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Estuarine, Coastal and Shelf Science (1989) 29,75-87

Litter Production and Turnover of the Mangrove Kandelia candel (L.) Druce in a Hong Kong Tidal Shrimp Pond

S. Y. Lee Department of Zoology, The University of Hong Kong, Pokfulam Road, Hong Kong

Received 26July 1988 and in revisedform 22 March 1989

Keywords: litter production; turnover; tidal ponds; Kandelia candel; sesarmid crabs; management; Hong Kong

Production and turnover of Kandelia candel litter were studied for 2 years in a tidal shrimp pond (10 ha) at the Mai PO Marshes, northwest Hong Kong. Annual litter production averaged 11.070 t ha-’ (equivalent to 4.880 x 10’ kcal ha-‘), with wood and leaf materials contributing, respectively, 6.15 and 53.94% of the total. The reproductive plus frass component contributed 40.69% of the total production. The mean standing litter biomass recorded during the same period was 9587 f 0.556 t ha-’ (4.968 x 10’ kcal ha-‘), with respective contributions by the three components of 19.07,42.26 and 38.65%. Residence times (standing biomass/production) of the three components were extraordinarily long, estimated to be, respectively, 980,300 and 252 days. Stand characteristics of average tree height and dbh were good predictors of litter production while climatic variables, especially rainfall, could be used to predict the production of various litter components. Residence times were related to both inundation frequency and crab (Chiromanthes spp.) consumption. As the Kandelia candel stands were located largely above mean water level, there was little export of litter. The litter produced was predominantly decomposed or consumed by macrofauna in situ, creating a large energy sink which was not coupled to pelagic secondary production. The significance of these findings are discussed in relation to the fishery production and wildlife conservation value of the marshes.

Introduction

The high productivity of mangals has long been utilized by man. Shrimp and fish farming in tidal ponds constructed from mangrove forests have long histories in southeast Asia. Ling (1977) and Macintosh (1982) both suggested a history for tidal pond (tambak) fish and shrimp farming of over 500 years in Indonesia. Fish and shrimp farming in tambaks are still important aquacultural methods in Indonesia (Knox & Miyabara, 1987). Tidal ponds were mainly constructed for shrimp farming along the Chinese coast (Macnae, 1968). In Hong Kong, the history of these ponds (gei wai> dates back to the 194Os, when a series of ponds were dug from the native mangrove forest fringing Deep Bay (Irving & Leung, 1988), on the eastern fringe of the Pearl River Estuary. Most of these ponds have

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76 S. Y. Lee

now been turned into freshwater fish ponds because of pollution threats. The whole area of the marsh (the Mai PO Marshes), covering just over 300 ha, has been preserved as a nature reserve for migrant birds since 1973. A total of over 250 bird species are recorded through- out the year in the Deep Bay area, including a number of endangered and threatened species.

Since tidal shrimp ponds receive no allochthonous nutrient input other than import through a small seaward sluice gate, they act as good ‘ enclosures ’ for the study of ecological processes in a mangrove-dominated environment. The traditional fishing technique has undergone little change and the ponds still depend on natural recruitment for stocks. Fishery production rests upon energy derived from autochthonous detrital input from mangrove and other macrophytes. Management of these ponds is also important to the conservation of migrant birds which use these ponds and the Deep Bay area for feeding. The present study examines the production and turnover of the major detrital input, namely, litter from the dominant mangrove Kundelia candel and discusses the possible implications of these to the utilization of the ponds for fishery and conservation objectives.

The study pond

All data were collected from a tidal shrimp pond at the Mai PO Marshes fringing Deep Bay, northwest Hong Kong (Figure 1). The pond has an area of c. 100 x 1000 m2 (10 ha). The pond communicates with Deep Bay through a single sluice gate of 1.35(w) x 1.70(h) m2. Details of the operation of the ponds may be found in Macintosh (1982). Kundeliu cundel (L.) Druce is the dominant mangrove, occupying 25.99O, (2599 ha) of the pond area as isolated patches. Other species present are Avicenniu marina and Aegicerus corniculutum, in decreasing abundance. Water is usually changed during every spring tide and remains in the pond for 4-5 days during neap tide periods. Water depth is mostly < 1 m, and is nowhere greater than 1.8 m at most times.

Methods

Litter production A total of 16 conical traps each of 0.20 m2 circular collection area were established at 0,8 m above the forest floor level under monospecific stands of K. cundel in December 1985. This height prevented wetting or loss of any litter collected. The traps were spaced in different parts of the pond with varying stand characteristics and inundation frequencies. Bi-weekly to monthly collections were made until January 1988. The litter collected was wrapped in paper bags and dried at 80 “C for 48 h before the components of (a) leaf litter; (b) woody materials; and(c) reproductive materials plus frass (insect faeces, miscellaneous organic materials) were respectively sorted and weighed. The energy contents of the different components were estimated by a Parr semi-micro bomb calorimeter.

Standing litter biomass The standing litter biomass at each of the litter collection sites was estimated by collecting all surface litter in 0.25 m2 quadrats in close vicinity to the traps. A total of 12 sampling visits were made during the two-year period, covering different seasons. The litter was dried at 80 “C for 48 h before sorting into the three components and weighed.

Litter dynamics of Kandelia candel in tidal ponds 77

Studv \ I

Restricted Access Area

Figure 1. The geographical setting of the tidal shrimp ponds at Mai PO.

Stand characteristics and environmental measurements In order to correlate litter production and turnover with physical and environmental conditions of the stands, parameters of average tree height (Ht), average tree diameter at breast height (dbh), stand substrate elevation (E), crab density (Crabs), distance of the stand from the sluice (Dist) and inundation frequency of the stands (Exposure) were measured. Tree height was measured by a graduated telescoping rod or by a Range optical range finder. Average dbh was obtained by measuring the dbh of all trees taller than 1.3 m in a marked plot. A metric scale was established at the sluice gate to provide an arbitrary reference for recording water level fluctuations. By noting the time and water level at the gauge before and after each flooding or draining operation, an accurate record of water level variation was made. From this, the percentage time the substrate at a particular collection site would be exposed could be read from a sigmoid curve relating substrate elevation (on the metric scale) with exposure to air. Crab density was taken as the density of crab burrows, after eliminating the occurrence of burrows with dual openings. No actual crab density or biomass could be obtained, as the high densities of interlocking mangrove roots and the thick litter hampered effective digging. Distance of the stand from the sluice was estimated, on an arbitrary scale, from aerial photographs.

Rainfall (Rain) at Mai PO was recorded daily by a standard rain gauge positioned in the marsh. Other climatic parameters (monthly mean air temperature (Temp), mean daily global radiation (Globrad) and monthly total evaporation (Totevap)) were obtained from the Royal Observatory, Hong Kong.

78 S. Y. Lee

Stepwise multiple regression was used to investigate the relationship between litter production and turnover and the above stand characteristics and climatic variables. Production was regressed with the stand characteristics and again with the climatic variables in two respective groups. Litter residence times were regressed with the stand characteristics only. All calculations were performed by SPSS/PC + software (SPSS Inc., 1986). Violation of the assumption for the method was checked by residual analyses.

Results

Litter production Annual production of total litter varied from 9.104 to 13.037 t ha-’ yrr ’ and averaged 11.070 t ha-’ yr-’ for the sites, with respective contributions of 5.971 (53.949,), 0.681 (6.15%) and 4.418 (39.91%) t ha-’ yr- ’ from the leaf, wood and reproductive plus frass components. After adjusting for the relative contributions from the three components, this figure is equivalent to an annual energy input of 4.880 x 1 O7 kcal ha- ’ yr - ‘.

The litter fall pattern was bimodal, with high inputs in spring (February to June) and in late summer (August to November) (Figure 2). This bimodal pattern is also evident for the reproductive plus frass and leaf components. The first peak in February to June corresponded to dropper production and the second in July to October to flowers for the reproductive plus frass component. The leaf component has a higher late summer peak, probably related to a high leafing rate in early summer. Pattern of wood litter input seemed less well defined, although a distinct mid-summer peak was consistent in July. Wood litter production was also highly variable among the sites, as reflected by the large standard errors.

The stand characteristics at the various stations and the climatic variations during the study period are summarized in Table 1.

Results of the stepwise multiple regressions between litter production and turnover, the stand characteristics and climatic variables are presented in Tables 2 and 3. In all equations generated, except that for leaf litter production with environmental variables, only one of the six parameters was included, indicating that production could be effec- tively predicted by one of the variables. In terms of stand characteristics, average tree height and average dbh were important in predicting leaf, wood and total litter production. The positive slopes indicate that production increased with increasing tree height and dbh. Production of reproductive plus frass, however, could not be predicted with accuracy from any of the stand characters. Table 2 shows the models of environmental control on litter production. Rainfall was the only variable included in the predictive equations for both the reproductive plus frass and total litter, indicating increasing inputs during the rainy seasons. This is in agreement with the generalization of Day et al. (1987) that peak litter production usually occurs in the wet season. Wood production was only related positively with mean air temperature. Leaf litter production was, however, related to both monthly total evaporation and mean daily global radiation. As the entry of the second independent variable (Globrad) brought a significant increase in the multiple r from 0.4898 to 0.6981, the second variable is also of importance.

Standing litter biomass and turnover High standing litter biomasses were recorded under K. candel stands in the pond. The mean value (n = 162) was 9587 f O-556 t ha-‘. An approximate energy equivalent would be 4.968 x lo7 kcal ha-‘. Of this, respective contributions from the leaf, reproductive


plus frass and wood components were 4,051 (42.27%), 3.705 (38.66%) and 1.828 (19.07%) t ha-‘.

Table 4 shows the results of a Mann-Whitney U test for yearly differences in standing biomasses of the various litter components. As no significant difference can be detected for any of the components nor for total litter, residence times (standing biomass/production) for the various components were calculated according to the model of Olson (1963), assuming steady state conditions and monomolecular accumulation (Chapman, 1986; Vogt et al., 1986). The overall values for the entire ponds were, respectively, 252,300 and 980 days. The residence time for total litter was 317 days.

Relationships between site specific residence times for the various components and total litter were further analysed by multiple regression (Table 3). Exposure (percentage time exposed) seemed to influence residence times for both leaf litter and total litter, with increasing residence times for longer exposure times. Biotic factors also contributed to the turnover of the reproductive plus frass component, as the equation indicates an inverse relationship between residence time and the density of Chiromanthes spp. The production and turnover of litter components in the tidal pond is summarized in Table 5.

Discussion

Although K. candel is widespread along the south coast of China and has a northern limit at Japan (Hosokawa et al., 1977; Chen et al., 1985; Lin, 1987), it is a relatively little known species. Both Watson (1928) and Tomlinson (1986) regarded it as being nowhere abundant and only occurring along river banks in small, isolated patches. Notwithstanding, this species is the dominant pioneer species in Hong Kong, grows to about 6-7 m and is a major source of detrital energy input into tidal shrimp ponds at Mai PO.

Litter production by K. candel at Mai PO falls within the documented range of c. 1-15 t ha-’ yr-’ for mangroves (Christensen, 1979; Odum et al., 1982; Bunt, 1982; Twilley et al., 1986), but is considerably higher than the value of 8.52 t ha-’ yr-’ recorded for the same species by Lin et al. (1985). According to the physiognomic classification of Lugo and Snedaker (1974), the K. candel stands in the shrimp pond may be regarded as belonging to the fringing forest type, with only rare inundation by water and a fairly high litter production. Since the stands are only covered for < 10% of the time, they may also be classified as the equivalent to inundation classes 4 or 5 of Watson (1928). This characteristic seems to be important in the production and turnover of litter at the stands.

With this annual rate of litter production, the overall litter input into the entire pond is estimated to be 28.77 t yr-’ (equivalent to 1.268 x lO*kcal yr-‘). The great majority (24.92 t, 86.6%) of this, unlike most other mangroves, is retained on the forest floor. The energy equivalent of this resident litter is about 1.291 x lo* kcal. This high standing litter biomass also indicates that the residence time for the litter at these stands is extraordinarily long. Poovachiranon (in press) recorded standing litter biomass of only 9.93 g dry wt. mP2 (0.0993 t ha-‘) under dwarf K. candel normally inundated by tides at Three Fathoms Cove, Hong Kong. The residence time at Mai PO is also much higher than all values reported upon by Christensen (1978), Gong et al. (1984) and Twilley et al. (1986), where most records were obtained from normal tidally inundated stands. It is probably this absence of frequent tidal inundation that causes such a slow turnover of litter under K. candel stands in the shrimp ponds at Mai PO. This is further suggested by the significant

80 S. Y. Lee

01 I DJFMAMJJASONDJFMAMJJASONDJ

86 87 88

DJFMAMJJASONDJFMAMJJASONDJ

86

Figure 2. (a) and (b). See page 81.

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positive relationships generated by multiple regression between residence time and exposure.

Turnover of mangrove litter is effected through export, in situ decomposition (including leaching and production of DOM) and macrofaunal consumption. Frequent inundation hastens litter turnover in at least two important ways. First, tidal action facilitates export of litter, especially freshly fallen parts (Boto & Bunt, 1981; Twilley, 1985). Second, a moist environment is conducive to faster disappearance rates, by enhancing microbial decomposition, accelerating leaching and promoting consumption by amphipods, gastropods and brachyurans (Twilley et al., 1986; Rodriguez, 1987; Steinke and Ward, 1987). As aforementioned, export of litter from these stands is negligible. The daily export of macrodetritus out of the stands is estimated to be around


oJ+ DJFMAMJJASONDJFMAMJJASOND

0.6

0 DJFMAMJJASONDJFMAMJJASONDJ

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Figure 2. Seasonal variations in the production of total litter and the three components (a) total litter; (b) leaf litter (L fraction); (c) reproductive plus frass (F fraction); (d) wood (T fraction).

1.024 x lop2 g dry wt mm2 of K, candel stand area per day (unpublished data), which is equivalent to about 0.34% of the daily litter production. This amount probably represents the litter input from trees with branches overhanging the water and is equivalent to only 0.45 and 053% of the values recorded, respectively, by Golley et al. (1962) and Boto and Bunt (1981). Thus, litter produced at these stands is mostly decomposed and recycled in situ either through microbial action or macrofaunal consumption. In this respect, therefore, the system functions similar to terestrial systems which are more or less closed, and for which long residence time and accumulation of nutrients are characteristics (Witkamp & Ausmus, 1976; Woodruffe, 1985).

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TABLE 1. (a) Summary of the variations in the four climatic variables during the two year study period; (b) litter production as categorized into the leaf (LP), reproductive plus frass (FP) and the wood (TP) components and the stand characteristics at the 16 litter collection stations. Key to abreviations of variables is found in the text (a)

Date Rain

(mm month ‘) Temperature

P-3

Globrad (MJ mm* day ‘)

Total evaporation

(mm month’)

Dee 1985 0 15.9 13.4 94.3 Jan 1986 46.2 14.7 9.6 62.3 Feb 57-o 17.6 9.2 58.9

Apr 135.4 22.6 12.1 89.1

May 461.3 25.9 15.2 116.4

Jun 304.8 28.0 16.0 136.0

Jul 481.9 28.5 17.2 150.4

Aw 438.3 29.0 16.3 144.0

Sep 48.8 27.8 17.1 158.5 Ott 39.4 25.0 14.4 134.5 Nov 137.8 20.5 11.3 93.5 Dee 37.3 17.7 10.8 77.3 Jan 1987 2.7 17.3 11.9 93.3 Feb 6.7 18.3 11.7 75.0 Mar 211.6 21.3 8.1 57.3

Apr 247.3 21.9 12.5 83.4

May 308.6 25.0 11.7 84.9

Jun 146.6 27.5 15.1 119.9

Jul 347.2 28.9 15.8 124.3

Aw 100.0 28.6 19.4 152.8

Sep 48.2 29.2 14.0 122.3 Ott 57.2 25.7 13.5 109.7 Nov 107.6 21.8 9.6 83.7 Dee 5.0 16.8 12.0 99.7

Site

LP FP TP

(g dwt 0.2 mm2 yr~ ‘) Crabs

(?) fz) (m l) E Distance

2.7 111.6 88.6 32.5 4.29 49.0 2.38 -4 21 2.16 104.7 76.1 13.0 3.28 25.4 3.96 -1 45 2.20 113.7 55.3 40.9 4.22 35.9 8.10 -9 49 2.26 101.0 60.8 8.8 3.69 33.2 3.70 1 57 3.5 113.8 81.0 15.1 3.62 28.3 8.40 -9 80 4.5 119.7 81.0 13.0 3.70 29.1 6.11 7 113 4.12 98.3 59.1 1.7 2-10 18.7 3.81 12 131 4.19 92.9 78.3 2.9 3.10 23.2 1.68 12 140 4.27 103.0 100.9 10.6 3.20 25.1 2.15 12 150 4.34 124.6 94.4 22.5 3.70 26.2 6.80 17 162 4.35 131.5 68.4 25.2 3.72 31.7 2.51 10 165 4.36 94.7 107.4 3.7 3.10 33.8 2.39 12 167 5.3 129.1 87.2 8.5 3.50 29.2 3.27 10 178 5.4 88.1 81.3 4.0 2.68 26.0 2.22 2 183 5.5 89.6 78.2 20.5 3.50 27.7 4.79 2 195 5.6 106.1 139.5 6.2 2.50 34.2 2.32 5 205

Exposure

(“u)

94.5 96.5 91.0 97.0 91.0 98.0 100 100 100 100 100 100 100 97.5 97.5 98.5


TABLE 2. Results of stepwise multiple regression between production and turnover times of litter components and stand characteristics. Only statistics of variables included in the equations are given

Dependent variable

Independent variable in equation and regression coefficients

Variable Slope Constant r

Production of leaf litter

Reproductive plus frass Wood Total litter

Ht 12.03 67.14 0.0415 - - - -

Ht 15.72 -38.65 0~0001 dbh 2.016 145.50 0.0436

Residence time of

leaf litter Exposure 0.055 -5.77 0.0030 Reproductive plus frass Crabs -0.083 1.479 0.0246 Wood Ht -4.02 22.51 0.0054 Total litter Exposure 0.058 -5.91 0.0023

TABLE 3. Results of stepwise multiple regression between litter production and climatic conditions during the study period. Only statistics of variables included in the equations are given

Dependent variable

Independent variable in the equation and and regression statistics

Variable Slope Constant P

Production of leaf litter Totevap 0.051 1.889 0.0009

Globrad - 0.430 Reproductive plus frass Rain 0.0059 0.372 0.0113 Wood Temp 0.013 -0.097 0.0037 Total litter Rain 0.0060 2.126 0.0098

TABLE 4. Results of a Mann-Whitney U-test for yearly differences in standing biomasses of total litter and the three components. Values are g dry wt. 0.25 m-* f S.D.

Sample N Leaf Wood Reproductive

plus frass Total

1986 84 106.5 k 44.8 40.5k31.1 73.9 * 57.1 220.9* 98.1 1987 81 94.3 + 37.0 50.2 k 43.9 106.4k91.9 250.9& 118.4

0.1162 0.1857 0.0513 0.1398

84 S. Y. Lee

TABLE 5. Summary of the production, standing biomass and residence time of litter in the tidal shrimp pond

Component

Annual production (t ha-l yrr ‘)

Mean standing biomass (t ha-‘)

Residence time

(days)

Leaf litter 5.971 4,051 252 Reproductive plus frass 4.418 3,705 300 Wood 0.681 1.828 980 Total litter 11.070 9.587 317

Experiments showed that the grapsid crabs Chiromanthes bidens and C. maipoensis consumed between 22.78 to 38.38 mg dry wt of K. candel leaves per gram crab weight per day (Poovachiranon, in press) and further experiments suggested even higher consumption rates (unpublished data). As these crabs would be able to consume only moist leaves, inundation would control turnover rates via regulating the palatability of the leaves to the crabs.

Multiple regression also suggests that crabs are important regulators of the turnover rates of the reproductive plus frass component. Watson (1928) documented attack on Rhizophora conjugata seedlings by Sesarma taeniolata and protective measures had to be undertaken in plantations. Similar observations were reported by Macnae (1968) and Smith (1986, 1987), the former further attributing crab consumption to the scarcity of fallen leaves on the mangrove floor. Robertson (1986) assessed quantitatively the importance of sesarmid crabs to litter turnover in tropical Australia and stressed their importance in Indo-Pacific mangrove ecosystems. Chiromanthes at Mai PO were often observed feeding on detached droppers. Consumption of these fleshy droppers, unlike the leaves, seems independent of moisture regimes. Further, these crabs fragment leaf litter and return the nutrients as faecal pellets or shredded pieces which are easier to degrade and export as POM or DOM (Leh & Sasekumar, 1985; Maruno, 1987; Robertson, 1987; Sasekumar & Loi, 1983). The high densities and biomasses of these crabs, added to their high consumption rates, warrant a reappraisal of their roles in the structure and function of mangrove ecosystems.

Litter under these K. candel stands in the pond was, thus, predominantly processed by either in situ microbial decomposition or crab consumption. Export, which is largely responsible for the much lower standing litter biomass at normally inundated stands (Boto &Bunt, 1981), is unimportant (Figure 3). This has created large nutrient and energy sinks under the stands, recycled only by occasional leaching of DOM and some POM during high flooding. The major sources of secondary production, the crabs and other detritivores (amphipods, lepidopteran larvae) in this semi-interrestrial habitat are not coupled to the aquatic portion of the system. This is because few predators would have the time nor the water depth to forage in these areas. The role of the mangal as an energy source as proposed by Odum and Heald (1972; 1975a; 1975b), Odum et aE. (1982) does not therefore operate under the setting of the tidal shrimp pond, as both ‘ outwelling ’ and trophic coupling are ineffective. This is largely a result of continuous accretion around the K. candel stands, due to the dominance of a mainly depositional sedimentation regime during water exchange operations (Lee, unpublished data). Although probably an important subsidy for energy in form of fine POM, sedimentation lifts the stands to

Litter dynamics of Kandelia candel in tidal ponds

Macrofaunal Macrofaunal Consumption Consumption

Microbial Microbial decomposition decomposition

, ,

Figure 3. A schematic representation of the cycling of litter from the K. candel stands of a tidal shrimp pond at Mai PO.

elevations above average water levels. Such ‘ closed circuit ’ energy cycles are themselves positive feedback systems, channeling much of the energy into secondary production of crabs and other semi-terrestrial detritivores while depleting the aquatic consumers of food and energy resources from mangrove primary production. This may explain the gradual decline in fish and shrimp production of a tidal ponds with time. The decline in overall secondary production also depreciates the value of the ponds as sanctuaries for migrant avifauna which are the top consumers in the ecosystem.

Mangroves in the tidal pond reflect energy flow patterns typical of landward mangrove communities. Because of markedly decreased inundation frequency and duration, in situ litter accumulation and turnover, low export is characteristic, resulting in localized energy flow pathways. The rapid build-up of the litter layer also further decreases inundation frequency and duration, causing low mangrove seedling survivorship on the raised and light-sheltered substrates. Any disturbance to clear away the mangroves results in colonization by terrestrial plants, e.g. A4ucuranga. These mangroves thus demonstrate an intermediate stage between the more conservative, closed terrestrial forest systems and the open, export-dominant tidal mangroves. Where succession of mangroves into terrestrial communities does occur, the importance of this integral stage in the process is apparent. The functioning of these unique, transitional, mangrove environments deserves more attention.

Traditionally, operators of the ponds favour periodic landscape restructuring to create a pattern of numerous cross bunds of Kundeliu cundel stands separated by deep channels. From the results of this study, this management practice is readily explicable, as such landscape pattern would significantly increase the portion of litter entering the aquatic sector of the pond. Landscape heterogeneity of the tidal ponds probably also affects their attraction to birds (Freemark & Merriam, 1986; Kaminski & Prince, 1981), in addition to the regulation of bird populations through food supply (Murkin & Kadlec, 1986). It therefore seems more appropriate to manage the nature reserve as a dynamic, rapidly changing habitat rather than to ‘preserve as it is’.

86 S. Y. Lee

Acknowledgements

I wish to thank World Wide Fund For Nature Hong Kong and its staff for allowing me to work in the pond under their control. The logistic support they have provided is also appreciated. I am also grateful to Prof. Brian Morton for constructive criticism of the drafts of the manuscript. This work was carried out during the tenure of a John Swire Scholarship in Wetland Ecology administered by WWFHK.

References

Boto, K. G. & Bunt, J. S. 1981 Tidal export of particulate organic matter from a Northern Australian mangrove system. Estuarine, Coastal and Shelf Science 13,247-255.

Bunt, J. S. 1982 Studies of mangrove litter fall in tropical Australia. In: Mangrove Ecosystems in Australia: Structure, Function and Management (Clough, B. F., ed.). Canberra: Australian National University Press, pp. 223-237.

Chapman, S. B. 1986. Production ecology and nutrient budgets. Methods in Plant Ecology (Moore, I’. D. & Chapman, S. B., eds). Oxford: Blackwell Scientific Publications, pp. l-60.

Chen, S., Liang, Z. St Deng, Y. 1985 The mangrove in coast of east Guangdong Province. Acta Phytoecologica et Geobotanica Sinica 9,59-63 (in Chinese).

Christensen, B. 1978 Biomass and primary production of Rhizophora apiculata Bl. in a mangrove in northern Thailand. Aquatic Botany 4,43-52.

Day, J. W., Jr., Conner, W. H., Ley-lou, F., Day, R. H. & Navarro, A. M. 1987 The productivity and composition of mangrove forests, Laguna de Terrninos, Mexico. Aquatic Botany 27,267-284.

Freemark, K. E. & Merriam, H. G. 1986. Importance of habitat heterogeneity to bird assemblages in temperate forest fragments. Biological Conservation 36,115-141.

Golley, F. B., Odum, H. T. T. & Wilson, R. F. 1962 The structure and metabolism of a Puerto Rico red mangrove in May. Ecology 43,9-19.

Gong, W. K., Ong, J. E., Wong, C. H. & Dhanarajan, G. 1984 Productivity of mangrove trees and its significance in a managed mangrove ecosystem. In: Proceedings of the Asian Symposium on Mangrove Management, Research and Development (Saepadmo, E., Rao, A. N. &Macintosh, D. J., eds). University of Malaya and Unesco, pp. 216-225.

Hosokawa, T., Tagawa, H. & Chapman, V. J. 1979 Mangals of Micronesia, Taiwan, Japan, the Philippines and Oceana. In: Ecosystems of the World. 1. Wet Coastal Ecosystems (Chapman, V. J., ed.). Amsterdam: Elsevier Scientific Publications, pp. 271-291.

Irving, R. T. A. & Leung, K. W. 1988 Landuse and landuse change in the reclaimed coastal areas of Deep Bay. Hong Kong: Centre of Urban Studies and Urban Planning, University of Hong Kong, 26 pp.

Kaminski, R. M. & Prince, H. H. 1981 Dabbling duck and aquatic macroinvertebrate responses to manipulated wetland habitat. Journal of Wildlife Management 45, l-15.

Knox, G. A. & Miyabara, T. 1984. Coastal Zone Resource Development and Conservation in Southeast Asia with Particular Reference to Indonesia. Hawaii: Unesco and East-West Center.

Leh, C. M. U. & Sasekumar, A. 1985 The food of sesarmid crabs in Malaysia mangrove forests. Malayan NatureJournal 39,135-145.

Lin, P. 1987 The mangrove ecosystem in China. In Mangrove Ecosystems of Asia and the Pacific: Status, Exploitation and Management (Field, C. D. & Dartnall, A. J., eds). Townsville: Australian Institute of Marine Science, pp. 40-52.

Lin, P., Lu, C., Lin, G., Chen, R. & Su, L. 1985 Studies on mangrove ecosystem of Jiulongjing River Estuary in China. I. The biomass and productivity of Kandelia candel community. Journal of Xiaman University (Natural Science) 24,508-514 (in Chinese).

Ling, S. W. 1977 Aquaculture in Southeast Asia: a Historical Overview (A Washington Sea Grant Publi- cation). Seattle: University of Washington Press.

Lugo, A. E. & Snedaker, S. C. 1974 The ecology of mangroves. Annual Review of Ecology and Systematics 5, 39-64.

Macintosh, D. J. 1982 Fisheries and aquaculture significance of mangrove swamps, with special reference to the Indo-west Pacific region. In Recent Advances in Aquaculture (Muir, J. F. & Roberts, R. J., eds). Canberra: Croom-Helm, pp. 5-85.

Macnae, W. 1968 A general account of the fauna and flora of mangrove swamps and forests in the Indo-west- Pacific region. Advances in Marine Biology 6,7>270.

Maruno, R. 1987 Biological research in aquatic regions in Japan. In: Mangrove Ecosystems of Asia and the Pacific: Status, Exploitation and Management (Field, C. D. & Dartnall, A. J., eds). Townsville: Australian Institute of Marine Science, pp. 70-83.


Murkin, H. R. & Kadlec, J. A. 1986 Relationships between waterfowl and macroinvertebrate densities in a northern prairie marsh. ‘journal of Wildlife Management 50,212-217.

Odum, W. E. & Heald, E. J. 1972 Trophic analyses of an estuarine mangrove community. Bulletin of Marine Science 22,671-738.

Odum, W. E. & Heald, E. J. 1975a. The detritus-based food web of an estuarine mangrove community. In: Estuarine Research. VoZume I (Cronin, L. E., ed.). New York: Academic Press, pp. 265-286.

Odum, W. E. & Heald, E. J. 19756 Mangrove forests and aquatic productivity. In Coupling of Landand Water Systems (Hasler, A. D., ed.). Berlin: Springer-Verlag, pp. 129-136.

Odum, W. E., McInvor, C. C. & Smith III, T. J. 1982 The Ecology of the Mangrove of South Florida: a Community Profile. U.S. Fish and Wildlife Service, Office of Biological Services, Washington, D.C.

Olson, J. S. 1963 Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44,322-331.

Poovachiranon, S. in press. The food of two sesarmid crabs Chiromanthes bidens and C. maipoensis in Hong Kong mangrove stands. In: Proceedings of the Second International Workshop on the Marine Flora and Fauna of Hong Kong and Southern China, Hong Kong, 1986 (Morton, B., ed.). Hong Kong: Hong Kong University Press.

Robertson, A. I. 1986 Leaf-burying crabs: their influence on energy flow and export from mixed mangrove forests (Rhizophora spp.) in northern Australia.3ournal of Experimental Marine Biology and Ecology 102, 237-248.

Robertson, A. I. 1987 The determination of trophic relationships in mangrove dominated systems: areas of darkness. In: Mangrove Ecosystems of Asia and the Pacific: Status, Exploitation and Management (Field, C. D. & Dartnall, A. J., eds). Townsville: Australian Institute of Marine Science, pp. 292-304.

Sasekumar, A. & Loi, J. J. 1983 Litter production in three mangrove forest zones in the Malay Peninsula. Aquatic Botany 17,283-290.

Smith, T. J. III. 1987a Effects of seed predators and light level on the distribution of Avicennia marina (Forsk.) Vierh. in tropical tidal forests. Estuarine, Coastal and Shelf Science 25,43-51.

Smith, T. J. III. 19873 Seed predation in relation to tree dominance and distribution in mangrove forests. Ecology 68,266-273.

SPSS Inc. 1986 SPSS/PC+. New York: SPSS Inc and McGraw-Hill Book Company. Steinke, T. D. &Ward, C. D. 1987 Degradation of mangrove leaf litter in the St Lucia Estuary as in8uenced

by season and exposure. South AfricanJournal of Botany 53,323-328. Tomlinson, P. B. 1986. The Botany of Mangroves. Cambridge: Cambridge University Press. Twilley, R. R., Lugo, A. E. & Patterson-Zucca, C. 1986 Litter production and turnover in basin mangrove

forests in southwest Florida. Ecology 67,670-683. Watson, J. G. 1928 Mangrove Forests of the Malay Peninsula. Malayan Forest Records. No. 6.275 pp. Witkamp, M. & Ausmus, B. S. 1976 Process in decomposition and nutrient transfer in forest systems. In The

Role of Terrestrial and Aquatic Organisms in Decomposition Process (Anderson, J. M. & Macfadyen, A., eds). Oxford: Blackwell Scientific Publications: pp. 375-396.

Woodruffe, C. D. 1985 Studies of a mangrove basin, Tulf Crater, New Zealand: 1. Mangrove biomass and production of detritus. Estuarine, Coastal and Shelf Science 20,265-280.