Both field investigations and controlled experiments with seedlings under constant salinities have demonstrated that A. corniculatum has limited salt tolerance (Ye et al. 2005; Ball 1988). Aegiceras corniculatum growth performance is best under fresh water (Ye et al. 2005) or low salinity (50 mM NaCl, or 10–25% seawater) conditions (Ball 1988; Ball and Farquhar 1984b; Burchett et al. 1989; Clarke and Hannon 1970). In this study, the growth and photosynthetic performance of A. corniculatum were best at the intermediate site, which is characterized by moderate interstitial water salinity (14–54% seawater) (Table 1).
At the downstream site, both the soil interstitial water salinity (> 17‰) and water salinity (> 20‰) were higher than the optimum salinity for A. corniculatum growth (0–14‰) (Burchett et al. 1989; Clarke and Hannon 1970; Ye et al. 2005). Aegiceras corniculatum here thus suffers from strong salt stress. At the upstream site, both the soil interstitial water salinity (0.5‰) and river water salinity (1.2‰) were close to that of fresh water in the wet season, indicating that A. corniculatum at this site has to tolerate long − term (up to 310 h) freshwater conditions.
Many field reports have demonstrated that changes in leaf δ13C values are independent of N or P levels (McKee et al. 2002), but are affected by changes in salinity (Lin and Sternberg 1993, McKee et al. 2002; Medina and Francisco 1997). Although the N and P concentrations of the soils from the upstream and intermediate sites were significantly higher than that of the downstream site, there were no significant differences in N or P concentrations in the mature leaves among the three sites (Table 2). This implied that nutrition was not the key factor accounting for the significant differences in growth conditions. In the wet season, the increase in leaf δ13C values from the upstream to intermediate to downstream sites was parallel to the increase in soil water salinity (from 0.5 to 20.2‰) (Fig. 5, Table 1). However, this trend was not observed in the dry season. In the dry season, although water salinity increased from the upstream (2.3‰) to intermediate (8.3‰) to downstream (24.3‰) sites, the lowest leaf δ13C value occurred at the intermediate sites rather than the upstream site. In a southern mangrove region in China, Wei et al. (2008) found that an increase in salinity (from 14.1 to 19.8‰) was associated with an increase in δ13C values in the mature leaves of K. obovata, but a decrease in the leaves of A. corniculatum. Rhizophora mangle in south Florida and Twin Cays in Belize demonstrated a pattern of increasing δ13C values with decreasing tree height from fringe to draft stands (Lin and Sternberg 1992; McKee et al. 2002). McKee et al. (2002) suggested that leaf δ13C values simply reflect the variation in environmental conditions caused by changes in tree height and canopy development. A similar result was also found in the dry season in the present study. From the intermediate to upstream to downstream sites, the mean heights of A. corniculatum trees decreased from 4.9 m to 2.5 m to 1.1 m, while the δ13C values increased from − 29.83 to − 29.19 to − 27.07‰ (Fig. 5, Table 1). However, this pattern was not observed in the wet season. The relationship between salinity and leaf δ13C value in the natural environment is thus more complex than previously thought.
Changes in PSII activity can be rapidly diagnosed by measuring chlorophyll fluorescence (Ball et al. 1994; Maxwell and Johnson 2000; Papageorgiou and Govindjee 2004). The actual PSII efficiency and electron transport rate were significantly lower at the downstream site than the other two sites in both seasons, suggesting that the high salinity of the downstream site adversely modified the PSII photochemistry in light-adapted leaves. Our results also showed that 1 − qP and NPQ were higher at the downstream site in both seasons (Fig. 4d, e). 1 − qP, the proportion of PSII reaction centers that were closed, is also termed the ‘excitation pressure’ on PSII (Maxwell et al. 1994). The higher 1 − qP suggested that the excitation pressure on PSII, which has been recognized as a determining factor for photodamage to PSII (Demmig-Adams and Adams 1992), was higher at the downstream site. As high salinity resulted in a significant decrease in actual PSII efficiency and an increase in 1 − qP at the downstream site, the high NPQ at this site may be a mechanism for dissipating excess excitation energy and down-regulating photosynthetic electron transport, thus protecting PSII from photodamage. However, a depression in Fv/Fm in A. marina seedlings was previously observed at high salinities (Björkman et al. 1988; Naidoo 2006). Similarly, Fv/Fm at the downstream site was significantly lower than the other two sites in both seasons (Fig. 3a), indicating that the photoprotection was insufficient and A. corniculatum at this site suffered a higher degree of photoinhibition than at the other sites.
In the dry season, the water salinity at the upstream site recovered to a moderate levels suitable for A. corniculatum growth (Table 1). The ФPSII and ETR at the upstream site were higher, whereas 1 − qP and NPQ were lower than those at the downstream sites. There was also no difference in these parameters between the upstream and intermediate sites. Thus, in the dry season, A. corniculatum at the upstream site had a relatively high photochemistry efficiency and suffered no salt stress. In the wet season, A. corniculatum at the intermediate site had the highest ФPSII and ETR and the lowest 1 − qP and NPQ, indicating that the water salinity here (mean value 4.9‰) was optimal for A. corniculatum. This suggests that A. corniculatum has limited salt tolerance. Our result is consistent with previous results obtained under greenhouse culture (Burchett et al. 1989; Clarke and Hannon 1970).
In the wet season, the water salinity was very low (0–6.8‰) at the upstream site. ФPSII and ETR were significantly lower, while 1 − qP and NPQ were significant higher, at this site than at the intermediate site where the soil salinity was moderate. These results indicated that low salinity adversely modified the PSII photochemistry of A. corniculatum and that there may be a higher degree of photoinhibition/photoprotection in the leaves at the upstream site. Many studies have demonstrated that many mangrove species, including A. corniculatum, grow poorly under extremely low salinities (Ball 2002; Ball and Pidsley 1995; Clarke and Hannon 1970; Clough 1984; Downton 1982; Tuffers et al. 2001; Werner and Stelzer 1990; Yan et al. 2007). In the present study, although the average tree height of A. corniculatum at the upstream site was lower than that of the intermediate site, they still exhibited normal growth. The relatively high Fv/Fm suggested that there was no photodamage at this site (Fig. 3a), but rather simply down − regulated photoprotection. In comparison to the downstream site, the lower water salinity at the intermediate site was associated with increased photosynthesis and tree height. This was consistent with the conclusion that a reduction in salinity led to an increase in primary production (Gabler et al. 2017; Osland et al. 2018).
Although the Na+ and Cl− concentrations of the soil interstitial water were higher in the dry season than in the wet season, the concentrations of these two elements in the leaves in the dry season were similar to those of the wet season. From upstream through to the intermediate to downstream sites, the Na+ and Cl− concentrations of the soil interstitial water increased significantly. The Na+ and Cl− concentrations of the leaves also increased, but not to the same extent. In the wet season, the Na+ concentration of the soil interstitial water increased 33.8 times from the upstream site to the downstream sites; however, the Na+ concentrations of the leaves only increased by 0.6 times, and Cl− showed similar results (Table 4). There were no significant differences in leaf osmolality between the upstream and downstream sites in both seasons (Fig. 2). These results suggested that despite the significant seasonal and spatial variations in water salinity and Na+ and Cl− concentrations of the soil interstitial water, A. corniculatum can maintain relatively constant concentrations of Na+, K+, Ca2+ and Cl− on a bulk-leaf water basis in its body.
Mangroves show higher Na+ and Cl− accumulation ability under low salinity or freshwater (Downton 1982; Mallery and Teas 1984; Patel and Pandey 2009). Though only traces of NaCl were present in the growth medium, the tissue Na+ and Cl− concentrations in mangrove organs were comparatively high (Aziz and Khan 2001; Clough 1984; Patel and Pandey 2009; Werner and Stelzer 1990). Kura-Hotta et al. (2001) discovered that high-salt treatment induced Na+ extrusion and low − salt treatment induced Na+ accumulation in suspension-cultured cells of the mangrove Bruguiera sexangula (Lour.) Poir. Energy − dispersive X-ray microprobe analyses showed that the root vacuoles of R. mangle under freshwater had a Na+ preference, while those of salt-treated plants revealed a strong Na+ exclusion (Werner and Stelzer 1990). In the wet season, A. corniculatum showed very high Na+ and Cl− enrichment ratios of 45.7 and 25.2, respectively, at the upstream site where the water salinity was very low. Even at the intermediate site, the enrichment ratios of Na+ and Cl− were higher than 1. However, in the dry season, none of the enrichment ratios of these two elements were higher than 1. These results suggest that preferentially taking up Na+ and Cl− is a strategy for A. corniculatum dealing with freshwater or low salinity.
The surprisingly higher Na+ and Cl− enrichment ratios in the wet season can be explained in the way: A. corniculatum has a very strong enrichment capacity for Na+ and Cl− under low salinity. However, many greenhouse studies under constant salinity have indicated that the Na+ and Cl− concentrations of mangrove seedlings living under freshwater were much lower than the salinity-treated groups (Paliyavuth et al. 2004; Parida et al. 2004; Yan et al. 2007). According to the above findings, the Na+ and Cl− concentrations of the leaves of A. corniculatum at the upstream site should be lower in the wet season than the dry season. However, our data showed that the Na+ and Cl− concentrations of A. corniculatum at the upstream site remained at a high level in the wet season and did not differ significantly from the dry season. Under constant salinity, the concentrations of Na+ and Cl− in the leaves of A. corniculatum seedlings grown in a solution containing 250 mmol NaCl were significantly higher than those grown in 50 mmol NaCl (Ball and Farquhar 1984a). These two salt levels are similar to the mean salt levels of soil interstitial water at the downstream site (20.2) and intermediate site (4.9) in the wet season in the present study (Table 1). However, there were no significant differences in the leaf Na+ and Cl− concentrations between the two sites in the wet season (Table 4). We thus assumed that A. corniculatum at the upstream site was unable to take up much Na+ and Cl− from the soil during the wet season. Munns (2002) and Tattini et al. (1995) revealed that soil leaching will rapidly restore the water relations of plants but will not affect salt levels in the leaves. This means that plants can store certain salts in their leaves. Thus, some of the salt in the leaves of A. corniculatum at the upstream site in the wet season is accumulated during the dry season when water salinity is relatively high. Our results confirm the suggestion that mangroves grown under fluctuating salinity behave differently from those grown under constant salinity (Beckett et al. 1995; Lin and Sternberg 1993; Wang et al. 2020).
Stored water in the leaves plays an important role in salt tolerance in mangroves (Lechthaler et al. 2016; Nguyen et al. 2017). By storing water in the leaves, mangroves can buffer rapid increases in rhizosphere salinity (Lechthaler et al. 2016). Our results indicated that under long-term freshwater, A. corniculatum can actively accumulate a certain level of salts in its body in order to maintain low water potentials. This helps to maintain water uptake in response to a sudden increase in salinity (Reef et al. 2015). Under fluctuating salinity, stored salts (mainly Na + and Cl−) in the leaves are also important for osmotic adjustment.