Oligotrophic regions represent up to 75 % of Earth's open-ocean
environments. They are thus areas of major importance in understanding the
plankton community dynamics and biogeochemical fluxes. Here we present
fluxes of total planktonic foraminifera and 11 planktonic foraminifer
species measured at the Oceanic Flux Program (OFP) time series site in the
oligotrophic Sargasso Sea, subtropical western North Atlantic Ocean.
Foraminifera flux was measured at 1500 m water depth, over two
Planktonic foraminifera (PF) comprise 23–56 % of the total open marine calcite flux and thus exert an important control on global carbon cycling (Schiebel, 2002). They are used extensively in palaeoceanographic and palaeoclimatic reconstructions via utilisation of their species abundance and assemblage composition (e.g. Lutz, 2011; Sexton and Norris, 2011), geochemical signatures (e.g. Zeebe et al., 2008), shell mass (e.g. Barker and Elderfield, 2002) and in evolutionary and biogeographic studies (e.g. Sexton and Norris, 2008). However, gaps remain in our understanding of the controls on their spatial and temporal distribution in the upper water column. Following the early 1980s when sea surface temperatures (SSTs) were thought to dominantly control PF distributions and abundance (CLIMAP project members, 1994), a number of other environmental parameters have also been shown to exert influence on the distribution and abundance of PF, such as salinity (Kuroyanagi and Kawahata, 2004), productivity, nutrient availability (Schiebel, 2002; Northcote and Neil, 2005; Žarić et al., 2005; Storz et al., 2009; Sexton and Norris, 2011) and water column stability (Hemleben et al., 1989; Lohmann and Schweitzer, 1990; King and Howard, 2003). It is thus imperative to better understand the environmental factors controlling modern-day PF abundance in order to produce accurate interpretations of palaeorecords based on PF assemblages.
The response of PF flux and species composition to environmental and/or oceanographic factors have been studied using plankton tow materials which can give information about living populations' species distribution and depth habitats within the upper ocean (Tolderlund and Be; 1971, Fairbanks et al., 1980; Schiebel, 2002). However, temporal resolution is often limited when using plankton tows. The continuous time series records provided by sediment traps allow a more complete understanding of the seasonal and interannual changes in PF flux and can aid in integrating living assemblages with the sedimentary record.
Earlier studies of planktonic foraminifer flux off Bermuda at the Seasonal
Changes in Foraminifera Flux (SCIFF) site (Fig. 1) (Deuser et al., 1981;
Hemleben et al., 1985; Deuser, 1987; Deuser and Ross, 1989) were based on a
bi-monthly sampling interval and provide a general description of
foraminifera flux, species composition and seasonality. These studies found
that PF > 125
Map to show locations of the Oceanic Flux Program (OFP)
mooring (31
The Sargasso Sea is located within the North Atlantic gyre, which is
characterised by high temperatures and salinities, and weak, variable
surface currents (Lomas et al., 2013, and references therein). The OFP and
BATS sites are situated in a transition region between the northern
eutrophic waters and the relatively oligotrophic subtropical convergence
zone in the south (Steinberg et al., 2001, and references therein).
Subtropical Mode Water (STMW) forms on the fringes, north of the gyre, owing
to convective deep winter mixing and entrainment of nutrients and is
characterized by temperatures of 17.8–18.4
The hydrography and biogeochemistry of the area have been summarised by
Michaels and Knap (1996), Steinberg et al. (2001), Lomas et al. (2013) and
references therein. In the absence of large changes in salinity, the 10
The OFP mooring is located at 31
On average,
The BATS site (31
The seasonal cycle and interannual variability of the PF flux at
1500 m depth is highly correlated with that of the total mass, carbonate and
organic carbon fluxes. All fluxes are strongly characterized by an abrupt
spring maximum during February–April, which varies significantly on an
interannual basis (Fig. 2). For example, the spring PF flux peak ranged
from a low of 400 tests m
Temporal changes in total planktonic foraminifera flux and mass, carbonate, and organic carbon fluxes at 1500 m depth over the 6-year study period.
In Fig. 3 we compare interannual variations in bi-weekly resolved total PF
flux to
Sea level anomaly (SLA) provides information about eddies passing through the area (Fig. 3b). A negative anomaly is associated with cyclonic eddies and a positive anomaly associated with anticyclonic and mode water eddies. The SLA data show that the particularly high and prolonged PF fluxes, total mass flux and organic carbon flux in spring 2009 and 2010 coincided with the passage of cold, cyclonic eddies (Fig. 2), which enhance nutrient upwelling into the euphotic zone.
The annual and interannual PF flux is in phase with the deepening and
shoaling of the mixed layer depth (MLD) (Fig. 3c) and with chlorophyll
Temporal changes in environmental parameters measured at the
BATS site in relation to total planktonic foraminiferal flux in the 1500 m OFP
trap (thin, black line):
In general, all planktonic foraminifera, and especially deeper-dwelling
species, show strong, consistent seasonal variance (Figs. 5–7). Our
results demonstrate a clear depth progression towards more pronounced
seasonality in the deeper species, compared to a larger intra-seasonal
variability in the surface and intermediate dwellers. In addition, the deep-dwelling PF species exhibit repeatable species successions throughout the
winter and early spring (Fig. 8, Table 1). Figure 8 shows that
Correlation between total planktonic foraminifera flux in
the 1500 m OFP trap (thin, black line) with environmental parameters
measured at the BATS site.
The controls on PF flux in the Sargasso Sea was first introduced by Bé (1960) and later developed by Tolderlund and Bé (1971), who suggested that PF flux is dominantly controlled by the availability of their food phytoplankton. Thus, the environmental factors controlling PF flux should be closely aligned with the factors controlling phytoplankton productivity and export flux.
Temporal changes in surface-dwelling planktonic foraminifera fluxes in the 1500 m trap with changes in sea surface temperature (0–25 m) shown in the dashed black line for reference. The approximate depth habitat (Anand et al., 2003) is shown in figures.
Annual fluxes for planktonic foraminifera species at 1500 m depth
in 1998–1999, 1999–2000, 2008–2009 and 2009–2010 and the 4-year averages.
Fluxes were calculated from the sum of bi-weekly averages between July and June
for each year and converted to tests m
Previous studies suggest that increased chlorophyll concentrations and
larger phytoplankton abundances occur when the MLD deepens (Townsend et al., 1994; Waniek, 2003; Nelson et al., 2004) and the amplitude and timing of MLD
deepening determines the size of the following spring bloom (Menzel and
Ryther, 1961; Michaels et al., 1994). Here, we also observe a simultaneous
seasonal peak in chlorophyll
The majority of the increased PF flux in the winter–spring is driven by
increased fluxes of deeper-dwelling species, in particular
The correlation observed here between the seasonality in the PF flux,
chlorophyll
Temporal changes in intermediate-dwelling planktonic foraminifera fluxes in the 1500 m trap with changes in sea surface temperature (0–25 m) for reference. The approximate depth habitat (Anand et al., 2003) is shown in figures.
In contrast, the surface-dwelling symbiont-bearing foraminifera have lifecycles which strongly benefit from stratified surface waters and shallow mixed layers in order to photosynthesise – allowing them to succeed in low-nutrient conditions (Hemleben et al., 1989). Surface dwellers generally calcify in late summer when sea surface temperatures are at a maximum and dinoflagellates are abundant (Tolderlund and Bé, 1971). We thus conclude that the depth and structure of the mixed layer plays an important role in regulating PF species flux by controlling the abundance and timing of their food availability throughout the seasonal cycle.
Current models based on the light-limited higher latitudes (Waniek, 2003;
Mao, Y., personal communication, 2013), suggest that if the MLD shoals early
and slowly, the consequent bloom will be long and weak compared to if the
MLD shoals late and quickly, which causes a short and sharp bloom. At our
subtropical study site, the spring bloom is predominantly limited by
nutrient input into the euphotic zone, which is determined by the depth of
the mixed layer. Increased heat loss and wind stress leading to higher
convective mixing during the winter months controls the rate of deepening of
the mixed layer, which is strongly correlated to the maximum MLD reached
(
To test whether the rates of mixed layer deepening in early winter and of
shoaling in spring affect the PF flux, we computed a mixed layer dynamics
index,
Temporal changes in deeper-dwelling planktonic foraminifera fluxes in the 1500 m trap with changes in sea surface temperature (0–25 m) for reference. The approximate depth habitat (Anand et al., 2003) is shown in figures. Graphs are ordered according to seasonal succession.
Mixed layer depth and mean rates of mixed layer (ML) deepening and
shoaling. The
Seasonal succession for deeper-dwelling species averaged
over six spring blooms (1998, 1999, 2000, 2008, 2009, 2010) from the 1500 m
trap.
Years where the shoaling rate is twice as quick as the deepening rate (e.g.
winters 1997, 2008, and 2009) have average
The negative sea level anomalies in spring of 2009 and 2010 indicate that
the large (and in 2010 prolonged) PF fluxes in these years were clearly
associated with the passage of cyclonic eddies (Fig. 3b). Eddy pumping of
nitrate into the euphotic zone has been shown to significantly increase new
production (Oschlies and Garçon, 1998; Oschlies, 2002). Cianca et al. (2007) estimate that eddy pumping contributes
In fact, the largest PF flux
observed over the entire record was associated with this eddy passage, even
though the maximum MLD and
This observation is consistent with an exceptionally large increase in the
flux of
Along with the timing of the eddy passage, our observations also suggest
that the PF flux response is dependent on whether the eddy is intensifying
or weakening. For instance, both cyclonic eddies in 2009 and 2010
intensified over the spring bloom (Fig. 3b) eliciting a large biological
response indicated by elevated subsurface Chl
Annual integrated PF flux from this study (1500 m trap,
square symbols) and 1979–1984 (*3200 m trap, round symbols, Deuser, 1987;
Deuser and Ross, 1989) plotted against wintertime (DJFM) NAO index
Recent studies have found that eddies which are a minimum of 1–2 months in duration are more likely to induce a larger biological response (Mouriño-Carballido and McGillicuddy, 2006, Sweeny et al., 2003). Our observations also suggest that eddies need to be present for at least a month to elicit responses in the flux of PF which have minimum lifecycles of 2 weeks. For instance, in winter 1998–1999 a cyclonic eddy passed over the sediment trap site in only 1 month and elicited no biological response, compared to cyclonic eddies in 2009 and 2010, which both remained over the site for a minimum of 2–3 months and elicited large biological responses (Fig. 3b). These findings suggest that cyclonic eddies which intensify over the spring bloom and last for 1–3 months can elicit a significant biological response and increased PF flux.
Our results show that environmental factors and mesoscale eddy variability play an important role in regulating the planktonic foraminifera fluxes, by regulating the MLD and consequent magnitude of the spring bloom and biological export flux.
An overarching climatological variable affecting this region especially is
the North Atlantic Oscillation (NAO), which exerts a strong influence on air
temperature, storminess, heat loss, winter mixed layer depth, and,
therefore, nutrient injection into the upper ocean during the winter months
(Bates, 2012; Bates and Hansell, 2004; Rodwell et al., 1999). Modelling
studies have shown that when the NAO is in its low phase, i.e. negative NAO
(e.g. winter 2010), there is increased heat loss that intensifies convective
mixing and results in enhanced nutrient upwelling into the euphotic zone to
support primary production (Oschlies, 2001). The NAO influence on upper
ocean productivity and biogeochemical fluxes is demonstrated by the inverse
correlation between the wintertime (NDJF) NAO index and the deep particulate
nitrogen flux in the OFP traps over a 30-year period (Conte and Weber,
2014) and increased primary productivity in negative wintertime NAO phases
(Lomas et al., 2010). If convective mixing and nutrient entrainment into the
euphotic zone is stronger during negative NAO years, this could serve to
modulate PF flux, and therefore carbonate flux, on decadal timescales. When
we compare PF fluxes covering a range of NAO indexes, from this study using
the 1500 m trap to the 3200 m trap between 1978 and 1984 (Deuser and Ross, 1989;
Deuser, 1987), we find a weak inverse correlation between total PF flux and
(DJFM) NAO index in-phase (not significant), but we do find a significant
inverse correlation with a (DJFM) NAO with a 1-year lag (
This study shows that the productivity of the dominant deep-dwelling species
Our study demonstrates that the interannual variability in planktonic
foraminifera flux can be linked to the MLD and the rate of
deepening/shoaling of the mixed layer associated with nutrient injection
into the euphotic zone. We find that higher PF fluxes coincide with deeper
MLDs, especially when combined with cyclonic eddy-induced nutrient
upwelling. In particular, the production of the dominant deep-dwelling
species
We would like to thank two anonymous reviewers for their time and constructive comments that helped improve the manuscript. This research was funded through the U.K. Ocean Acidification Research Program by Natural Environment Research Council grant to P. Anand and P. Sexton (grant NE/I019891/1). We acknowledge the National Science Foundation for its support of the Oceanic Flux Program time series (most recently by grant OCE-1234292) and the Bermuda Atlantic Time Series (most recently by grant OCE-0801991). We thank Mike Lomas for providing MLD data and Yolanda Mao for providing insights and useful discussion on the data. P. Anand is also thankful to Werner Deuser for communication regarding published data. Edited by: J. Bijma