Oil Spill Incidents on Coral Reefs: Impacts and Remediation Technologies

Abstract

Despite the great ecological and economic importance of coral reefs, these ecosystems are especially sensitive to environmental changes and vulnerable to impacts from various anthropogenic activities, including contamination by oil spills. Oil spills occur worldwide, mostly in marine environments, and have been reported for decades. Furthermore, the main oil transport routes in the oceans are close to important coral reefs and many of the major oil spills in history have occurred near these areas. Because of the widespread use of petroleum products, offshore oil and gas production has significantly increased its potential since the 1990s, thus increasing the risk of accidents in marine environments and consequently on coral reefs. Despite the great risk of oil exploitation to coral reefs, there is still no efficient, sustainable, and large-scale applicable remediation strategy to protect or to clean up reefs impacted by oil spills. Current methodologies to remediate oil pollution in marine environments are based on the use of chemical dispersants; however, these can be more harmful to corals than oil itself. Meanwhile, the use of bioremediation strategy, through the manipulation of the coral microbiome, has been proposed as a possible alternative to mitigate the impacts of oil on coral reefs.

1. Introduction

Petroleum is a naturally occurring complex mixture composed predominantly of carbon and hydrogen compounds (hydrocarbons) that occur in liquid, gaseous, or solid form. Hydrocarbons form a large variety of complex molecular structures, which can vary in terms of physicochemical properties, toxicity, and biodegradability. Based on their molecular structure, the hydrocarbons can be classified into four main groups: alkanes, alkenes, cycloalkanes, and aromatics [1].

Alkanes, also known as paraffins or saturated aliphatics, are the simplest hydrocarbons and contain only single covalent bonds between carbon atoms. They comprise the largest fraction of most oils, their toxicity is usually low, and they are easily biodegraded, excepting those that can act as solvents, such as n-hexane and n-heptane. Alkenes, or olefins, are unsaturated hydrocarbon molecules that contain one or more double bonds between carbon atoms. They are usually in small amounts or absent in oil; however they are highly present in refining products such as gasoline. Cycloalkanes, or naphthenes, are the monocyclic saturated hydrocarbons and they represent the second largest fraction of most oils. Aromatics are cyclic unsaturated hydrocarbons, with one or more aromatic rings in their molecule. When they have more than one aromatic ring, they are called polycyclic aromatic hydrocarbons (PAHs). PAHs contamination is a major environmental concern due to their acute toxic potential, their resistance to biodegradation and their potential to bioaccumulate [1].

Crude oil, the liquid form of petroleum, constitutes the most important primary fossil fuel. It can be found in underground reservoirs, and its accessed and extracted by drilling, on land (onshore reservoirs), or at sea (offshore reservoirs). Once extracted it is refined to produce fuels such as gasoline, diesel, jet and heating fuel, lubricating oils, asphalts and also petrochemical intermediate feedstocks, which are used in the production of a wide range of solvents, plastics, and detergents, among other important products for our modern life. Thus, since the rapid global economic growth has increased the demand for all products mentioned above, oil production, processing, and transportation activities have also experienced an intensification in the last decades, bringing with them higher risk of oil spills, even considering the advance of oil spill prevention technologies.

In addition, with increasing risk of spills occurrence, concerns about the differentiation of oils in terms of composition, environmental behavior, and toxicity have arisen.

In a general manner, it is possible to say that once in the sea, oil begins to suffer a set of transformations, such as evaporation, aerosolization, photooxidation, mixing, emulsification, diffusion, partial water dissolution, spreading, transport, biodegradation, aggregation, adhesion, and sedimentation [2]. The magnitude of those phenomena depends on the physicochemical characteristics, composition, and the amount of oil spilled, as well as on atmospheric and oceanographic conditions, level of particulates and organic matter in suspension, availability of nutrients in the water, and mainly on the type of spill (superficial or subsea). Figure 1 summarizes most of those phenomena.

Figure 1.

Summary of phenomena that occur in oil spills and some potential affected marine organisms. Source: Modified from [2].

The impact of a complex mixture of hydrocarbons on marine organisms affected by a spill event can vary a lot, spatially, among species, and also with time. At the surface, for instance, seabirds, turtles, and marine mammals can be harmed by direct contact, inhalation, and aspiration of oil, instead in the water column, fishes can be impacted and at the seafloor, corals can be strongly damaged [2]. The time variable is also important, since some processes largely occur in the first days or weeks of spill (i.e., photooxidation, evaporation), while others start later and last longer, for months or years (i.e., emulsification, biodegradation). As pollutant composition varies with time and environmental compartments as result of natural processes, it is expected that bioavailability and toxicity also change dynamically. Thus, it is common to find large quantities of light hydrocarbons at the surface and in the water column at the beginning of the spill event ready for evaporation, photooxidation, and even biodegradation, and to find sinking aggregates or seabed deposits of enriched PAH due to incomplete photooxidation in the surface and/or biodegradation in the water column [2].

2. Oil spills in coral reefs

Accidents involving oil or its derivatives can happen during drilling activity, refining, transportation, distribution, or use. Because of the widespread use of petroleum products, oil spills are frequent [3] and have been reported for decades [4, 5, 6, 7].

Most oil spills occur in the ocean. The annual amount of oil spilled into the ocean is approximately 10³ tons [8]. Unfortunately, the main transport routes for oil in the oceans are close to important coral reefs (Figure 2) and many of the major oil spills in history have occurred close to coral reef areas [7].

Figure 2.

The figure shows coral reefs on the planet, oil routes in the oceans, and some of the major oil spills. Arrows represent common oil routes, small red circles represent coral reefs, and yellow stars represent oil spills.

Besides, due to the worldwide increase in oil and gas demand and the dwindling of onshore reserves, offshore oil, and gas production have significantly increased their potential since the 1990s [9]. This increased the risk of accidents in marine environments and, consequently, in coral reefs.

Until recent days, several incidents involving oil and its derivatives have occurred in coral reef regions, leading to a considerable loss of coral cover.

In April 1986, in Bahia Las Minas (Panamá), a crude oil incident spilled around 10 to 16 million liters of crude oil, causing lethal, and sublethal effects in the coral regions [10]. During the Gulf War, in January 1991, a large spill of 6.3 million barrels also caused irreversible damages to coral reefs in Kuwait and Saudi Arabia [11]. In the Caribbean Sea, a continuing petroleum contamination between 1923 and 1985 by a refinery in Aruba (Venezuela) also resulted in serious damage to corals. Currently, in this region, coral cover is very low, and younger corals are not found within 9 km of the refinery’s surroundings [12].

In April 2010, the biggest environmental disaster in the history of the United States, the explosion on the British Petroleum Deepwater Horizon platform, located in the Gulf of Mexico, caused the opening of the oil well, generating a leak of about 1 million liters per day. A study conducted on the impact of this spill on deep-sea corals concluded that the spilled oil devastated corals living about 7 km southwest of the well. The affected coral reef occupies an area equivalent to almost half a football field, being approximately 1.6 km deep [13]. Most of the Gulf floor is muddy, but the coral colonies that appear are vital oases for marine life in the cold ocean depths. There is still a great connection between animals that live on the surface and the life in the deep-sea, and problems in this ecosystem can cause damage to the entire marine environment for a long time.

The largest and richest coral reef on the planet, the Great Barrier Reef in Australia, has also been suffering from the leakage of oil and its derivatives. At the same time as the Gulf of Mexico disaster, in April 2010, the Chinese ship Shen Neng 1 ran aground near the barrier reef. The accident was responsible for a spill from 3 to 4 tons of oil, reaching about 3 km in length and 250 m in width, the largest ever recorded in the region. Some damaged areas have become completely devoid of marine life. It is estimated that this disaster will cause considerable damages to the coral reef in the long term, lasting for approximately 20 years [14].

In 2019, more than 5 x 10³ tons of crude oil leaked from the Greek oil tanker Bouboulina reached more than 3000 km of the Brazilian coast and more than 980 beaches. The oil reached important coral reefs, including two of the largest protected coral reef areas in the South Atlantic: Costa dos Corais Environmental Protection Area and the Abrolhos Marine National Park [15]. The Abrolhos Marine National Park contains the largest and richest coral reefs in the South Atlantic, with a high degree of endemism [16]. However, they are vulnerable to local and global impacts [17].

This oil spill was the most extensive and severe environmental disaster ever recorded in Brazilian history [15]. However, environmental monitoring studies are needed to assess the real impact of this oil spill on marine life in the affected coral reefs.

3. Effects of oil on coral reefs

Coral reefs are among the most biodiverse and productive ecosystems on Earth, with great ecological and economic importance. However, they are especially sensitive to environmental changes and vulnerable to impacts from various anthropogenic activities, including contamination by oil spills [18].

Direct contact with oil or its soluble fraction is extremely harmful to reefs, leading to the death of corals and, consequently, several other marine organisms. Stress caused by oil contamination on corals includes histological effects, such as tissue death; biochemical effects, such as changes in the zooxanthellae primary productivity and increase in mucus production; reproductive effects, such as larval premature expulsion and losses in larval settlement; development effects, such as changes in the calcification rates and muscle atrophy; and changes in the coral’s symbiotic microbiota (Table 1).

DAMAGE TO CORAL	References
Tissue death	[19, 20, 21, 22, 23]
Impaired feeding	[20, 22, 24]
Impaired polyp retraction	[21, 22, 25, 26]
Impaired debug or recovery ability	[27, 28]
Increased mucus production	[22, 29, 30, 31, 32]
Change in calcification rate	[21, 33, 34, 35]
Damage to the gonads	[29, 36]
Premature expulsion of larva	[37, 38]
Larval death	[36, 39, 40]
Impaired larval settlement	[36, 41, 42, 43, 44, 45]
Expulsion of zooxanthellae	[21, 29]
Change in primary production of zooxanthellae	[21, 23, 26, 46]
Increased expression of genes associated with oxidative, immune, and metabolic stress responses	[28, 47]
Muscle atrophy	[29]
Tissue and fragment loss	[48]
Bioaccumulation	[10, 49]
Change in the symbiotic microbiota	[23, 46]

Table 1.

Effects of oil pollution on corals.

A common feature of corals against petroleum contamination is their ability for biological accumulation. The hydrocarbons rapidly bioaccumulate in the tissues (probably due to the high concentration of lipids), where they undergo a slow degradation. This bioaccumulation can still expose the zooxanthellae to hydrocarbons. In areas with chronic contamination, the hydrocarbons remain for a long period in the deposited coral’s exoskeleton. It is important to note that corals have the ability to acquire hydrocarbons from the water column. It has already been observed that, in some cases, hydrocarbons may be absent in the sediment but present in the coral skeleton. On the other hand, bioaccumulation allows the use of coral skeletons as historical records of hydrocarbons contaminations.

The differences in tolerance by coral species are an important consideration, and species morphology seems to be directly linked to its susceptibility. For example, studies have found that branched corals appear to be among the most susceptible, while massive corals are more tolerant against oil exposure, probably due to higher oil adhesion and tissue damage in the former ones [50, 51]. In a field study of the incident that occurred in Bahia Las Minas (Panamá), it was observed that almost all branched corals were dead in the reef areas where the spill occurred [39].

In addition, studies have shown that chronic contaminations, even with low oil concentrations, can be more harmful to corals than shorter contaminations with higher oil concentrations. Exposure to chronic oil contamination can impair coral’s biological functions, such as reproduction and recruitment, which will considerably reduce the survival of the corals.

4. Remediation technologies

Despite the great risk of oil exploitation to coral reefs, there is still no efficient, sustainable and large-scale applicable remediation strategy to protect or to clean up reefs impacted by oil spills.

Three main groups of emergency response strategies have been used to minimize marine oil contamination: physical/mechanical methods, chemical methods, and biological methods.

The most widely used chemical method is the application of dispersants. Dispersant consists of a mixture of surfactants and solvents that act to break oil into small droplets that are dispersed into the water column, where they are subjected to natural processes – such as wind, waves, and currents – leading to the intensification of evaporation, dispersion, aggregation into marine oil snow, sedimentation and, also, biodegradation. An extensive discussion about environmental implications of dispersants use as oil spills response method can be found in [2].

Meanwhile, studies have shown that dispersants can be more harmful to corals than oil itself, not only because of its toxicity but also because of the consequent increase in hydrocarbon concentration throughout the water column [46, 47]. In fact, regardless of the type of oil (light, medium, or heavy crude oil), the NOAA Office of Response and Restoration cites, at least in shallow coral reef areas, the natural recovery as the lower impact alternative for oil spill response, due to the negative effect of dispersants in those organisms [52]. In this sense, the use of dispersants in emergency response plans is usually avoided in sensitive areas and even subjected to environmental trade-off analysis, usually done by Spill Impact Mitigation Assessment (SIMA) methodology (see [53]). Nevertheless, the application of dispersants is mandatory in some extreme cases (i.e., blowout), for oil spill control or explosivity risk reduction, even in sensitive areas. Among examples of disasters where dispersants were prioritized, those occurred in Bahia Las Minas in Panama, near the Great Barrier Reef in Australia and the explosion of the Deepwater Horizon platform in the Gulf of Mexico must be highlighted.

A methodology that has shown excellent results in oil degradation and in reducing coral mortality is microbial bioremediation in conjunction with the use of probiotic microorganisms for corals.

The microorganisms associated with corals (coral microbiome) include virus, dinoflagellates, archaea, bacteria, and fungi, which are essential for the host’s health [54, 55, 56]. These microorganisms provide multiple beneficial functions, such as production of photosynthate, supply of other micronutrients, protection against pathogens, nitrogen fixation, and UV-damage protection [57, 58, 59, 60, 61, 62, 63, 64].

The coral animal and its associated microorganisms are known as coral holobiont. This holobiont is a dynamic system, whose members can fluctuate depending on environmental conditions and daily requirements [65]. The microbiome interactions can drive holobiont biology and define its phenotype [66].

Bioremediation is a biological remediation method that uses living organisms, or their enzymes, to reduce or remove environmental contaminants, and it can be applied in a wide range of ecosystems. Microorganisms are directly involved in biogeochemical cycles as key drivers of the degradation of many carbon sources, including petroleum hydrocarbons. Several microorganisms, such as bacteria, cyanobacteria, green algae, and fungi, can degrade different components of petroleum under different environmental conditions [67]. The use of probiotic microorganisms for corals has recently been proposed as a promising method to improve coral health, potentially promoting coral resistance and resilience helping to protect and recover impacted reefs [23, 54, 68, 69, 70, 71]. The probiotic microorganisms can enhance coral fitness through their symbiotic relationships with the host [72, 73, 74, 75, 76].

In sensitive ecosystems such as coral reefs, bioremediation in conjunction with the probiotics for corals represents an efficient, sustainable, and low-cost alternative to chemical remediation of oil spills [23, 46].

Bioremediation can be carried out through bioaugmentation or biostimulation. The first one is the strategy in which pollutant degrading microorganisms, previously selected in laboratory are introduced into the contaminated environment. The use of microorganisms from the same environment in which they will be introduced is not mandatory; however, it is recommended. Biostimulation, on the other hand, is a bioremediation strategy that aims to stimulate the ability of native microorganisms to degrade pollutants, by identifying and adjusting certain physical and chemical parameters that may be undermining their biodegradation rate.

Studies based on bioaugmentation have shown that it is possible to manipulate the microbiome of coral species, making corals more resistant to environmental changes, and impacts. Some authors [23] showed that using probiotic and oil-degrading microorganisms to improve the health of corals under stress can protect corals from the effects of oil exposure. In this study, a consortium of 10 different bacterial species capable of degrading oil was isolated from corals of the Mussismilia harttii species. This bacterial consortium was able to degrade 72.75% of total petroleum hydrocarbons (TPH), and 56.20% of 38 polycyclic aromatic hydrocarbons (PAHs) in only 10 days of the experiment. Besides, the consortium was able to preserve the photochemical ability of zooxanthellae, protecting the corals against the negative effect of oil exposition.

Some authors [46] selected a multi-domain microbial consortium composed of bacteria, filamentous fungi, and yeast, which was able to mitigate oil impacts, substantially degrading oil components and improving coral health in the presence of oil. The microbial consortium was isolated from seawater and from corals of the species Millepora alcicornis and Siderastrea stellata. The coral species evaluated was M. alcicornis, a different species from that evaluated by other authors [23]. These studies showed that using probiotic and oil-degrading microorganisms to improve the health of corals under stress from oil exposure can foster coral survival. This bioremediation strategy can help companies and government agencies about the use of chemical or biological remediation since it has been shown that probiotic and oil-degrading microorganisms minimize the negative effects of oil without being toxic to coral.

In this context, some authors [54] proposed the term BMC (Beneficial Microorganisms for Corals) to refer to probiotic coral bacteria used to increase overall coral fitness through specific mechanisms, and suggested strategies for the use of this knowledge to manipulate the microbiome to restore and protect coral reefs. These strategies can be used not only to mitigate the stress and impacts of toxic compounds such as oil spills, but also to promote coral nutrition and growth, deter pathogens, and benefit early life-stage development.