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.