Elisabeth M. R. Robert

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.

A tree-centered approach to assess impacts of extreme climatic events on forests

A major task of our society is to manage forests in a way that their resources are preserved to meet future generation needs (Forest Europe et al., 2015). Current scenarios of climate change effects are making this task extremely challenging (Kirilenko and Sedjo, 2007). Climate shifts will impact forest vitality and affect goods and services forests provide, including carbon sequestration and climate change mitigation (IPCC, 2014). To guide sustainable forest management, forest researchers are asked to provide concrete answers about forest resilience in response to expected climatic trends, and extreme climatic events (Lindner et al., 2014). This is not an easy task, because responses of trees and forest ecosystems to environmental conditions are often non-linear and moreover vary on spatial and temporal scales (Smith, 2011; Anderegg et al., 2012; Reichstein et al., 2013). For instance, although drought is one of the most frequent and widespread climatic extremes affecting forests worldwide (e.g., Allen et al., 2010), the assessment of its impact on future forests is currently under intense debate. Mechanisms behind tree growth and mortality are complex (McDowell et al., 2008, 2011; Fatichi et al., 2014; Anderegg et al., 2015; Meir et al., 2015). Besides strength or frequency of external factors, such as extreme events, also the trees ability to resist and recover is relevant, which, in turn, is largely determined by intrinsic factors such as the trees life stage, life history, and genetic characteristics. In this paper, we advocate for a tree-centered approach. By providing an improved mechanistic understanding of physiological and growth responses of trees growing under various conditions we can define the trees capacity to respond to external stress factors. This concept can valuably contribute to the debate on how to shape future forests toward resilient forest ecosystems.

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.

Osmolality and Non-Structural Carbohydrate Composition in the Secondary Phloem of Trees across a Latitudinal Gradient in Europe.

Phloem osmolality and its components are involved in basic cell metabolism, cell growth, and in various physiological processes including the ability of living cells to withstand drought and frost. Osmolality and sugar composition responses to environmental stresses have been extensively studied for leaves, but less for the secondary phloem of plant stems and branches. Leaf osmotic concentration and the share of pinitol and raffinose among soluble sugars increase with increasing drought or cold stress, and osmotic concentration is adjusted with osmoregulation. We hypothesize that similar responses occur in the secondary phloem of branches. We collected living bark samples from branches of adult Pinus sylvestris, Picea abies, Betula pendula and Populus tremula trees across Europe, from boreal Northern Finland to Mediterranean Portugal. In all studied species, the observed variation in phloem osmolality was mainly driven by variation in phloem water content, while tissue solute content was rather constant across regions. Osmoregulation, in which osmolality is controlled by variable tissue solute content, was stronger for Betula and Populus in comparison to the evergreen conifers. Osmolality was lowest in mid-latitude region, and from there increased by 37% toward northern Europe and 38% toward southern Europe due to low phloem water content in these regions. The ratio of raffinose to all soluble sugars was negligible at mid-latitudes and increased toward north and south, reflecting its role in cold and drought tolerance. For pinitol, another sugar known for contributing to stress tolerance, no such latitudinal pattern was observed. The proportion of sucrose was remarkably low and that of hexoses (i.e., glucose and fructose) high at mid-latitudes. The ratio of starch to all non-structural carbohydrates increased toward the northern latitudes in agreement with the build-up of osmotically inactive C reservoir that can be converted into soluble sugars during winter acclimation in these cold regions. Present results for the secondary phloem of trees suggest that adjustment with tissue water content plays an important role in osmolality dynamics. Furthermore, trees acclimated to dry and cold climate showed high phloem osmolality and raffinose proportion.

Flood-Ring Formation and Root Development in Response to Experimental Flooding of Young Quercus robur Trees

Spring flooding in riparian forests can cause significant reductions in earlywood-vessel size in submerged stem parts of ring-porous tree species, leading to the presence of ‘flood rings’ that can be used as a proxy to reconstruct past flooding events, potentially over millennia. The mechanism of flood-ring formation and the relation with timing and duration of flooding are still to be elucidated. In this study, we experimentally flooded 4-year-old Quercus robur trees at three spring phenophases (late bud dormancy, budswell, and internode expansion) and over different flooding durations (2, 4, and 6 weeks) to a stem height of 50 cm. The effect of flooding on root and vessel development was assessed immediately after the flooding treatment and at the end of the growing season. Ring width and earlywood-vessel size and density were measured at 25- and 75-cm stem height and collapsed vessels were recorded. Stem flooding inhibited earlywood-vessel development in flooded stem parts. In addition, flooding upon budswell and internode expansion led to collapsed earlywood vessels below the water level. At the end of the growing season, mean earlywood-vessel size in the flooded stem parts (upon budswell and internode expansion) was always reduced by approximately 50% compared to non-flooded stem parts and 55% compared to control trees. This reduction was already present 2 weeks after flooding and occurred independent of flooding duration. Stem and root flooding were associated with significant root dieback after 4 and 6 weeks and mean radial growth was always reduced with increasing flooding duration. By comparing stem and root flooding, we conclude that flood rings only occur after stem flooding. As earlywood-vessel development was hampered during flooding, a considerable number of narrow earlywood vessels present later in the season, must have been formed after the actual flooding events. Our study indicates that root dieback, together with strongly reduced hydraulic conductivity due to anomalously narrow earlywood vessels in flooded stem parts, contribute to reduced radial growth after flooding events. Our findings support the value of flood rings to reconstruct spring flooding events that occurred prior to instrumental flood records.

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.

Effects of experimental sedimentation on the phenological dynamics and leaf traits of replanted mangroves at Gazi bay, Kenya

Sedimentation results in the creation of new mudflats for mangroves to colonize among other benefits. However, large sediment input in mangrove areas may be detrimental to these forests. The dynamics of phenological events of three mangrove tree species (Avicennia marina, Ceriops tagal, and Rhizophora mucronata) were evaluated under experimental sediment burial simulating sedimentation levels of 15, 30, and 45 cm. While there was generally no shift in timing of phenological events with sedimentation, the three mangrove tree species each responded differently to the treatments. Partially buried A. marina trees produced more leaves than the controls during the wet season and less during the dry season. Ceriops tagal on the other hand had higher leaf loss and low replacement rates in the partially buried trees during the first 6 months of the experiment but adapted with time, resulting in either equal or higher leaf emergence rates than the controls. Rhizophora mucronata maintained leaf emergence and loss patterns as the unaffected controls but had a higher fecundity and productivity in the 15-cm sedimentation level. The results suggest that under incidences of large sedimentation events (which could be witnessed as a result of climate change impacts coupled with anthropogenic disturbances), mangrove trees may capitalize on “advantages” associated with terrestrial sediment brought into the biotope, thus maintaining the pattern of phenological events.

The Anatomy and Functioning of the Xylem in Oaks

Because of its economic and ecological importance, the genus Quercus has been relatively intensively studied for its anatomical and hydraulic characteristics, having often been testing ground for development of methods and hypotheses related to tree structure and function. However, despite long-withstanding interest, we are still far from having obtained a clear understanding of the hydraulic functioning of the species within this genus, the occurrence of trade-offs among various xylem properties and the prevalence of syndromes of characters under different environmental conditions. We conducted a review of the xylem anatomical literature of the genus Quercus , an undertaking that does not appear to have been carried out before. We also updated existing quantitative databases of vessel diameter and density, volumetric fractions of parenchyma, wood density and xylem hydraulic properties, to synthesise the main patterns of variation in the hydraulic architecture and functioning of the genus. We found that ring-porous (deciduous) species have lower wood density, higher hydraulic conductivity, xylem that is more vulnerable to embolism and lower Huber values compared to diffuse-porous (evergreen) species. We also report systematic differences among taxonomic groups, with species of sections Quercus and Lobatae having smaller but more numerous vessels, lower wood density, more vulnerable xylem, higher conductivity and lower Huber values as opposed to species of section Cerris . Many of these trends appeared to map onto environmental differences across the three main biomes where Quercus species are found, i.e. the temperate, the Mediterranean/semi-arid and the tropical biomes. Although limited by the coverage of the empirical data, our compilation contributes to characterise the hydraulic architecture and functioning of the genus as a function of taxonomic grouping, biome, ring-porosity and leaf phenology . Future investigations can benefit by the identification of the main factors responsible for these patterns and their likely ecological significance.

Wide Ranging Insect Infestation of the Pioneer Mangrove Sonneratia alba by Two Insect Species along the Kenyan Coast.

Insect infestation of mangroves currently threatens mangrove forest health and management. In the Western Indian Ocean region, little is known about insect damage to mangroves despite the fact that numerous infestations have occurred. In Kenya, infestations of Sonneratia alba have persisted for almost two decades, yet the taxonomic identity of the infesting pest(s), the extent of infestation, the pests’ biology, the impacts of infestation on host and the ecosystem, the host’s defensive strategies to the infestation are poorly understood. S. alba is a ubiquitous, pioneer mangrove species of the Indo-Pacific, occurring along the waterfront in a variety of mangrove ecosystem settings. Our main objectives were to identify the pest(s) responsible for the current dieback of S. alba in Kenya, and to determine the extent of infestation. To identify the pests responsible for infestation, we trapped emergent insects and reared larvae in the laboratory. To determine the overall extent of infestation within the S. alba zone, we assessed nine sites along the entire Kenyan coastline for the presence or absence of infested mangroves. Insect infestation in two mangrove embayments (Gazi and Mida) was quantified in depth. Two wood-boring insects were identified: a metarbelid moth (Lepidoptera, Cossoidea) of undescribed genus and the beetle Bottegia rubra (Cerambycidae, Lamiinae).The metarbelid moth infests mangroves in both northern (from Ngomeni to Kiunga) and southern regions (from Vanga to Mtwapa) of the Kenyan coast. B. rubra appeared in low density in Gazi, and in high density in Mida, Kilifi, and Ngomeni, with densities gradually decreasing northward. Insect infestation levels reached 18% in Gazi and 25% of S. alba stands in Mida. Our results indicate that B. rubra has the ability to infest young mangrove trees and expand its range, posing a danger to rehabilitation efforts where plantations have been established. Thus, there is great need for forest managers to address the recent increased levels of infestation in Kenyan mangroves; apart from the ecological interest such plant-herbivore relations bring in this ecosystem.

Rhizophoraceae Mangrove Saplings Use Hypocotyl and Leaf Water Storage Capacity to Cope with Soil Water Salinity Changes

Some of the most striking features of Rhizophoraceae mangrove saplings are their voluminous cylinder-shaped hypocotyls and thickened leaves. The hypocotyls are known to serve as floats during seed dispersal (hydrochory) and store nutrients that allow the seedling to root and settle. In this study we investigate to what degree the hypocotyls and leaves can serve as water reservoirs once seedlings have settled, helping the plant to buffer the rapid water potential changes that are typical for the mangrove environment. We exposed saplings of two Rhizophoraceae species to three levels of salinity (15, 30, and 0–5‰, in that sequence) while non-invasively monitoring changes in hypocotyl and leaf water content by means of mobile NMR sensors. As a proxy for water content, changes in hypocotyl diameter and leaf thickness were monitored by means of dendrometers. Hypocotyl diameter variations were also monitored in the field on a Rhizophora species. The saplings were able to buffer rapid rhizosphere salinity changes using water stored in hypocotyls and leaves, but the largest water storage capacity was found in the leaves. We conclude that in Rhizophora and Bruguiera the hypocotyl offers the bulk of water buffering capacity during the dispersal phase and directly after settlement when only few leaves are present. As saplings develop more leaves, the significance of the leaves as a water storage organ becomes larger than that of the hypocotyl.