Article

Foraminiferal assemblage and reef check census in coral reef health monitoring of East Brazilian margin

Abstract and Figures

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 N 4.00. Stations located in Corumbau and Abrolhos had FI values b 4.00. 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.
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Foraminiferal assemblage and reef check census in coral reef health monitoring of
East Brazilian margin
Cátia Fernandes Barbosa
a,
, Martina de Freitas Prazeres
a
,
Beatrice Padovani Ferreira
b
, José Carlos Sícoli Seoane
c
a
Departamento de Geoquímica, Universidade Federal Fluminense, Outeiro de São João Batista, s/n
o
,5
o
andar, Centro, Niterói, Rio de Janeiro, CEP: 24020-141, Brazil
b
Departamento de Oceanograa, Universidade Federal de Pernambuco, Av. Arquitetura, s/n, Cidade Universitária, Recife, Pernambuco, CEP: 50670-901, Brazil
c
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
abstractarticle info
Article history:
Received 18 September 2008
Received in revised form 30 June 2009
Accepted 3 July 2009
Keywords:
Benthic foraminifers
Coral reef
FORAM index
Southwestern Atlantic
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 dene 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 specic
preferences for physical conditions, especially hydrodynamics and light availability, which inuence 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.
1. Introduction
Coral reefs are among the ecosystems affected not only by direct
human impacts such as urban costal development, sedimentation,
over shing and land-derived pollution causing nutrication, but also
by global climate changes, increasing ultraviolet radiation and
diseases, and acidication of the oceans (Hughes et al., 2003; Hallock,
2005; Pandolet 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 shes 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) 6269
Corresponding author. Tel.: +55 21 2629 2209; fax: + 55 21 2629 2234.
E-mail address: catia@geoq.uff.br (C.F. Barbosa).
0377-8398/$ see front matter © 2009 Elsevier B.V. All rights reserved.
doi:10.1016/j.marmicro.2009.07.002
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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 ux
increases, generating conditions for autotrophic and heterotrophic
organisms, the benthic community shifts to an increasing dominance
by eshy 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 specic 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 rst 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 sufcient 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
identication 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
Atlantic.
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 difcult 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
uxes 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 ve islands (Fig.1b) and the study sites are
within this MPA, which encloses a 6000 km
2
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) shing 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 overowing 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 intensication of
sedimentation processes, with an increase of about 100% of sediment
ux 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
chapeirões.
Hard coral cover was quantied 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
identied 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) 6269
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The samples were xed in a solution of 4% formaldehyde containing
1gl
1
rose Bengal for differentiation of the living specimens at the
moment of sampling. The samples were stored inside plastic pots in a
freezer.
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 identied at specic
level, when possible, and the relative frequency and density were
calculated. For the calculation of FORAM Index (FI), foraminifers were
arranged into functional groups dened as: symbiont-bearing
foraminifers, stress-tolerant, and other smaller taxa, as previously
described by Hallock et al. (2003), and modied by Carnahan et al.
(in press).
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
(40 gl
1
) was added as a deocculating agent. The samples were then
placed in an automatic shaker (Mod. 109 Nova Ética), at speeds
between 7 and 8x10
2
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):
FI ¼ð10×PsÞþðPoÞþð2×PhÞ
where P
s
,P
o
and P
h
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) 6269
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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 sufciently 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 coefcient 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 prole (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 specied 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 dened 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
inuence 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
normalized.
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
group.
4. Results
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 classied as very poorly sorted. The Parcel dos Abrolhos
area, where the chapeirõesare located (Fig. 1), had the nest 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 chapeirõessediments
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
chapeirõesof the Parcel Barracuda, Debora, Abrolhos 4, and Pierre).
65C.F. Barbosa et al. / Marine Micropaleontology 73 (2009) 6269
Author's personal copy
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 ve different
species identied. 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 chapeirõesof 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
rst group (a) was composed of chapeirõesstations 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 prole (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 signicant internal structure. The similarity
levels were 65% within group (a); 62% for group (b) and 66% for
Corumbau stations (c) (Table 3), conrmed 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).
5. Discussion
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
Pacic 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 6080% are not an exception; however for the Caribbean and
southwestern Atlantic areas, 30% can now be considered relatively
high coverage.
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
calcication has been observed for Abrolhos reefs (Oliveira et al.,
2008). Francini-Filho et al. (2008) present the rst 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 prole (actual) of internal group structure of the
full set of samples of Corumbau and Abrolhos, the mean simulated prole (mean,
continuous line) and the upper and lower limits within which 99% of the simulated
proles lie, at each rank value (broken lines).
66 C.F. Barbosa et al. / Marine Micropaleontology 73 (2009) 6269
Author's personal copy
diseases in Abrolhos reefs through monitoring, showing intensica-
tion during 20052007.
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 uctuations 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 ux (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 inuence 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 ux than is optimum for
symbiont-bearing calciers. Genera like Ammonia spp., Elphidium
spp., and Nonion spp., that were more frequent in Corumbau stations,
show this area to be under the inuence of uvial 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 sufcient 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-
queloculina spp.
Castro et al. (2006) measured high sedimentation rates as a result of
regional sediment re-suspension at the Itacolomis reefs (Corumbau),
which may inuence 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) 6269
Author's personal copy
hydrodynamics (Renema and Troelstra, 2001), the latter which also
inuences sediment texture. Fine sediment was found at the majority
of sampling sites, demonstrating an environment of low energy and
low hydrodynamics, especially in the chapeirõesof 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, ne-sediment deposition is favored by bafing
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 chapeirõespresent higher turbidity, the penetra-
tion of light is reduced, resulting in a narrow zone where light is
sufcient 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 uffy 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 rst 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 intensied 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.
6. Conclusions
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 inuences the proportion of
functional groups.
The dominance of smaller taxa,including stress-tolerant species, and
minimal representation of symbiont-bearing taxa, indicate unsuitable
conditions for these important calciers. In the caseof foraminifers, high
values of ecological descriptors such as evenness and diversityindices in
most of the sample sites further indicate that ux 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 inuenced 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 sufcient 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.
Acknowledgments
We thank the Reef Check Brazil team for the eld work and PROBIO -
Ministério do Meio Ambiente (Environmental Ministry) for the nancial
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.
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... FI values obtained in this study appear similar to those from other regions with anthropogenic pollution (Barbosa et al. 2009;Carnahan et al. 2009;Caruso et al. 2011;Barbosa et al. 2012). However, FI values of 10 are seldom recorded in other studies even in pristine regions (Barbosa et al. 2009;Barbosa et al. 2012). ...
... FI values obtained in this study appear similar to those from other regions with anthropogenic pollution (Barbosa et al. 2009;Carnahan et al. 2009;Caruso et al. 2011;Barbosa et al. 2012). However, FI values of 10 are seldom recorded in other studies even in pristine regions (Barbosa et al. 2009;Barbosa et al. 2012). In this study, five samples (1-3, 5, 6) recorded a FI value of approximately 10 in the outer bay of Kāneʻohe, mainly consisting of lens-shaped Amphistegina spp. ...
... However, winter storm motion and trade wind influence is restricted to the northern area (Bathen 1968) and should not influence samples from the southern area. Although the FI can vary with other parameters such as sediment texture (Narayan and Pandolfi 2010), hydrodynamic regime, and light penetration (Barbosa et al. 2009), various studies have shown that the FI is primarily related to water quality (Uthicke and Nobes 2008;Koukousioura et al. 2011;Velásquez et al. 2011;Banner 1974;Oliver et al. 2014). The results from our Bayesian regression framework might support this as there was no apparent relationship between the FI and water depth (Table S3). ...
... FI values obtained in this study appear similar to those from other regions with anthropogenic pollution (Barbosa et al. 2009;Carnahan et al. 2009;Caruso et al. 2011;Barbosa et al. 2012). However, FI values of 10 are seldom recorded in other studies even in pristine regions (Barbosa et al. 2009;Barbosa et al. 2012). ...
... FI values obtained in this study appear similar to those from other regions with anthropogenic pollution (Barbosa et al. 2009;Carnahan et al. 2009;Caruso et al. 2011;Barbosa et al. 2012). However, FI values of 10 are seldom recorded in other studies even in pristine regions (Barbosa et al. 2009;Barbosa et al. 2012). In this study, five samples (1-3, 5, 6) recorded a FI value of approximately 10 in the outer bay of Kāneʻohe, mainly consisting of lens-shaped Amphistegina spp. ...
... However, winter storm motion and trade wind influence is restricted to the northern area (Bathen 1968) and should not influence samples from the southern area. Although the FI can vary with other parameters such as sediment texture (Narayan and Pandolfi 2010), hydrodynamic regime, and light penetration (Barbosa et al. 2009), various studies have shown that the FI is primarily related to water quality (Uthicke and Nobes 2008;Koukousioura et al. 2011;Velásquez et al. 2011;Banner 1974;Oliver et al. 2014). The results from our Bayesian regression framework might support this as there was no apparent relationship between the FI and water depth (Table S3). ...
Article
Context: Tropical coral reef environments provide a wide variety of goods and ecosystem services but are experiencing growing pressure from coastal development and tourism. Assessing the status of reef communities along gradients of human pressure is therefore necessary to predict recovery and resilience capacity of reefs. Aims: First, to determine the overall water quality in Kāne‘ohe Bay, O’ahu, Hawai‘i, by employing a low-cost monitoring approach for anthropogenic stress on coral reef areas. Second, to assess the suitability of the monitoring approach to complement existing monitoring programmes. Methods: Sediment samples containing benthic foraminifera were used to determine water quality and stressor sources in Kāne‘ohe Bay, O’ahu, Hawai‘i, by applying the Foram Index (FI) and Bayesian regression analysis. The FI is based on relative abundance of functional groups of larger benthic foraminifera. Key results: Overall water quality in Kāne‘ohe Bay may support active growth and recovery of coral reefs in the northern sector but deteriorates around Kāne‘ohe City. Conclusions: Benthic foraminifera can be used as bio-indicators in Hawaiian reefs, providing an easy and fast-to-apply method for assessing short-term changes in water quality and stress sources. Implementing benthic foraminifera studies within existing long-term monitoring programs of Hawaiian reefs can be beneficial for conservation efforts. Implications: Within a historic context, our findings illustrate the modest recovery of an ecosystem following pollution control measures but highlight the need of conservation efforts for reef environments adjacent to major human settlements.
... As such, to derive an FI value > 2 'symbiont-bearing' taxa must be present. Where 'symbiont-bearing' taxa account for at least 25% of the overall foraminiferal assemblage, the FI will be > 4. Given the faster turnover rates of smaller foraminifera, for environments to support the proliferation of 'symbiont-bearing' taxa, average water quality must be sufficiently deficient of nutrients and suspended sediment (Barbosa et al. 2009). On this basis, where FI > 4, prevailing environmental conditions are considered to consistently support communities of calcifying mixotrophic organisms, and therefore also reef development. ...
... Food supply is an important factor influencing foraminiferal microhabitat availability (Jorissen et al. 1995). For example, in mud rich sediments such as within the PSRC, organic matter is readily trapped within interstitial sediment pore spaces and utilised by heterotrophic foraminifera as a food source (Jorissen et al. 1995;Barbosa et al. 2009). However, when food supply is scarce and sufficient light is available, kleptoplastic taxon such as Elphidium may profit from photosynthetic products derived from chloroplasts sequestered from their food source (mainly diatoms) (Lopez 1979;Renema 2008). ...
... Outside of Australia's GBR, instances of turbid nearshore reef development are geographically widespread, with exemplars found in the Arabian Gulf, Borneo, Brazil, China, Hawaii, India, Japan, Micronesia, Mozambique, New Caledonia, the Red Sea, Singapore, Thailand, and western Australia (Perry 2011;Roy and Smith 1971;Tudhope and Scoffin 1994;Renema and Troelstra 2001;Kleypas et al. 1999;Barbosa et al. 2009;Goodkin et al. 2011;van Woesik et al. 2012;Cacciapaglia and van Woesik 2015a;Richards et al. 2015;Guest et al. 2016b). ...
Thesis
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Understanding how coral reefs have developed in the past is crucial for placing contemporary ecological and environmental change within appropriate reef building timescales (i.e. centennial to millennial). On Australia’s Great Barrier Reef (GBR), coral reefs situated within nearshore settings on the inner continental shelf are a particular priority. This is due to their close proximity to river point sources, and therefore susceptibility to reduced water quality as the result of extensive modification of adjacent river catchments following European settlement in the region (ca. 1850 CE). However, the extent of water quality decline and its impact on the coral reefs of the GBR’s inner-shelf remains contentious and is confounded by a paucity of long-term (> decadal) datasets. Central to the on-going debate is uncertainty related to the impact of increased sediment loads, relative to the natural movement and resuspension of terrigenous sediments, which have accumulated on the inner-shelf over the last ~6,000 years. The main aim of this thesis was to characterise and investigate the vertical development of turbid nearshore coral reefs on the central GBR. This aim was achieved through the recovery of 21 reef cores (3 - 5 m in length) from five proximal turbid nearshore reefs, currently distributed across the spectrum of reef ‘geomorphological development’ within the Paluma Shoals reef complex (PSRC). The recovered reef cores were used to establish detailed depositional and palaeoecological records for the investigation of the (1) internal development and vertical accretionary history of the PSRC; and (2) compositional variation in turbid nearshore coral and benthic foraminiferal assemblages during vertical reef accretion towards sea level. Established chronostratigraphic and palaeoecological records were further used to assess the impact of post-European settlement associated water quality change in a turbid nearshore reef setting on the central GBR. Radiocarbon dating (n = 96 dates) revealed reef initiation within the PSRC to have occurred between ~2,000 and 1,000 calibrated years before present, with subsequent reef development occurring under the persistent influence of fine-grained (< 0.063 mm) terrigenous sediments. The internal development of the PSRC was characterised by discrete reef facies comprised of a loose coral framework with an unconsolidated siliciclastic-carbonate sediment matrix. A total of 29 genera of Scleractinian coral and 86 genera of benthic foraminifera were identified from the palaeoecological inventory of the PSRC. Both coral and benthic foraminiferal assemblages were characterised by distinct assemblages of taxa pre-adapted to sediment stress (i.e. low light availability and high sedimentation). At the genus level, no discernable evidence of compositional change in either coral or benthic foraminiferal assemblages was found, relative to European settlement. Instead, variations in assemblage composition were driven by intrinsic changes in prevailing abiotic conditions under vertical reef accretion towards sea level (e.g. hydrodynamic energy, light availability, and sedimentation rate). These findings therefore highlight the importance for considering reef ‘geomorphological development’ when interpreting contemporary reef ecological status. Furthermore, this research emphasises the robust nature of turbid nearshore reefs and suggests that they may be more resilient to changes in water quality than those associated with environmental settings where local background sedimentary conditions are less extreme (e.g. towards the inner/mid-shelf boundary). To this end, this thesis presents new baseline records with which to assess contemporary ecological and environmental change within turbid nearshore settings on the central GBR.
... The FORAM (Foraminifera in Reef Assessment and Monitoring) Index (FI) by Hallock et al. (2003) has been widely used as an indicator of water quality favorable to the growth and resurgence of photosynthesizing holobionts like corals. The FI has already been applied to reef environments in Puerto Rico (Oliver et al., 2014), Florida (Carnahan et al., 2009), Brazil (Barbosa et al., 2009), Pacific Islands (Fajemila et al., 2015), Australia (Schueth and Frank, 2008;Uthicke and Nobes, 2008;Uthicke et al., 2010) and Greece (Koukousioura et al., 2011). Analogous to FI, the Foram Stress Index (FISI) introduced by Dimiza et al. (2016) has also gained popularity as an effective monitoring tool for soft-bottom marine environments (Gomez-Leon et al., 2018;Elshanawany et al., 2018;El Kateb et al., 2020;Minhat et al., 2020;Sanchez et al., 2020;Fossile et al., 2021). ...
... However, despite the high assemblage of SBF, the coral cover in Nogas Island is generally poor, with a present live hard coral cover of 20.5%. Barbosa et al. (2009) and Velasquez et al. (2011) reported no correlation between FI and coral cover. This can be explained with corals requiring a longer recruitment and recovery period than foraminifers due to acute disturbances such as cyclones, bleaching, disease outbreak, and Acantahster planci attacks (Uthicke et al., 2010). ...
Article
Global coral reef decline is largely due to natural and anthropogenic stressors such as climate change-related bleaching, frequent storm damage, pollution, and overfishing. Benthic foraminifera is used as a powerful tool for environmental assessment because of its susceptibility to both physical and chemical changes in the environment. This study evaluated the abundance, diversity, and functional group composition of benthic foraminifera in Nogas Island, Philippines. The FORAM Index (FI) was used as an indicator to determine whether the environmental condition is favorable or unfavorable to the growth and recovery of calcifying mixotrophs. Similarly, the Foram Stress Index (FSI) was used to evaluate the ecological quality of sedimentary habitats according to the sensitivity and tolerance of benthic foraminifera to pollution. The foraminifera assemblage was dominated by large symbiont-bearing (94.75%) , followed by small and heterotrophic (4.0%) , and opportunistic (1.25%) taxa. The assemblages were consistently dominated by Family Calcarinidae at 76.8%, followed by Genus Amphistegina (8.0%), and Heterostegina depressa (3.5%). FI values were very high at >4.0, indicating that the current environment is suitable for the growth of corals and could support recovery from significant disturbances. The >9.0 FSI revealed that the sediment habitat is unpolluted or pristine. The results of this study showed the status of the island’s coral reef conditions and resiliency to disturbances through the use of foraminiferal indicators.
... This index was developed as a water quality-based reef assessment tool in Florida and the Caribbean (Prazeres et al., 2020;Uthicke et al., 2012;Schueth and Frank, 2008;Hallock et al., 2003). At the time that it was proposed, however, Hallock et al. (2003) foresaw the need to evolve the FI to tune its performance beyond the region where it was created; a premonition supported by some subsequent data collection (Barbosa et al., 2012(Barbosa et al., , 2009Renema, 2010Renema, , 2008. Furthermore, the FI was created using three functional groups of forams, whose relative abundance primarily responded to nutrients-a highly relevant parameter for reef health, but, in an age of rapidly warming seas inducing catastrophic coral bleaching, not always predominant. ...
Article
Coral reefs are in terminal decline. For conservation to be effective, naturally depauperate reefs must be distinguished from those recently degraded by humans. Traditional reef monitoring is time consuming and lacks the longevity to make this distinction. Success in using foraminifera as bioindicators for reef health has hitherto levered their response to nutrients. Because ocean heat waves are the dominant driver of coral bleaching and death, there is compelling motivation to develop new foraminiferal bioindicators that inform on temperature stress over meaningful timescales. This study focuses on identifying which foraminifera respond systematically to the temperature stress that kills corals. Statistical models were used to compare endosymbiont-bearing foraminiferal families, collected along a heat-stress gradient spanning the Solomon Islands and New Caledonia, to live coral cover at the same sites. Results indicate that Amphisteginidae foraminifera and coral cover show a significant decline in abundance as heat stress increases along the transect sites. Furthermore, ocean productivity and salinity, both recognized environmental influences on foraminifera, are shown to be subordinate to temperature in their sway of this ecological patterning. These findings indicate the potential for using foraminifera to develop new indices capable of quantifying long-term thermal impacts on reefs.
... Therefore, by using these two indices, we have the unique opportunity to observe and document some of the complex physical and ecological interactions that control reef equilibrium. A factor that can influence both indices is grain size (Hallock et al., 2003;Ramirez et al., 2008;Carnahan et al., 2009;Barbosa et al., 2009). In particular, higher values of FI can be expected to positively correlate with coarser grain size (Hallock et al., 2003;Ramirez et al., 2008) and negatively with fine grain size (e.g., Narayan and Pandolfi, 2010). ...
... On the other hand, smaller heterotrophic taxa and stress-tolerant (e.g., opportunis c) taxa thrive in condi ons where light penetra on is not a limi ng factor but variability in food sources (labile organic ma er) (Uthicke and Nobes, 2008) and changes in salinity and oxygena on are limi ng (e.g., Prazeres et al., 2020). In addi on, FI has been demonstrated to reflect substrate type, distance from shore, algae and coral cover changes (e.g., Barbosa et al., 2009;Emrich et al., 2017). ...
Technical Report
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Multiple assessment techniques (in situ active water samplers, Ames test, sea urchin development toxicity assay, Colitag, sediment analysis, foram community characterization) were used to assess the pollution status of Fagatele Bay, a unit of the National Marine Sanctuary of American Samoa. Pollution levels were generally low, but coastal managers can use these data to make sure that conditions don't deteriorate over time.
... On the other hand, smaller heterotrophic taxa and stress-tolerant (e.g., opportunis c) taxa thrive in condi ons where light penetra on is not a limi ng factor but variability in food sources (labile organic ma er) (Uthicke and Nobes, 2008) and changes in salinity and oxygena on are limi ng (e.g., Prazeres et al., 2020). In addi on, FI has been demonstrated to reflect substrate type, distance from shore, algae and coral cover changes (e.g., Barbosa et al., 2009;Emrich et al., 2017). ...
Article
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Fagatele Bay is an embayment within the NaƟonal Marine Sanctuary of American Samoa for which there are minimal data regarding contaminant distribuƟon in this protected area. Resource managers have significant concerns about the potenƟal inputs of contaminants from an unlined, solid waste landfill located approximately 600 m upslope from the Bay. Leachate from the landfi ll potenƟally includes both organic (e.g. PCBs, PAHs, personal care products) and inorganic (e.g. heavy metals) pollutants, and could reach the Bay through surface runoff, or, given the permeability of the volcanically derived soils, through groundwater flux. There is also the potenƟal for other land-based sources of polluƟon (LBSP, such as pesƟcides) to reach the Bay. The treatment of solid waste is a serious problem on most islands that can result in toxic substances entering the coastal environment. The potenƟal transport of pollutants from the landfill to the Bay has not been previously quanƟfi ed. This study addresses this important research quesƟon, i.e. what contaminants are present in Fagatele Bay? This assessment is important for two reasons: 1) to determine the extent (magnitude and spaƟ al distribuƟon) of polluƟon in the Bay; and 2) to serve as baseline for future assessment, and to evaluate the effecƟveness of future watershed management acƟviƟes which might be designed to improve coral reef ecosystem health by reducing LBSP. The approach presented here assessed contaminaƟon risk to the Bay using mulƟple techniques: acƟve in situ water samplers for organic chemistry analysis, metals analysis of sediment samples, bacterial (Colitag) and nutrient analyses of boƩom water discrete samples, sea urchin embryo development toxicity assays using SPE-concentrated site water, applicaƟon of the Salmonella typhimurium reverse mutaƟon assay (Ames test) for mutagenic acƟvity of SPE-concentrated site water, and analysis of foraminifera populaƟons as an indicator of stress. This study found 32 organic pollutants at detectable levels in the Bay. These were all at relaƟvely low concentraƟons that are unlikely to be of acute toxicological concern. With the excepƟon of nickel, sediment metal concentraƟons were below previously published Sediment Quality Guidelines, indicaƟ ng that toxicity to benthic infauna is unlikely. Laboratory toxicity tesƟng of Fagatele Bay samples did not show signifi cant toxicity using the sea urchin embryo development toxicity assay. None of the sample extracts analyzed exhibited mutagenicity via the Ames test (strains TA98 or TA100). Six out of ten water samples tested posiƟve for Escherichia coli, and all samples tested posiƟve for total coliform (Colitag test) demonstraƟng that mammalian (possibly human) or avian waste is reaching the Bay. Examining the populaƟon of benthic foraminifera (FoRAM Index) was not conclusive, perhaps because of the extremely coarse substrate which limited the number and variety of forams collected. Overall, these methods suggest that while some pollutants are reaching the Bay, the water quality of the system is relaƟvely good. Resource managers can use these data as a baseline to ensure that water quality does not degrade over Ɵme, and to be aware of specific pollutant groups (e.g. pharmaceuƟcals) that might be of emerging concern.
... Adaptación basada en Ecosistemas: alternativa para la gestión sostenible de los recursos marinos y costeros del Caribe Ambos índices (FoRAM y AMPHI) han sido muy empleando en el mundo (McField et al., 2007;Scheuth et al. 2008; Uthicke y Nobes 2008; Barbosa et al. 2009;Velázquez et al. 2011;Uthicke et al. , 2012. ...
Book
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Los ecosistemas marinos y costeros del Caribe garantizan la mayor parte de las actividades socioeconómicas que sostienen a más de 43 millones de personas. Esta región es altamente vulnerable a los impactos potenciales del cambio climático, principalmente los producidos por el incremento del nivel del mar y los efectos de eventos meteorológicos extremos como huracanes, fuertes lluvias o sequías intensas, y se encuentra también afectada por los cambios de hábitat, invasiones biológicas, sobreexplotación de los recursos marinos y costeros y la contaminación, que son presiones que ejerce el desarrollo descontrolado en las zonas marinas y costeras, cuyos efectos continuarán amplificándose por los impactos del cambio climático en la región. Para evitar la magnificación de los impactos asociados al cambio climático sobre los ecosistemas marinos y costeros y por tanto sobre el beneficio que recibe la sociedad caribeña de los servicios ecosistémicos que estos proveen, resulta imprescindible disminuir las presiones que el hombre ejerce sobre los ecosistemas fomentando para ello su resiliencia. La integración en planes de adaptación de las estrategias de conservación, rehabilitación ecológica y gestión sostenible a nivel local, nacional y regional deberá promoverse destacando el papel de los ecosistemas para la adaptación y mitigación al cambio climático, encaminando en una sola vía los vínculos entre diversidad biológica, cambio climático, reducción de desastres y desarrollo sostenible, lo que ha sido ampliamente reconocido como una necesidad a nivel mundial. La Adaptación basada en Ecosistemas (AbE) es una propuesta para construir resiliencia y reducir la vulnerabilidad de las comunidades al cambio climático, integrando justamente el uso sostenible de la biodiversidad y de los servicios ecosistémicos en una estrategia para ayudar a las personas a adaptarse al cambio climático considerando como puntos de partida tanto el conocimiento científico como el conocimiento comunitario local. La AbE propone que los ecosistemas pueden ser manejados para limitar los impactos del cambio implementando enfoques basados en el ecosistema para la adaptación que incluyan la gestión sostenible, la conservación y la rehabilitación de ecosistemas teniendo en cuenta los múltiples beneficios sociales, económicos y culturales para la sociedad. Para la implementación de la AbE en el Caribe resulta esencial prestar atención a temas como el incremento de la resiliencia a partir de la rehabilitación ecológica de arrecifes coralinos, manglares y playas, entre otros ecosistemas relevantes en esta región por su función como protectores de la costa, de la degradación de los suelos agrícolas y de la calidad del agua por la intrusión salina; al estudio, control y manejo de las invasiones biológicas y de nuevas y crecientes amenazas a estos ecosistemas posiblemente asociadas al cambio climático como las arribazones de sargazos a las costas caribeñas; y a la definición de mejoras en las herramientas esenciales para el manejo y gestión de la zona marina y costera como el planeamiento espacial marino, la elaboración de estrategias locales de adaptación, la evaluación de la vulnerabilidad ecológica y la evaluación de la salud de los ecosistemas, compartiendo experiencias a través de redes de intercambio como las redes CYTED. La profundización en estos temas contribuirá a la implementación de la AbE con una mirada hacia la naturaleza incluyendo al hombre, como una especie componente esencial del ecosistema, capaz de revertir la situación ambiental actual promoviendo la integración de voluntades, como una alternativa de convivencia entre el cambio climático y el bienestar socioeconómico para el desarrollo sostenible en la región caribeña
... A majority of the FI values obtained in the waters around Pulau Tioman were greater than 4, which indicate that the water quality is favorable for reef growth and recovery 8,14 . Despite the excellent performance of the FI in numerous studies 8,16,29,30 , Prazeres et al. 26 have raised some concerns on the application of this index in new study areas. ...
Article
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Pulau Tioman is a famous tourist island off Peninsular Malaysia with beautiful coral reefs. This study aims to assess the health of the coral reefs surrounding Pulau Tioman based on the application of the Foraminifera in Reef Assessment and Monitoring Index (FI). Ten sampling sites around Pulau Tioman were studied with a total of 30 samples. Eight orders, 41 families, 80 genera, and 161 species of benthic foraminifera were identified. The agglutinated type of foraminifera constituted 2–8% of the total assemblages. Calcareous hyaline and porcelaneous groups represented 79% and 19% of the total assemblages, respectively. Symbiont-bearing taxa were the most common foraminifera. The results indicate that most of the sampling sites are conducive for coral reef growth with good recoverability from future stress to the ecosystem. However, several areas with higher coastal development and tourism have reduced water and sediment quality. Therefore, the limit on the number of visitors and tourists should be revised to enable coral growth and health. The FI values in this study showed a positive correlation with good water qualities and a negative correlation with organic matter enrichment. The FI is a good measure to assess the health of a coral reef and can be applied to other reef ecosystems around Malaysia.
Article
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Mass mortalities due to disease outbreaks have recently affected major taxa in the oceans. For closely monitored groups like corals and marine mammals, reports of the frequency of epidemics and the number of new diseases have increased recently. A dramatic global increase in the severity of coral bleaching in 1997–98 is coincident with high El Niño temperatures. Such climate-mediated, physiological stresses may compromise host resistance and increase frequency of opportunistic diseases. Where documented, new diseases typically have emerged through host or range shifts of known pathogens. Both climate and human activities may have also accelerated global transport of species, bringing together pathogens and previously unexposed host populations.
Article
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The benthic communities of fringing and mushroom-shaped shallow-water reefs of the Abrolhos region (southern coast of Bahia) were surveyed. Line transects were used to estimate coral and algal percentage cover. Mussismilia braziliensis is the most conspicuous coral species in the majority of the communities surveyed, but turf algal make up the dominant cover in all but one studied reef. In general, communities on mushroom-shaped reefs have higher diversity and higher coral cover than on fringing reefs. For both reef morphologies, the coral to alga cover ratio does. not show marked differences between annual surveys, despite the high productivity characteristic of the dominant algal species.
Article
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The benthic communities of fringing and mushroom-shaped shallow-water reefs of the Abrolhos region (southern coast of Bahia) were surveyed. Line transects were used to estimate coral and algal percentage cover. Mussismilia braziliensis is the most conspicuous coral species in the majority of the communities surveyed, but turf algal make up the dominant cover in all but one studied reef. In general, communities on mushroom-shaped reefs have higher diversity and higher coral cover than on fringing reefs. For both reef morphologies, the coral to alga cover ratio does. not show marked differences between annual surveys, despite the high productivity characteristic of the dominant algal species.Foram estudadas comunidades bentônicas de pouca profundidade nos recifes em franja e chapeirões da região de Abrolhos (costa sul da Bahia). A cobertura das espécies foi estimada pelo método de transect de linha. Mussismilia braziliensis é a espécie de coral mais importante na maioria das comunidades estudadas, porém as algas em tufo são os organismos dominantes em todos os recifes estudados à exceção de apenas um. Em geral, as comunidades nos chapeirões têm maior diversidade e maior cobertura de coral do que as dos recifes em franja. Nos dois tipos de recife, a relação de cobertura coral-alga não apresenta diferença significativa no tempo, apesar da alta produtividade característica do tipo de alga dominante.
Article
Resumo Foram coletadas 54 amostras de sedimento superficial de fundo no litoral norte do Estado da Bahia, sendo dezesseis amostras na Praia do Forte, nove em Guarajuba, dezenove em Arembepe, e seis em Itapuã, com o objetivo de avaliar a fauna de foraminíferos e correlacionar sua distribuição com a textura e composição dos sedimentos. A fauna está distribuída em quatro tipos de substrato: (1) sedimento areno-biodetrítico, (2) sedimento areno-quartzoso, (3) sedimento de granulometria areia fina lamosa biodetrítica e (4) sedimentos carbonáticos onde ocorrem recifes de coral. A assembléia é bem diversificada em todos os substratos, porém nos substratos de areia fina e lama e no de recifes de coral, é onde há uma maior expressividade de espécies. A fauna é predominantemente bentônica, representada por 246 espécies, e a planctônica por dez espécies. As espécies dos macroforaminíferos Archaias angulatus, Peneroplis bradyi, Amphistegina gibbosa e Peneroplis carinatus foram consideradas importantes produtoras de areias carbonáticas. Palavras-Chaves: Foraminíferos, Tipo de substrato, Macroforaminíferos Abstract The foraminifera fauna from the bottom sediment of four areas (Itapuã, Arembepe, Guarajuba and Praia do Forte) from the North Coast of the State of Bahia was studied in order to verify its relationship with the type of substrate. Four major sediment types occur in the investigated areas: 1) biogenic sand; 2) quartz sand; 3) muddy biogenic sand and 4) coarse reefal carbonate. The identified fauna is dominantly composed of benthonic forms, having 246 species, and the planctonic fauna is represented by ten species. The bottom substrates composed of muddy fine sand and reefal carbonates are the ones that have the highest foraminiferal diversity. The macroforaminifera Archaias angulatus, Peneroplis bradyi, Amphistegina gibbosa and Peneroplis carinatus are the species that most contribute to the production of carbonate sediments.