Growth overcompensation against O₃ exposure in two Japanese oak species, Quercus mongolica var. crispula and Quercus serrata, grown under elevated CO₂

Highlights

• Quercus mongolica var. crispula and Quercus serrata were grown under elevated CO₂ and O₃.

• O₃ induced a preferable biomass allocation into leaves.

• Photosynthesis was predominantly enhanced under elevated CO₂ exceeding O₃ impacts.

• Combination of elevated CO₂ and O₃ enhanced the growth of two oak species.

Abstract

To assess the effects of elevated concentrations of carbon dioxide (CO₂) and ozone (O₃) on the growth of two mid-successional oak species native to East Asia, Quercus mongolica var. crispula and Quercus serrata, we measured gas exchange and biomass allocation in seedlings (initially 1-year-old) grown under combinations of elevated CO₂ (550 μmol mol⁻¹) and O₃ (twice-ambient) for two growing seasons in an open-field experiment in which root growth was not limited. Both the oak species showed a significant growth enhancement under the combination of elevated CO₂ and O₃ (indicated by total dry mass; over twice of ambient-grown plants, p < .05), which probably resulted from a preferable biomass partitioning into leaves induced by O₃ and a predominant enhancement of photosynthesis under elevated CO₂. Such an over-compensative response in the two Japanese oak species resulted in greater plant growth under the combination of elevated CO₂ and O₃ than elevated CO₂ alone.

Introduction

Tropospheric ozone (O₃) levels have increased globally since preindustrial times (Stockwell et al., 1997, IPCC., 2001, IPCC., 2007) and continue to rise, particularly in the region of East Asia (Fowler et al., 1999, Fowler et al., 2008, Vingarzan, 2004, Ashmore, 2005, Dentener et al., 2006). Increased O₃ levels have the potential of limiting the carbon sink strength of forest ecosystems (IPCC., 2007, Sitch et al., 2007, Wittig et al., 2009, Pretzsch et al., 2010) because of reduced net photosynthesis, accelerated leaf senescence, and increased dark respiration (for review see Matyssek and Sandermann, 2003, Matyssek et al., 2010). Atmospheric carbon dioxide (CO₂) concentration is predicted to double during the next century (IPCC., 2001, IPCC., 2007). Elevated CO₂ has been linked to increased plant growth via enhanced photosynthetic carbon assimilation (Tissue et al., 1997, Ainsworth and Long, 2005, Norby and Zak, 2011), although long-term exposure to elevated CO₂ results in photosynthetic downregulation, typically a decrease in the carboxylation capacity of Rubisco (V_c,max) (Rogers and Ellsworth, 2002, Ainsworth and Long, 2005, Bernacchi et al., 2005).

Quercus mongolica var. crispula (Japanese oak) and Quercus serrata (konara oak) are representative deciduous broadleaf tree species found in Japan and throughout East Asia (Menitsky, 2005). The former is mainly distributed in the cool-temperate and the latter in the warm-temperate zone of deciduous broadleaf forests in East Asia. Both species have a high sprouting ability with well-developed tap roots as they are commonly used for coppicing in secondary forests in Japan (Sakai et al., 1997, Sakai and Sakai, 1998). Both have mid-successional traits, i.e., moderately shade-tolerant and need a gap formation for regeneration (Higo, 1994). Their shoot development pattern is categorized as a flush and succeeding-type leaf emergence (Kikuzawa, 1983); they flush shoots generally once in spring, sometimes flushing new shoots if environmental conditions are preferable, such as gap formation. According to Yamaguchi et al. (2011), both the oak species are relatively O₃ tolerant among the Japanese tree species and are related to a noted capacity for isoprene emission (Loreto and Fares, 2007, Tani and Kawawata, 2008, Miyama et al., 2013). Although there have been several studies primarily investigating the effects of elevated CO₂ and/or O₃ on leaf physiological and morphological traits in oak species (e.g., Velikova et al., 2005, Paoletti et al., 2007, Watanabe et al., 2007, Watanabe et al., 2013), only a few studies have investigated the combined effects of elevated CO₂ and O₃ on the growth and carbon allocation in oak species (Quercus petraea, Broadmeadow and Jackson, 2000; cf. King et al., 2013). A thorough assessment of the effects of elevated O₃ and CO₂ on the growth of these oak species (Q. mongolica and Q. serrata) is necessary to predict the effects of global change on the carbon sequestering capacity of forest ecosystems, particularly in East Asia.

Plant growth is mainly regulated by two factors: leaf area-based carbon assimilation rate and leaf area ratio (Poorter, 1989). The former is involved in photosynthetic capacity and the latter in photosynthate allocation. O₃ exposure is known to shift carbon allocation preferably into shoots (Pell et al., 1994, Selldén et al., 1997, Landolt et al., 2000, Oksanen and Rousi, 2001), which may promote plant growth in response to the O₃-induced reduction in photosynthesis (Mooney et al., 1988, Pell et al., 1994, Yamaji et al., 2003). Conversely, carbon allocation in plants grown under elevated CO₂ is reported to be relatively unresponsive when compared with that in plants under the effects of O₃, which are dependent on species, resource supply, and environmental factors (Rogers et al., 1996, Poorter and Nagel, 2000). In previous studies, the root to shoot ratio of Japanese white birch seedlings was considerably changed according to water and nitrogen availability, whereas no significant response was triggered by elevated CO₂ (Kitao et al., 2005, Kitao et al., 2007).

Elevated CO₂ concentration may alleviate the toxicological impacts of elevated O₃ if elevated CO₂ level is accompanied by lower stomatal conductance (Ainsworth and Long, 2005, Ainsworth and Rogers, 2007) or by a greater quantity of carbohydrates available for detoxification and repair in elevated CO₂ (Riikonen et al., 2004, Riikonen et al., 2005). If greater carbon allocation into shoots directly induced by O₃ occurs as a defense mechanism (Kangasjärvi et al., 1994, Pell et al., 1994), the impact of O₃ is alleviated and photosynthesis is enhanced under elevated CO₂, particularly in the Quercus species that are generally less sensitive to the damaging effects of O₃; this may ultimately increase plant growth as an overcompensation.

We hypothesized that the growth of the two O₃-tolerant oak species (Q. mongolica var. crispula and Q. serrata) native to East Asia with a plastic shoot developmental pattern (Kikuzawa, 1983) was enhanced when grown under elevated O₃ and CO₂ through an O₃-induced carbon allocation into shoots and CO₂-enhanced photosynthesis exceeding O₃ impacts. Furthermore, as a greater cumulative O₃ uptake via higher stomatal conductance was observed in Q. mongolica than in Q. serrata (Kinose et al., 2014), O₃ impact on photosynthesis would be greater in the former species leading to a less enhancement in the growth. To test this hypothesis, we investigated the growth and photosynthetic responses in the seedlings of Q. mongolica and Q. serrata grown under free-air fumigation of elevated O₃ and CO₂.