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Mangrove vegetation: An evolutionary

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C S I R O P U B L I S H I N G

Marine
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Volume 49, 1998
CSIRO 1998

A journal for the publication of original contributions

in physical oceanography, marine chemistry,
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 CSIRO 1998 Mar. Freshwater Res., 1998, 49, 277286

Mangrove vegetation: an evolutionary perspective

P. Saenger

Centre for Coastal Management. Southern Cross University, Lismore, NSW 2480, Australia.

Abstract. The world-wide occurrence of mangrove vegetation and the modern floristic divergence
between the IndoPacific and the Atlantic mangroves, can only be explained by historical processes, in
that the composition of the modern mangrove flora at any one location, while subject to present-day
climatic and geographical conditions, is largely relict. Although several interpretations have been offered
to relate mangrove distributions to past events, none has been universally accepted. What is explored
here, is that there are several historical and modern processes which in combination, have resulted in the
present day distribution of mangroves. Evolutionary processes are reviewed from the fossil record and
from the data on continental drift. Next, the ecological processes that are selectively acting on the
various species and their distributions are examined with particular emphasis on aridity, temperature and
latitudinal attentuation of species. Finally, some modern anthropogenic processes (e.g. species
introductions, over-exploitation and habitat modification, afforestation) are examined in terms of their
effects on mangrove distribution. As an outcome of these various processes, the modern mangrove
vegetation is analysed particularly in relation to regions of endemism, vicariance among species,
discontinuous distributions, hybridization and divergence. Finally, some speculation is offered in terms
of future trends and evolutionary possibilities.

Introduction likely, that the southerly extensions of Africa and South

The world-wide occurrence of mangrove vegetation and
the floristic divergence between the old and the new
world mangroves can only be explained by historical events,
because the composition of the modern mangrove flora at
any one locality, although subject to present-day ecological
processes, is essentially relict (Tomlinson 1986; Duke
1995). Although some authors (Smith 1973; Thorne 1973)
have suggested that angiosperms arrived on the scene too
late for their modern distribution to have been seriously
affected by continental drift, mangroves, being water-
dispersed, could be dispersed only where suitable passages
of water existed between continents. Hence, the present
distribution of mangroves and their constituent species must
be seen within the context of plate tectonics and continental
drift. Although several interpretations have been offered to
relate mangrove distributions to past events (van Steenis
1962; McCoy and Heck 1976; Specht 1981; Mepham 1983;
Rico-Gray 1993; Duke 1995; Plaziat 1995), none has been
universally accepted.
Each of these various interpretations is based on the
existence during the Cretaceous of an extensive tropical sea,
the Tethys Sea, separating the northern supercontinent of
Laurasia from the southern Gondwanaland. Mangroves
evolved in the late Cretaceous within the Tethys Sea and
dispersed outwards via the available coastal waterways.
Ultimately, around 18 million years ago (mya), the western
Tethys Sea became isolated with the enclosure of the
Mediterranean by the collision of Africa and Asia Minor. At
that time, the pantropical mangrove flora became disjunct
and developed as two isolated floras (assuming, as seems
America formed impassable barriers to mangrove dispersal).
Finally, around 3 mya, the Panama gap closed by the
collision of North and South America. Thus, today, there are
three disjunct mangrove floras of which that of the eastern
Pacific is too recent in origin to differ morphologically from
its Atlantic progenitor.
The primary disputes about the phytogeography of
mangroves concern the exact centre(s) of origin of
mangroves and their subsequent dispersal routes around the
various continents. However, to understand the modern
distributions of mangrove vegetation and the component
species, several historical and modern processes must also
be considered, and these are reviewed here.
Evolutionary processes of the mangrove flora and
habitat
The known fossil record of mangroves (Table 1) suggests
that mangroves evolved soon after the appearance of
flowering plants, with the earliest records of Nypa in the late
Cretaceous to early Palaeocene (Dolianiti 1955), closely
followed by Sonneratia (Gruas-Cavagnetto et al. 1988).
Other genera evolved at various times and in apparently
differing regions. Given this evolutionary history, four broad
views have been suggested for the centre of origin and the
dispersal of the mangrove flora:
(1) Eastern Tethys Sea origin with eastward dispersal
across the Pacific and via the Panama gap into the Atlantic
eastwards (e.g. van Steenis 1962; Muller and Caratini 1977).
(2) Eastern Tethys Sea origin with dispersal north-
westwards into the Atlantic and then via the Panama gap into

10.1071/MF97139 1323-1650/98/040277
278 P. Saenger

the eastern Pacific (e.g. Specht 1981; Rico-Gray 1993).
(3) Western Tethys Sea origin with dispersal south via
southern Africa to the eastern Tethys Sea (e.g. Duke 1995).
(4) A two-way dispersal from a central Tethys Sea origin
(Por 1984; Plaziat and Cavagnetto 1996) or an eastern
Tethys Sea origin (Bousquet-Melou 1996).
None of these interpretations can be entirely ruled out,
because mangrove fossil records (Table 1) are somewhat
ambiguous and certain genera (e.g. Avicennia) are not well
represented (Plaziat 1995). However, the fossil record
generally supports an eastern Tethys Sea origin for
Rhizophora and perhaps Avicennia (Cookson and Eisenack
1967; Churchill 1973; Stover and Evans 1973; Martin
1982), with a westward dispersal via the Mediterranean
route, which until about 18 mya contained extensive
Avicennia communities with IndoPacific affinity (Bessedik
1981, 1985). For Avicennia, a cladistic analysis of the
species of this genus (Bousquet-Melou 1996) indicated that
the AsianAustralasian species A. marina and A. alba are the
ancestral species whereas the three American species (A.
germinans, A. schaueriana and A. bicolor) are of later
origin. Fossil remains of several other mangrove genera
(including Aegialitis, Camptostemon and Scyphiphora) have
been found only in the Australasian region and are clearly of
somewhat later, eastern Tethys Sea origin. However, it
seems equally clear that the genera Nypa and perhaps
Laguncularia and Conocarpus of the Combretaceae have a
western Tethys Sea origin (Berry 1924, 1930).
Finally, it appears on the basis of presently known fossil
location and ages that genera such as Sonneratia, Heritiera,
Pelliciera and Aegiceras made their earliest appearances in
the central Tethys Sea in the late Palaeocene to mid Eocene
(Gruas-Cavagnetto et al. 1988; Cavagnetto and Anadn
1995).
Given these various centres of origin, the following
dispersal patterns seem plausible. During the late Cretaceous
to Palaeocene (6355 mya), when the western Tethys Sea
(proto-Atlantic) was still a relatively narrow waterway and
western Africa was experiencing a wet phase, there was no
mangrove vegetation per se in the Niger delta but extensive
estuarine swamp communities dominated by Nypa
(Sowunmi 1981, 1986). Nypa, which is first known from the

Table 1. Significant geological events and mangrove fossil records

mya, million years ago

Era Period Approx. Fossil record

mya

Cainozoic Pliocene 3 Panama route closed

Miocene 10 Avicennia and Sonneratia pollen in Borneo; Aegialitis and Sonneratia pollen in India;
Avicennia pollen in Nigeria
16 Acanthus, Aegialitis and Camptostemon pollen in Australia; Bruguiera, Sonneratia, Avicennia,
Rhizophora, Ceriops, Scyphiphora, Nypa and Excoecaria pollen in Japan; Tethys Sea route closed;
Avicennia still present in Mediterranean
23 Aegialitis, Avicennia and Camptostemon pollen in Borneo; Scyphiphora, Lumnitzera and
Avicennia pollen in the Marshall Islands
24 Rhizophora in Nigeria, Senegal and South America
Oligocene 36 Pelliciera pollen in Cameroon and Puerto Rico
38 Sonneratia in south-east Asia; Rhizophora in South America
Eocene 40 Rhizophora, Avicennia and Sonneratia in south-west Australia; Rhizophora and Pelliciera pollen
in Panama; Rhizophora, Conocarpus and Laguncularia in North America
42 Fossils of Nypa, Ceriops, Palaeobruguiera, Rhizophora and Acrostichum-like ferns in
London Clay Flora; Bruguiera, Ceriops, Avicennia, Pelliciera and Nypa pollen in Paris basin;
Heritiera and Aegiceras pollen near Pyrenees; Nypa in Egypt and Sonneratia wood in Libya
50 Pelliciera pollen in Jamaica; Rhizophora in Borneo and India; Nypa and Rhizophoraceae near Pyrenees
54 Nypa pollen and/or fruit in Europe, North America, Asia and Australia; Acrostichum spores
and fronds in Japan; Pelliciera pollen near Pyrenees
Palaeocene 57 Sonneratiaceae pollen near Pyrenees
60 Rhizophora pollen in Australia
63 Nypa pollen in Nigeria
69 Nypa fruit in Brazil
Mesozoic Cretaceous 110 First flowering plants

Based on: Anderson and Muller 1975; Arnold 1952; Berry 1924, 1930; Bessedik 1981; Biosca and Via 1988; Bonnet 1904; Cavagnetto and Anadn 1995;
Chandler 1951; Chikhi 1992; Churchill 1973; Cookson and Eisenack 1967; Dolianiti 1955; Gee 1990; Germeraad et al. 1968; Graham 1975; Graham and
Jarzen 1969; Gruas-Cavagnetto 1987; Gruas-Cavagnetto et al. 1988; Hekel 1972; Lakhanpal 1970; Leopold 1969; Louvet 1970; Martin 1982; Muller 1959,
1964, 1981; Muller and Caratini 1977; Ollivier-Pierre et al. 1987; Salard-Cheboldaeff 1976; Sowunmi 1981, 1986; Stover and Evans 1973; Tanai 1972;
Thanikaimoni 1987; Tissot 1980; Tsuchi 1992; Tsuda et al. 1984, 1986; Van der Hamm 1963, 1972, 1974; Wilkinson 1981, 1983.
Mangrove vegetation: an evolutionary perspective
late Cretaceous of Brazil (Dolianiti 1955), apparently
evolved in, and spread throughout, the proto-Atlantic at this
time (Moore 1973). This Nypa-dominated swamp
community remained in West Africa during the entire
Eocene (Sowunmi 1981, 1986) and may have extended as
far north as Europe (Wilkinson 1981) where, however, only
fruits and pollen grains have been found.
At much the same time (i.e. Palaeocene), Sonneratia
appeared in the central Tethys Sea (Gruas-Cavagnetto et al.
1988), followed in the mid Eocene by Heritiera, Aegiceras
and Pelliciera (Cavagnetto and Anadn 1995). Three of
these genera apparently dispersed towards the eastern Tethys
Sea while Pelliciera dispersed first westwards to Jamaica
(Graham 1975) then southwards to Cameroon (Salard-
Cheboldaeff 1976).
Genera of the Rhizophoraceae together with Avicennia
rapidly dispersed westwards from the eastern Tethys Sea
during the early Eocene. Thus, by the mid Eocene, Europe
appears to have been the first tropical meeting point of
mangrove genera from the eastern, central and western
Tethys Sea. It is interesting to note that, in the fossil beds of
France and England from this tropical era, pollen or spores
of Sonneratia, Avicennia, Rhizophora, Palaeobruguiera,
Ceriops, Nypa, Aegiceras, Heritiera, Acrostichum and
Pelliciera have been recorded (Chandler 1951; Wilkinson
1981; Gruas-Cavagnetto 1987; Ollivier-Pierre et al. 1987;
Gruas-Cavagnetto et al. 1988; Plaziat and Cavagnetto 1996).
By the late Eocene, the genera Conocarpus and
Laguncularia appeared in the western Tethys Sea (Berry
1924, 1930) and became widely dispersed around the
American and West African shorelines. As seasonally dry
conditions were widespread in West Africa at the end of the
Eocene, Nypa declined in abundance and finally disappeared
altogether in the early Miocene (24 mya) incidentally at
the same time Nypa disappeared from the fossil record of
Venezuela. These disappearances coincided with the sudden
and predominating appearance of Rhizophora throughout
the region (Sowunmi 1981, 1986) which, given the earlier
records of this genus from the eastern Tethys Sea, must have
reached West Africa via the Mediterranean. This is further
supported by the earlier appearance of Rhizophora in
southern France (50 mya; Gruas-Cavagnetto et al. 1988) and
in the London Clay (45 mya; Chandler 1951) than in North
(40 mya; Berry 1924, 1930) and South America (38 mya;
Germeraad et al. 1968; Van der Hamm 1972).
Plaziat and Cavagnetto (1996) have suggested that the
climatic cooling of the late Eocene not only changed the
species composition and distribution of the mangroves but
also started the process of the differentiation of the old and
new world mangroves during the Oligocene, rather than in
the mid Miocene when the Tethys Sea route closed.
Thus, while some mangroves appear to have evolved in
the central Tethys Sea (Mediterranean), several other
279
mangroves (Nypa and an ancestral Combretaceae)
apparently evolved in the western Tethys Sea (the proto-
Atlantic) and dispersed out of the region (Exell and Stace
1972; Moore 1973; Saenger and Bellan 1995). In addition,
some members (Rhizophora and Avicennia) of the eastern
Tethys Sea (IndoPacific) mangrove flora were able to enter
and survive in the proto-Atlantic before the Tethys Sea
became unavailable as a migration route. Acrostichum may
have had a north-eastern Tethys Sea origin where the earliest
remains of Acrostichum have been found in Japan (Tanai
1972). However, Acrostichum, which has been world-wide
in its distribution since the mid Eocene and extra-tropical in
many parts of its distribution, is a great disperser and
opportunist.
If, as indicated by the cladistic analysis of Avicennia
(Bousquet-Melou 1996), the West AfricanAmerican
species are derived from Australasian ancestral stock, then
the process of differentiation between the IndoPacific and
AfricanAmerican species has occurred relatively recently,
i.e. during the climatic cooling of the late Eocene, or after
the closure of the Mediterranean around 18 mya. Similarly,
the differentiation between the AfricanAmerican genus
Laguncularia and the closely related IndoPacific genus
Lumnitzera would also date from this period.
Whatever the exact origin(s) and dispersal routes of
mangroves, the present distributions of mangroves also
show features reflecting some of the more modern processes
described below.
Selective processes ecological sorting
Superimposed onto the historical events described above
are the present constraints of climatic, geographical and
socioeconomic conditions. These constraints are
manifested by a reduction of species with increasing latitude
or aridity on the one hand, and selective removal or loss of
species by human activity on the other. Natural changes
have included the sudden formation and subsequent decline
of a giant mangrove swamp in northern Australia due to
continued estuarine infilling about 6000 years ago
(Woodroffe et al. 1985). Similarly, over the past 12 000
years there has been a large reduction of Rhizophora in the
swamps of the Panama isthmus as a result of changing sea-
levels, with Rhizophora disappearing from Gatun Lake 4200
years ago after dominating the area for the previous 30 000
years (Bartlett and Barghoorn 1973). In Guiana, a similarly
large reduction in Rhizophora occurred approximately 3500
years ago with stabilizing sea-levels (Tissot et al. 1988).
Floristic attenuation with latitude
The latitudinal limits of mangrove vegetation on each of
the major land masses (Table 2) show these limits to be quite
variable and broadly related to temperature and aridity. In
addition, these latitudinal limits are preceded by a gradual
280 P. Saenger

Table 2. Latitudinal limits of mangrove vegetation on major land limited more by aridity rather than by temperature
masses (Cluesener and Breckle 1987). Similar considerations would
, not applicable
also be relevant to parts of West Asia and the Middle East.
Continental land mass Northern limit Southern limit Another interesting example of aridity-induced species
attenuation (but with decreasing latitude) is provided by the
Atlantic America 32208 28568 East AfricanArabian Peninsula region. The extreme aridity
Pacific America 30158 5328 of the Horn of Africa (northern Somalia) causes an abrupt
Atlantic Africa 19508 12208
Eastern Africa/Red Sea 28248 32598
loss of species (Fig. 1), and only Avicennia, Rhizophora,
Western Australia 33168 Bruguiera and Ceriops are able to extend north to the
Eastern Australia 38458 southern Red Sea.
Pacific Asia 31218
Modern processes human-induced changes
In addition to massive natural changes in mangrove
vegetation, human activities have significantly modified the
reduction of mangrove development (e.g. height and extent mangrove vegetation in various parts of the world. In
of mangrove vegetation Saenger and Snedaker 1993) and particular, these include species introductions and habitat
an attenuation of species with increasing latitudes. By way modification, as well as the more recent phenomena of
of example, the southward attenuation of species on the non- mangrove afforestation.
arid east coasts of Africa and Australia are shown in Table 3.
This comparison indicates some intra-specific variability but Plant introductions
supports the suggestion that, in the presence of an adequate As with other plant groups, mangroves have been
rainfall, temperature is the major factor in reducing species deliberately introduced into areas beyond their natural
abundance with latitude (Saenger and Moverley 1985). distributional ranges to meet human needs or aspirations.
Some of these introductions are well documented, but others
Floristic attenuation with aridity are not and are likely to affect apparent distributional ranges.
As shown in Table 2, the latitudinal limits of mangroves Thus, the present West African populations of Nypa
on the West African and South American Pacific coasts are fruticans were introduced to Calabar in 1906 and Oron in
unexpectedly curtailed. These limits coincide with the limits 1912 (Wilcox 1985) from the Singapore Botanic Gardens,
of arid regions (Anon. 1979) defined as summer rainfall and even though this species had occurred throughout the Niger
winter drought, <30mm rainfall in each month of the year, delta until 25 mya (Sowunmi 1986). To date, this species has
and a precipitation to potential evapotranspiration ratio spread into the Niger, Imo, Bonny and Cross Rivers and its
(P/PEt) of <0.03. This suggests that the mangrove rate of spread is perceived to be accelerating over recent
distribution on western coasts of continents is generally years. It has now reached the Wouri Estuary in Cameroon

Table 3. Southern latitudinal limits of mangrove species on the

eastern coasts of Australia and Africa
African limits based largely on Day (1981) and Hughes and Hughes (1992);
Australian limits based on Wells (1982); Saenger and Moverley (1985); and
A. Specht, personal communication

Species E. African E. Australian

Sonneratia alba 23558 22308

Pemphis acidula 24188 15428
Thespesia populnea 2601 27308
Xylocarpus granatum 26018 25308
Xylocarpus moluccensis 26338 23508
Heritiera littoralis 26338 22158
Ceriops tagal 26508 28118
Lumnitzera racemosa 26508 27308
Acrostichum aureum 28588 26058
Barringtonia racemosa 30448 17218
Rhizophora mucronata 31428 18258
Bruguiera gymnorhiza 32148 29258
Hibiscus tiliaceus 32168 31278 Fig. 1. Northern and southern limits of mangrove species and mangrove
Avicennia marina 32598 38458 associates on the east coast of Africa.
Mangrove vegetation: an evolutionary perspective
where its dispersal is facilitated by local villagers who value
its thatching properties (Din 1991). Most recently, stands of
this species have been recorded from the mouth of the Volta
River in Ghana (A. K. Armah, personal communication),
presumably as a result of human dispersal. Introduced stands
of Nypa fruticans have also recently been recorded from the
Atlantic coast of Panama, where a similar spread is
predicted (Duke 1991a).
Even though Pelliciera fossils indicate its presence in the
Caribbean, Europe and West Africa during the Eocene to
Oligocene, the present populations of Pelliciera rhizophorae
on the Atlantic coasts of Panama and Colombia have a
questionable origin. This species was introduced from the
Pacific to the Atlantic coast of Colombia, around the Canal
del Dique y Covenas, in the last twenty years (Paez 1994),
although apparently ancient stands occur on the Atlantic
coast of Panama (Duke, personal communication).
An extreme example of the extension of the distribution
of species is the introduction and establishment of
Rhizophora mangle, Rhizophora mucronata, Bruguiera
parviflora and Bruguiera sexangula on Oahu, Hawaii,
around the turn of the present century. Similarly, the
occurrence of Rhizophora mangle in Fiji is almost certainly
due to introductions, most probably by the American
Missionary Society which has been active on the island
since the 1840s.
Mangrove over-exploitation and habitat modification
Human activity such as pollution, water diversion and
selective clearing can significantly change mangrove
distributional ranges. Thus, the northernmost stands of R.
racemosa in West Africa, reported by Adam (1965) from the
Ile de Thiong (1603N), Mauritania, have been cleared by
the local inhabitants in the past two decades (Gowthorpe and
Lamarche 1993). Similarly, significant stands of Bruguiera
gymnorhiza have been selectively felled for boat building in
the Sudan and Yemen (Zahran 1977; Ormond et al. 1988),
and Rhizophora mucronata has disappeared from the
Arabian Gulf for similar reasons in historical time.
In parts of eastern Africa, tanbark extraction from
mangroves commenced reasonably early, with Germany
being the major importer. Tanbark export commenced in
Kenya in 1900, with Tanzania, Mozambique and
Madagascar soon following (Grewe 1941). The tanbark
export from Kenya reached record values around the start of
the first World War but this activity had collapsed by the end
of the war (Fig. 2). Even with some regrowth during the first
World War, the tanbark resources of Madagascar were
exhausted by 1927, whereas those of Mozambique managed
to survive until 1935, largely supplying the American leather
industry. Unsustainably high tanbark extraction was initiated
in Tanzania from 1921 onwards until that resource also was
exhausted by 1937. Given that tanbark was derived only
281
Fig. 2. Combined mangrove bark export from East Africa and Madagascar
from 1900 to 1937 (adapted from Grewe 1941).
from Rhizophora, Ceriops and Bruguiera, the volume of
bark exported represents a huge and selective loss of these
species.
The large-scale replacement of mangroves by aquaculture
ponds is a widespread modern phenomenon that has been
responsible for major losses of mangroves in, for example,
the Philippines, Indonesia and Ecuador. Elsewhere, the
construction of dams and barrages has shifted prevailing
salinity regimes to the exclusion of one species rather than
another. For example, Heritiera fomes appears to be
increasingly confined in its distribution to the wetter eastern
Sundarbans in Bangladesh as a result of tectonic changes in
combination with dam construction and freshwater
extraction (Blasco et al. 1996).
Mangrove afforestation
There are several major mangrove afforestation
programmes around the world as well as numerous less
extensive ones (for a review, see Field 1996). An example of
the way in which mangrove afforestation programmes can
change mangrove distributions or abundance is found in the
Bangladesh mangrove afforestation programme, in which
~120 000 ha of mangrove plantations have been established
over the past 15 years (Saenger and Siddiqi 1993). However,
because of the ease of transplanting seedlings of Sonneratia
apetala, the greatest part of the plantations consists of
monocultures of this species, which had previously been a
relatively obscure species.
Mangrove vegetation today
The contemporary mangrove vegetation is the integrated
outcome of the various processes outlined above. Thus,
discontinuities in species distributions have become
apparent while areas of high endemism can be recognized.
Discontinuities and endemism
Because of their seawater dispersal, most mangrove
species have a more or less continuous distribution around
282
various coastlines, but there are exceptions. Some examples
of discontinuities from among the most ancient mangrove
genera include the following.
The new world species of Rhizophora show disjunct
distributions, with West African, Atlantic-American and
Pacific-American occurrences. In the case of Rhizophora
mangle, even the West African distribution appears to be
disjunct, with a Senegal-to-Liberia and a Nigeria-to-Angola
distribution (Saenger and Bellan 1995). Bruguiera hainesii
is discontinuous between western Malaysia and New
Guinea (Tomlinson 1986), and Ceriops tagal and Bruguiera
gymnorhiza show major discontinuities between eastern
Africa and south-west Asia.
Sonneratia alba also appears to have several disjunct
populations respectively centred on East Africa
Madagascar, IndiaSri Lanka and Australasia. Even the
northern Australian distribution appears to be separated by a
significant discontinuity in the Gulf of Carpentaria.
Similarly, Sonneratia ovata has a major disjunction between
its ThaiIndonesian and its Papua New Guinea occurrences.
Sonneratia lanceolata appears to have three discontinuous
distributions in south-east Asia and northern Australia.
Avicennia rumphiana appears to be the only species of
Avicennia with three disjunct distributional ranges.
Pelliciera rhizophorae is of very limited distribution and
endemic to the tropical Pacific coast of America. Its
presence on the Caribbean coasts, first noted in the early
1980s, is of uncertain origin, as discussed above.
Other locally restricted species include Heritiera fomes,
Aegialitis rotundifolia, Avicennia integra, Avicennia bicolor,
Avicennia schaueriana, Excoecaria ovalis, Excoecaria
indica, Sonneratia griffithii and Sonneratia apetala.
The explanations for many of these disjunctions are
undoubtedly to be found in the ecological requirements of
the individual species but, in a broad biogeographical sense,
temperature and rainfall are probably the main determinants.
Nevertheless, the high endemicity of the South Asian and
northern Australian areas may reflect their proximity to the
main centre of mangrove origin and subsequent dispersal
routes.
Conversely, there are no endemic mangroves on the coast
of Africa; this contrasts with all other major mangrove
regions, which have at least one endemic species. The
absence of any endemic species suggests that the African
mangrove flora is a relict flora; this, in turn, is supported by
the fossil record which indicates that during the late Eocene
to early Miocene a much richer mangrove flora was present.
To that must be added that the mangrove vegetation of
Africa is in retreat from relatively recent changes in climate
and sea-level (Rossi 1981; Saenger and Bellan 1995). The
absence of any endemic species also suggests that the
conditions along this coastline were not conducive to
speciation in the taxa present.
P. Saenger
Vicariants
Since mangroves are dispersed by seawater, there are few
examples of divergent species of one genus with non-
overlapping ranges. However, such vicariant species are
found in Aegialitis and Camptostemon (Tomlinson 1986),
two genera whose earliest fossils are known from Borneo 23
mya (Muller 1964). Aegialitis annulata is distributed from
northern Australia to Papua New Guinea, whereas Aegialitis
rotundifolia is restricted to shorelines of the Bay of Bengal
and the Andaman Sea. Similarly, Camptostemon schultzii
occurs in northern Australia, Papua New Guinea and,
possibly, as far north as Borneo, whereas Camptostemon
philippinense occurs in the Philippines, Borneo and
Sulawesi. Whether there is any overlap between these
species in Borneo is not known.
By way of contrast, the genus Aegiceras contains one
species (Aegiceras corniculatum) with a wide Australasian
distribution that totally includes the more restricted
Philippine distribution of Aegiceras floridum. Similarly, the
genus Heritiera contains two mangrove species with one of
limited distribution (H. fomes) being totally included within
the range of the other, wide-ranging, species (H. littoralis).
Both mangrove species in the genus Cynometra (C. iripa
and C. ramiflora) have largely overlapping distributions in
south-east Asia, although only C. iripa extends southwards
to Australia.
Hybridizations
The genetic isolation between species of some genera of
mangroves is not complete; interspecific hybrids are known
in the genera Sonneratia, Rhizophora, Xylocarpus and
Lumnitzera (Duke and Bunt 1979; Duke 1984; Tomlinson
1986). On the other hand, new methods such as biochemical
studies have cast doubt on the status of some putative
hybrids; for example, the hybrid status of R. harrisonii has
not been confirmed on the basis of foliar wax chemistry
(Dodd et al. 1995).
Future trends and evolutionary possibilities
Before examining the evolutionary possibilities, there are
some aspects of mangroves that need to be emphasized.
First, a better understanding of the phylogeny of
mangroves is gradually being attained through newly
developed molecular and related techniques. For example,
on the basis of morphological and anatomical features, the
Rhizophoraceae has been included in the order Myrtales
(Takhtajan 1980) or assigned to its own separate order
Rhizophorales (Thorne 1992). However, a parsimony
analysis of the DNA sequence data from the chloroplast
gene rbcL (Conti et al. 1996), strongly suggests that the
Rhizophoraceae does not belong to the Myrtales. Rather,
this analysis puts this family as part of a rosid clade that
includes the families Euphorbiaceae, Humiriaceae and
Malpighiaceae.
Mangrove vegetation: an evolutionary perspective
Second, new morphological and biochemical markers are
being found within species, intraspecific taxa and
populations which will facilitate an improved understanding
of the processes of species divergence. These include such
markers as iridoid glycosides (Fauvel et al. 1995), foliar leaf
waxes (Dodd et al. 1995; Rafii et al. 1996), DNA analyses
(Brajou 1996), isozyme analyses (McMillan 1986; Ballment
et al. 1988; Duke 1991b; Huang 1993) and cladistic analyses
(Juncosa and Tomlinson 1988; Ricklefs and Latham 1993;
Bousquet-Melou 1996).
Third, mangroves as a group appear to be relatively slow
in undergoing evolutionary change. Thus, for example,
Moore (1973) noted that the earliest fossils of Nypa are not
distinguishable from the modern Nypa fruticans, concluding
that Nypa has essentially sat still for 70 million years i.e.
morphologically but certainly not geographically!
Thus, the evolutionary history and relationships of
mangroves are becoming better understood while the
dynamics of the evolutionary processes themselves are
becoming clearer. On that basis, it seems likely that the
populations of the most widespread species, e.g. A. marina
and A. germinans, are diverging because they no longer
consist of single inbreeding populations. In the case of A.
marina, this divergence has proceeded further and has been
recognized by subspecific ranking (Duke 1991b; Everett
1994). In A. germinans, on the other hand, this divergence is
not so advanced and has allowed chemotypes but not
morphotypes to be recognized (Compre 1963; Bousquet-
Melou 1996).
In an evolutionary sense, biochemical differences
between populations, requiring one or two gene mutations or
frequency changes only, should be apparent first and that
seems to be the case. For example, chemotypes of A.
germinans were readily identifiable in West African
populations (Dodd et al. 1995), between Pacific and Atlantic
America (Rafii et al. 1996), and between African and
American populations (Bousquet-Melou 1996).
Physiological changes, requiring at least 510 gene
mutations or frequency changes, should become apparent
with further divergence. For example, slight physiological
differences were detected between West African mangroves
and American Atlantic mangroves of the same species
(Saenger and Bellan 1995). Similarly, ecophysiological
variation in chilling tolerance was studied by McMillan
(1975) who tested different populations of mangroves from
30N to 38S. Comparison of A. germinans and A. marina in
experimental chilling tests revealed that plants from tropical
climates showed severe damage to all leaves and stems after
12 successive chilling nights, whereas plants from temperate
climates showed no leaf damage. These preliminary studies
have been successful in indicating infraspecific variation
which appeared to have a genetic basis.
Morphological changes, which might require >10
mutations or gene frequency changes, are not apparent in
283
Rhizophora in America and Africa, but are apparent in all
genera shared by the old world and new (Duke 1995;
Bousquet-Melou 1996). On the other hand, morphologically
based subspecies in Avicennia marina can be recognized on
the basis of allozyme patterns in specimens from western,
northern and eastern Australia (Duke 1991b).
Taxonomic changes measured by isozymes or DNA
analysis generally require >100 mutations or gene frequency
changes (because of the relatively insensitive analytical
techniques), and would therefore be the later stages in
species divergence. Thus, although subspecies formation
can be recognized in Avicennia marina on the basis of
isozymes (Duke 1991b, 1995), DNA analysis failed to
demonstrate the differentiation into subspecies in Avicennia
germinans (Brajou 1996). On the other hand, McMillan
(1986), using isozyme analysis to determine genetic
differences among populations of A. germinans, found that
plants from the western side of the Gulf of Mexico differed
in their predominant patterns of phosphoglucose isomerase
and phosphoglucose mutase from plants on the Caribbean
side of the Gulf of Mexico. Similarly, Ballment et al. (1988)
differentiated three sibling species of Ceriops by
biochemical genetics which indicated a uniform genetic
structure within taxa but a high genetic divergence among
taxa; that study showed that the sympatric populations of
two taxa maintained fixed differences in genes at a number
of loci and were reproductively isolated, without the
presence of any hybrid forms.
All these diverging processes are happening against the
background of further fragmentation of populations and
decreases in species distribution due to anthropogenic
effects. For example, Huang (1993) studied the genetic
variability between and within populations of the mangrove
Kandelia candel on Taiwan using isozymes and concluded
that a moderate level of genetic variation existed between
the four mangrove populations studied but that there was
little differentiation within populations. Local selection and
restricted gene flow between the populations had
contributed to the limited genetic variability of this species
in Taiwan. Thus, it seems likely that this fragmentary
process will accelerate in the mangroves, which appear to be
an inherently slow group to respond in an evolutionary
sense.
In addition, however, research is underway to determine
the genetic variation within certain taxa with a view to
identifying specific genotypes that are high performers
under specific environmental conditions. At the same time,
micropropagation techniques are being developed to
propagate those specific genotypes. This combination of
genetic selection and micropropagation will add a further, as
yet unknown, dimension to the three primary processes
discussed.
In conclusion, a number of poorly understood historical
as well as current processes are implicated in the
284
biogeography of mangrove communities and species. In
addition, evolutionary processes going on at present are
tending to cause some of the more isolated species or
populations to diverge. However, and most importantly,
present-day mangrove distributions and their governing
processes are based on incomplete data for considerable
areas of the world a situation that must be urgently
addressed if the information is not to be lost along with the
mangrove resources.
Acknowledgments
This review was prepared while the author was on study
leave at the Laboratoire dEcologie Terrestre in Toulouse,
and it is a pleasure to thank its Director, Professor Franois
Blasco, for facilities and support. The financial support,
provided by a Senior Science Fellowship from the French
Ministry for Research and Higher Education, is gratefully
acknowledged.
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