Introduction
Planktic foraminifera have a long history as paleoceanographic proxies due to
their environmental sensitivity, cosmopolitan distribution, and extensive
fossil record. The close association between planktic species and local
hydrography means that fossil foraminiferal assemblages have often been used
to reconstruct the distribution of water masses through time (e.g., Berger,
1968; McIntyre et al., 1972; Oberhänsli et al., 1992; Ufkes et al.,
1998). However, at sites where overlying water masses change seasonally, the
foraminiferal fossil record will represent a combination of individuals that
may have grown under vastly different conditions. This averaging of
short-term variability has the potential to impact the interpretation of any
proxy based on foraminifera. Seasonality in a variety of environments has
been shown to have a pronounced effect on foraminiferal communities, with
species assemblages changing throughout the year (Thunell et al., 1983;
Reynolds and Thunell, 1985; Thunell and Honjo, 1987; Thunell and Sautter,
1992; Ortiz et al., 1995; Marchant et al., 1998; Eguchi et al., 2003; Pak et
al., 2004). Previous studies have explored seasonal assemblage shifts in the
North Pacific, including at Station Papa (50∘ N, 145∘ W;
Thunell and Reynolds, 1984; Reynolds
and Thunell, 1985), in the California Current off of Oregon (> 130 km offshore) (Ortiz et al., 1995),
in the Santa Barbara Basin (Kincaid et al., 2000; Darling et al., 2003), off
Southern California (Sautter and Thunnell, 1991), and in the western Pacific
(Eguchi et al., 2003). The majority of this prior work has focused on
open-ocean assemblages, however, leaving a gap in understanding the seasonal
dynamics in coastal upwelling regions, as well as a significant spatial gap
within the California Current system between the Southern California Bight
and Oregon.
An improved understanding of coastal upwelling fauna is also important for
interpreting the paleoclimate record of these conditions (Reynolds and
Thunell, 1986; Naidu and Malmgren, 1995; Vénec-Peyré and Caulet,
2000; Ishikawa and Oda, 2007). Many modern surveys have characterized
upwelling-associated foraminifera through plankton tow and sediment trap
studies in the tropics and subtropics (e.g., Thiede, 1975; Naidu, 1990;
Thunell and Sautter, 1992; Pak et al., 2004; Salgueiro et al., 2008).
Temperate and subpolar upwelling communities such as those found along the
central California shelf, however, remain poorly understood. On-shelf
assemblages are particularly important for regions dominated by coastal
upwelling processes where the alternation between upwelling and relaxation
(periods of reduced wind strength in between upwelling periods) has large
regional impacts on oceanography and planktic communities (Botsford et al.,
2006; Dugdale et al., 2006; Largier et al., 2006; Garcí-Reyes et al.,
2014). From a paleontological perspective, modern nearshore assemblages are
of interest because sediments in these regions are among those most likely to
contain a preserved carbonate fossil record, and thus intact fossil
assemblages, due to the high sedimentation rates and the limitations of a
narrow continental shelf above a shallow lysocline.
Understanding planktic foraminiferal assemblages in coastal upwelling regions
is also relevant for predicting future climate and ecosystem perturbations.
The California Current and other Eastern Boundary Current upwelling systems
have been identified as especially susceptible to ocean acidification due to
the incorporation of anthropogenic CO2 into the surface ocean
superimposed on naturally corrosive waters (Feely et al., 2008; Hofmann et
al., 2010; Hauri et al., 2013). The pronounced influence of upwelling in this
region is also likely to intensify due to anthropogenic impacts (Bakun, 1990;
García-Reyes and Largier, 2012; Sydeman et al., 2014), compounding the
impacts of ocean acidification. Planktic calcifiers such as pteropods
(Bednaršek et al., 2014; Busch et al., 2014), coccolithophorids (Beaufort
et al., 2011; Iglesias-Rodriguez et al., 2008; Langer et al., 2006), and
foraminifera (Barker and Elderfield, 2002; Manno et al., 2012; Moy et al.,
2009) may be especially vulnerable to reductions in ocean calcite and
aragonite saturation state. Upwelled waters are already becoming more acidic
along the California margin, and the seasonal duration for which fauna are
exposed to waters undersaturated with respect to aragonite and calcite is
predicted to increase in the near future (Feely et al., 2008; Gruber et al.,
2012; Harris et al., 2013; Hauri et al., 2013). The response of planktic
foraminiferal assemblages to 20th century warming has been documented in
Southern California (Field et al., 2006). An understanding of the modern
seasonality of planktic foraminifera in this intense upwelling region can
therefore serve as a baseline for future climate-driven change and may help
to identify which upwelling species may already be living at low-saturation
state and be potentially tolerant of low calcite saturate state waters that may
resemble future conditions in the open ocean.
Here we focus on planktic foraminiferal assemblages sampled along a
cross-shore transect over the central California shelf extending from 1 km
offshore to the shelf break (30–60 km offshore). Plankton tows, supported
by in situ water column data and discrete bottle samples, allow a
documentation of species associations based on instantaneous (as opposed to
time-averaged) water column conditions. Our goal was to understand (1) the
spatial and temporal distribution of planktic foraminifera along the central
California shelf and (2) the manner in which species assemblages respond to
high frequency changes in water mass, especially those associated with
upwelling. These efforts may offer a general framework for interpreting
seasonality in foraminiferal records drawn from analogous oceanographic
regions and could yield new insights into how this important group of marine
calcifiers responds to ongoing climate change and acidification in coastal
upwelling systems.
Regional setting
The California Current is the southward flowing arm of the North Pacific
Subtropical Gyre and, along with the seasonal Davidson
Countercurrent, flows adjacent to the
central Californian coastline to the west of our study sites. At many
locations along the coast, wind-driven coastal upwelling brings deeper,
colder, nutrient-rich and low-O2 water to the surface, with the
strongest upwelling signal found in a 10 to 25 km band just offshore
(Hickey, 1979, 1979; Huyer, 1983; Lynn and Simpson, 1987).
At the latitudes of our study sites (37–39∘ N), wind-driven coastal
upwelling is generally strongest in April–June (García-Reyes and
Largier, 2012). During the upwelling
season, wind-driven upwelling events are interspersed with relaxation
periods, the combination of which is responsible for large changes in
productivity in the plankton (Botsford et al., 2006; Dugdale et al., 2006;
Largier et al., 2006; García-Reyes et al., 2014). During the upwelling
season, further complexity is introduced through the advection of upwelled
water masses both away from the continent and alongshore, with water parcels
in the region which are dominantly sourced from the north (Kaplan and
Largier, 2006). Outside of the upwelling season (∼ September–March),
upwelling events are generally absent and there is occasional occurrence of
downwelling, with net northward flow of water. Advection rates are variable
but have been reported in the range of 10–30 km d-1 (Kaplan and
Largier, 2006). This stable post-upwelling season generally lasts into
December when the stability can be punctuated by storm conditions (Kaplan and
Largier, 2006; García-Reyes and Largier, 2012). Together, these conditions create an environment of strong
seasonality in terms of productivity, temperature, O2, carbon chemistry,
and water mass, all of which would be expected to influence the species of
planktic foraminifera present in the region.
Methods
Study area
Plankton collection took place at eight stations located at increasing distances
from shore across the continental shelf (Fig. 1). Bodega Line (BL)
(38∘) sites start at nearshore station BL1, 1 km offshore, and
extend across the shelf to station BL5, 32 km offshore. These stations were
sampled monthly to bimonthly from September 2012 to September 2014. Three
additional stations were sampled in 2013 and 2014 as part of the Applied
California Current Ecosystem Studies (ACCESS) cruises (three times per year)
and are located just over the shelf break at 40–60 km offshore, spanning a
latitudinal range from 37–39∘ N (Table 1). All sampling stations
are shoreward of the central core of the California Current (Lynn and
Simpson, 1987) and are strongly influenced by both spring/summer upwelling as
well as winter storms (Fig. 1).
Station locations, depths, and the number of times sampled over the
course of this study.
Station
Latitude
Longitude
Depth
No. of times
sampled (m)
sampled
BL1
38∘16′59′′
-123∘04′60′′
25
15
BL2
38∘23′38′′
-123∘13′00′′
45
15
BL3
38∘21′05′′
-123∘14′20′′
90
15
BL4
38∘26′20′′
-123∘27′01′′
120
15
BL5
38∘21′05′′
-123∘37′59′′
200
14
A2W
38∘02′45′′
-123∘33′47′′
200
5
A4W
37∘52′55′′
-123∘28′30′′
200
4
A6W
37∘43′20′′
-123∘13′59′′
200
5
Map of tow stations BL1-5, A2W, A4W, and A6W.
Sample collection
Vertical net tows integrated foraminifera across the water column from the
surface to a depth of 200 m or to 10 m above the sea floor at shallower
sites. All foraminifera were sampled with a 150 µm mesh net. This
approach potentially excludes juveniles and small adults and therefore
limited the samples to foraminifera of readily identifiable adult
developmental stages and to species normally included in fossil analyses.
Most samples were placed in ambient surface seawater and kept chilled without
further preservation to be picked immediately upon return to shore. When this
procedure was not feasible, samples were preserved shipboard in 95 %
ethanol, buffered to a pH > 8.5 with
Tris(hydroxymethyl)aminomethane. Foraminifera were picked wet from bulk tow
material, rinsed in DI water and archived in slides. All archived
foraminifera were identified to the lowest possible taxonomic level, with
N. incompta and N. pachyderma defined primarily by shell
coiling direction (following Darling et al., 2006). No distinction was made between living
and dead individuals although almost all shells still contained some
cytoplasm at the time of sorting. Taking into account the conservative end of
the range of sinking rates for shells (e.g., 29–552 m d-1; Takahashi
and Be, 1984) and that foraminifera were sampled from the upper 200 m of the
water column, we can assume that all foraminifera were likely alive within
6 days of collection. Transport data from the region allow us to further
estimate a maximum horizontal transport of 50 km in 5 days, indicating that
all shells still within the water column were locally sourced (Kaplan and
Largier, 2006).
Environmental measurements
Water column profiles for temperature, salinity, dissolved O2 (DO), and
fluorescence were obtained across the plankton tow depths using a Seabird
Electronics SBE 19 conductivity–temperature–depth (CTD) profiler. Plankton
tow nets were equipped with a flow meter for each cast; however, due to
frequent failures, flow rates were unreliable and are not reported here. At
each station, discrete bottle samples of surface water and water from the
bottom of each CTD cast were collected using a Niskin sampler. All water
samples were analyzed spectrophotometrically for pH (total scale) using
either a Sunburst SAMI (Submersible Autonomous Moored Instrument) modified
for benchtop use (SD ± 0.009) or an Ocean Optics Jaz Spectrophotometer
EL200 (SD ± 0.003) using m-cresol purple (Dickson et al., 2007). Total alkalinity
was determined via automated Gran titration on a Metrohm 809 Titrando (SD ± 2.809 µmol kg-1),
with acid concentrations standardized to Dickson
certified reference materials (A. Dickson, Scripps Institution of
Oceanography, CA, USA). Measurements of pH and alkalinity were carried out
at UC Davis Bodega Marine Laboratory and used to calculate other inorganic
carbon system parameters, including calcite saturation state (ΩCa) and [CO3=], using the software CO2Calc (Robbins et al.,
2010). Thermocline depths were defined as the depth (below 5 m) at which the
greatest gradient in temperature occurred, exclusive of any temperature
change with a slope of less than 0.1 ∘C m-1, in which case
the thermocline was assumed to be deeper than the profiled water. Upwelling
index is taken from the PFEL upwelling index modeled for 39∘ N
(http://www.pfeg.noaa.gov/products/PFEL/modeled/indices/upwelling/upwelling.html),
which is in general agreement with temperature measurements from the Bodega
Ocean Observing Node (BL1).
Data analysis
For the four most abundant species, G. bulloides, Turborotalia quinqueloba, N. incompta, and
N. pachyderma, we performed a CCA (canonical
correspondence analysis) on relative abundances using the “vegan” package in
R (R Core Team, 2013; Oksanen et al., 2016). Potential explanatory
variables included day of the lunar cycle relative to the new moon,
upwelling index, duration of sustained upwelling as indicated by the PFEL
upwelling index, surface and deep water carbonate system parameters, and CTD
temperature, salinity, fluorescence, and DO. CTD data were binned into
depths at 5 m intervals to a depth of 25 m and then at 10 m intervals. A
subset of variables was selected for CCA by exclusion of all variables not
related to any total abundances by pairwise correlation at a 95 %
confidence level. Strongly interrelated or redundant parameters were
additionally excluded (i.e., a parameter correlated at multiple consecutive
depths would have been considered at only one of these depths).
Results
The assemblage was heavily dominated by the planktic species N. pachyderma,
N. incompta, T. quinqueloba, and G. bulloides,
representing 35.3, 23.1, 13.5, and 11.7 % of all recovered
foraminifera, respectively. Less common forms included
Globigerinita glutinata, Globorotaloides hexagonus, Globigerinella calida, Globigerinita uvula, and Globorotalia spp., as well the
occasional cosmopolitan species, Orbulina universa and subtropical Neogloboquadrina dutertrei, and, rarely, benthic
species of foraminifera. The presence of these latter taxa was sporadic and
in low abundance (all < 1 % of the overall recovered foraminifera,
with the exception of G. glutinata at 2.1 %); therefore, further analysis will be
confined to the four most abundant species.
At offshore stations BL3, BL4, and BL5 and off-shelf stations A2W, A4W, and
A6W, foraminifera displayed a clear seasonality. The year can be divided
between spring / summer and fall / winter faunas that coincide with the
upwelling-dominated and non-upwelling season (Fig. 2). Beginning in May,
shortly after the onset of upwelling, samples began to show a high abundance
of T. quinqueloba. A bloom of N. pachyderma, seen here as
an increase in total abundance to > 200 individuals, occurs in
July or August, after several months of sustained upwelling, followed by a
decrease in both total and relative abundance to less than 50 % by the end
of summer (Fig. 3). N. pachyderma was also present through much of
the winter in lower numbers in 2012–2013. By contrast, this species was
virtually absent in the winter of 2013–2014, before reappearing after a
period of sustained upwelling in July 2014 (Fig. 3). In both years, the
earliest N. pachyderma blooms appeared to initiate farther offshore,
although abundances within a given samples did not appear to be directly
linked to specific upwelling events.
A time series of CTD cast profiles for
(a) temperature, (b) productivity, and (c) DO
taken between September 2012 and October 2014. Time series are compiled from
CTD casts at BL5 in conjunction with plankton tows and supplemented with data
from weekly CTD casts taken at BL1 as a part of the Bodega Ocean Observing
Node. Black points at the top of each figure denote the location of each CTD
cast.
Following the end of the summer season, the fall–winter fauna shows a more
even distribution of species and a distinct shift in the ratio of N. pachyderma to N. incompta
(Fig. 3). N. incompta was equally or more abundant than N. pachyderma during the non-upwelling season
although it was present year-round. G. bulloides also began to appear in the water column
in the fall, strongly associated with non-upwelled waters, and is present
throughout the winters. G. bulloides was present primarily in the winter and either
absent or found only in very low numbers during the summer season.
The same suite of species was present at nearshore stations BL1 and BL2,
but counts were lower year-round and most seasonal patterns seen
offshore were not evident. N. pachyderma did appear to increase in relative abundance
during the summer at these stations but remained in low abundance along
with N. incompta year-round (Fig. 4). T. quinqueloba was also observed year-round at these nearshore
stations. A greater proportional abundance of G. bulloides was seen during the fall and
winter at nearshore sites, consistent with findings at the offshore stations
(Fig. 4).
Relative abundance of all species at nearshore stations BL1 and
BL2, with total number of foraminifera marked at the top of each bar.
Upwelling index for 39∘ N (PFEL; http://www.pfeg.noaa.gov/products/PFEL/modeled/indices/upwelling/upwelling.html),),
with “upwelling season” shaded in grey and periods of sustained upwelling
conditions during the relevant years shaded in red. The range of
Calcite observed on each tow is marked in black, with Ωcalcite= 1 marked in red and Ωcalcite= 1.5 in
pink. Percent abundances from vertical tows of
G. bulloides, T. quinqueloba, N. incompta, and N. pachyderma from offshore
stations BL3, BL4, BL5, and off-shelf stations AW2, AW4, and AW6 shown in
orange, pink, green, and purple, respectively.
Environmental measurements
In spring and summer, surface hydrographic conditions were highly variable,
reflecting alternating upwelling events and relaxation periods. Frequent
changes in thermocline depth were observed, as well as intermittent blooms of
near-surface productivity (Fig. 2). This resulted in a more
surface-stratified and productive water column, with a shallow thermocline
and high fluorescence in the upper water column. During upwelling season,
near-surface temperatures cool to 8–9 ∘C, and subsurface waters
approach calcite undersaturation (ΩCa < 1) and display low
DO (< 4 mg L-1 at < 90 m) (Fig. 5). Despite consistently lower
subsurface DO and pH, high near-surface productivity often increased DO and
pH near-surface values, creating a noticeable down-profile gradient in these
parameters.
Biplot of canonical correspondence analysis of relative abundance of
the four most abundant species compared with environmental variables at the
time of collection for all tows in which foraminifera were found. Dominant
species are represented by large red points, and small points represent
individual tows. Grey points are tows that fall within upwelling season, as
shown in Fig. 2, and black points outside of this season. Points with a
golden halo represent tows during lunar days 14–18.
Beginning in the late fall, and continuing into early spring, a consistently
deep thermocline was observed at all stations. This trend often had the
effect of confining the entire on-shelf water column (including all tow
samples) to this deep mixed layer, which dominated the shelf in winter.
Temperatures were generally warmer (11–14 ∘C) than during the
upwelling season with relatively low fluorescence in the upper water column
(< 4) (Fig. 5) and ΩCa > 1.5 throughout the
sampled water column. García-Reyes and Largier (2012) describe storm
conditions, which are likely to have contributed to the deep mixed layer,
observed outside of upwelling season (especially between January and March).
Canonical correspondence analysis
A CCA shows that the highest relative abundances of both G. bulloides and N. incompta fall along
dimensions strongly influenced by environmental variables characteristic of
non-upwelling season, such as higher temperatures and increased dissolved
oxygen. The highest relative abundances of N. pachyderma are most closely associated with
fluorescence, especially near the surface (5 m) and at 60–70 m water depth,
more associated with upwelling waters. T. quinqueloba is also distinct, falling within the
quadrant most associated with tows taken during upwelling (Fig. 6). Figure 5
additionally shows the range of environmental conditions captured by
sampling around the full moon (lunar days 14–18).
Ratio of N. pachyderma to N. pachyderma
and N. incompta at 40 m depth with 95 % confidence envelopes.
Neogloboquadrina coiling direction
Coiling direction for Neogloboquadrinids is recognized as an empirical proxy
for sea-surface temperature in the sedimentary record (Ericson, 1959; Bandy,
1960; Kennett, 1968; Bé and Tolderlund, 1971; Vella, 1974; Arikawa,
1983; Reynolds and Thunell, 1986). We tested whether the relationship is
consistent on shorter timescales with mixed assemblages of N. pachyderma (primarily
sinisterly coiling) and N. incompta (primarily dextral coiling) (Darling et al.,
2006). A very weak linear correlation with surface temperature is observed,
between the ratio of N. pachyderma to all N. pachyderma and N. incompta
(r2= 0.09626; p value = 0.02).
Correlations improved deeper in the water column, with a weak but notable
relationship at 40 m (r2= 0.3285; p value < 0.001) (Fig. 7).
Discussion
Foraminiferal seasonality
A key finding of this study is the clear seasonality of the four most
abundant species of planktic foraminifera at offshore stations along the
central California shelf. Our findings highlight the importance of
seasonal-scale water column shifts in dictating foraminiferal species
abundances, as well as suggest which species may be most vulnerable to ocean
acidification in the region. It may also act as a guide to
paleoceanographers in deciphering the specific species most likely to be
recording seasonal signals along the shelf. T. quinqueloba appears to be associated mainly
with the early summer months and the beginning of upwelling season as
indicated by the PFEL Upwelling Index for the relevant study years. N. pachyderma
increased in both total number and relative abundance in the late summer
months following the onset of upwelling. G. bulloides is largely confined to the winter
non-upwelling season while N. incompta is present in all seasons. The year-round
presence of N. incompta combined with the high summer abundance of N. pachyderma creates the
appearance of a seasonal switch in the relative abundances of the two
Neogloboquadrinids (Fig. 3). These trends are described in more detail for
each of the four species below.
Neogloboquadrinids
The seasonal trade-off observed at offshore stations between N. pachyderma and N. incompta is in
agreement with previous studies interpreting seasonality from the
geochemistry of the two species. Sediment trap data from the western North
Pacific found that N. incompta and G. bulloides reflect
winter sea-surface temperature while N. pachyderma reflects summer
(Sagawa et al., 2013). Similarly, Mg / Ca ratios in recent fossils from the
Norwegian Sea indicate that N. pachyderma is primarily a summer bloom species while N. incompta
records winter conditions (Nyland et al., 2006). The close association
between G. bulloides and N. incompta seen here has also been noted previously both in the water
column and in coretop records (Reynolds and Thunell, 1986; Giraudeau, 1993;
Ufkes et al., 1998).
The ratio of N. pachyderma to N. incompta (previously N. pachyderma
var. sinistral and N. pachyderma var. dextral, respectively)
has long been recognized to be paleoceanographically significant in marine
sediments, with N. pachyderma associated with subpolar water masses, N. incompta associated with
subtropical to temperate waters, and the ratio between the two acting as a
proxy for sea-surface temperature (Ericson, 1959; Bandy, 1960; Kennett,
1968; Bé and Tolderlund, 1971; Vella, 1974; Arikawa, 1983; Reynolds
and Thunell, 1986). The relationship observed here between coiling
direction of Neogloboquadrinids and temperature is weak, at best, at the
surface. The relationship is slightly stronger at 40 m depth (Fig. 7), with
an equal ratio between N. incompta and N. pachyderma found around 10.5 ∘C. This ratio can
largely be explained by the year-round presence of N. incompta, punctuated by an
increase in N. pachyderma in the summer along with cooler temperatures, especially in the
subsurface. These findings validate on short timescales what has been seen
to be empirically true over longer timescales: N. pachyderma is found primarily in high-latitude waters and, when occurring in temperate regions, occurs mixed with
N. incompta, in both the water column or sediment. This pattern is suggestive of an
incursion of these cooler northern waters and not solely the impact of
upwelled waters in this region (< 10 ∘C conditions).
Water column fluorescence data and total number of foraminifera
recovered at stations BL 1–5 on 4 days of extremely low productivity. CTD
data from these five stations demonstrate small-scale variability from 1 to
32 km offshore along the continental shelf. This is
compared with the total
number of foraminifera retrieved at each of these stations.
G. bulloides, T. quinqueloba,
N. incompta, and N. pachyderma counts by lunar day from the new moon (day 0) to full moon
(Day ∼ 14). Abundances are taken from integrated tows, at 25, 45,
90, 120, and 200 m depending on the station (see Table 1).
Symbols denote tow station.
Globigerina bulloides
Globigerina bulloides has previously been associated with active upwelling in Southern California
(Sautter and Thunell, 1991; Field et al., 2006) and the Arabian Sea
(Peeters et al., 2002). Observations along the central California shelf are
in direct contrast to this, with G. bulloides observed to be far more abundant during
the fall/winter relaxation and storm season (Fig. 3). It is notable that in
at least one previous study, G. bulloides has shown a bimodal abundance in Southern
California, with one population of G. bulloides associated with winter and another
population with the spring / summer upwelling season (Sutter and Thunell,
1991). Furthermore, two distinct genotypes of G. bulloides have been identified in
Southern California, one of which is present in winter samples and was
previously recognized in “subpolar” regions (Darling et al., 2003). We
interpret the G. bulloides observed along the central California coast as connected to
this “subpolar”/winter population, accounting for the differences in
seasonal abundance seen at our northern site compared to Southern
California.
Spatial dynamics
Nearshore stations BL1 and BL2 are shoreward from the primary band of
coastal upwelling (Huyer, 1983) and show less seasonality in species
abundances with the exception of G. bulloides, which is more abundant in the fall and
winter nearshore as well as offshore. Although non-spinose forms are also
occasionally present at both nearshore sites, they do not show the
seasonality that they do at offshore sites (Fig. 4). Some of the differences
seen in the fauna at BL1 and BL2 compared to offshore stations may be due to
shallower tow depths at these sites (25 and 45 m, respectively) and
therefore a bias in favor of species living closer to the surface, which may
include G. bulloides. However, shallow tows conducted at BL4 and BL5 confirm that all
four species considered here are present in the upper water column
(< 30 m) at these sites, so depth alone cannot completely account
for the nearshore/offshore difference in foraminiferal abundances. Nearshore
stations may be sheltered from larger-scale transitions in source water that
happen over most of the shelf and be more impacted by terrestrial processes.
Short-term spatial dynamics were also observed to impact foraminiferal
abundance. On days when overall productivity was low, abundances of all
foraminifera species were higher at sites with higher fluorescence
(indicating higher biomass and suggesting higher primary productivity).
Especially low fluorescence (near-surface fluorescence < 2) was
observed on collection days 4 February 2013, 16 January 2014, 1 July 2014,
and 26 February 2013. On
these days, foraminifera were recovered in much greater numbers at stations
associated with peak fluorescence regardless of where along the transect the
station was located (Fig. 8). No foraminifera were recovered at
very low-productivity stations BL1 and BL5 on 16 January 2014 or at BL1 on 1 July 2014, while other
sites yielded > 100 individuals. On 4 February 2013, BL2 was associated
with the only observation of surface fluorescence > 10 and
yielded more foraminifera than all other sites combined. Fluorescence was
low at all sites on 26 February 2013 and no foraminifera were recovered from these
tows (Fig. 8). These data indicate that phytoplankton productivity may
ultimately be a limiting factor for all species. On days with higher
measured fluorescence (productivity), the dominant spatial trend was towards
higher abundances further offshore regardless of where peak productivity was
observed.
Foraminifera in reduced pH waters
Upwelling associated waters with low ΩCa were observed on
multiple occasions during plankton tows. Foraminifera are widely thought to
be susceptible to ocean acidification (i.e., Barker and Elderfield, 2002;
Manno et al., 2012; Moy et al., 2009; Orr et al., 2005), although this
susceptibility may not always manifest through a reduction in shell weight
in open-ocean conditions (i.e., Beer et al., 2010; Aldridge et al., 2012;
Weinkauf et al., 2016). The association of multiple species of foraminifera
already living at ΩCa < 1 or very low ΩCa (< 1.5) waters is notable. In particular, more than a
quarter (26 %) of all observed N. pachyderma, with its strong upwelling association,
was found to occur in a water column with ΩCa < 1 in
the upper 160 m. Culture studies with this species have indicated a decrease
in shell weight associated with low ΩCa well within the range
of those that N. pachyderma was found in during upwelling season, indicating the
potential to impact carbonate flux in areas where this organism is an
important calcifier (Manno et al., 2012). If N. pachyderma is already living near its
ΩCa tolerance, this species may be exceptionally vulnerable
to a continued increase in ocean acidification in this region. However, it
is possible that upwelling-adapted N. pachyderma may prove to be an example of
a calcifying plankton able to tolerate undersaturated waters.
Causes of seasonality and fluctuations in abundance
Seasonality has previously been identified in temperate regions globally for
all four of the species addressed here (Jonkers and Kucera, 2015). One
important mechanism contributing to the seasonal progression of foraminifera
species along the shelf in central California is the alternation between the
direction of net water transport between upwelling and non-upwelling
seasons. This phenomenon would account for the occurrence of G. bulloides in greater
numbers outside of upwelling season when net poleward water transport is
expected (Kaplan and Largier, 2006). Similarly, the influx of subpolar
associated N. pachyderma could be due to this species being carried into the region
during the southward transport of water that occurs during upwelling season
(Kaplan and Largier, 2006). This is in slight contrast to the hypothesis of
N. pachyderma dormancy outside of upwelling season suggested in the Arabian Sea (Ivanova
et al., 1999), since in the California Current as well as on the Namibian
margin there is some synchronicity between the preferred seasonality of N. pachyderma and
greater transport into the region from high-latitude waters (Ukfes and
Zachariasse, 1993). An alternation between the foraminiferal fauna of source
waters additionally offers an explanation for the seasonal absence and
reappearance of both N. pachyderma and G. bulloides. N. incompta, found year-round in the study region, may be
present in both water masses.
In addition to the broad oscillation of source waters, higher counts of each
species are associated with some specific water column characteristics. In
most cases, species abundances could not be linked strongly to single
environmental parameters, but rather a suite of hydrographic and temporal
variables were required to account for faunal assemblages. For some species,
particular variables can be identified through pairwise correlation as having
a significant effect on abundance (Fig. S2 in the Supplement). In G. bulloides, higher
abundance correlates with higher water temperatures throughout the water
column. In N. pachyderma, higher abundances are associated with
higher fluorescence and thus enhanced primary production. For N. incompta, counts seem to loosely correlate with higher O2 and lower
salinities, while T. quinqueloba is not clearly correlated with any
single measured parameter (Fig. S2).
A CCA shows the relative abundances of G. bulloides, N. incompta, and N. pachyderma to be dependent upon
environmental variables strongly associated with coastal upwelling
conditions (Fig. 6). However, the directions of those associations vary. N. pachyderma and,
to a lesser extent, T. quinqueloba seem to be associated with upwelling-like water
conditions. Sediment trap time series have previously linked T. quinqueloba to productivity
in the North Atlantic (Chapman, 2010), which could explain the association
of this species with the higher-productivity season, although it is not
directly associated with shifts in productivity as is N. pachyderma. G. bulloides, however, is
negatively associated with upwelling-like water conditions and more
associated with warmer waters and higher DO levels seen outside of upwelling
season. N. incompta relative abundances also increase outside of upwelling season,
although in this case relativity may be key, especially with regards to N. pachyderma
(see Sect. 4.1.1). This outcome is supported by total counts, which indicate that
this species is the only one clearly present at the tow sites year-round.
Lunar periodicity
Abundances of G. bulloides, T. quinqueloba, N. incompta, and
N. pachyderma all display an abundance cycle with a 28-day period
that appears to coincide with the lunar cycle (Fig. 9). Peak counts for each
species occur within 7 days of the full moon, before dropping off before the
new moon (Fig. 8). This trend offers further evidence that planktic
foraminifera reproduce on a lunar cycle (Spindler et al., 1979; Bijma et al.,
1990, 1994; Schiebel et al., 1997; Jonkers et al., 2015;
Venancio et al., 2016; Erez et al., 1990). The peak abundance for G. bulloides occurs
before that in the other species, starting 3 days before the full moon and
remaining high until 4 days after the full moon. Abundances in N. pachyderma and N. incompta begin to increase around the same time,
but high abundances in these species continue until 5 and 7 days after the
full moon, respectively. Whether the observed offsets in peak abundance around
the full moon represent inter-species differences in reproductive timing or
are an artefact of sampling against a background of strong seasonality in a
highly variable environment cannot be resolved from this dataset, even though
sampling days surrounding the full moon occurred across seasons (Fig. 5).
Application to the fossil record
The presence of seasonally distinct faunas along the central California
margin can be used in increasing the resolution of paleoceanographic and
paleoecological records, as different species clearly represent different
states of the seasonal upwelling regime. Single-species geochemical records
are likely to show a strong bias towards either upwelled or non-upwelled
water masses and, therefore, could potentially be harnessed as a record of
changes in upwelling intensity and associated water chemistry. Our findings
reaffirm a strong relationship between the dominance of N. pachyderma in conditions
favorable to upwelling. This pattern has been noted along the African
margin (Giraudeau, 1993), in the Arabian Sea (Ivanova et al., 1999), and on
the Namibian margin (Ufkes and Zachariasse, 1993). It remains possible that
other genotypes of N. pachyderma have distinct and ecological preferences particularly
those associated with the Arctic and Antarctic (Darling et al., 2006, 2007). As our record is based on discrete tows and not a
continuous record, the percent composition of species cannot be directly
translated into a sediment flux or to what would be preserved in aggregate
in the fossil record. However, the upwelling season bloom of N. pachyderma seen here is
strong enough that this signal would likely dominate the annual assemblages,
although the vast majority of N. pachyderma (81 % of those seen in tows) occur between
July and November.
Globigerina bulloides has been associated with upwelling at other sites globally (Sautter
and Thunell, 1991; Peeters et al., 2002; Field et al., 2006) and even used as an
upwelling indicator in the fossil record (e.g., Naidu, 1990; Kroon et al.,
1991; Anderson and Prell, 1993; Naidu and Malmgren, 1996). However, within
our study region, this species was present almost exclusively outside of
upwelling season. The majority (88 %) of the G. bulloides seen in our samples was
observed between November and February. CCA supports these observations in
indicating that the relative abundance of this species is negatively
associated with upwelling-like conditions in the region. This situation
contrasts with findings in Southern California and the Oman Margin (Peeters
et al., 2002; Field et al., 2006), highlighting the importance of using
regionally specific associations where possible when interpreting planktic
assemblages in the sediment record.