Effect of intercropping hybrid poplar and switchgrass on biomass yield, forage quality, and land use efficiency for bioenergy production

Biomass and Bioenergy 111 (2018) 31–38

Contents lists available at ScienceDirect

Biomass and Bioenergy journal homepage: www.elsevier.com/locate/biombioe

Research paper

Effect of intercropping hybrid poplar and switchgrass on biomass yield, forage quality, and land use efficiency for bioenergy production

T

Emi Kimuraa, Steven C. Fransenb,∗, Harold P. Collinsc, Brian J. Stantond, Austin Himese, Jeffrey Smithf,1, Stephen O. Guyg,2, William J. Johnstong,2 a

Department of Soil and Crop Sciences, Texas A&M AgriLife Extension Service, Vernon, TX, 76384, USA Department of Crop and Soil Sciences, Washington State University, Irrigated Agriculture Research and Extension Center, Prosser, WA, 99350, USA c Agricultural Research Service, U.S. Department of Agriculture, Grassland Soil and Water Research Laboratory, Temple, TX, 76502, USA d GreenWood Resources, Portland, OR, 97201, USA e GreenWood Resources, Boardman, OR, 97818, USA f Agricultural Research Service, U.S. Department of Agriculture, Pullman, WA, 99164, USA g Department of Crop and Soil Sciences, Washington State University, Pullman, WA, 99164, USA b

A R T I C L E I N F O

A B S T R A C T

Keywords: Hybrid poplar Populus sp. Switchgrass biomass Forage quality

Land use efficiency can be maximized if an intercropping system is utilized to produce switchgrass (Panicum virgatum L.) biomass within the alleys between hybrid poplar trees (Populus spp.). Information is limited on switchgrass production and intercropping system in the Pacific Northwest of U.S. The objectives of this study were to evaluate the effects of hybrid poplar trees on switchgrass yield and forage quality and to determine the land use efficiency in an intercropping system under irrigation. Three cultivars of switchgrass (‘Kanlow’, ‘Blackwell’, and ‘Trailblazer’) were planted in the alleys between hybrid poplar trees (Clones: OP367 and PC4) at the Greenwood Resources, Boardman, OR in 2011. Switchgrass growth was negatively influenced by hybrid poplar trees with mean leaf area index, tiller density, and switchgrass dry matter (DM) yield in the monoculture and intercropped plots equal to 4.9 and 1.7, 383 and 69 tillers m−2, and 15 and 4 Mg ha−1, respectively, in the third year of this study. The 3-year cumulative switchgrass monoculture, switchgrass intercropping, and tree yield was 47.7, 21.5, and 58.5 Mg ha−1. As a result, cumulative land equivalent ratio during the three years of the study was 1.45 in intercropped compared to 1.0 in monoculture plots. This indicates that 45% more land would be required in monoculture system to produce the same amount of DM produced in the intercropping system. This study revealed that, despite the reduced switchgrass growth under hybrid poplar trees, intercropping hybrid poplar and switchgrass can improve land use efficiency for biomass production.

1. Introduction

Mountains, switchgrass DM yields observed in western states are comparable or greater when grown under irrigation [1,5,8]. A study established in 2004 in southeastern WA near the Colombia River showed the cultivar Kanlow produced DM yield of 3.3, 21.0, and 22.6 Mg ha−1 during first, second, and third year of establishment, respectively [5] and maintained mean DM yield of 26.7 Mg ha−1 yr−1 for fourth to sixth year [1]. A study reported DM yields ranging between 13.0 and 27.1 Mg ha−1 yr−1 across four locations in CA, and showed a high capability for switchgrass feed stock production [8]. As many U.S. states concentrate on producing important cash crops (e.g., cotton, corn, soybean, and wheat), it is wise to diversify the feedstock production regions, reducing pressure of feedstock production across the

Switchgrass (Panicum virgatum L.) is a model herbaceous species selected for second generation biofuel feedstock due to its high yielding capacity [1], low greenhouse gas emissions [2], greater net energy than oil-seeds [3], high water use efficiency [4], and high C sequestration ability [5]. Research highlighting switchgrass as viable feedstock for the production of cellulosic ethanol has been concentrated in the eastern U.S. [6]. Among southeastern states (NC, TN, VA, and WV), an average dry matter (DM) yield of 14.2 Mg ha−1 yr−1 was reported in seven year-old stands grown under dryland conditions [7]. Although the majority of switchgrass studies have been conducted east of the Rocky

∗ Corresponding author. Department of Crop and Soil Sciences, Washington State University, Irrigated Agriculture Research and Extension Center, 24106 N Bunn Rd, Prosser, WA, 99350, USA. E-mail address: [email protected] (S.C. Fransen). 1 Deceased. 2 Retired.

https://doi.org/10.1016/j.biombioe.2018.01.011 Received 22 May 2017; Received in revised form 14 December 2017; Accepted 18 January 2018 0961-9534/ © 2018 Elsevier Ltd. All rights reserved.

Biomass and Bioenergy 111 (2018) 31–38

E. Kimura et al.

U.S. There are concerns that using limited land resources for biofuel feedstock production may reduce resources for food and fiber. Alley cropping is the practice of intercropping plants in open areas between woody species. Intercropping of trees and crops improves N cycling [9], C sequestration [10], activity of soil microorganisms, and wildlife [11]. It reduces ground water contamination [12,13] and has early economic returns [14,15]. Incorporating alley cropping could substantially improve biomass production and land use efficiency. Hybrid poplar (Populus spp.) is a fast growing bioenergy woody species used for cogeneration of heat, electricity, and liquid fuel [16,17]. At some locations, hybrid poplar can produce up to 22 Mg ha−1 yr−1 of above ground biomass [18] and is often harvested in 10 years or less for timber production. Among other woody species, such as willow (Salix spp.) and eucalyptus (Eucalyptus spp.), investigated for biofuel production by the Department of Energy, hybrid poplar contains high cellulose (40%) and low lignin (22%), which make liquid fuels conversion easier [19]. Although intercropping two perennial crops is beneficial for many reasons, it also increases management difficulties. Generally, establishment of small-seeded warm-season grass is difficult because of high amounts of dormant seeds [20] and weak seedling vigor [21,22]. Shading may contribute to establishment failure by slowing plant growth [23,24] and decreasing biomass yield [25] especially in C4 species with a higher light saturation point than C3 grasses [26]. Switchgrass intercropped with loblolly pine (Pinus taeda L.) showed no shading effect on the second year after planting in eastern NC [27]. In view of the light efficiency of P. taeda plantations, a shading effect is anticipated to develop over time as suggested by the authors. Yield reduction associated with shading effect has been observed in warmseason grasses intercropped with tree species in other studies [28,29]. The yield reduction was correlated with the relative position of the grass to trees [30]. Given the well documented yield reduction of warmseason grasses in intercropping system, it is critical to assess overall productivity per unit land area. Land equivalent ratio (LER) is utilized to measure the degree of land use efficiency in intercropping [31,32]. A LER value greater than 1.0 indicates total biomass produced within a given intercropped area is greater than the biomass produced in a monoculture practice where by definition LEA equal to 1.0. Despite the ongoing challenges of alley cropping, limited information is available on establishment and management of two leading biofuel crops, hybrid poplar and switchgrass, in an intercropping system in Pacific Northwest. A large quantity of feedstock can contribute to future energy demand in this region. Intercropping two leading bioenergy species, switchgrass and hybrid poplar, might increase biomass production per unit land area. The objectives of this study were to evaluate the effect of hybrid poplar trees on switchgrass DM yield and biomass quality and to determine a land use efficiency of the intercropping system in Pacific Northwest under irrigation.

Fig. 1. Monthly temperature (a.) and precipitation (b.) along 2012 to 2014 at Boardman, OR.

field on the GreenWood Resources Inc., Boardman Tree Farm, Boardman, OR (45°46″, 119°32″ W; elevation 192 m; Frost Free Days 162; climatic data in Fig. 1) in 2011 on Quincy soil series (mixed, Mesic Xeric Torripsamments). The previous use of the site was continuous hybrid poplar plantation under the operation by Boardman Tree Farm. The field experiment was designed as a randomized complete block design with four experimental blocks. We tested three levels of each factor. The three deployment patterns were: 1) intercropping with Populus × generosa ‘OP367’, 2) intercropping with P. × Canadensis ‘PC4’, and 3) no poplar intercrop as a control. The three switchgrass cultivars, 1) Kanlow [34], 2) Blackwell [35], and 3) Trailblazer [36], were assigned to the subplots. Switchgrass monoculture plots were established at the same location under the same site conditions and management, adjacent to the switchgrass-hybrid poplar intercropped plots. The switchgrass monoculture plots allowed comparison of switchgrass production between intercropped plots and monoculture plots. Table 1 shows the analysis of variance that was used in analyzing the quantitative response data. Field plots comprise an area occupied by 30 poplar trees with north-south orientation configured 5 rows × 6 trees within rows. Tree spacing was 6 m between rows and 3 m between trees within rows. There was a single grass/poplar buffer bordering each plot; so, that the total plot dimension including the buffer was 5 rows × 12 trees (60 trees per plot). Each plot occupied 792 m2. Each poplar varietal block containing four replicates was 6336 m2. The total area occupied

2. Materials and methods 2.1. Climate The 20-years (1998–2017) average daily temperature and annual precipitation at the study site were 11.2 °C and 204 mm, respectively (Fig. 1a and b). Average annual temperature and precipitation during the growing season (April to October) were 17.2 °C and 93 mm, respectively (Fig. 1a and b). Average daily temperature peaked in July and August during the study years. Annual precipitation in 2012 was 114 mm higher than the 20-years average. For more detail on monthly maximum, monthly average, monthly minimum temperatures, and soil temperatures, see Ref. [33].

Table 1 Analysis of Variance (ANOVA).

2.2. Field preparation and experimental design The poplar-switchgrass intercropping study was established in a 32

Source of Variation

DF

Block Deployment Pattern Whole Plot Error Switchgrass Cultivar Deployment × Cultivar interaction Experimental Error

3 2 6 2 4 18

Total

35

Biomass and Bioenergy 111 (2018) 31–38

E. Kimura et al.

by the four poplar blocks was 25,344 m2 for switchgrass-hybrid poplar intercropped plots. Two hybrid poplar clones were planted on 2 March to 4 March 2011. Poplar poles with the height of 6 m tall with 7–10 cm diameter were used for this study. The GreenWood Resources Inc., Nursery, Boardman Tree Farm, Boardman, OR provided the poplar poles. Clones were selected because of their high productivity and different growth habits in the region (Personal communication with Boardman Tree Farm personnel). Three switchgrass cultivars, Kanlow [34], Blackwell [35], and Trailblazer [36] were seeded between tree rows at a seeding rate of 11.2 kg pure live seed (PLS) ha−1 on 10 June to 13 June 2011 using a Tye Drill (Great Plains Manufacturing, Salina, KS) with double disk openers. Kanlow is a lowland cultivar, while Blackwell and Trailblazer are upland cultivars. Kanlow has high productivity in the region [1,5], while upland cultivars were selected for comparison. All plots received a blended dry granular fertilizer containing 112 kg ha−1 of N, 28 kg ha−1 of P, 112 kg ha−1 of K, and 56 kg ha−1 of S, in March and 112 kg ha−1 of N, after the first harvest by mid-July. Weeds were controlled annually with glyphosate [N(phosphonomethyl) glycine] at 13.0 g eq ha−1 in late March during switchgrass dormancy. Irrigation was applied evenly over all plots by overhead sprinklers set up along the tree rows. The amount and timing of water applied during the study was adjusted to poplar tree demand estimated by Boardman Tree Farm personnel based on seasonal trends and short term forecasts. On average, 216 cm ha−1 of water was applied from April to October during the study years. For more detail on the site preparation, plot layout, and photos, see Ref. [33].

2.3.3. Above-ground switchgrass biomass Switchgrass biomass was harvested once during the establishment year in 2011 (Sept. 26) and twice in 2012 (1 July and 1 October), 2013 (8 July and 1 October), and 2014 (1 July and 30 September). Harvesting was conducted with a Hesston discbine swather (AGCO Corporation, Duluth, MN) to a residual stubble height of 15 cm. Plot weight was determined by weighing fresh weight collected within a 6m by 4-m at the center of each plot. Subsamples were taken to estimate DM yield. The plot weight and subsample DM were used to estimate DM yield on a Mg ha−1 basis. Harvested switchgrass was aerated by a hay tedder, turning the grass at least five times, then baled with a Case International Harvester 8555 baler (Racinem, WI), and removed from the field. 2.3.4. Forage quality by growth stage Another set of above-ground biomass was clipped using randomly placed 0.25 m2 quadrats at vegetative, elongation, and flowering stages of switchgrass. Samples were dried, ground, and analyzed by NIRS following the same procedures described under 2.3.2. 2.3.5. Tree yield and land equivalent ratio Hybrid poplar tree yield was estimated by non-destructive methods using regression models to estimate tree weight from measurements of given age and clone from standing tree diameter and height. Tree yields in the intercropped plots were used for conservative estimate of the tree yield in monoculture plots. The land equivalent ratio (LER) was calculated with the following formula [31]; LER = Yield of intercropped grass/yield of monoculture grass + Yield of intercropped tree/yield of monoculture tree. The LER is obtained by a sum of partial LER calculated for each biomass crop in monoculture and intercropped system [31]. Monoculture system, regardless of crops, has an LER value of 1.0; therefore, the value of 1.0 is the break-even point, where no yield advantage is observed for intercropping between the two biomass crops. The LER value greater than 1.0 indicates over-yielding, indicating the yield advantage of the intercropping system [31].

2.3. Data collection All data collection was conducted from 2012 except for switchgrass DM yield, which had been collected since 2011. 2.3.1. Above canopy photosynthetically active radiation and leaf area index Switchgrass above canopy photosynthetically active radiation (PAR) and leaf area index (LAI) were collected using PAR/LAI ceptometer (AccuPAR model LP-80, Decagon Device, Pullman, WA, USA). All above canopy PAR in the text hereafter indicates above switchgrass canopy and below tree canopy. Measurements were strictly restricted to clear sunny day between 10 a.m. and 2 p.m. Measurements were taken from six randomly selected sites across the plot during growing seasons on Day of the Year (DOY) 159, 171, 219, 235, 249, and 274 in 2012, DOY 157, 184, 232, and 274 in 2013, and DOY 135, 153, 179, 233, 251, and 266 in 2014. Switchgrass was not planted immediately below the tree canopy or tree rows; therefore, the LAI was not taken immediately below the tree canopy.

2.4. Statistical analyses A mixed model analysis of variance was used for the study of those variables assessed at the conclusion of the experiment (i.e. biomass yield of switchgrass and tree, tiller yield and quality, and LER) [39]. These response variables are not repeated measurements; therefore, we did not include a repeated statement in the Proc Mixed procedure. Blocks were considered a random effect, while deployment pattern (intercropped with PC4, intercropped with OP367, and no poplar intercropping), and switchgrass cultivars were considered fixed effects. We used the mixed model because the experiment includes both fixed and random effects. In contrast to the above analyses, a repeated statement was included in the model for those response variables assessed at successive each growth stages (LAI, PAR, and forage quality). Repeated factor for LAI and PAR was Day of the Year, while repeated factor for the forage quality was maturity stages (vegetative, elongation, and flowering stages). Panicle biomass data were Log10 transformed. Means and standard errors were reported as back-transformed values as original scale of panicle biomass data provide more useful expression than Log10 transformed values. However, it needs to be noted that the back-transformed values may underestimate the population mean [40].

2.3.2. Tiller density, tiller component DM, and tiller component forage quality Tiller density was assessed by counting the number of tillers on clipped samples using randomly placed 0.25 m2 quadrats on July and October prior to harvesting. Following the tiller counting, the same samples were separated into stems, leaf blades, and panicles. Each plant part was dried separately at 55 °C for at least 48 h. Dried samples were ground by passing through a hammer mill and then a Wiley mill (Thomas Scientific, Swedesboro, NJ) with 1 mm screen openings, and used for forage quality analysis by Near Infrared Spectroscopy (NIRS) at the Washington State University (WSU) Forage Laboratory located at the Irrigated Agriculture Research and Extension Center (IAREC) in Prosser, WA. The NIRS standard curve was calibrated using wet chemistry results of crude protein (CP), neutral detergent fiber (NDF), acid detergent fiber (ADF), lignin [37], NDF digestibility (NDFD), nonfibrous carbohydrate (NFC), and relative feed quality (RFQ) from representative samples (AgSource Lab, Umatilla, OR). A bias adjustment was made based on wet chemistry results on the standard NIRS equations [38]. These equations were then used to predict CP, NDF, ADF, lignin, NDF, NDFD, NFC, and RFQ [38].

3. Results 3.1. PAR and LAI The above-canopy PAR of the switchgrass in intercropped and monoculture plots averaged 1443 and 1250 μmol photons m−2s−1 in 33

Biomass and Bioenergy 111 (2018) 31–38

E. Kimura et al.

2012 and 2014, with a greater reduction in intercropped plots. 3.3. Forage quality by tiller component Forage quality of switchgrass stems in monoculture and intercropped plots averaged over hybrid poplar clones were 72 and 68 g mg−1 CP, 713 and 727 g mg−1 NDF, 417 and 427 g mg−1 ADF, 34 and 38 g mg−1 lignin, 547 and 529 g mg−1 NDFD, 128 and 118 g mg−1 NFC, and 86 and 82% RFQ, respectively, in the first harvest (Table 2). Overall forage quality of stems was higher in the monoculture than intercropped plots in terms of higher CP, NDFD, NFC, and RFQ and lower NDF, ADF, and lignin. Forage quality of leaves in monoculture and intercropped plots were 100 and 116 g mg−1 CP, 662 and 656 g mg−1 NDF, 389 and 378 g mg−1 ADF, 25 and 26 g mg−1 lignin, 574 and 583 g mg−1 NDFD, 138 and 128 g mg−1 NFC, and 102 and 106% RFQ, respectively. Forage quality of leaves was higher in the intercropped than monoculture plots during the first harvest. The deployment pattern did not affect forage quality of the tiller component in the second harvest; therefore, values are presented as the tiller component (P < .05) averaged over the rest of treatments.

Fig. 2. Above switchgrass canopy photosynthetically active radiation (PAR) was influenced by year × deployment pattern × day of year (P < .01). Monoculture, SWG-OP, and SWG-PC represent switchgrass monoculture, switchgrass intercropped with OP367, and switchgrass intercropped with PC4, respectively. Bars represent the standard error of the mean.

2012 and 2013, respectively (Fig. 2). In 2014, PAR in intercropped plots was lower than that measured in monoculture plots throughout the growing season; 685 μmol photons m−2s−1 versus 1332 μmol photons m−2s−1, respectively (Fig. 2). We found that the deployment pattern did not affect LAI until DOY 219 in 2012; Leaf area indices were lower in the intercropped plots than switchgrass monoculture plots in 2012 and all subsequent years (Fig. 3). Mean LAI of intercropped plots increased from 1.7 in June 2012 (DOY 159) to 4.5 in September 2012 (DOY 249) and declined to 2.9 in October 2012 (DOY 274). The seasonal LAI trend was similar in the monoculture plots where overall higher indices were measured (Fig. 3). LAI in monoculture exceeded those in the intercropped plots by 0.4, 1.5, and 2.2 in 2012, 2013, and 2014, respectively, a reflection of yearly increases in the poplar LAI.

3.4. Above-ground switchgrass DM yield Switchgrass DM yield at the end of each growing season averaged over all treatment was 1.1 Mg ha−1 in 2011, which then increased to 14.7, 17.5, and 15.4 Mg ha−1 in switchgrass monoculture plots in 2012, 2013, and 2014, respectively (Fig. 5). Switchgrass DM yield intercropped with OP 367 and PC 4 were 10.4 and 9.1 Mg ha−1 in 2013, which was the peak of the switchgrass DM yield during study years in intercropped plots, then declined to 8.4 and 6.2 Mg ha−1 in 2013, and 4.8 and 4.0 Mg ha−1 in 2014, respectively (Fig. 5).

3.2. Tiller density and tiller composition DM

3.5. Forage quality by growth stage

Maximum tiller density in the first harvest of 2012 was 1249 and 1383 tillers m−2 for monoculture and intercropped plots, respectively. Tiller density decreased yearly thereafter in both cropping systems until the lowest densities were recorded at the final harvest in 2014; 383 in intercropped plots and 69 tillers m−2 in monoculture plots (Fig. 4). Stem and leaf blade DM averaged over all treatments in the first harvest were 109 and 245 g m−2 in 2012, 198 and 288 g m−2 in 2013, and 93 and 127 g m−2 in 2014, respectively (Fig. 4). Tiller composition DM in the second harvest was significantly influenced by year × deployment interaction (P < .0001 for stem and P < .001 for leaf blade). Stem DM in monoculture and intercropped plots were 295 and 209 g m−2 in 2012, 413 and 79 g m−2 in 2013, and 236 and 12 g m−2 in 2014, respectively. The decline in DM between 2012 and 2014 was more obvious in intercropped plots (Fig. 4). Leaf DM in monoculture plots and intercropped plots were 272 and 155 g m−2 in 2012, 363 and 117 g m−2 in 2013, and 216 and 25 g m−2 in 2014, respectively (Fig. 4). Paralleling the trend in stem DM, Leaf DM declined between

Forage quality of whole switchgrass (including stem, leaf, and panicle) was influenced by deployment patter × growth stage interaction (P < .01) (Table 3). Higher forage quality was observed in intercropped plots at advanced growth stages (e.g., elongation and flowering) than monoculture plots, while forage quality was similar between monoculture and intercropped plots at vegetative stage (Table 3). Crude protein of switchgrass in monoculture and intercropped plots were 161 and 173 g mg−1, 99 and 126 g mg−1, 60 and 108 g mg−1 at vegetative stage in August, the elongation stage in September, and flowering stage in October, respectively (Table 3). Neutral detergent fiber of switchgrass in monoculture and intercropped plots were 578 and 580 g mg−1, 659 and 638 g mg−1, 567 and 621 g mg−1 in August, September, and October, respectively (Table 3). Non-fibrous carbohydrate was lower in intercropped than monoculture plots throughout the growing season. 3.6. Tree yield and land equivalent ratio Tree yield increased linearly over the study years from 3.8, 15.3, and 39.4 Mg ha−1 in 2012, 2013, and 2014, respectively (Table 4). Land equivalent ratios averaged over the two clones were 1.7, 1.5, and 1.3 in 2012, 2013, and 2014, respectively (Table 4). 4. Discussion and conclusions The objectives of this study were to evaluate the effects of hybrid poplar trees on switchgrass DM yield and biomass quality and to determine a land use efficiency of the intercropping system as compared to switchgrass monoculture. The study revealed that land use efficiency was greater in the intercropping system at least for the first three years after planting hybrid poplar trees and switchgrass than switchgrass monoculture regardless of the reduction of switchgrass growth and

Fig. 3. Leaf area index (LAI) was influenced by year × deployment pattern × day of year (P < .01). Monoculture, SWG-OP, and SWG-PC represent switchgrass monoculture, switchgrass intercropped with OP367, and switchgrass intercropped with PC4, respectively. Bars represent the standard error of the mean.

34

Biomass and Bioenergy 111 (2018) 31–38

E. Kimura et al.

Fig. 4. Density of switchgrass (SWG) tiller component (stem, blade, and panicle) was influenced by years × deployment pattern in harvest 2 (P < .0001). Harvest 1 and harvest 2 were conducted in July and October, respectively. Monoculture, SWG-OP, and SWG-PC represent switchgrass monoculture, switchgrass intercropped with OP367, and switchgrass intercropped with PC4, respectively. Bars represent the standard error of the mean.

Table 2 Forage quality was influenced by deployment pattern × tiller component interaction for the first harvest (P < .01), while forage quality in the second harvest was influenced by tiller component (P < .05). Values were reported as average and (standard error). CP

aNDF

ADF

Lignin

NDFD

NFC

g mg−1

RFQ %

Stem

Monoculture SWG-OP SWG-PC

First harvest (July) 72 (4) 713 (5) 68 (3) 727 (5) 68 (3) 728 (4)

417 (2) 427 (3) 427 (2)

34 (1) 38 (1) 39 (1)

547 (5) 533 (4) 525 (3)

128 (3) 117 (3) 118 (2)

86 (2) 82 (2) 81 (1)

Leaf

Monoculture SWG-OP SWG-PC

100 (4) 116 (5) 116 (5)

662 (5) 655 (6) 658 (6)

389 (4) 379 (5) 377 (4)

25 (1) 26 (1) 26 (1)

574 (6) 584 (7) 583 (7)

138 (5) 130 (3) 127 (4)

102 (2) 106 (2) 106 (2)

Second harvest (October) 43 (5) 726 (6) 104 (9) 664 (9)

459 (5) 419 (9)

53 (1) 28 (1)

490 (6) 595 (7)

126 (10) 79 (13)

61 (3) 85 (5)

Stem Leaf

intercropped with loblolly pine (P. taeda) was reported to be 2.5 in North Carolina [27], while the peak LAI of switchgrass intercropped with hybrid poplar in our study was 4.5. The reason for the higher LAI in our study may be due to the difference in tree ages, level of canopy closure, and tree management. The LAI differences in switchgrass monoculture and intercropped plots increased each year from 2012 to 2014 (Fig. 3) because growing tree canopy reduced switchgrass above canopy PAR in intercropped plots (Fig. 2). Patterns of tiller density and tiller component DM within a growing season observed in this study were consistent with other studies, where tiller density decreases, while tiller component DM increases toward fall [46,47]. Leaf DM was decreased, while stem DM increased toward fall [45,48]. This phenomenon has been described as size-density compensation [49]. In addition, tiller formation is controlled by the interaction between formation of new tillers and death of old tillers [50]; therefore, the tiller density is higher in spring to summer when plants are actively generating new tillers [50]. Wide range of tiller density (100–2200 tillers m−2) in switchgrass monoculture has been reported in other studies depending on the cultivars, planting width, fertility management, and locations [42,46,47,50–53]. However, there are a few studies that report switchgrass tiller density in intercropping systems [27,54]. The lowest tiller density observed in our study was 59 tillers m−2 in intercropped plot in 2014. Albaugh et al. [54] reported that tiller density of 49 tillers m−2 in low shade treatment created by 36% shade cloth, under which PAR was in the range of 7–14 μmol photons m−2 s−1. Although our seasonal average PAR in 2014 was 744 μmol photons m−2 s−1, tiller density was similar to the tiller density reported under the PAR of 7–14 μmol photons m−2 s−1 [54]. A potential reason for the reduced tiller density in the intercropped plots in current study may be due to the amount of water applied to the site. The irrigation amount was adjusted to maximize growth of hybrid

Fig. 5. Switchgrass (SWG) above-ground biomass (Mg ha−1) was influenced by deployment pattern × year interaction (P < .0001). Monoculture, SWG-OP, and SWG-PC represent switchgrass monoculture, switchgrass intercropped with OP367, and switchgrass intercropped with PC4, respectively. Bars represent the standard error of the mean.

switchgrass biomass yield observed under intercropping system. Reduction of switchgrass growth and biomass production in intercropped compared to switchgrass monoculture plots was observed a year after planting in 2012, in terms of reduced LAI (Fig. 3), tiller density and tiller composition DM (Fig. 4), and total switchgrass DM (Fig. 5). The seasonal LAI patterns within a growing season observed in this study was consistent with other studies, where LAI peaked during summer months and declined toward fall [27,41–44]. The LAI declined toward fall because old tillers senesce leaves in fall and translocate energy to reproductive parts [45]. The highest LAI observed in this study was 6.9, which was in the higher end of the range (3.3–8.0) reported in other studies conducted in the southeast, north central, and Midwest U.S. and Canada [27,41,43,44]. The peak LAI of switchgrass 35

Biomass and Bioenergy 111 (2018) 31–38

E. Kimura et al.

Table 3 Forage quality was influenced by deployment pattern × growth stage interaction (P < .01). Monoculture, SWG-OP, and SWG-PC represent switchgrass monoculture, switchgrass intercropped with OP367, and switchgrass intercropped with PC4, respectively. Values were reported as average and (standard error). CP

aNDF

ADF

Lignin

NDFD

NFC

g mg−1

RFQ %

Vegetative June

Monoculture SWG-OP SWG-PC

136 (4) 138 (5) 137 (5)

319 (4) 323 (4) 325 (4)

576 (6) 583 (5) 592 (4)

20 (1) 20 (0) 21 (0)

645 (7) 642 (7) 634 (5)

191 (4) 177 (4) 174 (4)

135 (1) 130 (1) 129 (1)

Elongationa July

Monoculture SWG-OP SWG-PC

76 (2) 96 (5) 105 (6)

394 (6) 391 (7) 382 (8)

673 (9) 667 (11) 660 (11)

38 (1) 38 (1) 37 (1)

529 (3) 541 (2) 546 (4)

148 (6) 127 (5) 125 (4)

89 (2) 93 (3) 96 (3)

Vegetative August

Monoculture SWG-OP SWG-PC

161 (5) 173 (5) 172 (3)

343 (4) 341 (6) 340 (6)

578 (5) 577 (8) 583 (7)

26 (0) 27 (1) 28 (1)

676 (4) 670 (9) 668 (12)

141 (2) 128 (3) 125 (4)

122 (1) 116 (2) 118 (2)

Elongation September

Monoculture SWG-OP SWG-PC

99 (3) 126 (4) 126 (3)

392 (3) 384 (3) 382 (2)

659 (3) 638 (4) 638 (3)

30 (1) 33 (1) 33 (1)

598 (6) 597 (6) 602 (7)

133 (4) 126 (3) 122 (4)

102 (1) 106 (1) 106 (1)

Floweringa October

Monoculture SWG-OP SWG-PC

60 (3) 104 (3) 112 (3)

417 (3) 417 (4) 410 (3)

657 (4) 619 (5) 623 (5)

40 (1) 41 (1) 39 (1)

544 (6) 582 (6) 576 (7)

181 (5) 144 (3) 135 (4)

85 (2) 95 (2) 96 (1)

a

Harvest was conducted following this date.

Generally, nutritive values of warm-season grasses decrease with maturity advancement from spring to summer as NDF and lignin concentrations increase [58,59]. Sugar and lignin tissue concentrations strongly depend on time of harvest [60], plant maturity [61–64], plant component (e.g., stem and leaf), and location within the stem (e.g., basal or apical) [65]. The higher CP and NDFD and lower fibers (NDF and ADF) under intercropped plots during elongation and flowering stages indicate that forage quality was higher in intercropped than monoculture plots. Shading delayed maturity of switchgrass growth under lower temperatures, where reduction of cell wall content and increased nutrient content has been observed [66,67]. Non-fibrous carbon was always higher in the monoculture as compared to intercropped plots regardless of the maturity stages (Table 3). This indicates that photosynthetic rate may have been slower in intercropped with lower PAR than monoculture plots with higher PAR (Fig. 2). This has been a commonly reported observation in other studies [55,68]. The 3-year cumulative DM (2012–2014) of switchgrass and tree yield were 47.7 and 58.5 Mg ha−1 for monoculture and 21.5 and 58.5 Mg ha−1 for intercropped plots, respectively (Fig. 5 and Table 4), which resulted in a 3-year cumulative LER value of 1.45 (LER = 21.5/ 47.7 + 58.5/58.5) in intercropped system relative to LER value of 1.00 in monoculture plots. This indicates that 45% more land would be required in monoculture system to produce the same amount of DM produced in the intercropping system. This study explored the unique intercropping system between C4-grass and C3-tree and is the first to report successful biomass production system with high land use efficiency in the Pacific Northwest. Although shading created by hybrid poplar trees gradually decreased switchgrass growth and DM yield over the study years. The intercropping system produced a greater DM biomass as compared to switchgrass monoculture system. We believe that the amount of water applied for the maximum growth of hybrid poplar production adversely affected the growth of switchgrass, which could be a significant biomass production issue when grass biomass is intercropped within commercial tree plantation. It is important to note that the plot size utilized in this study was small (792 m2) to draw definitive conclusion on management of warm-season grass for the large tree plantation system. Therefore, further investigations of irrigated-intercropped systems and its economic viability of intercropping are warranted.

Table 4 Tree dry matter (DM) yield was influenced by year (P < .001) and averaged over switchgrass cultivar and clones. Land equivalent ratio (LER) was influenced by deployment pattern (P < .0001) and averaged over hybrid poplar clones. SWG-OP and SWG-PC represent switchgrass intercropped with OP367 and switchgrass intercropped with PC4, respectively. Values were presented as mean and (standard error). 2012

2013

2014

3-year cumulative

−1

Tree

Tree DM (Mg ha ) 3.8 (0.13) 15.3 (0.37)

39.4 (0.80)

58.5 (1.2)

SWG-OP SWG-PC

LER 1.7 (0.09) 1.7 (0.06)

1.3 (0.05) 1.3 (0.03)

1.45 (0.03)

1.5 (0.05) 1.4 (0.04)

poplar trees, which resulted in excessive water supply for proper growth of switchgrass. Although water was applied equally to both switchgrass monoculture and intercropped plots the water applied was 97–214 cm ha−1 yr−1 above the amount required for switchgrass grown in Pacific northwest [1,5]. This may explain why the switchgrass yield in monoculture plot did not reach a switchgrass yield normally observed in the Pacific Northwest under irrigation [1,5]. In a study reported by Kimura et al. [1], switchgrass DM yield reached its maximum yield of 28.9 Mg ha−1 in the fourth year (2007) after planting in 2004 with five-year average DM yield of 20.2 Mg ha−1. Another study reported by Collins et al. [5] showed two-year average DM yield of 18.0 Mg ha−1. In our study, the maximum yield of 17.5 Mg ha−1 was observed in the third year (2013) after planting in 2011 with three-year average DM yield of 15.9 Mg ha−1 (Fig. 5), which is 4.3 and 2.1 Mg ha−1 lower than the yield reported by Kimura et al. [1] and Collins et al. [5] in Pacific Northwest under irrigation, respectively. Therefore, the declining trend of switchgrass growth and DM in intercropped plots may be attributed to compounding effects of shading and excess water for the optimum growth of switchgrass. Forage quality of switchgrass stems was lower in intercropped plots in terms of increased fiber component and decreased CP values (Table 2). This may be caused because lignification is influenced by temperature, soil moisture, light, and soil fertility [55,56]. In contrast to stem quality, forage quality of leaves was higher in the intercropped than monoculture plots during the first harvest (Table 2). Stressed perennial plants mobilize N to storage organs and deposit fibers in the stem [57].

36

Biomass and Bioenergy 111 (2018) 31–38

E. Kimura et al.

Acknowledgements

[23] K.J. Moore, L.E. Moser, K.P. Vogel, S.S. Waller, B.E. Johnson, K.J. Moore, et al., Describing and quantifying growth stages of perennial forage grasses, Agron. J. 83 (1991) 1073–1077 http://digitalcommons.unl.edu/agronomyfacpub. [24] D.R. Buxton, S.L. Fales, Plant environment and quality, in: G.C.J. Fahey (Ed.), Forage Qual. Eval. Util. ASA, CSSA, and SSSA, Lincoln, NE, 1994, pp. 155–199. [25] G. Suresh, J.V. Rao, Intercropping sorghum with nitrogen fixing trees in semiarid India, Agrofor. Syst. 42 (1999) 181–194. [26] O. Björkman, Responses to different quantum flux densities, in: O.L. Lange, P.S. Nobel, C.B. Osmond, H. Ziegler (Eds.), Physiol. Plant Ecol. I Responses to Phys. Environ. Springer Berlin Heidelberg, Berlin, Heidelberg, 1981, pp. 57–107, , http:// dx.doi.org/10.1007/978-3-642-68090-8_4. [27] J.M. Albaugh, E.B. Sucre, Z.H. Leggett, J.C. Domec, J.S. King, Evaluation of intercropped switchgrass establishment under a range of experimental site preparation treatments in a forested setting on the Lower Coastal Plain of North Carolina, U.S.A, Biomass Bioenergy 46 (2012) 673–682, http://dx.doi.org/10.1016/j.biombioe. 2012.06.029. [28] C.H. Lin, R.L. McGraw, M.F. George, H.E. Garrett, Shade effects on forage crops with potential in temperate agroforestry practices, Agrofor. Syst. 44 (1998) 109–119, http://dx.doi.org/10.1023/A:1006205116354. [29] M.A. Blazier, T.R. Clason, Z. Vance, E.B. Leggett, E.B. Sucre, Loblolly pine age and density affects switchgrass growth and soil carbon in an agroforestry system, For. Sci. 58 (2012) 485–496. [30] S. Tian, J.F. Cacho, M.A. Youssef, G.M. Chescheir, M. Fischer, J.E. Netteles, et al., Switchgrass growth and pine-switchgrass interactions in established intercropping systems, GCB Boenergy (2015), http://dx.doi.org/10.1111/gcbb.12381. [31] S.R. Gliessman, Agroecosystem Diversity and Stability, CRC Press, Boca Raton, FL, 2007. [32] S. Haile, M. Palmer, A. Otey, Potential of loblolly pine: switchgrass alley cropping for provision of biofuel feedstock, Agrofor. Syst. 90 (2016) 763–771, http://dx.doi. org/10.1007/s10457-016-9921-3. [33] H.P. Collins, E. Kimura, S. Fransen, A. Himes, P.A. Fay, Intercropping with switchgrass improves net greenhouse gas balance in hybrid poplar plantations on a sand soil, Soil Sci. Am. J 81 (2017) 781–795. [34] USDA Natural Resources Conservation Service, “Kanlow” Switchgrass, (2011). [35] USDA Natural Resources Conservation Service, “Blackwell” Switchgrass (Panicum Virgatum) Conservation Plant Release, (2011). [36] K.P. Vogel, F.A. Haskins, Registration of “Trailblazer” switchgrass, Crop Sci. 31 (1991) 1388. [37] H.K. Goering, P.J. Van Soest, Forage Fiber Analyses: Apparatus, Reagents, Procuedures and Some Applications, Washington D.C. (1970). [38] W.R. Windham, D.R. Mertens, F.E.I. Barton, Protocol for NIRS Calibration: Sample Selection and equation Development and Validation, Washington D.C. (1989). [39] SAS, Institute, SAS Software Version 9.3, (2013) Cary, NC, U.S.A. [40] P. Rothery, A cautionary note on data transformation: bias in back-transformed means, Bird stud 35 (1998) 219–221. [41] D.D. Redfearn, K.J. Moore, K. Vogel, S.S. Waller, R.B. Mitchell, Canopy architecture and morphology of switchgrass populations differing in forage yield, Agron. J. 89 (1997) 262–269, http://dx.doi.org/10.2134/agronj1997. 00021962008900020018x. [42] R.B. Mitchell, L.E. Moser, K.J. Moore, D.D. Redfearn, Tiller demographics and leaf area index of four perennial pasture grasses, Agron. J. 90 (1998) 47–53, http://dx. doi.org/10.2134/agronj1998.00021962009000010009x. [43] I.C. Madakadze, B.E. Coulman, P. Peterson, K.A. Stewart, R. Samson, D.L. Smith, Leaf area development, light interception, and yield among switchgrass populations in a short-season area, Crop Sci. (1998), http://dx.doi.org/10.2135/cropsci1998. 0011183X003800030035x. [44] E.A. Heaton, F.G. Dohleman, S.P. Long, Meeting US biofuel goals with less land: The potential of Miscanthus, Global Change Biol. (2008), http://dx.doi.org/10.1111/j. 1365-2486.2008.01662.x. [45] A.J. Smart, L.E. Moser, K.P. Vogel, Morphological characteristics of big bluestem and switchgrass plants divergently selected for seedling tiller number, Crop Sci. 44 (2004) 607–613, http://dx.doi.org/10.2135/cropsci2004.6070. [46] R.B. Mitchell, K.J. Moore, L.E. Moser, J.O. Fritz, D.D. Redfearn, Predicting developmental morphology in switchgrass and big bluestem, Agron. J. 89 (1997) 827–832. [47] A. Boe, D.L. Beck, Yield components of biomass in switchgrass, Crop Sci. 48 (2008) 1306–1311, http://dx.doi.org/10.2135/cropsci2007.08.0482. [48] J.L. Griffin, G.A. Jung, Leaf and stem forage quality of big bluestem and switchgrass, Agron. J. 75 (1983) 723, http://dx.doi.org/10.2134/agronj1983. 00021962007500050002x. [49] A.H. Garay, C. Matthew, J. Hodgson, Tiller size/density compensation in perennial ryegrass miniature swards subject to differing defoliation heights and a proposed productivity index, Grass Forage Sci. 54 (1999) 347e56. [50] R.H.M. Langer, S.M. Ryle, O.M. Jewiss, The changing plant and tiller populations of timothy and meadow fescue swards: I. Plant survival and the pattern of tillering, J. Appl. Ecol. 1 (1964) 197–208. [51] P.C. Kassel, R.E. Mullen, T.B. Bailey, Seed yield response of three switchgrass cultivars for different management practices, Agron. J. 77 (1985) 214, http://dx.doi. org/10.2134/agronj1985.00021962007700020010x. [52] A. Boe, Genetic and environmental effects on seed weight and seed yield in switchgrass, Crop Sci. 43 (2009) 63–67. [53] K.A. Cassida, J.P. Muir, M.A. Hussey, J.C. Read, B.C. Venuto, W.R. Ocumpaugh, Biofuel component concentrations and yields of switchgrass in south central U.S. environments, Crop Sci. 45 (2005) 682–692, http://dx.doi.org/10.2135/ cropsci2005.0682. [54] J.M. Albaugh, T.J. Albaugh, R.R. Heiderman, Z. Leggett, J.L. Stape, K. King, et al.,

This publication is based on work supported by the USDA Agricultural Research Service under the GRACEnet Project and a grant from the USDA Agriculture and Food Research Initiative Carbon Sequestration and Sustainable Bioenergy Production program (20116700930001). The authors wish to thank Jason R. Mieirs and (Washington State University, IAREC, Prosser, WA), R. Cochran, M. Silva, and B. Wilson (USDA-ARS, Prosser, WA) for field assistance, and G.R. Godinez (Washington State University, IAREC, Prosser, WA) for sample processing and laboratory analyses. References [1] E. Kimura, H.P. Collins, S. Fransen, Biomass production and nutrient removal by switchgrass under irrigation, Agron. J. 107 (2015) 204–210, http://dx.doi.org/10. 2134/agronj14.0259. [2] M.R. Schmer, K.P. Vogel, R.B. Mitchell, L.E. Moser, K.M. Eskridge, R.K. Perrin, Establishment stand thresholds for switchgrass grown as a bioenergy crop, Crop Sci. 46 (2006) 157–161, http://dx.doi.org/10.2135/cropsci2005.0264. [3] D. Tilman, J. Hill, C. Lehman, Carbon-negative biofuels from low-input high-diversity grassland biomass, Science (80-. ) 314 (2006) 1598–1600. [4] M. Wu, M. Mintz, M. Wang, S. Arora, Consumptive Water Use in the Production of Bioethanol and Petroleum Gasoline, Oak Ridge, TN, (2008), http://dx.doi.org/10. 1017/CBO9781107415324.004. [5] H.P. Collins, J.L. Smith, S. Fransen, A.K. Alva, C.E. Kruger, D.M. Granatstein, Carbon sequestration under irrigated switchgrass (Panicum virgatum L.) production, Soil Sci. Soc. Am. J. 74 (2010) 2049–2058, http://dx.doi.org/10.2136/ sssaj2010.0020. [6] S.B. McLaughlin, L.A. Kszos, Development of switchgrass (Panicum virgatum) as a bioenergy feedstock in the United States, Biomass Bioenergy 28 (2005) 515–535, http://dx.doi.org/10.1016/j.biombioe.2004.05.006. [7] J.H. Fike, D.J. Parrish, D.D. Wolf, J.A. Balasko, J.T. Green, M. Rasnake, et al., Longterm yield potential of switchgrass-for-biofuel systems, Biomass Bioenergy 30 (2006) 198–206, http://dx.doi.org/10.1016/j.biombioe.2005.10.006. [8] G.M. Pedroso, R.B. Hutmacher, D. Putnam, S.D. Wright, J. Six, C. Van Kessel, et al., Yield and nitrogen management of irrigated switchgrass systems in diverse ecoregions, Agron. J. 105 (2013) 311–320, http://dx.doi.org/10.2134/agronj2012. 0354. [9] S.C. Allen, S. Jose, P.K.R. Nair, B.J. Brecke, C.L. Ramsey, Competition for 15Nlabeled fertilizer in a pecan (Carya illinoensis K. Koch)-cotton (Gossypium hirsutum L.) alley cropping system in the southern United States, Plant Soil 263 (2004) 151–164, http://dx.doi.org/10.1023/B: PLSO.0000047732.95283.ac. [10] S. Fang, H. Li, Q. Sun, L. Chen, Biomass production and carbon stocks in poplar-crop intercropping systems: a case study in northwestern Jiangsu, China, Agrofor. Syst. 79 (2010) 213–222, http://dx.doi.org/10.1007/s10457-010-9307-x. [11] G.A. Stainback, J.R.R. Alavalapati, Restoring longleaf pine through silvopasture practices: an economic analysis, For. Pol. Econ. 6 (2004) 371–378 https://doi.org/ 10.1016/j.forpol.2004.03.012. [12] S. Jose, A.R. Gillespie, S.G. Pallardy, Interspecific interactions in temperate agroforestry, Agrofor. Syst. 61 (2004) 237–255, http://dx.doi.org/10.1023/B: AGFO. 0000029002.85273.9b. [13] M. Bergeron, S. Lacombe, R.L. Bradley, J. Whalen, A. Cogliastro, M.-F. Jutras, et al., Reduced soil nutrient leaching following the establishment of tree-based intercropping systems in eastern Canada, Agrofor. Syst. 83 (2011) 321–330, http://dx. doi.org/10.1007/s10457-011-9402-7. [14] F.C. Zinkhan, M.D. Evan, An assessment of agroforestry systems in the southern USA, Agrofor. Syst. 35 (1997) 303–321. [15] M.A. Gold, H.E. Garrett, Agroforestry nomenclature, concepts, and practices, in: H.E. Garrett (Ed.), North Am. Agrofor. An Integr. Sci. Pract., Second, American Society of Agronomy, Madison, WI, 2009, pp. 45–56. [16] E. Hansen, L. Moore, D. Netzer, M. Ostry, H. Phipps, J. Zavitkovski, Establishing Intensively Cultured Hybrid Poplar Plantations for Fuel and Fiber, St. Paul, MN, (1983). [17] L.A. Newman, S.E. Strand, N. Choe, J. Duffy, G. Ekuan, M. Ruszaj, et al., Uptake and biotransformation of trichloroethylene by hybrid poplars, Environ. Sci. Technol. (1997), http://dx.doi.org/10.1021/es960564w. [18] X. Guo, X. Zhang, Performance of 14 hybrid poplar clones grown in Beijing, China, Biomass Bioenergy 34 (2010) 906–911, http://dx.doi.org/10.1016/j.biombioe. 2010.01.036. [19] Advanced Hardwood Biofuels Northwest, Pre-treatment. Hydrolysis Releases Sugars from Wood, (2013) http://hardwoodbiofuels.org/conversion/pre-treatment/. [20] E. Kimura, S.C. Fransen, H.P. Collins, S.O. Guy, W.J. Johnston, Breaking seed dormancy of switchgrass (Panicum virgatum L.): a review, Biomass Bioenergy 80 (2015) 94–101, http://dx.doi.org/10.1016/j.biombioe.2015.04.036. [21] G.W. Evers, M.J. Parson, Soil type and moisture level influence on Alamo switchgrass emergence and seedling growth, Crop Sci. 43 (2003) 288–294. [22] D.S. Loch, S.W. Adkins, M.R. Heslehurst, M.F. Paterson, S.M. Bellairs, Seed formation, development, and germination, in: L.E. Moser, B.L. Burson, L.E. Sollenberger (Eds.), Warm-Season (C4) Grasses, Agronomy Society of America, Inc., 2004, pp. 95–144.

37

Biomass and Bioenergy 111 (2018) 31–38

E. Kimura et al.

[55] [56]

[57]

[58]

[59] [60]

[61]

0011183X003100040043x. [62] P.R. Adler, M.A. Sanderson, A.A. Boateng, P.J. Weimer, H.J.G. Jung, Biomass yield and biofuel quality of switchgrass harvested in fall or spring, Agron. J. 98 (2006) 1518–1525, http://dx.doi.org/10.2134/agronj2005.0351. [63] B.S. Dien, H.J.G. Jung, K.P. Vogel, M.D. Casler, J.F.S. Lamb, L. Iten, et al., Chemical composition and response to dilute-acid pretreatment and enzymatic saccharification of alfalfa, reed canarygrass, and switchgrass, Biomass Bioenergy 30 (2006) 880–891, http://dx.doi.org/10.1016/j.biombioe.2006.02.004. [64] D.G.J. Mann, N. Labbé, R.W. Sykes, K. Gracom, L. Kline, I.M. Swamidoss, et al., Rapid assessment of lignin content and structure in switchgrass (Panicum virgatum L.) grown under different environmental conditions, Bioenergy Res. 2 (2009) 246–256, http://dx.doi.org/10.1007/s12155-009-9054-x. [65] G. Sarath, L.M. Baird, K.P. Vogel, R.B. Mitchell, Internode structure and cell wall composition in maturing tillers of switchgrass (Panicum virgatum. L), Bioresour. Technol. 98 (2007) 2985–2992, http://dx.doi.org/10.1016/j.biortech.2006.10. 020. [66] G. Allard, C.J. Nelson, S.G. Pallardy, Shade effects on growth of tall fescue: I. Leaf anatomy and dry matter partitioning, Crop Sci. 31 (1991) 163–167. [67] K.D. Kephart, D.R. Buxton, Forage quality response of C3 and C4 perennial grasses to shade, Crop Sci. 33 (1993) 831–837. [68] J.R. Wilson, Environmental and nutritional factors affecting herbage quality, in: J.B. Hacker (Ed.), Nutr. Limits to Anim. Prod. from Pastures, Commonwealth Agricultural Bureaux, Farnham Royal, U.K., 1982, pp. 111–131.

Evaluating changes in switchgrass physiology, biomass, and light-use efficiency under artificial shade to estimate yields if intercropped with Pinus taeda L. Agrofor. Syst. 88 (2014) 489–503, http://dx.doi.org/10.1007/s10457-014-9708-3. D.R. Buxton, M.D. Casler, Environmental and Genetic Effects on Cell Wall Composition and Digestibility, ASA, CSSA, SSSA, Madison, WI, 1993. C.J. Nelson, L.E. Moser, E. Lowell, Plant factors affecting forage quality, in: G.C. Fahey, M. Collins, D.R. Mertens, L.E. Moser (Eds.), Forage Qual. Eval. Util. ASA, CSSA, SSSA, Madison. WI, 1994, pp. 115–154. E.H.D. Scott, A. Heckathorn, Drought-Induced Nitrogen Retranslocation in Perennial C4 Grasses of Tallgrass Prairie, Ecology 75 (1994) 1877–1886 http:// www.jstor.org/stable/1941592. H.J.G. Jung, K.P. Vogel, Lignification of switchgrass (Panicum virgatum) and big bluestem (Andropogon gerardii) plant part maturation and its effect on fibre degradability, J. Sci. Food Agric. 59 (1992) 169–176. J.W. Macadam, M.S. Kerleyj, E.J. Piwonkas, Tiller Development Influences Seasonal Change in Cell Wall Digestibility of Big Bluestem, (1996) 79–88. N. Waramit, K.J. Moore, A.H. Heggenstaller, Composition of native warm-season grasses for bioenergy production in response to nitrogen fertilization rate and harvest date, Agron. J. 103 (2011) 655–662, http://dx.doi.org/10.2134/ agronj2010.0374. J.H. Grabber, G.A. Jung, R.R. Hill, Chemical composition of parenchyma and sclerenchyma cell walls isolated from orchardgrass and switchgrass, Crop Sci. 31 (1991) 1058–1065, http://dx.doi.org/10.2135/cropsci1991.

38