Mary Anne McGuire

Responses of tree species to heat waves and extreme heat events

The number and intensity of heat waves has increased, and this trend is likely to continue throughout the 21st century. Often, heat waves are accompanied by drought conditions. It is projected that the global land area experiencing heat waves will double by 2020, and quadruple by 2040. Extreme heat events can impact a wide variety of tree functions. At the leaf level, photosynthesis is reduced, photooxidative stress increases, leaves abscise and the growth rate of remaining leaves decreases. In some species, stomatal conductance increases at high temperatures, which may be a mechanism for leaf cooling. At the whole plant level, heat stress can decrease growth and shift biomass allocation. When drought stress accompanies heat waves, the negative effects of heat stress are exacerbated and can lead to tree mortality. However, some species exhibit remarkable tolerance to thermal stress. Responses include changes that minimize stress on photosynthesis and reductions in dark respiration. Although there have been few studies to date, there is evidence of within-species genetic variation in thermal tolerance, which could be important to exploit in production forestry systems. Understanding the mechanisms of differing tree responses to extreme temperature events may be critically important for understanding how tree species will be affected by climate change.

Transport of root‐respired CO2 via the transpiration stream affects aboveground carbon assimilation and CO2 efflux in trees

Upward transport of CO₂ via the transpiration stream from belowground to aboveground tissues occurs in tree stems. Despite potentially important implications for our understanding of plant physiology, the fate of internally transported CO₂ derived from autotrophic respiratory processes remains unclear. We infused a ¹³CO₂-labeled aqueous solution into the base of 7-yr-old field-grown eastern cottonwood (Populus deltoides) trees to investigate the effect of xylem-transported CO₂ derived from the root system on aboveground carbon assimilation and CO₂ efflux. The ¹³C label was transported internally and detected throughout the tree. Up to 17% of the infused label was assimilated, while the remainder diffused to the atmosphere via stem and branch efflux. The largest amount of assimilated ¹³C was found in branch woody tissues, while only a small quantity was assimilated in the foliage. Petioles were more highly enriched in ¹³C than other leaf tissues. Our results confirm a recycling pathway for respired CO₂ and indicate that internal transport of CO₂ from the root system may confound the interpretation of efflux-based estimates of woody tissue respiration and patterns of carbohydrate allocation.

Stem respiration and carbon dioxide efflux of young Populus deltoides trees in relation to temperature and xylem carbon dioxide concentration

Oxidative respiration is strongly temperature driven. However, in woody stems, efflux of CO2 to the atmosphere (EA), commonly used to estimate the rate of respiration (RS), and stem temperature (Tst) have often been poorly correlated, which we hypothesized was due to transport of respired CO2 in xylem sap, especially under high rates of sap flow (fs). To test this, we measured EA, Tst, fs and xylem sap CO2 concentrations ([CO2*]) in 3-year-old Populus deltoides trees under different weather conditions (sunny and rainy days) in autumn. We also calculated RS by mass balance as the sum of both outward and internal CO2 fluxes and hypothesized that RS would correlate better with Tst than EA. We found that EA sometimes correlated well with Tst, but not on sunny mornings and afternoons or on rainy days. When the temperature effect on EA was accounted for, a clear positive relationship between EA and xylem [CO2*] was found. [CO2*] varied diurnally and increased substantially at night and during periods of rain. Changes in [CO2*] were related to changes in fs but not Tst. We conclude that changes in both respiration and internal CO2 transport altered EA. The dominant component flux of RS was EA. However, on a 24-h basis, the internal transport flux represented 9–18% and 3–7% of RS on sunny and rainy days, respectively, indicating that the contribution of stem respiration to forest C balance may be larger than previously estimated based on EA measurements. Unexpectedly, the relationship between RS and Tst was sometimes weak in two of the three trees. We conclude that in addition to temperature, other factors such as water deficits or substrate availability exert control on the rate of stem respiration so that simple temperature functions are not sufficient to predict stem respiration.

CO2 transported in xylem sap affects CO2 efflux from Liquidambar styraciflua and Platanus occidentalis stems, and contributes to observed wound respiration phenomena

The [CO2] in the xylem of tree stems is typically two to three orders of magnitude greater than atmospheric [CO2]. In this study, xylem [CO2] was experimentally manipulated in saplings of sycamore (Platanus occidentalis L.) and sweetgum (Liquidambar styraciflua L.) by allowing shoots severed from their root systems to absorb water containing [CO2] ranging from 0.04% to 14%. The effect of xylem [CO2] on CO2 efflux to the atmosphere from uninjured and mechanically injured, i.e., wounded, stems was examined. In both wounded and unwounded stems, and in both species, CO2 efflux was directly proportional to xylem [CO2], and increased 5-fold across the range of xylem [CO2] produced by the [CO2] treatment. Xylem [CO2] explained 76–77% of the variation in pre-wound efflux. After wounding, CO2 efflux increased substantially but remained directly proportional to internal stem [CO2]. These experiments substantiated our previous finding that stem CO2 efflux was directly related to internal xylem [CO2] and expanded our observations to two new species. We conclude that CO2 transported in the xylem may confound measurements of respiration based on CO2 efflux to the atmosphere. This study also provided evidence that the rapid increase in CO2 efflux observed after tissues are excised or injured is likely the result of the rapid diffusion of CO2 from the xylem, rather than an actual increase in the rate of respiration of wounded tissues.

Resistance to radial CO2 diffusion contributes to between-tree variation in CO2 efflux of Populus deltoides stems

Rates of CO2 efflux of stems and branches are highly variable among and within trees and across stands. Scaling factors have only partially succeeded in accounting for the observed variations. In this study, the resistance to radial CO2 diffusion was quantified for tree stems of an eastern cottonwood (Populus deltoides Bartr. ex Marsh.) clone by direct manipulation of the CO2 concentration ([CO2]) of xylem sap under controlled conditions. Tree-specific linear relationships between rates of stem CO2 efflux (JO) and xylem [CO2] were found. The resistance to radial CO2 diffusion differed 6-fold among the trees and influenced the balance between the amount of CO2 retained in the xylem v. that which diffused to the atmosphere. Therefore, we hypothesised that variability in the resistance to radial CO2 diffusion might be an overlooked cause for the inconsistencies and large variations in woody tissue CO2 efflux. It was found that transition from light to dark conditions caused a rapid increase in JO and xylem [CO2], both in manipulated trees and in an intact tree with no sap manipulation. This resulted in an increased resistance to radial CO2 diffusion during the dark, at least for trees with smaller daytime resistances. Stem diameter changes measured in the intact tree supported the idea that higher actual respiration rates occurred at night owing to higher metabolism in relation to an improved water status and higher turgor pressure.

Higher growth temperatures decreased net carbon assimilation and biomass accumulation of northern red oak seedlings near the southern limit of the species range

If an increase in temperature will limit the growth of a species, it will be in the warmest portion of the species distribution. Therefore, in this study we examined the effects of elevated temperature on net carbon assimilation and biomass production of northern red oak (Quercus rubra L.) seedlings grown near the southern limit of the species distribution. Seedlings were grown in chambers in elevated CO(2) (700 µmol mol(-1)) at three temperature conditions, ambient (tracking diurnal and seasonal variation in outdoor temperature), ambient +3 °C and ambient +6 °C, which produced mean growing season temperatures of 23, 26 and 29 °C, respectively. A group of seedlings was also grown in ambient [CO(2)] and ambient temperature as a check of the growth response to elevated [CO(2)]. Net photosynthesis and leaf respiration, photosynthetic capacity (V(cmax), J(max) and triose phosphate utilization (TPU)) and chlorophyll fluorescence, as well as seedling height, diameter and biomass, were measured during one growing season. Higher growth temperatures reduced net photosynthesis, increased respiration and reduced height, diameter and biomass production. Maximum net photosynthesis at saturating [CO(2)] and maximum rate of electron transport (J(max)) were lowest throughout the growing season in seedlings grown in the highest temperature regime. These parameters were also lower in June, but not in July or September, in seedlings grown at +3 °C above ambient, compared with those grown in ambient temperature, indicating no impairment of photosynthetic capacity with a moderate increase in air temperature. An unusual and potentially important observation was that foliar respiration did not acclimate to growth temperature, resulting in substantially higher leaf respiration at the higher growth temperatures. Lower net carbon assimilation was correlated with lower growth at higher temperatures. Total biomass at the end of the growing season decreased in direct proportion to the increase in growth temperature, declining by 6% per 1 °C increase in mean growing season temperature. Our observations suggest that increases in air temperature above current ambient conditions will be detrimental to Q. rubra seedlings growing near the southern limit of the species range.

Assimilation of xylem-transported 13C-labelled CO2 in leaves and branches of sycamore (Platanus occidentalis L.)

Previous reports have shown that CO2 dissolved in xylem sap in tree stems can move upward in the transpiration stream. To determine the fate of this dissolved CO2, the internal transport of respired CO2 at high concentration from the bole of the tree was simulated by allowing detached young branches of sycamore (Platanus occidentalis L.) to transpire water enriched with a known quantity of 13CO2 in sunlight. Simultaneously, leaf net photosynthesis and CO2 efflux from woody tissue were measured. Branch and leaf tissues were subsequently analysed for 13C content to determine the quantity of transported 13CO2 label that was fixed. Treatment branches assimilated an average of 35% (SE=2.4) of the 13CO2 label taken up in the treatment water. The majority was fixed in the woody tissue of the branches, with smaller amounts fixed in the leaves and petioles. Overall, the fixation of internally transported 13CO2 label by woody tissues averaged 6% of the assimilation of CO2 from the atmosphere by the leaves. Woody tissue assimilation rates calculated from measurements of 13C differed from rates calculated from measurements of CO2 efflux in the lower branch but not in the upper branch. The results of this study showed unequivocally that CO2 transported in xylem sap can be fixed in photosynthetic cells in the leaves and branches of sycamore trees and provided evidence that recycling of xylem-transported CO2 may be an important means by which trees reduce the carbon cost of respiration.

CO2 efflux, CO2 concentration and photosynthetic refixation in stems of Eucalyptus globulus (Labill.)

In spite of the importance of respiration in forest carbon budgets, the mechanisms by which physiological factors control stem respiration are unclear. An experiment was set up in a Eucalyptus globulus plantation in central Portugal with monoculture stands of 5-year-old and 10-year-old trees. CO(2) efflux from stems under shaded and unshaded conditions, as well as the concentration of CO(2) dissolved in sap [CO(2)(*)], stem temperature, and sap flow were measured with the objective of improving our understanding of the factors controlling CO(2) release from stems of E. globulus. CO(2) efflux was consistently higher in 5-year-old, compared with 10-year-old, stems, averaging 3.4 versus 1.3 mumol m(-2) s(-1), respectively. Temperature and [CO(2)(*)] both had important, and similar, influences on the rate of CO(2) efflux from the stems, but neither explained the difference in the magnitude of CO(2) efflux between trees of different age and size. No relationship was found between efflux and sap flow, and efflux was independent of tree volume, suggesting the presence of substantial barriers to the diffusion of CO(2) from the xylem to the atmosphere in this species. The rate of corticular photosynthesis was the same in trees of both ages and only reduced CO(2) efflux by 7%, probably due to the low irradiance at the stem surface below the canopy. The younger trees were growing at a much faster rate than the older trees. The difference between CO(2) efflux from the younger and older stems appears to have resulted from a difference in growth respiration rather than a difference in the rate of diffusion of xylem-transported CO(2).

Effects of predicted future and current atmospheric temperature and [CO2] and high and low soil moisture on gas exchange and growth of Pinus taeda seedlings at cool and warm sites in the species range

Predicted future changes in air temperature and atmospheric CO(2) concentration ([CO(2)]), coupled with altered precipitation, are expected to substantially affect tree growth. Effects on growth may vary considerably across a species range, as temperatures vary from sub-optimal to supra-optimal for growth. We performed an experiment simultaneously at two locations in the current range of loblolly pine, a cool site and a warm site, to examine the effect of future climate conditions on growth of loblolly pine seedlings in contrasting regions of the species range. At both sites 1-year-old loblolly pine seedlings were grown in current (local ambient temperature and [CO(2)]) and predicted future atmospheric conditions (ambient +2 °C temperature and 700 μmol mol(-1) [CO(2)]). Additionally, high and low soil moisture treatments were applied within each atmospheric treatment at each site by altering the amount of water provided to the seedlings. Averaged across water treatments, photosynthesis (A(net)) was 31% greater at the cool site and 34% greater at the warm site in elevated temperature and [CO(2)] compared with ambient temperature. Biomass accumulation was also stimulated by 38% at the cool site and by 24% at the warm site in that treatment. These results suggest that a temperature increase of 2 °C coupled with an increase in [CO(2)] (predicted future climate) will create conditions favorable for growth of this species. Reduced soil moisture decreased growth in both current and predicted atmospheric conditions. Biomass accumulation and A(net) were reduced by ∼39 and 17%, respectively, in the low water treatment. These results suggest that any benefit of future atmospheric conditions may be negated if soil moisture is reduced by altered precipitation patterns.

Stem girdling affects the quantity of CO2 transported in xylem as well as CO2 efflux from soil

There is recent clear evidence that an important fraction of root-respired CO2 is transported upward in the transpiration stream in tree stems rather than fluxing to the soil. In this study, we aimed to quantify the contribution of root-respired CO2 to both soil CO2 efflux and xylem CO2 transport by manipulating the autotrophic component of belowground respiration. We compared soil CO2 efflux and the flux of root-respired CO2 transported in the transpiration stream in girdled and nongirdled 9-yr-old oak trees (Quercus robur) to assess the impact of a change in the autotrophic component of belowground respiration on both CO2 fluxes. Stem girdling decreased xylem CO2 concentration, indicating that belowground respiration contributes to the aboveground transport of internal CO2 . Girdling also decreased soil CO2 efflux. These results confirmed that root respiration contributes to xylem CO2 transport and that failure to account for this flux results in inaccurate estimates of belowground respiration when efflux-based methods are used. This research adds to the growing body of evidence that efflux-based measurements of belowground respiration underestimate autotrophic contributions.