ArticlePDF Available

Abstract and Figures

Small plastic detritus, termed 'microplastics', are a widespread and ubiquitous contaminant of marine ecosystems across the globe. Ingestion of microplastics by marine biota, including mussels, worms, fish and seabirds, has been widely reported, but despite their vital ecological role in marine food-webs, the impact of microplastics on zooplankton remains under-researched. Here, we show that microplastics are ingested by, and may impact upon, zooplankton. We used bio-imaging techniques to document ingestion, egestion and adherence of microplastics in a range of zooplankton common to the northeast Atlantic, and employed feeding rate studies to determine the impact of plastic detritus on algal ingestion rates in copepods. Using fluorescence and coherent anti-Stokes Raman scattering (CARS) microscopy we identified that thirteen zooplankton taxa had the capacity to ingest 1.7 - 30.6 µm polystyrene beads, with uptake varying by taxa, life-stage and bead-size. Post-ingestion, copepods egested faecal pellets laden with microplastics. We further observed microplastics adhered to the external carapace and appendages of exposed zooplankton. Exposure of the copepod Centropages typicus to natural assemblages of algae with and without microplastics showed that 7.3 µm microplastics (>4000 ml-1) significantly decreased algal feeding. Our findings imply that marine microplastic debris can negatively impact upon zooplankton function and health.
Content may be subject to copyright.
Microplastic Ingestion by Zooplankton
Matthew Cole,
,,
*Pennie Lindeque,
Elaine Fileman,
Claudia Halsband,
Rhys Goodhead,
§
Julian Moger,
§
and Tamara S. Galloway
Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth PL1 3DH, United Kingdom
Akvaplan-niva AS, FRAM High North Research Centre for Climate and the Environment, N-9296 Tromsø, Norway
§
College of Engineering, Mathematics and Physical Sciences: Physics, Physics Building, University of Exeter, Stocker Road, Exeter
EX4 4QL, United Kingdom
College of Life and Environmental Sciences: Biosciences, Georey Pope Building, University of Exeter, Stocker Road, Exeter EX4
4QD, United Kingdom
ABSTRACT: Small plastic detritus, termed microplastics,
are a widespread and ubiquitous contaminant of marine
ecosystems across the globe. Ingestion of microplastics by
marine biota, including mussels, worms, sh, and seabirds, has
been widely reported, but despite their vital ecological role in
marine food-webs, the impact of microplastics on zooplankton
remains under-researched. Here, we show that microplastics
are ingested by, and may impact upon, zooplankton. We used
bioimaging techniques to document ingestion, egestion, and
adherence of microplastics in a range of zooplankton common
to the northeast Atlantic, and employed feeding rate studies to
determine the impact of plastic detritus on algal ingestion rates
in copepods. Using uorescence and coherent anti-Stokes
Raman scattering (CARS) microscopy we identied that
thirteen zooplankton taxa had the capacity to ingest 1.730.6 μm polystyrene beads, with uptake varying by taxa, life-stage and
bead-size. Post-ingestion, copepods egested faecal pellets laden with microplastics. We further observed microplastics adhered to
the external carapace and appendages of exposed zooplankton. Exposure of the copepod Centropages typicus to natural
assemblages of algae with and without microplastics showed that 7.3 μm microplastics (>4000 mL1) signicantly decreased algal
feeding. Our ndings imply that marine microplastic debris can negatively impact upon zooplankton function and health.
1. INTRODUCTION
It has been estimated that up to 10% of plastics produced
globally enters our oceans, so it is of little surprise that plastic
debris is now a pervasive and resilient pollutant of the marine
environment.
1,2
Larger plastic debris, such as monolament
line, plastic strapping, and plastic bags, can entangle, garrotte,
drown, or be eaten by an array of marine wildlife.
3
There is
compelling evidence that microplasticssmall plastic <5 mm
in diameteralso negatively impact upon marine biota.
4
Microplastics consist of synthetic polymer products manufac-
tured to be of a small size, such as exfoliates in cosmetics,
5
and
those items derived from the fragmentation of larger plastic
debris, for example polyester bers from fabrics,
6
polyethylene
fragments from plastic bags
7
and polystyrene particles from
buoys and oats.
8
Typically, high-density plastics (e.g.,
polyvinyl chlorides, polyester) settle out of the water column,
whereas low-density plastics (e.g., polyethylene, polystyrene)
remain buoyant, although freshwater inputs, storms, and
biolm formation may result in vertical mixing.
9,10
Floating
plastic debris is susceptible to local and ocean currents resulting
in higher-than-average waterborne microplastic concentrations
in areas of conuence.
11
Microplastics are of environmental concern as their small size
makes them available to a wide range of marine biota.
12
Microplastic ingestion has been demonstrated in marine
organisms, including amphipods, lugworms, and barnacles,
4
mussels,
13
decapod crustaceans,
14
seabirds,
15
and sh.
16,17
Ingested microplastics might obstruct feeding appendages,
aggregate, and block the alimentary canal, limit the food intake
of an organism or be translocated into the circulatory
system.
13,14
Further, microplastics may introduce toxicants to
the organism: rst, additives incorporated into a plastic during
manufacture to improve its properties (e.g., phthalates for
malleability and polybrominated diphenyl ethers (PDE) for
heat resistance) might leach out of weathered plastic debris;
18,19
second, the large surface area to volume ratio and hydrophobic
properties of microplastics leave them susceptible to the
accumulation of hydrophobic organic contaminants (HOCs)
which could dissociate post-ingestion.
20
Received: February 12, 2013
Revised: May 16, 2013
Accepted: May 21, 2013
Article
pubs.acs.org/est
© XXXX American Chemical Society Adx.doi.org/10.1021/es400663f |Environ. Sci. Technol. XXXX, XXX, XXXXXX
The extent to which microplastics are ingested and can
impact upon zooplankton is uncertain. Zooplankton have a vital
ecological role in marine ecosystems, both as primary
consumers in the marine food web, and in the case of
meroplankton, consisting of the juvenile life stage of numerous
commercially important species. The widespread presence of
small plastic debris in the water column makes interactions
between zooplankton and microplastics highly likely; indeed,
both small plastic debris and zooplankton >333 μm in diameter
have been recurrently sampled together in sea surface trawls
and by continuous plankton recorders.
4,11,21,22
Zooplankton
display a range of feeding modes, which vary by life-stage,
species and prey availability.
23
Zooplankton can use a
combination of chemo- and mechano-receptors to select prey,
and their ability to preferentially feed on one species of algae
over other algae, plastic beads or detritus has been
demonstrated.
2426
Laboratory experiments, in which latex
beads were used to model algal ingestion, have shown that
zooplankton have the potential to ingest small plastics.
2628
Uptake of these small plastics likely results from indiscriminate
feeding modes (e.g., lter-feeding), by which prey with
equivalent spherical diameters (ESD) <100 μm are non-
selectively fed upon.
23,29
Due to the complexities of sampling and extracting
microplastics from the marine environment, existing studies
have largely focused on detritus >333 μm.
1,30
However, there is
evidence of very small microplastics (<100 μm) both in the
benthos and water column. Sampling of shoreline, estuarine
and harbor sediments has shown the presence of 20 μm
diameter brous polymers,
4,6,31
and microplastic bers,
granules, lms, and polystyrene spheres ranging in size from
38 μm to 1 mm.
32
In the water column, sampling with a 80 μm
mesh in Swedish coastal waters captured 100 000 times greater
concentrations of microplastics than when using a 450 μm
mesh, with a maximal concentration of 102 000 microplastics
per m3sampled near a polyethylene production facility.
33
Sampling of microplastics in this size range is exceptional, as
such there is currently insucient data to determine realistic
environmental concentrations of these particles.
Here, we investigate the ingestion of minute microplastics,
31 μm diameter, by a range of zooplankton species, and
examine their impact on zooplankton function and feeding. To
explore the hypothesis that zooplankton are capable of
ingesting microplastics, 15 zooplankton taxarepresentative
of abundant mesozooplankton in northeast Atlantic coastal
systemswere exposed to polystyrene spheres in the size range
7.330.6 μm suspended in natural seawater, then analyzed
using uorescence microscopy. Using the copepod Temora
longicornis,weexploredwhere0.43.8 μmmicroplastics
accumulate, both internally and externally, using a novel
bioimaging technique: coherent anti-Stokes Raman scattering
(CARS) microscopy. Finally, to test the hypothesis that
microplastics negatively impact upon zooplankton feeding, we
exposed the copepod Centropages typicus to natural assemblages
of algae and polystyrene beads, using uorometry and ow
cytometry to quantify algal ingestion.
2. MATERIALS AND METHODS
2.1. Zooplankton Sampling. Zooplankton sampling was
conducted between November 2011 and October 2012 at
Station L4 (50°15N, 4°13W), a coastal site located in the
western English Channel 12 km south of Plymouth, UK.
34,35
A
200 μm mesh was used to collect zooplankton via horizontal
surface tows and vertical hauls. Collected zooplankton were
held in 2 L of seawater within a coolbox, and transported to
controlled-temperature facilities at Plymouth Marine Labo-
ratory (Plymouth, UK). For all experimental procedures, we
maintained the zooplankton at ambient sea-surface temper-
atures (ranging 1017 °C depending on sampling date).
Specimens were hand-selected under a dissecting microscope
within two hours of sampling, and then collectively held in 2 L
of ltered seawater (0.22 μm Millipore lter) for 24 h to allow
full gut depuration. In all, fourteen mesozooplankton taxa (size:
0.220 mm), representative of the most commonly occurring
zooplankton in the western English Channel and covering a
range of life-stages and life-strategies, in addition to cultured
Oxyrrhis marina, a heterotrophic dinoagellate (size: 1530
μm), were selected for microplastic ingestion studies (Table 1).
2.2. Natural Seawater Preparation. For the algal
ingestion studies, natural seawater (5 L) was collected from
the sea surface at station L4, passed through a 200 μm mesh
into a polycarbonate carboy and returned to the laboratory
within 2 h. The seawater was further screened with a 100 μm
mesh to ensure the removal of any grazing micrometazoans
then stored in the dark for 24 h at ambient sea-surface
temperature to maintain the natural communities of algae at
normal concentrations. Prior to experimental work, the
seawater was mixed thoroughly by gentle inversion of the
water in the carboy.
2.3. Microplastics. Exposures used commercial polystyrene
spheres (SPHERO Spherotech). With global production rates
of 10.6 million tons in 2001, polystyrene is the fourth most
commonly produced polymer in the world and its presence as a
constituent of marine debris is commonly reported.
30,36
The
bead sizes used in each experiment (0.430.6 μm) were
selected to be comparable with the prey size range of the
zooplankton exposed.
23,37
2.4. Microplastic Ingestion by Zooplankton. To
ascertain whether zooplankton ingest microplastics we
conducted exposures using uorescent polystyrene beads, and
used microscopy to assess uptake. Microplastic suspensions
were made up by pipetting 20 μL of 7.3, 20.6, or 30.6 μm
diameter uorescently labeled (yellow uorescence: 400500
nm excitation, 450550 nm emission) polystyrene spheres into
glass vials containing 20 mL of ltered seawater (0.1% v/v:
3000 beads mL1(7.3 μm); 2240 beads mL1(20.6 μm); 635
beads mL1(30.6 μm)), then mixed through repeated
inversion. With larger zooplankton (e.g., copepods, decapod
larvae, chaetognaths), individual specimens were added directly
to the vial (n=6 per exposure), and tted to a rotating
plankton wheel (<5 rpm) for 24 h. For smaller zooplankton or
those with low survivability in the laboratory (e.g., bivalve
larvae, gelatinous holoplankton, O. marina), individual speci-
mens were exposed to microplastic suspensions in Petridishes
(n=6 per exposure) at ambient sea temperature for 1 h (with
the exception of bivalve larvae which were exposed for 24 h
using this method). Post-exposure, zooplankton were washed
with ltered seawater and transferred to Eppendorf tubes
containing 1 mL of 4% formalin . Ingestion was ascertained by
viewing specimens at ×40400 magnication with an Olympus
IMT2 inverted light microscope with uorescence to determine
the presence of polystyrene beads (uorescing yellow-green)
within the alimentary canal or body cavity of the zooplankton.
To better understand the interactions between zooplankton
and microplastics, both live and preserved copepods and select
zooplankton specimens were viewed under the microscope for
Environmental Science & Technology Article
dx.doi.org/10.1021/es400663f |Environ. Sci. Technol. XXXX, XXX, XXXXXXB
varying lengths of time to observe the feeding process,
ingestion, gut passage, and egestion of polystyrene beads.
2.5. Interactions between Microplastics and Cope-
pods. To explore the internal distribution and external
adherence of microplastics in zooplankton, we rst exposed
the copepod Temora longicornis to polystyrene beads and then
employed CARS microscopy (see below) to visualize their
uptake. Microplastic suspensions were formulated by adding 12
μL of 0.4, 1.7, or 3.8 μm diameter non-labeled polystyrene
spheres to 24 mL of ltered seawater (0.05% v/v: 1 ×106beads
mL1(0.4 μm), 380 ×103beads mL1(1.7 μm), and 40 ×103
beads mL1(3.8 μm)), which were mixed through inversion
and sonication. Individual T. longicornis (n=6 per exposure)
were added to each vial, rotated at <5 rpm at ambient sea
temperature for 24 h. Post-exposure, specimens were poured
onto a 200 μm mesh suspended in ltered seawater (to prevent
damage to the copepods), washed gently, preserved in 4%
formalin and then transferred to the bioimaging suite at the
University of Exeter (Exeter, UK).
2.6. Coherent Anti-Stokes Raman Scattering (CARS)
Microscopy. CARS microscopy is a novel microscopy
technique that provides label-free contrast, based on vibrational
spectroscopy
38
which has exceptional capability for locating
polymer particles within biological tissues with subcellular
precision.
39,40
CARS imaging was performed using a custom-
built microscopy system based on a commercial confocal laser-
scanning microscope and a synchronized dual-wavelength
picosecond laser source. Laser excitation was provided by an
optical parametric oscillator (OPO) (Levante Emerald, APE,
Berlin) pumped with a frequency doubled Nd:vandium
picosecond oscillator (High-Q Laser Production GmbH).
The pump laser generated a 6 ps, 76 MHz pulse train at 532
nm with adjustable output power up to 10 W. The OPO
produced collinear signal and idler beams with perfect temporal
overlap and provided continuous tuning over a range of
wavelengths. The signal beam was used as the pump, ranging
from 670 to 980 nm and fundamental of Nd:vandium (1064
nm) used as the Stokes beam. The maximum combined output
power of the pump and Stokes was approximately 1 W, which
was attenuated to reduce the power at the sample to between
15 and 30 mW. To improve the transmission of the near-IR
excitation through the commercial microscope (IX71 and
FV300, Olympus UK) the galvanometer mirrors were replaced
with silver mirrors and the tube lens was replaced with a MgF2
coated lens. The collinear pump and Stokes beams were
directed onto the scanning confocal dichroic which was
replaced by a silver mirror with high reectivity throughout
the visible and NIR (21010, Chroma Technologies, Bellows
Falls, VT ). The forward-CARS signal was collected by the air
condenser, transmitted by the dichroic mirror and directed
onto a red-sensitive photomultiplier tube (R3896, Hamamatsu
Photonic UK). The epi-CARS signal was collected using the
objective lens and separated from the pump and Stokes beams
by a long-wave pass dichroic mirror (z850rdc-xr, Chroma
Technologies) and directed onto a second R3896 photo-
multiplier tube at the rear microscope port. The CARS signal
was isolated at each photodetector using a single band-pass
lters centered at the anti-Stokes wavelengths. Imaging was
performed using either a 60×water immersion, or 20×air
objective (UPlanS Apo, Olympus UK).
2.7. Impact of Microplastics on Copepod Feeding. To
determine whether microplastics negatively impact upon a
copepods ability to ingest natural prey, we exposed the
copepod Centropages typicus to natural assemblages of algae
with and without microplastics, and compared algal ingestion
Table 1. Capacity for a Range of Zooplankton to Ingest
Microplastics, Demonstrated Using Fluorescent
Microscopy
a
organism taxonomy microplastic
ESD (μm)
exposure
duration
(h) ingestion
(Y/P/N?)
Holoplankton (Copepods)
Acartia clausi Copepoda
(Calanoida) 7.3 24 yes
Acartia clausi Copepoda
(Calanoida) 20.6 24 no
Acartia clausi Copepoda
(Calanoida) 30.6 24 partial
Calanus
helgolandicus
Copepoda
(Calanoida) 7.3 24 yes
Calanus
helgolandicus
Copepoda
(Calanoida) 20.6 24 yes
Calanus
helgolandicus
(juv.)
Copepoda
(Calanoida) 20.6 24 yes
Calanus
helgolandicus
Copepoda
(Calanoida) 30.6 24 partial
Centropages
typicus
Copepoda
(Calanoida) 7.3 24 yes
Centropages
typicus
Copepoda
(Calanoida) 20.6 24 yes
Centropages
typicus
Copepoda
(Calanoida) 30.6 24 yes
Temora
longicornis
Copepoda
(Calanoida) 7.3 24 yes
Temora
longicornis
Copepoda
(Calanoida) 20.6 24 yes
Temora
longicornis
Copepoda
(Calanoida) 30.6 24 yes
Holoplankton (Other)
Doliolidae Tunicata 7.3 1 yes
Euphausiidae Euphausiacea 20.6 24 yes
Parasagitta sp. Chaetognatha 20.6 1 no
Parasagitta sp. Chaetognatha 30.6 24 no
Obelia sp. Cnidaria
(Hydrozoa) 20.6 1 partial
Siphonophorae Cnidaria
(Hydrozoa) 20.6 1 no
Meroplankton
Bivalvia (larvae) Mollusca 7.3 24 yes
Brachyura
(megalopa) Decapoda 20.6 24 yes
Brachyura
(zoea) Decapoda 20.6 24 no
Caridea (larvae) Decapoda 20.6 24 yes
Paguridae
(larvae) Decapoda 20.6 24 partial
Porcellanidae
(zoea) Decapoda 30.6 24 partial
Microzooplankton
Oxyrrhis marina Dinoagellata 7.3 1 yes
a
Microplastic uptake is based upon the number of individuals in a
treatment (n=6) that contained beads in their alimentary canals or
body cavity following 1 or 24 h exposures to either 7.3, 20.6, or 30.6
μmuorescent polystyrene beads. ESD = equivalent spherical
diameter. Scoring system: yes (>50%); partial (<50%); no (0%).
Environmental Science & Technology Article
dx.doi.org/10.1021/es400663f |Environ. Sci. Technol. XXXX, XXX, XXXXXXC
rates between treatments. In our initial experiment, designed to
identify the size of microplastic that would have the greatest
impact on C. typicus feeding, we exposed individual C. typicus
specimens (n=6 per exposure) to 23 mL of natural seawater
containing 0 or 23 μL of 7.3 or 20.6 μmuorescent polystyrene
beads (0.1% v/v), rotated at <5 rpm for 24 h. To quantify algal
concentrations within the natural seawater pre- and post-
exposure, we vacuum ltered the exposure media through a
glass ber lter, and then transferred the lter to 7 mL of
acetone, held at 4 °C in the dark for 24 h. The chlorophyll
levels within the acetone solution were measured using a
Turner uorometer. Since 7.3 μm microplastics had the most
notable impact on C. typicus feeding, we conducted a further
experiment to establish a doseresponse relationship between
microplastic concentration and food uptake. Microplastic
suspensions consisted of 0, 2.5, 5, 10, or 20 μL additions of
Figure 1. Microplastics of dierent sizes can be ingested, egested and adhere to a range of zooplankton, as visualized using uorescence microscopy:
(i) the copepod Centropages typicus containing 7.3 μm polystyrene (PS) beads (dorsal view); (ii) the copepod Calanus helgolandicus containing 20.6
μm PS beads (lateral view); (iii) a D-stage bivalve larvae containing 7.3 μm PS beads (dorsal view); (iv) a Brachyuran (decapod) larvae (zoea stage)
containing 20.6 μm PS beads (lateral view); (v) a Porcellanid (decapod) larvae, containing 30.6 μm PS beads (lateral view); (vi) 30.6 μm PS beads
in the posterior-gut of the copepod Temora longicornis during egestion, (vii) 1.4 μm PS beads trapped between the lamental hairs of the furca of C.
typicus; (viii) a T. longicornis faecal pellet containing 30.6 μm PS beads; (ix) proportion of copepods (Acartia clausi,Calanus helgolandicus,Centropages
typicus, and Temora longicornis) with microplastics in their guts following 24 h of exposure to 7.4, 20.6, and 30.6 μm polystyrene beads. *denotes
statistically signicant (P0.05) lower consumption of larger beads compared with that of 7.3 μm beads. Scale bar (gray line): 100 μm.
Environmental Science & Technology Article
dx.doi.org/10.1021/es400663f |Environ. Sci. Technol. XXXX, XXX, XXXXXXD
7.3 μmuorescent polystyrene beads in 23 mL of natural
seawater. A 1.8 mL aliquot of natural seawater was taken from
all vials at T0and xed with 40 μL of 50% glutaraldehyde (4%
nal concentration), inverted for 2 min, refrigerated at 4 °C for
30 min and subsequently snap-frozen in liquid nitrogen and
stored in a 80 °C freezer prior to analysis using analytical ow
cytometry. Individual C. typicus (n=6 per exposure) were
added to experimental vials, while controls (with no copepod)
were set up to determine natural growth or decline of algae
over the exposure period. The vials were incubated on a
rotating plankton wheel (5 rpm) for 24 h in the dark. Post-
exposure (T24), a further 1.8 mL aliquot was xed (as with T0).
Flow cytometric analysis was carried out on thawed natural
seawater samples using a BD Accuri C6 ow cytometer.
41
Particle abundance data was subsequently used to calculate the
ingestion rates of algae by C. typicus.
42
2.8. Statistical Analysis. Data was analyzed using Micro-
soft Excel. Studentsttests were used to compare experimental
data with controls, with signicant dierence attributed where P
0.05. Regression analysis was used to analyze the correlation
between algal ingestion rates and microplastic concentration.
3. RESULTS
3.1. Microplastic Ingestion by Zooplankton. The
majority of zooplankton (13 of 15) exposed to polystyrene
beads (7.330.6 μm) demonstrated the capacity to ingest
microplastics (Table 1). Organisms exhibiting uptake included
copepods (Figure 1i, ii), bivalve larvae (Figure 1iii) and
decapod larvae (Figure 1iv, v). Only two specimens
chaetognaths (Parasagitta sp.) and siphonophorae (Cnida-
ria)showed no evidence of ingestion. All four species of
copepods examined demonstrated some anity for ingesting
microplastics, with Centropages typicus and Temora longicornis
able to consume 7.3, 20.6, and 30.6 μm polystyrene beads
(Figure 1ix). The other copepods showed evidence of size-
based selectivity: Acartia clausi ingested 7.3 μm beads but
ingested signicantly fewer 20.6 and 30.6 μm beads, and
Calanus helgolandicus showed signicantly less anity for 30.6
μm beads than for 7.3 μm beads. The decapod Brachyurans
demonstrated variability in microplastic ingestion depending
upon life-stage: brachyuran zoea showed no anity for 20.6 μm
beads, while the more developed brachyuran megalopa readily
ingested such beads. Obelia sp., Paguridae larvae and
Porcellinidae (zoea) exhibited individual variability in their
ability to ingest polystyrene beads, with less than half the
Figure 2. Coherent anti-Stokes Raman scattering (CARS) microscopy: (i) Spontaneous [black] and stimulated [grey] peaks for polystyrene beads,
Raman shifts of 2845 cm1(CH) and 3050 cm1(aromatic CH) were used to visualize the polystyrene; (ii) 3.4 μm microplastics accumulated in
the alimentary canal [ac] of the copepod Temora longicornis (yellow dots); beads further adhered to the exterior of the copepods urosome [u], furca
[f] and posterior swimming legs [sl] (blue dots); (ii) 3.4 μm microplastics (red dots) adhered to the external surface of the posterior swimming legs
of T. longicornis. Scale bar [gray line]: 50 μm.
Environmental Science & Technology Article
dx.doi.org/10.1021/es400663f |Environ. Sci. Technol. XXXX, XXX, XXXXXXE
exposed specimens in a cohort showing evidence of micro-
plastic uptake.
Live observations of copepods, euphausids, and doliolids
found microplastics were ingested via lter-feeding. In
copepods and euphausids, this process relied upon the rapid
movement of the swimming legs and external appendages,
which generated a feeding current that indiscriminately drew
surrounding beads toward the organism. With doliolids, we
observed the microplastics being drawn through the anterior
siphon into their body cavity, where the polystyrene beads were
entrapped and drawn toward the gut. Oxyrrhis marina, a single
celled heterotrophic dinoagellate, demonstrated a more direct
method of ingestion, locating particles with their agella and
then engulng the polystyrene beads. Post-ingestion, copepods
typically aggregated beads within the anterior midgut, shifted
them to the posterior midgut via peristaltic action (Figure 1i, ii)
and egested them within densely packed faecal pellets (Figure
1vi, viii). Typically, microplastic-laden faecal pellets were
egested within hours. In the absence of food, individual
microplastic beads could remain in the intestinal tract of C.
helgolandicus for up to 7 days (data not shown). During
observations of both live and preserved zooplankton specimens,
including copepods, decapod larvae and euphausids, micro-
plastics often adhered to the specimensexternal surfaces. In
copepods that died during the exposure period, polystyrene
beads would coat the carapace in vast numbers; similarly, beads
were observed to cling to the shed carapace of a molting C.
helgolandicus copepodite. In live specimens, microplastics were
found to concentrate between the external appendages of
copepods, including the swimming legs, feeding apparatus,
antennae, and furca (Figure 1vii).
3.2. Interactions between Microplastics and Cope-
pods. CARS microscopy used a blend of transmitted light to
capture the structure of the copepod, and Raman shifts of 2845
cm1(CH) and 3050 cm1(aromatic CH) to visualize the
polystyrene (Figure 2i). Temora longicornis ingested both 1.7
and 3.8 μm polystyrene beads; use of Z-stackingin which 2D
images at incremental focal plains are layered together to form a
Figure 3. Exposure to increasing concentrations of microplastics in the copepod Centropages typicus (n=5). Treatments comprise seawater
containing natural assemblages of algae [A] with 4000 [B], 7000 [C], 11 000 [D], and 25 000 [E] 7.3 μm polystyrene beads per mL. *denotes
statistically signicant (P0.05) lower ingestion rates (cells individual1hour1) than in controls. Graphs show ingestion rates of (i) Synechococcus
sp.; (ii) Picoeukaroytes; (iii) all algae present; (iv) plot comparing positive C. typicus algal ingestion rates at diering microplastics concentrations
logarithmic regression: R2= 0.70 (P0.05).
Environmental Science & Technology Article
dx.doi.org/10.1021/es400663f |Environ. Sci. Technol. XXXX, XXX, XXXXXXF
3D imageconrmed that microplastics clumping in the
posterior midgut were, indeed, internalized (Figure 2ii; yellow
dots), but sucient resolution to identify microplastic trans-
location was not possible. CARS imaging conrmed that
microplastics adhere to the external appendages of the
zooplankton: polystyrene beads (0.43.8 μm) accumulated
between the lamental hairs on appendages, including the furca
(Figure 2iii; blue dots), rear swimming legs (Figure 2iii; red
dots) and antennules, and between the segments of the
carapace, particularly around the urosome and swimming legs.
3.3. Impact of Microplastics on Copepod Feeding.
Using chlorophyll concentration as a proxy for algal abundance,
we identied that 7.3 μm microplastics had a signicant impact
on algal ingestion by the copepod Centropages typicus (data not
shown) and identied a signicant doseresponse relationship
between ingestion rates and the concentration of 7.3 μm
polystyrene beads. Exposed to seawatercontaining natural
assemblages of algaeC. typicus ingested 12 Synechococcus sp.
ind1h1(Figure 3i) and 24 picoeukaryotes ind1h1(Figure
3ii). These ingestion rates decreased when additionally exposed
to 4000 microplastics mL1; this decrease was statistically
signicant at concentrations of 7000 microplastics mL1(t
test: P0.05). When considering all of the <20 μm ESD algal
groups identied using ow cytometry Synechococcus sp.,
picoeukaryotes, nanoeukaryotes, and cryptophytes,in
combination (hereafter referred to as total algae), C. typicus
presented total algal ingestion rates of 34 algae ind1h1in
the absence of microplastics. Total algal ingestion rates for C.
typicus were signicantly reduced with the addition of 4000
microplastics mL1(ttest: P0.05; Figure 3iii). Furthermore,
we identied a strong, logarithmic relationship (R2= 0.70, P
0.05) between the ingestion rate of total algae and microplastic
concentration (Figure 3iv).
4. DISCUSSION
Our results show that a range of zooplankton common to the
northeast Atlantic can ingest microplastics (1.430.6 μm
diameter), with capacity for uptake varying between species,
life-stage, and microplastic size. Microplastics were indiscrim-
inately ingested via lter-feeding and later egested in faecal
pellets, typically within a matter of hours. Microplastics
accumulated on the external surface of dead zooplankton, and
were found trapped between the external appendages of live
copepods. We visualized 1.7 and 3.8 μm polystyrene beads
clustered within the alimentary canal and aggregated between
the setae and joints of external appendages. Lastly, we
demonstrated that the presence of 7.3 μm polystyrene beads
could signicantly reduce the algal ingestion rate of the
copepod Centropages typicus, in a doseresponse relationship.
We demonstrated that 13 zooplankton taxaincluding
holoplankton, meroplankton, and microzooplanktonhave
the capacity to ingest polystyrene beads in the absence of
natural food. All four copepod species showed uptake of
microplastics, with varying degrees of selectivity: T. longicornis
and C. typicus ingested 7.3, 20.6, and 30.6 μm beads, whereas A.
clausi and C. helgolandicus fed on 7.3 μm beads but less
frequently ingested larger beads. Using CARS microscopy, we
further identied that T. longicornis could ingest 1.7 and 3.8 μm
microplastics; however, we found no evidence of 0.4 μm beads
being ingested. Brachyuran larvae only ingested 20.6 μm
polystyrene beads as megalopa (postzoea larvae), with no
uptake observed when in the earlier zoea stage. Microplastics
were also ingested by the lter-feeding euphausids and
doliolids, and Oxyrrhis marina, a heterotrophic dinoagellete
that ingests motile or immotile prey through engulfment via a
non-permanent cytosome.
43
These ndings corroborate the
results of several previous studies, which documented the
uptake of <100 μm microplastics by Acartia tonsa,
28
Calanus
pacificus adults, copepodites and nauplii,
26,44,45
Oxyrrhis
marina,
46
ciliates,
47,48
echinoderm larvae
27
and salps.
49
We did not observe microplastic uptake in Parasagitta sp.
(chaetognaths) following 1 or 24 hour exposures to 30.6 μm
beads, or siphonophorae (Cnidaria) exposed to 20.6 μm
plastics, possibly as a result of handling stress, or more likely
because these zooplankton are raptorial predators and feed
actively, so were not enticed to capture the immotile
microplastics.
37
Furthermore, only 1050% of Obelia sp.,
Paguridae larvae and Porcellinidae (zoea) specimens presented
with polystyrene beads in their intestinal tracts post-exposure.
As we also observed size-selective ingestion in A. clausi and C.
helgolandicus, it is important to consider how microplastics may
impact on dierent zooplankton feeding strategies. Zooplank-
ton use both mechanoreception (i.e., detection of pressure
disturbances within the water) and chemoreception (i.e.,
detection of infochemicals emitted by algal cells) to sense
prey.
29,37
As such, the clean immotile beads used in our algal-
free experiments are less likely to be detected by exposed
zooplankton, although it is possible that aged microplastics, that
have developed biolms during their residence within the
marine environment,
10
may generate a chemosensory response;
this eect was observed in the copepod Eurytemora aff inis
which more readily ingested beads spiked with bacteria than
when oered beads alone.
50
While some copepods will
continuously lter-feed regardless of prey availability, others
(e.g., C. pacificus,A. tonsa) can limit their movement and lter-
feed at reduced rates to conserve energy when faced with low
food concentrations.
51,52
The presence of algae promotes
greater uptake of microplastics in the lter-feeding copepods
Calanus pacificus
26
and Eucalanus pileatus CV copepodites;
53
notably, A. clausi only ingests 16 μm polystyrene beads in the
presence of algae.
24
Some zooplankton can ingest or reject prey
upon capture, depending on surface characteristics and charge
of the particle, both echinoderm larvae and the copepods A.
clausi and E. pileatus can reject plastic beads that coalesced
within their mouthparts.
27,53,54
The presence of microplastics
may also alter the behavior of zooplankton, limiting their
capacity to feed; in Acartia tonsa copepodites, contact with 45
μm plastic beads caused the organisms to jump, limiting time
dedicated to feeding bouts and reducing their clearance rates by
60%.
55
Post-ingestion, polystyrene beads were observed to coalesce
within the midgut of copepods prior to egestion. While gut-
retention times of these microplastics were typically similar to
natural food items (i.e., egestion occurred within hours), a
follow-up experiment found some Calanus helgolandicus
individuals retained microplastics for up to 7 days. Micro-
plastics found in the marine environment include bers,
granules, and fragments manufactured from a range of
polymers;
30
if such irregularly shaped and brous microplastics
were ingested, they may become entangled within the intestinal
tract, potentially resulting in a nonbiodegradable gut-blockage
and greater gut-retention times. Plastic bers entangle within
the intestinal tracts of Nephrops in this manner,
14
wheras
sh
16,17
and seabird dissections
15
have demonstrated that
marine wildlife can retain a range of plastic detritus within their
stomachs near-indenitely. Prolonged gut-retention times of
Environmental Science & Technology Article
dx.doi.org/10.1021/es400663f |Environ. Sci. Technol. XXXX, XXX, XXXXXXG
plastics and gut-blockages in zooplankton may limit the ability
of these organisms to ingest and digest food, and may pose a
toxic risk. During manufacture, a suite of additives (e.g.,
plasticisers, ame-retardants, antimicrobials) are added to
plastics, and large surface area to volume ratio and hydrophobic
properties of microplastics make them particularly susceptible
to the adherence of waterborne contaminants (e.g., PCBs,
DDT, and PAHs).
19
The leaching of additives and disassoci-
ation of toxic contaminants post-ingestion has been modeled in
polychaete worms
56
and demonstrated in streaked shear-
waters.
57
In zooplankton, as with other marine biota, these
contaminants might be considered endocrine-disruptors,
carcinogenic, or toxic, with repercussions for growth, sexual
development, fecundity, morbidity, and mortality.
58,59
Of
further concern is trophic-transfer: microplastics (and con-
taminants released from microplastics) within lower-trophic,
keystone organisms such as zooplankton may result in the
trophic-transfer of these contaminants up the food-chain, with
the potential for bioaccumulation and therefore adverse health
consequences in higher trophic organisms.
Copepods that died during exposures, and shed molts of
copepodites, were coated in microplasticspresumably
because of hydrophobic- or static-attractions between the
negatively charged polystyrene (average zeta potential: 41.8
mV) and organic materiala process that acts to concentrate
microplastics from the surrounding seawater. Our observations
of microplastic-laden faecal pellets egested by copepods
provided no indication that passage through the alimentary
canal had any discernible impact on the microplastics.
However, plastics may alter the density and structural integrity
of faecal pellets with potential repercussions on vertical carbon
ux.
60
During our studies, we also found microplastics were
becoming trapped between the external appendages and
carapace segments of live copepods. We found that very
small microplastics (0.43.8 μm) became lodged between the
lamental hairs and setae of the antennules, furca, and the
swimming legs.
29,61
As these appendages have key roles in
copepod function and behavior, this may have repercussions for
locomotion, ingestion, mating, and mechanoreception, that
may limit their ability to detect prey, feed, reproduce, and evade
predators.
We found that the presence of 7.3 μm beads signicantly
reduced the amount of algae eaten by the copepod Centropages
typicus, whereas 20.6 μm beads showed no discernible impact
on algal consumption. This suggests C. typicus can preferentially
feed upon algae over 20.6 μm beads (but could not dierentiate
between the algae and 7.3 μm beads), or, that only the smaller
beads impact on copepod feeding (i.e., 7.3 μm beads are small
enough to become entrapped between external appendages or
be recurrently ingested). A similar nding has been observed
with Acartia clausi and Calanus pacificus nauplii, which
selectively fed upon small algae while avoiding larger beads,
but could not discriminate between algae and beads of a similar
size.
24,45,54
We found that a concentration of 4000 beads mL1
was enough to result in signicantly reduced algal ingestion
rates. This relationship reached saturation at concentrations of
>5000 beads mL1. Two previous studies have found similar
results, where the ingestion rates of the copepod A. clausi
24
and
C. pacificus
45
were signicantly reduced by the presence of
beads of a similar size to the algae. A reduction in algal feeding
may have severe consequences for copepods, as limited energy
intake, in particular with species that have minimal lipid
reserves (e.g., Centropages,Acartia), could result in decreased
fecundity and growth, or increased mortality.
24,62
We do not
yet know whether 5000 particles mL1can be considered an
environmentally relevant concentration for microplastics <10
μm in size. Perpetual fragmentation of plastic litter, coupled
with the increasing popularity of household products
containing microscopic plastic exfoliates,
5
suggests marine
plastic debris is becoming, on average, smaller over time.
63
However, due to the complexities of sampling and extraction,
and in the absence of unied sampling methodologies,
microplastics are still considered to be an under-researched
fraction of marine litter, with no consistent data relating to
plastic detritus <333 μm in diameter.
1,30,64
Further, we must
consider that microplastics made of polymers other than
polystyrene, potentially laden with chemical additives or
adhered contaminants, could result in dierent interactions
with zooplankton with variable impacts on function.
Our ndings conrm that ingestion of marine microplastic
debris by zooplankton in the ocean is feasible. Potential impacts
include reduced function and health of the individual, trophic-
transfer of contaminants to predators, and the egestion of faecal
pellets containing microplastics. Better knowledge of the extent
of microplastic contamination of oceans waters is now a
research imperative.
AUTHOR INFORMATION
Corresponding Author
*Phone: +44 (0)1752 633165; fax: +44 (0)1752 633101; e-
mail: mcol@pml.ac.uk.
Notes
The authors declare no competing nancial interest.
ACKNOWLEDGMENTS
M.C. is supported by a NERC PhD studentship (Grant
I528034). We thank the crews of the Plymouth Quest and MBA
Sepia for the collection of zooplankton and seawater, Rachel
Harmer and Andrea McEvoy for zooplankton identication and
Glen Tarran for assistance with ow cytometry.
REFERENCES
(1) Cole, M.; Lindeque, P.; Halsband, C.; Galloway, T. S.
Microplastics as contaminants in the marine environment: A review.
Mar. Pollut. Bull. 2011,62, 25882597.
(2) Thompson, R. C. Plastic debris in the marine environment:
Consequences and solutions. Marine Nature Conservation in Europe
2006,193, 107115.
(3) Derraik, J. G. B. The pollution of the marine environment by
plastic debris: A review. Mar. Pollut. Bull. 2002,44 (9), 842852.
(4) Thompson, R. C.; Olsen, Y.; Mitchell, R. P.; Davis, A.; Rowland,
S. J.; John, A. W. G.; McGonigle, D.; Russell, A. E. Lost at sea: Where
is all the plastic? Science 2004,304 (5672), 838.
(5) Fendall, L. S.; Sewell, M. A. Contributing to marine pollution by
washing your face: Microplastics in facial cleansers. Mar. Pollut. Bull.
2009,58 (8), 12251228.
(6) Browne, M. A.; Crump, P.; Niven, S. J.; Teuten, E.; Tonkin, A.;
Galloway, T.; Thompson, R. Accumulation of microplastics on
shorelines worldwide: Sources and sinks. Environ. Sci. Technol. 2011,
45 (21), 91759179.
(7) OBrine, T.; Thompson, R. C. Degradation of plastic carrier bags
in the marine environment. Mar. Pollut. Bull. 2010,60 (12), 2279
2283.
(8) Davidson, T. M. Boring crustaceans damage polystyrene floats
under docks polluting marine waters with microplastic. Mar. Pollut.
Bull. 2012,64 (9), 18211828.
(9) Lattin, G. L.; Moore, C. J.; Zellers, A. F.; Moore, S. L.; Weisberg,
S. B. A comparison of neustonic plastic and zooplankton at different
Environmental Science & Technology Article
dx.doi.org/10.1021/es400663f |Environ. Sci. Technol. XXXX, XXX, XXXXXXH
depths near the southern California shore. Mar. Pollut. Bull. 2004,49
(4), 291294.
(10) Lobelle, D.; Cunliffe, M. Early microbial biofilm formation on
marine plastic debris. Mar. Pollut. Bull. 2011,62 (1), 197200.
(11) Collignon, A.; Hecq, J.-H.; Galgani, F.; Voisin, P.; Collard, F.;
Goffart, A. Neustonic microplastic and zooplankton in the North
Western Mediterranean Sea. Mar. Pollut. Bull. 2012,64 (4), 861864.
(12) Barnes, D. K. A.; Galgani, F.; Thompson, R. C.; Barlaz, M.
Accumulation and fragmentation of plastic debris in global environ-
ments. Philos. Trans. R. Soc., B 2009,364 (1526), 19851998.
(13) Browne, M. A.; Dissanayake, A.; Galloway, T. S.; Lowe, D. M.;
Thompson, R. C. Ingested microscopic plastic translocates to the
circulatory system of the mussel, Mytilus edulis (L.). Environ. Sci.
Technol. 2008,42 (13), 50265031.
(14) Murray, F.; Cowie, P. R. Plastic contamination in the decapod
crustacean Nephrops norvegicus (Linnaeus, 1758). Mar. Pollut. Bull.
2011,62 (6), 12071217.
(15) van Franeker, J. A.; Blaize, C.; Danielsen, J.; Fairclough, K.;
Gollan, J.; Guse, N.; Hansen, P.-L.; Heubeck, M.; Jensen, J.-K.; Le
Guillou, G.; Olsen, B.; Olsen, K.-O.; Pedersen, J.; Stienen, E. W. M.;
Turner, D. M. Monitoring plastic ingestion by the northern fulmar
Fulmarus glacialis in the North Sea. Environ. Pollut. 2011,159 (10),
26092615.
(16) Boerger, C. M.; Lattin, G. L.; Moore, S. L.; Moore, C. J. Plastic
ingestion by planktivorous fishes in the North Pacific Central Gyre.
Mar. Pollut. Bull. 2010,60 (12), 22752278.
(17) Davison, P.; Asch, R. G. Plastic ingestion by mesopelagic fishes
in the North Pacific Subtropical Gyre. Mar. Ecol.: Prog. Ser. 2011,432,
173180.
(18) Talsness, C. E.; Andrade, A. J. M.; Kuriyama, S. N.; Taylor, J. A.;
vom Saal, F. S. Components of plastic: Experimental studies in animals
and relevance for human health. Philos. Trans. R. Soc., B 2009,364
(1526), 20792096.
(19) Teuten, E. L.; Saquing, J. M.; Knappe, D. R. U.; Barlaz, M. A.;
Jonsson, S.; BjÃrn, A.; Rowland, S. J.; Thompson, R. C.; Galloway, T.
S.; Yamashita, R.; Ochi, D.; Watanuki, Y.; Moore, C.; Viet, P. H.; Tana,
T. S.; Prudente, M.; Boonyatumanond, R.; Zakaria, M. P.; Akkhavong,
K.; Ogata, Y.; Hirai, H.; Iwasa, S.; Mizukawa, K.; Hagino, Y.; Imamura,
A.; Saha, M.; Takada, H. Transport and release of chemicals from
plastics to the environment and to wildlife. Philos. Trans. R. Soc., B
2009,364 (1526), 20272045.
(20) Mato, Y.; Isobe, T.; Takada, H.; Kanehiro, H.; Ohtake, C.;
Kaminuma, T. Plastic resin pellets as a transport medium for toxic
chemicals in the marine environment. Environ. Sci. Technol. 2001,35
(2), 318324.
(21) Moore, C. J.; Moore, S. L.; Leecaster, M. K.; Weisberg, S. B. A
comparison of plastic and plankton in the North Pacific central gyre.
Mar. Pollut. Bull. 2001,42 (12), 12971300.
(22) Moore, C. J.; Moore, S. L.; Weisberg, S. B.; Lattin, G. L.; Zellers,
A. F. A comparison of neustonic plastic and zooplankton abundance in
southern Californias coastal waters. Mar. Pollut. Bull. 2002,44 (10),
10351038.
(23) Wirtz, K. W., Who is eating whom? Morphology and feeding
type determine the size relation between planktonic predators and
their ideal prey. In 2012; Vol. 445, pp 1-12.
(24) Ayukai, T. Discriminate feeding of the calanoid copepod Acartia
clausi in mixtures of phytoplankton and inert particles. Mar. Biol. 1987,
94 (4), 579587.
(25) DeMott, W. R. Discrimination between algae and detritus by
freshwater and marine zooplankton. Bull. Mar. Sci. 1988,43 (3), 486
499.
(26) Frost, B. W. Feeding behavior of Calanus pacif icus in mixtures of
food particles. Limnol. Oceanogr. 1977,22 (3), 472491.
(27) Hart, M. W. Particle captures and the method of suspension
feeding by echinoderm larvae. Biol. Bull. 1991,180 (1), 1227.
(28) Wilson, D. S. Food size selection among copepods. Ecology
1973,54 (4), 909914.
(29) Mauchline, J. The Biology of Calanoid Copepods. Academic Press:
London, 1998.
(30) Hidalgo-Ruz, V.; Gutow, L.; Thompson, R. C.; Thiel, M.
Microplastics in the marine environment: A review of the methods
used for identification and quantification. Environ. Sci. Technol. 2012,
46 (6), 30603075.
(31) Browne, M. A.; Galloway, T. S.; Thompson, R. C. Spatial
patterns of plastic debris along estuarine shorelines. Environ. Sci.
Technol. 2010,44 (9), 34043409.
(32) Claessens, M.; Meester, S. D.; Landuyt, L. V.; Clerck, K. D.;
Janssen, C. R. Occurrence and distribution of microplastics in marine
sediments along the Belgian coast. Mar. Pollut. Bull. 2011,62 (10),
21992204.
(33) Lozano, R. L.; Mouat, J. Marine Litter in the North-East Atlantic
Region: Assessment and Priorities for Response; KIMO International:
2009.
(34) Harris, R. The L4 time-series: The first 20 years. J. Plankton Res.
2010,32 (5), 577583.
(35) Smyth, T. J.; Fishwick, J. R.; Al-Moosawi, L.; Cummings, D. G.;
Harris, C.; Kitidis, V.; Rees, A.; Martinez-Vicente, V.; Woodward, E.
M. S. A broad spatio-temporal view of the Western English Channel
observatory. J. Plankton Res. 2010,32 (5), 585601.
(36) PlasticsEurope PlasticsThe facts 2010. http://www.
plasticseurope.org/documents/document/20101028135906-nal_
plasticsthefacts_26102010_lr.pdf
(37) Kiørboe, T. How zooplankton feed: Mechanisms, traits and
trade-offs. Biological Reviews 2011,86, 311339.
(38) Moger, J.; Johnston, B. D.; Tyler, C. R. Imaging metal oxide
nanoparticles in biological structures with CARS microscopy. Opt.
Express 2008,16 (5), 34083419.
(39) Garrett, N. L.; Lalatsa, A.; Begley, D.; Mihoreanu, L.; Uchegbu,
I. F.; Schä
tzlein, A. G.; Moger, J. Label-free imaging of polymeric
nanomedicines using coherent anti-stokes Raman scattering micros-
copy. J. Raman Spectrosc. 2012,43 (5), 681688.
(40) Garrett, N. L.; Lalatsa, A.; Uchegbu, I.; Schätzlein, A.; Moger, J.
Exploring uptake mechanisms of oral nanomedicines using multimodal
nonlinear optical microscopy. J. Biophotonics 2012,5(56), 458468.
(41) Tarran, G. A.; Heywood, J. L.; Zubkov, M. V. Latitudinal
changes in the standing stocks of nano- and picoeukaryotic
phytoplankton in the Atlantic Ocean. Deep Sea Res., Part II 2006,
15161529.
(42) Frost, B. W. Effect of size and concentration of food particles on
the feeding behaviour of the marine planktoinic copepod Calanus
pacificus.Limnol. Oceanogr. 1972,17, 805815.
(43) Roberts, E. C.; Wootton, E. C.; Davidson, K.; Jeong, H. J.;
Lowe, C. D.; Montagnes, D. J. S. Feeding in the dinoflagellate Oxyrrhis
marina: Linking behaviour with mechanisms. J. Plankton Res. 2011,33
(4), 603614.
(44) Huntley, M. E.; Barthel, K. G.; Star, J. L. Particle rejection by
Calanus pacificus: Discrimination between similarly sized particles.
Mar. Biol. 1983,74, 151160.
(45) Fernandez, F. Particle selection in the nauplius of Calanus
pacificus.J. Plankton Res. 1979,1(4), 313327.
(46) Hammer, A.; Grüttner, C.; Schumann, R. The effect of
electrostatic charge of food particles on capture efficiency by Oxyrrhis
marina Dujardin (Dinoflagellate). Protist 1999,150 (4), 375382.
(47) Christaki, U.; Dolan, J. R.; Pelegri, S.; Rassoulzadegan, F.
Consumption of picoplankton-size particles by marine ciliates: Effects
of physiological state of the ciliate and particle quality. Limnol.
Oceanogr. 1998,43 (3), 458464.
(48) Juchelka, C. M.; Snell, T. W. Rapid toxicity assessment using
ingestion rate of cladocerans and ciliates. Arch. Environ. Contam.
Toxicol. 1995,28 (4), 508512.
(49) Chan, W. Y.; Witting, J. The impact of microplastics on salp
feeding in the tropical Pacific. ANU Undergrad. Res. J. 2012,4.
(50) Powell, M. D.; Berry, A. Ingestion and regurgitation of living
and inert materials by the estuarine copepod Eurytemora af f inis
(Poppe) and the influence of salinity. Estuarine, Coastal and Shelf
Science 1990,31 (6), 763773.
Environmental Science & Technology Article
dx.doi.org/10.1021/es400663f |Environ. Sci. Technol. XXXX, XXX, XXXXXXI
(51) Lam, R. K.; Frost, B. W. Model of copepod filtering response to
changes in size and concentration of food. Limnol. Oceanogr. 1976,21
(4), 490500.
(52) Tiselius, P. Behavior of Acartia tonsa in patchy food
environments. Limnol. Oceanogr. 1992,37 (8), 16401651.
(53) Paffenhöfer, G.; Van Sant, K. B. The feeding response of a
marine planktonic copepod to quantity and quality of particles. Mar.
Ecol.: Prog. Ser. 1985,27,5565.
(54) Donaghay, P.; Small, L. Food selection capabilities of the
estuarine copepod Acartia clausi.Mar. Biol. 1979,52 (2), 137146.
(55) Hansen, B.; Hansen, P. J.; Nielsen, T. G. Effects of large
nongrazable particles on clearance and swimming behaviour of
zooplankton. J. Exper. Mar. Biol. Ecol. 1991,152 (2), 257269.
(56) Teuten, E. L.; Rowland, S. J.; Galloway, T. S.; Thompson, R. C.
Potential for plastics to transport hydrophobic contaminants. Environ.
Sci. Technol. 2007,41 (22), 77597764.
(57) Betts, K. Why small plastic particles may pose a big problem in
the oceans. Environ. Sci. Technol. 2008,42 (24), 89958995.
(58) Lithner, D.; Larsson, Å.; Dave, G. Environmental and health
hazard ranking and assessment of plastic polymers based on chemical
composition. Sci. Total Environ. 2011,409 (18), 33093324.
(59) Oehlmann, J. r.; Schulte-Oehlmann, U.; Kloas, W.; Jagnytsch,
O.; Lutz, I.; Kusk, K. O.; Wollenberger, L.; Santos, E. M.; Paull, G. C.;
Van Look, K. J. W.; Tyler, C. R. A critical analysis of the biological
impacts of plasticizers on wildlife. Philos. Trans. R. Soc., B 2009,364
(1526), 20472062.
(60) Urrè
re, M. A.; Knauer, G. A. Zooplankton fecal pellet fluxes and
vertical transport of particulate organic material in the pelagic
environment. J. Plankton Res. 1981,3(3), 369387.
(61) DeMott, W. R.; Watson, M. D. Remote detection of algae by
copepods: Responses to algal size, odors and motility. J. Plankton Res.
1991,13 (6), 12031222.
(62) Dagg, M. Some effects of patchy food environments on
copepods. Limnol. Oceanogr. 1977,99107.
(63) Andrady, A. L. Microplastics in the marine environment. Mar.
Pollut. Bull. 2011,62 (8), 15961605.
(64) Doyle, M. J.; Watson, W.; Bowlin, N. M.; Sheavly, S. B. Plastic
particles in coastal pelagic ecosystems of the Northeast Pacific ocean.
Mar. Environ. Res. 2011,71 (1), 4152.
Environmental Science & Technology Article
dx.doi.org/10.1021/es400663f |Environ. Sci. Technol. XXXX, XXX, XXXXXXJ
... Globally, plastic pollution is a major problem with adverse effects for freshwater and marine ecosystems (Thompson et al., 2004;Cole et al., 2013;Free et al., 2014;Lechner et al., 2014;Schmidt et al., 2017;Lau et al., 2020;Van Emmerik et al., 2022a). Once plastic is produced and discarded on land, a large amount is retained in riverine sinks while only a fraction ends up in marine ecosystems via riverine transport (Moore et al., 2011;Lebreton et al., 2017;Schmidt et al., 2017;D'Hont et al., 2021;Meijer et al., 2021;Van Emmerik et al., 2022b). ...
Article
Full-text available
Plastic pollution in the ocean occurs mainly via riverine transport. In rivers, plastic is pervasive in sediments and in the water column. Monitoring of floating plastics in rivers is time consuming as it is usually collected using nets and classified by hand, or counted and classified visually. To make plastic detection in the water column more time- and cost-efficient, there is a need to explore remote sensing options. Here we present the results of two semi-controlled pilot tests in standing water using two imaging sonar technologies: an Adaptive Resolution Imaging Sonar (ARIS) sonar and a low-cost side-scan sonar (SSS). Additionally, the ARIS sonar was tested in flowing water at a sheltered shore channel behind a longitudinal training dam in the river Waal, Netherlands. Both technologies were able to detect 100% of the macroplastics tested in standing water. The ARIS sonar provided higher resolution images of the targets tested due to its high operation frequency detecting macroplastics down to a size of 1 cm2. The ARIS sonar detected macroplastics in the field, however, the detection decreased to 67% in flowing water. This sonar was limited to the 2D horizontal position of targets. The SSS is a low-cost option for monitoring of plastics and is integrated with CHIRP sonar technology that combines side and down imaging providing the 3D position of targets. For future monitoring, an ARIS sonar in motion or two ARIS sonars used simultaneously may provide the necessary 3D spatial information of plastic targets.
... The movement of plastic waste through the marine environment is mainly driven by ocean currents, but is mediated by coastal, sea-surface, and seabed interactions, as well as the specific characteristics of plastic pollution (Kaiser et al., 2017;Kooi et al., 2017;Long et al., 2015;ter Halle et al., 2016). Additionally, plastic particles can be redistributed organically within faecal pellets of marine organisms (Cole et al., 2016;Cole et al., 2013; see Section 3.4.1). The Indonesia Through Flow (Fig. 4) is the major current between the Pacific and Indian Oceans (Sprintall et al., 2009), and its stratified profile interacts with the region's complex bathymetry (Gordon and Fine, 1996;Sprintall et al., 2009), strong internal tides (Nugroho et al., 2018), seasonal surface-currents (Lee et al., 2019), and currents from the South China Sea . ...
Article
Southeast Asia is considered to have some of the highest levels of marine plastic pollution in the world. It is therefore vitally important to increase our understanding of the impacts and risks of plastic pollution to marine ecosystems and the essential services they provide to support the development of mitigation measures in the region. An interdisciplinary, international network of experts (Australia, Indonesia, Ireland, Malaysia, the Philippines, Singapore, Thailand, the United Kingdom, and Vietnam) set a research agenda for marine plastic pollution in the region, synthesizing current knowledge and highlighting areas for further research in Southeast Asia. Using an inductive method, 21 research questions emerged under five non-predefined key themes, grouping them according to which: (1) characterise marine plastic pollution in Southeast Asia; (2) explore its movement and fate across the region; (3) describe the biological and chemical modifications marine plastic pollution undergoes; (4) detail its environmental, social, and economic impacts; and, finally, (5) target regional policies and possible solutions. Questions relating to these research priority areas highlight the importance of better understanding the fate of marine plastic pollution, its degradation, and the impacts and risks it can generate across communities and different ecosystem services. Knowledge of these aspects will help support actions which currently suffer from transboundary problems, lack of responsibility, and inaction to tackle the issue from its point source in the region. Being profoundly affected by marine plastic pollution, Southeast Asian countries provide an opportunity to test the effectiveness of innovative and socially inclusive changes in marine plastic governance, as well as both high and low-tech solutions, which can offer insights and actionable models to the rest of the world.
... Neben direkten Auswirkungen wie z. B. das Verfangen von Meeressäugern, Schildkröten und Seevögeln in Plastiknetzen oder -schlingen (Croxall et al., 1990;Arnould & Croxall, 1995;Gregory, 2009;Phillips et al., 2010;Votier et al., 2011;Duncan et al., 2017;Franco-Trecu et al., 2017) sowie das Verschlucken von Plastikpartikeln (Moser & Lee, 1992;Pierce et al., 2004;Gregory, 2009;Brandão et al., 2011;Kühn & van Franeker, 2012;Schuyler et al., 2012;Codina-García et al., 2013;Cole et al., 2013;de Stephanis et al., 2013;Bond et al., 2014;Cousin et al., 2015;Lusher et al., 2015;Gilbert et al., 2016;Denuncio et al., 2017;van Franeker et al., 2018) sind auch indirekte negative Auswirkungen durch enthaltende bzw. anhaftende Schadstoffe zu erwarten (z. ...
Technical Report
Full-text available
Antarctica and the surrounding Southern Ocean are under increasing pressure from cumulative impacts of climate change, pollution, fisheries, tourism and a variety of other human activities. These changes pose a high risk both to local polar ecosystems and to the regulation of the global climate, as well as through global sea-level rise. Thus, long-term monitoring programmes serve to assess the state of ecosystems as well as to make projections for future developments. The Fildes Region in the southwest King George Islands (South Shetland Islands, Maritime Antarctica), consisting of the Fildes Peninsula, Ardley Island and several offshore islands, is one of the largest ice-free areas in the Maritime Antarctic. As a continuation of a long-term monitoring programme started in the 1980s, local breeding bird and seal populations were recorded during the summer months (December, January, February) of the 2018/19 and 2019/20 seasons and supplemented by individual count data for the 2020/21 season. This study presents the results obtained, including the population development of the local breeding birds. Here, some species showed stable populations in a long-term comparison (brown skuas, southern polar skuas) or a significant increase (gentoo penguin, southern giant petrel). Other species, however, recorded significant declines in breeding pair numbers (Adélie penguin, chinstrap cenguin, Antarctic tern, kelp gull) up to an almost complete disappearance from the breeding area (cape petrel). In addition, the number of seals at their haul-out sites was recorded and the distribution of all seal reproduction sites in the Fildes Region was presented. Furthermore, data on the breeding bird population in selected areas of Maxwell Bay were added. Additionally, the rapid expansion of the Antarctic hairgrass was documented with the help of a completed repeat mapping. The documentation of glacier retreat areas of selected areas of Maxwell Bay was updated using satellite imagery and considered in relation to regional climatic development. Furthermore, the distribution and amount of marine debris washed up in the Fildes Region and the impact of anthropogenic material on seabirds will are addressed. In addition, the current knowledge of all introduced non-native species in the study area and the need for further research are presented.
Article
Increases in temperature/salinity promote nanoplastics toxicity, while organic matter/natural colloids mitigate toxicity.
Article
This study evaluates the toxicity of pristine (Unwashed) and aged, clean (Biofilm-) or fouled (Biofilm+), PS microspheres (3 μm,10 μm), using Washed particles as a reference material, on selective and continuous larval culture of Amphibalanus amphitrite. Exposure to 3 μm Unwashed and Biofilm+ particles for 24h induced significant mortality (60% and 57% respectively) in stage II larvae. Stage II and VI nauplii showed greater uptake of 3 μm Biofilm- particles. Accumulative exposure to microplastics in continuous larval culture significantly affected the naupliar survival, particularly of stage III and IV. Cumulative mortality was >70% after exposure to 3 μm Unwashed and 10 μm Biofilm+ particles. Unwashed particles with increasing concentration and aged particles with increasing size, delayed the development of nauplii to cyprids. Though,>50% cyprids showed successful settlement however the highest concentration of 3 μm Biofilm+ microspheres inhibited the settlement and induced precocious metamorphosis in 9% of the cyprids.
Article
Full-text available
Plastic production began in the early 1900s and it has transformed our way of life. Despite the many advantages of plastics, a massive amount of plastic waste is generated each year, threatening the environment and human health. Because of their pervasiveness and potential for health consequences, small plastic residues produced by the breakdown of larger particles have recently received considerable attention. Plastic particles at the nanometer scale (nanoplastics) are more easily absorbed, ingested, or inhaled and translocated to other tissues and organs than larger particles. Nanoplastics can also be transferred through the food web and between generations, have an influence on cellular function and physiology, and increase infections and disease susceptibility. This review will focus on current research on the toxicity of nanoplastics to aquatic species, taking into account their interactive effects with complex environmental mixtures and multiple stressors. It intends to summarize the cellular and molecular effects of nanoplastics on aquatic species; discuss the carrier effect of nanoplastics in the presence of single or complex environmental pollutants, pathogens, and weathering/aging processes; and include environmental stressors, such as temperature, salinity, pH, organic matter, and food availability, as factors influencing nanoplastic toxicity. Microplastics studies were also included in the discussion when the data with NPs were limited. Finally, this review will address knowledge gaps and critical questions in plastics’ ecotoxicity to contribute to future research in the field.
Article
Microplastics (MPs) released from both primary and secondary sources affect the functioning of aquatic system. These MPs and components leached, can interact with aquatic organisms of all trophic levels, including the primary producers, such as microalgae. Considering the ecological value of microalgae and the toxicological effects of MPs towards them, this review provides: (1) a detailed understanding of the interactions between MPs and microalgae in the complex natural environment; (2) a discussion about the toxic effects of single type and mixtures of plastic particles on the microalgae cells, and (3) a discussion about the impacts of MPs on various features of microalgae -based bioremediation technology. For this purpose, toxic effects of MPs on various microalgal species were compiled and plastic components of MPs were ranked on the basis of their toxic effects. Based on available data, ranking for various plastic components was found to be: Polystyrene (PS) (rank 1) > Polyvinyl Chloride (PVC) > Polypropylene (PP) > Polyethylene (PE) (rank 4). Furthermore, the review suggested the need to understand joint toxicity of MPs along with co-contaminants on microalgae as the presence of other pollutants along with MPs might affect microalgae differently. In-depth investigations are required to check the impact of MPs on microalgae-based wastewater treatment technology and controlling factors.
Article
Full-text available
The oceanic convergence zone in the North Pacific Subtropical Gyre acts to accumulate floating marine debris, including plastic fragments of various sizes. Little is known about the ecological consequences of pelagic plastic accumulation. During the 2009 Scripps Environmental Accumulation of Plastics Expedition (SEAPLEX), we investigated whether mesopelagic fishes ingest plastic debris. A total of 141 fishes from 27 species were dissected to examine whether their stomach contents contained plastic particles. The incidence of plastic in fish stomachs was 9.2%. Net feeding bias was evaluated and judged to be minimal for our methods. The ingestion rate of plastic debris by mesopelagic fishes in the North Pacific is estimated to be from 12 000 to 24 000 tons yr–1. Similar rates of plastic ingestion by mesopelagic fishes may occur in other subtropical gyres.
Article
The marine copepod Acartia tonsa was fed small plastic beads (7-70 microns) in a variety of size-frequency distributions and a concentration of 3,000-4,000 beads/ml. Both selective and non-selective feeding were observed. Selective feeding was intense over a narrow size range (selected particle sizes over 20 times more abundant in the gut than in the water); the actual sizes selected depended on the size frequency distribution offered, associating always with the largest abundant particles. A hypothesis for the mechanism of food size selection is that the animals "scan" the size distribution by capturing particles larger than the previous one ingested more efficiently than those that are smaller; the copepods then "locate" an abundance peak and halt the process just to the right of it.
Article
Body size determines the position of organisms in plankton food webs. The mass or diameter ratio between predators and their optimal prey is therefore a central element of size-based models, which attempt to link consumer groups across trophic levels. Despite a renaissance of size-based approaches in plankton ecology, however, this relation still lacks a generic and also mechanistically sound formulation. An empirically derived constant value of this ratio cannot describe the wide scatter in optimal prey diameter for specific predator size classes, especially in the mesozooplankton range. In this study, I propose that a given morphometric ratio between feeding-related apparatus and total body volume decreases when predator size increases. This ratio decrease is due to the additional need for structural components in larger organisms for maintaining intra-body transport. Non-isometric scaling results in a non-linear dependency of optimal prey size on predator diameter. This dependency defines an average relation which enables the quantitative definition of feeding mode. This new trait variable explains a component of the variability in optimal prey diameter that is independent of predator diameter. Feeding mode as a trait can be interpreted as activity during grazing, mostly in terms of speed regulation in swimming or in feeding-current generation. Feeding mode, in concert with the classical trait predator size, accurately determines optimal prey size. This was extensively tested using literature data for the entire plankton domain. The theory predicts increasing feeding activity in larger consumer species. It elucidates how successional shifts in the composition of zooplankton communities are linked to weakly coupled changes in mean body size and feeding mode.
Article
Motility of individual female Acartia tonsa in response to patchiness of the diatom Thalassiosira weiss$Zogii was investigated with a digitizing technique and standard video recordings. Motility, measured as 10-s displacement, was reduced after 24 h of starvation but was unaffected by 4 h of starvation; it increased temporarily after transfer from food to filtered seawater. When food was present only in the upper half of the aquarium, copepods spent most of their time there and produced as many fecal pellets as in homogeneous food distributions. Detailed video analysis showed that feeding bout frequency was higher and jump frequency lower in the presence of food than in filtered seawater. Copepods performed fast vertical ascents by repetitive jumps to reach the food layer from greater distances; by such behavior they were able to remain in food layers only 30 mm thick placed in the middle of a 200-mm column of filtered seawater. Even with such thin layers of food, copepods produced as many fecal pellets as in homogeneous food distributions over 2-h periods. Fast response to food and strong ability to remain inside patches probably is crucial for copepods confronted with ephemeral or thin patches of food.
Article
This article is in Free Access Publication and may be downloaded using the “Download Full Text PDF” link at right.
Article
ABSTRACT When,adult,females,of Calanus,pacificus,are,fed,on,monospecific,cultures,of,centric diatoms which grow as single cells, a predictive relationship is found between feeding behavior,of the,copepods,and,size,and,concentration,of,food,particles.,Ingestion,rate of copepods increases linearly with cell concentration up to a maximal,rate. This maximal ingestion rate, expressed as carbon, is the same for copepods feeding on diatoms ranging in diameter from 11-87 P. As the size of food particles increases, the carbon,concentration,at,which,this,ingestion,rate,is achieved,decreases.,Thus,females ofpacificus can,obtain,their maximal,daily,ration at relatively,low,carbon,concentrations of large cells, INTRODUCTIOS In oceanic food webs, Calanoid copepods