Ecosystems (2009) 12: 473–488 DOI: 10.1007/s10021-009-9236-6 � 2009 Springer Science+Business Media, LLC

Effects of Dry-Season N Input on the Productivity and N Storage of Mediterranean-Type Shrublands

George L. Vourlitis,1* Sarah C. Pasquini,1,2 and Robert Mustard1

1Department of Biological Sciences, California State University, San Marcos, California 92096, USA; 2Department of Botany and Plant Sciences, University of California, Riverside, California 92521, USA

ABSTRACT Anthropogenic nitrogen (N) deposition is a globally leaching in chaparral but not CSS. Nitrogen addi­ important source of N that is expected to increase tion also lead to an increase in litter and tissue N with population growth. In southern California, N concentration and a decline in the C:N ratio, but input from dry deposition accumulates on vegeta­ failed to alter the ecosystem productivity and N tion and soil surfaces of chaparral and coastal sage storage of the chaparral and CSS shrublands over scrub (CSS) ecosystems during the summer and fall the 4-year study period. The reasons for the lack of and becomes available as a pulse following winter a treatment response are unknown; however, it is rainfall. Presumably, N input will act to stimulate possible that these semi-arid shrublands are not N the productivity and N storage of these Mediterra­ limited, cannot respond rapidly enough to capture nean-type, semi-arid shrublands because these the ephemeral N pulse, are limited by other nutri­ ecosystems are thought to be N limited. To assess ents, or the N response is dependent on the amount whether dry-season N inputs alter ecosystem pro­ and/or distribution of rainfall. These results have ductivity and N storage, a field experiment was important implications for understanding the po­ conducted over a 4-year period where plots were tential effects of anthropogenic N deposition on the exposed to either ambient N deposition (control) or C and N cycling and storage of Mediterranean-type, ambient + 50 kgN ha -1 y- 1 (added N) that was semi-arid shrublands. added as NH4NO3 during the fall dry-season of each year. Plots exposed to added N had significantly Key words: Adenostoma fasciculatum; Artemisia cal­ higher accumulation of NH4 and NO3 on ion ifornica; biogeochemistry; Ceanothus greggii; chap­ exchange resins that was due in part to direct fer­ arral; coastal sage scrub; global change; Salvia tilization and N mineralization, and the increase in mellifera; semi-arid ecosystems. N availability lead to a significant increase in NO3

INTRODUCTION Anthropogenic nitrogen (N) deposition is a signif­

Received 11 January 2008; accepted 16 January 2009; icant input of N into many southern Californian published online 21 February 2009 semi-arid ecosystems (Bytnerowicz and Fenn 1996; Author Contributions: GLV conceived or designed study, performed Fenn and others 2003a). Nitrogen deposition in research, analyzed data, contributed new methods or models, and wrote polluted urban shrublands and woodlands is esti­ the article. SCP performed research, analyzed data, and contributed to the -1 -1 writing of the article. RM performed research, analyzed data, and con­ mated to be 20–45 kgN ha y (Riggan and tributed to the writing of the article. others 1985; Bytnerowicz and Fenn 1996; Meixner *Corresponding author; e-mail: [email protected]

473 474 G. L. Vourlitis and others and Fenn 2004); however, some more exposed 1 year of N addition and it may take several years locales can receive up to 145 kgN ha -1 y -1 (Fenn for a treatment effect to be discernible in slow- and Poth 2004). Approximately, 85–95% of N growing, woody ecosystems (Oechel and Vourlitis deposition is in the form of dry deposition that is 1994; Milchunas and Lauenroth 1995). composed of oxidized and particulate N (By­ Assuming that the productivity of chaparral and tnerowicz and Fenn 1996; Padgett and others CSS shrublands is N limited, we hypothesized that 1999). Deposited N accumulates on shrub and soil repeated dry-season N addition would significantly surfaces during the summer and fall when atmo­ increase the productivity and N storage of chaparral spheric inversion traps pollutants within urban and CSS shrublands. To test this hypothesis we basins, and becomes available as a large and conducted a field experiment in chaparral and CSS, ephemeral pulse after the first rainfall event (By­ where N was added at the end of the dry season tnerowicz and Fenn 1996; Padgett and others 1999; (fall) each year. The experiment is ongoing and Fenn and others 2003a and b). part of a long-term research effort designed to Chaparral and coastal sage scrub (CSS) shrub- quantify the effects of chronic, dry-season N addi­ lands are major recipients of anthropogenic N in tion on ecosystem structure and function. Here we southern California, and represent over 70% of the report the response of aboveground biomass pro­ natural vegetation of coastal, interior, and moun­ duction and N storage after 4 years of fertilization. tain regions (Westman 1981). Chaparral is com­ posed of evergreen shrubs and is distributed in mid- to high-elevation foothill and mountain regions, MATERIALS AND METHODS whereas CSS is composed of semi-deciduous shrubs Site Description and Experimental and is distributed in coastal and low-elevation re­ Design gions (Westman 1981; Keeley 2000). Both shrub- lands tolerate intense summer drought (Poole and Field experiments were conducted between Sep­ Miller 1975; Gill and Mahall 1986; Kolb and Davis tember 2003 and 2007 at the Santa Margarita 1994), have similar rates of annual net primary Ecological Reserve (SMER: 33°29’N:117°09’W) and productivity (Gray and Schlesinger 1981, 1983), the Sky Oaks Field Station (SOFS: 33°21’N: and are subject to fire that has an average return 116°34’W). SMER is a CSS stand located in SW interval of 20–30 years (Keeley 2000). Chaparral Riverside County, California, USA at an elevation of and CSS have high biodiversity (Cowling and oth­ 338 m on a 9–11o S-SW facing slope. The site burned ers 1996) and large numbers of endangered species approximately 35 years ago and is dominated by the (Dobson and others 1997), and are relevant models semi-deciduous shrubs Artemisia californica Less. and for many semi-arid ecosystems worldwide, includ­ Salvia mellifera Greene (nomenclature according to ing Chilean mattoral, Spanish maquis, South Afri­ Munz 1974). Herbaceous species comprise 1–2% of can fynbos and thorn-scrub, and Australian the total plant cover, and are only found during the kwongan/mallee (DiCastri 1991), which share spring rainy season. Soil is a sandy clay loam of the similar adaptations to drought (Cody and Mooney Las Posas Series derived of igneous and weathered 1978), fire (Bond and van Wilgen 1996), and Gabbro material (Knecht 1971) with a bulk density nutrient-poor soils (Canadell and Zedler 1995). of 1.22 g/cm3. SMER receives an average of 36 cm Anthropogenic N inputs have the potential to of rainfall annually, most of which occurs between increase net primary productivity because the December and April. SOFS is a chaparral stand growth of chaparral and CSS shrubs is thought to located in NE San Diego County, California, USA at be N limited (McMaster and others 1982; Kum­ an elevation of 1418 m on a 4–10o SE-SW facing merow and others 1982; Gray and Schlesinger slope. The stand burned in July 2003, and unfortu­ 1983; Padgett and Allen 1999). However, drought nately this unplanned perturbation limits the that develops over the summer and fall reduces potential for direct comparison to the mature CSS physiological activity (Poole and Miller 1975; Gray stand. Before fire the site was a monoculture of the and Schlesinger 1981; Oechel and others 1981), evergreen shrub Adenostoma fasciculatum H. & A., and presumably, the ability of plants to utilize whereas after fire the stand was dominated by ephemeral pulses of anthropogenic N (Fenn and A. fasciculatum, but Ceanothus greggii A. Gray became others 2003b; Meixner and Fenn 2004). Previous a sub-dominant toward the end of 2005. The site research (Vourlitis and others 2007a) indicates that receives an average of 53 cm of precipitation dry-season N input significantly increases tissue annually consisting of rain with occasional snow and litter N concentration but not ecosystem C that occurs in November–April. The soil is an Ultic storage. However, these results were after only Haploxeroll derived of micaceous schist (Moreno Dry-Season N Addition Effects on Ecosystem C and N 475 and Oechel 1992) with a sandy loam texture and a resins consisting of 15 g anion (USF-A244B) and bulk density of 1.34 g/cm3 . 15 g cation (USF-C211) exchange resin (US Filter, The experimental layout at each site consisted of Rockford, Illinois, USA) mixed within a 6.25 9 a completely randomized design where four­ 15.0 cm 160-mesh nylon bag (n = 4 per plot). 10 9 10 m plots received 50 kgN ha -1 y- 1 as Resin bags were deployed for approximately granular NH4NO3 (added N) and an additional 3 months and the NH4–N and NO3–N that accu­ four-10 9 10 m plots served as un-manipulated mulated on the mixed-resins over the 3-month controls. N deposition estimated from a high-reso­ period was extracted with 2 M KCl and analyzed lution (4 km) model suggest that both sites receive using an auto-analyzer (Quikchem 3000, Lachat 6–8 kgN ha -1 y -1 (Tonnesen and others 2007); Instruments, Milwaukee, Wisconsin, USA). thus, control plots received 6–8 kgN ha -1 y -1 , Surface organic matter (litter pool) was collected whereas plots exposed to added N received 56– seasonally within a 25 cm 9 12.5 cm rectangular 58 kgN ha -1 y -1. The added N treatment is higher quadrat that was centered on a randomly chosen than the maximum N deposition reported for urban point (n = 2–4 per plot). Litter was defined as dead shrublands of southern California (45 kgN ha- 1 y- 1); plant matter that was recognizable and larger than however, the spatial pattern of N deposition is 1 mm in size. Aboveground litter production (litter highly variable and poorly understood, and N fall) larger than 1 mm was collected seasonally deposition can be as high as 145 kgN ha -1 y- 1 within 25 9 25 cm wooden traps equipped with a depending on elevation, slope aspect, and proxim­ 1-mm stainless steel mesh that were placed at ity to urban and/or agricultural source areas (Fenn random inside each plot (n = 4 traps per plot per and others 2003a; Meixner and Fenn 2004;Fenn site). Litter samples were sieved through a 1-mm and Poth 2004). Thus, the N exposure level used sieve to remove mineral debris that adhered to the here is consistent with highly polluted areas in litter, dried at 70°C, weighed, and ground to a fine southern California and levels expected over the powder. Litter N and C concentration was mea­ next 2–3 decades (Fenn and others 2003a; Gallo­ sured by dry combustion using a CHN analyzer way and others 2004). (ECS 4010, Costech Analytical Technologies, Inc., Beginning in 2003, granular NH4NO3 was added Valencia, California, USA). using a handheld spreader during a single applica­ Soil samples were obtained from the surface tion in September–October of each year. Granular (0–10 cm) mineral layer using a 4.7 cm diame­ NH4NO3 may not adequately simulate atmospheric ter 9 10 cm deep bucket auger immediately after dry deposition, which consists of particulate N that collection of the surface litter pool (n = 2–4 per adheres to soil and vegetation surfaces, and gaseous plot). Samples were placed in polyethylene bags, N that may be assimilated by stomatal conductance transferred to the lab in an ice-filled cooler, and (Padgett and others 1999). However, our objective stored at 4°C until analysis. A portion of the fresh was not to simulate dry N deposition per se but to sample was analyzed for pH within 4 days of col­ determine if dry-season N inputs stimulated pri­ lection, where 15 g of soil was added to 30-ml DI- mary production and N storage. Fertilizer granules water and pH was measured after 30 min using a pH disintegrated rapidly (2–3 days) after application meter (MP 220, Mettler-Toledo, Columbus, Ohio, and remained on the soil surface until the first USA). Another portion of the soil sample was dried rainfall event, which occurred 1–7 weeks following at 105°C and measured for N and C concentration application. This scenario of N accumulation, and using a CHN analyzer (ECS 4010, Costech Analytical pulsed-mobilization following rainfall, is similar to Technologies, Inc., Valencia, California, USA). that observed for dry deposition in southern Cali­ Nitrogen loss from leaching was measured using fornia shrublands (Padgett and others 1999). passive lysimeters (Drain Gauge, Decagon, Inc., Pullman, Washington, USA) installed 1 m below Field Sampling and Laboratory Analysis the soil surface (n = 3 per treatment at each site), which is below the main surface rooting zone Field sampling was conducted quarterly at each site (Hellmers and others 1955). The lysimeters were to coincide with the seasonal variation in rainfall installed in December 2003, and flow rates were (spring, March–April; summer, June–July; fall, monitored by a datalogger (CR 10X, Campbell September–October; and winter, December–Janu­ Scientific, Inc., Ogden, Utah, USA). Water samples ary). Fall sampling was conducted immediately were retrieved every 3 months using a 50-ml syr­ before N addition. inge, and the NH4–N and NO3–N concentration was Inorganic N availability was measured in the analyzed using an auto-analyzer (Quikchem 3000, surface (0–10 cm) mineral soil using ion exchange Lachat Instruments, Milwaukee, Wisconsin, USA). 476 G. L. Vourlitis and others

Approximately 10–15 cm long samples of live of water (to maintain soil moisture) and approxi­ apical shoots (leaf + stem) of A. fasciculatum and C. mately 50 ml of soda lime (to absorb respired CO2). greggii (chaparral) and A. californica and S. mellifera Soil NO3 and NH4 were extracted before and after (CSS) shrubs were randomly collected on a sea­ incubation using 0.5 M K2SO4, and extracts were sonal basis (n = 4–8 shoots per plot); however, analyzed for NO3 and NH4 concentration using an shoot samples for C. greggii were not obtained until auto-analyzer (Quikchem 3000, Lachat Instru­ fall 2005 when the abundance of this species had ments, Milwaukee, Wisconsin, USA). Net nitrifi­ substantially increased. These shrubs were selected cation and ammonification was calculated as the because they accounted for 94% (chaparral) and change in NO3 and NH4 concentration, respec­ 98% (CSS) of the total aboveground biomass, and tively, over the 10-day incubation. apical stems were selected because these stems Soil microbial N content was determined on a represent current-year’s growth (Gill and Mahall seasonal basis between fall 2006–summer 2007 1986). Tissue samples from other plant species using a fumigation and extraction procedure were collected seasonally beginning in spring 2005. (Joergensen and Brookes 1990). Soil samples ad­ Tissue samples were dried at 70°C and ground to a justed to 40% WHC and incubated for 10 days fine powder, and the tissue N and C concentration (described above) were divided into two sub-sam­ was measured using a CHN analyzer (ECS 4010, ples, one that was extracted with 0.5 M K2SO4 and Costech Analytical Technologies, Inc., Valencia, another that was exposed to 25 ml of ethanol-free California, USA). chloroform for 24 h. Fumigated samples were The aboveground biomass of all shrubs rooted immediately extracted with 0.5 M K2SO4, and the within a 2-m radius (12.57 m2) quadrat located in concentration of ninhydrin-reactive N in fumigated the center of each plot was quantified as a function and unfumigated extracts was analyzed by mea­ of shrub volume, which was calculated as the suring absorbance at 570 nm using a spectropho­ product of canopy area and height (Bonham tometer (DU 520, Beckman Instruments, Fullerton, 1989). Shrub canopy area was calculated as pD2/4, California, USA). Microbial N content was calcu­ where D is the average shrub diameter calculated lated as the difference in ninhydrin-reactive N from measurements of the maximum and per­ between fumigated and unfumigated extracts. pendicular diameter. Biomass was calculated as a function of shrub volume using regression equa­ Data Analysis tions (LN-biomass versus LN-volume) that were Aboveground net primary production (ANPP) was developed for each species from previously har­ calculated annually for 2004–2007 by summing the vested individuals (n = 18–26 shrubs depending on positive aboveground biomass increment and the species, coefficients of determination varied annual litter production (Kelly and others 1974; between 0.95 and 0.99). Aboveground biomass Barbour and others 1999). Losses to herbivores and of other annual and perennial plants was quan­ emission of volatile organic compounds were not tified beginning in spring 2005 by either estimat­ quantified, and although these losses are likely to ing biomass as a function of shrub volume or be small relative to the aboveground biomass by harvesting all plants in a 0.25 m2 quadrat increment and litter production (Mills 1983; Bar­ located in the center of each plot. Aboveground aldi and others 2004), their omission may cause (shrub + herbaceous) biomass was calculated on a ANPP to be underestimated (Barbour and others seasonal basis, and the aboveground N pool was 1999). calculated by multiplying the biomass (g dry mass/ Response variables were repeatedly measured m2 ) of a given species and/or vegetation type by its over approximately 3-month intervals, but some respective N concentration. gaps in data occurred, especially for chaparral Potential N Mineralization and Microbial immediately after fire. Repeated-measures ANOVA was used to assess whether N addition and time N Content caused significant (P < 0.05) variations in

Net NO3 and NH4 production in surface (0–10 cm) response variables. Box’s M and Mauchly’s tests soil was assessed on a seasonal basis between fall were used to test the assumptions of equality and 2006 and summer 2007 from aerobic laboratory compound-symmetry (sphericity) of the between- incubations. Field-moist soil samples were adjusted group covariance matrices, respectively (P £ to 40% water holding capacity (WHC) and incu­ 0.10), and probability values were calculated using bated at room temperature for 10 days in a dark­ the Geisser-Greenhouse corrections for data that ened cabinet that contained approximately 50 ml violated these assumptions (Hintze 2004). Dry-Season N Addition Effects on Ecosystem C and N 477

RESULTS and the decline in NH4 was significantly larger in plots exposed to N in CSS but not chaparral (Ta­ Soil C and N Dynamics and pH ble 1). However, the quantity of ninhydrin-reac­

Resin-extractable NO3 and NH4 content of the tive N (BNiN), which is a measure of microbial N chaparral and CSS surface (0–10 cm) mineral soil content (Joergensen and Brookes 1990), was not varied significantly as a function of N addition and significantly affected by N addition nor was there a time (Figure 1). Resin-accumulated NO3 and NH4 significant N 9 time interaction. BNiN varied sig­ were highest during the winter and spring and nificantly over time and was highest in the winter lowest during the fall. Chaparral plots exposed to N and summer for both chaparral and CSS (Table 1). had 4- to 5-times more resin-accumulated NO3 and Dry-season N addition significantly increased the 6- to 9-times more resin-accumulated NH4 than amount of NO3 leaching to 1 m below the soil sur­ control plots during the winter and spring (Fig­ face in chaparral, whereas in CSS no leaching of N ure 1A and C). Similarly, CSS plots exposed to N was observed during the study period (Table 2). The had 3-to 4-times more resin-accumulated NO3 and largest NO3 and NH4 losses were observed in 2005 -2 -1 -2 -1 2- to 8-times more resin-accumulated NH4 than when over 12 gN m y of NO3 and 0.2 gN m y control plots in the winter and spring (Figure 1B of NH4 was collected in the lysimeters (Table 2). and D). Differences in resin-extractable N between Nitrogen fertilization lead to a significant decline control and added N plots declined in the summer in surface soil pH for chaparral, and on average, the and fall accounting for the significant N addi­ pH of plots exposed to N was 0.2 units lower than tion 9 time interaction (Figure 1). control plots (Figure 2A). In CSS, soil pH varied Net nitrification was 2-to 3-times higher from 6 to 7 and was lower in added N plots only (P < 0.001) in chaparral plots exposed to N but not during the winter (Figure 2B). Temporal trends in in CSS (Table 1). Nearly all plots, regardless of N pH were statistically significant for chaparral and addition, exhibited a decline in NH4 over the 10­ CSS regardless of N treatment, due in part to large day incubation, indicating immobilization and/or seasonal variation and a general decline over the conversion of extractable N by microbial biomass, study period.

Figure 1. Mean (±1 SE, n = 4) extractable NO3–N (A, B) and NH4–N (C, D) accumulation on mixed anion-cation resins buried in the surface soil (0–10 cm) for chaparral (left panels) and coastal sage scrub ecosystems (right panels) exposed -1 to 50 kgN ha NH4NO3 (added N: open symbols) or ambient N (control: closed symbols). Also shown are the results (F-statistics and degrees of freedom) from a repeated-measures ANOVA for differences between N treatment (N), time (T), and the N 9 time interaction (N 9 T). *, P < 0.05; **, P < 0.01; ***, P < 0.001. W = winter (December–January), Sp = spring (March–April), S = summer (June–July), F = (September–October). Note the log-scale. 478 G. L. Vourlitis and others

Table 1. Mean Potential Net Nitrification and Ammonification and Microbial Biomass N (BNiN) for Surface 0–10 cm Soil from Control and Added N Plots in Fall 2006 and Winter, Spring, and Summer 2007

2 2 2 Chaparral Net nitrification (gN/m ) Net ammonification (gN/m ) BNiN (gN/m )

Control Added N Control Added N Control Added N

Fall 2006 0.35 ± 0.04 0.66 ± 0.10 -0.02 ± 0.01 -0.02 ± 0.05 0.68 ± 0.12 0.54 ± 0.09 Winter 2007 0.56 ± 0.03 1.28 ± 0.13 -0.09 ± 0.04 -0.65 ± 0.44 1.49 ± 0.23 0.80 ± 0.28 Spring 2007 0.28 ± 0.04 0.99 ± 0.18 0.01 ± 0.01 -0.27 ± 0.13 0.71 ± 0.04 0.70 ± 0.11 Summer 2007 0.83 ± 0.20 1.15 ± 0.19 -0.22 ± 0.06 -0.86 ± 0.49 1.23 ± 0.20 1.51 ± 0.44 N1,6 38.6*** 3.7 0.5 T3,18 5.7** 2.1 6.5** N 9 T3,18 1.4 0.9 2.1

2 2 2 Coastal sage scrub Net nitrification (gN/m ) Net ammonification (gN/m ) BNiN (gN/m )

Control Added N Control Added N Control Added N

Fall 2006 1.05 ± 0.44 0.97 ± 0.16 -0.22 ± 0.07 -0.26 ± 0.05 1.32 ± 0.37 0.73 ± 0.07 Winter 2007 1.02 ± 0.05 1.36 ± 0.15 -0.22 ± 0.04 -0.57 ± 0.09 1.15 ± 0.23 0.76 ± 0.20 Spring 2007 0.59 ± 0.09 0.93 ± 0.15 -0.05 ± 0.02 -0.14 ± 0.05 0.66 ± 0.22 0.71 ± 0.11 Summer 2007 1.75 ± 0.25 1.88 ± 0.32 -0.27 ± 0.06 -0.66 ± 0.41 1.67 ± 0.39 1.11 ± 0.25 N1,6 1.0 7.1* 2.4 T3,18 8.0** 2.0 3.6* N 9 T3,18 0.4 0.6 1.0

(±se; n = 4). Also shown are the results of a repeated-measures ANOVA (F-statistic, degrees of freedom) for the main effects of nitrogen addition (N) and time (T) and the N x time interaction (N 9 T). *P < 0.05; **P < 0.01; ***P < 0.001.

Table 2. Mean Nitrate and Ammonium Leaching to a Depth of 1 m Below the Ground Surface from Control and Added N Plots in 2004–2006 in the Post-Fire Chaparral Stand at Sky Oaks Field Station

Year Nitrate (mgN m- 2 y -1) Ammonium (mgN m -2 y- 1)

Control Added N Control Added N

2004 431.2 ± 266.5 544.5 ± 153.0 11.2 ± 6.2 28.1 ± 8.6 2005 12258.9 ± 6140.8 12995.2 ± 4942.0 297.4 ± 153.4 221.4 ± 45.6 2006 0.2 ± 0.1 128.5 ± 36.7 3.5 ± 1.4 5.1 ± 3.7 N1,4 71.6** 0.5 T2,8 40.9*** 13.4** N 9 T2,8 8.4** 0.5

(±se; n = 4). Also shown are the results of a repeated-measures ANOVA (F-statistic, degrees of freedom) for the main effects of nitrogen addition (N) and time (T) and the N 9 T interaction. **P < 0.01; ***P < 0.001.

Total soil N and C pool size in the upper 10 cm Litter N and C Dynamics soil layer was not significantly affected by N addi­ 2 Nitrogen fertilization significantly altered the sur­ tion (Figure 3). Total soil N was 40–100 gN/m for chaparral plots and 50–160 gN/m2 for CSS plots face litter N concentration and C:N ratio for CSS but not chaparral (Figure 4). Before winter 2005, and was highest in the summer and fall (Figure 3A 2 chaparral surface litter N concentration varied be­ and B). Total soil C was 1000–2200 gC/m for tween 0.5 and 1.1% regardless of N treatment, but chaparral and there was no significant temporal after winter 2005, the N concentration of surface trend (Figure 3C), whereas in CSS, total soil C was 2 litter became higher in added N plots (Figure 4A). 500–2000 gC/m and there was significant varia­ tion over time due to a weak seasonal trend and a There was a significant temporal trend in surface decline in soil C over the study period (Figure 3D). litter N concentration that reflected an overall Dry-Season N Addition Effects on Ecosystem C and N 479

significantly over time reflecting high interannual variability and a general increase in litter N storage over the study period (Figure 5A and B). The N concentration of chaparral litter fall was significantly higher in plots exposed to N (Fig­ ure 6A), whereas in CSS, the N concentration of litter fall from control and added N plots was nearly identical until winter 2006, but thereafter the N concentration of litter fall was higher in added N plots, resulting in a significant N 9 time interaction (Figure 6B). The C:N ratio of chaparral litter pro­ duced in control and added N plots began to diverge after winter 2005, and with the exception of only two sample dates (summer 2006 and spring 2007), the difference between control and added N plots became larger over the course of the study period resulting in a significant N 9 time interaction (Fig­ ure 6C). In CSS there was also a significant N 9 time interaction as the C:N ratio of added N plots declined relative to control plots after 2 years of N addition (Figure 6D). Both sites exhibited a significant temporal trend in the litter fall C:N ratio that reflected a seasonal signal and an increase over time, especially in the chaparral control plots (Fig­ ure 6C and D). Nitrogen input failed to alter litter fall Figure 2. Mean (±1SE,n = 4) surface soil (0–10 cm) pH mass (Figure 7A and B) and N pool size (Figure 7C for chaparral (A) and coastal sage scrub ecosystems (B) and D); however, litter fall mass and N pool size exposedto50kgN ha - 1 NH NO (added N: open symbols) 4 3 varied significantly over time, reaching a maximum or ambient N (control: closed symbols). Also shown are the results (F-statistics and degrees of freedom) from a repeated- in 2005 for both chaparral and CSS (Figure 7). measures ANOVA for differences between N treatment (N), time (T), and the N 9 time interaction (N 9 T). *, Aboveground Biomass and N Dynamics P < 0.05; **, P < 0.01; ***, P < 0.001. W = winter (December–January), Sp = spring (March–April), S = sum­ The N concentration of chaparral biomass was con­ mer (June–July), F = (September–October). sistently higher in added N plots, with the exception of fall 2004–summer 2005, and tissue N concentra­ decrease in litter N concentration over the study tion was highest immediately after fire in fall 2003 period. The surface litter N concentration for CSS (Figure 8A). The tissue N concentration of CSS became higher in plots exposed to added N after the aboveground biomass was also consistently higher in summer of 2004, and on average, the N concen­ added N plots and there was a significant temporal tration increased over the study period regardless of trend that reflected a seasonal signal and a decline in N treatment (Figure 4B). The C:N ratio of surface tissue N concentration from 2005 to 2007 (Fig­ litter in chaparral was not significantly affected by ure 8B). The tissue C:N ratio was consistently lower N, but there was a significant temporal trend that in chaparral (Figure 8C) and CSS (Figure 8D) plots reflected an overall increase in litter C:N over the exposed to N, and there was a significant N 9 time study period (Figure 4C). In CSS, the surface litter interaction for CSS as the effects of N addition in­ C:N was on average 5–30 units lower in plots ex­ creased over time. Tissue C:N also exhibited a signif­ posed to N and there was a significant decline in icant temporal trend for both chaparral and CSS that litter C:N over the study period regardless of N reflected a seasonal signal and a long-term increase in addition (Figure 4D). Litter pool mass was not sig­ the C:N ratio over the study period. nificantly affected by N addition nor was there a Dry-season N inputs did not significantly affect significant temporal trend, and was on average aboveground biomass (Figure 9A and B) or N 40–50 gdw/m2 for chaparral and 450–600 gdw/m2 storage (Figure 9C and D) in chaparral or CSS. for CSS over the study period (data not shown). Both shrublands exhibited a significant temporal Litter pool N content was not significantly affected trend in aboveground biomass and N storage, by N exposure in chaparral and CSS, but varied which appeared to be associated with a seasonal 480 G. L. Vourlitis and others

Figure 3. Mean (±1 SE, n = 4) surface soil (0–10 cm) total N (A, B) and C (C, D) pool size for chaparral (left panels) and -1 coastal sage scrub ecosystems (right panels) exposed to 50 kgN ha NH4NO3 (added N: open symbols) or ambient N (control: closed symbols). Also shown are the results (F-statistics and degrees of freedom) from a repeated-measures ANOVA for differences between N treatment (N), time (T), and the N 9 time interaction (N 9 T). *, P < 0.05; **, P < 0.01; ***, P < 0.001. W = winter (December–January), Sp = spring (March–April), S = summer (June–July), F = (September–October).

Figure 4. Mean (±1 SE, n = 4) surface litter pool N concentration (A, B) and C:N ratio (C, D) for chaparral (left panels) -1 and coastal sage scrub ecosystems (right panels) exposed to 50 kgN ha NH4NO3 (added N: open symbols) or ambient N (control: closed symbols). Also shown are the results (F-statistics and degrees of freedom) from a repeated-measures ANOVA for differences between N treatment (N), time (T), and the N 9 time interaction (N 9 T). *, P < 0.05; **, P < 0.01; ***, P < 0.001. W = winter (December–January), Sp = spring (March–April), S = summer (June–July), F = (September–October). Dry-Season N Addition Effects on Ecosystem C and N 481

storage of chaparral and CSS shrublands. This assumption was based on previous experiments where added N significantly increased the growth of chaparral and CSS shrubs (McMaster and others 1982; Kummerow and others 1982; Gray and Schlesinger 1983; Padgett and Allen 1999). How­ ever, contrary to our hypothesis, our data indicate that although short-term (4 years) exposure to dry- season N input significantly altered soil N avail­ ability and litter and tissue chemistry, N addition failed to stimulate ecosystem N storage, above- ground standing crop, or ANPP for the chaparral and CSS stands studied here. Dry-season N addition enhanced inorganic N availability for several months after N was mobi­ lized from rainfall, and with the levels of N addition utilized here an increase in available N is not surprising. However, N fertilization significantly increased net nitrification (chaparral) and NH4 consumption (CSS), indicating that microbial activity and N transformations were altered by added N. Similar patterns have been observed after only 1 year of fertilization (Vourlitis and others 2007a) and across N deposition gradients in southern California (Fenn and others 1996; Vour­ Figure 5. Mean (±1SE,n = 4) surface litter N pool size for litis and Zorba 2007; Vourlitis and others 2007b), chaparral (A) and coastal sage scrub ecosystems (B)ex­ indicating that N enrichment causes rapid and posed to 50 kgN ha -1 NH NO (added N: open symbols) or 4 3 sustained alterations in soil N cycling. ambient N (control: closed symbols). Also shown are the results (F-statistics and degrees of freedom) from a re­ The increase in NO3 availability with N deposi­ peated-measures ANOVA for differences between N treat­ tion has important consequences for soil chemistry, ment (N), time (T), and the N 9 time interaction (N 9 T). nutrient cycling, and the quality of groundwater *, P < 0.05; **, P < 0.01; ***, P < 0.001. W = winter and aquatic ecosystems. Chaparral ecosystems ex­ (December–January), Sp = spring (March–April), S = posed to high levels of atmospheric N deposition summer (June–July), F = (September–October). export significantly more NO3 to adjacent streams (Fenn and Poth 1999; Meixner and Fenn 2004), especially in post-fire chaparral stands because of trend, and over longer time scales, post-fire low biomass and high NH availability (Riggan and recovery in chaparral (Figure 9A and C) and 4 others 1994). In contrast, no leaching was observed interannual climatic variation in CSS (Figure 9B in CSS; however, the CSS soil had a 10–15% lower and D). Added N did not significantly affect ANPP sand content than the chaparral soil, which should or N uptake in chaparral or CSS (Table 3). ANPP in result in a slower rate of water infiltration and chaparral plots was highest in 2006 regardless of N leaching (Teepe and others 2003). The CSS site also treatment, whereas for CSS mean (±SE; =4) n had a high density of mature shrubs, and CSS ANPP reached a maximum of 616 ± 85 g m- 2 y- 1 shrubs have a higher density of roots in the upper in 2005 for added N plots and 540 ± 137 g m -2 y- 1 50 cm soil layer than chaparral shrubs (Hellmers in 2006 for control plots. Nitrogen uptake varied and others 1955), which should reduce the po­ significantly over time in both chaparral and CSS tential for NO leaching. High rates of nitrification and was highest in 2006 regardless of N treatment 3 and leaching can lead to soil acidification (Fenn (Table 3). and others 1996), which may in part explain the significant decline in chaparral soil pH in plots ex­ DISCUSSION posed to N addition and the lack of a significant N treatment effect on CSS soil pH. Effects of Dry-Season N Addition Nitrogen addition failed to alter surface (0– We hypothesized that dry-season N addition would 10 cm) soil C and N pools over the 4-year study significantly increase the productivity and N period, which is consistent with results from other 482 G. L. Vourlitis and others

Figure 6. Mean (±1 SE, n = 4) aboveground litter fall N concentration (A, B) and C:N ratio (C, D) for chaparral (left -1 panels) and coastal sage scrub ecosystems (right panels) exposed to 50 kgN ha NH4NO3 (added N: open symbols) or ambient N (control: closed symbols). Also shown are the results (F-statistics and degrees of freedom) from a repeated- measures ANOVA for differences between N treatment (N), time (T), and the N 9 time interaction (N 9 T). *, P < 0.05; **, P < 0.01; ***, P < 0.001. W = winter (December–January), Sp = spring (March–April), S = summer (June–July), F = (September–October).

Figure 7. Mean (±1 SE, n = 4) aboveground litter fall mass (A, B) and N pool size (C, D) for chaparral (left panels) and -1 coastal sage scrub ecosystems (right panels) exposed to 50 kgN ha NH4NO3 (added N: open symbols) or ambient N (control: closed symbols). Also shown are the results (F-statistics and degrees of freedom) from a repeated-measures ANOVA for differences between N treatment (N), time (T), and the N 9 time interaction (N 9 T). *, P < 0.05; **, P < 0.01; ***, P < 0.001. W = winter (December–January), Sp = spring (March–April), S = summer (June–July), F = (September–October). Note the differences in scale for chaparral and coastal sage scrub. Dry-Season N Addition Effects on Ecosystem C and N 483

Figure 8. Mean (±1 SE, n = 4) aboveground tissue N concentration (A, B) and C:N ratio (C, D) for chaparral (left panels) -1 and coastal sage scrub ecosystems (right panels) exposed to 50 kgN ha NH4NO3 (added N: open symbols) or ambient N (control: closed symbols). Also shown are the results (F-statistics and degrees of freedom) from a repeated-measures ANOVA for differences between N treatment (N), time (T), and the N 9 time interaction (N 9 T). *, P < 0.05; **, P < 0.01; ***, P < 0.001. W = winter (December–January), Sp = spring (March–April), S = summer (June–July), F = (September–October).

Figure 9. Mean (±1 SE, n = 4) aboveground biomass (A, B) and N pool size (C, D) for chaparral (left panels) and coastal -1 sage scrub ecosystems (right panels) exposed to 50 kgN ha NH4NO3 (added N: open symbols) or ambient N (control: closed symbols). Also shown are the results (F-statistics and degrees of freedom) from a repeated-measures ANOVA for differences between N treatment (N), time (T), and the N 9 time interaction (N 9 T). *, P < 0.05; **, P < 0.01; ***, P < 0.001. W = winter (December–January), Sp = spring (March–April), S = summer (June–July), F = (September– October). Note the differences in scale for chaparral and coastal sage scrub. 484 G. L. Vourlitis and others

Table 3. Mean Annual Aboveground Net Primary Production and N Uptake for Chaparral and Coastal Sage -1 Scrub Ecosystems Exposed to 50 kgN ha NH4NO3 or Ambient N (control)

Year Chaparral Coastal sage scrub

ANPP (gdw m -2 y -1 ) N uptake (gN m -2 y- 1 ) ANPP (gdw m -2 y- 1 ) N uptake (gN m -2 y -1 )

Control Added N Control Added N Control Added N Control Added N

2004 220 ± 53 68 ± 33 1.7 ± 0.4 0.5 ± 0.2 157 ± 29 135 ± 44 3.3 ± 0.8 5.2 ± 0.6 2005 382 ± 86 289 ± 121 3.5 ± 0.1 2.6 ± 0.8 409 ± 35 616 ± 85 6.5 ± 0.4 8.6 ± 2.1 2006 487 ± 135 305 ± 123 4.3 ± 1.2 2.5 ± 0.7 540 ± 137 493 ± 161 7.9 ± 2.4 9.5 ± 2.0 2007 187 ± 57 71 ± 25 3.5 ± 1.3 1.6 ± 0.7 265 ± 53 139 ± 24 6.0 ± 1.5 4.6 ± 1.6 N1,6 2.4 4.8 0.1 0.9 T3,18 6.8* 4.3* 9.2* 3.2* N 9 T3,18 0.2 0.2 1.2 0.5

(±1SE, n = 4). Also shown are the results (F-statistics and degrees of freedom) from a repeated-measures ANOVA for differences between N treatment (N), time (T), and the N 9 time interaction (N 9 T). *P < 0.05.

in situ N addition experiments (Magill and others Magill and others 2004; Vourlitis and Zorba 2007; 2004), but not with data across N deposition gra­ Vourlitis and others 2007b). The decline in litter dients where chronic N input leads to soil N C:N may reflect the deposition of senescent tissue enrichment (Korontzi and others 2000; Vourlitis with a low C:N ratio or may indicate a change in N and Zorba 2007; Vourlitis and others 2007b). resorption and/or N use efficiency (Bridgeham and However, N and C pools are highly variable and others 1995; Killingbeck 1996). For the chaparral change slowly in response to environmental per­ and CSS ecosystems studied here the former is turbations (Binkley and Hart 1989), so it may take probably more likely as changes in N resorption several years of fertilization to alter soil C and N and N use efficiency of the dominant shrubs appear pools. Similarly, added N failed to significantly alter to be small. The decline in the litter C:N ratio has microbial N storage for either chaparral or CSS. important implications for decomposition and Variable effects of N addition on microbial N con­ mineralization dynamics, and although litter tent have been observed for other CSS ecosystems decomposition may be C or N limited depending on (Sirulnik and others 2007) and may be due to labile substrate quality and microbial physiology (Hobbie C limitation that reduces the capacity for microbial 2005; Choi and others 2006), decomposition and N N sequestration (Choi and others 2006). mineralization are often significantly negatively Dry-season N input significantly affected the lit­ correlated with the litter and soil C:N ratio (Staaf ter pool N concentration and C:N ratio of CSS but and Berg 1981; Currie 1999). not chaparral. Nitrogen exposure can increase the Dry-season N addition lead to significant N litter pool N concentration through the input of N- enrichment of aboveground tissue and a decline in enriched litter and/or by the binding of added N to the tissue C:N ratio for both chaparral and CSS, surface litter (Nadelhoffer and others 1999; Magill which is consistent with results from other studies and others 2004). For CSS, the N enrichment of (Fenn and others 1996; Korontzi and others 2000; surface litter appeared to be due more to the Magill and others 2004; Vourlitis and others binding of N to litter than from inputs of N-rich 2007b). However, tissue N enrichment did not lead litter, as the litter fall N concentration was not al­ to an increase in aboveground standing crop, N tered by N addition. For chaparral, the binding of storage, or net primary production (ANPP) as added N to surface litter may have been limited by anticipated based on previous research (McMaster a small litter pool (50–60 gdw/m2) during the ini­ and others 1982; Kummerow and others 1982; tial stages of post-fire recovery. Gray and Schlesinger 1983; Padgett and Allen The C:N ratio of litter fall exposed to added N 1999). Why didn’t dry-season N addition stimulate declined significantly for both ecosystems, which is the productivity of these semi-arid shrublands? consistent with previous research in a variety of Unfortunately this question cannot be answered ecosystems exposed to chronic, high N deposition with data on-hand; however, there are several (Fenn and others 1996; Korontzi and others 2000; possible explanations. First, it is possible that Dry-Season N Addition Effects on Ecosystem C and N 485 vegetation, which is not physiologically active organic matter, even during the windiest days. This when the N was added (Poole and Miller 1975; leaves the possibility of large gaseous losses of N, Gray and Schlesinger 1981; Oechel and others especially NO, during the process of nitrification 1981), cannot respond rapidly enough to capture (Fenn and others 1996). Large gaseous losses of N the ephemeral N pulse after the first rainfall event are plausible given that NO flux is highly correlated (Fenn and others 2003b; Meixner and Fenn 2004). with nitrification (Davidson and others 2000). However, shrubs adapted to arid environments can Substantial N may also be stored belowground in rapidly respond to pulses of water and N after a roots and burls (Sparks and others 1993); however, period of drought (BassiriRad and others 1999; preliminary evidence suggests that N storage is not Gebauer and others 2002; James and Richards significantly higher in surface (0–40 cm) roots ex­ 2005), and it is reasonable to assume that semi-arid posed to N. As this research continues the long- shrubs have the same capacity. Second, assimilated term response of these semi-arid shrublands and N may not be immediately allocated to growth the pathways of N storage and loss will be quanti­ (Chapin 1980), and such ‘‘luxury consumption,’’ fied. where N is assimilated in excess of demand, has been observed in Mediterranean-type shrubs, Temporal Trends especially post-fire chaparral (Rundel and Parsons 1980; Gillon and others 1999). Third, added N may Almost all of the variables studied here exhibited not enhance production because of an imbalance in significant temporal variation. Over seasonal time tissue nutrient ratios (Mohren and others 1986; scales, variations in rainfall and soil water avail­ Vitousek and Howarth 1991), which may be par­ ability were likely the most important influence on ticularly relevant in chaparral where a decline in N and C cycling processes. During the winter and soil pH implies a decline in base cation availability spring rainy season, resin-accumulated N was (Fenn and others 1996). After 1 year of N fertil­ highest when ample soil moisture mobilized avail­ ization, Vourlitis and others (2007a) found that the able N and promoted organic matter decomposition N:P ratio of chaparral and CSS shrubs was less than and N mineralization (Binkley and Hart 1989). In 14 regardless of N treatment, suggesting that shrubs turn, high soil water and N availability enhanced N were relatively more limited by N than P (Koers­ uptake causing an increase in tissue N concentra­ elman and Meuleman 1996), but for subsequent tion and aboveground biomass production (Gray years, the tissue N:P ratio has increased, especially and Schlesinger 1981; Vourlitis and Zorba 2007). in chaparral. Finally, N-induced increases in pro­ During the summer and fall, tissue N concentration ductivity for arid or semi-arid ecosystems may be declined because low soil moisture limited N intimately tied to the amount and/or distribution of availability, transport, and/or uptake, whereas the rainfall (James and Richards 2005). Focusing on N concentration of litter fall increased as N-rich processes such as ANPP, N uptake, litter fall, and leaves were abscised in response to summer litter N input, differences between CSS plots ex­ drought (Gray and Schlesinger 1981; Gill and posed to added and ambient N (calculated as added Mahall 1986). N-control) were significantly positively correlated There were also temporal trends in response with annual rainfall for ANPP (r = 0.98; P = 0.01; variables that were influenced by interannual n = 4 years) and litter fall N input (r = 0.96; variations in climate and/or responses to distur­ P = 0.04; n = 4 years). Thus, the relative effects of bance. For example, annual litter fall production N addition on ANPP and litter fall N increased as and N content for chaparral and CSS were signifi­ rainfall increased. Similar patterns were observed cantly positively correlated (P < 0.05) with annual in chaparral but correlations were weaker, pre­ rainfall, which was highest in 2005. Similar pat­ sumably reflecting the post-fire status of the stand. terns were observed for ANPP and N uptake; The processes described above are not mutually however, correlations were weaker and not statis­ exclusive and likely interact to limit the response of tically significant. Leaching losses of NO3 and NH4 ecosystem productivity to dry-season N addition. in post-fire chaparral increased by 1–2 orders of If N enrichment failed to stimulate ecosystem magnitude in 2005 when rainfall was 325 and productivity and N storage, what happened to the 120 mm higher than in 2004 and 2006, respec­ inputted N? Our results suggest that only a small tively. Indeed, interannual variations in rainfall fraction was lost to leaching (except in 2005), and likely influence C and N cycling and storage pro­ there is scant evidence of large losses from runoff or cesses more than N deposition in these semi-arid wind, as there were no signs of a debris flow or ecosystems (Poole and Miller 1975; Oechel and wind-aided movement of fertilizer, soil minerals, or others 1981; Westman 1981; Gill and Mahall 1986; 486 G. L. Vourlitis and others

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