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Gopher–Plant–Fungal Interactions Affect Ecology, 84(1), 2003, pp. 120±128 q 2003 by the Ecological Society of America GOPHER±PLANT±FUNGAL INTERACTIONS AFFECT ESTABLISHMENT OF AN INVASIVE GRASS VALERIE T. E VINER1,3 AND F. S TUART CHAPIN, III2 1Department of Integrative Biology, University of California, Berkeley, California 94720 USA 2Institute of Arctic Biology, University of Alaska, Fairbanks, Alaska 99775 USA Abstract. Many attempts have been made to link invasions of exotic plants to speci®c plant traits and key attributes of invaded ecosystems. While these factors play a role in determining the potential for invasion, they are often inadequate in predicting the success of a speci®c invasion. We show that interactions of an invasive grass with other members of the community determine the local pattern of invasion. A fungus, Ulocladium atrum, aids the establishment of barbed goatgrass (Aegilops triuncialis) by weakening the grass's tough seed head, thereby accelerating germination and seedling establishment. In contrast, gophers, Thomomys bottae, decrease establishment of this invader by selectively burying patches of goatgrass seedlings under mounds. Plants that survive these gopher disturbances produce seeds that are uninfected by Ulocladium atrum, which may further decrease the establishment of the next generation of goatgrass. A ®eld survey indicated that goatgrass achieves dominance in areas with minimal gopher disturbance, but has limited establishment in pastures with high gopher activity, indicating that the landscape pattern of gopher activity in¯uences patterns of goatgrass invasion by manipulating gopher±plant±fungal interactions. Key words: Aegilops triuncialis; California (USA) annual grasslands; disturbance; fungus; ger- mination; goatgrass; plant invasion; pocket gophers; species interactions, role in plant invasion; Thomomys bottae; Ulocladium atrum. INTRODUCTION members of the community. The success of some in- The invasion of exotic plant species can have major vasive species due to release from natural enemies is impacts on natural and managed systems, with large a clear example of the importance of biological inter- negative consequences for conservation of native spe- actions in invasions (Mack et al. 2000), but other types cies, diversity, and the economy (Mack 1996, Mooney of species interactions can be important as well. and Hobbs 2000). The globalization of trade and travel Aegilops triuncialis (barbed goatgrass) is an aggres- has dramatically increased the introduction of exotic sive exotic annual grass that is invading central and species, and consequently the invasion of these species northern California (USA) annual grasslands. This has become one of the most pressing global-change grass is capable of establishing in a variety of sites, issues (Lovel 1997, Mooney and Hobbs 2000). In order ranging from deep fertile soils to shallow rocky soils. to stem this in¯ux of invasive species, it is critical to It is even capable of invading serpentine soils (Cali- determine the mechanisms responsible for successful fornia Exotic Pest Plant Council 1999), which have invasions. Most research has focused on predicting in- largely resisted invasions by many exotic plants due to vasions based on plant traits that characterize success- their low nutrients, high Mg/Ca ratio, low water-hold- ful invaders (e.g., high growth rate, high allocation to ing capacity, and possible heavy metal toxicity (Huen- reproduction [Newsome and Noble 1986, Noble 1989, neke et al. 1990). Although goatgrass is capable of Hobbs and Humphries 1995, Rejmanek 1995]), and establishing in a wide variety of sites, its ability to characteristics of invaded ecosystems (e.g., disturbance dominate a site varies greatly, even among neighboring [Orians 1986, Hobbs and Huenneke 1992, Hobbs and ®elds (V. T. Eviner, personal observation). The mech- Humphries 1995] and diversity [Tilman 1997, Levine anisms responsible for determining patterns of invasion 2000]). Any of these factors can determine the potential of the same species across different sites in the same of a species to invade, but often cannot be used to ecosystem could be critical additions to the current predict if a species will actually invade (Mack et al. framework for predicting invasion success. Since pat- 2000). Here we argue that, when a species has the terns of goatgrass invasion vary locally, they are un- potential to invade a site, its successful establishment likely to be determined by coarse-scale environmental ultimately is determined by its interactions with other factors or dispersal limitation. However, there are dif- ferences in the local environment or distribution of Manuscript received 15 April 2002; accepted 25 May 2002. other organisms that might in¯uence the establishment Corresponding Editor: D. R. Strong. of goatgrass. In particular, there is considerable spatial 3 Present address: Institute of Ecosystem Studies, Box AB, Millbrook, New York 12545 USA. variability associated with the presence of a fungus, E-Mail: [email protected] Ulocladium atrum, which infects the seed head of this 120 January 2003 ROLE OF INTERACTIONS IN PLANT INVASIONS 121 invasive grass. Furthermore, the distribution of pocket number of advantages in the native habitat of goatgrass. gophers varies across the landscape due to variation in The seed head is responsible for dormancy of some soil depth (Howards and Childs 1959). We propose that goatgrass seeds (Peters et al. 1996), which can be crit- these other organisms might determine the local in- ical for the persistence of annual species (Foley 2002). vasion patterns of goatgrass. In addition, this tough seed head protects seeds from Goatgrass seeds normally germinate by breaking ®re (Hopkinson et al. 1999) and ingestion by animals through their intact seed head (Peters et al. 1996), (Lyon et al. 1992), both of which are prevalent in the which is thick and woody. This seed head substantially native habitat of goatgrass. delays germination, compared with germination of Ulocladium atrum (nomenclature according to IMI seeds removed from their spike (Peters 1994). The fun- [1995]) is a dematiaceous hyphomycetes that is found gus, Ulocladium atrum, is often associated with the in a wide variety of geographic areas, including Africa, seed head of goatgrass. Ulocladium fungi produce cel- North America, South America, Asia, the Middle East, lulolytic enzymes (Srivastav and Srivastav 1986) and Australia, and Europe (IMI 1995). It is a very common break down lignin (Almendros and Martinez 1987) and fungus throughout these regions, and can be found on may weaken the seed head and possibly quicken ger- the leaves (Abdel-Hafez 1985, Kohl et al. 1995), twigs mination of goatgrass. Alternatively, this fungus could (Agarwal et al. 1993), seeds (Hashmi 1988, Hashmi et act as a pathogen and decrease the establishment of al. 1990, Lilja et al. 1995) and roots (Taheri et al. 1994, goatgrass by decreasing seed size and survival. Hashem and Al-Farraj 1995) of a variety of plants, as Gophers are an important component of California well as in the soil (Eastburn and Butler 1988) and in grasslands. On average they disturb 26% of the soil airborne dust (Abdel-Hafez et al. 1993, IMI 1995). It surface annually (Hobbs and Mooney 1991). Soil dis- is likely that this fungus is associated with Aegilops turbance by gophers can have large effects on plant triuncialis in its native habitat since the geographic community composition (Hobbs and Mooney 1985, ranges of these species overlap, and Ulocladium atrum 1991, Huntly and Inouye 1988, Martinsen et al. 1990, is frequently found on many plants, including on the Huntly and Reichman 1994) and may increase invasion roots (Taheri et al. 1994) and straw (Almendros et al. by creating sites for establishment of exotic species 1987) of wheat, whose close relation to Aegilops allows (Hobbs and Mooney 1991, Kotanen 1997). Gophers can these species to hybridize (Crampton 1974). The dark also exert their effects on plant community composition fungal lesions of U. atrum that we observe on A. triun- by selectively disturbing patches of certain plant spe- cialis seed heads are common on Aegilops species in cies (Tilman 1983). Japan, and are often a key attribute in the classi®cation The purpose of this study was to investigate the roles of these grasses (H. Tsujimoto, personal communica- of U. atrum and gophers on the establishment of goat- tion). grass and to determine if these biotic interactions could Infection of A. triuncialis seed heads with U. atrum account for the spatial variability in the invasion suc- was evident in California grasslands, but there were no cess of this grass. visible signs of fungal presence associated with seeds of other grassland species. There are two distinct char- METHODS acteristics of A. triuncialis that may account for its Field site unique association with U. atrum in our system. A. This research took place in the California (USA) triuncialis has tough glumes that form a woody seed annual grassland at the University of California Hop- head, which is a likely substrate for U. atrum, a com- land Research and Extension Center in the northern petitive saprobe (Kohl et al. 1995) with cellulolytic coastal mountains of Mendocino County (160 km north capabilities (Almendros and Martinez 1987). This fun- of San Francisco, 398009 N latitude, 1238049 W lon- gus is known to establish on similar tough seed heads, gitude). including sun¯ower seeds (Shtienberg 1994). There was no visible evidence of U. atrum infection on the Study organisms other
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