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Acta Oecologica 24 (2003) S117S123

www.elsevier.com/locate/actoec

Taxonomic survey of the microphytobenthic


communities of two Tagus estuary mudflats
Loureno Ribeiro a,*, Vanda Brotas a, Grard Mascarell b, Alain Cout b
a

Faculdade de Cincias, Instituto de Oceanografia, Universidade de Lisboa, Campo Grande, 1749-017 Lisbon, Portugal
b
Laboratoire de Cryptogamie, Musum National dHistoire Naturelle, 12, rue Buffon, 75005 Paris, France

Abstract
A taxonomic survey of the microphytobenthic communities was conducted in two intertidal mudflats of the Tagus estuary. These mudflats
are located in different littoral zones of the estuary and had distinct sediment characteristics and salinity range. Sampling was performed
monthly during low tide over a 14-month-period. Sediment cores were collected and brought to the laboratory, where the microalgae were
harvested using the lens-tissue technique under light stimulation. Samples were examined using both light and scanning electron microscopy.
The epipelic pennate diatoms dominated the microphytobenthic assemblages on both mudflats but cyanobacteria and euglenophytes were also
found. Of the 52 taxa identified, 47 were pennate diatoms, five of which seem to be previously unreported for Portugal. The species more
frequently found in the samples were Gyrosigma fasciola, Cylindrotheca cf. signata, Cylindrotheca closterium, Staurophora amphioxys and
Navicula gregaria.
2003 ditions scientifiques et mdicales Elsevier SAS. All rights reserved.
Keywords: Microphytobenthos; Species identification; Tagus estuary

1. Introduction
Microphytobenthic communities are the main primary
producers in intertidal flats of many estuaries. In the case of
the Tagus estuary, they have an estimated primary production
of 11 000 tonnes carbon per year (Brotas and Catarino,
1995), which is about two-fold of the annual primary production of the phytoplankton indicated by (Cabeadas et al.,
2000). The extensive biofilms that develop on the surface of
intertidal sediments are also an active element of the biogeochemistry cycles of sediment-air and sediment-water column interfaces (Cabrita and Brotas, 2000; Dong et al., 2000).
While the taxonomical composition of the phytoplankton
communities of the Tagus estuary has been assessed several
times in the last 30 years ((Moita and Vilarinho, 1998), and
references herein), a thorough taxonomic characterisation of
the benthic microalgae of the Tagus and other Portuguese
estuaries is yet to be achieved. Nevertheless, the overall
structure of the microphytobenthic communities found in the
Tagus intertidal flats and salt marshes, as well as their seasonal and spatial variation, was already established (Brotas
and Plante-Cuny, 1998; Brotas et al., 1995). The former
* Corresponding author.
E-mail address: lourosr@fc.ul.pt (L. Ribeiro).
2003 ditions scientifiques et mdicales Elsevier SAS. All rights reserved.
DOI: 1 0 . 1 0 1 6 / S 1 1 4 6 - 6 0 9 X ( 0 3 ) 0 0 0 1 2 - 2

work, where these communities were studied using HPLC


pigment analysis, concluded that diatoms were dominant but
euglenoids and cyanobacteria were also frequently present.
Brotas and Catarino (Brotas and Catarino, 1995) refer a set of
the 10 most common epipelic species found in the intertidal
mudflats of the Tagus estuary.
The benthic estuarine microalgae have always posed
problems to algal taxonomists (Riznyk, 1973). Sampling, as
well as the separation of the microphytobenthos from the
sediment, and cleansing procedures are hampered by several
methodological difficulties. An additional obstacle comes
from the fact that the taxonomical literature regarding this
brackish water group is still quite scarce and scattered, when
compared to the fresh water and planktonic studies.
The objective of this work was to contribute to the knowledge on the taxonomical composition of the microphytobenthic assemblages of the Tagus intertidal estuarine areas,
giving special attention to the motile epipelic fraction.
2. Materials and methods
The Tagus estuary (3844'N, 0908'W) is the largest estuary in Western Europe, covering an area of approximately
320 km2. The estuary has a vast inner bay with extensive
intertidal areas. These areas are essentially constituted of

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L. Ribeiro et al. / Acta Oecologica 24 (2003) S117S123

Fig. 1. Map of the Tagus estuary showing the sampled stations (Pancas and
Rosrio). Hatched areas, saltmarsh. Thin line, lower limit of intertidal zone.

mudflats, which have an estimated total area of 100 km2


(Brotas and Catarino, 1995). The Tagus estuary is mesotidal
with a mean tidal rage of 2.4 m, varying from about 1 m at
neap tides to about 4 m at spring tides.
Sampling was carried out at two stations, Pancas (P) and
Rosrio (R), situated on two mudflats in the southeastern
margin of the estuary (Fig. 1). Pancas is located in the inner
estuary on the upper eullitoral zone, while Rosrio is located
in the outer estuary on the lower eullitoral zone. Various
physicochemical parameters were analysed during sampling
and were previously published (Cabrita and Brotas, 2000).
Pancas had an annual salinity range of 3-33 and had
muddy sediment (97.5% of silt and clay, in average), whereas
Rosrios salinity range was 16-37 and its sediment, although muddy, was much more sandier (59.9% of silt and
clay, in average) and showed a considerably variation during
the sampling period.
Both stations were sampled monthly between March 1997
and April 1998. A second site was sampled at each station,
every 3 months, to account for local variability. A total of 34
samples were collected during the sampling period.
The method chosen for harvesting the microphytobenthic
community was the lens-tissue technique (Eaton and Moss,
1966). This selective method collects the motile epipelic
fraction of the microphytobenthos, which is known to migrate vertically in response to light stimulus and tidal
rhythms. Sediment samples were taken using cylindrical
Plexiglas corers (13 cm long 8 cm i.d.) during low spring
tides and brought to the laboratory for further processing.
The sediment corers were then placed in a box filled with
estuarine water and several 2 cm2 pieces of lens-tissue were

laid on the sediments surface and left undisturbed for 24 h.


During the exposure period, the corers were artificially illuminated for 2 h, after which two lens-tissue pieces were
picked and placed in a 10 ml beaker containing a mixture of
filtered estuarine water and glutaraldehyde (final concentration 2.5% glutaraldehyde).
For each sample several slides were screened under a M20
WILD optic microscope, equipped with a Camera Lucida.
Drawings of every taxon encountered were made for subsequent identification. The slides were made directly from the
samples, without any kind of cleansing treatment, in order to
preserve other algal groups beside diatoms. Specific samples
that covered the majority of the taxa observed during the light
microscopy sessions were selected for electron microscopy.
Aliquots of these samples were placed in a transparent inkwell, treated with hydrogen peroxide 33% and rinsed with
bi-distilled water. The liquid containing the cleaned frustules
was then siphoned by a 10 ml syringe and filtered using a
Millipore Membrane Filter with an average pore diameter
of 1.2 m. The filters were dehydrated in pure ethanol and
critical point dried. Each dried filter was placed on an aluminium pin stub and gold-palladium coated. An alternative
method was also used and consisted in isolating the cleaned
frustules with a capillary pipette, under a compound dissecting microscope, and mounting them directly on the surface of
the pin stub. The diatom micrographs (ILFORD FP4 LM 125
ASA/120 film) were taken on a JEOL 840 Scanning Electron
Microscope using an acceleration voltage of 8 kV.
The taxa were identified following the descriptions by
Bourrely (Bourrely, 1981), Cox (Cox, 1996), Germain (Germain, 1980), Krammer and Lange-Bertalot (Krammer and
Lange-Bertalot, 1986; Krammer and Lange-Bertalot, 1988),
Patrick and Reimer (Patrick and Reimer, 1966; Patrick and
Reimer, 1975), Peragallo and Peragallo (Peragallo, 1897),
Ricard (Ricard, 1987), Round et al. (Round et al., 1990) and
Witkowski et al. (Witkowski et al., 2000).
3. Results
A total of 48 diatom taxa were identified to the genus or
species level (Table 1). With the exception of Cyclotella
meneghiniana, they were all pennate monoraphid or biraphid
diatoms and belonged to 24 different genera. Regarding other
algal groups, two unidentified species of Euglena, as well as
one Oscillatoria sp., were found in both stations. A species of
the cyanobacteria Merismopedia occurred only in Rosrio.
Out of 43 taxa found in Pancas, 29 occurred in Rosrio
also, which had a slightly lower number of species (38).
Although the majority of the taxa encountered were common
to both stations, Pancas had 14 specific taxa and Rosrio
nine.
The additional sampling made every 3 months in Pancas
and Rosrio did not show any apparent difference in terms of
taxa composition within each station. Although these
samples were collected 400 and 250 m apart from the sites
sampled monthly, in Pancas and Rosrio, respectively, only

L. Ribeiro et al. / Acta Oecologica 24 (2003) S117S123

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Table 1
List of the taxa found on two mudflats of the Tagus estuary. Pancas (P) and
Rosrio (R)

Table 2
Taxa found in more than 2/3 (66%) of the samples of each station and
considering both stations together

Taxa
Bacillariophyta
Achnanthes brevipes Agardh
Amphora coffeaeformis (Agardh) Ktzing
Amphora spp.
Bacillaria paxillifer (O.F. Mller) Hendey
Berkeleya sp.
Caloneis westii W. Smith
Cocconeis sp.
Cosmioneis pusilla (W. Smith) Mann and Stickle
Cyclotella meneghiniana Ktzing
Cylindrotheca closterium Reinmann and Lewin
C. cf. signata Reinmann and Lewin
Cymatopleura solea (Brbisson) W. Smith
Diploneis didyma (Ehrenberg) Cleve
Entomoneis alata (Ehrenberg) Ehrenberg
E. paludosa (W. Smith) Reimer
Epithemia sp.
Frustulia interposita (Lewis) De Toni
Gyrosigma cf. acuminatum (Ktzing) Rabenhorst var. gallica
Grunow
G. (Ktzing) Cleve
G. balticum (Ehrenberg) Rabenhorst
G. distortum (W. Smith) Griffith and Henfrey
G. fasciola (Ehrenberg) Cleve
G. limosum Sterrenburg and Underwood
Gyrosigma sp.
Navicula cryptocephala Ktzing
N. gregaria Donkin
N. phyllepta Ktzing
N. cf. digito-radiata (Gregory) Ralfs
Navicula spp.
Nitzschia acicularis (Ktzing) W. Smith
N. alexandrina (Cholnoky) Lange-Bertalot and Simonsen
N. navicularis (Brbisson) Grunow
N. reversa W. Smith
N. sigma (Ktzing) W. Smith
N. tubicula Grunow
Nitzschia sp.
Petrodyction gemma (Ehrenberg) D.G. Mann
Plagiotropis sp. 1
Plagiotropis sp. 2
Pleurosigma angulatum (Quekett) W. Smith
P. angulatum (Quekett) W. Smith var. aestuarii (Brbisson)
Staurophora amphioxys (Gregory) D.G. Mann
Surirella brebissonii Krammer and Lange-Bertalot
Surirella cf. brightwellii W. Smith
Tryblionella apiculata Gregory
T. gracilis W. Smith
T. hungarica (Grunow) D.G. Mann
Vanheurckia lewisiana (Greville) Brbisson

Pancas
T. gracilis
C. cf. signata
G. limosum
N. gregaria
S. amphioxys
G. attenuatum
G. fasciola
N. sigma
G. distortum
N. naviculares
G. cf. acuminatum
S. cf. brightwellii

Cyanophyta
Oscillatoria spp.
Merismopedia sp.
Euglenophyta
Euglena sp. 1
Euglena sp. 2

Station

P
P

R
R
R
R
R

P
P
P
P
P
P
P
P
P
P

R
R
R
R
R
R
R
R
R
R

P
R
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P

R
R
R
R
R
R

R
R
R
R
R
R
R
R
R
R
R
R

R
R

P
P

R
R

Rosrio
C. closterium
G. fasciola
C. cf. signata
S. amphioxys
N. gregaria
D. dydima
G. limosum
S. cf. brightwellii
Plagiotropis sp2

Both stations
C. cf. signata
G. fasciola
S. amphioxys
N. gregaria
C. closterium
G. limosum
S. cf. brightwellii
D. dydima
N. sigma

two to three taxa were not common to both sets of samples


from the same station. For this reason it was decided to
consider the samples of each station as a whole in order to
attain a maximal number of taxa per station.
The taxa most frequently found in the studied samples are
shown in Table 2, where a set of 15 different species is
presented. This table displays encountered species from decreasing order of occurrence (ratio of number of samples
where species occurred to total number of samples observed), from 96 to 66%.
A close observation of Tables 1 and 2 indicates that several taxa were frequently found in both stations, e.g. Cylindrotheca signata, Gyrosigma fasciola (Fig. 2), Gyrosigma
limosum (Fig. 4), Navicula gregaria (Fig. 9) and Staurophora amphioxys (Fig. 8). Other taxa, Cylindrotheca closterium (Fig. 10), Diploneis dydima and Plagiotropis sp. 2,
were more frequently found in Rosrio. Some of the most
frequently found species in Pancas occurred exclusively in
this station, namely Tryblionella gracilis (Fig. 15), Gyrosigma attenuatum (Fig. 6), Gyrosigma distortum (Fig. 3)
and Nitzschia navicularis.
Many species listed in Table 1 have never been reported
for the Tagus estuary, moreover, five species may be considered as new records for Portugal: Frustulia interposita
(Fig. 7), Nitzschia alexandrina (Fig. 12), Nitzschia tubicula
(Fig. 13), S. amphioxys, Vanheurckia lewisiana. To our
knowledge, both F. interposita and V. lewisiana are also first
reports for Europe.
Being a qualitative study, it is difficult to infer the possible
seasonal fluctuations in the assemblages without quantitative
data (cell counts). The optic microscopy observations suggested the existence of an increase in cell number during
spring-summer, followed by a decrease in the autumn-winter
period. However, in terms of species occurrences, most of the
reported taxa did not show any kind of marked seasonality.
All taxa listed in Table 2 were present throughout the year,
for they were reported for at least nine of the 14 months
surveyed. The majority of the other taxa reported, such as
Gyrosigma cf. acuminatum (Fig. 5) Nitzschia sigma
(Fig. 11), Tryblionella apiculata (Fig. 15), Entomoneis palu-

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Figs. 29. Diatom SEM micrograph. Fig. 2. G. fasciola, Fig. 3. G. distortum, Fig. 4. G. limosum, Fig. 5. Gyrosigmasp. [cf. acuminatum var. gallica],
Fig. 6. G. attenuatum, Fig. 7. Frustulia interposita, Fig. 8. Staurophora amphioxis, Fig. 9. Navicula gregaria.

dosa (Fig. 16) and Surirella cf. brightwellii (Fig. 17), although not as frequent, did not show any apparent preference
for a given season during the sampling period.
4. Discussion
The microphytobenthic taxa found on both mudflats were
essentially epipelic pennate diatoms, as previously reported

(Brotas and Catarino, 1995; Brotas and Plante-Cuny, 1998)


for several similar sites in the Tagus estuary. The taxonomic
composition of the microphytobenthic assemblages of the
two studied intertidal mudflats confirms the cosmopolitan
nature of the majority of the estuarine microalgae, in particular epibenthic diatoms. Most of the identified diatoms in this
study are also listed in the revision papers of Round (Round,
1971), McIntire and Moore (McIntire and Moore, 1977) and

L. Ribeiro et al. / Acta Oecologica 24 (2003) S117S123

S121

Figs. 1017. Diatom SEM micrograph. Fig. 10. Cylindrotheca closterium, Fig. 11. Nitzschia sigma, Fig. 12. N. Alexandrina, Fig. 13. N. tubicula,
Fig. 14. Tryblionella apiculata, Fig. 15. T. gracilis, Fig. 16. Entomoneis paludosa, Fig. 17. Surirella sp. [cf. brightwellii].

Admiraal (Admiraal, 1984) for world-wide benthic estuarine


and littoral diatoms. Other taxa have also been reported in
several floristic and ecological studies from French (Riaux
and Germain, 1980; Rinc and Robert, 1983), Italian (Tolomio et al., 1999), British (Round, 1960; Zong and Horton,

1998) and North American (Amspoker and McIntire, 1978;


Riznyk, 1973) estuarine tidal flats and salt marshes.
Although motile epipelic species often dominate muddy
estuarine tidal flats (Admiraal, 1984) they are not exclusive
of these substrata. In fact, several diatoms reported in this

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work, such as C. meneghiniana, C. closterium or Entomoneis


alata, have been reported in publications concerning the
Tagus estuary phytoplankton (Sousa e Silva et al., 1969).
Admiraal (Admiraal, 1984) defined as plankton-benthic diatoms the species that are frequently found in estuarine plankton as well as on the sediment. This author considered them
an essential feature of estuaries and coastal ecosystems,
allowing the intermingling of benthic and pelagic food
chains.
Although Pancas and Rosrio had a similar number of
species and shared more than 2/3 of the taxa, the differences
in the taxonomic structure of the assemblages of the two
stations should not be discarded. As much as 33% of the taxa
reported in Pancas and 24% in Rosrio were exclusive to
each station. In Pancas, some of the most frequently found
species (e.g. T. gracilis, G. attenuatum) only appeared in this
station. Pancas and Rosrios stations were clearly distinct in
a number of environmental factors: Pancas had lower salinity, lower immersion periods, finer grain size and lower
nutrient content in sediment interstitial water (Cabrita and
Brotas, 2000). These results support the idea that there is a
general overlapping pattern in the species distribution along
the estuary and that some species may have a specific set of
environmental conditions, as has been suggested by several
authors (e.g. (Moore and McIntire, 1977; Underwood et al.,
1998)).
The seasonal succession of the microphytobenthic diatom
assemblages has been documented in several reports, usually
from Northern Europe (Round, 1960; Underwood, 1994).
However, there is no systematic account on the seasonal
occurrence of individual species (Admiraal, 1984). The continuous occurrence of the most frequent taxa during this
study, as well as the apparent lack of periodicity of the other
reported species in both mudflats may point otherwise. One
striking example is C. closterium that occurred abundantly in
every month surveyed, during our study, and has been often
referred as a summer species in British estuaries (Hopkins,
1964; Underwood, 1994). One possible explanation to this
fact is that the studies that reported a seasonal effect in the
overall structure of the diatom communities were made at
higher latitudes, where the annual variation of light and
temperature may have a more decisive effect on the seasonal
succession of benthic diatoms than under a mild climate,
such as in Tagus estuarys.
Studies of the microphytobenthic taxonomy in the Tagus
estuary are fundamental for the understanding the overall
ecology of these communities. Consistent quantitative and
qualitative are still needed to disclose the seasonal and spatial
changes of the epipelic assemblages, as well as their distribution along salinity or nutrient gradients in the Tagus and
other Portuguese estuaries.
Acknowledgements
The authors gratefully acknowledge Professor Yves Rinc
(Universit de Nantes) for the confirmation of the taxonomi-

cal identifications and Michle Dumont (MNHN, Paris) for


technical support, Bruno Jesus for the digitalisation of the
micrographs and Paulo Cartaxana for the text revision. This
work was supported by the Europe Union ELOISE program
under the framework of NICE project, Contract MAS3CT96-0048 and partly by Project Sat-Tagis no.
PDCTM/MAR/15256/99.

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