Chapter Three
ESTUARIES
Estuaries in Sulawesi (fig. 3.1) are not as large or as many in Java, Sumatra and Irian Jaya but they are nevertheless important for fisheries and communication. They are therefore often foci of habitation and are usually the final sampling station for water quality studies of rivers. Estuaries would all, in the absence of man's activities, be fringed by mangroves.
Water Characteristics
Estuaries vary in their physical, chemical and biological properties, being affected by short- and long-term changes in river flow and tides, changing seasons, and occasional extreme weather conditions. These have considerable influence on determining salinity, temperature, nutrient levels and sediment load.
The rate of change from the freshwater riverine environment to a marine environment depends on the interaction of the volume of freshwater flowing to the sea, on friction such as wind and currents, and on tidal mixing. In a highly stratified estuary (fig. 3.2), freshwater flows over a layer of saline water with little mixing. Friction between these two layers, however, generally occurs causing varying degrees of mixing. Highly stratified estuaries are found where river flow is large compared with tidal flow. Where tidal and river flow are more equal, moderate stratification is found, and it is here that salinity increases gradually with depth. Vigorous tidal mixing can lead to a vertically homogeneous estuary in which salinity down a column of water is the same but varies with time according to the tidal state. Such stratification is found only in small estuaries. These patterns can also vary through the year depending on rainfall, and wind strength, and will also be complicated by any sand bars at the entrance to the estuary (Uktolseya 1977).
Figure 3.1. The major estuaries of Sulawesi (circled).
After Salm and Halim 1984
Fauna
Estuarine organisms have to contend with large fluctuations in salinity. This presents physiological challenges because adjustments must be made in the ionic composition of body fluids to ensure that the preferred ionic concentration is maintained in the body tissues. It is the responses and adaptations to changing salinity gradients of an estuary that determines the pattern or zonation of species. Since estuaries represent the transition between freshwater and marine environments, one would expect a change from freshwater to marine organisms along the length of an estuary, and this is indeed the case. Between about 5-8 ppt salinity there is a distinct dearth of species (fig. 3.3) and this may represent the threshold above which ion regulation is not necessary for marine animals but is necessary for freshwater animals (Khlebovich 1968). Not only presence of animals is affected by water salinity, but also the size to which a particular species will grow; for example, the size of certain bivalve molluscs decreases with decreasing salinity (Barnes and Hughes 1982).
Figure 3.2. Three classes of stratification in estuaries.
After Levington 1982
The flow of freshwater out to sea might be expected to sweep organisms away from the estuary, but some members of the zooplankton are adapted to sink to the bottom of the estuary where water movement is least during the ebb tide, and to rise again when the water rises. Phytoplankton have no such adaptation and so there is no distinct estuarine phytoplankton community (Levington 1982). In the freshwater reaches of the Malangke estuaries in the north of Bone Bay, the phytoplankton is dominated by the blue-green alga Anabaena and the diatom Navicula. In the more saline locations, Navicula dominated the samples and Anabaena is more or less absent (Anon. 1980a). There appear to be no other distinct changes.
Some of the larvae of commercially-important prawns and fish, both migratory and resident, may live in estuaries for one or more years because of the high inputs of nutrients (Hadikoesworo 1977; Polunin 1983). The adults may have spawned offshore or among coastal vegetation. The most abundant fish of estuaries are those that have a broad niche, exploiting a wide range of foods and habitats. A total of 36 fish species have been found in estuaries of the Malangke region (table 3.1) some of which have considerable economic importance (Anon. 1980a).
From Anon. 1980a. Ecological information from Carcasson 1977; Schroeder 1980
Figure 3.3. Changes in the number of freshwater, brackish water and marine species in different salinities.
After Barnes 1984a
Figure 3.4. Archer fish Toxotes jaculator shooting a beetle off a leaf with a jet of water.
One of the more curious fishes found in brackish water of estuaries and mangrove creeks is the archer fish Toxotes jaculator (fig. 3.4). It is commonly kept as an aquarium fish because of its stunning ability to shoot jets of water from its mouth to knock insects off over-hanging vegetation. It is accurate up to about a metre and is capable of compensating for the bending or refraction of light as it passes, from air to water as well as allowing for the trajectory of the water it shoots.
Primary Productivity
Estuaries are very productive marine environments with abundant food, low predation pressure and few specifically estuarine species. The nutrients in an estuary originate from three sources: river inputs, marine inputs and bottom sediments, although rivers contain higher concentrations of dissolved and particulate nutrients than sea water. The particulate matter may be deposited on the bottom of the sanctuary becoming a food source for benthic organisms thereby entering the foodweb. A flow of deep-sea water towards the land brings dissolved nutrients into estuaries which can be utilized by phytoplankton. Plankton becomes less abundant with distance from an estuary, and primary productivity can be 20 times as great in an estuary as it is in the open sea (Doty et al. 1963). Concentrations of phosphorus, a key limiting nutrient, can be twice as great. The availability of organic matter in estuarine systems can be particularly high because it is supplemented by adjacent systems. For example, rivers bring down detached plants and freshwater phytoplankton that die on contact with sea water (Hadi et al. 1977), and colloidal matter comprising very fine sediment, aggregates or flocculates in estuaries and then sinks. Mangroves also export nutrients into estuaries (p. 135), where particulate organic material from the decomposition of mangrove forest litter is the primary source of energy for aquatic organisms.
SEAGRASS MEADOWS
Seagrasses
Seagrasses are the marine members of the aquatic plant families Hydrocharitaceae and Potamogetonaceae. In Sulawesi the former family has three genera (Enhalus, Thalassia and Halophila), and the latter four (Halodule, Cymodocea, Syringodium and Thalassodendron), and their identification is relatively easy1 (figs. 3.5-3.8). Seagrasses bind shallow sediments and fast growing pioneer species play an important role in stabilizing land.
Seagrasses are found in shallow coastal waters or in lagoons between coral reefs and the shore. A few species extend into the intertidal or littoral zone and these can tolerate quite high temperatures as might be experienced during the day at spring low tides. In such sites, species with narrow or small leaves tend to be most common (McMillan 1984). Seagrasses generally grow gregariously and the larger ones can be said to form meadows. They often grow in associations of species, and if conditions are suitable for one species, others will probably be close by.
Figure 3.5. Halophila seagrasses. a - H. beccarii, b - H. minor, c - H. ovalis, d - H. decipiens, e - H. spinulosa.
After den Hartog 1957
Figure 3.6. Thalassia and Enhalus seagrasses. a - T. hemprichii (female), b - T. hemprichii (male); c - Enhalus acoroides. Scale bar indicates 1 cm.
After den Hartog 1957
Around northern Minahasa, seagrasses are found on all reef flats and floors of shallow bays with Thalassia hemprichii being the most common and conspicuous. This species frequently grows in association with Halophila ovalis, Halodule urrightii, H. pinifolia and Syringodium isoetifolium. Enhalus acoroides is most commonly found bordering mangroves and lagoons or in bays where the water is warm, still, slightly greenish or turbid with a relatively high organic load. In these conditions the leaf blades of this species can grow to 2 m in length. In very different conditions, on the outer reef flat close to or in the surf zone, Thalassodendron ciliatum is common in pure patches. Pure patches of Halodule uninervis also occur but on firm sand on the lower slope of beaches or between the roots of Sonneratia mangrove trees (p. 120) (Anon. 1981). Around the Tukang Besi Islands and the islands of Taka Bone Rate (p. 217) there are very extensive meadows of Thalassodendron ciliatum that stretch for several kilometres (Brouns 1985). Studies of seagrass distribution at Labuan Peropa (east of Kendari) and at Tanjung Karang (west of Donggala), concluded that the nature of the substrate was the most important factor determining the presence of a species at any particular place, although water depth and exposure clearly played a role. Transects perpendicular and parallel to the beach demonstrated that species composition changed with distance from the shore (fig. 3.9) (L. Clayton pers. comm.).
Figure 3.7. Seagrasses. a - Thalassodendron ciliatum, b - Halodule pinifolia, c - Syringodium isoetifolium, d - H. uninervis. Scale bars indicate 1 cm.
After den Hartog 1970
Figure 3.8. Cymodocea seagrasses. a - C. rotundata, b - C. serrulata. Scale bars indicate 1 cm.
After den Hartog 1970
Almost as important as the seagrasses in terms of biomass and productivity are epiphytic algae found on the seagrasses. These algae vary in species composition and abundance between and within seagrass species, but there are few differences in the dominant species (Heijs 1985).
Reproduction
The reproductive biology of these higher plants is very interesting: Halophila and Thalassia are pollinated under water but Enhalus has flowers which reach the surface where they are pollinated by wind or insects. The flowering of Enhalus is gregarious and coincides, with low spring tides, a few days after the new and full moons. The male flowers are released from the parent plant, float to the surface and, due to their waxy, water-repellent coating, tend to clump together, moving around in response to the wind and currents. The simultaneous release of these small flowers is probably caused by the increase in water temperature around the plants when the tide is extremely low, although dissolved oxygen and salinity concentrations, as well as light intensity also change at such times (den Hartog 1957). The female flowers remain attached to the plant and they also have a waxy, water-repellent coating which attracts the free-floating male flowers by surface tension. Pollination usually occurs when the tide rises: the stem of the female plant reaches its greatest extension and then, when the tide gets higher still the flower can stay above the water no longer, surface tension pulls the edges of the petals together and male flowers are 'caught' between them. The fruits of seagrasses ripen only under the water and dispersal distances are probably short since the seeds are not buoyant and cannot grow in water more than 8-10 m deep presumably because the light intensity is too low. It is, however, possible that the dugong and turtles disperse the seeds after accidentally ingesting ripe fruit heads with seagrass leaves and rhizomes (Janzen 1984). The fruit, which some coastal people eat, bursts open when ripe and the developing embryo breaks out of its very thin seed coat, falls to the sand or mud, and germinates immediately (den Hartog 1957).
Figure 3.9. Patterns of species distribution along a 35 m transect across a seagrass meadow perpendicular to the shore at Tanjung Karang, Donggala.
After L. Clayton pers. comm.
Biomass, Productivity and Decomposition
The biomass of leaves and stems in a seagrass meadow can reach about 700 g dry matter/m2, although most meadows studied by EoS teams had biomass densities of 80-400 g/m2 (L. Clayton pers. comm.). About 25% of this biomass is accounted for by the epiphytic algae (Heijs 1985). The net primary productivity can be very high, and a rate equivalent to 16.4 t/ha/yr has been measured for Thalassodendron ciliatum meadows around one of the islands at Taka Bone Rate. This is higher than the rates for lowland forests (p. 365). There is considerable variation between sites, however, and the different methodologies used in different studies make it rather difficult to compare results. For example, the epiphytic algae can contribute at least 35% of the primary production of the system in locations where the plants are relatively widely spaced (Heijs 1985). Where the plants grow closer, less light penetrates through the seagrass stand and the algae do not thrive.
Seagrass blades contain about 30% ash or mineral matter, 10% protein, 1% fat, 60% carbohydrate and have an energy content of 3 Kcal (Dawes and Lawrence 1983),2 compared with 8%, 8%, 2%, 82% and 18 Kcal respectively for alang-alang grass Imperata cylindrica, which is frequently used when young as a stock food. The main grazers on seagrasses are certain fish, turtles, dugongs and a few sea-urchins with cellulose-digesting bacteria in their guts, but only 5% of the seagrass production is consumed directly, most consumers depending more on decomposing seagrasses. This is probably because the detritus of seagrasses is rich in microorganisms; one dry gram supporting about ten thousand million bacteria, one hundred million flagellates, and one hundred thousand ciliates with a total biomass of about 9 mg.
It is not known how much seagrass material enters off-shore food webs, but it should be borne in mind that the attempts that have been made to measure the export of material are, for practical reasons, usually conducted during relatively calm weather. A single strong storm, however, could tear up and wash away considerable quantities of plants (Barnes and Hughes 1982). In contrast to conventional wisdom concerning the role of seagrass detritus in estuarine food webs, research in the meadows in the Gulf of Mexico has demonstrated that it is the epiphytic algae, not the actual seagrasses, that are the most important component in the ecosystem. These algae are grazed intensively at night by invertebrates. In the same study carbon in the seagrasses and their epiphytes was tracked through the animal community and it was shown that animals were assimilating carbon from epiphytes rather than from seagrasses (Kitting et al. 1984). In the Seribu Islands north of Jakarta, 78 fish species have been found associated with sea-grass meadows (Hutomo and Martosewojo 1977). Molluscs such as the bivalve Pinna, and the gastropod snails Lambis and Strombus (fig. 3.10) sea cucumbers such as the long Synapta and shorter Holothuria (p. 228), and the brown-spotted, sand-coloured sea star Archaster are reported as common in seagrass meadows (Atmadja 1977).
Effects of Development
Agricultural, industrial and domestic effluents discharged into the sea, dredging, heavy boat traffic and other human activities can have detrimental effects on seagrass meadows. Where seagrasses are lost the subsequent changes that can be expected include:
• a reduction of detritus from seagrass leaves with consequent changes in coastal food webs and fish communities;
• a change in the dominant primary producers from benthic to plank-tonic;
• changes in beach morphology due to loss of the sand-binding properties of seagrasses;
• a loss of considerable structural and biological diversity and their replacement with bare sand (Cambridge and McComb 1984).
It may be possible to detect early stress on the meadows by monitoring changes in the communities of epiphytic algae (May et al. 1978), but any change must be judged against the quite considerable long-term changes that occur unrelated to development activities (May 1981).
Figure 3.10. Gastropods of seagrass meadows. Scale bar indicates 1 cm.
It may be possible to detect early stress on the meadows by monitoring changes in the communities of epiphytic algae (May et al. 1978), but any change must be judged against the quite considerable long-term changes that occur unrelated to development activities (May 1981).
In areas where seagrass meadows have been lost through mechanical disturbance, or where a once damaging effluent source has since been removed or purified, it is quite possible to restore the meadows by planting. This has been successful in a number of situations (Thorhaug 1983, 1985; Thorhaug et al. 1985). It would be reasonable to insist upon seagrass restoration if it is found that the construction of the new fishing port at Kendari, intended to become the largest in eastern Indonesia, has a negative impact on nearby meadows.
Dugongs
Dugongs, or sea cows Dugong dugon, are the sole species in the family Dugongidae, and are one of only four living species in the order Sirenia3. The dugong is the world's only vegetarian marine mammal, living in shallow coastal areas in the south-western Pacific and Indian Oceans (Nishi-waki et al. 1979). It is believed that sirenians evolved from an animal that fed in vast seagrass meadows in the west Atlantic and Caribbean during the Eocene Period (54-38 million years ago). This animal was closely related to the ungulates and was descended from an ancestor shared by elephants. Like elephants and horses, dugongs are non-ruminant herbivores4 and consequently have a very long intestine. Bacterial activity in the hind gut assists in the digestion of the large quantities (about 10% of body weight) of the relatively high quality food they consume each day (Murray et al. 1977).
Dugongs grow up to 2.5 m in length, are mid-brown in colour, slow-moving, and have few predators except man who seeks their meat, oil and tusks. Their life span is about 50 years for females and 30 years for males, and sexual maturity is reached between about 9 and 15 years. The gestation period is about one year after which a single calf, one metre long, is born (Marsh 1981). The period between two consecutive births can be 3-7 years (Marsh 1981; Marsh et al. 1984). The calves generally swim above and slightly behind their mother. They are typical K-selected species (p. 345) and have little potential for rapid population increase if hunted too heavily. Under the most favourable conditions the maximum rate of population increase is probably about 5% per year, and so any man-induced mortality must be kept at that level or below if the population is not to decline (p. 335) (Marsh 1986). As a result of being vastly over-hunted dugongs are rare around the coasts of Sulawesi with viable populations being found only in remoter areas (fig. 3.11). Many dugongs are caught accidentally (but fortuitously for the fisherman) in gill nets set for fish, but some are deliberately hunted despite their protected status. A hunter interviewed near the Vesuvius reef southwest of the Banggai Islands reported killing one every ten days (Holdway n.d.), a rate which is surely not sustainable. Dugongs tend to aggregate in herds of about ten animals5 and to have preferred feeding areas (Anderson 1981). The dugong needs and deserves much better protection than it receives at present and it is probably necessary to identify the major populations and their ranges6, to ban gill nets from key areas, and to enforce the prohibition of hunting.
Dugongs are extremely hard to study, partly because the waters above the seagrass meadows they frequent tend to be turbid7, and partly because they are generally shy, fleeing at up to 18 km per hour (Domning 1977), faster than a human can swim. Even so, they are curious when danger is not perceived, approaching and watching divers (but not necessarily behaving normally) until their curiosity is satisfied. Unlike whales, they disturb the water little when surfacing to breathe, something they do about every one or two minutes (Anderson and Birtles 1978; Anderson 1982).
Figure 3.11. Distribution of dugongs around Sulawesi.
After Hendrokusumo et al. 1981; Salm and Halim 1984
Dugongs dig into the sediment when grazing on seagrasses because over half the biomass of the smaller seagrasses, their major food, is in the rhizomes and it is here that carbohydrates are concentrated (Johnstone and Hudson 1981; Marsh 1982). Their main potential competitor, the green turtle Chelonia mydas (p. 151), eats only leaf blades. Dugongs 'chew' their food between the horny pads at the front of their upper and lower jaws.
The differences in proportions of different seagrasses in the dugong diet probably reflect only differences in meadow composition rather than direct selection of certain plants by the dugongs. Seaweeds, or macro-algae, were found in half the stomachs examined in one study but only as a minor item (Marsh 1982).
Useful work can be done on dugong diets by examining either stomachs or residual samples from the mouths of dead animals. The latter technique is easier because the plant remains are relatively intact and can be identified quickly to species (Johnstone and Hudson 1981), whereas the stomach analyses require microscopic analysis of the structure of the masticated vegetable matter. The cell patterns of different seagrass genera are characteristic and so are relatively easy to identify (Channels and Morrissey 1981).
Measurements of metal concentrations in the tissues of dugong from northern Queensland provided several surprises. The livers contained exceptionally high concentrations of iron and zinc, and relatively high concentrations of copper, cadmium, cobalt and silver. Certain metals, particularly iron, increased in concentration with the age of the dugong. It seems unlikely that wastes from man's activities were having an effect on these animals from relatively remote populations and so the chemical composition of seagrasses were examined. These revealed very high concentrations of iron but low levels of copper compared with grasses from pastures. These imbalances in dietary metal intake have significant effects on dugong metabolism (Denton et al. 1980).
Heavy metal and organochlorine concentrations were examined in tissues from two female dugongs caught off Sulawesi for an exhibition in Japan,8 and were found to be very low and undetectable respectively (Miyazaki et al. 1979). These results would have been expected since the dugong is a primary consumer (p. 559) and therefore is unlikely to accumulate pollutants. It is animals in the higher trophic levels that would be expected to accumulate pollutants from their prey.
CORAL REEFS
Importance and Species Richness
Coral reefs are of considerable importance because of their protective role and the value of the larger animals (both alive and dead) associated with the reef. Perhaps the largest coral reef fishery in all Indonesia is found in the shallow sea of the Sangkarang Archipelago within 80 km of Ujung Pandang, and thousands of people depend on this for income and protein. Coral reefs are also extremely valuable to the tourist industry, and North Sulawesi promotes diving reefs as one of its major tourist attractions. Indeed, the Nusantara Diving Centre in Manado was awarded a Kalpataru Environment Award by President Soeharto in 1985 in recognition of its work in bringing the economic role and beauty of coral reefs to the attention of the public and local authorities. It even convinced the port authorities not to allow large ships to pass the straits between Manado and Bunaken Islands where the most spectacular reefs are located. Tourists from Indonesia and many other countries now visit the reefs and find excitement, wonder and fulfillment.
Coral reefs are enormously rich in species (pp. 219 and 221) which interact with each other to form an extremely complex community. In the early days of ecology it used to be believed that complexity of a community, such as the animals and plants of a coral reef, begets stability. It was noted, for example, that crop monocultures were extremely vulnerable to invasion and destruction by pests and diseases and that forests in temperate regions were far more prone to insect outbreaks than forests in tropical regions. These and other arguments seemed reasonable but fell when it was found that natural, rather than man-made, species-poor communities were stable, and when the relationships between complexity and stability were examined mathematically. Some mathematical models indicated that stability in fact decreased with increasing complexity. Further refinements have shown that the stability of a complex community will increase if simplicity is achieved by the removal of top predators, but will decrease (as was originally proposed) when species from nearer the bottom of the food web, such as primary consumers, are removed. The stability of communities is influenced by the stability and predictability of the environment in which they live. Thus it may be that complex yet fragile communities can persist, and thereby give an impression of stability, in benign and predictable environments. The implication for management should be noted: the complexity of many communities is related to the relatively stable natural environments. When even quite minor and short-term changes are made to the environment, the members of a complex community, not used to such disturbance, may exhibit some initial resistance (an ability to avoid change), but low resilience (the speed with which the community can return to its original state) after the change has occurred (p. 569). Coral reefs, then, may be able to withstand just so much stress before the living community completely collapses.
Structure and Formation
Coral reefs form in warm water (generally above 22°C) that is relatively clear and illuminated by the sun, and has a near-to-normal seawater salinity (p. 109). Reefs are poor or absent around coasts near large river mouths because they are intolerant of lowered salinity and high sediment loads. Large rivers are rare in Sulawesi, however, and consequently much of the coasts is fringed with coral (fig. 3.12). Since coral is dependent on light, the depth to which it grows increases with distance from major landmasses where water is rather more turbid. This intolerance of turbid or brackish water results in corals growing faster the further away they are from the land. Thus reefs grow gradually away from the land, leaving shallow lagoons behind them floored with sand composed of broken, dead coral skeletons. The different structures of the steep reef edge and the gently sloping reef flat or reef platform result in changes across the reefs in physical parameters (fig. 3.13).
The coral reef structure is formed by the compacted and cemented skeletons and skeletal sediment of sedentary organisms which formerly lived on the reef but have since been smothered by other organisms. The outermost layer of a coral reef is living tissue comprising primarily of scler-actinian (hard) corals and algae with limestone-impregnated tissues (p. 223).
Figure 3.12. Coral reefs around Sulawesi.
After Salm and Hatim 1984
It was Charles Darwin in 1842 who first distinguished the three main forms of coral reefs still recognized today—fringing reefs, barrier reefs and atolls. Fringing reefs are formed close to the shore on rocky coastlines. If water depth remains the same or decreases over time growth of the reef is entirely seawards, vertical limits being set by the level of low spring tides and the depth to which light can penetrate. Between the crest of a fringing reef and the shore there is usually a shallow reef flat where coral growth is poorer because of reduced water circulation, higher sediment and slightly lower salinity due to run-off from the shore. Vertical growth can occur over geological time if the sea bed subsides or if water depth increases as a result of a rise in sea level, such as happens after an ice age (p. 16). Periods of low sea level during the ice ages would have exposed and killed most the coral reefs and wave action would have eroded their remains into platforms. At the current time, sea level is rising between 3 mm and 15 mm per year and this rate has been maintained for much of the last ten thousand years. Vertical growth of coral has been able to keep pace with this (Barnes and Hughes 1982).
Figure 3.13. The zones of, and changes across, a typical fringing reef which grows away from the land. Zones D, E and F are together sometimes known as the reef flat, reef platform or lagoon. In this illustration, the maximum depth at which there is sufficient light is 20 m.
After Barnes and Hughes 1982
Figure 3.14. Formation of fringing, barrier and atoll reefs.
After Barnes and Hughes 1982
Barrier reefs occur where the coast has subsided and only the seaward reefs have been able to continue their growth. Barrier reefs are therefore separated from the shore by a lagoon. Atolls are formed in a similar manner where a volcanic island has subsided and disappeared (fig. 3.14). Holes drilled vertically through a South Pacific atoll passed through over 1,200 m of dead coral rock before the ancient volcanic cone was encountered (Henrey 1982). Coral reefs have been inhabited by creatures very similar to those found today for at least 200 million years and the great diversity of creatures is at least in part due to this enormous period of relative constancy although conditions in any one location have varied considerably.
These different reef forms all have the same basic biological structure, and differences between the corals found on the three types would probably be no greater than the differences encountered within any one type.
The major reef areas around Sulawesi include:
• Taka Bone Rate (formerly Tijger) Atoll which is the third largest atoll in the world, with an area of some 2,220 km.2 This is only 20% smaller than the largest, Kwajalein in the Marshall Islands (Anon 1982b). It is situated southeast of Salayar and north of Bonerate and comprises a complex of patch and barrier reefs with 21 sandy islands nine of which have permanent inhabitants (fig. 3.15). It is adjacent to the smaller atoll of Taka Garlarang to the northeast and both rise abruptly from 2,000 m on the side of a submerged ridge, similar to the atolls and islands of the Tukang Besi group (Umbgrove 1939, 1940). Part of the northeast corner was studied during the Snellius II Expedition (Moll 1985).
• Sangkarang (formerly Spermonde) Archipelago comprises a loose group of about 160 small islands off Ujung Pandang and covers an area of about 16,000 km2 (de Neve 1982). This has been the site of the most intensive coral reef studies in Sulawesi conducted by Universitas Hasanuddin and the National Natural History Museum in Leiden, Holland.
• The Togian Islands in Tomini Bay are unique in the Indonesian archipelago in having all the major reef environments around their shores. Two atolls lie about seven kilometres off the northwest shore of Batudaka Island (p. 413) and comprise a deep (20-50 m) lagoon surrounded by shallow reef flats. The corals on the lagoon and seaward sides are dominated by different communities. The barrier reef lies close to the 200 m depth contour which in places is 15 km from the shore but elsewhere only 5 km. It reaches the surface only in certain areas and it lacks boulder or shingle ramparts and certain other features indicating that the Togian Islands enjoy calm seas in all sea-sons. Fringing reefs are found around virtually all the coasts and are similar throughout in their composition except in the bays where they merge on the shoreward side with seagrass meadows, which in turn are bounded by Rhizophora mangrove trees. Patch reefs are common within the barrier reef, and where they reach the surface are similar in composition to the fringing or barrier reefs, depending on which is closer (Anon. 1982i).
• Bunaken Island is probably one of the most-visited reefs and this and other coral areas near Manado feature in holidays promoted by international tourist agencies (fig. 3.16).
Figure 3.15. Taka Bone Rate Atoll showing land (black), coral reefs (stippled) and the 500 m bathymetric contour.
Figure 3.16. Coastal habitats near Manado.
After Anon. 1981
In addition, the Vesuvius reefs that lie 80 km south-southwest of the Banggai can claim some notoriety as the place where Sir Francis Drake jettisoned a canon from his ship 'The Golden Hind' during his voyage around the world in 1580. An unsuccessful search for the canon was made 400 years later as part of Operation Drake.
Zonation of corals in the Indo-Pacific is determined by exposure to winds and waves, distance from the reef edge exposed to waves, and water depth (p. 213). As with other types of ecosystems, there is no 'typical' area or 'typical' community, and the composition of communities of organisms varies from place to place as single species respond to differences in the environment. Groups of species may generally be found together but rarely in identical proportions between areas. Where sharp changes do occur in the species composition across an area, this can invariably be related to some major environmental change—such as a reef drop-off, rock outcrops, pollutants, or damage from fishing activities (Barnes and Hughes 1982).
Reef Invertebrates
There are many animals quite unknown to the average reader bearing no names that convey any concrete idea to any one who is not a specialist in the particular branch of natural history to which they belong. A long list of the Latin names of the corals of a reef, for example, conveys no impression, even to many zoologists, of the infinite variations of form, structure and colour which those corals actually present in the living state. A coral reef cannot be properly described. It must be seen to be thoroughly appreciated. — HICKSON 1889
Thus wrote one of the earliest experts on coral, the Englishman Sidney Hickson, who actually got his feet wet on a reef. In 1885 he came to live in North Sulawesi, primarily on Talisse Island off the north Minahasa coast, in order to study corals in nature, and many of his observations are still extremely useful.
There are seven major invertebrate phyla represented on a coral reef and a simple classification of these is shown in table 3.2 and short descriptions follow.
Sponges are the most primitive of multicellular animals. They are generally rather shapeless aggregations of cells whose main distinguishing feature is a maze of canals along which water and suspended food is carried by the action of flagella, or tiny hairs. A sponge the size of a tea cup can pump an astounding 5,000 litres of water per day through its canals. The holes out of which the water passes are usually visible, but the entrances are often very small. Some sponges are cup-like in shape, others are erect branches or mounds but most are encrusting forms seen as red, brown, yellow, blue or black patches on rocks. Many sponge cells are inhabited by blue-green algae, or zooxanthellae, that live symbiotically in the same way as those in corals, sea squirts and giant clams. One group of sponges, the Clionidae, are extremely important in determining the architecture of the reef because they bore into the coral rock using specialized etching cells which dissolve the limestone. Chips which fragment off are 'exhaled' in the stream of water passing through the sponge. The galleries produced in coral rock obviously weaken the structure and may result in the collapse of sections during storms (Bergquist 1978).
Classification from Barnes 1984b
Cnidarians (formerly known as coelenterates) have a tube-shaped body with one opening at the upper end through which food and waste is alternately passed. The hydroids have a simple sac for a digestive chamber but this is more complex in corals and sea anemones. The two most-commonly seen hydroids are rather different. The sea nettle Aglaophenia grows like a pinkish-brown fern about 20-30 cm high. Fire coral Millepora however, looks ostensibly like an ordinary coral, but with a hand lens the characteristic pattern of five or six small holes surrounding a larger hole can be seen. The 'mouth' of all cnidarians is surrounded by tentacles armed with stinging cells or nematocysts out of which barbed harpoons are shot when touched (fig. 3.17). These can just be felt if a sea-anemone is touched but those fired from jellyfish and some hydroids can caused intense pain. Hence the common names of 'fire coral' or 'sea nettle' given to some hydroids that are capable of delivering a memorable sting to unwary divers.
An individual coral animal starts life as a small planktonic larva which comes to rest on a suitable substrate and metamorphoses into a polyp. This polyp begins dividing and forming genetically-identical polyps next to it, and this process continues until the coral dies. Within the 'skin' of the coral polyps are small yellowish-brown granules, which are in fact small plants from the phylum Dinophyta (dinoflagellates), other members of which are found in the marine phytoplankton. Only a single species, Symbiodinium microadriaticum, is known to live symbiotically with corals. These plants, called zooxanthellae because they live within animals, absorb waste products produced by the host polyp converting the phosphates and nitrates into protein and, with energy from the sun, the carbon dioxide into carbohydrates. Their waste product, oxygen, is used in turn by the polyp in its respiration. Coral polyps secrete their external skeleton of limestone from their bases but each polyp is connected to its neighbours by strands of tissue (fig. 3.18).
Corals mature after three to eight years and tend to breed seasonally and often simultaneously in a certain area. Until recently it was thought that most scleractinian corals were viviparous, that is brooding fertilized eggs within the polyp, often releasing larvae throughout the year. Careful observations in northeast Australia revealed, however, that most corals release gametes simultaneously at night a few days after full moons (Harrison et al. 1984).
Why should corals breed simultaneously? If breeding were not simultaneous, there would be great risks involved in spawning eggs or sperm, both of which have limited periods of viability, into the sea. The chances of egg meeting sperm if spawning were random would be very low. In addition, if only a few eggs were in the water at any given time it is likely that a relatively large proportion of the eggs would be eaten both by opportunistic or by specialist predators. Thus simultaneous spawning gives the maximum opportunity for successful fertilization, minimum chance of any particular egg, fertilized or not, of being eaten, and prevents any animal specializing on coral eggs as food.
Figure 3.17. Cnidarian nematocyst before and after the firing of the 'harpoon'.
After Henrey 1982
Not all corals breed every year, though this would most often be the case for the slower-growing, longer-lived species. An individual Pontes measuring 5.8 m in diameter was estimated to be 140 years old but was still increasing its diameter by over 4 cm per year. Monitoring of young colonies of about 1 cm diameter (about one month old) on the Great Barrier Reef revealed that five colonies per m2 were recruited per year on a reef flat but that half of these died within a year (Connell 1972).
Most human visitors to a reef swim during the day and see but a pale shadow of the wonders that can be seen at night. It is then that the sharp edges of coral seen during the day are transformed into soft, fuzzy outlines as millions of colourful tentacles sweeping through the water catching minute plankton or other particles of food. Startling examples are the mushroom corals such as Fungia which lie loosely on the reef bed like large, upturned mushrooms.9 During the day these are dull, lifeless and gray-brown but at night thick, bright-coloured tentacles emerge from the mushroom's gills, totally obscuring the skeleton beneath. In addition, because the wavelengths of red, green and yellow light are quickly absorbed by water, much of the deeper reef appears blueish by day, but the true colours can be seen by torchlight.
Figure 3.18. Cross-section through a coral polyp.
A total of 262 species of hard (scleractinian) corals from 78 genera and subgenera have been identified from the Sangkarang Archipelago.10 This is more than is known anywhere else in the Indo-Pacific region. Of this total of species, six have recently been described for the first time (Moll and Borel-Best 1984).
Surveys of the Sangkarang reefs revealed that similar numbers of species were found on the reef edge, reef flat and reef slope but that only 110 species were found in all three situations. There were 24 species confined to the reef flat and 17 species to both the reef edge and reef slope (Moll 1983). However, the number and coverage of coral units or colonies is higher on the reef edge than elsewhere. The islands were divided into three strips according to their distance from the shore but little difference was found between them in terms of corals present in each strip. The northern reefs were richer, however, than those in the east or the south, and the western reefs had a greater cover than those in the east and south. Differences between the compositions that were detected, however, could be related to distance from the mainland but there was great similarity between the composition of reefs in similar situations throughout the islands. The data were obtained by repetitive transects and the method is explained more fully elsewhere (Moll 1983).
A total of 115 species from 59 genera of coral have been found around the Togian Islands. Little difference in the number of coral species was found between the three types of reefs examined in detail but their distributions were distinct, as revealed by discovery curves11 (fig. 3.19). Thus the initial rapid rate at which genera were encountered over the atoll reflects a well-mixed and diverse community of corals. The rate of discovering coral genera over the two fringing reefs was slower and no new genera were found after about 30 minutes. The smooth curve from the reef inside a barrier lagoon is again typical of a well-mixed community of corals but in this case the individual coral colonies are either larger or occupy larger areas. The step-like discovery curve from a sheltered fringing reef reveals that different communities of coral were distributed somewhat patchily rather than being mixed.
Figure 3.19. Discovery curves for coral genera and subgenera from three reefs around the Togian Islands.
After Anon. 1982a
At a relatively undisturbed part of the Bunaken reef 58 genera of coral have been recorded, mostly in well-mixed assemblages (Anon. 1981). A total of 68 genera (158 species) have been recorded from a lagoon in Taka Bone Rate (Anon. 1982a).
The reason for the high diversity of corals in Sulawesi and certain other tropical regions is not fully understood but it is certainly related to three factors—more specialization, more time (because of lack of seasonality) and greater area. A longer time allows a greater proportion of species and/or their descendants to survive in the tropics by favouring greater specialization (Rosen 1981). The greater area is probably the most fundamental.
Figure 3.20. A sea wasp (left) and a typical rhizostome jellyfish (right).
After Henrey 1982
Whereas most cnidarians are colonial, some such as sea anemones and jellyfish are not. A sea anemone is a single large polyp with a thick muscular body attached to a rock. Some are over 50 cm across and the spaces between the tentacles are often occupied by clownfish. Jellyfish and hydroids pass through a life stage called a medusa in addition to the stages of the free-swimming larva and the polyp. In hydroids this is a relatively minor stage but in jellyfish the medusa is the dominant life form. Most jellyfish seen around reefs are members of the Rhizostomeae with no tentacles around the bell edge but many 'arms' around the central mouth. However, dangerous sea wasps are creatures with cuboid bells with four flattened sides and tentacles hanging from the four corners. The vicious stings from these tentacles make sea wasps among the most venomous animals in the sea (fig. 3.20; p. 232).
Soft corals do not secrete a limestone skeleton; the polyps sit instead in a gelatinous material of dull grey, brown or yellow colour. They grow into various shapes like mushrooms, fingers or just flat masses. Black corals and sea fans are similar in that they have a central axis of horny material around which the polyps live, but in black corals the axis is black and thorny and in sea fans it is brightly-coloured and branched. Black corals are generally found below 20 m, somewhat deeper than sea fans.
Bryozoans are small colonial animals looking like lacy moss attached to rocks, seaweeds or shells. Bryozoans are one of the more common organisms found growing on ship hulls leading to drag and loss of speed.
Many gastropod snails with exquisitely-patterned shells can be found around reefs, although shell hunters have drastically reduced the numbers of certain species (p. 230). For example, shells of over 170 species of snails have been found on the beaches of Tangkoko-Batuangus Reserve, Minahasa, and most of these were presumably thrown up from the fringing reef (Anon. 1980b). Other molluscs known as sea slugs (Nudibranchia) have lost their shells and evolved incredibly beautiful skin colours. The best known of the bivalve molluscs are the giant clams, most of which burrow backwards into coral rock. All that a diver sometimes sees is the intense blue, spotted flesh of the 'tips' which, like coral and sponges, contain zooxanthellae, or algae, living symbiotically within the cells. One of the species of giant clam found around Sulawesi, Tridacna gigas, has been found to spawn sperm during incoming tides during the full, third quarter and new phases of the moon. Plans are being aired to culture or translocate giant clams in Indonesia and it is important that the spacing and sexual behaviour of these animals be studied. In Australia it has been found that mature animals are on average 9 m apart and even where collectors have left some clams in place, this is no guarantee that the density is high enough for effective fertilization of eggs. The management of giant clams is further complicated by the ability of an adult clam to change its sex (Braley 1984).
If the word 'worms' conjures up a picture of dull, pinkish-gray creatures, then examining a coral reef will change that limited view. Here, polychaete worms live in burrows they build into the coral rock and extend their stunningly beautiful feeding structures into the water. The worms stop feeding and retract into their burrow when they detect unusual movement close by. The most common polychaetes are the intense blue, yellow, brown, orange or red bottlebrush worms Spirobranchus which have two sets of feeding apparatus, each of which has about five tiers of tentacles. Young bottlebrush worms in fact occupy cavities left by dead polyps and grow up as the coral grows.
The two most commonly seen echinoderms are very conspicuous in the inshore regions. They are black-spined sea urchins Diadema, the long spines of which are venomous and can cause considerable pain, and the blue starfish Linckia laevigata, which is commonly seen lying in the sun in shallow water on rocks or sand. One of the best-known starfish in coral areas is the large and very spiny crown-of-thorns starfish Acanthaster planci. This preys on coral by inverting its stomach over an area of coral, secreting digestive juices and sucking out the digested polyps (Chester 1969). This starfish is quite common around Bunaken Island near Manado. In the 1960s the population of this animal exploded in the Indo-West Pacific Ocean. Large areas of coral were devastated—a single adult destroys about 5 m2 of coral per year—and the tourist industry at certain places along Australia's Great Barrier Reef suffered considerably. Information from Indonesia is scanty. Even now, there is no satisfactory hypothesis as to why the population explosion occurred, but with an adult female producing about 20 million eggs each year the potential for growth is enormous. It is unlikely that man was directly responsible for the population explosion because the area over which it occurred was vast. It may be, however, that release from predator pressure could have caused the explosion because the only predator of any importance is the giant triton Charonia tritonis (fig. 3.21) which, because of its size and beauty, is much sought after by shell collectors (Anon. 1984a). Large-scale collection did not begin, however, until after about 1950 and it could be that their removal allowed numbers of A. planci to increase (Paine 1969).
Figure 3.21. Giant triton Charonia tritonis, the major predator of the crown-of-thorns starfish.
Sea cucumbers look just like their name suggests.12 Instead of five arms or segments they have five rows of tubefeet. When annoyed, species of Bohadschia can exude sticky secretions to distract or entangle predators. They may even eject some of their sticky internal organs if extreme defence measures are required. The lost organs subsequently regenerate. There are probably about 30 species around the coasts of Sulawesi but the most common species are Holothuria atra which measures up to 60 cm in length and has sand stuck to its black body; Stichopus chloronotus which is smaller (about 30 cm long), dark green with orange-tipped lumps; and Holothuria scabra which is variable in colour but is generally yellowish cream with black and grey spots. This last species has a symbiotic relationship with a small pea crab Pinnotheres (similar to those found in cockle Anadara granosa shells and giant clams) which lives in its anus. Rather rarer are the wormlike or synaptid sea cucumbers which reach a metre in length, have a relatively thinner body and tentacles around the mouth.
Figure 3.22. A typical sea squirt or tunicate. Arrows indicate the flow of water.
Feather stars, or crinoids, have 10 or more brightly-coloured feather-like arms along which food is passed to the mouth.
Sea squirts, or tunicates, are sac-like animals with two openings—water and suspended food are drawn through the top opening and exhaled through the side (fig. 3.22). These can be found as solitary individuals or in small groups such as the green grape ascidian Didemnum, which is indicative of somewhat polluted water, such as near a town. Sea squirts, like sponges, corals and giant clams, have symbiotic blue-green algae growing inside their cells.
Colonial animals such as sponges, corals, bryozoans, and compound sea squirts comprise genetically identical units which together can grow to a size far greater than that possible for the individual. The modular construction permits flexibility in growth form which can adapt to the force of water currents, light intensity, silting and competitors. The colonies, or fragments of them, have considerable regenerative capabilities and large branching corals may propagate following damage caused by storms. For example, extremely large waves associated with strong winds in January 1986 bombarded the southwest coast of Sulawesi and reduced growths of Acropora coral to rubble even at 4 m below the surface. At one site studied intensively it was calculated that waves with velocities of 1.7 and 1.0 m/s at 0.1 m and 4 m depths respectively had caused the destruction; typical maximum wave velocities at the surface are around 0.4 m/s (P. Bloks pers. comm.). Four months later some regeneration of the Acropora had occurred. It would appear that Acropora actually benefits from this fragmentation (Bak 1981; Bothwell 1981; Highsmith 1982).
From November to April winds from the west buffet the western side of Bahuluang Island southwest of Salayar, and during the southeast monsoon it is protected from the wind's strongest effects by the much larger Salayar. The effects of this differential exposure on reef composition is quite dramatic (table 3.3). Thus, in the east (Transect 4), foliose corals contribute 40% of the cover and massive corals are very scarce. Conversely, in the west (Transects 2 and 3) there are few foliose corals but there are large numbers of massive corals. The exposed coral (Transect 1) is intermediate in its cover characteristics but it has the most species and colonies of massive corals and the least number of branching coral colonies. In each transect, however, the percentage cover of branching corals is remarkably similar. Considerable differences are found at the species level: for example, only one species of the branching Acropora is found on both the east and west of the island and some genera of smaller corals are found only in the east. On this eastern side, the large and fragile growth forms reflect the more sheltered conditions prevalent there (Moll 1985).
Coral transects around the small sand bar of Tinanja at the edge of the northeast part of the Taka Bone Rate Atoll also showed the effects of exposure (Moll 1985), as did the much more detailed work in the Sangkarang Archipelago (Moll 1983). In summary, harsh exposure combined with heavy sediment transport results in low coral cover. Where water movement is moderate in a situation close to the open sea, corals flourish.
After Moll 1985
The incredible diversity of animals on a reef poses intriguing questions of how so many can co-exist, for it is generally believed that coexistence of two or more competing species can only occur if each species is exploiting a different set of limiting resources or, possibly, a similar set of limiting resources to different intensities. This is known as the 'Principle of Competitive Exclusion' or 'Cause's theorem'13 (named after the Russian biologist who first investigated the means by which closely related species of micro-organisms coexist in the laboratory). Many closely-related species, such as those from a single genus, are often too similar in their ecology and behaviour to live in the same area because they compete for the same limiting resource and the species least able to compete is excluded—that is, the species live allopatrically (p. 69). Species that live sympatrically, that is, in the same area, exploit the available resources in different ways. An example are the cone snails Conus (fig. 3.23), the shells of 41 species of which have been reported from the beaches of Tangkoko-Batuangus Reserve, Minahasa (Anon. 1980b). One might reasonably ask how all these similar creatures achieve exclusive niches. That would be an interesting research topic, but some clue is given by the results of work on just eight Conus species conducted around Hawaii. The major food items of these predatory snails were examined and it was found that no two species had exactly overlapping diets (table 3.4). In areas where fewer sympatric Conus snails are found, the niche breadth or range of food in the diet would be expected to increase, and where more species coexist even more specialized diets would probably be found (Kohn 1979).
Many of the reef invertebrates, such as giant clams, are used by coastal people as food or, like sea cucumbers, have been exploited for centuries as items of international trade (p. 85). In general the inefficiency of the collecting methods have meant that the harvesting has been sustainable, and this is proven by the great age of the sea cucumber trade.
A number of invertebrates have considerable value on modern markets and the harvesting has been conducted from motorised vessels using teams of scuba divers. The most important collecting and export centre for this trade in Indonesia is Ujung Pandang which, in 1981, recorded foreign exports of 2,100 tons of reef invertebrates14 which comprised 740 tons of pearl oysters Pinctada, 820 tons of mother-of-pearl shells Trochus, 220 tons of other shells, and 320 tons of sea cucumbers. In addition to these there were also quantities of black coral and spiny lobsters as well as catering for the growing domestic market, particularly for giant clams whose shells are now used in the manufacture of floor tiles. Some of the markets, particularly that for pearl oysters, are on the verge of collapse due to extreme over-exploitation (Anon. 1984a). If this is not to happen to all the markets then some effective controls must be promulgated and enforced by the appropriate authorities.
Figure 3.23. Braided cone shell Conus textile.
After Kohn 1959
Reef Fish
There is a greater density of fish species on a reef than in any other place in the sea, with 100-200 species present in a single hectare. The colours, patterns and shapes are breathtaking. The relative ease of observation and the beauty of the subjects make study of their diverse behaviour and ecology extremely rewarding.
The enormous numbers of fish species associated with coral reefs and the high diversity has led to a bewildering array of shapes, patterns and colours enabling individuals from the same species to identify one another (fig. 3.24). Two field guides are available to assist in fish identification (Carcasson 1977; Schroeder 1980).
Reef fish can be divided roughly into those found in rock pools, on the reef flat and those of the reef edge and slope, characterized by 9, 45 and 80 species of fish respectively off Salu Island, Singapore. The reef edge species tended to be larger species of the open sea belonging to the jacks or scads (Carangidae) and snappers (Lutjanidae). The more inconspicuous frog fish (Batrachoididae) and scorpion fish (Scorpaenidae) were restricted to the reef flat and rocky areas. In terms of abundance more fish were found on the reef edge and slope than on the reef flat and this may relate to the amount of available cover (Tay and Khoo 1984).
The most dangerous animals around a reef are fish. Among the fish this group would include sharks (generally small except in deeper water), stingrays (Dasyatidae), moray eels (Muraenidae), lionfish (Scorpaenidae) and stonefish (Synanceiidae). These last two could not be more different: lionfish flounce around the reef in gaudy colours, whereas the drab, grotesque stonefish lies still with its large warty head and mouth almost invisible among the corals. Spines of the dorsal fin inject a poison which can be fatal to humans (fig. 3.25). For this reason if no other, stout shoes should be worn if one is intending to walk on a reef. The other dangerous vertebrates are the sea snakes but most are rarely seen. One, however, the gray-and-black striped Laticauda colubrina is confined to coral reefs and the beaches where it lays its eggs (fig. 3.26). The bites of some sea snakes can be extremely dangerous but L. colabrina is reluctant to bite, even when handled, and has a venom of low toxicity.
Some fish, particularly those seen just off the reef edge are schooling species with large ranges. On the reef itself there is a bewildering range of social organizations. Some species feed over a 10 m wide stretch of reef reacting aggressively only to others of their species; others, such as small damselfish, occupy very small territories which they defend against everything, including divers. Some live alone, others in groups often with just one male, which results in the formation of bachelor-only groups. In some such one-male groups, when the leading male dies, the largest female in the group immediately adopts male behaviour and soon assumes the physical and physiological characters of the male.
Figure 3.24. Reef fish of Sulawesi to show the range of shapes and patterns, a - Spotted seahorse Hippocampus kuda; b - Starry moray Echidna nebuiosa; c - Blue-lined sea bream Symphorichthys spilurus; d - White-spot humbug Dascyllus trimaculatus; e - Pennant coralfish Heniochus acuminatus; f - Orange clownfish Amphiprion ocellaris; g - White-barred triggerfish Rhizecanthus acuieatus; h - Two-eyed coral fish Coradion melanopus; i - Toadfish Arothron areostaticus; j - Black-tailed thrush eel Moringua bicolor; k - Black-barred garfish Hemirhamphus far; l - Patterned tongue sole Paraplagusia bilineata; m - Tapefish Anacanthus barbartus; n - Boxfish Tetrasomus gibbosus; o - Red-purple parrotfish Scarops rubroviolaceus.
After Carcasson 1977
Figure 3.25. Two venomous fish of coral reefs: Lionfish Pterois volitans (right) and stonefish Synanceichthys verrucosa (left).
After Carcasson 1977; Schroeder 1980
Some peculiar niches occupied by fish are well-known but are nonetheless interesting. There are small fish called 'wrasses', some of which establish cleaning stations on the reef which are visited by larger fish to have their gills, teeth and bodies cleaned of parasites, algae and debris. Another small fish, a blenny, has very similar markings and behaviour which larger fish mistake for the cleaner to their cost because the blennies take bites of flesh instead of removing parasites (fig. 3.27).
Anemone, or clownfish (Amphiprionidae), lessen the chance of falling prey to other fish by taking refuge among the stinging arms of large sea anemones. It used to be thought that they slowly covered themselves with anemone mucus, from their tail forwards, thereby becoming indistinguishable to the anemone from its own tentacles, but it appears now that the fish itself produces its own protective mucus (Brooks and Mariscal 1984).
A study of coral reef fish off the southwest coast of Sangihe Island found seven dominant species (table 3.5). Analyses of the stomach contents showed that all except the rabbitfish ate mainly crustaceans and that the parrotfish tended to eat fewer snails than the snapper or rock cod (table 3.6). Diets also changed from month to month possibly due to changes in availability of food, but the relative contribution of the different food types remained quite similar (Tilaar 1982).
Figure 3.26. Venomous sea snake Laticauda colubrina. It has a grey-and-black striped body, a yellowish belly, and yellow marks above and below its eyes.
After Tweedie 1983
Parrotfish generally swim by using their pectoral fins, their tails being employed only when they have to swim faster. They are sometimes seen in small groups which can comprise of adult females and a single adult male who defends the females against other males. Older males sometimes develop a bump on their head. At night they shelter in small caves or under overhanging ledges. These are used consistently such that even if a parrotfish is taken some way from the reef it will swim directly back to its shelter, so long as the sun is visible. Parrotfish and wrasses are peculiar in that at nighttime they secrete mucus from glands in their skin which forms a shroud around them. Whether this is a protection against enemies or whether it is to prevent the gills becoming clogged with silt while the fish is asleep is not known.
Reef fish, like reef invertebrates are objects of trade (p. 230). Indeed most of the marine ornamental fish traded on the domestic and international markets are associated with reefs. The Indonesian region has more potential ornamental marine fish species, perhaps more than 250, than any other region. For comparison, the next most important areas are Sri Lanka with 165 species, the Philippines and Ethiopia with about 110, and Kenya with about 95 (Kvalvågnaes, 1980). Major collecting areas are near Ujung Pandang, Manado and Kendari, as well as around the islands of Kabaena, Salayar and Siau (fig. 3.28). Most of the fish caught are sent to Jakarta for export.
The impact on the wild populations of this collecting is hard to assess with any accuracy but it should be remembered that of every 1,000 fish caught, only about 70% survive to be sold and only half of these live more than six months (Anon. 1986). The regulation of the trade and captive breeding needs to be encouraged with economic incentives.
Figure 3.27. The cleaner wrasses Labriodes dimidiatus (left) and its mimic, the blenny Aspidontus tractus.
Figure 3.28. Capture sites of marine ornamental fish (indicated in black).
After Sa/m and Halim 1984
Average length (cm) given in parentheses.
After Titaar 1982
Epinephelus tauvina (Et)
Argyrops spinifer (As)
Scarus dimidiatus (Sd)
S. chlorodon (Sc)
S. bowersi (Sb)
S. lepidus (Sl)
Siganus furcescens (Sf)
Reef Algae and Herbivores
Although a coral reef may appear to be dominated by animals, plants can in fact constitute 75% of the biomass in an area of reef. These plants include both very fine filamentous algae growing in dense mats or turfs, larger seaweeds or macroalgae (fig. 3.29), and coralline algae. This last group are red algae that are calcified, that is they deposit limestone in their cells and are consequently extremely hard. Nearly 22% of the surface of a coral reef near Hawaii was found to be covered with coralline algae (Johansen 1981). The green algae Halimeda are also calcified and together with the coralline algae appear to be the major suppliers of sediment below the reef slope (C.V.G. Phipps pers. comm.). Large algae show distinct patterns in their distribution; red algae are found on inner reef flats and outer edges of coral reefs, brown algae such as Sargassum usually occur throughout the reef flat, and green algae tend to be found in intertidal zones. The reasons for these patterns do not seem to have been investigated.
Certain seaweeds are cultivated and harvested to produce compounds for the food and chemical industries. Red seaweeds such as Gelidium and Gracilaria produce agar used in fish and meat canning to prevent breakage, in the manufacture of ice cream, milk drinks, cakes, jams, jellies, as well as in cosmetics. Other red seaweeds such as Eucheuma produce gums called carrageenan which are similar to agar but are thicker and are used in the food and cosmetic industries, as well as in paint, insect-sprays and insecticides (Chapman 1970; Teo and Wee 1983). The Menui Islands in extreme southeast Central Sulawesi are a major producer of carrageenan (Hasan 1975) and areas with potential for commercial alga production are found all round the coast (fig. 3.30).
Most herbivorous mammals possess specialized, symbiotic gut organisms which assist in the digestion of plant material or secondary metabolites, producing compounds usable by the animal. Such a relationship has only recently been discovered in marine fish, specifically in the reef-dwelling surgeonfish Acanthurus nigrofuscus, a species studied in the Red Sea but also found around Sulawesi (Carcasson 1977). Many day-feeding fish empty their guts before resting for the night but, A. nigrofuscus retains a ball of undigested algae. When it begins to feed in the morning it voids this onto the reef upon which it then grazes and this may be the pathway by which it reinfects itself with the symbiotic organisms (Fishelson et al. 1985).
Sea urchins are among the most important grazing animals on the reef and exert heavy pressure on plant biomass. For example, the biomass of algae in a plot from which sea urchins were removed reached 159 g/m2 in contrast to 12 g/m2 in areas where sea urchins grazed, although the net productivity of ungrazed tufts may be lower than grazed turfs (N. Polunin pers. comm.).
The presence of sedentary animals seems to be inversely related to the presence of algae. It appears that filamentous algae interfere with the feeding structures of erect bryozoans. In addition, in places exposed to grazing by parrotfish and surgeonfish, the presence of algae around sessile animals, such as sea squirts, exposes the latter to damage from those fish species that scrape algae off rocks. In this way fish 'weed out' sedentary animals from algal beds (Day 1983).
Figure 3.29. Common coral reef algae. Red algae: a - Gracilaria lichenoides (Grac.); Green algae: b - Caulerpa racemosa (Caul.), c - Halimeda tuna (Codi.), d - H. opuntia; Brown algae: e - Turbinaria conoides (Fuca.), f - Padina gymnospora (Dict.), g - Sargassum polycystum (Sarg.). Scale bars indicate 1 cm.
After Teo and Wee 1983
Figure 3.30. Areas around Sulawesi with potential for the harvesting of commercially-useful algae. Dotted line shows the Taka Bone Rate reef shoals.
After Salm and Halim 1984
Productivity and Plankton
The gross primary productivity of coral reefs is high, about 3,000-7,000 g C/m2/yr (equivalent to 70 t/ha/yr) (pp. 207 and 311). This is balanced by very high respiration, however, so that the net primary productivity is about 300-1,000 g C/m2/yr (Mann 1982). Even so, coral reefs are about 20 times as productive as the open sea where net primary productivity is only about 20-40 g C/m2/yr. The symbiotic zooxanthellae are about as productive as the benthic algae but, because the zooxanthellae are less abundant than the algae, they probably account for less than half of the net primary productivity (Levington 1982).
Coral reefs support many fish, coral and other invertebrates, but early studies of zooplankton densities showed that the density of plankton drifting over coral reefs from the sea was too low to support the reef organisms. In fact, certain zooplankton leave the reef at night and return before dawn (Alldredge and King 1977). Another major source of zooplankton is found close to the coral. These plankton rise from their refuges at dusk and retreat at dawn and thus represent the most important food for the night-emerging corals. So, most of the zooplankton are not drifting in from the sea but are resident among the coral resulting in most of the nutrient minerals being recycled within the reef ecosystem. It is important to note that neither of the major sources of plankton would have been detected by the standard methods of plankton sampling such as net towing (Birkeland 1984).
The filamentous algae growing on the rock (dead coral) on reefs are grazed, and up to 6% of the filamentous algal biomass per day can be removed from some areas. About 50% or more of the algal production enters the grazer food chain (Hatcher 1981), primarily through parrotfish and surgeonfish. The flow of energy through a reef ecosystem is therefore primarily through grazing not through detritus feeding and this is a major factor in understanding coral reef systems (Hatcher 1983; Hatcher and Larkum 1983).
Causes of Coral Death and Reef Destruction
The major and most insidious cause of coral death is suffocation by sediment, either in suspension in the water or that has settled on the coral polyps. Both prevent light from reaching the photosynthetic zooxanthellae and the suspended matter may overburden the filter-feeding polyps with inorganic material. Thus, any plan concerning coral in coastal zone management must include considerations of the sources of that sediment: uplands subject to bad farming practice, deforestation and logging, overgrazed pastures, and public works projects that expose bare soil to the full force of the rain. To incorporate such concerns in regional planning requires dedicated and co-ordinated government action.
One of the most common causes of reef destruction is the use of explosives to catch fish and to break coral into rubble for use in construction projects. For both purposes, explosives are very efficient but it is not without cause that using explosives over reefs has been outlawed in many areas. Explosions kill fish indiscriminately without regard to food value, and more fish probably sink and decay than float to the surface for collection (Burbridge and Maragos 1985). This is because the major site of internal damage is the swim bladder, a sac of gas used to control buoyancy. This is ruptured in explosions and so many fish lose that buoyancy and sink when they die. Bottom-dwelling fish, with poorly-developed swim bladders, are less likely to be killed than other species (Wright 1982). The effects of underwater explosions on invertebrates or dugongs has not been studied, but it is known that divers can suffer perforated ear drums if diving while coral is being blasted. Despite the regulations, the use of explosives is still widespread particularly in the remote, uninhabited areas that are the most valuable for conservation purposes,
The coral itself may recover from blasting (Parrish 1980), but it would take many decades before the effects of blasting are no longer obvious to even a casual diver. The coral rubble and the algae growing on it have a relatively low productivity and the biomass of plankton over such areas is little greater than that over plain sand (Porter et al. 1977). When considering different impacts on coral it is worth remembering that most coral has a radial growth rate of between only 1 and 10 mm/yr (Soegiarto and Polunin 1980).
Although at first sight this may be difficult to understand, coral reefs play a very significant role in protecting coasts from erosion. In deep water the height of an ocean wave is one-twentieth of its length. When a wave approaches shallow water, however, the drag of the sea bed shortens the wave length and the wave is forced up into a peak. This sharp-topped wave breaks when its height is in the ratio of 3:4 with the water depth. Thus a wave 30 cm high will break in water 40 cm deep. It is for this reason that waves can be seen breaking (and have much of their energy dispelled) some distance offshore above the reef slope. In places where the reef is broken or blown apart for the collection of hard core for roads and other constructions, the concave nature of the reef lagoon is changed into a sloping shore partly because the coral 'lip' is being removed and partly because of increased sedimentation. The waves now break nearer the shore and the wave energy is now not just effective in creating water turbulence but also scours the coastline. The killing of coral reefs also greatly reduces the productivity of the coastal waters with the result that the production of reef-related fisheries is certain to fall (fig. 3.31).
It is generally true that the closer a coral reef is to a centre of human habitation, the more disturbed it will be. Thus on the eastern shore of Bunaken Island, four sites at increasing distance from the main village had more or less the same number of coral species present in the study plots (about 18-21 species), but the area of dead coral decreased with distance from habitation (fig. 3.32) (Lalamentik 1985).
Figure 3.31. The consequences of destroying fringing coral reefs which protect the coast are that the land suffers erosion, the coral no longer supports fish and other commercial animals, the water becomes turbid, and fishing yields decline.
Coral Reef Fisheries
The largest reef fishery in Indonesia is probably found in the shallow sea of the Sangkarang Archipelago which lies within 80 km of Ujung Pandang. This fishery is based largely on the islands of the archipelago. Some of the islands of the Sangkarang Archipelago west of Ujung Pandang, and coastal areas north and south of Ujung Pandang have dense human populations many of which are dependent on reef fisheries (fig. 3.33). Fishing villages are the least developed of coastal villages and in general have the lowest household and per capita income of all types of villages. This is due to the seasonal nature of their fish harvests, the lack of relevant technology and skills, and the paucity of supplementary jobs available in such villages (Makaliwe et al. 1985).
Figure 3.32. Bunaken Island, Minahasa, to show the percentage of dead coral in four study sites.
After Lalamentik 1985
This is well illustrated by a comparison of the situation on two islands 2 km apart that lie 12-15 km from Ujung Pandang. One is based on a mixed economy and the other is entirely dependent on reef-fisheries (table 3.7). Over the last two decades, the numbers of fishermen have increased and the capture per unit effort has increased for those fishermen able to exploit new technologies. Those who have been unable to exploit such changes have been locked into a situation of poverty combined with increasingly intense exploitation of coral reef fish. They can escape from this situation only if money for development is available outside the private sector for consolidating fishermen's cooperatives and possibly for the introduction of mariculture projects based on clams, pearl oysters, mussels, etc. Any such initiative will, however, have to contend with an established philosophy of resource use in a conservative and proud people (Davie and Mustafa 1984). In addition, it should not be taken for granted that all fishing communities appreciate the connection between healthy reefs and successful fisheries. The fishermen on Bunaken Island, for example, apparently do not, and therefore need to be educated in this regard. They see tourists coming to snorkel and dive around their island, but they themselves see little financial incentive for encouraging such attention (Rondo and Sondakh 1984).
Figure 3.33. Number of fishing households per kilometer of coast by county.
After Salm and Halim 1984
Based on Basuni 1983; Davie and Mustafa 1984
The view is sometimes expressed that, in days past, coastal communities devised systems of tenure that conserved marine resources. A recent exhaustive review of historical information relating to this subject failed to find any such systems reported from the Sulawesi (or Borneo) mainland, although there are many reports from eastern Sumatra, the Moluccas and New Guinea. The only report of marine tenure from a Sulawesi island was from Salayar where the ownership of reef areas was passed from father to son. The dearth of information from elsewhere probably indicates that other tenure systems ceased to operate before those interested in writing about such matters arrived, and that the systems were not very common anyway. The conclusion of the review was that tenure systems were instituted not through a desire to conserve resources, but rather because fishermen wanted to increase their exploitation and eventually found their neighbours doing the same thing. Traditional ownership patterns are therefore an imperfect and risky route to follow to establish responsibility among fishermen within a plan for coastal zone management, because they are based on human gain rather than on an ethic of restraint (Polunin 1984).
Coral Reef Survey Techniques
If the impacts of development activities on coral reefs are ever going to be assessed, then it is essential that work begin now on collecting data from those reefs closest to centres of development. The techniques used need to be able to provide systematic information on changes and natural variation. This repeatable collection of data on all aspects of the coral reef does not appear to have begun in Indonesia, although relevant work has been conducted in New Caledonia since 1973 (Dahl 1981b).
Sea water is an unnatural environment for man and for him to survey coral reefs requires a certain amount of skill and equipment. Firstly, those doing the survey work clearly must be able to swim. Surveys at low tide conducted by walking over the coral can cause considerable damage, puts people in danger of touching venomous fish (p. 232), and is not to be recommended. Scuba diving using tanks of pressurized air is by far the best for examining reefs but it should only ever be done in pairs and after training from qualified instructors. Snorkel and mask, particularly with belt of weights, represent a very good second best and are quite sufficient for working over the reef flat and reef edge.
Figure 3.34. A line-transect across a patch of coral showing the measurements taken. Thus: cover by species A = b+g+h, cover by species B = d+e, cover by species C = e+f+g, overlap = e+g, total cover = b+d+e+f+g+h.
After Moll 1985
A wide variety of techniques are available for making quantitative surveys of coral but the line-transect method has been used extensively around Sulawesi and elsewhere. For example, it was used for the study of coral during the Indonesian-Dutch Snellius II Expedition in 1984-85. A series of 30-m transects are laid at set intervals from the shore and measurements are made of the coral cover, or any other parameter directly below the transect tape15 (fig. 3.34) (Moll 1985).
Line-transects are less suitable for broader studies in a coral reef monitoring program. The methods described below are based on those recommended by the South Pacific Commission for environmental monitoring programs and are well suited to non-specialists. A single person can collect data related to all parameters after some training (Dahl 1981a). A blank data sheet is provided in Appendix N and this could be photocopied, placed back to back, and laminated in plastic. The plastic surfaces can be roughened with fine sandpaper so that they can be written upon underwater.
Circular plots of 50 m2 can be established by fixing a permanent marker to some obvious feature and marking a circle with a radius of 4 m around this marker. Plots should be established in each of the major reef habitats: inner lagoon near the shore, mid-lagoon or patch reef, outer lagoon just inside the reef, back reef where it slopes into the lagoon inner reef flat, outer reef flat, and reef slope. None of the plots need to be deeper than about four metres except on the reef slope which may have to be omitted if appropriate equipment is not available. The sites chosen as plots should appear to be typical of the area within the zone, and given this qualification, may be selected by random sampling.
The number of plots established will depend on the time and manpower available and the type of study. For a straightforward monitoring study at least two plots in each habitat should be established, but for an environmental impact analysis more plots and control plots would be necessary. Repeat surveys are necessary every year at roughly the same time but surveys every two months would provide valuable information on natural variations.
The parameters to be recorded are as follows:
Fish Counts. Since fish are easily scared, it is best to tie a floating rope to the permanent marker and to swim 100 m parallel to the reef edge counting particular fish within an imaginary 5 m transect below the swimmer. Only two groups of fish are to be counted: predators and butterfly fish. Predators to be recorded are longer than an outstretched hand16 and belong to three families. Butterfly fish are generally smaller than an outstretched hand and are often seen in pairs around coral (fig. 3.35). They are territorial and will be seen in more or less the same location on the return swim.
Percentage Cover. Some of the 50 m2 circle will not be covered with corals, etc., but by mud (grains not distinguishable), sand (grains obvious), rubble (finger-size to head-size) or blocks (larger than head-size). The percentage of the circle covered by major biological groups: live hard coral, soft coral and sponges, dead standing coral,17 and marine plants that can be held in the hand is also recorded. Percentage cover is not easy to assess and the shapes in figure 3.36 may help.
Life Forms Present and Dominant. The major types of corals and plants present and dominant are recorded. The main groups are hard corals (fig. 3.37), soft corals and sponges (fig. 3.38), and marine plants (fig. 3.39). The dominant form (the most obvious one which covers the largest area) is noted as is its most common size: about fist-size, about the size or diameter of forearm, or equivalent to outstretched arms.
Benthic Animal Counts. Reef health can be indicated by the presence or absence of certain animals (fig. 3.40). Totals in excess of 20 need only be expressed as >20.
Visible Pollution. Objects to be recorded include cans, bottles, plastic and other synthetic materials; leaves, palm logs, and other land plant debris; and notes should be made on sediment in the water sufficient to reduce visibility, oily film on the water, or tar on rocks and sand, etc.
Figure 3.35. Fish to be recorded: predators (three above) and butterfly fish (three below). Not drawn to scale.
After Dahl 1981a
Other Notes. Other items worth noting are recent storms, nearby developments, proximity of human habitation, signs of fishing, etc.
In addition to the above parameters, temperature, salinity and turbidity should be measured in the different zones, preferably repeated regularly during a tidal cycle.
The data collected on their own are clearly useless without interpretation. Interpretation can either be made from a single survey, or from three or more successive surveys. Small variations between surveys are to be expected since variation is a natural condition and no observer is free from error. Important measures or changes can, however, be interpreted (table 3.8). If significant effects are noticed then survey intervals should be shortened, the results communicated to the appropriate authorities, and experts invited to make independent assessments.
Figure 3.36. Examples of percentage cover.
After Dahl 1981a
Figure 3.37. Forms of hard coral, a - branching, b - staghorn, c - massive, d - encrusting, e - tabulate/flat, f - erect foliose, g - cup-shaped, h -mushroom.
After Dahl 1981 a
Figure 3.38. Forms of soft corals and sponges. Only two forms are distinguished, a - massive, b - fans and whips.
After Dahl 1981a
Figure 3.39. Forms of marine plants, a -thick turf; b - long filaments; c - large browns; d - Halimeda; e - other fleshy plants; f - seagrass.
After Dahl 1981a
Figure 3.40. Benthic animals to be recorded, a - mushroom coral, b - giant clams, c - synaptid sea cucumbers, d - other sea cucumbers, e - Acanthaster, f - other starfish, g - urchins, h - Trochus.
After Dahl 1981a
After Dahl 1981a