Rhizophora apiculata Blume, 1827
Bakau minyak
"One of the most common mangrove tree species"


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Features of R. apiculata. Top-left: Flowers on short bracts. Bottom-left 1: Eye-shaped leaves. Bottom-left 2: Stilt roots and aerial roots. Top-right: Grey bark with vertical fissures. Bottom-right: Cylindrical propagule. (Photo: Wild Singapore)



Basic Information


Name

Binomial: Rhizophora apiculata Blume, 1827
Vernacular: Bakau minyak, Bakau putih, Bakau tandok (Tan, 2008), Corky stilt mangrove (Duke, 2006a), Tall stilt-root mangrove (Wightman, 2006), Tall-stilted mangrove (Lovelock, 1993)

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First description of R. apiculata (Blume, 1827).

Etymology

Rhizo-phora means 'root bearing' in Greek, referring to the stilt roots characteristic of the genus. apiculata means 'to end abruptly' in Latin, referring to the leaf apex (Duke, 2006; Wightman, 2006).
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R. apiculata has numerous stilt roots emerging from the stem. (Photo: Wild Singapore)

Leaf - � Pierre GRARD - IFP
Leaf - � Pierre GRARD - IFP

The leaf apex of R. apiculata is abrupt and pointed. (Photo: Checklist of Mangrove species of South East India and Sri Lanka)


Taxonavigation
Kingdom: Plantae
Phylum: Tracheophyta
Class: Magnoliopsida
Order: Malpighiales
Family: Rhizophoraceae
Genus: Rhizophora
Species: R. apiculata




Distribution


R. apiculata is found in south Asia including Bangladesh, Brunei Darussalam, Cambodia, India, Indonesia, Malaysia, Myanmar, Philippines, Singapore, Sri Lanka, Thailand, southern Viet Nam, and China (Hainan Island). It is also found in the Northern Maldives. In Australasia, its range includes Northwest Australia, Northeast Australia, Federated States of Micronesia, Guam, New Caledonia, Palau, Papua New Guinea, Solomon Islands, and Vanuatu.

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Global distribution of R. apiculata. Adapted from the IUCN list of threatened species.


Description


Overall


  • Trees 20-30m tall
  • Bark dark grey and chequered
  • Conspicuous arching stilt roots that can extend 5m up the stem
  • Often with lots of aerial roots emerging from the branches

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R. apiculata along the coast of Thailand. (Photo: Britannica Online for Kids)

Leaves

  • Leaves 8-15cm long
  • Eye-shaped
  • Glossy green
  • Stiff
  • Tiny evenly distributed black spots on the underside
  • Stipule (i.e., outgrowths on the base of leafstalk) usually (but not always) red

Leaves - � Pierre GRARD - IFP
Leaves - � Pierre GRARD - IFP

Leaves of R. apiculata. (Photo: Checklist of Mangrove species of South East India and Sri Lanka)

Flowers

  • Flowers 1-2cm in diameter
  • In pairs
  • Grow on short and swollen bracts
  • Calyx globular, hard, thick, brown on the outside yellow inside
  • Petals yellow to white, flat membranous and hairless, falling off soon after blossoming
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Flowers of R. apiculata grow on very short bracts so that they appear to be stuck directly onto the branch. (Photo: Checklist of Mangrove species of South East India and Sri Lanka)

Fruits

  • About 2cm in length
  • The fruit looks like a brown, upside down pear
  • Crowned by short persistent sepals
  • The cylindrical hypocotyl can be up to 40cm long, smooth, green ripening purple
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Pear-like fruits of R. apiculata with long hypocotyls. (Photo: Wild Singapore)

Hypocotyl - � Pierre GRARD - IFP
Hypocotyl - � Pierre GRARD - IFP

Propagules of R. apiculata turn purple when ripening. (Photo: Checklist of Mangrove species of South East India and Sri Lanka)


Diagnosis


Rhizophora in Indo-West Pacific region consists of 3 species, R. apiculata, R. mucronata and R. stylosa. They can be distinguished in the field by some easily observed characters. R. mucronata and R. stylosa have slender (i.e., length much greater than the width) bracts at the base of mature buds and fruits as distinguished from R. apiculata that have bracts almost as wide, or wider than the length (Duke, 2006b). In addition, the bark of R. apiculata is grey, almost smooth, with vertical fissures, whereas the bark of R. mucronata is nearly black or reddish, rough or sometimes scaly (Hanum & Van der Maesen, 1997).

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Left: R. apiculata. Middle: R. mucronata. Right: R. stylosa. R. mucronata and R. stylosa have slender bracts at the base of fruits, whereas R. apiculata have short bracts. (Photo: John Yong)

Bark - � Pierre GRARD - IFP
Bark - � Pierre GRARD - IFP
Bark - � Pierre GRARD - IFP
Bark - � Pierre GRARD - IFP

Left: Grey bark of R. apiculata. Right: Black bark of R. mucronata. (Photo: Checklist of Mangrove species of South East India and Sri Lanka 1, 2)



Biology


Habitat

R. apiculata is found in the intermediate estuarine zone in the mid-intertidal region. This species tolerates a maximum salinity of 65 ppt and a salinity of optimal growth of 8-15 ppt (Robertson & Alongi, 1992). It grows gregariously on deep, soft and muddy soils that are flooded by normal high tides, often consolidated and sheltered from surf and currents by pioneer species of Avicennia L. and Sonneratia L.f. It avoids hard soils and develops well in per-humid regions where it can form almost pure stands, sometimes in association with Bruguiera spp. or R. mucronata. It does not occur in freshwater swamps. It is killed by frost and extended periods of near-freezing temperatures (Hanum & Van der Maesen, 1997).

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Rhizophora habits the mid-zone sheltered by pioneer species(Waycott et al., 2011).

Reproduction


The tiny flowers are wind-pollinated, producing lots of powdery pollen and no fragrance or nectar. They are also self-pollinating. Insects have occasionally been observed foraging for pollen. One-seeded fruits start to germinate when still hanging on the tree. The root protrudes from the fruit, producing a green, spindle-shaped rod (hypocotyls) of up to 40cm long. Eventually, the seedling falls from the fruit, floats with the high tide and establishes if it reaches a suitable site (Hanum & Van der Maesen, 1997). Seedlings may retain their viability for several months. Rhizophora seedlings grow rapidly to avoid being submerged at high tide. They can grow by 60cm in the first year (Tan, 2008).

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R. apiculata propagules. (Photos: John Yong)



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Development of seedling (Photo: A Guide to Mangroves of Singapore)


Adaptations

  • Prop and Stilt Roots

In Rhizophora, branched, looping roots arise from the trunk and lower branches. At this stage, they are known as prop roots.They become stilt roots only when they take the function of flying buttresses when the tree is older and the bottom of the trunk becomes upside down conical and may even lose contact with the ground. The stilt roots improve the stability of the tree by providing a broader base and support in the soft and unstable mud. They also help in aeration as they are exposed for at least most of the day between tides.

Stilt and prop roots - � Pierre GRARD - IFP
Stilt and prop roots - � Pierre GRARD - IFP

Prop and stilt roots of R. apiculata. (Photo: Checklist of Mangrove species of South East India and Sri Lanka)


  • Ultrafiltration of salt
Unlike mangrove species that secrete salt from the leaves, Rhizophora uses ultrafiltration at the root level to exclude salt. They can selectively absorb ions from the solutions they come into contact with by ultrafiltration. However, even with this, exclusion is not complete. Some salt is lost by transpiration through the leaf surface or accumulates in some cells of the leaf. It has been suggested that R. apiculata might deposit excess salts in the old leaves which are shed.

  • Vivapary
Characteristic of Rhizophora species, vivipary is the condition whereby the embryo grows first to break through the seed coat then out of the fruit wall while still attached to the parent plant. One suggestion has been that the mangrove presents relatively unstable conditions so having propagules which can grow practically immediately is an advantage. For instance, it is easy to observe that the seedlings of Rhizophora can often plant themselves directly below the parent tree because the centre of gravity is close to the root tip.


Economical Values



The wood is heavy and hard and requires careful seasoning to prevent splitting. It is used for foundations in piling, beams and the outriggers of dugout canoes, as well as furniture and interiors of houses. Branched stilt roots are used for making anchors. It is also a valuable fuelwood species and is often commercially planted for charcoal production. It is sometimes planted to protect bunds and dykes. It is also the preferred species for mangrove silviculture used in mangrove rehabilitation and plantation forestry (Tan, 2008).


Charcoal making industry in Malaysia. Adapted from Youtube.

Ecological Values


  • Refuge
Tree climbing crabs and sea snails climb up their aerial roots at high tide to avoid aquatic predators. The roots provide a surface for all kinds of creatures from algae to shellfish. And the tangle of roots provide hiding places for young fishes and shrimps from larger predators. Their branches provide shelter for creatures from Proboscis Monkeys and nesting sites for large herons, to crevices for insects and other tiny creatures.


  • Food
While on the tree, leaves are eaten by all kinds of creatures. Monkey snack on the shoots and leaves, small insects nibble on them. Fallen leaves are an important source of nutrients both within the mangrove habitat and when it is flushed out to the coral reefs. The leaves are rapidly broken up by crabs and other small creatures, and further broken down by micro-organisms into useful minerals.

  • Natural water filter
Underwater, a huge number of filter-feeders are fastened on the tangle of roots: barnacles, sponges, shellfish. These filter feeders clean the water of nutrients and silt. As a result, clear water washes out into the sea, allowing the coral reef ecosystem to flourish.

  • Coast stabilization
Their roots prevents mud and sand from being washed away with the tide and river currents. Mangrove trees also slowly regenerate the soil by penetrating and aerating it (other creatures such as crabs and mud lobsters also help in . As the mud builds up and soil conditions improve, other plants can take root. Mangrove trees also reduce the damage from violent storms.




Conservation Status


R. apiculata is widespread and common within its range. It is threatened by the loss of mangrove habitat throughout its range, primarily due to extraction and coastal development, and there has been an estimated 20% decline in mangrove area within this species range since 1980. Mangrove species are more at risk from coastal development and extraction at the extremes of their distribution, and are likely to be contracting in these areas more than in other areas. It is also likely that changes in climate due to global warming will further affect these parts of the range. Although there are overall range declines in many areas, they are not enough to reach any of the threatened category thresholds. This species is listed as Least Concern (Duke et al., 2010).



Phylogeny


The combined Bayesian phylogeny based on chloroplast and ITS data provided strong support to taxon relationships (Lo et al., 2014). Rhizophora taxa were divided into three strongly supported clades namely NW, RA, and RMS, corresponding to three groups of taxa. All individuals of R. apiculata belong to Clade RA. This clade is further divided into two subclades – one contains individuals from Australia, islands of the NW Pacific (Guam and Micronesia), and subtropical Asia (Japan); and the other contains individuals from Southeast Asia (Malaysia, North Sulawesi, Philippines, and Thailand) and Sri Lanka.


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Genetic relatedness among population samples of Rhizophora. (A) Bayesian tree based on combined chloroplast and nuclear ribosomal ITS data using the GTR + I + G model. Bootstrap (BS; above branch) and posterior probability (PP; below branch) values >50% are indicated. Individuals of Bruguiera gymnorrhiza were used for rooting purposes. (B) Neighbour-joining tree based on Jaccard distances, showing relatedness among population samples of Rhizophora species. Bootstrap values >50% are indicated. (Figure from Lo et al., 2014)


In the Indo-West Pacific, the divergence of R. apiculata from R. mucronata and R. stylosa likely occurred during the Eocene (~38.9 ± 12Ma), although these species co-occur in many areas of the Indo-West Pacific and have a similar wide distribution range. Within Clade RA, the split between {Southeast Asia, Sri Lanka} and the {Australia, Kenya, Northwest Pacific Islands, subtropical Asia} lineages was dated to the Oligocene-Miocene boundary (~29-24 Ma).




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Chronogram of Rhizophora based on BEAST analyses of the combined chloroplast and ITS data. White bars indicate confidence interval of the estimated time of divergence of the respective nodes. Pie charts indicate the probable ancestral areas based on Lagrange (black and white) and Mesquite (color) analyses for the clade of interest. (Figure from Lo et al., 2014)



Type Information


R. apiculata was first described in Java. Lectotypes can be found in Nationaal Herbarium Nederland, Leiden University branch (L), L0009917 and L0009918.



Literature and References

Blume, C. L. (1827). Enumeratio plantarum Javae et insularum adjacentium: minus cognitarum vel novarum ex herbariis Reinwardtii, Kohlii, Hasseltii et Blumii. apud JW van Leeuwen.
Duke, N.C. (2006a). Australia's Mangroves. The authoritative guide to Australia's mangrove plants. University of Queensland, Brisbane.
Duke, N. C. (2006b). Rhizophora apiculata, R. mucronata, R. stylosa, R.× annamalai, R.× lamarckii (Indo-West Pacific stilt mangrove), ver. 2.1. Species profiles for pacific island agroforestry. Permanent Agriculture Resources (PAR), Holualoa, Hawaii.
Duke, N., Kathiresan, K., Salmo III, S.G., Fernando, E.S., Peras, J.R., Sukardjo, S. & Miyagi, T. 2010. Rhizophora apiculata. The IUCN Red List of Threatened Species. Version 2014.3. <www.iucnredlist.org>. Downloaded on 24 November 2014.
Hanum, I. F., & Van der Maesen, L. J. G. (1997). PROSEA: Plant Resources of South-East Asia 11, Auxiliary Plants. Yayasan Obor Indonesia.
Lo, E. Y., Duke, N. C., & Sun, M. (2014). Phylogeographic pattern of Rhizophora (Rhizophoraceae) reveals the importance of both vicariance and long-distance oceanic dispersal to modern mangrove distribution. BMC evolutionary biology, 14(1), 83.
Lovelock, C. (1993). Field Guide to the Mangroves of Queensland. Australian Institute of Marine Science.
Robertson, A. I., & Alongi, D. M. (1992). Tropical mangrove ecosystems (Vol. 41, pp. 1-330). American Geophysical Union.
Waycott, M., McKenzie, L.J., Mellors, J.E., Ellison, J., Sheaves, M.T., Coller, C., Schwarz, A-M., Webb, A., Johnson, J.E. and Payri, C.E. (2011). Vulnerability of mangroves, seagrasses and intertidal flats in the tropical Pacific to climate change.
Wightman, G. (2006). Mangroves of the Northern Territory, Australia: identification and traditional use. Northern Territory. Dept. of Natural Resources, Environment and the Arts, Palmerston.

Useful links:
R. apiculata in Wild Singapore
R. apiculata on the NParks Flora and Fauna website.
R. apiculata in Guide to the mangroves of Singapore.