Aquatic Botany 66 (2000) 311320

Canopy leaf area index and litter fall in stands of the mangrove Rhizophora apiculata of different age in the Mekong Delta, Vietnam
Barry Clough a, , Dang Trung Tan b , Do Xuan Phuong b , Dang Cong Buu b
b a Australian Institute of Marine Science, PMB 3, Townsville Qld 4810, Australia Minh Hai Wetland Forest Research Centre, 49A Hung Vuong Street, Ca Mau, Vietnam

Received 7 April 1999; accepted 22 June 1999

Abstract Leaf area index (LAI) and seasonal patterns of litter fall, leaf production and seed (propagule) production were measured in monocultures of the mangrove Rhizophora apiculata aged from 6 to 36 years in Ca Mau Province, southern Vietnam. There was no clearly dened seasonal pattern in leaf fall, but leaf emergence was signicantly correlated with the monthly precipitation/evaporation (P/E) ratio. Propagule production was markedly seasonal, with more than 80% of the propagules being shed in the wet season period of MayNovember. Total annual litter fall ranged from 941 g dwt m2 year1 to 1879 g dwt m2 year1 . Leaf litter was the main component of litter fall in all the stands, twigs and branches being a signicant component of litter fall in only one stand which was undergoing self-pruning of the lower branches. Propagules were a signicant component of litter fall only in the two older stands of 21 years and 36 years, which produced an average of about 40 and 68 propagules m2 years1 , respectively, highlighting the importance of older forests of R. apiculata as seed stands. Stand LAI decreased with age, ranging from 4.9 in the younger stands down to 3.3 in older stands. These leaf area indices are comparable to those of Rhizophora stands elsewhere. 2000 Elsevier Science B.V. All rights reserved.
Keywords: Mangrove; Leaf area index; Litterfall; Phenology

1. Introduction Mangroves, mainly the species Rhizophora apiculata Bl., are widely used in SE Asia as a source of fuel wood, to produce timber for construction, and for the manufacture of charcoal. Following the cessation of hostilities in Vietnam in 1975, mangrove forests in
Corresponding author. Present address: NACA PO Box 1040, Kasetsart Post Ofce, Bangkok, 10903, Thiland; Tel.: +66-2-561-1728; fax: +66-2-561-1727. E-mail address: bclough@aims.gov.au (B. Clough)

0304-3770/00/$ see front matter 2000 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 4 - 3 7 7 0 ( 9 9 ) 0 0 0 8 1 - 9

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the Ca Mau Peninsula, southern Vietnam, initially recovered as a result of both natural regeneration and manual planting of the preferred forestry species, R. apiculata. However, recent expansion of shrimp culture in the region has now substantially reduced the area of mangroves, to the point where the remaining mangrove forest may not meet the projected demand for timber, fuel wood and charcoal. The work described below was carried out as part of a larger study with the overall objective of developing better strategies for integrating aquaculture and mangrove forestry in the lower Mekong Delta, Vietnam, where a number of provincial governments have established shrimp farming-forestry enterprises (SFFEs). In these mixed aquaculture-mangrove forestry systems, shrimp and other cultured species dependent mostly on natural food chains for their food supply. It is now widely recognised that mangrove derived detritus may be a major source of carbon for estuarine food webs along tropical and subtropical coastlines (e.g. Odum and Heald, 1972; Beumer, 1978; Malley, 1978; Robertson, 1986; Robertson and Daniel, 1989; Daniel and Robertson, 1990). The rst objective of this study was to quantify the rate of litter fall in mangrove forests of different age in Ca Mau Peninsula. In addition, the balance between leaf loss as litter and leaf production is important in the maintenance of canopy leaf area index (LAI), which underpins the primary productivity, growth and yield of mangrove forests in the study area. Thus, a second objective of the present work was to investigate the dynamics of leaf production and leaf loss in relation to the leaf area index of mangrove stands of different age. Finally, there was a lack of quantitative data on reproductive phenology and propagule production for mangrove forests in the southern provinces of Vietnam, without which it is not possible to predict the supply of seed for further planting of mangrove forests in the region. The third objective of this work was, therefore, to investigate reproductive phenology and quantify seed (propagule) production in stands of different age.

2. Methods Sampling was carried out in monocultures of R. apiculata aged between 6 and 36 years in three mixed shrimp farming-mangrove forestry enterprises (Tam Giang 3, SFFE 184 and Kienvang) in Ca Mau Province, southern Vietnam (Fig. 1). This region of Vietnam, located at a latitude of about 8 50 N, is characterised by a strongly bimodal rainfall pattern, with a clearly dened wet season extending from May to November, and very little rainfall in the dry season (Fig. 2). Three litter traps of 1 m2 in cross-sectional area were hung beneath the canopy in each stand. The litter traps were emptied at monthly intervals for 1 year, and the samples sorted into leaves, stipules, ower parts, propagules and a combination of woody material and debris. After counting the number of leaves, stipules and propagules in each sample, the fractions were then oven dried to constant weight at 80 C. Stand (LAI) were measured using a light attenuation method (Clough et al., 1997). Briey, this method estimates leaf area index from the ratio of the light ux density beneath the canopy to that above the canopy, assuming that light attenuation within the canopy follows the BeerLambert Law. In the present study, between 100 and 200 measurements were made of the light ux density beneath the canopy on a clear sunny day between 1100 and

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Fig. 1. Map of Ca Mau Province, Vietnam, showing the location of study sites.

1400 hours, using a handheld quantum sensor. Measurements of the light ux density before and after the readings taken beneath the canopy were made in an open area well outside the canopy. All light readings were corrected for solar angle. This correction was calculated from the length of the shadow cast by a stick of known height thrust vertically into a at area of ground outside the canopy. 3. Results 3.1. Total litter fall and its components Total annual litter fall ranged from 941 g dwt m2 year1 in a 9-year-old-stand up to 1879 g dwt m2 year1 in a 12-year-old-stand (Table 1).

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Fig. 2. Average monthly rainfall, evaporation and sunshine hours in Ca Mau Province, Vietnam. Averages are for the period 19711994 (Ca Mau Meteorological Station).

Leaves represented more than 75% of the total litter fall in stands up to 10 years of age, thereafter falling to only 38% in the 36-year-old-stand (Fig. 3). Woody components represented an unusually high proportion (30.4%) of the total litter fall in the 12-year-old-stand, suggesting that this stand was undergoing self pruning of the lower branches (Fig. 3). Propagules represented less than 1% of the total litter fall in stands up to 12 years of age, but were a very signicant component of the litter fall in the two older stands, where they amounted to 25.7% and 37.5% of the total in stands aged 21 years and 36 years, respectively (Fig. 3). The contribution of ower parts to the total litter fall was also much greater in the stands aged 21 years and 36 years (5.8 and 6.1%, respectively) compared to the younger stands (Fig. 3). Stands up to 10 years of age produced an average of < 1 propagule m2 years1 ; the 12-year-old-stand produced an average of 3.7 propagules m2 year1 (ca. 37,000 ha1
Table 1 Total annual litter fall and its components for R. apiculata stands aged from 6 to 36 years. Values are in units of g dwt m2 year1 ( S.E.), unless otherwise indicated Age Component Leaves Stipules Wood Flower parts Propagules Total (g m2 year1 ) Total (t ha1 year1 ) Total (g m2 d1 ) 6 886.1 (18.2) 101.8 (2.5) 99.1 (37.5) 5.3 (1.5) 2.3 (1.3) 1094.6 10.95 3.00 9 758.3 (28.1) 95.8 (4.0) 75.2 (17.4) 10.5 (0.9) 1.6 (0.6) 941.5 9.41 2.58 10 939.4 (32.0) 104.2 (3.7) 170.6 (17.8) 10.5 (1.9) 0.6 (0.3) 1225.2 12.25 3.36 12 1162.8 (24.6) 119.8 (2.3) 572.2 (59.7) 10.0 (1.4) 14.6 (2.4) 1879.4 18.79 5.15 21 584.2 (20.5) 79.1 (1.1) 166.9 (10.5) 71.0 (3.3) 312.1 (47.1) 1213.4 12.13 3.32 35 665.5 (21.1) 76.3 (2.0) 238.0 (59.6) 106.2 (8.2) 651.7 (16.8) 1737.7 17.38 4.76

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Fig. 3. Proportions of leaves, stipules, wood, ower parts and propagules in the total annual litter fall of R. apiculata stands of different age.

year1 ), the 21-year-old-stand produced 39.7 propagules m2 year1 (ca. 397,000 ha1 year1 ), and the 36-year-old produced 68 propagules m2 year1 (ca. 680,000 ha1 year1 ). In R. apiculata the number of new leaves produced can be estimated from the number of stipules in the litter samples, because two stipules are lost for each new pair of leaves that unfolds (Duke et al., 1984). Annual rates of leaf production were less than annual rates of

Fig. 4. Annual leaf loss and leaf production in stands of R. apiculata of different age. (A) Numbers of leaves lost and produced. (B) Ratio of leaf production to leaf loss. (C) Relationship between leaf production and leaf loss. The regression equation was y = a + bx, where y and x are the number of leaves produced and lost, respectively, constant a = 189.3 and constant b = 0.7402 (r2 = 0.99; p = <0.0001).

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leaf loss in stands of all ages. About 0.83 new leaves being produced for every leaf lost in stands up to 12 years of age, rising to about 0.94 new leaves produced per leaf lost in the 21 and 36-year-old-stand (Fig. 4). These two older stands had lower annual rates of leaf loss and production than the younger stands (Fig. 4A). On an annual basis, leaf production and leaf loss were closely correlated (Fig. 4C), but there was no seasonal correlation between them (Fig. 5). 3.2. Seasonal patterns of litter fall Seaonal patterns in leaf fall and leaf production are shown in Fig. 5. Correlations of leaf fall and leaf production with monthly climatic parameters were carried out using the non-parametric Spearman Rank Order Correlation. Signicant correlations were obtained only with precipitation and the precipitation/evaporation (P/E) ratio, these two parameters being closely related; therefore, for the sake of brevity only the correlations between leaf fall, leaf production and P/E ratio will be presented here. A signicant correlation between leaf fall and the P/E ratio was found only in the 12-year-old-stand (r2 = 0.613; p < 0.001). In contrast, leaf production and P/E ratio were signicantly correlated in all the stands from 6 to 12 years of age (r2 from 0.41 to 0.63; p > 0.005). The 36-year-old-stand was unusual in having a strong single peak in leaf production at the end of the wet season in October (Fig. 5). The fall of ower parts and propagules was strongly seasonal in both stands that had reached reproductive age (21 and 36 years). Flower parts were present in the litter samples

Fig. 5. Seasonal patterns of leaf production and leaf loss in R. apiculata stands of different age in Ca Mau Province, Vietnam.

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Fig. 6. Seasonal pattern of ower and propagule drop in stands of R. apiculata of 21 and 36 years of age.

throughout the year, with a peak between April and July, in the early part of the wet season (Fig. 6). In both the stands, propagule fall commenced in May, peaked in AugustSeptember, and continued through until OctoberNovember (Fig. 6). A few propagules were present in the litter samples from the 36-year-old-stand in most months outside the main fruiting rseason (Fig. 7). 3.3. Leaf area index Canopy leaf area indices were measured in six plots of each age, including those in which litter samples were collected. Leaf area indices ranged from 3.3 to 4.9, the two

Fig. 7. Leaf area index of R. apiculata stands ranging from 6 to 36 years of age.

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stands with the lowest LAI being those aged 12 and 36 years (Fig. 7). The low LAI for the 12-year-old-stand is consistent with it going through a phase of self-pruning of the lower branches, as indicated by the high overall rate of litter fall, and the relatively high proportion of woody material (mainly small branches and twigs) in the litter samples (Table 1, Fig. 3). Data for 12-year-old-stand were, therefore, excluded from the non-linear regression line shown in Fig. 8. The data were best tted by a power curve, L = K AB , where L is the canopy LAI, A is the age in years, and K and B are constants. A least squares t to the data yielded values of 6.97 ( 0.73 S.E.) for K and 0.204 ( 0.042 S.E.) for B (r2 = 0.86; p = 0.015). It should also be noted that three of the six plots measured in the 36-year-old-stand had been thinned by about 30% approximately 3 years prior to the present measurement of their LAI. These three plots had measured LAI, without correction for prior thinning, ranging from 1.8 to 2.8. However, visual inspection of the canopies in these three plots indicated that the canopies of trees left after thinning had not expanded laterally to ll the space left by those removed during thinning, and the canopy was, therefore, not closed. The method used to measure LAI is strictly valid only for closed canopies (Clough et al., 1997). Data for thinned plots were, therefore, omitted from the analysis presented in Fig. 7.

4. Discussion Saenger and Snedaker (1993), tabulated litter fall data for mangroves from 91 sites over a range of latitudes and found that annual litter fall rates were generally negatively correlated with latitude, although rates of litter fall within latitudinal bands were also highly variable (Saenger and Snedaker, 1993). Annual rates of litter fall found in the present study, ranging from 9.4 to 18.9 t dwt ha1 year1 , were similar to those reported for Rhizophora species at similar latitudes (Sasekumar and Loi, 1983; Ong et al., 1984; Leach and Burgin, 1985; Saenger and Snedaker, 1993). Several studies in Australia and Papua New Guinea have reported marked seasonal periodicity in both leaf fall and leaf emergence for Rhizophora spp., with a a peak in both leaf fall and leaf emergence during the wet season (Williams et al., 1981; Duke et al., 1984; Leach and Burgin, 1985). In the present study there was no evidence of a consistent seasonal pattern in leaf fall in all the stands, notwithstanding climatic similarities between the Australian and Papua New Guinean sites, and those in the present work, notably in the strongly seasonal rainfall pattern. On the other hand, in all the six stands included in the present study, rates of leaf emergence were signicantly higher in the wet season than the dry season, as observed in Australia (Williams et al., 1981; Duke et al., 1984) and Papua New Guinea (Leach and Burgin, 1985). Furthermore, four of the six stands showed two peaks in leaf emergence during the wet season one early in the wet season, and a second towards the end of the wet season. These correspond closely to the bimodal wet season peaks in leaf emergence observed by Duke et al. (1984). As expected from past studies (Duke et al., 1984; Leach and Burgin, 1985), owering and propagule production were highly seasonal (Fig. 6). The number of owers and buds in litter samples was not counted, but based on the dry weights of ower parts, owering occurs mainly during the period April to July, although some owers were clearly present

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throughout most of the year, particularly in the two older stands of 21 and 36 years (Fig. 6). Similarly, propagules fell mainly in the wet season, with a peak during the period from May to November. These patterns correspond closely with those observed in Australia and Papua New Guinea, where open owers were present mainly from the late dry season through to the early wet season, or in some cases through to the late wet season, and ripe propagules were produced mainly in the wet season (Duke et al., 1984; Leach and Burgin, 1985). It is clear from the present data that, as in Papua New Guinea (Leach and Burgin, 1985), only a small proportion of the owers develop into propagules, even in the more mature 21 and 36-year-old-stand. Moreover, only the 21 and 36-year-old-stand produced signicant numbers of propagules. Based on the present data, 1 ha of forest aged 21 would produce sufcient propagules each year to plant about 40 ha of new forest at the preferred planting density of 10,000 ha1 , while 1 ha of the 36 year old forest would produce enough propagules annually to plant about 68 ha at 10,000 ha1 . By contrast, 1 ha of 12-year-old forest would produce enough propagules annually to plant only about 4 ha at 10,000 ha1 . This highlights the importance of preserving older aged stands as a source of seed for further planting. Unfortunately, most of the 36-year-old-stand were destroyed by a rare typhoon that struck the Ca Mau Peninsula in October 1997, after the measurements reported in this paper had been completed; the 21-year-old-stand in Kienvang Enterprise were reported also to have suffered signicant damage. Since most remaining stands of R. apiculatain coastal provinces south of the Mekong River are less than 15 years of age, there is likely to be a serious shortage in the supply of propagules over the next 1015 years in these southernmost provinces of Vietnam. The annual rate of leaf loss in all the stands exceeded the annual rate at which new leaves were produced, on average about 0.85 new leaves being produced for every leaf lost in stands up to 12-years-of-age, and about 0.94 new leaves being produced for every leaf lost in the older stands (Fig. 4). This implies a decline in canopy LAI as stands age, as indeed was observed from direct measurements of canopy LAI (Fig. 7). However, there are several expanations for the large difference between annual leaf production and annual leaf loss. Firstly, an examination of changes in stand density in the present stands up to 12-years-old, and in other stands of similar ages, showed that these stands were all undergoing self thinning. Secondly, stipules are difcult to count, particularly if fragmented, and stipule numbers could have been underestimated. Thirdly, the litter fall data were collected over a relatively short period of 1 year, and rates of litter fall may not be representative of longer term trends; however, an examination of weather records for the period of study did not reveal weather events or patterns that were signicantly different from long term averages, and which might have induced anomalies in the litter fall data. Nevertheless, our results strongly suggest that in self-thinning monocultures of R. apiculata in southern Vietnam, canopy LAI increases rapidly during the rst 56 years of stand development, reaching a maximum of somewhere between 4 and 5 at around 69 years of age, and thereafter declines gradually with increasing age to an asymptotic value of around 3. Acknowledgements This work was carried out as part of the project, Mixed Shrimp Farming-Mangrove Forestry Models in the Mekong Delta (FIS/94/12), supported by the Fisheries Program of

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the Australian Centre for International Agricultural Research, by the Ministry of Fisheries, Vietnam, and by the Asutralian Institute of Marine Science. We wish to thank Mr. B. Smith, Coordinator of the ACIAR Fisheries Program for his guidance and support, and Mr. Tran Thanh Xuan, the Vietnamese Project Leader, for assistance with logistics in Vietnam. We also thank the leaders of Tam Giang 3, SFFE 184 and Kienvang Enterprises, and their staff for their encouragement and assistance. Valuable comments on an earlier draft of the manuscript were provided by D. Alongi. Finally, we wish to acknowledge the assistance and hospitality of the farming families on whose farms this work was carried out. Contribution No. 972 from the Australian Institute of Marine Science. References
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