Nele Schmitz

Successive Cambia: A Developmental Oddity or an Adaptive Structure?

Background Secondary growth by successive cambia is a rare phenomenon in woody plant species. Only few plant species, within different phylogenetic clades, have secondary growth by more than one vascular cambium. Often, these successive cambia are organised concentrically. In the mangrove genus Avicennia however, the successive cambia seem to have a more complex organisation. This study aimed (i) at understanding the development of successive cambia by giving a three-dimensional description of the hydraulic architecture of Avicennia and (ii) at unveiling the possible adaptive nature of growth by successive cambia through a study of the ecological distribution of plant species with concentric internal phloem. Results Avicennia had a complex network of non-cylindrical wood patches, the complexity of which increased with more stressful ecological conditions. As internal phloem has been suggested to play a role in water storage and embolism repair, the spatial organisation of Avicennia wood could provide advantages in the ecologically stressful conditions species of this mangrove genus are growing in. Furthermore, we could observe that 84.9% of the woody shrub and tree species with concentric internal phloem occurred in either dry or saline environments strengthening the hypothesis that successive cambia provide the necessary advantages for survival in harsh environmental conditions. Conclusions Successive cambia are an ecologically important characteristic, which seems strongly related with water-limited environments.

Growth responses of the mangrove Avicennia marina to salinity: development and function of shoot hydraulic systems require saline conditions

BACKGROUND AND AIMS Halophytic eudicots are characterized by enhanced growth under saline conditions. This study combines physiological and anatomical analyses to identify processes underlying growth responses of the mangrove Avicennia marina to salinities ranging from fresh- to seawater conditions. METHODS Following pre-exhaustion of cotyledonary reserves under optimal conditions (i.e. 50% seawater), seedlings of A. marina were grown hydroponically in dilutions of seawater amended with nutrients. Whole-plant growth characteristics were analysed in relation to dry mass accumulation and its allocation to different plant parts. Gas exchange characteristics and stable carbon isotopic composition of leaves were measured to evaluate water use in relation to carbon gain. Stem and leaf hydraulic anatomy were measured in relation to plant water use and growth. KEY RESULTS Avicennia marina seedlings failed to grow in 0-5% seawater, whereas maximal growth occurred in 50-75% seawater. Relative growth rates were affected by changes in leaf area ratio (LAR) and net assimilation rate (NAR) along the salinity gradient, with NAR generally being more important. Gas exchange characteristics followed the same trends as plant growth, with assimilation rates and stomatal conductance being greatest in leaves grown in 50-75% seawater. However, water use efficiency was maintained nearly constant across all salinities, consistent with carbon isotopic signatures. Anatomical studies revealed variation in rates of development and composition of hydraulic tissues that were consistent with salinity-dependent patterns in water use and growth, including a structural explanation for low stomatal conductance and growth under low salinity. CONCLUSIONS The results identified stem and leaf transport systems as central to understanding the integrated growth responses to variation in salinity from fresh- to seawater conditions. Avicennia marina was revealed as an obligate halophyte, requiring saline conditions for development of the transport systems needed to sustain water use and carbon gain.

Light‐dependent maintenance of hydraulic function in mangrove branches: do xylary chloroplasts play a role in embolism repair?

• To clarify the role of branch photosynthesis in tree functioning, the presence and function of chloroplasts in branch xylem tissue were studied in a diverse range of mangrove species growing in Australia. • The presence of xylary chloroplasts was observed via chlorophyll fluorescence of transverse sections. Paired, attached branches were selected to study the effects of covering branches with aluminium foil on the gas exchange characteristics of leaves and the hydraulic conductivity of branches. • Xylary chloroplasts occurred in all species, but were differently distributed among living cell types in the xylem. Covering stems altered the gas exchange characteristics of leaves, such that water-use efficiency was greater in exposed leaves of covered than of uncovered branches. • Leaf-specific hydraulic conductivity of stems was lower in covered than in uncovered branches, implicating stem photosynthesis in the maintenance of hydraulic function. Given their proximity to xylem vessels, we suggest that xylary chloroplasts may play a role in light-dependent repair of embolized xylem vessels.

NATURE AND PERIODICITY OF GROWTH RINGS IN TWO BANGLADESHI MANGROVE SPECIES

SUMMARY Nature and periodicity of growth rings were investigated in Sonneratia apetala and Heritiera fomes, two Bangladeshi mangrove species. From both species we collected three stem discs in the natural forest reserve of the Sundarbans. In addition, three discs were sampled from plantation-grown S. apetala trees of known age. Sanded stem discs revealed distinct growth rings but no periodic fluctuations in vessel variables (vessel density, vessel diameter, vessel grouping), which were measured at high resolution along a transect from pith to bark. The number of growth rings in plantation-grown S. apetala trees corresponded with the documented tree age, hence strongly suggesting the growth rings to be annual. Within species, the annual nature of the rings was further supported by a good match between the tree-ring series. The similar mean curves of S. apetala and H. fomes, growing at the same site in the Sundarbans, pointed to the presence of an external factor influencing their growth. A combination of precipitation and temperature was suggested influencing substrate salinity and phenological events. It became evident that tree-ring research in combination with the analysis of vessel patterns is a valuable tool to further investigate the complex interactions between tree growth and site ecology in mangrove forests.

Variation in wood density and anatomy in a widespread mangrove species

Wood density is an important plant trait that influences a range of ecological processes, including resistance to damage and growth rates. Wood density is highly dependent on anatomical characteristics associated with the conductive tissue of trees (xylem and phloem) and the fibre matrix in which they occur. Here, we investigated variation in the wood density of the widespread mangrove species Avicennia marina in the Exmouth Gulf in Western Australia and in the Firth of Thames in New Zealand. We assessed how variation in xylem vessel size, fibre wall thickness and proportion of phloem within the wood contributed to variation in wood density and how these characteristics were linked to growth rates. We found the wood density of A. marina to be higher in Western Australia than in New Zealand and to be higher in taller seaward fringing trees than in scrub trees growing high in the intertidal. At the cellular level, high wood density was associated with large xylem vessels and thick fibre walls. Additionally, wood density increased with decreasing proportions of phloem per growth layer of wood. Tree growth rates were positively correlated with xylem vessel size and wood density. We conclude that A. marina can have large xylem vessel sizes and high growth rates while still maintaining high wood density because of the abundance and thickness of fibres in which vessels are found.

Using expert knowledge and modeling to define mangrove composition, functioning, and threats and estimate time frame for recovery

Mangroves are threatened worldwide, and their loss or degradation could impact functioning of the ecosystem. Our aim was to investigate three aspects of mangroves at a global scale: (1) their constituents (2) their indispensable ecological functions, and (3) the maintenance of their constituents and functions in degraded mangroves. We focused on answering two questions: “What is a mangrove ecosystem” and “How vulnerable are mangrove ecosystems to different impacts”? We invited 106 mangrove experts globally to participate in a survey based on the Delphi technique and provide inputs on the three aspects. The outputs from the Delphi technique for the third aspect, i.e. maintenance of constituents and functions were incorporated in a modeling approach to simulate the time frame for recovery. Presented here for the first time are the consensus definition of the mangrove ecosystem and the list of mangrove plant species. In this study, experts considered even monospecific (tree) stands to be a mangrove ecosystem as long as there was adequate tidal exchange, propagule dispersal, and faunal interactions. We provide a ranking of the important ecological functions, faunal groups, and impacts on mangroves. Degradation due to development was identified as having the largest impact on mangroves globally in terms of spatial scale, intensity, and time needed for restoration. The results indicate that mangroves are ecologically unique even though they may be species poor (from the vegetation perspective). The consensus list of mangrove species and the ranking of the mangrove ecological functions could be a useful tool for restoration and management of mangroves. While there is ample literature on the destruction of mangroves due to aquaculture in the past decade, this study clearly shows that more attention must go to avoiding and mitigating mangrove loss due to coastal development (such as building of roads, ports, or harbors).

How to catch the patch? A dendrometer study of the radial increment through successive cambia in the mangrove Avicennia

BACKGROUND AND AIMS Successive vascular cambia are involved in the secondary growth of at least 200 woody species from >30 plant families. In the mangrove Avicennia these successive cambia are organized in patches, creating stems with non-concentric xylem tissue surrounded by internal phloem tissue. Little is known about radial growth and tree stem dynamics in trees with this type of anatomy. This study aims to (1) clarify the process of secondary growth of Avicennia trees by studying its patchiness; and (2) study the radial increment of Avicennia stems, both temporary and permanent, in relation to local climatic and environmental conditions. A test is made of the hypothesis that patchy radial growth and stem dynamics enable Avicennia trees to better survive conditions of extreme physiological drought. Methods Stem variations were monitored by automatic point dendrometers at four different positions around and along the stem of two Avicennia marina trees in the mangrove forest of Gazi Bay (Kenya) during 1 year. KEY RESULTS Patchiness was found in the radial growth and shrinkage and swelling patterns of Avicennia stems. It was, however, potentially rather than systematically present, i.e. stems reacted either concentrically or patchily to environment triggers, and it was fresh water availability and not tidal inundation that affected radial increment. CONCLUSIONS It is concluded that the ability to develop successive cambia in a patchy way enables Avicennia trees to adapt to changes in the prevailing environmental conditions, enhancing its survival in the highly dynamic mangrove environment. Limited water could be used in a more directive way, investing all the attainable resources in only some locations of the tree stem so that at least at these locations there is enough water to, for example, overcome vessel embolisms or create new cells. As these locations change with time, the overall functioning of the tree can be maintained.

The anatomical basis of the link between density and mechanical strength in mangrove branches

Tree branches are important as they support the canopy, which controls photosynthetic carbon gain and determines ecological interactions such as competition with neighbours. Mangrove trees are subject to high wind speeds, strong tidal flows and waves that can damage their branches. The survival and establishment of mangroves partly depend on the structural and mechanical characteristics of their branches. In addition, mangroves are exposed to soils that vary in salinity. Highly saline conditions can increase the tension in the water column, imposing mechanical stresses on the xylem vessels. Here, we investigated how mechanical strength, assessed as the modulus of elasticity (MOE) and the modulus of rupture (MOR), and density relate to the anatomical characteristics of intact mangrove branches from southeast Queensland and whether the mechanical strength of branches varies among mangrove species. Mechanical strength was positively correlated with density of mangrove intact branches. Mechanical strength (MOE) varied among species, with Avicennia marina (Forssk.) Vierh. branches having the highest mechanical strength (2079±176MPa), and Rhizophora stylosa Griff. and Bruguiera gymnorrhiza (L.) Savigny ex Lam. and Poiret having the lowest mechanical strength (536.8±39.2MPa in R. stylosa and 554±58.2MPa in B. gymnorrhiza). High levels of mechanical strength were associated with reductions in xylem vessel lumen area, pith content and bark content, and positively associated with increases in fibre wall thickness. The associations between mechanical strength and anatomical characteristics in mangrove branches suggest trade-offs between mechanical strength and water supply, which are linked to tree growth and survival.

A Structural and Compositional Analysis of Intervessel pit Membranes in the Sapwood of some Mangrove Woods

Intervessel pits are prominent wall structures involved in the water transport mechanism of land plants. The role of their intra-tree variation in the regulation of water transport, however, remains enigmatic. The hypothesis was tested that pit membrane thickness and degree of impregnation with phenolic substances increase along the stem axis with increasing tension on the water column as an adaptation to the higher risk for cavitation. Wood samples were taken at different heights from the mangrove tree Rhizophora mucronata growing at Gazi Bay (Kenya). Additional samples were taken along the stem radius to distinguish height from age effect, and from six other mangrove species growing in the same forest. Intervessel pit membranes were studied via transmission and scanning electron microscopy and cellular UV-microspectrophotometry. The hypothesis of pit membrane thickness and composition as a static adaptation to the hydrostatic conditions during vessel differentiation could be refuted. Instead, our findings point to a more dynamic pit membrane appearance with seasonal changes in thickness and chemical composition.

Differential responses of the mangrove Avicennia marina to salinity and abscisic acid

Salinisation of the soil can cause plant water deficits, ion and nutrient imbalances and toxic reactions. The halophyte, Avicennia marina (Forssk.) Vierh., is a mangrove that tolerates a wide range of soil salinities. In order to understand how salinity affects plant growth and functioning and how salinity responses are influenced by the water deficit signalling hormone abscisic acid (ABA) we grew A. marina seedlings under two non-growth limiting salinities: 60% seawater and 90% seawater and with and without exogenously supplied ABA. We measured growth, photosynthesis, sap flow, aquaporin gene expression, hydraulic anatomy and nutrient status as well as sap ABA concentrations. ABA addition resulted in a drought phenotype (reduced sap flow, transpiration rates and photosynthesis and increased water use efficiency and aquaporin expression). In contrast, growth in high salinity did not lead to responses that are typical for water deficits, but rather, could be characterised as drought avoidance strategies (no reduction in sap flow, transpiration rates and photosynthesis and reduced aquaporin expression). Tissue nutrient concentrations were higher in seedlings grown at high salinities. We did not find evidence for a role for ABA in the mangrove salinity response, suggesting ABA is not produced directly in response to high concentrations of NaCl ions.