Introduction

The biological pump, in which sinking microaggregate (< 500 μm) and marine snow (> 500 μm) particles (Simon et al., 2002) transport carbon from the surface into the deep ocean, is a key part of the global carbon cycle (Neuer et al., 2014; Turner, 2015). Organic matter flux into the deep ocean (>1000 m) is a function both of export from the photic zone into the mesopelagic (export flux), and the fraction of that flux that crosses through the mesopelagic (transfer efficiency) (Francois et al., 2002; Passow & Carlson, 2012; Siegel et al., 2016). While definitions vary between studies, we define “mesopelagic” as the region between the base of the photic zone, and 1000 m (following Francois et al., 2002; Cram et al., 2018). The transfer efficiency of the biological pump may affect global atmospheric carbon levels (Kwon & Primeau, 2008). Thus, understanding the processes that shape organic matter degradation in the mesopelagic is critical.
Oxygen concentrations, and especially the geographic and vertical extent of anoxic ocean regions, appear to modulate particle flux through the mesopelagic. Observations of particle flux in the Eastern Tropical North Pacific near the Mexican coast (Hartnett & Devol, 2003; Van Mooy et al., 2002; Weber & Bianchi, 2020), the Eastern Tropical South Pacific (Pavia et al., 2019), and Arabian Sea (Keil et al., 2016; Roullier et al., 2014) have suggested lower flux attenuation in these ODZ systems. Models have shown that accounting for oxygen limitation in ODZs is necessary to fit global patterns of particle transfer (Cram et al., 2018; DeVries & Weber, 2017). Analysis of remineralization tracers has also shown evidence of slow flux attention in the ODZs (Weber & Bianchi, 2020). Understanding the driving mechanisms of these patterns is important because the oxygen content of the ocean is decreasing (Ito et al., 2017; Schmidtko et al., 2017), and the spatial extent and depth range of ODZs, including the Eastern Tropical North Pacific (ETNP) Oxygen Deficient Zone (ODZ), are likely to change, though there is disagreement over whether they are expanding or undergoing natural fluctuation (Deutsch et al., 2014; Horak et al., 2016; Stramma et al., 2008). Recent data informed models suggest that ODZs may enhance carbon transport to the deep ocean, by inhibiting microbial degradation of sinking marine particles (Cram et al., 2018). However, biological organic matter transport is also modulated by zooplankton whose interactions with particle flux in pelagic ODZs are only beginning to be quantitatively explored (Kiko et al., 2020).
Zooplankton modulate carbon flux through the mesopelagic (Jackson & Burd, 2001; Steinberg & Landry, 2017; Turner, 2015), and by extension the transfer efficiency of the biological pump (Archibald et al., 2019; Cavan et al., 2017), in three key ways that could be affected by ocean oxygen concentrations:
(1) Active transport : Zooplankton migrate between the surface and mesopelagic, consuming plankton and particles in the surface and producing particulate organic carbon (POC), dissolved organic carbon (DOC), respiratory CO2, and zooplankton carcasses at depth (Archibald et al., 2019; Bianchi et al., 2013; Hannides et al., 2009; Steinberg et al., 2000; Stukel et al., 2018, 2019). This manuscript focuses on particles, so we only consider POC and carcass production, which cause particles to “appear” in the midwater.
(2) Repackaging : Zooplankton fecal pellets have different physical properties than the parrticles and plankton that they ingest (Wilson et al., 2008). In this paper we define repackaging as zooplankton feeding in the mesopelagic and producing fecal pellets, effectively aggregating POM.
(3) Disaggregation : Zooplankton break large particles into smaller ones in two ways – by Coprorhexy (also sometimes called sloppy feeding) in which they break particles apart while feeding on them (Lampitt et al., 1990; Noji et al., 1991; Poulsen & Kiørboe, 2005), and by generating turbulence while they swim (Dilling & Alldredge, 2000; Goldthwait et al., 2005). Disaggregation can reduce particle transfer efficiency, because smaller particles sink more slowly and so reside longer in mesopelagic, allowing them to be consumed before reaching deep waters (Goldthwait et al., 2005; Lampitt et al., 1990; Noji et al., 1991; Poulsen & Kiørboe, 2005). In some cases, disaggregation can explain around 50% of the particle flux attenuation over depth (Briggs et al., 2020).
The migratory zooplankton that drive these mesopelagic processes spend the night in the surface layer and migrate into the core of the OMZ during the day (Bianchi et al., 2014). These organisms likely survive in ODZs by slowing their metabolic processes, but may supplement these with very efficient oxygen uptake and anaerobic metabolism (Seibel, 2011). Acoustic data suggest that zooplankton do not migrate as deeply into ODZs as they do into regions where ODZs are absent (Bianchi et al. 2011). New evidence suggests that in ODZ regions with shallower oxyclines, night-time migration depth remains the same but the depth where the organisms spend the day is compressed (Wishner et al., 2020). The rates at which zooplankton transport, repackage and disaggregate particles in ODZs are difficult to measure and therefore poorly constrained. Despite the importance of zooplankton mediated processes to global carbon flux, zooplankton are often missing from models of particle transfer.
Current models of particle transfer through the mesopelagic ocean predict that particle size, ocean temperature, and oxygen concentrations are the dominant factors controlling particle flux attenuation (Cram et al., 2018; DeVries & Weber, 2017). These models, however, do not account for active transport or disaggregation by zooplankton. As a result of this assumption, the models predict that small particles preferentially attenuate with depth, which is often not borne out by observations (Durkin et al., 2015). Therefore, these models’ predictions provide a useful null hypothesis of expected particle size distributions in the absence of zooplankton effects, which can be compared to observed distributions of particles to explore the magnitude of zooplankton effects.
Underwater vision profilers are cameras that can count and size many particles over large water volumes (Picheral et al., 2010) and provide valuable information about particle distributions and transport. When deployed in concert with particle traps in some regions, they can be used to predict flux in other regions where traps have not been deployed (Guidi et al., 2008; Kiko et al., 2020). Connecting UVP and trap data can furthermore inform about total particle flux variability across space and time, relationships between particle size, biomass, composition, and sinking speed, as well as the contributions of the different particle sizes to flux (Guidi et al., 2008; Kiko et al., 2017). Combined particle trap flux and UVP data from the North Atlantic suggest active transport by zooplankton into hypoxic water (Kiko et al., 2020), but the authors suggest that in more anoxic and larger ODZs, such as the modern day ETNP, there might be reduced active transport into the mesopelagic, since many migratory organisms would presumably not migrate into the anoxic water and would be less active. In this manuscript we provide the first combined flux measurement and UVP data from such a fully anoxic region, the ETNP ODZ.
In addition to being fully anoxic, the ETNP ODZ is primarily oligotrophic: most of the volume of the ETNP ODZ is below regions of very low surface productivity (Fuchsman et al., 2019; Pennington et al., 2006). Meanwhile most flux data have been measured in more coastal, higher productivity regions of the ETNP (Hartnett & Devol, 2003; Van Mooy et al., 2002).
A recent modeling study posed three hypotheses to explain why particle flux attenuates slowly in ODZs (Weber & Bianchi, 2020), which are susceptible to testing with UVP data. These are: H1: Allparticles in ODZs remineralize more slowly than in oxic water, regardless of their size, due to slower carbon oxidation during denitrification than aerobic respiration. H2: Breakdown of large particles into small particles is suppressed in the ODZ because there is less disaggregation by zooplankton than elsewhere. H3:Large particles remineralize more slowly in ODZs, but smaller ones do not, because carbon oxidation in large particles can become limited by the diffusive supply of oxygen and nitrate. In this case, respiration can only proceed by thermodynamically inefficient sulfate reduction (Bianchi et al., 2018; Lam & Kuypers, 2011). Sulfide and organic matter sulfurization have been found on particles at this site at nanomolar concentrations (Raven et al., 2021). Microbial analysis of particles found sulfate reducers and S-oxidizing denitrifiers at low abundances (Fuchsman et al., 2017; Saunders et al., 2019). Each of the hypotheses outlined above were predicted to leave distinct signatures in particle size distributions in the core of ODZ regions (Weber & Bianchi, 2020). The model with slow remineralization of all particles, predicts an increase in the abundance of small particles in the ODZ core relative both to overlying waters and to similar, oxygenated environments (H1 ). The model with suppressed disaggregation predicts a large decrease in small particle biomass in the ODZ, both relative to the surface and to oxygenated water (H2 ). The model in which remineralization is depressed only in large particles predicts a small decrease with depth in small particle abundance, similar to that seen in oxygenated environments (H3 ). However, the necessary particle size data from an ODZ was not previously available to support any hypothesis at the exclusion of the others. In this manuscript we present a new dataset that is sufficient to test these three hypotheses.
To provide the data to test hypotheses H1-H3 and illuminate zooplankton particle interactions in oligotrophic ODZs, we collected particle size data at high temporal resolution over the course of a week in an anoxic site typical of the oligotrophic ETNP ODZ, well away from the high productivity zone in the coast. We integrated this size data with observed flux measurements, and acoustic data. We quantified, throughout the water column, how changes in size distribution deviate from changes that would be predicted by remineralization and sinking only models.
We ask the following four questions:
Question A: How does the particle size distribution at one location in the oligotrophic Eastern Tropical North Pacific vary with respect to depth and time?
Question B: Do our data support any of the three Weber and Bianchi (2020) models (H1-H3 )?
Question C: Do our data suggest that regions of the oxygen deficient zone harbor disaggregation-like processes, and if so, do these co-occur with migratory zooplankton?
Question D : How do particle size distribution spectra in the ODZ compare to those seen in the oxic ocean?
By addressing these four questions, we demonstrate that our dataset from the ETNP supports Weber and Bianchi’s first hypothesis, that microbial remineralization of all particles slows in the ODZ, while disaggregation continues unabated. Additionally, disaggregation-like processes do appear to co-occur with acoustic measurements of migratory zooplankton, suggesting that exclusion of zooplankton is not a major contributor to slow flux attenuation.