Archives of Environmental Contamination and Toxicology

https://doi.org/10.1007/s00244-020-00706-1

Short‑Term Exposure to Storm‑Like Scenario Microplastic and Salinity

Conditions Does not Impact Adult Sea Urchin (Arbacia punctulata)
Physiology
Coleen C. Suckling1   · Joëlle Richard2,3

Received: 24 August 2019 / Accepted: 7 January 2020

© Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract
The effects of microplastic pollution on sea urchins has received little attention despite their ecological and economical
importance. This is the first study to focus on adult sea urchins (Arbacia punctulata). These organisms were exposed to
storm-like sediment resuspension of microplastic concentrations (9-μm polystyrene 25,000 spheres L ­ −1) combined with
salinity reductions (salinity 25 vs. 33) associated with high precipitation. Urchins were exposed to these parameters for 24 h
before assessing righting times and for 48 h before assessing oxygen consumption rates. No significant impacts on urchin
physiology were observed showing resilience to short-term exposures of storm-like induced microplastics and salinity. No
microplastic particles blocked the madreporite pores indicating the active removal of particles by cilia and pedicellariae.
Gut tissue samples indicated consumption of microplastics. Studies on more species are urgently required to determine their
responses to plastic pollution to inform management decision-making processes.

In recent years, there has been an increasing focus on assess-
ing the impacts of microplastic pollution on marine organ-
isms. Microplastic loading into the marine environment is
largely sourced from wastewater treatment plants, which
input a wide range of microplastic types and sizes (GES-
AMP 2015, 2016; Lusher et al. 2017; Wolff et al. 2019).
Along with the hydrodynamic and physicochemical forc-
ing of seawater, these microplastics are distributed along
the coast and beyond. During this dispersal, microplastics
with greatest densities due to physical characteristics and/or
the development of surface biofilms sink through the water
column and settle onto surface sediments (GESAMP 2015,
2016; Kazmiruck et al. 2018). Concentrations of micro-
plastics found within coastal sediments vary but have been
recorded to be as high as 25,000 particles ­kg−1 (Kazmiruck
* Coleen C. Suckling
coleensuckling@uri.edu
1 Echinodermata: Echinoidea—a keystone species within
Fisheries, Animal and Veterinary Sciences, University
of Rhode Island, 129 Woodward Hall, 9 East Alumni
Avenue, Kingston, RI, USA
2
Florida Gulf Coast University, FGCU Blvd. South,
10501 Fort Myers, FL, USA
3
Present Address: IFREMER, CNRS, UMR 6308, AMURE,
IUEM, University of Brest, 29280 Plouzane, France
et al. 2018). During major water movement events (e.g.,
storms), seawater turbulence resuspends surface sediments
along with other materials, such as microplastics, integrated
within their matrix. However, the amount resuspended dur-
ing turbulent events (e.g., storms) are currently unknown.
Furthermore, during high precipitation storm events loading
of microplastics into coastal waters from wastewater treat-
ment plants connected to storm water outlets (Wolff et al.
2019) can increase, meaning that benthic animals within
these coastal regions will most likely be exposed to tempo-
rarily high concentrations of suspended microplastics.
Ingestion of microplastics through passive feeding is
evident, but most research has focussed on filter feeding
shellfish and fish species of commercial relevance (Lusher
et al. 2017). There is rich biodiversity in our oceans, and
microplastic pollution is prevalent in all regions sampled so
far (see GESAMP 2015, 2016). Yet, the potential impacts
on many marine organismal groups have still received lit-
tle to no investigation. One of these groups includes the
many coastal marine communities. Sea urchin juveniles
and adults live on the benthos grazing on food materials
meaning that these organisms are at the interface for plastic
exposure, through plastic loading and resuspension dur-
ing events of significant water movement (e.g., storms).
How these organisms respond to plastic pollution is largely

13
Vol.:(0123456789)

unknown. Early work used carboxylate beads as an instru-
ment to study homeostasis on juvenile sea urchins (Fergu-
son 1996). However, more recent literature has focused on
these materials as marine pollutants that may accumulate
inside organisms leading to negative impacts. For example,
microplastic materials, such as polystyrene spherical beads
(PS), have been exposed to embryos and the early stages of
plutei development to investigate the impacts on the sur-
vival and development (Kaposi et al. 2014; Torre et al. 2014;
Messinetti et al. 2018; Martínez-Gómez et al. 2017). While
largely negative, responses varied and depended on the con-
centration of plastic particles used. For example, Martínez-
Gómez et al. (2017) highlighted that P. lividus fertilization
success was reduced by as much as ~ 18–32%, similarly lar-
vae growth was reduced by ~ 40–55% when reared within
extremely high concentrations of PS at concentrations of
­103–105 PS ­mL−1. At much lower concentrations of 1–300
PS ­mL−1, larval responses are much less pronounced with
little impact on the growth of Tripneustes gratilla (Kaposi
et al. (2014). Types of plastic materials utilized also induced
differing responses with virgin plastics inducing ~ 61% more
reductions in Lytechinus variegatus embryo development
compared with weathered beach collected materials (Nobre
et al. 2015).
Sea urchins are osmoconformers with a limited capacity
to cope with large variations in salinity in the surrounding
environment (Freire et al. 2011). Despite some species dem-
onstrating a narrow scope to regulate ions during short-term
diurnal hypo-osmotic conditions, these short-term exposures
can generally lead to negative impacts, such as increased
production of reactive oxygen species, a reduction in oxy-
gen consumption, and mortality (Sabourin and Stickle 1981;
Russell 2013; Honorato et al. 2017). While these have been
investigated to some extent in species, such as Strongylo-
centrotus droebachiensis and Echinometra lucunter, there
remains a significant information gap on how other species
will physiologically respond to short-term salinity changes.
The purpose of this study was to expand our understand-
ing on how microplastics impact sea urchins by focussing
on adults, a stage of the life cycle not yet previously inves-
tigated in the context of marine pollution. A multi-stressor
approach was taken to assess the short-term influence of
storm-like scenarios, which could induce microplastic
resuspension from sediments coupled with salinity changes
associated with high precipitation during storm events. We
assessed responses using oxygen consumption and righting
time as proxies for physiological function. Sea urchins are
osmoconformers, with a narrow scope to regulate ions dur-
ing salinity change events (Vidolin et al. 2007; Russell 2013;
Santos et al. 2013), and use a combination of ciliated lined
tissues and appendages, such as pedicellariae to remove
marine debris from external surfaces (Ruppert & Barnes
1994; Ferguson 1996; Tamori et al. 1996). We hypothesized
13
Archives of Environmental Contamination and Toxicology
that a reduction in the physiological function of these organ-
isms under elevated microplastic and reduced salinity con-
ditions, reflecting an increase in particle removal and ion
regulation efforts.
Materials and Methods
Animal Collection and Maintenance
Arbacia punctulata were hand collected by SCUBA divers
from a depth of 12  m from the Edison Artificial Reef
(26°18.444′ N, 82°13.284′ W) in the Gulf of Mexico from
May 14–16, 2016. The urchins were transported in seawa-
ter in cool boxes and then transferred to holding tanks at
the Florida Gulf Coast University Vester field station for
1–2 days. Thirty-six sea urchins were measured in dupli-
cate for test diameter with Vernier callipers (mm ± 0.1)
and whole wet mass with bench top scales (g ± 0.01) and
then randomly allocated to individual static 6-L beakers
containing 1-µm filtered seawater, gently aerated via a plas-
tic rod. All urchins were found to be significantly similar
in test diameter (TD; mean (± SE) = 31.2 ± 0.2 mm) and
mass (21.61 ± 0.47 g) across all beakers (TD: ­F3,35 = 1.90,
p = 0.150; wet mass: F ­ 3,35 = 1.06, p = 0.379). After alloca-
tion to beakers, the urchins were starved and seawater was
fully exchanged daily (100%). Pumped from the local bay,
seawater required for exchanges was filtered and was stored
in large tanks overnight in advance of use to ensure targeted
temperatures were achieved. The natural ambient photoper-
iod was applied to the study.
The urchins were held under these conditions for 10 days
following the methods described by Lawrence et al. (2003)
to ensure that the gut passage was cleared of food and fecal
particles before the measurement of oxygen consump-
tion. Before water changes, seawater was measured daily
for salinity, temperature, pH, oxygen (WTW Multi 3430
Multiparameter Meter equipped with TetraCon 925 salin-
ity probe, SenTix pH probe, and FDO 925 oxygen optode),
ammonia, nitrate, and nitrite within urchin beakers and new
seawater supplies using aquarium test kits (API: Ammonia
and Nitrite; Nutrafin: Nitrate). Throughout the experiment,
ammonia and nitrite levels were kept at 0 mg L ­ −1, nitrate
−1
levels were kept < 5 mg ­L , and temperature (~ 25.0 °C),
pH (~ 8.3 pH), and oxygen (~ 6.9 mg ­L−1) remained simi-
lar across all beakers (Table 1). During the holding period,
salinity remained similar across all beakers (salinity ~ 33;
Table 1).
Sea Urchin Exposure and Data Collection
Following the 10-day period of starvation, the urchins were
exposed to differing treatment conditions for a period of
Archives of Environmental Contamination and Toxicology
Table 1  Seawater parameters and microplastic concentration counts under which Arbacia punctulata were exposed to for up to 48 h
Treatment Temperature (°C) Holding Salinity
Control 25.0 ± 0.1 33.4 ± 0.0
LS 25.0 ± 0.1 32.7 ± 0.2
MP 25.0 ± 0.1 33.4 ± 0.0
LS + MP 25.0 ± 0.1 32.6 ± 0.2
F-Statistic 0.76
P value 0.555
Absence of subscripted letters indicates no significant differences, differing subscripted letters indicate significant differences
LS low salinity, MP microplastic
up to 48 h, during which they remained unfed. Treatments
consisted of: (1) Control (C) conditions where no changes
to the experimental conditions were made; (2) Low salin-
ity (LS; salinity 25); (3) Presence of microplastics (MP;
25,000 MP ­L−1); and (4) Combination of low salinity (25)
and microplastics (25,000 MP ­L−1; LS + MP). Each treat-
ment comprised of nine individuals each considered an inde-
pendent replicate. Microplastics comprised of fluorescent
polystyrene microspheres 9 µm in diameter (FS06F Bangs
Laboratory Inc., USA) were diluted with 1-µm of filtered
seawater to achieve a working stock solution and were kept
in this form for 8 days. This procedure allowed the plastics
to be washed of any potential leachates and to start build-
ing a biofilm following the suggestions of Martínez-Gómez
et al. (2017). From this stock solution, appropriate volumes
were added to relevant sea urchin beakers using adjustable
pipettes and disposable pipette tips to achieve a concentra-
tion of 25,000 MP ­L−1. This concentration was selected
based on the hypothetical resuspension levels for surface
sediment concentrations (~ 25,000 particles k­ g−1) reported
in Kazmiruck et al. (2018; see Introduction). Concentra-
tions were confirmed by gently mixing seawater within each
replicate and 100-mL subsample removed. The subsample
was then inverted five times and a 1-mL sample was trans-
ferred onto a Sedgewick rafter cell. Counts were conducted
under an inverted fluorescing microscope (Olympus IX73)
by using a hand counter. This procedure was repeated three
times. Between samples, the counting cell was washed with
DI water and checked if it was clear of spheres prior to con-
ducting the next count. Treatments containing the microplas-
tics were confirmed with a mean number of 24,250 polymer
particles ­L−1 (Table 1), demonstrating that they were close
within target concentrations. Low salinity was achieved by
diluting seawater in storage tanks (described above) with
distilled seawater. The targeted salinity of 25 in LS treat-
ments was chosen, beacuse it represents the lowest yet sea-
sonally consistent value experienced in the coastal region
of the Gulf of Mexico coast of Florida (Blakey et al. 2015).
During the experimental period, salinity was significantly
Treatment salinity pH Oxygen (mg L−1) Microplastics
(Number L−1)
33.5 ± 0.1a 8.25 ± 0.01 6.89 ± 0.01 0 ± 0a
25.0 ± 0.0b 8.26 ± 0.01 6.95 ± 0.03 0 ± 0a
33.5 ± 0.1a 8.27 ± 0.01 6.89 ± 0.01 24,250 ± 366b
25.1 ± 0.0b 8.22 ± 0.03 6.93 ± 0.01 24,250 ± 250b
2447.03 1.76 2.59 2851.21
< 0.001 0.153 0.153 < 0.001
lower in the LS treatments (salinity ~ 25) compared with full-
strength salinity treatments (Control and MP; salinity ~ 33;
Table 1). The control and salinity 25 treatments were con-
firmed to contain no polymers demonstrating no contamina-
tion (Table 1).
After a 24-h period of exposure to the treatment condi-
tions, immediately after seawater exchanges occurred the
sea urchins were timed on how quickly they could right
themselves from an inverted to a fully upright position.
The urchins were not measured for righting times after 48 h
exposure to treatments so that minimal disturbance was
made prior to measuring oxygen uptake (see below; Suck-
ling et al. 2015; Morley et al. 2016). These exposure time-
frames reflect major storm durations (Kao and Govindaraju
2007; Cid et al. 2016; Lamjiri et al. 2017).
The rate of oxygen uptake was measured for animals after
48 h exposure to treatments using an oxygen optode closed
chamber system (Presens Fibox-3 Precision Sensing GmbH,
Regensburg, Germany) described in Suckling et al. (2015)
and Morley et al. (2016). The sea urchins were placed into
open individual chambers (750 mL) within the 6-L holding
beakers to prevent aerial exposure and allowed to adjust to
these new conditions for a period of 1 or 2 h. Each chamber
contained a magnetic stirrer separated from the sea urchins
by a mesh platform. After this period, the chambers were
closed and transferred onto benchtop magnetic stirrers to
ensure that seawater within chambers was gently yet well
mixed. Measurements for oxygen consumption were taken
approximately every 5 min and did not exceed a 70% oxy-
gen reduction to minimize stress (Peck and Prothero-Thomas
2002). Blank chambers, containing no sea urchins, were
measured simultaneously for each sea urchin beaker, and the
background oxygen levels were accounted for in sea urchin
respiration data.
Following oxygen uptake measurements, the animals
were weighed and the test diameters measured. Subsamples
of five sea urchins per treatment were then dissected, and the
madreporite and a 1-cm section from the middle of the stom-
ach tract were retained in small Petri dishes. The madreporite
13

was gently washed with 1-µm of filtered seawater to remove
loose microplastic particles. These tissues were then visu-
ally inspected under the fluorescing microscope (described
above) to determine the presence of particles.
Data Handling and Statistical Analysis
Following the assumptions of normality and homogeneity of
variance (p > 0.05), all data were analysed using a one-way
ANOVA in R Studio (2015).
Results
There were no significant differences in the rate of right-
ing time (F (3,21) = 1.32, p = 0.293; Fig. 1a) or oxygen con-
sumption (F (3,30) = 0.64, p = 0.597; Fig. 1b). No microplas-
tic spheres were observed to be lodged within or around or
on the madreporite plate or pores; however, they were found
within the gut tract of the sampled urchins.
Fig. 1  Mean (± 1 SE) righting time (a) and oxygen uptake (b) of
Arbacia punctulata after 24 and 48 h, respectively, exposure to con-
trol conditions, low salinity (LS), the presence of microplastics (MP)
or a combination of both low salinity and microplastics (LS + MP)
13
Archives of Environmental Contamination and Toxicology
Discussion
Short-term exposures to storm-like induced scenarios
of resuspended microplastics and salinity appears to
have no impact on A. punctulata physiology. Thus, they
show good capacities to cope with transient resuspension
events even when under low salinity stress. Unlike Fer-
guson (1996), we did not observe microplastic spheres
being trapped in the pores of the madreporite, nor did we
identify any significant impact on the physiology of these
urchins. The inside diameter of these pores is approxi-
mately 21 μm, which is large enough for our particles to
pass through. However, cilia lining the pore canals can
forcefully exclude particles (Tamori et al. 1996; Ferguson
1996). The microplastics used in the current study could
have been large enough to be detected and redirected from
the madreporite pores. Similarly, it is likely that the com-
bined actions of the pedicellariae (a stalk-like appendage
with microscopic jaws) and surface cilia located exter-
nally across the urchin’s body (Ruppert and Barnes 1994)
removed the microplastic debris from the sea urchin’s body
surface. This action would prevent any potential obstruc-
tions to the surface of the gills, located aborally around
the mouth where the major part of gas exchange occurs.
Ferguson (1996) did not measure the metabolic impact of
the microplastic markers on juvenile Strongylocentrotus
droebachiensis, but the study highlights that exposure to
0.2-μm polymer spheres at an extremely high concentra-
tion of 2.27 × 1010 spheres ­mL−1 can be taken in through
to the water vascular system. Whether this was because the
particles were too small or too dense to allow for selective
removal by cilia, or whether this affected other important
regions, such as the external gills or the overall physiology
of the animal, is currently unknown and would warrant
further investigation into assessing the potential impacts
of microplastic pollution.
Martínez-Gómez et al. (2017) highlighted that the direct
use of virgin microplastics in laboratory-controlled studies
can illicit lethal toxic effects due to leaching of additive/
residual chemicals. These authors recommend washing or
weathering microplastics before toxicity testing to allow
for more realistic environmental conditions. This study
followed these recommendations by soaking the micro-
plastics before use, which may have influenced our results
observing no physiological impact. Our observations did
show that some microplastic spheres were ingested by
adult A. punctulata. Despite our beaker cultures being
well mixed due to aeration (as evidenced by microplastic
confirmation counts), ingestion will have occurred due to
grazing of any spheres located near/on the beaker surface.
Ingestion (and egestion) of microplastics have previously
been observed within sea urchin larvae. For example,
Archives of Environmental Contamination and Toxicology
Messinetti et al. (2018) exposed embryos through to the
onset of plutei development of Paracentrotus lividus to
0.125–25 μg mL−1 of polystyrene spheres (10 μm diam-
eter) and Kaposi et al. (2014) exposed well-developed
plutei Tripneustes gratilla larvae to 1–300 polyethylene
spheres ­mL−1 (10–45 μm diameter). Both studies reported
no significant impact on survival but did report reduc-
tions in larval morphological growth (Kaposi et al. 2014;
Messinetti et al. 2018). Sea cucumbers have been shown to
consume plastics within laboratory conditions (polyvinyl
chloride (PVC) and nylon, 0.25–15 mm size; Graham and
Thompson 2009) and within the field (acrylic and polypro-
pylene fibres; Taylor et al. 2016), but the impacts on the
sea cucumbers physiology remain unknown. At present,
there is a paucity of literature on how other species of
adult sea urchins (and other echinoderm species) respond
to microplastic pollution and the presence of plastics
within sea urchins in the natural environment is currently
unknown. Both of these knowledge gaps urgently require
investigation given the ecological and economical impor-
tance of sea urchins (Pearse 2006; Daggett et al. 2010;
Suckling et al. 2011, 2018).
Wells (1961) surveyed an Estuary in North Carolina
(USA) and found A. punctulata only within regions where
salinity was greater than 30.9 and an absence of them when
salinity was lower. This therefore indicates that these low
salinity conditions are unsuitable for these osmoconform-
ers, and they mobilize to regions of suitable salinity condi-
tions. However, despite our study animals being collected
from a fully marine (salinity ~ 34) site, they demonstrated a
capacity to cope with short-term low salinity conditions of
1–2 days. Psammechinus miliaris crossed between differing
salinity littoral and sublittoral habitats (salinities 20–38) has
been shown to cope with these altered conditions for up to
50 days but are unknown beyond this time frame (Gezelius
1963). Long-term exposure periods (5–14 days) have been
associated with high rates of mortality for other species (S.
droebachiensis and E. lucunter) and despite E. lucunter,
Lytechinus variegatus, and Arbacia lixula exhibiting a nar-
row scope to regulate ions, these have only been assessed
within short-term diurnal hypo-osmotic conditions (Vidolin
et al. 2007; Freire et al. 2011; Russell 2013; Santos et al.
2013). Therefore, any potential for long-term acclimation
of osmoconforming echinoids to reduced salinity conditions
is extremely limited and unlikely but short-term tolerances
are possible. At present, the ion regulatory mechanisms in
low salinity environments remain unknown for A. punctulata
but, given their capacity to cope with low salinities, would
be worth investigating to explain these short-term tolerance
capabilities. This study highlights that the combination of
altered salinity and the presence of microplastics does not
impose any measurable negative impacts on the physiology
of A. punctulata within a short-term storm-like event.
Conclusions
This study is the first to investigate adult urchin physiology
under short-term storm-associated microplastic and salin-
ity changes and shows resilience in A. punctulata. Further
studies are needed on a wider range of sea urchin species
(particularly adults) to determine the short- and long-term
potential impacts of microplastic pollution. Such informa-
tion will be needed for decision-making processes on coastal
plastic pollution.
Acknowledgements  The authors thank the Challenger Society for
Marine Science’s Stepping Stones Bursary for financial support, Flor-
ida Gulf Coast University staff for the use of the Vester field station
facilities, Bob Wasno for animal collections and support with setting up
the aquarium, Brett Sutton for animal husbandry assistance, and Darren
Rumbold for constructive comments on the manuscript.
References
Blakey T, Melesse AM, Rousseaux S (2015) Toward subtropical algal
blooms to freshwater nutrient sources using long term, spatially
distributed, in situ chlorophyll-a record. CATENA 133:119–127
Cid A, Menéndez M, Castanedo S, Abascal AJ, Méndez FJ, Medina R
(2016) Long-term changes in the frequency, intensity and dura-
tion of extreme storm surge events in Southern Europe. Clim Dyn
46:1503–1516
Daggett TL, Pearce CM, Robinson SMC, Chopin T (2010) Does
method of kelp (Saccharina latissimi) storage affect its food
value for promoting somatic growth of juvenile green sea urchins
(Strongylocentrotus droebachiensis)? J Shellfish Res 29:247–252
Ferguson JC (1996) Madreporite function and fluid relationships in sea
urchins. Biol Bull 191:431–440
Freire CA, Santos IA, Vidolin D (2011) Osmolality and ions of the
perivisceral coelomic fluid of the intertidal sea urchin Echinome-
tra lucunter (Echinodermata: Echinoidea) upon salinity and ionic
challenges. Zoologia 28:479–487
GESAMP (Joint Group of Experts on the Scientific Aspects of Marine
Environmental Protection) (2015) In: Kershaw PJ (ed) Sources,
fate and effects of microplastics in the marine environment: a
global assessment. (IMO/FAO/UNESCO-IOC/UNIDO/WMO/
IAEA/UN/UNEP/UNDP Joint Group of Experts on the Scien-
tific Aspects of Marine Environmental Protection). Report Studies
GESAMP No. 90
GESAMP (Joint Group of Experts on the Scientific Aspects of Marine
Environmental Protection). 2016) In: Kershaw PJ, Rochman CM
(eds) Sources, fate and effects of microplastics in the marine
environment: part two of a global assessment. (IMO/FAO/UNE-
SCO-IOC/UNIDO/WMO/IAEA/UN/UNEP/UNDP Joint Group
of Experts on the Scientific Aspects of Marine Environmental
Protection). Report Studies GESAMP No. 93
Gezelius G (1963) Adaptation of the sea urchin Psammechinus mil-
iaris to different salinities. Zoologiska Bidrag Från Uppsala
35:329–337
Graham ER, Thompson JT (2009) Deposit and suspension-feeding sea
cucumbers (Echinodemrata) ingest plastic fragments. J Exp Mar
Biol Ecol 368:22–29
Honorato T, Boni R, Mirella da Silva P, Marques-Santos LF (2017)
Effects of salinity on the immune system cells of the tropical sea
urchin Echinometra lucunter. J Exp Mar Biol Ecol 486:22–31
13

Kao S-C, Govindaraju RS (2007) Probabilistic structure of storm sur-
face runoff considering the dependence between average inten-
sity and storm duration of rainfall events. Water Resources Res
43:W06410
Kaposi KL, Mos B, Kelaher P, Dworjanyn SA (2014) Ingestion of
microplastic has limited impact on a marine larva. Environ Sci
Technol 48:1638–1645
Kazmiruck TN, Kazmiruk VD, Bendell LI (2018) Abundance and
distribution of microplastics within surface sediments of a key
shellfish growing region of Canada. PLoS ONE 13(5):e0196005
Lamjiri MA, Dettinger MD, Ralph FM, Guan B (2017) Hourly storm
characteristics along the U.S. West Coast: role of atmospheric
rivers in extreme precipitation. Geophys Res Lett 44:7020–7028
Lawrence JM, Plank LR, Lawrence AL (2003) The effect of feeding
frequency on consumption of food, absorption efficiency, and
gonad production in the sea urchin Lytechinus variegatus. Comp
Biochem Physiol Part A 134:69–75
Lusher A, Hollman P, Mendoza-Hill J (2017) Microplastics in fisher-
ies and aquaculture. FAO Fisheries and Aquaculture Technical
Paper, 615
Martínez-Gómez C, León VM, Calles S, Gomáriz-Olcina M, Vethaak
AD (2017) The adverse effects of virgin microplastics on the fer-
tilization and larval development of sea urchins. Mar Environ Res
130:69–76
Messinetti S, Mercurio S, Parolini M, Sugni M, Pennati R (2018)
Effects of polystyrene microplastics on early stages of two marine
invertebrates with different feeding strategies. Environ Pollut
237:1080–1087
Morley SM, Suckling CC, Clark MS, Cross EL, Peck LS (2016) Long-
term effects of altered pH and temperature on the feeding energet-
ics of the Antarctic sea urchin, Sterechinus neumayeri. Biodiver-
sity 17:34–45
Nobre CR, Santana MFM, Maluf A, Cortez FS, Cesar A, Pereira CDS,
Turra A (2015) Assessment of microplastic toxicity to embryonic
development of the sea urchin Lytechinus variegatus (Echinoder-
mata: Echinoidea). Mar Pollut Bull 92:99–104
Pearse JS (2006) Ecological role of purple sea urchins. Science
5801:940–941
Peck LS, Prothero-Thomas E (2002) Temperature effects on the metab-
olism of larvae of the Antarctic starfish Odontaster validus using a
novel micro-respirometry method. Mar Biol 141:271–276
13
Archives of Environmental Contamination and Toxicology
RStudio Team (2015) RStudio: Integrated Development for R. RStudio,
Inc., Boston, MA. http://www.rstud​io.com/
Ruppert EE, Barnes RD (1994) Invertebrate Zoology, 6th edn. Brookes/
Cole Thomson Learning, London
Russell MP (2013) Echinoderm responses to variation in salinity. Adv
Mar Biol 66:171–212
Sabourin TD, Stickle WB (1981) Effects of salinity on respiration
and nitrogen excretion in two species of echinoderms. Mar Biol
65:91–99
Santos IA, Castellano GC, Freire CA (2013) Direct relationship
between osmotic and ionic conforming behaviour and tissue water
regulatory capacity in echinoids. Comp Biochem Physiol A Mole-
cul Integr Physiol 162:466–476
Suckling CC, Symonds RC, Kelly MS, Young AJ (2011) The effect
of artificial diets on gonad colour & biomass in the edible sea
urchin Psammechinus miliaris. Aquaculture 318:335–342
Suckling CC, Clark MS, Richard J, Morley SA, Thorne MAS, Harper
EM, Peck LS (2015) Adult acclimation to combined temperature
and pH stressors significantly enhances reproductive outcomes
compared to short-term exposures. J Animal Ecol 84:773–784
Suckling CC, Terrey D, Davies AJ (2018) Optimising stocking density
for the commercial cultivation of sea urchin larvae. Aquaculture
488:96–104
Tamori M, Matsuno A, Takahashi K (1996) Structure and function of
the pore canals of the sea urchin madreporite. Philos Trans R Soc
B Biol Sci 351:659–676
Taylor ML, Gwinnet CG, Robinson LF, Woodhall LC (2016) Plastic
microfibre ingestion by deep-sea organisms. Sci Rep 6:33997
Torre CD, Bergami E, Salvati A, Faleri C, Cirino P, Dawson KA,
Corsi I (2014) Accumulation and embryotoxicity of polystyrene
nanoparticles at early stage of development of sea urchin embryos
Paracentrotus lividus. Environ Sci Technol 48:12302–12311
Vidolin D, Santos IA, Freire CA (2007) Differences in ion. Regula-
tion in the sea urchins Lytechinus variegatus and Arbacia lixula
(Echinodermata: Echinoidea). J Mar Biol Assoc UK 87:769–775
Wells HW (1961) The fauna of oyster beds, with special reference to
the salinity factor. Ecol Monogr 31:239–266
Wolff S, Kerpen J, Prediger J, Barkmann L, Muller L (2019) Determi-
nation of the microplastics emission in the effluent of a municipal
waste water treatment plant using Raman microscopy. Water Res
X 2:100014