Photosynthetic Temperature Responses of Co-Occurring Desert Winter Annuals with Contrasting Resource-Use Efficiencies and Differ

Journal of Arid Environments 91 (2013) 95e103

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Journal of Arid Environments

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Photosynthetic temperature responses of co-occurring desert winter annuals with contrasting resource-use efﬁciencies and different temporal patterns of resource utilization may allow for species coexistence

G.A. Barron-Gafford a,b,*,1, A.L. Angert b,1, D.L. Venable b, A.P. Tyler b, K.L. Gerst b, T.E. Huxman a,b,c,d a B2 Earthscience, Biosphere 2, University of Arizona, Tucson, AZ 85721, USA b Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA c Ecology and Evolutionary Biology, University of California, Irvine, CA 92617, USA d Center for Environmental Biology, University of California, Irvine, CA 92617, USA article info abstract

Article history: A mechanistic understanding of population dynamics requires close examination of species’ differences Received 20 June 2012 in how physiological traits interact with environmental variation and translate into demographic var- Received in revised form iation. We focused on two co-occurring winter annual species (Pectocarya recurvata and Plantago insu- 14 December 2012 laris) that differ in photosynthetic resource-use efficiency and demographic responses to environmental Accepted 15 December 2012 variation and covariation between temperature and water availability. Previous work showed that Pec- Available online 26 January 2013 tocarya has higher water-use efficiency and nitrogen allocation to light-driven dynamics of the Calvin cycle (J :V ) than Plantago, which is often associated with enhanced electron transport capacity at Keywords: max Cmax Chlorophyll fluorescence low temperatures and better light harvesting capacity. These traits could enhance Pectocarya photo- Photosynthetic temperature response synthesis during reliably moist but cool, cloudy periods following precipitation. We acclimated plants to Resource partitioning low and high temperatures and then measured gas exchange across a 30 C temperature range. As Respiration predicted, optimal temperatures of photosynthesis were lower for Pectocarya than Plantago. Additionally, Species coexistence Pectocarya experienced greater respiratory carbon loss than Plantago at higher temperatures (every 1 C Variable environments increase beyond 24 C increased the ratio of carbon loss to gain 9% and 27% in cold and warm-acclimated plants, respectively). These differential patterns of photosynthetic optimization and assimilation in response to differing rainfall distributions may have important implications for population dynamic differences and species coexistence. Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction

2 1 fi Abbreviations: Anet, steady-state photosynthesis (mmol CO2 m s ); Amax, Examining interspeci c differences in physiological traits can m 2 1 fl maximum photosynthetic rate ( mol CO2 m s ); Fo, initial uorescence illuminate the link between environmental variation and de- 0 fl when dark-adapted; F o, initial uorescence when light-adapted; Fm, maximum mographic variation and thereby contribute to a mechanistic un- fluorescence when dark-adapted; F0 , maximum fluorescence when light-adapted; m derstanding of population and community dynamics (McGill et al., Fs, steady state light-adapted fluorescence signal; Fv, variable fluorescence level 0 2006). In dryland ecosystems, precipitation exerts a dominant in- when dark-adapted ¼ (Fm Fo); F v, variable fluorescence level when light- 0 0 0 0 adapted ¼ (F m F o); Fv/Fm, maximum quantum yield of photosystem II; F v/F m, fluence on most biological processes, from short-term responses light-adapted PSII yield; Jmax, maximum electron transport rates; NPQ, non-pho- such as plant photosynthetic activity to longer-term demographic 0 0 0 tochemical quenching ¼ [(Fm F m)/F m]; qP, photochemical quenching ¼ [(F m Fs)/ 0 0 2 1 responses such as growth, survival and recruitment (Barron- (F m F o)]; Rd, respiration after 5 min in complete darkness (mmol CO2 m s ); Tacc, Gafford et al., 2012; Huxman et al., 2004; Schwinning and Sala, acclimation temperatures ( C); Tleaf, leaf temperature ( C); Tmeas, measurement 2004). Functional trait differences that underlie plant response to temperatures ( C); Topt, optimal temperature of photosynthesis ( C); VCmax , carboxylation capacity; WUE, water-use efficiency; D, leaf carbon isotope discrimination precipitation may explain within-year and between-year resource (ppm). partitioning among coexisting species (Chesson et al., 2004; * Corresponding author. B2 Earthscience, Biosphere 2, University of Arizona, Novoplansky and Goldberg, 2001). For example, species differences Tucson, AZ 85721, USA. Tel.: þ1 520 548 0388; fax: þ1 520 621 9190. fi E-mail address: [email protected] (G.A. Barron-Gafford). in physiology or phenology may cause species-speci c patterns of 1 These authors contributed equally to this work. resource-use in response to the same precipitation event, or they

0140-1963/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jaridenv.2012.12.006 96 G.A. Barron-Gafford et al. / Journal of Arid Environments 91 (2013) 95e103 may enable species to take advantage of precipitation sequences of precipitation events may contribute disproportionately to plant differing magnitudes and timing. Most examinations of biological seasonal carbon gain (Huxman et al., 2004), yet they may coincide responses to precipitation have focused on the direct effects of with low-temperature and low-light limitations for some species. increased soil moisture, but a more complete understanding will Therefore, enhancing photosynthesis under these conditions could require investigation of the sensitivity of resource gain to co- allow species to better exploit this resource-rich window of varying environmental factors such as light availability and opportunity. temperature. Photosynthetic carbon assimilation is strongly affected by Precipitation in deserts typically falls in discrete events that temperature, but many species exhibit a remarkable ability to may be clustered in space and time, and patterns of event clus- adjust photosynthetic processes to altered growth temperatures tering determine the amount of resources and the duration of their (Berry and Björkman, 1980). Temperature acclimation of photo- availability (Huxman et al., 2004; Noy-Meir, 1973; Reynolds et al., synthesis and respiration can allow plants to maintain relatively 2004). Monthly precipitation is highly variable between years, constant rates of net CO2 exchange as daily temperatures change with some years experiencing consistent precipitation across across the growing season. Desert plants have played an important a growing season, while others have predominance of early- or role in the development of our understanding of photosynthetic late-season rain (Noy-Meir, 1973, Fig. 1a). Temperature exhibits far adaptations to temperature (e.g., Lange et al., 1974; Mooney et al., less inter-annual variation than precipitation, but desert plants 1978; Nobel et al., 1978). Yet many comparative studies have often experience a wide range of temperatures within a growing season focused on adaptive differentiation between geographic regions or (Fig. 1b). Thus for a winter annual plant, early-season precipitation on long-lived perennials that must withstand extremes of tem- occurs when temperatures tend to be low, but late-season pre- perature and drought. Annual species constitute over half the flora cipitation occurs when atmospheric temperatures tend to be high. of the Sonoran Desert (Shreve and Wiggins, 1964), and winter Therefore, if species differ in temperature sensitivity, then they annuals, in particular, present an opportunity to examine the might differ in seasonal dynamics of carbon uptake during and photosynthetic temperature responses of species that begin after rain events. Additionally, storm events themselves change growth during times of relatively low temperature but face resource availability by temporarily reducing light and atmo- increasingly hot and dry conditions toward the end of their life spheric temperature and by stimulating nutrient mobilization (Cui cycle (Forseth and Ehleringer, 1982; Seemann et al., 1986; Werk and Caldwell, 1997; Woodhouse, 1997). In the Sonoran Desert, et al., 1983). As such, we used a pair of winter annuals to exam- periods following winter rainfall are significantly cooler than pre- ine how species’ differences in physiological traits might interact storm periods for an average of three-five days (Huxman et al., with temperature variation to translate into demographic variation 2008, Fig. 1c and d). These short periods of time following over time.

Fig. 1. Microclimatic data from the winter growing season of the Sonoran Desert that illustrate inter- and intra-annual covariation between precipitation, temperature, and photosynthetically active radiation. (a) Mean total monthly precipitation (cm) and (b) mean monthly temperatures (C) across 2002e2011 are shown within the shaded region indicating the longer-term average (1982e2007; solid line). (c) Relative changes in atmospheric temperature (D Temperature; C). Averaged across all precipitation events between 2002 and 2011, 24-h temperature was reduced by mean 7.0 0.67 C. Temperatures remained significantly lower than pre-event conditions for five days within the early growing season (OcteDec) and three days within the late growing season (JaneMar), highlighting seasonal variation in the influence of precipitation on other micrometeorological variables.

(d) Average maximum photosynthetically active radiation (PARmax) for the ﬁve days after all rain events (d ¼ 0) from within the early (NoveDec) and late (FebeMarch) from 2006 to 2012. PARmax decreased from pre-event levels an average of 27 3% in the early growing season and 39 4% in the late growing season on the days of precipitation events but recovered to pre-event levels within one day, regardless of growing season period. Vertical bars represent one standard error of the mean. G.A. Barron-Gafford et al. / Journal of Arid Environments 91 (2013) 95e103 97

Our previous research on physiological differences among (Pectocarya) would experience a more rapid increase in respiration Sonoran Desert winter annuals has demonstrated that species with temperature, and (iii) both species would shift the photo- exhibit a trade-off between relative growth rate (RGR) and inte- synthetic temperature optimum toward the growth temperature grated water-use efficiency (WUE, assayed by leaf carbon isotope (Table 1). discrimination, D)(Angert et al., 2007; Huxman et al., 2008; Table 1). Species with high RGR exhibit high growth and alloca- 2. Materials and methods tional plasticity in response to infrequent, large precipitation pulses (Angert et al., 2010) and have highly variable reproductive success 2.1. Study species and experimental treatments across years (Venable, 2007). Conversely, species with high WUE exhibit low RGR but have more buffered population dynamics over P. recurvata (Boraginaceae; hereafter, Pectocarya) and P. insularis time (Venable, 2007). We have also found that winter annuals with (Plantaginaceae; hereafter, Plantago) occur in the Sonoran and high WUE tend to have high nitrogen allocation to light-driven Mojave Deserts of the southwestern United States and northwest- dynamics of the Calvin cycle (Jmax) relative to carboxylation ern Mexico. The species commonly co-occur on low elevation fl (VCmax )(Huxman et al., 2008). Maximum electron transport rate desert bajadas and creosote bush ats, where they germinate with (Jmax) is often a major controller of net assimilation rate at low late autumn or winter rainfall, flower in early spring, and complete temperatures (Harley et al., 1992; Hikosaka et al., 2006), so we their reproductive life cycle before the onset of the arid fore- hypothesized that elevated Jmax:VCmax would enhance carbon summer in May. Seeds were collected in April 2005 from The Desert assimilation at low temperatures. Together, these traits could favor Laboratory at Tumamoc Hill, Arizona, (32130 N, 111010 W) and carbon assimilation during the reliably moist, but temporarily cool were after-ripened by over-summering them in mesh bags in and less light-saturating, periods following rainfall events. These outdoor shelters. In October, seeds were sown on 2% agar and traits could also boost carbon assimilation during cool, early- placed in a growth chamber at 22 C. Upon germination, seedlings morning hours or early in the growing season, when evaporative were transplanted into 164 mL ConeTainer pots (Stuewe & Sons, demand is lower. We also hypothesized that the high leaf nitrogen Inc. Corvallis, Oregon) filled with 20-grit sand that had observed in species with high Jmax:VCmax would incur a large res- been bleached and washed. Plants were grown in four controlled piratory load, particularly at warm temperatures, due to a higher environment chambers (Conviron E7/2, Controlled Environments leaf protein concentration and the associated higher maintenance Ltd, Winnipeg, Manitoba, Canada) with an irradiance of respiration rates (Amthor, 2000; Ryan, 1995, Table 1). A decrease in 500 mmol m 2 s 1 and received a daily maintenance irrigation of carbon assimilation efficiency would explain the low relative approximately 2 mL of a 1:20 Hoagland’s nutrient solution. growth rates observed in these species. Growing plants under these chamber irradiance conditions (the To test these hypotheses we studied two common, co-occurring maximum capacity of the environmental chambers) should not Sonoran Desert species (Pectocarya recurvata and Plantago insularis) have created anomalous results as 500 mmol m 2 s 1 is approach- that differ in position along the physiological and population dy- ing the light saturation point for these species, as determined from namic tradeoff mentioned above. We used gas exchange mea- a series of light response curves (unpublished data) and data surements to quantify photosynthetic and respiratory responses published for a congeneric annual (Niklas and Owens, 1989). Plants across a range of leaf temperatures for both cold- and warm- were randomly shuffled weekly among the four chambers during acclimated plants. We also used measures of chlorophyll fluo- this initial phase of establishment. Just prior to initiating temper- rescence to further investigate the primary photochemistry of each ature acclimation treatments, we applied a large 20 mL pulse of species at different temperatures to aid in our understanding of irrigation. Ten plants of each species were then randomly assigned how these plants dissipate excessive light energy when outside to a permanent treatment of either a cool (10/4 C, day/night) or their temperature optima. Given previously identified differences warm (20/5 C) acclimation temperature (Tacc), yielding five plants in traits, we predicted that (i) the species with the greater Jmax:VCmax per species per treatment. The cool treatment realistically simu- ratio (Pectocarya) would have a lower photosynthetic temperature lated natural rain events, during and after which nighttime tem- optimum, (ii) that the species with the greater leaf nitrogen content peratures remain approximately unchanged but daytime temperatures are lower by 5e7 C(Huxman et al., 2008). We simulated a 10 C temperature difference, representative of more Table 1 extreme recorded differences, to better detect physiological re- Summary of ecophysiological measures previously conducted on two Sonoran Desert winter annual plants with contrasting rates of resource use and allocation sponses and to provide insights for projected climate change sce- and corresponding predictions for photosynthetic performance across a range of narios for this region. To minimize unintended spatial and chamber atmospheric temperatures. These metrics illustrate the means by which leaf- effects, plants were randomly shuffled within and between the fi physiological traits may inform patterns of demography and species-speci c growth chambers assigned to the same temperature treatment. resource acquisition and utilization. Plants were provided with 2 mL maintenance irrigations daily. Ecophysiological Pectocarya Plantago Predictions for resource acquisition Background environmental data were acquired using a weather metric recurvata insularis and utilization station (HOBO, Onset Computer Corp., Bourne, MA, USA) deployed (PERE) (PLIN) at The Desert Laboratory to examine changes in field temperature J :V [YPERE should have higher rates max Cmax and light conditions in response to winter precipitation events. electron transport (therefore, better photosynthetic performance) Longer-term records come from a NCDC/NOAA weather station at at low temperatures than PLIN the University of Arizona in Tucson, Arizona, USA (5.4 km from Leaf [N] [YPERE should experience greater study site), as described by Huxman et al. (2008). respiratory CO2 loss at higher temperatures than PLIN Water use [YPERE should be less constrained to 2.2. Leaf-level gas exchange efficiency large, saturating precipitation events Y[ Relative growth Links between RGR and acclimation Net photosynthesis rate versus internal [CO2](AeCi) response rate (RGR) potential suggest that PLIN may be curves and measures of net photosynthetic and respiratory re- more able to acclimate to increased sponses of attached leaves to temperature were determined with temperature variability than PERE a portable open-flow gas exchange system (LI-6400, LI-COR 98 G.A. Barron-Gafford et al. / Journal of Arid Environments 91 (2013) 95e103

Biosciences, Lincoln, NE, USA). Due to the small size of the study interactions on Anet or Rd, using the Akaike Information Criterion to species, we used the leaf chamber (model 6400-15) that provided select an autoregressive order 1 covariance structure (Littell et al., the smallest chamber gasket circumference and un-occupied 1996). We evaluated the significance of fixed effects with Type I chamber space per unit leaf area, making it the most appropriate sums of squares, which generate sequentially formulated hypoth- chamber for this project. The red/blue LED light source (model eses that are appropriate for polynomial models (Littell et al., 1996), 6400-02B) light source was secured over the clear-top leaf cuvette, with denominator degrees of freedom obtained by Satterthwaite’s and a quantum sensor (LI-185) was used to verify light levels approximation (Satterthwaite, 1946). These analyses were per- transmitted through the transparent film of the cuvette (data not formed with SAS Proc Mixed (SAS, version 9.1, SAS Institute Inc., shown). Once the leaf was placed into the chamber, we used Pol- Cary, NC, USA). ‘Estimate’ statements computed differences in ytetrafluoroethylene grease provided by the chamber’s manu- least-squares means for Anet or Rd between species within each Tacc facturer (210-05774) to seal around the gas junctions. On each leaf and between warm- and cold-acclimated plants of each species at measured, we then directed high-concentration CO2 gas through five Tleaf (8, 15, 22, 29, and 36 C). We also analyzed two key pa- Bev-A-Line tubing (Thermoplastic Processes, Georgetown, DE, USA) rameters of the photosynthetic temperature response curve, the around this now-sealed gasket junction to ensure that no leak was optimal temperature of photosynthesis (Topt) and the maximum detectable by the instrument’sCO2 gas analyzer. AeCi response photosynthetic rate (Amax). For each individual, we fit a quadratic curves were conducted using three individuals of each species at equation to the curve of Anet versus Tleaf and solved for Topt where a common temperature typical of an average growing season the derivative of this equation equaled zero. Solving the quadratic (23 C). equation at Topt yielded Amax for each individual. We then used Photosynthetic and respiratory temperature response curves at analysis of variance (ANOVA) to examine the effects of species, Tacc, ambient concentrations of CO2 were conducted on plants that were and their interaction on Topt or Amax. transferred from the growth chamber to a large incubator, which was used to control external air temperature (Percival Scientific, 2.3. Chlorophyll fluorescence model I-36LLVL, Perry, IA, USA) to match air temperatures within the cuvette. As such, the entire plant experienced each step of the To further decompose the photosynthetic response of each spe- leaf-chamber temperature response curve rather than individual cies to temperature, we measured patterns of chlorophyll fluo- leaves. This minimized any temperature-induced pressure differ- rescence in response to a specific series of dark, moderate, and super- ences that might cause a leak into/from the measurement chamber saturating light (Kitajima and Butler, 1975; Maxwell and Johnson, and extended the temperature range for our measurements beyond 2000). As detailed below, chlorophyll fluorescence parameters pro- the capacity of the LI-6400’s Peltier coolers. Leaves were clamped vide insight into several aspects of a leaf’s capacity for function, e.g. within the cuvette, where they were incubated under saturating light harvesting and electron transport, and the means by which the 2 1 light (1200 mmol photons m s ), ambient CO2 concentration, leaf is dissipating excessive light energy when it cannot be used for a flow rate of 200 mmol s 1, and a block temperature of 8 C. Leaf photosynthesis. Chlorophyll fluorescence was measured using temperature (Tleaf) was calculated based on standard energy bal- a pulse modulated chlorophyll fluorometer (FMS2, Hansatech In- ance equations as described in Huxman et al. (2008). After 30 min, struments Ltd, Norfolk, UK) at cool (15 C) and warm (29 C) meas- 2 1 steady-state photosynthesis (Anet, mmol CO2 m s ), stomatal urement temperatures (Tmeas). These temperatures were chosen 2 1 conductance to water vapor (mol H2Om s ) and other asso- because they are lower than and higher than typical Topt for photo- ciated parameters were recorded. synthesis, respectively. Plants were irrigated and then maintained at The light source was then turned off and leaf respiration rate 15 C under lighted conditions (intensity w 500 mmol m 2 s 1) for after five minutes in complete darkness (Rd) was determined. one hour. After 30 min of dark adaptation, initial fluorescence (Fo) Longer dark incubation is generally recommended (Atkin et al., was measured in response to weak red irradiation (650 nm), and 1997; Laisk, 1977), however, prior to conducting these measure- then maximum fluorescence (Fm) was measured in response to ments, we used the Kok method (Kok, 1948; Sharp et al., 1984)to a saturating light pulse (intensity w 15,300 mmol m 2 s 1). Variable determine how Rd estimates differed between shorter and longer fluorescence (Fv) was calculated as Fm Fo. Light sufficient to drive dark incubation periods. The Kok method estimates Rd from the photosynthesis (actinic light) was then applied for two minutes, and 0 0 intercept of a light response curve, determined by measuring the fluorescence level just prior to (F t) and during (F m) a second photosynthetic rates after long periods of incubation across saturating pulse was measured. After this pulse, actinic light was 0 sequentially decreasing, low light intensities. For these two species, switched off and fluorescence in response to far-red light (F o)was measurements after five minutes of darkness were stable (i.e., not measured (Maxwell and Johnson, 2000). Accompanying measure- decreasing) and only minimally inflated (11%) compared to esti- ments of light intensity and leaf temperature were made with the mates after 30e60 min using the Kok method. Further, the esti- microquantum sensor/measurement arm of the FMS2. The entire mates were similarly inflated for both species. Hence, we focus on acclimation and measurement process was then repeated at 29 C. the comparison of relative differences in Rd among species and Chlorophyll fluorescence measurements were conducted on five temperatures, with the caveat that all estimates are likely to be plants per species per Tacc. slightly inflated in an absolute sense by short-term dark incubation. From this series of measurements, we calculated the maximum This process was repeated in 7 C increments from 8 Cupto36 C. quantum yield of photosystem II (Fv/Fm), which is a measure of the We minimized potentially confounding variation in vapor pressure proportion of all photons absorbed by chlorophyll that are used in deficit between temperatures by varying the flow of air through photochemistry. The quantum yield of photochemistry in open silica gel desiccant with a constant setpoint of approximately photosystem II (PS II) reaction centers ready for electron capture 0 0 0 0 1.5 kPa. Gas exchange measurements at each of the five block was also determined as F v/F m, where F v ¼ F m Ft (Genty et al., temperature settings were conducted on four to six plants per 1989; Kitajima and Butler, 1975). We also calculated measures of 0 0 0 species per Tacc treatment. The temperature sensitivity (Q10)ofRd photochemical quenching (qP) as qP ¼ [(F m Ft)/(F m F o)] was calculated as Q10 ¼ the Rd rate at T þ 10 C/Rd rate at T, where T (Maxwell and Johnson, 2000; Schreiber et al., 1995). qP was used to was set to acclimation temperature for each treatment. gain insight into the proportion of PSII reaction centers that were We used repeated measures mixed models to examine the ef- open. Non-photochemical quenching (NPQ) is induced under con- fects of Tleaf (linear and quadratic terms), species, Tacc, and their ditions when the photosynthetic apparatus cannot use all absorbed G.A. Barron-Gafford et al. / Journal of Arid Environments 91 (2013) 95e103 99 light energy for photochemistry, which can occur at quite low light (Fig. 2c,d). When cold-acclimated, Pectocarya displayed greater Anet intensity even under optimum conditions for photosynthesis. than Plantago at low temperatures (Fig. 2a,c). Conversely, when Stressful conditions, such as high light intensity, low internal CO2 warm acclimated, Plantago displayed equivalent Anet to Pectocarya concentration due to drought, or low temperature, markedly pro- at low temperatures but significantly greater Anet across higher mote NPQ. Therefore, the amount of NPQ is an indicator of stress temperatures (Fig. 2b,d). severity and measures changes in heat dissipation relative to the Pectocarya optimal temperature of photosynthesis (Topt)aver- 0 0 dark-adapted state. NPQ was calculated as NPQ ¼ (Fm F m)/F m. aged 17.9 1.4 C when cold acclimated and 16.1 1.0 C when warm For each species separately, we analyzed each chlorophyll flu- acclimated, underscoring the lack of significant photosynthetic 0 0 orescence variable (dark-adapted Fv/Fm, light-adapted F v/F m, qP, acclimation in this species. For Plantago, Topt averaged 21.6 1.7 C and NPQ) with repeated measures ANOVA with fixed effects of Tacc, when cold acclimated but increased to 24.6 1.0 C when warm Tmeas, and their interaction using SAS Proc Mixed (SAS, version 9.1, acclimated. Thus, Topt of Pectocarya was significantly lower than that SAS Institute Inc., Cary, NC, USA). We evaluated the significance of of Plantago (F1, 14 ¼ 15.21, P ¼ 0.0016), regardless of acclimation fixed effects with Type III estimable functions. When ANOVA conditions. Although Anet data clearly suggest acclimation of Plan- indicated a significant main effect or interaction, we used Tukeye tago to warm temperatures, Topt was not significantly affected by Tacc Kramer adjusted comparisons of least square means to assess dif- (F1, 14 ¼ 0.15, P ¼ 0.76) or by the interaction between species and Tacc ferences among levels of the effect. The PDMIX800 macro was used (F1, 14 ¼ 2.45, P ¼ 0.14). Pectocarya maximum photosynthetic rate at 2 1 to convert pairwise differences between least square means to Topt (Amax) averaged 14.4 1.4 mmol CO2 m s when cold accli- 2 1 letter groupings, where means sharing the same letter code are not mated and 12.7 1.8 mmol CO2 m s when warm acclimated 2 1 significantly different (Saxton, 1998). (Fig. 2a,b). Plantago Amax averaged only 9.6 1.3 mmol CO2 m s 2 1 when cold acclimated, but increased to 16.4 1.6 mmol CO2 m s when warm acclimated (Fig. 2c,d). Species differences in the 3. Results response of Amax to acclimation temperature are confirmed by a significant species Tacc interaction (F1, 14 ¼ 6.61, P ¼ 0.02). 3.1. Leaf level gas exchange: photosynthesis 3.2. Leaf level gas exchange: respiration Analysis of steady-state net photosynthesis (Anet) versus [CO2] response curves showed that P. recurvata and P. insularis grown in Pectocarya and Plantago differed in the response of dark respi- the growth chamber had a similar allocation to maximum electron ration (Rd) to increases in Tleaf, but neither species displayed an transport rates (Jmax) relative to carboxylation capacity (VC )as max apparent respiratory acclimation to Tacc (Table 2B). The species naturally-occurring, field-grown plants used in previous experienced similar rates of Rd at low temperatures, but Pectocarya studies (Huxman et al., 2008). Relative to one another, the species 2 1 experienced greater Rd under warmer temperatures (Table 3). had similar rates of VC (68.22 16.28 mmol m s and max Furthermore, Pectocarya Rd rates were twice as sensitive to 62.44 13.21 mmol m 2 s 1 in Pectocarya and Plantago, respec- increasing Tleaf (Q10 ¼ 2.00 0.31) than Plantago (0.98 0.11), tively, P ¼ 0.6992), but Pectocarya had a significantly greater Jmax when cold acclimated, and 46% more sensitive (Q10 ¼ 2.76 0.40 than Plantago (414.40 48.04 mmol m 2 s 1 versus for Pectocarya versus 1.89 0.36 for Plantago) when warm accli- 178.63 45.55 mmol m 2 s 1, respectively, P ¼ 0.0403). Pectocarya mated. The ratio of Rd:Anet provides a unitless measure of the in- and Plantago differed in the response of A to leaf measurement net fluence of increasing temperature on carbon balance within the temperature (T ), acclimation temperature (T ), and the leaf acc plant because it normalizes rates of carbon loss (Table 3) relative to interaction between T and T (Table 2A, Fig. 2). Although A leaf acc net each plant’s carbon gain at that measurement temperature (Fig. 2). showed a significant quadratic response to Tleaf, the degree of The Rd:Anet for Pectocarya was similar across lower temperatures, curvature was not affected by species or T (Table 2A). Cold- and acc but beyond 24 C, every 1 C increase in temperature increased the warm-acclimated Pectocarya plants had A values for a given leaf net ratio of carbon loss to gain 8.8 1.1% in cold acclimated plants and measurement temperature, indicating no photosynthetic acclima- 26.9 6.3% in warm acclimated plants (Fig. 3a). The Rd:Anet ratio tion to T (Fig. 2a,b). However, warm-acclimated Plantago showed acc remained unchanged across measurement temperatures in warm- greater A than cold-acclimated plants at most leaf temperatures net acclimated Plantago, and only declined for cold-acclimated Plantago when exposed to leaf temperatures approaching 36 C(Fig. 3b). Table 2

Repeated measures analysis of (A) photosynthesis (Anet) and (B) respiration (Rd) response to Tleaf (linear and quadratic terms), species, Tacc, and all interactions. 3.3. Chlorophyll fluorescence: dark- and light-adapted yield Significance of fixed effects evaluated with Type I sums of squares (Littell et al., ’ 1996), with denominator degrees of freedom obtained by Satterthwaite s approx- To more thoroughly examine physiological responses of these imation (Satterthwaite, 1946). species to temperature stress, we examined several chlorophyll Source A. Anet B. Rd fluorescence parameters that provide insights into how efficiently

Between-subjects dfN dfD FP dfN dfD FP plants are harvesting light, transferring that light energy through Species 1 14 0.61 0.4476 1 14 19.37 0.0006 photochemistry when they are able to do so, and dissipating

Tacc 1 14 1.85 0.1954 1 14 0.14 0.7139 excessive light energy when they are too stressed to maximize Species Tacc 1 14 8.73 0.0105 1 14 0.98 0.3384 photosynthesis. Measures of the maximum quantum yield of Within-subjects dfN dfD FP dfN dfD FP photosystem II (Fv/Fm) illustrate the proportion of all photons

Tleaf 1 65 49.19 <0.0001 1 75 126.16 <0.0001 absorbed by chlorophyll that are used in photochemistry. Cold- Tleaf species 1 65 53.72 <0.0001 1 76 37.74 <0.0001 acclimated Plantago and Pectocarya had significantly higher levels Tleaf Tacc 1 65 0.7 0.4058 1 76 0 0.9603 of dark-adapted Fv/Fm when measured at low temperatures than Tleaf species Tacc 1 64 6.75 0.0116 1 76 1.96 0.1658 2 when measured at high temperatures (Tables 4 and 5). There was Tleaf 1 64 69.16 <0.0001 1 63 32.4 <0.0001 2 fi Tleaf species 1 64 2.84 0.0966 1 63 4.56 0.0366 no signi cant difference, however, in Fv/Fm of warm-acclimated 2 Tleaf Tacc 1 64 2.21 0.1418 1 63 0.05 0.8228 plants measured at high versus low temperatures (Table 4). Both T2 species T 1 64 0.31 0.5818 1 63 0.78 0.3811 leaf acc species had greater Fv/Fm at cold Tmeas, and neither species dis- Significant effects are indicated in bold. played acclimation to Tacc in terms of changes in Fv/Fm (Table 5A). 100 G.A. Barron-Gafford et al. / Journal of Arid Environments 91 (2013) 95e103

Fig. 2. Gas exchange response to leaf temperature (Tleaf; C) for cold-acclimated (solid symbols) and warm-acclimated (open symbols) plants. Net photosynthesis (Anet; 2 1 mmol CO2 m s ) data are shown for Pectocarya recurvata (a,b; upper panels) and Plantago insularis (c,d; lower panels). Dashed lines indicate the 95% conﬁdence interval of the ﬁtted temperature response of Anet across the range of measurement temperatures.

Both species experienced significantly greater light-adapted PSII suggesting a greater ability to adjust physiological processes asso- 0 0 yield (F v/F m) when measured at cold temperatures, but unlike Fv/ ciated with photosynthesis to deal with this change in temperature Fm, this was true regardless of original Tacc (Tables 4 and 5B). (Table 5C). Neither species displayed a significant interaction be- Additionally, Plantago displayed photosynthetic acclimation as tween Tmeas and Tacc. Rates of induction of photochemical 0 0 measured by increases in F v/F m in warm temperatures quenching (proportion of open PSII reaction centers, qP) were sig- (P ¼ 0.0203), but Pectocarya did not (P ¼ 0.1969, Table 5B). Thus, nificantly greater at the higher Tmeas regardless of species or Tacc 0 0 measures of Plantago F v/F m were significantly greater at high (Tables 3 and 5D). While both species were significantly affected by measurement temperatures relative to low temperatures, illus- Tacc, qPofPlantago showed a smaller magnitude of change between trating a greater amount of open photosystem II reaction centers warm and cold Tmeas when cold-acclimated, suggesting a greater ready for electron capture under warmer conditions. ability to maintain function across a range of temperatures. Neither species was significantly affected by the Tmeas Tacc interaction 3.4. Chlorophyll fluorescence: non-photochemical and (Table 5D). photochemical quenching 4. Discussion Rates of induction of non-photochemical quenching (heat dissipation relative to the plant’s dark-adapted state; NPQ) were sig- Our study identifies key trade-offs between physiological nificantly greater in both species at warm Tmeas, regardless of Tacc, function and resource acquisition/utilization within two co- indicative of reduced photosynthetic performance as temperature occurring winter annuals that, ultimately, relate to patterns of increases (Tables 4 and 5C). Plantago, however, displayed a signifi- performance under varying environmental conditions. Previous cant acclimation in terms of NPQ, while Pectocarya did not, work had shown that Pectocarya had higher integrated WUE,

Table 3 Means and standard errors (in parentheses) for leaf-level dark respiration (Rd). Plants were growth under low (10 C) and high (20 C) acclimation temperatures (Tacc) and then measured across a range of ﬁve temperatures (Tmeas; C).

Tacc: Low High

Tmeas: 8 15 22 29 36 8 15 22 29 36

Rd Pectocarya 1.85 (0.81) 2.74 (1.02) 4.81 (1.45) 10.76 (2.36) 14.34 (2.56) 2.85 (1.06) 2.6 (0.91) 5.91 (1.12) 11.35 (2.23) 15.81 (2.68) Plantago 2.1 (0.83) 0.85 (0.33) 2.05 (0.6) 3.8 (0.72) 6.8 (1.26) 1.04 (0.58) 0.88 (0.48) 1.95 (0.71) 2.35 (0.65) 4.87 (1.06) G.A. Barron-Gafford et al. / Journal of Arid Environments 91 (2013) 95e103 101

Fig. 3. Ratios of leaf respiration to net photosynthesis rates (Rd:Anet) across leaf temperatures (Tleaf; C) for cold-acclimated (solid symbols) and warm-acclimated (open symbols) plants. Mean data (n ¼ 5) are shown for Pectocarya recurvata (a) and Plantago insularis (b), and horizontal and vertical bars represent standard errors of the mean leaf temperature and Rd:Anet, respectively.

higher leaf N, and high maximum electron transport rates (Jmax) reduced RuBP regeneration and limited net CO2 uptake as tem- ’ relative to carboxylation capacity (VCmax ) compared to Plantago, perature increases. Pectocarya s elevated Jmax may explain the which has lower values for these physiological traits (Huxman patterns of reduced photosynthetic rates beyond 25 C. Badger et al. et al., 2008, Table 1). Based on these findings, we proposed that (1982) showed that some plants grown under a low Tacc can have the physiology of desert annual species with traits like that of higher activity of some photosynthetic enzymes at lower temper- Pectocarya may be optimized for carbon gain during predictably atures but then experience reduced heat stability at higher meas- moist, but cooler, growing conditions, while species with the urement temperatures relative to plants grown at a high Tacc, opposite traits, like Plantago, experience optimal performance similar to what we see with Pectocarya. Such a trade-off is impor- across a broader suite of temperatures, including warmer growth tant in understanding the temporal niches of these desert annual conditions. Given patterns of cooler temperatures in the Sonoran species relative to the known weather variation existing in the Desert immediately following rain events, early in the day, and Sonoran Desert. earlier in the winter growing season (Fig. 1c, d), these tradeoffs are Pectocarya experienced greater respiratory carbon loss than likely to decouple resource utilization and carbon gain dynamics Plantago at moderate to high temperatures, regardless of Tacc among co-occurring species across multiple temporal scales (e.g., (Table 3). Increasing rates of respiration with temperature have daily, surrounding storm events, and seasonally). been shown repeatedly in the literature (Atkin et al., 2006; Griffin et al., 2002; Teskey and Will, 1999). Rates of Pectocarya Rd at 4.1. Carbon balance across temperatures 15 C were approximately equal to those of Plantago at 30 C, suggesting that high Rd rates of Pectocarya may be advantageous for Under colder acclimation conditions, Pectocarya out performed maintaining favorable carbon metabolism at lower temperatures. Plantago under low-to-moderate temperatures in terms of net These high Rd rates could be a byproduct of Pectocarya leaves photosynthetic rates (Anet). This greater function under cold con- containing greater levels of nitrogen-rich proteins, which increase ditions is likely tied to Pectocarya investment in greater Jmax:VCmax , Anet at lower temperatures yet decrease net assimilation under allowing for greater electron transport under low-temperature warmer conditions. High leaf nitrogen content is often associated conditions than possible within Plantago (Fig. 2). However, these with high protein concentration (Lexander et al., 1970), which leads same physiological traits have a cost in terms of function under to higher maintenance respiration rates (Amthor, 2000; Wright warmer temperatures. Many species experience a deactivation of et al., 2001) and lower conversion efficiency of photosynthetic Jmax at elevated temperatures (Hikosaka et al., 2006), which leads to assimilation to biomass. Atkin et al. (2006) note that because the temperature sensitivity of light-saturated photosynthesis, light- Table 4 respiration, and dark-respiration are so different, short-term per- Means and standard errors (in parentheses) for the chlorophyll fluorescence pa- turbations in air temperature alter the balance between photo- rameters dark-adapted yield (F /F ), light-adapted yield (F0 /F0 ), non- v m v m synthesis (Anet) and respiration in individual leaves (Rd) and photochemical quenching (NPQ), and photochemical quenching (qP). Plants were dramatically affect the carbon balance of leaves. As such, we growth under low (10 C) and high (20 C) acclimation temperatures (Tacc) and then directly analyzed the ratio of R :A and found that carbon balance measured under low (15 C) and high (29 C) measurement temperatures (Tmeas). d net within Pectocarya tended toward much greater carbon loss under Tacc: Low High higher temperatures (Fig. 3). Together, these results highlight Tmeas: Low High Low High a trade-off between maximizing photosynthesis at low tempera-

Fv/Fm Pectocarya 0.82 (0.00) 0.80 (0.01) 0.81 (0.00) 0.81 (0.00) tures when evaporative demand is low, and minimizing respiration Plantago 0.84 (0.00) 0.82 (0.01) 0.83 (0.00) 0.83 (0.00) 0 0 when temperatures climb. F v/F m Pectocarya 0.64 (0.01) 0.50 (0.02) 0.64 (0.01) 0.54 (0.02) Plantago 0.65 (0.01) 0.47 (0.01) 0.65 (0.01) 0.52 (0.01) NPQ Pectocarya 1.51 (0.13) 2.11 (0.20) 1.25 (0.08) 1.90 (0.22) 4.2. Patterns of optimality, plasticity and acclimation Plantago 1.56 (0.08) 2.80 (0.09) 1.44 (0.05) 2.53 (0.14) qP Pectocarya 0.15 (0.01) 0.37 (0.02) 0.14 (0.01) 0.31 (0.02) Our results suggest that different suites of leaf physiological Plantago 0.18 (0.01) 0.31 (0.02) 0.15 (0.01) 0.28 (0.02) characteristics should yield very different temporal niches for 102 G.A. Barron-Gafford et al. / Journal of Arid Environments 91 (2013) 95e103

Table 5 0 0 Repeated measures analysis of (A) dark-adapted PSII yield (Fv/Fm), (B) light-adapted PSII yield (F v/F m), (C) non-photochemical quenching (NPQ), and (D) photochemical quenching (qP) by species in response to Tmeas, Tacc, and the Tmeas Tacc interaction. Signiﬁcance of ﬁxed effects evaluated with Type III sums of squares.

0 0 Species Source A. Fv/Fm B. F v/F m C. NPQ D. qP

Pectocarya Between-subjects dfN dfD FP F P F P F P recurvata Tacc 1 10 0.21 0.6536 1.91 0.1969 1.74 0.2168 5.48 0.0413 Within-subject dfN dfD FP F P F P F P Tmeas 1 10 15.58 0.0027 162.38 <0.0001 27.39 0.0004 155.11 <0.0001 Tmeas Tacc 1 10 10.9 0.008 4.28 0.0653 0.05 0.8217 0.42 0.5307 Plantago Between-subjects dfN dfD FP F P F P F P insularis Tacc 1 10 0.43 0.529 7.59 0.0203 5.35 0.0434 7.07 0.0239 Within-subject dfN dfD FP F P F P F P Tmeas 1 10 6.06 0.0335 215.69 <0.0001 334.87 <0.0001 102.54 <0.0001 Tmeas Tacc 1 10 10.19 0.0096 5.07 0.0481 2.47 0.147 0.81 0.3896 Significant effects are indicated in bold. optimal performance between these co-occurring species. We measurement temperatures for Plantago indicated both a greater found a lower temperature optimum (Topt) for Pectocarya than for amount of open photosystem II reaction centers ready for electron Plantago, regardless of acclimation temperature (Tacc; Fig. 2), capture under warmer conditions and a greater capacity for pho- matching our hypothesis. Based on measures of both Rd and the tosynthetic acclimation. Combined with the data indicating lower ratio of Rd:Anet, better performance under cool conditions is likely respiratory loss in Plantago at high temperatures (Fig. 2c,d), the tied to elevated carbon loss at higher temperatures. We found fluorescence data help explain the greater photosynthetic perfor- a relative lack of acclimation of Pectocarya to the treatment differ- mance of Plantago than Pectocarya across higher temperatures. We ences, in either Topt or maximum photosynthetic rates (Amax), also calculated the rates at which the two species induced which corresponded well with the limited allocational plasticity we quenching mechanisms to deal with excess excited energy (Müller also have found in this species (Angert et al., 2010). In contrast, et al., 2001; Niyogi, 2000). Rates of induction of non-photochemical Plantago demonstrated photosynthetic acclimation to temperature, quenching via heat dissipation (NPQ) were significantly greater in as evidenced by the significantly greater Anet at high temperatures both species at warm Tmeas, but Plantago NPQ illustrated a signifi- for warm-acclimated plants compared to cold-acclimated plants. cant change in response to acclimation temperature, whereas Plantago also showed some evidence of acclimation to cold, in that Pectocarya did not. These patterns suggest that Plantago may have Anet of cold-acclimated plants at low temperatures was a greater been regulating excessive electrons more actively via non- percentage of Amax than for warm-acclimated plants measured at photochemical, heat dissipating pathways, whereas Pectocarya low temperatures. However, the Amax of cold-acclimated Plantago was preferentially using photochemical pathways to dissipate was significantly depressed relative to Amax of warm-acclimated excitation energy. The low rates of net assimilation of Pectocarya plants, indicating that acclimation to lower temperatures incur- indicate that photochemical quenching of electrons may have been red a cost for Plantago. The overall depression of Plantago photo- assimilatory, but rates of respiration might have been too high at synthetic rates when cold-acclimated may be indicative of higher temperatures to yield a strong response of net carbon gain a feedback inhibition, in that sink-strength could be reduced due to (Berry and Björkman, 1980; Seemann et al., 1986; Yamasaki et al., limited respiration. A review by Atkin and Tjoelker (2003) sug- 2002). gested that limitations in maximum catalytic activity of respiratory enzymes are likely the most limiting factor in restricting respiration 5. Conclusions at low temperatures. The lack of photosynthetic acclimation manifested by changes in Overall, Pectocarya had a lower temperature optimum, whereas Topt (both species) or Amax (Pectocarya) observed here could be Plantago displayed greater photosynthetic performance at moder- a true inability to shift, but it is also possible that we measured ate and high temperatures and a capacity to adjust its physiological leaves produced before the change in temperature regime. Previous functions to alterations in growth temperature. These differences in studies, however, have shown acclimation to new temperatures in both optimization and acclimation of photosynthesis may con- preexisting leaves formed under previous growth temperatures tribute to these species having different diel and seasonal peaks for (Loveys et al., 2002; Pisek et al., 1973). In the desert environment, carbon assimilation and for maximizing photosynthetic function changes in soil moisture availability and temperature occur quickly across different time periods following rainfall events. Based solely and unpredictably. These species must respond to variation in on the physiological differences demonstrated here, we would temperature and water availability on a much faster time scale than predict that Pectocarya should display greater performance in years would allow for the development of new canopy material. Only dominated by early rains, small rain events, and cooler tempera- following relatively rare periods of very high rainfall would soil tures, whereas Plantago should display greater performance in water availability persist for a sufficient period to deploy new years characterized by large, saturating rainfall events, late-season leaves (Angert et al., 2007, 2010). Therefore, it is likely that the lack rainfall, or sequential rainfall events in which adequate soil mois- of acclimation observed in this study is relevant to the behavior of ture is present over a greater range of temperatures. Recent analysis these species in their natural environment under most conditions. of inter-annual variation in demographic performance revealed that species with high WUE, such as Pectocarya, did indeed have 4.3. Chlorophyll fluorescence highlights biochemical differences in greater relative fitness in years with small rain events and longer plant function across temperatures durations between rain events than species with higher RGR, such as Plantago (Kimball et al., 2011). Somewhat paradoxially, high- We used measures of chlorophyll fluorescence to further WUE species also tended to have greater relative fitness in years investigate the physiology of the two species and their differences that were warmer, particularly toward the end of the growing in responses to acclimation and measurement temperatures. Sig- season (Kimball et al., 2011). High temperatures in the spring are 0 0 nificantly greater light adapted yield (F v/F m) at high relative to low likely to truncate the growing season. Thus, a species with a cooler G.A. Barron-Gafford et al. / Journal of Arid Environments 91 (2013) 95e103 103 photosynthetic optimum may be more successful in a warm year by Kimball, S., Gremer, J.R., Angert, A.L., Huxman, T.E., Venable, D.L., 2011. Fitness and e virtue of being able to complete their growth and reproduction physiology in a variable environment. Oecologia 169, 319 329. Kitajima, M., Butler, M.L., 1975. 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