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Stomatal CO2 Responsiveness and Photosynthetic Capacity of Tropical Woody Species in Relation to Taxonomy and Functional Traits

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Stomatal CO2 Responsiveness and Photosynthetic Capacity of Tropical Woody Species in Relation to Taxonomy and Functional Traits Oecologia DOI 10.1007/s00442-017-3829-0 PHYSIOLOGICAL ECOLOGY - ORIGINAL RESEARCH Stomatal CO2 responsiveness and photosynthetic capacity of tropical woody species in relation to taxonomy and functional traits Thomas B. Hasper1 · Mirindi E. Dusenge1,2 · Friederike Breuer1 · Félicien K. Uwizeye2 · Göran Wallin1 · Johan Uddling1 Received: 27 November 2015 / Accepted: 22 January 2017 © The Author(s) 2017. This article is published with open access at Springerlink.com Abstract Stomatal CO2 responsiveness and photosynthetic rather than to area-based total leaf N content. Within-leaf capacity vary greatly among plant species, but the factors N allocation and water use were strongly co-ordinated controlling these physiological leaf traits are often poorly (r2 0.67), such that species with high fractional N invest- = understood. To explore if these traits are linked to taxo- ments into compounds maximizing photosynthetic capac- nomic group identity and/or to other plant functional traits, ity also had high stomatal conductance. We conclude that we investigated the short-term stomatal CO2 responses and while stomatal CO2 responsiveness of tropical woody spe- the maximum rates of photosynthetic carboxylation (Vcmax) cies seems poorly related to other plant functional traits, and electron transport (Jmax) in an evolutionary broad photosynthetic capacity is linked to fractional within-leaf N range of tropical woody plant species. The study included allocation rather than total leaf N content and is closely co- 21 species representing four major seed plant taxa: gym- ordinated with leaf water use. nosperms, monocots, rosids and asterids. We found that stomatal closure responses to increased CO2 were stronger Keywords Carbon dioxide · Transpiration · Leaf traits · in angiosperms than in gymnosperms, and in monocots Stomatal patterning · Tropical trees compared to dicots. Stomatal CO2 responsiveness was not significantly related to any of the other functional traits investigated, while a parameter describing the relation- Introduction ship between photosynthesis and stomatal conductance in combined leaf gas exchange models (g1) was related to Anthropogenic fossil fuel burning and land use change leaf area-specific plant hydraulic conductance. For photo- have increased the atmospheric carbon dioxide concentra- synthesis, we found that the interspecific variation in Vcmax tion [CO2] by over 40% (Ciais et al. 2013), with today’s 1 and Jmax was related to within leaf nitrogen (N) allocation concentration of over 400 μmol mol− being the highest in approximately 40 millions years (Frank et al. 2015). This large and rapid ongoing increase in [CO2] has profound Communicated by Bettina Engelbrecht. impacts on land plants, which typically respond to altered [CO2] by increasing leaf photosynthesis (A) and decreas- Electronic supplementary material The online version of this ing stomatal conductance (gs; Ainsworth and Rogers 2007). article (doi:10.1007/s00442-017-3829-0) contains supplementary However, the direct stomatal responses to a short-term material, which is available to authorized users. increase in [CO2] vary greatly among species and experi- * Johan Uddling ments, from no change to 75% reduction in gs at doubled [email protected] compared to ambient [CO2] (Morison 1998). Understand- ing this variation is important, since the short-term stoma- 1 Department of Biological and Environmental Sciences, University of Gothenburg, PO Box 461, 405 30 Gothenburg, tal CO2 response appears to be an important determinant Sweden for the long-term effect of growth in elevated [CO2] on gs 2 Department of Biology, University of Rwanda, University under field conditions. In so called free-air CO2 enrichment Avenue, PO Box 56, Huye, Rwanda (FACE) experiments with trees, the interspecific variation 1 3 Oecologia in long-term (years) effects of growth under elevated [CO2] Short-term gs responses to [CO2] (%) on gs was significantly and positively related to the varia- -12-10 -8 -6 -4 -2 tion in short-term stomatal CO2 responsiveness, measured Betula as the effect of short (hours) interruptions in CO enrich- papyrifera 2 0 ment on sap flow (Cech et al. 2003; Keel et al. 2007; Tor- Fagus ngern et al. 2015) or leaf gs (Maier et al. 2008; Domec et al. ) -5 Quercus sylvatica 2009; Onandia et al. 2011) in some of these experiments petraea ] (% responses 2 2 s Pinus g -10 (Fig. 1; r 0.81; P 0.014). Tree species that exhibit O Tilia platyphyllos = = taeda a pronounced direct stomatal closure response to a short- Acer campestre to [C -15 Prunus avium term increase in [CO2] are thus also likely to develop a long-term gs reduction in the field. Therefore, a better y = 2.02x + 2.52 Long-term 2 understanding of the factors that control the large natural -20 Carpinus r = 0.81 betulus P = 0.014 variation in short-term stomatal CO2 responses would pro- vide indication of which plant species and groups that are likely to experience large increases in water-use efficiency Fig. 1 Relationship between the short-term response of gs to elevated in future higher [CO ] scenarios. [CO2] [measured during short (hours) interruptions in CO2 enrich- 2 ment] and the long-term effect of growth under elevated [CO ] on Both the short-term stomatal CO response and the long- 2 2 gs in temperate forest free-air CO2 enrichment (FACE) experiments. term effect of growth under elevated [CO2] on gs have been Regression statistics are shown in the figure. Based on data from found to be weaker in gymnosperms compared to angio- Cech et al. (2003), Keel et al. (2007), Maier et al. (2008), Domec sperms (Medlyn et al. 2001; Brodribb et al. 2009). Brodribb et al. (2009), Onandia et al. (2011) and Tor-ngern et al. (2015) et al. (2009) even suggested that gymnosperms lack a pri- mary stomatal CO2 response, while others have found that types and in different biomes (Lin et al. 2015). In angio- this is not the case (Haworth et al. 2013). To our knowl- sperm trees, it was found that g1 was positively related to edge, there has been no study designed to explore possi- wood density, reflecting a higher cost of wood construction ble taxonomic patterns in the large interspecific variation in per unit water transported in species with higher wood den- stomatal CO2 responsiveness among different angiosperm sity (Lin et al. 2015). However, the relationship with wood taxa. Furthermore, possible functional determinants of the density was quite weak (r2 0.21; Lin et al. 2015) and = interspecific variation in stomatal CO2 responsiveness have when gymnosperms were included it was not significant also been poorly explored. If stomatal CO2 responses are at all. There is thus a need to further explore the relation- linked to physiological, chemical or structural plant traits ship of g1 with wood density and other plant traits, such as for which more knowledge is available, this could facili- hydraulic conductance. Hydraulic conductance and gs are tate future trait-based modelling of plant water-use under often co-ordinated in trees (Brodribb and Jordan 2008) and rising [CO2] (Van Bodegom et al. 2012). For example, it since high hydraulic conductance essentially reduces the is possible that (but unknown if) stomatal CO2 responsive- carbon cost of water use (Prentice et al. 2014) it is plausible ness is linked to stomatal density since, in general, plants that (but unexplored if) g1 is positively related to hydraulic with high stomatal density have more efficient stomatal conductance. With respect to taxonomic patterns, there are regulation (Franks et al. 2009). It is also plausible that sto- typically distinct differences in water-use strategy between matal CO2 responsiveness is linked to hydraulic traits since angiosperm and gymnosperm trees, with angiosperms typi- plants with high hydraulic conductance often exhibit tight cally exhibiting higher gs, hydraulic conductance and g1 at stomatal control over transpiration to avoid severe cavita- the expense of considerably smaller hydraulic safety mar- tion (Bond and Kavanagh 1999). Since stomatal regulation gin compared to gymnosperms (Choat et al. 2012; Lin et al. is an energy consuming process, CO2 sensitivity may also 2015). be linked to indicators of leaf metabolic activity, such as There is also considerable uncertainty with respect to the photosynthetic capacity. variation in the maximum rates of photosynthetic carboxy- Most land-surface and ecosystem models apply com- lation (Vcmax) and electron transport (Jmax) among plant spe- bined stomatal–photosynthesis models (Ball et al. 1987; cies in general (Ali et al. 2015) and tropical tree species in Leuning 1995; Medlyn et al. 2011), in which plant car- particular (Dusenge et al. 2015). Current vegetation models bon and water vapor fluxes are linked as they both pass typically base their values of Vcmax and Jmax on area-based through plant stomata. The empirical slope parameter of total leaf N content (e.g., Zaehle et al. 2005; Rogers 2014). the combined stomatal–photosynthesis model (g1), which However, a recent global meta-analysis found that Vcmax is inversely proportional to leaf water use efficiency (at and Jmax were more closely related to within-leaf nitrogen constant environmental conditions; Medlyn et al. 2011), (N) allocation than to total leaf N content (Ali et al. 2015), has been determined for a large number of plant functional as also observed in two studies with tropical tree species 1 3 Oecologia (Coste et al. 2005; Dusenge et al. 2015). Part of the reason woody plants of 21 species growing at four
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