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ОглавлениеChapter Two
Seashores
INTRODUCTION
This chapter is concerned with those habitats that lie between the reach of the lowest low and highest high tides.1 Thus all these areas are inundated by the sea at some time. Habitats such as seagrass meadows and coral reefs that are found below the level of the lowest low tide, are discussed in chapter 3.
Sulawesi has proportionately more coastline relative to its land area than any other Indonesian island, because of its long, narrow peninsulas (table 2.1). No point on the mainland is more than 90 km from the sea and most locations are within 50 km. In addition there are over 110 offshore islands each with an area in excess of 1.5 km2 within the administrative areas of the four provinces. Coastal ecosystems are of great economic and ecological importance for fisheries and other commercial activities, and those concerned with development on Sulawesi should, therefore, have a grounding in understanding the components, interactions, and mechanisms of coastal ecosystems to ensure that these resources are managed for sustainable production and benefit.
PHYSICAL CONDITIONS
Tides
The process that largely determines the characteristic features of the seashore is the ebb and flow of the tides. The tides around most of Sulawesi are termed mixed prevailing semi-diurnal. This means that each day two high and two low tides occur and that the successive tides are different in height and duration. Around the southwest peninsula the tides are termed mixed prevailing diurnal. This means that each day only one high and low tide occur and that successive tides are different in height and duration (fig. 2.1). In narrow straits and bays, such as the Gulf of Bone (Anon. 1980a), however, the patterns may become rather more complicated.
Figure 2.1. The forms of a typical mixed, prevailing semidiurnal tide (above), and a typical mixed, prevailing diurnal tide (below) over the period of a month.
After Pethick 1984
Tides are enormous waves with wavelengths of half the circumference of the earth. These 'waves' are primarily the result of the gravitational pull of the moon which acts not only on the water closest to it, but also on the mass of the orbiting earth itself, thereby pulling the earth away from the water on the opposite side.2 This is similar to pulling someone towards you by one arm, and seeing his other arm move away from his body.
The sun also has an effect on tides but although it has 27 million times the mass of the moon, it has less than half of the moon's gravitational pull because it is 389 times as distant. Tides are greatest when the sun, moon and earth are in a straight line (i.e., on days of the full and new moon). These large tides are called 'spring tides'. At the half-moons, when the sun, earth and moon form a right-angled triangle the combined forces are least. These small tides are called 'neap tides' (fig. 2.2). The moon rises about 50 minutes later ever)' day so that successive high tides are 25 minutes later each day.
Figure 2.2. The tidal cycle.
After Pethick 1984
The arc traced by the sun changes throughout the year, being directly above the equator and in a straight line with the moon on the equinoxes: March 21 and September 21. This produces the strongest tide-raising forces. When the sun is directly above the Tropic of Capricorn or Tropic of Cancer (23.5° S and N respectively) on June 21 and December 21—the solstices—the tides are a minimum. Towards the end of the year the sun is closest to the earth and so high tides in this period, particularly around the September equinox, are among the highest of the year. For example, the extreme tides during early October in South Sulawesi each year cause the death of coral exposed to the air, and flooding in the coastal regions.
There are further complications: the moon swings 28° north and south of the equator every month, the distance from the sun to the earth varies through the year, and the gravitational pull of the other planets also has an effect. As a result there are longer cycles of tidal behaviour including the 18-year cycle and the 1,800-year cycle. For example, tides were particularly high in the 1500s and will reach a minimum around the year 2400.
Figure 2.3. General pattern of tidal exposure up a beach.
After Brehaut 1982
The pattern of periodic inundation of the shore leads to a gradient of exposure (fig. 2.3). Thus the beach at the mid-tide level is covered for 50% of the time and exposed for 50%. At the mean highwater of neap tides, the beach is exposed for about 70% of the time. This exposure gradient determines to a large extent the occurrence of different species of animals and plants up a shore.
Surface Currents
Surface currents are relevant to the coastal regions because they carry detritus, animal larvae, etc., from or between coastal areas. During the north-westerly monsoon (approximately November to April) the currents run approximately anti-clockwise around Sulawesi. From May to November no such simple pattern can be discerned. The currents on the Sulawesi side of the Makassar Straits run southwards throughout the year, and there is also a year-long eastward current along the northern coast of North Sulawesi (fig. 2.4).
Figure 2.4. Surface currents.
After Wyrtki 1961
Salinity
As rocks weather chemically and physically, so the salts that are dissolved from them in the rain are carried by rivers, sub-surface and groundwater flows to the sea. The seas have therefore been getting saltier over time, but the rate of increase is extremely slow. The most common salt is sodium chloride.
The average level of salinity in the world's oceans is about 33.5 ppt (parts per thousand) but in coastal regions just after the onset of the wet season, the concentration falls, and the degree of variation differs between areas, being most marked off the shores of seasonal areas. Pools of seawater left on a muddy shore as the tide falls can sometimes increase their salinity to about 50 ppt as a result of evaporation, but this decreases again to 15 ppt after rain. The challenges of living in such an environment are discussed next.
For trees growing in the intertidal zone, the salinity of the tidal water is less important than the salinity of the water within the sediment where the plant roots are found. The salinity in this sediment is often less than sea water because of dilution by freshwater flowing through the soil from the land to the sea. This is an important factor in the management of mangrove forest (p. 192) and in understanding the effects of agricultural and industrial pollutants that may enter into the ground water. Some mangrove trees and other organisms are resistant to certain types of pollution, but the demise of sensitive species may upset the equilibrium of the whole system (Bunt 1980; Saenger et al. 1981).
While high concentrations of sodium and chloride ions are toxic to plants, the osmotic potential of the water is also most important as it influences the ability of a plant's roots to take up the water on which its growth depends. The osmotic pressure depends on the sediment type, being greater in fine than in coarse-grained sediments. Fine-grained sediments are capable of withholding more pure water against gravity due to the small size of the pore spaces, and therefore their osmotic pressure is higher than in coarse sediments. If it is not practicable to measure osmotic potential, then salinity and conductivity are a good second best.
Temperature
Tropical coastal waters usually have a temperature of between 27° and 29°C but can be much warmer in shallow areas. The temperature on the surface of mudflats or rocks can be so high that it is uncomfortable to walk on them in bare feet. Inside a shady mangrove forest, however, the air and soil surface temperature is much more equitable (table 2.2).
Dissolved Oxygen and Nutrients
In general, concentrations of neither dissolved oxygen nor nutrients impose any limits on productivity in coastal environments although the concentrations vary between locations. The greatest concentration of dissolved oxygen in the coastal environment is at the water's edge where wave action constantly agitates the water. The abundance of life in most coastal environments and the general abundance of nutrients in coastal environments (except sandy shores), results in a very high biological oxygen demand and this tends to lower the concentrations of available oxygen. Thus there is a gradient of increasing nutrient concentrations and decreasing oxygen concentrations moving from the water's edge through a mangrove forest. This is a result of dilution in the greater volume of water at sea, and the greater incorporation of nutrients into the sediments in the upper tidal areas where the litter is retained for longer (p. 131) (Davie 1984).
Data from an EoS team
Sediment
It is a matter of debate whether new sediments should be termed soils but they can nevertheless be defined by standard soil classifications. Thus, in the Malangke mangrove forest area, the sediment is primarily a grey hydro-morphic alluvium but towards the terrestrial margin merges into a gley humus reflecting alternating periods of aeration and flooding. These sediments have very low fertility but a high organic content. This was highest (4% -5.8% carbon) in the drier parts of the forest where the vegetation was older and the trees faller, in the foreshore under Sonneratia alba there was much less organic matter (0.5%-2.7%). The sediments are generally acidic and this increases with depth although different regimes occur under different species. Conductivity (which is directly proportional to salinity) at Malangke was highest (5.9-6.4 mhos/cm) under Rhizophore forest somewhat inland; a situation probably related to the fact that the percentage of sand is higher near the foreshore (due to greater wave action) and this does not bind the salt (Anon. 1981a, b).
The grain size of sediments is measured by passing the substrate through a series of sieves and calculating the percentage of the total retained by each sieve. If the grains were identical and perfect spheres then 26% of the volume of the sediment would be pore spaces (i.e., a porosity of 26%), regardless of whether the grains were large or small. In nature, of course, grains are neither spherical nor packed as closely as possible, and in many cases small grains fill the spaces between large grains.
The water content of a beach sediment depends on its grain size and porosity, but not all pore spaces will always be filled with water. When the tide is out, the water table falls faster in coarse-grained sediments than in fine-grained because the average pore size is greater. These coarse sediments therefore have a higher permeability (i.e., are better drained than fine sands or muds [fig. 2.5]). In fine sand or mud beaches the water table may stay at or near the surface, even when the tide is out, due to the massive surface tension resulting from the very large surface area in a finegrained sediment, and to the low permeability.
When the pore spaces remain filled with water the sediment may become thixotropic, or liquid when agitated or subjected to pressure. As the water drains away, external pressures are met by increased resistance and the sediment may become dilatant or solid when agitated or subjected to pressure. This is why sand saturated with water feels soft and sloppy, whereas drier sand, whitens and becomes firm when walked upon. These properties are important to burrowing animals since thixotropic sediments are easily entered but burrows are hard to maintain whereas dilatant sediments are hard to burrow into but the burrows are easily maintained. Certain shorebirds follow the waters edge up and down the beach in order to remain in an optimal feeding zone (p. 149). In general, heavy wave action is associated with steeply sloping beaches and coarse-grained sediments. Whereas shores subjected to little wave action slope gently and are comprised of fine grains.
Figure 2.5. Time taken (minutes) to drain a 50 cm column of water through 10 cm of different sand mixtures. The sand mixture is assessed by the percentage of each sample passing through a 0.28 mm sieve.
After Brafield 1972
Oxygen within the Sediment
Oxygen concentrations are affected by three major factors. First, concentrations drop rapidly with depth. In a fine-grained sediment, oxygen concentration at 2 cm may be only 15% of the saturation concentration and virtually zero at 5 cm, and supersaturated in small surface puddles as a result of photosynthesis by diatom phytoplankton. Second, oxygen concentrations fall with an increase in temperature; for example, an increase in temperature from 25°-30°C reduces saturated dissolved oxygen concentrations by nearly 10%. Third, in coarse-grained sediments, which are relatively well oxygenated when the tide leaves, the concentration can fall rapidly in the first few hours after exposure due to the respiration of the animals within it. Should an oil slick drift onto the shore and settle on the sediment at low tide, oxygen cannot diffuse into the sediment pores with obvious extremely adverse effects on the animals below (Ganning et al. 1984).
Bacteria
As mentioned above, fine-grained sediments have a much larger surface area per unit volume of particles than coarse-grained ones thereby providing more attachment sites for micro-organisms such as diatoms and bacteria. Fine-grained sediments also tend to contain more organic debris and so it is not surprising that chemical processes involving bacteria are more complex and proceed faster in these than in coarse-grained sediments (Brafield 1972).
Only near the surface can the organic matter be broken down by oxidation processes. Below this zone, in an anaerobic environment at a level called the redox (reduction-oxidation) potential discontinuity layer, anaerobic bacteria break down organic matter by fermentation or reduction processes producing alcohols and fatty acids. Sulphate ions are reduced to hydrogen sulphide and much of this is fixed as iron (ferrous) sulphides which gives the sediment below this layer a black or dark grey colour (fig. 2.6).
The boundary of the black layer is found closer to the surface where the sediment is fine-grained and where organic matter content is high (i.e., mudflats in front of mangrove forest). Differences between the features of steep and shallow beaches are shown in figure 2.7.
Adaptations of the Fauna
Organisms in the intertidal area experience cycles of wetting and drying quite unlike those in any other ecosystem. Most animals of marine origin are unable to live in such extreme conditions because they quickly dry out, cannot breathe gaseous oxygen, can feed only on water-borne food, and are bound to the sea for reproduction. Two groups, however, the crabs and gastropod snails, have members which have met the challenges by having exoskeletons of impervious shell to restrict water loss, they are able to breathe gaseous oxygen, feeding on damp organic material or microorganisms, and climb into trees to find food. In addition, by fertilizing eggs internally, they can care for the young in brood pouches, or capsules, rather than having to let them take their chances among the plankton.
Figure 2.6. Physical changes across the black layer.
After Brafield 1978
Figure 2.7. Comparison between steep, coarse-grained beaches (a) and shallow, finegrained beaches (b).
After Brafield 1978
Figure 2.8. Typical limpets, a - Cellana testudinaria, b - Patella exusta, c - Patella pica, d - Cellana radiata.
The primitive gastropods known as top shells or limpets (fig. 2.8) cope with exposure in at least two ways. Some species return to a 'scar' in a rock when the tide falls and the shells grow to match this scar exactly. Others are not restricted to occupying a single home site and instead secrete a mucus sheet between the shell margin and the rock surface to reduce water loss. The effectiveness of their adhesion is soon realized when attempts are made to pry them off rocks. It is water loss, rather than temperature which is the main danger to limpets even though they are more tolerant of desiccation than most animals: they can lose about 80% of their water and still recover when water becomes available. These animals, as well as mussels, and Littomrid3 snails, can also lower their metabolic rate thereby allowing them to survive periods of exposure when the only oxygen available is in the water held within their shells (Brehaut 1982).
Animals and plants can survive short periods at high temperatures which would be lethal over a longer period. This may have a significant effect on the degree of exposure, or distance up a rocky shore, that an animal can endure (Brehaut 1982). In addition, most marine organisms are only able to tolerate very minor variations in salinity because they do not have mechanisms of regulating the salt and water balance of their body fluids except within narrow limits. The crabs and snails cope with this problem in different ways: crabs can regulate the concentration of salt in their body tissue, whereas snails are remarkably tolerant of a wide variation in the concentration of salts in their body fluids.
Figure 2.9. Percentages of total aquatic animal taxa recorded at three types of shore (omitting microscopic forms). Note that crustaceans and gastropod molluscs account for 74% of the total on the mangrove shore. Note that these data are not based on complete lists or on equally exhaustive surveys but they serve to illustrate the major differences.
Data from Berry 1972
The success of crabs and snails in the intertidal zone is illustrated by their predominance in mangrove, rocky and sand/mud environments (fig. 2.9).
MANGROVE FOREST VEGETATION
Mangrove forests would once have fringed much of the coast of Sulawesi (fig. 1.20) but major expanses of mangroves are now found in relatively few locations (fig. 2.10), the remainder having been largely felled and used for timber or fibre or converted into brackish fish and prawn ponds (p. 187). South Sulawesi has more mangrove forest than the other three provinces combined (Darsidi 1982) and small patches can be found along most shallow beaches and river mouths away from centres of human habitation.
Figure 2.10. Present distribution of mangrove forests around Sulawesi (indicated in black).
After Salm and Halim 1984
Composition
Mangrove forests are characteristic of tropical coastlines and have very similar compositions irrespective of climate. Only 19 tree species are commonly encountered in Sulawesi mangrove forest, although there are about 16 species of tree that may be found only occasionally or in the forest closest to dry land (table 2.3). In addition there may be 20 species of orchids and other epiphytes but these are generally rare. Some plants have been reported from only small areas, such as Camptostemon philip-pinense (Bomb.) (fig. 2.11) from Kwandang Bay in Bolaang Mongondow (Steup 1939), but this must in part be due to inadequate collecting. A detailed list of plants found in Philippine mangrove forests (Arroyo 1979) is useful to those working in North Sulawesi. A key to the trees most likely to be encountered in mangrove forest and other coastal vegetation is given in Appendix C.
In addition to higher plants, various algae and bryophytes (mosses and liverworts) are also found. Some of the algae appear to have adaptations for living in brackish conditions and these species can be quite abundant. The algae are greenish, brownish or reddish (Johnson 1979), but are unfortunately rather difficult to identify (Teo and Wee 1983). Bryophytes were found on most of the major species of mangrove trees in Thailand (all of which occur in Sulawesi), but not on all trees present. They comprised of five species of moss and 21 species of leafy liverwort. Rhizophora apiculata bore the most species (23) but R. mucronata only four (Thaithong 1984). This may have been due as much to microclimate differences as to differences between the substrates provided.
After Hickson 1889; Heringa 1920; Steup 1933, 1939; Anon. 1980a; Darneedi and Budiman 1984
Figure 2.11. Camptostemon philippinense an uncommon mangrove tree known from North Sulawesi. Scale bar indicates 1 cm.
After Anon. 1968
Many different plant communities of mangrove trees have been identified in Southeast Asia (Chapman 1977b), many dominated by a single species, but these are not discrete. It may be that given the wide range of micro-environmental conditions occurring, there may be a virtually infinite variety of mangrove forest types. Thus any effort to classify an area of mangrove forest that is being studied as a certain 'type' is probably misguided and ultimately not particularly useful.
Figure 2.12. Fruits of the three species of Sonneratia found in mangrove forests in Sulawesi. Scale bar indicates 1 cm.
After Backer and van Steenis 1951
Mangrove trees are tolerant of saline soils, that is they are halophytes (Walsh 1974), but they are facultative rather than obligate in that they can also grow successfully in freshwater. This is demonstrated by the growth, fruiting and germination of Bruguiera sexangula, B. gymnorrhiza, and Sonneratia caseolaris (fig. 2.12) in the Botanic Gardens in Bogor (Ding Hou 1958). This is typical of many plants that might be regarded as restricted to growing in certain soil conditions. In fact, there are many organisms which exist not where they fare best, their 'fundamental niche', but where they grow most successfully in competition with other species, their 'realized niche'. Mangrove trees can sometimes be seen growing at the sides of rivers in seemingly freshwater conditions but in these cases there is generally a wedge of (heavier) salt water permanently or periodically near the bed of the river which maintains saline conditions for the tree roots. The occurrence of these trees in such locations may also be due to the flooding regime of the river (J. Davie pers. comm.).
Mangrove forests, particularly those that are frequently flooded, differ markedly from dryland forests and from most inland swamp forest in the virtual absence of climbing and understorey plants (Ding Hou 1958). In essence, the only plants that grow in mature mangrove forests are trees whose crowns reach the canopy. The reason for this has yet to be confirmed, but it would seem that regular tidal (rather than seasonal) flooding is the most important factor, rather than a difference in salt tolerance between trees and smaller plants (Janzen 1985; Corlett 1986). Exactly how this flooding acts against the establishment of herbs has yet to be determined. Living in saline conditions is clearly costly in terms of energy, and this is supported by the observation that mangroves were killed after only a single spraying with defoliants in Vietnam, whereas nearby terrestrial trees had to be sprayed several times to achieve the same results (Janzen 1985).
Most trees of the mangrove forest have developed peculiar root systems to allow for gaseous exchange above a water-logged and anoxic soil (Mann 1982) (fig. 2.13). Such 'breathing roots' are known as 'pneumatophores'. The stilt roots of Rhizophora may also be effective in preventing the growth of seedlings too close to a growing tree. These stilt roots are generally unbranched but secondary or tertiary branching can occur due to damage of the primary root tip by scolytid beetles (Docters van Leeuwen 1911) or by boring isopod crustaceans (Ribi 1981, 1982; Whitten et al. 1984) (fig. 2.14).
The roots of Sonneratia and Avicennia are similar in gross structure and consist of a horizontal cable root held in place by anchor roots growing vertically downwards. The pneumatophores grow upwards from the cable roots and, small nutritive roots grow horizontal from these. As mud is deposited on the forest floor, so new nutritive roots are produced higher up the pneumatophores. In Bruguiera the cable root loops in and out of the soil and the exposed 'knee-roots' act as pneumatophores. Ceriops does not have special root adaptations but its bark has many large openings, or lenticels, to assist in gas exchange. If oil drifts into a mangrove forest the lenticels on the exposed parts of the pneumatophores become clogged and this is the primary reason that trees so afflicted will die. The dark oil also causes the water temperature to rise and the concentrations of dissolved oxygen to fall (Mathias 1977; Lugo et al. 1978; Getter et al. 1984). Mangrove trees that survive exhibit signs of chronic stress such as reduced productivity and gradual leaf loss (Lugo et al. 1978; Saenger et al. 1981). These effects can be quite local, however, as is evidence by the relatively small patches of dead mangrove trees around the natural oil seeps on the shore near Kabali, southwest of Luwuk.
The feathery flowers of Sonneratia are superficially similar to those of the Myrtaceae (such as rose apples Eugenia spp., and eucalypts Eucalyptus) and in common with many of those, are pollinated by bats which may fly up to 40 km from their inland roost when Sonneratia is in flower (Start and Marshall 1975). The flowers of Rhizophoraceae have a range of mechanisms by which they effect pollination. For example, the anthers of Bruguiera open explosively when the flowers are visited by sunbirds Nectarinia (in the large flowered such as B. gymnorrhiza), or butterflies and other insects (in the smaller-flowered species such as B. paruiflora) in search of nectar. Ceriops tagal also has explosive anthers, triggered largely by moths. Rhizophora flowers are largely wind-pollinated but bees may also be involved (Ding Hou 1958; Tomlinson et al. 1979). Sunbirds can sometimes be seen visiting Rhizophora trees but this is largely to lick the sweet, sticky exudate from leaf buds or young flowers which have been slightly damaged by insects. Since the sunbirds also eat insects the birds help to reduce the damage to Rhizophora by scale insect Coccidae (Christensen and Wium-Anderson 1977; Primack and Tomlinson 1978; Wium-Anderson and Christensen 1978; Wium-Anderson 1981).
Figure 2.13. Different types of roots in mangrove trees.
Figure 2.14. Branching of Rhizophora mucronata roots caused by small scolytid beetles burrowing into the pith of the root tip.
After Doctors van Leeuwen 1911
Observations of fruiting and flowering of mangrove trees in Australia and Thailand showed that there was activity in every month but that most species flowered during the dry season, and dropped ripe fruits during periods of peak rainfall. This pattern is very similar to that often found in dry lowland forests (p. 366) and is probably related to insect abundance. The production of new leaves was depressed when fruit and flower production were maximal. The time it took for a flower to form a ripe fruit varied both between and within species but was about 1-2 months for Nypa, 2-6 months for Avicennia and about 15 months for Ceriops (Chris-tensen and Wium-Anderson, 1977; Wium-Anderson and Christensen 1978; Wium-Anderson 1981; Duke et al. 1984).
A few species of mangrove trees have evolved an unusual, though not unique, form of reproduction. Generally speaking, fruit develops on a plant and, when it is ripe or fully developed, the fruit or the seed inside it is then dispersed; the seed germinates when, or if, it comes to rest in suitable conditions. In most of the Rhizophoraceae such as Rhizophora and Bruguiera, however, the fruits ripen and then, before leaving the parent tree, the seeds germinate inside the fruit, possibly absorbing food from the tree. The hypocotyl (embryonic root) of the seedling pierces the wall of the fruit and then grows downwards. The cotyledons (first leaves) remain inside the fruit. Eventually, in Rhizophora mucronata for example, the root may reach a length of 45 cm. The seedling then drops off by separating it self from the cotyledon tube, the scar of which forms a ring around the top of the fallen seedling, and the small leaf-bud can be seen above this scar (fig. 2.15). Bruguiera behaves similarly, but the break occurs at the stalk of the fruit. This form of behaviour presumably allows the rapid establishment of the young plant. These types of fruit are described in more detail elsewhere (MacNae 1968).
Figure 2.15. The propagule of Rhizophora mucronata showing the root (often mistaken for part of the fruit) and the top of the seedling that detaches itself from the parent plant.
Zonation
Mangrove tree species tend to grow in zones or belts (figs. 2.16, 2.17 and 2.18). On gently sloping accreting shores (where sediment is being actively deposited), the forest nearest the sea is dominated by Avicennia and Sonneratia, the latter usually growing on deep mud rich in organic matter (Troll and Dragendorf 1931). On firm clay sediment A. marina is more common whereas on softer muds A. alba predominates (Ding Hou 1958). Behind these zones Bruguiera cylindrica can form almost pure stands on firm clays which are only rarely inundated by the tide. Further inland B. cylindrica becomes mixed with Rhizophora apiculata, R. mucronata, B. panriflora and Xylocarpus granatum (the canopy of which can reach 35-40 m). The mangrove forest furthest from the sea is often a pure stand of B. gymnorrhiza. Seedlings and saplings of this species are tolerant of shade but only under larger trees of other species; they are unable to grow under the canopy of their parents. This is presumably due to some chemical interaction. The boundary zone between mangrove forest and inland forest is marked by the occurrence of Lumnitzera racemosa,4 Xylocarpus moluccensis, Intsia bijuga (fig. 2.19), Ficus retusa, rattans, pandans, the stemless palm Nypa fruticans, and the tall spiny-trunked palm Oncosperma tigillaria. Where the mangrove forest has been opened, the most common undergrowth plant is the fern Acrostichum aureurn. Relatively steep-sided creeks, bays and lagoons are generally fringed with Rhizophora trees.
Figure 2.16. Zones of mangrove forest observed in part of Malangke.
After Anon. 1980a
Figure 2.17. Changing abundance of adults (above) and juveniles (below) of four tree species along a transect inland from the seaward edge of mangrove forest at Lainea, Kendari. Vertical bars represent 10 trees or seedlings/10 m2.
After EoS team
Recognizable zones may arise for two different reasons where neighbouring vegetation associations have little or no floristic affinity despite growing in the same environmental conditions (continuous variation), and where neighbouring environmental conditions are different enough to result in sudden changes between vegetation associations (discontinuous variation) (Bunt and Williams 1981). Thus vegetational changes can be continuous, discontinuous, or a combination of both. This is why it is crucial to consider scale before attempting an analysis of mangrove forest and why, in the absence of such consideration, data from isolated transects, even from the same area, are so hard to interpret. Comparisons of transect data from different sites are useful in compiling inventories and in noting similarities, but are not a basis for a discussion of zonation which should be based instead on air photos of, and ground surveys over, parts of a number of forests.
Figure 2.18. Profile diagram through somewhat disturbed mangrove forest at Lapangga, Morowali National Park. Note: the general predominance of R. apiculata and discrete occurrence of the other species.
After Darnaedi and Budiman 1984
The tendency of mangrove forests to occur in distinct zones has been interpreted variously by different authors as a consequence of plant succession, geomorphology, physiological ecology, differential dispersal of propagules and seed predation. Each of these is considered next.
Figure 2.19. Intsia bijuga. Scale bar indicates 1 cm.
After Soewanda (n.d.)
Plant Succession. Plant succession is a classic ecological concept and is defined as being the progressive replacement of one plant community with another of more complex structure (p. 366). Much of the early work on mangrove forests focused on its supposed land-building role and it seemed clear from this that one species colonized an exposed bank of mud and, as conditions changed (such as an increase in the organic debris of the mud), so other species took over. For example the colonization of a new shallow or exposed substrate by Avicennia or Sonneratia trees, such as on the banks of the Rongkong River delta at the north of Bone Bay, produces a network of erect pneumatophores which have three indirect functions:
Figure 2.20. Succession in mangrove forests.
After Chapman 1970 in Walsh 1974
they protect the young trees and germinating seeds from wave damage;
• they entangle floating vegetation which decays and becomes incorporated in the soil; and
• they provide a habitat for burrowing crabs which help to aerate the soil (Chambers 1980).
These changes, and subsequent additional sedimentation, lead to a succession of species or communities of species over a period of time (fig. 2.20). It is clear, however, that the stages of succession are not always consistent and different local environmental conditions and man's impact on those have an influence (Steup 1941; Anon 1980a).
A total of 20 characteristics have been noted for secondary succession in tropical forests (Boudowski 1963). If the characteristics are examined in relation to the succession of mangrove forests, only seven of the characters apply, nine do not, and four are inconclusive. This suggests that attributing the apparent zonation to succession is not the whole story (Snedaker 1982b).
Geomorphological Change. As stated above, early workers on mangrove felt that it was mangroves that 'built land'. However, it is clear from observations in the huge deltas of the Ganges, Indus and Irrawaddy on the coast of the Indian sub-continent, that it is the process of sediment deposition that builds land. It is now generally agreed that mangroves do not have any influence on the initial development of the land forms. Mangroves may accelerate land extension but they do not cause it (Ding Hou 1951).
From a geomorphological perspective, it is the shape, topography and history of the coastal zone that determine the types and distributions of mangrove trees in the resulting habitats. The position of species relative to tidal levels (and thus soil type) is obviously important and the pattern of tidal inundation and drainage has been considered to be the major factor in mangrove zonation (Watson 1928). This idea has been developed to include variation in the salinity of the tidal water and the direction of its flow into and out of the forest (Lugo and Snedaker 1974). Although good correlations exist between salinity and zonation, they are not proofs of direct cause and effect.
Physiological Response to Soil-Water Salinity. If salinity is an actual cause of zonation in mangrove forests it needs to be shown that the plants actually respond through their physiology to salinity gradients and not to a factor such as oxygen levels which, under certain conditions, will fall with increasing salinity. It has already been mentioned that mangrove trees are able to live in freshwater (i.e., they are facultative, not obligate, halo-phytes), but each species probably has a definable optimum range of salinity for its growth. Indeed, it has been found that within each zone the characteristic species had apparently maximized its physiological efficiency and therefore had a higher metabolic rate than any invading species (Lugo et al. 1975). Thus invading species would be at a competitive disadvantage due to their lower metabolic efficiency in that habitat. Similarly, it has been found that each species of the mangrove forest grows best under slightly different conditions such as the amount of water in the mud, the salinity, and the ability of the plant to tolerate shade. This means that the various species are not mingled together in a haphazard way but occur in fairly distinct zones.
Salinity can vary considerably between high and low tides and between seasons (p. 109), and thereby presents a confusing picture to a scientist conducting a short-term study. Thus, to identify the salinity levels to which the different species are optimally adapted requires long-term and detailed measurements to determine long-term averages and ranges of salinity. It is often the case that a species' ecological limits are defined by relatively rare events such as occasional extremely dry years (p. 22) or, in the case of mangroves, high salinity levels in the dry season when there is little freshwater input to the system.
Differential Dispersal of Propagules. The suggestion that differential dispersal of propagules (fruit, etc.) influences zonation of mangroves rests on the idea that the principal propagule characteristics (e.g., size, weight, shape, buoyancy, viability, numbers, means of release and dispersal, and location of source areas) result in differential tidal sorting and therefore deposition. There are as yet few data to support this hypothesis (Rabi-nowitz 1978; Snedaker 1982b).
Seed Predation. Experiments conducted in Australia have shown that about 75% of the propagules of five species of mangrove trees were consumed by predators, primarily grapsid crabs, and there were significant differences among species and between forest types. Rhizophora stylosa was preyed upon the least and Avicennia marina the most. As might have been expected, predation was generally highest where a particular tree did not have neighbouring trees of the same species. Predation rates seem to be associated with chemical composition because A. marine, selected by predators over all the other species, had the highest concentrations of protein and sugars and the lowest concentrations of fibre and tannins. The propagules with the highest tannin content appeared to be preyed upon only by a single, specialist crabs (Smith 1986). These differences will influence the pattern of seedling establishment in a mangrove forest, such that establishment is most likely to occur in areas where seed predators are least likely to occur. In the case of A. marina this may mean establishment in the areas most frequently inundated.
Geomorphology, physiology and seed predation thus appear to be the most relevant forest. The impact of human activities, so ubiquitous in coastal regions, plays a major role in modifying species composition and physical conditions, however, and so should be considered first in any study of zonation.
Biomass and Productivity
'Biomass' is a term for the weight of living material usually expressed as dry weight, in all or part of an organism, population or community. It is commonly expressed as the 'biomass density' or 'biomass per unit area'. Plant biomass5 is the total dry weight of all living plant parts and for convenience is sometimes divided into above-ground plant biomass (leaves, branches, boughs, trunk) and below-ground plant biomass (roots). It appears that no study of mangrove biomass has yet been conducted in Sulawesi but several studies have been conducted in Peninsular Malaysia (Ong et al., 1980a, b; 1985). In one undisturbed forest the biomass was found to be between 122 t/ha and 245 t/ha, but in another, which has been exploited and managed for timber on a sustained basis for 80 years, the biomass of trees was 300 t/ha (Ong et al. 1980b). As is explained below, the higher biomass in managed forest is not unexpected. Above-ground biomass in Australian mangrove forests has been found to correlate with parameters of soil quality such as extractable phosphorus, redox potential, and salinity (Boto et al. 1984).
Biomass is a useful and a relatively easy-to-obtain measure but it gives no indication of the dynamics of an ecosystem. Ecologists are interested in productivity because, if the dry weight of a community can be determined at a moment, and the rate of change in dry weight measured, then the rate of energy flow through an ecosystem can be calculated. Using this information different ecosystems can be compared, and their relative efficiencies of converting solar radiation into organic matter can be calculated.
Plant biomass increases because plants secure carbon dioxide from the atmosphere and convert this into organic matter through the process of photosynthesis. Thus, unlike animals, plants make their own food. The rate at which a plant assimilates organic matter is called the 'gross primary productivity'. This depends on the leaf area exposed, amount of solar radiation, temperature and upon the characteristics of individual plant species (Whitmore 1984). Plants, like all other living organisms, respire and use up a proportion of the organic matter produced through photosynthesis. What is left after respiratory loss is called 'net primary productivity' and the accumulation over a period of time is termed 'net primary production'. Net primary productivity is obviously greatest in a young forest which is growing and it should be remembered that a dense, tall forest with a high biomass does not necessarily have a high net primary productivity. Large trees may have virtually stopped growing. Indeed in an old 'overmature' forest, the death of parts of the trees and attacks by animals and fungi may even reduce the total plant biomass while net primary productivity remains more or less constant. The major aim of silvicultural management in forests of timber plantations is to maximize productivity and so the trees are usually harvested while they are still growing fast and before the net primary productivity begins to decrease too much (fig. 2.21).
One means of assessing net primary production is to measure the rate at which litter is produced. The production of litter appears to be very similar between the sites examined in the Indo-Australian region, being about 7-8 t/ha/yr for leaf litter, and 1-1.2 t/ha/yr for all small litter (mainly leaves, but with twigs, flowers and fruit) (Ong et al. 1985; Woodroffe 1985). The total litter production of mangrove forests in Peninsular Malaysia and Papua New Guinea has been found to be about 14 t/ha/yr (Sasekumar and Loi 1983; Leach and Burgin 1985), which is similar to results obtained in Queensland (Duke et al. 1981), and therefore probably similar to that found in Sulawesi. Interestingly, these figures are similar to or higher than those obtained in lowland forest (p. 365) and support the contention that mangroves grow, reproduce, and die fast (Jimenez et al. 1985), similar to dry lowland forest on young terraces (p. 361).
Figure 2.21. Changes in: a - biomass, b - mean annual increment, c - litter, and d - net productivity in four even-aged stands of Rhizophora apiculata in Peninsular Malaysia. In the forest from which these data were collected, the trees are harvested on a 30-year rotation.
After Ong et al. 1985
Variation in net primary production in mangrove forests in northeast Australia and Papua New Guinea has been ascribed to availability of phosphorus (Boto et al. 1984), which is consistent with the view that nitrogen and phosphorus are limiting in coastal marine environments (Rhyther and Dunstan 1971). The approximate annual accumulation of litter on the mangrove forest floor at Merbok was calculated to be 0.33 t/ha for leaf litter and 1.13 t/ha for total litter. An experiment at the same site revealed that 40%-90% of fallen leaves were lost after 20 days on the forest floor. The major agents in the disappearance were probably crabs which either bury them or eat them, later to be excreted as detritus. The importance of the crabs is seen when they are prevented from reaching the leaves, in which case the time needed for total decomposition was 4-6 months (Ong et al. 1980a).
The detritus becomes rich in nitrogen and phosphorous because of the fungi, bacteria and algae growing on and within it and is therefore an important food source for many 'detritivore' animals such as zooplankton, other small invertebrates, prawns, crabs, and fish. These detritivores are eaten in turn by carnivores which are dependent to varying degrees on these organisms. It is probable that most of the micro- and macro-fauna in the mangroves and surrounding coastal areas are dependent on the productivity of litter from mangrove forests (Ong et al. 1980a, b). A major initiative to study the important issue of transport of material in mangrove estuaries in the Indo-Australian region is currently underway (Ong et al. 1985).
Mangrove forests are highly productive ecosystems but only about 7% of their living leaves are eaten by herbivores (Johnstone 1981), and most of the mangrove forest production enters the energy system as detritus or dead organic matter (fig. 2.22). This detritus plays an extremely important role in the productivity of the mangrove ecosystems as a whole and of other coastal ecosystems (Lugo and Snedaker 1974: Ong et al. 1980a, b; Saenger et al. 1981; Mann 1982). Its importance to offshore ecosystems is not clear (Nixon et al. 1980).
The high productivity of mangroves and the physical structure and shading they provide forms a valuable habitat for many organisms, some of which are of commercial importance. At present the most valuable mangrove-related species in Indonesia are the penaeid prawns. The juvenile stages of several of these prawn species live in mangrove and adjacent vegetation, while the adults offshore (Soegiarto and Polunin 1980).
The influence of mangroves extends far beyond the prawn fisheries (p. 187). For example, carbon from mangrove trees has been found in the tissues of commercially important bivalves such as the cockle Anadara granosa, oyster Crassostrea, shrimps such as Acetes, used in the making of belacan paste, crabs such as Scylla serrata, and many fish (Rodelli et al. 1984) such as mullet Mugil, milk fish Chanos and barramundi or giant perch Lates (MacNae 1968; Moore 1982; Polunin 1983).
Figure 2.22. Major pathways of energy flow in a mangrove-fringed estuary.
After Saenger et al. 1981
OTHER COASTAL VEGETATION
There are three main types of beach vegetation: the pes-caprae formation, the Barringtonia formation and the vegetation of rocky shores. The removal through development of the vegetation on a sandy beach may not be regarded as a particularly serious loss in itself, but its ability to hold together a loose sandy substrate means that in its absence more or less continuous coastal erosion occurs. This, and its resultant impact on human settlements is most damaging during severe storms, because the power of the wind and waves is no longer countered by deep-rooted vegetation.
Pes-caprae Formation
The pes-caprae formation is found along sandy beaches which are actively accreting; that is, where sand is being deposed, or on already-developed beaches that are now being eroded. Its name is derived from the conspicuous, purple-flowered creeper with two-lobed leaves, Ipomoea pes-caprae (Conv.).6 The other plants found in this formation also tend to be low, sand-binding herbs, grasses and sedges whose long, deep-rooting stems or stolons spread across or just under the surface of the sand.7 The herbs include the small legume Canavalia, the herb Euphorbia atoto (Euph.), the sedge Cyperus pendunculatum (Cype.) and various grasses. Full lists are given elsewhere (van Steenis 1957; Wong 1978; Soegiarto and Polunin 1980; Whitmore 1984). Most of the species are confined to this habitat type and many are pantropical in their distribution.
The actual composition of the vegetation depends to some extent on the type of sand. There are two main forms on Sulawesi beaches: black, andesitic (volcanic) particles found in the north, and white, calcareous sand from the erosion of coral reefs as found in the southern part of Sulawesi and most of the offshore islands. The black beaches of Minahasa have a poor beach flora probably because the black surfaces absorb more heat and become extremely hot.
Plants are dependent on non-saline soil water but are tolerant of the periodic droughts, salt spray, almost constant winds, low levels of soil nutrients, and high temperatures found in the habitat. The plants also typically have small seeds which are dispersed by water, some even having air sacks around the seeds to assist floating.
The green mat formed by the pes-caprae formation traps leaves and other organic material blown by the wind or tossed up by waves at high tides. Small animals can also take refuge there. As a result, soil conditions improve, nutrients increase and plant succession proceeds (table 2.4).
One of the first large plants to be seen at the landward edge of the pes-caprae formation is the she-oak Casuarina equisitifolia (Casu.), which frequently forms pure stands at the top of the beach. She-oak seedlings are intolerant of shade, but even in open conditions, if there is a carpet of she-oak twigs and litter, the seedlings will not grow. This may indicate the presence of some chemical or allelopathic prevention of regrowth, but this has yet to be proven. Thus, unless the shoreline advances, the belt of she-oak will be replaced by other species.
Barringtotiia Formation
The Barringtonia formation is found behind the pes-caprae formation on sandy soils. It is also found behind on abrading coasts, where sand is either being removed by unhindered ocean waves or where sand has at least ceased to accumulate; in such areas a beach wall about 0.5-1 m tall can be found and the formation is found inland of this. The plants are generally tolerant of salt spray, nutrient-deficient soil and seasonal drought and grow in a belt along the coast, usually between 25 m and 50 m wide, where the lie of the land allows it. The belt will be much narrower where the coast is steep and rocky. Large trees sometimes sprawl across the upper parts of the beach, and as the beach wall is eroded away these eventually fall over, die and become shelters for many small seashore animals.
The larger trees of the Barringtonia association are of three species: Barringtonia asiatica (Lecy.) which has huge 15 cm wide feathery flowers and unusual-shaped fruit (fig. 2.23), Calophyllum inophyllum (Gutt.) which has transparent yellow sap and round fruit of 3 cm diameter, and Terminalia catappa (Comb.) whose large leaves turn red before falling and whose boughs stand out at right-angles to the trunk in a manner similar to kapok trees Ceiba pentandra (Bomb.). Barringtonia itself is not invariably present in the formation which bears its name (van Steenis 1957) and it is sometimes found on sandy ground away from the coast. As with the pes-caprae formation, the plants found in this type of beach vegetation are found in similar locations throughout the Indo-Pacific region and some are typical of sandy shores throughout the tropics. Many of the species are not found outside these formations. In addition to the trees mentioned above, other typical species include the coconut palm Cocos nucifera, the large bush Ardisia elliptica (Myrs.) with its pink young twigs and leaves, Heritiera littoralis with its peculiar boat-shaped floating fruit (fig. 2.23), and other trees such as Excoecaria agallocha (Euph.) with sticky, white sap which may cause temporary blindness (Burkill 1966), pandans Pandanus, the white-flowered and large-leafed Scaevola taccada (Good.) the fruits of which are dispersed by birds (Leenhouts 1957), and two types of hibiscus Hibiscus tiliaceus (Malv.) and Thespesia populnea (Malv.) (van Steenis 1957). Both hibiscus have large, yellow flowers with purple bases, but H. tiliaceus has slightly hairy lower-leaf surfaces, heart-shaped leaves which are as long as they are broad, black-coloured longitudinal glands on the leaf undersur-face near the base, flowers which fall off as soon as they have dried, and smaller fruit. T. populnea has smooth leaves, longer than they are broad with a sharper tip, no black glands on the base of the leaf undersurface, flowers which remain on the plant for some days after they have died and larger fruit (fig. 2.24). Hibiscus tiliaceus is commonly planted in towns and villages.
After L. Clayton pers. comm.
Figure 2.23. Fruits of Barringtonia asiatica (left) and Heritiera littoralis (right). Scale bars indicate 1 cm.
The Calophyllum trees near the mouth of the Lariang River in northern South Sulawesi bear the epiphyte8 Myrmecodia (Witkamp 1940). Myrmecodia and certain other epiphytes are able to grow where there is insufficient organic debris for most epiphytes. This is because Myrmecodia shelters ants within chambers in its swollen stem, and these ants deposit organic matter in the chambers (p. 465). The cycad Cycas rumphii is also sometimes found in the Barringtonia formation. Despite their appearance, cycads are not palms, neither are they ferns, but they are related to the now-extinct seed-ferns that flourished between 280 and 180 million years ago. In addition to the species above, certain species from the pes-caprae association can also be found, particularly near the beach wall.
Figure 2.24. Leaves and fruit of Hibiscus tiliaceus (left) and Thespesia populnea (right). Scale bars indicate 1 cm.
The vegetation on small islands used by seabirds as nesting sites has a peculiar composition, although such islands as Sangisangian (p. 160) have not been investigated in this (or any other) regard. Here the normally basic reaction of the calcareous soil is changed because of the large quantity of uric acid and high phosphate levels in the birds' faeces although the soil pH is about 6.5-8.5 depending on the organic matter content. One tree Pisonia grandis9 with opposite leaves and reddish veins, is confined to such islands and can dominate the vegetation. Islands which lose their populations of seabirds eventually also lose this tree, whose fruit is dispersed by birds, and the more usual Barringtonia formation species take over (Stemmerik 1964). The status of bird islands is discussed below (p. 159).
Rocky Shores
Rocky shores occur where hard, resistant rock faces the sea in such a manner that the products of rock weathering by the waves are swept out to sea rather than deposited to form a beach. Such shores are usually steep with the rocky face often continuing down below the sea surface. There is, however, occasionally a narrow coarse sand or shingle beach. Such steep coasts and cliffs are usually formed of old limestone (e.g., Kaloatoa Island) or volcanic rock (e.g., Lembeh Island).
The vegetation clinging to the upper rock face, above the level of extreme high tides but still affected by sea spray, is similar to that found in the Barringtonia formation.
FAUNA OF SEDIMENT BEACHES
Open Area Communities
Most animals of sediment beaches rarely emerge on the surface and these are known collectively as the 'infauna'. Those that spend some time on the surface such as crabs and snails10 are known as the 'epifauna'. Most of the epifauna are large (macrofauna) but the infauna can be grouped into the microfauna or protozoans, the meiofauna (defined as animals able to pass through a 0.6 mm mesh sieve but retained by a 0.05 mm mesh sieve11), and the large, conspicuous macrofauna such as bivalve molluscs or large worms. These are all resident animals although their larvae may have originated elsewhere. Beaches also receive visitors such as shorebirds (p. 144) and turtles (p. 151).
The meiofauna, being too small to move the grains, generally comprises elongate creatures able to wriggle between the grains. Among the most common animals are nematode worms of which hundreds of thousands may occupy a single square metre of beach. These worms are an important food source for larger animals. A new species of Collembola (p. 48) was recently found in the sandy beach near Tangkoko-Batuangus Reserve, Minahasa (Greenslade and Deharveng 1986). The worms and most other members of the meiofauna are most common in fine sediments since coarse sands dry out too quickly and very fine sands are too easily deoxy-genated. The meiofaunal infauna is less rich in sediments comprising a mixture of grain sizes, probably because the weak waves which result in such sediments are incompatible with the animals in some way.
Figure 2.25. Polychaete worm burrowing into sediment. The anterior segments act alternately as a terminal anchor while the longitudinal muscles contract and the middle segments are pulled in (left), and as a penetration anchor as the circular muscles are contracted and the segments of the head are pushed further in (right).
After Trueman 1975
The ability to burrow is crucial to beach animals in order to avoid excessive wave action, surface predators, high temperatures and desiccation. Soft-bodied animals such as bivalve molluscs and polychaete worms pump their way through sediments (fig. 2.25).
The beach ecosystems are unusual in that the common plant-herbivore-predator structure of food chains is absent. The only 'plants' available are diatoms and bacteria, and predation on or in the sediment is difficult. Predators are found primarily among the epifauna-birds, certain mudskippers, polychaete worms, and snails. Thus the majority of animals either filter plankton from the seawater (suspension feeders) or suck organic deposits and micro-organisms off the sediment surface or sort out edible particles after ingesting sediment (deposit feeders), although the distinction between these is not always clear. The amount of organic material on or in the sediment is generally greater in the finer sediments for these contain higher concentrations of organic carbon and nitrogen (protein in bacteria) (p. 113), and so deposit feeders flourish here. Suspension feeders are more common lower down the beach because they are covered by water for longer and so able to feed for longer.
All these animals have an affect on the environment within which they live. Burrows increase the depth to which oxygen can penetrate and the digging of them brings lower sediments to the surface; suspension feeders deposit faecal pellets on the sediment surface which become a food source for deposit feeders; the action of deposit feeders can resuspend deposits in the sea water. These suspended particles can, however, clog up the filters of suspension feeders so deposit feeders often predominate in very fine sediments while suspension feeders predominate in coarser sediments (Brafield 1978).
Animals living in finer sediments may, when the tide is out, experience oxygen deficiency. Those with burrows opening into surface pools will have few problems, and nor will those that can utilize atmospheric oxygen. Most, however, have to rely on oxygen in the pore spaces which is at low concentrations at the best of times (p. 113). Some animals reduce their metabolic rate below normal levels at low tide, some create currents of water past their gills or body by waving cilia or fine hairs, whereas others move towards the surface as soon as oxygen levels fall below a threshold. Others are able to withstand low oxygen concentration because of the structure of their respiratory pigments, such as haemoglobin, in their body fluids which have exceptional affinity for oxygen. Some, such as fiddler crabs Uca, have no problems at low tide and are able to respire anaerobically for short periods when the sea is covering the sediment and the crabs are in their burrows.
The sediment on a shallow sloping beach can be extremely soft, comprising about 75% very fine sand with the remainder being even finer particles. The area below the mean low water level of neap tides is covered by every tide of the year and never left exposed for many hours. The fauna here is marine with certain crab species, bivalve and gastropod (snail) molluscs12 such as Telescopium telescopium (fig. 2.26), and two or three species of polychaete worms predominating. A variety of mudskippers13— an unusual group of fish capable of living out of water for a short periods—occur commonly along the water's edge and in burrows in the mud (MacNae 1968).
Underwater, mudskippers breathe just like other fishes, but in air they obtain oxygen by holding water and air in their gill chambers. This water to be renewed about every 5-6 minutes (Burhanuddin 1980). The oxygen they obtain in this way is supplemented by gas exchange through their skin and fins (Stebbins and Kalk 1961). On land, mudskippers move in a variety of ways: they themselves forward on their pectoral fins which move in synchrony with each other (i.e., not true walking) leaving characteristic tracks in the mud, they skip over the mud by flicking their tails, and they climb on vegetation using their pectoral and pelvic fins.
Figure 2.26. Telescopium telescopium.
Although they look very similar, the different species of mudskipper have very different diets; some such as Boleophthalmus boddarti take mud into their mouths, retain algal material, and blow out the rest; some are omnivorous, eating small crustaceans as well as some plant material; and others such as Periophthalmus hoelreuteri are voracious carnivores feeding on crabs, insects, snails and even other mudskippers (Burhanuddin and Martosewojo 1978; Mcintosh 1979; Martosewojo et al. 1982).
Most mudskippers occupy deep burrows and some species have burrows with turretted tops (fig. 2.47). All their activities centre on these burrows which are entered briefly throughout the day to moisten the skin and to replace water in the gill pouches. They are usually evenly spaced on the mud thereby reducing the likelihood of conflicts (Stebbins and Kalk 1961), but fights within and between and species are avoided by complex behavioural mechanisms (MacNae 1968). Males dig the burrows and make courtship displays to nearby females by jumping, and by erecting their dorsal fin in the hope of being chosen as a mate. After pairing, eggs are laid on the sides of the burrow which is then defended by the male. Territorial defence is rare outside the breeding season (Nursall 1981; Hutomo and Naamin 1982).
The other main representatives of the epifauna are fiddler crabs Uca which can be observed by waiting patiently on the beach. Population densities of the often colourful crabs can reach 50 per m2. Male fiddler crabs have one huge claw which is useless for feeding because it cannot reach the mouth, and they therefore have to pick organic deposits off the sediment surface at half the rate of the females which have two normal-sized claws. Presumably the males have to eat for twice as long. The large claw is used for warning away males and for attracting females.
Males compete with other males for females rather than for breeding sites because food resources are so rich and potential sites so abundant. Mating occurs near the burrow defended by the female, but the male-female association is very brief. Preliminary observations suggest that large and small, resident and non-resident males all have the same likelihood of breeding, but smaller males produce fewer viable larvae. Since food resources are not limiting and do not have to be defended, promiscuity is possible (Christy and Salmon 1984).
On coarser-grained beaches near the high water level, burrows about 8 cm across can be found with small piles of sand around them. Their occupants are adult, beige-coloured sand crabs Ocypode (fig. 2.27) which are rarely seen during the day. It is extremely difficult to dig these crabs out of their burrows or to catch them as they run across the sand. Young Ocypode are very numerous, and can be seen on the sand surface both by day and night. Ocypode feed mainly on organic material in the sand, but are sometimes predatory on small crustaceans.
On wider beaches the small ghost crabs Dotilla may occur in thousands with densities of over 100/m2 (Mclntyre 1968; Hails and Yaziz 1982). Although some of the larger individuals are coloured light blue with pinkish legs, the majority are sand-coloured. As the tide rises and covers the beach, each ghost crab builds a shelter of wet sand pellets over its back. Air becomes trapped beneath the crab, and as it burrows down so the air pocket is carried down with it. The crabs emerge as the tide falls, and they are followed by a stream of small bubbles.
Isopod crustaceans can be found by careful examination of the sand and the organic material washed ashore onto the upper shore, and wading birds can sometimes be seen feeding on these and other small animals.
Lower down the beach a variety of molluscs occur but are rarely seen because they burrow beneath the surface. Examples of the bivalves are the white and pinkish Tellina, the large Pinna, and the economically important edible cockle Anadara granosa. This bivalve mollusc spawns seasonally, and breeding seems to be triggered by a drop in water salinity at the start of the wet season. Since plankton and algae on mud always seem to be available, the reason for synchronous breeding is probably to ensure maximum fertilization of the eggs, and to reduce the chance of any one larva being eaten by swamping the potential predators (Broom 1982).
Shorebirds
In addition to four species of resident shorebirds, at least 34 migratory species visit Sulawesi's coasts twice each year. They can be seen between February and April and between September and November, on their way to and from their breeding grounds in northeastern and eastern Asia and their wintering grounds, possibly in northwestern Australia (White 1975). One species, the Australian courser Stiltia isabella, migrates from the south between February and April, and returns between September and November (table 2.5; fig. 2.28). These birds would most often be encountered on muddy rather than sandy shores (fig. 2.29).
Figure 2.27. An Ocypode crab, a common member of the beach epifauna.
Very little is known about the movements of these birds within Indonesia and the basic questions posed thirty years ago have barely begun to be answered. That is: What are the normal migration routes? How many birds are there (Coomans de Ruiter 1954)? EoS teams had the opportunity to work with an ornithologist from Interwader, an international shore-bird study programme, during the first part of 1986, and two areas of mudflat were visited: the north of Bone Bay, and the coast north and south of Watampone. The northern site had extensive mangroves but the mud was rather sandy and, therefore, not especially suitable for waders. One exception was the muddy estuary of the Balease River where at least 18 species were seen, four of which constituted about half of the total number of birds seen. The coasts around Watampone were found to have less sand than in the north, and the shorebirds were consequently more common though of fewer species (Uttley 1986).
* Indicates resident species
White and Bruce 1986
Figure 2.28. Some waders that visit Sulawesi shores, a - broad-billed sandpiper Limicola falcinellus; b - grey-tailed tattler Tringa breviceps; c - rufous-necked stint Calidris ruficollis.
After Beadle 1985
Figure 2.29. Areas of mudflats, the habitat most often visited by shorebirds (indicated in black).
After Salm and Halim 1984
From the above it is clear that the physical composition of the sediment influences the numbers of shorebirds feeding upon it, but within a suitable area of mud it is still not known precisely what attracts birds to one part of a beach and not to another. There are clues, however. Small Ocypode crabs, prawns, fish larvae, polychaete worms and small bivalves are among the most important foods for shorebirds and the distribution of these foods between beaches is very uneven. Differences in the fauna in mudflats can really only be determined by direct investigation (Swennen and Marteijn 1985). Where suitable prey is present, density is the most important factor, followed by prey size, prey depth and the penetrability of the substrate (Myers et al. 1980).
Tidal state, wind and disturbance all affect the density and availability of prey, and this is why certain beaches are only used by the waders at certain times (Evans 1976; Grant 1984). Casts of mud thrown up by suspension feeders and swimming movements of small crustaceans are visual clues for the birds, showing them where to feed (Pienkowski 1983), but some birds use tactile rather visual clues and have sensitive beak tips which can sense prey underground. Sandpipers, one group of partially tactile feeders, may avoid sandy mud because the sand grains are very similar in size to the polychaete and oligochaete worms upon which they feed (0.5-1 mm) (Quammen 1982).
The penetrability of a beach sediment depends on its water content (p. 111). This may be the reason that some shorebirds can be seen running along the water's edge on the ebbing tide pushing their bills into the thixotropic (fluid) sand. A careful examination of bill marks made in tidally formed sand ripples by dowitchers, a wading bird similar to godwits, showed that more marks were found on the crests than in the water-logged troughs. Neither the distribution of prey nor sediment grain size showed any difference between crests and troughs, but penetrating the crests required only 50%-70% of the force required to penetrate the troughs. Thus, concentrating effort on the crests reduced energy expenditure. Ripple crests are sites of active sediment transport and the arrangement of the grains is relatively unstable. This larger volume of pore space allows a higher water content and offers less resistance to penetration. Although the differences in water content between crest and trough are small, minor differences in pore volume can produce major changes in the reaction of sand grains to a shearing force (Grant 1984).
Wading birds are often seen in mixed-species flocks which might be thought to be disadvantageous to the individuals by virtue of increased competition. In fact, more often than not, the birds are taking different foods and being together has the advantage that the more birds present the more likely it is that a predator, such as a bird of prey, will be seen. One particular species is usually first to settle on a certain stretch of beach having used visual clues to make its choice. Other species follow when it is clear that food is being found. A few species act as pirates taking food away from the other species. This is disadvantageous in that the birds which lose food have to spend more time feeding to compensate for the loss, but there are advantages in that feeding birds have their heads down searching for food whereas the pirate generally keeps its head up and serves an early warning of the approach of predators (Barnard and Thompson 1985).
In addition to the waders, other common large birds of the coast include the white-bellied sea eagle Haliaeetus leucogaster, the osprey Pandion halietus and Brahminy kite Haliastur indus all of which fish in the shallow waters and scavenge food along undisturbed beaches. There also various storks, herons, egrets and ducks seen around the shore and roosting and nesting in mangrove forest (fig. 2.30). Palopo Bay and the delta of the Cenrana River are good sites for seeing these birds (Uttley 1986). The milky stork Ibis cinereus is of particular interest because until a few years ago it was thought to be quite rare. Large numbers have now been found in Sumatra (Silvius et al. 1985) and they have also been observed, some in breeding plumage, in the Tiworo Straits between Muna Island and the mainland of Southeast Sulawesi (L. Clayton pers. comm.), near Ujung Pandang and in the Cenrana River delta (Uttley 1986).
Figure 2.30. Large birds seen feeding in or near mangrove forests, a - woolly-necked stork Cicortia episcopus; b - little egret Egretta garzetta; c - Chinese egret E. eulophotes; d - plumed egret E. intermedia; e - great egret E. alba; f - milky stork Ibis cinereus; g - grey heron Ardea sumatrana.
After King et al. 1975
Figure 2.31. Yellow-bellied sea snake Pelamis platurus.
After Tweedie 1983
Such fish-eating birds might occasionally encounter venomous sea snakes (p. 232) in the shallow waters of mudflats. One species, the yellow-bellied sea snake Pelamis platurus (fig. 2.31), is the most widely distributed species of snake, being found from south Siberia to Tasmania, and from the west coast of America to the Indian Ocean. It is about 1 m long and is often found near the water surface and eats mainly rabbitfish and mulletlike fish (Voris and Voris 1983). Young, hand-reared egrets and herons were presented with live and dead, poisonous and non-poisonous snakes, with and without their tails. The tails of sea snakes are very distinctive. The birds were most frightened by the yellow-bellied sea snake, even if its tail had been removed. This indicates a genetically-based response; they could not have learned that the snake was dangerous from experience (Caldwell and Rubinoff 1983).
Turtles
The sandy beaches of Sulawesi are used as nesting sites by four species of sea turtle which differ in size and in the shape of the carapace (fig. 2.32):
• green turtle Chelonia mydas which has an olive-brown carapace about 1 m long, can weigh 100 kg and feeds mainly on seagrass in shallow seas (p. 201);
• hawksbill turtle Eretochelys imbricata which has a dark-brown carapace about 90 cm long, weight up to 80 kg and feeds on invertebrates on coral reefs;
• loggerhead turtle Caretta caretta which has a brown carapace about 1 m long, a weight of about 100 kg and feeds on crustaceans and molluscs; and
• the enormous leatherback turtle Dermochelys coriacea which has a dark brown, ridged carapace up to 2.5 m long and can weigh up to a ton; perhaps surprisingly, this species feeds solely on jellyfish. It is a strong swimmer and can maintain a body temperature 18°C above the sea water temperature. Individuals migrate over large distances, in excess of 3,000 km, and although generally found in the tropics, they are have been found feeding inside the Arctic Circle.
Figure 2.32. The four species of turtle found around the coasts of Sulawesi, a - green turtle Chelonia mydas; b - hawksbill turtle Eretochelys imbricata; c - leatherback turtle Dermochelys coriacea; and d - loggerhead turtle Caretta caretta.
From Anon. 1979
The green turtle is more or less absent as a nesting species in South Sulawesi except on the remote Taka Bone Rate Atoll and the Sembilan Islands near Watampone (fig. 2.33; table 2.6). This may be the result of overhunting or overexploitation of eggs but the fact that the hawksbill turtle is present on the small islands in this province and the green turtle common in the other provinces, hints at an ecological factor being responsible. It has been suggested that hawksbill turtles favour small remote islands, even those with no vegetation, with beaches rather steeper than those favoured by green turtles (Nuitja and Uchida 1983). It is important to determine what factors make a beach acceptable so that human activities can be managed or controlled. A study in Australia found that nesting beaches tended to be protected from prevailing winds and to have sand moisture with a lower salinity than beaches not used for nesting (Johannes and Rimmer 1984). How the turtles detect these differences is not known.
Figure 2.33. Turtle nesting beaches. For key to numbers see table 2.6.
From Salm and Halim 1984
? = requires confirmation
After Salm and Halim 1984
Many turtle research and management programs have involved the taking of newly-laid eggs and hatching them with some form of protection from predators. These eggs have frequently been taken at the start of the laying season when the intensity of predation is greatest. It has been known for some years that the sex of hatchling turtles (and other reptiles, p. 303) is determined by temperature during incubation (Vogt and Bull 1982). The weather can very over the laying season causing the sex ratio of hatchlings to also vary. In the sub-tropics the percentage of females can change from 0% in the cooler, early parts of the season to 80% in the warmest month (Mrosovsky et al. 1984a). Even close to the equator effect is still noticeable and differences can be expected in sex ratio of clutches laid in different environments—in beach vegetation, in open beach with or without inundation by cool seawater during the critical middle third of incubation when sex is determined (Mrosovsky et al. 1984b). Where eggs are hatched under conservation management programs, great care must be taken not to unwittingly distort the sex ratio of the hatchlings.
The overexploitation of turtle eggs and adults for food makes the problem of survival for the turtle population progressively harder because the mass nesting behaviour of turtles is ecologically akin to the gregarious fruiting behaviour of dipterocarps (p. 368). Both act to satiate the appetites of their predators with the result that at least some of their eggs or seeds will get the chance to develop. The smaller the population of turtles, however, the large the proportion of eggs destroyed.
Maleo Birds
The maleo Macrocephalon maleo is a member of a small family of mound builders, or incubator birds (Megapodiidae), which with one exception is confined to eastern Indonesia, New Guinea, Australia, and Polynesia.14 The maleo itself, however, is found only in North, Central and Southeast Sulawesi. It is about the size of a domestic hen, weighing around 1.6 kg (Guillemard 1889), with striking black and rose-white plumage, an erect tail, and a head with a bare, helmeted cranium which may serve to keep the brain cool when it is on hot beaches (Watling 1983). The bill is pale green and red at the base. Maleo are primarily inhabitants of forest, but only lay eggs where the ground is sufficiently hot for incubation—that is, near hot springs (Wiriosoepartho 1979), near volcanic vents, or on sandy beaches. The megapodes and the Egyptian plover Pluvianus aegyptius are the only living birds which do not use the heat of their own bodies for incubation.
Pairs arrive at a nesting area the night before eggs are laid. The following morning, amid much duck-like quacking and turkey-like gobbling, the birds examine holes and make trial digs. When a suitable spot is found, both male and female start digging, throwing earth or sand behind them using their strong legs and claws. The toes are slightly webbed at the base which must help when scratching away loose sand (Wallace 1869). As the hole becomes deeper, so the birds take it in turns to dig and drive away other maleos that venture too close.
This digging can take over three hours, particularly where the sand is loose, after which the female lays her enormous egg, 11 cm long and 240-270 g in weight15 (Guillemard 1889), in the bottom of the pit. Subsequent eggs are laid at approximately 10-day intervals. The refilling takes nearly as long as the digging and is lengthened by the digging of false pits near the real one to divert predators such as monitor lizards and pigs. Against humans who value maleo eggs as a delicacy, however, these precautions are of little use. During the nesting period the maleos seek food such as figs, and fruit of Macaranga (Euph.) and Dracontomelum (Anac.) in the beach forest and roost primarily in Casuarina (Casu.) trees (Wiriosoepartho 1980).
Maleos are communal nesters and on the largest known site at Bakiriang, on the south coast of the north-east peninsula, more than 600 birds nest early in the year with the holes only two or three metres apart. Two hundred of the birds nest on just 1 ha of sand (Wading 1983).
The surface of a sandy beach can become extremely hot, over 50°C and 80°C on white and black sand respectively (MacKinnon 1978), yet just a few centimetres below the surface, the temperature is relatively stable at about 36°C. It seems as if most eggs, on beaches or elsewhere, are laid in positions where the temperature is between 32°C and 38°C (MacKinnon 1978; Wiriosoepartho 1980). The depth of the hole might be thought to be critical, and it has been suggested that the bare head of the maleo is efficient at sensing temperature but, in reality, the exact depth and temperature (within certain limits) are not so critical. Instead it seems that the eggs are laid as deep as possible for protection against predators.
Hatching takes about three months and if the chicks survive the one-or two-day scramble to the surface, for ants are a major predator of chicks in the ground (R. Dekker pers. comm.), they are able to fly away immediately, already having adult plumage. The manner in which they 'explode' from the sand and rush away is probably an adaptation to avoid the attention of predators (Watling 1983). The great size of the egg is related to the need to produce a chick strong enough to struggle up to the surface (Guillemard 1889).
The size of the egg makes it an attractive source of food for humans and maleo nesting beaches have probably been exploited since man first arrived on Sulawesi. Unfortunately, however, over-exploitation has been a common phenomenon: for example, the beach at the Batuputih16 just north of the present Tangkoko-Batuangus Reserve, where Alfred Wallace (p. 59) watched maleo nesting in 1859, was at one time visited by egg collectors in an apparently more or less sustainable manner, but within six years of a settlement being established at Batuputih in 1913, maleos no longer visited the beach (MacKinnon 1978). In 1947 about 10,000 eggs were laid in 2 ha of the Panua Reserve on the coast near Marisa, Gorontalo (fig. 2.34) (Uno 1949), but the present total is less than 10% of this (Anon. 1982a). The total number of breeding hens is between 25% and 67% of the total 40 years ago (Wiriosoepartho 1980).
Figure 2.34. Panua Nature Reserve between Gorontalo and Marisa, showing the maleo nesting site, the large expanse of Rhizophora forest, coastal forest and the two small lakes.
After Wiriosoepartho 1980
Figure 2.35. Differential use of habitats by maleo at Panua to demonstrate the importance of lowland forest to beach-nesting maleo.
Based on Wiriosoepartho 1980
The largest site, at Bakiriang, is only a few kilometres away from a transmigration site. The lowland forest the birds depend on behind the beach is being felled and unless this is protected the demise of this population seems almost certain (fig. 2.35). The Bakiriang site is so special that, until 50 years ago, the raja of Banggai, on Peleng Island 100 km away, determined who should collect the eggs and he received a revenue from the eggs collected. The first 100 eggs were sent to the raja and only after he had approved these could they be consumed by local people. Although the Banggai rajas were notorious pirates and unacceptable in many ways, they were among Indonesia's first resource managers. Now, however, eggs are taken despite legal prohibition and they can be found, wrapped in individual palm-leaf baskets, in the markets of Ujung Pandang and even Jakarta.
Experiments by the head of the Gorontalo Forest Service in the mid-70s showed that maleo eggs could be collected and reburied in a cage so that predation was avoided, and then hatched with significant rates of success (MacKinnon 1978). This was tried again in the Tangkoko-Batuangus Reserve and a hatching rate of 78% was achieved. This technique, together with the control of pig and lizard predators and the clearing of undergrowth to increase the area with a suitably high soil temperature, could make a significant contribution to increasing maleo populations affected by overexploitation where forest areas are sufficient (MacKinnon 1981).
Work is currently being conducted in Bogani Nani Wartabone National Park on the management of an inland population of maleo birds and results are awaited with interest.
Seabirds
The coasts and islands of Sulawesi are visited by at least a dozen species of seabirds which, unlike waders, spend months or even years at sea without returning to land. They tend to nest in large colonies, often on small islands, which are extremely sensitive to disturbance (fig. 2.36; table 2.7). Some islands, like the precipitous Batu Kapal off the northeast coast of Lembeh Island, appear to be roosting rather than nesting sites (Hickson 1889). It is likely that seabirds once nested on or near beaches on the mainland and that human disturbance is the cause of the nesting pattern seen today. Indeed, the seabird populations of Indonesia are experiencing a serious decline in numbers (de Korte 1984).
The habit of nesting in large colonies is disadvantageous because disturbance can have so serious an effect, but it has evolved for at least three important reasons: for ease of pair formation (most seabirds are solitary or live in small groups and range over vast distances when they are not breeding), for defence against predators (there is less risk to one individual of becoming the prey), and for the information shared concerning locations of the abundant food necessary for feeding young birds (Nelson 1980). Fishermen well know the value of these birds since they help to locate schools of tuna and other fish. Indeed, along the north coast of North Sulawesi frigatebirds enjoy a traditional protection because of the service they give (Polunin 1983). Since seabirds are top predators,17 they tend to concentrate some pollutants, the effects of which only become obvious when the levels exceed a certain limit and reproduction is disrupted. Monitoring programs of pollution levels in seabird tissues can thus be extremely valuable in assessing levels of marine pollution.
Seabirds that visit Sulawesi are boobies (Sulidae), frigatebirds (Fregatidae), and terns and noddies (Laridae) (fig. 2.37). Terns can take off easily and consequently can nest directly on the ground. The red-footed booby and frigatebirds, on the other hand, are masters of soaring flight on their long wings and so they need to nest a few metres above the ground in order to take off successfully.
The nutrients which seabirds contribute to the islands on which they nest can be quite considerable. For example, colonies of the white-capped noddy Arums minutus, known in Sulawesi only from the small Sangisangian Island north of Kalaotoa Island in the Flores Sea, deposit in their faeces an average of about 2g dry matter/m2/day. This is equivalent to 1,030, 220, 140 and 50 kg/ha/yr of nitrogen, phosphorus, potassium and magnesium respectively (Allaway and Ashford 1984). It is not surprising, then, that the guano of seabirds is much sought and if the collection is conducted at times of year when the birds are not breeding (the peak breeding season is probably between February and April) and with minimum disturbance, this activity can be sustainable. The rocky rather than sandy substrate of some birds islands, however, together with the high acidity of the guano result in an unfavourable habitat for plants. On Batu Kapal, for example, the only plant found was one young fig tree Ficus nitida (Mora.) (Hickson 1889).
Figure 2.36. Nesting and roosting sites of seabirds around Sulawesi.
After Salm and Halim 1984
| Ss - red-footed booby Sula sula | Sta - little tern Sterna albifrons |
| SI - brown booby S. leucogaste | Stal - bridled tern S. alaetheta |
| Fa - lesser frigatebird Fregata ariel | Stb - lesser crested tern S. bengalensis |
| Fm - great frigatebird F. minor | Sts - black-naped tern S. Sumatrana |
| Fsp - unidentified frigatebird | Stsp - unidentified tern |
| Am - white-capped noddy Anous minutus | (•) - needs confirmation |
| As - brown noddy A. stolidus |
After de Korte 1984; Salm and Halim 1984
Figure 2.37. The most common seabirds found around the coasts of Sulawesi. a - great frigatebird Fregata minor (adult male); b - F. minor (adult female); c - lesser frigatebird F. ariel (adult male); d - F. ariel (adult female); e - brown noddy Anous stolidus; f - bridled tern Sterna alaetheta; g - little tern S. albifrons; h - lesser-crested tern S. bengalensis; i - black-naped tern S. sumatrana; j - brown booby Sula leucogaster. The red-footed booby S. sula can be white or brown but always has bright red feet.
After King et al. 1975
Invertebrates of Mangrove Forest
Just as the composition to the mangrove vegetation varies with distance from the sea, so also does the fauna (MacNae 1968; Berry 1972; Sugondo 1978; Anon. 1980a; Budiman 1985) (table 2.8). A number of somewhat overlapping zones can be recognised and these are described below.
Data collected by an EoS team with Identifications by M. Djajasasmita and A. Budiman
Figure 2.38. Snails of the pioneer zone, a - Fairbankia sp.; b - Syncera brevicula; c - Cerithidea cingulata; d - Salinator burmana; e - Terebralia sulcata.
Pioneer Zone. The pioneer zone is that area where seedlings of Avicennia and Sonneratia grow and which is covered by almost all high tides. The sediment is essentially the same as in the open areas and the fauna is also similar, although fewer strictly marine animals are found. Snails such as Syncera, Salinator and Fairbankia may occur on the wet surface of the sediment (fig. 2.38).
Mudskippers are common and large- and medium-sized fiddler crabs Uca can be very abundant. Various species of polychaete worms, a few bivalve molluscs and the peculiar peanut worm (fig. 2.39) which can store oxygen in its coelomic fluid when the tide is out (Brafield 1978) live permanently in the soil of this zone.
The abundance and type of fauna living on the mangrove trees depends largely on the age of the tree—older ones have denser populations consisting of more species. Littoraria snails (fig. 2.40) occur on almost all the vegetation, sometimes up to 2 m above the soil surface. Some species are generally found on leaves while others are found mainly on bark (Reid 1986). Various authors have also noticed that individuals of a species can be pale coloured in trees and dark on the ground (Sugondo 1978; Anon. 1980a; Cook 1983) presumably as a means of camouflage. Populations of sedentary animals encrust the lower stems of trees as they grow. These animals typically include barnacles with the larger Balanus amphitrite below and the smaller Chthamalus withersii extending higher; oysters, commonly Crassostrea cucullata; and the small black mussels Brachyodontes sp. which are attached to the tree by 'byssus' threads. A total of 15,401 animals, 60% of which were mussels of the genus Brachyodontes, have been found on a single Avicennia tree (Tee 1982). These attached fauna may be eaten off the lower stems by the carnivorous snails Thais and Murex (fig. 2.41) which may move in groups decimating their prey (Broom 1982). Barnacles and mussels sometimes suffer 50% mortality in the first 10 m above the soil surface but the number of dead animals decreases upward, indicating that predation higher up the tree is less (Tee 1982).
Figure 2.39. Peanut worm, Phascolosoma from the pioneer zone of the mangrove forest.
Figure 2.40. Littorina scabra (left) and L. carinifera (right). Scale bar indicates 1 cm.
Around the roots of mangrove trees can sometimes be found a bright green sea anemone which, when disturbed, buries itself very quickly, so that collecting a specimen is a very frustrating task (Hickson 1889).
Two or three species of hermit crab are found in this zone. These crabs have lost the hard protective carapace over the rear part of their bodies and depend for protection on finding empty shells. The combination of security and mobility of the adopted shells is clearly advantageous and hundreds of hermit crabs can sometimes be seen on a beach. Suitable shells are, unfortunately for the crabs, a limited resource and this affects growth and reproduction. It has been found that crabs with roomy shells put their energy into growth and do not reproduce, whereas crabs with tight shells, stop growing and put their energy into reproduction. The scarcity of shells leads to active competition between species of hermit crabs (Bertness 1981a, b).
When water inundates the pioneer zone it is sometimes possible to find the pond skater/water strider Halobates, one of the very few insects that has adapted to the marine environment (fig. 2.42) (Anderson and Polhemus 1976; Cheng 1976).
Eroded Banks. The edge of mangrove forest along a winding estuary is often marked by a nearly vertical bank 1-1.5 m high instead of a sloping pioneer zone. This is caused by currents sweeping away the consolidated sediment and is most obvious on the outer bend of rivers, where the current flows faster than on the inner bend. The bank may be broken in places and mangrove trees at its edge often fall into the sea as the sediment is eroded slowly away. The top of this bank is usually at, or slightly above, the mean high water of neap tides, and may sometimes be left 9-10 days without tidal cover. The sediment of an eroded bank resembles that of the mangrove forest floor behind it, with less fine sand (commonly about 65%) than in the pioneer zone. The bank is burrowed into by various crab species (Berry 1963).
Figure 2.41. Thais (left) and Murex (right), carnivorous snails of the mangrove forest. Scale bars indicate 1 cm.
True Mangrove Forest The fauna of this zone differs in several respects from that in the preceding zones. Most of the ground is very flat and the sediment surface is exposed to the air for an average of 27 days per month. Since the trees provide heavy shade, however, the humidity is very high, and this together with the poor drainage means that the soil rarely dries out. There is also abundant leaf litter and other organic matter so that detritus feeders abound. The soil contains less sand and more of the finer clay and silt particles than in sediment near the water's edge. There is also more organic matter. A total of 15 species of mollusc and 15 species of crustaceans were found in one study around the estuary of the Malili River in the Gulf of Bone, but the study was not exhaustive and it is difficult to compare these results with those of the other sites investigated. For example, two species of ellobid snails were found at Malili, compared with 12 at Way Sekampung in Lampung. The comparative study of these two sites together with one more in Lampung and one at Cilacap did show, however, that generic similarities existed between the snails found at each of the sites, but that in many cases the species were different. Snail species common to all the areas were Littoraria scabra, Cerithidea quadrata, Telescopium telescopium and Neritina violacea (Sabar et al. 1979).
Figure 2.42. Halobates, one of the few insects adapted to the marine environment. Scale bar indicates 1 cm.
After Anderson and Polhemus 1976
About 75% of the fauna of this zone is not found in the other zones (Frith et al. 1976). The fauna is best divided into three groups: tree, ground surface, and burrowing.
Perhaps the most striking change observed in going towards the dry lands is the rapid decrease in encrusting animals on the lower stems and trunks of the trees (fig. 2.43). The remaining tree fauna is mobile, for these animals can to some extent determine their immersion in water. It is largely composed of snails such as species of Littoraria and Nerita (fig. 2.44) which are also found in the pioneer zone. Further back from the sea Cerithidea obtusa and Cassidula are found, and even further inland are species of air-breathing pulmonate snails (fig. 2.45) (Budiman and Dar-naedi 1982). Most of these feed on algae growing on the sediment and move up trees when tides wet the ground, but Littoraria very rarely leaves the tree trunks. All these snails are able to breathe efficiently in air and the pulmonate snails, such as Ellobium, have lungs.
Figure 2.43. Relative abundance of four species of tree-dwelling animals along a transect through mangrove forest near Roraya, Tinanggea, on the south coast of Southeast Sulawesi, a - barnacle Balanus sp.; b - mussel Brachyodontes sp.; c - snail Littoraria 'scabra'; d - barnacle Chthamalus sp.
After L. Clayton pers. comm.
Figure 2.44. Nerita birmanica. Scale bar indicates 1 cm.
The encrusting animals on a tree also show a vertical zonation depending on their tolerance to desiccation. In a case examined in Southeast Sulawesi, the small Chthamalus barnacle appeared to have greater tolerance than the larger Balanus barnacle (fig. 2-46).
The animals seen on the sediment surface comprise mostly crabs that have emerged from their burrows, and snails, although the medium-sized mudskipper Periophthalmus vulgaris can be common. Among the snails, actual distance from the sea seems to matter less than details of ground conditions. In wetter areas such as where drains into small gullies, Syncera brevicula can be more common than anywhere else in the mangrove forest.
Molluscs at the seaward edge of the mangrove forest comprise a mixed sample of gastropods and bivalves. Further back in the mangrove forest, however, carnivorous and filter-feeding molluscs disappear. The vast majority of the molluscs in the true mangrove forest feed by grazing on algae or micro-organisms on the soil surface. Little is known about mollusc reproductive behaviour in mangrove forest but most have internal fertilization of eggs and, unlike many aquatic snails, have eggs which develop directly into tiny snails rather than water-borne larvae.
Figure 2.45. Air-breathing snails of the inland parts of mangrove forest, a -Ellobium auris-judae; b - Pythia pantherina; c - Auriculastra subula; d -Cassidula sulculosa. Scale bar indicates 1 cm.
Nearly all the mangrove crustaceans and worms make burrows which reach down to the water table. Many different types of tunnels are constructed (fig. 2.47) and the elliptical tunnels of the edible crab Scylla serrata may slope down from the bank of a river for as far as 5 m. In general, these burrows serve as: a refuge from predators at the surface, a reservoir of water, a source of organic food, a home for pairing and mating which is defended, and a place for brooding eggs and young, although no single species uses its burrow for all these purposes.
Figure 2.46. Vertical distribution of barnacles on a Rhizophora tree 10 m from the seaward margin of mangrove forest near Roraya, Tinanggea, on the south coast of Southeast Sulawesi, a - Balanus sp.; b - Chthamalus sp.
After L. Clayton pers. comm.
In the landward areas of true mangrove forest, the first signs are seen of an animal which itself is rarely seen, the mud lobster Thalassina anomala (fig. 2.48). This animal builds volcano-like mounds of mud which can reach over a metre high (fig. 2.47), and feeds on mud, digesting the algae, protozoa and other organic particles within it. The burrow below the mound is up to three metres long, extending down below the water table. The entrance leading to the main burrow is generally plugged with layers of earth. The habit of burrowing deeply in generally plugged with layers of earth. The habit of burrowing deeply in anoxic mud, closing itself off in poorly oxygenated air and water suggests that it may have evolved means of anaerobic respiration (Malley 1977).
The bivalve mollusc Geloina (fig. 2.49) lives buried in mud and can occasionally be found in this zone, but is more common in mangrove forests on islands in or near river deltas. Geloina is remarkable in its ability to feed, respire and breed so far from open water and at levels where it is sometimes not covered by tidal seawater for several weeks at a time.
Figure 2.47. Different types of animal burrows in mangrove forest areas. The horizontal line indicates the water table. A - crab Scylla serrata (with transverse section of burrow); B - mud lobster Thalassina anomala; C - crab Uca spp. (burrows may reach water table nearer the low-tide level); D - crab Sesarma spp.; E - peanut worm Phascolosoma; F - large mudskipper Periophthalmodon schlosseri; G - smaller mudskipper Boleophthalmus bodarti; H - pistol prawns Alphaeus spp.; smaller mudskipper Periophthalmus vulgaris.
From Berry 1972
Rivers, Streams and Gullies. The banks and beds of water courses in the mangrove forest have a fauna which is generally distinct from that on the forest floor. For example, many of the forest floor species of polychaete worms and crabs are missing, whereas juvenile fiddler crabs and some snail species are more common. The edible crab Scylla serrata18 occurs in firmer sediment near the larger streams and rivers in the mangrove forest where it is caught in traps (Anon. 1980a).
Terrestrial Margin. Far back from the sea, the soil of the mangrove forest is covered by fewer and fewer tides and suffers longer and longer intervals of exposure. Unlike other types of shore, there is virtually no wave action in mangrove forest to carry seawater higher than the true tidal level, because the wave energy is absorbed by the abundant tree trunks and roots. Thus, animals in the terrestrial margin live on a salt-impregnated soil but are covered by seawater only at irregular and infrequent intervals. Insects, snakes, lizards and other typically terrestrial animals are much more common here than further seaward. Sesarma and some large crabs occur here and in the Nypa palm swamps behind, where a small bivalve mollusc Enigmonia aenigmatica is found in association with the palms (Kartiwinata et al. 1979). The crabs' basic requirement is that their burrows must reach down to the water table. Where there is moving water some snails, such as Fairbankia and Syncera, and the large mudskipper Periophthalmodon schlosseri, may be found.
Figure 2.48. The nocturnal mud lobster Thalassina anomala.
Figure 2.49. The bivalve mollusc Geloina ceylonica.
From Berry 1972
Only one estimate of biomass of aquatic mangrove fauna seems to have been made in the Indo-Malayan Region and that was for tree-dwelling aquatic fauna in four types of mangrove forest (table 2.9). The results show a general reduction of biomass with increasing distance from the sea. It is supposed that the turnover rate (time for one generation to replace another) must be quite rapid because most of the tree-dwelling aquatic fauna are in the lower trophic group (i.e., suspension feeders), none of which have long life spans (Tee 1982).
The biomass of molluscs in an Australian mangrove area was greater on the mudflats and pioneer zone where they tended to be filter-feeders, than in the forest where they were largely deposit-feeders. The crabs were very abundant in the open areas but they had a relatively low biomass. The biomass, density and diversity was highest in Avicennia forest but lower in Rhizophora forest (Wells 1984).
Terrestrial Fauna of Mangrove Forest
Insects, birds and mammals live chiefly in the canopy of mangrove forest. Ground-living animals such as rats, pigs and lizards only venture into the landward edge of mangrove forest for brief forays. Macaques will eat Sonneratia and other fruit and descend to the ground to search for crabs, peanut worms and other suitable food. Flying foxes Pteropus commonly roost in the mangrove canopy and others with feathery-tipped tongues such as the cave fruit bat Eonycteris and long-tongued fruit bat Macroglossus are important for the pollination of Sonneratia. In addition, species of insectivorous bats roost in the forest and different species feed in different microhabitats: over the canopy, just above the canopy, in the open beside the trees, and inside the forest. The composition of the guilds of bats feeding in each microhabitat can to some extent be predicted from their wing morphology and details of this from a study in northwest Australia can be found elsewhere (McKinzie and Rolfe 1986). Prediction of ecology and behaviour from gross and dental morphology can be useful tool for little known species of animal (Clutton-Brock and Harvey 1977; Kay and Hylander 1978).
From Tee 1982
The frog Rana cancrivora is common inland around lakes and other aquatic habitats, but is exceptional among amphibians in being able to live and breed in weakly saline water. The tadpoles are more resistant to salt than the adults and metamorphosis into adults will only occur after considerable dilution of the salty water (MacNae 1968).
Mangroves are inhabited by a variety of reptiles such as the monitor lizard Varanus salvator, the common skink Mabuya multifasciata, and the venomous yellow-ringed catsnake Boiga dendrophila with 40 to 50 narrow yellow rings around its body (fig. 2.50). Most snakes seen in or near mangroves are not in fact sea snakes (Hydrophidae) which live primarily in open water (p. 232). The prey of mangrove snakes comprises primarily small fish (Supriatna 1982). Potentially the largest animal of the mangrove swamps is the estuarine crocodile Crocodylus porosus, but persecution for centuries has reduced its number to a very low level and large specimens (they can exceed 9 m) are extremely rare around Sulawesi (p. 303).
The most conspicuous of the insects are mosquitoes, and the larvae of some species can live in water with a salinity of 13 ppt (MacNae 1977). Species of Aedes mosquitoes have been seen feeding on mudskippers but they are also attracted to human skin (p. 617). Mosquito collections made in an area of coconuts near the mangrove-fringed north coast of Bolaang Mongondow included large numbers of the potential vector of malaria Anopheles subpicta (Hii et al. 1985). Another potential insect hazard is the leaf-weaving ant Oecophylla smaragdina (fig. 2.51) which makes nests by glueing together adjacent leaves while they are still attached to the tree. The making of the nest is extraordinary because the adult ants have no means of producing a sticky secretion to join the leaves of the nest together. The larvae do have appropriate glands, however, and when a leaf is to be added to the nest or a tear repaired, some of the worker ants seize the leaf edges to be joined and hold them in the required position. Other workers enter the nest and collect larvae. These are held near the head in the workers' jaws and moved back and forth between the leaf edges, as they secrete the glue (Sarasin and Sarasin 1905).
Fauna of Beach Forests, Particularly Coconut Crabs
Virtually nothing seems to have been written about the fauna of beach forests, although travellers sometimes report seeing macaques in the trees.
An interesting snail Cochleoslyla leucophtalma has been observed in bushes near the beaches of Sangihe Island. This animal, about 2 cm across with a brown and white shell and an orangey-red body, lies across a leaf and bends its body over so the edges meet. It then starts to glue the edges together with mucus to form a bag. Before finishing, it lays large eggs inside the bag, completes the glueing and then eats a hole in the leaf blade which it covers with a very thin film of mucous. This is supposed to ensure that some air enters the leaf bag (Sarasin and Sarasin 1905).
Figure 2.50. Yellow-ringed catsnake Boiga dendrophila.
After Tweedie 1983
Figure 2.51. Oecophylla smaragdina which sews its leaf nest with larval secretions.
The beach forest animal about which most is know is the coconut crab Birgus latro (fig. 2.52). The most recent major studies of this interesting animal, the world's largest terrestrial arthropod, were conducted in the Marshall Island and the Mariana Island in the western Pacific (Helfman 1977; Amesbury 1980, 1982; Reese 1981), and it is on the results of those that much of the information below is based.
Figure 2.52. Coconut crab Birgus latro.
The coconut crab is a member of the land hermit crab family Coenobit-idae19 but, unlike the other members, it does not occupy a snail shell when adult. It was once widely distributed throughout the western Pacific and eastern Indian Oceans but now is restricted to small islands, particularly those uninhabited by man. In Sulawesi it now known only from Sangihe and the Kawio, Talaud, Togian and Banggai Islands, the Togian Islands being the most westerly part of its range in Indonesia20 (Reyne 1938; Anon. 1982b; Salm and Halim 1984) (fig. 2.53). Man has found the crab to be a desirable food item and it is easily caught even though it may be the largest animal on some of the islands it inhabits. In the Togian Islands, for example, crabs are occasionally collected by residents for their own consumption or for sale to visitors. Much more damaging though are the parties of non-residents from Gorontalo, Ampana and Poso who remove whole boatloads of crabs for sale in their respective towns as food or tourist curios. If this exploitation were regulated under an ecological management plan it could be sustained, but this is not the case (Anon. 1982b).
Most crabs are obliged to seek water for mating, but coconut crabs mate on dry land. The fertilized eggs, totalling tens of thousands, are carried under the crab's abdomen. Females release their eggs into sea water when the tides are highest; that is, around the full moon, and the larvae hatch in response. At this time eggs are most likely to be washed out to the open sea where predation is less and availability of plankton greater than over the reef flat. The larvae spend three to eight weeks as part of the oceanic plankton before the glaucothoe or transitional larva finds a small shell to shelter inside, like a hermit crab, and migrates to land. At this stage it may face severe competition with smaller species of hermit crabs for both shells and food. This larva moults several times and then experiences a metamorphosis to become a miniature adult. When its carapace is only about 2.5 cm across, at about two years of age, it gives up living in shells, a move which brings new opportunities and problems. It is sexually mature when the carapace is only 5 cm across but the largest crabs can weigh 5 kg with a thoracic length21 of 70 mm. Their large-clawed legs can span 90 mm. Females are smaller than males and have a maximum thoracic length of about 50 mm. Estimates of the ages of such large individuals have not been made. This large size would clearly be impossible if they were dependent on living in borrowed shells. They do need to avoid direct sun, however, so they are active primarily at night, although not all those who have studied them agree that they are strictly nocturnal (Harries 1983).
Figure 2.53. Distribution of coconut crab Birgus latro (dark shading). Dotted lines represent coral shoals.
After Salm and Halim 1984
Coconut crabs generally shelter in burrows in the old coral other rocks around the coast or under coconut leaves and pandan roots. These burrows are analogous to the shells they have abandoned. They bring large pieces of food into their shelters and remain there for a few days eating. It is possible that the crabs moult in these burrows to provide protection from anything that might endanger them during this critical time. A newly-moulted crab is largely defenceless and its body is soft and easily damaged.
If a food item is too large to move, a coconut crab will defend it from all other competitors such as other crabs and rats. Apart from coconut and pandan fruits, two of their most common foods, coconut crabs will eat virtually anything organic from moulted crab exoskeletons to other crabs, and decaying wood to unwary birds. In captivity they will readily take lettuce, cabbage and live giant African snails Achatina fulica as well as a wide range of other food (Reyne 1939).
