Plant Ecol DOI 10.1007/s11258-011-9943-x
Disturbance of biological soil crust increases emergence of exotic vascular plants in California sage scrub Rebecca R. Hernandez • Darren R. Sandquist
Received: 22 November 2010 / Accepted: 18 June 2011 Ó Springer Science+Business Media B.V. 2011
Electronic supplementary material The online version of this article (doi:10.1007/s11258-011-9943-x) contains supplementary material, which is available to authorized users.
In a separate germination study, seed fate in disturbed BSC cores was compared to seed fate in undisturbed BSC cores for three exotic and three native species. In the field, disturbed BSCs had significantly ([39) greater exotic plant emergence than in undisturbed BSC, particularly for annual grasses. Native species, however, showed no difference in emergence between disturbed and undisturbed BSC. Within the disturbed treatment, emergence of native plants was significantly, and three times less than that of exotic plants. In the germination study, seed fates for all species were significantly different between disturbed and undisturbed BSC cores. Exotic species had greater emergence in disturbed BSC, whereas native plants showed either no response or a positive response. This study demonstrates another critical ecosystem service of BSCs—the inhibition of exotic plant species—and underscores the importance of BSC conservation in this biodiversity hotspot and possibly in other aridland ecosystems.
R. R. Hernandez (&) D. R. Sandquist Department of Biological Science, California State University, Fullerton, CA 92831, USA e-mail:
[email protected]
Keywords Alien grasses Biological soil crust Exotic plant invasion Germination Mediterranean shrublands Sage scrub
Present Address: R. R. Hernandez Department of Environmental Earth System Science, Stanford University, Stanford, CA 94305, USA
Introduction
R. R. Hernandez Department of Global Ecology, Carnegie Institution for Science, Stanford, CA 94305, USA
Biological soil crusts (BSCs) are delicate ecological structures comprised of assemblages of soil particles;
Abstract Biological soil crusts (BSCs) are comprised of soil particles, bacteria, cyanobacteria, green algae, microfungi, lichens, and bryophytes and confer many ecosystem services in arid and semiarid ecosystems worldwide, including the highly threatened California sage scrub (CSS). These services, which include stabilizing the soil surface, can be adversely affected when BSCs are disturbed. Using field and greenhouse experiments, we tested the hypothesis that mechanical disturbance of BSC increases emergence of exotic vascular plants in a coastal CSS ecosystem. At Whiting Ranch Wilderness Park in southern California, 22 plots were established and emergence of exotic and native plants was compared between disturbed and undisturbed subplots containing BSC.
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microscopic bacteria, cyanobacteria, fungi, and green algae; and macroscopic bryophytes and lichens. BSCs are found within or on top of undisturbed soil surfaces in arid and semiarid habitats worldwide. Recently, there is increasing awareness of the importance of BSCs because of their many ecosystem services, including their prevention of erosion, influence on soil hydrologic properties, and augmentation of soil fertility (Belnap and Lange 2003; Belnap and Harper 1995). Another critical biological service of BSCs may be their inhibition of exotic vascular plant germination and establishment (Belnap et al. 2003). Previous studies have found that the effect of BSCs on vascular plants may be positive or negative depending on the plant species or functional type. This variability has led to speculation about coevolutionary relationships between BSC and native plants that show a favorable response to BSC presence (Eckert et al. 1986; Bashkin et al. 2003; Belnap et al. 2003). For example, the presence of late-successional BSC deterred root penetration of the noxious exotic annual grass Bromus tectorum more than for native annual grass Vulpia microstachys (Dienes et al. 2007). Similarly, Belnap et al. (2003) noted that many desert natives have seeds with selfburial mechanisms (e.g., hygroscopic awns) that can penetrate BSC—a characteristic that exotic desert species, especially annuals, often lack, but when present (e.g., Erodium spp.), require surface crevices or ‘cracks’ to establish (Stamp 1984; Larsen 1995; Howell 1998). In that vein, it has been proposed that disturbance of BSC may facilitate germination and establishment of certain exotic plant species that have not coevolved with BSCs (Stohlgren et al. 2001; Warren and Eldridge 2003). The effects of BSC on seedbed characteristics are many, thus it is not surprising that they have both positive and negative effects on seedling germination and establishment (Belnap et al. 2003). In aridland ecosystems, one of the more important benefits conferred to seedbeds by BSCs is higher soil water balance, which may help fulfill germination imbibition requirements of seeds, regardless of functional type (Brotherson and Rushforth 1983; Campbell et al. 1989; Gold and Bliss 1995; Fierer and Gabet 2002). BSCs also influence soil surface roughness, or microtopography, which increases as BSCs develop successionally. Microtopography directly influences
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microsite fertility owing to the trapping of organic matter, longer residence time of water, and greater collection of soil fines, all of which may positively affect emergence (Eckert et al. 1986; Barger 2003; Belnap et al. 2003; Dienes et al. 2007). The adverse effects of BSCs may stem from their influence on soil pH and production of secondary compounds (e.g., metabolites or hormones), either of which can reduce or inhibit germination and growth in certain plants (Miller et al. 1963; Pyatt 1967; Rundel 1978; Lawrey 1986; Garcia-Pichel and Belnap 1996; Fisher 1979; Belnap et al. 2003). BSC microcanopies (lichen thalli, and bryophyte gametophytes and sporophytes) can have a negative effect by increasing the time a seed spends above ground and preventing burial. Seeds lacking adaptations, such as burial mechanisms or endozoochory, might then be subject to desiccation or predation by granivores (Boeken and Shachak 1994; Stohlgren et al. 2001; Morgan 2006). Disturbance of BSCs can enhance emergence of some species, especially exotics, and a number of different mechanisms for this observation have been proposed (Belnap et al. 2003). Among the most likely is that disturbance liberates nutrients locked up in BSCs while concomitantly reducing competition with BSCs for water, nutrients, space, and light (Belnap et al. 2003; Serpe et al. 2006). Therefore, BSCs may function as a barrier to exotic plant invasions simply by preempting resource availability (Beymer and Klopatek 1991; Stohlgren et al. 2001; Belnap et al. 2003). In the Great Basin, for example, the number of cracks in BSC is used to predict Bromus tectorum invasion (Harper et al. 1965; Evans and Young 1984). Disturbance also increases the probability that soil particles can be dislodged by rain splash, which may enhance germination by partially covering seeds and preventing desiccation (McIlvanie 1942; Dienes et al. 2007). Although these soil disturbances might also enhance opportunities for native plants, exotic annual grasses have been shown to germinate earlier and grow more rapidly than natives under such conditions (D’Antonio and Vitousek 1992; Larsen 1995). Regardless of the mechanism, disturbance of BSC appears to enhance emergence of exotic plants and may help them to out-compete natives, particularly in low-nutrient ecosystems like CSS (Hobbs and Atkins 1988; D’Antonio and Vitousek 1992; Padgett and Allen 1999).
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To our knowledge, studies of seedling emergence from naturally occurring propagule sources (e.g., seed rain) following disturbance of BSCs at the community level are limited (Belnap 1995), and few studies have been specifically designed to test the effects of BSC disturbance on exotic plant emergence. These studies generally show an inhibitory effect of BSCs on exotic plant germination, but they are limited to individual species (McIlvanie 1942; Eckert et al. 1986; Crisp 1975; Larsen 1995; Howell 1998; Kaltenecker et al. 1999; Morgan 2006; Serpe et al. 2006; Dienes et al. 2007) or correlations based on observations at the landscape-scale (Stohlgren et al. 2001; Bashkin et al. 2003). In this study, we examined relationships between BSC disturbance and vascular plant emergence in California sage scrub (CSS), a highly biodiverse (Myers et al. 2000) and semiarid ecosystem in which BSCs are largely understudied. Well-developed BCSs are an important component of CSS communities throughout southern California; however, in many areas, exotic plant species, particularly annual grasses, have colonized these communities and altered their composition, structure, and function (D’Antonio and Vitousek 1992; Padgett and Allen 1999; Talluto and Suding 2008). Using a field manipulation and germination experiment, we tested the hypotheses that (1) disturbance of BSC in CSS increases emergence of exotic vascular plants, and (2) intact BSCs engender the microenvironment more suitable for recruitment of native vascular plants. Given the threats that invasive species pose worldwide, and specifically to the California Floristic Provence biodiversity hotspot, this study will provide valuable knowledge of the potential role played by BSCs in regulating plant invasion, and of their fundamental importance in CSS ecosystems.
Methods Study site The study was conducted within coastal CSS stands at Whiting Ranch Wilderness Park, in Lake Forest, California (Fig. 1) at elevations ranging from 307 to 461 m above sea level (United States Geological Survey 2006). The Park encompasses 16.8 km2 of coastal CSS, chaparral, and oak and riparian
woodlands. Precipitation averages around 327 mm per year, occurring primarily between November and April. Typically, maximum temperatures occur in August, 22.3 ± 0.4°C (95% CI) with minimum temperatures occurring in January and rarely below freezing, 11.93 ± 0.3°C (95% CI; 1902–2003, Tustin Irvine Ranch, CA Station #049087, Western Regional Climate Center). Soils include well-drained Cieneba sandy loams and Calleguas and Balcon clay loams with other series in less abundance (United States Department of Agriculture—Natural Resource Conservation Service Soil Survey 2007). Where the soil is undisturbed and conditions favorable, rugose latesuccessional BSCs with a low microtopography (\3 cm) typically develop. These BSCs support a scattered mosaic (1 cm2 \ clumps \ 1 m2, pers. obs.) of bryophytes and lichens (Fig. 2) in addition to the abundant primary matrix of early successional BSC constituents (i.e., bacteria, cyanobacteria, green algae, and microfungi).
Field experiment Twenty-two field plots, each plot comprised of two paired subplots (30 9 30 cm2 = 900 cm2) separated by a 10-cm buffer, were established throughout Whiting Ranch Wilderness Park in August 2006 based on the criteria that plots (1) contained [60% rugose/late-successional BSC cover; (2) were in the interspaces of shrubs; (3) showed no evidence of recent human disturbance (e.g., clearing, footprints); and (4) contained \5% exotic plant cover. Plots encompassed a large degree of the heterogeneity of the Park, varying in their elevation, aspect, slope, distance to nearest trail, and soil properties (see Table S1 in Supplementary Material). Precipitation and temperature data were drawn from Tustin Irvine Ranch climate station. Prior to treatment, a 900 cm2 grid, subdivided into twenty-five 36 cm2 square cells, was placed over each subplot. Percent BSC cover and exotic plant cover were quantified visually for each cell (0–1%) and percent cover for the 25 cells was summed to derive total percent cover for each subplot. Within each plot, one randomly chosen subplot was physically disturbed in August 2006 by repeatedly stepping, within subplot boundaries, 60 times by a 84 kg human (emulating off-trail use by human hikers;
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Fig. 1 Map of paired study plots (aerial photograph) in Whiting Ranch Wilderness Park (left polygon), located in Lake Forest (star), Orange County (shaded region) California
Fig. 2). This disturbance equaled compression of *200 g cm2 and caused homogenization of mineral soil and BSC to a depth of *3 cm. After the disturbance treatment, emergence of native and exotic plant seedlings was recorded in plots every 30 days from January (i.e., December emergence) to July 2007 (i.e., June emergence) and without stepping within plot boundaries. During the study, one plot was damaged and therefore removed from the study. Upon emergence, the location of each seedling was mapped, using the aforementioned 36-cell grid, and identified to genus and when possible to species. Preexisting seedlings and seven seedlings that could not be identified were left out of analyses. Subplot emergence data were paired for analyses but lacked normality and homogeneous variances. Consequently, a Wilcoxon-signed rank analysis (non-parametric, JMP 5.0, SAS Institute Inc., Cary, NC) was used to test hypotheses and specifically, determine monthly and total differences in vascular plant emergence between disturbed and undisturbed BSC sublots.
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Germination experiment In a separate study, a controlled experiment was used to evaluate the effect of BSC disturbance on emergence of three exotic and three native plant species. Seventy-two cores (*2.0 cm depth) of intact rugose/ late-successional BSC were taken from 6 sites (12 cores per site) within CSS stands at Whiting Ranch Wilderness Park. Modified soil tins (diameter 7.75 cm, depth 4.70 cm, bottoms removed) were pushed into BSC and extracted with mineral soil and BSC intact. The lid, with four 0.15 cm holes for drainage, was placed on the bottom of the tin to retain the BSC core. Half of the number of cores (randomly chosen by site) were left intact and half were disturbed with a spade. Disturbance included homogenizing the soil by breaking up all BSC components for 1 min and compressing the soil at 200 g cm-2. Twenty seeds of a single plant species were placed on an individual BSC core. There were six replicates for each soil treatment and species. Replicates included BSC cores from all six sites. Native species
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2008. Cores did not dry out between watering. BSC cores were arrayed in a 5 9 15 matrix and their location in the array was randomized every 5 days. Microclimate data were collected at 1.2 m height above the mist bench using a HOBO Pro-Series Datalogger (Onset Computer Corporation, Bourne, MA). Cores were examined daily and emerging seedlings, defined by the presence of the radicle or cotyledon, were flagged and recorded. During this experiment, seeds were unprotected from avian granivory and wind. Seeds remaining in each BSC core were counted mid-way through the experiment and again at the end. Seed fate was identified as either emerged, missing (due to wind or granivory), or not emerged. BSC cores were examined carefully to account for buried seeds and none were found. A contingency analysis (JMP 5.0, SAS Institute Inc., Cary, NC) was used to determine if seeds in disturbed BSC had significantly different seed fates than seeds in undisturbed BSC for each species.
Results Field experiment Fig. 2 a Field plot showing disturbed and undisturbed biological soil crust subplots (30 9 30 cm2 = 900 cm2) in coastal California sage scrub interspaces; b rugose/latesuccessional biological soil crust in subplot at Whiting Ranch Wilderness Park in Lake Forest, CA
included a perennial grass, Nassella pulchra (Hitchc.) Barkworth (Poaceae), an annual forb, Lepidium lasiocarpum Nutt. (Brassicaceae), and a perennial shrub, Artemisia californica Less. (Asteraceae). Exotic species were the three most abundant invasive plants in the Park (pers. obs.), a perennial grass, Pennisetum setaceum (A. Forsk.) Chiov. (Poaceae), an annual forb, Brassica rapa L. (Brassicaeae), and an annual grass, Bromus madritensis ssp. rubens L. (Poaceae). All seeds were collected from local stands of CSS. For all species, germination or viability of seeds exceeded 75% (for viability details see Hernandez 2009). BSC cores were placed on a mist bench in an unobstructed outdoor area and watered with approximately 0.5 mm of fine mist (*0.2 ml per tin; Serpe et al. 2006) daily from November 2007 to January
Prior to the disturbance treatment, observations showed disturbed and undisturbed subplots had a mean rugose/late-successional BSC cover of 90.2 ± 2.3% (±1 SE) and 88.7 ± 2.1%, respectively, and were not significantly different (P = 0.56, paired Student’s t test). Mean exotic plant cover prior to disturbance was 0.20 ± 0.2% (±1 SE) for disturbed subplots and 0.22 ± 0.1% for undisturbed subplots, and did not significantly differ (P = 0.93, paired Student’s t test). Native plant species observed within plots were mapped and included Artemisia californica (n = 21), Eriogonum fasciculatum (n = 4), and Mimulus aurantiacus (n = 3) seedlings. Mean emergence of exotic vascular plants after plot establishment was significantly greater in disturbed BSC subplots, 35.5 ± 10.1 (±1 SE) seedlings m-2, than in subplots containing intact BSC, 10.6 ± 4.7 seedlings m-2 (P \ 0.018, Fig. 3). For native vascular plants, total mean emergence did not statistically differ between disturbed and undisturbed BSC, 11.1 ± 3.3 seedlings m-2 versus 13.2 ± 4.2 seedlings m-2, respectively (P = 0.691, Fig. 3).
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Fig. 3 Total emergence of exotic and native vascular plants in subplots containing rugose/late-successional biological soil crust that were disturbed or left undisturbed in a California coastal sage scrub community. Emergence occurred from December 2006 to July 2007. Letters represent significantly different means at the P \ 0.05 level (n = 21, Wilcoxonsigned rank test). Error bars are ±1 standard error
Comparisons within treatments found that in disturbed BSCs, exotic emergence was significantly greater than native emergence (P \ 0.011), whereas in undisturbed BSCs, exotic, and native emergence did not significantly differ (P = 0.562, Fig. 3). Emergence of exotic vascular plants was numerically greater in disturbed BSC subplots compared to undisturbed BSC subplots across all months in which seedlings were observed (Fig. 4). This difference, however, was significant only in the month of December (P \ 0.037, Wilcoxon-signed rank test), the first month of substantial precipitation and the month with the greatest precipitation (Fig. 5). Native plant species showed no significant difference in emergence between disturbed and undisturbed subplots in the months that germination was recorded (Fig. 4). For both natives and exotics, no emergence was observed from May to July, months in which no precipitation occurred. Total exotic plant species richness was six for disturbed and five for undisturbed BSC subplots (Fig. 6). The exotic annual grasses Avena barbata (Poaceae), Avena fatua (Poaceae), and Bromus madritensis ssp. rubens, had the greatest numerical emergence among all taxa and across all treatments,
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Fig. 4 Monthly emergence of exotic and native plant species in subplots containing rugose/late-successional biological soil crust that were disturbed or left undisturbed in a California sage scrub community at Whiting Ranch Wilderness Park. A significantly greater emergence was seen only in the December period for exotic plants in disturbed BSC subplots (P \ 0.05 denoted by asterisk, n = 21, Wilcoxon-signed rank test). Error bars are ±1 standard error
Fig. 5 Monthly observed precipitation (mm) for the 2006–2007 growing season (dark gray) and long-term average (light gray) from 1902 to 2003 at Whiting Ranch Wilderness Park, Lake Forest, California. Total observed precipitation (87.4 mm) was 25% of the long-term average. Data collected from Tustin Irvine Ranch Climate Station (Irvine, California, 15.9 km from study plots)
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with greatest emergence in disturbed BSC subplots. For one of these species, Avena fatua, emergence was significantly less in undisturbed BSC subplots than disturbed BSC subplots (P \ 0.025, Wilcoxon-signed rank test, Fig. 6). Three other exotic species had greater numbers in disturbed BSC subplots than in undisturbed subplots: Anagallis arvensis (Myrsinaceae), Brassica rapa (Brassicaceae), and Crassula tillaea (Crassulaceae), albeit not statistically greater. Marrubium vulgare (Lamiaceae), an exotic perennial, was only observed in undisturbed BSC. Total native species richness was five in disturbed subplots and six in undisturbed BSC subplots (Fig. 6). In undisturbed BSC subplots, the dominant native plants found were the common CSS shrub Artemisia californica and species in the Liliaceae family. Native emergence was greater, although only numerically, in undisturbed BSC for the parasitic vine Cuscuta sp. (Cuscutaceae) and the perennial shrub Mimulus aurantiacus (Scrophulariaceae). Germination experiment Temperature and humidity conditions throughout the germination experiment were similar to long-term means in nearby CSS habitat between December and March. Mean daily temperature was 12.4°C and ranged from 8.1 to 18.4°C, whereas mean daily relative humidity was 61.2% and ranged from 23.8 to 89.8% (Fig. 7). In the germination study, seed fate (emerged, missing, or not emerged) was compared between disturbed and undisturbed BSC. Missing seeds resulted from granivory by birds and loss due to wind, thus the total number of seeds available for emergence varied among species and treatments (Table 1). Seed fates of the three exotic vascular plant species, Brassica rapa, Bromus madritensis ssp. rubens, and Pennisetum setaceum, differed significantly between disturbed and undisturbed BSC cores (P \ 0.0001, Fig. 8). Percent emergence of seeds remaining for all three exotic species (Table 1) was greater in disturbed than in undisturbed BSC cores by 39.9% for B. rapa, 29.2% for B. madritensis ssp. rubens, and 10.8% for P. setaceum. The percentage of seeds missing for all three exotic species was greater in undisturbed than in disturbed BSC cores (Fig. 8). For B. madritensis ssp. rubens, seed loss was relatively low (1.7 ± 0.3% in
disturbed BSC and 5.8 ± 0.7% in undisturbed BSC). A high percentage of seeds were missing for both B. rapa and P. setaceum, especially in the undisturbed BSC cores. Sixty-four percent ±4.3 of B. rapa seeds were missing in undisturbed BSC cores and 40.5 ± 3.4% were missing from disturbed soil crusts. Similarly high numbers of seeds were missing for P. setaceum—69.2 ± 1.4% (the greatest amount for all species) and 31.7 ± 2.6%, respectively. Seed fates differed significantly between disturbed and undisturbed BSC cores for two of the three native species tested, Lepidium lasiocarpum (P \ 0.0134) and Nassella pulchra (P \ 0.0005, Fig. 8). Seed fate data for Artemisia californica was not analyzed as almost all seeds were missing (Table 1), but of those remaining (n = 3), all emerged. Percent emergence of the native annual L. lasiocarpum was greatest among all species in both undisturbed BSC cores and disturbed BSC cores (Table 1). In contrast, emergence of N. pulchra was among the lowest of all species in both disturbed and undisturbed BSC cores (Table 1). Percent seed loss differed by species and treatment for native plants. For L. lasiocarpum, slightly more seeds were missing in disturbed BSC than in undisturbed BSC, 27.5 ± 2.5 and 24.2 ± 1.4%, respectively (Fig. 8). The difference for N. pulchra was in the opposite direction—more seeds were missing on undisturbed BSC (16.7 ± 0.8%) than on disturbed BSC (5.8 ± 0.5%).
Discussion Seedling emergence following field disturbance of biological soil crust Disturbance of biological soil crusts (BSCs), emulating human trampling, significantly increased total emergence of exotic vascular plants in this CSS ecosystem. Emergence of exotics was also significantly greater than that of native plants indicating that modest disturbance of BSCs has the potential to alter species composition in this community by increasing the establishment of exotic plants. In this study, species with greatest emergence were exotic annual grasses indigenous to the Mediterranean Basin: Avena barbata, Avena fatua, and Bromus madritensis ssp. rubens. Therefore, the structure of this plant community may also be altered by disturbance of
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Plant Ecol Fig. 6 Mean emergence of exotic and native vascular plant species between disturbed and undisturbed biological soil crust subplots (P \ 0.05 denoted by asterisk, n = 21, Wilcoxon-signed rank test). Error bars are ±1 standard error. ^Plants listed as ‘‘Liliaceae’’ are one of the following: Calochortus splendens, C. catalinae, C. plummerae, or Dichelostemma capitatum
BSCs, shifting from perennial shrubland to annual grassland—a conversion that has been shown to modulate ecosystem and global-level functions (D’Antonio and Vitousek 1992; Vitousek et al. 1996; Stylinski and Allen 1999). Disturbance of BSCs also produced species-specific effects on the emergence of native dominant perennials that comprise the bulk of CSS biomass. For example, emergence of Artemisia californica, the indicator species for CSS, was six times greater in intact BSC than in disturbed BSC, paralleling the
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observation that well-developed BSCs are often found in association with Artemisia shrub canopies here (pers. obs.) and in the Great Basin (Serpe et al. 2006). In contrast, Lotus scoparius, a native perennial found in abundance in ruderal sites had a greater number of individuals emerge in disturbed BSC compared to undisturbed subplots, however, this is not surprising given this plant’s ‘early succession’ life history characteristics (Hickman 1993). The observation that BSC disturbance favors exotic plant emergence whereas overall native plant
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Fig. 7 Mean daily temperature (black line) and relative humidity (gray line) during germination experiment
emergence is proportionally greater on intact BSCs may be explained by three general hypotheses: (1) native plants have adaptive traits that enhance their emergence on BSC; (2) exotic plants lack such traits because they have no evolutionary relationship with BSCs; and (3) exotic, and particularly invasive, plants have adaptive traits that increase their emergence on disturbed soils (e.g., utilizing resources at a faster rate than native plant species; Jackson 1985; Kaltenecker et al. 1999; Stohlgren et al. 2001; Belnap et al. 2003). Table 1 Mean emergence (±1 SE; n = 6), total emergence, and total seeds per treatment for three exotic (E) and three native (N) vascular plant species on undisturbed and disturbed biological soil crusts
Class
Species
E, A
Brassica rapa
Native plant traits that facilitate emergence on BSC include both morphological and physiological characteristics (Belnap et al. 2003). Examples of morphological traits known to enhance emergence on BSC include: burial mechanisms, myxospermy (production of mucilaginous seeds) dispersal by animal consumption (e.g., endozoochory), and abiotic dispersal mechanisms, such as anemochory (wind) and hydrochory (water) (Crisp 1975; Boeken and Shachack 1994; Zaady et al. 1997; Howell 1998; Prasse and Bornkamm 2000; Belnap et al. 2003; Li et al. 2005). In CSS, dispersal by wind, runoff, and gravity appear to be more prevalent than other dispersal mechanisms (Keeley 1991; Boeken and Shachack 1994; Li et al. 2005) and may be adaptive in the presence of BSC. Physiological traits may also promote native seed emergence on crusts, as BSCs alter microsite conditions in many ways that interact with the physiological requirements for germination. For example, BSC increases soil surface temperatures (Gold and Bliss 1995), modifies run-off patterns and microtopography (Maestre et al. 2002), increases nutrient levels (Evans and Ehleringer 1993; Belnap et al. 2003), alters light quality and the microcanopy (Dienes et al. 2007), changes soil chemical properties (e.g., pH; GarciaPichel and Belnap 1996; Belnap et al. 2003), and produces secondary compounds (Fisher 1979; Pyatt 1967; Lawrey 1986;). Individually or collectively, these conditions may inhibit or decrease emergence in exotic species not adapted to such distinctive seedbed characteristics (Stohlgren et al. 2001; Morgan 2006; Serpe et al. 2006).
Treatment
Disturbed
Total emergence
Total seeds
46.3 ± 2.6
56
Undisturbed
6.4 ± 0.9
8
72 45
E, A
Bromus madritensis
Disturbed Undisturbed
65.8 ± 1.7 36.7 ± 2.0
79 44
121 113
E, P
Pennisetum setaceum
Disturbed
15.8 ± 1.3
19
82
N, P
Artemisia californica
Undisturbed Species are classified as annuals (A) or perennials (P). Total seeds varied across species and treatments due to seed losses during experiment (see Results)
Emergence (%)
N, A
Lepidium lasiocarpum
N, P
Nassella pulchra
5.0 ± 0.6
6
37
Disturbed
100.0 ± 0.0
2
2
Undisturbed
100.0 ± 0.0
1
1
70.8 ± 2.4
85
87
Undisturbed
65.0 ± 1.1
78
91
Disturbed
20.8 ± 1.0
25
113
6.7 ± 0.8
8
100
Disturbed
Undisturbed
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Plant Ecol Fig. 8 Fates of seeds [emerged (black bars), missing (gray bars), not emerged (white bars)] on disturbed and undisturbed biological soil crust cores for three exotic (a–c) and three native (d–f) species in the germination experiment. Seed fates were significantly different for all exotic species (P \ 0.0001, Contingency analysis) and for two of the three native species tested, L. lasiocarpum (P \ 0.0134) and N. pulchra (P \ 0.0005, Contingency analysis). Seed fate data for A. californica was not analyzed
Alternatively, exotic plant species may have traits that increase germination success in disturbed sites. A majority of the exotic grasses and forbs that are invasive in southern California plant communities originated in habitats with longstanding disturbance regimes implemented by humans, domesticated livestock, and native animals (e.g., Mediterranean Basin). As such, they typically have a syndrome of traits, such as epizoochory (dispersal of propagules by transport on animal surfaces) observed in Bromus caryopses, which are adaptive in the presence of these disturbance regimes (Jackson 1985; D’Antonio and Vitousek 1992; Belnap et al. 2003). In contrast, most CSS native species are not adapted to mechanical disturbances (e.g., off-road vehicles, foot, and bike traffic) and therefore may be at a competitive disadvantage under these conditions (Keeley 1991; Belnap et al. 2003). Effects of BSC disturbance on seed fate of exotics versus natives For all exotic species used in the greenhouse portion of this study (Brassica rapa, Bromus madritensis ssp. rubens, and Pennisetum setaceum), percent
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emergence was greater in disturbed BSC cores than in intact cores. As annual grasses are often effective primary colonizers after disturbance (D’Antonio and Vitousek 1992), it is not surprising that the annual grass B. madritensis ssp. rubens had the greatest percent emergence in disturbed BSC cores among all exotic species and treatments. In the germination experiment, seeds of B. rapa showed 40% greater emergence in disturbed BSC cores than undisturbed cores—the greatest disparity among all species. In contrast to disturbed BSCs, intact BSC appeared to inhibit exotic seedling establishment. When B. madritensis ssp. rubens and B. rapa seeds germinated on intact crust, we observed radicle growth pushing the seed away from the seedbed for 2–3 and 1–2 days, respectively, after which the radicle finally penetrated through the BSC. This soil/root interaction was also observed by Dienes et al. (2007), and merits further investigation. Seed loss, due to wind and granivory, varied by species and across treatments. The least seed loss was for B. madritensis ssp. rubens, whose seeds were not eaten by birds (pers. obs.). In contrast, seed loss was very high for P. setaceum and B. rapa, especially on undisturbed BSC. The latter two results support
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Stohlgren et al. (2001) who suggested that undisturbed BSC might actually increase seed apparency and granivory for exotic species, thereby reducing their establishment. The late-successional BSC used in this study confer an array of green and brown colors and when misted become more verdant. In contrast, seeds of P. setaceum and B. rapa are yellow and dark brown, respectively, and visually stand out against the green crust, as did the light beige seeds of B. madritensis ssp. rubens. Disturbed crusts, on the other hand, were mixed with mineral soil and became lighter and sand-colored. Consequently, all exotic seeds appeared less conspicuous to the human eye in disturbed BSC cores. These seeds on undisturbed BSC might be even more apparent to avian predators that can see twice the number of colors as do trichromatic human eyes (Goldsmith 1980). Significant differences in seed fate between disturbed and undisturbed BSC were also observed for two native species, Lepidium lasiocarpum and Nassella pulchra. The third native species used in this study, A. californica, has seeds that are easily displaced by wind. No conclusions could be drawn about their emergence because so few remained (n = 3) in the study cores. Emergence of the two remaining native species, unlike that of the exotic species, was markedly different from each other. Although percent emergence was higher on disturbed BSC cores for both species, the difference in emergence between treatments was much less pronounced for L. lasiocarpum than for Nassella pulchra. L. lasiocarpum had the greatest emergence for all species, including exotics, on disturbed BSC, but unlike other species, emergence was almost equally high for seeds on undisturbed BSC cores. In contrast, percent emergence of N. pulchra was low for both treatments. Lepidium lasiocarpum was the only species for which seed loss was greater in disturbed cores than in undisturbed cores. Seeds of this species become mucilaginous and sticky when wet (myxospermy), and we observed seeds of L. lasiocarpum adhered to intact BSC but not to the loose soil particles of disturbed BSC. This trait may be advantageous on BSCs, by preventing displacement of seeds by wind or water runoff and by curtailing granivory (Gutterman and Shem-Tov 1997; Zaady et al. 1997; Morgan 2006).
Conclusions Our field experiment suggests that BSCs act as inhibitors of exotics and possibly as facilitators for emergence of certain native species. This field experiment likely represents conservative estimates of emergence since precipitation was nearly onequarter of the annual average. In addition, BSC development is variable across the landscape in coastal CSS communities (pers. obs.) and because this study concentrated on late-successional BSC, it may represent a situation in which disturbance has the most pronounced impact. These findings were further supported by the germination study that clearly showed exotic emergence to be enhanced by disturbance of BSC and largely deterred by intact BSC. For native plants, disturbance had less impact overall and varied by species. BSCs have been identified as important components of many terrestrial ecosystems, worldwide (Belnap and Lange 2003), and our results indicate that they are also of considerable importance in CSS, a highly modified and threatened vegetation type in the United States (Talluto and Suding 2008). Specifically, disturbance of rugose/late-successional BSCs in coastal CSS increases emergence of exotic (and usually invasive) vascular plant species. This study, the first of its kind in a semiarid mediterranean ecosystem, corroborates findings from other ecosystems indicating that BSC disturbance may have adverse impacts on community composition and structure—effects that can ultimately alter natural ecosystem function (D’Antonio and Vitousek 1992; Belnap 1995; Belnap and Eldridge 2003). The consequences of BSC disturbance in CSS may be even more detrimental than we have measured here given the long recovery period required for BSCs to return to a pre-disturbed state (Belnap and Eldridge 2003). In conclusion, we propose that BSCs act as inhibitors of exotic plant emergence in CSS and likely other BSC-supporting semiarid ecosystems, especially those threatened by invasive annual grasses. Consequently, managers should take stock of BSC presence and develop conservation programs that include efforts to curtail activities (e.g., foot traffic, biking, off-road vehicles, etc.) that disturb the sensitive BSCs that occupy these communities.
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Plant Ecol Acknowledgments We would like to thank Matthew A. Bowker and Scott T. Bates for helpful comments that greatly improved this manuscript. We thank Steven Murray, C. Eugene Jones, and Sean Walker for suggestions during experimental design and data analysis. Maya Mazon played a key role in fieldwork in addition to Amy Arispe, Tamim Sultan, and Vanessa Lopez. Financial support was provided by the U.S. Geological Survey, Priority Ecosystems Program; the Society of Women Geographers; California Garden Clubs; California Garden Club of Lake Forest; and CSU Fullerton Arboretum, Associated Students Incorporated, and Department of Biological Science.
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