The state of a population of planktic foraminifers at a
certain time reflects multiple processes in the upper ocean, including
environmental conditions to which the population was exposed during its
growth, the age of the cohorts, and spatiotemporal patchiness. We carried
out depth-stratified (0–60, 60–100 m) replicated sampling off Puerto
Rico in autumn 2012, revisiting three stations previously sampled in autumn 1994 and spring 1995, in order to analyze seasonal and interannual
variability of planktic foraminifers and the stable isotopic composition of
their tests. The merged dataset from all three sampling campaigns allows us
to assess short- and long-term changes in foraminiferal population dynamics
and the spatial assemblage coherency along the shelf edge. All three
sample series cover more than 2 weeks during either spring (1995) or
autumn (1994, 2012) and include the time of the full moon when reproduction
of some surface-dwelling planktic foraminifers has been postulated to take
place. Our analyses indicate that interannual variability affected the
faunal composition, and both autumn assemblages were characterized by
oligotrophic tropical species, dominated by Trilobatus sacculifer and Globigerinoides ruber (white and pink variety).
However, G. ruber (white) had a higher abundance in 1994 (37 %) than in 2012 (3.5 %), which may be partially due to increasing sea surface temperatures
since the 1990s. Between 60 and 100 m water depth, a different faunal
composition with a specific stable oxygen isotope signature provides
evidence for the presence of the Subtropical Underwater at the sampling
site. Measurements on T. sacculifer sampled in autumn 2012 revealed that test size,
calcification and incidence of sac-like chambers continued to increase after
full moon, and thus no relation to the synodic lunar reproduction cycle was
recognized. During autumn 2012, outer bands of hurricane Sandy passed
the Greater Antilles and likely affected the foraminifers. Lower standing
stocks of living planktic foraminifers and lower stable carbon isotope
values from individuals collected in the mixed layer likely indicate the
response to increased rainfall and turbidity in the wake of the hurricane.
Introduction
Planktic foraminifers are unicellular marine eukaryotes that live in the
open ocean and build calcareous shells (called tests) around their cell.
Their assemblage composition in different water masses and the stable
isotope composition of their tests are widely used as proxies to reconstruct
past ocean conditions (e.g., Fischer and Wefer, 1999; Kučera, 2007;
Schiebel et al., 2018). Prevailing water mass conditions can influence the
distribution of planktic foraminifers in various ways. Studies on plankton
tows have shown that, for example, seasonal changes in temperature, food
availability (chlorophyll concentration), and upwelling conditions influence
the assemblage composition and standing stocks (e.g., Bé, 1977; Schiebel
et al., 2001; Retailleau et al., 2011; Jentzen et al., 2018b). Additionally,
foraminiferal assemblages in the water column are marked by small-scale
spatial variability (patchiness; Siccha et al., 2012; Meilland et al.,
2019) and also variability in the proportion between different ontogenetic
stages (juvenile and adult individuals). It has been suggested that the
reproduction of various species follows a lunar or semilunar periodicity
(Spindler et al., 1979; Almogi-Labin, 1984; Bijma et al., 1990). The
evidence is based on a laboratory culturing experiment, in which the
majority of individuals of a certain morphospecies reproduced around the
same day (Spindler et al., 1979) and is supported by field observations on
changes in abundance and size of individuals in the water column (e.g.,
Bijma et al., 1990; Schiebel et al., 1997; Jentzen et al., 2018b), as well as by
sediment trap series that reflect a periodic flux of tests (Lončarić
et al., 2005; Jonkers et al., 2015). Stable isotopes in foraminiferal tests
allow us to assess the physical properties of the ambient water column when
the foraminifer calcified (e.g., Steph et al., 2009); however, studies from
living planktic foraminifers reveal species-specific offsets to the seawater
isotopic composition (Spero and Lea, 1993; Jentzen et al., 2018a).
To add to our understanding of regional assemblage structure changes over
different timescales, we collected living specimens off the southern coast
of Puerto Rico and revisited the sampling sites of Schmuker (2000a, b)
from September to October 1994 and March 1995. The previous studies assessed
the influence of neritic environmental conditions and their seasonal changes
on living planktic foraminiferal assemblages. In particular, they revealed a
seasonal influence of the Orinoco River outflow plume on the southern coast
of Puerto Rico, which leads to eutrophic conditions in autumn. A higher
abundance of planktic foraminifers was consequently observed in autumn, with
Globigerinoides ruber (pink and white) as dominant species, while Globigerinella calida was the most abundant species
during oligotrophic conditions in spring. The studies additionally revealed
a faunal gradient from neritic environments near the coast to offshore
conditions, with lower standing stocks close to the shelf break. Shallow-water benthic foraminifers were found in plankton tows as well. Some of
those benthic species, for instance Tretomphalus bulloides, have a planktic stage during their
life cycle (meroplanktic life cycle; Rückert-Hilbig, 1983). Others were
probably brought in suspension on the shelf and transported further offshore (Schmuker, 2000b; Fornshell, 2005). Stable isotope measurements of the
planktic foraminifer G. ruber (white), conducted by Schmuker (2000b), showed lower
values of δ13CCALCITE during autumn compared to spring,
which might indicate reduced photosynthesis of the symbionts of the
foraminifers due to higher turbidity of the upper water column or reduced
light attenuation during the rainy season. This assumption refers to the
hypothesis of Spero and Lea (1993) that decreasing light levels lower
metabolic activity of the symbionts and thereby reduce photosynthetic
fixation of 12C in the calcifying foraminiferal microenvironment.
The results of Schmuker (2000a, b) from 1994 and 1995 are used as
baseline data to assess long-term changes in the foraminiferal assemblage
that happened during the past 17 years. In our study, we repeatedly
collected living planktic foraminifers over 2 weeks in 2012 at three
stations and two depth intervals off the southern coast of Puerto Rico. The
sampling sites of 2012 were close to those chosen by Schmuker in 1994 and
1995 (Schmuker, 2000b; Fig. 1). We intended to determine the dynamics and
spatial distribution of the foraminiferal assemblage on a weekly and decadal
perspective. Stable isotopes (δ18O and δ13C) were
measured in tests of G. ruber (pink) and related to in situ temperature and δ18OSEAWATER. Since the time span of our sampling campaign
extended over the full moon, we measured size and weight changes in the tests
of Trilobatus sacculifer, which may be related to synchronized reproduction, and monitored their
approximate living depth to detect ontogenetic migration. During the
sampling campaign in 2012, hurricane Sandy passed the Greater Antilles.
We used this unforeseen opportunity to examine the impact of such a storm on
the foraminiferal assemblage.
Location of the study area in southwestern Puerto Rico (Caribbean
Sea). The red crosses mark the plankton net stations of this study (1–3;
2012) and the blue dots mark the plankton net stations of Schmuker (2000b;
I–IV; 1994/1995; see Table 1). The maps were generated at
https://sfb574.geomar.de/gmt-maps.html (last access: 28 November 2012).
Our goal within this study is to assess the population dynamics of living
planktic foraminifers on a weekly, seasonal, and interannual timescale, and
to evaluate the spatial assemblage coherency along the shelf edge to
improve our understanding of short- and long-term variations. The results
will ultimately help to improve the applicability of foraminiferal
paleoproxies.
Regional settings
The southwestern margin of Puerto Rico is characterized by a very steep
slope, which commences at 20 m water depth on the shelf and extends to
1000 m water depth. This slope was probably created by the counterclockwise
rotation of the Puerto Rico block and associated strike-slip movements along
the branches of the Great Southern fault zone (Glover, 1971; Byrne et al.,
1985; Masson and Scanlon, 1991). Different water masses impinge the slope in
our study area. The uppermost water mass is the Caribbean Water (CW, between
0 and 50–80 m depth), which is a mixture of the Amazon and Orinoco River
outflow and North Atlantic surface water, with low salinity of <35.5 (Gordon, 1967; Schmuker, 2000b). The highly saline Subtropical Underwater
(SUW, >37 salinity) prevails between 50 and 250 m. The
18 ∘C Sargasso Sea Water and the Tropical Atlantic Central Water
belong to the water mass at depths below 250 m (Gordon, 1967; Morrison and
Nowlin, 1982; Gallegos, 1996). From August to November, surface waters in
the southeastern Caribbean Sea are influenced by plumes of the Amazon and
Orinoco rivers (Chérubin and Richardson, 2007), which result in
silicate-rich and low-salinity surface waters (Froelich et al., 1978;
Corredor and Morell, 2001). From June to November, the Atlantic hurricane
season affects the Caribbean Sea, inducing a thorough mixing of the upper
water column (Jacob et al., 2000; Blake et al., 2013; NHC, 2014).
Materials and methodsSample collection in 2012
The sampling campaign in 2012 took place at three different stations off
southern Puerto Rico and on 4 d within 2 weeks from October to
November (Fig. 1, Table 1). The stations were located on the upper slope
(station 1: 850 m water depth), shelf edge (station 2: 150 m), and on the
shelf (station 3: 20 m). An Apstein net (Hydro-Bios) and an open plankton
net were used to collect living planktic foraminifers. At station 1 and
station 2, the Apstein net with a mesh size of 100 µm and an aperture
of 17 cm in diameter was used to sample the 0–60 and 60–100 m depth
intervals. The net was hauled twice to double the volume of the filtered
water during each haul. A trigger weight was attached to the rope, which
released the shutter and closed the aperture of the net afterwards. The open
plankton net, which was used at station 3, also had a mesh size of
100 µm but an aperture of 40 cm in diameter. Because of the shallow
depth of about 20 m, vertical sampling was not possible. Instead, the open
net was pulled with the boat for 5 min horizontally in the upper 5 m
of the water column. The collected plankton samples were transferred to PVC
vials, diluted with filtered ambient seawater, and brought to the laboratory
within 2 h after sampling for further processing. In addition to the
plankton net hauls, salinity and temperature were measured in situ using a
hand-held conductivity meter (WTW LF 320 with a TetraCon 325 conductivity
cell) in the upper 25 m of the water column at stations 1 and 2 and down to
10 m water depth at station 3. The precision of the conductivity meter is
0.1 units, the accuracy is 0.116 units (1σ). Seawater samples of the
surface waters for stable oxygen isotopes were taken with a bucket and
stored in 100 mL glass bottles.
Station list with latitude, longitude, water depth (m), sampling
date, and sampling depth (m) from this study and Schmuker (2000b).
StationLatitudeLongitudeWater depthSampling dateSampling depth(m)(day/month/year)(m)1a17∘51.5′ N66∘59.13′ W85022 Oct 20120–60, 60–10029 Oct 20122 Nov 20125 Nov 20122a17∘53.13′ N66∘59.49′ W15022 Oct 20120–60, 60–10029 Oct 20122 Nov 20125 Nov 20123a17∘53.25′ N66∘59.51′ W2029 Oct 201252 Nov 2012Ib17∘53.6′ N67∘1.48′ W20Oct 19940–10Mar 1995IIb17∘52.3′ N67∘1.3′ W500Sep–Oct 19940–120Mar 1995IIIb17∘51.18′ N67∘1.3′ W900Sep–Oct 19940–120Mar 1995IVb17∘49.12′ N67∘0.36′ W1300Sep–Oct 19940–120Mar 1995
a This study. b Schmuker (2000b).
Sample preparation
In the laboratory of the marine station of the University of Puerto Rico at
Isla Magueyes, foraminifers were immediately wet-picked from the plankton
net samples and collected in Plummer cell slides. Samples that could not be
picked on the same day of sampling were preserved in a 50 %
ethanol–seawater solution and stored at 4 ∘C.
All tests of planktic foraminifers were filled with cytoplasm (i.e.,
yellowish, greenish-grey, or green cytoplasm) indicating that they were
alive at the time of collection. The specimens were identified on
a morphospecies level following the taxonomy of Bé (1967) and Schiebel and
Hemleben (2017). For Trilobatus sacculifer we differentiated the individuals with a sac-like
final chamber (T. sacculifer with sac) from the trilobus-morphotype with a regular, spherical
terminal chamber (T. sacculifer without sac). We distinguished between
Globigerinoides ruber (white), G. ruber (pink), and G. elongatus following Aurahs et al. (2011).
Benthic foraminifers in the plankton net haul samples were sorted into
separate Plummer cell slides by species, fixed with glue, and counted.
Specimens of Bolivina variabilis were filled with orange-red cytoplasm indicating that they
were alive at the time of sampling (Kučera et al., 2017). Tretomphalus bulloides contained
yellowish-brown cytoplasm as described by Cushman (1922) from living
individuals. Three Cibicidoides pachyderma specimens contained a greenish-brown granular infill,
which was interpreted as cytoplasm. Other individuals and species were empty
and the tests were dull, indicating that they were probably not alive at the
time of collection.
Foraminiferal assemblage analyses
To determine the relationship between species abundance, faunal composition,
environmental factors, and time, different statistical methods were used in
this study. Paired sample t tests (abundance of paired species within two
samples) and hierarchical cluster analyses with the Bray–Curtis similarity
were performed using the software PAST v.3.14 (Hammer et al., 2001). These
analyses test and visualize the similarity within and between each of the
different assemblages from sample stations (1–3) in 2012. Nonmetric
multidimensional scaling (NMDS; Kruskal, 1964) was used to compare the 2012
assemblage with assemblages from the same locations sampled in 1994 and 1995
by Schmuker (2000b). NMDS is a form of ordination that allows one to project the
multidimensional assemblage data into a 2-D space for better visualization of
the similarities and differences of assemblages observed across the decades.
For this, we used the R package “vegan” v. 2.0-10 in R v. 3.1.0
framework (R Core Team, 2014). For the NMDS, the dataset by Schmuker (2000b)
was reduced to the same species that we found in 2012 (Table 2), in order to
eliminate an overly strong influence of rare species. Additionally, we
limited the comparison to our stations 1 and 2, which correspond to stations III and II in Schmuker (2000b), respectively (see Fig. 1), because station 3
used a different sampling scheme making it incomparable. Schmuker (2000b)
sampled the complete 0–120 m interval at once; therefore, we combined our
stratified data to represent the complete 0–100 m depth interval for this
step. Only the fraction >150µm was analyzed in Schmuker (2000b); therefore, Turborotalita quinqueloba and Globoturborotalita rubescens are excluded from the analyses, because they are
commonly smaller in diameter than 150 µm and would thus be
overrepresented in our samples >100µm. The rare species
Pulleniatina obliquiloculata and Candeina nitida were excluded for the NMDS analyses as well in order to emphasize the
assemblage changes with a focus on abundant taxa. The standing stock of the
foraminiferal assemblage is given as individuals per cubic meter (ind. m-3). The filtered seawater volume was estimated by multiplying the
lengths of the net hauls with the opening net aperture area.
Species collected during sampling period in 1994/1995 (Schmuker,
2000b) and in 2012 (this study). Relative abundance of each species from the
total planktic or benthic assemblage is given for every sampling period.
Taxonomy is according to Bé (1967) and Schiebel and Hemleben (2017). We
distinguished the species based on morphogenetic studies following
a Weiner et al. (2015), b Aurahs et al. (2011), c André et
al. (2013), d Spezzaferri et al. (2015), and e Darling et al. (2009).
Type references are from the Ellis and Messina (1940) catalogue.
Test size and weight analyses of Trilobatus sacculifer
Since the time span of our sampling campaign in 2012 extended over the full
moon, we analyzed size and weight changes of Trilobatus sacculifer to test for lunar-synchronized reproduction (Erez et al., 1991). Therefore, all 655 intact and
cytoplasm-bearing individuals of T. sacculifer (622 specimens without sac, 33 specimens
with sac) from stations 1 and 2 were picked from the dried plankton samples.
We chose to use T. sacculifer for two reasons: (1) it had a sufficiently large population
size so that resulting morphometric analyses would be robust, and (2) it
consists of only one genotype (André et al., 2013), so any observed
changes could not be the result of changes in the inventory of cryptic
species.
Individual foraminifers were photographed using a binocular stereomicroscope
with a Canon EOS 600D camera. The length of each individual was manually
measured as a straight line along the longest visible axis of the shell,
i.e., maximum test diameter on the basis of these photographs using the
program FIJI v. 1.47q (Schindelin et al., 2012). All subsequent statistical
analyses were performed in SPSS v. 20 (IBM Corporation, 1989–2011).
Individual length measurements were log-transformed (natural logarithm) and
subjected to a generalized linear model (GLM) analysis (Nelder and
Wedderburn, 1972). The test size (as the dependent variable) was regressed
against the station (replication), sampling date, sampling depth, and the
interaction term of sampling date and sampling depth as independent
variables. As link function we used the identity for all species. The
log-transformed length measurements for T. sacculifer were not normally distributed (p<0.001), but it was clear from the histogram that the data follow a unimodal
asymmetrical distribution, thus we used the gamma distribution for the GLM.
All GLMs were tested using Spearman's rank-order correlation (Spearman,
1904) against their residuals, to evaluate their quality.
For the weight measurements we chose randomly 29 individuals of T. sacculifer without a
sac-like chamber, and 27 individuals with a sac-like chamber from all
samples. The weight was measured using a Sartorius SE 2 microbalance in
order to investigate test mass differences throughout the sampling period.
Together with measurements of the cross-sectional area obtained with
FIJI v. 1.47q (Schindelin et al., 2012), we calculated the area density
(AD = weight/area) of the specimens to constrain relative weight changes
throughout the sampling interval, which may indicate the precipitation of
gametogenic calcite (Bé, 1980).
Weight measurements were subjected to two additional analyses. For the first
analysis, all raw weight data were plotted against the log-transformed
cross-sectional area, and a linear regression (Eq. 1) was calculated for the
data points. On the basis of this regression line we categorized the weight
data into two categories: 1 – weight(observed)≤weight(calculated), and 2 – weight(observed)>weight(calculated). With those two weight categories we could calculate
the cross table with the respective date values and use a χ2 test
of association to determine whether or not the relative occurrence of light
and heavy individuals changed over the investigated time interval. For the
second analysis we applied a GLM corresponding to the one described above on
the AD instead of the length measurements, with identity as link function and
based on the normal distribution (p=0.162).
weight(calculated)=0.0165×logarea-0.1755
Analyses of stable isotopes
Stable oxygen and carbon isotopes of the calcite tests (δ18OCALCITE and δ13CCALCITE) of living
G. ruber (pink), with a similar test size of >100µm, were analyzed
in order to study the isotope signal of living specimens from the water
column and compare them to in situ environmental conditions (e.g.,
temperature). For each analysis, 4 to 10 individuals were taken from
different samples (see the Supplement, Table S2). Prior to the measurements, the
foraminifers were cracked to open the tests and to remove the remaining
cytoplasm with a needle. The measurements were performed on a
Thermo Scientific MAT 253 mass spectrometer equipped with a Kiel CARBO IV
carbonate preparation device at GEOMAR. The stable isotope results are given
relative to the Vienna Pee Dee Belemnite (V-PDB) in per mil
(‰) and calibrated versus the National Bureau of
Standards (NBS) 19. The reproducibility (±1σ) of the
in-house standard (Solnhofen limestone) is <0.06 ‰ for δ18O and <0.03 ‰ for δ13C. Stable oxygen isotope values of
the seawater (δ18OSEAWATER) were measured on an
isotope-ratio mass spectrometry (IRMS) at Hydroisotop GmbH
(Schweitenkirchen). The results were reported in per mil
(‰) versus Vienna Standard Mean Ocean Water (VSMOW) and
the analytic precision is ±0.1 ‰ (1σ).
δ18OEQUILIBRIUM was calculated after the δ18O temperature equation of Kim and O'Neil (1997) for inorganic
precipitation with in situ temperatures recorded during the sampling
campaign, and seawater values (δ18OSEAWATER) scaled to PDB
by subtracting 0.27 ‰ (Hut, 1987).
ResultsSeawater properties during sampling
Sea surface temperatures (SSTs) and sea surface salinities (SSSs) were
measured in near-surface waters during the sampling campaigns in 1994, 1995,
and 2012 (Fig. 2a). High SSS values were recorded in March 1995 and lowest
values were measured in October/November 2012. In general, the SST showed
low values during early spring (March) and higher temperatures during autumn
(September–November). Further, we note generally higher SSTs (around
1 ∘C) in 2012 as compared to 1994 at the same locations (Figs. 1,
2a). Stable oxygen isotope values of ambient surface water (δ18OSEAWATER) ranged from 0.76 ‰ to 0.91 ‰ VSMOW
(see the Supplement, Table S3). At the marine station of Isla Magueyes, an
increased daily average wind speed (up to ∼12 km h-1) and a
high daily precipitation (up to ∼70 mm) were recorded in late
October 2012, depicting the impact of the outer rainbands of hurricane
Sandy (Fig. 3).
Hydrographical data in the study area. (a) Sea surface temperature
(SST), sea surface salinity (SSS), and moon phases during the sampling
campaigns in 1994/1995 (Schmuker, 2000b) and 2012 (this study, see
the Supplement for data). Hurricane Sandy passed the Greater Antilles in
late October 2012 (red arrow). (b) MODIS-Aqua monthly climatology chlorophyll
concentration for October (2002–2018) and March (2003–2019). Images are
derived from NASA Goddard Space Flight Center, Ocean Ecology Laboratory,
Ocean Biology Processing Group (https://oceancolor.gsfc.nasa.gov/l3/, last
access: 8 October 2019).
Wind speed and precipitation record during October and November 2012 recorded by the Bio-Optical Oceanography Laboratory at the field
station at Isla Magueyes, La Parguera (University of Puerto Rico,
Mayagüez Campus (UPRM); http://bio-optics.uprm.edu, last access: 12 December 2018).
Grey dots and dashed line: average daily wind speed (km h-1); blue bars: daily
precipitation (mm); red numbers indicate the sampling dates (day/month) in
2012; circles indicate the moon phases. Hurricane Sandy passed the
Greater Antilles in late October 2012.
Foraminiferal assemblage in plankton net haulsOverview
Fifteen living planktic foraminiferal species and nine benthic species were
identified in the plankton net hauls at the different stations in 2012
(Table 2). The planktic assemblages are dominated by the tropical and
subtropical species G. ruber (pink) and T. sacculifer, followed by Globigerinita glutinata. Bolivina variabilis dominates the floating
benthic assemblage, while Tretomphalus bulloides, Trifarina bella and Cibicidoides pachyderma are common (Table 2).
The standing stock of the planktic foraminiferal assemblage varied highly
from 0.2 to 131.6 ind. m-3 in single net hauls (Fig. 4). In 2012, the
highest standing stock was observed on 22 October. On 29 October, the standing stock was markedly lower in the upper sampling
interval (0–60 m) and rose again thereafter (Fig. 4). Station 3 was sampled
on 29 October and 2 November only. This station is on the
shelf (Fig. 1) and showed the lowest standing stocks (0.59 and 3.15 ind. m-3, respectively) of all net samples. The abundance of benthic
foraminifers varied from 0.3 to ∼21 ind. m-3 in single
net hauls (Fig. 4). A shift to a higher abundance of benthic specimens was
observed concomitant with a decline of planktic foraminifers on the 29 October at stations 1 and 2 in the upper sampling interval. Even though
the species composition did not show any significant differences between
sampling days in 2012 (paired sample t tests, p>0.05), different
Bray–Curtis similarity indices can be observed across sampling days (Fig. 5, the Supplement, Table S4). The samples from 2 and 5 November have shown the highest similarity (0.81). The sample from
22 October showed a lower similarity, and the sample from the
29 October was most different (0.36) from the assemblages on the other
sampling days in 2012. The sampling season (autumn or spring) and the
sampling year (1994/1995 or 2012) showed a significant relationship (p=0.001) with the observed changes in the foraminiferal assemblage (Fig. 6a).
While the analyses imply that a spring assemblage and an autumn assemblage
of planktic foraminifers can be clearly distinguished, it also indicates a
long-term assemblage change. From autumn 1994 to 2012 we observe a decrease
in the relative abundance of G. ruber (white) and an increase in the relative
abundance of T. sacculifer (Fig. 6, Table 2).
Foraminiferal abundance (individuals per m3 seawater) at
station 1 (a) and station 2 (b) of the upper (0–60 m; light grey bars) and
deeper (60–100 m; dark grey bars) sampling intervals in 2012. Hurricane
Sandy is marked by dashed red arrows.
Hierarchical cluster analysis showing the similarity of
foraminiferal assemblages from station 1 and station 2 between different
sampling days (day/month) in 2012. Cluster analysis was performed using the
unweighted pair group method with arithmetic mean (UPGMA) based on the
Bray–Curtis similarity index (values from 0 to 1; 1 indicates the highest
similarity between the faunas).
Comparison of planktic foraminiferal assemblages between spring (1995) and autumn (1994, 2012). (a) Optimal NMDS ordination (Wisconsin
double-standardized relative abundances, Bray–Curtis similarity index) of
planktic foraminifers during spring (green) and autumn (brown) 1994/1995
(Schmuker, 2000b), and autumn 2012 (this study). Ellipses indicate standard
deviation of assemblages around the centroid of the groups. (b) Average
assemblage composition of planktic foraminifers at stations 1 and 2 in 2012.
Percentages were calculated from the total living planktic assemblage of the
sampling intervals 0–60 and 60–100 m water depths. (c) Average assemblage
composition of planktic foraminifers from autumn 1994 and spring 1995, mesh
size >150µm (Schmuker, 2000b).
Depth distribution pattern of foraminifers
In order to test whether habitat depths of different species depend on the
water masses, two depth intervals (0–60 and 60–100 m) were sampled at
stations 1 and 2 in 2012. The highest average standing stock of living
planktic foraminifers was found in the upper interval (Fig. 4). Differences
in the assemblage composition between the upper and the lower interval were
limited to rare species (Fig. 6b). Station 1 had a slightly higher standing
stock in the upper interval than station 2, although both stations showed a
profound abundance fluctuation during the sampling time. This variability
was not recognized in the deeper intervals (Fig. 4). In the upper part of
the water column, G. ruber (pink), T. sacculifer, and G. glutinata dominated the assemblages (Fig. 6b). Among
the common species, G. ruber (white) and Globoturborotalitarubescens showed the highest abundance in the upper
interval too. Higher abundances in the deeper interval are observed for
Globorotalia menardii, Globigerinella calida, Globigerinella siphonifera, and Orbulina universa (Figs. 4, 6b).
The highest abundance of benthic species was recorded at station 2 on the
first sampling day in the lower depth interval (60–100 m, Fig. 4), mainly
due to a high number of Trifarina bella. On the 29 October, higher abundances of
benthic foraminifers were found in the upper interval at both stations. This
was mainly caused by the exceptionally high abundance of B. variabilis (Fig. 4). On the
2 and 5 November 2012, the upper interval at station 2 also
had a high standing stock of B. variabilis. Station 1 yielded benthic specimens on the
29 October and 2 November only. Rare Bolivina species,
Asterigerina carinata and Cornuspira involvens, were collected on the 29 October. Cibicidoides pachyderma was found in several net
samples and showed no distinctive pattern over time or space.
Analyses of size and weight of Trilobatus sacculifer
Size and weight changes of T. sacculifer individuals were investigated along the sampling
period of 2 weeks. A slight increase in size of 125 µm of the
individuals was recognized within the 2 weeks (Fig. 7a, b). This change
in shell length over time is statistically significant as shown by the GLM
(Table 3). The size difference between the individuals of stations 1 and 2
is statistically not significant (Table 3), indicating that the sampling was
representative for the waters south of Puerto Rico. Individuals occurring
above 60 m water depth were smaller than specimens from below 60 m water
depth. Although a size difference between the two depth intervals is
statistically significant, the interaction term of sampling date and depth
showed no significant influence on the size of individuals of T. sacculifer (Table 3).
This means, that at each date sampled we found a majority of big, mature
individuals in the deep sampling interval, but there was no migration of
these individuals in the water column throughout our sampling period.
Size and area density changes of Trilobatus sacculifer in autumn 2012. The data are
log-transformed (a, b) across the sampling period in 2012 at stations 1 and
2 and different depth intervals. A full moon occurred on the second sampling day,
29 October 2012. Hurricane Sandy passed the Greater Antilles
in late October 2012. (a) Logarithmic sizes of T. sacculifer (red symbols indicate
individuals with a sac-like chamber, and blue symbols indicate individuals
without a sac-like chamber) at two different stations (1 and 2), pooled over
the complete depth range from 0 to 100 m. Black lines show kernel density
distributions of sizes at station 1 (solid) and station 2 (dashed). (b) Logarithmic sizes of T. sacculifer (red symbols indicate individuals with a sac-like
chamber and blue symbols indicate individuals without a sac-like chamber) at
two different depth intervals, pooled over stations 1 and 2. Black lines
show kernel density distributions for depth of 0–60 m (solid) and depth
60–100 m (dashed). (c) Area density (AD) of T. sacculifer (with sac-like chamber) along the
sampling period sampled at two different depth intervals, pooled over
stations 1 and 2. Black lines show kernel density distributions of weights
at a depth of 0–60 m (solid) and at a depth of 60–100 m (dashed). (d) Comparison of AD between T. sacculifer with sac-like chamber and without sac-like chamber.
Grey bars depict the mean AD including 95 % confidence interval as error
bars.
Results of the generalized linear model (link function: identity,
gamma distribution) approach to analyze the statistical significance of size
changes of Trilobatus sacculifer (n=655) as a function of station (replicate), sampling date,
sampling depth, and the interaction between sampling date and sampling
depth.
SourceType III linear regression Wald chi-square testdfSig.(Intercept)51 719.4481<0.001Sampling station0.80310.344Sampling date42.4903<0.001Sampling depth6.72310.004date * depth2.07230.393
Regarding the weight measurements, we observed a trend with heavier (higher
AD) individuals in the deep sampling interval (Fig. 7c, Table 4), but a change
of weight over time is not significant in a GLM (Table 4). This is
corroborated by the χ2 test of association, which showed no
significant change in the frequency of light and heavy specimens over the
investigated time interval (χ2=1.031, df=2, p=0.597).
The interaction term of sampling date and depth showed no significant
influence on the weight of specimens of T. sacculifer. Yet, we found fewer individuals of
T. sacculifer with a sac-like last chamber at the first two sampling days than at the
later dates, a fact that might influence the accuracy of the results. There
is no detectable correlation between the GLM's predicted values and their
residuals (p=0.859), indicating an effective detrending of the data.
Individuals of T. sacculifer without a sac-like last chamber (trilobus-morphotype) are on average
lighter than individuals with the sac (Fig. 7d).
Results of the generalized linear model (link function: identity,
normal distribution) approach to analyze the statistical significance of
AD changes of Trilobatus sacculifer with a sac-like chamber (n= 27) as a function of station
(replicate), sampling date, sampling depth, and the interaction between
sampling date and sampling depth.
SourceType III linear regression Wald chi-square testdfSig.(Intercept)795.5531<0.001Sampling station0.02410.876Sampling date4.61820.099Sampling depth5.83010.016date * depth0.78410.376Stable isotopes of Globigerinoides ruber (pink) and ambient seawater
The stable oxygen isotopes (δ18OCALCITE) of G. ruber (pink)
averaged -2.54 ‰ and the stable carbon isotopes (δ13CCALCITE) averaged 0.49 ‰. Samples of the deeper
net (60–100 m water depth) yielded higher δ18OCALCITE
(-2.4 ‰) and higher δ13CCALCITE values (0.65 ‰) than samples of the upper water mass
(δ18O=-2.62 ‰; δ13C=0.38 ‰; Fig. 8). The lowest δ13CCALCITE values were measured in individuals collected on the
29 October 2012. Individuals sampled at station 3 showed the
lowest stable isotope values (-2.96 ‰ for δ18OCALCITE and -0.4 ‰ for δ13CCALCITE). The equilibrium value of the seawater (δ18OEQUILIBRIUM) averaged -2.13±0.07 ‰, indicating the predicted inorganic calcite value
precipitated in thermodynamic equilibrium with ambient seawater temperature
and δ18OSEAWATER (Fig. 8).
Stable oxygen and carbon isotope values of G. ruber (pink) and average
δ18OEQUILIBRIUM value of ambient surface water. Green and
blue dots indicate the average values of stations 1 and 2 from the four
sampling days and two sampling depth intervals in 2012 (this study). Stars
indicate the isotope data of Schmuker (2000b) from G. ruber (white) collected in
autumn 1994 and spring 1995. Orange dot: stable isotope value of individuals
collected at station 3 on the 29 October 2012 (this study).
Note: hurricane Sandy passed the Greater Antilles in late October 2012
resulting in high δ13CCALCITE values on 29 October in the mixed layer.
DiscussionSeasonal response and interannual variation of planktic foraminifers
Previous studies revealed that the distribution and community composition of
planktic foraminifers from the Caribbean Sea are generally influenced by
biological and environmental factors, as well as geographical settings
(e.g., Jones, 1968, 1971; Schmuker, 2000a; Schmuker and Schiebel, 2002;
Tedesco et al., 2009; Spear et al., 2011; Poore et al., 2013; Jentzen et
al., 2018b). Our planktic foraminiferal composition of Puerto Rico comprises
common surface dwellers for the study area and surrounding basins (e.g., T. sacculifer,
G. ruber (pink and white), G. glutinata; Jones, 1968; Bé et al., 1971; Schmuker and Schiebel,
2002; Tedesco and Thunell, 2003; Jentzen et al., 2018b). Furthermore, our
data from autumn 2012 show a similar species inventory as described in 1994
for the same area, and the autumn assemblage of our survey in 2012 is closer
to the autumn assemblage in 1994 of Schmuker (2000b) than to their spring
assemblage in 1995 (Fig. 6a, Table 2). In spring 1995, Globigerinella calida, Globigerinella siphonifera, Orbulina universa, Hastigerina pelagica, and Globorotalia truncatulinoides were common,
whereas the autumn assemblage in 1994 mainly comprised
Globigerinoides ruber (pink and white), Trilobatus sacculifer, Globorotalia menardii, Neogloboquadrina dutertrei, and Globigerinita glutinata (Fig. 6c). In our survey from autumn 2012,
T. sacculifer (∼40 % of the total planktic assemblage) and G. ruber (pink)
(∼37 %) were the dominant species. Species of the spring assemblage by Schmuker (2000b) were, with the exception of G. truncatulinoides, also found in the
samples from 2012, but they occurred in low numbers and mainly in the deeper
interval (Fig. 6b). Schmuker (2000b) sampled the upper 10 m of the water
column and from the surface to 120 m water in one haul, thus a change of the
habitat depths of the species during different seasons was not resolved.
Even though the capability of planktic foraminifers to perform fast,
diurnal vertical migrations or buoyancy changes are unlikely (Harbers, 2011;
Siccha et al., 2012; Meilland et al., 2019), we speculate about the
existence of a seasonal change in species-specific habitat depths, probably
facilitated by a variable seasonal hydrography and thermocline depth changes
(see Schmuker, 2000b; Rebotim et al., 2017). Our data from 2012 indicate
preferred habitats of certain species, although the dominant faunal
elements, G. ruber (pink) and T. sacculifer, were found in high numbers in the entire sampled
water column (up to 80 % together of the total planktic assemblage, Fig. 6b). Both species are common in tropical and subtropical oceans, and they
are frequent in the Caribbean Sea (Jones, 1968; Bé et al., 1971;
Schmuker and Schiebel, 2002; Jentzen et al., 2018b). The species G. ruber (pink) and
G. glutinata indicate a high nutrient supply (e.g., Bé and Tolderlund, 1971;
Schiebel et al., 2001; Retailleau et al., 2011). A high nutrient flux into
the Caribbean Sea during autumn is likely caused by the riverine plumes of
the Amazon and Orinoco rivers (Fig. 2b; Bidigare et al., 1993; Corredor and
Morell, 2001; Chérubin and Richardson, 2007).
Higher abundances of G. calida, G. siphonifera, N. dutertrei, and G. menardii in the deep sampling interval (Fig. 4) point
to a change in the character of the foraminiferal habitat below 60 m. The
species G. calida and G. siphonifera show variable depth habitats in the Atlantic and Caribbean Sea
and may live above, in, and below the pycnocline (Rebotim et al., 2017;
Jentzen et al., 2018b). Globigerinella calida is linked to oligotrophic conditions during spring
in the Caribbean Sea off Puerto Rico (Schmuker, 2000b), and is associated
with neritic conditions in the upwelling area of the Bay of Biscay
(Retailleau et al., 2012). Based on oxygen isotope (δ18O) data,
N. dutertrei and G. menardii are known to dwell in the seasonal pycnocline (Tedesco et al., 2007;
Steph et al., 2009); however, plankton tows from the Caribbean Sea
(foraminiferal census and δ18O data) indicate that juvenile
specimens live in the mixed layer before they sink to deeper waters and
continue calcifying (Jentzen et al., 2018a, b). Even though, in our plankton
tows in 2012, only small numbers of the abovementioned species were collected
(<5 ind. m-3; Fig. 4), the change in the composition of rare
species with preferred habitats in the pycnocline most likely indicates the
influence of the SUW, and thus a change of the food source and light
availability.
A slight but conspicuous change of the foraminiferal assemblage composition
took place between 1994 and 2012. In autumn 1994, G. ruber (white) had a
substantially higher percentage (37 %) than in 2012 (3.5 %), resulting
in a high G. ruber pink-to-white ratio of 10.3 in 2012, compared to a low ratio of
0.8 in 1994 (Fig. 6, Table 2). A decline of G. ruber (white) during the last decade
has previously been observed in the Caribbean Sea (Jentzen et al., 2018b)
and in the tropical Atlantic (Harbers, 2011). Furthermore, variable
abundances of G. ruber (white) were observed in sediment traps of the Gulf of
Mexico, with low numbers in 2008 and 2009 supporting the trend of a
decreasing abundance but also indicating a high variability (Poore et al.,
2013). Jentzen et al. (2018b) related the low numbers of G. ruber (white) and the
higher pink-to-white ratio (up to 6 in the eastern Caribbean Sea) to
increasing SSTs over the past decades and changes in nutrient flux and
primary production, rather than to seasonal variations or local, short-term,
and/or spatial variability (patchiness in time and space). Our data
collected south of Puerto Rico show higher SSTs in autumn 2012 compared to
the year 1994 (average increase of 1 ∘C). These data support the
contention that the observed faunal change in the foraminiferal assemblages
can be linked to increasing SST; nevertheless, patchiness and drifting of
planktic foraminifers can result in variable abundances of planktic
foraminifers in the water column (e.g., Siccha et al., 2012).
The influence of the shelf and benthic species
The near-shore station 3 showed distinctively low numbers of foraminifers
(average 1.69 ind. m-3). The difference of station 3 to the other
stations could partially be due to a different way of sampling (only in
±5 m water depth). However, low abundances of planktic foraminifers
close to the coast and in shallow waters have been observed before, e.g., in the Bay of Biscay (Retailleau et al., 2009) and in the Santaren
Channel between the Bahamas and Cuba (Jentzen et al., 2018b). In the Bay of
Biscay, freshwater input has been suggested as a factor influencing the
foraminiferal assemblage. In the Santaren Channel, the low abundance of
living planktic foraminifers has been suggested as consequence of the
prevailing neritic conditions at shallow water depths (>530 m),
which most likely inhibits the reproduction of planktic foraminifers and
chance of survival. The abundance of benthic foraminifers in the water
column in 2012 off Puerto Rico was lower than previously reported by
Fornshell (2005) from plankton hauls in the vicinity of reefs around Puerto
Rico. Nonetheless, the abundances were similar to numbers in autumn 1994 as
reported by Schmuker (2000b). In the benthic assemblage of 2012,
meroplanktic species (such as Tretomphalus bulloides) were common in the plankton nets. This
species builds a floating chamber in the late stage of its life cycle to
release gametes in the upper water column (Sliter, 1965; Rückert-Hilbig,
1983; see SEM image of the floating chamber in the Supplement, Fig. S4). A
high relative abundance of living individuals of the biserial Bolivina variabilis
(Streptochilus globigerus) was observed in the nets as well (Table 2). This species was found in
plankton tows from the Caribbean Sea and northern Atlantic (Hemleben et al.,
1989; Schmuker and Schiebel, 2002; Jentzen et al., 2018b), but it was either
absent or rare in near-shore surface sediments off southern Puerto Rico
(Brooks, 1973; Seiglie, 1975). Bolivina variabilis grows and calcifies in both a planktic and
benthic habitat (tychopelagic lifestyle) (Darling et al., 2009; Kučera
et al., 2017). Kučera et al. (2017) suggested that the tychopelagic mode
of life of Bolivina/Streptochilus mirrors the transition process from a benthic to a holoplanktic
lifestyle that has been performed several times during Earth's history.
After 29 October 2012, the abundance of B. variabilis increased and was
higher in the uppermost 60 m of the water column than at depths below (Fig. 4). It is conceivable that B. variabilis was swept into the water column by wave action
during the stormy weather conditions of hurricane Sandy. Thus, we assume
that this species thrived suspended in the upper water column, pursuing a
part of their planktic lifestyle during the days after the hurricane. The
empty tests of other benthic species (e.g., Trifarina bella) collected in the water column
have probably been eroded from the surface sediments or brought in
suspension, attached to seagrass, and were transported further offshore
(Loose, 1970; Murray, 1987; Schmuker, 2000b; Fornshell, 2005).
Lunar reproductive cycle
Our dataset facilitated the investigation of synchronized size changes of
T. sacculifer through time, which could indicate reproduction cycles. Trilobatus sacculifer was reported to
have a lunar reproduction cycle, based on observations from plankton net
samples (Almogi-Labin, 1984; Bijma et al., 1990; Erez et al., 1991; Jentzen
et al., 2018b). The individuals reproduced preferentially at full moon and
underwent a migration from the surface to deeper waters, near the seasonal
thermocline (e.g., Erez et al., 1991). The formation of a sac-like final
chamber, which is diagnostic for T. sacculifer, was described to be associated with the
onset of reproduction. The release of gametes will take place around 24–48 h after the sac-like chamber formation (Bé, 1980). Yet, other factors
such as environmental stress (e.g., by salinity changes) can influence the
morphology of T. sacculifer as well (Weinkauf et al., 2019). Nevertheless, we expected
that the number of individuals of T. sacculifer with a sac-like chamber should be highest
before full moon and drop significantly afterwards, as observed in the Red
Sea (Erez et al., 1991). In contrast to these observations, we found most
individuals with a sac-like chamber at the third day after full moon and
hardly any before (Fig. 7c). Test sizes in T. sacculifer appeared to have increased with
time, which by itself is indicative of the existence of a growth cohort
(Fig. 7a, b). Yet, the size does not peak at full moon, the population
continues to grow and thicken for 7 d after the full moon, although
the change was not significant. Therefore, the size increase of T. sacculifer over time
did not seem to be related to reproduction synchronized with the full moon.
Our data also do not support evidence for migration of T. sacculifer in the water column
throughout its reproductive cycle. Both size data and weight data show the
biggest individuals dwelling in the deeper sampling interval independent of
the sampling day (Fig. 7b, c). The comparison of the area density of T. sacculifer
confirms that the development of the sac-like chamber is associated with
heavier calcification, probably indicating gametogenic calcification (e.g.,
Bé, 1980), and such individuals might be close to reproduction (Fig. 7d).
Stable oxygen isotope signal
In the upper water column, stable oxygen isotope values of G. ruber (pink) show an
offset of -0.46 ‰ to the equilibrium values of
ambient seawater (Fig. 8). As the species G. ruber (pink) hosts symbionts, this
offset possibly indicates photosymbiont activity (e.g., Kahn, 1979; Erez and
Honjo, 1981). Symbiont activity lowers the stable oxygen isotope composition
of calcite tests (Spero and Lea, 1993) and high negative disequilibrium
values (up to -0.35 ‰) in symbiont-bearing species
(e.g., O. universa and T. sacculifer) were observed before in living foraminifers in the Caribbean
Sea (Jentzen et al., 2018a). Off the coast of Puerto Rico, δ18OCALCITE values from autumn 1994 (Schmuker, 2000b) of
G. ruber (white) yield the same average values as G. ruber (pink) in 2012 (-2.5 ‰) and are lower than in spring 1995. Based on the
sediment trap study of Richey et al. (2019), no discernable difference can
be determined in δ18OCALCITE between the chromotypes G. ruber
(white) and (pink) from individuals co-occurring in the Gulf of Mexico. For
this reason, we assume that the seasonal isotope signal overprints any
species-specific bias of the two chromotypes, which thus can be compared to
each other. Applying the δ18O paleotemperature equations for
G. ruber (pink) of Farmer et al. (2007; 4.86 ∘C ‰-1,
calibration error (standard deviation σ) of 0.24 ‰), specimens of the upper 60 m of the water column in
2012 yield average δ18O temperatures of ∼29.5∘C, which are in the range of the average measured in situ
temperatures of ∼29.2∘C. Below 60 m water depth,
the living individuals yield on average higher δ18OCALCITE values (+0.17 ‰), which likely depict the
properties of the SUW (lower temperature and higher salinity than shallower
waters), and thus corroborates that G. ruber (pink) calcifies over a broad depth
range within the upper water column (i.e., 0–100 m; Fig. 8).
Hurricane Sandy
Hurricane Sandy, which passed the Greater Antilles on 24 October 2012, induced higher waves and precipitation at the sampling site off
Puerto Rico (Fig. 3), and thereby most likely affected the foraminiferal
assemblage. After hurricane Sandy, the planktic foraminiferal abundance in the
upper water column was much lower on 29 October when next sampled and
at the same time, a higher number of living benthic species (B. variabilis) was found
(Fig. 4). Other factors such as patchiness and drifting of living planktic
foraminifers can vary the abundance in the water column as well (e.g.,
Siccha et al., 2012). However, Schiebel et al. (1995) have described the
influence of two storms with wind speeds up to 12 on the Beaufort scale on living
planktic foraminiferal assemblages in the North East Atlantic Ocean. They
affected the mixed layer and the total abundance of small specimens was
higher afterwards. The storm events raised the nutrient and chlorophyll
concentrations in the mixed layer and thereby pushed the reproduction. An
elevated chlorophyll concentration after hurricanes was reported from the
Sargasso Sea (Babin et al., 2004) and from Puerto Rico after hurricane
Georges in 1998 (Gilbes et al., 2001). A higher chlorophyll
concentration was measured 3 d after hurricane Georges had
crossed the island. Additionally, a higher rainfall and river runoff with
terrestrial load was observed, which affected neritic environments after the
storm. Even though, the measured wind speed was low on Puerto Rico in late
October 2012 compared to the hurricane in 1998, intense precipitation and
extensive flooding were recorded during the passage of hurricane Sandy
(Fig. 3; Blake et al., 2013). A higher nutrient input in combination with
terrestrial runoff might have contributed to a higher turbidity in the water
column close to the coast and most likely to a lower δ13CDIC signature in the seawater (Ravelo and Hillaire-Marcel,
2007; Zhao et al., 2015). If this was the case, the living conditions
changed for a short time and may have affected the planktic assemblage
observed within this study. On the 29 October, low δ13CCALCITE values of G. ruber (pink), collected in the upper water
column and at station 3, probably recorded the storm event (Fig. 8).
Symbiont photosynthetic activity can strongly influence the incorporation of
δ13C in foraminiferal tests (Spero and DeNiro, 1987; Spero and
Williams, 1988; Spero and Lea, 1993). The studies showed that during lower
light irradiance, foraminiferal calcite is depleted in δ13CCALCITE, as observed in our study. Lin et al. (2004, 2011) indicated depleted δ13CCALCITE in
foraminiferal tests in relation to high nutrient concentrations and supply
of 12C-rich water in the South China Sea. Based on those observations
we conclude that the vicinity of the coast has influenced the station on the
shelf break. The data support the assumption of a higher terrestrial runoff
and higher turbidity after the hurricane, which may have caused lower
irradiance light levels, reduced photosymbiont activity, and lower δ13CDIC of the seawater, hence lowered δ13CCALCITE values in the mixed layer.
Summary and conclusion
Depth-stratified replicated plankton net sampling off Puerto Rico in autumn 2012, revisiting three stations previously sampled in autumn 1994 and spring 1995, denotes that the foraminiferal assemblage in autumn 2012 was largely
similar to the autumn assemblage in 1994, although a decline of G. ruber (white) in
2012 was observed off the coast of Puerto Rico. This decline might indicate
a change of environmental factors such as increasing SST during the last
decades. Below 60 m water depth, the assemblage composition was different
than at the surface, the first specimens of deep-dwelling species emerged
and δ18OCALCITE values indicate the influence of the
SUW. Test size and weight measurements of T. sacculifer indicate no synchronization of
the reproduction linked to the lunar cycle; nonetheless, T. sacculifer were continuously
growing during the sampling time. Hurricane Sandy passed the Greater
Antilles during the sampling period in 2012 and affected the planktic
foraminiferal assemblage. The storm most likely triggered a decrease in the
standing stock and depleted δ13CCALCITE values in the
upper water column as a result of a higher turbidity and terrestrial runoff
after the storm and the vicinity of the coast. The exact mechanism by which
stormy weather and heavy rainfall may affect the foraminiferal assemblage is
beyond the scope of the present study; nonetheless, it should be considered
that such tropical cyclones may perturb the plankton assemblage, and hence
make it even more difficult to decipher the factors controlling living
planktic foraminifers on a small spatiotemporal scale.
Data availability
The dataset of this article can be found in the
Supplement and in Schmuker (2000b).
The supplement related to this article is available online at: https://doi.org/10.5194/jm-38-231-2019-supplement.
Author contributions
AJ, AKMW, JS, MK, and MFGW collected the samples
and processed the data. AJ, AKMW, JS, MK, and MFGW drafted the article and all
authors critically revised it. The final version was approved by all
authors.
Competing interests
The authors declare that they have no conflict of interest.
Acknowledgements
Amos Winter (University of Puerto Rico) and
colleagues and boat crews at the Isla Magueyes Marine Laboratories (Puerto
Rico) are gratefully acknowledged for the help offshore and providing lab
facilities during the sampling campaign in 2012. We thank Fynn Wulf (GEOMAR)
for stable isotope measurements on foraminiferal calcite and Hydroisotop
GmbH for stable isotope analyses of the seawater samples. We acknowledge
Sebastian Meier and Birgit Mohr (University of Kiel) for the help with
scanning electron microscope photographs of our foraminifers and Birgit Lübben and Nele Vollmar (MARUM, Bremen) for their help with size and
weight measurements. We gratefully thank Kirsty Edgar for
handling the manuscript and two anonymous reviewers for their constructive
comments which helped to improve our article.
Financial support
This research has been supported by the German Research Foundation
DFG (grant SCHO605/8-1 and KU2259/19). The article processing charges for this open-access publication were covered by a Research Centre of the Helmholtz Association.
Review statement
This paper was edited by Kirsty Edgar and reviewed by two anonymous referees.
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