Effects of salinity on germination, seedling growth and ...

Aquatic Botany 83 (2005) 193–205 www.elsevier.com/locate/aquabot

Effects of salinity on germination, seedling growth and physiology of three salt-secreting mangrove species Yong Ye a,*, Nora Fung-Yee Tam b, Chang-Yi Lu a, Yuk-Shan Wong b a

State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, Fujian, China b Department of Biology and Chemistry, City University of Hong Kong, Kowloon, Hong Kong Received 2 August 2004; received in revised form 1 June 2005; accepted 22 June 2005

Abstract Propagules of three salt-secreting mangrove species, i.e. Acanthus ilicifolius L., Aegiceras corniculatum Blanco. and Avicennia marina (Forsk) Vierh., were germinated at salinities of 0, 5, 15, 25 and 35 parts per thousand (ppt). Their tolerance to salt stress was compared in terms of some parameters on germination, growth and physiology. Root initiations of Ae. corniculatum and Av. marina, two viviparous species, were about 3 and 6 d, respectively, not significantly affected by salinity, but those of Ac. ilicifolius, a non-viviparous species, were significantly delayed about 4 d at salinities over 25 ppt. Final seedling establishment percentages of Av. marina were 100% at all salinity treatments, while salinities over 25 ppt significantly reduced the values of Ae. corniculatum (28%) and Ac. ilicifolius (38%). As salinities increased from 0 to 35 ppt, decrease in relative growth rate (RGR) of Av. marina was only 5%, less than those of Ae. corniculatum (56%) and Ac. ilicifolius (70%). For each species, salt secretion from leaves increased with increases in salinity and the increases in salt secretion with every salinity increase of 10 ppt were about 0.9, 0.6 and 0.2 g m 2 d 1 for Av. marina, Ae. corniculatum and Ac. ilicifolius, respectively. When seedlings were cultured in fresh water, leaf tissue water of each species had salt concentrations around 2%, much higher than the environmental salinity (0 ppt). Under saline conditions from 5 to 35 ppt, salt concentrations in leaf tissue water of Av. marina maintained steady (4.3–5.0%), while the corresponding values increased from 2.4 to 4.5% in Ae. corniculatum and from 2.3 to 5.3% in Ac. ilicifolius. Evaporation and transpiration (evapo-transpiration) rates of these three species were similar under fresh water * Corresponding author. Fax: +86 592 2185622. E-mail address: [email protected] (Y. Ye). 0304-3770/$ – see front matter # 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.aquabot.2005.06.006

194

Y. Ye et al. / Aquatic Botany 83 (2005) 193–205

condition, but under saline conditions (5–35 ppt), Av. marina had significantly higher rates than Ac. ilicifolius and Ae. corniculatum. At salinities of 5–35 ppt, variations of evapo-transpiration were different between species with an order of Av. marina < Ae. corniculatum < Ac. ilicifolius. All of the parameters indicated that salt tolerance of the three salt-secreting mangrove species was in the descending order of Av. marina > Ae. corniculatum > Ac. ilicifolius. # 2005 Elsevier B.V. All rights reserved. Keywords: Acanthus ilicifolius; Aegiceras corniculatum; Avicennia marina; Salt tolerance; Growth; Salt secretion; Transpiration

1. Introduction Mangroves are distributed along inter-tidal coastlines and usually subjected to salt stress. It is well known that mangrove species can resist salt stress by excluding salt from entering the plant and some species can secrete salt through salt glands in leaves (Mizrachi et al., 1980; Tomlinson, 1986). In Hong Kong, eight mangrove species, i.e. Acanthus ilicifolius, Aegiceras corniculatum, Avicennia marina, Bruguiera gymnorrhiza, Excoecaria agallocha, Heritiera littoralis, Kandelia candel and Lumnitzera racemosa, are naturally distributed along the coastlines (Tam et al., 1997; Tam and Wong, 2002). Ac. ilicifolius, Ae. corniculatum and Av. marina have salt glands in leaves and are salt-secreting species. Many documents indicated that increases in salinity had significant impact on growth and/ or physiology of Ae. corniculatum and Av. marina, two viviparous species in which germination and subsequent development of the propagule took place while still on the mother tree. Following release of these propagules, the onset of further development into seedlings was maximum at salinity 3 ppt for Ae. corniculatum (Clarke and Hannon, 1970) and 15 ppt for Av. marina (Connor, 1969; Clarke and Hannon, 1970; Ball, 1988). It has been reported that moderate levels of salinity stimulated growth of Av. marina (Clarke and Hannon, 1970; Downton, 1982; Burchett et al., 1984; Clough, 1984) and Ae. corniculatum (Ball and Anderson, 1986). Burchett et al. (1989) found that both species had maximum growth in 25% seawater (9 ppt), but a number of growth parameters consistently revealed that Av. marina was the more salt-tolerant species than Ae. corniculatum as growth of Av. marina in tap water was similar to that in 100% seawater and growth of Ae. corniculatum was significantly lower in 100% seawater than in fresh water. Though the photosynthetic capacity of both species decreased with increase in salinity from 3 to 30 ppt (Ball and Farquhar, 1984), Av. marina was tolerant to salt stress due to its conservative water use characteristics (Ball, 1988). Some of the absorbed salts were retained in shoots for osmo-regulation and the remainder was secreted. Salt glands in leaves secrete a variety of ions and the secretion in Ae. corniculatum and Av. marina increased with increases in salinity (Ball, 1988). However, few reports have been found to compare their salt tolerance in terms of rates of root initiation and seedling establishment of propagules and salt-secreting characteristics of seedlings although Ball (1988) gave their salt balance. Furthermore, studies on salt tolerance of Ae. corniculatum and Av. marina have been done in South Africa and Australia but not in Southeast Asia, where these two species are widespread, although the tropical and subtropical populations showed different water use characteristics (Youssef and Saenger, 1998). Especially, there has been not any


195

experimental report on salinity tolerance of the non-viviparous mangrove species Ac. ilicifolius, another widespread salt-secreting species. These three species have obvious inter-tidal zonation in Hong Kong and the sequence of distribution from landward to seaward zones is Ac. ilicifolius, Ae. corniculatum and Av. marina (Tam and Wong, 2002), suggesting that the order of salt tolerance is Av. marina > Ae. corniculatum > Ac. ilicifolius. However, the experimental evidences have been still scanty. The present study, therefore, aims to compare the responses of the three salt-secreting mangrove species commonly distributed along coastlines of Hong Kong, Ac. ilicifolius, Ae. corniculatum and Av. marina, to different salinities (0–35 ppt) in terms of propagule germination, seedling growth, salt secretion, salt content in leaf tissues and evapotranspiration. We hypothesize that the order of salt tolerance is Av. marina > Ae. corniculatum > Ac. ilicifolius.

2. Materials and methods 2.1. Plant culture Mature propagules of three salt-secreting mangrove species, Ac. ilicifolius L., Ae. corniculatum Blanco. and Av. marina (Forsk) Vierh., were collected from mangroves along coastlines of Hong Kong. Ac. ilicifolius is non-viviparous and one mature fruit contains three to four seeds (propagules), each with weight of 0.015–0.020 g and size of about 1.5 cm long and 1.2 cm wide. Mature seeds have drier and thinner coats than the immature ones. Ae. corniculatum and Av. marina are crypto-viviparous species whose embryo emerges from the seed coat but not the fruit before it abscises and the whole fruit is considered one propagule or commonly known as a dropper (Tomlinson, 1986). Mature droppers of Ae. corniculatum are red and each weighs about 0.5 g and has a length of 3.5–5 cm and a diameter of 0.5 cm. One mature propagule of Av. marina weighs about 6.0 g and has large size of 2.0–3.0 cm long and 1.5–2.5 cm wide with more yellowish coat and flatter shape than immature one. For each species, nine mature propagules were planted in one plastic pot with about 350 g coastal sand washed thrice with tap water before planting. The pots were irrigated with artificial seawater (prepared by dissolving a commercial salt purchased from Instant Ocean, Aquarium Systems Inc., Mentor, OH) with different salinities of 0, 5, 15, 25 and 35 ppt and the sand surface was exactly covered by seawater. For each salinity and species, triplicate pots were set up. Water level in each pot was maintained by daily addition of tap water to compensate evapo-transpiration loss. Seawater in each pot was weekly replaced by freshly prepared seawater to ensure that seawater would not become stale. The cultivation lasted for 90 d. 2.2. Propagule establishment and seedling growth Propagule establishment in each pot, for each species, was evaluated by daily recording of root initiation and seedling establishment. Root initiation was referred as the date when the first root appeared, while seedling establishment was defined as the date when the first pair of leaves unfurled. At the end of the cultivation, each plant was harvested and dried at

196


65 8C, and then, relative growth rate (RGR) was determined by dividing dry weight by culture time (90 d). 2.3. Salt secretion from leaves and salt content in leaf tissue solution During the last week of the cultivation, in each pot, two leaves with similar ages of about 40 d were rinsed with double distilled water and blotted dry. After 24 h, the chosen leaves were harvested and salt secretion from leaves and salt contents in leave tissues were determined. The leaves were rinsed with double distilled water and conductivity in the rinse water was measured with a conductivity meter made by Orion. Conductivity values were then converted to salt contents using a standard curve showing linear relationships between salt contents and conductivity values: y = 1.0773x (d.f. = 5, r = 0.9991), where y is conductivity (ms cm 1) and x is salt content (different salt contents were obtained by preparing artificial seawater with different salinities in ppt). The two rinsed leaves were, respectively, blotted dry, weighed and scanned to determine area. Salt secretion from leaves was expressed as salt quantity in the rinse water per leaf area per day. One leaf was ground with double distilled water and salt concentration in the extract in terms of conductivity value was determined. Water content in leaf tissue was measured by oven drying the other leaf at 70 8C. Salt content in leaf tissue solution was expressed as salt per gram of water in leaf tissue. Salt contents were measured by conductivity because the main ion contents of the secreted material and leaf tissue solution were similar to those in artificial seawater (Ball, 1988). 2.4. Evapo-transpiration During the last week of the cultivation, evaporation and transpiration (evapotranspiration) rates from each pot were estimated by water loss in each pot system in 24 h. 2.5. Data analysis Mean and standard deviation values of triplicate pots were calculated. A parametric twoway analysis of variance (ANOVA) with species and salinity treatments as the factors was employed to test any difference among three mangrove species, among five salinity levels and interactions between species and salinity. If a significant difference were found in either the species factor or the interaction term, the effect of salinity on each species would be tested again using one-way ANOVA. The Student–Newman–Keuls multiple comparison method was used to test significant difference between any two salinity levels for each species.

3. Results 3.1. Propagule establishment Propagules of Ac. ilicifolius started to initiate roots on days 3 and 7 at low and high salinities, respectively (Table 1). The propagules planted at low salinities of 0 and 5 ppt


197

Table 1 Effects of salinity on root initiations and final establishment percentages of three salt-secreting mangrove species, Acanthus ilicifolius, Aegiceras corniculatum and Avicennia marina Salinity (ppt)

Root initiation (d)a

Final establishment rate (%)

Acanthus ilicifolius

Aegiceras corniculatum

Avicennia marina

Acanthus ilicifolius

Aegiceras corniculatum

Avicennia marina

0 5 15 25 35

3.0 0.0b 3.0 0.0b 3.7 0.5b 7.7 1.6a 7.3 0.9a

6.0 0.0a 6.0 0.0a 6.0 0.0a 6.0 0.0a 5.7 0.5a

3.0 0.0 a 3.0 0.0 a 3.0 0.0 a 3.3 0.5 a 3.0 0.0 a

100.0 0.0a 100.0 0.0a 100.0 0.0a 91.7 11.8a 27.8 3.9b

100.0 0.0a 96.3 5.2a 100.0 0.0a 85.2 5.2b 38.4 22.7c

100.0 0.0a 100.0 0.0a 100.0 0.0a 100.0 0.0a 100.0 0.0a

Significance

p < 0.05

p > 0.05

p > 0.05

p < 0.05

p < 0.05

p > 0.05

Mean S.E. from three replicate pots are given and different letters in the same column are significantly different at the level of 0.05. a Root initiation was referred as the date when the first root appeared.

reached the maximum rooting percentages within 6 d, while took about 15 d for those at 10, 15, 25 and 35 ppt salinities (Fig. 1A). The final rooting percentages were similar (nearly 100%) among all salinities below 25 ppt, but the maximum value at a very high salinity of 35 ppt was only about 60%. For Ae. corniculatum, all propagules had their root initiations on day 6 (Table 1), but rooting percentages decreased with increases in salinity and almost all propagules were rooted on day 10, irrespective to salinity levels (Fig. 1B). Salinity levels had little effects on root initiation of Av. marina propagules. They began to be rooted on day 3 and all were rooted before day 11 (Table 1 and Fig. 1C). Rooting speed was fastest at 0 ppt salinity, but there were no significant differences among the other salinities. In terms of root initiations, significant differences were found among the three species and interactions between species and salinity (Tables 1 and 2). Propagules of Av. marina had significantly more rapid root initiations than those of Ae. corniculatum. Salinity did not significantly affect root initiations of Ae. corniculatum and Av. marina, but significantly slower root initiations of Ac. ilicifolius were found at high salinity levels. At salinities below 15 ppt, Ac. ilicifolius, similar to Av. marina, had rapid root initiations. However, root initiations of Ac. ilicifolius at high salinities (over 25 ppt) were even slower than those of Ae. corniculatum. On day 26, propagules of Ac. ilicifolius reached 100% seedling establishment percentage at low salinity of 0 ppt and took 30 d at 5 and 15 ppt salinities (Table 1 and Fig. 2A). However, the maximum seedling establishment percentages at 25 and 35 ppt salinities were 92 and 28%, respectively and took more than 42 d. Almost, all of the Ae. corniculatum propagules were established on day 30 at salinities of 0, 5 and 15 ppt, but the final seedling establishment percentages at salinities of 25 and 35 ppt were only about 85 and 38%, respectively (Table 1 and Fig. 2B). These results indicate that Ae. corniculatum had slow germination rate at salinity over 25 ppt but salinities below 15 ppt did not have any significant effects on their germination. Salinity had little effect on seedling establishment for Av. marina. Their first pair of leaves unfurled 8 d after planting in all salinity treatments and all propagules were established before day 18 (Fig. 2C).

198


Fig. 1. Rooting percentages of propagules of Acanthus ilicifolius (A), Aegiceras corniculatum (B) and Avicennia marina (C). The total number of propagule is 27 for each salinity treatment of each species.

There were significant differences in final establishment percentages among the three species and interaction between species and salinity (Table 2). Av. marina had significantly higher establishment percentages than those of Ae. corniculatum and Ac. ilicifolius, especially, at high salinities. Salinity did not significantly affect final establishment percentages of Av. marina but significantly lower values were found at high salinity levels for Ac. ilicifolius and Ae. corniculatum. At salinities below 15 ppt, Ac. ilicifolius and Ae. corniculatum had 100% establishment, similar to Av. marina, but at 35 ppt salinity, only 28 and 38% final establishment percentages were recorded for Ac. ilicifolius and Ae. corniculatum, respectively.


199

Table 2 Results of ANOVA Source of variation

Root initiation

Final establishment

RGR

Leaf salt secretion

Leaf salt concentration

Evapotranspiration

Salinity (d.f. = 4) Species (d.f. = 2) Salinity species (d.f. = 8)

12.8* 71.5* 12.6***

51.9*** 19.9* 14.0***

100.9*** 3043.5*** 24.8***

130.9*** 317.7*** 28.8***

158.3*** 65.2* 14.3***

159.0*** 355.0*** 19.7***

* ***

F-values are given and significance is denoted as p < 0.05. F-values are given and significance is denoted as p < 0.001.

3.2. Growth Salinity had a significant effect on RGR of Ac. ilicifolius (F = 106.3, p < 0.001) as well as Ae. corniculatum (F = 40.72, p < 0.001). Seedlings of Ac. ilicifolius and Ae. corniculatum grew more at low salinities than high ones (Fig. 3A). For Av. marina seedlings, RGR significantly increased from 0 to 5 ppt but significantly decreased at salinities over 15 ppt (F = 44.34, p < 0.001) and the highest value was at low to moderate salinities (5–15 ppt). Significant interaction was found between species and salinity on RGR of the three salt-secreting mangrove species (Table 2). As salinities increased from 0 to 35 ppt, decrease in RGR of Av. marina was about 5%, much less than those of Ae. corniculatum (56%) and Ac. ilicifolius (70%). 3.3. Salt secretion and concentration Salt secretion from leaves of the three species significantly increased with increases in salinity but the degree of increases depended on the salinity range (Table 2 and Fig. 3B). At moderate salinity range, from 5 to 25 ppt, increase in salt secretion of Ac. ilicifolius was about 0.1 g m 2 d 1 at every 10 ppt increases, while the corresponding increase was about 0.2 g m 2 d 1 with salinity increases from 0 to 5 ppt and from 25 to 35 ppt. At the low salinity from 0 to 5 ppt, increase in salt secretion of Ae. corniculatum was 0.1 g m 2 d 1 and at salinities from 5 to 35 ppt, the corresponding increase was about 0.6 g m 2 d 1 at every 10 ppt increases. At low salinity from 0 to 5 ppt, increase in salt secretion of Av. marina was 1.8 g m 2 d 1, while the increase was 1.3 g m 2 d 1 from 25 to 35 ppt. However, increases in salt secretion were less obvious at moderate salinities ranging from 5 to 25 ppt with an increase of 0.8 g m 2 d 1 when salinities increased from 5 to 15 ppt and no significant increase was found from 15 to 25 ppt. The responses of salt secretion to salinity were significantly different among the three species (Table 2) and the mean increases in salt secretion at every 10 ppt increases in salinity were about 0.9, 0.6 and 0.2 g m 2 d 1 for Av. marina, Ae. corniculatum and Ac. ilicifolius, respectively. Salt concentration in leaf tissue water of Ac. ilicifolius significantly increased with the increase in salinity (r = 0.988, p < 0.01), especially, from 5 to 35 ppt (Fig. 3C). At low salinities of 0–5 ppt, salt concentration did not significantly change with salinity. However, from 5 to 35 ppt, every increase of 10 ppt salinity resulted in an increase of about 1% in salt concentration. Salt concentration in leaf tissue water of Ae. corniculatum was in direct proportion with salinity (r = 0.994, p < 0.01) with an increase of about 0.8% salt

200


Fig. 2. Effects of salinity on seedling establishment rates of propagules of Acanthus ilicifolius (A), Aegiceras corniculatum (B) and Avicennia marina (C). The total number of propagule is 27 for each salinity treatment of each species.

concentrations in every increase of 10 ppt salinity (Fig. 3C). Compared to Ac. ilicifolius and Ae. corniculatum, no significant linear correlation between salinity and salt concentration in leaf tissue water was found in Av. marina (r = 0.783, p > 0.05) (Fig. 3C). The increases (2.5%) in salt concentration were most obvious when salinities increased from 0 to 5 ppt, but the increase was 0.5% at every increase of 10 ppt salinity from 5 to 25 ppt. Salt concentration did not show any changes at high salinities, from 25 to 35 ppt. The three mangrove species showed significant different responses to salinity in terms of salt concentration in leaf tissue water (Table 2). The increases in salt concentration with


201

Fig. 3. Effects of salinity on relative growth rate (RGR) per seedling (A), leaf salt secretion from leaves (B), salt content in leaf tissue water (C) and evapo-transpiration per pot (D) of Acanthus ilicifolius, Aegiceras corniculatum and Avicennia marina. Different letters on the same line shows significant differences from each other at p < 0.05.

202


salinities raised from 0 to 5 ppt followed the descending order of Av. marina > Ae. corniculatum > Ac. ilicifolius, but at salinities ranging from 5 to 35 ppt the order was Ac. ilicifolius > Ae. corniculatum > Av. marina (Fig. 3C). 3.4. Evapo-transpiration Evapo-transpiration of Ac. ilicifolius pots decreased linearly with the increase in salinity (Fig. 3D). The value of Ae. corniculatum pots also decreased with increases in salinity but the differences between high and low salinities were less than that of Ac. ilicifolius pots (Fig. 3D). Compared to Ac. ilicifolius and Ae. corniculatum, Av. marina pots had the highest evapo-transpiration at moderate salinities and had low variations in evapotranspiration between different salinities (Fig. 3D).

4. Discussion For a plant species, capacity to invade upper estuarine habitats may be dependent on its salt tolerance at germination (Harradine, 1982; Krauss et al., 1998). Increases in salinity lead to a reduction and/or delay in germination of both halophyte and glycophyte seeds (Ungar, 1982; Khan and Ungar, 1984; Katembe et al., 1998). Werner and Finkelstein (1995) indicated that elevated salinity slowed down water uptake by seeds, thereby inhibited their germination and root elongation. No significant effects of salinity were found on root initiations for propagules of the two viviparous mangrove species, Ae. corniculatum and Av. marina (Table 1). For the non-viviparous species, Ac. ilicifolius, increases salinity significantly prolonged root initiations. These results suggested that propagules of viviparous species had higher salt tolerance than those of non-viviparous ones. Previous researchers concluded that the adaptation of viviparous propagules to saline environments actually starts when they are still attached to the mother tree by continuously absorbing salts from the tree or by a desalinating process (Joshi et al., 1972; Zheng et al., 1999). Root initiations of both viviparous species were not significantly affected by increases in salinity, indicating that early development during germination was determined by propagules themselves but not external salinity. However, effects of salinity on final establishment percentages were different between Ae. corniculatum and Av. marina. At salinities over 25 ppt, low final establishment were recorded for Ae. corniculatum but not for Av. marina. These suggested that late development during germination of Ae. corniculatum was determined by external salinity, while propagules themselves had more influence on establishment percentages for Av. marina. In terms of the whole germination process, salt tolerance of the three salt-secreting mangrove species had the descending order of Av. marina > Ae. corniculatum > Ac. ilicifolius. High salinity significantly decreased CO2 assimilation of mangroves, such as Ae. corniculatum, Av. marina and Rhizophora mangle (Ball and Farquhar, 1984; Lin and Sternberg, 1992). However, the present study showed that effects of salinity on seedling growth differed among the three salt-secreting species, Ac. ilicifolius, Ae. corniculatum and


203

Av. marina. Although RGR of Ac. ilicifolius and Ae. corniculatum decreased with increases in salinity from 5 to 35 ppt, Ac. ilicifolius had larger variations than Ae. corniculatum, indicating the latter was more tolerant to salt stress. For Av. marina, the largest RGR was recorded at salinities between 5 and 15 ppt and differences due to changes in salinity were less than the other two species, demonstrating that Av. marina was the most salt-tolerant species. These results again tested the hypothesis that the order of salt tolerance is Av. marina > Ae. corniculatum > Ac. ilicifolius. Salt stimulation to secretion was a common feature in salt-secreting mangrove species (Boon and Allaway, 1982, 1986; Drennan and Pammenter, 1982; Ball, 1988; Sobrado, 2002). In the present study, all of the three species exhibited increases in salt secretion with increases in salinity, consistent with previous reports. Capacity to secrete salts at any given salinity was different between species, following an order of Av. marina > Ae. corniculatum > Ac. ilicifolius, similar to the case of seedling growth. This indicated that salts secretion from leaves was related to salt tolerance. When propagules were cultured in fresh water, salt concentration in leaf tissue solution of the three mangrove species was about 2%, much higher than that in culture water. This phenomenon was previously reported in several mangrove species, such as Av. marina (Downton, 1982; Clough, 1984; Ball et al., 1987; Naidoo, 1987), Rhizophora stylosa (Clough, 1984) and Kandelia candel (Hwang and Chen, 2001) and was considered as an osmo-regulatory function (Flowers et al., 1986). For salt-secreting species with strong salt tolerance, salt concentration in plants maintained saturated and changed little at different salinities (Sobrado, 2002). This could prevent the occurrence of an imbalance between salt reaching the leaf and being secreted. If salt builds up in leaf cell walls it will cause cell dehydration (Munns and Passioura, 1984). In the present study, salt concentrations in leaf tissue solution of Av. marina grown at salinities of 5–35 ppt maintained a high level of 4.3– 5.0% and the corresponding variations were 2.4–4.5 and 2.3–5.3% for Ae. corniculatum and Ac. ilicifolius, respectively. This showed that salt concentration variations between seedlings at high and low salinities among the three species had the order of Av. marina < Ae. corniculatum < Ac. ilicifolius, indicating that the capacity to maintain water potentials at high salinities was Av. marina > Ae. corniculatum > Ac. ilicifolius. This also supported the hypothesis that the order of salt tolerance is Av. marina > Ae. corniculatum > Ac. ilicifolius. Torrecillas et al. (2003) concluded that species with conservative water use at various salinities had high salt tolerance. Among the three species examined in the present study, evapo-transpiration rates were similar under fresh water. However, at salinities of 5–35 ppt variations of evapo-transpiration were different between species with an order of Av. marina < Ae. corniculatum < Ac. ilicifolius, i.e. the conservation in water use is Av. marina > Ae. corniculatum > Ac. ilicifolius. This further supported the hypothesis that the order of salt tolerance is Av. marina > Ae. corniculatum > Ac. ilicifolius.

Acknowledgements We thank Mr. K.L. Fong for his assistance in this study. The work described in this paper is supported by grants from the Environment and Conservation Fund of the HKSAR

204


(Project No. 9210007), National Natural Science Foundation of China (Project No. 40476040) and Fujian Natural Science Foundation (Project No. 0410006). References Ball, M.C., 1988. Salinity tolerance in the mangroves Aegiceras corniculatum and Avicennia marina. Part I: water use in relation to growth, carbon partitioning and salt balance. Aust. J. Plant Physiol. 15, 447–464. Ball, M.C., Anderson, J.M., 1986. Sensitivity of photosystem II to NaCl in relation to salinity tolerance: comparative studies with thylakoids of the salt-tolerant mangrove, Avicennia marina, and the salt-sensitive pea, Pisum sativum. Aust. J. Plant Physiol. 13, 689–698. Ball, M.C., Chow, W.S., Anderson, J.M., 1987. Salinity-induced potassium deficiency causes loss of functional photosystem II to NaCl in leaves of the grey mangrove, Avicennia marina, through depletion of the atrazinebinding polypeptide. Aust. J. Plant Physiol. 14, 351–361. Ball, M.C., Farquhar, G.D., 1984. Photosynthetic and stomatal responses of the two mangrove species, Aegiceras corniculatum and Avicennia marina, to long term salinity and humidity conditions. Plant Physiol. 74, 1–6. Boon, P.I., Allaway, W.G., 1982. Assessment of leaf-washing techniques for measuring salt secretion in Avicennia marina (Forsk.) Vierh.. Aust. J. Plant Physiol. 9, 725–734. Boon, P.I., Allaway, W.G., 1986. Rates and ionic specificity of salt secretion from excised leaves of the mangrove, Avicennia marina (Forsk.). Vierh. Aquat. Bot. 26, 143–153. Burchett, M.D., Clarke, C.J., Field, C.D., Pulkownik, A., 1984. Salinity, growth and root respiration in the grey mangrove, Avicennia marina. Physiol. Plant 60, 113–118. Burchett, M.D., Clarke, C.J., Field, C.D., Pulkownik, A., 1989. Growth and respiration in two mangrove species at a range of salinities. Physiol. Plant 75, 299–303. Clarke, L.D., Hannon, N.J., 1970. The mangrove swamp and salt marsh communities of the Sydney district. Part III: plant growth in relation to salinity and waterlogging. J. Ecol. 58, 351–369. Clough, B.F., 1984. Growth and salt balance of the mangrove Avicennia marina (Forsk.) Vierh. and Rhizophora stylosa Griff. in relation to salinity. Aust. J. Plant Physiol. 11, 419–430. Connor, D.J., 1969. Growth of grey mangrove (Avicennia marina) in nutrient culture. Biotropica 1, 36–40. Downton, W.J.S., 1982. Growth and osmotic relations of the mangrove Avicennia marina, as influenced by salinity. Aust. J. Plant Physiol. 9, 519–528. Drennan, P., Pammenter, N.W., 1982. Physiology of salt secretion in the mangrove Avicennia marina (Forsk.) Vierh.. New Phytol. 91, 597–606. Flowers, T.J., Hajibagheri, M.A., Clipson, N.J.W., 1986. Halophytes. Q. Rev. Biol. 61, 313–337. Harradine, A.R., 1982. Effect of salinity on germination and growth of Pennisetum macrourum in southern Tasmania. J. Appl. Ecol. 19, 273–282. Hwang, Y.H., Chen, S.C., 2001. Effects of ammonium, phosphate, and salinity on growth, gas exchange characteristics, and ionic contents of seedlings of mangrove Kandelia candel (L.) Druce. Bot. Bull. Acad. Sin. 42, 131–139. Joshi, G.V., Pimplaskar, M., Bhosale, L.J., 1972. Physiological studies in germination of mangroves. Bot. Mar. 45, 91–95. Katembe, W.J., Ungar, I.A., Mitchell, J.P., 1998. Effect of salinity on germination and seedling growth of two Atriplex sepecies (Chemopodiaceae). Ann. Bot. 82, 167–175. Khan, M.A., Ungar, I.A., 1984. The effect of salinity and temperature on germination of polymorphic seeds and growth of Atriplex triangularis. Am. J. Bot. 71, 481–489. Krauss, K.W., Chambers, J.L., Allen, J.A., 1998. Salinity effects and differential germination of several half-sib families of baldcypress from different seed sources. New Forest. 15, 53–68. Lin, G., Sternberg, L.S.L., 1992. Effect of growth form, salinity, nutrient and sulfide on photosynthesis, carbon isotope discrimination and growth of red mangrove (Rhizophora mangle L.). Aust. J. Plant Physiol. 19, 509–517. Mizrachi, D., Pannier, R., Pannier, F., 1980. Assessment of salt resistance mechanisms as determinant physioecological parameters of zonal distribution of mangrove species. Part I: effect of salinity on nitrogen metabolism balance and protein synthesis in the mangrove species Rhizophora mangle and Avicennia marina nitida. Bot. Mar. 53, 289–296.


205

Munns, R., Passioura, J.B., 1984. Effect of prolonged exposure to NaCl on the osmotic pressure of leaf xylem sap from intact transpiring barley plants. Aust. J. Plant Physiol. 11, 497–507. Naidoo, G., 1987. Effects of salinity and nitrogen on growth and relations in the mangrove, Avicennia marina (Forsk.) Vierh.. New Phytol. 107, 317–325. Sobrado, M., 2002. Effect of drought on leaf gland secretion of the mangrove Avicennia marina germinans L.. Trees 16, 1–4. Tam, N.F.Y., Wong, Y.S., Lu, C.Y., Berry, R., 1997. Mapping and characterization of mangrove plant communities in Hong Kong. Hydrobiologia 352, 25–37. Tam, N.F.Y., Wong, Y.S., 2002. Conservation and sustainable exploitation of mangroves in Hong Kong. Trees 16, 224–229. Tomlinson, P.B., 1986. The Botany of Mangroves. Cambridge University Press, Cambridge, pp. 123–128. Torrecillas, A., Rodrı´guez, P., Sa´nchez-Blanco, M.J., 2003. Comparison of growth, leaf water relations and gas exchange of Cistus albidus and C. monspeliensis plants irrigated with water of different NaCl salinity levels. Sci. Horti. 97, 353–368. Ungar, I.A., 1982. Germination ecology of halophytes. In: Sen, D.N., Rajpurohit, K.S. (Eds.), Contributions to the Ecology of Halophytes. Dr. W. Junk Publishers, The Hague, pp. 143–154. Werner, J.E., Finkelstein, R.R., 1995. Arabidopsis mutants with reduced response to NaCl and osmostic stress. Physiol. Plant 93, 659–666. Youssef, T., Saenger, P., 1998. Photosynthetic gas exchange and water use in tropical and subtropical populations of the mangrove Aegiceras corniculatum. Mar. Freshwater Res. 49, 329–334. Zheng, W.J., Wang, W.Q., Lin, P., 1999. Dynamics of element contents during the development of hypocotyls and leaves of certain mangrove species. J. Exp. Mar. Biol. Ecol. 233, 247–257.