Assessing the Impacts of Oil-Associated Marine Snow Formation And

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Anthropocene 13 (2016) 18–33

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Anthropocene

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Review

Assessing the impacts of oil-associated marine snow formation and

sedimentation during and after the Deepwater Horizon oil spill

a, b c a

Kendra L. Daly *, Uta Passow , Jeffrey Chanton , David Hollander

College of Marine Science, University of South Florida, St. Petersburg, FL 33705, United States

Marine Science Institute, University of California, Santa Barbara, CA 93106, United States

Earth, Ocean, Atmospheric Science, Florida State University, Tallahassee, FL 32306, United States

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

Article history: The Deepwater Horizon oil spill was the largest in US history, unprecedented for the depth and volume of

Received 20 October 2015

oil released, the amount of dispersants applied, and the unexpected, protracted sedimentation of oil-

Received in revised form 27 January 2016

associated marine snow (MOS) to the seaﬂoor. Marine snow formation, incorporation of oil, and

Accepted 28 January 2016

subsequent gravitational settling to the seaﬂoor (i.e., MOSSFA: Marine Oil Snow Sedimentation and

Available online 2 February 2016

Flocculent Accumulation) was a signiﬁcant pathway for the distribution and fate of oil, accounting for as

much as 14% of the total oil released. Long residence times of oil on the seaﬂoor will result in prolonged

Keywords:

exposure by benthic organisms and economically important ﬁsh. Bioaccumulation of hydrocarbons into

Deepwater Horizon oil spill

the food web also has been documented. Major surface processes governing the MOSSFA event included

Gulf of Mexico

an elevated and extended Mississippi River discharge, which enhanced phytoplankton production and

Marine oil snow

MOSSFA suspended particle concentrations, zooplankton grazing, and enhanced microbial mucus formation.

Bacteria Previous reports indicated that MOS sedimentation also occurred during the Tsesis and Ixtoc-I oil spills;

Plankton thus, MOSSFA events may occur during future oil spills, particularly since 85% of global deep-water oil

exploration sites are adjacent to deltaic systems. We provide a conceptual framework of MOSSFA

processes and identify data gaps to help guide current research and to improve our ability to predict

MOSSFA events under different environmental conditions. Baseline time-series data and model

development are urgently needed for all levels of ecosystems in regions of hydrocarbon extraction to

prepare for and respond to future oil spills and to understand the impacts of oil spills on the environment.

ã 2016 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND

license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Contents

1. Introduction ...... 19

2. Characterization of oil-associated marine snow: processes and pathways ...... 20

2.1. Marine snow distribution and sedimentation patterns ...... 20

2.2. Factors affecting MOSSFA processes ...... 21

2.3. Field and lab MOS formation ...... 22

2.4. Microbial processes ...... 22

2.5. Plankton impacts on MOS ...... 23

2.6. Oil-mineral aggregates (OMAs) ...... 24

2.7. MOS sedimentation ...... 24

3. Temporal and spatial patterns of MOS ...... 24

4. Deep oil plumes ...... 25

5. Oil accumulation rates and fate at the seaﬂoor ...... 26

6. Ecosystem effects ...... 27

7. Proposed framework for MOSSFA investigations and data gaps ...... 28

7.1. Physical and chemical characteristics of oil droplets and associated hydrates (A) ...... 29

7.2. Formation of subsurface oil plumes: droplet and bubble size (B) ...... 29

* Corresponding author. Fax: +1 7275531189.

E-mail address: [email protected] (K.L. Daly).

http://dx.doi.org/10.1016/j.ancene.2016.01.006

2213-3054/ã 2016 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

K.L. Daly et al. / Anthropocene 13 (2016) 18–33 19

7.3. Important processes in the surface mixed layer (C) ...... 29

7.3.1. Interaction of oil droplets with euphotic zone plankton (C1) ...... 29

7.3.2. Transformation of oil ﬂoating at the atmosphere-ocean interface (C2) ...... 29

7.3.3. New sources of material at the surface (C3) ...... 29

7.3.4. Sinking of oil-derived material from the surface (C4) ...... 29

7.4. Processes impacting MOS during sedimentation (D) ...... 29

7.5. Processes impacting MOS on the seaﬂoor (E) ...... 29

7.6. Processes impacting resuspension of oiled sediments (F) ...... 29

8. Conclusions ...... 30

Acknowledgements ...... 30

References ...... 30

1. Introduction ultimately covered up to 68,000 square miles (180,000 km ) of

ocean before it was contained (Norse and Amos, 2010), including

The 2010 Deepwater Horizon (DWH) oil spill (Fig. 1), which coastal, deep water, and riverine inﬂuenced regions. The outﬂow

began on April 20th and ended on July 15th, was unprecedented for from the Mississippi River and associated distributary channels

several reasons: (1) the oil outﬂow originated from an ultra-deep was above climatological mean between mid-May and October of

well at 1500 m, (2) the large volume of oil released (about 2010, which inﬂuenced the near surface transport of oil

4.9 million barrels or 779 million L), (3) the large amount of (Kourafalou and Androulidakis, 2013). Typically, the river

6 À1

dispersants (Corexit EC9500A and EC9527A; about 2.1 million discharges about 130–150 10 t year of sediment (Corbett

gallons or 7.9 million L) released in deep water and at the sea et al., 2006; Bianchi et al., 2007); hence, riverine suspended

surface (Kujawinski et al., 2011; McNutt et al., 2012; Lubchenco mineral particles likely interacted with oil (Muschenheim and Lee,

et al., 2012), and (4) the unexpected and protracted sedimentation 2002; Khelifa et al., 2005) to form sinking oil-mineral aggregations

event of oil-associated marine snow to the seaﬂoor (Passow, 2014; (OMAs) in addition to MOS. Signiﬁcant sediment and hydrocarbon

Brooks et al., 2015; Romero et al., 2015). deposition to the seaﬂoor was observed in the DeSoto Canyon

The Oil Budget Calculator Science and Engineering Team region to the east of the Deepwater Horizon wellhead (Brooks et al.,

reported that by the end of the oil spill 17% of the South Louisiana 2015; Romero et al., 2015) and elsewhere (White et al., 2012;

Sweet Crude oil (MS252) had been recovered at the wellhead, 5% Montagna et al., 2013; Valentine et al., 2014; Chanton et al., 2015).

burned, 16% chemically dispersed, 13% naturally dispersed, 23% Based on combined sedimentology, geochemical, and biological

evaporated or dissolved, with 23% remaining in an Other category approaches, this mass deposition was primarily a product of

(Lehr et al., 2010; McNutt et al., 2012). The Oil Budget Calculator marine snow formation and appears to have occurred over a

was designed as a response tool to inform response actions and 4–5 month period during and after the oil spill, far exceeding pre-

cleanup decisions and was not intended to be a research or damage spill sediment accumulation rates (Brooks et al., 2015). A high

assessment tool. Consequently, oil sedimentation and its accumu- degree of patchiness in the deposition of oil on the seaﬂoor,

lation on the seaﬂoor were not speciﬁcally considered in the oil combined with the large geographic area of the sedimentation

budget calculation. However, early scientiﬁc investigations of the event (including on the upper continental slope and shelf), makes

oil spill noted that high concentrations of oil-associated marine it a difﬁcult task to estimate the total amount of oil transported to

snow (herein marine oil snow or MOS) were observed in the depth. Nevertheless since the oil spill ended, Valentine et al. (2014)

vicinity of surface oil and the sub-surface oil plumes (e.g., Passow estimated that 1.8–14% of the oil was transported to the seaﬂoor

et al., 2012; Daly et al., 2013). Based on satellite images, the oil spill using hopanes as a biomarker-tracer, while Chanton et al. (2015)

3 2

Fig. 1. The surface distribution of Deepwater Horizon oil. Average volume of surface oil (m /km ) in 5 Â 5 km gridded cells between 24 April and 3 August 2010, based on SAR

satellite data (after MacDonald et al., 2015).

20 K.L. Daly et al. / Anthropocene 13 (2016) 18–33

estimated the amount at 0.5–9% using radiocarbon distributions. 2. Characterization of oil-associated marine snow: processes

For comparison, Boehm and Fiest (1980) estimated 1–3% of the oil and pathways

from the Ixtoc-I spill in the southern Gulf of Mexico (1979–1980)

reached the shallower seaﬂoor in that region, while Jernelöv and 2.1. Marine snow distribution and sedimentation patterns

Lindén (1981) estimated 25% of the Ixtoc oil sank to the seaﬂoor by

mass balance. Marine snow is deﬁned as particles >0.5 mm to 10 s of cm in

In May 2010, BP committed $500 M for the Gulf of Mexico size, which may consist of aggregations of smaller organic and

Research Initiative (GOMRI) to investigate the impacts of oil and inorganic particles, including bacteria, phytoplankton, micro-

dispersants on the Gulf of Mexico ecosystems. Preliminary ﬁndings zooplankton, zooplankton fecal pellets and feeding structures

reported at conferences and in discussion groups indicated that (e.g., larvacean houses), biominerals, terrestrially-derived litho-

MOS led to signiﬁcant oil sedimentation to the seaﬂoor. The GOMRI genic components, and detritus (Alldredge and Silver, 1988).

funded Marine Oil Snow Sedimentation and Flocculent Accumula- Marine snow occurs throughout the world’s oceans and at all

tion (MOSSFA) Workshop was held during October 2013, with the depths. Marine snow is formed in near surface waters where

goal to obtain community input, particularly on three topic areas: particle abundances vary spatially and seasonally, usually between

À1 À1

(1) factors affecting the formation and sinking of MOS in the water 1 and 14 particles per L (range 0–500 particles L ) (Alldredge

column, (2) the deposition, accumulation, and biogeochemical fate and Silver, 1988). In the Gulf of Mexico, suspended particle

of MOS on the seaﬂoor, and (3) the ecologic impacts of MOS on concentrations off Louisiana during April 1987 were reported to

À1 À1

pelagic and benthic species and communities (MOSSFA Workshop range from 10–60 particles L on the shelf to 0.2 to >3 particles L

Report, 2014; Kinner et al., 2014). The purpose of this review is to on the slope, declining with depth and then increasing near bottom

À1

raise awareness that the settling of MOS may play a signiﬁcant role (1.6–3.3 particles L ) (Gardner and Walsh, 1990). Aggregates in

in the distribution and fate of spilled oil in both shallow and deep the Mississippi Canyon were assessed for size and settling rates

water environments, and that sinking and sedimentary-oil below the mixed layer at 167 m depth during October 1993

deposition should be considered in future oil spill response (Diercks and Asper, 1997). Aggregates typically ranged between

assessments. Here, we report on the MOSSFA Workshop ﬁndings, 0.5 and 3.5 mm in diameter, with one aggregate at 7.3 mm. Settling

À1

provide a summary of the current state of knowledge related to the rates ranged from 10 to 85 m d , with the largest particle having a

Deepwater Horizon marine snow-oil deposition event, present a rate similar to 1–2 mm particles. Particle abundances near coastal

mechanistic framework of MOSSFA processes, and offer examples shelves in this region also may be elevated at midwater depths as a

of data gaps, as well as providing recommendations for future result of benthic resuspension by mesoscale circulation features

research. A comprehensive review of marine snow is outside the and transport (lateral advection) of particles off the shelf and slope

scope of this paper; for general background information see, for (Walsh and Gardner, 1992; Diercks and Asper, 1997). Relatively

example, Alldredge and Silver (1988),Simon et al. (2002), Turner high concentrations of suspended aggregates (20–250 particles

À1

(2002), and Burd and Jackson (2009). L ) were observed in a bottom nepheloid layer in the Mississippi

Canyon following the passage of Hurricane Isaac in August 2012,

with most aggregates <1 mm in diameter (Ziervogel et al., 2015).

Fig. 2. Particle size spectra of marine snow and examples of marine snow images observed by the SIPPER imaging system during August 2010, September 2011, August 2012,

August 2013, and August 2014. The particle size distribution data are from a station 50 km to the east of the DWH site.

K.L. Daly et al. / Anthropocene 13 (2016) 18–33 21

In comparison, within one month after the wellhead was capped 2.2. Factors affecting MOSSFA processes

(August 2010), marine snow concentrations ranged from 10.5 to

À1

64.6 particles L in the upper 20 m of off-shelf waters in the region There are many factors that impact the formation and

of the oil spill, with particle sizes ranging from 0.150 to 17.6 mm in modiﬁcation of MOS in the water column (Figs. 3–5). Figs. 3–5

diameter (Daly et al., 2014). Oil concentrations (total petroleum were developed as part of the MOSSFA Workshop discussions.

hydrocarbons, TPH, and polycyclic aromatic hydrocarbons, PAH) Fig. 3 focuses on surface processes, Fig. 4 illustrates processes from

were still elevated compared to background levels within 800 km the origin of oil outﬂow to ﬁnal oil deposition, and Fig. 5 depicts the

of the wellhead during August, albeit at lower concentrations than impacts of gradients driven by riverine processes on MOS in the

were observed prior to capping the wellhead (Wade et al., 2015). water column, on the seaﬂoor, and within the sediments. These

The August 2010 maximum marine snow concentrations diverse factors emphasize the complex nature of the ocean

À1

(64.6 particles L ) were considerably higher in near surface environment and its interactions with oil blowouts. Factors shown

À1

waters, than during September 2011 (2 particles L ), August in Fig. 3 include (1) riverine gradients of salinity and inputs of

À1 À1

2012 (4.9 particles L ), August 2013 (20.7 particles L ), or August nutrients, dissolved organic matter, and lithogenic material

À1

2014 (1.5 particles L ) at a deep-water station 50 km to the east of inﬂuences particle aggregation (Muschenheim and Lee, 2002),

the DWH site. Integrated abundances (0–140 m) of marine snow because coagulation is a function of particle abundance and size

also showed a similar pattern of maximum concentrations during (Burd and Jackson, 2009). Nutrients enhance phytoplankton

À2

August 2010 (866,862 particles m ) at this site compared to growth and dissolved organic matter forms gel particles, especially

summer concentrations during the following four years in salinity gradients (Wetz et al., 2009; Verdugo et al., 2004).

(September 2011: 190,375, August 2012: 181,644, August 2013: (2) Marine biota may form or destroy marine snow (Alldredge and

À2

238,574, and August 2014: 74,311 particles m ) (Fig. 2). Silver, 1988; Burd and Jackson, 2009). For example, phytoplankton

The dominant factors controlling gravitational settling of and bacteria release ‘sticky’ exopolymeric substances (EPS) due to

surface particles and aggregates vary spatially and temporally oil and dispersant exposure and mucus acts as glue, providing the

(Boyd and Trull, 2007). Sinking speeds, however, are primarily a matrix for aggregates (Passow, 2014). Biological formation also

function of particle size and excess density (i.e., particle includes processes such as incorporation into zooplankton feeding

density > seawater density) (Armstrong et al., 2002; Iverson and structures and feces and microbial generated marine snow.

Ploug, 2010; De La Rocha and Passow, 2007). Sinking speeds of Alternatively, zooplankton feeding on MOS may lead to fragmen-

marine snow range from 10 s to 100 s of meters per day. Slowly tation of particles. Both microbial degradation of hydrocarbons to

sinking particles are removed by microbial remineralization or non-toxic forms (Kleindienst et al., 2015a) and bioaccumulation

grazing and, therefore, rarely reach great depths. The formation into the food web (Lee et al., 2012; Chanton et al., 2012) occur.

and ﬂux of rapidly sinking marine snow is one of the primary (3) Mediating measures, such as chemical dispersants and burning,

processes by which the marine biological pump exports surface affect the properties and behavior of hydrocarbons and inﬂuence

carbon and other elements to the deep ocean and seaﬂoor. the formation of MOS (Passow, 2014). Dispersants break down oil

Fig. 3. Image depicts the factors that affect the formation and modiﬁcation of MOS. The blue triangle represents the area of the oil spill. MOS is affected by the ocean

environment, the state (degree of weathering) and composition of oil, spatial overlap with riverine and shelf processes, the type of marine biota present and their related

processes, and the timing and location of spill mediation measures (e.g., application of dispersants and burning).

22 K.L. Daly et al. / Anthropocene 13 (2016) 18–33

Fig. 4. Conceptual diagram of MOS related processes from the source of oil discharge to the fate of hydrocarbons in sediments. (A) Shows the release of oil at the wellhead and

application of dispersants and (B) represents rising oil droplets and gas bubbles and the formation of a deep oil plume. (C1–C4) Shows surface processes inﬂuencing the

formation of MOS: (C1) illustrates wind impacts, a diatom bloom, and application of surface dispersants, (C2) shows oil transformation due to UV light and evaporation, (C3)

depicts the role of aerosols and oil burning in creating new material sources, and (C4) shows processes impacting sinking MOS particles in surface waters and as particles sink

through (D) a benthic nepheloid layer and deep oil plumes. (E) Shows benthic sedimentation of MOS and ﬂocculation onto corals, and (F) represents resuspension of oiled

sediments due to turbulence. See the text for a more detailed explanation of the ﬁgure.

À1

into small droplets, but may inhibit microbial oil degradation (see 68 to 553 m d . Laboratory experiments elucidated some of the

Section 2.5, Kleindienst et al., 2015b). Oil burning leaves about 5% mechanisms leading to the formation of MOS by using roller tanks

of the original volume as burned residue such as black carbon and to simulate in situ conditions. Roller tanks allow marine snow to

other pyrogenic by-products (Lehr et al., 2010). Black carbon settle continuously without contact with surfaces (container

particles efﬁciently absorb organic matter, including PAHs walls) (Ploug et al., 2010). These experiments revealed a number

(Koelmans et al., 2006), and can stimulate transparent exopolymer of important processes, including, (1) diatom aggregates incorpo-

particle (TEP) production and aggregation of marine snow (Mari rated appreciable amounts of oil, either by collision and attach-

et al., 2014). (4) Weathering, or aging, and photochemical ment of oil droplets with phytoplankton cells, or via absorption of

alterations to oil similarly impact MOS properties (Bacosa et al., oil to phytoplankton, (2) oil droplets were incorporated into

2015; Passow, 2014). Photo-oxidation is the process by which colonies of cyanobacteria (Trichodesmium) through coagulation,

hydrocarbons, particularly PAHs, react with oxygen in the presence and (3) bacteria mediated MOS formation in the absence of other

of sunlight, resulting in chemical and structural changes to oil that particles, possibly through the release of high concentrations of

may lead to increased water solubility or decreased microbial mucus (Passow et al., 2012; Fu et al., 2014; Passow, 2014).

biodegradation. (5) Physical processes may lead to aggregation of Interactions between oil components, bacteria, and natural

particles due to collision or high turbulence may result in particle suspended matter formed ﬂocs (relatively large, ﬂuffy aggregates)

fragmentation (Hill et al., 2002; Burd and Jackson 2009). Currents, likely due to the formation of macro-gels, such as TEP, from EPS

eddies, subductions, benthic resuspension and cross-shelf ﬂow, released by bacteria in response to the presence of oil (Passow

and other physical processes impact the distribution of particles et al., 2012; Ziervogel et al., 2014). A complicating factor was the

and oil pollutants in space and time (e.g., Paris et al., 2012; Smith presence of the dispersant, Corexit, which at near in situ

et al., 2014). These processes all inﬂuence the dynamics of sinking concentrations slowed or inhibited the formation of microbial

MOS. MOS (Passow 2014). However, after longer incubations, possibly

once Corexit was degraded, marine snow formed (Fu et al., 2014).

2.3. Field and lab MOS formation

2.4. Microbial processes

Large, mucus-rich MOS particles were observed in surface oil

during May, ranging in size from small compact particles to Numerous microbes are able to utilize oil as a major source of

particles several centimeters in size. Large, stringy marine snow carbon and energy, including 175 genera of bacteria, several

particles (<10 cm), with mucous threads resembling web-like haloarchaeal genera, and many Eukarya (McGenity et al., 2012).

structures, were also common (Passow et al., 2012). Sinking Microbial response to an oil spill is governed by many factors,

velocities for settling MOS particles were estimated to range from including oil composition, degree of oil weathering, and

K.L. Daly et al. / Anthropocene 13 (2016) 18–33 23

Fig. 5. Diagram illustrates the environmental gradients of material properties and fluxes associated with a point source of oil released in regions influenced by river outflow

compared to offshore regions not inﬂuenced by riverine processes. Gradient shifts include the concentration and composition of suspended particles (clays to carbonate), the

magnitude of particulate organic carbon (POC) and petrochemical ﬂuxes to the seaﬂoor, the depth of the sediment redoxcline, and the tolerance of benthic organisms, such as

foraminifera, to different oxygen levels in sediments. Oil-mineral aggregations (OMAs) may sediment separately or in association with marine oil-snow (MOS). These

environmental gradients overlap and interact with gradients generated by oil spills, e.g., oil and dispersant distributions, causing a complex temporal-spatial distribution of

interactive effects.

environmental conditions, such as temperature and nutrient which was abundant during the DWH oil spill (Yan et al. in review,

concentrations. The temporal and spatial variability in microbial Passow unpubl.), provide a biotope for hydrocarbonclastic bacteria,

populations before, during, and after the DWH oil spill, and in which appear to specialize in PAH degradation. While signiﬁcant

comparison with communities outside of the spill, showed that progress has been achieved in documenting shifts in the bacterial

groups of oil-degrading bacteria responded to the presence of oil community in response to the oil spill, the spatial and temporal

by May 2010, including alkane, PAH, and methane degraders, and variability of microbial effects on MOS formation and degradation

nitrifying microorganisms (Dubinsky et al., 2013; Yang et al., 2014; remain poorly known.

Crespo-Medina et al., 2014; King et al., 2015). Overall, the relative

importance of different taxa was governed by changes in 2.5. Plankton impacts on MOS

hydrocarbon composition and supply. Surface oil communities

appeared to have been more diverse than communities in the deep Microplankton, microzooplankton, and mesozooplankton were

oil plumes (Kimes et al., 2014). By September 2010, the pre-spill impacted by the spilled oil, which likely affected marine snow

community was re-established, with low background concen- formation and sedimentation. Crude oil and the dispersant Corexit

trations of oil degrading bacteria. In both surface and deep waters, are reported to have had direct lethal and sublethal effects on

MOS particles were colonized by heterotrophic microbes, which bacteria, phytoplankton, microzooplankton (Garr et al., 2014;

expressed high speciﬁc rates of enzymatic activity that were Almeda et al., 2014b; Kleindienst et al., 2015a,b) and mesozoo-

different from those of the surrounding seawater (Ziervogel et al., plankton, including changes in physiology and reproduction

2012; Arnosti et al., 2015). In addition, several bacterial species that (Ortmann et al., 2012; Almeda et al., 2013a,b, 2014c; Cohen

are noted for producing EPS had elevated concentrations in surface et al., 2014; Peiffer and Cohen, 2015). The impact of dispersants,

waters during the oil spill and formed mucus aggregates that however, is being debated. Prince (2015) argues that dispersants

contained oil droplets in lab experiments (Gutierrez et al., 2013). are not signiﬁcantly toxic under typical oil spill ﬁeld conditions,

In situ MOS particles also had signiﬁcant concentrations of they make oil more bioavailable for degradation, and impacts on

glycoprotein (carbohydrate and protein), a primary component seabirds are minimized. In contrast, a number of studies have

of EPS (Arnosti et al., 2015). Speciﬁc bacteria respond to oil in indicated that toxic effects on pelagic organisms increased with the

different ways, but in general, microbial communities produce addition of Corexit to oil treatments, although results varied

mucus that acts like a bioﬁlm, allowing a complex community to between taxa (e.g., Almeda et al., 2013b, 2014b; Cohen et al., 2014;

establish, which jointly utilizes the different components of oil and Garr et al., 2014). Kleindienst et al. (2015b) also reported that the

its metabolites (McGenity et al., 2012). Bacterial EPS also may presence of Corexit decreased microbial degradation rates of

stimulate non-oil degrading bacterial communities. Mishaman- hydrocarbons, by selecting for bacteria that degrade dispersant

dani et al. (2015) demonstrated that eukaryotic phytoplankton, (i.e., Colwellia) rather than bacteria that degrade hydrocarbons (i.e.,

such as the cosmopolitan marine diatom, Skeletonema costatum, Marinobacter). These authors suggested that dispersants might

24 K.L. Daly et al. / Anthropocene 13 (2016) 18–33

stimulate hydrocarbon degradation in other marine systems that Since the DWH platform was about 75 km offshore directly

do not already have a background population of hydrocarbon- southeast from the Mississippi River, OMAs may have played a

degrading bacteria. The Gulf of Mexico harbors hydrocarbon- role in DWH oil deposition.

degrading bacteria at low densities, due to chronic oil input from

cold seeps. 2.7. MOS sedimentation

Crustacean molts and dead zooplankton typically become part

of the marine snow assemblage, sinking rapidly out of the water The role of MOS in DWH oil sedimentation is supported by data

column. Zooplankton (e.g., dinoﬂagellates, gelatinous doliolids, from a sediment trap deployed in late August 2010 about ﬁve km

copepods) ingest oil and egest oil in fecal pellets, which sink southwest of the DWH platform, 140 m above the seaﬂoor at

rapidly to the seaﬂoor (Lee et al., 2012; Almeda et al., 2014a,c). 1400 m depth. The trap results showed exceptionally high POC

Størdal et al. (2015) demonstrated that despite reduced feeding sedimentation rates relative to other years, which were due to the

activity by a North Sea copepod in the presence of oil, their fecal sinking of a large diatom bloom that was almost entirely composed

pellets contained oil plus oil-degrading bacteria (Rhodobacter- of Skeletonema sp. (Yan et al. in review, Passow unpubl.), a

aceae), which were indigenous to the copepods. This family of cosmopolitan taxa that thrives under brackish conditions and is

bacteria was a dominant group present after the DWH spill tolerant of the presence of oil (Parsons et al., 2014). Sedimentation

(Dubinsky et al., 2013; Kimes et al., 2014); hence, zooplankton may of oil continued for >5 months after the spill ended, characterized

contribute to oil degradation. In addition, oil may adhere to by numerous smaller events (Yan et al. in review, Passow unpubl.).

zooplankton and be passively absorbed or ingested; thus, Lithogenic minerals (i.e., silts and clays) co-settled with organic

contributing to bioaccumulation of PAHs (Mitra et al., 2012). particles and constituted on average 60% per weight of the settled

Furthermore, carbon isotopic depletion in suspended particulate material. Biogenic silica from diatom frustules and organic carbon

matter and zooplankton supports the notion that oil carbon was composed other signiﬁcant portion, whereas little calcium

incorporated into the lower trophic food web through biodegra- carbonate was observed in trap material.

dation by bacteria (Graham et al., 2010; Chanton et al., 2012;

Cherrier et al., 2014). 3. Temporal and spatial patterns of MOS

2.6. Oil-mineral aggregates (OMAs) Although the overall processes related to the formation of MOS

and OMAs are reasonably well know, less is known about the

Interactions between oil and suspended particulate material, or temporal and spatial variability of their formation and deposition,

OMAs as they have been designated in the literature, have long which are generally regulated by physical processes. Wind forcing

been recognized to result in oil sedimentation in freshwater and was the primary mechanism governing surface oil drift (Le Hénaff

marine systems, especially in tidal and subtidal areas (Lee, 2002; et al., 2012). In addition, freshwater discharge from the nearby

Payne et al., 2003). OMAs are usually smaller (<1 mm, often Mississippi River, which is the world’s third largest river, often

<50 mm) than most marine snow particles (Stoffyn-Egli and Lee, results in strong stratiﬁcation and enhanced wind-driven coastal

2002) and form primarily in surf zones, near river outﬂows, jets (Morey et al., 2003; Jochens and DiMarco, 2008). During April

melting glaciers or sea ice, and in semi-enclosed bays, where 2010, freshwater diversions along the lower Mississippi River were

suspended lithogenic particle concentrations are relatively high opened with the intent to minimize the impact of the oil spill on

(Lee and Page, 1997; Payne et al., 2003). Boehm (1987) estimated estuaries and wetlands (Bianchi et al., 2011). Kourafalou and

that suspended particle concentrations need to be > 10 mg/L for Androulidakis (2013) concluded that in addition to wind forcing,

significant deposition of oil to occur and >100 mg/L for large Mississippi River induced circulation also significantly influenced

deposition events. Since inorganic particles concentrations are near surface oil transport based on satellite and in situ data and

usually <10 mg/L in the open ocean, this pathway was considered numerical simulations. Winds blowing from the south reduced the

to be relatively unimportant offshore of intertidal/subtidal regions. interaction of surface oil with the Loop Current, consequently only

Offshore suspended drilling muds may be considered an exception. a small amount of oil was trapped in a spin off eddy (Eddy Franklin)

A review of near-shore oil spills indicated that 1–13% of spilled (Le Hénaff et al., 2012). A number of processes, which likely

oil settled to the seaﬂoor due to OMA processes (Lee and Page, inﬂuenced weathering of MC252 crude oil, including physical

1997). The interactions between suspended particulate matter, oil agitation, wave conditions, evaporation, photo-oxidation, and

weathering, adsorption, microbial processes, other marine snow dispersability, were summarized in Daling et al. (2014). Three

particles, and grazing zooplankton impact oil packaging and MOS storm events during the oil spill, of which two were named (e.g.,

sedimentation (reviewed in Muschenheim and Lee, 2002). OMAs Hurricane Alex, Tropical Storm Bonnie), led to a change in surface

sink rapidly, in spite of their small size, because of their high oil extent and deep mixing (Goni et al., 2015), but the storm

mineral content. OMA formation increases the surface to volume impacts on the oil spill and oil deposition are for the most part

ratio of oil, thereby extending and enhancing the weathering unknown. Previous studies during hurricanes observed signiﬁcant

processes of dissolution, evaporation, and biodegradation vertical variations in currents and internal waves (Shay and

(Lee, 2002). Water turbulence (i.e. breaking waves, strong ﬂood Elsberry, 1987; Keen and Allen, 2000) Storm induced resuspension

currents) enhances OMA formation and transport and mineral-oil of ﬂocculent material deposited on the seaﬂoor during the DWH

ﬂocculation rates are typically highest in low to intermediate event was shown to lead to increased microbial activities

salinity waters. Danchuk and Willson (2011) suggested that OMA (Ziervogel et al., 2015). In addition, the Loop Current, eddies,

formation in the vicinity of the Mississippi River would vary cross-shelf ﬂows, and mesoscale circulation are important physical

depending on the time of year and type of oil. Lighter oils had a processes in the NE Gulf of Mexico, which impact biological

higher probability of forming OMAs during winter and spring, production and oil transport (Nababan et al., 2011; Olascoaga et al.,

when there was higher sediment availability and denser, high- 2013; Goni et al., 2015; Jones and Wiggert, 2015; Smith et al., 2014).

viscosity oil may form more OMAs during summer, when salinity Biological factors were another major inﬂuence on the spatial—

was higher. OMAs form where oil and suspended minerals temporal patchiness of the formation and fate of MOS. During

(including clay-sized particles) co-occur, whereas lithogenic August 2010, satellite data (MODIS Fluorescence Line Height)

material from, for example, a deep nepheloid layer may be showed unusually high chlorophyll concentrations compared to

scavenged by sinking marine snow passing through that layer. the mean of an eight-year time-series for the NE Gulf of Mexico.

K.L. Daly et al. / Anthropocene 13 (2016) 18–33 25

This chlorophyll maximum was located to the east of the DWH wellhead was capped, the plumes were estimated to have reached

wellhead and covered an area >11,000 km (Hu et al., 2011). These up to 300 km in extent, with oil concentrations ranging from 5 to

elevated phytoplankton concentrations appeared to be related to 500 ppb, and had interacted with the slope sediments of the

the oil spill since the high river ﬂow anomalies did not correlate Mississippi and Desoto canyons (Paris et al., 2012; Lindo-Atichati

with the spatial area of the chlorophyll anomaly. Whereas et al., 2014; Romero et al., 2015).

exposure to high concentrations of oil is lethal to most Socolofsky et al. (2011) demonstrated that the deep subsurface

phytoplankton, sensitivity to hydrocarbons varies and some oil plumes derived from a stratiﬁcation-dominated multiphase

species thrive under low concentrations of oil (Parsons et al., plume, which was characterized by multiple subsurface intrusions

2014; González et al., 2013). In addition to the region of the of dissolved gas and oil, as well as small droplets of liquid oil.

elevated chlorophyll anomaly, nutrients from the Mississippi River Simulations by North et al. (2015) emphasized the importance of

fueled phytoplankton blooms during 2010 (Hu et al., 2011), which oil droplet size and rates of biodegradation in understanding

are typically observed every year in the vicinity of the river plume factors controlling oil transport. Based on a model comparison

(Lohrenz et al., 1997). Large mucus-rich marine snow particles study, DWH oil droplet sizes were predicted to have ranged from

were observed ﬂoating in surface waters during May, but had 0.3 to 6 mm without the addition of dispersants and between 0.01

disappeared by June (Passow et al., 2012). Other types of marine and 0.8 mm with the addition of dispersants (Socolofsky et al.,

snow, however, remained in relatively high concentrations at least 2015). Ryerson et al. (2012) estimated that the majority of oil

into August (Daly et al., 2014). Similarly, Patton et al. (1981) noted droplets that arrived at the sea surface were millimeters in

that pancakes and ﬂakes of mousse or weathered oil occurred at diameter based on hydrocarbon mass transport calculations. Aman

the surface during the Ixtoc-I oil spill. In addition, large numbers of et al. (2015) reported that droplets <40 mm formed the deep lateral

dead gelatinous zooplankton (Pyrosoma sp.) were observed ﬂoating oil intrusions, whereas larger droplets >100 mm rapidly rose to the

in an area covering a two mile radius on 14 June 2010, about three surface, based on results from high-pressure laboratory experi-

nautical miles southwest of the DWH spill site (R. Amon pers. ments and model simulations (Paris et al., 2012). The simulations

comm.), suggesting that thalacians (e.g., pyrosome, salp, or doliolid further suggested that the application of dispersants might not

zooplankton) also may have contributed to MOS ﬂux. have played a signiﬁcant role in the partitioning of surface and

subsea oil, in that the amount of oil reaching the surface may have

4. Deep oil plumes only been reduced by 3%. Details on the impacts of droplet size and

pathways for the formation of MOS await further investigations.

After the DWH explosion, persistent subsurface oil plumes Microbial degradation rates of oil and gas hydrocarbons in the

(Fig. 4) were detected by early May and later veriﬁed by chemical deep-water plumes are the subject of debate. Ziervogel and Arnosti

analyses to have occurred primarily between 1000 and 1400 m (2013) observed higher microbial rates of protein and carbohy-

depth (Camilli et al., 2010; Diercks et al., 2010; Spier et al., 2013). drate hydrolysis in the deep oil plume compared to waters outside

Ryerson et al. (2012) estimated that >30% of the hydrocarbon mass the plume, suggesting EPS and oil degradation products enhanced

released may have gone into the deep plumes. The subsurface oil bacterial metabolism in the plume. Hazen et al. (2010) suggested

plumes contained a complex mixture of soluble and insoluble that degradation rate in these deep cold waters (5 C) were

liquid hydrocarbons, including alkanes, monoaromatic hydro- relatively high (turnover rates on order of days) due to several

carbons (e.g., BTEX), PAHs, and gaseous C1–C4 hydrocarbons, factors: (1) the MC252 oil was a light (volatile) crude and thus

including methane, ethane, propane and butane (Spier et al., 2013; more easily degraded, (2) the deep oil plumes included accessible

Reddy et al., 2012). The application of dispersants at the wellhead small oil droplets, and (3) oil from natural seeps in the Gulf of

in deep water was intended to decrease the mean oil droplet size, Mexico maintained an oil-adapted deep-sea microbial community.

which may have decreased the droplet rising velocity and Camilli et al. (2010), however, reported relatively slow rates of

increased the residence time of oil in the water column and hydrocarbon degradation on the order of months. The observed

impacted its transport (Socolofsky et al., 2015). In contrast, high- differences in rate measurements are likely related to variability in

pressure experimental studies of oil droplet size by Aman et al. the temporal and spatial response of the microbial community to

(2015) suggest that the sub-surface plume would have formed oil and Corexit input. Degradation rates also may have been

even without dispersant application. Marine snow particles, which depressed by dispersants (Kleindienst et al., 2015b). Recent topic

formed at the surface and sank to the seaﬂoor, likely interacted reviews suggest that the initial microbial response to the DWH oil

with rising oil droplets and/or the oil plumes at depth (Valentine spill was driven by light hydrocarbons (Valentine et al., 2010) and

et al., 2014). Surface bacteria and phytoplankton-afﬁliated gene that overall the microbial response was rapid and robust (Kimes

sequences were found in sediments at and below the subsurface et al., 2014; King et al., 2015). Although little methane emitted at

plume (Mason et al., 2014; Brooks et al., 2015), substantiating the the wellhead made it to the sea surface (Yvon-Lewis et al., 2011),

notion of transport of surface-formed MOS to depths. MOS likely the timing of methane degradation is controversial (Kessler et al.,

formed in the deep-water plumes as well, as many bacteria were 2011; Joye et al., 2011a,b; Crespo-Medina et al., 2014). In addition,

active in these regions (Hazen et al., 2010; Redmond and Valentine, the rates of hydrocarbon degradation under high-pressure

2012; Dubinsky et al., 2013) and because MOS formed in conditions remain poorly understood (Gutierrez and Aitken,

experiments using bacteria from the deep plume (Baelum et al., 2014; Joye et al., 2014; King et al., 2015), even though pressure

2012; Kleindienst et al., 2015b). affects reaction rates of dissolved gasses (Bowles et al., 2011).

The temporal and spatial dynamics of the deep oil plumes were Metabolic function in some bacterial strains which degrade

complex and variable. A coupled 3-D hydrodynamic and oil particle hydrocarbons were recently shown to be inhibited by pressure

tracking model indicated that local topography and hydrodynamic levels typical of the deep oil plumes (Schedler et al., 2014),

processes, such as eddies, were important in governing the DWH emphasizing that pressure must be considered when evaluating

oil distribution and that use of deep dispersants may have led to a degradation rates in deep water. In contrast, methane oxidation,

deeper vertical distribution of suspended oil (Paris et al., 2012). The which is a ﬁrst order kinetic process, occurs at signiﬁcantly higher

relatively narrow plumes occurred at multiple depths and rates under deep-sea pressures, preventing methane supersatura-

extended both to the southwest and to the northeast of the tion (Bowles et al., 2011). Nonetheless, early concerns raised about

wellhead, with the maximum oil concentrations in the plume the onset of hypoxic conditions as a result of the large methane

generally ﬂowing along the 1200 m isobath. By the time the releases in the deep sea (Joye et al., 2011a,b) were not realized, as

26 K.L. Daly et al. / Anthropocene 13 (2016) 18–33

dissolved oxygen concentrations did not decrease substantially. with river discharge, marine detritus, phytoplankton, microbial,

Instead, the methanotroph community appears to have consumed and petrochemical substances. The relative importance of these

methane relatively rapidly, transforming it into particulate organic materials will vary with distance from rivers and continental

carbon (Redmond and Valentine, 2012; King et al., 2015; Cherrier shelves and water depth. Except for regions inﬂuenced by the

et al., 2014). Overall microbial processing of oil components has Mississippi River Plume, Loop Current, or eddies, offshore areas in

been estimated to account for 40–60% of the discharged hydro- the central Gulf of Mexico typically have lower productivity than

carbons (gas and oil) (Joye, 2015). Because marine snow particles shelf regions and phytoplankton communities are dominated by

are considered hot spots of microbial activity (Azam and Long, small cells, primarily cyanobacteria (Wawrik and Paul, 2004;

2001), with greatly enhanced enzyme activities and degradation Muller-Karger et al., 2015). While Fig. 5 shows a simpliﬁed pattern

rates compared to surrounding seawater (Smith et al., 1992), MOS of onshore to offshore gradients in properties and productivity, the

and OMAs likely contributed to the high microbial degradation off-shelf region of the oil spill in the NE Gulf of Mexico is much

rates of oil in the deep oil plumes. more environmentally complex and generally has higher produc-

tivity than other regions of the Gulf of Mexico (Nababan et al.,

5. Oil accumulation rates and fate at the seaﬂoor 2011). Sedimentation rates coupled to sediment grain-size and

organic content are the major controls on the rates and depths of

Factors affecting the long-term sediment accumulation rates in oxidation–reduction (redox) reactions in sediments (Hastings

the northeast GOM and during the DWH marine snow-oil event are et al., 2015). Redox reactions, in turn, will inﬂuence porewater

shown in Figs. 3–5. The Mississippi River typically dominates chemistry, microbial community structure/function, dissolved and

sediment transport and composition on Mississippi, Louisiana, and solid-phase metal concentrations, degradation rates, and decom-

Texas shelves, as well as the offshore Mississippi Deep-Sea Fan position and transformation of petrochemicals. Furthermore, the

(Balsam and Beeson, 2003). The Apalachicola River to the east on impacts of oil deposition on benthic fauna via smothering, shoaling

the Florida Gulf coast affects sediment transport and composition of the oxic–anoxic boundary, and toxic effects of oil will affect the

too. Fig. 5 illustrates the large gradients of ocean properties driven depth and occurrence of sediment bioturbation and oil and organic

by riverine processes. Sediment deposition from riverine sources is matter degradation rates.

a function of discharge rate, grain size, clay minerology, sediment MOS deposition was observed in bottom sediments within

resuspension, cross-shelf transport, and slumping (Gardner and 256 km of the DWH platform, as an approximately 1 cm-thick

Walsh, 1990; Corbett et al., 2006; Bianchi et al., 2007). River sedimentary layer (Montagna et al., 2013; Mason et al., 2014;

additions of nutrients also fuels marine phytoplankton blooms of Valentine et al., 2014; Brooks et al., 2015). The Brooks et al. (2015)

diatoms (Lohrenz et al.,1997; Dagg and Breed, 2003). Thus, sources study area extended up to 100 nautical miles (185 km) northeast of

of organic matter accumulated on the seaﬂoor include anthropo- the DWH wellhead where thorium inventories of sediment cores

genic and terrestrially-derived biogenic substances associated indicated that the deposition occurred within four to ﬁve months,

Fig. 6. Conceptual model illustrating the complexity of ecosystem response to a disturbance, such as an oil spill. In order to understand the impact and system response,

information is needed at all levels from genes to species, populations, communities, and ecosystems. The green arrows depict ecosystem impacts ﬂowing down to impact

genetic adaptation and red arrows show impacts of genetic variability on changes at the species, population, and community levels. Impacts may vary for different parts of an

ecosystem and can be positive, negative, or no observable change.

K.L. Daly et al. / Anthropocene 13 (2016) 18–33 27

through the summer and fall of 2010. Mass accumulation rates over abundance of microbial genes for hydrocarbon degradation

the past ca. 100 years ranged from 0.05 to 0.16 g/cm /year. In suggested that sediment surface microbes could rapidly deplete

contrast, the 2010 deposition rate was four-fold higher oil in that environment. Ziervogel et al. (2014), however, observed

(0.48–2.40 g/cm /year) compared to rates before 2010 or after only a moderate increase in microbial rates in sediments in

the oil spill during 2011 and 2012. Sedimentation at these sites was response to the MOSSFA event several months (November and

principally due to marine snow, with minor input from the December 2010) after the well-head was capped, leading these

extended Mississippi River discharge (Brooks et al., 2015). authors to hypothesize that this oil may have a long residence time

Petrographic investigations, biomarker analyses, and gene on the seaﬂoor. Furthermore, Hastings et al. (2015) recognized,

sequencing indicated that the amorphous aggregates in sediments through the analysis of redox sensitive metals (e.g., Re and Mn),

were derived mainly from surface-derived diatoms, coccolitho- that the intensity of redox reactions and anaerobic conditions

phores, and cyanobacteria sources, which co-occurred with increased for up to three years after the DWH event, likely a result

pyrogenic PAHs from surface oil burning (Brooks et al., 2015; of excess organic matter and hydrocarbon burial and decomposi-

Romero et al., 2015). In addition, Lincoln et al. (2015) observed tion. These redox changes over time and space were associated

increased carbohydrate concentrations associated with relatively with dramatic shifts in the benthic community composition

large particles in sediments. These authors utilized scanning (Schwing et al., 2015). While the fate of DWH oil on the seaﬂoor

confocal laser microscopy and ﬂuorescently-labeled lectins (that remains uncertain, Soto et al. (2014) reported that during the Ixtoc-

bind to speciﬁc glycoconjugates common in marine exopolysac- I oil spill total hydrocarbon concentrations in sediments had

charides) to show that the labeled carbohydrates occurred as blebs returned to background levels two years after the release of

with distinct drape and stringer morphologies and that their 3 million barrels of oil.

collapsed appearance suggested a water column origin as opposed

to formation in situ by hydrocarbon-degrading bacteria. These 6. Ecosystem effects

microscopy results provide further evidence that the carbohydrate

source was from surface-derived EPS in marine snow. It is uncertain to what extent the MOSSFA event impacted Gulf

The amount and distribution of DWH oil in sediments was of Mexico ecosystems. The MOSSA Workshop participants devel-

estimated by Chanton et al. (2015) to be 0.5–9% of the total oil oped a conceptual model (Fig. 6) to convey the complexity of an

from the wellhead, using radiocarbon distributions. Their results ecosystem response to a perturbation and the need for information

indicated that oil was deposited within the upper 1 cm of the on all levels: genes, organisms, populations, communities, and

sediments over an area of 8400 km , mostly to the southwest and ecosystem, for both water column and seaﬂoor habitats. All levels

as far as 190 km to the southwest of the wellhead (Chanton are connected through food web and environmental processes,

unpubl.). Valentine et al. (2014), using hopane as a tracer, with impacts transmitted from genes up to ecosystem scales and

reported that 1.8–14% of the oil from DWH was in the upper 1 cm vice versa with ecosystems impacting changes in populations and

of sediments over an area of 3200 km around the wellhead. DWH ultimately genetic adaptation. Connectivity through currents with

PAH concentrations in sediment cores from the same sites unimpacted regions is an important factor in recovery following

reported in Brooks et al. (2015) were signiﬁcantly elevated during severe disturbances in marine systems. However, ecosystem

2010 (up to two orders of magnitude greater than background), response to disturbances and long-term changes may involve

À1

ranging from 70 to 524 ng g and diagnostic markers were threshold effects and non-linear dynamics (Folke et al., 2004).

consistent with a MC252 oil origin (Romero et al., 2015). The PAHs Thus, the complexity of these interactions at all temporal and

appeared to be a mix of petrogenic and pyrogenic (burn-derived) spatial scales makes it difﬁcult to assess the impacts of

material. In addition, these authors point out that the deep oil disturbances, such as the DWH oil spill and MOSSFA, on marine

plumes likely impinged on the continental slope and acted as ecosystems.

another mechanism for oil deposition on the seaﬂoor. Mason et al. Baseline data, which are essential for assessing the impacts of

(2014) evaluated 64 sediment cores collected primarily south- disturbances, unfortunately, are not available for most components

southwest of the DWH site and observed the highest PAH of the food web in the NE Gulf of Mexico. Bernhardt and Leslie

À1

concentrations (19,258 ng g ) within ﬁve km of the wellhead and (2013) recommend obtaining time-series data for the underlying

À1

the lowest concentrations (18 ng g ) further away. Valentine ecological components of food webs that are important for

et al. (2014) tabulated hopane concentrations for 534 locations, resilience, i.e., population size, species diversity, and functional

noting that the highest concentrations occurred within 40 km of groups. Information also is needed on response patterns to MOS

the wellhead, primarily to the southwest. These authors argued sedimentation for key species, such as those that are ecologically or

that there is a mismatch between the location of the surface oil economically important. Ecologically important species should

slick and where oil was observed on the seaﬂoor, implying that include those that are representative of speciﬁc habitats, or

surface oil was not the primary source of the seaﬂoor oil. Instead, foundation species, at all depths of the water column and in the

they suggested that the majority of the oil stemmed from the benthos. Laboratory mesocosm studies would provide information

deep plume, rather than from the surface layer, based on the for the many species that were not adequately studied during the

composition of oil residues at the seaﬂoor. In addition, Kolian DWH spill. Furthermore, laboratory studies would permit data

et al. (2015) reported continued deposition of oil near the collection on lethal and sublethal exposure and impacts to

wellhead and in coastal waters of Mississippi, suggesting that the different ﬂux rates of MOS and concentrations of oil and

wellhead may have continued to leak until at least May 2012. dispersants.

Thus, a number of different processes may have contributed over Several studies have shown that MOSSFA due to the oil spill

different time and space scales resulting in the heterogeneous impacted the marine ecosystem (Fisher et al., 2014; Schwing

distribution of oil on the seaﬂoor. et al., 2015). Direct and indirect impacts of MOS may have

Oil deposition in these deep-sea sediments resulted in occurred through ingestion, microbial activity, smothering,

enhanced microbial response and an intensiﬁcation of redox suboxic and anoxic conditions, transfer through the marine food

reactions and anaerobic conditions relative to unoiled sediments web, and immunotoxicity through gills and transdermal exposure

(Mason et al., 2014; Hastings et al., 2015; King et al., 2015). Both and/or bioaccumulation. Bioaccumulation of hydrocarbons

aerobic and anaerobic processes were detected in surface sedi- through the planktonic food web would increase exposure of

ments, with shifting community compositions. The relatively high higher trophic-level organisms (Meador, 2003). Zooplankton

28 K.L. Daly et al. / Anthropocene 13 (2016) 18–33

ingested oil droplets directly (Lee et al., 2012; Almeda et al., year later there was evidence of recovery at some, but not all sites

2014c) or may have ingested oil-containing marine snow, as many including the site 111 km away. This is consistent with the

zooplankton are known to feed on marine snow (Alldredge and protracted and increasing intensity of sediment redox conditions

Silver, 1988). Typically 70–90% of marine snow particles sinking for up to three years after MOSSFA (Hastings et al., 2015). In

from surface waters are ingested (repackaged) or fragmented by addition, deep-water coral communities were impacted.

mesopelagic zooplankton or remineralized by bacteria (Guidi Oil-containing ﬂocculent material was observed on 90% of the

et al., 2008). It is not known what percent of the sinking MOS was corals within 6 km of the wellhead with less impact on

deposited on the seaﬂoor or the fate of the mesopelagic communities up to 22 km to the southwest (White et al., 2012;

community during and after the oil spill. Carbon and nitrogen Fisher et al., 2014). Corals that were covered with brown

stable isotope analyses and natural abundance radiocarbon ﬂocculent material (MOS) showed evidence of stress (e.g., excess

analysis have indicated that oil entered particulate organic mucus production, sclerite enlargement, tissue loss) and mortali-

carbon and the planktonic food web in surface waters (Graham ty (DeLeo et al., 2015). Shallow water mesophotic corals at the

et al., 2010; Chanton et al., 2012; Mitra et al., 2012; Cherrier et al., Pinnacles Reef offshore of Alabama were impacted as well, with

2014; Fernandez et al. in review) and mesopelagic ﬁsh and shrimp corals having bare skeletons and broken or missing branches

in deep water (>600 m) likely through trophic transfer (Sam- (Silva et al., 2015). Coral branches that were exposed to higher

marco et al., 2013; Quintana-Rizzo et al., 2015). Pelagic ﬁsh that concentrations of settling MOS have not recovered to date

swim with their mouths open to maintain a continuous current of (Hsing et al., 2013). Prouty et al. (2014) reported that corals had

water across their gills (e.g., scombrid ﬁshes; Klinger et al., 2015) incorporated oil carbon up to 30 km from the spill site. Experi-

could experience increased oil exposure from suspended or ments using toxicological assays of coral fragments demonstrated

sinking MOS. There is evidence that coastal macrofauna ingested that all three coral species tested exhibited more severe health

petrocarbon as well (Sammarco et al., 2013; Wilson et al., 2015). decline (e.g., polyp retraction, mucous discharge, exposed

The mesopelagic community primarily feeds on zooplankton and skeleton, mortality) when exposed to dispersant and oil-

vertically migrates into the upper 200 m at night, so they may dispersant mixtures than to oil alone (DeLeo et al., 2015). Since

have encountered subsurface oil plumes and food sources these corals are very slow growing and may live >600 years, they

enriched in oil both at depth and at the surface. In turn, surface are highly vulnerable to disturbance and may be very slow to

and mesopelagic ﬁsh are eaten by higher trophic animals, such as recover (Prouty et al., 2014). Some ﬁsh and sharks use deep corals

tuna, seabirds, and dolphins. An unusual mortality event has been as spawning grounds; thus, impacts to corals could lead to larger

reported for bottlenose dolphins (Tursiops truncatus) in coastal ecosystem impacts.

waters of Louisiana, Mississippi, and Alabama starting in 2010 and Sedimentation of MOS also impacted bottom dwelling ﬁsh. An

continuing into 2014 (Venn-Watson et al., 2015). This is the longest assessment of offshore ﬁshes between 2011 and 2012 revealed red

marine mammal die-off in recorded history of the Gulf of Mexico. snapper (Lutjanus campechanus), king snake eel (Ophichthus rex),

Although the majority of strandings are bottlenose dolphins, and golden tileﬁsh (Lopholatilus chamaeleonticeps) had elevated

spinner dolphins (Stenella longirostris), Atlantic spotted dolphins PAH and metabolite concentrations, with a composition similar to

(Stenella frontalis), and melon-headed whales (Peponocephala that from the DWH oil (Murawski et al., 2014; Snyder et al., 2015).

electra) also have stranded. While the factors contributing to Elevated PAHs were detected in ﬁsh bile, but not in muscle tissue,

the high mortalities are still being investigated, dolphins in at sites near the wellhead and extending to the west Florida shelf.

Barrataria Bay, Louisiana have exhibited moderate to severe lung Skin lesions were present on up to 9% of the ﬁsh. Although skin

disease and evidence of hypoadrenocorticism since 2010 consis- lesions may be a short-term consequence of acute PAH contami-

tent with immunotoxic effects of oil. nation, PAH exposure may result in a variety of immunotoxicity

The large sedimentation of MOS clearly had a negative impact population-level effects, including impaired growth, increased

on benthic organisms, including injuries, mortality, and changes disease susceptibility, reduced larval survival, and reduced net

in community composition. The Gulf of Mexico has a high benthic population fecundity. Red snapper and king snake eels showed

species diversity, with maximum diversity on the mid to upper signs of recovery during 2012 and 2013, while golden tileﬁsh,

continental slope between 1200 and 1600 m depth (Wei et al., which burrows into sediments and likely had a longer exposure to

2010), which coincides with the depth of the DWH well site. PAHs, still had elevated biliary PAH metabolites during 2013

Montagna et al. (2013) and Baguley et al. (2015) reported on the (Snyder et al., 2015). The recovery of the deep-sea ecosystem is

results of benthic fauna sampled at 170 stations after the oil spill, uncertain given the spatial complexity of the sedimentation event

of which 68 stations were located 0.5–125 km from the wellhead. and lower biodegradation rates of oil in sediments (Mason et al.,

These authors observed a severe to moderate impact on benthic 2014; Ziervogel et al., 2014).

meiofauna, with the highest impact within 3 km of the wellhead

and a moderate impact within 60 km to the southwest. 7. Proposed framework for MOSSFA investigations and data

Community changes in severely impacted areas included an gaps

increase in nematode worms (an indicator of organic pollution), a

decline in harpacticoid copepod abundance, and low meiofauna MOSSFA Workshop participants created a conceptual diagram

and macrofauna diversity compared to unimpacted sites. Overall, (Fig. 4) to (1) better deﬁne the processes that impact MOS

copepods had the largest population decline (10-fold), followed formation and sedimentation from the point of the deep-water oil

by polychaete worms, ostracods, and kinorhynchs. The dramatic discharge to MOS sedimentation on the seaﬂoor, (2) identify

increase in nematode abundance could be due to organic signiﬁcant research questions, (3) determine the space and time

enrichment from sinking MOS and/or a higher tolerance to scales of processes and events, and (4) identify data gaps that may

hydrocarbons. Moreover, Schwing et al. (2015) determined that be important for further deﬁning and modeling of MOSSFA

there was an 80–93% decline in benthic foraminifera following events. Examples of data gaps and questions relating to the

the oil spill up to 111 km from the wellhead, likely due to suboxic MOSSFA processes are provided below to help guide future

conditions (Hastings et al., 2015). Using principal component research. The MOSSFA Workshop Report (2014) provides a more

analysis, Schwing et al. (2015) strongly suggested that oil comprehensive list of questions and discussion of data gaps. The

exposure coupled to the onset of suboxic-anoxic conditions in letter-designated sections below correspond to topics illustrated

the sediments were the factors controlling foraminifera decline. A in Fig. 4.

K.L. Daly et al. / Anthropocene 13 (2016) 18–33 29

7.1. Physical and chemical characteristics of oil droplets and associated 7.3.3. New sources of material at the surface (C3)

hydrates (A) Oil was burned at the surface and pyrogenic particles were

observed in the sediments. The role of aerosols and burning oil

The characteristics of oil released at a point source are by-products in MOS formation and sedimentation, however, are

determined by the type of oil released, water temperature, water unknown. Did Saharan dust input interact with the sea surface

depth (ambient pressure), and the pressure within the petroleum microlayer to inﬂuence MOS formation? What was the role of soot

reservoir. Laboratory experiments and models analyses of oil (i.e., charred combustion products of burning oil) in particle

droplet size distributions are required over a range of conditions formation and sedimentation?

(pressure, turbulence) to predict the fate of bubbles of gas hydrates

and oil droplets as they rise to the surface. During the DWH oil spill,

7.3.4. Sinking of oil-derived material from the surface (C4)

chemical dispersants were applied directly to the deep subsea oil

Increasing the density of marine snow was key to forming

jet to promote smaller oil droplet size and longer residence time in

sinking particles. Although the general physical and biological

the water column. The consequences of this action need further

investigation. factors contributing to MOS formation and sedimentation are

known, there is little information on the composition of MOS

particles and the factors controlling its spatial and temporal

7.2. Formation of subsurface oil plumes: droplet and bubble size (B)

variation and sinking rates. Lithogenic deposition was evident in a

sediment trap deployed ﬁve km SW of the DWH site and on the

Deep horizontal intrusions of dissolved gas and oil formed at

seaﬂoor shortly after the oil spill. However, the role of OMAs

mid-water depths, which impacted the mesopelagic environment,

(mineral ballast) in oil sedimentation and whether OMAs

sedimentation of oil, and sediments where plumes impinged on

aggregated with MOS particles over the broad area of the oil spill

the continental shelf and slope. In addition, MOS particles may

is not known.

have formed in the plumes and marine snow particles that formed

at the surface may have entrained additional oil as they sank

through the plumes. Many questions remain relating to the

7.4. Processes impacting MOS during sedimentation (D)

characteristics of oil in the plumes, the role of the physical

environment in plume formation and spatial extent, the plume’s

Microbial activity, turbulent disruption, and zooplankton

role in the MOSSFA event, and an evaluation of the conditions

fragmentation transform sinking aggregates. Currents laterally

under which subsurface plumes may form during future oil well

advect sinking particles. There is evidence that a subsurface

blowouts.

nepheloid layer occurred off the shelf slope during the oil spill. It is

not known how surface-formed sinking particles interacted with

7.3. Important processes in the surface mixed layer (C)

suspended sediment layers and/or the deep subsurface oil plumes,

or to what extent particles were laterally advected. Clay

All surface ocean processes that impacted MOS formation and

mineralogy, the size range of clay particles, and oil emulsions

sedimentation varied spatially and temporally. Atmosphere-ocean

likely controlled whether oil droplet/particles are buoyant or sink,

interactions and submesoscale physical processes inﬂuenced the

as clay particles may stabilize emulsiﬁed droplets (Sullivan and

spatial distribution of oil, marine biota, and MOS. Winds and

Kilpatrick, 2002). The extent to which sinking aggregates

current shear spread the surface oil slick. Breaking waves disperse

scavenged organisms, organic detritus, inorganic particles, and

oil into the water column resulting in oil droplets of different sizes.

other oil droplets is uncertain.

The impacts of large storms are unknown. Continued model

development is needed to better understand the role of physical

processes in oil dispersion and MOS aggregation and sedimenta- 7.5. Processes impacting MOS on the seaﬂoor (E)

tion, as well as the recovery (replacement via advection) of the

marine food web. Although it is clear that a signiﬁcant percentage of DWH oil

sedimented to the sea ﬂoor, an accurate assessment of the amount

of oil and its spatial distribution remain to be determined. The

7.3.1. Interaction of oil droplets with euphotic zone plankton (C1)

dominant factors controlling the persistence and degradation of

Oil that rose to the surface encountered high concentrations of

hydrocarbons in sediments needs further investigation. What are

phytoplankton fueled by nutrients from river discharge. Dis-

the roles of microbial communities, redox interactions, and

persants also were applied at the surface. Laboratory experiments

sediment oxygen demand in the degradation of hydrocarbons?

demonstrated that MOS particles were formed by interactions of

In particular, long-term studies are needed to determine microbial

oil with bacteria, phytoplankton, and zooplankton. Did the oil

rates of hydrocarbon degradation over time and to assess the

spill contribute to the observed enhanced phytoplankton bloom?

recovery rate of benthic communities.

How did variation in oil and dispersant concentrations change

microbial mucus formation and zooplankton behavior and

survival?

7.6. Processes impacting resuspension of oiled sediments (F)

7.3.2. Transformation of oil ﬂoating at the atmosphere-ocean interface

The role of water motion in resuspension, disaggregation, and

(C2)

re-aggregation of oiled sediments in benthic boundary layers is

UV light acts to weather oil and evaporation of more volatile

poorly known. What is the role of storm-generated deep currents

constituents acts to change oil composition and density over time.

in resuspending oiled sediments? How do these processes impact

Both evaporation and emulsiﬁcation increases the density and

benthic communities? There is little information on the role of

viscosity of the surface slick. Why does weathered oil enhance

natural oil seeps in accumulation and re-suspension of oiled

MOS aggregation in experiments? Microbial activity was shown to

sediments. Are marine snow particles produced near natural

create large ﬂocs early during the oil spill. Why did this phenomena seeps?

change over time? How did dispersants impact MOS formation?

30 K.L. Daly et al. / Anthropocene 13 (2016) 18–33

8. Conclusions Acknowledgements

The DWH MOSSFA event was unexpected, but now recognized The MOSSFA workshop was supported by a grant from the Gulf

to be a signiﬁcant pathway for the distribution and fate of oil. The of Mexico Research Initiative. Research support was provided by

contribution to sedimentation and interactions between MOS and the University of South Florida Division of Sponsored Research and

OMA particles will vary with distance from shore and river water Florida Institute of Oceanography (FIO)/BP to Daly, and grants from

plumes. Evidence suggests that the prolonged DWH sedimentation the Gulf of Mexico Research Initiative through its consortia: Center

event may have been comprised of numerous smaller sedimenta- for Integrated Modeling and Analysis of Gulf Ecosystems

tion events during and after the spill, with the overall accumula- (C-IMAGE) to Daly, Hollander, and Chanton, Deep-C to Chanton

tion at the seaﬂoor of as much as 14% of the total oil released, and Hollander, and Ecosystem Impacts of Oil & Gas Inputs to the

thereby relocating oil to mesopelagic and deep benthic ecosys- Gulf (ECOGIG) to Passow and Chanton. We thank the workshop

tems. Clearly, understanding the impact of MOS processes on the participants (http://deep-c.org/mossfa/) for their signiﬁcant con-

transport and fate of oil spilled into the environment is important tributions to the workshop discussions. We are especially grateful

and should be considered for future oil spill assessments. to Dr. Nancy Kinner for facilitating the workshop and Dr. Peter

Consequences of the MOSSFA event include the fact that MOS Kinner for organizing and editing the ﬁnal report. Meredith Fields

particles in surface waters and aggregates sinking through the and Kathy Mandsager provided excellent logistical support. A.

water column were remineralized by bacteria and/or ingested by Remsen and K. Kramer provided analyses of marine snow. We also

zooplankton. Assimilation of petrocarbon into food web biomass thank the reviewers for thoughtful comments and suggestions.

would be a more favorable pathway for marine food webs than Data are publically available through the Gulf of Mexico Research

bioaccumulation of oil in organisms, which negatively impact Initiative Information and Data Cooperative (GRIIDC) at http://

higher trophic levels. In addition, the accumulation of DWH oil on data.gulfresearchinitiative.org (doi: 10.7266/N78P5XFP, http://dx.

the seaﬂoor may have a relatively long residence time, with doi.org/10.7266/N76T0JKS).

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