Plastic microfibre ingestion by deep-sea organisms

Abstract

Plastic waste is a distinctive indicator of the world-wide impact of anthropogenic activities. Both macro- and micro-plastics are found in the ocean, but as yet little is known about their ultimate fate and their impact on marine ecosystems. In this study we present the first evidence that microplastics are already becoming integrated into deep-water organisms. By examining organisms that live on the deep-sea floor we show that plastic microfibres are ingested and internalised by members of at least three major phyla with different feeding mechanisms. These results demonstrate that, despite its remote location, the deep sea and its fragile habitats are already being exposed to human waste to the extent that diverse organisms are ingesting microplastics.

Full text

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Scientific RepoRts | 6:33997 | DOI: 10.1038/srep33997
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Plastic microbre ingestion by
deep-sea organisms
M. L. Taylor1, C. Gwinnett2, L. F. Robinson3 & L. C. Woodall1,4
Plastic waste is a distinctive indicator of the world-wide impact of anthropogenic activities. Both macro-
and micro-plastics are found in the ocean, but as yet little is known about their ultimate fate and their
impact on marine ecosystems. In this study we present the rst evidence that microplastics are already
becoming integrated into deep-water organisms. By examining organisms that live on the deep-sea
oor we show that plastic microbres are ingested and internalised by members of at least three major
phyla with dierent feeding mechanisms. These results demonstrate that, despite its remote location,
the deep sea and its fragile habitats are already being exposed to human waste to the extent that
diverse organisms are ingesting microplastics.
ere appears to be no environment on Earth that has escaped plastic pollution. Indeed, despite the distance from
land, plastics are ubiquitous in remote marine environments, including polar regions1,2. ese plastics are known
to cause impacts to terrestrial and marine ecosystems both at the macro- and micro-scale. For example, ingestion
of plastic debris or entanglement has been recorded in 44–50% of all seabirds3, sea snakes, sea turtles (all species),
penguins, seals, sea lions, manatees, sea otters, sh, crustaceans and half of all marine mammals3–5. Ingestion can
block the digestive tract, damage stomach lining and lessen feeding, all leading to starvation (reviewed in ref. 4).
Of growing concern are microplastics (typically dened as < 5 mm6). e large surface area-to-volume ratio of
microplastics, compared to macroplastics, means they concentrate persistent organic pollutants which can be
up to six orders of magnitude more contaminated than ambient seawater7 and absorb metals8,9. e subsequent
transfer of such pollutants and additives from microplastics to marine organisms has been conrmed under
experimental conditions6,10,11. However, the ecological eects on marine organisms in the wild is understudied
and not yet conclusive12.
It has already been shown that microplastics are ingested by large pelagic marine organisms such as
lter-feeding salps13, tuna14, and whales15,16. However, only a few observations have demonstrated that microplas-
tics are being ingested in natural settings by benthic organisms, mostly in shallow coastal waters. ese obser-
vations include organisms with dierent feeding strategies. Organisms such as the detritivorous and predatory
lobster17,18 and shrimp19 presumably consume microplastic passively with prey (or in the prey itself) and/or
sediment. Deposit-feeding lugworms20 likely consume microplastic that are within sediment, and suspension/
lter-feeding mussels likely take in plastics that are suspended in sea water20. In a natural setting microplas-
tics have been found in the stomach21,22, oral23 and ventilation areas22,24 of shallow-water organisms; and on the
outer surface of deep water octocoral25. Laboratory studies suggest that benthic and invertebrate taxa, including
corals23, copepods21, zooplankton26, crabs24,27, molluscs6, sea cucumbers28, scallops29, barnacles30, oyster31, lug-
worms and polychaetes10,32 will ingest microplastics if they are introduced under experimental conditions. e
eects across this range of organisms included reductions in fecundity21, lower feeding rates26, enhanced suscep-
tibility to oxidative stress, reduced ability to remove pathogenic bacteria10, reduced feeding activities27,33, reduced
energy reserves and balance27,32, and decreased lysome stability22. e results of these studies are not yet conclu-
sive, but the sum of existing laboratory experiments, most of which use microbeads and not microbres, high-
light the detrimental eects of microplastics in a broad range of benthic taxa and the importance of considering
organism biology e.g. low metabolism27, feeding method33 and behaviour.
e ultimate fate of microplastics that reach the deep-sea realm is also not as well studied as in shallow waters.
Recently, microplastics have been identied in the deep and abyssal oceans25,34,35, the largest marine habitat on
the planet. ese studies suggested that deep-sea microplastics are already being found in similar concentrations
as intertidal and shallow sub-tidal sediments25. e rate of accumulation of microplastics in the deep sea has not
1Department of Zoology, University of Oxford, Tinbergen Building, South Parks Road, Oxford OX1 3PS, UK.
2Department of Forensic and Crime Science, Staordshire University, Stoke-On-Trent ST4 2DF, UK. 3School of Earth
Sciences, University of Bristol, Bristol, BS8 1RJ, UK. 4Department of Life Sciences, Natural History Museum, London
SW7 5BD, UK. Correspondence and requests for materials should be addressed to M.L.T. (email: michelle.taylor@
zoo.ox.ac.uk)
Received: 13 May 2016
Accepted: 01 September 2016
Published: 30 September 2016
OPEN

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been researched, neither has impacts on deep-sea organisms. However, given the ever-increasing plastic load
reaching our oceans36, and that a large portion of plastics will likely eventually end up on or buried in the seaoor,
the potential is there for an unseen pervasive impact on deep-marine ecosystems.
As yet, there have been no studies to establish whether organisms of the deep sea will ingest microplastics or
what the impacts may be. Indeed, impact studies will be even more challenging in the deep sea than for shallow
marine organisms given the logistical constraints of studying life hundreds to thousands of metres beneath the
waves. Here we use specimens collected from two deep submergence research cruises to two dierent ocean
basins to show for the rst time that deep-sea organisms from at least three dierent phyla are ingesting and /or
internalising plastic microbres.
Results
All microplastics found in this study were microbres (e.g. Fig.1c,d), not microbeads. All bres (15) were of
dierent classes and were constructed from 1 of 5 dierent materials (modied acrylic, polypropylene, viscose,
polyester, and acrylic). is variability between samples provides evidence that there was limited or no contami-
nation as there was no consistency in microbres across expedition or organism. In a wider study of microbres
from the deep-sea37 just 2 of the 52 classes of plastics found in samples were found in contamination monitoring
eorts; this minimal overlap makes it unlikely, given the same protocols were followed, that the microbres from
within organisms presented here are the results of contamination. In addition, following Woodall et al.37 clean
room protocols, monitoring of potential laboratory contamination using dampened lter papers indicated that
there were no synthetic bres contaminating the laboratory used for dissection.
Plastic microbres were found on and inside six of the nine organisms examined (Table1), including exam-
ples of taxa from the phyla Cnidaria, Echinodermata and Arthropoda. Specically microbres were found inside
either oral areas (seapen tentacles and upper mesentry, JC094-3717, Figs1a and 2a–c), feeding apparatus (hermit
crab maxilliped, see Fig.2f,g; JC066-702), symbiotic zoanthid tentacles (zoanthid on hermit crab, JC066-702,
Figs1b and 2g), gill (squat lobster, JC094-771) or stomach areas (sea cucumber, JC094-212, Fig.2h). Similar to24,
one of the Crustacea studied (squat lobster, JC094-771) had microbres in the gut and in the ventilation/gill areas.
Microbres were not found inside zoanthids that were covering a bamboo coral skeleton (Fig.2d,e; JC094-767)
but were found externally. No microbres were found in or associated with the anemone, armoured sea cucumber
or other octocoral investigated.
Discussion
Microbres inside deep-sea organisms were found from 334–1783 m depth in the equitorial mid-Atlantic and
954–1062 m in the SW Indian Ocean (Fig.3). Previous studies have found microbres in sediments down to
2000 m in the subpolar North Atlantic, 2200 m in the NE Atlantic, 3500 m in the Mediterranean and 5768 m in the
West Pacic35. Most deep-sea organisms rely either directly or indirectly on the supply of organic detritus from
the euphotic zone, oen called ‘marine snow’. Our conrmation of biological integration of microplastics makes
recent evidence of a shi towards smaller plastic size categories, equivalent to the ‘marine snow’ size38, something
now particularly relevant for deep-sea organisms.
In the few instances where they have been studied in deep sea sediments, microplastics occur in similar con-
centrations as in inter-tidal and shallow sub-tidal sediments25. Enders, et al.39 recently modelled microplastic
distribution to 250 m depth but there is no raw data from deep-sea water columns on the High Seas. We assume
that microplastics in sediment represent a vertical accumulation from falling ‘marine snow’25. We observed that
the suspension-feeding anemone, armoured sea cucumber and octocoral had no microbre load, although bres
were found inside the suspension-feeding sea pen and zoanthid from the SW Indian Ocean (Table1, Fig.3). By
contrast bres were found in all predatory, deposit and detritivore feeders examined. If this general observation
(albeit based on very few samples), of lter-feeders having lower microplastic loads, holds true more widely, the
implication is that deposit-feeding organisms may be more vulnerable to microplastic ingestion than suspension
feeders. Of course, load depends on a wide range of factors, such as an animal’s ability to avoid microplastic inges-
tion, any size or shape-selection of food particles etc. and the abundance and density of microplastics found in an
organism’s environment. Knowledge of background microplastic load, systematic surveys with multiple replicates
of sediment, seawater collections and sampling of deep-sea organisms across a range of feeding strategies would
be required to test if feeding strategy alone impacts organism vulnerability to microplastic ingestion.
Despite microbres being the majority of microplastic pollution40,41, including in the deep-sea25,35, most feed-
ing experiments that have been undertaken thus far use microbeads and plastic shavings, with a few exceptions,
Hämer, et al.42, Watts, et al.27, Au, et al.43. Our study shows for the rst time that deep-sea organisms are ingesting
microbres in a natural setting, thus we suggest that experimental designs using bres are needed to determine
the potential long-term impact of microplastics for both shallow and deep marine organisms.
e range of plastic microbres found ingested/internalised by organisms studied here included modied
acrylic, polypropylene, viscose, polyester, and acrylic. Polypropylene has been found to adsorb PCBs (polychlo-
rinated biphenyls), nonylphenol and DDE, an organochlorine pesticide7. Polyethylene, a type of polyolen bre
whose chemical composition in part is the basis of some polyester bres (e.g. polyethylene terephthalate), has
been found to adsorb four times more PCBs than polypropylene44. Polypropylene has also been found to adsorb
a range of metals in a marine environment; the concentrations of most of these metals did not saturate over a
year period suggesting plastics in the oceans for long time periods accumulate greater concentrations of metals9.
Chemical contamination experiments are rare in the marine environment, and oen present unrealistic
experimental scenarios45. Yet with the chemical ingredients in 50% of plastics listed as hazardous (United Nations’
Globally Harmonized System of Classication and Labelling of Chemicals) such issues maybe just the start of

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long-term ecological and health problems associated with waste plastics in the environment46; impacts that have
not been looked at in many marine animals6,10,11 and no deep-sea animals as yet.
Of course, ingestion, and any subsequent biological impacts, depend on many factors32 including characteristics
of the microplastics themselves, such as size, shape, density, abundance (as seen in shallow water sea cucumbers28),
colour, and importantly, dierential adsorption of harmful substances7, as well as organism physiology, ecology
Figure 1. Images of specimens in situ (a,b) and close-up images of microplastic bres exhibiting their interference
colours (used to aide classication) under cross-polarised illumination (c) and under plain polarised light (d); (a)
sea pen, JC066-3717; (b) hermit crab with zoanthid symbionts, JC066-702; (c) polyester microbre, JC066-702-09;
(d) acrylic microbre, JC066-702-10. Images (a,b) taken by MLT. Images (c,d) taken by CG.

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and behaviour; this also includes whether microplastics accumulate in the organism, feeding method and/or
prey of organisms, and where microplastics accumulate, or are egested and/or translocate within the organism.
A nal factor is whether transfer of the microplastic up the food chain is a possibility. All of these facets of the
microplastic biological impact problem are relevant to deep-sea organisms however as science knows less about
deep-sea biology and ecology (as there are fewer experimental opportunities in this challenging environment)
these aspects of marine pollution will be relatively dicult to pursue.
Shallow-water experiments have found microplastic bioaccumulation e.g. lobster17, mussel and oyster47. Given
that our data are a snapshot of the bres within six organisms we cannot determine whether microbres are
bioaccumulating. Five microbres was the most found within one organism (the hermit crab, JC066-702) and not
in a ball as was seen in the lobster Nephrops17 and crab, Carcinus maenas27. is could suggest that microplastics
are transient within the organisms studied. Or, this could be indicative of low densities of microplastics in the
deep-sea feeding areas of organisms studied here, or that microbres have dierent residency times to other more
intensively studied microplastics (e.g. microbeads), or that the organisms here have dierent gut residency times
to other organisms studied. It may also be that certain feeding strategies convey less suspectibility to microplastic
bioaccummulation. Given the low number of organisms it was possible to sample here, and without concurrent
environmental sampling, the link between background microplastic densities and microplastic abundance within
organisms is not possible to establish.
Conclusions
Studied organisms have a range of feeding mechanisms, from suspension feeding (sea pens, zoanthids, anemo-
nes, barnacles, armoured sea cucumbers) to deposit feeders (sea cucumbers), detritivores and predators (hermit
crabs, squat lobsters). Given the breadth of feeding strategies found in deep-sea organisms and their reliance
Sample ID Organism ID Phylum Organism Loca lity Depth (m) Fibre ID Material Class§
JC094-201 Anemone Cnidaria Equatorial mid-Atlantic 836 None N/A N/A
JC094-224 Armoured
holothurian (sea
cucumber) Echinodermata Equatorial mid-Atlantic 671 None N/A N/A
JC066-3155 Octocoral -
Anthomastus Cnidaria SW Indian Ocean 562 None N/A N/A
JC094-212 Holothurian (sea
cucumber) Echinodermata Equatorial mid-Atlantic 334
212-1 Natural
212-2 Modied Acrylic 1
212-3 Natural
212-4 Cotton
212-5 Cotton
212-6 Polyprop¶1
JC094-771 Squat Lobster Arthropoda Equatorial mid-Atlantic 611
771-1 Natural
771-2 Viscose 1
771-3 Cotton
771-4 Polyester 4
771-5 Viscose 2
771-6 Natural
*JC094-767 Zoanthid on
bamboo coral Cnidaria Equatorial mid-Atlantic 1783
767-1 Viscose 4
767-2 Natural
767-3 Natural
JC066-3717 Sea pen (octocoral) Cnidaria SW Indian Ocean 954
3717-1 Viscose 3
3717-2 Natural
3717-3 Natural
3717-4 Polyester 1
JC066-702 Hermit Crab Arthropoda SW Indian Ocean 1062
702-1 Acrylic 1
702-2 Synthetic (nylon or
polyethylene) 1
702-3 Natural
702-4 Natural
702-5 Natural
702-6 Polyester 2
702-7 Polyprop¶2
702-8 Acrylic 2
JC066-702 Zoanthid Cnidaria SW Indian Ocean 1062 702-9 Modied acrylic 2
702-10 Polyester 3
Table 1. Organisms examined for microplastics. *Fibres found on exterior of organism. §Fibre classes
dierentiated as in ref. 37 (Table S1). ¶polyprop is an abbreviation of polypropylene.

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on ‘marine snow’ (which is the same size fraction as microplastics), and evidence of ingestion in shallow-water
counterparts, there is a high likelihood of microplastic ingestion across a wider range of taxa than presented here.
However, without the context of environmental sampling of microplastics (water and sediment) or investigations
into the impacts of the chemicals ingested, it is not easy to understand the impact microplastic presence will have
Figure 2. Organisms found to have ingested microbres and microbres in situ; (a) blue microbre from
mouth area of sea pen polyp (b) sea pen, JC066-3717; (c) example sea pen polyp; (d) black mirobre embedded
in surface of zoanthid; (e) zoanthids on bamboo coral skeleton, JC094-767; (f) blue microbre on feeding
maxilliped of hermit crab; (g) hermit crab, JC066-702, with symbiotic zoanthid; (h) sea cucumber, JC094-212.
Images taken by MLT.

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Figure 3. Microplastic presence by material and depth, (a) mid-Atlantic data from JC094; (b) SW Indian
Ocean data from JC066; (c) depth of all other known deep-sea microbres found in sediments represented by
grey bars.
Figure 4. Map showing all known deep-sea microbre collection locations (sediment cores from25,
unpublished sediment core results from JC094, West Pacic microbres from35, specimens – white circles
- are from this study). Labels refer to specimen codes of organisms (see Table1). Map made with ArcGIS
v.10.3.1. http://desktop.arcgis.com/en/arcmap/.

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on biology, and subsequently ecology, of deep-sea organisms. Broadly, the important individual organism eects
of microplastic ingestion are being investigated (albeit mostly with microbeads rather than the more commonly
found microbres) but, given the ubiquity of microplastics in our marine environments, research should start
considering population and ecosystem level eects48 such as dierential age/cohort survival causing demographic
shis, food/prey shis, hazard to human foods, taxa specic vulnerability etc; this is a dicult task in any marine
environment, most especially the deep-sea, regardless it is still an important challenge to undertake.
Materials and Methods
e organisms were collected using the manipulator arm and suction hose of a remotely operated vehicle (ROV)
on expeditions on the R.R.S. James Cook in the SW Indian Ocean (JC066 in 2011) and equatorial mid-Atlantic
(JC094 in 2013) (Fig.4). At the same time core-top sediment samples were collected and microplastics were also
found in those sediments25.
Historically, collections of deep-sea organisms have been made using dredging/trawling equipment, so that
the exact locations of sample collection were unknown. Dredge sampling also causes organisms to be in a highly
disturbed condition on recovery at the sea surface and trawls are oen made of plastic bres precluding the study
of plastic contamination. By using ROVs the exact location and habitat is known, as the collections are made
using a suction hose or manipulator arm and deposited into sample containers (bioboxes – made of plastic but
not of the type and colour found). ese sampling methods limit the potential for contamination by surrounding
sediments and reduce trauma, maintaining the structural integrity of organisms. ere is potential for contami-
nation when ascending to the surface in bioboxes as they have some seawater through ow. However this type of
contamination (and feeding during ascent) is unlikely and should result in microbres of similar compositions
being found on the external surfaces of the organisms37, which was not observed. Preservation uid (70–80%
ethanol) was not ltered for microplastics however some organisms were dead (caused by the pressure and tem-
perature change when moving from deep to shallow water) when preserved i.e. not feeding and no organisms
were observed feeding once on ship.
Laboratory fibre contamination was minimised through a stringent set of protocols based upon known
and accepted procedures used in forensic laboratories that examine bres evidence49. All on-shore work was
undertaken in a sealed room (with door covered by 100% cotton muslin cloth) where only natural bre clothing
and non-plastic equipment (metal and glass) were utilised; the room had been cleaned and was monitored for
microplastics. Clean dampened lter paper was used to sample for any microbres present in the room during
specimen dissection (see Woodall, et al.37 for full laboratory procedures). No synthetic bres were found on the
lters in any part of the study.
Stomach, mouth, all internal cavities and breathing organs (gills and ventilation cavities) were dissected
from nine deep-sea organisms and examined under a binocular microscope to identify whether or not they had
ingested or internalised microplastics (Table1). Material was placed into glass petri dishes that had been cleaned
using 0.22 μ m membrane ltered Millipore water (as was all equipment). Only the dish under the microscope
was open to the air and nearby dampened lters were monitored post-dissection to check for contamination.
All plastic bres were picked up using a metal entomological pin, and placed into Millipore water contained in
a small, clean, glass vial which was immediately sealed. ese anti-contamination procedures have proven to
eectively minimise bre contamination and, although complete removal of bres from an environment is not
possible, the amount remaining is minimal, can be monitored, and is acceptable for the exacting standards of the
criminal justice system50. Microbres were classied using a Nikon polarised light microscope. is method is
commonly used in forensic science and other polymer sciences and has proven benets for the fast and eective
identication of bres. is method is described in Woodall et al.37.
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Acknowledgements
We would like to thank the scientists and crew of JC066 and JC094 for their assistance, specically the ROV Isis
team, whose hard work resulted in the collection of the organisms studied here. We would also like to thank Joe
Walsh for his unpublished sediment data from JC094. JC066 was funded by NERC grant NE/F005504/1: Benthic
Biodiversity of Seamounts in the Southwest Indian Ocean, and cruise JC094 ERC grant 278705. MT was funded
by the International Union for the Conservation of Nature.

www.nature.com/scientificreports/
9
Scientific RepoRts | 6:33997 | DOI: 10.1038/srep33997
Author Contributions
M.L.T. and L.C.W. conceived the idea and undertook the research. C.G. undertook chemical analysis. L.F.R.
provided samples and, along with all authors, developed and wrote the manuscript.
Additional Information
Competing nancial interests: e authors declare no competing nancial interests.
How to cite this article: Taylor, M. L. et al. Plastic microbre ingestion by deep-sea organisms. Sci. Rep. 6,
33997; doi: 10.1038/srep33997 (2016).
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