Introduction
The skeletons of photosymbiotic, zooxanthellate corals (z corals) are highly
organised, porous structures formed of the mineral aragonite (CaCO3).
Main structures include the tubular corallites in which the living polyps
reside, and (in some taxa) the bulbous coenosteum between the corallites
which is covered by a thin layer of living organic tissue. The architecture
of the corallites is complicated by a well-defined wall and
radially arranged blades (septa), sometimes more or less axially fused to
form a columnar structure within the centre (columella), and laterally
fused, convex upward sheets (dissepiments) which serve to separate the
living tissue from abandoned parts of the skeleton. Representatives of
z corals having this type of organization are the genera Orbicella and Solenastrea. In Porites, the
spongy aspect of the skeletal architecture results from laterally fused tiny
corallites with perforated walls and irregularly arranged dissepiments. In
X-ray images of slices parallel to the axes of the corallites (axes of
maximum growth), the skeletons of both groups of massive z corals display
alternating light and dark bands, the “density bands”, which reflect zones
of different skeletal density concordant with successive upward growth and
former growth stages (Knutson et al., 1972). The origin of the
rhythmic density changes has been suggested to have two underlying causes:
(i) variations in the density of packing of the sclerodermites at the
micro-architectural level, and/or (ii) thickness of the meso-scale skeletal
structural elements (septa, costae, columnellae) relative to porosity
remaining open (Buddemeier et al., 1974; Dodge et al., 1992; Le Tissier
et al., 1994). In the Orbicella-type skeleton, the density banding is very pronounced
and sharply defined, reflecting the thickness of exothecal structural
elements (dissepiments, costae), but not variations in their spacing,
whereas it is the overall thickness of the skeletal
structures and/or size-variability of the pore spaces and likely also
micro-structural organization within the spongy skeleton and/or the
thickness of the tissue layer which causes the density bands in Porites (Dodge
et al., 1992; Le Tissier et al., 1994; Reuter et al., 2005).
A pair of high and low density bands is generally assumed to represent 1 year of growth and forms the basis for the calibration of internal age
models and estimates of rates of annual upward and outward growth of the
colony surface (extension rate [cm yr-1]; (Knutson et al., 1972;
Lough and Cooper, 2011). Density is a measure of the thickness of the
skeletal elements and the total amount of pore volumes (measured as g cm-3): the thicker and more massive the individual skeletal
elements and the smaller the pores, the higher and closer the density will be to
that of the mineral aragonite (2.9 g cm-3). The two parameters,
extension rate and density, combine for estimates of calcification rates
according to Eq. (1; Lough and Cooper, 2011):
calcification rate(gcm-2yr-1)=annual extension rate(cmyr-1)×density(gcm-3)
Although a pair of density bands typically corresponds with 1 year of
growth, no universal pattern of band formation and timing of the high
density (HDB) and low density (LDB) bands over the seasonal cycle has been
found among reef sites world-wide (Highsmith, 1979). Many examples of
missing bands or additional bands (“stress bands”) and sequences of double
HDBs (dHDB) have been reported (Brachert et al., 2013; Dodge et al.,
1992; Highsmith, 1979; Leder et al., 1991; Lough and Cooper, 2011; Worum et
al., 2007). More recent studies have shown the systematics of calcification
to differ among taxa and ocean regions. While temperature tends to boost
calcification rates in recent z corals, temperature effects on extension
rate and density markedly differ (Carricart-Ganivet, 2004;
Elizalde-Rendon et al., 2010; Lough, 2008; Norzagary-Lopez et al., 2014). In
the Indo-Pacific genus Porites, linear extension rate shows a significant increase
with sea-water temperature but a concomitant decrease in bulk skeletal
density (Lough, 2008). Importantly, however, extension rates have been
shown to decline at unusually high temperatures (Cantin et al., 2010;
De'ath et al., 2009, 2013). In Orbicella from the Western Atlantic,
relationships of skeletal growth with ambient water temperature are less
clear. In the Gulf of Mexico and Caribbean Sea, linear extension rates
decline when skeletal bulk density increases with temperature
(Carricart-Ganivet, 2004). In Atlantic Porites (Elizalde-Rendon et
al., 2010) the response of linear extension with temperature agrees with
that of Porites from the Indo-Pacific, but no temperature effect on bulk density is
evident (Elizalde-Rendon et al., 2010). It has been suggested,
therefore, that the calcification strategies of the two coral genera and
their species differ with regard to successfully colonising space on a reef.
Likely, Orbicella is adapted to high-latitude settings by investing more of their
calcification resources into linear extension rather than thickening, i.e.
“sacrificing density” in order to occupy space on a reef efficiently near
the lower temperature threshold of distribution (Carricart-Ganivet,
2004). In addition to the environment, gender seems to represent another
poorly understood component controlling calcification
(Cabral-Tena et al., 2013).
Some evidence has been documented that calcification does not respond in a
linear way to temperature or environmental changes in general
(Worum et al., 2007). In one study using stable isotope data
from fossil Porites (9–10 Ma), inconsistent subannual timing of the HDB-LDB
rhythms among specimens and within individual specimens has been observed,
i.e. shifts in the timing of the HDB from the summer to the winter season
and the presence of double HDBs in a single year (Brachert et
al., 2013). The reasons for this variable timing of the HDB in z corals of
the same coral taxon at any given site of growth remains poorly known, but
may represent the effect of multiple environmental factors acting in concert
on non-linear calcification responses (Brachert et al., 2013).
One of these factors has been shown to be water depth, i.e. the timing of
the HDB varies with water depth (Klein et al., 1992). Here we
present seasonally resolved stable isotope records from fossil z corals in
combination with data on their calcification history. This study aims at
constraining the environment of growth and the annual and seasonal water
temperatures on the Florida carbonate platform during some Pliocene and
Pleistocene interglacials and how these factors controlled skeletal
calcification in z corals. We discuss the calcification signatures with
regard to upwelling and the fate of coral calcification along the Florida
reef tract with continued global warming. This study complements a previous
study on long-term seasonality recorded by Florida corals and mollusks
(Brachert et al., 2014) and forms the basis for a
companion paper on fossil z coral calcification rates
(Brachert et al., 2015).
Stratigraphy and oceanography of the Florida Platform
The Neogene Florida platform represents a stack of depositional units
forming marginal wedges or rather continuous sheets over the southern part
of the peninsula. The units are comprised of shallow-marine skeletal
carbonate deposits and date from interglacials when seal levels were up to
35 m above present (Dowsett and Cronin, 1990; Miller et al., 2012).
Intercalated freshwater sediments and paleosols formed during glacial sea
level lowstands (Jones et al., 1991; Petuch and Roberts,
2007). At some time, an extensive reef system existed along the south-eastern
margin of the platform, associated with a complex system of platform
interior environments (Meeder, 1979). Details of the facies, the
biota, and the palaeogeography of the single stratigraphic units are
described elsewhere (Allmon, 1992; Banks, 1967; Brachert et al., 2014;
DuBar, 1958; Locker and Doyle, 1992; Meeder, 1979; Petuch, 1982; Petuch and
Roberts, 2007).
Modern surface hydrology around the Florida peninsula differs substantially
on the Gulf and Atlantic sides. On the western shelf, SSTs are strongly
linked with winter coolings of the northern Gulf of Mexico and range
approximately between 17 to 32 ∘C. This contrasts with a more
subdued seasonal SST cycle along the eastern coast ranging between 22 to 30 ∘C. This pattern is modified during El Niño/La Niña
events and positive and/or negative phases of the North Atlantic Oscillation
(NAO) causing either wet and cool or dry and warm deviations from seasonal
average (Böcker, 2014). Upwelling occurs episodically and
intermittently on both sides of the peninsula and depends on the prevalent
seasonal wind systems and the strength of the Loop Current (LC) and Florida
Current (FC) systems (Fernald and Purdum, 1981). On the eastern side,
upwelling occurs during summer, in connection with an intensified FC
(Fernald and Purdum, 1981; Pitts and Smith, 1997; Yang, 1999), whereas on
the western Florida shelf, more sustained upwellings occur in winter and
respond essentially to an intensified LC and wind-assisted Ekman transport.
A concomitant shoaling of the thermocline in the LC causes an intrusion of
sub-surface water onto the shelf and shallow water zones (Li and
Weisberg, 1999).
Sampling sites in southern Florida. The numbering follows Brachert
et al. (2014).
No.
Site
Sample ID
GPS coordinates
Lithostratigraphy
Age
(Ma)
4
Palm Beach
EP8
26∘41.742′ N,
Bermont Fm.
1.2
Aggregates
EP9A
80∘21.270′ W
(Holey Land Mb.)
EP9C
EP9D
8
Brantley Pit,
EP6-S2
27∘2.988∘ N,
Caloosahatchee Fm.
1.8
Arcadia
81∘49.611′ W
(Bee Branch Mb.)
9
DeSoto Sand
452-K1-S61
27∘3.587′ N,
Caloosahatchee Fm
1.8
and Shell LLC
452-K4-S1
81∘47.627′ W
(Bee Branch Mb.)
(site 452)
452-K14-S6
10
unnamed pit
509A
26∘27.149′ N,
Caloosahatchee Fm.
1.8
(site 509)
81∘42.988′ W
15
Mule Pen
EP1-S2
26∘10.410′ N,
Tamiami Fm. (Golden Gate Mb.)
2.9
Quarry
EP2-S2
81∘42.468′ W
(Golden Gate Mb.)
EP3
EP4-S2
EP5-S2
16
Quality Aggregates
Coral #12
N/A
Tamiami Fm.
3.2
(APAC)
(Pinecrest Mb., unit 7)
1 From Böcker (2014), 2 from Roulier and Quinn (1995).
Sampling stations in southern Florida, USA (dots). See Table 1 for
details and numbering of sampling stations.
Materials
The z corals studied derive from four chronostratigraphic units of the
Florida carbonate platform representing interglacial highstands of sea level
and spanning collectively the period from the middle Pliocene to the early
Pleistocene (Table 1). Sampling sites in southern Florida selected for this
study are pits for carbonate gravels and de-watering canals exposing
carbonate sediments with well-established stratigraphic position (middle
Pliocene to early Pleistocene; Fig. 1, Table 1). Most of the fossil samples
were taken years ago by Edward Petuch (Boca Raton, USA) when the gravel pits
were dry through pumping and allowed for documenting and sampling exactly
according to stratigraphic position. In order to improve the database for
the present study, this material was complemented by one specimen described
in the literature (Roulier and Quinn, 1995) and additional specimens
collected by our group from spoil piles adjacent to the gravel pits and
canals because the outcrops are presently flooded with groundwater.
Materials from spoil piles are reworked and sediments not in their original
stratigraphic position, though all fossils from the spoils were considered
to derive from the stratigraphic unit exposed on site. Collections are
dominated by specimens of Solenastrea (n= 12), but also include Orbicella (n= 2) and
Porites (n= 1), both as entire coralla (< 20 cm) and fragments of large
coralla (< 60 cm). The scleractinian genus name Orbicella is used for corals
previously assigned to the Montastraea annularis group according to the revised taxonomic
classification of the reef coral family Mussidae (Budd et
al., 2012).
Methods
The fossil corals (n= 15, Table 1) were cut into slabs of < 1 cm
thickness along the plane of maximum growth using a conventional rock saw at
lowest speed and equipped with a water-cooled diamond blade. All corals were
screened for diagenetic alteration using a binocular microscope and SEM. In
order to detect minimal contaminations by secondary calcite, powder samples
taken at random were prepared for X-ray diffraction (XRD) and analysed using
a Rigaku Miniflex diffractometer with scanning angles of 20 to
60∘ 2θ. The detection limit of the method is
∼ 1 %. Only skeletal areas that retained their original
aragonite mineralogy, skeletal porosity and microstructure with no evidence
for significant secondary crystal growth or dissolution (microscopic and SEM
observation) were accepted for further analyses. Coral slabs of equal
thickness were X-rayed using a digital X-ray cabinet (SHR 50 V) to identify
potential zones of diagenetic alteration (McGregor and Gagan,
2003; Reuter et al., 2005) and to document cyclic density variations, i.e.
the density bands (Knutson et al., 1972). Density bands were
defined visually along the zones of maximum change in the grey scale of the
radiographs.
Quantitative measurements of density were made using X-ray densitometry
(Helmle et al., 2002). Measurements were undertaken along
transects parallel to the corallites and parallel to the isotope transects
(see below). The individual measurement transects were carefully selected so
as not to cross secondary cavities resulting from bioerosion, e.g. borings
from bivalves, and potential zones of diagenetic alteration. Bulk skeletal
density was calculated as the mean of all individual measurements along a
given transect. Calibration of the measurements was tested by measurements
of standards for zero density (air) and massive aragonite (slice of an
aragonitic bivalve shell having a thickness equaling that of the coral
slice). External analytical precision was tested by multiple measurements,
and mean deviation from regression (R2= 0.9) was found to be
0.04 ± 0.01 g cm-3 (range 0.02–0.06 g cm-3), i.e.
better than 5 %. All quantitative data of density and linear extension are
given as mean values and standard deviations (±1σ).
Z coral stable isotope data described here are the same as reported by
Brachert et al. (2014) supplemented by data from two additional
Solenastrea samples (Table 1). Sample powders for stable isotope analysis were taken
using a microdrill fixed to a manually operated X/Y/Z table. A 0.6 mm drill
bit and a drilling depth of 1 mm yielded > 20 µg of sample
powder from the theca wall. Sampled corallites were selected according to
their orientation parallel to the surface of the coral slices in order to
avoid geometric distortions between stable isotope cycles and the density
bands (Le Tissier et al., 1994). For sampling of the corallite
wall, all endothecal skeletal elements such as septae, columella and
endothecal dissepiments were removed prior to sampling using a hand-held
microdrill. For technical reasons, we sampled the inner surface of the
corallite wall instead of its external side (endothecate sampling method of
Leder et al., 1996). Sampling the cleaned inner surface of the corallite
wall assured all potentially existent secondary overgrowths (early or late
diagenetic cements) were removed prior to sampling. Samples for isotopic
analysis were taken at equal distances of 0.5 mm (or 0.7 mm for coral sample
452K1). In Porites we used a simplified technique where the sample drilling was
made without prior cleaning of inner corallite surfaces. Our sampling
approach assured the calculation of annual extension rates on the basis of
the number of samples per oxygen isotope year. Oxygen isotope years for the
age models were defined by the most positive δ18O values
assuming them to reflect maximum winter conditions. The age models were
further refined by linear interpolation of sampling points between winter
values (Brachert et al., 2006a). One long
Solenastrea δ18O record was spliced together from four overlapping
transects along parallel corallites using the software package AnalySeries
(Paillard et al., 1996). In order to document the relationships of
stable isotope data with the density bands, steel balls were placed within
some of the drill holes of the sampling path and the coral slices X-rayed
again.
Oxygen and carbon stable isotope analyses were carried out at the Institute
of Geophysics and Geology, Leipzig University. Carbonate powders were
reacted with 102 % phosphoric acid at 70 ∘C using a Kiel IV
online carbonate preparation line connected to a MAT 253 mass spectrometer.
All carbonate values are reported in per mil (‰)
relative to the PDB standard according to the delta notation.
Reproducibility was checked by replicate analysis of laboratory standards
and was better than ±0.04 ‰ (1σ) for
carbon (δ13C) and better than ±0.06 ‰
(1σ) for oxygen isotopes (δ18O). Water values of
δ18Ow are reported vs. SMOW. The seasonal difference in
δ18O values is given as Delta – delta values (Δδ18O). For calculations of paleotemperatures, we followed the
methodology described by Leder et al. (1996). SMOW to PDB conversions were
made according to the relationships given by Friedman and
O'Neil (1977).
Statistical analyses were performed using the PAST palaeontological
statistics software package (version 3.01) for education and data analysis
(freeware folk.uio.no/ohammer/past/). Stable isotope data (δ18O, δ13C) were
evaluated using the t test. A linear bivariate model was tested as to
whether there were no statistical differences in the stable isotope values
in a data set (p > 0.05) against the alternate hypothesis that
there were significant differences (p < 0.05). Equality of
regression slopes was tested using the f test as assumed by analyses of
covariance (ANCOVA).
SEM view of septa and dissepiments. (a) Septal surface with traces
of broken dissepiments. Septa and dissepiments are devoid of biogenic
incrustations and inorganic cements (EP6). (b) Cross section of a dissepiment
displaying radial fiber architecture of the sclerodermites. The centres of
calcification exhibit minor dissolution. (c) Detail of a dissepiment showing
polycrystalline aragonite fibers composed of granular crystallites (EP6). (d) Surface view of a septum. The septum is perforated by abundant near-surface,
filamentous microborings but exhibits no secondary incrustations and/or cements
(EP9c). (e) Cross section of dissepiment showing radial arrangement of bladed
crystal fibers (EP9c). (f) Surface view of a septum with biogenic
incrustation (EP4). (g) Sectional view of the coenosteum porosity infilled
with densely packed fibers of bladed aragonite. Some channel porosity is
present between fibers (EP4). This specimen was not used for density
measurements.
Results
Macroscopic and microscopic aspect of the coral samples
In outcrop, coral specimens were selected according to the retention of all
anatomical features of the corallites and a low weight taken to imply the
absence of secondary cements and mineral transformation and/or recrystallisation.
Upon microscopic investigation using SEM (Fig. 2a–g), the skeletons display
stacked spherulites or fans and layers of fibrous aragonite which represent
the microstructures typical of scleractinian corals (Constantz, 1986;
Nothdurft and Webb, 2007). Within the centres of the single calcifying units
(sclerodermites), porosity is more or less enhanced and the aragonite
crystallites are particularly small, granular in shape and have no
preferential orientation (Fig. 2b, c, e). The fiber crystals of the
sclerodermites display bladed or platy morphologies (Fig. 2e), whereas
fibers with beaded shape and rounded crystal rims (Fig. 2c) enclosing
submicron-sized, rounded channels at crystal contacts are of minor abundance
(Fig. 2g).
Bulk stable isotope values of Florida reef corals. Circles: recent
and Holocene; Dots: Interglacial Pliocene and Pleistocene. Recent and
Holocene data from literature (Leder et al., 1991, 1996;
Smith, 2006; Swart et al., 1996).
XRD analyses of the skeletons documented 100 % aragonite with no
measurable amount of secondary calcite. Also, in stereo-microscope and SEM
view, skeletal surfaces are smooth and devoid of syntaxial overgrowths or
continuous crusts of secondary incrustations of cement (Fig. 2a, d, f),
except for rare patches of isopachous or radial aragonite cement occurring
at random within a few specimens and rare biogenic incrustations
(Böcker, 2014). Near-surface, open, straight tubular cavity systems,
commonly Y-branched, with diameters < 5 µm and parallel to
skeletal surfaces (Fig. 2d) are less than 1 % by volume and probably
caused by endolithic fungi (Nothdurft and Webb, 2007).
Interpretation: XRD analyses did not reveal any measurable amount of calcite which agrees
with the results of microscopic and radiographic visual inspections
documenting no significant amounts of secondary calcite cements. Early
marine aragonite cements representing common modifiers of skeletal porosity
in recent z corals (Nothdurft and Webb, 2009) have not been recorded
on a regular basis in our material and represent rare occurrences of patches
of small spherulites rather than isopachous rims of acicular cement
(Böcker, 2014). Thus, precipitation of secondary cement was
volumetrically not important, neither at sea floor as aragonite or magnesium calcite, nor as
calcite formed during late stages of diagenesis.
Enhanced porosity at the centres of calcification (Fig. 2b) and channels
along crystal boundaries, rounded crystal rims, and tiny beaded crystals
within the centres of calcification are all potential effects of post-mortem
dissolution (Fig. 2c, g). Evidence for secondary aragonite–aragonite
transformations (Perrin, 2004) has not been observed in SEM. Taken
together, all cements and possible dissolution features are never
volumetrically important as to visibly blur the density bands documented in
x-radiographs (see below). For this reason, we consider the skeletons to be
in a mode of preservation suitable for measurements of stable isotope
proxies and calcification rates.
(a) Serial records of δ18O and δ13C in
z corals from the Holey Land Member of the Bermont Formation (Palm Beach
Aggregates, 1.2 Ma). Notice inverted scale of δ18O. (b) Serial records of δ18O and δ13C in
z corals from the Bee Branch Member of the Caloosahatchee Formation (1.8 Ma). Notice inverted scale of δ18O.
(c) Serial records of δ18O and δ13C in
z corals from the Golden Gate Member of the Tamiami Formation (Mule Pen
quarry, 2.5 Ma). Notice inverted scale of δ18O. (d) Serial records of δ18O and δ13C in a
coral from the Pinecrest Member of the Tamiami Formation (Quality
Aggregates, 3.2 Ma; Roulier and Quinn, 1995). Notice inverted scale of
δ18O.
Stable isotope data and linear extension rates
The bulk stable isotope compositions of the z corals studied were calculated
as the arithmetic mean of all measurements in a given specimen. The bulk
values range from -3.56 to -1.42 ‰ (mean -2.59 ± 0.65 ‰) in δ13C and -3.49
to -2.04 ‰ (mean -2.75 ± 0.37 ‰) in δ18O resulting in a significant
positive correlation (R2= 0.39; p= 0.013; Fig. 3).
All corals display cyclic variations in δ18O and in δ13C, interpreted to reflect seasonal cycles of sea surface temperature
(SST), seawater δ18O (δ18Ow), the ratio of
symbiont photosynthesis vs. heterotrophic feeding, and δ13C of
seawater DIC. The mean amplitude of the δ18O cycle ranges from
0.96 to 2.25 ‰ (mean 1.5 ± 0.41 ‰; Table 2). The mean annual maximum and minimum δ18O
values are -1.87 ± 0.60 ‰
(range -2.74 to -0.85 ‰) and -3.49 ± 0.32 ‰ (range -4.03 to -3.02 ‰),
respectively.
Carbon and oxygen stable isotope composition (‰
vs. PDB) of z corals, Pliocene and Pleistocene, Florida, USA.
Specimen
Taxon
Number of
Length of record
Bulk δ13C
Mean annual
Correlation
Average annual
Average annual
Mean seasonal
analyses (n)
(δ18O years)
(±1σ)
δ18O (±1σ)
coefficient (r)
maximum
minimum
Δδ18O (±1σ)
of δ13C/δ18O
δ18O (±1σ)
δ18O (±1σ)
EP1-S2
Solenastrea
76
16
-2.60 ± 0.99
-2.69 ± 0.22
-0.57
-1.95 ± 0.39
-3.41 ± 0.23
1.39 ± 0.48
EP2-S2
Orbicella
34
10
-2.19 ± 0.58
-3.21 ± 0.19
0.19
-2.71 ± 0.27
-3.74 ± 0.29
0.99 ± 0.43
EP3
Porites
58
4
-1.42 ± 0.43
-2.46 ± 0.43
0.06
-1.50 ± 0.42
-3.05 ± 0.28
1.60 ± 0.20
EP4-S2
Solenastrea
35
4
-1.93 ± 0.76
-2.62 ± 0.19
0.73
-2.27 ± 0.30
-3.45 ± 0.13
1.15 ± 0.24
EP5-S2
Solenastrea
62
8
-2.38 ± 0.66
-2.60 ± 0.23
-0.55
-1.67 ± 0.27
-3.35 ± 0.09
1.67 ± 0.22
EP6-S2
Solenastrea
54
4
-2.86 ± 1.18
-2.26 ± 0.25
-0.68
-1.30 ± 0.55
-3.51 ± 0.29
2.25 ± 0.86
EP8
Solenastrea
42
5
-3.35 ± 0.43
-3.50 ± 0.10
0.21
-2.74 ± 0.15
-4.03 ± 0.15
1.28 ± 0.33
EP9A
Solenastrea
68
15
-3.26 ± 0.54
-3.02 ± 0.26
0.45
-2.61 ± 0.35
-3.55 ± 0.27
0.96 ± 0.31
EP9B
Orbicella
48
4
-3.02 ± 0.72
-2.93 ± 0.33
-0.26
-2.14 ± 0.39
-3.86 ± 0.08
1.57 ± 0.43
EP9C
Solenastrea
135
12
-2.76 ± 0.52
-2.98 ± 0.25
-0.12
-2.35 ± 0.18
-3.60 ± 0.29
1.25 ± 0.33
EP9D
Solenastrea
69
12
-3.03 ± 0.77
-3.11 ± 0.23
0.45
-2.12 ± 0.29
-3.91 ± 0.30
1.79 ± 0.36
Coral #1**
Solenastrea
286
49
-3.56 ± 0.57
-3.19 ± 0.19
0.33
-2.22 ± 0.27
-3.89 ± 0.21
1.68 ± 0.26
452-K1*
Solenastrea
468
35
-1.69 ± 0.55
-2.23 ± 0.30
-0.03
-1.02 ± 0.46
-3.10 ± 0.28
2.06 ± 0.50
452-K4-S1
Solenastrea
99
14
-2.88 ± 0.72
-2.59 ± 0.19
0.15
-1.61 ± 0.42
-3.29 ± 0.28
1.69 ± 0.48
452-K14-S6
Solenastrea
77
14
-1.84 ± 0.50
-2.58 ± 0.24
0.26
-1.95 ± 0.76
-3.36 ± 0.35
1.73 ± 0.93
* From Böcker (2014).
** From Roulier and Quinn (1995).
For δ13C, we present the bulk values of the z corals which
range from -3.56 to -1.42 ‰ with a mean of -2.59 ± 0.65 ‰ (Table 2). We do not present
statistics for the seasonal amplitude of δ13C because the
variation of δ18O and δ13C is not necessarily in
phase within a year and no independent age model has been used for δ13C. Phase relationships among
the δ18O and δ13C cycles differ between individual coral colonies as expressed by
the correlation of their δ18O and δ13C data. Three
well-expressed patterns exist: positive correlation, no correlation, and
negative correlation (Fig. 4, Table 2). Positive correlations denote
spatially coincident negative and/or positive isotope values whereas negative
correlations are the expression of coincident positive and negative peaks of
the isotope cycles (= 180∘ phase shift). No correlation is less
straight forward to interpret and has two possible underlying causes: (1) a
phase shift between 0 and 180∘ or, (2) the absence of
any well expressed cyclic signal in δ13C. Relationships of the
coefficient of correlation from subannual δ18O/δ13C values with skeletal δ18O values are noisy and barely
significant; nonetheless, a significant positive correlation exists with
mean annual δ18O (R2= 0.28; p= 0.050) but not so with
mean seasonality (R2= 0.13; p= 0.214) and mean peak summer values
(R2= 0.08; p= 0.317), but to some degree with mean peak winter
values (R2= 0.22; p= 0.087). All seasonally resolved coral records
are shown in Fig. 4, and an overview of the main compositional trends is
given in Table 2.
Relationships of skeletal δ18O with the coefficient
of correlation between subannual δ18O and δ13C
values.
In the seasonally resolved data sets, a positive correlation exists between
bulk δ18O and winter-δ18O (R2= 0.90; p < 0.001) and summer-δ18O (R2= 0.80; p < 0.001),
respectively, however, the slopes of the two relationships significantly
differ and document large δ18O-seasonality to coincide with
more positive bulk δ18O and small δ18O-seasonality
to coincide with more negative bulk δ18O (equality of slopes
can be rejected at p < 0.001; Fig. 6). A positive relationship also
exists between bulk δ13C and the means of peak seasonal δ18O
(R2= 0.61; p= 0.001 and R2= 0.28; p= 0.051),
but the slopes of the relationships remain indistinguishable (equality of
slopes cannot be rejected at p= 0.78), i.e. seasonality does not change
with bulk δ13C (Fig. 6). Further, the mean of the maximum
values in δ18O and mean seasonal δ18O contrast
(Δδ18O) display a positive correlation (R2= 0.76, p < 0.001), whereas there is no such relationship among means
of the minimum δ18O values and mean Δδ18O
(R2= 0.22, p= 0.069; Fig. 7). For the sake of simplicity in the
following text, we use the terms mean summer for the mean of the minimum
values and mean winter for the mean of the maximum values of δ18O.
Bulk stable isotope composition (δ13C, δ18O) compared to the averages of the minimum and maximum values of
δ18O interpreted to represent maximum summer and winter,
respectively.
From this pattern we infer the following general nature of the δ18O and δ13C cycles: (1) low seasonality coincides with
particularly negative bulk δ18O values, whereas bulk δ13C has no relationship with seasonality; (2) variability in the
seasonality of the δ18O cycle (Δδ18O) is
an effect of variations of the mean winter δ18O values only,
whereas the mean summer δ18O values display little variation;
(3) mean peak winter δ18O values are increasingly positive in
parallel with the bulk δ18O, and (4) the phase shift between
the δ18O and δ13C cycles increases with more
positive winter δ18O values of the δ18O cycles.
(5) Bulk δ13C values are particularly negative in specimens
displaying negative mean summer and winter δ18O (Fig. 6). These
relationships imply a causative link between bulk δ18O, Δδ18O and the phase relationship of δ13C and
δ18O.
Z-corals from one single sampling site or between sites do not exhibit any
consistent distributional systematic of the three δ13C/δ18O correlation patterns described above, i.e. all three patterns
might be encountered at one single site and, therefore, no systematic
distribution exists over geological time and inconsistent patterns over
geological time are not the effects of potential shortcomings of
stratigraphic classifications.
Mean seasonal contrast of skeletal δ18O (mean Δδ18O) compared to the means of maximum summer and winter
skeletal δ18O.
Calcification
In positive prints of radiographs all corals display well expressed
alternations of light and dark bands arranged parallel to the surface of the
corallum (the colonial skeleton) and normal to the direction of maximum
growth of the corallites (Fig. 8). No specimens without density bands, or
specimens displaying a patchy concentration of zones with high or low
density, except for the expression of large borings by bivalves, were
documented in the material recovered (Fig. 8).
These alternating bands of high and low density are commonly present in
massive heads of z corals, and referred to as “density bands” because the
changes in grey tones of the radiographs reflect density variations of the
coral skeleton (Knutson et al., 1972; Lough and Cooper, 2011). The
alternating density bands without any indication of patchy or blurred
density variations is an indication of the good preservation of the original
skeletal density variation without any secondary modifications through
diagenesis. In this study, however, we do not use the density bands for
calibrating internal chronologies and calculating linear extension rates but
use the oxygen isotope cycles instead (Fig. 8). Skeletal linear extension
rates were established from δ18O cyclicity, and they range from
0.16 to 0.83 cm yr-1, with a mean of 0.49 ± 0.22 cm yr-1 (Table 3). More details on the determination of linear extension
rates and relationships with the δ18O cycles are given in the
“methods” section.
Mean annual skeletal extension rate (±1σ),
bulk density (±1σ), and calcification rate of massive
corals (Solenastrea, Orbicella, Porites) from the Plio-/Pleistocene of Florida. Minimum δ18O
values reflecting high water temperature and/or positive water balance are
being referred to as “summer”, maximum δ18O values cool
temperatures and/or negative water balance are referred to here as
“winter”. Timing of the high density band (HDB) relative to the δ18O cycle.
Specimen
Taxon
Mean extension
Bulk density
Calcification rate
Timing of HDB
rate (cm yr-1)
(g cm-3)
(g cm-2 yr-1)
(summer/winter/
intermediate)
EP1-S2
Solenastrea sp.
0.28 ± 0.08
1.22 ± 0.17
0.34
10/0/1
EP2-S2
Orbicella annularis
0.16 ± 0.03
1.14 ± 0.25
0.18
6/3/1
EP3
Porites sp.
0.86 ± 0.22
0.60 ± 0.12
0.52
0/4/0
EP4-S2
Solenastrea sp.
0.45 ± 0.28
n.a.
n.a.
0/4/0
EP5-S2
Solenastrea sp.
0.37 ± 0.06
1.22 ± 0.21
0.45
8/2/0
EP6-S2
Solenastrea sp.
0.83 ± 0.21
0.55 ± 0.06
0.46
1/2/0
EP8
Solenastrea sp.
0.38 ± 0.05
1.16 ± 0.12
0.44
2/3/1
EP9A
Solenastrea sp.
0.22 ± 0.08
0.94 ± 0.16
0.21
10/3/0
EP9B
Orbicella annularis
0.64 ± 0.25
0.76 ± 0.09
0.48
0/4/0
EP9C
Solenastrea sp.
0.58 ± 0.11
0.73 ± 0.08
0.43
0/10/2
EP9D
Solenastrea sp.
0.29 ± 0.05
1.00 ± 0.18
0.29
9/1/2
Coral #1a
Solenastrea bournoni
0.41 ± 0.09
n.a.
n.a.
0/42/9
452 K1 total
Solenastrea sp.
0.63 ± 0.16
0.73 ± 0.90
0.4 to 0.5
10/20/11
(ø = 0.45)
452, lower segment
Solenastrea sp
0.71 ± 0.14
0.70
0.50
452, upper segment
Solenastrea sp.
0.55 ± 0.17
0.56
0.31
452-K4-S1
Solenastrea sp.
0.35
0.93 ± 0.14
0.33
7/2/6
452-K14-S6
Solenastrea sp.
0.26
1.52 ± 0.25
0.40
7/3/2
509Ab
Solenastrea sp.
0.36 ± 0.15 (0.22)
n.a.
n.a.
n.a.
a No data on bulk density and extension rates available (Roulier
and Quinn, 1995).
b Extension rate from spacing of density bands, in parentheses from
δ18O data (Böcker, 2014).
Digital radiographs (positive prints) of fossil z corals showing
density bands (Pliocene and Pleistocene) of Florida. Circular white spots
represent open voids of bivalves borings. (a) Solenastrea sp. (EP9D). (b) Solenastrea sp. (EP9B).
(c) Solenastrea sp. (EP9A). (d) Orbicella encrusted on a hardground (EP 8). (e) Solenastrea sp.,
white patch within
the centre is from bioerosional cavity. (g) Solenastrea sp. (EP1) (f) Porites sp. (EP3). For
better contrast, steel balls (ø = 0.5 mm) mark sampling transect. Scale
bar 2 cm, all radiographs reproduced to same size.
With regard to the δ18O and δ13C cycles, no
consistent relationship was found with the density bands. Rather, within any
given fossil sample, maximum skeletal density either coincides with the
maximum or minimum δ18O values, but specimens with an irregular
timing of the HDB with respect to the δ18O cycle are also
present. We express the relationship of the density bands and δ18O cycles by the winter HDB portion (Fig. 9, Table 2). The winter HDB
portion was calculated as the ratio of the number of winter HDBs and the
total number of HDBs in a stable isotope record; the summer HDB and
intermediate-HDB portions were calculated respectively. In one of the two
long records (452K1) the overall timing of the HDBs is irregular with a low
summer HDB portion, although within short segments of a few years of
duration, the timing of the HDBs is uniform and related either to maximum,
minimum or intermediate δ18O values (Fig. 4, Table 2). Because
the corallites sampled were selected according to their orientation parallel
to the surface of the coral slabs, asynchronies between stable isotope
cycles and density bands are not an artifact of distortions in our X-ray
images (Le Tissier et al., 1994). With regard to the
distribution of the patterns on the scale of a reef (geological outcrop) or
geological time (time slice), we do not observe any consistent pattern;
rather all types of density band/δ18O relationships were
recovered at one single site or time slice.
Relationship of annual extension rate, density and calcification
rate with the timing of density banding in Pliocene and Pleistocene z corals
from southern Florida (USA).
Quantitative measurements of density were performed in transects arranged
parallel to the corallites and transects of the isotope measurements. Bulk
density, calculated as the means of all individual measurements along a
transect is highly variable among corals with a range from 0.6 to 1.2 g cm-3 (mean 0.9 ± 0.2 g cm-3). Bulk density and
extension rate display a significant negative correlation (R2= 0.42, p= 0.003). Over time, no significant changes in density were recorded
(R2= 0.04, p= 0.438).
Discussion
Interpretation of the stable isotope systematics
Linear positive correlations of paired δ13C/δ18O
data are common in skeletal carbonates and have been shown to be related to
kinetic isotope effects responding to variable rates of skeletogenesis
(McConnaughey, 1989). Kinetic behaviour involves simultaneous depletion
of δ13C and δ18O with respect to isotopic
equilibrium which results in a positive correlation of δ13C/δ18O along a straight line between equilibrium and
values 10 to 15 ‰ more negative in δ13C and
4 ‰ in δ18O than expected from equilibrium
precipitation (McConnaughey, 1989). The positive correlation of the
paired bulk stable isotope values from the fossil Florida z corals, however,
is not a kinetic signature because a positive correlation of δ13C and δ18O is not necessarily present in the seasonal
data which do show all transitions from positive correlation to no
correlation and negative correlation among the various coral specimens.
Furthermore, average linear skeletal extension rates of the Florida fossils
are rather high (n= 15; mean = 0.49 ± 0.22 cm yr-1;
Table 3) which rules out variability of the serial stable isotope data
presented in this study having no environmental meaning (McConnaughey,
1989). The positive trend of bulk δ13C/δ18O as
recorded by the Pliocene and Pleistocene z corals, therefore, represents a
distinct environmental proxy record (Fig. 3). The pattern may have at least
two different underlying causes: (1) a proximity trend reflecting a
continuum of settings from freshwater-influenced environments with the most
negative δ18O and δ13C values towards
near-shore-restricted, and finally open, well mixed environments with the
most positive stable isotope signatures (Andrews, 1991; Joachimski,
1994), or (2) variable upwelling of cool, nutrient enriched subsurface water
masses. According to scenario (1), corals with the most positive δ13C and δ18O signatures may be interpreted as the most
marine and the least affected by environmental restriction and hinterland
effects. Such a trend of positive correlation between bulk oxygen and carbon
stable isotope values of the fossil z corals is not, however, present in
data from modern and Holocene z corals from Florida Bay, Florida Reef Tract,
and Dry Tortugas (Figs. 1, 3). In these corals, bulk stable isotope values
display substantially larger variation than in the Pliocene and Pleistocene
fossils, and range from -4.07 to -0.20 ‰ in δ13C (n= 11; mean
-1.53 ± 1.31 ‰)
and δ18O from -4.11 to -2.47 ‰ (mean -3.64 + 0.46 ‰) with a negative correlation
(R2= 0.40; p= 0.036; Fig. 3). The negative correlation, however, is an
artifact of the set of literature data available to us and is lost if the
coral data from Florida Bay and from the reef systems were considered
separately (reef tract only: n= 10; R2= 0.02; p= 0.668). In the
recent corals, the negative δ13C value derives from a single
Florida Bay coral and records the low δ13C of the DIC in the
bay waters formed by oxidative decay of organic matter and/or vegetative
respiration (Halley and Roulier, 1999). In the fully open-marine
settings of the reef tract positive skeletal δ13C reflects the
marine carbon source of the DIC modified by metabolic effects. There,
spatially variable skeletal δ13C records also derive from bay
waters leaving the bay through passes in the Florida Keys where they mix
with waters of the reef tract (Swart et al., 1996; Figs. 1, 3). In contrast, the δ18O values from z corals are essentially
identical among reef sites along the present-day reef system and are
predominantly controlled by SST effects with minor modifications by δ18Ow (Leder et al., 1996; Smith, 2006). Skeletal
δ18O values in Florida Bay are the most positive and reflect a
high temperature signal to be overcompensated by the counteracting effects
of evaporation in conjunction with influx of pre-evaporated freshwaters from
adjacent swamps (Swart et al., 1996). For these reasons,
the modern Florida model is likely not a good analogue for understanding the
middle Pliocene to early Pleistocene records. This inference has also been
made from the highly diverse Plio-Pleistocene reefs in south-west Florida
(Meeder, 1979). In contrast, in the upwelling scenario (scenario 2)
increasingly positive δ18O reflects surface water cooling in
response to upwelling of cool nutrient-rich subsurface waters, while
concomitant increasingly positive skeletal δ13C documents
enhanced organic productivity (Berger and Vincent, 1986). Below, we
will discuss the significance of the δ18O cycles for a
plausible identification of the mechanisms behind the stable isotope record.
Significance of the δ18O cycles
The annual δ18O cycle is typically represented by seven samples,
however, the resolution ranges from 2 to 21 samples per cycle (n= 185;
mean 7.0 ± 3.3 samples cycle-1). Irrespective of the
number of samples over a cycle, we consider the cycles to represent a
seasonal signal which is used for defining the internal age models of the
corals and for calculating annual linear extension rates (Table 3). Although
there is little doubt the δ18O cycles reflect seasonality,
sampling resolution within a year has been suggested to have a measurable
effect on the amount of reconstructed seasonality (Leder et al.,
1996). Earlier work on fossil corals has suggested a minimum of four samples in
a year to be sufficient to resolve the seasonal cycle in geological data
(Brachert et al., 2006b). For this reason, we consider our
records a useful approximation to palaeoseasonality during the late Neogene.
Mean summer δ18O values of the fossils display little variation
around their mean, whereas mean winter values display high variability and a
strong link with mean Δδ18O variability (Fig. 7). For
this reason, variability of Δδ18O is a function of
variable winter values. For evaluating the question whether variability of
winter δ18O values is a temperature or seawater effect, we use
the bulk δ13C data. Bulk δ13C shows no
relationship with Δδ18O, i.e. the amount of variation
in Δδ18O is not related with seasonal changes of the
isotopic composition of the DIC as might occur through freshwater discharge
or upwelling (Fig. 6). For this reason, significant subannual variations in
δ18Ow are not very plausible as an explanation for the
observed variable seasonality which is rather controlled by fluctuations of
the winter temperature.
Paleotemperatures
For quantitative temperature reconstructions, the isotope composition of the
ambient water itself plays a critical role. Because the oxygen isotope
composition of the palaeoseawater is not known, we use the modern seawater
composition at the Florida reef tract (δ18Ow= 1.1 ‰; Leder et al., 1996) as a baseline for
our reconstructions and for eventually making inferences about palaeoseawater
δ18Ow and the extent of freshwater discharges or
evaporation. For our estimates we further assume all corals to have lived
within the same water-depth window and type of environment. Following this
approach, the mean annual temperature averaged over all coral specimens
(n = 15) was 22.6 ± 1.9 ∘C (range 19.5 to
26.0 ∘C) with an average mean seasonality of 7.2 ± 1.9 ∘C (range 4.3 to 10.2 ∘C). The latter
reconstruction is surprisingly similar to modern instrumental seasonality of
7 to 9 ∘C along the reef tract (Leder et al.,
1996; Smith, 2006), but the reconstructed mean annual SST is below
present-day's annual mean temperature of 27 ∘C
recorded at Looe Key (Smith, 2006) and ∼ 25 ∘C along the south-western Florida coast (Fort Myers). In contrast, middle
Pliocene to early Pleistocene interglacial temperatures in the western
Atlantic warm pool were ∼ 2 ∘C above present values
(O'Brien et al., 2014). For this reason, changes in global
interglacial seawater δ18Ow and the hydrological balance
of the Florida peninsula must be taken into account for interglacials of the
late Neogene (Brachert et al., 2014). In order to resolve
Pliocene–Pleistocene interglacial SSTs 2 ∘C above present, we
infer values of local δ18Ow with a range between 1.9 to
2.9 ‰ on the basis of the temperature equation of Leder
et al. (1996), although middle Pliocene to early Pleistocene global
interglacial seawater δ18Ow was similar to the
present day, or even more negative (Zachos et al., 2001).
Substantially more negative water values for the peninsula of δ18Ow= 1.0 ‰ have been inferred by
modelling Pliocene conditions (Williams et al., 2009).
According to this line of reasoning, evaporation should have been an
essential driver of Pliocene and Pleistocene bulk skeletal δ18O,
and the z corals with the most positive bulk δ18O values being
similar in magnitude to the recent Florida Bay coral have an evaporative
signature in δ18O. These corals, however, according to the
positive relationship of paired bulk δ13C/δ18O
values, have the most open-marine δ13C signature, incompatible
with concomitant maximum evaporation archived in skeletal δ18O.
We suggest, therefore, rejecting scenario (1) with evaporation having a
strong imprint in δ18O signatures in favour of an alternate
scenario (2) involving upwelling of cool and nutrient-rich waters peripheral
to the Florida carbonate platform causing positive bulk δ13C
signatures and lower than expected water temperatures.
Schematic of endmember relationships of stable isotope data with
the patterns of calcification and the timing of the HDB in middle Pliocene
to early Pleistocene z corals from south-western Florida.
Relationships between stable isotope signatures and calcification
systematics
The couplets of light and dark bands visible in radiographs orientated
parallel to the individual corallites reflect the successive upward growth
of the colony surface and are analogous to bands of density variation
reported from modern z corals (Knutson et al., 1972; Lough and Cooper,
2011). The density bands reflect the coral's response to
environmental changes in growth conditions, commonly seasonal, and have,
therefore, been used to create multi-annual chronologies and to make
reconstructions of environmental change during the last few centuries
(Felis and Pätzold, 2004). In contrast to records from
modern corals, the couplets of high and low density bands seem to not
represent necessarily 1 year of coral growth, because the δ18O cycles do not consistently correspond with the density couplets.
Instead, we observe corals from the same site of growth where the HDBs
coincide with the most positive, intermediate or the most negative δ18O values. Although there is no evidence for the asynchronies
resulting from distortions of the bands in the X-ray images, the
asynchronies of the density bands and stable isotope cycles bear some risk
of representing an artifact of our age models which are based on the most
positive δ18O values to define the beginning of each year, i.e.
the winter temperature minimum. This assumption is only valid, however,
under the premise of a dominant temperature control on the δ18O
values with no or subordinate isotope effects related to
evaporation and precipitation. In our material, this assumption is valid for the
following three reasons: (1) no evidence exists in the cyclic isotope
patterns for some of the cycles to be inverted from being controlled by SST
to effects related to evaporation and precipitation. Rather, the δ18O cycles are regular, and do not exhibit any erratic pattern on an
annual basis as described for a recent Solenastrea from Florida Bay subject to variable
evaporation (Swart et al., 1996; Fig. 4). (2) Within
individual specimens, the cycles of δ18O and δ13C
exhibit consistent phase relationships which implies the driver of δ18O variability, likely SST, to have been systematically related to an
independent environmental parameter, e.g. cloud cover and/or DIC changes due
to river discharge in a rainy season or variable symbiont photosynthesis and
upwelling, and (3) the amount of SST seasonality inferred from the δ18O values is fully consistent with modern seasonality
(Leder et al., 1996; Smith, 2006). For these three
inferences we suggest the oxygen isotope cycle to represent the more
reliable internal chronology than the patterns of density banding, and the
rhythm of density banding to have been variable from coral to coral and to
some degree within corals. Disparities in skeletal growth rhythms have been
reported recently from female and male colonies within one taxon (Porites panamensis), with
female colonies growing slower and calcification rates being lower than in
males (Cabral-Tena et al., 2013). Fossil coral specimens from
the same site displaying reciprocal calcification rhythms relative to the
oxygen isotope cycles may, therefore, reflect gender differences as well.
Sex proportions of female : male colonies in the modern P. panamensis are
2:1
(Cabral-Tena et al., 2013), however, our set of data is too
small for a statistical evaluation, and gender differences are not
documented in the skeleton. Nonetheless, the observed variations in
calcification are likely not gender specific, because in some specimens no
relationship exists between the δ18O cycle and the rhythm of
growth banding, whereas it changes in others from the summer mode of HDB
formation to the winter mode or vice versa upon continual growth. This is
particularly obvious in records of long time series (Fig. 4, Tables 2, 3).
Interestingly, the timing of the density bands corresponds with annual
extension rate (and calcification rate). Small extension rates coincide with
HDBs formed during summer (R2= 0.50; p= 0.002), intermediate
extension rates with an irregular timing of the HDBs, and large extension
rates with the predominance of winter HDBs (R2= 0.56; p= 0.001; Fig. 9). Bulk density also displays relationships with the chronology of
the HDBs: a high summer HDB portion corresponds with high density (R2 = 0.50; p= 0.029), and high winter HDB portions with low bulk density
(R2= 0.38; p= 0.012). With regard to calcification rate, corals
having winter HDBs have the highest calcification rates (R2= 0.52;
p= 0.003) and those with summer HDBs have the lowest calcification rates
(R2= 0.41; p= 0.014). This overall relationship differs from
modern z corals of the Western Atlantic region which have summer HDBs but,
on average, higher rates of extension and higher density than the fossil
corals (own data base, not shown). From this difference we deduce the
variability in calcification to be not so much related to gender but rather
to the type of growth environment. Interestingly, in a modern reef site from
the Red Sea, a distinct water-depth effect on extension rate and the timing
of the HDB has been reported (Klein et al., 1993). At a depth of 3 m extension rates are highest and the HDB is formed during winter, whereas
at 51 m of water depth extension rates are at their lowest and the HDB is formed
during summer. This corresponds with a decrease of the
phototrophy/heterotrophy ratio (P / H) reflected in δ13C
(Klein et al., 1993). This shift of the timing is consistent with
the data from the Florida fossil z corals, however, we rule out any
water-depth effect, because repeated shifts of the timing of the HDB, and
likely also changes in extension rate, are present at the level of single
z coral specimens and not between specimens or sites only. Rather, the
fossil data may document changes in the P / H ratio due to turbidity and or
food supply for heterotrophic feeding.
In addition to the oxygen isotope signal, the carbon stable isotopic signal
of the corals displays a more or less distinct cyclic variation with the
same wavelength as the oxygen isotope cycle though variably phase shifted.
For this reason, it can be considered an annual signal as well. For
evaluating the principal driver of δ13C variability in the
fossil z corals, we consider the phase relationships of the δ18O and δ13C cycles expressed by the significant
correlation coefficients (r). They differ among specimens with values
between r=+1 (= in phase) and r=-1 (= in antiphase). A clear
negative linear relationship of r exists with mean annual δ18O
values (R2= 0.28; p= 0.050), whereas there is no well-defined
relationship with the seasonal means: mean winter δ18O (R2 = 0.22; p= 0.087) and mean summer (R2= 0.08; p= 0.317; Fig. 5).
This suggests specimens recording rather temperate temperatures and cold
winters to have the δ13C cycles in antiphase with the δ18O cycles, i.e. specimens reflecting cold winter periods have the
δ13C minimum during winter and vice versa.
Upwelling as a driver of high skeletal productivity?
Enhanced upwelling peripheral to the Florida platform causing cool and
nutrient-enriched waters to flush the platform was suggested earlier as a
cause for high skeletal productivity during the Pliocene and Pleistocene
interglacials. This reconstruction was based on taxonomical, paleoecological
and taphonomical data (Allmon, 2001; Allmon et al., 1995, 1996; Emslie and Morgan, 1994; Jones and Allmon, 1995). Most conspicuous is
the occurrence of the cormorant bed from the Pliocene, illustrating events
of mass mortality in seabirds depending on upwelling (Emslie and
Morgan, 1994). For the cormorant bed we tend to infer the upwelling to have
been intermittent. Stable isotope evidence found in molluscan shells,
however, remains inconclusive with regard to the origin of high productivity
(Jones and Allmon, 1995; Tao and Grossman, 2010). In
contrast to earlier work, we use a positive correlation of bulk δ18O and bulk δ13C as a signature of upwelling (Figs. 3,
10), which documents the combined effects of SST cooling and enhanced
organic productivity on skeletal carbonate production (Berger and
Vincent, 1986). The δ13C in corals is controlled by a number of
factors, and the identification of single factors driving z coral δ13C is not currently possible (Swart, 1983). Most important are
the activity of the photosymbionts relative to heterotrophic feeding (P / H
ratio) and δ13C of the DIC in ambient seawater (Klaus et
al., 2013; Swart, 1983; Swart et al., 2010). Organic production by
zooxanthellae and plankton preferentially consumes 12C, driving coral
skeletal δ13C towards more positive values (Berger and
Vincent, 1986; Swart, 1983). A positive bulk skeletal δ13C
will, therefore, reflect either a high longer-term P / H ratio, organic
production, or a combination of both, and specimens displaying positive bulk
skeletal δ13C in conjunction with positive bulk δ18O values will correspondingly reflect increased photosymbiont
activity during cool years or prolonged upwelling. In order to sort out the
principal driving mechanism, we have identified two endmember scenarios in
the isotope and calcification data (Fig. 10). Endmember 1 is represented by
z corals with the most negative bulk δ18O and δ13C
values, low Δδ18O and positive correlation of the
sub-annually resolved δ18O and δ13C data (positive
r). We suggest endmember scenario 1 to represent a hot water situation with low organic
productivity and low seasonality; maximum organic productivity occurred
during winter. Annual skeletal extension rates were low, bulk density high,
and bulk calcifications rates were low; the HDB formed during summer, likely
in parallel with lowest extension rates. Endmember 2 has the most positive
bulk δ18O and δ13C values, high Δδ18O and negative r. Annual skeletal extensions rates were high but
bulk density low; annual calcification rates were high as well, and the HDB
formed during winter. Relative to endmember 1, it represents a more
temperate situation with high bulk organic productivity and high temperature
seasonality; maximum organic production occurred during summer (Fig. 10).
Low organic productivity in endmember 1 is likely an effect of hot,
oligotrophic surface waters as indicated by combined negative bulk δ18O and δ13C. Maximum symbiont activity and skeletal
calcification occurred during winter, whereas they were low during summer
time, likely because light saturation was reached at excessive summer SSTs
causing photoinhibition, bleaching or expulsion of photosynthetic algae
(McConnaughey, 1989). A shallow depth of growth of the corals seems not
to be the crucial factor here, because many corals record fluctuations
between both endmember stages (Fig. 4). Expulsion of symbiotic algae is
perhaps the most likely cause because modern Solenastrea dominating our samples is
known to be facultatively zooxanthellate (Allmon, 1992). Under the
cooler annual SSTs of endmember 2, organic productivity and skeletal
calcification were high, particularly during summer. Organic production,
planktonic and/or zooxanthellate, were on average higher than in scenario 1,
and maximum production during summer likely reflects the positive
interference of planktonic and zooxanthellate productivity on skeletal
δ13C during the warm and sunny season in a context of
longer-term upwelling. Because recorded SST seasonality was high under these
conditions, upwelling is likely to have been less intense during summer or
to have been complemented by pronounced winter cooling. Winter cooling is
compatible with the recent upwelling systems on the western Florida shelf,
i.e. a positive interaction of an intensified LC and wind systems favouring
Ekman transport of subsurface waters onto the shelf and into the shallow
water zone (Fernald and Purdum, 1981; Li and Weisberg, 1999). This
inference is in agreement with notions of an intensified LC during
interglacials (Nürnberg et al., 2008). The high sea levels during
interglacials may have further promoted intrusions of nutrient-rich water
masses in the shallow water zone. In present-day Florida, exceptionally wet and
cool winter seasons also occur during El Niño events. Subdecadal, El
Niño-type cyclicity has been shown to be present in sclerochronology
records from corals in Florida and the Pacific and may explain the
interannual variability of our data sets (Roulier and Quinn, 1995; Watanabe
et al., 2011).
With regard to the systematics of z coral calcification, it is important to
note that the formation of the HDB dates during the period of minimum
organic production, likely minimum zooxanthellate activity, in both
endmember scenarios. We conclude the HDB is, therefore, the expression of
maximum skeletal density developed during periods of minimum skeletal
extension and minimum calcification rates, also because the fossil z corals
having small bulk extension rates have the highest bulk density but minimal
rates of skeletal extension and calcification. This calcification model is
compatible with modern z coral calcification patterns
(Carricart-Ganivet, 2004) and fits the environmental reconstructions
for the two endmember scenarios. Endmember 2 reflects growth conditions more
suitable to z coral growth than endmember 1, however, endmember 2 represents
a situation with more moderate SSTs than endmember 1. As suggested in
previous studies (Brachert et al., 2013; Worum et al.,
2007), our work confirms coral calcification to be non-linear, and coral
growth during Pliocene and Pleistocene interglacials to have occurred at
high temperatures beyond optimum as reflected by low calcification.
Although Pliocene global average temperature was higher than today, episodic
upwelling may have provided SSTs on Florida platform variably protected from
overheating (endmember 2).
But upwelling is generally ascribed as an adverse condition on z coral growth
and coral reef accretion because the upwelling deep-water masses potentially
cause cold reef kills, impose nutrient stresses and impede carbonate
cementation and skeletal calcification through phosphate poisoning and low
pH (Hallock, 1988; Hallock and Schlager, 1986; Manzello et al., 2014).
These negative effects, however, may be mitigated depending on the
intra-annual timing of seasonal upwelling (Chollett et al., 2010),
or if upwelling waters derive from rather shallow sources (Riegl and
Piller, 2003). In agreement with our inferences regarding calcification in a
context of upwelling (endmember 2), a study on z coral calcification in the
Galapagos upwelling zone found a negative effect on density but not so on
extension rates and calcification rates which were higher than expected from
known relationships (Manzello et al., 2014).
Our data set documents specimens representing the two endmember situations to
occur at one single sampling site and the two endmember situations to be
recorded even by one single coral specimen (Fig. 4). Therefore, the changes
of the two endmember conditions occurred on the time scale of a few years to
decades which seems to have created suboptimal environmental conditions for
most z coral taxa. The abundant occurrence of the eurytopic Solenastrea, which is also
tolerant to high turbidity, also suggests the platform not to have been an ideal refuge for z coral growth within the Western Atlantic warm pool as it may be
the case in an upwelling regime. In contrast to the global, long-term trend
of seawater δ18O (Zachos et al., 2001), interglacial
δ18O values of mollusk and z corals from Florida platform
became increasingly negative over time which implies an increasing moisture
import (Brachert et al., 2014), and likely a decrease in
upwelling intensity towards the present. The oldest specimen (age 3.2 Ma;
Table 1) investigated during this study represents a rather continuous record
of endmember 2 for ∼ 50 years of duration (Fig. 4d). More
records are needed, however, to test if this is a robust temporal trend.
It should be noted that modern z corals at the Florida Reef Tract form their
HDBs during the summer season, and therefore, their calcification patterns
resemble the endmember 1 situation described in this study. This may
possibly imply that further warming of the region will endanger coral
growth.