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

Abstract

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.

Keywords: Avicennia marina; hydraulic anatomy; mangrove; obligate halophyte; plant growth; salinity.

Fig. 1.

Variation along a salinity gradient in (A) total dry mass of A. marina seedlings at the beginning of the experiment and at harvest, and (B) biomass allocation to roots, stems and leaves (see key). Values are means, n = 5; the bar in (A) shows the least significant difference between means at the 5 % level (LSD). P value indicates the overall effect of salinity.

Fig. 2.

Total leaf area in A. marina seedlings grown along a salinity gradient. Values are means, n = 5; the bar shows the least significant difference between means at the 5 % level (LSD). P value indicates the overall effect of salinity.

Fig. 3.

RGR (A), average LAR during growth (B) and NAR (C) of A. marina seedlings grown along a salinity gradient. Values are means, n = 5; the bar shows the least significant difference between means at the 5 % level (LSD). P value in each panel indicates the overall effect of salinity.

Fig. 4.

Gas exchange characteristics of leaves of A. marina grown along a salinity gradient. (A) CO₂ assimilation rate. (B) Stomatal conductance – g_s. Inset shows CO₂ assimilation rate as a function of stomatal conductance. Line drawn by linear regression. (C) Evaporation rate, E. Inset shows CO₂ assimilation rate as a function of evaporation rate. Line drawn by linear regression. Values are means, n = 5; bars show least significant differences between means at the 5 % level (LSD). P value in each panel indicates the overall effect of salinity. Each point in an inset is from an individual plant. Symbols indicate salinities (per cent seawater) in which the plants were grown, as indicated in the key in (B).

Fig. 5.

Transverse sections of stems of A. marina grown in (A) 0 % and (B) 75 % seawater. Sections were stained with Alcian blue and Safranin O. Each panel shows a sector of the stem from the pith through the first two vascular rings, each containing both xylem and phloem. The first or inner-most ring was grown prior to the experiment when seedlings were in 50 % seawater. The second or outer-most ring formed while seedlings grew in the experimental treatments. Abbreviations: arrow, xylem vessel; Ph, phloem; asterisks (***), successive cambia; F, fibres; P, pith. Scale bar = 50 µm.

Fig. 6.

Xylem vessel characteristics in the second vascular ring of stems of A. marina seedlings grown along a salinity gradient. (A) Total lumen area, (B) vessel density, (C) vessel diameter, and (D) sum of the 4th power of vessel radii presented in per cent of the maximum value. Values are means, n = 5; bars show least significant differences between means at the 5 % level (LSD). P value in each panel indicates the overall effect of salinity.

Fig. 7.

Huber value of A. marina seedlings grown along a salinity gradient. Values are means, n = 5; bar shows least significant difference between means at the 5 % level (LSD). P value indicates the overall effect of salinity.

Fig. 8.

Area of individual leaves in A. marina seedlings grown along a salinity gradient ranging from 25 to 100 % seawater. Values are means ± s.e., n = 5. Inset shows leaf area as a function of total number of midvein vessels. Each point is from an individual plant. Line drawn by linear regression. Symbols indicate salinity (per cent seawater) in which the plants were grown, as indicated in the key.