Chapter Nineteen
The beaches on that coast I had come to visit are treacherous and sandy and the tides are always shifting things about among the mangrove roots… A world like that is not really natural… Parts of it are neither land nor sea and so everything is moving from one element to another, wearing uneasily the queer transitional bodies that life adopts in such places. Fish, some of them, come out and breathe air and sit about watching you. Plants take to eating insects, mammals go back to the water and grow elongate likefish, crabs climb trees. Nothing stays put where it began because everything is constantly climbing in, or climbing out, of its unstable environment.—EISELEY 1971
INTRODUCTION
Mangroves are complex and dynamic coastal evergreen formations, generally restricted to subtropical and tropical regions. Their widest latitudinal distribution occurs in the western Pacific, where they extend from the warm temperate parts of southern Japan through the tropics to New Zealand (Chapman 1977). Their world distribution in fact parallels those of scleractinian corals and seagrasses (McCoy and Heck 1976). Mangroves are highly productive intertidal ecosystems found mainly in sheltered coastal, estuarine and deltaic environments, where they often form distinct vegetational units at the junction of the land and the sea. Due to their intertidal habitat, mangroves are influenced by the tides and subjected to wide environmental fluctuations, notably, salinity gradients controlled partly by climatic factors (i.e., rainfall and evaporation).
Living in harsh environments, mangroves display a number of unique morphological and physiological adaptations that enable them to colonize and dominate otherwise hostile and dynamic shoreline environments (Carter 1988). Note that many processes that regulate the ecological functioning of mangrove ecosystems have their origins elsewhere (Hutchings and Saenger 1987). Since mangroves are open systems in terms of inputs and outputs of energy and matter, they are very sensitive to external influences (Chapman 1977). Mangroves also occur in offshore oceanic environments distant from the effects of terrestrial processes, as well as in isolated lagoonal environments with microtidal conditions and low salinities. In these offshore environments, mangroves invariably occur with coral reefs and seagrass beds.
The vast mangrove forests of Southeast Asia are among the most species-rich in the world, with the Indo-Malayan region recognized as the current centre of diversity (Chapman 1977). Extensive mangrove forests are also found in Nigeria (3.24 million ha), Mexico (1.42 million ha) and Australia (1.16 million ha) (Groombridge 1992). With an area somewhere between 2.5 to 3.8 x 106 ha, Indonesian mangrove forests are the most extensive in the region, and provide the nation with a rich natural resource base that cuts across numerous economic sectors (Burbridge and Koesoebiono 1980; Burbridge 1982; Djadjadiredja and Dauley 1983; Lanly and Lindquist 1985; Giesen 1993; Sukardjo 1994). Mangroves are widely dispersed throughout the Indonesian Archipelago, from the vast muddy coasts of Sumatra, Kalimantan and Irian Jaya to the shores of small oceanic high islands (Pulau Sago, Banggai Islands) as well as offshore intertidal patch reefs (e.g., Pulau Rambut, Java Sea) where they grow on coralline substrates (fig. 19.1). It is important to realize that on a geological time scale, mangrove forests of the Indonesian Archipelago are relatively recent, and ephemeral, coastal features (Eong 1993). None of the extensive mangrove forests we see today along the east coast of Sumatra, as well as along the south and west coasts of Kalimantan and Irian Jaya (e.g., Bintuni Bay), existed at the end of the last glacial maximum, some 15,000 years ago (figs. 19.2 and 19.3). At the time, present coastal areas were 100-120 m above the glacial sea level and were occupied by grasslands, shrublands or tropical inland forests (van der Kaars 1991). However, based on shelf topography, it is possible that the present-day mangrove forests in the Berau River delta (East Kalimantan) may be among the oldest mangrove communities in Indonesia.
Figure 19.1. Approximate distribution of remaining mangrove forests in the Indonesian Archipelago.
From Atmadja and Soerojo 1994.
The term mangrove has a double meaning, which may be initially confusing, since it refers both to individual species of bushes (e.g., Acanthus) and trees (Rhizophora spp.), as well as to a community consisting of one or more species (e.g., small stand or a forest) (Hutchings and Saenger 1987). It has been suggested that mangal is a more appropriate term to describe mangrove communities (MacNae 1968; Chapman 1975; Chapman 1977; Tomlinson 1986). As was pointed out by Tomlinson (1986), the term mangal defines a community of plants characterized by their association with tides and not necessarily salinity fluctuations (e.g., tidal fluctuations in the Mahakam River occur far inland without corresponding salinity changes). Since we are dealing here with plants living in coastal intertidal environments periodically inundated by seawater, the term mangrove is used interchangeably in this book according to current usage (Hutchings and Saenger 1987).
Figure 19.2. Sundaland at the height of the last glaciation some 20,000-18,000 years ago with reconstructed river systems and possible areas of mangrove occurrence. Note the absence of mangroves along the east coast of Sumatra and the south and west coasts of Kalimantan. Sea level about 120 m below present.
From MacNae 1968.
Throughout the Indonesian Archipelago, mangrove forests play a vital role in economic and social development of coastal communities. Mangrove ecosystems have a number of important functions. In addition to being physical barriers against storm waves, mangroves are productive systems that export energy and organic matter to adjacent systems, which, in turn, may support commercially important coastal finfish and shrimp fisheries. The critical role of mangrove ecosystems relates to their high primary production rates attributed to the mangroves themselves. While gross primary production rates are high (e.g., 100 mt C.ha-1.yr-1), the net production rates are similar to other shallow-water coastal systems (e.g., 18 mt C.ha-1.yr-1), mainly due to the high respiratory and metabolic requirements of the system that consumes about 80% of its gross production (Eong 1993). Organic biomass consists mostly of living mangrove vegetation and fully or partly decomposed leaf litter and roots. It is the mangrove litter which forms the basis of a complex food web that includes a variety of invertebrates (e.g., crustaceans and molluscs), fish, reptiles, birds and mammals. A number of commercially important penaeid species (e.g., Penaeus monodon and P. indicus) are associated with mangroves during certain stages of their life cycles. Martosubroto and Naamin (1977) demonstrated that there is a strong positive relationship between the surface area of mangrove forests and commercial shrimp production in Indonesian waters. Pauly and Ingles (1986) derived a logarithmic model linking penaeid shrimp yield, mangrove area, and latitude, thus supporting the long-held perception that mangrove forests play a key role in penaeid shrimp recruitment. Results from mangrove studies in Australia also support the view that mangrove forests are important habitats for many species of juvenile fish and crustaceans (Robertson and Duke 1987a). What remains to be discerned is whether mangrove forests function purely as a protective refuge for a host of marine organisms, or whether they are in fact a substantial source of organic matter and nutrients (i.e., energy) that supports adjacent coastal food webs. Recent studies have demonstrated that while mangrove forests seem to conserve and recycle dissolved material (except phosphorous species), they export a significant quantity of particulate organic matter to adjacent coastal benthic communities, mainly in the form of intact mangrove plant litter (Boto et al. 1991; Atmadja and Soeroyo 1994).
Figure 19.3. Possible distribution of vegetation types during the last glacial maximum (18,000 yrs B.P.) in eastern Indonesia and north Australia. Note that woodland-open forest vegetation in Irian Jaya covered most of the area currently dominated by mangroves (e.g., Bintuni Bay).
From van der Kaars 1991.
A comprehensive bibliography of mangrove literature was compiled by Rollet (1981), and includes articles published from the years 1600 to 1975. The main list contains 5608 numbered articles, while the total number of mangrove publications is 6000 (Rollet 1981). Articles published since 1975 are easily accessible through the Aquatic Sciences and Fisheries Abstracts (ASFA) database. Mangrove literature in Indonesia is numerous and dispersed widely in published and unpublished reports. MacNea's (1968) outstanding review of the Indo-west Pacific mangroves should be consulted to introduce the reader to a fascinating coastal ecosystem. Detailed reviews of mangrove ecosystems in Indonesia are to be found in: Whitten et al. (1987) for Sumatra; Whitten et al. (1988) for Sulawesi; MacKinnon et al. (1996) for Kalimantan; Whitten et al. (1996) for Java and Bali; and Monk et al. (in press) for the Moluccas and the Lesser Sunda Islands. Since this book is part of the Ecology of Indonesia series, only cursory review of mangroves is given, and the reader is referred to the above publications for detailed regional reviews.
MANGROVE ORIGINS
The origin of mangroves is somewhat problematic, since, unlike corals that leave well-preserved fossil remains, the mangrove fossil record is rather depauperate. It is, therefore, not surprising that little is known about the relative geological ages of most mangrove species (Tomlinson 1986). Among the oldest extant mangroves is the genus Nypa, which dates to the Cretaceous (c. 63 MaB.P.), while Rhizophora dates to the Eocene (c. 30 Ma B.P.). Mangroves are widely distributed throughout the tropical and subtropical regions and penetrate into the warm temperate northern and southern latitudes in the Atlantic, Indian and Pacific Oceans (Chapman 1977; Tomlinson 1986). A comprehensive treatment of mangrove biogeography is given by Barth (1982).
The most visible feature of mangrove distribution is that the best- (i.e., largest) developed forests occur in sheltered environments, where, invariably, major rivers debouch into the sea (Chapman 1977). From a worldwide perspective, mangroves have a bimodal tropical distribution, when viewed along a longitudinal axis, since there are two main centres of mangrove diversity (fig. 19.4). The western centre of diversity includes west Africa, Atlantic South America, the Caribbean, Florida and Bermuda, Central America, and Pacific North and South America (Tomlinson 1986). The eastern centre covers the Eastern Hemisphere from east Africa to the western Pacific, and contains 40 true mangrove species (Tomlinson 1986). Figure 19.4 clearly illustrates the large floristic disparity (i.e., five-to-one) between the two mangrove diversity centres, closely reflecting similar patterns found in reef-building corals and seagrasses. The close co-occurrence of the three major shallow-water coastal ecosystems points to a similar evolutionary explanation for their distributional patterns, a topic which is receiving much attention.
Figure 19.4. Global distribution of mangroves. Above: approximate distributional boundaries for west and east mangrove groups. Some overlap may exist in the western Pacific (Rhizophora samoensis) (arrow). Below: The bimodal distribution of mangroves, illustrating differences in species richness between the western and eastern groups.
From Tomlinson 1986. (p. 41; fig. 3.1)
Mangroves can be viewed as products of convergent angiosperm evolution, where plants from different families have evolved similar adaptations that enabled them to colonize and reproduce in harsh tropical intertidal environments. It has been suggested that the evolution of mangroves necessarily postdates the evolution of the seed (an adaptation to terrestrial living), which offered early plant embryos protection from desiccation and salt water (Raymond and Phillips 1983). This evolutionary breakthrough occurred at the end of the Devonian (360 Ma B.P.), and made possible the subsequent emergence of flowering plants (i.e., Angiosperms), including present-day mangroves (c. 55 species and 20 families; Tomlinson 1986). While stilt-roots are not in the strictest sense characteristic of mangroves, since they occur in recent freshwater-wetland species, these mangrove-like features were present in early Cordaitales during the Carboniferous period (365 Ma B.P.) (Cridland 1964 cited in Tomlinson 1986). By the early Cretaceous angiosperm diversification was well underway, and by the late Cretaceous they became the dominant plants on the planet. Retallack and Dilcher (1982) suggested that angiosperm radiation may well have originated from coastal environments. King et al. (1990) suggested that mangroves may have been the first established angiosperm-vegetation types, based on fossil evidence of early Tertiary pollen types that are similar to those of present-day mangroves (Muller 1970).
There are several hypotheses to explain present-day mangrove distribution patterns, a number of them sharply contrasting (reviews in Chapman 1977; Tomlinson 1986; Hutchings and Saenger 1987). However, it seems that mangrove origins stem from the coasts of the early Cretaceous Tethys Sea that separated the northern Laurasia from the southern Gondwana. According to Tomlinson (1986), the species-rich Indo-Malayan region is a relict of their origin somewhere on the eastern margin of Laurasia. Specht (1981) is, however, of the opinion that the centre of origin was most likely along the southwestern and northern shores of Australia and Papua New Guinea and not in the Malayan Archipelago. The present-day bimodal distribution (i.e., Atlantic vs. Indo-Pacific) is probably the result of the closure of the Tethys Sea that subsequently prevented further dispersal, and made the present-day Mediterranean too harsh an environment for mangrove vegetation. Since the Atlantic and Indo-Pacific share three mangrove genera (i.e., Avicennia, Rhizophora and Hibiscus), it is assumed that they are the earliest mangroves to have evolved and dispersed (Hutchings and Saenger 1987).
ENVIRONMENTAL REQUIREMENTS
Chapman (1977) identified seven key environmental factors that, to a large extent, determine the distribution of mangroves, namely: 1) air temperature; 2) protected coastlines; 3) currents; 4) substrate type; 5) shallow shores; 6) salt water; and 7) tidal range.
1. Temperature. Considering the humid equatorial climate that predominates throughout much of the archipelago, air and water temperatures probably play a relatively minor role (if at all) in determining mangrove distributions and structuring of mangrove communities. The average air and water temperatures of the coldest month in Indonesia are well above the minimum values required for vigorous mangrove development (i.e., 20°C and 24°C, respectively) (Chapman 1977; Hutchings and Saenger 1987). For example, Danielsen and Verheugt (1990) reported that the minimum average sea temperature of the coldest month in South Sumatra was 23°C, while the maximum average temperature of the warmest month was 32°C. Water temperatures in the shallow regions of the west Java Sea generally do not drop below 27°C. However, coastal upwelling in the eastern regions of the archipelago periodically brings up cold water (as low as 14°C; C. Cook, pers. comm.) that may impinge on mangroves (e.g., Komodo, Alor, etc.). These temperature "shock" events have an insignificant effect on mangroves in general.
As was pointed out earlier, coral reefs and mangroves have similar latitudinal distribution patterns. Interestingly enough, as is the case with corals and coral reefs, individual mangrove species have much wider latitudinal distributions than do the mangrove forests. For example, Chapman (1977) points out that Avicennia germinans in Florida can tolerate minimum temperatures of 12.7°C and 10°C in Brazil. Sheppard et al. (1992) report that Avicennia marina, which has a wide distribution throughout the archipelago, is a eurythermal and euryhaline species able to tolerate a wide range of seawater temperatures (12°C-35°C) and salinities (40-50 psu). In Indonesia, Avicennia spp. dominate many arid intertidal coastal areas in Nusa Tenggara (e.g., Solor Strait), where excess evaporation during die hot and dry Southeast Monsoon raises salinities in intertidal areas exposed during peak insolation periods.
2. Sheltered environments. Throughout the archipelago mangrove forests occur mainly in sheltered environments protected from strong wave action. Chapman (1977) stated that mangroves generally do not become established in areas where seedlings cannot take root. While this seems quite logical, it is also clear that wave action covers a wide spectrum of energies which fluctuate daily, monthly and yearly, depending on weather conditions. Within the archipelagic seas, external influences from the Pacific and Indian Oceans (i.e., storm-generated waves) are greatly minimized and do not play a significant role in structuring of mangrove communities. Once established, mangroves are robust plants that can withstand the force of tropical cyclones, as is quite evident from the Sunderbans in Bangladesh. * Much of the Indonesian Archipelago is influenced by a strong monsoonal climate with seasonal shifts in wind and wave direction. Most coastlines in the archipelago are therefore sheltered, at least during part of the year", which may provide sufficient time for mangrove seedlings to become established. Extensive mangrove forests that cover the relatively exposed coastlines of South Kalimantan may benefit from the seasonal fluctuations in the strength and direction of wind-generated waves associated with the monsoonal shifts in weather patterns. However, the effects of wave action on mangroves have not been fully quantified.
3. Oceanic currents. Oceanic currents have been noted as essential for mangrove dispersal, and thus a major factor in mangrove biogeography (Chapman 1977; Hutchings and Saenger 1987). However, the effects of strong longshore currents that frequently occur throughout many regions of the archipelago have yet to be considered for their contribution to mangrove development. Note that strong currents are not necessarily detrimental to mangrove development. For example, the luxuriant intertidal mangrove forest on Samama Island (East Kalimantan) is often swept by tidal currents than exceed velocities of 1 m.sec-1. An abundance of Rhizophora spp. seedlings suggests that high current velocities do not prevent establishment of mangroves.
4. Substrate type. The majority of the extensive mangrove forests in Sumatra, Kalimantan, Sulawesi and Irian Jaya are associated with mud and muddy fluvial deposits. This fits well with the general preference of most mangroves for soft-bottom substrates (Chapman 1977; Hutchings and Saenger 1987). However, there are exceptions, and mangroves are known to have developed on pure calcareous substrates associated with offshore patch reefs and coral cays. Examples of well-developed mangrove forests associated with coralline substrates are Pulau Rambut (Jakarta Bay) and Pulau Panjang (Berau Islands, East Kalimantan). The establishment of mangroves has contributed to the growth of both cays, since, once established, mangroves facilitate sedimentation and accumulation of new sediments along their seaward margin. New seedlings of Rhizophora are frequently seen at the outer margin of the coral-associated mangroves. In contrast, the seaward margins of mangrove forests in Bintuni Bay (Irian Jaya), are dominated by seedlings and young plants from genus Avicennia. Erftemeijer et al. (1989) characterized this zone as a pioneering Avicennia forest, which is frequently dominated by Avicennia marinaas well as A. eucalyptifolia. In South Sumatra, Avicennia marina dominates coastlines with soft muddy substrates, while Sonneratia alba becomes dominant on firm soils (Danielsen and Verheugt 1990).
5. Shallow shelf. Chapman (1977) points out that extensive mangrove forests are invariably associated with shallow and gently sloping shelves that extend long distances offshore. These conditions exist along the east coast of Sumatra (i.e., Strait of Malacca), the east, south and west coasts of Kalimantan, and the southwest coast of Irian Jaya (i.e., Arafura and Halmahera Seas). Not surprisingly, these are the regions with the most extensive mangrove forests in the archipelago. Figure 19.5 illustrates the extent of mangrove development in Bintuni Bay, Irian Jaya, which, according to Erftemeijer et al. (1989), extend up to 30 km inland. The eastern part of Bintuni Bay contains numerous large and actively expanding mangrove islands. The mangrove vegetation is dominated by Rhizophoraceae, Sonneratiaceae and Verbenaceae, with Rhizophora, Bruguiera, Sonneratia and Avicenniabeing the most abundant genera. These forests are considered to be the most extensive (i.e., 260,000 ha), best-developed and least-disturbed mangrove areas in Southeast Asia (Erftemeijer et al. 1989). Similar conditions exist along the east coast of South Sumatra, where a wide contiguous belt of mangrove swamps covers the coastal area of low-lying alluvial plains. According to Danielsen and Verheugt (1990), the extensive (i.e., 195,000 ha) mangrove forest in South Sumatra forms a continuous belt along the shallow coastal areas, extending some 35 km inland (fig. 19.6).
6. Salinity. Only a few plants are able to thrive under saline conditions and mangroves are such a group. Mangroves are halophytic (i.e., salt-tolerant), phanerogamic plants able to survive in coastal environments frequently inundated by seawater. Many mangrove species, such as Rhizophora stylosa, are able to tolerate very high concentrations of sodium chloride (salt), and are frequently found on offshore patch reefs in full-strength seawater. As mentioned earlier, Avicennia marineis among the most euryhaline mangrove species.
It is generally agreed that mangroves are not obligate halophytes, even though many show improved growth (and size) at moderate salinities. Chapman (1977), however, suggested that Rhizophora is most likely an obligate halophyte, its growth being poor or reduced under glycophytic conditions (i.e., < 0.5% NaCl). It is a general consensus that under saline conditions the halophytic lifestyle provides the relatively slow-growing mangroves with a competitive advantage over the faster-growing glycophytes (i.e., non-salt-tolerant plants) (Hutchings and Saenger 1987). Along rivers where seawater penetrates far inland, mangroves frequently dominate the riverbanks. Further upstream where fresh water conditions predominate, mangroves are quickly replaced by fast-growing freshwater wetland vegetation. The distance that seawater penetrates upstream depends on tidal conditions and topography. Hardenberg (1937) studied the hydrology of the Kumai River (9-15 m deep), and demonstrated that saltwater intrusion occurs as far as 37 km upstream. The Kumai River is located in Central Kalimantan and empties into Kumai Bay, Java Sea. The river apparently contains only small amounts of mud during some parts of the year. The river is rainfall-dependent, with highest flow volumes during the Northwest Monsoon (i.e., rainy season) (Hardenberg 1937). Along most of its length the river is fringed by tropical lowland forest, with Nypa and mangroves becoming the dominant vegetation near the estuary. Figure 19.7 illustrates the intrusion of seawater into the upper regions of the river.
Figure 19.5. Map of Bintuni Bay showing the extent of mangrove forests associated with shallow shelves.
From Erftemeijer et al. 1989.
Figure 19.6. Interpretation of SPOT satellite image of Sembilang Wildlife Reserve in South Sumatra showing the extent of mangrove forests along the shallow shelf. The 5 m isobath is located 10-15 km offshore.
From Danielsen and Verheugt 1990 (p. 210; Spot map).
Figure 19.7. Seawater intrusion into Kumai River, Central Kalimantan, during wet and dry seasons. (Conversion: 1 nautical mile =1.853 km). Negative values imply upstream direction from river mouth. Salinity in psu (physical salinity units formerly ppt).
Studies from South Sumatra provide additional support for the above generalization. At the mouth of the Simpangalangan River, South Sumatra, where salinities of coastal waters fluctuate between 26-32.7 psu, Rhizophora apiculata (12-15 m high) is one of the dominant mangrove species (Danielsen and Verheugt 1990). About 8 km upstream moderate salinities predominate and R apiculata is replaced by tall R mucronata (20-25 m high). As one moves further inland and conditions become gradually more glycophytic, R. mucronata trees become progressively shorter. Fifteen kilometres from the river mouth, R mucronata is restricted to the riverbank and the trees are only 3 m tall. Danielsen and Verheugt (1990) reported that saline intrusions in a number of South Sumatra rivers are noticeable some 3060 km inland, however, Rhizophora seems to be absent from these areas. Along the Musi River, Sonneratia caseolaris is the dominant vegetation up to Palembang, 85 km from the sea (Danielsen and Verheugt 1990).
7. Tidal range. According to Chapman (1977), the greater the tidal range the greater the vertical range available for mangrove communities. However, local topography (land elevation and shelf slope) plays an important role as well. Most extensive mangrove development occurs on shallow, gently sloping shorelines and flat alluvial plains. Wide tidal range is, however, not necessary, since mangroves occur even under microtidal conditions (e.g., 19 cm; Kakaban Lagoon) (Tomascik and Mah 1994). While Chapman (1977) considered tidal range to be an important factor, the importance of topography can be illustrated by examples from South Sumatra and Bintuni Bay. In both areas mangroves penetrate as far as 30 km inland, yet the maximum tidal amplitude (V2 of tidal range) in South Sumatra is 1.75 m (Danielsen and Verheugt 1990), while in Bintuni Bay the maximum tidal amplitude is 5.6 m (tidal range of 11.2 m) (Erftemeijer 1989). While tides are not a direct physiological requirement (Hutchings and Saenger 1987), they inundate coastal areas with seawater, which is essential for most mangroves. Tides also play an important role in the ecological functioning of the system, since tidal currents are the primary means by which nutrients and organic matter are transported into, through and out of the mangrove system.
Figure 19.8. Sonneratia and Awcennia-dominated mangrove at low tide. Note the drained tidal creek through which seawater is channeled in and out of the mangrove.
Photo by Tomas and Anmarie Tomascik.
MANGROVE ADAPTATIONS
The daily rise and fall of the tides results in repeated inundation of mangroves in a saline medium and creates environmental conditions that are generally harmful to most other phanerogamic (seed-bearing) plants (fig. 19.8). Soil conditions fluctuate from low salinity to high salinity, and most often the soil is anoxic and waterlogged (King et al. 1990). Superimposed on the daily tidal cycle are the daily fluctuations in insolation and annual fluctuations in rainfall that render coastal intertidal mangrove habitats highly dynamic and generally stressful systems for most organisms. Mangroves were able to colonize these inhospitable environments through the development of numerous specialized morphological, anatomical, physiological and reproductive adaptations which provide protection against extreme fluctuations in physico-chemical parameters (Hutchings and Saenger 1987).
The presence of high salt concentrations is one of the key characteristic features of the mangrove environment. Among halophytes there are a variety of adaptive responses to deal with salinity, which often relate to the distribution of different species (Tomlinson 1986). It has been demonstrated that some mangrove species exhibit growth stimulation with addition of salt (e.g., Rhizophord), while optimal growth of other mangrove species seems to occur under more fresh water conditions (e.g., Oncosperma tigillarium).
Living in a saline environment requires mangroves to deal with excess salt. Based on how they control internal NaCl concentrations, mangroves are divided functionally into three main groups: 1) those that secrete salt (salt-secretors); 2) those that do not (salt-excluders); and 3) those that accumulate salt in their tissue (accumulators) (Scholander 1968; Tomlinson 1986; Hutchings and Saenger 1987). The nonsecretors include genera such as Rhizophora, Sonneratia, Lumnitzera, Hibiscus and Eugenia, while the secretors are Aegiceras, Aegialitis and Avicennia (Tomlinson 1986). Species from both the secretors and nonsecretors, as well as Xylocarpus, Excoecaria, Osbornia, Ceriops, Bruguiera, etc., accumulate NaCl in various parts of plant tissue (e.g., bark or leaves) (Atkinson et al. 1967; Jenning 1968). Many species of mangroves employ one or a combination of the above salt-regulating mechanisms, which are not mutually exclusive (Hutchings and Saenger 1987).
Figure 19.9. Salt glands in:(A) Aegiceras corniculata, and (B) Acanthus ilicifolius.All are transverse sections of adaxial epidermis. (C) cuticle.
Modified from Tomlinson 1986.
Salt Secretion
A number of mangrove species possess specialized salt glands (fig. 19.9) in their leaves that enables them to secrete solutions of Na+ and CI-. These salt-secreting structures are trichomes, which are outgrowths of the epidermis. Salt glands are present in Avicennia, Sonneratia, Aegiceras, Aegialitis, Acanthus and Laguncularia(Hutchings and Saenger 1987). In addition, the cork warts in the leaves of Rhizophora may possibly function as salt-secreting glands (Hutchings and Saenger 1987). Many species with salt glands (e.g., Aegiceras corniculatum) have their leaves frequently covered by numerous white salt crystals.
The general cellular structure of salt glands varies among families, but is surprisingly uniform within a family (King et al. 1990). Salt glands in mangroves have most likely evolved from pre-existing excretory structures, and are, in fact, excellent examples of convergent evolution (Tomlinson 1986; King et al. 1990). The secreting activity of salt glands appears to be highest during daylight hours (c. 90 p-equiv.Cl-.cm-2.sec-1), dropping by more than 90% in the dark (Atkinson et al. 1967). While the mechanism of salt secretion is not well understood, it is clear that it requires energy which is probably derived from respiratory processes (Clough et al. 1982). It has been demonstrated that major ions (i.e., Na+, K+ and CI-) are moved out of the parenchyma by an active transport system, operated by the gland cells, that can be stopped by metabolic inhibitors (Cardale and Field 1975). The most efficient salt glands are present in Avicennia, which is able to tolerate highly saline conditions. In Avicennia salt glands develop only under saline conditions (MacNae 1968). However, in many other species salt glands develop whether or not salt is present in the substrate (e.g., Aegiceras) (Cardale and Field 1971). Salt glands are totally absent from species found growing in fresh water (e.g., Acanthus) (Mullan 1931).
Salt Exclusion
Most mangroves regulate their salt intake through an efficient ultra-filter that presumably exists in their roots (Scholander 1968). Most other vascular plants also possess roots capable of selective ion uptake and transport to xylem, and mangrove roots are not much different in this respect. A number of physiological studies on mangroves have demonstrated that they are able to efficiently exclude salt (NaCl) from xylem (i.e., water transport system) (Scholander et al. 1962,1966; Atkinson et al. 1967; Scholander 1968). Among the most efficient salt excluders are Rhizophora, Ceriops, Sonneratia, Avicennia, Osbornia, Bruguiera, Excoecaria, Aegiceras, Aegialitis, and the fern Acrostichum. During water uptake these mangroves are able to exclude as much as 95%-98% of the salt in seawater (Scholander et al. 1962,1966; Atkinson et al. 1967; Scholander 1968). According to Clough et al. (1982), the low salt content in mangrove xylem sap is primarily due to selective discrimination against Na+ cations, and that CI- anions are regulated to maintain ionic balance in the xylem sap following the exclusion of Na+. While the system is efficient, it does not exclude all the salt, which is reflected in high concentrations of salt in xylem sap (i.e., about 10 times that of secretors). Note that mangroves with salt glands are able to exclude only 80%-85% of salt in seawater. In general, mangrove species exhibiting the most efficient salt exclusion lack the capacity for salt secretion (King et al. 1990). Some of the accumulated salt is disposed of by cuticular transpiration, but the most obvious mechanism is through leaf shedding. Note, that many mangrove species apparently exclude Na+ and CI- from the xylem sap under rapid transpiration. Scholander (1968) was able to show that salt exclusion is most likely a passive process linked to differential permeability of root membranes. Nonetheless, the exact process by which the high exclusion rates are achieved in most mangrove species remains obscure (King et al. 1990).
Salt Accumulation
Salt accumulation occurs in most mangrove species in bark, roots or leaves, and in general salt content of foliage increases with age. A number of nonsecreting mangroves maintain salt balance by diluting incoming ions either by growth or increased succulence (King et al. 1990). Increase in leaf succulence in mangroves is associated with the presence of a well-developed, large-celled, water-storing hypodermis as well as strongly developed palisade mesophyll tissue and small intercellular space volume (Saenger 1982). Concentrations of Na+ and CI- in the leaves of Rhizophora mucronata are high, but relatively constant, for much of the life of a leaf (King et al. 1990). Increased leaf succulence increases cell volume, thus diluting the incoming ions (King et al. 1990). In mangroves such as Sonneratia, Excoecaria and Lumnitzera, salt accumulates in old leaves and photosynthetic stems. When these structures are shed, it may appear that large quantities of excess salt are removed from the metabolic tissue (Hutchings and Saenger 1987). Annual leaf fall in Xylocarpus and Excoecaria may be an important mechanism for removal of large quantities of salt from the plant tissue. However, Clough et al. (1982) point out that there is very little evidence to support this contention, since shedding does not appear to decrease the average salt content per unit dry weight of the plant.
Even though halophytes have much higher salt concentrations in their tissue than glycophytes, their salt tolerance (i.e., sensitivity of enzymes to salt) is not much different (King et al. 1990). It is a well-known fact that enzyme systems of higher plants are highly sensitive to high salt concentrations (i.e., loss of function at high salt concentrations) (Flowers et al. 1977). It has been suggested that mangroves maintain cellular regions of high metabolic activity free from contact with high salt levels by sequestering salt in specialized vacuoles where it does not interfere with enzyme function. Low cytoplasmic salt levels are maintained by balancing the water potential of the cytoplasm and the vacuole by the presence of harmless organic solutes (e.g., glycinebetaine), that achieve a water potential equal to that of the vacuole (Hutchings and Saenger 1987). In many halophytes, osmotic adjustment in the cytoplasm is thought to be maintained by accumulation of proline (an amino acid) as well as choline and betaine (ammonium compounds) (Flowers et al. 1977). It is probable that this process also occurs in mangroves, since Clough et al. (1982) reported choline sulphate in mangroves, as well as positive correlation between substrate salinity and concentrations of choline and betaine in leaves of some mangrove species.
Water Conservation
It may seem ironic, at first, that mangroves which live in an aquatic environment surrounded by water have a water shortage problem. However, we need to keep in mind that the aquatic medium is saline compared with mangrove tissue concentration, and water uptake must necessarily occur against an osmotic gradient. The average salt content in seawater is about 35 grams solute per litre (NaCl) with an osmotic potential of about -2.5 MPa (1 MPa = 10 bars). Thus mangroves have to generate an additional 2.5 MPa of hydrostatic pressure to maintain water balance comparable to plants rooted in fresh water (Tomlinson 1986). For mangroves to move water from sites of absorption (i.e., root hairs and roots) to sites of transpiration (i.e., leaves), representing a height difference of up to 40 m, a negative hydrostatic pressure gradient must be maintained by lowering water potential (ψ or psi) in plant tissue. In mangroves, this is accomplished through uptake of salt, since salt is the most readily available solute with which to develop low internal osmotic potentials (King et al. 1990). During transpiration, mangroves maintain lower water potential in their xylem elements, compared to seawater, thus preventing backflow to the substrate. If water potential of xylem cells exceeds that of the seawater, water will flow back into the sea (Tomlinson 1986), since water will always flow passively from a location with greater water potential to a location where water potential is less. Water in mangroves, like all plants, is moved up the xylem vessels by root pressure and transpiration pull along a gradient of decreasing water potential (fig. 19.10). Note that in most plants, root pressure is not a major mechanism driving the ascent of xylem sap. Nonetheless, the process requires energy since, to maintain lower water potential in plant tissue, ions (salt) must be pumped into the xylem, which is an active transport powered by ATP generated during respiration. The major force driving water molecules (and ions) from roots to leaves (up the xylem vessels) is the transpiration pull. This is a physical process powered by solar energy through evaporation of water from leaves, which maintains lower water potential in the leaves relative to roots. The cohesion of water due to hydrogen bonding transmits the upward pull along the entire length of the xylem vessels to the roots. The upward flow of sap also creates a certain amount of tension (i.e., negative pressure) within the xylem, which further reduces the water potential inside the transport system.
Figure 19.10. Schematic illustration of the ascent of water in a mangrove tree. The primary force that drives the ascent of xylem sap (water) is the gradient of water potential (ψ). Common values for ψ for mangroves rooted in seawater.
From Tomlinson 1986.
Active water transport against an osmotic gradient, which basically involves desalination, requires substantial expenditure of energy. Therefore, the amount of fresh water available to mangroves depends on the amount of metabolic energy the plants can make available for desalination. To prevent unnecessary loss of fresh water from the tissue, mangroves have developed various specialized adaptations that are generally associated with plants from arid regions (Hutchings and Saenger 1987). These xeromorphic features include a thick-walled epidermis covered on the upper leaf surface by a thick waxy cuticle. This feature is a well-known adaptation to prevent water loss through evaporation, and may be of considerable benefit in more arid regions (e.g., East Nusa Tenggara). In some species with secreting salt glands, these structures, as well as stomata, are covered by hairs (e.g., Avicennid) or scales (e.g., Heritiera) (Hutchings and Saenger 1987). All mangrove leaves have well-developed stomata (pores) which are restricted mainly to the underside of leaves. Stomata function in gas exchange, and therefore considerable water losses are known to occur through evaporation, and water loss is most immediately controlled by stomatal closure (Tomlinson 1986). In many mangrove species the stomata are sunk into the epidermis (e.g., Avicennia, Aegiceras, Bruguiera, Ceriops, Lumnitzera and Rhizophora) (Hutchings and Saenger 1987). Another important water storage adaptation in mangroves characteristic of xeromorphic plants is succulence. Leaves of both Rhizophora and Sonneratia are very succulent and able to store water. It has been shown that succulence in these two species is a direct response to the presence of chloride ions (Hutchings and Saenger 1989).
In addition to these basic xeromorphic features, mangroves have a number of specializations related to the structure of their vascular bundles, leaf anatomy (e.g., stone cells) as well as anatomy of the wood. The combined effects of these adaptive features in mangroves is a significant reduction in transpiration.
Root Adaptations
'Waterlogged' and 'anoxic' are two characteristic descriptions of mangrove substrates. Waterlogging is a function of elevation and the composition of the substrate (King et al. 1990). In waterlogged soils with high inputs of organic matter anoxic conditions are frequently encountered. The black anoxic and semi-fluid mangrove sediments - which provide little mechanical support - as well as the smell of H2S are the hallmarks of mangrove swamps worldwide. To cope with these adverse conditions, many mangrove species have developed highly specialized adaptations (morphological, physiological and anatomical) in their root systems. Most mangrove root systems are characterized by laterally spreading subsurface cable roots (fig. 19.11), from which numerous smaller vertically descending anchor roots, bearing fine nutritive roots, branch out (Hutchings and Saenger 1987). A number of mangroves do not possess any root specialization (e.g., Aegialitis, Excoecaria), however, their roots are located on or near the substrate surface (Hutchings and Saenger 1987). High substrate to above-ground biomass ratio may be an adaptation to unstable substrate conditions. For a comprehensive review on the structure and function of mangrove root systems refer to Tomlinson (1986).
The various root morphologies present in mangroves can be conveniently grouped into four main types: 1) stilt roots (fig. 19.12); 2) pneumatophores (fig. 19.13); 3) knee roots (fig. 19.14); and 4) buttress roots. The stilt roots characteristic of Rhizophora are perhaps the most conspicuous and the most familiar of all mangrove roots (fig. 19.15). These roots arise from the main trunk and lower branches of Rhizophora and grow downward into the substrate. The above-ground looping cable roots function in gas exchange, while the below-ground roots function in water transport and support. In older trees the stilt roots form flying buttresses that support the mature Rhizophora trunk which becomes obconical at the base (Tomlinson 1986). Stilt roots are not restricted to Rhizophora and occur to a limited extent in Bruguiera and Ceriops. Under certain conditions, stilt roots can also be very common features of Avicennia officinalis and A. alba.
Pneumatophores are erect roots that project vertically from the subterranean cable roots and are subaerially exposed (fig. 19.16). A number of mangrove genera have pneumatophores, each with unique features characteristic of a genus or a group of species (Tomlinson 1986). The main function of pneumatophores is gas exchange. The pneumatophores of Avicennia and Sonneratia are quite similar and are basically erect lateral branches of the buried horizontal cable roots which originate at the base of the trunk. While the general morphology of the erect pneumatophores is very similar between the two genera, their height varies. In Avicennia, the smooth, spongy pneumatophores extend less than 30 cm above the substrate, while in Sonneratia a height of 3 m has been recorded (Tomlinson 1986). In Sonneratia the pneumatophores are covered by bark (fig. 19.17). Under certain environmental conditions, the roots of Laguncularia sometimes develop erect and blunt pneumatophores, which rarely exceed a height of 20 cm (Tomlinson 1986). According to Hutchings and Saenger (1987), pneumatophores are also present in Bruguiera, Camptostemon, Lumnitzera and Osbornia.
Figure 19.11. Mangrove cable roots branch out laterally from the main trunk and give rise to various modified roots for anchoring as well as water and nutrient uptake.
Photo by Tomas and Anmarie Tomascik.
Figure 19.12. The stilt roots of Rhizophora apiculata.
Photo by Tomas and Anmarie Tomascik.
Figure 19.13. Mangrove pneumatophores function primarily in gas exchange. A) Sonneratia sp. B) Avicennia sp.
Photos by Tomas and Anmarie Tomascik.
Figure 19.14. A) The knee roots of Bruguiera gymnorrhiza. B) The roots of Excoecaria sp.
Photo by Tomas and Anmarie Tomascik.
Figure 19.15. Schematic illustration of a stilt root system that may be found in various forms in groups such as Rhizophora, Bruguiera, Ceriops, Lumnitzera and Avicennia. The stilt roots are, however, a characteristic feature of the genus Rhizophora.
Figure 19.16. Schematic illustration of pneumatophores characteristic of Avicennia and Sonneratia. The above-ground pneumatophores function in gas exchange.
Figure 19.17. Submerged pneumatophores of Sonneratia sp. on Samama Island, East Kalimantan. Samama Island is an intertidal mangrove cay about 50 km east of the Berau River. Note Holothuriasp. (front left) and two seastars (Protoreaster nodosus) among the pneumatophores (centre). Seagrasses are Cymodocea rotundata and Thalassia hemprichii. A school of Choerodon anchorago (yellow-cheeked tuskfish) at the back, two spinecheeks (Scolopsis sp.) at front.
Photo by Anmarie and Tomas Tomascik.
Knee roots are modified sections of the below-ground cable roots and are characteristic features of a number of species of Bruguiera and Ceriops (fig. 19.18). As the near-surface horizontal cable roots grow outwards from the trunk, they periodically grow upwards and then downwards again, forming distinct knee-like loops, which are the result of primary growth. The size, shape and frequency of these loops is species-specific, but variable according to substrate conditions (Tomlinson 1986). In Lumnitzera, the small knee roots are basically secondary structures derived from lateral branches of the main cable roots. The blade-like knee roots of certain species of Xylocarpus are produced by localized cambial activity and may reach a height of 30-50 cm.
Figure 19.18. Schematic illustration of two types of kneeroots. Left: knee roots frequently seen in Bruguiera and Ceriops. Right: blade knee roots seen in some species of Xylocarpus.
Figure 19.19. Schematic illustration of buttress roots found in Heritiera and Xylocarpus.
Buttress roots occur in a number of genera and have a similar origin as the stilt roots. The sinuous roots arise radially from the main trunk, and expand vertically by eccentric cambial activity throughout their lengths into flat, blade-like structures (fig. 19.19). Buttress roots occur in Bruguiera, Camptostemon, Ceriops, Cynometra, Heritiera, Sonneratia and Xylocarpus. They are best developed in Heritiera and Xylocarpus.
There are a number of genera that normally lack any special root adaptations, however, they may possess specialized structures that are involved in aerating the root system (Tomlinson 1986). In Nypa, for example, the leaves growing close to the stem apex are, in fact, functional pneumatophores.
Root Function
The roots of mangroves have three basic structural components, namely: 1) aerating component; 2) absorbing and anchoring component; and 3) cable component (Tomlinson 1986). The function of the above-ground aerating component relates to gas exchange, keeping the below-ground roots well oxygenated. The absorbing and anchoring component of the root system provides a dual function. It provides physical support for the main trunk and serves as an anchor in an unstable environment, and it is involved in water and nutrient absorption. Note that absorption is conducted through the finer branchlets of the main anchorage roots. The cable component constitutes the lateral root system that unifies the aerating and absorbing/anchoring part of the system (Tomlinson 1986).
Mangroves, like all other vascular plants, respire aerobically and have a low capacity for anaerobic respiration (King et al. 1990). To cope with anoxic and waterlogged conditions, mangroves have developed a number of adaptive anatomical features that allow them to cope and thrive under these circumstances. Mangrove roots have well-developed aerenchyma tissue (i.e., air-storing tissue; air spaces) and numerous lenticles that connect the underground roots with the above-ground parts of the plant so that the above-ground component of the root system can ventilate the buried portion for respiratory purposes. Aerenchyma has a low metabolic activity which reduces the respiration rate per unit volume of tissue, and offers low resistance to the movement of gases (e.g., oxygen) between roots and above-ground plant parts. The supply of oxygen to the roots seems to be important, since the desalination of seawater that occurs in roots may be a metabolically expensive active-transport system requiring continual supply of oxygen, which cannot be obtained from the anoxic sediments that dominate mangrove habitats. Indeed, anoxic conditions frequently associated with organic-rich waterlogged sediments seem to promote the development of aerenchyma, which may serve as an oxygen reservoir.
Reproduction
Reproductive Modes. Very little is known about the seasonal reproductive activity of Indonesian mangroves, or their modes of reproduction. Tomlinson (1986) reported that 85% of common mangrove species are hermaphrodites (i.e., having perfect flowers containing both stamens and carpels), 11% are monoecious (i.e., having male and female flowers on the same plant) and only 4% are dioecious (having male and female flowers on different plants). Some common hermaphroditic genera with perfect flowers are Rhizophora, Bruguiera, Avicennia, Sonneratia, Lumnitzera, Aegiceras, Aegialitis, Ceriops, Kandelia, Osbornia and Camptostemon. Monoecious genera are Nypa (with protogynous inflorescence), Heritiera and Xylocarpus,while Laguncularia and Excoecaria are dioecious (Tomlinson 1986). Outbreeding is obligate in bisexual species, and according to Tomlinson (1986), many monoecious species have developed breeding mechanisms, such as sexual segregation where male and female flowers develop at different times to ensure that outbreeding occurs. Hermaphroditism in pioneering groups, such as Avicennia, may provide these species with a competitive advantage, since this reproductive mode may facilitate rapid population growth in isolated localities. However, most hermaphrodites (e.g., Avicennia) have developed a variety of breeding mechanisms to ensure genetic mixing through outbreeding (e.g., protandrous dichogamy where pollen is shed before the maturation of carpels). Perfect flowers of the three Rhizophora species found in Indonesian waters are illustrated in figure 19.20.
Flowering and Pollination. In central Queensland, flowering and pollination peak during the summer months (Hutchings and Saenger 1987). Pollination in mangrove species occurs through both biotic and abiotic vectors (table 19.1). According to Tomlinson (1986), mangroves are almost exclusively pollinated by animal vectors, while wind pollination occurs only in Rhizophora, which may also be self-pollinating. Wright (1977) found that the majority of Australian mangroves, including Rhizophora, have small, non-sticky pollen grains. The morphology of mangrove pollen is characteristic of each species, and has been used in palynological studies.
Figure 19.20. Flowers of Indonesian Rhizophora spp. (a) Longitudinal section (LS.) through the flower of R. apiculata (x 2.2). (b) L.S. of R. mucronata flower (x 2.2). (c) L.S. of R. stylosa flower (x 2.2).
Modified from Tomlinson 1986.
Table 19.1. Pollination and pollen-discharge mechanisms in the Family Rhizophoraceae (tribe Rhizophoreae).
Whether wind pollination in Rhizophora is the only means or the primary means of male gamete transfer is still debated, since floral features such as elaborated stigmas for capture of wind-borne pollen are absent in the genus, while numerous adaptations for wind pollination (e.g., high pollen-to-ovule ratio, light powdery pollen, absence of odour and pollinator reward, pendulous [inverted] flowers, brief pollen presentation times, etc.) have been described (Tomlinson 1986). Nonetheless, insect pollination in Rhizophora may be important, since the flowers are known to exude a sweet, odourless substance. Bees and other insects (ants and thrips) have been observed on the flowers of Rhizophora mucronata in artificial monospecific stands at Demak Moro, Central Java (T. Tomascik, pers. obs.).
Animal Pollinators. Animal pollinators range from small insects (e.g., fruitflies) to large mammals (e.g., bats), and are either nocturnal or diurnal. Nocturnal pollinators include moths and bats, while diurnal pollinators are birds, bees, butterflies and numerous other insects that are attracted to flowers by colour and/or odour. The sweetly scented white flowers of Ceriops tagal are probably pollinated by moths (Tomlinson 1986). Pollination in Sonneratia is predominantly by two nocturnal species of nectarivorous bats, namely Macroglossus minimus and Eonycteris spelaea.Start and Marshall (1976) have reported that in West Malaysia, E. spelaea shows great preference for durian (Durio zibethinus) flowers. In fact, these small bats are the main animal pollination vector for this economically important plant. However, flowering in durian is strongly seasonal, and the bats need alternative sources of food during periods when durian flowers are not available. Mangroves seem to be an important alternative food source, since E. spelaea are known to fly long distances (up to 50 km) to feed on the nectar and pollen of Sonneratia flowers (Start and Marshall 1976). E. spelaea are frequently found roosting in large limestone caves from which they venture out each night in search of food (e.g., Goa Lawah in Bali, Liang Rampah and Kotabuluh in North Sumatra as well as numerous caves in, Sulawesi) (Whitten et al. 1987,1988). The largest population of bats on Java may be found in a number of limestone caves just south of Sukabumi, West Java, where over a million bats are roosting.
Many limestone caves are located in coastal areas in close proximity to mangroves. It is well-known that mangroves are key components of coastal food webs, however, their terrestrial connections are rarely emphasized. The durian-bat-mangrove linkage is an excellent example of the important role that mangroves play in sustaining important terrestrial animal groups. Large-scale destruction of mangroves may result in local extinctions of terrestrial animals that depend on mangroves for food. For example, conversion of large mangrove areas into tambaks significantly reduces food availability for nectarivorous bats, thus forcing them to move to other areas. Displacement, or local extinctions, of nectarivorous bat populations may in turn have a negative impact on durian production in the region, thus affecting local economies. Bats are, however, not essential for Sonneratia pollination, since in areas where bats are not present, Sonneratia are pollinated by hawk moths (Sphingidae) (Primack et al. 1981).
Large-flowered Bruguiera species are particularly well-adapted to bird visitors (Davey 1975; Tomlinson et al. 1979; Tomlinson 1986). The flowers of these mangrove species contain abundant nectar, and have exploding petal pouches that spray pollen grains onto birds' heads as they probe deep in the base of the flowers for nectar. Birds such as the copper-throated sunbirds (Nectarinia calcostetha), olive-backed sunbirds (Nectarina jugularis) and brown honeyeaters (Lichmera indistincta) are common visitors to large-flowered Bruguiera species (e.g., B. gymnorrhiza) and Lumnitzera littorea.
Figure 19.21. Inflorescence and flower of Nypa fruticans (Palmae; Neopoideae). (a) Distal part of inflorescence (x 0.11). (b) Female flower head with lower bracts removed (x 0.278). (c) Floral diagram of female flower. (d) Male flower just before anthesis (i.e., flowering), (e) Young male spike enclosed by bract (x 0.278). (f) Male spike in anthesis (x 0.278). (g) Floral diagram of male flower.
Modified from Tomlinson 1986.
The economically important Nypa fruticans has small and very sticky pollen grains that are easily carried by drosophilid flies (Drosophilidae) or small trigonid bees (Trigona), which are attracted to the inflorescence (fig. 19.21) by their sweet nectar (Essing 1973; Tomlinson 1986). Industrial alcohol is distilled from fermented sugars extracted from Nypa inflorescence. Nypa nectar is also an. important source of brown sugar.
According to Tomlinson (1986), bees are the most frequent flower visitors in mangroves, and have been observed on flowers of Xylocarpus, Avicennia, Acanthus, Aegiceras, Excoecaria, Scyphiphora and Rhizophora. Not surprisingly, mangrove forests in many parts of the world (India, Bangladesh, U.S.A., etc.) are used for honey production, and in some areas are key components of local economies. For example, a natural 200,000 ha mixed mangrove forest in the Sunderbans (India and Bangladesh) was reported to produce up to 20 metric tonnes (mt) of honey per year (Hamilton and Snedaker 1984). Ceriops appears to be the dominant form in these forests, however, superior-quality honey can be produced from pollen of Aegialitis and Cynometra ramiflora (Hamilton and Snedaker 1984). FAO statistics showed that honey production in Bangladesh averaged about 177 mt per year (between 1957-1977), while industrial beeswax contributed an additional 49 mt per year to the local economy (FAO 1982). Honey and industrial wax production have been reported in Indonesia, however, their production values and importance to local economies have not been quantified (Sukardjo 1994).
While there are a large number of bee species, many of which are solitary, the most important are social bees of the genus Apis, which are also used in beekeeping (Hamilton and Snedaker 1984). From an ecological perspective, the two most important species found in Asia are Apis dorsata and A. florea. However, they build relatively small nest structures which do not yield large quantities of honey. On the other hand, Apis mellifera and A. cerana can be kept in hives and can produce commercial quantities of honey and beeswax (Hamilton and Snedaker 1984). In Florida, commercial quantities of mangrove honey are being produced from the nectar of Avicennia germinans.
Butterflies are another important group of flying pollinators that visit small-flowered species such as Bruguiera parviflora. Other flying insects that serve as pollinators are wasps and flies. The large diversity and the generalized nature of mangrove pollinators ensures that no plant is dependent on one specific vector (Tomlinson 1986). Furthermore, floral adaptations that facilitate animal pollination are relatively general in scope, thus competition for pollinators is greatly reduced.
Vivipary. Vivipary is a characteristic feature of many Australian (Hutchings and Saenger 1987) as well as Indonesian mangrove species. In all viviparous mangrove species seeds develop precociously (i.e., early in development) and germinate while still attached to the parent tree. In contrast to most seed plants where embryo development is interrupted by a period of seed dormancy, embryo development in viviparous mangroves is continuous (Tomlinson 1986). According to Hutchings and Saenger (1987), vivipary occurs in Rhizophora, Bruguiera, Ceriops, Kandelia and Nypa.In these species, the embryo ruptures the pericarp and grows outwards into a seedling (fig. 19.22), reaching considerable length (Tomlinson 1986). Thus in viviparous mangrove species dispersal occurs through seedlings and not seeds (Tomlinson 1986). For example, the seedlings of Rhizophora mucronata are on an average 40-50 cm long, but have been known to reach 70 cm or more (Tomlinson 1986). Vivipary also occurs in Aegialitis, Acanthus, Avicennia and Aegiceras (mangroves not found in Indonesia excluded), however, in these species the embryo does not rupture the pericarp, and the condition is termed cryptovivipary (Hutchings and Saenger 1987).
The explanation for the evolutionary significance of vivipary in some, but not all, mangrove species has been elusive. It has been often suggested that the main advantage of vivipary is production of heavy seedlings (e.g., Rhizophora) that can become quickly (10 days) established (i.e., rooted) in relatively unstable intertidal environments (Chai 1982). General zonation patterns in mangrove forests have been linked to dispersal properties of mangrove seedlings, whose dispersal seems to be determined primarily by their length and wave action (Rabinowitz 1978). Others have explained vivipary as an adaptation to protect the embryo from seawater during early development (Joshi et al. 1972). The adaptive significance of mangrove vivipary (i.e., Rhizophoraceae) and cryptovivipary are still being debated, but the main advantages can be summarized as rapid rooting, salt regulation, ionic balance, development of buoyancy, and prolonged attainment of nutrients from the parent (nutritional parasitism) (Tomlinson 1986; Hutchings and Saenger 1987; King et al. 1990).
Figure 19.22. Seedlings of selected viviparous mangrove species common in Indonesia.(1) Bruguiera gymnorrhiza; (2) Rhizophora mucronata; (3) Bruguiera parviflora; (4) Avicennia marina (a) newly germinated, (b) plumule elongating; (5) Aegiceras corniculatum (a) fruits, (b) single young fruit and (c) germinating fruit.
From MacNae 1968.
Mangrove Environments
On a global scale, mangrove ecology studies may appear to be a chaotic mess of special cases represented by unique combinations of climatic, hydrologic, geo physical, geomorphic, pedologic and biologic conditions.—THOM 1982
Along the seaward margin of the wide coastal floodplains of north Java and the extensive coastal lowlands of South Sumatra, Kalimantan and Irian Java, as well as the narrow intertidal zones of thousands of large and small coral islands, Indonesian mangroves inhabit a great variety of coastal environments. The popular view of mangroves as smelly swamps along muddy, flood-prone coastlines certainly describes a vast majority of mangroves in Indonesia, however, there are numerous exceptions. Diving in a clear-water mangrove swamp? An unlikely adventure, unless you happen to be 50 km off the coast of East Kalimantan. Thanks to the adventurous spirit of Ron Holland, Borneo Divers at Sangalaki Island, we were able to do just that at Samama Island. Moving with a strong 1.5 kn tidal flood current, we entered an environment we have not seen before, where mangroves, corals and sea-grasses formed a single unique ecosystem. Mangrove islands, which may be similar to Samama Island, have been reported from the Caribbean (Stoddart and Steers 1977) and the Great Barrier Reef (Spenceley 1976; Hopley 1982). In the Caribbean, these islands form in sheltered environments with low tidal range, and appear to be mostly monospecific stands of Rhizophora, as has also been reported by Hopley (1982) from the Great Barrier Reef. In contrast, the diverse ecosystem of Samama Island is located 50 km offshore in a delta-front setting with a tidal range of about 2.5 m. It seems that most of the island is intertidal. No obvious zonation in mangrove vegetation was apparent, with the exception of a thick Rhizophora stylosa fringe along the sheltered southeast coast of the island. Parts of the east coast of the mangrove island were fringed by a white sandy beach. Immediately behind the beach was luxuriant mangrove vegetation. The widespread occurrence of coral reef-associated mangrove communities in Indonesia is well-known (van Steenis 1958; Kartawinata and Waluyo 1977; Soemodihardjo et al. 1977; Prawiroatmodjo et al. 1984; Budiman et al. 1985, 1986; Indiarto 1986). A total of 38 mangrove tree species have been recorded from coral reef-associated mangrove ecosystems, with Rhizophora stylosa, R apiculata, Sonneratia caseolaris, Xylocarpus granatum and Bruguiera gymnorrhiza being the most important (Budiman et al. 1986). The nature of the substrate as well as tidal and salinity regime are major environmental factors that determine the structure of coral reef-associated mangroves. Rhizophora stylosa is an important pioneering coral reef-associated species in many parts of the archipelago (Budiman et al. 1986).
A number of classification schemes exist to group mangrove ecosystems into distinct classes. Various biotic interactions (e.g., competition, parasitism, amensalism, mutualism, grazing, sediment turnover, etc.) and abiotic factors (salinity, inundation, topography, etc.) have been used to classify particular mangrove forests (Hutchings and Saenger 1987). The three most common classification schemes used are based on structural attributes of the mangrove forests (Specht 1970), physiographic characteristics (Lugo and Snedaker 1974), and coastal geomorphology (Thorn 1982).
Structural Attributes. In his analysis of Australian evergreen forest vegetation, Specht (1970) developed a classification scheme based on the height of the tallest vegetation and its "foliage projective cover". Under this classification, vegetation units can be grouped into shrublands, scrublands, and woodlands. Hutchings and Saenger (1987) suggested the addition of taxon names of the dominant vegetation units, thus subdividing the vegetation into finer units, such as Rhizophora scrublands or Avicennia woodlands. This classification has not been widely used in Indonesia, however, mangroves are often classified according to the dominant mangrove species (e.g., Avicennia pioneering community). The system is, however, also very useful in studies of mangrove zonations within specific mangrove ecosystem types.
Physiography. In terms of wide applicability, the two most useful mangrove classification schemes are those of Lugo and Snedaker (1974) and Thorn (1982). The physiographic and structural scheme developed by Lugo and Snedaker (1974) for relatively simple mangrove systems in Florida can be modified and applied to Indonesian settings. Lugo and Snedaker recognized six basic community types based predominantly on the physiographic setting, which is a function of environmental conditions and biological interactions (fig. 19.23). It should be noted, however, that the classification scheme is based on a simple mangrove community consisting of three mangrove species, and its applicability to Indonesian settings has not been tested quantitatively. Nonetheless, an explanation of the classification is given with possible examples from various Indonesian regions. Note that some of the zonations described below are based on visual observations only.
Figure 19.23. Classification of mangrove environments using physiographic characteristics.
Adapted from Lugo and Snedaker 1974.
Overwash mangrove forests. In Florida, this community type is dominated by Rhizophora mangle, whose trees reach a height of 5-7 m. The community is characteristic of small coral cays, mud banks and coastal promontories in estuaries and shallow bays. Their characteristic feature is daily inundation by flood tides, which, due to strong currents, keep mangrove litter accumulation to a minimum. An excellent example of this mangrove forest type is Samama Island in East Kalimantan. In contrast to Florida, however, the overwash mangrove forest on Samama Island is very diverse (e.g., Rhizophora spp., Sonneratia spp., Avicennia spp., and Bruguiera spp.). In Kepulauan Seribu, a number of patch reefs have small stands of Rhizophora stylosa (2-3 m in height), which are similar to the Rhizophora mangleoverwash communities in the Florida Keys. Much larger versions of this community type can be found in Bintuni Bay, Irian Jaya. For example, Sianir Kecil, just north of Babo, is a small island which is flooded each high tide. A Rhizophora stylosa community forms a narrow outer fringe around much of the island. The interior of Pulau Sianir Kecil is dominated by a R apiculata and Bruguiera parviflora/B. gymnorrhiza mixed forest. Trees of R apiculata are up to 40 m high. In contrast to Pulau Samama where the substrate is of reefal origin (i.e., carbonate sands), and relatively devoid of organic detritus, the substrate at Pulau Sianir Kecil consists of fluvial sediments with considerable accumulations of organic matter.
Fringe mangrove forests. These forests attain their most extensive development along the protected coastlines and flood plains of east and South Sumatra, Kalimantan and Irian Jaya. The most luxuriant development occurs where coastal alluvial plains are just above die mean high-tide mark (e.g., South Sumatra, Bintuni Bay). Fringe mangrove forests are, however, widespread throughout the archipelago, and are found in a variety of environments. Fringe mangrove forests once covered much of the north coast of Java, however, most of them have been logged and converted into fish and shrimp pond (tambaks). The remnants of Java's mangrove forests now form a narrow fringe along short sections of the north coast, seldom more than 100 m wide. In other regions of the archipelago, pristine fringe mangrove forests are found as narrow belts. On Pulau Rinca, the fringe mangrove forest forms a green belt that surrounds the island's dry, desert-like landscape. Euryhaline species such as Avicennia marina and A. alba dominate the seaward fringe, along open sheltered coastlines, while Rhizophora spp. are found along tidal creeks and small seasonal freshwater streams. The characteristic feature of fringe communities is their distinct zonation that is perpendicular to the coastline (fig. 19.24). The zonation patterns vary from place to place, and are primarily a function of topography, frequency of tidal inundation, salinity gradients and fresh water inputs.
Riverine mangrove forests. The banks and flood plains of many large rivers on Sumatra (e.g., Sungai Banyuasin), Java (Sungai Brantas and Solo), Kalimantan (Sungai Berau and Mahakam), Sulawesi (Sungai Kaladu and Kalaena), Irian Jaya (Sungai Bintuni), as well as smaller rivers and creeks of hundreds of small islands throughout Indonesia are fringed by riverine mangrove forests. Riverine forests are often fronted by fringe mangrove forests (e.g., Sembilang Wildlife Reserve, South Sumatra). Riverine mangrove forests extend as far as 35 km inland in Sumatra and Irian Jaya, generally to the upper regions of saltwater intrusion. However, along the Musi River in South Sumatra, Sonneratia caseolaris can be found 65 km upriver near Palembang (Danielsen and Verheugt 1990). Riverine mangrove forests are primarily under a freshwater influence and exhibit zonation perpendicular to the river. These zonation patterns are not universal, but vary from region to region, as well as along the river course. The extensive riverine mangrove forest at the mouth of the Simpangalangan River (South Sumatra) consists predominantly of Rhizophora apiculata, R. cylindrica, Bruguiera gymnorrhiza and Xylocarpus granatum. In contrast, the riverine mangrove forest at the mouth of the Bintuni River (Irian Jaya) consists of Avicennia marina, A. eucalyptifolia, Aegiceras corniculatum and Sonneratia alba. Further inland, however, the forest is dominated by Rhizophora apiculata (up to 40 m high) and Bruguiera spp.
Figure 19.24. Zonation of mangrove communities based on dominant mangrove species.
From Ministry of Forestry (GOI) 1993.
Basin mangrove forests. These mangrove types occur along coastlines with inland depressions that channel terrestrial runoff towards the coast. Landward areas are under the influence of fresh water runoff, while the seaward margins are intertidal. Indonesian examples of these forest types are difficult to find, since many coastal basin areas are dominated by peat-swamp or freshwater-swamp forests. However, Sukardjo (1995) noted that the Apar Nature Reserve in East Kalimantan contains basin-type mangrove forests.
Hummock mangrove forests. Similar to basin type but slightly elevated. No documented example in Indonesia.
Scrub mangrove forests. In Indonesia, this type of mangrove community is commonly associated with vegetated sand cays. The dominant mangroves are usually dwarfed Rhizophora stylosa trees, which are rarely more than 2 m high. An excellent example of this community type are the reef flat associated Rhizophora stylosa stands on many patch reefs in Kepulauan Seribu. In Florida, this community is restricted to south Florida and the Keys.
As was illustrated above, the physiographic classification scheme (Lugo and Snedaker 1974) can be successfully applied in studies of Indonesian mangrove communities. However, as Hutchings and Saenger (1987) point out, it remains to be quantitatively determined whether the scheme developed for a simple mangrove community consisting of three species is really applicable to regions with greater habitat and species diversity.
Geomorphological Classification. Thorn (1982) described five terrigenous coastal environmental settings (i.e., physical) in which Australian mangrove forests are commonly found. Hutchings and Saenger (1987) added a sixth class, namely the carbonate (coral coast or coral island) setting. They pointed out that on a global scale the carbonate class is relatively insignificant. However, in Indonesia, the carbonate setting is 'locally' important, considering the fact that the vast majority of the 17,000-plus Indonesian islands are carbonate in origin.
ALLUVIAL PLAINS. Alluvial plains are among the most characteristic coastal features of all large islands in the archipelago (i.e., Sumatra, Java, Kalimantan, Sulawesi and Irian Jaya). These are depositionary environments, where terrestrial runoff leads to rapid accumulation of terrigenous (siliciclastic) sediments (sands,*silt and clays) and coastal accretion. The extensive alluvial plains along much of the north coast of Java are prime examples, even though 90% of the mangroves were long ago logged and converted to tambaks. Coastal accretion is generally most rapid at river deltas. For example, the Solo River delta is accreting at a horizontal rate of about 70 m per year (Hoekstra 1989). In Bintuni Bay, numerous rivers discharge large volumes of siliciclastics at the river mouth-forming large mud banks or mud islands, which are rapidly colonized by mangroves. For example, Pulau Keraka at the mouth of the Tatawori River consists entirely of alluvial deposits (fine clays) and has been colonized by a young Avicennia forest (Erftemeijer et al. 1989; T. Tomascik, pers. obs.). The vast Mahakam delta supports 150,000 ha of mangrove forests (Dutrieux 1991). With high sediment load and a discharge rate of some 1500 m3.s-1, the Mahakam delta is continually accreting (fig. 19.25) (Allen et al. 1979). The seaward margin of the delta (salinity range 20-32 psu) is vegetated by diverse mangrove forests, with Avicennia sp. being the prominent mangrove along with Bruguiera gymnorrhiza, Aegiceras corniculatum and the fern Acrostichum aureum(Dutrieux 1991). Under more fresh water conditions behind the Avicennia forests thick Nypa fruticans vegetation dominates the intertidal areas. Further upriver salinity drops to 0-10 psu, and the monospecific Nypa forests are slowly replaced by the paired association of Heritiera littorals and Oncosperma tigillarium (Denis et al. 1988; Dutrieux 1990, 1991; Dutrieux et al. 1990a). In areas where rapid coastal accretion is occurring, Sonneratia caseolaris is the pioneering species (Dutrieux et al. 1990b). The transitional community from marine to fresh water-dominated mangrove flora is at the apex of the delta (Dutrieux 1991).
The Mahakam delta mangrove forests are physically controlled, with biotic factors such as competition or predation playing subordinate roles. Dutrieux (1991) recognized four environmental zones, namely the fresh water apex zone, middle distributary zone, river-mouth zone and central non-distributary zone. While the mangrove flora occupies most of these environmentally distinct zones, the abundance and diversity of aquatic flora and fauna vary greatly. Highest diversity occurs at both the fresh water apex zone (i.e., predominately freshwater flora and fauna) and at the river-mouth zone (i.e., predominately marine flora and fauna) (Dutrieux 1991).
Figure 19.25. The Mahakam River delta, illustrating salinity gradients. Mangrove forests occupy the deltaic islands (white), and extend up to 20 km inland from the main river tributaries.
From Dutrieux 1991.
TIDAL PLAINS. The environmental (geomorphological) setting of tidal plains is very similar to those of alluvial plains, but in this setting tidal influence predominates. Coastal areas under this classification are dominated by strong bi-directional tidal currents generated by high tides. Terrigenous sediments discharged by rivers are dispersed along the coastline by the tidal and longshore currents, and often form elongated mud banks seaward of the river mouth. According to Thorn (1982), the main river channels are typically funnel-shaped and are fed by numerous tidal creeks, which are separated by extensive tidal-flat surfaces (e.g., mud flats). The Berau River may be an example of this type of environmental setting. A number of rivers along the southwest coast of Irian Jaya, with a tidal range of up to 10 m, may also be placed in this environmental setting.
BARRIERS AND LAGOONS. This environmental setting is characterized by higher wave energy and relatively low amounts of river discharge (Thorn 1982). This setting is associated with offshore barrier islands, barrier spits or bay barriers (Thorn 1982). In Indonesia, this environmental and geomorphological setting would most likely occur in the southeastern regions of the archipelago, where it may be associated with barrier reefs. For example, mangroves form a thin belt along the northeast coast of Adonara Island, which is protected by a small barrier reef. Fresh water discharge is limited to the Northwest Monsoon (wet season), thus the mangroves are predominantly under a marine influence.
ALLUVIAL PLAINS AND BARRIERS. According to Thorn (1982), this geomorphological setting represents a combination of high wave energy and high river discharge. Fluvial sediments are rapidly redistributed along the coastline by wave action and strong longshore currents and form extensive sand sheets. Segara Anakan on the south coast of Central Java may be considered as a variant of this geomorphological setting. The major difference lies in the origin of the barrier, which in the case of Segara Anakan is the rocky island of Nusa Kambangan. The lagoon of Segara Anakan is a bar-built estuary (Barnes 1984) receiving high volumes of river discharge. In fact, the lagoon is rapidly being filled with sediments due to high rates of upland soil erosion (Ecology Team 1984).
DROWNED BEDROCK VALLEYS. This geomorphological setting is characteristic of drowned river valleys (Thorn 1982). This setting may occur on slowly subsiding islands with open estuaries that resulted from recent transgression over a former bedrock river valley. It is most likely that this type will be rare in the archipelago, given the tectonic nature of the region, where uplift (i.e., regression) is relatively more common than subsidence.
CORAL COASTS. In this geomorphological setting, mangroves are associated with coral reefs either indirectly or directly (see Budiman et al. 1986). Numerous mangroves occur on terrigenous sediments that have accumulated behind fringing reefs, where they are protected from strong wave action. While they are not universal, by any means, these environmental settings are found throughout the archipelago. Their presence in one area and absence in another has not been studied. Some excellent examples can be found in the Salabanka Islands, Southeast Sulawesi, where a luxuriant mangrove belt is protected by a fringing reef for a considerable length of the coastline. This geomorphological setting is frequently used as a classical example of mangrove/coral reef/seagrass linkage, however, in Indonesia this association is, in fact, quite rare.
The direct mangrove/coral reef setting is best exemplified by the mangrove vegetated coral islands that are found throughout the archipelago (Budiman et al. 1986). Rhizophora stylosa is the most important coral reef-associated mangrove species. Soemodihardjo et al. (1977) noted significant differences in mangrove species composition between the fringe mangrove type along the coastline of Jakarta Bay and the coral reef-associated mangroves common on many sand cays in the Kepulauan Seribu patch reef complex. It was noted that while Avicennia was the dominant pioneering mangrove species along the rapidly accreting Java coastline, the hard coralline substrates characteristic of coral cays were dominated by Rhizophora stylosa, and to some extent by Sonneratia alba (Soemodihardjo et al. 1977). Throughout the archipelago, where mangroves are associated with coral cays, Rhizophora stylosa replaces Avicennia as the primary pioneering mangrove (fig. 19.26). However, the distribution of R. stylosa in the archipelago remains problematic, since many areas of the archipelago have yet to be surveyed.
Mangrove Zonation and Distribution
Studies of tropical shoreline vegetation are extensive (see Chapman 1977 for review). Schimper (1898) was among the first to group tropical coastal vegetation (i.e., associations) based on the dominance of certain groups of higher vascular plants. His classification was particularly suited for tropical humid climates, since most of his work was carried out in the regions between western Indonesia and India. The classification system as developed by Schimper (1898) recognizes four plant associations that are still widely used today. The system was later modified by MacNae (1968) to include areas where evaporation frequently exceeds fresh water input. MacNea's modified classification system is as follows:
i) Mangrove (Mangal) association. Communities growing below the high-tide mark (i.e., littoral zone) consist of several tree and non-woody herbaceous plant species. Mangrove associations (i.e., forests) are restricted to sheltered shorelines and generally do not extend above the high water mark.
ii) Nypa association. The Nypa association occurs landward and upstream from mangroves in protected environments, and is dominated by the rhizomatous palm tree Nypa fruticans. In Indonesia, N. fruticans forms extensive monospecific forests in intertidal to supratidal riverine or deltaic environments (e.g., Mahakam delta, Berau delta, etc.). N fruticans is able to tolerate waterlogged substrates, and its presence is generally indicative of strong freshwater influence (MacNae 1968). Just landward of the Nypa association one frequently finds isolated stands oiHeritiera littoralis,and, in drier areas, the ubiquitous fern Acrostichum aureum.
iii) Barringtonia association. Indonesian shorelines with well-drained sandy soils are frequently dominated by Barringtonia asiatica, which is usually found behind the Ipomoea pes-caprae vegetation, in relatively sheltered environments. According to MacNae (1968), species composition of this association changes if it is located behind mangrove forests. The dominant species on well-drained soils, which may, however, be seasonally waterlogged, are B. racemosa and/or Heritiera spp. (MacNae 1968).
iv) Pes-Caprae association. This association is often characteristic of open, wave-beaten shores (e.g., south coast of Java, Bali, etc.). However, it is an equally characteristic beach vegetation of thousands of small coral islands located in the sheltered intra-archipelagic seas. This association is dominated by Ipomoea pes-caprae,which is frequently accompanied by Canavalia sp., Scaevola spp. and Sophora tomentosa. On the exposed wind- and wave-beaten south coast of Java, the pes-caprae vegetation unit is an important dune-stabilizing component. The sandy coral beaches of many islands are fringed by Casuarina equisetifolia.
v) Saltwort association. This association was added to the Schimper (1891) classification scheme by MacNae (1968) to include areas where evaporation far exceeds limited fresh water input from rainfall, ground water or river runoff. The saltwort association is dominated by bushes and low shrubs of the perennial Arthrocnenum, and by the annual herb Salicornia (MacNae 1968).
Mangrove Inundation Classes. Among the most widely used approaches for mangrove zonation in Indonesia is the scheme based on degree and frequency of tidal inundation, which was developed by Watson (1928) from his work on Malayan mangroves (i.e., Port Klang) (table 19.2). It is, however, important to recognize that Watson's (1928) zonation is not universal, and that local environmental factors such as rainfall, runoff, substrate type and coastal topography will often modify and create new patterns, many of which may be ephemeral.
Figure 19.26. Schematic profile of coral reef-associated mangrove forests. A) Location map of mangrove sites. B) General profile of coral reef-associated mangroves at Elpaputhih, south Seram; Wailale, west Seram; Waila, Saparua Island; Baluran, east coast of East Java; and Pualu Rambut in southwest Java Sea. RS-Rhizophora stylosa.
From Budiman et al. 1986.
Class 1. Mangroves in this class are inundated by all high tides. Predominant species found in these environments are Rhizophora apiculata, R stylosa and R. mucronata. R mucronata prefers areas that are under greater freshwater influence, while R apiculata and R stylosa do well under saline conditions. In some areas, such as Bintuni Bay, Irian Jaya, this zone is frequently dominated by a pioneering Avicennia forest. These vegetation units are, however, found as fringes on newly formed, accreting land along large- and medium-sized rivers (Erftemeijer et al. 1989). Dominant species is Avicennia marina, however, A. eucalyptifolia can be locally abundant.
Class 2. Mangroves in this class are inundated by all medium-high tides. Predominant species are Avicennia alba, A. marina, Sonneratia alba and R mucronata.
Class 3. Inundation by normal high tides. Most species thrive under these conditions. A large part of the mangrove ecosystem falls into this class. The most species are present (i.e., highest diversity). Common species are Rhizophora spp. (often dominates), Ceriops tagal, Xylocarpus granatum, Lumnitzera littorea and Excoecaria agallocha.
Class 4. Inundation only during spring tides. Area generally too dry for Rhizophora spp., but it may be present in low numbers. Common species are Bruguiera spp., Xylocarpus spp., Lumnitzera littorea and Excoecaria agallocha.
Class 5. Inundation only during equinoctial or other exceptionally high tides. Predominant species are Bruguiera gymnorrhiza (dominates), Intsia bijuga, Nypa fruticans, Heritiera littoralis, Excoecaria agallocha, Rhizophora apiculata (rare) and Xylocarpus granatum (rare).
Based on his work in Cilacap (i.e., Segara Anakan, Central Java), De Haan (1931) proposed a modified zonation scheme which integrated frequency of tidal inundation with the salinity of interstitial water.
Table 19.2. Inundation classes for zonation of Malaysian mangroves at Port Klung as developed by Watson (1928), and frequently used in Indonesian mangrove studies.
Figure 19.27. Young Avicenniasp. tree colonizing new soft muds along a tidal creek.
Photo by Tomas and Anmarie Tomascik.
Class 1. Outer zone. Salinity varies from 10 to 30 psu (i.e., psu is equivalent to ppt or %o); inundation two times per day up to 20 days per month; substrate consisting of new soft mud colonized by Avicennia spp. and Sonneratia spp. (fig. 19.27) Substrate consisting of hard and compact sediments (siliciclastics and carbonates) frequently colonized by Rhizophora spp.
Class 2. Middle zone. Salinity varies from 10 to 30 psu. Seawater inundation occurs about 10 to 19 days/month. Most common species Bruguiera gymnorrhiza.
Class 3. Middle zone. Salinity same as in Class 2 with a range of 10 to 30 psu, however, inundation frequency reduced to 9 days/month, or less. Most frequently seen species are Xylocarpus spp. and Heritiera spp.
Class 4. Inner zone. Salinity ranges between 10-30 psu, with inundation frequency down to only a few days/year. Dominant species are Bruguiera spp., Scyphiphora spp. and Lumnitzera spp.
Class 5. This is a transitional zone leading to freshwater swamps, with a small tidal influence. Salinity is 0 psu, indicating a dominant freshwater environment. This transition zone is frequently dominated by species belonging to genera Cerbera and Oncosperma.
Class 6. Similar to Class 5, but located on higher ground and thus much drier. Salinity is 0 psu, but affected by water only during the rainy season. Dominant mangrove species belonging to genera Cerbera and Oncosperma.
The complexity and structure of mangrove forests in Indonesia vary from place to place, depending on the coastal physiography and tidal dynamics. Along the straight coastal areas mangrove forests can be relatively narrow (e.g., 25 to 50 m) while in river deltas and along coastal flood plains where rivers and sea currents bring large volumes of allochthonous material, such as mud and sands, mangroves can grow rapidly and spread out widely along the coastline. In general, the zonation of mangrove forests is determined by: local topography; tidal amplitude, duration and frequency; substrate stability; sediment composition (i.e., type, consistency, and texture); water/soil salinity; as well as degree of exposure and water movement.
Based on the above considerations, mangrove vegetation in Indonesia may be grouped into several communities as follows:
1. Rhizophoraceae Communities. In these communities, Rhizophora spp. and Bruguiera spp. are the dominant mangrove units, with Xylocarpus spp. and Ceriops spp. being subdominant on higher ground.
2.Complex Mangrove Communities. These are mixed communities consisting predominantly of Avicennia spp., Rhizophora spp., Bruguiera spp., Ceriops spp. and Xylocarpus spp. Occasionally, Nypa fruticans and undergrowth of Scyphiphora spp., Brownlowia spp. and Acrostichum spp. are intermingled within the mangrove forests to varying degrees, depending on fresh water input and degree of waterlogging. Mixed mangrove communities often extend long distances inland (e.g., 30 km in South Sumatra) and are often characteristic of coastal areas influenced by large river systems. In general, undergrowth is very limited in undisturbed mangrove forests, however, thick undergrowth consisting of Scyphiphora spp., Brownloxvia spp. and Acrostichum spp. is very common in mangrove areas degraded by various anthropogenic activities (e.g., logging, conversion, etc.).
3. Transitional Communities I. These communities form the transition from seawater-dominated systems to freshwater communities, and consist primarily of Sonneratia/Oncosperma and Nypa/Acanthus associations. Further inland (i.e., higher ground), or upriver, transitional communities may consist of paired associations of Excoecaria/Acrostichum and Brownlowia spp. These associations are often found bordering some of the larger rivers and are under strong freshwater influence.
4. Transitional Communities II. These communities form the transition to upland vegetation. Excoecaria forests are found generally on ripe soils, and are associated with Lumnitzera/Scyphiphora and Nypa/Heritiera spp., often with dense Brownlowia/Acrostichum spp. undergrowth. In Indonesia, these associations are frequently found on the outer, landward fringes of both basin and coastal mangrove types.
5. Cleared Mangrove Areas. Vast clear-cut areas may be eventually recolonized by a secondary growth of sparse Avicennia scrub and Excoecaria regrowth. Mangrove species frequently invading clear-cut areas are invasions consisting of Acrostichum spp., Pluchea spp., and some Lumnitzera spp. Extensive growths of Acrostichum ferns are very common on the landward side of clear-cut mangrove forests, and are a serious problem for management, since they prevent recolonization by more economically important tree species (e.g., Rhizophora, Bruguiera, Avicennia, Xylocarpus, etc.).
Indonesian mangrove forests are characterized by great variations in species composition that can be very distinctive. For example, in accretionary environments (e.g., deltas), pure stands of Avicennia, Sonneratia, or both, frequently develop at the seaward margin. Along open, wave-protected coastlines, mangroves are usually dominated by Sonneratia alba and Avicennia marina. Sonneratia is associated with softer muds, while Avicennia tends to grow on firm sandy soil. In contrast, non-accretionary environments are normally vegetated by diverse mixed mangrove communities consisting of several species. Closer to dryland ecosystems, where the marine influence diminishes and the terrestrial influence increases, vegetation consists of salt-tolerant dryland vegetation, such as Polichandrone sp., Intsia sp., and Ficus sp.
It should be noted, however, that biological interactions (competition, predation, parasitism, etc.) play a significant role in determining mangrove zonation patterns, in addition to the physical environmental factors mentioned above. For example, the herbivorous mangrove crabs of the Subfamily Sesarmidae are numerically dominant members of the benthic mangrove fauna in Indonesian, and other Indo-west Pacific, mangrove forests (MacNae 1968). Sesarmid crabs are known to consume up to 30% of annual mangrove litter production and a large proportion (75%) of mangrove propagules (Leh and Sasekumar 1985; Robertson 1986,1991; Smith 1987a,b,c; Robertson and Daniel 1989). In Queensland mangroves, sesarmid crabs show a distinct preference for propagules of certain mangrove species which is determined by their nutritive value (Smith 1987a). The most heavily predated propagules are those of Avicennia marina, which have the highest sugar content but are low in crude fiber and tannins (Smith 1987a). This mangrove species is strongly euryhaline, and while it is often abundant in the seaward intertidal margins of mangrove forests, it is generally absent from the mid-intertidal zone (Bunt and Williams 1981; Elsol and Saenger 1983; Johanstone 1983; Erftemeijer et al. 1989). Experimental studies in Australia demonstrated that predation on Avicennia propagules by sesarmid crabs was highest in the mid-intertidal and lowest in the low and high intertidal zones (Smith 1987b). Caging experiments (i.e., to exclude sesarmid crabs) in the mid-intertidal with propagules of Avicennia marina demonstrated that while the seedlings are able to take root, they grow very slowly. Robertson (1991) suggested that the combination of seed predation and shade intolerance effectively limits the distribution of A. marina to the seaward margins of mangrove forests. The propagules of A. marina will survive and take root in all intertidal areas where sesarmid crabs are absent, or are present in relatively low densities, but seedlings grow to maturity only where light is not a limiting factor (Smith 1987b). Comparison of seed predation rates between Australian, Asian and American (North and Central) mangroves showed that while grapsid crabs are the dominant predators in Australia and Asia (Malaysia), this role in Florida is delegated to three genera of gastropods (Smith et al. 1989). Predation rates and patterns in'Australian and Malaysian mangroves are similar for both Rhizophora and Avicennia(Smith et al. 1989).
Segara Anakan, Central Java. Perhaps the most intensively studied mangrove forest in Indonesia is that of Segara Anakan in Cilacap, on the south coast of Central Java (fig. 19.28). The 21,750 ha mangrove (12,610 ha tidally affected) was the subject of a multidisciplinary research program coordinated by the Ecology Team from the Bogor Agricultural University (see Ecology Team 1984). Erftemeijer et al. (1988) reported a total of 80 plant species from the area, while the Ecology Team (1984), in contrast, recorded 26 mangrove species in their quantitative analysis (quadrat sampling). The differences are related to sampling methodology, and illustrate the value of both large-scale qualitative visual surveys (i.e., Erftemeijer et al. 1988) and quantitative surveys (i.e., Ecology Team 1984).
Figure 19.28. Map of Segara Anakan illustrating the location of mangrove area and the four zones (l-IV) that were surveyed by the Ecology Team (1984).
From White et al. 1989.
The mangrove forest of Segara Anakan contains 26 primary mangrove species, of which Rhizophora apiculata, R mucronata and Bruguiera gymnorrhiza are the most abundant. The Segara Anakan study (Ecology Team 1984) was conducted at four distinct physiographic and environmental zones, differentiated by salinity gradients and sedimentation rates (i.e., coastal accretion). Three species associations were recognized, namely monospecific stands, paired associations and mixed associations (Ecology Team 1984). The study identified four types of monospecific mangrove stands:
1) Avicennia marina and A. alba. Monospecific stands of these pioneering species are common along the seaward fringe frequently inundated by seawater. Both species are very tolerant of high-salinity conditions.
2) Rhizophora mucronata. Extensive monospecific stands are common along tidally affected creeks and extend into the interior of the mangrove upstream. R. mucronata grows well in less saline conditions.
3) Ceriops tagal Monospecific stands form in the landward margins of the mangrove forest, especially along predominantly freshwater creeks.
4) Aegiceras corniculata. This species is found along the seaward fringe, river mouths and flowing creeks (Ecology Team 1984).
Certain environmental conditions that are functions of specific tidal levels, soil types, drainage patterns and currents give rise to typical paired mangrove associations. For example, high tidal flats in Segara Anakan are vegetated predominantly by the Avicennia officinalis - Sonneratia caseolaris association, while areas that are inundated by high neap tides along flowing creeks are vegetated by the A. alba - Aegiceras corniculata association (Ecology Team 1984). The mangroves in Segara Anakan also form distinct multi-species associations. The Ecology Team (1984) identified seven mangrove communities, which are listed below. The primary mangrove species are listed in order of dominance from high to low.
Figure 19.29. Zonation profile of Rhizophora apiculata - Bruguiera gymnorrhiza - B. cylindrica mangrove community in Zone I, Segara Anakan. The understory consists of shrubs Derris heterophylla and Sarcolobus banksii, and the seedlings of Bruguiera gymnorrhiza. Abbreviations: Aa- Avicennia alba; Ac- Aegiceras corniculata; Ra- Rhizophora apiculata; Rm- R. mucronata; Bg- Bruguiera gymnorrhiza; Bp- B. parviflora; Be- B. cylindrica; Ct- Ceriops tagal; Xg- Xylocarpus granatum; Dh- Derris heterophylla; Sb- Sarcolobus banksii. Tidal abbreviations: ET- exceptional high tides, c. 190 cm; HT- high tide, c. 167 cm; LT- low tide, c. 49 cm.
From Ecology Team 1984.
1) Rhizophora apiculata, Bruguiera gymnorrhiza and B. cylindrica community (fig. 19.29). The community consists of 12 primary mangrove species, with undergrowth dominated by the seedlings of B. gymnorrhiza and the shrubs Derris heterophylla and Sarcolobus banksii, which is considered as a marginal mangrove species in Segara Anakan.
2) R. apiculata, Avicennia alba and R. mucronata community (fig. 19.30). The community consists of 12 primary mangrove species. The undergrowth is dominated by seedlings of Avicennia alba and R. apiculata, and by the herbaceous shrub Acanthus ilicifolius.
3) R. apiculata, Xylocarpus granatum and Nypa fruticans community (fig. 19.31). The community consists of 15 primary mangrove species, with undergrowth dominated by the fern Acrostichum aureum as well as the shrubs and seedlings of D. heterophylla and A. ilicifolius.
4) R. apiculata, Avicennia alba and R. mucronata community in association with 19 other primary mangrove species (fig. 19.32). Undergrowth dominated by D. heterophylla, A. ilicifolius and seedlings of Nypa fruticans.
5) R. apiculata, R. mucronata and Avicennia alba community consisting of 19 primary mangrove species. Undergrowth dominated by S. banksii, A. ilicifolius and by the seedlings of A. alba.
6) R. apiculata, B. gymnorrhiza and R. mucronata community, with 10 primary mangrove species. Undergrowth dominated by the seedlings of R. mucronata, R apiculata and the herbaceous shrub A. ilicifolius.
7) R apiculata, R mucronata and Avicennia marina with seven primary mangrove species. Undergrowth dominated by the seedlings of R apiculata, A. alba and R mucronata.
Figure 19.30. Zonation profile of Rhizophora apiculata -Avicennia alba - R. mucronata mangrove community in Zone I, Segara Anakan. The understory consists of Acanthus ilicifolius and seedlings of Rhizophora apiculata and Avicennia alba. Abbreviations: Aa- Avicennia alba; Ac-Aegiceras corniculata; Ra- Rhizophora apiculata; Rm- R. mucronata; Sc- Sonneratia caseolaris; Ai-Acanthus ilicifolius; Xg- Xylocarpus granatum; Dh- Derris heterophylla; Sb-Sarcolobus banksii. Tidal abbreviations: ET- exceptional high tides, c. 190.2 cm; HT- high tide, c. 160.7 cm; LT- low tide, c. 50.75 cm.
From Ecology Team 1984.
Figure 19.31. Zonation profile of Rhizophora apiculata - Xylocarpus granatum - Nypa fruticans mangrove community in Zone II, Segara Anakan. The understory consists of Derris heterophylla (shrub), Acrostichum aureum (fern) and Acanthus ilicifolius. Abbreviations: Ai- Acanthus ilicifolius;Aa-Acrostichum aureum; Ac- Aegiceras corniculata; Ra- Rhizophora apiculata; Bg-Bruguiera gymnorrhiza; Bp- B. parviflora; Xg- Xylocarpus granatum; Dh- Derris heterophylla; Nf- Nypa fruticans; Pk- Phragmites karka; Ic- Imperata cylindrica; Pv- Paspalum vaginatum. Tidal abbreviations: ET- exceptional high tides, c. 179 cm; HT- high tide, c. 157 cm; LT- low tide, c. 49 cm.
From Ecology Team 1984.
Figure 19.32. Zonation profile of Rhizophora apiculata - Avicennia alba -ft. mucronata mangrove community in Zone III, Segara Anakan. The understory consists of Derris heterophylla (shrub) and seedlings of Acanthus ilicifolius and Nypa fruticans. Abbreviations: Ai-Acanthus ilicifolius; Aa- Avicennia alba; Am- A. marina; Ac- Aegiceras corniculata; Ra- Rhizophora apiculata; Rm-ft. mucronata; Bp- 8. parviflora; Xg- Xylocarpus granatum; Dh-Derris heterophylla; Nf- Nypa fruticans; Pa- Paramignya angulata; HI- Heritiera littoralis. Tidal abbreviations: ET- exceptional high tides, c. 190 cm; HT- high tide, c. 167 cm; LT- low tide, c. 49 cm.
From Ecology Team 1984.
The most important mangrove species in Segara Anakan (ecologically and commercially) is Rhizophora apiculata, which dominates in all community types. This indicates that R apiculata is the most euryhaline species, since it was found in all zones, from the seaward margin to inland areas where inundation occurs only at high tides and salinity drops to 17 psu (Ecology Team 1984). Table 19.3 shows the distribution of dominant mangrove species in Segara Anakan, based on Watson's (1928) inundation classification system. According to the Ecology Team (1984), Segara Anakan has three tidal habitats, namely:
1) Areas that are permanently inundated (Watson's Class 1-3);
2) Areas inundated by high tides only (Watson's Class 4); and
3) Areas only occasionally inundated (i.e., transition zone; Watson's Class 5).
The zonation patterns of vegetation units within mangrove forests are so distinct that they are easily identifiable by remote (satellite or airborne) sensing techniques (colour plate 19.1). The satellite image of the Sungai Sembilang area in South Sumatra clearly illustrates the extent of the mangrove forest. The use of remote sensing technology, which is now widely available, has been greatly underutilized in Indonesia, even though it offers cost-effective management and monitoring services suitable for both mangrove and coral reef management. The SPOT image of Sungai Sembilang clearly shows that the dominant vegetation consists primarily of Rhizophora-Bruguiera association. A schematic profile of the mangrove vegetation in Sungai Sembilang is given in figure 19.33. The structure and zonation as well as the fauna of mangrove forests in South Sumatra have been described in detail in a number of studies (Adiwiroyono et al. 1984; Sukardjo et al. 1984; Silvius 1986; Danielsen and Verheugt 1990).
Table 19.3. Zonation of Segara Anakan mangroves based on Watson's (1928) inundation classification system (i.e., Classes 1 to 5). Column 6 represents inland and adjacent areas which are either freshwater swamps or drylands.
Figure 19.33. Vegetation profile of Sungai Sembilang mangrove forest, South Sumatra. The transect covers a distance of about 15 km from survey locations at the river mouth (left) to survey locations 15 km upriver. One tree in the diagram equals 500 ex. per ha.
From Danielsen and Verheugt 1990.
Mangrove Production
The vast mangrove forests of Southeast Asia and Australia are sites of high primary production (Hutchings and Saenger 1987). Unlike many other wedands (e.g., salt marshes) where a large percentage of primary production (i.e., plant biomass) enters the detrital pathway, a large percentage (30%-80%) of mangrove litter fall is consumed directly by a wide assemblage of invertebrate grazers. Mangroves in Indonesia attain their greatest diversity, canopy height (up to 40 m) and productivity in estuarine environments. Mangroves with high productivity are generally characterized by a high influx of fresh water (e.g., Mahakam delta, Berau River delta, Bintuni River estuary, etc.), low salinities (e.g., 10-15 psu), cloudy-humid climate, and high nutrient concentrations in the substrate (Boto and Wellington 1983; Boto et al. 1984; Citron and Novelli 1984; Clough 1984; Smith and Duke 1987; Clough and Sim 1989). Mangrove trees themselves are the main primary producers in mangrove ecosystems. While there is a great variety of other mangrove-associated plants (terrestrial and marine), their contribution to the total production of the mangrove ecosystem is relatively insignificant when compared to mangroves. Photosynthetically fixed carbon in the form of litter (i.e., fallen leaves) is the main energy currency in mangrove systems. Leaves, flowers, fruits and timber (i.e., trunks, branches and roots) are the main food sources for a variety of invertebrate and vertebrate herbivores. Among the most important invertebrate herbivores in the Indo-west Pacific are the sesarmid crabs, whose grazing activity greatly speeds the decomposition of mangrove litter (MacNae 1968; Giddins et al. 1986; Robertson and Daniel 1989). Litter decomposition is an important process since it fuels the detrital-based food web that is the key building-block of all mangrove ecosystems. Environmental factors that, to a large degree, determine the productivity of mangrove forests are briefly summarized in table 19.4.
Mangrove Primary Productivity. Gross and net primary productivity (PG and PN respectively) are concepts defined in earlier chapters (e.g., Seagrasses) and will not be repeated here. In summary, net primary production in plants is the total accumulation of new organic matter in plant tissue in excess of respiration per unit area per unit time (Hutchings and Saenger 1987). Total net primary production is difficult to measure, and, as a result, a number of different methods were developed. Techniques used measure total biomass accumulation, leaf growth and litter production, photosynthetic rates of leaves or small branches, and light attenuation, which is an indirect measure of potential mangrove community net production.
In general, mangroves are found in areas of high solar radiation and thus have a high potential to achieve high primary productivity. However, differences in mangrove primary productivity are known to vary between different regions of the archipelago and neighbouring countries. It should be expected that higher rates of primary productivity should occur in areas with a greater number of cloud-free days, and higher number of sunshine hours per month, provided sufficient fresh water is available. It has been suggested that higher net primary production rates in Australian mangroves than Malaysian mangroves is attributed to cloudy conditions that predominate in the Malaysian region (Gong et al. 1991).
In their studies of potential PN in Papua New Guinea and Australia, Boto et al. (1984) suggested that environmental conditions at specific sites are more important than mangrove type. They suggested that the highest potential Pirates are usually found in upstream environments subject to regular freshwater influence, while the highest variability in PNvalues occurs in the upper intertidal zone, most closely exposed to inundation by seawater (Boto et al. 1984). They were also able to demonstrate that higher potential PN in Papua New Guinea than in Australia (table 19.5) was related to greater availability of soil phosphorus in Papua New Guinea mangroves.
Table 19.4. Key factors and processes involved in the maintenance of ecological processes of mangrove ecosystems.
Using the light-attenuation method, Atmadja and Soerojo (1991) compared the net primary production (i.e., potential productivity) of mangroves at Ujung Kulon (West Java) with 13 mangrove species, and Grajagan (East Java) with 17 mangrove species. Interestingly, Avicennia spp., Bruguiera cylindrica, B. sexangula, Ceriops tagal, C. decandra, Lumnitzera racemosa, Aegiceras comiculatum and Scyphiphora hydrophyllacea,while present in Grajagan, are absent from Ujung Kulon. The average PN values at Ujung Kulon (17.3 kg C.ha-1.day-1) were not much lower than at Grajagan (20.2 kg C.ha-1.day) (Atmadja and Soerojo 1991). In Malaysia, PN values seem to be similar, ranging from 4.8 to 27.9 kg C.ha-1.day-1 (Gong et al. 1991). In Queensland, PN rates have been estimated at 16 to 26 kg C.ha-1.day (Bunt et al. 1979). In contrast, De Leon et al. (1991) measured Pirates in a damaged mangrove system in the Philippines, and recorded values of 5.1 to 11.6 kg C.ha-1.day, with an average value of 7.7 kg C.ha-1-1.day-1. Mann (1982) reported that the average Pirates for red mangrove (Rhizophora mangle) in Florida were about 11 kg C.ha-1.day-1. Table 19.5 lists known PN values from a number of Indonesian sites.
Estimates of total net primary production vary from place to place, but productivity depends more on environmental conditions than on the type of mangrove community. In recent studies in East Kalimantan, Sukardjo (1995) arrived at conclusions similar to those of Boto et al. (1984). In a study of five different mangrove communities (i.e., associations), PN irates were very similar, irrespective of species composition (table 19.6). According to Sukardjo (1995), higher PN irates were measured at upstream locations subject to regular freshwater influence. It was further suggested that PN variability was associated with differential nutrient loading and freshwater turnover. In a comparative study of PN rates during the Northwest (i.e., rainy season) and Southeast (i.e., dry season) Monsoons, Sukardjo (1995) demonstrated strong climatic influence (table 19.7). Higher PN rates were measured during the rainy season, when rainfall exceeds 300 mm/month, than during the dry season when rainfall falls to 100 mm/month or less.
Table 19.5. Potential primary production (PN) estimates for Indonesia, Australia and Papua, New Guinea.
Other sources of primary production (e.g., marine macrophytes and benthic algae) are not considered important in the Rhizophoraceae-dominated forests, because of low light levels reaching the mud surface and penetrating the muddy mangrove waters. However, benthic algae may be important in some areas with open canopies, or along fringes of mangroves and shallow creeks.
Litter Production. In very simple terms, primary production of a mangrove community can be expressed by the annual weight of leaf litter produced per unit area. There are a number of techniques used, the simplest being a network of baskets (c.0.25 m each) located in mangrove undergrowth beneath the trees. Usually, litter collections are made once a week, since leaf decomposition in humid tropical climates is relatively rapid. Because litter-fall measurements are relatively easy and inexpensive, they have been used widely in production estimates.
Table 19.6. Estimated average potential net primary production (PN) of five mangrove associations at the Apar Nature Reserve in East Kalimantan. Standard error of the mean in parentheses. Species abbreviations: Am-Avicennia marina; Ao-A officinalis; Be-Bruguiera cylindrica; Bp- B. parviflora; Bg- B. gymnorrhiza; Bs- B. sexangula; Ra-Rhizophora apiculata; Rm-R. mucronata; Sa-Sonneratia alba; Ca- Ceriops tagal; Kc-Kandelia candel;Xm- Xylocarpus moluccensis; Fm- Ficus microcarpa.
Table 19.7. Estimated average potential net primary production (PN) rates (kg C.ha-1.day-1) during the Northwest and Southeast Monsoons.
Mangrove litter fall accounts for about 50% to 78% of the total net primary production of mangrove forests, while wood production accounts for 22%-50% of the total net primary production. In Segara Anakan, the net primary production of litter was 134.3 g DW.m-2.day-1, and included leaves, branches, buds, flowers and budscales. Table 19.8 provides information on litter production of some common mangrove species in Segara Anakan, while table 19.9 provides an overall regional comparison of total litter production.
Sukardjo (1989) studied the litter production at Muara Angke-Kapuk in Jakarta Bay and obtained values ranging from 4.9 to 17.5 mt DW.ha1.year-1, depending on species present. The Avicennia community produced the highest rates of litter fall, while monospecific stands of Rhizophora had the lowest litter fall. In Malaysia, litter production ranges between 13.98 and 23.4 mt DW.ha-1.year-1. The highest litter production measured in Indonesian mangroves is from the Apar Nature Reserve in East Kalimantan (Sukardjo 1995). Total litter production (i.e., leaves, buds, flowers, fruits and twigs) ranged from 20.5 to 29.4 mt DW.ha-1.year-1,, far surpassing all previous studies. In East Kalimantan, highest litter production occurs during the rainy season. The most productive mangrove associations were those of Ceriops tagal and Rhizophora apiculata (Sukardjo 1995). According to Sukardjo (1995), Apar Bay is an important commercial fishery area in East Kalimantan. Considering the surprisingly high primary productivity of the 128,000 ha mangrove forest, it is likely that the outwelling of litter plays an important role in productivity of coastal waters.
In a recent study at Handeueluem in the Sunda Strait, Soeroyo and Atmadja (1994), measured rates of litter production at a number of locations. Litter production from mangrove stands dominated by Rhizophora apiculata, Sonneratia alba and Aegiceras corniculatumwere about 10.4 mt DW.ha-1.year-1, and while these production rates are higher than in Segara Anakan (7.7 mt DW.ha-1.year-1) and Rambut Island (8.4 mt DW.ha-1.year-1), they are much lower than those in East Kalimantan (Sukardjo 1995). In a parallel study, Atmadja and Soeroyo (1994) determined the outwelling rates of mangrove leaf litter through river and tidal flows. They estimated that about 1.2 to 1.3 mt DW.ha-1.year-1 of litter is exported from the Cikabembem and Cihandeuleum Rivers which, represents roughly 11% of annual litter production. It seems that much of the litter in these mangroves is being used inside the mangrove. In contrast, De Leon et al. (1992) reported that up to 38% of total leaf litter from Rhizophora apiculata forests were being exported to the coastal waters. Boto et al. (1991) demonstrated that mangrove detritus derived from the mangrove litter production contributes about 16%-20% of the energy requirements of the nearshore benthos. Based on these conservative figures, it seems that mangroves (litter production or particulate organic matter export) may have a significant effect on benthic food chains (Boto et al. 1991). De Leon et al. (1992) have demonstrated that up to 62% of total export from a Rhizophora apiculata mangrove in the Philippines is exported to seagrass beds in the form of litter and detritus. On the other hand, it seems that mangroves do not export dissolved nutrients to adjacent systems, but rather these are utilized and recycled within the mangrove system. Boto et al. (1991) point out that since their research was carried out in mangroves devoid of terrestrial input via rivers, it is likely that earlier studies reporting significant outwelling of dissolved nutrients may have been reflecting terrestrial influence.
Table 19.8. Average net primary production of litter (±SD) for common mangrove species from Segara Anakan, south coast of Central Java.
Table 19.9. Regional comparison of mangrove litter production (total) in selected mangrove forests. Yield in: mt DW.ha-1.year-1.
Litter Processing. Mangrove litter is the primary autochthonous product of mangrove vegetation and the main energy currency in the mangrove ecosystem. The large quantity of particulate organic matter, that can be seen leaking out of mangrove forests with each ebb flow, has long been suspected of making a significant contribution to adjacent coastal ecosystems (Golley et al. 1962; Odum 1971; Odum and Heald 1972; Boto and Bunt 1981). These early pioneering studies in the Atlantic demonstrated that particulate organic matter (i.e., detritus) from mangrove forests may be a significant energy source for adjacent coastal waters, and that mangrove ecosystems are nursery grounds for a variety of marine organisms (Twilley 1988; Daniel and Robertson 1990; Singh et al. 1994).
Leaf litter provides the highest biomass contribution, and is the primary source for mangrove detritus which fuels the mangrove ecosystem. Of the total mangrove litter production, 98% enters the benthic detrital pathway as litter fall. In most mangroves of the Indo-west Pacific, the majority of the mangrove litter fall is exported to sub tidal waters, where it decomposes through the combined action of grazers as well as bacterial and saprophytic decomposers (Heald 1971; Odum 1971; Cundel et al. 1979; Fell and Masters 1980; Flores-Verdugo et al. 1987; Robertson 1988a; Robertson and Daniel 1989a,b). Considering the refractory nature of the exported detrital organic matter (Robertson 1988a; Robertson and Daniel 1989a), its nutritional and energy value to adjacent coastal food chains and nutrient cycles has been recently questioned (Rodelli et al. 1984; Alongi et al. 1989; Alongi 1990). However, Robertson (1988) points out that since the nature of mangrove detritus depends on the degree and frequency of tidal inundation (Twilley 1985; Twilley et al. 1986) as well as the presence, absence, and species composition of consumers (Odum and Heald 1975; Leh and Sasekumar 1985; Robertson 1986), the dynamics of leaf litter breakdown, and thus detrital quality, will vary among sites and mangrove forest types.
Robertson (1986) demonstrated that in Rhizophora-dominated mangroves in northern Queensland, up to 30% of annual leaf litter production is taken underground (e.g., 62 g Cm-2.yr-1; Robertson and Daniel 1989b) and consumed by leaf-eating crabs within six hours. In subtidal areas, leaf litter is rapidly degraded through the grazing action of both crabs (primarily sesarmids) and amphipods (e.g., Parhyale) (Heald 1971; Odum and Heald 1972; Poovachiranon et al. 1986). Sesarmid crabs (e.g., Sesarma messa) are numerically dominant members of Indowest Pacific mangroves, and can remove between 22% to 44% of daily leaf litter fall (Robertson 1986). There are more than 40 species of detrivores that feed on mangrove litter and many show a strong preference for specific mangrove litter. For example, Camilleri (1989) demonstrated that Sesarma erythrodactyla shows a strong preference for the leaves of Avicennia marina, which have lower tannin and higher sugar contents than the leaves of Khizophora stylosa and Bruguiera gymnorrhiza. It was also demonstrated that, of the total litter material processed by sesarmid crabs, 20% was lost due to "sloppy-feeding", 68% was egested as faeces and only 12% was converted into crab biomass (Camilleri 1989). This clearly demonstrates that most of the litter fall that is processed by the grazers is returned to the system as detritus, which then becomes available to other organism in the mangrove food web. Among the more important mangrove litter processors (i.e., leaf-shredders) are the crabs Sesarma erythrodactyla, S. meinerti, S. sulcatum S. guttatum, S. dehaani, S. messa, Neosesarmatium smithii, Parasesarma pictum, Helice leachii, Chiromantes bidens, C. maipoensis, C. messum, Metopograpsus frontalis, Clistoceloma merguiensis, Leptograptus variagatus, Paragrapsus laevis, Hyograpsus paludicula and Episesarma mederi. Other invertebrates that are important mangrove litter processors are amphipods (Orchestia sp., Melita sp.), isopods (Exospaeroma alata, Campaecopia sp.) and capitelid polychaetes (e.g., Capitellides sp.) (Camilleri 1992). These mangrove litter processors effectively reduce the size of the fallen plant material to particle sizes ranging from about 30 to 1200 um. Camilleri (1992) found that the size range of particulate organic matter in the stomachs of 38 invertebrate species was within the above range, suggesting that the leaf-shredders constitute a primary link in the marine food web of mangroves.
Leaf removal and consumption rates by crabs are expected to be higher in high intertidal forests than in low intertidal forests. Most studies suggest that it is probable that the link between leaf litter and crab consumption is important throughout Southeast Asia. The crab-leaf link has two important implications with respect to nutrient turnover and nutrient flux between mangroves and coastal waters. Firstly, leaf turnover rates in Asia may be much faster when compared to systems where decomposition of litter occurs primarily through leaching and saprophytic decay. Secondly, high turnover rates, by releasing materials tied up in leaf biomass, may have a significant impact on the larger consumers, since more food is readily available. This also implies that reduction in the amount of leaf fall through logging will have a faster impact on consumers in these areas.
Retention of leaf production in the mangrove forest may affect potential rates of tidal export to adjacent coastal waters. Litter export and removal experiments suggest that approximately 19.5 kg DW.ha-1.d-1 could be exported to adjacent coastal waters. Modifying the above figure for crab removal (e.g., 4.2 kg. ha-1.d-1) would reduce the export of litter by 11% to 15.3 kg DW.ha-1.d-1. In addition to consuming fallen leaves, sesarmid crabs can remove a large percentage (76%) of available propagules. Since propagules make up approximately 16% of litter fall, the export of organic material to the coastal waters would be even lower.
ROLE OF BACTERIA. Decomposition of mangrove litter and detrital material is a microbially mediated process (Alongi 1988). Decomposing leaf material and fine particulate and dissolved organic matter in the mangrove soil support extremely high bacterial densities and productivity. The numbers of heterotrophic bacteria in mangrove soil are generally two to three orders of magnitude greater than in the waters above them (Millis 1981). Bacterial densities average about 1.1 x 1011 cells g DW-1, while bacterial productivity accounts for 1.6 g C.m-2.d-1, with maximum values of about 5.2 g C.m-2d-1 (Alongi 1988). Between 0.5 to 10 g C.m-2.d-1 maybe required to support the bacterial productivity, and total net primary production in Australian mangroves may range from 0.5 to 12 g Cm-2.d-1 (Robertson 1987; Alongi 1988). The data suggest that most of the primary production in mangroves is channeled through bacteria before becoming available to higher consumers. Exploitation of mangrove forests, especially through logging, should minimize the impacts on benthic bacterial communities.
Herbivory in Mangroves
Even though mangrove forests in general contain a high biomass of organic plant matter, rich in fiber, minerals, protein and amino acids (Soeroyo and Atmadja 1994), relatively few organisms feed directly on live mangroves. Herbivory is the direct exploitation of living plant (i.e., mangrove vegetation) tissue by animals, and in the mangroves it includes groups such as insects, crustaceans, molluscs and mammals (Murphy 1990). The definition includes the consumption of all mangrove plants, including diatoms, algae, lichens and vascular plants. In this discussion we restrict ourselves to the consumption of mangrove plant tissue before abscission. As Sivasothi et al. (1993) point out, consumption of mangrove plant material after abscission is generally referred to as litter consumption (i.e., processing), and should not be considered as herbivory. While some scattered information exists on the herbivory of various crabs (Watson 1928; Crichton 1960; Warner 1967; Von Hagen 1977; Hutchings and Recher 1982; Rodelli et al. 1984; Rau and Murphy 1990; Sivasothi et al. 1993), very little is known about them in Indonesia. Our rather limited knowledge of this subject is reflected in a recent review (Wolcott and O'Conner 1992) where it was stated that: "Crabs do not eat living leaves in the Indo-Pacific region…". This sweeping generalization is clearly no longer valid considering the new evidence provided by Rau and Murphy (1990) and Sivasothi et al. (1993).
Throughout Indonesia, mangrove litter is widely used as animal feed for cattle and goats, indicating the high potential nutritional value of this resource to mangrove inhabitants. Hutchings and Saenger (1987) noted that in Australia, both kangaroos and wallabies graze on live mangroves. While Indonesian mangroves support a highly diverse fauna, very little is known about the trophic structure of these communities, including the mangrove herbivores.
Insects. Mangrove forests are frequently called mosquito-infested swamps, and therefore it seems appropriate that something should be mentioned about mosquitoes, even though they are not part of the herbivorous group of insects. What role mosquitoes play in the mangrove food chain remains elusive. They are mentioned here only because of their great abundance, their impact on human health, and their significant nuisance value to most mangrove workers. Table 19.10 lists the most common mosquito species associated with mangroves. It is assumed that mosquitoes have no role in the direct consumption of mangrove primary production, however, their diets remain generally unknown. The most obvious predators of adult mosquitoes are birds and amphibians. During their aquatic larval life cycle, mosquito larvae may make a significant contribution to the benthic food chain, and various marine organisms (i.e., fish) feed on them.
Among the most common mosquitoes in Southeast Asia is the Anopheles (Myzomyia) sundaicus, which apparently is restricted to the western regions of the Indonesian Archipelago, where it is responsible for most cases of malaria (MacNae 1968). According to MacNae (1968), Aedes amesiiis the most common mosquito in mangroves from Malaysia and Sumatra to the Philippines and Thailand. In Sulawesi alone, there are about 125 species of mosquitoes, but only four genera act as vectors for debilitating diseases, such as malaria (Anopheles and Culex), dengue fever (Aedes)and filariasis (Mansonia and Culex) (Whitten et al. 1988). Mosquito attacks are not restricted to any particular group of organisms, since MacNae (1968) reported that he observed mosquitoes biting the heads of mudskippers (Boleophthalamus boddaerti). However, certain mosquito species show preferences for specific hosts.
While mangrove insects have been poorly studied, they played a key role in the development of the theory of "Island Biogeography" (MacArthur and Wilson 1967). A number of small mangrove islands, dominated by Rhizophora mangle, in the Florida Keys were used as natural laboratories to study the theory of island biogeography. Why would small Florida mangrove islands be so important? According to Wilson (1992): "We needed a series of little Krakataus, islands that could be completely cleared of all insects, spiders, and other arthropods and then monitored month by month. To accomplish that much would be to witness recolonization from scratch and to learn unambiguously whether biodiversity is at equilibrium". Wilson (1992) mentions that the experiments in the Florida Keys were inspired by the Krakatau eruption and the subsequent recolonization of Anak Krakatau. The large-scale field experiments in Florida provided a wealth of new information on island colonization, including the fact that each, seemingly empty, mangrove island, supported over 100 species of insects (Simberloff and Wilson 1969, 1970; Wilson and Simberloff 1969). After the induced catastrophic disturbance (i.e., fumigation), the insect fauna of the mangrove islands returned rapidly (i.e., in less than a year) to near their original numbers (Simberloff and Wilson 1970). However, the equilibrium was dynamic with a high degree of species turnover. Only 7% to 28% of the new colonists were the same as those present before the fumigation (Wilson 1992).
Table 19.10. Common mosquito species that are associated with mangroves.
Murphy (1990) provides an excellent account of insect herbivory in Singapore mangroves, where 102 insect species were documented to attack 12 principal mangrove genera (i.e., Avicennia, Lumnitzera, Excoecaria, Pemphis, Aegiceras, Bruguiera, Rhizophora, Ceriops, Sonneratia, Heritiera, Hibiscus and Thespesia). With copious colour photographs (over 260), Murphy's (1990) wonderfully illustrated publication provides an excellent introduction to insect herbivory in Malayan mangroves.
How important are herbivorous mangrove insects? Research conducted in the Caribbean suggests that herbivory by insects and crabs is relatively insignificant, and accounts for a very small portion of the total litter production (Heald 1971; Onuf et al. 1977; Beever et al. 1979). Looking at the Indo-west Pacific mangroves, with their great abundance and diversity of insects, it seems logical to assume that herbivorous insects may play a significant role in the structure and function of mangrove communities (Hutchings and Saenger 1987). It is, therefore, rather surprising to learn that direct consumption of live mangrove leaves by herbivorous insects represents only about 2% of leaf primary production (i.e., leaf litter fall) (Robertson and Duke 1987a). In his review of plant-animal interactions in mangrove ecosystems, Robertson (1991) concluded that herbivorous insects consume less than 5% of canopy production. Johnstone (1981) reported that mangrove species in Papua New Guinea lose less than 10% of their leaf surface area to herbivorous insects, however, Robertson and Duke (1987) suggested that the PNG values are probably much lower.
Insect herbivores can be broadly classified into grazers (i.e., consumption of solid plant tissue) and sap-flow ectoparasites (i.e., piercing and sucking insects that feed on sap) (Murphy 1990). However, most damage to mangrove vegetation is done by grazing insects. Some bugs (Hemiptera) are known to inject toxins that cause local lesions, resulting in severe damage to plant tissue. Murphy (1990) observed that foliage damage may be internal, as with leaf miners, from the edge or from dorsal or ventral surfaces (i.e., patch grazing). Young mangrove seedlings may be especially sensitive to insect attack due to their lower physical toughness relative to mature plants (Robertson 1991). For example, leaves of Avicennia marina seedlings suffer greater leaf loss to insect herbivores than the more mature saplings (Robertson and Duke 1987). It appears that seedlings of A. marina and Xylocarpus granatum are particularly susceptible to mortalities associated with insect attacks (Robertson 1991). Young leaves of Avicennia alba can be heavily grazed by two species of the Monolepta cavipennis complex (Coleoptera, Chrysomelidae) (Murphy 1990). Some insects may be specific to particular mangrove species (i.e., they are structurally limited to one mode of attack), but feeding strategies and food preferences may change during their development (Murphy 1990).
Table 19.11. Known herbivorous insects from Singapore. O: order; SubO: suborder; SF:
Table 19.11 provides the list of known groups of herbivorous mangrove insects recorded in Singapore (Murphy 1990). The two most important groups of herbivorous insects in mangroves are the Orders Lepidoptera (Butterflies and Moths) and Coleoptera (Beetles) (Murphy 1990). While butterflies and moths are grazers only during their larval stages, the beetles are herbivorous either during their larval (e.g., Mordellidae) or adult life cycles, or both. Beetles do most of their damage during the "maturation-feeding", when females are maturing eggs (e.g., Scarabaeoidea and Chrysomeloidae) (Murphy 1990). The grasshoppers (Orthoptera) and their allies apparently feed during all stages.
The main controlling factor of leaf consumption by herbivorous insects is the nutrient content of the leaves themselves. Some mangrove species that are used for medicinal purposes by local people seem to suffer little from insect grazing pressures. For instance Excoecaria agallocha, whose sap and wood are used to make strong purgatives and fish poisons, suffers less than 1 % leaf loss to grazing. Furthermore, Ohigaski et al. (1974) demonstrated that, when damaged, the leaves of E. agallocha exude a sticky latex sap with strong piscicidal properties, and may thus act as a deterrent to insect herbivores (Robertson 1991). Nonetheless, Whitten and Damanic (1986) reported large-scale defoliation of Excoecaria agallocha by large caterpillars of Ophiusa melicerata (Lepidoptera, Noctuidae) in the Belawan area of North Sumatra. However, the defoliation did not cause any mangrove mortality. Murphy (1990) points out that large-scale local defoliation can also occur from day-feeding gregarious caterpillars of Selepa discigera (Lepidoptera, Noctuidae), and that Excoecaria can be heavily grazed by pheneropterine nymphs (Orthoptera, Tettigoniidae). This illustrates that mangrove chemical defenses (very weak) are not effective against all insect herbivores. Other mangrove trees that seem to be resistant to insect attacks are species belonging to genera Rhizophora, Bruguiera and Ceriops (Robertson and Duke 1987a).
Insects may have their greatest influence on mangrove structure through their predation on mangrove seeds. It has been demonstrated that infestations of insects such as scolytid beetles Poecilips rhizophorae can severely affect the viability of Rhizophora mangle propagules (Onuf et al. 1977). Studies from Queensland, Aus tralia, reported that 20%-80% of seeds/propagules of eight common mangrove species were damaged by insects (Robertson 1991). Similar damage has been reported in Singapore, where Avicennia propagule mortality seems to be very high (Murphy 1990). Among the most notorious are the caterpillars of Eupoicilia (Lepidoptera, Tortricidae), which also attack buds of Bruguiera cylindrica (Murphy 1990). Numerous other insects, such as weevils and moths, attack the flower buds and fruits of all mangroves, which reduces propagule viability. Table 19.12 illustrates the high frequency of insect infestation of seeds and propagules of Australian mangroves.
While herbivorous insects may play a relatively minor role in overall trophodynamics of mangrove ecosystems, locally they can be very important. It has been shown that insects can remove up to 35% of leaf area from some mangrove species and cause high seedling mortalities (Robertson 1991). As was pointed out by Murphy (1990), while insects rarely cause severe damage to healthy plant hosts, they respond rapidly to declining resistance. Major changes in insect population densities and/or species composition in mangrove forests may be indicative of changing environmental conditions, that can be either natural or anthropogenically induced (i.e., pollution, over exploitation, etc.). There is a possibility that certain insect groups may be used as indicator organisms, however, research in this field in Indonesia is nonexistent.
Litter-Eating Crabs. Mangrove crabs (Grapsidae) are among the major consumers of mangrove litter. The crabs that feed on mangrove litter (i.e., abscised leaves) are not considered here as herbivores, and the vast majority of them are mud-burrowing species rarely venturing far from their burrows. Herbivory in mangrove crabs is associated with tree-climbing ability. Surprisingly, very little information exists on herbivory by crabs in Indo-Pacific mangroves (Rail and Murphy 1990; Sivasothi et al. 1993). Two groups of tree-climbing crabs were identified in Singapore mangroves. The first group consists of burrowing crabs of the genus Episesarma which are facultative climbers during periods of nocturnal low tide (Sivasothi et al. 1993). Episesarma versicolor, E. chengtongense and E. singaporensehzve been observed to climb trees to heights of 5 m or more. The second group of tree-climbers consists of the non-burrowing habitual climbers Selatium brockii, Metopograpsus gracilipes and M. latifrons (Sivasothi et al. 1993). S. brockii climbs up to 4 m while Metopograpsus are rarely seen above 3 m.
Table 19.12. Mean percentage of dispersed mangrove seeds or propagules attacked by insects.
Not all tree-climbing crabs are, however, herbivorous. It appears that crabs from the genus Episesarma are, in fact, the only true herbivores. Supporting evidence comes from actual observations and gut content analysis (Sivasothi et al. 1993). Based on gut analysis, Avicennia leaves are the main diet of Episesarma spp., which appear to be nocturnal foragers (Sivasothi et al. 1993). The other two genera of tree-climbers are also nocturnal-feeders, but they do not feed on vascular plant tissue. Both Selatium and Metopograpsus feed predominantly on epiphytic algae, lichen and fungi which they scrape from the surface of tree trunks and in between fissures in the bark (Sivasothi et al. 1993). However, it has been suggested that Metopograpsus is primarily a carnivorous crab, since it has been observed to attack Selatium brockii and to feed on animal carcasses (Sivasothi et al. 1993). It was further reported that all tree-climbing crabs will consume dead animal matter. It is apparent that Episesarma spp. are not obligate herbivores, and will opportunistically scavenge for any available food, including mangrove litter. Sivasothi et al. (1993) suggested that Episesarma may be forced to climb and consume fresh mangrove leaves when litter is scarce. Episesarma spp. inhabit a range of inundation frequencies, and thus tree-climbing and herbivory is a response to the low availability of mangrove litter which, under strong tidal regimes, is flushed away.
Mangrove Flora and Fauna
Flora. In Indonesia, there are at least 47 principal mangrove species, the majority being trees. Of the 115 plant species recorded in Indonesian mangroves (i.e., mangrove-associated), there are 75 trees, 10 bushes, 10 lianas, eight herbs and grasses, two ferns, six parasites and four epiphytes (table 19.13). The least known components of the terrestrial mangrove flora appear to be the epiphytic and parasitic plants. In general, epiphytic plants are very sensitive to saltwater, and as a result they are restricted mainly to areas under fresh-water or terrestrial influence. According to Tomlinson (1986), even in back mangrove areas the epiphytes are limited to the high canopy. They become more abundant in the transitional communities that lead to terrestrial vegetation. Table 19.14 lists the known epiphytic plants found in Sarawak (Malaysia, Borneo) mangroves, which are most likely also found in East Kalimantan.
In addition to the terrestrial plant component, there are marine macrophytes associated with certain mangrove species, particularly with the stilt roots of R. apiculata and R. mucronata. However, few mangrove algal studies have been carried out in Indonesia, and our knowledge is extremely fragmentary. Saenger et al. (1977) have conducted an indepth literature survey and found that 16 species of Chlorophyta, one species of Phaeophyta (i.e., Colpomenia sinuosa), 25 species of Rhodophyta, 37 species of Cyanobacteria (Cyanophyta) and one species of Chrysophyta (Vanheurekia lewisiana) were associated with Australian mangroves and salt marshes. Hutchings and Saenger (1987) noted that 94 species of algae have been recorded from trunks, pneumatophores, stilt roots and canopies of mangroves in Australia, the majority belonging to Rhodophyta (55 species) and Chlorophyta (24 species). Comparable lists are still lacking from Indonesia.
Table 19.13. Vegetation associated with mangrove forests in Indonesia. '*' indicates principal mangrove species. Type: T - trees; P - parasites; B - bushes and shrubs; H. herbs and grasses; F - Ferns; L - lianas and climbers; E - epiphytes.
Erftemeijer et al. (1989) reported that in Bintuni Bay, Irian Jaya, Gracillaria crassa was very common between the pneumatophores of Avicennia and Sonneratia alba. Tomascik and Mah (1994) documented an interesting epiphytic flora associated with Rhizophora stilt roots in the anchialine lagoon of an uplifted atoll (Kakaban Island) off the east coast of Borneo. The entire shoreline on the anchialine lagoon is fringed by a thin mangrove belt dominated by Rhizophora spp. along the outer margin. The stilt roots form almost a continuous wall around the 390 ha lagoon. An unusual feature of the lagoon is the total absence of large herbivores. The dominant macrophytes in the lagoon are two species of Halimeda and three species of Caulerpa. The most abundant epiphytes found on the Rhizophora stilt roots are Halimeda tuna, Caulerpa sertularoides, C. lentillifera and C. racemosa (fig. 19.34). The great profusion of these macrophytes throughout the lagoon may be related to the total absence of large herbivores (Tomascik and Mah 1994). The unusual epiphytic lifestyle of Halimeda tuna may be related to environmental characteristics of the lagoonal waters. Under normal marine conditions CaCO3 content of H. tuna is about 91.6% (Drew and Abel 1985), however, in Kakaban Lagoon the CaCO3 content is only 71.2% (Tomascik and Mah 1994). None of the macrophytic epiphytes are found in the intertidal portion of the roots. The most luxuriant growth seems to occur in slightly shaded locations. While most mangrove-associated macrophytes prefer shaded environments, Atherton and Dyne (1975) reported that Enteromorpha clathrata prefers brightly illuminated open spaces. We have observed this in Kakaban Lagoon, where E. clathrata is an epiphyte on Halimeda opuntia, which forms extensive monospecific meadows throughout the lagoon. E. clathrata forms a unique "canopy" which is a major habitat for a new synaptid sea cucumber Synaptula spinifera (Massin and Tomascik 1996).
Table 19.14. List of epiphytic plants associated with mangrove vegetation in Sarawak (Borneo), Malaysia.
Figure 19.34. Epiphytic communities on Rhizophora stilt roots. A) Halimeda tunacovers most of the subtidal portion of Rhizophora stilt roots. B) Mixed epiphytic community (H. tuna, Caulerpa racemosa, C. sertularoides, C. lentillifera) (sponges and tunicates) on subtidal stilt roots of Rhizophora sp., Kakaban Lagoon, East Kalimantan.
Photos courtesy of R. Steene, Cairns, Australia.
Mangrove Fauna
Molluscs. Indonesian mangrove forests support a rich molluscan fauna consisting of about 90 species belonging to 32 families (Kartawinata et al. 1979; Sabar et al. 1979; Kastoro et al. 1991). However, this list also includes molluscs from fronting and adjacent mangrove habitats, such as tidal creeks and mud flats (fig. 19.35). Because of their strong physico-chemical (i.e., currents, tides, outwelling of organic particulate matter and nutrients, etc.) and biological linkages (feeding grounds, nursery grounds, animal migrations, etc.) to mangroves, these transitional (i.e., ecotones) habitats are considered as part of the mangrove ecosystem. According to MacNae (1968), relatively few families of molluscs have actually adapted to live inside the mangrove forests. Only two families of gastropods, namely Potamididae and Ellobiidae, evolved life history strategies that allowed them to invade mangrove habitats.
Figure 19.35. Tidal mud flats are an important component of mangrove ecosystems. Tidal mud flats are important feeding areas for resident, wintering and migrating waterbirds.
Photo by Tomas and Anmarie Tomascik.
In studies conducted in the mangroves of Morowali, Central Sulawesi, Budiman and Darnaedi (1984) found that the community structure of molluscs consisted of 22 species. Class Gastropoda was represented by 16 species, Bivalvia by six species. However, when we examine the data from other Indonesian mangrove regions, it appears that bivalve diversity is comparable to gastropods; nonetheless, there is considerable temporal (i.e., monsoonal) and spatial variability (Kastoro et al. 1991). Furthermore, bivalves, with the exception of mangrove root epifauna, are restricted primarily to tidal creeks, estuaries and mud flats, while gastropods, due to their motility and various physiological adaptations, have been able to spread through much of the mangrove forest. Table 19.15 provides a list of recorded molluscs known to be associated with Indonesian mangrove ecosystems. Interestingly enough, the molluscan fauna did not exhibit strong distributional patterns in the Morowali mangrove forest, however, the bivalves recorded in the mangroves were proportionally larger than in other known Indonesian mangrove areas (Soemodihardjo 1987). The most abundant bivalves in Morowali were Brachydontes bilocularis, Crassostrea cucullata and Spondylus hystrix.Table 19.16 lists the various known molluscan species recorded in Indonesian mangroves, and compares them in a regional context with regions outside of the archipelago.
Numerically, gastropods are the dominant group of molluscs in Indonesian mangroves. At the seaward margin of most mangroves Littorina scabra is frequently found in large numbers, accompanied by Monodonta labio (Soemodihardjo 1987). Littorina melanostoma is frequently found attached to tree trunks well above the high water mark, whereas L. scabra seems to prefer leaf substrates, since it is usually observed attached to leaves. Kartawinata et al. (1979) found that in the interior of mangrove forests Ellobiidae and Potamididae are the dominant molluscs. Along the mangrove fringe in Kakaban Lagoon, Cerithidea sp. (most likely a new species) is very abundant under the mangrove canopy. Unlike other cerithids (e.g., Cerithidae decollata) the Kakaban species does not climb trees, which may be related to the relatively narrow tidal range (i.e., 19 cm). However, it was seen attached to the knee-roots of Bruguiera sp.
In Indonesia, Potamididae are an important intertidal component on many coral islands fringed by mangroves. On Pulau Rambut, southwest Java Sea, Terebralia palustris occurs in very high densities (>130 indiv.m-2), and is an important source of cheap protein for local communities (Soemodihardjo and Kastoro 1977). It is, however, restricted to the sheltered west side of the island, where it is associated with Terebralia sulcata and Telescopium telescopium, usually in a Rhizophora stylosa community (Soemodihardjo and Kastoro 1977). The mangrove forest of Pulau Rambut is dominated by Rhizophora mucronata, with R stylosa being the pioneering species often colonizing reef flat areas just behind the shingle rampart (Kartawinata and Walujo 1977). On the neighbouring Burung Island, Soemodihardjo (1987) reported that population densities of Terebrallia and Telescopiumcan reach 480 indiv.m-2. On the mud flats of Tatawori Estuary, Bintuni Bay, gastropod densities reach 142 indiv.m-2 and are dominated by Melampus (Erftemeijer et al. 1989). Inside the mangrove forests, Nerita spp. and Littorina spp. are found on mangrove roots and tree trunks, whereas Telescopium telescopium dominates the intertidal substrate where it feeds on detritus and epibenthic microalgae.
The bivalves in Indonesian mangroves are represented by only a few species. The dominance of gastropods is related to their epibenthic nature. However, the bivalve Enigmonia can be found attached to mangrove leaves deep inside the mangrove forests. According to MacNae (1968), Enigmonia rosea can be found on mangrove leaves of the most seaward trees. Bivalves present in mangrove soils must be able to tolerate long periods of high temperatures and low oxygen, and as a result only a few groups have been able to adapt to these harsh conditions. However, bivalves become a dominant benthic component at the seaward margin of mangrove forests frequently characterized by extensive intertidal mud flats. Kastoro et al. (1991) found that the molluscan soft-bottom community of a mangrove creek in Grajagan (south coast of East Java) was dominated by bivalves in biomass as well as species richness. Most bivalves in mangrove habitats are found in the seaward mud flats, where they are an important source of food for waders and other waterbirds, and thus they are.not strictly mangrove species. Erftemeijer et al. (1988) found that the average benthic biomass of Segara Anakan mud flats was 2.9 g AFDW.m-2, which apparently is low, even though the average density of benthic organisms was about 6123 indiv.m-2. In contrast, benthic biomass values from mud flats at the Brantas and Solo deltas varied from a low of 0.03 g AFDW.m-2 to a high of 36.8 g AFDW.m-2 (Erftemeijer and Djuharsa 1988). The average benthic biomass for the Brantas and Solo delta study was 8.7 g AFDW.m-2, which, according to Erftemeijer and Djuharsa (1988), are comparable to other important areas for migrating or wintering waders. Average benthic biomass on the extensive mud flats at the Tatawori Estuary in Bintuni Bay, Irian Jaya, was measured at 10.4 g AFDW.m-2 (Erftemeijer et al. 1990). Interestingly, the benthos at the Tatawori Estuary was dominated by crabs (up to 120 indiv.m-2), including a large number of Uca seismella (Erftemeijer et al. 1990). This small fiddler crab was believed to be endemic to Australia (George and Jones 1982), and thus its occurrence in Bintuni Bay was an important new discovery.
Table 19.15. The molluscan fauna associated with Indonesian mangrove forests.
Table 19.16. Molluscan families and species reported from the mangrove forests of Asia and Oceania. Asia: 1) India, Sri Lanka, Burma and surroundings; 2) China, Japan and surroundings; 3) Malaysia, Indonesia (western part), Thailand, Philippines and surroundings. Oceania: 4) Eastern Indonesia (Moluccas, Irian Jaya and surroundings; 5) Australia, New Zealand and surroundings; 6) Pacific islands. Regions including parts of Indonesia in bold.
Crustaceans.
CRABS. About 80 species of highly specialized crustaceans have been recorded in various Indonesian mangroves. Crabs, with about 50 known species (Brachyura), are the most important group of mangrove invertebrates (table 19.17). The crustacean fauna of Indonesian mangroves has been briefly mentioned by Soemodihardjo (1987). The role of crabs in the structure and function of mangrove communities has been discussed earlier. The landward fringe of mangroves, and most tambak areas, are dominated by the land crabs of the Family Gecarcinidae. According to MacNae (1968), Cardisoma carnifex is the most closely mangrove-associated land crab species. As a result of mangrove conversion to tambaks, many mangrove brachyurans, particularly sesarmids, have been outcompeted by the more opportunistic land crabs, which are able to feed on a greater variety of terrestrial food (fig. 19.36). Sesarmids belong to the Family Grapsidae, which includes a variety of mangrove-associated crab genera (e.g., Utica, Metasesarma, Metopograpsus, Cyclograpsus, Helice, Clistocoeloma, etc.). Mangrove conversion into tambaks has greatly reduced mangrove litter fall in many coastal areas. Mangrove litter fall is the primary food source for the majority of mangrove crabs. Furthermore, many sesarmids and tree-climbing crabs (Episesarma) have a strong food preference for certain mangrove leaf litter, thus, afforestation with monospecific stands of Rhizophorahas limited benefit for many crab species. For example, while Chiromantes bidens has a strong preference for decaying leaves of Kandelia candel, Sesarma dehaani prefers the fallen leaves and seeds of Bruguiera gymnorrhiza. Sesarmid crabs known to feed on Rhizophora leaf litter or seedlings are Sesarma taeniolata (=mederi), Sesarma meinerti, Parasesarma pictum and Chiromantes messum. However, most of the available information on mangrove crabs comes from outside of Indonesia, and therefore it may not be necessarily applicable. Unfortunately, no data on sesarmid food preferences are available from Indonesian mangroves.
In terms of economic importance, the portunid crab Scylla serrata is by far the most important. Scylla is a carnivorous scavenger living in deep burrows around the roots of mangrove trees as well as along the banks of rivers and tidal creeks. It is the only swimming portunid crab characteristic of mangroves. It is primarily a nocturnal scavenger-restricted to the intertidal zone. Crabs in subtidal habitats will venture out in late afternoons and move into the mangrove forest with incoming tides. The species exhibits colour plasticity. It is frequently deep green in the western regions of the archipelago, while mostly dark brown in some eastern localities (e.g., Bintuni Bay). While they inhabit mangrove swamps during their adult lives, females migrate to marine coastal waters where they spawn (mating takes place in mangrove environments), while the males remain in mangroves. The megalopa larvae begin to move into the estuarine environments. By the post-larval stage they are sedentary and mature in mangrove and estuarine habitats.
Verwey (1930c) used crab abundance and their clear distributional patterns to develop a zoning classification for the mangroves along the Jakarta Bay coastline and some small mangrove islands in the bay. Moving from the sea inland the five zones are: 1) Scylla serrata zone; 2) Metaplax elegans zone; 3) Uca signatus zone; 4) Uca corsobrinus zone; and 5) Sesarma taeniolata zone. With the large-scale conversion of coastal mangroves into tambaks, the crab fauna has undergone major changes. Scylla serrata is heavily exploited, and is one of the most popular items on seafood restaurants throughout Indonesia. However, efforts are being made, with some success, to culture Scylla on a commercial basis.
Figure 19.36. Mangrove conversions into tambaks or agricultural lands have changed crab distribution patterns. Cardisoma carnifex (A) is a land crab that is now common in tambak areas where it competes with sesarmid crabs such as Sesarma smithii (B). Rearing of the commercially important Scylla serrata (C) is very common in many artisanal tambaks.
Modified from MacNae 1968.
Table 19.17. List of common crab species recorded from Indonesian mangroves.
Figure 19.37. Two fiddler crabs (Ocypodidae). A) Uca dussumieri. B) Uca lactea.
From MacNae 1968.
The fiddler crabs are among the most conspicuous ocypodids (Ocypodidae) in intertidal mangrove areas where the substrate is more compact (fig. 19.37). The substrates are generally classified as 'sandy-mud' or 'mud', and are usually within the intertidal (Moosa and Aswandy 1983). Their burrows can be up to 30 cm long, and are curved to L-shaped. They can be found in various tidal zones and are not necessarily inundated by seawater every day (Moosa and Aswandy 1983). Worldwide, there are about 60 known species, with 24 species (depending on taxonomy used) in Indonesia (Crane 1975). Uca are gregarious, omnivorous detrivores which are active both day and night during low tides, when they can be seen moving about. They can locate their burrows, even in the dark, by kinesthetic orientation (Barnes 1980). However, they tend to be more active during diurnal low tides. Uca and many other small ocypodid crabs feed on detritus and benthic microphytes (e.g., diatoms). Food particles are picked (i.e., selected) from the sediment surface, while the rest of the material is rolled into small pellets which are left behind to form intricate patterns on the hard substrate, a noticeable feature of large Uca colonies.
Their burrow entrances are also surrounded by small sand balls, which the crabs roll out of their burrows during daily burrow maintenance. Uca are always found in large colonies, most frequently on seaward mud flats, and exhibit distinct zonation (i.e., species separation). They are best known for their intricate mating (i.e., courting) and aggressive behavioural patterns. One of the claws in the males is enlarged, and is used to attract females and to repel other males.
The zonation of Uca in most mangroves is a result of habitat partitioning based on particle size of the substrate on which the crabs feed, using specialized feeding maxillipeds that are distinctive of each species. The chelae function as spoons to scoop the sediment, which is then transferred to the mouth parts, which are the highly specialized first and second maxillipeds (fig. 19.38). In the small mangrove in the inner Ambon Bay (i.e., mangrove Passo), Uca vocans is the dominant species of the seaward mud flats and fringing Sonneratia vegetation (Susetiono 1989). Uca triangularis and U lactea dominate in the landward portion of the Sonneratia vegetation and the mixed mangrove forest. Further inland, the transition from the mixed mangrove forest (i.e., Sonneratia, Avicennia, Rhizophora, Bruguiera) to Nypafruticans forest excludes all species except Uca triangularis. However, in the monospecific Nypa fruticans forest Uca vocans once again dominates (Susetiono 1989).
Figure 19.38. Specialized maxillipeds of three common fiddler crabs inhabiting different substrate types. From the top: I) Uca lactea f. annulipes - feeds off sand; II) Uca urvillei - feeds off fine mud; III) Uca dussumieri - feeds off very fine mud. Horizontal: A) Outer view of first maxilliped; B) Inner view of second maxilliped; C) Outer view of third maxilliped.
Modified from MacNae 1968.
One of the most detailed studies of Uca distributions is that of Moosa and Aswandy (1983) for the Sunda Strait. They found 10 species which have relatively wide distributions throughout the archipelago (fig.19.39). However, comparable studies are lacking and thus very little can be determined about their general distribution patterns. The high diversity of Uca in Indonesian waters may be a function of geography, since the archipelago is a mixing-pot of species from three distinct biogeographical regions, namely the Indian Ocean, Asia (Japan, Philippines, Indochina) and Australia/New Guinea (Moosa, unpubl.).
Figure 19.39. Distribution of Uca species known from the Sunda Strait and other parts of the Indonesian Archipelago.
From Moosa and Aswandy 1983.
Figure 19.40. The robber crab or coconut crab
Birgus latro.
Photo by Tomas and Anmarie Tomascik.
As was pointed out by MacNae (1968), the landward fringe of mangrove forest is theoretically equivalent to the supralittoral zone developed by Stephensons for rocky shores. The ecotone between mangrove forests and the dryland vegetation is inhabited by a variety of land crabs and hermit crabs. Hermit crabs are abundant, particularly on coral islands with well-developed pes-caprae associations just landward of the mangrove. In some areas of the eastern archipelago, one conspicuous member of the hermit crab group (Anomura, Coenobitidae) that should be mentioned in this discussion is the robber crab Birgus latro (fig. 19.40). Sir Francis Drake reported on this unusual animal from his stop in Celebes (Sulawesi), where, in fact, he had to abandon his cannons after being grounded on the reefs of Vesuvius Atoll in the Banggai Islands. However, it was Rumphius who first made a detailed description of this species. In the past, Birgus latro was widespread throughout the archipelago. However, it had the misfortune to be an excellent-tasting dish, and therefore it is not surprising that its distribution has been severely reduced. In many regions of the archipelago, the robber crab has become locally extinct, and is in fact fully protected under Indonesian law. Nonetheless, it is a common delicacy that is still being served in restaurants in Jakarta.
The robber crab, while being fully adapted to its terrestrial lifestyle, will drown if immersed in water, yet relies on the sea for reproduction. The branchiostegites in robber crabs are equivalent to lungs, which has made the gills mostly redundant. However, the most unique feature of this group is their tree-climbing ability, which allows them to exploit a wide range of foods. However, robber crabs feed primarily on the ground, where they scavenge for fallen ripe fruits (e.g., Pandanus fruits). On most coral cays they feed primarily on coconuts, which are very abundant throughout the archipelago. At night they may be seen climbing coconut trees, and in many areas they are in fact called "coconut crabs" (kepiting kelapa).Mating takes place on land, however, the females spawn their eggs directly into the sea. Not much, however, is known about their life cycles.
Figure 19.41. Thalassina anomala, a side view of a female. The second pair of walking legs are modified, and are used to push up mangrove mud to build the characteristic mounds.
Modified from MacNae 1968.
Thalassinidae. The mud lobster Thalassina anomala is among the most important mangrove sediment "mixers" (fig. 19.41). Mud lobsters build large U-shaped tunneling burrows that are 2-3 m long, extending up to 1.5 m below the sediment surface. Their burrow entrances are surrounded by a thick wall of mud mat extends 4075 cm above the entrances. Mud lobsters are nocturnal and the burrows are closed during the day with a mud-plug that the lobsters remove at nightfall when they move out to forage. Through their burrowing, mud lobsters have a significant effect on mangrove structure. Large mounds of mud that are brought to the surface are often devoid of vegetation due to their acidic nature (acid-sulphate soils), which results from the oxidation of anoxic sediments full of FeS (Hutchings and Saenger 1987). In general, however, the burrowing activity of mud lobsters, and other burrowers, is beneficial since it allows drainage and oxidation of deeper areas of mangrove sediments.
Penaeid Prawns. It is now well recognized that mangroves play an important role in coastal productivity, and are closely linked with the life cycles of many economically important penaeid prawn species (Robertson and Duke 1987b; Robertson 1988b; Vance et al. 1990; Singh et al. 1994). The life cycle of the banana prawn Panaeus marguiensis is closely associated with mangroves, and, in Indonesia, Martosubroto and Naamin (1977) found a significant correlation (r = 0.89) between the total area of mangrove forests and the offshore commercial catch of prawns. This positive relationship has since been demonstrated by Camacho and Bagarinao (1987) for the Philippines, by Sasekumar and Chong (1987) for Malaysia and by Staples et al. (1985) for Australia. The positive relationship between the area of coastal mangrove vegetation and coastal penaeid and fish landings may be related to two factors: 1) mangroves are an important source of detritus (i.e., particulate organic matter) and nutrients that fuel the nearshore food chains; and 2) mangroves act as either nursery or feeding grounds or both (Singh et al. 1994). It has already been mentioned that the outwelling of mangrove nutrients to adjacent environments is most likely not significant. Most of the primary production is consumed within the mangrove system. However, the export of particulate organic matter (detritus) may have a significant role in offshore food chains. Mangrove waters are particularly rich in zooplankton, which the crab zoeae dominate in abundance and biomass. Robertson and Duke (1987b) demonstrated the role of mangroves as possible nursery and feeding grounds, since postlarvae, juveniles and small sub-adults of fish and crustaceans were significantly more abundant in mangrove habitats than in adjacent habitats such as seagrass beds. It is obvious that each mangrove habitat will have its own unique value with regards to its nursery or feeding-ground role. For example, three highly valuable fisheries are directly tied to mangrove habitats; these are the banana prawn (Penaeus marguiensis) fishery, the mangrove snapper (Lates calcarifer) fishery and the mangrove crab (Scylla serrata) fishery. Table 19.18 lists all commercially important penaeid prawn species, many of which may have direct links to mangrove habitats.
The commercial value of the Indonesian penaeid prawn fishery is substantial. Between 1972 and 1979, landings from offshore prawn fisheries fluctuated between 49,000 and 133,000 mt per year (Unar and Naamin 1984). In 1990, Indonesian penaeid prawn landings from offshore fisheries reached 143,993 mt. Since 1986 the landing fluctuated between 100,000 to 150,000. mt per year, and thus are not much different from the 1970 values. However, with a market value of US$6.65/kg, the penaeid fishery value in 1990 was a staggering US$957 million. The catch statistics clearly show that Indonesian prawn fisheries are currently being heavily overexploited. Combined with the rapid destruction of remaining mangrove forests, the future of Indonesian offshore prawn fisheries is in doubt. Ruitenbeek (1991) reported that, while the prawn fishery landings from Bintuni Bay in 1991 had a value of US$35 million, a large scale-wood-chip operation which was destroying large areas of mangrove (i.e., habitat destruction) had a projected value of US$20 million per year. More important, however, was the finding that the traditional uses from hunting, fishing and gathering in the vast mangrove forests accounted for a value of US$10 million per year! The importance of the mangrove forests to the local populations is clear.
Table 19.18. Penaeid prawn species commercially exploited in Indonesia. Fishery importance: 1) minor fishery; 2) medium fishery; 3) major fishery.
Fish Fauna. In Segara Anakan Lagoon, which represents the only large mangrove forest left in Central Java, various species offish (table 19.19), shrimps, crabs and molluscs were found either in the lagoon or in the tidal creeks (Ecology Team 1984). Twenty-nine fish species, representing 18 families, have been reported from the mangroves in the Kepulauan Seribu Complex, however, only eight species are considered as permanent residents (i.e., occurring at all stages of the tidal cycle). In comparison to the amount of literature available on Indonesian seagrass-associated fish, literature on mangrove fish fauna is depauperate.
One of the most in-depth surveys of Indonesian mangrove fish fauna was conducted in Bintuni Bay, which contains one of the largest, still undisturbed mangrove habitats in Indonesia. However, there are comprehensive reports on the riverine fish faunas of Papua New Guinea (Munro 1967; Kailola 1987; Roberts 1978; Harness 1979). The 1989 survey of Bintuni Bay recorded 144 fish species of which 16 were restricted to fresh water and the remainder occurred in either mangrove-Nypa streams or marine habitats to a depth of about 30 m (Erftemeijer et al. 1989). The extensive mangrove-Nypa zone forms a transitional area between the open waters of Bintuni Bay and the inland rain forest (Erftemeijer 1989). These vast mangrove forests of Bintuni Bay support 58 species offish, most of which are characteristic of tropical brackish-water habitats. Included in the fish fauna is a small gobiid Pandaka lidwilli, which has the distinction of being one of the world's smallest extant vertebrates, attaining maturation at a length of 6-8 mm (Erftemeijer et al. 1989). The most abundant groups offish in the mangrove-Nypa habitats were the catfish (Arius leptaspis), gudgeon (Priomobutis microps), glassfish (Ambassis) and puffers (Tetraodon erythrotaenia), which accounted for 60% offish biomass (Erftemeijer et al. 1989).
Most of Indonesian mangrove-associated fish species (table 19.19) are widely distributed throughout the central Indo-west Pacific region. Their wide distribution is related to their pelagic larval life cycles, which allows them to be transported by oceanic currents for considerable distances. It is therefore not surprising that species with the most restricted distributions lack pelagic life-cycle stages. Mouth brooding in the ariid catfish Batrachomoeus and demersal eggs of the plotosid catfishes Pseudomugil, Arrhamphus and Strongylura greatly restrict their potential dispersal to other regions. The two habitats that are comparable in table 19.19 are the mangrove-Nypa waterways in Bintuni Bay and the lagoon of Segara Anakan. The striking feature about these areas is that, given the general wide distribution of most mangrove-associated fish species throughout the Indo-west Pacific, these two man grove-associated habitats contrasted in table 19.19 share only a single species, Arothron reticularis. The open waters of Bintuni Bay have a strong estuarine component, with 24% of species inhabiting both marine and estuarine environments. In contrast, 53% offish species inhabiting the mangrove-Nypa zone are estuarine (Erftemeijer 1989).
Table 19.19. Indonesian mangrove-associated fish fauna. Irian Jaya (A): Mangrove Nypa waterways in Bintuni Bay; Irian Jaya (B): Bintuni Bay open water (marine); Java: SegaraAnakan Lagoon.
The fish fauna is affected by the tidal cycle in regions with a wide tide range. In Bintuni Bay, where tidal range can reach 5 m or more, many tidal creeks undergo tidal filling and draining. Mangrove forests in general have four types of aquatic habitats: 1) the well-lit seaward coastal intertidal areas; 2) well-lit open waters of main river branches, creeks and tidal channels; 3) poorly lit small creeks and tidal channels enclosed by thick mangrove canopy; and 4) the intertidal areas throughout the forest (e.g., among mangrove roots).
Mangrove Avifauna. Out of the 105 bird species recorded in Segara Anakan, at least 85 species are associated with the mangrove forests (Erftemeijer et al. 1988). The intertidal mud flats and mangroves of Segara Anakan are important habitats for large waterbirds such as herons (10 species) and storks (three species) (fig. 19.42). However, it appears that Segara Anakan is not a breeding area, since no nesting activity was observed. During a 1988 survey, Erftemeijer et al. (1988) recorded 164-186 milky storks in Segara Anakan. The milky stork (Mycteria cinerea) is one of the most endangered waterbird species in Southeast Asia, with an estimated population size of only 5000 birds (Verheugt 1987). The milky storks nest only in Indonesia, and there are only two known nesting sites, one at Pulau Rambut (West Java) and the other in Jambi (southeast Sumatra). It seems that Segara Anakan is a feeding ground, with birds foraging on the intertidal mud flats. The majority of the birds roost on top of small Avicennia trees/shrubs (Erftemeijer et al. 1988). Table 19.20 lists all the known heron and stork species from Segara Anakan.
Migratory waders such as the common sandpiper (Actitis hypoleucos) are common in Segara Anakan and other mangrove areas, where they forage along the banks of rivers and creeks. The extensive intertidal mud flats are, however, important feeding habitats for thousands of migratory and non-migratory waders. Erftemeijer et al. (1988) recorded 1440 waders during their survey. The majority of waders roost on the islets inside the Segara Anakan Lagoon during high tides, however, wimblers, Numenius phaeopus, are frequently found roosting on Rhizophora trees along rivers and creeks (Erftemeijer 1988). The lesser golden plover Pluvialis fulva was observed to roost in disturbed Nypa-Acrostichum areas. Table 19.21 lists the common waders encountered in Segara Anakan.
Table 19.20. Species checklist of herons and storks in Segara Anakan.
Figure 19.42. Large waterbirds such as the great egret (Egretta alba), little egret (Egretta garzetta) and purple heron (Ardea purpurea) are permanent inhabitants of many mangroves.
Photo by Tomas and Anmarie Tomascik.
Additional waterbirds found in many mangrove areas are Oriental darters Anhinga melanogaster and the white-breasted waterhen Amaurornis phoenicurus. Ducks and sea birds are frequently seen in mangrove areas with open lagoons. In Segara Anakan the gray teal Anas gibberifrons and lesser treeduck Dendrocygna javanicahave been sighted in the past (Erftemeijer et al. 1988). In addition to waterbirds, Erftemeijer et al. (1988) recorded 51 terrestrial bird species within the actual mangrove area. However, the only obligate mangrove bird species is the mangrove blue flycatcher Cyornis rufigaster, which, in Segara Anakan, seems to be excluded from the neighbouring woodlands by its competitive congener, the hill blue flycatcher Cyornis banyumas (Erftemeijer et al. 1988). The typical mangrove birds which can, however, be found in neighbouring forests are Pelargopis capensis (storkbilled kingfisher), Alcedo caerulescens (small blue kingfisher), Centropus nigrorufus(Sunda coucal), Pachycephala cinerea (mangrove whistler), Nectarinia sperata (purplethroated sunbird) and Nectarinia chalcostetha (copper-throated sunbird) (Erftemeijer et al. 1988). Segara Anakan appears to be the last refuge for a poorly known Javan endemic, the Sunda coucal Centropus nigrorufus. According to Erftemeijer et al. (1988), the species appear to be restricted to the Nypa and young mangrove stands at the seaward margin of the mangrove, where most of the vegetation was observed floating.
Table 19.21. Waders found in Segara Anakan.
The mangrove-associated tidal mud flats in eastern Sumatra are vital feeding grounds for about 28 species of migratory waterbirds, among which are two Red Data Book species, namely, the Asian dowitcher Limnodromus semipalmatus and the Nordmann's greenshannk Tringa guttifer (Danielsen and Verheugt 1990). The extensive mangrove forests of the proposed Sungai Sembilang Wildlife Reserve contain 141 bird species, many of which are extremely rare. For example, 90% of the world population of the milky stork Mycteria cinerea and the only known population of spot-billed pelican Pelicanus philippensis in Indonesia are found in Sungai Sembilang mangroves. Table 19.22 illustrates population trends of five species of large waterbirds in the Banyuasin Peninsula, South Sumatra. Most bird species are maintaining stable populations, however, Danielsen and Verheugt (1990) reported that the population of the lesser adjutant Leptoptilos javanicus has declined sharply since 1989. They have suggested that the decline may be associated with large-scale exploitation and/or extensive use of pesticides in the paddy fields.
Mangrove Mammals. The number of mangrove-associated mammals has declined dramatically, especially along the north coast of Java, where much of the once flourishing mangroves have been converted to shrimp ponds. The otters (e.g., Lutra), once common inhabitants of coastal waters, have virtually disappeared from the north coast of Java, hunted-out from tambak areas where they are considered as a pest. However, in more remote areas (e.g., South Sumatra) they maintain stable populations. Among the most unique mammal inhabitants of the mangrove forest in Kalimantan are the endemic proboscis monkeys, Nasalis larvatus. These relatively shy primates are mangrove-dependent (MacNae 1968), feeding primarily on young leaves of Avicennia and Sonneratia. Their digestive tracks have become highly specialized to digest mangrove leaves. They are frequently seen feeding along the banks of major rivers (e.g., Mahakam, Berau and Barito) during early morning hours and late afternoon. During the day the troops move into the adjacent forests, where they forage for other food. Considering their conservation value, it is surprising that very little is actually known about their functional role in the mangrove ecosystem. Other primates found in mangrove habitats are the crab-eating macaques, Macaca fascicularis, and the silvered leaf monkey, which feeds on crabs and whelks. Full species lists of associated mammal species in mangrove forests are often lacking in most reports. Among the most comprehensive mammal inventories is from the Sungai Sembilang mangrove forest (table 19.23).
Table 19.22. Large waterbird surveys in the Banyuasin Peninsula, South Sumatra 19841986 and monthly surveys 1988-1989.
From Danielsen and Verheugt 1990.
In Segara Anakan, mangrove-associated mammals are relatively rare, most likely as a result of human presence in the area. Erftemeijer et al. (1988) recorded groups of silvered leaf monkey Presbitys cristatus, as well as the crab-eating macaque Macaca fascicularis. In addition, squirrels, wild pigs and otters (Lutra perspicillata)have been observed. Occasionally, dugongs (Dugong dugon) and dolphins (Orcaella spp.) are observed in the Segara Anakan Lagoon (Erftemeijer et al. 1988).
Table 19.23. List of mammals recorded in the mangrove forests of South Sumatra.
Functional Role of Mangroves
The functional role of mangrove communities in coastal ecosystems has received a lot of attention due to their presumed link with important coastal fisheries (Odum and Heald 1972; Pauly and Ingles 1996; Singh et al. 1994). Numerous studies have shown that mangrove creeks contain significantly higher abundances of post-larvae, juveniles and small adult fish than adjacent seagrass beds or adjacent habitats in the area. What is, however, clear, is that mangrove areas within one mangrove stand can differ significantly in their importance as nursery grounds. There are currently two hypotheses to explain the differences in the abundance of juvenile and small fish among mangrove and other nearshore habitats. It is generally believed that the abundance of juveniles (fish and shrimps) is greater in mangrove areas than in sea-grass beds because of greater availability of food (i.e., prey items), and that mangrove areas, in general, may provide greater refuge from large predators than do seagrass beds or other comparable habitats (Robertson and Duke 1987b).
Mangrove forests and tidal channels are dominated, both in abundance and biomass, by zooplankton-feeders throughout the year (Robertson et al. 1988). Copepods form a major portion of diets during much of the year, but during the Australian summer (November-February) crab zoea dominate fish diets (Robertson et al. 1988). Mangrove waters during this period are dominated by brachyuran larvae. Summer is also the period of recruitment of post-larvae of many fish species. Therefore, it is possible that higher abundance of juvenile fish in the mangrove habitat during the summer months may reflect differences in prey densities and abundance among habitats (Robertson et al. 1988). The high abundance of crab zoea in mangrove waters may be a significant functional trophic link between the primary production of mangrove forests (i.e., litter fall) and the secondary production of several fish and crustacean species that utilize mangroves and estuaries as nursery grounds (Micheli 1993a,b). Figure 19.43 illustrates the various possible pathways that link primary production of mangrove forest to secondary production.
The Mangrove Forest Status in Indonesia
It is often stated that Indonesia supports the world's largest area of mangroves (Groombridge 1992; Giesen 1993; Sukardjo 1994). Review of Indonesian historical and recent government records suggests that 15 to 20 years ago, the coastal area under mangrove cover may have exceeded 4.3 million ha. However, overexploitation, conversion and mismanagement of this important coastal resource, coined the "edible wetland" (Petersen 1991 cited in Giesen 1993), during the past two decades has led to significant losses. The precise extent of mangrove losses in many areas remains uncertain, and as a result all present values for total Indonesian mangrove area coverage are probably gross overestimates. Depending on what database is used, total mangrove area in the archipelago varies from as much as 4.25 million ha (Bina Program 1982; Soemodihardjo and Serianegara 1989; Sukardjo 1994) to as little as 2.5 million ha remaining between 1986-1990 (Giesen 1993). Burbridge and Koesoebiono (1984) estimated that the total area of Indonesian mangroves was about 3,806,119 million ha. One of the major errors in most estimates relates to a great inconsistency in the estimates for mangroves of Irian Jaya. Giesen (1993) has pointed out that government computations range from 0.97 to 2.94 million ha, which clearly is insufficient accuracy for management purposes. Perhaps the best approximation of mangrove losses are available for Java, where 88.8% of former mangrove area (170,500 ha) has been lost. Most of the losses in Java can be directly attributed to conversion of coastal mangroves into tambaks, which, according to the 1991 government records, cover an estimated area of 128,740 ha (Directorate of Fisheries 1991). On Java, the province of Central Java retains the largest mangrove area, with about 13,577 ha, most of it concentrated in Segara Anakan on the south coast, while less than 1% of former mangroves remain in East Java. South Sulawesi has converted about 69% of its coastal mangroves into tambaks (c. 73,088 ha).
Figure 19.43. Main pathways of energy flow in mangrove and estuarine environments.
Alter Saenger et al. 1983.
The mangrove forests of Indonesia are among the largest in the world, and account for 67.7% of the total mangrove area in the ASEAN region (table 19.24). The forests of Irian Jaya dominate Indonesian figures, with some 55% of the mangrove area, while the rest of the islands contribute relatively little. For example, Sumatra accounts for 19.5% of the total mangrove area and Kalimantan 15.8%; the Moluccas account for 2.6% and Java and Nusa Tenggara 1.2% of the total mangroves in Indonesia (table 19.25).
Table 19.24. Mangrove area of ASEAN countries.
Table 19.25. Mangrove area (ha) estimates in Indonesia.
Economic Value of Mangroves. Not too long ago mangrove forests were viewed as mosquito-infested, unproductive wastelands without too many redeeming features. This view has changed dramatically within the past two decades, as it was realized that mangrove forests are not only essential ecological components of many tropical and subtropical coastlines, but that they are also an important economic asset to many tropical countries (table 19.26). While much of the pioneering work on the functional role of mangrove ecosystems originates from Florida (Odum 1971; Odum and Heald 1972, 1975), there has been a recent explosion of mangrove studies in Southeast Asia and Australia (e.g., ASEAN-Australian Cooperative Program in Marine Science), home to some of the most diverse mangrove ecosystems.
Much has been written about the importance of mangrove resources, both in terms of products taken directly from the mangroves themselves as well as from the amenities provided by the resource from within and beyond its boundaries (Saenger et al. 1983; Hamilton et al. 1984; FAO 1985; Dixon 1989). Products that are provided by the mangrove forests range from timber for boat building and home construction, to production of honey and medicines. In the past, mangrove wood has often been considered to be the most important commodity of mangrove forests (table 19.27). Unfortunately, this misconception is difficult to erase, even though it has been demonstrated that coastal fisheries which depend on the wellbeing of mangroves provide greater revenues than mangrove forestry products (Ruitenbeek 1991). Considering the ecological and economic value of Indonesian mangroves, it is useful to view current uses of mangrove products and amenities in terms of sustainable and non-sustainable (i.e., elimination) practices (table 19.28). In addition, the various benefits provided by the mangroves can be direct or indirect (tables 19.29, 19.30 and 19.31).
Table 19.26. Some worldwide economic values of mangrove ecosystems.
Table 19.27. Wood quality of various Indonesian mangrove species for fuel. Range of classes: Class 1 is excellent - Class 5 is poor.
Table 19.28. Potential sustainable and non-sustainable uses of mangrove ecosystems from a worldwide perspective.
Economic Considerations. Mangrove management should ideally be based on three options, namely preservation, utilization and conservation. Preservation of the natural state will guarantee that future options remain open until it can be shown that major alteration of the ecosystem is the only option available. This will require cost-benefit analysis. Considering the impressive number of products and amenities provided by many individual mangrove species (table 19.31), this option is a key component of management plans, since future options may include the sustainable use of the ecosystem or converting the system to other uses. Once conversion occurs, all potential benefits are eliminated. Preservation safeguards many of the off-site and on-site, marketed and non-marketed values at a relatively small cost. It should be kept in mind that, initially, this option imposes opportunity costs in the form of lost revenues from development of sustainable or nondestructive mangrove uses or the revenue from total conversion to a use such as shrimp or fish ponds.
Utilization assumes that extraction of goods and services from the mangrove system occurs on a sustainable basis. It is absolutely essential that a multiple-use strategy, through a wide variety of single-purpose activities, is provided within the same area and time frame. It is clear that sustainable use of mangrove resources depends on a sound management strategy, which must be based on sound environmental, ecological and socioeconomic analysis. It must be emphasized that no single use can be maximized without constraints being imposed on the other mangrove uses. To maximize the output value of the managed resource so that users obtain greater benefit, it seems that giving people (i.e., the users) greater access to the mangrove products (goods and services) is essential.
Table 19.29. Direct products and amenities provided by Indonesian mangrove forests.
The conversion of mangroves is too often viewed from a local perspective only, which, in the long run, will have serious consequences on coastal fisheries. Conversion not only destroys the resource itself (i.e., the forest), but impacts on adjacent systems as well. While these secondary effects are difficult to quantify, conversion forecloses all future options for other uses. The loss of all the potential goods and services represents a cost that must be subtracted from the benefits obtained from the conversion, which has seldom been done in practice since it is difficult to measure. Nonetheless, conversion costs are usually higher than preservation or utilization on a sustainable basis. Additional costs of conversion (i.e., destruction) that have to be included relate to the ongoing management costs that may be necessary to counteract many of the biophysical features of the mangrove ecosystem.
Economic Valuation of Mangroves. Dixon (1989) has pointed out that conventional economic analysis techniques are not appropriate in the economic evaluation of mangrove ecosystems for two reasons: 1) Most of the mangrove resources (goods and services) are difficult to monetize; and 2) Many of these resources occur off-site, that is, they are external to the mangrove ecosystem and thus become economic externalities. The objective of economic valuation of mangrove ecosystems is to include explicitly all of the benefits, as well as the costs of changes or loss of benefits from these changes, and thereby better evaluate alternatives. This has been attempted, to some degree of success, in a Bintuni Bay case study (Ruitenbeek 1991). It is essential that included in the valuation, or economic analysis, of mangrove ecosystems should be the full range of resources (goods and services) produced by the system, and that the area should not be treated in isolation. All proposed projects need to have critical evaluation in terms of what will be gained versus what may be lost by altering the natural processes and properties of the ecosystem. This type of evaluation needs to be based on an accurate physico-chemical, ecological and socioeconomic database.
Table 19.30. Indirect products and amenities obtained from Indonesian mangroves.
Table 19.31. The use of various species of mangroves and associated plants in Southeast Asia, with particular reference to Indonesia.
Dixon (1989) points out that traditional or conventional valuation analysis relies heavily on observed market prices to place value on various goods and services. This approach is not appropriate for mangrove ecosystems, primarily because only a few of the goods and services produced by the ecosystem are usually included in the analysis. For example, a decision on whether to convert a mangrove for aquaculture development that will be based only on the value of lost firewood production may be very different than if the value of fish caught in the coastal waters is included. Ruitenbeek (1991) has demonstrated that traditional uses (fishing, hunting, gathering, etc.) of the vast mangrove resources in Bintuni Bay by the local people account for US$10 million per year. In Bintuni Bay mangrove forests are clearly not wastelands, but rather they are highly productive ecosystems that not only contain an amazing diversity of flora and fauna, but also serve as a life-support system for thousands of coastal people.