Chapter Seven
INTRODUCTION
The lowland forests of Sumatra are among the most diverse, awe-inspiring, complex and exciting ecosystems on Earth. They are probably the best-studied forested natural ecosystem on the island, but for information on how these forests actually function it is frequently necessary to turn elsewhere in the Sunda Region. In many respects, the Sunda Region lags behind tropical America in unravelling and understanding ecological interactions. For this reason, occasional examples are taken from lowland forests in countries such as Costa Rica, when illustrations of particular aspects of ecology are required.
Diversity of Plants
The diversity of tree species in Sumatran lowland forest is extremely high. In a valley area around the River Ranun in North Sumatra, the Simpson Index of Diversity1 for trees of 15 cm diameter and over at breast height was 0.96, and in the neighbouring hills it was 0.93 (from data in MacKinnon [1974]). In a hill forest on Bangka Island investigated by a CRES team, the index of diversity was 0.94. Both studies used local vernacular names which always underestimates actual species number, as explained on page 198. Corresponding figures for a forest in Europe would be much lower, at about 0.4-0.6.
The problem of explaining the very high diversity of plants in tropical forests, particularly lowland forests, has taxed many minds. Before detailed investigations of fossil pollen began about 15 years ago, it was thought that tropical forests had experienced climatic stability for millions of years and this had allowed time for the evolution of many species. This has now been shown to be false as tropical vegetation has experienced considerable changes over time (p. 17). Other writers have suggested that the formation of isolated forest blocks or refuges during the peaks of glacial activity, when climates were cooler and drier, would have resulted in the species of each block following a course of evolution different from species in other blocks. When the climate ameliorated and the forest blocks were reunited, some of the closely related species would be incompatible for reproduction and thus a greater degree of diversity would exist than before the forest blocks were separated. This is generally known as the refuge theory (Haffer 1982) and has been useful in explaining diversity in certain taxa in Amazonia and Africa. It is less satisfying as a theory in Southeast Asia, however, where it is suggested that the whole of Peninsular Malaysia, Sumatra, Borneo and West Java formed one 'refuge' and the majority of New Guinea the other. The refuge theory does not explain all species distributions (Endler 1982) and it is clear that more detailed surveys are required (Meijer 1982a).
Figure 7.1. Relative abundance of tree species near the River Ranun, Dairi. Note that 73% of the species contribute only about 20% of the trees.
After MacKinnon 1977
An ecosystem with high diversity has, by corollary, a large number of rare species (fig. 7.1) so, as Flenley (1980) suggests, instead of asking "why is lowland forest so diverse", we could equally well ask "why are there so many rare species?". Reproductive strategies adopted by living organisms can be described as falling within a spectrum between two extremes: r-selected strategies in which as many offspring are produced as possible, and K-selected strategies in which few offspring are produced but each has a great deal of care, attention and material resources devoted to it in order to ensure its survival and success. Thus elephants, cows and bats are K-selected, and rats, pigs, and many fish and insects are r-selected. If an organism adopts the K-strategy in a lowland forest, it will almost certainly be relatively rare. It is then necessary to ask "under what circumstances can rarity be an advantage?". It is generally true that the herbivores on a plant species in lowland forest are restricted to a few species which have evolved as the plant species evolved and found ways to circumvent whatever forms of physical or chemical defence the plant has adopted (see p. 231). The chances of a pest finding an individual of a particular tree species are greater if that tree is common, and so the pressure exerted by herbivores on an abundant or otherwise dominant tree species puts it at a disadvantage and permits subordinate species to coexist (Janzen 1970).
A hypothesis has been suggested by Ricklefs (1977) that greater heterogeneity in soil properties and surface microclimate in the tropics might be the basis of the trend of increasing tree species diversity from temperate to tropical regions. He proposes that ranges of angle and intensity of incident solar radiation, precipitation, temperature, and the partitioning of nutrients between soil and vegetation are wider in a tropical forest clearing than in a similar clearing in temperate regions. The differences are because:
a) the large biomass of a tropical forest modifies factors such as light levels, humidity, temperature, and environmental constancy to a greater extent than does a temperate forest of smaller biomass;
b) more rapid decomposition of leaf litter and other organic detritus in tropical forests accelerates the release of mineral nutrients and organic detritus from trees and increases the flush of nutrients into the soil (see also Anderson and Swift [1983]);
c) even if nutrient levels in soils under temperate and tropical forests were similar, the humus content of tropical forest soils is lower. Humus content influences the retention of soil moisture and the stability of other soil properties when exposed to more intense physical forces within forest gaps;
d) the higher rainfall of tropical areas increases the leaching of certain ions from exposed soils. This differential leaching would further increase variation across a forest gap;
e) for much of the day the sun is more or less overhead and so the light hits the soil in a tropical forest gap more directly and for a longer time each day than in a temperate forest.
These differences create a greater heterogeneity of environmental conditions for seedling establishment in tropical forests and it is this heterogeneity that provides the basis for resource partitioning and the coexistence of competing species.
The natural rarity of some plant species is compounded because some also are dioecious (bearing flowers of only one sex on one tree) and because many plants are endemic to quite restricted areas. One consequence of this is that reserves hoping to conserve these species have to be extremely large (Ng 1983).
Diversity of Animals
The large number of animal species in lowland forest is generally associated with structural and taxonomic heterogeneity of the plants. The number of animal species is high in Sumatra and other parts of the Sunda Region, but not as high as in other tropical regions. For example, the total number of birds in about 15 ha of primary lowland forest in seven sites is shown in table 7.1 and it is clear that those for sites in the Sunda Region are considerably lower than for South America (Pearson 1982). If exactly equivalent habitats are compared, however, counts of Sunda forest birds are higher than counts in Africa and not far behind South America (D. Wells, pers. comm.).
Significance was achieved, however, when the geological history of the localities was considered in terms of separations from, and connections to, other landmasses. Since islands theoretically have higher extinction rates and lower immigration rates than similar continental areas (p. 46), sites in Borneo, Sumatra, and New Guinea would be expected to have fewer species than sites in tropical continental South America.
Inger (1980) compared the densities of frogs and lizards in lowland forests in Borneo (the data are probably applicable to Sumatra) and Central America. In Borneo about 1.5 individuals were found per 100 m2 but in Central America the figures ranged from 15 to 45. He proposed (as Janzen [1974, 1977a] had done earlier) that the low abundance was due to many major tree species in the Sunda Region exhibiting the phenomenon of gregarious fruiting at long intervals (p. 221). This in turn would reduce the numbers of seed-eating insects available as frog and lizard food. The same argument would apply to other insect-eating animals.
Based on Pearson 1982; figure for Sumatra from Rijksen 1978 and R. Eve and A.M. Gigue, pers. comm., for rather more than 15 ha at the Ketambe Research Station.
VEGETATION
Characteristics
Tropical lowland forests are characterised by the huge amount of plant material they contain, and this can be measured in terms of the amount of carbon present. The tropical forests of the world (i.e., not just lowland forests but also montane, swamp and dry forests) cover 1,838 million ha or 11.5% of the earth's land surface, yet they contain 46% of the living terrestrial carbon (Brown and Lugo 1982). The type of lowland forest found in Sumatra would certainly contain an even more disproportionate percentage of the carbon. Of the total of organic matter in a lowland forest, only about 1% is accounted for by the litter, about 40% by the soil, but about 60% is in the vegetation (Brown and Lugo 1982). In temperate regions the corresponding biomass figures are about 10%-20%, 35% and 50%.
Lowland forests are characterised by the conspicuous presence of thick climbers, large buttressed trees, and the prevalence of trees with tall, smooth-barked trunks. Although the canopy may occasionally be dominated by small-leaved leguminous trees (such as the magnificent Koompasia excelsa and K. malaccensis), the vast majority of trees have simple mesophyll-sized leaves (p. 283) between 8 and 24 cm long. The leaves of understorey trees, including the immature individuals of large trees, often have larger leaves (Parkhurst and Loucks 1972).
Leaves with smooth edges and 'drip-tips' (fig. 7.2) are particularly common in lowland forest and there is considerable convergence between plant families in leaf shape which, together with the high diversity of species, frequently makes identification somewhat difficult. Even so, characters such as sap, type of bark, size of buttresses, leaf vein arrangement and arrangement of leaves on twigs give ample information to allow identification of the majority of specimens, even without flowers. For a convenient key see Wyatt-Smith and Kochummen (1979) but see page 198 for cautions. Since plant taxonomy is based on flower anatomy, final identification relies on the examination of flowers.
The drip-tips are most prevalent in understorey saplings. Since one theory of the function of drip-tips is that they allow water to run easily off the leaf surface and thus prevent or hinder the growth of epiphylls (p. 210), it is reasonable that these should be most common where the relative humidity is highest (i.e., rates of evaporation lowest).
Forest Growth Cycle
Different types of tropical rain forests, and indeed forests throughout the world, have many fundamental similarities because the processes of forest succession and the range of ecological strategies of tree species are more or less the same (Whitmore 1982a, 1984). These strategies form what is known as the forest growth cycle; that is, the events of a large mature tree falling over in a closed forest, forming a gap, the gap filling with a succession of plant species until another large mature tree falls over. Vigorous, light-tolerant (shade-intolerant) species grow up in the gap and these create favourable conditions for seeds of shade-tolerant (but not necessarily light-intolerant) tree species to germinate and for the seedlings to grow and eventually to supersede the initial gap fillers. The process leading from a gap to mature forest is known as secondary succession. Whitmore divides the cycle into three phases - the gap, building and mature phases -which together form a mosaic throughout the forest which is continually changing in state and shape (Whitmore 1982a, 1984) (figs. 7.3. and 7.4).
Figure 7.2. Leaves of a) Dialium platysepalum, b) Dracontomelon mangiferum, and c) Sterculia foetida to show drip-tips characteristic of many lowland forest trees.
For example, a patch of forest in building phase may return to gap phase should a tree in a neighbouring mature patch fall across it. The size of a gap depends on its cause - from the falling of a single dead tree, to a landslide, a fire, or even a widespread drought. The floristic composition of a forest will depend on the size of former gaps because a large gap will be filled initially with tree species requiring light, whereas small gaps will be filled by shade-tolerant tree species. Many of the latter may have grown slowly for many years to become part of the understorey but have been unable to form part of the main canopy until a small gap was formed. It should be noted that since a single tree can contribute to gap, building, and mature phases, it is incorrect to refer to 'gap-phase' or any other phase species (Whitmore 1982a). Terms which describe the behaviour of a species, such as pioneer, shade-tolerant or light-intolerant, are more useful. Since forest comprises a mosaic of gap, building and mature areas, it is a matter of debate whether the term 'climax' vegetation has any meaning in the field.
Figure 7.3. Mosaic of a) gap, b) building and c) mature phases at S. Menyala, Peninsular Malaysia. The extensive area of building phase was caused by partial clearance in 1917.
After Whitmore 1984
Figure 7.4. Gaps near the River Pesisip, Batang Hari, formed within 10 years preceding the study of Huc and Rosalina (1981b).
Gaps and their plants have been studied in Sumatra at various locations in West Sumatra, Jambi, South Sumatra and Lampung by Huc (1981) and Huc and Rosalina (1981b). They concluded that the size of gaps influences the duration of the forest growth cycle. Small gaps created by dead standing trees produced short cycles without a gap phase. That is, immature trees beneath the dead tree were able to grow up as soon as the light intensity increased. Large gaps created by the fall of several adjacent large trees allowed the full growth cycle to occur (fig. 7.5). Huc and Rosalina's findings confirmed those of Kramer (1933) on the slopes of Mt Gede. Kramer made artificial clearings of 1,000, 2,000, and 3,000 m2. The first was soon filled by regenerating mature-forest trees but the larger clearings were swamped by vigorous pioneer species. This has also been observed in Mount Leuser National Park by Rijksen (1978). Huc and Rosalina (1981) calculated that the average duration of the growth cycle in the forests they examined was about 117 years, and at Ketambe Research Station an approximate duration of 108 years has been estimated by van Noordwijk and van Schaik (pers. comm.). These results are comparable to estimates ranging from 80 to 138 years in Costa Rica (Hartshorn 1978) but rather less than the 250 to 375 years estimated by Poore (1968) for part of Peninsular Malaysia.
Within each of the different stages of the forest growth cycle the trees which are found have a number of ecological characteristics in common. For example, the first species that grow up in a gap (often called pioneer species) generally produce large numbers of small seeds frequently, if not continuously. These seeds tend to be easily dispersed (often by wind, squirrels or birds) and, probably because of this, these species tend to have wide geographical distributions (Huc 1981). They have high viability even in full light, and the seedlings grow rapidly. In addition, these species are often dioecious (each plant bearing flowers of only one sex), which leads to considerable genetic variability. An index of the pioneering ability of different species has been devised (Sakai et al. 1979).
The trees of later stages in the succession are shade-bearers (that is, they tolerate growing in shade, but if more light is available they will grow faster) and can regenerate beneath their living parents. These species often have large seeds with rather specialised means of dispersal and a relatively restricted geographical distribution. Between these two extremes are large numbers of species of 'late-secondary growth' which are unable either to colonise open sites or to regenerate beneath their living parents (Whitmore 1982a, 1984).
Figure 7.5. Silvigenetic cycles. 1, 2 and 3 are short cycles due to the replacement of dead trees by trees below, with no gap formation. 4 is a long cycle due to the formation of a gap in which pioneer vegetation grows, a, b and c represent pioneer-, building-, and mature-phase forest.
After Huc and Rosalina 1981
Changes in species composition during succession may be due to availability of nutrients, availability of seeds, suppression of some species by chemicals produced by the same or other species (allelopathy), crown competition or root competition (Huc 1981), but there is still very little information available on how regeneration actually occurs. There are three ways in which trees can grow: from shoots growing out of roots, stumps or fallen trunks, from established seedlings, or from seeds. Beneath a mature forest there are clearly no seedlings of light-demanding species and, conversely, in gaps light-intolerant species will die. Seed may lie dormant in or on the soil surface (seed bank), or it can be brought into an area in the 'seed rain' (seeds dispersed from their parents). The existence of seed banks in rain forest in northern Thailand has been demonstrated by Cheke et al. (1979). They found dormant, viable seeds of pioneer species such as Trema, Mallotus, Macaranga, Melastoma and grasses in locations where those species were not represented. Similar findings are reported from Peninsular Malaysia (Liew 1973; Ng 1980; Symington 1933). Some of the seeds that were found 20 cm below the soil surface were still able to germinate although they must have arrived many years before. In addition, a long period of dormancy for these seeds is suggested by the low rate of seed input and the large numbers of seeds found.
Whereas trees of the gap and early building phases may have seeds which can lie dormant for many years, this is not so for many of the trees of the mature phase. These tend to fruit infrequently (p. 219), to have poor dispersal and little or no potential for extended dormancy. Their continued existence in an area therefore depends on fruit from mature trees falling into a spot with the correct conditions for immediate germination. Dipterocarpaceae trees fall into this category. Secondary succession is discussed further on page 340.
Floristic Composition and Variation
As was stated in the introduction to Part B, the lowland forests of West Malesia (p. 44) are amongst the most diverse and species-rich ecosystems in the world. Vernacular names allow differentiation of some of the trees and represent a common and useful means of conducting a general forest survey (MacKinnon 1974; Rijksen 1978; Whitten 1980b). It should, however, be realised that vernacular or commercial names generally greatly underestimate the number of species present. For example, 'meranti' describes the genus Shorea but the 'specific' names such as 'meranti merah', 'meranti putih' and 'meranti damar hitam' each represent a group of species. For example, in Sumatra there are over 26 true species of 'meranti merah' (W. Meijer, pers. comm.).
Most types of forest formation in West Malesia are dominated by a single family of tree called Dipterocarpaceae (fig. 7.6). These are the only forests in the world in which a single family has such a high density of genera, species and individuals (Whitmore 1982a, 1984). This domination is usually, but not always, particularly marked in lowland forests. Sumatra has 112 species of dipterocarps including 11 endemic species (Ashton 1982).
The emergent trees in Sumatran lowland forest, some of which can reach 70 m tall, are generally of the families Dipterocarpaceae (e.g., Dipterocarpus, Parashorea, Shorea, Dryobalanops) and Caesalpiniaceae (formerly part of Leguminosae) (e.g., Koompasia, Sindora and Dialium). An extensive and interesting enumeration of large trees in part of Peninsular Malaysia was conducted by Whitmore (1973). For identification of large and medium-sized trees see Meijer (1974), Symington (1943) and Wyatt-Smith and Kochummen (1979). It must be remembered that the last two of these books were written for Peninsular Malaysia, and although most Sumatran tree species are included, an unknown tree may be one of the ones that is not. It is generally quite satisfying to identify a tree to its genus.
Figure 7.6. Fruits of live Sumatran dipterocarp trees: a) Shorea assamica, b) Hopea ferruginea, c) Vatica maingayi, d) Dipterocarpus cornutus, and e) Dipterocarpus palembanicus.
After Symington 1943
Common families for the smaller trees are Burseraceae, Sapotaceae, Euphorbiaceae, Rubiaceae, Annonaceae, Lauraceae, Myristicaceae and smaller species of Dipterocarpaceae, but some will also be immature emergents.
Dipterocarp trees dominate much of the lowland forests of Sumatra. For example, on the hill ridges examined on Siberut Island, between 20% and 59% of all trees over 15 cm diameter at breast height were dipterocarps; Myristicaceae, Euphorbiaceae and Sapotaceae were the next most common families. On level ground between the ridges, Euphorbiaceae, Dipterocarpaceae and Myristicaceae ranked more or less first equal (Whitten 1982e). Other families may be dominant, however, such as at the Ketambe Research Station where Meliaceae accounts for 17% of the trees over 10 cm diameter and dipterocarps are not particularly common, accounting for only 4% of the trees (LBN 1983; Rijksen 1978). Near the Pesisip River, Batang Hari, the dominant families are Dipterocarpaceae and Olaceae (particularly Scorodocarpus borneensis) (Franken and Roos 1981).
Numerous surveys of Sumatra's lowland forests have been conducted for forestry evaluations but these are of limited use for ecological work because:
• they enumerate only those trees providing profitable timber, and
• they concentrate on areas where timber trees are likely to be most common.
Variation in the floristic composition of a given phase in the growth cycle of lowland forest can be quite considerable, but because the variation is often continuous (that is, there are no sharp boundaries, forest of one composition changes gradually into forest with another composition), it is very hard to study. Poore (1968) was of the opinion that floristic composition was largely determined by chance factors, particularly at the times of fruit dispersal and seedling establishment. Within a given area, however, composition is related to large-scale habitat features such as soils and topography (Ashton 1976; Baillie and Ashton 1983; Franken and Roos 1981). A detailed study of species composition and various soil and other site variables in Sarawak showed that soil texture, levels of iron and aluminium oxides, and the acidity of the soil parent material were the most important factors determining species composition (Baillie and Ashton 1983). These effects are very subtle and occur more as a variation in the relative abundance of different species rather than as the presence or absence of one or more species. This is partly because a particular soil type will not always exclude ill-adapted species, but adults of such species will be relatively rare and have reduced vigour. The minor variations between the forest type studied on Siberut Island were sufficiently clear to the gibbons occupying the area for it to be possible to detect differences in their behaviour and activity between the various forest types (Whitten 1982c,d).
A particularly noticeable variation in lowland forest occurs along streams, and certain tree species tend to be restricted to these areas. Below these trees, alongside fast-flowing rivers, rheophytes (river-plants) can be found. These are usually shrubs which, although diverse taxonomically, have narrow leaves and often brightly coloured fruits dispersed by either water or fish (Jacobs 1981; van Steenis 1952, 1978; Whitmore 1984).
Layering
The canopies of forest trees are often said to form several (usually three) 'layers'. While this is a convenient theoretical concept it has limited application in the field. An emergent layer is often quite clear but below that the supposed layers may be difficult to distinguish. Some trees may clearly belong to a particular layer but many more are generally indefinable. Part of the difficulty in applying the concept of layering lies in the existence of the mosaic of gap, building and mature phases in the forest (p. 193), each of which is in a dynamic flux. In an analysis of various forest types on Siberut Island, each of the 2,459 trees along 11.5 ha of 20 m wide transects was scored for the position of its crown relative to the neighbouring canopy. 'Emergence' (defined as 0%-25% of the crown in contact or enclosed by other crowns) did not correlate with tree height because, within a large area in building phase, a medium-sized tree can be emergent, and in mature forest a 40 m high tree can be more or less completely enclosed by taller trees (Whitten 1982c).
Figure 7.7. Mature and building phases at Belalong, Brunei. Dipterocarps are shaded - note that in the building phase these have the tall, monopodial crown of youth.
After Ashton 1964, in Whitmore 1984, in which the identification of each tree is given
The shape of tree crowns changes as the trees grow and thus a certain amount of layering of crown shape occurs. Young trees tend to have monopodial stems (that is, a single main stem) and the crown is tall and narrow around that stem. Mature trees, however, tend to be sympodial (that is, without a single main stem) at the canopy level. This difference is shown in figure 7.7. Layering is discussed more fully by Whitmore (1984) and Richards (1983).
Basal Area
The basal area for trees of 15 cm diameter and over at breast height in seven lowland forest types on Siberut Island ranged from 16 to 42 m2/ha. The tree palm Oncosperma horridum was most common in the forest types with the lowest basal area of trees, and when this species was added, the range decreased to 23-42 m2/ha. It was suggested that the inclusion of all other woody plants (e.g., small trees, other palms, shrubs and climbers) in the basal area calculation would have resulted in the basal area of the forest types becoming very similar (Whitten 1982c). The basal area of trees in 171/4 -ha plots at Ketambe Research Station was 16-45 m/ha (van Noordwijk and van Schaik, pers. comm.) and near the Pesisip River, Batang Hari, was 27.9 m2/ha (Huc and Rosalina 1981). Two adjacent forest areas of 0.5 ha examined by a CRES team on Bangka Island had basal areas equivalent to 24.7 and 25.7 m2/ha.
Biomass
The above-ground biomass of two areas of Pasoh Forest Reserve in Peninsular Malaysia was estimated using destructive sampling (felling, cutting and weighing) by Kato et al. (1978). The results were 475 and 664 t/ha. Ogawa et al. (1965) have estimated root biomass as one-tenth of above-ground biomass and so Kato et al. (1978) suggest that average total plant biomass for the Pasoh Forest Reserve was 500-550 t/ha. The changes in biomass with height above ground are shown in figure 7.8. The total plant biomass increment was found to be about 7 t/ha/yr. The ratio between leaf area and leaf dry weight (sometimes known as mean specific leaf area) varied with height above the ground; it decreased steadily from 13 m2/kg in ground-layer seedlings to 7 m2/kg in the tallest trees, showing that leaves are generally thicker in the higher parts of the canopy.
Leaf Area Index
Leaf area index (total leaf area perpendicularly above a unit area of ground) was measured at Pasoh Forest Reserve in different height categories (fig. 7.9) (Kato et al. 1978). It was relatively constant between 10 and 35 m and the increase below this was caused by the plants in the shrub and herb layers. There were relatively few leaves between 5 and 10 m, and leaves of climbers maintained a surprisingly constant contribution (average 10%). The total leaf area index in the two destructive plots was 7.15 and 7.99 m/ha.
Litter Production
Litter production has been investigated at Ketambe Research Station and by teams from the National Biological Institute (LBN 1983) and by van Noordwijk and van Schaik. The second study indicates that 4.7-8.3 t/ha/yr of leaves and 2.2-5.9 t/ha/yr of other litterfall. Litter production was lower in forests with lower pH (lower fertility) (van Noordwijk and van Schaik 1983, in prep). Yearly production of all small litter (twigs, branches and leaves) at Pasoh Forest Reserve was found to be between 7.5 and 10.6 t/ha/yr (Lim 1978; Ogawa 1978) with a likely average of 9.0 t/ha/yr. Similar values were obtained in lowland forest in Sarawak (Proctor et al. 1983) and East Kalimantan (Kartawinata et al. 1981). The proportion of the litter in different forms at Pasoh was as follows: leaves 72%, twigs 17%, fruit and flower parts 6%, other 5% (Lim 1978). Ogawa (1978) found that the annual leaf fall (6.5 t/ha) was less than the leaf biomass (8 t/ha) and thus calculated the mean life of the leaves to be 15.2 months. Litter usually accounts for only 1% of the organic carbon in a lowland forest compared with about 20% in a European forest (Brown and Lugo 1982).
Figure 7.8. Vertical distribution of leaf and wood biomass density in a plot at Pasoh Forest Reserve, Peninsular Malaysia.
After Kato et al. 1978
Figure 7.9. Vertical distribution of leaf area index in a plot at Pasoh Forest Reserve, Peninsular Malaysia.
After Kato et al. 1978
Figure 7.10. Lowland forest on Siberut Island, West Sumatra, showing many young rattans and the abundance of the spiny tree palm Oncosperma horridum.
Total Primary Production
Very few studies of total forest primary production (p. 86) have been conducted anywhere in the Sunda Region, largely because of the many methodological difficulties involved (Whitmore 1984). At Pasoh Forest Reserve three methods were used (Kira 1978; Koyama 1978; Yoda 1978a; Yoda and Kira 1982). The results suggested a net primary productivity of 25-50 t/ha/yr and a gross primary productivity of 70-100 t/ha/yr. Kato et al. (1978) remark that the net primary productivity is lower than for rubber and oil palm plantations. As was described on page 86, however, a mature forest would be expected to have a lower productivity than a managed, growing forest or an agricultural plantation.
Mineral Cycling
Cycling of minerals through a lowland forest has not been investigated in its entirety in the Sunda Region, but relevant papers have been written on various stages of the cycle (Anderson et al. 1983; Lim 1978; Manokaran 1978, 1980; Ogawa 1978; Yoda 1978a, 1978b; Yoda and Kira 1982; Yoneda et al. 1978). A review of mineral cycling in tropical forests has recently been published (Vitousek 1984). See page 296 for details of a study of mineral cycling in a lower montane forest.
ECOLOGY OF SOME FOREST COMPONENTS
Roots
A relatively small proportion of the organic carbon and other nutrients in a lowland forest is in the soil. Organisms such as fungi, bacteria, soil animals and roots therefore compete for what are probably limiting resources. It appears that almost all trees in lowland forests and almost all non-grain crops can develop a mutualistic relationship between their roots and fungi (Janos 1980a). This is called a mycorrhiza. The most common form found in the tropics has the hyphae ('root' strands) of the fungus penetrating the plant's roots, where they take up carbohydrates from the plant. For its part the fungus channels minerals into the roots (Janos 1980b, 1983). Many plant species with mycorrhiza appear not to possess root hairs because these structures are improved upon by the mycorrhizae. Mycorrhizae are probably common among trees in heath forest (p. 255), but are poorly developed among plants of early successional stages which normally grow on soil enriched from fire ash, deposits left by flood water, or the decomposition products of fallen trees (Janzen 1975). In such situations a plant would be at a disadvantage if it had to wait for its roots to be infected with fungus before it could start growing and competing (Janos 1980b, 1983). Some species cannot grow without mycorrhizae, whereas others grow better without mycorrhizae where mineral nutrients are not limited, but better with mycorrhizae in poor soils (Janos 1980a, 1983). For trees that depend on mycorrhizae it is advantageous for their fruit to have large seed reserves because they provide a source of food for the seedling before infection with fungus occurs. It is not surprising, then, that seedlings kept experimentally without mycorrhizae, stopped or slowed their growth after attaining a size correlated with the average dry weight of a seed for that species (Janos 1980b).
Buttresses and Trunks
Buttresses are common features of trees in lowland forest. Setten (1953) found that 41% of 18,067 large ('timber-sized') trees in a forest in Peninsular Malaysia had buttresses reaching more than 1.35 m up the trunk. Different species are relatively constant in the presence, shape and surface characteristics of buttresses and these characters can be helpful in identification (Wyatt-Smith and 1979).
Buttresses are sometimes said to act as structural supports for trees whose roots are relatively shallow and where the substrate affords little anchorage (Henwood 1973; Smith 1972). They are also said to be composed of 'tension wood' to reduce the pulling strain on the roots and so would be expected to form on the uphill side of a trunk, on the side of a trunk opposite a major congregation of heavy climbers, or on the side the wind blows from - that is, on the 'tension' side. From subjective impressions, however, it is clear that some trees do not 'obey' the rules and instead form buttresses on the 'compression' side of the trunk; see, for example, photographs by Corner (1978). In addition, of course, many trees grow well in similar conditions without buttresses.
Recent hypotheses on buttress formation have been unrelated to structural problems. It has been suggested, for example, than since buttresses increase the space of forest floor occupied by an individual tree, they could be viewed as a competitive mechanism (Black and Harper 1979). The physical presence of a buttress prevents or hinders the establishment of neighbouring (i.e., competing) trees. If this hypothesis is correct then it should be possible to observe that:
• the density of trees near a buttressed tree are less than near a tree of similar bole size, canopy form and age without buttresses;
• the distance to the nearest neighbours of buttressed trees are greater on the average than from a non-buttressed tree to its nearest neighbours;
• the density of trees around different individuals of a buttress-forming species bear a relationship to the age of the individual trees. Older buttressed trees should have both more distant and fewer neighbours in the smaller size classes;
• species diversity of trees around a buttressed tree are lower than around a non-buttressed tree because some species are likely to be less competitive against buttresses than others (Black and Harper 1979).
These hypotheses need testing, and collecting appropriate data does not require in-depth botanical knowledge.
Trees with rotten, empty trunks are surprisingly common in lowland forest. This may appear to be unfortunate for the tree but it has been suggested that it is in fact a strategy of distinct advantage. Empty cores of large trees are inhabited by bats, porcupines and rats in addition to a host of invertebrates. Faeces and other products from these animals are broken down by microbes and thus provide an exclusive supply of nutrients for the tree in a generally nutrient-poor environment (Fisher 1976; Janzen 1976a).
It is not generally known that tree trunks exhibit a daily fluctuation in girth, being largest in the early morning and smallest in the late afternoon. These changes are presumably caused by water being drawn out of the plant by evapotranspiration during the day. Although measurable, the changes are very small, being in the region of 0.1 mm around an average timber tree (Yoda and Sato 1975).
Climbing Plants
Climbing plants abound in many types of lowland forest. The crown of a large climber may be as large as that of a tree but because (with the exception of rattan) they do not possess any real commercial value, they have been little studied. Identifying climbers is very difficult but the coiled or convoluted ones with flattened stem sides are generally leguminous species, and the ones with regular hoops around the stem are members of the Gnetaceae, relatives of the conifers. The best-known member of the Gnetaceae in Sumatra is the tree Gnetum gnemon from which emping crisps are made, but almost all members of the family are climbers.
When young, many species of tree-hanging climbers in the forest understorey can look very similar to young trees as they grow slowly, waiting for an opportunity to rise to the canopy. Such opportunities are afforded when a gap is formed, and it is then that a young climber can attach itself to a rapidly growing tree and be carried upwards. During a similar period of apparent dormancy, some species are growing a large tuber below ground. In response to a particular cue the energy available in the tuber is suddenly used up in a rapid burst of upward growth, whether or not a gap has formed (Janzen 1975). Some climbers, such as rattans, have elaborate hooks by which they can climb their own way to the light at the top of the canopy. Other climbers begin to coil their way up their chosen host as soon as they have germinated. Some species have populations which coil in a left-handed manner in the northern hemisphere, and in a right-handed manner in the southern hemisphere so as to make most efficient use of the sun's rays (Janzen 1975). It would be interesting to know whether this phenomenon exists in Sumatra, which is more or less equally divided by the equator.
The stems of climbers can sometimes be seen to loop down towards the forest floor and back again, indicating that the major bough or the whole tree supporting the climber may have fallen and the climber then grew up again. Mature climbers are rarely supported by a single tree but rather grow horizontally through the canopy, sewing together the tree crowns. This may help to prevent trees from falling over in strong winds but, if a tree is felled, the climbers in its crown often pull over other trees as well (p. 366).
A considerable portion of the apparent 'seedlings' of climbers (and a certain proportion for some forest trees) are in fact no more than shoots growing up from a horizontal root of an established climber (Janzen 1975). This is a means by which a plant can increase the size of its crown, and since these shoots are obviously genetically identical to their 'parent', the actual number of genetically distinct individuals in a given area may be extremely low.
Climbers compete with trees for light, nutrients and water and can cause mechanical damage to trees. In well-managed production forest this is the reason climber stems are cut (see p. 366). In addition, bole diameter is often greater than average for trees with heavy climbers in their crown, indicating that trees have to divert resources away from vertical growth and reproduction in order to increase the strength of the supporting structure (Whitten, unpubl.). Where climbers are abundant, regeneration of trees can be seriously delayed, and so for all these reasons it is an advantage to a tree to shed or to avoid climbers.
Figure 7.11. Lowland forest near Kebamse, Mount Leuser National Park.
A.J. Whitten
Fast-growing trees are better able to avoid climbers than are slow-growing trees. Trees which are able to rapidly increase their bole diameter as well as their height are also more likely to escape certain climbers which coil up the stem, because such climbers are limited in the diameter of support they can ascend. Rapid increase in girth can also break potentially strangling plants. Some trees exhibiting a symbiotic relationship with ants (such as Macaranga, p. 376) may benefit from the ants removing vines from the branches as they have been shown to do in Central America (Janzen 1973a). Other strategies used by trees to avoid climbers are suggested by Putz (1980).
Epiphytes and Epiphylls
An epiphyte is a perennial plant rooted upon, not in, a larger host, and one which does not have to produce or maintain massive woody stems and branches to live above the forest floor. Epiphytes are common in lowland forest, but even more common in certain montane and heath forests (pp. 257 and 284), and they are thought to make a significant contribution to the totals of biomass and species-richness in a forest (Benzing 1983). The major higher plant families of epiphytes in Sumatra are Gesneriaceae, Melastomaceae, Rubiaceae (including the ant-plants Myrmecodia and Hydnophytum), Asclepiadaceae and Orchidaceae. In addition to these are numerous epiphytic ferns, lichens and bryophytes (including mosses and liverworts).
Bryophytes are small but common epiphytes in lowland forest. Their small size makes them less restricted than other plants in the range of micro-habitats they can occupy, and these are shown in figure 7.12. The most luxuriant bryophyte communities in wet lowland forest are generally found on the bases of large trees (see Pócs [1982] for detailed descriptions).
Epiphytes might seem to have an easy life but they live on a substrate which is extremely poor in nutrients. Most of them rely upon nutrients dissolved in rain, a small amount of litterfall, and occasional mineral inputs from animals. Epiphytes also have to contend with a very erratic water supply - being drenched when it rains, and parched when the sun is shining and the wind is blowing (Janzen 1975).
Epiphytes cope with growing in nutrient-poor conditions in various ways (although few species will exhibit all these features):
Figure 7.12. Bryophyte microhabitats in a lowland forest. 1. bases of large trees, 2. upper parts of trunks, 3. macro-epiphyte 'nests', 4. bark of main branches, 5. terminal twigs and leaves, 6. bark of climbers, shrub branches and thin trunks, 7. pandan stem, 8. tree-fern stems, 9. palm trunks, 10. rotting trunks, 11. soil surface and termite mounds, 12. roadside cuttings, 13. rocks and stones, 14. submerged or emergent rocks in streams.
After Pocs 1982
• their own tissues may have very low nutrient concentrations;
• juvenile stages are prolonged even though little growth is required to become mature;
• their vegetative parts are reduced in size;
• they may obtain nutrients from unconventional sources such as ants;
• their leaves tend to be long-lasting (due perhaps to some form of defence against herbivores) so that the replacement of nutrient-expensive leaves is required only infrequently; and their flowers are pollinated by animals because wind dispersal of the pollen would result in 'expensive' losses (Benzing 1983).
Figure 7.13. Taeniophyllum, an example of a leafless orchid.
In addition, it has been observed that some epiphytes concentrate their roots on the underside of boughs where water and nutrients would remain longest (Whitten 1981).
The third strategy, vegetative reduction, has been studied by Benzing and Ott (1981). They investigated three species of shoot-less orchid; that is, orchids with no leaves and a shoot which merely initiates roots and produces occasional flowers (fig. 7.13). It was found that these orchid roots were green in colour and that they were capable of fixing carbon in their tissues, whereas roots of normal, leafy orchids, while able to photosynthesise, were unable to exhibit a net gain of carbon. Benzing and Ott consider that the shootless habit, by reducing the 'cost' of the vegetative body, has evolved for reasons of nutrient economy so that maximum nutrient resources can be directed towards reproductive effort.
As Janzen (1975) has pointed out, epiphyte leaves seem to suffer very little damage from herbivores, and he further suggests that these valuable leaves may be defended chemically to prevent their loss. There appears to be no data yet to confirm this. Some epiphytes, notably Myrmecodia (p. 257), harbour ants in their stems and these may well protect their leaves from caterpillars and other arthropod herbivores. It seems unlikely that the succulent leaves of Myrmecodia contain concentrations of chemical defences because on Siberut Island, Mentawai gibbons, whose diet indicated a marked avoidance of potential sources of defence compounds, ate Myrmecodia leaves (Whitten 1982b,e). Myrmecodia on Siberut Island appeared to grow further away from the tree trunks than other species and it may have been helped in such extreme habitats by the nutrients provided through its relationship with ants (Whitten 1981). Although epiphytes (by definition) do not take nutrients directly from the host plant, they have been called 'nutritional pirates' (Benzing 1981, 1983).
This is because they can tie up nutrients in their own biomass from dust, leaf leachates and rain which would otherwise have fallen onto the soil to be utilised by the hosts. While this is true, Nadkarni (1981) has found that host trees can turn the tables at least partially back in their favour by producing small roots beneath the mats of dead and living epiphyte tissue. These roots thus give the tree access to canopy nutrient sources. The main boughs of some tree species are almost invariably covered with epiphytes but it would appear that other species actively deter epiphyte growth, presumably because the relationship is disadvantageous. Thus, on Siberut Island, Sterculia macrophylla were always laden with epiphytes but Endospermum malaccensis bore none (Whitten 1981).
Epiphylls are mosses, liverworts, algae and lichens which grow on the living surface of leaves in shady situations where the air is almost continually saturated. Thus they are generally restricted to the leaves of young trees, shrubs and long-lived herbs of the lowest layer of forest up to about 2-3 m and also near streams. Over 10 species of epiphylls can occur on a single leaf and some of these are obligate; that is, they are found only on leaves (Pócs 1982). Epiphylls are restricted to certain types of leaves and are possibly more common on leaves lacking drip-tips (p. 194).
Gaps
Pioneer plants (p. 196) are generally thought to be low in defensive compounds; their growth strategy is to grow and reproduce quickly because, in the nature of succession, they are limited in both space and time. Resources are not diverted into possibly unnecessary defence. Plants growing in gaps, the location of which is unpredictable, are able to avoid herbivores partly through that unpredictability of occurrence and partly through relatively short life cycles (Janzen 1975). Maiorana (1981) noticed that some species growing in shaded habitats suffered more from being eaten than did the same species in open habitats. Strangely, when leaves from both habitats were presented to snails, generalist herbivores frequently used in palatability experiments (Edwards and Wratten 1982; Wratten et al. 1981), it was found that the plants from open areas were preferred. It is suggested that the 'defence' used by pioneer plants might in fact be the hot, unshaded, low humidity of the gap environment itself.
The fast-growing and often succulent plants of lowland forest gaps are food for the larger herbivorous mammals such as deer, tapir and elephant (p. 373). Studies of birds in forest gaps indicated that the number of species caught in nets in gaps was greater than those caught in surrounding forest (Schemske and Brokaw 1981), perhaps because forest birds cross gaps to reach areas of forest but birds of gaps rarely enter forest.
As described on page 194, gaps experience considerable differences in microclimate compared with mature forest (Ricklefs 1977) and this is reflected in the behaviour of some animals which are found in both habitats. For example, the orientation of webs of one spider species was found to be north/south in closed habitats and east/west in open habitats. The longer a spider spends on the web, the more prey it captures (some prey manage to wriggle loose before being killed by the spider), and so presumably an orientation is chosen to allow maximum time on the web. Web orientation seems to be related to the body temperature of the spiders because both too little and too much heat can affect spider activity. Thus, in open habitats, the spiders' webs face east/west to reduce heat load and in closed habitats face north/south to increase body temperature (Biere and Uetz 1981).
Figs
Fig plants exhibit numerous interesting characteristics (e.g., the strangling habit of some species - figure 7.14) and represent an extremely important source of food for many forest animals. Fig plants are, however, probably most interesting for the way in which pollination is effected.
According to botanical terminology, figs are syconia, not fruit, but ecologically they are fruit and so that noun is retained (Janzen 1979d). The wall of flowers arches over and around so that the flowers are inside a small, almost entirely enclosed, cup (fig. 7.15). The hole at the end of a fig is partially closed by scales formed by bracts.
Fig flowers are pollinated exclusively by tiny (±1 mm) fig-wasps (Agaonidae) (fig. 7.16), and both figs and wasps are entirely dependent on each other for their survival. In addition, one species of fig plant (and there are about 100 species in Sumatra [Corner 1962]) will generally have only one species of pollinator wasp. The female flowers develop first and female wasps fly to the figs, probably attracted by smell. One or more females climb inside the fig by forcing their way through the scales and in the process lose their wings and antennae. Once inside, a female pushes her ovipositor down into the ovary of one of the female flowers and lays an egg. It used to be thought (Corner 1952; Galil 1977) that females oviposited in ovaries of flowers specifically intended for developing larvae but various authors have shown that this is not so (Janzen 1979d). During oviposition and as she moves around inside of the fig, the female deposits pollen from the flowers where she hatched onto other flowers and so effects pollination. Thus although the wasps pollinate the flowers, they are also seed 'predators'. Janzen (1978b, 1979b) found that in a sample of 160 figs from four species, 98% of the figs had more than 30% of their potential seeds killed by pollinating wasps. The larvae develop and pupate and the wingless males emerge first. They search for female pupae and fertilise them before they emerge.
Figure 7.14. One means by which a strangling fig forms. A bird, squirrel or monkey deposits a seed in the crown of a tree. A small bush grows, from which a long root descends to the ground. Side roots then form and grow around the trunk, joining where they meet. The supporting tree eventually becomes encased in a basket of roots which eventually strangle the host to death. In time the fig will stand like a tree with a hollow trunk.
After Corner 7952
Janzen (1979c) found that most figs are only entered by one or two females. This means that there is a very high probability of brothers and sisters mating, a situation avoided in most other organisms. The males' role is not yet completed because they then make a tunnel through the fig to the outside. The carbon dioxide level inside the fig is about 10%, but when the hole is made the concentration drops to atmospheric levels (i.e., 0.03%). This change appears to stimulate the development of the male flowers, the emergence of the females and the process of ripening. In some species the females fly out through the tunnel made by the males and in other species both males and females eat away the scales at the fig entrance. Either way, the females fly off carrying pollen in search of a developing fig; and so the cycle continues. The males die within the fig.
Figure 7.15. A cross-section through a fig fruit showing the ring of male flowers (arrowed) around the end, and the bract scales partially closing the opening.
After Corner 1952
Figure 7.16. Fig-wasps; female above, male below.
Figure 7.17. Fig-wasps' wasp parasite.
After Corner 1952
Not all the insects emerging from a fig are fig-wasps because small parasitic wasps oviposit from the outside of the fig into developing fig-wasp larva. How they locate a larva without seeing it is unknown. The story is further complicated by some of the parasites being parasitised themselves by other wasps (fig. 7.17).
Rafflesia
One of the best-known wild flowers in Sumatra is Rafflesia, although it is rarely seen by most people except in photographs. It is a member of the family Rafflesiaceae which includes two other peculiar flowers found in Sumatra, Rhizanthes and Mitrasternon (Palm 1934; Meijer 1997). Sumatra has six species of Rafflesia: R. arnoldii (the largest flower in the world) throughout (Brown 1822, 1845; Justessen 1922), R. gadutensis, endemic, found in west central Sumatra, R. hasseltii found in central Sumatra, R. micropylora, endemic in Aceh, R. patma in southern Sumatra, and R. rochussenii in northern Sumatra (Meijer 1997). Rafflesia occurs mainly in lowland forest but van Steenis (1972) reports finding one at 1,800 m on Mount Lembuh, Aceh.
Rafflesia is exceptional not just because of its size but because it is the most specialised of all parasitic plants— it has no stem, leaves or roots. Apart from the flower, the plant consists of only strands of tissue growing inside the stem and larger roots of a few species of Tetrastigma climbers (family Vitaceae). Flower buds form on the stem and, for R. arnoldii, take about 19-21 months before they open as flowers. R arnoldii buds of 10 cm diameter will take about five months to flower, of 15 cm diameter two to three months, and of 25 cm 20 to 30 days (Meijer 1958). There appears to be no evidence for seasonal flowering but this has not been investigated in detail.
Figure 7.18. Cross-section of Rafflesia arnoldii on a Tetrastigma root. Arrow indicates location of sexual parts.
After Meijer 1958
When Rafflesia flowers open (fig. 7.18), a smell of decaying meat arises from inside the flower and this attracts flies which presumably effect pollination. Male and female flowers are separate, and for pollination to occur both need to be open simultaneously. Flowers may remain open for a week and then wither and decay. The fruits inside the flower are very small and their means of dispersal to other Tetrastigma is unknown (Ernst and Schmidt 1983; Justessen 1922). It seems feasible, however, that pigs, squirrels, rats and tree shrews may get Rafflesia fruits stuck in their feet while searching for food in the forest undergrowth. If they disturb the ground around another Tetrastigma climber, the seeds may be rubbed off onto the bark where they can germinate.
The name 'bunga bangkai' is sometimes given to Rafflesia but this name is also used for Amorphophallus titanum, the tallest flower in the world which was featured on the old Rp 500 banknote. Amorphophallus plants are quite easily recognised by their characteristic blotchy stems and unusual leaves (fig. 7.19), but those seen in disturbed areas are generally smaller species. The flower of Amorphophallus titanum has a foetid odour which attracts small beetles and these effect pollination (van der Pijl 1937).
Figure 7.19. The form of the stalk of Amorphophallus and detail from part of a leaf.
CYCLES OF FLOWER, FRUIT AND LEAF PRODUCTION
As far as is known, cycles of flower, fruit and leaf production have been studied in Sumatra only at the Ketambe Research Station (Rijksen 1978), and on Siberut Island (Whitten 1980b). None of the published accounts cover a period of more than two years. There is considerable variation within and between species, between months and between years, and the patterns become clearer if the cycles are studied for longer periods such as the six years achieved at Ulu Gombak (Medway 1972a) and the long-term but intermittent studies at Kuala Lompat (Raemaekers et al. 1980), both in Peninsular Malaysia.
At Ulu Gombak 61 mature canopy trees representing 45 species were monitored. Only one of these flowered and fruited at consistent non-annual intervals, and that was the large strangling fig Ficus sumatrana which had a cycle of four to five months. Strangely, that rhythm was unconnected with the weather and yet it always produced a heavy crop. Ten species were represented by two or more trees in the sample and only five of these synchronised their flowering and fruiting. In only 10 species was flowering and fruiting consistent with annual cycles; the remaining 34 species flowered and fruited at irregular intervals usually exceeding one year and irrespective of weather. Ten species produced flowers each year, but only six of these produced fruit every year. This illustrates the fact that flowering does not necessarily lead to fruiting. This can be because of a lack of pollination, fruit and seed predation, or adverse weather conditions. In a review of this subject it is suggested that abortion of flowers or young fruit is often caused by a lack of necessary resources such as inorganic nutrients, water and products of photosynthesis (Stephenson 1981).
Figure 7.20. Monthly percentages of trees with unripe fruit, with ripe fruit, with flowers and with leaf flush at Ulu Gombak, Peninsular Malaysia. Figures are averaged over six years.
Data from Medway 1972a
Leaf flush was also variable between species. Three species produced new leaves almost all of the time and 21 species showed consistent annual patterns. Five other species exhibited irregular biannual patterns. Eight species were deciduous (lost all their leaves), four on an annual basis and four at intervals greater than a year.
Despite these variations, the tree community does show clear patterns of flower, fruit and leaf production (fig. 7.20). At the Ulu Gombak forest new leaves were produced twice each year with a major peak in March to June (just after the driest time of year) and a minor peak from October to December beginning just before and extending into the wettest time of year (Medway 1972a). Flowering at Ulu Gombak peaked after the driest time of year, that is from March to July, and, not surprisingly, fruiting peaked in August to September just before the wettest time of year. The flowering of many lowland forest trees seems to be initiated by water stress (Whitmore 1984). The apparent higher percentage of fruiting trees than flowering trees is caused by the fact that fruit remains on a tree longer than flowers and is thus counted in more months. For this reason the percentage of trees with ripe fruit is also shown.
The rainfall patterns in much of northern Sumatra are very similar to those of Ulu Gombak and so similar cycles of flower, fruit and leaf production would be expected. In the south of the island, however, where the driest months are usually June/July (Oldeman et al. 1979), the cycles are presumably adjusted accordingly.
Gregarious Fruiting
Gregarious (or mast) fruiting is a term applied to the simultaneous mass fruiting of certain trees over wide areas at intervals in excess of one year and often in excess of five years. In the tropics, this phenomenon is only found in Southeast Asia and virtually only among the Dipterocarpaceae. On pages 88, 177 and 259, mention is made of the strategy of chemical defence of leaves by trees growing with low productivity on poor soils in climates favourable for animal life, leading to low numbers of animals. Janzen (1974a) has proposed that gregarious fruiting is an indirect consequence of low productivity and, possibly, relatively low animal biomass (p. 192).
The primary purpose of gregarious fruiting is to escape seed predation. The trees produce so much seed that, after satiating the appetites of seed-predators which find the fruit, some seed still remains for germination. The synchrony also means that seed predators are unable to specialise on the particular fruit and so the population of potential seed predators is kept at a low level until gregarious fruiting begins. If only a single tree species adopted the strategy of gregarious fruiting there would be no chance of satiating the seed predators and the strategy only works because most of the family members fruit at the same time. It was shown on page 198 that dipterocarp trees often make up a considerable proportion of the trees in a lowland forest.
Dipterocarp seeds are eaten by squirrels, rats and probably also by larger animals such as pigs, tapir, deer, rhino and elephant (Payne 1979; Poore 1968; Woods 1956). They do not seem to be heavily defended with chemicals. Janzen (1974a) suggests that if such oil-rich, defence-poor seeds lay on the floor of most African, Central or South America forests, none would escape predation. It was shown on page 192 that there are fewer species of animals in the Sunda Region than in Central and South America and it is the subjective view that animal biomass is probably also less (Janzen 1974a, 1977a). This is due, at least in part, to:
• the long gaps between periods of fruiting which reduce the amount of regularly available food needed to sustain denser populations; and
• too much of the forest floor being occupied by immature dipterocarp seedlings and saplings which 'steal' resources from species which flower and fruit (produce animal food) at comparable heights.
If it is presumed that a fruiting interval for dipterocarps of only two years is sufficient to avoid most of the insects that might specialise on dipterocarp seeds (Medway 1972) (p. 225), and to reduce the populations of vertebrate seed predators, it is necessary to ask why they wait so much longer than two years. It is probably because the longer interval between fruiting seasons enables more products of photosynthesis to be stored, and thus more fruit to be produced. The longer the interval, the smaller is the percentage of the total seed crop consumed or lost. It appears that intervals of six years are common but the interval appears to be longer on poorer soil (Janzen 1974a).
It is interesting that although fruiting time is synchronised between species, flowering time is not. This disparity is probably because pollinating insects are shared between species. However, fruit of late-flowering trees develop quickly and fruit of early-flowering trees develop more slowly. It will have been noticed by those accustomed to working in forests, that mast fruiting does not operate perfectly and trees sometimes make 'mistakes' (McClure 1966; Medway 1972; Wood 1956). Janzen (1974a) suggests that since flowering appears to be triggered by climatic events (probably occasional, severe droughts) within a generally very uniform climate, minor localised droughts may sometimes cause flowering in a small population of a species. Trees sometimes deal with such mistakes by absorbing flower buds or flowers, or by producing sterile fruit (Medway 1972; Wood 1956). None of the seeds produced in fertile fruit by a single tree or small population are likely to survive because the crop would be insufficient to satiate all the potential seed predators (Wood 1956).
Effects of Flower, Fruit and Leaf Production Cycles on Animals
Since many of the trees in lowland forest are pollinated by insects, it is not surprising that peaks in abundance of certain insect species coincide with peaks of flower production. These peaks occur at the drier times of year and usually coincide with, or come slightly after, peaks of leaf production which are exploited by butterfly and moth caterpillars. Other insect species, particularly those associated with rotting wood, or those dependent on pools of water for breeding, become most abundant during the wetter months (McClure 1978; Hails 1982).
The Mentawai snub-nosed monkey Simias con-color is peculiar in having both single-female and multi-female groups.
The Mentawai "joja" Presbytis potenziani is the world's only leaf monkey found only in single-female groups.
This striking frog Rana siberu is known only from Siberut Island.
The soil dwelling burrowing snake Ramnotyphlops braminus is quite common but rarely seen. It grows to just 15 cm, and only females are known.
Pythons Python reticulatus are quite common and are avidly sought by farmers to reduce predation on their small livestock and to sell to skin traders.
Distribution of four species and twenty one subspecies of leaf monkey to illustrate the zoo-geographic zones.
Based on Chasen (12), Chasen and Kloss (13), Medway (75), Miller (85), Pocock (135), Whitten (125) and Wilson and Wilson (127, 128). From top left: Ptn - Prebytis thomasi nubilis; Ptt - P.t. thomasi; Pmm - P. melalophos margae; Pfpa - P. lemoralis paenulata; Pfpe - P.f. percura; Pfn - P.f. natuna; Pfr - P.f. rhionis; Pm? - P. melalophos (subspecies not yet named); Pfc - P. femoralis canus; Pm? - P. melalophos (subspecies not yet named); Pmfu 1 - P.m. fuscomurina (lowland form); Pmfu2 - P.m. fus-comurina (highland form); Pmfl - P.m. fluviatilis; Pmme - P.m. melalophos; Pmm - P.m. nobilis; Ppp - P. potenziani; Pps - P.p. siberu; Pmf - P. melalophos; Pmm - P.m. nobilis; Ppp - P. potenziani; Pps - P.p. siberu; Pmf - P. melalophos ferruginea; Pmb - P.m. batuana; Pma - P.m. aurata; Pms - P.m. sumatrana. The only leaf monkey that lives in the stippled area is the silvered leaf monkey Presbytis cristata, which is also common throughout the rest of Sumatra in coastal and riverine areas.
A megalith from Pasemah showing a man wrestling with an elephant.
One of the Hindu-Buddhist temples near Padang Lawas, South Tapanuli.
A long Islamic grave of an early Indian nobleman at Barus, Central Tapanuli.
Pneumatophore roots radiating from Sonneratia alba; near Bubun, Langkat.
The yellow-ringed cat snake Boiga dendrophila is quite common in mangrove forest. Its venom has little effect on people.
One of the Ophiusa serva caterpillars which Isopod crustaceans in a Rhizophora root tip. defoliated areas of Excoecaria mangrove trees near Medan in 1983.
Isopodcrustaceans in a Rhizophora root tip
Nypa palm swamp near Sicanggang.
Typical pes-caprae vegetation, north of Padang.
Casuarina forest near Singkil.
A river in Mt. Leuser National Park. In such forested rivers there is a high diversity of fish and other aquatic organisms.
Lake Dusun Besar, Bengkulu, is fringed by lance-like Hanguana plants.
Shallow, fast-moving streams such as this have specially adapted animals and plants
Aerial view of a blackwater lake in peatswamp forest on Padang Island, Riau.
Stinkhorn fungus Dictyophora indusiata.
Agamid lizard Gonocephalus grandis.
The fish-eating false ghavial Tomistomus schlegeli is becoming increasingly rare as its swamp forest homes are diminished by fire and clearing.
A view from Mt. Kerinci to Lake Tujuh across the highest freshwater swamp in Sumatra.
On Bangka pitcher plants are common on the infertile sandy soils.
Typical small trees in a remnant heath forest, Bangka.
Padang forest, Bangka.
The convex leaves of Dischidia on Bangka shield colonies of biting ants.
Tin tailings on Bangka Island with dying heath forest at the back.
Insectivorous sundews Drosera in padang forest, Bangka.
Forested limestone hills, Payakumbuh
The world's largest flower Raffesia arnoldii, West Sumatra.
Scutigerids are relatives of millipedes and are found among leaf litter and in caves.
Limestone hills have characteristic plants adapted to long periods of drought, as well as many highly restricted species of snails, Lho'Nga.
The ironwood forests of Jambi are among the very few natural tropical forests which exist in virtually single-species stands.
The seeds of ironwood are large, produced continuously, and probably toxic.
Ironwood provides an excellent timber resistant to rot and insects.
The tree heather Vaccinium varingaefolium is found from about 2,000 m to the highest vegetation belts in Sumatra.
Upper montane forest, Mt. Kemiri, 2,700 m.
Sphagnum lake in a hollow formed by glacial action near the 3,200 m summit of Mt. Kemiri.
Nephenthes gymnamphora pitcher plant, 2,500 m, Mt. Kemiri.
Potentilla borneensis, 2,900 m, Mt. Kemiri.
The hairy undersides of some montane herbs, such as this Potentilla, may be a protection against high temperatures, intense ultraviolet radiation or frost.
Usnea lichen growing in misty upper montane forest, Mt. Kemiri.
Lobelia sumatrana, 2,900 m, Mt. Kemiri.
Epigenium pulchellum orchids, 3,300 m, Mt. Kemiri.
Viola biflora, 3,250 m, Mt. Kemiri.
A large cave near Lho'Nga.
One of the authors (Jazanul Anwar, left) researching in a dry cave near Bohorok.
The cave fruit bat Eonycteris spelaea is a major pollinator of commercial fruit trees.
False vampire bats Megaderma spasma feed on lizards, frogs and insects picked off the ground and branches.
The roundleaf horseshoe bat Hipposideros diadema is one of the largest insectivorous bats living in caves.
Many saw mills waste a great deal of wood in saw dust and mis-sized planks.
Canals dug in peatswamp areas allow its water to drain away, drying the peat soil and making it more susceptible to fire.
Species of Macaranga are among the most characteristic trees of secondary growth.
Sustainable swidden cultivation is practiced by very few in Sumatra today. The exceptions include groups of Talang Mamaq near Bukit Tigapuluh National Park.
Prints of beleaguered tigers can be seen around remnant areas of forest.
Legal logging begets illegal logging begets clearance for agriculture.
Rubber, both in commercial plantations and in rubber "forests" is a mainstay of many of Sumatra's rural population.
There has been a massive increase in the area under oil palm in the last few years, with a concomitant decrease in the area of lowland forest.
The tomb bat Taphozous longimanus is a common roof-roosting bat in Sumatra's cities.
Bronchocela cristatella is a common lizard in leafy gardens.
Flying foxes Pteropus vampyrus visit fruit trees such as this jambu to dring nectar.
Figure 7.21. Percentage incidence of breeding and moulting birds of insectivorous of partially-insectivorous habit in the Malay Peninsula. The heavy line describes the percentage of breeding birds and the light line the percentage of moulting birds.
After Wells 1974
These variations in insect abundance are probably reflected in the behaviour of insectivorous or partially-insectivorous birds. The second category is included because, for birds that feed largely but not entirely on fruit, seeds or nectar, insects represent a protein-rich source of food essential for the energy-expensive tasks of feeding their young and for moulting. The insectivorous and partially-insectivorous birds of Peninsular Malaysia breed and moult all year round but there are major peaks in March-May and July-August, respectively (fig. 7.21). It is believed that these peaks depend on food availability (Wells 1974) and similar results have been found for insectivorous birds in Sarawak lowland forest (Fogden 1972), and insectivorous bats (Gould 1978b).
Frugivorous mammals and birds differ in their response to changing fruit abundance depending on the degree to which they are restricted to particular areas (p. 237). For example, animals such as bearded pigs, certain hornbills (p. 245), mynahs, broadbills, small parrots and, to some extent, orangutans are free to move away from an area when food is scarce because they are either nomadic, migratory or have huge home ranges. Frugivores with fixed home ranges, however, such as squirrels, gibbons, some monkeys and certain hornbills, have to eat more non-fruit foods or take aseasonal fruit. Important among these aseasonal fruits are figs (Leighton and Leighton 1983).
Figure 7.22. Relationship between rainfall (columns), reproductive activity as a percentage of 13 rodent species (upper graph), and percentage of trees in fruit (lower graph) in a lowland forest in Zaire. Note the similar shapes.
After Dieterlen 1982
Variations in fruit abundance have been shown to affect the behaviour of gibbons (Raemaekers 1979). During months when fruit was scarce the animals did not travel very far and stayed close to a few good fruit sources, but when fruit was abundant they travelled widely in their home range and ate a wide variety of foods. The peaks of pregnancy in Malaysian forest rats coincided with the seasonal peak in fruiting (Harrison 1955; Medway 1972), and this has been shown in more detail for rodents in a lowland forest in Zaire (Dieterlen 1982) (fig. 7.22).
SEED DISPERSAL
The dispersal of a seed is not simply the event of a mature fruit being released by its parent. Dispersal implies the carrying of a seed by some agent to a place where the seed will, perhaps, germinate, grow and reproduce. Most seeds die because the places they are dropped are unsuitable for growth; that is, they are not successfully dispersed. Seeds found directly below the parent tree are probably undispersed seeds, that is, they have simply dropped from the branches. Very few seeds and seedlings beneath their parent tree have any chance of survival because they will experience severe competition from others of their species. In addition, the parent tree and its offspring would represent a clumped food resource for seed predators. Thus dispersal of seeds can be envisaged as a means of escape from seed predators (Howe and Smallwood 1982) as well as a method of colonising widely separated available sites. In the species-rich lowland forest where, as shown on pages 189 and 198, most species are rare, a seed dispersed away from its parent will stand a relatively low chance of being adjacent to a tree of the same species.
A further advantage of dispersal away from the parent is that the biological and physical environment of the location where the parent germinated has in almost all cases changed by the time it has matured (Janzen 1975). In general, this means that the environment below the parent tree is now unsuitable for its own seeds. Gap, building and mature forest areas (p. 194) occur in more or less predictable proportions and patterns in a forest, and the means of seed dispersal will aim to maximise the colonisation of suitable areas with seeds.
The area over which seeds come to rest on the forest floor is known as a 'seed shadow'. The seed shadow of a tree is generally most dense close to the parent tree and much less dense overall when dispersed by an animal than when dispersed by wind. Whereas a wind-generated seed shadow is quite homogeneous, a seed shadow generated by animals will usually be heterogeneous. That is, animal-dispersed seeds will occur in dung piles, along animal paths, especially in certain vegetation types, etc. Exceptions are fig trees whose fruit is fed upon by many species of animals whose modes of living are so varied that a relatively homogeneous seed shadow can result. There is also variation in seed shadows for neighbouring individuals of the same species because access for the dispersing animals may be easier into one tree than into another, and because other attractive food sources may be close to one but not to the other (Janzen 1975; Janzen et al. 1976). These seed shadows are not simply of academic interest but are of major importance in determining future forest structure and composition (Flemming and Heithaus 1981).
Wind-dispersed fruits are generally borne by tall trees - the only forest trees to be affected by wind to any extent. Wind-dispersed fruits are either very light or have wings - in both cases their descent to the ground is delayed. Although wind does not disperse tree seeds particularly far from the parent, wind can at least be relied upon, whereas animals cannot.
Figure 7.23. Lowland forest on Siberut Island, West Sumatra. The most common family of trees is Dipterocarpaceae followed by Myristicaceae, Euphorbiaceae, and Sapotaceae.
A.J. Whitten
The majority of forest tree seeds are dispersed by animals which eat the fruit and carry away the still-living seeds in their guts to be deposited some distance away when the animal defaecates. Seeds can be dispersed by animals in at least six different ways and the fruit can be classified accordingly (Payne 1979, 1980). They are:
• bird fruits (divisible into opportunistic fruit, seed-eating bird fruits, specialist bird fruits and mimetic fruit),
• opportunistic fruits,
• arboreal mammal fruits,
• bat fruits,
• terrestrial rodent fruits, and
• large mammal fruits.
Thus fruits can usually be identified as being adapted for dispersal by a particular group of animals. It is worth considering what effect hunting and forest reduction has had on those species of tree whose fruits are adapted for dispersal by large mammals such as Sumatran rhino (van Strien 1974) and elephants (Olivier 1978a).
The dispersal agent for a particular fruit depends on the nutritional requirements of the animals, the accessibility of the fruit, its shape and its size. The fruits produced by a tree vary in size and, in some species, by the number of seeds they contain. Thus different portions of the fruit crop may be dispersed by different animals over different distances (Howe and Smallwood 1982; Howe and Vande Kerckhove 1981; Janzen 1982a).
It is obviously to a plant's advantage to ensure that its fruit are dispersed to the right type of location, and numerous means are used to selectively advertise the presence of fruit and to encourage certain dispersers while discouraging others. These characteristics have been shaped over evolutionary time by reciprocal interactions between animals and plants but, unlike the process of pollination, few species-specific relationships exist (Janzen 1983a; Wheelwright and Orians 1982). Edible fruits are basically seeds covered with a bait of food, and Janzen (1982b) has hypothesised that grasses and other herbs also encourage active dispersion by surrounding dry, small seeds with a bait of nutritious foliage. When the foliage is eaten, the seeds are, too. The fruit bait can vary greatly in nutritional value and plants tend to adopt one of two strategies. They can produce large numbers of 'cheap' fruit (small, sugary), most of which may be wasted or killed by the many species of frugivores attracted to them. Alternatively, a plant can produce smaller numbers of 'expensive' fruit (large, lipid-rich, oily) that have to be searched for by those few specialised species of frugivores which gain a balanced diet almost entirely from fruit (Howe 1980, 1981; Howe and Smallwood 1982; Howe and Vande Kerckhove 1980).
Fruits advertise their ripeness to dispersers using colour, texture, taste, conspicuous shapes, and odour. However, between ripening and being taken by a disperser, the fruit is also exposed to destructive animals and microorganisms.
The destructive animals may be termed 'seed predators'. It should be noted that a disperser animal can become a predator if it eats the fruit before the seeds are mature. Thus a fruit needs to be as unattractive as possible before the seed is viable and this is commonly achieved by the presence of defence compounds whose concentration is reduced as ripening progresses. For example, on Siberut Island the endemic gibbons eat the fruit of wild sugar palms Arenga obtfusifolia. These fruits contain water-soluble sodium oxalate which, if it comes into contact with mucous membranes (such as lips, mouth and throat), absorbs calcium and becomes water-insoluble needle-sharp crystals of calcium oxalate. The pain and the loss of calcium can kill. As the fruit ripens, however, the sodium oxalate is broken down and when fully ripe the fruit can be eaten safely (Whitten 1980a).
Some fruit do not lose all their defence compounds when they are ripe and this is thought to be a means of protecting fruit from being eaten or destroyed by non-disperser animals or microorganisms (Herrera 1982; Janzen 1983b). Defence compounds can be divided into two groups: toxins which can debilitate or kill, and quantitative defences or digestion inhibitors such as resins, gums, volatile oils and phenols which deter potential seed predators or cause some mildly adverse physiological effect (such as feeling sick) (Maiorana 1979; Waterman 1983; Waterman and Choo 1981). A review of these defended ripe fruits concluded that the species producing them were at a competitive disadvantage for dispersal relative to species without defended ripe fruit. If the defences are viewed as means by which undesirable seed predators can be avoided, then extreme toxicity may be a 'last resort' (Herrera 1982).
Orangutans are probably the sole fruit disperser for some plants amongst which is the climber Strychnos ignatii (Rijksen 1978). The large fruit contains the 'deadly' alkaloid strychnine but it appears to have no effect on orangutans except for an excessive production of saliva. Indeed, strychnine appears to be dangerous only for carnivorous animals and for omnivores such as humans (Janzen 1978a). Orangutans also eat the fruits of the ipoh tree Antiaris toxicaria which contain another poisonous alkaloid (Rijksen 1978). Ipoh latex is used by some peoples in the preparation of poisoned arrows and darts but it is actually not as deadly as popularly believed (Burkill 1966; Corner 1952). It may be that these plants use their toxins to deter the 'wrong' dispersers.
Seed predators are commonly larvae of small beetles and these show a high level of specificity. Of over 975 species of shrubs and trees in an area of Costa Rica, at least 100 species regularly had beetle larvae in their mature or nearly-mature seeds. Three-quarters of the 110 beetle species found (primarily from the family Bruchidae) were confined to a single species of plant; if a beetle species was found on more than one plant species, the plants were closely related. Of the 100 species of plants, 63 were legumes and 11 were Convolvulaceae (Janzen 1980). This 'preference' for legumes might be because most plant families have had strong defences against attacks from bruchid beetles (fig. 7.24), whereas a few families have not. It seems more likely, however, that bruchid beetles became legume seed predators many millions of years ago and were able to counter whatever forms of defence the plant used. As the legumes evolved and diversified so the beetles evolved - a case of coevolution. Since plant defences appear to be so complex, the specialisations required to predate on a particular species or genus are such that a beetle species would be unlikely to be able to also become a predator on seeds in another plant family.
Figure 7.24. A bruchid beetle.
In general, the larger the seed the longer the time between ingestion and excretion. In experiments with a tapir, it was found that a considerable proportion of large, unchewed seeds were killed in the animal's gut because they germinated before being excreted and thus were acted upon by digestive juices (Janzen 1981b).
Destructive microorganisms (fungi and bacterial) represent a form of competition for frugivores. Fungi are not generally envisaged in this role but Janzen (1977b, 1979a) has suggested that this interpretation is valid. To a microbe, a ripe fruit is a considerable food resource which can be digested and converted into more microbes. It is obviously preferable, having started, to exploit the whole of the fruit and so competitors have to be dissuaded from using it as food. The microbe produces antibiotic substances to prevent other microorganisms from colonising the fruit, and toxic and unpleasant-tasting substances to deter larger frugivores. Producing tasteless toxins alone would not be a successful strategy because an animal may still eat the fruit, kill the microbe and later die itself. In that case neither party wins. Fruits invaded by microbes have to look, smell and taste different from untainted fruit or else the microbes have lost the battle.
Some fruits are known to produce their own antibiotics against decomposer microorganisms (Janzen 1978a) but this field of study has received little attention.
LEAVES AND BARK AS SOURCES OF FOOD
Leaves
About 50% of at leaf consists of cellulose, a complex sugar molecule which makes up the outer cell walls. Most animals lack the necessary enzymes to break down the cellulose into easily digestible, volatile fatty acids but some employ certain bacteria (or fungi - p. 233) to conduct this first stage of digestion on their behalf. The possession of these bacteria allows access to a widely distributed and abundant food source. The bacteria themselves form an important source of protein for the host and can synthesise most vitamins except A and D. In vertebrates there are two major forms of bacteria-assisted digestion: foregut and hindgut fermentation. Foregut fermentation is found in, for example, cattle, deer and leaf monkeys, and hindgut fermentation in, for example, rabbits, horses, koalas, rodents and flying lemurs (Bauchop 1978; Muul and Lim 1978). Leaves are eaten by a wide range of mammals and larval and adult insects, but not by amphibians and by very few reptiles or birds (Morton 1978; Rand 1978). It is estimated that 7%-12.5% of leaf production is eaten by insects (Leigh 1975; Wint 1983) and only 2.4% by vertebrates (Leigh 1975). However, as Janzen (1978a) points out, these figures are usually calculated from the remains of fallen leaves and so do not necessarily include leaves or shoots eaten in their entirety.
The actual amount of leaf material eaten is not the most important ecological measurement because different parts have different values to the plant and hence different 'costs' for replacement. For example, the loss of a small shoot from a seedling is considerably more costly to the individual plant than the loss of a great many leaves on a mature plant. Leaves pay back their cost by photosynthesising and contributing the products of photosynthesis to the plant. So, once a leaf has paid back its 'debt', its value to the plant decreases with time. It is clear, then, that for advanced ecological analysis of an ecosystem, a list of plant species eaten by a particular animal species is not nearly so useful as knowledge of what parts of each species are eaten and the likely cost to individual plants of the material lost.
To the eyes of a human observer the leaves of a lowland forest, or indeed other tropical vegetation types, vary in shape and shade of green. To an animal which depends on leaves as a food source, however, they are 'coloured' "nicotine, tannin, lectin, strychnine, cannabinol, sterculic acid, cannavanine, lignin, etc., and every bite contains a horrible mix of these" (Janzen 1981a). These phenolic and alkaloid compounds (Walker 1975) are just some of the toxic and digesdon-inhibiting chemicals used by plants to defend their leaves against herbivores (Edwards and Wratten 1980). Some of the ecological consequences of these chemicals are described on pages 177 and 259. See also page 213 for a discussion of the defence strategies of plants growing in gaps.
A recent laboratory study in North America has added a further dimension to the study of defence compounds. The response of tree seedlings was monitored before and after 7% of their leaf area was removed. Within two days the seedlings had increased the concentration of phenolic compounds in their remaining leaves - perhaps as a defence against further loss of leaves. Strangely, however, nearby undamaged seedlings of the same species behaved similarly. This suggests that the damaged plants were able to communicate a warning to the other plants. How this is effected is as yet unknown (Baldwin and Schultz 1983).
Some animals may be able to eat leaves because they have coevolved with the plant - that is, changes in a plant's chemical defences have been met by changes in the animal's digestive capability (Edwards and Wratten 1980; Wratten et al. 1981). It could be, however, that an animal has evolved the ability to cope with the defences with no corresponding innovation in the plant's chemistry. Conversely, a plant may produce defences which cause the partial 'defeat' of the herbivore with no response by the animal.
There is probably no plant whose defences preclude attack by all herbivores, and there is certainly no animal which can eat all types of leaves. A particular moth caterpillar in Costa Rica is able to eat leaves containing 40% by dry weight of phenolic compounds. This caterpillar eats almost only phenol-rich leaves from nearly 20 species, but it grows at only half the rate of moth caterpillars eating phenol-poor leaves from just a few species of plants (Janzen 1983c). Similar results were obtained in experiments with locusts (Bernays 1978; Bernays and Chamberlain 1980). When eating a leaf rich in defence compounds, a herbivore gains less usable food per unit effort (per mouthful) than when eating a leaf low in defence compounds, but it probably has more species to use as food and experiences relatively less competition from other herbivores unable to cope with the chemicals.
Experiments on the selection of leaves by a captive South American tapir showed that out of 381 species offered, only 55% were eaten, and only one of the 55 leguminous species was accepted. The tapir of the Sunda Region is also a very selective feeder in the wild, eating from saplings of only a fraction of the available tree species (Medway 1974; Williams and Petrides 1980).
Monkeys are also very selective in the plants they eat, choosing particular species, particular ages and parts of leaves, and quantities. Recent studies of food selection by leaf monkeys in Peninsular Malaysia and Sabah have shown that leaves selected as food are consistently low in lignin (fibre), and usually relatively high in protein; that is, the leaves are highly digestible. Tannin levels did not show consistent significant correlations with food selection (Bennett 1984; Davies 1984). Similar results have been obtained in Africa and India (Oats et al. 1977,1980) and it is now generally felt that the role of tannins in food choice has been overemphasised (Waterman 1983). They do, however, probably remain a potent force in ecosystems where poor soil conditions cause some form of stress in the trees growing on them.
Tannins and lignins are classed as digestion-inhibiting phenolic compounds (although lignin is 10-20 times less effective than tannins), whereas others, such as the alkaloid strychnine, are classed as toxins. The term 'toxic' is really a measure of the energy expended by an animal in utilising a food relative to the energy value of usable materials gained from the digestion process. Toxicity is therefore an outcome rather than an inherent property of a chemical, although some chemicals are more likely to be toxic than others. Whether a certain percentage composition of a potentially dangerous chemical is toxic or not will depend on the food value of the material eaten and on the efficiency of the animal's detoxification system. Thus, a leaf may be more toxic than a seed with the same weight and concentration of defence compounds, because the seed has a greater nutritive value (Freeland and Janzen 1974; Janzen 1978a; McKey 1978). Defence compounds should not be thought of as purely disadvantageous from the herbivore's point of view because they can have decidedly beneficial effects, as described in the next section.
Bark
Bark is, perhaps, an unlikely food but it has been recorded as a constituent of the diet of orangutans (Rijksen 1978), gibbons (Whitten 1980b), elephants (Olivier 1978a), Sumatran rhino (van Strein 1974) and squirrels (Payne 1979; Whitten 1979, 1980). Bark is not a rich food source and it may be eaten as a supplementary food to provide dietary fibre or trace elements.
On Siberut Island the small squirrel Sundasciurus lowii eats bark as a major item of its diet (p. 244), and an analysis of the bark and bark-eating was conducted by J. Whitten (1979). Physical characteristics of trees (size, roughness of bark, ease of access for squirrels, etc.), food value and concentration of phenolic compounds in the bark of trees chosen as food sources were compared with similar data from trees not chosen as food sources. Trees on which the squirrels fed tended to be large, smooth-barked and relatively free of climbers, and certain tannins were absent in the barks eaten. These barks were not noticeably richer in food value than those which were not eaten.
Defence compounds in bark, and indeed other food items, need not necessarily be selected against by animals; indeed, Janzen (1978a) suggests that certain compounds may be actively sought for specific purposes. For example, elephants have been reported to feed extensively on a certain leguminous creeper before embarking on a long period of travel, and it may be that the plant contains some stimulating or sustaining chemical (Hubback 1941). The high levels of tannins in some barks may be eaten to combat heavy parasite loads or upset stomachs. For example, Asian buffalo eat a plant with an informative scientific name Holarrhena antidysenterica (Ogilvie 1929) and Sumatran rhino have been observed to eat so much of the tannin-rich bark of the mangrove tree Ceriaps tagal that their urine is stained bright orange (Hubback 1939). It is worth noting, however, that the once-popular drug for diarrhoea 'Enterovioform' contains 50% (dry weight) tannin, a concentration not unknown in nature, but its role in combating diarrhoea has now been largely discredited.
SOIL AND ITS ANIMALS
The soil under the majority of lowland forest in Sumatra is red-yellow podzolic, and this has been described by Burnham (1975), Sepraptohardjo et al. (1979) and Young (1976).
The majority of soil fauna in the Sunda Region is known very poorly and the only quantitative studies seem to have been conducted in Peninsular Malaysia and Sarawak (Collins 1980, 1983). In 1 m2 at Pasoh an average of 2,000 ants, 300 termites, 30 earthworms, 30 fly larvae, 50 spiders and 100 beedes and their larvae were found. The total biomass of these invertebrates was about 3 g/m2 (3,000 kg/km2) but this and the proportions of different groups varied gready from month to month. Similar results with more termites were obtained in Sarawak where the biomass was 4-6 g/m2 (Collins 1980). To compare these figures with vertebrate biomass see page 250. Among the smaller animals at Pasoh, over 10,000 mites (Acarina) and about 56,000 nematode worms were found per m2. These totals are not particularly high and some temperate areas would have greater densities but species diversity in the tropics is almost undoubtedly greater.
Termites
The soil animals about which about most is known are termites. Termites may look superficially like ants but they are classified in a completely different order which is more closely related to cockroaches. Termites are Isopterans, ants (together with bees and wasps) are Hymenopterans (fig. 7.25). Termites are like ants, however, in that they form enormous colonies with (at least in some parts of the world) possibly a million or more members. A colony is not a simple community of distinct individuals because all except two of the colony members are siblings. The other two, the 'royal pair', are the parents. The parents originated in other termite nests from which they flew along with thousands of others. In these swarms some manage to escape the hordes of ants, amphibians, reptiles, birds and mammals for which such a swarm is a food bonanza. After landing, their wings drop off and if a male finds a female, they will look for a suitable crack in the ground or a tree (depending on the species) and here they build their 'royal cell'. They copulate and the female begins laying eggs. The larvae, unlike the helpless larvae of ants, bees and wasps, are fully able to move around and undergo several moults (like cockroaches) rather than a single metamorphosis before becoming adults. These first larvae have to be fed by their parents but as soon as they are large enough to forage for food and to build walls for the nest, the royal pair devote themselves entirely to the production of eggs. The abdomen of the female, or queen, grows to grotesque proportions and a production rate of thousands of eggs per day is common.
A termite colony can be likened to a single, although sometimes disparate, organism because none of its components is capable of independent life. The workers are blind and sterile, and the soldiers which protect the columns of foraging workers and guard entrances to the colony's nest have jaws so large that they can no longer feed themselves and have to be fed by the workers. The king and queen are also fed by the workers. In the same way that communication between different organs or parts of a single body is effected by chemicals flowing through a body's tissues, so chemicals (pheromones2) link the different members of a termite colony into a coordinated and organised whole. All of the colony members continually exchange food and saliva which contain pheromones. Workers pass these materials from mouth to mouth and also consume one another's faeces to reprocess whatever partially digested food remains. Workers feed the soldiers, larvae and royal pair as well as collect the queen's faeces. There is thus a continual interchange of chemicals through the colony and this coordinates the operations of the colony. For example, larvae are potentially fertile termites of either sex but the food with which the workers feed them contains quantities of pheromone from the queen which inhibits the development of larvae and produces workers. The soldiers also produce a pheromone which prevents the larvae from developing into soldiers. When, for some reason, the number of soldiers falls, the level of 'soldier repression pheromone' circulating through the colony members falls and some eggs develop into soldiers. On other occasions the queen will reduce her repressive pheromones and her eggs will develop into fertile winged termites which, when the air is moist, will leave the nest in a swarm and the cycle of colony formation begins again.
Figure 7.25. Typical termites (worker on left, soldier on right) and an ant.
Most invertebrate decomposers of the lowland forest soil depend on free-living saprophytic fungi and bacteria to break down indigestible plant material into a digestible form before they can play their role, and termites are no exception. One subfamily of termites, the Macrotermitinae, represented in Sumatra by Macrotermes, Odontotermes and Microtermes, maintain a fungus in 'gardens' in their nests which releases them from competing for partially decomposed material outside their nest. The workers of the above genera build complex frameworks, or combs, from their own round faecal pellets (not, as was once thought, from chewed food) - other groups of termites use faeces for building the fabric of their nests. (An identification key to genus level based on the head shape of soldiers has been written by Harris [1957]). Since the main food of the Macrotermitinae is wood and leaf litter, the combs look like thin, fragile pieces of moist, spongy, rotten wood. These combs are the food of a form of fungus called Termitoinyces which is unknown outside termite nests. Small white dots, which are clumps of asexual spores, can sometimes be seen on the combs if a nest is cut open. It takes up to two months for the fungus to process the combs (Collins 1982).
This relationship with the fungus confers several advantages on the termites. No animal has the necessary digestive enzymes to digest lignin, a largely inert compound which is the main component of wood and thus one of the major items in a termite diet, and so lignin is excreted unchanged in the termite faeces. The fungus, however, can digest lignin. The termites are also unable to digest cellulose - the main component of plant cell walls - but the fungus does produce the necessary enzymes for breaking down cellulose. When the termites eat the fungus-permeated comb, these cellulose-digesting enzymes persist in the termite gut, thereby improving the efficiency of its own digestion (Collins 1982). The fungus removes carbon from the comb during the digestion process and releases carbon dioxide as a result of its respiration. This has the advantage to the termite that the proportion of nitrogen in the combs increases roughly four-fold when processed by the fungus (Matsumoto 1976, 1978b). The tremendous contribution the fungus makes to Macrotermitinae nutrition has resulted in these termites being unable to live without Termitomyces - an example of obligate symbiosis. It has made them so successful that they have been reported to be responsible for the removal of 32% of leaf litter in Pasoh Forest Reserve in Peninsular Malaysia (Matsumoto 1978a). In the same forest Abe (1978, 1979) studied the role of termites in the decomposition of fallen trees. He found that the rate of wood removal was higher for small branches (3-6 cm diameter) than for trunk wood (30-50 cm diameter) which is harder and more difficult to cut and remove. In a species of meranti Shorea parviflora, 81% of the tree's dry weight of small branches was removed in the first 18 months after it fell compared with 18% of the trunk. Termites thus play a major role in the breakdown and cycling of plant material (Wood 1978).
There are at least 55 species of termite at Pasoh (Abe and Matsumoto 1978,1979) and for population studies Matsumoto (1976,1978b) chose the four most abundant species with conspicuous mound nests, part of which projected above the soil surface. Approximately 100 nests were found per ha for three of the species but there were only 15 large nests of Macrotermes. The population size per nest for Macrotermes (about 88,000) was, however, at least twice that for the other species. The number of nests built by other genera in trees averaged four per species per ha. Nests and the queen or queens they contain can survive for many years but some colonies may last less than a year (Abe and Matsumoto 1978, 1979). Colonies die for various reasons: because of extensive parasitism by small wasps, because the queen or king dies, or because the nest is destroyed by pangolins. Harrison (1962) examined the stomach of a pangolin Manis javanica and found approximately 200,000 ant workers and pupae within it. If this is taken as an average daily diet (probably an underestimate), then a single pangolin could eat 73,000,000 ants or termites per year.
SPACING OF VERTEBRATE ANIMALS
Different species organise the distribution and grouping of their members in a variety of different ways. It is beyond the scope of this book to cover the theoretical reasons behind different kinds of social structure but the major patterns found in Sumatran lowland forest animals are described below.
Social Systems
Adult male orangutans, slow loris, pangolins, shrews, tigers, bears, tapirs and Sumatran rhinos all live in more or less exclusive ranges within which single female/offspring groups live in somewhat smaller, overlapping ranges. The male attempts to maintain exclusive breeding rights over these females and the extent of his claimed area is communicated to other males by loud calls, regularly visited dung or urine sites or a combination of these two (Borner 1979; Lekagul and McNeely 1977; MacKinnon 1977; Rijksen 1978; van Strein 1974; Williams 1979). Male pigs also live a largely solitary existence but several females and their offspring form groups of 10 to 20 animals. When a female pig is ready to give birth she will go off on her own and remain alone until the piglets are old enough to run after her.
Mouse deer live singly for most of the year but form stable pairs for breeding (Davison 1980). Elephant males and females also live apart but the males will sometimes form bachelor groups and the females form herds with their young. Even when one or more males are attending the females and offspring, that group is still led by a matriarch (Olivier 1978a).
Wild forest dogs Cuon alpinus live in mixed-sex packs of 10 or more, led by a dominant male. They travel and hunt together and are quite capable of killing a large deer even though its greater size, antlers and speed would make it unlikely prey in a one-to-one contest.
Almost all monkeys live in single- or multi-adult-male groups with more adult females than adult males (polygynous). The exception, unique among the world's monkeys, is the joja leaf monkey Presbytis potenziani of the Mentawai Islands. It lives, like gibbons, siamang and tarsiers, in permanent, monogamous (one adult male and one adult female) groups within home ranges (the areas normally used by individuals or groups) containing territories which are defended against others of the same species (Aldrich-Blake 1980; Curtin 1980; Gittins 1980; Gittins and Rae-maekers 1980; Niemitz 1979; Raemaekers 1979; Tilson and Tenaza 1976; Whitten 1982b, 1982d; Whitten and Whitten 1982; Wilson and Wilson 1973). The other Mentawai leaf monkey or simakobu Simias con color lives in both monogamous and polygynous groups (Tilson 1977; Watanabe 1981; Whitten 1982b).
Most species of forest birds are more or less solitary for most of the year. Amongst these, the great argus pheasant Argusianus argus (fig. 7.26) is of particular interest. The male scratches conspicuous, cleared 'dancing grounds' about 12 m2 in area on the forest floor on the top of hills or knolls. He utters his well-known 'ki-au' call from the dancing grounds to attract females for breeding and when they arrive he performs a dramatic dance displaying his ornate, 1.5 m long tail. After mating he plays no further role in the development of the chicks (Davison 1981a).
Figure 7.26. Great Argus Pheasant Argusianus argus.
After King et al. 1975
Most pigeons (Columbidae), small parrots (Loriculus and Psittinus), ioras and leafbirds (Aegithina and Chloropsis - see p. 42), minivets (Pericrocotus), some hornbills3 (Bucerotidae) and some other birds are gregarious and form flocks for most of the year but separate into pairs for breeding. Drongos (Dicruridae) and some hornbills spend most of their adult life in pairs and these tend to be territorial. Other hornbills are territorial, communal breeders living in more or less permanent flocks of up to 10 (Leighton 1982). In addition, mixed-species flocks are found (Croxall 1976; Leighton 1982). These have been interpreted as a means by which relatively specialised insect-eating birds can increase their food supply, particularly during times of food shortage (p. 222), because of the insects flushed by the activity of the other species in the flock. The different responses of insects to disturbance and the different specialisations of the species could ensure benefit for all the flock members (Croxall 1976).
Niches
The type of niche discussed below is the realised niche (p. 156), or that part of the total environment which a species actually exploits. A species' niche has been likened to its profession and this is a useful way to understand the term.
The enormous structural complexity and the high plant species diversity of lowland forest provides an uncountable number and often unexpected range of niches for possible exploitation by animals. For example, certain bark beetles (Scolytidae) (fig. 7.27) breed only in the leaf stalks of certain species of trees (Beaver 1979a,b). The large number of animal species in turn provide a wealth of exploitation opportunities for other animals. For example, when spiders move about they leave behind them trails of fine 'silk' which may be on a substrate or suspended between two objects. Certain flies, wasps and moths habitually hang on these abandoned threads at night and are thus out of danger of walking predators (e.g., ants) and can effect a rapid escape from danger (Lahmann and Zuniga 1981). In addition, certain wasps have developed the ability to take flies out of spiders' webs before the fly is killed by the spider and without getting caught themselves (Bristowe 1976).
Figure 7.27. Side arid dorsal views of a scolytid beetle.
Three Sumatran reptiles (the geckos Cnemaspis kandianus and Peropus mutilatus and the skink Sphenomorphus cyanolaemus) are 'specialists' on buttress in lowland forests. That is, when reptiles were collected for six weeks at Bukit Lawang, Langkat, those three species were only caught on buttresses. There were even microhabitat preferences within the 'buttress-niche' depending on the amount of litter present between the arms of the buttresses (Voris 1977).
As stated elsewhere (p. 326), although the niches of two species cannot be exactly the same, one species frequently shares part of its niche with another species. This can cause competition between two species such that the removal of one species will increase the abundance of the other. This has been shown for frogs found on the banks of lowland forest streams in Sarawak. Three species (two of which are found in Sumatra) were studied along three streams and each was found to range from the stream bank different distances into the forest from the stream: thus Rana blythi, the largest of the three, was found up to 10 m from the stream, R. ibanorum up to 7 m, and R. macrodon up to 3 m. The last two species were almost exactly the same size and only slightly smaller than R blythi. The prey of the three species also showed considerable overlap. After a complete censuses of the frogs had been made along the three streams, R. ibanorum was removed from along the stream where R. blythi was least common, R. blythi from the stream where R. ibanorum was least common, and the third stream was left as a control. The results are shown in figure 7.28. Where R. ibanorum was removed, R. blythi increased its population, but where R. blythi was removed, the R. ibanorum population fluctuated but did not increase. Thus R. ibanorum seemed to have been restricting the realised niche of R blythi but not vice versa. Exactly how the competition was effected is not known (Inger 1969; Inger and Greenberg 1966).
Niche Differentiation
The manner in which similar species are able to coexist in the same area is termed 'niche differentiation'. This can be effected by spatial separation, dietary separation, temporal separation, or, more usually, a combination of all three. To illustrate this, the niche differentiation within three groups of lowland forest animal communities will be described: primates, squirrels, and hornbills.
Primates
The most species of primates in an area of mainland Sumatran lowland forest is eight4: orangutan Pongo pygmaeus or tarsier Tarsier bancanus5, sia-mang Hylobates syndactylus, white-handed gibbon H. lar or dark-handed gibbon H. agilis, silvered leaf monkey Presbytis cristata, Thomas' leaf monkey P. thomasi or banded leaf monkey P. melalophos or eastern leaf monkey P. femoralis, long-tailed macaque Macaca fascicularis, pig-tailed macaque M. nemestrina, and slow loris Nycticebus coucang. The tarsier and slow loris have a very different niche from the others: they are both nocturnal, the slow loris eating fruit and insects, the tarsier mainly insects. The niche separation of the other six is not so obvious.
Spatial separation. The actual areas of lowland forest used by the diurnal primate species are more or less identical, although long-tailed macaques and, to some extent, silvered leaf monkeys are more common in riverine forest (Wilson and Wilson 1973). Wilson and Wilson also report that silvered leaf monkeys rarely enter deep into lowland forest but, on Bangka Island where banded and eastern leaf monkeys are absent, they appear to be quite common inland (Whitten, unpubl.). Each species has its own altitudinal range (p. 305). Marked separation also occurs in the use each species makes of the canopy (fig. 7.29). The difference between the two macaques is the most marked, with pig-tailed macaques being much more terrestrial (Crockett and Wilson 1980). The two species do use the canopy in a similar manner for feeding but pig-tailed macaques are anatomically better suited to walking on the ground than to jumping or leaping. The sia-mang and gibbon are very similar in their use of the canopy (MacKinnon and MacKinnon 1980) but the orangutan uses the middle canopy more than either of them (Rijksen 1978). Orangutans never leap between trees and often rock back and forth on trees in the middle canopy of the forest until they can reach a neighbouring tree.
Figure 7.28. Estimates of frog population size on three streams in Sarawak at five census periods distributed over one year, showing mean and one standard deviation either side of the mean: a) untampered with to act as a control, b) streams with R. ibanorum removed, after the first census, c) streams with R. blythi removed after the first census.
After Inger and Greenberg 1966
Dietary separation. Representative diets of some of the diurnal primates are shown in figure 7.30. These figures disguise considerable variations between days, months and seasons, but illustrate the major differences in the relative importance of fruit and leaves. The differences are clearer still if the actual food items are considered. In other words, different plant species and different parts of the same plant species are counted separately; this is shown in figure 7.31. Thus, whereas in figure 7.30 siamang and banded leaf monkeys were apparently quite similar in their diet, the actual overlap between the food items they eat is very small. Insufficient data are available for a complete analysis, but in the Ranun River area of North Sumatra pig-tailed macaques have a high dietary overlap of 48% with their close relative, the long-tailed macaques (MacKinnon and MacKinnon 1980), and the diets of orangutan and white-handed gibbons overlap by 40% (MacKinnon 1977). The orangutan diet probably overlaps more with that of gibbons and siamang than with the diets of the other primates.
Figure 7.29. Vertical use of the canopy by six primates at Ketambe Research Station, Mount Leuser National Park. Bars beneath each column represent 50% of total observations.
After Rijksen 1978
Figure 7.30. Average diets for five Sumatran primates. The proportions are typical but disguise a wide variation between days and between months. Thomas' and Mentawai leaf monkeys probably have similar diets to banded leaf monkeys. Silvered leaf monkeys probably eat more leaves than fruit.
From data in MacKinnon 1977; Rijksen 1978; MacKinnon and MacKinnon 1980 and from E.L. Bennett, pers. comm. and A.G. Davies, pers. comm.
Figure 7.31. Number of different food items eaten by four primate species (in brackets), the number of shared items, and the percentage of dietary overlap between each pair of species. E.L. Bennett (pers. comm.) believes the overlap between white-handed gibbons and banded leaf monkeys is only about 1%.
Based on MacKinnon and MacKinnon 1980
The greatest dietary overlap is between the siamang and gibbon, which also appear to have the most specialised diets (fewest types of items). The way in which they segregate food resources between them is a function of body size which influences their different foraging strategies. Siamang are twice as heavy as gibbons but travel only half as far each day. They feed at only half as many feeding sites, but feed for twice as long at each site. Siamang have to travel direct routes between trees with abundant food but gibbons are able to exploit smaller, more dispersed food sources (Gittins and Raemaekers 1980; MacKinnon 1977; MacKinnon and MacKinnon 1980; Raemaekers 1979). These two compete by depleting each other's food supplies, and exploitation competition is probably the major form of this competition. The larger siamang, however, is able to dominate the gibbon if they meet at a food source (disturbance competition). The rarity of meetings between the two species, even when they occupy the same areas of forest, is probably avoidance of this form of competition by the gibbons which are able to seek alternative food sources (Raemaekers 1978).
Temporal separation. The activity patterns of five Sumatran primates is shown in figure 7.32. Different activity patterns have probably evolved so that food is eaten at optimally spaced intervals through the day. Thus leaf monkeys, which eat seeds and leaves (both of which contain high levels of defence compounds), need to space their feeding more or less evenly through the day so that the effects of these compounds do not cause debilitating peaks. Conversely, gibbons and siamang eat mainly fruit and young leaves and feed more intensively during the early part of the day. Since leaves are most nutritious at the end of the day when the products of photosynthesis (carbohydrates and sugars) have accumulated, it would be expected that these are eaten most in the afternoon. This is found in leaf monkeys (Curtin 1980), siamang and gibbons (Gittins and Raemaekers 1980). Temporal separation also occurs in the times at which the different primate species call (fig. 7.33) (see also p. 248).
Squirrels. Ecological separation of three diurnal squirrels was investigated on Siberut Island by J. Whitten (1980). The species (relative sizes shown in fig. 7.34) were separated largely on their vertical-use of the forest (fig. 7.35), but in the areas of overlap in the lower levels they were separated by both activity (as indicated by calling) (fig. 7.36) and by diet. The large Callosciurus melanogaster ate mainly fruit and insects, the small Sundasciurus lowii ate bark, moss, lichens, insects and earthworms, and the largely ground-dwelling Lariscus obscurus ate mainly fruit (fig. 7.37).
Similar results were obtained in Peninsular Malaysia by Payne (1979). Peninsular Malaysia has the two very large diurnal squirrels Ratufa ajfinis and Ratufa bicolor, which are both also found in Sumatra. These two species are almost exactly the same size and weight (factors which usually influence ecological separation) and exploit the forest in very similar ways. Their niche separation is thought to be due to minor differences in canopy use and diet (Payne 1979).
Figure 7.32. Daily activity patterns of five primate species. Note the relatively high proportion of travel for white-handed gibbons, the double peak of feeding and marked midday rest for orangutan, and the relatively late start for banded leaf monkeys and long-tailed macaques.
After MacKinnon 1977, MacKinnon and MacKinnon 1980
Hornbills. Sumatra has 10 species of hornbill and at least eight can be found in a single area of forest. The means by which available resources are divided between them so that these species can coexist have not been studied in Sumatra, but this subject was studied in East Kalimantan where seven species (all of which are found on Sumatra) live in the same forest (Leighton 1982). Two of the species are nomadic, flocking species, three live as territorial pairs and two live in territorial but communal groups. Fruit forms the major part of all their diets but they will all also eat small animals. The two major classes of fruit eaten, sugary figs and lipid-rich fruits, differed in their abundance, distribution and profitability (net rates of energy gain for the hornbills). The economics of searching for these different foods together with the hornbills' body weight and competitiveness probably influence group size and the relative importance of figs or other fruit to the birds. The nomadic species travel large distances (i.e., expend considerable energy) but track temporary peaks in fruiting of lipid-rich fruits within localised habitats over a large area. The territorial species, living within fixed areas and thus with lower energy costs, supplement their diets with figs and animal prey between the periods of lipid-rich fruit availability.
Figure 7.33. Percentage of calls occurring through the day for four primate species around the River Ranun, Dairi.
After MacKinnon 1977
Figure 7.34. Relative sizes of the three diurnal squirrels on Siberut Island.
Figure 7.35. Vertical distribution of three species of squirrel on Siberut Island.
After J. Whitten 1980
Figure 7.36. Distribution of calling through the day by three species of squirrel on Siberut Island. Note that the vertical axis for S. lowii and L. obscurus are calls per hour, whereas for C. melanogaster the vertical axis is total number of calls heard.
After J. Whitten 1980
Figure 7.37. Diets of three squirrels on Siberut Island.
Simplified from data in J. Whitten 1980
Temporal Separation of Animal Calls
The way in which sound transmits through forest, particularly the structurally complex lowland forest, is quite different from the way sound moves through open air. Foliage, air turbulence, air temperature gradients and ground effects can rapidly degrade the vocal signals which animals use to communicate with others of the same species. In brief, the principles governing sound transmission in lowland forest are:
Figure 7.38. Lowland forest near a stream in Mount Leuser National Park, Southeast Aceh.
A.J. Whitten
a) sounds with wavelengths shorter than objects in their path will be reflected whereas longer wavelengths will not;
b) low-frequency sounds are absorbed less rapidly by humid air than high-frequency sounds;
c) animals calling from the forest canopy, above the range of ground effects and at times when other animals are not calling, increase the distance to which their calls will be carried;
d) complex structural properties of forests produce 'sound windows' through which certain frequencies can pass but others cannot;
e) temperature increases with height above the forest floor during the day and this causes sound to be trapped and attenuated within the forest (Richards and Wiley 1980; Whitten 1982f).
After Chivers and Davies 1978; Davison 1981b; Fiynn and Abdullah 1983; Lekagul and McNeely 1977; MacKinnon 1974, 1977; MacKinnon and MacKinnon 1980; Medway & Wells 1971; van Noordwijk and van Schaik 1983; Olivier 1978a; Payne 1979; Poniran 1974; Rijksen 1978; Robertson 1982; van Strien 1974; West 1979; World Wildlife Fund (Malaysiaf/Payne and Davies 1981
Given the above principles one would expect animals to call when conditions allow maximum transmission of their calls. Examination of the spacing of calls by cicadas (Young 1981), birds and other vertebrates (Hen-wood and Fabrick 1979; Medway 1969), and gibbons (Whitten 1980b) have shown that calls are indeed given at the times and frequency that provide for best transmission.
Density of Larger Animals
Knowledge of the home range occupied by a single group cannot necessarily be used to calculate a density, because for some species there are frequently gaps between home ranges or, for other species, home ranges overlap. The densities of selected large mammals and birds in Sumatran lowland forest shown in table 7.2 must not be used to calculate densities in a given patch of forest in, for example, an environment impact assessment. They are included in this book so that the reader can form an impression of the natural rarity of many of the larger animals and of the density that might be expected. Densities van' considerably between areas and between forest types (Marsh and Wilson 1981; Payne and Davies 1981) and results from one area should not be applied indiscriminately to another area. The methodology of faunal surveys can be found elsewhere (MacKinnon 1981; Marsh and Wilson 1981; Payne and Davies 1981). Data are available on numbers and biomass of insectivorous birds in lowland forest (Wells 1978), on approximate ranges of forest rats (Harrison 1958) and of other mammals (Gitins 1980; Medway and Wells 1971) and on the density and biomass of squirrels (Payne 1979).