Diel vertical migration (DVM) can enhance the vertical
flux of carbon (C), and so contributes to the functioning of the biological
pump in the ocean. The magnitude and efficiency of this active transport of
C may depend on the size and taxonomic structure of the migrant zooplankton.
However, the impact that a variable community structure can have on
zooplankton-mediated downward C flux has not been properly addressed. This
taxonomic effect may become critically important in highly productive
eastern boundary upwelling systems (EBUSs), where high levels of zooplankton
biomass are found in the coastal zone and are composed by a diverse community
with variable DVM behavior. In these systems, presence of a subsurface
oxygen minimum zone (OMZ) can impose an additional constraint to vertical
migration and so influence the downward C export. Here, we address these
issues based on a vertically stratified zooplankton sampling at three
stations off northern Chile (20–30∘ S) during
November–December 2015. Automated analysis of zooplankton composition and
taxa-structured biomass allowed us to estimate daily migrant biomass by taxa
and their amplitude of migration. We found that a higher biomass aggregates
above the oxycline, associated with more oxygenated surface waters and this
was more evident upon a more intense OMZ. Some taxonomic groups, however,
were found closely associated with the OMZ. Most taxa were able to perform
DVM in the upwelling zone withstanding severe hypoxia. Also, strong
migrants, such as eucalanid copepods and euphausiids, can exhibit a large
migration amplitude (∼500 m), remaining either temporarily or
permanently within the core of the OMZ and thus contributing to the release
of C below the thermocline. Our estimates of DVM-mediated C flux suggested
that a mean migrant biomass of ca. 958 mg C m-2 d-1 may contribute
with about 71.3 mg C m-2 d-1 to the OMZ system through respiration,
mortality and C excretion at depth, accounting for ca. 4 % of the net
primary production, and so implies the existence of an efficient mechanism
to incorporate freshly produced C into the OMZ. This downward C flux
mediated by zooplankton is however spatially variable and mostly dependent
on the taxonomic structure due to variable migration amplitude and DVM
behavior.
Introduction
The oxygen minimum zone (OMZ) in the southeast Pacific, the fourth largest
of the six permanent hypoxic regions in the world oceans
(Paulmier et al., 2006), is a key component of the
water column and a permanent feature intruding the coastal zone of Ecuador,
Peru and Chile (Fuenzalida et al.,
2009; Paulmier et al., 2006). In the highly productive upwelling region of northern
Chile, the OMZ is closely linked to wind-driven upwelling in the coastal
area and associated to the Equatorial Subsurface Water (ESSW), which is
transported southward along the continental shelf by the Peru–Chile
Undercurrent (PUC), as far south as 48∘ S
(Fuenzalida
et al., 2009; Morales et al., 1996a; Silva and Neshyba, 1979). Off Iquique (20∘ S) the OMZ is characterized by being thick (500 m), very intense (< 20 µmol kg-1) and with O2 concentrations in the core of OMZ
among the lowest found in the global ocean reaching the current detection
limit (< 1 µM) (Ulloa and
Pantoja, 2009), although it becomes thinner at about 30∘ S
(Paulmier et al., 2006).
During the last decades, the OMZ systems have attracted much scientific
interest because of evidence showing that hypoxic and anoxic conditions in
coastal areas are expanding and becoming more intense
(Ekau et al., 2010; Stramma et al., 2008). At
present, ongoing ocean deoxygenation is widely recognized as being linked to
global warming, and it is raising much concern in modern oceanography
(Breitburg et al., 2018).
The presence of oxygen-depleted water becomes a critical physiological
constraint for pelagic and benthic organisms inhabiting the upwelling zone,
impacting their biomass and productivity, species diversity,
distribution, behavior and metabolic activity
(Wishner
et al., 2018; Ekau et al., 2010; Grantham et al., 2004). For instance, diel vertical migration
(DVM), a common feature of the various size groups of zooplankton and also
one of the most important movements of biomass in the ocean, can also be
affected by changes in intensity and distribution of the OMZ
(Wishner
et al., 2018, 2013; Escribano et al., 2009; Fernández-Álamo and Färber-Lorda,
2006; Hidalgo et al., 2005; Morales et al., 1996; Judkins, 1980). The OMZ can act as an
ecological barrier for vertical distribution of many organisms, constraining
most zooplankton to a narrow (50 m) upper layer, as shown in the coastal
upwelling zone off Chile according to the works of Escribano (2006) and Donoso and Escribano (2014). Zooplankton also
become limited to the upper 150 or 300 m in the eastern tropical North Pacific (Wishner et al., 2013).
However, the OMZ can also offer refuge for species adapted to live there,
creating microhabitats of differing oxygen concentration that are
characterized by layers of high zooplankton biomass and abundance, with
distinct species zonation
(Antezana,
2009; Wishner et al., 2008; Fernández-Álamo and Färber-Lorda,
2006), which, in turn, may have important consequences for carbon (C)
cycling and its vertical flux. For example, it is known that zooplankton in
the coastal upwelling region off northern Chile may play a significant
biogeochemical role by promoting carbon flux into the subsurface OMZ
(Escribano et al., 2009). Therefore a significant proportion of the
vertical material flux from the euphotic zone to the deep sea (> 200 m) and within the food chain could be determined by DVM of zooplankton
(Longhurst and Williams, 1992; Steinberg and
Landry, 2017).
Study area at the northern upwelling region of Chile,
indicating sampling stations during the Lowphox cruise conducted in
November–December 2015 onboard the R/V Cabo de Hornos. Satellite estimated net primary
production (NPP), averaged for November–December 2015 is shown. NPP was
obtained from http://www.science.oregonstate.edu/ocean.productivity/, last access: 17 December 2019.
As important contributors to the functioning of the biological pump, diel
zooplankton migrants can actively increase the magnitude of C export by
transporting surface-ingested material in their guts to deep waters where it
can be metabolized (Steinberg and Landry, 2017).
Zooplankton moults or mortality at depth can also contribute to the
transportation of assimilated organic biomass into the deep waters
(Ducklow et al., 2001). The biological pump process is also
thought to be related to the size structure of dominant zooplankton. This
because some groups with large body sizes may exhibit a greater range of
vertical migration and sometimes higher levels of biomass, and so
influences the biogeochemical fluxes
(Dai et al., 2016;
Ducklow et al., 2001). However, the effect of variable size structure on DVM
performance and its consequence for active C transport has indeed not been
assessed. Size structure is certainly related to zooplankton composition,
which has hardly been properly addressed when examining the role of DVM on C
flux. For instance, in areas with hypoxic subsurface layers some species are
more active migrants and thus more efficient C transporters, because they
have developed adaptations to low oxygen conditions and can even use the OMZ
as their habitat, either temporarily or permanently
(Escribano et al., 2009;
Gonzalez and Quiñones, 2002; Seibel, 2011). Adaptation may include in
some cases reduction of aerobic metabolism by more than 50 % during
exposure to hypoxic conditions as a mechanism to facilitate low oxygen
tolerance, reducing dramatically energy expenditure during daytime
within low oxygen waters and therefore affecting the C flux in areas
subjected to low concentrations of oxygen (Seibel et al., 2016).
C export to depth may also depend on the amount of biomass being produced in
the photic zone. Primary production promotes zooplankton feeding and growth,
and therefore determines C availability for both passive and active
transport to depth. In this context, highly productive upwelling zones can
be assumed as systems where the C flux mediated by zooplankton DVM can be
enhanced, although it certainly depends on the size and taxonomic structure
of zooplankton. In these regions, a shallow OMZ might exert a further impact
on the C flux by affecting DVM or zooplankton metabolism at depth. In the
present study, based on vertically resolved resolution sampling and
automated analysis of mesozooplankton, we assessed zooplankton vertical
migration and downward C to the OMZ in the highly productive upwelling
region of northern Chile. We aimed at understanding the role that taxonomic structure
and size structure can play in the magnitude and variability of the DVM
behavior interacting with a shallow OMZ and the implications this
interaction can have on the magnitude of the downward C flux in a highly
productive coastal upwelling zone
MethodsStudy area
The study area was located in the southeast Pacific Ocean and covered the
coastal zone of the northern upwelling region of Chile
(21–29∘ S) (Fig. 1), which is a region known to be
subjected to wind-driven upwelling throughout the year and contains an
intense and shallow OMZ (Ulloa et al.,
2012). The sampling design comprised three stations: two stations (St. T3
and St. T5) across a zonal section off Iquique (20∘ S) and a
coastal station (St. L6) off Coquimbo (29∘ S). The study was
carried out during the Lowphox cruise conducted in November–December 2015
onboard the R/V Cabo de Hornos. At each station, temperature, salinity and dissolved oxygen
(DO) were recorded from 1000 m (St. T5 and St. T3) and only 356 m (St. L6)
using an oceanographic rosette with a CTD Sea-Bird 911 (SBE 911 plus)
equipped with a Sea-Bird SBE-43 oxygen sensor and a Sea Tech fluorometer.
Discrete water samples were also obtained for chemical measurements of
oxygen.
Zooplankton sampling
Zooplankton samples were collected during daytime and nighttime conditions
on 2 consecutive days at the three stations off northern Chile (T5–T3–L6)
(Fig. 1), also as indicated in Table S1 (Supplement). Vertical hauls of zooplankton were performed from 600 to 0 m
depth with a Multi Plankton Sampler Hydro-Bios MultiNet system with a 0.25 m2 opening area and equipped with 200 µm mesh-size nets. The
MultiNet towing speed was 1 m s-1 and the flowmeter in the mouth of the
MultiNet estimated the volume of filtered water. Once onboard the
collected zooplankton samples were preserved immediately in 5 % buffered
formalin–seawater solution. At T3 and T5, 4 replicate day and night hauls
were conducted (resulting in a total of 8 hauls and 40 discrete samples
at these stations). At L6, 2 replicate day and night hauls were conducted
(4 hauls and 20 samples total) from 600 to 0 m depth. Each sample
corresponded to a different depth strata (30–0, 90–30, 150–90, 400–150 and
600–400 m depth). These strata were defined in according to distribution of
oxygen concentration and localization of the OMZ (Fig. 2). Then,
from the vertical profiles of oxygen and coinciding with the sampled layers
of the MultiNet, strata were defined as follows:
oxic mixed layer (OX-ML), a well-oxygenated stratum with
oxygen approaching air saturation (> 250 µmol O2 kg-1);
upper O2
gradient (oxycline), the level at which O2 reaches 4 % of the
surface O2 (Paulmier et al., 2006), of which the
base is located in the upper boundary of the OMZ (45 µmol O2
isoline, OMZ-UB)
(Escribano et al., 2009; Hidalgo
et al., 2005; Morales et al., 1999);
OMZ core, an upper boundary (OMZ-UC) with
the lowest concentration of O2 (< 20 µmol O2 kg-1);
lower boundary (OMZ-LC) (1 to < 20 µmol O2 kg-1);
lower O2 gradient (OMZ-LW).
Depth
ranges and oxygen levels for these strata are detailed in Table S2.
Vertical profiles of dissolved oxygen (O2),
temperature, chlorophyll a and water density (σt), at three stations off
northern Chile (see Fig. 1) during the Lowphox Cruise in the
austral spring 2015. Shaded areas represent different layers sampled with
the MultiNet and defined according to oxygen concentration. OX-M is the oxic
mixed layer, OMZ-UB is the upper boundary of the oxygen minimum zone, OMZ-UC is the upper core of the oxygen minimum zone, OMZ-LC is the lower core of the OMZ and
OMZ-LW is the lower oxygen gradient.
Taxonomic and size measurements
Taxonomic identification and enumeration of taxa were carried out by
analysis of digitized images obtained with the Hydroptic ZooScan digital
imaging system (Gorsky et al., 2010). Each sample was wet sieved
through a 1000µm mesh into two size fractions, although a few
samples were not split into two fractions, because they contained too few animals.
Then, each size fraction was fractionated again separately with a Motoda
splitter until the zooplankton concentration was sufficiently diluted to
avoid contact between organisms in the ZooScan scanning frame. Fractioning
into small and large organisms, and consequent separate image acquisition of
the two size classes prevented underestimates of large, rare objects which
may need less fractioning (Gorsky et al., 2010). A total of 179 subsamples were
scanned and digitized at a resolution of 2400 dpi after manual separation of
objects on the scanning tray. After processing the samples with ZooProcess
software, each of the objects was automatically sorted with the help of a
learning set, and then the sorting was visually validated by an expert (for
details, see Chang et al.,
2012; Gorsky et al., 2010). Organisms making up the ZooScan datasets were
enumerated, measured, biomass estimated and classified into 27 taxonomic
groups, such as copepods, chaetognaths, euphausiids, gelatinous and other
zooplankton. The volume-specific abundance (ind. m-3) of total
zooplankton or of each taxonomic group was calculated following Eq. (1):
Abundancem-3=N⋅SVol,
where N is the number of individuals with same identification (e.g. in last
column written “copepod”), S (subpart) is the splitting ratio and Vol is net volume stratum-integrated
abundance (ind. m-2) was obtained after multiplying by width (m) of a
given stratum.
Patterns of vertical distribution of migrating zooplankton
For the analysis of vertical distribution of organisms, the density
estimates of the organisms were standardized to number the of individuals per
cubic meter (m3) (for each stratum) or per square meter (m2) (for integrated values). In order
to quantify the presence and extent of DVM of various taxa at each station,
we calculated weighted mean depth (WMD) for zooplankton abundance, as a
measure of the center of gravity of a population's vertical distribution for
each taxon and haul, according to
Andersen et al. (2004) following Eq. (2):
ΣΣWMD=(ni⋅zi⋅di)(ni⋅zi),
where d is the mean depth of the strata (m), zi the width (m) of the strata and
ni the abundance (ind. m-3) of a given i taxonomic group.
We calculated the amplitude of vertical migration (ΔDVM) as the
difference between the WMD of the organisms during the day and the night, and
therefore this ΔDVM was considered as the criterion to assess the
DVM behavior for each taxonomic group. Positive values indicated normal DVM
(pattern of nocturnal ascent by individuals that reside at depth by day) and
negative values indicated reverse DVM (pattern of nocturnal descent by
individuals that reside near the surface by day). The individuals that
occupied the same depth stratum by day and by night, whether near the
surface or at depth, were considered as non migrant according to
Ohman (1990).
Biomass estimates and carbon fluxes
The ZooScan Integrated System also provided zooplankton body size in terms
of area (mm2) or volume (mm3) for each organism. We used the
organisms' area or volume to estimate dry weight of each
individual of different taxonomic groups using published regression
equations relating organism size, area or volume to individual weight as
detailed in Table S3. Mass unit conversions
between dry weight (DW) and carbon content (C) were performed using averaged
conversion factors obtained for different zooplankton groups
(Kiørboe, 2013) and ichthyoplankton (Childress
and Nygaard, 1973) (Table S3). Added biomasses
(µg C ind.-1) of individuals within taxonomic categories
identified by ZooScan allowed us to estimate total biomass per taxon (mg C m-3) for each sample by station, daytime vs. nighttime condition, and
depth strata. Integrated values of biomass per depth stratum (mg C m-2)
and taxon were calculated multiplying by the stratum width (m).
To calculate the migrant biomass, we integrated biomass in the upper 90 m
layer from our two sampled strata 0–30 m and 30–90 m. This 0–90 m stratum
was considered the approximate above-oxycline layer after examining the
vertical profiles of oxygen. Biomass at night was thus subtracted from the
corresponding day biomass in this layer to assess daily changes involving
migrants as in
Putzeys et al. (2011).
Thus, the negative values of the day–minus–night biomass corresponded to
migrant biomass that reached the epipelagic layer at night, including
organisms inhabiting above and below the oxycline.
The proportion of migrant biomass with respect to observed biomass in the
upper 90 m of a given taxonomic group was defined at the rate of migration
on a daily basis. This rate of migration could thus be used as an index of
DMV behavior for a taxonomic group. We additionally estimated daily migrant
biomass from the difference between day and night samples in the deeper
90–600 m layer (integrated data) and compared these estimates with those
from upper 0–90 m layer.
To estimate the active C flux at each sampling station, we considered three
processes contributing to C at depth mediated by migrant zooplankton:
respiration (R), excretion (E) and mortality (M) at depth. Respiration at
depth (> 90 m) was estimated using the equation provided by
Ikeda (1985) that relates individual respiration rate with
body mass and temperature (Table S2),
independent of taxonomic category, which may have a minor effect on R, according to a more recent assessment (Ikeda, 2014). Mean body
mass (µg C) for each taxonomic group from ZooScan estimates and mean
in situ temperature were used to obtain integrated R at each depth stratum.
Estimates of R for each taxonomic group are shown in Table S6. Integrated R per station for the 0–600 depth
strata along with the corresponding integrated biomass was then used to
estimate the fraction of C being respired at depth by zooplankton. The
contribution of C by excretion (E) at depth was assumed to be 31 % of R, as
suggested by Steinberg et al. (2000), and
daily mortality at depth (M) was considered to be in the range of 0.03 and
0.05, as suggested by Edvardsen et al. (2002), so that a median
value of 0.04 as a fraction of migrant biomass was assumed. Vertical C flux
mediated by zooplankton was thus estimated as,
CFlux=MBx[(R+M+E)/2)]
where MB is the migrant biomass (mg C m-2), R and M are daily
respiration and mortality (expressed as a fraction of migrant biomass), and
E is the C excretion expressed as 0.31 R. The three processes are divided by 2, assuming a 12 h incursion at depth. We did not include the contribution by
egestion at depth because of the lack of reliable estimates of ingestion rates
in the photic zone during our study.
Statistical analysis
For statistical analysis, as a criterion for determining if the DVM was
significant, we tested for differences in the WMD mean between day and night
using a two-tailed t test. We considered the occurrence of DVM when the
difference in the WMD mean between day and night was significant (p<0.05). In order to evaluate the similarity or dissimilarity in the abundance
and biomass among stations, strata and day–night conditions, multivariate grouping techniques were applied (“cluster analysis”), including ANOSIM
(two-way crossed analysis) tests and multidimensional scaling (MDS) with the
data transformed in PRIMER v 6.1.16 (2013) prior to the application of the
Bray-Curtis similarity index (Bray and Curtis, 1957). In general,
WMD for taxonomic groups did not exhibit a pronounced bimodal vertical
distribution.
ResultsHydrographic conditions
Across the zonal section off Iquique the offshore station (St. T5) and
onshore station (St. T3) showed two contrasting hydrographic regimes
regarding the OMZ. Station T5 had a less pronounced and thicker OMZ than
station T3. At both stations the five strata were well defined in the water
column (Fig. 2). The OX-ML (> 250 µmol O2 kg-1) was present at 18 m (St. T5) and 15 m (St. T3). The oxycline
gradually decreased from oxic (∼250µmol O2 kg-1) to suboxic (< 20 µmol O2 kg-1) conditions associated with a strong stratification in the upper
80 m depth. The 45 µmol O2 isoline (OMZ-UB) was at the base of
the oxycline at 70 m (St. T5) and 59 m (St. T3). The OMZ core (< 20 µmol O2 kg-1) was below the thermocline and
below the 26.5 kg m-3 isopycnal, following description of
Paulmier et al. (2006). In the oceanic station
(St. T5) the OMZ core was between 80 and 514 m, while in the coastal station
(St. T3) it was between 80 and 507 m with 423 m thickness. The O2
concentration in the OMZ core was ca. 1 µmol O2 kg-1. The
OMZ-LW at both stations was delimited above the core and below the depth
where the O2 slope changed significantly (slope break > 20 µmol m-1) (Fig. 2).
The structure of the OMZ at the coastal station (St. L6) off Coquimbo
(29∘ S) (Fig. 1) was similar to St. T3
(21∘ S), but in this area the OMZ was deeper and thinner.
The OX-ML was shallower. The OMZ -UB (45 µmol O2) in the base of
the oxycline was down to 80 m. The low O2 concentrations in the core
were less intense than at 21∘ S (4 to 20 µmol O2 kg-1), and it was located below 100 m (Fig. 2). The
OMZ-LW could not be assessed because of lack of CTD data below 350 m.
Additional oceanographic variables showed a surface warming (> 20 ∘C) and strongly stratified conditions at the three stations with
a sharp thermocline in the upper 100 m, coinciding with the oxycline,
whereas chlorophyll a maximum (> 5 mg chlorophyll a m-3was
in the upper 20 m (Fig. 2).
Zooplankton composition and abundance
A total of 27 zooplankton taxa were identified by the ZooScan and ZooProcess
(Table S4). The number of taxa varied among
stations and strata. Across the zonal section off Iquique the number of
taxonomic groups fluctuated between 23 (St. T3) and 26 (St. T5), whereas 25
taxa were off 29∘ S (St. L6). The most dominant taxa at both
daytime and night conditions were copepods 87 % (in St. T5), 79 % (in
St. T3) and 69 % (in St. L6). This group was constituted by small
copepods, large copepods, the eucalanid copepods and the Acartia spp copepods; fish
eggs constituting 2 % (in St. T5), 5 % (in St. T3) and 6 % (in St. L6); Nauplii being < 1 % (in St. T5), < 1 % (in St. T3)
and 7 % (in St. L6); Appendicularia 5 % (in St. T5), 4 % (in St. T3)
and 3 % (in St. L6) (Table S5). The
remaining 19 pooled groups only constituted < 6 % (in St. T5),
11 % (in St. T3) and 15 % (in St. L6). The total integrated abundances
of zooplankton (0–600 m) by sampling station are in Table S4. Based on a two-way crossed analysis
ANOSIM test, this water column integrated abundance did not show significant
differences between day and night samples (p>0.05). However, the
abundance of these zooplankton groups regarding stations was significantly
different (two-way crossed analysis ANOSIM, p<0.05), so that the
stations were treated independently. Off Iquique the abundance was the
lowest at the onshore station (St. T3 with 18 %), which was characterized
by the strongest and most extensive OMZ in the study area. These values
increased at the offshore station (St. T5 with 31 %), where the OMZ was
less pronounced and thicker. Unlike stations T3 and T5, the onshore station
off 29∘ S (St. L6) had a weaker and less extensive OMZ,
showing the highest zooplankton abundance (51 % greater).
Diel vertical migration (DVM) and vertical distributionMain migrant groups of zooplankton
The diel vertical migration of 27 zooplankton taxa in the 0–600 m water
column is in Fig. 3. These taxa were classified into four groups
according to their amplitude of migration (ΔDVM) (Table 1).
Group 1. Strong migrants, represented by taxa with a strong DVM and a
broad range of ΔDVM from 225 to 99 m (in St. T5), 440 to 84 m (in St. T3) and 208 to 87 m (in St. L6). This group constituted 70 % of taxa with
higher ΔDVM. The composition of taxa in this group was variable at
each station (Table 1), but in general this group was well represented by
eucalanid copepods (EC), euphausiids (EU), Acartia copepods (AC), ctenophores (CT),
decapods (DC), annelids (AN), Bryozoa L (BR), pteropods (PT) and
chaetognaths (CH). These taxa were mostly concentrated in the oxic surface
stratum (OX-ML) and the OMZ core, showing a strong
interaction with both the OMZ-UC and the OMZ-LC, and so
changing from normoxic to hypoxic conditions and vice versa between 0 and 550 m (Fig. 3).
Group 2. Intermediate migrants, represented by taxa
with a moderate DVM and a range of ΔDVM from 73 to 34 m (in St. T5),
70 to 27 m (in St. T3) and 49 to 22 m (in St. L6). This group constituted
23 % of taxa with moderate ΔDVM. The composition of taxa in this
group was also variable at each station (Table 1), but it was
mostly represented by small (SC) and large copepods (LC), Amphipods (AM),
Cirripedia larvae (CL), gastropods (GA), siphonophores (SIP) and
Appendicularia (AP). These taxa were mostly concentrated in the oxic surface
strata (OX-ML) and in the OMZ-UC, showing some interaction
with the OMZ core and vertically changing from normoxic to hypoxic
conditions, and vice versa between 0 and 200 m.
Group 3. Weak migrants, represented by taxa with a weak DVM and a range of ΔDVM of 24 to 18 m (in St. T5), 23 to 12 m (in St. T3) and 21 to 11 m (in St. L6). This group constituted 5 % of taxa with a of low range of ΔDVM. The
composition of taxa in this group was also variable at each station
(Table 1), but in general it was represented by Hydrozoa (HY),
salps (SA), Platyhelminthes (PT), Decapoda larvae (DL), ostracods
(OS), Nauplii (NL) and Ichthyoplankton (IC). These taxa were concentrated
mainly in the oxic surface strata (OX-ML) and in the OMZ-UP, but also in the OMZ-UC at the onshore stations
(Station T3 and Station L6), showing much less interaction with the OMZ core, while spatially moving from normoxic to hypoxic conditions
and vice versa between 0 and 100 m.
Group 4. Non-migrants, represented
by taxa which did not exhibit a significant DVM and had a range of ΔDVM from 16 to 0 m (in St. T5), 7 to 0 m (in St. T3) and 6 to 0 m (in St. L6). This group constituted 1 % of taxa with not significant ΔDVM.
The composition of taxa in this group was also variable at each station
(Table 1), but in general it was represented by fish eggs (FE),
radiolarian (RA) and echinoderm larvae (EL).
Weighed mean depth distribution (WMD) of the zooplankton
community interacting with the OMZ off Iquique (Stations T5 and T3) and off
Coquimbo (Station L6) at the northern upwelling area of Chile during the
austral spring 2015. Shaded gray areas represent different layers defined by
their oxygen levels (defined in Methods). The taxonomic groups were
classified by automated analysis (ZooScan): EC is eucalanid copepods, AM is amphipods, BR is Bryozoa larvae, AC is Acartia copepods, CT is ctenophores,
CL is Cirripedia larvae, OS is ostracods, CH is chaetognaths, PT is pteropods,
SA is salps, GA is gastropods, PL is Platyhelminthes, DL is Decapoda larvae,
FO is Foraminifera, HY is Hydrozoa, LC is large copepods, SIP is siphonophores,
EU is euphausiids, FE = fish eggs, NP is nauplii, SC is small copepods, AN is annelids, AP is Appendicularia, RA is radiolarian, DC is decapods,
IC = ichthyoplankton, EL = echinoderm larvae.
Diel vertical migration indices for 27 taxonomic groups
(Taxa) identified and sorted by ZooScan at three stations off northern Chile
(see Fig. 3 for acronyms), during the austral spring 2015. Amplitude
of migration (ΔDVM) is in meters. Positive values indicate normal
DVM and negative values indicate reverse DVM (see Methods). Four groups are
defined in according to DVM behavior. Relative abundances are shown in %.
T5 T3 L6 TaxaΔDVM%TaxaΔDVM%TaxaΔDVM%MigrantsEC22514EC-44028EC-20820StrongPT-18812EU14910AM11511migrantsEU18111BR-1298BR-10710> 5 %AN1459CH-1147AC-10310FO1268AN1057CT-949DC906AP-886CL-878CH886GA-845OS495SIP735LC-705CH353IntermediateAM644SC-705PT293migrantsCL513NP-423SA293> 2 %DL503AM423GA-273LC473FO-382PL262HY392SA322DL222SC342HY-272FO-222NP242PT-231HY212WeakSA231SIP-151LC192migrantsBR181CL121SIP151> 1 %IC-181OS-91EU111FE493FE-523FE252Non-OS161DL-70NP61migrantsGA151AC––SC-40< 1 %AP70IC––AN-40AC––CT––AP20CT––RA––RA––PL––DC––DC––RA––PL––IC––EL––EL––EL––Vertical distribution and DVM of dominant groups
Vertical distributions of zooplankton were assessed for 5 taxonomic groups,
which represented 80 % of total abundance in average: copepods represented
by small copepods, large copepods, eucalanid copepods and Acartia copepods;
euphausiids; decapods larvae; chaetognaths and annelids, as well as their
patterns of strata–station–abundance relationships are detailed in
Table S4. The abundance of these
zooplankton groups regarding depth strata was significantly different
(ANOSIM, p<0.05) at each station and therefore
represent distinctive microhabitats characterized by specific depth and
oxygen concentration. In general, the higher abundance
(> 80 %) was found in the shallower strata and well oxygenated
layers (OX-ML and OMZ UB) (> 250 µmol O2 kg-1), and then it decreased rapidly in the strata associated with
the OMZ core (OMZ-UC and OMZ-LC). Below this stratum a
second slight peak in abundance was in the OMZ-LW in special at
Sts. T5 and L6, occurring between 400 and 600 m, both daytime and night
conditions.
As expected, copepods numerically dominated the zooplankton community both
within and outside the OMZ. Small copepods (SC) were the most
abundant (70 %) followed by large copepods (LC) (6 %), whereas
the copepods Acartia (AC) and eucalanid copepods (EC) showed the lowest abundances
among copepods. The largest aggregation of copepods (pooled data) altogether
during the entire study period was at the offshore station St. T5 (87 %),
where abundances reached 192 088 ind. m-2. At the onshore station (St. T3) the percentage of the contribution of copepods was 79 % and 69 % at the
St. L6 (Table S5). Off Iquique, the highest
abundances were in the shallower strata (OX-ML) at St. T5 (46 %)
and at St. T3 (47 %), and they were reduced in the core of the OMZ at St. T5 (4 % to
1 %) and at T3 (8 % to 1 %) between 90 and 400 m, where oxygen was at the lowest
concentrations (< 20 µM to 1 µM). At the St. T5, the second
peak abundance was in the OMZ-LW stratum during daytime
condition, where oxygen levels increased after the extremely low levels
within the OMZ, while at the onshore station St. T3 it was much less and it was present during nighttime conditions. At the onshore station off 29∘ S (St. L6), which has a weaker and less extensive OMZ, the vertical distribution of
abundance was similar. However, the abundance of copepods was lowest in this
station (at about 69 %) in comparison with stations off Iquique, in the
core of the OMZ the percentage was between 5 % and 3 %.
DVM of copepods was pronounced at onshore stations (Stations T3 and L6), but
the strength of migration was higher overall at St. T3 off Iquique, as
reflected by the migration indices (WMD and ΔDVM) (Table 1). The WMD of these taxa had a broad range (17–500 m), which varied
significantly among copepods groups and stations, both in day and night
samples (p<0.05) (Fig. 3). During the night, at the
offshore station (St. T5) most copepods exhibited normal DVM, and they were
concentrated mainly in the oxic surface strata (OX-M) and OMZ-UB (40–60 m) without interacting with the OMZ; an exception were the eucalanid
copepods, which concentrated deeper in the OMZ-LC stratum
associated with the lower core of the OMZ and showing a high ΔDVM
(225 m). During the day these four groups of copepods tended to remain deeper
in the stratum associated with the lower core of the OMZ (OMZ-UC)
and lower O2 gradient (OMZ-LW), except for the small copepods that
remained at the OMZ-UB stratum with a smaller ΔWMD (34 m).
At the offshore stations (Stations T3 and L6) the DVM was reverse in most
copepods, except for large copepods (LC) that showed slightly normal DVM at
St. L6 off 29∘ S. At night copepods were concentrated deeper
in the stratum associated with the lower core of the OMZ (OMZ-U) and
lower O2 gradient (OMZ-LW), particularly Eucalanidae with a
strong DVM and high ΔWMD of 440 m (St. T3) and 208 m (St. L6) and
Acartia copepods with 103 m (St. L6) (Table 1). Whereas at St. L6 small
copepods (SC) were caught in abundance at the OMZ-UB stratum down
to 82–90 m depth, respectively (Fig. 3). During the day, copepods
remained shallower than at night, although they concentrated at different
depths. Small copepods were in the oxic surface strata OX-ML (St. T3) and remained in the upper boundary of the OMZ (St. L6) without
detectable DVM, as judging by the small difference between their daytime and
nighttime distributions (DVM ca. 4 m). Large copepods (LC), as expected,
showed a normal migration and stayed inside the OMZ, concentrated in the
OMZ-UC stratum (St. L6) and OMZ-UB (St. T3). Finally,
Eucalanidae with a strong DVM tended to distribute in the OMZ-UC
(St. T3) and the OMZ UB (St. L6) (Fig. 3).
Unlike copepods, the euphausiids were more abundant at the onshore Station L6 (< 1 %), where they reached up to 1683±473 ind. m-2 d-1. The OMZ-UB stratum was the most abundant in this station, with a
peak of abundance during the daytime, however no DVM was detectable, judging
by the small difference between their daytime and nighttime distributions
(Fig. 3). Off Iquique, the highest abundance was also in OMZ-UB
stratum at night, but with a second peak in OMZ-LC stratum during daytime in
both stations (Sts. T3 and T5) (Table S4). The
euphausiids appeared to perform a strong DVM in these stations (Fig. 3), with a vertical range between 236 and 56 m and a mean ΔDVM of
181 m at St. T5, and at St. T3 between 222 and 73 m with a mean ΔDVM of
149 m (Table 1).
Decapods larvae were more abundant at St. T5 (428±132 ind. m-2 d-1) and were associated with the OMZ-UB stratum, where they
performed a strong normal DVM with a vertical range between 120 and 30 m, and
a mean ΔDVM of 90 m (Table 1). At the offshore station
(St. T3), the surface peak of abundance was in the OX-ML stratum
during the day and in the OMZ-UB layer at night, where they
reached up to 292±62 ind. m-2 d-1, with a weak reverse DVM
(ΔDVM-7 m). Off Coquimbo (St. L6) they reached up to 400±88 ind. m-2 d-1, the OMZ-UB stratum was the most abundant,
with a slight second peak in the OMZ-LW stratum during daytime, at this
station the vertical range was between 70 and 48 m, with a mean ΔDVM
of 22 m (Fig. 3).
The largest aggregation of chaetognaths was at the onshore station St. L6
(∼2 %), where their abundances reached up to 4755±1038 ind. m-2 d-1. The abundance and biomass of this group
increased in the upper boundary of the OMZ (OMZ-UB) during day and
night. No DVM was discernible for this group in this station, because of the
slight difference between their daytime and nighttime distributions. By
contrast, off Iquique they appeared to perform a strong DVM between the
OMZ-UB and the OMZ-UC strata, as indicated by the
migration indices (WMD-ΔDVM) (Table 1). However, at the
onshore station (St. T3) they showed a reverse DVM.
The other main taxon, Annelida was more abundant at the onshore station St. L6, where their abundances reached up to 7395±847 ind. m-2 d-1 (Table S4). In the whole area, the
highest of abundance was in the OMZ-UB, however a second peak of abundance
was in the OMZ-LC during daytime at St. T5 and T3 and during the night at St. L6. The DVM of this group was high off Iquique with ΔDVM of 145 m
(St. T5) and 105 m (St. T3), while at St. L6 off Coquimbo no DVM was
discernible for this group.
Others groups with vertical distribution associated to OMZ UC
The remaining 19 groups constituted 11 % (in St. T5) 17 %, (in St. T3)
and 27 % (in St. L6) in abundance. The DVM behavior was variable at each
station, but in general it was normal at St. T5 and reverse at Sts. T3-L6
(Table 1). These groups clearly exhibited different daytime and
night depths associated with the OMZ core (OMZ UC-LC). Overall,
they tended to reside deeper by day and shallower by night in St. T5 than at
the other sites (Fig. 3).
Vertical distribution of zooplankton biomass
Estimates (mean ± SD) of biomasses of the taxonomic groups integrated
by depth strata are summarized in Table 2. These data, averaged
from day and night measurements, contrast with the numerical abundances,
which were dominated by copepods. In this case, the bulk of zooplankton
biomass was dominated by different groups depending on stations. In terms of
biomass, copepods, euphausiids, decapods L., chaetognaths and annelids
accounted, more or less equally, for > 84 % in the whole area
(Table 2). At the stations less affected by the effect of OMZ, the
bulk of biomass was dominated by copepods ∼50 % at St. T5
and ∼40 % at St. L6, while decapods largely dominated the
bulk of biomass at Station T3 (∼40 %), followed by
copepods (19 %) and euphausiids (16 %) (Table 2).
Mean and standard deviation (±) of integrated
biomass (mg C m-2) by taxonomic groups identified and sorted by ZooScan
during daytime and nighttime conditions at three stations (T5, T3 and L6)
sampled off northern Chile, during the austral spring 2015. Mean ± SD
are from n=8 for Stations T5 and T3, and n=4 for
Station L6.
When assessing the day vs. night vertical distribution of taxonomic groups
in terms of their contribution to biomass, different patterns arise compared
to numerical abundance. In this case, we used nine taxonomic categories to
examine vertical distribution and DVM in terms of biomass: small copepods
(SC), large copepods (LC), Acartia copepods (AC), eucalanid copepods (EC),
euphausiids (EU), decapod larvae (DL), chaetognaths (CH), annelids and all
the other taxa (Fig. 4). Contrasting with numerical abundance, the
vertical distribution of biomass was more heterogeneously divided among
taxonomic groups, and DVM patterns vary strongly between stations. Small
copepods continue to dominate at the St. T5 (24 %), with two peaks of
biomass, a surface peak associated to the upper oxic layer (OX-ML)
and OMZ-UB stratum during night condition, and a second peak associated to
deeper stratum (OMZ-LW) during daytime. At the onshore Stations T3 and L6
the biomass had a similar vertical distribution but lower (∼7 %). At the Station T3 the peak of biomass was in the upper oxic layer
(OX-ML) during daytime condition and then it decreased sharply
within the OMZ-UB and within the OMZ core (OMZ-UC and
OMZ-LC). This abrupt decrease in biomass coincides with the intense
OMZ present at this station T3. The second peak of biomass during daytime
was in deeper stratum (OMZ-LW), where oxygen conditions seem to be restored.
Large copepods dominate at the onshore St. L6 (30 %), where their biomass
reached up to 1727.49±340.8 mg C m-2 d-1 (Table 2). A surface peak of biomass was associated with OMZ-UB stratum during
daytime condition, and a second peak was associated with deeper stratum (OMZ-LW)
also during daytime. Off Iquique, they were the second dominant group with a
surface peak in OX-ML stratum during night at St. T5 and during daytime at St. T3,
and with a second peak in the deeper stratum (OMZ-LW) during daytime in both
stations (Fig. 4). The biomass of Eucalanidae and Acartia copepods
were lower than the other copepods in the whole area, but in general
Eucalanidae were associated to the deeper stratum.
Daytime vs. nighttime vertical distribution of biomass of
dominant taxonomic groups at three stations off northern Chile: off Iquique
(Stations T5 and T3) and off Coquimbo (Station L6). Data are from night and
day replicated samples during 2 consecutive days in the austral spring 2015. Values represent means from sampling size n=4 for Sts. T5 and T3,
and n=2 for St. L6.
Following copepods, euphausiids were the second dominant group in term of
biomass in the whole area. In general, their ascent from deep layers to the
upper ones at night was also evidenced by increasing proportions of this
group in the OMZ-UB stratum at night. The highest biomass was in St. L6
(19 %), where it reached up to 1060.58±305.8 mg C m-2 d-1 (Table 2). A surface peak of biomass was associated to OMZ-UB
stratum during night conditions, decreasing in the deep strata (Fig. 4). Across of the zonal section off Iquique, two peaks of biomass were in both
stations. A surface peak was in OMZ-UB stratum during night condition
followed by lower biomass within the OMZ core, then a second peak was in the
OMZ-LC during daytime.
Decapod larvae clearly dominated over copepods in the St. T3 (39 %). The
high biomass was in OMZ-UB stratum during night conditions followed by lower
biomass within the OMZ core. During night condition at the St. L6, a second peak of biomass was observed. Chaetognaths and annelids were other groups with
an important vertical movement of biomass between day and night across
strata, and like other groups they had two peaks of biomass. The high biomass
was at St. L6 in both groups (Fig. 4).
Total added biomass of zooplankton revealed more clearly DVM behavior of
the whole zooplankton community (Fig. 5). The vertical distribution
and daytime vs. nighttime variability of zooplankton biomass showed
distinctive features associated with the OMZ structure, with significant
differences (p<0.05) between strata for both daytime and nighttime
samplings, as based on the ANOSIM test (p<0.05). In the whole area
most of the biomass was concentrated in a narrow band within the OX-ML and
OMZ UB strata associated with more oxygenated surface waters, with reduced
values in deeper waters associated with the OMZ core, especially at the
onshore station off Iquique (St. T3) (Fig. 5). Overall, we observed that
highest values of biomass were during the night at the shallower sampling
stratum (Ox-ML) and in the subsurface during the day. There was also an
important increase in biomass at the deepest stratum (OMZ-LW) during daytime and night conditions.
Vertical distribution of total zooplankton biomass during
daytime and nighttime conditions at three stations off northern Chile: off
Iquique (Stations T5 and T3) and off Coquimbo (Station L6) during 2 consecutive days in the austral spring 2015.).
Migrant biomass of the zooplankton taxa
The migrant biomass of the zooplankton taxa and the rate of migration (RM),
represented by the proportion of biomass (%) being vertically moved daily
from the upper 90 m, are shown in Table 3. Most dominant groups
showed a high rate of migration as reflected in the RM. In terms of migrant
biomass, Decapod larvae, euphausiids, decapods, copepods and chaetognaths
accounted for a large proportion of total migrant biomass (81 %), although
high estimates of migrant biomasses were also associated with high standard
deviations, indicating a strong variation among replicated samples
(Table 3). Presence of zero values in Table 3 represents
absence of a given taxonomic group in the upper 90 m layer or extremely low
values of biomass under both daytime and nighttime conditions (such groups
did not contribute or had a non-significant contribution to total
migrant biomass).
Migrant biomass (mg C m-2) and rate of migration (RM)
(%) for taxonomic groups of zooplankton sampled off northern Chile at three stations: off Iquique (Stations T5 and T3) and off Coquimbo (Station L6)
during the austral spring 2015. RM represents the proportion (%) of
migrant biomass with respect to total biomass found at night in the 0–90 m
for a given taxonomic group. SD is standard deviation of the migrant biomass
estimated from n=4 (Sts. T5 and T3) and n=2 (St. L6).
Studies on zooplankton DVM and the active transport of C mediated by
zooplankton have been documented previously for the Pacific Ocean and for
other areas of the world's oceans, as summarized in Table 4.
However, downward C flux due to DVM in highly productive upwelling regions,
such as northern Chile, which is also characterized by severe subsurface
hypoxic conditions upon presence of a shallow OMZ, is still poorly
understood. Some studies have shown that hypoxic conditions can interfere
with DMV of many meso- and macrozooplankton species
(Wishner
et al., 2013; Ekau et al., 2010; Escribano et al., 2009; Apablaza and Palma, 2006; Antezana, 2002;
Escribano, 1998). These studies have shown that small differences in oxygen
concentration can make a large difference for zooplankton behavior,
physiology and adaptation
(Wishner
et al., 2018; Kiko et al., 2016; Seibel, 2011; Gonzalez and Quiñones, 2002;
Escribano and McLaren, 1999). Therefore, it seems
that the OMZ can play a very significant role influencing vertical
distribution, DVM and ultimately the downward C flux mediated by
zooplankton.
Comparison of active transport of carbon (AC) (mg C m-2 d-1) by vertically migratory taxa in Pacific Ocean. Diel
vertically migratory taxa (DVM), productivity primary (PP) (mg C m-2 d-1), migrant biomass (MB) (mg C m-2), respiratory loss (R) (mg C m-2 d-1), faecal pellets production (F) (mg C m-2 d-1)
and mortality (M) (mg C m-2 d-1). Where provided by authors,
estimated passive export (POC) is listed. Fluxes refer to carbon export
beneath the epipelagic zone (150–200 m depth, depending on the study) in mg C m-2 d-1.
LocationTaxaPPMBACRFM% POCReferencesN.Hawaii ALOHADVM zooplankton108–2167.12.6–4.812–18Al-Mutairi and Landry (2001)N. Hawaii ALOHA157.93.2–13.63.718Steinberg et al. (2008)N.W. Pac.DVM Metridia418144935123.1–61.8Kobari et al. (2008)N.W. Pac.DVM copepods822.3Takahashi et al. (2009)N.E. Pac.Mesopelagic fishes17023.9Davison et al. (2013)Eastern Equator96.0±25.24.2±1.22.9±0.818.4Zhang and Dam (1997)Eastern EquatorDVM zooplankton154.8±32.47.3±1.45.4±1.125.4Zhang and Dam (1997)Central Equator (HNLC)52.964Rodier and Le Borgne (1997)Western Equator46.936Rodier and Le Borgne (1997)E. Eq. Pac.DVM zooplankton12147.17.1204Rodier and Le Borgne (1997)Western EquatorDVM zooplankton144–44723.53–9.977.3–19.12.6–4.413–35Hidaka et al. (2002)Equator divergence2.8–21.80.9–1.2< 1–2Roman et al. (2002)Oligotrophic area30.2–33.81.3–1.74Roman et al. (2002)E. S. Pac. N. Chile5503Gonzalez et al. (1998)E. S. Pac. N. Chile10 000Daneri et al. (2000)E. S. Pac. N. ChileDVM Eucalanus8.0–3414.1Hidalgo et al. (2005)E. S. Pac. N. ChileDVM zooplankton37 81072006700Escribano et al. (2009)E. S. Pac. N. ChileDVM zooplankton2833±1155958±77871±64This study
Our approach to assess downward C flux into the oxygen minimum zone, based
on estimates of the migrant biomass and our proposed migration indices,
allowed us on one hand to examine the contribution that different
zooplankton can have to the vertical flux of C and hence export production. On the other hand, it allowed us to assess zooplankton responses (e.g. vertical
distribution and DVM performance) to changes in environmental conditions
over the vertical gradient, such as temperature, water density and the
abrupt changes in oxygenation levels. In this subtropical upwelling region,
vertical gradients are much stronger than in temperate upwelling zones. For
example, the coastal zone in this region is more stratified and has a very
shallow OMZ (< 50 m) with a weak seasonal signal and moderate
upwelling throughout the year
(Paulmier
and Ruiz-Pino, 2009; Fuenzalida et al., 2009; Escribano et al., 2004). This means that
zooplankton must cope with hypoxic conditions during their entire life
cycle, except for some species that may reside in near surface water
(< 30 m), such as C. chilensis and C. brachiatus which have been reported as mostly
restricted to the upper layer without performing any substantial DVM
(Escribano
et al., 2012, 2009; Escribano and Hidalgo, 2000; Escribano, 1998).
The vertical distribution and diurnal variability of zooplankton biomass
seem to be disturbed by the OMZ, such that high biomass aggregates above the
oxycline in a narrow band within the OX-ML and OMZ-UB layers, associated
with more oxygenated surface waters, whereas extremely low biomass reside in
deeper waters, in particular within the OMZ core. This condition was more
evident in the coastal station off Iquique (St. T3), characterized by the
most intense OMZ in the whole study area. In the eastern tropical North
Pacific, biomass distribution seemed different, exhibiting a secondary peak
at depth during the daytime within the upper oxycline or OMZ core
(Wishner et al., 2013).
Regarding the estimates of biomass for each of the taxonomic groups, our
approaches can certainly introduce variation, depending on selected
regressions and conversion factors from highly diverse body shapes and body
densities of the zooplankton taxa affecting the estimates of body area and
volume, dry weight and C content. Various approaches have been adopted for
converting sizes to body masses. For example,
Lehette and Hernández-León (2009) provided
some general regression equations for subtropical and Antarctic zooplankton
describing the relationship between scanned area and body mass (C content).
These authors also proposed two separate regressions for crustacean and
gelatinous zooplankton, because of different body densities. In our study,
we adopted more direct estimates of body masses by converting individual
areas or volumes (from ZooScan) using published regressions for separate
taxonomic groups. Also, in our samples there was a high diversity of
taxonomic groups as identified by ZooScan, such that unique regressions for
crustacean and gelatinous organisms may lead to strong biases in body mass
estimates, because of high variability in C content, which is the key
component of body mass needed to estimate C flux. Therefore, the use of
taxa-specific conversion factors, as those detailed in our Table S3
is strongly recommended.
Mean net primary production rate and estimates of daily
downward C flux due to passive sinking and mediated by diel vertical
migration (DVM) of mesozooplankton at three stations (T5, T3 and L6) in the
coastal upwelling region off northern Chile during the austral spring 2015.
Primary production represents satellite-based estimates of monthly mean
(November–December 2015) at the three sampling stations. Passive C flux is a
mean value estimated from sediment traps by González et al. (2000) off
Antofagasta (northern Chile, 23∘ S) for January 1997. Total
biomass and epipelagic biomass are mean observed values from day–night
conditions after 2 consecutive days of sampling.
Despite the apparently hostile oxygen-deficient habitat, associated with the
OMZ, we found that most taxa were able to perform DVM in the upwelling zone
withstanding severe hypoxia. Even, several zooplankton groups are strong
migrants, exhibiting large DVM amplitude (∼500 m). Among them, an
important migrant group is comprised by the eucalanid copepods, which have
been described as even being able to enter the core of the OMZ and then
migrate downward to the lower limit of the OMZ, which is slightly more
oxygenated (Hidalgo et al., 2005). In our
study however, their contribution to total migrant biomass was too small
(ca. 0.4 mg C m-2 d-1), as compared to the estimate made by
Hidalgo et al. (2005). In fact, the
migrant biomass and rate of migration of this group was non-significant when
considering DVM between the upper 90 m and below, suggesting a little or no
contribution to downward flux of C for this group of copepods. However it
seems that eucalanid copepods remain below the oxycline or nearby the base
of the oxycline day and night, as shown by their weighted mean depth (WMD)
and therefore suggesting that they may still contribute to vertical flux by
feeding at the base of the oxycline at night and then migrating into the OMZ
during the day.
Other taxa, such as euphausiids, Acartia spp., other copepods, ctenophores,
decapods, Annelidae, Bryozoa L, pteropods and chaetognaths tended to
concentrate their populations inside the OMZ core showing a strong link to
the OMZ with important movement throughout the water column.
Antezana (2010) showed that E. mucronata, an endemic and abundant euphausiid in the coastal
upwelling zone off Chile, is a well-adapted species to vertically migrate
into the core of the OMZ. In fact, the euphausiids studied here showed a
large DVM amplitude (∼250 m), descending into the core of the OMZ and
below 250 m each day. In general, all strong migrants' taxa showed a strong
interaction with the core of OMZ, remaining there either temporarily or
permanently during day or night conditions, contributing in this way to
the release of C below the thermocline, despite presence of hypoxic
conditions.
Our estimates of DVM-mediated C flux showed that migrant biomass (958±778 mg C m-2 d-1) and C flux estimates (71±64 mg C m-2 d-1) of the major taxa performing DVM were greater than those reported
for the Pacific Ocean, both in oligotrophic, such as Hawaii, and mesotrophic
waters such as the subarctic North
Pacific (Steinberg
et al., 2008), and even greater than that informed
by Yebra et al. (2005)
within eddies with enhanced biological production. Most of these previous
estimates however have not been done in regions with severe hypoxia or
anoxia at mid water depths (e.g. Kiko et al., 2016), such as
the highly productive upwelling region of the coastal zone off northern of
Chile, where the oxygen concentrations may fall below < 1 µmol
in the core of OMZ (Paulmier
and Ruiz-Pino, 2009). Moreover, only few works have considered the whole
zooplankton community (Table 4). High productivity and strong
aggregation of zooplankton in coastal areas of this region
(Escribano et al., 2000; Escribano and
Hidalgo, 2000) may promote greater amounts of migrant biomass. This requires
however that DVM should not be majorly constrained by presence of the OMZ
and that most migrant taxa are tolerant to low oxygen. On the other hand,
our estimates of downward C flux were substantially lower than previous ones
reported off northern Chile by
Hidalgo et al. (2005) for Eucalanus inermis alone (14.1 mg C m-2 d-1). Although, such previous estimates may be too
high, considering the level of primary production in the upwelling zone of
Chile (∼10000 mg C m-2 d-1, the maximum estimated value)
(Daneri
et al., 2000). It should be noted that potential contribution to C at depth by
faecal pellet production (egestion) was not considered in our estimate of
active transport. The lack of an estimate of ingestion rates at the upper
layer (nominally 0–90 m) precludes us to make reliable calculations of
egestion at depth. We also consider that in situ production of faecal
pellets at depth (below the thermocline) and its actual contribution to
active transport of C need further study, and it should be estimated for
particular feeding conditions.
Differences in our estimates with previous works may also be accounted for by
strong variability of zooplankton abundance in the upwelling zone. In fact,
our estimates of migrant biomasses of the different taxonomic groups based
on 2 d of sampling and two replicates for each condition (day and night)
are strongly variable, as shown by the standard errors in Table 3,
which can be as much as 100 % from the mean value. Therefore, comparisons
must take caution upon strong time–space variation when assessing
zooplankton abundance. Nevertheless, a strong spatial variation in migrant
biomass was also evident when comparing the three sampling stations. For
instance, St. L6 had more biomass than the other stations, but much less
migrant biomass in the upper layer (Table 5), and thus a very low
contribution to vertical flux of C by DVM. At station L6, large copepods,
euphausiids, annelids and chaetognaths largely contributed to biomass,
although they did not show significant DVM. Therefore, species composition
and their DVM behavior appear as a key factor to determine the downward
flux of C mediated by active transport. Even although the OMZ did not
greatly prevent DVM migration, zooplankton behavior appeared disrupted or
exhibited reversed patterns, depending on vertical distribution of OMZ and
on the taxonomic group being considered. This behavior was more evident at
the onshore stations (Stations T3 and L6), but in particular at the station
off Iquique (St. T3) that also showed a higher migration rate (60 %).
According to Ekau et al. (2010), other
indirect effects could also be caused by the hypoxic conditions, such as
changes in prey availability, prey size or predation risk, as well as
changes in species composition, the strength of which depends on the
duration and intensity of the hypoxic events. This could explain why
individuals with in a single population can perform reverse, normal, or non
DVM, apparently depending on the more important sources of mortality:
predation by nocturnal feeding, normally migrating carnivorous zooplankton
or visually hunting planktivorous fish (Ohman, 1990). These kind
of DVM behaviors can only be better assessed and understood when looking at
the population level, although again time–space variation in zooplankton
abundance in a highly heterogeneous upwelling zone should be kept in mind.
It is important to consider that our automated analysis of the zooplankton
community may not account for differences in species composition between
stations or between strata, and therefore changing DVM behavior within assigned groups
between stations, such as strong migrants, or non-migrants may obey to
variable species compositions. Although the possibility that same
populations change their DVM performance depending on changing environmental
conditions cannot be discarded, in particular referring to vertical
distribution of oxygen. Such effects may provide explanations for observed
variation in migrant biomass between stations, but also between strata. In
fact, we noted strong differences in estimates of migrant biomass when
comparing the upper 0–90 m stratum and the deeper 90–600 m stratum
(Table 5, also by taxa in Table S7). Furthermore, sampling biases should also be considered,
especially when using a vertically towed MultiNet which may not properly
sample large-sized zooplankton at daytime conditions in the 0–90 m because
of net avoidance, introducing a source of variation when comparing
surface vs. deeper layers under daytime and nighttime conditions.
Concerning C fluxes, our estimates of active transport of carbon by
zooplankton were about half the estimates of passive C sinking obtained off
northern Chile at 60 m depth off Antofagasta (23∘ S) by
Gonzalez et al. (1998) based on sediment traps (125 to 176 mg C m-2 d-1). Regarding the efficiency of active C
transport mediated by DVM, we obtained satellite-based (http://www.science.oregonstate.edu/ocean.productivity/, last access: 17 December 2019) estimates of net
primary production (monthly means for November–December 2015) for the
coastal area (Stations T3 and L6) and for the coastal transition zone (Station T5), averaged for the months of November and December 2015. Our estimates of
downward C flux represented a mean of ca. 4 % of export of carbon
resulting from net primary production in the upwelling region, estimated in
the range of 1500–3500 mg C m-2 d-1 (Table 5). If we consider this is accounted only by mesozooplankton, then an
important fraction of freshly produced C might be taken downward by
zooplankton, and this DVM-mediated C flux ought to be taken into account
when analyzing and modeling the C budget in the upwelling zone.
Conclusions
In the coastal upwelling zone off northern Chile the presence of a
subsurface oxygen minimum zone (OMZ) can impose an important constraint for
diel vertical migration of zooplankton and so influences the downward C
export mediated by zooplankton. We found that most of the zooplankton
biomass aggregates above the oxycline associated with more oxygenated
surface waters, and this was evident upon presence of a more intense OMZ.
Some taxonomic groups, however, were found closely associated with the OMZ,
and several taxa were able to perform DVM in the upwelling zone withstanding
severe hypoxia. Also strong migrants, such as large sized copepods and
copepods of the group Eucalanidae and euphausiids, can exhibit a large
migration amplitude (∼500 m), remaining either temporarily or
permanently during day or night conditions within the core of the OMZ,
and so contributing to the release of C below the oxycline (and
thermocline). Our estimates of DVM-mediated C flux suggested that a mean
migrant biomass of 957.7 mg C m-2 d-1 may contribute about
71.1 mg C m-2 d-1 to the OMZ system through respiration,
mortality and C excretion a at depth, accounting for ca. 4 % of the net
primary production and thus implying the existence of a efficient mechanism
to incorporate freshly produced C into the OMZ. This downward C flux
mediated by zooplankton DVM is however strongly dependent on the taxonomic
structure due to variable migration amplitude and DVM behavior. These
estimates should also consider the strong temporal–spatial variation in
zooplankton abundance in the upwelling zone for comparison purposes.
Data availability
Data from this study have been deposited on the PANGEA server (https://doi.pangaea.de/10.1594/PANGAEA.911368, Tutasi and Escribano, 2020, last access: 28 January 2020) upon publication.
The supplement related to this article is available online at: https://doi.org/10.5194/bg-17-455-2020-supplement.
Author contributions
Both authors have equally contributed to the research and writing of the work.
Competing interests
The authors declare that they have no conflict of interest.
Special issue statement
This article is part of the special issue “Ocean deoxygenation: drivers and consequences – past, present and future (BG/CP/OS inter-journal SI)”. It is a result of the International Conference on Ocean Deoxygenation, Kiel, Germany, 3–7 September 2018.
Acknowledgements
This work has been funded by the Millennium Institute of Oceanography (IMO)
(grant no. IC 120019) and the CONICYT Project (grant no. AUB 150006/12806) through
which the Lowphox I cruise was conducted. We are thankful to the two anonymous
reviewers who greatly contributed to improving our work. We are also grateful
to Daniel Toledo for assistance during field work. The work is a contribution to
IMBeR Program and SCOR EBUS WG 155.
Financial support
This research has been supported by the Millennium Institute of Oceanography (grant no. IC 120019) and the CONICYT (grant no. AUB 150006/12806).
Review statement
This paper was edited by Hermann Bange and reviewed by two anonymous referees.
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