JMJournal of MicropalaeontologyJMJ. Micropalaeontol.2041-4978Copernicus PublicationsGöttingen, Germany10.5194/jm-37-499-2018Benthic foraminiferal assemblages and test accumulation in coastal
microhabitats on San Salvador, BahamasForaminifera in a tropical nearshore habitat, BahamasFischelAndreaSeidenkrantzMarit-Solveigmss@geo.au.dkhttps://orcid.org/0000-0002-1973-5969Vad OdgaardBentCentre for Past Climate Studies, and iClimate, Department of Geoscience, Aarhus University, Hoegh-Guldbergs Gade 2, 8000 Aarhus, C, DenmarkDepartment of Geoscience, Aarhus University, Høegh-Guldbergs Gade 2, 8000 Aarhus C, DenmarkMarit-Solveig Seidenkrantz (mss@geo.au.dk)14November201837249951824November201722September20183October2018This work is licensed under the Creative Commons Attribution 4.0 International License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/4.0/This article is available from https://jm.copernicus.org/articles/37/499/2018/jm-37-499-2018.htmlThe full text article is available as a PDF file from https://jm.copernicus.org/articles/37/499/2018/jm-37-499-2018.pdf
Benthic foraminiferal populations were studied in a shallow bay of San Salvador
Island, the Bahamas. Surface sediments and marine macrophytes were collected
from 14 sample sites along a 500 m transect at Grahams Harbour to
investigate the foraminiferal assemblage in each microhabitat and to test the
link between dead foraminiferal test accumulation patterns and living
epiphytic and sedimentary foraminiferal assemblages, macrophyte distribution,
and environmental gradients. The analyses include grain size measurements,
macrophyte biomass quantification, and qualitative and quantitative
studies of benthic foraminifera. The foraminifera found attached to
macrophytes differed between macrophyte habitats. However, a correlation
between these living communities and the dead assemblages in the sediments at
the same sites could not be observed. Principal component analysis (PCA) and
redundancy analysis (RDA) suggest that the presence of the macroalgae
Halimeda explains 16 % of the residual faunal variation in the dead
foraminiferal assemblage after the effects of sorting according to fall speed
are
partialled out. The RDA also reflects a positive correlation between
foraminifera larger than 1.0 mm in diameter and the 0.25–0.5 mm sediment
grain size, indicating sedimentological processes as the main factor
controlling the sedimentary epiphytic foraminiferal assemblages. These
sedimentary processes overprint most effects of ecological features or
macrophyte-specific association.
Introduction
Benthic foraminifera generally show high abundances and diversity in
tropical shallow marine realms (e.g. Brasier, 1975; Boltovskoy and Wright,
1976) where they inhabit surface sediments and submerged macrophyte
communities (Bock et al., 1971; Brasier, 1975; Culver and Buzas, 1982;
Buchan and Lewis, 2009). Their tests are among the most important
contributors to the sediment matrix in nearshore environments in tropical
regions (Berkeley et al., 2008; Darroch, 2012). However, the typically
oligotrophic waters with low organic carbon and nutrient content as well as
the often coarse-grained sediments and strong currents in nearshore
sediments in the Caribbean region result in severe food limitation for local
microorganisms, including benthic foraminifera (Lipschultz et al., 2002; Buchan
and Lewis, 2009). Consequently, the number of benthic foraminiferal taxa
living in surface sediments is generally low (Wright, 1964; Murray, 1991;
Morgan and Lewis, 2010). Instead, as more nutrients are available in the
proximity of marine macrophytes (Murray, 1970), the majority of nearshore
foraminifera in these environments have adopted an epiphytic life modus,
living motile or permanently to temporarily attached to macrophyte
substrates, i.e. leaves, exposed rhizomes, algae thalli and seagrasses
(Cushman, 1922; Wright and Hay, 1971; Waszczak and Steinker, 1978; Langer,
1993; Alve, 1999; Wilson, 1998, 2007, 2008; Wilson and Ramsock, 2007).
Distinctive epiphytic foraminiferal communities develop on different
macrophyte taxa (Langer, 1993; Fujita and Hallock, 1999; Ribes et al.,
2000; Wilson, 2000, 2008; Fujita, 2004; Debenay and Payri, 2010),
leaving tests of dead foraminifera to accumulate in the sediment (Steinker
and Clem, 1984; Darroch, 2012).
As epiphytic foraminifera are very abundant in nearshore environments,
especially in tropical and subtropical regions (Renema and Troelstra, 2001;
Renema, 2006), they are often used in palaeoecological studies as indicators
of the presence of macroalgae or seagrasses or for determining the degree
of allochthonous influence in assemblages of deeper-water sites (Thomas and
Schafer, 1982; Davaud and Septfontaine, 1995; see also review of Reich et
al., 2015). However, several studies have indicated a disparity between the
living foraminiferal populations (biocoenoses) found in macroalgae and
standing seagrass and macroalgae and the dead assemblages (thanatocoenoses)
found in the sea-floor sediment below (e.g. Martin, 1986; Martin and Wright,
1988; Buchan and Lewis, 2009), a finding which questions sedimentary
assemblages of epiphytic species as a reliable proxy for past macroalgal and
seagrass cover. Nevertheless, relatively few studies exist of
modern benthic foraminifera in environments potentially dominated by
epiphytes (Langer, 1993; Hickmann, 2005; Buchan and Lewis, 2009; Darroch et
al., 2016), with some of these studies concentrating on specific species
and/or preservation rather than assemblage composition (Martin, 1986;
Darroch et al., 2016). Other studies suggest that a potential mismatch
between biocoenosis and thanatocoenosis is mainly relevant at deeper-water
sites (e.g. Martin and Wright, 1988). The cause of potential
discrepancy has also been discussed (e.g. Martin and Wright, 1988; Darroch et
al., 2016). As a result, the assumption of a direct relation between
living epiphytic communities and dead assemblages needs further testing.
In this context, the distribution of living and fossil foraminiferal
assemblages in the sediment and epiphytic habitats helps assess the
significance of post-mortem transport and accumulation from currents and
wave actions (Kotler et al., 1992; Berkeley et al., 2008). Comparison of
living populations and dead assemblages also provides a means to evaluate
the impact of abrasion and dissolution of foraminiferal tests, which may
cause important faunal and abundance differences between the biocoenosis and
the thanatocoenosis (Wilson, 2006, 2010).
A multiplicity of shallow marine habitats is found in the oligotrophic water
environments of the Bahamas archipelago (e.g. Cushman, 1931; Hofker, 1956;
Bock et al., 1971; Culver and Buzas, 1982; Wilson, 1998, 2000). On
San Salvador Island, one of the outermost islands of the Bahamas, epiphytic
habitats like seagrass meadows are well established and widely distributed,
especially along the northern shore of the island. The area is directly
connected to the Atlantic Ocean and is influenced by the Antilles Current
(Gerace et al., 1998), providing stable water temperatures throughout the
annual cycle. Finally, a low human population density and little touristic
infrastructure on the island result in limited effects from pollution,
eutrophication, anthropogenic disturbance and other human impacts on the
shallow marine lagoons (Buchan and Lewis, 2009). The island is thus an
excellent site for shallow benthic foraminiferal habitat research, not the
least for the study of epiphytic species.
The purpose of the present study is to test the distributional pattern of
benthic foraminifera in living populations and dead assemblages
associated with sediment as well as macrophytes. The main focus is a
comparison between the epiphytic foraminiferal community and various types
of macrophyte habitats as well as a comparison between the epiphytic and
surface sediment communities to test for similarities and differences between
biocoenosis and thanatocoenosis, i.e. whether the thanatocoenosis in the
regions of macrophytes is in fact more enriched in epiphytic foraminiferal
tests than areas without vegetation. We will also test for possible links
between sediment grain size and dead foraminiferal test distributions to
evaluate the possible role of sediment transport in the distribution of
epiphytes in the thanatocoenosis. These tests will provide important
information on the reliability of sedimentary assemblages of epiphytic
foraminifera as indicators of macrophytes.
(a) Map of the Bahamas in the western North Atlantic
Ocean and location map of San Salvador; modified after Robinson and Davis
(1999). Light grey areas: distribution of fresh and saltwater lakes on San
Salvador. The dotted line indicates water depths less than 10 m. Red square:
study area at Grahams Harbour. (b) Schematic map of the studied transect
(dashed line) with 14 sample sites from the Old Dock (site GH12-01) to the
Cut (site GH12-14), with a water depth of approx. 1 m. The sample sites are
categorized into microhabitats M0 (vegetation absent), M1 (sparse vegetation),
M2 (moderate vegetation) and M3 (dense vegetation) in accordance with the
dominant macrophyte species in the respective habitats. Black rectangles indicate the location of building structures.
Study area
San Salvador is one of the outermost islands of the eastern part of the
Bahamas archipelago and is located approximately 600 km off the Florida
coast. With a size of 11×19km, it is one of the smaller islands in the
Bahamas (Gerace et al., 1998; Gould and Vermette, 2005) (Fig. 1a).
Topographically isolated from the main Bahama Banks (Great and Little
Bahamas Bank) as a submarine carbonate platform including the majority of the
Bahamas islands, it is surrounded by marine water basins reaching up to
4000 m of water depth (Gerace et al., 1998). Due to its open, unprotected
connection to the Atlantic Ocean, San Salvador is year-round exposed to
relatively strong trade winds, primarily from the NE to SE, and associated
high-energy waves (Thomas A. McGrath, unpublished data, 1993). The island is
furthermore commonly
subject to hurricanes primarily reaching San Salvador from the SE and E with
the main path along the archipelago (Caribbean Hurricane Network, 2011).
Such hurricanes can result in significant beach erosion (Curran et al.,
2001).
The hydrographic conditions of offshore regions of the island are
characterized by the Antilles Current, part of the North Atlantic
Subtropical Gyre (Gerace et al., 1998), which transports equatorial waters
to San Salvador, causing relatively cool sea-surface temperatures (SSTs) in
the summer (range 22–32 ∘C) and a relatively warm SST during
winter (17–27 ∘C) (Shaklee, 1994). However, nearshore waters are
primarily affected by the longshore current, which is induced by north-easterly
trade winds and is strongest during winter. During summer months, the wind
direction shifts to predominantly south-eastern, resulting in a weakening of
the coastal current (Thomas A. McGrath,
unpublished data, 1993; Gerace et al., 1998). Despite a strong
current and often heavy winds, shallow carbonate banks and reef formations
around the island create protected habitats for marine endemic flora and
fauna (Fig. 1a).
One such protected basin is the 3 km long embayment Grahams Harbour. It is
located at the northern tip of San Salvador Island at 24∘07′24′′ N,
74∘27′30′′ W, and bounded by San Salvador to the south, the
coastline of North Point to the east, and a series of reefs and small islands
to the north (Fig. 1) (Adams, 1980; Gerace et al., 1998). The basin reaches
a maximum water depth of ca. 6 m (average depth ca. 1.5 m) and in its
deepest part sediments consist of up to 4 m thick calcareous ooze and
bioclastic sand resting on top of hard bedrock sediments. The ooze is mainly
composed of poorly sorted fragments of calcifying green algae of the genus
Halimeda, corals and sponges, as well as benthic foraminifera and microgastropods
(Colby and Boardman, 1989; Darroch, 2012; Darroch et al., 2016). In the
shallow margins of the basin, the unconsolidated ooze can be as shallow as
5–10 cm. The subsurface geology consists of Holocene sand and limestone
stratigraphically belonging to the North Point Member of the Rice Bay
Formation (Colby and Boardman, 1989; Hearty and Kindler, 1993; Mylroie
and Carew, 2010).
Surrounded by reefs and barrier islands to the north and east, Grahams
Harbour remains open to deeper waters in the west (Armstrong and Miller,
1988). This results in a windward high-energy lagoon that is highly
affected by the longshore currents entering through a narrow opening, the
Cut, between North Point and Cut Cay, and moving southwards along the shore
(Gerace et al., 1998) (Fig. 1b). No detailed long- or short-term
hydrographic monitoring of this current exists, but during sampling we
clearly observed the highest current velocities closest to the Cut and lower
energy levels further into the bay, a phenomenon that has previously been
described by Buchan and Lewis (2009). The current is strongly affected by
tidal action with a general tidal range of 50–90 cm at near-coastal sites
(source: NOAA/NOS/CO-OPS, referenced to station Settlement Point, Grand
Bahamas). In July and August 2012 the tidal range was likewise
50–90 cm
and in late July 2012 water depths at low tide ranged between 80 and
130 cm
at near-coast sampling sites along Graham Harbour (Table 1).
Sample sites. List of the 14 sample sites (GH12-01 to
GH12-14) at Grahams Harbour, including water depth in centimetres, water temperature
in ∘C and salinity in psu. The temperature and salinity of the
water were measured 5–10 cm above the sediment surface. The grain size is
given in relative abundance (%). The vegetation biomass corresponds to
grams dry weight of vegetation per studied quadrant (0.25×0.25m). The most
abundant macrophytes in the respective sites are also given. Algae complexes
mainly consisted of Halimeda, Penicillus, Udotea, Batophora and
Rhipocephallus. Sampling was performed under intermediate low tide
conditions.
SampleSampleWaterBottom waterBottom waterCoarse grainsMedium grainsFine grainsTotalDegree of macrophyteDominantHabitatsitedatedepthtemperaturesalinity(>0.5mm)(0.5–0.251 mm)(0.25–0.06 mm)biomasscoveragemacrophytestype(cm)(∘C)(psu)(%)(%)(%)(g/0.25×0.25m)GH12-0121 July 201210030.834.216.912.370.80.0absent–M0GH12-0221 July 201212030.733.729.85.964.325.9denseThalassiaM3GH12-0321 July 201212030.733.629.413.956.812.4moderateThalassia–SyringodiumM3GH12-0421 July 201211030.733.636.08.155.94.8moderateSyringodiumM2GH12-0524 July 201212030.733.737.521.740.810.7sparseAlgae complexM1GH12-0624 July 201211030.633.731.518.849.720.7sparseAlgae complexM1GH12-0726 July 201213029.534.247.87.045.20.8sparseAlgae complexM1GH12-0826 July 201213029.834.223.311.265.53.7moderateSyringodiumM2GH12-0926 July 201212030.134.235.220.544.41.2moderateSyringodiumM2GH12-1026 July 201213030.034.239.224.136.71.7moderateThalassia–SyringodiumM2GH12-1127 July 201212029.434.224.116.459.56.4denseThalassiaM3GH12-1227 July 201212029.334.035.414.649.919.2denseThalassiaM3GH12-1327 July 201210029.634.110.911.577.60.0absent–M0GH12-1427 July 20128029.433.738.222.339.53.4sparseAlgae complexM2
Grahams Harbour provides diverse habitats, e.g. patch reefs in the outer
zone and seagrass meadows in the inner part (Beck, 1991; Wilson and Ramsook, 2007;
Morgan and Lewis, 2010; Darroch et al., 2016). The relatively
protected embayment forms an especially important habitat for seagrass meadows, ranging
from patchy to dense and hosting a number of different macrophytes typical
for the region, with an associated but fragile benthic microfauna (Gerace
et al., 1998; Buchan, 2006; Morgan and Lewis, 2010; Darroch et al., 2016).
The microhabitats within the studied transect vary from habitats subject to
strong currents with sparse vegetation of Halimeda spp. and other macroalgae close to
the Cut to environments with weak current activity and moderate to dense
vegetation dominated by the seagrasses Thalassia testudinum and Syringodium filiforme along the coast (Fig. 1b).
The Grahams Harbour section from Old Dock (start
transect) to the Cut (end transect). Photo: Andrea Fischel, 2012.
Material and methodsSampling and material
A 500 m long transect was sampled in July 2012 in a shallow lagoon along the
shoreline of Grahams Harbour in the north of San Salvador, starting at the
Old Dock (24∘7′23.50 N, 74∘27′29.41 W; sample station
GH12-01) and terminating at the Cut (24∘7′39.72 N, 74∘27′27.22 W;
sample station GH12-14) (Figs. 1b, 2). The transect consists of
14 sample stations 40 m apart (Fig. 1b). Samples were taken while swimming
with a snorkel using a small sealable beaker. At each station we collected
one surface sediment sample (0–1 cm of sediment depth) used for foraminiferal
analyses and one combined surface–subsurface sediment sample (0–5 cm
of sediment depth) for grain size analyses by scraping up the sediment using a
plastic beaker. In addition, at each station we collected all marine
macrophytes from the sea floor in an area of 0.25×0.25m (i.e. in one-quarter
of the 0.50×0.50m frame used in sample collection). Samples were
all taken in July 2012 during intermediate low tide conditions (neither
spring nor neap tide) at water depths between 80 and 130 cm (Table 1, Fig. 1b).
Water temperature and salinity at the sea floor at the time of sampling
were measured to 29.3–30.8∘ and 33.6–34.2 psu (Table 1),
respectively, using a standard handheld salinity–conductivity–temperature
meter.
Sediment samples mainly consist of carbonate grains. Grain size analysis was
applied to the 14 sediment samples (upper 5 cm) using wet sieving with mesh
widths no. 12 (1.5 mm), no. 35 (0.5 mm), no. 60 (0.25 mm), no. 120
(0.125 mm) and
no. 230 (0.063 mm). The relative proportion of each grain size fraction
at each sample station was subsequently estimated based on the dry-weight
fractions (Table 1). The average grain size was calculated and used as an
index of the grain size distribution of each habitat. In lieu of actual
current velocity measurements, energy settings and coastal current strength
along the transect were estimated based on field observation and the
proximity to the current inflow; current strength was highest at the Cut and
weakening with increasing distance from the Cut, which is in accordance with
the general hydrography (Gerace et al., 1998; Buchan and Lewis, 2009). Clay
and silt contents were not investigated. Colby and Boardman (1989) reported
that clay and silt were absent from recent sediments of Grahams Harbour.
These grain sizes occur mainly in resuspension and accumulate further
offshore, which was not part of the present study.
Macrophytes, distribution and density. Marine macrophyte
species recovered from the sample sites at Grahams Harbour. For each 0.25×0.25m quadrant, the absolute abundance of each macrophyte species is given
in grams of dry weight and as a percentage distribution in relation to the entire
macrophyte assemblage. The dry weights of Cladophora prolifera at the sample sites GH12-05
and GH12-06, and thus also the percentage calculations, are somewhat
overrepresented as the algal rhizomes contained sediment which could not be
washed off without destroying the algae.
Macrophyte taxa were identified following Littler et al. (1989) and Littler
and Littler (2000) (Table 2). To determine the vegetation density (biomass)
at each site, the marine macrophytes collected at each station were
oven-dried (40 ∘C) and weighed after sampling (Table 2). The
macrophyte distribution is presented here both as a mass (grams of dry
weight per quadrant)
and as a percentage distribution. For this latter parameter,
it must be kept in mind that some samples contain very low abundances of
macrophytes with associated higher error of determination. In addition, some
macrophytes were encrusted with calcium carbonate, which added to the
biomass estimation. Based on the identification of the macrophytes in each
sample combined with the visual inspection during sampling, each sample site
was categorized into one of four microhabitats: M0 (vegetation absent), M1
(sparse vegetation), M2 (moderate vegetation) and M3 (dense vegetation).
Foraminiferal assemblage collected from macrophytes. The
table shows the absolute abundance of epiphytic foraminifera collected from
the macrophytes in an area of 0.25×0.25m for each sample site at Grahams
Harbour (GH12-01–GH12-14). The letter after the species name denotes the
morphogroup by Langer (1993).
Species abundanceGH12-01GH12-02GH12-03GH12-04GH12-05GH12-06GH12-07GH12-08GH12-09GH12-10GH12-11GH12-12GH12-13GH12-14Total no. of(relative) onforam. onmacrophytesmacrophyte samplesHabitat typeM0M3M3M2M1M1M1M2M2M2M3M3M0M2Archaias angulatus (A)020100000000003Elphidium sp. (C)000000000002002Sorites marginalis (A)030915000115380072Rosalina–Discorbis sp. (B)010000000003026Cornuspira sp. (A) and Spirillina sp. (D)030400000011180036Planogypsina acervalis (A)0254000601180431Spirolina sp. (D) and Peneropolis sp. (D)00300000001120016Indeterminate epiphytic species0500000100130010Total number of specimens on vegetation in0431724000816175406176sample (0.25×0.25m)Laboratory treatment and analyses of foraminiferal samples
The 14 surface (0–1 cm) sediment samples for foraminiferal analysis were
treated with denatured ethanol (92 % ethanol mixed with seawater,
resulting in an alcohol percentage of 60 %–70 %) and rose-bengal staining
(Walton, 1952) immediately after sampling. Although the number of living
specimens was overall low, those specimens that were found to be alive
showed a very clear staining, indicating a successful staining procedure.
After staining for 24 h, the surface samples were wet-sieved using
no. 230 (0.063 mm) and no. 120 (0.125 mm) mesh-size sieves and subsequently
oven-dried. The >0.125mm fraction was analysed for its dead
(unstained) and living (stained) benthic foraminifera (Table 3) using a
stereomicroscope Olympus SZ 3060. In total, a minimum of 200 dead specimens
were counted for each sample site. Living foraminifera were
registered separately in the same sample aliquot used for analysing the dead
assemblage, but living specimens were only found in very low numbers. The
taxonomy of Loeblich and Tappan (1988) as well as Darroch (2012) was used.
Relative species abundances and absolute concentrations (tests per gram
of surface sediment, i.e. test density) of the dead (thanatocoenosis) and
living assemblage (biocoenosis) were calculated based on the weight of the
analysed sediment (Table 3). The 0.063–0.125 mm fraction of the subsurface
samples was also tested for its foraminiferal assemblage. However, as this
fraction only contained relatively few foraminifera belonging to a
restricted number of species, all of which were also present in the
>0.125mm fraction, it was not studied further.
The foraminifera of the macrophyte samples from the 14 sites were analysed
without applying rose-bengal staining. The foraminifera of the macrophyte
samples were only identified to genus level. Each sample represents all
macrophytes found in an area of 0.25×0.25m (one-quarter of the 0.5×0.5m quadrant used for foraminiferal and grain size analyses) at the vegetated
sample sites.
Foraminiferal assemblage collected from sediment samples.
Dead and living benthic foraminiferal assemblages in surface sediment
samples at Grahams Harbour. Foraminiferal test densities are presented as
absolute abundances (number of specimens) calculated in specimens per gram
of surface sediment. The ratio of living versus dead foraminifera is based on
the absolute number of living and dead foraminifera registered in each
sample. Species marked with (EPI) comprise the group of epiphytal
foraminiferal, with A, B, C and D to the right denoting the morphotype of
Langer (1993). The test density of the total fauna and epiphytal fauna in
the thanatocoenosis is given in specimens per gram of surface sediment. The
ratio of the total epiphytic foraminifera in the total assemblage is
presented in %.
Species abundance (relative) in the sediment samplesGH12-01GH12-02GH12-03GH12-04GH12-05GH12-06GH12-07GH12-08GH12-09GH12-10GH12-11GH12-12GH12-13GH12-14MorphotypeHabitat typeM0M3M3M2M1M1M1M2M2M2M3M3M0M2Spirolina arietinus2.00.90.50.41.70.91.60.02.92.01.81.33.13.6DSpiroloculina antillarum0.72.22.00.00.00.00.00.00.00.00.00.40.00.0DTriloculina spp. and Quinqueloculina spp.34.035.830.944.625.932.642.042.534.633.338.332.627.729.1DTextularia candeina0.00.00.00.00.00.00.00.00.00.00.00.00.40.9DTextularia oviedoiana0.00.01.00.05.74.21.20.42.92.51.40.90.40.4DTextularia sp.0.00.00.00.00.00.00.40.00.00.50.00.40.00.0DTrifarina bella0.00.00.50.40.00.50.80.00.01.50.00.00.91.3DTrifarina bradyi0.00.00.50.00.00.00.00.00.00.00.00.00.00.0DVertebrasigmoilina mexicana2.70.02.00.00.60.00.01.10.50.00.00.01.30.0DIndeterminate (non-epiphytic)4.83.52.97.52.93.35.13.19.64.52.75.72.73.6Total dead foraminiferal assemblage (spec. g-1 sediment)22626278226762589166521851347510406091301117622402662Epiphytic dead foraminiferal assemblage (spec. g-1 sediment)70023069111852505297573109234520650444010501265Ratio of epiphytic foraminifera of the total dead assemblage (%)33.739.843.630.756.347.937.336.838.038.845.043.547.348.9Living (stained) assemblage Archaias angulatus (EPI)00003000000000Bolivina–Brizalina sp.00000000001000Cibicidoides sp. (EPI)00000000000100Cymbaloporetta squamosa00000000100000Nonionella atlantica00000010000000Nonion? sp.00000000001000Peneroplis bradyi00000130122100Rosalina globularis (EPI)00000020001000Siphonodosaria lepidula00000000020000Spirolina arietinus00001000000000Total living foraminifera00004160245200Test density Dead foraminifera per gram22626278226762589166521851347510406091301117622402662Living foraminifera per gram00001234401012291000Ratio living per 100 dead forams00002130123100
List of benthic foraminiferal species and author names
encountered in the biocoenosis and thanatocoenosis in surface sediments and on
macrophytes from Grahams Harbour, San Salvador Island.
In order to compare the distribution of the (generally dead) epiphytic
foraminifera in the surface sediment to the assemblages on the macrophytes,
we calculated the relative abundance of sedimentary epiphytic foraminifera
based on the total benthic faunal assemblage. All epiphytic foraminifera
were collected from the macrophytes and identified; the occurrence of each
species is reported as a percentage of the total number of epiphytic specimens
collected in each sample. To specify the assemblage of epiphytic
foraminifera, the classification based on morphotypes by Langer (1993) was
applied: A, permanently attached foraminifera, e.g. planorbulinids and
Sorites (morphotype A: flat concave test); B, temporarily attached foraminifera,
e.g. Rosalina, Discorbis, and Asterigerina (morphotype B: trochospiral test); C,
motile suspension-feeding foraminifera, e.g. elphidiids, (morphotype C: complex test
structures with canal systems and multiple apertural openings); and D,
permanently motile epiphytic species such as Quinqueloculina, Triloculina and Textularia (morphotype D: various
test shape) (Table 4). This classification was applied in order to evaluate
potential differences in the results related to the various morphotypes and
their way of life (i.e. permanently attached vs. motile). In the present
study, permanently to temporarily attached species (morphotypes A–C) were
furthermore classified into the group epiphytic-type I, while epiphytic taxa
with a permanently motile mode of life (morphotype D) were grouped as
epiphytic-type II. These permanently motile epiphytic-type II taxa are not
limited to macrophyte habitats or even an attached way of life, in fact
often living as epifaunal to shallow infaunal species on or in sediments
substrates. Hence, it would not be possible to judge if a specimen of
epiphytic-type II found in the dead assemblage in the sediment in fact
originally lived in the sediment or on macrophytes. Consequently, only
epiphytic species that belong to epiphytic-type I are included in our
calculations.
In total, the following species are included in the epiphytic-type I group:
Archaias angulatus (morphotype A), Asterigerina carinata (morphotype B),
Cibicides spp. (B), Cibicidoides spp. (B), Discorbis rosea (B),
Discorbis spp. (B),
Cornuspira involvens (A), Cyclorbulina compressa (B), Cymbaloporetta bradyi
(A), Cymbaloporetta squammosa (A), Elphidium spp. (morphotype C),
Hauerina speciose (C), Osangularia culter (B), Parasorites spp. (A),
Planogypsina acervalis (A),
Rosalina floridana (B), Rosalina globularis (B), Rosalina subaraucana (B),
Rosalina spp. (B) and Sorites marginalis (A).
Multivariate statistics
Ordination was applied to the dataset using the CANOCO v4.5 software
package (ter Braak and Šmilauer, 2002). An initial detrended
correspondence analysis (DCA) on foraminiferal percentage data gave
(irrespective of transformation methods) gradient lengths of DCA axis 1 of
the total dead assemblage below 2, indicating that linear models (e.g. PCA,
RDA) are appropriate for the ordinations. Due to a high number of different
epiphytic-type I species in the fossil assemblage
(nepi=21) compared to the limited number of
samples (n=14), a principal component analysis (PCA) was used
to reduce the dimensionality to four main axes. Subsequently, the
relationship between the axis (species) scores and environmental factors was
assessed using a series of redundancy analyses (RDA) with associated
Bonferroni-adjusted Monte Carlo permutation tests of significance
(n=999).
ResultsLiving foraminiferal assemblages attached on macrophytes
The in situ living foraminiferal assemblages found attached to the
macrophytes were studied in the different habitats of Grahams Harbour. In
total, five genera were identified, encompassing at least 15 species (Tables 3, 5).
Sorites marginalis (morphotype A) was the most abundant species, dominating the
assemblages in the habitats distal from the tidal inflow (M2, M3 habitats),
as also previously described by Buchnan and Lewis (2009) from Grahams
Harbour. In contrast, the Rosalina–Discorbis group (morphotype B) dominated the assemblage
proximal to the current inflow at the Cut (site GH12-14; M1 habitat).
Spirulina sp., Elphidium sp. and Cornuspira sp. (morphotypes D, C and A, respectively) have the highest
abundances in the Thalassia–Syringodium habitats (M3) of intermediate energy setting (sites
GH12-11 and GH12-12). The remaining species found in habitats M1–M3 were
only found in low abundances.
Despite the limited number of sample points making the comparison
uncertain, maximum epiphytic species diversities seem to be linked to
Thalassia habitats (M3). Here seven different taxa were registered. Lower diversities
among epiphytic foraminifera occur in assemblages collected from
Syringodium and macroalgae habitats (M2), where only three taxa were observed.
Also,
population densities were highest in connection to the
Thalassia–Syringodium community with 172–216 specimens in an area of 0.25×0.25m in contrast
to 4–24 specimens observed on calcareous macroalgae substrate (e.g.
Halimeda, Penicillus) in a similar area size. Multivariate analyses were not applied to the
living assemblage due to the quantitative limitation of the dataset.
Foraminiferal assemblages in surface sediments
In total, 56 different benthic foraminiferal taxa were identified in the
dead assemblages, whereas 8 taxa were found in the living community of the
surface sediments (Tables 4, 5). The dead foraminiferal assemblages
(thanatocoenoses) were dominated by Triloculina spp. and Quinqueloculina spp. (morphotype D) each with
35 %–45 % relative abundance. Other common taxa were Discorbis spp. and Rosalina spp., whereas
Nonionidae (D), Neoconorbina terquemi (D) and Archaias angulatus (A) were observed in lower numbers.
Quantitative analyses showed only low numbers of living foraminifera
(biocoenosis) in the sediment. Four sample sites (GH12-05, GH12-06, GH12-09,
GH12-12) contained one to three living specimens in the analysed material, while
sites GH12-07, GH12-10 and GH12-11 held four to six living specimens, with the
majority of the specimens belonging to Peneroplis sp. (morphotype D) (Table 4). Seven
out of the 14 stations contained no living benthic foraminifera.
The test densities of the dead assemblage varied between 609 and 6258
specimens per gram (spec. g-1) of surface sediment (Table 4), with
foraminiferal tests on average making up ca. 5 % of all grains in the
>0.125mm sediment fraction. The highest abundance of dead
foraminiferal tests (>6200 spec. g-1) was observed in sample
sites with moderate to dense vegetation located distally from the tidal inflow
(GH12-02 and GH12-04), whereas relatively low test densities, approximately
600–900 spec.g-1, occurred in areas with sparse vegetation and a solid
carbonate bedrock underlying the few-centimetres-thin unconsolidated surface
sediments (GH12-05, GH12-06 and GH12-10). Closer to the tidal inflow
(GH12-11 to GH12-14) where current energy is higher, test densities varied
between 1100 and 2600 spec.g-1. The estimates of test density of the
living assemblages have a high sample error but seem to follow a pattern
inverse to the dead assemblages. Here the highest densities of 29–44 spec.g-1 were recorded in sparsely to
moderately vegetated areas (GH12-07 and
GH12-11) (Table 4). Remarkably, the highest abundances of living
foraminifera were concentrated in the middle part of the transect, including
the stations GH12-05 to GH12-12. In close proximity (stations GH12-13,
GH12-14) and further distal to the tidal inflow (stations GH12-01 to
GH12-05) living foraminifera seemed to be absent (or abundance is extremely
low, as it could not be registered in the present study). One to three living
foraminifera per 100 dead specimens were observed at the sample sites which
contained foraminifera (Table 4).
Examples of sea-floor vegetation also showing the metal
frame used during sampling. (a) Sparsely to moderately vegetated area
typical for an M2 vegetation habitat, with a mix of calcareous algae and some
seagrass (Thalassia). (b) Densely vegetated sea floor covered by seagrass typical
for an M3 habitat. Photo: Sonja Reich, 2012.
Graph showing physical and biological proxies (grain
size, macrophyte biomass, and the number of living and dead epiphytic
foraminifera) recorded at each sample site. The cumulative relative
percentage of the grain size fractions is shown as a bar chart (dashed
column: grains less than 0.25 mm in diameter; dotted column:
grain sizes between 0.25 and 0.5 mm; hatched column: grains larger than 0.5 mm).
Macrophyte biomass, indicated by the green curve (green circles), is
given in grams of dry biomass per m2. The distribution of epiphytic
foraminifera is plotted as the number of specimens in the dead assemblage
per gram of dry surface sediment (blue curve, blue diamonds). The number of
specimens in the living assemblage per m2 of vegetated area is shown in the red
curve (red triangles). The curves show a subjective interpolation between
the sample sites. The microhabitat index M0 for areas with no vegetation;
areas with sparse vegetation, mainly calcareous macroalgae (M1); habitats
with moderate vegetation of Syringodium–algae complexes (M2); and dense
seagrass beds dominated by Thalassia and Syringodium (M3).
RDA plot showing the total foraminiferal thanatocoenosis
against grain size. Sample sites are indicated by a black circle as well as
by site number (GH12-01 to GH12-14). Sample sites 1 and 13 showed identical
scoring. The foraminiferal fauna is statistically divided into four PCA axes
(PCA-AX1, PCA-AX2, PCA-AX3 and PCA-AX4) illustrated as black vectors.
Grain size fractions in millimetres are shown as red and blue vectors; only the
0.25–0.5 mm fraction (shown as the blue vector) was significant for the
faunal variation in the foraminiferal thanatocoenosis.
Microhabitat classification of foraminiferal sedimentary
thanatocoenosis
Of the 56 taxa in the dead assemblages (thanatocoenoses) of the surface
sediment samples (Table 4), 21 were epiphytic taxa (epiphytic-type I + II).
Specimens were overall well preserved, including the smaller, more fragile
taxa such as Nonionidae. The epiphytic-type I group in the foraminiferal
thanatocoenoses was dominated by Archaias angulatus (morphotype A),
the Rosalina–Discorbis group (e.g. Rosalina floridana, Rosalina subaraucana and
Discorbis rosea; all B), Laevipeneroplis proteus (D) and Laevipeneroplis bradyi (D). To specify the foraminiferal abundance in the
dataset, the foraminiferal assemblages were classified with respect to the
four microhabitats (M0, M1, M2, M3) distinguished based on the macrophyte
vegetation in each habitat. The density of macrophytes per m2 was
also taken into account (Figs. 3, 4, 5, Table 1).
Microhabitat M0 is defined as areas lacking marine macrophytes and
is found at sample stations GH12-01 and GH12-13 (Fig. 1b). The grain size
distribution in these habitats is highly homogeneous and fine grains
(<0.25mm) make up more than 70 % of the sediment. Epiphytic-type
I foraminifera (dominantly the Rosalina–Discorbis group B) encompass 34 %–47 % of the
thanatocoenoses (Fig. 4, Table 4).
Microhabitat M1 (stations GH12-05 to GH12-07) is characterized by
sparse vegetation, primarily inhabited by calcareous algae, mainly
Cladophora, Acetabularia, Laurentia and Batophora. The grain size distribution appears broader than for M0,
with a high fraction of coarse grains. Epiphytic (type I) foraminifera
(dominated by Archaias angulatus (A) and the Rosalina–Discorbis group B) are abundant, encompassing 37 %–56 %
of the total dead benthic foraminiferal assemblages (Table 4). They increase
in abundance towards the tidal inflow (the Cut).
Microhabitat M2 is characterized by moderate vegetation, mainly of
Syringodium filiforme and various calcareous algae, e.g. Halimeda, Rhipocephalus and Udotea, but also some Thalassia reaching a
vegetation biomass density of 5–20 gm-2 (sample sites GH12-04, GH12-08,
GH12-09, GH12-10 and GH12-14; Figs. 1b, 3, Table 2). The epiphytic-type I
foraminiferal abundance in the dead assemblages is lowest in M2 habitats
(30 %–38 %), dominated by the Rosalina–Discorbis group (B) and by Archaias angulatus (A) (Table 4). In
general, total test densities of dead foraminifera in M2 habitats vary by a
factor of 10 (i.e. 6260 specimens g-1 sediment distal to the tidal inflow
at site GH12-04 and 610 specimens g-1 sediment proximal to the tidal inflow
at site GH12-10).
Microhabitat M3 is dominated by Thalassia testudinum and Syringodium filiforme (stations GH12-02, GH12-03,
GH12-11 and GH12-12; Figs. 1b, 3b), forming dense seagrass beds with a high
vegetation biomass (25–100 gm-2). The total dead foraminiferal test
density decreases towards the tidal opening, similar to M2 habitats. The
proportion of epiphytic (type I) foraminifera varies between 40 % and 45 %
of the total dead fauna, decreasing towards the tidal opening and being
dominated by the Rosalina–Discorbis group (B) and Archaias angulatus (A) (Table 4).
Multivariate analyses of the thanatocoenosis
PCA axes 1–4 together account for 82.7 % of the variation of the dead
foraminiferal assemblages. Taxa with high scores on PCA axis 1 (PCA-AX1,
eigenvalue: 44.8 %) include the species Archaias angulatus (+0.84), Textularia oviedoiana (+0.82) and
Cyclorbiculina compressa (+0.68). In contrast, the following taxa show low scores:
Triloculina–Quinqueloculina sp. (-0.84), Planogypsina acervalis (-0.67),
Neoconorbina terquemi (-0.66) and Rosalina spp. (-0.64). This suggests that
PCA axis 1 can be seen as reflecting morphological variations from large
(>400µm), compressed species (positive score) to
smaller, more rounded tests (negative score). PCA axis 2 (PCA-AX2,
eigenvalue: 22.9 %) seems to reflect a second morphological feature, with
species with a convex test shape scoring positively (Osangularia culter with +0.879, Rosalina floridana
with +0.85 and Amphistegina gibbosa with +0.76), while species with a more compressed or
elongated test shape score negatively (Archaias angulatus with -0.49, Nonionidae with
-0.46 and
Textularia oviedoiana with -0.47). PCA axes 3 and 4 (PCA-AX3, eigenvalue: 8.2 %; PCA-AX4,
eigenvalue: 6.8 %) are less easy to interpret as no common morphological
features or ecological preferences can be defined for the species with
high and low scores along these axes.
RDA with forward selection and a Monte Carlo permutation test (n=999)
of the foraminiferal PCA axes against grain size distributions shows
that the particle size 0.25–0.5 mm explains a significant proportion
(16 %, p<0.05) of the foraminiferal variation represented by the
four PCA axes (Fig. 5). This analysis also identifies the grain size
>1.5mm as important (p<0.05), but scatter plots show
that this correlation depends on a single extreme sample. Accordingly, the
apparent correlation with >1.5mm grains is disregarded here. In
contrast, the importance of the 0.25–0.50 mm grain size fraction is
supported by the fact that the sum of percentages of foraminifera larger
than 1 mm in diameter shows a clear positive relationship with exactly this
grain size fraction. Since foraminifera generally make up ∼5 % of this sediment fraction it is unlikely that the correlation is an
artefact of the increasing test size itself, supporting the fact that this
correlation is reliable.
Partial RDA plot demonstrating the total sedimentary
foraminiferal assemblage against the absolute macrophyte biomass, including
the 0.25–0.5 mm grain size fraction as a co-variable. Black circles show
each of the sample sites (GH12-01 to GH12-14), with sample sites GH12-01 and
GH12-13 showing identical scores. The black vectors comprise four PCA
axes (PCA-AX1 to PCA-AX4), covering all species of the thanatocoenosis. The
most abundant macrophyte species are shown as red and blue vectors.
Exclusively the macrophyte species H. incrassata (singled out as the blue
vector) was statistically significant for the faunal variability of the
total foraminiferal thanatocoenosis.
A partial RDA with the 0.25–0.5 mm grain size as a co-variable was run
against macrophyte relative frequencies. The purpose was to explore if
macrophyte biomass or cover pattern could explain a significant part of the
residual variation (after accounting for the variation explained by grain
size) (Fig. 6). Variations in the density distribution of Halimeda incrassata explain 16 % (p
<0.05) of the residual foraminiferal variation, while no other
single macrophyte taxon gave any significant contribution. Similarly, a
partial RDA (co-variable: 0.25–0.5 mm) against biomass (absolute and
in percentage) showed only Halimeda incrassata to be significantly related to the total
foraminiferal assemblage (explanatory power 17 %, p<0.05). An
RDA of macrophyte biomass against grain size showed no significant
relationship. When testing the faunal variation in the epiphytic-type I
foraminiferal dead assemblage only, PCA axes 1–4 accounted for a total of
87.2 % of the variance. No further significant relationships were found
when comparing the sample score of these PCA axes in a series of RDAs with
sediment grain size, absolute biomass and percentage of biomass.
DiscussionEnvironmental control of the biocoenoses and thanatocoenoses
The relative abundances of dead epiphytic (type I) foraminifera, excluding
the permanently motile epiphytic (type II) species (Langer, 1993) range
between 31 % and 56 % in the thanatocoenoses at Grahams Harbour. Similar to
findings of previous studies (Brasier, 1975; Wilson and Ramsook, 2007;
Wilson, 2010), a large part of the foraminiferal community is adapted to the
nutrient-depleted conditions of surface sediments in Caribbean nearshore
environments by living attached to the leaves and rhizomes of macrophytes. The
generally low abundance of direct predators (predation on foraminifera) in
nearshore waters in the Caribbean (Lipps, 1983, 1988) combined with
a very low indirect predation, e.g. grazing of the macroalgae and
seagrasses by sea turtles and manatees (Jackson et al., 2001), enables
epiphytic foraminifera to colonize exposed macrophytes. Foraminifera are not
only restricted to macrophyte rhizomes, as they are also found on
the thalli of species of e.g. Halimeda, Penicillus and
Udotea and on the leaves of Thalassia and Syringodium. Thus, the
abundance of epiphytic foraminifera in the foraminiferal community is very
high compared to extratropical realms. A large proportion of the epiphytic
foraminifera included in our study represents group A and B of Langer's
classification, including the permanently attached (group A) and temporarily
attached species (group B). Both groups are characterized by a flat
orbitoidal to discoidal shape (e.g. Loeblich and Tappan, 1988; Langer,
1993).
Abundance patterns of living and dead foraminifera at Grahams Harbour
demonstrated differences between habitats with variance in macrophyte
coverage. This is especially clear for the thanatocoenoses, for which test
densities varied between 250 and 2500 specimens g-1 surface sediment.
The lowest test concentrations were observed in habitats with sparse vegetation
of calcareous macroalgae in a low-current-energy regime, but also in areas
with dense vegetation in a high-current regime. The highest test densities
were observed in habitats with dense to moderate vegetation dominated by
Thalassia and Syringodium in low-current environments. All epiphytic morphotypes (A–D; Langer,
1993) were present on the macrophytes and in the thanatocoenoses
(Tables 3, 4), albeit with the sediment biocoenosis dominated by living
morphotype D species. However, the number of specimens was too low to
reliably test for any link between habitat (M0–M3) and morphotypes.
The canonical ordination results of the dead foraminifera found in surface
sediments clearly show that the main patterns of distribution are linked to
grain size and hence to sedimentary processes (see below). However, after
the foraminiferal variation correlated with sediment grain size was separated
out statistically, a small part of the residual variation could successfully
be related to variations in the density of one species of plant macrophyte,
namely Halimeda incrassata. The lack of correlation between grain sizes and macrophyte
distribution furthermore suggests that sedimentary processes had little
significance for macrophyte cover patterns. This finding is somewhat
unexpected, but an explanation may be sought in the relatively limited
environmental gradient along the sampled coastline.
Sedimentation and current control of foraminiferal habitats
Quantitative analyses of the surface sediments of Grahams Harbour show a
high but variable abundance of dead foraminifera in the top sediment. The
RDA results of the dead foraminiferal assemblages suggest that a large
proportion of the assemblage variation cannot be accounted for by any of the
environmental factors recorded in our study. However, the correlation
between the main gradient of foraminiferal assemblages (PCA-AX1) and the
0.25–0.5 mm grain size fraction (Fig. 5), apparently governed by the
relationship between larger tests of foraminifera and the same grain size
fraction, clearly suggests that sedimentary processes, i.e. transport of dead
foraminiferal tests as part of the sediment fraction, play a very important
role for the thanatocoenoses. The pattern of maximum concentration of empty
tests in habitats with moderate to dense macrophytal coverage distal from
the tidal inflow, with relatively low concentrations in areas with
a higher-energy regime, is also likely a function of sedimentation processes.
As previously described from the Bahamas regions (Winland and Matthews,
1974; Hine et al., 1981; Park, 2012), sedimentation processes are highly
affected by tidal currents and wave and wind action. Areas with the highest test
densities may thus be assumed to represent accumulation areas linked to
lower current velocities and less impact from winds due to the distance to
the tidal inflow and with the presence of dense seagrass meadows acting as
sediment traps. In contrast, abrasion and resuspension in a higher-energy
regime likely dominate areas with a low dead foraminiferal density, most
prominent at sites close to the tidal inflow and areas with solid bedrock in
the subsurface. Such an overprint of the autochthonous foraminiferal
thanatocoenosis is often governed by post-mortem lateral transport and
energy-controlled facies mixing (Ginsburg and Lowenstam, 1958; Taylor and
Lewis, 1970; Miller, 1988). A similar distribution pattern was observed in a
sedimentological study in the same area (Colby and Boardman, 1989).
In contrast, Martin and Wright (1988) in a study off Florida found little
impact of sediment processes on the thanatocoenosis, instead linking the
differences between the biocoenosis and the thanatocoenosis to different
post-mortem test preservation in different species. As the dead specimens in
our study were overall well preserved, including the smaller more fragile
taxa, we cannot confirm significant post-mortem test preservation as the
main cause for the differences between the living epiphytic assemblages
on the macrophytes and the dead assemblage in the sediment. However, we also
cannot rule out that differential preservation plays some role, as Buchan
and Lewis (2009) and Darroch et al. (2016) have in fact described some
degradation, especially in dead Archaias angulatus from Grahams Harbour. Furthermore, the
near absence of Sorites marginalis in the thanatocoenosis, despite it being the dominant
species living on the macroalgae, indeed supports the conclusion that test
degradation may also play a role (see Martin and Wright, 1988; Buchan and
Lewis, 2009).
The accumulation of foraminiferal tests in nearshore environments is
generally believed to be macrophyte dependent, though sediment mixing occurs
through lateral transport linked to energy-controlled processes, e.g. tidal
currents or longshore currents (Ginsburg and Lowenstam, 1958; Taylor and
Lewis, 1970; Miller, 1988). A secondary shift in the grain matrix may also
occur due to tropical storms and hurricanes hitting the Bahamian
archipelago annually with maximum intensities in September–October (Colby
and Boardman, 1989; Park, 2012).
Swinchatt (1965) and Scoffin (1970) suggested that the macrophyte cover
determines the depositional environment in shallow bays of the Bahamian
islands as it tends to control the sorting and sediment deposition. It would
thus cause a reduction in grain size in habitats with dense macrophyte cover, e.g.
in connection to Thalassia mats. Although fine sand made up a major
component of the sediment in our study area, a relatively higher abundance
of coarser grains was in fact found in the surface sediment of
Thalassia-dominated habitats. Our findings are thus in accordance with those of Colby
and Boardman (1989) that coarse grains were more abundant in the
Thalassia-vegetated areas of Grahams Harbour. It thus supports the interpretation
that sedimentation patterns, and consequently post-mortem transport of
foraminiferal tests, is governed by strong lateral sediment transport caused
by longshore currents, although the influence of strong storms and
hurricanes cannot be excluded. This conclusion is further supported by the
fact that in our study dead epiphytic foraminifera were also abundant at
locations without any macrophytes. Thus although plant cover does play a
role for the dead assemblages, this factor is largely overprinted by the
consequences of sediment transport (see also Winland and Matthews, 1974;
Hine et al., 1981).
Living foraminifera were only found in low abundances in the
surface sediments and a relatively richer living foraminiferal assemblage
was only found in the epiphytic foraminiferal community attached to
macrophytes at these sites (Table 3; see also discussion below). The overall
very low abundance of living foraminifera in the surface sediments at
Grahams Harbour is in agreement with earlier reports in oligotrophic
nearshore sediments in the Caribbean of a general scarcity of living
foraminifera, the majority of which adopt an epiphytic life style (Langer,
1993; Wilson, 1998; Wilson and Ramsock, 2007). Due to this limited amount
of data on living foraminifera in the present study, a more precise
definition of habitat preferences of the living foraminifera could not be
investigated. Nevertheless, our study suggests that sedimentation processes
also strongly impact the distribution of living foraminifera in the surface
sediments in the area. The presence of stainable foraminiferal tests in the
sediment was found to be restricted to the middle part of the transect
(sample sites GH12-05 to GH12-12), where moderate current strength and wave
action cause relatively stable sediment transport and deposition. In
contrast, habitats with either a high- or a low-energy regime and thus with
either sediment abrasion or strong accumulation were barren of living
foraminifera. Examples are sites close to the Cut (sample sites GH12-13,
GH12-14) and close to the Old Dock (i.e. sample sites GH12-01, GH12-02). This pattern suggests that a moderate energy regime is more
hospitable for colonization by living foraminifera than higher-energy
environments.
The role of macroalgae Halimeda
The relation between macrophyte biomass and foraminiferal assemblages is
difficult to ascertain due to the carbonate encrustations of the algae,
making estimations of biomass imprecise. However, our results indicate that
when variation associated with grain size has been partialled out, the
calcareous macroalgae Halimeda incrassata accounts for a significant fraction of the residual
foraminiferal variation of the thanatocoenoses. In general, Halimeda is highly
abundant in shallow bays in the northern Caribbean, especially on coarse or
solid substrates (Brasier, 1975; Hillis-Colinvaux, 1980; Liddell et al.,
1988; Davaud and Septfontaine, 1995). Halimeda is colonized by various epiphytic
foraminifera (Wilson, 2007; Buchan and Lewis, 2009). Compared to
seagrasses, e.g. Thalassia that forms up to 50 cm long leaves (Littler et al.,
1989), the inhabitable surface area on Halimeda thalli is small (thallus size of only
2–5 cm; Littler et al., 1989; Multer and Clavijo, 2004), and Wilson (2008)
reported a further areal limitation of those foraminiferal colonies that do
not grow over the entire macrophyte leaf. In spite of its short life span
of only a few weeks (Multer and Clavijo, 2004), Halimeda contributes between 15 % and
50 % of the total carbonate production in shallow, tropical marine realms
(Scoffin and Tudhope, 1985; Liddell et al., 1988; Darroch, 2012, varying
Multer and Clavijo, 2004). Due to thallus fragility, high-energy processes
such as increased wave action during storms and strong currents may result
in high spalling rates. Halimeda is reported as a primary producer of sea-floor
sediments in nearshore environments and may also enhance the accumulation
of particulate organic matter (Multer and Clavijo, 2004). Through its
contribution to carbonate production it also influences habitat
chemistry (Elliot et al., 1998), which can be expected to affect the local
foraminiferal fauna and its preservation. The fact that Halimeda is primarily found
in more open vegetation in our study area may also explain the link between
Halimeda and dead epiphytic foraminifera in the sediments: such areas are subject to
sediment transport shown by the RDA to be the main controlling factor (Fig. 5).
However, these areas also form the open vegetation still acting as a
depositional area for the allochthonous foraminiferal specimens. If this
hypothesis is correct, it would mean that Halimeda is not in itself the cause of the
increased presence of dead epiphytic foraminifera in the sediment, but
rather that the habitat dominated by Halimeda offers the best conditions for
sediment deposition, including deposition of the empty foraminiferal tests
transported form surrounding areas.
Living and dead epiphytic foraminiferal assemblages
As is quite common in tropical shallow marine habitats with sandy
substrates, our sample sites showed distinctive variations in living
epiphytic foraminiferal species distribution between sites with unvegetated,
sparse colonization of calcareous macroalgae (mainly Halimeda and Penicillus) and those with
dense seagrass meadows dominated by Thalassia and Syringodium (Table 2, Hillis-Colinvaux, 1980;
Littler et al., 1989; Gerace et al., 1998; Buchan and Lewis, 2009; Farid et
al., 2008). The number of living foraminifera on the macrophytes is overall
low compared to some earlier studies (e.g. Wilson, 2008), but similar in
magnitude to those found in other investigations (e.g. Wilson, 1989). The
observed differences in species composition of the living foraminiferal
assemblages between the various macrophytic habitats (Table 1) are likely
controlled by habitat selection: macroalgal habitats are reported to be
primarily colonized by pioneering foraminifera, while more diverse
foraminiferal communities are found in seagrass meadows (Wilson and
Ramsook, 2007). Furthermore, Morgan and Lewis (2010) observed
substrate-dependent colonization in which calcareous algae were inhabited by
the Rosalina–Discorbis group, whereas Planorbulina spp. dominated the Thalassia habitats. Walker et al. (2011)
identified a foraminiferal community living attached to shells. However, our
study shows some differences compared to these previous studies: in sparsely
vegetated habitats at Grahams Harbour (typically M1 habitats) dominated by
Halimeda, Udotea and Penicillus, specimens of Archaias angulatus,
Sorites marginalis and Planorbulina sp. were found. Seagrass-covered habitats at
Grahams Harbour (mainly M3 habitats) were primarily inhabited by the genera
Cornuspira, Laevipeneroplis, Planorbulina and Sorites. A substrate-dependent foraminiferal assemblage of specific
species could not be confirmed here and due to the limited macrophyte
material in the present study it was not possible to statistically compare
foraminiferal communities from algal and seagrass habitats. Morgan and
Lewis (2010) suggest that current regimes may determine colonization by
different epiphytic foraminiferal species. In our study the highest
abundance of epiphytic foraminifera attached to macrophyte leaves was
observed in the Thalassia habitat (M3) close to the Cut (GH12-12), where currents are
strong. This supports the suggestion by Langer (1993) that vegetation
density and diversity, including the relative algae-to-plant ratio, seems to
control the distribution of epiphytic foraminifera that colonize
shallow marine macrophyte habitats.
Due to a high calcification rate in the area (Mylroie and Carew, 2010), the
surface sediments analysed here likely only contain biogenic material from
the last few years, lessening the risk of mixing with older sediments of a
potentially different palaeoenvironment, although some mixing due to
hurricane activity cannot be ruled out. Moreover, macrophyte habitats,
especially Thalassia meadows, have life spans lasting several years (Wilson, 2008) and
they are relatively resistant to damage by storms and hurricanes (Thomas et
al., 1961; Wilson and Ramsook, 2007). A stabilization of the sediment by
rhizomes and a reduction of current energy due to leaves is especially
supported in densely vegetated areas with Thalassia and Syringodium. Satellite images of our
study site in fact suggest very little change in the marine vegetation cover
in recent years (source: Google Earth, accessed to 20 February 2013,
comparing satellite images within the previous 5 years). Thus, it is
unlikely that any difference between epiphytic biocoenoses and
thanatocoenoses at the same site is due to a change in macrophyte
community over time. Hence, comparison of the living and dead epiphytic
assemblages may be used to test the correlation between macrophytes and both
living and dead epiphytic foraminiferal faunas.
Comparing the living epiphytic community from the macroalgae with the dead
assemblages of epiphytic species in the sediment, both living and dead
epiphytic-type I assemblages seem to follow a similar trend in abundance
across habitats, with maximum densities in Thalassia–Syringodium (M3) beds (Figs. 3b, 4). However,
a discrepancy is observed at sample station GH12-12, showing a high number
of living specimens on the fibrous substrate, while the concentration of
dead epiphytic (type I) foraminifera in the sediment is very low. The
proximity of this site to the relatively high-energy regime near the current
inflow suggests that the observed disproportion between the dead and living
test density may be due to lateral sediment transport removing the dead
epiphytic-type I foraminifera.
The comparison also illustrates some dissimilarity with respect to species
dominance. Thalassia–Syringodium-vegetated habitats in strong current settings close to the Cut
(Fig. 1b) are generally dominated by Archaias angulatus and Rosalina subaraucana in the dead epiphytic-type I
assemblage, while Cornuspira sp. and the Rosalina–Discorbis group dominate the living community on the
macrophyte leaves at the same sites. In the similar macrophyte community of
the low-energy habitats proximal to the Old Dock (Fig. 1b) Sorites marginalis seems to
dominate the living community, whereas the Rosalina–Discorbis group and Planorbulina sp. characterize the
dead epiphytic-type I assemblage. A similar scenario was noticed by Wilson
(2008), who attributed this phenomenon to longshore transport of the
macrophytes with their attached epiphytic biocoenosis through current
activity or storms. Other possible explanations include differences in
breakage, hydrodynamic properties, sedimentation rates or possibly even
test production rates. Kloos (1980) suggested that the dominance of Sorites marginalis may be
attributed to seasonal blooms, which highlights the possibility that the
living foraminiferal assemblage is only a momentary snapshot of the
environmental conditions in the habitat and does not represent the
average living assemblage. Seasonal changes in epiphytic foraminiferal
density on different macrophytes were in fact reported from shallow marine
habitats on Nevis in the NE Caribbean by Wilson (2008).
Conclusions
Living and dead benthic foraminifera in surface sediments and from
macroalgae were studied at 14 sample sites along a 500 m long nearshore
transect at Grahams Harbour, San Salvador Island, Bahamas, to investigate
the abundance and distribution of living vs. dead foraminifera in relation
to habitat conditions. A main focus was on the comparison between epiphytic
populations found living on the macroalgae and dead assemblages in the
sediment, among others, to evaluate the reliability of epiphytic species in
sediments as a proxy for past macroalgae and vegetation cover.
Foraminiferal tests of the thanatocoenosis were highly abundant and
contributed to the grain matrix with up to 6200 tests per gram of surface
sediment at Grahams Harbour. Habitats with the highest current and wave
action regime contained less foraminifera per gram than areas with a more
moderate energy environment, presumably due to abrasion and accumulation
processes overprinting an autochthonous thanatocoenosis. Living (stained)
foraminifera were much rarer with maximum abundances reaching 44 specimens
per gram of surface sediment (1–3 living foraminifera per 100 dead
foraminiferal tests). In addition to the oligotrophic conditions, the energy
regimes at the sea floor seem to restrict the occurrence of living specimens
as no living foraminifera were found in areas with either a very high
(inducing grain abrasion) or a low current strength (resulting in grain
accumulation), i.e. close to the tidal inflow and distal of the tidal
inflow, respectively.
Our study showed that despite the fact that the foraminiferal assemblage
living on the macrophytes was dominated by Sorites marginalis, none were found in the dead
assemblages in the sediments; the same was the case for Peneropolis sp. Thus, there was
a significant difference in the living epiphytic assemblage and the dead
assemblage. Multivariate analyses suggest that the thanatocoenoses of
epiphytic-type I (permanently to temporary attached) foraminifera in the
shallow-water sediments of this tropical island are mainly determined by
sediment transport, i.e. sorting by grain size through sediment transport.
Specimens were overall well preserved and we also find smaller, more fragile
taxa such as Spirillina sp. and Elphidium sp. in the thanatocoenosis. We could therefore not
confirm post-mortem test preservation as a main cause for the differences
between biocoenosis and thanatocoenosis as previously reported from other
areas (e.g. Martin and Wright, 1988).
The area of macrophyte cover and diversity also seems to affect the
foraminiferal abundance to some extent. There was no discernible significant
link between habitat type (density of vegetation) and the frequency or
concentration of epiphytic foraminifera in the sediment. However, our
statistical analyses found the macrophyte Halimeda incrassata to have a significant correlation
with the foraminiferal assemblage composition, indicating that this
macrophyte may act as a sediment trap.
Consequently, our study suggests that in shallow-water tropical areas the
epiphytic (type I) component of a dead foraminiferal assemblage may not
always give a reliable indication of the past macrophyte cover in the
region. It furthermore indicates that in carbonate platform regions,
epiphytic species should only be used cautiously as direct indicators of
past in situ macroalgae growth, as previously suggested by Reich et al. (2015) and
references herein.
All main data are already included in the paper. Further information and
raw data can be requested from the authors.
AF and MSS designed the
study, and AF carried out the fieldwork and foraminiferal analyses. BVO and AF carried out
the statistical treatments. AF wrote the first draft of paper, and all authors provided comments
and corrections.
The authors declare that they have no conflict of
interest.
Acknowledgements
We gratefully thank Dena Smith, Michal Kowalewski and Thomas Rothfuss
as well as the staff of the Gerace Research Centre, San Salvador, for their
assistance during the field work on San Salvador. We thank Simon Darroch for
his help and suggestions during the early stage of this study. The
Paleontological Society, Graduate School of Science and Technology (GSST)
at Aarhus University, Denmark, as well as the Independent Research Fund
Denmark projects TROPOLINK, OCEANHEAT and G-ICE (project nos. 09–069833/FNU,
12–126709/FNU and 7014-00113B/FNU), and the Knud-Højgaard Fond in Denmark
are gratefully thanked for their financial support. The two reviewers, Simon Darroch
and Ronald Lewis, as well as the journal editor Laia Alegret are
thanked for their thorough comments and constructive suggestions for
improving the paper.
Edited by: Laia Alegret
Reviewed by: Simon Darroch and Ronald Lewis
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