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Agricultural and Meteorology 268 (2019) 269–278

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Agricultural and Forest Meteorology

journal homepage: www.elsevier.com/locate/agrformet

Native and managed buffelgrass in drylands: Implications for carbon and water fluxes T ⁎ César Hinojo-Hinojoa, Alejandro E. Castellanosa, , Travis Huxmanb, Julio C. Rodriguezc, Rodrigo Vargasd, José R. Romo-Leóna, Joel A. Biedermane a Departamento de Investigaciones Científicas y Tecnológicas, Universidad de Sonora, Hermosillo, Sonora 83000, México b and Evolutionary Biology, Center for Environmental Biology, University of -Irvine, Irvine, CA 92629, USA c Departamento de Agricultura y Ganadería, Universidad de Sonora, Hermosillo, Sonora 83000, México d Department of Plant and Soil Sciences, University of Delaware, Newark, Delaware 19716, USA e Southwest Watershed Research Center, Agricultural Research Service, Tucson, AZ 85719, USA

ARTICLE INFO ABSTRACT

Keywords: and land-use change (LCLUC) between woody- and grass-dominated in drylands comprise ff Bu elgrass one of the largest uncertainties in the land CO2 sink. This is especially true for the widespread transition from to / caused by the establishment of exotic C4 grass species for grazing or through Eddy covariance biological invasion of these species, where information about its impacts on ecosystem CO2 fluxes is limited. For Land cover change studying this, we used three years of eddy covariance measurements of net ecosystem production (NEP), gross Sonoran primary production (GPP), ecosystem respiration (R ) and evapotranspiration (ET) over a Sonoran Desert Carbon and water fluxes eco ff Grass encroachment shrubland and an adjacent grazing savanna of bu elgrass (Cenchrus ciliaris L.), established 35 years ago. At monthly, seasonal and annual time scales, we assessed whether between-site differences in CO2 fluxes were related to differences in ecosystem water use, measured as the fraction ET to , water use efficiency

(WUE, i.e. the ratio between GPP and ET) and/or to the relation between Reco and GPP. Although the savanna had higher WUE than the shrubland, its NEP was limited by water use, due to limitations in leaf area index and likely rooting patterns. Conversely, the savanna had higher NEP than the shrubland during fall to spring due to increased WUE; possibly due to activity of buffelgrass and remaining woody species using (summer) water from deeper soil layers. However, differences across these compensated each other at the inter-annual scale, and both sites had comparable net carbon sinks over the three-year study period. Further studies are needed to understand and reduce the uncertainty associated with carbon and water fluxes associated with LCLUC in dryland ecosystems.

1. Introduction studied than drylands, LCLUC typically results in net CO2 emissions to the atmosphere due to biomass loss and decomposition (Le Quéré et al. Dryland ecosystems have a key role in the trend and interannual 2016). Changes in the net carbon balance in drylands following LCLUC variability of the global land (Ahlstrom et al., 2015; Poulter are still unclear and represent one of the largest uncertainties in the et al., 2014). These globally distributed ecosystems have large temporal global carbon balance (Hayes et al., 2018; King et al., 2007). and spatial variability in net ecosystem production (NEP), and conse- Woody and grasses are dominant in drylands (Safriel et al., quently in CO2 uptake by gross primary production (GPP) and emis- 2005). The transitions from woody- to grass-dominated ecosystems and sions to the atmosphere by ecosystem respiration (Reco)(Ahlstrom vice versa are recognized as the most widespread LCLUC across dry- et al., 2015; Biederman et al., 2016, 2017). Furthermore, extensive lands (Barger et al., 2011; Marshall et al., 2012; Sala and Maestre, land-cover and land-use change (LCLUC) has been documented across 2014). The gradual change over decades from grass- to woody-domi- drylands (Safriel et al., 2005), which in turn directly influence the nated ecosystems is referred as woody encroachment, which is regu- magnitude of these fluxes (Le Quéré et al., 2016; Baldocchi, 2008). In lated by interactions among climate, , and management temperate forest ecosystems, which have traditionally have been more across drylands (Van Auken, 2009). In the opposite direction, a change

⁎ Corresponding author. E-mail address: [email protected] (A.E. Castellanos). https://doi.org/10.1016/j.agrformet.2019.01.030 Received 6 March 2018; Received in revised form 14 November 2018; Accepted 21 January 2019 0168-1923/ © 2019 Elsevier B.V. All rights reserved. C. Hinojo-Hinojo et al. Agricultural and Forest Meteorology 268 (2019) 269–278 from woody- (e.g., shrublands) to grass-dominated ecosystems could modified by land cover: the relation of GPP with ET, and the relation of occur by the anthropogenic introduction of highly productive and Reco with GPP (Biederman et al., 2016). ET/GPP describes how avail- -resistant African/Asian C4 grass species to increase forage able water is used for photosynthesis, reflecting the ecosystem water- production (Castellanos et al., 2002, 2010; Marshall et al., 2012; use efficiency. Meanwhile, Reco/GPP reflects how carbon availability Williams and Baruch, 2000). Vegetation structure may be dramatically drives ecosystem respiration, and is sensitive to changes in vegetation, changed within a through land clearing of native vegetation and carbon pools and allocation caused by LCLUC or disturbances seeding of grass or more gradually through invasion of exotic grasses (Baldocchi, 2008; Biederman et al., 2016). In this context, C4 grasslands (Arriaga et al., 2004; Williams and Baruch, 2000). These bidirectional have higher water-use efficiency than woody-encroached ecosystems

LCLUC transitions could have important consequences for regional-to- dominated by C3 plants (Emmerich, 2007; Kurc and Small, 2007; Scott global carbon budgets, but large uncertainties remain (Barger et al., et al., 2014). This advantage is counteracted by an increased Reco/GPP, 2011; Houghton et al., 2012 Jackson et al., 2002; Pacala et al., 2001). which is likely related to the high proportion of root biomass in grasses Woody encroachment has been more extensively studied (Petrie et al., (Scott et al., 2014; Petrie et al., 2015). The balance between these re- 2015; Scott et al., 2006, 2014), and because of the lack of information, lationships further contributes to explain the lower NEP of grasslands larger uncertainties exist for the shrubland-to- transition and when compared to woody-encroached sites. It is unclear how a LCLUC particularly the consequences for whole-ecosystem stocks and annual in the opposite direction (i.e., shrublands converted into C4 grasslands) fluxes (Bradley et al., 2006; Prater et al., 2006). influences NEP in dryland ecosystems. We could expect diminished NEP Woody encroachment increases whole-ecosystem carbon fluxes by reversing the typical results of woody encroachment. However (NEP, Reco, GPP) in drylands because access to deeper soil and exotic grass species have historically been selected for high productivity groundwater sources supports longer growing seasons (Scott et al., under limiting abiotic conditions (Cox et al., 1988) and could lead to a 2006, 2014; Petrie et al., 2015), and because encroaching woody spe- different outcome. cies can physiologically outperform native grass species under a wide Buffelgrass (Cenchrus ciliaris L.) is one of the main C4 exotic grass range of drought conditions (Barron-Gafford et al., 2012; Throop et al., species used for converting xeric shrublands into more productive 2012). Changes are expected in evapotranspiration (ET), the water flux grasslands/savannas for cattle grazing over America and (Cox of available soil moisture (SM) that remains after infiltration from et al., 1988; Marshall et al., 2012). Notably, the Sonoran Desert of precipitation (P), and losses to runoff (R) and drainage (D) beyond the and the US may be one of the region's most heavily impacted by rooting zone (Fig. 1). ET approximates the available water that drives these practices (Bravo-Peña et al., 2010; Bravo-Peña and Castellanos, carbon fluxes (Biederman et al., 2016), and ET/P represents the fraction 2013; Castellanos et al., 2002, 2010; Marshall et al., 2012). This per- of water used at the ecosystem scale. Two relations are particularly ennial bunchgrass has one of the highest photosynthesis rates important and explain the variation of NEP in drylands, which can be (Castellanos et al., 2010; Larcher, 2014) and can physiologically out-

perform dominant C3 woody species from the Sonoran Desert (Castellanos et al., 2010) enabling exotic buffelgrass savannas to be substantial carbon sinks (Hinojo-Hinojo et al., 2016). However, remote sensing estimates suggest that buffelgrass-dominated ecosystems have less above—ground biomass production than Sonoran Desert - lands (Bravo-Peña and Castellanos, 2013; Franklin et al., 2006; Franklin and Molina-Freaner, 2010). Thus, research is needed to contribute to our understanding of shrubland—to—grassland transitions across dry- land ecosystems.

In this study we compare three years of CO2 and water fluxes over a shrubland and an adjacent ecosystem converted to exotic buffelgrass savanna ˜35 years ago to address the following questions: 1) Does the change from shrubland into an exotic buffelgrass savanna modifies

carbon fluxes (e.g., NEP, GPP and Reco) at seasonal and annual scales?; and if so, 2) are changes related to responses in water use (ET/P), water

use efficiency (GEP/ET) and/or the relation between Reco/GPP? We hypothesize that the high-productivity potential and water-use effi-

ciency of buffelgrass will compensate with a high Reco/GPP and lower water use in the savanna; which is characterized by a shallower rooting structure and allows this ecosystem to sustain similar or higher NEP than in the shrubland. Our ultimate aim is to contribute to the discus- sion about the bidirectional changes of -to-grass transitions across globally important drylands ecosystems.

2. Materials and methods

2.1. Study sites

Two adjacent sites representing a native shrubland and a buffelgrass savanna were selected for installing eddy covariance (EC) systems to measure ecosystem scale carbon dioxide (CO ), water and energy Fig. 1. Conceptual diagram of the main ecosystem CO2 and water fluxes in a 2 native shrubland and one changed to exotic buffelgrass savanna, and the main fluxes. These sites are part of the Mexican eddy covariance network structural characteristics which may influence the magnitude of those fluxes. (MexFlux, Vargas et al., 2013) and are located in Sonora, Mexico,

GPP: gross primary production, Reco: ecosystem respiration, ET: within the Southeastern portion of the Sonoran Desert, a heavily im- Evapotranspiration, P: precipitation, R: runoff, D: drainage (For interpretation pacted region by LCLUC for buffelgrass since its introduction to Mexico of the references to colour in this figure legend, the reader is referred to the web in 1960′s(Bravo-Peña and Castellanos, 2013; Castellanos et al., 2002, version of this article). 2010 Franklin et al., 2006). Both sites are located in El Churi, a private

270 C. Hinojo-Hinojo et al. Agricultural and Forest Meteorology 268 (2019) 269–278

Fig. 2. Location of the study area within the Sonoran Desert and of the eddy covariance (EC) towers in the . See Figure S1 on supplementary material for further details on footprint analysis. ranch near La Colorada, Sonora, where rotational management of cattle of photosynthetic activity between July and September (period of grazing is the prevalent activity throughout the year. The sites are se- monsoon ), but some activity can occur during other seasons given parated by 1.8 km, thus both are exposed to the same regional en- sufficient precipitation (Hinojo-Hinojo et al., 2016). The species Olneya vironmental conditions but with different vegetation cover. tesota, velutina, Encelia farinosa and Lycium berlandieri can re- The shrubland site (located at 28° 41′ 53.60″ N, 110° 32′ 20.59″ W, tain their leaves during most of the year when sufficient soil moisture with 450 m elevation; Fig. 2) has a Sonoran Desert scrub vegetation remains in their rooting zone (Castellanos et al., 2016). Terrain is flat characteristic of the of Sonora (Brown, 1994). The vegetation within the tower footprints with an average slope < 2% (Fig. 2). Soils cover is composed of 14% (Olneya tesota, Fouquieria macdougalii, are calcic regosol and haplic phaeozem with loamy sand texture with Ipomoea arborescens, in descending order of importance) and 28% 0.6–2.6 % of organic matter content (Celaya-Michel et al., 2015). shrubs (Jatropha cardiophylla, Encelia farinosa, Mimosa laxiflora, Lycium berlandieri)(Celaya-Michel et al., 2015). During the study period, in- terspaces between trees and shrubs were mostly covered with summer- 2.2. Eddy covariance and meteorological measurements active herbs, grasses and litterfall. Vines can also have some cover during summer (about 10%). Mean vegetation height is nearly 1 m, but The instrumentation installed in both sites allowed us to measure a few of the tallest trees can grow up to 7 m. The EC tower is located at the net ecosystem CO2 exchange (NEE), evapotranspiration (ET), and the center of homogeneous vegetation for more than 1 km in every energy fluxes between the ecosystems and the atmosphere using the direction (Fig. 2, Footprint analysis in Supplementary material, Figure eddy covariance technique (Aubinet et al., 2012) and to monitor the S1). environmental conditions under which these fluxes occur. In this study The buffelgrass savanna site (located at 28° 42′ 40.32″ N, 110° 32′ we used six site—years of EC comparative data (from March 2013 to the 58.14″ W, with 399 m elevation; Fig. 2) was a former Sonoran Desert end of 2015). At the buffelgrass site, the EC system on a 6 m-tall tower scrub converted to savanna approximately 35 years ago through se- consisted of a sonic anemometer (CSAT3, Campbell Scientific, Logan, lective land clearing and re-cleared periodically, with only few of the UT, USA) for measuring 3D components of wind velocity and sonic dominant species left (J. Dueñas, oral communication, June 2009), temperature and an open path CO2/H2O gas analyzer (Li-7500, and some shrub and other species that have partially recolonized the LI−COR, Lincoln, NE, USA), both sampling at 10 Hz. Also at the top of site since. The vegetation cover was 32% buffelgrass (Cenchrus ciliaris), the tower, net radiation (NR Lite, Kipp & Zonen, Delft, The Nether- 3% trees (Olneya tesota and Prosopis velutina), and 7% shrubs (mostly lands) and air temperature and relative humidity (HMP45C, Vaisala Mimosa laxiflora, and Jatropha cardiophylla). During the study period, Inc., Vantaa, Finland) were measured every minute. All other en- interspaces between plants had a cover of summer active herbs, grasses vironmental sensors had a sampling rate of 15 min including a and litterfall. Mean vegetation height is about 0.5 m, but a few trees gauge (TR-525USW-R, Electronics, Dallas, TX, USA) and two grow up to 4 m. pairs of soil heat flux plates (HFP01-L50, Hukseflux, Delft, The Neth- Climate for these sites (30-year averages from nearby station 26268, erlands) located at 5 cm depth under buffelgrass cover and beneath San Jose de Pima, Servicio Meteorológico Nacional) is warm-semi-arid, open spaces (with annual herbs cover). All data were sampled and with a mean annual precipitation of 476 mm, 70% of which occurs stored using a data-micrologger (CR3000, Campbell Scientific, Logan, during the summer monsoon as thunderstorms. Mean annual tem- UT, USA). perature is 22.8 °C, with mean maximum in the hottest month (June) of At the shrubland site, the EC system on a 9 m tall tower had a 3D 40.1 °C, and a mean minimum of 5.4 °C in the coldest month (January). sonic anemometer (Wind Master Pro, Gill Instruments) and an open

Most plant species from both sites are with the major period path CO2/H2O gas analyzer (Li-7500 A, LI−COR, Lincoln, NE, USA) at the top, both taking measurements at 10 Hz. All other sensors measured

271 C. Hinojo-Hinojo et al. Agricultural and Forest Meteorology 268 (2019) 269–278 at a sampling rate of 1 min. Also at the top, the tower has a net (either a single season or a single year). Given that the daily mean radiometer (NR Lite2, Kipp & Zonen, Delft, Netherlands), and at 6 m multiplied by the number of days equals the sum for a given period, any height an air temperature and relative humidity probe (HMP-155, between-site difference detected at daily means could be interpreted as Vaisala Inc., Vantaa, Finland). Rainfall was measured with a rain gauge a potentially significant difference that influence flux sums. For the (TR-525 M, Texas Electronics, Dallas, TX, USA). Soil heat flux was seasonal flux comparison, we split each year in two seasons; (a) summer measured (HFP01SC, Hukseflux, Delft, The Netherlands) at 5 cm depth from July to September, where most of the annual precipitation and the under tree, shrub and open space cover. All 1-minute frequency data highest flux rates occur, and (b) the rest of the year including data from was sampled with a datalogger (Xlite 9210, Sutron, Sterling, VA, USA) January to June and October to December where rainy events are un- and 1 min and 10 Hz frequency data are stored in the interface unit (Li- common and flux rates tend to be low. 7550, LI−COR, Lincoln, NE, USA) of the gas analyzer. 2.5. Drivers of ecosystem carbon flux differences between-sites 2.3. Data processing Our second research question was about identifying whether be- The high frequency (10 Hz) raw data processing and flux calculation tween-site differences in ecosystem carbon fluxes were related to dif- were performed on Eddy Pro software (v. 4-5, LICOR Biosciences) on ferences in the amount of water used by the ecosystem; in terms of

30-minute blocks. Displacement height and roughness length settings water use efficiency or in the relation Reco/GPP. Both monthly ET and used on Eddy Pro were set to be a function of vegetation height at the seasonal ET/P were used as a measure of water use by the ecosystem, as sites (see Study sites section). Prior to flux calculation, the following both have been shown to represent well the available water that drives processing was performed on raw data: despiking and other statistical CO2 fluxes (Biederman et al., 2016, 2017). Water-use efficiency was quality tests (following Vickers and Mahrt, 1997), time lags compen- assessed at the monthly scale in two ways: (a) as the linear relationship sation due to instrument separation by maximizing covariance, and of GPP against ET, which gives an estimate of realized water-use effi- double axis rotation for wind components (Wilczak et al., 2001). Angle ciency at the ecosystem scale (WUE) (Emmerich, 2007); and (b) as the of attack correction (Nakai and Shimoyama, 2012) was performed on linear relationship of the product of GPP and vapor pressure deficit the shrubland anemometer data to compensate for errors in wind ve- (VPD) against ET, which is an estimate of inherent water use efficiency locity data due to instrument design, whereas the anemometer used at (WUEi) and better reflects changes in plant physiology by controlling the buffelgrass savanna is designed to minimize such errors, and this for the effect of VPD (Beer et al., 2009). The linear relationship of correction was not used. Turbulent fluxes of CO2, ET, sensible (H) and monthly Reco against GPP was also assessed. To compare how sites latent heat (LE) were calculated using the vertical component of wind differed in these relationships, we fit the data to a statistical model velocity, CO2 and water vapor molar densities, and sonic temperature. evaluating the effects of the independent variable (either ET or GPP), These fluxes were corrected for frequency spectral attenuations site, and independent variable*site interaction on the dependent vari- (Moncrieff et al., 1997 and 2004), humidity effects on sonic tempera- able. The site effect gives an estimate of mean displacement of the ture (van Dijk et al., 2004), and air density fluctuations (Webb et al., dependent variable between sites, when all other effects are controlled. 1980). The interaction effect gives an estimate of the amount of between-site As a quality control, we discarded data under the following condi- change in slopes of the independent vs dependent variables. We inter- tions: 1) when data failed tests for steady state and sufficiently devel- pret any statistically significant effect of site and/or interaction as a oped turbulence assumptions of the EC technique (Mauder and Foken, significant change in WUE, WUEi or Reco/GPP. 2004), 2) fluxes measured below a friction velocity threshold to avoid keeping underestimated nighttime flux data at conditions of low air 2.6. Vegetation phenology mixing, 3) during rain events, 4) when bird feces occluded the gas analyzer lenses dropping CO2 concentration below 350 ppm (which We followed vegetation phenology through remote sensing data and caused substantial overestimation of CO2 fluxes, personal observation). with field observations to assess whether changes in flux dynamics and Friction velocity thresholds for the shrubland were 0.15–0.13 m/s while relations could be related to changes in development or phe- savanna thresholds were 0.1 m/s for all years. Quality control and nology of dominant species. For remote sensing data, we used time system failure resulted in an annual NEE gap fraction of 37–51% for series of 8-day composites of leaf area index (LAI) derived from MODIS shrubland, and 40–51 % for the savanna, depending on the year. The (Moderate-Resolution Imaging Spectroradiometer, MOD15A2, collec- estimation of friction velocity thresholds, gap-filling and NEE flux tion 5) for the same dates as flux measurements obtained from the partitioning into Reco and GPP were performed according to Reichstein webpage of Distributed Active Archive Center for Biogeochemical et al. (2005) using the online tool available at www.bgc-jena.mpg.de/ Dynamics (http://daac.ornl.gov/MODIS/). Linear regression analysis MDIwork/eddyproc/. We followed the ecosystem-centered nomen- was used to assess how LAI responded to seasonal rainfall and how LAI clature where Net Ecosystem Production (NEP = - NEE) positive values influenced CO2 fluxes at both sites. For field observations of leaf phe- indicate net carbon uptake by the ecosystem and negative values in- nology, we qualitatively censed the presence of green leaves on 10 in- dicating net carbon emission to the atmosphere (Chapin et al., 2006). dividuals of the dominant species (> 0.5% cover) during visits to the Monthly, summer and annual flux sums were obtained by adding up sites every three to four weeks throughout the study period. Any given through time the half-hourly gap-filled data. We estimated uncertainty species was considered to have green leaves when they were the most in flux sums derived from gapfilling processing (obtained from the abundant in more than six individuals. Leaf phenology was combined in online tool, following Reichstein et al., 2005) and from random errors some of our analyses placing special attention to whether buffelgrass and long gaps (following Richardson and Hollinger, 2007). We ana- phenology could help explain the observed differences in fluxes and lyzed the energy balance closure for the sites as a way to assess the flux relations between sites. All statistical analyses were performed in accuracy of the eddy covariance measurements (Supplementary mate- JMP version 9.0.1 (SAS Institute, Inc, 2010). rial, Figure S2). 3. Results 2.4. Comparison of carbon and water fluxes between sites 3.1. Temporal dynamics of meteorological conditions and ecosystem fluxes To answer our first research question, we compared seasonal and annual CO2 fluxes between the study sites. For this, a t-test was per- Marked differences in precipitation amounts and seasonal timing formed to compare mean daily flux values for the period of interest characterized the three years of study (Fig. 3a–c). In 2013, annual

272 C. Hinojo-Hinojo et al. Agricultural and Forest Meteorology 268 (2019) 269–278

Fig. 3. Annual course of monthly rainfall (a–c), mean daily air temperature (d–f), and vapor pressure deficit (g–i) at the shrubland (black symbols) and buffelgrass savanna sites (gray symbols) during the study period. In a–c, bars represent monthly rainfall during the study period and lines represent long-term average monthly rainfall. Vertical dotted lines are the limits between seasons (i.e. Winter, Spring, Summer and Fall).

rainfall (253 mm) was below the long-term average, mostly dominated between years and sites. During the years with minimal rains in winter (86%) by summer rains (Fig. 3a), which also had the coldest winter of and spring (2013 and 2014), summer contribution to the total annual the three years (Fig. 3d). In contrast, total annual precipitation in 2014 NEP was over a hundred percent in the shrubland, but only 59–89 % in was 412 mm with a rainy summer but dry winter and spring (Fig. 3b–c), the buffelgrass savanna (Table 2). In those same years, summer con- and in 2015, a wet year (505 mm), rains were spread throughout the tributed with 68–86 % of the yearly fluxes of GPP, Reco and ET at both year with above-average precipitation in winter and spring but below- sites, with about 7–18 % higher contribution of carbon fluxes and 1–7 average in summer (Fig. 3c). Temperature patterns were similar for % higher ET in the shrubland than the buffelgrass savanna. However, years 2014 and 2015 (Fig. 3e-f), which drove daily mean air VPD during the more widespread rainfalls of 2015 (with rains in winter, highest during late spring (4 kPa), and 1–3 kPa for the rest of the sea- spring and summer), summer contribution to annual flux totals was 46 sons (Fig. 3g–i). Thus, the three years allowed us to compare CO2 and to 56% (ET and NEP respectively) in the buffelgrass savanna, and 46 water fluxes over a wide range of conditions for the two sites, with (ET) to 72% (NEP) in the native shrubland. weekly and monthly values providing a first approach for comparisons. Leaf area index was related to summer precipitation. We found 1.6 Important differences were detected in monthly fluxes and 8-day times higher slope between summer rainfall and LAI for the shrubland LAI dynamics between sites (Fig. 4). Except for the summer, buffelgrass site than for the buffelgrass savanna (Fig. 6a), but no differences in the savanna had higher monthly CO2 fluxes at other times during the three slope of the relationship between LAI and NEP were found (Fig. 6b). years (Fig. 4g–o), especially for GPP and NEP, but these were not ex- ff – clusively related to bu elgrass activity in 2013 and 2014 (Fig. 4a b). 3.3. Comparison of water use, water use efficiency and Reco/GPP On-site phenological observations showed that bufflegrass had green leaves mainly during summer in 2013 and 2014, but rain patterns in Lower ET/P was always found at the buffelgrass savanna site. 2015 allowed this species to maintain green leaves during seasons of Annual ET/P was lower during the rainy years (2014 and 2015) and the year that otherwise they would not have been active already every summer season during our period of study in the buffelgrass sa- – fl (Fig. 4a c). The shrubland had higher CO2 uxes, ET and LAI than the vanna (Table 2). The buffelgrass savanna had also higher WUEi than the buffelgrass savanna early in the summer seasons of 2014 and 2015, but shrubland, either when buffelgrass was active or inactive (Fig. 5a). The −1 −1 were similar and highly variable for both sites during 2013 (Fig. 4). savanna assimilated about 2.4 g C mm H2O month and 188 g C hPa and had higher GPP*VPD for a given ET (marginally significant 3.2. Annual and growing season comparisons of ecosystem fluxes interaction effect and significant site effect in Table 1) than the shrubland. Our estimates indicate that the shrubland could only had −1 Annual CO2 fluxes ranged from being carbon neutral to a sink higher NEP than the savanna if it diminished 5.5 mm month ET or during the years of study. Carbon and water fluxes for the years 2013 to more (y=-5.8 + 1.06x, Fig. 7), which only happened during summer 2015 ranged from being carbon neutral in the shrubland in 2013 (t-test months and few times in other seasons. against 0: t = 0.0544, P = 0.3524) to a sink in the buffelgrass savanna (year 2013). Both sites were carbon sinks during 2014 and 2015 and no 4. Discussion statistically significant differences were found between-sites for both years. Flux uncertainties for annual NEP estimates were ± 65 to 68 g C 4.1. Comparison with current understanding of reverse LCLUC transitions − − m 2 for the shrubland and ± 66 to 78 g C m 2 for the buffelgrass sa- from woody- to grass- dominated ecosystems vanna. When summed over the three years, both sites had similar NEP − (393 and 414 g C m 2 year-1 for shrubland and savanna, respectively). Our study supports the hypothesis that a LCLUC from shrubland to −2 -1 Reco at the savanna was 75–90 g C m year higher than the shrubland savanna dominated by a highly productive exotic C4 grass may result in during 2013 and 2015, but GPP at the savanna compensated for those an ecosystem that is as productive as the shrubland. This contradicts the differences. Sites had similar ET during 2013, but the savanna had prediction from the reverse transition, woody encroachment, where lower ET than the shrubland during 2014 and 2015 and lower ET/P woody-dominated ecosystems tend to have higher NEP than grass- ratios, which were evident both in the total annual and during the dominated ecosystems (Barger et al., 2011; Scott et al., 2006, 2014; summer (Table 2). Petrie et al., 2015). Our findings are supported by an experimental The importance of summer fluxes to the total annual was always study that found increasing carbon pools in shrublands invaded by higher, although their magnitude and annual sums were different exotic grasses (Wolkovich et al., 2010). Here, we discuss mechanisms

273 C. Hinojo-Hinojo et al. Agricultural and Forest Meteorology 268 (2019) 269–278

Fig. 4. Annual course of a–c) leaf area index, d–f) monthly evapotranspiration (ET), g–i) net ecosystem production (NEP), j-l) ecosystem respiration (Reco) and m–o) gross primary production (GPP) for the shrubland (black symbols) and buffelgrass savana (grey symbols) sites. Horizontal grey bars in a–c) indicate periods of green leaf phenology of buffelgrass. Vertical dotted lines as in Fig. 3.

changes did not operate in the same way at our sites. Growing season length was fairly similar between sites (as suggested by time series of NEP and GPP, Fig. 4) despite increased water availability at the shrubland (ET/P from Table 2), probably because vegetation at both sites is dominated by deciduous and highly seasonal species (Turner

et al., 1995). Furthermore, the relationship between GPP and Reco did not differ between sites (Fig. 5b). Although Reco was higher at the sa- vanna than shrubland during some years (2013, 2015), GPP throughout those years compensated such increases at both sites (Fig. 5b), which agrees with our hypothesis that the high productivity potential of

buffelgrass would compensate the typical high Reco/GPP relation ffi Fig. 5. a) Intrinsic water-use e ciency and b) Reco/GPP relationship for the commonly reported for grass-dominated ecosystems. Alternatively, sites ff shrubland (black symbols-full line) and bu elgrass savanna (open symbols- differed in their seasonal contributions to annual fluxes, making the dotted line) sites. Star symbols represent months when buffelgrass was active, shrubland NEP more dependent on the summer season than the buf- and lines are linear regressions for each site. Labels as in Fig. 4 and text. felgrass savanna (Table 2, Fig. 7). and feedbacks operating in both ecosystems that could explain the observed pattern and possible implications of bidirectional woody- 4.2. Water use and water use efficiency as drivers of seasonal differences in grassland transitions on dryland ecosystem carbon fluxes. ecosystem fluxes When compared, the buffelgrass savanna had either higher or si- milar annual NEP than the shrubland in the same year but summed over Although both sites had similar NEP sums over the three years, the the study period (3 years) the sites were net carbon sinks and ended up underlying seasonal fluxes and water-carbon relationships differed with closely similar NEP. This contrasts with higher NEP expected from among sites, specifically water use (ET/P, Table 2), and water-use ef- woody-dominated compared to grass-dominated ecosystems attributed ficiency (GPP*VPD/ET, Fig. 5). The buffelgrass savanna had higher to woody plants having access to deeper water sources, allowing higher WUEi than the shrubland throughout the year, supporting our hy- ET/P ratio, longer growing seasons, and lower Reco/GPP (Huxman pothesis that at least part of this increase in WUE is due to the C4 et al., 2005; Petrie et al., 2015; Scott et al., 2006, 2014). These expected physiology of buffelgrass, as has been found for other C4 dominated

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Table 1

Results of the statistical comparison of monthly water use efficiency (WUE), intrinsic water use efficiency (WUEi) and the relationship of Reco/GPP the shrubland and the buffelgrass savanna site.

R2 Intercept Independent variable effect Site (savanna) effect Independent variable × Site (savanna) effect

WUE (GPP vs ET) 0.90 −5.91 1.95**** 7.28* 0.02 WUEi (GPP*VPD vs ET) 0.90 25.86 31.42**** 189.17**** 2.43* Reco vs GPP 0.91 9.60**** 0.65**** 0.41 0.02

*p < 0.1 (marginally significant). **p < 0.05. ***p < 0.01. ****p < 0.001. When no significant interaction effect is found, the independent variable effect corresponds to the overall slope. When interaction effect is statistically significant, the independent variable effect corresponds to that of shrubland site and the independent variable x Site effect correspond to the amount of change in the slope of the savanna in relation to that of the shrubland. The Site (savanna) effect corresponds to the difference of the means of the dependent variable of the savanna in relation to that of the shrubland when the other factors are controlled.

grasslands when compared to C3 dominated shrublands (Ehleringer and rainy season. Monson, 1993; Emmerich, 2007; Scott et al., 2014, 2015). However, the We found that LAI is another mechanism that may be limiting NEP savanna had lower NEP and ET than shrubland during most summer in the savanna. LAI was similar for both sites in the low range of pre- months (Fig. 7) despite having higher WUE, which suggests water cipitation, but differences increased as summer rainfall increased, with limitation. Two biotic mechanisms appear to be limiting water use and shrubland LAI exceeding that of the buffelgrass savanna by up to 60% NEP at the savanna during summer. First, the conversion of a shrubland in wet years (Fig. 6). Knapp et al. (2008) reported similar patterns and into a buffelgrass savanna reduces the cover of most plant functional suggested that grasses may have an intrinsic LAI limitation due to their types, especially woody species with deep roots (Saucedo-Monarque architecture, with meristematic disposition only close to or below the et al., 1997; Castellanos et al., 2002, 2010; Franklin and Molina- soil surface, while the branching and meristem arrangement of shrubs Freaner, 2010). At the savanna site, deep-rooted woody species cover allow for greater canopy deployment and higher possible values of LAI. less than 10%, and buffelgrass and annual plants are known to have Because LAI is one of the parameters that greatly determine CO2 and roots limited to the top 60 cm of soil (Forseth et al., 1984; Mnif and water fluxes over ecosystems (Allen et al., 1998; Bonan, 1993), these Chaieb, 2009). Thus, most plant cover at the savanna is dependent on differences in canopy responses contribute to explain most between-site shallow soil water availability. In the shrubland, at least 30% of its differences on summer fluxes. Taking both limitations into account, − cover is deep-rooted woody plants, and there is an important propor- when the shrubland increase ET by more than 5 mm month 1 above the tion of herbs and shrubs with shallow roots, thus allowing this eco- savanna, the effect of ET over NEP in the shrubland can surpass the system to better exploit water throughout the soil profile during advantage of higher WUE of the buffelgrass savanna (Fig. 7). summer and thus allowing higher summer transpiration and associated During the seasons of fall, winter and spring, the buffelgrass sa- GPP (Castellanos et al., 2016; Celaya-Michel et al., 2015 Huxman et al., vanna had higher NEP than the shrubland, mostly related to increased 2005). However, the small proportion (˜10%) of deep-rooted woody GPP as a consequence of increased WUE (Figs. 4 and 5). The higher GPP plants remaining in the savanna may benefit at other seasons, from the and WUE could be attributed to the physiology of C4 photosynthesis deep water that buffelgrass was not able to utilize during the summer when buffelgrass was active (e.g. winter and spring of 2015) in

Table 2 Annual and summer fluxes and seasonal contributions for the study years at shrubland and buffelgrass savanna sites. P values are for between-site t-test comparison for the same period.

Annual sums Summer sums Summer contribution

2013* 2014 2015 2013 2014 2015 2013 2014 2015

− Net ecosystem production (g C m 2) Shrubland 16 183 193 36 193 139 222 105 72 Savanna 75 140 199 44 125 112 59 89 56 p 0.029 0.318 0.843 0.772 0.069 0.215 Ecosystem respiration (g C m−2) Shrubland 326 561 674 261 448 337 80 80 50 Savanna 402 557 763 283 406 368 70 73 48 p 0.017 0.938 0.026 0.085 0.005 0.012 − Gross primary production (g C m 2) Shrubland 343 744 867 298 641 476 87 86 55 Savanna 477 697 962 327 531 480 68 76 50 p 0.005 0.579 0.127 0.383 0.017 0.870 Evapotranspiration (mm) Shrubland 236 400 582 194 324 268 82 81 46 Savanna 246 321 519 185 257 240 75 80 46 p 0.722 0.044 0.047 0.555 < 0.001 0.095 Evapotranspiration / Precipitation Shrubland 0.94 0.97 1.15 0.9 0.84 1.15 Savanna 0.97 0.78 1.03 0.85 0.66 1.03

* Data for winter 2013 is missing at the shrubland site. Thus, annual flux sums for 2013 at both sites were based on data from March 6 through the rest of the year. − Omitting winter data may cause and error of around ± 7 g C m 2 or less as this is the flux that we have registered during the winters at both sites for 2013 and 2014.

275 C. Hinojo-Hinojo et al. Agricultural and Forest Meteorology 268 (2019) 269–278

Fig. 6. a) Peak summer leaf area index response to seasonal precipitation and b) the effect of leaf area index on net eco- system production. Black symbols are for the shrubland and gray symbols for the buffelgrass savanna. Numbers in a) are years for each pair of points. Arrow is the six year average of summer precipitation in our sites (2009–2015).

summer gives evidence of its use (Castellanos et al., 2016; Celaya- Michel et al., 2015). Deep soil water accumulation could be expected in sites invaded with exotic grasses, as suggested by modeling studies of water balance in drylands (Wilcox et al., 2012). This evidence suggests that the high WUE and biological limitations at the savanna, because

the buffelgrass C4 physiology, cause a lower ET/P during summer rainy seasons and years (e.g., 2014 and 2015), and results in the observed water accumulation that feedbacks to the activity at the savanna during dry fall, winter and spring seasons (Fig. 8).

5. Concluding remarks

There is a long way ahead the scientific community to understand how LCLUC impacts NEP when woody shrublands change to

C4—grass—dominated ecosystems. The high productivity, photosynth- esis rates, resource-use efficiency, and other traits of C4 exotic grass- es—dominated ecosystems, can make important differences in their impact and feedbacks of these transitions from those reported in woody encroachment studies (Huxman et al., 2005; Petrie et al., 2015; Scott Fig. 7. Between-site difference in evapotranspiration as a driver of the differ- et al., 2014; Wolkovich et al., 2010). By using the EC techniques over ence in net ecosystem production for shrubland buffelgrass savanna sites. ff Closed circles are values for summer months, and open circles are for months adjacent shrubland and bu elgrass savanna sites, we documented that fl from the other seasons. such LCLUC altered the temporal dynamics of carbon uxes, and were able to link these differences to changes in water use and WUE. The representation of photosynthetic pathway, rooting pattern, and differ- agreement with our hypothesis that buffelgrass activity would enhance ential canopy responses were the main factors responsible for such WUE. Unexpectedly, WUE in the savanna was also higher during fall, changes (Fig. 8), all of these characteristics greatly modified by LCLUC winter and spring when buffelgrass was not active (e.g. winter and from shrublands to grass-dominated ecosystems. However, our findings spring of 2013 and 2014). We suggest that water infiltration into deeper suggest that the effects of temporal changes in water use and WUE on soil layers and subsequent use by native woody species that retain their NEP compensated in time, either between seasons (e.g., 2014) or be- leaves during most of the year, such as Prosopis and Olneya, increased tween years (e.g., 2013 vs 2014), to a similar NEP over the years despite GPP and thus WUE at the savanna. In agreement with this, water ac- the strong biotic, and vegetation-specific structural and functional dif- cumulation in soil at 1.5–2 m depth was found at the same savanna site ferences in land cover. Further studies on LCLUC from woody-domi- after rainy summer and fall seasons, in which a decrease in soil water nated to grass-dominated ecosystems should focus on understanding content at these depths during the drier months until the following how the impact of biotic traits (photosynthetic pathway, rooting

Fig. 8. Summary of seasonal differences in water use, water

use efficiency and CO2 fluxes between shrubland and exotic buffelgrass savanna. P: precipitation, ET: evapotranspiration,

GPP: gross primary production, Reco: ecosystem respiration, NEP: net ecosystem production. The symbols “-” and “+” in- dicate that savanna has a lower (or higher, respectively) magnitude of that process. Double symbols indicate the pro- cesses that are considered the main drivers of differences in NEP between sites.

276 C. Hinojo-Hinojo et al. Agricultural and Forest Meteorology 268 (2019) 269–278 pattern, differential LAI canopy responses) affect water use, WUE and Bravo-Peña, L.C., Castellanos, A.E., 2013. Tendencias del índice de la diferencia nor- NEP over ecological gradients such as rainfall (amount and season- malizada de la vegetación (NDVI) en el estado de sonora. Implicaciones potenciales ff sobre el sector pecuario en el contexto del cambio climático. In: Sanchez-Flores, E., ality), vegetation (over di erent kinds of woody dominated ecosys- Díaz-Caravantes, R.E. (Eds.), Aplicaciones de Percepción Remota y Análisis Espacial tems), and management conditions (low and high cover of exotic en la Evaluación del Uso del Territorio. Universidad Autónoma de Ciudad Juárez, Cd. grasses, overgrazed, non-overgrazed). Such studies will help to reduce Juárez, pp. 245–283. 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