Coccolithophores are calcifying phytoplankton and major contributors
to both the organic and inorganic oceanic carbon pumps. Their export
fluxes, species composition, and seasonal patterns were determined in
two sediment trap moorings (M4 at 12
The two trap locations showed a similar seasonal pattern in total
coccolith export fluxes and a predominantly tropical coccolithophore
settling assemblage. Species fluxes were dominated throughout the
year by lower photic zone (LPZ) taxa (
The centres of subtropical gyres and tropical open-ocean regions are marked
by nearly permanently stratified waters, which result in nutrient depletion
at the surface and low primary production, particularly at the surface during
most of the year (see Mann and Lazier, 2006). With the exception of
equatorial upwelling areas where the renewal of nutrients in the mixed layer
results from the upward advection of nutrient-rich deeper water, algal blooms
in subtropical gyres and tropical oceans are highly dependent on the seasonal
dynamics of the mixed layer depth, the latter changing as a geostrophic
response to the wind field and the curl of the wind stress (e.g. Longhurst
et al., 1995). Basin-scale thermocline tilting, mesoscale eddies, and
vertical mixing due to wind forcing and winter cooling are recognized as the
main mechanisms responsible for bringing nutrients to the upper photic layer
and promoting algal blooms in tropical and subtropical areas (e.g. Longhurst,
1993; Dufois et al., 2016). In addition, millions of tons of Saharan dust
blown over and into the Atlantic Ocean every year are also thought to act as
major nutrient suppliers to the nutrient-depleted equatorial North Atlantic
(see Goudie and Middleton, 2001 and refs. therein; Okin et al., 2011). The
fertilizing potential of Saharan dust is supported by previous studies in the
Amazon Basin (Mahowald et al., 2008, 2009; Bristow et al., 2010), the Gulf of
Mexico and the coast of southern Florida (Walsh et al., 2006; Lenes et al.,
2012), and the North Atlantic subtropical gyre (Pabortsava et al., 2017). In
addition to Saharan dust inputs,
Despite relatively low primary production rates, tropical oceans play an important role in the global carbon cycle because of their large surface area (e.g. Wang et al., 2013; Signorini and McClain, 2012; Longhurst, 1993). How these oceanographic and atmospheric processes are linked to phytoplankton productivity on seasonal to annual timescales in the tropics, however, remains poorly understood. As longer-term phytoplankton sampling in the vast and remote open ocean is rather costly, most of the available studies are based on data from snapshots taken during research cruises or remote-sensing estimates that only cover the phytoplankton biomass at the surface of the photic layer. Time-series sediment traps collecting settling particles (organic and inorganic) from phytoplankton export productivity over longer periods of time (from weeks to years) offer a good alternative to plankton studies for assessing the seasonal variation of marine phytoplankton and the relative proportion of individual species or groups of species in the open ocean (e.g. Milliman, 1993; Baumann et al., 2005).
Coccolithophores, being at the same time photosynthetic and
calcifying, are major contributors to the organic and inorganic
oceanic carbon pumps (e.g. Rost and Riebesell, 2004). Due to their
ability to cover their cells with tiny calcite plates (the
coccoliths), coccolithophores can be studied in time series samples
collected by deep-ocean sediment traps (e.g. Broerse et al., 2000;
Sprengel et al., 2002; Ziveri et al., 1995; Köbrich et al., 2015),
thus providing insight into the seasonal to inter-annual dynamics of
open-ocean phytoplankton. Coccolithophores are amongst the most
important phytoplankton groups within open-ocean,
stratified oligotrophic waters (e.g. Winter et al., 1994), hence
displaying features more typical of
Although a significant amount of sediment trap data on
coccolithophores fluxes exists for the open ocean (e.g. Knappertsbusch
and Brummer, 1995; Broerse et al., 2000) and for regions near
continental margins and islands (Beaufort and Heussner, 2001; Romero
et al., 2002; Köbrich et al., 2015; Sprengel et al., 2002) at
subtropical and temperate latitudes in the Atlantic, there is no
information available on the export and seasonal patterns of
coccolithophores in the equatorial Atlantic region. Previous studies
by Kinkel et al. (2000) and Winter et al. (2002) focusing on the
living coccolithophore communities in the tropical Atlantic have
reported
Here, we present new data on the coccolithophore export fluxes, seasonal patterns, and species composition from the open equatorial North Atlantic to investigate the environmental factors triggering phytoplankton productivity, including Saharan dust deposition and the discharge and eastward dispersion of the Amazon River water. To assess the spatio-temporal variability of these processes, we (a) compare results from two sediment trap moorings, M2 and M4, located in the central and western parts of the equatorial North Atlantic, respectively, and (b) relate coccolithophore data with environmental time series data obtained from satellite remote sensing for the sediment trap sampling period and with particle flux data collected from the same sediment traps and recently published by Korte et al. (2017).
Location of the trap mooring sites M4 and M2 and a schematic
representation of
Surface water circulation in the study area, involving tropical
surface water (TSW) and the South Atlantic Central Water (SACW), is
mostly driven by the north-easterly trade winds responsible for
generating the westward-flowing North Equatorial Current (NEC) between
approximately 10 and 20
The western equatorial North Atlantic where station M4 was located is
also seasonally influenced by the Amazon River, the world's largest
river with respect to freshwater discharge into the open ocean (Mann
and Lanzier, 2006). From August to December, when the retroflection of
the NBC carries the river plume eastward in the uppermost
The upper water masses in the study area, including the mixed layer,
consist mostly of the warm, salty, and nutrient-depleted TSW in the
upper
Two sediment traps at sites M2 (14
Background information regarding the DUSTTRAFFIC sediment trap moorings (M4 and M2) used in this study.
Sediment trap samples from stations M4 and M2 were initially
wet-sieved over a 1
The taxonomic identification of coccolithophore species followed Jordan
et al. (2004) and Young et al. (2011). Coccolith species counts were
converted into coccolith export fluxes
(i.e. coccoliths
Shallowing or deepening of the nutricline was inferred from the ratio
between upper photic zone (UPZ) species and lower photic zone (LPZ)
species, with larger ratios (i.e. higher abundance of UPZ taxa)
indicating shallower depths of the nutricline. The ratio was
calculated as the sum of the fluxes of
Time series of hydrological (sea surface temperature – SST, salinity – SSS,
and Chl
The relationship between the coccolithophore taxa and the
environmental conditions during the monitored period was investigated
on the basis of a statistical multivariate analysis (
Time series of relevant atmospheric and oceanographic
parameters during the monitored time interval determined from
remote sensing;
The seasonal development of sea surface conditions did not differ
drastically between the two mooring stations during the monitored
period, despite considerable differences in the range of values of
salinity and Chl
Temporal variation in total coccolith export fluxes
(coccolith
Deviation from the annual mean coccolith flux determined for trap stations M4 (green) and M2 (transparent white).
Atmospheric conditions were similar at both locations. Despite the narrow
range of PAR values observed at both stations, a clear seasonality is
evidenced from slightly higher PAR during spring and summer (up to
65.615 Einstein
Station M4 received much higher fluxes than M2 during most of the
year, reaching an annual mean of
The number of species or groups of species was similar at stations M4 and
M2 (47 and 43 taxa, respectively) although slightly higher at the
westernmost site as also indicated by the higher Shannon–Weaver
diversity index (
Percentage of the most abundant coccolithophore taxa (
Most of the taxa produced much higher coccolith fluxes at the western
station M4. Such was particularly the case of
Coccoliths produced by
In comparison to the western site where different species revealed
distinct seasonal variations, at the more central site M2 most of the
taxa revealed a very similar seasonality, with the highest fluxes in late
October 2012 and early July 2013 and lower fluxes in early
November 2012, late May, and August 2013 (Fig. 6) The exceptions were
Coccolith export fluxes and relative abundance of the most
important species at stations M4 and M2:
Annual mean and range of coccolith fluxes and relative
abundances of the most abundant coccolithophore taxa (mean
Four factors were extracted from the multivariate factor analysis,
together explaining 63 % of the total variability within the data
(Fig. 7, Table 3). Factor 1 (F1, explaining 30 % of the total
variance) is represented by
Factor 2 (F2 – 16 %) is represented by precipitation, SST, and
Chl
Factor 3 (F3, 10 %) is represented by
Factor 4 (F4, 8 %) reflects
Spatio-temporal variation in the scores obtained from factor analysis. For taxonomical references, see Table 3.
Factor loadings (varimax raw), eigenvalues, and percentage of the
explained variance extracted from the data matrices referring to the
period from October 2012 to October–November 2013 at stations M4 and
M2 (
Comparable seasonal patterns in total coccolith fluxes observed at
stations M4 and M2 point to similar environmental background
conditions during the sampling period at both sites (Figs. 3
and 4). This is better expressed in Factor 2 (explaining 16 % of
the variance), showing that the overall atmospheric and oceanographic
conditions did not vary considerably between the two locations
(Fig. 7). In the tropical North Atlantic, meteorological conditions are
mostly controlled by seasonal variations in the trade winds and the
Intertropical Convergence Zone (ITCZ), the latter being a zone of low
pressure and increased cloudiness and precipitation near the Equator
(e.g. Oschlies and Garçon, 1998). The ITCZ migrates in latitude
during summer and winter months in the Northern Hemisphere, shifting
on average between 5
Climatological seasonal means of wind (speed and direction;
reference vector length: 3
Comparable seasonal developments in total coccolith export fluxes at
stations M2 and M4 were also reflected in the species composition.
A predominantly tropical assemblage was found throughout the
investigated period in both areas (Figs. 5 and 6), in general
agreement with previous studies from nearby tropical and subtropical
areas (Kinkel et al., 2000; Haidar and Thierstein, 2001; Winter
et al., 2002; Boeckel and Baumann, 2008; Poulton et al., 2017). It
included species considered well adapted to the high-nutrient and
low-light conditions prevailing in the LPZ, such as
In terms of seasonal patterns, however, little is known about the
living coccolithophore communities thriving in the tropical
Atlantic. In the subtropical Atlantic near Bermuda, 2200
That
In spite of similar seasonal developments in both coccolith fluxes and species composition, stations M2 and M4 revealed striking differences in export fluxes by most species, pointing to the influence of environmental factors that are specific to each location. Below we highlight the main differences between the two areas and discuss the factors that potentially trigger them.
Fluxes recorded at station M4 were high not only in comparison to
station M2, but also to several other locations in the Atlantic Ocean,
including open-ocean temperate and subtropical settings
(e.g. Knappertsbusch and Brummer, 1995; Broerse et al., 2000; Sprengel
et al., 2002), areas in the vicinity of islands (Sprengel et al.,
2002), and more marginal regions, even when under the influence
of coastal upwelling (Beaufort and Heussner, 1999; Köbrich and
Baumann, 2009). Furthermore, most of these flux studies referred to
the opportunistic
The persistent and overwhelming dominance of the LPZ flora suggests profiting from some subsurface and year-round nutrient supply. Forced by the trade winds, the westward deepening of the equatorial mixed layer and associated nutricline (see Hastenrath and Merle, 1987; Longhurst, 1993; Philander, 2001) could have promoted higher production of the LPZ flora in the western equatorial Atlantic (Fig. 10). In situ CTD and nutrient measurements at both stations do indicate a consistently deeper nutricline at M4, particularly during spring when the deep chlorophyll maximum (DCM) was found deeper at station M4 compared to station M2 (data not shown; Roepert and Brummer in Stuut et al., 2016).
In addition to the westward tilting of the nutricline, changes in the
depth range of the Antarctic Intermediate Water (AAIW) flowing in from
the south-west (Reid, 1994) may have also contributed to the enhanced
fluxes of the LPZ flora further west (see
Higher fluxes at station M4 may also be related to the higher production of faecal pellets by zooplankton grazers acting as vehicles for the downward flux of coccolithophores in this area. Recent observations by Knebel (2016) report higher fluxes of spinose planktonic foraminifera at station M4 compared to M2. Knappertsbusch and Brummer (1995) argued earlier that the export of coccolithophores is intimately related to day-to-day fluctuations in faecal pellet production by migrating zooplankton and nekton in the overlying mesopelagic zone. Therefore, higher zooplankton grazing in the western equatorial North Atlantic may have increased the coccoliths' transfer efficiency, hence contributing to the much higher coccolith fluxes compared to the central equatorial North Atlantic (Fig. 10).
Schematic figure summarizing
the main environmental mechanisms interpreted as being at the
origin of the ecological contrasts observed between stations M4
and M2 from October 2012 to October–November 2013: (A)
nutrient supply by AAIW depth range oscillations (dark blue
lowermost layer) combined with (B) nutricline E–W
basin-scale tilting (dashed black line), promoting the development
of the LPZ species
Spatial environmental variability in the equatorial North Atlantic is
most clearly expressed by the much higher fluxes and the pulsed maxima
of the more opportunistic species
The pronounced maximum of
Similar conditions appear to have recurred in April 2013 (sample
M4–12), with a pulsed maximum of
The pulsed maxima of
During the fall 2013 event, SSS had dropped to a minimum of 33.9 at
station M4 compared to
The present-day deposition of Saharan dust has been recently quantified
based on a transatlantic array of four sediment trap moorings between
NW Africa and the Caribbean, which included mooring traps M4 and M2
(Korte et al., 2017; van der Does et al., 2016). The increase in AOD
from spring to mid-summer at both stations (Fig. 2e and f) and its
positive correlation with wind speed during this time (F2 positive
scores; Fig. 7) corresponds to the same period when Korte
et al. (2017) found the best accordance between dust outbreaks
detected from satellite and high fluxes of dust-driven lithogenic
particles. This agrees with previous observations that transatlantic
Saharan dust fluxes are the highest during summer (e.g. Prospero et al.,
2014). Since precipitation started to increase at the beginning of
July at both stations (Fig. 2c and d), wet dust deposition probably
contributed to the observed enhanced coccolith fluxes (Figs. 3
and 4). Through the exposure of the dust particles to cloud processes and
mixing with anthropogenic species such as
Two prominent dust flux peaks not detected by satellite were
recorded in April and October–November of 2013 at station M4 (Korte
et al., 2017), precisely when
The observed short-term shift from a more typically tropical (
In spite of all this evidence, mineral dust deposition is also thought to increase carbon sequestration to the deep ocean by acting as a mineral ballast of sinking particles (Pabortsava et al., 2017). Van der Jagt et al. (2017) report more abundant and faster-sinking aggregates when formed from a natural plankton community that has been exposed to Saharan dust deposition compared to less abundant and slower-sinking aggregates when formed without dust. The same authors argue that such dust-influenced aggregates would become heavily ballasted with lithogenic material at the surface and hence without scavenging any additional particles during their settling. This could at least partially explain why the dust peaks in spring and fall were marked by maxima of surface-dwelling species but not maxima of the deep-dwelling species. To confirm whether the pulsed flux maxima of opportunistic species presented in our study truly reflected the response of living coccolithophores thriving in the overlying photic layer to such a combination of factors (ecological signal) or resulted from enhanced particle transfer efficiency (e.g. ballasting by dust; faecal pellet production by zooplankton grazers; Armstrong et al., 2002; Ziveri et al., 2007; Fischer and Karakas, 2009; Fischer et al., 2016), a comparison between settling coccolith assemblages and the living coccolithophore communities as well as with in situ atmospheric–oceanographic observations would be required.
Whereas the spring and fall
In contrast to station M4, persistently lower abundances of opportunistic
coccolithophore species, in particular the gephyrocapsids, and the absence of
major pulse-like increases in these species at station M2 point to comparably
more stable and oligotrophic conditions in this area. A narrower range and
lower values of the
That the evidence we found for ocean fertilization by Saharan dust is more significant at station M4 than at station M2 may be due to the presence of buoyant Amazon water retaining nutrients and phytoplankton near the surface at M4 and to higher wet dust deposition during fall 2013 at station M4 (e.g. Ridame et al., 2014; Fig. 2c and d). A longer distance to the dust source in Africa at M4 compared to M2 may have also contributed to increasing the bioavailability of dust-driven nutrients further west (see Stuut and Prins, 2014). This could also help explain the lack of clear evidence for dust fertilization in open-ocean regions west of Africa (see Fischer et al., 2016; Neuer et al., 2004) since aerosols sinking in these areas would not be fine and chemically processed enough to act as fertilizers.
Our study provides important insights into the environmental factors
governing the spatio-temporal variability of coccolithophores in the
equatorial North Atlantic and illustrates how this supposedly
oligotrophic and stable open-ocean region actually reveals significant
ecological variability. The main findings from our sediment trap study
are as follows.
A predominantly tropical coccolith settling assemblage and
a generally similar seasonality in total coccolith fluxes at the
western station M4 and central station M2 point to comparable
background environmental conditions at both sites. Flux maxima were
associated with stronger stratification conditions under the
influence of the Intertropical Convergence Zone (ITCZ) during
summer and fall, whereas flux minima occurred during stronger NE trade
winds and lower SSTs during winter and spring. Low-light- and deep-nutricline-dwelling In spite of the similar seasonal pattern, the two open-ocean
locations in the oligotrophic equatorial North Atlantic revealed
striking differences in coccolith export fluxes, species
proportions, and oceanographic processes. Total coccolith fluxes were almost 4 times higher at the western
station M4 than at the central station M2, mostly due to
Higher abundances and pulsed flux maxima of more opportunistic
species at station M4 point to the occurrence of transient
productivity in this area: (a) the increase in Enhanced surface buoyancy provided by the relatively less saline
Amazon River Plume appears to have contributed through retaining
dust-derived nutrients in the surface layer during the fall of 2013,
promoting the development of several opportunistic phytoplankton
groups in the western site M4. In contrast, persistently low coccolith fluxes in the central
site M2, in particular of more opportunistic species, and the
absence of major
Our findings (i) provide relevant evidence to support the hypothesis
of Saharan dust acting as a fertilizer for marine phytoplankton in the
Atlantic Ocean and (ii) highlight the importance of LPZ
coccolithophore species in terms of coccolith export production in the
tropical Atlantic, with possible implications for the global oceanic
carbonate budget.
Data are available at
The authors declare that they have no conflict of interest.
Moorings were deployed during RV