Journal of Arid Environments 91 (2013) 95e103
Contents lists available at SciVerse ScienceDirect
Journal of Arid Environments
journal homepage: www.elsevier.com/locate/jaridenv
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
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
b
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 20 June 2012
Received in revised form
14 December 2012
Accepted 15 December 2012
Available online 26 January 2013
A mechanistic understanding of population dynamics requires close examination of species’ differences
in how physiological traits interact with environmental variation and translate into demographic variation. We focused on two co-occurring winter annual species (Pectocarya recurvata and Plantago insularis) that differ in photosynthetic resource-use efficiency and demographic responses to environmental
variation and covariation between temperature and water availability. Previous work showed that Pectocarya has higher water-use efficiency and nitrogen allocation to light-driven dynamics of the Calvin
cycle (Jmax:VCmax ) than Plantago, which is often associated with enhanced electron transport capacity at
low temperatures and better light harvesting capacity. These traits could enhance Pectocarya photosynthesis during reliably moist but cool, cloudy periods following precipitation. We acclimated plants to
low and high temperatures and then measured gas exchange across a 30 C temperature range. As
predicted, optimal temperatures of photosynthesis were lower for Pectocarya than Plantago. Additionally,
Pectocarya experienced greater respiratory carbon loss than Plantago at higher temperatures (every 1 C
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.
Keywords:
Chlorophyll fluorescence
Photosynthetic temperature response
Resource partitioning
Respiration
Species coexistence
Variable environments
1. Introduction
Abbreviations: Anet, steady-state photosynthesis (mmol CO2 m2 s1); Amax,
maximum photosynthetic rate (mmol CO2 m2 s1); Fo, initial fluorescence
when dark-adapted; F0 o, initial fluorescence when light-adapted; Fm, maximum
fluorescence when dark-adapted; F0 m, maximum fluorescence when light-adapted;
Fs, steady state light-adapted fluorescence signal; Fv, variable fluorescence level
when dark-adapted ¼ (Fm Fo); F0 v, variable fluorescence level when lightadapted ¼ (F0 m F0 o); Fv/Fm, maximum quantum yield of photosystem II; F0 v/F0 m,
light-adapted PSII yield; Jmax, maximum electron transport rates; NPQ, non-photochemical quenching ¼ [(Fm F0 m)/F0 m]; qP, photochemical quenching ¼ [(F0 m Fs)/
(F0 m F0 o)]; Rd, respiration after 5 min in complete darkness (mmol CO2 m2 s1); Tacc,
acclimation temperatures ( C); Tleaf, leaf temperature ( C); Tmeas, measurement
temperatures ( C); Topt, optimal temperature of photosynthesis ( C); VCmax , carboxylation capacity; WUE, water-use efficiency; D, leaf carbon isotope discrimination
(ppm).
* Corresponding author. B2 Earthscience, Biosphere 2, University of Arizona,
Tucson, AZ 85721, USA. Tel.: þ1 520 548 0388; fax: þ1 520 621 9190.
E-mail address: [email protected] (G.A. Barron-Gafford).
1
These authors contributed equally to this work.
0140-1963/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.jaridenv.2012.12.006
Examining interspecific differences in physiological traits can
illuminate the link between environmental variation and demographic variation and thereby contribute to a mechanistic understanding of population and community dynamics (McGill et al.,
2006). In dryland ecosystems, precipitation exerts a dominant influence on most biological processes, from short-term responses
such as plant photosynthetic activity to longer-term demographic
responses such as growth, survival and recruitment (BarronGafford et al., 2012; Huxman et al., 2004; Schwinning and Sala,
2004). Functional trait differences that underlie plant response to
precipitation may explain within-year and between-year resource
partitioning among coexisting species (Chesson et al., 2004;
Novoplansky and Goldberg, 2001). For example, species differences
in physiology or phenology may cause species-specific patterns of
resource-use in response to the same precipitation event, or they
96
G.A. Barron-Gafford et al. / Journal of Arid Environments 91 (2013) 95e103
may enable species to take advantage of precipitation sequences of
differing magnitudes and timing. Most examinations of biological
responses to precipitation have focused on the direct effects of
increased soil moisture, but a more complete understanding will
require investigation of the sensitivity of resource gain to covarying environmental factors such as light availability and
temperature.
Precipitation in deserts typically falls in discrete events that
may be clustered in space and time, and patterns of event clustering determine the amount of resources and the duration of their
availability (Huxman et al., 2004; Noy-Meir, 1973; Reynolds et al.,
2004). Monthly precipitation is highly variable between years,
with some years experiencing consistent precipitation across
a growing season, while others have predominance of early- or
late-season rain (Noy-Meir, 1973, Fig. 1a). Temperature exhibits far
less inter-annual variation than precipitation, but desert plants
experience a wide range of temperatures within a growing season
(Fig. 1b). Thus for a winter annual plant, early-season precipitation
occurs when temperatures tend to be low, but late-season precipitation occurs when atmospheric temperatures tend to be high.
Therefore, if species differ in temperature sensitivity, then they
might differ in seasonal dynamics of carbon uptake during and
after rain events. Additionally, storm events themselves change
resource availability by temporarily reducing light and atmospheric temperature and by stimulating nutrient mobilization (Cui
and Caldwell, 1997; Woodhouse, 1997). In the Sonoran Desert,
periods following winter rainfall are significantly cooler than prestorm periods for an average of three-five days (Huxman et al.,
2008, Fig. 1c and d). These short periods of time following
precipitation events may contribute disproportionately to plant
seasonal carbon gain (Huxman et al., 2004), yet they may coincide
with low-temperature and low-light limitations for some species.
Therefore, enhancing photosynthesis under these conditions could
allow species to better exploit this resource-rich window of
opportunity.
Photosynthetic carbon assimilation is strongly affected by
temperature, but many species exhibit a remarkable ability to
adjust photosynthetic processes to altered growth temperatures
(Berry and Björkman, 1980). Temperature acclimation of photosynthesis and respiration can allow plants to maintain relatively
constant rates of net CO2 exchange as daily temperatures change
across the growing season. Desert plants have played an important
role in the development of our understanding of photosynthetic
adaptations to temperature (e.g., Lange et al., 1974; Mooney et al.,
1978; Nobel et al., 1978). Yet many comparative studies have often
focused on adaptive differentiation between geographic regions or
on long-lived perennials that must withstand extremes of temperature and drought. Annual species constitute over half the flora
of the Sonoran Desert (Shreve and Wiggins, 1964), and winter
annuals, in particular, present an opportunity to examine the
photosynthetic temperature responses of species that begin
growth during times of relatively low temperature but face
increasingly hot and dry conditions toward the end of their life
cycle (Forseth and Ehleringer, 1982; Seemann et al., 1986; Werk
et al., 1983). As such, we used a pair of winter annuals to examine how species’ differences in physiological traits might interact
with temperature variation to translate into demographic variation
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
Our previous research on physiological differences among
Sonoran Desert winter annuals has demonstrated that species
exhibit a trade-off between relative growth rate (RGR) and integrated water-use efficiency (WUE, assayed by leaf carbon isotope
discrimination, D) (Angert et al., 2007; Huxman et al., 2008;
Table 1). Species with high RGR exhibit high growth and allocational plasticity in response to infrequent, large precipitation pulses
(Angert et al., 2010) and have highly variable reproductive success
across years (Venable, 2007). Conversely, species with high WUE
exhibit low RGR but have more buffered population dynamics over
time (Venable, 2007). We have also found that winter annuals with
high WUE tend to have high nitrogen allocation to light-driven
dynamics of the Calvin cycle (Jmax) relative to carboxylation
(VCmax ) (Huxman et al., 2008). Maximum electron transport rate
(Jmax) is often a major controller of net assimilation rate at low
temperatures (Harley et al., 1992; Hikosaka et al., 2006), so we
hypothesized that elevated Jmax:VCmax would enhance carbon
assimilation at low temperatures. Together, these traits could favor
carbon assimilation during the reliably moist, but temporarily cool
and less light-saturating, periods following rainfall events. These
traits could also boost carbon assimilation during cool, earlymorning hours or early in the growing season, when evaporative
demand is lower. We also hypothesized that the high leaf nitrogen
observed in species with high Jmax:VCmax would incur a large respiratory load, particularly at warm temperatures, due to a higher
leaf protein concentration and the associated higher maintenance
respiration rates (Amthor, 2000; Ryan, 1995, Table 1). A decrease in
carbon assimilation efficiency would explain the low relative
growth rates observed in these species.
To test these hypotheses we studied two common, co-occurring
Sonoran Desert species (Pectocarya recurvata and Plantago insularis)
that differ in position along the physiological and population dynamic tradeoff mentioned above. We used gas exchange measurements to quantify photosynthetic and respiratory responses
across a range of leaf temperatures for both cold- and warmacclimated plants. We also used measures of chlorophyll fluorescence to further investigate the primary photochemistry of each
species at different temperatures to aid in our understanding of
how these plants dissipate excessive light energy when outside
their temperature optima. Given previously identified differences
in traits, we predicted that (i) the species with the greater Jmax:VCmax
ratio (Pectocarya) would have a lower photosynthetic temperature
optimum, (ii) that the species with the greater leaf nitrogen content
Table 1
Summary of ecophysiological measures previously conducted on two Sonoran
Desert winter annual plants with contrasting rates of resource use and allocation
and corresponding predictions for photosynthetic performance across a range of
atmospheric temperatures. These metrics illustrate the means by which leafphysiological traits may inform patterns of demography and species-specific
resource acquisition and utilization.
Ecophysiological
metric
Pectocarya
recurvata
(PERE)
Plantago
insularis
(PLIN)
Predictions for resource acquisition
and utilization
Jmax:VCmax
[
Y
Leaf [N]
[
Y
Water use
efficiency
Relative growth
rate (RGR)
[
Y
Y
[
PERE should have higher rates
electron transport (therefore,
better photosynthetic performance)
at low temperatures than PLIN
PERE should experience greater
respiratory CO2 loss at higher
temperatures than PLIN
PERE should be less constrained to
large, saturating precipitation events
Links between RGR and acclimation
potential suggest that PLIN may be
more able to acclimate to increased
temperature variability than PERE
97
(Pectocarya) would experience a more rapid increase in respiration
with temperature, and (iii) both species would shift the photosynthetic temperature optimum toward the growth temperature
(Table 1).
2. Materials and methods
2.1. Study species and experimental treatments
P. recurvata (Boraginaceae; hereafter, Pectocarya) and P. insularis
(Plantaginaceae; hereafter, Plantago) occur in the Sonoran and
Mojave Deserts of the southwestern United States and northwestern Mexico. The species commonly co-occur on low elevation
desert bajadas and creosote bush flats, where they germinate with
late autumn or winter rainfall, flower in early spring, and complete
their reproductive life cycle before the onset of the arid foresummer in May. Seeds were collected in April 2005 from The Desert
Laboratory at Tumamoc Hill, Arizona, (32130 N, 111010 W) and
were after-ripened by over-summering them in mesh bags in
outdoor shelters. In October, seeds were sown on 2% agar and
placed in a growth chamber at 22 C. Upon germination, seedlings
were transplanted into 164 mL ConeTainer pots (Stuewe & Sons,
Inc. Corvallis, Oregon) filled with 20-grit sand that had
been bleached and washed. Plants were grown in four controlled
environment chambers (Conviron E7/2, Controlled Environments
Ltd, Winnipeg, Manitoba, Canada) with an irradiance of
500 mmol m2 s1 and received a daily maintenance irrigation of
approximately 2 mL of a 1:20 Hoagland’s nutrient solution.
Growing plants under these chamber irradiance conditions (the
maximum capacity of the environmental chambers) should not
have created anomalous results as 500 mmol m2 s1 is approaching the light saturation point for these species, as determined from
a series of light response curves (unpublished data) and data
published for a congeneric annual (Niklas and Owens, 1989). Plants
were randomly shuffled weekly among the four chambers during
this initial phase of establishment. Just prior to initiating temperature acclimation treatments, we applied a large 20 mL pulse of
irrigation. Ten plants of each species were then randomly assigned
to a permanent treatment of either a cool (10/4 C, day/night) or
warm (20/5 C) acclimation temperature (Tacc), yielding five plants
per species per treatment. The cool treatment realistically simulated natural rain events, during and after which nighttime temperatures 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
extreme recorded differences, to better detect physiological responses and to provide insights for projected climate change scenarios for this region. To minimize unintended spatial and chamber
effects, plants were randomly shuffled within and between the
growth chambers assigned to the same temperature treatment.
Plants were provided with 2 mL maintenance irrigations daily.
Background environmental data were acquired using a weather
station (HOBO, Onset Computer Corp., Bourne, MA, USA) deployed
at The Desert Laboratory to examine changes in field temperature
and light conditions in response to winter precipitation events.
Longer-term records come from a NCDC/NOAA weather station at
the University of Arizona in Tucson, Arizona, USA (5.4 km from
study site), as described by Huxman et al. (2008).
2.2. Leaf-level gas exchange
Net photosynthesis rate versus internal [CO2] (AeCi) response
curves and measures of net photosynthetic and respiratory responses of attached leaves to temperature were determined with
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
species, we used the leaf chamber (model 6400-15) that provided
the smallest chamber gasket circumference and un-occupied
chamber space per unit leaf area, making it the most appropriate
chamber for this project. The red/blue LED light source (model
6400-02B) light source was secured over the clear-top leaf cuvette,
and a quantum sensor (LI-185) was used to verify light levels
transmitted through the transparent film of the cuvette (data not
shown). Once the leaf was placed into the chamber, we used Polytetrafluoroethylene grease provided by the chamber’s manufacturer (210-05774) to seal around the gas junctions. On each leaf
measured, we then directed high-concentration CO2 gas through
Bev-A-Line tubing (Thermoplastic Processes, Georgetown, DE, USA)
around this now-sealed gasket junction to ensure that no leak was
detectable by the instrument’s CO2 gas analyzer. AeCi response
curves were conducted using three individuals of each species at
a common temperature typical of an average growing season
(23 C).
Photosynthetic and respiratory temperature response curves at
ambient concentrations of CO2 were conducted on plants that were
transferred from the growth chamber to a large incubator, which
was used to control external air temperature (Percival Scientific,
model I-36LLVL, Perry, IA, USA) to match air temperatures within
the cuvette. As such, the entire plant experienced each step of the
leaf-chamber temperature response curve rather than individual
leaves. This minimized any temperature-induced pressure differences that might cause a leak into/from the measurement chamber
and extended the temperature range for our measurements beyond
the capacity of the LI-6400’s Peltier coolers. Leaves were clamped
within the cuvette, where they were incubated under saturating
light (1200 mmol photons m2 s1), ambient CO2 concentration,
a flow rate of 200 mmol s1, and a block temperature of 8 C. Leaf
temperature (Tleaf) was calculated based on standard energy balance equations as described in Huxman et al. (2008). After 30 min,
steady-state photosynthesis (Anet, mmol CO2 m2 s1), stomatal
conductance to water vapor (mol H2O m2 s1) and other associated parameters were recorded.
The light source was then turned off and leaf respiration rate
after five minutes in complete darkness (Rd) was determined.
Longer dark incubation is generally recommended (Atkin et al.,
1997; Laisk, 1977), however, prior to conducting these measurements, we used the Kok method (Kok, 1948; Sharp et al., 1984) to
determine how Rd estimates differed between shorter and longer
dark incubation periods. The Kok method estimates Rd from the
intercept of a light response curve, determined by measuring
photosynthetic rates after long periods of incubation across
sequentially decreasing, low light intensities. For these two species,
measurements after five minutes of darkness were stable (i.e., not
decreasing) and only minimally inflated (11%) compared to estimates after 30e60 min using the Kok method. Further, the estimates were similarly inflated for both species. Hence, we focus on
the comparison of relative differences in Rd among species and
temperatures, with the caveat that all estimates are likely to be
slightly inflated in an absolute sense by short-term dark incubation.
This process was repeated in 7 C increments from 8 C up to 36 C.
We minimized potentially confounding variation in vapor pressure
deficit between temperatures by varying the flow of air through
silica gel desiccant with a constant setpoint of approximately
1.5 kPa. Gas exchange measurements at each of the five block
temperature settings were conducted on four to six plants per
species per Tacc treatment. The temperature sensitivity (Q10) of Rd
was calculated as Q10 ¼ the Rd rate at T þ 10 C/Rd rate at T, where T
was set to acclimation temperature for each treatment.
We used repeated measures mixed models to examine the effects of Tleaf (linear and quadratic terms), species, Tacc, and their
interactions on Anet or Rd, using the Akaike Information Criterion to
select an autoregressive order 1 covariance structure (Littell et al.,
1996). We evaluated the significance of fixed effects with Type I
sums of squares, which generate sequentially formulated hypotheses that are appropriate for polynomial models (Littell et al., 1996),
with denominator degrees of freedom obtained by Satterthwaite’s
approximation (Satterthwaite, 1946). These analyses were performed with SAS Proc Mixed (SAS, version 9.1, SAS Institute Inc.,
Cary, NC, USA). ‘Estimate’ statements computed differences in
least-squares means for Anet or Rd between species within each Tacc
and between warm- and cold-acclimated plants of each species at
five Tleaf (8, 15, 22, 29, and 36 C). We also analyzed two key parameters of the photosynthetic temperature response curve, the
optimal temperature of photosynthesis (Topt) and the maximum
photosynthetic rate (Amax). For each individual, we fit a quadratic
equation to the curve of Anet versus Tleaf and solved for Topt where
the derivative of this equation equaled zero. Solving the quadratic
equation at Topt yielded Amax for each individual. We then used
analysis of variance (ANOVA) to examine the effects of species, Tacc,
and their interaction on Topt or Amax.
2.3. Chlorophyll fluorescence
To further decompose the photosynthetic response of each species to temperature, we measured patterns of chlorophyll fluorescence in response to a specific series of dark, moderate, and supersaturating light (Kitajima and Butler, 1975; Maxwell and Johnson,
2000). As detailed below, chlorophyll fluorescence parameters provide insight into several aspects of a leaf’s capacity for function, e.g.
light harvesting and electron transport, and the means by which the
leaf is dissipating excessive light energy when it cannot be used for
photosynthesis. Chlorophyll fluorescence was measured using
a pulse modulated chlorophyll fluorometer (FMS2, Hansatech Instruments Ltd, Norfolk, UK) at cool (15 C) and warm (29 C) measurement temperatures (Tmeas). These temperatures were chosen
because they are lower than and higher than typical Topt for photosynthesis, respectively. Plants were irrigated and then maintained at
15 C under lighted conditions (intensity w 500 mmol m2 s1) for
one hour. After 30 min of dark adaptation, initial fluorescence (Fo)
was measured in response to weak red irradiation (650 nm), and
then maximum fluorescence (Fm) was measured in response to
a saturating light pulse (intensity w 15,300 mmol m2 s1). Variable
fluorescence (Fv) was calculated as Fm Fo. Light sufficient to drive
photosynthesis (actinic light) was then applied for two minutes, and
the fluorescence level just prior to (F0 t) and during (F0 m) a second
saturating pulse was measured. After this pulse, actinic light was
switched off and fluorescence in response to far-red light (F0 o) was
measured (Maxwell and Johnson, 2000). Accompanying measurements of light intensity and leaf temperature were made with the
microquantum sensor/measurement arm of the FMS2. The entire
acclimation and measurement process was then repeated at 29 C.
Chlorophyll fluorescence measurements were conducted on five
plants per species per Tacc.
From this series of measurements, we calculated the maximum
quantum yield of photosystem II (Fv/Fm), which is a measure of the
proportion of all photons absorbed by chlorophyll that are used in
photochemistry. The quantum yield of photochemistry in open
photosystem II (PS II) reaction centers ready for electron capture
was also determined as F0 v/F0 m, where F0 v ¼ F0 m Ft (Genty et al.,
1989; Kitajima and Butler, 1975). We also calculated measures of
photochemical quenching (qP) as qP ¼ [(F0 m Ft)/(F0 m F0 o)]
(Maxwell and Johnson, 2000; Schreiber et al., 1995). qP was used to
gain insight into the proportion of PSII reaction centers that were
open. Non-photochemical quenching (NPQ) is induced under conditions when the photosynthetic apparatus cannot use all absorbed
G.A. Barron-Gafford et al. / Journal of Arid Environments 91 (2013) 95e103
light energy for photochemistry, which can occur at quite low light
intensity even under optimum conditions for photosynthesis.
Stressful conditions, such as high light intensity, low internal CO2
concentration due to drought, or low temperature, markedly promote NPQ. Therefore, the amount of NPQ is an indicator of stress
severity and measures changes in heat dissipation relative to the
dark-adapted state. NPQ was calculated as NPQ ¼ (Fm F0 m)/F0 m.
For each species separately, we analyzed each chlorophyll fluorescence variable (dark-adapted Fv/Fm, light-adapted F0 v/F0 m, qP,
and NPQ) with repeated measures ANOVA with fixed effects of Tacc,
Tmeas, and their interaction using SAS Proc Mixed (SAS, version 9.1,
SAS Institute Inc., Cary, NC, USA). We evaluated the significance of
fixed effects with Type III estimable functions. When ANOVA
indicated a significant main effect or interaction, we used Tukeye
Kramer adjusted comparisons of least square means to assess differences among levels of the effect. The PDMIX800 macro was used
to convert pairwise differences between least square means to
letter groupings, where means sharing the same letter code are not
significantly different (Saxton, 1998).
3. Results
3.1. Leaf level gas exchange: photosynthesis
Analysis of steady-state net photosynthesis (Anet) versus [CO2]
response curves showed that P. recurvata and P. insularis grown in
the growth chamber had a similar allocation to maximum electron
transport rates (Jmax) relative to carboxylation capacity (VCmax ) as
naturally-occurring, field-grown plants used in previous
studies (Huxman et al., 2008). Relative to one another, the species
had similar rates of VCmax (68.22 16.28 mmol m2 s1 and
62.44 13.21 mmol m2 s1 in Pectocarya and Plantago, respectively, P ¼ 0.6992), but Pectocarya had a significantly greater Jmax
than Plantago (414.40 48.04 mmol m2 s1 versus
178.63 45.55 mmol m2 s1, respectively, P ¼ 0.0403). Pectocarya
and Plantago differed in the response of Anet to leaf measurement
temperature (Tleaf), acclimation temperature (Tacc), and the
interaction between Tleaf and Tacc (Table 2A, Fig. 2). Although Anet
showed a significant quadratic response to Tleaf, the degree of
curvature was not affected by species or Tacc (Table 2A). Cold- and
warm-acclimated Pectocarya plants had Anet values for a given leaf
measurement temperature, indicating no photosynthetic acclimation to Tacc (Fig. 2a,b). However, warm-acclimated Plantago showed
greater Anet than cold-acclimated plants at most leaf temperatures
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.
Significance of fixed effects evaluated with Type I sums of squares (Littell et al.,
1996), with denominator degrees of freedom obtained by Satterthwaite’s approximation (Satterthwaite, 1946).
Source
A. Anet
Between-subjects
dfN
dfD
Species
Tacc
Species Tacc
1
1
1
14
14
14
Within-subjects
dfN
Tleaf
Tleaf species
Tleaf Tacc
Tleaf species Tacc
T2leaf
T2leaf species
T2leaf Tacc
T2leaf species Tacc
1
1
1
1
1
1
1
1
B. Rd
F
P
dfN
dfD
0.61
1.85
8.73
0.4476
0.1954
0.0105
1
1
1
14
14
14
dfD
F
P
dfN
65
65
65
64
64
64
64
64
49.19
53.72
0.7
6.75
69.16
2.84
2.21
0.31
<0.0001
<0.0001
0.4058
0.0116
<0.0001
0.0966
0.1418
0.5818
1
1
1
1
1
1
1
1
Significant effects are indicated in bold.
F
P
19.37
0.14
0.98
0.0006
0.7139
0.3384
dfD
F
P
75
76
76
76
63
63
63
63
126.16
37.74
0
1.96
32.4
4.56
0.05
0.78
<0.0001
<0.0001
0.9603
0.1658
<0.0001
0.0366
0.8228
0.3811
99
(Fig. 2c,d). When cold-acclimated, Pectocarya displayed greater Anet
than Plantago at low temperatures (Fig. 2a,c). Conversely, when
warm acclimated, Plantago displayed equivalent Anet to Pectocarya
at low temperatures but significantly greater Anet across higher
temperatures (Fig. 2b,d).
Pectocarya optimal temperature of photosynthesis (Topt) averaged 17.9 1.4 C when cold acclimated and 16.1 1.0 C when warm
acclimated, underscoring the lack of significant photosynthetic
acclimation in this species. For Plantago, Topt averaged 21.6 1.7 C
when cold acclimated but increased to 24.6 1.0 C when warm
acclimated. Thus, Topt of Pectocarya was significantly lower than that
of Plantago (F1, 14 ¼ 15.21, P ¼ 0.0016), regardless of acclimation
conditions. Although Anet data clearly suggest acclimation of Plantago to warm temperatures, Topt was not significantly affected by Tacc
(F1, 14 ¼ 0.15, P ¼ 0.76) or by the interaction between species and Tacc
(F1, 14 ¼ 2.45, P ¼ 0.14). Pectocarya maximum photosynthetic rate at
Topt (Amax) averaged 14.4 1.4 mmol CO2 m2 s1 when cold acclimated and 12.7 1.8 mmol CO2 m2 s1 when warm acclimated
(Fig. 2a,b). Plantago Amax averaged only 9.6 1.3 mmol CO2 m2 s1
when cold acclimated, but increased to 16.4 1.6 mmol CO2 m2 s1
when warm acclimated (Fig. 2c,d). Species differences in the
response of Amax to acclimation temperature are confirmed by
a significant species Tacc interaction (F1, 14 ¼ 6.61, P ¼ 0.02).
3.2. Leaf level gas exchange: respiration
Pectocarya and Plantago differed in the response of dark respiration (Rd) to increases in Tleaf, but neither species displayed an
apparent respiratory acclimation to Tacc (Table 2B). The species
experienced similar rates of Rd at low temperatures, but Pectocarya
experienced greater Rd under warmer temperatures (Table 3).
Furthermore, Pectocarya Rd rates were twice as sensitive to
increasing Tleaf (Q10 ¼ 2.00 0.31) than Plantago (0.98 0.11),
when cold acclimated, and 46% more sensitive (Q10 ¼ 2.76 0.40
for Pectocarya versus 1.89 0.36 for Plantago) when warm acclimated. The ratio of Rd:Anet provides a unitless measure of the influence of increasing temperature on carbon balance within the
plant because it normalizes rates of carbon loss (Table 3) relative to
each plant’s carbon gain at that measurement temperature (Fig. 2).
The Rd:Anet for Pectocarya was similar across lower temperatures,
but beyond 24 C, every 1 C increase in temperature increased the
ratio of carbon loss to gain 8.8 1.1% in cold acclimated plants and
26.9 6.3% in warm acclimated plants (Fig. 3a). The Rd:Anet ratio
remained unchanged across measurement temperatures in warmacclimated Plantago, and only declined for cold-acclimated Plantago
when exposed to leaf temperatures approaching 36 C (Fig. 3b).
3.3. Chlorophyll fluorescence: dark- and light-adapted yield
To more thoroughly examine physiological responses of these
species to temperature stress, we examined several chlorophyll
fluorescence parameters that provide insights into how efficiently
plants are harvesting light, transferring that light energy through
photochemistry when they are able to do so, and dissipating
excessive light energy when they are too stressed to maximize
photosynthesis. Measures of the maximum quantum yield of
photosystem II (Fv/Fm) illustrate the proportion of all photons
absorbed by chlorophyll that are used in photochemistry. Coldacclimated Plantago and Pectocarya had significantly higher levels
of dark-adapted Fv/Fm when measured at low temperatures than
when measured at high temperatures (Tables 4 and 5). There was
no significant difference, however, in Fv/Fm of warm-acclimated
plants measured at high versus low temperatures (Table 4). Both
species had greater Fv/Fm at cold Tmeas, and neither species displayed 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;
mmol CO2 m2 s1) 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
yield (F0 v/F0 m) when measured at cold temperatures, but unlike Fv/
Fm, this was true regardless of original Tacc (Tables 4 and 5B).
Additionally, Plantago displayed photosynthetic acclimation as
measured by increases in F0 v/F0 m in warm temperatures
(P ¼ 0.0203), but Pectocarya did not (P ¼ 0.1969, Table 5B). Thus,
measures of Plantago F0 v/F0 m were significantly greater at high
measurement temperatures relative to low temperatures, illustrating a greater amount of open photosystem II reaction centers
ready for electron capture under warmer conditions.
3.4. Chlorophyll fluorescence: non-photochemical and
photochemical quenching
suggesting a greater ability to adjust physiological processes associated with photosynthesis to deal with this change in temperature
(Table 5C). Neither species displayed a significant interaction between Tmeas and Tacc. Rates of induction of photochemical
quenching (proportion of open PSII reaction centers, qP) were significantly greater at the higher Tmeas regardless of species or Tacc
(Tables 3 and 5D). While both species were significantly affected by
Tacc, qP of Plantago showed a smaller magnitude of change between
warm and cold Tmeas when cold-acclimated, suggesting a greater
ability to maintain function across a range of temperatures. Neither
species was significantly affected by the Tmeas Tacc interaction
(Table 5D).
4. Discussion
Rates of induction of non-photochemical quenching (heat dissipation relative to the plant’s dark-adapted state; NPQ) were significantly greater in both species at warm Tmeas, regardless of Tacc,
indicative of reduced photosynthetic performance as temperature
increases (Tables 4 and 5C). Plantago, however, displayed a significant acclimation in terms of NPQ, while Pectocarya did not,
Our study identifies key trade-offs between physiological
function and resource acquisition/utilization within two cooccurring winter annuals that, ultimately, relate to patterns of
performance under varying environmental conditions. Previous
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).
Rd
Tacc:
Low
Tmeas:
8
15
22
29
36
8
15
22
29
36
Pectocarya
Plantago
1.85 (0.81)
2.1 (0.83)
2.74 (1.02)
0.85 (0.33)
4.81 (1.45)
2.05 (0.6)
10.76 (2.36)
3.8 (0.72)
14.34 (2.56)
6.8 (1.26)
2.85 (1.06)
1.04 (0.58)
2.6 (0.91)
0.88 (0.48)
5.91 (1.12)
1.95 (0.71)
11.35 (2.23)
2.35 (0.65)
15.81 (2.68)
4.87 (1.06)
High
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)
relative to carboxylation capacity (VCmax ) compared to Plantago,
which has lower values for these physiological traits (Huxman
et al., 2008, Table 1). Based on these findings, we proposed that
the physiology of desert annual species with traits like that of
Pectocarya may be optimized for carbon gain during predictably
moist, but cooler, growing conditions, while species with the
opposite traits, like Plantago, experience optimal performance
across a broader suite of temperatures, including warmer growth
conditions. Given patterns of cooler temperatures in the Sonoran
Desert immediately following rain events, early in the day, and
earlier in the winter growing season (Fig. 1c, d), these tradeoffs are
likely to decouple resource utilization and carbon gain dynamics
among co-occurring species across multiple temporal scales (e.g.,
daily, surrounding storm events, and seasonally).
4.1. Carbon balance across temperatures
Under colder acclimation conditions, Pectocarya out performed
Plantago under low-to-moderate temperatures in terms of net
photosynthetic rates (Anet). This greater function under cold conditions is likely tied to Pectocarya investment in greater Jmax:VCmax ,
allowing for greater electron transport under low-temperature
conditions than possible within Plantago (Fig. 2). However, these
same physiological traits have a cost in terms of function under
warmer temperatures. Many species experience a deactivation of
Jmax at elevated temperatures (Hikosaka et al., 2006), which leads to
Table 4
Means and standard errors (in parentheses) for the chlorophyll fluorescence parameters dark-adapted yield (Fv/Fm), light-adapted yield (F0 v/F0 m), nonphotochemical quenching (NPQ), and photochemical quenching (qP). Plants were
growth under low (10 C) and high (20 C) acclimation temperatures (Tacc) and then
measured under low (15 C) and high (29 C) measurement temperatures (Tmeas).
Fv/Fm
F0 v/F0 m
NPQ
qP
Tacc:
Low
Tmeas:
Low
Pectocarya
Plantago
Pectocarya
Plantago
Pectocarya
Plantago
Pectocarya
Plantago
0.82
0.84
0.64
0.65
1.51
1.56
0.15
0.18
High
High
(0.00)
(0.00)
(0.01)
(0.01)
(0.13)
(0.08)
(0.01)
(0.01)
0.80
0.82
0.50
0.47
2.11
2.80
0.37
0.31
Low
(0.01)
(0.01)
(0.02)
(0.01)
(0.20)
(0.09)
(0.02)
(0.02)
0.81
0.83
0.64
0.65
1.25
1.44
0.14
0.15
High
(0.00)
(0.00)
(0.01)
(0.01)
(0.08)
(0.05)
(0.01)
(0.01)
0.81
0.83
0.54
0.52
1.90
2.53
0.31
0.28
(0.00)
(0.00)
(0.02)
(0.01)
(0.22)
(0.14)
(0.02)
(0.02)
reduced RuBP regeneration and limited net CO2 uptake as temperature increases. Pectocarya’s elevated Jmax may explain the
patterns of reduced photosynthetic rates beyond 25 C. Badger et al.
(1982) showed that some plants grown under a low Tacc can have
higher activity of some photosynthetic enzymes at lower temperatures but then experience reduced heat stability at higher measurement temperatures relative to plants grown at a high Tacc,
similar to what we see with Pectocarya. Such a trade-off is important in understanding the temporal niches of these desert annual
species relative to the known weather variation existing in the
Sonoran Desert.
Pectocarya experienced greater respiratory carbon loss than
Plantago at moderate to high temperatures, regardless of Tacc
(Table 3). Increasing rates of respiration with temperature have
been shown repeatedly in the literature (Atkin et al., 2006; Griffin
et al., 2002; Teskey and Will, 1999). Rates of Pectocarya Rd at
15 C were approximately equal to those of Plantago at 30 C,
suggesting that high Rd rates of Pectocarya may be advantageous for
maintaining favorable carbon metabolism at lower temperatures.
These high Rd rates could be a byproduct of Pectocarya leaves
containing greater levels of nitrogen-rich proteins, which increase
Anet at lower temperatures yet decrease net assimilation under
warmer conditions. High leaf nitrogen content is often associated
with high protein concentration (Lexander et al., 1970), which leads
to higher maintenance respiration rates (Amthor, 2000; Wright
et al., 2001) and lower conversion efficiency of photosynthetic
assimilation to biomass. Atkin et al. (2006) note that because the
temperature sensitivity of light-saturated photosynthesis, lightrespiration, and dark-respiration are so different, short-term perturbations in air temperature alter the balance between photosynthesis (Anet) and respiration in individual leaves (Rd) and
dramatically affect the carbon balance of leaves. As such, we
directly analyzed the ratio of Rd:Anet and found that carbon balance
within Pectocarya tended toward much greater carbon loss under
higher temperatures (Fig. 3). Together, these results highlight
a trade-off between maximizing photosynthesis at low temperatures when evaporative demand is low, and minimizing respiration
when temperatures climb.
4.2. Patterns of optimality, plasticity and acclimation
Our results suggest that different suites of leaf physiological
characteristics should yield very different temporal niches for
102
G.A. Barron-Gafford et al. / Journal of Arid Environments 91 (2013) 95e103
Table 5
Repeated measures analysis of (A) dark-adapted PSII yield (Fv/Fm), (B) light-adapted PSII yield (F0 v/F0 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.
Species
Source
Pectocarya
recurvata
Between-subjects
Tacc
Within-subject
Tmeas
Tmeas Tacc
Between-subjects
Tacc
Within-subject
Tmeas
Tmeas Tacc
Plantago
insularis
B. F0 v/F0 m
A. Fv/Fm
dfN
1
dfN
1
1
dfN
1
dfN
1
1
dfD
10
dfD
10
10
dfD
10
dfD
10
10
F
0.21
F
15.58
10.9
F
0.43
F
6.06
10.19
P
0.6536
P
0.0027
0.008
P
0.529
P
0.0335
0.0096
F
1.91
F
162.38
4.28
F
7.59
F
215.69
5.07
C. NPQ
P
0.1969
P
<0.0001
0.0653
P
0.0203
P
<0.0001
0.0481
F
1.74
F
27.39
0.05
F
5.35
F
334.87
2.47
D. qP
P
0.2168
P
0.0004
0.8217
P
0.0434
P
<0.0001
0.147
F
5.48
F
155.11
0.42
F
7.07
F
102.54
0.81
P
0.0413
P
<0.0001
0.5307
P
0.0239
P
<0.0001
0.3896
Significant effects are indicated in bold.
optimal performance between these co-occurring species. We
found a lower temperature optimum (Topt) for Pectocarya than for
Plantago, regardless of acclimation temperature (Tacc; Fig. 2),
matching our hypothesis. Based on measures of both Rd and the
ratio of Rd:Anet, better performance under cool conditions is likely
tied to elevated carbon loss at higher temperatures. We found
a relative lack of acclimation of Pectocarya to the treatment differences, in either Topt or maximum photosynthetic rates (Amax),
which corresponded well with the limited allocational plasticity we
also have found in this species (Angert et al., 2010). In contrast,
Plantago demonstrated photosynthetic acclimation to temperature,
as evidenced by the significantly greater Anet at high temperatures
for warm-acclimated plants compared to cold-acclimated plants.
Plantago also showed some evidence of acclimation to cold, in that
Anet of cold-acclimated plants at low temperatures was a greater
percentage of Amax than for warm-acclimated plants measured at
low temperatures. However, the Amax of cold-acclimated Plantago
was significantly depressed relative to Amax of warm-acclimated
plants, indicating that acclimation to lower temperatures incurred a cost for Plantago. The overall depression of Plantago photosynthetic rates when cold-acclimated may be indicative of
a feedback inhibition, in that sink-strength could be reduced due to
limited respiration. A review by Atkin and Tjoelker (2003) suggested that limitations in maximum catalytic activity of respiratory
enzymes are likely the most limiting factor in restricting respiration
at low temperatures.
The lack of photosynthetic acclimation manifested by changes in
Topt (both species) or Amax (Pectocarya) observed here could be
a true inability to shift, but it is also possible that we measured
leaves produced before the change in temperature regime. Previous
studies, however, have shown acclimation to new temperatures in
preexisting leaves formed under previous growth temperatures
(Loveys et al., 2002; Pisek et al., 1973). In the desert environment,
changes in soil moisture availability and temperature occur quickly
and unpredictably. These species must respond to variation in
temperature and water availability on a much faster time scale than
would allow for the development of new canopy material. Only
following relatively rare periods of very high rainfall would soil
water availability persist for a sufficient period to deploy new
leaves (Angert et al., 2007, 2010). Therefore, it is likely that the lack
of acclimation observed in this study is relevant to the behavior of
these species in their natural environment under most conditions.
4.3. Chlorophyll fluorescence highlights biochemical differences in
plant function across temperatures
We used measures of chlorophyll fluorescence to further
investigate the physiology of the two species and their differences
in responses to acclimation and measurement temperatures. Significantly greater light adapted yield (F0 v/F0 m) at high relative to low
measurement temperatures for Plantago indicated both a greater
amount of open photosystem II reaction centers ready for electron
capture under warmer conditions and a greater capacity for photosynthetic acclimation. Combined with the data indicating lower
respiratory loss in Plantago at high temperatures (Fig. 2c,d), the
fluorescence data help explain the greater photosynthetic performance of Plantago than Pectocarya across higher temperatures. We
also calculated the rates at which the two species induced
quenching mechanisms to deal with excess excited energy (Müller
et al., 2001; Niyogi, 2000). Rates of induction of non-photochemical
quenching via heat dissipation (NPQ) were significantly greater in
both species at warm Tmeas, but Plantago NPQ illustrated a significant change in response to acclimation temperature, whereas
Pectocarya did not. These patterns suggest that Plantago may have
been regulating excessive electrons more actively via nonphotochemical, heat dissipating pathways, whereas Pectocarya
was preferentially using photochemical pathways to dissipate
excitation energy. The low rates of net assimilation of Pectocarya
indicate that photochemical quenching of electrons may have been
assimilatory, but rates of respiration might have been too high at
higher temperatures to yield a strong response of net carbon gain
(Berry and Björkman, 1980; Seemann et al., 1986; Yamasaki et al.,
2002).
5. Conclusions
Overall, Pectocarya had a lower temperature optimum, whereas
Plantago displayed greater photosynthetic performance at moderate and high temperatures and a capacity to adjust its physiological
functions to alterations in growth temperature. These differences in
both optimization and acclimation of photosynthesis may contribute to these species having different diel and seasonal peaks for
carbon assimilation and for maximizing photosynthetic function
across different time periods following rainfall events. Based solely
on the physiological differences demonstrated here, we would
predict that Pectocarya should display greater performance in years
dominated by early rains, small rain events, and cooler temperatures, whereas Plantago should display greater performance in
years characterized by large, saturating rainfall events, late-season
rainfall, or sequential rainfall events in which adequate soil moisture is present over a greater range of temperatures. Recent analysis
of inter-annual variation in demographic performance revealed
that species with high WUE, such as Pectocarya, did indeed have
greater relative fitness in years with small rain events and longer
durations between rain events than species with higher RGR, such
as Plantago (Kimball et al., 2011). Somewhat paradoxially, highWUE species also tended to have greater relative fitness in years
that were warmer, particularly toward the end of the growing
season (Kimball et al., 2011). High temperatures in the spring are
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
photosynthetic optimum may be more successful in a warm year by
virtue of being able to complete their growth and reproduction
during the earlier, cooler months of the growing season. This
finding reinforces the importance of the interaction between phenology and physiological traits, which together influence patterns
of temporal resource partitioning. Given our understanding of the
within-year and year-to-year environmental variation and patterns
of demography, differences in patterns of peak physiological function may contribute to the coexistence of these species in the variable desert environment.
Acknowledgments
The authors thank C. Pearson, A. Hazard, M. Martineau, H.
Lawson, and S. Kunkel for assistance with plant care. J. Gremer and
S. Kimball provided helpful comments on earlier drafts. This
research was supported by the National Science Foundation DEB
0453781 to DLV and TEH and DEB 0817121 to DLV. Additional
support from the Philecology Foundation of Ft. Worth Texas supported this project. This experiment complies with the current laws
of the United States of America.
References
Amthor, J.S., 2000. The McCree-de Wit-Penning de Vries-Thornley respiration
paradigms: 30 years later. Annals of Botany 86, 1e20.
Angert, A.L., Horst, J.L., Huxman, T.E., Venable, D.L., 2010. Phenotypic plasticity and
precipitation response in Sonoran Desert winter annuals. American Journal of
Botany 97, 405e411.
Angert, A.L., Huxman, T.E., Barron-Gafford, G.A., Gerst, K.L., Venable, D.L., 2007.
Linking growth strategies to long-term population dynamics in a guild of desert
annuals. Journal of Ecology 95, 321e331.
Atkin, O.K., Scheurwater, I., Pons, T.L., 2006. High thermal acclimation potential of
both photosynthesis and respiration in two lowland Plantago species in contrast
to an alpine congeneric. Global Change Biology 12, 500e515.
Atkin, O.K., Tjoelker, M.G., 2003. Thermal acclimation and the dynamic response of
plant respiration to temperature. Trends in Plant Science 8, 343e351.
Atkin, O.K., Westbeek, M.H.M., Cambridge, M.L., Lambers, H., Pons, T.L., 1997. Leaf
respiration in light and darkness e a comparison of slow- and fast-growing Poa
species. Plant Physiology 113, 961e965.
Badger, M.R., Bjorkman, O., Arnold, P.A., 1982. An analysis of photosynthetic response
and adaptation to temperature in higher plants: temperature acclimation in the
desert evergreen Nerium oleander L. Plant, Cell, Environment 5, 85e99.
Barron-Gafford, G.A., Scott, R.L., Jenerette, G.D., Hamerlynck, E.P., Huxman, T.E.,
2012. Temperature and precipitation controls over leaf- and ecosystem-level
CO2 flux along a woody plant encroachment gradient. Global Change Biology
18, 1389e1400. http://dx.doi.org/10.1111/j.1365-2486.2011.02599.x.
Berry, J., Björkman, O., 1980. Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology and Plant Molecular
Biology 31, 491e543.
Chesson, P., Gebauer, R.L.E., Schwinning, S., Huntly, N., Wiegand, K., Ernest, M.S.K.,
Sher, A., Novoplansky, A., Weltzin, J.F., 2004. Resource pulses, species interactions, and diversity maintenance in arid and semi-arid environments.
Oecologia 141, 236e253.
Cui, M.Y., Caldwell, M.M., 1997. A large ephemeral release of nitrogen upon wetting of
dry soil and corresponding root responses in the field. Plant and Soil 191, 291e299.
Forseth, I.N., Ehleringer, J.R., 1982. Ecophysiology of 2 solar-tracking desert winter
annuals. 1. Photosynthetic acclimation to growth temperature. Australian
Journal of Plant Physiology 9, 321e332.
Genty, B., Briantais, J.M., Baker, N.R., 1989. The relationship between the quantum
yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87e92.
Griffin, K.L., Turnbull, M., Murthy, R., Lin, G., Adams, J., Farnsworth, B., Mahato, T.,
Bazin, G., Potasnak, M., Berry, J.A., 2002. Leaf respiration is differentially affected
by leaf vs. stand-level night-time warming. Global Change Biology 8, 479e485.
Harley, P.C., Thomas, R.B., Reynolds, J.F., Strain, B.R., 1992. Modeling photosynthesis
of cotton grown in elevated CO2. Plant Cell and Environment 15, 271e282.
Hikosaka, K., Ishikawa, K., Borjigidai, A., Muller, O., Onoda, Y., 2006. Temperature
acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. Journal of Experimental Botany 57,
291e302.
Huxman, T.E., Barron-Gafford, G., Gerst, K.L., Angert, A.L., Tyler, A.P., Venable, D.L.,
2008. Photosynthetic resource-use efficiency and demographic variability in
desert annual plants. Ecology 89, 1554e1563.
Huxman, T.E., Snyder, K.A., Tissue, D., Leffler, A.J., Ogle, K., Pockman, W.T.,
Sandquist, D.R., Potts, D.L., Schwinning, S., 2004. Precipitation pulses and carbon fluxes in semiarid and arid ecosystems. Oecologia 141, 254e268.
103
Kimball, S., Gremer, J.R., Angert, A.L., Huxman, T.E., Venable, D.L., 2011. Fitness and
physiology in a variable environment. Oecologia 169, 319e329.
Kitajima, M., Butler, M.L., 1975. Quenching of chlorophyll fluorescence and primary
photochemistry in chloroplasts by dibromothymoquinone. Biochimica Biophysica Acta 376, 105e115.
Kok, B., 1948. A critical consideration of the quantum yield of Chlorella-photosynthesis. Enzymology 13, 1e56.
Laisk, A.K., 1977. Kinetics of Photosynthesis and Photorespiration in C3-Plants.
Nauka, Moscow.
Lange, O.L., Schulze, E.D., Evenari, M., Kappen, L., Buschbom, U., 1974. Temperaturerelated photosynthetic capacity of plants under desert conditions. 1. Seasonal
changes of photosynthetic response to temperature. Oecologia 17, 97e110.
Lexander, K., Carlsson, R.,V.,S., Simonsson, A., Lundborg, T., 1970. Quantities and
qualities of leaf protein concentrates from wild species and crop species grown
under controlled conditions. Annals of Applied Biology 66, 193e216.
Littell, R.C., Milliken, G.A., Stroup, W.W., Wolfinger, R.D., 1996. SAS System for Mixed
Models. SAS Institute Inc., Cary, N. C.
Loveys, B.R., Scheurwater, I., Pons, T.L., Fitter, A.H., Atkin, O.K., 2002. Growth temperature influences the underlying components of relative growth rate: an
investigation using inherently fast- and slow-growing plant species. Plant Cell
and Environment 25, 975e987.
Maxwell, K., Johnson, G.N., 2000. Chlorophyll fluorescence e a practical guide.
Journal of Experimental Botany 51, 659e668.
McGill, B.J., Enquist, B.J., Weiher, E., Westoby, M., 2006. Rebuilding community
ecology from functional traits. Trends in Ecology & Evolution 21, 178e185.
Mooney, H.A., Björkman, O., Collatz, G.J., 1978. Photosynthetic acclimation to temperature in desert shrub, Larrea divaricata. 1. Carbon dioxide exchange characteristics of intact leaves. Plant Physiology 61, 406e410.
Müller, P., Xiao-Ping, L., Niyogi, K.K., 2001. Non-photochemical quenching:
a response to excess light energy. Plant Physiology 125, 1558e1566.
Niklas, K.J., Owens, T.J., 1989. Physiological and morphological modifications of
Plantago major (Plantaginaceae) in response to light conditions. American
Journal of Botany 76, 370e382.
Niyogi, K.K., 2000. Safety valves for photosynthesis. Current Opinion in Plant
Biology 3, 455e460.
Nobel, P.S., Longstreth, D.J., Hartsock, T.L., 1978. Effect of water stress on temperature optima of net CO2 exchange for 2 desert species. Physiologia Plantarum 44,
97e101.
Novoplansky, A., Goldberg, D.E., 2001. Effects of water pulsing on individual performance and competitive hierarchies in plants. Journal of Vegetation Science
12, 199e208.
Noy-Meir, I., 1973. Desert ecosystems: environment and producers. Annual Review
of Ecology and Systematics 4, 25e51.
Pisek, A., Larcher, W., Vegis, A., Napp-Zinn, K., 1973. The normal temperature range.
In: Precht, H., Christopherson, J., Hensel, H., Larcher, W. (Eds.), Temperature and
Life. Springer, Berlin, pp. 102e194.
Reynolds, J.F., Kemp, P.R., Ogle, K., Fernandez, R.J., 2004. Modifying the ‘pulsereserve’ paradigm for deserts of North America: precipitation pulses, soil water,
and plant responses. Oecologia 141, 194e210.
Ryan, M.G., 1995. Foliar maintenance respiration of subalpine and boreal trees and
shrubs in relation to nitrogen content. Plant Cell and Environment 18, 765e772.
Satterthwaite, F.W., 1946. An approximate distribution of estimates of variance
components. Biometrics Bulletin 2, 110e114.
Saxton, A.M., 1998. A macro for converting mean separation output to letter
groupings in Proc Mixed. In: Proceedings of the 23rd SAS Users Group Intl. SAS
Institute, Nashville, TN.
Schreiber, U., Bilger, W., Neubauer, C., 1995. Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Schule, E.D., Caldwell, M.M. (Eds.), Ecophysiology of Photosynthesis. Springer, New York,
pp. 49e70.
Schwinning, S., Sala, O.E., 2004. Hierarchy of responses to resource pulses in arid
and semi-arid ecosystems. Oecologia 141, 211e220.
Seemann, J.R., Downton, W.J.S., Berry, J.A., 1986. Temperature and leaf osmotic
potential as factors in the acclimation of photosynthesis to high temperature in
desert plants. Plant Physiology 80, 926e930.
Sharp, R.E., Matthews, M.A., Boyer, J.S., 1984. Kok effect and the quantum yield of
photosynthesis: light partially inhibits dark respiration. Plant Physiology 75,
95e101.
Shreve, F., Wiggins, I.L., 1964. Vegetation and Flora of the Sonoran Desert. Stanford
University Press, Stanford.
Teskey, R.O., Will, R.E., 1999. Acclimation of loblolly pine (Pinus taeda) seedlings to
high temperatures. Tree Physiology 19, 519e525.
Venable, D.L., 2007. Bet hedging in a guild of desert annuals. Ecology 88, 1086e
1090.
Werk, K.S., Ehleringer, J., Forseth, I.N., Cook, C.S., 1983. Photosynthetic characteristics of Sonoran Desert winter annuals. Oecologia 59, 101e105.
Woodhouse, C.A., 1997. Winter climate and atmospheric circulation patterns in the
Sonoran Desert region, USA. International Journal of Climatology 17, 859e873.
Wright, I.J., Reich, P.B., Westoby, M., 2001. Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and highand low-nutrient habitats. Functional Ecology 15, 423e434.
Yamasaki, T., Yamakawa, T., Yamane, Y., Koike, H., Satoh, K., Katoh, S., 2002. Temperature acclimation of photosynthesis and related changes in photosystem II
electron transport in Winter wheat. Plant Physiology 128, 1087e1097.