Over the last decades, hypoxia in marine coastal
environments has become more and more widespread, prolonged and intense.
Hypoxic events have large consequences for the functioning of benthic
ecosystems. In severe cases, they may lead to complete anoxia and the presence
of toxic sulfides in the sediment and bottom-water, thereby strongly
affecting biological compartments of benthic marine ecosystems. Within these
ecosystems, benthic foraminifera show a high diversity of ecological
responses, with a wide range of adaptive life strategies. Some species are
particularly resistant to hypoxia–anoxia, and consequently it is interesting
to study the whole foraminiferal community as well as species-specific
responses to such events. Here we investigated the temporal dynamics of
living benthic foraminiferal communities (recognised by
CellTracker™ Green) at two sites in the saltwater Lake
Grevelingen in the Netherlands. These sites are subject to seasonal anoxia
with different durations and are characterised by the presence of free
sulfide (H2S) in the uppermost part of the sediment. Our results
indicate that foraminiferal communities are impacted by the presence of
H2S in their habitat, with a stronger response in the case of longer
exposure times. At the deepest site (34 m), in summer 2012, 1 to 2
months of anoxia and free H2S in the surface sediment resulted in an
almost complete disappearance of the foraminiferal community. Conversely, at
the shallower site (23 m), where the duration of anoxia and free H2S
was shorter (1 month or less), a dense foraminiferal community was found
throughout the year except for a short period after the stressful event.
Interestingly, at both sites, the foraminiferal community showed a delayed
response to the onset of anoxia and free H2S, suggesting that the
combination of anoxia and free H2S does not lead to increased
mortality, but rather to strongly decreased reproduction rates. At the
deepest site, where highly stressful conditions prevailed for 1 to 2
months, the recovery time of the community takes about half a year. In Lake
Grevelingen, Elphidium selseyense and Elphidium magellanicum are much less affected by anoxia and free H2S than
Ammonia sp. T6. We hypothesise that this is not due to a higher tolerance for
H2S, but rather related to the seasonal availability of food sources,
which could have been less suitable for Ammonia sp. T6 than for the elphidiids.
Introduction
Hypoxia affects numerous marine environments, from the open ocean to coastal
areas. Over the last decades, a general decline in oxygen concentration was
observed in marine waters (Stramma et al., 2012), with an extent varying
between the concerned regions. In coastal areas, oxygen concentrations have
been estimated to decrease 10 times faster than in the open ocean, with
indications of a recent acceleration, expressed by increasing frequency,
intensity, extent and duration of hypoxic events (Diaz and Rosenberg, 2008;
Gilbert et al., 2010). This is due to the combination of (1) global warming,
which is strengthening seasonal stratification of the water column and
decreasing oxygen solubility, and (2) eutrophication resulting from increased
anthropogenic nutrient and/or organic matter input, which is enhancing
benthic oxygen consumption in response to increased primary production (Diaz
and Rosenberg, 2008). Bottom-water hypoxia has serious consequences for the
functioning of all benthic ecosystem compartments (see Riedel et al., 2016,
for a review). Benthic faunas are strongly impacted by these events (Diaz
and Rosenberg, 1995), even though the meiofauna, especially foraminifera,
appears to be less sensitive to low dissolved oxygen (DO) concentrations
than the macrofauna (e.g. Josefson and Widbom, 1988). Many foraminiferal
taxa are able to withstand seasonal hypoxia–anoxia (see Koho et al., 2012,
for a review), and consequently they can play a major role in carbon cycling in
ecosystems affected by seasonal low-oxygen concentrations (Woulds et al.,
2007). Anoxia is often accompanied by free sulfide (H2S) in pore
and/or bottom waters (e.g. Jørgensen, 1982; Seitaj et al., 2015), which
is considered very harmful for the benthic macrofauna (Wang and Chapman,
1999). Neutral molecular H2S can diffuse through cellular membranes and
inhibits the functioning of cytochrome c oxidase (a mitochondrial enzyme
involved in ATP production), finally inhibiting aerobic respiration
(Nicholls and Kim, 1982; Khan et al., 1990; Dorman et al., 2002).
Lake Grevelingen (southwestern Netherlands) is a former branch of the
Rhine–Meuse–Scheldt estuary, which was closed in its eastern part
(riverside) by the Grevelingen Dam in 1964 and in its western part (seaside)
by the Brouwers Dam in 1971. The resulting saltwater lake, with a surface of
115 km2, is one of the largest saline lakes in western
Europe. Lake Grevelingen is characterised by a strongly reduced circulation
(even after the construction of a small sluice in 1978) with a strong
thermal stratification occurring in the main channels in summer, leading to
seasonal bottom-water hypoxia–anoxia in late summer and early autumn
(Bannink et al., 1984). This situation results in a rise of the H2S
front in the uppermost part of the sediment, sometimes up to the
sediment–water interface.
These observations especially concern the Den Osse Basin (i.e. one of the
deeper basins, maximum depth 34 m; Hagens et al., 2015), which has been
intensively monitored over the last decades, so that a large amount of
environmental data are available (e.g. Wetsteijn, 2011; Donders et al.,
2012). The annual net primary production in the Den Osse Basin (i.e. 225 g C m-2 yr-1; Hagens et al., 2015) is comparable to other estuarine
systems in Europe (Cloern et al., 2014). However, there is almost no
nutrient input from external sources; thus primary production is largely
based on autochthonous recycling (> 90 %; Hagens et al.,
2015), both in the water column and in the sediment, with a very strong
pelagic–benthic coupling (de Vries and Hopstaken, 1984). The benthic
environment is characterised by the presence of two antagonistic groups of
bacteria, with contrasting seasonal population dynamics (i.e. cable bacteria
in winter–spring and Beggiatoaceae in autumn–winter), which have a profound impact on all
biogeochemical cycles in the sediment column (Seitaj et al., 2015;
Sulu-Gambari et al., 2016a, b). The combination of hypoxia–anoxia with
sulfidic conditions, which is rather unusual in coastal systems without
external nutrient input, and the activity of antagonistic bacterial
communities makes Lake Grevelingen a very peculiar environment. In the Den
Osse Basin, seasonal anoxia coupled with the presence of H2S at or very
close to the sediment–water interface occurs in summer (i.e. between
July–September). However, euxinia (i.e. diffusion of free H2S in the
water column) does not occur, because of cable bacterial activity (Seitaj et
al., 2015).
Although the tolerance of foraminifera towards low DO contents and long-term
anoxia (from weeks to 10 months) has been well documented for many species
from different types of environments in laboratory culture (e.g. Moodley and
Hess, 1992; Alve and Bernhard, 1995; Bernhard and Alve, 1996; Moodley et
al., 1997; Duijnstee et al., 2003, 2005; Geslin et al., 2004, 2014; Ernst et al., 2005; Pucci et al., 2009; Koho et al., 2011) as well as in field studies (e.g. Piña-Ochoa et al., 2010b;
Langlet et al., 2013, 2014), their tolerance of free H2S is still
debated. In the vast majority of previous studies, no decrease in the total
abundances of living foraminifera (i.e. strongly increased mortality) was
observed during anoxic events. Unfortunately, studies on foraminiferal
response in systems affected by seasonal hypoxia–anoxia with sulfidic
conditions are still very sparse. The few available observations are not
conclusive, but they suggest that H2S could be toxic for foraminifera even
on fairly short timescales (Bernhard, 1993; Moodley et al., 1998b; Panieri
and Sen Gupta, 2008; Langlet et al., 2014).
To our knowledge, all earlier studies show that the foraminiferal response
to hypoxia–anoxia is species-specific (e.g. Bernhard and Alve, 1996; Ernst
et al., 2005; Bouchet et al., 2007; Geslin et al., 2014; Langlet et al.,
2014). However, this species-specific response generally follows the same
scheme (usually decrease in density, reduction of growth and/or
reproduction), with different response intensities. Duijnstee et al. (2005)
suggested that oxic stress leads to an increased mortality and inhibited
growth and reproduction. The suggestion of inhibited growth is supported by
LeKieffre et al. (2017), who observed that the morphospecies Ammonia tepida (probably
Ammonia sp. T6) showed minimal or no growth under anoxia. Conversely, Geslin et al. (2014) and Nardelli et al. (2014) suggested that, in the same morphospecies,
reproduction was strongly reduced, but growth would not be affected by
hypoxic and/or short anoxic events. Additionally, under low-oxygen
conditions, some species are able to shift to anaerobic metabolism (i.e.
denitrification; Risgaard-Petersen et al., 2006; Piña-Ochoa et al.,
2010a), to sequester chloroplast (i.e. kleptoplastidy; Jauffrais et al.,
2018), to associate with bacterial symbionts (Bernhard et al., 2010) or to
enter into a state of dormancy (Ross and Hallock, 2016; LeKieffre et al.,
2017).
The highly peculiar environmental context of Lake Grevelingen offers an
excellent opportunity to study this still poorly known aspect of
foraminiferal ecology.
The conventional method to discriminate between live and dead foraminifera
uses Rose Bengal, a compound which stains proteins (i.e. organic matter).
This method was proposed for foraminifera by Walton (1952) and is based on
the assumption that “the presence of protoplasm is positive indication of a living or very recently dead organism”. The author already noted that this assumption
implied that the rate of degradation of organic material should be
relatively high. Previous studies of living benthic foraminifera in
environments subjected to hypoxia–anoxia were almost all based on Rose
Bengal-stained samples (e.g. Gustafsson and Nordberg, 1999, 2000; Duijnstee
et al., 2004; Panieri, 2006; Schönfeld and Numberger, 2007; Polovodova
et al., 2009; Papaspyrou et al., 2013). However, foraminiferal protoplasm
may remain stainable from several weeks to months after their death (Corliss
and Emerson, 1990), especially under low dissolved oxygen concentrations
where organic matter degradation may be very slow (Bernhard, 1988; Hannah
and Rogerson, 1997; Bernhard et al., 2006). The Rose Bengal staining method
is therefore not suitable for studies in environments affected by
hypoxia–anoxia. Consequently, the results of foraminiferal studies in
low-oxygen environments based on this method have to be considered with
reserve. In order to avoid this problem, we used CellTracker™
Green (CTG) to recognise living foraminifera. CTG is a fluorescent probe
which marks only living individuals with cytoplasmic (i.e. enzymatic)
metabolic activity (Bernhard et al., 2006). Since metabolic activity stops
after the death of the organism, CTG should give a much more accurate
assessment of the living assemblages at the various sampling times and
thereby avoid overestimation of the live foraminiferal abundances.
In this study, samples were collected in August and November 2011 and then
every month through the year 2012, at two different stations in the Den Osse
Basin, with two replicates dedicated to foraminifera. The two stations were
chosen in contrasted environments regarding water depth (34 and 23 m,
respectively) and duration of seasonal hypoxia–anoxia and sulfidic
conditions. Living foraminiferal assemblages were studied in the uppermost
sediment and size distributions were determined in order to get insight into
the possible moment(s) of reproduction or accelerated growth in test size.
The seasonal variability study of the foraminiferal community allows us (1) to better understand the foraminiferal tolerance of seasonal hypoxia–anoxia
with the presence of free H2S in their microhabitat and (2) to obtain
information about the responses of the various species to adverse
conditions. This knowledge will be useful for the development of indices
assessing environmental quality (i.e. biomonitoring) and may also improve
palaeoecological interpretations of coastal records (e.g. Murray, 1967;
Gustafsson and Nordberg, 1999).
Material and methodsStudied area – environmental settings in the Den Osse Basin
Lake Grevelingen is a part of the former Rhine–Meuse–Scheldt estuary, in the
southwestern Netherlands. This former estuarine branch was turned into an
artificial saltwater lake during the Delta Works project. In Lake
Grevelingen, the water circulation is strongly limited by the construction
of dams (in the early 1970s) and only a small sluice allows water exchanges
with open seawater (i.e. very weak hydrodynamics). In the lake,
development of bottom-water hypoxia–anoxia occurs in the deepest part of the
basin in summer (i.e. July–September) to early autumn (i.e.
October–December; Bannink et al., 1984; Hagens et al., 2015). In the
literature, the terminology and threshold values used to describe oxygen
depletion are highly variable (e.g. oxic, dysoxic, hypoxic, suboxic,
microxic, postoxic; see Jorissen et al., 2007; Altenbach et al., 2012). In
this study we defined hypoxia as a concentration of oxygen < 63 µmol L-1 (1.4 mL L-1 or 2 mg L-1) whereas anoxia is
defined as no detectable oxygen (following Rabalais et al., 2010).
In Den Osse Basin, the nutrient input from external sources is very low and
pelagic–benthic coupling is essential, as already noted by de Vries and
Hopstaken (1984). In 2012, phytoplankton blooms occurred in April–May and
July (Hagens et al., 2015) in response to the increasing solar radiation and
nutrient availability in the water column following organic matter recycling
in winter. This led to an increased food availability in the benthic
compartment in the same periods. In general, Chl a concentrations in Den Osse
Basin are below 10 µg L-1, excluding very short peaks during
blooms in April–May and July which did not exceed 30 µg L-1 in
2012 (Hagens et al., 2015). Thermal stratification of the water column and
increased oxygen consumption due to organic matter input (i.e. from
phytoplankton blooms) are both responsible for the development of seasonal
bottom-water hypoxia–anoxia in summer (i.e. July–September). Although
euxinia (i.e. the presence of free H2S in the water column) does not
occur in the Den Osse Basin due to cable bacterial activity in winter, free
H2S is present in the uppermost layer of the sediment in summer (Seitaj
et al., 2015). Summarising, in the benthic ecosystem, increased food
availability in summer is counterbalanced by strongly decreasing oxygen
contents, sometimes accompanied by the presence of free sulfides in the
topmost sediment.
Field sampling
The two studied sites are located along a depth gradient in the Den Osse
Basin of Lake Grevelingen. Both station 1 (51∘44.834′ N,
3∘53.401′ E) and station 2 (51∘44.956′ N, 3∘53.826′ E) are located in the main channel, at 34 and 23 m depth,
respectively (Fig. 1).
Map of Lake Grevelingen showing the
location of the two sampled stations in the Den Osse Basin (red star). The
transversal section of the Den Osse Basin (top right) shows the depth at
which station 1 (S1) and station 2 (S2) were sampled (34 and 23 m depth,
respectively). This figure was modified from Sulu-Gambari et al. (2016b).
Measurements of bottom-water oxygen (BWO) concentrations were performed at 2 m above the sediment–water interface and are from Donders et al. (2012),
whereas the data for 2012 were published in Hagens et al. (2015). Sediment
cores were collected monthly in 2012 using a single core gravity corer
(UWITEC, Austria) using PVC core liners (6 cm inner diameter, 60 cm length).
All cores were inspected upon retrieval and only visually undisturbed
sediment cores were used for further analysis (Seitaj et al., 2017). Oxygen
penetration depth (OPD) and depth of free H2S detection were determined
by Seitaj et al. (2015) using profiling microsensors for station 1. The
data for station 2 (Supplement Table S1) were acquired similarly and
during the same cruises but never published; for further details about the
sampling method, see Seitaj et al. (2015).
Two replicate sediment cores dedicated to the foraminiferal study were
sampled in August and November 2011 using the same gravity corer (UWITEC,
Austria) and then monthly throughout the year 2012 at the same sampling time
as for BWO concentration and OPD and H2S measurements in the sediment
(see Seitaj et al., 2015). Consequently, for 2012 at stations 1 and 2, OPD
and H2S were measured in the sediment column at the same time as
foraminifera were sampled (Seitaj et al., 2015). For each replicate, the
uppermost centimetre (0–1 cm) of the core was then transferred on board in
a vial of 250 mL, and 30 mL of seawater (at the same temperature as in situ) was
added to the vial. Then we labelled the samples with
CellTracker™ Green CMFDA (CTG, 5-chloromethylfluorescein
diacetate, final concentration of 1 µmol L-1 following Bernhard
et al., 2006) and slowly agitated manually to allow the CTG diffusion in the
whole sample. Samples were then fixed in 5 % sodium-borate-buffered
formalin after 24 h of incubation in the dark.
Sample treatment
All samples were sieved over 315, 150 and 125 µm meshes, and
foraminiferal assemblages were studied in all three size fractions.
Individuals were picked wet under an epifluorescence stereomicroscope
(Olympus SZX12, light fluorescent source Olympus URFL-T, excitation/emission
wavelengths: 492 nm/517 nm) and placed on micropalaeontological slides. Only
specimens that fluoresced brightly green were considered living and were
identified to the (morpho)species level when possible. Since picking
foraminifera under an epifluorescence stereomicroscope is particularly
time-consuming, we decided to study samples only every 2 months for the
year 2012. At a later stage, in view of the large differences in
foraminiferal abundances between the samples of September and November 2012
at station 2, we decided to study the October and December 2012 samples as
well for this station. The sampling dates investigated in this study are
listed in Table 1.
Sampling dates of the samples which were investigated
for living foraminifera for stations 1 and 2. X: one core investigated; O: no core investigated.
YearMonthDayStation 1Station 22011Aug22X XX X2011Nov15X XX X2012Jan23X XX X2012Mar12X XX X2012May30X XX X2012Jul24X XX X2012Sep20X XX X2012Oct18OX X2012Nov2X XX X2012Dec3OX X
Abundances were then standardised to a volume of 10 cm3. The abundances
of living foraminifera for each sampling time and replicate are listed in
Tables S2 and S3. The mean abundance and standard deviation
(x‾±SD) for the two replicates for each sampling date were
calculated for both the total living assemblage and the individual species,
as an indication of spatial patchiness.
Taxonomy of dominant species
Four dominant species (> 1 % of the total assemblage) were
present in our material: Ammonia sp. T6, Elphidium magellanicum (Heron-Allen and Earland, 1932), Elphidium selseyense
(Heron-Allen and Earland, 1911) and Trochammina inflata (Montagu, 1808). As we identified these
species on the basis of morphological criteria, we will use them as
“morphospecies”.
Concerning the genus Ammonia, two living specimens collected at Grevelingen station 1 were molecularly identified (by DNA barcoding) as phylotype T6 by Bird et
al. (2019). At the same site, we genotyped seven other living Ammonia specimens,
which were all T6. Their sequences were deposited in GenBank (accession
numbers MN190684 to MN190690), and Supplement Fig. S1 shows scanning
electron microscope (SEM) images of the spiral side and of the penultimate
chamber at 1000× magnification for four individuals. A morphological
screening based on the criteria proposed by Richirt et al. (2019) confirmed
that T6 accounts for the vast majority (> 98 %) of Ammonia
individuals, whereas phylotypes T1, T2, T3 and T15 are only present in very
small amounts (Table S3).
The specimens of Elphidium magellanicum were identified exclusively on the basis of morphological
criteria, as there are no molecular data available yet. This morphospecies,
although rare, is regularly recognised in Boreal and Lusitanian provinces of
Europe (e.g. Gustafsson and Nordberg, 1999; Darling et al., 2016; Alve et
al., 2016). However, as the type species was described from the Strait of Magellan
(Southern Chile), the European specimens may represent a different
species and further studies involving DNA sequencing of both populations are
needed to confirm or disprove this taxonomic attribution (see Roberts et al.,
2016).
Elphidium selseyense has often been considered an ecophenotype of Elphidium excavatum (Terquem, 1875) and has
been identified as E. excavatum forma selseyensis (e.g. Feyling-Hanssen, 1972; Miller et al., 1982).
Four living specimens were already sampled for DNA analysis at station 1 and
were all identified as the species E. selseyense (phylotype S5, Darling et al., 2016). We
only observed minor morphological variations in our material, especially
concerning the number of small bosses in the umbilical region, which we
considered to be intraspecific variability. Consequently, we identified all our
specimens as E. selseyense.
The specimens attributed to Trochammina inflata were also identified exclusively on the basis
of morphological criteria, as no molecular data are available yet.
Size distribution measurement
In order to detect periods of increased growth and/or reproduction, size
measurements were performed on all samples of 2012. The measurements were
made for all species (4176 individuals for station 1 and 19624 individuals
for station 2), and trochospiral species were all orientated spiral side up
prior to measurements. High-resolution images (3648 pixels × 2736 pixels) of all
micropalaeontological slides were taken with a stereomicroscope (Leica S9i,
10× magnification) and individual measurements were processed using ImageJ
software (Schneider et al., 2012, Fig. S2).
Each individual was isolated (Fig. S2) and its maximum
diameter was measured (i.e. Feret's diameter). We represented all size
distributions using histograms with 20 µm classes (the best
compromise between the total number of individuals and the size range
(Fig. S3). As we only examined the size fractions
>125 µm, our analysis mainly concerns adult specimens
and does not include juveniles. This limitation should be kept in mind when
interpreting the results.
Assuming that the size distribution was a sum of Gaussian curves, each of
them representing a cohort, we tried to identify the approximate mode for
the Gaussian curves (i.e. cohorts) using the changes in slope (i.e.
inflexion points) of the second-order derivative of the total size
distribution (Gammon et al., 2017). Unfortunately, this tentative attempt to
distinguish cohorts by using a deconvolution method was not conclusive. The
main problem was the lack of information concerning individuals smaller than
125 µm, so that our size distributions were systematically skewed toward small individuals. Because the identification of
individual cohorts was not successful, a study of population dynamics was
not possible. For this reason, the data are only shown in Figs. S2 and S3. Nevertheless, the size
distribution data give some clues concerning the possible moment(s) of
reproduction or intensified test growth for the different species.
Encrusted forms of E. magellanicum
In our samples, we found abundant encrusted forms of E. magellanicum at station 1 (May 2012) and station 2 (May, July, September and December 2012, Fig. 2). Most
individuals were totally encrusted (Fig. 2a), others only partly (Fig. 2b).
These crusts were hard, firmly stuck to the shell (difficult to remove with
a brush), thin (Fig. 2c–e) and rather coarse. In order to determine if the
crust matrix is constituted of carbonate, we placed some specimens in
microtubes and exposed them to 0.1 M of EDTA (ethylenediaminetetraacetic
acid) diluted in 0.1 M cacodylate buffer (acting as a carbonate chelator).
After an exposition of 24 h, we checked under a stereomicroscope if the crust
was still cohesive (no carbonate in the crust) or was disaggregated (crust
contains carbonate).
SEM images of fully encrusted specimen (a), partially encrusted specimen (b) and crushed encrusted specimen of Elphidium magellanicum(c). Note the
thinness of the crust and the spinose structures in (d) and (e).
ResultsTotal abundances of foraminiferal assemblages
Averaged total abundances varied between 1.1±1.5 and 449.9±322.1 ind. 10 cm-3 for station 1 and between 91.1±25.0 and
604.8±3.5 ind. 10 cm-3 for station 2 (Fig. 3 and Table 2).
For every studied month, the total density was higher at station 2 than at
station 1. The seasonal succession is very different between the two sites
(Fig. 3). Station 1 shows very low total foraminiferal abundances for most
months, contrasting with much higher densities in May and July. Conversely,
station 2 shows high total foraminiferal abundances throughout the year,
with somewhat lower values in November 2011 and October and November 2012
(Fig. 3).
The grey bars represent the living foraminiferal
abundances for the two replicates. The mean abundances (diamonds) and
standard deviations (black error bars) were calculated for the two
replicates for stations 1 (34 m depth, a) and 2 (23 m depth, b). All abundance values are for the 0–1 cm layer and were standardised
to 10 cm3. Months where foraminiferal communities were investigated are
indicated in bold (excluding October and December at station 1).
Mean living foraminiferal absolute (ind. 10 cm-3)
and relative abundances (percentage of the total fauna, in parentheses) of
the dominant species. Last column: absolute abundance of the total fauna.
At station 1, almost no individuals were present in August (x‾=3.4±1.3) and November 2011 (x‾=1.1±1.5). In 2012, total
abundances were very low in January (x‾=11.5±9.3), showed a
slight increase in March (x‾=62.1±19.3) and reached a maximal
abundance in May (x‾=449.9±322.1). Total abundances then
progressively decreased from May to September (x‾=34.0±17.0)
and almost no foraminifera were present in November (x‾=1.6±0.3).
At station 2, total abundances were comparatively low in August and November 2011 (x‾=174.0±48.0 and x‾=128.7±25. ind. 10 cm-3, respectively). In 2012, total abundances were relatively high and
stable from January to September (between x‾=523.6±30.7 and
x‾=604.8±3.5), then decreased in October (x‾=211.5±8.0) and November (x‾=91.1±25.3), and finally
increased again in December (x‾=377.9±38.8).
SEM images of Elphidium selseyense in lateral (a) and peripheral (b)
views; Elphidium magellanicum in lateral (c) and peripheral (d) views; Ammonia sp. T6 in spiral (e),
peripheral (f) and umbilical (g) views; and Trochammina inflata in spiral (h), peripheral (i) and umbilical (j) views. All scale bars are 50 µm.
Dominant species
At station 1, the major species were, in order of decreasing abundances,
Elphidium selseyense (Fig. 4a–b), Elphidium magellanicum (Fig. 4c–d) and Ammonia sp. T6 (Fig. 4e–g). In Fig. 4, we added
Trochammina inflata (Fig. 4h–j) to facilitate comparison with station 2, where this species is
among the dominant ones. The “other species” account only for 2.2 % of
the total assemblage at station 1. The fact that they are well represented
in some months (e.g. 26.3 % of the assemblage in August 2011) is due to
the extremely low number of individuals (see Fig. 3 and Table 2). At station 2, the dominant species, in order of decreasing abundances, were E. selseyense, Ammonia sp. T6,
E. magellanicum and T. inflata (Table 2). Here, “other species” account only for 2.6 % of the
total assemblage. Whereas E. selseyense and E. magellanicum were dominant species at both stations, both
Ammonia sp. T6 and T. inflata were present in much higher abundances at station 2 compared to
station 1, where the latter species was almost absent (Figs. 5–6).
The bars represent the living foraminiferal
abundances for the two replicates for Elphidium selseyense(a), Elphidium magellanicum(b), Ammonia sp. T6 (c) and Trochammina inflata(d) at station 1 in 2011 and 2012. The mean abundances (diamonds)
and standard deviations (black error bars) were calculated for the two
replicates. All abundance values are for the 0–1 cm layer and were standardised
to 10 cm3. Months when foraminiferal communities were investigated are
indicated in bold. Scales were chosen in order to facilitate comparison with
station 2.
The bars represent the living foraminiferal
abundances for the two replicates for Elphidium selseyense(a), Elphidium magellanicum(b), Ammonia sp. T6 (c)
and Trochammina inflata(d) at station 2 in 2011 and 2012. The mean abundances (diamonds)
and standard deviations (black error bars) were calculated for the two
replicates. All abundances values are for the 0–1 cm layer and were standardised
to 10 cm3. Months when foraminiferal communities were investigated are
indicated in bold. Scales were chosen in order to facilitate comparison with
station 1.
At station 1, only some very scarce individuals of E. selseyense were observed in August
and November 2011 (Fig. 5 and Table 2). In 2012, E. selseyense abundances were very low
in January and started to increase in March (x‾=23.9±6.8),
reaching maximal values in May (x‾=336.5±275.8). In July, values
for E. selseyense were still high (x‾=162.0±121.5) and further decreased
until an almost total absence in November 2012. No specimen of E. magellanicum was observed
in 2011 (Fig. 5 and Table 2). The abundance of E. magellanicum was very low in January
2012, started to increase in March (x‾=21.6±11.0), reaching
maximal values in May (x‾=96.4±47.3), and then strongly decreased
in July (x‾=3.7±0.3). The species was absent from samples in
September and November 2012. Ammonia sp. T6 was almost absent in August and November 2011 and present with very few specimens in January 2012 (x‾=3.2±3.5). Maximum abundances were reached between March and July 2012
(ranging between x‾=9.2±6.5 and x‾=12.9±1.3).
Then abundances rapidly decreased until the species was almost absent in
November. Trochammina inflata was absent in 2011 and was only present in very low abundances
from January to May and in September 2012.
At station 2, the two dominant species were E. selseyense and Ammonia sp. T6, which together
always represented at least 70 % of the total assemblage (Fig. 6 and
Table 2). These two species showed a different seasonal pattern over the
considered period. Abundances of E. selseyense were comparable in August (x‾=74.8±29.8) and November 2011 (x‾=52.3±27.0) and then showed
a progressive increase until a maximum in September 2012 (x‾=365.5±70.3). Abundances then showed a sharp decrease in October and
November (respectively x‾=98.7±8.5 and x‾=30.9±2.3) to increase again in December (x‾=252.2±41.0). For
Ammonia sp. T6, abundances strongly increased between November 2011 (x‾=60.8±1.5) and January 2012 (x‾=226.2±52.3) and then
progressively decreased until the end of 2012 (x‾=48.1±26.0
in November 2012). Trochammina inflata showed an analogous pattern to Ammonia sp. T6. Abundances
strongly increased between November 2011 (x‾=11.8±1.8) and
January 2012 (x‾=121.5±29.8) and then progressively
decreased until very low abundances in November (x‾=3.7±3.0).
E. magellanicum was completely absent in August and November 2011, almost absent in January
2012 (x‾=0.9±0.3), and then suddenly increased until a maximum
of x‾=116.0±6.5 in May. Abundances stayed relatively high in
July (x‾=37.8±2.5) and September (x‾=72.0±35.8) and then drastically decreased until minimum numbers in October and
November. Finally, like all other species, E. magellanicum abundances increased again in
December (x‾=25.5±13.0).
Encrusted forms of Elphidium magellanicum
After exposition to 0.1 M of EDTA diluted in 0.1 M cacodylate buffer, the
crusts remained cohesive, indicating that they do not consist of carbonate
and suggesting that they are composed of sediment particles cemented by an
organic matrix.
At station 1, encrusted forms of E. magellanicum were present in moderate proportions in
May (26.8 % of the total E. magellanicum population, Fig. 7) and July (47.6 %); the
species disappeared thereafter. At station 2, encrusted forms strongly
dominated the E. magellanicum population from May (72.3 %) to December (88.0 %, Fig. 7).
Mean abundances (ind. 10 cm-3) of non-encrusted
(grey) and encrusted forms (black) of Elphidium magellanicum in 2012, at stations 1 (a) and 2 (b), with proportion of encrusted forms above each bar (%).
Investigated months are indicated in bold.
DiscussionTolerance of foraminiferal communities towards anoxia and free sulfide
At station 1, bottom waters were hypoxic in July 2012 and became anoxic in
August (Fig. 8). Both in July and in August, oxygen penetration into the
sediment was null, whereas it was 0.7±0.1 mm depth in September. In
all 3 months (July to September 2012), sulfidic conditions were
observed very close to the sediment–water interface (1 mm or less, Fig. 8
and Table S1). In view of these results, the duration of anoxic
and sulfidic conditions in the uppermost sediment layer can be estimated as
1 to 2 months (in July and August, Fig. 8).
The top panel represents bottom-water oxygen concentrations
(µmol L-1) in 2011 and 2012 at station 1, from Donders et al. (2012) and Seitaj et al. (2017). The grey horizontal dotted line indicates
the hypoxia limit (63 µmol L-1). The middle panel represents the
depth (mm) distribution of the oxic zone (blue), absence of oxygen and
sulfides (orange), and sulfidic zone (black) within the sediment in 2012,
from Seitaj et al. (2015). The bottom panel shows the total living
foraminiferal abundances for both replicates (grey bars), mean abundances
(diamonds) and standard deviations (black error bars) calculated for the two
replicates, for all investigated months (in bold) in 2011 and 2012.
After the strong increase in foraminiferal densities in May 2012, there was
a decrease starting in July, leading to a near absence of foraminifera at
station 1 in November (Fig. 8). The most probable cause of the strong
decline of the foraminiferal community appears to be a prolonged presence of
sulfides in the foraminiferal microhabitat. However, the fact that
foraminiferal abundances reached almost zero only in September (about 2
months after the first occurrence of anoxic and sulfidic conditions in the
upper sediment, in July) suggests that the presence of H2S did not
cause instantaneous mortality, but that the disappearance of the
foraminiferal community was a delayed response, probably caused by inhibited
reproduction and, eventually, increased mortality. Inhibited reproduction
has previously been suggested as a response to hypoxic–short anoxic (Geslin
et al., 2014) and sulfidic conditions (Moodley et al., 1998b).
Such a time lag between a change in foraminiferal abundances and changes in
environmental parameters affecting reproduction and/or growth of
foraminifera has been suggested previously by Duijnstee et al. (2004). These
authors highlighted that the density patterns of some foraminiferal species
showed a higher correlation with measured environmental parameters (e.g.
oxygenation or temperature) when a time lag of about 3 months was
applied.
For 2011, at station 1, no pore-water O2 and H2S measurements are
available. However, severe hypoxia was observed in the bottom waters from
May to August, with anoxia in June 2011 (Fig. 8). We therefore assume that,
like in 2012, anoxic and probably co-occurring sulfidic conditions were
responsible for the very low standing stocks in August and November 2011 and
January 2012.
Our observations confirm the suggestion in previous studies that the
foraminiferal community is severely affected by a long-term presence of
H2S in its habitat but does not show instant mortality. In fact, after
a 66 d incubation in euxinic conditions (a maximum of 11.9±0.4µmol L-1 of H2S in the overlying water) of foraminiferal
assemblages collected at a 19 m deep site in the Adriatic Sea, Moodley et
al. (1998a) found a strong decrease in the total density of Rose Bengal-stained foraminifera. After 21 d, living specimens were still observed,
whereas after 42 and 66 d, the live checks (based on protoplasm movement)
gave only negative results. Langlet et al. (2013, 2014) performed an in situ
experiment with closed benthic chambers at a 24 m deep site in the Gulf of
Trieste, in the Adriatic Sea. They observed a decrease in living
foraminiferal density (labelled with CTG), but they also found that almost all
species survived after 10 months of anoxia and periodically co-occurring
H2S in the sediment and overlying water. However, the duration of
sulfidic conditions, which was estimated to be several weeks, could not be
assessed precisely (Metzger et al., 2014). The suggestion that short
exposure to euxinic conditions is not directly lethal for foraminifera is
confirmed by the experimental results of Bernhard (1993), who found that
foraminiferal activity (as determined by ATP content) was not significantly
affected after 30 d exposure to euxinia (32.6±8.6 % of active
individuals, n=174 in control conditions versus 29.5±6.2 %,
n=173 in sulfidic conditions).
After the 2011 hypoxia–anoxia, standing stocks at station 1 only started to
increase in March 2012, indicating a very long recovery time (about 6 months) of the foraminiferal faunas after a temporary near-extinction due to
anoxic and sulfidic conditions. This confirms observations of relatively
long recovery times in the literature (e.g. Alve, 1995, 1999; Gustafsson and
Nordberg, 2000; Hess et al., 2005). For instance, Gustafsson and Nordberg (1999) showed that in the Koljö Fjord, at comparable water depths,
foraminiferal populations responded with increased densities only 3
months after a renewal of sea-floor oxygenation following hypoxic conditions
in the bottom waters. However, in that case, the disappearance of the
foraminiferal population was only partial and not nearly as complete as in our
study.
At station 2, in 2012, hypoxia was only observed in August, when the OPD was
zero, and sulfidic conditions were observed in the superficial sediment
(i.e. from 0.4±0.2 mm downwards, Fig. 9, Table S1).
Both in July and in September, oxygen penetrated more than 1 mm into
the sediment (1.3±0.4 and 1.2±0.2 mm, respectively).
However, free H2S was still detected at about 1 mm depth in
the sediment (1.1±0.8 mm in July and 0.8±0.2 mm in
September). Although the sampling plan does not allow us to be very precise
about the duration of anoxic and sulfidic conditions, we can estimate their
duration to be 1 month or less (Fig. 9).
The top panel represents bottom-water oxygen concentrations
(µmol L-1) in 2011 and 2012 at station 2, from Donders et al. (2012) and Seitaj et al. (2017). The grey horizontal dotted line indicates
the hypoxia limit (63 µmol L-1). The middle panel represents the
depth (mm) distribution of the oxic (blue), suboxic (orange, absence of
oxygen and sulfides) and sulfidic (black) zones within the sediment in 2012. The bottom panel shows the total living foraminiferal abundances for
both replicates (grey bars), mean abundances (diamonds) and standard
deviations (black error bars) calculated for the two replicates, for all
investigated months (in bold) in 2011 and 2012.
Foraminiferal abundances showed a strong decrease in October and November 2012, about 2 months after the presence of anoxic and sulfidic conditions
in the topmost part of the sediment (Fig. 9). Like at station 1, this
temporal offset between the presence of anoxia–sulfidic conditions at
station 2 (in August) and the strong decrease in faunal densities may be
explained as a delayed response, mainly due to inhibited reproduction during
the anoxic–sulfidic event. If true, the mortality of adults did not
strongly increase in the months following the H2S production in the
uppermost sediment. Nevertheless, there was no replacement in the
> 125 µm fraction by growing juveniles, probably because
reproduction was interrupted when H2S was present in the foraminiferal
microhabitat. A renewed recruitment after the last stage of sulfidic
conditions somewhere in September would then explain why the faunal density
in the > 125 µm fraction increased again in December 2012
(Fig. S3).
In 2011, at station 2, bottom waters oscillated between hypoxic and oxic
conditions between May and August (Fig. 9). Although we have no measurements
of H2S in the pore waters for this year, it seems probable that
bottom-water hypoxia was accompanied by the presence of free H2S very
close to the sediment surface, strongly affecting the foraminiferal
communities. If we assume that, like in 2012, rich foraminiferal fauna was
present in May–July 2011 at both stations, the low faunal densities
observed in August and November 2011 could suggest that foraminifera may
have also shown a delayed response to sulfidic conditions in 2011.
It is interesting to note that the foraminiferal densities observed at
station 2 were lower in August 2011 than in July or September 2012. This may
be a consequence of the repetition of short hypoxic events in the
bottom water between May and August 2011 (probably associated with anoxia
and maybe H2S in the uppermost part of the sediment), which possibly
affected the foraminiferal community more substantially in 2011 than in
2012, when a hypoxic event was recorded in August only.
The important decrease in total standing stocks at station 2 in October and
November 2012 (Fig. 9) suggests that, in spite of the shorter duration of
anoxia and sulfide conditions (compared to station 1; 1 month or less
compared to 1 to 2 months), the foraminiferal faunas were still strongly
affected. However, at station 2, foraminiferal abundances increased again in
December 2012, suggesting a recovery time of about 2 months, which is
likely much shorter than at station 1, where standing stocks in the
> 125 µm fraction only increased 6 months after the
presence of anoxia and free sulfides.
Summarising, the foraminiferal communities of both stations 1 and 2 seem
strongly impacted by the anoxic and sulfidic conditions developing in the
uppermost part of the sediment in summer (i.e. July–September). However, at
station 1, where anoxic and sulfidic conditions lasted for 1 to 2
months, the response is much stronger, leading ultimately (in November) to
almost complete disappearance of the foraminiferal fauna. The delayed
response at both stations shows that instantaneous mortality was limited
and suggests that the decreasing standing stocks might rather be the result
of inhibited reproduction and, eventually, increased mortality. Recovery is
much faster at station 2 (about 2 months) than at station 1 (about 6
months), probably because at station 1 (in contrast to station 2) the
foraminiferal extinction was nearly complete, and the site had to be
recolonised (e.g. possibly by nearby sites or by the remaining few
individuals) after reoxygenation of the sediment. At station 2, a reduced
but significant foraminiferal community remained present, explaining the
faster recovery.
Species-specific response to anoxia, sulfide and food availability in
Lake Grevelingen
The comparison of the different seasonal patterns of the major species at
the two investigated stations allows us to draw some conclusions about
interspecific differences in the response to seasonal anoxic and sulfidic
conditions.
First, there is a clear faunal difference between the two stations. Station 1 is dominated by E. selseyense and E. magellanicum while at station 2 these two taxa are accompanied
by Ammonia sp. T6 and T. inflata. The latter species is almost absent at station 1, where
Ammonia sp. T6 is present with low densities. At first glance, the dominance of the
two Elphidium species at station 1 would suggest that they have a greater tolerance
of the seasonal anoxic and sulfidic conditions, which lasted much longer
there. It is interesting to note that the temporal evolution of standing
stocks at station 1 is different for the two Elphidium species. Elphidium magellanicum shows a strong drop in
absolute density in July 2012, at the onset of H2S presence in the
uppermost part of the sediment, whereas the diminution of E. selseyense is more
progressive and the species disappears almost completely only in November
(Fig. 5). This strongly suggests that E. magellanicum is more affected by increased
mortality than E. selseyense in response to the combined effects of anoxic and sulfidic
conditions. This hypothesis is confirmed by the patterns observed at station 2, where the drop in standing stocks in October–November is also more
drastic in E. magellanicum than in E. selseyense (Fig. 6).
As mentioned earlier, certain species of foraminifera can use an anaerobic
metabolism (i.e. denitrification; Risgaard-Petersen et al., 2006;
Piña-Ochoa et al., 2010a), sequester chloroplasts (i.e. kleptoplastidy;
Jauffrais et al., 2018), host bacterial symbionts (Bernhard et al., 2010) or
enter dormancy (Ross and Hallock, 2016; LeKieffre et al., 2017) to deal
with low-oxygen conditions. Concerning the species found in this study,
although the presence of intracellular nitrate was shown for Ammonia,
denitrification tests yielded negative results (Piña-Ochoa et al.,
2010a; Nomaki et al., 2014). Similarly, the presence of active symbionts was
previously suggested for Ammonia but never confirmed (Nomaki et al., 2016; Bernhard
et al., 2018). To our knowledge, denitrification or the presence of
bacterial symbionts was never shown for Elphidium either. In conclusion, a shift to
an alternative anaerobic metabolism or an association with bacterial
symbionts has never been shown conclusively for the dominant foraminiferal
species found in Lake Grevelingen.
The greater tolerance of E. selseyense towards low-oxygen conditions could be explained by the
fact that it is able to sequester chloroplasts from ingested diatoms and
keep them active for several days to weeks, in contrast to Ammonia sp. T6 (Jauffrais
et al., 2018). These active chloroplasts could serve as an alternative
source of oxygen and/or food through photosynthesis (Bernhard and Alve,
1996) or another metabolic pathway (Jauffrais et al., 2019) and thereby
increase the capability of this species to survive anoxic events. Although
sequestration of chloroplasts was never investigated for E. magellanicum, its abundant
spinose ornamentation in the umbilical region and in the vicinity of the
aperture (Fig. 4c–d) suggests that this species is capable of crushing diatom
frustules like some kleptoplastic species (Bernhard and Bowser, 1999; Austin
et al., 2005). Hagens et al. (2015) observed that the light penetration
depth in the Den Osse Basin never exceeded 15 m in 2012, and therefore
photosynthesis by kleptoplasts (Bernhard and Alve, 1996) appears unlikely
for both our aphotic stations (34 and 23 m depth). However, other
foraminifera from aphotic and anoxic environments such as deep fjords are
kleptoplastic and use these kleptoplasts for a yet unknown purpose
(Jauffrais et al., 2019).
Rather surprisingly, the drop in foraminiferal densities at station 2 in
October–November, which we interpreted as a delayed response to sulfidic
conditions, is less strong for Ammonia sp. T6 than for the two Elphidium species, suggesting
that this species is less affected. However, this does not agree with our
previous suggestion that the two Elphidium species would be more tolerant to anoxic
and sulfidic conditions. As already proposed by LeKieffre et al. (2017),
Ammonia seems to be able to deal with anoxia (up to 28 d, but with no sulfide)
by reducing its metabolic activity, but this ability was never shown for
Elphidium species. If E. selseyense and E. magellanicum are indeed unable to resist anoxia by reducing their
metabolism or by entering a dormancy state, this could explain their
stronger decrease in density at station 2 compared to Ammonia sp. T6.
Nevertheless, further studies about the ability and mechanisms of the two
Elphidium species to resist anoxic–sulfidic conditions are necessary.
Another remarkable observation is that Ammonia sp. T6 (and T. inflata) shows maximum
densities in January–March, contrasting with the two Elphidium species, which have
their density maxima later in the year (May–September). This temporal
offset could possibly be explained by a difference in preferential food
source, with food particles available in winter (January–March) being more
suitable for Ammonia sp. T6 (and T. inflata) and food particles available later in the
year, resulting from phytoplankton blooms, being more favourable for E. selseyense and E. magellanicum.
In our study, for E. selseyense (and E. magellanicum), the continuous presence of a high proportion of
small-sized specimens and progressively increasing densities between January
and September 2012 strongly suggest ongoing and continuous reproduction
(Fig. S3a). Continuous reproduction during the year has been
described earlier for different foraminiferal genera, such as Elphidium, Ammonia, Haynesina, Nonion and
Trochammina (e.g. Jones and Ross, 1979; Murray, 1983, 1992; Cearreta, 1988;
Basson and Murray, 1995; Gustafsson and Nordberg, 1999; Murray and Alve,
2000). Conversely, for Ammonia sp. T6, a decrease in densities coupled with a rapid
increase in overall test size between March and May 2012 (small sized
specimens remain present but in smaller proportions) could be indicative of
a period of reduced recruitment (Fig. S3b).
In fact, foraminifera exhibit a large range of feeding strategies, with
several species showing selective feeding with specific food particles
(Muller, 1975; Suhr et al., 2003; Chronopoulou et al., 2019). Hagens et al. (2015) reported that in Lake Grevelingen the phytoplankton composition was
different between April–May and July 2012. In April–May, the phytoplankton
bloom was mainly composed of the haptophyte Phaeocystis globose (Scherffel, 1899), whereas it
was dominated by the dinoflagellate Prorocentrum micans (Ehrenberg, 1834) in July. Elphidium was reported
to be able to feed on various food sources (e.g. diatoms, dinoflagellates,
green algae; Correia and Lee, 2002; Pillet et al., 2011). However, diatoms
are a major food source for kleptoplastic species (Bernhard and Bowser,
1999), such as E. selseyense (Jauffrais et al., 2018; Chronopoulou et al., 2019).
Ammonia spp. seem able to feed on very diverse food sources including microalgae,
diatoms, bacteria or even metazoans (Lee et al., 1969; Moodley et al., 2000;
Dupuy et al., 2010; Jauffrais et al., 2016; Chronopoulou et al., 2019).
Recently, Chronopoulou et al. (2019) showed different feeding preferences
for Ammonia sp. T6 and E. selseyense in intertidal environments in the Dutch Wadden Sea.
Although diatoms are ingested by both species (but much more by E. selseyense),
dinoflagellates were consumed by E. selseyense but not by Ammonia sp. T6. The latter species is
also capable of feeding on metazoans by active predation (Dupuy et al., 2010).
These observations suggest that at station 2 the different seasonal density
patterns of Ammonia sp. T6 and the two Elphidium species are not the consequence of a large
difference in tolerance of anoxia–sulfides, but rather a different
adjustment to the seasonal cycle of food availability. At station 1, the
very low densities of Ammonia sp. T6 could possibly be explained by a
recolonisation starting in January, when food conditions were favourable for
this taxon (as testified by the strong density increase in January 2012 at
station 2). However, once a more abundant pioneer population had developed
(in March–May), food conditions may have been no longer favourable for
Ammonia sp. T6, explaining why its density did not show a further increase.
Conversely, the food conditions may have become optimal for the two
Elphidium species, explaining their strong density increase between March and May
2012. If true, this would mean that the lower densities of Ammonia sp. T6 would not
be due to a lower resistance to anoxia and free sulfides, but rather due to
an unfavourable seasonal succession of food availability. Previous studies
already suggested that hypoxic–anoxic conditions coupled with increased food
input from autumnal phytoplankton blooms (composed of diatoms and
dinoflagellates) would favour the development of E. magellanicum (Gustafsson and Nordberg,
1999). The fact that also at station 2 this species was mainly observed
between March and September 2012 corroborates our conclusion of its
dependence on a specific food regime.
Finally, encrusted forms of E. magellanicum were observed at both stations from May until
the end of the year but were absent in the samples of March 2012. In view
of the fact that the crusts consist mainly of organic matter, the encrusted
individuals appear to be specimens with preserved feeding cysts. The precise
functions of cysts observed around foraminifera are not clear and include
feeding, reproduction, chamber formation, protection or resting (Cedhagen,
1996; Heinz et al., 2005). Concerning the cysts of E. magellanicum described here, very
similar observations have been made for Elphidium incertum at different locations (Norwegian
Greenland Sea and Baltic Sea in Linke and Lutze, 1993; Koljö Fjord in
Gustafsson and Nordberg, 1999; Kiel Bight in Polovodova et al., 2009). If we
assume that encrusted specimens indeed present the remains of feeding cysts, the
observation of abundant encrusted specimens corroborates our conclusion that
the surface water phytoplankton bloom in May 2012 (i.e. probably mainly
Phaeocystis globosa) provided a food source particularly well suited to the nutritional
preferences of this species.
Conclusions
In this study we examined the foraminiferal community response to different
durations of seasonal anoxia coupled with the presence of sulfide in the
uppermost layer of sediment at two stations in Lake Grevelingen. In both
stations investigated, foraminiferal communities are highly impacted by the
combination of anoxia and H2S in their habitat. The foraminiferal
response varied depending on the duration of adverse conditions and led to
a near extinction at station 1, where anoxic and sulfidic conditions were
present for 1 to 2 months, compared to a drop in standing stocks at
station 2, where these conditions lasted for 1 month or less. At both
sites, foraminiferal communities showed a 2-month delay in the response to
anoxic and sulfidic conditions, suggesting that the presence of H2S
inhibited reproduction, whereas mortality was not necessarily increased. The
duration of the subsequent recovery depended on whether the foraminiferal
community was almost extinct (station 1) or remained present with reduced
numbers (station 2). In the former case, 6 months were needed for faunal
recovery, whereas in the latter case, it took only 2 months. We
hypothesise that the dominance of E. selseyense and E. magellanicum at station 1 is not due to a lower
tolerance of Ammonia sp. T6 towards anoxic and sulfidic conditions, but is rather the
consequence of a different adjustment between the two Elphidium species and Ammonia sp. T6
with respect to the seasonal cycle of food availability.
Data availability
Raw data are available in the Supplement.
The supplement related to this article is available online at: https://doi.org/10.5194/bg-17-1415-2020-supplement.
Author contributions
BR, DL and JR produced the foraminiferal data. DS, AM and CPS
provided and interpreted geochemical data. MS provided, verified and
integrated all available genetic information concerning the foraminiferal
taxa of Lake Grevelingen. FJRM and CPS coordinated a much larger research
project concerning Lake Grevelingen, of which this foraminiferal study is a
part. They were also responsible for the foraminiferal sampling and provided
environmental data. FJJ designed the foraminiferal study and directed the
postdoctoral research of BR and, together with AM and MS, the PhD
thesis of JR. All authors contributed actively to the several successive
versions of the manuscript.
Competing interests
The authors declare that they have no conflict of interest.
Acknowledgements
We are very grateful to Sandra Langezaal for inviting us to study the
fascinating environments of the Grevelingenmeer. We acknowledge the support
of Pieter van Rijswijk, Mathilde Hagens, Anton Tramper and the crew of the R/V Luctor (Peter Coomans and Marcel Kristalijn) during the sampling campaigns. We are grateful to
Romain Mallet and the team of the SCIAM imaging facility at the University
of Angers. We acknowledge Jassin Petersen for his help with recovering some
of the environmental data and Thierry Jauffrais and Charlotte LeKieffre for
discussion about alternative metabolisms. This paper benefited from the
comments and suggestions of Laurie M. Charrieau and the two anonymous reviewers.
Financial support
This research has been supported by Rijkswaterstaat and the CNRS programme CYBER-LEFE (project AMTEP).
Review statement
This paper was edited by Hiroshi Kitazato and reviewed by Laurie M. Charrieau and two anonymous referees.
References
Altenbach, A. V., Bernhard, J. M., and Seckbach, J. (Eds.): Anoxia: evidence
for eukaryote survival and paleontological strategies, Springer, Dordrecht, 648 pp.,
2012.Alve, E.: Benthic foraminiferal distribution and recolonization of formerly
anoxic environments in Drammensfjord, southern Norway, Mar. Micropaleontol.,
25, 169–186, 10.1016/0377-8398(95)00007-N, 1995.Alve, E.: Colonization of new habitats by benthic foraminifera: a review,
Earth-Sci. Rev., 46, 167–185, 10.1016/S0012-8252(99)00016-1, 1999.
Alve, E. and Bernhard, J. M.: Vertical migratory response of benthic
foraminifera to controlled oxygen concentrations in an experimental
mesocosm, Mar. Ecol. Prog. Ser., 116, 137–151, ISSN: 0171-8630, 1995.Alve, E., Korsun, S., Schönfeld, J., Dijkstra, N., Golikova, E., Hess,
S., Husum, K., and Panieri, G.: Foram-AMBI: A sensitivity index based on
benthic foraminiferal faunas from North-East Atlantic and Arctic fjords,
continental shelves and slopes, Mar. Micropaleontol., 122, 1–12,
10.1016/j.marmicro.2015.11.001, 2016.Austin, H. A., Austin, W. E. N., and Paterson, D. M.: Extracellular cracking
and content removal of the benthic diatom Pleurosigma angulatum (Quekett) by
the benthic foraminifera Haynesina germanica (Ehrenberg), Mar.
Micropaleontol., 57, 68–73, 10.1016/j.marmicro.2005.07.002, 2005.Bannink, B. A., Van der Meulen, J. H. M., and Nienhuis, P. H.: Lake
grevelingen: From an estuary to a saline lake. An introduction, Neth. J. Sea
Res., 18, 179–190, 10.1016/0077-7579(84)90001-2, 1984.Basson, P. W. and Murray, J. W.: Temporal Variations in Four Species of
Intertidal Foraminifera, Bahrain, Arabian Gulf, Micropaleontology, 41,
69–76, 10.2307/1485882, 1995.Bernhard, J. M.: Postmortem vital staining in benthic foraminifera; duration
and importance in population and distributional studies, J. Foraminifer.
Res., 18, 143–146, 10.2113/gsjfr.18.2.143, 1988.Bernhard, J. M.: Experimental and field evidence of Antarctic foraminiferal
tolerance to anoxia and hydrogen sulfide, Mar. Micropaleontol., 20,
203–213, 10.1016/0377-8398(93)90033-T, 1993.Bernhard, J. M. and Alve, E.: Survival, ATP pool, and ultrastructural
characterization of benthic foraminifera from Drammensfjord (Norway):
response to anoxia, Mar. Micropaleontol., 28, 5–17,
10.1016/0377-8398(95)00036-4, 1996.Bernhard, J. M. and Bowser, S. S.: Benthic foraminifera of dysoxic
sediments: chloroplast sequestration and functional morphology, Earth-Sci.
Rev., 46, 149–165, 10.1016/S0012-8252(99)00017-3, 1999.Bernhard, J. M., Ostermann, D. R., Williams, D. S., and Blanks, J. K.:
Comparison of two methods to identify live benthic foraminifera: A test
between Rose Bengal and CellTracker Green with implications for stable
isotope paleoreconstructions, Paleoceanography, 21, PA4210,
10.1029/2006PA001290, 2006.Bernhard, J. M., Goldstein, S. T., and Bowser, S. S.: An ectobiont-bearing
foraminiferan, Bolivina pacifica, that inhabits microxic pore waters:
cell-biological and paleoceanographic insights, Environ. Microbiol., 12,
2107–2119, 10.1111/j.1462-2920.2009.02073.x, 2010.Bernhard, J. M., Tsuchiya, M., and Nomaki, H.: Ultrastructural observations
on prokaryotic associates of benthic foraminifera: Food, mutualistic
symbionts, or parasites?, Mar. Micropaleontol., 138, 33–45,
10.1016/j.marmicro.2017.09.001, 2018.Bird, C., Schweizer, M., Roberts, A., Austin, W. E. N., Knudsen, K. L.,
Evans, K. M., Filipsson, H. L., Sayer, M. D. J., Geslin, E., and Darling, K.
F.: The genetic diversity, morphology, biogeography, and taxonomic
designations of Ammonia (Foraminifera) in the Northeast Atlantic, Mar.
Micropaleontol., 155, 101726, 10.1016/j.marmicro.2019.02.001, 2019.Bouchet, V. M. P., Debenay, J.-P., Sauriau, P.-G., Radford-Knoery, J., and
Soletchnik, P.: Effects of short-term environmental disturbances on living
benthic foraminifera during the Pacific oyster summer mortality in the
Marennes-Oléron Bay (France), Mar. Environ. Res., 64, 358–383,
10.1016/j.marenvres.2007.02.007, 2007.
Cearreta, A.: Population dynamics of benthic foraminifera in the Santoña
estuary, Spain, Revue de Paleobiologie, 2, 721–724, ISSN:0253-6730, 1988.
Cedhagen, T.: Foraminiferans as food for cephalaspideans (Gastropoda:
Opisthobranchia), with notes on secondary tests around calcareous
foraminiferans, Phuket Marine Biological Center Special Publication, 16,
279–290, 1996.Chronopoulou, P.-M., Salonen, I., Bird, C., Reichart, G.-J., and Koho, K. A.:
Metabarcoding Insights Into the Trophic Behavior and Identity of Intertidal
Benthic Foraminifera, Front. Microbiol., 10, 1169,
10.3389/fmicb.2019.01169, 2019.Cloern, J. E., Foster, S. Q., and Kleckner, A. E.: Phytoplankton primary production in the world's estuarine-coastal ecosystems, Biogeosciences, 11, 2477–2501, 10.5194/bg-11-2477-2014, 2014.Corliss, B. H. and Emerson, S.: Distribution of rose bengal stained deep-sea
benthic foraminifera from the Nova Scotian continental margin and Gulf of
Maine, Deep-Sea Res. Pt. A, 37, 381–400,
10.1016/0198-0149(90)90015-N, 1990.
Correia, M. and Lee, J. J.: Fine structure of the plastids retained by the
foraminifer Elphidium excavatum (Terquem), Symbiosis, 32, 15–26,
ISSN: 03345114, 2002.Darling, K. F., Schweizer, M., Knudsen, K. L., Evans, K. M., Bird, C.,
Roberts, A., Filipsson, H. L., Kim, J.-H., Gudmundsson, G., Wade, C. M.,
Sayer, M. D. J., and Austin, W. E. N.: The genetic diversity, phylogeography
and morphology of Elphidiidae (Foraminifera) in the Northeast Atlantic, Mar.
Micropaleontol., 129, 1–23, 10.1016/j.marmicro.2016.09.001, 2016.de Vries, I. and Hopstaken, C. F.: Nutrient cycling and ecosystem behaviour
in a salt-water lake, Neth. J. Sea Res., 18, 221–245,
10.1016/0077-7579(84)90003-6, 1984.
Diaz, R. J. and Rosenberg, R.: Marine benthic hypoxia: a review of its
ecological effects and the behavioural responses of benthic macrofauna,
Oceanogr. Mar. Biol., 33, 245–303, 1995.Diaz, R. J. and Rosenberg, R.: Spreading Dead Zones and Consequences for
Marine Ecosystems, Science, 321, 926–929,
10.1126/science.1156401, 2008.
Donders, T. H., Guasti, E., Bunnik, F. P. M., and van Aken, H.: Impact van de
Brouwersdam op zuurstofcondities in de Grevelingen; reconstructies uit
natuurlijke sediment archieven, TNO-report TNO-060-UT-2011-02116, Utrecht, the Netherlands, 2012.Dorman, D. C., Moulin, F. J.-M., McManus, B. E., Mahle, K. C., James, R. A.,
and Struve, M. F.: Cytochrome Oxidase Inhibition Induced by Acute Hydrogen
Sulfide Inhalation: Correlation with Tissue Sulfide Concentrations in the
Rat Brain, Liver, Lung, and Nasal Epithelium, Toxicol. Sci., 65, 18–25,
10.1093/toxsci/65.1.18, 2002.Duijnstee, I., de Lugt, I., Vonk Noordegraaf, H., and van der Zwaan, B.:
Temporal variability of foraminiferal densities in the northern Adriatic
Sea, Mar. Micropaleontol., 50, 125–148,
10.1016/S0377-8398(03)00069-0, 2004.Duijnstee, I. A. P., Ernst, S. R., and van der Zwaan, G. J.: Effect of anoxia
on the vertical migration of benthic foraminifera, Mar. Ecol. Prog. Ser.,
246, 85–94, 10.3354/meps246085, 2003.Duijnstee, I. a. P., Nooijer, L. J. de, Ernst, S. R., and van
der Zwaan, G. J.: Population dynamics of benthic shallow-water foraminifera: effects of a
simulated marine snow event, Mar. Ecol. Prog. Ser., 285, 29–42,
10.3354/meps285029, 2005.Dupuy, C., Rossignol, L., Geslin, E., and Pascal, P.-Y.: Predation of mudflat
meio-macrofaunal metazoans by a calcareous foraminifer, Ammonia tepida (cushman, 1926), J.
Foraminifer. Res., 40, 305–312, 10.2113/gsjfr.40.4.305, 2010.Ernst, S., Bours, R., Duijnstee, I., and van der Zwaan, B.: Experimental
effects of an organic matter pulse and oxygen depletion on a benthic
foraminiferal shelf community, J. Foraminifer. Res., 35, 177–197,
10.2113/35.3.177, 2005.Feyling-Hanssen, R. W.: The Foraminifer Elphidium excavatum (Terquem) and
Its Variant Forms, Micropaleontology, 18, 337–354, 10.2307/1485012,
1972.Gammon, P. R., Neville, L. A., Patterson, R. T., Savard, M. M., and Swindles,
G. T.: A log-normal spectral analysis of inorganic grain-size distributions
from a Canadian boreal lake core: Towards refining depositional process
proxy data from high latitude lakes, Sedimentology, 64, 609–630,
10.1111/sed.12281, 2017.Geslin, E., Heinz, P., Jorissen, F., and Hemleben, C.: Migratory responses
of deep-sea benthic foraminifera to variable oxygen conditions: laboratory
investigations, Mar. Micropaleontol., 53, 227–243,
10.1016/j.marmicro.2004.05.010, 2004.
Geslin, E., Barras, C., Langlet, D., Nardelli, M. P., Kim, J.-H., Bonnin,
J., Metzger, E., and Jorissen, F. J.: Survival, Reproduction and
Calcification of Three Benthic Foraminiferal Species in Response to
Experimentally Induced Hypoxia, in: Approaches to Study Living Foraminifera:
Collection, Maintenance and Experimentation, edited by: Kitazato, H. and
Bernhard, J. M., Springer Japan, Tokyo, 163–193, 2014.Gilbert, D., Rabalais, N. N., Diaz, R. J., and Zhang, J.: Evidence for
greater oxygen decline rates in the coastal ocean than in the open ocean,
Biogeosciences, 2283–2296, 10.5194/bg-7-2283-2010, 2010.Gustafsson, M. and Nordberg, K.: Benthic foraminifera and their response to
hydrography, periodic hypoxic conditions and primary production in the
Koljö fjord on the Swedish west coast, J. Sea Res., 41, 163–178,
10.1016/S1385-1101(99)00002-7, 1999.Gustafsson, M. and Nordberg, K.: Living (Stained) Benthic Foraminifera and
their Response to the Seasonal Hydrographic Cycle, Periodic Hypoxia and to
Primary Production in Havstens Fjord on the Swedish West Coast, Estuar.
Coast. Shelf Sci., 51, 743–761, 10.1006/ecss.2000.0695, 2000.Hagens, M., Slomp, C. P., Meysman, F. J. R., Seitaj, D., Harlay, J., Borges,
A. V., and Middelburg, J. J.: Biogeochemical processes and buffering capacity
concurrently affect acidification in a seasonally hypoxic coastal marine
basin, Biogeosciences, 12, 1561–1583, 10.5194/bg-12-1561-2015, 2015.Hannah, F. and Rogerson, A.: The Temporal and Spatial Distribution of
Foraminiferans in Marine Benthic Sediments of the Clyde Sea Area, Scotland,
Estuar. Coast. Shelf Sci., 44, 377–383, 10.1006/ecss.1996.0136,
1997.Heinz, P., Geslin, E., and Hemleben, C.: Laboratory observations of benthic
foraminiferal cysts, Mar. Biol. Res., 1, 149–159,
10.1080/17451000510019114, 2005.Hess, S., Jorissen, F. J., Venet, V., and Abu-Zied, R.: Benthic foraminiferal
recovery after recent turbidite deposition in Cap Breton canyon, Bay of
Biscay, J. Foraminifer. Res., 35, 114–129, 10.2113/35.2.114, 2005.Jauffrais, T., Jesus, B., Geslin, E., Briand, F., and Jézéquel, V.
M.: Locomotion speed of the benthic foraminifer Ammonia tepida exposed to
different nitrogen and carbon sources, J. Sea Res., 118, 52–58,
10.1016/j.seares.2016.07.001, 2016.Jauffrais, T., LeKieffre, C., Koho, K. A., Tsuchiya, M., Schweizer, M.,
Bernhard, J. M., Meibom, A., and Geslin, E.: Ultrastructure and distribution
of kleptoplasts in benthic foraminifera from shallow-water (photic)
habitats, Mar. Micropaleontol., 138, 46–62,
10.1016/j.marmicro.2017.10.003, 2018.Jauffrais, T., LeKieffre, C., Schweizer, M., Geslin, E., Metzger, E.,
Bernhard, J. M., Jesus, B., Filipsson, H. L., Maire, O., and Meibom, A.:
Kleptoplastidic benthic foraminifera from aphotic habitats: insights into
assimilation of inorganic C, N and S studied with sub-cellular resolution,
Environ. Microbiol., 21, 125–141, 10.1111/1462-2920.14433, 2019.
Jones, G. D. and Ross, C. A.: Seasonal Distribution of Foraminifera in
Samish Bay, Washington, J. Paleontol., 53, 245–257, ISSN: 0022-3360,
1979.Jørgensen, B. B., Postgate, J. R., Postgate, J. R., and Kelly, D. P.:
Ecology of the bacteria of the sulphur cycle with special reference to
anoxic – oxic interface environments, Philos. T.
Roy. Soc. Lond. B, 298, 543–561,
10.1098/rstb.1982.0096, 1982.
Jorissen, F. J., Fontanier, C., and Thomas, E.: Chapter Seven
Paleoceanographical Proxies Based on Deep-Sea Benthic Foraminiferal
Assemblage Characteristics, in: Developments in Marine Geology, Vol. 1,
edited by: Hillaire-Marcel, C. and De Vernal, A., Elsevier,
263–325, 2007.Josefson, A. B. and Widbom, B.: Differential response of benthic macrofauna
and meiofauna to hypoxia in the Gullmar Fjord basin, Mar. Biol., 100,
31–40, 10.1007/BF00392952, 1988.Khan, A. A., Schuler, M. M., Prior, M. G., Yong, S., Coppock, R. W.,
Florence, L. Z., and Lillie, L. E.: Effects of hydrogen sulfide exposure on
lung mitochondrial respiratory chain enzymes in rats, Toxicol. Appl.
Pharmacol., 103, 482–490, 10.1016/0041-008X(90)90321-K, 1990.
Koho, K. A. and Piña-Ochoa, E.: Benthic Foraminifera: Inhabitants of
Low-Oxygen Environments, in: Anoxia: Evidence for Eukaryote Survival and
Paleontological Strategies, edited by: Altenbach, A. V., Bernhard, J. M., and
Seckbach, J., Springer Netherlands, Dordrecht, 249–285, 2012.Koho, K. A., Piña-Ochoa, E., Geslin, E., and Risgaard-Petersen, N.:
Vertical migration, nitrate uptake and denitrification: survival mechanisms
of foraminifers (Globobulimina turgida) under low oxygen conditions, FEMS
Microbiol. Ecol., 75, 273–283, 10.1111/j.1574-6941.2010.01010.x,
2011.Langlet, D., Geslin, E., Baal, C., Metzger, E., Lejzerowicz, F., Riedel, B.,
Zuschin, M., Pawlowski, J., Stachowitsch, M., and Jorissen, F. J.:
Foraminiferal survival after long-term in situ experimentally induced
anoxia, Biogeosciences, 10, 7463–7480, 10.5194/bg-10-7463-2013,
2013.Langlet, D., Baal, C., Geslin, E., Metzger, E., Zuschin, M., Riedel, B.,
Risgaard-Petersen, N., Stachowitsch, M., and Jorissen, F. J.: Foraminiferal
species responses to in situ, experimentally induced anoxia in the Adriatic
Sea, Biogeosciences, 11, 1775–1797, 10.5194/bg-11-1775-2014, 2014.Lee, J. J., Muller, W. A., Stone, R. J., McEnery, M. E., and Zucker, W.:
Standing crop of foraminifera in sublittoral epiphytic communities of a Long
Island salt marsh, Mar. Biol., 4, 44–61, 10.1007/BF00372165, 1969.LeKieffre, C., Spangenberg, J., Mabilleau, G., Escrig, S., Meibom, A., and
Geslin, E.: Surviving anoxia in marine sediments: The metabolic response of
ubiquitous benthic foraminifera (Ammonia tepida), PLoS ONE, 12, e0177604.,
10.1371/journal.pone.0177604, 2017.Linke, P. and Lutze, G. F.: Microhabitat preferences of benthic
foraminifera – a static concept or a dynamic adaptation to optimize food
acquisition?, Mar. Micropaleontol., 20, 215–234,
10.1016/0377-8398(93)90034-U, 1993.Metzger, E., Langlet, D., Viollier, E., Koron, N., Riedel, B., Stachowitsch,
M., Faganeli, J., Tharaud, M., Geslin, E., and Jorissen, F.: Artificially
induced migration of redox layers in a coastal sediment from the Northern
Adriatic, Biogeosciences, 11, 2211–2224, 10.5194/bg-11-2211-2014,
2014.Miller, A. A. L., Scott, D. B., and Medioli, F. S.: Elphidium excavatum
(Terquem); ecophenotypic versus subspecific variation, J. Foraminifer. Res.,
12, 116–144, 10.2113/gsjfr.12.2.116, 1982.Moodley, L. and Hess, C.: Tolerance of Infaunal Benthic Foraminifera for Low
and High Oxygen Concentrations, Biol. Bull., 183, 94–98,
10.2307/1542410, 1992.Moodley, L., van der Zwaan, G. J., Herman, P. M. J., Kempers, L., and
van Breugel, P.: Differential response of benthic meiofauna to anoxia with
special reference to Foraminifera (Protista: Sarcodina), Mar. Ecol. Prog.
Ser., 158, 151–163, 10.3354/meps158151, 1997.Moodley, L., van der Zwaan, G. J., Rutten, G. M. W., Boom, R. C. E., and
Kempers, A. J.: Subsurface activity of benthic foraminifera in relation to
porewater oxygen content: laboratory experiments, Mar. Micropaleontol.,
34, 91–106, 10.1016/S0377-8398(97)00044-3, 1998a.Moodley, L., Schaub, B. E. M., van der Zwaan, G. J., and Herman, P. M. J.:
Tolerance of benthic foraminifera (Protista: Sarcodina) to hydrogen
sulphide, Mar. Ecol. Prog. Ser., 169, 77–86, 10.3354/meps169077, 1998b.Moodley, L., Boschker, H. T. S., Middelburg, J. J., Pel, R., Herman, P. M.
J., de Deckere, E., and Heip, C. H. R.: Ecological significance of benthic
foraminifera: 13C labelling experiments, Mar. Ecol. Prog. Ser., 202,
289–295, 10.3354/meps202289, 2000.Muller, W. A.: Competition for food and other niche-related studies of three
species of salt-marsh foraminifera, Mar. Biol., 31, 339–351,
10.1007/BF00392091, 1975.Murray, J. W.: Production in benthic foraminiferids, J. Nat. Hist., 1,
61–68, 10.1080/00222936700770631, 1967.Murray, J. W.: Population dynamics of benthic foraminifera; results from the
Exe Estuary, England, J. Foraminifer. Res., 13, 1–12,
10.2113/gsjfr.13.1.1, 1983.Murray, J. W.: Distribution and population dynamics of benthic foraminifera
from the southern North Sea, J. Foraminifer. Res., 22, 114–128,
10.2113/gsjfr.22.2.114, 1992.Murray, J. W. and Alve, E.: Major aspects of foraminiferal variability
(standing crop and biomass) on a monthly scale in an intertidal zone, J.
Foraminifer. Res., 30, 177–191, 10.2113/0300177, 2000.Nardelli, M. P., Barras, C., Metzger, E., Mouret, A., Filipsson, H. L.,
Jorissen, F., and Geslin, E.: Experimental evidence for foraminiferal
calcification under anoxia, Biogeosciences, 11, 4029–4038,
10.5194/bg-11-4029-2014, 2014.Nicholls, P. and Kim, J. K.: Sulphide as an inhibitor and electron donor for
the cytochrome c oxidase system, Can. J. Biochem., 60, 613–623,
10.1139/o82-076, 1982.Nomaki, H., Chikaraishi, Y., Tsuchiya, M., Toyofuku, T., Ohkouchi, N.,
Uematsu, K., Tame, A., and Kitazato, H.: Nitrate uptake by foraminifera and
use in conjunction with endobionts under anoxic conditions, Limnol.
Oceanogr., 59, 1879–1888, 10.4319/lo.2014.59.6.1879, 2014.Nomaki, H., Bernhard, J. M., Ishida, A., Tsuchiya, M., Uematsu, K., Tame,
A., Kitahashi, T., Takahata, N., Sano, Y., and Toyofuku, T.: Intracellular
Isotope Localization in Ammonia sp. (Foraminifera) of Oxygen-Depleted
Environments: Results of Nitrate and Sulfate Labeling Experiments, Front.
Microbiol., 7, 163, 10.3389/fmicb.2016.00163, 2016.Panieri, G.: Foraminiferal response to an active methane seep environment: A
case study from the Adriatic Sea, Mar. Micropaleontol., 61, 116–130,
10.1016/j.marmicro.2006.05.008, 2006.Panieri, G. and Sen Gupta, B. K.: Benthic Foraminifera of the Blake Ridge
hydrate mound, Western North Atlantic Ocean, Mar. Micropaleontol., 66,
91–102, 10.1016/j.marmicro.2007.08.002, 2008.Papaspyrou, S., Diz, P., García-Robledo, E., Corzo, A., and
Jimenez-Arias, J.-L.: Benthic foraminiferal community changes and their
relationship to environmental dynamics in intertidal muddy sediments (Bay of
Cádiz, SW Spain), Mar. Ecol. Prog. Ser., 490, 121–135,
10.3354/meps10447, 2013.Pillet, L., de Vargas, C., and Pawlowski, J.: Molecular Identification of
Sequestered Diatom Chloroplasts and Kleptoplastidy in Foraminifera, Protist,
162, 394–404, 10.1016/j.protis.2010.10.001, 2011.Piña-Ochoa, E., Koho, K. A., Geslin, E., and Risgaard-Petersen, N.:
Survival and life strategy of the foraminiferan Globobulimina turgida
through nitrate storage and denitrification, Mar. Ecol. Prog. Ser., 417,
39–49, 10.3354/meps08805, 2010a.Piña-Ochoa, E., Høgslund, S., Geslin, E., Cedhagen, T., Revsbech, N.
P., Nielsen, L. P., Schweizer, M., Jorissen, F., Rysgaard, S., and
Risgaard-Petersen, N.: Widespread occurrence of nitrate storage and
denitrification among Foraminifera and Gromiida, P. Natl. Acad. Sci. USA,
107, 1148–1153, 10.1073/pnas.0908440107, 2010b.Polovodova, I., Nikulina, A., Schönfeld, J., and Dullo, W.-C.: Recent
benthic foraminifera in the Flensburg Fjord (Western Baltic Sea), J.
Micropalaeontol., 28, 131–142, 10.1144/jm.28.2.131, 2009.Pucci, F., Geslin, E., Barras, C., Morigi, C., Sabbatini, A., Negri, A., and
Jorissen, F. J.: Survival of benthic foraminifera under hypoxic conditions:
Results of an experimental study using the CellTracker Green method, Mar.
Pollut. Bull., 59, 336–351, 10.1016/j.marpolbul.2009.08.015, 2009.Rabalais, N. N., Díaz, R. J., Levin, L. A., Turner, R. E., Gilbert, D.,
and Zhang, J.: Dynamics and distribution of natural and human-caused
hypoxia, Biogeosciences, 7, 585–619, 10.5194/bg-7-585-2010, 2010.
Richirt, J., Schweizer, M., Bouchet, V. M. P., Mouret, A., Quinchard, S., and
Jorissen, F. J.: Morphological distinction of three Ammonia phylotypes
occurring along european coasts, J. Foraminifer. Res., 49, 77–94, 2019.
Riedel, B., Diaz, R., Rosenberg, R., and Stachowitsch, M.: The ecological
consequences of marine hypoxia: from behavioural to ecosystem responses, in:
Stressors in the marine environment: physiological responses and ecological
implication, edited by: Solan. M. and Whiteley, N. M., Oxford University
Press, 175–194, 2016.Risgaard-Petersen, N., Langezaal, A. M., Ingvardsen, S., Schmid, M. C.,
Jetten, M. S. M., Camp, H. J. M. O. den, Derksen, J. W. M., Piña-Ochoa,
E., Eriksson, S. P., Nielsen, L. P., Revsbech, N. P., Cedhagen, T., and
van der Zwaan, G. J.: Evidence for complete denitrification in a benthic
foraminifer, Nature, 443, 93–96, 10.1038/nature05070, 2006.Roberts, A., Austin, W., Evans, K., Bird, C., Schweizer, M., and Darling, K.:
A New Integrated Approach to Taxonomy: The Fusion of Molecular and
Morphological Systematics with Type Material in Benthic Foraminifera, PLOS
ONE, 11, e0158754, 10.1371/journal.pone.0158754, 2016.Ross, B. J. and Hallock, P.: Dormancy in the Foraminifera: A Review, J.
Foraminifer. Res., 46, 358–368, 10.2113/gsjfr.46.4.358, 2016.Schneider, C. A., Rasband, W. S., and Eliceiri, K. W.: NIH Image to ImageJ:
25 years of image analysis, Nat. Methods, 9, 671–675,
10.1038/nmeth.2089, 2012.Schönfeld, J. and Numberger, L.: Seasonal dynamics and decadal changes
of benthic foraminiferal assemblages in the western Baltic Sea (NW Europe),
J. Micropalaeontol., 26, 47–60, 10.1144/jm.26.1.47, 2007.Seitaj, D., Schauer, R., Sulu-Gambari, F., Hidalgo-Martinez, S., Malkin, S.
Y., Burdorf, L. D. W., Slomp, C. P., and Meysman, F. J. R.: Cable bacteria
generate a firewall against euxinia in seasonally hypoxic basins, P.
Natl. Acad. Sci. USA, 112, 13278–13283, 10.1073/pnas.1510152112, 2015.Seitaj, D., Sulu-Gambari, F., Burdorf, L. D. W., Romero-Ramirez, A., Maire,
O., Malkin, S. Y., Slomp, C. P., and Meysman, F. J. R.: Sedimentary oxygen
dynamics in a seasonally hypoxic basin, Limnol. Oceanogr., 62, 452–473,
10.1002/lno.10434, 2017.Stramma, L., Oschlies, A., and Schmidtko, S.: Mismatch between observed and
modeled trends in dissolved upper-ocean oxygen over the last 50 yr,
Biogeosciences, 9, 4045–4057, 10.5194/bg-9-4045-2012, 2012.Suhr, S. B., Pond, D. W., Gooday, A. J., and Smith, C. R.: Selective feeding
by benthic foraminifera on phytodetritus on the western Antarctic Peninsula
shelf: evidence from fatty acid biomarker analysis, Mar. Ecol. Prog. Ser.,
262, 153–162, 10.3354/meps262153, 2003.Sulu-Gambari, F., Seitaj, D., Meysman, F. J. R., Schauer, R., Polerecky, L.,
and Slomp, C. P.: Cable Bacteria Control Iron–Phosphorus Dynamics in
Sediments of a Coastal Hypoxic Basin, Environ. Sci. Technol., 50,
1227–1233, 10.1021/acs.est.5b04369, 2016a.Sulu-Gambari, F., Seitaj, D., Behrends, T., Banerjee, D., Meysman, F. J. R.,
and Slomp, C. P.: Impact of cable bacteria on sedimentary iron and manganese
dynamics in a seasonally-hypoxic marine basin, Geochim. Cosmochim. Ac.,
192, 49–69, 10.1016/j.gca.2016.07.028, 2016b.
Walton, W. R.: Techniques for recognition of living foraminifera, Contrib.
Cushman Found. Foraminifer. Res., 3, 56–60, 1952.Wang, F. and Chapman, P. M.: Biological implications of sulfide in
sediment – a review focusing on sediment toxicity, Environ. Toxicol. Chem.,
18, 2526–2532, 10.1002/etc.5620181120, 1999.
Wetsteijn, L. P. M. J.: Grevelingenmeer: meer kwetsbaar? Een beschrijving van de ecologische ontwikkelingen voor de periode 1999 t/m 2008–2010 in vergelijking met de periode 1990 t/m 1998, RWS Waterdienst, Lelystad 2011, 2011.Woulds, C., Cowie, G. L., Levin, L. A., Andersson, J. H., Middelburg, J. J.,
Vandewiele, S., Lamont, P. A., Larkin, K. E., Gooday, A. J., Schumacher, S.,
Whitcraft, C., Jeffreys, R. M., and Schwartz, M.: Oxygen as a control on sea
floor biological communities and their roles in sedimentary carbon cycling,
Limnol. Oceanogr., 52, 1698–1709, 10.4319/lo.2007.52.4.1698, 2007.