Soil Respiration and Litter Decomposition Increased Following Perennial Forb Invasion into an Annual Grassland

Pedosphere 26(4): 567–576, 2016 doi:10.1016/S1002-0160(15)60066-2 ISSN 1002-0160/CN 32-1315/P c 2016 Soil Science Society of China ⃝ Published by Elsevier B.V. and Science Press

Soil Respiration and Litter Decomposition Increased Following Perennial Forb Invasion into an Annual Grassland ZHANG Ling1,2 , MA Xiaochi2 , WANG Hong2 , LIU Shuwei2 , Evan SIEMANN2,3 and ZOU Jianwen2,∗ 1 College

of Forestry, Jiangxi Agricultural University, Nanchang 330045 (China) of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095 (China) 3 Department of Ecology and Evolutionary Biology, Rice University, Houston TX 77005 (USA) 2 College

(Received April 9, 2015; revised April 13, 2016)

ABSTRACT Exotic plant invasions may alter ecosystem carbon processes, especially when native plants are displaced by plants of a different functional group. Forb invasions into grasslands are common, yet little is known about how they impact carbon cycling. We conducted a field study over 2 years from April 2010 to March 2012 in China to examine changes in soil respiration (Rsoil ) following invasion of exotic perennial forb species (Alternanthera philoxeroides or Solidago canadensis) into an annual grassland dominated by a native annual graminoid (Eragrostis pilosa). Measurements of Rsoil were taken once a week in stands of the native annual graminoid or one of the forb species using static chamber-gas chromatograph method. Aboveground litterfall of each of the three focal species was collected biweekly and litter decomposition rates were measured in a 6-month litterbag experiment. The monthly average and annual cumulative Rsoil increased following invasion by either forb species. The increases in cumulative Rsoil were smaller with invasion of Solidago (36%) than Alternanthera (65%). Both invasive forbs were associated with higher litter quantity and quality (e.g., C:N ratio) than the native annual graminoid. Compared to the native annual graminoid, the invasive forbs Alternanthera (155%) and Solidago (361%) produced larger amounts of more rapidly decomposing litter, with the litter decay constant k being 3.8, 2.0 and 1.0 for Alternanthera, Solidago and Eragrostis, respectively. Functional groups of the invasive plants and the native plants they replaced appear to be useful predictors of directions of changes in Rsoil , but the magnitude of changes in Rsoil seems to be sensitive to variations in invader functional traits. Key Words:

carbon cycling, exotic plant, functional group, functional traits, invasive plants, litterfall, native plants

Citation: Zhang L, Ma X C, Wang H, Liu S W, Siemann E, Zou J W. 2016. Soil respiration and litter decomposition increased following perennial forb invasion into an annual grassland. Pedosphere. 26(4): 567–576.

INTRODUCTION Exotic plant invasions profoundly alter ecosystem element processes (Ehrenfeld, 2003; Liao et al., 2008; Laungani and Knops, 2009). Carbon cycling is one of the processes that experience much alteration following plant invasions (Liao et al., 2008). Studies on the impacts of plant invasions on ecosystem carbon cycling have increased rapidly in number, particularly on soil carbon sequestration and soil respiration (Rsoil ) (Ehrenfeld, 2003; Liao et al., 2008; Tamura and Tharayil, 2014). Soil respiration plays a major role in carbon loss from terrestrial ecosystem carbon pools, exceeding all other terrestrial-atmospheric carbon exchanges, and it is estimated to be an order of magnitude greater than the combination of carbon emitted by fossil fuel combustion and deforestation (Schlesinger and Andrews, 2000). Therefore, a slight shift in Rsoil due to plant invasions may lead to significant changes ∗ Corresponding

author. E-mail: [email protected].

in atmospheric composition and related pools (e.g., soil organic carbon pools). Successful plant invaders may be from a different functional group rather than the native plant community. Indeed, impacts of plant invasions on Rsoil are various, suggesting that carbon cycling alteration following plant invasions may be ecosystem dependent (Litton et al., 2008; Strickland et al., 2010). For instance, invasive plants generally have a higher net primary production that leads to higher litter input after each growing season (Liao et al., 2008; Wolkovich et al., 2010). Woody plants are characterized by deep roots and may have slower litter decomposition rates than herbaceous plants (Jobbagy and Jackson, 2000; Jackson et al., 2002; Funk, 2005). Differences in these traits would underlie changes in Rsoil with grass invasions into woody communities (Jackson et al., 2002; Knapp et al., 2008; Litton et al., 2008; Strickland et al., 2010; Wolkovich et al., 2010; Cable et al., 2012).

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Even if invasive plants are from the similar functional groups with the native plant community, differences in growth traits between the invasive plants and the native plants may also alter carbon cycling following plant invasions (De Deyn et al., 2008). Some studies showed that introduced grasses had a different rooting depth compared to native grasses, leading to alteration of belowground carbon input in cases of grass invasions (Wilsey and Polley, 2006; Adair and Burke, 2010). Grass invasions into grasslands may also lead to variations in Rsoil via different growth forms, life spans or litter properties (Adair and Burke, 2010; Scharfy et al., 2011). Therefore, studying multiple combinations of invaded ecosystem types and functional types of invasive species would help to fully understand how plant invasions impact Rsoil . To date, considerable attention has been paid to herbaceous invasions into woody ecosystems, while very few studies have focused on forb invasions into grassland dominated by native annual grasses, despite their widespread abundance and known impacts on ecosystem processes (Scott et al., 2001; Hook et al., 2004; Drenovsky and Batten, 2007; Weber et al., 2008; Adair and Burke, 2010). Besides differences in functional traits between invasive and native plants, abiotic factors such as soil microclimate (i.e., soil temperature or soil moisture) could be altered by increased litter coverage at the soil surface in invaded areas (Smith and Johnson, 2004; Wolkovich et al., 2009). Because soil microclimate and carbon substrate availability can be important factors controlling Rsoil , such litter-related changes in invaded plots might alter Rsoil (Raich and Schlesinger, 1992; Wan and Luo, 2003; Scott-Denton et al., 2006; Litton et al., 2008; Wolkovich et al., 2010). In this study, we examined an annual grassland that had experienced serious exotic perennial invasions in Southeast China. A 2-year field experiment was conducted to understand impacts of perennial forb invasions on Rsoil . We hypothesized that perennial forb invasions might increase Rsoil due to the higher litter production and faster litter decomposition rate of invasive perennials than those of the native annual grass. MATERIALS AND METHODS Study site This study was conducted in an annual grassland at the Nanjing Agricultural University Experimental Station (32◦ 0′ N, 118◦ 3′ E, 6 m above sea level) in Jiangsu Province, China. The study area has a typical monsoonal climate. The plant growing season is

generally from March to November and winter season covers through December to February of the next year. Mean annual temperature is 25.0 ◦ C with monthly mean temperature ranging from −10 ◦ C in January to 32.5 ◦ C in July. The mean annual precipitation is about 980 mm, 90% of which is distributed in the plant growing season from March to November. The soil is classified as a Gleysol or a hydromorphic soil with high clay content. Focal species and stand selection The grassland studied was flooded by the Yangtze River and cultivated to paddy rice until the early 20th century. Since the termination of paddy rice cultivation, some parts of the grassland have been dominated by one native annual graminoid, Eragrostis pilosa (L.) P. Beauv., before invasions of two perennial forbs, Alternanthera philoxeroides (Mart.) Griseb. and Solidago Canadensis L., which occurred approximately 5 years ago before this study. Currently, the remaining native annual grass is still threatened by these two range-expanding invasive forbs. The present distributions of these two forbs are just where they have advanced to so far. The native annual graminoid Eragrostis is a broadly distributed temperate bunchgrass native to China. In this region, Eragrostis has been the dominant plant species prior to recent exotic plant invasions. Moreover, the global distribution of Eragrostis species makes it a good model plant to study carbon cycling change in grasslands after perennial forb invasions. The invasive perennial forb Alternanthera is native to South America and it was introduced to China via Japan in the 1930s. This perennial forb is classified as one of the most aggressive invaders in China and has been detected in at least 19 provinces in China (Weber et al., 2008). It is commonly found in agricultural areas, wetlands and disturbed areas in Australia, North America and Asia. The other invasive perennial forb Solidago, another widely distributed perennial forb, was introduced into China from North America and has been reported as a serious invasive plant species that is still expanding its range (Liu et al., 2006). We surveyed the study site to locate stands dominated by the native species (Eragrostis) and by either of the two exotic perennial forb species (Alternanthera or Solidago) in December 2009. Stands with at least 80% of the coverage occupied by one focal species were considered dominated. Three stands (16 m × 30 m) dominated by one of the three species (Eragrostis, Alternanthera or Solidago) were selected.

FORB INVASION EFFECT ON SOIL RESPIRATION AND LITTER

Measurements of Rsoil Within each stand selected, we established three plots (2 m × 2 m) that were approximately 5 m away from each other and at least 5 m from the edge of the stands. In the center of each plot established, we conducted in-situ measurement of Rsoil at fixed circle quadrats. The in-situ measurements of Rsoil were conducted simultaneously in both the native and invaded plots over a 2-year period from April 2010 to March 2012, using the static chamber-gas chromatograph (GC) method (Zhang et al., 2014). Details of Rsoil measurements were shown by Zhang et al. (2014). Two weeks before Rsoil was measured within each plot, circular ceramic flux collars (20-cm height and 20-cm inside diameter) were permanently installed flush with the soil surface to ensure reproducible placement of gas collecting chambers during the successive gas flux measurements over the 2-year period. The top edge of the collar had a groove (5 cm depth) for filling with water to seal the rim of the chamber. Aboveground vegetation inside the collars was periodically removed by hand throughout the measurement period and Rsoil measurements refer to the soil surface CO2 fluxes representing the sum of soil heterotrophic respiration and root respiration. Opaque and open-bottomed cylindrical PVC gas sampling chambers (100 cm height) were used for each measurement. The bottom of a chamber was fit into the circular groove that filled with water to produce an airtight system during measurements (Zhang et al., 2014). To minimize temperature change during the gas sampling period, the chamber was wrapped in sponge and aluminum foil. Gas samples were taken once a week between local time 13:00 and 15:00 of the day as soil temperature during this period was close to the daily average soil temperature (Zou et al., 2005). Gas samples in triplicate of the headspace of the chamber were collected using single-use syringes when chambers were firstly installed (0 min) and 10 and 20 min after installation. The CO2 concentration of each gas sample was determined with a gas chromatograph (Agilent 7890, Agilent, Santa Clara, USA) equipped with a flame ionization detector (FID). Carbon dioxide was separated by one stainless steel column (2 m length and 2.2 mm inner diameter) packed with a Porapack Q column (50 to 80 mesh). Afterwards, hydrogen reduced CO2 to CH4 in a nickel catalytic converter at 375 ◦ C and CH4 was detected by the FID. The oven and the FID were operated at 55 and 200 ◦ C, respectively. Then, Rsoil (mg CO2 -C m−2 h−1 ) was determined using the following equation (Zhang et al., 2014):

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d[CO2 ] 1 × × dt R×T 1 Mc M× × A M

Rsoil = P × V ×

(1)

where [CO2 ] is the CO2 concentration of each gas sample; P is the standard atmospheric pressure (Pa); V and A are the volume (m3 ) and interior bottom area (m2 ) of the cylindrical chamber, respectively; t is time; R stands for the universal gas constant; T is the absolute air temperature (K) when the gas sample was aspirated and Mc and M are the molecular mass of carbon and CO2 (g mol−1 ), respectively. Cumulative Rsoil within a given time period was calculated by multiplying the average Rsoil by the time span. Monthly mean Rsoil values were calculated by averaging weekly measurements. When the gas samples were collected, soil temperature and moisture at the depth of 0–15 cm were measured with a digital thermometer and a portable soil moisture detector (TZS-IW, Zhejiang Top Instrument, Hangzhou, China). Aboveground litterfall and litter decomposition measurements Three randomly-placed quadrats of 0.5 m × 0.5 m were established within each species stand in February before the growing season in 2010, to collect aboveground litterfall. These quadrats were not associated with the plots for measuring Rsoil so that those plots received natural litter inputs. Plant litter that fell onto the soil surface within the quadrats was collected biweekly throughout the experimental period. Litter collected during the period was stored in a refrigerator until it was processed. At the end of each growing season, all the litter collected combined with the dead standing plants from the same quadrat was dried in forced air oven at 65 ◦ C to a constant weight. To examine litter quality differences, litter samples were ground, weighed and analyzed for carbon and nitrogen contents with a CNS elemental analyzer (Variomax CNS Analyser, Elementar GmbH, Hanau, Germany). The litter decomposition rate of each focal species was examined through in-situ litterbag incubations. Recently produced litter was collected from dead standing plants (not in plots for litter collection or plots for Rsoil measurement) and combined within a species type to produce a composite sample. Three replicate samples of air dried litter (10 g weight and 3 cm length) of each of the three focal species placed in litter bags (10 cm × 15 cm, 1 mm mesh) were used to assess decomposition rate (Crossley and Hoglund, 1962). The in-situ decomposition rate measurement was conducted from the end of March to the end of September,

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mostly coincided with the growing season. All remaining litter was processed by carefully removing dirt or other contaminants before being dried for litter mass measurement. We calculated litter decay constants (k, month−1 ) to examine litter decomposition rate of different species. The k values were calculated from a negative firstorder exponential model as follows (Olson, 1963; Tu et al., 2014): Mt = M0 e−kt

(2)

where Mt is the litter mass remaining at time t and M0 is the initial litter biomass at t = 0. Statistical analyses A two-way analysis of variance (ANOVA) was used to test whether Rsoil varied significantly among species with time. We used exponential regressions to study the relationship between Rsoil and soil temperature and second-order polynomial functions to elucidate the relationship between Rsoil and soil moisture. A One-way ANOVA was used to test whether cumulative CO2 emissions, litter production and litter decomposition rate over the 2-year experiment varied significantly among species. Post-hoc means comparisons using adjusted means partial difference tests at P = 0.05 were conducted when a significant difference was detected for factors with more than two levels. For each of the invasive forbs, we used path analysis to estimate the magnitude of direct effects of exotic forb invasion (dummy variables: 0 = native, 1 = exotic) on soil tem-

perature, soil moisture and Rsoil based on standardized regression coefficients (r). All statistical analyses were carried out using SAS 9.0 (SAS Institute, Cary, USA). RESULTS Soil respiration Monthly mean Rsoil depended significantly on species, sampling month and their interactions (Fig. 1). Soils under invasion of both the perennial forbs were characterized by higher Rsoil , while soils under the native annual graminoid Eragrostis vegetation had the lowest Rsoil (Fig. 1). Compared with the stands of the native Eragrostis, the cumulative Rsoil over the 2-year period was 65% and 36% greater in the stands invaded by Alternanthera and Solidago, respectively (Table I). The Rsoil was exponentially correlated with soil temperature under the native Eragrostis species (Fig. 2c) and the invasive Solidago species (Fig. 2d) as well as when the three species were taken as a whole (Fig. 2a), but no such relationship was observed for the Alternanthera-invaded soils (Fig. 2b). Second-order polynomial functions were used to fit the relationships between Rsoil and soil moisture over the 2-year study period for the three species combined as a whole (Fig. 3a) and separately (Figs. 3b– d). Significant relationships were found for Alternanthera (Fig. 3b) and Solidago (Fig. 3d) as well as when the three species were combined as whole (Fig. 3a); however, no significant relationship was observed for Eragrostis (Fig. 3c).

Fig. 1 Monthly average soil respiration (Rsoil ) in stands dominated by one of the three focal species (two exotic invasive perennials, Alternanthera and Solidago, and one native annual graminoid, Eragrostis) calculated from weekly in-situ measurements throughout 2 years from April 2010 to March 2011 in an annual grassland studied. *** and **** indicated significant differences at P < 0.001 and P < 0.000 1, respectively.

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TABLE I Cumulative soil respiration (Rsoil ) and selected litter properties in stands dominated by one of the three focal species (two exotic invasive perennials, Alternanthera and Solidago, and one native annual graminoid, Eragrostis) throughout 2 years from April 2010 to March 2011 in an annual grassland studied Focal species

Cumulative Rsoil First year

Litter biomass

Second year

Total

First year

m−2

Eragrostis Alternanthera Solidago

0.54 ± 1.20 ± 0.06 1.19 ± 0.13

0.01b)

kg CO2 -C 1.20 ± 0.08 1.67 ± 0.10 1.18 ± 0.04

Litter C:N

Second year

Total

m−2

1.74 ± 2.87 ± 0.04a 2.36 ± 0.10b

0.06cc)

110.4 ± 1.8 135.3 ± 2.6 318.6 ± 4.7

gC 81.5 ± 1.4 128.5 ± 2.0 358.7 ± 13.6

ka)

191.9 ± 0.8c 263.9 ± 7.8b 677.4 ± 16.7a

73 ± 2a 56 ± 3c 65 ± 1b

month−1 0.09 ± 0.01c 0.34 ± 0.01a 0.18 ± 0.00b

a) Litter

decay constant calculated by a negative first-order exponential model in the 6-month litterbag experiment. ± standard errors (n = 3). c) Values followed by the same letter in a column are not significantly different at P = 0.05 according to a one-way analysis of variance.

b) Means

Fig. 2 Relationships between soil respiration (Rsoil ) and soil temperature in stands dominated by one of the three focal species (two exotic invasive perennials, Alternanthera and Solidago, and one native annual graminoid, Eragrostis) throughout 2 years from April 2010 to March 2011 in an annual grassland studied: all species together (a), Alternanthera (b), Eragrostis (c) and Solidago (d). The relatioship is not significant for Alternanthera.

Aboveground litterfall and litter decomposition Results of the one-way ANOVA indicated that litterfall on the soil over the 2-year study period depended on species (P < 0.000 1), with significant differences in the amount of litter among each species in the post-hoc tests, but there was no significant interaction between species and year (Table I). The invasive forbs produced more litter biomass compared to the native annual grass. Over the 2 years, litter biomass of the invasive forb species, Alternanthera and Solidago, was 55% and 260% greater than that of

the native graminoid Eragrostis. Litter carbon:nitrogen (C:N) ratios of the invasive forbs were significantly lower than that of the native graminoid Eragrostis. Correspondingly, litter decomposition rate varied significantly among species (P < 0.000 1) (Table I). The litter of the invasive forbs decomposed faster than the native graminoid litter. Compared with the native graminoid Eragrostis, litter mass loss was 101% and 51% greater for the invasive forbs Alternanthera and Solidago, respectively, during the in-situ litterbag experiment. The litter k values of the invasive forbs Alternanthera and Solidago were 3.8 and 2.0 times hi-

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Fig. 3 Relationships of soil respiration rate (Rsoil ) with soil moisture in stands dominated by one of the three focal species (two exotic invasive perennials, Alternanthera and Solidago, and one native annual graminoid, Eragrostis) throughout 2 years from April 2010 to March 2011 in an annual grassland studied: all species together (a), Alternanthera (b), Eragrostis (c) and Solidago (d). The relatioship is not significant for Eragrostis.

Fig. 4 Soil temperature (a) and soil moisture (b) in stands dominated by one of the three focal species (two exotic invasive perennials, Alternanthera and Solidago, and one native annual graminoid, Eragrostis) throughout 2 years from April 2010 to March 2011 in an annual grassland studied.

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gher relative to that of the native Eragrostis, respectively (Table I). Invasive species effects on microclimate Soil temperature varied with month (P < 0.000 1), but there were no significant differences among species (P = 0.73) or interactions between species and month (P = 0.97) (Fig. 4a). Soil moisture depended on species (P < 0.000 1), with an order of Solidago < Alternanthera < Eragrostis, and month (P < 0.000 1), but no interaction of species and month (P = 0.18) (Fig. 4b) was found. Path analysis on effects of invasive forbs on soil respiration Species dominance shifts from Eragrostis to either of the perennial forbs significantly contributed to the increase in Rsoil (Fig. 5a, b). For Alternanthera, there was only a direct effect but no indirect effects via changes in soil temperature or moisture on Rsoil (Fig. 5a). For Solidago, there were both a direct positive effect of species dominance shifts and an indirect negative effect via decreased soil moisture on Rsoil (Fig. 5b). Despite a significant correlation between soil temperature and Rsoil following invasion of either of the perennial forbs into the annual Eragrostis grassland, the indirect effect on Rsoil of invasive perennial forbsvia changes in soil temperature was not significant in path analyses (Fig. 5a, b). DISCUSSION Rsoil increases following perennial forb invasions into annual grassland Increased Rsoil was observed following either perennial forb invasion into the annual grassland. Enhanced

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Rsoil following exotic plant invasions was also reported in previous studies (Ehrenfeld et al., 2001; Liao et al., 2007; Litton et al., 2008; Wolkovich et al., 2010). In general, higher net primary production and photosynthetic capacity of invasive plant species would result in more litter input in the invaded area (Feng et al., 2007; Liao et al., 2008). Moreover, Haper et al. (2010) found that invasive plants had better litter quality than the native co-occurring plants. In the present study, litter input and decay constants of both invasive forbs were significantly greater than those of the native graminoid, which would directly contribute to the enhanced Rsoil following perennial forb invasions into the annual grassland in this study. Differences in plant functional traits, such as life spans and growth forms, have also been proposed as factors influencing carbon cycling and Rsoil (Scharfy et al., 2011; Drenovsky et al., 2012; Conti and D´ıaz, 2013). In this study, both invasive species were perennial forbs that were functionally different from the native graminoid (Scharfy et al., 2011). The longer life span and year-round active belowground parts may enable perennial forbs to fix more carbon during the growing season. Moreover, perennials generally have larger allocations of gross primary productions belowground relative to annuals. While root biomass positively correlates with Rsoil , more carbon allocations belowground by perennials would also enhance Rsoil via microbial activities or plant root respiration process in their invaded areas (Dornbush and Raich, 2006; Irvine et al., 2008; Maher et al., 2010). In other words, belowground carbon pools may decrease following annual grass invasion into perennial grassland (Koteen et al., 2011) due to functional differences between the annual invasive grass and the native perennial, even though results varied among invasion sites (Kramer et al., 2012).

Fig. 5 Path diagrams describing direct and indirect effects of invasions of perennial forbs, Alternanthera (a) and Solidago (b), on soil respiration (Rsoil ) based on the standardized regression coefficients (r). **, *** and **** indicate significant differences at P < 0.01, P < 0.001 and P < 0.000 1, respectively. NS = not significant.

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Unfortunately, variations in aboveground carbon storage and associated belowground carbon pools were not directly measured in our study, which might be a limit of this study. The differences between the two focal invasive forbs also influenced their impacts on Rsoil relative to the native graminoid. Alternanthera was characterized by lower litter mass and lower C:N ratio than Solidago. These differences in litter production and litter quality in combination might impact Rsoil . We should note that the forbs have invaded the study area recently (only for about 5 years) and they are still expanding their distribution. Thereby, Rsoil changes following the perennial forb invasions of the annual grasslands may not yet have reached a steady state. Also, only naturally occurred plant stands within a single location were selected for Rsoil measurement to control variations among locations. The limited replication of the invaded stands in this study did not allow us to examine if particular soil characteristics facilitated the invasion of these forb species, or if the soil characteristics were the result of the invasion in the context of soil responses to invaders. Multi-location effects should be considered in future studies to generalize the results obtained in this study. Relationships between soil microclimate and Rsoil following perennial forb invasions into annual grassland Besides quantity and quality of plant photosynthetic productivity, soil microclimate can be an important factor regulating soil carbon cycling (Raich and Tufekciogul, 2000; Scott-Denton et al., 2006; Wolkovich et al., 2009). Overall, Rsoil correlated with both soil temperature and soil moisture for all three species types as a whole (Figs. 3a and 4a). Hence, changes in soil microclimate conditions following the forb invasions might impact Rsoil in the invaded areas. Path diagrams (Fig. 5) and analyses of effects within each forb species (Figs. 3 and 4) showed that both soil temperature and soil moisture had significant effects on Rsoil . However, the effects of plant-mediated soil microclimate changes on Rsoil in our study were not as important as those observed in previous studies (Raich and Tufekciogul, 2000; Scott-Denton et al., 2006; Wolkovich et al., 2009). While the seasonal variations in Rsoil were strongly correlated with soil temperature changes (Figs. 1a and 2), no substantial soil temperature changes were found following the forb invasions (Fig. 5). Therefore, soil temperature changes as affected by the forb invasions could not have significantly contributed to the enhanced Rsoil (Table I). Moreover, while soil moisture positively impacted

Rsoil , it was not influenced by Alternanthera invasion (Figs. 1b and 5a). Although Solidago invasion had negative effects on soil moisture, it did not contribute to the increase in Rsoil ; instead, a negative indirect effect was observed by the path analysis (Figs. 1b and 5b). It has been documented that soil temperature, soil moisture and soil carbon availability are important factors controlling Rsoil with soil carbon supply considered as a critical factor (Raich and Tufekciogul, 2000; ScottDenton et al., 2006). The weaker effects of invasions on Rsoil via soil microclimate we observed relative to other studies (Smith and Johnson, 2004; Kaur et al., 2012) indicate that direct effects of forb invasions on Rsoil may be more important. Other mechanisms accounting for Rsoil following perennial forb invasions into annual grassland Carbon derived from invasive plant may be preferred by soil microbes or have a priming effect on carbon derived from native plant (Strickland et al., 2010). Although we did not study the belowground microbial community, other studies proposed that variations in the effects of invasions on Rsoil reflect shifts in soil microbial composition (Kourtev et al., 2002; Wolkovich et al., 2010; Kaur et al., 2012). Since soil microbial communities may vary with plant functional types (Wardle et al., 2004), soil microbial composition may change when an annual grassland is invaded by species of a different functional group such as the perennial forbs. Furthermore, differences in litter chemistry could also impact microbial composition (Wolkovich et al., 2010), resulting in altered microbial communities in the invaded areas. A higher fungi to bacteria ratio in soil microbial communities may affect the efficiency of carbon use, which may further influence Rsoil (Kandeler et al., 2008). Compared to native plants, invasive plants may have litter with higher nitrogen and lower lignin content, which might lead to faster litter decomposition (Ehrenfeld et al., 2001; Liao et al., 2007; Haper et al., 2010), but might not favor higher fungi infection. Additional research on variations in soil microbial communities would increase our understanding of mechanisms underlying the effects of perennial forb invasions on ecosystem carbon cycling. Further studies are also needed to determine different forms of soil carbon under forb invasions. CONCLUSIONS Soil respiration increased following invasions of perennial forbs Alternanthera and Solidago into the annual grassland. Except for possible contributions of

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