Science of the Total Environment 912 (2024) 169276

Contents lists available at ScienceDirect

Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Common types of microdebris affect the physiology of reef-building corals

Jessica Reichert a, b, *, Vanessa Tirpitz a, Katherine Plaza a, Elisabeth Wörner a, c, Luisa Bösser a,
Susanne Kühn d, Sebastian Primpke e, Patrick Schubert a, Maren Ziegler a, Thomas Wilke a
a
Department of Animal Ecology & Systematics, Justus Liebig University, Giessen, Germany
b
Hawai'i Institute of Marine Biology, University of Hawai'i at Mānoa, HI, Kāne'ohe, USA
c
Department of Geoscience, University of Oslo, Oslo, Norway
d
Wageningen Marine Research, Den Helder, the Netherlands
e
Alfred-Wegener-Institute Helmholtz Centre for Polar and Marine Research, Biologische Anstalt Helgoland, Helgoland, Germany

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• The effects of major sources of micro­

debris pollution on coral physiology
were compared.
• Overall, microdebris had only minor
impacts on coral physiology.
• Artificial fibers and tire wear caused the
strongest effect on coral physiology.
• Single polymer and complex micro­
debris caused similar, yet species-
specific effects.
• Species-specific effects might be due to
different feeding behaviors.

A R T I C L E I N F O A B S T R A C T

Editor: Olga Pantos Marine debris, particularly microdebris (< 1 mm) poses a potential threat to marine life, including reef-building
corals. While previous research has mainly focused on the impact of single polymer microplastics, the effects of
Keywords: natural microdebris, composed of a mixture of materials, have not been explored. Therefore, this study aimed to
Artificial clothing fibers assess the effects of different microdebris, originating from major sources of pollution, on reef-building corals.
Tire wear
For this, we exposed two scleractinian coral species, Pocillopora verrucosa and Stylophora pistillata, known to
Secondary microplastic
frequently ingest microplastics, to four types of microdebris in an 8-week laboratory experiment: fragmented
Marine debris
Coral growth environmental plastic debris, artificial fibers from clothing, residues from the automobile sector consisting of tire
Coral photosynthesis wear, brake abrasion, and varnish flakes, a single polymer microplastic treatment consisting of polyethylene
particles, and a microdebris-free control treatment. Specifically, we (I) compared the effects of the different
microdebris on coral growth, necrosis, and photosynthesis, (II) investigated the difference between the micro­
debris mixtures and the exposure to the single polymer treatment, and (III) identified potential mechanisms
causing species-specific effects by contrasting the feeding responses of the two coral species on microdebris and
natural food. We show that the fibers and tire wear had the strongest effects on coral physiology, with
P. verrucosa being more affected than S. pistillata. Both species showed increased volume growth in response to
the microdebris treatments, accompanied by decreased calcification in P. verrucosa. Photosynthetic efficiency of

* Corresponding author at: Hawai'i Institute of Marine Biology, University of Hawaiʻi at Mānoa, HI, Kāne'ohe, USA.
E-mail address: jreichert.sci@gmail.com (J. Reichert).

https://doi.org/10.1016/j.scitotenv.2023.169276
Received 2 September 2023; Received in revised form 4 December 2023; Accepted 8 December 2023
Available online 11 December 2023
0048-9697/© 2023 Elsevier B.V. All rights reserved.
J. Reichert et al.
the symbionts was enhanced in both species. The species-specific physiological responses might be attributed to
feeding reactions, with P. verrucosa responding significantly more often to microdebris than S. pistillata. These
findings highlight the effect of different microdebris on coral physiology and the need for future studies to use
particle mixtures to better mimic naturally occurring microdebris and assess its effect on corals in more detail.
1. Introduction
Since the expansion of organic chemistry in the 1950s, the pollution
of the world's oceans with marine debris – manufactured or processed
material that is discarded in marine and coastal environments (UNEP,
2009) – has become a tremendous problem (Gregory, 2009; Provencher
et al., 2017; Ryan, 2018; Wilcox et al., 2018). Small particles (i.e.,
microdebris) in particular pose a threat to marine life, as they are
frequently ingested by mollusks, fish, or corals (Ding et al., 2022; Huang
et al., 2021; Savoca et al., 2021). Tire wear, artificial fibers from
clothing, and discarded plastic products are major contributors to
pollution (Carr, 2017; Coyle et al., 2020; Sommer et al., 2018; Wagner
et al., 2018). Yet, little is known about the effect of microdebris on reef-
building corals, the main framework builders of coral reef ecosystems.
Most studies to date have shown the adverse influence of single
polymer types, often in the form of unfouled manufactured beads
(Barnes et al., 2009; Paul-Pont et al., 2018; Phuong et al., 2016). Yet,
marine microdebris (i.e., particles between 1 μm and 1 mm in size)
occurs as a mixture in a variety of types and shapes (Galgani et al., 2015;
Hartmann et al., 2019; Kroon et al., 2018; UNEP, 2009). The most
obvious source of microdebris is plastic litter of everyday products that
enters the ocean and degrades into smaller particles over time, consis­
tent with our classic understanding of secondary microplastics
(Andrady, 2011; Hidalgo-Ruz et al., 2012). It includes polyethylene
(PE), polypropylene (PP), polyethylene terephthalate (PET), polyamide
(PA), and polyvinyl chloride (PVC), with PE being one of the most
common particle types found (Andrady, 2011; Kühn et al., 2018).
Another major source of marine microdebris is artificial fibers from
clothing, which are released during the washing process and mainly
consist of polyester, acrylic, PP, PE, and PA (Boucher and Friot, 2017;
Browne et al., 2011; Siegfried et al., 2017). Traffic-related residues, such
as tire wear or break abrasion, also contribute substantially to marine
microdebris, but are often underestimated or omitted in monitoring
approaches, due to their inconsistent classification as microplastic
(Jeong et al., 2022; Rødland et al., 2022; Siegfried et al., 2017).
Reef-building corals – the ecosystem engineers of coral reefs – have
been found to be affected by microplastics (reviewed in Huang et al.,
2021). Exposure to microplastics is often associated with subtle but
negative effects on growth and calcification (Chapron et al., 2018;
Hankins et al., 2021; Reichert et al., 2019). Occasionally, compromised
coral health, such as bleaching or necrosis, is observed after prolonged
exposure or under high pollution scenarios (Reichert et al., 2019, 2018;
Syakti et al., 2019). Further, microplastic exposure has been found to
impact the associated photosymbionts, affecting their photosynthetic
rate and efficiency (Chapron et al., 2018; Hankins et al., 2021; Mendrik
et al., 2021; Reichert et al., 2019). The physiological impacts are often
attributed to the handling and ingestion of particles, which has been
frequently observed (Allen et al., 2017; Hall et al., 2015) and is sus­
pected to affect their feeding behavior (Chapron et al., 2018; Savinelli
et al., 2020). These effects on feeding coincide with elevated energetic
needs, caused by mucus production for cleaning from the particles, as
well as overall increased stress and immune responses of the coral (Chen
et al., 2022; Lanctôt et al., 2020; Tang et al., 2018). However, the effects
of microplastics are species-specific and some species, such as Porites
spp. or Stylophora spp. appear to be less affected than others, such as
Pocillopora spp. or Acropora spp. (Mendrik et al., 2021; Mouchi et al.,
2019; Reichert et al., 2019). Reasons for the species-specific differences
are still largely unknown but might be attributed to differential feeding
behavior, particle recognition, or colony shape (Hankins et al., 2022;
2
Science of the Total Environment 912 (2024) 169276
Martin et al., 2019; Rades et al., 2022; Reichert et al., 2022).
Observations on the effects of microplastics on reef-building corals
have mostly been made under controlled exposure to particles of a single
plastic polymer, with standardized shape and size. Yet, little is known
about how the effects of microplastics of individual polymers on reef-
building corals compare to the effects of microdebris, which is found
as a complex mixture in natural environments (reviewed in Huang et al.,
2021). Thus, the major goal of this study was to assess the effect of
microdebris, originating from major sources of ocean pollution, on reef-
building corals. These mixtures comprised fragmented plastic debris
from the beach, artificial fibers from clothing, and residues from the
automobile sector, consisting of tire wear, brake abrasion, and varnish
flakes. We compared the effects of microdebris exposure to a single-type
microplastic treatment consisting of polyethylene and a microdebris-
free control treatment. Two scleractinian coral species (Pocillopora ver­
rucosa (Ellis & Solander, 1786) and Stylophora pistillata (Esper, 1792))
were used as test organisms. These ecologically similar species both
belong to the Pocilloporidae family, but are known to be differentially
affected by microplastics in their physiology (Lanctôt et al., 2020;
Reichert et al., 2021, 2018). Since impacts on coral physiology might be
linked to particle detection and handling, influencing the frequency of
microplastic ingestion and, consequently, the overall effects, we inves­
tigated the feeding responses of the corals to the tested microdebris.
Specifically, we (I) compared the effects of different microdebris
mixtures on coral growth, necrosis, and photosynthesis, (II) investigated
the difference between the microdebris mixtures and the exposure to the
single polymer treatment, and (III) identified potential mechanisms
causing species-specific effects by contrasting the feeding responses of
the two reef-building coral species on microdebris and natural food.
2. Material and methods
2.1. Experimental design and replication
The study assessed the effects of different types of common micro­
debris on the two scleractinian coral species Pocillopora verrucosa and
Stylophora pistillata (experimental overview: Fig. 1). These species both
have small corallite sizes (P. verrucosa: 0.3–0.7 mm and S. pistillata:
0.9–1.4 mm), are presumed to be sensitive to environmental stressors,
and have been shown to frequently interact with and regularly ingest
microplastics (Lanctôt et al., 2020; Reichert et al., 2018). The micro­
debris treatments were selected to represent major sources of pollution
(Agamuthu et al., 2019). These are secondary marine microplastics
derived from fragmented plastic debris from the beach (treatment:
‘beach’), an assortment of artificial fibers from clothing (treatment: ‘fi­
bers’), residues from the automobile sector consisting of tire wear, brake
abrasion, and varnish flakes (treatment: ‘tire wear’), and a single poly­
mer exposure with polyethylene (treatment: ‘PE’). The average size of
the microdebris varied depending on the treatment within a range of
350 to 1000 μm, which is within the size range for particles commonly
consumed by corals (Houlbrèque and Ferrier-Pagès, 2009).
Physiological responses of corals to the microdebris treatments were
examined in an 8-week exposure study. The experiment was conducted
in 15 tanks, each with a volume of 40 L (n = 3 tanks per treatment). For
this, six mother colonies were used per species (colony origin and CITES
numbers are given in Table S1). One fragment from each colony was
placed in each of the 15 tanks resulting in n = 18 replicates per treat­
ment and species.
J. Reichert et al.
Fig. 1. Experimental design. a) The study tested the effects of the microdebris
treatments ‘beach’, ‘fibers’, ‘tire wear’, and the single polymer treatment ‘PE’
on the two reef-building coral species Pocillopora verrucosa and Stylophora pis­
tillata. b) The effects on growth, necrosis, and photosynthesis were assessed
after 4 and 8 weeks of an exposure experiment (I). The feeding responses to the
different particle types were studied in feeding trials (II). c) The exposure
experiment was conducted in 15 recirculating 40 L tanks. Six fragments per
species originating from different colonies were placed in each tank. The 3D
model illustrates the technical setup that allowed for continuous water circu­
lation while retaining particles within the tanks: 1. Water inflow; 2. Inflow
filter; 3. Temperature sensor; 4. Hanging coral fragments; 5. Heater; 6. Turn­
over pump; 7. Wavemaker pump; 8. Outflow filters; 9. Water outflow.
Feeding responses of the tested coral species to the four types of
microdebris (beach, fibers, tire wear, and PE) as well as copepods,
serving as natural control feed, were assessed in direct feeding trials,
performed in separate feeding chambers under a stereomicroscope. Fifty
feeding responses were assessed in one fragment from each of the six
colonies, resulting in n = 300 feeding offers per particle type and
species.
2.2. Coral fragment preparation
Corals were fragmented 6–9 weeks before the experiment to allow
for tissue recovery in the cutting areas. Corals were cut from terminal
branches into fragments of 3–5 cm and tied to fishing lines to avoid the
buildup of detritus on the colonies and decrease algal overgrowth. To
control for position effects, replicates from the same colony were placed
in the same spot in each tank.
3
Science of the Total Environment 912 (2024) 169276
2.3. Technical setup and maintenance
This experiment was conducted in the Ocean2100 facility at Justus
Liebig University Giessen. The experimental tanks (n = 15, Fig. 1) were
part of a closed laboratory setup, containing 2300 L artificial seawater
(salt: Instant Ocean, Aquarium Systems, France). The setup contained a
technical tank, fitted with a protein skimmer and a calcium reactor and
other tanks harboring reef organisms. The experimental tanks were fil­
led with 38 L of seawater (salinity: 35) and connected to the system at an
exchange rate of 78 L h− 1. The outflows of the tanks were equipped with
two self-made 65-μm filters to retain the microdebris within the tanks
and allow for a biofilm to form on the particles. Incoming water was
filtered before entering the tanks through a mesh (mesh size: 65 μm) to
minimize contamination through algae or detritus as well as potential
cross-contamination with microdebris from the connected system.
Light was provided at an intensity of 120 μmol photons m− 2 s− 1
(Apogee Quantum Flux MP-200, Apogee Instruments, USA; measuring
range: 410–655 nm, PAR) with a 10:14 h light:dark photoperiod (four
SunaECO LED Lighting Strips per tank, Tropical Marine Centre, United
Kingdom). Water flow in the tanks was created with a wavemaker pump
generating horizontal pulsating currents (easySTREAM pro Wavemaker
Pump, ES-18, Aqualight GmbH, Germany) and a turnover pump (Sub­
marine Water Pump, Resun S-700, Resun, China) generating vertical
currents to submerge floating debris, which resulted in a flow velocity of
3.8 cm s− 1 (OTT MF pro, HydroMet, Germany). Water temperatures
were maintained at 27 ± 0.3 ◦ C using feedback-controlled titanium
heaters (Schego Heater 300 W, Protection class IP 68, SCHEGO Schemel
& Goetz GmbH & Co KG, Germany) coupled to temperature sensors
(GHL Temp Sensor digital, GHL Advanced Technology GmbH & Co. KG,
Germany) and GHL aquarium computers (ProfiLux 3 and ProfiLux 4,
GHL Advanced Technology GmbH & Co. KG, Germany).
Gastropods (12 × Turbo sp. and 2 × Euplica sp.) were included in
each tank to reduce algal growth. Corals were fed daily with copepods
(~0.5 g per tank, Calanoide Copepoden, Zooschatz, Germany) and
amino acids were added to the water column (~0.5 mL amino acid
mixture per tank, Pohl's Xtra special, Korallenzucht.de Vertriebs GmbH,
Germany). All maintenance activities were carried out so that micro­
debris remained in the tank, e.g., if filters were cleaned, they were rinsed
above the tanks before being removed. Further details on the technical
setup and maintenance can be found in Supplementary Material and
Methods.
2.4. Microdebris exposure treatments
To represent secondary marine microplastics, plastic debris was used
(treatment: ‘beach’; Fig. 2a). The plastic was collected on a beach in
Texel, The Netherlands, and fragmented by cryogenic milling, resulting
in a representative mix of 60.9 % polyethylene, 27.7 % polypropylene,
3.1 % polyamide, 1.9 % polyurethane, 1.7 % polystyrene, 0.9 % poly­
vinyl chloride, 0.5 % polyethylene terephthalate, 0.2 % ethylene-vinyl
acetate, 0.1 % ethylene-vinyl acetate, and 3.1 % unidentified particles
(% by mass, details on the collected mixture are provided in Kühn et al.,
2018). The particles were sieved to a particle size >100 μm. The upper
limit was maintained and not further sieved, due to the limited amount
of debris available, resulting in a mean particle length of 346 ± 240 μm
and a mean particle width of 184 ± 126 μm.
To represent a naturally occurring mixture of fibers, synthetic fabrics
were used (treatment: ‘fibers’; Fig. 2b). Fibers were produced from
clothing, i.e., a grey pullover consisting of 70 % acrylic and 30 %
polyamide as well as a black and a green fleece, both made of 100 %
polyester, manually cut into small pieces, resulting in a mean length of
1006 ± 840 μm and a mean width of 16 ± 4 μm. The fibers were mixed
to consist of 67 % Polyester, 23 % acrylic, and 10 % polyamide to mimic
natural occurrences in the ocean (Browne et al., 2011).
To represent residues from the automobile sector, tire wear particles,
brake abrasion, and varnish flakes were swept from a cart track
J. Reichert et al.
Fig. 2. Types of microdebris used in the experiment: a) Secondary marine
microplastics, composed of fragmented plastic debris (treatment: ‘beach’), b)
artificial fibers from clothing (treatment: ‘fibers’), c) residues from the auto­
mobile sector, consisting of tire wear, brake abrasion, and varnish flakes
(treatment: ‘tire wear’), and d) polyethylene particles (treatment: ‘PE’).
(treatment: ‘tire wear’; Fig. 2c). Carts were at most 12 months old, built
with a hydraulic brake system, and equipped with wheels from Dunlop
(Cart Tires, Goodyear Dunlop Tires Germany GmbH, Germany). Parti­
cles were strained with a metal sieve (stainless steel ISO 3310-1, Joa­
chim Edinger Industrievertretungen, Germany) to 100–355 μm,
resulting in a mean particle length of 583 ± 235 μm and a mean particle
width of 218 ± 71 μm.
To represent a treatment commonly used in previous experimental
approaches, a single polymer reference with polyethylene (PE) micro­
plastic particles was included (treatment: ‘PE’; Fig. 2d), which is one of
the most common polymers in the marine environment (Nie et al., 2019;
Patterson et al., 2020; Saliu et al., 2018). Black polyethylene particles of
irregular shape (Novoplastik Produktions- und Vertriebs-GmbH, Ger­
many) were used as in previous studies (Reichert et al., 2019, 2018).
Particles were strained to 100–355 μm, resulting in a mean particle
length of 371 ± 112 μm and a mean particle width of 226 ± 70 μm.
Although microdebris sizes differ significantly depending on the treat­
ment, their mean lengths, ranging between 350 and 1000 μm, all falls
into the size spectrum corals commonly feed on (Houlbrèque and Fer­
rier-Pagès, 2009).
2.5. Microdebris preparation and concentration
Particles were incubated for at least two days in seawater to initiate
biofilm formation on the surface and ease submerging in the water. For
this, 0.4 g of particles were incubated with 10 mL of seawater in 15 mL
falcon tubes for each tank. The exposure was standardized by mass and
the incubated particles were added to each tank, equivalent to ~10 mg
per L and resulting in a target concentration of ~200 particles per L in
each treatment. Microdebris concentrations were monitored and main­
tained over the course of the experiment, by adding particles when
necessary (e.g., due to debris removal during tank maintenance, inges­
tion, and overgrowth by the corals). The concentration of microdebris in
each tank was determined once a week. For this, 100 mL of water was
taken with a dropper pipette from the water surrounding the corals (n =
3 per tank). Each sample was vacuum filtered onto a separate 8 μm
cellulose filter (Whatman filter papers Grade 540, General Electric
4
Science of the Total Environment 912 (2024) 169276
Healthcare Life Sciences, United States). Debris was counted under a
stereomicroscope and extrapolated to assess the concentration as par­
ticles per L. Although water flow in the tanks was optimized to distribute
all debris types equally in the water column, they exhibited different
buoyancy and behavior in the water (e.g., tire wear and beach particles
tended to sink to the bottom, while fibers and PE particles rather
accumulated at the surface). This resulted in slightly different debris
concentrations (particles per L) in the water column, depending on the
treatment (beach: 86 ± 63, fibers: 228 ± 206, tire wear: 66 ± 50, and
PE: 242 ± 126 particles per L, mean ± SD, Fig. S1). Fibers and PE
polymer identities were confirmed by FTIR (Fig. S2). The particle
composition of the beach treatment is characterized by Kühn et al.
(2018). Identification of tire wear particles could not be included due to
technical limitations.
2.6. Growth measurements and necrosis
To study the physiological response of the coral host to exposure to
the different microdebris, growth in tissue surface area, skeletal volume,
and calcification was measured. Tissue surface area and volume of the
coral fragments were assessed at the beginning, and after 4 and 8 weeks
of the experiment via 3D scanning (Artec Spider 3D with Artec Studio
11, Artec Europe, Luxembourg, settings see Table S2) following estab­
lished procedures (Reichert et al., 2016). Briefly, fragments were
mounted on toothpicks and scanned in air in two full rotations with the
handheld scanner. The sensitivity of the scanner was set at 60 %. For
tissue surface area determination, bleached or necrotic tissue was
removed from the model, so that only healthy coral surface remained. To
study coral tissue necrosis, the difference between the total surface area
of each coral fragment and its living tissue surface area was calculated
and expressed as percentage of the total tissue surface area. Models were
exported as .obj files and surface area and volume were calculated in
MeshLab Visual Computing Lab-ISTI-CNR (v.1.3.4 В, 2014) using the
‘compute geometric measures’ tool. Coral calcification was assessed
using buoyant weight measurements (Davies, 1989). For this, coral
fragments were weighed with a precision balance (Kern KB 360-3N,
KERN & Sohn GmbH, Germany, precision: 0.001 g) in a separate 18 L
tank. The change in buoyant weight was converted to dry weight using
an aragonite density of 2.93 g cm− 3.
2.7. Photosynthesis and respiration of the coral holobiont
Rates of photosynthesis and respiration of the coral holobiont were
measured in individual temperature-controlled incubations, conducted
in glass jars with 1050 mL water volume (Weck, Germany). Coral
fragments were processed colony-wise (n = 15 fragments from each
species) together with six control incubations without coral fragments.
Oxygen was measured before and after the incubations using an optical
oxygen probe (FDO 925-3) coupled to a multiparameter probe (Multi
3620 IDS SET G, WTW, Germany). Net photosynthesis was measured in
light (162 ± 9 μmol photons m− 2 s− 1) during daytime (2 h into the
photoperiod). Respiration was measured after light incubations in
darkness. Incubations (both light and dark) lasted 90 min after 4 weeks
and 60 min after 8 weeks, to account for the increased fragment size and
avoid oxygen saturation. Differences in oxygen values were normalized
to water volume and the duration of the incubation, and corrected for
photosynthesis/respiration in the water by subtracting mean measure­
ments of the control incubations. Gross photosynthesis was calculated as
the sum of net photosynthesis and respiration values.
2.8. Photosynthetic efficiency of symbionts
The photosynthetic efficiency of the photosymbionts was determined
using a Pulse-Amplitude-Modulation fluorometer (PAM, Ralph and
Gademann, 2005) at the beginning and after 4 and 8 weeks of the
experiment. Data was collected with the ‘PAM-2500 Portable
J. Reichert et al.
Chlorophyll Fluorometer’ (Walz GmbH, Germany) 5 mm above and at
an angle of 60◦ to the coral tissue using a distance clip. PAM settings
were set to measure stable fluorescence levels (F, Table S3). Effective
quantum yield (ΔF/Fm′) was measured for each fragment during day­
time (6 h into the photoperiod, n = 3 per fragment). Maximum quantum
yield (Fv/Fm) was measured after dark acclimation at the end of the day
(after 40 min of darkness, n = 1 per fragment). Rapid light curves (RLC)
were generated to assess the maximum relative electron transport rate
(rETRmax), the minimum saturating irradiance (Ek), and the efficiency of
light capture in the light-limited phase (α). The RLCs consisted of suc­
cessive measurements of the effective quantum yield (Fv/Fm) under
ambient light, where light intensity increased in 11 steps (0, 4, 29, 99,
196, 361, 617, 979, 1384, 1661, 2013 μmol photons m− 2 s− 1) lasting 10
s each. Hyperbolic tangent functions (Jassby and Platt, 1976), which
included an exponent for photoinhibition at high irradiances (Platt et al.,
1980), were fitted to each curve to extract rETRmax, Ek, and α. RLCs were
measured during daytime (3 h after light until 2 h before darkness).
2.9. Feeding response to microdebris
Feeding responses of the coral fragments to the four types of
microdebris (beach, fibers, tire wear, and PE) as well as copepods as a
natural control feed were assessed in additional coral fragments that
were not included in the tank experiment (n = 6 per species). Coral
fragments were cut from the six colonies as described above and
mounted to self-made concrete bases to ease the handling in the feeding
trials. Particles were manually offered to the coral fragments in indi­
vidual feeding chambers (200 mL) under a stereomicroscope (Leica
Microsystems GmbH, Leica EZ4, Germany). The microdebris was
sampled from the treatment tanks to provide particles covered with a
biofilm. The natural control feed (Calanoide Copepoden, Zooschatz,
Germany) was defrosted in seawater for 1 h before feeding. Five coral
polyps were consecutively fed per fragment in 10 repetitions conducted
over two days, resulting in n = 300 feeding trials per treatment per
species. Using forceps, the particle was placed in contact with a tentacle
for 5 s and the responses to, the uptake, and egestion of the particle were
assessed. Reactions were classified as positive if the particle remained
attached to the coral tentacle and the time of the reaction was recorded.
Reactions were classified as negative if the particle was not retained and
released. Particle uptake was classified as positive if the particle was
completely ingested by the coral mouth. Coral polyps that ingested
particles were observed for up to 2 h to record a potential egestion,
which was defined as complete upon release from the tentacles and
mesenterial filaments. The time the particle was ingested was noted
accordingly.
2.10. Statistical analyses
We performed all data processing and analyses in the R statistical
environment (v.3.6.1; R Core Team, 2019). Differences in physiological
responses between the microdebris treatments (beach, fibers, tire wear,
and PE) and the control were assessed for each species (P. verrucosa and
S. pistillata) and timepoint (after 4 and 8 weeks) using linear mixed-
effects models (for surface area growth, volume growth, calcification,
net photosynthesis, respiration, gross photosynthesis, effective quantum
yield (Y(II)), maximum quantum yield (Fv/Fm), maximum relative
electron transport rate (rETRmax), minimum saturating irradiance (Ek),
and efficiency of light capture (α)) and generalized mixed effects models
(for necrotic tissue surface area). Models were constructed with treat­
ment as a fixed factor and colony ID set as a random factor, on scale- or
log-transformed data, followed by holm-adjustment for multiple testing.
Details on the model specification are given in Tables S4–6. Differences
in physiological responses between the microdebris mixtures (beach,
fibers, tire wear) and the single polymer PE were assessed for each
species over both time points using linear mixed-effects models. Models
were constructed with treatment as fixed factor and timepoint and
5
Science of the Total Environment 912 (2024) 169276
colony ID set as a random factor, on scale or log-transformed data, fol­
lowed by holm-adjustment for multiple testing. Differences in polyp
behavior (i.e., reaction, uptake, and egestion) between the microdebris
treatments (beach, fibers, tire wear, and PE) and natural food (co­
pepods) for each species were tested with pairwise Fisher's exact tests,
followed by holm-adjustment for multiple testing. Differences in inter­
action times between microdebris types and food in cases of positive
reactions, uptake events, and rejection events were tested with Wilcox
rank-sum tests. Differences in coral feeding behavior (i.e., reactions,
uptake, and egestion) between Pocillopora verrucosa and Stylophora pis­
tillata to the different microdebris treatments (beach, fibers, tire wear,
and PE) and natural food (copepods) were tested with Fisher's exact
tests.
3. Results
3.1. Effects of microdebris mixtures on growth rates and necrosis
The microdebris mixtures differed in their effects on coral growth
rates (Figs. 3a, b, S3, Table S4, linear mixed-effects models). While most
microdebris treatments had no significant impacts after 4 and 8 weeks,
both enhancing and decreasing effects on growth rates were observed
occasionally. Volume growth of P. verrucosa was three-fold higher in the
fibers treatment after 8 weeks of exposure than in the control (fibers:
0.012 ± 0.011 cm3 cm− 2 vs. control: 0.004 ± 0.012 cm3 cm− 2, p =
0.006). In S. pistillata volume growth in the PE treatment was 36 %
higher after 4 weeks of exposure than in the control (PE: 0.03 ± 0.029
cm3 cm− 2 vs. control: 0.022 ± 0.028 cm3 cm− 2, p = 0.050). Calcification
of P. verrucosa in the beach and the fibers treatment decreased by 40 %
and 32 %, respectively, compared to the control, after 8 weeks of
exposure (beach: 8.59 ± 7.80 mg cm− 2 and fibers: 9.71 ± 7.62 vs.
control: 14.2 ± 9.55 mg cm− 2, p = 0.004 and p = 0.026, respectively,
Fig. 3b). Calcification of S. pistillata was not affected and the microdebris
treatments had no effects on growth in surface area at any time point
(Fig. S3, p > 0.05). Necrosis was not affected significantly (Fig. 3c).
3.2. Changes in photosynthesis and respiration
Most microdebris treatments had no significant effect on the
photosynthetic productivity of the tested coral species (Figs. 3d, S4,
Table S5, linear mixed-effects models). Only net and gross photosyn­
thesis of P. verrucosa were 22 % and 15 % higher in the PE treatment
after 4 weeks in comparison to the control (PE: 32.7 ± 11.7 μg O2 cm− 2
h− 1 vs. control: 26.6 ± 11.2 μg O2 cm− 2 h− 1, p = 0.005 and PE: 46.8 ±
13.4 μg O2 cm− 2 h− 1 vs. control: 39.9 ± 11.7 μg O2 cm2 h− 1, p = 0.015,
respectively). The effects were similar, but less pronounced after 8
weeks (p = 0.052 and p = 0.064, respectively). Respiration was also not
affected significantly (Fig. S4, p > 0.05).
3.3. Changes in photosynthetic efficiency
More impacts were observed on parameters relating to the photo­
synthetic efficiency of the associated photosymbionts of P. verrucosa and
S. pistillata, which was enhanced by the exposure to microdebris (Figs. 4,
S5, S6, and S7, Table S6, linear mixed-effects models). For P. verrucosa,
microdebris caused small but significant increases of ~2 % in effective
quantum yield (Y(II); beach: 0.615 ± 0.034, p = 0.025, fibers: 0.614 ±
0.029, p = 0.025, and tire wear: 0.618 ± 0.029, p = 0.002 vs. control:
0.604 ± 0.029) after 8 weeks of exposure. Similarly, the efficiency of
light capture was enhanced (α; beach: 0.244 ± 0.019, p = 0.048, fibers:
0.245 ± 0.025, p = 0.035, and tire wear: 0.245 ± 0.018, p = 0.035 vs.
control: 0.234 ± 0.022) after 8 weeks of exposure. Further, the fibers
treatment caused an increased relative electron transport rate (rETRmax;
fibers: 122 ± 25.2 vs. control: 101 ± 21.2, p = 0.006) and reduced
minimum saturating irradiance (Ek; fibers: 499 ± 93.3 vs. control: 429
± 78.9, p = 0.015) after 8 weeks of exposure. In contrast, fewer
J. Reichert et al. Science of the Total Environment 912 (2024) 169276

Fig. 3. Effects of microdebris treatments (beach, fibers, tire wear, and PE) compared to the control (no microplastics added) on coral growth (volume, and calci­
fication), necrosis, and net photosynthesis for P. verrucosa and S. pistillata after 4 and 8 weeks. Data are displayed as box-and-whisker plots with raw data points; lines
indicate medians, boxes indicate the first and third quartile, and whiskers indicate ±1.5 IQR. Significant differences between the control and the microdebris
treatments are derived from linear mixed effects models or generalized linear mixed effects models followed by holm-adjusted posthoc comparison (n = 18) and are
defined as p < 0.001 (***), p < 0.01 (**), and p < 0.05 (*).

parameters of the photosynthetic efficiency of the photosymbionts of
S. pistillata were affected by the exposure to microdebris. The exposure
to tire wear caused an increase of ~4 % in effective quantum yield both
after 4 and 8 weeks of exposure (Y(II); tire wear: 0.607 ± 0.033, p =
0.035 vs. control: 0.585 ± 0.035, p < 0.001 and tire wear: 0.602 ±
0.037 vs. control: 0.58 ± 0.035, p = 0.010, respectively). The exposure
to fibers caused an increase of ~3 % in effective quantum yield after 4
weeks of exposure (fibers: 0.600 ± 0.032 vs. control: 0.585 ± 0.035, p =
0.030), which was no longer evident after 8 weeks (p = 0.766).
3.4. Difference between single polymer and complex microdebris
treatments
Overall, the effects of the single polymer treatment PE on the tested
12 physiological response variables of the corals did not differ signifi­
cantly from those of the three complex microdebris treatments (Fig. 5a,
Permutational Multivariate Analysis of Variance, p = 0.615, Table S7).
Comparing the effects of the PE treatment to the three complex micro­
debris treatments on the individual physiological parameters reveals
parameter- and species-specific differences. PE had less pronounced

6
J. Reichert et al. Science of the Total Environment 912 (2024) 169276

Fig. 4. Photosynthetic efficiency of P. verrucosa and S. pistillata after 8 weeks of exposure to the different microdebris treatments (beach, fibers, tire wear, PE) and a
microplastic-free control. a) Rapid light curves constructed from rETR measured at increasing PAR intensities after 8 weeks of exposure. b) Effects of microdebris
treatments in comparison to the control on photosynthetic efficiency (effective quantum yield: Y(II), maximum quantum yield: Fv/Fm, maximum relative electron
transport rate: rETRmax, minimum saturation irradiance: Ek, and efficiency of light capture: α) of P. verrucosa and S. pistillata after 4 and 8 weeks. Statistical dif­
ferences (z-value) between the control and the microdebris treatments are illustrated as heatmap with higher values (blue) indicating positive effects and lower
values (red) indicating negative effects compared to the control. Significant differences are marked with asterisks, defined as p < 0.001 (***), p < 0.01 (**), and p <
0.05 (*), and derived from linear mixed-effects models followed by holm-adjusted posthoc comparison (n = 18).

effects on effective quantum yield than the other microdebris treat­
ments, but stronger effects on net photosynthesis (Fig. 5b, Table S8,
Linear mixed effects models). Further, the differences occurred mainly
in P. verrucosa, and were less pronounced for S. pistillata.
3.5. Feeding responses to different microdebris
Reaction, uptake, and egestion of corals differed between the
microdebris (beach, fibers, tire wear, and PE) and the natural food
(copepods), (Fig. 6, Table S9). P. verrucosa responded significantly more
often to PE (13 %), tire wear (11 %), and beach particles (9 %) than to
fibers (3 %); (Fisher's exact test, PE: p < 0.001, tire wear: p < 0.001,
beach: p = 0.019). S. pistillata responded similarly to all debris types, in
~5 % of the cases. Overall, the microdebris elicited significantly less
frequent responses from P. verrucosa and S. pistillata compared to their
response to natural food (92 % and 79 %, respectively, Fisher's exact
test, p < 0.001). However, both species handled microdebris signifi­
cantly longer (P. verrucosa: 49 ± 237 s and S. pistillata: 72 ± 316 s) than
natural food particles (P. verrucosa: 5 ± 6 s and S. pistillata: 5 ± 7 s;
Wilcox test, both p < 0.001).
Of 300 PE particles offered to P. verrucosa three particles were
ingested, of which two were egested after 10 s and 5 min, respectively.
S. pistillata ingested only one fiber, which was egested after 13 s. In
contrast, most of the copepods were ingested (~86 %), which was
significantly higher than the ingestion of microdebris (Fisher's exact test,
p < 0.001). Natural food particles were generally taken up within 5 ± 2 s

7
J. Reichert et al. Science of the Total Environment 912 (2024) 169276

Fig. 5. Effects of the single polymer treatment PE in comparison to the three

complex microdebris treatments (beach, fibers, and tire wear). a) Principal
component analyses (PCA) are constructed using 12 physiological parameters
(growth in surface area, growth in volume, calcification, Y(II), Fv/Fm, rETRmax,
Ek, α, net photosynthesis, respiration, and gross photosynthesis) of P. verrucosa
and S. pistillata. b) Statistical differences (z-values) between the PE treatment
and the complex microdebris treatments are illustrated as heatmap with higher
values (blue) indicating increasing effects and lower values (red) indicating
decreasing effects compared to the PE treatment. Statistically significant dif­
ferences are marked with an asterisk, defined as p < 0.001 (***), p < 0.01 (**),
and p < 0.05 (*) and derived from linear mixed-effects models followed by
holm-adjusted posthoc comparison (n = 18).

by both species. In contrast, the uptake of microdebris took much longer

for P. verrucosa (6 ± 1 min, n = 3; Wilcox test, p = 0.026, Table S10).
Natural food particles were not released after ingestion in any case.
P. verrucosa reacted significantly more often to microdebris than
S. pistillata (Fisher's exact test, p < 0.001, Table S11). Specifically,
P. verrucosa reacted significantly more often to tire wear and PE than
S. pistillata (Fisher's exact test, p = 0.001 and p = 0.044, respectively).
Both P. verrucosa and S. pistillata reacted equally often to natural food
particles (~55 %), yet P. verrucosa ingested significantly more than
S. pistillata (92 % vs. 79 % Fisher's exact test, p > 0.050).

4. Discussion

Microdebris occurs in complex mixtures in coral reefs, yet experi­

mental approaches to date have focused on the effects of single polymers
on stony corals. This is the first study that investigated the effects of
complex microdebris mixtures. While most microdebris types had no
significant physiological effects, parameter- and species-specific effects
occurred in some of the treatments. Overall, the fibers and the tire wear
treatment had the strongest effects, and P. verrucosa was more affected
than S. pistillata. Positive effects of the microdebris treatments were
observed on volume growth in both species, accompanied by decreased
calcification rates in P. verrucosa. Both species responded with an
upregulation in photosynthesis but showed no signs of compromised
health. In comparison, the single polymer treatment PE and the complex
microdebris treatments had similar, yet again parameter- and species-
specific effects on coral physiology. The two species also differed in
their feeding responses to the particles, where P. verrucosa reacted
significantly more often to the microdebris than S. pistillata.

4.1. Microdebris treatments have differential effects on coral physiology

In some cases, microdebris caused increased growth in skeletal vol­

ume in both species. Specifically, volume growth of P. verrucosa was
increased in the fibers treatment while calcification decreased in the
fibers and beach treatment. This might indicate an overgrowth of par­
ticles, as observed in previous studies (Hierl et al., 2021; Reichert et al.,
2022, 2018), potentially modifying skeletal structure and leading to
increased growth in volume despite decreased calcification. In contrast,
photosynthetic rates remained largely unaffected by the exposure to
microdebris. Stronger effects were observed in the photosynthetic effi­
ciency of the associated photosymbionts, which was enhanced in both
species by the exposure to microdebris. These observations correspond
to enhanced photosynthetic efficiency of corals exposed to single poly­
mer particles (Lanctôt et al., 2020; Reichert et al., 2019), but their cause
remains a subject of speculation. This upregulation might be a mecha­
nism to compensate for impaired feeding success and associated loss of
energy. It appears to successfully mitigate the impacts of microdebris as
the exposure had no effects on surface growth and coral health (i.e.,
necrosis). Another reason for the altered photochemistry might be that
the presence of microdebris might have subtle impacts on the light
conditions (both intensity and/or spectral composition), which remains
to be assessed.

(caption on next column) 8

J. Reichert et al.
Overall, the microdebris treatments caused only occasional, minor
impacts on the physiology of the tested coral species, which were often
masked by the large biological variation between colonies. This is in line
with previous studies on the effects of microplastics on corals exposed to
moderate concentrations over the timeframe of weeks to months
(Reichert et al., 2021, 2019). This suggests that the concentration tested
here only constitutes a minor, sublethal stressor for corals, which seem
to possess mechanisms to cope with the exposure over the tested time­
frame. Yet, some specific effects occurred and artificial fibers from
clothing, in particular, induced the most changes in coral physiology.
Reasons for this might be that fibers frequently entangle on the coral
colonies, and cleaning mechanisms that might be effective for micro­
debris fragments fail to work (Hierl et al., 2021; Oldenburg et al., 2021;
Rades et al., 2022; Reichert et al., 2018). Once fibers are entangled,
leaching chemicals might be directly transferred to the neighboring
tissue (Aminot et al., 2020; Montano et al., 2020; Saliu et al., 2019). If
the exposure is prolonged over several months, it might cause necrosis
(Hierl et al., 2021; Reichert et al., 2019). This has, however, not been
observed during the 8 weeks of exposure in this study. Rather it
appeared that fibers, which could not be removed by the corals, were
overgrown, causing increased volume growth. The stronger effects of
these treatments observed in this study might be partly caused by the
higher amount of fibers in the water column (Fig. S1). However,
P. verrucosa responded significantly less often to fibers than to frag­
ments, which suggests that the negative effects are not caused by the
reaction to and the ingestion of fibers, but rather by the entanglement
and potentially resulting interferences (i.e., movement impairments of
polyps, mechanical disturbance or abrasion, and toxin or pathogen
Fig. 6. Feeding responses of P. verrucosa and S. pistillata to natural food (copepods) and microdebris (beach, fibers, tire wear, and PE). a) Frequency of reaction to,
uptake, and egestion of copepods and microdebris are shown as bar charts with positive events in dark and negative events in light color, as % of all trials (n = 300
offered particles per species and food type). b) Reactions of both species to the different particles. Arrows indicate the interacting polyp. Scale bars: 500 μm.
9
Science of the Total Environment 912 (2024) 169276
transfer to the coral surface). Tire wear and other residues from the
automobile sector also caused several effects, specifically on the
photosynthetic efficiency of the symbionts. This can hint towards a
chemical leaching (Carrasco-Navarro et al., 2022; Jeong et al., 2022),
especially as the tire wear particles, which seemed to sink to the ground
due to their negative buoyancy, resulted in the lowest concentration of
particles in the water column. The major constituents of tire wear are
synthetic and natural rubber, and vulcanization agents such as sulfur,
zinc, polyaromatic hydrocarbons, and thiazoles (Wagner et al., 2018).
Tire wear has been shown to leach considerable amounts of these sub­
stances, which are known to be toxic to corals and other organisms
(Halle et al., 2020; Ouédraogo et al., 2021) and have been identified to
exhibit a higher toxicity than other plastic polymers (Sørensen et al.,
2023). In contrast, the effect of the beach treatment appeared rather
low, comparable to the impact of the PE treatment. These findings are
supported by the observation that the corals responded as often to the
beach particles as to all other fragments. Further, this could be explained
by the fact that the beach treatment primarily consisted of PE (~60 %,
Kühn et al., 2018) and that the treatment consisted of environmental
microdebris that had been collected from the seaside, where their
chemical load had likely already reduced over time.
4.2. Single polymer treatments are representative of complex microdebris
types but differ in specifics
The PE treatment had no consistently different effect compared to
the mixed microdebris treatments. Yet parameter- and species-specific
differences occurred. In particular, when exposed to PE, P. verrucosa
J. Reichert et al.
showed no upregulation in photosynthetic efficiency as observed for
other microdebris treatments, but in photosynthesis. This indicates that
corals respond differently to complex microdebris compared to single
polymer microdebris. This is likely due to the different physical and
chemical properties found in the microdebris treatments (i.e., density,
shape, polymer composition, and additives). Although the results from
single polymer experiments were not generally different, future labo­
ratory experiments should rather use mixed microdebris to mimic
naturally occurring microdebris and assess the effects of microdebris on
corals in more detail.
4.3. Species-specific effects might be related to particle detection
The effects of the microdebris treatments were species-specific,
which is in line with previous observations on single polymer expo­
sure experiments (Mendrik et al., 2021; Mouchi et al., 2019; Reichert
et al., 2021, 2019). Overall, the physiology of S. pistillata was less
strongly affected by the microdebris exposure than P. verrucosa. To date,
reasons for species-specific effects are poorly understood but hint to­
wards differences in colony morphology and feeding strategy of the
coral species (Hankins et al., 2022; Martin et al., 2019; Rades et al.,
2022; Reichert et al., 2022). Here we find that particle detection and
handling might be a reason for the observed differences. The interaction
might hinder feeding and be energetically costly. This might also explain
why the upregulation in photosynthetic efficiency is more pronounced
(i.e., affected more parameters) in P. verrucosa, although it occurred
earlier (after 4 weeks) in S. pistillata. The lower reaction rates of
S. pistillata to microdebris than of P. verrucosa suggest differences in
particle detection mechanisms between the species. These may underlie
the differences observed here, with better compensation strategies to
environmental impacts in S. pistillata, as previously observed with other
stressors, such as thermal stress and bleaching (Kvitt et al., 2011;
Meziere et al., 2022).
4.4. Implications for coral reef conservation
Taken together, we found that microdebris had minor impacts on
reef-building corals in our study, yet, the fibers and tire wear treatments
impacted multiple physiological parameters. Although these effects had
no detrimental impacts on coral health, they might add up to the already
existing stress posed on coral reef ecosystems and may push coral reef
communities past their tipping points (Mendrik et al., 2021; Reichert
et al., 2021). This highlights the urgency for stronger regulations of
microdebris influxes from land (Trudsø et al., 2022). While methods to
effectively remove these residues from our wastewater are already
available, they need to be implemented more broadly to protect coral
reefs from the effects of microdebris. Thus, we call for prioritized mea­
sures to reduce residues from artificial clothes and the automobile
sector. This should be considered in both our individual actions as well
as policy-making.
4.5. Conclusions
Our study is the first to present the effects of common microdebris
types from major sources of anthropogenic pollution on two reef-
building coral species. We show that residues from artificial clothes
and the automobile sector had the strongest effects on the tested corals
and that the effects of these mixtures might be more pronounced than
those of single polymers. Although single polymer treatments appeared
overall representative to investigate the effects of microdebris pollution,
the underlying physiological mechanisms of how corals respond to
naturally occurring complex microdebris might not be resolved, as
different mixtures seem to cause different responses. Reasons for
species-specific differences in the effects of microdebris on corals might
be attributed to different feeding strategies and the capability to reject
unwanted particles. However, this warrants further evidence. Our study
10
Science of the Total Environment 912 (2024) 169276
underlines the urgency to implement effective wastewater treatments
and address the major sources of pollution for microdebris.
CRediT authorship contribution statement
Jessica Reichert: Conceptualization, Formal analysis, Investigation,
Writing – original draft, Writing – review & editing. Vanessa Tirpitz:
Conceptualization, Formal analysis, Investigation, Writing – review &
editing. Katherine Plaza: Investigation. Elisabeth Wörner: Investiga­
tion. Luisa Bösser: Investigation. Susanne Kühn: Resources, Writing –
review & editing. Sebastian Primpke: Investigation. Patrick Schubert:
Conceptualization, Resources, Writing – review & editing. Maren Zie­
gler: Conceptualization, Resources, Writing – review & editing. Thomas
Wilke: Conceptualization, Resources, Writing – review & editing.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Data availability
The analyzed data and 3D models of the studied corals are available
at figshare.com: https://doi.org/10.6084/m9.figshare.23983125.v1.
Acknowledgments
We thank Birgit Zettl and Christina Anding from Justus Liebig Uni­
versity Giessen, Germany for the animal care and maintenance. The
study was conducted as part of the ‘Ocean 2100’ global change simu­
lation project of the Colombian-German Center of Excellence in Marine
Sciences (CEMarin). The ‘beach’ treatment material was prepared
within the JPI Oceans ‘PLASTOX’ project.
Use of generative AI
During the preparation of the graphical abstract, the authors used
Canva Text-to-image in order to generate an illustration of a coral reef.
After using this tool, the authors reviewed the content as needed and
take full responsibility for the content of the publication.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.scitotenv.2023.169276.
References
Agamuthu, P., Mehran, S.B., Norkhairah, A., Norkhairiyah, A., 2019. Marine debris: a
review of impacts and global initiatives. Waste Manage. Res. 37, 987–1002. https://
doi.org/10.1177/0734242X19845041.
Allen, A.S., Seymour, A.C., Rittschof, D., 2017. Chemoreception drives plastic
consumption in a hard coral. Mar. Pollut. Bull. 124, 198–205. https://doi.org/
10.1016/j.marpolbul.2017.07.030.
Aminot, Y., Lanctôt, C., Bednarz, V., Robson, W.J., Taylor, A., Ferrier-Pagès, C.,
Metian, M., Tolosa, I., 2020. Leaching of flame-retardants from polystyrene debris:
bioaccumulation and potential effects on coral. Mar. Pollut. Bull. 151, 1–7. https://
doi.org/10.1016/j.marpolbul.2019.110862.
Andrady, A.L., 2011. Microplastics in the marine environment. Mar. Pollut. Bull. 62,
1596–1605. https://doi.org/10.1016/j.marpolbul.2011.05.030.
Barnes, D.K. a, Galgani, F., Thompson, R.C., Barlaz, M., 2009. Accumulation and
fragmentation of plastic debris in global environments. Philos. Trans. R. Soc., B 364,
1985–1998. https://doi.org/10.1098/rstb.2008.0205.
Boucher, J., Friot, D., 2017. Primary microplastics in the oceans: a global evaluation of
sources. IUCN Int. Union Conserv. Nat. https://doi.org/10.2305/IUCN.CH.2017.01.
en.
Browne, M.A., Crump, P., Niven, S.J., Teuten, E., Tonkin, A., Galloway, T., Thompson, R.,
2011. Accumulation of microplastic on shorelines worldwide: sources and sinks.
Environ. Sci. Technol. 45, 9175–9179. https://doi.org/10.1021/es201811s.
J. Reichert et al.
Carr, S.A., 2017. Sources and dispersive modes of micro-fibers in the environment.
Integr. Environ. Assess. Manag. 13, 466–469. https://doi.org/10.1002/ieam.1916.
Carrasco-Navarro, V., Nuutinen, A., Sorvari, J., Kukkonen, J.V.K., 2022. Toxicity of tire
rubber microplastics to freshwater sediment organisms. Arch. Environ. Contam.
Toxicol. 82, 180–190. https://doi.org/10.1007/s00244-021-00905-4.
Chapron, L., Peru, E., Engler, A., Ghiglione, J.F., Meistertzheim, A.L., Pruski, A.M.,
Purser, A., Vétion, G., Galand, P.E., Lartaud, F., 2018. Macro- and microplastics
affect cold-water corals growth, feeding and behaviour. Sci. Rep. 8, 15299. https://
doi.org/10.1038/s41598-018-33683-6.
Chen, Y.T., Ding, D.S., Lim, Y.C., Singhania, R.R., Hsieh, S., Chen, C.W., Hsieh, S.L.,
Dong, C. Di, 2022. Impact of polyethylene microplastics on coral Goniopora columna
causing oxidative stress and histopathology damages. Sci. Total Environ. 828
https://doi.org/10.1016/j.scitotenv.2022.154234.
Coyle, R., Hardiman, G., Driscoll, K.O., 2020. Microplastics in the marine environment: a
review of their sources, distribution processes, uptake and exchange in ecosystems.
Case Stud. Chem. Environ. Eng. 2, 100010 https://doi.org/10.1016/j.
cscee.2020.100010.
Davies, S.P., 1989. Short-term growth measurements of corals using an accurate buoyant
weighing technique. Mar. Biol. 101, 389–395. https://doi.org/10.1007/
BF00428135.
Ding, J., Sun, Y., He, C., Li, J., Li, F., 2022. Towards risk assessments of microplastics in
bivalve mollusks globally. J. Mar. Sci. Eng. https://doi.org/10.3390/jmse10020288.
Galgani, F., Hanke, G., Maes, T., 2015. Global distribution, composition and abundance
of marine litter. In: Bergmann, M., Gutow, L., Klages, M. (Eds.), Marine
Anthropogenic Litter. Springer, Cham Heidelberg New York Dordrecht London,
pp. 29–56. https://doi.org/10.1007/978-3-319-16510-3.
Gregory, M.R., 2009. Environmental implications of plastic debris in marine settings-
entanglement, ingestion, smothering, hangers-on, hitch-hiking and alien invasions.
Philos. Trans. R. Soc. B Biol. Sci. 364, 2013–2025. https://doi.org/10.1098/
rstb.2008.0265.
Hall, N.M., Berry, K.L.E., Rintoul, L., Hoogenboom, M.O., 2015. Microplastic ingestion by
scleractinian corals. Mar. Biol. 162, 725–732. https://doi.org/10.1007/s00227-015-
2619-7.
Halle, L.L., Palmqvist, A., Kampmann, K., Khan, F.R., 2020. Ecotoxicology of micronized
tire rubber: past, present and future considerations. Sci. Total Environ. 706, 135694
https://doi.org/10.1016/j.scitotenv.2019.135694.
Hankins, C., Moso, E., Lasseigne, D., 2021. Microplastics impair growth in two Atlantic
scleractinian coral species, Pseudodiploria clivosa and Acropora cervicornis. Environ.
Pollut. 275, 116649 https://doi.org/10.1016/j.envpol.2021.116649.
Hankins, C., Raimondo, S., Lasseigne, D., 2022. Microplastic ingestion by coral as a
function of the interaction between calyx and microplastic size. Sci. Total Environ.
810, 152333 https://doi.org/10.1016/j.scitotenv.2021.152333.
Hartmann, N.B., Hüffer, T., Thompson, R.C., Hassellöv, M., Verschoor, A., Daugaard, A.
E., Rist, S., Karlsson, T., Brennholt, N., Cole, M., Herrling, M.P., Hess, M.C., Ivleva, N.
P., Lusher, A.L., Wagner, M., 2019. Are we speaking the same language?
recommendations for a definition and categorization framework for plastic debris.
Environ. Sci. Technol. 53, 1039–1047. https://doi.org/10.1021/acs.est.8b05297.
Hidalgo-Ruz, V., Gutow, L., Thompson, R.C., Thiel, M., 2012. Microplastics in the marine
environment: a review of the methods used for identification and quantification.
Environ. Sci. Technol. 46, 3060–3075. https://doi.org/10.1021/es2031505.
Hierl, F., Wu, H.C., Westphal, H., 2021. Scleractinian corals incorporate microplastic
particles: identification from a laboratory study. Environ. Sci. Pollut. Res. https://
doi.org/10.1007/s11356-021-13240-x.
Houlbrèque, F., Ferrier-Pagès, C., 2009. Heterotrophy in tropical scleractinian corals.
Biol. Rev. 84, 1–17. https://doi.org/10.1111/j.1469-185X.2008.00058.x.
Huang, W., Chen, M., Song, B., Deng, J., Shen, M., Chen, Q., Zeng, G., Liang, J., 2021.
Microplastics in the coral reefs and their potential impacts on corals: a mini-review.
Sci. Total Environ. 762, 143112 https://doi.org/10.1016/j.scitotenv.2020.143112.
Jassby, A.D., Platt, T., 1976. Mathematical formulation of the relationship between
photosynthesis and light for phytoplankton. Limnol. Oceanogr. 21, 540–547.
https://doi.org/10.4319/lo.1976.21.4.0540.
Jeong, Y., Lee, S., Woo, S.H., 2022. Chemical leaching from tire wear particles with
various treadwear ratings. Int. J. Environ. Res. Public Health 19. https://doi.org/
10.3390/ijerph19106006.
Kroon, F.J., Motti, C.E., Jensen, L.H., Berry, K.L.E., 2018. Classification of marine
microdebris: a review and case study on fish from the Great Barrier Reef, Australia.
Sci. Rep. 8, 1–15. https://doi.org/10.1038/s41598-018-34590-6.
Kühn, S., van Oyen, A., Booth, A.M., Meijboom, A., van Franeker, J.A., 2018. Marine
microplastic: preparation of relevant test materials for laboratory assessment of
ecosystem impacts. Chemosphere 213, 103–113. https://doi.org/10.1016/j.
chemosphere.2018.09.032.
Kvitt, H., Rosenfeld, H., Zandbank, K., Tchernov, D., 2011. Regulation of apoptotic
pathways by Stylophora pistillata (anthozoa, pocilloporidae) to survive thermal stress
and bleaching. PloS One 6. https://doi.org/10.1371/journal.pone.0028665.
Lanctôt, C.M., Bednarz, V.N., Melvin, S., Jacob, H., Oberhaensli, F., Swarzenski, P.W.,
Ferrier-Pagès, C., Carroll, A.R., Metian, M., 2020. Physiological stress response of the
scleractinian coral Stylophora pistillata exposed to polyethylene microplastics.
Environ. Pollut. 263, 114559 https://doi.org/10.1016/j.envpol.2020.114559.
Martin, C., Corona, E., Mahadik, G.A., Duarte, C.M., 2019. Adhesion to coral surface as a
potential sink for marine microplastics. Environ. Pollut. 255, 113281 https://doi.
org/10.1016/j.envpol.2019.113281.
Mendrik, F.M., Henry, T.B., Burdett, H., Hackney, C.R., Waller, C., Parsons, D.R.,
Hennige, S.J., 2021. Species-specific impact of microplastics on coral physiology.
Environ. Pollut. 269, 116238 https://doi.org/10.1016/j.envpol.2020.116238.
Meziere, Z., Rich, W.A., Carvalho, S., Benzoni, F., Morán, X.A.G., Berumen, M.L., 2022.
Stylophora under stress: a review of research trends and impacts of stressors on a
11
Science of the Total Environment 912 (2024) 169276
model coral species. Sci. Total Environ. 816, 151639 https://doi.org/10.1016/j.
scitotenv.2021.151639.
Montano, S., Seveso, D., Maggioni, D., Galli, P., Corsarini, S., Saliu, F., 2020. Spatial
variability of phthalates contamination in the reef-building corals Porites lutea,
Pocillopora verrucosa and Pavona varians. Mar. Pollut. Bull. 155, 111117 https://doi.
org/10.1016/j.marpolbul.2020.111117.
Mouchi, V., Chapron, L., Peru, E., Pruski, A.M., Meistertzheim, A.-L., Vétion, G.,
Galand, P.E., Lartaud, F., 2019. Long-term aquaria study suggests species-specific
responses of two cold-water corals to macro-and microplastics exposure. Environ.
Pollut. 253, 322–329. https://doi.org/10.1016/j.envpol.2019.07.024.
Nie, H., Wang, J., Xu, K., Huang, Y., Yan, M., 2019. Microplastic pollution in water and
fish samples around Nanxun Reef in Nansha Islands, South China Sea. Sci. Total
Environ. 696, 134022 https://doi.org/10.1016/j.scitotenv.2019.134022.
Oldenburg, K.S., Urban-Rich, J., Castillo, K.D., Baumann, J.H., 2021. Microfiber
abundance associated with coral tissue varies geographically on the Belize
Mesoamerican Barrier Reef System. Mar. Pollut. Bull. 163 https://doi.org/10.1016/
j.marpolbul.2020.111938.
Ouédraogo, D.Y., Delaunay, M., Sordello, R., Hédouin, L., Castelin, M., Perceval, O.,
Domart-Coulon, I., Burga, K., Ferrier-Pagès, C., Multon, R., Guillaume, M.M.M.,
Léger, C., Calvayrac, C., Joannot, P., Reyjol, Y., 2021. Evidence on the impacts of
chemicals arising from human activity on tropical reef-building corals; a systematic
map. Environ. Evid. 10, 1–18. https://doi.org/10.1186/s13750-021-00237-9.
Patterson, J., Jeyasanta, K.I., Sathish, N., Edward, J.K.P., Booth, A.M., 2020. Microplastic
and heavy metal distributions in an Indian coral reef ecosystem. Sci. Total Environ.
744, 140706 https://doi.org/10.1016/j.scitotenv.2020.140706.
Paul-Pont, I., Tallec, K., Gonzalez-Fernandez, C., Lambert, C., Vincent, D., Mazurais, D.,
Zambonino-Infante, J.-L., Brotons, G., Lagarde, F., Fabioux, C., Soudant, P.,
Huvet, A., 2018. Constraints and priorities for conducting experimental exposures of
marine organisms to microplastics. Front. Mar. Sci. 5, 1–22. https://doi.org/
10.3389/fmars.2018.00252.
Phuong, N.N., Zalouk-Vergnoux, A., Poirier, L., Kamari, A., Châtel, A., Mouneyrac, C.,
Lagarde, F., 2016. Is there any consistency between the microplastics found in the
field and those used in laboratory experiments? Environ. Pollut. https://doi.org/
10.1016/j.envpol.2015.12.035.
Platt, T., Gallegos, C.L., Harrison, W.G., 1980. Photoinhibition of photosynthesis in
natural assemblages of marine phytoplankton. J. Mar. Res. (U. S. A.) 38, 687–701.
Provencher, J.F., Bond, A.L., Avery-Gomm, S., Borrelle, S.B., Bravo Rebolledo, E.L.,
Hammer, S., Kühn, S., Lavers, J.L., Mallory, M.L., Trevail, A., Van Franeker, J.A.,
2017. Quantifying ingested debris in marine megafauna: a review and
recommendations for standardization. Anal. Methods 9, 1454–1469. https://doi.
org/10.1039/c6ay02419j.
R Core Team, 2019. R: A Language and Environment for Statistical Computing [WWW
Document]. URL. http://www.r-project.org/.
Rades, M., Schubert, P., Wilke, T., Reichert, J., 2022. Reef-building corals do not develop
adaptive mechanisms to better cope with microplastics. Front. Mar. Sci. 9, 1–9.
https://doi.org/10.3389/fmars.2022.863187.
Ralph, P.J., Gademann, R., 2005. Rapid light curves: a powerful tool to assess
photosynthetic activity. Aquat. Bot. 82, 222–237. https://doi.org/10.1016/j.
aquabot.2005.02.006.
Reichert, J., Schellenberg, J., Schubert, P., Wilke, T., 2016. 3D scanning as a highly
precise, reproducible, and minimally invasive method for surface area and volume
measurements of scleractinian corals. Limnol. Oceanogr. Methods 14, 518–526.
https://doi.org/10.1002/lom3.10109.
Reichert, J., Schellenberg, J., Schubert, P., Wilke, T., 2018. Responses of reef building
corals to microplastic exposure. Environ. Pollut. 237, 955–960. https://doi.org/
10.1016/j.envpol.2017.11.006.
Reichert, J., Arnold, A.L., Hoogenboom, M.O., Schubert, P., Wilke, T., 2019. Impacts of
microplastics on growth and health of hermatypic corals are species-specific.
Environ. Pollut. 254, 113074 https://doi.org/10.1016/j.envpol.2019.113074.
Reichert, J., Tirpitz, V., Anand, R., Bach, K., Knopp, J., Schubert, P., Wilke, T.,
Ziegler, M., 2021. Interactive effects of microplastic pollution and heat stress on reef-
building corals. Environ. Pollut. 290, 118010 https://doi.org/10.1016/j.
envpol.2021.118010.
Reichert, J., Arnold, A.L., Hammer, N., Miller, I.B., Rades, M., Schubert, P., Ziegler, M.,
Wilke, T., 2022. Reef-building corals act as long-term sink for microplastic. Glob.
Chang. Biol. 28, 33–45. https://doi.org/10.1111/gcb.15920.
Rødland, E.S., Lind, O.C., Reid, M.J., Heier, L.S., Okoffo, E.D., Rauert, C., Thomas, K.v.,
Meland, S., 2022. Occurrence of tire and road wear particles in urban and peri-urban
snowbanks, and their potential environmental implications. Sci. Total Environ. 824,
153785 https://doi.org/10.1016/j.scitotenv.2022.153785.
Ryan, P.G., 2018. Entanglement of birds in plastics and other synthetic materials. Mar.
Pollut. Bull. 135, 159–164. https://doi.org/10.1016/j.marpolbul.2018.06.057.
Saliu, F., Montano, S., Garavaglia, M.G., Lasagni, M., Seveso, D., Galli, P., 2018.
Microplastic and charred microplastic in the Faafu Atoll, Maldives. Mar. Pollut. Bull.
136, 464–471. https://doi.org/10.1016/j.marpolbul.2018.09.023.
Saliu, F., Montano, S., Leoni, B., Lasagni, M., Galli, P., 2019. Microplastics as a threat to
coral reef environments: detection of phthalate esters in neuston and scleractinian
corals from the Faafu Atoll, Maldives. Mar. Pollut. Bull. 142, 234–241. https://doi.
org/10.1016/j.marpolbul.2019.03.043.
Savinelli, B., Vega Fernández, T., Galasso, N.M., D’Anna, G., Pipitone, C., Prada, F.,
Zenone, A., Badalamenti, F., Musco, L., 2020. Microplastics impair the feeding
performance of a Mediterranean habitat-forming coral. Mar. Environ. Res. 155
https://doi.org/10.1016/j.marenvres.2020.104887.
Savoca, M.S., McInturf, A.G., Hazen, E.L., 2021. Plastic ingestion by marine fish is
widespread and increasing. Glob. Chang. Biol. 27, 2188–2199. https://doi.org/
10.1111/gcb.15533.
J. Reichert et al.
Siegfried, M., Koelmans, A.A., Besseling, E., Kroeze, C., 2017. Export of microplastics
from land to sea. A modelling approach. Water Res. 127, 249–257. https://doi.org/
10.1016/j.watres.2017.10.011.
Sommer, F., Dietze, V., Baum, A., Sauer, J., Gilge, S., Maschowski, C., Gieré, R., 2018.
Tire abrasion as a major source of microplastics in the environment. Aerosol Air
Qual. Res. 18, 2014–2028. https://doi.org/10.4209/aaqr.2018.03.0099.
Sørensen, L., Gomes, T., Igartua, A., Lyngstad, I.L., Almeida, A.C., Wagner, M., Booth, A.
M., 2023. Organic chemicals associated with rubber are more toxic to marine algae
and bacteria than those of thermoplastics. J. Hazard. Mater. 458 https://doi.org/
10.1016/j.jhazmat.2023.131810.
Syakti, A.D., Jaya, J.V., Rahman, A., Hidayati, N.V., Raza’i, T.S., Idris, F.,
Trenggrono, M., Doumenq, P., Chou, L.M., 2019. Bleaching and necrosis of staghorn
coral (Acropora formosa) in laboratory assays: immediate impact of LDPE
microplastics. Chemosphere 228, 528–535. https://doi.org/10.1016/j.
chemosphere.2019.04.156.
12
Science of the Total Environment 912 (2024) 169276
Tang, J., Ni, X., Zhou, Z., Wang, L., Lin, S., 2018. Acute microplastic exposure raises
stress response and suppresses detoxification and immune capacities in the
scleractinian coral Pocillopora damicornis. Environ. Pollut. 243, 66–74. https://doi.
org/10.1016/j.envpol.2018.08.045.
Trudsø, L.L., Nielsen, M.B., Hansen, S.F., Syberg, K., Kampmann, K., Khan, F.R.,
Palmqvist, A., 2022. The need for environmental regulation of tires: challenges and
recommendations. Environ. Pollut., 119974 https://doi.org/10.1016/J.
ENVPOL.2022.119974.
UNEP, 2009. Marine Litter: A Global Challenge, Unep 2009 (Nairobi).
Wagner, S., Hüffer, T., Klöckner, P., Wehrhahn, M., Hofmann, T., Reemtsma, T., 2018.
Tire wear particles in the aquatic environment - a review on generation, analysis,
occurrence, fate and effects. Water Res. 139, 83–100. https://doi.org/10.1016/j.
watres.2018.03.051.
Wilcox, C., Puckridge, M., Schuyler, Q.A., Townsend, K., Hardesty, B.D., 2018.
A quantitative analysis linking sea turtle mortality and plastic debris ingestion. Sci.
Rep. 8, 1–11. https://doi.org/10.1038/s41598-018-30038-z.