Reproductive biology

Reproduction

The high species diversity of the tropical rain forest is inevitably associated with low population densities for a majority of species. Most tree species will exist at densities below ten mature individuals per hectare of forest, and many will live in much sparser populations. Tropical ecologists have long been intrigued by the possible ability of tropical tree populations of widely separated individuals to outbreed successfully. In recent years, new techniques for genetically fingerprinting individuals have provided strong evidence that many tropical tree species are strongly outbreeding despite large average distances between trees within a population.

Vegetative reproduction

There have been relatively few studies of vegetative reproduction in tropical trees. However, a number of reports refer to the marked ability of some understorey species to root from plant fragments including stems and leaves (Gartner 1989; Kinsman 1990; Sagers 1993). Shrubs, such as species of Psychotria and Piper, may need to be resilient to damage as they stand a relatively high chance of being broken by falling tree parts or large animals. An ability to re-sprout and produce adventitious roots will allow broken fragments to establish as new plants. Even the large-tree species, Tetramerista glabra, from the peat swamp forests of Borneo has been reported to employ this method of propagation (Gavin & Peart 1997, 1999). Many Tetramerista 'seedlings' are actually sprouts from fallen branches or collapsed saplings.

A wide range of tropical trees are typically multi-stemmed. Palms, pandans and many dicot tree species spread laterally by sprouting from the trunk base or producing root suckers. A few species from tropical Africa (e.g. An-thonotha macrophylla and Scaphopetalum amoenum) are reported habitually to bend over as they grow and when the crown touches the ground to root and send up more shoots, which in turn arch and spread (Richards 1996). When root suckers emerge at a distance from the main trunk it can be difficult to distinguish clones from populations of genetically distinct individuals without close observation. It seems likely that some species in the rain forest are using root suckering to propagate themselves, but there have been few investigations into the phenomenon.

The opposite of one individual appearing as many, many individuals appearing as one, is also seen in tropical trees. Hemiepiphytic figs produce anastamosing aerial root systems by the fusion of separate roots. This union can occur between different fig individuals of the same species, leading to large stranglers that are genetic mosaics derived from two or more plants (Thomson et al. 1991). Somatic mutations within trees could possibly also lead to genetically heterogeneous individuals. Murawski (1998) has provided some preliminary evidence for genetic variation among branches of the same crown, for two trees from French Guiana.

Sexual systems

Plants, unlike animals, show a wide diversity of sexual systems. Truly hermaphrodite, monoecious and dioecious species can be found in the tropical rain forest. Surprisingly similar proportions of the tree flora among these groups have been reported in different neotropical rain forests (Table 4.1). Dioecy-separate male and female trees-is quite common in tropical forests. Monoecy is rarer and is largely confined to palms, figs and members of the Euphorbiaceae.

There was no significant difference in the relative proportion of species among different sexual systems between 'pioneer' and 'persistent' groups at Los Tuxtlas, Mexico (Ibarra-Manriquez & Oyama 1992). In a comparison between dioecious and non-dioecious species, the dioecious species had significantly smaller flowers and more seeds per fruit and a higher proportion of simple as against showy flowers and fleshy rather than dry fruits.

Reviewing descriptions of pollination in tropical dioecious species, Renner & Feil (1993) concluded that vertebrate pollination and exploitation of long-tongued bees were rare in this group. Small insects were the main pollinators. About one third of the dioecious tropical species for which they had data were found not to offer floral rewards to visitors in pistillate flowers. Instead the female flowers mimic the reward-giving male flowers and dupe pollinators into visiting them. Papaya (Carica papaya), nutmeg (Myristica fragrans) and the vegetable ivory palm (Phytelephas seemannii) are examples. In the last named, the female inflorescences produce the same smell as the male ones and attract tiny staphylinid beetles, which normally lay eggs on the decaying male inflorescences (Bernal & Ervik 1996).

Dioecy is the most certain way of ensuring outcrossing. Many species also use temporal differences in the activity of male and female parts to avoid autogamy. Controlled crossing experiments have revealed quite high levels of

Table 4.1. Relative frequency (%) of different sexual systems among the tree flora at various tropical-forest sites

Some of the rows fail to add up to 100% because of a small number of species with mixed sexuality.

Table 4.1. Relative frequency (%) of different sexual systems among the tree flora at various tropical-forest sites

Some of the rows fail to add up to 100% because of a small number of species with mixed sexuality.

Site

Forest type

Reference

Hermaphrodite

Monoecious

Dioecious

La Selva

lowland

Kress & Beach 1994

67

10

23

Barro Colorado Island

lowland

Croat 1979

63

15

21

Los Tuxtlas

lowland

Ibarra-Manriquez & Oyama 1992

63

9

27

Altos de Pipe

montane

Sobrevila & Arroyo 1982

n.d.

n.d.

31

Blue Mountains

montane

Tanner 1982

68

11

21

Canopy and subcanopy classes combined, understorey omitted. The data may include a few non-tree species, but the results are not substantively different from those of Bawa et al. (1985b). Trees.

self-incompatibility in tropical tree species. Some 88% of hermaphrodite tree species (n = 17) studied at La Selva, Costa Rica, were found to be self-incompatible (Kress & Beach 1994). Outbreeding was observed to predominate in the Malaysian rain forest also (Ha et al. 1988a).

An entirely female population of Garcinia scortechinii has been reported from Pasoh, Peninsular Malaysia (Thomas 1997). Agamospermy has been reported before in the genus (Ha et al. 1988b, Richards 1990a), and this and other forms of apomixis are probably present in some species in most tropical forests. Clues to the likely presence of apomixis include very consistent fruit crop size and polyembryony (multiple embryos from one ovule), often observable as more than one seedling germinating per seed.

Genetic diversity

Allozyme analysis and, more recently, DNA fingerprinting techniques have revolutionised our understanding of the genetic structure of tropical forest tree populations. Hamrick (1994), reviewing the published data, concluded that tropical trees have a lower proportion of polymorphic loci and lower levels of heterozygosity per individual than tree species from colder climates. Possibly this is due to smaller effective population sizes in tropical trees because of the low population densities. Despite this, it is clear from allozyme analysis that most tropical canopy species have high outcross-ing rates (Murawski 1995; Doligez & Joly 1997), with multi-locus outcrossing estimates normally above 0.9. Considerably lower values have been recorded, however, particularly in species of Bombacaceae and Dipterocarpaceae. In most species studied, there is more homozygosity in the progeny (seeds) than the adult population, but there is no evidence of a decrease in heterozygosity in the population over the successive generations. This implies a tendency to select against homozygotes among the new recruits, and the existence of inbreeding depression. Lower levels of outcrossing have been observed in years with lower flowering densities, for example in Cavanillesia platanifolia on Barro Colorado Island (Murawski & Hamrick 1992).

Genetic markers have been used to demonstrate successful long-distance pollen dispersal and to infer breeding areas for tropical trees (Table 4.2). Chase et al. (1996) used microsatellite DNA techniques to assign paternity to seeds of known mothers in a population of Pithecellobium elegans in Costa Rica. Mating distance between confirmed parents averaged 142 m, with pollination over 350 m proven. Interestingly, proximity had little influence on likelihood of paternity, the modal class of distance between parents was more than 10 individuals away from the focal tree. Stacy et al. (1996) conducted research on three tree species (Calophyllum longifolium, Spondias mombin and

Table 4.2. Breeding unit parameters estimated for tropical tree species

The breeding unit corresponds to the circular area about a female tree within which 99% of potential mates are expected to occur.

Table 4.2. Breeding unit parameters estimated for tropical tree species

The breeding unit corresponds to the circular area about a female tree within which 99% of potential mates are expected to occur.

Species

Reference

Pollen vector

Density (ha )

Adults (no.)

Area (km )

Radius (km)

Astrocaryum mexicanum

1

beetle

1364

1542

0.011

0.060

Calophyllum longifolium

2

small insect

0.28

35

1.241

0.629

Cordia alliodora

3

small insect

20.9

520

0.249

0.282

Ficus dugandii

4

fig wasp

0.004

252.7

631.7

14.2

Ficus obtusifolia

4

fig wasp

0.072

762.1

105.9

5.8

Ficus popenoei

4

fig wasp

0.013

393.1

294.8

9.7

Pithecellobium elegans

5

hawkmoth

0.88

45

0.636

0.450

Platypodium elegans

6

small bees

0.78

68

0.866

0.525

Spondias mombin

2

small insect

0.33

6

0.196

0.250

Turpinia occidentalis

2

unknown

1.27

5

0.040

0.113

References: 1, Eguiarte et al. (1992); 2, Stacy et al. (1996); 3, Boshier et al. (1995); 4, Nason et al. (1998); 5, Chase et al. (1996); 6, Nason & Hamrick (1997).

Turpinia occidentalis ssp. brevifolia) that occur at low population densities (one mature tree per 2.2 to 6 ha) on Barro Colorado Island and have diminutive flowers pollinated by small generalist insects. Allozyme studies showed that all three species were 100% outcrossed and that they were effectively pollinated over long distances. Multi-locus paternity exclusion analysis showed that for Calophyllum longifolium 62% of effective pollen moved at least 210 m. A small proportion (2.5-5.2%) of successful Spondias mombin pollen moved more than 300 m. Even when pollinated by diverse, small insects, tropical trees can be effectively outcrossed over large distances. However, figs (Ficus spp.) have by far the most effective long-distance dispersal of pollen yet reported from the tropical rain forest, with effective breeding areas of hundreds of square kilometres (Nason et al. 1998).

When to flower?

It can only be favourable for a plant to delay reproduction if the benefits of waiting are greater than the advantages of going ahead at the present time. In other words, if total reproductive output as a larger plant will be greater than a small plant could achieve on average, then flowering should be delayed. Thomas (1996c) found that flower and fruit production follow allometric constants averaging 5.2 for D (stem diameter) and 1.8-2.0 for D H for trees at Pasoh in Peninsular Malaysia. These values are higher than would be predicted by biomechanical considerations of supporting the reproductive organs alone. They indicate a very considerable advantage of tree size in reproductive output. There seems little doubt that allocation of resources to reproduction does compromise growth rates in trees. Thomas (1996b) found evidence of a reduction in height growth with onset of reproductive activity in tropical trees, based on allometric studies (Fig. 4.1). Thus most species grow to relatively large size and then reproduce rather than combining both activities throughout development. But then, why don't all trees grow as big as possible before starting to flower? It is probably a question of risk of mortality. If there is a high chance of death there is no point in delaying reproduction. Fast-growing species that exploit transient high-resource sites such as canopy gaps are at risk of being overtopped by competing individuals. Species in the shade of the understorey risk trees or large branches falling on them from above.

In dioecious species, the cost of reproduction may differ between the sexes. Thomas & LaFrankie (1993) studied five dioecious species in the Euphor-biaceae at Pasoh. They found that the two species of smallest mature stature showed a consistent male bias in the flowering population with a greater variance in size among flowering males than among females. The male bias

Baccaurea Diospyros

Stem diameter (cm)

Figure 4.1 Representative height-diameter relations for six species of tree in two genera at Pasoh Forest Reserve, Peninsular Malaysia. Allometric curves illustrated for each species are least-squares fits of a generalised allometric function. On each graph, the upper dotted line represents the asymptotic maximal height (H' ), and the lower dotted line indicates the estimated height at reproductive onset. After Thomas (1996a).

was particularly marked in the years when relatively few individuals flowered. A male bias in dioecious species is also evident in other published reports. It probably reflects the greater cost of reproduction in females that makes it less feasible for them to reproduce at small size, or in years when conditions do not favour reproduction. This gender difference will be more pronounced in the deep shade of the forest understorey where many of these small-statured species tend to occur.

Most trees reproduce over many years, but there are a few that do so only once. The only reports of monocarpic tropical dicotyledonous trees are some species in the neotropical genera Tachigali (Foster 1977; Richards 1996) and Spathelia (Richards 1996; Young & Augspurger 1991), and the tropical Asian Harmsiopanax (Philipson 1979). The genus Strobilanthes and some other species in the Acanthaceae are monocarpic and gregarious in flowering (Young & Augspurger 1991), events of which occur at long and irregular intervals (Janzen 1976b). These species are mostly herbaceous, but some are woody shrubs of the rain forest.

There is a link between architecture and monocarpy. Most monocarps utilise Holttum's model (Halle et al. 1978): a terminal inflorescence on an unbranched shoot. When the apical meristem switches to producing flowers, vegetative growth must cease and the shoot module must die. This is clearly demonstrated in the palms, which represent the major group of rain forest monocarps. After death of the flowering shoot, suckers may grow from the base to replace the earlier one. Hapaxanthy is the term used to describe this behaviour, which is probably the most common form of monocarpy, at least in the rain forest (Young & Augspurger 1991). Bamboos are often monocar-pic, frequently in synchrony across a population (Janzen 1976b), but it must not be assumed that all species of bamboo fit this pattern and there is no clear evidence of synchronous monocarpy being a common feature of tropical rain-forest bamboo species. The few species of Tachigali that are monocarpic are unique because they are highly branched trees that flower once and die.

The polycarpic majority of trees in the forest shows a wide range of temporal patterns of flowering activity. In a 12-year study of 254 trees from 173 species at La Selva it was found that 7% of species flowered continuously, 55% subannually, 29% annually and 9% supra-annually (Newstrom et al. 1993). Synchronous supra-annual flowering is a notable feature of the forests of West Malesia, which are dominated by the Dipterocarpaceae (Appanah 1985; Ashton et al. 1988). Many theories have been put forward to explain such masting or mass-flowering/fruiting behaviour (Kelly 1994). The predator-satiation hypothesis seems easily the most tenable for tropical examples of masting and will be dealt with later. However, synchronous flowering may also have the advantage of promoting the success of pollination, both in terms of number of pollination events and the likelihood of cross-pollination. Synchronously flowering individuals of the treelet Hybanthus prunifolius showed higher fruit and seed set (86% vs. 58% and 78% vs. 40%, respectively) than those induced to flower at a time different from the main population (Augspurger 1981).

Pollination

The immobility of plants makes it necessary for them to have means of dispersing gametes between sedentary individuals in order to achieve sexual reproduction. In seed plants, pollen is the mobile, though not motile, vector of genetic material. Wind, and sometimes water, may carry the tiny pollen grains, and of the many millions liberated a few will come to land on the stigmas of flowers of the same species. Many plant species rely on animals, generally unwittingly, to carry pollen from flower to flower.

Notable features of the pollination biology of tropical forest trees are the rarity of wind pollination and the wide range of animal pollinators represented. There are some anemophilous species present. The best places to find them are on ridge tops, along seashores and riverbanks. This rarity is not surprising given that the general climatic conditions seem highly unfavourable to the dispersal of pollen on the wind. The high humidity dampens the pollen and causes it to stick together making it difficult for grains to remain airborne. The rain washes the pollen out of the air. The dense canopy filters out the pollen and makes the conditions inside the forest very still, not conducive to pollen dispersal by wind in the understorey. Linskens (1996) could not find any pollen in moss cushions examined in lowland and montane forest in Borneo. Adhesive-coated slide pollen traps also failed to detect any airborne pollen inside the rain forest. Not a single species of angiosperm in the rain forests of central French Guiana is known to be wind-pollinated (Mori & Brown 1994).

It has been estimated that 98-99% of tropical rain-forest plants are animal-pollinated (Bawa 1990). The most important groups of pollinating animals are insects, birds and mammals. The recent discovery of cockroach pollination in an annonaceous liana from Borneo (Nagamitsu & Inoue 1997) makes a sixth order of insects (Blattodea) reported to include pollinating species. The other five orders, Hymenoptera, Coleoptera, Lepidoptera, Diptera and Thysanoptera, are all known as pollinators of tropical trees. Mammals responsible for pollination in tropical trees include bats and to a lesser extent non-volant arboreal mammals. Birds are the final major animal group involved.

There has been an evolutionary tendency for plant species pollinated by the

Table 4.3. Names ofbioticpollination syndromes

Syndrome

Pollinators cantharophily chiropterophily entomophily lepidopterophily melittophily micromelittophily myiophily ornithophily phalaenophily psychophily sapromyiophily sphingophily therophily beetles (Coleoptera) bats (Chiroptera) insects (Insecta) Lepidoptera in general bees (Hymenoptera: Apoidea) small bees flies (Diptera) birds (Aves)

moths (Lepidoptera in part) day-flying Lepidoptera saprozoic and coprozoic flies (Diptera) hawkmoths (Lepidoptera: Sphingidae) non-flying mammals same sort of animal to converge on a similar set of traits in inflorescence and flower morphology and presentation, attractants and rewards. These allow the recognition of a series of pollination syndromes, which in turn may permit the likely pollinating organism to be predicted from the floral traits of a species. However, caution is necessary in accepting the results of such extrapolations. Pollinators often visit flowers that are not 'typical' for them. Some species are visited by a wide range of organisms and careful observations are needed to confirm which species are the effective pollinators. For example, inflorescences of Artocarpus species are visited by many nocturnal insects including moths, flies, beetles and cockroaches (Momose et al. 1998a).

There follows a summary of the most important pollination syndromes found in tropical trees. These notes include information on the pollinators, examples of the plants they pollinate, common features of floral design and reference to case studies of pollination involving the pollinator group in question. The names of the pollination syndromes are given in Table 4.3. Important sources of general information about pollination syndromes not directly referred to include Bawa (1990), Prance (1985), Endress (1994) and Fffigri & van der Pijl (1979).

Pollination syndromes

Bats pollinator

Bats comprise two suborders of the mammals. The Megachiroptera are restricted to the Old World where they are frequently agents of pollination and seed dispersal for tropical trees. Microchiropterans perform this role in the New World.

flowers

Despite pollination being performed by different bat lineages in the palaeo-and neotropics, the bat-flower syndrome is quite uniform. Flowers open in the evening to coincide with the largely nocturnal foraging of the pollinators. They are usually large and pale with a distinctive musky, fermented odour and copious nectar. The flowers are mostly held away from the foliage to allow easy detection and access by the bats (Fig. 4.2). This is often acheived by having the flowers on the ends of branches held above, or dangling below the main crown. Alternatively, cauliflory or ramiflory are often associated with bat-pollination. The individual flowers are either large and robust or small and aggregated into many-flowered inflorescences that present a shaving brush-like array to the visiting bat (e.g. Parkia). Large bat-flowers are either the brush type with many long stamens, e.g. Adansonia, Barringtonia, or big, thick fleshy bowls, e.g. Oroxylum indicum, Fagraea racemosa . The large size of bats in comparison to most other pollinators often means that bat-pollinated species have bigger flowers than most other members of their genus or even family. New World bat-flowers tend to produce hexose-rich nectar whereas the Old World equivalents secrete nectar with abundant sucrose (Baker & Baker 1983; Baker et al. 1998). Whether this reflects a difference between micro- and megachiropterans remains unclear. Bat-flowers are possibly the most nectariferous of all flowers, with copious, often mucilaginous, nectar and abundant pollen. This clearly makes bat-pollination an expensive undertaking for the plant. The benefits gained, however, are the long flights of bats, securing cross-pollination with distant individuals.

plants

Many tropical rain-forest tree species that are bat-pollinated are from the families Bignoniaceae, Bombacaceae and Myrtaceae. The syndrome is also quite common in Leguminosae subfamily Caesalpinioideae. The Cary-ocaraceae are a small neotropical family of which all members are believed to be bat-pollinated.

case studies

Bat pollination is the subject of a book (Dobat & Peikert-Holle 1985). Hopkins (1984) conducted research on the pollination of the pantropical caesalpinoid genus Parkia. The flowers of Ceiba pentandra were visited by a wide range of both diurnal and nocturnal animals in Central Amazonia, but only two species of phyllostomid bat actually pollinated them (Gribel et al. 1999). A bat-pollinated understorey palm was studied by Cunningham (1995). The Australian rain-forest tree Syzygium cormiflorum is largely bat pollinated (Crome & Irvine 1986). Several species of the genus Lafoensia (Lythraceae) were reported to be pollinated by bats in the Atlantic forests of

Kato (1996) reports this species to be pollinated by anthophorid bees. This is probably a reflection of the taxonomic problems (Wong 1996) associated with this species or group of species.

Trees Peat Swamp Forest

Figure 4.2 The positions of flowers on some Malaysian chiropterophilous trees. 1. Musaceae: Musa species. 2. Palmae: Cocos nucifera. 3. Arenga pinnata. 4. Anacardiaceae: Mangifera indica. 5. Bignoniaceae: Oroxylum indicum. 6. Pajanelia longifolia. 7. Bombacaceae: Bombax valetonii. 8. Ceiba pentandra. 9a. Durio zibethinus. 9b. Durio graveolens. 10. Lecythidaceae: Barringtonia racemosa. 11. Mimosaceae: Parkia species. 12. Myrtaceae: Syzygium malaccense. 13. Sonneratiaceae: Duabanga grandiflora. 14. Son-neratia alba/ovata. 15. Sonneratia caseolaris. After Marshall (1983).

Figure 4.2 The positions of flowers on some Malaysian chiropterophilous trees. 1. Musaceae: Musa species. 2. Palmae: Cocos nucifera. 3. Arenga pinnata. 4. Anacardiaceae: Mangifera indica. 5. Bignoniaceae: Oroxylum indicum. 6. Pajanelia longifolia. 7. Bombacaceae: Bombax valetonii. 8. Ceiba pentandra. 9a. Durio zibethinus. 9b. Durio graveolens. 10. Lecythidaceae: Barringtonia racemosa. 11. Mimosaceae: Parkia species. 12. Myrtaceae: Syzygium malaccense. 13. Sonneratiaceae: Duabanga grandiflora. 14. Son-neratia alba/ovata. 15. Sonneratia caseolaris. After Marshall (1983).

Brazil (Sazima et al. 1999). Gould (1978) investigated the flower and inflorescence form and nectar production in Oroxylum indicum in relation to the behaviour of pollinating bats.

Non-volant mammals pollinator

Arboreal mammals including primates, marsupials and rodents have been suspected of being involved in pollination of tropical trees, but studies confirming pollen transfer, not just flower-visiting, are relatively few (Janson et al. 1981; Bawa 1990; Carthew & Goldingay 1997). The syndrome seems better defined in the shrublands of Australia and southern Africa. Primates will often eat flowers and in so doing may become liberally dusted with pollen but it seems probable that in relatively few cases are they effective pollinators, and are more likely to have a deleterious effect due to flower damage and removal.

flowers

There are probably too few tree species designed for pollination by arboreal mammals to recognise a typical flower form. Diurnal and nocturnal pollinating species may even select for different floral traits (Carthew & Goldingay 1997), with dull-coloured but odoriferous blooms attracting night foragers and brightly hued and weakly scented flowers those species active during daylight hours.

plants

A taxonomically diverse group of species has been associated with non-volant-mammal pollination (Carthew & Goldingay 1997). There is as yet no evidence of any families or genera of tropical trees being particularly specialised for pollination by arboreal mammals.

case studies

The South American bombacaceous tree Matisia cordata produces bright yellow flowers on its branches that attracted a range of both diurnal and nocturnal primates and marsupials (Janson et al. 1981). Despite damage to the flowers by these visitors attracted to the copious nectar, fruit set was high. Birds and butterflies were also seen to attend flowering trees. Similarly, flowering individuals of the Central African Daniellia pynaertii (Legumin-osae; Caesalpinioideae) attracted four species of diurnal primate (Gautier-Hion & Maisels 1994), yet still had large fruit crops. Few other potential pollinators were observed to visit the trees. A dormouse and two species of prosimian might act as pollinators of Parkia bicolor in Cameroon (Griin-meier 1990), although bats are probably the main agents of pollen dispersal. Momose et al. (1998d) report a squirrel-pollinated species of Ganua (Sapotaceae) from Sarawak. The sweet and fleshy berry-like corolla of the tree was the reward for the foraging squirrels. However, F»gri & van der Pijl (1979) considered the members of the Sapotaceae with corollas that act as food rewards to be bat-pollinated. The green, scentless flowers of the hemi-epiphytic shrub Blakea chlorantha (Melastomataceae) found in montane Costa Rica attracted two species of rat that are believed to pollinate the plant (Lumer 1980).

Birds pollinator

There are several families of nectarivorous bird found in the tropics that are important pollinators. According to the ranking of Stiles (1981), the hummingbirds (Trochilidae) are the family most uniformly specialised for exploiting flowers. Hummingbirds are confined to the New World, with many of the more than 300 species found in humid tropical forests. The next most specialised are the sunbirds and spiderhunters (Nectariniidae), which are an Old World group. Honeyeaters (Meliphagidae) and Hawaiian honey-creepers (Drepaniidae) are somewhat less specialised. The lorikeets (Psitta-

Gnarled Tree Drawing

Figure 4.3 A golden-winged parakeet visiting a Moronobea coccinea flower. The parakeet inserts its beak in the flower apex, contacting the anthers and stigmatic lobes. Drawn by Alexandre Kirovsky. From Vicentini & Fischer (1999). Copyrighted 1999 by the Association for Tropical Biology, P.O. Box 1897, Lawrence, KS 66044-8897. Reprinted by permission.

Figure 4.3 A golden-winged parakeet visiting a Moronobea coccinea flower. The parakeet inserts its beak in the flower apex, contacting the anthers and stigmatic lobes. Drawn by Alexandre Kirovsky. From Vicentini & Fischer (1999). Copyrighted 1999 by the Association for Tropical Biology, P.O. Box 1897, Lawrence, KS 66044-8897. Reprinted by permission.

cidae; Loriinae) regularly feed from flowers, but tend to be destructive. Some species of white-eye (Zosteropidae) and honeycreeper (Coerebidae) are also specialised flower visitors. Many small omnivorous birds such as starlings (Sturnidae) and bulbuls (Pycnonotidae) will feed on nectar if it is available and accessible. Hummingbirds are the only family where most foraging is done while in flight by hovering near the flower. Sunbirds are capable of hovering, but perch if a perch is available. This difference in foraging styles is reflected in floral morphology (Westerkamp 1990).

flowers

Bird-flowers are typically diurnal and scentless. Birds, it is widely believed, have limited abilities at olfaction, but they generally have excellent colour vision. Red is a common bird-flower colour, and as insects have a poor capacity to distinguish red it makes this a good colour as a general attractant for birds. Yellow, often in combination with red, is another tint favoured by flowers designed to attract birds. Bird-flowers often have long tubular co-

rollas, sometimes with reflexed lobes at the tube mouth, what Endress has called the 'dogfish flower.' The long corolla tubes match the long beaks of the pollinating birds, a probable example of co-evolution. However, in a study of avian flower visitors in New Guinea there did not appear to be much congruence between floral morphology and beak form (Brown & Hopkins 1995). The flowers are fairly robust, often with inferior ovaries to protect the ovules from the quite large visitors. Another bird-flower form is the brush flower with an array of long stamens as seen in Calliandra. Hummingbird-flowers are usually held singly, or in clusters, in a horizontal or pendent position on flexible pedicels. The flowers produce large quantities of nectar, which appears to be the sole reward offered by bird-flowers (Stiles 1981). This generally has low concentrations of sugars and amino acids. Hummingbird-flowers tend to produce sucrose-rich nectar (Baker & Baker 1983; Baker et al. 1998), whereas bird-flowers from the palaeotropics are more likely to be rich in glucose and fructose. Many birds are thought to be physiologically intolerant of sucrose.

plants

Erythrina, Spathodea and probably Hibiscus are tropical tree genera with bird-pollinated members. The species of Rhododendron with brightly coloured flowers found on tropical mountains are mostly bird-pollinated. In the cooler climates of the mountains birds are probably more active than insects.

case studies

There has been surprisingly little research that focuses on bird-pollination of tropical trees. The classic studies of hummingbirds as pollinators in rain forests (see, for example, Stiles 1975, 1978) largely concern herbaceous and epiphytic species. However, Symphonia globulifera is pollinated by hummingbirds in Central Amazonia (Bittrich & Amaral 1996a). Perching birds may also be involved in pollination in the neotropics. Toledo (1977) outlined evidence for a range of small birds being involved in the pollination of two bombacaceous trees, Bernoullia flammea and Ceiba pentandra, in the rain forests of Southern Mexico. The latter is generally considered chirop-terophilous, but birds may forage for nectar during the day. Vicentini & Fischer (1999) have given an account of the pollination of the Central Amazonian canopy tree Moronobea coccinea (Guttiferae) by the golden-winged parakeet (Brotogeris chrysopterus) (Fig. 4.3). Among the bananas (Musaceae) there are bat- and bird-pollinated species. Itino et al. (1991) compared the chiropterophilous Musa acuminata ssp. halabensis with the ornithophilous Musa salaccensis at a site in Sumatra. The bat-pollinated banana had pendent inflorescences with dark purple bracts and gelatinous sugary nectar. Sunbird-pollinated Musa salaccensis had erect inflorescences with paler pink-purple bracts and less sweet and runnier nectar.

Bees pollinator

Current evidence points to bees as the most important pollinating organisms in tropical forests. They can be divided into two pollination guilds according to size: the medium- to large-sized species in the families Andrenidae, Apidae, Anthophoridae, Halictidae and Megachilidae and the small bees in the Apidae (Apini), Halictidae and Megachilidae. Some wasps also fall into the small-bee guild. The two groups are heterogeneous in terms of taxonomy, behaviour and ecology.

Bees are specialist foragers after pollen and nectar and are very efficient at doing so (Fig. 4.4). They are the only group capable of buzz-pollination, with the possible exception of some hoverflies (Syrphidae). That is the stimulation of pollen release from poricidal anthers by vibrating (buzzing) them at the correct frequency (Buchmann 1983). Big bees are more prevalent in the forest canopy, small bees in the understorey. Xylocopa (An-thophoridae) is a good example of a big-bee genus, members of which are able long-distance high-fidelity pollinators, but tend to be forest margin species, and their low numbers make them unreliable as pollinators for big trees. The euglossines (Apidae; Euglossini) are a neotropical group that are important long-tongued pollinators. At Lambir Hills National Park in Sarawak, the honeybee Apis dorsata was found to be an important pollinator during mass (general) flowering in the rain-forest community (Momose et al. 1998d). The number of colonies increased dramatically during this period. This bee is unusual in that it forages for an hour or two before dawn and after dusk. Some tree species at Lambir may open flowers at night to give Apis dorsata sole access to the flowers during their crepuscular activity periods.

flowers

Bee-flowers are extremely varied in morphology, from small, simple, open flowers to complex structures that require particular modes of entry to obtain the floral reward. Specialist big-bee-flowers are often brightly coloured, sometimes with nectar guides, markings on the petals directing the bee to the appropriate place to forage for nectar and pick up or deposit pollen. Nectar and/or pollen are the rewards in bee flowers. Bees are often early morning foragers, so bee-flowers open early, sometimes during the night before. Small-bee-flowers are generally small, white or cream and short-tubed.

plants

Leguminosae, Bignoniaceae and Melastomataceae often possess specialised bee-flowers, including poricidal anthers that require buzz-pollination. Bur-seraceae, Euphorbiaceae, Flacourtiaceae, Lecythidaceae and Sapotaceae are often equipped with less specialised bee-flowers. Tropical trees of the Mal-pighiaceae and Melastomataceae tribe Memecyleae have been shown to bear

Figure 4.4 Trigonid bee (Trigona erythrogastra) on Melastoma malabath-ricum flower in Lambir Hills National Park, Sarawak. Photo: Tamiji Inoue.

flowers offering oils rather than sugary nectar as rewards to bees (Buchmann & Buchmann 1981; Buchmann 1987). Species of Clusia and Dalechampia (mostly climbers) provide resin as a reward to flower visitors (Armbruster 1984; Bittrich & Amaral 1996b; Lopes & Machado 1998). This is collected by bees to use in building their nests (Armbruster 1984).

case studies

Perry & Starrett (1980) found that the emergent Dipteryx panamensis was pollinated by at least 13 species of bee. Medium-sized stingless bees (Trigona, Apidae) are pollinators of the large dipterocarp Dryobalanops lanceolata in Sarawak (Momose et al. 1996). Similar bees pollinate Garcinia hombroniana in Peninsular Malaysia (Richards 1990b). The palm Prestoea decurrens is probably mostly bee-pollinated (Ervik & Bernal 1996). Trigonid bees and drosophilid flies are duped into visiting unrewarding pistillate flowers of the protandrous palm Geonoma macrostachys in Ecuador, because of their similarity to the rewarding staminate blooms (Olesen & Balslev 1990). The Mexican understorey shrub Dalechampia spathulata is visited by male Eu-glossine bees that collect aromatic substances from an extra-floral gland in the inflorescences (Armbruster & Webster 1979).

Moths pollinator

Hawkmoths (Sphingidae) are the commonest moth pollinators, but some species of Noctuidae, Pyralidae and Geometridae are probably also involved. Hawkmoths have the longest tongues of any insect group, are excellent hoverers and are generally nocturnal. They appear to be rare in the mountains, probably because of the low temperatures.

flowers

Moth-pollinated flowers are typically heavily scented (strong and sweet), particularly at night, pale-coloured, and nectariferous with long tubular corollas or spurs, and nocturnal anthesis. An alternative flower form is that of the relatively small corolla with many long exerted stamens as seen in the Capparidaceae. Flowers designed for sphingid visitors can be fairly delicate, even pendulous, as the insect does not need to land. Noctuids have short proboscides and therefore the phalaenophilous flowers are short-tubed. Lepidopteran-pollinated flowers tend to produce sucrose-rich nectar (Baker & Baker 1983).

plants

Tropical tree families that contain moth-pollinated species include the Rubiaceae, Apocynaceae, Meliaceae, Solanaceae (e.g. Datura) and Leg-uminosae (subfamily Mimosoideae).

case studies

Prance (1985) provided a comparison of moth and butterfly pollination in two genera of the Chrysobalanaceae of Amazonia. The discovery of moth-pollination in Gnetum (Kato & Inoue 1994; Kato et al. 1995) (Fig. 4.5) has interesting implications for the evolutionary origins of insect pollination. The Madagascan shrub Ixora platythyrsa is visited by noctuid and geomet-rid moths (Nilsson et al. 1990). The markedly protandrous flowers have a secondary pollen-presentation mechanism to facilitate pollination by the moths. The pollen is released onto the unripe stylar heads from where it is picked up by the proboscides of the moths. Linhart & Mendenhall (1977) used dyed pollen to demonstrate pollen movement of more than 350 m by hawkmoths that pollinated the rubiaceous shrub Lindenia rivalis in Belize. The plants, which grow along watercourses, were visited regularly by the sphingids, which appeared to have set routes for foraging. Chase et al. (1996) used genetic markers to show that the hawkmoths can effectively pollinate Pithecellobium elegans over long distances.

Butterflies pollinator

Butterflies are the other group of the Lepidoptera that is involved in pollination. Butterflies are active during the day, have shorter proboscides than hawkmoths and alight on their chosen flowers before feeding.

flowers

Butterfly flowers usually have long tubular corollas or spurs, and are brightly coloured, often in shades of orange, red or pink, or contrasting combinations of the same, to attract day-flying butterflies to the nectar reward. In large flowers there is usually a landing platform and exserted stamens and style imprecisely deposit, or pick up, pollen from the visiting butterfly. Alternatively, small flowers aggregated in an inflorescence create a landing platform.

plants

Tropical tree genera such as Delonix, Caesalpinia, Lantana, Cordia and Mussaenda are believed to be butterfly-pollinated.

case studies

Xerospermum intermedium, a common tree at Pasoh in Peninsular Malaysia,

Figure 4.5 Moth (Herpetogramma sp.) on Gnetum gnemon strobilus. Photo: Tamiji Inoue.

was visited by trigonid bees and butterflies (Appanah 1982). Kato (1996) reported Ixora griffithii, an understorey shrub, to be pollinated by papilionid butterflies, as well as xylocopine bees, at Lambir in Sarawak. Gardenia actinocarpa is a rare, dioecious shrub endemic to the rain forests of northern Queensland that is pollinated by butterflies (Osunkoya 1999).

Beetles pollinator

The pollinating coleopterans are a very diverse group, ranging in size from tiny weevils and staphylinids to large scarabs. Beetle pollination was long believed to be the primitive angiosperm condition. However, recent debate over the actual nature of the earliest angiosperms, and the finding that the more primitive extant Magnoliidae are not beetle-pollinated, rather dampens that view. Nevertheless, beetle pollination is very important in tropical forests in both families thought of as primitive and those considered relatively advanced. As Endress remarked, beetles are uncouth floral visitors, performing 'mess-and-soil' pollination. The beetles blunder around the flowers chewing parts, apparently indiscriminately, and becoming covered in pollen.

flowers

Beetle-pollinated flowers of tropical trees are quite variable in construction, ranging from small (e.g. palm flowers) to quite large (a few centimetres across in some Annonaceae). They are usually quite open-the beetle traps of the aroids and waterlilies are not encountered among tropical trees-with a strong smell and plentiful pollen. Thermogenicity is sometimes involved in attracting the beetles. Temperatures 6 K above ambient have been recorded in Annona sericea. Palms have many small flowers on large inflorescences, and are often beetle-pollinated.

plants

Annonaceae, Lauraceae and Myristicaceae are important tropical tree families with many beetle-pollinated species (Schatz 1990; Irvine & Armstrong 1990). Eupomatiaceae, Degeneriaceae (Thien 1980) and Winteraceae are examples of other, relatively primitive, cantharophilous families. Among the monocots, the Palmae and the Cyclanthaceae attract beetles (Henderson 1986; Schatz 1990).

case studies

The beetle pollination of various nutmeg species has been studied in detail in Australia (Armstrong 1997). Palms found to be beetle-pollinated include Bactris porschiana (Beach 1984), B. gasipaes, B. bifida and B. montícola (Listabarth 1996), Cryosophila albida (Henderson 1984), Phytelephas seemannii (Bernal & Ervik 1996) and Socratea exorrhiza (Henderson 1985). Momose et al. (1998d) report that chrysomelid beetles are the pollinators of many dipterocarp species during general flowering at Lambir in Sarawak

(Fig. 4.6). In tropical Queensland, beetles have been found to be important pollinators of rain-forest trees. Tree species involved include Diospyros pentamera (House 1989), Flindersia brayleyana, Alphitonia petriei and Eu-pomatia laurina (Irvine & Armstrong 1990). Eupomatia is dependent on a tiny weevil for pollination. This species (Elleschodes hamiltoni) breeds in the synandria of the flowers and hence is dependent on the tree also.

Various small flying insects pollinator

This is a catch-all category for relatively unspecialised flowers thought to be visited by small insects. These will include thripses2 (Thysanoptera).

flowers

Small and unspecialised flowers characterise this group. Thripses appear to be attracted to white, perfumed flowers.

plants

Families such as Anacardiaceae, Euphorbiaceae and Guttiferae often have small, unspecialised flowers.

case studies

Sympatric species of Shorea section Mutica have been shown to be thrips-pollinated in Peninsular Malaysia (Chan & Appanah 1980). The tiny insects reproduce inside the flowers and rapidly increase in population numbers, resulting in a high chance of pollination during a general flowering event. In other regions, endemic dipterocarps have been reported to use different pollinators: bees in Sri Lanka (Dayanandan et al. 1990) and chrysomelid beetles in Sarawak (Momose et al. 1998d). Sakai et al. (1999) found that Shoreaparvifolia, which had been reported as thrips-pollinated in the Malay Peninsula, was probably more effectively pollinated by chrysomelid beetles at Lambir Hills National Park in Sarawak. Several tropical Annonaceae are apparently thrips-pollinated. In Sarawak Popowia pisocarpa is visited by thysanopterans (Momose et al. 1998c), as are Bocageopsis multiflora and Oxandra euneura in Amazonia (Webber & Gottsberger 1995).

Flies pollinator

Flies (Diptera) are possibly the second most important group of insect pollinators in the rain forest, although myiophily has been very little studied. Relatively few species of fly appear to be dependent on flowers for food. They can be attracted by using a variety of means, including odours and nectar. Saprophilous (carrion and dung) flies can be employed as pollinators

The English name for these insects is derived from the generic name Thrips, leading to the apparently infantile plural.

Figure 4.6 Flowers of Shorea parvifolia being visited by chrysomelid beetles (Monolepta sp.). Photo: Tamiji Inoue.

through floral form and odour imitating the preferred food of these flies. flowers

Small, pale flowers with nectar attract flies, particularly hoverflies (Syr-phidae). Sapromyiophily is not common in tropical trees.

plants

Sterculiaceae have been reported as fly-pollinated, although Momose et al. (1998d) state that the species at Lambir are mostly beetle-pollinated.

case studies

Cocoa (Theobroma cacao) is principally pollinated by tiny midges of the family Ceratopogonidae (Young 1982). House (1989) found that dipterans were the most abundant flower visitors for two lauraceous trees in the Queensland rain forest, Neolitsea dealbata and Litsea leefeana, and that they were probably the most effective pollinators. Thien (1980) reported fly pollination of Drimyspiperata (Winteraceae) in the montane forests of New Guinea. Schmid (1970) described syrphid fly pollination of the palm Aster-ogyne martiana. A hoverfly (Copestylum sp.) was probably the most efficient pollinator among many insect flower visitors of another understorey palm, Prestoea schultzeana, in Amazonian Ecuador (Ervik & Feil 1997).

Wind pollinator

The wind is not a very reliable pollinator in the tropics, as outlined above. flowers

Small, often with many flowers in an inflorescence. The perianth is often reduced and there is no nectar or perfume. Pollen is produced in large amounts and the stigmas are often feathery to improve pollen capture from the air.

plants

Tropical conifers are probably wind-pollinated (Richards 1996). Some palm and pandan (screw-pine) species may be also.

case studies

Wind pollination is not entirely absent from the rain-forest understorey. There is some evidence that it may occur quite widely in the understorey Moraceae. The small Central American tree Trophis involucrata has explosive anthesis (Bawa & Crisp 1980), as does Streblus brunonianus from Australia (Williams & Adam 1993).

Tropical flowers

Endress (1994) notes a number of special features of flowers in the tropics, which are relevant to a discussion of tropical rain-forest trees. The rarity of wind pollination has already been mentioned. The presence of some very large flowers is notable. With large pollinators, such as birds and bats and even substantial bees and beetles, lone individual flowers, if they are to attract pollinators and survive their visitation, need to be big. There are many small-flowered species in the rain forest, but the range of flower size is very wide. There are probably also more short-lived flowers in the tropics than elsewhere. Such flowers are usually only receptive for a single day. This probably reflects an abundance of 'trap-lining' pollinators. Trap-liners are species that visit individual plants on a regular basis to exploit their floral resources, as a trapper visits a set of traps in repeated, routine fashion to collect what has been caught and re-set the trap. Trap-lining pollinaters include species of bat, bird, bee, butterfly and moth. Trap-liners are advantageous as pollinators because they often move long distances between flower visits and frequently specialise on relatively few species. The propensities of trap-liners tend to improve the chances of pollen being transferred between distant individuals of the same species. Plants can encourage trap-liners by the regular production of few flowers over a long flowering season. The pollinators then visit the plant on a consistent basis. The relatively small floral

Lambir -

La Selva -

Lambir -Canopy

La Selva -

Lambir -Subcanopy

La Selva -

0 20 40 60 80 100

Percentage of Tree Species

Figure 4.7 Relative frequencies of pollinator type among tree species at La Selva, Costa Rica, and Lambir, Malaysia. Comparisons are given for all trees and for canopy and subcanopy components. Data from Kress & Beach (1994) and Momose et al. (1998d).

display does not attract many opportunist exploiters of flowers, but is sufficient to maintain daily attendance by the reliable pollinators. Hence the presence of one-day flowers in tropical forests.

A great variety of positions on the tree for the production of flowers is another feature of the tropical forest. Flowers are generally borne at the ends of twigs, but in some species flowers or inflorescences can arise from the branches, the trunk or even the roots. A few species also exhibit epiphyllous flowers. Ramiflory, cauliflory and rhizoflory are probably adaptations to exploit pollinators and/or seed dispersers active in the forest understorey.

Relative importance of different pollinators

There are only two tropical rain-forest sites where detailed studies of pollination of a large number of tree species have been conducted. These are La Selva in Costa Rica (Bawa et al. 1985a; Kress & Beach 1994) and Lambir Hills National Park in Sarawak (Momose et al. 1998d). At La Selva, bees are the most important pollinators, particularly in the upper layers of the forest. Small diverse insects are second and moths third in importance (Fig. 4.7). Vertebrate pollination is relatively rare in the canopy, being commoner

Lambir -

La Selva -

Lambir -Canopy

La Selva -

Lambir -Subcanopy

La Selva -

0 20 40 60 80 100

Percentage of Tree Species

Figure 4.7 Relative frequencies of pollinator type among tree species at La Selva, Costa Rica, and Lambir, Malaysia. Comparisons are given for all trees and for canopy and subcanopy components. Data from Kress & Beach (1994) and Momose et al. (1998d).

among the large herbs (Heliconia spp. and other Zingiberales). The under-storey generally exhibits a greater diversity of pollination syndromes than the canopy. The dipterocarp forest at Lambir differs from La Selva in having fewer trap-lining pollinator species. This may be because of the mass-flowering pattern of the community with fewer species flowering regularly. The use of migratory bees to allow adequate pollination during the mass flowering means that there is less selection pressure in favour of maintaining pollinator numbers all the time. The report that possibly herbivorous chrysomelid beetles are important pollinators of dipterocarp species during the general-flowering events provokes the fascinating speculation that dipterocarps may maintain their pollinators by providing foliage as food. The forest community at Lambir shows greater reliance on beetles, particularly the canopy species, and small bees than that at La Selva, but contains fewer species pollinated by moths and the small-diverse-insect group.

Momose et al. (1998b) have proposed that much of the vertical variation in pollinator type (specialist versus generalist) and interval between reproductive events in the tropical rain forest can be explained in terms of display effects. They have developed a mathematical model based on the premise that large plants can produce large displays that attract more generalist pollinators and increase pollination success. Canopy trees with large stature and low rates of mortality can maximise pollination success by producing huge displays at long intervals. Small, understorey plants are unable to compete in terms of attracting generalist pollinators with floral displays and therefore employ specialist pollinators. The greater risk of mortality in the lower parts of the forest also makes it risky to delay reproduction for long intervals, therefore flowering is predicted to be more frequent in the understorey. These general predictions, greater use of generalist pollinators and longer reproductive intervals in the canopy compared to the understorey, appear to fit with observations at Lambir Hills National Park (Momose et al.1998d).

Grubb & Stevens (1985) found an increasing frequency of ornithophilous and anemophilous species with altitude in forests on the mountains of New Guinea.

Figs

Figs are members of the genus Ficus in the family Moraceae. The many species share the syconium as the form of inflorescence and the use of tiny wasps as pollinators. Otherwise, the figs show a huge diversity of form from small shrubs and climbers to huge trees and stranglers. Figs are unique in the tropical rain forest in that each species has its own obligate pollinating species. Despite being tiny and unable to survive for long, recent studies employing genetic markers have shown that fig wasps are very effective long-distance pollinators. The tiny fig wasps are probably dispersed on the wind, but once near a fig tree of the correct species at the right stage of syconium development they can fly to the ostiole of an inflorescence and make their way inside. Concomitant to the necessity of maintaining populations of the fig wasps that have relatively short life-cycle times and short adult lives is the virtually continuous reproductive activity of a fig population. This results in a regular fruit supply. Fig fruits (mostly made up of the fleshy receptacle of the syconium) are palatable to many frugivorous animals and because of their regular availability they can be relied on in periods of relative fruit scarcity. For this reason, figs have been termed keystone species in tropical rain forests because of their role in seeing frugivore communities through hard times (Terborgh 1986). Fig fruits are also relatively high in calcium concentration compared with other fruits (O'Brien et al. 1998) which will increase their nutritional importance to frugivores. However, in some forests figs are too rare to represent keystone resources (Gautier-Hion & Michaloud 1989).

Dispersal mechanisms

After successful pollination, fertilised ovules will develop into seeds and the ovary will become a fruit. The seeds, the offspring of the tree, will then require to leave their mother plant in order to establish as new individuals. There are four main agents of seed dispersal: gravity, wind, water and animals. Their relative importance in the dispersal of a species allows its classification as autochorous, anemochorous, hydrochorous or zoochorous. In addition to the primary dispersal of the seed from the tree, there may also be secondary dispersal by another agent from the first landing site. For instance, there is growing evidence of an important role played by ants in removing tiny seeds from animal droppings and dispersing them further (Roberts & Heithaus 1986; Kaufman et al. 1991; Levey & Byrne 1993).

Autochory

Autochorous species include those with explosive dehiscence (ballis-tochores) and those with apparently no other means of dispersal than falling off the parent tree. The biggest seed of all, the double coconut or coco-de-mer Lodoicea maldivica, is an example of the latter. Unlike the true coconut, it cannot survive long immersed in water and is therefore not hydrochorous. In the rain forest, the Euphorbiaceae (the rubber tree Hevea brasiliensis is a good example), Leguminosae and Bombacaceae are the families most likely to be present as autochorous tree species. Nearly 60% of seeds fall less than 10 m away from the parent plant in ballistochorous Eperua falcata in French Guiana (Forget 1989), with maximal dispersal distance of 30 m. An 11 m tree of Hura crepitans growing in an open site in Ghana did somewhat better, sending seeds up to 45 m, with a modal dispersal distance of 30 m (Swaine & Beer 1977).

Anemochory

Wind-dispersal involves modification in the form of the disseminule to increase its time of descent. This is achieved by either the use of wings, hairs or plumes or a reduction to very small size. Augspurger (1986) introduced a functional terminology for anemochores (Table 4.4). She found that the winged disseminules fell significantly more slowly than the floaters. Wind direction and force at the time of fruit maturity will be highly influential on the spatial distribution of dispersed seeds of anemochorous species. The density patterns for seeds dispersed from two parent trees of Tachigali versicolor showed a strong skew in the direction of the prevailing wind (Fig. 4.8).

The taller a tree, the greater the release height for anemochores and the longer the period of descent. It has often been argued therefore that anem-ochory should be favoured in tall species. Short trees in the forest understorey are rarely exposed to high winds that facilitate anemochore dispersal and the low release height does not allow prolonged descent. In a study of the rolling autogyro disseminules of Lophopetalum wightianum, Sinha & Davidar (1992) did indeed find that tall trees had a significant dispersal advantage (Fig. 4.9). Average and maximum dispersal distances increased with tree height. Most surveys of dispersal type among tropical forest tree species have found an increase in abundance of anemochory (or at least possession of dry rather than fleshy fruits) in taller trees (see Table 4.5).

Wind dispersal also seems to become commoner at higher elevations (Table 4.6; Grubb & Stevens 1985), and in drier forests (Gentry 1982). Suzuki & Ashton (1996) report that among members of the largely anemochorous Dipterocarpaceae wingless fruits tend to occur in understorey, riverine or very large-seeded species. The riverine species are hydrochorous and the investment needed in wings for very large seeds is probably too big to be worth while.

Wind dispersal tends to be poorly effective; for instance, in the tall Indonesian rain-forest tree Swintonia schwenkii few seeds landed more than 50 m from the parent (Fig. 4.10). Important families of tropical trees with many anemochorous species include the Bignoniaceae, Bombacaceae, Leg-uminosae, Vochysiaceae, Dipterocarpaceae and Apocynaceae. Anemochory appears to be restricted to advanced subclasses of flowering plants in French

Table 4.4. A functional classification of anemochores.

Type

Description

Examples

Dust diaspores

Floaters

Undulators

True gliders

Tumblers

Helicopters

Autogyros

Rolling autogyros microscopic seeds so small they float on the lightest breeze plumed fruits or seeds where feathery hairs provide buoyancy reducing the rate of descent flat, thin disseminules that glide and undulate downwards, with frequent stalls, like falling sheets of paper similar to undulators, but better aerodynamic performance allows them to glide forwards in still air rotate about an axis parallel to the ground as they fall; they often resemble tiny paddle wheels spin about their central axis as they fall, with wings above to provide lift winged disseminules that spiral around one end (usually where the seed is placed) of their length as they fall a form of autogyro where the disseminule rotates about its long axis while spiralling around one end; the seed tends to be more centrally placed on the

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