

Our transplant experiments exposed plants from both

high and low latitudes to the ambient herbivore

populations in both geographic regions. These experi-

ments documented strong latitudinal differences in

herbivore pressure, with plants placed in low-latitude

sites accumulating two orders of magnitude more

herbivore damage than plants placed in high-latitude

sites. Thus, the results of these experiments confirmed

the geographic sampling in suggesting that damage from

chewing herbivores was much greater at low-latitude

than at high-latitude sites. The fact that the patterns

were more extreme in the transplant experiment than in

the geographic sampling likely reflects the fact that the

geographic sampling confounded latitude with plant

palatability, which is lower at low latitudes (Pennings et

al. 2001). Thus, the geographic sampling likely under-

estimated the potential differences in herbivore pressure

across latitude. In contrast, the transplant experiments

compared plants of the same quality placed at different

sites, and so standardized for plant quality. It is possible,

however, that herbivores aggregated on the plants

originating from high latitudes because they represented

small patches of highly palatable vegetation amidst an

extensive matrix of low-palatability vegetation when

placed at low-latitude sites. If so, the transplant

experiments might have overestimated the potential

differences in herbivore pressure across latitude. Because

both approaches yielded similar conclusions, we con-

clude that the general result is robust to the differences

in methodology, and that the exact latitudinal difference

in herbivore pressure likely lies somewhere in between

the results of the sampling and the results of the

transplant experiment.

In addition, because plants originating from high-

latitude sites experienced two to three times more

herbivore damage than plants originating from low-

latitude sites, the transplant experiments also confirmed

previous results showing latitudinal differences in plant

palatability (Pennings et al. 2001). Moreover, because

one of the test species, Iva, had been grown in common-

garden conditions from seeds or seedlings for a year

before the experiments and yet still displayed strong

differences in damage based on geographic origin, these

results also extend to a new species the previous

conclusion that a large proportion of the geographic

difference in plant palatability is genetically based

(Salgado and Pennings 2005).

We used three methods (herbivore counts, surveys of

damage, transplant experiments) to document latitudi-

nal variation in chewing herbivores. Each method has its

strengths and weaknesses. Count data provide direct

information on herbivore densities, but may be impre-

cise or variable for highly mobile herbivores such as

grasshoppers, or for small plants such as Solidago.

Moreover, the fact that we were forced to sample

FIG. 4. Latitudinal variation (mean þ SE) in herbivore densities and chewing damage per leaf to Iva frutescens: (A) acrididgrasshoppers (shrub counts); (B) acridid grasshoppers (transect counts); (C) beetles; (D) the crab Armases cinereum; (E) aphids; (F)terminal galls; (G) leaf galls; (H) chewing damage to leaves. Sample sizes are as described in Fig. 1.


different sites at different times of day, and on days with

different weather patterns, probably introduced a fair

bit of variability into the count data, although some of

this would have been ameliorated by the fact that we

sampled sites on multiple dates and averaged the results.

In addition, species with short life cycles (aphids,

planthoppers) might have peaked in abundance at sites

in between visits; however, this problem probably was

ameliorated by the fact that we sampled on multiple

dates, and would have been much less of an issue for the

other species with annual or multiyear life cycles.

Finally, herbivore counts may not predict herbivore

damage if per capita feeding rates differ among taxa or

geographically within taxa (Pennings and Silliman

2005). Surveys of chewing damage avoid these problems

by directly measuring damage, which integrates over

different times of day and different days for the life of

the leaf; however, observed damage confounds latitudi-

nal variation in herbivore abundance and per capita

feeding rates with latitudinal variation in plant palat-

ability (lower at low latitudes), and so may underesti-

mate herbivore pressure at low latitudes. The transplant

experiments avoided the latter problem by presenting

plants from the same origin sites to herbivore popula-

tions at high and low latitudes; but isolated, highly

palatable plants may be subject to aggregation by

herbivores. Thus, these experiments may have overesti-

mated herbivore pressure at low latitudes. In addition,

some plants originating from high-latitude sites ap-

peared water stressed when placed at hotter and saltier

low-latitude sites (Pennings and Bertness 1999, Bertness

and Pennings 2000), which could either increase or

decrease palatability to herbivores (Bernays and Lewis

1986). Thus, each method had different strengths and

weaknesses. Ultimately, the fact that all three methods

led to the same conclusions lends far more credibility to

the results than if we had used any one method alone.

FIG. 5. Latitudinal variation (mean þ SE) in herbivoredensities and chewing damage per leaf to Baccharis halimifolia:(A) the beetle Trirhabda baccharidis; (B) acridid grasshoppers;(C) chewing damage to leaves. Sample sizes are as described inFig. 1.

FIG. 6. Chewing herbivore damage per leaf (meanþ SE) onplants transplanted between high-latitude and low-latitudesites: (A) Spartina alterniflora, (B) Solidago sempervirens, and(C) Iva frutescens.


Similar but less extensive work suggests that a similar

latitudinal gradient in herbivore pressure occurs in

European salt marshes (Pennings et al. 2007). Plants

from low latitudes tended to experience more herbivore

damage than conspecifics or congeners from high

latitudes. Perhaps as a consequence, low-latitude plants

tended to be less palatable (better defended) than high-

latitude plants, and produced less palatable litter.

Although these results are far less extensive than

comparable studies on Atlantic Coast marshes in the

United States, the fact that the results are similar

suggests that the processes governing plant–herbivore

interactions in coastal salt marshes vary across latitude

in similar ways on different continents. Both United

States and European studies, however, have focused on

chewing arthropods, and have neglected herbivores that

are logistically harder to work with, such as mammals,

birds, and sucking arthropods. As noted previously, the

results presented here suggest that sucking arthropods

may show different patterns than chewing arthropods. It

would be valuable, therefore, to extend these studies to

these other groups of herbivores in order to assess their

generality.

This paper has focused on Atlantic Coast salt

marshes, but the evidence available to date suggests

that similar patterns occur in other habitat types. In

broad-leaved forests, annual rates of herbivory are

greater in tropical than in temperate sites, and tropical

plants tend to have more extensive chemical defenses

and tougher but less nutritious leaves than temperate

plants, and to rely more heavily than temperate plants

on ant associates to deter herbivores (Coley and Aide

1991, Coley and Barone 1996). These patterns, however,

are not universal (Andrew and Hughes 2005) and may

reverse at very high latitudes (Bryant et al. 1994).

Additional studies are needed to compare herbivore

pressure and plant palatability across latitude in a wider

range of terrestrial communities.

On subtidal reefs, herbivory rates are generally greater

in the tropics than in the temperate zone (Gaines and

Lubchenco 1982, Hay 1991) and tropical algae tend to

be less palatable and to have more effective chemical

defenses than temperate algae (Steneck 1986, Hay and

Fenical 1988, Bolser and Hay 1996), although the

quality of the data is, with some exceptions, mostly

anecdotal or circumstantial (Hay 1996). Some results are

inconsistent among studies. For example, different

geographic regions appear to support different latitudi-

nal patterns in phlorotannin concentrations (Steinberg

1992), and results differ regarding whether phlorotan-

nins from temperate algae are capable of deterring

herbivory by tropical consumers (Van Alstyne and Paul

1990, Steinberg et al. 1991). Additional studies are

needed to clarify these patterns and to compare

herbivore pressure and plant palatability across latitude

in a wider range of marine communities.

Latitudinal differences in plant and seaweed defenses

appear to have selected for latitudinal differences in

herbivore ‘‘offense’’ (Cronin et al. 1997, Toju and Sota

2006) and feeding behavior (Sotka and Hay 2002, Sotka

et al. 2003), with herbivores at low latitudes possessing a

greater ability to tolerate or overcome plant defenses, or

showing greater discrimination among potential host

plants. Such adaptations, however, are likely to come at

a cost. Everything else being equal, herbivores feeding

on low-latitude diets with lower nutritional quality,

increased toughness, or increased chemical defenses are

likely to grow more slowly than herbivores feeding on

high-latitude, high-quality diets (C.-K. Ho and S. C.

Pennings, unpublished data). Slower growth will expose

herbivores to a variety of additional sources of

mortality. In particular, it is likely that low-quality diets

at low latitudes, by slowing herbivore growth, will

increase the potential for top-down control of herbi-

vores by predators (Coley and Barone 1996). As a result,

latitudinal variation in plant quality could interact with

top-down control to produce different types of control

on food web structure across latitude.

In summary, we suggest that herbivore pressure and

plant quality to herbivores may vary across latitude in

both terrestrial and marine systems, with likely conse-

quences for interactions with the third trophic level. At

present, data supporting this statement are limited and

vary widely in quality. If these patterns are truly general,

however, these geographic differences in plant–herbi-

vore interactions, plant–herbivore coevolutionary pro-

cesses, and food web controls (and any exceptions) must

be incorporated into any general theory of ecology and

evolution (Thompson 1994, 2005).

Finally, although we have presented compelling

evidence that herbivore pressure varies with latitude in

Atlantic Coast salt marshes, this does not rule out the

possibility that other factors also vary with latitude. In

particular, bottom-up effects on plants such as N and P

availability, physical stress (salinity, drought, tempera-

ture), and trade-offs between growth and defense driven

by growing season length are all likely to vary with

latitude and to affect leaf traits (Bryant et al. 1983,

Coley and Aide 1991, Coley and Barone 1996, Reich and

Oleksyn 2004, Wright et al. 2004, Thompson et al. 2007).

These factors likely interact with herbivore pressure to

mediate coevolutionary interactions between plants and

herbivores in ways that are currently poorly understood,

but deserve further attention.

ACKNOWLEDGMENTS

We thank L. Block, A. Bortolus, J. Daughtry, C. Gormally,L. Johnson, E. King, K. Leach, C. McFarlin, Kvita Dave-Coombe, and D. Pamplin for assistance in the field andgreenhouse. We thank M. Bertness, R. Denno, C. Hopkinson,and B. Silliman for advice, assistance with field sites, orcomments on a draft of the manuscript. We are grateful to theNERR and LTER networks and the local managers of all thestudy sites for allowing access and for their assistance. Thismanuscript is based upon work supported by the NationalScience Foundation (DEB 0296160, DEB-0638796, OCE99-82133), the National Geographic Society (5902-97), NOAA(NERR fellowship to C.-K. Ho), and the Baruch Marine Field


Laboratory (Visiting Scientist Award to S. C. Pennings). This iscontribution number 971 from the University of GeorgiaMarine Institute. This work is a contribution of the GeorgiaCoastal Ecosystems LTER program.

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APPENDIX A

List of study sites and plant species sampled at each site (Ecological Archives E090-011-A1).

APPENDIX B

Photographs of selected plant and herbivore species studied (Ecological Archives E090-011-A2).


latitudinal variation in herbivore pressure in atlantic

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