Content uploaded by Culum Brown
Author content
All content in this area was uploaded by Culum Brown on Oct 10, 2017
Content may be subject to copyright.
1 3
Mar Biol (2016) 163:199
DOI 10.1007/s00227-016-2973-0
ORIGINAL PAPER
Microplastics on beaches: ingestion and behavioural
consequences for beachhoppers
Louise Tosetto1 · Culum Brown1 · Jane E. Williamson1
Received: 6 April 2016 / Accepted: 22 August 2016
© Springer-Verlag Berlin Heidelberg 2016
show that short-term ingestion of microplastics have an
impact on survival and behaviour of P. smithi. A reduction
in the capacity for beachhoppers to survive and function
may have flow on effects to their local environment and
higher trophic levels.
Introduction
Plastic is a global issue for marine environments due to its
conspicuous role in modern lifestyle and economy. Micro-
plastic contamination is an increasing issue in our marine
systems, and one that has been gaining momentum for
the past decade (Thompson et al. 2004; Law and Thomp-
son 2014). Microplastics, small plastic fragments less than
5 mm (GESAMP 2010), pose a diverse risk to organisms
within marine ecosystems. Microplastics are introduced
to the environment directly (for example, via cosmetic
beads) or indirectly through breakdown and fragmenta-
tion of larger plastic debris (Andrady 2011; Cole et al.
2011; Thompson 2015) or via fibers from clothing (Browne
2015). Microplastics derive from a range of plastics such as
polyvinyl chloride (PVC), polyethylene (PE) and polysty-
rene and have an array of uses (Andrady 2011). They range
in densities and thus are spread throughout the water col-
umn (Engler 2012). Such widespread distribution exposes
a broad range of organisms across the food chain with
consumption of microplastics demonstrated in a range of
feeding guilds (Thompson et al. 2004) and across multiple
trophic levels from zooplankton (Cole et al. 2013) to fish
(Boerger et al. 2010) and seals (Eriksson and Burton 2003).
In addition to the potential physical effects resulting from
microplastic ingestion such as false satiation and reduced
nutrition (Murray and Cowie 2011; Cole et al. 2013), chem-
ical effects due to associated contaminants on microplastics
Abstract Microplastics are ubiquitous in the marine envi-
ronment worldwide, and may cause a physical and chemi-
cal risk to marine organisms. Their small size makes them
bioavailable to a range of organisms with evidence of
ingestion at all levels of the marine ecosystem. Despite an
increasing body of research into microplastics, few studies
have explored how consumption changes complex behav-
iours such as predator avoidance and social interactions.
Pollutant exposure can result in alterations in behaviour
that not only leads to sub optimal conditions for individual
organisms but may also serve as a warning sign for wider
effects on a system. This research assessed the impacts of
microplastics on the ecology of coastal biota using beach-
hoppers (Platorchestia smithi) as model organisms. We
exposed beachhoppers to marine-contaminated micro-
plastics to understand effects on survival and behaviour.
Beachhoppers readily ingested microplastics, and there
was evidence for accumulation of microplastics within the
organisms. Exposure tests showed that microplastic con-
sumption can affect beachhopper survival. Individuals also
displayed reduced jump height and an increase in weight,
however, there was no significant difference in time taken
to relocate shelter post disturbance. Overall, these results
Responsible Editor: M. Huettel.
Reviewed by undisclosed experts.
Electronic supplementary material The online version of this
article (doi:10.1007/s00227-016-2973-0) contains supplementary
material, which is available to authorized users.
* Louise Tosetto
louise.tosetto@mq.edu.au
1 Department of Biological Sciences, Macquarie University,
Sydney, NSW 2109, Australia
Mar Biol (2016) 163:199
1 3
199 Page 2 of 13
now present additional implications for marine biota. Poten-
tially toxic additives such as phthalates, bisphenol A (BPA)
and flame-retardants are incorporated into many plastics
during manufacturing to increase functionality and extend
the life of the plastics (Browne et al. 2008b). Furthermore,
plastics are porous and thus accumulate and concentrate
contaminants including polychlorinated biphenyls (PCBs),
pesticides and fertilizers at high intensities from the sur-
rounding seawater (Teuten et al. 2007). Many of the addi-
tives and the absorbed contaminants are known endocrine
disruptors, carcinogens and mutagens (Lithner et al. 2009).
Some conceptual and biodynamic models simulating effects
of plastic on the bioaccumulation of contaminants suggest
that plastics are negligible pathways for exposure (Koe-
lmans 2013; 2014). Other recent studies find that gut sur-
factants, temperature and pH all influence the rate of des-
orption into animals (Bakir et al. 2014). Moreover, transfer
of pollutants from microplastics to animals has been dem-
onstrated (Ryan et al. 1988; Teuten et al. 2009; Avio et al.
2015), and it is possible that microplastics provide addi-
tional passage for contaminants to accumulate in biota.
While a wide range of organisms can ingest microplas-
tics, our understanding of biological effects of such inges-
tion remains limited. Reported effects on survival, growth
and fecundity are inconsistent and often found at high
concentrations of microplastic exposure. Increased mortal-
ity was observed in copeopods (Tigriopus japonicus) but
only at large dilutions of microplastics (Lee et al. 2013).
An effect on growth was reported for body width of sea
urchin larvae (Tripneustes gratilla) at the highest concen-
tration of microplastics (Kaposi et al. 2014). Impacts on
fecundity have been reported for copeopods T. japonicus in
a two generation chronic toxicity test (Lee et al. 2013) and
Calanus helgolandicus with a reduction in egg size (Cole
et al. 2015). However, a recent study on a marine isopod
(Idotea emerginata) showed no significant effect of micro-
plastics on survival, growth and fecundity following inges-
tion (Hämer et al. 2014). Variations in biological responses
to different concentrations of microplastics advocate a
more consistent approach to assessing environmentally rel-
evant concentrations of microplastics.
In many animals, behaviour modification is often the
first response to a change in conditions (Wong and Can-
dolin 2015), and can indicate subsequent survival and
physiological issues (Scott and Sloman 2004). Studies so
far assessing any behavioural effects from microplastics
have focused on changes to foraging rates (Besseling et al.
2012; Wegner et al. 2012; Cole et al. 2013; Wright et al.
2013b), but changes to complex behaviours such as preda-
tor avoidance, burrowing and orientation are also essential
to our understanding of the ecological impacts (Ungher-
ese and Ugolini 2009; Weis 2014). Behavioural responses
provide useful markers of pollution effects on individuals,
potentially performing as reliable and economical indicators
of sub lethal effects of pollutants (Weis 2014). Accordingly,
there is growing emphasis in ecotoxicology on examining
changes in behaviour in response to exposure to contami-
nants, which is far more sensitive than the standard LD50
(median lethal dose) approach (Oulton et al. 2014). Given
the connection that behaviour provides between physiologi-
cal and ecological processes, behavioural alterations not
only indicate issues at the individual level but also serve as
a warning sign for wider effects on a system (Weis 2014).
Microplastics accumulate in coastal areas (Browne et al.
2011; Turra et al. 2014; Setälä et al. 2016) and contami-
nants have been shown to adhere to microplastics in coastal
sediments (Frias et al. 2010). Density of microplastic has
been reported as high as 30 % by weight in highly pol-
luted sites (Carson et al. 2011) with evidence for particles
as deep as two metres (Turra et al. 2014). The supralitto-
ral zone is an ecologically important area on sandy shores
providing important connectivity between the surf and
sand dunes (Ungherese et al. 2012). These zones receive
large inputs of algal and seagrass wrack (Gonçalves and
Marques 2011) and are typically dominated by crustaceans
such as coastal talitrid amphipods (Gonçalves et al. 2013).
Coastal talitrids, or beachhoppers (Amphipoda, Talitridae)
are highly mobile organisms that inhabit sediment in wave-
washed beaches. They carry out an important ecological
role in the function of sandy shores by commencing the
decomposition processes of algae and wrack, essential for
benthic sediment remineralisation processes (Dugan et al.
2011). They are also primary consumers and a food source
for birds, (Dugan et al. 2003), beetles (Poore and Gallagher
2013) and fish (Fanini and Lowry 2014), therefore impor-
tant in the transfer of energy between the different trophic
levels (Griffiths et al. 1983).
Beachhoppers have been shown to consume microplas-
tic (Ugolini et al. 2013), and have been identified as a good
bioindicator species for accumulation of chemicals within
the environment (Ungherese et al. 2012). Their life history
and behaviour is well understood (Scapini 2006) and with
a lifespan of between four and eighteen months (Wildish
1988), they make a useful species on which to study the
effects of microplastics. The physical exposure on sandy
beaches places beachhoppers at risk of predation, fur-
thermore, beachhoppers do not have a large physiological
capacity to survive in such harsh environments and desic-
cation is another threat (Koch 1989). Salutatory locomotion
and behavioural adaptations such as well-refined hygroki-
nesis, along with the ability to locate and remain in opti-
mal humidity are important in avoiding desiccation and
predation (Ugolini 1996; Morritt 1998). Any fundamental
changes to the behaviour of key organisms such as beach-
hoppers could have flow on effects to their environment
and higher trophic levels.
Mar Biol (2016) 163:199
1 3
Page 3 of 13 199
This study assessed the effects of microplastics on Pla-
torchestia smithi (Lowry 2012), a beachhopper found in
the Sydney region of Australia. Exposing animals to more
environmentally relevant concentrations and evaluating
behaviours in relation to an animal’s habitat is impor-
tant. Given dessication and predation are risks to talitrids,
the ability to quickly relocate shelter or escape predation
is key to survival. Whole organism performance capac-
ity is important in terms of broad ecological function, but
prey can increase their probability of escaping a predator
attack by using behaviours that enhance response times
or shorten distances to the nearest refuge (Hawlena et al.
2011; McGinley et al. 2013). Given Ugolini (1996) sug-
gests that jumping in talitrids is an important anti-predator
approach, this study assesses jumping height and frequency
as a proxy for fitness. It is possible that microplastics may
negatively impact on these behaviours, reducing the capac-
ity of these animals to survive in their environment. Specif-
ically we asked the following questions. (1) Do beachhop-
pers ingest microplastics when exposed at environmentally
relevant concentrations? (2) Are additives from contami-
nated microplastic concentrated in beachhoppers? (3) Does
microplastic ingestion affect their survival? (4) Does micro-
plastic ingestion affect beachhopper behaviours important
for existence in their environment?
Materials and methods
To examine marine contaminated microplastics and the
effects on beachhoppers there were a number of sequential
experiments undertaken. (1) We contaminated microplas-
tics in an urban bay for two months and then assessed con-
tamination of microplastics post exposure. (2) We exposed
P. smithi to contaminated microplastics and examined
if microplastics were readily ingested in a 24 h ingestion
study. (3) To evaluate if the contaminant load of beach-
hoppers increased following microplastic exposure, we
analysed beachhoppers using gas chromatography –mass
spectrometry (GC-MS) at three time points. (4) We then
examined effects of microplastic ingestion on survival
and behaviour of beachhoppers through exposure tests;
(a) A 72 h exposure study [timeframe based on previous
amphipod exposure studies; (Chua et al. 2014; Hämer et al.
2014)] was conducted to assess changes in survival and
behaviour. (b) The exposure study was repeated at 120 h
to assess the effects of extended microplastic exposure. (5)
Following findings from the behavioural experiment, a final
study was designed to evaluate differences in beachhopper
weight following exposure to microplastics (a schematic of
the overall study design is provided in Fig. 1).
All five stages of the experiment were carried out inde-
pendently of each other. It was not possible to reuse the
animals across multiple experiments given excessive han-
dling compromised the health of the animals. All animals
were collected from the same location and are representa-
tive of that population’s response. Beachhoppers used in
experiments were adults, size range 8–10 mm. They were
housed in identical conditions and randomly selected for
each experimental stage.
Treatment assays consisted of natural sediments that had
had an addition of contaminated PE microplastics at 3.8 %
Fig. 1 A schematic diagram of
the five different experimental
stages that were undertaken as
part of the overall beachhopper
ingestion and behaviour study
Microplastic Contamination & Analysis
Deployed PE in Port Jackson for two months
Analyzed microplastics with GC-MS for
contamination of PAHs
Microplastic Ingestion Study
Assessed ingestion of microplastics over 24 hours
Beachhopper Contamination Analysis
Analysed beachhoppers at three time points
72 hour Exposure Study:
Survival
Jump Height & Frequency
Shelter Relocation
120 hour Exposure Study:
Survival
Jump Height & Frequency
Weight Difference Study
1
2
3
4a
5
4b
Mar Biol (2016) 163:199
1 3
199 Page 4 of 13
(Dry Weight (DW)). A recent study assessing ingestion
of microplastics in coastal talitrids used identical micro-
plastics with a concentration of 10 % (DW) (Ugolini et al.
2013). Other studies that have reported deleterious effects
on organisms have used microplastic weights of over 5 %
wet weight (Besseling et al. 2014; Graham and Thompson
2009; Wright et al. 2013a). The maximum observed weight
of microplastic in a core from a highly polluted beach has
been recorded as 30.2 % with an average plastic distribution
on a polluted beach of 3.3 % (Carson et al. 2011). Given
that microplastics continue to accumulate in coastal sedi-
ments (Turra et al. 2014) we deemed 3.8 % an environmen-
tally relevant concentration to use in the current study. Sedi-
ment was obtained from beachhopper sampling locations
at Forrester’s Beach, NSW (33°24′37.06″, 151°28′05.39″)
thus providing the same baseline condition for all beachhop-
pers used in the study. The sampling location was chosen in
a non-industrial, minimally urbanised area so that possible
background contamination was reduced. Prior to placement
into replicates, sand was dried at 40°C for 24 h.
Preparation of microplastics
Commercial polyethylene (PE) microspheres (Cospheric
UVPMS-BG, 1.004 g mL−1 density, nominal 38–45 µm
diameter, colour green) were used as proxies for primary
microplastics in marine environments (Kaposi et al. 2014).
To replicate microplastics from the marine environment we
deployed microspheres in the aquarium at Sydney Insti-
tute of Marine Science (SIMS), in Port Jackson, Australia
(33°50′24″/151°15′13″) prior to use. Seawater at SIMS is
pumped from Port Jackson, Sydney and filtered through
100 µm disc filters with all other physical parameters such
as water temperature, salinity and pH remaining ambi-
ent. To absorb any pollutants available in the surrounding
marine environment, 40 g of microspheres were placed
in a banjo filter (100 × 100 mm) fitted with 22 µm mesh.
Water from the harbour flowed freely through the filter,
thus exposing the microspheres to contaminants present.
The banjo filter was regularly rotated to ensure adequate
absorbtion on all microspheres. We contaminated the
microspheres for two months (Rochman et al. 2013) after
which the filter was collected and dried in a sealed con-
tainer at room temperature for three weeks prior to use in
experiments. While all efforts were made to reduce expo-
sure to airborne contamination, all microplastics were han-
dled in the same way, thus any additional contamination
would have affected treatments equally.
Contamination analysis—PE microplastics
Microplastics were assessed for contamination post expo-
sure to seawater from Port Jackson, NSW. We analysed
0.2 g at two time periods: one when the microplastics were
initially obtained prior to use (uncontaminated), and the
other after two months of exposure to seawater in the field
(contaminated). Polycyclic Aromatic Hydrocarbons (PAHs)
are one of the most widespread organic pollutants in the
aquatic environment (Gonçalves et al. 2008). Given PE has
a high sorption capacity for PAHs (Fries and Zarfl 2012), PE
microplastics were assessed for uptake of PAHs, which were
used as a proxy for a range of contaminants including poly-
chlorinated biphenyls (PCBs) and polybrominated diphenyl
ether (PBDEs). PE microsphere treatment samples (0.2 g)
were placed in a beaker with 30 mL of dichloromethane/n-
hexane (1:1) and extracted using ultrasonication for 25 min.
Sample solutions were allowed to settle, then transferred to
another beaker for reduction using nitrogen blow-down, and
were then transferred to 2 mL injection vials. Samples were
spiked with an internal standard (p-Terphnyl-d14).
Samples were analysed using GC-MS. The instru-
ment was a gas chromatograph (Agilent 7890A), coupled
to a Pegasus time-of-flight-mass spectrometer (GCxGC-
ToFMS), operated in one-dimensional mode. Samples were
injected (1 μL) through a split/splitless injector operating
at 310 °C in splitless mode onto a J&W DB5MS column
(60 m × 0.25 mm i.d., 0.25 mm film thickness) coated with
modified 5 % phenyl 95 % methyl silicone, with He as the
carrier gas. The temperature programme was 40 °C (2 min)
to 310 °C (held 45 min) at 4 °C / min, and the detector volt-
age of the mass spectrometer was 1850 v for both untreated
and marine-exposed microplastic samples. Aromatic
hydrocarbon fractions of an international external stand-
ard (North Sea Oil, NSO-1; (Weiss et al. 2000)) were run
using the same GC-MS programme to aid component iden-
tification. The aromatic hydrocarbons were identified based
on relative retention times and mass spectral information.
Peak areas were integrated using LECO® Chromatof® and
quantified relative to the peak areas of the internal standard
p-Terphynl-d14 and the recorded weight for each sample.
Study organisms
Platorchestia smithi were collected by hand from March to
July 2015 from the supralittoral zone of Forrester’s Beach,
NSW (33°24′37.06″, 151°28′05.39″). Individuals were
maintained in damp sand and transported to Macquarie
University in Sydney where they were held in plastic tubs
(60 cm × 40 cm) with approximately 4 cm sand and a
covering of the fresh kelp Ecklonia radiata (C. Agardh) J.
Agardh. Abiotic conditions such as light and temperature
mimicked those at the site of collection. Tubs were cov-
ered with 2 mm mesh to allow for air circulation but inhibit
escape of animals. Sand was kept damp with seawater and
carefully mixed every third day to maintain aeration. Fresh
kelp was provided to beachhoppers every week. Housing
Mar Biol (2016) 163:199
1 3
Page 5 of 13 199
conditions of all beachhoppers were identical so that there
was no difference in baseline condition prior to microplas-
tic exposure. Experiments were carred out in sterile glass
beakers, beachhoppers were randomly selected and placed
into treatments for each of the experimental stages.
Beachhopper ingestion study
To assess the time for beachhoppers to consume and digest
microspheres, five beakers were prepared with 25 g sedi-
ment (~0.5 cm thick layer) and an additional 1 g contami-
nated microplastics (3.8 % DW). Twenty five adult P. smithi
(size range 8–10 mm) were randomly selected and five
placed in each beaker. Time of exposure was recorded from
when beachhoppers were placed into the beakers. Beach-
hoppers were monitored hourly from time of exposure until
all twenty five beachhoppers had consumed microplastic or
24 h had elapsed.
Beachhopper contamination analysis
Contaminant uptake in beachhoppers following ingestion
of microplastics was examined at three time points. (1) To
assess beachhoppers exposed to beach sand without micro-
plastics. (2) To assess contamination of beachhoppers fol-
lowing 72 h exposure to microplastics. (3) To examine if
there were residual contaminants absorbed in beachhop-
pers following egestion of microplastics. Experiments were
setup in three, 2 L beakers; the control beaker consisted
of 52 g sediment and two treatment beakers each had 50 g
sediment and 2 g microplastics (3.8 % DW). Twenty beach-
hoppers were added to each of the three beakers. All beak-
ers had 15 g of fresh E. radiata placed on top of the sand
and 15 ml of freshwater to emulate their natural environ-
ment. Beakers were covered with mesh and left in ambient
conditions in the laboratory with natural light. 3–5 ml of
freshwater was added to the beakers every two days. Fol-
lowing 72 h exposure, all individuals in the control beaker
were collected, rinsed with distilled water and frozen in liq-
uid nitrogen. This process was repeated for all individuals
in one of the treatment beakers. The beachhoppers in the
second treatment beaker were transferred into an uncon-
taminated beaker containing just 52 g clean sediment for
48 h to allow for egestion of microplastics. Reports suggest
that coastal talitrids egest majority of ingested microplas-
tics after 24 h (Ugolini et al. 2013), thus we deemed 48 h
a suitable timeframe for egestion. After 48 h the beach-
hoppers from the second treatment were collected and fro-
zen in liquid nitrogen. All samples were stored at −30 °C.
Contaminant concentration analysis was undertaken for the
pool of beachhoppers at each time point.
For beachhopper contamination analyses, samples were
freeze dried, ground and extracted in 5 mL dichloromethane
using ultrasonication for 30 min. Samples were allowed to
settle and a 4 mL aliquot of the solution was taken. The
aliquot was dried over MgSO4, filtered and then concen-
trated to approximately 100 µL by nitrogen blow-down.
The samples were spiked with an internal standard (p-Ter-
phnyl-d14), and then run on the GC-MS as per the methods
outlined above for contamination analysis of microplastics.
The detector voltage of the mass spectrometer was 1600 v
for the amphipod samples at the three exposure timepoints.
The amount of PAH (µg g−1) in each sample was calculated
by taking the total area for all PAHs (excluding the internal
standard) using the following formula:
Exposure tests
Exposure tests assessed effects of microplastics on survival
and behaviour of beachhoppers. When algal wrack is dis-
turbed on a sandy shore, beachhoppers need to relocate
suitable shelter quickly as to minimise the risks (biotic and
abiotic) present in the surrounding environment (Morritt
1998). P. smithi were observed to congregate under patches
of algae and seek shelter together (Tosetto, personal obser-
vation), thus behavioural tests of beachhoppers were car-
ried out in groups. Experiments were set up in sterile 1L
glass beakers (90 mm high, 50 mm diameter). Treatment
beakers consisted of 25 g sediment (~0.5 cm thick layer)
covering the bottom of the beaker, with an additional 1 g
contaminated microplastics (3.8 % DW) evenly mixed
through. Control beakers contained 26 g of sediment only.
Five adult P. smithi, were randomly selected and placed
into each of the replicate beakers. Both treatment and con-
trol beakers had 10 g of fresh E. radiata placed on top of
the sand and 10 ml of freshwater. Beakers were covered
with mesh and left in ambient conditions in the laboratory
with natural light. 3–5 ml of freshwater was added to the
beakers every two days.
72 h exposure test
Two exposure tests were carried out at 72 h (n = 13 beak-
ers for test 1 and n = 14 beakers for test 2). Survival, jump
height, jump frequency and shelter relocation times were
assessed. Data for the two 72 h exposure experiments were
pooled (n = 27) given that there were no significant differ-
ences in survival or behaviour between the two 72 h expo-
sure tests (P > 0.05).
120 h exposure test
Given the trend that was observed after 72 h, the study was
repeated for an extended timeframe. An exposure test at
Total PAH/p
−
Terphenyl
−
d14
(
internal standard)
∗
Total µg standard
Mar Biol (2016) 163:199
1 3
199 Page 6 of 13
120 h (n = 11 beakers) was carried out assessing survival,
jump height and jump frequency. The shelter relocation test
was not undertaken at 120 h as five beachhoppers in each
replicate beaker did not survive, thus insufficient numbers
were available to undertake this component of the study.
Details on each component of the exposure tests are out-
lined below.
Survival
The number of live beachhoppers remaning in each beaker
was recorded at the end of the exposure period. Dead
beachhoppers (typcially darker in appearance and nonmo-
tile) were removed from the treatments after the number
surviving was recorded. A two-sample t-test of differences
was undertaken to assess differences in the average number
of beachhoppers alive per treatment (R Core Team 2013).
Jump height and frequency
Differences in jumping height between individuals exposed
to microplastics were compared to control individuals.
Height was assessed in a 2 L beaker with measurements
outlined in the beaker in 1 cm vertical intervals from 0 to
18 cm. A piece of fresh E. radiata, 100 × 50 mm, was
placed in the experimental beaker and the five beachhop-
pers from a replicate beaker were added, allowing two
minutes for individuals to acclimate and shelter under the
algae. After two minutes E. radiata was removed and the
beachhoppers were given five puffs of air in rapid succes-
sion from a lens cleaner (Daiso blower) to simulate stress
resulting following disturbance on a sandy beach. A digi-
tal single-lens reflex (DSLR) Canon 650D camera, was
set up adjacent to the beaker and trials recorded onto a SD
card for future analysis. Videos were analysed frame by
frame for 500 frames (20 s) from the time the last puff was
administered using Quick Time Player 7 (version 7.6.1).
Jump height and frequency was recorded for each of the
five beachhoppers.
Experiments were conducted at 72 h exposure (n = 27)
and then again at 120 h exposure (n = 11). Jump height
and frequency was recorded for individuals, summed and
averaged for each replicate beaker. To assess differences in
jump height, a mixed effects model was produced to assess
differences in hopping height between the two treatments
taking into account any variability between individual
beakers (see Bolker et al. (2009) on using mixed models in
ecology). Treatment group was the fixed effect with repli-
cate beakers as a random effect. The mixed effects model
was analysed using lme4 package (Pinheiro J et al. 2014)
in R (R Core Team 2013). To calculate jump frequency the
total number of hops recorded over 500 frames was divided
by the number of individuals in the beaker (5), to provide
the average number of hops per individual. A linear model
was used to assess for differences between the treatment
groups using the lm function in stats package in R (R Core
Team 2013).
Shelter relocation
Potential benefits that beachhoppers obtain from residing
in groups include social syncronity and predator avoid-
ance (Ugolini 1996; Ayari et al. 2015b). Given this we
expected that we expected individual beachhoppers would
seek shelter with other conspecifics as quickly as possible
following disturbance. To understand if microplastic expo-
sure affected group behaviour, an assessment of time to
relocate shelter following disturbance was undertaken for
individuals in each replicate beaker at 72 h (n = 27). The
five individuals from each replicate beaker were placed
into a clean 1 L beaker with a 100 × 50 mm piece of E.
radiata in the centre. The beaker was placed under a cold
light and individuals left for two minutes to seek shelter
beneath E. radiata. After two minutes the macroalga was
removed, and the beachhoppers scattered actively for 30 s,
after which the macroalga was replaced in the centre. The
time taken for each individual to relocate the algae and hide
underneath was recorded. Shelter relocation was classified
as when the beachhopper’s entire body was underneath the
macroalga. The relocation trial ended when all five beach-
hoppers had sought shelter under the alga, or once 90 s had
expired. Trials were recorded on web camera (Logitech
C920), and measurements were taken on a frame by frame
basis from the recordings to ensure accuracy.
Differences in mean relocation times for individual hop-
pers were compared between treatments using a Wilcoxon-
signed rank test of differences in R (R Core Team 2013).
Overall differences in shelter relocation times between
treatment and control groups was explored using a linear
mixed effects model (Bolker et al. 2009). Fixed effect was
treatment with individual beakers as the random factor.
The mixed effects model was analysed using lme4 package
(Pinheiro J et al. 2014) in R (R Core Team 2013).
Beachhopper weight differences
It is possible that any effects of microplastic on beachhop-
per behaviour were simply due to the change in weight
of the animals following ingestion. Differences in beach-
hopper weight between treatment and control groups were
therefore assessed for 72 and 120 h. Experiments were set
up in 1L glass beakers (90 mm high, 50 mm diameter).
Treatment beakers consisted of 59.7 g sediment (~0.8 cm
thick layer) covering the bottom of the beaker with 2.3 g
microplastics (3.8 % DW) evenly mixed through, while
control organisms were exposed to 62 g of sediment only.
Mar Biol (2016) 163:199
1 3
Page 7 of 13 199
Two beakers were set up for each treatment group (control
and treatment) for each time period (72 and 120 h), making
eight beakers in total. Thirty beachhoppers (size 8–10 mm)
were randomly selected and placed in each of the beakers.
Both treatment and control beakers had 10 g of fresh E.
radiata placed on top of the sand with 10 ml of freshwater
added. Beakers were covered with mesh and left in ambi-
ent conditions in the laboratory with natural light. 3-5 ml of
freshwater was added to the beakers every two days. At the
end of 72 h and 120 h the respective hoppers were removed
from treatments and placed into ethanol for subsequent
measuring and weighing.
Individual length (cm) and weight (g) was recorded.
Regression between weight and length was done and stand-
ardised residuals were obtained. A nested ANOVA assess-
ing differences in residual beachhopper weights between
treatment and time (beaker nested in treatment) was
assessed with IBM SPSS Statistics (version 21). Post-hoc
comparison was undertaken using Fisher’s Least Squares
Differences (LSD).
Results
PAH analysis
Analysis of the two sets of PE microplastics showed no
PAHs present on the microplastics prior to deployment
at SIMS. Following exposure to seawater from Sydney
Harbour, the contaminated microplastics contained 0.007
ug g−1 of PAHs were present, suggesting that the micro-
plastics had absorbed contaminants from the seawater.
Microplastic ingestion
Observations of beachhoppers demonstrated that micro-
plastics can be ingested as part of normal feeding. Of the
twenty five beachhoppers exposed to microplastics, 22
(88 %) consumed the plastics over the 24 h duration of the
experiment. In the first 2 h following exposure, 18 (72 %)
beachhoppers consumed microspheres, and the other 6
consumed them in the next 4 h. Ingestion of microplas-
tics was not identified in one of the individuals. A sample
beachhopper demonstrates the extent to which microplas-
tics can accumulate through the animal. Microplastics seen
throughout the gut caeca as well as within the coxal gills of
the animals (Fig. 2).
Beachhopper contamination
After 72 h of exposure, the beachhoppers in the control
group contained a total of 2.34 ug g−1 PAH, while those in
the treatment group had a total of 3.09 ug g−1, an increase
of 0.74 ug g−1. However, following 48 h post treatment,
contamination levels had dropped to concentrations on par
with those in the control group (2.21 ug g−1) suggesting
there was little or no residual contamination of PAHs fol-
lowing egestion of microplastics.
Fig. 2 A representative beach-
hopper following 72 h exposure
to microplastics. The green cir-
cles are polyethylene microplas-
tics that have moved through
the gut cacae and into the gills
(located behind the coxal plates)
of the beachhopper
Eye
Antennae
Microplastics foundthroughoutgut
Microplastics transferredtogills
Mar Biol (2016) 163:199
1 3
199 Page 8 of 13
Survival
There was no difference in survival in the 72-hour expo-
sure between control and treatment groups (t52 = 0.103,
P = 0.367). In the 120-hour exposure there was a differ-
ence in survival with the average number of beachoppers
alive in the control group (2.64 ± 0.28) significantly higher
than in the treatment group (1.73 ±0.27) (t20 = 2.331,
P = 0.015) (Fig. 3).
Jump height and frequency
No significant difference was found in jump height after
72 h, although microplastic treatment beachhoppers did
jump slightly lower than those in the control treatment
(−0.52 ± 0.28 cm, P = 0.069, n = 27). No significant dif-
ference between the number of jumps taken over twenty
seconds between the pooled control and treatment groups
was observed (P = 0.887). Following an exposure period
of 120 h, however, the jumping height of beachhoppers
exposed to microplastics was significantly lower than
those in the control group. The linear mixed effects model
demonstrated that beachhoppers exposed to microplastics
hopped significantly lower than those in the control group
(−1.57 ± 0.56 cm, P = 0.012, n = 11). The mean num-
ber of jumps per beachhopper did not differ significantly
between the treatment and control groups after 120 h
(P = 0.744) (Fig. 4).
Group shelter relocation
Individual beachhoppers exposed to microplastics took five
to seven seconds longer, on average, to relocate the algae
and hide than those in the control treatment, but these dif-
ferences were not statistically significant (Table 1). Overall,
beachhoppers in the microplastic treatment took 6.5 ± 3.3 s
longer than those in the control group to relocate the algae
following disturbance (W = 7702.5, P = 0.499, n = 135).
Residual weight differences
There was a significant interaction between time and treat-
ment (X2 = 14.44, df = 1, P = <0.001). Post-hoc com-
parisons show no difference in the residual weight at 72 h
(P = 0.817), however, at 120 h those beachhoppers in the
treatment group weighed significantly more than those in
the control group (P < 0.001) (Fig. 5).
Discussion
Our results demonstrate that microplastics are ingested by,
and can accumulate in, beachhoppers. Microplastics that
had been placed in the marine environment increased in
concentration of PAHs suggesting that they readily absorb
such contaminants from seawater. A slight increase in
PAHs was observed in beachhoppers following 72 h expo-
sure to microplastics. This was reversable for short term
contamination, however, as 48 h after transfer to uncon-
taminated sediment the concentration of PAHs dropped
to background levels, suggesting no residual PAHs in the
beachhoppers post egestion. No difference in survival was
observed after 72 h, however, after 120 h there were sig-
nificantly greater numbers of beachhoppers alive in the
control than the treatment group. Consumption of micro-
plastics resulted in decreased jump height after longer
exposure times, potentially resulting from an increase in
****
2
3
4
5
72 hour
s1
20 hours
Exposure Time
Mean beachhoppers alive per beaker
Treatment
Control
Microplastic
Fig. 3 Mean survival (±SE) for beachhoppers for the 72 and 120 h
microplastic exposure tests. The 72 h test was run twice and data
pooled (n = 27), whereas the 120 h test was run once (n = 11). Aster-
isks represent significance: *P < 0.05
**
3
4
5
6
7
8
Control Microplastic
Treatment
Height (cm)
a
P = 0.74P = 0.74
5
6
7
8
9
ControlMicroplastic
Treatment
No. Jumps
b
Fig. 4 Mean (+SE) Jump Height (a) and Frequency (b) for beach-
hoppers after 120 h exposure to microplastics (n = 11). Control
groups indicated by white bars, treatment groups indicated by grey
bars. Asterisks represent significance: *P < 0.05
Mar Biol (2016) 163:199
1 3
Page 9 of 13 199
beachhopper weight. Exposure to microplastics did not
affect the time taken for beachhoppers to relocate shelter
after disturbance.
Rapid ingestion rates exhibited in the laboratory sug-
gest that beachhoppers will readily consume microplas-
tics if present in the surrounding environment. There was
evidence of accumulation throughout the gut caeca and
transfer to the coxal gills of the animals. Previous stud-
ies on European talitrids, Talitrus saltator (Ugolini et al.
2013) and marine isopods I. emarginata (Hämer et al.
2014) found continual egestion of plastics in comparable
timeframes but with no reported accumulation in the ani-
mals. In mussels (Mytilus edulis), microplastics were found
to translocate from the gut to the circulatory system where
they persisted for up to 48 days (Browne et al. 2008a).
Retention of microplastics has also been reported in shore
crabs (Carcinus maenas) where microplastics have shown
to be retained in the gills and gut of crabs for two to three
weeks (Watts et al. 2014). The findings in this study show-
ing that microplastics can translocate in P. smithi suggest
that retention timeframes may be extended in natural envi-
ronments and in longer exposure scenarios.
PAHs had absorbed to microplastics during two months
exposure to seawater in Port Jackson, Sydney. The concen-
tration of 0.007ug g−1 is at the lower end of what has been
reported worldwide where PAHs range from 0.001 to 9.3
ug g−1, with the highest concentrations occurring in indus-
trialised and urban areas (Hirai et al. 2011). The micro-
plastics conditioned to seawater in this study were well
preserved after the two months and did not display pit-
ting or fragmentation. Given that weathered and degraded
plastics have increased capacity for pollutant absorption
(Endo et al. 2005; Ogata et al. 2009) it is possible that the
PAHs quantified in this study are lower than what would
be found under more natural circumstances. Following
72 h exposure to contaminated microplastics there was an
increase in the amount of PAHs in beachhoppers, however,
little or no residual PAHs following egestion of micro-
plastics. A recent study assessing absorption of the PAH
pyrene from PE to mussels following six days exposure
reported an increase of 0.145 um g−1 in digestive tissues
(Avio et al. 2015). Whether this was residual contamina-
tion or due to the presence of internal plastics is unclear as
there is no mention of a transfer of mussels to an uncon-
taminated diet prior to analysis. Although contaminant
analysis in this study focused only on the uptake of PAHs,
previous studies have shown PEs to also absorb PCBs and
PBDEs (Endo et al. 2005; Mizukawa et al. 2009; Ogata
et al. 2009). Given high concentrations of heavy metals,
organochlorine pesticides and PCBs have been reported in
Port Jackson sediments (McCready et al. 2006), it is pos-
sible that other contaminants also had an impact on the
beachhoppers. The aim of our study, however, was sim-
ply to see the impact of beachhoppers on PAH-contami-
nated microspheres and not to quantify the complete type
and amount of adherence. More research is needed with
replicate samples, sites and times of deployment to rigor-
ously quantify absolute concentrations of PAH adherence
and absorption rates, along with a broad spectrum of other
contaminants (see Browne 2015).
Survival of beachhoppers was affected by exposure to
microplastics at 120 h exposure. There were correspond-
ing differences in behaviour at 120 h with beachhoppers
in the treatment group jumping 28 % lower than control
Table 1 Summary statistics from the group shelter relocation experi-
ment
Shown is the mean time (±SE) in seconds for beachhoppers in treat-
ment and control groups to relocate algae following disturbance, the
Wilcoxon signed-rank test statistic (W) and associated P value (P).
Times are not cumulative but average the time for each individual
beachhopper to relocate shelter (n = 27)
Mean SE W P
First beachhopper Control 5.5 0.8 346 0.685
Microplastic 10.3 19.5
Second beachhopper Control 13.4 13.3 292.5 0.559
Microplastic 18.3 24.8
Third beachhopper Control 25.5 2.7 336.5 0.821
Microplastic 30.8 32.6
Fourth beachhopper Control 39.5 5.6 313.5 0.850
Microplastic 48.9 7.3
Final beachhopper Control 66.1 7.6 285 0.464
Microplastic 73.9 7.0
−0.5
0.0
0.5
1.0
ControlMicroplastic
Treatment
Standardised Residuals(g)
a
**
−0.5
0.0
0.5
1.0
Control Microplastic
Treatment
StandardisedResiduals(g)
b
Fig. 5 Mean (±SE) differences in standardised residual weights
of beachhoppers following microplastic ingestion. a Differences
between beachhoppers after 72 h. b Differences between beachhop-
pers after 120 h. Control groups indicated by white bars, treatment
groups indicated by grey bars. Residuals >0 indicate heavier hoppers
at a given length, whereas residuals <0 are lighter than expected at a
given length
Mar Biol (2016) 163:199
1 3
199 Page 10 of 13
individuals. The corresponding increase in weight gain
suggests that internal microplastics may have affected the
jumping ability of the beachhoppers. No studies to date
have assessed changes in organism weight due to micro-
plastic ingestion but extended digestion timeframes and
inflammation have been described in lugworms (Wright
et al. 2013a) and longer gut residence times reported for
bethic invertebrates (Hyalella Azteca) (Au et al. 2015) fol-
lowing consumption of microplastics. It is possible weight
gain is a short term consequence of ingested material tak-
ing longer to digest through organisms. Alternatively,
the reduction in jump height may be due to a reduction
in energy availability in beachhoppers. Consumption of
microplastics has been shown to reduce feeding activity,
possibly due to false satiation, in shore crabs (C. maenas)
(Watts et al. 2014), lugworms (A. marina) (Besseling et al.
2012) and marine copepods (Calanus helgolandicus) (Cole
et al. 2015). Moreover, extensive digestion and gut resi-
dence times are both costly energetic processes that may
over longer periods reduce primary metabolism and respi-
ration (Weis 2014). Interestingly, there was no difference in
jump frequency between treatments with individuals aver-
aging 5 and 6.7 jumps over 20 s for 72 and 120 h expo-
sure tests, respectively. This was comparable with Ugolini
(1996) reporting that following shelter disturbance, T. sal-
tator individuals jumped on average 4.8 times over 20 s
suggesting the disturbance response may be similar for
coastal talitrids and the consumption of microplastics has
no effect on this response.
While the time taken to relocate shelter following dis-
turbance did not differ between treatments, there was a
trend observed with beachhoppers in microplastic treat-
ments taking six seconds longer, on average, than those in
the control. A more consistent and longer period of expo-
sure to microplastics may have reaped different results. It
has been suggested that amphipods have have class-level
recognition (definition provided in Gherardi et al. 2012).
Chemical cues, such as molt hormones are the most domi-
nant channel of communication between conspecifics in
amphipods (Thiel 2011). There is evidence that pollutants
can disrupt these chemical cues (Rodríguez et al. 2007),
that may in turn also affect the ability for amphipods to
identify conspecifics (Beermann et al. 2015). It is possible
that increased contamination via persistent microplastic
ingestion may alter recognition processes amongst beach-
hoppers subsequently affecting group behaviour. Variations
in individual body clocks and locomotor activity rhythms
stabilise when in groups (Bregazzi and Naylor 1972; Ayari
et al. 2015b) and this social synchronisation is thought to
be important for individual survival (Ayari et al. 2015a).
Group cohesion may also be an important anti-predator tac-
tic whereby dispersal in different directions following dis-
turbance creates a confusion effect for potential predators
(Ugolini 1996). Furthermore, it is possible that residing
in groups may provide navigational benefits to beachhop-
pers in finding new habitats (see ‘many wrongs principle’
discussed in Codling et al. (2007) and Simons (2004)).
Impacts on group behaviour, whether altering activity lev-
els or relocation strategies, may have effects on local popu-
lations and in this regard the effects of longer term expo-
sure to microplastics should be explored.
It is unclear whether the observed alterations to the
behaviour of beachhoppers in our experiments were due
to the physical nature of the ingested microplastics or their
associated contaminants. Evidence for desorbtion of pyrene
from polyethylene and polystyrene into mussel tissue sug-
gests that microplastics may be a vector for the transfer of
contaminants (Avio et al. 2015). However, the presence of
microplastics in amphipods has been shown to significantly
reduce the uptake of PBDEs when compared with unab-
sorbed free chemicals (Chua et al. 2014). More recently, a
critical evaluation the scientific literature regarding micro-
plastics and associated contaminants determined that the
uptake of contaminants through natural pathways possibly
exceeds accumulation via microplastic in the majority of
marine habitats (Koelmans et al. 2016). It is possible that
the behavioural alterations in beachhoppers are resulting
from the physical nature of the ingested microplastics.
This study has demonstrated that microplastics compro-
mise both survival and behaviour of beachhoppers. Differ-
ences in survival were mirrored by alterations in behaviour
suggesting that behavioural assays are a reasonable tool to
assess disturbance. At this stage it is unclear if this change
is due to the physical or chemical effects of microplastic
ingestion. It is abundantly clear, however, that behavioural
assays are effective indicators when assessing the effects of
microplastics on organisms. Desiccation and predation are
the two greatest risks that beachhoppers face in their harsh
environment (Defeo and McLachlan 2005). The ability for
these animals to move away from desiccating environments
is key to survival (Morritt and Spicer 1998). Changes in
behaviour can lead to reduced fitness such as reduced nutri-
tion, an accumulation of contaminants within the organism,
and a reduction in the ability of individuals to respond to
various biotic and abiotic cues (eg predators or desicca-
tion). Results from the present study cannot be merely
extrapolated to field scenarios. This was a short-term study
using only one type of plastic polymer. Longer-term studies
and assessing effects in situ is necessary to understand the
implications of these results in more realistic field settings.
Acknowledgments We thank the members and interns of the MEG
and BEEF labs for field and laboratory assistance, to Carlita Foster-
Hogg for work on beachhopper weight analysis, Sarah Houlhan for
undertaking GC MS analysis of microplastics and beachhoppers,
and to Alistair Poore for advice on beachhopper husbandry. Beach-
hopper collections were conducted under NSW Fisheries Scientific
Mar Biol (2016) 163:199
1 3
Page 11 of 13 199
Collection Permit number P14/0032-1.1. This is contribution #189
from the Sydney Institute of Marine Science (SIMS).
Funding This research was funded by the Department of Biological
Sciences at Macquarie University.
Compliance with ethical standards
Conflict of interest All the authors declares that they have no conflict
of interest.
Ethical approval This article does not contain any studies with verte-
brate animals performed by any of the authors.
References
Andrady AL (2011) Microplastics in the marine environment. Mar
Pollut Bull 62:1596–1605. doi:10.1016/j.marpolbul.2011.05.030
Au SY, Bruce TF, Bridges WC, Klaine SJ (2015) Responses of Hya-
lella azteca to acute and chronic microplastic exposures. Environ
Toxicol Chem 34:2564–2572
Avio CG, Gorbi S, Milan M, Benedetti M, Fattorini D, d’Errico
G, Pauletto M, Bargelloni L, Regoli F (2015) Pollutants bio-
availability and toxicological risk from microplastics to
marine mussels. Environ Pollut 198:211–222. doi:10.1016/j.
envpol.2014.12.021
Ayari A, Jelassi R, Ghemari C, Nasri-Ammar K (2015a) Effect of
age, sex, and mutual interaction on the locomotor behavior of
Orchestia gammarellus in the supralittoral zone of Ghar El Melh
lagoon (Bizerte, Tunisia). Biol Rhythm Res 46:703–714. doi:10.
1080/09291016.2015.1048950
Ayari A, Jelassi R, Ghemari C, Nasri-Ammar K (2015b) Locomo-
tor activity patterns of two sympatric species Orchestia mon-
tagui and Orchestia gammarellus (Crustacea, Amphipoda). Biol
Rhythm Res 46:863–871. doi:10.1080/09291016.2015.1060677
Bakir A, Rowland SJ, Thompson RC (2014) Enhanced desorp-
tion of persistent organic pollutants from microplastics under
simulated physiological conditions. Environ Pollut 185:16–23.
doi:10.1016/j.envpol.2013.10.007
Beermann J, Dick JTA, Thiel M (2015) Social recognition in amphi-
pods: an overview. In: Aquiloni L, Tricarico E (eds) Social
recognition in invertebrates the knowns and the unknowns.
Springer, Berlin, pp 85–100. doi:10.1007/978-3-319-17599-7_6
Besseling E, Wegner A, Foekema EM, van den Heuvel-Greve MJ,
Koelmans AA (2012) Effects of microplastic on fitness and PCB
bioaccumulation by the lugworm Arenicola marina. Environ Sci
Technol 47:593–600
Besseling E, Wang B, Lurling M, Koelmans AA (2014) Nanoplas-
tic affects growth of S. obliquus and reproduction of D. magna.
Environ Sci Technol 48:12336–12343. doi:10.1021/es503001d
Boerger CM, Lattin GL, Moore SL, Moore CJ (2010) Plastic ingestion
by planktivorous fishes in the North Pacific Central Gyre. Mar
Pollut Bull 60:2275–2278. doi:10.1016/j.marpolbul.2010.08.007
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens
MHH, White J-SS (2009) Generalized linear mixed models:
a practical guide for ecology and evolution. Trends Ecol Evol
24:127–135. doi:10.1016/j.tree.2008.10.008
Bregazzi P, Naylor E (1972) The locomotor activity rhythm of Tali-
trus saltator (Montagu)(Crustacea, Amphipoda). J Exp Biol
57:375–391
Browne MA (2015) Sources and pathways of microplastics
to habitats. In: Bergmann M, Gutow L, Klages M (eds)
Marine anthropogenic litter. Springer, Litter, pp 229–244.
doi:10.1007/978-3-319-16510-3_9
Browne MA, Dissanayake A, Galloway TS, Lowe DM, Thompson
RC (2008a) Ingested microscopic plastic translocates to the cir-
culatory system of the mussel, Mytilus edulis (L.). Environ Sci
Technol 42:5026–5031. doi:10.1021/es800249a
Browne MA, Galloway T, Thompson R (2008b) Microplastic—an
emerging contaminant of potential concern? Integr Environ
Assess Manag 3:559–561
Browne MA, Crump P, Niven SJ, Teuten E, Tonkin A, Galloway T,
Thompson R (2011) Accumulation of microplastic on shorelines
woldwide: sources and sinks. Environ Sci Technol 45:9175–
9179. doi:10.1021/es201811s
Carson HS, Colbert SL, Kaylor MJ, McDermid KJ (2011) Small plas-
tic debris changes water movement and heat transfer through
beach sediments. Mar Pollut Bull 62:1708–1713. doi:10.1016/j.
marpolbul.2011.05.032
Chua E, Shimeta J, Nugegoda D, Morrison PD, Clarke BO (2014)
Assimilation of polybrominated diphenyl ethers from microplas-
tics by the marine amphipod, Allorchestes Compressa. Environ
Sci Technol 48:8127–8134. doi:10.1021/es405717z
Codling EA, Pitchford JW, Simpson SD (2007) Group navigation and
the “many-wrongs principle” in models of animal movement.
Ecology 88:1864–1870. doi:10.1890/06-0854.1
Cole M, Lindeque P, Halsband C, Galloway TS (2011) Microplastics
as contaminants in the marine environment: a review. Mar Pollut
Bull 62:2588–2597. doi:10.1016/j.marpolbul.2011.09.025
Cole M, Lindeque P, Fileman E, Halsband C, Goodhead R, Moger
J, Galloway TS (2013) Microplastic ingestion by zooplankton.
Environmental science & technology 47: 6646–6655. http://
pubs.acs.org/doi/abs/10.1021/es400663f
Cole M, Lindeque P, Fileman E, Halsband C, Galloway TS (2015)
The impact of polystyrene microplastics on feeding, function
and fecundity in the marine copepod Calanus helgolandicus.
Environ Sci Technol 49:1130–1137
Core Team R (2013) R: A language and environment for statistical
computing. R Foundation for Statistical Computing, Vienna
Defeo O, McLachlan A (2005) Patterns, processes and regulatory
mechanisms in sandy beach macrofauna: a multi-scale analysis.
Mar Ecol Prog Ser 295:1–20. doi:10.3354/meps295001
Dugan JE, Hubbard DM, McCrary MD, Pierson MO (2003) The
response of macrofauna communities and shorebirds to mac-
rophyte wrack subsidies on exposed sandy beaches of south-
ern California. Estuar Coast Shelf Sci 58(Supplement):25–40.
doi:10.1016/S0272-7714(03)00045-3
Dugan JE, Hubbard DM, Page HM, Schimel JP (2011) Marine mac-
rophyte wrack inputs and dissolved nutrients in beach sands.
Estuaries Coasts 34:839–850. doi:10.1007/s12237-011-9375-9
Endo S, Takizawa R, Okuda K, Takada H, Chiba K, Kanehiro H, Ogi
H, Yamashita R, Date T (2005) Concentration of polychlorinated
biphenyls (PCBs) in beached resin pellets: variability among
individual particles and regional differences. Mar Pollut Bull
50:1103–1114. doi:10.1016/j.marpolbul.2005.04.030
Engler RE (2012) The complex interaction between marine debris and
toxic chemicals in the ocean. Environ Sci Technol 46:12302–
12315. doi:10.1021/es3027105
Eriksson C, Burton H (2003) Origins and biological accumulation
of small plastic particles in fur seals from Macquarie Island.
AMBIO: a Journal of the Human. Environment 32:380–384.
doi:10.1579/0044-7447-32.6.380
Fanini L, Lowry J (2014) Coastal talitrids and connectivity between
beaches: a behavioural test. J Exp Mar Biol Ecol 457:120–127.
doi:10.1016/j.jembe.2014.04.010
Frias J, Sobral P, Ferreira A (2010) Organic pollutants in microplas-
tics from two beaches of the Portuguese coast. Mar Pollut Bull
60:1988–1992. doi:10.1016/j.marpolbul.2010.07.030
Mar Biol (2016) 163:199
1 3
199 Page 12 of 13
Fries E, Zarfl C (2012) Sorption of polycyclic aromatic hydrocarbons
(PAHs) to low and high density polyethylene (PE). Environ Sci
Pollut Res 19:1296–1304. doi:10.1007/s11356-011-0655-5
GESAMP (2010) Proceedings of the GESAMP international work-
shop on plastic particles as a vector in transport0069 ng persis-
tent, bio-accumulating and toxic substances in the oceans. GES-
AMP Rep Stud, vol. 82
Gherardi F, Aquiloni L, Tricarico E (2012) Revisiting social recog-
nition systems in invertebrates. Animal cognition 15:745–762.
doi:10.1007/s10071-012-0513-y
Graham ER, Thompson JT (2009) Deposit-and suspension-feeding
sea cucumbers (Echinodermata) ingest plastic fragments. J Exp
Mar Biol Ecol 368:22–29. doi:10.1016/j.jembe.2008.09.007
Gonçalves SC, Marques JC (2011) The effects of season and wrack
subsidy on the community functioning of exposed sandy
beaches. Estuar Coast Shelf Sci 95:165–177
Gonçalves R, Scholze M, Ferreira AM, Martins M, Correia AD
(2008) The joint effect of polycyclic aromatic hydrocarbons on
fish behavior. Environ Res 108:205–213
Gonçalves SC, Anastácio PM, Marques JC (2013) Talitrid and Tylid
crustaceans bioecology as a tool to monitor and assess sandy
beaches’ ecological quality condition. Ecol Ind 29:549–557
Griffiths CL, Stenton-Dozey JME, Koop K (1983) Kelp Wrack
and the flow of energy through a Sandy beach ecosystem.
In: McLachlan A, Erasmus T (eds) sandy beaches as eco-
systems: based on the proceedings of the first international
symposium on sandy beaches, held in Port Elizabeth, South
Africa, 17–21 January 1983. Springer, Dordrecht, pp 547–556.
doi:10.1007/978-94-017-2938-3_42
Hämer J, Gutow L, Köhler A, Saborowski R (2014) Fate of Micro-
plastics in the Marine Isopod Idotea emarginata. Environ Sci
Technol 48:13451–13458
Hawlena D, Kress H, Dufresne ER, Schmitz OJ (2011) Grasshop-
pers alter jumping biomechanics to enhance escape performance
under chronic risk of spider predation. Funct Ecol 25:279–288
Hirai H, Takada H, Ogata Y, Yamashita R, Mizukawa K, Saha M,
Kwan C, Moore C, Gray H, Laursen D (2011) Organic micro-
pollutants in marine plastics debris from the open ocean and
remote and urban beaches. Mar Pollut Bull 62:1683–1692.
doi:10.1016/j.marpolbul.2011.06.004
Kaposi KL, Mos B, Kelaher BP, Dworjanyn SA (2014) Ingestion of
microplastic has limited impact on a marine larva. Environ Sci
Technol 48:1638–1645. doi:10.1021/es404295e
Koch H (1989) The effect of tidal inundation on the activity and
behavior of the supralittoral talitrid amphipod Traskorchestia
traskiana (Stimpson, 1857). Crustaceana 57:295–303. doi:10.11
63/156854089X00635
Koelmans AA (2013) Plastic as a Carrier of POPs to Aquatic Organ-
isms: a Model Analysis. Environ Sci Technol 47:7812–7820.
doi:10.1021/es401169n
Koelmans AA (2014) Leaching of plastic additives to marine
organisms. Environ Pollut 187:49–54. doi:10.1016/j.
envpol.2013.12.013
Koelmans AA, Bakir A, Burton GA, Janssen CR (2016) Microplas-
tic as a vector for chemicals in the aquatic environment: criti-
cal review and model-supported reinterpretation of empirical
studies. Environ Sci Technol 50:3315–3326. doi:10.1021/acs.
est.5b06069
Law KL, Thompson RC (2014) Microplastics in the seas. Science
345:2. doi:10.1126/science.1254065
Lee K-W, Shim WJ, Kwon OY, Kang J-H (2013) Size-dependent
effects of micro polystyrene particles in the marine copepod
Tigriopus japonicus. Environ Sci Technol 47:11278–11283
Lithner D, Damberg J, Dave G, Larsson Å (2009) Leachates
from plastic consumer products–Screening for toxicity with
Daphnia magna. Chemosphere 74:1195–1200. doi:10.1016/j.
chemosphere.2008.11.022
Lowry J (2012) Talitrid amphipods from ocean beaches along the
New South Wales coast of Australia (Amphipoda, Talitridae).
Zootaxa 3575:1–26
McCready S, Birch GF, Long ER (2006) Metallic and organic
contaminants in sediments of Sydney Harbour, Australia
and vicinity–A chemical dataset for evaluating sediment
quality guidelines. Environ Inl 32:455–465. doi:10.1016/j.
envint.2005.10.006
McGinley RH, Prenter J, Taylor PW (2013) Whole-organism perfor-
mance in a jumping spider, Servaea incana (Araneae: salticidae):
links with morphology and between performance traits. Biol J
Linn Soc 110:644–657
Mizukawa K, Takada H, Takeuchi I, Ikemoto T, Omori K, Tsuchiya
K (2009) Bioconcentration and biomagnification of poly-
brominated diphenyl ethers (PBDEs) through lower-trophic-
level coastal marine food web. Mar Pollut Bull 58:1217–1224.
doi:10.1016/j.marpolbul.2009.03.008
Morritt D (1998) Hygrokinetic responses of talitrid amphipods. J
Crustac Biol 18:25–35. doi:10.2307/1549517
Morritt D, Spicer JI (1998) The physiological ecology of talitrid
amphipods: an update. Can J Zool 76:1965–1982. doi:10.1139/
z98-168
Murray F, Cowie PR (2011) Plastic contamination in the decapod crus-
tacean Nephrops norvegicus (Linnaeus, 1758). Mar Pollut Bull
62:1207–1217. doi:10.1016/j.marpolbul.2011.03.032
Ogata Y, Takada H, Mizukawa K, Hirai H, Iwasa S, Endo S, Mato
Y, Saha M, Okuda K, Nakashima A (2009) International Pel-
let Watch: global monitoring of persistent organic pollutants
(POPs) in coastal waters. 1. Initial phase data on PCBs, DDTs,
and HCHs. Mar Pollut Bull 58:1437–1446. doi:10.1016/j.
marpolbul.2009.06.014
Oulton LJ, Taylor MP, Hose GC, Brown C (2014) Sublethal toxicity
of untreated and treated stormwater Zn concentrations on the for-
aging behaviour of Paratya australiensis (Decapoda: atyidae).
Ecotoxicology 23:1022–1029. doi:10.1007/s10646-014-1246-2
Pinheiro J BD, DebRoy S, Sarkar D, R Core Team (2014) nlme: Lin-
ear and Nonlinear Mixed Effects Models. R package version
3.1–117
Poore AG, Gallagher KM (2013) Strong consequences of diet choice
in a talitrid amphipod consuming seagrass and algal wrack. Hyd-
robiologia 701:117–127
Rochman CM, Hoh E, Kurobe T, Teh SJ (2013) Ingested plastic trans-
fers hazardous chemicals to fish and induces hepatic stress. Sci
Rep 3:3263. doi:10.1038/srep03263
Rodríguez EM, Medesani DA, Fingerman M (2007) Endocrine dis-
ruption in crustaceans due to pollutants: a review. Comp Bio-
chem Physiol A: Mol Integr Physiol 146:661–671. doi:10.1016/j.
cbpa.2006.04.030
Ryan P, Connell A, Gardner B (1988) Plastic ingestion and PCBs in
seabirds: is there a relationship? Mar Pollut Bull 19:174–176.
doi:10.1016/0025-326X(88)90674-1
Scapini F (2006) Keynote papers on sandhopper orienta-
tion and navigation. Mar Freshw Behav Physiol 39:73–85.
doi:10.1080/10236240600563412
Scott GR, Sloman KA (2004) The effects of environmental pollut-
ants on complex fish behaviour: integrating behavioural and
physiological indicators of toxicity. Aquat Toxicol 68:369–392.
doi:10.1016/j.aquatox.2004.03.016
Setälä O, Norkko J, Lehtiniemi M (2016) Feeding type affects micro-
plastic ingestion in a coastal invertebrate community. Mar Pollut
Bull 102:95–101. doi:10.1016/j.marpolbul.2015.11.053
Simons AM (2004) Many wrongs: the advantage of group navigation.
Trends Ecol Evol 19:453–455. doi:10.1016/j.tree.2004.07.001
Mar Biol (2016) 163:199
1 3
Page 13 of 13 199
Teuten EL, Rowland SJ, Galloway TS, Thompson RC (2007) Poten-
tial for plastics to transport hydrophobic contaminants. Environ
Sci Technol 41:7759–7764. doi:10.1021/es071737s
Teuten EL, Saquing JM, Knappe DR, Barlaz MA, Jonsson S, Björn A,
Rowland SJ, Thompson RC, Galloway TS, Yamashita R (2009)
Transport and release of chemicals from plastics to the environ-
ment and to wildlife. Philosoph Trans R Soc Lond Ser B Biol Sci
364:2027–2045. doi:10.1098/rstb.2008.0284
Thiel M (2011) Chemical communication in peracarid crus-
taceans. In: Breithaupt T, Thiel M (eds) Chemical com-
munication in crustaceans. Springer, Berlin, pp 199–218.
doi:10.1007/978-0-387-77101-4_10
Thompson RC (2015) Microplastics in the marine environment:
sources, consequences and solutions. In: Bergmann M, Gutow
L, Klages M (eds) Marine Anthropogenic Litter. Springer, Cham,
pp 185–200. doi:10.1007/978-3-319-16510-3_7
Thompson RC, Olsen Y, Mitchell RP, Davis A, Rowland SJ, John AW,
McGonigle D, Russell AE (2004) Lost at sea: where is all the
plastic? Science 304:838. doi:10.1126/science.1094559
Turra A, Manzano AB, Dias RJS, Mahiques MM, Barbosa L, Balt-
hazar-Silva D, Moreira FT (2014) Three-dimensional distri-
bution of plastic pellets in sandy beaches: shifting paradigms.
Scientific reports 4: 4435. http://www.nature.com/articles/
srep04435
Ugolini A (1996) Jumping and sun compass in sandhoppers: an anti-
predator interpretation. Ethol Ecol Evol 8:97–106. doi:10.1080/0
8927014.1996.9522937
Ugolini A, Ungherese G, Ciofini M, Lapucci A, Camaiti M (2013)
Microplastic debris in sandhoppers. Estuar Coast Shelf Sci
129:19–22. doi:10.1016/j.ecss.2013.05.026
Ungherese G, Ugolini A (2009) Sandhopper solar orientation as a
behavioural biomarker of trace metals contamination. Environ
Pollut 157:1360–1364. doi:10.1016/j.envpol.2008.11.038
Ungherese G, Cincinelli A, Martellini T, Ugolini A (2012) PBDEs
in the supralittoral environment: the sandhopper Talitrus sal-
tator (Montagu) as biomonitor? Chemosphere 86:223–227.
doi:10.1016/j.chemosphere.2011.09.029
Watts AJ, Lewis C, Goodhead RM, Beckett SJ, Moger J, Tyler CR,
Galloway TS (2014) Uptake and retention of microplastics by the
shore crab Carcinus maenas. Environ Sci Technol 48:8823–8830
Wegner A, Besseling E, Foekema E, Kamermans P, Koelmans A (2012)
Effects of nanopolystyrene on the feeding behavior of the blue
mussel (Mytilus edulis). Environ Toxicol Chem 31:2490–2497
Weis J (2014) Physiological. Springer, Netherlands, Devel-
opmental and Behavioral Effects of Marine Pollution.
doi:10.1007/978-94-007-6949-6
Weiss H, Wilhems A, Mills N, Scotchmer J, Hall P, Lind K, Brekke
T (2000) The Norwegian industry guide to organic geochemi-
cal analyses [online]. http://www.npd.no/engelsk/nigoga/default.
htm. pp. 102
Wildish DJ (1988) Ecology and natural history of aquatic Talitroidea.
Can J Zool 66:2340–2359. doi:10.1139/z88-349
Wong BB, Candolin U (2015) Behavioral responses to changing envi-
ronments. Behav Ecol 26:665–673. doi:10.1093/beheco/aru183
Wright SL, Rowe D, Thompson RC, Galloway TS (2013a) Micro-
plastic ingestion decreases energy reserves in marine worms.
Curr Biol 23:R1031–R1033. doi:10.1016/j.cub.2013.10.068
Wright SL, Thompson RC, Galloway TS (2013b) The physical
impacts of microplastics on marine organisms: a review. Environ
Pollut 178:483–492. doi:10.1016/j.envpol.2013.02.031
A preview of this full-text is provided by Springer Nature.
Content available from Marine Biology
This content is subject to copyright. Terms and conditions apply.
