Introduction
The habitat of pelagic marine organisms is vertically structured by several
biotic and abiotic factors, such as light, prey density, temperature, oxygen
concentration and others. In the eastern tropical North Atlantic (ETNA), a
permanent oxygen minimum zone (OMZ) exists in the mesopelagial. The core of
this OMZ is centred at approximately 450 m, with the upper and lower
oxyclines at approximately 300 and 600 m depth (Karstensen et al., 2008).
Oxygen concentrations in this deep OMZ hardly fall below 40 µmol O2 kg-1
(Karstensen et al., 2008), but are sufficiently low to
exclude highly active top predators such as billfishes from the OMZ (Prince
et al., 2010; Stramma et al., 2012). In the eastern tropical South Atlantic,
with its more pronounced midwater OMZ, this layer may act as an effective
barrier for some species (e.g. Auel and Verheye, 2007; Teuber et al., 2013),
but seems to be diurnally crossed by others (Postel et al., 2007). Many
zooplankton and nekton taxa perform diurnal vertical migrations (DVMs),
usually spending the daylight hours in the mesopelagic OMZ and migrating
into the productive surface layer at night. These taxa include for example
euphausiids (Tremblay et al., 2011), sergestid and penaeid shrimp (Andersen
et al., 1997), myctophid fishes (Kinzer and Schulz, 1985) as well as several
large calanoid copepods (e.g. Pleuromamma species, Teuber et al., 2013). As DVM is a
survival mechanism to evade predation, hindrance thereof could lead to
substantial changes in ecosystem functioning. The ETNA OMZ has been observed to intensify (i.e. decrease in core O2 concentrations) and vertically
expand over the past decades and is predicted to further deoxygenate and
expand laterally (Stramma et al., 2008, 2009) under future
expectations of anthropogenic global warming (Cocco et al., 2013).
Submesoscale and mesoscale eddies (which in the tropics/subtropics comprise
diameters of the order of 101 and 102 km, respectively) often
represent hotspots (or “oases”) of biological productivity in the otherwise
oligotrophic open ocean (e.g. Menkes et al., 2002; McGillicuddy et al., 2007;
Godø et al., 2012), even translating up to top predators (Tew Kai and
Marsac, 2010). Their basin-wide relevance for biogeochemical cycles has been
increasingly recognized (e.g. Stramma et al., 2013). Numerous eddies spin off
the productive Mauritanian and Senegalese coasts (between Cap Blanc and Cap
Vert) throughout the year, with most anticyclones being generated in
summer/autumn and most cyclones in winter/spring (Schütte et al., 2015).
Both eddy types propagate westward at about 4 to 5 km day-1,
passing the Cabo Verde archipelago to the north or south. They can be tracked
by satellite altimetry for up to 9 months (Schütte et al., 2016;
Karstensen et al., 2015). While normal anticyclones are usually relatively
warm and unproductive (e.g. Palacios et al., 2006), both cyclonic and
anticyclonic modewater eddies (ACMEs) are characterized by a negative sea
surface temperature (SST) and positive surface chlorophyll a (chl a)
anomaly (Goldthwait and Steinberg; 2008; McGillicuddy et al., 2007). In
particular, ACMEs were observed to exceed cyclones in terms of upwelled
nutrients and productivity in the subtropical Atlantic (McGillicuddy et al.,
2007).
The recent discovery of mesoscale eddies (cyclones and ACMEs) with extremely
low oxygen concentrations just below the mixed layer (Karstensen et al.,
2015) has changed our view of current oxygen conditions in the ETNA. In that
study, it had been observed that oxygen values
< 2 µmol O2 kg-1 can be found in the shallow
oxygen minimum. The authors concluded that the low oxygen concentrations were
the result of isolation of the eddy core from surrounding water (a result of
the rotation of the eddy) paired with enhanced respiration (a result of the
high productivity and subsequent export and degradation of particulate
organic matter; Fischer at al., 2015), and introduced the term
“dead-zone eddy” (Karstensen et al., 2015). The lowest oxygen
concentrations so far in such an eddy
(< 2 µmol O2 kg-1 at about 40 m depth) were
observed in February 2010 at the Cape Verde Ocean Observatory (CVOO) mooring.
During the eddy passage across the mooring, an almost complete lack of
acoustic scatterers at depths below the oxygenated mixed layer was observed.
The acoustic backscattering signal received by the 300 kHz acoustic Doppler
current profiler (ADCP) is largely created by organisms > 5 mm
(thus missing a substantial part of the mesozooplankton) and does not allow
for the discrimination of different zooplankton groups.
Here, we characterize the ecology of zooplankton in response to the shallow
OMZ within an ACME that was identified, tracked and sampled in spring 2014.
We used acoustic (shipboard ADCP) and optical (Underwater Vision Profiler, UVP)
profiling methods as well as vertically stratified plankton net hauls to
resolve the vertical and horizontal distribution of zooplankton. Moreover,
we used acoustic and oxygen time series data from the CVOO mooring of one
extreme low oxygen eddy observed in February 2010 (Karstensen et al., 2015;
Fischer et al., 2015) to derive a more general picture about the zooplankton
sensitivity to low oxygen concentrations.
Materials and methods
In order to characterize the ecology, biogeochemistry and physical processes
associated with low-oxygen eddies in the tropical North Atlantic, a dedicated
field experiment (“eddy hunt”) north of the Cabo Verde archipelago was
designed. In summer 2013, the identification and tracking of candidate eddies
began by combining remotely sensed data and Argo float profile data. In
spring 2014, a candidate low-oxygen eddy was identified and on-site sampling
with gliders and research vessels began, covering genomics, physics and
biogeochemistry (see also Löscher et al., 2015; Schütte et al., 2016;
Fiedler et al., 2016; Karstensen et al., 2016). Ship-based sampling presented
here was carried out on 18 and 19 March 2014 during the RV Meteor
cruise M105. Two ADCP sections perpendicular to each other, a CTD/UVP5 cast
section and five multinet hauls were conducted. To better characterize the
average distribution of zooplankton during normal conditions in the
investigation area (as compared to conditions within the eddy), we combined
the single time point observation at the CVOO time series station with
previously collected data at the same station. For the multinet data, we used
three additional day/night casts (RV Maria S. Merian cruise
MSM22: 25 October and 20 November 2012; RV Meteor cruise M97:
26 May 2013). For the UVP data, we used seven nighttime profiles (because the
four eddy core stations were obtained during nighttime only) from cruises
M105, MSM22, M97 and M106 (19/20 April 2014).
In order to evaluate in greater detail the critical oxygen concentrations
that lead to avoidance behaviour, we used the mean volume backscatter
(Sv) and oxygen time series data from the CVOO mooring. Here, we focus
on the spring 2010 period that covered the transit of an extreme low oxygen
eddy, with oxygen content < 2 µmol kg-1 (Karstensen et
al., 2015).
ADCPs
Underway current measurements were performed during cruise M105 using two
vessel mounted ADCPs (vmADCPs), a 75 kHz RDI
Ocean Surveyor (OS75) and a 38 kHz RDI Ocean Surveyor (OS38). Standard
techniques (see Fischer et al., 2003) were used for data post-processing.
Depending on the region and sea state, the ranges covered by the instruments
are around 550 m for the OS75 and around 1000 m for the OS38. To locate the
eddy centre from the observed velocities, two sections were conducted (Fig. 1).
The first was a southeast-to-northwest section through the estimated (by
remote sensing) eddy centre. The second section was a perpendicular,
northeast-to-southwest section through the location of the lowest
cross sectional current velocity of the first section. The lowest
cross sectional velocity of the second section defines the eddy centre.
Cruise track (M105, only shown from 17 to 20 March 2014) with
horizontal current velocities (arrows) and CTD/UVP sampling positions
(triangles) as well as multinet stations (grey circles are night, empty
circles are day). Large dashed circle indicates the estimated radius of the
eddy based upon current structure.
The ADCP installed at the CVOO mooring site in 109 m water depth was an
upward looking 300 kHz Teledyne RDI workhorse instrument, recording data
every 1.5 h. It has a four-beam design in Janus configuration with a
20∘ opening. Based on accompanying hydrographic and pressure data,
each 4 m depth cell was allocated discrete pressure/depth information as
well as a sound speed profile (harmonic mean). Sv from the four
ADCP beams was averaged and matched to the oxygen data (i.e. backscatter
values in the depth cell where the oxygen sensor was located were used, which
varied around approximately 50 m, depending on the current strength). Only
data from 1 January to 14 March 2010 were used for the analysis to avoid the
influence of seasonal changes in scatterer abundance. Data collected from 11:00 to 18:00 and from 22:00 to
07:00 UTC were considered daytime and nighttime data, respectively. Apparent
sunrise and sunset in the period of January to March are around 08:00 and
19:30 UTC, respectively.
For vessel-mounted as well as moored ADCPs, Sv (MacLennan et al., 2002) was estimated for each beam and each depth
cell by a recalculation of a simplified sonar equation (Deimes, 1999). From
the vessel-mounted ADCPs, only the OS75 was used to assess backscatter
distribution. Since we were not attempting to estimate biomass, no further
calibration was applied and Sv values are relative.
CTD and UVP5
Oxygen concentration was measured using a SBE (Sea–Bird Electronics) CTD with two SBE 43 oxygen
sensors. The oxygen sensors were calibrated against 641 discrete oxygen
samples measured by Winkler titration during cruise M105. Inside the
CTD rosette, a UVP5 was mounted. This imaging tool allows for in situ quantification of
particles > 60 µm and plankton > 500 µm
with high vertical resolution (Picheral et al., 2010). Thumbnails of all
objects > 500 µm were extracted using the ImageJ-based ZooProcess macro set (Gorsky et al., 2010) and sorted automatically into 41
categories using Plankton Identifier (Gasparini, 2007). Experts validated
the automated image sorting. The observed volume of each image was 0.93 L
and approximately 10 images were recorded per metre depth. The mean total
sampling volume for the upper 600 m of the water column was 6.34
(±0.99) m3. Volume-specific abundance was calculated in 5 m depth bins.
Multinet
Zooplankton samples were collected with a Hydrobios multinet Midi (0.25 m2
mouth opening, five nets, 200 µm mesh, equipped with flowmeters)
hauled vertically from the maximum depth to the surface at 1 m s-1.
A full day/night multinet station was conducted well outside of the eddy
at 17.3474∘ N and 24.1498∘ W at the CVOO site, where a
set of physical and biogeochemical variables are measured on a monthly
basis. For this reason, CVOO standard depths were used in this multinet haul
(800–600–300–200–100–0 m) as it also served as the time series observation. As
the northwestward eddy transect was conducted during daytime, the “eddy core
day” multinet haul was collected on this transect (12:40 UTC) and the
“eddy core night” haul was collected at 02:10 UTC during the second
transect (for classification of stations, see hydrography results section),
at the location of the CTD profile with the lowest O2 concentration.
Thus, the eddy core day haul is approximately 14 km away from the eddy
centre (Fig. 1). Depth intervals (600–300–200–120–85–0 m) were chosen
according to the O2 profile. When leaving the eddy, a second day
haul was collected at the margin of the eddy, approximately 26 km from the
eddy centre, using the depth intervals from the eddy core station.
Zooplankton samples were fixed in 100 mL Kautex® jars in 4 %
borax-buffered formaldehyde in a seawater solution.
Zooplankton samples were analysed using a modification of the ZooScan Method
(Gorsky et al., 2010), employing an off-the-shelf flatbed scanner (Epson
Perfection V750 Pro) and a scan chamber constructed of a 21 cm × 29.7 cm
(DIN-A4) size glass plate with a plastic frame. Scans were 8bit greyscale,
2400 dpi images (tagged image file format; *.tif). The scan area was
partitioned into two halves (i.e. two images per scanned frame) to reduce
the size of the individual images and facilitate the processing by
ZooProcess/ImageJ. Samples were size fractionated by sieving into three
fractions (< 500, 500–1000 and > 1000 µm)
and split using a Motoda plankton splitter if necessary. The
> 1000 µm fraction was scanned completely, whereas
fractions comprising no more than approximately 1000 objects were scanned
for the two other fractions. “Vignettes” and image characteristics of all
objects were extracted with ZooProcess (Gorsky et al., 2010) and sorted into
39 categories using a Plankton Identifier (Gasparini, 2007). Automated image
sorting was then manually validated by experts.
Results
Hydrography
The site survey with RV Meteor succeeded in sampling the eddy core with CTD
and UVP casts. The lowest measured O2 concentration was
3.75 µmol O2 kg-1 at 106 m depth. Based upon the current velocity, the
eddy was approximately 110 km in diameter (Fig. 1), but oxygen
concentrations below 20 and 5 µmol O2 kg-1 were only found
within approximately 18 and 8 km from the centre, respectively. For the
purpose of this study, the four stations within 20 km of the eddy core (with
minimum O2 concentrations well below 20 µmol O2 kg-1) were
considered “eddy core”, while the four stations within 20 to 35 km from
the eddy core were considered “eddy margin” (with minimum O2
concentrations between 21 and 53 µmol O2 kg-1) and the CVOO
station (M105 data complemented with data from previous cruises, n=7
profiles; see methods) was considered to represent ambient conditions
outside of the eddy. Here, a shallow OMZ was not present. The midwater OMZ
(centred around approximately 450 m depth) featured mean minimum oxygen
concentrations of 70 µmol O2 kg-1).
Vertical distribution and DVM – acoustic observations
During the M105 ADCP survey, several features were apparent in the vertical
distribution and migration of scatterers outside of the eddy (Fig. 2).
First, a deep scattering layer was detected centred between below 350 and
400 m depth. From this layer, part of the population started its ascent to
the surface layer at about 18:00 UTC. The centre of the nighttime
distribution outside the eddy ranged from approximately 30 to 130 m depth.
During the day, the lowest Sv was recorded between 100 and 300 m depth,
with a residual non-migrating population in the upper 100 m. The ascendant
and descendent migration took place from approximately 18:00 to 20:00 UTC
(16:15 to 18:15 solar time) and 07:00 to 09:00 UTC (05:15 to 07:17 solar
time), respectively.
Cruise track with indicated day- and nighttime hours
(panel a, red cross indicates intersection of day- and nighttime
section) and shipboard acoustic Doppler current profiler (ADCP) mean volume
backscatter Sv at 75 kHz (panel b, red crosses indicate
the two profiles obtained at the intersection). White contour lines indicate
oxygen concentrations interpolated from CTD profiles (triangles denote CTD
stations).
A very different nighttime distribution was observed when traversing the
eddy. The scattering in the surface layer was located further up in the
water column than outside the eddy and their lower distribution margin
coincided with the upper oxycline (approximately 85 m in the eddy centre).
In the core of the shallow OMZ, below approximately 20 µmol O2 kg-1,
an absolute minimum Sv was observed.
The intersection of the two transects (see red crosses in Fig. 2) was
visited shortly after 12:00 and 00:00 UTC, representing full day/night
conditions, respectively. Here, the difference between Sv in the
surface at daytime and nighttime suggests substantial vertical migration into/out of
the surface layer, crossing the OMZ (Fig. 2b). Furthermore, the distribution of the
surface daytime resident population (with Sv values of approximately
75 dB) is bimodal, peaking again at approximately 90 m. This is well within
the shallow OMZ (note that there are no O2 isolines shown in the
daytime transect in Fig. 2b since there were no CTD casts performed on the
first transect).
Reanalysis of acoustic backscatter and oxygen time series data from the CVOO
mooring before and during the transit of an ACME in 2010 (Karstensen et al.,
2015) shows that the daytime Sv at the depth level of the oxygen sensor
(around 50 m, depending on wire angle) is reduced below approximately
20 µmol O2 kg-1 (Fig. 3a, power function; r2= 0.69). For
nighttime data (Fig. 3b), the relationship between Sv and oxygen
concentration is best described by a linear function (r2= 0.94).
Sv in the subsurface increases around approximately 07:00 and 19:00 UTC
(Supplement Fig. S1). These dusk and dawn traces suggest that DVM
species migrate through the OMZ even when the daily mean oxygen
concentration is between 5 and 20 µmol kg-1.
Moored ADCP (300 kHz, matched to depth of moored oxygen sensor,
approximately 50 m) mean volume backscatter Sv (dB) as a function
of oxygen concentration (µmol O2 kg-1) during daytime
(a) and nighttime hours (b). Higher Sv indicates
a higher biomass of zooplankton and nekton. Transparent symbols are
1.5-hourly data, filled symbols are mean values (±SD) for
10 µmol O2 kg-1 bins. Data are from 1 January to
14 March 2010.
Left column shows oxygen contours
(µmol O2 kg-1) across the eddy (from NE to SW) with
superimposed bubble plots of UVP-based abundance (individuals m-3, in
5 m depth bins) of aggregates (a), copepods (b),
collodaria (c), gelatinous plankton (d) and shrimp-like
organisms (euphausiids and decapods) (e). Note break in distance
axis on section panels. Triangles denote CTD/UVP stations. Middle column are
profiles of mean (±SD) abundance within the eddy core (n= 4) and at
the CVOO station (n= 7) along with mean oxygen profiles with the exception
of euphausiids and decapods (e), where “+” denotes positive
observations. For better visibility at low values, data with mean
abundance = 0 are omitted. Right column shows representative images of
the respective category.
UVP5-derived integrated abundance (m-2, upper 600 m) of large
aggregates (> 500 µm) (a), copepods (b),
collodaria (c), gelatinous plankton (d), shrimp-like micronekton
(euphausiids/decapods)
(e) and phaeodaria (f) in the eddy core (n= 4 profiles), eddy margin (n= 4)
and outside of the eddy (n= 7). Different letters denote significant
differences.
Optical profiling
The UVP5 transect across the eddy revealed a pronounced increase of
aggregates in the eddy core (Fig. 4a). This pattern was still evident at the
maximum profile depth (600 m, below the midwater OMZ). At the same time,
surface abundance of copepods (Fig. 4b) and, to a lesser degree, collodaria
(Fig. 4c) is higher than in surrounding waters. Copepods were observed in
substantial abundance within the OMZ, while collodaria appeared to avoid it.
On the other hand, gelatinous zooplankton (comprising medusae, ctenophores
and siphonophores; Fig. 3d) were observed in the inner OMZ core. Not a
single observation of shrimp-like micronekton (euphausiids and decapods; Fig. 4e) was made at oxygen concentrations lower than 28 µmol O2 kg-1.
Integrated abundance (upper 600 m; Fig. 5) of large aggregates
was significantly higher in the core stations compared to the
outside (one-way ANOVA, Tukey's HSD test p < 0.001) and margin
(p < 0.05) stations. The integrated abundance of gelatinous plankton
was significantly higher in the core stations than in the outside
stations (p < 0.05). For the other groups, differences in integrated
abundance were not significant.
Multinet
The multinet data provide a higher taxonomic resolution, but lower spatial
(horizontal and vertical) resolution than the optical profiles (UVP). In
Fig. 6, the abundance and vertical distribution of eight conspicuous taxa
are depicted, ordered by their apparent sensitivity to hypoxia. While
euphausiids (Fig. 6a), calanoid copepods (Fig. 6b) and foraminifera (Fig. 6c)
are abundant in the surface layer (exceeding the mean abundance at
CVOO), they appear to avoid the shallow OMZ. Siphonophores (Fig. 6d), the
poecilostomatoid Oncaea spp. (Fig. 6e) and eucalanoid copepods (Fig. 6f) are all
very abundant in the eddy's surface layer during nighttime (with the latter
also being observed in the shallow OMZ during nighttime) and appear to take
refuge within the shallow OMZ during daylight hours. Two groups that
appeared to favour the shallow OMZ even during nighttime hours were
polychaetes (Fig. 6g) and ostracods (Fig. 6h), but also the harpacticoid
copepod Macrosetella gracilis (Table S1 in the Supplement). Taxa that were more abundant in the surface layer of
the eddy core compared to the mean outside eddy situation included
eucalanoid and other calanid copepods, Oithona spp.,
Macrosetella gracilis, Oncaea spp., ostracods, decapods,
siphonophores, chaetognaths, molluscs (mainly pteropods), polychaetes and
foraminifera (Table S1). In contrast, taxa that were less abundant in the
surface layer in the eddy were amphipods, salps and appendicularia. Although
not sampled quantitatively by this type of net, this also seemed to be the
case for fishes. In particular, no single individual was caught in the upper
200 m of the eddy core night station. Total area-integrated abundance of all
zooplankton organisms in the upper 600 m was 151 000 (±34 000) m-2
in the eddy core and 101 000 (±15 000) at the outside
station (Table S2).
Oxygen contours (µmol O2 kg-1) across the eddy
(from NE to SW) with superimposed bar plots of multinet-based abundance
(individuals m-3) of euphausiids (a), calanoid copepods (b),
foraminifera (c), siphonophores (d), Oncaea sp. (e),
eucalanid copepods (f), polychaetes (g) and ostracods (h).
White and grey bars indicate daylight
and nighttime hauls, respectively. Triangles denote CTD stations used for
the O2 section. For the CVOO station (outside eddy situation), the
mean (+SD) of four D / N samplings is shown and the distance to core is not
calculated because data were combined from different cruises. Representative
images are shown next to the respective category panel.
Discussion
Already during the remote survey, it became apparent that the tracked
mesoscale eddy was a hotspot of primary productivity. Lowered sea surface
temperature and elevated surface chl a values (satellite imagery;
Schütte et al., 2016) as well as increased nitrate levels in the eddy
interior (autonomous gliders; Karstensen et al., 2016; Fiedler et al., 2016)
indicate active upwelling and translate into substantially increased
productivity (Löscher et al., 2015). During westward propagation, the
hydrographic character was found to be remarkably constant (Karstensen et
al., 2016; Schütte et al., 2016), while the genomic characterization
(Löscher et al., 2015) indicated that the eddy had created a unique
ecosystem that has not much in common with the coastal one it originated
from. The present study is the first to observe the impact of such eddies on
pelagic metazoans. Since process understanding and zooplankton production
estimates are still lacking, we cannot conclude whether the system is
ultimately bottom-up or top-down controlled and whether the seemingly high
zooplankton productivity may be due to lacking higher trophic levels.
We deliberately chose not to attempt a direct comparison of methods (e.g. by
trying to derive biomass from ADCP backscatter), but rather use the three
methods complementary to each other: the acoustic survey reveals the
horizontal and vertical fine-scale spatial distribution of scatterers
(macrozooplankton and micronekton). It suggests a complete avoidance of the
OMZ by these groups, whose identity remains somewhat unclear (see also
Karstensen et al., 2015). The UVP has an excellent vertical and an
intermediate horizontal (several profiles along transect) resolution, with
restricted information regarding the identity of the organisms (limited by
image resolution and sampling volume to more abundant mesozooplankton). The
multinet has low vertical and horizontal resolution, and low catch
efficiency for fast-swimming organisms. Its main asset is that it allows for a
detailed investigation of zooplankton and some micronekton organisms. Since
the samples are still intact after scanning, taxonomists interested in one
of the groups presented here would even be able to proceed with more
detailed work.
Using the shipboard and moored ADCP to investigate acoustic backscatter
(rather than a calibrated scientific echosounder) resulted from the
necessity to gather ADCP-derived current velocity data for eddy
identification and localization of the core (see Fig. 1). It has to be noted
that the backscatter signals from the 75 kHz shipboard ADCP and the 300 KHz
moored ADCP are strictly not comparable, as for organisms that are small
compared to the acoustic wavelengths, the backscatter strength increases
rapidly with increasing frequency (Stanton et al., 1994). Also, smaller
organisms contribute more to the 300 kHz signal than to the 75 kHz. Nevertheless,
both instruments suggest that OMZ avoidance sets in at O2
concentrations lower than approximately 20 µmol O2 kg-1.
The marked decrease in ADCP Sv in the shallow OMZ is only partly
confirmed by the other two techniques. The animals that contribute most to
the ADCP backscatter at a frequency of 75 kHz are targets in the centimetre-size
range (75 kHz correspond to a wavelength of 20 mm), i.e. larger zooplankton
and micronekton such as euphausiids, amphipods, small fish, pteropods,
siphonophores and large copepods (Ressler, 2002). Thus, the community of
organisms contributing most to the backscatter is not quantitatively (i.e.
providing accurate abundance estimates) sampled by the multinet and the
UVP5. Both mostly target organisms < 10 mm in size and the sampling
volume is small, in particular with the UVP5. Still, spatial observation
patterns of these organisms derived from the multinet and UVP5 may help to
provide explanations for the patterns observed in the ADCP, even though
abundance estimates are to be taken with caution. For example, euphausiids
contribute substantially to the backscatter at 75 kHz in this region (as
observed through horizontal MOCNESS tows during dusk and dawn, resolving ADCP migration traces; Buchholz et al., unpublished data). Thus, the
relative decrease of observed euphausiids in the OMZ (and in the eddy in
general) in both multinet samples and UVP profiles suggests that they may be
partly responsible for the lack of backscatter in the OMZ.
High-resolution profiles obtained by the UVP5 indicated OMZ avoidance by
euphausiids and collodaria, while copepods (albeit at lower concentrations
than in the surface layer) were observed in the OMZ core. Gelatinous
zooplankton was even more abundant in the shallow OMZ than in surface
waters. The multinet data (providing higher taxonomic resolution and larger
sampling volume, but lower vertical resolution) suggest that there are four
strategies followed by zooplankton in the eddy, which will be discussed
below.
Shallow OMZ avoidance and compression at the surface
We ascribe this behaviour to euphausiids and most calanoid copepods as well
as collodaria and foraminifera (from the supergroup rhizaria). While the
total abundance of krill is probably underestimated by the comparatively slow
and small plankton net, their vertical distribution in relation to the OMZ
and the marked total decrease within the eddy compared to outside stations
suggests that they are susceptible to OMZ conditions and may suffer from
increased predation in the surface layer. This is in line with physiological
observations, where a critical partial pressure of 2.4 and 6.2 kPa (29.6 and
64.2 µmol O2 kg-1) was determined at subsurface
(13 ∘C) and near-surface temperatures (23 ∘C),
respectively, in Euphausia gibboides in the ETNA (Kiko et al.,
2015). Calanoid copepods represent the largest group in terms of abundance
and biomass and comprise approximately 100 species in Cabo Verdean waters
(Séguin, 2010) with a wide range of physiological and behavioural
adaptations. Species most tolerant to low-oxygen conditions are vertically
migrating species, such as Pleuromamma spp., while epipelagic
species, such as Undinula vulgaris, are less tolerant (Teuber et
al., 2013; Kiko et al., 2015). From the rhizaria supergroup, the fine-scale
distribution pattern of solitary collodaria (a group that is abundant in
surface waters of the oligotrophic open ocean; see Biard et al. 2015 and
references therein) suggests OMZ sensitivity, but direct evidence from the
literature is lacking. The foraminifera, which are mostly too small to be
quantified well with the UVP5, but in contrast to other rhizaria are well
preserved in buffered formaldehyde in seawater solution, were highly abundant
in the surface of the eddy core. Here, the distribution shift likely also
includes a community shift, since a marked dominance change from
surface-dwelling to subsurface-dwelling species was found in sediment trap
data during the transit of the 2010 ACME (Fischer et al., 2015). In that
ACME, also an export flux peak by foraminifera was observed.
Migration to the shallow OMZ core during daytime
This strategy seems to be followed by siphonophores, Oncaea spp. and eucalanoid
copepods.
Although it seems unlikely that siphonophores in this survey were
contributing substantially to the ADCP backscatter, as those retrieved by
the multinet were almost exclusively calycophorans (see Fig. 6d for a type
specimen), which do not have a pneumatophore and, therefore, lack gas bubbles
that are highly resonant in other siphonophore groups (e.g. Ressler, 2002).
They may, however, contribute to the weak backscatter signal in the shallow
OMZ during daytime (Figs. 2b and 6d). Oncaea spp. are particle-feeding copepods that
are directly associated with marine snow (Dagg et al., 1980). They were
observed in quite extreme OMZs in other oceanic regions (e.g.
Böttger-Schnack, 1996; Saltzman and Wishner, 1997); however, our
results suggest that at least in the tropical Atlantic biome they cannot
permanently endure hypoxia but have to pay their oxygen debt during
nighttime. The majority of adult eucalanoid copepods were Rhincalanus nasutus, a species that
is frequently found in the midwater OMZ of the ETNA. In the eastern tropical
Pacific, however, R. nasutus was reported to be excluded from the extreme midwater OMZ
(500–1000 m depth, below approximately 22 µmol O2 kg-1),
unlike the key OMZ-adapted eucalanoid species of that region (e.g.
Eucalanus inermis), which are able to permanently inhabit the OMZ (Saltzman and Wishner,
1997). In our study, R. nasutus were also found in the shallow (extreme) OMZ of the
eddy (well below 20 µmol O2 kg-1), indicating that this
copepod species also may be able to cope with further deoxygenation of the
midwater OMZ in the Atlantic. Both Oncaea and Rhincalanus are unlikely to be seen in the
Sv signal at 75 kHz.
Residing in the shallow OMZ day and night
Contrary to most crustaceans, collodaria and euphausiids, a remarkable
ability to endure OMZ conditions for prolonged periods of time seems to be
present in ostracods, polychaetes, Macrosetella gracilis and gelatinous plankton. “Jellies” are
a group of organisms of which several taxa, such as siphonophores, salps,
hydromedusae and ctenophores, have been reported to tolerate hypoxic
conditions much better than most crustacean zooplankton (Mills, 2001; Thuesen
et al., 2005). In addition to reduced metabolic activity (e.g. Rutherford Jr. and
Thuesen, 2005), using the mesoglea gel matrix as an oxygen reservoir was
shown to be a strategy in scyphomedusae to temporarily survive anoxia
(Thuesen et al., 2005). It has also been suggested that “jellyfish” (i.e.
pelagic cnidarians and ctenophores) outcompete other planktonic groups in
coastal systems under eutrophication-induced hypoxia (Mills, 2001). The UVP5
nighttime section suggests that many gelatineous organisms reside within the
shallow OMZ even during nighttime. This is only partly confirmed by the
multinet data; however, ctenophores and medusae are often destroyed during
sampling and not well preserved in formaldehyde. For ostracods, it is known
that several limnic (Teixeira et al., 2014) and marine (Corbari et al., 2004)
benthic species tolerate hypoxia for prolonged periods of time (and
preferentially select hypoxic habitats over oxygenated ones), which lead to
the use of their abundance in sediment cores as a proxy for past ocean
oxygenation (Lethiers and Whatley, 1994). In pelagic marine ostracods,
however, there is little evidence for particular pre-adaptation to OMZ
conditions. To the best of our knowledge, no physiological studies exist
that describe the metabolic response of pelagic ostracods to hypoxia.
Recently, it was found that the oxygen transport protein hemocyanin occurs
in several groups within the class ostracoda, including planktonic species
(Marxen et al., 2014). In the Arabian Sea, the highest ostracod abundances were
found in the oxygenated surface layer, but consistent occurrence in the
extreme OMZ (< 5 µmol O2 kg-1) was reported
(Böttger-Schnack, 1996). In the eastern tropical Pacific, most species
were reported to avoid the OMZ, with the notable exception of Conchoecetta giesbrechti, which is
classified as an OMZ-adapted species (Castillo et al., 2007). For pelagic
polychaetes, Thuesen and Childress (1993) even state that they may have the
highest metabolic rates (and, thus, oxygen demand) in the meso- and
bathypelagic zones of the oceans, with the exception of the aberrant species
Poeobius meseres.
Migration through the shallow OMZ core to better-oxygenated depths
To rigorously assess DVM reduction by the underlying OMZ, acoustic
24 h observations would be necessary to directly observe the migration
pattern. Unfortunately, the dawn and dusk migration observations took place
at the northeast- and southwest-margin of the eddy, respectively, just outside the
30 µmol O2 kg-1 boundary (Fig. 2). Nevertheless, it appears
from the day/night difference in the shipboard ADCP Sv (at the
intersection of the two transects) as well as from the moored ADCP data (Fig. S1)
that at least part of the migrating population “holds its breath” and
crosses the OMZ during ascent/descent. In this respect, the thin shallow OMZ
seems to be different from the several hundred metres thick mesopelagic OMZ,
which at low core oxygen concentrations can serve as a quite effective
migration barrier (Auel and Verheye, 2007; Teuber et al., 2013).
The enhanced surface primary productivity of the eddy also resulted in an
approximately 5-fold increase of large particles, well visible down to 600 m
depth. This indicates a massive export flux by sinking marine snow (see also
Fischer et al. (2015) for sediment trap data of the 2010 ACME), which is thus
made available to higher trophic levels at greater depths. As an example,
phaeodaria (in supergroup rhizaria) are one of the few exclusively
mesopelagic groups (only found deeper than approximately 200 m in UVP
profiles). Their integrated abundance seemed to be positively affected by
the eddy conditions, which may indicate favourable feeding/growth conditions
at depth.
In summary, mesozooplankton biomass was generally enhanced in the euphotic
zone of the ACME, suggesting that it may represent an “oasis in the
desert” sensu Godø et al. (2012), although the differences to outside
conditions were not quite as large as those reported by Goldthwait and
Steinberg (2008). On the other hand, subsurface hypoxia appears to be
detrimental to some surface-dwelling as well as vertically migrating
zooplankton taxa. We lack quantitative estimates of higher trophic levels
(the multinet is too small and slow to efficiently sample fast-swimming
nekton organisms), but it seems that the small migratory mesopelagic fishes,
which were usually caught (albeit in low numbers) outside the eddy, were less
abundant in the eddy core's surface. To draw robust conclusions on the
identity and whereabouts of acoustic scatterers, the additional use of
several types of stratified nets is necessary (e.g. 10 m2 MOCNESS in
addition to a multinet or 1 m2 MOCNESS) but was logistically impossible
during the opportunistic sampling on M105. Since gelatinous plankton
organisms appear to play a key role in these oceanic OMZs and are
notoriously undersampled by nets and/or destroyed by fixatives, it even
seems worthwhile to employ a dedicated camera system (with larger sampling
volume than the UVP5) for such a survey. It also remains an open question
whether the rich zooplankton prey field is exploited by epipelagic fishes
and their predators (see, e.g., Tew Kai and Marsac (2010) for examples of tuna
and seabird interaction with cyclonic eddies). By providing isolated bodies
of water with distinct (and sometimes, like in our case, extreme)
environmental conditions for many months, mesoscale eddies are important
vectors of species dispersal and invasion (Wiebe and Flierl, 1983) and
subject the population fragments they contain to their own mutations,
selection forces and genetic drift effects. Thus, they not only are
hypothesized to play a central role in speciation of planktonic species
(Bracco et al., 2000; Clayton et al., 2013), but also may resemble a key mechanism
to equip oceanic metapopulations with the range of physiological and
behavioural adaptations deemed necessary to survive under global change.