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Marine
&
Freshwater
Research
Volume 49, 1998
© CSIRO 1998
w w w. p u b l i s h . c s i r o . a u / j o u r n a l s / m f r
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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 Indo–Pacific 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.
10.1071/MF97139 1323-1650/98/040277
278 P. Saenger
the eastern Pacific (e.g. Specht 1981; Rico-Gray 1993). origin. Fossil remains of several other mangrove genera
(3) Western Tethys Sea origin with dispersal south via (including Aegialitis, Camptostemon and Scyphiphora) have
southern Africa to the eastern Tethys Sea (e.g. Duke 1995). been found only in the Australasian region and are clearly of
(4) A two-way dispersal from a central Tethys Sea origin somewhat later, eastern Tethys Sea origin. However, it
(Por 1984; Plaziat and Cavagnetto 1996) or an eastern seems equally clear that the genera Nypa and perhaps
Tethys Sea origin (Bousquet-Melou 1996). Laguncularia and Conocarpus of the Combretaceae have a
None of these interpretations can be entirely ruled out, western Tethys Sea origin (Berry 1924, 1930).
because mangrove fossil records (Table 1) are somewhat Finally, it appears on the basis of presently known fossil
ambiguous and certain genera (e.g. Avicennia) are not well location and ages that genera such as Sonneratia, Heritiera,
represented (Plaziat 1995). However, the fossil record Pelliciera and Aegiceras made their earliest appearances in
generally supports an eastern Tethys Sea origin for the central Tethys Sea in the late Palaeocene to mid Eocene
Rhizophora and perhaps Avicennia (Cookson and Eisenack (Gruas-Cavagnetto et al. 1988; Cavagnetto and Anadón
1967; Churchill 1973; Stover and Evans 1973; Martin 1995).
1982), with a westward dispersal via the Mediterranean Given these various centres of origin, the following
route, which until about 18 mya contained extensive dispersal patterns seem plausible. During the late Cretaceous
Avicennia communities with Indo–Pacific affinity (Bessedik to Palaeocene (63–55 mya), when the western Tethys Sea
1981, 1985). For Avicennia, a cladistic analysis of the (proto-Atlantic) was still a relatively narrow waterway and
species of this genus (Bousquet-Melou 1996) indicated that western Africa was experiencing a ‘wet’ phase, there was no
the Asian–Australasian species A. marina and A. alba are the mangrove vegetation per se in the Niger delta but extensive
ancestral species whereas the three American species (A. estuarine swamp communities dominated by Nypa
germinans, A. schaueriana and A. bicolor) are of later (Sowunmi 1981, 1986). Nypa, which is first known from the
Based on: Anderson and Muller 1975; Arnold 1952; Berry 1924, 1930; Bessedik 1981; Biosca and Via 1988; Bonnet 1904; Cavagnetto and Anadón 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 279
late Cretaceous of Brazil (Dolianiti 1955), apparently mangroves (Nypa and an ancestral Combretaceae)
evolved in, and spread throughout, the proto-Atlantic at this apparently evolved in the western Tethys Sea (the proto-
time (Moore 1973). This Nypa-dominated swamp Atlantic) and dispersed out of the region (Exell and Stace
community remained in West Africa during the entire 1972; Moore 1973; Saenger and Bellan 1995). In addition,
Eocene (Sowunmi 1981, 1986) and may have extended as some members (Rhizophora and Avicennia) of the eastern
far north as Europe (Wilkinson 1981) where, however, only Tethys Sea (Indo–Pacific) mangrove flora were able to enter
fruits and pollen grains have been found. and survive in the proto-Atlantic before the Tethys Sea
At much the same time (i.e. Palaeocene), Sonneratia became unavailable as a migration route. Acrostichum may
appeared in the central Tethys Sea (Gruas-Cavagnetto et al. have had a north-eastern Tethys Sea origin where the earliest
1988), followed in the mid Eocene by Heritiera, Aegiceras remains of Acrostichum have been found in Japan (Tanai
and Pelliciera (Cavagnetto and Anadón 1995). Three of 1972). However, Acrostichum, which has been world-wide
these genera apparently dispersed towards the eastern Tethys in its distribution since the mid Eocene and extra-tropical in
Sea while Pelliciera dispersed first westwards to Jamaica many parts of its distribution, is a great disperser and
(Graham 1975) then southwards to Cameroon (Salard- opportunist.
Cheboldaeff 1976). If, as indicated by the cladistic analysis of Avicennia
Genera of the Rhizophoraceae together with Avicennia (Bousquet-Melou 1996), the West African–American
rapidly dispersed westwards from the eastern Tethys Sea species are derived from Australasian ancestral stock, then
during the early Eocene. Thus, by the mid Eocene, Europe the process of differentiation between the Indo–Pacific and
appears to have been the first tropical meeting point of African–American species has occurred relatively recently,
mangrove genera from the eastern, central and western i.e. during the ‘climatic cooling’ of the late Eocene, or after
Tethys Sea. It is interesting to note that, in the fossil beds of the closure of the Mediterranean around 18 mya. Similarly,
France and England from this tropical era, pollen or spores the differentiation between the African–American genus
of Sonneratia, Avicennia, Rhizophora, Palaeobruguiera, Laguncularia and the closely related Indo–Pacific genus
Ceriops, Nypa, Aegiceras, Heritiera, Acrostichum and Lumnitzera would also date from this period.
Pelliciera have been recorded (Chandler 1951; Wilkinson Whatever the exact origin(s) and dispersal routes of
1981; Gruas-Cavagnetto 1987; Ollivier-Pierre et al. 1987; mangroves, the present distributions of mangroves also
Gruas-Cavagnetto et al. 1988; Plaziat and Cavagnetto 1996). show features reflecting some of the more modern processes
By the late Eocene, the genera Conocarpus and described below.
Laguncularia appeared in the western Tethys Sea (Berry
1924, 1930) and became widely dispersed around the Selective processes — ecological sorting
American and West African shorelines. As seasonally dry Superimposed onto the historical events described above
conditions were widespread in West Africa at the end of the are the present constraints of climatic, geographical and
Eocene, Nypa declined in abundance and finally disappeared socio–economic conditions. These constraints are
altogether in the early Miocene (24 mya) — incidentally at manifested by a reduction of species with increasing latitude
the same time Nypa disappeared from the fossil record of or aridity on the one hand, and selective removal or loss of
Venezuela. These disappearances coincided with the sudden species by human activity on the other. Natural changes
and predominating appearance of Rhizophora throughout have included the sudden formation and subsequent decline
the region (Sowunmi 1981, 1986) which, given the earlier of a ‘giant mangrove swamp’ in northern Australia due to
records of this genus from the eastern Tethys Sea, must have continued estuarine infilling about 6000 years ago
reached West Africa via the Mediterranean. This is further (Woodroffe et al. 1985). Similarly, over the past 12 000
supported by the earlier appearance of Rhizophora in years there has been a large reduction of Rhizophora in the
southern France (50 mya; Gruas-Cavagnetto et al. 1988) and swamps of the Panama isthmus as a result of changing sea-
in the London Clay (45 mya; Chandler 1951) than in North levels, with Rhizophora disappearing from Gatun Lake 4200
(40 mya; Berry 1924, 1930) and South America (38 mya; years ago after dominating the area for the previous 30 000
Germeraad et al. 1968; Van der Hamm 1972). years (Bartlett and Barghoorn 1973). In Guiana, a similarly
Plaziat and Cavagnetto (1996) have suggested that the large reduction in Rhizophora occurred approximately 3500
‘climatic cooling’ of the late Eocene not only changed the years ago with stabilizing sea-levels (Tissot et al. 1988).
species composition and distribution of the mangroves but
also started the process of the differentiation of the ‘old’ and Floristic attenuation with latitude
‘new’ world mangroves during the Oligocene, rather than in The latitudinal limits of mangrove vegetation on each of
the mid Miocene when the Tethys Sea route closed. the major land masses (Table 2) show these limits to be quite
Thus, while some mangroves appear to have evolved in variable and broadly related to temperature and aridity. In
the central Tethys Sea (Mediterranean), several other 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 32°208 28°568 East African–Arabian Peninsula region. The extreme aridity
Pacific America 30°158 5°328 of the ‘Horn of Africa’ (northern Somalia) causes an abrupt
Atlantic Africa 19°508 12°208
Eastern Africa/Red Sea 28°248 32°598
loss of species (Fig. 1), and only Avicennia, Rhizophora,
Western Australia – 33°168 Bruguiera and Ceriops are able to extend north to the
Eastern Australia – 38°458 southern Red Sea.
Pacific Asia 31°218 –
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
Second, new morphological and biochemical markers are Rhizophora in America and Africa, but are apparent in all
being found within species, intraspecific taxa and genera shared by the old world and new (Duke 1995;
populations which will facilitate an improved understanding Bousquet-Melou 1996). On the other hand, morphologically
of the processes of species divergence. These include such based subspecies in Avicennia marina can be recognized on
markers as iridoid glycosides (Fauvel et al. 1995), foliar leaf the basis of allozyme patterns in specimens from western,
waxes (Dodd et al. 1995; Rafii et al. 1996), DNA analyses northern and eastern Australia (Duke 1991b).
(Brajou 1996), isozyme analyses (McMillan 1986; Ballment Taxonomic changes measured by isozymes or DNA
et al. 1988; Duke 1991b; Huang 1993) and cladistic analyses analysis generally require >100 mutations or gene frequency
(Juncosa and Tomlinson 1988; Ricklefs and Latham 1993; changes (because of the relatively insensitive analytical
Bousquet-Melou 1996). techniques), and would therefore be the later stages in
Third, mangroves as a group appear to be relatively slow species divergence. Thus, although subspecies formation
in undergoing evolutionary change. Thus, for example, can be recognized in Avicennia marina on the basis of
Moore (1973) noted that the earliest fossils of Nypa are not isozymes (Duke 1991b, 1995), DNA analysis failed to
distinguishable from the modern Nypa fruticans, concluding demonstrate the differentiation into subspecies in Avicennia
that ‘Nypa has essentially sat still for 70 million years’ — i.e. germinans (Brajou 1996). On the other hand, McMillan
morphologically but certainly not geographically! (1986), using isozyme analysis to determine genetic
Thus, the evolutionary history and relationships of differences among populations of A. germinans, found that
mangroves are becoming better understood while the plants from the western side of the Gulf of Mexico differed
dynamics of the evolutionary processes themselves are in their predominant patterns of phosphoglucose isomerase
becoming clearer. On that basis, it seems likely that the and phosphoglucose mutase from plants on the Caribbean
populations of the most widespread species, e.g. A. marina side of the Gulf of Mexico. Similarly, Ballment et al. (1988)
and A. germinans, are diverging because they no longer differentiated three sibling species of Ceriops by
consist of single inbreeding populations. In the case of A. biochemical genetics which indicated a uniform genetic
marina, this divergence has proceeded further and has been structure within taxa but a high genetic divergence among
recognized by subspecific ranking (Duke 1991b; Everett taxa; that study showed that the sympatric populations of
1994). In A. germinans, on the other hand, this divergence is two taxa maintained fixed differences in genes at a number
not so advanced and has allowed chemotypes but not of loci and were reproductively isolated, without the
morphotypes to be recognized (Compère 1963; Bousquet- presence of any hybrid forms.
Melou 1996). All these diverging processes are happening against the
In an evolutionary sense, biochemical differences background of further fragmentation of populations and
between populations, requiring one or two gene mutations or decreases in species distribution due to anthropogenic
frequency changes only, should be apparent first and that effects. For example, Huang (1993) studied the genetic
seems to be the case. For example, chemotypes of A. variability between and within populations of the mangrove
germinans were readily identifiable in West African Kandelia candel on Taiwan using isozymes and concluded
populations (Dodd et al. 1995), between Pacific and Atlantic that a moderate level of genetic variation existed between
America (Rafii et al. 1996), and between African and the four mangrove populations studied but that there was
American populations (Bousquet-Melou 1996). little differentiation within populations. Local selection and
Physiological changes, requiring at least 5–10 gene restricted gene flow between the populations had
mutations or frequency changes, should become apparent contributed to the limited genetic variability of this species
with further divergence. For example, slight physiological in Taiwan. Thus, it seems likely that this fragmentary
differences were detected between West African mangroves process will accelerate in the mangroves, which appear to be
and American Atlantic mangroves of the same species an inherently slow group to respond in an evolutionary
(Saenger and Bellan 1995). Similarly, ecophysiological sense.
variation in chilling tolerance was studied by McMillan In addition, however, research is underway to determine
(1975) who tested different populations of mangroves from the genetic variation within certain taxa with a view to
30°N to 38°S. Comparison of A. germinans and A. marina in identifying specific genotypes that are ‘high performers’
experimental chilling tests revealed that plants from tropical under specific environmental conditions. At the same time,
climates showed severe damage to all leaves and stems after micropropagation techniques are being developed to
12 successive chilling nights, whereas plants from temperate propagate those specific genotypes. This combination of
climates showed no leaf damage. These preliminary studies genetic selection and micropropagation will add a further, as
have been successful in indicating infraspecific variation yet unknown, dimension to the three primary processes
which appeared to have a genetic basis. discussed.
Morphological changes, which might require >10 In conclusion, a number of poorly understood historical
mutations or gene frequency changes, are not apparent in as well as current processes are implicated in the
284 P. Saenger
biogeography of mangrove communities and species. In Cavagnetto, C., and Anadón, P. (1995). Une mangrove complèxe dans le
addition, evolutionary processes going on at present are Bartonien du Bassin de l’Erbe (NE de l’Espagne). Paleontographica, B
236, 147–65.
tending to cause some of the more isolated species or Chandler, M. E. J. (1951). Note on the occurrence of mangroves in the
populations to diverge. However, and most importantly, London Clay. Proceedings of the Geological Association of London 62,
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processes are based on incomplete data for considerable Chikhi, H. (1992). Une palynoflore méditerranéenne à subtropicale au
areas of the world — a situation that must be urgently Messinien pré-évaporitique en Algérie. Géologie Méditerranéenne 19,
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mangrove resources. in the early Tertiary floras of southern Australia. Geological Society of
Australia Special Publications 4, 79–86.
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