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Physiology and Biochemistry |
School of Forestry and Environmental Studies, Yale University, 370 Prospect St., New Haven, Connecticut 06511 USA
Received for publication July 14, 2006. Accepted for publication March 19, 2007.
ABSTRACT
To investigate the relationship between the altitudinal distribution of Quercus laceyi and Q. sideroxyla and their physiological responses to drought, we measured relative water content (RWC), water potentials (
predawn and midday), photosynthesis (Amax), stomatal conductance (g), chlorophyll fluorescence (Fv/Fm), and spectral reflectance (400–1100 nm) five times during a 7 wk acute drought. Quercus laceyi was drought tolerant, while Q. sideroxyla was a drought avoider; Q. laceyi tolerated lower RWC (Q. sideroxyla = 54%, Q. laceyi = 44%), pd (Q. sideroxyla = –2.6 MPa, Q. laceyi = –3.3 MPa), and md (Q. sideroxyla = –4.5 MPa, Q. laceyi = –6.6 MPa). The Fv/Fm also declined first in Q. sideroxyla in wk 6, whereas Fv/Fm did not decline in Q. laceyi until wk 7. Amax and g fell in wk 4, 6, and 7 in drought seedlings of both species, suggesting a decline in CO2 assimilation during the drought. Leaf spectral reflectance increased with time in response to decreases in leaf photosynthetic pigment concentrations in latter weeks of the drought. The results suggest a close association between the altitudinal distributions of these species and their adaptation to water stress.
Key Words: chlorophyll fluorescence • elevation gradient • Fagaceae • photosynthetic efficiency • Quercus • spectral reflectance • stress physiology • water relations
The genus Quercus (oaks; Fagaceae) is one of the most diverse groups of temperate trees, with greater than 500 species in the temperate and subtropical latitudes of the Old and New worlds (Nixon, 1993
). Mexico represents the origin of oak diversification in North America and contains the highest oak diversity in the world (Muller and McVaugh, 1972
; Rzedowski, 1978
; González, 1993
; Nixon, 1993
). Oak and pine–oak forests cover almost half (45%) of the temperate coniferous forest of Mexico (World Forest Institute, 1994
) and are globally significant centers of vascular plant diversity and of endemism in both plant and animal species (Manuel-Toledo and Jesús-Ordóñez, 1993). However, the mechanisms underlying oak diversification across Mexico are poorly understood.
With 63% of its surface area covered by desert, Mexico contains the most arid regions in North America. In these extreme environments, water is the predominant factor limiting carbon gain and primary production (Noy-Mier, 1973
; DeLucia and Schlesinger, 1991
; Lajtha and Getz, 1993
; Kozlowski and Pallardy, 1997
). Yet, no published information quantifies the variability of oak drought tolerance in relation to species distribution patterns in Mexico.
Oaks are some of the most drought tolerant trees of the temperate latitudes (Abrams, 1990
; Ogaya and Peñuelas, 2003
; Aranda et al., 2005
). North American oaks are adapted to drought prone sites through a variety of mechanisms including drought avoidance and drought tolerance (Abrams, 1990
, 1996
), and the distribution of oak species in the United States is tightly linked to the physiological, anatomical, and morphological variation among species and across sites (Kubiske and Abrams, 1992
; Ashton and Berlyn, 1994
).
Understanding the relationship between oak physiology and moisture regimes is especially important in arid regions of North America, where precipitation is already greatly exceeded by evaporative demand and where the water deficit might be increased as a result of global warming (Houghton et al., 2001
; Loik et al., 2004
). Some reports describe the response of several oak species in the Rocky Mountains (Neilson and Wullstein, 1987
; Dickson and Tomlinson, 1996
; Ehleringer and Phillips, 1996
; Balok and St. Hilaire, 2002
), yet to our knowledge, no prior research explains the effects of moisture regime variability across mountain ranges on oak ecophysiology and adaptations to water stress in the oak species complexes in Mexico.
The objective of this study was to measure the physiological responses of a high and a low elevation endemic Mexican oak species of the genus Quercus to an experimental acute drought similar to that experienced by seedlings in the field before the onset of the North American Monsoon System (NAMS), which occurs in the spring across the southwestern United States and Northern Mexico (Adams and Comrie, 1997
). Our intent was to investigate the physiological mechanisms responsible for the distribution of two oak species, Quercus laceyi Small (subgenus Leucobalanus; Fagaceae) and Q. sideroxyla Humb. et Bonpl (subgenus Erythrobalanus; Fagaceae), on different sites within the same mountain range.
Seedling performance was examined under two moisture regimes (unlimited water and drought) on two species inhabiting sites that vary dramatically in local environmental conditions. Quercus laceyi is the lowest elevation tree of any species in the Sierra del Carmen, Coahuila, Mexico, and it is the dominant low-elevation oak in savannahs and riparian areas. It is a medium stature tree that ranges from 3–8 m in height, and it typically colonizes hot, dry sites. Quercus sideroxyla is the dominant high-elevation oak in the Sierra del Carmen. This species colonizes cooler, wetter sites compared to Q. laceyi. It coexists with a mixture of other oak and conifer species in closed canopy forests that reach over 30 m in height. The two species have overlapping elevational ranges, but occur in different forest types giving them spatially segregated distributions.
By measuring a suite of physiological parameters during an imposed 7-wk drought, we tested the hypothesis that these species have distinct physiological responses to drought that reflect their different altitudinal distributions. Differences in the physiological response of these species to drought may explain the niche differentiation or specialization of oaks on different sites within the same mountain range (May and MacArthur, 1972
; Pianka, 1976
). Furthermore, this research has the potential to elucidate the mechanisms responsible for the high oak diversity in northern Mexico.
MATERIALS AND METHODS
Experimental conditions and experimental design
Ripe acorns were collected from 20 mature trees of each species in the Sierra del Carmen of Coahuila, Mexico in November 2004 (Fig. 1). In montane woodlands of this region, acorns mature in the fall, germinate, and establish under frequent winter precipitation, and are then exposed to a prolonged drought from March until mid-July when precipitation returns with the NAMS. While stratification is necessary for the germination of some oaks of the subsection Erythrobalanus, oaks in the southwestern United States and Mexico germinate readily after maturation (Nyandiga and McPherson, 1992
).
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Eighty percent of the acorns planted in our study germinated under greenhouse conditions. No information exists that describes the germination success of these two species in the field. However, two similar species, Q. arizonica Sarg. (subgenus Leucobalanus) and Q. emoryi Torr. (subgenus Erythrobalanus), also in the Sierra del Carmen, had 72% and 21% germination, respectively, under field conditions in Arizona (Nyandiga and McPherson, 1992
).
After 3 wk, when the radical was 3 cm long, germinants were transplanted to 10-cm plastic pots. Seedlings were transplanted again to 18-cm plastic pots filled with Metromix growing medium on 18 September 2005. A modified Hoagland's nutrient solution (Hoagland and Arnon, 1950
) was applied monthly for 3 mo to all plants before the onset of the experiment. Metromix growing medium was chosen because it is a commercially available medium that drains well. The soils of the natural habitats of the two species are generally shallow to moderately deep and are volcanic in origin. The underlying rocks are predominantly extrusives, consisting of lavas and pyroclastics.
On 21 March 2006, 120 healthy seedlings of each species (240 total) were divided into two treatments, drought and control, using a completely randomized sampling design. The date of experiment onset was chosen to simulate the drought experienced by these species in the field before the onset of the NAMS (Adams and Comrie, 1997
). High temperatures and little precipitation characterize the natural drought. No climatic data exist for the Sierra del Carmen, but mean annual precipitation for the Chisos Basin approximately 150 km to the north is 70 cm (range 32–135 cm from 1948–2003). Mean January precipitation is 1.5 cm (range 0–2.5 cm), mean precipitation in March before the NAMS is 0.1 cm (range 0–3.7 cm), and mean precipitation in July during the NAMS is 8.0 cm (range 0.2–20.5 cm). Mean monthly minimum temperatures are 1.8°C in January, 6.3°C in March and 17.0°C in July. Maximum temperatures are 14.1°C in January, 20.9°C in March, and 29.1°C in July. Relative humidity during the drought (March–July) fluctuates between 10 and 25%. Daily greenhouse temperatures and relative humidity were not controlled during the experiment, although the mean relative humidity and temperatures were within the ranges experienced by seedlings in the field during the natural drought.
The experimental unit was a single seedling in a pot, and soil moisture was monitored using gravimetric methods. All pots were watered to saturation (field capacity) at the onset of the experiment and were weighed. Control seedling pots were watered to 100% of field capacity three times per wk by bringing them to their field capacity weight. After initial watering, seedlings in the drought treatment were exposed to an acute drought, where water was completely withheld for the duration of the experiment. Drought seedlings were weighed weekly to determine their percentage of field capacity mass. Drought seedlings reached 10% field capacity at the end of the experiment (reached 48 d after the onset of the drought treatment).
Water relations
Predawn (0400 to 0500 hours) and midday (1200 to 1300 hours) water potentials (pd and md) (MPa) were measured at the onset of the experiment, and at 2, 4, 6, and 7 wk into the experiment. Three individuals of each species-treatment combination (N = 12) were destructively sampled at predawn for the determination of pd using a pressure chamber (PMS Instruments, Corvallis, Oregon, USA). Water potential measurements were repeated at 1200 hours on the same days on 12 additional individuals to obtain midday md values.
Leaf relative water content (RWC) was determined for five leaf discs from leaves on the same seedlings used in the measurements. Leaf discs were cut and immediately weighed on a digital balance (A & D Systems, Milpitas, California, USA) to obtain their fresh mass (FM). Leaf discs were then saturated to full turgor by immersing them in distilled water in the dark for 24 h. Leaves were reweighed to obtain their turgid mass (TM) and put into an oven at 70°C for 3 d to obtain their dry mass (DM). RWC was calculated as: RWC = (FM – DM)/(TM – DM) x 100.
Repeated physiological measurements
Carbon assimilation (A), stomatal conductance (g), intracellular CO2 concentrations (Ci), chlorophyll fluorescence (Fv/Fm), and spectral reflectance were measured on a subset of 40 individuals (10 individuals from each species-treatment combination) at each of the sampling intervals (onset, 2 wk, 4 wk, 6 wk, and 7 wk) during the drought. A mature, fully expanded leaf was chosen at the onset of the experiment for the repeated physiological measurements, and the same leaf was used at each of the subsequent sampling intervals. All repeated physiological measurements were conducted between 0800 and 1130 hours.
Maximum photosynthesis (Amax), g, and Ci were measured in situ using an open-system portable infrared gas analyzer (Welles, 1986
) (LI-6400, Li-Cor, Lincoln, Nebraska, USA). Measurements of Amax were taken under saturating light (1800 µmol·m–2·s–1) using the LED attachment for the LI-6400 photosynthesis system. Light curves were used to verify saturating light levels for the two species (data not shown).
The maximum efficiency of photosystem II (PSII) chemistry (Fv/Fm) was measured in situ on attached leaves using a portable pulse-modulated fluorometer (OS 500, Opti-Sciences, Hudson, New Hampshire, USA). Leaves were dark-adapted for 1 h, which was sufficient to allow complete relaxation of energy-dependent quenching. The ratio Fv/Fm was calculated as (Fm – Fo)/Fm, where Fm and Fo are the maximum and basal fluorescence yields, respectively, of dark-adapted leaves (Gentry et al., 1989
).
Spectral reflectance of the upper leaf surface (adaxial side) was measured using a UNIspec Spectral Analysis System (PP Systems, Haverhill, Massachusetts, USA) over the range of 400-1000 nm with a 2.0 mm diameter foreoptic and an internal 6.8 W halogen lamp. Standard controls were dark and a spectralon reflectance white standard. The UNIspec unit was recalibrated after every 10 measurements using the reflectance white standard. Leaves were held in a black polyvinyl chloride (PVC) clip at a 60° angle relative to the foreoptic for scanning (R
= leaf radiance at wavelength ). We used four indices based on the reflectance properties of plant pigments and their biochemical components to identify differences in the reflectance spectra according to species and treatment: (1) a measure of carotenoids: chlorophyll a ratio, the structure independent pigment index (Peñuelas et al., 1995
) (SIPI) = (R800 – R445)/(R800 – R680); (2) the normalized difference vegetation index, NDVI = (R750 – R680)/(R750 + R680); (3) a revised version of NDVI that is sensitive to chlorophyll a concentrations (Gitelson and Merzlyak, 1996
), chlNDI = (R750 – R705)/(R750 + R705); and (4) a water band index, WBI = (R900 + (R900 – R830))/R970, a measure of vegetation water content (Riedell and Blackmer, 1999).
The red edge position (REP) is the name given to the change in reflectance in the 670–780 nm range of vegetation spectra caused by strong chlorophyll absorption by photosystems I and II and by internal leaf scattering. It is defined as the wavelength of the inflection point of the reflectance slope across this region and is indicative of leaf chlorophyll content. Under stress, the red edge position shifts toward the shorter wavelengths as a result of senescence or stress-induced chlorosis (Rock et al., 1988
; Peñuelas et al., 1994
; Thorhaug et al., 2006
). REP was calculated using the four-points formula developed by Guyot et al. (1992)
, which performs well in comparison to other more computationally intensive REP measures (Pu et al., 2003
). The REP was determined by calculating the reflectance at the red edge inflection point (Rre) given by Rre = (R670 + R780)/2, and then by deriving the red edge wavelength (re) given by re = 700 + 40*[(Rre – R700)/(R740 – R700)] where R670,R700, R740, and R780 are the reflectance values at 670, 700, 740, and 780 nm wavelength, respectively.
Growth and biomass allocation
Seedling growth and dry mass gain were determined at the end of the experiment for 20 individuals in each species-treatment combination (N = 80) in a stratified random manner. Species height and leaf number were determined on the same individuals at the onset of the experiment and at wk 4 and 7. Root collar diameter was measured at wk 4 and 7. Seedlings were harvested at the end of the experiment, and leaves, stems, and roots were separated, dried at 70°C for 3 d, and then dried at 90°C until a constant mass was reached. Whole shoot and root dry masses were recorded for each individual, and the root : shoot ratio (R : S) was calculated. The differences between root and shoot masses in the control and the drought treatment were also determined.
Statistical analyses
Multifactor ANOVAs were used to determine the effects of species, treatment, and time on seedling performance. All statistical analyses were performed using the R Statistical Language (R Development Core Team, 2005
). RWC, pd, md, dry plant matter mass (leaves, stems, roots), and root : shoot measurements were analyzed using a general linear model (GLM) procedure with fixed effects of species, treatment, and time and the interaction effects of species x treatment, species x time, treatment x time, and species x treatment x time. Differences between species–treatment combinations at each sampling interval were determined using a Tukey's test of significant difference. Differences between pd and md measurements were also were assessed using a GLM. Repeated measurements of Amax, Ci, g, SIPI, PRI, chlNDI, NDVI, WBI, RE, Fv/Fm, and seedling growth (number of leaves, height, root collar diameter) were analyzed using separate ANOVAs with repeated measures by a mixed models procedure with species and treatment as fixed effects and time as a random effect. Mixed models were used rather than repeated measures GLMs to account for differences in the covariance structure of the repeated measures. A regression was also performed to assess the relationship between Amax and g.
RESULTS
Water relations
The ANOVAs (Table 1) revealed significant (P < 0.0001) effects of treatment, time, and the interaction of treatment x time for md, which demonstrated the impact of the drought treatment on the seedlings of both species, and showed the accelerating impact of drought over time. Species-level differences for md were significant at P < 0.01. Differences between pd and md were significant (P < 0.0001) according to a GLM test. Quercus sideroxyla had significantly higher pd, md, and RWC than Q. laceyi (P < 0.01) at the onset of the experiment. Species differences in pd and md continued throughout the drought, with Q. laceyi having consistently lower pd and md than Q. sideroxyla (P < 0.05). Treatment-level differences in pd and md were significant (P < 0.05) beginning in wk 4 (Table 2).
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, and they differed little between treatments or species until wk 6 and 7 of the drought (Table 2). Chlorophyll fluorescence in Q. sideroxyla declined first during wk 6 of the drought, while Q. laceyi had no significant decline in chlorophyll fluorescence until wk 7 (P < 0.05).
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The red edge differed significantly (P < 0.01) by species, treatment, and time (Tables 1 and 2). Quercus sideroxyla had a higher REP than Q. laceyi at all samplings until wk 6 of the drought, when treatment-level differences became significant (P < 0.05). The shift in REP toward shorter wavelengths in drought seedlings began in wk 6, although treatment effects were most pronounced in wk 7.
Growth and biomass allocation
Treatment effects on plant height were evident in wk 4 and 7 (P < 0.05) (Tables 1 and 2). Quercus sideroxyla had significantly more leaves than Q. laceyi (Tables 1 and 2), but there were no significant treatment effects on leaf number. Control seedlings had significantly (P < 0.001) thicker root collar diameters than drought seedlings (Tables 1 and 2).
Control seedlings had significantly greater (P < 0.01) root and shoot biomass than drought seedlings, and control Q. sideroxyla had greater (P < 0.001) dry root mass than Q. laceyi (Table 1). Decline in root and shoot mass was significantly greater (P < 0.01) with Q. sideroxyla than Q. laceyi (Fig. 5A, B). Quercus sideroxyla roots were longer and more branched than those of Q. laceyi, and control seedling roots were longer and more branched than drought seedling roots. Root : shoot ratios did not differ significantly between species or treatments.
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Our results suggest that the oaks of northern Mexico have evolved to survive and reproduce under a range of climatic conditions. The species-level differences in oak physiology reflect each species' adaptation to local growing conditions, potentially explaining the differentiation and diversification of oaks within and between mountain ranges in Mexico. The similar drought responses of Q. laceyi and Q. sideroxyla suggest that both species are well adapted to drought, although their performance differs substantially under conditions that are not moisture-limited.
The dominance of Q. sideroxyla on cooler, wetter sites is explained by its higher photosynthesis, stomatal conductance, relative water content, and water potentials and its lower spectral reflectance relative to Q. laceyi, conferring competitive advantages on high-productivity sites at upper elevations. Likewise, the dominance of Q. laceyi on hotter, drier sites reflects its adaptation to the more extreme conditions typical at lower elevations. Our water potential (pd and md) and reflectance ratio data corroborate these findings, by showing that Q. laceyi was better able to carry out key physiological processes than was Q. sideroxyla under drought conditions. This suggests that Q. sideroxyla avoids drought as a high-elevation site specialist, while Q. laceyi is a drought tolerant species that competes well under more extreme, low elevation conditions.
In general, higher water potential, higher photosynthetic rate, and higher relative water content equate to less drought tolerance in oaks (Nardini et al., 1999
; Fotelli et al., 2000
; Thomas and Gausling, 2000
). While our results suggest that Q. sideroxyla is less drought adapted than is Q. laceyi, Q. sideroxyla remained highly resilient to drought, even with its initially higher water potentials, photosynthetic rate, and relative water content. A possible explanation for this pattern is that the high variability in year-to-year precipitation in southwestern North America has caused species across a range of elevations to be adapted to wet and dry climatic cycles in order to persist long-term. Such findings further suggest that even less drought tolerant species such as Q. sideroxyla may be able to persist under future climate change scenarios (Houghton et al., 2001
).
Biomass allocation and growth
The first and most sensitive response to water deficiency is a decrease in turgor and a slowing of the growth processes (Larcher, 2003
). Plants of both species were shorter, had smaller root collars, and allocated less biomass to roots and shoots in the drought than in the control treatment because the rate of cell division and the duration of leaf expansion drop as cell turgor declines. Likewise, the drop in photosynthesis during the drought limited CO2 assimilation, thereby limiting growth.
Water relations
Plant water status is controlled by the relative rates of water absorption (uptake by roots) and water loss (transpiration), and a plant's drought tolerance depends upon its ability to tolerate internal water deficits. As soil moisture is depleted under drought, the leaf water content and the overnight recovery of are inhibited by progressive increases in liquid flow resistance by the soil or plant (Kozlowski and Pallardy, 1997
). The lower RWC and water potentials (pd and md) of Q. laceyi relative to Q. sideroxyla suggest that Q. laceyi is more drought tolerant than Q. sideroxyla because it is better able to endure extreme water deficits, although these differences in adaptation did not translate to species' differences in growth or biomass.
At wk 7 in the drought treatment, pd and md of both species were more negative (Q. laceyi = –6.6 MPa and Q. sideroxyla = –4.5 MPa) than water potentials of seedlings of oak species from other geographical regions including Q. suber (–3.0 MPa) in Spain (Aranda et al., 2005
) and Italy (–1.5 MPa) (Nardini et al., 1999
), Q. robur (–3.0 MPa) and Q. petraea (–3.2 MPa) in Germany (Thomas and Gausling, 2000
), Q. rubra (–2.5 MPa) in the northeastern United States (Kubiske and Abrams, 1992
; Cavendar-Bares, 2000
), and several other oak species of the southwestern United States (Q. buckleyi, Q. lobata, Q. macrocarpa, Q. muehlenbergii, and Q. shumardii) (Balok and St. Hilaire, 2002
).
Week 7 pd and md compare more closely to other oaks, pinyon pines, and junipers from other arid regions of the Southwest, and oaks such as Q. gambelii and Q. turbinella appear to tolerate even lower md (–7.3 MPa and –7.0 MPa, respectively) upon exposure to a similar 7-wk drought than did the seedlings in our study (Neilson and Wullstein, 1987
). This suggests that oak trees from the southwestern United States and northern Mexico are more drought tolerant than oaks from other geographical regions, but that there is a lower limit of 
–7.0 MPa for oak water stress tolerance.
Photosynthesis
The decreases in pd and md in wk 6 and 7 of the drought induced stomatal closure, which decreased the supply of CO2 to the mesophyll cells, and consequently, decreased the rate of leaf photosynthesis. Increases in internal water deficit are associated with disruption of biosynthetic activities, including the generation of the chlorophyll necessary for photosynthesis (Fitter and Hay, 2002
), and photophosphorylation and photosynthetic carbon metabolism may be particularly sensitive to dehydration because of the toxic effects of Mg2+ concentrations that accompany the removal of water from chloroplasts in dehydrating leaves (Kozlowski and Pallardy, 1997
).
The higher photosynthetic rates of Q. sideroxyla relative to Q. laceyi also correspond to their elevational distributions. Adiabatic lapse rates and increases in relative humidity with increasing elevation can ameliorate climates in xeric environments (Barry, 1992
; Robinson et al., 1999
; Whiteman, 2000
), providing more favorable growing conditions for plants at higher elevations. The pattern of increased photosynthesis with increasing elevation in our study is the reverse of the patterns observed in other alpine environments near upper treeline (Tranquillini, 1979
). In the Southwest, the harshest sites are at low elevations, where lower treelines are limited by moisture and temperature (VanDevender, 1995
). Lower temperatures and higher relative humidity at high elevations can therefore explain the pattern of high photosynthesis by Q. sideroxyla relative to Q. laceyi, and the lower maximal photosynthesis of Q. laceyi is likewise explained by its distribution in a more water-limited environment that demands lower maximum metabolic rates.
Chlorophyll fluorescence
The reduction in Fv/Fm during the drought reflects a decline in the efficiency of light use for electron transport by PSII. Under drought conditions, the decreases in photosynthesis are accompanied by a decrease in the rate of consumption of ATP and NADPH for CO2 assimilation, which can reduce the rate of linear electron transport from the quinone acceptors of PSII, and consequently, in Fv/Fm (Baker and Rosenqvist, 2004
). The decline in Fv/Fm of Q. sideroxyla in wk 6 of the drought and a similar decline by Q. laceyi in wk 7, support our findings from the water relations data that low elevation Q. laceyi is more drought tolerant than high elevation Q. sideroxyla. These data suggest that Q. laceyi can better compensate for decreases in the use of ATP and NADPH in photosynthesis metabolism resulting from drought.
Spectral reflectance
Leaf optical properties are well correlated with vegetation water content (Sims and Gamon, 2003
) and leaf pigment content (Curran, 1989
; Gamon and Surfus, 1999
; Sims and Gamon, 2002
), and reflectance is known to shift in response to environmental stress (Peñuelas et al., 1994
; Rock et al., 1998; Carter and Knapp, 2001
; Thorhaug et al., 2006
). The higher reflectance spectrum of Q. sideroxyla, along with the higher chlNDI index and reflectance ratios of control seedlings, suggest that Q. sideroxyla has a higher concentration of plant pigments than Q. laceyi, which relates to its higher maximum photosynthetic capacity.
Changes in the reflectance properties of drought-stressed seedlings are the product of decreases in plant water balance and photosynthetic pigment concentrations. The drop in WBI in latter weeks of the drought indicated decreased plant RWC (Peñuelas et al., 1997; Sims and Gamon, 2003
). Decreases in chlNDI, increases in SIPI, the shift of the REP to shorter wavelengths, and the increases in reflectance observed over a broader portion of the visible spectrum are typical plant responses to stress (Peñuelas et al., 1994
; Carter and Knapp, 2001
; Richardson et al., 2001
; Richardson and Berlyn, 2002
; Thorhaug et al. 2006
), although the position of the red edge was high compared to other studies (i.e., Richardson et al., 2001
; Richardson and Berlyn, 2002
). Furthermore, the reflectance ratios between species in the drought and control reflectance spectra had noticeable peaks in the 680 nm region, suggesting a greater shutdown of PSII in Q. sideroxyla than in Q. laceyi during wk 6 and 7.
While photosynthetic rates tended to increase with oak elevational distribution, the reflectance spectra and reflectance ratios show an opposite trend, with lowland Q. laceyi having higher reflectance than upland Q. sideroxyla. This pattern is consistent with work in mountains of the northeastern United States (Richardson et al., 2001
; Richardson and Berlyn, 2002
), and the observed differences in spectral reflectance also probably relate to variation in the two species' growing conditions. The reflectance data suggest that the light green leaves of Q. laceyi have lower chlorophyll concentrations, which correspond both to its lower photosynthetic rate and its distribution on hot, dry, low-elevation sites. In contrast, the lower reflectance spectrum of Q. sideroxyla corresponds to higher chlorophyll absorption and higher photosynthetic capacity, most likely related to its distribution on cooler, wetter, high-elevation sites.
Application of greenhouse results to field conditions
The application of greenhouse experiments to field conditions warrants discussion (e.g., Harper, 1977
), because the field environment can differ dramatically from controlled greenhouse conditions. We addressed this by mimicking natural patterns of oak germination, growth, and drought timing in the southwestern United States and northern Mexico.
Results from this study correspond to other field-based studies of plant water potential in the southwestern United States (i.e., Lajtha and Barnes, 1991
; Lajtha and Getz, 1993
; Linton et al., 1998
), suggesting that our experiment approximated field soil moisture conditions. Seedling survival over the course of the acute drought was similar to other acute drought studies (Neilson and Wullstein, 1987
; Lajtha and Barnes, 1991
; Barton and Teeri, 1993; Lajtha and Getz, 1993
; Linton et al., 1998
; Balok and St. Hilaire, 2002
). Although pots are known to constrain root elongation and subsequent water uptake, roots of the seedlings in this study failed to reach the bottom of their pots during the experiment.
Conclusions
Results from this study demonstrate the physiological mechanisms responsible for the observed elevational separation and niche partitioning of Q. sideroxyla and Q. laceyi in the Sierra del Carmen, Coahuila, Mexico. Quercus laceyi is a drought tolerant species that can grow under the high water stress conditions typically observed at low elevations during summer months in northern Mexico, while Q. sideroxyla is a drought avoider species that grows poorly under extreme water stress and is therefore restricted to higher elevations with lower temperatures and higher relative humidity. However, both species are adapted to dry conditions, suggesting that they can survive under a range of climate scenarios. The differentiation of these two oaks according to elevation suggests that similar mechanisms may be responsible for the diversification of the genus Quercus across Mexico and the rest of North America. Future studies that investigate the niche partitioning of oaks across other mountain ranges in Mexico are warranted to explain the high diversity of this genus across Mexico.
FOOTNOTES
1 The authors thank S. Arsenault for field assistance, R. Barnes for logistical support, and P. Marshall, J. Karanian, and N. Reagle for help with seedling watering. They also thank Dr. A. Barton, Dr. M. Ashton, Dr. A. Camp, and two anonymous reviewers for comments on earlier drafts of this manuscript. Funding for this research was provided by the Joint Fire Sciences Program of the Department of the Interior (#03-3-3-13). 
2 Author for correspondence (helen.mills{at}yale.edu
; phone: 860-426-0266, fax: 203-432-3929
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