ArticlePDF Available

Abstract and Figures

Rising sea temperatures and increasing pollution threaten the fate of coral reefs and millions of people who depend on them. Some reef-building corals respond to thermal stress and subsequent bleaching with increases in heterotrophy, which may increase the risk of ingesting microplastics. Whether this heterotrophic plasticity affects microplastics ingestion or whether ingesting microplastics affects heterotrophic feeding in corals is unknown. To determine this, two coral species, Montipora capitata and Pocillopora damicornis, were exposed to ambient (~27 °C) and increased (~30 °C) temperature and then fed microplastics, Artemia nauplii, or both. Following thermal stress, both species significantly reduced feeding on Artemia but no significant decrease in microplastics ingestion was observed. Interestingly, P. damicornis only ingested microplastics when Artemia were also present, providing evidence that microplastics are not selectively ingested by this species and are only incidentally ingested when food is available. As the first study to examine microplastics ingestion following thermal stress in corals, our results highlight the variability in the risk of microplastics ingestion among species and the importance of considering multiple drivers to project how corals will be affected by global change.
Content may be subject to copyright.
1
SCIENTIFIC REPORTS | (2019) 9:18193 | https://doi.org/10.1038/s41598-019-54698-7
www.nature.com/scientificreports
Microplastics ingestion and
heterotrophy in thermally stressed
corals
Jeremy B. Axworthy & Jacqueline L. Padilla-Gamiño
Rising sea temperatures and increasing pollution threaten the fate of coral reefs and millions of people
who depend on them. Some reef-building corals respond to thermal stress and subsequent bleaching
with increases in heterotrophy, which may increase the risk of ingesting microplastics. Whether this
heterotrophic plasticity aects microplastics ingestion or whether ingesting microplastics aects
heterotrophic feeding in corals is unknown. To determine this, two coral species, Montipora capitata and
Pocillopora damicornis, were exposed to ambient (~27 °C) and increased (~30 °C) temperature and then
fed microplastics, Artemia nauplii, or both. Following thermal stress, both species signicantly reduced
feeding on Artemia but no signicant decrease in microplastics ingestion was observed. Interestingly,
P. damicornis only ingested microplastics when Artemia were also present, providing evidence that
microplastics are not selectively ingested by this species and are only incidentally ingested when food
is available. As the rst study to examine microplastics ingestion following thermal stress in corals, our
results highlight the variability in the risk of microplastics ingestion among species and the importance
of considering multiple drivers to project how corals will be aected by global change.
Reef building corals (Scleractinia) are increasingly challenged by a suite of anthropogenic stressors including
pollution and rising sea temperatures due to climate change1,2. ese stressors threaten the fate of coral reefs
and the ecosystem services they provide which support the livelihoods of tens of millions of people worldwide3.
Model projections forecast that more than 75% of coral reefs will be subjected to annual severe bleaching before
2070 due to thermal stress alone4, but the fate of corals may be worsened when they face additional stressors5,6.
Recent evidence suggests that microplastics (plastic particles or bers <5 mm), may negatively aect corals710.
To date, however, no studies have looked at the potential for thermal stress to aect microplastics ingestion by
reef-building corals.
Under normal conditions, most reef-building corals acquire the majority of their energy from a symbiotic
partnership with photosynthetic dinoagellates in the family Symbiodiniaceae11, while less energy is generally
derived from heterotrophic feeding on zooplankton1214. When thermally stressed, Symbiodiniaceae are expelled
from corals (bleaching) leading to a net decrease in autotrophic energy acquisition15,16. If elevated temperatures
persist, corals deplete their energy reserves and can starve, but if the temperature reduces before the corals’ energy
reserves are exhausted, Symbiodiniaceae can be reacquired and the coral may recover1719.
Some corals respond to thermal stress and subsequent bleaching by increased heterotrophy which shis the
corals’ reliance from energy derived from photosynthesis to energy derived from zooplankton prey, an adapta-
tion termed heterotrophic plasticity14,2023. While the underlying mechanisms and timing of this response are
still unclear, increased carbon acquisition from heterotrophy can help corals maintain daily metabolic costs until
Symbiodiniaceae can be reacquired. In contrast, other corals decrease their feeding rate during, or following,
thermal stress2224 which may negatively impact their resilience. For corals that display heterotrophic plasticity,
increased feeding of zooplankton prey could potentially increase their risk of ingesting unwanted particles in the
water, such as microplastics.
Microplastics are considered ubiquitous in aquatic ecosystems worldwide and are negatively impacting
marine life25. By 2014, there was an estimated 15 to 51 trillion microplastic particles in the oceans26, which are
derived from direct manufacturing or break down from larger plastic debris due to abrasion, wave action, and UV
radiation. Plastic waste entering the oceans is expected to increase 10-fold by 202527 leading to growing concerns
about the potential for these pollutants to negatively aect marine organisms. eir similarity in shape and size to
School of Aquatic and Fishery Sciences, University of Washington, Seattle, Washington, 98195, USA. *email:
jeremyax@uw.edu
OPEN
Content courtesy of Springer Nature, terms of use apply. Rights reserved
2
SCIENTIFIC REPORTS | (2019) 9:18193 | https://doi.org/10.1038/s41598-019-54698-7
www.nature.com/scientificreports
www.nature.com/scientificreports/
zooplankton make microplastics particularly problematic for planktivorous animals such as corals that can ingest
them while feeding8. In some organisms, ingesting microplastics can lead to decreased feeding eciency, growth
and fecundity9,28,29 but for corals these eects are still not fully understood. Further, there is increasing concern
about the role of plastics, large and small, to act as vectors for diseases and contaminants3032.
Previous studies have demonstrated that ingesting, and exposure to, microplastics can have negative eects
on corals. Corals that ingested microplastics tended to egest most of them within 48 h which limited the time
microplastics could cause internal damage but is still thought to be energetically costly79. For some coral spe-
cies, exposure to microplastics resulted in increased mucous production, bleaching, necrosis, changes in pho-
tosynthetic performance, and decreased growth and feeding rates7,9,10. One coral species, Astrangia poculata,
appeared to selectively feed on clean microplastics when also oered bio-fouled particles, leading researchers to
suggest that chemical cues released by plastics (i.e., chemoreception) drove ingestion33. Additional research also
showed that A. poculata preferred to feed on microplastics over similar sized brine shrimp eggs, and that ingesting
microplastics can inhibit later feeding on nutritious prey32. While we are beginning to understand the responses
and mechanisms of microplastics ingestion by corals, we still do not know how this pervasive pollutant interacts
with other stressors, such as rising sea temperatures.
e objective of this study was to examine whether prior exposure to thermal stress aects microplastics
ingestion and if microplastics exposure and ingestion aects the amount of prey ingested by reef-building corals.
To determine this, we compared ingestion rates of corals exposed to microplastics (MP) only, Artemia only, or MP
and Artemia following ambient and increased temperature treatments. We hypothesized that if Artemia ingestion
changed due to thermal stress, we would also see a similar trend in MP ingestion rates. Additionally, if a chemical
in microplastics makes them more appealing to corals33, then we hypothesized that corals exposed to microplas-
tics would ingest less prey in favor of microplastics. As thermal stress events are predicted to occur with greater
frequency and intensity, and microplastics continue to accumulate in the oceans, it is critical that we understand
how corals respond to these stressors to better manage coral resilience in our changing world.
Results
Microplastics ingestion. Both species, Montipora capitata and Pocillopora damicornis, ingested microplas-
tics (Fig.1). e number of microplastics ingested by individual polyps ranged from zero to one in M. capitata,
and from zero to seven in P. damicornis. Overall, P. damicornis ingested over 520% more microplastics than M.
capitata.
Compared to ambient temperature controls, corals exposed to three weeks of thermal stress were visibly pale
(bleached). is did not, however, result in signicantly dierent microplastics ingestion rates (Fig.2A,B). M.
capitata, ingested very few microplastics overall, ingesting only 0.2 ± 0.2 (mean ± 1 SEM) microplastics per 200
polyps h1 in the MP only treatment aer thermal stress, and 0.3 ± 0.2 microplastics per 200 polyps h1 in the MP
& Artemia treatment at ambient temperature (Fig.2A). M. capitata did not ingest any microplastics in the MP
only treatment at ambient temperature or in the MP & Artemia treatment aer thermal stress (Fig.2A).
ough thermal stress was not a signicant factor, P. damicornis ingested signicantly more microplastics in
the MP & Artemia treatments than in the MP only treatments aer both temperature treatments (Permutation
ANOVA [aovp], df = 1, F = 20.16, p = 0.00012, Fig.2B). In the MP & Artemia treatments P. damicornis ingested
15.7 ± 5.2 microplastics per 200 polyps h1 at ambient temperature and 9.6 ± 3.1 microplastics per 200 polyps h1
aer thermal stress (Fig.2B). When P. damicornis was exposed to microplastics only, particle ingestion was absent
or negligible aer both ambient and increased temperature treatments (Fig.2B).
Artemia ingestion. Artemia were ingested by both species in all treatments (Fig.2C,D). e number of
Artemia ingested by individual polyps ranged from zero to one in M. capitata and zero to twelve in P. damicornis.
Following thermal stress, Artemia ingestion was signicantly decreased in both M. capitata (aovp, df = 1,
F = 11.65, p = 0.002, Fig.2C) and P. damicornis (aovp, df = 1, F = 6.658, p = 0.0156, Fig.2D) compared to ambi-
ent temperature controls. For both species, there was no signicant dierence in Artemia ingestion between MP
only and MP & Artemia treatments aer either temperature treatment. M. capitata in the Artemia only treatments
Figure 1. Microplastics ingested in the polyps of (A) Montipora capitata, and (B) Pocillopora damicornis. e
yellow dotted circles show where the polyp was dissected exposing the contents of the gut.
Content courtesy of Springer Nature, terms of use apply. Rights reserved
3
SCIENTIFIC REPORTS | (2019) 9:18193 | https://doi.org/10.1038/s41598-019-54698-7
www.nature.com/scientificreports
www.nature.com/scientificreports/
ingested 12.3 ± 5.4 Artemia per 200 polyps h1 at ambient temperature and 3.7 ± 1.6 Artemia per 200 polyps h1
aer thermal stress. In the MP & Artemia treatments, M. capitata ingested 12.1 ± 5.4 Artemia per 200 polyps h1
at ambient temperature and 4.3 ± 1.6 Artemia per 200 polyps h1 aer thermal stress (Fig.2C). P. damicornis
in the Artemia only treatments ingested 120.6 ± 17.5 Artemia per 200 polyps h1 at ambient temperature and
73.3 ± 17.3 Artemia per 200 polyps h1 aer thermal stress. In the MP & Artemia treatments, P. damicornis
ingested 134.2 ± 11.9 Artemia per 200 polyps h1 at ambient temperature and 111.3 ± 17.7 Artemia per 200 pol-
yps h1 aer thermal stress (Fig.2D).
Discussion
In this study we investigated how microplastics ingestion and heterotrophy are impacted aer thermal stress in
two reef-building corals, Montipora capitata and Pocillopora damicornis. Our results revealed that prior exposure
to thermal stress did not aect microplastics ingestion but can lead to decreased feeding on prey. We also found
that ingesting microplastics did not aect the amount of prey ingested, and that these corals did not selectively
ingest microplastics as has been observed in another species33. Additionally, we observed considerable varia-
bility in microplastics and Artemia ingestion rates under dierent scenarios between the two studied species.
Our results suggest that coral species will respond dierently to microplastics pollution following thermal stress
events.
In contrast to previous studies14,23, we did not observe higher feeding rates in corals following thermal stress
and subsequent bleaching. On the contrary, Artemia feeding rates signicantly decreased for both species, and
microplastics ingestion rates decreased slightly in P. damicornis. is may be due to the corals being stressed,
which has been suggested to cause decreased tentacle activity and/or nematocyst function22,24,34. e fact that
feeding did not increase may be due to not reaching a “bleaching threshold” needed to see an increased feed-
ing response. In the present study, we followed a similar thermal stress regime to that of Grottoli et al.14 and,
though we did not quantify bleaching (symbiont counts, pigment concentrations, photophysiology), most coral
Figure 2. Mean ( ± SEM) microplastics ([MP], A,B) and Artemia nauplii (C,D) ingestion rates of corals
exposed to ambient (dark bars) and increased (light bars) temperature. Note the dierence in scale of the y-axes.
Content courtesy of Springer Nature, terms of use apply. Rights reserved
4
SCIENTIFIC REPORTS | (2019) 9:18193 | https://doi.org/10.1038/s41598-019-54698-7
www.nature.com/scientificreports
www.nature.com/scientificreports/
fragments were completely white, and the rest were very pale. Alternatively, it may be that energy reserve status
is the mechanism controlling heterotrophic plasticity. In our study we measured ingestion immediately aer
thermal stress, whereas Grottoli et al.14 measured it two weeks aer thermal stress exposure. us it may be that
these corals needed to spend more time bleached in order to reach such critical energy levels and increase heter-
otrophy. Two corals, Turbinaria reniformis and Galaxea fascicularis, display increased feeding rates in as little as
ve days of exposure to thermal stress22 suggesting that such critical thresholds can be met rapidly, and support-
ing that this response is considerably variable among species. Furthermore, heterotrophic plasticity can also be
driven by other environmental factors such as ultraviolet radiation and seasonal weather patterns24,35. With the
increasing threat of thermal stress events and microplastics accumulation in the oceans, further research should
compare feeding rates of prey (and microplastics), as well as assimilation and allocation of heterotrophic carbon
to the corals’ energy reserves (e.g. lipids, carbohydrates). Feeding rates (prey/microplastics) and carbon transfer
should be evaluated at several periods over the entire bleaching cycle, from the initiation of thermal stress to the
full recovery of the coral.
Even though exposure to microplastics led to them being ingested by both species, it did not aect Artemia
ingestion rates as expected. A similar behavior was observed in A. poculata which, following exposure to
microplastics, did not change the amount it fed on live Artemia and copepods32. While this suggests that ingesting
microplastics may not have a large eect on heterotrophic energy acquisition for these species, more information
is needed to draw such a conclusion. First, this study was limited by the short duration (1 h) of feeding trials. For
many corals that generally feed all night, constant exposure could allow microplastics to accumulate in the polyps
and prevent further ingestion of prey. However, the amount of accumulation that occurs depends on retention
time and egestion rates, which were not measured in this study. To our knowledge, there is currently no published
information on accumulation rates (e.g. mass balance) in coral polyps constantly exposed to microplastics and
should be a priority for future research. Additionally, we lack data on the assimilation rate of carbon and nutrients
from the Artemia prey in corals exposed to microplastics. ough microplastics did not appear to act as a barrier
to prey ingestion, at least in the short-term, they may act as a barrier to digestion and nutrient assimilation. In the
oyster, Pinctada margaritifera, microplastics exposure did not aect ingestion rate but did signicantly decrease
macroalgae assimilation eciency36.
Chemoreception did not appear to drive microplastics ingestion for either species studied here. In contrast,
the presence of Artemia prey appeared to strongly inuence whether microplastics were ingested for P. damicor-
nis, which did not selectivity ingest microplastics. Allen et al.33 found that A. poculata ingested clean weathered
plastics over bio-fouled ones and suggested that microplastics ingestion by corals was driven by phagostimulant
(feeding cue) release by the plastics. However, in the present study, microplastics ingestion by P. damicornis
was absent or negligible when exposed only to clean microplastics. In a similar study, symbiotic sea anemones,
Aiptasia pallida, were also reluctant to ingest any microplastics, including nylon, polyester and polypropylene
bers, in the absence of prey tissue37. Dierences among studies could be due to species specic responses to
phagostimulants in plastics, and/or the use of dierent types of microplastics. e microplastics used in our
study were all polyethylene, whereas Allen et al. (2017) used a mixture of plastic particles consisting of two-thirds
polyethylene and one-third polystyrene, and it might be that only polystyrene released a phagostimulant. Further
research should focus on the potential of phagostimulant release by dierent types of plastic. Our results suggest
that chemicals released by certain plastics may drive selectivity in some corals, such as A. poculata, but not so in
other corals, such as P. damicornis, that are simply at risk of inadvertently ingesting microplastics during times
when they are feeding.
e fact that acute thermal stress led to decreased microplastics ingestion in this study does not eliminate
corals’ risk of exposure, as microplastics were still ingested. e act of ingesting and then egesting microplas-
tics is assumed to be energetically costly79, although further research is needed to determine how costly those
behaviors are38. Additionally, exposure to microplastics can trigger rejection mechanisms, similar to how corals
handle sediment exposure39,40, that also consume the coral’s energy reserves7. In other benthic marine inver-
tebrates, microplastics ingestion has also led to weight loss28 and decreased tness29 which were attributed to
decreased prey ingestion or assimilation eciency due to the presence of microplastics in the gut. In corals,
chronic exposure to microplastics resulted in species-specic stress responses, including decreased growth, sup-
porting the notion of depleted energy reserves10. Future research should focus on examining how and to what
degree microplastics exposure and ingestion can aect a coral’s energetic status in the long-term, especially dur-
ing bleaching when energy reserves are critical for the coral’s survival41. Furthermore, the ability of some corals
to increase feeding due to bleaching or other factors could exacerbate these eects if microplastics ingestion
increases accordingly, but this still needs to be determined. For future corals that will have to endure increasingly
prolonged and intense thermal stress, and numerous other stressors4, any amount of energy wasted could be
signicant.
Results from this study, and from other studies that investigated microplastics ingestion by corals, support
that some corals are likely more at risk of microplastics exposure than others10. For example, in agreement with
Reichert et al. (2018), this study observed variable microplastics ingestion rates among coral species, and chal-
lenging Allen et al. (2017), our work showed that plastics are not so “tasty” to all corals. Furthermore, coral feed-
ing rates can vary depending on a variety of factors14,2224,35 and may potentially aect microplastics ingestion.
Given the various responses to microplastics and feeding behaviors of corals, future research should focus on
how, and which, corals are likely to be aected by microplastics under future scenarios.
Here we present the first study to examine the roles of thermal stress on microplastic ingestion and of
microplastics exposure on heterotrophy in two reef-building corals. Overall, P. damicornis ingested more
microplastics and fed more heavily on Artemia than M. capitata, while both species displayed decreased feeding
on Artemia under thermal stress. When oered Artemia, P. damicornis readily ingested microplastics, but with-
out live prey it ingested virtually no microplastics, indicating that chemoreception does not drive microplastics
Content courtesy of Springer Nature, terms of use apply. Rights reserved
5
SCIENTIFIC REPORTS | (2019) 9:18193 | https://doi.org/10.1038/s41598-019-54698-7
www.nature.com/scientificreports
www.nature.com/scientificreports/
ingestion in all corals. Collectively, these results suggest that some coral species may be at greater risk of microplas-
tics exposure than others. Further research should focus on the physiological eects of microplastics, how a cor-
als’ feeding behavior inuences its potential to ingest microplastics, how ingesting microplastics aect nutrient
assimilation, which plastics release phagostimulants, and which coral species are aected by these phagostimu-
lants. When used in the context of global change, these data will be critical for predicting the potential impact of
microplastics on future corals and coral reefs.
Methods
Location and species. is study was conducted from June 21 to August 20, 2018, at the Hawai’i Institute
of Marine Biology (HIMB), located in Kaneohe Bay, O’ahu, Hawai’i (21.4282° N, 157.7919° W). We performed
our experiments on two locally common reef-building coral species. Montipora capitata (rice coral) is a dominant
reef-builder in Hawai’i. It was chosen for this experiment because it displays heterotrophic plasticity (increased
feeding) following bleaching due to thermal stress14,23. is species occurs in plating and branching forms though
only the branching form was used in this experiment. M. capitata is a small polyp species (ca. 0.8 mm diameter),
has a perforate skeleton and has a plocoid coralite arrangement. Pocillopora damicornis (cauliower coral) is a
less-dominant branching coral species on Hawaiian reefs but is locally abundant42. To our knowledge, hetero-
trophic plasticity following thermal stress had not been reported for this species, which allowed us to investigate
whether it also employs this strategy. P. damicornis has small polyps (ca. 1 mm diameter), a plocoid coralite
arrangement and an imperforate skeleton.
Experimental set-up. Ten colonies of M. capitata and P. damicornis (ca. 14 cm in diameter) were collected
from 1–2 m depth in the inner lagoon surrounding HIMB on June 21 and July 12, 2018, respectively (DAR Special
Activities Permit No. 2019–21). Colonies were collected at least 5 m apart to reduce the likelihood of getting
genetically identical clones. From each colony, eight fragments (ca. 5 cm) were removed, attached to ceramic
tiles and allowed to acclimate in an outdoor ow-through tank for 6–7 days. All tanks, one for acclimation and
three for each temperature, were maintained with a volume of 400 L of sand-ltered seawater from Kane’ohe
Bay and shaded to mimic photosynthetically active radiation (PAR) on the reef. Mean daytime PAR was 235
µmol photons m2 s1 and mean PAR at 12:00 was 522 µmol photons m2 s1 (Odyssey Submersible PAR
Logger, Dataow Systems LTD.). e average temperature of ambient seawater supplied during the acclimation
period was 27.3 ± 0.5 °C, measured hourly (HOBO pendant temperature loggers #UA-002-64, Onset Computer
Corporation).
Aer the acclimation period, four fragments from each colony were moved to ambient temperature treat-
ments (27.2 ± 0.5 °C) and the other four were moved to increased temperature treatments (see below). e coral
fragments were randomly assigned to one of the three tanks for each temperature treatment, and rotated weekly
between tanks to minimize potential tank eects. For M. capitata, the temperature was increased slowly over
ve days to 30.8 ± 0.8 °C, similar to Palardy et al.23. In a preliminary experiment, P. damicornis experienced ca.
50% mortality under 30.8 °C so the water temperature was increased to only 29.2 ± 0.4 °C over ve days. For
both species, the increased temperature treatments lasted for 20 days and noticeable bleaching was observed,
although not quantied. Aer the temperature treatment, the heaters were turned o and feeding trials began
the following day, based on the assumption that M. capitata would increase feeding following thermal stress and
bleaching14,23.
Feeding trials. Feeding chambers were constructed of rectangular polycarbonate 3.7 L food pans t with
an adjustable circulation pump (Hydor pico 70, Hydor USA Inc.) on the lowest ow setting (49 L h1) and an
air-stone. e circulation pump was glued to the oor of one end of the chamber and the nozzle was pointed up
at a 45° angle towards the middle of the chamber to break the water’s surface tension. It was necessary to supply
air bubbles in the chamber to facilitate microplastics suspension in the water. irty minutes prior to adding the
coral fragments, the chambers were lled with 2 L of 1 µm ltered seawater (FSW) and placed in water baths at
ambient seawater temperature.
Each night, for ten consecutive nights, feeding trials were performed with all eight fragments from each colony
(four fragments previously exposed to ambient temperature and four fragments previously exposed to increased
temperature). e experiments started on July 20 for M. capitata and Aug. 11 for P. damicornis. e fragments
from each temperature treatment were given one of four feeding treatments: (i) microplastics (2 particles mL1)
only, (ii) Artemia nauplii (2 individuals mL1) only, (iii) microplastics (2 particles mL1) and Artemia nauplii
(2 individuals mL1), and (iv) 1 µm FSW control. e concentration of microplastics used in this study was
higher than what has been reported for coral refs. 43,44 but was lower than most previous experiments that studied
microplastics ingestion by corals7,8,33,45. A high concentration of Artemia was also used because, as noted in pre-
vious studies22,23, it allowed for smaller sample sizes, minimized dissection time and increased statistical power.
Green uorescent polyethylene (conrmed by Fourier Transform Infrared Spectroscopy, see Supplementary
Fig.S1) microbeads (Cospheric LLC.) with a diameter of 150–180 µm and a density of 1.025 g mL1 were used
for the microplastics treatment because they had similar mass (2.4 µg per particle) to the Artemia used and the
same density as sea water. e microbeads were served clean (not bio-fouled) to allow for potential chemical cues
to inuence the corals’ feeding behavior33. Freshly hatched Artemia nauplii (Grade A, SLU strain, Brine Shrimp
Direct, Ogden, UT; dry weight = 2.42 µg per individual46) were used because they fall within the prey size range
for P damicornis and M, capitata23,47, and to facilitate the quantication of treatment concentrations and ingestion
rates. FSW controls were used to account for the potential ingestion of residual microplastics that stuck to cham-
ber components despite rigorous cleaning between trials. No microplastics were found in dissected control corals,
thus control data were le out of further analyses.
Content courtesy of Springer Nature, terms of use apply. Rights reserved
6
SCIENTIFIC REPORTS | (2019) 9:18193 | https://doi.org/10.1038/s41598-019-54698-7
www.nature.com/scientificreports
www.nature.com/scientificreports/
Coral fragments were placed in the feeding chambers each day at 12:00 h to give them ample time to acclimate
to the chamber and digest any previously ingested prey23. At 20:00 h, microplastics and Artemia nauplii were
added to the feeding chambers and the coral fragments were allowed to feed for one hour before being removed
from their chambers and xed immediately in 10% formalin. ough both species used in this study presumably
feed throughout the night, previous research has shown that they feed heavily enough within the rst hour of
dusk to draw meaningful biological conclusions23,48, thus a one hour feeding duration was used. e next day, the
number of microplastics and Artemia ingested by 200 polyps were counted by dissecting 200 polyps from each
fragment under a stereo microscope (10–40x) using ne dissection probes, forceps and a UV light. An ingestion
was dened as a microplastic or Artemia nauplii found in the coral polyp and did not include any information on
egested particles. Microplastics counted in the polyps were nudged suciently to be certain that we were counting
the green uorescent microbeads and not autouorescence of the coral or symbionts. Microplastics and Artemia
ingestion rates are reported as the mean number of ingestions per 200 polyps h1 ± one standard error.
Statistics. Microplastic and Artemia ingestion were compared separately for each species (n = 10) following a
fully factorial 2 × 3 (2 temperatures × 3 feeding treatments) mixed eects permutation analysis of variance, using
the aovp function49 in R (Rstudio v.1.1.463). is randomization procedure was used because most of the data
did not meet the normality nor the equal variance assumptions of a typical ANOVA, due to high occurrences of
zeros in the data (no ingestions by corals in some treatments). Temperature and feeding treatments were treated
as main eects and colony as a random eect. e aovp function was ran with 10,000 iterations and results were
considered signicant when p < 0.05.
Data availability
e datasets generated during and analysed during the current study are available in the Figshare repository,
https://doi.org/10.6084/m9.gshare.8264084.v1.
Received: 18 June 2019; Accepted: 18 November 2019;
Published: xx xx xxxx
References
1. Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidication. Science 318, 1737–1742 (2007).
2. U.S. Global Change esearch Program. Fourth National Climate Assessment. II, 1–470 (2018).
3. Moberg, F. & Fole, C. Ecological goods and services of coral reef ecosystems. Ecol. Econ. 29, 215–233 (1999).
4. Van Hooidon, . et al . Local-scale projections of coral reef futures and implications of the Paris Agreement. Sci. Rep. 6, 1–8 (2016).
5. Hughes, T. P. & Connell, J. H. Multiple stressors on coral reefs: A long-term perspective. Limnol. Oceanogr. 44, 932–940 (1999).
6. Ban, S. S., Graham, N. A. J. & Connolly, S. . Evidence for multiple stressor interactions and eects on coral reefs. Glob. Chang. Biol.
20, 681–697 (2014).
7. eichert, J., Schellenberg, J., Schubert, P. & Wile, T. esponses of reef building corals to microplastic exposure. Environ. Pollut. 237,
955–960 (2018).
8. Hall, N. M., Berry, L. E., intoul, L. & Hoogenboom, M. O. Microplastic ingestion by scleractinian corals. Mar. Biol. 162, 725–732
(2015).
9. Chapron, L. et al. Macro- and microplastics aect cold-water corals growth, feeding and behaviour. Sci. Rep. 8, 1–8 (2018).
10. eichert, J., Arnold, A. L., Hoogenboom, M. O., Schubert, P. & Wile, T. Impacts of microplastics on growth and health of
hermatypic corals are species-specic. Environ. Pollut. 254, 113074 (2019).
11. LaJeunesse, T. C. et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Cur r.
Biol. 28, 2570–2580.e6 (2018).
12. Muscatine, L. e role of symbiotic algae in carbon and energy ux in reef corals. in Ecosystems of the world, Vol. 25. Coral reefs (ed.
Dubinsy, Z.) 75–87 (Elsevier, 1990).
13. Muscatine, L. & Porter, J. W. eef corals: Mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27, 454–460
(1977).
14. Grottoli, A. G., odrigues, L. J. & Palardy, J. E. Heterotrophic plasticity and resilience in bleached corals. Nature 440, 1186–1189
(2006).
15. Hoegh-Guldberg, O. & Smith, G. J. e eect of sudden changes in temperature, light and salinity on the population density and
export of zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora histrix Dana. J. Exp. Mar. Bio. Ecol. 129,
279–303 (1989).
16. Iglesias-Prieto, ., Matta, J. L., obins, W. A. & Trench, . . Photosynthetic response to elevated temperature in the symbiotic
dinoagellate Symbiodinium microadriaticum in culture. Proc. Natl. Acad. Sci. 89, 10302–10305 (1992).
17. Loya, Y. et al. Coral bleaching: the winners and the losers. Ecol. Lett. 4, 122–131 (2001).
18. Jones, A. M., Berelmans, ., Van Oppen, M. J. H., Mieog, J. C. & Sinclair, W. A community change in the algal endosymbionts of a
scleractinian coral following a natural bleaching event: Field evidence of acclimatization. Proc. R. Soc. B Biol. Sci. 275, 1359–1365
(2008).
19. Hayes, . L. & Bush, P. G. Microscopic observations of recovery in the reef-building scleractinian coral, Montastrea annularis, aer
bleaching on a Cayman reef. Coral Reefs 8, 203–209 (1990).
20. Hughes, A. D. & Grottoli, A. G. Heterotrophic compensation: A possible mechanism for resilience of coral reefs to global warming
or a sign of prolonged stress? PLoS One 8, 1–10 (2013).
21. Bessell-Browne, P., Stat, M., omson, D. & Clode, P. L. Coscinaraea marshae corals that have survived prolonged bleaching exhibit
signs of increased heterotrophic feeding. Coral Reefs 33, 795–804 (2014).
22. Ferrier-pagès, C., ottier, C., Beraud, E. & Levy, O. Experimental assessment of the feeding eort of three scleractinian coral species
during a thermal stress: Eect on the rates of photosynthesis. J. Exp. Mar. Bio. Ecol. 390, 118–124 (2010).
23. Palardy, J. E., odrigues, L. J. & Grottoli, A. G. e importance of zooplanton to the daily metabolic carbon requirements of healthy
and bleached corals at two depths. J. Exp. Mar. Bio. Ecol. 367, 180–188 (2008).
24. Courtial, L., oberty, S., Shic, J. M., Houlbreque, F. & Ferrier-pages, C. Interactive eects of ultraviolet radiation and thermal stress
on two reef-building corals. Limnol. Oceanogr. 62, 1000–1013 (2017).
25. Gideon, C. & Faggio, C. Microplastics in the marine environment: Current trends in environmental pollution and mechanisms of
toxicological prole. Environ. Toxicol. Pharmacol. 68, 61–74 (2019).
26. Sebille, E. van et al. A global inventory of small oating plastic debris. Environ. Res. Lett. 10 (2015).
Content courtesy of Springer Nature, terms of use apply. Rights reserved
7
SCIENTIFIC REPORTS | (2019) 9:18193 | https://doi.org/10.1038/s41598-019-54698-7
www.nature.com/scientificreports
www.nature.com/scientificreports/
27. Jambec, J. . et al. Plastic waste inputs from land into the ocean. Science 347, 768–771 (2015).
28. Besseling, E., Wegner, A., Foeema, E. M., Van Den Heuvel-Greve, M. J. & oelmans, A. A. Eects of microplastic on tness and
PCB bioaccumulation by the lugworm Arenicola marina (L.). Environ. Sci. Technol. 47, 593–600 (2013).
29. Sussarellu, . et al. Oyster reproduction is aected by exposure to polystyrene microplastics. Proc. Natl. Acad. Sci. 113, 2430–2435
(2016).
30. Goldstein, M. C., Carson, H. S. & Erisen, M. elationship of diversity and habitat area in North Pacic plastic-associated raing
communities. Mar. Biol . 161, 1441–1453 (2014).
31. Lamb, J. B. et al. Plastic waste associated with disease on coral reefs. Science 359, 460–462 (2018).
32. otjan, . D. et al. Patterns, dynamics and consequences of microplastic ingestion by the temperate coral, Astrangia poculata. Proc.
R. Soc. B 286 (2019).
33. Allen, A. S., Seymour, A. C. & ittschof, D. Chemoreception drives plastic consumption in a hard coral. Mar. Pollut. Bull. 124,
198–205 (2017).
34. Johannes, . E. & Tepley, L. Examination of feeding of the reef coral Porties lobata in situ using time lapse photography. in Proc. 2nd
Int. Coral Reef Symp 1:127–131 (1974).
35. Mies, M. et al. In sit u shis of predominance between autotrophic and heterotrophic feeding in the reef-building coral Mussismilia
hispida: an approach using fatty acid trophic marers. Coral Reefs 37, 677–689 (2018).
36. Gardon, T., eisser, C., Soyez, C., Quillien, V. & Le Moullac, G. Microplastics aect energy balance and gametogenesis in the pearl
oyster Pinctada margaritifera. Environ. Sci. Technol. 52, 5277–5286 (2018).
37. omano de Orte, M., Clowez, S. & Caldeira, . esponse of bleached and symbiotic sea anemones to plastic microber exposure.
Environ. Pollut. 249, 512–517 (2019).
38. Hanins, C., Duffy, A. & Drisco, . Scleractinian coral microplastic ingestion: Potential calcification effects, size limits, and
retention. Mar. Pollut. Bull. 135, 587–593 (2018).
39. iegl, B. & Branch, G. M. Eects of sediment on the energy budgets of four scleractinian (Bourne 1900) and ve alcyonacean
(Lamouroux 1816) corals. J. Exp. Mar. Bio. Ecol. 186, 259–275 (1995).
40. Staord-Smith, M. G. & Ormond, . F. G. Sediment-rejection mechanisms of 42 species of Australian scleractinian corals. Mar.
Freshw. Res. 43, 683–705 (1992).
41. odrigues, L. J. & Grottoli, A. G. Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol. Oceanogr.
52, 1874–1882 (2007).
42. Joiel, P. L. Jokiel’s Illustrated Scientic Guide to Kaneohe Bay, Oahu. (1991).
43. Connors, E. J. Distribution and biological implications of plastic pollution on the fringing reef of Mo’orea, French Polynesia. PeerJ 5
(2017).
44. Saliu, F. et al. Microplastic and charred microplastic in the Faafu Atoll, Maldives. Mar. Pollut. Bull. 136, 464–471 (2018).
45. Tang, J., Ni, X., Zhou, Z., Wang, L. & Lin, S. Acute microplastic exposure raises stress response and suppresses detoxication and
immune capacities in the scleractinian coral. Pocillopora damicornis 243, 66–74 (2018).
46. Vanhaece, P. & Sorgeloos, P. International Study on Artemia IV. e biometrics of Artemia strains from dierent geographical
origin. in e Brine Shrimp Artemia Vol. 3 Ecology, Culturing, Use in Aquaculture (eds. Persoone, G., Sorgeloos, P., oels, O. &
Jaspers, E.) 3, 456 (Universa Press, 1980).
47. Palardy, J. E., Grottoli, A. G. & Matthews, . A. Eect of naturally changing zooplanton concentrations on feeding rates of two coral
species in the Eastern Pacic. J. Exp. Mar. Bio. Ecol. 331, 99–107 (2006).
48. Palardy, J. E., Grottoli, A. G. & Matthews, . e eect of morpholog y, polyp size, depth, and temperture on feeding in three species
of Panamanian corals. Mar. Ecol. Prog. Ser. 300, 79–85 (2005).
49. Wheeler, . E. & Torchiano, M. lmPerm: Permutation tests for linear models, http://CAN.-project.org/pacage=lmPerm. 24 p
(2016).
Acknowledgements
We oer our warmest gratitude to the Gates Coral Lab for hosting and supporting us during this experiment
at the Hawaii Institute of Marine Biology. We thank Lisa Rodrigues for advice about the experimental design
and manuscript. We thank Tanya Brown, Brenner Wakayama, Gavin Kreitman, Melissa Jae and Sean Frangos
for help with collecting and culturing the experimental corals. We thank Samantha Pham for validating the
polymer composition of our experimental microplastics. We would also like to especially thank Yanbo Ge and the
Biostatistics Consulting group from the University of Washington Department of Statistics for guidance on the
statistical tests used in our analyses. Work was supported by NSF IOS (1655682) awarded to J.L.P.G. is material
is based upon work supported by the National Science Foundation Graduate Research Fellowship Program
under Grant No. (DGE1762114). Any opinions, ndings, and conclusions or recommendations expressed in this
material are those of the author(s) and do not necessarily reect the views of the National Science Foundation.
Author contributions
J.B.A. developed and ran the experiments, analyzed the data, produced the gures and wrote the manuscript.
J.L.P.G. developed and funded the experiment and wrote the manuscript.
Competing interests
e authors declare no competing interests.
Additional information
Supplementary information is available for this paper at https://doi.org/10.1038/s41598-019-54698-7.
Correspondence and requests for materials should be addressed to J.B.A.
Reprints and permissions information is available at www.nature.com/reprints.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and
institutional aliations.
Content courtesy of Springer Nature, terms of use apply. Rights reserved
8
SCIENTIFIC REPORTS | (2019) 9:18193 | https://doi.org/10.1038/s41598-019-54698-7
www.nature.com/scientificreports
www.nature.com/scientificreports/
Open Access This article is licensed under a Creative Commons Attribution 4.0 International
License, which permits use, sharing, adaptation, distribution and reproduction in any medium or
format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Cre-
ative Commons license, and indicate if changes were made. e images or other third party material in this
article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the
material. If material is not included in the article’s Creative Commons license and your intended use is not per-
mitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the
copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
© e Author(s) 2019
Content courtesy of Springer Nature, terms of use apply. Rights reserved
1.
2.
3.
4.
5.
6.
Terms and Conditions
Springer Nature journal content, brought to you courtesy of Springer Nature Customer Service Center GmbH (“Springer Nature”).
Springer Nature supports a reasonable amount of sharing of research papers by authors, subscribers and authorised users (“Users”), for small-
scale personal, non-commercial use provided that all copyright, trade and service marks and other proprietary notices are maintained. By
accessing, sharing, receiving or otherwise using the Springer Nature journal content you agree to these terms of use (“Terms”). For these
purposes, Springer Nature considers academic use (by researchers and students) to be non-commercial.
These Terms are supplementary and will apply in addition to any applicable website terms and conditions, a relevant site licence or a personal
subscription. These Terms will prevail over any conflict or ambiguity with regards to the relevant terms, a site licence or a personal subscription
(to the extent of the conflict or ambiguity only). For Creative Commons-licensed articles, the terms of the Creative Commons license used will
apply.
We collect and use personal data to provide access to the Springer Nature journal content. We may also use these personal data internally within
ResearchGate and Springer Nature and as agreed share it, in an anonymised way, for purposes of tracking, analysis and reporting. We will not
otherwise disclose your personal data outside the ResearchGate or the Springer Nature group of companies unless we have your permission as
detailed in the Privacy Policy.
While Users may use the Springer Nature journal content for small scale, personal non-commercial use, it is important to note that Users may
not:
use such content for the purpose of providing other users with access on a regular or large scale basis or as a means to circumvent access
control;
use such content where to do so would be considered a criminal or statutory offence in any jurisdiction, or gives rise to civil liability, or is
otherwise unlawful;
falsely or misleadingly imply or suggest endorsement, approval , sponsorship, or association unless explicitly agreed to by Springer Nature in
writing;
use bots or other automated methods to access the content or redirect messages
override any security feature or exclusionary protocol; or
share the content in order to create substitute for Springer Nature products or services or a systematic database of Springer Nature journal
content.
In line with the restriction against commercial use, Springer Nature does not permit the creation of a product or service that creates revenue,
royalties, rent or income from our content or its inclusion as part of a paid for service or for other commercial gain. Springer Nature journal
content cannot be used for inter-library loans and librarians may not upload Springer Nature journal content on a large scale into their, or any
other, institutional repository.
These terms of use are reviewed regularly and may be amended at any time. Springer Nature is not obligated to publish any information or
content on this website and may remove it or features or functionality at our sole discretion, at any time with or without notice. Springer Nature
may revoke this licence to you at any time and remove access to any copies of the Springer Nature journal content which have been saved.
To the fullest extent permitted by law, Springer Nature makes no warranties, representations or guarantees to Users, either express or implied
with respect to the Springer nature journal content and all parties disclaim and waive any implied warranties or warranties imposed by law,
including merchantability or fitness for any particular purpose.
Please note that these rights do not automatically extend to content, data or other material published by Springer Nature that may be licensed
from third parties.
If you would like to use or distribute our Springer Nature journal content to a wider audience or on a regular basis or in any other manner not
expressly permitted by these Terms, please contact Springer Nature at
onlineservice@springernature.com
... These studies demonstrate that the capture of microplastic particles by anthozoans is not uniform, and responses to microplastics will be different across species. Moreover, mixed microplastic and food treatments have resulted in increased microplastic uptake by some anthozoan species (Axworthy and Padilla-Gamiño, 2019;Romanó de Orte et al., 2019;Savinelli et al., 2020), due to the presence of prey promoting feeding activity (Kamio and Derby, 2017). For example, the coral Pocillopora damicornis and anemone E. pallida ingested significantly more microplastics in the presence of shrimp, while little or no uptake occurred when exposed to only microplastics (Axworthy and Padilla-Gamiño, 2019;Romanó de Orte et al., 2019). ...
... Moreover, mixed microplastic and food treatments have resulted in increased microplastic uptake by some anthozoan species (Axworthy and Padilla-Gamiño, 2019;Romanó de Orte et al., 2019;Savinelli et al., 2020), due to the presence of prey promoting feeding activity (Kamio and Derby, 2017). For example, the coral Pocillopora damicornis and anemone E. pallida ingested significantly more microplastics in the presence of shrimp, while little or no uptake occurred when exposed to only microplastics (Axworthy and Padilla-Gamiño, 2019;Romanó de Orte et al., 2019). ...
... This study observed no significant influence of elevated temperature on fibre or fragment uptake in A. viridis. A similar multi-stressor study using the tropical corals Montipora capitata and Pocillopora damicornis, also found no significant difference in microplastic uptake at ambient (27°C) and increased (30°C) temperatures (Axworthy and Padilla-Gamiño, 2019). Conversely, the anemone E. pallida was more susceptible to microplastic ingestion when thermally stressed (Romanó de Orte et al., 2019). ...
Article
Full-text available
Microplastics (<1 mm) are ubiquitous in our oceans and widely acknowledged as concerning contaminants due to the multi-faceted threats they exert on marine organisms and ecosystems. Anthozoans, including sea anemones and corals, are particularly at risk of microplastic uptake due to their proximity to the coastline, non-selective feeding mechanisms and sedentary nature. Here, the common snakelocks anemone (Anemonia viridis) was used to generate understanding of microplastic uptake in the relatively understudied Anthozoa class. A series of microplastic exposure and multi-stressor experiments were performed to examine particle shape and size selectivity, and to test for the influence of food availability and temperature on microplastic uptake. All A. viridis individuals were found to readily take up microplastics (mean 142.1 ± 83.4 particles per gram of tissue) but exhibited limited preference between different particle shapes and sizes (n = 40). Closer examination identified that uptake involved both ingestion and external tissue adhesion, where microplastics were trapped in secreted mucus. Microplastic uptake in A. viridis was not influenced by the presence of food or elevated water temperature (n = 40). Furthermore, environmental sampling was performed to investigate microplastic uptake in A. viridis (n = 8) on the coast of southwest England, with a mean of 15.8 ± 4.0 particles taken up per individual. Fibres represented the majority of particles (91%) followed by fragments (9%), with 87% either clear, blue or black in colour. FTIR analysis identified 70% of the particles as anthropogenic cellulosic or plastic polymers. Thus, this study provides evidence of microplastic uptake by A. viridis in both laboratory exposures experiments and in the marine environment. These findings support recent literature suggesting that external adhesion may be the primary mechanism in which anthozoans capture microplastics from the water column and highlights the potential role anemones can play as environmental microplastic bioindicators.
... With respect to their exogenous feeding, coral are suspension feeders, ingesting plankton, both actively and passively, that are entrapped on their tentacles (Fig. 1). In addition to plankton, corals can also ingest microplastics (Hall et al., 2015;Hankins et al., 2018;Rotjan et al., 2019;Corona et al., 2020;Hankins et al., 2021), with smaller pieces likely being inadvertently consumed (Hankins et al., 2018;Axworthy and Padilla-Gamiño, 2019). Ingested plastics may block the gastrovascular cavity of the coral polyp leaving the polyp feeling satiated or may prevent feeding on nutritious food sources, as has been seen in other taxa (McCauley and Bjornal, 1999;Xu et al., 2017;Egbeocha et al., 2018;Ory et al., 2018;de Barros et al., 2020). ...
... Ingested plastics may block the gastrovascular cavity of the coral polyp leaving the polyp feeling satiated or may prevent feeding on nutritious food sources, as has been seen in other taxa (McCauley and Bjornal, 1999;Xu et al., 2017;Egbeocha et al., 2018;Ory et al., 2018;de Barros et al., 2020). While large percentages of ingested MPs (64-92%) will likely be egested (Allen et al., 2017;Hankins et al., 2018;Hankins et al., 2021) by coral polyps, microplastic exposure has been shown to impact feeding, stress response, immune system, coralhost signaling, zooxanthellae photosynthetic performance, growth, and can cause bleaching and tissue necrosis (Chapron et al., 2018, Tang et al., 2018, Axworthy and Padilla-Gamiño, 2019, Reichert et al., 2019, Syakti et al., 2019, Huang et al., 2021a, 2021b, Lanctôt et al., 2020, Hankins et al., 2021. ...
... The 3D model presented in Fig. 3a interpolates ingestion potential between 0.231 and 0.462 mm; the lower threshold is likely within this size range. Additionally, the lower threshold may be indicative of the MP sizes in which coral passively feed on MPs (Hankins et al., 2018;Axworthy and Padilla-Gamiño, 2019) suggesting that smaller MPs do not elicit a tactile response from the coral tentacles. ...
Article
Full-text available
Coral reefs have been heavily impacted by anthropogenic stressors, such as global warming, ocean acidification, sedimentation, and nutrients. Recently, microplastics (MP) have emerged as another potential stressor that may also cause adverse impacts to coral. MP ingestion by scleractinian coral among four species, Acropora cervicornis, Montastraea cavernosa, Orbicella faveolata, and Pseudodiploria clivosa, was used to identify the relationship between calyx and MP size as it pertains to active coral ingestion. A range of MP sizes (0.231–2.60 mm) were offered to the coral species across a wide range of calyx sizes (1.33–4.84 mm). Laboratory data showed that as the mean calyx size increased, so too did the mean percent of ingestion with increasing MP size. From laboratory data, a logistic model was developed to extrapolate the range of MP sizes that can be actively ingested by coral species based on calyx size. The data and model presented here offer the first predictive approach that can be used to determine the range of MP sizes that have a high likelihood of being actively ingested by coral of various sizes, thus offering insight to possible impacts on scleractinian coral.
... g cm-3 for PEST and PA, respectively, and 1.028 g cm-3 ASW used in the experiment). Conversely, experimental results showed a preferential ingestion of PA, that more than driven by density characteristics could be explained by the possible presence or release from the polymeric matrix of phagostimulants acting as feeding cue (Allen et al., 2017;Axworthy and Padilla-Gamiño, 2019). Evidence of preferential ingestion of PA over other synthetic MFs (polyester and polypropylene) has already been observed also in anemones and ascribed to a higher palatability (Romanóde Orte et al., 2019). ...
Article
Full-text available
Textile microfibers (MFs) have natural (e.g. cotton, wool and silk) or synthetic origin (e.g. polyester and polyamide), and are increasingly documented in the marine environment. Knowledge on their biological effects in marine organisms is still limited, and virtually unexplored is their capability to modulate the responsiveness toward other stressors, including those of emerging relevance under global changes scenario. With such background, the aims of this study were to i) determine the ingestion and biological effects of MFs, discriminating between synthetic and natural ones, and ii) elucidate the possibility that MFs alter the responsiveness toward additional stressors occurring at a later stage, after exposure. Adult mussels Mytilus galloprovincialis were exposed for 14 days to a high but still environmentally realistic concentration of 50 MFs L-1 of either polyester (618 ± 367 µm length, 13 ± 1 µm diameter), polyamide (566 ± 500 µm length, 11 ± 1 µm in diameter) or cotton (412 ± 342 µm length, 16 ± 4 µm diameter). After the exposure, mussels were left for 7 days to recover at control temperature (23°C) or exposed to a heatwave condition (27°C). At the end of each phase (exposure – recovery – heat stress), MFs ingestion-elimination was evaluated, along with a wide panel of biological responses, including neuro-immune and antioxidant systems alterations, lipid metabolism and onset of cellular damages. Results were elaborated through a Weight of Evidence approach to provide synthetic hazard indices based on both the magnitude and toxicological relevance of observed variations. Beside limited differences in retention and elimination of MFs, biological analyses highlighted disturbance of the immune system and demand of protection toward oxidative insult, particularly evident in mussels exposed to synthetic-MFs. Carry-over effects were observed after 7 days of recovery: organisms that had been previously exposed to MFs showed a higher susceptibility of the neuroendocrine-immune system and lipid metabolism to thermal stress compared to un-exposed mussels. Overall, this study provided evidence of direct cellular effects of MFs, emphasizing differences between synthetic and natural ones, and highlighted their capability to modulate organisms’ susceptibility toward additional stressors, as those predicted for future changes in marine ecosystems.
... After offering both types of particles independently, we found that the corals ingested the natural food at a higher rate than microplastics. In general, these findings are consistent with previous studies (Axworthy and Padilla-Gamiño, 2019;Savinelli et al., 2020), although there is also a counterexample (Rotjan et al., 2019). Yet, particle numbers deviated (SD) in average by 38 microplastic particles and 141 Artemia sp. ...
Article
Full-text available
Microplastics are omnipresent in the oceans and threaten marine animals through physical contact or ingestion. Short-term studies have already shown that reef-building stony corals respond differently to microplastics than natural food. However, it remains unknown whether corals exhibit acclimation mechanisms to combat the effects of microplastic exposure. Specifically, the long-term effects of microplastics on the feeding and defense behavior of reef-building corals remain unexplored. Therefore, the goal of this study was to infer potential acclimation mechanisms in the behavior of the corals. For this, four reef-building species (Acropora muricata, Porites lutea, Pocillopora verrucosa, and Heliopora coerulea) were exposed in a long-term experiment to microplastics for 15 months. Subsequently, coral feeding rates on microplastics and natural food (Artemia sp. cysts), feeding discrimination, and reactions to both were assessed in a 24 h pulse exposure experiment. The results showed that corals’ feeding rates did not decrease after long-term exposure to microplastics. Similarly, the feeding discrimination (i.e., ratio of feeding on microplastics and natural food) did not differ after long-term exposure to microplastics. Moreover, corals showed no changes in defense behavior (i.e., mucus production or extrusion of mesenterial filaments) against microplastics. These findings suggest that symbiotic, reef-building corals do not develop mechanisms to adapt to long-term microplastic exposure. Thus, microplastic pollution might constitute a constant stressor for coral organisms, likely leading to sustained energy expenditures and impaired health.
... There is some evidence that other anthropogenic stressors have a synergistic effect with MNPs in Anthozoa. For example, thermally bleached anemones and corals ingested more MNPs relative to prey, and experience greater internal exposure to MNPs due to longer retention times [120,121]. This is of particular concern given that coral reef ecosystems are facing increases in frequency and intensity of bleaching events due to ocean warming in conjunction with the predicted increase in MNP exposure. ...
Article
Full-text available
Plastic pollution in a growing problem globally. In addition to the continuous flow of plastic particles to the environment from direct sources, and through the natural wear and tear of items, the plastics that are already there have the potential to breakdown further and therefore provide an immense source of plastic particles. With the continued rise in levels of plastic production, and consequently increasing levels entering our marine environments it is imperative that we understand its impacts. There is evidence microplastic and nanoplastic (MNP) pose a serious threat to all the world's marine ecosystems and biota, across all taxa and trophic levels, having individual- to ecosystem-level impacts, although these impacts are not fully understood. Microplastics (MPs; 0.1–5 mm) have been consistently found associated with the biota, water and sediments of all coral reefs studied, but due to limitations in the current techniques, a knowledge gap exists for the level of nanoplastic (NP; <1 µm). This is of particular concern as it is this size fraction that is thought to pose the greatest risk due to their ability to translocate into different organs and across cell membranes. Furthermore, few studies have examined the interactions of MNP exposure and other anthropogenic stressors such as ocean acidification and rising temperature. To support the decision-making required to protect these ecosystems, an advancement in standardised methods for the assessment of both MP and NPs is essential. This knowledge, and that of predicted levels can then be used to determine potential impacts more accurately.
... Of the 20 coral-microplastic experiments published to date, less than half exposed corals to microplastics in combination with other common seawater particulates (e.g. microinvertebrates and sediments) 29,36,41,44 . Only one study so far compared how corals react to both sediments and microplastics, briefly documenting that significantly more cnidocytes are fired towards microplastics 29 and no study has addressed whether microplastics compromise sediment rejection efficiency in corals. ...
Article
Full-text available
Investigations of encounters between corals and microplastics have, to date, used particle concentrations that are several orders of magnitude above environmentally relevant levels. Here we investigate whether concentrations closer to values reported in tropical coral reefs affect sediment shedding and heterotrophy in reef-building corals. We show that single-pulse microplastic deposition elicits significantly more coral polyp retraction than comparable amounts of calcareous sediments. When deposited separately from sediments, microplastics remain longer on corals than sediments, through stronger adhesion and longer periods of examination by the coral polyps. Contamination of sediments with microplastics does not retard corals’ sediment clearing rates. Rather, sediments speed-up microplastic shedding, possibly affecting its electrostatic behaviour. Heterotrophy rates are three times higher than microplastic ingestion rates when corals encounter microzooplankton ( Artemia salina cysts) and microplastics separately. Exposed to cysts-microplastic combinations, corals feed preferentially on cysts regardless of microplastic concentration. Chronic-exposure experiments should test whether our conclusions hold true under environmental conditions typical of inshore marginal coral reefs.
Article
Microplastic pollution can harm organisms and ecosystems such as coral reefs. Corals are important habitat-forming organisms that are sensitive to environmental conditions and have been declining due to stressors associated with climate change. Despite their ecological importance, it is unclear how corals may be affected by microplastics or if there are synergistic effects with rising ocean temperatures. To address this research gap, we experimentally examined the combined effects of environmentally relevant microplastic concentrations (i.e., the global average) and elevated temperatures on bleaching of the threatened Caribbean coral, Acropora cervicornis. In a controlled laboratory setting, we exposed coral fragments to orthogonally crossed treatment levels of low-density polyethylene microplastic beads (0 and 11.8 particles L-1) and water temperatures (ambient at 28 °C and elevated at 32 °C). Zooxanthellae densities were quantified after the 17-day experiment to measure the bleaching response. Regardless of microplastic treatment level, corals in the elevated temperature treatment were visibly bleached and necrotic (i.e., significant negative effect on zooxanthellae density) while those exposed to ambient temperature remained healthy. Thus, our study successfully elicited the expected bleaching response to a high-water temperature. However, we did not observe significant effects of microplastics at either individual (ambient temperature) or combined levels (elevated temperature). Although elevated temperatures remain a larger threat to corals, responses to microplastics are complex and may vary based on focal organisms or on plastic conditions (e.g., concentration, size, shape). Our findings add to a small but growing body of research on the effects of microplastics on corals, but further work is warranted in this emerging field to fully understand how sensitive ecosystems are affected by this pollutant.
Chapter
Plastic contamination in the ocean has recently received a lot of attention. Plastic production has been growing and its use spread to many sectors. More than 80% of plastic enters the ocean from land-based sources, with the remaining having ocean-based sources. Once in the ocean, plastic undergoes fragmentation and degradation that lead to the formation of microplastics (MPs) and nanoplastics (NPs), and their dimensions are becoming an environmental concern. Thus, this chapter provides an overview of the effects of MPs and NPs on marine organisms, from bacteria to fish. Plastic affects marine organisms from molecular to population levels but some knowledge gaps exist regarding the biogeochemical cycle of plastic, how it behaves and is distributed in the aquatic-sediment compartment and in deep-sea. Moreover, more attention is necessary concerning NPs ecotoxicological effects already detected and because not all polymer types and size effects have been investigated. In addition, risk assessment of plastic particles is needed to characterize their risks and for data to be comparable.
Article
Full-text available
Microplastics are ubiquitous in marine systems, but their effects on coral physiology are still largely unknown. This study aimed to determine if exposure to a range of sizes of microplastic (10–100 µm) over a 4-week period affected selected physiological processes of healthy and moderately bleached corals. Two separate feeding experiments in which similar sized healthy and bleached Anomastraea irregularis and Pocillopora verrucosa nubbins from the south coast of KwaZulu-Natal, South Africa (30.3167° S, 30.7333° E) were fed either 0.8 mg of zooplankton only or a mix (a combination of 0.4 mg polypropylene fragments, 0.4 mg polyester fibres, and 0.8 mg zooplankton) were conducted in closed chambers for a period of 28 nights during May and June 2018. No significant differences in the physiology (ingestion, respiration, photosynthetic and growth rates) and tissue composition (Symbiodiniaceae, chlorophyll a and lipid contents) were found between corals fed the mix and those fed zooplankton only (p > 0.05). An egestion analysis revealed that both healthy and bleached A. irregularis and P. verrucosa egested the majority of the ingested microplastics after 18 h. This study shows that corals can ingest different types of microplastics but are also able to egest them over a few hours, preventing any detrimental effects.
Article
Full-text available
Increasing marine microplastic pollution has detrimentally impacted organismal physiology and ecosystem functioning. While previous studies document negative effects of microplastics on coral reef animals, the potential responses of organisms such as large benthic foraminifera (LBF) are largely unknown. Here, we document the impact of microplastics on heterotrophic feeding behavior of LBF. Specimens of Amphistegina gibbosa were incubated in three experimental treatments: (1) Artemia sp. nauplii only; (2) pristine microplastic particles only; and (3) choice of nauplii and pristine microplastic. Feeding responses were evaluated 24 h after initiation of treatments. A separate experiment was conducted to compare the effect of conditioned vs. pristine microplastic. Our results indicate that A. gibbosa is able to selectively feed on Artemia, avoiding interactions with pristine microplastic. However, the presence of conditioned microplastic causes similar feeding interaction rates as with Artemia. This suggests that microplastics with longer residence times may have a larger impact on facultative detritivores.
Article
Full-text available
Plastic contamination is now recognized as one of the most serious environmental issues for oceans. Both macro- and microplastic debris are accumulating in surface and deep waters. However, little is known about their impact on deep marine ecosystems and especially on the deep-sea reefs built by emblematic cold-water corals. The aim of this study was to investigate whether plastics affected the growth, feeding and behaviour of the main engineer species, Lophelia pertusa. Our experiments showed that both micro- and macroplastics significantly reduced skeletal growth rates. Macroplastics induced an increased polyp activity but decreased prey capture rates. They acted as physical barriers for food supply, likely affecting energy acquisition and allocation. Inversely, microplastics did not impact polyp behaviour or prey capture rates, but calcification was still reduced compared to control and in situ conditions. The exact causes are still unclear but they might involve possible physical damages or energy storage alteration. Considering the high local accumulation of macroplastics reported and the widespread distribution of microplastics in the world ocean, our results suggest that plastics may constitute a major threat for reef aggradation by inhibiting coral growth, and thus jeopardise the resilience of cold-water coral reefs and their associated biodiversity.
Article
Full-text available
The impact that microplastics (< 5 mm) have on scleractinian coral is largely unknown. This study investigated calcification effects, size limits, and retention times of microbeads and microfibers in two Caribbean species, Montastraea cavernosa and Orbicella faveolata, in a series of three experiments. No calcification effects were seen in the two-day exposure to a microbead concentration of 30 mg L −1. M. cavernosa and O. faveolata actively ingested microbeads ranging in size from 425 μm-2.8 mm, however, a 212-250 μm size class did not elicit a feeding response. The majority of microbeads were expelled within 48 h of ingestion. There was no difference in ingestion or retention times of 425-500 μm microbeads versus 3-5 mm long microfibers. M. cavernosa and O. faveolata have the ability to recognize and reject indigestible material, yet, there is still a need to study effects of energetics and microplastic contamination as a result of ingestion and egestion.
Article
Full-text available
The advent of molecular data has transformed the science of organizing and studying life on Earth. Genetics-based evidence provides fundamental insights into the diversity, ecology, and origins of many biological systems, including the mutualisms between metazoan hosts and their micro-algal partners. A well-known example is the dinoflagellate endosymbionts (“zooxanthellae”) that power the growth of stony corals and coral reef ecosystems. Once assumed to encompass a single panmictic species, genetic evidence has revealed a divergent and rich diversity within the zooxanthella genus Symbiodinium. Despite decades of reporting on the significance of this diversity, the formal systematics of these eukaryotic microbes have not kept pace, and a major revision is long overdue. With the consideration of molecular, morphological, physiological, and ecological data, we propose that evolutionarily divergent Symbiodinium “clades” are equivalent to genera in the family Symbiodiniaceae, and we provide formal descriptions for seven of them. Additionally, we recalibrate the molecular clock for the group and amend the date for the earliest diversification of this family to the middle of the Mesozoic Era (∼160 mya). This timing corresponds with the adaptive radiation of analogs to modern shallow-water stony corals during the Jurassic Period and connects the rise of these symbiotic dinoflagellates with the emergence and evolutionary success of reef-building corals. This improved framework acknowledges the Symbiodiniaceae’s long evolutionary history while filling a pronounced taxonomic gap. Its adoption will facilitate scientific dialog and future research on the physiology, ecology, and evolution of these important micro-algae.
Article
Full-text available
Many species of reef-building corals are mixotrophic, relying on both photoautotrophy performed by their dinoflagellate symbionts and heterotrophy from con sumption of zooplankton. Autotrophy and heterotrophy supply corals with specific w3 fatty acids, which can be used as trophic markers and record the contribution of each feeding strategy. This study investigated whether the reef-building coral Mussismilia hispida, endemic to Brazil, is able to shift between predominantly autotrophic and predominantly heterotrophic by monitoring the concentration of fatty acids in the host tissue. We then examined whether shifts are related to changes in temperature and wind stress. For that purpose, M. hispida colonies were monitored for a year with monthly tissue sampling. Symbiont concentration was determined and lipid extraction performed. Four fatty acids were quantitatively analyzed by gas chromatography with flame ionization detector: the autotrophy markers: stearidonic acid (SDA), docosapentaenoic acid (DPA), docosahexaenoic acid (DHA), and a heterotrophy marker: cis-gondoic acid (CGA). Three preliminary experiments confirmed the specificity of SDA, DPA and CGA, but not of DHA. Shifts of predominance occurred multiple times during the year and were associated with minimal tem- peratures and wind stress. Colonies underwent mild bleaching during summer months, which they seemed to compensate with heterotrophic feeding. Our major findings include the validation of three FATM and a trophic index for coral reef ecology studies and also describing the in situ occurrences of shifts between feeding modes, while highlighting the role of temperature and meteorological events
Article
Coral reefs are increasingly affected by the consequences of global change such as increasing temperatures or pollution. Lately, microplastics (i.e., fragments < 5 mm) have been identified as another potential threat. While previous studies have assessed short-term effects caused by high concentrations of microplastics, nothing is known about the long-term effects of microplastics under realistic concentrations. Therefore, a microcosm study was conducted and corals of the genera Acropora, Pocillopora, Porites, and Heliopora were exposed to microplastics in a concentration of 200 particles L-1, relating to predicted pollution levels. Coral growth and health, as well as symbiont properties were studied over a period of six months. The exposure caused species-specific effects on coral growth and photosynthetic performance. Signs of compromised health were observed for Acropora and Pocillopora, those taxa that frequently interact with the particles. The results indicate elevated energy demands in the affected species, likely due to physical contact of the corals to the microplastics. The study shows that microplastic pollution can have negative impacts on hermatypic corals. These effects might amplify corals' susceptibility to other stressors, further contributing to community shifts in coral reef assemblages.
Article
Microplastics (less than 5 mm) are a recognized threat to aquatic food webs because they are ingested at multiple trophic levels and may bioaccumulate. In urban coastal environments, high densities of microplastics may disrupt nutritional intake. However, behavioural dynamics and consequences of microparticle ingestion are still poorly understood. As filter or suspension feeders, benthic marine invertebrates are vulnerable to microplastic ingestion. We explored microplastic ingestion by the temperate coral Astrangia poculata. We detected an average of over 100 microplastic particles per polyp in wild-captured colonies from Rhode Island. In the laboratory, corals were fed microbeads to characterize ingestion preference and retention of microplastics and consequences on feeding behaviour. Corals were fed biofilmed microplastics to test whether plastics serve as vectors for microbes. Ingested microplastics were apparent within the mesenterial tissues of the gastrovascular cavity. Corals preferred microplastic beads and declined subsequent offerings of brine shrimp eggs of the same diameter, suggesting that microplastic ingestion can inhibit food intake. The corals co-ingested Escherichia coli cells with microbeads. These findings detail specific mechanisms by which microplastics threaten corals, but also hint that the coral A. poculata, which has a large coastal range, may serve as a useful bioindicator and monitoring tool for microplastic pollution.
Article
The global plastics production has increased from 1.5 million tons in the 1950s to 335 million tons in 2016, with plastics discharged into virtually all components of the environment. Plastics rarely biodegrade but through different processes they fragment into microplastics and nanoplastics, which have been reported as ubiquitous pollutants in all marine environments worldwide. This study is a review of trend in marine plastic pollution with focus on the current toxicological consequences. Microplastics are capable of absorbing organic contaminants, metals and pathogens from the environment into organisms. This exacerbates its toxicological profile as they interact to induced greater toxic effects. Early studies focused on the accumulation of plastics in the marine environment, entanglement of and ingestions by marine vertebrates, with seabirds used as bioindicators. Entanglement in plastic debris increases asphyxiation through drowning, restrict feeding but increases starvation, skin abrasions and skeletal injuries. Plastic ingestion causes blockage of the guts which may cause injury of the gut lining, morbidity and mortality. Small sizes of the microplastics enhance their translocation across the gastro-intestinal membranes via endocytosis-like mechanisms and distribution into tissues and organs. While in biological systems, microplastics increase dysregulation of gene expression required for the control of oxidative stress and activating the expression of nuclear factor E2-related factor (Nrf) signaling pathway in marine vertebrates and invertebrates. These alterations are responsible for microplastics induction of oxidative stress, immunological responses, genomic instability, disruption of endocrine system, neurotoxicity, reproductive abnormities, embryotoxicity and trans-generational toxicity. It is possible that the toxicological effects of microplastics will continue beyond 2020 the timeline for its ending by world environmental groups. Considering that most countries in African and Asia (major contributors of global plastic pollutions) are yet to come to terms with the enormity of microplastic pollution. Hence, majority of countries from these regions are yet to reduce, re-use or re-circle plastic materials to enhance its abatement.
Article
Microplastics are emerging contaminants in the marine environment. They enter the ocean in a variety of sizes and shapes, with plastic microfiber being the prevalent form in seawater and in the guts of biota. Most of the laboratory experiments on microplastics has been performed with spheres, so knowledge on the interactions of microfibers and marine organisms is limited. In this study we examined the ingestion of microfibers by the sea anemone Aiptasia pallida using three different types of polymers: nylon, polyester and polypropylene. The polymers were offered to both symbiotic (with algal symbionts) and bleached (without algal symbionts) anemones. The polymers were introduced either alone or mixed with brine shrimp homogenate. We observed a higher percentage of nylon ingestion compared to the other polymers when plastic was offered in the absence of shrimp. In contrast, we observed over 80% of the anemones taking up all types of polymers when the plastics were offered in the presence of shrimp. Retention time differed significantly between symbiotic and bleached anemones with faster egestion in symbiotic anemones. Our results suggest that ingestion of microfibers by sea anemones is dependent both on the type of polymers and on the presence of chemical cues of prey in seawater. The decreased ability of bleached anemones to reject plastic microfiber indicates that the susceptibility of anthozoans to plastic pollution is exacerbated by previous exposure to other stressors. This is particularly concerning given that coral reef ecosystems are facing increases in the frequency and intensity of bleaching events due to ocean warming. The ingestion and retention time of microfibers by sea anemones depend on the presence of chemical cues of prey in the seawater and on the symbiotic status of the anemone.
Article
Microplastics are widespread emerging contaminants that have been found globally in the marine and freshwater ecosystem, but there is limited knowledge regarding its impact on coral reef ecosystem and underpinning mechanism. In the present study, using Pocillopora damicornis as a model, we investigated cytological, physiological, and molecular responses of a scleractinian coral to acute microplastic exposure. No significant changes were observed in the density of symbiotic zooxanthellae during the entire period of microplastic exposure, while its chlorophyll content increased significantly at 12 h of microplastic exposure. We observed significant increases in the activities of antioxidant enzymes such as superoxide dismutase and catalase, significant decrease in the detoxifying enzyme glutathione S-transferase and the immune enzyme alkaline phosphatase, but no change in the other immune enzyme phenoloxidase during the whole experiment period. Transcriptomic analysis revealed 134 significantly up-regulated coral genes at 12 h after the exposure, enriched in 11 GO terms mostly related to stress response, zymogen granule, and JNK signal pathway. Meanwhile, 215 coral genes were significantly down-regulated at 12 h after exposure, enriched in 25 GO terms involved in sterol transport and EGF-ERK1/2 signal pathway. In contrast, only 12 zooxanthella genes exhibited significant up-regulation and 95 genes down-regulation at 12 h after the microplastic exposure; genes regulating synthesis and export of glucose and amino acids were not impacted. These results suggest that acute exposure of microplastics can activate the stress response of the scleractinian coral P. damicornis, and repress its detoxification and immune system through the JNK and ERK signal pathways. These demonstrate that microplastic exposure can compromise the anti-stress capacity and immune system of the scleractinian coral P. damicornis, despite the minimal impact on the abundance and major photosynthate translocation transporters of the symbiont in the short term.