Gas exchange at whole plant level shows that a less conservative water use is linked to a higher performance in three ecologically distinct pine species

Abstract

Increasing temperatures and decreasing precipitation in large areas of the planet as a consequence of global warming will affect plant growth and survival. However, the impact of climatic conditions will differ across species depending on their stomatal response to increasing aridity, as this will ultimately affect the balance between carbon assimilation and water loss. In this study, we monitored gas exchange, growth and survival in saplings of three widely distributed European pine species (Pinus halepensis, P. nigra and P. sylvestris) with contrasting distribution and ecological requirements in order to ascertain the relationship between stomatal control and plant performance. The experiment was conducted in a common garden environment resembling rainfall and temperature conditions that two of the three species are expected to encounter in the near future. In addition, gas exchange was monitored both at the leaf and at the whole-plant level using a transient-state closed chamber, which allowed us to model the response of the whole plant to increased air evaporative demand (AED). P. sylvestris was the species with lowest survival and performance. By contrast, P. halepensis showed no mortality, much higher growth (two orders of magnitude), carbon assimilation (ca. 14 fold higher) and stomatal conductance and water transpiration (ca. 4 fold higher) than the other two species. As a consequence, P. halepensis exhibited higher values of water-use efficiency than the rest of the species even at the highest values of AED. Overall, the results strongly support that the weaker stomatal control of P. halepensis, which is linked to lower stem water potential, enabled this species to maximize carbon uptake under drought stress and ultimately outperform the more water conservative P. nigra and P. sylvestris. These results suggest that under a hotter drought scenario P. nigra and P. sylvestris would very likely suffer increased mortality, whereas P. halepensis could maintain gas exchange and avoid water-induced growth limitation. This might ultimately foster an expansion of P. halepensis to higher latitudes and elevations.

The “isohydric trap”: A proposed feedback between water shortage, stomatal regulation, and nutrient acquisition drives differential growth and survival of European pines under climatic dryness

“…According to the dual isotope conceptual model (Grams, Kozovits, Häberle, Matyssek, & Dawson, ; Scheidegger, Saurer, Bahn, & Siegwolf, ), the combination of high δ 18 O and low δ 13 C values in the drought‐sensitive mountain pine species (compared to P. halepensis ) indicates low time‐integrated stomatal conductance and water use efficiency, as well as low photosynthesis rates (Querejeta, Allen, Caravaca, & Roldán, ), which is consistent with the poor growth of these species. This interpretation of isotope data is in strong agreement with gas exchange measurements conducted at whole plant level with transient‐state closed chambers in the same common garden experiment, which showed higher stomatal conductance and transpiration, photosynthetic rates and water use efficiency in P. halepensis than in the other pine species during the dry season (Salazar‐Tortosa et al., ). Furthermore, the potential influence of the use of different water sources among species can be discarded as the lower predawn water potential of P. halepensis compared to other species would be incompatible with the alternative explanation that it was using a more δ 18 O depleted source water stored in deeper, wetter soil layers (Nardini et al., ; Voltas, Lucabaugh, Chambel, & Ferrio, ; West et al., ).…”

“…Second, leaf‐level measurements suggest the existence of large interspecific differences in stomatal sensitivity to low plant water potentials, with P. halepensis showing the lowest water potentials at stomatal closure, followed by P. nigra and P. sylvestris (Martin‐StPaul, Delzon, & Cochard, ). Finally, previous measurements at whole‐plant level in the study site showed that P. halepensis exhibits less tight stomatal control and higher transpiration rates under dry conditions than P. nigra and P. sylvestris (Salazar‐Tortosa et al., ). Therefore, we may assume that the studied species can be ordered along an iso‐anisohydry gradient from P. uncinata (most isohydric), P. sylvestris , P. nigra to P. halepensis (most anisohydric).…”

“…Finally, previous measurements at whole-plant level in the study site showed that P. halepensis exhibits less tight stomatal control and higher transpiration rates under dry conditions than P. nigra and P. sylvestris (Salazar-Tortosa et al, 2018). Therefore, we may assume that the studied species can be ordered along an iso-anisohydry gradient from P. uncinata (most isohydric), P. sylvestris, P. nigra to P. halepensis (most anisohydric).…”

“…Therefore, in a global scenario of climate warming combined with increasing rates of anthropogenic N deposition (Güsewell, ; Jonard et al., ) we should expect plant P status (along with K and micronutrients like Cu or Zn) to be particularly vulnerable to decreases in transpiration fluxes during prolonged periods of climatic dryness, whereas plant N status may be less responsive. In addition, the reduced carbon assimilation exhibited by drought‐sensitive mountain pine species at the common garden site (Salazar‐Tortosa et al., ) could lead to low carbon availability to support the growth and activity of fine roots and ectomycorrhizal (EMF) fungi (Gessler et al., ; Matías et al., ; Moran et al., ). This could hamper even more the assimilation of low mobility nutrients, whose absorption has high energy and carbon costs such as the production of extramatrical EMF mycelium, the secretion of phosphatases and organic acids by roots and mycorrhizae for solubilization and mineralization of inorganic and organic P, or rhizosphere priming effects (Achat, Augusto, Gallet‐Budynek, & Loustau, ; Kreuzwieser & Gessler, ).…”

“…Soil moisture content remained above the permanent wilting point throughout the summer dry period in both years of the experiment (Appendix S1, Table S4), which suggests that high temperature and evaporative demand may have also been key drivers of the contrasting responses observed among pine species (McDowell & Allen, ; McDowell et al., ; Salazar‐Tortosa et al., ; Williams et al., ). In fact, mean summer temperature at the common garden site was considerably higher than that experienced by the mountain pine species in their original habitat ( P. nigra , P. sylvestris , and P. uncinata ).…”