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Effects of invasive forb litter on seed germination, seedling growth and survival
Basic Appl. Ecol. 3, 309–317 (2002) © Urban & Fischer Verlag http://www.urbanfischer.de/journals/baecol
Basic and Applied Ecology
Effects of invasive forb litter on seed germination, seedling growth and survival Bret E. Olson*, Roseann T. Wallander Department of Animal and Range Sciences, Montana State University-Bozeman, Bozeman, U.S.A.
Received May 28, 2001 · Accepted March 18, 2002
Abstract Two Eurasian forbs, Euphorbia esula L. and Centaurea maculosa Lam., continue to spread in the northwestern United States despite extensive and expensive control efforts. We investigated whether litter from these forbs and associated soils suppress germination and growth of two native perennial grasses (Pseudoroegneria spicata [Scribn. & Smith A. Love], Pascopyrum smithii [Rydb.] A. Love), which may partly explain the success of these invasive forbs. Seed germination was unaffected, but roots were shorter at higher leachate concentrations. The physical presence of litter (Euphorbia, Centaurea, none) did not affect seed germination or number of leaves of seedlings of the four species, but it affected seedling heights; the tallest seedlings were those covered with Centaurea litter; the shortest were those without litter. As a mechanical barrier, litter type did not affect survival or number of leaves of pregerminated seeds, but litter inhibited shoot growth. Seed germination of the four species on soils from infested or noninfested areas differed; Euphorbia germination, albeit low (< 4%) was higher on soils collected from Euphorbia- infested areas, whereas germination of the other species was higher on soils from noninfested areas. These results indicate that litter from these invasive forbs can have subtle effects on growth of seedlings of these native grasses, especially the native Pseudoroegneria, and that these forbs have some unknown effect on soil properties which reduce germination. Die Ausbreitung zweier Unkräuter eurasiatischer Herkunft (Euphorbia esula L. und Centaurea maculosa Lam.) in den nordwestlichen USA konnte trotz umfangreicher Gegenmaßnahmen bisher nicht aufgehalten werden. Wir untersuchten, ob diese Kräuter durch Streuproduktion oder andere Bodenveränderungen eine negative Wirkung auf Keimfähigkeit und Wachstum zweier heimischer mehrjähriger Gräser (Pseudoroegneria spicata [Scribn. & Smith A. Love], Pascopyrum smithii [Rydb.] A. Love) ausüben, was zum Teil den Erfolg dieser Unkräuter erklären könnte. Saataufgang war nicht beeinträchtigt, aber Wurzeln waren kürzer und wiesen höhere Exsudatkonzentrationen auf. Die pure Anwesenheit von Euphorbia- oder Centaurea streu hatte keinen Effekt auf Auflauf oder Blattanzahl der Sämlinge aller vier Arten, sowohl auf Böden aus verunkrauteten Arealen als auch auf vorher unkrautfreien Böden. Streu beeinflusste aber die Sämlingshöhe: die höchsten Sämlinge traten in Verbindung mit Centaurea Streu auf, die niedrigsten unter streulosen Bedingungen. Die Streuart hatten keinen Einfluss auf Überlebensfähigkeit oder Blattzahl vorgekeimter Samen, jedoch beeinträchtigte das Vorhandensein von Streu die Sprosslänge. Die Keimfähigkeit der vier Arten hing davon ab, ob die Böden aus verunkrauteten oder unkrautfreien Gebieten stammten. Die Euphorbia-Keimrate, obwohl generell niedrig (< 4 %), war höher auf Böden aus Euphorbia-befallenen Gebieten, die Keimfähigkeit der anderen Arten war höher auf Böden aus unkrautfreien Arealen. Un-
*Corresponding author: Bret E. Olson, Department of Animal and Range Sciences, Montana State University-Bozeman, Bozeman, MT 59717, USA, Phone: +1-406-994-5571, Fax +1-406-994-5589, E-mail: [email protected]
1439-1791/02/03/04-309 $ 15.00/0
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Olson and Wallander sere Resultate zeigen, dass Streu dieser eingeschleppten Kräuter leichte Effekte auf das Keimlingswachstum der beiden heimischen Gräser ausübt, insbesondere auf die heimische Pseudoroegneria und dass diese Käuter die Bodeneigenschaften in bisher unbekannter Weise beeinflussen, welche die Keimungsrate beeinträchtigen. Key words: allelopathy – Centaurea maculosa – Euphorbia esula – invasive species – leachate – shoot extension – soils
Introduction Certain Eurasian forbs, such as Euphorbia esula L. and Centaurea maculosa Lam., are spreading rapidly on mixed grass prairies of western North America. When we attempt to eradicate these forbs to restore native plant communities, we assume these communities will then proceed toward the potential natural plant community based on Clements’ (1916) model of plant succession. However, the Clementsian model may not be appropriate if these forbs permanently alter site conditions. Alternatively, a multiple steady state, state and transition model may best represent steady states dominated by invasive forbs (Westoby et al. 1989, Laycock 1991, Pimm 1993, Rietkerk & van de Koppel 1997). These new steady states may be maintained by mechanisms, e.g. interference, allelopathy, etc. (Inderjit & del Moral 1997, Ridenour & Callaway 2001) that hinder the establishment of native grasses by reducing seed germination or seedling growth. In some cases, steady states dominated by invasive forbs may reflect that their presence and the relative absence of native species on a local scale are determined by species presence/absence on a larger scale (Zobel 1997). However, as a potential source of propagules, native species seldom become extinct at such larger scales, which would be needed to explain their depauperate status at local scales, because they are usually present in seedbanks or isolated refugia. Different properties of plant litter can have a major influence on native plant establishment (Facelli & Pickett 1991, Bosy & Reader 1995). Litter from certain plants can reduce seed germination and seedling growth by leaching inhibitory compounds, altering microclimate, and preventing shoot extension (Schlatterer & Tisdale 1969, Bosy & Reader 1995). Many invasive forbs contain secondary compounds which can be leached from litter, released with decomposition, or exuded from roots (Kelsey & Everett 1995). For example, Euphorbia esula contains di- and tri-terpenoids, and condensed tannins (Evans & Kinghorn 1977, Roberts & Olson 1999). Centaurea maculosa contains high concentrations of cnicin, a
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sesquiterpene lactone (Kelsey & Locken 1987, Olson & Kelsey 1997). In laboratory bioassays, cnicin is phytotoxic toward native grasses and conifers; root growth is inhibited more than germination (Kelsey & Locken 1987). On agar gel, root and shoot growth of lettuce (Lactuca sativa L.) was reduced by certain terpenoids, whereas only root growth was reduced on natural soils (Inderjit et al. 1997); they recommended that natural soils should be used for growth bioassays. Litter from invasive forbs may accumulate rapidly because of structural and/or the aforementioned chemical deterrents to detritivores and decomposers. Euphorbia and Centaurea litter can accumulate up to 10– and 5 cm thick, respectively, on mixed grass prairies (Olson & Wallander, unpublished data). This added physical structure may alter irradiance, relative humidity, soil and air temperatures, and wind velocity close to the soil surface (Bosy & Reader 1995). Depending on litter thickness, an altered microenvironment often affects seed germination, and benefits or hinders early growth of seedlings (Facelli & Pickett 1991, Foster 1999, Molofsky et al. 2000). For example, seeds that germinate earlier under such conditions will accumulate greater biomass, and have a greater probability of establishing during this crucial, life history stage (Weigelt et al. 2002). Besides altering the microenvironment, litter may present a mechanical barrier for shoot extension of recently germinated seeds (Kucera & Dahlman 1967, Mufti et al. 1977, Bosy & Reader 1995). This would reduce a seedling’s ability to capture sunlight, photosynthesize, and grow. Assessing litter’s physical effect on seed germination and its mechanical effect on shoot extension and survival of seedlings covers two critical life-history stages (Nash Suding & Goldberg 1999). Our objective was to determine whether chemical, physical, or mechanical properties of litter, or soils influenced by the invasive forbs Euphorbia and Centaurea affect seedling emergence, growth, and survival of two native grasses (Pseudoroegneria spicata [Scribn. & Smith A. Love], Pascopyrum smithii [Rydb.] A. Love), and of themselves (autotoxicity).
Effects of invasive forb litter on seedlings
Materials and methods Plant materials Leafy spurge (Euphorbia esula L.) is a perennial forb from Eurasia. It has a deep (5–9 m) and extensive lateral root system (Bakke 1936, Best et al. 1980). It currently infests over 1.25 million hectares in the northern Great Plains in the United States and Canada (Lajeunesse et al. 1997). Spotted knapweed (Centaurea maculosa Lam.), a perennial tap-rooted forb from Eurasia, infests over 2.8 million hectares in the northwestern United States (Lacey 1989). These invasive forbs have the potential to spread onto many sites in Montana (Chicoine et al. 1985, Lajeunesse et al. 1997). Bluebunch wheatgrass (Pseudoroegneria spicata [Scribn. & Smith A. Love]) is a native, perennial tussock grass. Common co-dominants are Idaho fescue (Festuca idahoensis Elmer) and blue grama (Bouteloua gracilis [H.B.K.] Lag.). Western wheatgrass (Pascopyrum smithii [Rydb.] A. Love) is a native, perennial rhizomatous grass. Common co-dominants are needleand-thread (Stipa comata Trin. & Rupr.) and green needlegrass (Stipa viridula Trin.). Historically, these grass species dominated many mixed grass prairies in northwestern United States. Euphorbia and Centaurea co-occur with both grass species, but usually on different sites, mainly because Pseudoroegneria and Pascopyrum seldom co-occur. Pseudoroegneria grows primarily on well-drained, upland soils whereas Pascopyrum grows on swales and bottomlands. All four species have the C3 photosynthetic pathway (B. Olson, unpublished data). Litter was collected from a Centaurea-infested (> 50% Centaurea based on foliar cover) site 50 km west of Bozeman, Montana U.S.A. on 13 September 1996. Soil samples from infested and adjacent noninfested areas (< 5% Centaurea) were collected with a 10-cm diameter core. Soil was a deep, well-drained loamy sand in the taxonomic class, mixed rigid Ustic Torripsamment. Litter was collected from our Euphorbia-infested (> 50% Euphorbia based on foliar cover) site 5 km northeast of Bozeman, Montana U.S.A. on 30 September 1996. Soil samples from infested and adjacent noninfested areas (< 5% Euphorbia) were collected with the same core. Soil was a well-drained cobbly loam in the taxonomic class, clayey-skeletal, mixed superactive Udic Argiborolls. Overall, the invasive forbs and grasses grew in distinct, interspersed patches, presumably reflecting clumping associated with dispersal or micro-disturbances. The litter represented that year’s senescent stems, leaves, and flowerheads only; most of the material was standing.
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Seeds from these invasive forbs were collected from heavily infested areas where soils and litter were collected. Seed of Pseudoroegneria (Goldar variety) and Pascopyrum (Rosana variety) was provided by the Bridger Plant Materials Center, USDA-ARS, Bridger, Montana, U.S.A. Chemical effect of litter on seedling emergence and roots To determine the chemical effect of Euphorbia and Centaurea litter on germination and root development, we created a leachate by soaking Euphorbia (8.2 g leaves, 24.8 g stems) and Centaurea (2.4 g leaves, 13.6 g stems) litter in 600 ml and 300 ml, respectively, of deionized, distilled water for 72 h, and then we filtered the solution. Leachate was diluted with distilled water to create 0X (distilled water), 0.25X, 0.5X, and 1.0X concentrations. Twenty-five seeds of either Pseudoroegneria, Pascopyrum, Euphorbia or Centaurea were placed on filter paper in petri plates. Twelve ml of each leachate solution combination (two source species, four concentrations) were added to the filter paper. Petri plates were sealed with parafilm to reduce evaporation. They were placed in a cold (4 °C) dark room for 7 d, and then placed in seed germinators (Hoffman Manufacturing, Albany, Oregon, U.S.A.) at an alternating cycle of 25 °C and 15 °C for 12 h every 24 h for 7 d. There were five blocks for each leachate source (Euphorbia, Centaurea), leachate concentration (0X, 0.25X, 0.5X, 1.0X), seeded species (Pseudoroegneria, Pascopyrum, Euphorbia or Centaurea) combination. Plates were removed from the germinators after 14 d. Germination (%) was determined and root length was measured. Physical effect of litter on seed germination and seedling growth We determined the physical effect of Euphorbia and Centaurea litter on seed germination and early seedling growth by sowing seeds into sand-filled trays covered with litter packs. The litter packs (galvanized steel mesh netting; 0.6 cm; after Bosy & Reader 1995) were elevated 2–3 cm above the sand surface in a series of 13 cm × 18 cm plastic trays. The amount of litter placed in litter packs mimicked the amount found on a heavily infested site of each species (Euphorbia 500 g m–2; Centaurea 225 g m–2, unpublished data). For the control (NONE), mesh netting without litter was placed over trays. Trays were arranged randomly within a glass house. Day and night temperatures in the glass house were 20 °C and 15 °C, respectively, with ambient light only. The galvanized mesh netting reduced light intensity
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11–33% depending on sky conditions (unpublished data). In each tray, 50 seeds of either Pseudoroegneria, Pascopyrum, Euphorbia or Centaurea were placed on top of pasteurized sand. Sand was used to facilitate recovery of seed. Tap water was added daily to the bottom of the tray to keep the sand moist and the litter dry. There were six blocks per litter type (3), seeded species (4) combination. The number of germinated seeds was counted after 32 d to determine germination (%). Seedling heights and the number of leaves were determined at this time. Mechanical effect of litter on transplant survival and growth Besides physically altering the microenvironment, litter may present a mechanical barrier for shoot extension of recently germinated seeds. Thus, we used pregerminated seed to circumvent the potential physical effect of litter, as tested above, on seed germination. Twelve pregerminated seed of either Pseudoroegneria, Pascopyrum, Euphorbia or Centaurea were placed on top of potting soil (.33 soil, .33 potting mix, .34 sand) in each tray. Litter packs, as described above, were then placed on these trays to determine the mechanical effects of Euphorbia and Centaurea litter on seedling survival and growth. Glass house conditions were similar to those of the physical effect trial. Tap water was added daily to the bottom of the tray to keep the soil moist and the litter dry. There were six blocks per litter type (3) – seeded species (4) combination. Survival (%) of these pregerminated seedlings, and height and number of leaves were determined after 28 d. Soil effect on seed germination We collected soils from noninfested and adjacent heavily infested (> 50% Euphorbia or Centaurea) areas to determine the integrative effect of soils on seed germination. Soil cores, approximately 10 cm × 10 cm × 10 cm deep, were collected in late August 1997, and stored in a cold (4 °C), dark room until early March 1998. Soil cores were seeded with 40 seeds of Pseudoroegneria or Pascopyrum or Euphorbia or Centaurea, and misted daily. Treatments were applied randomly within a glass house. Day and night temperatures in the glass house were 20 °C, 15 °C, respectively, with ambient light only. There were ten blocks per soil type/infested-noninfested combination (Euphorbia infested, noninfested; Centaurea infested, noninfested) and seeded species (4). Germination (%) was determined 12 and 24 d after seeding.
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Statistical analyses For the leachate treatment, germination and root length were analyzed with ANOVA in a randomized complete block design (SAS 1988). Main effects of leachate source (Euphorbia, Centaurea), leachate concentration (0X, 0.25X. 0.5X and 1.0X), and seeded species (Pseudoroegneria, Pascopyrum, Euphorbia, Centaurea), and all interactions were tested. For the physical and mechanical studies, germination (%, survival for mechanical), height, and number of leaves were analyzed with ANOVA in a randomized complete block design (SAS 1988). Main effects of litter type (Euphorbia, Centaurea, NONE) and seeded species (Pseudoroegneria, Pascopyrum, Euphorbia, Centaurea), and the litter type-seeded species interaction were tested. For the soils comparison, germination (%) was analyzed with ANOVA in a randomized complete block design (SAS 1988). Main effects of site (Euphorbia, Centaurea), infested (infested, noninfested), and seeded species (Pseudoroegneria, Pascopyrum, Euphorbia, Centaurea), all two way interactions, and the three way interaction were tested. As percent data, germination and survival were arcsine transformed before analysis (Sokal & Rohlf 1995). Non-transformed least square means and standard errors are presented in the tables. Main effects and interactions with P-values less than 0.15 are presented (Gill 1981).
Results Chemical effect of litter on seedling emergence and roots Seed germination was reduced by higher concentrations of leachate (Table 1, P = 0.11). Overall, Centaurea had the highest, Pseudoroegneria was intermediate, and Euphorbia and Pascopyrum had the lowest germination (species, P < 0.0001). Euphorbia roots were longest at intermediate leachate concentrations, whereas roots of the other species were longest at the lowest leachate concentrations (concentration × species, P < 0.0001). Higher Euphorbia leachate concentrations reduced root lengths more than higher Centaurea leachate concentrations (leachate × concentration, P = 0.06). Overall, Euphorbia leachate reduced root lengths more than Centaurea leachate (leachate, P < 0.0001). Physical effect of litter on seed germination and seedling growth Litter type did not affect germination (Table 2). Overall, seed germination was much higher for Cen-
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Table 1. Chemical effect of 0X, 0.25X, 0.5X and 1.0X Centaurea maculosa and Euphorbia esula leachate on seed germination (%) and root length (cm) of Centaurea maculosa – CEMA, Euphorbia esula – EUES, Pascopyrum smithii – PASM, and Pseudoroegneria spicata – PSSP. Non-transformed means for germination (%) are presented. Non-transformed least square mean standard errors of the leachate × concentration × seeded species interaction for germination and root length are 4.3 and 0.3, respectively. Centaurea leachate
Germination (%) CEMA EUES PASM PSSP Root length (cm) CEMA EUES PASM PSSP
Euphorbia leachate
0X
0.25X
0.5X
1.0X
0X
0.25X
0.5X
1.0X
96 61 60 77
98 61 59 78
94 56 63 72
89 50 58 78
96 61 60 77
83 70 67 74
86 53 63 75
93 64 61 72
3.5 2.5 3.3 5.6
3.7 3.4 3.0 5.5
3.4 3.2 3.0 4.7
Table 2. Physical effect of litter type (Centaurea maculosa, Euphorbia esula, no litter – control) on seed germination (%), and shoot height (cm), and number of leaves of seedlings of Centaurea maculosa – CEMA, Euphorbia esula – EUES, Pascopyrum smithii – PASM, and Pseudoroegneria spicata – PSSP. Non-transformed means for germination (%) are presented. Nontransformed least square mean standard errors of the litter × seeded species interaction for germination, shoot height, and number of leaves are 2.8, 0.20, and 0.14. Centaurea litter
Euphorbia litter
No litter
Germination (%) CEMA EUES PASM PSSP
64.7 11.7 77.7 73.0
68.3 7.0 80.7 71.7
68.3 9.7 81.3 73.0
Shoot height (cm) CEMA EUES PASM PSSP
2.3 2.9 7.6 11.0
2.7 3.6 8.4 11.8
1.7 1.2 2.0 2.5
1.8 1.3 1.9 2.4
Leaves (#) CEMA EUES PASM PSSP
3.0 3.1 2.5 3.9
3.5 2.5 3.3 5.6
3.0 3.0 3.0 5.0
2.7 2.9 2.3 4.2
2.2 3.4 1.9 3.1
Table 3. Mechanical effect of litter type (Centaurea maculosa, Euphorbia esula, no litter – control) on survival (%), and shoot height (cm) and number of leaves of seedlings of Centaurea maculosa – CEMA, Euphorbia esula – EUES, Pascopyrum smithii – PASM, and Pseudoroegneria spicata – PSSP. Non-transformed means for survival (%) are presented. Non-transformed least square mean standard errors of the litter × seeded species interaction for survival, shoot height, and number of leaves are 3.6, 0.54, and 0.22. Centaurea litter
Euphorbia litter
No litter
Survival (%) CEMA EUES PASM PSSP
81.9 87.5 98.6 94.4
86.1 91.7 97.2 95.8
94.4 95.8 95.8 91.3
1.6 2.7 6.7 9.9
Shoot height (cm) CEMA EUES PASM PSSP
5.2 5.1 19.1 19.0
5.7 5.4 21.4 20.8
5.8 5.3 21.6 21.7
1.7 1.4 2.0 2.6
Leaves (#) CEMA EUES PASM PSSP
3.5 7.2 3.8 4.6
3.2 7.4 3.8 4.6
3.5 7.6 3.9 4.7
taurea and the native grass species than for Euphorbia (P < 0.0001). Litter type affected seedling heights (litter, P < 0.0001). The tallest seedlings were those covered with Centaurea litter, whereas the shortest were those without litter cover (NONE). Pseudoroegneria and Pascopyrum seedlings were taller than Euphorbia and Centaurea seedlings (species, P < 0.001). Litter type did not affect number of leaves of the four species. Overall, Pascopyrum and Pseudoroegneria seedlings had more leaves than Euphorbia and Centaurea seedlings (species, P < 0.0001).
Mechanical effect of litter on transplant survival and growth Litter type did not affect transplant survival (Table 3). Overall, transplant survival differed among species (species, P = 0.02), ranging from Centaurea’s 88% to Pascopyrum’s 97% The shortest transplants were those covered with Centaurea litter; the tallest were those without litter cover (NONE, litter, P < 0.0005). Pseudoroegneria and Pascopyrum transplants were much taller than Euphorbia and Centaurea transplants (species, P < 0.0001).
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Table 4. Effect of soils from Centaurea maculosa- and Euphorbia esula-infested areas and adjacent noninfested areas on 12 d and 24 d seed germination (%) of Centaurea maculosa – CEMA, Euphorbia esula – EUES, Pascopyrum smithii – PASM, and Pseudoroegneria spicata – PSSP. Non-transformed means for germination (%) are presented. Non-transformed least square mean standard errors for the 12 and 24 d site × infested × seeded species interactions are 6.8 and 5.3, respectively. Centaurea site Infested Germination CEMA EUES PASM PSSP
12 d 32.3 0.8 8.3 33.8
Euphorbia site Noninfested
24 d 86.0 14.3 48.3 58.0
12 d 73.5 4.0 36.3 51.0
Infested 24 d 93.3 21.5 60.8 65.3
Litter type did not affect number of leaves of the four species. Overall, the number of leaves on the transplants differed among species; Euphorbia had the most leaves, whereas Centaurea and Pascopyrum had the least (species, P < 0.0001). Soil effect on seed germination Overall, early germination (12 d) on soils from noninfested areas was higher than germination on soils from infested areas (infested, P = 0.02, Table 4), but this differed between soils from the two sites (site × infested, P = 0.01). Seed germination on soils from Centaureainfested areas was much lower than from noninfested areas, whereas the difference was not as great for seed germination on soil from Euphorbia-infested and adjacent noninfested areas. Early germination of the four species differed depending on whether soils were from infested or noninfested areas (species × infested, P = 0.15). Euphorbia germination was similar on infested and noninfested soils. Pascopyrum germination was similar on soils from Euphorbia infested and adjacent noninfested sites. Besides these exceptions, germination of the other species was higher on noninfested soils. Differences in germination 24 d after seeding were not as pronounced as at 12 d, partly because germination of Euphorbia was higher on soils from Euphorbia-infested than adjacent noninfested areas (site × infested, P = 0.04).
Discussion Chemical effect of litter on seedling emergence and roots Leachate of both species, even at full strength, had minimal effect on seed germination. Similarly, aqueous extracts of Euphorbia foliage had minimal effect on germination of Alaskan pea (Pisum sativa L. Alaska CV, Tourneau & Heggeness 1957). In laboratory bioassays, cnicin in Centaurea was phytotoxic toward
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12 d 48.5 7.0 19.0 27.8
Noninfested 24 d 85.3 31.5 53.0 61.3
12 d 58.3 2.5 19.5 42.0
24 d 87.0 14.0 54.5 66.5
native grasses and conifers (Kelsey & Locken 1987), however the major effect was on root growth, not seed germination. Sometimes the effect of a leachate can be species specific. A leachate of litter from the perennial grass Poa pratensis L. reduced germination of Centaurea nigra L. and Dipsacus sylvestris Huds., but did not affect germination of Verbascum thapsus L. and Hypericum perforatum L. (Bosy & Reader 1995). An extract of Setaria sphacelata completely inhibited, and a leachate reduced, germination of the native Sporobolus indicus (Andrew et al. 1997). Apparently, leachate of Euphorbia and Centaurea in our trial was not imbibed and thereby did not cause seed mortality or inhibit germination, but leachate can affect normal seedling development. Our findings agree with Kelsey & Everett’s (1995) suggestion that the mode of action of phytotoxins often interferes with a particular physiological process, and has no effect on germination. For example, root lengths of our seeded species were affected by leachate concentration, but the response differed among species. Root growth of Euphorbia seedlings was actually stimulated at intermediate concentrations. Many secondary compounds stimulate plant growth at low concentrations, but inhibit growth at high concentrations (Stevens & Merrill 1985, Leather & Einhellig 1988). For our other species, roots were shorter at higher leachate concentrations, similar to findings from other studies (Tourneau & Heggeness 1957, Kelsey & Locken 1987). Andrew et al. (1997) found that leachate of Setaria sphacelata reduced shoot and root growth of Sporobolus indicus, but that leachate from Axonopus affinis had no effect. Because of Setaria’s effect on root and shoot growth, they suggested that Setaria would be more resistant to infestation than Axonopus affinis. Like many leachate studies, our leachate trial was highly controlled, lacking soil particles which may adsorb compounds, and microorganisms which may render compounds harmless or use them as a carbon and energy source (Vokou et al. 1984). The value of such
Effects of invasive forb litter on seedlings
bioassays has been questioned (Stowe 1979, Henn et al. 1988), but bioassays may be used to indicate the role of chemical compounds in plant-plant interaction (Kelsey & Everett 1995). However, this role should be validated in the field or at least with natural soils (Kelsey & Everett 1995, Inderjit et al. 1997), as we did with soils collected from infested sites. Physical effect of litter on seed germination and seedling growth Litter reduces irradiance and moderates temperature (Bosy & Reader 1995), especially when litter thickness exceeds a threshold amount. Litter reduced seed germination and survival of the annual weed Cardamine pensylvanica (Molofsky et al. 2000), although their population dynamics model indicated this reduction would not be demographically significant over the long term. In a litter pack study, the physical presence of grass litter reduced seed germination of four different herbs from 14% to 41% (Bosy & Reader 1995). In a field study, litter cover inhibited germination of several forb species, but most seedlings died within the first month, with or without litter cover (Wilby & Brown 2001). In a meta-analysis of 35 independent litter studies, germination and establishment were reduced and aboveground biomass was enhanced by litter in grassland ecosystems (Xiong & Nilsson 1999). Forb litter had a negative effect on all of these variables, whereas the effect of grass litter ranged from neutral (germination) to slightly negative (establishment) to slightly positive (aboveground biomass). Our litter packs did not reduce germination of the seeded species, unlike Bosy & Reader (1995). However, their litter packs contained 715 g m–2, whereas our packs contained 500 g m–2 of Euphorbia litter and 225 g m–2 of Centaurea litter. Thus, we would expect greater interception of light and less germination in Bosy & Reader’s (1995) study compared with ours, especially with Centaurea. They used more plant material in their litter packs because they collected litter from a mesic old-field in eastern Canada. Our litter mass mimicked amounts from less productive, mixed grass prairies in southwestern Montana. Although litter type did not affect seed germination in our study, seedling heights differed among litter types. The tallest seedlings were those covered with Centaurea litter; the shortest were those without litter cover. Most plants exposed to full irradiance do not need to allocate resources to extend shoot growth to compete for light (Lambers et al. 1998), which may explain the latter result. For the same reason, we would have expected Euphorbia litter, with mass greater than twice as much as Centaurea’s litter, to have the tallest seedlings to compete for light, but they
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were shorter than those under the Centaurea litter. The thicker Euphorbia litter may have mechanically prevented seedlings from growing taller, or may have reduced soil temperatures enough to reduce growth rates of seedlings. Mechanical effect of litter on transplant survival and growth In our glass house trial, litter type did not affect survival of the pregerminated seeds of our four species. In a field study, most forb seedlings died within the first month, with or without litter cover (Wilby & Brown 2001). In some systems characterized by low to intermediate levels of productivity, litter may facilitate survival of young seedlings (Foster 1999, Nash Suding & Goldberg 1999), possibly because litter ameliorates abiotic stress at this sensitive life history stage (Callaway & Walker 1997). Litter type affected heights of our seedlings. The tallest seedlings were those without litter cover (NONE). For four different herbaceous species, shoot extension above a layer of litter was reduced 95–100% (Bosy & Reader 1995). These results differed from our seedlings in the physical effects trial where the shortest were those without cover. In that trial, germinating seeds may have received a cue about their light environment immediately, and adjusted growth form accordingly. In our mechanical effects trial, the pregerminated seeds may not have been exposed to an early cue created by litter type, resulting in a different growth response. Soil effect on seed germination Germination was greatest on noninfested soils, except for Euphorbia germination on infested soils from the Euphorbia site. However, germination of Euphorbia was so low that whether infested soils actually “enhanced” germination for this species, or whether these results reflect chance or our relatively small sample size cannot be identified. For the other seeded species, germination was 14 to 26% higher on noninfested soils. Using soil cores in this trial essentially integrates the effects of these invasive forbs on soil properties. Apparently, Euphorbia and Centaurea in some unknown way alter soil physical or chemical properties, which in turn reduces, but does not eliminate, seed germination. Soils infested or amended with chickweed Stellaria media reduced shoot and root growth of wheat Triticum aestivum (Inderjit & Dakshini 1998), although effects on germination were not measured. Compared with seed germination on noninfested soils, soils from infested Centaurea areas reduced seed
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germination more than soils from infested Euphorbia areas. This may reflect the effect of different secondary chemistry or root structure of these two species on soil chemical and physical properties.
Conclusions Does litter from invasive forbs hinder seedling establishment of native species? Our results indicate that litter from these invasive forbs can have subtle effects on growth of seedlings of Pascopyrum and especially Pseudoroegneria, and that these forbs have some, unknown effect on soil properties which reduces germination. Leachate from litter of Euphorbia also had a negative effect on Centaurea. This may partly explain why Euphorbia is currently replacing Centaurea in western Montana, which has displaced the native Pseudoroegneria on many sites. The “negative” effects of Centaurea litter on Centaurea seedlings, or autotoxicity, may synchronize germination with the wettest season, or minimize effects of intraspecific competition which may actually benefit Centaurea at the population level (Kelsey & Everett 1995). Physical and mechanical effects associated with Euphorbia and Centaurea litter were more subtle than chemical effects, and probably are not specific to invasive forbs. For example, thick grass litter (Poa pratensis L.) reduces germination and shoot extension of several forbs (Bosy & Reader 1995). Many of the litter effects in this controlled glass house study were subtle. In a meta-analysis of 35 independent studies, plant responses were more affected by litter in field than in glasshouse studies (Xiong & Nilsson 1999), suggesting effects of our invasive forb litter could be greater in the field. This is supported by reduced seed germination, except for Euphorbia, on soils collected from infested sites. Litter of Euphorbia and Centaurea in mixed grass prairies may accumulate simply because they are not grazed by the dominant large herbivores, cattle and horses. Using sheep or goats to graze these weeds (Olson 1999), or prescribed fire periodically will reduce litter accumulation and any associated physical, mechanical and chemical litter effects on native species establishment.
Acknowledgements. This study was supported by the USDA-CSREES and the Montana Agricultural Experiment Station. We thank K. Olson-Rutz for reviewing the manuscript. Published with approval of the Director, Montana Agricultural Experiment Station, as Journal No. J-2000-42.
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References Andrew TS, Jones CE, Whalley RDB (1997) Factors affecting the germination of Giant parramatta grass. Australian Journal of Experimental Agriculture 37: 439–446. Bakke AL (1936) Leafy spurge, Euphorbia esula L., Iowa Agricultural Experiment Station Research Bulletin 198: 209–246. Best KF, Bowes GG, Thomas AG, Maw MG (1980) The biology of Canadian weeds. 39. Euphorbia esula L. Canadian Journal of Plant Science 60: 651–663. Bosy JL, Reader RJ (1995) Mechanisms underlying the suppression of forb seedling emergence by grass (Poa pratensis) litter. Functional Ecology 9: 635–639. Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78: 1958–1965. Chicoine TK, Fay PK, Nielsen GA (1985) Predicting weed migration from soil and climate maps. Weed Science 34: 57–61. Clements FE (1916) Plant succession. Carnegie Institute of Washington. Pub 242. Evans FJ, Kinghorn AD (1977) A comparative phytochemical study of the diterpenes of some species of the genera Euphorbia and Elaeophorbia (Euphorbicaceae). Botanical Journal of the Linnaean Society 74: 23–27. Facelli JM, Pickett STA (1991) Plant litter: its dynamics and effects on plant community structure. The Botanical Review 57: 1–32. Foster BL (1999) Establishment, competition and the distribution of native grasses among Michigan old-fields. Journal of Ecology 87: 476–489. Gill JL (1981) Evolution of statistical design and analysis of experiments. Journal of Dairy Science 64: 1494–1519. Henn H, Petit D, Vernet P (1988) Interference between Hieracium pilosella and Arrhenatherum elatius in colliery spoils of north France. Oecologia 76: 268–272. Inderjit, Dakshini KMM (1998) Allelopathic interference of chickweed Stellaria media with seedling growth of wheat (Triticum aestivum). Canadian Journal of Botany 76: 1317– 1321. Inderjit, del Moral R (1997) Is separating resource competition from allelopathy realistic? Botanical Review 63: 221–230. Inderjit, Muramatsu M, Nishimura H (1997) On the allelopathic potential of certain terpenoids, phenolics, and their mixtures, and their recovery from soil. Canadian Journal of Botany 75: 888–891. Kelsey RG, Everett RL (1995) Allelopathy. In: Bedunah D, Sosebee R (eds) Wildland Plants: Physiological Ecology and Developmental Morphology. Society for Range Management, Denver, Colo, pp. 479–549. Kelsey RG, Locken LJ (1987) Phytotoxic properties of cnicin, a sesquiterpene lactone from Centaurea maculosa (spotted knapweed). Journal of Chemical Ecology 13: 19–33. Kucera CL, Dahlman RC (1967) Total net productivity and turnover on an energy basis for tallgrass prairie. Ecology 48: 536–541.
Effects of invasive forb litter on seedlings Lacey JR (1989) A complete takeover by knapweed in 2001? Montana Farmer-Stockman 70: 32–34. Lambers H, Chapin FS, Pons TL (1998) Plant Physiological Ecology. Springer, New York. Lajeunesse S, Sheley R, Lym R, Cooksey D, Duncan C, Lacey J, Rees N, Ferrell M (1997) Leafy spurge: biology, ecology and management. Montana State University Extension Service EB-134. Laycock WA (1991) Stable states and thresholds of range condition on North American rangelands: a viewpoint. Journal of Range Management 44: 427–433. Leather GR, Einhellig FA (1988) Bioassay of naturally occurring allelochemicals for phytotoxicity. Journal of Chemical Ecology 14: 1821–1828. Molofsky J, Lanza J, Crone EE (2000) Plant litter feedback and population dynamics in an annual plant, Cardamine pensylvanica. Oecologia 124: 522–528. Mufti MM, Sydes CL, Furness SB, Grime JP, Band SR (1977) A quantitative analysis of shoot phenology and dominance in herbaceous vegetation. Journal of Ecology 65: 759– 791. Nash Suding K, Goldberg DE (1999) Variation in the effects of vegetation and litter on recruitment across productivity gradients. Journal of Ecology 87: 436–449. Olson BE (1999) Grazing and weeds. In: Sheley R, Petroff J (eds) Biology and management of noxious rangeland weeds. Oregon State University Press, Corvallis, pp 85–96. Olson BE, Kelsey RG (1997) Effect of Centaurea maculosa on sheep rumen microbial activity and mass. Journal of Chemical Ecology 23: 1131–1144. Pimm SL (1993) Biodiversity and the balance of nature. In: Schulze E-D, Mooney HA (eds) Biodiversity and Ecosystem Function. Springer-Verlag, Berlin, pp 347–359. Rietkerk M, van de Koppel J (1997) Alternate stable states and threshold effects in semi-arid grazing systems. Oikos 79: 69–76. Ridenour WM, Callaway RM (2001) The relative importance of allelopathy in interference: the effects of an invasive weed on a native bunchgrass. Oecologia 126: 444–450.
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Roberts J, Olson BE (1999) Effect of Euphorbia esula on sheep rumen microbial activity and mass in vitro. Journal of Chemical Ecology 25: 297–314. SAS (1988) Statistical Analysis System. SAS Institute, Inc. Raleigh, North Carolina. Schlatterer EF, Tisdale EW (1969) Effects of litter of Artemisia, Chrysothamnus and Tortula on germination and growth of three perennial grasses. Ecology 50: 869–873. Sokal RR, Rohlf FJ (1995) Biometry, 3rd Edition. W.H. Freeman and Co. New York. Stevens KL, Merrill GB (1985) Sesquiterpene lactones and allelochemicals from Centaurea species. In: Thompson A (ed) The Chemistry of Allelopathy. ACS Symposium Series 268., American Chemical Society, Washington, DC, pp 83–98. Stowe LG (1979) Allelopathy and its influence on the distribution of plants in an Illinois old-field. Journal of Ecology 67: 1065–1085. Tourneau DL, Heggeness HG (1957) Germination and growth inhibitors in leafy spurge foliage and quackgrass rhizomes. Weeds 5: 12–19. Vokou D, Margaris NS, Lynch JM (1984) Effects of volatile oils from aromatic shrubs on soil microorganisms. Soil Biology and Biochemistry 16: 509–513. Weigelt A, Steinlein T, Beyschlag W (2002) Does plant competition intensity rather depend on biomass or on species identity? Basic and Applied Ecology 3: 85–94. Westoby M, Walker B, Noy-Meir I (1989) Opportunistic management for rangelands not at equilibrium. Journal of Range Management 42: 266–274. Wilby A, Brown VK (2001) Herbivory, litter and soil disturbance as determinants of vegetation dynamics during oldfield succession under set-aside. Oecologia 127: 259– 265. Xiong S, Nilsson C (1999) The effects of plant litter on vegetation: a meta-analysis. Journal of Ecology 87: 984–994. Zobel M (1997) The relative role of species pools in determining plant species richness: an alternative explanation of species coexistence. Trends in Ecology and Evolution 12: 266–269.
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Basic and Applied Ecology
Effects of invasive forb litter on seed germination, seedling growth and survival Bret E. Olson*, Roseann T. Wallander Department of Animal and Range Sciences, Montana State University-Bozeman, Bozeman, U.S.A.
Received May 28, 2001 · Accepted March 18, 2002
Abstract Two Eurasian forbs, Euphorbia esula L. and Centaurea maculosa Lam., continue to spread in the northwestern United States despite extensive and expensive control efforts. We investigated whether litter from these forbs and associated soils suppress germination and growth of two native perennial grasses (Pseudoroegneria spicata [Scribn. & Smith A. Love], Pascopyrum smithii [Rydb.] A. Love), which may partly explain the success of these invasive forbs. Seed germination was unaffected, but roots were shorter at higher leachate concentrations. The physical presence of litter (Euphorbia, Centaurea, none) did not affect seed germination or number of leaves of seedlings of the four species, but it affected seedling heights; the tallest seedlings were those covered with Centaurea litter; the shortest were those without litter. As a mechanical barrier, litter type did not affect survival or number of leaves of pregerminated seeds, but litter inhibited shoot growth. Seed germination of the four species on soils from infested or noninfested areas differed; Euphorbia germination, albeit low (< 4%) was higher on soils collected from Euphorbia- infested areas, whereas germination of the other species was higher on soils from noninfested areas. These results indicate that litter from these invasive forbs can have subtle effects on growth of seedlings of these native grasses, especially the native Pseudoroegneria, and that these forbs have some unknown effect on soil properties which reduce germination. Die Ausbreitung zweier Unkräuter eurasiatischer Herkunft (Euphorbia esula L. und Centaurea maculosa Lam.) in den nordwestlichen USA konnte trotz umfangreicher Gegenmaßnahmen bisher nicht aufgehalten werden. Wir untersuchten, ob diese Kräuter durch Streuproduktion oder andere Bodenveränderungen eine negative Wirkung auf Keimfähigkeit und Wachstum zweier heimischer mehrjähriger Gräser (Pseudoroegneria spicata [Scribn. & Smith A. Love], Pascopyrum smithii [Rydb.] A. Love) ausüben, was zum Teil den Erfolg dieser Unkräuter erklären könnte. Saataufgang war nicht beeinträchtigt, aber Wurzeln waren kürzer und wiesen höhere Exsudatkonzentrationen auf. Die pure Anwesenheit von Euphorbia- oder Centaurea streu hatte keinen Effekt auf Auflauf oder Blattanzahl der Sämlinge aller vier Arten, sowohl auf Böden aus verunkrauteten Arealen als auch auf vorher unkrautfreien Böden. Streu beeinflusste aber die Sämlingshöhe: die höchsten Sämlinge traten in Verbindung mit Centaurea Streu auf, die niedrigsten unter streulosen Bedingungen. Die Streuart hatten keinen Einfluss auf Überlebensfähigkeit oder Blattzahl vorgekeimter Samen, jedoch beeinträchtigte das Vorhandensein von Streu die Sprosslänge. Die Keimfähigkeit der vier Arten hing davon ab, ob die Böden aus verunkrauteten oder unkrautfreien Gebieten stammten. Die Euphorbia-Keimrate, obwohl generell niedrig (< 4 %), war höher auf Böden aus Euphorbia-befallenen Gebieten, die Keimfähigkeit der anderen Arten war höher auf Böden aus unkrautfreien Arealen. Un-
*Corresponding author: Bret E. Olson, Department of Animal and Range Sciences, Montana State University-Bozeman, Bozeman, MT 59717, USA, Phone: +1-406-994-5571, Fax +1-406-994-5589, E-mail: [email protected]
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Olson and Wallander sere Resultate zeigen, dass Streu dieser eingeschleppten Kräuter leichte Effekte auf das Keimlingswachstum der beiden heimischen Gräser ausübt, insbesondere auf die heimische Pseudoroegneria und dass diese Käuter die Bodeneigenschaften in bisher unbekannter Weise beeinflussen, welche die Keimungsrate beeinträchtigen. Key words: allelopathy – Centaurea maculosa – Euphorbia esula – invasive species – leachate – shoot extension – soils
Introduction Certain Eurasian forbs, such as Euphorbia esula L. and Centaurea maculosa Lam., are spreading rapidly on mixed grass prairies of western North America. When we attempt to eradicate these forbs to restore native plant communities, we assume these communities will then proceed toward the potential natural plant community based on Clements’ (1916) model of plant succession. However, the Clementsian model may not be appropriate if these forbs permanently alter site conditions. Alternatively, a multiple steady state, state and transition model may best represent steady states dominated by invasive forbs (Westoby et al. 1989, Laycock 1991, Pimm 1993, Rietkerk & van de Koppel 1997). These new steady states may be maintained by mechanisms, e.g. interference, allelopathy, etc. (Inderjit & del Moral 1997, Ridenour & Callaway 2001) that hinder the establishment of native grasses by reducing seed germination or seedling growth. In some cases, steady states dominated by invasive forbs may reflect that their presence and the relative absence of native species on a local scale are determined by species presence/absence on a larger scale (Zobel 1997). However, as a potential source of propagules, native species seldom become extinct at such larger scales, which would be needed to explain their depauperate status at local scales, because they are usually present in seedbanks or isolated refugia. Different properties of plant litter can have a major influence on native plant establishment (Facelli & Pickett 1991, Bosy & Reader 1995). Litter from certain plants can reduce seed germination and seedling growth by leaching inhibitory compounds, altering microclimate, and preventing shoot extension (Schlatterer & Tisdale 1969, Bosy & Reader 1995). Many invasive forbs contain secondary compounds which can be leached from litter, released with decomposition, or exuded from roots (Kelsey & Everett 1995). For example, Euphorbia esula contains di- and tri-terpenoids, and condensed tannins (Evans & Kinghorn 1977, Roberts & Olson 1999). Centaurea maculosa contains high concentrations of cnicin, a
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sesquiterpene lactone (Kelsey & Locken 1987, Olson & Kelsey 1997). In laboratory bioassays, cnicin is phytotoxic toward native grasses and conifers; root growth is inhibited more than germination (Kelsey & Locken 1987). On agar gel, root and shoot growth of lettuce (Lactuca sativa L.) was reduced by certain terpenoids, whereas only root growth was reduced on natural soils (Inderjit et al. 1997); they recommended that natural soils should be used for growth bioassays. Litter from invasive forbs may accumulate rapidly because of structural and/or the aforementioned chemical deterrents to detritivores and decomposers. Euphorbia and Centaurea litter can accumulate up to 10– and 5 cm thick, respectively, on mixed grass prairies (Olson & Wallander, unpublished data). This added physical structure may alter irradiance, relative humidity, soil and air temperatures, and wind velocity close to the soil surface (Bosy & Reader 1995). Depending on litter thickness, an altered microenvironment often affects seed germination, and benefits or hinders early growth of seedlings (Facelli & Pickett 1991, Foster 1999, Molofsky et al. 2000). For example, seeds that germinate earlier under such conditions will accumulate greater biomass, and have a greater probability of establishing during this crucial, life history stage (Weigelt et al. 2002). Besides altering the microenvironment, litter may present a mechanical barrier for shoot extension of recently germinated seeds (Kucera & Dahlman 1967, Mufti et al. 1977, Bosy & Reader 1995). This would reduce a seedling’s ability to capture sunlight, photosynthesize, and grow. Assessing litter’s physical effect on seed germination and its mechanical effect on shoot extension and survival of seedlings covers two critical life-history stages (Nash Suding & Goldberg 1999). Our objective was to determine whether chemical, physical, or mechanical properties of litter, or soils influenced by the invasive forbs Euphorbia and Centaurea affect seedling emergence, growth, and survival of two native grasses (Pseudoroegneria spicata [Scribn. & Smith A. Love], Pascopyrum smithii [Rydb.] A. Love), and of themselves (autotoxicity).
Effects of invasive forb litter on seedlings
Materials and methods Plant materials Leafy spurge (Euphorbia esula L.) is a perennial forb from Eurasia. It has a deep (5–9 m) and extensive lateral root system (Bakke 1936, Best et al. 1980). It currently infests over 1.25 million hectares in the northern Great Plains in the United States and Canada (Lajeunesse et al. 1997). Spotted knapweed (Centaurea maculosa Lam.), a perennial tap-rooted forb from Eurasia, infests over 2.8 million hectares in the northwestern United States (Lacey 1989). These invasive forbs have the potential to spread onto many sites in Montana (Chicoine et al. 1985, Lajeunesse et al. 1997). Bluebunch wheatgrass (Pseudoroegneria spicata [Scribn. & Smith A. Love]) is a native, perennial tussock grass. Common co-dominants are Idaho fescue (Festuca idahoensis Elmer) and blue grama (Bouteloua gracilis [H.B.K.] Lag.). Western wheatgrass (Pascopyrum smithii [Rydb.] A. Love) is a native, perennial rhizomatous grass. Common co-dominants are needleand-thread (Stipa comata Trin. & Rupr.) and green needlegrass (Stipa viridula Trin.). Historically, these grass species dominated many mixed grass prairies in northwestern United States. Euphorbia and Centaurea co-occur with both grass species, but usually on different sites, mainly because Pseudoroegneria and Pascopyrum seldom co-occur. Pseudoroegneria grows primarily on well-drained, upland soils whereas Pascopyrum grows on swales and bottomlands. All four species have the C3 photosynthetic pathway (B. Olson, unpublished data). Litter was collected from a Centaurea-infested (> 50% Centaurea based on foliar cover) site 50 km west of Bozeman, Montana U.S.A. on 13 September 1996. Soil samples from infested and adjacent noninfested areas (< 5% Centaurea) were collected with a 10-cm diameter core. Soil was a deep, well-drained loamy sand in the taxonomic class, mixed rigid Ustic Torripsamment. Litter was collected from our Euphorbia-infested (> 50% Euphorbia based on foliar cover) site 5 km northeast of Bozeman, Montana U.S.A. on 30 September 1996. Soil samples from infested and adjacent noninfested areas (< 5% Euphorbia) were collected with the same core. Soil was a well-drained cobbly loam in the taxonomic class, clayey-skeletal, mixed superactive Udic Argiborolls. Overall, the invasive forbs and grasses grew in distinct, interspersed patches, presumably reflecting clumping associated with dispersal or micro-disturbances. The litter represented that year’s senescent stems, leaves, and flowerheads only; most of the material was standing.
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Seeds from these invasive forbs were collected from heavily infested areas where soils and litter were collected. Seed of Pseudoroegneria (Goldar variety) and Pascopyrum (Rosana variety) was provided by the Bridger Plant Materials Center, USDA-ARS, Bridger, Montana, U.S.A. Chemical effect of litter on seedling emergence and roots To determine the chemical effect of Euphorbia and Centaurea litter on germination and root development, we created a leachate by soaking Euphorbia (8.2 g leaves, 24.8 g stems) and Centaurea (2.4 g leaves, 13.6 g stems) litter in 600 ml and 300 ml, respectively, of deionized, distilled water for 72 h, and then we filtered the solution. Leachate was diluted with distilled water to create 0X (distilled water), 0.25X, 0.5X, and 1.0X concentrations. Twenty-five seeds of either Pseudoroegneria, Pascopyrum, Euphorbia or Centaurea were placed on filter paper in petri plates. Twelve ml of each leachate solution combination (two source species, four concentrations) were added to the filter paper. Petri plates were sealed with parafilm to reduce evaporation. They were placed in a cold (4 °C) dark room for 7 d, and then placed in seed germinators (Hoffman Manufacturing, Albany, Oregon, U.S.A.) at an alternating cycle of 25 °C and 15 °C for 12 h every 24 h for 7 d. There were five blocks for each leachate source (Euphorbia, Centaurea), leachate concentration (0X, 0.25X, 0.5X, 1.0X), seeded species (Pseudoroegneria, Pascopyrum, Euphorbia or Centaurea) combination. Plates were removed from the germinators after 14 d. Germination (%) was determined and root length was measured. Physical effect of litter on seed germination and seedling growth We determined the physical effect of Euphorbia and Centaurea litter on seed germination and early seedling growth by sowing seeds into sand-filled trays covered with litter packs. The litter packs (galvanized steel mesh netting; 0.6 cm; after Bosy & Reader 1995) were elevated 2–3 cm above the sand surface in a series of 13 cm × 18 cm plastic trays. The amount of litter placed in litter packs mimicked the amount found on a heavily infested site of each species (Euphorbia 500 g m–2; Centaurea 225 g m–2, unpublished data). For the control (NONE), mesh netting without litter was placed over trays. Trays were arranged randomly within a glass house. Day and night temperatures in the glass house were 20 °C and 15 °C, respectively, with ambient light only. The galvanized mesh netting reduced light intensity
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11–33% depending on sky conditions (unpublished data). In each tray, 50 seeds of either Pseudoroegneria, Pascopyrum, Euphorbia or Centaurea were placed on top of pasteurized sand. Sand was used to facilitate recovery of seed. Tap water was added daily to the bottom of the tray to keep the sand moist and the litter dry. There were six blocks per litter type (3), seeded species (4) combination. The number of germinated seeds was counted after 32 d to determine germination (%). Seedling heights and the number of leaves were determined at this time. Mechanical effect of litter on transplant survival and growth Besides physically altering the microenvironment, litter may present a mechanical barrier for shoot extension of recently germinated seeds. Thus, we used pregerminated seed to circumvent the potential physical effect of litter, as tested above, on seed germination. Twelve pregerminated seed of either Pseudoroegneria, Pascopyrum, Euphorbia or Centaurea were placed on top of potting soil (.33 soil, .33 potting mix, .34 sand) in each tray. Litter packs, as described above, were then placed on these trays to determine the mechanical effects of Euphorbia and Centaurea litter on seedling survival and growth. Glass house conditions were similar to those of the physical effect trial. Tap water was added daily to the bottom of the tray to keep the soil moist and the litter dry. There were six blocks per litter type (3) – seeded species (4) combination. Survival (%) of these pregerminated seedlings, and height and number of leaves were determined after 28 d. Soil effect on seed germination We collected soils from noninfested and adjacent heavily infested (> 50% Euphorbia or Centaurea) areas to determine the integrative effect of soils on seed germination. Soil cores, approximately 10 cm × 10 cm × 10 cm deep, were collected in late August 1997, and stored in a cold (4 °C), dark room until early March 1998. Soil cores were seeded with 40 seeds of Pseudoroegneria or Pascopyrum or Euphorbia or Centaurea, and misted daily. Treatments were applied randomly within a glass house. Day and night temperatures in the glass house were 20 °C, 15 °C, respectively, with ambient light only. There were ten blocks per soil type/infested-noninfested combination (Euphorbia infested, noninfested; Centaurea infested, noninfested) and seeded species (4). Germination (%) was determined 12 and 24 d after seeding.
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Statistical analyses For the leachate treatment, germination and root length were analyzed with ANOVA in a randomized complete block design (SAS 1988). Main effects of leachate source (Euphorbia, Centaurea), leachate concentration (0X, 0.25X. 0.5X and 1.0X), and seeded species (Pseudoroegneria, Pascopyrum, Euphorbia, Centaurea), and all interactions were tested. For the physical and mechanical studies, germination (%, survival for mechanical), height, and number of leaves were analyzed with ANOVA in a randomized complete block design (SAS 1988). Main effects of litter type (Euphorbia, Centaurea, NONE) and seeded species (Pseudoroegneria, Pascopyrum, Euphorbia, Centaurea), and the litter type-seeded species interaction were tested. For the soils comparison, germination (%) was analyzed with ANOVA in a randomized complete block design (SAS 1988). Main effects of site (Euphorbia, Centaurea), infested (infested, noninfested), and seeded species (Pseudoroegneria, Pascopyrum, Euphorbia, Centaurea), all two way interactions, and the three way interaction were tested. As percent data, germination and survival were arcsine transformed before analysis (Sokal & Rohlf 1995). Non-transformed least square means and standard errors are presented in the tables. Main effects and interactions with P-values less than 0.15 are presented (Gill 1981).
Results Chemical effect of litter on seedling emergence and roots Seed germination was reduced by higher concentrations of leachate (Table 1, P = 0.11). Overall, Centaurea had the highest, Pseudoroegneria was intermediate, and Euphorbia and Pascopyrum had the lowest germination (species, P < 0.0001). Euphorbia roots were longest at intermediate leachate concentrations, whereas roots of the other species were longest at the lowest leachate concentrations (concentration × species, P < 0.0001). Higher Euphorbia leachate concentrations reduced root lengths more than higher Centaurea leachate concentrations (leachate × concentration, P = 0.06). Overall, Euphorbia leachate reduced root lengths more than Centaurea leachate (leachate, P < 0.0001). Physical effect of litter on seed germination and seedling growth Litter type did not affect germination (Table 2). Overall, seed germination was much higher for Cen-
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Table 1. Chemical effect of 0X, 0.25X, 0.5X and 1.0X Centaurea maculosa and Euphorbia esula leachate on seed germination (%) and root length (cm) of Centaurea maculosa – CEMA, Euphorbia esula – EUES, Pascopyrum smithii – PASM, and Pseudoroegneria spicata – PSSP. Non-transformed means for germination (%) are presented. Non-transformed least square mean standard errors of the leachate × concentration × seeded species interaction for germination and root length are 4.3 and 0.3, respectively. Centaurea leachate
Germination (%) CEMA EUES PASM PSSP Root length (cm) CEMA EUES PASM PSSP
Euphorbia leachate
0X
0.25X
0.5X
1.0X
0X
0.25X
0.5X
1.0X
96 61 60 77
98 61 59 78
94 56 63 72
89 50 58 78
96 61 60 77
83 70 67 74
86 53 63 75
93 64 61 72
3.5 2.5 3.3 5.6
3.7 3.4 3.0 5.5
3.4 3.2 3.0 4.7
Table 2. Physical effect of litter type (Centaurea maculosa, Euphorbia esula, no litter – control) on seed germination (%), and shoot height (cm), and number of leaves of seedlings of Centaurea maculosa – CEMA, Euphorbia esula – EUES, Pascopyrum smithii – PASM, and Pseudoroegneria spicata – PSSP. Non-transformed means for germination (%) are presented. Nontransformed least square mean standard errors of the litter × seeded species interaction for germination, shoot height, and number of leaves are 2.8, 0.20, and 0.14. Centaurea litter
Euphorbia litter
No litter
Germination (%) CEMA EUES PASM PSSP
64.7 11.7 77.7 73.0
68.3 7.0 80.7 71.7
68.3 9.7 81.3 73.0
Shoot height (cm) CEMA EUES PASM PSSP
2.3 2.9 7.6 11.0
2.7 3.6 8.4 11.8
1.7 1.2 2.0 2.5
1.8 1.3 1.9 2.4
Leaves (#) CEMA EUES PASM PSSP
3.0 3.1 2.5 3.9
3.5 2.5 3.3 5.6
3.0 3.0 3.0 5.0
2.7 2.9 2.3 4.2
2.2 3.4 1.9 3.1
Table 3. Mechanical effect of litter type (Centaurea maculosa, Euphorbia esula, no litter – control) on survival (%), and shoot height (cm) and number of leaves of seedlings of Centaurea maculosa – CEMA, Euphorbia esula – EUES, Pascopyrum smithii – PASM, and Pseudoroegneria spicata – PSSP. Non-transformed means for survival (%) are presented. Non-transformed least square mean standard errors of the litter × seeded species interaction for survival, shoot height, and number of leaves are 3.6, 0.54, and 0.22. Centaurea litter
Euphorbia litter
No litter
Survival (%) CEMA EUES PASM PSSP
81.9 87.5 98.6 94.4
86.1 91.7 97.2 95.8
94.4 95.8 95.8 91.3
1.6 2.7 6.7 9.9
Shoot height (cm) CEMA EUES PASM PSSP
5.2 5.1 19.1 19.0
5.7 5.4 21.4 20.8
5.8 5.3 21.6 21.7
1.7 1.4 2.0 2.6
Leaves (#) CEMA EUES PASM PSSP
3.5 7.2 3.8 4.6
3.2 7.4 3.8 4.6
3.5 7.6 3.9 4.7
taurea and the native grass species than for Euphorbia (P < 0.0001). Litter type affected seedling heights (litter, P < 0.0001). The tallest seedlings were those covered with Centaurea litter, whereas the shortest were those without litter cover (NONE). Pseudoroegneria and Pascopyrum seedlings were taller than Euphorbia and Centaurea seedlings (species, P < 0.001). Litter type did not affect number of leaves of the four species. Overall, Pascopyrum and Pseudoroegneria seedlings had more leaves than Euphorbia and Centaurea seedlings (species, P < 0.0001).
Mechanical effect of litter on transplant survival and growth Litter type did not affect transplant survival (Table 3). Overall, transplant survival differed among species (species, P = 0.02), ranging from Centaurea’s 88% to Pascopyrum’s 97% The shortest transplants were those covered with Centaurea litter; the tallest were those without litter cover (NONE, litter, P < 0.0005). Pseudoroegneria and Pascopyrum transplants were much taller than Euphorbia and Centaurea transplants (species, P < 0.0001).
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Table 4. Effect of soils from Centaurea maculosa- and Euphorbia esula-infested areas and adjacent noninfested areas on 12 d and 24 d seed germination (%) of Centaurea maculosa – CEMA, Euphorbia esula – EUES, Pascopyrum smithii – PASM, and Pseudoroegneria spicata – PSSP. Non-transformed means for germination (%) are presented. Non-transformed least square mean standard errors for the 12 and 24 d site × infested × seeded species interactions are 6.8 and 5.3, respectively. Centaurea site Infested Germination CEMA EUES PASM PSSP
12 d 32.3 0.8 8.3 33.8
Euphorbia site Noninfested
24 d 86.0 14.3 48.3 58.0
12 d 73.5 4.0 36.3 51.0
Infested 24 d 93.3 21.5 60.8 65.3
Litter type did not affect number of leaves of the four species. Overall, the number of leaves on the transplants differed among species; Euphorbia had the most leaves, whereas Centaurea and Pascopyrum had the least (species, P < 0.0001). Soil effect on seed germination Overall, early germination (12 d) on soils from noninfested areas was higher than germination on soils from infested areas (infested, P = 0.02, Table 4), but this differed between soils from the two sites (site × infested, P = 0.01). Seed germination on soils from Centaureainfested areas was much lower than from noninfested areas, whereas the difference was not as great for seed germination on soil from Euphorbia-infested and adjacent noninfested areas. Early germination of the four species differed depending on whether soils were from infested or noninfested areas (species × infested, P = 0.15). Euphorbia germination was similar on infested and noninfested soils. Pascopyrum germination was similar on soils from Euphorbia infested and adjacent noninfested sites. Besides these exceptions, germination of the other species was higher on noninfested soils. Differences in germination 24 d after seeding were not as pronounced as at 12 d, partly because germination of Euphorbia was higher on soils from Euphorbia-infested than adjacent noninfested areas (site × infested, P = 0.04).
Discussion Chemical effect of litter on seedling emergence and roots Leachate of both species, even at full strength, had minimal effect on seed germination. Similarly, aqueous extracts of Euphorbia foliage had minimal effect on germination of Alaskan pea (Pisum sativa L. Alaska CV, Tourneau & Heggeness 1957). In laboratory bioassays, cnicin in Centaurea was phytotoxic toward
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12 d 48.5 7.0 19.0 27.8
Noninfested 24 d 85.3 31.5 53.0 61.3
12 d 58.3 2.5 19.5 42.0
24 d 87.0 14.0 54.5 66.5
native grasses and conifers (Kelsey & Locken 1987), however the major effect was on root growth, not seed germination. Sometimes the effect of a leachate can be species specific. A leachate of litter from the perennial grass Poa pratensis L. reduced germination of Centaurea nigra L. and Dipsacus sylvestris Huds., but did not affect germination of Verbascum thapsus L. and Hypericum perforatum L. (Bosy & Reader 1995). An extract of Setaria sphacelata completely inhibited, and a leachate reduced, germination of the native Sporobolus indicus (Andrew et al. 1997). Apparently, leachate of Euphorbia and Centaurea in our trial was not imbibed and thereby did not cause seed mortality or inhibit germination, but leachate can affect normal seedling development. Our findings agree with Kelsey & Everett’s (1995) suggestion that the mode of action of phytotoxins often interferes with a particular physiological process, and has no effect on germination. For example, root lengths of our seeded species were affected by leachate concentration, but the response differed among species. Root growth of Euphorbia seedlings was actually stimulated at intermediate concentrations. Many secondary compounds stimulate plant growth at low concentrations, but inhibit growth at high concentrations (Stevens & Merrill 1985, Leather & Einhellig 1988). For our other species, roots were shorter at higher leachate concentrations, similar to findings from other studies (Tourneau & Heggeness 1957, Kelsey & Locken 1987). Andrew et al. (1997) found that leachate of Setaria sphacelata reduced shoot and root growth of Sporobolus indicus, but that leachate from Axonopus affinis had no effect. Because of Setaria’s effect on root and shoot growth, they suggested that Setaria would be more resistant to infestation than Axonopus affinis. Like many leachate studies, our leachate trial was highly controlled, lacking soil particles which may adsorb compounds, and microorganisms which may render compounds harmless or use them as a carbon and energy source (Vokou et al. 1984). The value of such
Effects of invasive forb litter on seedlings
bioassays has been questioned (Stowe 1979, Henn et al. 1988), but bioassays may be used to indicate the role of chemical compounds in plant-plant interaction (Kelsey & Everett 1995). However, this role should be validated in the field or at least with natural soils (Kelsey & Everett 1995, Inderjit et al. 1997), as we did with soils collected from infested sites. Physical effect of litter on seed germination and seedling growth Litter reduces irradiance and moderates temperature (Bosy & Reader 1995), especially when litter thickness exceeds a threshold amount. Litter reduced seed germination and survival of the annual weed Cardamine pensylvanica (Molofsky et al. 2000), although their population dynamics model indicated this reduction would not be demographically significant over the long term. In a litter pack study, the physical presence of grass litter reduced seed germination of four different herbs from 14% to 41% (Bosy & Reader 1995). In a field study, litter cover inhibited germination of several forb species, but most seedlings died within the first month, with or without litter cover (Wilby & Brown 2001). In a meta-analysis of 35 independent litter studies, germination and establishment were reduced and aboveground biomass was enhanced by litter in grassland ecosystems (Xiong & Nilsson 1999). Forb litter had a negative effect on all of these variables, whereas the effect of grass litter ranged from neutral (germination) to slightly negative (establishment) to slightly positive (aboveground biomass). Our litter packs did not reduce germination of the seeded species, unlike Bosy & Reader (1995). However, their litter packs contained 715 g m–2, whereas our packs contained 500 g m–2 of Euphorbia litter and 225 g m–2 of Centaurea litter. Thus, we would expect greater interception of light and less germination in Bosy & Reader’s (1995) study compared with ours, especially with Centaurea. They used more plant material in their litter packs because they collected litter from a mesic old-field in eastern Canada. Our litter mass mimicked amounts from less productive, mixed grass prairies in southwestern Montana. Although litter type did not affect seed germination in our study, seedling heights differed among litter types. The tallest seedlings were those covered with Centaurea litter; the shortest were those without litter cover. Most plants exposed to full irradiance do not need to allocate resources to extend shoot growth to compete for light (Lambers et al. 1998), which may explain the latter result. For the same reason, we would have expected Euphorbia litter, with mass greater than twice as much as Centaurea’s litter, to have the tallest seedlings to compete for light, but they
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were shorter than those under the Centaurea litter. The thicker Euphorbia litter may have mechanically prevented seedlings from growing taller, or may have reduced soil temperatures enough to reduce growth rates of seedlings. Mechanical effect of litter on transplant survival and growth In our glass house trial, litter type did not affect survival of the pregerminated seeds of our four species. In a field study, most forb seedlings died within the first month, with or without litter cover (Wilby & Brown 2001). In some systems characterized by low to intermediate levels of productivity, litter may facilitate survival of young seedlings (Foster 1999, Nash Suding & Goldberg 1999), possibly because litter ameliorates abiotic stress at this sensitive life history stage (Callaway & Walker 1997). Litter type affected heights of our seedlings. The tallest seedlings were those without litter cover (NONE). For four different herbaceous species, shoot extension above a layer of litter was reduced 95–100% (Bosy & Reader 1995). These results differed from our seedlings in the physical effects trial where the shortest were those without cover. In that trial, germinating seeds may have received a cue about their light environment immediately, and adjusted growth form accordingly. In our mechanical effects trial, the pregerminated seeds may not have been exposed to an early cue created by litter type, resulting in a different growth response. Soil effect on seed germination Germination was greatest on noninfested soils, except for Euphorbia germination on infested soils from the Euphorbia site. However, germination of Euphorbia was so low that whether infested soils actually “enhanced” germination for this species, or whether these results reflect chance or our relatively small sample size cannot be identified. For the other seeded species, germination was 14 to 26% higher on noninfested soils. Using soil cores in this trial essentially integrates the effects of these invasive forbs on soil properties. Apparently, Euphorbia and Centaurea in some unknown way alter soil physical or chemical properties, which in turn reduces, but does not eliminate, seed germination. Soils infested or amended with chickweed Stellaria media reduced shoot and root growth of wheat Triticum aestivum (Inderjit & Dakshini 1998), although effects on germination were not measured. Compared with seed germination on noninfested soils, soils from infested Centaurea areas reduced seed
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germination more than soils from infested Euphorbia areas. This may reflect the effect of different secondary chemistry or root structure of these two species on soil chemical and physical properties.
Conclusions Does litter from invasive forbs hinder seedling establishment of native species? Our results indicate that litter from these invasive forbs can have subtle effects on growth of seedlings of Pascopyrum and especially Pseudoroegneria, and that these forbs have some, unknown effect on soil properties which reduces germination. Leachate from litter of Euphorbia also had a negative effect on Centaurea. This may partly explain why Euphorbia is currently replacing Centaurea in western Montana, which has displaced the native Pseudoroegneria on many sites. The “negative” effects of Centaurea litter on Centaurea seedlings, or autotoxicity, may synchronize germination with the wettest season, or minimize effects of intraspecific competition which may actually benefit Centaurea at the population level (Kelsey & Everett 1995). Physical and mechanical effects associated with Euphorbia and Centaurea litter were more subtle than chemical effects, and probably are not specific to invasive forbs. For example, thick grass litter (Poa pratensis L.) reduces germination and shoot extension of several forbs (Bosy & Reader 1995). Many of the litter effects in this controlled glass house study were subtle. In a meta-analysis of 35 independent studies, plant responses were more affected by litter in field than in glasshouse studies (Xiong & Nilsson 1999), suggesting effects of our invasive forb litter could be greater in the field. This is supported by reduced seed germination, except for Euphorbia, on soils collected from infested sites. Litter of Euphorbia and Centaurea in mixed grass prairies may accumulate simply because they are not grazed by the dominant large herbivores, cattle and horses. Using sheep or goats to graze these weeds (Olson 1999), or prescribed fire periodically will reduce litter accumulation and any associated physical, mechanical and chemical litter effects on native species establishment.
Acknowledgements. This study was supported by the USDA-CSREES and the Montana Agricultural Experiment Station. We thank K. Olson-Rutz for reviewing the manuscript. Published with approval of the Director, Montana Agricultural Experiment Station, as Journal No. J-2000-42.
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References Andrew TS, Jones CE, Whalley RDB (1997) Factors affecting the germination of Giant parramatta grass. Australian Journal of Experimental Agriculture 37: 439–446. Bakke AL (1936) Leafy spurge, Euphorbia esula L., Iowa Agricultural Experiment Station Research Bulletin 198: 209–246. Best KF, Bowes GG, Thomas AG, Maw MG (1980) The biology of Canadian weeds. 39. Euphorbia esula L. Canadian Journal of Plant Science 60: 651–663. Bosy JL, Reader RJ (1995) Mechanisms underlying the suppression of forb seedling emergence by grass (Poa pratensis) litter. Functional Ecology 9: 635–639. Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78: 1958–1965. Chicoine TK, Fay PK, Nielsen GA (1985) Predicting weed migration from soil and climate maps. Weed Science 34: 57–61. Clements FE (1916) Plant succession. Carnegie Institute of Washington. Pub 242. Evans FJ, Kinghorn AD (1977) A comparative phytochemical study of the diterpenes of some species of the genera Euphorbia and Elaeophorbia (Euphorbicaceae). Botanical Journal of the Linnaean Society 74: 23–27. Facelli JM, Pickett STA (1991) Plant litter: its dynamics and effects on plant community structure. The Botanical Review 57: 1–32. Foster BL (1999) Establishment, competition and the distribution of native grasses among Michigan old-fields. Journal of Ecology 87: 476–489. Gill JL (1981) Evolution of statistical design and analysis of experiments. Journal of Dairy Science 64: 1494–1519. Henn H, Petit D, Vernet P (1988) Interference between Hieracium pilosella and Arrhenatherum elatius in colliery spoils of north France. Oecologia 76: 268–272. Inderjit, Dakshini KMM (1998) Allelopathic interference of chickweed Stellaria media with seedling growth of wheat (Triticum aestivum). Canadian Journal of Botany 76: 1317– 1321. Inderjit, del Moral R (1997) Is separating resource competition from allelopathy realistic? Botanical Review 63: 221–230. Inderjit, Muramatsu M, Nishimura H (1997) On the allelopathic potential of certain terpenoids, phenolics, and their mixtures, and their recovery from soil. Canadian Journal of Botany 75: 888–891. Kelsey RG, Everett RL (1995) Allelopathy. In: Bedunah D, Sosebee R (eds) Wildland Plants: Physiological Ecology and Developmental Morphology. Society for Range Management, Denver, Colo, pp. 479–549. Kelsey RG, Locken LJ (1987) Phytotoxic properties of cnicin, a sesquiterpene lactone from Centaurea maculosa (spotted knapweed). Journal of Chemical Ecology 13: 19–33. Kucera CL, Dahlman RC (1967) Total net productivity and turnover on an energy basis for tallgrass prairie. Ecology 48: 536–541.
Effects of invasive forb litter on seedlings Lacey JR (1989) A complete takeover by knapweed in 2001? Montana Farmer-Stockman 70: 32–34. Lambers H, Chapin FS, Pons TL (1998) Plant Physiological Ecology. Springer, New York. Lajeunesse S, Sheley R, Lym R, Cooksey D, Duncan C, Lacey J, Rees N, Ferrell M (1997) Leafy spurge: biology, ecology and management. Montana State University Extension Service EB-134. Laycock WA (1991) Stable states and thresholds of range condition on North American rangelands: a viewpoint. Journal of Range Management 44: 427–433. Leather GR, Einhellig FA (1988) Bioassay of naturally occurring allelochemicals for phytotoxicity. Journal of Chemical Ecology 14: 1821–1828. Molofsky J, Lanza J, Crone EE (2000) Plant litter feedback and population dynamics in an annual plant, Cardamine pensylvanica. Oecologia 124: 522–528. Mufti MM, Sydes CL, Furness SB, Grime JP, Band SR (1977) A quantitative analysis of shoot phenology and dominance in herbaceous vegetation. Journal of Ecology 65: 759– 791. Nash Suding K, Goldberg DE (1999) Variation in the effects of vegetation and litter on recruitment across productivity gradients. Journal of Ecology 87: 436–449. Olson BE (1999) Grazing and weeds. In: Sheley R, Petroff J (eds) Biology and management of noxious rangeland weeds. Oregon State University Press, Corvallis, pp 85–96. Olson BE, Kelsey RG (1997) Effect of Centaurea maculosa on sheep rumen microbial activity and mass. Journal of Chemical Ecology 23: 1131–1144. Pimm SL (1993) Biodiversity and the balance of nature. In: Schulze E-D, Mooney HA (eds) Biodiversity and Ecosystem Function. Springer-Verlag, Berlin, pp 347–359. Rietkerk M, van de Koppel J (1997) Alternate stable states and threshold effects in semi-arid grazing systems. Oikos 79: 69–76. Ridenour WM, Callaway RM (2001) The relative importance of allelopathy in interference: the effects of an invasive weed on a native bunchgrass. Oecologia 126: 444–450.
317
Roberts J, Olson BE (1999) Effect of Euphorbia esula on sheep rumen microbial activity and mass in vitro. Journal of Chemical Ecology 25: 297–314. SAS (1988) Statistical Analysis System. SAS Institute, Inc. Raleigh, North Carolina. Schlatterer EF, Tisdale EW (1969) Effects of litter of Artemisia, Chrysothamnus and Tortula on germination and growth of three perennial grasses. Ecology 50: 869–873. Sokal RR, Rohlf FJ (1995) Biometry, 3rd Edition. W.H. Freeman and Co. New York. Stevens KL, Merrill GB (1985) Sesquiterpene lactones and allelochemicals from Centaurea species. In: Thompson A (ed) The Chemistry of Allelopathy. ACS Symposium Series 268., American Chemical Society, Washington, DC, pp 83–98. Stowe LG (1979) Allelopathy and its influence on the distribution of plants in an Illinois old-field. Journal of Ecology 67: 1065–1085. Tourneau DL, Heggeness HG (1957) Germination and growth inhibitors in leafy spurge foliage and quackgrass rhizomes. Weeds 5: 12–19. Vokou D, Margaris NS, Lynch JM (1984) Effects of volatile oils from aromatic shrubs on soil microorganisms. Soil Biology and Biochemistry 16: 509–513. Weigelt A, Steinlein T, Beyschlag W (2002) Does plant competition intensity rather depend on biomass or on species identity? Basic and Applied Ecology 3: 85–94. Westoby M, Walker B, Noy-Meir I (1989) Opportunistic management for rangelands not at equilibrium. Journal of Range Management 42: 266–274. Wilby A, Brown VK (2001) Herbivory, litter and soil disturbance as determinants of vegetation dynamics during oldfield succession under set-aside. Oecologia 127: 259– 265. Xiong S, Nilsson C (1999) The effects of plant litter on vegetation: a meta-analysis. Journal of Ecology 87: 984–994. Zobel M (1997) The relative role of species pools in determining plant species richness: an alternative explanation of species coexistence. Trends in Ecology and Evolution 12: 266–269.
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