The Year in Ecology and Conservation Biology

Abstract

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.

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.¹ Along with the inherent biodiversity these habitats support, reefs built by corals also provide many valuable services for humans, including shoreline protection, livelihoods from ecotourism, fisheries production, and a living synthesis engine of biomedical and industrially 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 provide are under severe threat, with evidence of a general 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 activities^7–10 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 Recent work cataloging the status of reefs has estimated that we have functionally lost at least 25% of coral reefs globally, and one-third of all coral species are threatened with extinction.¹² Chief among threats identified in Reefs at Risk Revisited (RRR) are overfishing, pollution, coastal development, and climate change.⁸ For example, increasing temperature of surface waters from climate change has led to increased bleaching events and subsequent reef loss.¹³ Bleaching owing to elevated water temperatures is perhaps the most notable stress, with some reefs experiencing 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 additive and synergistic effects of long-term overfishing, chronic coastal pollution, and poorly regulated 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.⁸ For example, RRR emphasizes that more than 55% of the world’s reefs are under immediate threat from overfishing,⁸ which 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 certain key fish species, and global efforts to influence consumer choice by limiting the demand for ecologically important species. Notably, the threat to coral reefs from pollution and eutrophication, although potentially just as important as overfishing, as suggested by the assessments of RRR⁸ and Halpern et al.,²¹ has received much less attention from conservation organizations (S. Wear, personal observation). Reasons for this disparity may include the practical challenges of dealing with a large-scale diffuse threat, the diversity of pollutants involved, the high cost of water-treatment facilities, and bureaucracy. The solutions to reducing and understanding the exact impacts of coastal pollution, where it is likely to be strong, have been lacking because of the inherent difficulties of monitoring and evaluating nonpoint sources of pollution, along with jurisdictional issues such as agency and private land conflicts.

The largest component of coastally derived pollution is sewage.^22–25 Most coral reefs are located 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 components 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 nutrients could lead to increased growth of algae and coral diseases.^29,30 However, sewage in its raw form contains many more compounds than just inorganic 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, suspended solids, sediments, heavy metals, and other toxins.^25,31 Below, we describe each of these constituents in detail and briefly summarize what is known about negative impacts on coral reefs and the mechanism(s) underlying the impact (Table1). 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.

Table 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

Freshwater

The primary component of sewage is freshwater, a known stressor to corals. Although there are surprisingly few studies examining impacts of freshwater on coral health, classic laboratory studies conducted 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 studied 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 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 specific 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. A number of studies have examined the 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 generally 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 monospecific 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 macroalgae as they interact with corals and compete for space.^44,45 This increase in macroalgal competition, when combined with nutrient pollution, may further reinforce a coral-depauperate state by reducing the growth and survival of adult corals^46–48 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 and in the Florida Keys⁵¹ found a positive correlation between 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 positively 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 prevalence 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 pollution 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 μM) generally had negative effects on corals, but increased P (0.11–26 μM) 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 branching) 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 acting 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 relationship, 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 scleractinian corals.^62,63 For example, mucus-associated bacteria are believed to regulate the settlement and/or growth of opportunist microbes by occupying space or producing effective antibiotics.^64–66 Alterations in ambient conditions, 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 addition 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 microbiome 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 experienced the devastating consequences of coral diseases, 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 Australia’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 Acroporid species, Acroporid palmata and Acroporid cervicornis, 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 management responses, including the listing of both taxa under the Endangered Species Act.

Recent work has started to link certain environmental conditions,^30,54,85 as well as a changing climate, 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 During 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 demonstrably transmitted to a marine invertebrate, providing strong evidence for the linkage between sewage exposure and disease in the marine environment. While evidence showing that sewage is an important disease reservoir is limited to one type of disease 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 synthetic estrogens, polychlorinated biphenyls (PCBs), plasticizers, pharmaceuticals, parabens, phthalates, dioxins, petrochemicals, organochlorinated pesticides, microplastics, and detergents.^94–98 Endocrine disrupters are chemicals with the ability to disrupt the endocrine or hormone system in living organisms. They can act on multiple processes in animals, 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 sediments adjacent to coral reefs.^95,100,101

Both distance from the source of sewage and the physical characteristics of an area affect the concentrations 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 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, incorporate 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 accompany sewage discharge and are threats to coral health.^25,107–110 Sewage typically contains high concentrations 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 photosynthetic 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 suspended 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 Table1 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 originating from other sources, such as agricultural runoff and natural erosion flows.²⁴ Suspended solids may contain toxic compounds and high levels of nutrients, 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 biological oxygen demand in surrounding waters, as bacterial consumption of oxygen rises with increasing 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, copper, 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 respiration and nerve communication. Numerous studies 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 increasing success of certain microbes. For example, Fe²⁺, which is common in raw sewage, plays an important 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 limiting 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 further multiply and increase their success in attacking and infecting live corals.¹²⁸ Finally, increases in this essential bacterial micronutrient have been implicated in altering reef community structure and function 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, pesticides, 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 mortality, to bleaching, to reduced lipid concentrations (see Table1 for examples of responses).

Field evidence linking sewage exposure and coral reef health

The section above reviews the impacts that individual components of sewage have on coral reef health and suggests that sewage as a whole has the potential to have strong negative impacts. However, this prediction is based on studies that did not experimentally expose corals in the field to sewage. To evaluate the findings of field experiments and observational studies assessing the effects of sewage and its constituents 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 studies 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 observational 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 communities varied with decreased water quality (e.g., fecal coliform counts, turbidity, and inorganic nutrients) associated with sewage outflows. In seven of the eight studies, a negative impact of sewage on reefs was implicated, and, in one study, no effect was suggested. Below, I briefly review the findings of these studies. Caution should be taken in interpreting 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 different sites in St. Croix, U.S. Virgin Islands—a sewage-impacted site, and an ecologically and geologically similar site nearby with no known sewage exposure. 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 conducted 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 δ¹⁵N was a strong predictor of severity of this disease.¹⁴⁷

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 Thailand, 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 changes at multiple ecological levels of organization 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 examined the interactions between bleaching and sewage pollution in Curaçao 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 outflow 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, suggest that Grigg’s strongly worded conclusions¹⁴⁰ that sewage does not impact coral reef ecosystems should be reevaluated.

Figure 1.

Interaction diamond illustrating impacts of sewage on concentrations of known stressors to corals and the positive feedbacks those stressors can have.

In summary, seven of eight of these observational 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, we have concerns about the analysis and interpretation of data provided. Future investigations should use both experimental manipulations of sewage presence in the field and more rigorously designed before–after–control–impact studies¹⁴⁸ to test for this putative causal relationship. Furthermore, new studies should (1) employ varying degrees of sewage exposure, in order to produce 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, synergistic impacts can occur.¹⁴⁹ In particular, exposure to multiple stressors has been cited as a key factor in habitat loss in marine ecosystems^150,151 and to decreasing growth rates in many marine species (e.g., see Refs. ¹⁴⁹ and ¹⁵²).

This is an important point, because sewage discharge is often mischaracterized as a single stressor in coral reef management. This review challenges that view and documents that sewage is a conglomerate of many potentially toxic and distinct coral and coral reef stressors, including freshwater, inorganic nutrients, pathogens, endocrine disrupters, suspended solids, sediments, heavy metals, and other toxins. Given the high number of individual stressors found in sewage and that the negative impacts of many of these pollutants are likely to combine at least additively because of positive feedbacks (see Fig. 1 and discussion below), we argue that sewage should be viewed primarily as a multiple, 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, 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 synergistic interactions between sewage discharge and the many non-sewage stressors that affect coral reefs worldwide. For example, warming seas are hypothesized to play a role in facilitating disease outbreaks by increasing the susceptibility of coral to disease through temperature stress and increasing the virulence of pathogens.^80,154 Evidence to support this hypothesis is present in recent work examining temperature anomalies and disease outbreaks.^86,155 Furthermore, 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 introduction of heavy metals and inorganic nutrients, could also interact with ocean warming and acidification to decrease coral growth and reproduction in an additive or synergistic way.^87,160 These interactions with sewage are likely to lead to greater declines in coral cover and ultimately more disease, 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 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 occur when stress levels are high, future scientific 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 Reefs⁷ list of coral reef geographies, we conducted 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 majority of our cases of sewage-impacted coral reef geographies in this way, with the remainder identified 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 territories, 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 contamination. 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.

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.

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 infrastructure, 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 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 treatment systems comes the issue of a widespread lack of proper sanitation. There are 2.4 billion people without access to sanitation, many in tropical, developing countries.¹⁶³ This lack of proper sanitation is linked to public health problems, including significant illness and death rates associated with diarrheal disease in developing countries.^164,165 There are many geographies where the ocean is used as a toilet in common practice (open defecation), with this disposal method widely socially accepted.¹⁶³ While there is much progress being made on the Millennium 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 overall 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 contamination 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 conservationists have paid relatively less attention (e.g., in comparison to overfishing) to understanding and abating sewage impacts on coral reefs. This is surprising because it is well documented that sewage contains a range of contaminants that individually 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 stressors beyond sewage, such as warming waters, to accelerate coral reef ecosystem declines. Mitigating this growing global threat will require future research that focuses on (1) understanding tolerance thresholds that corals have to sewage exposure, evaluating individual contaminants as well as additive and synergistic combinations of contaminants; (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 to reduce the adverse impacts of the massive amounts of human sewage that enter tropical coastal waters. Pursuing only advanced treatment options for sewage systems 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 creatively to solve this problem, by forging partnerships among human health organizations, sewage infrastructure and treatment experts, entrepreneurial groups, and development and environmental conservation organizations. Sewage pollution is a global threat that humans and coral reefs share. Combining 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.

Conflicts of interest

The authors declare no conflicts of interest.