Journal of Foraminiferal Research, v. 42, no. 2, p. 169–183, April 2012
FORAMINIFER-BASED CORAL REEF HEALTH ASSESSMENT FOR SOUTHWESTERN
ATLANTIC OFFSHORE ARCHIPELAGOS, BRAZIL
CÁTIA F. BARBOSA1,5, BEATRICE P. FERREIRA2, JOSÉ CARLOS S. SEOANE3, PATRICIA OLIVEIRA-SILVA1, ANA LIDIA B.
GASPAR1, RENATO C. CORDEIRO1 AND ABILIO SOARES-GOMES4
environmental change, leading to replacement of species.
These changes results in economic losses in oligotrophic
areas, where coral reefs are responsible for biodiversity
maintenance. Most ecologic models predict a substantial
time lag between loss of habitat and species extinction in
coral reefs, which indicates that low-diversity regions are
especially vulnerable to damage (Knowlton, 2001). In a
long term global study, Kiessling (2005) found that above
average species diversity during one time interval led to
below average changes in reef ecology in the next.
Decline of tropical biodiversity in coral reefs, seagrass
beds, mangroves, and shelf environments associated with
corals has been observed worldwide. True coral reefs, algaldominated reefs, and beachrock-sand reefs are distributed
along 3,000 km of the Brazilian coast, where 23 species of
stony corals and five species of hydrocorals are found.
Eighteen coral and four hydrocoral species occur in eastern
Brazilian reefs (Leão and others, 2010). Of these, six are
endemic to the western South Atlantic, some have affinities
with Caribbean corals, and some are remnants of a relict
fauna dating back to the Tertiary. The latter probably
survived during Pleistocene sea-level low stands in a refuge
provided by the sea mounts off the Abrolhos Bank (Leão
and others, 2003), reflecting the vulnerability of South
Atlantic coral reef environments and biodiversity. Currently, it is important to establish threshold levels for key reef
micro- and macroorganisms and to assess changing trends
in abundance and dominance, preferably using standardized monitoring methods.
To monitor coral reef environments, it is necessary to
integrate bioindicators which can link reef health to
environmental data derived from remote sensing techniques, water quality measurements, benthic community
status, and others (Hallock and others, 2004). Benthic
foraminifers are cosmopolitan, diverse, small, and abundant, and include species with different stress tolerances.
Therefore, they are high-priority bioindicators for use in
long- and short-term monitoring programs (Cooper and
others, 2009), and also present a good cost-benefit ratio for
these programs (e.g., Schafer, 2000). The foraminifers’
shorter life cycle relative to that of reef-building corals
allows differentiating between short-term stress events and
long-term decline in water quality, and the composition of
foraminiferal assemblages preserved in the sediment can
indicate whether the community has changed (Cockey and
others, 1996; Hallock, 2000a, 2000b; Ishman, 2000).
Hallock and others (2003) developed the Foraminifera in
Reef Assessment and Monitoring (FORAM) Index or FI,
which uses foraminifers to evaluate coral-reef water quality.
The aim of this study, then, was to test the applicability
of taphonomy and counts of living specimens of Amphistegina spp., the FI (which is based on total foraminiferal
counts), and coral-cover percentages through time to
ABSTRACT
Benthic foraminiferal assemblages can indicate the ecological status of coral-reef ecosystems. Their functional groups
have been used to calculate the previously published FORAM
Index (FI), which is based on total counts (living and dead) to
indicate whether an environment is suitable to support prolific
calcification by organisms that are dependent upon algal
endosymbionts. Sediment was sampled from the Archipelago
of Fernando de Noronha and the Abrolhos Archipelago and
Parcel, which harbor important coral reef communities off the
NE and E coasts of Brazil. Quantifying live specimens and
taphonomic features of Amphistegina spp., along with the FI
in 2005 and monitoring of the percentage of coral cover from
2002–2009, provided an assessment of coral reef health,
which was mapped for both areas. Results indicated that FI
was good (.4) in half of the sampled stations, but no living
Amphistegina was found in the Abrolhos Archipelago and
Parcel, possibly indicating recently unfavorable conditions
there. These findings suggest that palimpsest sediment can
disguise FI so that, in some cases, the index fails to correlate
with coral cover. A more realistic approach can be obtained
by using the living counts of Amphistegina and their
taphonomy to augment the ecological results from the FI.
INTRODUCTION
The stress tolerance and regeneration capacity of coral
reef populations to impacts caused by agents mainly related
to sea-surface temperatures (SST) has been a concern of the
scientific community, given that climatic changes are likely
to continue in the near future (Berkelmans and Willis, 1999;
Hendy and others, 2003; Pandolfi and others, 2003;
McClanahan and others, 2005; Thornhill and others,
2006; Bruno and Selig, 2007). Indeed, the link between
greenhouse gases, climate change, and the regional-scale
bleaching of corals, which many reef researchers questioned
previously, is now incontrovertible (Hoegh-Guldberg, 1999;
Watson and others, 2001; Hughes and others, 2003).
In many cases, the regenerative capacity of corals does
not compensate for the intensity and frequency of
1
Departamento de Geoquı́mica, Universidade Federal Fluminense,
Outeiro de São João Batista, s/no., Niterói, Rio de Janeiro, CEP: 24020141, Brazil
2
Departamento de Oceanografia, Universidade Federal de Pernambuco, Av. Arquitetura s/no., Cidade Universitária, Recife, Pernambuco,
CEP: 50670-901, Brazil
3
Departamento de Geologia, Universidade Federal do Rio de
Janeiro, Av. Athos da Silveira Ramos 274, CCMN, Bloco G, Rio de
Janeiro, R. J., CEP: 21941-916, Brazil
4
Departamento de Biologia Marinha, Universidade Federal Fluminense, Outeiro de São João Batista, s/no., Niterói, Rio de Janeiro, CEP:
24020-141, Brazil.
5
Corresponding author. E-mail: [email protected]
169
170
BARBOSA AND OTHERS
FIGURE 1. a South Atlantic Ocean circulation patterns: sSEC (southern branch of the South Equatorial Current), NBC and NBUC (North Brazil
Current and Undercurrent), BC (Brazil Current) and cSEC (central South Equatorial Current); adapted from Schott and others (2005). b Locations
of FN and AB and the states of Pernambuco (PE) and Bahia (BA). c, d Sampling stations and depth for FN and ABa (islands in yellow) and Parcel
ABp (light blue shallow area to the east). Filled triangles are foraminiferal sampling sites; open triangles are Reef Check survey sites; filled and open
triangles are both foraminiferal sampling and Reef Check survey sites.
determine the health of coral reefs at sites monitored by the
Brazilian National Coral Reef Monitoring Program.
MATERIAL AND METHODS
STUDY AREAS
The present study encompasses the Archipelago of
Fernando de Noronha (FN), and the Abrolhos Archipelago
(ABa) and Parcel (ABp) off the NE and E coasts of Brazil
(Fig. 1a–d). These areas comprise the largest coral reefs in
the southwestern Atlantic, and are either partially (FN) or
entirely (ABa and ABp, collectively termed AB) protected
as national marine parks under federal legislation that
minimizes human activity.
Coral communities in these three areas are substantially
different. The FN is composed of Miocene-Pliocene volcanics, which do not support true coral reefs, although nine
hermatypic coral species occur there on a rocky substrate,
under clear waters and high hydrodynamic conditions
(Almeida, 2000). The AB, constructed of Paleocene-Eocene
volcanics and subsequent extensive carbonate deposition,
has the highest diversity of coral reefs in the southwestern
Atlantic. Fringing reefs surround the ABa islands, located
,60 km from the continent. Coral reefs that border the ABp
are characterized by a goblet-like morphology known as
‘‘chapeirões’’ (Hartt, 1870), and form an outer arc located
,70 km from the mainland, where recruitment and
maximum coral growth occur (Leão and others, 2003). They
are remnants of an extensive carbonate paleo-platform that
was severely eroded by lower sea-level stands (Knoppers and
others, 1999).
All the reefs are influenced by western boundary currents
of the tropical South Atlantic (Figs. 1a, b). The FN is affected
by the central part of the South Equatorial Current (cSEC)
and the North Brazil Current and Undercurrent (NBCNBUC) that brings warm and salty water. The southern
branch of the South Equatorial Current (sSEC) bifurcates
and becomes the North Brazil Undercurrent (NBUC), which
goes across the equator into the Northern Hemisphere
(Stramma and Schott, 1999; Stramma and others, 2005;
Rodrigues and others, 2007; Silva and others, 2009). Another
FORAMINIFER-BASED CORAL HEALTH
branch flows southward and merges into the Brazil Current
(BC) as part of the South Atlantic gyre system. The AB is
influenced by the warm, saline, and nutrient-poor waters of
the BC.
DATA SAMPLING AND SURVEYS
Sediments from both FN and AB were sampled by
SCUBA diving during the austral summer and winter of
2005. The ABa and ABp have very different reef
morphologies, but because they are within 10 km of one
another, they were sampled together (Fig. 1d). Here we
sampled the bottom sediment of chapeirão structures at the
border of the ABp. A sample consists of an ,50-g aliquot
collected for foraminfers, and an ,250-g aliquot for grain
size, carbonate, and organic matter analysis, along three
depth-orthogonal transects. Three stations were sampled on
each transect at depths of 2–6 m (here labeled 6), 6–12 m
(labeled 12), and 12–20 m (labeled 20), providing 18
sampling stations and 36 samples (Figs. 1c, d).
The depth at each station was recorded from a diving
computer. The foraminiferal samples were fixed in the field
using a solution of 4% formaldehyde buffered by 10 g of
sodium tetraborate (Na2B4O7) (Boltovskoy, 1965), and
stained with rose Bengal (1 g/l21) to distinguish between
living (stained) and dead (unstained) protoplasm (Murray,
2006).
Coral-cover data were obtained from the Brazilian
National Coral Reef Monitoring Program, which uses a
Reef Check-based protocol (Ferreira and others, 2004). At
each of the reef monitoring program sites four replicate 40point-intercept transects were surveyed in 2002, 2005, and
2007. Both scleractinean and milleporid species were
grouped as mean hard-coral cover in the survey. Low coral
coverage was considered to be #10%, medium coverage
.10–25%, and high coverage .25%, as most of the
healthiest reefs in the world have probably never had more
than about 30% coverage (Hodgson and Liebeler, 2002). In
general these coral-reef sites (labeled by name) were not
sampled for foraminifers, with the exception of Dois Irmãos
in FN, labeled as station 2-20 (Figs. 1c, 2), and Chapeirão
do Pierre in ABp, labeled as 3-20 (Figs. 1d, 3).
LABORATORY ANALYSIS
Foraminifers
Benthic foraminiferal samples were standardized from a
gross weight of 10 g/sample, washed over a 63-mm mesh
sieve, and dried at 50uC. The weight-split samples contained
.150 individuals/sample that were examined under a
stereomicroscope to separate living and dead specimens
(Hallock and others, 2003). Specimens were considered
living when stained protoplasm was spread evenly throughout the test (Duchemin and others, 2007). Because the
number of living individuals was negligible, only total
counts, rather than ones based on living and dead
categories were used in calculations.
Murray (2006) considered total numbers to be an arbitrary
mixture of living and dead specimens and preferred living
assemblages to be the primary indicators in ecological
171
studies. However, dead assemblages have the potential to
yield information about both the long-term contribution of
foraminiferal tests to the sediment and the effects of
taphonomic alteration. In this study ‘‘optimally preserved,’’
unstained (i.e., dead) specimens were considered to be good
representatives of the present-day biocoenosis (Yordanova
and Hohenegger, 2002).
Taphonomic patterns were analyzed only for Amphistegina spp. because it is the most representative of the larger
symbiont-bearing foraminifers found in this study. Identified
species include A. gibbosa d’Orbigny, 1839, A. lessonii sensu
Parker, Jones, and Brady, 1865 (rare), and A. papillosa Said,
1949 (rare), hereafter referred to collectively as Amphistegina.
They were separated into living (stained protoplasm) and
dead, with the latter divided into intact white tests with no
protoplasm, deformed (defined as genetic and/or broken and
repaired while growing), and broken (any post-mortem shell
damage).
Foraminifers were quantified by the FI developed by
Hallock and others (2003), which can reflect water-quality
conditions. For this calculation, the specimens were sorted
by genera among three functional groups (symbiont-bearing,
stress-tolerant, and other small taxa), and a ratio was
calculated for each group using the number of specimens of
that group divided by the total number of specimens counted
in each sample. The proportions were weighted to calculate
the FI:
FI~ð10|PsÞzðPoÞzð2|PhÞ
ð1Þ
where Ps, Po, and Ph represent the proportion of symbiontbearing, stress-tolerant, and other smaller species, respectively (Barbosa and others, 2009; Carnahan and others,
2009). Given the faster turnover rates of smaller taxa, water
quality must be sufficiently nutrient-poor on average for the
tests of symbiont-bearing taxa to make up at least 25% of the
foraminiferal assemblage. Therefore, if the FI is .4, water
quality should support calcifying mixotrophs (Hallock and
others, 2003; Carnahan and others, 2008), whereas FI values
between 2–4 represent marginal conditions for calcifying
mixotrophs, meaning that coral communities may exist but
any damage will not likely be followed by recovery.
Biofacies distribution mapping was done using GIS on a
1:25,000 scale. Nautical charts of the Brazilian navy were
used for navigation with field points taken by Wide Area
Augmentation System (WAAS)-enhanced GPS. Mapped
themes are limited by influence areas (Appendix 1) and
obtained from the interpolation of sampling points using an
Inverse Distance Weighed (IDW) algorithm, where weight
is power selected to better represent spatial variability. In
general, when the power is larger, the influence of distant
points’ values is less. The square of the distance was used
for the AB, whereas the fourth power was used for FN.
Sediment
Grain size was analyzed using a 3 g gross-weight aliquot of
sediment washed on a 500-mm mesh screen; fine particle
composition was determined with a Cilas 1064 laser analyzer.
Only a few shell fragments coarser than the 500 mm mesh
were encountered and discarded. The sedimentary parameters were determined by Gradistat routine (Blott and Pye,
172
BARBOSA AND OTHERS
FIGURE 2. Taphonomic conditions of Amphistegina spp. at Fernando de Noronha (pie charts), FORAM index (interpolated surface), and coral
and algal cover (histograms). a Austral summer. b Austral winter. Station markings as in Figure 1.
FORAMINIFER-BASED CORAL HEALTH
173
FIGURE 3. Taphonomic conditions of Amphistegina spp. (pie charts), FORAM index (interpolated surface), and coral and algal cover
(histograms) in the Abrolhos Archipelago islands (center in yellow) and Parcel border (chapeirões) to the east. a Austral summer. b Austral winter.
Station markings as in Figure 1.
174
BARBOSA AND OTHERS
2001) using Folk and Ward graphical methods for statistical
calculations.
Calcium carbonate concentration was determined by
acidifying the sediment with 1M HCl (Loring and Rantala,
1992). The organic matter (OM) was obtained from the
standardized weighed gross-wet samples, which were dried at
60uC, weighed again after 72 h, and subsequently subjected
to ignition in a muffle furnace at 450uC for 10 h (Müller,
1967).
Data Analysis
Foraminiferal distributional patterns were calculated by
using the number of genera (S), number of specimens (N),
diversity [index of Shannon, H95 2SUM (p*Log(p)) using
Loge], evenness [e‘H/S], and dominance [sum((ni/n)2) where
ni is number of individuals of taxon i] using PAST software
(Hammer and others, 2001).
To examine the grouping of faunal density among all sites
and sampling periods, an analysis of multidimensional
scaling (MDS) was carried out using Bray-Curtis similarity
matrices on faunal-density data that were square-root
transformed (truncated to include only the genera that
contribute at least 4% of the total abundance in at least one
sample). An analysis of similarity percentage (SIMPER)
determined which species were primarily responsible for the
grouping. The distributional patterns were tested using the
two-way crossed analysis of similarities (ANOSIM, Clarke
and Gorley, 2006) to determine if assemblage-averaged
densities varied among the three different bathymetries (6,
12, and 20 m) and sampling periods (summer and winter).
The two-way ANOVA (STATISTICA software) was
employed to test differences in the mean densities of living
and non-living Amphistegina among sites and sampling
periods. Prior to the analysis, data were tested for normality
and homogeneity of variances. First, the mean density of
total dead categories (intact white, broken, and deformed)
were analyzed between sampling periods (summer and
winter) for both the FN and AB, but density measurements
on living specimens were performed only for FN collections, as no living individuals were found at AB.
Annual mean coral and algal cover for each location from
both sites is represented by box-whisker plots. Inter-annual
variation was checked by the Kruskall-Wallis nonparametric test (Siegel and Castellan, 1988, in STATISTICA) for sites surveyed every year at FN, including Ze
Ramos, Sancho, and Dois Irmãos (5 station 2-20) (Fig. 1c),
and at ABa (station 1-6) and ABp (Debora) (Fig. 1d).
Significance was considered at p , 0.05.
RESULTS
FERNANDO DE NORONHA
Ninety-eight genera were identified in the 18 stations
sampled at FN in 2005 (Appendix 2), with Amphistegina as
the dominant large benthic foraminifer (LBF) at all sites.
Live Amphistegina specimens were found during both the
summer and winter sampling periods (Figs. 1c, 2a, b).
Taphonomic mapping of dead specimens revealed seasonal
differences in Amphistegina density (pie graphs in Figs. 2a,
b) and the FI (colored bottom surface in Figs. 2a, b), and
illustrates the hydrodynamic influence on these results.
However, taphonomic patterns for Amphistegina showed
no statistical seasonal difference (p 5 0.35; f 5 0.90), but
there were significant differences between living and nonliving populations (p 5 0.0075; f 5 8.13), with significance
,0.01 based on 173 living individuals out of a total of 1,332
specimens (i.e., 13% live).
SIMPER analysis revealed that Amphistegina was the
dominant genus, contributing from 11–35% of the total
foraminiferal fauna (Appendix 3). The next most abundant
genera were the smaller heterotrophic Quinqueloculina and
stress-tolerant Elphidium; their variability was responsible
for the high dissimilarity among sites. SIMPER groups ‘‘a’’
and ‘‘b’’ were the least similar (Appendix 3). The multidimensional scaling plot (Fig. 4) provides an excellent
representation of the sample groupings (Stress: 0.04). The
‘‘a’’ assemblage was a) by far of the lowest density, b)
characterized by relatively few genera, c) strongly dominated by Amphistegina, and d) found at the northeasternmost shallow site (1-6). The ‘‘b’’ assemblage was much
more diverse and abundant than ‘‘a,’’ with more than twice
as many genera and 50–1003 more tests/10 g. The ‘‘b’’
assemblage was found at the southwestern sites (transect 3)
and the northeasternmost deep site (1-20). Assemblages in
sample groups ‘‘c,’’ ‘‘d,’’ and ‘‘e’’ were intermediate in both
diversity and density between those extremes (Fig. 4), and
were found at site 1-12 and at all sites of transect 2, which is
in the vicinity of the assessed coral reef sites. Foraminiferal
densities showed no significant difference among all depths
(average across all time periods, ANOSIM2: Global R 5
20.08, p # 71.5%), and were not altered seasonally either
(averaged across depths, ANOSIM2: Global R 5 20.27,
p # 94.5%).
The mean number of genera grouped by station depth
increases with bathymetry for both summer and winter,
while the mean number of individuals does not significantly
vary between seasons, maintaining the homogeneity of the
assemblage. Mean values of dominance are high for shallow
sites during summer and are negatively correlated to
evenness, i.e., the latter is lower for shallower depths. In
winter, dominance and evenness are also negatively correlated (Fig. 5).
In the 2005 samples, FI . 4 was recorded for fully half the
stations, indicating that water quality should support coral
growth and recovery from impacts. For the other half, FI
values ranged from 2.8–4.0, indicating that water quality
should support coral growth but may be marginal for
recruitment following mortality events. Values of FI ,3 were
recorded only at the deepest station of transect 2 in summer
and the shallowest of transect 3 in winter (Appendix 2).
Hard coral and algal cover (yearly average for 2002–
2008) were relatively high at all stations in the vicinity of
transect 2 (Figs. 2, 6a), with 38% at Ze Ramos, 53% at
Sancho, and 30% at Laje Dois Irmãos (station 2-20). No
significant differences were found in mean coral cover
among these years for those sites (KW of p 5 0.2204, p 5
0.7114, and p 5 0.079, respectively).
Mean grain size (Fig. 7A) was relatively homogenous
with values #4W for the majority of samples in both
sampling periods with the exception of 1w20 (.7W) and
3s20 (.8W). These deep stations (1-20 and 3-20) showed an
FORAMINIFER-BASED CORAL HEALTH
175
FIGURE 4. Multi-dimensional scaling (MDS) of Fernando de Noronha faunal assemblages by depth. Sampling stations shown in Figure 1c; s 5
austral summer, w 5 austral winter.
FIGURE 5. Box-whisker plots of foraminiferal faunal patterns for Fernando de Noronha and Abrolhos data sets, showing mean values by depth
transects for summer and winter.
176
BARBOSA AND OTHERS
FIGURE 6. Box-whisker plots of mean hard coral and algal cover percentages for the years 2002–2008 at Fernando de Noronha stations Laje Dois
Irmãos (5 2-20), Sancho, and Ze Ramos; and for 2002–2009 at Abrolhos Archipelago and Parcel stations Chapeirão (5 station 3-20), Abrolhos-04,
Barracuda, Debora, and 3-20. Sampling stations located in Figures 1c, d.
inversion of mud and sand between sampling periods.
Organic matter (OM) was higher in the winter than in the
summer for most of the stations, with the exception of
stations 2-12 and 3-6 (Fig. 7B). Carbonate was high with
the exception of station 3-6 (Fig. 7C).
ABROLHOS ARCHIPELAGO AND PARCEL
Due to the proximity of ABa and ABp, results of their
sampling programs are presented in the same figures and
appendices. The ANOVA two-way results comparing total
dead categories (intact white, broken, and deformed)
FIGURE 7. Sedimentologic variables measured at each station of Fernando de Noronha (A–C) and Abrolhos Archipelago and Parcel (D–F)
during the austral summer (s) and winter (w) of 2005. A, D—Grain size (W units); B, E—Organic matter percentages; C, F—Carbonate percentages.
FORAMINIFER-BASED CORAL HEALTH
177
FIGURE 8. Multi-dimensional scaling (MDS) of Abrolhos faunal assemblages by depth. Sampling stations shown in Figure 1d; s 5 austral
summer, w 5 austral winter.
showed that there were no significant differences between
AB and FN (p 5 0.34; f 5 0.92), even when comparing
total dead between summer and winter (p 5 0.75; f 5 0.99).
No living Amphistegina was found during either sampling
period in AB, and high proportions of the dead tests were
broken and deformed (Fig. 3, Appendix 4). The dominant
foraminifers at all sites in AB were Quinqueloculina spp.,
contributing 22–38% of the total foraminiferal fauna as
revealed by SIMPER analysis (Appendices 4, 5). The next
most abundant were symbiont-bearing representatives of
Archaias, Peneroplis, and Amphistegina. Quinqueloculina is
also responsible for much of the dissimilarity among sites
(Appendix 5). The multi-dimensional scaling plot (Fig. 8)
provides an excellent representation of the sample groupings
(Stress: 0.07), with groups ‘‘a’’ and ‘‘b’’ the most dissimilar
and groups ‘‘c–g’’ at intermediate distances. Assemblage
‘‘a,’’ found at the shallow site 1-6, had low diversities of
mostly symbiont-bearing genera. The ‘‘b’’ assemblage was
dominated by miliolids with the highest abundances by far at
sites 1s12 and 3s20. Groups ‘‘c,’’ ‘‘d,’’ ‘‘f,’’ and ‘‘g’’ were also
dominated by Quinqueloculina, but with the symbiontbearing genera as important contributors (Appendix 5).
The number of individuals/10 g sample was highly variable
between stations, with no significant seasonal trends [Friedman ANOVA values (X2 (N 5 19, df 5 1) 5 0.22 p , .637)
and Kendall Coefficient of Concordance of .011 Average r
rank of 20.0432]. Comparisons of foraminiferal densities by
stations of equal depth have no comparable means for
summer and winter transects, except for the summer 6-m
bathymetries (One-Way ANOVA, p # 0.05).
The mean number of genera grouped by station depth
increases with bathymetry in summer. Specimen numbers
are higher in summer than in winter, with high standard
deviation of mean values for deeper sites. Mean diversity
values increase with depth in both seasons, while dominance decreases with depth and is negatively correlated
(Fig. 5). Evenness increases with depth in summer and is
stable in the winter.
At AB more than half of the FI is .4.0, with the majority
of lower values found in summer (Appendix 4). The three
highest FI values (6.8, 8.9, and 9.1) were found at site 1-6 in
both seasons and 1-12 in winter.
Mean hard coral cover for ABa (data from 2002–2009)
and for ABp (data from 2002–2007) included 13% for
station 1-6 and 17% for 3-6 and 2-6. Higher coral cover was
found in ABp at Abrolhos 04 (27%), station 3-20 (30%),
Debora (33%), and Barracuda (36%) (Figs. 3, 6b, c). For
ABa no variation in coral cover was found for all years at
station 1-6 (KW, p 5 0.4063), but a significant increase
between years was observed for the ABp Debora and
Chapeirão (5 3-20) sites (KW, p 5 0.0152).
Mean sand-grain size (0-2W) was homogeneous for both
sampling periods, except at stations 1-20 and 2-12 at ABa,
where mud (.4W) was found in summer, and at harbor
station 1-6, which yielded silt in both seasons (Fig. 7D).
Low OM values were found for both sampling periods
except for station 1-20 and all stations of transect 3 in
winter with values .5% (Fig. 7E). Carbonate concentration in sediments was high in both seasons (from 55–93%)
with the exception of station 3-6 (Fig. 7F).
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BARBOSA AND OTHERS
DISCUSSION
CORAL REEF ENVIRONMENTS
The biological and economic significance of the coral
communities of Fernando de Noronha and the coral reefs
of the Abrolhos Archipelago and Parcel are reflected in
their protection as national marine parks. Thus, methods
for assessment and protection of their water quality are of
critical interest to park management. The precipitous
decline of coral cover, which has been well documented in
the northwestern Caribbean (e.g., Palandro and others,
2008), has not been observed in these Brazilian reefs. It is
possible that coral reefs in Brazil are adapted to very
dynamic environmental processes. Leão and others (2008)
suggested that nearshore corals exposed to high nutrient
flux and sediment loads, as well as to large sea-surface
temperature fluctuations, may be more resistant to coral
bleaching and to post-bleaching effects such as infectious
diseases and mass mortality.
High mean coral cover was observed at FN and ABp but
not at ABa. Francini-Filho and others (2008) reported
white plague diseases on Mussismilia braziliensis Verrill,
1867, (Laborel, 1969) at ABa beginning in January 2005,
after which coral cover tended to decrease. Coral cover at
ABa reefs has declined more over recent decades than in the
coral communities at FN and ABp, possibly indicating
more susceptibility to environmental degradation. Although easy to measure, coral cover is not always the best
indicator of coral-reef health (Smith and others, 2004;
Cooper and others, 2009). Water transparency is strongly
related to water quality; FN has more transparent water
(mean vertical visibility of 9.8 m) than AB (mean of 5.6 m).
However, in recent years, coral cover in the Florida reef
tract, U.S.A., and elsewhere has declined most precipitously
in the clearest waters (e.g., Palandro and others, 2008). In
general, coral cover was relatively stable at all sites for the
years analyzed with the exception of ABp, where coral
cover increased in the last two years.
The seasonal depositional regime at FN is influenced by
trade winds and the NE-SW orientation of the volcanic
archipelago. The north shore receives North Atlantic swells
during summer, generating long-shore transport in a
southwesterly direction. Conversely, in winter the south
shore receives South Atlantic swells, transporting fine
sediment to the northeast where waning eastern trade winds
promote deposition along the NE shore. Strong oceanic
currents influence sponge occurrences at the NE and SW
extremes of FN (Moraes, 2011) and also the foraminiferal
densities of transects 1 and 3, clearly separated on the multidimensional scaling plot (Fig. 4)
In the Abrolhos, the Brazil Current, adjacent to the
Brazilian coastline, washes the shelf with a southward flow
of warm, nutrient-poor waters. The current is narrow
(,75 km wide) and limited to the upper 500 m of the water
column (Miranda and Castro, 1981), with meridional
velocities ranging between 10–20 cm21 (Silva and others,
2009). During winter, central South Atlantic currents bring
the coldest water of the year to the archipelago.
The percentage of calcium carbonate and sand-sized grains
was generally high, with little seasonal variance in either area.
However, lower carbonate percentages were found at the
same shallow stations where fine-grained sediment predominated and high OM occurred, with no significant seasonal
differences. Such conditions can greatly influence coral reef
health, promoting stress for ABa coral populations.
FORAMINIFERAL ASSEMBLAGES
A total of 155 foraminiferal genera were identified
between the two study areas. Of these, 13 were assigned
to the functional group of stress-tolerant foraminifers, 10 to
symbiont-bearing, and 132 to other small heterotrophic
taxa. More genera were found at AB (112) than at FN (98).
The highest diversity values were found during summer at
the 20 m depth in both areas (Fig. 5). The lowest diversity
values for both areas were found at 6 m depths, with high
dominance and low evenness determined by the symbiontbearing species at the shallow sites in both FN and AB
(Fig. 5). Foraminiferal assemblages show species homogeneity intra-location and no seasonality under MDS
analysis. Assemblages of Amphistegina, Quinqueloculina,
and Elphidium were dominant at FN compared to AB,
where only dead Amphistegina was found in lower densities.
Quinqueloculina, Archaias, and Peneroplis dominated AB.
The fact that both areas had many genera in common, with
no significant seasonal variation, is expected because most
of these genera have circumtropical distributions.
Among symbiont-bearing foraminifers, Amphistegina is
often the best indicator of water-quality status for coral
reefs and algae in warm-water coastal environments.
(Triantaphyllou and others, 2005, 2009). In spite of high
wave energy on the reef front (Fig. 1c, transect 2) along the
FN north shore in summer, living Amphistegina were found
in both sampling seasons near sites of high coral cover.
Higher living test densities, however, occurred in winter
(Fig. 2) when wave energy is reduced on the north shore, in
agreement with Fujita and others (2009), who showed that
this genus has lower tolerance to water motion. At ABa,
which lacked living Amphistegina, the density of broken
tests increased in winter as tests can be swept toward
protected sites (e.g., station 1-6) along the south shores of
the islands. This movement facilitates the long-term
contribution of Amphistegina and other foraminiferal tests
to the palimpsest carbonate sediment (Fig. 3).
The most abundant genus at AB was Quinqueloculina, as
Araújo and Machado (2008) also found, but contrary to
Sanches and others (1995), who reported symbiont-bearing
species to be dominant. The increase in Quinqueloculina
numbers and size (Boltovskoy, 1964) over the past 15 years
may be related to the genus’s opaque, porcelaneous test,
which can be less susceptible to changes in solar radiance than
that of hyaline foraminifers, permitting species to thrive in
shallow waters exposed to wave- and tide-related turbidity.
Similarly, the most abundant symbiont-bearing foraminifers
in AB, Archaias and Peneroplis, are also porcelaneous taxa.
Their presence can indicate high carbonate saturation in
seawater and high solar irradiance (Baker and other, 2009).
Elphidium was common in both areas, with percentages
.4% for all FN stations (with the exception of FN3s12)
and for 13 of 18 AB stations. Representatives of this genus
span a variety of functional possibilities. Some species are
179
FORAMINIFER-BASED CORAL HEALTH
stress tolerant, adapted to low light and oxygen (Bernhard
and Sen Gupta, 1999) and to higher nutrient levels and
euryhaline conditions (Uthicke and Nobes, 2008). They can
also thrive with other smaller forms or with the symbiontbearers, as Elphidium can sequester chloroplasts (Bernhard
and Bowser, 1999; Uthicke and Nobes, 2008). These
adaptations give Elphidium an ecological advantage in
fluctuating environments (Sharifi and others, 1991; Yanko
and others, 1999; Carnahan and others, 2009), but make its
placement in the FI equation problematic, as noted by
Carnahan and others (2009). The latter authors found that
Elphidium clustered with the other smaller taxa in data from
Biscayne Bay, Florida, though its location in the resulting
MDS plot was relatively close to the stress-tolerant cluster.
They also reported that, in a preliminary study of a subset
of their data, Elphidium clustered with the clearly stresstolerant Ammonia.
FORAM INDEX
Mean FI values across all stations for both sampling
periods were 4.62+/21.85 and 4.46+/21.2 for AB and FN,
respectively, and no statistical difference was detected by a
t-test (p , 0.05), which indicates water quality generally
suitable for calcifying symbioses in both regions. These
averages, although comparable, are slightly higher than the
4.1 Ramirez and others (2008) found in Biscayne National
Park in Florida; coral cover is also higher in both AB and
FN (Figs. 2, 3) than in Biscayne National Park (Dupont
and others, 2008, and references therein).
The FI has already been applied to Atlantic coastal
environments (Hallock and others, 2003; Carnahan and
others, 2008; Ramirez and others, 2008; Barbosa and others,
2009) and the Great Barrier Reef (Schueth and Frank, 2008;
Uthicke and Nobes, 2008; Narayan and Pandolfi, 2010;
Uthicke and others, 2010), as well as in saltwater aquaria
(Ernst and others, 2011). At all these sites, the FI achieves
good results in describing the health status of the environment, although some adjustments are needed to compensate
for local conditions.
At AB, FI ,4 occurred at 80% of the stations during
austral summer (Appendix 4). In fact, the lower FI values,
reflecting the higher abundance and diversity of smaller
foraminifers, provide indicators of seasonal environmental
changes that could predict future problems for the AB reefs.
Higher indices at shallow depths at both FN and AB,
where wave-influenced shadow zones facilitate test accumulation and resuspension, are considered results of relict
sediments. This is also implied by the taphonomy, although
Archaias and Peneroplis are common in shallow reef-flat
environments elsewhere (e.g., Baker and others, 2009). Boat
activity in shallow harbors can create local eutrophic
conditions (Schueth and Frank, 2008) that favor growth
of heterotrophic smaller foraminifers. No living Amphistegina was found at any harbor site where carbonate silt was
predominant.
At ABp station 3-20, which had the lowest FI in both
sampling periods, coral cover and reef morphology are very
different from where the FI has been applied previously. The
characteristic mushroom shape of the chapeirões sustains
healthy corals on the top, whereas the fine bottom sediments
shaded beneath these structures contain relatively high levels
of organic matter that favor the heterotrophic smaller taxa
rather than symbiont-bearing larger foraminifers. In fact,
despite the substantial coral cover on the chapeirões, the
sediment beneath them is currently unfavorable for coral
recruitment, as no hard substrate is available.
The FI provided a reliable proxy for water quality and
reef health at FN, but may not be suitable for the atypical
sedimentary habitats found under chapeirões in AB. The
occurrence of only dead Amphistegina tests at ABp station
3-20 illustrates that these foraminifers either fell off the top
of the chapeirões upon death or were transported to the
site by currents. High FI values for the more vulnerable
ABa sites may indeed reflect palimpsest sediments under
seasonal hydrodynamic conditions.
Introducing living counts of foraminiferal functional
groups into the FI formula (equation 1) might improve the
applicability of FI as an ecological monitoring index by
assessing water quality from the sediment assemblage at the
time of sampling. However, since living specimens typically
make up only about 10–15% of the assemblage in sediment
samples, distinguishing and identifying adequate numbers
of them can require as much as 5–103 more time, greatly
increasing the cost of sample analysis. Moreover, because
many of the characteristic reef-associated species primarily
live on hard or phytal substrates rather than in sediments,
the living assemblage in the sediments may not reflect
environmental conditions for calcifying symbioses. Care
should be taken to assess relatively ‘‘fresh-appearing’’ tests,
even if broken, and to disregard degraded tests.
CONCLUSIONS
Foraminiferal assemblages in Brazilian coral reef environments were tested to determine if the FORAM Index (FI)
indicates that water quality supports benthic communities of
calcifying symbionts, and the results were correlated to coral
cover data available at sampled sites. In Fernando de
Noronha (FN), risk areas appeared at the southwestern
and northeastern ends of the north shore of the main island.
High FI values were associated with the best coral cover over
the volcanic rock platform along transect 2 (Fig. 1c), whereas
the lowest values were found in the harbor area (station 1-6)
where corals were sparse. The FI data in the Abrolhos (ABa)
indicated a healthy status for nearshore stations; however,
the absence of living Amphistegina specimens and its
taphonomy showed that coral communities may be at risk,
as also indicated by hard coral percentages in Figure 6b
compared to Figures 6a and 6c. At Parcel (ABp), the unique
morphology of the reef structures (chapeirões) precludes
reliable use of the FI, since corals flourish on the structure
tops despite the low FI and the absence of living Amphistegina in the sheltered sedimentary environments below.
ACKNOWLEDGMENTS
The authors thank PROBIO-Ministério do Meio Ambiente,
the World Bank, Global Environmental Funding and the
180
BARBOSA AND OTHERS
Conselho Nacional de Desenvolvimento Cientı́fico e Tecnológico (CNPq) for funding the FOCO project. Thanks also to
Reef Check Brazil and the Atlantis Divers teams: Fabio
Pitombo, Rodrigo Portilho-Ramos, Carine M. Almeida, and
Fábio Negrão, who assisted in diving and sampling. We thank
IBAMA for authorizing sampling in both areas and the
administrators of the FN and AB archipelagos. We also thank
Dr. Pamela Hallock for her review as well as those of
anonymous reviewers and editor Paul Brenckle.
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Received 23 July 2011
Accepted 15 February 2012
APPENDIX 1
APPENDIX 2
Mapped area comparison. Attributed sample reach is the maximum
distance a sample is considered in surface interpolation. Islands and
50 m depth isobaths were used for masking. This table can be found on
the Cushman Foundation website in the JFR Article Data Repository
(http://www.cushmanfoundation.org/jfr/index.html) as item number
JFR-DR2012006
Foraminiferal generic density, number of individuals, FORAM
Index (FI), and counts by taphonomic category/10 g for Amphistegina
at Fernando de Noronha. This table can be found on the Cushman
Foundation website in the JFR Article Data Repository (http://www.
cushmanfoundation.org/jfr/index.html) as item number JFRDR2012006
182
BARBOSA AND OTHERS
APPENDIX 3.
Group
a
b
c
d
e
Groups
a&b
a&e
b&d
b&c
a&c
e&b
a&d
e&c
e&d
c&d
Abbreviated similarity percentages (SIMPER) of foraminiferal assemblages at FN.
Average similarity
Main Genera
Average similarity
72
Amphistegina
25
Elphidium
12
70
Amphistegina
8
Quinqueloculina
7
Miliolinella
6
Textularia
5
Sigmamiliolinella
5
Borelis
4
69
Amphistegina
15
Elphidium
14
Textularia
7
#2 samples to form group (only station 2w12)
79
Amphistegina
10
Quinqueloculina
8
Sigmamiliolinella
7
Textularia
7
Cibicides
5
Peneroplis
5
Contribution %
Cumulative %
35
17
11
11
8
7
7
6
22
20
11
52
12
10
9
9
6
6
52
51
53
Dissimilarity
Genera that explained $31% dissimilarity among stations
84
66
64
64
51
45
44
41
36
36
Quinqueloculina, Miliolinella, Amphistegina, Sigmamiliolinella
Sigmamiliolinella, Quinqueloculina, Textularia, Cibicides
Quinqueloculina, Amphistegina, Miliolinella, Sigmamiliolinella
Quinqueloculina, Miliolinella, Sigmamiliolinella, Bolivina
Elphidium, Amphistegina, Fissurina, Cibicides
Quinqueloculina, Miliolinella, Amphistegina, Borelis
Miliolinella, Quinqueloculina, Sigmamiliolinella, Elphidium
Quinqueloculina, Sigmamiliolinella, Elphidium, Textularia
Textularia, Amphistegina, Sigmamiliolinella, Quinqueloculina
Amphistegina, Elphidium, Cibicicoides, Miliolinella
APPENDIX 4
Foraminiferal generic density, number of individuals, FORAM
Index (FI), and counts by taphonomic category/10 g for Amphistegina
for the Abrolhos Archipelago and Parcel. This table can be found on
the Cushman Foundation website in the JFR Article Data Repository
(http://www.cushmanfoundation.org/jfr/index.html) as item number
JFR-DR2012006
183
FORAMINIFER-BASED CORAL HEALTH
APPENDIX 5.
Group
a
b
c
d
e
f
g
Groups
a&b
a&g
a&e
b&c
b&d
c&e
a&f
a&c
g&c
b&f
d&e
b&g
g&d
c&d
f&c
a&d
b&e
f&d
g&e
f&e
g&f
Abbreviated similarity percentages (SIMPER) of foraminiferal assemblages at AB.
Average similarity
Main Genera
67
Average similarity
Archaias
33
Amphistegina
25
64
Quinqueloculina
24
Miliolinella
10
65
Quinqueloculina
17
Amphistegina
8
Peneroplis
7
Archaias
6
#2 samples to form group (only station 1w12)
#2 samples to form group (only station 3w20)
79
Quinqueloculina
18
Archaias
11
Peneroplis
7
Amphistegina
7
75
Quinqueloculina
20
Peneroplis
10
Amphistegina
9
Contribution %
Cumulative %
49
37
38
15
26
12
10
10
86
22
14
9
8
27
13
12
53
Dissimilarity
Genera that explained $ 41–63% of dissimilarity among sites
84
79
78
74
68
66
64
63
56
54
54
52
50
47
47
45
39
33
33
33
31
Quinqueloculina, Miliolinella, Peneroplis, Elphidium
Quinqueloculina, Sigmamiliolinella, Archaias, Peneroplis
Quinqueloculina,Triloculina,Peneroplis,Elphidium
Quinqueloculina, Miliolinella, Peneroplis, Elphidium
Quinqueloculina, Miliolinella, Elphidium, Bolivina
Triloculina, Archaias, Quinqueloculina, Peneroplis
Quinqueloculina, Peneroplis, Pyrgo, Textularia
Archaias, Amphistegina, Quinqueloculina, Peneroplis
Quinqueloculina, Sigmamiliolinella, Pyrgo, Amphistegina
Quinqueloculina, Miliolinella, Sigmamiliolinella, Bolivina
Triloculina,Elphidium,Peneroplis,Cycloforina
Quinqueloculina, Miliolinella,Elphidium,Sigmamiliolinella
Archaias,Sigmamiliolinella,Quinqueloculina,Miliolinella
Archaias,Amphistegina,Quinqueloculina,Pyrgo
Quinqueloculina,Archaias,Pyrgo,Amphistegina
Quinqueloculina,Archaias,Pyrgo,Triloculina
Quinqueloculina,Triloculina,Sigmamiliolinella,Cycloforina
Miliolinella,Elphidium,Sigmamiliolinella,Quinqueloculina
Archaias,Triloculina,Elphidium,Cycloforina
Triloculina,Peneroplis,Cycloforina,Elphidium
Archaias,Sigmamiliolinella,Bolivina,Quinqueloculina
53
58
52