Discussion
Diel migrators spend time in the ODZ
core
Organisms of all sizes appear to migrate into the core of the ODZ at our
site. Most migrators appear to leave the surface at dawn, spend the day
in the top 500 m of the ODZ and return to the surface at dusk (Figure
2A), while others show the opposite pattern, leaving the surface at dusk
and returning at dawn (Figure 2B). Diel migration is prevalent
throughout the oceans (Cisewski et al., 2010; Hays, 2003; Heywood, 1996;
Jiang et al., 2007; Rabindranath et al., 2011; Sainmont et al., 2014;
Yang et al., 2019), including at Oxygen Minimum Zone (<20 μM
O2) sites (Antezana, 2009; Kiko et al., 2020;
Riquelme-Bugueño et al., 2020), and highly anoxic ODZ sites (Bianchi et
al., 2014; Herrera et al., 2019; Hidalgo et al., 2005). Sampling efforts
in the Costa Rica Dome, a unique system in the ETNP, find that
euphausiids and fish migrate into the ODZ (Maas et al., 2014; Wishner et
al., 2013), but that diel migrators are primarily 2 mm–5 mm in size
(Wishner et al., 2013). Krill in the Humboldt current OMZ similarly
spend the day at depth and migrate to the surface at night
(Riquelme-Bugueño et al., 2020). The presence of organisms that appear
and disappear just above the base of the photic zone, in the region of
the deeper anoxic fluorescence peak region, but absence of a tell-tale
signature of mass migration before or after they appear (Figure 2C) may
suggest that these organisms migrate at different times of the day to
this deep region, rather than all at once. Another possibility is that
they pass through our station at this depth in mid-day, but migrate to
depth at another location.
The organisms that appear between
500 m and 1000 m (Figure 2E) have acoustic signatures that resemble
those of jellyfish (Kaartvedt et al., 2007), but could also represent
other organisms such as salps (Maas et al., 2014; Ressler, 2002). They
appear in horizontal bands that do not appear to trend upwards over time
which suggests that these swarms are traveling through our site at
progressively shallower depths over the course of the day, but that the
individual swarms are not themselves moving upward at this station. This
pattern indicates that any vertical migration by these organisms happens
elsewhere or occurs more slowly than the advection seen at this site.
That they appear at different depths at different times of the day
suggest that these organisms have some sort of vertical migration
pattern. Future work may consider more highly resolved spatial and
temporal monitoring of this phenomenon. Indeed molecular surveys have
found evidence of both Cnidarians and Ctenophores both within and below
the ETSP ODZ near Chile (Parris et al., 2014).
Flux is lower at this site than previous measurements in the
ETNP
Flux at P2 was lower at all depths, ranging from
10–100 μmol/m2/day, than was seen in previous
measurements by traps at other, more productive, ODZ sites, which ranged
from 1000–10000 μmol/m2/day (Hartnett & Devol, 2003;
Van Mooy et al., 2002).
The flux to size relationship is typical of other
sites
The exponent of the particle size to flux relationship that we saw at
our site (2.00) is of a similar magnitude to, but slightly smaller than,
those seen by other studies that compare UVP flux to trap flux (Guidi et
al., 2008; Kiko et al., 2020). Differences in the size-flux relationship
could indicate that this relationship truly varies between sites, or
that imprecision in flux measurements leads to differences in these
values between studies. The single fit relationship that we carried out
does not account for variation in the size to flux ratio across time and
depth, nor does it account for differences in particles of different
origin. In practice, this value could change over depth and time.
Setting up, deploying and retrieving each trap array is a large effort.
However, coupled particle flux and size measurements that are more
resolved with respect to depth, space or time might allow for further
exploration of the spatiotemporal variability of this relationship. In
other systems, combined image analysis and gel traps (McDonnell &
Buesseler, 2010, 2012) have provided opportunities to explore particle
size to flux relationships and how they vary between particle types in
more detail.
Remineralization rates of all particles decrease in the ODZ,
but disaggregation does
not
Particle size profiles, particle size distribution slopes, and estimated
biovolume, averaged across all casts and smoothed, are all similar to
the predictions made by Weber and Bianchi’s (2020) “Model 1”.
(Figure 5), and therefore our
hypothesis H1 , that all particles are remineralized more slowly
than in oxic sites. This suggests that the low oxygen at this site
decreases the remineralization rate of all particles, including
<500 μm microaggregates. It does not support the H2in which disaggregation is suppressed in the ODZ, nor H3 in
which only the very large particles’ remineralization is slowed due to
sulfate reduction. The data at the oxic site generally conformed to
Weber and Bianchi’s null model, “Model 0”, which was their prediction
for particle distributions at oxic sites (2020). However, one difference
was that the observed particle size distribution slope, while
essentially constant from the base of the photic zone through 1000 m,
appeared to steepen between 1000 m and 2000 m, suggesting an increase in
the abundance of <500 μm particles, relative to Model 0. This
could indicate increased disaggregation in this region or horizontal
transport of small particles through advection in this region. A similar
though less abrupt steepening of the particle size distribution slope
was visible at the ODZ station.
One possible source of
disaggregation in the ODZ are zooplankton communities that have been
found to specialize in feeding in the lower oxycline (Saltzman &
Wishner, 1997; Wishner et al., 1995).
These communities actively seek
out the lower oxycline and feed on particles that have escaped
remineralization in the ODZ, potentially resulting in the increased
disaggregation we observe in this depth interval. Such a community would
likely be comprised primarily of small organisms which the EK60 is not
able to measure at this depth. One possible source of horizontal
transport is colloids in a deep iron plume (Homoky et al., 2021; Lam et
al., 2020).
Zooplankton likely transport organic matter into the ODZ
core
Predicted flux levels sometimes increase between 275 m and 625 m, and at
all other times attenuate very slowly in this region. The EK60 data
suggest the diel migration of all sizes of organisms to this region,
agreeing with previous analysis of copepods collected with nets (Wishner
et al., 2020). Taken together, the concurrent intermittent increases in
flux with diel migration in the top 500 m suggests that zooplankton are
transporting organic matter. The observation that the rate of change in
flux changes with depth suggests some day-to-day variability in this
transport. That this rate does not vary statistically significantly
between day and night suggests that any diel release of particles is
relatively small compared to the particles already present in situ.
Indeed, it suggests that particle sinking is slow enough that any
particles that are transported to depth during the day are retained at
night. Furthermore, nocturnal migrators are likely playing a role in
carbon transport which may smooth out any diel signal. Another
possibility, given that the magnitude of the day-to-day variability in
apparent particle flux is small, is that the zooplankton themselves,
which likely make up about 5% of what the UVP counts as particles, may
be driving this apparent pattern and that particle flux itself does not
vary. More likely, especially given the observation that this flux
variability did not track well with the within day backscattering
patterns seen by the EK60 and the small number of particles that are
zooplankton, is that this factor accounts for some, but not all, of the
observed variability in flux. An additional source of temporal
variability in flux is variation in particle export from the photic
zone. Zooplankton, if they are
more common in large particle size bins, or even if they have a flatter
size distribution spectrum than non-living particles, will flatten the
particle size spectrum, where they are present. However, this effect, if
present at our site, appears to be overpowered by
the disaggregation effect, since
the particle size spectra appear to be steeper where zooplankton are
present.
Zooplankton are also known to congregate at the lower boundaries of ODZs
(Wishner et al., 2018, 2020) and high urea concentrations in the lower
oxycline of the ETNP have been suggested to be due to these zooplankton
(Widner et al., 2018). Beam attenuation indicates a third peak in the
oxycline below the ODZ. We do not see this congregation in the EK60
data; which is unsurprising as the EK60’s 12000 and 20000 kHz signals do
not penetrate to 1000m in our data. The EK60 data do however suggest
that larger, krill to fish sized organisms are not abundant in the lower
oxycline.
Zooplankton likely disaggregate particles in the ODZ
core
The observation that there is greater flux by microaggregate particles
(< 500 μm) than would be predicted by remineralization and
sinking alone (Figure 7), between the photic zone and 500 m suggests
that some process is disaggregating large particles into smaller ones.
That this apparent disaggregation corresponds with the region where
migratory organisms are found suggests that some of these organisms,
likely small animals such as copepods and euphausiids (Herrera et al.,
2019; Maas et al., 2014), may break down particles (Dilling &
Alldredge, 2000; Goldthwait et al., 2005). While, in principle, other
processes such as horizontal advection of water containing
<500 μm particles (Inthorn, 2005) could be responsible for
this increase in <500 μm particles, there is no reason to
expect horizontal differences at this site, which is at the core of the
ODZ and far from shore.
Other deviations from model assumptions could alternatively explain the
increase in <500 μm particles relative to model predictions.
In particular, smaller particles might break down more slowly than
larger ones, or sink more quickly for their size than expected, as has
been seen elsewhere (McDonnell & Buesseler, 2010). Our model assumes a
spherical particle drag profile, such that the particle sinking speed
fractal dimension (γ) is one less than the particle size fractal
dimension (α) (Cram et al., 2018; Guidi et al., 2008), and that these
two values sum to the particle flux fractal dimension. If any of these
assumptions do not hold, the magnitude of the values may differ.
In contrast to the upper ODZ core, there is an apparent flattening of
the particle size distribution below 500 m, beyond the expected effects
generated by particle remineralization. This could suggest aggregation
processes (Burd & Jackson, 2009). Indeed, aggregation could be
occurring throughout the ODZ core, but only exceed disaggregation in the
lower ODZ region. Alternatively, in this region, processes resembling
Weber and Bianchi’s (2020) Model 3, corresponding to H3 , in
which large particles remineralize more slowly than small ones, could
also occur. Like aggregation, such processes could be occurring through
the ODZ but are overwhelmed by the effects of disaggregation above
500 m.
Water mass changes may affect particle flux and size
changes
The observation that particle flux begins to attenuate below 500 m more
quickly than it does between the base of the photic zone and 500 m could
be explained in part by a shift in water mass at this depth where AAIW
begins to mix with NEPIW (Figure S2). The AAIW is suggested to have
micromolar oxygen concentrations, as compared to the NEPIW, such that a
small contribution of AAIW can raise the oxygen concentration (Evans et
al., 2020). However, measurements taken at this station in 2012 observed
zero oxygen though 800 m with the highly sensitive STOX electrode,
suggesting that oxygen, if present, is below 4 nM (Tiano et al., 2014).
It is conceivable that the AAIW has larger particle sizes and lower
particle abundance characteristics due to its having advected from
different geographic regions than the overlying water, but it is
difficult to see why this would be the case as these water masses stay
in the ODZ region for years (DeVries et al., 2012) and particles have a
much shorter residence time. In any case, the NEPIW to AAIW transition
coincides with the lower limit of the depth to which vertically
migrating zooplankton travel (Figure 2), and so we are not able to
deconvolve the effects of water mass changes from that of changes in
zooplankton effects on particle characteristics.
The change in water mass between 13CW and NEPIW, around 250 m, in
contrast, does not appear to correspond to any apparent changes in
particle flux or size. Thus, we would argue that any historical effects
of these water mass differences are likely to be small, and that active
transport differences above and below 500 m likely have a larger effect.
Oxic site differences
The oxic site provides validation that the patterns that we see at the
ETNP are unique to the ODZ region, and do not apply to a same latitude
ODZ site. The particle size distribution slope varied little and there
was not an increase in particle mass in the oxic site, consistent with
Weber and Bianchi’s (2020) null model (Figure S10), in which oxygen is
not limiting and particle sizes are not affected by anoxia. In this
case, small particles break down more quickly in the oxic site than our
site and so there is no small particle excess in this region. Similarly,
the higher flux attenuation in the oxic site (Figure S9A) suggests that
the differences in attenuation of all particle sizes by microbes at both
sites do indeed drive differences in flux profiles, and by extension
transfer efficiency, between oxic and anoxic regions. The lack of
increases in flux at the oxic site (Figure S9B) suggest that active
transport may play a greater role in the anoxic region than elsewhere.
The lack in apparent excess of small particles over model prediction
(Figure S9C) could either indicate less activity by zooplankton in this
region, or perhaps that remineralization of small particles quickly
removes any small particles produced by zooplankton in this
region.
Future directions
We advocate exploring the relationships between particle size
distribution, flux and acoustic signatures in other parts of the ETNP
and other ODZ regions. Expanded spatial analysis of particle size
spectra in ODZs would allow the community to confirm whether Weber and
Bianchi’s (2020) model (H1) , that particles of all sizes break
down more slowly in ODZs, applies elsewhere. Similarly, a clear next
step is to apply our disaggregation model to other ocean regions,
perhaps using particle size data already collected by other groups
(Guidi et al., 2008; Kiko et al., 2017, 2020).
While the UVP characterizes
dynamics of particles >100 μm, particles smaller than this
range contribute dramatically to carbon flux (Durkin et al., 2015), and
so their size distribution matters as well. However, at some point
particles become small enough that they likely do not sink, and so
exploring remineralization and disaggregation of <500 μm
microaggregate particles into non-sinking size classes would provide
valuable context to these measurements. In-situ pumped POC data from the
GEOTRACES program have been used to describe the dynamics of smaller
particle size classes (Lam et al., 2011; Lam & Marchal, 2015). Other
sensors, such as coulter counters (Sheldon et al., 1972) and Laser
In-Situ Scattering transmissometers (Ahn & Grant, 2007) provide size
resolved distribution information about these smaller size classes of
particles. Comparison between UVP data and past and ongoing (Siegel et
al., 2016) studies of the characteristics of <100 μmparticles provide opportunities to better understand the
dynamics of the full range of
particle sizes.
The image data collected by
the UVP offers opportunities to quantify the abundance and taxonomic
distribution of the zooplankton that migrate into the mesopelagic, as
well as the particle types within this region. Identifying this visual
data would have the added benefit of allowing researchers to analyze
particle size spectra, rather than the sum of particles and zooplankton
as we do here.