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Boring crustaceans damage polystyrene floats under docks polluting marine waters with microplastic

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Boring crustaceans damage polystyrene floats under docks polluting marine
waters with microplastic
Timothy M. Davidson
Aquatic Bioinvasion Research and Policy Institute, Environmental Science and Management, Portland State University (ESM), P.O. Box 751, Portland, OR 97207, USA
article info
Keywords:
Burrowing isopod
Invasive species
Marine borers
Microplastic
Plastic pollution
Sphaeroma quoianum
abstract
Boring isopods damage expanded polystyrene floats under docks and, in the process, expel copious num-
bers of microplastic particles. This paper describes the impacts of boring isopods in aquaculture facilities
and docks, quantifies and discusses the implications of these microplastics, and tests if an alternate foam
type prevents boring. Floats from aquaculture facilities and docks were heavily damaged by thousands of
isopods and their burrows. Multiple sites in Asia, Australia, Panama, and the USA exhibited evidence of
isopod damage. One isopod creates thousands of microplastic particles when excavating a burrow; col-
onies can expel millions of particles. Microplastics similar in size to these particles may facilitate the
spread of non-native species or be ingested by organisms causing physical or toxicological harm.
Extruded polystyrene inhibited boring, suggesting this foam may prevent damage in the field. These
results reveal boring isopods cause widespread damage to docks and are a novel source of microplastic
pollution.
Ó2012 Elsevier Ltd. All rights reserved.
1. Introduction
Marine borers can cause substantial damage to marine struc-
tures. The most extensive and costly damage occurs in wooden
structures by teredinid bivalves (shipworms) and isopod crusta-
ceans (Cragg et al., 1999; Neily, 1927). For example, the non-native
shipworm Teredo navalis destroyed the timber pilings and supports
of docks in San Francisco Bay causing nearly 50 structures to
collapse and causing $615 million in damages (Cohen and Carlton,
1995; Miller, 1926; Neily, 1927). Crustacean borers are also very
destructive (Cookson et al., 1986; Cragg et al., 1999; Kofoid and
Miller, 1927), especially in Australia where timber replacement
costs from marine borers are around $20 million per year (in
1986 AUD dollars; Cookson et al., 1986). Moreover, borers can
attack non-wooden structures as well, such as rock sea walls
(Chilton, 1919), concrete structures (Kofoid and Miller, 1927),
and even steel support beams (Irwin, 1953).
Burrowing sphaeromatid isopods bore into numerous substrata
used in marine structures and facilities in brackish temperate and
tropical regions (Carlton, 1979; Chilton, 1919; Cragg et al., 1999;
Kofoid and Miller, 1927). Boring isopods are native to the Indo
and West Pacific but are non-native in North America and perhaps
in the Caribbean (Carlton and Iverson, 1981; Carlton and
Ruckelshaus, 1997; Harrison and Holdich, 1984). These estuarine
isopods tolerate a wide range of salinities (0–43 PSU, Estevez,
1994; Riegel, 1959) and temperatures (5–42 °C; Jansen, 1971).
However, they suffer mortality after several days at the lowest
salinity (0 PSU) or temperature (5 °C; Jansen, 1971; Riegel, 1959).
In the field, the boring isopods Sphaeroma quoianum, Sphaeroma
terebrans, and Sphaeroma peruvianum are most often found
between 5 and 31 PSU salinity (Davidson, 2008; Davidson et al.,
2008, unpublished data). The burrowing isopods S. quoianum and
S. terebrans live for 12–18 months and 10 months, respectively,
and can produce up to two cohorts before dying (Schneider 1976,
Thiel, 1999).
These borers are especially destructive to expanded polystyrene
floats (commonly known as Styrofoam) used in many docks.
Densely clustered colonies of these direct-developing isopods
perforate the submerged surface of the float and appear to reduce
its functionality. While burrows are initially shallow (less than
30 mm deep, and rarely exceeding 60 mm; Davidson and de Rivera,
2012; Perry and Brusca, 1989; Talley et al., 2001), subsequent
generations and colonizers extend and build from old burrows,
creating an interconnected burrow network (as described by Talley
et al., 2001; Thiel, 1999). This extensive network substantially
reduces the density of the outer 60 mm of the float, making the
foam noticeably weaker and more susceptible to breakage. As the
outer surface is removed, additional area of the float becomes
vulnerable to attack. Boring sphaeromatid isopods are filter feeders
that excavate burrows for habitat (Rotramel, 1975; Si et al., 2002);
therefore, any consumption of excavated material is likely
0025-326X/$ - see front matter Ó2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.marpolbul.2012.06.005
Present address: Smithsonian Tropical Research Institute, Apartado Postal
0843-03092, Balboa, Ancon, República de Panamá. Tel.: +507 212 8830; fax: +507
212 8790.
E-mail address: DavidsonT@si.edu
Marine Pollution Bulletin 64 (2012) 1821–1828
Contents lists available at SciVerse ScienceDirect
Marine Pollution Bulletin
journal homepage: www.elsevier.com/locate/marpolbul
incidental (Messana et al., 1994; Rotramel, 1975; Si et al., 2002).
While some floats are encapsulated with hard plastic shells or
sheets, many docks or facilities either do not use these materials,
or the encapsulation materials are damaged and vulnerable to iso-
pod burrowing (per. obs.).
Minute plastic particles are created through the boring process
of polystyrene floats by S. quoianum (Carlton, Chang, and Wells,
unpublished, as cited in Carlton and Ruiz, 2005), S. terebrans, and
S. peruvianum (per. obs.). Like other microplastics (defined as
<5 mm in diameter, Arthur and Bamford, 2009) in the marine envi-
ronment, these particles may have detrimental effects to marine
organisms (Carpenter et al., 1972; Cole et al., 2011; Gregory,
1996; Thompson et al., 2004). Plastics persist for hundreds to thou-
sands of years in normal oceanic conditions (Barnes et al., 2009).
Also, polystyrene fragments and other minute plastics in the mar-
ine environment are readily colonized by biofilm and other organ-
isms causing them to sink (Barnes, 2002; Gregory, 2009; Ye and
Andrady, 1991). Thus, these particles may interact with benthic
(Graham and Thompson, 2009; Thompson et al., 2004) and pelagic
organisms (Boerger et al., 2010; Carpenter et al., 1972; Davison and
Asch, 2011). Ingested microplastics may cause both toxicological
effects by transmitting bioaccumulating toxins (Mato et al., 2001;
Teuten et al., 2009) and possibly physical effects by occluding feed-
ing structures or inducing a false indication of satiation.
The damage caused by boring isopods to polystyrene floats un-
der floating docks can result in economic costs and contribute to
microplastic pollution. This paper reports observations of the
destructive effects of boring isopods on foam floats, quantifies
the density of burrows and individuals in floats, quantifies the
abundance of plastic particles created from the boring process,
and discusses the morphology and ecological implications of the
plastic particles created through the boring process. Furthermore,
results of an experiment examining how different polystyrene float
types may prevent damage by borers are presented. Together these
observations, surveys, and experimental results reveal (a) the dam-
aging effects of non-native and native borers on the floatation in
docks, (b) how a non-native species contributes to microplastic
pollution, and (c) approaches to reduce these effects in the many
bays that harbor populations of boring isopods.
2. Methods
2.1. Observations of isopods attacking floats
Shoreline surveys were conducted in Yaquina Bay, Oregon, USA,
and in Budai Township and Tainan, Taiwan. Both the high tide lines
and docks and marinas in intertidal and shallow subtidal areas
were examined for damaged polystyrene flotsam or floats; popula-
tions of Sphaeroma sp. occurring in adjacent substrata were also
noted. Search effort was focused on areas between 5 and 31 PSU,
where boring isopod populations are most often found (Davidson,
2008; Davidson et al., 2008). Polystyrene floats and flotsam were
considered burrowed by sphaeromatids if they harbored living or
dead individuals in their burrows or if vacant burrows were consis-
tent with the morphology of burrows created by sphaeromatid iso-
pods: (i) vermiform burrows with smooth walls, (ii) circular
diameters between 2 and 10 mm, and (iii) up to 77 mm deep,
and (iv) mostly straight without abrupt changes in direction
(Barrows, 1919; Davidson and de Rivera, 2012; Talley et al.,
2001). To my knowledge, no other boring organism creates bur-
rows consistent with this morphology and the burrows of other
organisms (e.g. small grapsid crabs) are rare (per. obs.). Further-
more, these surveys are supplemented with additional reports of
isopod burrowing from both published sources and unpublished
observations.
2.2. Mean density of individuals and burrows of S. quoianum in
expanded polystyrene flotsam
Between February 2005 and May 2006, samples of burrowed
expanded polystyrene floating dock flotsam encountered during
surveys of Coos Bay (n= 18 pieces) were collected. Each piece
was photographed with a haphazardly placed 10 10 cm quadrat
in the burrowed area of the float. The number of quadrats photo-
graphed varied concomitantly with the size of the expanded poly-
styrene flotsam found. One quadrat was used to estimate the
burrow density of small pieces (30–60 cm long) and between 6
and 50 quadrats for larger pieces (entire floats >60–100 cm long).
Digital analysis software, ImageJ 3.0 version 1.49u, was then used
to count the total numbers of burrows per quadrat.
Burrowed expanded polystyrene float mimics were deployed in
Coos Bay, Oregon for 1 year (2005–2006) to provide an estimate for
how many isopods inhabit expanded polystyrene floats. The float
mimics were constructed of a burrowed expanded polystyrene
float found in the field (devoid of isopods). Blocks were cut to
10 10 8 cm (length, width, depth). Each block was surrounded
in polyethylene tape exposing only the burrowed 100 cm
2
face.
Burrow densities in these mimics were 64.2 ± 2.3 burrows per
100 cm
2
(mean ± 95% CI). The blocks were affixed facing down-
wards to weighted PVC tubing and placed around a length of rebar
planted into the ground. The weighted PVC tube kept the orienta-
tion of the blocks pointing downward while allowing the floats to
move up and down with the tide along the rebar pole. These ex-
panded polystyrene dock mimics were deployed in six different
locations with salinity between 10 and 31 PSU in Coos Bay, Oregon.
2.3. Quantity and morphology of the plastic particles created during
boring by S. quoianum
A lab experiment was conducted to quantify the numbers of par-
ticles created by S. quoianum during the boring process (methodol-
ogy described in detail in Davidson et al., in preparation). Small
colonies of 20 adult isopods (7–12 mm in length) from Coos Bay,
Oregon were placed inside cages with an expanded polystyrene
foam block (800 cm
3
) with one exposed surface (100 cm
2
). Fifteen
small holes (4 mm deep) were created in each block to prompt iso-
pods to begin burrowing; these values were not included in the
measurements of burrow length. Each cage was then submerged
in a closed aerated aquarium at one of 13 water temperatures
(7.5–25.2 °C) to vary burrowing intensity (Davidson et al., in prep-
aration). Isopods were allowed to burrow for 2 months. At the end
of the experiment, the number of burrows created and mean
lengths were measured in each foam block and the plastic particles
were collected by discharging the aquarium water through a 63
l
m
sieve. The particles were placed on a gridded paper filter (1 cm
2
grid) and agitated to help homogenize the distribution of particles
on the grid. The total number of grid squares occupied by plastic
particles was counted and then five subsamples (1 cm
2
squares)
were randomly selected to be photographed using a digital micro-
scope camera. The numbers of particles in each square subsample
were counted using digital analysis software. The total number of
particles created during the boring process in the different blocks
was calculated by multiplying the mean number of particles per
subsample (1 cm
2
) by the total number of squares occupied by plas-
tic particles. The relationship between the number of particles cre-
ated per burrow and mean burrow length (total burrow length in a
block/number of burrows created) was examined using ordinary
least squares regression. The data were square-root transformed
to meet assumptions of linearity, homogenous variance, normality,
and reduce the influence of outliers. The lowest value appeared to
be influential (Cook’s Distance = 0.81), however, its removal did
not substantially change the shape of the relationship (but reduced
1822 T.M. Davidson / Marine Pollution Bulletin 64 (2012) 1821–1828
the R
2
to 0.67). This potentially influential value was retained since
there was not a non-statistical reason to merit its removal.
To examine the morphology of the particles, particles from
aquaria where adult individuals of S. quoianum (7–12 mm long)
had burrowed into a block of expanded polystyrene were collected.
The plastic particles and surrounding water were haphazardly col-
lected from aquarium water and placed on a microscope slide. The
particles were photographed using a digital camera attached to a
light microscope (with a calibrated scale bar). Image analysis and
preprocessing were completed using ImageJ. Images were prepro-
cessed using the Sharpen and Find Edges functions to make the
main body of the particle more conspicuous. The area (as measured
by ImageJ), perimeter, longest axis (length), and the widest axis
(orthogonal to the longest axis, width) of each of 200 particles
was measured and the equivalent circular diameter calculated
(ECD ¼ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
4
p
Area
q;Russ, 2007; Sprules et al., 1998). The ECD stan-
dardizes irregular objects to a standard circle to allow comparisons
of objects of variable shape and orientation (Russ, 2007). All mea-
surements were recorded from the areas of the particles that were
solid and opaque; the many light, short, diaphanous plastic threads
exuding from most sides were not included in measurements.
2.4. The effects of polystyrene float type on colonization by a non-
native boring isopod
The effects of three different types of polystyrene floats on bur-
rowing by S. quoianum were tested using a lab experiment in a La-
tin square design. One block of polystyrene (5 612 cm) was
affixed vertically per cylindrical microcosm (946 ml). The treat-
ments were: (a) expanded polystyrene (EPS; n= 23), (b) extruded
polystyrene (XPS; n= 22), or (c) expanded polystyrene encapsu-
lated with a damaged polyethylene cover (encapsulated EPS;
4 cm single tear at the bottom, mimicking wear and tear of encap-
sulation material exposed to boats and floating debris, n= 23). Thin
polyethylene encapsulation sheeting was often used to encapsu-
late floats in floating docks in Coos Bay and other Pacific coast estu-
aries (per. obs.). While the use of encapsulation material over foam
is mandatory in Oregon (G. Dolphin, per. comm.; Oregon Adminis-
trative Rule 250-014-0030), many docks do not use it or the mate-
rial is degraded and torn (per. obs.). Each microcosm was filled
with saltwater (25 PSU) and phytoplankton, their primary food
source in nature, was periodically added for sustenance (Rotramel,
1975). Since S. quoianum is thigmotactic, a small divot was created
in the bottom of each block to prompt isopods to start burrowing.
One adult isopod between 7 and 12 mm in length was then added
to each microcosm and allowed to burrow for 24 days. The status
of the isopods (burrowing, not burrowing, moribund, or dead)
was recorded each day for 15 days. The status of the isopods on
days 19 and 24 (the last day of the experiment) were also noted.
A chi-square test (with 10,000 randomizations) was used to test
if the total number of isopods that burrowed in a block differed
among treatments. The differences in total burrow length and bur-
row use (the percent of the time isopods were present in burrows
they created) between EPS and encapsulated EPS treatments were
analyzed using Mann–Whitney tests since transformations failed
to normalize the data. Statistical analysis of the XPS treatment data
was unnecessary as burrowing was not observed.
3. Results
3.1. Damage to the dock floats of aquaculture facilities and marinas by
sphaeromatid isopods
Damage from dense colonies of boring isopods was observed in
aquaculture facilities in Yaquina Bay, Oregon, USA and Tainan,
Taiwan. In Yaquina Bay, Oregon, colonies of the non-native isopod
S. quoianum damaged the expanded polystyrene floats used by an
aquaculture facility to raise oysters. Repair of the docks required
removing around 60 heavily-riddled floats (each 1 m long;
Fig. 1A–C). Some floats still harbored dead isopods. The outer sur-
face of many of the floats had become eroded, vacuous, and easily
ablated by touching the surface. The attack was so concentrated in
some floats that it reduced the normally rectangular shaped float
to a t-shaped cross-section (Fig. 1B).
Similar patterns were observed in Tainan, Taiwan; fifteen floats
removed from an adjacent aquaculture facility were found onshore
and heavily riddled with isopod burrows (Fig. 1D–F). In Taiwan, the
native isopod S. terebrans was likely responsible for the damage
since this species was abundant in the mangroves lining the pond.
In addition to the above observations of isopods impacting
these aquaculture facilities, field surveys revealed the presence of
burrowed foam flotsam or floats in Yaquina Bay, several sites in
Taiwan, and one site in Caribbean Panama. Five out of six sites in
Yaquina Bay with foam flotsam or exposed floats accessible for
examination were damaged by isopods. Burrowed floats were also
observed in Taiwanese sites including flotsam in Kinmen Island
(presumably washed ashore from neighboring Xiamen, mainland
China), and two burrowed floats each in Budai Township and
Tainan. Two small lightly burrowed floats were also observed at
Galeta Point near Colon in Caribbean Panama. These floats were
likely burrowed by S. terebrans since these isopods were abundant
in the adjacent red mangroves.
Burrows and isopods were also found in high densities in ex-
panded polystyrene foam flotsam and in float mimics. The foam
collected from Coos Bay harbored thousands of burrows of S. quoia-
num per square meter (Table 1). Similarly, isopods were found in
high densities in the experimental float mimics.
3.2. Quantity and morphology of the microplastic created by S.
quoianum
The numbers of particles created per burrow were strongly re-
lated to the length of the burrow (R
2
= 0.89, F= 85.8, P< 0.001;
Fig. 2). A minimum of 89 particles were created from a burrow
1.6 mm long and a maximum of 4630 particles were created from
a burrow 17.4 mm long. The plastic particles created by S. quoia-
num were variable and irregular in shape (Fig. 3). Most of the plas-
tic particles were roughly globular or rectangular in shape and
lined with fine strands; others were highly irregular. The mean
(±95% CI) maximum length of the particles was 462.6 ± 29.2
l
m
and mean maximum width (orthogonal to the maximum length)
was 283.0 ± 19.0
l
m(Fig. 4). The mean ECD was 255.1 ± 12.4
l
m.
The mean perimeter-area ratio was 0.033 ± 0.002, which was
200% higher than a similar-sized circle (diameter = 255
l
m,
perimeter-area ratio = 0.016). While the histograms of the mor-
phological characteristics were centered around the means de-
scribed above, they were skewed to the right due to a few high
values (Fig. 4).
3.3. The effects of polystyrene float type on colonization by a non-
native boring isopod
The type of polystyrene float affected the frequency of burrow-
ing, burrow length, and burrow use by S. quoianum. Isopods
burrowed more often in expanded polystyrene (10 of 23 floats
were burrowed, 43.5%) than damaged encapsulated expanded
polystyrene (7/23, 30.4%) and extruded polystyrene (0/22, 0%;
v
2
= 10.3, df = 2, P= 0.006). There was no difference in the fre-
quency of burrowing between EPS and damaged encapsulated
EPS (
v
2
= 0.89, df = 1, P= 0.35). Isopods did not burrow into (hence
did not use burrows) in the extruded foam treatment. While the
T.M. Davidson / Marine Pollution Bulletin 64 (2012) 1821–1828 1823
expanded polystyrene had greater values in all measures than the
encapsulated treatment, mean burrow length (±95% CI) was not
significantly greater in the EPS (3.23 ± 1.49) than in the damaged
encapsulated EPS (2.21 ± 1.49; U= 311, P= 0.26). Likewise, isopods
did not use burrows significantly more in the EPS (13.52 ± 8.09)
than the encapsulated EPS (9.14 ± 7.00; U= 318, P= 0.19).
4. Discussion
4.1. Damage to foam floats in aquaculture facilities and marinas by
non-native and native boring isopods
The floats of docks and facilities in Asia, Australia, Central Amer-
ica, and North America suffered damage from burrowing sphaero-
matids (Fig. 5,Table 2). These damaging effects are exemplified in
the two aquaculture facilities examined. Dense colonies of boring
isopods attacked the floats used in aquaculture facilities in Yaquina
Bay, Oregon, USA and Tainan, Taiwan, forcing the replacement of
floats and incurring economic costs. The burrow densities in these
floats, foam flotsam, and float mimics exceeded many thousands
per exposed square meter of foam. Floats inhabited by high densi-
ties of isopods were noticeably weaker and vacuous; the outermost
surface was easily removed by hand. Given such a weakened sur-
face, additional damage occurs to heavily burrowed floats when
they are scoured by water movement or abraded by debris (per.
obs.). Docks damaged by isopods have also been reported from
Coos Bay and San Francisco, California (Carlton, per comm.; Cohen
and Carlton, 1995; Davidson, 2008) with non-native populations of
S. quoianum. Previous surveys of Coos Bay revealed a ten-meter
section of a derelict dock riddled with burrows (Davidson, 2008)
and another dock in a state of disrepair with the exposed floats
burrowed by isopods (per. obs.). Likewise, a tugboat terminal in
Coos Bay was abandoned when severe burrowing by isopods ren-
dered it virtually inoperable (Carlton, per comm). While a previous
study reported polystyrene foam (Styrofoam) was rarely inhabited
compared to other substrata (Davidson, 2008), few docks accessi-
ble to surveying were available and thus may reflect low sampling
effort. Four out of five surveyed docks with exposed floats exhib-
ited burrowing damage consistent with S. quoianum (unpublished
data from Davidson, 2008). Furthermore, Cohen and Carlton
(1995) report the dock floats in marinas of San Francisco Bay were
frequently riddled by S. quoianum. This report is consistent with
accounts by Rotramel (1971), per comm who first observed exten-
sive damage by S. quoianum in floating docks at Berkeley Marina
(San Francisco, CA) in 1966. Damage to floats under docks was also
noted in Moss Landing Harbor in 1998 (Elkhorn Slough, CA;
Wasson, per comm).
Fig. 1. Extensive burrowing by populations of boring isopods damaged the polystyrene floats in the docks used by aquaculture facilities in (A–C) Yaquina Bay, Oregon, USA
(Sphaeroma quoianum; 7/15/2007) and (D–F) Tainan, Taiwan (presumably Sphaeroma terebrans; 8/5/2010). The floats in A and D were approximately 1 m and 2 m in length,
respectively. Images in C and F are at differing scales, but the burrows pictured in these images are similar in size (8–10 mm).
Fig. 2. The relationship between the numbers of plastic particles created (square-
root transformed) per burrow and the mean length of burrows created by
Sphaeroma quoianum.
Table 1
Mean, maximum, and minimum of densities of burrows and isopods (Sphaeroma
quoianum) collected from expanded polystyrene floats (n= 18; burrow densities) and
float mimics (n= 6; isopod densities) in Coos Bay, Oregon.
Density Mean (±95% CI) Max. Min.
Burrows per m
2
7875 (±1687) 25,000 2400
Burrows per float
a
23,413 (±5016) 74,322 7134
Isopods
b
per m
2
14,900 (±7576) 32,000 2400
Isopods per float 44,296 (±22,523) 95,133 7135
a
Calculations were based on a float with the following dimensions:
244 122 46 cm; surface area 3m
2
assuming the outer 6 cm was vulnerable to
burrowing damage.
b
Isopod densities are based on the colonization of the outer 6 cm of expanded
polystyrene float mimics (n= 6) deployed for 1 year.
1824 T.M. Davidson / Marine Pollution Bulletin 64 (2012) 1821–1828
Furthermore, the presence of large pieces of foam floats found
throughout Coos Bay suggests rafting may be an important dis-
persal mechanism for the non-native S. quoianum and likely other
sphaeromatids. Since isopod boring may facilitate the breakage of
floats, large floating colonies may potentially be dispersed to new
areas within a bay or possibly between bays. The movement of
large colonies of hundreds or thousands of direct developing iso-
pods may enhance invasion success in new locations (Johannesson,
1988; Thiel and Gutow, 2005).
The spread of S. quoianum to new estuaries may result in
damage to floats under docks and facilities but may also have
destructive effects to other estuarine habitats and substrata. By
perforating saltmarsh banks with burrows, populations of S.
quoianum appear to exacerbate erosion rates of saltmarshes
(Carlton, 1979; Davidson and de Rivera, 2010; Talley et al.,
2001); areas in saltmarsh banks inhabited by S. quoianum experi-
ence erosion rates 300% higher than adjacent unburrowed areas
(Davidson and de Rivera, 2010). Burrowing by isopods also alters
and damages other estuarine substrata (e.g. friable rocks, wood),
and provides a novel habitat for other organisms including dispro-
portionately large numbers of non-native species compared to
other habitats (Davidson et al., 2010).
4.2. Microplastic pollution created by a non-native boring isopod
Boring by colonies of sphaeromatid isopods in expanded poly-
styrene floats can create millions of microplastic particles and
may have negative effects to marine organisms. An individual of
S. quoianum can create up to 4630 plastic particles when excavat-
ing a burrow 17.4 mm long. Extrapolating that estimate to a popu-
lation of 100,000 (a density observed in a cubic meter of substrata,
Davidson et al., 2010; or two floats, Table 1), the total number of
particles created by 100,000 isopods each creating a burrow is
416.7 million. However, the mean burrow length (±95% CI) created
by S. quoianum in the lab (22.6 ± 2.2 mm in the lab at 14 °C) and
from field measurements (25.3 ± 17.5 mm; Davidson and de
Rivera, 2012) are longer than the burrow lengths observed in this
experiment. When estimating the number of plastic particles
created using these mean values and the equation presented in
Fig. 2 (and back transforming), one adult of S. quoianum would
create between 4900 (±1.1) and 6300 (±2801) particles during
the boring process (490–630 million per 100,000 isopods). While
there is variation in the specific number of particles created in
the boring process, these estimates reveal the extremely high mag-
nitude of microplastic that is created through the boring process by
this non-native isopod and likely other boring isopods.
4.3. Potential implications of microplastic pollution
Microplastics, similar in size to those created by this bioeroder,
persist in the marine environment (Barnes et al., 2009) and may be
consumed or colonized by numerous species (Gregory, 2009; Cole
Fig. 3. Microscope images of the plastic particles created by Sphaeroma quoianum
during the burrowing process into expanded polystyrene floats. The images are
shown at two magnifications: (A) Each square in the image is 0.25 cm
2
. (B) The scale
bar in this image is 500
l
m.
Fig. 4. Frequency histograms of the (A) area, (B) perimeter, (C) maximum length,
(D) maximum width (orthogonal to the length measurement), (E) equivalent
circular diameter (ECD) and (F) perimeter-area ratio of the microplastic particles
created during burrowing by Sphaeroma quoianum in expanded polystyrene floats
(n= 200).
T.M. Davidson / Marine Pollution Bulletin 64 (2012) 1821–1828 1825
et al., 2011). These particles were similar in size to numerous spe-
cies of zooplankton and some phytoplankton (Hansen et al., 1994;
Sprules et al., 1998) and thus may be confused for planktonic food.
Microplastics are ingested by species in a variety of trophic levels,
habitats, and feeding modes. They have been ingested by
detritivorous amphipods (Thompson et al., 2004); deposit feeding
echinoderms (Graham and Thompson, 2009) and polychaetes
(Thompson et al., 2004); filter feeding mussels (Browne et al.,
2008), crustaceans (Thompson et al., 2004), and echinoderms
(Graham and Thompson, 2009); omnivorous lobsters (Murray
and Cowie, 2011); and small planktivorous fish (Boerger et al.,
2010; Davison and Asch, 2011). Larger predators such as birds
(Laist, 1997), turtles (Laist, 1997), numerous species of fish
(Carpenter et al., 1972; Kartar et al., 1976; Laist, 1997) and mam-
mals (Ericsson and Burton, 2003) were also found with microplas-
tics inside their guts. Since isopods damage the floats used in
aquaculture facilities, the microplastic pollution created may even
become ingested by the cultured species (for example, oysters) and
thus may be transferred to humans.
There are three primary effects of microplastics to marine life
including facilitating the spread of non-native or toxic species
and both physical and toxicological effects when ingested.
Microplastics may facilitate the spread of non-native species
(Barnes, 2002; Gregory, 2009) by providing a surface to which
Fig. 5. Global occurrences of boring isopod damage to expanded polystyrene floats. The open circles in North America and Central America represent areas with known
damage from non-native sphaeromatid isopods. The closed circles in Asia and Australia denote areas damaged by native populations. See Table 2 for details.
Table 2
Locations where boring sphaeromatid isopods have attacked expanded polystyrene floats.
Location Date Species Invasion status Substratum Reference
Yaquina Bay, Oregon 2007 Sphaeroma quoianum Non-native Floats, flotsam This paper
Coos Bay, Oregon 1995 Sphaeroma quoianum Non-native Floats, flotsam Cohen and Carlton (1995)
San Francisco Bay, California 1966 Sphaeroma quoianum Non-native Floats, flotsam Rotramel (1975); per comm.
Elkhorn Slough, California 1998 Sphaeroma quoianum Non-native Floats, flotsam Wasson, per comm.
Throughout southwest Florida 1978 Sphaeroma terebrans Non-native Floats, flotsam Estevez (1978), per comm
Lake Pontchartrain, Louisiana 2004 Sphaeroma terebrans Non-native Flotsam Wilkinson (2004)
Colon, Panama 2012 Sphaeroma terebrans Non-native Flotsam This paper
Kinmen Island, Taiwan 2010 Sphaeroma terebrans Native Flotsam This paper
Budai township, Taiwan 2010 Sphaeroma terebrans Native Flotsam This paper
Tainan, Taiwan 2010 Sphaeroma terebrans Native Floats, flotsam This paper
Tamar river, Tasmania 2006 Sphaeroma quoianum Native Flotsam Davidson et al. (2008)
Port Stephens, Australia 1986 Sphaeroma quoianum,
Sphaeroma terebrans,
Ptyosphaera alata
Native Floats Cookson et al. (1986)
Townsville Australia
a
1973 Sphaeroma triste Native Floats Harrison and Holdich (1984)
Philippines
b
1986 Sphaeroma terebrans,
Sphaeroma triste
Native Floats Angell (1986)
a
Harrison and Holdich (1984) noted Sphaeroma triste in polystyrene blocks (in 1973) affixed beside a dock in Townsville, Australia but is unclear if the dock used these
blocks as floats.
b
Angell (1986) reports the necessity of protecting expanded polystyrene floats used in oyster culture facilities in the Philippines from borers; while not explicitly stated,
these borers are likely S. terebrans or S. triste.
1826 T.M. Davidson / Marine Pollution Bulletin 64 (2012) 1821–1828
those organisms can attach and subsequently floating to a new
area. Numerous non-native taxa have been found on plastics
including sponges, hydroids, bryozoans, mollusks, isopods, barna-
cles, polychaetes (Barnes, 2002; Gregory, 2009) and toxic microal-
gae (Masó et al., 2003). Even microplastics may be a viable vector;
plastics similar in size to the current study have been found trans-
porting non-native bryozoans (Barnes, 2002; Gregory, 2009). The
high surface area of these microplastics and high abundances cre-
ated through burrowing may provide additional opportunities for
small non-native taxa to colonize and disperse to new areas.
When ingested, microplastics can also accumulate in some
organisms (Browne et al., 2008; Murray and Cowie, 2011), which
may possibly lead to physical effects. The accumulation of plastics
may lead to intestinal obstructions (Carpenter et al., 1972) and
stomach ulcers (as with birds, Pettit et al., 1981). It also may cause
false indication of satiation, hence reduced growth and perhaps fit-
ness (Connors and Smith, 1982; Ryan, 1988). Researchers have
found negative correlations between plastic load and body mass
(Ryan, 1987; Spear et al., 1995) and possibly the amount of fatty
deposits in seabirds (Connors and Smith, 1982). However, it is un-
clear if microplastics can also cause similar negative physical ef-
fects to biota; this question remains an important gap that needs
to be addressed (Cole et al., 2011). Browne et al. (2008) did not find
a significant short-term biological effect of the ingestion of micro-
plastic in the mussel Mytilus edulis; however, they caution addi-
tional longer-term studies with an array of different polymers
and organisms are necessary.
Microplastics are chemically inert (Andrady, 2011; Teuten et al.,
2009), yet may become toxic due to degradation or the accumula-
tion of toxins from the ambient environment. When the plastics
degrade, they release toxic additives including phthalates, organo-
tin, and nonylphenol (Mato et al., 2001; Teuten et al., 2009; Zitko,
1993). Other toxins, such as persistent organic pollutants, have a
higher affinity for plastics than ambient seawater and accumulate
in very high concentrations (Mato et al., 2001; Teuten et al., 2007)
and may be absorbed into marine fauna (Ryan et al., 1988; Teuten
et al., 2007; Thompson, unpublished, as cited in Teuten et al.,
2009).
These persistent organic pollutants including polychlorinated
biphenyls (PCBs), polycyclic aromatic hydrocarbons (PAH’s), chlo-
rinated phenols, organochlorine pesticides (DDT and DDE) and
Bisphenol-A (BPA) are of particular concern since they are endo-
crine disruptors and carcinogenic (Walker et al., 2006). Further-
more, heavy metals (Cadmium and Lead) can also accumulate in
microplastics (Ashton et al., 2010). Since the microplastics created
by isopods are small, irregular, and have a high perimeter to area
ratio (and likely a high surface area to volume ratio), it seems likely
they would accumulate toxins more rapidly than larger spherical
plastic particles and pellets.
4.4. Polystyrene float type prevents colonization by a non-native
boring isopod
Isopods did not burrow into the XPS foam treatments during the
lab experiment, which suggests this foam type may prevent isopod
colonization and burrowing in the field. These lab results are con-
sistent with observations from the field. The XPS floats or flotsam
encountered during surveys were never burrowed by isopods
(per. obs.). The XPS foam is noticeably harder than EPS foam and
it is likely this substratum is too hard for boring. In contrast, EPS
foam, such as the type used in many floating docks, was burrowed
more frequently and burrowed deeper than the other treatments.
The damaged encapsulated EPS float mimics also exhibited lower
colonization rates, burrow use, and shorter burrows than the EPS
floats, although the results were not statistically different. While
these results suggest a thin encapsulation material may inhibit
boring to some degree, I recommend using a hardened polyethyl-
ene shell around an XPS foam core to prevent damage from borers
and debris and degradation from the ambient seawater. This labo-
ratory experiment, combined with field and lab observations, sug-
gests that XPS is resistant to isopod damage and thus may be a
viable option to reduce the impacts of burrowing by S. quoianum
and other boring isopods.
5. Conclusions
The destruction of expanded polystyrene floats used in floating
docks and aquaculture facilities by boring isopods can be exten-
sive. Burrowing by dense colonies of isopods degrades floats,
reducing their longevity and function. Burrowing also releases mil-
lions of microplastic particles into the marine environment. These
particles are similar in morphology to other microplastic particles
(Carpenter et al., 1972; Gregory, 1996) and may have detrimental
effects to marine organisms. These negative effects, however,
may be prevented or mitigated by using extruded polystyrene
floats and/or a thick rigid encapsulation material under docks
and facilities.
Acknowledgments
I thank James Carlton, Andy Chang, Simon Cragg, Catherine de
Rivera, Glenn Dolphin, Ernie Estevez, George Rotramel, Gregory
Ruiz, Kerstin Wasson, and Elizabeth Wells for providing technical
advice, information on the distribution of borers, and helpful con-
versations. The comments from the reviewers helped improve a
previous version of this manuscript. I am grateful to Hwey Lian
Hsieh for providing lab space and transportation assistance while
in Taiwan. Aspects of this research were supported by the Western
Regional Panel on Aquatic Nuisance Species (under United States
Fish & Wildlife Service Grant Agreement number 60181-7G256
to C.E. de Rivera), the Estuarine Reserves Division, Office of Ocean
and Coastal Resource Management, National Ocean Service,
National Oceanic and Atmospheric Administration (fellowship to
T.M. Davidson), and the National Science Foundation East Asia
and South Pacific Summer Institute fellowship in Taiwan (fellow-
ship to T.M. Davidson).
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1828 T.M. Davidson / Marine Pollution Bulletin 64 (2012) 1821–1828
... Organisms interact with all sizes of plastics, with possible effects ranging from physical stress to chemical assimilation. Plastics significantly larger than the organism can represent a substrate for colonization of smaller organisms and invertebrates (Davidson, 2012). Large yet ingestible size classes of plastics represent a risk of gastrointestinal blockages (Gall and Thompson, 2015). ...
... Les organismes interagissent avec toutes les tailles de plastiques, avec des effets possibles allant du stress physique à l'assimilation chimique. Les débris de plastiques d'une plus grosse taille peuvent représenter un substrat pour la colonisation d'organismes et d'invertébrés plus petits (Davidson, 2012). Les classes de tailles de plastiques de grande taille mais ingérables représentent un risque de blocage gastro-intestinal (Gall and Thompson, 2015). ...
Thesis
The omnipresence of microplastic (MP) represents a novel environmental pressure acting on freshwater ecosystems and a better understanding of the dynamic of this pollution is needed. Here, we investigated the spatial and temporal changes in MP pollution (size range 700 μm – 5 mm) in the Garonne catchment (Southwestern France) and the consumption of these particles by aquatic organisms. The composition of MP was verified through attenuated total reflectance Fourier transformed infrared spectroscopy (ATR-FTIR). First, a total of 14 sites located in the main river and several tributaries were sampled during four seasons. We found that MP concentration averaged 0.15 particles.m-3 (± 0.46 SD) and strongly varied both in space and in time, driven by urbanization and hydrological conditions. Higher MP concentrations and smaller particle sizes were observed in warm seasons with low discharge. Second, we analysed the changes in MP pollution caused by flooding. Two sites in the Garonne River, located upstream and downstream of Toulouse, were sampled during two flood episodes. We found a general increase in MP concentration during flood episodes. This was driven by river discharge, but this increase was greater in the downstream site. Regarding MP characteristics, a predominance of larger particles was observed. Using multivariate analysis of the infrared spectra, we quantified the changes in MP chemical profile during flooding. A higher oxidation profile, represented by an increased carbonyl spectral band, was found in particles collected during the flood. Third, a novel pathway of MP into freshwaters was assessed by quantifying MP pollution in angling baits. We analysed three different categories of industrially-produced baits (‘groundbait’, ‘boilies’ and ‘pellets’). From 160 bait samples, 28 MP were identified in groundbait and boilies. No MP within the studied size range were found in pellets. We revealed that MPs introduced accidentally during bait manufacturing and/or those originating from contaminated raw ingredients might be transferred into freshwaters. Fourth, the consumption of MPs by macroinvertebrates and fish was quantified. This consumption was linked to individual trophic niches, which were measured by stable isotope analyses (δ13C and δ15N). We demonstrated that the abundance of ingested MP differed between macroinvertebrates and fish and was not significantly related to MP pollution. We also found that MP characteristics differed between the abiotic (water and sediment) and biotic (macroinvertebrates and fish) compartments. The abundance of ingested MP increased with organism size in both fish and macroinvertebrates and tended to increase with the trophic position of macroinvertebrates. The origin of the resources consumed by fish significantly affected the abundance of MP ingested in fish. Altogether, these results suggested the absence of MP bioaccumulation in the studied size range in freshwater food webs and the dominance of direct consumption, most likely accidentally. In conclusion, we highlighted that MP pollution should be perceived as a multi-stressor due to the particulate behaviour and potential interactions with other environmental contaminants. The consequences of these interactions should be the focus of future research. This work contributes to improve our understanding to elucidate the drivers of the dynamic and consumption of MP, and further studies are needed to quantify the actual risks associated with this pollution in freshwater ecosystems.
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Plastic equipment such as fishing nets and foam buoys has been widely used in aquaculture. This kind of equipment would gradually decompose while being subject to the long-term effects of physical, chemical, and biological degradation processes, leading to the release of large amounts of microplastics (MPs) into the local marine environment and the generation of aquaculture-derived MPs (AD-MPs). The rapid growth of aquaculture has resulted in an explosion of AD-MPs with various environmental consequences. The accumulation of MPs in aquatic products was found closely related to the abundance of environmental MPs, suggesting the importance of determining whether AD-MPs increase the risk of MP ingestion by aquatic products and thus endanger aquatic food safety. In this short communication, the ecological and health risks of AD-MPs were discussed and perspectives were proposed for future studies.
... 如韩国Heungnam海滩占总MPs的比例可超过90% [22] ), 或被钻孔甲壳动物破坏(其在浮体中挖掘洞穴时可向 水环境中释放数百万个MPs颗粒 [23] ). 此外, 在养殖区丢 弃、遗失或以其他方式丢置的渔具(abandoned, lost or otherwise discarded fishing gears, ALDFGs)也会裂解形 成多种MPs进入水环境甚至水生生物体内, 造成不良影 响 [11,24] . ...
... Microplastics are comprised of synthetic polymer products manufactured to a smaller size ( Cole et al., 2013 ) (i.e., exfoliates in cosmetics) ( Fendall and Sewell, 2009 ) and fragments of larger plastic debris (i.e., polyester fibres -synthetic fabrics; polyethylene -plastic bags; polystyrene particles -buoys and floats) ( Browne et al., 2011 ;O'Brine, et al., 2010 ;Davidson, 2012 ). Microfibers and microbeads from cosmetics, clothes, and sanitary goods, are usual constituents of municipal and domestic wastewater sludge ( Bayo et al., 2020 ;Zhang et al., 2020 ;Ren et al., 2020 ;Mendoza et al., 2018 ). ...
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