Plastic waste associated with disease on coral reefs

Abstract

Corals wrapped in plastic
Coral reefs provide vital fisheries and coastal defense, and they urgently need protection from the damaging effects of plastic waste. Lamb et al. surveyed 159 coral reefs in the Asia-Pacific region. Billions of plastic items were entangled in the reefs. The more spikey the coral species, the more likely they were to snag plastic. Disease likelihood increased 20-fold once a coral was draped in plastic. Plastic debris stresses coral through light deprivation, toxin release, and anoxia, giving pathogens a foothold for invasion.
Science , this issue p. 460

Full text

CORAL REEFS
Plastic waste associated with disease
on coral reefs
Joleah B. Lamb,
1,2,3
*Bette L. Willis,
2,3
Evan A. Fiorenza,
1,4
Courtney S. Couch,
1,5,6
Robert Howard,
7
Douglas N. Rader,
8
James D. True,
9
Lisa A. Kelly,
3,10
Awaludinnoer Ahmad,
11,12
Jamaluddin Jompa,
12
C. Drew Harvell
1
Plastic waste can promote microbial colonization by pathogens implicated in outbreaks of
disease in the ocean. We assessed the influence of plastic waste on disease risk in 124,000
reef-building corals from 159 reefs in the Asia-Pacific region. The likelihood of disease
increases from 4% to 89% when corals are in contact with plastic. Structurally complex corals
are eight times more likely to be affected by plastic, suggesting that microhabitats for
reef-associated organisms and valuable fisheries will be disproportionately affected.
Plastic levels on coral reefs correspond to estimates of terrestrial mismanaged plastic
waste entering the ocean. We estimate that 11.1 billion plastic items are entangled on coral
reefs across the Asia-Pacific and project this number to increase 40% by 2025. Plastic
waste management is critical for reducing diseases that threaten ecosystem health and
human livelihoods.
Outbreaks of disease on coral reefs threaten
one of the most biodiverse ecosystems
on the planet (1), jeopardizing the U.S.
$375 billion in goods and services that
they provide to people each year through
fisheries, tourism, and coastal protection (2). Plas-
tic waste can host pathogens that are frequently
implicated as triggers of disease outbreaks on
coral reefs (3–9). For example, microbial commu-
nities colonizing polypropylene marine debris
were dominated by the genus Vibrio (10), an
opportunistic pathogenic bacteria of a globally
devastating group of coral diseases known as
white syndromes (11). Although an estimated
4.8 million to 12.7 million metric tons of plastic
waste enter the ocean in a single year (12), the
resulting influence on disease susceptibility in
the marine environment is unknown. Microbial
rafting on plastic debris has been shown to
strongly control surface longevity (13)andis
highestintropicalregionsneartheequatorcom-
pared with more polar regions (14), suggesting
that coral reef ecosystems could have high levels
of colonized plastic waste.
We surveyed 159 coral reefs spanning eight
latitudinal regions from four countries in the
Asia-Pacific for plastic waste and evaluated
the influence of plastic on diseases that affect
keystone reef-building corals (15)(benthicarea=
12,840 m
2
) (Fig. 1). The Asia-Pacific region con-
tains 55.5% of global coral reefs (2)andencom-
passes 73.0% of the global human population
residing within 50 km of a coast (12) (table S1).
Overall, we documented benthic plastic waste
(defined as an item with a diameter >5 0 mm)
on one-third of the coral reefs surveyed, amount-
ing to 2.0 to 10.9 plastic items per 100 m
2
of reef
area [95% confidence interval (CI), n=8survey
regions]. The number of plastic items observed on
each reef varied markedly among countries, from
RESEARCH
Lamb et al., Science 359, 460–462 (2018) 26 January 2018 1of3
2010 2025
1
2
3
4
5
7
6
8
Australia
Myanmar
Thailand
Indonesia
Asia-Pacific
2000 km
1 Myeik Archipelago
2 Koh Tao
3 Sulawesi
4 Bali
5 West Papua
6 Palm Islands
7 Whitsunday Islands
8 Keppel Islands
Survey Regions
Estimated mismanaged plastic waste
entering the ocean (thousand metric tons)
Plastic debris on coral reefs (100 m-2)
0
30
60
90
Plastic debris on
coral reefs (100 m
-2
)
N = 159
No coast
55.5% of global
coral reefs
73.0% of global coastal human population
within 50 km of coral reefs
0250 500
120
20
>30
10
0
750
Fig. 1. Estimated plastic debris levels on coral reefs. (A) Modeled association
between plastic debris on coral reefs from surveys of 159 reefs in eight regions [red
squares in (B)] from 2011–2014 and estimated levels of mismanaged plastic waste
(thousand metric tons), assuming that 25% of waste entered the ocean in 2010
from human populations living within 50 km of the coast for each country (12).
Reef locations can be found in table S14. The Asia-Pacific region encompasses 9 of
10 countries with the highest global levels of estimated mismanaged plastic waste
entering the ocean (table S3). Gray shading represents the upper and lower 95%
CIs for the model. (Band C) Modeled plastic debris levels on coral reefs (100 m
−2
),
as projected using the association between estimated mismanaged plastic waste
entering the ocean in 2010 for each sovereign country (12) and plastic debris
surveys between 2011–2014 [shown in (A)].The color scale represents the minima
and maxima model estimates of mismanaged plastic waste on coral reefs from
2010 (table S5). Projections of plastic debris on coral reefs for Indonesia and China
in 2025 were set to the maxima from 2010, owing to the limitations of the
model range. Countries without a coastline are shown in white.
1
Department of Ecology and Evolutionary Biology, Cornell
University, Ithaca, NY 14853, USA.
2
Australian Research
Council Centre of Excellence for Coral Reef Studies, James
Cook University, Townsville, Queensland 4811, Australia.
3
College of Science and Engineering, James Cook University,
Townsville, Queensland, Australia.
4
School of Aquatic and
Fishery Sciences, University of Washington, Seattle, WA
98195, USA.
5
Hawaii Institute of Marine Biology (HIMB),
University of Hawaii at Manoa, Kaneohe, HI 96744, USA.
6
Ecosystem Sciences Division, National Oceanic and
Atmospheric Administration (NOAA) Pacific Islands Fisheries
Science Center, Honolulu, HI 96818, USA.
7
Marine
Programme, Fauna & Flora International, Yangon, Myanmar.
8
Oceans Program, Environmental Defense Fund, New York,
NY 10010, USA.
9
Center for Biodiversity in Peninsular
Thailand, Prince of Songkla University, Hat Yai, Songkhla,
Thailand.
10
Fish Ecology and Conservation Physiology
Laboratory, Department of Biology and Institute of
Environmental Science, Carleton University, Ottawa,
Ontario, Canada.
11
The Nature Conservancy, Raja Ampat
Field Office, North Sorong, West Papua, Indonesia.
12
Faculty
of Marine Science and Fisheries, Hasanuddin University,
Makassar, South Sulawesi, Indonesia.
*Corresponding author. Email: joleah.lamb@cornell.edu
on January 26, 2018 http://science.sciencemag.org/Downloaded from

maxima in Indonesia [25.6 items per 100 ± 12.2 m
2
(here and elsewhere, the number after the ± sym-
bol denotes SEM)] to minima in Australia (0.4
items per 100 ± 0.3 m
2
) (table S2).
Terrestrially derived pollutants have been
implicated in several disease outbreaks in the
ocean (16). However, no studies have examined
the influence of plastic waste on disease risk in
a marine organism. In this work, we visually ex-
amined 124,884 reef-building corals for signs of
tissue loss characteristic of active disease lesions
(15) (fig. S1). We found plastic debris on 17 genera
from eight families of reef-forming corals. When
corals were not in contact with plastic debris, the
likelihood of disease was 4.4 ± 0.2% across all
eight regions (range = 2.8 to 8.4%, generalized
linear mixed model, likelihood ratio test among
regions: c2
7¼10:382, P=0.168) (Fig. 2A). In con-
trast, in the presence of plastic debris, the like-
lihood of disease occurrence in corals increased
significantly by more than a factor of 20 to 89.1 ±
3.2% (generalized linear mixed model: zscore =
27.24, P<0.001, n= 331 transects) (Fig. 2B and
table S3).
Human population size in coastal regions and
the quality of waste management systems largely
determine which countries contribute the
greatest plastic loads entering the ocean, given
that an estimated 80% of marine plastic debris
originates from land (12). Accordingly, we mod-
eled the relationship between our documented
levels of plastic debris on coral reefs (n=437
transects from Australia, Myanmar, Thailand, and
Indonesia) and Jambeck et al.’s estimated levels of
mismanaged plastic waste entering the ocean (12)
from these four countries in 2010 (15)(generalized
linear mixed model: Akaike information crite-
rion = 662.3, z=3.95,P< 0.001) (Fig. 1A, fig. S2,
and table S4). Our model encompasses the range
of mismanaged plastic waste entering the ocean
introduced by coastal populations from 15 of the 17
(88%) sovereign countries in the Asia-Pacific re-
gion (maximum = 804,214 metric tons, minimum =
3472 metric tons), of which 9 are among the top 10
plastic-polluting countries globally (table S5).
Assuming that improvements in waste manage-
ment infrastructure did not occur during our
survey period (2011–2014) and that the plastic
waste emanated from adjacent terrestrial point
sources, we estimate that levels of plastic debris
on coral reefs for each country in the Asia-Pacific
ranged from 0.9 to 26.6 plastic items per 100 m
2
in 2010 (95% CI) (Fig. 1B and table S5). This
amounts to an estimated 11.1 billion items of
plastic on coral reefs across the Asia-Pacific (95%
CI = 1.2 billion to 105.5 billion items, n=15
countries), which is likely underestimated owing
to the exclusion of China and Singapore because
they fall outside of the model range (table S5).
By 2025, the cumulative quantity of plastic
wastepotentiallyenteringthemarineenvironment
from land is predicted to increase by one order of
magnitude (12). Using this projection and assuming
that the area encompassed by coral reefs remains
constant, we estimate that 15.7 billion plastic
items will be entangled on coral reefs across the
Asia-Pacific by 2025 (the “business-as-usual”sce-
nario for global infrastructure: 95% CI = 1.7 billion
to 149.2 billion items) (Fig. 1C and table S5). Ac-
cording to our model, the predicted geographic
distribution of plastic debris on coral reefs does
not change substantially between now and 202 5
(Fig. 1, B and C), but the disparity in quantities of
accumulated plastic waste between developing
andindustrializedcountriesgrowsconsiderably.
For example, plastic debris on coral reefs in-
creases by only ~1% in high-income countries
such as Australia but nearly doubles in a similarly
populated low-income country such as Myanmar
(Fig. 1C and table S5).
Comparative analyses of disease prevalence
among different diseases in the presence versus
absence of plastics can offer insights into poten-
tial mechanisms that increase disease suscepti-
bility in corals. Reef-building corals in contact
with plastic debris were affected by four of six
common diseases globally (17), whereas corals
without plastic debris were affected by all six
diseases but at much lower prevalence levels
(table S6). Disease assemblages on reef-building
corals differ distinctly when contact with plastic
waste is present versus absent, as visualized by a
principal coordinates ordination analysis (15)
(permutational multivariate analysis of variance:
F= 11.86, P<0.001,n= 75 paired transects) (Fig. 3).
In particular, three key diseases associated with
rapid coral mortality increased markedly when
plastic debris was in contact with coral tissues:
Skeletal eroding band disease increased from
1.2 ± 0.1% to 43.9 ± 5.1% (increased likelihood =
24%), white syndromes increased from 1.9 ± 0.2%
to 19.0 ± 4.0% (increased likelihood = 17%), and
black band disease increased from 0.6 ± 0.1% to
14.7 ± 3.9% (increased likelihood = 5%) (tables S7
to S10).
Given the widespread distribution of plastic
debris on coral reefs and the consequent increased
Lamb et al., Science 359, 460–462 (2018) 26 January 2018 2of3
Likelihood of disease (%)
Without plastic debris
0 10025 50 75
With plastic debris
Plastic debris on
coral reefs (100 m
-2
)
Group Mean
SEM
MYAN 1
THAIL 2
INDO 3
INDO 4
INDO 5
AUST 6
AUST 7
AUST 8
0 10025 50 75
20
>30
10
0
Fig. 2. Plastic waste influences disease susceptibility of reef-building corals. (Aand B)Box
(median and 50% quantile) and whisker (95% quantile) plots of coral disease likelihood for each of
eight regions in four countries in the Asia-Pacific when no plastic waste is present (A) (n= 362
transects) and when plastic waste is present (B) (n= 75 transects). The red line represents the mean
and the light red bar denotes ±1 SEM across all eight regions. Boxes are shaded according to model
estimates of plastic debris on coral reefs per 100 m
2
from Fig. 1C. MYAN, Myanmar; THAIL, Thailand;
INDO, Indonesia; AUST, Australia.
Fig. 3. Reef-building corals with plastic
debris have different disease assem-
blages than corals without plastic
debris. Multivariate spatial representation
of the relative abundance and composition
of coral disease assemblages, as determined
by a principal coordinates analysis (PCoA)
(n= 75 paired transects). Vectors for each
group illustrate the median spatial distance
within the group. Disease assemblages
represent six diseases—skeletal eroding
band, white syndromes, black band,
growth anomalies, brown band, and
atramentous necrosis—recorded commonly
across the globe.
PCoA 1
PCoA 2
−0.4 −0.2 0.0 0.2 0.4
−0.2
0.0
0.2
0.6
0.4
With plastic debris
Without plastic debris
RESEARCH |REPORT
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likelihood of coral mortality from disease, we
evaluated the potential for plastic debris and
disease to affect structural complexity provided
by habitat-forming corals. The structural com-
plexity formed by corals underpins the avail-
ability of microhabitats for coral reef–associated
organisms (18). We grouped coral species into
three broad classifications based on the increas-
ing structural complexity of their colony mor-
phologies (massive < branching < tabular) (table
S11) and determined that plastic debris is eight
times more likely to affect reef corals with greater
structu ral complexity (tabular and branching
versus massive, n= 348 transects; posterior prob-
ability functions) (Fig. 4A and table S12). Massive
coral morphologies are less likely to maintain
contact with plastic debris; however, they exhibit
the greatest increase in disease risk when this
occurs (likelihood is increased by 98%) (Fig. 4, B
to D, and table S13).
Our study shows that plastic debris increases
the susceptibility of reef-building corals to dis-
ease. Plastics are a previously unreported cor-
relate of disease in the marine environment.
Although the mechanisms remain to be inves-
tigated, the influence of plastic debris on dis-
ease development may differ among the three
main global diseases that we observed. For ex-
ample, plastic debris can cause physical injury
and abrasion to coral tissues by facilitating in-
vasion of pathogens (19) or by exhausting resources
for immune system function during wound-healing
processes (20). Experimental studies show that
artificially inflicted wounds to corals are fol-
lowed by the establishment of the ciliated pro-
tozoan Halofolliculina corallasia, the causative
agent of skeletal eroding band disease (21).
Plastic debris could also directly introduce
resident and foreign pathogens or may indirectly
alter beneficial microbial symbionts. Cross-ocean
bacterial colonization of polyvinylchloride (PVC)
is dominated by Rhodobacterales (22), a group
of potentially oppo rtunistic pathogens asso-
ciated with outbreaks of several coral dis-
eases (23). Additionally, recent studies have
sh ow n t hat experimental shading and low-light
microenvironments can lead to anoxic conditions
favoring the formation of polymicrobial mats
characteristic of black band disease (24).
By disproportionately reducing the composi-
tion or abundance of structurally complex reef-
building coral species through disease, widespread
distribution of plastic waste may have negative
consequences for biodiversity and people (25).
For example, on coral reefs, the loss of structural
habitat availability for reef organisms has been
shown to reduce fishery productivity by a factor
of 3 (26).
Climate-related disease outbreaks have already
affected coral reefs globally and are projected to
increase in frequency and severity as ocean tem-
peratures rise (27). With more than 275 million
people relying on coral reefs for food, coastal
protection, tourism income, and cultural impor-
tance (2), moderating disease outbreak risks in
the ocean will be vital for improving both human
and ecosystem health. Our study indicates that
decreasing the levels of plastic debris entering
the ocean by improving waste management in-
frastructure is critical for reducing the amount of
debris on coral reefs and the associated risk of
disease and structural damage.
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ACKNO WLE DGME NTS
WethankS.Atto,S.Beveridge,F.J.Pollock,G.Torda,A.Tracy,
A.Wenger,C.Wood,S.Yusuf,andS.Piromvaragorn for their a ssistance.
This research was supported by The Nature Conservancy NatureNet
Science Fellowship, an AIMS@JCU (Australian Institute of Marine Science
at James Cook University) Postgraduate Scholarship, the NSF Ecology of
Infectious Marine Disease Research Coordination Network [Division of
Ocean Sciences (OCE) award 1215977], the Capturing Coral Reef and
Ecosystem Related Services (CCRES) Project funded by the Global
Environment Facility and the World Bank (project ID P123933), NOAA/
National Ocean Service (NOS)–HIMB agreement code MOA-2009-039,
Australian Research Council (grant CEO561435), and the Environmental
Defense Fund Innovation for Impact partnership with the At kinson Center
for a Sustainable Future at Cornell Univ ersity. Surveys in Australia were
conducted under Great Barrier Reef Marine Park Authority permi ts G10/
33393.1 and G12/35232.1. All data and cod e to understand and assess
the conclusions of this research are available in the main text,
supplementary materials, and via the Dryad Digital Repository (https://
doi.org/10.5061/dryad.mp480).
SUPPLEMENTARY MATERIALS
www.sciencemag.org/content/359/6374/460/suppl/DC1
Materials and Methods
Figs. S1 and S2
Tables S1 to S14
References (28–30)
31 October 2017; accepted 21 December 2017
10.1126/science.aar3320
Lamb et al., Science 359, 460–462 (2018) 26 January 2018 3of3
10
2.2 2.8 4.2
4
0.02 0.1 0.4 44 91 98 85 99
10
B
Disease likelihood
without plastic debris (%)
Likelihood of contact
with plastic debris (
‰)
Increase in disease likelihood
with plastic debris (%)
Disease likelihood
with plastic debris (%)
Massive
Branching
Tabular
00
0100 100
0
Fig. 4. Coral morphological complexity influences risk to plastic debris
and disease. (Ato D) Posterior probability density functions of coral species
grouped into three broad morphological classifications. Structural complexity is
determined by coral species (18); see table S11 for classifications. Minimum,
maximum, and peak values are shown for each structural complexity classification
group: massive (dark red), branching (medium red), and tabular (light red). For
ease of comparison, the inset in (C) represents the likelihood of disease without
plastic debris [as shown in (B)].
RESEARCH |REPORT
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Plastic waste associated with disease on coral reefs
A. Kelly, Awaludinnoer Ahmad, Jamaluddin Jompa and C. Drew Harvell
Joleah B. Lamb, Bette L. Willis, Evan A. Fiorenza, Courtney S. Couch, Robert Howard, Douglas N. Rader, James D. True, Lisa
DOI: 10.1126/science.aar3320
(6374), 460-462.359Science
, this issue p. 460Science
and anoxia, giving pathogens a foothold for invasion.
increased 20-fold once a coral was draped in plastic. Plastic debris stresses coral through light deprivation, toxin release,
entangled in the reefs. The more spikey the coral species, the more likely they were to snag plastic. Disease likelihood
surveyed 159 coral reefs in the Asia-Pacific region. Billions of plastic items wereet al.effects of plastic waste. Lamb
Coral reefs provide vital fisheries and coastal defense, and they urgently need protection from the damaging
Corals wrapped in plastic
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MATERIALS
SUPPLEMENTARY http://science.sciencemag.org/content/suppl/2018/01/24/359.6374.460.DC1
REFERENCES http://science.sciencemag.org/content/359/6374/460#BIBL
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