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Foraminiferal assemblage and reef check census in coral reef health monitoring of
East Brazilian margin
Cátia Fernandes Barbosa
⁎, Martina de Freitas Prazeres
Beatrice Padovani Ferreira
, José Carlos Sícoli Seoane
Departamento de Geoquímica, Universidade Federal Fluminense, Outeiro de São João Batista, s/n
andar, Centro, Niterói, Rio de Janeiro, CEP: 24020-141, Brazil
Departamento de Oceanograﬁa, Universidade Federal de Pernambuco, Av. Arquitetura, s/n, Cidade Universitária, Recife, Pernambuco, CEP: 50670-901, Brazil
Departamento de Geologia, Universidade Federal do Rio de Janeiro, Avenida Athos da Silveira Ramos, 274, bloco G, Cidade Universitária, Rio de Janeiro, RJ, CEP: 21941-916, Brazil
Received 18 September 2008
Received in revised form 30 June 2009
Accepted 3 July 2009
Human activity is changing environmental conditions on a global scale. Among the ecosystems that are
affected by human activities, coral reefs are among the most prominent. In Brazil, the coral reefs of the
Corumbau Marine Extractive Reserve (CMER) and Abrolhos National Marine Park (ANMP) in Bahia state have
some of the highest coral cover in the South Atlantic Ocean. Hard coral cover, algal cover, and foraminiferal
population distribution patterns were used to assess the coral reef benthic environments, and deﬁne a
background that can be used in worldwide comparisons in future studies. To compare these two monitoring
approaches in different coral reef environments, relative frequency data for occurrence of hard coral and algal
cover, using point-intercept transects as proposed by the Reef Check protocol, and foraminiferal samples
were collected from Corumbau (nearshore) and Abrolhos (offshore) in April 2005. The foraminiferal
assemblage was evaluated using the FORAM index (FI —Foraminifera in Reef Assessment and Monitoring),
which provides a numeric diagnosis of suitability of benthic habitat to support calcifying organisms that host
algal symbionts, originally developed for Caribbean reef areas. Coral cover in the surveyed areas, both in
Corumbau and in Abrolhos, ranged from 13% to 37%, while high foraminiferal diversities (H') were found in
all stations. Dominance of symbiont-bearing taxa of Amphistegina lessonii and Archaias angulatus only
occurred at two shallow stations, Mato Verde and Siriba, both in Abrolhos, where FI N4.00. Stations located in
Corumbau and Abrolhos had FI valuesb4.00. Q-mode cluster analysis showed that foraminifers have speciﬁc
preferences for physical conditions, especially hydrodynamics and light availability, which inﬂuence the FI
index. Although coral cover in these areas can be considered good by regional standards, foraminifer analysis
showed that the benthic system was unfavorable for symbiont-bearing foraminiferal species at most stations.
This discrepancy reveals that the FI must be used with caution in areas other than the northwestern Atlantic
and Caribbean where it was developed, and that some coral species can thrive in muddier conditions than
can most symbiont-bearing foraminifers.
© 2009 Elsevier B.V. All rights reserved.
Coral reefs are among the ecosystems affected not only by direct
human impacts such as urban costal development, sedimentation,
over ﬁshing and land-derived pollution causing nutriﬁcation, but also
by global climate changes, increasing ultraviolet radiation and
diseases, and acidiﬁcation of the oceans (Hughes et al., 2003; Hallock,
2005; Pandolﬁet al., 2005). Although coral reefs are considered
among the most diverse and productive marine ecosystem, in many
locations these impacts have contributed to loss of resilience, and
failure of coral-reef ecosystems to recover from stress events (Moberg
and Folke, 1999; Hughes et al., 2003; Buddemeier et al., 2004; Ferreira
and Maida, 2006), causing dramatic shifts in species composition and
resulting in severe economic loss (Bellwood et al., 2004).
Coral reef assessment, monitoring and management are essential
to the future of human populations that depend directly on the
resources provided by the reefs. The Reef Check monitoring program
focuses on the diagnosis of reef health, based on the census of reef
organisms, such as ﬁshes and invertebrates. These organisms were
chosen based on their economic and ecological value, as well as their
sensitivity to human impacts (Hodgson and Liebeler, 2002). The
concern with the status of conservation of coral reefs in theworld led,
in 1997, to the creation of the Global Coral Reef Monitoring Network,
bringing together results from coral-reef monitoring efforts in various
countries around the world. Coral cover is measured in all monitoring
protocols, as the trends observed over the years are a measure of reef
Marine Micropaleontology 73 (2009) 62–69
⁎Corresponding author. Tel.: +55 21 2629 2209; fax: + 55 21 2629 2234.
E-mail address: firstname.lastname@example.org (C.F. Barbosa).
0377-8398/$ –see front matter © 2009 Elsevier B.V. All rights reserved.
Contents lists available at ScienceDirect
journal homepage: www.elsevier.com/locate/marmicro
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health. More recently foraminifers have been used to quantify
environmental quality with respect to coral health (Hallock et al.,
2003; Barbosa et al., 2006; Schueth and Frank, 2008).
Reef-dwelling benthic foraminifers that host algal symbionts, also
called larger foraminifers, are shelled calcareous protists that can
attain relatively large shell sizes, ranging from 1 mm to several
centimeters (Hallock, 1999; Sugihara et al., 2006). In the reef
ecosystem, their shells are one of the main sources of calcium-
carbonate sediments that are incorporated into the reef structure
(Hallock et al., 2003; Hohenegger, 2006). Larger benthic foraminifers
host algal symbionts in a relationship analogous to that of corals and
their zooxanthellae, and are thus restricted to the photic zone (e.g.,
Lee, 1995). Most larger foraminifers thrive in relatively clear, nutrient-
poor warm waters of tropical and warm-temperate seas (Hallock,
1999; Hohenegger, 2004), where they reach their highest diversity.
However some species of larger foraminifers can also be found in
areas with poor visibility and high nutrients, such as the inshore
regions of carbonate platforms in the Java Sea and SW Sulawesi
(Indonesia), Great Barrier Reef (Australia), Madang (Papua, New
Guinea), and in Porto Seguro in Bahia state (Brazil) (e.g., Renema and
Troelstra, 2001; Langer and Lipps, 2003; Renema, 2006a, 2006b, 2008;
Schueth and Frank, 2008; Oliveira-Silva, 2008). In some cases even
extremely high densities of low diversity assemblages have been
observed under these conditions (e.g., Renema, 2008). However,
oligotrophic conditions tend to increase the relative contribution of
symbiont-bearing foraminifers to the assemblage. When nutrient ﬂux
increases, generating conditions for autotrophic and heterotrophic
organisms, the benthic community shifts to an increasing dominance
by ﬂeshy algae and sponges. The foraminiferal assemblage also shifts
to an increasing prevalence of smaller, faster growing species,
resulting in an increase in total foraminiferal diversity. Under
eutrophic conditions, stress-tolerant taxa, which can survive pollution
and anoxic conditions, will dominate (Alve, 1995; Hallock et al., 2003;
Schueth and Frank, 2008). Some advantages of using foraminifers as
bioindicators are their short life span, as compared with long-lived
colonial corals and speciﬁc niches, and therefore their ability to
respond more quickly to environmental change (Hallock et al., 2003).
Hallock et al. (2003) developed an ecological index, the FORAM
index (FI), to provide a ﬁrst order assessment of whether water quality
supports dominance by mixotrophic calcifying organisms, including
corals and larger foraminifers. The FI is based on comparison of
relative abundances of three functional groups of foraminifers
(symbiont-bearing, stress-tolerant, and other small taxa), which can
provide resource managers with a measure that is independent of
coral populations. This measure was developed, in part, to indicate
whether water quality in the benthic system is sufﬁcient to support
reef growth and recovery after a stress event (Hallock et al., 2003).
In Brazil, a National Coral Reef Monitoring Program has been under
way since 2002, and has adopted the global protocol Reef Check as a
basis. Gathering of more detailed data was incorporated, such as
identiﬁcation at species level, while still keeping the results
compatible with the Reef Check protocol (Ferreira and Maida, 2006).
The main objective of our study is to evaluate and compare the
results of coral reef health assessments based on coral and algae cover
data to those based on foraminiferal assemblages, and to test the
applicability of the FORAM Index in two southwest Atlantic reef areas.
This study compares foraminiferal assemblages with coral and algal
cover in Corumbau and Abrolhos coral reef areas (Eastern Brazil),
which have some of the best areas of coral reef cover in Southwest
2. Study sites
The Corumbau Marine Extractive Reserve (CMER, Fig. 1a) was
created in 2000, and encloses a total area of 98,174 ha, located between
the cities of Porto Seguro and Prado, close to the coast. Unlikely the
Abrolhos National Marine Park (ANMP, Fig. 1b), this reserve allows
sustainable exploitation by local populations (Prates, 2006). The
Itacolomis reefs, up to 7 km wide, are located in Corumbau, which
harbors little known coral reef areas. Human impacts are almost non-
existent, thanks to the difﬁcult access and restricted use. However, the
proximity to the coast makes this reef area more affected by the
agricultural activity in the region and consequent muddy sediment
ﬂuxes from nearby rivers (Ferreira and Maida, 2006).
The Abrolhos National Marine Park (ANMP) was established in
1983 with an area of 91,400ha and includes the Abrolhos Archipelago
plus Parcel dos Abrolhos reefs located 70km offshore in the wider
eastern Brazilian continental shelf. This area is economically impor-
tant for ecotourism (Ferreira and Gonçalves, 1999). The Abrolhos
archipelago is composed of ﬁve islands (Fig.1b) and the study sites are
within this MPA, which encloses a 6000 km
area. The coral reefs
present a mushroom shape called ‘chapeirão’, which form wide
structures that can grow to 5 to 25 m in height and 5 to 50 m in
diameter at the uppermost surface. These structures are built by an
endemic coral fauna that is capable of rising from a shallow muddy
environment (Leão, 2002).
The ANMP is under many threats, the most important being (i)
sedimentation (ii) ﬁshing activities, and (iii) tourism, which increased
400% between 1980s and 1990s (Garzón-Ferreira et al., 2000).
Abrolhos reefs have been studied from several perspectives (e.g.,
Leão, 2002; Leão and Kikuchi, 2005, Barbosa et al., 2006; Leão et al.,
2006; Evangelista et al., 2007; Spanó et al., 2008), including their
foraminiferal fauna (e.g., Sanches et al., 1995; Barbosa et al., 2006;
Oliveira-Silva, 2008; Araújo and Machado, 2008), however Corumbau
reefs and their foraminiferal faunas have only recently been surveyed
(e.g., Araújo and Machado, 2008).
Terrigenous sediment from the continent, which reaches the outer
reefs, are diluted and washed out by the southward overﬂowing Brazil
Current, thus allowing the reef's survival in the area (Leipe et al.,
1999). Seasonal wind-driven re-sedimentation associated with polar
front activity is the major contributor to the intensiﬁcation of
sedimentation processes, with an increase of about 100% of sediment
ﬂux during the summer when compared to the winter season (Segal
et al., 2008).
3. Materials and methods
3.1. Field and laboratory methods
Surveys of hard coral cover and sediment sampling were carried
out at the same sites, by the Brazilian National Coral Reef monitoring
program, at Corumbau and Abrolhos (Fig. 1). Sampling location was
recorded using a GPS set atop the diving buoy, while bathymetry was
recorded with a scuba diving computer, and visibility (water
transparency) was observed using a Secchi disk (Table 1). The stations
from Corumbau are located in the Itacolomis reefs. At Abrolhos, the
sampling stations of Siriba and Mato Verde are located in the
archipelago, while the others lie further east, in the portion of the
reef known as Parcel dos Abrolhos, site of the reef structures named
Hard coral cover was quantiﬁed using the point intercept transect
method performed on 40 points on a 20 m transect length. For each
site, four transects were sampled, then the mean percentages of
occurrence of hard coral and algae were calculated. Corals were
identiﬁed at the species level at each point.
Samples for the study of foraminifers were collected at these same
sites during the Reef Check Brazil campaign of April 2005. Nine
samples of bottom sediment were collected through SCUBA diving at
six stations in the ANMP and three stations in the CMER.
At each station, an average of 10g of sediment was homogenized
and split from the bulk sample collected, for the determination of the
benthic foraminiferal fauna and also for sediment grain-size analysis.
63C.F. Barbosa et al. / Marine Micropaleontology 73 (2009) 62–69
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The samples were ﬁxed in a solution of 4% formaldehyde containing
rose Bengal for differentiation of the living specimens at the
moment of sampling. The samples were stored inside plastic pots in a
In the laboratory, 5 g of gross weight sediment was standardized
for each sample, which were washed for foraminiferal analysis over a
63 µm sieve to remove mud, and dried in oven at 50 ° C for 24h
(Hallock et al., 2003). Subsamples were weighed, then poured into a
black tray, where the benthic foraminifers from each sample were
sorted dry under a stereomicroscope, picked out and stored on
micropaleontological slides. The picking was continued until reaching
a minimum of 150 individuals. Foraminifers that appeared highly
abraded or eroded were avoided on picking. Total fauna was used
because the number of specimens exhibiting stained protoplasm (all
chambers or one chamber) was negligible.
Individuals picked from each sample were identiﬁed at speciﬁc
level, when possible, and the relative frequency and density were
calculated. For the calculation of FORAM Index (FI), foraminifers were
arranged into functional groups deﬁned as: symbiont-bearing
foraminifers, stress-tolerant, and other smaller taxa, as previously
described by Hallock et al. (2003), and modiﬁed by Carnahan et al.
Grain-size analysis was performed using 3g of sediment from each
sample, which was washed twice with distilled water to remove the
formaldehyde. Subsequently 20 ml of sodium hexametaphosphate
) was added as a deﬂocculating agent. The samples were then
placed in an automatic shaker (Mod. 109 –Nova Ética), at speeds
between 7 and 8x10
rpm for 24h. After the incubation, the samples
were washed on a 500 µm mesh sieve in running water. No grains
larger than 500 µm were retained in any sample. Samples were placed
in the laser particle size analyzer, Cilas
model 1064, which gives a
measurement range from 500 to 0.04 µm.The procedure was
performed in accordance with the manufacturer norm.
3.2. Data analysis
The distributional pattern of the foraminiferal assemblage was
described based on univariate indices including number of species (S),
Shannon-Wiener diversity (H') and Pielou evenness (J') indices, using
the Primer v6
(Clarke and Gorley, 2006). The numerical treatment
was based on the density of each foraminiferal species.
For the calculation of FI, the specimens were arranged among the
three functional trophic groups (symbiont-bearing, stress-tolerant
and other small taxa), and for each group the proportion was
calculated as the ratio between the number of specimens of that
group and the total number of specimens counted in each sample. The
proportions were weighted to calculate the FORAM Index (FI)
(Hallock et al., 2003):
”represent the proportion of symbiont-
bearing, stress-tolerant, and other smaller species, respectively.
Fig. 1. Location of sample sites in A) Corumbau and B) Abrolhos.
64 C.F. Barbosa et al. / Marine Micropaleontology 73 (2009) 62–69
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Hallock et al. (2003) developed FI for tropical western North
Atlantic and Caribbean reef areas. The basic premise upon which the
formula for the FI was based is that 100% other smaller taxa gives an
FI=2. Any addition of symbiont-bearing taxa raises the FI, any
addition of stress-tolerant taxa lowers the FI from that reference value.
To have an FIN2, there must be some symbiont-bearing taxa, and for
FIN4, symbiont-bearing taxa must make up at least 25% of the
assemblage. Given the faster turnover rates of smaller taxa, water
quality must be sufﬁciently nutrient poor on average for the shells of
symbiont-bearing taxa to be relatively abundant. This is the basis for
the assumption that if FIN4, the environment consistently supports
calcifying mixotrophs. FI values higher than or equal 4 indicate an
environment that is suitable for coral growth, FI values between 2 and
4 represent an environment with marginal conditions for coral growth
and probably unsuitable for recovery after a stress event, and FI values
less than or equal 2 indicate conditions unsuitable for coral growth
(see also Carnahan et al., in press).
To compare the sampling sites, a data matrix was obtained from
the original matrix (Appendix A), to perform a Q-mode cluster
analysis using the Bray-Curtis coefﬁcient with fourth-root trans-
formed data, applied to species of foraminifers with relative
abundance above 4% in any sample. The same similarity matrix was
used for other analyses. A second permutation procedure, the
similarity proﬁle (SIMPROF) routine was applied to test for greater
similarity of sample groups in a priori unstructured sets of samples
(Clarke et al., 2008). All multivariate analysis was performed in Primer
v6 software (Clarke and Gorley, 2006). The SIMPROF is the set of all
resemblances between the speciﬁed samples, ranked from smallest to
largest. Next, the ordered resemblances are plotted (y-axis) against
their rank (x-axis). A Non-metric Multi-Dimensional Scaling (NMDS)
ordination was applied, resulting in a 2-d with minimum stress of
0.04. To avoid a local stress minimum the analysis was run 38 times.
A Similarity Percentages (SIMPER) of species contributions using
Bray Curtis similarity, revealed species that deﬁned the groups
observed in cluster analysis (Table 2). To test which the environmental
variables are related to the foraminiferal assemblage, the BIO-ENV
procedure was carried to discriminate the variables which most
inﬂuence the fauna.
Under the reef check protocol there are four replicate 40 point-
intercept transects for each sampling site. To compare with forami-
nifers (with no replication) we calculated the average percentage of
each variable to generate one data point per site in the matrix. The
percentages were re-calculated to include only the variables most
related to coral cover, such as calcareous algae, leaf algae, and
nutrient-indicator algae (grouped as average algae cover percentage),
and hard and soft coral (grouped as average percent coral cover).
Percentage data were arc-sine transformed; other variables were
The foraminiferal data was subjected to ANOSIM using Bray-Curtis
similarity matrix to calculate R, which is always ≤1. R=0 when there
are no group differences and R=1 when all samples in different
groups are more dissimilar to each otherthan any samples in the same
The coral reef survey shows that Corumbau and Parcel dos
Abrolhos have areas with coral cover among the highest in Brazil
(Ferreira and Maida, 2006). At Corumbau area, stations Canudos
and Silva presented the highest coral covers percentages respectively
of 30±13 and 36± 6 (Table 1). At Parcel dos Abrolhos only Barracuda
presented coral cover percentages with 37±8. Archipelago dos
Abrolhos had the lowest coral cover among the surveyed areas, and
highest algal cover. Mato Verde station had the lowest coral cover with
13 ± 8% (Fig. 2). The other stations had coral covers of around 20%. The
main coral reef species differ between the two locations but in general
the most representative species are Favia leptophylla,Mussismilia
braziliensis and Millepora nitida for Abrolhos and Mussismilia harttii
for Corumbau, some of which are endemic to Brazilian waters.
Description of the dominant grain size for each sampling station
shows that Siriba and Mato Verde (shallow areas in Abrolhos
Archipelago), and Silva (in Corumbau) had coarse sediments. All the
stations were classiﬁed as very poorly sorted. The Parcel dos Abrolhos
area, where the ‘chapeirões’are located (Fig. 1), had the ﬁnest bottom
sediment (Table 2). The sediment accumulates at the base of the
‘chapeirões’, in an area of no coral growth.
The benthic foraminiferal fauna consisted of 149 taxa belonging
mainly to the orders Rotaliida and Miliolida. Among the families of
these two orders, Peneroplidae, Alveolinidae, Amphisteginidae,
Cornuspiridae, Hauerinidae and Spiroloculinidae are the most diverse
and attain the highest densities. Living (stained) specimens were
found only at Cavalo and Siriba stations, but too few to be considered,
so that the total assemblage (living+ dead) was used in the analysis.
The Cavalo station showed the highest number of species, followed
by Silva, Pierre, Barracuda, Canudos, Abrolhos 4, Debora, Siriba and
Mato Verde (Table 2). This high number of species at Cavalo station
induced the highest diversity followed by Pierre and Barracuda. This
diversity is composed mainly by smaller heterotrophic species. At all
other stations the Shannon diversity was less than 3.1, with the lowest
found at Mato Verde (2.1). Evenness and dominance indexes were also
higher for Cavalo, Pierre and Debora stations, with the lowest values
again found at Mato Verde, where Archaias angulatus and Amphiste-
gina lessonii dominated. Densities of specimens for Corumbau stations
were very low, contrary to what was found for ‘chapeirões’sediments
where the highest density was found in Pierre, followed by Debora,
Abrolhos 4, and Barracuda. The lowest density values were found in
shallow areas at the Abrolhos' archipelago (Mato Verde and Siriba).
In all stations the presence of smaller heterotrophic species was
remarkable, with a contribution higher than 50%, except in Mato
Verde. The most abundant among these species are Quinqueloculina
lamarckiana,Q. seminulum,Spirillina vivipara,Cornuspira involvens
and Triloculina spp. Eponides repandus and Sigmamiliolinella australis
were more common in Silva and Cavalo, respectively, with relative
frequencies above 5%.
Only in Siriba and Mato Verde was the relative frequency of
symbiont-bearing foraminifers greater than 25%, where Archaias
angulatus and Amphistegina lessonii were prevalent (Fig. 3). A few
symbiont-bearing species, such Peneroplis pertusus and Laevipeneroplis
proteus, were found in most stations, at low percentages ranging from
Fig. 2. Mean relative frequency of hard coral and algae cover (%) and FORAM index for
the three stations of Itacolomis- Corumbau (Cavalo, Canudos, and Silva) and six stations
at Abrolhos (2 stations at the Archipelago —Mato Verde and Siriba; and four at the
‘chapeirões’of the Parcel —Barracuda, Debora, Abrolhos 4, and Pierre).
65C.F. Barbosa et al. / Marine Micropaleontology 73 (2009) 62–69
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0.6% to 5.5%. Among the most abundant stress-tolerant species is Boli-
vina spp., being found in almost all the stations, except in those where
the symbiont-bearing species were dominant.
In Corumbau, the symbiont-bearing foraminifers were much less
frequent than in Abrolhos (Fig. 3). Only four species were found, He-
terostegina depressa,Amphistegina lessonii,Archaias angulatus and Pe-
neroplis pertusus, in the station Silva, with relative frequencies
between 0.6 and 2.6%. The dominant stress-tolerant species were
Ammonia spp. and Elphidium spp., the latter with up to ﬁve different
species identiﬁed. The FI index exceeded 4.0 only in Mato Verde and
Siriba stations, both in the Abrolhos archipelago, with 7.3 and 4.6
respectively. The other stations located in ‘chapeirões’of the Parcel
dos Abrolhos and Corumbau had an FI lower than 4.0. Canudosstation
(located in Corumbau) and Barracuda (‘chapeirões’) had the lowest FI
(1.9); the latter had 98% of its fauna composed by stress-tolerant and
other small heterotrophic species (Figs. 2 and 3).
Hierarchical clustering based on sample similarities using Bray-
Curtis distinguished three major station groups (a, b and c) (Fig. 4).
Species primarily responsible for each group are listed in Table 3. The
ﬁrst group (a) was composed of ‘chapeirões’stations from Parcel dos
Abrolhos: Barracuda, Pierre, Abrolhos 4 and Debora; the second group
(b) included the Archipelago stations of Siriba and Mato Verde
stations; and the last group (c) was included stations from Corumbau
(Silva, Cavalo, and Canudos). The similarity proﬁle (SIMPROF) test
(Fig. 5) was used to test for evidence of internal group structure in the
full set of samples. This procedure uses randomization to test whether
the similarity within a group is greater than expected by randomly
selecting samples from the entire data set. All stations presented high
overall similarity and a signiﬁcant internal structure. The similarity
levels were 65% within group (a); 62% for group (b) and 66% for
Corumbau stations (c) (Table 3), conﬁrmed by a low stress of 0.04 in
2D multi dimensional scaling (Fig. 6).
The one-way ANOSIM analysis resulted in a global R=0.93, which
shows that all samples in the three groups are more dissimilar to each
other than any samples in the same group, i.e., the groups are distinct.
The BIO-ENV procedure was performed to identify which mea-
sured environmental variables most closely matched the foraminiferal
assemblages. The environmental variables modeled were coral and
algal cover, grain size, depth and visibility. The highest correlation
(0.66) to the foraminiferal assemblages was found for the combined
parameters algal cover, coral cover, and visibility (Table 4).
Geographic areas that naturally have low to moderate coral cover
must be taken into account in categorizing reef health (Brown et al.,
2008). Coral cover around 30% can be considered low for Indo West
Paciﬁc areas (Hodgson and Liebeler, 2002; Renema and Troelstra,
2001), even in extremely turbid environments such as the Bay of
Jakarta (Renema, 2008) or the inshore Great Barrier Reef, where coral
covers of 60–80% are not an exception; however for the Caribbean and
southwestern Atlantic areas, 30% can now be considered relatively
Only Silva, Canudos and Barracuda, all characterized by chapeirões
structures, have high coral cover (N30%). Garzón-Ferreira et al. (2000)
reported that offshore chapeirões at Parcel dos Abrolhos were in
better environmental conditions, but parts of the Abrolhos archipe-
lago showed signs of degradation. Within the archipelago, where the
Siriba and Mato Verde stations are located, the lowest coral cover was
found. Mato Verde is an area of boat anchorage and intense tourism,
and the low coral coverage and the highest percentage of algae
coverage have probably decreased its capacity to support reef growth.
In fact, a reduction of 10% in the mean annual rate of the coral
calciﬁcation has been observed for Abrolhos reefs (Oliveira et al.,
2008). Francini-Filho et al. (2008) present the ﬁrst evidence of coral
Fig. 3. The relative frequency (%) of foraminifers functional trophic groups (symbiont-
bearing, stress-tolerant, and other smaller taxa) by sampling stations.
Fig. 4. Dendrogram from hierarchical clustering. Dashed lines indicate groups of samples
not separated (at Pb0.03) by SIMPROF. Data set is from Abrolhos and Corumbau
foraminifers percentages (groups a, b and c).
Fig. 5. SIMPROF Test of the similarity proﬁle (actual) of internal group structure of the
full set of samples of Corumbau and Abrolhos, the mean simulated proﬁle (mean,
continuous line) and the upper and lower limits within which 99% of the simulated
proﬁles lie, at each rank value (broken lines).
66 C.F. Barbosa et al. / Marine Micropaleontology 73 (2009) 62–69
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diseases in Abrolhos reefs through monitoring, showing intensiﬁca-
tion during 2005–2007.
The outer reef area of Parcel dos Abrolhos, where the chapeirões
are located, still show good coral cover of up to 32%. Similar results
were reported by Villaça and Pitombo (1997), who found coral
coverage of up to 39%) in some offshore areas of the Abrolhos reefs. At
Corumbau, coral cover was comparable and reefs have a higher
species richness compared to Abrolhos archipelago reefs (Castro and
Segal, 2001). Previous data published by Ferreira and Maida (2006),
monitoring the same stations as the present work, revealed similar
patterns of coral cover for both Abrolhos and Corumbau.
Despite the proximity of the coast and the sediment runoff from the
nearby rivers, coral cover reached around 35% at Silva. Castro et al.
(2006) and (Leãoand Ginsburg,1997) reported thatcoral speciesappear
to have mechanisms to adapt to such conditions, including the
chapeirões structures, which elevate the coral habitat well above the
surrounding sediment. Sea level ﬂuctuations that have occurred since
5.1 ky BP have increased the runoff in coastal reef areas during the
Holocene. This increased sedimentation may have affected the
nearshore reef-building fauna, causing a replacement of more suscep-
tible coral fauna by species better adapted to low light levels and higher
sediment ﬂux (Leão and Kikuchi, 2005). Several authors suggest that
sediment can affect the reef-building fauna in such environments
(Coutinhoet al., 1993; Leão and Ginsburg,1997; Leão and Kikuchi, 2005;
Leão et al., 2006), while others have not described this inﬂuence in their
sampling protocols (Knoppers, 1996; Bittencourt et al., 2008).
One paradox that has been revealed previously by foraminiferal
studies is that diversity tends to increase somewhat in areas with
some human impact (e.g., modeled by Alve,1996). Similarly, we found
a high Shannon-Wiener diversity index for foraminifers found at
Cavalo, Pierre and Barracuda stations, which is associated with the
diverse assemblage of stress-tolerant and other smaller heterotrophic
taxa. This high diversity with abundance of smaller taxa indicates
either muddier conditions or higher nutrient ﬂux than is optimum for
symbiont-bearing calciﬁers. Genera like Ammonia spp., Elphidium
spp., and Nonion spp., that were more frequent in Corumbau stations,
show this area to be under the inﬂuence of ﬂuvial conditions, since
these species are tolerant of low-salinity waters (Murray, 1991) and
highly variable (seasonal or shorter term) conditions (e.g., Renema
and Troelstra, 2001).
Similarly, the Pielou evenness was usually high, except at Silva and
Mato Verde where three species dominated. The former had the
dominance of Eponides repandus (small heterotrophic taxon) and the
latter of Amphistegina lessonii/Archaias angulatus. In the latter case, the
dominance by symbiont-bearing species in the benthic system could
be interpreted to indicate high water quality. However, specimens of
A. lessonii were found in low density assemblages in sandy sediments
from Siriba and Mato Verde, indicating that hyrdrodynamic sorting
may have removed smaller taxa. Moreover, the shells of these
foraminifers have good preservation potential and can have long
residence time in the sediment. Thus, symbiont-bearing species,
which require relatively good water quality in coral reef areas, can
actually be part of a relict scenario. This is evidenced by the fact that
foraminiferal shells were broken, corroded and discolored, with no
stained specimens observed; demonstrating that the environmental
quality indicated is not necessarily the present situation for Mato
Verde. The same pattern was found by Araújo and Machado (2008) in
the Abrolhos archipelago.
The relatively shallow depth (7m), which allows sufﬁcient light
incidence at these two stations, also favored the occurrence of
A. angulatus, which seemed to have preference for shallow and
high-illuminated areas and generally lives attached to algae as noticed
by Machado et al. (2006), working at coral reefs from Bahia State. In
fact the highest algae cover was found at Mato Verde station (Fig. 2).
Sanches et al. (1995) reported the predominance of Archaias spp.
(relative frequency of foraminiferal shells of 24%) in Abrolhos area.
However, 10years later, we found that symbiont-bearing taxa were
replaced by smaller-miliolid taxa, such as Triloculina spp. and Quin-
Castro et al. (2006) measured high sedimentation rates as a result of
regional sediment re-suspension at the Itacolomis reefs (Corumbau),
which may inﬂuence the density of symbiont-bearing species as
observed in the same area, where the lowest visibility was measured
(Table 1). High turbidity prevents light penetration, indispensable for
symbiont-bearing genera such as Sorites and Peneroplis (Fujita, 2004). In
addition, the chapeirões structures themselves tend to shade the
sedimentary environment beneath them, also restricting light penetra-
tion in their immediate vicinity.
Foraminiferal densities and distributions are determined by
environmental parameters including food supply, light intensity and
Fig. 6. Foraminifers assemblage of Abrolhos and Corumbau. MDS of samples with similar community composition represented by contour lines of similar resemblance level.
67C.F. Barbosa et al. / Marine Micropaleontology 73 (2009) 62–69
Author's personal copy
hydrodynamics (Renema and Troelstra, 2001), the latter which also
inﬂuences sediment texture. Fine sediment was found at the majority
of sampling sites, demonstrating an environment of low energy and
low hydrodynamics, especially in the ‘chapeirões’of Parcel dos
Abrolhos and Corumbau sites. The sediment is deposited at the base
of the reef several meters below the area of richer coral growth. In
these shaded areas, ﬁne-sediment deposition is favored by bafﬂing
effects of the reef structures. In general, FI tended to be higher in sandy
sediments of the archipelago sites, while lower FI was found in
muddy, deeper sites as in the ‘chapeirões’.
Muddy sediments also tend to trap organic matter in the
interstitial grain spaces, supporting blooms of small heterotrophic
species. Organic matter, reported by Barbosa et al. (2006) and
Oliveira-Silva (2008), presented the highest values for the area at
the Pierre station and adjacencies. Furthermore, since these areas at
the bottom of the ‘chapeirões’present higher turbidity, the penetra-
tion of light is reduced, resulting in a narrow zone where light is
sufﬁcient to support photosynthesis. The result is that while this site
in the Abrolhos area presents one of the best coral covers within the
top of the mushroom shape of the ‘chapeirão’, high above the
sediment's ﬂuffy layer, the bottom surface sediment samples yield a
low FI, indicating that larger foraminifers do not thrive in the habitats
beneath the reefs. Similar results were also found by Barbosa et al.
(2006) for the Abrolhos reefs.
Data from this ﬁrst survey indicate that the water quality at
Abrolhos and Corumbau reefs may be becoming unsuitable. If the
symbiont-bearing foraminifers are responding to environmental
changes, while the long-living hermatypic corals are protected to
some degree by their location on the chapeirões structures, which
isolates them somewhat form the muddy sediments below and allows
them access to full sunlight. An important question for coral biologists
is, can the corals survive if rates of bioerosion increase, resulting in
destruction of the chapeirões structures?
Our study shows the importance of also focusing on bioindicators
that might respond faster to water quality changes, so preventive
measures can be taken. It is also important to verify what kind of
damages are more likely for each area. Recently, Francini-Filho et al.
(2008) found diseases affecting coral populations from the Abrolhos
bank, possibly intensiﬁed by the deterioration of the coastal environ-
ments through climate and human impacts, as has been found
elsewhere (Harvell et al., 1999). These impacts were already indicated
by foraminifers during the 2005 sampling (Barbosa et al., 2006),
reinforcing the use of thisgroup of organisms in detectingchanges in the
reef ecosystems of Brazil. Despite the result of the coral coverage, which
shows that in general the mature corals are healthy, the foraminifers-
based FI index reveals that the benthic system may be marginal for the
growth of new coral colonies in both Abrolhos and Corumbau.
Relative frequencies of hard coral and algal cover from Abrolhos
and Corumbau sites demonstrate that coral communities are well
developed in these regions. Foraminiferal analysis from the same
areas revealed, through the proportion of functional groups and FI
interpretation that water quality might be declining. The foraminiferal
assemblage appears to be responding most strongly to sediment
texture, algae and coral cover, which inﬂuences the proportion of
The dominance of smaller taxa,including stress-tolerant species, and
minimal representation of symbiont-bearing taxa, indicate unsuitable
conditions for these important calciﬁers. In the caseof foraminifers, high
values of ecological descriptors such as evenness and diversityindices in
most of the sample sites further indicate that ﬂux of nutrients and
organic matter are higher that optimal for larger foraminifers. Thus, high
diversity and evenness indicators should be used along with functional
group indicators like the FI in environmental analyses. Our work also
reveals that the FI can be strongly inﬂuenced by sediment texture and
should be interpreted accordingly. Finally, our work demonstrates that
caution should be used when applying a bioindicator developed in one
region to a new region, because there are regional differences in the
adaptability of coral communities.
However, the unique chapeirões structures characteristic of Brazilian
coral reefs supports thecorals well above the muddy sediments and near
the surface where there is sufﬁcient sunlight. Thus, the greater threat to
Brazilian reefs may be bioerosion of the undersurfaces and pillars of the
chapeirões, because if those structures are lost, the coral communities
will be lost as well. Thus, the possibility of water quality decline
indicated by the larger foraminifers and the FI suggests that monitoring
of water quality, coral recruitment and rates of bioerosion are essential
to the long-term protection of these reefs, which are important natural
resources of Brazil.
We thank the Reef Check Brazil team for the ﬁeld work and PROBIO -
Ministério do Meio Ambiente (Environmental Ministry) for the ﬁnancial
support, as well as Patricia Oliveira Silva for helping MFP in the lab.
Reviews and comments by Pamela Hallock, Marcelle K. Bou-Dagher and
Willem Renema greatly improved the manuscript. The former is kindly
thanked for pre-submittal reading of the manuscript.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at doi:10.1016/j.marmicro.2009.07.002.
Alve, E., 1995. Benthic foraminifera responses to estuarine pollution: a review. Journal of
Foraminiferal Research 25 (3), 190–203.
Alve, E., 1996. Benthic foraminiferal evidence of environmental change in the Skagerrak
over the past six decades. Norges geologiske undersøkelse bulletin 430, 85–93.
Araújo, H.A.B., Machado, A.J., 2008. Benthic foraminifera associated with the south
Bahia coral reefs, Brazil. Journal of Foraminiferal Research 38 (1), 23–38.
Barbosa, C.F., Oliveira-Silva, P., Seoane, J.C.S., Ferreira, B.P., Campello, R.C., Turcq, B.J.,
Almeida, C.M., Portilho-Ramos, R., Soares-Gomes, A., 2006. Diagnóstico da saúde
ambientalde ecossistemasrecifais da costabrasileiracom a utilização de foraminíferos
bentônicos. Projeto FOCO-PROBIO-Tamandaré e Fernando de Noronha (PE), Porto
Seguro e Arquipélago dos Abrolhos (BA), Brasil. Relatório técnico do Ministério do
Meio Ambiente - Período de 2004 a 2005, Distrito Federal, Brasil.
Bellwood, D.R., Hughes, T.P., Folke, C., Nystrom, M., 2004. Confronting the coral reef
crisis. Nature 429, 827–833.
Bittencourt, A.C.S.P., Leão, Z.M.A.N., Kikuchi, R.K.P., Domínguez, J.M.L., 2008. Deﬁcit of
sand in a sediment transport model favors coral reef development in Brazil. Anais
da Academia Brasileira de Ciências 80 (1), 205–214.
Brown, E.K., Jokiel, P.L., Rodgers, K.S., Smith, W.R., Roberts, L.M., 2008. The status of the
reefs along South Moloka'i: Five Years of Monitoring. In: Field, M.E., Cochran, S.A.,
Logan, J.B., Storlazzi, C.D. (Eds.), The Coral Reef of South Moloka'i, Hawai'i—Portrait
of a Sediment-Threatened Fringing Reef. U.S. Geological Survey Scientiﬁc
Investigations Report 2007–5101, pp. 51–58.
Buddemeier, R.W., Kleypas, J.A., Aronson, R.B., 2004. Coral reefs and global climate
change: potential contributions of climate change to stresses on coral reef
ecosystems. Pew Center on Global Climate Change, Arlington, USA.
Carnahan, E.A., Hoare, A.M., Hallock, P., Lidz, B.H., Reich, C.D. IN PRESS. Foraminiferal
Assemblages in Biscayne Bay, Florida, USA: Responses to Urban and Agricultural
Pollution in a Subtropical Estuary. Marine Ecology, special issue.
Castro, C.B., Segal, B., 2001. The Itacolomis: large and unexplored reefs at the arrival
point of the ﬁrst Europeans in Brazil. Coral Reefs, Berlin 20, 18-18.
Castro, C.B., Amorim, L.C., Calderon, E.M., Segal, B., 2006. Cobertura e recrutamento de
corais recifais (Cnidaria: Scleractinia e Milleporidae) nos recifes Itacolomis, Brasil.
Arquivos do Museu Nacional 64, 29–40.
Clarke, K.R., Gorley, R.N., 2006. PRIMER v.6: User manual/Tutorial. PRIMER-E, Plymouth.
Clarke, K.R., Somerﬁeld, P.J., Gorley, R.N., 2008. Testing of null hypotheses in exploratory
community analyses: similarity proﬁles and biota-environment linkage. Journal of
Experimental Marine Biology and Ecology 366, 56–69.
Coutinho, R., Villaça, R.C., Magalhães, C.A., Guimarães, M.A., Apolinário, M., Muricy, G.,
1993. Inﬂuencia antrópica nos ecossistemas coralinos da região de Abrolhos, Bahia,
Brasil. Acta biologica Leopoldensia 15 (1), 133–144.
Evangelista, H., Godiva, D., Sifeddine, A., Leão, Z.M.A.N., Rigozo, N.R., Segal, B., Ambrizzi,
T., Kampel, M., Kikuchi, R.K.P.Le, Cornec, F., 2007. Evidences linking ENSO and coral
growth in the Southwestern-South Atlantic. Climate Dynamics 29, 869–880.
68 C.F. Barbosa et al. / Marine Micropaleontology 73 (2009) 62–69
Author's personal copy
Ferreira, C., Gonçalves, J.E.A., 1999. The unique Abrolhos Reef Formation (Brazil): need
for speciﬁc management strategies. Coral Reefs 18, 352.
Ferreira, B.P., Maida, M., 2006. Monitoramento dos recifes de coral do Brasil –Situação
Atual e Perspectivas. Série Biodiversidade 18, Instituto do Meio Ambiente e dos
Recursos Naturais Renováveis, Ministério do Meio Ambiente, Brasília, Brasil.
Francini-Filho, R.B., Moura, R.L., Thompson, F.L., Reis, R.M., Kaufmand, L., Kikuchi, R.K.P.,
Leão,Z.M.A.N., 2008. Diseasesleading to accelerated declineof reef coralsin the largest
South Atlantic reef complex (Abrolhos Bank, eastern Brazil. Marine Pollution Bulletin
56 (5), 1008–1014.
Fujita, K., 2004. A ﬁeld colonization experiment on small-scale distributions of algal
symbiont-bearing largerforaminiferaon reef rubble. Journalof ForaminiferalResearch
34 (3), 169–179.
Garzón-Ferreira, J., Cortés, J., Croquer, A., Guzmán, H., Leão, Z.M.A.N., Rodríguez-Ramírez,
A., 2000. Statusof coral reefsin southern tropicalAmerica: Brazil,Colombia, CostaRica,
Panama and Venezuela. In: Wilkinson, C. (Ed.), Status of Coral Reefs of the World:
2000. Australian Institute of Marine Science, Townsville, pp. 331–348.
Hallock, P., 1999. Symbiont-bearing Foraminifera. In: Sen Gupta, B.K. (Ed.), Modern
Foraminifera. Kluwer Academic Publishers, Netherlands, pp. 123–139.
Hallock, P., Lidz, B.H., Cockey-Burkhard, E.M., Donnely, K.B., 2003. Foraminifera as
bioindicators in coral reef and monitoring: the FORAM Index. Environmental
Monitoring and Assessment 81, 221–238.
Hallock, P., 2005. Global change and modern coral reefs: New opportunities to
understand shallow-water carbonate depositional processes. Sedimentary Geology
Harvell,C.D., Kim, K.,Burkholder,J.M., Colwell,R.R., Epstein,P.R.,Grimes, D.J.,Hofmann, E.E.,
Lipp, E.K., Osterhaus, A.D.M.E., Overstreet, R.M., Porter, J.W., Smith, G.W., Vasta, G.R.,
1999. Emerging marinediseases: climatelinks and anthropogenic factors.Science 285,
Hodgson, G., Liebeler, J., 2002. The global coral reef —5 years of reef check. Institute of
the Environment, Los Angeles, USA, Reef Check Foundation, LA.
Hohenegger, J., 2004. Depth coenoclines and environmental considerations of western
Paciﬁc larger foraminifera. Journal of Foraminiferal Research 34 (1), 9–33.
Hohenegger, J., 2006. The importance of symbiont-bearing benthic foraminifera for
West Paciﬁc carbonate beach environments. Marine Micropaleontology 61, 4–39.
Hughes, T.P., Baird, A.H., Bellwood, D.R., Card, M., Connolly, S.R., Folke, C., Grosberg, R.,
Hoegh-Guldberg, O., Jackson, J.B.C., Kleypas, J., Lough, J.M., Marshall, P.,Nyström, M.,
Palumbi, S.R., Pandolﬁ, J.M., Rosen, B., Roughgarden, J., 2003. Climate change,
human impacts, and the resilience of coral reefs. Science 301, 929–933.
Knoppers,B.A., 1996.Particulate organic matter andnutrients. In: Ekau, W., Knoppers, B.A.
(Eds.), Sedimentation processes and productivity in the continental shelf waters of
East and Northeast Brazil. Join Oceanographic Projects. JOPS Cruise report and ﬁrst
results. Center for Tropical Marine Ecology, Bremen, pp. 36–37.
Langer, M.R., Lipps, J.H., 2003. Foraminiferal distribution and diversity, Madang Reefand
Lagoon, Papua New Guinea. Coral Reefs 22,143–154.
Leão, Z.M.A.N., 2002. Abrolhos, BA- O complexo recifal maisextenso do Atlântico Sul.In:
Schobbenhaus, C., Campos, D.A., Queiroz, E.T., Winge, M., Berbert-Born, M.L.C. (Eds.),
Sítios Geológicos e Paleontológicos do Brasil. DNPM/CPRM - Comissão Brasileira de
Sítios Geológicos e Paleobiológicos (SIGEP), Brasília, Brasil, pp. 345–359.
Leão, Z.M.A.N., Dutra, L.X.C., Spanó, S., 2006. The characteristics of bottom sediments. In:
Dutra, G.F., Allen, G.R., Werner, T., McKenna, S.A. (Eds.), A rapid marine biodiversity
assessmentof the Abrolhos bank, Bahia. Brazil: RAP Bulletin of Biological Assessment,
vol. 38, pp. 75–81.
Leão, Z.M.A.N., Ginsburg, R.N., 1997. Living reefs surrounded by siliciclastics sediments:
the Abrolhos coastal reefs, Bahia, Brazil: Proceedings of 8th International Coral Reef
Symposium, vol. 2, pp. 1767–1772 .
Leão, Z.M.A.N., Kikuchi, R.K.P., 2005. A relic coral fauna threatened by global changes
and human activities, Eastern Brazil. Marine Pollution Bulletin 51, 599–611.
Lee, J.J., 1995. Living sands —the symbiosis of protists and algae can provide good
models for the study of host/symbiont interactions. BioScience 45, 252–261.
Leipe, T., Knoppers, B., Marone, E., Camargo, R., 1999. Suspended matter transport in
coral reef waters of the Abrolhos Bank, Brazil. Geo-Marine Letters 19, 186–195.
Machado, A.J., Andrade, E.J., Nascimento, H.A., 2006. Fauna de foraminíferos do litoral
norte do Estado da Bahia. Revista de Geologia (Fortaleza) 19, 147–154.
Moberg, F., Folke, C., 1999. Ecological goods and services of coral reef ecosystems.
Ecological Economics 29, 215–233.
Murray, J.W., 1991. Ecology and palaeoecology of benthic foraminifera. Longman
Scientiﬁc and Technical, England.
Oliveira, M., Leão, Z.M.A.N., Kikuchi, R.K., 2008. Calciﬁcation rates of the endemic coral
Mussismilia braziliensis declined associated with ocean warming. 11th ICRS, Interna-
tional Coral Reef Symposium, Fort Lauderdale, 7-11 July, Florida, Abstracts, p.272.
Oliveira-Silva,P., 2008.Diagnóstico ambiental dos ecossistemasrecifaisde Abrolhos e Porto
Seguro,BA com ênfase em foraminíferos e indicadores geoquímicos. Doctorate Thesis,
Programa de Geoquímica,Universidade Federal Fluminense, Niterói, Brasil.
Pandolﬁ, J.M., Bradbury, R.H., Sala, E., Hughes, T.P., Bjorndal, K.A., Cooke, R.G., McArdle, D.,
McClenachan, L., Newman, M.J.H., Paredes, G., Warner,R.R., Jackson, J.B.C., 20 05. Are
U.S. coral reefs on the slippery slope to slime? Science 307, 1725–1726.
Prates, A.P.L., 2006. Reserva Extrativista Marinha do Corumbau. In: Prates, A.P.L. (Ed.),
Atlas dos Recifes de Coral nas Unidades de Conservação Brasileiras. 2ª Edição,
Ministério do Meio Ambiente, Brasília, Brasil, pp. 116–129.
Renema, W., 2006a. Large benthic foraminifera from the deep photic zone of a mixed
siliciclastic-carbonate shelf off East Kalimantan, Indonesia. Marine Micropaleontology
Renema, W., 2006b. Habitat variables determining the occurrence of large benthic
foraminifera in the Berau area (East Kalimantan, Indonesia. Coral Reefs 25, 351–359.
Renema, W., 2008. Habitat selective factors inﬂuencing the distribution of large benthic
foraminiferal assemblages over the Kepulauan Seribu. Marine Micropaleontology
Renema, W., Troelstra, S.R., 2001. Larger foraminifera distribution on a mesotrophic
carbonate shelf in SW Sulawesi (Indonesia). Palaeogeography, Palaeoclimatology,
Palaeoecology 175, 125–146.
Sanches, T.M., Kikuchi, R.K.P., Eichler, B.B., 1995. Ocorrência de foraminíferos recentes
em Abrolhos, Bahia. Publicação especial do Instituto Oceanográﬁco de São Paulo 11,
Segal, B., Evangelista, H., Kampel, M., Gonçalves, A.C., Polito, P.S., dos Santos, E.A., 2008.
Potential impacts of polar fronts on sedimentation processes at Abrolhos coral reef
(South-West Atlantic Ocean/Brazil. Continental Shelf Research 28 (4-5), 533–544 30.
Schueth, J.D., Frank, T.D., 2008. Reef foraminifera as bioindicators of coral reef health:
Low Isles Reef, Northern Great Barrier Reef, Australia. Journal of Foraminiferal
Research 38, 11–22.
Spanó, S., Leão, Z.M.A.N., Kikuchi, R.K.P., 2008. Diagnóstico do estado de conservação
dos recifes em franja do Parque Nacional Marinho dos Abrolhos. OLAM Ciência &
Tecnologia 8, 245–277.
Sugihara, K., Masunaga, N., Fujita, K., 2006. Latitudinal changes in larger benthic
foraminiferal assemblages in shallow-water reef sediments along the Ryukyu
Islands, Japan. Island Arc 15, 437–454.
Villaça, R.C., Pitombo, F.B., 1997. Benthic communities of shallow-water reefs in
Abrolhos, Brazil. Revista Brasileira de Oceanograﬁa 45, 35–43.
69C.F. Barbosa et al. / Marine Micropaleontology 73 (2009) 62–69