occurrence and distribution of macroalgae (rhodophyta

OCCURRENCE AND DISTRIBUTION OF MACROALGAE (RHODOPHYTA) ASSOCIATED WITH
MANGROVES ON THE AJURUTEUA PENINSULA, BRAGANÇA, PARÁ, BRAZIL.
OCORRÊNCIA E DISTRIBUIÇÃO DE MACROALGAS (RHODOPHYTA) ASSOCIADAS AOS
MANGUEZAIS NA PENÍNSULA DE AJURUTEUA, BRAGANÇA, PARÁ, BRASIL.
Marcus Emanuel Barroncas Fernandes1;
Eliane de Fátima Silva Alves1.
1
Universidade Federal do Pará. Instituto de Estudos Costeiros - IECOS. Laboratório de Ecologia de Manguezal. e.mail: [email protected]
KEY WORDS:
ABSTRACT
Avicennia germinans;
The present study evaluates the natural occurrence and distribution of macroalgae species
of the division Rhodophyta which colonize the pneumatophores of Avicennia germinans
(L.) Stearn in the mangroves on the Ajuruteua Peninsula, Bragança, Pará, Brazil. Field
measurements showed that mean length of the pneumatophores reached 12 cm, where
five species of macroalgae were recorded: Bostrychia radicans (Montagne) Montagne, B.
moritziana (Sonder ex Kützing) J. Agardh, B. calliptera (Montagne) Montagne, Catenella
caespitosa (Whitering) L. M. Irvine, and Caloglossa leprieurii (Montagne) J. Agardh.
Monthly evaluation revealed B. moritziana, B. radicans, and C. leprieurii occurrence
on the basal and median portion of the pneumatophore during the dry period, while B.
calliptera and C. caespitosa were distributed all over the pneumatophore. B. calliptera
and C. caespitosa were only recorded during the wet period. A number of species and
pH presented significant differences (ANOSIM, R=0.069; p<0,05). Considering the
reproductive cycle, C. caespitosa was only found during the sporophytic phase, whereas
B. calliptera and B. radicans presented the tetrasporophytic phase.
Mangrove forests;
Intertidal zone;
Brazilian Amazon coast.
PALAVRAS-CHAVE:
RESUMO
Avicennia germinans;
O presente estudo avalia a ocorrência natural e distribuição das espécies de macroalgas
da divisão Rhodophyta que colonizam os pneumatóforos de Avicennia germinans (L.)
Stearn nos manguezais da península de Ajuruteua, Bragança, Pará, Brasil. Medidas de
campo mostraram que o comprimento médio dos pneumatóforos é de 12 cm, onde cinco
espécies de macroalgas foram registradas: Bostrychia radicans (Montagne) Montagne, B.
moritziana (Sonder ex Kützing) J. Agardh, B. calliptera (Montagne) Montagne, Catenella
caespitosa (Whitering) L. M. Irvine e Caloglossa leprieurii (Montagne) J. Agardh. Avaliações
mensais revelaram a ocorrência de B. moritziana, B. radicans e C. leprieurii na porção
basal e média do pneumatóforo durante o período seco, enquanto B. calliptera e C.
caespitosa estavam distribuídas por todo o pneumatóforo. B. calliptera e C. caespitosa
foram registradas somente durante o período chuvoso. O número de espécies e o pH
apresentaram diferença significativa (ANOSIM, R=0,069; p<0,05). Considerando o ciclo
reprodutivo, C. caespitosa foi encontrada somente durante a fase esporofítica, ao passo
que B. calliptera e B. radicans apresentaram a fase tetraesporofítica.
Florestas de mangue;
Zona entremarés;
Costa amazônica brasileira.
35
Fernandes, M. E. B.; Alves, E. F. S. Macroalgae associated with mangroves in Pará, Brazil.
INTRODUCTION
and able to occupy areas with high desiccation
(ESTON et al., 1992). This desiccation tolerance has
been demonstrated in several studies on the vertical
distribution of macroalgae (YOKOYA et al., 1999;
BOUZON; OURIQUES, 1999).
Mangrove trees form a suitable environment for growing
typical algal flora associated with the mangrove system
(Dawes, 1996). Hutchings; Saenger (1987) describe this
flora as represented by microalgae, cyanobacteria, and
diatoms that are mostly attached to the sediment in the
forest floor, and by macroalgae which adhere to trunks,
Considering the lack of information on species
composition of macroalgae in the Brazilian Amazon
coastline, the present study aims both: i) to contribute
to the occurrence of this group on the coastline of the
state of Pará and ii) to evaluate the influence of different
abiotic variables on vertical and horizontal distribution
of macroalgae assemblage associated to mangrove
pneumatophores.
pneumatophores, and rhizophores of mangrove tree
species.
In Brazil, many authors have exhaustively investigated
the typical algal flora in association with the mangrove
system (OLIVEIRA, 1984; HADLICH, 1984; HADLICH;
BOUZON, 1985; MIRANDA et al., 1988; PINHEIROJOVENTINO; LIMA-VERDE, 1988; CORDEIROMARINO et al., 1992; ESTON et al., 1991; ESTON
et al., 1992; BOUZON; OURIQUES, 1999; CUNHA
et al., 1999; CUNHA; COSTA, 2002; CUNHA;
DUARTE, 2002). Nevertheless, most of these studies
were carried out in the southern, southeastern, and
northeastern region of the country. Only a few studies
were concentrated northward on the Brazilian Amazon
coastline, where mangrove forests are well developed;
such an association remains to be better understood
(PAULA et al., 1989 - in the state of Amapá; CUTRIM
et al., 2004; CUTRIM; AZEVEDO, 2005 - in the state of
Maranhão; and FERNANDES et al., 2005 - in the state
of Pará).
MATERIAL AND METHODS
Study Area
According to Cohen et al. (1999), the study site is
located 200 km southeast of the mouth of the Amazon
estuary in the municipality of Bragança, Pará, Brazil,
between the Caeté River and the Maiaú Bay (Figure 1).
Fieldwork was carried out in the mangrove forests at
the Furo do Meio (46°50’46°30’W and 0°45’1°07’S),
a typical mangrove stand on the Ajuruteua Peninsula,
Bragança, Pará. It is characterized by mangrove forests
with trees up to 20 m tall, with Rhizophora mangle
L. and Avicennia germinans (L.) Stearn. being the
dominant species. This mangrove area covers 110 km2,
with spring and ebb tides reaching circa 3 and 4 m,
respectively.
According to Dawes (1996), macroalgae associated to
intertidal environment are exposed to the fluctuation of
different abiotic variables (e.g. salinity, pH, desiccation,
etc). Such environmental fluctuations can influence the
patterns of horizontal and vertical distribution of these
species, changing assemblage structure and dynamics
of macroalgae biomass production along the estuarine
environment. B. radicans for example, are very tolerant
to variations in salinity (BRODERICK; DAWES, 1998)
The equatorial climate of the region is hot and humid.
The annual mean rainfall reaches 3000 mm and relative
air humidity ranges between 80 and 91%, with a rainy
season from January to June and a dry season from July
to December (MARTORANO et al., 1993).
36
UAKARI, v. 7, n. 2 , p. 35 - 42, 2011
At the laboratory, pneumatophores were sized
and on average they measured 12 cm. The
pneumatophores of median size were divided
into three portions: basal (0-4 cm), median
(4-8 cm), and apical (8-12 cm). Tweezers were
used to collect the macroalgae incrusted on
the pneumatophores, which were preserved in
formalin 4% (BOUZON; OURIQUES, 1999)
for further identification. Macroalgae species
were identified according to descriptions of
Cordeiro-Marino (1978), Blair (1983), and King;
Puttock (1989). In addition, water attributes
were measured in situ. After pneumatophores
were collected, water transparency, salinity,
dissolved oxygen, and pH were measured in
order to record the variation of these variables
throughout the year.
Raw data were not normally distributed by
Lilliefors test. Thus, Kolmogorov-Smirnov
non-parametric test was used to analyze the
horizontal distribution of macroalgae during
the annual cycle (AYRES et al., 2007). Relative
Frequency considering the vertical distribution
of macroalgae on the three portions of the
pneumatophores during dry and wet periods
were calculated. The multivariate analysis
ANOSIM (Analysis of Similarity) was used
Figure 1 - Map showing the study site (Furo do Meio), Ajuruteua Peninsula,
to test whether abiotic variables [dry and wet
Bragança, Pará, Brazil.
period, salinity, water transparency (cm),
dissolved oxygen (mg/l), and pH] were related to
presence/absence of algae species during the annual
cycle (CLARKE; GORLEY, 2006).
Data Collection
A transect of 60 m was opened parallel to a creek to
sample macroalgae=assemblage. This transect was
divided into three even points, of which one was
sorted for data collection. From this sorted point,
another transect of 30 m was opened, perpendicular
to the creek. Along this transect a sample of five
pneumatophores were collected closest to the transect
at each 2 m interval, totaling 15 replicates per month.
Fieldwork was carried out bimonthly during the ebb
tide from August/2005 to June/2006.
RESULTS AND DISCUSSION
One-hundred-ninety pneumatophores were collected
and identified five species of the division Rhodophyta,
represented by: Bostrychia radicans (Montagne)
Montagne, B. moritziana (Sonder ex Kützing) J.
Agardh, B. calliptera (Montagne) Montagne, Catenella
caespitosa (Whitering) L. M. Irvine, and Caloglossa
37
Fernandes, M. E. B.; Alves, E. F. S. Macroalgae associated with mangroves in Pará, Brazil.
to 25 m high, forming a closed canopy avoiding light
exposure, which, in turn, may promote homogeneous
distribution of red algae.
leprieurii (Montagne) J. Agardh. In general, the species
composition of macroalgae found in the present study
associated to pneumatophores of A. germinans is
similar to typical algal flora in the mangrove forest from
other regions of Brazil: south (CORDEIRO-MARINO,
1978; HADLICH; BOUZON, 1985; BOUZON;
OURIQUES, 1999; CUNHA; DUARTE, 2002) and
southeast (ESTON et al., 1991; YOKOYA et al., 1999).
Although many studies have been undertaken in the
northeast (MIRANDA et al., 1988; CUTRIM; AZEVEDO,
2005), there are no available records confirming the
occurrence of B. moritziana in the state of Maranhão,
eastern Amazonia. In the northern region, the species
of macroalgae found on the Ajuruteua peninsula
in Pará (FERNANDES et al., 2005) are the same
species described in the present study. However, the
macroalgae recorded on the peninsula share only two
species (B. radicans and C. caespitosa) and disagree with
five others, which include B. moritziana, B. calliptera,
and C. leprieurii recorded at the Furo do Meio and B.
pilulifera Montagne and Caloglossa ogasawaraensis
Okamura on the Maracá Island, in the state of Amapá,
far northern Brazil (PAULA et al., 1989).
On the other hand, the vertical distribution
(pneumatophores) showed a monthly trend. In the
months of the dry period, for example, C. leprieurii, B.
radicans and B. moritziana were registered on the basal
and median portions of the pneumatophores, while
B. calliptera and C. caespitosa occurred all over the
pneumatophores. In the wet months, only B. calliptera
and C. caespitosa were recorded on the basal and
median portions of the pneumatophores. There was no
record of macroalgae on the apical portion during the
rainy season (Figure 2).
12 cm
12 cm
8 cm
8 cm
B. calliptera
C. caespitosa
4 cm
B. radicans
B. moritziana
C. leprieurii
Dry Period
along transects, and there was no significant difference
(Kolmogorov-Smirnov, p>0.05) in the number of
species along the perpendicular transect at the Furo
do Meio. This result may reflec the response of these
species to different biotic and abiotic factors such as
the availability of shadowed places in the study area.
In fact, red algae (ex. Bostrichia) can present periodic
photosynthetic responses from a salt marsh and
mangrove vegetation (BRODERICK; DAWES, 1988).
According to Karsten et al. (1994a), these species are
often protected from solar radiation by the shade of
the canopy, in the case of mangrove forests. In fact, at
the Furo do Meio emergent mangrove trees reach up
B. calliptera
C. caespitosa
0 cm
0 cm
The macroalgae species found attached to the mangrove
roots presented homogeneous horizontal distribution
4 cm
PNEUMATOPHORES
Wet Period
Figure 2 - Patterns of vertical distribution of macroalgae on the
pneumatophores of Avicennia germinans during the dry and
wet period at the study site (Furo do Meio), Ajuruteua Peninsula,
Bragança-Pará, Brazil.
During the dry period B. radicans and C. leprieurii
dominated the basal portion of pneumatophores with 80
and 83% respectively. B. moritziana and C. caespitosa
dominated the median portion, while B. calliptera
and C. caespitosa dominated the apical portion. The
species B. calliptera and C. caespitosa were dominant
in the first two basal portions during the rainy season
(Table 1).
38
UAKARI, v. 7, n. 2 , p. 35 - 42, 2011
Table 2 - Collection of abiotic data in situ during both dry and
wet period at the study site (Furo do Meio), Ajuruteua Peninsula,
Bragança-Pará, Brazil.
Table 1 - Relative Frequency (%) of the vertical distribution of
macroalgae on the three portions of the pneumatophores of
Avicennia germinans during the dry and wet period at the study
site (Furo do Meio), Ajuruteua Peninsula, Bragança, Pará, Brazil.
0-4 cm
Species
Dry
Wet
4-8 cm
Dry
Wet
Period
8-12 cm
Dry
Wet
Bostrychia radicans
80
0
20
0
0
0
Bostrychia calliptera
43
56
33
44
24
0
Bostrychia moritziana
5
0
50
0
0
0
Caloglossa leprieurii
83
0
17
0
0
0
Catenella caespitosa
34
67
41
33
24
0
Dry
Wet
Date
Transparency
Dissolved Oxygen
Salinity
(mm/dd/yyyy)
(cm)
(mg/l)
pH
08/24/2005
12
30
5.2
7.1
10/27/2005
18
37
9.4
7.5
12/19/2005
12
38
6.7
7.2
02/28/2006
19
23
2.6
6.6
04/27/2006
20
7
1.8
6.6
06/28/2006
15
24
1.5
7.1
It is noteworthy that abiotic factors seem to have great
relevance to horizontal and vertical distribution of the
algal flora associated with mangroves. In the present
study, for example, only pH was statistically significant
in relation to presence/absence of macroalgae species.
This suggests that water alkalinity in the main channel of
the study site may play an important role in determining
such distribution during the annual cycle. According to
Berrêdo (2006), on a study carried out in Marapanim
estuary on the coast of Pará, the pH indicates alkaline
conditions during the dry period (e.g. pH=7.3 to 7.9),
while during the rainy period, the waters tend to reach
higher rates of acidity (e.g. pH=4.4 to 6.5) during the
flood tides, due to the contact with organic compounds
from both sediments and litterfall during the ebb tides.
However, other abiotic factors can also be relevant to
this algal flora, such as: luminosity (CUNHA; DUARTE,
2002); desiccation (CUTRIM; AZEVEDO, 2005), flood
frequency (CUNHA; COSTA, 2002), and salinity
(KARSTEN et al., 1994b; FERNANDES et al., 2005).
According to Oliveira (1984), algae associated with
mangrove forests present vertical distribution resulting
from tolerances and adaptation to variations of many
biotic and abiotic parameters. The trend of vertical
distribution, described in the present study, is different
from the one described in the eastern Brazilian Amazon
coastline by Cutrim; Azevedo (2005). B. radicans
and C. leprieurii, in the present study, for example,
were recorded only on the basal and median portion
of the pneumatophores, while these species are found
in the eastern Amazon attached all over the root. A
great variation on the vertical distribution seems to
be common for red macroalgae. On the other hand,
green macroalgae seem to be found attached mainly to
the upper portions of the pneumatophores, indicating
that a gradient of microclimate (ex. humidity, drought)
may affect the vertical distribution of these species
(CUTRIM; AZEVEDO, 2005). In addition, we observed
that B. radicans occurred only in the dry period and
on the basal portion, in contrast to the study of Mann;
Steinke (1988), in South Africa, where macroalgae
are distributed on the apical portion, suggesting more
resistance to drought, solar radiation, and high salinity.
According to Karsten et al. (1999), salinity can be
considered a limiting factor for the reproduction of
this species. So, considering the reproductive phases
of the macroalgae species at the Furo do Meio, it was
recorded that B. calliptera was the only species to
present reproductive structures during the entire annual
cycle, while B. radicans and C. caespitosa presented
them only in the dry and wet period, respectively. The
species B. moritziana and C. leprieurii did not present
reproductive structures.
The comparison between abiotic factors showed
that pH presented a significant difference (ANOSIM,
R=0.069; p<0.05), when related to presence/absence
of algae during the entire annual cycle (Table 2).
39
Fernandes, M. E. B.; Alves, E. F. S. Macroalgae associated with mangroves in Pará, Brazil.
Regarding transparency, it did not present a significant
correlation to macroalgae distribution at the Furo do
Meio. The high sedimentation in the channel during
the wet period was reflected in the transparency rates.
In fact, high sedimentation seemed to influence the
absence of B. radicans, C. leprieurii, and B. moritziana
during this period, since pneumatophores were
totally covered by sediment. On the other hand, the
two former species were already recorded adhered to
pneumatophores during the wet period, so the presence
of these two species seems to be associated to their
reproductive cycles rather than sedimentation process.
In sum, given the great variations in the vertical and
monthly distributional trends of macroalgae associated
with mangroves, it is important to emphasize that local
biotic and abiotic characteristic can generate all the
trends described so far.
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ACKNOWLEDGEMENTS
We are grateful to Dr. M.V.J. Cutrim (Universidade
Federal do Maranhão, São Luís, Maranhão, Brazil) for
confirming macroalgae identification from herbarium
material. Financial support for fieldwork was provided
by the Laboratório de Ecologia de Manguezal,
UFPA,Campus de Bragança, Pará, Brasil.
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Received: Fev./2011
Accepted: Dec./2011
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