Abstract
Key message
This review gives a comprehensive overview of adaptations of mangrove root system to the adverse environmental conditions and summarizes the ecological importance of mangrove root to the ecosystem.
Abstract
In plants, the first line of defense against abiotic stress is in their roots. If the soil surrounding the plant root is healthy and biologically diverse, the plant will have a higher chance to survive in stressful conditions. Different plant species have unique adaptations when exposed to a variety of abiotic stress conditions. None of the responses are identical, even though plants have become adapted to the exact same environment. Mangrove plants have developed complex morphological, anatomical, physiological, and molecular adaptations allowing survival and success in their high-stress habitat. This review briefly depicts adaptive strategies of mangrove roots with respect to anatomy, physiology, biochemistry and also the major advances recently made at the genetic and genomic levels. Results drawn from the different studies on mangrove roots have further indicated that specific patterns of gene expression might contribute to adaptive evolution of mangroves under high salinity. We also review crucial ecological contributions provided by mangrove root communities to the ecosystem including marine fauna.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Introduction
Mangrove ecosystems are one of the major types of natural wetlands along tropical and subtropical shores, and play a vital role in estuarine ecosystems (Peters et al. 1997). Mangrove forests are among the most productive and biologically important ecosystems of the world, because they provide an important and unique ecosystem that impacts positively human society by stabilizing shorelines and reducing the devastating impact of natural disasters, as well as providing food, medicines, fuels and building materials (Tomlinson 1986; Giri et al. 2011). There are 9 orders, 20 families, 27 genera, and roughly 70 species of trees found in mangroves across the world (Alongi 2009). The principal genera are Avicennia (Avicenniaceae), Laguncularia and Lumnitzera (Combretaceae), Nypa (Palmae), Bruguiera, Ceriops, Kandelia and Rhizophora (Rhizophoraceae), and Sonneratia (Sonneratiaceae) (Tomlinson 1986). Indonesia, Australia, Brazil, and Nigeria accommodate roughly 43 % of the world’s mangrove forests, which represent a total area of approximately 160,000 km2 (FAO 2003). Mangrove forests are a characteristic feature of the intertidal zone of tropical and subtropical coasts. Since these forests are regularly flooded with seawater, mangrove trees not only have to cope with high temperatures and low relative air humidity, but also with high and changing salt concentrations, and hypoxia due to regular inundation (MacFarlane et al. 2007; Agoramoorthy et al. 2008; Robert et al. 2012). However, these plants have adapted in various ways, with features such as aerial roots, vivipary, salt exclusion and salt secretion to overcome these threats and thus are able to survive in intertidal zones (Scholander 1968; Tomlinson 1994; Shi et al. 2005).
The success of mangrove plants growing in intertidal zones is generally ascribed to anatomical adaptations (Youssef and Saenger 1996; Liu et al. 2009; Pi et al. 2009) that facilitate O2 supply to submerged roots (Thomson et al. 1990; Colmer 2003; Evans 2003). Mangrove roots must cope with short periods of anoxia, as survival and sustained growth of the plants depend on maintaining oxygen levels in the roots (Alongi 2009). Their shallow nature and the presence of numerous lenticels and extensive aerenchyma facilitate oxygen availability. Most species have structural features (pneumatophores, knee roots, stilt roots or plank roots) to provide root ventilation via atmospheric exposure, at least during low tides (McKee 1993). Some species have above-ground roots with the ability to photosynthesize and thus provide oxygen directly to underground roots (Yabuki et al. 1985; Dromgoole 1988).
This review article gives a comprehensive overview of studies on different morphological, anatomical and physiological adaptations of mangrove root system to the adverse environment. This article also summarizes the positive impact of mangrove roots to costal ecosystems such as protection against floods and hurricanes, reduction of shoreline and riverbank erosion, controlling water pollution, and maintenance of marine fauna.
Mangrove root adaptations to adverse environmental conditions
The most typical adaptations of mangrove species resulted in many types of specialized roots: buttress roots (Xylocarpus granatum), flying buttresses (Rhizophora sp.), surface roots (Excoecaria agallocha), prop roots (Rhizophora apiculata), stilt roots (R. stylosa), spreading roots (Rhizophora sp.), cable roots with pneumatophores, knee roots (Bruguiera gymnorrhiza and B. cylindrica), pencil roots (Sonneratia caseolaris) and cone roots (Avicennia sp.) (Fig. 1a–k). Mangrove species have roots with a higher proportion of gas space when waterlogged and are capable of salt exclusion, or are tolerant to high tissue salt concentrations. Other adaptations include the ability to excrete excess salt from leaves, vivipary or the development of the embryo in seeds before they are dispersed, and seeds and propagules having different morphological adaptations that facilitate flotation (Baskin and Baskin 2001; Hogarth 1999; Tomlinson 1986).
Specialized root for physical stability
In some mangrove species relative root depths differ by both species and growth conditions such as soil compaction, competition for assimilates, water logging, wind force, direction of wave or storm surges, which in turn affects the tree stability (Mickovski and Ennos 2003; Ong et al. 2004). To overcome these adverse circumstances, some mangrove species develops above-ground, functional, modified, spreading root systems such as stilt roots/prop roots and buttress roots instead of consistent below-ground tap root system (Ong et al. 2004). Root adaptations increase physical stability of mangrove trees in the soft sediments along shorelines in unstable mud and enable them to withstand currents and storms. Also, thigmomorphogenetic responses of some mangrove roots might aid in resisting the tension and compression forces created as the crown moves with surging storms by resisting tree toppling.
R. mangle and R. apiculata (Fig. 1d) have prop roots descending from both trunk and branches, providing a stable support system. Submerged prop roots or stilt roots (Fig. 1d, e) help to anchor the plant in place and collect water-borne silt and debris to build soil beneath it. Furthermore, based on the biomechanical adaptations of the rhizophore system (prop roots/flying buttresses from trunk) in R. mangle, it is proven that they can act as a defensive hindrance against storm surges and is higher than that of other mangrove species (Bayas et al. 2011; Ohira et al. 2013; Mendez-Alonzo et al. 2015).
Buttress root development is stimulated in trees parallel to the predominant wind heading, especially on the leeward side. Furthermore, the shape of the roots becomes more oval in weaker soils looking like the “I” shafts regular in engineering (Nicoll and Ray 1996; Clair et al. 2003; Dupuy et al. 2005; Mendez-Alonzo et al. 2015). These roots develop from stress-induced cambial activity found in some species such as Heritiera littoralis, X. granatum (Fig. 1a), Pelliciera rhizophora and Ceriops sp. and provide physical support to prevent tree fall (Clair et al. 2003; Duke 2011). A buttress root bears a narrow strip of bark along the base, which covers its underlying cambium and conductive tissue and connects vertical or inclined root branches with the stem. In addition to anchorage, buttress roots serve as conduits for long distance transport of water, nutrients, and metabolites (Tomlinson 1986; Day et al. 2010). When these roots spread horizontally, they are able to cover a wider area for collecting nutrients from the soil surface. They spread near the upper soil layer where the main nutrients are available (Crook et al. 1997; Mickovski and Ennos 2003; Mendez-Alonzo et al. 2015). Buttresses are tension elements, being larger on the side away from the stress of asymmetrical canopies (Young and Perkocha 1994). Other species of mangrove trees, which grow at higher elevations in drier soils, do not require specialized root structures for physical balance.
Tidal inundation
In mature mangrove trees, different root systems such as cable roots, pneumatophores, feeding roots and anchor roots facilitate gas exchange when they are subjected to tidal inundation. Pneumatophores (Fig. 2a) arise vertically from cable roots and have evolved independently in at least five mangrove families and genera: Laguncularia (Combretaceae), Avicennia (Acanthaceae), Bruguiera (Rhizophoraceae), Xylocarpus (Meliaceae), and Sonneratia (Sonneratiaceae) (Tomlinson 1986). They have abundant lenticels (Fig. 2b), and aerenchyma may account for up to 70 % of root volume (Hogarth 1999). The pneumatophores of Sonneratia and Avicennia are slender and cone shaped (Fig. 2), standing erect and aligned on the cable root of 1–20 m or more in length, which spread horizontally in the soil (Yanez-Espinosa and Flores 2011). Curran et al. (1986) demonstrated that the conductance of pneumatophores in A. marina was sufficient to resupply the root internal gas space during a normal low tide when they exposed to the atmosphere. Curran et al. (1996) measured that the gas space in the roots of the same species was 40–50 % by volume. Upon exposure to low tide, pressure recovers immediately to atmospheric level, but oxygen slowly rises to a plateau below the concentration in the atmosphere. These changes in oxygen concentration are consistent with continuous oxygen diffusion through the pneumatophores (Allaway et al. 2001).
The anatomy of mangrove roots has been extensively studied in relation to development and function (Tomlinson 1986). Prolonged flooding alters physical and chemical properties of soil, as well as bacterial composition, directly affecting the adapted mangrove roots (Rajaniemia and Allison 2009). The affected root vascular system in turn affects the stem vascular system and leaf structure of mangrove species (Visser and Pierik 2007).
Transverse sections of matured pneumatophores show enlarged polygonal or irregular aerenchymatous cells in the cortical region (Fig. 3a). These cells are described as lacunae, which are distributed between epidermis and endodermis without any cell sap (Purnobasuki and Suzuki 2005). Matured pneumatophores consist of more extensive lacunose cortex and a little focal stele in contrast to the young pneumatophores. Usually the root tissue of halophytes shows differential growth responses to different saline concentrations. Hajibagheri et al. (1985) reported that Suaeda maritima grown in the presence of 340 mM NaCl had greater root stele diameter and cortical thickness than those grown in the absence of NaCl. Kandelia candel had a larger ratio of stele to root cross section in low and moderate salinities, suggesting the influence of NaCl on the growth (Hwang and Chen 1995a). The trend was reversed when K. candel was cultured in high salinities (400 and 550 mM NaCl), which could be the result of salt stress caused by the accumulation of Na+ and Cl− in the tissues (Hwang and Chen 1995b). The lower salt concentration or lower rate of exposure to higher salt concentration might be the reason for larger stele regions in young pneumatophores. Early development of the Casparian strips, and their location close to the root apex was observed in salt-grown Puccinellia intermedia (Stelzer and Lauchli 1977) and in S. maritima (Hajibagheri et al. 1985). Moreover, early lignification of secondary tissues, such as metaxylem, was believed to be a general characteristic of plants growing in habitats with a low water potential (Saadeddin and Doddema 1986). These could be the reasons for smaller stele with reduced pith in matured pneumatophores. The clorenchymatous cortex of pneumatophores might be the reason for green color in aerial surface of pneumatophores (Fig. 2).
Lenticels can be seen noticeably on aerial parts of pneumatophores and also on young stilt roots or prop roots and helps to supply oxygen for the underground roots. These are varied in size and morphology, and composed of a complementary tissue (Fig. 3c) with thin-walled spheroidal cells (Purnobasuki and Suzuki 2005). Generally, lenticels develop from the parenchymatous cells adjoining the aerenchyma in cortical region. These parenchymatous cells become specialized and increase in size and then divide. The resulting cells are aligned as complementary cells with intercellular spaces (Fig. 3c). In older pneumatophores, which are covered by periderm, the lenticels arise from the phellogen. At certain places, it also produces complementary tissues in an uninterrupted cortical layer and thus acts as lenticellular meristem (Purnobasuki and Suzuki 2005). The pressure of rapidly dividing and expanding complementary tissue causes the epidermis to protrude outward and finally to rupture exposing the complementary tissue to air.
Apart from the morphological adaptations of mangrove root systems, the vital anatomical modification that enables tolerance to inundation and soil anoxia is the development of aerenchyma with interconnected air channel frameworks throughout the plant. N. fruticans Wurmb. is the only extant mangrove palm which has no specialized root structures to provide oxygen supply to the submerged roots (Chomicki et al. 2014). Since Nypa does not produce any breathing roots, it is believed that the leaves play the role of a ‘giant pneumatophore’, as they are the only emergent parts of the plant (Tomlinson 1994). As an aftermath of senescence, the leaf rachis abscised from the leaf base (petiole) at the zone of intersection and lenticels develop at the same time on the leaf base (Fig. 1l). Soon after, these leaf bases will develop aerenchyma with increasing porosity towards the stem junction. Subsequently, a network of mature lenticels covers the leaf base and connects with aerenchyma network which helps in gases exchange up to 4 years following abscission (Chomicki et al. 2014).
Morphological adjustments such as pneumatophores and lenticels are believed to increase the rate of oxygen diffusion from the aerated parts to the flooding root and eliminate by-products of anaerobic metabolism (ethanol, CO2 and CH4), which is required for the mangrove survival and growth. It is reported that lenticel formation is associated with ethylene and auxin accumulation due to stress caused by O2 deficiency in flooded soil (Bruna et al. 2012; Patel et al. 2014). Flooded roots contain more amount of ethylene and its precursor (acid-1 aminocyclopropane-1-carboxylic acid—ACC), and high activity of ACC synthase and ACC oxidase compared with normal roots (He et al. 1996; Rieu et al. 2005; Vidoz et al. 2010). Even though their presence is often linked to flooding tolerance in plants, the actual physiological responsibility of lenticels is still unclear (Parelle et al. 2006; Liu et al. 2014).
Anaerobic conditions
In submerged mangroves, specialized root structures (Fig. 1) facilitate oxygen supply to live in oxygen-poor or anaerobic sediments. These root adaptations to anaerobic condition help to conserve the atmospheric oxygen by diffusion into the underground root parts. A part of this conserved O2 inside the roots is used for aerobic respiration, while the excess O2 may be released through aerenchyma into the rhizosphere or soil sediments. This mechanism is defined as radial oxygen loss (ROL) in wetland plants (Armstrong 1978; Colmer and Pedersen 2008). To prevent O2 loss from aerenchyma of the root while transporting it to aerial parts of plant, mangrove plants have developed an impermeable layer within the exodermis to mitigate ROL (a barrier to ROL) (Visser et al. 2000; Vasellati et al. 2001; Colmer et al. 2006). Variations in lignin and suberin composition of exodermal cell walls determine the function of this impermeable barrier (Armstrong and Beckett 1987; Soukup et al. 2007). External environmental factors interact perpetually with the root architecture and ROL (Kotula et al. 2009). Some adverse environmental factors, such as continuous flooding (Armstrong et al. 1988), heavy metal attack (Liu et al. 2009; Cheng et al. 2010) and potential phytotoxins (Armstrong and Armstrong 2005) increase the levels of lignification and suberization within cell walls of the exodermis. Lignin deposition within the exodermis could regulate the fluxes of gas, water, and solutes at the interface between root and rhizosphere (Degenhardt and Gimmler 2000; Pollard et al. 2008; Colmer and Greenway 2011).
Halophytic nature
Mangrove communities represent marine halophytes whose different life history stages were framed within the context of salinity tolerance (Tomlinson 1986; Ball 1988; Parida and Jha 2010). No other environmental factors other than salinity admitted more in the mangrove history. Some authors have also categorized mangroves under obligate halophytes (Downton 1982; Clough 1984; Wang et al. 2011). Several mangrove tree species reach an optimum growth at salinities of 5–25 % of standard seawater (Downton 1982; Clough 1984; Ball 1988; Burchett et al. 1989; Ball and Pidsley 1995). However, the range of salinity in which the plant is able to survive varies across the species (Ball 1988); in several species growth may be affected by either absence of or excess of NaCl in the substrate (Downton 1982; Clough 1984; Burchett et al. 1989; Pezeshki et al. 1990; Ball and Pidsley 1995). Krauss and Ball (2013) reported mangroves as a group of facultative halophytes since they can survive and tolerate fresh water. But when these mangroves are grown in normal terrestrial land provided with ample amount of oxygen and fertility, they might not develop any specialized roots with lenticels. As an example, a true mangrove species of S. caseolaris developed pencil roots when it grew in the fresh water (Fig. 4b) as compared to its relative S. alba (Fig. 4a) which produces pencil roots in tidal inundation. In contrast, this species did not produce any specialized roots when it grew under normal terrestrial conditions (Fig. 4c). However, different species exhibit a wide range of tolerance from salt sensitive to those that require higher levels of salt for optimal growth and reproduction (Krauss and Ball 2013).
Salinity balance
It is important for mangroves to control cytosolic salt concentration when living in intertidal zones with high salinity (Tomlinson 1986). Mangrove species develop diverse mechanisms associated with anatomic or physiological characteristics to regulate salt absorption and exclusion, such as ultra-filtration, salt secretion (Tomlinson 1986) and ion sequestration (Mimura et al. 2003; Kura-Hotta et al. 2001). Some species can even accumulate saline ions to balance transmembrane osmotic potentials (Kura-Hotta et al. 2001). Diverse anatomic and physiological strategies of salt management enable mangrove species to adapt to high salinity. Many mangrove species (e.g., K. obovata, Avicennia marina) are able to accumulate inorganic ions to maintain osmotic and water potential (Kura-Hotta et al. 2001; Suarez and Medina 2006). This characteristic confers a survival advantage to these species in a saline environment (Tomlinson 1986).
Nevertheless, intracellular K+/Na+ balance is fundamental to the physiology of living cells and is crucial for plant normal growth (Chen et al. 2007; Shabala and Cuin 2008). Hence excessive ions in the cells would be harmful to the structure and activity of cytosolic proteins (Zhu et al. 2012). In order to maintain the optimal cytosolic K+/Na+ balance and to avoid the adverse effects of high salinity on plant growth and development, halophytes have developed different strategies to avoid excessive Na+ accumulation and to maintain osmotic balance in plants. A common strategy involves the transport restriction of excess Na+ via inhibiting non-selective cation channels (NSCCs) in the root cells (Sun et al. 2010). Moreover, halophytes can elevate the Na+ extrusion from the cytosol to external medium and/or Na+ compartmentation into the vacuoles through transmembrane transport proteins like plasma membrane (PM)-located Na+/H+ antiporter (SOS1) and tonoplast located Na+/H+ antiporter (NHX1) (Wu et al. 2009; Chen et al. 2010). Vacuoles of root cells represent more than 40 % of the total root volume and they contain relatively high Na+ and Cl− concentrations. The vacuoles of these cells act as salt traps, protecting subsequent cell layers (Werner and Stelzer 1990). Chen et al. (2013) reported that nitric oxide greatly contributes to K+/Na+ balance in high salinity-treated K. obovata roots, by activating AKT1-type K+ channel and Na+/H+ antiporter, which are the critical components in K+/Na+ transport system. AKT1, the most important inward-rectifying shaker K+ channel, whose gene is mainly expressed in root epidermal cells, is involved in K+ acquisition by plants (Ardie et al. 2010).
While sequestering excessive ions into vacuoles, mangroves could also accumulate organic osmolytes in cytoplasm to obtain osmotic equilibrium across the tonoplast. Organic osmolytes of mangroves mainly include hydroxyl compounds, free amino acids (especially proline), and polysaccharides (e.g., starch) (Ru et al. 2006). As water salinity increases, some species of mangroves simply become increasingly conservative in their water use, thus achieving greater tolerance (Ball and Passioura 1995). Some species actively excrete excess salt by ultra-filtration at the root cell membrane of cortical cells (Parida and Jha 2010). Since mangrove roots exclude salts when they extract water from soil, soil salts could become very concentrated, creating strong osmotic gradients (Passioura et al. 1992). Zimmermann et al. (1994) reported that the xylem vessels of the roots and stems of mangrove (R. mangle) contain high molecular weight, viscous mucilage made up of acid polysaccharides (mucopolysaccharides). These mucopolysaccharides in the xylem sap are apparently involved in water transport in the xylem conduit of R. mangle (Zimmermann et al. 1994). Accumulation of mucilage in xylem vessels is an important strategy of mangrove trees to save water. The viscous, polymeric substances in the xylem sap limit the rate of water flow and decrease transpiration (Zimmermann et al. 1994, 2002). Combined with high water-use efficiency this mechanism slows the rate of water uptake and prevents salts from accumulating in the soil surrounding the roots. This helps the mangroves conserve water and regulate internal salt concentrations (Ball and Passioura 1995).
Oxidative stress is a secondary effect of salinity, which causes the formation of reactive oxygen species (ROS), such as the superoxide anion (O2 −), hydrogen peroxide (H2O2), the hydroxyl radical (·OH) and singlet oxygen (1O2). Wang et al. (2014) reported the effect of salt stress on antioxidant defense system in the root of a mangrove K. candel. The results showed that a certain salt concentration (<300 mmol/L) was required for the growth of K. candel seedlings. At the early stage of high salt stress, K. candel can rapidly activate antioxidant defense system to resist the salt induced oxidative stress, thus reducing the damages of oxidative stress to plasma membrane, which could be an effective means for K. candel to resist high salt stress (Wang et al. 2014).
The tolerance of mangroves to a high saline environment is also tightly linked to the regulation of gene expression (Parida and Jha 2010). In A. marina, salt stress induces transcription of betaine/proline transporter genes (AmT1, AmT2 and AmT3) in roots and leaves (Waditee et al. 2002). Wong et al. (2007) have identified and isolated 126 cDNA sequences that confer tolerance to salinity from the root of a mangrove plant, B. cylindrica (L.) Blume by suppression subtractive hybridization (SSH) and bacterial functional screening. Among these 75 cDNA sequences of B. cylindrica that conferred salinity tolerance to Escherichia coli 29 tentative unique genes (TUGs) have putative functions in transportation, metabolism and other functions. To identify key genes in the regulation of salt tolerance in the mangrove plant B. gymnorrhiza, cDNA expression libraries were constructed from salt-treated roots and leaves using the host organism Agrobacterium tumefaciens (Ezawa and Tada 2009). Functional screening of the Agrobacterium libraries identified 44 putative salt tolerance genes in B. gymnorrhiza. Miyama et al. (2006) identified 14,842 expressed sequence tags from leaves and roots of B. gymnorrhiza under high salinity or hormone treatments. In total, 129 statistically confident genes were grouped into four clusters depending on their expressed sequence tag (EST) frequency and each group has a specific pattern of transcript profiling under high salinity. Unique gene collections obtained from the assembly of those ESTs were later used in microarray experiments to obtain transcript profiles in leaves and roots of salt-stressed B. gymonorrhiza (Miyama and Hanagata 2007). Totally 228 genes displayed transcript levels fivefold higher than controls, while 60 genes were down-regulated to one-fifth of control levels. Among these remarkably differentially expressed genes, only 32.5 % up-regulated and 3.3 % down-regulated genes were co-regulated in upper and lower leaves, as well as in roots (Miyama and Hanagata 2007).
Basyuni et al. (2009) studied the molecular mechanisms of salinity tolerance in the halophytic K. candel and B. gymnorrhiza roots. mRNA level of multifunctional terpenoid synthase KcMS was increased with salt concentration in both roots and leaves of K. candel. Similarly, salt stress increased the mRNA levels of BgLUS lupeol synthase and BgbAS β-amyrin synthase in the root of B. gymnorrhiza. To isolate anti-salt stress genes from mangrove plants, a cDNA library of R. stylosa roots was constructed and screened for stress-related genes by PCR-based suppressive subtractive hybridization (SSH). Basyuni et al. (2011) isolated and sequenced 240 up-regulated ESTs from the SSH library. Significantly increased expression level of 13 genes was found to contribute to the salt tolerance of this plant. Tada and Kashimura (2009) reported that fructose-1,6-bisphosphate (FBP) aldolase and osmotin were related to salt tolerance in B. gymnorrhiza roots. Zhu et al. (2012) reported that protein folding and degradation-related proteins and cell organization-related proteins were up-regulated and played important roles in salt tolerance of B. gymnorrhiza under severe salt stress. Different concentrations of NaCl treatments revealed differential salt stress mechanisms in this species. Salt-tolerant plants could change their protein expression patterns rapidly to adapt to the saline environment under optimum growth conditions (Pang et al. 2010). Salt stress results in the formation of cytotoxic ROS, which severely disrupt normal metabolism through oxidative damage to lipids, proteins and nucleic acids (Parida and Das 2005). Tolerant plants could overcome oxidative stress, by inducing various defense enzymes and antioxidants (Smirnoff 1995).
Heavy metal exposure
Mangrove roots are also continuously flooded with salty tides of potentially toxic compounds that come from human activities in coastal areas and heavy metal pollutants released into the marine system. Heavy metals in marine water such as copper (Cu), zinc (Zn), lead (Pb), cadmium (Cd), chromium(Cr), iron (Fe), nickel (Ni), manganese (Mn), sulphide (S) and many more trace elements have been reported (Ponnamperuma 1984; Bazzi 2014). Unfortunately, the mechanisms involved in heavy metal tolerance by mangrove plants are poorly understood. Mangrove plants commonly induce changes in the sediment chemistry (e.g., due to O2 release by roots) that can prevent a potentially deleterious metal uptake and tend to show a low transfer of metals from below-ground to above-ground tissues (Lacerda 1998). Absorption, accumulation and dynamics of seven heavy metal elements were studied in mature R. stylosa mangroves (Wen-jiao et al. 1997). In A. marina, the root epidermis has been found to form a major barrier to Pb (MacFarlane and Burchett 2000). Machado et al. (2002) identified the trace metals (Zn, Pb, Cu, Ni, and Mn) in Laguncularia racemosa (L.) Gaertn with low potential of remobilization and biotic uptake. Heavy metal concentrations in mangrove species tissues are associated with the concentration in sediments (Machado et al. 2002).
Cheng et al. (2010) reported that lignification thickening within the exodermis could directly prevent excessive levels of metals entering the roots. Keshavarz et al. (2012) revealed that the Cd and V were negligible in sediments surrounding roots zones of A. marina and R. mucronata, whereas Pd concentrations were higher compared to leaves and roots. Cheng et al. (2014) revealed that the three rhizophoraceous species (B. gymnorrhiza (L.) Poir, K. obovata Sheue, Liu and Yong, and R. stylosa (Griff) consistently exhibited higher metal (Pb, Zn and Cu) tolerances than the three pioneer species [Aegiceras corniculatum (Linn.) Blanco, Acanthus ilicifolius L. and A. marina (Forsk)]. Also, metal-tolerant species develop a thick exodermis with high lignification and suberization and this lignified exodermis delays the metal entry into the roots (Cheng et al. 2014). Silica (Si) is another heavy component that present in marine water, which plays a major role in improving plant resistance towards abiotic and biotic stresses. Sahebi et al. (2014) reported that the Si was mainly observed in the epidermal roots’ cell walls of mangrove plants compared to other parts. The study showed that the candidate gene of serine-rich protein expressed in Si-stressed R. apiculata, using the suppression subtractive hybridization technique (Sahebi et al. 2014).
Ecological importance of mangrove roots
The ecological benefits provided by mangroves roots are generally underestimated. Mangroves provide protection against floods and hurricanes, reduction of shoreline and riverbank erosion, and maintenance of biodiversity (Fig. 5). Moreover, a number of food products are harvested directly within the mangrove system through hunting, gathering, and fishing by native populations.
Mitigation of calamities
Mangroves protect coastal communities from cyclones and storms. Rhizophora has been documented to act as a protective force against natural calamities (McCoy et al. 1996, Mendez-Alonzo et al. 2015). The ability of mangroves in flood control is due to the root system, which has a large spread and also the ability to promote sedimentation. Mangroves and Casuarina plantations reduced tsunami-induced waves and have been shown to protect shorelines against damage (Danielsen et al. 2005). The mitigating effect of mangroves depends on two physical processes of tsunami: (1) wave attack, and (2) towing flow. The protective role of mangroves depends on vegetation characteristics such as, density, height, species composition, density of forest, diameter of mangrove roots and trunks, and elevation of habitats, as well as status of ecological degradation of the forests. Harada et al. (2002) has proved that mangroves form “live seawalls”, and are very cost effective as compared to concrete seawalls and other structures for the protection of coastal erosion. Protection and restoration of mangroves, coastal forests and sand dunes would mitigate the impact of not only tsunamis, but also storms and sea level rise (Kathiresan 2012).
Maintain biodiversity
Mangrove roots serve as a nursery habitat for juvenile fish and protect them from large fish and birds in shallow water environments (Fig. 5). Furthermore, the survival of juvenile fish is promoted by the long residence time of water amongst the mangroves, which is facilitated by the mangrove roots (Gilber and Janssen 1998). Fish species richness has been reported to be as high as almost 200 species in mangrove-dominated estuaries in Australia and India (Robertson and Blaber 1992). Highly valued food and game fish that have a close association with mangroves in the Indo-West Pacific include mullets (Liza, Mugil), groupers (Epinephelus), snappers (Lutjanus), tarpons (Megalops), sea-perch (Lates, Centropomus) and catfish (e.g., Arius, Tachysurus) (Macintosh 1982). In addition to teleosts, a great number of shark and ray species can also be found in mangrove environments (Matthes and Kapetsky 1988). Fisheries production is believed to constitute the major value of marketed products from an unexploited mangrove forest (Hamilton and Snedaker 1984). Mangrove areas are also used as nurseries or breeding grounds for several commercially important species of marine fauna (Saenger 2002). The limited availability of food and the smaller habitat size associated with mangrove removal will result in weaker and more exposed fish populations vulnerable to increased rates of predation (Gilber and Janssen 1998). Many species of palaemonid shrimps are also associated with mangroves, including the commercially important giant freshwater shrimp, Macrobrachium rosenbergii (Macnae 1974; Matthes and Kapetsky 1988; Singh et al. 1994). The mangrove crab fauna is of major ecological and economic importance (Macnae 1974; Macintosh 1982; Matthes and Kapetsky 1988), including the high-priced mangrove mud crab, Scylla serrata. Mangrove-associated fauna are not restricted to the waters and substrate surrounding mangrove roots, as the roots themselves support a thriving and diverse community of molluscs, arthropods and other animals (Ng and Sivasothi 1999). Mangrove roots regulate water quality and this service prevents the deterioration of sea grass or coral reef habitats. Moreover, mangrove-associated mudflats provide feeding grounds not only for resident species, but also for migratory birds that rely on coastal mudflats during their annual migrations to warmer climates.
Furthermore, mangrove rhizosphere is also an excellent habitat for bacteria from estuarine sediments. Alongi (2005) identified sulfate-reducing genera (Desulfovibrio, Desulfotomaculu, Desulfosarcina and Desulfococcu), and other bacterial types such as methanogens, iron- and manganese-reducers, denitrifiers, nitrogen fixers (e.g., Azotobacter, Rhizobium) as the major decomposers in the mangrove soils. Gomes et al. (2010) reported that the R. mangle rhizosphere samples contained the most distinct composition of the major taxonomic groups included, significantly higher amount of Acidobacteria, Actinobacteria, Verrucromicrobia, Burkholderiales, Caulobacterales and Rhizobiales and significantly lower amount of Chloroflexi, Firmicutes and Desulfobacterales. The microbes in the mangrove habitats are known to decompose mangrove litter (Kathiresan 2012). Nitrogen-fixing bacteria play a major role in re-mineralization processes in mangrove ecosystems which interact with mangrove roots making nitrogen available for plants. Nypa palm roots possessed active nitrogen-fixing endophytic bacteria called Burkholderia vietnamiensis (Tang et al. 2010). Understanding the nitrogen-fixing bacteria–mangrove model system is essential to study the interaction of molecular mechanisms involved. Soares Junior et al. (2013) isolated different taxonomical groups of cellulolytic bacteria from mangrove sediments (Alphaproteobacteria, Gammaproteobacteria, Actinobacteria, Firmicutes and Bacteroidetes) and reported that mangrove soils harbor cellulolytic organisms with distinctive characteristics that can be further explored for cellulose degradation for distinct purposes.
Carbon accumulation
Mangrove root biomass is another important factor in forest ecosystems, which is studied in the yield of wood as a function of age, stand density, and as an indicator of atmospheric, soil pollution input and forest health (Komiyama et al. 2002). Mangrove forests develop massive root biomass to stand upright in the muddy and unstable substrates (Komiyama 2014). The root production may contribute towards half or total standing biomass in mangroves (Briggs 1977). Since they grow in saturated, muddy, low oxygen soils, more amount of carbon is stored in roots, resists decay and can become long-term sinks as mangrove peat (Middleton and McKee 2001). Hence, mangrove roots provide other significant ecological services such as carbon storage. Extensive studies have been conducted on the considerable biomass stored in mangroves, which interestingly have a disproportionately high level of biomass stored in roots compared to other forest systems (Komiyama et al. 2008). The large allocation of biomass to the roots can be understood given the muddy and unstable substrate to which mangroves have to be anchored. Sizeable investments must be made to the roots to ensure that mangroves can stand upright in soft mud (Komiyama 2014). This alone, however, cannot explain the surprising root to shoot biomass allocation, which may be better understood through the nature of decomposition in mangrove roots. Though root decomposition is dependent on a variety of factors (Poungparn et al. 2009), fine root decomposition in mangroves appears to be a slow process; a study of fine root necro-mass in eastern Thailand found an astonishingly high dead to total fine root mass, as much as 98.5 % (Chalermchatwilai et al. 2011). Mangrove peat may be predominantly made up of fine roots (Ono et al. 2015), suggesting that mangroves may play an unappreciated role in carbon sequestration. Ecosystem features of mangroves are not independent. For example, animal richness and density is positively correlated with root biomass (Wada et al. 1987). Most of the substrata in the tropics except under deltaic environments consist of mangrove peat, which mainly derives from mangrove roots. They accumulate sediments via their complex aerial and submerged root systems and play a major role in land expansion (Fig. 5).
Conclusion
The anatomical and morphological characteristics of living plants are commonly correlated with the particular combination of environmental conditions under which individual plants are established and grown (Arens 1997). Mangroves tolerate high salinity by rejecting potentially harmful salts. Some species of mangroves actively excrete those salts by means of specialized salt glands in their leaves and some species excrete salt by ultra-filtration at the root cell membranes of cortical cells. Adaptability of mangroves to adverse conditions makes them ideal ecological models to study adaptation of mangroves to different abiotic stresses. Mangroves also provide a reservoir for some of the best known novel genes and proteins, involved in tolerance to salinity stress and water logging conditions that are likely to be applicable in other crop plants.
The rhizosphere of mangrove trees extend into the intertidal and subtidal zones where they turn into a rare feature: hard substrata in a soft sediment environment. As such, mangrove roots have become a good source for terrestrial as well as marine plants, algae, invertebrates and vertebrates. Also, their prolific habitats support coastal fisheries for prawns and fishes (Manson et al. 2005). Apart from the above uses, they are also essential to humans for a variety of reasons, including aquaculture, agriculture, forestry, protection against shoreline erosion, as a source of fire-wood and building materials, and other local subsistence uses (Walters et al. 2008). Mangrove sediments also have a high capacity for absorbing and holding heavy metals thereby preventing the spread of metal pollution in coastal areas. Globally, mangrove forests are being reduced at an alarming rate. They get affected either by direct impacts such as cutting and pollution, or by indirect impacts such as changes in local freshwater management (Dahdouh-Guebas et al. 2005), and are often regarded as unpleasant environments with little intrinsic value. In 26 developing countries, about 90 % of mangroves are critically endangered and in extant condition (Zhila et al. 2014). Therefore, understanding and appreciating the importance of mangrove to the coastal ecosystem is crucial to the wise use and stewardship of this unique plant community.
Author contribution statement
Z.C. initiated the project. S.S. contributed to the figures. S.S. and Z.C. wrote the manuscript. S.K.Y.L. and Z.C. revised the manuscript.
References
Agoramoorthy G, Chen FA, Hsu MJ (2008) Threat of heavy metal pollution in halophytic and mangrove plants of Tamil Nadu, India. Environ Pollut 155:320–326
Allaway WG, Curran M, Hollington LM, Ricketts MC, Skelton NJ (2001) Gas space and oxygen exchange in roots of Avicinia marina (Forssk.) Vierh. Var. australiasia (Walp.) Moldenke ex N.C. Duke, the grey mangrove. Wetland Ecol Manag 9:211–218
Alongi DM (2005) Mangrove-microbe-soil relations. In: Kristensen E, Haese RR, Kostka JE (eds) Macro- and microorganisms in marine sediments. American Geophysical Union, Washington, pp 85–103
Alongi DM (2009) The energetics of mangrove forests. Springer, New York
Ardie SW, Liu S, Takano T (2010) Expression of the AKT1-type K+ channel gene from Puccinellia tenuiflora, PutAKT1, enhances salt tolerance in Arabidopsis. Plant Cell Rep 29:865–874
Arens NC (1997) Responses of leaf anatomy to light environment in the tree fern Cyatheaca racasana (Cyatheaceae) and its application to some ancient seed ferns. Palaios 12:84–94
Armstrong W (1978) Plant aeration in the wetland condition. In: Hook DD, Crawford RMM (eds) Anaerobiosis and plant adaptations. Ann Arbor Pub Inc, Michigan, pp 269–297
Armstrong J, Armstrong W (2005) Rice: sulfide-induced barriers to root radial oxygen loss, Fe2+ and water uptake, and lateral root emergence. Ann Bot 96:625–638
Armstrong W, Beckett PM (1987) Internal aeration and the development of stelar anoxia in submerged. A multi shelled mathematical modal combining axial diffusion of oxygen in the cortex with radial losses to the stele, the wall layers and the rhizosphere. New Phytol 105:221–245
Armstrong J, Armstrong W, Beckett PM (1988) Phragmites australis: a preliminary study of soil-oxidising sites and internal gas transport pathways. New Phytol 108:373–382
Ball MC (1988) Ecophysiology of mangroves. Trees Struct Funct 2:129–142
Ball MC, Passioura JB (1995) Carbon gain in relation to water use: photosynthesis in mangroves. In: Schulze ED, Caldwell NM (eds) Ecophysiology of photosynthesis. Springer, Berlin, pp 247–257
Ball MC, Pidsley SM (1995) Growth response to salinity in relation to distribution of two mangrove species, Sonneratia alba and S. lanceolata. Funct Ecol 9:77–85
Baskin CC, Baskin JM (2001) Seeds: ecology, biogeography, and evolution of dormancy and germination. Academic Press, London. ISBN 0-12-080260-0
Basyuni M, Baba S, Inafuku M, Iwasaki H, Kinjo K, Oku H (2009) Expression of terpenoid synthase mRNA and terpenoid content in salt stressed mangrove. J Plant Physiol 166:1786–1800
Basyuni M, Kinjo Y, Baba S, Shinzato N, Iwasaki H, Siregar EBM, Oku H (2011) Isolation of salinity tolerance genes from roots of mangrove plant, Rhizophora stylosa Griff., using PCR-based suppression subtractive hybridization. Plant Mol Biol Rep 29:533–543
Bayas JCL, Marohn C, Dercon G, Dewi S, Piepho PH, Joshi L, Noordwijk M, Cadisch G (2011) Influence of coastal vegetation on the 2004 tsunami wave impact in west Aceh. PNAS 108:18612–18617
Bazzi AO (2014) Heavy metals in seawater, sediments and marine organisms in the Gulf of Chabahar, Oman Sea. J Oceanogr Mar Sci 5:20–29
Briggs SV (1977) Estimates of biomass in a temperate mangrove community. J Aust Ecol 2:369–373
Bruna CR, Fabiana ZB, Alex-Alan FA (2012) Regulation of gene expression in response to abiotic stress in plants. In: Bubulya P (ed) Cell metabolism—cell homeostasis and stress response, InTech. ISBN: 978-953-307-978-3. doi:10.5772/26636
Burchett MD, Clarke CJ, Field CD, Pulkownik A (1989) Growth and respiration in two mangrove species at a range of salinities. Plant Physiol 75:299–303
Chalermchatwilai B, Poungparn S, Patanaponpaiboon P (2011) Distribution of fine-root necromass in a secondary mangrove forest in Trat province, Eastern Thailand. Sci Asia 37:1–5
Chen Z, Pottosin II, Cuin TA, Fuglsang AT, Tester M et al (2007) Root plasma membrane transporters controlling K+/Na+ homeostasis in salt-stressed barley. Plant Physiol 145:1714–1725
Chen J, Xiao Q, Wu F, Dong X, He J et al (2010) Nitric oxide enhances salts secretion and Na+ sequestration in a mangrove plant, Avicennia marina, through increasing the expression of H+-ATPase and Na+/H+ antiporter under high salinity. Tree Physiol 30:1570–1586
Chen J, Xiong DY, Wang WH, Hu WJ, Simon M (2013) Nitric oxide mediates root K+/Na+ balance in a mangrove plant, Kandelia obovata, by enhancing the expression of AKT1-type K+ channel and Na+/H+antiporter under high salinity. PLoS One 8(8):e71543. doi:10.1371/journal.pone.0071543
Cheng H, Liu Y, Tam NFY, Wang X, Li SY, Chen GZ, Ye ZH (2010) The role of radial oxygen loss and root anatomy on zinc uptake and tolerance in mangrove seedlings. Environ Pollut 158:1189–1196
Cheng H, Jiang ZY, Liu Y, Ye ZH, Wu ML, Sun CC, Sun FL, Fei J, Wang YS (2014) Metal (Pb, Zn and Cu) uptake and tolerance by mangroves in relation to root anatomy and lignification/suberization. Tree Physiol 34:646–656
Chomicki G, Bidel LPR, Baker WJ, Jay-Allemand C (2014) Palm snorkelling: leaf bases as aeration structures in the mangrove palm (Nypa fruticans). Bot J Linn Soc 174:257–270
Clair B, Fournier M, Oise Prevost MF, Beauchene J, Bardet S (2003) Biomechanics of buttressed trees: bending strains and stresses. Am J Bot 90:1349–1356
Clough BF (1984) Growth and salt balance of the mangroves Avicennia germinans (Forsk.) Vierh. And Rhizophora stylosa Griff. in relation to salinity. Aust J Plant Physiol 11:419–430
Colmer TD (2003) Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deep-water rice (Oryza sativa L.). Ann Bot 91:301–309
Colmer TD, Greenway H (2011) Iron transport in seminal and adventitious roots of cereals during O2 deficiency. J Exp Bot 62:39–57
Colmer TD, Pedersen O (2008) Oxygen dynamics in submerged rice (Oryza sativa). New Phytol 178:326–334
Colmer TD, Cox MCH, Voesenk LACJ (2006) Root aeration in rice (Oryza sativa): evaluation of oxygen, carbon dioxide, and ethylene as possible regulators of root acclimatizations. New Phytol 170:767–778
Crook MJ, Ennos AR, Banks JR (1997) The function of buttress roots: a comparative study of the anchorage systems of buttressed (Aglaia and Nephelium ramboutan species) and non-buttressed (Mallotus wrayi) tropical trees. J Exp Bot 48:1703–1716
Curran M, Cole M, Allaway WG (1986) Root aeration and respiration in young mangrove plants (Avicennia marina (Forsk) Vierh). J Exp Bot 37:1225–1233
Curran M, James P, Allaway WG (1996) The measurement of gas spaces in the roots of aquatic plants: Archimedes revisited. Aquat Bot 54:255–261
Dahdouh-Guebas F, Hettiarachchi S, Lo Seen D, Batelaan O, Sooriyarachchi S, Jayatissa LP, Koedam N (2005) Transitions in ancient inland freshwater resource management in Sri Lanka affect biota and human populations in and around coastal lagoons. Curr Biol 15:579–586
Danielsen F, Sorensen MK, Olwig MF, Selvam V, Parish F et al (2005) The Asian tsunami: a protective role for coastal vegetation. Science 310:643
Day DS, Wiseman EP, Dickinson SB, Harris JR (2010) Contemporary concepts of root system architecture of urban trees. Arboric Urban For 36:149–159
Degenhardt B, Gimmler H (2000) Cell wall adaptations to multiple environmental stresses in maize roots. J Exp Bot 51:595–603
Downton WJS (1982) Growth and osmotic relations of the mangrove Avicennia marina, as influenced by salinity. Aust J Plant Physiol 9:519–528
Dromgoole FI (1988) Carbon dioxide fixation in aerial roots of the New Zealand mangrove Avicennia marina var resinifera. NZ J Mar Freshw Res 22:617–619
Duke NC (2011) Mangroves. Structure, form and process. In: Hopley D (ed) Encyclopedia of modern coral reefs. Springer, Dordrecht, pp 655–663
Dupuy L, Fourcaud T, Stokes A (2005) A numerical investigation into factors affecting the anchorage of roots in tension. Eur J Soil Sci 56:319–327
Evans DE (2003) Aerenchyma formation. New Phytol 161:35–49
Ezawa S, Tada Y (2009) Identification of salt tolerance genes from the mangrove plant Bruguiera gymnorrhiza using Agrobacterium functional screening. Plant Sci 176:272–278
FAO (2003) Status and trends in mangrove area extent worldwide. Forest resources assessment working paper 63. Forest Resources Division, Rome. http://www.fao.org/docrep/007/j1533e/J1533E00.htm. Accessed 28 Jan 2010
Gilber AJ, Janssen R (1998) Use of environmental functions to communicate the values of a mangrove ecosystem under different management regimes. Ecol Econom 25:323–346
Giri C, Ochieng E, Tieszen LL, Zhu Z, Singh A, Loveland T, Masek J, Duke N (2011) Status and distribution of mangrove forests of the world using earth observation satellite data. Global Ecol Biogeogr 20:154–159
Gomes NCM, Flocco CG, Costa R, Junca H et al (2010) Mangrove microniches determine the structural and functional diversity of enriched petroleum hydrocarbon-degrading consortia. FEMS Microbiol Ecol 74:276–290
Hajibagheri MA, Yeo AR, Flowers TJ (1985) Salt tolerance in Suaeda maritima (L.) Dum.: fine structure and ion concentrations in the apical region of roots. New Phytol 99:331–343
Hamilton LS, Snedaker SC (eds) (1984) Handbook for mangrove area management. UNEP and East West Center, Environment and Policy Institute, Honolulu, p 126
Harada K, Imamura F, Hiraishi T (2002) Experimental study on the effect in reducing tsunami by the coastal permeable structures. In: Final proceedings of international offshore polar engineering conference, USA, pp 652–658
He CJ, Finlayson SA, Drew MC, Jordan WR, Morgan PW (1996) Ethylene biosynthesis during aerenchyma formation in roots of Zea mays subjected to mechanical impedance and hypoxia. Plant Physiol 112:1679–1685
Hogarth PJ (1999) The biology of mangroves. Oxford University Press, New York. ISBN 0-19-850222-2
Hwang YH, Chen SC (1995a) Salt tolerance in seedlings of the mangrove Kandelia candel (L.) Druce, Rhizophoraceae. Bot Bull Acad Sin 36:25–31
Hwang YH, Chen SC (1995b) Anatomical responses in Kandelia candel (L.) Druce seedlings growing in the presence of different concentrations of NaCl. Bot Bull Acad Sin 36:181–188
Kathiresan K (2012) Importance of mangrove ecosystem. Int J Mar Sci 2:70–89
Keshavarz M, Mohammadikia D, Gharibpour F, Dabbagh A-R (2012) Accumulation of heavy metals (Pb, Cd, V) in sediment, roots and leaves of mangrove species in Sirik Creek along the sea coasts of Oman, Iran. J Appl Sci Environ Manag 16:323–326
Komiyama A (2014) Conservation of mangrove ecosystems through the eyes of a production ecologist. Rev Agric Sci 2:11–20. doi:10.7831/ras.2.11
Komiyama A, JintanaV SangtieanT, Kato S (2002) A common allometric equation for predicting stem weight of mangroves growing in secondary forests. Ecol Res 17:415–418. doi:10.1046/j.1440-1703.2002.00500.x
Komiyama A, Ong JE, Poungparn S (2008) Allometry, biomass and productivity of mangrove forests: a review. Aquat Bot 89:128–137
Kotula L, Ranathunge K, Schreiber L, Steudle E (2009) Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice (Oryza sativa L.) grown in aerated or deoxygenated solution. J Exp Bot 60:2155–2167
Krauss KW, Ball MC (2013) On the halophytic nature of mangroves. Trees 27:7–11. doi:10.1007/s00468-012-0767-7
Kura-Hotta M, Mimura M, Tsujimura T et al (2001) High salt treatment induced Na+ extrusion and low salt treatment-induced Na+ accumulation in suspension-cultured cells of the mangrove plant, Bruguiera sexangula. Plant Cell Environ 24:1105–1112
Lacerda LD (1998) Biogeochemistry of trace metals and diffuse pollution in mangrove ecosystems. International Society for Mangrove Ecosystems, Okinawa, p 64
Liu Y, Tam NFY, Yang JX, Pi N, Wong MH, Ye ZH (2009) Mixed heavy metals tolerance and radial oxygen loss in mangrove seedlings. Marine Poll Bull 58:1843–1849
Liu Z, Cheng R, Xiao W, Guo Q, Wang N (2014) Effect of off-season flooding on growth, photosynthesis, carbohydrate partitioning, and nutrient uptake in Distylium chinense. PLoS One 9(9):e107636. doi:10.1371/journal.pone.0107636
MacFarlane GR, Burchett MD (2000) Cellular distribution of copper, lead and zinc in the grey mangrove, Avicennia marina (Forsk.) Vierh. Aqua Bot 68:45–59
MacFarlane GR, Koller CE, Blomberg SP (2007) Accumulation and partitioning of heavy metals in mangroves: a synthesis of field-based studies. Chemosphere 69:1454–1464
Machado W, Moscatelli M, Rezende LG, Lacerda LD (2002) Mercury, zinc and copper accumulation in mangrove sediments surrounding a large landfill in southeast Brazil. Environ Pollut 120:455–461
Macintosh DJ (1982) Fisheries and aquaculture significance of mangrove swamps, with special reference to the Indo-West Pacific region. In: Muir JF, Roberts RJ (eds) Recent advances in aquaculture. Croom Helm, England, pp 4–85
Macnae W (1974) Mangrove forests and fisheries. FAO/UNDP Indian Ocean Programme. UN, IOFC/DEV/7434
Manson FJ, Loneragan NR, Skilleter GA, Phinn SR (2005) An evaluation of the evidence for linkages between mangroves and fisheries: a synthesis of the literature and identification of research directions. Oceanogr Mar Biol Annu Rev 43:483–513
Matthes H, Kapetsky JM (1988) Worldwide compendium of mangrove-associated aquatic species of economic importance. FAO, Rome FAO Fishery Circular No 814:238
McCoy ED, Mushinsky HR, Johnson D, Meshaka WE (1996) Mangrove damage caused by Hurricane Andrew on the southwestern coast of Florida. Bull Mar Sci 59:1–8
McKee KL (1993) Soil physicochemical patterns and mangrove species distribution reciprocal effects? J Ecol 81:477–487
Mendez-Alonzo R, Moctezuma C et al (2015) Root biomechanics in Rhizophora mangle: anatomy, morphology and ecology of mangrove’s flying buttresses. Ann Bot. doi:10.1093/aob/mcv002
Mickovski SB, Ennos AR (2003) Anchorage and asymmetry in the root system of Pinus peuce. Silva Fennica 37:161–173
Middleton BA, McKee KL (2001) Degradation of mangrove tissues and implications for peat formation in Belizean island forests. J Ecol 89:818–828
Mimura T, Kura-Hotta M, Tsujimura T et al (2003) Rapid increase of vacuolar volume in response to salt stress. Planta 216:397–402
Miyama M, Hanagata N (2007) Microarray analysis of 7029 gene expression patterns in Burma mangrove under high-salinity stress. Plant Sci 172:948–957
Miyama M, Shimizu H, Sugiyama M, Hanagata N (2006) Sequencing and analysis of 14,842 expressed sequence tags of Burma mangrove, Bruguiera gymnorrhiza. Plant Sci 171:234–241
Ng PKL, Sivasothi N (eds) (1999) A guide to the mangroves of Singapore II: Animal diversity. Singapore Science Centre, Singapore, p 168
Nicoll BC, Ray D (1996) Adaptive growth of tree root systems in response to wind action and site conditions. Tree Physiol 16:891–898
Ohira W, Honda K, Nagai M, Ratanasuwan A (2013) Mangrove stilt root morphology modeling for estimating hydraulic drag in tsunami inundation simulation. Trees Struct Funct 27:141–148
Ong JE, Gong WK, Wong CH (2004) Allometry and partitioning of the mangrove—Rhizophora apiculata. Forest Ecol Manag 188:395–408
Ono K, Hiradate S, Morita S, Hiraide M, Hirata Y, Fujimoto K, Tabuchi R, Lihpai S (2015) Assessing the carbon compositions and sources of mangrove peat in a tropical mangrove forest on Pohnpei Island, Federated States of Micronesia. Geoderma 245–246:11–20
Pang QY, Chen SX, Dai SJ, Chen YZ, Wang Y, Yan XF (2010) Comparative proteomics of salt tolerance in Arabidopsis thaliana and Thellungiella halophila. J Proteome Res 9:2584–2599
Parelle J, Brendel O, Bodenes C, Berveiller D, Dizengremel P et al (2006) Differences in morphological and physiological responses to waterlogging between two sympatric oak species (Quercus petraea [Matt.] Liebl., Quercus robur L.). Ann Forest Sci 63:849–859
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349
Parida AK, Jha B (2010) Salt tolerance mechanisms in mangroves: a review. Trees 24:199–217. doi:10.1007/s00468-010-0417-x
Passioura JB, Ball MC, Knight JH (1992) Mangroves may salinise the soil and in so doing limit their transpiration rate. Funct Ecol 6:476–481
Patel PK, Singh AK, Tripathi N, Yadav D, Hemantaranjan A (2014) Flooding: abiotic constraint limiting vegetable productivity. Adv Plants Agric Res 1(3):00016. doi:10.15406/apar.2014.01.00016
Peters EC, Gassman NJ, Firman JR, Richmond H, Power EA (1997) Ecotoxicology of tropical marine ecosystems. Environ Toxicol Chem 16:12–40
Pezeshki SR, DeLaune RD, JrWH Patrick (1990) Differential response of selected mangroves to soil flooding and salinity: gas exchange and biomass. Can J Forest Res 20:869–874
Pi N, Tam NFY, Wu Y, Wong MH (2009) Root anatomy and spatial pattern of radial oxygen loss of eight true mangrove species. Aq Bot 90:222–230
Pollard M, Beisson F, Li YH, Ohlrogge JB (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13:236–246
Ponnamperuma FN (1984) Effect of flooding on soils. In: Kozlowski T (ed) Flooding and Plant Growth. Academic Press, New York, pp 9–45
Poungparn S, Komiyama A, Tanaka A, Sangtiean T, Maknual C, Kato S, Tanapermpool P, Patanaponpaiboon P (2009) Carbon dioxide emission through soil respiration in a secondary mangrove forest of eastern Thailand. J Trop Eco l25:393–400
Purnobasuki H, Suzuki M (2005) Functional anatomy of air conducting network on the pneumatophores of a mangrove plant, Avicennia marina (Forsk.)Vierh. Asian J Plant Sci 4:334–347
Rajaniemia TK, Allison VJ (2009) Abiotic conditions and plant cover differentially affect microbial biomass and community composition on dune gradients. Soil Biol Biochem 41:102-109. ISSN 0038–0717
Rieu I, Cristescu SM, Harren FJ, Huibers W, Voesenek LA, Mariani C, Vriezen WH (2005) RP-ACS1, a flooding-induced 1-aminocyclopropane-1-carboxylate synthase gene of Rumex palustris, is involved in rhythmic ethylene production. J Exp Bot 56:841–849
Robert EMR et al. (2012) The ecological success of the mangrove Avicennia: the perfect combination of well-adapted wood anatomical characteristics and special radial growth? In: Proceedings of the international conference ‘Meeting on Mangrove ecology, functioning and management—MMM3’, Galle, Sri Lanka, 2–6 July 2012. VLIZ Special Publication, vol 57, p 158
Robertson AI, Blaber SJM (1992) Plankton, epibenthos and fish communities. Coast Estuar Stud 41:173–224
Ru QM, Zheng HL, Xiao Q (2006) Advances in salt tolerance mechanism of mangrove. Acta Bot Yunnanica (in Chinese) 28:78–84
Saadeddin R, Doddema H (1986) Anatomy of the `extreme’ halophyte Arthrocnemum fruticosum (L.) Moq. In relation to its physiology. Ann Bot 57:531–544
Saenger P (2002) Mangrove ecology, silviculture and conservation. Kluwer Academic Publishers, pp 360
Sahebi M, Hanafi MM, Abdullah SNA, Rafii MY, Azizi P, Nejat N, Idris AS (2014) Isolation and expression analysis of novel silicon absorption gene from roots of mangrove (Rhizophora apiculata) via suppression subtractive hybridization. Biomed Res Int, vol 2014, Article ID 971985, 11 pages. doi:10.1155/2014/971985
Scholander PF (1968) How mangroves desalinate seawater. Plant Physiol 21:251–261
Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plantarum 133:651–669
Shi SH, Huang YL, Zeng K, Tan FX, He HH, Huang JZ, Fu YX (2005) Molecular phylogenetic analysis of mangroves: independent evolutionary origins of vivipary and salt secretion. Mol Phylogenet Evol 34:159–166
Singh HR, Chong VC, Sasekumar A, Lim KH (1994) Value of mangroves as nursery and feeding grounds. Proceedings of the Third ASEAN-Australia Symposium on Living Coastal Resources, vol 1 Chulalongkorn University, Bangkok, pp 105-122
Smirnoff N (1995) Antioxidant systems and plant response to the environment. In: Smirnoff N (ed) Environment and plant metabolism: flexibility and acclimation. BIOS Scientific Publishers, Oxford, pp 217–243
Soares Junior FL et al (2013) Endo-and exoglucanase activities in bacteria from mangrove sediment. Braz J Microbiol 44:969–976
Soukup A, Armstrong W, Schreiber L, Franke R, Votrubova O (2007) Apoplastic barriers to radial oxygen loss and solute penetration: a chemical and functional comparison of the exodermis of two wetland species, Phragmites australis and Glyceria maxima. New Phytol 173:264–278
Stelzer R, Lauchli A (1977) Salt and flooding tolerance of Puccinelli apeisonis: I. The effect of NaCl- and KCl-Salinity on growth at varied oxygen supply to the root. Z. Pflanzen physiol 83:35–42
Suarez N, Medina E (2006) Influence of salinity on Na+ and K+ accumulation, and gas exchange in Avicennia germinans. Photosynthetica 44:268–274
Sun J, Wang MJ, Ding MQ, Deng SR, Liu MQ et al (2010) H2O2 and cytosolic Ca2+ signals triggered by the PM H+-coupled transport system mediate K+/Na+ homeostasis in NaCl− stressed Populus euphratica cells. Plant, Cell Environ 33:943–958
Tada Y, Kashimura T (2009) Proteomic analysis of salt-responsive proteins in the mangrove plant, Bruguiera gymnorhiza. Plant Cell Physiol 50:439–446. doi:10.1093/pcp/pcp002
Tang S, Hara S et al (2010) Burkholderia vietnamiensis isolated from root tissues of Nipa palm (Nypa fruticans) in Sarawak, Malaysia, proved to be its major endophytic nitrogen-fixing bacterium. Biosci Biotechnol Biochem 74:1972–1975
Thomson CJ, Armstrong W, Waters I, Greenway H (1990) Aerenchyma formation and associated oxygen movement in seminal and nodal roots of wheat. Plant Cell Environ 13:395–403
Tomlinson PB (1986) The botany of mangroves. Cambridge University Press, Cambridge
Tomlinson PB (1994) The botany of mangroves. Cambridge University Press, Cambridge
Vasellati V, Oesterheld M, Medan D, Loreti J (2001) Effect of flooding and drought on the anatomy of Paspalun dilatatum. Ann Bot 88:355–360
Vidoz ML, Loreti E, Mensuali A, Alpi A, Perata P (2010) Hormonal interplay during adventitious root formation in flooded tomato plants. Plant J 63:551–562
Visser EJ, Pierik R (2007) Inhibition of root elongation by ethylene in wetland and non-wetland plant species and the impact of longitudinal ventilation. Plant Cell Environ 30:31–38
Visser ED, Colmer TD, Blom CWPM, Voesenk LACJ (2000) Change in growth, porosity, and radial oxygen loss from adventitious roots of selected mono- and dicotyledonous wetland species with contrasting types of aerenchyma. Plant Cell Environ 23:1237–1245
Wada K, Komiyama A, Ogino K (1987) Underground vertical distributions of macro fauna and root in a mangrove forest of southern Thailand. Publication of the Seto Marine Biological Laboratory, vol 32, pp 329–333
Waditee R, Hibino T, Tanaka Y, Nakamura T, Incharoensakdi A, Hayakawa S et al (2002) Functional characterization of betaine/proline transporters in betaine-accumulating mangrove. J Biol Chem 277:18373–18382
Walters BB, Ronnback P, Kovacs JM, Crona B, Hussain SA, Badola R, Primavera JH, Barbier E, Dahdouh-Guebas F (2008) Ethnobiology, socio-economics and management of mangrove forests: a review. Aquat Bot 89:220–236
Wang W, Yan Z, You S, Zhang Y, Chen L, Lin G (2011) Mangroves: obligate or facultative halophytes? A review. Trees Struct Funct 25:953–963
Wang HM, Xiao XR, Yang MY, Gao ZL, Jian Z, Fu XM, Chen YH (2014) Effects of salt stress on antioxidant defense system in the root of Kandelia candel. Bot Stud 55:57–63
Wen-jiao Z, Xiao-yong C, Peng L (1997) Accumulation and biological cycling of heavy metal elements in Rhizophora stylosa mangroves in Yingluo Bay, China. Mar Ecol Prog 159:293–301
Werner A, Stelzer R (1990) Physiological responses of the mangrove Rhizophora mangle grown in the absence and presence of NaCl. Plant Cell Environ 13:243–255
Wong YY, Ho CL, Nguyen PD, Teo SS, Harikrishna JA, Rahim RA, Wong MCVL (2007) Isolation of salinity tolerant genes from the mangrove plant, Bruguiera cylindrica by using suppression subtractive hybridization (SSH) and bacterial functional screening. Aquat Bot 86:117–122
Wu C, Gao X, Kong X, Zhao Y, Zhang H (2009) Molecular cloning and functional analysis of a Na+/H+antiporter gene ThNHX1 from a halophytic plant Thellungiella halophila. Plant Mol Biol Rep 27:1–12
Yabuki K, Kitaya Y, Sugi J (1985) Studies on the function of the mangrove pneumatophore. In: Sugi J (ed) Studies on the mangrove ecosystem. Tokyo Institute of Agriculture, Toyko, pp 76–79
Yanez-Espinosa L, Flores J (2011) A review of sea-level rise effect on mangrove forest species: anatomical and morphological modifications. In: Casalegno S (ed) Global warming impacts—case studies on the economy, human health, and on urban and natural environments. InTech, Rijeka
Young TP, Perkocha V (1994) Tree falls, crown asymmetry and buttresses. J Ecol 82:319–324
Youssef T, Saenger P (1996) Anatomical adaptive strategies to flooding and rhizosphere oxidation in mangrove seedlings. Aust J Bot 44:297–313
Zhila H, Mahmood H, Rozainah MZ (2014) Biodiversity and biomass of a natural and degraded mangrove forest of Peninsular Malaysia. Environ Earth Sci 71:4629–4635
Zhu Z, Chen J, Zheng HL (2012) Physiological and proteomic characterization of salt tolerance in a mangrove plant, Bruguiera gymnorrhiza (L.) Lam. Tree Physiol. doi:10.1093/treephys/tps097
Zimmermann U, Zhu JJ, Meinzer FC, Goldstein G et al (1994) High molecular weight organic compounds in the xylem sap of mangroves: implications for long-distance water transport. Bot Acta 107:218–229
Zimmermann U, Wagner HJ, Heidecker M, Mimietz S, Schneider H, Szimtenings M, Haase A, Mitlohner R, Kruck W, Hoffmann R, Konig W (2002) Implications of mucilage on pressure bomb measurements and water lifting in trees rooting in high-salinity water. Trees 16:100–111
Acknowledgments
Thanks to National Institute of Education, Nanyang Technological University, Singapore, for providing the research fund to the project AcRF RI 3/13 CZ and Dr. F. Berger for proofreading.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by K. Noguchi and T. Koike.
Rights and permissions
About this article
Cite this article
Srikanth, S., Lum, S.K.Y. & Chen, Z. Mangrove root: adaptations and ecological importance. Trees 30, 451–465 (2016). https://doi.org/10.1007/s00468-015-1233-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-015-1233-0