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Water Research 205 (2021) 117658

Contents lists available at ScienceDirect

Water Research
journal homepage: www.elsevier.com/locate/watres

Review

Organic pollutants in deep sea: Occurrence, fate, and


ecological implications
Edmond Sanganyado a, b, *, Kudakwashe E. Chingono c, Willis Gwenzi e, Nhamo Chaukura d,
Wenhua Liu a, b
a
Guangdong Provincial Key Laboratory of Marine Biotechnology, Institute of Marine Science, Shantou University, Shantou, Guangdong 515063, China
b
Southern Marine Science and Engineering Guangdong Laboratory, Guangzhou 511458, China
c
School of Chemical and Process Engineering, University of Leeds, Leeds, LS2 9JT, UK
d
Department of Physical and Earth Sciences, Sol Plaatje University, Kimberley, South Africa
e
Department of Soil Science and Agricultural Engineering, Biosystems and Environmental Engineering Research Group, University of Zimbabwe, Harare, Zimbabwe

A R T I C L E I N F O A B S T R A C T

Keywords: The deep sea - an oceanic layer below 200 m depths – has important global biogeochemical and nutrient cycling
Deep sea functions. It also receives organic pollutants from anthropogenic sources, which threatens the ecological function
Persistent organic pollutants of the deep sea. In this Review, critically examined data on the distribution of organic pollutants in the deep sea
Biological pump
to outline the role of biogeochemical and geophysical factors on the global distribution and regional chemo­
Marine pollution
Polychlorinated biphenyls
dynamics of organic pollutants in the deep sea. We found that the contribution of deep water formation to the
Organochlorine pesticides influx of perfluorinated compounds reached a maximum, following peak emission, faster in young deep waters
(< 10 years) compared to older deep waters (> 100 years). For example, perfluorinated compounds had low
concentrations (< 10 pg L− 1) and vertical variations in the South Pacific Ocean where the ocean currents are old
(< 1000 years). Steep geomorphologies of submarine canyons, ridges, and valleys facilitated the transport of
sediments and associated organic pollutants by oceanic currents from the continental shelf to remote deep seas.
In addition, we found that, even though an estimated 1.2–4.2 million metric tons of plastic debris enter the ocean
through riverine discharge annually, the role of microplastics as vectors of organic pollutants (e.g., plastic
monomers, additives, and attached organic pollutants) in the deep sea is often overlooked. Finally, we recom­
mend assessing the biological effects of organic pollutants in deep sea biota, large-scale monitoring of organic
pollutants, reconstructing historical emissions using sediment cores, and assessing the impact of deep-sea mining
on the ecosystem.

1. Introduction water circulation, CO2 exchange, biological control, in situ primary


production, climate regulation, carbon sequestration, and waste detox­
Deep sea (layers below 200 m depth) ecosystems are currently ification (Da Ros et al., 2019). However, information on the structure,
threatened by multiple anthropogenic disturbances such as chemical function, and composition of the deep sea ecosystem remain scant
pollution, overfishing, resource extraction, and climate change (Rogers, despite its vast size, partly due to the putative high costs of exploring
2015). It is the largest ecosystem on Earth and is characterized by a 1.2 such ecosystems (Danovaro et al., 2020). Since less than 0.0001% of the
billion km3 volume, 434 million km2 seafloor, and a 4.2 km average ocean floor has been explored, it is difficult to predict the ecological
depth (Rogers, 2015). Deep sea ecosystems play a crucial role in main­ effects of anthropogenic disturbances in the deep sea (Rogers, 2015).
taining planetary health and function through supporting unique Deep sea ecosystems were previously considered pristine and free
biodiversity essential for the biogeochemical cycling of nutrients, from anthropogenic disturbances due to their remoteness. However,
metals, carbon, and nitrogen. They control nutrient and energy flux organic pollutants enter the deep sea through atmospheric deposition,
across environmental compartments and ecosystem services such as oceanic transport, and sometimes sea-based anthropogenic activities (e.

* Corresponding author at: Guangdong Provincial Key Laboratory of Marine Biotechnology, Institute of Marine Science, Shantou University, Shantou, Guangdong
515063, China
E-mail address: esang001@ucr.edu (E. Sanganyado).

https://doi.org/10.1016/j.watres.2021.117658
Received 2 June 2021; Received in revised form 4 September 2021; Accepted 7 September 2021
Available online 11 September 2021
0043-1354/© 2021 Elsevier Ltd. All rights reserved.
E. Sanganyado et al. Water Research 205 (2021) 117658

g., seabed mining, fishing, ship traffic, and accidental spillage) (Kal­ 2. Occurrence of organic pollutants in deep sea ecosystems
lenborn, 2006). Several studies detected organic pollutants such as
polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs), Rapid industrialization and urbanization compounded by increased
and polybrominated diphenyl ethers (PBDEs) in seawater, sediments, demand for food security and quality life have contributed to the rise in
and biota from the deep sea (Dasgupta et al., 2018; Lohmann et al., environmental emissions of organic pollutants (Table 1). Before their
2006). Out of the 17 Sustainable Development Goals set by the United ban or their production restrictions were effected by the Stockholm
Nations as targets for 2030, eight are directly or indirectly impacted by Convention, it is estimated 2.79 million metric tons of DDT and 1.51
deep sea pollution (Fig. 1). For example, the presence of organic pol­ million metric tons of PCBs were produced globally (Fiedler et al.,
lutants in the deep sea poses great harm to the ecosystem; thus, 2019). About 96,000 tons of chemicals based on perfluorooctane sul­
threatening the conservation and sustainable use of the ocean resources fonate (PFOS) were produced globally between 1970 and 2002, while
for sustainable development as required by SDG 14. Although deep sea between 1951 and 2015, up to 21,400 tons of perfluoroalkyl carboxylic
ecosystems are protected from pollution by global conventions (e.g., acids (PFCAs) were produced (Wang et al., 2014, 2013). In 2018, it was
Convention for the International Convention for the Prevention of estimated that about 400,000 and 100,000 tons of BDE209 (a PBDE
Pollution from Ships, United Nations Convention on the Law of the Sea, congener) were in use or disposed of in waste stocks, respectively
and Convention on the Prevention of Marine Pollution by Dumping of (Abbasi et al., 2019). About 30,000 tons of HBCDs are produced glob­
Wastes and Other Matter) and regional conventions (e.g., Protection of ally, with 238,000 tons estimated to be used in China before they are
the Marine Environment in the North-East Atlantic, Convention on the phased out (Li et al., 2016). Due to their extensive application in con­
Protection of the Marine Environment in the Baltic Sea, Convention for sumer and industrial products and a high potential for long-range at­
the Protection of Marine Environment and the Coastal Region of the mospheric (oceanic) transport, organic pollutants are frequently
Mediterranean, Convention for the Protection of the Black Sea), organic detected in deep sea ecosystems.
pollutants are continually discharged into the environment, and subse­ The presence of organic pollutants in the global oceans, especially
quently reach the deep sea directly or indirectly (Tornero and Hanke, the deep sea, is linked to various sources, which can be classified as land-
2016). Monitoring and characterizing anthropogenic disturbances and based and sea-based activities (Fig. 2) (Sanganyado et al., 2020). Their
their effect on key species are essential for a robust assessment of the main routes of entry include inputs from coastal regions transported by
health of the deep sea ecosystem. This review seeks to examine the oceanic currents, atmospheric deposition of free or particle-associated
literature on the distribution, fate, transport, and trophic transfer of organic pollutants released from land-based activities, unintentional
organic pollutants in deep sea ecosystems to determine their sources and shipping discharges (e.g., accidental oil spill and litter), and deep sea
transport mechanisms. The key factors influencing the accumulation resource extraction (e.g., seabed mining, fishing, and mariculture),
and transport of organic pollutants in deep sea ecosystems will be dis­ waste disposal (Tornero and Hanke, 2016). The entry route of the
cussed. Such knowledge is essential for assessing the environmental risk organic pollutants influences their profile (i.e., concentration and type)
of organic pollutants and developing conservation and management and the mechanism by which they transfer from the seawater column to
strategies for deep sea ecosystems. the seafloor. For example, semivolatile persistent organic pollutants
(POPs) are often transported to the deep sea by long-range atmospheric
transport (Wania and Mackay, 1996). The semivolatile organic

Fig. 1.. The impact of deep sea pollution by organic pollutants on the United Nations Sustainable Development Goals. Icons used with permission from the United
Nations (https://www.un.org/sustainabledevelopment).

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E. Sanganyado et al. Water Research 205 (2021) 117658

Table 1.
Examples of organic pollutants found in marine environments and their uses.
Class Compounds Uses
a b b b b b b
POPs Organochlorine Aldrin , chlordane , chlordecone, DDT , dicofol, dieldrin , endrin , heptachlor , Controlling pests in agriculture production
pesticides hexachlorobenzenes (α- and β-HCB)b, lindane, mirexb, pentachlorobenzene, and public health.
pentachlorophenols, endosulfan, toxapheneb
Brominated flame Decabromodiphenyl ether, hexabromobiphenyl, hexabromocyclododecane Flame retardant additives in sealants,
retardants (HBCDD), hexachlorobenzene, hexachlorobutadiene, tetrabromodiphenyl ether adhesives, textiles, paints, and upholstery.
Halogenated industrial Short-chain chlorinated paraffins (SCCPs), perfluorooctane sulfonate (PFOS) and its Lubricants, plasticizers, adhesives, flame
chemicals salts, perfluorooctane sulfonyl fluoride, polychlorinated biphenyls (PCBs)b retardants
Unintentional Polychlorinated naphthalenes, polychlorinated dibenzo-p-dioxins (PCDD)b, Byproducts of industrial processes
production polychlorinated dibenzofurans (PCDF)b
Other organic Perfluorinated Perfluorocarboxylic acids (PFCAs) (e.g., perfluorobutanoate (PFBA), Water-, stain-, and soil-resistant coatings,
pollutants compounds perfluorohexanoate (PFHxA), perfluorooctanoate (PFOA), perfluorononanoate insecticides, surfactants, lubricants, and
(PFNA), perfluorodecanoate (PFDA)), perfluoroalkylsulfonates (PFSAs) (e.g., flame retardants
perfluorobutanesulfonate (PFBS), perfluorohexanesulfonate (PFHxS),
perfluorodecanesulfonate (PFDS))
Brominated flame Other polybrominated diphenyl ethers (PBDEs), besides deca-BDE, Flame retardant additives in sealants,
retardants adhesives, textiles, paints, and upholstery.
Unintentionally Polycyclic aromatic hydrocarbons (PAHs) Byproducts of industrial processes or
produced compounds combustion
a
Refers to all the persistent organic pollutants listed in the Stockholm Convention for elimination, restriction, or reduction of unintentional release.
b
Represents legacy POPs that were initially listed under the Stockholm Convention; the remaining POPs were later listed and are referred to as emerging POPs.

Fig. 2.. Land- and sea-based sources of organic pollutants and their potential fate and transport pathways. From Sanganyado et al. (2020). Used with permission of
Taylor and Francis.

pollutants deposit on the ocean surface following changes in atmo­ Organic pollutants in deep sea ecosystems can also be of natural
spheric conditions. After a while, some of the organic pollutants are origin. For example, several studies found that marine bacteria produced
revolatilized and carried further by atmospheric transport. This type of organobromines such as hydroxylated PBDEs, methoxylated PBDEs,
long-range transport is called the grasshopper effect (Jurado and Dachs, polybrominated dibenzo-p-dioxins, and polybrominated pyrroles
2008). A study in Levantine Basin found sediment PCB (12–190 ng g− 1) (Agarwal et al., 2017). Agarwal et al. (2017) found that marine sponges,
and PAH (< 0.3–7.7 ng g− 1) concentrations were linked to nearby gas an important biodiversity hotspot in deep sea ecosystems, produced
well drilling and dumping sites for sediment dredge (Astrahan et al., various PBDEs using metagenome-mining techniques. In the western
2017). Tables S1 and 2 show the distribution of organic pollutants in Pacific Ocean, the concentration of methoxylated PBDEs in extractable
deep sea water and sediments, respectively. organic matter from marine sponges (i.e., Haliclona sp. and Callyspongia

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E. Sanganyado et al. Water Research 205 (2021) 117658

sp.) were 63,500 ng g− 1 and 36,500 ng g− 1, respectively (Haraguchi 3. Factors influencing the transport of organic pollutants in the
et al., 2011). Four methoxylated PBDEs were detected in endemic am­ deep sea
phipods collected from hadal trenches (6,000–11,000 m depth) in the
western Pacific Ocean (Cui et al., 2020). However, none were detected 3.1. Biological pump
in sediments or suspended particulate matter (Cui et al., 2020). Am­
phipods play an important role in regulating nutrient and energy flux in The transport of organic pollutants in deep sea ecosystems is often
marine environments; hence, their species density around marine regulated by a complex ensemble of biophysical processes involved in
sponges is often high (Amsler et al., 2009). Gut analysis of nearshore transporting organic carbon from the ocean surface to the deep sea and
amphipods in the Antarctica Peninsula revealed that some amphipods sediments (i.e., biological pump) (Fig. 3) (Galbán-Malagón et al., 2012).
feed on marine sponges (Amsler et al., 2009). Besides amphipods, The biological pump can be conceptualized as a biogeochemical system
organobromines can transfer indirectly to necrophagivore fish (e.g., comprising primary production, vertical transport, and sedimentation
Paraliparis bathybius, Notoliparis kermadecensis, Pachycara sp., and Bas­ (Lutz et al., 2007). Phytoplankton accumulate organic pollutants from
sozetus sp.), which feed primarily on amphipods and directly to mega­ the surface waters during the primary production stage, driving
faunal croppers (e.g., Notacanthus chemnitzii, Barathrites parri, and air-water disequilibrium in organic pollutant concentration. A previous
chimaerids) which feed on marine sponges (Drazen and Sutton, 2017). A study found phytoplankton uptake and gravitational settling of biogenic
study in the western Pacific Ocean found methoxylated PBDEs in fish particles increased the air-water influx of PCBs (Galbán-Malagón et al.,
samples (Haraguchi et al., 2011). Although studies on their distribution 2012). Primary productivity is often governed by solar, physical
and impact in deep sea ecosystems remain scarce due to sampling and oceanographic, and climatic factors, and this often results in seasonal
analytical challenges, previous studies have shown that naturally pro­ and regional trends in the efficacy of the biological pump in seques­
duced organohalogens can bioaccumulate and biomagnify in marine trating the organic pollutants (Lutz et al., 2007).
mammals; thus, threatening the structure and function of the deep sea Additionally, physicochemical properties of the organic pollutants
ecosystems (Sanganyado et al., 2020; Weijs et al., 2009). A study in the (e.g., aqueous solubility, hydrophobicity, volatility, and lipophilicity),
Sea of Japan and North Pacific Ocean found halogenated bipyrroles (up local environmental conditions in the deep-water (e.g., depth, oxygen
to 4,900,000 ng kg− 1 wet weight) and methoxylated PBDEs (up to 190, content, and temperature), settling particle characteristics (e.g., size,
000 ng kg− 1 wet weight) concentrations were detected in cetaceans in density, and type), climate/geographical factors (e.g., latitude, ocean
the order of killer whales > toothed whales > baleen whales demon­ currents), seafloor geomorphology (e.g., topographical features), and
strating the critical role of feeding ecology on natural organobromine biodiversity can further influence the organic pollutant sequestration
biomagnification (Fujii et al., 2018). Overall, although naturally pro­ efficiency of the biological pump. Since phytoplankton readily uptake
duced organohalogens are often present at concentrations lower than more hydrophobic compounds, higher air-water influxes have been
organic pollutants, biosynthesis needs to be seriously considered a key observed for PCB congeners with higher octanol-water partition co­
source of potentially toxic organohalogens in deep sea ecosystems. efficients (log KOW) in high productivity regions such as the North
Atlantic, North Pacific and Arctic Oceans (Gioia et al., 2008). PCB
congeners with low log KOW are often more abundant in high latitude
oceans such as subtropical regions, where biological pump efficiencies
are often low (Sobek and Gustafsson, 2004). The air-water flux of

Fig. 3.. An overview of the major biophysical processes governing the fate and transport of organic pollutants in deep sea ecosystems.

4
E. Sanganyado et al. Water Research 205 (2021) 117658

organic pollutants and changes in their export are critical determinants acids were first produced and used in the 1960s (Yamashita et al., 2008).
of the vertical profile of dissolved organic pollutants. Hence, under­ Hence, deep water formation can contribute to the depletion of per­
standing the sequestration efficiencies and mechanisms of the biological fluorinated compounds from the global ocean surface, particularly in the
pump is imperative since these processes impact the ‘sink and source’ North Atlantic and Southern Oceans (Lohmann et al., 2006). However,
role of the deep sea. PFAS contamination in the South Pacific Ocean was shown to be
negligible (below detection limit to < 10 pg L− 1) in ocean surface and
3.2. Physical pump the deep water compared to other oceans (Yamashita et al., 2008). This
was probably because there was no direct discharge of PFAS in the South
Water masses originating from continental margins transport organic Pacific Ocean since the water masses comprise of ~1000-years old ocean
pollutants to the deep ocean through lateral diffusion, eddy currents, currents and Antarctic circumpolar water masses. Previous mass flow
intrusion, and hyperpycnal flows/thermohaline currents (Puig et al., estimates showed that PFOS and PFOA flux in the deep water layer of the
2014). A study in the continental margin of the Gulf of Mexico found a Labrador Sea was four and ten times higher than PCB flux, respectively
positive correlation between particle-attached PAHs (0.9 and 7.0 ng (Lohmann et al., 2006; Yamashita et al., 2008). The results suggested
L− 1) and particulate organic carbon 4000–131,000 ng L− 1), although highly soluble and less volatile organic pollutants transferred from the
both variables negatively correlated with salinity (Adhikari et al., 2019). surface water to the deep water faster than the semi-volatile and rela­
The results suggested riverine discharge was the primary source of PAHs tively more hydrophobic organic pollutants. Even though deep water
in the deep sea (Adhikari et al., 2019). In the South Atlantic, upper flux of PFAS in the Labrador Sea is relatively fast, transferring the PFOAs
Equatorial, and Indian Oceans, lateral ocean circulation accounted for (emitted globally to date) into global oceans requires at least 4500 years
20–48% PCB influx (Wagner et al., 2019). At the same time, upwelling (Yamashita et al., 2008). In the North Atlantic Ocean, PFOS concen­
contributed up to 10% in removing PCBs from the deep sea to the ocean trations were higher and more variable in the surface water (0–10 m)
surface (Wagner et al., 2019). In the Fram Strait, a deep-water channel compared to the subsurface water (365–510 m) and the water layer
that transports organic pollutants into the Arctic Ocean, the West around the permanent thermocline (985–1335 m) (Zhang et al., 2017).
Spitsbergen and the East Greenland Currents contributed a total mass The lag time between peak PFOS emission and peak concentrations in
flux for α-HCH of 29 tons y− 1 and 67 tons y− 1, respectively (Ma et al., subsurface and permanent thermocline layer water was 2–3 years and
2018). However, the ocean currents moved in the opposite direction. more than 30 years, respectively. This was probably because vertical
The West Spitsbergen Current moved northwards from the Atlantic to mixing in the North Atlantic is intense during winters and can reach 600
the Arctic Ocean and the East Greenland Currents moving southwards m depths while subduction and ventilation of water in the surface mixed
along Greenland. In contrast, there was a net influx of PCBs (i.e., PCB 28, layer to the permanent thermocline is slow (Zhang et al., 2017). For that
101, 153, and 180) into the Arctic Ocean transported through the Fram reason, the distribution of perfluorinated acids in oceans is often used as
Strait between 1930 and 2015 (80 tons y− 1) (Ma et al., 2018). In the chemical tracer to assess the transport of anthropogenic pollutants by
Aegean Sea, cyclonic surface circulation and deep-water outflows from oceanic currents.
the Cretan Strait were shown to be a crucial advective source of PAHs PFAS profiles and concentrations significantly vary between surface
and contributed to the accumulation of PAHs in sediments (Hatzianestis and deep water oceans, except in seas that experience intense vertical
et al., 2020). In stratified oceans, ocean currents and the seafloor mixing (Wei et al., 2008; Yeung et al., 2017). A study on per­
interact over short timescales lasting (< 5 years) through horizontal, fluorooctanesulfonate (PFOS), perfluorooctanoate (PFOA) and per­
vertical, and eddy currents (i.e., internal solitary waves). By driving fluorobutanesulfonate (PFBS) in global oceans found distinct
processes such as sediment resuspension and transport in the seafloor, stratification in the sources of the compounds; the North Atlantic Cur­
internal solitary waves contribute to the outflow and inflow of organic rent was the major source of the perfluorinated acids in the surface
pollutants into the deep sea (Jia et al., 2019). Hence, the role of oceanic waters, the Labrador current in the subsurface waters, and the Denmark
currents in the total flux of organic pollutants in the deep sea is often in a Strait Overflow Water in the deep layers (below 2000 m depth)
state of competition whereby the net flow may be influenced by (Yamashita et al., 2008). In Western Mediterranean Sea, PFAs concen­
geophysical, seasonal, and climatic factors. trations in the deep water (141 pg L− 1) were about two times lowers
Global thermohaline currents driven by temperature and salinity than those in the surface water samples (357 pg L− 1) (Brumovský et al.,
gradients have been shown to move surface water together with organic 2016). The Western Mediterranean deep water has short renewal cycles
pollutants to the deep sea in a process called deep water formation since at least two intense dense shelf water cascading and open-sea
(Lohmann et al., 2006). A study on the Norwegian, Ross, Weddell, and convection events were observed between 2004 and 2012. The verti­
Labrador Seas found deep water formation was a major route of entry of cal profile of PFAS in the Mediterranean and Japan Seas substantially
PCBs to the deep sea (870 kg yr− 1) compared to particle settling (320 kg differed even though both are semi-enclosed seas with deep waters
yr− 1) (Lohmann et al., 2006). A study on the distribution of organic isolated from the open ocean (Yamazaki et al., 2019). Yamazaki et al.
pollutants in sediments from the Mediterranean Sea found that the (2019) found that the PFAS concentration in the Mediterranean Sea
Western Mediterranean Deep Water formation increased the deposition were an order of magnitude higher than in the Japan Sea. The PFAS
of POPs with a low air-water partition coefficient (log KAW) of -4.0 to concentrations steadily decreased with an increase in depth in the Japan
-2.0 such as lindane, tri-PCBs, tetra-PCBs, and methylphenanthrenes Sea, with only PFDA and PFHxS having a maximum concentration in the
(Salvadó et al., 2019). In contrast, there was a strong association be­ mid-deep waters (1000–1500 m). In contrast, PFAS vertical profile was
tween POPs with an intermediate log KAW (-2.0 to 0) and high highly variable in the Mediterranean Sea, although at some locations
octanol-water partition coefficient (log KOW > 6) and sediment particles higher concentrations of PFDA, PFNA, PFHxA, and PFHpA were detec­
suggesting horizontal transport in the continental shelf (Salvadó et al., ted in the deepest water columns sampled (2300–3600 m) (Yamazaki
2019). Perfluorinated compounds reached 3500 m depths in young deep et al., 2019). This is probably because PFNA, PFHxA, and PFHpA are
water masses (< 10 years) in the Labrador Sea (North Atlantic Ocean) legacy PFAS that were extensively used in fluoropolymer products (Lin
(Yamashita et al., 2008) but were not detected below the permanent et al., 2020). Overall, the PFAs profiles in young deep waters such as the
thermocline in old deep waters (> 450 years) in the Central Arctic Ocean Mediterranean Sea are indicative of the PFAS profiles in surface
Basins (Yeung et al., 2017). The intrusion of perfluorinated compounds seawater of a decade earlier, while those of old deep waters are asso­
to deep waters is often negligible in old deep waters such as those found ciated with legacy PFAs. However, currently missing are data on PFAS
in the Central Arctic Ocean Basins (Yeung et al., 2017) and Fram Strait profiles in deep sea waters surrounded by low-income countries, where
(Joerss et al., 2020) because the estimated time for deep water forma­ several banned PFAs are likely to be still in use.
tion in these regions is usually more than 100 years yet perfluorinated

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E. Sanganyado et al. Water Research 205 (2021) 117658

3.3. Settling particle characteristics coefficients of the compounds. For example, a previous study found light
PCB congeners desorbed faster (e.g., PCB-8 half-life = 14 days) than
Biogenic, inorganic, and anthropogenic particles are important heavier congeners (e.g., PCB-209 half-life = 210 years) (Endo et al.,
vectors for the vertical transport of organic pollutants in oceans. As the 2013). Hence, it is expected that microplastic-associated PCBs in the
(non)biogenic particles sink, organic pollutants may be released to the deep sea would be dominated by heavier congeners. However, the less
deep-water column via (bio)transformation or dissolution of particles. recalcitrant and more water-soluble tri-PCBs were the most dominant
However, the profile of organic pollutants transported can be influenced PCB congeners (> 92%), and the composition was consistent with the
by the nature of the settling particle. For example, a study in the Indian, technical mixtures produced in China (Dasgupta et al., 2021). Low
Pacific, and Atlantic Oceans found that the vertical flux of PFAS via molecular weight PCB congeners like tri-PCB have more extended at­
zooplankton fecal matter was one to two orders of magnitude higher mospheric reach; they are sometimes generated during the microbial
than that of PFAS associated with phytoplankton (González-Gaya et al., transformation of high molecular weight PCBs and are preferentially
2019). Settling of large particles (> 50 μm) in deep marine ecosystems exchanged during ocean-air interactions due to their lightweight (Das­
contributes significantly to the vertical transport of pollutants through gupta et al., 2021, 2018). In vitro digestive models have revealed
the water column, while small particles are carried by water masses and microplastic can act as a vector or cleaner (extracting organic pollutants
may also contribute to the advective transport of the organic pollutants from the gut) in aquatic organisms (Mohamed Nor and Koelmans, 2019).
(Martí et al., 2001). The primary source of organic pollutants in small However, comprehensive data on the flux of organic pollutants into the
particles is partitioning from water particles. In contrast, organic pol­ deep sea through microplastic transport are still lacking.
lutants in large biogenic particles come directly from the food chain
(Martí et al., 2001). A study in Mediterranean deep waters found that the 4. Factors influencing the accumulation of organic pollutants in
concentration of halogenated organic contaminants on the small parti­ the deep sea
cles (< 0.7 μm) decreased significantly with depth compared to large
particles (< 50 μm) (Martí et al., 2001). Hence, particle size can influ­ 4.1. Microbial biotransformation
ence the accumulation rate of organic pollutants in the water column
and sediments. It is often assumed that the biotransformation mechanisms of organic
Microplastics are complex particles comprising of a dynamic mixture pollutants in the deep sea and surface water ecosystems are similar
of monomers, additives, and processing agents (Galloway et al., 2017). despite the drastic differences in temperature and hydrostatic pressure
They often host microorganisms and bind organic pollutants and organic (Louvado et al., 2015). At low temperatures, the enzymatic activity of
material, which alters the microplastic density and surface charge organohalogen-degrading microorganisms often decreases, resulting in
resulting in a change in bioavailability of the organic pollutants low organic pollutant degradation efficiency. In contrast, high hydro­
(Galloway et al., 2017). An estimated 1.2–4.2 million metric tons of static pressure in deep sea ecosystems was shown to decrease the fungal
plastic debris enter the ocean through riverine discharge, of which degradation of poly-β-hydroxybutyric acid (Gonda et al., 2000). Previ­
14.4–236 thousand metric tons are floating in the global ocean (Jam­ ous studies showed that bacteria in deep sea ecosystems developed
beck et al., 2015; Weiss et al., 2021). Around 99.8% of the plastic debris phenotypical characteristics such as cell membrane with a higher
discharged into the oceans since the 1950s are estimated to be below the amount of unsaturated fatty acids and lack of genes involved in photo­
ocean surface, in the subsurface, deep water layer, or seafloor (Koel­ synthetic reactions, which enabled their adaptation to the
mans et al., 2017). Plastic particles are transferred to the deep water and psychro-peizophilic conditions (Louvado et al., 2015). These phenotypic
seafloor through accumulation in biota following ingestion, adaptations may reduce the permeability of the deep sea microorgan­
thermohaline-driven currents, and gravitational settling following loss isms, resulting in decreased organic pollutant uptake and intracellular
of buoyancy or incorporation into fecal matter (Kvale et al., 2020). A biotransformation. The low temperatures and high hydrostatic pressure
recent study showed that Bathochordaeus stygius, one of the most conditions can facilitate the role of deep sea ecosystems as the ultimate
abundant zooplankton, effectively transported microplastics from the sink of organic pollutants. However, organohalogen-degrading bacteria
ocean surface to the deep sea by ingesting and then excreting micro­ may have adapted to the psychro-peizophilic conditions as they devel­
plastics as part of their fecal pellets (Katija et al., 2017). During physi­ oped higher diversity in metabolic activity (Konstantinidis et al., 2009).
cochemical and biological weathering of plastic debris to form Since studies modeling the global fate and transport are often based on
microplastics, plastic monomers, additives, and plastic attached organic the chemodynamics of the organic pollutants in surface water, they may
pollutants inadvertently leach to the surrounding water column; thus, under- or overestimate the global distribution of organic pollutants,
contributing to the flux of organic pollutants in the deep sea (Dasgupta considering the deep sea is probably the largest environmental
et al., 2021). This is greatly concerning since around 10,500 compounds compartment organic pollutants partition.
are used worldwide as plastic monomers, additives (e.g., antioxidants, Microbial transformation of freely dissolved- or particle-attached
biocides, flame retardants, plasticizers, light stabilizers, and colorants), organic pollutants contributes to removing organic pollutants in the
and processing aids (e.g., heat stabilizer, crosslinking agent, lubricant, deep sea. Next-generation sequencing analysis of deep sea sediments
solvent, and antistatic agent), of which 2486 are substances of potential from the Great Australian Bight detected three genes (i.e., alkB, c23o,
concern while no hazard data was available for 4100 substances (Wie­ and pmoA) associated with aerobic hydrocarbon degradation (van de
singer et al., 2021). A previous study found polychlorinated biphenyl Kamp et al., 2019). Various studies have shown that bacteria isolated
(127–142 ng g− 1), organochlorine pesticides (4280–5350 ng g− 1), and from different deep sea geomorphologies such as hydrothermal vents
chlordane (1080–1260 ng g− 1) concentrations in microplastics and could degrade organohalogens. Bacteria isolated from hydrothermal
plastic pellets found in the Xisha Trough in the South China Sea (Das­ vents have been shown to readily degrade PAHs and n-alkanes since they
gupta et al., 2021). The concentration of organochlorine pesticides in evolved to use hydrocarbons as their primary carbon source (Ma et al.,
Xisha Trough was higher than those found in coastal beaches (2.2–1970 2021). Gammaproteobacteria (i.e., FJ613315, Pseudomonas stutzeri strain
ng g− 1) on the South China Sea, while PAH concentrations were an order hyss62) and Actinobacteria (i.e., HM222653, Nocardioides sp. 0701C5–1)
of magnitude lower than those found on the beach (11.2–7710 ng g− 1) that oxidize PCBs were previously isolated from deep sea sediments in
(Shi et al., 2020). Organochlorine pesticides such as DDT are more hy­ the Kongsfjorden (Papale et al., 2017). The removal efficiency of
drophobic than PAHs and tend to have lower desorption and degrada­ P. stutzeri contained the bphA gene, and its removal efficiency was
tion rates during transport to the deep sea from coastal environments 10–69% at 4 ◦ C and 7.3–93% at 15 ◦ C (Papale et al., 2017). The di- and
(Bakir et al., 2014). However, long-term desorption of organic pollutants tri-PCBs were more efficiently removed at both temperatures than
from microplastics is highly influenced by the polymer-water partition tetra-PCBs suggesting heavier congeners might be more recalcitrant

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E. Sanganyado et al. Water Research 205 (2021) 117658

than lighter congeners in the deep sea sediments. The degradation of primarily dependent on compound hydrophobicity but other properties
organic pollutants by deep sea bacteria might follow pathways different such as polarity (Ng and Hungerbühler, 2014). There is a need for
from those observed from coastal, soil, freshwater, and open ocean further studies to assess the effect of organic pollutant bioavailability on
bacteria. Deep sea bacteria adapted to lower oxygen, nutrient, and the efficacy of biological pumps in removing organic pollutants from the
temperature, and higher pressure conditions, which probably altered sea surface.
how they use organic pollutants as food sources (Scoma et al., 2019).
Studies on the biotransformation of organic pollutants other than hy­ 4.3. Water column depth
drocarbons in deep sea ecosystems remain scarce.
Biogeochemical processes in the water column influence the occur­
4.2. Bioavailability rence, settling, and fate of organic pollutants in the ocean
(Galbán-Malagón et al., 2012). In the Arctic Ocean, PBDE concentrations
Particle-associated organic pollutants often exhibit low bioavail­ were an order of magnitude higher in the deep waters than in the polar
ability, the extent to which depends on their hydrophobicity. The mixed layer suggesting a predominancy of vertical transport of the
bioavailability of organic pollutants often changes as the particle- PBDEs (Salvadó et al., 2016). The relative contribution of less bromi­
associated organic pollutants are transported to the deep water layer nated congeners (i.e., tri- to hepta-BDEs) increased with depth compared
due to changes in temperature, salinity, oxygenation, and particle to the heavier congeners (Salvadó et al., 2016). The increase with depth
characteristics. This is partly because the physicochemical characteris­ of BDE-71, which are not found in technical mixtures, and other less
tics of the organic pollutants (e.g., lipophilicity, dipole-moment, and brominated congeners suggest heavier congeners transformed to lighter
water solubility) may alter as the water chemistry changes between the congeners during vertical or oceanic transport (Salvadó et al., 2016).
surface, subsurface, to deep water (Lyytikäinen et al., 2003). Interest­ Previous studies in the Central Arctic Ocean Basin (Carrizo et al., 2017)
ingly, previous studies have shown that the accumulation of PFAS in and Fram Strait (Ma et al., 2018) found that transformation of DDTs to
biota was driven by phospholipid and protein interactions, processes DDEs contributed to the relative increase in DDEs with depth. In
that are governed by the polarity and hydrophobicity of the compound contrast, the concentration of highly chlorinated PCBs increased with
(Ng and Hungerbühler, 2014). Additionally, changes in sediment char­ depth, suggesting sorption to settling particles contributed to the verti­
acteristics (e.g., particle size, polarity, and organic carbon content) due cal transport of the PCBs (Ma et al., 2018). Passive sampling employed
to changes in water chemistry with depth or microbial degradation may by Ma et al. (2018) has shown to be a valuable tool for assessing the
alter the bioavailability of organic pollutants (Lyytikäinen et al., 2003). vertical distribution of organophosphate esters (OPEs) and PBDEs in the
For example, sediments in the Blanes Submarine Canyon had poly­ Fram Strait (McDonough et al., 2018) and PCBs, PAHs, and OCPs in the
chlorinated dibenzofurans (PCDF) concentrations (754 ng kg− 1) Irminger Sea (Booij et al., 2014), although little vertical trends were
strongly correlated with soot (r2 = 0.852, p = 0.008) but not organic observed. In the Fram Strait, chlorinated OPEs were the most dominant
carbon content (Castro-Jiménez et al., 2013). This was probably because OPEs (34–100%) in the deep water mass compared to alkyl and aryl
PCDF strongly sorbs to soot and not to organic carbon as demonstrated OPEs (McDonough et al., 2018). The total concentration of the chlori­
by the low fOC (KOW/ρOC)/fSC•KSCW ratio (0.2–1), where fOC represents nated OPEs (0.006–0.430 ng L− 1) was an order of magnitude higher than
the mass fraction organic carbon, KOW the octanol-water partition co­ that of the alkyl/aryl compounds (0.0001–0.066 ng L− 1) (McDonough
efficient, ρOC the octanol density (g L− 1), fSC the mass fraction of soot et al., 2018). Chlorinated OPEs are more persistent in the deep water
content, and KSCW is soot-water partition coefficient (Castro-Jiménez mass since they are less degradable via hydrolysis or indirect photolysis
et al., 2013). The partitioning of PCDFs to soot in deep sea ecosystems than the alkyl/aryl OPEs. Particle, sediment, and water sampling chal­
might reduce their bioavailability resulting in the sediments acting as an lenges continue to limit our understanding of the role of particle size on
ultimate sink. Furthermore, Hadal sediments are known to have very the mass influx of organic contaminants in the deep ocean ecosystem.
low organic carbon content (< 0.22%), yet high concentrations of PCBs Passive samplers are more suitable for assessing the vertical and global
(930–4200 ng kg− 1) and PBDEs (245–590 ng kg− 1) have been detected distribution of organic pollutants since they are cost-effective, easier to
in hadal sediments from the Marian Trench (Dasgupta et al., 2018). The handle, and have high analyte enrichment potential. As a result, a global
hadal sediments had high contents of clay minerals such as illite, cli­ monitoring program for organic pollutants in global oceans, including
nochlore, and nontronite, which are known to promote (i) steric effects deep waters, called the Aquatic Global Passive Sampling (AQUA-GAPS)
between bulky or nonplanar organic pollutants and the clay minerals network was established in 2017 (Lohmann et al., 2017).
and (ii) the formation of complexes between weakly hydrated cations in Accumulation of organic pollutants in the deep sea can be influenced
the clay minerals and the negatively charged moieties of the organic by ocean stratification. Stratification in the St. Lawrence Maritime Es­
pollutants (Liu et al., 2015). Hence, there is need for additional studies tuary and Gulf water column occurred due to cold and oxygen-rich
on the role of sediment characteristics on the bioavailability of organic waters from the Labrador Current and warm and oxygen-deficient wa­
pollutants in deep sea. ters from the Atlantic Ocean isolated the surface waters and the deep
Compounds with low water solubility and high hydrophobicity often waters (Picard et al., 2021). The concentration ratios in subsurface to
preferentially partition to the rapidly sinking particles while those with deep water ratios were significantly higher for current-use PFAS (e.g.,
high water solubility preferentially remain in the water column. The the ratio for PFBS was 6.1) than legacy PFAS (e.g., the PFOS and PFOA
trend is probably not universal because a previous study found that there ratios were 2.5 and 1.8, respectively) (Picard et al., 2021). Pharma­
was no significant correlation between PFAS flux to the deep water layer ceuticals in the Gulf of Cadiz exhibited a similar trend, probably due to
and the hydrophobicity of the compounds (González-Gaya et al., 2019). the water column stratification caused by the presence of dense Medi­
In fact, long chain PFCAs which had a relatively higher hydrophobicity terranean waters and less saline Atlantic Ocean waters (Biel-Maeso
had low flux to the deep chlorophyll maximum (González-Gaya et al., et al., 2018). Since the water masses in stratified seas have different
2019). PFAS are probably transported from the surface to the deep water physicochemical properties, it is expected that the (bio)transformation
through the biological pump since González-Gaya et al. (2019) of the organic pollutants and the settling particles will differ with depth.
demonstrated that particle settling flux negatively correlated to the However, there are few studies on the role of water mass characteristics
dissolved phase concentration of PFAS in the deep chlorophyll and the fate of organic pollutants.
maximum. However, a previous study found that there was no signifi­
cant correlation between PFAS accumulation in phytoplankton and 4.4. Seafloor geomorphology
PFAS hydrophobicity (Casal et al., 2017). Hence, the adsorption or
bioaccumulation of PFAS such as PFOA to sinking particles is not Recent advances in exploration and sampling technology revealed

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deep sea ecosystems contain distinct geomorphological features such as Bioaccumulation and biomagnification of organic pollutants in deep
seamounts, submerged plateaus, submarine canyons, trenches, and hy­ sea biota are influenced by an interplay between interspecies traits such
drothermal vents (McClain and Rex, 2015). Besides being a hotspot of as habitat niche, vertical mobility, respiration rate, lipid composition,
faunal abundance, diversity, and sometimes endemism, deep sea metabolic capacity, and food web interconnectivity and oceanographic
geomorphological features often alter oceanographic conditions factors such as ocean currents (Castro-Jiménez et al., 2013; Romero-R­
(Rogers, 2015). The interaction between ocean currents and a steep omero et al., 2017). For example, a study in the Avilés Submarine
geomorphological feature (e.g., valleys, ridges, and canyons) often Canyon found that PCBs and PBDEs biomagnified in the pelagic but not
promotes the accumulation of organic matter and sediments that origi­ in the benthic food web (Romero-Romero et al., 2017). PCB-108, 118,
nate from the continental shelf zone (Astrahan et al., 2017). For 138, 153, and 180 were the most dominant congeners in deep sea biota,
example, Castro-Jiménez et al. (2013) found that the total 2,3,7, probably due to their abundance in technical mixtures. There was high
8-PCDD/Fs concentration of 17 congeners (102–680 ng kg− 1 d.w.) inter-specific variation in the distribution of the in the deep sea fish.
were three to six times higher in sediments at the deepest locations of the However, considering the limited sampling size of the study, additional
Blanes Submarine Canyon (1700 m depths) than at the shallow locations studies are required to assess intra-specific variations in organic
(500 m depths) or the adjacent open slope. Ocean current circulations in pollutant bioaccumulation. In the Blanes Submarine Canyon, the highest
submarine canyons promote the flushing of sediment particles and their PCDD/F concentrations were detected in nektobenthic crustaceans
associated organic pollutants down the slope resulting in the accumu­ (220–795 ng kg− 1 l.w.) and fish (110–300 ng kg− 1 l.w.) (Castro-Jiménez
lation of the sediments and organic pollutants in the deepest locations of et al., 2013). Since pelagic species have high vertical mobility, organic
the canyon. These ocean currents are often initiated by coastal storms pollutants bioaccumulation in pelagic species tends to be associated
and dense shelf water cascading (i.e., movement of water masses with the concentration of organic pollutants in primary producers and
following cooling, evaporation, or freezing of the ocean surface in the the surface water. In contrast, by inhabiting primarily on the seafloor,
shelf continent, resulting in dense water formation that sinks as warm benthic and nektobenthic species often have organic pollutants profiles
and saline water rises). A recent study in the Gulf of Cagliari revealed linked to deep sea sediments and waters as well as relatively highly
submarines canyons were the primary physical pathway transporting hydrophobic contaminants (Castro-Jiménez et al., 2013).
PAHs and PCBs from land to the deep sea (Tamburrino et al., 2019).
Astrahan et al. (2017) found that the highest amounts of organic matter 5. Future directions
in bottom sediments corresponded with the locations of ridgelines and
canyons. The sediments with high organic carbon content had higher Determining the mechanisms, pathways, and rates of fate and
concentrations of highly hydrophobic PCBs and PAHs (Astrahan et al., transport of organic pollutants in deep sea ecosystems is challenging as it
2017). In addition, seafloor geomorphology can also affect critical is a multidisciplinary endeavor requiring skills in physical oceanog­
ecosystem features such as population structure, composition, and raphy, analytical chemistry, biogeochemistry, marine ecology, envi­
function, which drive biotransformation and bioaccumulation of POPs ronmental microbiology, and even hydrology. Traditional approaches
in the deep sea (Costello and Chaudhary, 2017). A previous study found for sampling and detecting organic pollutants in environmental samples
seafloor morphologies such as troughs, sediment waves, and furrows based on oceanographic cruises are often time-consuming, labor-inten­
increased biodiversity in the deep sea, which in turn influenced sive, complex, and impractical for long-term monitoring due to cost. The
ecosystem processes (e.g., biological processes involved in the biological depth, high hydrostatic pressure, and low temperatures prevalent in
pump mechanisms) at a regional scale (Zeppilli et al., 2016). deep sea ecosystems limit the applicability of traditional technologies
for collecting, storing, and manipulating samples; hence, the scarcity of
4.5. Ecological implications deep sea environmental samples (Cario et al., 2019). Since deep sea
conditions are difficult and expensive to replicate in the laboratory,
The fate and transport behavior of organic pollutants in deep sea microcosm studies to investigate the (bio)transformation and sorption
ecosystems determine their magnitude and duration of exposure to deep behavior of organic pollutants is challenging. Hence, future studies
sea organisms. Hydrophobic organic pollutants such as DDTs, highly should answer the research questions described in Table 2 to better
chlorinated PCBs, and highly brominated PBDEs readily bioaccumulate understand the fate, transport, and impact of organic pollutants in deep
in deep sea organisms due to their high lipophilicity and recalcitrant sea ecosystems. We discuss these critical research topics in the subse­
nature. However, biomagnification and bioaccumulation of organic quent passages.
pollutants in deep sea ecosystems is influenced by the habitat niche (e.g., Traditional ocean monitoring approaches lack adequate spatial,
pelagic, benthic, and demersal), physicochemical properties, and vertical, and temporal coverage required for a multiscale, multi-
occurrence of the organic pollutants and metabolic capacity. For compartment, and multidisciplinary assessment of complex biogeo­
example, hydrophobic organic pollutants such as PCBs, DDTs, and chemical processes in the cast deep sea ecosystems. Biogeochemical
PBDEs with log KOW of 6.0–8.0 were shown to significantly bio­ processes controlling the chemodynamics of organic pollutants vary
accumulate in carnivorous fish such as blackbelly lanternshark (Etmop­ with space and time, hence the need for multi-dimensional coverage
terus lucifer), Kaup’s arrowtooth eel (Synaphobranchus kaupii), (Kaiser and Barnes, 2008). While autonomous platforms such as floats,
snubnosed eel (Simenchelys parasitica), and eelpout (Lycodes hubbsi) underwater vehicles, and floats have been successfully used in
(Takahashi et al., 2010). This suggested that feeding habits contribute measuring physical oceanographic processes, gravitational settling of
significantly to the biomagnification of organic pollutants in deep sea particles, and mechanisms and efficiency of biological carbon pump,
ecosystems. Organic pollutants with log KOW < 6.0 (e.g., HCHs, HCB, very few studies used the platforms to understand the chemodynamics of
and HBCDs) equilibrate relatively faster with the aqueous phase than organic pollutants (Chai et al., 2020). Autonomous underwater vehicles
DDTs, PBDEs, and highly chlorinated PCBs. As a result, while trophic are often used to map seafloor geomorphologies, locate ocean dumping
magnification can be expected for highly hydrophobic organic pollut­ sites, track contaminant plumes and thermocline, and collect environ­
ants, concentrations of HCHs and HCB have smaller variations across mental samples (Jones et al., 2019). Tracking the thermocline can be a
trophic levels (Takahashi et al., 2010). In addition, fish from the western powerful tool for assessing the role of deep-water formation or water
North Pacific Ocean and along the Oyashio Current had higher HCH mass flux in the input of organic pollutants in the deep sea (Table 2).
concentrations than those from warmer locations along the Kuroshio Coupling autonomous underwater vehicles with photometry can offer a
Current. Due to their high vapor pressure, HCHs readily partition to the detailed ephemeral view of the seafloor, and it has been previously used
atmosphere under warm conditions resulting in less HCH available for to identify ocean dumping of DDT containers (Kivenson et al., 2019). A
bioaccumulation in fish (Takahashi et al., 2010). previous study used a Sentry Precision Robotic Impeller Driven plankton

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E. Sanganyado et al. Water Research 205 (2021) 117658

Table 2.
A summary of key research areas that require further study in understanding the impact of organic pollutants in deep sea ecosystems.
Research topic Research question Major challenges and limitations Research priorities Key Refs.

Biological Are the concentrations of organic The effects of organic pollutants are Employ integrated chemical and (Deleo et al., 2021;
effects pollutants present harmful to the deep complex and species-specific. Most bioanalytical analysis to understand McConville et al., 2018;
sea ecosystems? studies focused on: (i) single compound the biological effects at a molecular Theron et al., 2020)
toxicity rather than mixture effects; (ii) and cellular level.
single species
Continental shelf-deep How does continental shelf Seafloor geomorphologies are an Identify the key characteristics of (Haalboom et al., 2021;
sea exchange geomorphology influence the interface between the continental shelf different geomorphologies (e.g., Romero-Romero et al.,
accumulation and transport of organic and the deep waters. However, their submarine canyon and trenches) that 2017; Salvadó et al.,
pollutants in the deep sea? complex and spatially variable physical influence organic pollutants 2012)
attributes may govern the accumulation accumulation and transport.
and transport of organic pollutants.
Air-sea exchange Does air-air-sea exchange influence Volatile and semivolatile organic There is a need for large scale data on (Ge et al., 2021)
the profile of organic pollutants pollutants often enter the deep sea via the distribution of organic pollutants
accumulating or leaving deep sea atmospheric deposition and pass in multiple environmental
ecosystems? through the productive euphotic zone, compartments such as air, ocean
where the composition may be altered surface, deep waters, and sediments.
by abiotic and biotic processes before
reaching the deep sea.
Temporal trends in Does changing usage patterns due to Although regulatory actions resulted in Use dated sediment cores to (Combi et al., 2020)
organic pollutants regulations influence the distribution decreased production and fresh reconstruct the historical inputs and
loading of organic pollutants in deep sea discharge of organic pollutants, annual fluxes of organic pollutants s in
ecosystems? primarily discharge from stockpiles and deep sea sediments.
old equipment is ongoing. Organic
pollutants are also secondarily
discharged from electronic waste,
melting glaciers, and unintentional
production.
Physical vs biological Is water mass more important than the Tracking water mass origins and the Establish the effect of vertical depth on (Dachs et al., 2002; Sun
pump biological pump, phytoplankton gravitational settling of particles in the the biogeochemical processes et al., 2016)
uptake, and other biogeochemical deep sea is challenging due to sampling controlling the fate of organic
processes controlling the vertical difficulties. pollutants.
distribution of organic pollutants in Conduct large-scale studies on the role
deep sea ecosystems? of phytoplankton uptake on global
dynamics of organic pollutants.
Source apportionment What are the sources of POPs in Organic pollutants from primary Employ chiral signatures, congener (Jones, 2021)
different deep sea ecosystems? sources often retain the composition of ratios, and changes in ratios of parent
the commercial mixture while those organic pollutants and their
from secondary sources are altered. metabolites to determine contaminant
However, the organic pollutants in deep sources.
sea ecosystems originate from multiple
sources.
Bioaccumulation and What are the mechanisms and Constructing deep sea food webs to Employ stable isotope ratios and (Cui et al., 2020;
biomagnification of pathways of the long-term biouptake determine the long-term biouptake of opportunistic sampling to construct Webster et al., 2014)
organic pollutants of organic pollutants in the deep sea organic pollutants is challenging due to deep sea food webs.
food web? How does it differ from sampling challenges. Biomagnification
other ecosystems? across the food web is influenced by the
physicochemical properties of the
organic pollutants, the local
oceanographic conditions, and
ecological factors.
Emerging Are emerging contaminants and More than 1,600 emerging Prioritization of emerging (Azaroff et al., 2020)
contaminants and transformation products accumulating contaminants have been identified as contaminants based on QSAR and
transformation in deep sea ecosystems? priority pollutants in marine usage patterns.
products environments. Identification of major inputs
Emerging contaminants enter the deep pathways of emerging contaminants in
sea through multiple input pathways. the deep sea.
Hence, investigating all emerging
contaminants is expensive, tedious, and
require highly sensitive and selective
analytical equipment.
Emerging contaminants transform in
the deep sea to form potentially more
toxic contaminants.

sampler coupled with autonomous underwater vehicles successfully sea species, linking exposure to biological response using chemical
collected plankton and larva from the Blake Ridge Seep (2160 m depth) analysis combined with biomarker analysis, transcriptomics, lipidomics,
on the US Atlantic Margin (Billings et al., 2017). Therefore, autonomous or metabolomics (Deleo et al., 2021), and paleo-ecotoxicology linking
platforms are valuable for assessing the role of biological and physical historical contamination to deep sea fossils of different biological or­
pumps in the global dynamics of organic pollutants in deep sea ganisms or species diversity changes using environmental DNA (Korosi
ecosystems. et al., 2017). Understanding the biological effects of organic pollutants
The difficulties in assessing biological responses following organic in deep sea ecosystems is difficult due to the complexity of the mixture
pollutants exposure in biota at spatial or temporal scale could be alle­ effect as biota are exposed to multiple threats (Sanganyado et al., 2020).
viated by using an autonomous underwater vehicle for sampling deep Current ecotoxicological assays often disregard the potential mixture

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E. Sanganyado et al. Water Research 205 (2021) 117658

effects caused by the interaction of the organic pollutants with natural 6. Conclusion
stressors such as salinity, cold temperature, and high hydrostatic pres­
sure prevalent in deep sea ecosystems (Mestre et al., 2014). In addition, Although organic pollutants have been detected in deep sea envi­
the bulk of the literature on organic pollutants in deep sea ecosystems ronments for the past 50 years, more data on biogeochemical,
tend to report total concentrations, while data on bioaccessibility and geophysical, oceanographic, and sedimentological processes are
bioavailability which are more relevant for assessing impact of organic required to make meaningful predictions of the global fate of organic
pollutants on ecosystem health, are scarce. Future studies on the bio­ pollutants in the deep sea. Such data can be obtained using passive
logical effects of organic pollutants should mimic the deep sea condi­ samplers as they have high analyte enrichment factor, low matrix in­
tions to ensure the ecotoxicological data generated for environmental terferences, provide concentrations of the bioavailable phase, and can
risk assessment is relevant and accurate. provide time-weighted average concentrations. However, most in­
There is a need for comprehensive studies exploring the impact of vestigations on the distribution of organic pollutants in deep sea envi­
sea-based activities such as deep sea mining on organic pollutants che­ ronments were conducted using active sampling techniques, while
modynamics and deep sea biogeochemical processes. The discharge of passive sampling is rarely used. Therefore, future studies on the che­
dissolved substances and nutrients due to deep sea mining activities modynamics of organic pollutants in the deep sea should employ passive
alters the seafloor morphology, benthic geochemistry, deep water sampling.
chemistry, primary production, and food web structure, which may There were significant variations in the vertical profiles of organic
change the biological and physical pump efficiencies (Levin et al., pollutants in particular deep seas or between regions. The variations
2020). Deep sea mining can cause habitat degradation, resulting in loss could be attributed to the pollutants (e.g., physicochemical properties
of biodiversity and species connectivity; thus, altering the food web such as log KOW, volatility, aqueous solubility, and use and production
structure. However, the lack of large-scale studies on the ecological patterns), oceanic currents (e.g., deep water formation and eddy diffu­
consequences of deep sea mining makes it difficult for regulators such as sion), and biogeochemical processes in the water column. Considering
the International Seabed Authority to develop toxicity thresholds that much of the deep sea remains unexplored and targeted analysis was
are adequate for minimizing the adverse effects caused by deep sea predominantly used in these studies, the chemodynamics of several
mining (Kaikkonen et al., 2018). Baseline studies on the biological, organic pollutants in much of the unexplored ocean remains unknown.
chemical and physical condition of the deep seabed are required to To better understand the ecological risk posed by organic pollutants,
ensure future environmental monitoring programs for organic pollut­ future studies should explore the factors influencing their bio­
ants can adequately determine the effect of exploration and exploitation accumulation and biomagnification in deep sea food webs. In addition,
activities (Ginzky et al., 2020). since the toxicological effects of organic pollutants on much of the deep
Large-scale monitoring of spatial and temporal changes in mass flow sea biota remain poorly understood, there is a need for experimental and
of organic pollutants in deep sea ecosystem is essential for under­ in vitro models for understanding the toxicity mechanisms of organic
standing the impact of human activities on the deep sea. While global pollutants in various deep sea biota. Autonomous underwater vehicles
monitoring systems have been proposed for monitoring current trends in equipped to deploy passive samplers can help extend the region of deep
the distribution of organic pollutants in oceans, historical emissions seas investigated, while suspect and non-target screening techniques
have been widely estimated using historical usage patterns. Linking could help investigate the behavior of ‘known unknown’ and ‘unknown
historical emissions data to changes in deep sea ecosystems is difficult unknown’ pollutants in the deep sea.
due to uncertainties in estimating organic pollutant flux and linking
exposure to biological response. Recent studies demonstrated that
combining paleolimnology and ecotoxicology techniques by assessing Declaration of Competing Interest
changes in contaminant profile and biological proxies (e.g., fossils and
environmental DNA) down a dated sediment core analysis could provide The authors declare that they have no known competing financial
critical data on historical emission and its associated ecological conse­ interests or personal relationships that could have appeared to influence
quences (Korosi et al., 2017). Deep sea sediment cores have been suc­ the work reported in this paper. The content of this publication has not
cessfully used to reconstruct past climatic and oceanographic changes been approved by the United Nations and does not reflect the views of
(Artemova et al., 2019; Toomey et al., 2013), evaluate recovery of the United Nations or its officials or Member States.
seafloor from bottom trawling (Paradis et al., 2021), assess changes in
microbial community structure with sediment depth (Wang et al., Acknowledgment
2010), and estimate historical flux of mercury in the Northwest Pacific
Ocean (Aksentov and Sattarova, 2020). Reconstructing past emissions of The authors gratefully acknowledge the financial support by the Key
organic pollutants particularly in oceans could help in assessing the Special Project for Introduced Talents Team of Southern Marine Science
impact of chemical regulations on organic pollutant flux in deep seas. and Engineering Guangdong Laboratory (Guangzhou) (Grant No.
Transformation products should not be overlooked when monitoring GML2019ZD0606), and Shantou University Research Start-Up Program
the distribution of organic pollutants in deep water ecosystems. In the St. (Grant No. NTF20002), Li Ka Shing Foundation Interdisciplinary
Lawrence Maritime Estuary and Gulf, the concentration of metolachlor Research Project (Grant No. 2020LKSFG04E).
ethanesulfonic acid, a metolachlor transformation product, was nearly
thirty times higher than that of the parent compound (Picard et al., Supplementary materials
2021). This is particularly concerning since metolachlor ethanesulfonic
acid was shown to be more toxic to zebrafish larvae than S-metolachlor Supplementary material associated with this article can be found, in
as they caused overexpression of genes involved in the regulation of the the online version, at doi:10.1016/j.watres.2021.117658.
thyroid system and cell cycle (Rozmánková et al., 2020). Additionally,
determination of transformation product and parent compound ratios
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