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Ann. N.Y. Acad. Sci. ISSN 0077-8923
ANNALS OF THE NEW YORK ACADEMY OF SCIENCES
Issue: The Year in Ecology and Conservation Biology
Sewage pollution: mitigation is key for coral reef
stewardship
Stephanie L. Wear1,2 and Rebecca Vega Thurber3
1Institute of Marine Sciences, University of North Carolina at Chapel Hill, Morehead City, North Carolina. 2The Nature
Conservancy, Beaufort, North Carolina. 3Department of Microbiology, Oregon State University, Corvallis, Oregon
Address for correspondence: Stephanie L. Wear, The Nature Conservancy, 135 Duke Marine Lab Road, Beaufort, NC 28516.
swear@tnc.org
Coral reefs are in decline worldwide, and land-derived sources of pollution, including sewage, are a major force
driving that deterioration. This review presents evidence that sewage discharge occurs in waters surrounding at
least 104 of 112 reef geographies. Studies often refer to sewage as a single stressor. However, we show that it is
more accurately characterized as a multiple stressor. Many of the individual agents found within sewage, specifically
freshwater, inorganic nutrients, pathogens, endocrine disrupters, suspended solids, sediments, and heavy metals,
can severely impair coral growth and/or reproduction. These components of sewage may interact with each other
to create as-yet poorly understood synergisms (e.g., nutrients facilitate pathogen growth), and escalate impacts of
other, non-sewage–based stressors. Surprisingly few published studies have examined impacts of sewage in the field,
but those that have suggest negative effects on coral reefs. Because sewage discharge proximal to sensitive coral
reefs is widespread across the tropics, it is imperative for coral reef–focused institutions to increase investment in
threat-abatement strategies for mitigating sewage pollution.
Keywords: marine conservation; sanitation; coral disease; eutrophication; multiple stressors; reef management
Introduction
Coral reefs play a critical role in coastal ecosystem
function in the tropics, providing food and habitat
for 550,000 to 1,330,000 species.1Along with the
inherent biodiversity these habitats support, reefs
built by corals also provide many valuable services
for humans, including shoreline protection, liveli-
hoods from ecotourism, fisheries production, and
a living synthesis engine of biomedical and indus-
trially valuable compounds.2–5 The value of these
services varies globally, but is estimated at over $31
billion (US$, 2014) annually for all reefs combined.6
Unfortunately, reefs and the many benefits they pro-
vide are under severe threat, with evidence of a gen-
eral pattern of habitat degradation.7,8
Spatial variation and forces behind coral
reef decline
Coral reefs are exposed to a multitude of stressors
emanating from human activities7–10 and, as a result,
have experienced drastic declines in spatial coverage
and diversity over the past 50 years.7,8 At a regional
level in the Indo-Pacific, live coral cover has declined
at an annual rate of 1% from the early 1980s to 2003,
while in the Caribbean, the annual rate of coral cover
loss was 1.5% between 1977 and 2001.11 Recen t work
cataloging the status of reefs has estimated that we
have functionally lost at least 25% of coral reefs glob-
ally, and one-third of all coral species are threatened
with extinction.12 Chief among threats identified in
Reefs at Risk Revisited (RRR) are overfishing, pollu-
tion, coastal development, and climate change.8For
example, increasing temperature of surface waters
from climate change has led to increased bleach-
ing events and subsequent reef loss.13 Bleaching
owing to elevated water temperatures is perhaps
the most notable stress, with some reefs experienc-
ing over 85% mortality in the 1998 mass bleaching
event.14–17 While the 1998 bleaching event resulted
in significant losses, coral reefs were already in a
state of decline when this event occurred.10,18 The
doi: 10.1111/nyas.12785
1
Ann. N.Y. Acad. Sci. xxxx (2015) 1–16 C2015 The Authors. Annals of the New York Academy of Sciences
published by Wiley Periodicals Inc. on behalf of The New York Academy of Sciences
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and
distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
Sewage pollution and coral reef stewardship Wear & Thurber
additive and synergistic effects of long-term over-
fishing, chronic coastal pollution, and poorly regu-
lated coastal development had already compromised
coral reefs, making it difficult for reefs to withstand
more stressful conditions associated with increasing
frequency and intensity of bleaching events.10,18,19
Over the past two decades, the conservation
community has generally considered overfishing as
the threat to coral reefs that warrants the most
attention.8For example, RRR emphasizes that more
than 55% of the world’s reefs are under imme-
diate threat from overfishing,8which can lead to
phase shifts from coral-dominated reefs to algal-
dominated reefs as the number of algae-eating fish
decreases significantly.20 Halpern et al.21 also suggest
that overfishing is one of the most severe causes of
coral reef decline. The extensive scientific literature
on overfishing has prompted coral reef management
responses that include limiting or banning fishing in
some areas, regulations that prohibit the take of cer-
tain key fish species, and global efforts to influence
consumer choice by limiting the demand for ecolog-
ically important species. Notably, the threat to coral
reefs from pollution and eutrophication, although
potentially just as important as overfishing, as sug-
gested by the assessments of RRR8and Halpern
et al.,21 hasreceivedmuchlessattentionfromcon-
servation organizations (S. Wear, personal obser-
vation). Reasons for this disparity may include the
practical challenges of dealing with a large-scale dif-
fuse threat, the diversity of pollutants involved, the
high cost of water-treatment facilities, and bureau-
cracy. The solutions to reducing and understand-
ing the exact impacts of coastal pollution, where
it is likely to be strong, have been lacking because
of the inherent difficulties of monitoring and eval-
uating nonpoint sources of pollution, along with
jurisdictional issues such as agency and private land
conflicts.
The largest component of coastally derived pol-
lution is sewage.22–25 Mostcoralreefsarelocated
along the shorelines of developing countries, where
tertiary sewage treatment is rare. Most sewage
enters tropical waters as either poorly or completely
untreated discharge or stormwater runoff.25,26 In
fact, the United Nations Environmental Program
estimated that 85% of the wastewater entering the
sea in the Caribbean is untreated.27 As our global
population likely expands by 2 billion over the next
35 years,28 the amount of sewage polluting reefs
will also increase. It is thus critically important to
understand the role of sewage discharge in coral reef
declines and identify ways to minimize its impact
on reef health. In this review, we synthesize what is
known about the composition of sewage and how
each component may affect coral reef health. We
explore interactions between and among these com-
ponents to evaluate synergisms. We also present a
synthesis of previously conducted studies on the
impacts of sewage discharge on coral reefs. Finally,
we present a summation of the geographic extent of
sewage pollution, in regions where coral reefs occur.
What is in sewage and how do those
components affect corals?
Most reports addressing the impact of sewage on
coral reefs cite high inorganic nutrient content
as the primary reason for alarm—as those nutri-
ents could lead to increased growth of algae and
coral diseases.29,30 However, sewage in its raw form
contains many more compounds than just inor-
ganic nutrients (e.g., see Refs. 24, 25, and 31). In
particular, sewage discharged into tropical coastal
seas contains hundreds of different compounds, the
most common of which are freshwater, inorganic
nutrients, pathogens, endocrine disrupters, sus-
pended solids, sediments, heavy metals, and other
toxins.25,31 Below, we describe each of these con-
stituents in detail and briefly summarize what is
known about negative impacts on coral reefs and
the mechanism(s) underlying the impact (Table 1).
Importantly, this understanding does not come
from studies on sewage itself, but rather from work
investigating how explicit sewage components (e.g.,
freshwater, ammonium) affect corals.
Freshwater
The primary component of sewage is freshwater, a
known stressor to corals. Although there are sur-
prisingly few studies examining impacts of freshwa-
ter on coral health, classic laboratory studies con-
ducted over 80 years ago revealed that most corals
die after prolonged exposure to fresh or brackish
water sources and that the lower salinity tolerance
of corals is 15–20 ppt.32 In the field, the effect of
freshwater discharge onto coral reefs has been stud-
ied in a limited number of cases using correlational
methods.32,33 In these studies, increased freshwater
input into coastal waters associated with stormwater
runoff was correlated with rapid drops in near-shore
2Ann. N.Y. Acad. Sci. xxxx (2015) 1–16 C2015 The Authors. Annals of the New York Academy of Sciences
published by Wiley Periodicals Inc. on behalf of The New York Academy of Sciences
Wear & Thurber Sewage pollution and coral reef stewardship
Tab le 1. Examples of coral reef (corals and associated organisms) responses to common stressors found in sewage
Stressor Response References
Freshwater Increased coral mortality (with lowered salinity for
>24 h).
32, 33
Dissolved inorganic nutrients
(ammonium, nitrite +
nitrate, and phosphate)
Increased coral bleaching, increased coral disease
prevalence and severity, decreased coral fecundity,
algal overgrowth, decreased coral skeletal integrity,
decreased coral cover and biodiversity, and increased
phytoplankton shading.
30, 47, 50, 51, 54, 55, 57, 70,
107
Endocrine disrupters (e.g.,
steroidal estrogens)
Reduction in coral egg–sperm bundles, slowed coral
growth rates, coral tissue thickening.
95, 103, 105
Pathogens Source of white pox disease pathogen for corals and
associated mortality, and increased pathogenicity in
corals.
88–90
Solids Reduced photosynthesis of coral symbionts, coral
species richness, coral growth rates, coral
calcification, coral cover, and coral reef accretion
rates, and increased coral mortality.
107–112
Heavy metals Coral mortality, coral bleaching, reduction of basic
functions such as respiration and fertilization success;
Fe2+may increase growth of coral disease.
126–128
Toxins Lethal and sublethal effects on corals—highly variable
and dependent on specific toxin. Reduced
photosynthesis of coral symbionts, coral bleaching,
coral mortality, reduced coral lipid storage, reduced
coral fecundity, death of coral symbionts, and
decreased coral growth.
133 and references therein
salinity and, in turn, significant loss of nearby corals.
Reef mortality associated with these flood-related
reductions in salinity has been documented around
the world (e.g., see Ref. 32). Understanding the spe-
cific limits and tolerances of corals to freshwater
exposure, however, is relatively underexplored.
Nutrients
Sewage discharging into coastal tropical waters
contains very high concentrations of inorganic
nutrients, such as ammonium, nitrite, nitrate, and
phosphate.Anumberofstudieshaveexaminedthe
effects of these compounds on specific components
of coral health. Impacts can be categorized as either
direct, having effects on the coral animal or its
symbionts, or indirect, whereby nutrients influence
other aspects of the reef that in turn negatively
affect coral health. One of the most influential
single mechanisms is indirect, whereby nutrient
enrichment enhances macroalgal overgrowth,
killing corals and thereby removing a foundation
species. A growing body of new literature has also
examined direct impacts, such as how inorganic
nutrients modify microbial communities found on
and in corals, coral symbionts, and calcification
rates. Here, we briefly review key findings related
to each of these topics.
Nutrients and algae. Since tropical reefs are gen-
erally nutrient poor or oligotrophic, any significant
input of limiting macronutrients into coastal waters
could cause shifts in reef community composition.34
Most research on nutrient impacts on reefs has
focused on the direct effects of inorganic nutrients
on primary producers, such as phytoplankton or
macroalgae, both of which compete with corals for
light and space. For example, increases in nutrient
concentrations can facilitate large, often monospe-
cific blooms of algae.35–37 It is also well documented
that increasing inorganic nutrient levels increases
macroalgal cover on reefs, to the detriment of coral
cover.20,29,38–43
This reduction in coral cover is owing to the
increased proliferation of macroalgal biomass in the
presence of elevated dissolved inorganic nitrogen,
which translates to increased competitive ability for
3
Ann. N.Y. Acad. Sci. xxxx (2015) 1–16 C2015 The Authors. Annals of the New York Academy of Sciences
published by Wiley Periodicals Inc. on behalf of The New York Academy of Sciences
Sewage pollution and coral reef stewardship Wear & Thurber
macroalgae as they interact with corals and com-
pete for space.44,45 This increase in macroalgal com-
petition, when combined with nutrient pollution,
may further reinforce a coral-depauperate state by
reducing the growth and survival of adult corals46–48
and preventing the recruitment and establishment
of juveniles.45,48 Increased macroalgal growth and
competitive displacement of corals in response to
increasing nutrients from human activities has been
documented in enrichment studies in the Caribbean
Sea and the Indian and Pacific Oceans.29,49
Nutrients, coral disease, and bleaching. Nutrient
enrichment has also been hypothesized to be a
driver of coral disease and bleaching. Recent
studies on the Great Barrier Reef50 andinthe
Florida Keys51 foundapositivecorrelationbetween
bleaching prevalence and inorganic nitrogen (N)
levels. Field surveys have also found that coral
disease prevalence is often positively correlated
with ambient seawater nutrient concentrations.52,53
For example, increasing nutrient availability is pos-
itively correlated with increased disease progression
rates (i.e., the rate of movement of the disease over
a coral’s surface) of some coral diseases, such as
yellow blotch and black band disease.54,55 Recent
experimental evidence has confirmed predictions
from these observational studies and shown that
nutrients can cause an increase in both the preva-
lence of coral disease and the extent of bleaching on
natural reefs.30 Researchers have enriched replicate
portions of a coral reef with inorganic N and
phosphorus (P), to levels within the nutrient ranges
experienced by contaminated reefs.56 After 3 years
of this nutrient enrichment, disease incidence in
corals increased more than twofold and bleaching
prevalence in one coral species increased by more
than 3.5-fold.30 Perhaps most importantly, after
termination of nutrient additions, there was a
return to preenrichment water quality, followed by
rapid recovery (within 6 months) of the enriched
reef sites, such that disease and bleaching levels
returned to those in control reef sites lacking the
enrichment treatment. These findings demonstrate
that measures to reduce inorganic nutrient pollu-
tion through water quality mitigation efforts may
successfully reduce coral disease and bleaching
levels, perhaps even very rapidly.
Nutrients and coral growth. Nutrients have
long been hypothesized to reduce coral growth
rates. A recent meta-analysis showed that
exposure to nitrate and ammonium over a
wide range of concentrations (0.5–26 M)
generally had negative effects on corals, but
increased P (0.11–26 M) actually enhanced
calcification.57 Nevertheless, although elevated P
concentrations increased calcification rates, this
response also involved losses of skeletal integrity.
The effects were also context dependent such that
different morphologies (mounding versus branch-
ing) and different species of corals exhibited varying
calcification responses and varying impacts of N,
depending on type (nitrate or ammonium) and
source (natural or anthropogenically derived).57
The variable effects of nutrient pollution across
coral morphology and species carries implications
for how different habitat types will uniquely
respond to nutrient enrichment. In particular,
mounding and poritid corals were shown to be
more susceptible to the negative effects of increased
nutrients, and habitats or ecosystems dominated
by these taxa are more likely to suffer impacts from
increased inorganic nutrient concentrations that
often accompany reduced water quality.
Nutrients can also decrease coral growth by act-
ing on the autotrophic algal partner Symbiodinium,
which is a symbiont in corals. Nutrients have long
been hypothesized to decrease coral growth rates via
bleaching, through elevating the abundance of algal
symbionts.58,59 Increased symbiont density leads to
corresponding increases in reactive oxygen species,
which may result in damage to host cells and/or
death and expulsion of the symbiont.60 It is this loss
of the pigmented Symbiodinium that causes coral
bleaching, decreased growth rates, and even whole-
colony mortality. It should be noted, however, that
recent research has revealed that increased nutrient
levels do not always have a negative impact on coral
growth but instead can have a unimodal relation-
ship, where increasing nutrient levels first increase
coral growth but then decrease coral growth as levels
of nutrients rise.61
Nutrients and microbial communities. Coral-
associated microbes (i.e., eubacteria and archaea)
have a multitude of context-dependent roles in
health and physiological homeostasis of sclerac-
tinian corals.62,63 For example, mucus-associated
bacteria are believed to regulate the settlement
and/or growth of opportunist microbes by
4Ann. N.Y. Acad. Sci. xxxx (2015) 1–16 C2015 The Authors. Annals of the New York Academy of Sciences
published by Wiley Periodicals Inc. on behalf of The New York Academy of Sciences
Wear & Thurber Sewage pollution and coral reef stewardship
occupying space or producing effective
antibiotics.64–66 Alterations in ambient condi-
tions, such as water temperature and nutrient
concentrations, have been shown to induce shifts
in the associated microbes or microbiome of a
coral.67,68 These shifts can be the result of both
direct and indirect effects of inorganic nutrients.
For example, tank experiments suggest that addi-
tion of inorganic N can induce growth of potential
bacterial pathogens.68,69 An increase in nutrients
also can stimulate growth of macroalgae and turf
algae,70 which have been shown to have multiple
negative effects on the coral microbiome, such as
depletion of local oxygen concentrations,37,71,72
transferal of allelotoxins,73–76 and transmission or
vectoring of pathogens.77,78 Shifts in the micro-
biome can ultimately lead to coral health declines
and sometimes death.37,62,79
Pathogens
Coral disease has increased in prevalence in the
Caribbean, with as much as 20% of reefs affected
in some places.80 While the Pacific has not yet expe-
rienced the devastating consequences of coral dis-
eases, it is clear that many diseases are present, and
the problem is expected to grow with environmental
change (e.g., see Refs. 81 and 82). For example, at
least seven diseases have been documented in Aus-
tralia’s Great Barrier Reef, including cyanobacterial,
protozoan, and Vibrio spp. infections.80 The impacts
of disease on corals can be profound, ranging from
minor tissue loss to entire-colony mortality. For
example, in the 1980s, the two dominant Acrop-
orid species, Acroporid palmata and Acroporid cervi-
cornis, experienced Caribbean-wide die-offs owing
to white band disease, with estimates reaching as
high as 95% of colonies lost.83,84 Such losses are
unprecedented and have led to dramatic manage-
ment responses, including the listing of both taxa
under the Endangered Species Act.
Recent work has started to link certain environ-
mental conditions,30,54,85 as well as a changing cli-
mate, to the emergence of disease.86,87 However,
we understand very little about reservoirs for coral
disease. One such likely reservoir for pathogens is
sewage. In fact, sewage effluent has been identified
as the source of the pathogen complex that causes
white pox disease in Caribbean corals.88–90 Using
Koch’s postulates, Patterson et al.88 first identified
Serratia marcescens as the disease-causing agent for
white pox disease. At the time of this study, the
elkhorn coral, A. palmata, was experiencing a major
die-off in the Florida Keys, with more than 70% of
coral cover lost owing to white pox disease.88 Dur-
ing a subsequent outbreak of white pox disease in
2003, a unique strain of S. marcescens was identified
(PDR60) from samples taken from live A. palmata,
as well as two other species of non-Acroporid corals,
reef water, and nearby sewage sources.89
In their most recent publication, Sutherland
et al.90 used experimental laboratory manipulations
to demonstrate that sewage was indeed the source of
the disease, and that a human strain of the pathogen
was the causal agent. These findings marked the first
time that a human pathogen has been demonstra-
bly transmitted to a marine invertebrate, provid-
ing strong evidence for the linkage between sewage
exposure and disease in the marine environment.
While evidence showing that sewage is an impor-
tant disease reservoir is limited to one type of dis-
ease and its associated causal agent, the potential for
discovery of more examples is considerable, given
the sheer numbers of microbes and viruses present
in the average human gut and consequently in the
average sewage effluent (e.g., see Refs. 91–93).
Endocrine disrupters
Endocrine disrupters are common pollutants in
coastal waters. They include both natural and syn-
thetic estrogens, polychlorinated biphenyls (PCBs),
plasticizers, pharmaceuticals, parabens, phthalates,
dioxins, petrochemicals, organochlorinated pesti-
cides, microplastics, and detergents.94–98 Endocrine
disrupters are chemicals with the ability to disrupt
the endocrine or hormone system in living organ-
isms. They can act on multiple processes in ani-
mals, including reproduction, immune response,
and growth.99 Endocrine disrupters are commonly
identified in sewage effluent delivered by human
excretion,96 as well as through general household
wastewater. They have also been detected in sedi-
ments adjacent to coral reefs.95,100,101
Both distance from the source of sewage and the
physical characteristics of an area affect the concen-
trations of endocrine disrupters.96,100,102 As is the
case for some other pollutants, well-flushed areas
have lower concentrations of endocrine disrupters,
whereas areas that are enclosed, or semi-enclosed,
tend to have higher concentrations.96 Studies on
the effects of endocrine disrupters on corals have
5
Ann. N.Y. Acad. Sci. xxxx (2015) 1–16 C2015 The Authors. Annals of the New York Academy of Sciences
published by Wiley Periodicals Inc. on behalf of The New York Academy of Sciences
Sewage pollution and coral reef stewardship Wear & Thurber
shown that impacts are similar to those they have
on other organisms (i.e., suppressing growth and
reproduction).95,103 Early work on understanding
the role of endocrine disrupters, specifically
steroidal estrogens, established the presence of
estrogens in the water column and in the tissues
and skeletons of corals.96,104–106 Subsequent studies
demonstrated that corals take up estrogens, incor-
porate them into their tissues and skeletons, and
metabolize them.103 The metabolic mechanisms
are poorly understood, but what has been shown
is that certain estrogens affect coral reproductive
abilities, growth rates, and morphological features.
For example, Tarrant et al.95 showed that additions
of estradiol to Montipora spp. over 3 weeks resulted
in a 29% reduction of egg–sperm bundles, whereas
additions of estrone to Porites spp. over 2–8 weeks
slowed growth rates by 13–24%. Tarrant et al.95
also added estrone to Montipora spp. nubbins over
several weeks, and found an increase in tissue
thickness. Much more study is needed to better
understand these dynamics, so that informed
strategies for minimizing exposure to these and
other endocrine disrupters can be developed.
Suspended solids and sedimentation
Both suspended solids and sediments accom-
pany sewage discharge and are threats to coral
health.25, 107–110 Sewage typically contains high con-
centrations of suspended solids, primarily organic.
Suspended solids increase turbidity and block
sunlight, which can reduce growth of coral
symbionts.108,111,112 Corals may survive for many
days under severely reduced sunlight, but after a few
weeks, excessive shading can result in reduced pho-
tosynthetic activity, growth, and, ultimately, coral
cover.113 When chronic shading owing to increased
suspended solids occurs, this can result in coral
depth distribution shifts.114 Thus, the impact of sus-
pended solids on corals will depend on how long
solids remain in the water column and how much
sunlight they block.
High rates of sedimentation may also co-occur
with sewage discharge, especially coinciding
with storm events.115 The range of impacts
from prolonged sediment cover includes shading
and thus suppression of food production by
coral symbionts, smothering of corals,108,116,117
energetic losses owing to effort spent to reject
sediments,118 and disease.110,119 Corals differ in their
susceptibility to sedimentation based on differences
in morphology,117,120,121 size,122 and ability to reject
sediments.120 Regardless of any coping mechanisms
that corals may have, sedimentation impacts
are pervasive. Fabricius conducted an extensive
review on field studies that provided evidence
that sedimentation has negatively affected reefs
across all major coral reef geographies (see Table
1 in Ref. 107). This work also highlighted specific
stress responses of individual corals (e.g., reduced
growth rates, reduced calcification, and increased
mortality), communities (e.g., reduction in species
richness and coral cover), and ecosystems (e.g., net
productivity and accretion rates) to different levels
of sedimentation.
Besides the physical stress that sedimentation and
suspended solids can generate, there may also be
chemical stress generated, especially from sewage-
derived sediments, because they contain a wide
range of compounds. For instance, suspended solids
associated with sewage that eventually settle on
corals often have a different profile, both in chemical
composition and toxicology, from those originat-
ing from other sources, such as agricultural runoff
and natural erosion flows.24 Suspended solids may
contain toxic compounds and high levels of nutri-
ents, each of which can result in negative responses
in corals, such as disease and mortality.25,123 The
highly organic particles derived from sewage can
chemically stress corals by greatly increasing bio-
logical oxygen demand in surrounding waters, as
bacterial consumption of oxygen rises with increas-
ing availability of organic material.25,123
Heavy metals
Heavy metals are commonly present in sewage
worldwide.124 Metals routinely found in sewage
include mercury, lead, cadmium, chromium, cop-
per, nickel, zinc, cobalt, and iron.124,125 In general,
increasing levels of heavy metals in the tissues of
organisms interfere with metabolism and influence
the activity of a wide range of enzymes, suppressing
important physiological processes, such as respira-
tion and nerve communication. Numerous stud-
ies have shown that exposure to elevated levels of
metals can result in coral mortality, bleaching, and
decreased fertilization success.126,127 Heavy metals
also have the potential to damage corals by increas-
ing success of certain microbes. For example, Fe2+,
which is common in raw sewage, plays an important
6Ann. N.Y. Acad. Sci. xxxx (2015) 1–16 C2015 The Authors. Annals of the New York Academy of Sciences
published by Wiley Periodicals Inc. on behalf of The New York Academy of Sciences
Wear & Thurber Sewage pollution and coral reef stewardship
role in increasing both the virulence of pathogenic
microbes (e.g., Vibrio spp.), and the growth rates
of microalgae. This occurs because Fe2+is a lim-
iting nutrient for microbe reproduction, and thus
its addition leads to increased microbial growth.128
When iron is in excess and freely available, it is taken
up by pathogenic microbes, allowing them to fur-
ther multiply and increase their success in attacking
and infecting live corals.128 Finally, increases in this
essential bacterial micronutrient have been impli-
cated in altering reef community structure and func-
tion in extremely oligotrophic environments, such
as isolated coral atolls.129
Other toxins
The range of other toxins potentially present in
sewage is wide, but which toxins actually are
present is dependent on local conditions, such
as type and abundance of local industries and
agriculture. Chemicals commonly found in sewage
beyond the metals and endocrine disrupters
discussed above include PCBs, chlorine, pesti-
cides, herbicides, petroleum hydrocarbons, and
pharmaceuticals.24,25, 130–132 Numerous laboratory
studies and field studies have examined the impacts
of these toxins on corals. This work was summarized
by van Dam et al.,133 who reported that the response
of corals depended both on the type of toxin and its
concentration, with responses varying from mor-
tality, to bleaching, to reduced lipid concentrations
(see Table 1 for examples of responses).
Field evidence linking sewage exposure
and coral reef health
The section above reviews the impacts that individ-
ualcomponentsofsewagehaveoncoralreefhealth
and suggests that sewage as a whole has the potential
to have strong negative impacts. However, this pre-
diction is based on studies that did not experimen-
tally expose corals in the field to sewage. To evaluate
the findings of field experiments and observational
studies assessing the effects of sewage and its con-
stituents on coral reefs, we conducted a search of
the literature (Web of Science with following search
terms: TOPIC: “coral reef*” and TOPIC: “sewage”
and TOPIC: “pollution”). Remarkably, we did not
find one experimental field study that investigated
impacts of sewage on coral reef health. Most stud-
ies looking at linkages between sewage and coral
reefs focused on identifying indicators of sewage
presence and intensity, rather than on the actual
impacts of sewage on coral reef constituents, the
general untested assumption being that sewage had
a negative impact, and so should be monitored and
abated.134–139 We did, however, identify eight obser-
vational studies that surveyed coral reef areas with
substantial sewage input and compared them to
nearby, environmentally similar areas with little or
no known suspected sewage input.115, 140–147
In each of these correlational studies, scientists
investigated how the condition of coral reef commu-
nities varied with decreased water quality (e.g., fecal
coliform counts, turbidity, and inorganic nutrients)
associated with sewage outflows. In seven of the
eightstudies,anegativeimpactofsewageonreefs
was implicated, and, in one study, no effect was
suggested. Below, I briefly review the findings of
these studies. Caution should be taken in interpret-
ing the results of these studies, as none used the most
robust design (i.e., before–after–control–impact)148
for correlational testing of contaminant effects.
Nonetheless, taken together, their quantitative
results allow us to make informed hypotheses about
the probable impacts of sewage on coral health.
Two of these observational studies focused on
the incidence of coral disease in response to sewage
exposure. Kaczmarsky et al.141 examined two differ-
ent sites in St. Croix, U.S. Virgin Islands—a sewage-
impacted site, and an ecologically and geologically
similar site nearby with no known sewage expo-
sure. Water quality sampling by the Virgin Islands
Department of Planning and Natural Resources
showed high counts of fecal coliforms (1460/100
mL) after a sewage overflow event at the sewage-
impacted site, but no indication of fecal coliforms
(0/100 mL) at the nonimpacted site (approximately
1.5 km from the sewage pipe). The authors con-
ducted surveys to determine the prevalence of black
band disease and white plague type II at both sites,
and found significantly (P<0.0001) more disease
cases at the sewage-impacted sites, with 7 of the 10
species surveyed showing an increased incidence of
disease. Redding et al.147 reported similar trends of
increasing coral disease with exposure to sewage. In
this study on reefs in Guam, the authors found that
increasing sewage (estimated from measurements
of sewage-derived N) correlated significantly with
increases in white syndrome disease on Porites spp.
and that the level of ␦15Nwasastrongpredictorof
severity of this disease.147
7
Ann. N.Y. Acad. Sci. xxxx (2015) 1–16 C2015 The Authors. Annals of the New York Academy of Sciences
published by Wiley Periodicals Inc. on behalf of The New York Academy of Sciences
Sewage pollution and coral reef stewardship Wear & Thurber
Five other field studies implicated increased
sewage exposure as the factor generating inferred
changes in community structure on reefs, with
the most common responses being an increase in
macroalgae and a decrease in coral cover.115,144,146
For example, a study examining two bays in Thai-
land, one sewage impacted and the other not,
found that the sewage-impacted bay had significant
increases in turbidity and inorganic nutrients.115,143
The authors then correlated these differences to
changesatmultipleecologicallevelsoforganiza-
tion in the nearby coral reef community, including
increased macroalgal density and diversity, reduced
cover of reef-building corals, and reductions in fish
abundance on the reef.115,143 Similarly, a study of
reefs in Taiwan that examined the impacts of sewage
found that higher levels of sewage (as estimated by
measurements of nutrient and suspended sediment
levels) were linked to algal blooms and sediment
smothering of corals in shallow areas.145 Finally,
during a bleaching event in 1995, scientists exam-
ined the interactions between bleaching and sewage
pollutioninCurac¸ao and found that the highest
levels of coral tissue mortality occurred on reefs
chronically exposed to sewage.142
Our search yielded only one published field
study purporting to find no detectable effect of
sewage outflow on coral communities. Grigg used
a control–impact design to investigate effects of
sewage outflow coming from pipes deployed in the
coastal waters of Hawaii.140 Grigg stated that there
were no statistically significant impacts of sewage
outflow on coral species richness and cover,140 a
negative result that has been cited over 180 times
in the literature. Close examination of the methods
and results of Grigg,140 however, call into question
this inference and thus challenge the wisdom and
rigor of the widespread use of the conclusions of
this paper in the scientific literature. Specifically, for
the case of coral cover, no statistical results were
reported in the figures, tables, or text. In addition,
visual inspection of the differences in coral cover
at shallow depths (Fig. 1 in Ref. 140) next to out-
flow pipes versus coral cover in control sites suggests
the opposite effect—significantly less coral cover
around outflow pipes. These concerns, along with
the fact that there were no before–after data, sug-
gest that Grigg’s strongly wordedconclusions140 that
sewage does not impact coral reef ecosystems should
be reevaluated.
In summary, seven of eight of these obser-
vational field studies show positive correlations
between increasing sewage concentration on reefs
and increasing coral disease and degradation of
coral reef communities. The eighth study reports no
effect;however,wehaveconcernsabouttheanalysis
and interpretation of data provided. Future inves-
tigations should use both experimental manipu-
lations of sewage presence in the field and more
rigorously designed before–after–control–impact
studies148 to test for this putative causal relation-
ship. Furthermore, new studies should (1) employ
varying degrees of sewage exposure, in order to pro-
duce a functional relationship between increasing
sewage concentration and metrics of coral health
and reef community condition; and (2) measure
concentrations of as many sewage-associated toxins
as possible to help begin to decipher which toxin(s)
within sewage is most correlated with declines in
coral health.
Synergistic impacts of sewage
When organisms experience multiple stressors, syn-
ergistic impacts can occur.149 In particular, exposure
to multiple stressors has been cited as a key fac-
tor in habitat loss in marine ecosystems150,151 and
to decreasing growth rates in many marine species
(e.g., see Refs. 149 and 152).
This is an important point, because sewage dis-
charge is often mischaracterized as a single stressor
in coral reef management. This review challenges
that view and documents that sewage is a con-
glomerate of many potentially toxic and distinct
coral and coral reef stressors, including freshwa-
ter, inorganic nutrients, pathogens, endocrine dis-
rupters, suspended solids, sediments, heavy metals,
and other toxins. Given the high number of individ-
ual stressors found in sewage and that the negative
impacts of many of these pollutants are likely to
combine at least additively because of positive feed-
backs (see Fig. 1 and discussion below), we argue
that sewage should be viewed primarily as a multi-
ple, rather than a single stressor.
We propose a conceptual model to highlight
common direct and indirect negative impacts
that stressors found in sewage can have on corals
(Fig. 1). This model also highlights common
directional interactions that those stressors may
have with each other, and therefore additionally
points out opportunities for positive feedbacks,
8Ann. N.Y. Acad. Sci. xxxx (2015) 1–16 C2015 The Authors. Annals of the New York Academy of Sciences
published by Wiley Periodicals Inc. on behalf of The New York Academy of Sciences
Wear & Thurber Sewage pollution and coral reef stewardship
Figure 1. Interaction diamond illustrating impacts of sewage on concentrations of known stressors to corals and the positive
feedbacks those stressors can have.
additive effects, and subsequent multiple-stressor
effects. For example, sedimentation generated by
sewage can stress corals and deplete their energy
resources, resulting in increased susceptibility to
pathogens that are found in high concentrations in
sewage.107,153 Sediment-facilitated coral disease has
the potential to be fueled to an even greater degree
by increased nutrients54 derived from sewage.
The most important conclusion that can be taken
away from this model is that the pathways for
multiple-stressor effects generated by the multitude
of component pollutants within sewage are high
both in diversity and abundance, making sewage a
potentially lethal cocktail for coral reefs.
In addition to the synergistic effects that can
occur among the component stressors found within
sewage, there is also the strong possibility for syn-
ergistic interactions between sewage discharge and
the many non-sewage stressors that affect coral reefs
worldwide. For example, warming seas are hypoth-
esized to play a role in facilitating disease outbreaks
by increasing the susceptibility of coral to disease
through temperature stress and increasing the vir-
ulence of pathogens.80,154 Evidence to support this
hypothesis is present in recent work examining tem-
perature anomalies and disease outbreaks.86,155 Fur-
thermore, overfishing can lead to release of small
corallivores from predatory control, such that they
increase surface wounds on corals.156 Increased
wounding of corals is subsequently followed by
greater disease susceptibility in these foundation
species.136, 157–159 Sewage discharge, through intro-
duction of heavy metals and inorganic nutrients,
could also interact with ocean warming and acidi-
fication to decrease coral growth and reproduction
in an additive or synergistic way.87,160 These inter-
actions with sewage are likely to lead to greater
declines in coral cover and ultimately more dis-
ease, as stressed corals are more susceptible to
disease.87,160 We would expect sewage impacts to
be strongest in areas in close proximity to human
populations, especially in areas with low flushing.96
A common mechanism leading to synergies
between stressor impacts in both of these examples
9
Ann. N.Y. Acad. Sci. xxxx (2015) 1–16 C2015 The Authors. Annals of the New York Academy of Sciences
published by Wiley Periodicals Inc. on behalf of The New York Academy of Sciences
Sewage pollution and coral reef stewardship Wear & Thurber
Figure 2. Global map showing 104 of 112 distinct coral reef geographies listed in the World Atlas of Coral Reefs7(including 80
countries, 6 states, and 26 territories) with documented coastal sewage pollution problems.
is that non-sewage stressors increase susceptibility
to infection, while the addition of sewage renders
disease delivery more likely and disease progression
more rapid. The various effects that combined
anthropogenic stressors have on the complex
microbial community in the surface mucous layer
of corals have not been well explored. As we learn
more about the role this mucous layer plays in coral
health, we may learn that even small disturbances
have the potential to tip the balance in favor of more
harmful bacteria and viruses, ultimately leading
to serious outbreaks of coral disease. Given the
high potential for these synergistic interactions to
occurwhenstresslevelsarehigh,futurescientific
studies and conservation efforts focused on sewage
discharge should take their potential occurrence
into careful consideration.
How extensive is the sewage discharge
problem?
We conducted a literature review to determine how
many coral reef geographies had a documented
sewage pollution problem. Using the World Atlas of
Coral Reefs7list of coral reef geographies, we con-
ducted a Web of Science search with the following
terms: TOPIC: “coral reef*” and TOPIC: “sewage”
and TOPIC: “pollution” and TOPIC: “Location
Name” (e.g., “Bahamas”). We identified the major-
ity of our cases of sewage-impacted coral reef
geographies in this way, with the remainder iden-
tified through a Google search using the same key
words. In these cases, we typically found a local
government report, but a few were noted only in
newspaper articles. Our review revealed that, for
almost every coral reef geography, raw or partially
treated sewage is polluting the local environment.
Figure 2 illustrates the spatial extent of the sewage
contamination problem in the tropics, and clearly
shows that no region is immune to this problem.
Of the 112 coral reef geographies, including terri-
tories, states, and countries, 104 have documented
sewage contamination problems, with the majority
having documentation of direct ocean discharge.
Only three of those geographies are uninhabited,
and therefore have no potential for sewage contam-
ination. Although the amount of sewage discharged
into the environment is difficult to quantify with
accuracy, this survey reveals that the spatial extent
of the problem is global in that it occurs in almost all
coral reef geographies. However, the magnitude of
the problem in a particular place is not represented
in this assessment.
The ways by which sewage reaches waters bathing
coral reefs are diverse, including intentional sewage
contamination through direct-discharge outfall
pipes (e.g., Hollywood, Florida sewage outfall),161
and treatment systems that allow sewage overflows
or bypasses during rain events or system failures
(e.g., U.S. Virgin Islands Frederiksted sewage bypass
outfall).141 Unintended sewage contamination also
often occurs through faulty systems, attributable
to engineering design flaws, especially inadequate
capacity for flooding waters, a leaking infrastruc-
ture, shifts in soils and rock that surround the
sewerage system, or lack of maintenance.162 Even
when state-of-the-art sewage treatment plants are
installed, the governments of developing countries
10 Ann. N.Y. Acad. Sci. xxxx (2015) 1–16 C2015 The Authors. Annals of the New York Academy of Sciences
published by Wiley Periodicals Inc. on behalf of The New York Academy of Sciences
Wear & Thurber Sewage pollution and coral reef stewardship
often do not have the staff or long-term funding to
properly maintain the facility; thus, these facilities
often fall into disrepair, leaving the communities to
once again deal with a sewage problem.162,163
Along with the faulty sewer and sewage treat-
ment systems comes the issue of a widespread lack
of proper sanitation. There are 2.4 billion people
without access to sanitation, many in tropical, devel-
oping countries.163 This lack of proper sanitation is
linked to public health problems, including signifi-
cant illness and death rates associated with diarrheal
disease in developing countries.164,165 There are
many geographies where the ocean is used as a toi-
let in common practice (open defecation), with this
disposal method widely socially accepted.163 While
there is much progress being made on the Millen-
nium Development Goals,166 which are specifically
working to address the lack of access to sanitation,
there is still much work to be done to reduce over-
all sewage contamination in the environment. The
World Health Organization expects to fall short of its
sanitation goal in 2015 by half a billion people.163 As
human populations continue to grow and sea level
continues to rise, the problem of sewage contamina-
tion in the environment will persist in the absence
of truly significant interventions and likely grow as
a function of human population growth.
Research and conservation
recommendations
This review documents sewage discharge as a global
and intense threat to coral reefs. Remarkably, despite
the extent of this threat, both scientists and conser-
vationists have paid relatively less attention (e.g., in
comparison to overfishing) to understanding and
abating sewage impacts on coral reefs. This is sur-
prising because it is well documented that sewage
contains a range of contaminants that individu-
ally are known stressors of coral reef ecosystems.
Furthermore, the additive or synergistic impacts of
these multiple contaminants have the potential to
combine with one another and with other stres-
sors beyond sewage, such as warming waters, to
accelerate coral reef ecosystem declines. Mitigat-
ing this growing global threat will require future
research that focuses on (1) understanding toler-
ance thresholds that corals have to sewage expo-
sure, evaluating individual contaminants as well
as additive and synergistic combinations of con-
taminants; (2) quantifying the spatial extent and
magnitude of the sewage discharge problems; and,
most importantly, (3) testing both proactive and
reactive strategies that can be employed toreduce the
adverse impacts of the massive amounts of human
sewage that enter tropical coastal waters. Pursuing
only advanced treatment options for sewage sys-
tems is not an appropriate, viable solution to this
problem. In many cases, this approach is not even
feasible because of high costs. We must think cre-
atively to solve this problem, by forging partnerships
among human health organizations, sewage infras-
tructure and treatment experts, entrepreneurial
groups, and development and environmental con-
servation organizations. Sewage pollution is a global
threat that humans and coral reefs share. Combin-
ing forces across organizations in traditionally non-
interacting sectors (e.g., conservation and economic
development) is essential if we are to address the
strain of human sewage in our reef systems and
their associated human communities.
Acknowledgments
This work was funded in part from the following
sources: the Nature Conservancy’s NatureNet Fel-
lowship to S. Wear and a National Science Foun-
dation Grant (OCE-1130786) to R. Vega Thurber.
Special thanks go to P. Kareiva, R. Noble, C. Peter-
son, B. Silliman, and two anonymous reviewers for
critical reviews and improving the manuscript, and
C. Adams and T. Boucher for assistance in develop-
ing the sewage pollution map.
Conflicts of interest
The authors declare no conflicts of interest.
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