Oikos 116: 543  549, 2007 doi: 10.1111/j.2007.0030-1299.15591.x, Copyright # Oikos 2007, ISSN 0030-1299 Subject Editor: Lonnie Aarssen, Accepted 11 November 2006



Latitudinal variation in plant herbivore interactions in European salt marshes Steven C. Pennings, Martin Zimmer, Nata´lia Dias, Martin Sprung, Nilam Dave´, Chuan-Kai Ho, Amy Kunza, Caroline McFarlin, Malte Mews, Anett Pfauder and Cristiano Salgado S. C. Pennings ([email protected].), N. Dave´, C.-K. Ho and A. Kunza, Dept of Biology and Biochemistry, Univ. of Houston, Houston, TX 77204, USA. Present address for ND: 300 NC 54 Apartment C5, Carrboro, NC 27510, USA.  M. Zimmer, M. Mews and A. Pfauder, Zoologisches Institut: Limnologie, Christian Albrechts Univ., Olshausenstr. 40, DE-24098 Kiel, Germany. Present address for AP: Ahlmannstrasse 12, DE-24118 Kiel, Germany.  N. Dias and M. Sprung, Faculdade de Cieˆncias do Mar e do Ambiente, Univ. do Algarve, Campus de Gambelas, PT-8005-139 Faro, Portugal. Present address: School of Environmental Sciences, Univ. of East Anglia, Norwich, UK, NR4 7TJ.  C. McFarlin, Dept of Marine Sciences, Univ. of Georgia, Athens, GA 30602, USA.  C. Salgado, ENSR International, Praia de Botafogo, 440/24o, Rio de Janeiro-RJ, Brasil.

Ecological interactions often vary geographically. Work in salt marshes on the Atlantic Coast of the United States has documented community-wide latitudinal gradients in plant palatability and plant traits that may be driven in part by greater herbivore pressure at low latitudes. To determine if similar patterns exist elsewhere, we studied six taxa of saltmarsh plants (Atriplex , Juncus , Limonium , Salicornia , Spartina and Suaeda ) at European sites at high (Germany and the Netherlands) and low (Portugal and Spain) latitudes. We conducted feeding assays using both native and non-native consumers, and documented patterns of herbivore damage in the field. As in the United States, high-latitude plants tended to be more palatable than low-latitude plants when offered to consumers in paired feeding assays in the laboratory, although assays with grasshopper consumers were less consistent than those with crab consumers, and plants in the field at low-latitude sites tended to experience greater levels of herbivore pressure than plants at high-latitude sites. Similarly, high-latitude leaf litter was more palatable than litter from low-latitude plants when offered to consumers in paired feeding assays in the laboratory. Latitudinal gradients in plant palatability and herbivore pressure may be a general phenomenon, and may contribute to latitudinal gradients in decomposition processes.

Species often have large geographic ranges, but interactions among species occur locally (Menge 2003). At any given site, local abiotic conditions and community composition mediate interactions between organisms, creating different selective pressures than those experienced by conspecifics at other sites (Dunson and Travis 1991, Sotka and Hay 2002, Toju and Sota 2006). As a result of local differences in both ecological context and local adaptation, the nature of interactions between species may vary geographically (Thompson 1988, Travis 1996, Callaway et al. 2002, Sotka et al. 2003). If so, an understanding of the nature of this geographic variation will be an essential component of any general theory of species interactions (Thompson 1994, 2005).

One simple way that interactions among species might vary geographically is as a monotonic gradient across latitude. Ecologists have long speculated 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 assertions (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 good experimental design (Pennings et al. 2001). A number of studies support the hypothesis that plant-herbivore interactions are

543

more intense at lower latitudes (Coley and Aide 1991, Bolser and Hay 1996), but exceptions exist (Bryant et al. 1994), and many early studies suffered from limitations in design (reviewed by Pennings et al. 2001). One of the most comprehensive studies of latitudinal variation in plant herbivore interactions comes from coastal salt marshes on the Atlantic Coast of the United States, where similar plant communities extend from central Florida through Maine. For ten species of plants (the bulk of the plant 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 rather than induced (Salgado and Pennings 2005), and were linked to differences in plant nitrogen content, toughness, and chemical defenses (Siska et al. 2002). Herbivore pressure was greater at low latitudes (Pennings and Silliman 2005), and likely contributed to the different selective environments that produced plants with different traits at low versus high latitudes. It is likely that other factors in addition to herbivore pressure contribute to selecting for differences in plant traits that affect herbivory at low versus high latitudes, but these have not yet been studied. Because the characteristics of leaf litter reflect the characteristics of the leaves that produce the litter (Grime et al. 1996, Cornelissen et al. 2004), it is likely that less palatable leaves will produce less palatable litter. If so, we might expect to see the same latitudinal gradients in litter detritivore interactions that we see in plant herbivore interactions. Because detritivores play a basic role in mediating decomposition in many systems, a latitudinal gradient in litter palatability might lead to important differences in mechanisms of nutrient cycling between high- and low-latitude systems. This hypothesis, however, has not been tested to date. Although salt marsh studies from the Atlantic Coast of the US support the theory that plant herbivore interactions are more intense at low versus high latitudes, one could argue that this body of work represents only a single geographic gradient, and thus could be an artifact of some unique feature of the US Atlantic Coast. To be confident that this is a general result, one would like to replicate these results across latitudinal gradients elsewhere in the world. Here, we test the hypotheses that latitudinal gradients in 1) plant palatability, 2) litter palatability and 3) herbivore pressure also occur in European salt marshes. Our results suggest that latitudinal gradients in plant  herbivore interactions are a general phenomenon, and suggest that these gradients may also affect decomposition processes.

544

Methods Latitudinal comparisons of plant palatability To compare the palatability of high- and low-latitude leaves and leaf litter, we collected plant material from three sites in Germany and two sites in Portugal (Appendix 1). German sites represented both the Baltic and North Sea coasts. None of the sites had been subject to intensive livestock grazing in recent years, although some had been grazed in the past. We collected six taxa of plants in both geographic regions. In one case (Suaeda maritima) conspecifics were collected from the two geographic regions; in four cases, congeners; and in one case (Salicornia , Sarcocornia , Arthrocnemum ) a trio of morphologically-similar and closely-related genera (which are united in one genus in some taxonomic treatments). Thus, although these comparisons did not necessarily involve ‘‘identical’’ species at both latitudes, they did represent six independent comparisons in which phylogeny was controlled. Collections were made in the first two weeks of August, 2001, except for Atriplex hastata from Germany, which was collected in the second week of September, 2001. Live leaves were healthy and green; leaf litter was either standing-dead or fallen-dead, as appropriate for the species. For every species, material from each site represented multiple individual plants. Plant material was pooled, lyophilized and ground to a fine powder. The palatability of pairs of plants from the two geographic regions was compared in two-choice feeding assays using a detritivore from German salt marshes (the isopod Porcellio scaber , n /7 assays), and an omnivore from American salt marshes (the grapsid crab Armases cinereum , n /15 assays). We will refer to both species generically hereafter. Previous studies concluded that latitudinal differences in palatability were perceived similarly by a wide variety of consumers, with no indication of bias for or against ‘‘local’’ plants (Pennings et al. 2001); therefore, we selected these consumers for tractability in the laboratory. Porcellio is common among stranded litter at the upper fringe of German salt marshes (Pfauder and Zimmer 2005). Armases is a semi-terrestrial crab that is common at the upper fringe of salt marshes along the southeastern coast of the United States (Abele 1992). We used it as an assay organism because it is an omnivore that will readily eat both leaves and litter of a variety of salt marsh plants (Pennings et al. 1998, 2001, Siska et al. 2002, Buck et al. 2003) and because it was naı¨ve with respect to most of the plants studied. Only 2 of 12 taxa, Salicornia europaea and Suaeda maritima, occur in the southeastern United States, where they are both quite rare (Pennings, pers. obs.). We therefore expected

Armases not to favor plants from either geographic region on the basis of familiarity or novelty. We conducted four additional assays with herbivorous grasshoppers (Paroxya clavuliger , Orchelimum fidicinium , Orphulella pelidna) from the southeastern coast of the United States, limiting these assays to plant taxa that the grasshoppers would readily consume. Grasshoppers were naı¨ve with respect to all tested plant species. Sites were haphazardly paired for feeding comparisons. When possible, we replicated comparisons using more than one site from each geographic region to ensure that results were not site-dependent. Feeding assays with Porcellio Ground plant material was incorporated into an artificial diet. Agar (0.8 g) was dissolved in boiling water (20 ml). As the agar cooled, plant powder (4 g) was thoroughly stirred into the mixture. The diet was poured into the lid of a petri plate (9 cm diameter) and the inverted bottom of the petri plate was pressed into the lid in order to flatten the diet to a consistent thickness. After the diet cooled, we cut it into pieces for use in feeding trials. To determine the wet:dry ratio of the final mixture, four large pieces of the diet were removed, weighed, dried (508C, 24 h) and weighed again. Groups of five Porcellio were housed in petri dishes (9 cm diameter). We lined the lid of each petri dish with a piece of wet filter paper in order to maintain humid conditions. Each group of isopods was offered a choice between a high- and a low-latitude diet. Individual replicates (n /15) were stopped when at least ½ of one of the diets had been consumed, or after 4 d. Autogenic controls (n /510), which were treated identically except that they lacked isopods, were stopped in parallel with experimental replicates. Diets were weighed at the beginning of the experiment, and their dry mass calculated based on the wet:dry ratio of the diet. After the replicate was stopped, remaining diets were dried and re-weighed to calculate the dry mass consumed. The difference in mass change of the autogenetic controls was compared with the difference in mass change of the corresponding experimental diets using a paired t-test (Peterson and Renaud 1989). For clarity, only mass change of diets exposed to isopods is shown in figures. Feeding assays with Armases Assays with Armases were similar and followed Siska et al. (2002). Briefly, ground plant material in an agar diet was poured into a template resting on a screen with 1 mm2 openings. Assays were stopped when substantial feeding on at least one diet had occurred, or after 3 d.

Consumption was measured as mm2 of screen exposed by feeding, and was compared between regions using a paired t-test. Geographic survey of herbivore damage To determine if herbivore pressure could be selecting for geographic patterns of palatability, we measured damage to leaves by chewing herbivores on plants in 10 high- (Germany, The Netherlands) and 10 low-latitude (Portugal, Spain) sites (Appendix 2). At each site, we sampled 6 8 individuals of each species. Damage was estimated by visual estimates of missing leaf area (Atriplex , Juncus , Limonium , Spartina, 23 leaves/ plant, averaged to yield a single value/plant) or by counting the percentage of damaged segments out of 100 (Salicornia /Sarcocornia /Arthrocnemum ) or the percentage of damaged leaves out of 100 (Suaeda ). For statistical purposes, values from multiple leaves/plant were averaged to yield a single value/plant. Multiple plants within a site were then averaged to yield a single site mean for each variable at each site. Geographic comparisons used sites as replicates.

Results Using the conventional cutoff of pB/0.05 to indicate statistical significance, one would expect 1.3 assays out of 26 to be ‘‘significant’’ by chance alone. Twenty out of 26 of our feeding assays were significant, making it very unlikely that our results were due to chance. Given a choice between reconstituted leaves from high- and low-latitude sites, Armases tended to eat more of the high-latitude diet in 9 out of 10 cases; 8 of these comparisons were statistically significant (Fig. 1). In the tenth case (Limonium ), Armases preferred the lowlatitude diet. Grasshoppers significantly preferred the high-latitude diet in one case (Atriplex ), showing the same preferences for this taxa as did Armases . Grasshoppers preferred the low-latitude diet in three cases (Spartina, 2 of 3 assays significant), showing opposite feeding preferences for this taxa as did Armases . Given a choice between reconstituted leaf litter from high- and low-latitude sites, Porcellio tended to eat more of the high-latitude diet in 6 of 7 cases; 4 of these comparisons were statistically significant (Fig. 2). In the seventh case (Atriplex ), consumption of high- and lowlatitude diets was similar. Armases ate more of the highthan the low-latitude leaf litter diet in 5 out of 5 cases. Geographic surveys generally supported the hypothesis that damage from chewing herbivores was greater at low than high latitudes (Fig. 3). Limonium , Salicornia and Suaeda all had more herbivore damage at lowversus high-latitude sites. Juncus and Spartina had very

545

80

P<0.0001 P<0.0001

North South

P<0.0001

P<0.0001

Consumption (mm2)

60

P=0.005 P=0.008 P=0.008

P=0.0003 P=0.22

40

P=0.01

P=0.0004

P<0.0001

P=0.23 P=0.03

20

0 N= Consumer: Plant: Sites:

14 A A S/I

10 A A B/F

15 A J B/I

20 A J W/F

13 A L W/I

17 A Sa W/F

8 A Sa B/I

16 A Sp/M W/F

14 14 A A Sp/D Su W/I W/I

17 P A S/I

14 Of Sp/M W/F

10 Op Sp/M W/I

15 Of Sp/D W/I

Fig. 1. Consumption of reconstituted high vs low latitude leaves in paired feeding trials. Data are means9/1 SE; sample sizes, consumer species, plant species, and collection sites are indicated below paired bars. Consumers: A, Armases ; P, Paroxya ; Of, Orchelimum ; Op, Orphulella . Plants: A, Atriplex hastata (N) vs A. portulacoides (S); J, Juncus gerardi (N) vs J. maritima (S); L, Limonium vulgare (N) vs L. algarvensis (S); Sa, Salicorina europaea (N) vs Sarcocornia spp. (S); Sp, Spartina anglica (N) vs M, S. maritima , or D, S. densiflora (S); Su, Suaeda maritima (N vs S). Sites: B, Bottsand, Germany; W, Westerhever, Germany; S, Schobu¨ll, Germany; I, Bias, Portugal; F, Faro, Portugal. See Appendix 1 for additional information on sites.

little damage in either geographic region. In the case of Atriplex, low-latitude individuals of A. hastata tended to display more damage than high-latitude individuals of A. hastata ; however, this comparison was not

statistically significant because we only located A. hastata at 3 low-latitude sites. Low-latitude individuals of A. portulacoides had less damage than high-latitude A. hastata .

P<0.0001 North South

0.012

P<0.0001

P<0.0001

P<0.0001

70

P<0.0001 60

0.010

50

P=0.02

0.008

P=0.41 P=0.99

40

0.006 P=0.001

P=0.003 30

P=0.03 0.004

20 0.002

0.000 N= Consumer: Plant: Sites:

Consumption (mm2)

Consumption (g)

P=0.13

10

0 15 C A B/F

15 C A W/I

12 C L W/F

15 C L W/I

15 C Sp/M W/I

14 C Sp/M W/F

15 C Sp/D W/I

4 A A W/I

12 A L W/F

9 A L W/I

13 A Sp/M W/F

15 A Sp/D W/I

Fig. 2. Consumption of reconstituted high vs low latitude leaf litter in paired feeding trials. Data are means9/1 SE; sample sizes, consumer species, plant species, and collection sites are indicated below paired bars. Consumers: A, Armases ; C, Porcellio . Plants: A, Atriplex hastata (N) vs A. portulacoides (S); L, Limonium vulgare (N) vs L. algarvensis (S); Sp, Spartina anglica (N) vs M, S. maritima , or D, S. densiflora (S). Site abbreviations as in Fig. 1. See Appendix 1 for additional information on sites.

546

25

North South South (2)

Damage (%)

20

15

P=0.01 n=7, 8

N vs S, P=0.27 N vs S2, P=0.02 n=9, 3, 5 P=0.02 n=6, 9

10

P=0.02 n=7, 9

5

0

A

L

Sa

Su

Fig. 3. Geographic patterns in damage by chewing herbivores. Data are means9/1 SE; plant species are indicated below paired bars. In the case of Atriplex , two southern species were compared with one northern species. Sample sizes are number of sites. Data for Spartina and Juncus spp. are not shown because most values were zero or very low. Plants: A, Atriplex hastata (N) vs Atriplex hastata (S) or A. portulacoides (S2); L, Limonium vulgare (N) vs Limonium spp. (S); Sa, Salicorina europaea (N) vs Salicornia europaea and Sarcocornia spp. (S); Su, Suaeda maritima (N vs S). See Appendix 2 for more information on sites.

Discussion Ecologists have long been interested in the hypothesis that herbivore pressure is greater at low versus high latitudes (Gaines and Lubchenco 1982). Some studies have supported this hypothesis (Bolser and Hay 1996, Coley and Aide 1991, Toju and Sota 2006), but others have not (Bryant et al. 1994), and experimental design compromises in some early studies have hindered interpretation of results (reviewed by Pennings et al. 2001). The most comprehensive studies, in salt marshes on the Atlantic Coast of the US, strongly supported the hypotheses that high-latitude plants were less palatable than low-latitude conspecifics (Pennings et al. 2001, Siska et al. 2002, Salgado and Pennings 2005), and that high levels of herbivory at low-latitude sites might select for reduced palatability (Pennings and Silliman 2005). Here, we extend these results to European salt marshes. Although this data set from Europe is less extensive than that from the US, the results are largely consistent between regions. High-latitude plants were generally more palatable than low-latitude congeners, and this result carried over from leaves to leaf litter. The generalist omnivore Armases preferred to eat high- versus low-latitude leaves in 8 out of 10 comparisons. This strong preference for high-latitude leaves is similar to the results we previously obtained from salt marshes on the Atlantic Coast of the US (Pennings et al. 2001, Siska et al. 2002), and strongly suggests that high-latitude plants are in general more

palatable than low-latitude congeners. Results with grasshoppers were less conclusive, with one assay indicating a preference for high-latitude plants, two for low-latitude plants, and one no preference. The latter three assays all involved contrasts between Spartina anglica (high-latitude) and S. maritima or S. densiflora (low-latitude), and may simply reflect a low palatability of Spartina anglica to grasshoppers. The only time that Armases preferred the low-latitude plant was in the case of Limonium , but only one assay was run with Limonium and so we cannot be sure how repeatable this result would be. Results for leaf litter showed a striking preference for high-latitude material. Both the detritivore Porcellio and the omnivore Armases preferred to eat litter of high- versus low-latitude leaves (4 of 7 and 5 of 5 comparisons, respectively). In no case was the litter of low-latitude leaves significantly preferred. Because much of the physical structure and some of the secondary chemistry of leaves is retained in leaf litter, it is not surprising that leaves of unpalatable plants might produce unpalatable litter (Grime et al. 1996, Cornelissen et al. 2004). Thus, any factor that selects for geographic differences in leaf palatability to herbivores is likely to also create differences in litterdetritivore interactions across geographic scales. If so, this might also affect geographic variation in ecosystem processes, with litter being more recalcitrant to decomposition at low versus high latitudes. Because of logistic constraints, we worked with ground, freeze-dried plant material rather than unmanipulated leaves or litter. Our previous work suggested that processing plant material tends to reduce geographic differences (Siska et al. 2002), likely because differences in toughness are reduced when plant material is ground, and secondary chemicals may volatilize or degrade with processing. We speculate, therefore, that our results are likely to be conservative, and hypothesize that geographic differences in palatability of fresh leaves and litter are probably greater than suggested here. In studies on the Atlantic Coast of the US, latitudinal differences in plant palatability were linked to latitudinal differences in leaf toughness, nitrogen content and chemical defenses (Siska et al. 2002). We did not address these mechanisms in the present study; however, preliminary data (not shown) suggested that some taxa differed geographically in nitrogen content and toughness. Thus, these leaf traits and others may have played proximate roles in creating geographic differences in palatability in European marshes. Geographic surveys of leaf damage generally supported the hypothesis that herbivore pressure was greater at low latitudes, and thus, that herbivore pressure might be one factor selecting for lower palatability at low latitudes. Latitudinal patterns in

547

herbivore damage were striking for three taxa (Limonium , Salicornia /Sarcocornia /Arthrocnemum and Suaeda ), all of which had markedly higher levels of herbivore damage at low- versus high-latitude sites. Results for Atriplex were less clear: A. hastata tended to have higher levels of herbivory at low-latitude sites (although this pattern was not statistically significant because A. hastata was found at only 3 of our lowlatitude sites), but the most common low-latitude species of Atriplex , A. portulacoides , had less herbivore damage than high-latitude A. hastata . Little herbivore damage was observed on Juncus and Spartina species on the dates we surveyed the sites. Because we sampled herbivore damage on only one date at each site, it is possible that patterns might have varied seasonally. Nevertheless, the most common result was that herbivore damage was greater at low latitudes, as we have also found on the Atlantic Coast of the US (Pennings and Silliman 2005, Pennings, unpubl.). We did not address the reasons leading to higher herbivore pressure at low versus high latitudes in this study, but biologists have long speculated that higher arthropod populations are facilitated by milder climates at low latitudes (Dobzhansky 1950). High levels of herbivore damage might select for increased plant defenses, and thus be one selective factor leading to reduced plant palatability at low latitudes. It is likely that other factors are also important, and these may interact with herbivore pressure in complicated ways to affect plant palatability. As one example, the longer growing season at low latitudes might require tougher leaves (in order to extend leaf life-span), and increased leaf toughness might reduce palatability to herbivores. These alternative hypotheses deserve attention, because they bear on whether the latitudinal gradient in herbivory and plant defenses is a reciprocal coevolutionary process or simply a consequence of parallel evolutionary responses by plants and herbivores to climate or other external drivers. One potential caveat regarding our results is that, because the marsh plant flora differed between northern and southern Europe, we were not able to make many intraspecific comparisons. The only well-replicated intraspecific comparison that we were able to make was between high- and low-latitude individuals of Suaeda maritima, and this comparison showed a strong latitudinal pattern in palatability and herbivore damage. We also compared high- and low-latitude populations of Atriplex hastata , but this comparison was hampered by low replication at low latitudes, where A. hastata was rare. All other comparisons involved congenerics (five taxa) or closely related genera (Salicornia vs Sarcocornia and Arthrocnemum ). By comparing closely-related species, we minimized possible effects of phylogenetic constraints on our results. Nevertheless, it is possible that some of the variability in our results, compared to

548

results from the Atlantic Coast of the US (Pennings et al. 2001, Siska et al. 2002), was due to fundamental differences among species that were unrelated to herbivory. These results are probably not unique to salt marsh habitats. Studies in forests have found more herbivore damage and higher expression of plant defensive compounds at low versus high latitudes (Coley and Aide 1991, Coley and Barone 1996), and studies of seaweeds have found that low-latitude plants are less palatable to herbivores than high-latitude plants (Bolser and Hay 1996). Geographic differences in plant and seaweed defenses appear to select for geographic differences in herbivore ‘‘offense’’ (Cronin et al. 1997, Toju and Sota 2006) and feeding behavior (Sotka and Hay 2002, Sotka et al. 2003). Although contrary patterns may exist at very high latitudes (Bryant et al. 1994), studies in temperate and tropical latitudes appear to support the speculation of early naturalists (Dobzhansky 1950) that biological interactions are more intense at low latitudes, creating geographic differences in selection patterns on both plants and herbivores that must be understood as part of any general ecological or evolutionary theory (Thompson 1994, 2005). In summary, our results support the hypothesis that plant herbivore interactions are more intense at low versus high latitudes in European salt marshes: herbivore damage is more extensive at low versus high latitudes, and (perhaps in response) low-latitude plants are less palatable than high-latitude plants. Despite a less-extensive data set and a less-powerful methodology (i.e. freeze-dried plant material), our results were consistent with the latitudinal patterns found in US salt marshes. In addition, our results indicated that geographic differences in the palatability of leaves are likely to be paralleled by differences in the palatability of leaf litter. As a result, factors that create geographic patterns in leaf palatability may not only affect plant-herbivore interactions, but also litter  detritivore interactions and ecosystem processes such as nutrient cycling.

Acknowledgements  We thank the Deutscher Akademischer Austauschdienst (A/01/49084), Fundac¸a˜o para a Cieˆncia e Tecnologia (grant PRAXIS XXI/BD/11039/97), the US National Science Foundation (DEB-0296160, OCE9982133), the National Geographic Society, and the International Center of the Christian-Albrechts-Universita¨t for funding and other support. We thank Carl Carstensen, Bjo¨rn Demmin and Ru¨diger Schuhmann for allowing access to sites in Germany. We thank Jan Bakker and Dries Kuijper for facilitating access to sites in the Netherlands. We thank Tonio Lorenzen, Ute Kossack and Joan Marie Svedberg for assistance with laboratory and field work. We thank the editor Lonnie Aarssen for constructive comments on the manuscript. We

dedicate this paper to the memory of M. Sprung, who died in an accident on June 18, 2003.

References Abele, L. G. 1992. A review of the grapsid crab genus Sesarma (Crustacea: Decapoda: Grapsidae) in America, with the description of a new genus.  Smithsonian Contrib. Zool. No. 527. Bolser, R. C. and Hay, M. E. 1996. Are tropical plants better defended? Palatability and defenses of temperate vs tropical seaweeds.  Ecology 77: 2269 2286. Bryant, J. P. et al. 1994. Biogeography of woody plant chemical defense against snowshoe hare browsing: comparison of Alaska and eastern North America.  Oikos 70: 385 395. Buck, T. L. et al. 2003. Diet choice in an omnivorous saltmarsh crab: different food types, body size, and habitat complexity.  J. Exp. Mar. Biol. Ecol. 292: 103 116. Callaway, R. M. et al. 2002. Positive interactions among alpine plants increase with stress.  Nature 417: 844  848. Coley, P. D. and Aide, T. M. 1991. Comparison of herbivory and plant defenses in temperate and tropical broad-leaved forests.  In: Price, P. W. et al. (eds), Plant-animal interactions: evolutionary ecology in tropical and temperate regions. John Wiley & Sons, Inc, pp. 25 49. Coley, P. D. and Barone, J. A. 1996. Herbivory and plant defenses in tropical forests.  Annu. Rev. Ecol. Syst. 27: 305 335. Cornelissen, J. H. C. et al. 2004. Leaf digestibility and litter decomposability are related in a wide range of subarctic plant species and types.  Funct. Ecol. 18: 779 786. Cronin, G. et al. 1997. Are tropical herbivores more resistant than temperate herbivores to seaweed chemical defenses? Diterpenoid metabolites from Dictyota acutiloba as feeding deterrents for tropical versus temperate fishes and urchins.  J. Chem. Ecol. 23: 289 302. Dobzhansky, T. 1950. Evolution in the tropics., Am. Sci.: 209 221. Dunson, W. A. and Travis, J. 1991. The role of abiotic factors in community organization.  Am. Nat. 138: 1067  1091. Gaines, S. D. and Lubchenco, J. 1982. A unified approach to marine plant-herbivore interactions. II. Biogeography.  Annu. Rev. Ecol. Syst. 13: 111 138. Grime, J. P. et al. 1996. Evidence of a causal connection between anti-herbivore defence and the decomposition rate of leaves.  Oikos 77: 489 494.

MacArthur, R. H. 1972. Geographical ecology: patterns in the distribution of species.  Harper and Row. Menge, B. A. 2003. The overriding importance of environmental context in determining the outcome of speciesdeletion experiments.  In: Kareiva, P. and Levin, S. A. (eds), The importance of species: perspectives on expendability and triage. Princeton Univ. Press, pp. 16 43. Pennings, S. C. et al. 1998. Feeding preferences of a generalist salt-marsh crab: relative importance of multiple plant traits.  Ecology 79: 1968 1979. Pennings, S. C. and Silliman, B. R. 2005. Linking biogeography and community ecology: latitudinal variation in plant-herbivore interaction strength.  Ecology 86: 2310 2319. Pennings, S. C. et al. 2001. Latitudinal differences in plant palatability in Atlantic Coast salt marshes.  Ecology 82: 1344 1359. Peterson, C. H. and Renaud, P. E. 1989. Analysis of feeding preference experiments.  Oecologia 80: 82 86. Pfauder, A. and Zimmer, M. 2005. Intermediate tidal stress promotes the detritivore-mediated decomposition of Spartina litter.  Eur. J. Soil Biol. 41: 135 141. Salgado, C. S. and Pennings, S. C. 2005. Latitudinal variation in palatability of salt-marsh plants: are differences constitutive?  Ecology 86: 1571 1579. Siska, E. L. et al. 2002. Latitudinal variation in palatability of salt-marsh plants: which traits are responsible?  Ecology 83: 3369 3381. Sotka, E. E. and Hay, M. E. 2002. Geographic variation among herbivore populations in tolerance for a chemically rich seaweed.  Ecology 83: 2721 2735. Sotka, E. E. et al. 2003. Geographic and genetic variation in feeding preference for chemically defended seaweeds.  Evolution 57: 2262 2276. Stachowicz, J. J. and Hay, M. E. 2000. Geographic variation in camouflage specialization by a decorator crab.  Am. Nat. 156: 59 71. Thompson, J. N. 1988. Variation in interspecific interactions.  Annu. Rev. Ecol. Syst. 19: 65 87. Thompson, J. N. 1994. The coevolutionary process.  The Univ. of Chicago Press. Thompson, J. N. 2005. The geographic mosaic of coevolution.  The Univ. of Chicago Press. Toju, H. and Sota, T. 2006. Imbalance of predator and prey armament: geographic clines in phenotypic interface and natural selection.  Am. Nat. 167: 105 117. Travis, J. 1996. The significance of geographical variation in species interactions.  Am. Nat. 148: S1 S8. Vermeij, G. J. 1978. Biogeography and adaptation.  Harvard Univ. Press.

Appendices can be found at www.oikos.ekol.lu.se as Appendix O15591

549

Latitudinal variation in plantБherbivore interactions in ...

Present address: School of Environmental Sciences,. Univ. of East Anglia, ... limitations in design (reviewed by Pennings et al. 2001). One of the most ..... the distribution of species. Б Harper and Row. Menge, B. A. 2003. The overriding importance of environ- mental context in determining the outcome of species- deletion ...

95KB Sizes 1 Downloads 70 Views

Recommend Documents

Latitudinal variation in herbivore pressure in ... - Semantic Scholar
Jan 1, 2009 - three methods to test the hypotheses that (1) herbivores are more abundant .... or measurement was replicated six to eight times per site, and averaged ... combined with other data in a previous study (Pennings and Silliman ...

Small-scale spatial variation in the interactions between ...
dispersal services (Snow 1971; McKey 1975; Howe and Estabrook 1977). However, the ..... Chavez-Ramirez F. and Slack R.D. 1994. Effects of avian foraging.

The Andean Thrust System-Latitudinal Variations in ...
Farther north at 208S, broadband seismologic studies indicate a 70- to 74-km-thick ... higher topography of the Puna in comparison with the. Bolivian Altiplano ...

Latitudinal decrease in folivory within Nothofagus ...
60 m per degree of latitude, to reach 0–600 m ... foliage 1 year earlier during March 2006 in a subset of 17 sites at the northern part of N. ... Figure 1 Spatial pattern of variation in leaf damage frequency. (summed ..... Report, Fac. Cs. Agraria

Variation in dung beetle (Coleoptera: Scarabaeoidea) - CiteSeerX
Dec 13, 2016 - in the Bulgarian Rhodopes Mountains: A comparison. JORGE M. LOBO1 ... mators ACE (abundance-based coverage estimator) and Chao1.

Mate guarding, competition and variation in size in ...
97 Lisburn Road, Belfast BT9 7BL, Northern Ireland, U.K. (email: [email protected]). ..... Princeton, New Jersey: Princeton University Press. Arak, A. 1988.

Variation in chemical defenses against herbivory in ...
logical specialization to successfully prevent herbivory. Keywords: chemical ... haploid and diploid) individuals, most studies have been limited to .... data from Mori and Koga (1992). Description of ..... N.Z. Natural Sciences, Christ- church, New 

Mate guarding, competition and variation in size in ...
depletion of energy stores during the mate-searching period, when males feed ..... Rubenstein (1987) proposed size-dependent alternative mating behaviour in ...

Variation in chemical defenses against herbivory in ...
ulations of the same species growing in different habitats ... observed in other green seaweeds such as Caulerpa, .... It is characterized by high wave energy,.

Reconciliation and variation in post-conflict stress in ...
Nov 1, 2001 - have two functions: (1) to repair relationship damaged by aggression such that .... (SDB), such as scratching, auto-grooming, and yawning, is associated with .... begun within 15 min (either side) of the start time of the PC. MCs ... Wh

Drug interactions in cancer therapy
Pharmacia & Upjohn Company. Emcyt prescribing information. Pfizer [online] .... Crewe, H. K., Ellis, S. W., Lennard, M. S. & Tucker, G. T.. Variable contribution of ...

Fine-grained variation in caregivers' /s - ENS
An alternative hypothesis postulates instead that infants start out with certain auditory- .... acoustic characteristic of /s/ is that the peak of energy during the ...

Mate guarding, competition and variation in size in ...
97 Lisburn Road, Belfast BT9 7BL, Northern Ireland, U.K. (email: ... viously successful males that can copulate again within. 2 h (Bridge 1999), ..... Newsletter of.

Adaptive variation in judgment and philosophical intuitionq
Feb 12, 2009 - article (e.g. in Word or Tex form) to their personal website or .... external (e.g., social and physical) environments regardless of logical ...

Collective frequency variation in network ...
Apr 25, 2016 - systems and show that for generic directed networks the collective frequency of the ensemble is not the same as the mean of the individuals' ...

Fine-grained variation in caregivers' /s - ENS
Based on online coding, habituation was determined at the end of a trial if the average looking time for that trial and the two preceding ones dropped below 40% ...

Latitudinal Gradients in Species Diversity: A Review of ...
Despite the handicap of insufficient ecological data, or perhaps because ... these hypotheses separately, attempting to suggest possible tests and ob- servations .... 1965) has argued that predation enhances migration and speciation, thereby.

Latitudinal Gradients in Species Diversity: A Review of ...
there has as yet been little discussion of the application of statistical pro- cedures to this ..... An interesting variation on this theme is that of increased "niche over-.

Latitudinal gradients in species richness for South ...
2006; Prado and Castilla 2006; Borth- agaray and Carranza 2007). As such, they can have strong ecosystem-level impacts, including direct effects on the diversity patterns of associated species along large spatial scales. Besides their ecological or s

Fuentes Characterizing human-macaque interactions in Singapore.pdf
Fuentes Characterizing human-macaque interactions in Singapore.pdf. Fuentes Characterizing human-macaque interactions in Singapore.pdf. Open. Extract.

Drug interactions in cancer therapy
Improvements in in vitro methods and early clinical testing have made the prediction of potentially clinically ... as part of their cancer treatment or for the management of .... limited data that pertains to the interactions between grapefruit juice

Reconciliation and variation in post-conflict stress in ... - baillement.com
Nov 1, 2001 - have two functions: (1) to repair relationship damaged by aggression such .... (SDB), such as scratching, auto-grooming, and yawning, is associated with ..... culated individuals' mean rates of each class of SDB (in bouts per.

Investigating Variation in Replicability.pdf
There was a problem previewing this document. Retrying... Download. Connect more apps... Try one of the apps below to open or edit this item. Investigating ...

mitochondrial DNA variation in rotifer resting egg b
Apr 27, 2000 - Science Series, IOS Press. Hebert, P. D. N. & Wilson, C. C. 1994 Provincialism in plankton: endemism and allopatric speciation in Australian.