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Indirect and Diffuse Interactions Among Salt Marsh Plants University of Montana ScholarWorks at University of Montana Biological Sciences Faculty Publications Biological Sciences 10-2000 Facilitation May Buffer Competitive Effects: Indirect and Diffuse Interactions Among Salt Marsh Plants Ragan M. Callaway University of Montana - Missoula, [email protected] Steven C. Pennings Follow this and additional works at: https://scholarworks.umt.edu/biosci_pubs Part of the Biology Commons Let us know how access to this document benefits ou.y Recommended Citation Callaway, Ragan M. and Pennings, Steven C., "Facilitation May Buffer Competitive Effects: Indirect and Diffuse Interactions Among Salt Marsh Plants" (2000). Biological Sciences Faculty Publications. 209. https://scholarworks.umt.edu/biosci_pubs/209 This Article is brought to you for free and open access by the Biological Sciences at ScholarWorks at University of Montana. It has been accepted for inclusion in Biological Sciences Faculty Publications by an authorized administrator of ScholarWorks at University of Montana. For more information, please contact [email protected]. vol. 156, no. 4 the american naturalist october 2000 Facilitation May Buffer Competitive Effects: Indirect and Diffuse Interactions among Salt Marsh Plants Ragan M. Callaway1,* and Steven C. Pennings2 1. Division of Biological Sciences, University of Montana, species interact within communities. Within a trophic Missoula, Montana 59812; level, additional species can alter pairwise interactions via 2. University of Georgia Marine Institute, Sapelo Island, Georgia direct and indirect pathways (Lawlor 1979; Stone and Rob- 31327 erts 1991; Miller 1994; Wooton 1994) and through the Submitted October 15, 1999; Accepted May 30, 2000 cumulative, ªdiffuseº effects of many direct effects acting on a single species (Davidson 1980; Wilson and Keddy 1986a, 1986b; Vandermeer 1990). For example, Levine (1976) demonstrated that the addition of a third com- petitor to a model of two competing species could change abstract: Direct interactions among plant species may be highly modi®ed by indirect or diffuse effects within a multispecies com- the cumulative effect of a species from competitive to fa- munity. We investigated the direct and diffuse effects of two salt cilitative because of the suppression of a shared competitor. marsh perennials, Monanthechloe littoralis and Arthrocnemum sub- Similarly, models of interactions among invading exotic terminale, on winter annuals and the perennial herb Limonium cal- and native species have suggested that natives may be com- ifornicum in a salt marsh in central California. In permanent plots, pletely displaced in pairwise interactions but can coexist Monanthechloe had expanded substantially in the upper marsh over with exotics in diverse communities, apparently because the past 13 yr, while Arthrocnemum and all annual species had de- creased. These dynamics suggest that Monanthechloe may directly of the greater number of indirect interactions (Case 1991). outcompete most other species in the upper marsh. In contrast, Despite the potential importance of indirect interactions Arthrocnemum is known to facilitate some annual species. In our in plant communities, only a few experiments have at- ®eld experiments, Monanthechloe strongly suppressed Arthrocnemum, tempted to demonstrate the existence of interactions in all four common annual species, and Limonium in direct interactions. which ªa competitor's enemy is a friendº (Wilson and In contrast, Arthrocnemum directly facilitated the winter annuals Keddy 1986a; Miller 1994; Levine 1999). Parapholis incurva and Lasthenia glabrata, competed with Spergularia marina, and did not have a signi®cant effect on Limonium. However, Direct interactions among plants can also be facilitative when the combined effects of Monanthechloe and Arthrocnemum (Callaway 1995), and although positive interactions have were tested, Arthrocnemum ameliorated the negative effect of Mon- been demonstrated in many experiments, little is known anthechloe on all four species. Although isolated Arthrocnemum com- about indirect interactions involving species with facili- peted with Spergularia and had no direct effects on Limonium, Ar- tative effects. In the upper zones of coastal salt marshes throcnemum in the presence of Monanthechloe facilitated both species. in southern California, the two dominant perennial spe- We hypothesize that Arthrocnemum buffered the strong competitive cies appear to have strikingly opposite effects on most effects of Monanthechloe on Lasthenia and Parapholis via direct pos- itive effects and bene®ted Spergularia and Limonium through its co-occurring winter annual species. Arthrocnemum sub- competitive effect on Monanthechloe. These ®ndings add to the grow- terminale, a succulent subshrub, has been shown to fa- ing body of literature emphasizing the importance of diversity and cilitate two annual species, Parapholis incurva and Las- interdependence in the functioning of plant communities. thenia glabrata (Callaway 1994); whereas Monanthecloe Keywords: competition, diffuse interactions, facilitation, indirect in- littoralis, a clonal grass, appears to eliminate virtually all teractions, positive interactions, salt marsh. annuals by establishing a thick vegetative mat (R. M. Callaway and S. C. Pennings, personal observation). Fur- thermore, long-term monitoring (see ªResultsº) at our Pairwise, direct interactions often fail to predict the way study site indicates that Monanthechloe is increasing in abundance and displacing Arthrocnemum and winter an- * E-mail: [email protected]. nual species. Together, these patterns suggest the poten- Am. Nat. 2000. Vol. 156, pp. 416±424. q 2000 by The University of Chicago. tial for unusual indirect interactions. We hypothesized 0003-0147/2000/15604-0007$03.00. All rights reserved. that Monanthechloe might directly outcompete annual Indirect Interactions in Salt Marshes 417 position on the elevation gradient varies substantially among years, at least partly due to variation in precipitation (Cal- laway and Sabraw 1994). Methods To document the natural dynamics of species in the upper marsh, we quanti®ed the absolute cover of Arthrocnemum, Monanthechloe, and winter annuals in 59 permanent plots in 1986 and 1999. We also correlated the change of Mon- anthechloe absolute cover with the change of Arthrocne- mum cover and the percentage change of cover of all an- nual species combined in each plot. For simplicity, and Figure 1: Percentage cover of Monanthechloe littoralis, Arthrocnemum because of the year-to-year variation in the relative abun- subterminale, and winter annual species in permanent plots in Carpinteria dances of different annual species among years and with Salt Marsh, California, in 1986 and 1999. Bars represent 1 SE. species but that the positive effect of Arthrocnemum might buffer annual species from the full negative effect of Monanthechloe. We tested these hypotheses in four ways: ®rst, by correlating changes in the relative abun- dance of Monanthechloe with the abundance of other species over the past 13 yr, second, by measuring patterns of abundance of annual species associated with Arthroc- nemum in the presence and in the absence of Monan- thechloe, third, by conducting ®eld experiments in which we measured the direct effects of the perennials on each other and on annual species and a perennial herb, and ®nally, by conducting ®eld experiments in which we mea- sured the effects of Monanthechloe on other species in the presence and in the absence of Arthrocnemum. Study Site We conducted our study in the upper ªtransition zoneº at the Carpinteria Salt Marsh Reserve (347249N, 1197319W), approximately 15 km south of Santa Barbara, California. This site was described extensively in Ferren (1985), Cal- laway et al. (1990), and Pennings and Callaway (1992, 1996), and direct interactions among species in the transition zone have been examined in Callaway (1994). The dominant perennial species in the transition zone, approximately 0.4±0.6-m elevation above mean high high water, are the small shrub Arthrocnemum subterminale (Parish) Standl. and the highly rhizomatous, mat-forming Monanthlechloe littoralis. Winter annual species are distributed along an elevation-and-salinity gradient and include Spergularia ma- Figure 2: Regression relationship between the change in percentage cover of Monanthechloe littoralis and the change in percentage cover of Ar- rina, Parapholis incurva, Hutchinsia procumbens, Lasthenia throcnemum littoralis and annual species in Carpinteria Salt Marsh, Cal- glabrata, and Juncus bufonius (nomenclature follows Ferren ifornia. For Arthrocnemum,(y p 3.80 1 xr20.32),2 p 0.39 ,P ! .01 ; for 1985). The relative abundance of these species and their annuals,y p 22.53 1 xr (20.61),2 p 0.49 ,P ! .01 . 418 The American Naturalist the entire 400-cm2 plot because densities were much lower. Effects were tested using a one-way ANOVA (SPSS 1997) for each of the four most abundant annual species, Juncus, Parapholis, Lasthenia, and Spergularia, and the perennial herb Limonium in each removal treatment. Data for other annual species were not analyzed because they were present in only a small fraction of the plots. To examine the interactive effects of Monanthechloe and Arthrocnemum on annual species and Limonium,we established a second experiment in May 1997. Before manipulation, each 100-cm2 plot contained a single Ar- throcnemum individual and 100% cover of Monanthech- loe forming a 2±4-cm deep mat. We established the four following
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