Increased temperature and CO2 levels are not conducive to the photosynthetic activity of S. tabernaemontani. Photosynthetic rate, stomatal density and size, vein density, epidermal structure size, and vascular bundle size play an essential role in the adaptation of this species to changes in temperature and CO2 concentration. In the process of adaptation, hydraulic traits are not isolated from each other, and there is a functional association among traits.
Like terrestrial plants, wetland plants show significant changes in hydraulic traits in different climatic environments, reflecting their response strategies. Earlier studies on the ecological responses of wetland plants on the Southwest Plateau of China have shown that at elevated temperatures, Hippuris vulgaris increased the aboveground stem vascular structure of the ducts, sieves, and vascular bundles, along with the pronounced development of the belowground vascular network of the ducts and sieves to enhance mechanical supportability and water retention ability (Guan et al. 2019). Similarly, Schoenoplectus tabernaemontani significantly reduces its vessel perimeter, area, and cross-sectional surface, the cross-sectional area of the sieve tube, and its net photosynthetic rate but substantially increases the cross-sectional density of the sieve tube to adapt to higher temperatures (Feng et al. 2020a, b). In addition, warming significantly affects the light and CO2 use of dominant plants in the wetland lakeside zone of the Northwest Yunnan Plateau, with different species showing different responses. Zizania latifolia adapts to warming by reducing its photosynthetic CO2 use capacity and net photosynthetic rate (Liu et al. 2017). The species Sparganium stoloniferum adapts to warming by increasing its light saturation point, light energy use range, and net photosynthetic rate (Liu et al. 2017). At high CO2 concentrations, S. tabernaemontani can significantly increase its net photosynthetic rate, intercellular CO2 concentration, water use efficiency, and biomass and reduces stomatal conductance and transpiration rate (Xu et al. 2016). By inhibiting the photosynthetic mechanism of the leaves, Vallisneria natans lowers its photosynthetic capacity to adapt to changing atmospheric CO2 concentrations (Han et al. 2017). These studies reflect the interspecific differences in plateau wetland plants in adapting to increasing temperatures and CO2 concentrations, improving our understanding of the functional responses of plateau wetland plants to a changing climate. However, these studies did not comprehensively consider the transportation, loss, and maintenance of water and substances by plants from the hydraulics perspective and neglected the relationship between corresponding traits and photosynthetic production.
Different plant species show different responses to climate warming. Either on a global scale (Wright et al. 2004) or for individual plant species (Yin et al. 2008; Qi et al. 2012; Wang et al. 2017), most studies have shown that the photosynthetic capacity of most plants increases with increasing temperatures, mainly because the increase in temperature promotes the activity of plant photosynthetic enzymes and accelerate the gas exchange rate of plants, thereby promoting photosynthetic activity. Studies on specific types or individual species of plants have found that the relationship between plant photosynthetic capacity and temperature is not significant (Zhao et al. 2016) and decreases with increasing temperatures (Bresson et al. 2011; Liu et al. 2018) or first increases with temperature and then declines (Vo et al. 2015). This reflects the differences in the responses of different plants to temperature changes and indicates that the photosynthetic capacity is not only affected by temperature but also by other environmental factors. Under different environmental conditions and in various ecosystems, there are various controlling factors. For example, plants in high-elevation areas are strongly affected by temperature, light intensity, CO2 concentration, and microclimatic conditions (Bresson et al. 2011; Sun et al. 2016a, b). Epiphytes are significantly affected by water availability and light conditions (Sun et al. 2014), whereas wetland plants are generally largely affected by temperature, CO2 concentration, water, sediment environment, among others (Zhang et al. 2021). In our study, the photosynthetic and transpiration rates of S. tabernaemontani decreased significantly under increasing temperatures (Fig. 1), reflecting the decline in photosynthetic capacity and productivity. This is consistent with the results of Qi et al. (2012) for Phragmites australis and the in-situ field study by our research team in the Napahai of Shangri-La, Yunnan (Feng et al. 2020a, b), further confirming that against the background of a changing climate, warming is not conducive to photosynthetic production and biomass accumulation of S. tabernaemontani. Our earlier field investigations on the plateau area also found that this species is the dominant aquatic-terrestrial ecotone species in the Napahai area at an elevation of 3266 m and an average temperature of 5.4 °C, with its photosynthetic rate exceeding 30 μmol·m−2·s−1. In contrast, in the Lashihai area at an elevation of 2437 m and an average temperature of 13.6 °C, it is more slender and short and does not dominate the plant community, with a photosynthetic rate only occasionally reaching 20 μmol·m−2·s−1.
Several studies have found that the responses of herbaceous wetland plants to warming are more complex than those of woody plants. Even for plants colonizing the same habitat, small temperature changes can produce significantly different response trends. Liao et al. (2016) and Wang et al. (2019) have shown that between 1985 and 2008, the temperature in the Napahai has increased by 1.2 °C, and the differential responses of dominant plants in the aquatic-terrestrial ecotone can directly affect the wetland type, distribution area, and landscape diversity. An in-situ comparative study on the four plant species S. tabernaemontani, Sparganium emersum, H. vulgaris, and Eleocharis liouana in the Napahai of Shangri-La found that compared with the control group, increased temperatures affect the growth of S. tabernaemontani and H. vulgaris by promoting above-ground stem vascular structure, whereas the development of E. liouana and of the underground stem vascular structure of H. vulgaris was impeded. Also, the biomass of S. emersum first increased and then decreased (Dong et al. 2014; Guan et al. 2018). Plants have a certain tolerance level to changes in temperature. Moderate warming will increase photosynthetic rate, stomatal conductance, transpiration rate, and other parameters that reflect photosynthetic gas exchange capacity, whereas further increases in temperature with impede these processes (Ruan and Li 2001). At present, S. tabernaemontani grows in numerous aquatic-terrestrial ecotones on the Yunnan Plateau. It is the dominant plant species in the aquatic-terrestrial ecotone in Shangri-La, Lugu Lake, Dianchi Lake, and other places, indicating that the current temperature in Yunnan is generally suitable for its growth. However, with the predicted further increase in temperature, S. tabernaemontani may gradually become less competitive in plateau areas due to its inability to adapt to higher temperatures.
The responses of plant morphological and structural parameters to temperature correspond to the photosynthetic capacity. The stomata are the primary channels for plants to control water vapor exchange, and the greater the density and the smaller the size, the higher the sensitivity of stomatal opening and closing, the higher the rate of water vapor exchange, and the higher the water loss (Franks and Beerling 2009). The vascular structure is the center of water and material transportation and distribution and the main structure to maintain the upright state of plants (Sack et al. 2016; Nelson and Dengler 1997). The greater the vein density, the stronger the conveying capacity, enabling the plant to remain upright and stretched. The larger the vascular bundle structures, the more water, nutrients, and organic matter can be transported by a single vascular bundle, but the risk of cavitation of the vascular bundle is also higher (Chen et al. 2017). Therefore, when plants adapt to environmental stress, those with higher vascular bundle density and smaller tissue structure show increased photosynthetic productivity with transmission efficiency (Sack et al. 2016). On the other hand, plants with low vascular bundles density and larger tissue structure are at risk of vascular bundle cavitation, transporting large amounts of substances simultaneously to increase their photosynthetic production. The leaf epidermis and its appendages provide mechanical support and ultraviolet radiation resistance and prevent physical water loss (Ristic and Jenks 2002). The small and tightly arranged epidermal cells can effectively reduce the water loss rate and maintain the moisture levels in plants (Sun et al. 2016a, b). The cuticle can reduce water evaporation and increase refractivity, preventing plants from damages by intense radiation (Dylan et al. 2009). In this study, the increase in temperature significantly improved stomatal sensitivity and water loss capacity of the studied species while also increasing water and material support via higher vein density (Fig. 1). However, the risk of cavitation blockage of the vascular bundle also increased (larger vascular bundle size), and the physical water retention capacity of the epidermis and the ability to protect the plant against UV damage decreased because of the decreased cuticle thickness. Under warming conditions, higher stomatal density and vein density correspond to lower photosynthetic rates (Table 2). This is consistent with our previous research results for other plateau wetland plants. For example, increasing temperature will reduce the light saturation point, net photosynthetic rate, and other photosynthetic characteristics of Zizania latifolia, thereby decreasing the light use ability (Liu et al. 2017). In plateau areas, in addition to transporting water and materials, the vascular structure of wetland plants may also consume a considerable proportion to support the upright stature of plants. This is also related to the fact that wetland plants grow in water and are easily affected by the force of water currents. The significant positive correlation between photosynthetic rate and vascular bundle length (Table 2) indicates that maintaining an upright position of S. tabernaemontani is the prerequisite for photosynthetic production. At the same time, the smaller the vascular bundle reduces the risk of cavitation under increasing temperatures. This directly manifests the decline in the photosynthetic capacity of S. tabernaemontani.
At increasing temperatures, water loss through the stomata and the epidermis is high, and the photosynthetic activity of S. tabernaemontani is considerably more affected by stomatal sensitivity and epidermal water loss (thin cuticle) than by stomatal gas exchange (higher stomatal density). High stomatal water loss and low photosynthetic rate indicate that the water use efficiency of S. tabernaemontani is low. The water use efficiency are also decreased in ET and EC conditions (values of CK, ET, and EC are 9.704, 6.008 and 8.168 μmol·mmol−1 respectively). In addition to photosynthetic gas exchange, a large part of water is used for other purposes, such as physical cooling of leaves and stomatal opening to obtain more CO2. Water loss can be controlled by the physical barriers presented by epidermal structures, such as the cuticle and the epidermis (Kerstiens 1996; Riederer and Schreiber 2001). Greater cuticular thickness is hypothesized to decrease cuticular water permeability and reduce evaporative water loss through the epidermis (Kerstiens 1996; Riederer and Schreiber 2001). The photosynthetic rate was significantly positively correlated with cuticle thickness, indicating that thick cuticle with little water loss through the epidermis may essential for promoting water loss by stomatal gas exchange to increase photosynthetic rate.
The concentration of CO2 is closely related to photosynthesis. Since S. tabernaemontani is an aquatic plant, it has unlimited access to water; however, in wetland habitats, the amount of available CO2 is limited. Under warming conditions, wetland plants may physically cool the leaves with large amounts of readily available water, obtaining limited CO2 amounts through the stomata (Zhang et al. 2007). Plants often show enhanced photosynthetic capacity as the CO2 concentration rises. However, over time, they adapt to these high concentrations, resulting in a “downregulation of photosynthesis” (Wg 1991; Kimball 1991). In our study, net photosynthetic rate, stomatal conductance, and transpiration rate of S. tabernaemontani showed a downward trend under the condition of doubled CO2 concentrations but did not reach significant levels. This is consistent with the findings of Jiang et al. (1997), who reported that in some plants, under high CO2 concentrations, photosynthesis is downregulated; however, the underlying mechanisms still need to be explored. According to previous studies, elevated CO2 concentrations can inhibit photosynthesis via changes in plant physiology and metabolism. Excessive CO2 concentrations (> 700 μmol·mol−1) in plants will affect the consumption capacity of triose phosphate and the regeneration ability of phosphate radicals in the photophosphorylation process, resulting in a decreased CO2 use, which in turn leads to a reduction in the photosynthetic rate (Farquhar 1980). Increasing atmospheric CO2 concentrations also increase the intercellular CO2 concentrations of plants, and to maintain a stable osmotic potential, plants will adjust the opening and closing of their stomata (Guan et al. 2019; Farquhar and Sharkey 1982).
In our study, S. tabernaemontani showed a significant reduction in stomatal length and cuticle thickness under the condition of a doubled CO2 concentration, whereas stomatal density was substantially increased. This indicates a trade-off between stomatal and cuticle traits in the adaptation process. Similarly, Liu (2017) showed that the CO2 concentration regulates leaf wax synthesis by promoting or inhibiting the expression of leaf wax synthesis regulation genes. Increasing CO2 concentrations will significantly reduce leaf wax, which is consistent with the results of this study. Since an increase in CO2 reduces the wax synthesis of the leaves of S. tabernaemontani, which leads to a significant reduction in cuticle thickness, therefore, water is more likely to be lost through the leaves. The present study found a significant correlation between cuticle thickness and stomatal traits; to maintain its leaf water balance, the S. tabernaemontani responded by reducing its stomatal size and increasing its stomatal number, thereby reducing leaf water loss.