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.