Review of Palaeobotany and Palynology 156 (2009) 358375

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Review of Palaeobotany and Palynology

j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / r ev p a l b o

Comparison of pollen distribution patterns in surface sediments of a Colombian

Caribbean mangrove with geomorphology and vegetation
Ligia E. Urrego a,, Gladys Bernal b, Jaime Polana a
a
b

Departamento de Ciencias Forestales, Universidad Nacional de Colombia, Sede Medelln, AA 568 Medelln, Colombia
Escuela de Geociencias y Medio Ambiente, Universidad Nacional de Colombia, Sede Medelln, AA 568 Medelln, Colombia

a r t i c l e

i n f o

Article history:
Received 18 September 2008
Received in revised form 23 March 2009
Accepted 1 April 2009
Available online 15 April 2009
Keywords:
mangroves
pollen analysis
surface sediments
Caribbean

a b s t r a c t
Distribution patterns of mangrove pollen taxa in recent surface sediments of the lagoon system of Cispat are
compared with geomorphological and vegetational patterns. The pollen spectra of 51 samples show the oral
composition and structure of mangrove stands in three main geomorphic units in the study area. The oldest
mangrove stands, with the highest tree mean diameter at breast height and total height, are represented in
the pollen spectra by the highest mean percentages (N65%) mainly Rhizophora mangle. The area with
estuarine conditions shows, mean mangrove pollen percentages between 35 and 50% reecting the
mangrove colonization process since 1930, as well as current anthropogenic disturbance. Lowest proportions
of mangrove pollen (b 25%) are found in the foothills, reecting high disturbance of mangroves and the
transition from mangroves to terra rme forest. Distribution patterns of the pollen and spores indicate that
water transport is more important than wind transport over short distance and reect local vegetation. Fern
spores and pollen grains of secondary forest taxa and grasslands are widely distributed and reect regional
vegetation. Rhizophora pollen proportions reect its relative abundance in the forest stands. Even low
proportions of Avicennia pollen indicate this species dominance in sparse stands and saline back swamp
conditions. Conocarpus presence provides evidence of supratidal location of stands. An inverse relationship
between proportions of Laguncularia pollen and Acrostichum spores demonstrates successional processes
triggered by anthropogenic disturbance. This is the rst report on pollen in surface sediments in the
Colombian Caribbean. As such, the data should prove valuable in efforts to apply interpretations of marine
records to reconstruct past environmental and climate changes in the Caribbean.
2009 Elsevier B.V. All rights reserved.

1. Introduction
Mangroves are important ecosystems in the oceancontinent
ecotone, not only because of their role as a defense against hurricanes
and other catastrophic events (Dahdouh-Guebas et al., 2005), but also
because of the conspicuous intertidal environment that is home to
many organisms. Mangroves can trap sediment in their roots, which
contributes to the accretion processes of shorelines and helps impede
their erosion (Hogarth, 2007). Additionally, mangroves represent an
important economic resource for the local population, who gather
wood and many non timber forest products such as crustaceans and
sh (Kathiresan and Bingham, 2001).
The oristic composition of mangroves is mainly determined by the
tolerance of different species to substrate and saline conditions, which
in turn determines the dominance of one or various species at a specic
site. Although the local and regional pool of species can also inuence
the composition of the forests (Ellison, 2002). Morphological and
physiological adaptations of true mangrove species determine the

Corresponding author. Tel.: +57 4 4309133; fax: +57 4 4309018.

E-mail address: leurrego@unalmed.edu.co (L.E. Urrego).
0034-6667/$ see front matter 2009 Elsevier B.V. All rights reserved.
doi:10.1016/j.revpalbo.2009.04.004

existence of monospecic stands on specic environmental conditions. Rhizophora mangle dominates in sites on unstable substrate and
direct tide inuence, due to its aerial roots and pneumatophores. While
Avicennia germinans is the dominant species in highly saline inland
soils, Laguncularia racemosa is commonly found in less saline
environments and more disturbed stands (Hogarth, 2007).
Mangroves can grow along different environmental gradients
determined by salinity, landforms, and soil types that result from the
uvio-marine dynamics (accretion or erosion) (Thom,1984; Woodroffe,
1992). The specic ecological conditions where mangroves ourish
make them very sensitive to environmental changes such as sea level
rise, discharges from oodings by rivers, uvio-marine dynamics,
storms, changes in precipitation and seasonality due to ENSO, and
other climatic factors (Blasco et al., 1996; Alongi, 2008). The sensitivity
of mangroves to environmental changes has made them good indicators
of past sea level changes (Ellison, 1996; Behling et al., 2001; Cohen et al.,
2005; Engelhart et al., 2007), evolution of estuarine-lagoonal systems
(Carvalho do Amaral et al., 2006), as well as geomorphologic changes
and post glacial marine transgressions (Scourse et al., 2005; Gonzlez
et al., 2006; Mndez-Linares et al., 2007).
Past environmental reconstructions of mangroves and intertidal areas have been based on palynological analysis, mainly on the

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uctuations of relative abundances of mangrove species, mostly

Rhizophora mangle, along sediment cores, since it is a prolic pollen
producer and is present in most pollen spectra of marine cores.
The spatial distribution of Rhizophora pollen in surface samples
and core tops, and its relation to their sources has been used to
reconstruct sea level changes and shore line positions in the past
(Behling et al., 2001; Van Campo and Bengo 2004; Hooghiemstra
et al., 2006; Engelhart et al., 2007). Due to the low frequencies of
pollen of Avicennia germinans and Laguncularia racemosa, that are
poor pollen producers and insect pollinated (Hogarth, 2007), information on past vegetation dynamics, (e.g. succession and ) and
mangrove distribution along environmental gradients involving
Avicennia germinans and Laguncularia racemosa is still scarce.
Especially in the Colombian Caribbean in particular no records on
surface sediments have been obtained.
This study aims to evaluate whether surface pollen distribution
patterns reect the composition and structure of the mangroves in
Cispat lagoon system, and the geomorphological processes that
determine this vegetation. It would contribute to improve the
interpretation of marine pollen records in terms of changing past
environments in the Caribbean.
2. Study site
The study was carried out at the Cispat Bay lagoonal system,
located on the northwestern Caribbean coast of Colombia (Fig. 1). It is
part of the Sin River valley, one of the main Colombian rivers that
drains into the Caribbean Sea. The study area is located at the former
Sin River delta. The site is delimited by the Mestizos spit to the north,
the Cispat Bay to the east, the present Sin River bed to the west and

359

the Cispat ridges to the southwest. The predominant geomorphological units are related to the uvial marine processes, specically the
Sin River delta progradation during late Holocene (Robertson and
Chaparro, 1998; Serrano, 2004) and present uvio-marine processes
(Ministerio de Ambiente et al., 2004).
From the 880 km2 occupied by mangroves on the Colombian
Caribbean coast, 125 km2 is located in the Cispat Bay area, being one
of the most important areas in the Caribbean covered by this
vegetation (Snchez-Pez et al., 2004). The geomorphology of the
estuarine-lagoon system located at the Cispat Bay and its relation to
the Sin River delta dynamics has been described (Robertson and
Chaparro, 1998; Serrano, 2004), as well as the structure and plant
composition of the mangrove stands (Snchez-Pez et al., 1997; UlloaDelgado et al., 1998; Gil-Torres and Ulloa-Delgado, 2001; Ministerio de
Ambiente et al., 2004).
In 1762, Cispat Bay was a small body of water enclosed within the
Mestizos spit, where the Sin River delta was located. A marine
intrusion made the mangrove colonization on the spit possible when
inlling of the bay took place between 1849 and 1938 and the delta
became a complex of channels, swamps and lakes. After 1938,the river
bed abandoned the Cispat bay and started the present delta at a site
called Tinajones. A new marine intrusion gave place to the establishment of new mangrove stands on this plain, which process is still
taking place (Serrano, 2004). Since the Sin River no longer drains
directly into Cispat Bay, the fresh waters ow mainly through the
Sicar and Grande channels. These waters reach the shore line at the
bay, after distributing water into small lakes and an estuary, through a
network of smaller channels (Snchez-Pez et al., 1997).
The climate of the Colombian Caribbean is inuenced by the Inter
Tropical Convergence Zone. North and north-east trade winds hit the

Fig. 1. Location map of the study area. Geomorphological units littoral, estuary and foothills are shown.

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area from December to April (the dry season). During the wet season
(May to November) trade winds are weak and eventually the
Caribbean coast experiments south-west winds. The mean monthly
precipitation decreases during JuneAugust giving place to a mid wet
season short drought. Precipitation increases from shore to inland,
with uctuations between 1400 and 2000 mm (IDEAM, 2001).
Discharges of the Sinu River are 152 m3/s during dry season, and
495 m3/s during wet season and they are coupled with Caribbean
seasonality (Quiceno, 2008). The mean annual temperature over the
basin is 27 C (Snchez-Pez et al., 1997).
Two sea currents inuence the Colombian Caribbean. During the
dry season the Caribbean Current runs westward, and during the rainy
season the coastal Panam Countercurrent runs eastward. The regime
of the tides in the zone is semidiurnal, with an average of 0.4 m. Along
the Mestizos spit, the water transports a high load of sediments in a
westeast direction but this process is interrupted at Cispat Bay by a
calm waters zone, where muddy and calcareous sediments are
deposited (Molina et al., 1994). The discharge of the Sin River
inuences the hydrology of the zone where water salinity is always
under 34.
The salinity in the Cispat lagoon system shows a northeast
southwest gradient, being higher along the Salado Channel to the
north and the Cispat Bay to the east, and lower toward the Ostional
lagoon in the west, and the estuarine zone to the south. Seasonal
differences have also been recorded. The zone with the highest
salinity is wider during the dry season than the rainy season (Ruiz,
2006). However, salinity and hydrology of the system is changing with
sea level rise. For Colombian Caribbean has been estimated a sea level
rise between 2 and 3.6 mm/y during the 19071997 time span
(Torres-Parra et al., 2006).
3. Present vegetation
The Coastal vegetation has been widely studied (Gil-Torres and
Ulloa-Delgado 2001; Snchez-Pez et al., 2004, 1997). According
to geomorphology, distance to the coastline, fresh water inputs
(Snchez-Pez et al., 1997) and the distance to the present Sin river
delta, three vegetation types can be recognized. The littoral zone , is
situated between the shoreline and the Salado Channel. This zone
encloses the Mestizos spit, and is the northern limit of the system. An
estuarine zone is located between the Salado Channel and the Grande
Channel, and is characterized by the highest fresh water input through
several Sin River channels and streams that drain in a WE direction
into the Caribbean Sea. A third zone is located between the Grande
Channel and the foothills of the mountains. In the three zones, the
dominant mangrove species are Rhizophora mangle, Laguncularia
racemosa and Avicennia germinans. Conocarpus erectus and Pellciera
rhizophorae were also found but with lower frequencies than former
mangrove species.
The oldest and most structurally developed mangrove stands are
found in the littoral zone. They grow on young sandy soils under tidal
inuence (Ulloa-Delgado et al., 1998). The vegetation density is the
lowest (951 trees/ha) but the mean diameter at breast height (DBH),
the mean total tree height and the wood volumes are highest
(10.68 cm, 9.98 m, 138.4 m3/ha, respectively). The dominant species
are Rhizophora mangle and Avicennia germinans, but a high density of
Pellciera rhizophorae treelets is also found. The relatively high salinity
(35) in some sites in this zone has favored the establishment of
mono-specic Avicennia germinans stands; although in some places
these stands grow in association with Laguncularia racemosa and
Rhizophora mangle (Snchez-Pez et al., 1997; Gil-Torres and UlloaDelgado 2001). On the sand bars, seaward along the Mestizos spit,
coastal dynamics have caused high mangrove mortality, either by
erosion and the subsequent substrate loss, or by high sedimentation
loads that have caused anoxia to the tree roots (Gil-Torres and UlloaDelgado, 2001). In addition to the mangrove species, other herbs and

shrubs can be found in this zone, such as: Batis maritima, Melochia
cresanta, Sporobolus poiretti, Salicornia fruticosa, Ipomoea pes-caprae,
and Sesuvium portulacastrum. Poaceous species of the genera Brachiaria and Eragostis are also commonly found.
The estuarine zone was the previous Sin River delta. The bay was
open sea until the 18th century, and no mangroves were found. Silting
of the bay after the change of the Sin River delta in 1849 and high
fresh water availability, gave place to rice elds. In 1930, when the
river delta migrated again to the northwest, and due to the
consequent increase in soil salinity, the area became unsuitable for
rice production, and mangrove stands eventually took over. The forest
stands in this zone show the highest density and basal area values
(1688 trees/ha, 16.37 m2/ha, respectively), mainly of treelets and small
trees. Large mono-specic Rhizophora mangle stands are also
frequently found there. Toward the inner part of the zone, in sites
with less fresh water inputs Laguncularia racemosa and Avicennia
germinans dominate the stands. In this zone mangroves are most
exploited, and as such has contributed to these low basal area values
(Gil-Torres and Ulloa-Delgado, 2001). Nevertheless, some restoration
programs have been designed in order to protect and recover the
mangrove forests and their faunal resources.
The mangrove fern Acrostichum aureum is also commonly found at
sites with low salinity values, as well as at sites which reach minimum
salinity values during the rainy season. Floating vegetation is
characterized by Eichornia crasipes, Pistia stratiotes, Nymphoides indica,
Ludwigia peploides, Marsilea policarpa, among others.
In the foothills zone, despite the fresh water inputs that come from
some small river channels, the obstruction of some channels by
alluvial sediments and dead trees has caused hypersalinization of the
soils toward the inner part of the mangrove stands. The forest stands
are composed of Rhizophora mangle, Avicennia germinans and Laguncularia racemosa. The tree density is high (1511 trees/ha) but the total
tree height and mean DBH are relatively low (6.18.97 m and 6.07
7.3 cm, respectively). The increasing salinity has favored the
establishment of Avicennia germinans stands; however, these stands
are not being exploited as their wood is not appreciated by the local
people (Snchez-Pez et al., 2004, Gil-Torres and Ulloa-Delgado,
2001). Many tree species and climbers from secondary forests can be
found in this zone, such as Guazuma ulmifolia, Astronium graveolens,
Spondias mombin, Ceiba pentandra, Hura crepitans, Nectandra concinna,
Lecythis minor, Chamaestula fruticosa, Lonchocarpus sanctae-martae,
Macherium capote and Anacardium excelsum. Grasslands and livestock
elds neighbor the zone and many other trees such as Pithecellobium
saman, Enterolobium cyclocarpum, Sterculia apetala, Pseudobombax
septenatum, Bombacopsis quinata, Sapium aucuparium, Gliricidia
sepium, Tabebuia rosea and Cedrela odorata grow sparsely in the
foothill zone (Ministerio de Ambiente et al., 2004).
4. Methods
The eldwork was carried out in September 2005 (Ruiz et al.,
2008). Sixty four samples, widely distributed on the Cispat Bay, were
collected (Fig. 1). Surface sediment samples of 1 cm thick were taken
with a manual corer. The samples were obtained from the oor of the
lakes, some sites next to river channels and from supercial soils of the
mangrove stands.
Pollen samples of 3.5 cm3 were treated with standard preparation
techniques, which include pretreatment with KOH (10%), sodium
pyrofosfate (10%), HF (10%) and HCl (10%), followed by acetolysis
(Erdtman, 1960). Some samples with a very small organic fraction,
were also gravity separated with bromoform. One pellet with exotic
Lycopodium spores was added to each sample in order to calculate
pollen concentration values. The residues were mounted in a glycerin
jelly and were analyzed with an Olympus light microscope. A
minimum of 300 pollen grains was counted in each sample. Trees,
shrubs, herbs, climbers, and spores of the mangrove fern Acrostichum

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Fig. 2. Dendrogram, pollen zones grouped by cluster analysis. The correspondence with geomorphological units is indicated.

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aureum were included in the pollen sum and their relative abundance
was calculated on this basis. Other fern spores and microforaminifera
were not included in the pollen sum, but their percentages were
calculated based on this total. When the presence of Rhizophora
mangle was too high, at least 100 grains of the other species were
counted. The identication of the pollen grains and spores was based
on the reference collection held at the Ecology Laboratory of Forestry
Science Department of the National University of Colombia and some
published pollen atlases (Roubik and Moreno, 1991; Herrera and
Urrego, 1996; Colinvaux et al., 1999; Willard et al., 2004) and the
online tropical pollen data base of Bush and Weng (2007).
Spatial distribution of these data was evaluated by means of a
cluster analysis using the Ward's method and the Euclidean distance
in STATGRAPHICS Centurion XV version 15.1.02 (Stat point. INC., 1982
2006). The percentage pollen diagram was drawn using the C2
program (Juggins, 2003). Isopollen (lines with equal relative pollen
abundance) maps of the most widely distributed species were drawn
using SURFER version 8.02 (Golden software, INC., 2002) and kriging
interpolation method.
5. Results
Fifty one out of the 64 samples reached the minimum pollen sum
(300 grains). We distinguished 121 pollen taxa, 24 fern spores, one
microforaminifera and one thecamoeba species. Taxa with relative
abundance higher than 2% were included in the Cluster Analysis
(Fig. 2) and shown in the pollen diagram (Fig. 3).
The Cluster Analysis classied the samples into four groups. In the
pollen diagram (Fig. 3) the samples were sorted from top to bottom, as
grouped by the cluster analysis, and the vertical sequence of the
second and third groups was inverted in order to visualize spatial and
compositional proximity of the groups. On the left of the diagram,
mangrove and salt marsh taxa were sorted, followed on the right by
secondary forest and other taxa. In this diagram, three samples were
taken out of their clusters and moved to the proper ecological group.
The rst group enclosed nine samples located on the littoral zone
(Gil-Torres and Ulloa-Delgado, 2001) (Fig. 2). Three samples, included
in a separate cluster and located on the shoreline at the Mestizos
spit, were also encompassed within this group. In this cluster 67
pollen taxa and nine fern spores were identied. Mangrove taxa
showed highest proportions (70%), with values between 37 and 75%.
Rhizophora mangle was the most important taxon and reached 75% in
some samples; Laguncularia racemosa was the second and reached
30%. Avicennia germinans and Conocarpus erectus never reached values
higher than 2%, except in one sample where values showed 7% and 2%
respectively. Poacaeae (14%), Macherium (13%) and Senna (8%) also
reached relatively high proportions. Other taxa were present with
lower values, such as Ambrosia (4%), Cyperaceae (4%) and Araceae 1
(3%).
The second cluster grouped six samples located at the bayshore
under direct tide inuence; one sample placed at the shore line in the
littoral zone was also included in this group. The cluster analysis
incorporated in this group one sample from the foothills zone; it was
moved to its proper ecological group. Seventy seven different pollen
taxa and 18 fern spore taxa were identied in this cluster. The average
proportion of mangrove taxa is 30%. Rhizophora mangle (733), and
Laguncularia racemosa (317) are the dominant species. Avicennia
germinans and Conocarpus erectus are present in a few samples with
values lower than 1%. The mangrove fern, Acrostichum aureum reaches
values of 9% whereas other fern taxa reached 19%. In this group, taxa
from salt marshes, such as Cyperaceae (16%), Typha (11%), Ambrosia
(4%) and Salicornia (3%), reach their highest percentages. Taxa from
the secondary forest are frequent in this cluster and the presence of
several Leguminosae trees such as Caesalpiniaceae (29%), Fabaceae
(28%), Senna (25%), and Macherium (3%) is noteworthy. It is noted
that in this group, values of microforaminifera are rather high (10%).

The third cluster clumps together 14 samples located in the

estuarine zone. This group also includes one sample located on the
shore of the bay. In this cluster, sixty two pollen taxa and ten fern
spores are distinguished. Mangrove taxa values are lower than the
rst group, but higher than the second. The mean proportion of
mangrove taxa was 55% with Rhizophora mangle and Laguncularia
racemosa reaching values of 43 and 25%, respectively. Avicennia
germinans reaches relatively high percentages in only two samples
(11% and 13%); Conocarpus erectus is also present in two samples with
values below 4%. The Leguminosae group reaches higher values than
in the former group: Senna (41%), Fabaceae-PI (36%), Caesalpiniaceae
I (24%), Macherium (9%) and Lonchocarpus (4%). The herbs, Cyperaceae and Poaceae reach 7%. Acrostichum aureum reaches 25%, other
fern spores reach 10%, and Microforaminifera reaches 27%.
The last group encompasses 18 samples, located between the
northern shore of the Grande Channel and the foothills, and includes
those samples found in the surroundings of the Soledad lagoon in the
southern part of the study zone. One sample previously included in
the cluster analysis in the bay shore group, was drawn within this
group of taxa. The highest number of taxa (84 pollen taxa and 14 fern
spore taxa) was identied in this group. Mangrove percentages
display relative low mean values (25%); only in two samples Rhizophora mangle and Laguncularia racemosa reach values higher than
30% and 17% respectively, however, in most of the samples their
values oscillate between 5% and 20% for Rhizophora mangle and 2%
14% for Laguncularia racemosa. The fern Acrostichum aureum reaches
the highest values (66%), with other fern spores showing similarly
high values. Avicennia germinans reaches a relatively high percentage
in one sample (14%) but its percentages in the other samples are lower
than 2%. Conocarpus erectus is present in most of the samples
with percentages lower than 5%. Most taxa display percentages
lower than 2%; only some Leguminosae (Senna, Caesalpiniaceae,
and Fabaceae) display values that reached 29%. Lonchocarpus and
Macherium reach 6%. A constant presence of Poaceae and salt marsh
vegetation (Typha, Ambrosia, Salicornia, Cyperaceae) is recorded in
most of the samples with values that reach 4% for the rst, and 9% for
the second taxa.
Surface pollen maps show the distribution of the main taxa
grouped into vegetation units: mangroves, herbs and salt marsh
vegetation, and other palynomorfs. These will be discussed in the
following section.
6. Discussion
6.1. Matching pollen samples and standing vegetation
A cluster analysis of the pollen samples maps the present geomorphological and vegetation units in the study area (e.g. SnchezPez et al., 1997; Gil-Torres and Ulloa-Delgado, 2001). Although no
paired structural data of the standing vegetation were available, some
qualitative relations between the pollen data and vegetation structure
can be established. The four clusters match the local littoral, estuarine
and foothill vegetation zones, and a zone comprising the Cispat Bay
shoreline.
The rst group ts the littoral zone described by Snchez-Pez
et al. (1997) and Gil-Torres and Ulloa-Delgado (2001), and is the site
of the oldest and most vigorous mangroves. Historical maps show that
these mangroves were established during the 18th century when the
delta was located at this site. These well established mangroves show
the highest percentage of mangrove pollen (70%) among groups. As in
the Orinoco delta (Muller, 1959; Hoffmann, 2002), local mangrove and
salt marsh pollen represented only 14% of the taxa, but more than 70%
of the sum, consistent with the relative dominance of their standing
vegetation.
Rhizophora mangle is a prolic pollen producer (Muller, 1959;
Hogarth, 2007) and is overrepresented in most records (Behling et al.,

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Fig. 3. Pollen diagram. Taxa are clustered into ecological groups. From bottom to the top pollen spectra reect geomorphological units.

pp. 363368

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369

Fig. 4. Distribution maps of pollen percentages of mangrove taxa (a. Rhizophora mangle, b. Avicennia germinans, c. Laguncularia racemosa, d. Conocarpus erectus, e. all mangrove taxa,
Acrostichum aureum (f.).

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2001). Pollen production data for Rhizophora mangle are not available
for this study, but pollen percentages maintain a relationship to
standing vegetation structural parameters. The top pollen percentages
t the highest mean quadratic diameter (12.9 cm) and the mean total
height of the trees (25 m), and are indicative of the age of the forest
stands. Laguncularia racemosa pollen percentages are also high, and t
a mean quadratic diameter (16.3 cm) (Gil-Torres and Ulloa-Delgado,
2001). Large standing Avicennia germinans trees are present, but their
pollen percentages are rather low, an apparent discrepancy that can be
accounted for their poor pollen production (Hogarth, 2007). The
highest proportion of Poaceae pollen (14%) is attained within this
littoral group. Several species of Poaceae have been recorded on sandy
beaches along the Mestizos spit (Snchez-Pez et al., 2004), as have
some leguminous (e.g., Senna) treelets and Cyperaceae herbs.
The second cluster includes the shoreline samples at the bay, where
several channels discharge and salt marsh conditions predominate.
The pollen record is mainly characterized by salt marsh vegetation
(Cyperaceae, Typha, Salicornia and Ambrosia). Behling et al. (2001)
sampled pollen rain from a salt marsh with similar percentages of
Cyperaceae and Rhizophora mangle. The recorded Rhizophora mangle
proportion (30%) is related to pollen transport by watercourses, and is
comparable to that in the Ntem River mouth in Cameroon (Van Campo
and Bengo, 2004) and offshore west Equatorial Africa (Lzine and
Hooghiemstra, 1990). Additionally, fern spores, some dominant
legumes, mangrove taxa and many allochthonous pollen grains are
transported into this area by river tributaries after crossing the
estuarine zone. The vegetation source of 77 pollen and 19 fern spore
taxa found in the estuarine zone is probably upstream, conrming that
water is likely the main transport mechanism.
In the estuarine zone (sensu Ulloa-Delgado et al., 1998), salinity
conditions uctuate between 5 and 35, not only because of tidal
inuences but also because of the many lakes and channels crossing it.
Though high, the mangrove pollen percentages in this zone (up to
58%) are less than those in the littoral zone. This is probably due to the
high standing Rhizophora mangle basal areas, which are comparable to
those of dense small trees (1599 trees/ha) in young forest patches
reported by Gil-Torres and Ulloa-Delgado (2001).
There are three possible explanations for the early successional
stage of these stands. First, after 1930 the soils became salinized by
marine intrusion (Serrano, 2004) and the mangroves replaced the rice
elds of the Sin River delta (Fig. 1). Mortality of larger trees caused by
currently rising sea level (Ruiz et al., 2008) could also account for the
mean age of the stand and decline in pollen production, as has been
described for Australian mangroves (Scourse et al., 2005). Second, the
ongoing process of bay inlling and substrate stabilization are enabling
mangrove colonization. Finally, extensive Rhizophora mangle timber
extraction (Snchez-Pez et al., 2004) has created forest gaps that have
been invaded by Acrostichum aureum, as is also recorded in some
pollen samples. The mismatch between pollen percentages and the
high basal areas and young standing tree densities previously recorded
(Gil-Torres and Ulloa-Delgado, 2001) reveals the presence of both
natural and human disturbances on mangroves.
In the foothills zone, tree density (1511 trees/ha) is higher than in
the littoral zone, but lower than that in the estuarine zone. The
southeastern mangroves closer to the foothills also have the lowest
basal areas and smallest proportion of mangrove pollen relative to
other zones. The lower basal areas can be explained by soil
hypersalinization (2045), which, in turn, can be due to lower
freshwater discharge (Gil-Torres and Ulloa-Delgado, 2001) and rising
sea level (Bernal et al., 2008). The high frequency of Acrostichum
aureum spores is an indication of the early forest successional stage
after recent timber extraction (Gil-Torres and Ulloa-Delgado, 2001).
The high number of pollen and spore taxa may be linked to pollen
transport from the neighbouring secondary forest via wind and water,
as well as the presence of many Leguminoseae trees left standing in
cattle elds to provide shade.

The highest Rhizophora mangle pollen percentages (N65%) are found

on and adjacent to the pure mangrove stands or the coasts; the lowest
(b25%) are in landward stands, as has been described in Indonesia
and Africa (Hooghiemstra and Agwu, 1986; Lzine and Hooghiemstra,
1990; Van Campo and Bengo, 2004; Engelhart et al., 2007).
Rhizophora pollen values in the 30% range have been reported in
adjacent tidal ats (Hoffmann, 2002) or at the limit of the intertropical front in offshore marine samples from the Gulf of Guinea
(Hooghiemstra and Agwu, 1986). Rhizophora pollen values of approximately 50% have been found elsewhere between open tidal ats
and mangrove stands (Engelhart et al., 2007). Mangrove pollen in
marine sediments is a good indicator of mangrove zonation and the
disturbance of continental stands. It also reects the strong geomorphologic and hydrologic inuence on mangrove composition and
distribution (Grindrod et al., 1999).
6.2. Pollen distribution and transport of the individual taxa
Isopollen maps were used to visualize the spatial distribution of
taxa and their relationship to the coastline. The spatial distribution of
some pollen taxa also reects previous zonation, and the relationship
to source areas and operating transport vectors. Fig. 4 (ae) shows the
mangrove species spatial distribution.
Despite its high worldwide pollen production (Muller, 1959;
Hooghiemstra and Agwu, 1986; Lzine and Hooghiemstra, 1990;
Ellison, 1996; Behling et al., 2001; Van der Kaars, 2001; Van Campo
and Bengo, 2004), Rhizophora mangle percentages continue to
decrease along a northsouth gradient, matching the forest age
structure. The high percentages of Rhizophora mangle pollen close to
the major stands (N60%) match local forest conditions and proximity
to sources (Hooghiemstra and Agwu, 1986; Sun et al., 1999; Elenga et
al., 2000; Behling et al., 2001; Van der Kaars, 2001; Van Campo and
Bengo, 2004; Moss et al., 2005; Engelhart et al., 2007). Nevertheless,
transport vectors (wind, water) and the distance to pollen sources
play important roles, as does species phenology. Phenological studies
have shown that Rhizophora mangle owers all year long in the
Colombian Caribbean (Ulloa-Delgado et al., 1998) and in other
neotropical sites (Behling et al., 2001; Hoffmann, 2002). The owering
peaks occur during the dry season, when the highest distribution of
pollen by wind probably takes place. However, long-distance wind
transport of pollen from either the estuarine zone or the foothills to
the littoral zone, where the highest percentages are recorded, is
unlikely because northeast trade winds would blow the pollen
westward. During the rainy season, when southwestern trade winds
play a role in transport, the majority of the grains fall into the water;
thus higher importance is attached to water transport of Rhizophora
mangle pollen (Hooghiemstra and Agwu, 1986; Lzine and Hooghiemstra, 1990; Hoffmann, 2002). The paramount role of water
transport for pollen is also supported by the mean pollen percentage
in the Cispat Bay shoreline samples. Pollen grains from a very wide
area could conceivably be carried to sea by several west-to-east
running streams and channels that give the shoreline pollen spectra a
regional signicance. The predominance of water over wind transport
mean that the pollen spectra in Caribbean offshore cores show
vegetation changes that reect geomorphology, river discharges and
upstream climate variations. Because they run far from the coast,
marine currents do not inuence pollen transport; however, they
affect offshore deep-sea sediments, and thus could be relevant for
paleoclimate reconstructions in the Caribbean.
The widespread distribution of Laguncularia racemosa pollen
grains in the study area (Fig. 4b) is comparable to that in Pacic
Panamanian mangroves (Beneld et al., 2005), and can be explained
by river currents. The relatively high percentages of Laguncularia
racemosa pollen, which are greater than that reported by Behling et al.
(2001), might be attributable to growing conditions in the study zone.
This species was commonly mixed with Rhizophora mangle, especially

L.E. Urrego et al. / Review of Palaeobotany and Palynology 156 (2009) 358375

on stabilized substrates (Gil-Torres and Ulloa-Delgado, 2001) and

under lower salinity conditions (Medina et al., 1990). Although Laguncularia racemosa usually owers during the rainy season (UlloaDelgado et al., 1998) and is considered a poor pollen producer
(Behling et al., 2001; Hogarth, 2007), it starts to ower at a very early
age under stress conditions and owers year-round in the study area
(Ulloa-Delgado et al., 1998). Additionally, Rhizophora mangle exploitation is paving the way for Laguncularia racemosa colonization, and
represents a signicant anthropogenic disturbance (Hogarth, 2007).
The presence of signicant proportions of Laguncularia pollen in
Caribbean marine records may further indicate disturbance of
mangrove stands.
In our study area, Avicennia germinans pollen is under-represented
in relation to Rhizophora mangle, as has been reported at other sites
(Muller, 1959; Behling et al., 2001; Van Campo and Bengo, 2004). The
asymmetrical relationship between high basal area and low pollen
percentages reects the poor pollen production by Avicennia germinans (Ellison, 1996; Behling et al., 2001; Hogarth, 2007). However,
high percentages (10%12%) in a few samples are associated with
monospecic stands landward of the estuary (Engelhart et al., 2007)
and in the surrounding Salado Channel littoral zone (Gil-Torres and
Ulloa-Delgado, 2001).
In Avicennia germinans-dominated forests described elsewhere
(Behling et al., 2001), Avicennia germinans pollen is better represented
(1535%) than in our study area (b2%). This is also the case in mixed
Rhizophora mangle/Avicennia germinans stands, where Behling et al.
(2001) found Avicennia germinans pollen percentages of 2% to 5%. The
low A. germinans representation corresponds to its patchy standing
distribution. It is worth noting that even a low proportion of Avicennia
pollen indicates saline conditions typical of those found in salt pans.
Conocarpus erectus is poorly represented in both the pollen spectra
(Figs. 3 and 4d) and the standing vegetation (Gil-Torres and UlloaDelgado, 2001). However, its pollen distribution pattern match well
with littoral zone forest stands on more stabilized substrates and
inland mangroves of the estuarine zone. Above all, the pollen
distribution corresponds to stands close to the foothills, as has been
described by Tovilla and De la Lanza (1999) for an inland habitat in
Mexico. Despite the low percentage of Conocarpus erectus pollen and
vegetation, its presence could denote the position of the intertidal
zone and indicate displacements of the coastline.
The distribution of Acrostichum aureum spores (Figs. 3 and 4e) is
another good indicator of natural and anthropogenic standing
vegetation disturbance (Dahdouh-Guebas et al., 2000), because this
fern is known to invade open areas (Dahdouh-Guebas et al., 2005).
Acrostichum aureum predominates (i) in the undergrowth of open
mangrove stands in the estuarine zone, (ii) in the foothills, and (iii) on
the shorelines of streams and channels. This species colonizes forest
gaps under less saline conditions, where it competes for light with
Laguncularia racemosa. This can cause its elimination through shading
(Medina et al., 1990). The pollen diagram (Fig. 3) shows this antagonic
behaviour, where the presence of spores can be an indication of
cryptic ecological degradation (sensu Dahdouh-Guebas et al., 2005).
6.3. Herbs and salt marsh vegetation
The pollen distribution of salt marsh species is shown in Fig. 5. The
highest pollen percentages of Typha (Fig. 5a) are found mainly in
the foothills and on the shoreline of the Cispat Bay. Its standing
vegetation has been recorded along the oodplains of the Sin River
and its tributaries, and next to the foothills (Ministerio de Ambiente
et al., 2004). This pattern also indicates the rise of the water table and
saltwater dilution (Lzine and Hooghiemstra, 1990).
Ambrosia (Fig. 5b) and Cyperaceae (Fig. 5c) are also characteristic
inhabitants of salt marshes and permanently ooded sites (Behling
et al., 2001; Bush, 2002) surrounding the mangroves at Cispat
Bay. Their highest pollen percentages can be related to salt marsh

371

expansion due to rising sea levels (Gonzlez and Dupont, 2009) and
subsequent inlling of the bay. These species must be considered an
important indicator of the current water level increase, which reects
the combined effects of rising sea level and increasing precipitation
(Ruiz, 2006).
Although Poaceae species are found in secondary forest patches
and grasslands, the highest percentages of Poaceae in the pollen
spectra are found on recently deposited littoral zone sandbars.
Although these are anemophyllous plants, transport to Cispat Bay
by water currents is also feasible. Their presence, as is the case with
Cyperaceae, represents direct tidal inuences, sediment relocation
(Gonzlez and Dupont, 2009) and the current expansion of salt
marshes. Nevertheless, changes in the percentage of Cyperaceae and
Poaceae pollen also evidence the conversion of forests to crop elds
(Bush, 2002; Moss et al., 2005). As in other coastal plains (Elenga
et al., 2000), grasslands surrounding the foothills mangrove forests
are also an additional pollen source. Their taxa are signicant
indicators of both local continental and regional rises in water level
(Lzine and Hooghiemstra, 1990).

6.4. Andean, lowland and secondary forest vegetation

Pollen grains of trees and climbers from sources outside the
mangrove area also recorded among the spectra. Some of these, such
as Alchornea, Alnus, Croton, Hedyosmum, Iriartea and Podocarpus,
come from the Andean forest. Additional taxa, most likely from the
lowlands, are Acalypha, Arrabidaea, Cedrela, Jacaranda, Macrolobium,
Myrcia and Tabebuia. Low representation of lowland and lower
montane forest vegetation in the pollen spectra is common in marine
samples far from their sources (Sun et al., 1999; Van der Kaars, 2001).
Accurate recognition of regional diversity is limited by the predominance of mangrove pollen (Weng et al., 2006), and thus little can be
said about the ecological signicance of these species within the
marine pollen spectra.
The highest representation of secondary forest species is recorded
in foothills samples, where pollen grains could be transported
downward by wind and runoff. Mangroves represented a low
percentage of the vegetation here, and the higher number of taxa is
reected in the pollen spectra. This reproduces the composition of the
upstream vegetation, as was shown in the Orinoco delta (Hoffmann,
2002). In particular, some Leguminosae taxa (Lonchocarpus, Macherium, Senna) frequently grow in grasslands and secondary forests close
to the mangroves (Ministerio de Ambiente et al., 2004). Many of these
legumes ower at the end of the dry season and at the beginning of
the rainy season. The presence of their pollen in mangrove samples is
augmented not only by trade winds that hit the foothills during the
dry season, but also by runoff, which removes and transports deposits
seaward during the rainy season (Sun and Beug, 1999).
Allochthonous taxa increasingly dominate the pollen spectra
toward the southern foothills zone, where the neighbouring vegetation diversity is also higher than in the mangrove stands to north. In
the northern mangrove-dominated littoral zone, the bulk of pollen is
comprised of autochthonous mangrove taxa, as was the case in the
Orinoco delta (Hoffmann, 2002). This fact has direct implications for
the interpretation of marine records: low mangrove pollen percentages could be a reection of high amounts of allochthonous pollen
transported downward by uvial currents rather than an indication of
lesser mangrove dominance onshore, as has been previously highlighted (Moss et al., 2005; Carvalho do Amaral et al., 2006; Engelhart
et al., 2007).
The high number of allochthonous taxa and the mean percentages
of mangrove pollen in estuarine and shoreline samples do not
correspond well with the high standing tree density. Signicantly,
the uvial network allows the inwash of terrestrial pollen taxa to the
tidal at. Weng et al. (2006) have pointed to this as a dominance effect

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L.E. Urrego et al. / Review of Palaeobotany and Palynology 156 (2009) 358375

Fig. 5. Distribution maps of pollen percentages of herbs and salt marsh vegetation. a. Typha, b. Ambrosia, c. Cyperaceae, d. Salicornia, e. Ambrosia and f. all salt marshes taxa.

L.E. Urrego et al. / Review of Palaeobotany and Palynology 156 (2009) 358375

373

of local pollen on constant total pollen sum compared to the

proportionally low size of the depositional basin.
6.5. Other microfossils
Fig. 6a shows the distribution of fern spore taxa. Fern spores
appeared in most samples, but the highest percentages are found
close to the lakeshores, watercourses and the sea. They do not appear
in mangrove stands, as has been reported by Hoffmann (2002). Spores
are produced in the neighbouring vegetation, mainly in humid
upslope forests (Hooghiesmtra and Agwu, 1986). They are transported
by water (Van Campo and Bengo, 2004), especially by river channels
running eastward to the lakes and the sea. For fern spores, water
appears to be more important than wind as a transport vector
(Hooghiemstra et al., 2006; Sun et al., 1999; Van der Kaars, 2001). Fern
spores in bay-shore sediments indicate that spores (i) originate in the
Andean forest, (ii) are transported by the river, and (iii) contribute to
the regional representation.
The microforaminifera, Trochammina inata, and the thecamoeba,
Arcella cf. vulgaris, are also found in the samples. The most important
microforaminifera species in a recent study of a lagoonal system was
T. inata (Bernal et al., 2008). This agglutinated foraminifer is well
preserved in the acidic mangrove soils, as found by Woodroffe et al.
(2005) in Australian sediments. The highest relative abundance of
T. inata (Fig. 6b) is found towards the shorelines, especially at the
mouths of streams. Bernal et al. (2008) related the distribution of this
species to more river transport-inuenced, less saline environments.
The abundance of T. inata in the samples may also reect its
tolerance to the acids used in sample preparation; hence, it is not
possible to use its presence as an accurate paleoenvironmental
indicator. Consistent with this, Castao (2007) found very few tests
in a 4-m deep core drilled in a lake close to the mangroves at the study
area.
The highest percentages of A. cf. vulgaris (Fig. 6c) are found in
swamps and channels close to the present Sin River bed, and in the
Salado Channel in the western part of the estuary. Testate amoebae in
coastal sediments have been recognized as indicators of saline and
freshwater transition (Charman, 2001) and, hence, sea level changes
(Charman et al., 2002). Some species of Arcellaceans, especially
A. vulgaris, have been recorded in lakes with low pH, and high iron and
aluminum levels (Kumar and Patterson, 2000). In the Cispat lagoonal
system, especially during the dry season, high iron concentrations are
related to high organic matter decomposition rates and associated low
pH values (Ministerio de Ambiente et al., 2004). The presence of
A. vulgaris may also be related to its acid tolerance, which prevents its
destruction during chemical treatment. Nevertheless, its presence is
an interesting nding that must be further examined in order to detect
pollution in the lagoonal system, and pH changes related to organic
matter decomposition in the mangroves.
7. Conclusions

Fig. 6. Distribution maps of percentages of other microfossils. a. Spore richness,

b. forams and c. Arcella (Testacea).

The pollen assemblage of the Cispat Bay lagoon system reects

the composition and structure of local mangrove forests distributed
within the three geomorphological zones, which, in turn, respond to
former and current delta geomorphological processes. Mangrove taxa
pollen not only identies the dominant species in a forest stand, but
also serves as an indicator of environmental conditions. The old-age
mangroves are associated with a high proportion of mangrove pollen.
An intermediate representation of mangrove pollen characterizes
estuarine conditions, and corresponds to mangrove colonization in
response to current bay inlling as well as anthropogenic disturbances. The lowest percentages of mangrove pollen are found in the
foothills zone. Although Rhizophora pollen proportions match its
dominance in each forest type, other mangrove species represent
some environmental conditions as well, and should be used as reliable

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L.E. Urrego et al. / Review of Palaeobotany and Palynology 156 (2009) 358375

environmental indicators. For example, a low proportion of Avicennia

characterizes saline back swamp conditions and can be used to
identify changes in the saltwater wedge; Laguncularia and Acrostichum are indicative of disturbance in mid-saline conditions; and Conocarpus points to the presence of supratidal conditions. Coastline
displacements and geomorphological changes can be reconstructed
by analyzing pollen in marine and coastal sediments. The prevalence
of water over wind transport is reected in the spatial distribution of
pollen and spores. While mangrove pollen is transported over short
distances, non-mangrove pollen and ferns spores are transported over
longer distances, and provide an indication of upstream humidity
conditions and forest composition. Secondary forest and grassland
fern spores and pollen grains are widely distributed, reecting the
regional vegetation.
Because the pollen spectra of mangroves and salt marshes
corresponds to the local vegetation and sea level changes, pollen
analyses of marine and coastal cores must be complemented with
analyses of offshore marine currents that are distant from our study
area in order to draw inferences about regional climate variations. The
use of complementary proxies is also recommended. This is the rst
report on pollen distribution in surface sediments in the Colombian
Caribbean. Reconstructions of the coastal palaeoenvironment in the
Caribbean based on palynological analyses of the taxa in this study
could be expected to provide valuable information about past changes
in coastline, coastal vegetation and environment.
Acknowledgments
The authors are grateful to Direccion de Investigaciones de la
Universidad Nacional de Colombia (DINAIN and DIME) and to the staff
at the university's Ecology Laboratory Cesar Prez Figueroa. We
would also like to thank Mauricio Ruiz for the collection of eld
samples, Jaime Escobar for the identication of the Arcella species,
Eliana Molina, Mara Berro and Jose Montoya for the elaboration of
the maps, and Ana Rosa Castao for her unconditional help in the
laboratory. Two anonymous reviewers made important suggestions to
improve the manuscript. Thanks too to Ann Elizabeth Harvey and WSR
for the revision of English grammar in this paper.
References
Alongi, D., 2008. Mangrove forests: resilience, protection from tsunamis, and responses
to global climate change. Estuarine, Coastal and Shelf Science 76, 113.
Behling, H., Cohen, M.C.L., Lara, R.J., 2001. Studies on mangrove ecosystem dynamics of
the Bragana Peninsula in north-eastern Par, Brasil. Palaeogeography, Palaeoclimatology, Palaeocology 167, 225242.
Beneld, S.L., Guzman, H.M., Mair, J.M., 2005. Temporal mangrove dynamics in relation
to coastal development in Pacic Panama. Journal of Environmental Management
76, 263276.
Bernal, G., Ruiz, M., Piedrahita, M.T., Restrepo, E., 2008. Foraminferos en los sedimentos
superciales del sistema lagunar de Cispat y la interaccin Ro Sin Mar Caribe
Colombiano. Boletn de Ciencias de la Tierra 23, 520.
Blasco, F., Saenger, P., Janodet, E., 1996. Mangroves as indicators of costal change. Catena
27, 167178.
Bush, M.B., 2002. On the interpretation of fossil Poaceae pollen in the lowland humid
neotropics. Palaeogeography Palaeoclimatology Palaeocology 177, 517.
Bush, M.B., Weng, C., 2007. Introducing a new (freeware) tool for palynology. Journal of
Biogeography 34, 377380.
Carvalho do Amaral, P.G., Ledru, M.P., Ricardi, F., Fonseca, P.C., 2006. Late Holocene
development of mangrove ecosystem in southern Brazil (Itanham, State of Sao
Paulo). Palaeogeography Palaeoclimatology Palaeoecology 241, 608620.
Castao, A.R., 2007. Procesos sucesionales de la vegetacin y su relacin con la dinmica
ambiental en el Complejo Lagunar Cispat, Caribe Colombiano. Tesis de Maestra en
Bosques y Conservacin Ambiental Universidad de Colombia, Sede Medelln: 67 pp.
Charman, D.J., 2001. Biostratigraphic and palaeoenvironmental applications of testate
amoebae. Quaternary Science Reviews 20, 17531764.
Charman, D.J., Roe, H.M., Gehrels, R., 2002. Modern distribution of saltmarsh testate
amoebae: regional variability of zonation and response to environmental variables.
Journal Quaternary Science 17, 387409.
Cohen, M.C.L., Behling, H., Lara, R.J., 2005. Amazonian mangrove dynamics during
the last millennium: the relative sea-level and the Little Ice Age. Review of
Palaeobotany and Palynology 136, 93108.

Colinvaux, P., De Oliveira, P.E., Moreno-Patio, J.E., 1999. Amazon pollen manual and
atlas. SmithsonianTropical Research Institute, Woods Hole, USA. 344 pp.
Dahdouh-Guebas, F., Verheyden, A., De Genst, W., Hettiarachchi, S., Koedam, N., 2000. Four
decade vegetation dynamics in Sri Lankan mangroves as detected from sequential
aerial photography; A case study in Galle. Bulletin of Marine Science 67, 741759.
Dahdouh-Guebas, F., Jayatissa, L.P., Di Nitto, D., Bosire, J.O., Lo Seen, D., Koedam, N., 2005.
How effective were mangroves as a defence against recent tsunami? Current
Biology 15, 443447.
Engelhart, S.E., Horton, B.P., Roberts, D.H., Bryant, C.L., Corbett, D.R., 2007. Mangrove
pollen of Indonesia and its suitability as sea level indicator. Marine Geology 242,
6581.
Elenga, H., Namur, C., de Vincens, A., Roux, M., Schwartz, D., 2000. Use of plots to dene
pollen vegetation relationships in densely forested ecosystems of tropical Africa.
Review of Palaeobotany and Palynology 112, 7996.
Ellison, J.C., 1996. Pollen evidence of Late Holocene mangrove development in Bermuda.
Global Ecology and Biogeography 5, 315326.
Ellison, A., 2002. Macroecology of mangroves: large-scale patterns and processes in
tropical coastal forests. Trees 16, 181194.
Erdtman, G., 1960. The acetolysis method in a revised description. Svensk Botanisk
Tidskift Lund 54, 561564.
Gil-Torres, W., Ulloa-Delgado, G., 2001. Caracterizacin, diagnstico de los manglares
del departamento de Crdoba. Corporacin Autnoma Regional de los Valles del
Sin y el San Jorge. Montera: 195 pp.
Golden software, INC., 2002. SURFER program version 8.02.
Gonzlez, C., Dupont, L.M., 2009. Tropical salt marsh succession as sea-level indicator
during Heinrich events. Quaternary Science Reviews 28, 939946.
Gonzlez, C., Urrego, L.E., Martnez, J.I., 2006. Late Quaternary vegetation and climate
change in the Panam basin: palynologycal evidence from marine cores ODP 677B
and TR 163-38. Palaeogeography Palaeoclimatology Palaeoecology 234, 6280.
Grindrod, J., Moss, P., Van der Kaars, S., 1999. Late Quaternary cycles of mangrove
development and decline on the north Australian continental shelf. Journal of
Quaternary Science 14, 465470.
Herrera, L.F., Urrego, L.E., 1996. Atlas de polen de plantas tiles y cultivadas de la
Amazona colombiana. Estudios la Amazona Colombiana. Volumen XI. TropenbosFundacin Erigaie, Colombia. 462 pp.
Hogarth, P.J., 2007. The Biology of Mangroves. Oxford University Press, New York. 228pp.
Hoffmann, C.C., 2002. Pollen distribution in sub-recent sedimentary environments of
the Orinoco Delta (Venezuela) an actuo-palaeobotanical study. Review of
Palaeobotany and Palynology 119, 191217.
Hooghiemstra, H., Agwu, C.O.C., 1986. Distribution of Palynomorphs in marine
sediments: A record for seasonal wind pattern over NW Africa and adjacent
Atlantic. Geologische Rundschau 75, 8195.
Hooghiemstra, H., Lzine, A.M., Leroy, S.A.G., Dupont, L., Marret, F., 2006. Late
Quaternary palynology in marine sediments: A synthesis of the understanding of
pollen distribution patterns in the NW African setting. Quaternary International
148, 2944.
Juggins, S., 2003. Software versin 1.3 C2. User guide. Software for ecological and
palaeoecological data analysis and visualisation. University of Newcastle, Newcastle
upon Tyne, UK: 69 pp.
Kathiresan, K., Bingham, B.L., 2001. Biology of mangroves and mangrove ecosystems.
Advances in Marine Biology 40, 81251.
Kumar, A., Patterson, R.T., 2000. Arcellaceans (thecamoebians): new tools for monitoring
long and short-term changes in lake bottom acidity. Environmental Geology 39,
689697.
Lzine, A.M., Hooghiemstra, H., 1990. Land-sea comparisons during last glacialinteglacial transition: pollen record from West Tropical Africa. Palaeogeography,
Palaeoclimatology, Palaeoecology 79, 313331.
Medina, E., Cuevas, E., Popp, M., Lugo, A.E., 1990. Soil salinity, sun exposure, and growth
of Acrostichum aureum, the mangrove fern. Botanical Gazette 151, 4149.
Mndez-Linares, A.P., Lpez-Portillo, J., Hernndez-Santana, J.R., Ortiz-Prez, M.A., 2007.
The mangrove communities in the Arroyo Seco deltaic fan, Jalisco, Mexico, and their
relation with geomorphic and physicalgeographic zonation. Catena 70, 127142.
Ministerio de Ambiente, Vivienda y Desarrollo Territorial, Corporacin Autnoma Regional
de los Valles del Sinu y San Jorge CVS, Fondo Financiero de Proyectos de Desarrollo
Fonade 2004. Diagnstico Ambiental de la Cuenca Hidrogrca del Ro Sin.
Molina, A., Molina, C., Giraldo, L., Parra, C., Chevillot, P., 1994. Dinmica marina y sus
efectos sobre la geomorfologa del golfo de Morrosquillo. Boletn Cientco del CIOH
15, 93113.
Moss, P.T., Kershaw, A.P., Grindrod, J., 2005. Pollen transport and deposition in riverine
and marine environments within the humid tropics of the northeastern Australia.
Review of Palaeobotany and Palynology 134, 5569.
Muller, J., 1959. Palynology of recent Orinoco Delta and shelf sediments. Micropalaeontology 5, 132.
Quiceno, M.M., 2008. Patrones de variabilidad climtica y ocenica en la zona costera
del ro Sin y su seal en registros naturales lacustres y coralinos. MSc. Tesis.
Maestra en Ingeniera, Recursos Hidrulicos, Escuela de Geociencias y Medio
Ambiente, Universidad Nacional de Colombia, Medelln. 160 pp.
Robertson, K., Chaparro, J., 1998. Evolucin histrica del ro Sin. Cuadernos de
Geografa 7, 7087.
Roubik, D., Moreno, J., 1991. Pollen and spores of Barro Colorado Island. Missouri
Botanical Garden. Monographs in Systematic Botany 36 268 pp.
Ruiz, M., 2006. Dinmica uvio-marina en los manglares de la baha Cispat, Caribe
Colombiano. MSc Thesis. Universidad Nacional de Colombia, Sede Medelln.
Medelln.
Ruiz, M., Bernal, G., Polana, J., 2008. Inuencia del ro Sin y Mar Caribe en el sistema
lagunar de Cispat, Colombia. Boletn de Ciencias Marinas y Costeras 37, 2949.

L.E. Urrego et al. / Review of Palaeobotany and Palynology 156 (2009) 358375
Snchez-Pez, H., lvarez, L.R., Pinto, N.F., Snchez, A.A., Pino, R.J., Garca, H.I., Acosta, P.
M., 1997. Diagnstico y zonicacin preliminar de los manglares del Caribe de
Colombia. Ministerio de Medio Ambiente, Santa Fe de Bogot D.C. 511 pp.
Snchez-Pez, H., Ulloa-Delgado, G., Tavera-Escobar, H., 2004. Manejo Integral de
manglares por comunidades locales del Caribe de Colombia. Ministerio de
Ambiente, Vivienda y Desarrollo Territorial. CONIF-OIMT, Bogot DC. 32 pp.
Scourse, J., Marret, F., Versteegh, G.J., Jansen, F.J.H., Schefuss, E., Van der Plicht, J., 2005.
High resolution last deglaciation record from the Congo fan reveals signicance of
mangrove pollen and biomarkers as indicators of shelf transgression. Quaternary
Research 64, 5769.
Serrano, B.E., 2004. The Sin river delta on the north western Caribbean coast of
Colombia: bay inlling associated with delta development. Journal of South
American Earth Sciences 16, 623631.
Stat point, INC., 19822006. STATGRAPHICS Centurion XV version 15.1.02.
Sun, X., Li, X., Beug, H.J., 1999. Pollen distribution in hemipelagic surface sediments of
the South of China and its relation to modern vegetation distribution. Marine
Geology 156, 211226.
Thom, B.G., 1984. Coastal landforms and geomorphic processes. In: Snedaker, S.C.,
Snedaker, J.C. (Eds.), The mangrove ecosystems: research methods. UNESCO,
Bungay, UK, pp. 317.
Torres-Parra, R.R., Gmez-Lpez, J.C., Afanador-Franco, F., 2006. Variacin del nivel
medio del mar en el Caribe Colombiano (Mean sea level variation at the Colombian
Caribbean). Boletn Cientco CIOH 24, 6472.

375

Tovilla, C., De la Lanza, G., 1999. Ecologa, produccin y aprovechamiento del mangle
Conocarpus erecta L., en barra de Tecoanapa Guerrero, Mxico. Biotropica 31,
121134.
Ulloa-Delgado, G., Snchez-Paez, P.H., Gil-Torres, G., Pino-Renjifo, R.J., Rodriguez-Cruz, H.Y.,
lvarez-Leon, R., 1998. Conservacin y uso sostenible de los manglares del Caribe
Colombiano. MINISTERIO DEL MEDIO AMBIENTE-ACOFORE-OIMT. Edisoma ediciones
especiales Ltda. 224 pp.
Van der Kaars, S., 2001. Pollen distribution in marine sediments from south-eastern
Indonesian waters. Palaeogeography Palaeoclimatology Palaeoecology 171,
341361.
Van Campo, E., Bengo, M.D., 2004. Mangrove palynology in recent marine sediments off
Cameroon. Marine Geology 208, 315330.
Weng, C., Hooghiesmtra, H., Duivenvoorden, J., 2006. Challenges in estimating past
plant diversity from fossil pollen data: statistical assessment, problems, and
possible solutions. Diversity and distributions 12, 310318.
Willard, D.A., Bernhardt, C.E., Weimer, L., Cooper, S.R., Gamez, D., Jensen, J., 2004. Atlas
of pollen and spores of the Florida Everglades. Palynology 28, 175227.
Woodroffe, S., Horton, B.P., Larcombe, P., Whittaker, J., 2005. Intertidal mangrove
foraminifera from central great barrier reef shelf, Australia: implications for sealevel reconstruction. Journal of Foraminiferal Research 35, 259270.
Woodroffe, C., 1992. Mangrove sediments and geomorphology. In: Robertson, A.I.,
Alongi, D.M. (Eds.), Coastal and estuarine studies. Tropical mangrove ecosystems.
American Geophysical Union, Washington, DC, pp. 769.