Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
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Palaeogeography, Palaeoclimatology, Palaeoecology
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p a l a e o
Alpha and beta diversity of encrusting foraminifera that recruit to long-term
experiments along a carbonate platform-to-slope gradient: Paleoecological
and paleoenvironmental implications
Sally E. Walker a,⁎, Karla Parsons-Hubbard b, Suzanne Richardson-White a, Carlton Brett c, Eric Powell d
a
Department of Geology, University of Georgia, Athens, GA 30602, USA
Department of Geology, Oberlin College, 52 W. Lorain Street, Oberlin, OH 44074, USA
c
Department of Geology, University of Cincinnati, Cincinnati, OH 45221, USA
d
Haskin Shellfish Research Laboratory, Rutgers University, 6959 Miller Avenue, Port Norris, NJ 08349, USA
b
a r t i c l e
i n f o
Article history:
Received 13 August 2010
Received in revised form 21 April 2011
Accepted 21 April 2011
Available online 4 May 2011
Keywords:
Beta diversity
Dispersal
Invasibility
Ecological incumbent
Encrusting foraminifera
Opportunistic
Carbonates
a b s t r a c t
The spatial and temporal distribution and diversity of sediment-dwelling foraminifera are reasonably well
known, but encrusting (hard-substrate dwelling) foraminifera are little studied. Encrusting foraminifera are
common in the world's oceans, attached to floating debris or marine animals in the water column to living on
rocks, sand grains and organisms in benthic environments from shallow to deep marine regions. With
projected ocean acidification and warming conditions, these important calcifying protists that comprise
beaches, buffer sediments, and contribute to complex food webs are potentially in peril.
Results indicate that calcifying foraminifera were the first to colonize experimental molluscan substrates
within the first year in shallow habitats, with colonization offshore in subsequent years. Agglutinated
foraminifera become more common after one year. Species richness (α diversity) remained relatively similar
throughout the study, but species turnover (β diversity) was greatest within the first year and between the
shelf/slope break and deeper water, following the thermocline and photic zone regions. The equivalent of the
Shannon Entropy Index provided important information on β diversity and community structure.
Paleobathymetric distributions can be resolved after six years into four distinct foraminiferal distributional
zones: shallow shelf (15 m), outer shelf (33 m), shelf/slope break (73–88 m), and slope depths (N 213 m to
267 m). Some encrusting foraminifera are invasive, settling in high numbers within the first year, and
increasing their abundance through the duration of the experiment. A foraminiferan, Discorbis bertheloti, was
discovered to bioerode carbonate, and is a potentially excellent paleobathymetric indicator for 15–33 m
depths. Results differ from previously reported pioneer and climax foraminiferal communities documented
for Caribbean coral reefs, because long-term experiments reveal the spatial and temporal development and
distribution of carbonate-producing encrusting foraminifera in these climatically-sensitive regions.
© 2011 Elsevier B.V. All rights reserved.
1. Introduction
Encrusting organisms that grow attached or cemented to hard
substrates create communities that may reflect ambient environmental conditions. If these organisms secrete hard skeletons, they can be
preserved in the fossil record and thereby become valuable tools in
paleoecological and paleoenvironmental analysis (Taylor and Wilson,
2003). Because of this potential, studies have focused on encrusting
organisms that recruit to corals or coral rubble (Palmieri and Jell,
1985; Gischler and Ginsburg, 1996; Hart and Kench, 2007), cavity
⁎ Corresponding author.
E-mail addresses: [email protected] (S.E. Walker), [email protected]
(K. Parsons-Hubbard), [email protected] (S. Richardson-White),
[email protected] (C. Brett), [email protected] (E. Powell).
0031-0182/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.palaeo.2011.04.028
surfaces (Rasmussen and Brett, 1985; Holmes et al., 1997; Richter et
al., 2001), molluscan shells (Driscoll and Swanson, 1973; Walker,
1988; Walker and Carlton, 1995; Parsons-Hubbard, 2005) and many
other invertebrate substrates (e.g., Jackson and Buss, 1975; Osman,
1977; Sutherland and Karlson, 1977; Jackson, 1979; Mook, 1981;
Greene et al., 1983; Nebelsick et al., 1997; Patil and Anil, 2000;
Rodland et al., 2006). Despite these studies, there is limited
knowledge about how encrusting organisms vary along environmental gradients (Martindale, 1992; Walker et al., 1998; Parsons-Hubbard
et al., 1999; Lescinsky et al., 2002; Parsons-Hubbard, 2005; Mallela,
2007). Additionally, little is known about encrusting species diversity
(species richness, α diversity), abundance and species turnover (β)
and how these diversities vary spatially and temporally. Such studies
would refine the ecological dynamics that underpin paleoecological,
paleoenviromental and paleoclimatic reconstructions (Debenay and
Payri, 2010).
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S.E. Walker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
The present study focuses on foraminifera that encrust experimentally-deployed molluscan shells to examine diversity (species
richness, α and β) and abundance with depth and time across a
carbonate bathymetric gradient to determine: (1) whether assemblages of encrusting foraminifera are relatively stable, (2) how long it
takes for encrusting species to recruit to the substrates (invasibility or
colonization rate), and (3) whether predictions about the utility of
foraminiferal encrusting associations can be made for the fossil
record. Additionally, we tested various beta (β) diversity metrics,
including equivalents of Shannon Entropy (Jost, 2007), to find a β
metric that best captures foraminiferal species turnover.
Jost (2006, 2007) cogently argued that equivalents of Shannon
Entropy could represent true diversity. Following MacArthur (1965)
and Hill (1973), Jost (2007) showed that most estimates of β diversity
(e.g., Whittaker, 1965, βw; Lande, 1996, βadd) were biased because β
did not function independently of α (local diversity). Therefore, we
focused on using the equivalent of the Shannon Entropy Index (after
Jost, 2006, 2007) and compared it to additive and multiplicative β
diversity indices to understand the turnover dynamics of encrusting
foraminifera with depth and by year.
With global climate change and the resulting mass overturn of
species diversity in relation to shifting food webs (Richardson and
Schoeman, 2004; Frank et al., 2005; Parmesan, 2006; O'Conner et al.,
2009), it is crucial to have reliable and quantifiable species diversity
metrics that can be applied globally and across regions. Diversity
metrics are also very important for applications to the fossil record
that focus on past climate and environmental change (Olszewski,
2004; Patzkowsky and Holland, 2007; Holland, 2010; Wilson, 2011).
Majorities of encrusting foraminifera are small (b1 mm) and their
community dynamics may be more readily observed on smaller
substrates, such as molluscan shells or rocks. They may be invaluable
for evaluating ancient environments where fossilization may only
preserve hard substrates and skeletal debris, such as those that occur
at transgressive lags or flooding surfaces (refer to Brett, 1995;
Holland, 1995). Encrusting foraminifera also contribute to the
geologic record of reefs (Palmieri and Jell, 1985; Rasser and Piller,
1997; Bosellini and Papazzoni, 2003; Varrone and d'Atri, 2007) and,
like benthic foraminifera (e.g., Hallock et al., 1986; Murray, 2006),
they produce carbonate, but are often not considered in relation to the
carbonate budget of benthic and pelagic systems.
1.1. Background on encrusting foraminifera
Encrusting foraminifera include attached species (those that
attach by granuloreticulopods, like Amphistigina gibbosa), cemented
species (those that adhere to the substrate using an organic adhesive,
such as Rosalina globularis), and cemented species that also bore into
the substrate, such as Cibicides refulgens in Antarctica (Alexander and
DeLaca, 1987). Encrusting foraminifera are found at all depths and in
most depositional settings where suitable substrates occur, such as
manganese nodules in the deep sea (Mullineaux, 1988), inside the
tubes of deep-sea agglutinated foraminifera (Gooday and Haynes,
1983), on shallow water sea grass blades and algae (Hallock et al.,
1986; Martin, 1986; Langer, 1993), on invertebrates (Langer and Bagi,
1994) and on floating plastic debris (Gregory, 2009) among many
other substrates (Cushman, 1910; Korringa, 1951; Nyholm, 1961;
DeLaca and Lipps, 1972; Gooday and Haynes, 1983; Lipps, 1983;
Alexander and DeLaca, 1987; Mullineaux, 1987, 1988; Alve, 1995;
Resig and Glenn, 1997; Zampi et al., 1997; Mullineaux et al., 1998;
Alve, 1999; Vénec-Peyré, 2004; Murray, 2006; Richardson, 2006;
Mateu-Vicens et al., 2010). Encrusting foraminifera have a fossil
record dating back to the late Ordovician (Moreman, 1933), while
sediment-dwelling (benthic) calcareous and agglutinated foraminifera extend to the Cambrian (Riding and Brasier, 1975; McIlroy et al.,
2001; Scott et al., 2003).
Shallow-water encrusting foraminifera are the most studied
(Palmieri and Jell, 1985; Prager and Ginsburg, 1989; Martindale,
1992; Langer, 1993; Kitazato, 1994; Elliott et al., 1996; Gischler and
Ginsburg, 1996; Beaulieu, 2001; Wilson and Ramsook, 2007), but at
depths greater than SCUBA-diving depths (N25 m), much less is
known about encrusting foraminifera. Indeed, unlike sedimentdwelling foraminifera (i.e., Lee et al., 1980; Buzas et al., 1989; Alve,
1999; Alve and Olsgald, 1999; Fujita, 2004) few studies have
experimentally investigated the temporal dynamics of encrusting
foraminifera across shelf-and-slope habitats. Experiments of less than
six-months in duration have been done on encrusting foraminifera in
shallow-water habitats (b30 m; reviewed by Alve, 1999; Ribes et al.,
2000; Fujita, 2004); and, in deep-sea habitats, experiments have run
for up to three years (N2000 m; e.g., Van Dover, 1988; Mullineaux
et al., 1998). There are few experimental studies that bridge the gap
between shallow shelf and deep-sea environments (Parsons-Hubbard
et al., 1997; Walker et al., 1998).
Benthic foraminifera are important in modern seas as indicators of
water quality, pollution, eutrophication, paleoenvironments and
paleobathymetry (e.g., Alve, 1995; Goldstein, 1999; Hallock, 2000;
Hallock et al., 2003; Murray, 2006; Richardson, 2006; Uthicke and
Nobes, 2008; Martinez-Colón et al., 2009; Sen Gupta and Smith, 2010;
Gooday, in press), and encrusting foraminifera may be just as
important. For example, enhanced nutrient run-off from seabird
rookeries increased diversity but lowered the density of encrusting
foraminifera in sea grass beds, suggesting that encrusting foraminifera
could be used as indicators of eutrophic conditions in modern and
past ecosystems (Richardson, 2006).
Because of their long fossil record dating back to the early
Paleozoic, encrusting foraminifera may be invaluable for paleogeographic, paleoecological, and taphofacies studies. In the early Eocene
of Europe, encrusting acervulinid foraminifera constructed large
(8 × 2 km wide) reefs (Perrin, 1987; Plaziat and Perrin, 1992). These
unusual foraminifera grew much deeper than corals, extending
framework reefs into the deep sea during that time (Plaziat and
Perrin, 1992). Encrusting foraminifera may settle on specific locations
on the host shells, indicating feeding behavior of the fossil host
(Zumwalt and DeLaca, 1980) or parasitism, as in the case of Recent
Cibicides refulgens that live on the shells of the Antarctic scallop,
Adamussium colbecki (Alexander and DeLaca, 1987). Still, there is
limited knowledge about the utility of these foraminifera in
taphofacies analysis, especially how they vary along environmental
gradients or among different habitats within the same ecosystem
(Choi and Ginsburg, 1983; Choi, 1984; Mallela, 2007). Perhaps this is
because foraminifera are generally overlooked in favor of encrusting
invertebrates or algae, such as bryozoans, serpulid polychaetes and
coralline algae (Debenay and Payri, 2010). This need not be the case,
as we posit that encrusting foraminifera are just as important
members in structuring communities on hard substrates, whether
the substrates are sand grains on the sea floor or floating marine
debris (see Kitazato, 1994; Gregory, 2009).
2. Methods
2.1. Study site and deployment depths
Experiments were deployed in 1993 along two transects, AA and
BA, located on the eastern margin (windward side) of Lee Stocking
Island, Exuma Cays (Fig. 1). For this paper, only the AA experiments
will be discussed (for the BA transect data, see Richardson-White and
Walker, this issue). The AA transect has been used for coral reef
studies since the 1970s, including research on coral bleaching
(Manzello et al., 2009) and microbial bioerosion of reef substrates
(Vogel et al., 2007). The AA transect is also used by the Shelf-andSlope Experimental Taphonomy Initiative project (SSETI) to examine
carbonate accumulation, bioerosion, and chemical/physical factors
S.E. Walker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
327
Fig. 1. The study area, Lee Stocking Island, is located on the southwest side of Exuma Sound. The Caribbean Marine Research Center (CMRC) provided laboratory and field support and
experiments were deployed and collected along transect AA located perpendicular to the shelf edge northeast of CMRC.
that affect the taphonomy of macroinvertebrate hard parts and wood
(various authors, this issue).
Experiments were emplaced along the AA transect by SCUBA
divers at 15 m and 33 m, and below this depth, experiments were
deployed by submersibles to 267 m (Nekton Delta, Nekton Gamma and
Clelia) (Fig. 2). Deployment sites ranged from shallow hardground to
deep aphotic slope (Table 1). Lee Stocking's carbonate platform
extends approximately 2 km oceanward to the shelf/slope break at
88 m. Fringing and patch reefs are common on the platform (Kendall
et al., 1989). From the shelf/slope break, topography drops precipitously (called the Exuma Wall) to approximately 200 m, then
continues at a slope of 60° to 2000 m in water depth (Pitts and
Smith, 1993; Smith, 2001). The shelf/slope break topography records
the Wisconsin low still stand that occurred at 100 m below present
mean sea level (Liddell and Ohlhorst, 1988). Circulation in Exuma
Sound is dominated by large-scale gyres that extend to 200 m; water
regularly exchanges between the Atlantic Ocean and the shallow
carbonate banks (Colin, 1995; Stockhausen and Lipcius, 2001).
Sea Surface Temperatures (SST) remain relatively stable at Lee
Stocking Island: a ten-year seasonal record indicates winter temperatures of 23 °C ranging to 29 °C in summer (van Woesik et al., 2010).
Marine temperatures along the AA transect rapidly change from 29 °C
on the platform to 24 °C at 100 m, then decline steadily to about 19 °C
at the deepest site (267 m). Salinity increases from 36.7 ppt to 37.3 ppt
in the vicinity of 100 m, but returns to 36.7 ppt below 150 m (Hickey et
al., 2000). The photic zone in the Caribbean region (designated as 1.0%
of surface illumination) extends to 65 m, with 0.05% illumination to
110 m (Brakel, 1979; Liddell and Ohlhorst, 1988).
2.2. Experimental design
Deployed shells included five replicates each of two gastropod
species that were commercially available: the Philippine mud snail,
Telescopium telescopium, and the conch, Strombus luhuanus. Importantly,
Fig. 2. Shelf-slope deployment sites demarcated by depths along the AA transect. Sites
are: shallow shelf (15 m), outer shelf (33 m), shelf/slope break (73 m, 88 m), and slope
or bathyal sites (213 m, 264 m, and 267 m).
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Table 1
Description of deployment site, depth, habitat and site (substrate) description, collection interval and the burial state of the deployed mesh bags upon recovery.
Site
Depth
(m)
Habitat description
Site description
Collection interval
Recovery state
1 year
2 years
Fully exposed
Fully exposed, moved a short
distance by a hurricane
Buried
Partially buried
Buried
Buried
Fully exposed
Fully exposed
Fully exposed
Fully exposed
Fully exposed
Fully exposed
Fully exposed
Fully exposed
Fully exposed
Fully exposed
Partially buried
Partially buried
Fully exposed
Fully exposed
Fully exposed
AA50
15
Patch reefs, sand channels, and firm-grounds
Firm ground w/ coarse carbonate sand
AA100SO
33
Patch reefs and sand channels
Coarse carbonate sand
AA240WA
73
Steep near-vertical wall with narrow ledges
Hardground ledge
AA290WA
88
Steep near-vertical wall with narrow ledges
Hardground ledge
AA700CR
213
Talus slope with scattered allochthonous boulders
Thin veneer of fine carbonate sand
over hard bottom
AA850CR
264
Crest of relict sand dune
Fine carbonate sand
AA875TR
267
Trough of relict sand dune
Fine sand veneer over hard surface
both species have similar microstructure and mineralogy to native
species found in the area against which to compare our results (Cai et al.,
2006): Telescopium is a cerith with many common Caribbean relatives
such as Cerithium spp. Strombus also has a number of local relatives
(Strombus gigas, Strombus gallus, Strombus pugilis). All shells were clean
and deployed in mesh bags (mesh size 2 cm) and strung on weighted
PVC poles for ease of recovery via submersible (Fig. 3). The 1994 data
includes Telescopium that were deployed at 15 m, 33 m and 213 m; all
other arrays (1995, 1999) had complete sets of Telescopium for all
depths; Strombus were deployed at all depths for all years.
During the six years of this study, some shell bags were buried and
re-exhumed: one experiment at 15 m was moved a few meters from
its original deployment site by a hurricane (Table 1). Experiments
were recovered after one year (1994), two years (1995), and six years
(1999) via SCUBA for shallow sites (15 m, 33 m) and via submersible
for deeper sites (N33 m). Upon recovery, each shell was gently rinsed
of sediment and photographed.
Note: shells that were not in bags or tethered were also deployed
in 1993 at AA transect sites, but none were recovered from the
shallow shelf to upper bathyal sites (to 213 m). Shells from slope sites
6 years
1 year
2 years
6 years
1 year
2 years
6 years
1 year
2 years
6 years
1 year
2 years
6 years
1 year
2 years
6 years
1 year
2 years
6 years
(264–267 m) were recovered, but there was no statistical difference
between those shells and the bagged shells.
2.3. Taxonomic composition and alpha diversity
All foraminifera were identified by the first two authors under wet
and dry conditions using a dissecting scope at high magnification and
a Scanning Electron Microscope (SEM). Whenever possible, foraminiferal experts (R. Martin, P. Hallock and S. Goldstein) verified species.
Foraminifera were not stained with rose bengal or other live-tissue
marker, so the results presented here conservatively represent live
plus dead encrusting foraminifera. Rose bengal staining is an
imperfect method because the stain can be retained in organic matter
from foraminiferal skeletons (tests) even after the living foraminiferan has died (Boltovskoy and Lena, 1970; Murray and Bowser, 2000).
The focus of our work was to treat the modern specimens as if they
were already fossils, providing a snapshot of live + dead encrusting
assemblages of foraminifera with time. Total abundance and average
abundance of live + dead foraminiferal species that encrust
Telescopium and Strombus shells were analyzed.
Species richness (S, numbers of species; also a type of α diversity),
Shannon Entropy Index (H), and evenness (Pielou's J) were analyzed
for each year by depth. The Shannon Entropy Index is an information
statistic, with lower H values indicating that the assemblage or
community is affected by dominance, and higher H values indicating
equitable distributions of individuals among its species. The Shannon
Entropy Index is calculated as follows:
S
H = − ∑ pi ln pi
i=1
where H is Shannon Entropy and pi is the proportion of each species in
the sample (Hayek and Buzas, 1997). Evenness was calculated to
determine if individuals were equally partitioned among the species
per each depth using Pielou's J evenness metric:
J = H = ln ðSÞ
Fig. 3. Experimental array showing mesh bags tied to PVC rod. A polyethylene float is
tied to one end of the rod with a 4.5 kg weight to offset the flotation. The float allows the
experimental array to be easily relocated after many years on the sea floor.
where J is Pielou's evenness metric, H is the Shannon Entropy Index,
and S is species richness (Hayek and Buzas, 1997). Evenness (J) ranges
from 0 (individuals are distributed disproportionately among the
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S.E. Walker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
species, indicating dominance) to 1 (individuals are equally distributed among the species).
2.4. Beta-diversity metrics
To determine the turnover of species per depth and per year, four β
metrics were used and compared: (1) simple counts of turnover based
on unique species that were not shared between depths or time
periods, herein called “βcounts”; (2) Whittaker's β which is a
multiplicative process where total diversity (gamma or γ) is divided
by average local diversity (average alpha, or α̅): (βw = γ / α̅)
(Whittaker, 1965); (3) additive β, which is calculated by subtracting
average alpha from gamma (βadd = γ − α̅) (Lande, 1996); and (4)
calculating the Shannon Entropy Index and taking its equivalent for
both alpha and gamma diversity to calculate the equivalent β (herein
called βJost based on Jost, 2006, 2007).
Jost (2006, 2007) found that by converting the classic Shannon
Entropy Index (H) to its equivalent, exp(H) (also called: e H, eH, or
effective species diversity), that it represents true species richness if
the samples have individuals that are equally distributed among the
species. Jost's exp(H) gives an approximation of the dominant species
when individuals among species within the sample or community are
not equally distributed. Hence, taking the equivalent of the Shannon
Entropy can approximate true diversity when all species are equitably
distributed and also provides insights into community structure when
individuals among species are not equitably distributed.
2.5. Density of encrusting foraminifera and distributional pattern on
exposed versus unexposed shells
The number of foraminifera per cm 2 was determined by taking the
surface area of each shell and assuming that shell shape was roughly
equivalent to a right cone (Richardson-White and Walker, this issue).
Using this method, foraminiferal occurrence on each shell was
corrected for surface area and presented as the number of individuals
or number of species per cm 2. The mean shell surface area for
Telescopium telescopium was 52.5 cm 2 (n = 63, SD = 10.8) and a mean
of 34.3 cm 2 (n = 64, SD = 8.5) for Strombus luhuanus. Abundance
patterns of encrusting foraminifera on exposed (i.e., portion of
the shell exposed above the sediment–water interface) versus
unexposed regions of the shells (i.e., portion of shell below
the sediment–water interface) were analyzed using a Mann–Whitney
U-test (M–W U-Test).
Table 2
Species of encrusting foraminifera, their abundance (n) with depth (m, meters) for year
1994 and their diversity indices, Lee Stocking Island, Bahamas.
Species
15 m 33 m 88 m 213 m 267 m Totals
Acervulina inhaerens
Biarritzina
carpenteriaeformis
Caribeanella sp.
Carpenteria balaniformis
Cibicides refulgens
Cibicides lobatulus
Cibicides sp.
?Cibicorbis sp.
Cornuspiramia cf.
adherens/antillarum
Diffusilina/Iridia sp.
Discorbis bertheloti
Discorbinellidae
Gypsina globularis
Gypsina plana
Haplophragminoides sp.
Hemisphaerammina sp.
Homotrema rubrum
Neoconorbina terquemi
Nodobaculariella sp.
Placopsilina sp.
Planorbulina acervalis
Planorbulinella sp.
Rosalina-like sp.
Rotalliammina sp.
Sahulia ?patelliformis
Spirillina vivipara
Textulariella sp. Includes:
Textulariella cf. barrettii
and Textulariella cf. mayori
Tritaxis ?fusca
Unid. Foram A
Unid. Foram B
Unid. Foram C
Unid. Foram D
Unid. Foraminifera
Unid. Miliolidae
Unid. Textularidae
Total individuals
279
0
71
0
0
0
0
0
0
1
350
1
0
3
1
0
1
1
321
1
1
16
7
7
0
0
0
0
3
18
0
0
22
0
0
20
8
0
0
0
1
0
5
2
0
0
0
2
4
45
35
8
1
343
0
48
0
23
3
0
0
7
2
0
4
547
0
2
0
0
3
0
11
0
0
17
4
0
0
1
11
0
31
614
0
1
0
0
0
0
0
0
0
4
0
0
1
0
0
1
2
6
1
0
0
0
2
0
5
0
0
0
0
2
0
0
0
0
0
8
0
0
57
0
0
2
4
0
4
0
0
1
0
0
0
0
1
0
0
0
3
4
0
0
20
48
4
44
7
3
1
8
13
1
38
1175
1
3
60
4
5
2
0
73
17
1
1
0
1
0
1338
6
0
0
0
0
0
0
0
799
26
0
0
0
0
0
0
0
86
11
0
0
0
0
0
0
23
136
3
0
0
0
0
1
0
0
30
46
73
17
1
1
1
1
23
2389
20
1.57
4.83
0.52
–
15
1.00
2.72
0.37
13
12
1.81
6.14
0.73
14
9
1.73
5.64
0.79
12
12
2.31
10.11
0.93
9
γ = 35
Species richness (α)
Shannon Entropy (H)
exp(H)
Pielou's J evenness
Species turnover with
depth, βcounts
Average exp
(H): 5.9
2.6. PCA distributional patterns of encrusting foraminifera with depth
The distributions of foraminifera that encrusted Strombus and
Telescopium shells were examined for each site using Principle
Component Analysis (PCA using PC-ORD software; McCune and
Grace, 2002). PCA allows for the reduction of complex data on
abundance of multiple species to be reduced to fewer new variables.
Six-year data, corrected for surface area of each shell substrate was
used in the PCA. Species abundance data from five shells from each
species (Strombus, Telescopium) per depth were analyzed; data were
log transformed to minimize the effect of the few species that had
unusually high abundance.
3. Results
3.1. Taxonomic composition of abundant species and α and β diversity
with depth
In 1994, there were 35 species representing a total of 2389
individuals for all depths pooled; most of the richness was limited to
the shelf (Table 2). The Shannon Entropy values indicated that the five
sites were different, reflecting more dominance on the shelf and less
dominance at deeper depths. Evenness values indicate less equitability at 33 m, with the highest equitability at 267 m. The average
Shannon equivalent diversity (expH) suggest that five to six species
were dominant in 1994. Using this equivalent, the dominant species
were those that had N50 individuals (i.e., Planorbulina acervalis,
Acervulina inhaerens, Cornuspiramia adherens, Rotaliammina sp., and
unidentified foram A which appeared to be newly recruited
P. acervalis). Species turnover, based on counts, was relatively
high for all depths examined (Table 2). The pooled equivalence
(expHpooled) by depth was 29.43 species, a lower metric than counts
because of the influence of dominant taxa (Table 3). Beta diversity
among depths (βJost) was 5 for 1994, indicating that all five depths
had unique communities (Table 3).
A total of 3190 individual foraminifera encrusted the experimental
shells in 1995 for all depths pooled, and the highest species richness
occurred on the shelf and shelf/slope break sites. Taxonomic
composition included six species with greater than 100 individuals:
Planorbulina acervalis, Discorbis bertheloti, Placopsilina. sp., Rotalliammina., Tritaxis ?fusca, and Cibicides refulgens out of a total of 33 species
(Table 4). The Shannon Entropy values indicated that the seven sites
330
S.E. Walker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
Table 3
Species of encrusting foraminifera, their abundance (n) with depth (m, meters) for year 1995 and their diversity indices, Lee Stocking Island, Bahamas.
Species
15 m
33 m
73 m
88 m
213 m
264 m
267 m
Totals
Acervulina inhaerens
Amphistegina gibbosa
Ataxophragmoides sp.
Biarritzina carpenteriaeformis
Carpenteria balaniformis
Cibicides refulgens
Cibicides lobatulus
Cibicides sp.
Cornuspiramia cf. adherens/antillarum
Discorbis bertheloti
Dyocibicides ?biserialis
Gypsina globularis
Gypsina plana
Gypsina vesicularis
Haplophragminoides sp.
Hemisphaerammina sp.
Homotrema rubrum
Neoconorbina terquemi
Placopsilina sp.
Planorbulina acervalis
Planorbulinoides sp.
Rosalina-like sp.
Rotalliammina sp.
Sahulia ?patelliformis
Spirillina vivipara
?Sporadotrema sp.
Textulariella sp. includes: Textulariella cf. barrettii and Textulariella cf. mayori
Tritaxis ?fusca
Unid. Foram A
Unid. Foram D
Unid. Foraminifera
Unid. Miliolidae
Unid. Textularidae
Total individuals
35
1
4
0
3
16
4
0
8
233
0
19
12
0
0
6
14
0
55
596
0
2
0
0
4
0
0
0
0
0
0
41
0
1053
40
10
4
0
3
34
4
0
40
3
0
18
54
2
0
2
42
10
44
621
8
0
0
0
6
1
0
4
0
0
0
4
0
954
0
21
1
0
10
18
9
0
14
0
5
21
10
0
0
1
32
0
64
84
0
0
0
0
36
1
0
152
0
0
1
0
0
480
0
0
1
1
2
11
10
0
17
0
5
16
0
0
0
6
4
0
55
68
0
0
1
0
29
9
0
68
1
1
2
0
0
307
0
0
0
0
0
23
0
0
0
0
0
0
0
0
0
9
0
0
0
35
0
0
70
2
4
0
0
7
0
0
1
0
9
160
0
0
0
0
0
9
0
0
0
0
0
0
0
0
0
3
0
0
0
5
0
0
85
0
0
0
4
4
0
0
0
0
16
126
0
0
0
1
0
13
3
1
0
0
0
0
0
0
3
3
0
1
0
5
0
0
51
11
0
0
0
12
0
0
0
0
6
110
75
32
10
2
18
124
30
1
79
236
10
74
76
2
3
30
92
11
218
1414
8
2
207
13
79
11
4
247
1
1
4
45
31
3190
Species richness (α)
Shannon Entropy (H)
exp(H)
Pielou's J
Species turnover with depth βcounts
17
1.459
4.301
0.52
–
were different but that there was more equitability in species
distribution at the shelf/slope break sites (73 m, 88 m). The average
Shannon equivalent diversity (expH) indicated that six species were
dominant (i.e., the species listed above). The highest equitability
occurred at 213 m, with the lowest equitability at 15–33 m. Species
turnover was relatively moderate for all depths except between 88 m
and 213 m, where the highest species turnover occurred in 1995
(Table 4). In 1995, exp(Hpooled) was 40.72 when in fact there were 33
species that year based on species richness (Table 3). βJost for 1995
was 7, and there were seven sites at different depths, illustrating that
these depths were unique in species compositions (Table 3).
After six years, taxonomic composition included 11 species each
with N100 individuals out of a total of 34 species and 5193 individuals
(Table 5). Unlike the other two deployment years, there were three
major patterns for these common species: species that were restricted
to the shelf (b33 m: Acervulina inhaerens, Discorbis bertheloti), species
that were restricted to the shelf and shelf/slope break (b88 m:
Cornuspiramia cf. adherens/antillarum, Homotrema rubrum, unidentified Miliolidae), and species that occurred across all depths (15–
267 m: Cibicides refulgens, Placopsilina sp., Planorbulina acervalis,
Spirillina vivipara, and unidentified Textularidae). The highest species
richness occurred at 15 m and 88 m (Table 5). The Shannon Entropy
values indicated that the six depths were slightly different reflecting
more equitability of species distributions, with the 33-m site
exhibiting dominance. The Shannon equivalent diversities suggest
that five to ten species (average 8 species) were dominant in 1999
depending on the depth (Table 5). Evenness values were equitable
among most depths, with the 33-m site having the least equability.
21
1.509
4.526
0.50
6
17
2.148
8.567
0.76
8
19
2.207
9.088
0.75
6
9
1.612
5.013
0.91
14
7
1.152
3.165
0.59
4
12
1.802
6.067
0.73
7
γ = 33
Average exp(H): 5.8
Species turnover (βcounts) was moderately high for most depths; and,
like 1995, species turnover was highest between 88 m and 213 m
(Table 5). βJost for 1999 was 6, representing six depths with
distinguishable foraminiferal communities (Table 3). Based on exp
(Hpooled) there were 45 species in 1999, yet 34 species actually
occurred in 1996. What is remarkable is that the exp(Hpooled) of 1999
does reflect the total gamma diversity, 45 species, for the entire sixyear study (Table 3).
In general, the encrusting foraminifera that recruited to experimental shells at 15 m were calcareous foraminifera (Plates I, II).
Calcareous foraminifera also recruited to 33-m shells, with the
addition of calcareous agglutinated species, like Placopsilina sp.
(Plates III, IV). Encrusting foraminifera that were common at the
shelf/slope break (73–88 m) included calcareous forms such as
Planorbulina acervalis and Cibicides refulgens and agglutinated species
like Tritaxis ?fusca, Placopsilina sp., and Rotaliammina spp. (Plate V).
Textularid foraminifera were also typical below the shelf/slope break
(Plate VI). Some species, like Spirillina vivipara, were distributed from
the shallow shelf to slope (Plate VII).
3.2. Comparison of β-diversity metrics
Four β metrics were used to compare species turnover among
depths and between deployment years (Table 6). The two metrics,
βcounts and βJost, provided the most ecological information for
encrusting foraminiferal communities. Based on βcounts, there was
more turnover among species between depths within the first year of
deployment (1994), than the other two years (Table 6). Comparisons
331
S.E. Walker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
Table 4
Encrusting foraminifera species, their abundance (n) with depth (m, meters) for year 1999 and their diversity indices, Lee Stocking Island, Bahamas.
Species
15 m
33 m
88 m
213 m
264 m
267 m
Totals
Acervulina inhaerens
Amphistegina gibbosa
Ataxophragmoides sp.
Bdelloidina ?aggregata
Biarritzina carpenteriaeformis
Bueningia sp.
Carpenteria balaniformis
Cibicides refulgens
Cibicides lobatulus
Cibicides sp.
Cornuspiramia cf. adherens/antillarum
Discorbis bertheloti
Discorbinellidae
Dyocibicides ?biserialis
Gypsina globularis
Gypsina plana
Haplophragminoides sp.
Hemisphaerammina sp.
Homotrema rubrum
Neoconorbina terquemi
Nodobaculariella sp.
Placopsilina sp.
Planorbulina acervalis
Rhizammina sp.
Rotalliammina sp.
Sahulia ?patelliformis
Spirillina vivipara
?Sporadotrema sp.
Textulariella sp. Includes: Textulariella cf. barrettii and Textulariella cf. mayori
Tritaxis ?fusca
Unid. Foraminifera
Unid. Foraminifera D
Unid. Miliolidae
Unid. Textularidae
Total individuals
172
2
7
15
1
1
0
31
33
0
15
73
0
21
11
85
1
18
327
26
4
17
241
0
0
0
13
0
0
5
3
0
43
20
1185
70
4
8
0
0
0
0
194
23
0
8
84
0
6
18
1
4
0
2
32
0
205
897
0
0
2
64
0
0
11
0
0
49
0
1682
0
19
2
0
18
0
20
25
2
0
112
0
0
4
31
5
25
2
93
2
15
146
248
1
0
0
107
2
0
424
2
2
34
36
1377
0
1
0
0
1
0
0
60
1
1
0
0
0
3
0
0
0
4
0
0
0
19
120
1
24
0
1
0
0
55
3
0
0
43
337
0
0
0
0
3
0
0
52
4
0
0
0
4
1
0
0
2
1
0
0
0
1
58
11
33
2
1
0
0
76
1
0
0
26
276
0
0
0
0
4
0
0
79
6
0
0
0
0
0
0
0
13
0
0
0
0
35
43
0
16
3
4
0
3
106
12
0
0
12
336
242
26
17
15
27
1
20
441
69
1
135
157
4
35
60
91
45
25
422
60
19
423
1607
13
73
7
190
2
3
677
21
2
126
137
5193
Species richness (α)
Shannon Entropy (H)
exp(H)
Pielou's J
Species turnover with depth, βcounts
25
2.304
10.014
0.71
–
among years using βcounts indicated that more species turnover
occurred between 1994/1995 and 1994/1999. Whittaker's multiplicative βw also revealed the same trend, but not the true number of
species that turned over. βadd also revealed the same trend, but
species turnover was overestimated when compared to the true
species turnover based on βcounts. In contrast, the βJost metric
indicated that within years, the structure of the communities were
distinct for all depths for each time period. When βJost was compared
between years, the highest turnover also occurred in 1994/1995 and
1994–1999. Additionally, the true gamma diversity for all years
pooled can be calculated using the Shannon equivalents: If the
average expα is added to the average exp(H), 45 species will result
(refer to Table 3).
3.3. Temporal patterns in encrusting species richness and abundance for
Telescopium and Strombus
Species richness slightly differed among the shell types. In 1994,
species richness on Telescopium shells declined with depth from 14
species (n.b. Texturiella spp. was treated as two species here:
Textulariella cf. barrettii and Textulariella cf. mayori) on the shelf to
10 species at 213 m (Fig. 4). In contrast, species richness on Strombus
shells for 1994 was highest at 15 m (16 species), declined to 11
species between 33 m and 213 m, and increased to 14 species at
267 m (Fig. 4). In 1995, species richness on Telescopium shells from
15 m to 73 m varied between 16 and 18 species, respectively, and
declined in species richness below 73 m. Eleven foraminiferal species
19
1.686
5.397
0.57
8
25
2.247
9.459
0.70
12
15
1.824
6.196
0.67
14
16
1.947
7.007
0.70
5
13
1.973
7.192
0.77
5
γ = 34
Average exp(H): 7.5
encrusted Strombus shells at 15 m, increasing to 17 species at 33 m
and decreasing to 14 species at the shelf/slope break; thereafter,
declining to 8 species at the deepest sites. In 1999, species richness on
Telescopium shells was higher than that for the 1994 shells; Strombus
also had higher species richness for all depths except at 33 m. Both
shell types had the same species richness at the shallowest sites, and
at 88 m, Telescopium had more encrusting species than Strombus.
Species richness on sites b88 m was significantly different for both
shell types than species richness below 88 m (MW U-test, P b 0.001
Telescopium; P b 0.0001, Strombus).
Abundance differed among the depths per year. After one year of
deployment at the sediment–water interface, the 15-m site had the
highest abundance of foraminifera, with 597 individuals on Telescopium and 744 individuals on Strombus; abundance steeply dropped
for both shell types below this depth (Fig. 5). After two years,
Telescopium had 629 individual foraminifera, while Strombus had 422
individuals at 15 m; below this depth, abundance steeply declined.
After six years, the pattern of abundance was remarkably different,
with high abundance of encrusting foraminifera on Telescopium shells
at the 33 m rather than at 15 m as seen in previous deployment years.
The peak at 33 m for Telescopium in year six is largely due to an
increase in abundance of two foraminiferal species, Cibicides refulgens
and Planorbulina acervalis. After six years, overall abundance
increased for all deployment depths in comparison to previous
years. The highest abundance of foraminifera that encrusted Strombus
shells occurred at 15 m, rather than at 33 m for Telescopium shells.
Encrusting foraminifera on both shells increased in abundance
332
S.E. Walker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
Table 5
Diversity metrics for encrusting foraminifera from Lee Stocking Island, Bahamas for
1994, 1995 and 1999 deployment years. Key: S = species richness; H = Shannon
Entropy; exp(H) is exponentiated H of Jost, 2006, 2007; α is average alpha based on
actual species counts; expα is exponentiated H pooled and divided by 5 for the number
of depths; and βjost is species turnover based on exponentiated Shannon Entropy (Jost,
2007).
1994
S
15 m
33 m
88 m
213 m
267 m
Total
α
expα
βjost
Individuals
H
exp(H) Pielou's J
20
1338
15
799
12
86
9
136
12
30
35 unique species 2389
13.6
5.9
5
1.576
1.002
1.814
1.729
2.313
8.434
4.836
2.724
6.135
5.635
10.105
29.434
1995
S
H
exp(H) Pielou's J
15 m
33 m
73 m
88 m
213 m
264 m
267 m
Total
α
expα
βjost
17
1053
21
954
17
480
19
307
9
160
7
126
12
110
33 unique species 3190
14.5
5.8
7
1.459
4.301
1.509
4.526
2.148
8.567
2.207
9.088
1.612
5.013
1.152
3.165
1.802
6.067
11.889 40.727
1999
S
Individuals
H
15 m
33 m
73 m
88 m
213 m
264 m
267 m
Total
α
expα
βjost
25
19
–
25
15
16
13
34 unique species
18.8
7.5
6
1185
1682
–
1377
337
276
336
5193
2.304
10.014
1.686
5.397
–
–
2.247
9.459
1.824
6.196
1.947
7.007
1.973
7.192
11.981 45.267
Individuals
0.52
0.37
0.73
0.79
0.93
0.52
0.50
0.76
0.75
0.91
0.59
0.73
exp(H) Pielou's J
0.71
0.57
–
0.70
0.67
0.70
0.77
Grand totals 45 unique species 10,772 individuals
between years two and six at 33 m and 88 m. Below the photic zone,
abundance of encrusting foraminifera stayed relatively stable for both
shell substrates.
3.4. Density and averages of encrusting foraminifera per shell surface
area
Ten species of encrusting foraminifera contributed at least one
individual/cm 2 with Planorbulina acervalis the most abundant species
in 1995 per surface area (Table 7). After six years, a different
foraminiferal assemblage occurred, with three species represented by
at least one individual/cm 2 (Table 8). These six-year samples were
dominated by Cibicides, and not by Planorbulina. Additionally, Gypsina
plana first appeared as small round crusts (b4 mm diameter) within
two years, but by the sixth year, Gypsina crusts were covering most of
the shell surfaces.
When average abundance of encrusting foraminifera was computed, the most common species often had the widest depth range,
such as Planorbulina acervalis, Cibicides refulgens, and Spirillina
vivipara for both two years and six years (Figs. 6, 7). Shallow water
species were Acervulina, Discorbis bertheloti, Neoconorbina and an
unidentified miliolid; species representing the shelf included Homotrema rubrum, Gypsina globularis, Cornuspiramia spp. and Placopsilina;
deeper water genera were characteristically Rotalliammina, Tritaxis,
Sahulia and unidentified textularids (Figs. 6, 7). Overall, calcareous
encrusting foraminifera dominated the shallow shelf and shelf/slope
break, while agglutinated species and the calcareous C. refulgens
dominated the slope sites.
3.5. Encrusting patterns on exposed and unexposed shell surfaces
Foraminifera that encrusted the exposed surface of the shells were
significantly more common than foraminifera that attached to
unexposed shell surfaces (M–W U-test: exposed = 83, unexposed =
20; P b 0.0001). When individual species of foraminifera were
compared, most encrusted the exposed side of the shell (i.e.,
Planorbulina acervalis, Cibicides refulgens, Cornuspiramia cf. adherens/
antillarum, Placopsilina cf. bradyii, and Tritaxis ?fusca). Foraminifera
that exhibited no difference between exposed and unexposed
surfaces included Homotrema rubrum and Gypsina plana.
3.6. PCA of the distribution of encrusting foraminifera with depth
A principle component analysis was performed on the six-year
data to analyze the coherence of encrusting foraminiferal distribution
patterns as an indicator of depth and location across the shelf-andslope transect. The first four eigenvalues explain 60% of the variance in
the data. Fig. 8 plots the abundance of encrusting foraminifera on
Telescopium shells with depth. For Telescopium shells, a plot of
component 1 vs. component 2 (Fig. 8A) shows a negative association
between all the sites and 88 m. The highest scores, corresponding
with 15 m, are driven by those foraminifera that have their greatest
abundance at 15 m (Acervulina inhaerens, Bdelloidina sp., Gypsina
plana, Hemisphaeramia sp. and Homotrema rubrum). The negative
scores for 88 m are driven by the encrusting species, Tritaxis and
Cibicides lobatulus. Component 2 splits out the shelf/slope break sites
(88 m) from the rest of the data. The foraminifera that are driving this
negative loading are those that have their greatest abundance at 88 m
(e.g., Amphistegina gibbosa, Biarritzina carpenteriaeformis, Carpenteria
utricularis, Cornuspiramia cf. adherens/antillarum, Nodobaculariella sp.,
Spirillina vivipara, and Tritaxis ?fusca). In Fig. 8B, the 33-m site loads
negatively, driven by the foraminifera Cibicides refulgens, Haplophragmoides sp., Placopsilina cf. bradyii, Planorbulina spp., S. vivipara, and an
unidentified miliolid. The deep water samples (213–267 m) all plot
together, with Rotalliammina and textularids controlling the distribution. A plot of component 2 vs. 3 (Fig. 8C) emphasizes that 15 m,
33 m, and 88 m sites all plot in separate quadrants, while all deepwater sites (213–267 m) plot together.
PCA results for foraminifera on the Strombus shells have similar
trends as Telescopium (Fig. 9). The first component splits the shell
substrates based on depth (Fig. 9A). Unlike encrusting foraminifera on
Telescopium shells, the shelf/slope break (88 m) foraminifera load
positively with the sites below the photic zone (i.e., 213–267 m). The
15-m and 33-m sites load negatively on the first component. The
second component splits the shelf/slope break sites from all other
sites based on the foraminifera that have their peak abundance at
88 m (i.e., a similar list to that on Telescopium shells). Component 3
(Fig. 9B) separates the two shallowest sites from sites deeper than
88 m.
The species, Cibicides refulgens, Placopsilina cf. bradyii, Planorbulina
sp., and Neocornobina terquemi on the 33-m shells contribute to the
negative loading. Foraminifera that drive the positive loading of 15-m
shells are Bdelloidina sp., Gypsina plana, Homotrema rubrum, Planorbulina acervalis, Dyocibicides biserialis, and unidentified textularids.
When component 2 was plotted against component 3, a clear
separation of the three photic zone sites occurred (i.e., shallow
shelf, outer shelf, and shelf/slope break sites) based on foraminiferal
frequency and distribution (Fig. 9C).
S.E. Walker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
333
Plate I. Photomicrographs of common encrusting foraminifera at shallow shelf depths (15 m). From left to right, top row: Homotrema rubrum, Planorbulina acervalis, Acervulina
inhaerens; bottom row: Gypsina plana, Discorbis bertheloti, Gypsina globularis (top) and Neoconorbina terquemi (bottom).
4. Discussion
4.1. Alpha diversity and taxonomic composition of encrusting
foraminifera
Species richness of encrusting foraminifera remained remarkably
similar for all three sample years varying from 35 species in 1994 to 34
species in 1999 (average 33 species). The number of abundant taxa
(those with N100 individuals) increased over the duration of the
experiment, from 3 taxa in 1994, 6 taxa in 1995 to 11 taxa in 1999.
This pattern follows the overall increase in total abundance of
encrusting foraminifera, increasing from 2389 individuals in 1994 to
5193 individuals in 1999 (for all sample dates pooled: 10,772
individuals).
The most abundant encruster for all three sample years was
Planorbulina acervalis. Planorbulina first colonized in large numbers on
the shelf, and after two years, it became common at the shelf/slope
sites; by six years it was common at the deepest sites. The deep-water
sites are located within a dune field, which may experience
geostrophic currents (after Stockhausen and Lipcius, 2001); these
currents may increase mixing and help to introduce and advect larvae
at these depths.
Planorbulina acervalis is known from the Gulf of Mexico and
Caribbean Sea, and is a common shallow-water encruster (Cushman,
1922). Planorbulina also encrusts relatively protected regions of reefs
(Gischler and Möder, 2009) and exposed blades of sea grasses, such as
Thalassia and Syringodium (Wilson, 1998). We found it to encrust
carbonate-to-slope experimental shells, and it appears to be opportunistic. Perhaps P. acervalis is more tolerant of varying environmental
conditions than previously known or it may represent a species
complex like Cibicides refulgens (see Schweizer et al., 2009); once
genetic analyses are done, the environmental differences may be
parsed out. Planorbulina does not harbor photosymbionts, and this
may explain why its distribution was not depth limited in our study.
Rather, P. acervalis may consume microalgae (diatoms) and bacterial
biofilms by using its reticulopods (after Langer, 1993; Richardson,
2004).
Another taxon, Acervulina inhaerens, was very abundant in 1994
and 1999. Acervulinids are more common in deeper water, where
competition for space may be reduced (Rasser and Piller, 1997).
Acervulinids are also significant framework-builders in Recent and
fossil reef environments, and A. inhaerens, is known to make nodules
(or macroids) in its adult stage up to 10 cm in diameter (reviewed by
Perrin, 1994). These nodules are most common on deep-reef slopes
(Perrin, 1994). It is possible that this species is Gypsina plana, as there
has been some confusion in the literature about these species: In some
treatments, A. inhaerens may be called Gypsina inhaerens (Hohenegger,
2006).
In our study, however, Acervulina was restricted to the two
shallowest depths for all three sample years. Di Camillo et al. (2008)
report Acervulina inhaerens encrusting hydroids in very shallow water
from the Mediterranean and Peebles et al. (1997) found it in sediments
from the carbonate platform of the northern Nicaraguan Rise (Caribbean
Sea). At these shallow depths, interactions among encrusters are more
common and could lead to competition (refer to Richardson-White and
Walker, this issue). This species did settle in large numbers within the
first year of our experiment, and may act to exclude other encrusting
organisms via niche incumbency. Niche incumbency occurs when
species settle first and maintain their spatial distribution, at both
modern and geological time scales; and, they resist invasions of new
taxa over time (Bambach et al., 2002; Foote et al., 2007; Valentine et al.,
2008). It is quite possible that both Planorbulina acervalis and
A. inhaerens are important ecological incumbents for tropical carbonate
environments, but this awaits further study.
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A
B
1
2
C
D
Plate II. Scanning electron micrographs (SEMs) of 15 m encrusting foraminifera: A, Discorbis bertheloti; B, Neoconorbina terquemi; C, Acervulina inhaerens (with Cornuspiramia cf.
adherens noted by the number 1 and an unidentified foraminifera denoted by number 2); and D, Gypsina globularis.
Homotrema settled on the experimental shells within the first year,
but did not become very abundant until the sixth year. In our study, it
was restricted to water depths of less than 88 m. Homotrema is
reported from high-energy shallow-water settings (Langer, 1993;
Gischler and Ginsburg, 1996; Gischler and Möder, 2009) and is known
to settle in cryptic habitats, such as the underside of boulders and
corals (Cushman, 1922; Emiliani, 1951).
Homotrema has at least five morphotypes that are known from
Bermudian reefs (i.e., hemispherical, globose, knobby, encrusting and
globular; Elliott et al., 1996). The encrusting form is relatively rare
(i.e., 12.3%, n = 4002 tests) from Bermudian settings and may be
representative of juvenile forms (Elliott et al., 1996). In our study,
Homotrema were either crusts or globose forms, consistent with
exposed vs. unexposed surfaces of the shells, respectively. Homotrema
was also most common at the shallowest site (15 m) and the
shelf/slope edge (88 m), where water energy during tidal exchange
is greater. Likewise, Hauser et al. (2007) reported Homotrema rubrum
from bivalve shells retrieved from reef crest sediments associated
with coral atolls from Belize. Therefore, it appears that H. rubrum may
be an excellent indicator of high energy water conditions for shallow
near shore and shelf/edge (88 m) habitats in tropical and subtropical
environments.
An unusual bioeroding foraminiferan, Discorbis bertheloti, was very
abundant in 1995 and 1999. Until this study, it was not known that
this species bioerodes carbonate substrates. Discorbis bertheloti is very
small and can be overlooked unless high magnification is used
S.E. Walker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
335
Plate III. Photomicrographs of common encrusting foraminifera at outer shelf depths (33 m). Top row, from left to right: Acervulina inhaerens, Cibicides refulgens, Placopsilina cf.
bradyii; Bottom row, from left to right: Planorbulina acervalis, Cibicides lobatulus.
(N200×). We found that it bored holes within the internal apertural
area of the experimental gastropod shells, and thus appears to be a
cryptic species that bioerodes carbonate substrates. Because it makes
small (b.001 mm) round traces in carbonate, its trace can be used as a
bio-depth indicator for shallow tropical water (b33 m). In 1994, it
occurred only at the 15-m site, but by 1995 its abundance had
increased by five times at that site, while it was rare at 33 m; in 1999 it
was common at both sites and never occurred deeper than 33 m.
Discorbis bertheloti appears to be an opportunistic species with initial
high abundance, and it also maintained high abundance during the six
years of the experiment, despite other spatial competitors. This
species appears to be an opportunistic ecological incumbent, like the
other foraminifera in this study that colonize rapidly in high numbers
yet maintain their abundance through time, rather than have
population crashes as true opportunistic species are known to do
(refer to Levinton, 1970).
Discorbis bertheloti is a cosmopolitan species (Loeblich and Tappan,
1988) and is reported from sediments associated with sea grasses
(Brasier, 1975). This species is also reported from sediments along the
upper continental slope of Florida and is known by various names
(185 m; i.e., Rosalina floridana = Rosalinia floridensis = D. bertheloti
var. floridensis, Sen Gupta et al., 1981; also Discorbinella bertheloti, see
Loeblich and Tappan, 1988). It is also known from the Miocene of
Jamaica (Cushman and Jarvis, 1930).
Three other calcareous taxa were abundant: Cornuspiramia cf.
adherens, Cornuspiramia antillarum and Placopsilina cf. bradyii.
Cornuspiramia antillarum is an encrusting milioline with a tubular
branching test. This species is considered a bio-indicator of eutrophic
waters if its abundance is N70% of the encrusting foraminiferal
community that lives on sea grass blades (Richardson, 2006).
Richardson (2006) worked in sea grass beds proximal to bird
rookeries in Belize, where runoff from nutrient-rich guano occurred,
especially in the rainy season. These nutrient-rich waters in Belize had
low sea-grass inhabiting foraminiferal diversity, but had high
abundance of C. antillarum species.
At Lee Stocking Island, Cornuspiramia did not exceed the high
percentages reported by Richardson (2006), indicating relatively normal
oligotrophic waters. Importantly, Cornuspiramia antillarum has rapid
growth rates and is thought to reproduce by asexual fragmentation and
multiple fission (Arnold, 1967). This reproductive mode may explain
why Cornuspiramia was very common on our first-year experimental
arrays. Therefore, in oligotrophic waters, Cornuspiramia may be a pioneer
species that can settle quickly, but it is not an ecological incumbent like
Planorbulina acervalis or Acervulina inhaerens because it does not
maintain its abundance through time. Cornuspiramia was also restricted
to shallow shelf depths less than 88 m. Our findings are in agreement
with those of Hauser et al. (2007) who reported that C. antillarum was
an abundant encrusting taxon of empty bivalve shells and was
indicative of wave and current activity in coral atolls from Belize.
Placopsilina cf. bradyii only settled on the shallow-water experimental arrays within the first year, then increased in abundance and
colonized shelf/slope sites in the second year (to 88 m). By the sixth
year, P. cf. bradyii was found at all depths, with its greatest abundance
(N100 individuals) at 33 m and 88 m. This species is an agglutinated
foraminiferan, and is known from abyssal depths (Gooday and
Haynes, 1983). The fossil record of Placopsilina starts in the Middle
Jurassic, and some species have commensal or mutualistic associations with Cretaceous bioeroding sponges (Bromley and Nordmann,
1971; Loeblich and Tappan, 1988).
While we did not see Placopsilina associations with bioeroding
sponges (formerly named as clionid sponges, now called “clionaid”
sponges, after Rützler, 2002), we did see a similar agglutinated
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S.E. Walker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
A
B
C
Plate IV. SEMs of outer shelf in 33 m) encrusting foraminifera: A, Planorbulina acervalis; B, Cibicides lobatulus, and C, Placopsilina cf. bradyii.
species, Bdelloidina ?aggregata, that was associated with clionaid
holes at the 15-m site in 1999. In 1999, clionaids were much more
common than in previous years (Brett, this issue), perhaps facilitating
the settlement of Bdelloidina on the shells. Bdelloidina co-occurs in the
fossil record with Entobia, a trace fossil for bioeroding sponges like
clionaids (Bromley and Nordmann, 1971). Additionally, fossil Bdelloidina is a rare encruster of coral reefs from the Upper Eocene of Italy
(Bosellini and Papazzoni, 2003). In the Recent, Bdelloidina is rare in
coral reefs from the east and west Flower Garden in the Gulf of Mexico
(Poag and Tresslar, 1981). Its rarity may be related to its cryptic habit,
encrusting mollusc shells and corals in tropical regions; the deepest it
has been reported is 110 m, dredged from those depths during the
Challenger Expedition (Chapman, 1900).
4.2. Spatial and temporal difference in β diversity and
β-metric comparisons
Two metrics, βcounts and βJost, provided the most ecological information for the encrusting foraminiferal assemblages in our study.
Based on βcounts, there was more turnover among species between
depths within the first year, than the other two deployment years.
Comparisons among years using βcounts indicated that more species
turnover occurred between the first and second year (1994 to 1995),
and between the first and sixth year (1994 to 1999). Whittaker's
multiplicative βw revealed the same trend, but not the true number of
species that turned over. βadd also revealed a similar trend to βcounts
and βw, but species turnover was overestimated when compared to
the true species turnover based on βcounts. In contrast, the βJost metric
indicated that within years, the structure of the communities were
distinct for all depths for each time period. When βJost was compared
between years, the highest turnover also occurred from 1994 to 1995,
and from 1994 to 1999. Additionally, the true gamma diversity can be
calculated using the equivalents of the Shannon Entropy Index: if the
average expα is added to the average exp(H), 45 species will result.
Thus, βJost is a very important beta diversity metric, comparable to
βcounts, but giving more information about community structure, such
as the relative number of dominant species and whether sites are
similar or different in species composition.
S.E. Walker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
337
Plate V. Photomicrographs of common foraminifera below 73 m, from left to right, top row: Planorbulina acervalis, Rotaliammina spp., Placopsilina sp.: bottom row, left to right:
Cibicides refulgens and Tritaxis ?fusca.
4.3. Encrusting patterns on exposed and unexposed shell surfaces
Foraminifera that attached to the exposed side of the shell
occurred with greater frequency than those that occurred on the
unexposed surfaces of the shell. Foraminifera that showed no
significant difference between exposed and unexposed surfaces
included Homotrema rubrum and Gypsina plana, two generally
shallow-water taxa. Gypsina plana may harbor photosymbionts
(Prager and Ginsburg, 1989), and thus it is likely that its initial
attachment occurred on the upper surfaces of the shells (but see
Section 4.4.1.). In contrast, several taxa were significantly more
frequent on the exposed surfaces (i.e., Planorbulina, Cibicides refulgens,
Cornuspiramia, Placopsilina, and Tritaxis). Recognizing these taxa on
fossil shells should allow for reliable designation of original
orientation of shells in fossil assemblages.
4.4. Common guilds of encrusting foraminifera with depth and time with
remarks on dispersal capabilities
Species richness and abundance varied slightly by shell type
(Section 3.3), consequently, results were pooled to discuss the common
species (N20 individuals) that constitute the encrusting foraminiferal
guild for each depth. Environmental factors, such as waves, currents,
substrate type and the presence of marine grasses and algae are known
to affect the distribution and diversity of benthic foraminifera in reef
environments (Martin and Liddell, 1988, 1989; Culver, 1990; Lee and
Hallock, 2000; Murray, 2006; Gischler and Möder, 2009), and these
factors may apply to encrusting foraminifera as well. Additionally, it is
well known that populations of benthic foraminifera vary seasonally in
shelf-and deep-sea habitats (Duijnstee et al., 2004; Duchemin et al.,
2007), and our experiments may include these seasonal variations.
4.4.1. Shallow-water encrusting foraminiferal guild (15 m)
By the first year (1994), the most common encrusting foraminifera
for the 15-m site were all calcareous species: Acervulina inhaerens,
Cornuspiramia cf. antillarum and Cornuspiramia cf. adherens, Discorbis
bertheloti, Gypsina globularis, Planorbulina acervalis, and presumably just
settled P. acervalis (as unidentified foraminifera A) (Table 9). This
shallow guild is composed of foraminifera that may feed using their
reticulopods to dislodge bacteria, bacterial biofilms and/or diatoms from
the shell substrate (refer to Richardson, 2006). The encrusting
foraminifera from this shallow guild are not known to harbor
photosymbionts (see Lee and Anderson, 1991; Hallock, 1999; Lee, 2006).
Most of the first year guild continued into the second year (1995),
except for the addition of the agglutinated species, Placopsilina cf.
bradyii, and an unidentified miliolid (Table 9). Placopsilina is not
known to harbor photosymbionts, and may possibly acquire food
from the shell surface using its reticulopods. By the sixth year, guild
associations increased with the addition of the calcareous species,
such as Cibicides lobatulus, Dyocibicides ?biserialis, Gypsina plana,
Homotrema rubrum, and Neocornobina terquemi, and by the addition
of agglutinated textularids.
Gypsina globularis (n.b., systematics are varied, some suggest
G. globula var. vesicularis: Poag and Tresslar, 1981) is known to attach
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S.E. Walker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
A
Plate VII. SEM of Spirillina vivipara, a species found from the shallow shelf to slope sites.
B
Plate VI. SEMs of deep-water agglutinated species: A, Textulariella cf. barrettii;
B, Textularia cf. mayori.
to hard substrates and is hemispherical to spherical in shape (Poag
and Tresslar, 1981). In the West Flower Garden Reef (Gulf of Mexico),
this species was found attached to coralline algal nodules, reef rubble
and reef framework (Poag and Tresslar, 1981). In Poag and Tresslar's
study, G. globularis was covered with a dark green biofilm, but in our
study, this species was black in color and always spherical in shape
making it easy to distinguish from all other foraminifera.
Gypsina plana makes relatively large crusts (up to several
centimeters in diameter) and is an important component of reef
frameworks (Perry and Hepburn, 2008). In reef environments,
G. plana recruits to cryptic areas, and is known to encrust coral rubble
in patch reefs and lagoons (Perry and Hepburn, 2008). It is also known
to occur on exposed substrates in fore-reef environments (Martindale,
1992; Perry and Hepburn, 2008) and can be an epiphyte (Debenay
and Payri, 2010).
With coralline algae, Gypsina plana may form large (2–15 cm in
size) nodules in the eastern Caribbean, usually between 30 and 60 m
in water depth (Reid and Macintyre, 1988; Prager and Ginsburg,
1989). These nodules can produce a considerable amount of
carbonate: an estimated 391 tons of organic carbon per year may
form on the platform of the San Salvador Seamount, Bahamas, from
these protists (Littler et al., 1991). From our work, it takes at least six
years for G. plana to become common to start the process of nodule
formation in these regions.
Gypsina plana is cosmopolitan, reported from tropical/subtropical
regions in the Indopacific, Caribbean, and Gulf of Mexico (Poag and
Tresslar, 1981; Loeblich and Tappan, 1988). In our study, G. plana
rarely occurred in 1994, but became somewhat more common in
1995; by 1999, G. plana was very common at 15 m. This species
appears to colonize at a slower rate than the other encrusting species,
suggesting its dispersal capabilities are limited.
4.4.2. Outer shelf encrusting foraminiferal guild (33 m)
The number of common encrusting species for the outer-shelf
guild increased from three species within the first year to nine species
by the sixth year (Table 9). In 1994, there were only three common
species that encrusted the shells at 33 m: Acervulina inhaerens,
Placopsilina cf. bradyii and Planorbulina acervalis. In 1995, four more
common species were present in addition to the three species from
1994: Cibicides refulgens, Cornuspiramia adherens/antillarum, Gypsina
plana, and Homotrema rubrum. In 1999, nine species were common:
Table 6
Beta diversity comparisons for species turnover of encrusting foraminifera at Lee
Stocking Island within and between years.
Type of beta
diversity
Within years
1994
1995
1999
1994–1995
Between years
1994–1999
1995–1999
βcounts
βw (γ / α̅)
βadd (γ − α̅)
βJost
12
3
24
5
7
2
20
7
8
2
16
6
13
2.8
25.1
12.0
15
2.0
16.9
11.1
9
1.7
11.9
8.5
Key: within years is β diversity calculated in relation to a depth gradient, where βcounts
means the species turnover among depths; between years is a comparison of β diversity
metrics between sample dates; βcounts: actual counts of species that are unique between
the years compared; βw: Whittaker's β diversity calculated by total diversity (γ divided
by average alpha (α̅) diversity, and is a measure of turnover along a spatial gradient, in
this case, along a depth gradient; βadd, Lande's β diversity, where α̅ is subtracted from γ
Lande, 1996); βJost is based on Jost (2007) equivalent diversity: Hγ/Hα̅ (see also
Anderson et al., 2011). Numbers were rounded when appropriate.
S.E. Walker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
Fig. 4. Change in species richness for encrusting foraminifera on molluscan shell
substrates deployed along the shelf and slope, AA transect. A) Richness values for
foraminifera encrusting Telescopium shells after one year, two years, and six years of
exposure at the sediment–water interface. B) Richness values for foraminifera
encrusting Strombus shells after one year, two years, and six years of exposure at the
sediment–water interface. The number of different taxa is high on the platform shelf
and remains high down to the shelf/slope break at 88 m. Below the thermocline (at
100 m), species richness is significantly less.
A. inhaerens, C. refulgens, Cibicides lobatulus, Discorbis bertheloti,
Neocornobina terquemi, P. cf. bradyii, P. acervalis, Spirillina vivipara,
and an unidentified miliolid.
The temporal recruitment patterns may reflect the variation in
dispersal and biogeographic-range capabilities of the foraminifera.
Cibicides lobatulus is a cosmopolitan species found in shallow-to-outer
shelf depths depending on latitude (e.g., Corliss, 1991; Freiwald, 1995;
Buck et al., 1999). Cibicides refulgens is also a cosmopolitan species,
living in tropical to polar regions (Alexander and DeLaca, 1987; Javaux
and Scott, 2003). Cibicides lobatulus is known to graze diatoms and
bacteria using reticulopod extrusion and also may suspension feed
(Freiwald, 1993). This species (or a related species) may extract
extrapallial fluid from its host (Adamussium colbecki) in Antarctica
(Alexander and Delaca, 1987; see Schweizer et al., 2008). Both
C. lobatulus and C. refulgens were present in 1994, but their populations
increased after two and six years at the sediment–water interface.
Foraminifera are considered to be opportunists if they have high
reproductive rates and good dispersal capabilities (Lipps, 1983), and
the two species of Cibicides are opportunists in this sense. Opportunists have short generation times and low competitive abilities, but
both species of Cibicides increased in abundance at the same time as
other space-using species increased in abundance (i.e., Planorbulina
acervalis, Gypsina plana). Therefore, it is possible that Cibicides are
339
Fig. 5. Abundance of individual encrusting foraminifera on shell substrates after one-,
two-, and six years of exposure on the sea floor. A) Foraminifera on Telescopium shells:
greatest number of individuals occurred at 15 m. Year six shows a peak in abundance at
33 m largely due to the abundance of Cibicides refulgens and Planorbulina).
B) Foraminifera on Strombus shells. Peaks in abundance occur at the shallowest
depth (15 m) with abundance decreasing with increasing depth. Overall abundance
above the 100-m thermocline increased significantly between year two and year six on
the outer platform and upper slope.
opportunistic ecological incumbents. It is known that Cibicides
lobatulus is motile before it attaches, and this ability may allow it to
colonize rapidly if their propagules are in the area (Nyholm, 1961;
Zumwalt and DeLaca, 1980; Beaulieu, 2001).
Neocornobina terquemi is reported from a wide variety of depths
from very shallow (Goubert et al., 2001) to deep bathyal (Culver, 1988).
This species is also present in inland saline lakes of Egypt (Abu-Zied
et al., 2007) and from lagoons to reefs in Bermuda (Javaux and Scott,
2003). It is also known as an epiphyte (Langer, 1993). In 1994 and 1995,
N. terquemi was not very common on the shallow shelf, but by 1999, it
was relatively common on the shallow shelf and rare at the shelf/slope
break. This species is cosmopolitan in distribution (Loeblich and Tappan,
1988), yet it appears to have slower dispersal capabilities in comparison
to the other encrusting taxa in our study.
Spirillina vivipara is unusual in that its test is free, and it is rarely
attached to the substrate (Loeblich and Tappan, 1988). The specimens
that we examined were gently attached to the substrate, and thus, we
could be underestimating its true abundance if the specimens
detached during retrieval and processing of the samples. In 1994,
this species was very rare at 15 m and 88 m, but by 1995, its highest
abundance occurred at the shelf/slope break; in 1999, its highest
abundance was at 33 m and 88 m. This species has been reported in
nearshore lagoons and reefs near Bermuda (Javaux and Scott, 2003),
reefs in the Gulf of Mexico (Poag and Tresslar, 1981), and from cooler
water regions (Green, 1960).
340
Table 7
Mean abundance per cm2 of the top fifteen foraminiferan species that encrust Telescopium shells collected in 1995, AA transect, Lee Stocking Island, Bahamas. Note: Cibicides spp. includes Cibicides lobatulus and Cibicides refulgens;
Cornuspiramia spp. includes: Cornuspiramia cf. adherens and Cornuspiramia cf. antillarum; Tritaxis spp., includes Tritaxis ?fusca and unidentified Tritaxis spp.
Depth
Planorbulina
acervalis
Placopsilina
cf. bradyii
Rotaliammina
sp.
Tritaxis
?fusca
Cibicides
spp.
Spirillina
vivipara
Cornuspiramia
adherens/antillarum
Acervulina
inhaerens
Unid.
Miliolidae
Homotrema
rubrum
Gypsina
globularis
Hemisphaerammina
spp.
Gypsina
plana
Discorbis
bertheloti
Carpenteria
utricularis
1995
1995
1995
1995
1995
1995
1995
Mean
15
30
73
88
213
264
267
105
67
4
11
5.5
0.6
1
27.8
12.25
7.4
6.8
6.6
0
0
0
4.7
0
0
0
0.2
10
14.6
7.8
4.6
0
0.4
13
13.4
0.25
0
0.6
3.9
4.25
5.6
4.2
3.6
4
1
1.8
3.4
1
1.2
6.2
3.8
1
0
0
1.8
1.25
7.4
2.8
1.6
0
0
0
1.8
7
5.6
0
0
0
0
0
1.8
9.75
0.4
0
0
0
0
0
1.4
3.25
0.8
4.6
0
0
0
0
1.2
3.75
1.4
2
1.2
0
0
0
1.2
1.5
0.4
0.2
0.8
0.5
0.2
0.6
0.6
2.75
0.6
0.8
0
0
0
0
0.6
3.75
0
0
0
0
0
0
0.5
0.75
0
1.4
0.4
0
0
0
0.3
Table 8
Mean abundance per cm2 of the top fourteen species of foraminifera that encrust or attached to Telescopium shells collected in 1999, AA Transect, Lee Stocking Island, Bahamas. Note: Cibicides spp. does not include Cibicides lobatulus and
Cibicides refulgens; Cornuspiramia spp., includes: Cornuspiramia cf. adherens and Cornuspiramia cf. antillarum.
Year
Depth
(m)
Cibicides
spp.
Bdelloidina
?aggregata
Gypsina plana
Ataxophragmoides
sp.
Carpenteria
balaniformis
Cibicides
lobotulus
Discorbinellinae
Biarritzina
sp.
Cornuspiramia
spp.
Discorbis
bertheloti
Amphistigina
gibbosa
Cibicides
refulgens
Gypsina
globulus
Gypsina
vesicularis
1999
1999
1999
1999
1999
1999
Mean
15
30
88
213
264
267
0
0.8
1.4
0.6
21
0
3.9
0
6
2.4
2.4
1.9
0
2.1
11.6
2
1
0
0
0
2.4
0
1.4
1.4
1.8
0.2
0
0.8
0
0.4
0
0.6
0.8
0
0.3
0.2
0
0
0
1.4
0
0.2
0
0
0
0.2
0.6
0
0.1
0
0
0
0
0.8
0
0.1
0
0
0
0
0.8
0
0.1
0
0
0
0
0.6
0
0.1
0.2
0
0
0
0.2
0
0.06
0.2
0
0
0
0.1
0
0.03
0.2
0
0
0
0
0
0.03
0.2
0
0
0
0
0
0.03
S.E. Walker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
Year
S.E. Walker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
341
Fig. 6. Depth ranges of the average number of encrusting foraminifera on Telescopium shells after two years on the sea floor. The width of the bars represents the average number of
individuals of each species. Foraminifera with very low occurrences and unclear taxonomic affiliation are not depicted on these figures.
Spirillina vivipara is one of the few foraminifera whose life cycle is
known. At least twelve young can be asexually produced from one
individual, and these young can pair up and produce six young each
(Meyers, 1933). Thus, from one founder S. vivipara, many individuals
can be produced. Just a few founder S. vivipara may have generated
most of the individuals that were present on our experimental shells.
Dispersal in this species could be limited because it does not produce
biflagellated gametes, rather, the gametes are amoeboid and break out
of a cyst (Meyers, 1938) suggesting that S. vivipara could be localized
in their distributions, as they appear to be in our samples, unless their
tests, amoeboid gametes, or asexually-produced propagules are
moved by tidal currents, storm activity or other factors.
4.4.3. Shelf/slope break encrusting foraminiferal guild (73–88 m)
The common members of the shelf/slope break guild included
calcareous and agglutinated foraminifera. In the first year, only two
Fig. 7. Depth ranges of encrusting foraminifera on Telescopium shells after six years on the sea floor. The width of the bars represents the average number of individuals of each
species occurring at each depth over the five deployed shells at each depth (these are total pooled raw numbers from the five shells, not corrected for surface area). Foraminifera with
very low occurrences and unclear taxonomic affiliation are not depicted on these figures.
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groups of encrusting species were common, Cornuspiramia adherens/
antillarum and Tritaxis ?fusca (Table 9). By the second year, Cornuspiramia was not as common, but T. ?fusca increased its abundance six times
than that reported for 1994. In 1995, these two species were also joined
by Amphistegina gibbosa, Cibicides refulgens, Gypsina globularis, Homotrema rubrum, Placopsilina cf. bradyii, Planorbulina acervalis, and Spirillina
vivipara. The species that were common in 1995 were also common in
1999, joining Biarritzina carpenteriaeformis and Carpenteria utricularis. Of
these foraminifera, only A. gibbosa is an attached form that possesses
photobionts (Hallock, 1981).
Amphistegina gibbosa occurs in reefs, and is (or was) one of the
most abundant photosymbiont-bearing foraminiferan in tropical
habitats around the globe (Williams et al., 1997). Amphistegina ranges
from shallow water to 120 m (Hallock, 1999). It reproduces asexually
in the spring (Hallock, 1999), so propagules should have been present
when we deployed our experiments in 1993. However, off Florida in
1993, the juveniles of this species were anomalously missing
(Williams et al., 1997), and thus, the propagules may not have been
available to settle on our experiments. The A. gibbosa population
decline may stem from an increase of solar irradiance (UVB radiation;
Williams et al., 1997). The recovery of the shallow-water A. gibbosa
populations off Florida has been slow, while deeper water A. gibbosa
recovered faster. Williams et al. (1997) findings may explain why
A. gibbosa were more common in our shelf/slope break sites in 1995
and 1999, than at shallower sites.
Biarritzina is a cosmopolitan tropical genus (Loeblich and Tappan,
1988) and is known to encrust valves of the tiny brachiopod,
Tichosina floridensis, located in 119 m off Florida (Zumwalt and
DeLaca, 1980). Not much is known about Biarritzina, but it is most
likely a suspension feeder or is a commensal on brachiopod or other
filter-feeding organisms (see Zumwalt and Delaca, 1980). In our
study, Biarritzina carpenteriaeformis was very rare in 1994, with one
Fig. 8. Principle component plots of foraminifera encrusting Telescopium shells collected in year six. The analysis is based on the total community of foraminifera and their abundance
per square centimeter of shell area. A) Shells from below the photic zone (circles) plot higher on component one than all other shells. The separation of photic from aphotic shells is
likely based on greater abundance of foraminifera within the photic zone. Component two separates shells from 88 m from other shells based on a suite of foraminifera that peak in
abundance at 88 m. B) Component three plots the shallowest encrusters on shells (15 m) highest on the graph and 33 m plots negatively. C) Plotting component 2 vs. component 3
results in the three photic zone sites being plotted in three separate quadrants of the graph.
S.E. Walker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
occurrence at the deepest site (267 m). In 1995, one B. carpenteriaeformis was present at both the 88 m and 267 m sites, but in 1999, B.
carpenteriaeformis became common at 88 m, with a rare occurrence
below this depth. One individual also occurred at the shallowest site
(15 m). It appears that this species is a shelf/slope break and deeper
species.
Carpenteria is a cosmopolitan tropical genus (Loeblich and Tappan,
1988), and is known from shallow water (b10 m) in cryptic habitats
(Martindale, 1992) and from fore-reef sites (Perry, 1999). It is an
important contributor to reef framework by encrusting cryptic
recesses (Perry, 1999). In our study, Carpenteria utricularis was rare
between 15 and 33 m in 1994; in 1995 it was still rare, but it had
colonized the shelf/slope break; in 1999 it was somewhat common at
the shelf/slope break and occurred at no other site during this time.
Based on our samples, it is quite possible that this species is not a good
spatial competitor and is very patchy in its distribution.
343
Tritaxis is thought to only occur off England (Loeblich and Tappan,
1988). Clearly Tritaxis is widespread in tropical and polar regions (this
study; Schönfeld, 1997; Wissak and Rüggeberg, 2006; Martin, 2008)
and may be just overlooked. Tritaxis fusca encrusts foraminiferal tests
on the outer shelf off Washington, USA (Martin, 2008). Wissak and
Rüggeberg (2006) found that T. fusca was a common encrusting
foraminifera on PVC and carbonate substrates, but was restricted to
waters between 5 and 17 m. In our study, T. ?fusca was widely
distributed, from 33 m to 267 m within the first year, although it was
only common at the shelf/slope break. In 1995, it was very abundant
at the shelf/slope break sites, although it occurred at all sites except
15 m. In 1999, T. ?fusca occurred at all depths, with a peak abundance
at 88 m and was very common below this depth. It appears that T. ?
fusca's center of abundance is at the shelf/slope break, with
recruitment to other depths from this area. Nothing is known about
its reproductive biology or its dispersal mechanisms.
Fig. 9. Principle component plots of foraminifera encrusting Strombus shells collected in year six. The analysis is based on the total community of foraminifera and their abundance
per square centimeter of shell area. A) Encrusting foraminifera from below the photic zone (circles) plot in a tight group separate from all photic zone encrusters. The separation of
photic from aphotic encrusters is likely based on greater abundance of foraminifera on the shallow-water shells. Component two separates 88-m shell substrates from other shells
based on a suite of foraminifera that peak in abundance at 88 m. B) Component three plots the shallowest shells (15 m) highest on the graph and 33 m plots negatively. This is the
same trend as seen on Telescopium shells (Fig. 9). C) Plotting component 2 vs. component 3 again results in the three photic zone sites being plotted separately, but the deep-water
shells and the 15 m shells seem to overlap in this plot.
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Table 9
Common (N20 individuals per species) encrusting foraminifera species guilds with
depth and time, carbonate platform and slope, Lee Stocking Island, Bahamas.
1995
1999
Acervulina inhaerens
Discorbis bertheloti
Acervulina inhaerens
Cibicides lobatulus
Placopsilina cf. bradyii
Planorbulina acervalis
Unid. Miliolidae
Cibicides refulgens
Discorbis bertheloti
Dyocibicides ?biserialis
Gypsina plana
Homotrema rubrum
Neoconorbina terquemi
Planorbulina acervalis
Unid. Miliolidae
Unid. Textularidae
I. Inner shelf (15 M) 1994
Acervulina inhaerens
Cornuspiramia cf.
adherens/antillarum
Discorbis bertheloti
Gypsina globularis
Planorbulina acervalis
Unid. Foram A (possibly
new recruits of P. acervalis)
II. Outer shelf (33 M) 1994
Acervulina inhaerens
Placopsilina cf. bradyii
Planorbulina acervalis
Acervulina inhaerens
Cibicides refulgens
Cornuspiramia cf.
adherens/antillarum
Gypsina plana
Homotrema rubrum
Placopsilina cf. bradyii
Planorbulina acervalis
Acervulina inhaerens
Cibicides refulgens
Cibicides lobatulus
Discorbis bertheloti
Neoconorbina terquemi
Placopsilina cf. bradyii
Planorbulina acervalis
Spirillina vivipara
Unid. Miliolidae
III. Shelf/slope break (73–88 M) 1994
Cornuspiramia cf.
adherens/antillarum
Tritaxis ?fusca
Amphistigina gibbosa
Homotrema rubrum
Placopsilina cf. bradyii
Planorbulina acervalis
Spirillina vivipara
Tritaxis ?fusca
Biarritzina
carpenteriaeformis
Carpenteria balaniformis
Cibicides refulgens
Cornuspiramia cf.
adherens/antillarum
Gypsina globularis
Haplophragminoides
Homotrema rubrum
Placopsilina cf. bradyii
Planorbulina acervalis
Spirillina vivipara
Tritaxis ?fusca
Unid. Textularidae
Unid. Miliolidae
IV. Upper bathyal (213 M) 1994
Cibicides refulgens
Rotalliammina sp.
Unid. Textularidae
Cibicides refulgens
Planorbulina acervalis
Cibicides refulgens
Planorbulina acervalis
Rotalliammina sp.
Tritaxis ?fusca
Unid. Textularidae
V. Middle bathyal (264, 267 M) 1994
Cibicides refulgens
Rotalliammina sp.
Unid. Textularidae
Cibicides refulgens
Rotalliammina sp.
Unid. Textularidae
Cibicides refulgens
Placopsilina cf. bradyii
Planorbulina acervalis
Rotalliammina sp.
Tritaxis ?fusca
Unid. Textularidae
4.4.4. Slope encrusting foraminiferal guild (213–267 m)
At this depth, there was a mix of calcareous and agglutinated taxa
(Table 9). Cibicides refulgens and Planorbulina acervalis were the common
calcareous species at this depth, and were discussed previously. The
agglutinated taxa, in contrast to the calcareous taxa, are not as well
known biologically. The genus Haplophragmoides is cosmopolitan, while
Rotaliammina appears to be subtropical to tropical in distribution
(Loeblich and Tappan, 1988). In our study, Haplophragmoides had
variable colonization on the experimental shells. In 1994, this genus was
very rare, occurring only between 213 and 267 m. In 1995 it was still
rare, but only occurred at 267 m; in 1999, it was present at all depths,
with its peak in abundance at the shelf/slope break. It appears that this
species, or species complex, has episodic reproduction and doesn't
recruit readily to new substrates. In contrast, Rotaliammina, with its
orange color and agglutinated spicules, was very common at 213 m
within the first year. By the second year, it was very common at all
bathyal sites between 213 and 267 m. In 1999, it was still common at
those sites, and was not present at depths shallower than 213 m.
Rotaliammina, then, is a good indicator of bathyal depths.
4.5. PCA of foraminiferal species distribution with depth
The total foraminiferal assemblage, when examined by PCA,
indicates three otherwise relatively similar euphotic localities
(15 m, 33 m, and 88 m) that can be distinguished on foraminifera
distribution alone. Between these shelf and shelf/slope break sites, the
taxonomic make-up of the foraminiferal community seems to drive
the PCA-component loading. In particular, taxa that have a peak in
abundance at a specific depth, drive the clustering of the samples. For
example, Cornuspiramia and Tritaxis are most frequently found at
88 m, even though their overall range spans all three shallow sites for
the former and the entire depth range of the study for the latter. Taxa
with preferences for given depths are weighted most heavily by the
analysis, for instance, 88-m encrusting foraminifera plot separately
from either 15-m or 33-m foraminifera. The results of the PCA indicate
that there were no discernable differences among the encrusting
foraminiferal communities on shells from the three deepest (aphotic)
sites (213 m, 264 m, and 267 m) despite differences in bottom type
(hard ground at 213 m and 267 m vs. fine carbonate sand at 264 m)
and differences in species abundance. The most likely factor
controlling the split between deep and shallow samples is the overall
abundance of foraminifera and species composition that are in turn
influenced by light, nutrient levels, water energy, and time.
5. Concluding summary
5.1. Alpha diversity of encrusting foraminifera, stability, dispersal and
successional bypass
Diversity patterns for encrusting foraminifera at Lee Stocking
Island were similar to those found in reef macroinvertebrate studies,
where high species diversity can occur in outer shelf and shelf/slope
break habitats, but declines below 100 m in water depth (Huston,
1985; Liddell and Ohlhorst, 1988). Foraminiferal species richness was
highest in the photic zone, and decreased below the shelf/slope break
(88 m) at Lee Stocking Island, Bahamas. The patterns reported here for
encrusting foraminifera nearly parallels coral species diversity across
shelf-to-slope transects in tropical regions. For example, coral
diversity fluctuates in very shallow waters (~15 m), is highest at
30 m, and decreases below this depth (Huston, 1985). This change in
coral distribution roughly parallels the distribution of the photic zone,
as many coral species harbor photosymbionts (Huston, 1985;
LaJeunesse, 2002; van Woesik et al., 2010). Unlike corals, most of the
encrusting species in our study did not possess photosymbionts and
may be cueing in on food resources tied to the photic zone.
Previously, little was known about encrusting foraminiferal
species diversity (α), and species turnover (β) and how these
diversities vary with depth and time. Knowing such information
could provide more coherent paleoecological, paleoenviromental and
paleoclimatic reconstructions of these organisms (Debenay and Payri,
2010). We found that the units of species diversity (α) remained
relatively the same throughout the study (that is, 33–35 species), with
a majority of the species becoming common (N20 individuals) and a
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few species becoming very abundant (N100 individuals) with time.
Thus, there appears to be a remarkable stability in taxonomic units
(i.e., counts of species) within the first six years of this study,
regardless of the dominance of a number of encrusting species.
Species diversity decreases with depth after 213 m, and this
decrease is not related to the loss of photosymbiont-bearing taxa
because only two taxa in this entire study are thought to harbor
photosymbionts (i.e., Amphistegina gibbosa, and Gypsina plana). There
is a remarkable increase in the depth range of individual species with
time: Many taxa that appeared to be limited to the shallow photic
zone in year two had spread to sites below 100 m by year six. Reasons
for this long-term range extension can only be speculated. Dispersal
modes for attached foraminifera are limited to the release of
biflagellate gametes into the water column and alternatively, some
taxa have a meroplanktic life stage (Alve, 1999). Both of these
methods lead to short-lived propagules, so only local dispersal is
expected. Thus the jump in species richness from year 2 to year 6 may
be the result of 1) slow recruitment at depth due to a smaller pool of
foraminifera producing new individuals at any one time, 2) the ocean
thermocline at 100 m acting as a semi-permeable filter to the
introduction of shallow-water propagules, or 3) intermittent introduction of reef rubble and debris into deep water by hurricanes or
slumps and thereby transporting encrusters with them (that may
then reproduce and colonize new substrates at depth).
Alternatively, colonization of new substrates by foraminiferal
propagules may be faster in areas with high current velocities (Alve,
1999). In these areas, foraminiferal communities may bypass the typical
ecological successional stages starting with pioneer species; pioneer
communities are more likely to occur in areas with lower currents, and
therefore, slower dispersal times (Alve, 1999). It appears that this
relatively “fast” dispersal capability is occurring with the encrusting
foraminifera in our study, suggesting that the earliest pioneer stages are
by-passed, favoring diversity that is maintained by ecological incumbents, spatially and temporally. Whatever the mechanism, the
importance of long-term studies cannot be overemphasized.
5.2. Taxonomic composition with depth differs from previous research in
this region
Our taxonomic composition of encrusting foraminifera differ from
those reported by Choi and Ginsburg (1983) and Choi (1984) who
reported that Planorbulina, Homotrema rubrum and Gypsina were the
pioneer species that encrusted cryptic coral reef habitats. Two of those
taxa, Planorbulina and Homotrema, were common in our first year
deployment period on the experimental molluscan substrates, but
Gypsina plana was rare. Additionally, H. rubrum, Planorbulina spp.,
G. plana and Carpenteria are important secondary framework builders in
reef systems (Perry and Hepburn, 2008). We found that this secondaryframework group took time to assemble, and did not occur within the
first year: Planorbulina and Homotrema were common in year one;
Planorbulina common in year two; and G. plana and Carpenteria were
common in year six, suggesting a successional or community replacement change over the time period of our study for these secondary
framework builders. Choi (1984) reported that a climax stage for coral
rubble includes overgrowth by tunicates. In our study, G. plana was the
end member colonizer of these shell substrates and not tunicates.
Temporal and biogeographical differences in reef associations may exist,
and this needs to be furthered addressed to understand the development of secondary framework contributors to reef ecosystems.
345
the encrusting foraminifera in this study do not possess photosymbionts
and the very abundant foraminifera (Cibicides refulgens, Planorbulina
acervalis) do not appear to be limited by light. At 268 m, the deepest site
in this study, the light intensity was expected to be 0.0005% of the
surface, well below the photic zone for this region (Liddell and Ohlhorst,
1988). However, in other Caribbean studies, light sensitive organisms,
such as coralline algae and bioeroding cyanobacteria (Ostreobium) can
occur to 268 m and 210 m, respectively (Littler et al., 1985). Rather, a
steep decline in species diversity below the shelf/slope break could be
related to a lack of trophic resources (e.g., diatoms), or other factors.
Abundant species (C. refulgens, P. acervalis) that are putatively
suspension feeders colonized the bathyal sites by six years, and it may
be that long-time spans (N5 years) are needed to capture the full extent
of the species in this deeper region; but, there must be food resources at
this depth, perhaps brought in with deep geostrophic currents and the
Exuma gyre.
By years, the highest turnover of taxa occurred between the first
and the sixth year (1994/1999: 15 taxa) and between the first and the
second year (1994/1995: 13 taxa). Species turnover reflects approximately 25–40% of the encrusting foraminiferal assemblage in these
waters, depending on time on the seafloor, with greater species
turnover occurring within the first two years of recruitment to the
experimental shells.
5.4. Jost's, (2006, 2007) method was one of the best metrics for assessing
β diversity
The Jost beta diversity metric based on the Shannon Entropy Index
equivalent (βJost; Jost, 2006, 2007) in addition to βcounts (based on
actual counts of species) were deemed the best indicators of species
turnover in this study. Based on βJost, all of the depths had unique
species associations for all three sample periods. Between years, the
βJost indicated that the greatest species turnover occurred in the first
year and between the first and sixth year of the study, a similar result
as βcounts. The Jost method takes into consideration the abundance of
the species, and is based on equivalents which, if all species are
equitably distributed, will give true species diversity. If there are
dominant species, then βJost indicates which time periods were more
affected by dominance. We found, for low evenness assemblages, that
the approximate number of dominant species was indicated by the
βJost metric; it did not work for high evenness assemblages, only
stating which depths (or sites) were unique. A modified version of
Jost's Shannon Entropy equivalent was used on Pleistocene and Late
Quaternary benthic foraminifera from the eastern Caribbean Sea to
discriminate diversity differences between biozones (Wilson, 2011;
Wilson and Costellow, 2011).
5.5. Abundance and density of encrusting foraminifera decreases below
the shelf/slope break
For both one and two years on the sea floor, the shallowest site
(15 m) had the highest abundance of encrusting foraminifera. After
six years on the sea floor, the maximum amount of individuals
doubled from the early deployments, and the highest abundance on
the shells occurred at 33 m and declined steeply below the 33 m
depth. Density of encrusting foraminifera changed between two and
six years of exposure on the sea floor. After two years of deployment,
ten species of encrusting foraminifera made up at least one
individual/cm 2 with Planorbulina sp. being the most abundant. After
six years, a different assemblage occurred, dominated by Cibicides spp.
5.3. Species turnover (beta diversity) by depth and year
5.6. A new species of bioeroding foraminifera was discovered
By depth, beta diversity (βcounts) was highest between the
shelf/slope break and the upper bathyal, where species composition
changed with the addition of agglutinated foraminifera. Except for one
calcareous species (Amphistegina gibbosa and perhaps Gypsina plana), all
Discorbis bertheloti made very small (b0.001 mm) holes in cryptic
regions of the experimental gastropod shells. This species was
restricted to 15–33 m on the Lee Stocking carbonate platform,
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although it is known to have a wider geographic distribution based on
its occurrence within sediments.
long-term studies are needed to assess the spatial and temporal
resolution of encrusting foraminifera across biogeographic provinces
and shelf-to-slope regions.
5.7. Dispersal capabilities and time influence invasibility of encrusting
foraminifera
Dispersal mechanisms are not well known for benthic foraminifera
(Alve, 1999; Goldstein, 1999). Some species may have a passive
dispersal phase where the juveniles (zygotes, embryonic juveniles
which have the same density as sea water) may account for longerrange dispersal; and, adult tests may be advected by water currents
(reviewed by Alve, 1999). Shorter-range dispersal (within meters) for
other benthic foraminifera can be mediated by biflagellated gametes
(Alve and Goldstein, 2003). From our study, some species are much
better at dispersing than others, and must have propagules in the
water column at all times or have high reproductive rates.
Planorbulina acervalis and Cibicides refulgens, among others, appear
to be highly invasive foraminifera with relatively rapid colonization
rates. They act like opportunistic species, but unlike opportunistic
species, they maintain their spatial distribution and increase in
population size over time. Thus, these species may be opportunistic
ecological incumbents, where they invade new territory relatively
quickly with high numbers of propagules, but rather than have
population crashes like true opportunistic species, they increase their
abundance through time.
Some encrusting foraminifera appear to have a source area with
high relative abundance, and over time, spread to shallow and deeper
water from that source area. For example, Tritaxis ?fusca, has high
abundance at the shelf/slope break and spreads to both shallow and
deeper water over the years of our study, but still maintained its
highest abundance at the shelf/slope break. These recruitment
patterns would not have been seen without the long-term experimental arrays distributed along a bathymetric gradient.
5.8. Encrusting foraminifera have important applications for the fossil
record
Out of 16 genera of encrusting foraminifera found in this study,
two genera extend back to the Paleozoic, seven extend to the
Mesozoic, three have records to the early Cenozoic; only four are
known from the Recent and this may be because they haven't been
found as yet in the fossil record (Table 10). Given the limited coverage
of encrusting foraminifera in the literature, many of these fossil ranges
will be extended as more work is done on them. Therefore the utility
of modern encrusting foraminiferan communities to studies of
paleodepth, paleoclimate, and paleoecology have great potential but
Table 10
Known stratigraphic ranges of the encrusting foraminiferal genera in this study. All
ranges are derived from the Treatise on Invertebrate Paleontology or from Loeblich and
Tappan (1988) unless otherwise noted.
Genus
Stratigraphic range
Hemisphaerammina
Haplophragmoides
Placopsilina
Bdelloidina
Rotaliammina
Tritaxis
Spirillina
Cornuspiramia
Discorbis
Neoconorbina
Cibicides
Planorbulina
Acervulina
Gypsina
Amphistegina
Carpenteria
Middle Devonian–Recent
Carboniferous–Recent
Middle Jurassic–Recent
Paleocene–Recent
Recent
Recent
Triassic–Recent
Recent
Eocene–Recent
Recent
Cretaceous–Recent
Eocene–Recent
Jurassic–Recent (Hanzawa, 1939)
Cretaceous–Recent
Upper Cretaceous? Eocene–Recent
Upper Cretaceous–Recent
5.9. Encrusting foraminifera are an underutilized resource in deciphering
the environment of deposition of fossil hard-skeletal substrates
Four guilds of encrusting foraminifera composed of abundant and
common species delineated depth distributions in this carbonate
platform-to-slope region. Shells from four different depths (15 m,
33 m, 88 m, and deeper than 213 m) were distinguished by
foraminiferal species that reached their peak in abundance at specific
depths. Similar distributional patterns are known for reef macroinvertebrates from subtropical to tropical carbonate regions (Liddell
and Ohlhorst, 1988). The advantage of the encrusting foraminiferal
communities is that these communities develop over time, which can
give a time stamp to skeletal debris that enter the fossil record. These
encrusting species and their abundance are also useful as paleodepth
and paleoenvironmental indicators. And, lastly, because they cement
to skeletal or other surfaces they have an excellent chance of entering
the fossil record with their host substrate providing important
ecological forensic information beyond which their host substrate
could provide.
5.10. Calcifying foraminifera are essential to reefs
Calcifying foraminifera were the first to colonize experimental
molluscan substrates within the first year in shallow habitats, with
colonization offshore in subsequent years; agglutinated foraminifera
become more common after the first year. Many of these calcifying
foraminifera are important in building and maintaining coral reef
frameworks, from shallow to shelf/slope break depths; some are
important for carbonate nodule formation. One attached species,
Amphistegina gibbosa, harbors photosymbionts that are sensitive to
increased ultraviolet light, and this species may shift its distribution to
deeper water in response to the intensity of UVB (Williams et al.,
1997). Therefore, these important reef associates could be greatly
affected by the predicted warming of oceans and acidification
scenarios, and may be just as sensitive to these predicted changes as
their planktonic counterparts (see Moy et al., 2009; Lombard et al.,
2010). Not only are corals in peril, but all the carbonate-secreting
organisms that contribute to the formation of reefs, including the
important encrusting foraminifera.
Acknowledgments
Submersible work for this study was made possible through a
series of grants from the National Science Foundation (EAR-0345618
and EAR-9909317) and NOAA's National Undersea Research Program
at the Caribbean Marine Research Center. We are deeply indebted to
the pilots and support crews of the Nekton Delta, Clelia and Nekton
Gamma submersibles. We thank the CMRC staff at Lee Stocking Island
and the NURP personnel from CMRC who made our field program
possible. We also thank S. Goldstein, R. Martin, and P. Hallock Muller
for verification of foraminifera; the many undergraduate and graduate
students who facilitated this work from Oberlin College, Rutgers
University, The University of Cincinnati, Texas A & M University, and
The University of Georgia; Kathy Ashton-Alcox for her amazing
organizational skills and prowess; Rebekah Shepard for her expertise
on carbonate crusts; an NSF Polar Programs Grant # 0739512 that
facilitated updates concerning polar encrusting foraminifera; and,
especially to R. Martin and D. Rodland for their gracious and extensive
review.
S.E. Walker et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 312 (2011) 325–349
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