Elsevier

Forest Ecology and Management

Volume 432, 15 January 2019, Pages 73-82
Forest Ecology and Management

Oxidative stress as an indicator of niche-width preference of mangrove Rhizophora stylosa

https://doi.org/10.1016/j.foreco.2018.09.015Get rights and content

Highlights

Abstract

Inundation, elevation gradient and salinity fluctuations are considered the major abiotic drivers that influence the growth and distribution of mangroves. In certain conditions, these environmental stressors trigger excessive generation of reactive oxygen species (ROS), affecting mangrove physiology and homeostasis, leading to oxidative stress and mortality if the condition remains exacerbated. As a natural defense to quench the deleterious effects of ROS, mangroves have developed an antioxidant system to scavenge the toxic effects of excessive ROS. This study investigated environmental stress due to salinity, inundation, and elevation gradient using the biochemical responses in the leaves of Rhizophora stylosa as an oxidative stress indicator in greenhouse experiments and field conditions. From the variations of biochemical responses and levels of oxidative stress, the niche-width preference was extrapolated. The results of the study showed that the observed environmental factors significantly induced the generation of high H2O2 concentrations in the leaves of R. stylosa, which in return activated the antioxidant defense system. Inundation of the whole plant imposed a higher-order oxidative stress compared with the effect of salinity in the greenhouse condition, as shown by the significant increase in H2O2, and even caused sublethal damage, as manifested by the chlorotic leaves when prolonged. In the field, rare inundation and high elevation are also considered stressful to R. stylosa, as shown by the significantly higher H2O2 levels compared with those in the frequently inundated (but plants not submerged) areas. The long-term negative effects of high H2O2 at the plant and community levels were manifested in the reduction of growth rate in plants cultured in the greenhouse and the reduction of height in the 30-year-old R. stylosa plantation. Integrating the levels of oxidative stress induced by salinity, inundation and elevation from both greenhouse experiments and field conditions, it appears that relatively low oxidative stress results in a preference of the niche-width of R. stylosa in inundated areas as long as the leaves remain emerged, even during the spring tide. Thus, this species typically dominates middle intertidal areas. These findings could have valuable implications for the selection of areas appropriate for mangrove rehabilitation.

Introduction

Mangroves are halophytic plants inhabiting the intertidal zones of tropical and subtropical regions. Being at the interface between land and sea, the survival and establishment of seedlings are under the continuous influence of different environmental drivers, specifically salinity and tidal inundation (Tomlinson, 2016). Salinity is one of the primary abiotic drivers in mangroves, and the effect of salinity has been extensively studied (Ball, 1988a, Lugo and Snedaker, 1974). However, conflicting views remains unresolved concerning whether mangroves are facultative or obligate halophytes (Krauss and Ball, 2013, Wang et al., 2011). Different mangrove species show different salinity preferences and achieve optimum growth in varying salinity levels. A study by Jayatissa et al. (2008) showed optimum growth of Sonneratia caseolaris at low salinity (3–5 ppt), while Aziz and Khan (2001) reported that Ceriops tagal had optimum growth at 50% seawater. Most studies have found that seedlings grow best at 25% seawater, while high salinity or a total lack of salt (i.e., freshwater) adversely affect growth (Clough, 1984). Tidal inundation is another dominant abiotic drivers in mangroves and considered to have an important role in the paradigm of mangrove establishment and distribution (Krauss et al., 2008); however, research on tidal inundation and species distribution must also acknowledge that vegetation-inundation linkages are not universally applicable and that the species distribution is multifactorial (Friess, 2017).

The establishment of seedlings is the most critical stage in the life cycle of seed plants, and it is rendered difficult for mangroves by the unstable and variable substrates and tidal influence (Tomlinson, 2016). As an adaptation to inhabit the inundated conditions, most mangroves have developed a large propagating structure called the propagule (or seedling). While still attached to the parent tree, the embryo of the propagule is developed, or termed viviparous - typical among Rhizophora species (Hogarth, 2015). Mangrove vivipary results in considerable parental nutrients and energy investment in the early growth of seedlings (Hogarth, 2015, Tomlinson, 2016), providing ample nutrients and energy to support the early growth under nutrient-limited and salt-stressed conditions (Farrant et al., 1992, Krauss et al., 2008).

Mangroves are highly productive forests and known to host a rich and diverse associated marine fauna and provide considerable services to humans (Barbier et al., 2011). However, despite its ecosystem services, mangroves have suffered high decimation in the past decades arising from agriculture and aquaculture conversion (Primavera and Esteban, 2008, Richards and Friess, 2016). In response, mangrove rehabilitation initiatives have attracted a large amount of attention from different sectors to foster mangrove recovery and biodiversity. Most rehabilitation programs have utilized only a single species of Rhizophora (Primavera and Esteban, 2008, Samson and Rollon, 2008), creating a monospecific plantation with no postplanting management plan (Asaeda et al., 2016, Barnuevo et al., 2017). The results of the intensive efforts of mangrove rehabilitation programs are stories of mixed successes and failures. These efforts were often unsuccessful because of the high mortality of the planted seedlings due to inappropriate site selection (Primavera and Esteban, 2008, Samson and Rollon, 2008), and they failed to consider the niche-width preference or the area, which is less stressful to the planted species. Niche-width is a space, a segment of a community or a range of a condition that a species can inhabit and successfully survive (Van Valen, 1965). Mangrove forests worldwide naturally exist in a raised and sloped platform above the mean level, inundated approximately 30% or less by the tidal waters (Lewis III, 2005). More frequent inundation causes stress and eventually mortality. A field study by He and Lai (2009) in China showed that the survival rate of Rhizophora stylosa sharply decreased from 88.9% to 44.0% as the tidal flat elevation decreased. In the Philippines, there is a widespread tendency to plant mangroves in lower intertidal areas that result in low survival of 10–20% (Primavera and Esteban, 2008). Kodikara et al. (2018) showed that seedlings cultured in high salinity had significantly lower survival rates. Mangora et al. (2014) stress that the submergence time and water salinity affect the sustainability of mangrove habitats and that the areas experiencing prolonged submergence with saline water may be the most severely affected.

The combined effects of different abiotic factors affect the physiology of mangroves and, consequently, cause excessive induction of reactive oxygen species (ROS), leading to oxidative stress (Sreenivasulu et al., 2007, Wang et al., 2014). ROS are highly reactive oxygen derivatives that are formed as byproducts of various metabolic pathways localized in different cellular compartments, specifically in chloroplasts, mitochondria and peroxisomes (Nakano and Asada, 1981). In a biological context, ROS, specifically hydrogen peroxide (H2O2), act as signaling molecules; however, in extreme conditions, their levels significantly increase and damage cellular functions, eventually leading to mortality if the unfavorable condition persists (Sharma et al., 2012). As a response, mangroves have developed a species-specific natural defense system, specifically antioxidant enzymes (AOX) (including ascorbate peroxidase, catalase and guaiacol peroxidase) to scavenge the deleterious effects of ROS, and a range of physiological mechanisms (Das et al., 2016, Jaleel et al., 2009). This study determined the niche-width preference of Rhizophora stylosa Griff. by investigating its oxidative stress responses to salinity, water level and inundation, both in field and greenhouse conditions. An understanding of the niche-width of this species provides important insights and guidelines for policymakers and stakeholders in selecting rehabilitation sites to ensure the high survival of plantations.

Section snippets

Propagule collection and experimental design

Mature propagules of Rhizophora stylosa were collected from Olango Island, Lapu-lapu City, Cebu, in the central Philippines on March 2016 and transferred to Saitama University, Japan for culture in the greenhouse. Propagules were considered mature if they were easily detached from the parent tree after gentle shaking of the branch (Robert et al., 2015). The collected propagules were wrapped in a moist paper towel and transported to Japan by airplane. Immediately upon arrival, the propagules

Results

The H2O2 in the leaves of the 5-month cultures of R. stylosa in Experiment 1 showed an increasing trend with increasing salinity (Fig. 2a). The H2O2 levels ranged from 38.2 ± 4.5 to 64.8 ± 5.1 μmol/g FW, and the seedlings cultured in HS had the highest values. Salinity had a significant effect on the variability of H2O2 (F = 57.737, p < 0.0001), while the water depth (LW, MW, HW) and combination of salinity and water depth had no effect (Table 1). In experiment 2, the periodic inundation (SDI

Effects of dominant abiotic factors on biochemical stress responses

This study elucidated the niche-width preference of mangrove R. stylosa using biochemical indicators of oxidative stress in greenhouse and field conditions. The results showed that the H2O2 concentration in the leaves of R. stylosa for both the greenhouse-cultured and field-grown samples showed a positive correlation with increasing salinity. For the greenhouse experiment, the relationship of the leaf H2O2 concentration with salinity is given below:H2O2conc.incrementμmol/g FW=0.5±0.1salinityppt

Conclusion

The results of this study showed that salinity, inundation and elevation gradient caused a variation and significant induction of ROS, specifically of H2O2, in the leaves of R. stylosa. Inundation of the whole plant imposed a higher magnitude of stress, as indicated by ROS levels, compared with the effect of salinity in the greenhouse experiment, and even caused sublethal damage, as manifested by chlorosis of the leaves. This finding implies that the species of R. stylosa cannot withstand a

Acknowledgments

This study was financially supported by the APN project (Project Reference Number ARCP2012-02CMY-Fortes), by the Takahashi Foundation and by Grants-in-Aid for Scientific Research, Japan Society for the Promotion of Science (15H05219). The Department of Environment and Natural Resources Region 7 is duly recognized for granting permits in collecting samples. The valuable assistance of Lekkala Vamsi Krishna during the conduct of fieldwork is duly recognized.

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