Ecology, 90(1), 2009, pp. 183–195 Ó 2009 by the Ecological Society of America
Latitudinal variation in herbivore pressure in Atlantic Coast salt marshes STEVEN C. PENNINGS,1 CHUAN-KAI HO, CRISTIANO S. SALGADO,2 KAZIMIERZ WIESKI ˛ , NILAM DAVE´,3 AMY E. KUNZA,4 5 AND ELIZABETH L. WASON Department of Biology and Biochemistry, University of Houston, Texas 77204 USA
Abstract. Despite long-standing interest in latitudinal variation in ecological patterns and processes, there is to date weak and conflicting evidence that herbivore pressure varies with latitude. We used three approaches to examine latitudinal variation in herbivore pressure in Atlantic Coast salt marshes, focusing on five abundant plant taxa: the grass Spartina alterniflora, the congeneric rushes Juncus gerardii and J. roemerianus, the forb Solidago sempervirens, and the shrubs Iva frutescens and Baccharis halimifolia. Herbivore counts indicated that chewing and gall-making herbivores were typically 10 times more abundant at low-latitude sites than at high-latitude sites, but sucking herbivores did not show a clear pattern. For two herbivore taxa (snails and tettigoniid grasshoppers), correctly interpreting latitudinal patterns required an understanding of the feeding ecology of the species, because the species common at high latitudes did not feed heavily on plant leaves whereas the related species common at low latitudes did. Damage to plants from chewing herbivores was 2–10 times 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 highlatitude sites, and two to three times greater for plants originating from high- vs. low-latitude sites. Taken together, these results provide compelling evidence that pressure from chewing and 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 due to greater herbivore damage at low latitudes is likely to partially explain documented patterns of low plant palatability to chewing herbivores and greater plant defenses at low latitudes, but other 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 everywhere. Many species are widely distributed, but interactions 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 conspecifics 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 adaptaManuscript received 1 February 2008; revised 29 April 2008; accepted 14 May 2008. Corresponding Editor: J. F. Bruno. 1 E-mail:
[email protected] 2 Present address: StatoilHydro, Department of Health, Safety and Environment, Praia de Botafogo, 300—Eighth floor, 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.
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, MacArthur 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 experimental designs (Pennings et al. 2001). In the case of plant–herbivore interactions, a number of studies
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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 congeners (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 environment, such as temperature, humidity, nutrient availability, 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
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latitude, but doing this is quite labor intensive and, to the best of our knowledge, has not been done except for preliminary work by our group (Pennings and Silliman 2005). A somewhat easier approach would be to compare visible damage to leaves across latitude (Coley and Aide 1991). This approach might be inaccurate if some herbivores completely consume leaves, if leaf longevity differs among sites, or if leaves from different regions differ in palatability. All of these concerns are likely to apply, especially when plant taxa turn over across latitude; nevertheless, studies that have used this approach 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 compare herbivory levels on ‘‘phytometers’’ (e.g., standard plants placed at multiple sites; Hay 1984). This approach overcomes a number of the limitations involved in measuring herbivory on local vegetation because plant species, palatability, and leaf age can be standardized, but is more labor intensive and, to the best of our knowledge, has not been done. Finally, a fourth approach would be to conduct herbivore manipulation experiments across latitude. This method is the most labor 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 grass Spartina 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) herbivores are more abundant, and (2) do more damage to plants in low- vs. high-latitude salt marshes. Although these methods do not measure natural selection per se, documenting a strong geographic gradient in herbivory would lend support to the hypothesis that geographic variation in herbivory selects for geographic variation in plant traits. METHODS Study sites and species We worked at 39 study sites ranging from northern Florida to southern Maine (Appendix A). Most of these sites 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, New Hampshire, 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 sites were 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 on comparing high- and low-latitude regions, because the transplant experiments used high- and low-latitude sites as geographic replicates, and to minimize the logistical
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TABLE 1. Plant and herbivore species. Zone
Plant species
Latitude
Herbivore species sampled Orthoptera: Tettigoniidae. Concephalus spartinae, Orchelimum fidicinium Gastropoda. Littoraria irrorata, Melampus bidentatus Homoptera: Dephacidae. Prokelisia marginata, Prokelisia dolus Orthoptera: Acrididae. Paroxya clavuliger Orthoptera: Tettigoniidae. Concephalus spartinae, Conocephalus spp., Orchelimum concinnum Gastropoda. Littoraria irrorata, Melampus bidentatus Decapoda: Grapsidae. Armases cinereum Orthoptera: Acrididae. Paroxya clavuliger, Melanoplus bivittatus Coleoptera: Chrysomelidae. Erynephala maritima Hemiptera: Aphididae. Uroleucon pieloui Orthoptera: Acrididae. Paroxya clavuliger, Hesperotettix floridensis, Melanoplus spp. Coleoptera: Chrysomelidae. Ophraella notulata, Paria aterrima Decapoda: Grapsidae. Armases cinereum Hemiptera: Aphididae. Uroleucon ambrosiae Diptera: Cecidomyiidae. Asphondylia sp. Chelicerata: Acarina. Eriophyid mites Coleoptera: Chrysomelidae. Trirhabda baccharidis Orthoptera: Acrididae. Various spp.
Low marsh
Spartina alterniflora (Poaceae), smooth cordgrass
high and low
Middle marsh
Juncus gerardi (Juncaceae), black grass
high
J. roemerianus (Juncaceae), needle rush Solidago sempervirens (Asteraceae), seaside goldenrod
low
Marsh terrestrial border
Iva frutescens (Asteraceae), marsh elder
high and low
Marsh terrestrial border
Baccharis halimifolia (Asteraceae), silverling or groundsel tree.
high and low
High marsh and terrestrial border
high and low
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.
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 dominates 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, grasshoppers, crabs, and snails, but we also sampled the most common representatives from the sucking and gallmaking 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 elevations 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,
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which at high densities can damage S. alterniflora leaves by producing linear patterns of damage termed ‘‘radulations’’ (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, respectively. 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 grasshopper 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, and averaged over replicates and then over dates to yield 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
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by searching entire individual plants. The length and width of two leaves was measured, and leaf area estimated as an ellipse. Herbivore counts were standardized 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, and averaged over replicates and then over dates to yield 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. Herbivore counts were standardized by plant volume (estimated 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 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. Transplant experiments The sampling described in the previous section might be criticized on the grounds that we know that low-
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PLATE 1. Selected plant and herbivore species. Left to right: Solidago sempervirens, Eriophyid mite galls on leaf of Iva frutescens, Hesperotettix floridensis, Trirhabda baccharidis. All photographs are by S. Pennings. A color plate showing these and more of the species studied is available in digital Appendix B.
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 transplanting individual plants between high- and lowlatitude 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 elevational 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 conducted during seasons with high herbivore abundance for each plant species: late July to late August of 2003 for Spartina (N ¼ 158), mid-July to mid-August of 2002 for Solidago (N ¼ 152), and mid-June to mid-July of 2005 for Iva (N ¼ 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 lowlatitude sites (Fig. 1A); however, the tettigoniid community shifted from dominance by Conocephalus spartinae (which does little damage to Spartina leaves) at high latitudes to dominance by Orchelimum fidicinium (which
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FIG. 1. Latitudinal variation (mean þ SE) in herbivore densities and damage per leaf to Spartina alterniflora: (A) tettigoniid grasshoppers; (B) the snail Littoraria irrorata; (C) the snail Melampus bidentatus (note that this species does little damage to Spartina); (D) Prokelisia planthoppers; (E) chewing damage to leaves; (F) radulation damage to leaves. High-latitude sites ranged from 418 to 448 N; low-latitude sites ranged from 318 to 368 N. Sample sizes (N ¼ number of sites) are given first for the species at high latitude and then for the species at low latitude.
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 lowlatitude sites (Fig. 2B); however, the tettigoniid community shifted from dominance by Conocephalus spartinae (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 herbivores (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
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FIG. 2. Latitudinal variation (mean þ SE) 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 snail Littoraria irrorata; (D) the snail Melampus bidentatus (note that this species does little damage to Spartina); (E) the crab Armases cinereum; (F) chewing damage to leaves. Sample sizes are as described in Fig. 1.
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 highlatitude 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. grasshoppers and Melampus bidentatus snails) do relatively little damage to living angiosperm leaves, whereas the species present at low latitudes (Orchelimum fidicinium
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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, experimental manipulations in the field indicated that Littoraria 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 highlatitude sites. This result strongly supports the hypothesis 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 (Dobzhansky 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 abundance of these two groups. Past studies on latitudinal
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FIG. 3. Latitudinal variation (mean þ SE) in herbivore densities and chewing damage per leaf to Solidago sempervirens: (A) acridid grasshoppers; (B) beetles; (C) aphids; (D) chewing damage to leaves. Sample sizes are as described in Fig. 1.
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 population growth of sucking herbivores during summer months (C.-K. Ho, unpublished data). We doubt that our results with the sucking herbivores reflect idiosyncratic behavior of marsh species, because aphids in
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FIG. 4. Latitudinal variation (mean þ SE) in herbivore densities and chewing damage per leaf to Iva frutescens: (A) acridid grasshoppers (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.
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 abundance 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 experiments 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 underestimated 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 conclude 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 highlatitude sites experienced two to three times more herbivore damage than plants originating from lowlatitude 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 commongarden 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 latitudinal variation in chewing herbivores. Each method has its strengths and weaknesses. Count data provide direct information on herbivore densities, but may be imprecise 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
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mate herbivore pressure at low latitudes. The transplant experiments avoided the latter problem by presenting plants from the same origin sites to herbivore populations at high and low latitudes; but isolated, highly palatable plants may be subject to aggregation by herbivores. Thus, these experiments may have overestimated herbivore pressure at low latitudes. In addition, some plants originating from high-latitude sites appeared 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 herbivore densities 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 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 latitudinal variation in herbivore abundance and per capita feeding rates with latitudinal variation in plant palatability (lower at low latitudes), and so may underesti-
FIG. 6. Chewing herbivore damage per leaf (mean þ SE) on plants transplanted between high-latitude and low-latitude sites: (A) Spartina alterniflora, (B) Solidago sempervirens, and (C) Iva frutescens.
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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 highlatitude 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 latitudinal patterns in phlorotannin concentrations (Steinberg 1992), and results differ regarding whether phlorotannins 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
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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 herbivores 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 consequences 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–herbivore interactions, plant–herbivore coevolutionary processes, 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, temperature), 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 and greenhouse. We thank M. Bertness, R. Denno, C. Hopkinson, and B. Silliman for advice, assistance with field sites, or comments on a draft of the manuscript. We are grateful to the NERR and LTER networks and the local managers of all the study sites for allowing access and for their assistance. This manuscript is based upon work supported by the National Science Foundation (DEB 0296160, DEB-0638796, OCE9982133), the National Geographic Society (5902-97), NOAA (NERR fellowship to C.-K. Ho), and the Baruch Marine Field
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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).
