Successive cambia: a developmental oddity or an adaptive structure?

Abstract

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.

Figure 1. Spatial structure of the xylem and phloem tissue in Avicennia in comparison to other trees.

Schematic view of a stem disc from (a) a tree with only one cambium, (b) a tree with successive cambia organised in concentric cylinders, giving rise to a stem disc with concentric circles of xylem tissue, phloem tissue and cambium circles and (c) Avicennia, having a reticulate organisation of its cambia and transport structure. The spatial structure of Avicennia is depicted by smoothed surface images after three-dimensional reconstruction in Reconstruct (d,e). Only a small part of the xylem tissue has been visualised. It can be seen that Avicennia had a complex network of xylem patches that fused at certain heights of the tree and joined different patches at other parts of the stem. The connections between xylem patches changed rapidly with vertical distance. This is shown by the white arrowheads in the four serial micro-CT-scan images of an outside zone of an Avicennia marina stem disc, produced by a SkyScan 1172 scanner (g-k). Each section is 150 µm apart from the previous. On the micro-CT-images (g-k) the wide light grey bands are xylem tissue while the dark small strings are phloem tissue. The complexity of the internal structure can be expressed by the sum of the locations of free ending and branched phloem tissue (f) per stem disc surface area.

Figure 2. Characteristics of the spatial network of the transport system in Avicennia.

(a) Ratio of ending to branched phloem in function of the biogeographical mangrove regions; (b) Degree of branching of the transport network of Avicennia marina in function of the study site (Table 2); (c–d) Ratio of phloem surface area to wood surface area in function of the mangrove species (c) and in function of the study site (Table 2) for A. marina (d). Lines: medians. Different letters indicate significant differences.

Figure 3. Degree of branching of the internal transport structure of Avicennia in function of tree height.

Data are from one Avicennia marina tree from Gazi Bay (Kenya). Lines: medians; W: main root of the same tree; W*: main root of another A. marina tree from a different study site in the same mangrove forest.

Figure 4. Nature of the successive cambia in Avicennia: two models.

(a) Model of the fishnet stockings: multiple non-continuous cambial sheets give rise to the reticulate transport system. (b) Model of the broken cylinders: complete cambium shields have the ability to break at certain locations and can eventually line up in a later state of the development of the transport structure. Only one cambial layer is shown in both visualisations.

Figure 5. From wood anatomy to ecology: overview of the study.

The flow chart is showing the organisms involved (black boxes, capital text) and the results of the study of successive cambia and concentric internal phloem in these organisms (white boxes, normal text) establishing that internal phloem could offer advantages in ecological stressful conditions (grey box with black frame). In this way, the wood anatomical features of Avicennia can help in explaining its broad distribution compared to other mangrove genera.