A patchy growth via successive and simultaneous cambia: key to success of the most widespread mangrove species Avicennia marina?

Abstract

Background and aims: Secondary growth via successive cambia has been intriguing researchers for decades. Insight into the mechanism of growth layer formation is, however, limited to the cellular level. The present study aims to clarify secondary growth via successive cambia in the mangrove species Avicennia marina on a macroscopic level, addressing the formation of the growth layer network as a whole. In addition, previously suggested effects of salinity on growth layer formation were reconsidered.

Methods: A 1-year cambial marking experiment was performed on 80 trees from eight sites in two mangrove forests in Kenya. Environmental (soil water salinity and nutrients, soil texture, inundation frequency) and tree characteristics (diameter, height, leaf area index) were recorded for each site. Both groups of variables were analysed in relation to annual number of growth layers, annual radial increment and average growth layer width of stem discs.

Key results: Between trees of the same site, the number of growth layers formed during the 1-year study period varied from only part of a growth layer up to four growth layers, and was highly correlated to the corresponding radial increment (0-5 mm year(-1)), even along the different sides of asymmetric stem discs. The radial increment was unrelated to salinity, but the growth layer width decreased with increasing salinity and decreasing tree height.

Conclusions: A patchy growth mechanism was proposed, with an optimal growth at distinct moments in time at different positions around the stem circumference. This strategy creates the opportunity to form several growth layers simultaneously, as observed in 14 % of the studied trees, which may optimize tree growth under favourable conditions. Strong evidence was provided for a mainly endogenous trigger controlling cambium differentiation, with an additional influence of current environmental conditions in a trade-off between hydraulic efficiency and mechanical stability.

Fig. 1.

Climate diagram of Mombasa (39°36'E, 4°0'S) adapted from Lieth et al. (1999), showing the long (April–July) and short (October–November) rainy season and one distinct dry season (January–February). The precipitation axis is reduced to one-tenth scale above the dotted horizontal line.

Fig. 2.

Macro- and microscopic characteristics of Avicennia marina stem wood after wounding the cambium with a needle of 1·2 mm diameter. (A) Pinhole encircled by wound periderm, scale bar = 1 cm. (B, C) Detail of sanded stem discs showing (B) a decreased vessel density and vessel diameter in the zone around the pinhole, marking the time of cambial wounding, and (C) a double cambial wound illustrating the simultaneous formation of the two growth layers. Scale bars = 1 mm. P, phloem band; Pd, periderm; X, xylem band. Arrows, radial increment from May 2005 to June 2006. Small arrows, part of the growth layer already formed at the time of cambial wounding. Asterisks, pinhole.

Fig. 3.

Transverse microsections of the stem wood of Avicennia marina after wounding the cambium with a needle. (A) Microscopic wood structure after wounding of the two outermost cambia. Scale bar = 1 mm. (B) Detail of two phloem strands located inward from the pinhole showing a coating of the cells and an induced meristem (arrowhead) in the right and left phloem strand, respectively. Scale bar = 500 µm. P, phloem band; PA, parenchyma; Pd, periderm; Ps, phloem strand; Sc, sclereids; X, xylem band. Arrows, radial increment from February 2006 to June 2006. Small arrows, part of the growth layer already formed at the time of cambial marking. Asterisks, pinhole.

Fig. 4.

Networking pattern of the growth layers in the (A) transverse and (B) longitudinal plane as visualized by a CT scan of a tree stem portion of 7 cm diameter (Tw57798, Tervuren xylarium). Circles indicate the positions of branching phloem bands.

Fig. 5.

Number of growth layers of 79 Avicennia marina trees formed in the period from May 2005 to June 2006 (A), distribution of the annual growth layer number over the eight study sites (B) (see also Table 2). Line, mean; box, s.d.; whiskers, min.-max.